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Textbook of Epilepsy Surgery
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Textbook of Epilepsy Surgery Edited by
Hans O Lüders
MD PhD
Epilepsy Center Neurological Institute University Hospitals of Cleveland Case Western Medical Center Cleveland, OH USA
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© 2008 Informa UK Ltd First published in the United Kingdom in 2008 by Informa Healthcare, Telephone House, 69-77 Paul Street, London EC2A 4LQ. Informa Healthcare is a trading division of Informa UK Ltd. Registered Office: 37/41 Mortimer Street, London W1T 3JH. Registered in England and Wales number 1072954. Tel: +44 (0)20 7017 5000 Fax: +44 (0)20 7017 6699 Website: www.informahealthcare.com All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording, or otherwise, without the prior permission of the publisher or in accordance with the provisions of the Copyright, Designs and Patents Act 1988 or under the terms of any licence permitting limited copying issued by the Copyright Licensing Agency, 90 Tottenham Court Road, London W1P 0LP. Although every effort has been made to ensure that all owners of copyright material have been acknowledged in this publication, we would be glad to acknowledge in subsequent reprints or editions any omissions brought to our attention. The Author has asserted his right under the Copyright, Designs and Patents Act 1988 to be identified as the Author of this work. A CIP record for this book is available from the British Library. Library of Congress Cataloging-in-Publication Data Data available on application ISBN-10: 1 84184 576 0 ISBN-13: 978 1 84184 576 0 Distributed in North and South America by Taylor & Francis 6000 Broken Sound Parkway, NW, (Suite 300) Boca Raton, FL 33487, USA Within Continental USA Tel: 1 (800) 272 7737; Fax: 1 (800) 374 3401 Outside Continental USA Tel: (561) 994 0555; Fax: (561) 361 6018 Email: [emailprotected] Book orders in the rest of the world Paul Abrahams Tel: +44 (0) 207 017 4036 Email: [emailprotected] Composition by Cepha Imaging Pvt. Ltd., Bangalore, India Printed and bound in India by Replika Press Pvt. Ltd. Cover illustration: © ‘An operation for stone in head’ used with kind permission from the Wellcome Trust, UK 2008.
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Dudley S Dinner MD April 17, 1947 – May 1, 2007 I dedicate this book to Dudley, my dear friend and colleague, whose contributions to epilepsy surgery will have a permanent impact on the specialty. Dudley joined the Cleveland Clinic Epilepsy Center as a fellow in clinical neurophysiology in 1979, shortly after I became the Director of the Center. This marked the beginning of a remarkable thirty years of extremely productive, daily collaboration. Throughout this period, Dudley participated in all major projects of the Center: contributing ideas, assisting in the organization of these projects, and managing their execution. Dudley’s absolute loyalty, reliability, intellectual honesty, complete dedication, exemplary modesty, and willingness to sacrifice to achieve our objectives were essential ingredients in the development of the Epilepsy Center at the Cleveland Clinic. Dudley, as an expression of his unselfishness, never demanded recognition for his contributions. Dudley was so often the driving force behind the scenes. I would like to use this opportunity to express my deepest appreciation for Dudley’s invaluable contributions, but also – and perhaps most importantly – to thank him for his friendship and unwavering support. I particularly notice his absence in my current efforts to organize an Epilepsy Center at University Hospitals. I realize now how much I relied on Dudley’s help in so many of our projects. I greatly miss him as a colleague and as a dear friend. It is a great honor to dedicate this book to Dudley.
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Contents List of Contributors
xvii
Preface
xxiv
Color plates
xxv
SECTION 1: HISTORY OF SURGERY AND RELATED FIELDS
1
1.
Epilepsy surgery in Europe before the 19th century D Schmidt and H-J Meencke
3
2.
Epilepsy surgery in Asia before the 19th century N-S Chu, T Hori, S-K Lee, Y Mayanagi, K Radhakrishnan, and H Shibasaki
12
3.
Epilepsy surgery in Latin America before the 19th century MG Campos
15
4a.
The history of epilepsy surgery in the United Kingdom CE Polkey
24
4b.
Epilepsy surgery in Ireland P Widdess-Walsh, N Delanty, and JP Phillips
32
5.
Epilepsy surgery in Germany A Ebner, H Stefan, B Pohlmann-Eden, and PA Winkler
37
6.
Epilepsy surgery in France P Kahane, A Arzimanoglou, A-L Benabid, and P Chauvel
46
7.
Epilepsy surgery in Italy G Avanzini and L Tassi
54
8a.
Epilepsy surgery in Switzerland HG Wieser and K Schindler
59
8b.
Epilepsy surgery in Austria C Baumgartner, T Czech, and O Schröttner
73
9.
Epilepsy surgery in the Nordic countries K Källén, H Høgenhaven, KO Nakken, and R Kalviäinen
77
10.
The development of epilepsy surgery in the Netherlands and Belgium W van Emde Boas and PAJM Boon
84
11.
History of epilepsy surgery in the Middle- and East-European countries and Russia P Halász
97
12.
Epilepsy surgery in Canada W Feindel
103
13.
A brief history of epilepsy surgery in the United States PJ Connolly, DD Spencer, and AA Cohen-Gadol
116
14.
Epilepsy surgery in Latin America J Godoy, AC Sakamoto, and ALF Palmini
118
15.
Epilepsy surgery in Africa MF Moodley and EL Khamlichi
125
16a.
History of epilepsy surgery in Southeast Asia S-H Lim
130
16b.
Epilepsy surgery in India DK Lachhwani and K Radhakrishnan
134
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17.
Treatment of epilepsy in Australia A Mohamed
145
18.
Epilepsy surgery in Korea BI Lee
148
19.
Epilepsy surgery in Thailand T Srikijvilaikul, C Locharernkul, and A Boongird
152
20.
History of epilepsy and seizure classification T Loddenkemper and HO Lüders
160
21.
History of electroencephalography as a presurgical evaluation tool: the pre-Berger years WT Blume
174
22.
History of neuroimaging in the presurgical evaluation B Diehl and P Ruggieri
177
23.
Epilepsy surgery in literature and film P Wolf and S Baxendale
189
24.
The future of epilepsy surgery F Andermann and W Harkness
197
SECTION 2: OVERVIEW
201
25.
Medical intractability in epilepsy DV Lardizabal
203
26.
Epidemiology of the intractable generalized epilepsies AT Berg
207
27.
Genetic factors contributing to medically intractable epilepsy JF Bautista
215
28.
Informed consent FL Vale and S Benbadis
220
29.
Epilepsy surgery: access, costs, and quality of life MG Campos and S Wiebe
223
30.
Epilepsy surgery: patient selection H Morris, I Najm, and P Kahane
230
31.
Exclusion criteria EMT Yacubian
238
SECTION 3: EPILEPSIES REMEDIABLE BY EPILEPSY SURGERY
243
32.
Classification of epileptic seizures and epilepsies HO Lüders
245
33.
Mesial temporal sclerosis HO Lüders
249
34.
Neocortical temporal lobe epilepsy A Ebner
252
35.
Premotor and central lobe epilepsy S Bauer, HM Hamer, and F Rosenow
263
36.
Mesial frontal epilepsy A Bleasel and D Dinner
274
37.
Basal frontal lobe epilepsy AV Alexopoulos and N Tandon
285
38.
Parieto-occipital lobe epilepsy V Salanova
314
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39.
Insular epilepsy J Isnard, P Ryvlin, and F Mauguière
320
40.
Cingulate epilepsy E Garzon and HO Lüders
334
41.
Hypothalamic hamartomas AS Harvey
354
42.
Rasmussen syndrome CG Bien
362
43.
The Landau–Kleffner syndrome AM Kanner, A Balabanov, TP Hoeppner, and R Byrne
369
44.
The Lennox–Gastaut syndrome: a surgically remediable epilepsy? C Dravet
384
45.
Medically intractable epilepsies not remediable by surgery NK So
394
46.
Special characteristics of surgically remediable epilepsies in infants A Gupta
400
SECTION 4: PRE-SURGICAL EVALUATION: GENERAL PRINCIPLES
407
47.
409
General principles of pre-surgical evaluation M Carreño and HO Lüders
SECTION 5: THE SYMPTOMATOGENIC ZONE
423
48.
The symptomatogenic zone – general principles C Kellinghaus and HO Lüders
425
49.
Auras: localizing and lateralizing value S Rona
432
50.
Autonomic seizures: localizing and lateralizing value V Nagaraddi and HO Lüders
443
51.
Simple motor seizures: localizing and lateralizing value S Noachtar and S Arnold
450
52.
Complex motor seizures: localizing and lateralizing value MM Bianchin and AC Sakamoto
462
53.
Dialeptic seizures: localizing and lateralizing value S Noachtar
479
54a.
Special seizures: localizing and lateralizing value SR Benbadis
488
54b.
Secondary generalized tonic-clonic seizures SD Lhatoo and HO Lüders
492
SECTION 6: THE IRRITATIVE ZONE
501
55.
The irritative zone: general principles M Eccher and D Nair
503
56.
Noninvasive electroencephalography evaluation of the irritative zone HM Hamer
512
57.
The irritative zone evaluated with invasive recordings A Palmini
521
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The significance of interictal fast ripples in the evaluation of the epileptogenic zone A Bragin, RJ Staba, and J Engel Jr
530
59.
Magnetoencephalography in the evaluation of the irritative zone M Iwasaki and RC Burgess
537
60.
Magnetic resonance imaging in the evaluation of the irritative zone K Krakow, B Diehl, and JS Duncan
544
61.
Digital tools for reviewing the electroencephalogram: montage reformatting and filtering TD Lagerlund
550
62.
Average reference and Laplacian montages TD Lagerlund
558
63.
Automatic detection of epileptic spikes P LeVan and J Gotman
565
64.
Source localization of electroencephalography spikes TN Townsend and JS Ebersole
570
65.
Antiepileptic drug withdrawal in presurgical evaluation: advantages, disadvantages, and guidelines SP Claus, DN Velis, and W van Emde Boas
580
66.
Effects of sleep and sleep deprivation on seizures and the electroencephalography in epilepsy N Foldvary-Schaefer
588
SECTION 7: THE ICTAL ONSET ZONE
595
67.
The ictal onset zone: general principles, pitfalls, and caveats A Arzimanoglou and P Kahane
597
68.
Noninvasive electroencephalography in the evaluation of the ictal onset zone N Foldvary-Schaefer
603
69.
Indications for invasive electroencephalography evaluations SR Sinha, NE Crone, and RP Lesser
614
70.
Invasive electrodes in long-term monitoring GH Klem and S Nehamkin
623
71.
Foramen ovale and epidural electrodes in the definition of the seizure onset zone HG Wieser and K Schindler
629
72.
Subdural electrodes MZ Koubeissi
641
73.
Stereoelectroencephalography P Kahane and S Francione
649
74.
DC recordings to localize the ictal onset zone A Ikeda
659
75.
fMRI in the evaluation of the ictal onset zone K Hamandi and JS Duncan
667
76.
Ictal SPECT in the definition of the seizure onset zone GD Cascino and D Lachhwani
675
77.
Automatic detection of epileptic seizures FT Sun, TK Tcheng, EH Boto, BM Wingeier, TL Skarpaas, and MJ Morrell
681
78.
‘Preictal’ predictors of epileptic seizures F Mormann, K Lehnertz, and CE Elger
691
79.
Effect of anticonvulsant withdrawal on seizure semiology and ictal electroencephalography CT Skidmore and MR Sperling
702
80.
Zone of electrical stimulation induced seizures in subdural electrodes R Schulz
706
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SECTION 8: THE EPILEPTIC LESION
709
81.
The epileptogenic lesion: general principles HM Hamer and S Knake
711
82.
Magnetic resonance imaging in epilepsy: mesial temporal sclerosis GD Cascino
716
83.
Magnetic resonance imaging in neurocutaneous syndromes D Moon and A Gupta
721
84.
Magnetic resonance imaging in epileptogenic neoplasms J Tamraz and Y Comair
730
85.
Magnetic resonance spectroscopy in patients with epilepsy MA McLean, M Koepp, and FG Woermann
755
86a.
Post-processing of the magnetic resonance imaging to better define structural abnormalities S Knake, F Rosenow, and PE Grant
764
86b.
Multimodal image processing in pre-surgical planning C Vollmar, S Noachtar, and PA Winkler
771
SECTION 9: THE FUNCTIONAL DEFICIT ZONE
779
87.
The functional deficit zone: general principles C Baumgartner and E Lehner-Baumgartner
781
88.
Mesial temporal lobe epilepsy and positron emission tomography A Mohamed and MJ Fulham
792
89.
PET in neocortical epilepsies HT Chugani, C Juhász, E Asano, and S Sood
803
90.
Pre-surgical neuropsychological workup: risk factors for post-surgical deficits RM Busch and RI Naugle
817
91.
Pre-surgical psychiatric evaluations: risk factors for post-surgical deficits AM Kanner and AJ Balabanov
826
92.
Pre-surgical neuropsychological workup in children and intellectually disabled adults with epilepsy U Gleissner and C Helmstaedter
834
93.
Wada test and epileptogenic zone DS Dinner and T Loddenkemper
844
94.
Event-related potentials in patients with epilepsy K Usui and A Ikeda
858
SECTION 10: PRE-SURGICAL EVALUATION OF ELOQUENT CORTEX
869
95.
Eloquent cortex and tracts: overview and noninvasive evaluation methods J Reis and F Rosenow
871
96.
Noninvasive tests to define lateralization or localization of the motor area R Matsumoto and H Shibasaki
881
97.
Noninvasive tests to define lateralization or localization of memory EB Geller and C Santschi
889
SECTION 11: THE EPILEPTOGENIC ZONE
897
98.
The epileptogenic zone: general principles KM Klein and F Rosenow
899
99.
Future methods for the direct assessment of the epileptogenic zone J Engel Jr
902
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SECTION 12: THE PATIENT MANAGEMENT MEETING
909
100.
911
The patient management conference M Carreño and HO Lüders
SECTION 13: SURGICAL TECHNIQUES FOR PLACEMENT OF INTRACRANIAL ELECTRODES
921
101.
Anesthesia for epilepsy surgery M Lotto and A Schubert
923
102.
Placement of subdural grids F Salazar and WE Bingaman
931
103.
Placement of depth electrodes L Mulligan, K Vives, and D Spencer
938
104.
Stereoelectroencephalography D Hoffmann, GL Russo, and M Cossu
945
SECTION 14: CORTICAL MAPPING AND ELECTROCORTICOGRAPHY
961
105.
General principles of cortical mapping by electrical stimulation SU Schüle, C McIntyre, and HO Lüders
963
106.
Cortical mapping by electrical stimulation of subdural electrodes: primary somatosensory and motor areas AS Tanner and HO Lüders
107.
Cortical mapping by electric stimulation of subdural electrodes: negative motor areas P Smyth
108.
Cortical mapping by electrical stimulation of subdural electrodes: supplementary sensorimotor area in humans DS Dinner and HO Lüders
978 983
991
109.
Cortical mapping by electrical stimulation of subdural electrodes: language areas N Tandon
1001
110.
Cortical mapping by electrical stimulation: other eloquent areas M Hoppe
1016
111.
The role of electroencephalogram and magnetoencephalography synchrony in defining eloquent cortex G Kalamangalam and M Iwasaki
1026
112.
Cortical mapping using evoked potentials and Bereitschaftspotentials A Ikeda and H Shibasaki
1036
113a. Cortico-cortical evoked potentials to define eloquent cortex R Matsumoto and DR Nair
1049
113b. Cortical mapping by intra-operative optical imaging MM Haglund and DW Hochman
1060
114.
Functional localization of the cortex with depth electrodes J-P Vignal and P Chauvel
1068
115.
Intraoperative cortical mapping and intraoperative electrocorticography DR Nair and I Najm
1073
SECTION 15: RESECTIVE SURGICAL PROCEDURES FOR EPILEPSY
1081
116.
Resective surgical techniques: mesial temporal lobe epilepsy DK Binder and J Schramm
1083
117.
Resective neocortical techniques in adults EO Richter and SN Roper
1093
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118.
Epilepsy and vascular malformations: spectrum of lesions and strategies for management P Jabbour and I Awad
1098
119.
Resective neocortical techniques in children F Villarejo
1110
120.
Hemispherectomy techniques SJ Nagel, SK Elbabaa, EJ Hadar, and WE Bingaman
1121
SECTION 16: NONRESECTIVE SURGICAL PROCEDURES AND ELECTRICAL OR MAGNETIC STIMULATION FOR EPILEPSY TREATMENT
1131
121.
1133
Experimental multiple subpial transection: is it still indicated? T Tanaka, A Hodozuka, K Hashizume, M Kunimoto, and S Takebayashi
122a. Multiple subpial transections W Harkness 122b. Nonresective surgical procedures and electrical or magnetic stimulation for epilepsy treatment mutiple hippocampal transection H Shmizu 122c. Surgical disconnections of the epileptic zone as an alternative to lobectomy in pharmacoresistent epilepsy AL Benabid, S Chabardès, E Seigneuret, D Hoffmann, L Minotti, P Kahane, S Grand, and JF LeBas
1138
1149
1155
123.
Corpus callosotomy G Morrison and M Duchowny
1163
124.
Radiosurgical treatment of epilepsy I Yang and NM Barbaro
1173
125.
Vagal nerve stimulation: experimental data S Chabardès, I Najm, and HO Lüders
1179
126.
Vagal nerve stimulation: surgical technique and complications WE Bingaman
1184
127.
Vagus nerve stimulation: human studies T Loddenkemper and AV Alexopoulos
1188
128.
Experimental evidence for the involvement of the basal ganglia in the control of epilepsy C Deransart and A Depaulis
1201
129.
Repetitive transcranial magnetic stimulation F Tergau and BJ Steinhoff
1208
SECTION 17: SURGICAL OUTCOME
1221
130.
Mesial temporal lobectomy: post-surgical seizure frequency L Jehi
1223
131.
Resective surgery in children T Loddenkemper and E Wyllie
1236
132.
Hemispherectomy: post-surgical seizure frequency I Tuxhorn, H Holthausen, P Kotagal, and H Pannek
1249
133a. Psychiatric outcome of epilepsy surgery AM Kanner and AJ Balabanov
1254
133b. Sudden unexpected death in epileptic patients after epilepsy surgery D Schmidt and P Ryvlin
1263
134.
1269
Psychosocial outcome and quality of life outcome NK So and CB Dodrill
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135.
Neuropsychological outcome WB Barr
1277
136.
Temporal lobe epilepsy surgery: surgical complications D Sasaki-Adams and EJ Hadar
1288
137.
Neocortical focal epilepsy surgery: surgical complications JA González-Martínez and WE Bingaman
1300
SECTION 18: POST-SURGICAL MANAGEMENT
1307
138.
Early post-surgical management of patients with epilepsy I Melamed and AA Cohen-Gadol
1309
139.
Post-surgical pharmacotherapy: discontinuation of anticonvulsants AS Tanner and D Schmidt
1313
140.
Post-surgical rehabilitation R Thorbecke and B Hötger
1319
SECTION 19: NEUROPATHOLOGY AND RESEARCH RELATED TO EPILEPSY SURGERY
1329
141.
Neuropathology of mesial temporal sclerosis I Blümcke
1331
142.
Pathology of neocortical epilepsy M Thom and S Sisodiya
1338
143.
Pathology of malformations of cortical development R Spreafico and AJ Becker
1349
144.
Pathology of neurocutaneous abnormalities, vascular abnormalities: post-infectious and post-traumatic pathologies associated with epilepsy I Blümcke and M Hildebrandt
1359
145.
Pathology of epileptogenic neoplasms RA Prayson
1373
146.
In vitro neurophysiological studies GL Möddel and IM Najm
1384
147.
In vitro cytochemical studies in epilepsy JA González-Martínez, CQ Tilelli, and IM Najm
1397
148.
Animal models of epilepsy with special reference to models relevant for transitional research S Chabardès, I Najm, and HO Lüders
1405
SECTION 20: SURGICAL FAILURES: REOPERATION
1415
149.
Surgical failures: pre-surgical evaluation CT Skidmore and MR Sperling
1417
150.
Reoperation after failed epilepsy surgery A Boongird, JA González-Martínez, and WE Bingaman
1425
SECTION 21: CASE PRESENTATIONS
1433
151.
Lesional mesial temporal epilepsy: case discussions J Mani and IM Najm
1435
152.
A patient with nonlesional mesial temporal lobe epilepsy A Ray, G Kalamangalam, and HO Lüders
1446
153.
Patient with bitemporal lobe epilepsy AV Alexopoulos and HO Lüders
1456
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154.
Patient with lesional neocortical focal epilepsy B Abou-Khalil
1471
155.
Patient with nonlesional neocortical epilepsy L Tassi and GL Russo
1476
156.
Patient with extensive malformation of cortical development DK Lachhwani
1485
157.
Hemispherectomy in a patient with catastrophic epilepsy A Gupta
1491
158.
Case studies: Landau–Kleffner syndrome AM Kanner, MA Rossi, and MC Smith
1496
159.
Deep brain stimulation in a patient with medically intractable generalized seizures M Hodaie, C Hamani, D Zumsteg, DM Andrade, R Wennberg, and AM Lozano
1506
160.
Successful transcranial magnetic stimulation in a patient with medically intractable focal epilepsy F Fregni, G Thut, A Rotenberg, and A Pascual-Leone
1511
161.
Surgery in a patient with medically intractable gelastic seizures and a hypothalamic hamartoma S Mittal, JL Montes, J-P Farmer, and JD Atkinson
1518
162.
Surgery in a patient with focal epilepsy and dual pathology N Foldvary-Schaefer
1523
SECTION 22: APPENDICES
1535
163.
Essentials for the establishment of an epilepsy surgery program MG Campos, HB Pomata, MA Vanegas, and AC Sakamoto
1537
164.
Classification of seizure outcome following epilepsy surgery HG Wieser and K Schindler
1545
165.
Protocol for storage and processing of brain tissue for molecular studies PB Crino
1552
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Contributors B Abou-Khalil
MD
AV Alexopoulos
Department of Neurology, Vanderbilt University Medical Center, Nashville, TX, USA.
MD MPH
Department of Neurology, Section of Adult Epilepsy, The Cleveland Clinic Foundation, Cleveland, OH, USA.
F Andermann MD Montréal Neurological Hospital and Institute, McGill University; and the Hospital for Sick Children, Montréal, Quebec, Canada. DM Andrade MD Krembil Neuroscience Centre, Toronto Western Hospital; and Division of Neurology, Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada. S Arnold
Epilepsy Center, Department of Neurology, University of Munich, Munich, Germany.
MD
A Arzimanoglou MD Child Neurology and Metabolic Disorders, University Hospital Robert Debré (AP-HP), Paris; CTRS-IDEE, Hospices Civils de Lyon, Lyon, France. E Asano
G Avanzini I Awad
Departments of Pediatrics and Neurology, Children’s Hospital of Michigan, Wayne State University, Detroit, MI, USA.
MD PhD
Department of Neurophysiology, National Neurological Institute “Carlo Besta,” Milan, Italy.
MD
MD MSc FACS FICS FAHA
Department of Neurological Surgery, Northwestern University; Feinberg School of Medicine, Chicago, IL, USA.
JD Atkinson MD Division of Pediatric Neurosurgery, Montréal Children’s Hospital; McGill University Health Centre, Montréal, Quebec, Canada. AJ Balabanov
Department of Neurological Sciences, Rush Medical College, Rush University Medical Center, Chicago, IL, USA.
MD
NM Barbaro
MD
WB Barr
Departments of Neurology and Psychiatry, New York University Medical Center, New York, NY, USA.
S Bauer
PhD
Department of Neurology, Philipps University, Marburg, Germany.
MD
C Baumgartner JF Bautista
MD
S Baxendale AJ Becker
Department of Neurological Surgery, University of California, San Francisco, CA, USA.
MD
Department of Neurology, The Cleveland Clinic Foundation, Cleveland, OH, USA.
PhD
MD
Department of Neurology, Medical University of Vienna, Vienna, Austria.
Department of Neuropsychology, National Hospital for Neurology and Neurosurgery, London, UK.
Department of Neuropathology, University of Bonn Medical Center, Bonn, Germany.
A-L Benabid
MD PhD
SR Benbadis
MD
AT Berg
Department of Biology, Northern Illinois University, DeKalb, IL, USA.
PhD
MM Bianchin C Bien
MD PhD
MD PhD
WE Bingaman A Bleasel
Departments of Neurology and Neurosurgery, University of South Florida; and Tampa General Hospital, Tampa, FL, USA.
Department of Neurological Surgery, University of California, Irvine, CA, USA. Department of Neurosurgery, The Cleveland Clinic Foundation, Cleveland, OH, USA.
MD
MBBS FRACP
I Blümcke
Department of Neurology, Psychiatry and Psychology, University of São Paulo School of Medicine, São Paulo, Brazil.
Department of Epileptology, University of Bonn, Bonn, Germany.
MD
D Binder
Department of Clinical Neurosciences, Grenoble University Hospital, Joseph Fourier University, Grenoble, France.
MD
WT Blume
Department of Neurophysiology, The Children’s Hospital at Westmead, Westmead, New South Wales, Australia.
Department of Neuropathology, University of Erlangen, Erlangen, Germany.
MD FRCPC
W van Emde Boas
London Health Sciences Centre, University Campus, London, UK.
MD PhD
Departments of EEG and EMU, Epilepsy Institutions of the Netherlands, Heemstede and Zwolle, The Netherlands.
P Boon MD PhD Department of Neurology and Laboratory for Clinical and Experimental Neurophysiology, Ghent University Hospital, Ghent, Belgium. A Boongird
MD
Neurosurgery Unit, Department of Surgery, Bangkok, Thailand.
EH Boto
PhD
Clinical Scientist, Neuropace Inc, Mountain View, CA, USA.
A Bragin
PhD
Department of Neurology, David Geffen School of Medicine, University of California, Los Angeles, CA, USA.
RC Burgess RM Busch
MD PhD
MD PhD
MG Campos M Carreño
MD
Department of Neurology, The Cleveland Clinic Foundation, Cleveland, OH, USA.
Departments of Psychiatry and Psychology, The Cleveland Clinic Foundation, Cleveland, OH, USA.
Department of Neurosurgery, Pontifical Catholic University of Chile, Santiago de Chile, Chile.
MD PhD
Epilepsy Unit, Department of Neurology, Hospital Clínic de Barcelona, Barcelona, Spain.
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List of Contributors
GD Cascino
MD FAAN
S Chabardès
MD
Department of Neurology, Mayo Clinic, Rochester, MN, USA.
Department of Clinical Neurosciences, Grenoble University Hospital, Joseph Fourier University, Grenoble, France.
P Chauvel Laboratory of Clinical Neurophysiology and INSERM EMI La timone University Hospital, Marseille, France. PJ Connolly MD Head injury and Neurocritical Care Program, Indianapolis Neurosurgical Group, Clarian Neuroscience, Indianapolis, IN, USA. N-S Chu
Chang Gung Medical College and Memorial Hospital, Taiwan, Republic of China.
MD PhD
HT Chugani
Departments of Pediatrics, Neurology, and Radiology, Children’s Hospital of Michigan, Wayne State University, Detroit, MI, USA.
PhD
SP Claus Department of Child Neurology, Wilhelmina Children’s Hospital, University Medical Center of Utrecht, The Netherlands. AA Cohen-Gadol MD MSc Skull Base/Cerebrovascular and Epilepsy Surgery Programs, Indianapolis Neurosurgical Group, Clarian Neuroscience Institute (Methodist, Indiana University, and Riley Hospitals), Indianapolis, IN, USA. Y Comair
MD FRCSE
M Cossu
MD
PB Crino
MD PhD
NE Crone
Institute of Neurosurgery, University of Genoa, San Martino Hospital, Genoa, Italy.
MD
PhD MRCP(UK), FRCPCH
Department of Neurology, Beaumont Hospital, Dublin, Ireland.
PhD
A Depaulis
Department of Paediatric Neurology, Institute of Child Health and Great Ormond Street Hospital NHS Trust,
Department of Neurosurgery, Medical University of Vienna, Vienna, Austria.
MD
N Delanty
Department of Neurology, The Mahoney Institute of Neurological Sciences, University of Pennsylania, Philadelphia, PA, USA.
Department of Neurology, Johns Hopkins University, Baltimore, MD, USA.
H Cross MBChB London, UK. T Czech
Department of Surgery, Division of Neurosurgery, American University of Beirut, Beirut, Lebanon.
Grenoble Institute of Neurosciences, Joseph Fourier University, Grenoble, France.
PhD
C Deransart Grenoble Institute of Neurosciences, Joseph Fourier University, Grenoble, France. B Diehl
Department of Neurology, The Cleveland Clinic Foundation, Cleveland, OH, USA.
MD
†DS Dinner
MD
Department of Neurology, The Cleveland Clinic Foundation, Cleveland OH, USA.
C Dodrill Department of Neurology, University of Washington School of Medicine; Regional Epilepsy Center, Harborview Medical Center, Seattle, WA, USA. C Dravet Centre Saint-Paul – Hôpital Henri Gastaut, Marseille, France. MS Duchowny USA.
MD
Department of Neurology, Miami School of Medicine; Comprehensive Epilepsy Program, Miami Children’s Hospital, Miami, FL,
JS Duncan
MD
Department of Clinical and Experimental Epilepsy, Institute of Neurology, University College London, London, UK.
JS Ebersole
MD
Department of Neurology, Adult Epilepsy Center, University of Chicago Medical Center, Chicago, IL, USA.
A Ebner
Epilepsy Centre Bethel, Bielefeld, Germany.
MD
M Eccher
MD
SK Elbabaa CE Elger
Department of Neurology, University of Pennsylvania Medical Center, Philadelphia, PA, USA. Division of Neurological Surgery, University of North Carolina, Chapel Hill, NC, USA.
MD
MD PhD FRCP
Department of Epileptology, University of Bonn, Bonn, Germany.
J Engel Jr MD Departments of Neurology and Neurobiology, and Brain Research Institute, David Geffen School of Medicine, University of California, Los Angeles, CA, USA. J-P Farmer Canada. W Feindel
MD CM FRCS(C)
Division of Pediatric Neurosurgery, Montréal Children’s Hospital, McGill University Health Centre, Montréal, Quebec,
MD CM DPhil FRCSC FACS
N Foldvary-Schaefer S Francione
MD
DO
Montréal Neurological Institute, McGill University, Montréal, Quebec, Canada.
Sleep Disorders Center, The Cleveland Clinic Foundation, Cleveland, OH, USA.
Epilepsy Surgery Centre, Niguarda Hospital, Milano, Italy.
F Fregni MD PhD Center for Non-invasive Brain Stimulation, Harvard Medical School; Department of Neurology, Beth Israel Deaconess Medical Center and Boston Children’s Hospital, Boston, MA, USA. MJ Fulham
MD
PET Centre, Royal Prince Alfred Hospital, Campendown, New South Wales, Australia.
E Garzon
MD PhD
EB Geller
MD
Department of Neurology, Ribeirão Preto School of Medicine, University of São Paulo, São Paulo, Brazil.
The Institute of Neurology and Neurosurgery at Saint Barnabas, West Orange, NJ, USA.
U Gleissner
PhD
J Godoy
Department of Neurology, Pontifical Catholic University of Chile, Santiago de Chile, Chile.
MD
Department of Epileptology, University of Bonn, Bonn, Germany.
JA González-Martínez
MD PhD
Department of Neurological Surgery, The Cleveland Clinic Foundation, Cleveland OH, USA.
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List of Contributors J Gotman S Grand
xix
Montréal Neurological Institute, McGill University, Montréal, Quebec, Canada.
PhD
Department of Clinical Neurosciences, Grenoble University Hospital, Joseph Fourier University, Grenoble, France.
MD PhD
PE Grant
MD
Department of Radiology, Harvard Medical School, Massachusetts General Hospital, Cambridge, MA, USA.
A Gupta
MD
Department of Neurology, The Cleveland Clinic Foundation, Cleveland, OH, USA.
MM Haglund
MD PhD
P Halász
MD PhD DSc
EJ Hadar
MD
Division of Neurosurgery, Department of Surgery, Duke University Medical Center, Durham, NC, USA.
National Institute of Psychiatry and Neurology, Budapest, Hungary.
Division of Neurosurgery, University of North Carolina, Chapel Hill, NC, USA.
C Hamani Krembil Neuroscience Centre, Toronto Western Hospital; and Division of Neurosurgery, University of Toronto, Toronto, Ontario, Canada. K Hamandi Department of Clinical and Experimental Epilepsy, Institute of Neurology, University College London, London, UK. HM Hamer
MD
K Hashizume
Department of Neurology, University of Marburg, Marburg, Germany. Department of Neurosurgery, Asahikawa Medical College, Asahikawa, Japan.
MD
W Harkness MD Montréal Neurological Hospital and Institute, McGill University, Montréal, Quebec, Canada; Great Ormond Street Hospital for Children, London, UK S Harvey
MD FRACP
C Helmstaedter
Children’s Epilepsy Program, Department of Neurology, Royal Children’s Hospital, Melbourne, Victoria, Australia.
MD PhD
Department of Neurophysiology, University Clinic of Epileptology, Bonn, Germany.
M Hildebrandt
MD
Department of Neuropathology, University of Erlangen, Erlangen, Germany.
DW Hochman
PhD
Department of Surgery, Duke University Medical Center, Durham, NC, USA.
M Hodaie MD MSc Ontario, Canada.
FRCS
Krembil Neuroscience Centre, Toronto Western Hospital; Division of Neurosurgery, University of Toronto, Toronto,
A Hodozuka
MD
Department of Neurosurgery, Asahikawa Medical College, Asahikawa, Japan.
D Hoffmann
MD
Department of Clinical Neurosciences, Grenoble University Hospital, Grenoble, France.
H Holthausen
MD
Neuropediatric Department, Behandlungszentrum Vogtareuth, Germany.
M Hoppe
MD
T Hor
Department of Neurosurgery, Tokyo Women’s Medical University, Tokyo, Japan.
MD
B Hötger
Department of Presurgical Evaluation, Bethel Epilepsy Centre, Bielefeld, Germany.
Department of Presurgical Evaluation, Bethel Epilepsy Center, Bielefeld, Germany.
MD
A Ikeda
MD PhD
Department of Neurology, Kyoto University Graduate School of Medicine, Shogoin, Kyoto, Japan.
J Isnard
MD PhD
Department of Functional Neurology and Epileptology, Hôpital Neurologique, Lyon, France.
M Iwasaki
MD PhD
P Jabbour
MD
L Jehi
Department of Neurological Surgery, Thomas Jefferson University, Philadelphia, PA, USA.
Department of Neurosurgery, The Cleveland Clinic Foundation, Cleveland, OH, USA.
MD
C Juhász
Department of Neurosurgery, Tohoku University Graduate School of Medicine, Sendai, Japan.
Departments of Pediatrics and Neurology, Children’s Hospital of Michigan, Wayne State University, Detroit, MI, USA.
MD PhD
P Kahane
Department of Neurology and INSERM, Grenoble University Hospital, Grenoble, France.
MD PhD
G Kalamangalam MD DPhil Department of Neurology, Institute of Neurological Sciences, Southern General Hospital, Glasgow, UK; and The Cleveland Clinic Foundation, Cleveland, OH, USA. K Källén
Perinatal Epidemiology Research Center, Tornblad Institute, Lund University, Lund, Sweden.
MD
AM Kanner
MD
C Kellinghaus
Department of Neurological Sciences, Rush Medical College and Rush University Medical Center, Chicago, IL, USA.
MD
Department of Neurology, University Hospital Münster, Münster, Germany.
KM Klein
MD
Department of Neurology, Marburg Interdisciplinary Epilepsy Center, University Hospital Giessen, Marburg, Germany.
GH Klem
MD
Department of Neurology, Cleveland Clinic Foundation, Cleveland, OH, USA.
S Knake
MD
Clinic for Neurosurgery, Interdisciplinary Epilepsy Center, University Hospital Giessen, Marburg, Germany.
M Koepp
MD PhD
P Kotagal
MD
M Koubeissi K Krakow
M Kunimoto
Epilepsy Center, The Cleveland Clinic Foundation, Cleveland, OH, USA.
MD
MD
Department of Clinical and Experimental Epilepsy, Institute of Neurology, University College London, London, UK.
Department of Neurology, University Hospitals Case Medical Center, Case Western Reserve University, Cleveland, OH, USA.
The Department of Neurology, J.W. Goethe University; Brain Imaging Center, Frankfurt, Germany. MD
Department of Neurosurgery, Asahikawa Medical College, Asahikawa, Japan.
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List of Contributors
D Lachhwani
MD
Department of Neurology, The Cleveland Clinic Foundation, Cleveland, OH, USA.
TD Lagerlund
MD
Section of Electroencephalography, Mayo Clinic; Foundation Mayo Clinic College of Medicine, Rochester, MN, USA.
DV Lardizabal JF LeBas BI Lee
MD
Department of Neurobehavioral Sciences, Kirksville College of Osteopathic Medicine, Kirksville, MO, USA.
Department of Clinical Neurosciences, Neuroradiology, Grenoble University Hospital, Joseph Fourier University, Grenoble, France.
MD PhD
Department of Neurology, Yonsei University College of Medicine, Severance Hospital, Seoul, South Korea.
MD
K Lehnertz
Department of Epileptology, University of Bonn, Bonn, Germany.
MD
S-K Lee MD Department of Neurology, Seoul National University Hospital, Seoul National University Medical Research Institute, Seoul, South Korea. E Lehner-Baumgartner
PhD
Department of Neurology, University of Vienna, Vienna, Austria.
K Lehnertz Department of Epileptology, Helmholtz-Institute for Radiation and Nuclear Physics, University of Bonn, Bonn, Germany. RP Lesser
SD Lhatoo SH Lim
Department of Neurology and Neurosurgery, Johns Hopkins University, Baltimore, MD, USA.
MD
MBBS MD MRCP
MBBS MRCP
C Locharernkul
M Lotto
Department of Neurology, Singapore General Hospital, Outram Road, Singapore.
MD
T Loddenkemper
Department of Adult Epilepsy, The Cleveland Clinic Foundation, Cleveland, OH, USA.
Division of Neurology, Department of Medicine, King Chulalongkorn Memorial Hospital, Bangkok, Thailand.
MD
Department of Neurology, The Cleveland Clinic Foundation, Cleveland, OH, USA.
Department of Anesthesiology, The Cleveland Clinic Foundation, Cleveland, OH, USA.
MD
A Lozano Krembil Neuroscience Centre, Toronto Western Hospital; and Division of Neurosurgery, University of Toronto, Toronto, Ontario, Canada. HO Lüders
MD PhD
Epilepsy Center, Neurological Institute, University Hospitals of Cleveland, Case Western Medical Center, Cleveland, OH, USA.
J Mani Department of Neurology, Bombay Hospital and Medical Research Center, Wockhardt Hospitals, Mumbai, India; Department of Neurology, The Cleveland Clinic Foundation, Cleveland, OH, USA. R Matsumoto F Mauguière France.
MD PhD
Kansai Regional Epilepsy Center, National Hospital Organization, Utano National Hospital, Narutaki, Ukyo-ku, Kyoto, Japan.
MD PhD DSc
Functional Neurology and Epileptology, Federative Institute of Neurosciences, Neurological Hospital P. Wertheimer, Lyon,
Y Mayanagi
MD
Department of Neurosurgery, Tokyo Police Hospital, Tokyo, Japan.
C McIntyre
PhD
Department of Biomedical Engineering, The Cleveland Clinic Foundation, Cleveland, OH, USA.
MA McLean
H-J Meencke I Melamed L Minotti S Mittal
Department of Clinical and Experimental Epilepsy, Institute of Neurology, University College London, London, UK.
MD
MD PhD
Division of Neurosurgery, University of Missouri-Columbia, Columbia, MO, USA.
MD
MD
Berlin-Brandenburg Epilepsy Center; Department of Epileptology, Institute of Diagnostic Epilepsy, Berlin, Germany.
Department of Clinical Neurosciences, Epilepsy Unit, Grenoble University Hospital, Joseph Fourier University, Grenoble, France.
Department of Neurosurgery, Wayne State University, Detroit, MI, USA.
MD
GL Möddel
Department of Neurology, Münster University Clinic, Münster, Germany.
MD
A Mohamed
MBBS(Hons) BSc(Maths)FRACP
J Montes
Division of Pediatric Neurosurgery, Montréal Children’s Hospital, McGill University Health Centre, Montréal, Quebec, Canada.
MD
MF Moodley D Moon
Department of Neurology, The Cleveland Clinic Foundation, Cleveland, OH, USA.
Department of Neuroradiology, The Cleveland Clinic Foundation. Cleveland, OH, USA.
MD
F Mormann
MD
Royal Prince Alfred Hospital, The University of Sydney, New South Wales, Australia.
MD
Department of Epileptology, University of Bonn, Bonn, Germany.
MJ Morrell MD Department of Neurology, Columbia University, College of Physicians and Surgeons; Columbia Comprehensive Epilepsy Center, New York, NY, USA. H Morris
MD
G Morrison L Mulligan
Department of Neurology, The Cleveland Clinic Foundation, Cleveland, OH, USA.
MD
MD
V Nagaraddi
Division of Neurological Surgery, University of Miami School of Medicine, Miami Children’s Hospital, Miami, FL, USA.
Department of Neurosurgery, Yale University School of Medicine, New Haven, CT, USA.
MD
Department of Neurology, The Cleveland Clinic Foundation, Cleveland, OH, USA.
DR Nair
MD
Section of Epilepsy, Department of Neurology, The Cleveland Clinic Foundation, Cleveland, OH, USA.
SJ Nagel
MD
Department of Neurosurgery, The Cleveland Clinic Foundation, Cleveland, OH, USA.
I Najm,
MD
RI Naugle
Department of Neurology, The Cleveland Clinic Foundation, Cleveland, OH, USA.
PhD
Department of Psychiatry and Psychology, The Cleveland Clinic Foundation, Cleveland, OH, USA.
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List of Contributors
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S Noachtar Epilepsy Center, Department of Neurology, University of Munich, Munich, Germany. S Nehamkin R-EEG/EPT ALF Palmini
MD PhD
HW Pannek
MD
CNIM
South Euclid, OH, USA.
Department of Neurology, São Lucas Hospital, Cathólic University of Rio Grande do Sul, Porto Alegre, RS, Brazil.
Bethel Epilepsy Centre, Bielefeld, Germany.
A Pascual-Leone MD PhD Center for Noninvasive Brain Stimulation, Harvard Medical School; Departments of Neurology, Beth Israel Deaconess Medical Center and Boston Children’s Hospital, Boston, MA, USA. JP Phillips
MD
Department of Neurosurgery, Beaumont Hospital, Beaumont, Dublin, Ireland.
CE Polkey
MD FRCS
B Pohlmann-Eden HB Pomata R Prayson
Institute of Epileptology, King’s College London, London, UK. MD
Bethel Epilepsy Center, Bielefeld, Germany.
Department of Neurosurgery, Hospital de Pediatría J. P. Garrahan, University of Buenos Aires, Buenos Aires, Argentina.
MD
Department of Anatomic Pathology, The Cleveland Clinic Foundation, Cleveland, OH, USA.
MD
K Radhakrishnan Kerala, India.
DM
Department of Neurology, Sree Chitra Tirunal Institute for Medical Sciences and Technology, Thiruvananthapuram,
A Ray
MD
Department of Neurology, Fortis Hospital, Noida, India; The Cleveland Clinic Foundation, Cleveland, OH, USA.
J Reis
MD
Department of Neurology, Interdisciplinary Epilepsy Center, Philipps-University, Marburg, Germany.
EO Richter S Rona
Department of Neurological Surgery and McKnight Brain Institute, University of Florida, Gainesville, FL, USA.
MD
MD PhD MBA
SN Roper
Department of Neurological Surgery and McKnight Brain Institute, University of Florida, Gainesville, FL, USA.
MD
F Rosenow Germany. MA Rossi IL, USA.
Department of Neurosurgery, University Hospital, Eberhard Karls University, Tübingen, Germany.
Department of Neurology, Marburg Interdisciplinary Epilepsy Center, University Hospital Giessen and Marburg GmbH, Marburg,
MD
Department of Neurological Sciences, Rush Medical College, Rush Epilepsy Center and Rush University Medical Center, Chicago,
MD
A Rotenberg MD Center for Noninvasive Brain Stimulation, Harvard Medical School; Department of Neurology, Beth Israel Deaconess Medical Center and Boston Children’s Hospital, Boston, MA, USA. P Ruggieri GL Russo P Ryvlin
Department of Diagnostic Radiology, The Cleveland Clinic Foundation, Cleveland, OH, USA.
MD
“Claudio Munari” Epilepsy Surgery Centre, Niguarda Hospital, Milan, Italy.
MD
Working Group on Epilepsy Research, Berlin, Germany.
MD PhD
AC Sakamoto MD São Paulo, Brazil. V Salanova F Salazar
MD FAAN
Department of Neurology, Indiana University School of Medicine, Indianapolis, IN, USA.
The Institute of Neurology and Neurosurgery at Saint Barnabas, West Orange, NJ, USA.
MD
D Saski-Adams K Schindler
Department of Neurology, Psychiatry and Psychology, Ribeirão Preto Faculty of Medicine, University of São Paulo,
Department of Neurosurgery, The Cleveland Clinic Foundation, Cleveland, OH, USA.
MD
C Santschi
PhD
MD
MD PhD
Division of Neurosurgery, University of North Carolina, Chapel Hill, NC, USA. Abteilung für Epileptologie & Elektroencephalographie, Neurologische Klinik, Universitätsspital, Zürich, Switzerland.
D Schmidt
MD
Epilepsy Research Group Berlin, Berlin, Germany.
J Schramm
MD
Department of Neurosurgery University of Bonn Medical Center, Bonn, Germany.
O Schröttner A Schubert R Schulz
MD
MD
Department of General Anesthesiology, The Cleveland Clinic Foundation, Cleveland, OH, USA.
Bethel Epilepsy Center, Bielefeld, Germany.
MD
E Seigneuret H Shibasaki
Department of Neurosurgery, Medical University of Graz, Graz, Austria.
Department of Clinical Neurosciences, Grenoble University Hospital; Joseph Fourier University, Grenoble, France.
MD MD
Takeda General Hospital, Ishida, Fushimi-ku, Kyoto, Japan.
H Shmizu Department of Neurosurgery, Tokyo Metropolitan Neurological Hospital, Fuchu, Tokyo, Japan. SU Schüle
MD
TL Skarpaas
MD
CT Skidmore SR Sinha
The Cleveland Clinic Foundation, Cleveland, OH; Northwestern University, Chicago, IL, USA. Division of Laboratory Medicine, Sørlandet Hospital HF, Kristiansand, Norway.
MD
MD PhD
Jefferson Comprehensive Epilepsy Center, Department of Neurology, Thomas Jefferson University, Philadelphia, PA, USA. Department of Neurology, Johns Hopkins University; Sinai Hospital of Baltimore, Baltimore, MD, USA.
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List of Contributors
S Sisodiya MD PhD Department of Clinical and Experimental Epilepsy, Institute of Neurology, University College London, Queen Square, London; National Society for Epilepsy, Bucks, UK. MC Smith MD Department of Neurological Sciences, Rush Medical College, Rush Epilepsy Center and Rush University Medical Center, Chicago, IL, USA. P Smyth
Department of Political Science, University of Melbourne, Melbourne, Victoria, Australia.
PhD
NK So
MD
Oregon Comprehensive Epilepsy Program, Portland, OR, USA.
S Sood
MD
Department of Neurosurgery, Children’s Hospital of Michigan, Wayne State University, Detroit, MI, USA.
D Spencer
Department of Neurosurgery, Yale University, New Haven, CT, USA.
MD
MR Sperling R Spreafico
MD
Jefferson Comprehensive Epilepsy Center, Department of Neurology, Thomas Jefferson University, Philadelphia, PA, USA.
National Neurological Institute, “C. Besta,” Milano, Italy.
MD
T Srikijvilaikul MD Department of Neurosurgery, Chulalongkorn Comprehensive Epilepsy Program, King Chulalongkorn Memorial Hospital, Patumwan, Bangkok, Thailand. RJ Staba Department Neurobiology, David Geffen School of Medicine, University of California, Los Angeles, CA, USA. H Stefan
Department of Neurology, Center of Epilepsy (ZEE), University of Erlangen-Nuremberg, Erlangen, Germany.
MD
BJ Steinhoff FT Sun
MD
Epilepsy Center Kork, Kehl-Kork, Germany.
Clinical Scientist, NeuroPace Inc, Mountain View, CA, USA.
PhD
S Takebayashi
MD
Department of Neurosurgery, Asahikawa Medical College, Asahikawa, Japan.
J Tamraz
MD
Department of Neurosciences and Neuroradiology, Université Saint-Joseph, Beirut, Lebanon.
T Tanaka
MD
Department of Neurosurgery, Asahikawa Medical College, Asahikawa, Japan.
N Tandon
MD
Department of Neurosurgery, University of Texas Medical School, Houston, TX, USA.
AS Tanner
MD
Epilepsy Program, Saint Mary's Neuroscience Program, Grand Rapids, MI, USA.
L Tassi “Claudio Munari” Epilepsy Surgery Centre, Niguarda Hospital, Milan, Italy. TK Tcheng Neuropace Inc, Mountain View, CA, USA. M Thom
Department of Clinical and Experimental Epilepsy, Institute of Neurology, University College London, Queen Square, London, UK.
MD
G Thut Center for Noninvasive Brain Stimulation, Harvard Medical School; Departments of Neurology, Beth Israel Deaconess Medical Center and Boston Children’s Hospital, Boston, MA, USA. R Thorbecke
MD
F Tergau
Department of Clinical Neurophysiology, University of Göttingen, Göttingen, Germany.
MD
CQ Tilelli
Bethel Epilepsy Center, Bielefeld, Germany.
Department of Neurology, The Cleveland Clinic Foundation, Cleveland, OH, USA.
MD
TN Townsend MD Department of Neurology and Neurosurgery, McGill University; McConnell Brain Imaging Center, Montréal Neurological Institute, Montréal, Quebec, Canada. I Tuxhorn K Usui
MD ChB
Bethel Epilespy Center, Bielefeld, Germany.
Human Brain Research Center, Kyoto University Graduate School of Medicine, Shogoin, Sakyo-ku, Kyoto, Japan.
MD
FL Vale MD Department of Neurological Surgery, University of South Florida College of Medicine and Tampa General Hospital Comprehensive Epilepsy Program, Tampa, FL, USA. P LeVan
Montréal Neurological Institute, Montréal, Quebec, Canada.
MD
MA Vanegas
MD
DN Velis
Dutch Epilepsy Clinics Foundation, Heemstede, The Netherlands.
MD
Functional Neurosurgery, National Institute of Neurology and Neurosurgery, México D.F., México.
J-P Vignal
MD
Service de Neurologie, Centre Hospitalier Universitaire, Nancy, France
F Villarejo
MD
Department of Neurosurgery, Niño Jesus Hospital, Madrid, Spain.
K Vives
MD
C Vollmar
Departments of Neurology, Neurosurgery, and Pathology, Yale University School of Medicine, New Haven, CT, USA.
MD
Department of Radiology, Ludwig-Maximilians-University, Klinikum Innenstadt, Munich, Allemagne, Germany.
R Wennberg MD Krembil Neuroscience Centre, Toronto Western Hospital and Division of Neurology, Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada. P Widdess-Walsh S Wiebe
MD
HG Wieser
MD
Department of Neurology, The Cleveland Clinic Foundation, Cleveland, OH, USA.
Department of Clinical Neurosciences, University of Calgary, Alberta, Canada. MD
Abteilung für Epileptologie & Elektroencephalographie, Neurologische Klinik, Universitätsspital, Zürich, Switzerland.
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List of Contributors PA Winkler
MD
BM Wingeier
P Wolf
MD
E Wyllie
MD
MD
Brain Sciences Institute, Swinburne University of Technology, Hawthorn, Victoria, Australia.
MD
MRI Unit, Bethel Epilepsy Center, Bielefeld, Germany.
Research Unit for Photodermatology, Department of Dermatology, Medical University Graz, Graz, Austria. Section of Pediatric Neurology, Department of Neurology, The Cleveland Clinic Foundation, Cleveland, OH, USA.
EMT Yacubian I Yang
Department of Neurosurgery, University of Munich, Munich, Allemagne, Germany.
MD
FG Woermann
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MD
Department of Neurology and Neurosurgery, University of São Paulo, São Paulo, Brazil.
Department of Neurological Surgery, University of California, San Francisco, CA, USA.
D Zumsteg MD Krembil Neuroscience Centre, Toronto Western Hospital and Division of Neurology, Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada.
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Preface It was just 7 years back, in 2001, that Dr. Youseff Comair and I edited the last book dedicated to epilepsy surgery.1 It is encouraging to note that epilepsy surgery has again made major advances, calling for a complete rewriting of essentially all the chapters of that book. Interestingly, the development of new diagnostic techniques, which certainly permit a more precise and reliable diagnosis of the epileptogenic zone, with very few exceptions, have not replaced some of the more classical diagnostic methods. In this sense, it is notorious that clinical semiology and clinical neurophysiology continue to be irreplaceable diagnostic techniques that provide a wealth of information. Moreover, modern technology, which makes recording, storage, and computer analysis of large amounts of neurophysiological data possible, gives us access to new data, such as the high-frequency oscillations or the EEG DC shifts, which promise to play important roles in the definition of the epileptogenic zone. This Textbook of Epilepsy Surgery includes over 20 chapters dedicated exclusively to the history of epilepsy surgery in different countries. I felt that it was important to collect this information on a timely basis when many of the main players who actually participated in the development of epilepsy surgery, or at least directly witnessed the developments, are still active in the field. As in our previous book on epilepsy surgery, in this book too we devote significant space to the description of the semiological seizure classification and the detailed clinical description of the epilepsies that are remediable by epilepsy surgery. In this book, we follow a systematic approach to the diagnostic evaluation of patients who are candidates for epilepsy surgery. We first discuss the general principles of epilepsy surgery, and then divide the presurgical evaluation according to the six zones (symptomatogenic zone, irritative zone, ictal onset zone, the epileptic lesion, the functional deficit zone, and the epileptogenic zone) described in the general principles chapter. These series of chapters conclude with the description of the Epilepsy Surgery Management Meeting, an essential and indispensable part of the surgical evaluation.
REFERENCES 1. Lüders H. Epilepsy Surgery, Raven Press, 1992.
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The book also incorporates detailed discussions of the cortical mapping techniques and the numerous surgical techniques that can be used to surgically treat epilepsy. This is complemented by surgical outcome, the post-surgical medical management, surgical failures, and neuropathology. Finally, selected case presentations are discussed, and proposals for the establishment of an epilepsy surgery program, classification of surgical outcome, and protocols for storage and processing of brain tissue for molecular studies are presented. I feel that epilepsy surgery is still an extremely attractive management tool for patients with medically intractable epilepsy. Unfortunately, in spite of dramatic increases in the number and mechanisms of action of modern antiepileptics, close to a third of all epileptics still suffer from uncontrolled seizures. A significant proportion of these patients are excellent surgical candidates. The extreme precision of our current presurgical evaluation methods and the recent advances in neurosurgical techniques make it imperative that all these patients get evaluated at an epilepsy center that offers epilepsy surgery. In a significant proportion of these patients, the epilepsy can be either eliminated (cured) or a significantly better seizure control can be achieved, with relatively low surgical risk. Referrals for epilepsy surgery have been continuously increasing since the pioneering efforts at the end of the 19th century. I hope that this book will contribute to making epilepsy surgery available to an even larger percentage of patients with medically intractable epilepsy.
Acknowledgments I would like to acknowledge the help of Ms. Connie Scolaro and Ms. Autumn Semsel who, throughout the editorial process, assisted me as executive secretaries, making the editorial process so much easier. Hans O Lüders
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“Claudio Munari” Epilepsy Surgery Centre, Milano “Neuromed” Epilepsy Surgery Centre, Pozzilli
Figure 7.4
29 30 27 42
34 22 28 38
21
19
18 18
37
37
Paralimbic areas High-order (heteromodal) association areas Modality-specific (unimodal) association areas Idiotypic (primary) areas
20
Figure 34.1
VAC
VPC
i1
i2
AC-PC
i3
R
L
A
B C Figure 39.3
(a)
(b)
(c)
(d)
(e)
(f)
19
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(a)
(b)
Figure 55.2
Figure 55.7
(a)
(b)
(c)
(d)
(f) (e)
(g)
(i)
(h)
Figure 71.2
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(b)
SPM{F7.479,288.6}
SPM{T294.5}
P2 years after surgery) was observed in only 5% of all patients and was often preceded by a specific explanatory factor such as withdrawal of antiepileptic medication. In a multivariate analysis, unitemporal MRI abnormalities, early onset of epilepsy, or the predominance of focal seizures with impaired consciousness with focal ictal EEG, were identified as predictors for successful postoperative outcome. The epilepsy unit in Helsinki University Hospital (Hospital for Children and Adolescents and Department of Neurosurgery) started in 1991 with pediatric epilepsy surgery, and since 1998 the team has also offered epilepsy surgery to adult patients in collaboration with the Department of Neurology. Between 1991 and 2005 a total of 187 therapeutic epilepsy surgery interventions had been performed in Helsinki. The program has included temporal resections (n = 72), extratemporal resections (n = 49), callosotomies (n = 34), hemispherotomies (n = 29), multiple subpial transections (n = 1), and radiotherapy of hamartomas (n = 2). During preoperative evaluation all patients were studied with video-EEG, 1.5 T MRI, and neuropsychology. When necessary ictal-SPECT, MEG (localization of interictal spikes and functional areas), FDG-PET, magnetic resonance spectroscopy, and/or invasive monitoring with subdural grids (n = 22) and strips (n = 3) is used during the presurgical work-up. Nearly all patients undergo psychiatric evaluation. The majority of the patients are children or adolescents (76%) and due to the heterogeneous population regarding syndromes and etiologies (including catastrophic epilepsies of
Table 9.2 Long-term postsurgical seizure outcome in 140 adult temporal lobe epilepsy (TLE) patients in Kuopio Epilepsy Center22 Curative group with unilateral TLE (n=103) Entire group (%)
Seizure free Persisting auras Worthwhile outcome (Engel I-II)
81
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45 12
61 11
27 3
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62
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early childhood) general outcome figures are difficult to evaluate. The team has, however, recently evaluated the two-year follow-up of cognitive outcome after pediatric epilepsy surgery.23 Altogether 38 patients, between 3–17 years of age, were evaluated before surgery and six months and 2 years postoperatively. No significant change in verbal or performance IQ was demonstrated at group level. Lateralization, type of surgery, age, sex, and presurgical IQ did not affect outcome. In conclusion, epilepsy surgery in children and adolescents did not in general have a significant impact on cognitive development in a two-year perspective. Medical intractability is defined as persistent seizures despite 2–3 maximally tolerated AED trials. In older children and adults medical intractability can be diagnosed in two years in most cases. However, the median duration of epilepsy in patients referred to presurgical evaluation at Kuopio Epilepsy Center has been 19 years.22 In the future, emphasis should be put on early prediction of medically intractable temporal lobe epilepsy in children and adolescents, since early surgery probably improves the overall outcome, especially in younger patients. Further evaluation for longterm cognitive outcome is also warranted. The epilepsy unit in Helsinki continues to focus on pediatric epilepsy surgery, accepting pediatric patients from all parts of Finland and adults within their own catchment area. Kuopio Epilepsy Center continues to treat patients with medically refractory temporal or extra-temporal focal epilepsy of all ages from the whole country, especially focusing on getting patients referred earlier.
Norway and Finland are shown in Table 9.3. Too few patients, especially children in the Scandinavian three countries, with severe, drug-resistant epilepsy, are referred to the centers for surgical evaluation, and many are referred too late, i.e., long after psychosocial problems have become irreversible. This situation is most probably not at all unique since there is a general concern that epilepsy surgery is underused. One reason for this underutilization of the resource of epilepsy surgery might be lack of knowledge about epilepsy within the medical profession24 or lack of knowledge about the favorable results of surgical treatment of epilepsy within the neurological community. In a survey concerning the provision of epilepsy services in Europe which was undertaken by the ILAE Commission on European Affairs a few years ago, all countries but six stated that they had epilepsy surgery programs.24 Lack of epilepsy surgery was more commonly reported from Eastern and Southern Europe, whereas several western ILAE chapters mentioned as a problem that epilepsy surgery was present but underused. The epilepsy surgery groups in the Scandinavian countries together with Finland recently decided to organize a meeting for collaboration and the first Nordic epilepsy surgery meeting was held in Sweden in 2004. The second will be held in Norway 2006. In the future the epilepsy surgery groups in the Nordic countries plan to meet at regular intervals to learn from each other and expand their network cooperation for the benefit of the patients.
Acknowledgment The future of epilepsy surgery in the Nordic countries? Despite increased attention in recent years, epilepsy surgery is assumed to be under-utilized in the Nordic countries. Approximate yearly numbers of procedures in Sweden,
We want to thank Kristina Malmgren, professor in neurology at Sahlgrenska University Hospital in Gothenburg, for editorial help, and Kirsten E. Stabell, neuropsychologist at the National Centre for Epilepsy in Sandvika, for providing us with the number of presurgical investigations and surgical procedures in Norway.
Table 9.3 Yearly epilepsy surgery procedures in the Nordic Countries based on an average over a 10–15 year period Sweden (9 million inhab.)
Denmark (5.3 million inhab.)
Norway (4.5 million inhab.)
Finland (5.2 million inhab.)
Temporal lobe resections (selective AHE included)
41
14
25
19
Extra-temporal lobe resections
14
2
7
5
Mixed group Multilobar resections, hemispherotomies, MST, callosotomies, hamartomas (pure lesionectomies are also included in the mixed group in Finland)
14
4
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7
Inhab. = inhabitants.
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REFERENCES 14. 1. 2. 3. 4. 5. 6. 7.
8. 9.
10.
11. 12. 13.
Expertrapport – Epilepsi – förekomst, handläggning och vårdorganisation. Stockholm, Sweden: Socialstyrelsen, 1993. Malmgren K, Sullivan M, Ekstedt G, et al. Health-related quality of life after epilepsy surgery – A Swedish multicenter study. Epilepsia 1997;38(7):830–8. Silander HC, Blom S, Malmgren K, et al. Surgical treatment for epilepsy – a retrospective Swedish multicenter study. Acta Neurol Scand 1997;95:321–30. Forsgren L Prevalence of epilepsy in adults in northern Sweden. Epilepsia 1992;33(3):450–8. Malmgren K, Rydenhag B. Temporal lobe resections for epilepsy. Data from the Swedish National Epilepsy Surgery Register 1990–95. Epilepsia 2000;41(Suppl 7):140. Rydenhag B, Silander HC, Malmgren K, Flink R. Lesionectomy for epilepsy: data from the Swedish National Epilepsy Surgery Register 1990–1999. Epilepsia 2004;45(Suppl. 3):187. Malmgren K, Rydenhag B, Olsson I, Flink R. Temporal lobe resection for epilepsy in mentally retarded patients: Data from the Swedish National Epilepsy Surgery Register 1990–1999. Epilepsia 2005;46(Suppl 6): 320. Rydenhag B, Malmgren K, Flink R. Epilepsy surgery in mentally retarded patients: pathoanatomical diagnoses. Epilepsia 2005;46(Suppl 6): 68. Olsson I, Malmgren K, Rydenhag B, Flink R. Hemispherectomies and multilobar resections: data from the Swedish National Epilepsy Surgery Register 1990–99. Epilepsia 2005;46 (Suppl 6): 162. Rydenhag B, Silander HC. Complications of epilepsy surgery after 654 procedures in Sweden, September 1990–1995: a multicenter study based on the Swedish National Epilepsy Surgery Register. Neurosurg 2001;49(1): 51–5. Behrens E, Schramm J, Konig R. Surgical and neurological complications in a series of 708 epilepsy surgery procedures. Neurosurg 1997;41(1):1–9. Flink R, Malmgren K, Åmark P, Blom S. Trends in the use of epilepsy surgery in Sweden 1991–1999. Epilepsia 2002; 43(Suppl. 8):137. Jensen I, Vaernet K. Temporal lobe epilepsy. Acta Neurochirurgica 1977;37:173–200.
15. 16. 17.
18.
19.
20.
21.
22. 23. 24.
ILAE Commision Report. Commission on Neurosurgery of the International League Against Epilepsy (ILAE) 1993–1997: recommended standards. Epilepsia 2000;41(10):1346–9. Engel J Jr. Outcome with respect to epileptic seizures. In: Engel J Jr, ed. Surgical Treatment of the Epilepsies 2nd edn. New York: Raven Press, 1993. Guldvog B, Loyning Y, Hauglie-Hanssen E, et al. Surgical versus medical treatment for epilepsy. II. Outcome related to social areas. Epilepsia 1991;32(4):477–86. Bjørnæs H, Stabell KE, Røste GK, Bakke SJ. Changes in verbal and nonverbal memory following anterior temporal lobe surgery for refractory seizures: effects of sex and laterality. Epilepsy Behav. 2005;6(1):71–84. Bjørnæs H, Stabell KE, Heminghyt E, et al. Resective surgery for intractable focal epilepsy in patients with low IQ: predictors for seizure control and outcome with respect to seizures and neuropsychological and psychosocial functioning. Epilepsia 2004;45(2):131–9. Immonen A, Jutila L, Kälviäinen R, et al. Preoperative clinical evaluation, outline of surgical technique and outcome in temporal lobe epilepsy. Advances in Technical Standards in Neurosurgery 2004;29:87–132. Lamusuo S, Pitkänen A, Jutila L, Ylinen A, Partanen K, Kälviäinen R, Ruottinen HM, Oikonen V, Nagren K, Lehikoinen P, Vaplahti M, Vainio P, Rinne JO. [11C]Flumazenil binding in the medial temporal lobe in patients with epilepsy: correlation with hippocampal MR volumetry T2 relaxometry, and neuropathology. Neurology 2000;40(2–3):155–70. Jutila L, Immonen A, Partanen K, Partanen J, Mervaala E, Ylinen A, Alafuzoff I, Paljarvi L, Karkola K, Vapalahti M, Pitkanen A. Neurobiology of epileptogenesis in the temporal lobe. Adv Tech Stand Neurosurg 2002;27:5–22. Jutila L, Immonen A, Mervaala E et al.: Long term outcome of temporal lobe epilepsy surgery: analyses of 140 consecutive patients. JNNP 2002;73:486–94. Korkman M, Granström M-L, Kantola-Sorsa E et al. Two-year follow-up of intelligence after pediatric epilepsy surgery. Pediatric Neurology 2005;33(3):173–8. Malmgren K, Flink R, Guekht AB, et al. The provision of epilepsy care across Europe. Epilepsia 2003;44(5):727–31.
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The development of epilepsy surgery in the Netherlands and Belgium W van Emde Boas and PAJM Boon
The Netherlands1 In the Netherlands, initial development of brain surgery came relatively late. In his jubilee speech on the development of surgery during the last 30 years, at the occasion of the 25th anniversary of the Nederlands Tijdschrift voor Geneeskunde (NTvG) in 1882, J.W.R. Tilanus (1829–1914), professor of surgery in Amsterdam, does not yet even mention surgery of the nervous system2 and, apart from the usual descriptions of trepanation in early general medical or surgical texts, up to 1890 no papers on surgical intervention on either the central or the peripheral nervous system had been published in the NTvG, then as now the main Dutch medical journal, nor by Dutch authors, in other medical journals or books.3,4 This changed at the initiative of Cornelis Winkler (1855–1941), the first professor in psychiatry and neurology in the Netherlands and generally considered the founding father of modern Dutch Neurology (Figure 10.1). First steps: the neurologist and the surgeon Winkler studied medicine in Utrecht where he was greatly influenced by the strict scientific approach of ophthalmologist and physiologist F.C. Donders (1818–1889). Following graduation and obtaining a PhD degree on a thesis on Virus Tuberculosum 1879; and a brief period as clinical resident in The Hague, Winkler expressed to his former teacher the desire for a more research oriented position in Utrecht. Offered the position of reader in psychiatry, Winkler initially declined, considering psychiatry too philosophical and unscientific to his liking. After some clinical work with neurological patients in the clinic for internal medicine of S. Talma (1847–1918) and following visits to T. Meynert (1833–1892) and J. Wagner von Jauregg (1857–1940) in Vienna and to numerous German protagonists of the neuropathological oriented school of psychiatry and neurology, he became convinced of the advantages of teaching both neurology and psychiatry as a whole and accepted in 1885 the lectureship of psychiatry in Utrecht, followed in 1893 by the appointment to professor in psychiatry and neurology, the first such chair to be officially created in the Netherlands.’5 Winkler was well aware of the current clinical and experimental literature on the localization of brain functions and the application of these findings to clinical neurology and early on expressed his intention to follow the example of V. Horsley (1857–1916) and others and to focus attention also 84
on brain surgery as a possible treatment for neurological disorders, notably in epilepsy patients with seizures comparable to those, induced by electrical stimulation of the cortex in animals by E. Hitzig (1838–1907) or described in humans by J. Hughlings Jackson (1835–1911).5 As luck would have it, Winkler’s appointment coincided with that of his friend and fellow student J.A. Guldenarm (1852–1905) as general surgeon in the Deaconess Hospital in Utrecht. According to Winkler, Guldenarm was a gifted and inventive surgeon, who made his own instruments, operated very neatly and with whom he felt sufficiently confident to try to remove brain tumours, ‘a great endeavour, considering that we hardly knew what we were going to do’.5 On 11 November 1889 they performed their first published surgery on a 54-year-old ex-soldier with a two year history of Jackson type seizures, beginning in the right leg and with fast neurological and mental deterioration during the last few weeks. Exploring the left frontocentral area, they partially resected an angiosarcoma from the left gyrus frontalis superior, lobus paracentralis, and gyrus centralis anterior. The patient survived the procedure and remained without seizures but with hemiplegia, aphasia, progressive loss of consciousness and increasing prolapsus cerebri before dying, three weeks after surgery.6 Between 1891 and 1893 Winkler and Guldenarm, together with A. Huysman, ENT surgeon, and H. Buringh Boekhoudt, resident to Winkler, published a series of five ‘contributions to surgery of the brain’ in the NTvG in which they provided meticulous detailed clinical histories of 15 patients (3 not operated) and discuss the value, possibilities and – often – impossibilities of surgical intervention in various neuropathological conditions.6–10 Although epilepsy was not mentioned in the title of any of these five papers it was a major symptom in five and the primary indication for surgery in a further two of the twelve operated patients. The first of the latter was a 22-year-old man with an 11 year history of Jacksonian seizures in the left hand and arm who had a right frontocentral angioma removed by Guldenarm on 4 April 18906 and changed from >40 seizures a day to multiple days without seizures with a follow up of 7 years.11 This patient was also published in a thesis 1891; by a Dutch physician, P.C. Th. Lens, defended however in Giessen and thus not really to be considered the first Dutch thesis on epilepsy surgery.12 The second patient was a 19-year-old boy with an epilepsy history of 6 years, following a skull trauma at the age of 8 years. He became free of seizures, following extirpation of a calcified lesion from the left hand area9 but died from
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central and Sylvian sulci and of the targeted cortical gyri, using just two external reference points (the glabella and the protuberantia occipitalis externa) to create a grid of triangles, projecting over skin of the skull.15 Since this system was based on comparative rather than absolute measurements it was considered to be more reliable than that of Horsley or others and the ‘triangulation according to Winkler’ (Figure 10.2) became the standard procedure for guiding the trepanation in the Netherlands for the next few decades. Such was Winkler’s enthusiasm for brain surgery that in 1895 he even published a long popular paper on the subject in De Gids, the most important cultural monthly magazine in the Netherlands. Despite the overall poor results (only 4 out of 18 operated cases still alive at the time of publication and only Ned.Tijdschr. voor Geneeskunde, 1892.DI.II.No.3. f
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Figure 10.1 Cornelis Winkler (1855–1941). Pencil drawing by Jan Veth, 1896. The portrait was made just after Winkler resigned in Utrecht and before he moved to Amsterdam. While making this portrait Veth (1864–1925) proposed to Winkler to give art lessons to medical doctors, in order to improve the quality of the illustrations in their publications. The idea however was never realized.5
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an occupational accident a few years later. Some of the early tumor cases, including one patient with Jacksonian seizures, were collected and described in the really first Dutch PhD thesis on brain surgery, defended by Winkler’s pupil R. S. Hermanides13 and again in the NTvG.14 Surgical techniques are not dealt with in detail in these papers although there is some discussion about the relative advances of a bony versus a soft tissue closing of the trepanation area in certain circumstances. Some procedures were only performed ‘after we had ascertained ourselves on the cadaver that the surgery was possible’.6 Major emphasis is given on the other hand to the problem of correct localization, prior to surgical intervention. The papers include some patients where Winkler failed to make a proper preoperative localizing diagnosis and he frankly admits that in at least one patient, in whom surgery failed, the obduction showed a right tentorium meningioma that, on correct diagnosis, could have been successfully removed.6 Winkler strongly believed that, unless surgeons had extensive knowledge of brain anatomy and physiology, brain surgery should be guided by the neurologist as the one both to make the exact diagnosis and to decide about the indication for surgical exploration and the place and extent of the necessary trepanation. For the latter he developed a new method to enable the neurologist and the surgeon to estimate the position of the
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D . C.WINKLER.–DRIEHOEKSMETING TER BAPALING DER BETREKKELIJKE LIGGING VAN WINDINGEN EN SLEUVEN DER GROOTE HERSENEN
Figure 10.2 Winklers method of triangulation. By constructing a series of triangles, based on the line between the glabella and the protuberantia occipitalis and the perpendicular dissecting line at midpoint he obtained a reasonable estimate of the position of the underlying cortical structures. The drawing is based on studies on 10 adult subjects; the darkened areas and numbers indicate cortical areas or sulci that reliably will be found within that specific triangle (lithograph illustration of Winkler’s paper15 in the NTvG, Bohn: Haarlem, 1892).
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two really cured) he argues for an aggressive approach since the patients, mostly tumor cases, have little to lose. For patients with epilepsy he considers the loss of some function to be preferred to the constant irritation of the cortex and the risks of the recurrent seizures. He discussed the use of electrical stimulation to identify the epileptic focus and the different surgical options. He preferred resection of the cortex, notably when abnormal on inspection, and did not think highly of the practice of just cutting around the suspected area in order to prevent seizure propagation. In an interesting last paragraph he commented on some early efforts on psychosurgery by Burckhart in Switzerland, which he rejected since he was of the opinion that one should treat the underlying disease in mental patients and not just the symptoms.16 In 1896, being refused a new clinic that was initially promised to him, Winkler resigned his position in Utrecht and within months accepted the newly created chair of Neurology and Psychiatry in Amsterdam where he would have ample access to clinical beds both for neurology and psychiatry and would be able to work together with J.K.A. Wertheim Salomonson (1864–1922), who already ran a clinic for neurology and electrotherapy, and in 1899 would be appointed to the first chair in neurology, electrotherapy, and radiography in the Netherlands. In Amsterdam Winkler continued his neurosurgical activities, together with the surgeons J.A. Korteweg (1851–1930) and J.A. Rotgans (1859–1948) and the professor in Internal medicine P.K. Pel (1851–1919), who also was actively interested in neurological diseases. Epilepsy initially remained a major indication. In 1897 Winkler’s pupil H.H. van Eyk (1869–1930) obtained his Ph.D. on the first (and until Brekelmans17 the last) Dutch dissertation to deal specifically with the surgical treatment of partial epilepsy18 and in that same year Winkler, in recognition of his expertise in the field, was invited to lecture on ‘Surgical intervention in the epilepsies’ at the International Congress of Psychiatry, Neurology and Hypnology In Brussels.11 In his dissertation Van Eyk described 10 cases of predominantly posttraumatic epilepsy, nine of them operated and with clear improvement in five. In addition he summarized the data from the literature, 13 cases of epilepsy due to subdural haematoma and 100 cases of posttraumatic epilepsy, including 7 of his own, and showed that the best results were obtained in patients in whom a recognizable lesion could be removed. His case #9 concerns a 20-year-old man with a 2 year history of focal seizures, beginning in the left hand. A first exploration by Rotgans and Buringh Boekhoudt showed local thickening of the dura over the hand area, identified by electrostimulation by Wertheim Salomonson. Nothing was excised and there was no improvement. Following two further surgeries with temporary improvement the patient was operated upon a fourth time on 18 June 1897, this time with Winkler performing the electrostimulation. A seizure was provoked by stimulating the finger area ‘which was photographically documented and found to be identical to the spontaneously observed seizures’, the first case of intracranial and intraoperative seizure monitoring? Following a local cortectomy the patient became paretic but also free of seizures for at least the next two months.18 At the congress in Brussels Winkler discussed 20 patients who had surgery, including two patients, successfully operated for ‘reflex-epilepsy’, due to peripheral nerve injury (one a cornea corpus alienum, the other a bullet injury of a branch of
the trigeminal nerve), a clinical entity which certainly was not epilepsy but was generally accepted at the time and considered a good indication for surgical intervention.19 In 13 patients partial epilepsy was the primary indication for surgery, in 5 the seizures were but a symptom of more serious neurological disease. According to Winkler posttraumatic cases had the best prognosis, tumor cases a varying outcome and infectious cases (Lues, TBC, otogenic abcesses) or alcoholic cases a poor prognosis. In cases without an external or internal scar and with a normal aspect of the cortex, cortectomy should only be performed if a typical seizure could be elicited from that area by electrical stimulation. For toxic epilepsies, even if manifesting with partial seizures, surgery was not indicated.11 Even at the time of the congress, however, the initial enthusiasm for epilepsy surgery (or even brain surgery in general) appeared to be lessening. In a comprehensive review of all neurosurgical interventions performed in the Netherlands between 1889 and 1900, published in the famous 3 volume series of A. Chipault (1866–1920) on the current state of neurosurgery in 1902, Winkler and Rotgans briefly refer to the earlier work but epilepsy is not mentioned anymore as a specific indication.3 This appears to be in line with developments elsewhere. In a long letter from London where he was visiting a number of hospitals, Wertheim Salomonson describes his admiration for the surgical skills of Horsley but also mentioned that at that time, in 1898, Horsley had not operated for epilepsy in the last 18 months because of disappointing results.20 Two conference reports and a review in the NTvG from the same period but citing predominantly German and Swiss sources also emphasized overall poor results of surgery for epilepsy21–23 and W.J.M Indemans (1868–1932), a general practitioner in Maastricht, reporting one patient, operated with moderate success for posttraumatic partial epilepsy, actually complained that he could not find a surgeon willing to operate on a second case.24 Winkler himself apparently lost interest and did not publish anything on epilepsy surgery afterwards although he remained involved in some cases later published by others. Also the attitude of the surgeons to surgery on the nervous system was changing. While most of the surgeons with whom Winkler had collaborated in Utrecht and, after 1896, in Amsterdam, apparently had little problems with his approach by which they had to rely completely on the diagnostic and localizing acumen of the neurologist, J.E. van Iterson (1842–1901), with whom Winkler performed some surgeries in Utrecht, was the first to challenge this approach. In a 1899 paper on the present state of surgery effectively citing Winkler himself, he stated that: The recognition and localisation of the pathology [in the brain] still is wanting and I am pleased to report that according to the first Dutch authority in this field [Winkler] this situation will not improve unless the surgeons themselves take up the diagnosis of brain disorders and stop acting only on guidance by specialists.25 With this, van Iterson started a controversy that was to continue for the next three decades and would clearly influence the further development of neurosurgery, and thus epilepsy surgery, in the Netherlands. At the time, however,
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The development of epilepsy surgery in the Netherlands and Belgium his word was hardly heeded and for some time to come the neurologist remained either the active guide of the surgeon or, by reversing the situation sketched by Winkler, actually took over the scalpel and the trephine. Intermezzo: the neurologist–neurosurgeon Louis Jacob Joseph Muskens (1872–1937)26 studied medicine in Utrecht and, significantly influenced by Donders and Winkler, early on decided for a career in physiology and neurology. After obtaining his PhD in 1896 on a thesis on the reflex mechanisms of the frog heart, supervised by T. Engelmann (1843–1909), successor [and son in law] of Donders, Muskens, on a travel grant provided by the Donders Society, spent two years in the USA where he visited and worked with C.L. Dana (1853–1935) in New York and H.P. Bowditch (1840–1911) in Boston. Stimulated by Winkler to further specialize himself he spent a next period in London in the National Hospital for the Paralysed and the Epileptic, working under W. Gowers (1845–1911) and notably, for 20 months, under Horsley in order to master the surgical skills necessary to render him independent from the general surgeon.27,28 In the USA and in London Muskens appeared to have developed his interest in epilepsy which to a large extent would mark his further career. Back in the Netherlands he instigated the founding, in 1902 in the Hague, of the ‘Dutch Society Against Falling Sickness’, which, contrary to the older 1882; ‘Christian Society for the Care of Sufferers from the Falling Sickness’, aimed to promote treatment rather than care of epilepsy. In the same year Muskens moved to Amsterdam in 1902 and took up a practice as specialist for nervous disorders, including the position (from its inception until 1918) of medical supervisor of the clinical and outpatient departments of the ‘Amsterdamse Gasthuis Tegen Vallende Ziekte’ (Amsterdam Hospital for Epilepsy), an initiative by the Amsterdam Branch of the Dutch Society and, in 1903, the first non-university-associated neurological clinic in the country. Together with the Hungarian J. Donath, Muskens, in 1908, founded the Journal Epilepsia and, in 1909, the International League Against Epilepsy (ILAE) of which he would remain active as general secretary for many years and which he helped to revive in 1937, after a long interruption of the ILAE activities following the turmoil of World War I.29 A prolific writer, Muskens published extensively about epilepsy, both from an experimental and a clinical view and with major emphasis on the social aspects and needs of persons with epilepsy. His vast clinical and experimental experience culminated in a major monograph on epilepsy, published in 1924 and translated both in German and in English.30 Other subjects included the segmental distribution of the sensory input of the cerebral cortex, the anatomo-physio-pathology of upper brain-stem connections, subject of a second major monograph on the supra-vestibular system,31 technical and clinical aspects of neurosurgery and a series of papers on the relation between neurology, neurosurgery, and psychiatry and the way those specialties should be taught to students and be practiced. In 1906 Muskens was admitted as private lecturer on nervous diseases at the municipal university of Amsterdam and in
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his official public lecture advocated the further development of organ oriented (sub) specialties in medicine, a subject highly controversial at the time32 (Muskens, 1906). In Muskens’s view specialties should focus on the anatomy, physiology, pathology, conservative treatment options and surgery of specific organs, the central nervous system representing one of the most ideal organ systems for such an approach. Psychiatry was to be separated from neurology [in the Netherlands it was not until 1974 that this separation finally was realized] and the surgical approach to the nervous system was best left to the neurologist with specific surgical training (i.e., Muskens himself). Like Winkler had done before him Muskens published a series of ‘contributions to the surgical treatment of the central nervous system’ in the NTvG, the third including a number of patients with seizures and the last dealing specifically with posttraumatic epilepsy,33–36 in addition to a large number of other papers or reports of clinical demonstrations of neurosurgical cases in Dutch or foreign journals. Unfortunately and contrary to the papers of his predecessor and teacher Muskens’s patient descriptions are often rather short and, when repeated, as is often the case, factual data (dates, type of trauma, patient initials, patient age) differ in successive publications, in part probably due to the then current poor quality of proofreading and correction in association with very fast publication, but in part apparently due to either shoddy writing or – worse – ‘massaging’ the data. Moreover Muskens had a highly contentious style of writing and presenting, emphasizing presumed diagnostic errors or failed procedures by others and exaggerating his own activities and results. Repeatedly and usually with good arguments and in terms which in today’s perspective would be considered too offensive for public discussion in print, his claims are refuted, his results doubted, his qualifications as a neurologist-surgeon denied, and his references identified as incorrect, not only by the general surgeons but notably also by his fellow neurologists and by the chief editor of the NTvG.37–44 Although Muskens apparently was considered as sufficiently an expert to be invited by the Belgian Red Cross to assist in setting up a unit for war casualties with brain or spinal injuries in Antwerp45 the chiefs of the university clinics in Amsterdam repeatedly refused to have Muskens operate in their clinics.44 Significantly, the well-known Amsterdam neurologist C. T. van Valkenburg (1872–1962), who for a number of years was the medical director of Muskens’s hospital, relied on other surgeons for his work on the sensory neuroanatomy of the human cortex, based on electrical stimulation during surgery.46–48 As far as epilepsy is concerned only few successful surgery cases eventually are listed in the chapter on posttraumatic and focal epilepsy and the surgical treatment of epilepsy in Muskens’s 1924 monograph.30 These include three of his favorite cases which he published and presented at many occasions, the first a patient with probably posttraumatic serous meningitis, operated in 1907 because of fast neurological deterioration, in whom the seizures were but a secondary symptom, and the second, a girl of 18 (cranial trauma at age 3 years) in whom Muskens, guided by sensory loss in the ulnar region of the left arm, ligated some ‘abnormal pial veins’ and claimed successful treatment of ‘seizures’ that by all his peers of the Amsterdam Neurological community, many of which previously had observed this patient, were consistently interpreted
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as psychogenic events. Only the third represents a true epilepsy surgery success story: a female patient who following trauma at age 4 and two earlier surgical interventions by Winkler and Rotgans at the age of 4 and 16, finally was rendered seizure free by Muskens by removal of two tiny bone fragments, found under the previous bone flap and, when the seizures still persisted, in a second session a small cortisectomy from the area where habitual seizures could be elicited by electrical stimulation. The remaining 7 patients in the chapter, which purports to present ‘a comprehensive report’ of a lifetime experience include one non-traumatic tumor patient (presented to illustrate the limited value of surgery in those cases), one patient operated in 1910 but without clinical information (‘all files lost’) or follow up, other than that the patient was successfully employed as a marine officer, 1 patient, operated by others with poor results, 2 patients with less than a year of follow up at the time of writing, leaving only two more reasonably well-documented cases, successfully operated for posttraumatic epilepsy in 1913 and 1918.30 In the same period that Muskens was active, occasional reports indicated that, as before, some surgical procedures for posttraumatic or other symptomatic forms of epilepsy were performed by a general surgeons, assisted by a neurologist, generally with acceptable results for posttraumatic epilepsy and poor results for all other cases. These were not part of any organized program but in number and results appear equal or even superior to Muskens’s activities. Not surprisingly Muskens academic career never progressed beyond his private readership and even as a neurosurgeon his real activities appear to have remained limited. Looking back, Muskens remains a major figure in the development of epileptology and epilepsy care, both in the Netherlands and internationally.26 For the actual development of either neurosurgery in general or epilepsy surgery in particular, however, this self proclaimed ‘self operating neurologist’ did relatively little and achieved even less. A second start: the neurosurgeon and the neuro(physio)logist Since otherwise the field remained in the hands of general surgeons with neither specific training nor interest in neurological disorders, the overall practice of neurosurgery in the Netherlands remained limited and of relatively poor quality for well into the first three decades of the 20th century. Yet increasingly the need for surgical treatment of some neurological disorders was felt and again it was a neurologist who took the initiative. In 1923 Bernard Brouwer (1881–1949), who studied medicine in Amsterdam and then trained with Winkler, was appointed to the chair of neurology, now for the first time divided from psychiatry, in the city of his Alma Mater. For his surgical cases he worked with the general surgeons O. Lanz (1865–1935) and W. Noordenbos Sr. (1875–1954) but he was well aware of the gap between their results and those reported by others. Contacts with H. Cushing (1869–1939) and W. Dandy (1886–1946) during a lecture tour in the USA in 1926 convinced him that good quality neurosurgery was only possible in a special setting and by dedicated and undivided neurosurgeons with specific and adequate training. In Amsterdam he managed to convince the municipal authorities
to have a new 100 bed clinic to be built, exclusively for neurological patients and including a fully equipped neurosurgical unit that could function independent of the general surgical clinic. While the clinic was being built Brouwer selected Ignaz Oljenick (1888–1981), a young resident surgeon, and sent him to Boston for training with Harvey Cushing. In 1929 Oljenick returned to Amsterdam and in September of that year the neurosurgical unit in the newly opened clinic started its activities.1 As far as can be ascertained from his publications Oljenick did not perform any procedures specifically for epilepsy. His first trainee, however, would. Arnaud Cornelis de Vet (1904–2001), studied medicine in Amsterdam and in 1929 applied for and obtained the position, offered by Brouwer, of resident in neurosurgery. De Vet thus became the first physician to be trained formally as a neurosurgeon in the Netherlands. After finishing his years of training with Brouwer and Oljenick and a study trip of several months to neurosurgical clinics in numerous European cities, De Vet in 1936 obtained his PhD, supported by Brouwer, on a thesis on the diagnosis of cerebral meningioma.49 His material concerns a series of 36 operated and (with one exception, histologically verified) and two unoperated cases, including 17 patients in whom seizures were the major (n = 13) or a contributing symptom. Fifteen of these had their meningeoma removed, two died within a few days following surgery, and of the remaining 13 no follow up is provided. He points to the potential value but also the risks of ventriculography for the diagnosis of these (and other) intracranial processes but also emphasizes the need for a meticulous anamnesis and clinical work up and devotes a special chapter on the epileptic symptoms, found predominantly in patients with meningeoma over the convexity or the parasaggittal areas of the brain, and their localizing significance. In the summer of 1936 De Vet left Amsterdam and moved to Wassenaar, a suburban village near The Hague where a former psychiatric clinic had been rebuild as the second non university associated hospital for psychiatric and neurological disorders, including the first non-university neurosurgical unit in the country. In the St. Ursula Clinic De Vet continued to pursue his interest in epilepsy as a possible target for surgical intervention and in 1938 he was appointed consultant neurosurgeon in the epilepsy clinic ‘Meer and Bosch’ in Heemstede. ‘Meer and Bosch’ was named after the stately mansion and the surrounding grounds, acquired in 1885 by the Christian Foundation for the care of Sufferers from the Falling Disease, founded in 1882, as living quarters for the clergyman-director. The institute, modeled after the Bodelschwing Institutions in Bielefeld, Germany, started in a small garden building at the premises of the founder, Lady A. J. M. Teding van Berkhout (1833–1909), in Haarlem but by 1938 had grown into a conglomerate of many buildings for housing, care, occupation or education, of adults and children with chronic epilepsy. Whereas care, provided by deaconess brothers and sisters, had been the original task of the foundation, the second quarter of the 20th century brought a shift towards a more medical oriented approach. In 1930 B. Ch. Ledeboer (1897–1959) was appointed as the first medical director, working together and not any more under the still prevailing clergyman director. Within a few years he managed to have a modern clinic built on the premises, with observation wards for adults and children, laboratories and even surgical facilities. In 1934 the
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The development of epilepsy surgery in the Netherlands and Belgium Queen Emma Clinic was officially opened and it was there that De Vet, starting 22 November 1938, practiced part time, in addition to his work in the St. Ursula Clinic. De Vet strongly believed in the value of ventriculography and designed a movable and translucent model of the ventricular system for better understanding of the movement of air through the ventricles and for illustrating and teaching puposes.50,51 He advocated that every patient with epilepsy should have at least one diagnostic encephalogram and from the register of surgical procedures of the Queen Emma Clinic52 it is clear that he practiced what he preached. From the 377 procedures performed between November 1938 and February 1942, less than 40 appear to have involved real neurosurgical interventions, including five resections of cortical scars or areas from which seizures could be elicited. Others concerned lesiectomies (glioma, angioma, meningioma, etc.) which De Vet himself did not consider ‘epilepsy surgery’.53 The vast majority of the procedures were suboccipital ventriculgraphies, usually performed by A. Verjaal (1910–1973), the later Professor of Neurology in Leiden but then first assistant to Ledeboer, the remainder some 20–30 bi-occipital trepanations for direct puncture of the ventricles, performed by De Vet, Verjaal assisting. In 1942 the clinics in Heemstede closed and all patients returned home in order to prevent the German occupation forces and their Dutch collaborators to take over the management of the clinics. The St. Ursula clinic remained active. Occasional surgeries for epilepsy, either as the main symptom or as a secondary phenomenon, were also performed elsewhere since neurosurgical departments by this time also had been established in other university clinics in the Netherlands. In the Valerius Clinic, associated with the Free University of Amsterdam, general surgeon C. van Gelderen actually performed some interventions, including a tumor case with seizures, guided by some of the earliest electroencephalographic (EEG) recordings performed in the Netherlands.54 These early Dutch endeavors in the field of EEG by physicist L.J. Koopman, psychiatrist L.J. Franke, and physiologist J. ten Cate were discontinued, due to war conditions (Jonkman1). After the war the neurosurgical activities in Heemstede were resumed but according to the register it was not until 1949 that some real surgical intervention, other than diagnostic procedures was performed. In that year de Vet was joined by Otto Magnus, who, due to the vicissitudes of war had worked in Zurich with W.R. Hess (1881–1973), and then trained in Neurology in London. In 1947 De Vet had suggested that Magnus, rather than starting a residency in neurosurgery, should pursue his earlier neurophysiologic interest and acquaint himself with electroencephalography (EEG). Following two more years of training in Montreal with H. Jasper (1906–1999) and W. Penfield (1891–1976), Magnus returned and introduced EEG both in Wassenaar and in Heemstede. Magnus also introduced acute electrocorticography (ACoG) as a regular procedure for epilepsy surgery and according to the register, from June 1949 to September 1954 17 cortical excisions, guided by ACoG were performed, either by P. Hanraets, pupil and later associate of De Vet or by De Vet himself, who has his last entry on 23 September 1954. After that time no neurosurgical procedures were performed in Heemstede and on arrival of A.M. Lorentz de Haas (1911–1967) as successor to Ledeboer the operating room,
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which had remained in use for minor surgeries, was closed. All epilepsy surgery activities thus were moved to Wassenaar but Magnus remained head of the EEG department, both in Wassenaar and in Heemstede, acting as a liaison between the two clinics until 1968. In an early report, specifically mentioning epilepsy, De Vet reported 80 cases of epilepsy admitted to the clinic in Wassenaar between 1936 and 1938, 63 of them being symptomatic cases. No mention was made concerning number of surgeries or outcome.55 In 1949 he reported on 105 operated patients with a good outcome (comparable to Engel I and II) in 50%. Most patients had lesions. In 15 patients he removed small areas of normal looking cortex where seizures could be elicited and from those 15 only 4 had a satisfactory outcome.53 In 1962 Magnus compared the results of the first 45 procedures with ACoG with those of the earlier series and found them to be more or less equal56. In his last paper on the subject57 De Vet however emphasised the value of ACoG in cases of non-lesional temporal lobe epilepsy. From a total series of 213 patients, operated for epilepsy in the period 1936–1969, 78 could be identified with psychomotor epilepsy, where 33 of these turned out to have a lesion. From the remaining 45, all operated with the help of ACoG by Magnus, 18 became seizure free and another 13 showed major improvement, an outcome far superior to the 1949 results.53 In 1969 De Vet retired from the St. Ursula Clinic and after his departure the interest in epilepsy surgery quickly diminished. Only a few procedures were performed in the following years and in the new Westeinde Hospital in The Hague to which the neurological and neurosurgical departments were moved in 1979 no epilepsy surgery was performed any more. By this time however the torch had already been taken over by another team, already evident in De Vet’s 1972 paper57 where he discussed the options of stereotactic intracranial EEG investigations, advocated its application in cases of bitemporal lobe EEG foci and illustrated his point by an X-ray picture of a skull with multiple intracerebral and subdural electrodes, ‘Courtesy Prof. Dr. W. Storm van Leeuwen’. Consolidation: The Dutch Collaborative Epilepsy Surgery Programme Reference to stereotactic procedures had already been made by De Vet before. Like other neurosurgeons of the period he had been actively involved in psychosurgery and, well aware of the major drawbacks of both open or closed leucotomy techniques, he recognized the potential advances of multiple and successive microcoagulations, performed through chronic indwelling micro-electrodes, but considered the technique as yet insufficiently developed.58 By the time of his retirement this had changed. Willem Storm van Leeuwen (1912–2005) studied medicine in Leiden and specialized in physiology and neurophysiology with G. J. J. Rademaker (1887–1957). In 1945 he obtained his PhD on a thesis on cardiac arrhythmia, elicited by experimental injury of the central nervous system. Supported by a Rockefeller Fellowship he then spent some years in the UK with Lord Adrian in London and with W. Gray Walter in Bristol, where he obtained his training in EEG.59 On returning to the Netherlands Storm van Leeuwen was one of the driving forces behind the further development of clinical
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neurophysiology in the Netherlands. Following alternating appointments in Leiden and Utrecht he finally settled in Utrecht in 1959 as director of the department of clinical neurophysiology and of the department of brain research of the Medical Physical Institute (MFI) of the National Dutch organization for applied physical research (TNO). The fortuitous situation of clinical neurophysiologists such as Storm van Leeuwen, Magnus, and Portugese born Fernando Lopes da Silva, whom Storm van Leeuwen had brought to Holland from the UK, collaborating with physicists as Anton Kamp in Utrecht and Henk van der Tweel (1915–1997) in Amsterdam, resulted in major advances in recording techniques and equipment, innovative early methods of computer analysis, and the development of miniaturized radiotelemetry with depth electrodes which was to be decisive for the further development of psychosurgery and, in its wake, also of epilepsy surgery in the Netherlands. Following some pioneer stereotactic coagulation procedures by a group of Dutch and Belgian neurologists and neurosurgeons, including Arthur Sonnen (1932–2000) and Jan van Manen 60 in 1971, largely through an initiative of Harry Meinardi and the Dutch National Commission for Epilepsy Research (CLEO) a working group for neuro-physio-surgery was constituted to discuss all Dutch patients for whom psychosurgical interventions were considered.61 Medical, social and ethical impact of such interventions were considered to exceed the individual responsibility of individual doctors and requiring peer review and as such the working group, although initiated by some of the core members, soon obtained formal recognition by the Dutch health authorities. Storm van Leeuwen held the chair. Members were neurologists, psychiatrists, clinical neurophysiologists, and neurosurgeons actively involved in psychosurgery and came from different clinics in the Netherlands as well as from the Dutch speaking part of Belgium. Since gross leucotomy by that time was totally discredited the method of choice was chronic stereotaxic microcogulation as originally advocated by Crow et al.62 but employing the electrodes developed originally for animal experimentation by Kamp and Lopes da Silva. Since at the onset it was clear that evaluation of epileptic patients for possible surgery would require comparable electrode types and stereotactic techniques it was decided that the activities of the working group should also include epilepsy and that epileptologists should participate.61 Special multistranded depth electrodes and subdural wire and reed multi-electrodes were developed at MFI and a method was developed for the stereotactic implantation of two to six intracerebral electrodes, aimed at the hippocampus, amygdala and mesio-frontobasal cortex, combined with 8–16 narrow subdural reeds, guided by hand and fluoroscopy over wide areas of the lateral and basal frontal, temporal and centroparietal cortex of both hemispheres, all electrodes introduced through just two small bifrontal trephine holes63 (Figure 10.3). Although reaching fewer intracerebral sites than the orthogonal stereotactic approach, developed by Taillairach and Bancaud,63 the Dutch approach performed excellently64 and had the advantage of better access to the surface cortex bilaterally with less risk for intracerebral hemorrhage and with relatively minor surgical trauma, compared to the subdural strip and grid methods, developed shortly afterwards in the USA. All procedures, including those on patients from Belgium, were performed in Utrecht by neurosurgeon C.W.M van Veelen.
Figure 10.3 (a, b) Frontal and lateral scheme, drawn after postimplantation X-ray of a patient with bilateral subdural wire and reed electrodes (continuous lines) and four depth electrodes (dotted lines) in the mesilimbic structures, all electrodes implanted through small bifrontal trephine holes according to the method, developed by the group of Storm van Leeuwen, Lopes da Silva, and Van Veelen.62
Initially psychosurgery constituted the brunt of the working group’s activities. Although at the time of Storm van Leeuwen’s retirement in 1979 the number of such cases, was dwindling, the workgroup activities continued, stimulated by the arrival of C. D. Binnie, London and Cambridge trained clinical neurophysiologist, who in 1976 had taken up the position of director of the department of clinical neurophysiology at ‘Meer and Bosch’. There he had created the first telemetric long term EEG and video monitoring unit in the country
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The development of epilepsy surgery in the Netherlands and Belgium Dutch collaborative epilepsy surgery program 160 140 120 100 80 60 40 20 0 1973
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Figure 10.4 Dutch Collaborative Epilepsy Surgery Program activities 1973–2005: all patients A total of 1656 patients has been referred and evaluated resulting in 775 resections. 160 patients had intracranial recordings (135 bilateral or unilateral depth and subdural electrodes, 25 subdural grids).
where he could accommodate even depth implanted patients, who at that time could not be monitored in Utrecht.66 The emphasis now changed from psychiatry to epilepsy, at first still at a very low pace but, following the appointments, in 1985, of A. C. van Huffelen as successor of Storm van Leeuwen and of W. van Emde Boas on the position of Binnie, who returned to the UK, the program quickly expanded (Figure 10.4). In 1989–1990 Van Emde Boas spent 5 months for additional training with F. Andermann and P. Gloor (1923–2003) in Montreal and on his return in Heemstede expanded the capacity for presurgical evaluation by creating a new ‘nonhospital but home-like’ three bed epilepsy monitoring unit, where, weather permitting, patients, including those with implanted electrodes, could be recorded, even while sitting outside in the garden. Van Huffelen, at the same time, prepared a medical technology assessment project and obtained government funding for the period 1990–1992. The final report of this project, supervised by Van Huffelen, Van Veelen, and Van Emde Boas, was offered to the Dutch health authorities in 1993 and resulted in formal acceptance – and thus formal albeit hardly sufficient third-party payment – of epilepsy surgery, including the necessary presurgical evaluation for up to an initially 50 patient maximum per year, Utrecht Academic Hospital being the only recognized hospital allowed to perform these operations in close collaboration with the three specialized Dutch epilepsy centers. By that time the constitution and procedures of the working group had drastically changed. With monitoring facilities now also available in the Epilepsy Centers Kempenhaeghe in Heeze and the Dr. Hans Berger Clinic in Breda, more clinical neurophysiologists and neurologists attended the meetings in Utrecht together with the neuropsychologists, responsible for pre- and post-surgical assessment and the Intracarotid Sodium Amytal test.67 A second monthly meeting was organized in Heemstede for the clinical neurophysiologists only for a collective review of all the seizures, video and EEG, of the patients to be discussed in the next plenary session in Utrecht, where a brief summary would be presented. Other neurosurgeons joined van Veelen and pediatric epilepsy surgery,
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Figure 10.5 Dutch Collaborative Epilepsy Surgery Program activities 1973–2005: children, up to the age of 16 years. 357 children were referred of which 133 had surgery, with one exception all since 1990. Surgical procedures range from limited lesionectomies or partial resections to structural or functional hemispherectomies and a small number of anterior callosotomies.
already practiced on a limited scale, got a major impetus when O. van Nieuwenhuizen, shortly afterwards to be appointed professor of child neurology in Utrecht, joined the group in 1991 (Figure 10.5). Special MRI protocols were developed68 and PET and occasional SPECT studies69 were performed in selected patients, the former first in collaboration with the University clinic in Liege (Belgium)’ and later in the Free University in Amsterdam, where in 1997 Magneto Encephalography (MEG) also became available. After lifting of the earlier imposed restrictions the university hospitals of Maastricht and of the Free University in Amsterdam joined the workgroup activities in 1997 and 2002. While the number of referrals and surgeries steadily increased, until levelling off around 2002 (Figure 10.5) the number of intracranial investigations sharply dropped, then started to rise again following the introduction of Grids recordings in Utrecht under the supervision of Heemstede trained F. Leijten. Initially some Belgian patients continued to be referred to the Dutch program but this came to an end following the development of epilepsy surgery in Gent and elsewhere in Belgium. Collaboration between programs on both sides of the border continued however, notably in the field of research in addition to multiple contacts between the Dutch program (since renamed ‘National Working Group for Epilepsy Surgery’ [LWEC] within the Netherlands and ‘Dutch Collaborative Epilepsy Surgery Program’ [DCESP] for international purposes) and international circles. Members of the group actively participated in many international meetings and van Emde Boas and van Nieuwenhuizen acted as commission members for the commission on epilepsy surgery and the subcommission for pediatric epilepsy surgery of the International League Against Epilepsy. Between 1973 and 2005 775 patients had been operated, the last overall results (on 338 patients operated up to 1998) published by van Veelen in 2001.70 An overview of the papers published by participating workgroup members and associated research programs (Appendix) can be obtained through Pub Med.
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Vagal nerve stimulation never was part of the activities of the LWEC although some of the member epileptologists and surgeons were or are involved in early pilot studies and in the current multicenter program for a limited number of VNS implants per year, accepted by the health authorities and coordinated by G. Hageman (Enschede) for adults and M. Majoie (Heeze) for children. Growth of patient numbers and the increased complexity of presurgical work up of individual patients and of traffic in the densely populated Netherlands have made the process of regular, now two per month, general meetings in Heemstede and Utrecht an increasing burden on the participants and some members of the LWEC have advocated the creation of local teams, leaving only the most difficult cases for broad discussion in the central group. A team consisting of neurologists, neurophysiologists, neuropsychologists, and neurosurgeons from the University of Maastricht and Epilepsy Center Kempenhaeghe has started its activities in 2005, reviewing cases from the southern part of the Netherlands; the first resective procedures have recently been performed in Maastricht. However, it takes expertise also to recognize ‘easy cases’ inasmuch as these exist and the LWEC intends, with the development of teleconferencing techniques, to continue to monitor, coordinate, and guide all epilepsy surgery activities in the Netherlands.
Belgium At the end of the 16th century Jean Baptiste van Helmont (1577–1644), the founder of the Iatrochemical School, which looked to chemical explanations of vital phenomena, from Leuven, was the first to write about the underlying mechanism of epilepsy in the Low Countries. He attributed epilepsy to a dysfunction of the orifice of the stomach where a duumvirate of stomach and spleen was thought to regulate functions of life. However, he also acknowledged that seizures could be provoked by strong emotions affecting the sensitive soul.71 In modern times, it was only after 70 years of its independence from the Netherlands in 1830 that Belgium saw some early efforts in surgical treatment of patients with epilepsy. Crocq72 mentioned 13 mostly posttraumatic cases from nine authors in his 1902 review and in that same year Lowie from Eecloo reported another patient at a major Flemish meeting.73 Yet these activities, and comparable ones in the years to follow, remained isolated cases, performed by general surgeons and not incorporated in a structured program. The interest in neurosurgery and epilepsy in Belgium dates from immediately before the World War I. In 1905, Van Gehuchten began to film neurological and psychiatric patients, among some with epileptic fits; the original nitrate movies have survived and represent in fact the first Belgian films. The Great War, with 90% of the country under German occupation, represented a period of scientific stagnation. Only in Flanders Fields did some surgeons acquire great experience in traumatology. Noteworthy is the contribution by De Page who designed a special electromagnetic device used for removing deep seated shrapnel and bullets from the brain.74 As the capacity of (neuro)surgical care on the battlefield was very limited, the Belgian Red Cross called upon the services of Muskens from The Netherlands to help setting up a unit for central nervous
system war injuries in 1914. Immediately after the World War I, Paul Martin was the first Belgian surgeon who went to the USA for training in neurosurgery with Harvey Cushing and became head of the surgical laboratory at Harvard University. He later returned to Belgium to become the first professor of neurosurgery at the University of Brussels.74 In the meantime, Van Gehuchten had joined forces with Jean Morelle, a neurosurgeon who had also trained in the USA and set up a nucleus of neurosurgery within the general surgery department at Leuven. A similar attempt was made at the University of Liège, where Christophe, who had worked with Frazier, Adson and Cushing, became lecturer in neurosurgery in 1933, probably the first of his kind in Europe.74 However, the first independent neurosurgical departments were founded only after the World War II but initially there was no special interest for epilepsy surgery. In fact, specialized epilepsy care in Belgium as such did not start until in the fifties of the 20th century. In 1955 academical neuropsychiatrists from the Universities of Gent, Brussels, Leuven, and Liège and other interested professionals founded the Belgian National League against Epilepsy. The league has survived to date but currently serves as an umbrella organization of two active regional leagues (one Flemish-speaking and one French-speaking) reflecting the federal nature of the Belgian state. According to a review by Sorel, by the end of the fifties in-patient facilities for epilepsy patients were available in neurological departments of 59 hospitals throughout the country.75 In about 10 neurosurgical units nationwide occasional epilepsy surgery procedures were performed. In the late sixties and early seventies two institutions for residential care of refractory epilepsy patients were founded in Pulderbos and in Ottignies. Pulderbos, located in the Flemish-speaking part of the country, emerged from collaboration between the University Hospital of Leuven and a major health care provider. The ‘Centre Neurologique William Lennox’ was founded in 1972 and is associated with the French-speaking ‘Université Catholique de Louvain’. The first reports in the international peer-reviewed literature of epilepsy surgery in Belgium originate from Liège where in the mid-sixties A. Waltregny, a neurosurgeon and clinical neurophysiologist, performed experimental and human studies using invasive EEG recording based on the teachings of Gastaut and Bancaud in France.64,76 Relatively few resective procedures were performed, however, without further contributions to the international epilepsy surgery literature. Many patients eligible for surgery were referred to epilepsy surgery centers in France, The Netherlands, and Western Germany. In the beginning of the eighties P. Tugendhaft and J. Brotchi at Hôpital Erasme, an academical hospital associated with the French-speaking ‘Université Libre de Bruxelles’, performed a series of invasive EEG recordings using the methodology of Wyler from the USA. and initiated the first epilepsy surgery series in Belgium.77 Neuropsychological assessment and intracarotid amytal procedures were routinely performed. In 1990, the first comprehensive epilepsy surgery center in Belgium was established at Ghent University by P. Boon, and L. Calliauw, chair of neurosurgery at Ghent University Hospital. P. Boon, a neurologist and clinical neurophysiologist, trained at Winston-Salem, NC with Penry and at
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The development of epilepsy surgery in the Netherlands and Belgium Yale University with Williamson and Spencer. Soon E. Thiery, professor of neuropsychology at Ghent University and E. Achten, neuroradiologist at Ghent University Hospital, joined the team. Their collaboration resulted in the first multidisciplinary epilepsy surgery team in Belgium, evaluating and operating increasing numbers of patients and performing clinical research.78,79 The first combined placement of depth and subdural electrodes in patients requiring invasive EEG recording, the first implantation of a vagus nerve stimulator in Belgium, and the first long-term treatment with amygdalohippocampal deep brain stimulation for temporal lobe epilepsy in Europe were all performed by their team. Over time the group in Gent came to include K. Vonck, a neurologist with special expertise in neuromodulation and D. Van Roost, a functional neurosurgeon with longstanding experience in epilepsy surgery, who trained with the neurosurgical team of Schramm at Bonn University Hospital.80,81 At about the same time, the team from the ‘Université de Liège’ headed by G. Franck and B. Sadzot, who had trained in Baltimore, USA, established a positron emission tomography unit in which patients with refractory epilepsy were systematically investigated. Most of these patients were referred from the Dutch Collaborative Epilepsy Surgery Programme in Utrecht.69,82 In the late nineties W. Van Paesschen, a neurologist who trained with Duncan and his group in London and J. Van Loon, a neurosurgeon, started with presurgical evaluation and epilepsy surgery at the ‘Katholieke Universiteit Leuven’. Their group has a strong focus on non-invasive diagnostic tools such as ictal SPECT.83 This was quickly followed by similar initiatives to establish epilepsy surgery programs at the ‘Université de Liege’ (headed by B. Sadzot and T. Grisar), the ‘Cliniques Universitaires St-Luc’ in Brussels (headed by K. Van Rijckevorsel and C. Raftopoulos), and in the ‘Centrum voor Epilepsie en Psycho-organische Stoornissen’, a private initiative in Duffel (headed by R. Hauman). The already active programme at ‘Hôpital Erasme’, Bruxelles, now directed by B. Legros and P. Van Bogaert, during the same period expanded its activities. A major breakthrough in terms of acceptance by the health authorities and funding by the national reimbursement agency was the establishment of ‘Reference Centers for Refractory Epilepsy’ in 2000. Strict criteria were defined with regard to the necessary availability of technical infrastructure, human resources and neurological and neurosurgical expertise for academical centers to be recognized as a referral center for epilepsy surgery. The main purpose was to concentrate know-how in a limited number of centers, guarantee high quality standards and limit the costs. Only patients treated in such centers got reimbursement for presurgical evaluation and surgical procedures for refractory epilepsy. After an initial phase during which six centers were recognized in 2000, presently four Reference Centers for Refractory Epilepsy are active in Belgium: in Gent (Universitair Ziekenhuis Gent), Leuven (Universitair Ziekenhuis Gasthuisberg), and two in Brussels (Hôpital Erasme, Cliniques Universitaires St-Luc). All have dedicated epilepsy surgery teams and follow a similar presugical evaluation protocol. In each center, video-EEG monitoring, 1.5T or 3T optimum MRI facilities, PET, SPECT, and neuropsychological assessment are
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available. Biannually, in each center quality and performance parameters are assessed by the national reimbursement agency. In 2003–2004, 300 patients annually underwent presurgical evaluation (including invasive video-EEG monitoring in 20 patients) resulting in 70 resective procedures and 60 implantations of a vagus nerve stimulator in patients who were not eligible for resective surgery. Presurgical evaluation and epilepsy surgery are a strong impetus for performing clinical and experimental research. Epilepsy research in Belgium has basically followed the same timelines as the clinical development of epilepsy care described above. While scientific reports on epilepsy surgery related work were scarce until the 1980s, clinical researchers from Gent, Leuven, Bruxelles, Louvain and Liège have been increasingly active. Among the most published topics in the past 15 years are EEG source localization (Gent), optimal structural magnetic resonance imaging (Gent, Leuven), functional magnetic resonance imaging (Gent), PET (Liège), ictal SPECT (Leuven), magnetoencephalography (Gent), seizure anticipation (Gent, Leuven), antiepileptic drug research (all centers), vagus nerve stimulation (Gent), and deep brain stimulation (Gent, Bruxelles).80–89 The groups from Gent and Liège have experimental animal facilities providing many relevant epilepsy animal models and they are active in the field of basic neurophysiology, neurostimulation and stem cell applications in epilepsy.90–93
Appendix: Core membersa of the Dutch Collaborative Epilepsy Surgery Program workgroup 1980–2005 Secretariat and logistic coordination E. van Wijk-Leenaars5 Clinical Neurophysiology / Epileptology C.D. Binnie,1* M. Bourez-Swart,5 G.J.F. Brekelmans,1* S. Claus1, A. Colon,3 W. van Emde Boas1 (Chair 2003–present), J. Parra Gomez1, A.C. van Huffelen5, J. Jonkman*, V. van KranenMastenbroek7, F. Leijten5, W. v.d. Meij5*, J. Overweg1* (Chair 1990–1998), L. Reebok4, H.E. Ronner6, A.E.H. Sonnen4†, W. ter Spill4*, C.J. Stam6, D.N. Velis1, E. Veltman3 (Chair 1999–2002), P.H.A. Voskuil4*, L. Wagner4, A.W. de Weerd2, A. van Wieringen1* Neurology / Epileptology J. Bruens,4† R.M.C. Debets,1 A. Elderson5*, M.C.T.F.M de Krom7, H. van Lambalgen2, J. van Manen* (Chair 1980–1989), H. Meinardi1*, Th. Rentmeester3*, F.B.J. Scholtes4*, R.T.M. Starrenburg3*
a Many persons have occasionally attended the meetings as guest or as short term participants. In this list only those that have been actively involved for the whole period or major lengths of time are listed. The members of the still existing subgroup for psychosurgery are not mentioned. For a list of members of the original group 1971–1979 see reference 61. * Past member.
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Paediatric Neurology O. van Nieuwenhuizen,5 W.O. Renier* Neurosurgery H. Baaijen,6 J. Dings,7 P. Gosselaar5, G. van Overbeke5*, P. van Rijen5, C.W.M. van Veelen5*, V. Visser-Vandewalle7 Neuropsychology W.C. Alpherts,1 M.L. Franken3*, M.P. Hendriks3, A. Jennekens-Schinkel5*, M. Klein6, J. Vermeulen1 Neuroradiology L.C. Meiners,5* G.A.de Kort5, L.M. Ramos5*, T.D. Witkamp5* Psychiatry W.P. Haaijman*
Research associates A.P. Aldenkamp,2 J.Arends,2 E. Arronica9, P.A.J.M. Boon2, A.van Dieren5, B.W. van Dijk6, W.H. Gispen8, J.A. Gorter9, P.N. de Graan8, M. v.d. Heide1, G. Hoogland8, G.J. Huiskamp8, F. Jansen5, S. Kalitzin1, F. H. Lopes da Silva9, H. Meeren6, J. C. de Munck6, P. Ossenblok2, E.A. Proper8, J.P. Pijn1 †, N. Ramsey5, G.J. Rutten5, P. Suffczinski1, D. Troost9, M. Vreugdenhil9, W. J. Wadman9 Participating Hospitals 1 Epilepsy Centre Meer and Bosch; SEIN, Heemstede, 2Epilepsy Centre Heemstaete; SEIN, Zwolle, 3Epilepsy Centre Kempenhaeghe, Heeze, 4Epilepsy Centre Dr. H. Berger kliniek, Breda, 5University Medical Centre Utrecht, 6Free University Medical Centre Amsterdam, 7Academic Hospital Maastricht Main Associated research groups 8 Rudolf Magnus Institute of Neuroscience, Utrecht, 9 Swammerdam Inst. of Life Science, Amsterdam
REFERENCES 1. References in the text almost exclusively refer to original publications. For all Dutch historical and biographical data without specific references the source is: Frederiks JAM, Bruyn GW, Eling P, eds: History of Neurology in the Netherlands. Boom: Amsterdam, 2002. From this book notably the following chapters were consulted: Chapter 3. Koehler PJ, The Extra-Academic Centres, 37–51; Chapter 7. Alphen HAM van, Neurosurgery, 93–121; Chapter 11. Jonkman EJ, Clinical Neurophysiology, 193–215; Chapter 13. Meinardi H, Epileptology, 221–40; Chapter 19. Bruyn GW, Koehler PJ, B. Brouwer 1881–1949, 299–308; Chapter 27. Bruyn RPM, Bruyn, GW, C. T. van Valkenburg 1872–1962, 367–76; Chapter 29. Bruyn RPM, J. K. A. Wertheim Salomonson 1864–1922, 387–92; Chapter 30. Koehler, PJ: C. Winkler, 1855–1941, 393–401. For the sections concerning the post World War II developments and the period of the Dutch Collaborative Epilepsy Surgery Program, moreover, use was made of personal communications of O. Magnus, C. W. M. van Veelen, A. C. van Huffelen, E. van WijkLeenaars, H. Meinardi, F. Lopes da Silva, and A. W. de Weerd and of the private archive of DCESP and other documents of WvEB. 2. Tilanus JWR. Overzicht over de ontwikkeling der chirurgie in de laatste 30 jaren. Ned Tijdschr v Geneesk 1882-II; 26:214–19. 3. Winkler C, Rotgans J. [L’etat actuel de la chirurgie nerveuse] Pays Bas. In: Chipault A ed: L’Etat Actuel de la Chirurgie Nerveuse Vol I, 658–755. Rueff: Paris, 1902 (Preprint: No place, 1901 pp 1–98; Reprint: Winkler C: Opera Omnia Vol. 3 549–640. Bohn: Haarlem, 1918). 4. Mesdag MJ. Bibliographie van de werken van Nederlandse schrijvers op het gebied van de neurologie en psychiatrie en aanverwante vakken. Vol.II, systematisch gedeelte. No Publisher [Amsterdam University Clinic of Psychiatry and Neurology]: Amsterdam, 1923. 5. Winkler C. Herinneringen. Van Loghum Slaterus: Arnhem, 1947 (Reprint: Bohn: Scheltema & Holkema, Utrecht, 1982). 6. Winkler, C. Bijdrage tot de Hersen-Chirurgie uit de Diaconesseninrichting te Utrecht. II: Tumoren. Ned Tijdschr v Geneesk 1891I;35:371–418 (Reprint: Winkler C. Opera Omnia Vol 2, 33–77. Bohn: Haarlem, 1918. 7. Guldenarm JA, Huysman J, Winkler C: Bijdrage tot de HersenChirurgie uit de Diaconessen-Inrichting te Utrecht. Ned. Tijdschr v Geneesk 1890-I;34:657–64 (Reprint: Winkler C. Opera Omnia Vol 2, 3–11. Bohn: Haarlem, 1918). 8. Guldenarm JA, Winkler C. Bijdrage tot de Hersen-Chirurgie uit de Diaconessen-inrichting te Utrecht. III: Cerebrale verschijnselen na een trauma van den schedel. Ned Tijdschr v Geneesk 1891II;35:217–30 (Reprint: Winkler C: Opera Omnia Vol 2, 78–89. Bohn: Haarlem, 1918).
9. Winkler C. Bijdrage tot de Hersen-Chirurgie uit de Diaconesseninrichting te Utrecht IV: Siphylitische tumoren, diffuse gliomata en gliosarcomata, tumoren ontstaan na schedeltraumata, cysten en verkalkingen. Ned Tijdschr v Geneesk 1893-I;37:209–254 (Reprint: Winkler C. Opera Omnia Vol 2, 203–241. Bohn: Haarlem, 1918). 10. Buringh Boekhoudt H. Bijdrage tot de Hersen-Chirurgie uit de Diaconessen-inrichting te Utrecht V: Haematoma Durae Matris. Ned Tijdschr v Geneesk 1893-I;37:309–14. 11. Winkler C. L’intervention chirurgicale dans les epilepsies. Bohn: Haarlem et O. Doin: Paris, 1897 (Reprint: Winkler C: Opera Omnia Vol 3, 95–155. Bohn: Haarlem, 1918). 12. Lens PCTh. Trepanation in einem Falle Jacksonischer Epilepsie [thesis] Giessen, 1891. 13. Hermanides RS. Operatieve behandeling van Hersengezwellen [thesis] J.v. Boekhoven: Utrecht, 1894. 14. Hermanides RS: Operatief behandelde hersengezwellen. Ned Tijdschr v Geneesk 1895-I;39:302–18. 15. Winkler C. Een proeve om met behulp van driehoeksmeting de betrekkelijke ligging der windingen en sleuven van de groote hersenen tegenover de door huid bedekte schedeloppervlakte te bepalen. Ned Tijdschr v Geneesk 1892-II;36:158–73 (Reprint: Winkler C. Opera Omnia Vol 2, 97–115. Bohn: Haarlem, 1918). 16. Winkler C. Over hersenchirurgie. De Gids 1895;59:58ff (Reprint: Winkler C. Opera Omnia Vol 2, 309–33. Bohn: Haarlem, 1918). 17. Brekelmans GJF. Clinical Neurophysiology in the Presurgical Evaluation of Patients with Intractable Epilepsy [thesis]. Utrecht, 1999. 18. Eyk HH van. Partieele epilepsie en hare heelkundige behandeling [thesis], Van Heteren: Amsterdam, 1897. 19. Chipault A. France. In: Chipault A, ed: L’Etat Actuel de la Chirurgie Nerveuse Vol I, 84–92. Rueff: Paris, 1902. 20. Wertheim Salomonson J. Particuliere correspondentie. Ned Tijdschr v Geneesk 1898-I;42:190–9. 21. Rutgers M. XXVIII Congres van het Duitsche Gezelschap voor Chirurgie te Berlijn. Ned Tijdschr v Geneesk 1899-I;43:647–50. 22. Boks DB. 29ste Congres van de Deutsche Gesellschaft f¸r Chirurgie. Ned Tijdschr v Geneesk 1900-I;44:1090–6. 23. Boks DB. Operatieve behandeling van Epilepsie. Ned Tijdschr v Geneesk 1900-I;44:768–79. 24. Indemans JWM. Twee gevallen van partieele epilepsie van Jackson. Ned Tijdschr v Geneesk 1903-II;47:659–69. 25. Iterson JE van: De ontwikkeling der heelkunde. Ned Tijdschr v Geneesk 1899-II;43:87–94. 26. Eling P, Keyser A: Louis Muskens: a leading figure in the history of Dutch and World epileptology. J Hist Neurosci 2003; 12:276–85.
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The development of epilepsy surgery in the Netherlands and Belgium 27. Muskens LJJ. Neurologie en Neurochirurgie. Psychiat Neurol Bladen 1915;19:492–9. 28. Muskens LJJ. Psychiatrie, Neurologie und Neuro-Chirurgie. Monatschr Psychiat Neurol 1915;37:374–80. 29. Muskens LJJ. International League Against Epilepsy in war and postwar time. Epilepsia 1937;1(2nd series); 14–22. 30. Muskens LJJ. Epilepsie: vergelijkende pathogenese, verschijnselen, behandeling. Van Rossen: Amsterdam, 1924 (German edition: Epilepsie: vergleichende Pathogenese, Erscheinungen, Behandlung. Springer: Berlin, 1926; English edition: Epilepsy: Comparative Pathogenesis, Symptoms, Treatment. London; Ballière, Tyndall and Cox, 1928. 31. Muskens LJJ. Das supra-vestibuläre System bei den Tieren und beim Menschen. Noord Holland: Amsterdam, 1935. 32. Muskens LJJ. De ontwikkeling van het specialisme in de geneeskunde. [Public lecture, University of Amsterdam] Bohn: Haarlem, 1906. 33. Muskens LJJ. Mededeelingen omtrent de heelkunde van het centrale zenuwstelsel. I. Een betrekkelijk gevaarlooze techniek van heelkundig onderzoek der hersenen. Ned Tijdschr v Geneesk 1911-II;55:983–1002. 34. Muskens LJJ. Mededeelingen omtrent de heelkunde van het centrale zenuwstelsel. II. Ruggemergoperaties. Ned Tijdschr v Geneesk 1911-II;55:1053–63. 35. Muskens, LJJ. Mededeelingen omtrent hersenchirurgie. III. Het segmentaal beginsel in de gevoelsprojectie op de hersenschors. Ned Tijdschr v Geneesk 1912-I;56:70–85. 36. Muskens, LJJ. Mededeelingen omtrent de heelkunde van het centrale zenuwstelsel. IV. Uitkomsten van inwendige en heelkundige behandeling van traumatische epilepsie. Ned Tijdschr v Geneesk 1912-I;56:366–76. 37. Korteweg JA. Eenige opmerkingen over: Mededelingen, enz. door Dr. L.J.J. Muskens. Ned Tijdschr v Geneesk 1911-II;55:1134–8. 38. Muskens, LJJ. Antwoord op prof. Korteweg’s artikel. Ned Tijdschr v Geneesk 1912-I;56:85–6. 39. Korteweg, JA. Wederwoord op Muskens’ antwoord. Ned Tijdschr v Geneesk 1912-I;56:184–5. 40. Londen DM. Het segmentaal beginsel in de gevoelsprojectie op de hersenschors. Ned Tijdschr v Geneesk 1912-I;56:185–6. 41. Muskens, LJJ. Antwoord aan de Heeren Korteweg en Van Londen. Ned Tijdschr v Geneesk 1912-I;56:259–60. 42. Korteweg JA. Wederwoord op Dr. Muskens’antwoord. Ned Tijdschr v Geneesk 1912-I;56:317. 43. Burger H. Wederwoord op Dr. Muskens’antwoord. Ned Tijdschr v Geneesk 1912-I;56:317. 44. Scheer WM van der (minutes). Voordrachten-Vergadering der Nederlandsche Vereeniging voor Psychiatrie en Neurologie, 25 Juni 1916. Psych Neurol Bladen 1916;20:543–66. 45. Muskens LJJ. Brief uit Antwerpen. Ned Tijdschr v Geneesk 1914II;58:1006–8. 46. Valkenburg, CT van. ‘Sensibele punten’ op de schors der groote hersenen van den mensch. Ned Tijdschr v Geneesk 1914I;58:2142–54. 47. Valkenburg, CT van. Plaatselijke hersenvliesaandoening, haar diagnose en heelkundige behandeling. Ned Tijdschr v Geneesk 1915I;59:2055–67. 48. Valkenburg, CT van. Een dubbele vertegenwoordiging van het gevoel op de schors der menschelijke groote hersenen. Ned Tijdschr v Geneesk 1916-I;60:2181–92. 49. Vet, AC de. Over de diagnostiek van het meningeoma cerebri. [thesis], Scheltema & Holkema: Amsterdam, 1936. 50. Vet, AC de. Een glasmodel van het cerebrale ventrikelsysteem. Ned Tijdschr v Geneesk 1940-I;84:2034–36. 51. Vet AC de. Translucent model of the cerebral ventricular system. J Neurosurg 1951;7:454–5. 52. Operatieregister Koningin Emma Kliniek 1938–1956 [register of surgeries] manuscript. Historical Collection Stichting Epilepsie Instellingen Nederland, Heemstede, the Netherlands. 53. Vet AC de. Neurosurgical diagnosis and therapy of epilepsy. Fol Psychiat Neurol Neurochir Neerl 1949;52:59–71. 54. Gelderen C van. Hersengezwel en electrencephalogram, Ned Tijdschr v Geneesk 1941-II;85:3605–8. 55. Vet, AC de. Neurochirurgie en epilepsie. Annalen 1939;31:134–43. 56. Magnus O, de Vet AC, van der Marel A, Meyer E. Electrocorticography during operations for partial epilepsy. Develop Med Child Neurol 1962;4:35–48. 57. Vet AC de: Temporal Epilepsy, c.q. Psychomotor Epilepsy. Experiences and present-day conceptions. Arch Suisses Neurol Neurochir Psychiat 1972;111:453–61. 58. Vet AC de, Leyten AMJ: De betekenis van de leucotomie. Ned. Tijdschr. v. Geneesk 1963-I;107:447–456.
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59. Huffelen AC van, Lopes da Silva FH, Donker DNJ: In memoriam prof. dr. W. Storm van Leeuwen. Ned Tijdschr v Geneesk 2006;150:110. 60. A.E.H. Sonnen, Jan van Manen and B. van Dijk: Results of Amygdalotomy and Fornicotomy in Temporal Lobe Epilepsy and Behaviour Disorders. Acta Neurochirurgica (1976), suppl. 23: 215–19. 61. Storm van Leeuwen W: Neuro-Physio-Surgery in the Netherlands Since 1971. Acta Neurochir 1982;61:249–56. 62. Crow HJ, Cooper R, Phillips DG. Controlled multifocal frontal leucotomy for psychiatric illness. J Neurol Neurosurg Psychiat 1961;24:353–60. 63. Veelen CWM van, Debets RMC, van Huffelen AC et al. Combined use of subdural and intracerebral electrodes in preoperative evaluation of epilepsy. Neurosurgery 1990;26:93–101. 64. Bancaud J, Talairach J, Bonis A. La stéréo- électroencéphalographie dans l’épilepsie. Informations neurophysiopathologiques apportées par l’investigation fonctionelle stéreotactique. Paris: Masson, 1965. 65. Brekelmans GJF, van Emde Boas W, Velis, DN et al. Additional value of the use of combined versus subdural or intracerebral electrodes alone in presurgical focus localisation. Epilepsia 1998;39:1290–301. 66. Binnie CD, Rowan AJ, Overweg J et al. Telemetric EEG and video monitoring in epilepsy Neurology 1981;31:298–303. 67. Alpherts WCJ. Neuropsychological Aspects of Epilepsy Surgery. [thesis], Utrecht, 2003. 68. Meiners LC. The Role of MR in Drug Resistant Epilepsy with Special Emphasis on Mesial Temporal Sclerosis [thesis], Utrecht; 1997. 69. Huffelen AC, van Isselt JW, van Veelen CWM et al. Identification of the side of epileptic focus with 123 I-iomazenil SPECT. A comparison with 18 FDG-PET and ictal EEG findings in patients with medically intractable complex partial seizures. Acta Neurochir (Wien) 1990;50(suppl): 95–9. 70. Veelen CWM van, van Rijen PC, Debets, RMC et al. Het Nederlandse epilepsiechirurgieprogramma: aanvalsreductie, operatieve complicaties en vermindering van medicatie bij 338 patiënten. Ned Tijdschr v. Geneesk 2001;145: 2223–8. 71. Haas LF. Jean Baptiste van Helmont. J. Neurol Neurosurg Psychiatry 1998;65:916. 72. Crocq J. Belgique. I. Etude Générale. In: Chipault A ed.: L’Etat Actuel de la Chirurgie Nerveuse, Vol I, 543–649. Paris: Rueff, 1902. 73. Zwaardemaker H, Muntendam, P. Zesde Vlaamsche natuur- en geneeskundig congres. Ned Tijdschr vvGeneesk 1902-II;46:807–21. 74. Calliauw L. Neurosurgery in Belgium. Acta Neurochir 2001; 143:273–5. 75. Sorel L. Review of social and medical services for epileptic patients in Belgium. Epilepsia 1963;4:167–78. 76. Bancaud J, Talairach J, Waltregny P et al. Stimulation of focal cortical epilepsies by megimide in topographic diagnosis.Clinical EEG and SEEG study. Rev Neurol (Paris) 1968;119:320–5. 77. Vanbogaert P, Massager N, Tugendhaft P et al. Statistical parametric mapping of regional glucose metabolism in mesial temporal lobe epilepsy. Neuroimage 2000;12:129–38. 78. Boon P, Calliauw L, Vandekerckhove T et al. Epilepsy surgery in Belgium: the Flemish experience. Acta Neurol Belg 1996;96:6–18. 79. Boon P, Vandekerckhove T, Achten E et al. Epilepsy surgery in Belgium, the experience in Gent. Acta Neurol Belg 1999;99:256–65. 80. Vonck K, Boon P, D’Have M et al. Long-term results of vagus nerve stimulation in refractory epilepsy. Seizure 1999;8:328–334. 81. Vonck K, Boon P, Achten E et al. Long-term amygdalohippocampal stimulation for refractory temporal lobe epilepsy. Ann Neurol 2002;52:556–65. 82. Sadzot B, Debets RM, Maquet P et al. Regional brain glucose metabolism in patients with complex partial seizures investigated by intracranial EEG. Epilepsy Res 1992;12:121–9. 83. Van Paesschen W, Dupont P, Van Driel G et al. SPECT perfusion changes during complex partial seizures in patients with hippocampal sclerosis. Brain 2003;128:1103–11. 84. Boon P, D’Have M, Adam C et al. Dipole modelling in epilepsy surgery candidates. Epilepsia 1997;38:208–18. 85. Achten E, Boon P, De Poorter J et al. An MR protocol for presurgical evaluation of patients with complex partial seizures of temporal lobe origin. AJNR 1995;16:1201–13. 86. Deblaere K, Backes W, Hofman P et al. Developing a comprehensive presurgical functional MRI protocol for patients with intractable temporal lobe epilepsy. Neuroradiology 2002;44:667–73. 87. LeVan Quen M, Martinerie J, Navarro V et al. Anticipation of epileptic seizures from standard EEG recordings. Lancet 2001;357: 183–8.
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88. Ossenblok P, Leijten F, de Munck, J et al. Magnetic source imaging contributes to the presurgical identification of sensorimotor cortex in patients with frontal lobe epilepsy. Clin Neurophysiol 2003;114:221–32. 89. Van Rijckevorsel K, Abu Serieh B, de Tourtchaninoff M, Raftopoulos C. Deep EEG recordings of the mammillary body in epilepsy patients. Epilepsia 2005;46:781–5. 90. DeSmedt T, Vonck K, Raedt R et al. Rapid kindling in preclinical anti-epileptic drug development: the effect of levetiracetam. Epilepsy Res 2005;67:109–16.
91. Van Hese P, Martens JP, Boon P et al. Detection of spike and wave discharges in the cortical EEG of Genetic Absence Epilepsy Rats from Strasbourg. Phys Med Biol 2003;48:1685–700. 92. De Deurwaerdere S, Vonck K, Van Hese, P et al. The acute and chronic effect of vagus nerve stimulation in Genetic Absence Epilepsy Rats from Strasbourg (GAERS). Epilepsia 2005;46 (suppl 5): 94–7. 93. Lakaye B, De Borman B, Minet A et al. Increased expression of mRNA encoding ferritin heavy chain in brain structures of a rat model of absence epilepsy. Exp Neurol 2000;162:112–20.
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History of epilepsy surgery in the Middle- and East-European countries and Russia P Halász
Epilepsy surgery in the Middle- and East-European region and in Russia developed under the influence of the USA and of the French schools. In the majority of countries a strong neurosurgical school developed at the beginning of the 20th century, and epilepsy surgery was built up with a more or less delay on a double basis: on classical neurosurgery and on independently developing clinical neurophysiology. The two disciplines have been amalgamated by the emerging clinical epileptological knowledge throughout the world in the multidisciplinatory assessment of epilepsy surgery. In these countries the development of epilepsy surgery was severely hindered by the information blockade due to the realm of the antidemocratic political power and to the delayed application of the contemporary neuroimaging techniques due to economical reasons. Presently the development of epilepsy surgery practice reached the international standards of leading centers in the world in Poland, Czech Republic and Hungary.
Poland In the second half of the 19th century surgical treatment was directed to vascular surgery, mainly on the sympathetic system, according to the theory that the disturbance in blood supply, especially vasospasm, was the direct cause of the epileptic seizure. R. Baracz in 1888 and 1893 published papers ‘On the ligation and resection of the vertebral arteries and the resection of sympathetic nerve for treatment of spontaneous epilepsy’. In the same year (1893) J. Bogdanik published a similar paper ‘On the resection of sympathetic nerve in treatment of spontaneous epilepsy’ and found improvement after such operations. Later on this procedure was applied by Raum and others as well. Later it was held that epilepsy is the consequence of the collection of cerebrospinal fluid on the surface of the brain in various kinds of cysts and can be treated by trephination and decompression. Decompressive trephinations were used by Baracz in 1890, Krajewski in 1894 and 1899, Schramm in 1899, and Raum in 1900. A. Domaszewicz and J. Zaczek published the paper (1922): ‘On the surgical treatment of epilepsy with personal experience’ describing the operative findings and the results of the decompressive craniotomy. Founder of the modern Polish neurosurgery was Jerzy Choróbski (1903–1986), head of the Department of
Neurosurgery in Warsawa. He was Penfield’s pupil spending several years working with him and started neurosurgery in Poland in 1935. At the beginning, during World War II and directly after, he performed several procedures for removing brain scars in cases of posttraumatic epilepsy, so important at that time. As soon as conditions after the war allowed and necessary equipment was obtained, among others EEG apparatus, he carried out the first surgery of focal, cryptogenic epilepsy on 27 November 1957 by temporal lobectomy. Diagnosis was derived from the clinical picture, PEG, EEG, and was proved intraoperatively by electrocorticography and brain electrostimulation. Later Choróbski was doing mostly temporal resections or, in special cases, hemispherectomy. The epilepsy surgery team included L. Ste˛ pie n´ and J. Bidzinski ´ (neurosurgery), T. Bacia (electrophysiology), all trained at the Montreal Neurological Institute and J. Wislawski (neuropathology). After Choróbski’s retirement, the next head of the Department, Lucjan Ste˛ pien, ´ continued this work with the above mentioned co-workers. Anatomical hemispherectomy was replaced by functional hemispherectomy. Extensive electrophysiological non-invasive investigations included various pharmacological activations and whole night physiological sleep. New diagnostic methods were consequently introduced: the Wada test (1960), psychological examination, invasive diagnosis as stereotactically implanted chronic electrodes, chronic epi- and subdural electrodes (Bidzinski ´ and Bacia in 1974). PEG was replaced by CT and NMR, and isotope studies were introduced. The results of their work were published in several publications with very long followup of several hundred patients and presented at international meetings. Beyond resective surgery, other methods, such as stereotactic lesions (amygdala, Forel’s field, Bidzinski ´ in 1981) and cerebellar electrostimulation (Bidzinski and Bacia in 1981) were tried with questionable results. The Next head of the Department, J. Bidzinski, continued epilepsy surgery and introduced anterior callosotomy and vagal nerve stimulation in Poland (1990). The present head of the Department, Prof. A Marchel with co-worker A. Rysz, are continuing the tradition of epilepsy surgery in this department with electrophysiology. As the surgical treatment of epilepsy became more popular, new neurosurgical centers started to offer surgical treatment. E. Mempel in Warsawa for many years did stereotactic 97
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amygdalotomy in patients with emotional disturbances in epilepsy and introduced acute stereoEEG in 1968. Since 1961, Z. Huber in Pozna n´ has performed several temporal lobectomies in adults and recently in children. Specially important was the establishment of an epilepsy surgery center for children at the Children’s Hospital, Mother Health Center in Warsawa, in 1995 (head, M. Roszkowski.), and at the Children’s Hospital in Lodz, in 2001 (head, L. Polis). In these centers children are treated up to 16 years of age. Recently two more neurosurgical departments joined the centers doing epilepsy surgery: in 2002 the Department of Neurosurgery in the Ministry of Administration Hospital in Warsawa (head W. Maksymowicz) and in 2004 the Department of Children’s Neurosurgery Medical University in Katowice (head M. Mandela).
Russia Epilepsy surgery in Russia and the former Soviet Union dates back to the end of the 19th and the beginning of the 20th centuries. In his ‘clinical lectures’ published in St Petersburg in 1898, A. Tauberg described cases of surgical treatment of ‘cortical epilepsy’ after brain trauma. F. Rein (1897) published a paper ‘Results and indications for the surgical tratment of Jacksonian epilepsy’. V. A. Muratov considered Jacksonian type seizures to be the indication to surgery. S. Timopheev (1913) and L. Pusepp (1919) reported long-term follow up of patients operated because of ‘Jacksonian epilepsy’. There were also several attempts to treat non-focal epilepsies surgically at that time. Various types of operations has been suggested, including operations on the autonomic nervous system. Later the idea of surgical treatment of focal epilepsies was supported by the famous Russian neurosurgeon N. Burdenko. Since the middle of 20th century epilepsy surgery has been developed in several regions of the Soviet Union: in St Petersburg Bechterewa, in Tbilis, Georgia (P. Saragishvily and P Chencheli), in Kiev, Ukraine (A. RomodanovÍ), in Sverdlovsk (now Ekaterinburg) (D. Shefer), and in Omsk (Yu. Savchenko). Stereotactic methodology of the Paris school was the basis of surgical interventions in these centers. Several papers and books dedicated to epilepsy surgery have been published in the Russian language by the above-mentioned authors. Presently in Russia, epilepsy surgery is being performed in St Petersburg (V. Bernsev), Ekaterinburg (A. Shershever), Viatka (B. Bein), and Omsk (A. Savchenko) on a considerable number of patients. The basic diagnostic disciplines, the diagnostic system used, the participation of neuroimaging methods in the presurgical procedure are deviating in several aspects from the contemporary European and USA epileptological standards. Evidence based evaluation of the results have so far not been published. Five years ago a joint surgery program was established in Moscow between the Department of Neurology and Neurosurgery of the Russian State Medical University and the Institute of Neurosurgery, based on a multidisciplinary team. This team decided to join to the contemporary epilepsy surgery programs in Europe using the same standards, evaluation and surgical methods. More than 400 patients have been
evaluated and from them 58 patients selected for presurgical evaluation, 30 patients were operated, mainly on the temporal lobe, with good results.
Romania The founder of Romanian neurosurgery was Prof. Dimitrie Bagdasar, trained in Prof. Cushing’s Department in Boston, and the first dedicated neurosurgical department in Bucharest was founded by him in 1935. His follower Prof C. Arseni was the next determining leader in neurosurgery until 1989. The modern era of Romanian neurosurgery was introduced by Prof. Al. Constantinovici and later by Prof. A.V. Ciurea. In 1993, a large neurosurgical hospital was established in Bucharest, named ‘Bagdasar-Arseni’, having departments for general neurosurgery, pediatric nerosurgery, spine neurosurgery, and adult neurosurgery. In March 2005 a neuroimaging department was added. Epilepsy surgery is still restricted to resective procedures of standard temporal lobectomies (3–4 yearly), a few tailored temporal surgical procedures (5–7 yearly) and 3–4 extratemporal resections yearly, in the last three years. Within this hospital a multidisciplinary team is starting to perform epilepsy surgery together with the Romanian National Reference Center of ILAE ruled by Dr. R. Rogozea. They are equipped with video-EEG, SPECT, and 1.5 Tesla MRI, using special ‘epilepsy protocols’, they recently introduced cortical mapping by subdural electrodes, and transcranial magnetic stimulation. They do not have as yet PET, fMRI, or MEG.
Czech Republic Epilepsy surgery in the Czech Republic (at that time part of Czechoslovakia) started in departments of neurosurgery of Medical Faculties of Charles University in Prague and Hradec Králové. Since 1956 patients with epilepsy were operated in the Department of Neurosurgery of Faculty of General Medicine of Charles University and the Military Hospital in Prague. There were two young associate profesˇ sors (Sourek and Vladyka) deeply interested in epilepsy. At first they performed excisions of cortical foci and temporal lobe resections. Stereotaxic operations were introduced later. At the beginning surgery was performed only in patients with intractable epilepsy lasting for tens of years. Therefore the number of successful outcomes was relatively low but it increased with the shift to patients with a shorter history of ˇ therapy resistant epilepsy. Sourek and Vladyka introduced a method of local cooling of the temporal lobe with the aim to open the blood–brain barrier and then apply intravenously a bolus of an antiepileptic drug. Until 1974 they used this method on 71 patients and approximately 25% of them remained seizure free, unsuccessful operations also represented 27% of patients and the remaining patients exhibited different degrees of improvement. The number of neurosurgery departments interested in epilepsy progressively increased so that there are at present at least seven departments performing more or less frequent
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History of epilepsy surgery in the Middle- and East-European countries and Russia epileptosurgical operations (Prague, Brno, Hradec Králové, Plzen, ˇ and Olomouc). Modern techniques, including video-EEG studies and intracranial explorations, were introduced during the 1990s. The Homolka Center in Prague had been educated primarily in English-speaking countries, and subdural recordings were the dominant method of invasive explorations (62%). The Epilepsy Center Brno was based on the model of a French school using the stereo-EEG method when invasive intracranial detection was necessary (92%). A recent analysis of the surgical results of the two centers in 248 adult patients with post-surgical follow-up of at least two years displayed Engel I in 58.9%, Engel II in 15.5%, Engel III in 13.3%, and Engel IV and V in 11.3%.
Turkey2–6 Epilepsy surgery has a relatively long history in Turkey although a modern teamwork approach was started during 1990s. Prof. Kenan Tukel (Figure 11.1) who was a pupil of Penfield and Jasper in the Montreal Neurological Institute established the first EEG lab in the early 1950s in Istanbul University. However, the first case report related to epilepsy surgery was published from Hacettepe University Medical Faculty, Ankara in 1960 by V. Turkmen and A. Erbengi. It was about a patient with infantile hemiplegia operated by hemispherectomy. The first electrocorticography (ECoG) during surgery was applied again in the same hospital in 1965 where epilepsy surgery gained speed with the efforts of O. Kalabay and V. Bertan from the departments of neurology and neurosurgery. In 1986, A. Erdem performed extratemporal cortical
Figure 11.1
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resections guided by ECoG in Ankara University. After being trained by G. Yasargil in Zurich, A. Erdem in Ankara and later E. Ozyurt in Istanbul introduced selective amygdalohippocampectomy in the early 1990s. Epilepsy surgery teams working in a multidiciplinary fashion were established in 1993 in Hacettepe and 1995 in Cerrahpasa Medical faculties and have continued since then with addition of different centers including Gazi University, Istanbul Medical Faculty, Marmara University and others.
Estonia7–11 The founder of the national school of neurosurgery in Estonia was Professor Ludvig Puusepp (1875–1942) who operated 318 epileptic patients during 1901–1920. Thereafter, the summary of operations in 1921–1930 (1–5 cases per year) were published. During the following years the number of operations have fallen dramatically, primarily due to effective medical treatment. In Tartu, EEG has been available since 1961, intraoperative electrocorticography (ECoG) since 1967, computerized tomography scanning since 1983, and magnetic resonance imaging since 1992. In 1996, the measurement of AED concentration just became available for routine use. Long-term video-EEG has been available in Tartu since 2003. In recent years all patients for epilepsy surgery were investigated in long-term video-EEG (only scalp-electrodes). An average of two patients per year has been operated, all typical MRI-positive hippocampal temporal lobe epilepsies. ECoG was performed in 50% of the cases.
Dr. Kenan Tükel as a member of the Montreal team in 1952.
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Latvia12–17 Episodical epilepsy surgery in the case of symptomatic disease (mainly tumors) in the territory of Latvia was performed at the beginning of the 20th century (A. von Bergmann, P. Klemm, L. Bornhoupt, E. von Schwartz in Riga’s 1st Hospital). During the 1920s and 1930s neurosurgical operations in 3 hospitals in Riga were performed by general surgeons (V. Minz, J. Jankovsky, P. Mucenieks, A. Udre, P. Stradins, K. Dolietis et al.), and in rare cases neurosurgical operations were made for cerebral disease with epilepsy. In the year 1939, K. Dolietis became the first certified neurosurgeon in Latvia and operated several patients with symptomatic epilepsy. At the end of the World War II, K. Dolietis emigrated to Sweden. Development of neurosurgery continued in Riga’s 1st Hospital; in 1946, the Clinic of Neurology and Neurosurgery was opened (A. Liepukalns and K. Arajs). In 1969 I. Purins organized the Neurosurgical Center on the basis of P. Stradin’s Clinical Hospital in Riga. Soon after that T. Apinis and Z. Grinbergs, doctors of this hospital, made the first steps to specialized epilepsy surgery after practices in the clinics of Moscow and Leningrad. The main method for epilepsy surgery was temporal lobectomy. Sometimes intraoperative cerebral surface electrodes were used for more precise diagnosis of the lesion locus. Other types of operations were frontal lobotomies, gyrotomies, callosotomies; some hemispherectomies were also performed. Fifteen operations of intracranial superficial hypothermia in patients with epilepsy did not give any influence to the disease course. A total of 145 operations for epilepsy were registered in this hospital during the period from 1974 to 1988. Epilepsy surgery in other hospitals of Latvia at this time was not very significant. Recently epileptic patients were selected for surgery in two neurosurgical departments of Riga: in the Clinical Hospital ‘Gailezers’ and in the P. Stradin’s University Hospital. The surgery for symptomatic epilepsy due to cerebral tumors, dysplasias, heterotopias, mesial sclerosis etc. is accentuated; the number of operations of such type is approximately 20–30 per year. The new technologies (neuronavigation and invasive electrode techniques) are also used in the epilepsy surgery.
one who developed epilepsy surgery in Lithuania. Also, he was the founder and the president of the Society for Epileptology of Lithuania, which joined ILAE as a chapter in 1995. In 2001 the Neurosurgery Clinic was reorganized, and a specialized unit for cerebral surgery was established, with the Sector for – Zobakas. ˇ Epilepsy Surgery included and headed by Dr. Arunas The diagnostic method implanted depth electrodes was introduced in 1982, and the use of subdural electrodes for the localization of the epileptogenic focus in 1989. Sleep EEG and video-EEG for presurgical diagnostics have been introduced at Kaunas University Hospital since 2000. The development of comprehensive presurgical multidisciplinary evaluation is one of the strategic plans at Kaunas University Hospital for the near future.
Hungary18–21 Kálmán Sántha and István Környey, friends and legendary personalities in the Hungarian history of neurology contributed equally to establish neurosurgery in the 1930s in Szeged and later in the 1940s in Pécs and Debrecen. István Környei was educated in Boston and Ann Arbor, Kálmán Sántha (Figure 11.2) in Montreal by W. Penfield, supported by the Rockefeller fellowship. Sántha, together with Cipriani, was the first to provided evidence that during an epileptic seizure it was not vasoconstriction (as was stated in the theory of Mayer) but just the opposite procedure, an important elevation in blood flow, that occured (Sántha, Cipriani, and Penfield 1938) (Figure 11.3). This work should be held as a first move toward the contemporary development of the ictal SPECT method. The first decisive steps of Hungarian epilepsy surgery were taken by J. Hullay in Debrecen, a pupil of Sántha, who reported on 50 temporal lobectomies as early as 1958.18,19 Later in the 1970s in the same institution (Department of Neurology, Medical University of
Lithuania The first specialized neurosurgery unit in Lithuania was established in 1951 at Kaunas Clinical Hospital (Kaunas University Hospital at present). The start of epilepsy surgery took place in 1974 when the first temporal lobe resection was performed by doctors Henrikas Juozakas and Vytautas Paˇskauskas. Since 1976 subpial cortical suction, and since 1978 stereotactic hippocampo-amygdalotomy have been introduced, the latter also being performed nowadays. The stereotactic method for epilepsy surgery has been introduced and is still being develˇ skis. In 1980 the Neurosurgery oped by docent Juozas Sidiˇ Clinic was established in Kaunas, with six specialized neurosurgery units. The Unit of Functional Surgery was a specialized unit for epilepsy surgery and microneurosurgery, with Professor Egidijus Jarûemskas as the Head until 1998, and Dr. Jonas Gel–unas until 2001. Professor E. Jarˇzemskas was the
Figure 11.2
Prof. Dr. Kálmán Sántha.
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History of epilepsy surgery in the Middle- and East-European countries and Russia
(a) Figure 11.3
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Registration of blood flow changes during experimental and human epileptic seizures. Sántha and Cipriani MNI, 1938.
3%
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Etiology 33% 24%
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Figure 11.4
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Surgical results, TS, TLE (1989-2001) National Institute of Psychiatry and Neurology.
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Debrecen) within the framework of the epilepsy surgery program, invasive presurgical monitoring with the Bancaud–Tailerach stereotactic methods was carried out on several patients.20 The new wave of modern epilepsy surgery was started in the 1990s with the foundation of a ‘Co-operative epilepsy surgery program’ in which under the leadership of the National Institute of Psychiatry and Neurology, Epilepsy Center, several neurological institutions, and the National Institution of Neurosurgery participated including the Bethesda Children Hospital where a video-EEG monitoring unit has been working since 1997.21 The number of patients involved and operated using the presurgical protocol is 20–30 yearly. The overwhelming majority of surgical interventions are partial temporal lobectomies in therapy resistant MTLE syndrome, but a few extratemporal surgeries are done yearly
with invasive presurgical evaluation by subdural strips and grids. Results of temporal lobe surgery are illustrated in the Figure 11.4. In 2005 a new epilepsy surgery program was started in Pécs in the Neurological Clinic of the Medical University.
Acknowledgments I am really grateful to Prof. Alla Guekht (Russia), Prof Jerzy Bidzinski (Poland), Prof. Pavel Mares and Prof. Ivan Rektor (Czech Republic), Dr. V. Ciobotaru (Romania), Prof. Cigdem Özkara (Turkey), Prof. Milda Endziniene and Dr. Arunas Zobakas (Lithuania), and Dr. André Öun (Estonia), for providing essential information not easily obtainable / elsewhere.
REFERENCES 1. 2. 3. 4. 5. 6.
7. 8. 9.
10.
Bidzinski J. Historia operacyjnego leczenia padaczki w Polsce (History of surgical treatment of epilepsy in Poland) Neurol. Neurochir. Pol. 1998: Suppl. 2:19–23. Türkmen V, Erbengi A. An infantile hemiplegia case presentation and hemispherectomy. Turkish Journal of Pediatrics 1960;3(3):135–139. Avman N, Erbengi A, Kalabay O. Role of electrocorticography in surgery of focal epilepsies. Çocuk Saˇgliˇgi ve Hastaliklari Dergisi (Journal of Paediatrics) Turkish 1965;8(1):26–35. Erdem A, Yasargil G, Roth P. Microsurgical anatomy of the hippocampal arteries. J Neurosurg 1993;79(2):256–65. Bertan V, Tahta K, Saygi S. Results of surgical intervention in patients with drug-resistant epilepsy. E.A.N.S Winter Meeting, Feb 17–19, 1994. Özkara Ç, Ozyurt E, Hanoglu L, Eskazan E, Dervent A, Kocer N, Ozmen M, Onat F, Oz B, Kuday C. Surgical outcome of epilepsy patients evaluated with a noninvasive protocol. Epilepsia 2000;41: S4:41–4. Puusepp L. Treatment of epilepsy. (in Estonian). Eesti Arst 1922;8/9: 403–10. Puusepp L. Treatment of epilepsy. (in Estonian). Eesti Arst 1922;10: 464–9. Perk J. Surgical treatment of neurological diseases during 1921–1930 in the department of neurology, Tartu University (in Estonian). Folia Neuropathologica Estoniana 1931;9:108–13. In the after-war period, 1945–1966, the number of operation increased to 12–38 per year. Raudam E, Paimre R. Development of neurology and neurosurgery in Tartu (in Estonian). Tartu Vabariikliku Kliinilise Haigla
11. 12. 13. 14. 15. 16. 17. 18. 19. 20. 21.
konverentside materjale Proceedings of the conference, Tartu 1969;1:195–211. Õun A, Eelmäe J Epilepsy surgery in Tartu 1991–2000. Proceedings of the III Baltic Congress of Neurosurgeons, Tartu. Tartu, 2000. The text of the poster is attached to the mail. Derums VJ, New Dates about Trepanations in Latvia at Middle Ages. From the History of Medicine, Riga, 1984:52–53 (in Russian). Landa BF, Dubinsky MB. About History of Surgery in Riga’s City Hospital. Works of Riga’s 1st Hospital, Riga, 1957:63–76 (in Russian) Viksna A. Adolf von Bergmann and surgery in Riga. Latvijas Arsts, Riga, 1994;8:678–680 (in Latvian). Apinis T, Neurosurgery in Stradin’s Hospital through Ages. Stradin’s Hospital Works, Riga, 2000:70–75 (in Latvian). Sverzickis R, Aksiks I, Valeinis E, Pukitis E, Dzelzite S, Migals A, Otisone I, Bluma I, Plotniece R. Stereotactic neurosurgery: practice and possibilities. Arstu Zurnals, 2003:5/6:32–38 (in Latvian). Apinis T. Personal communication, 2006. Hullay J. Results of 50 surgically treated temporal epileptic patients. Acta Neurochir (Wien).1958;6(3):169–74. Kajtor F, Hullay J, Farago L, Haberland K. Electrical activity of the hippocampus of patients with temporal lobe epilepsy. AMA Arch Neurol Psychiatry. 1958 Jul;80(1):25–38. Hullay J, Gombi R, Velok G. Effects of stereotactic lesions in intractable epilepsy. Acta Neurochir (Wien).1976;(23 Suppl):205–9. Balogh A, Borbély K, Czirják S, Halász P, Juhos V, Kenéz J, Vajda J. Tapasztalataink a temporális epilepsziás betegek mütéti kezeléséveltöbbközpont–u vizsgálat. Clinical Neurosci/Ideggyógyászati Szemle 1997;50(7–8):221–32.
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The Montreal School From 1934, Wilder Penfield with his surgical partner William Cone, their associates and many successors, developed at the Montreal Neurological Institute a center that became known world-wide for its systematic surgical treatment, research and teaching related to epilepsy (Figure 12.1).1–6 Following Victor Horsley’s pioneer efforts,7 many surgeons in North America ventured to operate on patients suffering from seizures related mostly to cerebral trauma or tumors.8,9 But their reports were often a litany of failures. Harvey Cushing had treated patients with seizures by surgery under local anesthesia and was the first to report mapping by electrical stimulation of the sensory cortex.10 But Cushing centered his main interest on brain tumors, noting in 1932 to Wilder Penfield his former student, at all events, you can see that I, too, just thirty years ago was extirpating a cortex for epilepsy. If I had the industry and ability that you and Foerster combine, I might have gone ahead with it and made something of it. But I soon dropped it for things I thought I could do better.11 While at Columbia-Presbyterian Hospital in New York, in the 1920s, Penfield had taken a special interest in the problem of how a wounded brain heals, hoping that a better understanding would lead to improvement in excision of brain lesions, such as the post-traumatic scars associated with epilepsy.5,11 He pursued this interest by going to Madrid in 1924, where he studied with Ramon y Cajàl’s brilliant student Pio del Rìo-Hortega the role of neuroglia and microglia in brain healing, tumors and inflammation.12 As the first English speaking pupil of the Cajal school of neurohistology, Penfield returned to New York and applied his unique expertise to neurosurgical problems, and especially to epilepsy. Then in 1928 during his transition between New York and taking up neurosurgical practice in Montreal, he spent six months with Otfrid Foerster in Breslau. Here he learned the technique of electrical stimulation of the cortex with the patient awake under local anesthesia. He also took advantage of his familiarity with the Spanish methods to study the histology of the meningo-cerebral cicatrix in a dozen patients, mostly with head injuries, upon whom Foerster had operated for seizures.13 In September 1928, Penfield arrived in Montreal on the invitation of Edward Archibald to take over his neurosurgical practice at the Royal Victoria Hospital associated with
McGill University. Archibald had been a student in 1906 of Sir Victor Horsley and Sir William Gowers at the National Hospital, Queen Square, and thus became the first surgeon in Canada to focus on neurosurgery. In 1908, he published the 375-page monograph on ‘Surgical Affections and Wounds of the Head’ in Bryant and Buck’s American Practice of Surgery.90 It was the same year that Harvey Cushing’s extensive review of 259 pages on neurosurgery appeared in Keen’s Surgery: Its Principles and Practice.91 But Archibald began to take greater interest in thoracic surgery, in which he would become one of the American leaders. He also turned to the problem of post-graduate surgical education and directed his influence to establishing the American Board of Surgery. Earlier at McGill University, William Osler was a keen protagonist for the emerging specialty of neurosurgery. From 1869 to 1884 he performed a thousand autopsies at the Montreal General Hospital. Among these, he reported many examples of neurological disorders, including epilepsy.14,15 In commenting on the first operation for a brain tumor performed by Rickman Godlee in 1884 at London, Osler compared his own case where a post-mortem examination in 1883 disclosed a small glioma in the leg center of the cortex. This had caused Jacksonian seizures for twelve years, eventually ending in a fatal bout of status epilepticus: ‘an instance’, Osler wrote, ‘in which operation would have been justifiable and possibly have been the means of saving life’.16 Osler’s spirited humanism and his positive attitude toward brain surgery influenced the field of neurosurgery through his friendships with both Harvey Cushing and Wilder Penfield.17,18
The Royal Victoria Hospital, Montreal (1928–1934) In November 1928, two months after Penfield moved with his surgical partner William Cone from New York to Montreal, he performed his first operation at the Royal Victoria Hospital for focal epilepsy. (Figure 12.1) The young patient (RM) had fallen from a horse ten years earlier when he required surgery for a right-sided subdural hematoma and brain contusion. He developed seizures with increasing frequency, from 5 to 20 a day. Eventually, this complex post-traumatic epileptogenic lesion required three operations to control these intractable seizures. At the first procedure, a small area of cortex was
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The Montreal Neurological Institute
Figure 12.1 Wilder Penfield (left) and William Cone, the neurosurgical partners, at the Royal Victoria Hospital, 1932.
excised near the motor strip that was defined by stimulation. The attacks continued. A second exploratory craniotomy followed a few months later to expose the frontal lobe on the opposite side; no abnormalities were found so no removal of any sort was made. For the third and final operation, three years later, Stanley Cobb and William Lennox came from Boston as consultants. Cobb’s sketch and Penfield’s comments (in bold letters) show the sites of the stimulation responses and delineates the thin scarred cortex of the temporal area that was widely resected (Figure 12.2). Penfield referred to this as his first temporal lobectomy for seizures. He had applied stimulation and excision techniques learned in Foerster’s clinic at Breslau (Foerster and Penfield, 1930b) In the first few years after operation, the patient had a greatly reduced number of seizures. After starting dilantin in 1939, his attacks numbered four in the next 13 years.20 In 1930, Penfield listed the neurosurgical cases for the preceding two years at the Royal Victoria Hospital. Among the 325 operations carried out by him and William Cone, there were fourteen examples of surgery for focal epilepsy. The successful transfer to Montreal of the laboratory of neurocytology, which they had started in New York, was already attracting students from the United States and abroad. During this period Penfield edited for publication a three volume multi-authored work destined to become a neurological classic, Cytology and Cellular Pathology of the Nervous System.21
After a refusal and several delays, the Rockefeller Foundation responded in 1932 to the proposal of Wilder Penfield and McGill University for a Neurological Institute ‘to provide,’ Penfield hoped, ‘a center for neurological thought that would serve the whole continent.’ He envisaged clinical neurology and neurosurgery carried on in the same building that contained laboratories for research in neuropathology, neurophysiology and the anatomy and psychology relating to the nervous system.22 The Montreal Neurological Institute (MNI) opened its doors in 1934. An interesting hybrid, it was unique in its time, a 50-bed hospital for patients with neurological disorders, combined with a research center for the scientific study of the nervous system and a teaching Department of Neurology and Neurosurgery for McGill University. With the provision of endowment by the Rockefeller Foundation of $1,000,000, further support garnered from generous citizens in Montreal as well as ongoing pledges by the City and Provincial governments for hospital support, the stage was set and the actors were in place to carry out Penfield’s master plan.5,20,23 Penfield and his surgical partner, William Cone, expanded their studies on the histopathology of brain scars and brain tumors with an enthusiastic and ever growing team of young assistants. They made persistent efforts to treat intractable epilepsy caused by trauma or tumors, applying the Foerster technique to score some brilliant successes. At multidisciplinarian weekly conferences, seizure patterns of patients were scrutinized in great detail, catalogued, and matched with the type and location of the lesions predicted by X-ray and EEG and as revealed and photographed at operation. Meticulous analysis of hundreds of stimulation points were plotted out to constitute brain maps of the sensory and motor areas that gave more detail than the earlier maps published by Horsley, Foerster, Krause, and Cushing.24,25 These findings extended eventually to the definition of speech areas26 and to the complex problem of how the brain remembers.27,28,29 Maximal removals of frontal tumors and scars causing epilepsy resulted in surprising retention of intellectual functioning in the patients as determined by.29,30 Hebb’s studies on Penfield’s patients also activated the field of clinical neuropsychology which at the MNI over many years has been of critical importance for the pre- and post-operative evaluation of patients.31 Cortical stimulation: the homunculus In 1937, Penfield with Edwin Boldrey reviewed 163 patients, who were operated upon under local anesthesia and in whom the motor-sensory responses to cortical stimulation were carefully plotted. These composite stimulation maps became familiar in the numerous publications from Penfield and his team over the years. Their report marked also the first appearance of the ‘homunculus’ (Figure 12.3) who would later appear in several guises (Figure 12.4) to highlight the cortical localization subserving anatomical regions of the body (Penfield and Rasmussen, 1950; Penfield and Jasper, 1954).
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Figure 12.2 Penfield’s sketch and notes during the operation on patient R.M. The brain is upside down as viewed by the surgeon, with the frontal lobe to the left. Two excisions, outlined by dashed lines, include a small area in front of the motor cortex (1A) and a much larger resection of the temporal lobe shown in the upper part of the sketch. Penfield’s notes are in bold script; the notes in finer lettering and possibly some of the details of the sketch are in Stanley Cobb’s hand.
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Figure 12.4 A later version of the homunculus, with reference to the representation in the motor cortex, from the studies of Penfield and Rasmussen in 1948.
Figure 12.3 Homunculus appearing first in the article by Penfield and Boldrey in 1937, to illustrate the relative size of body parts represented on the motor cortex as defined by electrical stimulation at operation.
Herbert Jasper and the advent of electroencephalography A chance encounter at Brown University in 1937 led Penfield to bring Herbert Jasper to Montreal to apply the new techniques of electroencephalography (EEG) and electrocorticography (ECG). Jasper with Carmichael in 193593 had reported on the application of Berger’s new technique of EEG, in the same year that the Boston group led by Gibbs had noted its value in epilepsy.32 EEG refined the task of localizing the site of origin of seizure discharge by recording spikes and sharp waves that were pathognomonic for epilepsy.33 This greatly improved the selection of patients with focal seizures for surgical treatment. ECG mapped the localization of seizure activity during surgery by recording directly from the cortex and by monitoring stimulation responses. The application of the new technology to epilepsy resulted in a long series of clinical studies by Penfield, Jasper and their associates. Jasper’s background in psychology and
electrophysiology also generated at the MNI an expansion in neurophysiological research which over the years elucidated the complex mechanism of epilepsy and sharpened the criteria for surgical treatment.34 Jasper’s chapter in the monograph by Penfield and Erickson of 1941 on Epilepsy and Cerebral Localization provided the first comprehensive review of the use of EEG and corticography in the diagnosis and surgical treatment of epilepsy.94 Numerous monographs and publications by Penfield with his associates, Jasper, Kristiansen, Rasmussen and a long list of neurosurgical Fellows, continued to document from 1934 to 1950 much detailed evidence for the successful surgical treatment of focal epilepsy at the MNI.20
Surgery for temporal lobe seizures The anterior and lateral temporal cortex The emergence at the MNI in the early 1950s of surgery for seizures related to the temporal lobe opened a new era for what has now become the most frequent surgical approach for the surgical treatment of epilepsy. There were several phases in the development of such surgery, each distinguished by a substantial increase in knowledge about the pathophysiology of seizures arising from the temporal lobe. Penfield and Flanigin35 reviewed 68 temporal lobe operations carried out over the decade from 1939 to 1949, which had arrested or controlled seizures in over one-half of the patients. The resections in this series were limited mainly to the anterolateral temporal cortex; in only 10 cases was the uncus removed and in only two was a part of the hippocampus also removed. Bailey and Gibbs36 in the meantime performed antero-lateral cortical removal in a series of patients, with no encroachment on
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Epilepsy surgery in Canada mesial temporal structures because Bailey was aware of the severe behavioral deficits in monkeys after bilateral mesial temporal ablations as reported by Klüver and Bucy92 beginning in 1939.37 This limited anterolateral approach was also supported by the pre-operative localization offered by EEG, either antero-lateral temporal, anterior Sylvian, or fronto-temporal.38 Related experimental studies at the MNI were thus directed to clarify the connections of the temporal pole.39,40 This is also well illustrated by similar anterolateral temporal localization of ECG foci registered by Jasper and two young neurosurgeons41 in 39 of the same series of patients reported by Penfield and Flanigin in 1950. In only a few patients was ECG abnormality detected in the inferior and mesial part of the temporal lobe. (Figure 12.5). The mesial temporal region The success rate of just over 50% in the two major surgical series, reported from Montreal by Penfield and Flanigin35 and from Chicago by Bailey and Gibbs36 indicated that resection limited to the antero-lateral temporal cortex did not eliminate all the epileptogenic tissue in many patients. Indeed in some cases persistent seizures led Penfield to persevere and carry out a second operation. In these, he extended the resection, under electrocorticographic control, sometimes posteriorly along the lateral temporal cortex (if on the nondominant side for speech) and also included more of the uncus and hippocampus.20
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A second phase in the surgical approach to temporal lobe seizures unfolded rapidly in the early 1950s. Clues from experimental animal studies by Gastaut et al.42 and Kaada43 and from stimulation at operation44,45 pointed to the mesial and inferior surfaces of the temporal lobe for the origin of the epileptic attack. Penfield noted instances where stimulation in the uncinate region produced auras of the patients’ attacks. In one such instance, a seizure with automatism was recorded consisting of low voltage fast activity followed by 3 per second waves to spread from the stimulation point to involve a wide region of the temporal cortex. (Figure 12.6). These findings led Penfield in this case to extend his resection to include the mesial temporal region. Stimulation responses from the claustro-amygdaloid complex The most convincing evidence that the mesial temporal region was a crucial zone for the generation of temporal lobe seizures came in a third phase of surgical studies. This was the reproduction of the patient’s habitual auras and other typical features of these attacks by anatomically directed depth stimulation or stimulation under direct vision at operation within and around the amygdala involving also the ventral claustrum and the anterior insula.46 The resulting seizure discharges on corticography were seen to spread rapidly to encompass not only the temporal cortex but the exposed frontal parietal cortex. In 1951, the surgical findings in the first patient in this series, initiated convincing evidence for the role of the amygdaloid region in temporal lobe seizures.27
Lesions in group I 14 cases
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Figure 12.5 Localization of ECG foci and lesions reported by Jasper, Pertuiset, and Flanigan in 39 patients operated upon for temporal lobe seizures by Penfield. The maximum changes, areas indicated in black, involve mainly the antero-lateral cortex of the temporal lobe.
Case report Patient P.S., Age 26 He had a difficult birth and, from the age of 12, attacks which began with a vision of colored lights, a ‘shock in the head’, after which he became unresponsive, fumbled with his clothes and would later have no memory of his actions during this period. Pre-operative EEG study showed abnormal spike activity over the lateral and inferior temporal regions on the right side. At operation, a depth electrode was directed through the second temporal convolution 3.5 cm from the tip of the temporal lobe toward the region of the amygdala. One of his typical small attacks was produced with the electrode tip deep in temporalinsular sulcus, with electrodes recording from the lateral and inferior surface of the temporal lobe (Figure 12.7). Epileptic spikes were suddenly replaced by low voltage rapid activity, the patient was seen to stare and become unresponsive to questioning, while he plucked at the anaesthesist’s coat and made chewing movements. His appearance was much like that seen in his habitual attacks. The electrographic changes lasted a minute and a half, at which time the patient appeared to have recovered, but seemed unaware of the attack (Figure 14.7). There was smallness and toughness of the first temporal convolution and mesial temporal region, as well as a zone of gelatinoid tissue about the size of a small walnut deep in the temporal lobe, lateral and inferior to the ventricle and encroaching on the amygdala. Microscopically, this showed dense astrocytic gliosis. On later review, the neuropathologist interpreted this as a grade I astrocytoma. Resection included
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Figure 12.6 ECG recording at operation by Penfield. After stimulation of the uncinate region, a seizure discharge was recorded from a wide area of the inferior temporal cortex.4,41
6 cm. of antero-lateral cortex, as well as the mesial temporal region (amygdala; hippocampus) harboring the lesion. The patient continued free of attacks for 37 years later, with no reappearance of the tumor. The role of the claustro-amygdaloid complex In 15 other patients from that same study, similar features of automatism and amnesia were reproduced by stimulation in the peri-amygdaloid region (Figure 12.8). This first examination of stimulation and electrographic responses from the human amygdala demonstrated its role in visceral responses such as fear and its critical relation to recent memory.46 It was noted that these findings corresponded to the localization for ‘a particular variety of epilepsy’ that had been proposed by Hughlings Jackson and others, just before the turn of the century: the discharge-lesions in these cases are made up of some cells, not of the uncinate gyrus alone, but of some cells of different parts of a region of which this gyrus is part – a very vague circumscription, I admit – the uncinate region.47 The rich network of connectivity subtended by the amygdala offered a valid explanation for many of the characteristic clinical features of ‘uncinate’ attacks described by Jackson.27 Thus, the patient’s epigastric aura, sometimes associated with a sense of fear, was reproduced from stimulation either of the amygdala itself or of the adjacent anterior insular cortex, which would later be shown to be physiologically associated with gastric movement.48 The various emotional, autonomic, and visceral responses likewise seemed explicable because of
the robust anatomical pathways then known from the amygdala to the septal and hypothalamic regions. The initial feature of brief tonic movement with some temporal lobe attacks could be effected by the amygdaline efferent pathways to the striatum; chewing and swallowing movements could be explained by connections with the brain stem. The interference of the epileptic discharge with memory recording, characterized by the profound postictal amnesia, could reasonably be related, it was proposed, to the amygdala–hippocampal connection as well as the projection of the amygdala to the reticular system of the brain stem.49 Curiously, stimulation of the hippocampus directly at operation in the Montreal experience rarely produced such responses, even though epileptic abnormality might sometimes be recorded from the anterior part of the structure.50 Thus, this evidence indicated that the amygdala and the juxtaposed gray matter, including the ventral claustrum and the anterior insular cortex, could generate temporal lobe seizures; this provided a physiological hypothesis that explained for the first time many of the clinical aspects of these attacks (Figure 12.9a, b). It also indicated that the periamygdaloid zone should be removed in the surgical resection in order to produce the most beneficial outcome. This critical role of the peri-amygdaloid region in mesial temporal seizures became confirmed in many later studies, as summarized for example in the monograph by Gloor in 1997.51 Incisural sclerosis The pathological counterpart of this physiological hypothesis was offered in a concurrent study by Earle, Baldwin, and Penfield in 1953.52 They introduced the concept of incisural
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Figure 12.7 (a) Brain drawing to show electrode positions (in numbered circles) and depth stimulation in the amygdaloid region (black circles) from patient P.S.27 (b) ECG showing rapid low-voltage activity from the temporal lobe and then return of the prestimulation spike activity. The patient had automatism and amnesia for the episode. Compare with Figure 14.6.27
sclerosis, which they postulated was due to herniation of the mesial part of the temporal lobe over the tentorial edge associated with increased intracranial pressure during a difficult birth (Figure 12.10). They considered this to cause injury to the hippocampal region, both by direct compression of the tissue and by arterial and venous vascular compression with resulting ischemia. Although they did not emphasize this, the uncus with the contiguous amygdala and entorhinal cortex are even more likely to herniate into the prepeduncular space and to be subject to compressive damage.
Application of the Montreal procedure Based on these new findings from stimulation results and pathological studies, a radically different surgical approach was developed, with excision not only of the
anterolateral cortex, but also removal under direct vision of the mesial part of the temporal lobe to include the amygdala, hippocampus and entorhinal cortex. Details of this operative technique were first described by Penfield and Baldwin in 195253 (Figure 12.11) and revised in 1961 by Penfield et al.54 With the application of this approach, successful surgical outcome improved from 50% to 65%. From 1953 onward, many neurosurgical centers, often involving surgeons and scientists who had studied at The Montreal Neurological Institute, took up the procedure of temporal lobe resection for the treatment of seizures. A colloquium on advances in the surgical treatment of temporal lobe epilepsy, organized by Gastaut and his associates in Marseilles in 1954, gave an opportunity for Penfield to provide an overview of the early experimental and surgical results of his team, which firmly established the important role of the mesial temporal region in the pathogenesis and surgical treatment.55 The extensive monograph of 1954 by Penfield
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Insula and brain stem removed
INSULA REFLECTED POSTERIORLY
AMYGDALOID NUCLEUS
Figure 12.8 Sites of stimulation from 16 operations that produced features of temporal lobe seizures such as epigastric area, fear, memory disturbance, automatism and amnesia.
and Jasper reviewed this Montreal experience.(Figure 12.12) A second colloquium sponsored by Maitland Baldwin and Pearce Bailey56 in 1958 at the National Institutes of Health, USA, extended and confirmed the significance of subtotal temporal lobectomy, including particularly the mesial temporal structures, for treating temporal lobe seizures.57 Memory deficit with bilateral temporal lesions Scoville and his group at Hartford44 had also produced stimulation responses from the uncus which resembled some features
(a)
of temporal lobe seizures. This induced him to carry out bilateral resection of the mesial temporal region by a subfrontal approach in a few patients with epilepsy. One of these patients, H.M., who has since become noteworthy in the annals of neuropsychology, developed a severe deficit in recent memory.58 This was similar to the syndrome that had been reported earlier by Milner and Penfield28 from the MNI series, in three patients after unilateral temporal excision in the presence of what later became recognized as bitemporal mesial temporal pathology, especially involving the hippocampus.59,60 These findings, together with the initial observation by Feindel and Penfield27 that stimulation of the amygdala evoked ictal amnesia, directed attention to the important role of the mesial temporal structures in memory mechanisms.28 Toward a surgical cure The surgery of focal temporal seizures, augmented by many contributions, has become one of the most successful therapeutic measures in modern neurosurgery.61,62 Many thousands of patients have had the benefit of such surgery. The patterning of the surgical resection in order to obtain the most satisfactory surgical outcome and at the same time to minimize neurological deficit continues to be examined currently in over 100 neurosurgical centers.23,62 A vast literature has now become available on the anatomy, physiology, pathology, and cognitive aspects of the temporal lobe.63–68 Gloor summarized this field in 1997 in his masterly monograph on the temporal lobe and limbic system.51 The developments in EEG such as sphenoidal recordings and computerized-video monitoring greatly enhanced the pre-operative localization of the epileptogenic region.69 The increasing use of detailed neuropsychological evaluation by Milner and her associates and the application of the intracarotid amytal test developed by Wada and Rasmussen for defining lateralization of speech and memory function proved to be invaluable adjuncts.28,69,70
(b)
Figure 12.9 (a) Enlarged view of the claustro-amygdaloid complex which shows the Sylvian fissure (SF), claustrum (CL), anterior commissure (AC), globus pallidum (GP), centro-medial and baso-lateral nuclei of the amygdala (C-M, B-L) hippocampus (H), ventricle (V), and collateral fissure (C-F).27 (b) A more anterior coronal section shows the Sylvian fissure (SF) and grey matter of the ventral claustrum (VCL). This section relates to the site of the depth stimulation.27
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Int. carotid a. Mid. cerebral a UNCUS.
Ant. choroidal a Post. cerebral a.
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Figure 12.12 Wilder Penfield (seated), and Herbert Jasper photographed in 1954 on the publication of their monograph, Epilepsy and the Functional Anatomy of the Human Brain.
Figure 12.10 Drawing to show the region of sclerosis and the mesial blood vessels involved in tentorial herniation of the uncinate region, for example, during abnormal birth.52
Further surgical evidence from the MNI76 indicates that temporal corticectomy with radical resection of the amygdala and uncus but with minimal removal of the hippocampus can achieve an excellent surgical outcome in 65% of patients (Figure 12.13a) At the same time the relative sparing of the hippocampus reduces the possibility of deficit in memory function which had been assigned by Milner and others31,69 to varying degrees of damage to the hippocampal regions.
Surgical techniques have become refined and selection of patients for the surgical procedure has grown far more enlightened.71–73 Amygdalo-hippocampectomy introduced by Niemeyer in 195874 and adopted enthusiastically by Wieser and Yasargil in 1982,75 has yielded an excellent surgical outcome and may well prove on evidence to become the resection of choice in selected patients.72
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TEMPORAL LOBE SUPERIOR and MESIAL SURFACES
Figure 12.11 Drawing to show subtotal temporal lobectomy that includes the amygdala and up to 4 cm of the hippocampus as well as the antero-lateral temporal cortex, as described by Penfield and Baldwin in 1952.53 This operation became widely adopted.
Figure 12.13 (a) Anatomical dissection of the temporal lobe to show cortico-amygdalectomy (hatched line on the left) compared to cortico-amygdalo-hippocampectomy (hatched line on the right).76 (b) Post-operative MRI to show radical excision of the amygdala and minimal removal of the hippocampus.9
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The acquisition at the MNI of magnetic resonance imaging (MRI) in 1985 gave a significant new dimension to the selection of patients for operation by identifying small structural lesions in the temporal lobe in more than 25% of patient and also the presence in another 30% of patients of mesial temporal sclerosis involving the hippocampus and later demonstrated also to include the amygdala and entorhinal cortex.73,77,78 MRI also provided the sine qua non for monitoring the exact anatomical extent of the surgical resection to compare with the type of surgical outcome reported from different centers.20 In the span of fifty years covered by this review, the effective control of temporal lobe seizures by surgical treatment has thus improved from 50% to almost 90%, with minimal morbidity and mortality.71,79 The role of mesial temporal sclerosis in the pathogenesis of temporal lobe seizures is now widely recognized.68 The significance of the amygdalo-hippocampal region in the physiopathology has been well substantiated from many stimulation studies,80,81 and by greater detail available on the anatomy and pathology of these structures.82–84 Marked improvement based on limited excision of the hippocampus but radical resection of the amygdala and minimal cortical ablation has been achieved in the surgical cure of temporal lobe seizures.76
Contributions from the Toronto school Kenneth McKenzie trained with Harvey Cushing at Boston in 1923 and returned to establish the first neurosurgical unit in Toronto in 1924.15,85 He performed the first hemispherectomy for seizures in 1936. He reported the case in 1938 at a meeting of the American Medical Association. The patient, a 16-year-old woman, had seizures from infancy and progressive hemiplegia. After operation she was seizure-free and lived with her family for another 23 years. McKenzie’s experience antedated by 14 years the series of 12 patients with seizures treated by hemispherectomy by R.A. Krynau and published in 1950. McKenzie never published his case but the patient was studied and reported by Williams and Scott86 in 1939 in relation to autonomic responses following hemidecortication. At the Sick Children’s Hospital in Toronto, Stobo Pritchard established a comprehensive neurological clinic for childhood epilepsy. On his foundation the pediatric neurosurgeons of the Toronto school, especially Harold Hoffman, developed an active center for surgical treatment of epilepsy in the 1970s.
Epilepsy program at London, Ontario In 1977 Warren Blume, a neurologist and epileptologist, and John Girvin, a neurosurgeon and neurophysiologist, both trained at the MNI and McGill, established an Epilepsy Unit, coordinating a multidisciplinary team of health care professionals. Although somewhat in the shadow of the illustrious team led by Drake, Barnett, Ferguson, and Peerless, who were world-leaders in the cerebrovascular field, the Epilepsy Unit developed successfully over the next two decades. A convincing milestone in the long record of evidence for the effectiveness of surgery for temporal lobe epilepsy was reported by the London group from an ingen-ious randomized trial comparing medical treatment with surgical treatment at this unit from July 1996 to August 2000.87 From a study of 80 patients
divided into two groups, they found that 64% of the 36 patients operated upon by temporal lobe resection were free of seizures compared to 8% in the group assigned to medical treatment, an eight-fold benefit. The pre-operative investigation and selection for surgery in this London project evidently followed the same lines as those practiced for many years at the Montreal Neurological Institute. The pattern of surgical excision, based on the procedure introduced by the Montreal group in the 1950s,53 included the antero-lateral temporal cortex and the mesial structures, especially the amygdala and hippocampus.88 Thus the London study was another vindication of the successful results of surgery reported from the MNI over a period of 50 years and documented in extensive long-term follow-up studies by Rasmussen and many colleagues. These demonstrated a post-operative outcome of 65% of patients seizure-free and over 85% showing significant improvement in regard to seizure control.89
Other Canadian centers Neurological and neurosurgical trainees from the Montreal Neurological Institute and McGill introduced neurosurgical treament for epilepsy in many other Canadian cities, including Edmonton, Saskatoon, Vancouver, Calgary, Winnipeg, and Halifax. Returning to Montreal, the major neurosurgical unit at Notre-Dame Hospital affiliated with the University of Montreal and first established in 1947 by Claude Bertrand, who had trained with Penfield and Cone at the MNI, became a world center for functional neurosurgery. This included the operative treatment of epilepsy. Although many children with focal epilepsy had been treated over the years at the MNI by Penfield and his team, in the 1970s an active group dealing with childhood epilepsy was established through the efforts of Preston Robb, head of neurology, and Kathleen Metrakos in charge of EEG. José Montes after completing his training at the MNI developed one of the most active centers at the Montreal Children’s Hospital (MCH) for the surgical treatment of epilepsy in children.
Conclusion This historical outline highlights the contributions in Canada that enhanced our basic understanding of the surgical treatment of epilepsy. From 1934 to 1984 the MNI was headed by three successive Directors who were neurosurgeons with a persisting interest in epilepsy surgery (Figure 12.14). Trainees in neurosurgery, neurology, EEG, neurophysiology, neuropsychology and neuroimaging from the MNI have translated the benefits of surgical treatment throughout Canada and to many other countries around the world. In particular, many of the major centers for epilepsy surgery in the United States were established by MNI graduates. Since the early 1970s, the revolutionary advances in brain imaging have elucidated the pathological and neurochemical changes in epilepsy and also provided elegant three-dimensional visualization to the surgeon for pre-operative diagnosis, precise anatomical navigation during operation and exact monitoring of the surgical resection to correlate with clinical outcome.
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Figure 12.14 Successive neurosurgical directors of the MNI, from the left, Theodore Rasmussen, William Feindel, and Wilder Penfield who promoted research, teaching, and surgical treatment of epilepsy. Photograph taken in 1974 at the celebration of the 40th Anniversary of the MNI.
Acknowledgments This review reflects contributions over the past 60 years of my teachers and colleagues at the MNI as credited in the selected list of references. I appreciate the help of Helmut Bernhard, Department of Neurophotography for formatting the illustrations and thank Ann Watson and Linda Zegarelli for editorial assistance. The illustrations are reproduced from the Wilder
Penfield Archive and the Neuro Archives of the Montreal Neurological Institute. Research for this review was supported by the Class of Medicine McGill 1945 Wilder Penfield Archive Fund, the Thomas Willis Fund of the Montreal Neurological Institute, and by grants from the Donner Medical Foundation and Associated Medical Services, Inc. (through the Jason Hannah Institute for the History of Medicine), for the NeuroHistory Project, Montreal Neurological Institute.
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Cendes F, Andermann F, Gloor P, Feindel W. Relationship between a trophy of the amygdala and ictal fear in temporal lobe epilepsy. Brain 1994;117:739–46. Bernasconi A, Bernasconi N, Andermann F et al. Entothinal cortex in temporal lobe epilepsy: a quantative MRI study. Neurology 1999;52:1870–6. Yasargil MG, Teddy PJ, Roth R. Selective amygdalo-hippocampectomy. Operative anatomy and surgical technique. Adv Tech Stand Neurosurg 1985;12:93–123. Talairach J, David M, Tournoux P. l’Exploration Chirurgicale Stéréotaxique du Lobe Temporale dans l’Épilepsie Temporale. Repérage Anatomique Stéréotaxique et Technique Chirurgicale. Paris: Masson, 1958. Crandall PH. Historical trends: a conical spiral, in Apuzzo MLJ (ed): Neurosurgical Aspects of Epilepsy. Park Ridge, Ill: American Association of Neurological Surgeons, 1991;3–13. Mathieson G. Pathology of temporal lobe foci. Adv Neurol 1975;II:163–85. Pringle CE, Blume WT, Munoz DG, et al. Pathogenesis of mesial temporal sclerosis. Can J Neurol Sci 1993;20:184–93. Bruton CJ. The Neuropathology of Temporal Lobe Epilepsy. New York, NY: Oxford University Press, 1988. Morely TB. Kenneth George McKenzie and the Founding of Neurosurgery in Canada. Markham, ON: Fitzhenry and Whiteside, 2004.
86. 87. 88. 89. 90. 91. 92. 93. 94.
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Williams DJ, Scott JW, The functional responses of the sympathetic nervous system of man following hemidecortication. J Neurol Neurosurg Psychiat 1939;2(ns):313–21. Wiebe S, Blume WT, Girvin JP et al. A randomized, controlled trial of surgery for temporal-lobe epilepsy. New Engl J Med 2001;345:311–18. Girvin JP, Resection of intracranial lesions under local anesthesia. Int Anesthesiol Clin 1986;24:47–73. Rasmussen TB. Surgical treatment of complex partial seizures: results, lessons, and problems. Epilepsia 1983;24(suppl 1): S65–S76. Archibald E, Surgical affections and wounds of the head. In: Bryant JD, Buck AHT eds) American Practice of Surgery. New York: W. Wood & Co., 1908;4:3–378. Cushing H. Surgery of the head. In: Keen WW (ed): Surgery, its Principles and Practice. Philadelphia: WB Saunders Co., 1908;17–276. Klüver H, Bucy PC. Preliminary analysis of functions of the temporal lobes in monkeys. Arch Neurol Psychiat 1939;42:979–97. Jasper HH, Carmichael L. Electrical potentials from the intact human brain. Science 1935;81:51–3. Jasper HH, Electroencephalography. In: Penfield W, Erickson TC, eds. Epilepsy and Cerebral Localization. Springfield, IL: Charles C Thomas, 1941:380–454.
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A brief history of epilepsy surgery in the United States PJ Connolly, DD Spencer, and AA Cohen-Gadol
If I wished to show a student the difficulties of getting at the truth from clinical experience, I would give him The History of Epilepsy to read. Oliver Wendell Holmes1 The history of epilepsy treatment revolves around individuals who through their ingenuity and innovation have elucidated the understanding of epilepsy pathophysiology. In the following chapter, we will review some of the contributions of these key individuals from the United States of America.
responsible for epilepsy in the absence of a structural lesion. In 1948, the Gibbs studied 300 patients’ EEG findings associated with psychomotor seizures localized to the anterior temporal lobe.3 They convinced Percival Bailey (who was trained by Cushing) to perform anterior temporal resections for psychomotor epilepsy. By 1954, Bailey had operated on 72 patients with a five year follow-up and concluded that ‘major convulsions are abolished or greatly reduced in half of the cases.’ The hippocampus and hippocampal gyrus were spared in these operations.4 The Gibbs’ and Bailey’s efforts were one of the earlier attempts at surgical treatment of non-lesional epilepsy.
Benjamin Winslow Dudley Dudley who had earned his MD from University of Pennsylvania, traveled to England and France to learn the art of surgery and trephining. When he returned to Kentucky in 1818, he became the first American to perform surgery for epilepsy and the first surgeon to ever publish a series (five) of epilepsy surgery patients. He conducted surgery for post-traumatic epilepsy. All five patients in his series survived, three were seizure free and the other two had decreased seizure frequency.2 Dudley attributed his success to the ‘good clean air’ of the Kentucky frontier.
Harvey W Cushing The history of modern epilepsy surgery in many ways reflects the history of neurosurgery in the late 19th and early 20th centuries. During his training, Cushing (considered to be the father of modern neurosurgery) went abroad in 1901, where he visited Horsley but he was not impressed by Horsley’s speedy surgical techniques. Upon his return to the United States and expansion of his practice at Peter Bent Brigham Hospital in Boston, Cushing established the safety of intracranial surgery and neurosurgery training programs. He had a particular interest in surgical treatment of brain tumors. He demonstrated the localizing value of epileptic syndromes although he had no special interest in electrophysiology. He trained many future leaders in epilepsy surgery including Percival Bailey and Wilder Penfield.
Bailey and Gibbs As early as 1938, Frederic and Erna Gibbs along with Lennox had suggested the idea of operating on an electrical focus 116
More recent generation of epilepsy surgeons in the United States Earl Walker’s5 physiological studies on the brain and more specifically thalamus provided further data regarding electrophysiological mechanisms underlying epilepsy. Arthur Ward6,7 was the first to perform intracellular recordings from human epileptic neurons. His demonstration of temporal lobe electrophysiology responsible for epilepsy further complemented Crandall’s8 pioneering work in chronic depth electrode recordings. An amalgam of Falconer’s demonstration of anatomic abnormalities and Crandall’s analysis of corresponding electrophysiological characteristics has founded our current comprehension of temporal lobe epilepsy. The more complex electrophysiology responsible for extra-temporal epilepsy has partly delayed our more detailed understanding of mechanisms involved in extra-temporal epilepsy syndromes.
Other surgical procedures for epilepsy Hemispherectomy was initially described by Dandy in 1928 for gliomas, and used by Krynauw9 in 1950 for children with epilepsy and infantile hemiplegia. As was mentioned previously, Rasmussen described ‘functional hemispherectomy’ which further minimized the complications associated with an anatomic hemispherectomy. Based on Horsley’s and Erickson’s observations regarding the importance of corpus callosum in transferring epileptic discharges between hemispheres, Van Wagenen and Herron performed the first corpus callosotomy in 1940.
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A brief history of epilepsy surgery in the United States As the first part of the 20th century demonstrated the efficacy of epilepsy surgery; the second part of century defined who would be likely to benefit most from surgery and also expanded the repertoire of surgical technique: callosotomy,10 focal cortical resection,11 multiple subpial transactions.12 Multiple subpial transaction was first described in 1989.12 The technique has been applied successfully to epilepsy foci in eloquent cortex by severing the ‘horizontal’ or traversing fibers while preserving the descending fibers, therefore; isolating the route of seizure spread. In addition, application of intracranial monitoring strategies has made epilepsy surgery available for patients with focal epilepsy and non-structural abnormalities. Other procedures such as vagus nerve stimulation (VNS) (approved in 1997) has been used for patients with generalized seizures who have typically bilateral or non focal epileptiform activity on EEG and are not candidates for resective surgery. The mechanism of action of VNS is not known, but it may reduce seizure frequency with a similar efficacy as those of new generation of anticonvulsant drugs. Another new procedure for intractable generalized seizures is deep brain stimulation in the anterior nucleus of thalamus.13 The anterior thalamus is known to play a role in seizure propagation. This is a novel treatment for patients with generalized seizures, who are not typically candidates for resective surgery. The future treatments in epilepsy will depend on a better understanding of the cellular phenomenon and networks involved in seizure generation.
Neuroimaging and epilepsy The evolution of imaging modalities has significantly expanded the application of surgery through improved localization of seizure foci. In 1930s, Penfield used ventriculography, pneumoencephalography and angiography to evaluate epileptogenic mass lesions. MRI scanning was a significant
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advance due to its high resolution of soft tissues revealing anatomic details and pathologic signal changes with striking clarity. Multiplanar imaging allowed visualization of medial temporal and neocortical structures in anatomically useful cross sections.14 With the advent of MRI, there was a preoperative correlate to EEG. Hippocampal sclerosis and atrophy on the side of seizure origin was found to effectively predict seizure remission.15 Furthermore, the degree of hippocampal resection was found to affect seizure outcomes.16 Further evolution of imaging modalities including functional MRI, positron emission tomography and single photon emission computed tomography have further facilitated delineation of more subtle areas of structural and metabolic abnormality. Regions of electrographic abnormality have become correlated with areas of radiographic abnormality as disclosed by magnetic resonance imaging. Localization of a ‘seizure generator’ by two independent methods has improved the likelihood of obtaining a surgical cure. Functional imaging coregistered with structural and electrographic data has become an important tool in epilepsy surgery.17
Conclusions In the present chapter, we reviewed an abbreviated history of epilepsy surgery in the United States. We highlighted the milestones in the development of epilepsy surgery which began with an understanding of cortical electrical activity and its role in epilepsy. Advances in electrical localization, beginning with scalp EEG recordings and shortly followed by cortical and depth recordings, have enhances our preoperative localizing power, significantly increasing the effectiveness of epilepsy surgery. Further improvement in our treatment paradigms is possible with multicenter trials and understanding the networks and molecular basis of epilepsy.
REFERENCES 1. 2. 3. 4. 5. 6. 7. 8. 9.
Holmes G. Evolution of clinical medicine as illustrated by the history of medicine. BMJ 1946;2:1–4. Dudley D. Observations on injuries of the head. Transylvania J Med 1828;1:9–40. Gibbs E, Gibbs F, Fuster B. Psychomotor epilepsy. Arch Neurol Psychiatry 1948;60:331–9. Bailey P. Surgical treatment of psychomotor epilepsy: five year follow-up. South Med J 1961;54:299–301. Walker A. Stereotaxic methods for the study of subcortical activity in epilepsy. Confin Neurol 1962;22:217–22. Ward A, McCullough W, Kopeloff N. Temporal and spatial distribution of changes during spontaneous seizures in monkey brain. J Neurophysiol 1948;11:377. Ward A, Thomas L. The electrical activity of single units in the cerebral cortex of man. Electroencephalogr Clin Neurophysiol 1955; 7:135–6. Babb T, Mariani E, Crandall P. An electronic circuit for detection of EEG seizures recorded with implantd electrodes. Electroencephalogr Clin Neurophysiol 1974;37:305–8. Krynauw R. Infantile hemiplegia treated by removing one cerebral hemishphere. Neurol Neurosurg Psychiatr 1950;13:243–7.
10. 11. 12. 13. 14. 15. 16. 17.
Wilson D, Reeves A, Gazzaniga M. Division of the corpus callosum for uncontrollable epilepsy. Neurology 1978;28:649–53. Palmini A, Anderman F, Olivier A, Tampieri D, Robitaille Y. Focal neuronal migration disorders and intractable partial epilepsy: results of surgical treatment. Ann Neurol 1991;30:750–7. Morrell F, Whisler W, Bleck T. Multiple subpial transaction: a new approach to the surgical treatment of focal epilepsy. J Neurosurg 1989;70:231–9. Hodaie M, Wennberg R, Dostrovsky J, Lozano A. Chronic Anterior Thalamus Stimulation for Intractable Epilepsy. Epilepsia 2002; 43:603–8. Diaz-Arrastio R, Agostini M, VanNess P. Evolving treatment strategies for epilepsy. JAMA 2002;287:2917–20. Jack C, Sharbrough F, Twome C, et al. Temporal lobe seizures: lateralization with MR volume measurement of the hippocampal formation. Radiology 1990;175:423–9. Wyler A, Hermann B, Richey E. Extent of medial temporal resection on outcome from anterior temporal lobectomy: a randomized prospective study. Neurosurgery 1995;37:982–91. Kuzniecky R. Neuroimaging of epilepsy: advances and practical applications. Rev Neurol Dis 2004;1:179–89.
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Epilepsy surgery in Latin America J Godoy, AC Sakamoto, and ALF Palmini
Although waxing and waning, interest in epilepsy surgery appeared in Latin America shortly after this therapy was introduced by Penfield’s pioneering work at the Montreal Neurological Institute. The first systematic resective surgeries for epilepsy were performed in the region in the 1940s.1 For decades, this treatment was used mainly in isolated, anecdotal cases or performed in very small series, having included almost all its modalities: temporal and extratemporal resections, hemispherectomies, callosotomies, lesionectomies, stereotaxia, and amigdalo-hippocampectomies.2–4 During the last 15 years several systematic epilepsy surgery programs have been established in the region, including some centers that use advanced techniques. However many Latin-American countries still have not performed any epilepsy surgery and some even lack the facilities for a complete patient presurgical evaluation. As in the rest of the world, the actual number of epilepsy surgeries represents a very small fraction of the total number of patients that need this type of therapy. Certainly one of the main challenges on this regard is to make this treatment available to the whole region. Three are two major difficulties for the development of epilepsy surgery in Latin America. The first is economical limitations and the second the unawareness of the usefulness of surgical treatment and its proper timing within the neurological and neurosurgical community. Although unified by a common language and socio-cultural roots, Latin America is a continent where healthcare systems coexist with major differences not only between countries but also within a same country. According to World Bank data,5 per capita income in Latin America ranges from US$400 in Haiti to US$6,230 in Mexico, while health expenditure per capita ranges from as low as US$29 per year in Haiti up to US$361 per year in Uruguay, compared to US$5,274 in the USA. This latter figure is higher than the total per capita income of almost all countries in the region. The impact of the economical development on epilepsy care is shown by the fact that the five countries with the highest income in the region have established epilepsy surgery programs while none of the five poorest countries have them. In this context of economical constraints it is easy to understand that there are quite a number of priorities that compete for health resources and explains why epilepsy surgeries are virtually nonexistent in public health systems in the region, with very few exceptions. On this regard, a major political step in favor of the development of epilepsy surgery in Latin America was made on September 9, 2005, in Santiago, Chile, where the ‘LatinAmerican Declaration on Epilepsy’ was read on behalf of several international organizations, including ILAE, IBE, WHO, and UNICEF, as part of the ‘Epilepsy out of the Shadows’ global campaign. This declaration included a statement calling 118
to warrant availability and access to ‘surgery and all forms of effective treatments’.6 Even more critical than the economical restrictions is the need for well-trained medical professionals who not only make epilepsy surgery programs technically feasible but also inform and teach local and regional neurological communities about this modality of therapy, and promote changes in healthcare systems for setting up the epilepsy surgery programs. Indeed all current epilepsy surgery centers in the region are led by epileptologists and neurosurgeons trained at top world-class epilepsy centers, mainly the Montreal Neurological Institute and the Cleveland Clinic. Probably the best contribution first-world epileptologists can do for the further development of epilepsy surgery in Latin America is to train physicians and other professionals in the different disciplines needed in this field.
Precursors Before the development of modern neurophysiological techniques, surgery was performed in Latin America mainly for post-traumatic epilepsy.2,7 Usually, the site of an obvious structural lesion or simply the site of a head injury was selected for resection. Preoperative investigations were very limited because no EEGs were performed. Some patients were operated on based only on clinical history and plain skull X-ray findings (fractures, depressions, etc.). It is surprising to know that this approach was occasionally used in Latin America as early as the end of the 19th century. Razetti et al., in Venezuela, and Maldonado et al., in Colombia, operated on patients with jacksonian post-traumatic epilepsy, in 1893 and 1897, respectively;8 in 1894 Navarro,9 in Montevideo, Uruguay, operated on a patient who developed frequent seizures after a head injury with a skull depression. He used a silver plate as a craneoplasty; the patient developed a right hemiplegia and remained with seizures for a few days, improving afterwards and being able to return to work 6 weeks later.
Argentina The first systematic epilepsy surgery attempts were made almost 50 years ago in this country. In 1957, Ghersi et al.10 reported a series of 25 patients with no demonstrable structural lesion who underwent temporal lobectomies or gyrectomies based on clinical history, surface EEG, and intraoperative corticograms (performed before and after the
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Epilepsy surgery in Latin America initial resections in all cases). Although all patients improved significantly (40–80% seizure reduction), none was completely cured; their series also included some hemispherectomies which had good outcomes. Pardal et al.11 performed stereotaxic surgery on six epileptic patients in 1960 and reported good outcome in all of them. A few years later the group of Basso and Betti,3 from the University of Buenos Aires, using Bancaud and Talairach’s technique, implanted electrodes for acute or chronic recordings in 61 patients, 36 of whom had temporal lobe epilepsy. They explored the amygdala, hippocampus, temporal cortex, thalamus, and other structures; in some patients they produced thalamic injuries and in others they destroyed epileptogenic areas with yttrium (Y-90) or performed amygdalo-hippocampotomy. Unfortunately, detailed preoperative and follow-up protocols were not provided. These authors also used combined surgical approaches, which included stereotaxic treatment for temporal lobe epilepsies and, in case of failure, topectomy of the affected cortex or temporal lobectomy.3 In 1977 Chescotta et al.12 reported a group of 62 epileptic patients on whom amygdalotomies and fornicotomies were performed; a significant improvement was obtained in 66% of the patients. Costales and Ferrarese13 from Bahía Blanca, Argentina, presented a case report on a patient with a refractory status epilepticus successfully treated with temporal lobectomy. Nowadays, there are four groups performing epilepsy surgery in Argentina. The group of Pomata, working in Buenos Aires at Juan P. Garrahan National Pediatric Hospital and at the FLENI Institute, started epilepsy surgery in 1995 (Pomata H, personal communication). Up to 2005 their series included 158 temporal and 139 extratemporal lobe surgeries, 34 hemispherectomies (2 of them anatomical), 35 callosotomies, and 13 vagal nerve stimulators. These authors reported part of their experience in 2001,14 describing 60 children with extratemporal epilepsies, treated with resections, disconnections, and in one case, hemispherectomy; 10 of these patients underwent invasive evaluations; the one year follow-up showed that 38 patients were on Engel’s class I. They also presented a small group of patients with Rasmussen encephalitis who underwent hemispherectomy,15 and additionally described a 6 year-old child with refractory status epilepticus successfully treated with multiple subpial transection.16 Another epilepsy surgery program in Buenos Aires is located at the Hospital Italiano where Rabadan et al. have performed epilepsy surgery since 1999. They reported part of their series in 2000.17 As of 2005 they have operated on 35 adult patients, including temporal and extratemporal resections as well as callosotomies (Rabadan A, personal communication). Also in Buenos Aires, at the Ramos Mejia Hospital, Kochen, Silva, Seoane, and Consalvo continued the work of Basso and Betti.18 They introduced Video-EEG monitoring in 1996, invasive studies in 2001, and started extratemporal resections in 2003. They have also performed some callosotomies and vagal nerve stimulation since 2001 (Kochen S, personal communication). Outside the capital city, epilepsy surgery has been performed in two provinces. One in the northern city of Cordoba, where Bulacio, Sfaello, and Mu~ noz started an epilepsy surgery program at The Santisima Trinidad Children’s hospital and at the Center for the Study and Treatment of Epilepsy and Sleep Disorders (Bulacio J, personal
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communication); they have practiced temporal and extratemporal resections in a small group of patients since 2004. In Mendoza city, the above-mentioned neurosurgeon Pomata has also performed temporal and extratemporal resections in children (Pomata H, personal communication).
Bolivia In this country, cortical resections were reported in post-traumatic epilepsies by Enriquez in 1959.7 In his series, no EEG recordings were practiced and therefore patients were operated on based only on clinical history and plain skull X-ray findings, mainly guided by fractures and depressions. This same author also described the use of suboccipital pneumoencephalography for treating epilepsies after central nervous system infections, but no controlled results were reported.7 There are currently no established epilepsy surgery programs in Bolivia not are these known surgical treatment attempts in the past.
Brazil In the largest Latin-American country interest in epilepsy surgery goes back to the 1950s, and the most important and original contribution from the Brazilians to this field was made by the neurosurgeon Paulo Niemeyer Soares, one of the founders of the Brazilian League against Epilepsy, who also made contributions in several other neurosurgical pathologies, including Parkinson’s disease surgery (Figure 14.1).19 Niemeyer, who started to work at the Santa Casa de Misericordia Hospital, in Rio de Janeiro, initially as a general surgeon, was the first to propose and to perform amygdalohippocampectomies for the treatment of temporal lobe epilepsy. He used a transventricular approach, a technique that he presented for the first time in Washington in 1957, and later described in more detail in a book chapter.20 In 1973 his group presented a
Figure 14.1 Dr Paulo Niemeyer Soares, brazilian neurosurgeon who first described amygdalohippocampectomy in 1957 (courtesy of Americo Sakamoto, MD).
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series of 42 patients who underwent amygdalohippocampectomies,4 reporting satisfactory results in 74% of the patients, after a follow-up period ranging from 6 months to 10 years; this figure was similar to the one the same group had obtained in 35 temporal lobectomies with resections tailored according to post-ablation electrocorticographic recordings. In order to better understand the meaning of post resection epileptiform discharges he eventually left in place tiny copper electrodes over the operated cortex and performed post-surgical recordings.19 These electrodes were externalized through small trepanation holes and after finishing the recordings were simply pulled out. With this technique, he soon realized that there was an immediate post-operative worsening of the frequency of epileptiform discharges, an effect that vanished in hours or a few days. Many years later this finding was replicated in a prospective study by Cendes et al.,21 in a group of amygdalohippocampectomy patients; these authors coined the term ‘Niemeyer effect’ to describe this phenomenon. Niemeyer and his group also performed the first electrocortical recordings in Brazil in the early 1950s, using a single channel Garcier electroencephalograph.19 While Niemeyer’s pioneering work in the field of epilepsy surgery was developed as part of his extensive practice as a general neurosurgeon, more recent initiatives in Brazil already embraced the idea of a comprehensive epilepsy surgery program, involving a multidisciplinary team including neurologists, neurosurgeons, psychologists, technologists, and more recently, neuroradiologists, psychiatrists, social workers, and physicists. According to this principle the first Brazilian epilepsy surgery center was established in the 1970s, at the Hospital das Clinicas da Universidade de S~ ao Paulo, in the city of S~ ao Paulo, led by neurosurgeon Raul Marino Jr., who started a program mainly focused on treating diffuse epileptic encephalopathies through corpus callosotomy.22 In the 1980s the second epilepsy surgery center was implemented at the Instituto Neurologico de Goiânia, led by neurologist Paulo C. Ragazzo, who was trained at the MNI and had previously participated in the team from the Hospital das Clinicas da Universidade de S~ ao Paulo. It was really in the 1990s that the field of epilepsy surgery experienced major developments in Brazil. Two major reasons were of paramount importance in this move to provide the country with epilepsy surgery centers at the level of firstclass centers of the developed world, not only in terms of infrastructure and methodologies, but also in terms of results for both adult and pediatric patients.23,24 The first reason was the return to Brazil of well-trained physicians who established new epilepsy surgery centers and introduced state-ofthe-art methodologies for the presurgical evaluation and selection of surgical candidates, as well as for the surgical treatment itself. Two new centers were implemented in that decade, one at the Pontificia Universidade Católica, in Porto Alegre, in the early 1990s, under the leadership of the neurologists André L.F. Palmini (trained at the MNI) and Jaderson C. da Costa (trained in pediatric neurology at Boston Children’s Hospital), and the second at Hospital das Clinicas de Ribeir~ ao Preto, Universidade de S~ ao Paulo, in Ribeir~ ao ~ Preto, State of S ao Paulo, in the mid 1990s, under the leaderships of the neurologist Américo C. Sakamoto (trained at The Cleveland Clinic Foundation, Cleveland, USA, and Epilepsy Center Bethel, Bielefeld, Germany) and neurosurgeon Jo~ ao A. Assirati Jr. (extensive neurosurgical training in various
centers in the USA). The second and more important reason was the establishment of a national epilepsy surgery program in 1994, within the public health system, sponsored and coordinated by the Health Department. This program was created after joint effort from the Brazilian League of Epilepsy, the Brazilian Society of Clinical Neurophysiology, and the Brazilian Society of Neurosurgery, all of them active participants of a committee named directly by the Minister of Health. The main objectives of this committee were three-fold: (a) to establish a nationwide epilepsy surgery program, (b) to implement internationally accepted medical standards, and (c) to compromise maximal resources and minimal costs. In order to achieve these goals a two-steps strategy was implemented, which included strict criteria for accreditation of epilepsy surgery centers based on minimal requirements and clearly defined guidelines for indication of epilepsy surgery (temporal and extratemporal resective surgery, hemispherectomy and callosotomy). After completion of the first 10 years of experience (1994–2004), the program was shown to be highly successful in many different aspects. It started out in 1994 with three initially accredited centers (Hospital das Clinicas da Universidade de S~ ao Paulo – S~ ao Paulo, Instituto Neurologico de Goiânia – Goiânia, and Hospital S~ ao Lucas da Pontifícia Universidade Católica – Porto Alegre), and progressively expanded to the current eight centers distributed in different geographical regions, seven of them connected to academic institutions dedicated not only to medical assistance but also to education and research. In recent years many other epilepsy surgery centers were established and reached accreditation status: at the Hospital das Clinicas da Universidade Estadual de Campinas, in Campinas, under the leadership of the neurologist Fernando Cendes who was trained at the MNI, at the Hospital da Universidade Federal de S~ ao Paulo, in S~ ao Paulo, under the leadership of neurologists Américo C. Sakamoto and Elza M. T. Yacubian (trained at the National Institutes of Health, Bethesda, USA), at the Hospital das Clinicas da Universidade Federal do Paraná, in Curitiba, under the leadership of the neurologists Luciano de Paola (trained at the University of Minneapolis) and Carlos S. Silvado; and at Hospital Regional, in S~ ao José do Rio Preto, under the leadership of neurologist Lucia H. Marques (trained at Universidade Estadual de Campinas). Other emerging centers are currently applying for accreditation as epilepsy surgery centers, in an organized process led by the Health Department. The nationwide implementation of this program was able to assure universal access to epilepsy surgery in Brazil, to increase 13 times the total number of epilepsy surgery per year, to increase 2.7 times the number of epilepsy surgery accredited (or in final stages to be accredited) centers, to increase 5 times the number of surgeries per center per year, to boost the scientific development in the field of epileptology, and equally important, to create a network of centers with full capacity of training young Brazilian professionals in the area of epilepsy surgery, warranting the expansion and continuity of the program in the country, and consequently, the future of epilepsy surgery in Brazil.
Chile In this country there is also a lengthy history on epilepsy surgery. Alfonso Asenjo, who is recognized as one of the founders
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Epilepsy surgery in Latin America of Latin American neurosurgery, was actively involved in promoting this therapy more than 50 years ago. He established in 1950 the Instituto de Neurocirugía e Investigaciones Cerebrales de Chile (currently The Asenjo Institute), one of the first teaching and investigation centers in neurosurgery in Latina America, where hundreds of neurosurgeons have been trained, from Chile and other South and Central American countries. Asenjo worked with Carlos Villavicencio, a neurophysiologist trained in Montreal between 1939 and 1941 under Wielder Penfield25 and who started electroencephalography in Chile in 1944, in a room called ‘Hans Berger’, at the Instituto de Neurocirugía, in Santiago. In 1951 they published,2 a series of 221 epilepsy surgery patients, although only 96 of their patients had lesions without surgical indication per se, most of them frontal and mainly post-traumatic. Preoperative investigations included repeated surface electroencephalograms (EEGs), plain skull X-rays, cerebral angiograms, pneumoencephalograms, and ventriculograms; intraoperative corticograms and electrical stimulation were performed for tailoring the resections. The authors reported significant improvement or complete control in up to 69% of the patients. Other surgical procedures were also practiced at that time, such as hemispherectomies, performed in 1954 at the same institution;25 The group continued to perform epilepsy surgery for some years but with a progressive decay in interest. A new impulse came at this center in 1990 when a pediatric epilepsy surgery program started, under the leadership of Lilian Cuadra. Up to 2004, they have operated on more than 100 children, mainly using temporal lobectomies and callosotomies (Cuadra, personal communication), entirely supported by public funds. Another center with a long history in epilepsy surgery in Chile is the Hospital de la Universidad Catolica, where epilepsy surgery was initiated in 1962 led by Cristian Vera, a neurosurgeon trained at the Montreal Neurological Institute from 1956 to 1961; anecdotically, he had the opportunity to assist in the last epilepsy surgery that Penfield performed at the MNI. In Chile, Vera himself not only performed the surgery but also the electrocorticograms, using a portable eightchannel Hofner equipment, going back and forth from the operation table to the EEG machine. His group, that included Luis F. Quesney as a novel student, who later became a distinguished epileptologist, performed both temporal and frontal resections as well as hemispherectomies. Patients were also evaluated with surface EEG, skull X-rays, pneumoencephalography and an amytal test (Vera, personal communication). They also operated at the Hospital Psiquiatrico in Santiago, to where they eventually moved the only EEG machine they had. In some patients, before the resections, they made recordings from the amygdala, using implanted gold electrodes while at the same time tested memory. Again, interest decayed and no epilepsy surgeries were performed for almost 20 years, until 1990, when a new program was started by the neurophysiologist Godoy, trained at the Cleveland Clinic, and the neurosurgeon Torrealba;26 this program had an additional impulse in 1996, when Campos, neurosurgeon trained in Bonn, joined the group. At this center temporal and extratemporal resections are performed and patients undergo prolonged Video EEG monitoring, and when needed, evaluation with subdural grids or foramen ovale electrodes.27,28 In addition to high resolution MRI,
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SPECT (ictal and interictal) are performed and more recently PET scanning. Several stereotaxic techniques were used in the past both at the Asenjo Institute and at the Santiago’s Psychiatric Hospital.29 In this latter center this epilepsy surgery was performed in the 1960s and 1970s, led by Mario Poblete (L. Aranda, personal communication).
Colombia In Colombia, Sierra et al.30 reported in 1960 a Sturge– Weber–Dimitri patient with intractable epilepsy, successfully treated with hemispherectomy; he had no seizure recurrence, even after complete anti-convulsant withdrawal. GutierrezLara et al.31 performed stereotaxic surgery in 15 children between 1973 and 1976. Patients underwent Forel campotomy, amygdalotomy and, in those with associated hyperkinetic syndrome (probably meant attention deficit disorder), hypothalamotomy; they described good results in 8 patients, with a 6–18 month follow up. One of the largest, oldest and most significant epilepsy surgery program in Latin America has been developed in Cartagena de Indias, Colombia by Jaime Fandi~ no-Franky.32,33 It is worth mentioning that a huge personnel effort has been put by Fandi~ no-Franky, who has been able to overcome all kind of difficulties and established a comprehensive epilepsy program supported by non-governmental entities for more than 20 years. In 1996, an international workshop on specific aspects of epilepsy in the developing world was organized by ILAE Commission of Epilepsy in Developing Countries, during which it was stated that ‘Fandino-Franky inspired the entire Workshop when he described his experiences’.34 He was trained in Sweden and shortly after his return to Colombia got actively involved in epilepsy. Fandi~ no-Franky performed the first anatomical hemispherectomy in Colombia in 1981 and in 1989 founded an epilepsy hospital (Hospital Neurologico) that belongs to the Colombian League Against Epilepsy; the same year his group performed the first callosotomy and the first anterior temporal lobectomy. As of 2005 they have performed 680 epilepsy surgery procedures, including temporal and extratemporal resective surgeries, callosotomies, hemispherectomies (anatomical and functional), multiple subpial transections etc. This comprehensive program also includes a nicely developed rehabilitation program (Fandi~ no-Franky, personal communication). Other efforts have also been made in Colombia. In Bogotá, Nari~ no et al. developed an epilepsy surgery at the Hospital Central de la Policía and at the Palermo Clinic. They have already operated on 45 patients, including some with invasive studies (Nari~ no, personal communication).
Costa Rica Epilepsy surgery has been performed only recently in Costa Rica. Sittenfeld and his group at the Hospital Doctor Carlos Saenz, have operated on 45 children since 200l. the group includes callosotomies, temporal lobectomies and extratemporal resections; some patients required invasive studies. At 2-year follow-up the authors report Engel’s class I outcome
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in 2/3 of their patients, both temporal and extratemporal groups as well as significant seizure reduction in 8/17 callosotomies practiced on children (Sittenfeld, unpublished work).
Cuba An epilepsy surgery program was created in 2000, at the International Center for Restorative Neurology (CIREN) in Havana,35 where they have started to perform video-EEG monitorings in 2000; the first surgical procedures, temporal resections, began in 2002 and later a few callosotomies have been performed. The medical team, which includes neurophysiologists, epileptologists, neuropsychologist, and neurosurgeon, was trained at the MNI. Patients are evaluated with surface video-EEG monitoring, neuroimaging, and SPECT; Wada tests are not performed (Bender, personal communication).
Dominican Republic In this country there were no known epilepsy surgery treatments in the past. Since 2003 Video-EEG monitoring has been practiced at the Corazones Unidos Clinic, in Santo Domingo City where anecdotical extratemporal resections have been performed recently (Santos-Viloria, personal communication).
Ecuador There has been no known epilepsy surgeries performed in Ecuador. Just recently Video-EEG monitoring was started at the ‘Hospital Metropolitano’, in Quito, the capital city, by the epileptologists Abad and Pesantes and the neurosurgeon Varsallo, trained in epilepsy surgery in Freiburg, Germany (Pesantes J, personal communication).
Mexico The first communications about epilepsy surgery in Mexico date back to the early 1950s and were performed by Manuel Velasco Suarez, one of the most distinguished Mexican neurosurgeons. In 1951 he founded the Mexican League Against Epilepsy and later, in 1964, the National Institute of Neurology and Neurosurgery (Mexico City).36 Later, a pioneering work on deep brain stimulation has been developed since the mid-1980s by two other neurosurgeons, Francisco and Marcos Velasco, from the Instituto Mejicano de Seguridad Social Medical Center. They proposed centromedian median thalamic nuclei stimulation for the treatment of patients with intractable generalized tonic-clonic seizures,37–39 using this therapy for up to 2 years, through a special device they had developed; they described good outcomes in generalized seizures but not in generalized tonic nor complex partial seizures. These same authors also reported the use of subacute electrical hippocampal stimulation, with either depth or subdural electrodes, in 10 patients who had withdrawn anticonvulsants for 48–72 hours; after a stimulation period of 2–3 weeks the patients underwent anterior temporal resections. With this method seizures were abolished in
seven of these patients and even the interictal spiking was reduced significantly.40 The Velascos have also reported on the use of bilateral cerebellar stimulation in a group of five refractory epilepsy patients, in a double-blind controlled study which used the same patients as controls, and obtained a statistically significant seizure reduction.41 An epilepsy surgery program that uses a more conventional approach was established in Mexico City, at the National Institute of Neurology and Neurosurgery, where temporal and extratemporal resections are performed, using intraoperative electrocorticography and cortical stimulation whenever appropriate. A 2-year follow-up report of 100 resective surgeries in temporal lobe epilepsy was presented in 2004, showing seizure free outcome in 84% of the patients.42 At this center, vagal nerve stimulation was also implemented for refractory epilepsy in 2001.43 Pella et al., also in Mexico City, established an epilepsy surgery program at the Angeles del Pedregal Hospital in 1995. They have performed more than 100 surgeries, in both children and adults, including temporal and extratemporal lobectomies, callosotomies, and radiosurgical procedures (Pella et al., personal communication). Recently epilepsy surgery has been developed at the Instituto Potosino de Neurociencias, in San Luis de Potosí. Villalobos et al.44 reported their experience in a group of 40 patients, children and adults, who underwent resective surgery.
Peru Esteban Rocca, a neurosurgeon trained under the Chilean Alfonso Asenjo in the 1940s, founded the Neurosurgery Unit at the Hospital Obrero in Lima in 1947.45 Working with Juan Franco, a neurosurgeon trained in Chile and the USA, he performed resective surgeries in 1955, using corticograms as guidance.46 However, details of the surgical procedures and results were not presented. In Arequipa, a southern Peruvian city, Ortega and Gamero47 in 1973 reported on 30 intractable patients with generalized seizure disorders that were treated with surgical section of the genu of the corpus callosum and anterior white commissure; significant improvement or complete control was achieved in 90% of these patients. No epilepsy surgery programs are currently established in Peru.
Uruguay Alejandro Schroeder, the founder of Uruguayan neurosurgery, introduced the EEG and initiated epilepsy surgery at the Instituto Neurologico in Montevideo. He was initially trained in central nervous system histology in Hamburg, Germany and later he had the chance to work with Ostrid Fester in Breslau; after this latter experience he became interested in neurosurgery, starting his practice in 1930.9 In 1949 he reported the first Latin-American series on lesionectomies at the Third South American Neurosurgery Congress held in Buenos Aires, Argentina.1 It included ten patients studied preoperatively with surface EEG and cerebral angiograms; intraoperative electrocorticography was also performed and used as the main criterion for guiding surgery, since resections were done only when corticograms showed spikes, which was the case in the seven patients. The authors stated
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Epilepsy surgery in Latin America that, after clinical and EEG studies, ‘we mark on the skin the epileptic focus as exactly as possible’. Also in Montevideo, Arana I~ niguez, a neurosurgeon trained in Santiago, Chile, and Boston, USA performed one of the earliest hemispherectomies in Latin-America.9 In 1961, Bogacz et al.48 studied 62 patients with unilateral temporal lobe foci, using nasopharyngeal and sphenoidal electrodes. Seven of these patients underwent invasive studies with deep electrode threads for 24 hours, followed by temporal lobectomy. As has happened in many other countries, no further epilepsy surgeries were performed for decades and only recently has an epilepsy surgery program been started in Montevideo at the Instituto de Neurologia del Hospital de Clínicas, led by Alejandro Scaramelli. Up to date they have performed 17 temporal lobectomies using non-invasive techniques (Scaramelli, personal communication).
Venezuela Arminio Martinez et al.49 working at the José María Vargas Hospital, in Caracas, the capital city, started temporal lobectomies in 1955, following the Montreal Neurological Institute approach, including the use of intraoperative electrocorticography and electrical stimulation; up to 1972 they had operated on 13 patients, reporting complete control in 9 and improvement in 2 patients. The same group performed the first hemispherectomy in Venezuela in 1959. After several decades Scholtz and Ponce, at the same Vargas Hospital, performed some other epilepsy surgery procedures. In 2000, Soto, et al. established a new epilepsy surgery program, working at the Domingo Luciani University Hospital and the Floresta
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Medical Institute where they have performed temporal and extratemporal resections, callosotomies, and vagal nerve stimulations (Soto, personal communication).
Concluding remarks The history of epilepsy surgery in Latin America parallels the rest of the world. Very early attempts to develop this therapy following the Montreal Neurological Institute’s approach can be found in several countries of the region. The pioneering work of the Brazilian neurosurgeon Paulo Niemeyer Soares, who proposed almost 50 years ago the selective amygdalohippocampectomy, a technique still used nowadays, is a good example of the interest Latin America has historically shown in epilepsy surgery. More recently in the region, epilepsy surgery has followed the extraordinary development in first-world countries, including the area of neuroimaging. Unfortunately, Latin America has also great diversity in the organization of the health system and the breach between the number of patients needing epilepsy surgery and the actual amount of surgeries performed is certainly much larger than in developed countries. Only Brazil has a nationwide epilepsy surgery program and this experience, in this respect, probably has unique features, due to its universality (available to every citizen independent of socioeconomic status), high medical standards at minimal costs (strict definitions of human and technical requirements, and surgical protocols), and a controlled and organized accreditation system (supervised by Health Department and medical societies) which could be seen as an example not only for developing but also to developed countries.
REFERENCES 1. 2. 3. 4. 5. 6.
7. 8. 9. 10. 11. 12.
Schroeder A, Arana R, Fuster B, San Julian J. Contribución al tratamiento quirúrgico de la epilepsia. Actas III Congreso Sudamericano de Neurocirugía 1949;272–3. Asenjo A. Villavicencio C, Contreras M, Fierro J. Estado actual del tratamiento quirúrgico de la epilepsia. Neurocirugía 1951;8:86–130. Basso AA, Betti OO, Clucellas JL, et al. Stereo electroencephalography in temporal epilepsy. Acta Neurol Latinoamer 1969;15:72–86. Amygdalohippocampectomy for temporal lobe epilepsy. Excerpta Medica 1973;293:20. 2005 World Development Indicators. The World Bank. Available from http://devdata.worldbank.org/wdi2005. Devilat M. Conduciendo a la epilepsia fuera de las sombras. Declaración para la epilepsia en Latinoamérica. In: Campos M, Kanner A, Eds. Epilepsias. Diagnóstico y tratamiento 847–52. Mediterráneo: Santiago, 2004. Enríquez N. Nuestra experiencia en el tratamiento quirúrgico de la epilepsia post traumática. In: Homenaje a Alfonso Asenjo Gómez. Lima: Médica Peruana. 1959:38–56. Christiansen JC. History of neurosurgery in South America. Acta Neurol Latinoamer 1962;8:63–76. Wilson E. Historia de la neurocirugía en Uruguay. In: Mendez J. ed. Historia de la Federación de Sociedades Latinoamericanas de Neurocirugía 332–62. Barlovento: Santiago, 2002. Ghersi JA, Piaquadio N, Costales A. Nuestra experiencia electroencefalográfica en las epilepsias temporales. Actas VII Congreso Latinoamericano de Neurocirugía 1957;345–6. Pardal E, Morete de Pardal ML, Betti O. Cirugía estereotáxica de la epilepsia en los ganglios de la base. Anales de Neurocirugía 1960;5:9–23. Chescotta AR, Gotusso C, Stella O, Chinela A. Stereotaxic surgery for epilepsy. Excerpta Medica 1977;418:224–5.
13. 14. 15. 16. 17. 18. 19. 20.
21. 22.
23.
Costales A, Ferrarese L. La indicación quirúrgica en el estado de mal epiléptico focal irreversible. Neurocirugía 1960;18:387–94. Pomata HB, Gonzalez R, Bartuluchi M et al. Extratemporal epilepsy in children: candidate selection and surgical treatment. Child Nerv Syst 2000;16:842–50. Caraballo R, Tenembaum S, Cersosimo R et al. Rasmussen syndrome. Rev Neurol. 1998;26:978–83. D’Giano CH, Del C Garcia M, Pomata H, Rabinowicz AL. Treatment of refractory partial status epilepticus with multiple subpial transection: case report. Seizure 2001;10:382–5. Rabadan A, Baccaneli M, Consalvo D et al. Cirugía de la epilepsia refractaria. In: Devilat M, ed. La Epilepsia en Latinoamérica 276. Editorial Iku: Santiago, 2000. Silva W, Consalvo D, Solis P et al. Results of the temporal lobe epilepsy surgery in a developing country. Epilepsia 2002;43 (suppl 7):334. De Paiva Bello, H. Homenagem ao Dr. Paulo Niemeyer. J Epilepsy Clin Neurophysiol 2004;10:241–4. Niemeyer P. The transventricular amygdalohippocampectomy in temporal lobe epilepsy In: Baldwin M, Bailey P, and Eds. Temporal Lobe Epilepsy 461–82. Charles C Thomas: Springfield, Ill, 1958. Cendes F, Dubeau F, Olivier A et al. Neocortical spiking and surgical outcome after selective amygdalo-hippocampectomy. Epilepsy Res 1993;16:195–206. Huck F, Radvany J, Camargo CHP et al. Anterior callosotomy in epileptics with multiform seizures and bilateral synchronous spike and wave EEG pattern. Acta Neurochirurgica 1980;30 (suppl): 127–35. Paglioli E, Palmini A, Paglioli E et al. Analysis of the surgical outcome of temporal lobe epilepsy due to hippocampal sclerosis. Epilepsia 2004;45:1383–91.
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Textbook of epilepsy surgery Terra-Bustamante VC, Inuzuka LM, Fernandes RMF, et al. Surgically amenable epilepsies in children and adolescents: clinical, imaging, electrophysiological, and post-surgical outcome data. Childs Nerv Syst 2005;21:546–71. Nevens V. Inicios de la electroencefalografía en Chile. Rev Chil Epilep 2000;1:29–31. Torrealba G, Godoy J. Cirugía de la epilepsia. Cuándo, cómo y porqué. Rev Chil Neuropsiq 1989;43:239–45. Godoy J, Torrealba G, Aranda L, et al. Foramen ovale electrodes in the study of temporal lobe epilepsy. Rev Med Chil. 1992;120:134–9. Campos MG, Godoy J, Mesa MT, et al. Temporal lobe epilepsy surgery with limited resources: results and economic considerations. Epilepsia 2000;41 (suppl 4):S18–S21. Chiorino R, Donoso P, Díaz G, Aranda L, et al. Consideraciones sobre cirugía estereotáxica en el tratamiento de la epilepsia a propósito de una nueva técnica: la campotomía. Neurocirugía 1966;26:143–7. Sierra R, Bustamante E. Hemisferectomía en un caso de enfermedad de Sturge-Weber-Dimitri. Neurocirugía 1960;18:242–5. Gutierrez-Lara F, Alandete J, Vargas L, Díaz L. Stereotaxic surgery in the treatment of epilepsy. Excerpta Medica 1977; 418:225. Fandi~ no Franky J. Low cost Epilepsy Surgery in Colombia. In: Pachlatko Ch, Beran RG, Eds. Economic Evaluation of Epilepsy Management 91–104. Libbey Publishers: London, 1996. Fandi~ no-Franky J. Corpus Callosotomy in Colombia and Some Reflections on Care and Research Among the Poor in Developing Countries. Epilepsia 2000;4l (Suppl. 4):S22–S27. Jallon P. Epilepsy in developing countries. ILAE workshop report. Epilepsia 1997;38:1143–51. Bender JE, García I, Morales L et al. Epilepsy surgery. Preliminary Study. Rev Mex Neuroci 2004;5:239. Carrasco-Rojas JA. Distinción Dr. Clemente Robles Castillo al Dr. Manuel M. Velasco Suárez Humanista Universal. Cir Ciruj 2001;6:316–20. Velasco F, Velasco M, Ogarrio C, Fanghanel G. Electrical stimulation of the centromedian thalamic nucleus in the treatment of
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convulsive seizures: a preliminary report. Epilepsia 1987;28: 421–30. Velasco F, Velasco M, Velasco AL, Jimenez F. Effect of chronic electrical stimulation of the centromedian thalamic nuclei on various intractable seizure patterns: I. Clinical seizures and paroxysmal EEG activity. Epilepsia 1993;34:1052–64. Velasco F, Velasco M, Velasco AL, et al. Electrical stimulation of the centromedian thalamic nucleus in control of seizures: long-term studies. Epilepsia 1995;36:63–71. Velasco F, Velasco M, Velasco AL, et al. Electrical stimulation for epilepsy: stimulation of hippocampal foci. Stereotact Funct Neurosurg 2001;77:223–7. Velasco F, Carrillo-Ruiz JD, Brito F, et al. Double-blind, randomized controlled pilot study of bilateral cerebellar Stimulation for treatment of intractable motor seizures. Epilepsia 2005;46: 1071–81. Castillo MCR, Alonso-Vanegas MA, Brust-Maschere E et al. Institutional experience in one hundred surgically treated temporal lobe epilepsy patients with a follow-up over 2 years. Rev Mex Neuroci 2004;5:236. Alonso-Vanegas MA, Austria VJ, Santiago E. Vagus Nerve stimulation in patients with medically refractory epilepsy. Rev Mex Neuroci 2004;5:240. Villalobos R, Guzmán F, Torres JG, Rodriguez R. Epilepsy surgery assessment, pathology and prospective outcome variability in Mexico. Rev Mex Neuroci 2004;5:239. Uruiaga FJ. Historia de la Neurocirugía Peruana. In: Mendez J. ed. Historia de la Federación de Sociedades Latinoamericanas de Neurocirugía 286–297. Barlovento: Santiago, 2002. Rocca ED, Franco P. La electrocorticografía en Neurocirugía. Neurocirugía (Lima) 1955;4:3–5. Ortega VM, Gamero V. Anterior comissurotomy in the treatment for epilepsy. Excerpta Medica 1973;293:20. niguez R, García-Austt E. Complex Bogacz J, Vanzulli A, Arana-I~ structure of temporal epileptiform foci. Acta Neurol Latinoamer 1961;7:310–17. Martínez A, Poblete R, Galera R. Síndromes epilépticos, sus aspectos quirúrgicos. Arch. Venez Psiq Neurol 1972;39:93–112.
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Epilepsy surgery in Africa MF Moodley and EL Khamlichi
Introduction Epilepsy is the most common chronic neurological disorder estimated to affect at least 50 million people worldwide; 80% of whom reside in developing countries.1 In Africa where 50% of the population is under 16 years of age, the prevalence is even higher making epilepsy a significant health and socioeconomic burden. Africa is the second largest continent with 35 million square kilometers and more than 800 million people distributed in 52 different countries.2 Seventy-five percent of people with epilepsy in Africa receive inadequate or no treatment at all. Paralleling the enormous geographic, cultural and economic differences in this continent the neurological and neurosurgical services are equally diverse. Limited financial resources, illiteracy, social instability, war, lack of prioritization, poor health system infrastructure, and inadequate supplies of antiepileptic drugs in concert hinder the delivery of appropriate treatment. Furthermore, the vast majority of Africans still live in villages and there is a significant rural/urban divide in epilepsy services, with the vast majority of neurologists and neurosurgeons being concentrated in the major cities. Belief in supernatural causes and traditional treatment of epilepsy in Africa further contribute to the under-utilization of available medical services, to discrimination and social isolation.
Epidemiology and etiology of epilepsy In Africa preventable causes of epilepsy (central nervous system infections, head trauma, poor antenatal and perinatal care) are more frequent resulting in greater disability and mortality in Africa than elsewhere.3 The high incidence figures for epilepsy in developing countries is significantly attributable to symptomatic epilepsies caused by a host of parasitic and infectious diseases that are largely absent in industrialized countries.4–6 Neurocysticercosis, for example is frequently found in people with epilepsy in developing countries and in South Africa it is a major cause of seizures in both children and adults.4,7 Furthermore, in South Africa, 50% of children with recurrent seizures had had their first seizure before the age of 2 years, and 32% and 11% of the patients studied had a history of perinatal complications and meningitis respectively.6 Epidemiologic studies from North Africa are scarce, but in general, prevalence and incidence of epilepsy are much lower, perhaps because of a lower rate of infection than in SubSaharan Africa, better medical infrastructures, and more
trained medical personnel in the North than in Sub-Saharan Africa.8 Despite the advent of modern anti-epileptic drugs in the last three decades, 30–40% of patients with epilepsy have intractable seizures. Almost half of these patients are potential surgical candidates and of these carefully selected patients, chance of freedom from seizures after surgery is in the range of 60–75%. If we consider the high number of African patients with refractory epilepsy, the cost of the anti-epileptic drugs, hospitalization, and the economic conditions of the majority of patients, it becomes clear that surgical treatment is more cost effective than sustained pharmacotherapy. Epilepsy surgery has thus become readily adapted in many developing countries with limited resources like Brazil, China, India, and Turkey.9,10 These all argue in favor of the development of epilepsy surgery programs in Africa, and African neurologists and neurosurgeons should develop epilepsy surgery programs with the knowledge that the success of epilepsy surgery depends more on well-trained clinical teams, than on high-level technology.
Contribution of Africa to the history of epilepsy and epilepsy surgery Epilepsy is an ancient disorder, well described in many early civilizations with remarkable descriptions of epileptic attacks in early Babylonian texts of medicine (1000 BC)11 Despite this very ancient description, the concept of epilepsy etiology has remained for centuries dominated by supernatural views, considering seizure attacks as a divine visitation (religious concept), or with an invasion of the body by evil spirits (superstitious concept). Consequently the treatment was not medical but spiritual with religious and/or various social approaches. The contributions of Africa, particularly the Northern part, to the history of epilepsy had been significant in the Middle Ages, between the 9th and 13th centuries, the golden age of the Arab–Islamic civilization, which extended at the time around the Mediterranean Sea. Among some outstanding individuals with medical knowledge, two individuals stand out: Abu-Bakr Al Razi, ‘Rhazes’ (830–923) and Hussein Ibn Sina, ‘Avicenna’ (980–1037), who left us the best descriptions of epilepsy.12 In his huge monograph (‘Alkanun FiTib’, Rules of Medicine), Avicenna described different types of epilepsy syndromes: tonic-clonic seizures, absence and focal seizures including focal-motor seizures, with its typical extension from the toes to the proximal lower limbs and from the fingers to the proximal upper limbs, and known today under the name 125
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of Jackson, who described it 800 years later.13 In Avicenna’s monograph he also described many symptoms which can occur before or after a seizure which we now recognize as auras and postictal phenomena. The interesting point in this historical manuscript is that Avicenna, referring to Hippocrates, mentions the concept that epilepsy is a brain disease and that seizures result from an invasion of the frontal lobes by a noxious substance which then propagates towards the posterior part of the brain and later to the spinal cord and the peripheral nerves. This propagation engenders generalized seizures. He considered these seizures of the body as resulting from a contraction of the brain which is necessary for the expulsion of noxious substances, and comparing also these contractions of the brain to the contractions of the stomach during hiccup or vomiting in order to ‘chase noxious food’.13 This medical knowledge about epilepsy and many other brain diseases that excelled between the 9th and the 13th centuries in Fez and Marrakech (Morocco), in Kairouan (Tunisia), and in Cairo (Egypt), was later transmitted to Europe in the 14th and 15th centuries, where it would be improved to prepare the Renaissance movement of neurology in the 18th and 19th centuries and the modern era of epilepsy. As far as African neurosurgery is concerned it is well known that during the pharaonic era, neurosurgical procedures like trephinations were widely used in the whole continent, practiced and taught by healers in African tribes.14 The technical concepts of this trephination are based, to a great extent, on the descriptions of Arab physicians of the Middle Ages.14 Of the many outstanding Arab physicians it was mainly Abulkassim Al Zahraoui (Abulkassis) who was the pioneer of neurosurgery. He is credited with devoting a volume of his treatise (made up of 30 volumes) to neurosurgery, a precise description of many aspects of neurosurgical pathology, its treatment, instruments and neurosurgical techniques.14 In Kenya, the traditional art of skull trephination, passed down from generation to generation, and is still practiced by the Kisii tribesmen in the highlands of the South Nyanza District of Kenya.15 As recently as 1982 a local daily newspaper featured an article entitled ‘Skull Surgeon Who Never Went to Medical School’. This story focused on one of the well-known practitioners of trephination since 1955 having learned it from his grandfather. He claimed that he had performed hundreds of these procedures and that most of his patients had already been treated at hospitals without success.15 He added, ‘Doctors in Kenya are not able to open the skull the way I do, and when a patient goes to them full of broken bones in the head, the treatment is often incomplete.’ Neurosurgeons in Kenya encounter patients who have undergone this procedure. The openings in the skull vary from a few centimeters to removal of the entire vault. Trephinations were made for ritual or therapeutic purposes. It is speculated that they were intended to free the body from devils and spirits. It is thus easy to imagine that epileptics, in many African cultures viewed as possessed, underwent these trephinations.15 It is interesting to note that despite these significant contributions and the fact that this land was the birth place of our early human ancestors the vast majority of its population has not yet been part of the great technological/industrial revolutions that has occurred in many other parts of the world.
Thus, the challenges facing Africa in the domain of medicine remain immense.16 Neurosurgical practice developed in many African countries only during colonization, together with the development of the health system as soon as the European colonizers came to these countries. Initially, neurosurgery was practiced in the departments of general surgery either by general surgeons or rarely by neurosurgeons themselves.14 Modern neurosurgery was introduced and started to develop in most African countries in the early 1960s, and the teaching of this subspecialty in many African universities began between 1960 and 1970, soon after their independence. However, in South Africa neurosurgery as an independent discipline commenced much earlier at the Groote Schuur Hospital in Cape Town with the return of Hermann de Villiers Hammann from Munich, Germany in 1946.17 Neurosurgery for intractable epilepsy, on the other hand, was practiced even earlier as the late 1940s. Roland A. Krynauw, a neurosurgeon from the Department of Neurosurgery, Johannesburg Hospital in South Africa pioneered hemispherectomy for children, adolescents and young adults with intractable seizures accompanying infantile hemiplegia.18 Over a 5-year period he performed hemispherectomies on 12 patients with intractable seizures accompanying infantile hemiplegia with remarkable success. Epilepsy, either focal or generalized, was present in 10 of the 12 patients and in all these patients epileptic manifestations ceased in the post-operative period without any sedative medication. Furthermore, marked improvement in personality, behavior, and mental function was noted in all cases. His success with hemispherectomy soon attracted world wide attention to this neurosurgical procedure for intractable seizures.18
Management of epilepsy in Africa While remarkable progress has been made worldwide in the second half of the 20th century in the diagnostic evaluation of neurological diseases, including epilepsy, in Africa this development was mainly-in the more affluent North and South Africa and remains restrained in the rest of the continent by the poor socio-economic conditions. In many countries in Sub Saharan Africa neurological and neurosurgical services are nonexistent creating a broad divide – ‘From excellence to total absence’. Fortunately, EEG is available in the majority of countries in Africa (82.4%), however, the availability of other investigations are limited in the majority of African countries.19 Video EEG monitoring is available in 25.7% of African countries, 18 African countries have no CT scanners, 13 countries have only 1 CT scanner for each country and only 13 other countries have more than 2 CT scanners. Only North African countries and South Africa have an adequate number of CT and MRI scanners.19–21 In addition, even in those countries with neuroimaging equipment, the majority of the population who live in rural areas do not have access to this equipment, because of limited economic resources and a lack of medical insurance. In the absence of these advanced technologies, most of the common causes of symptomatic epilepsy cannot be diagnosed in many countries in Africa. The management of epilepsy in Africa is highly influenced by the socio-cultural misrepresentation of epilepsy. Consequently,
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Epilepsy surgery in Africa less than 20% of patients will seek medical attention after their first seizure, the other 20–30% will seek a healer or marabout (holy temple) for traditional treatment.22 The remaining 50–60% will not seek any treatment. This delays diagnosis and treatment, with more than 50% of patients seeking medical help one year after their first seizure, and 30% 5 years after their first seizure.23,24 The mainstay of pharmacological treatment throughout Africa is phenobarbital, which has two main advantages: reliability of supplies and affordability with 50–80% of treated patients being on phenobarbital.25 Most of the other older anticonvulsants like phenytoin, carbamazepine, valproic acid, and benzodiazepine are available in secondary and tertiary hospitals. The ‘new’ anticonvulsants discovered in the last 15 years are generally not available in the vast majority of countries in Africa. In South Africa on the other hand, it is available in most tertiary and quartenary hospitals and also in private clinics but cost is again a prohibitive factor for its widespread use.
Epilepsy surgery in Africa Epilepsy surgery is a well accepted, safe and effective alternative treatment for patients with medically intractable epilepsy in developed countries.26,27 However, in addition to appropriate technologies for pre-surgical evaluation, the success of epilepsy surgery depends on availability of well-trained clinical teams made up of neurologists, neurosurgeons, clinical neurophysiologists, neuropsychologists, and neuroradiologists, components not easily available in developing countries. In the 1990s, 10 of 142 developing countries conducted epilepsy surgery and by 2000, 26 such countries have reported results of epilepsy surgery in carefully selected patients and this number is gradually increasing.10 In Africa most of these reports emanate from the two extremes of the continent, the more affluent North and South Africa with almost the entire rest of the continent still experiencing a significant delay in the development of neurosurgery. The challenge is resource allocation in competition with other demands, in particular primary healthcare. A survey conducted in 1998 under the hospices of WHO, found only 565 neurosurgeons for a population of over 800 million (ratio of 1 neurosurgeon to 1,352,000 people).20 The world wide ratio is 1 neurosurgeon to 230,000 people with 1 neurosurgeon to 121,000 people in Europe and 1 Neurosurgeon to 81,000 people in North America.2 The distribution of neurosurgeons in the African continent shows that the majority are located in North Africa (Egypt 165, Algeria 130, Morocco 80, Tunisia 25) and South Africa (86). Consequently the total number of neurosurgeons in these countries is 486 for a total population of 174 million, with a ratio of 1 neurosurgeon to 358,000 people. Between North and South there are three countries that have between 8 and 15 neurosurgeons (Nigeria, Senegal, and Kenya), and the majority of other countries have between 1 and 5 neurosurgeons, with no neurosurgeons at all in 11 countries. Therefore, the ratio in Sub-Saharan Africa is 1 neurosurgeon to 7 million people. The biomedical equipment available has almost the same distribution.2 A local training program in neurosurgery is currently available only in North African countries and in South Africa.
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Most young neurosurgeons in the rest of Africa are trained outside the continent, mainly in Europe. Currently in South Africa there are a few centers in Cape Town, Johannesburg and Durban that have impressive pre-surgical technology and clinical teams who perform epilepsy surgery in carefully selected patients. (personal communication Roger Melville and James Butler). Subdural electrode placements, temporal lobectomies, and cortical resections account for the bulk of the surgery performed. Multiple subpial resections and functional hemisperectomies are also performed occasionally (personal communication Roger Melville). In Morocco it took many years to find motivated people to create a multidisciplinary team and to commence epilepsy surgery which only began in February 2005. Surgical procedures so far have included temporal lobectomies and simple structural lesion surgery. Faced with the reality of a scarcity of human and technological resources, is there room for epilepsy surgery in developing countries like those in Africa? Because of the high prevalence of epilepsy in Africa, the high cost of sustained pharmacotherapy, its medical intractability, and the high frequency of symptomatic epilepsy, epilepsy surgery offers a potential treatment to rescue a large number of patients with epilepsy in Africa. Moreover, these are the reasons behind the development of many epilepsy surgery programs in countries with limited resources, like Brazil, China, and Turkey and these programs have demonstrated that surgery is more cost effective than sustained pharmacotherapy.9 In addition, surgery will have a positive impact on the mental capacity of epileptic patients and of society in Africa, allowing patients to conceive of epilepsy as an organic disease originating from the brain, which can be cured with surgery. Even with limited technological and human resources carefully selected patients from an abundance of surgical candidates, the teams achieve outcomes comparable to those in the developed world with direct epilepsy surgery costs at a fraction of those in the developed world.
Future of neurosurgery and epilepsy in Africa More than 80% of the 50 million people suffering from epilepsy around the world live in developing countries like those of Sub-Saharan Africa where the vast majority do not receive any modern treatment or are not even identified.28 The main reasons behind this treatment gap are poor health care systems, illiteracy and cultural beliefs especially in SubSaharan Africa. Some other potential causes of this treatment gap are a lack of prioritization of epilepsy as a public health issue, inadequate preventative programs and a high prevalence of epilepsy in Africa. Regarding the ‘surgical treatment gap’ in epilepsy there is a great divide – well catered for in North African countries (Egypt and Morocco) and South Africa and almost non-existent in the rest of the continent.10,29 If we consider the proposed ratio by H. G. Wieser of 1 epilepsy center for 7 million people as estimated in developed countries, Africa with more than 800 million people, needs more than 100 epilepsy surgery centers making the bridging of the surgical treatment gap in
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epilepsy in Africa an impossible dream.10 The main problem to overcome is the scarcity of neurosurgeons and neurologists in the majority of African countries. Without their expertise it becomes difficult to organize any multidisciplinary team to solve the huge challenge of reducing the treatment gap in epilepsy between Africa and the developed world. Pioneering African neurosurgeons should develop neurosurgery in their countries by encouraging local training programs which remain the major pillar in the development and quicker promotion of neurosurgery in their countries as exemplified by North African countries and South Africa. African trainees in developed countries generally are not keen to return, and when they return do not have the resources which they have trained with rendering them ineffective or demoralized and thus paving the way for the growing ‘brain drain’ from Africa to Europe and North America. The second main problem is to convince the political authorities and health planners that epilepsy is a public health issue, despite other high priority health demands, as in most African countries epilepsy and neurosurgery in general seem to have a very small place on public health priority programs. Neurologists and neurosurgeons as advocates for patients with epilepsy should sensitize other individuals including non-medical professionals, patients and community NonGovernmental Organization (NGOs) to apply pressure on governments, health planners, and decision makers so that proposals for building sustainable training programs are put in place. Epilepsy care development in Africa can also benefit from international cooperation and the help of international institutions like the WHO, the ILAE, and the International Bureau for Epilepsy (IBE). These three institutions make a major collaborative effort through the global campaign against epilepsy ‘Out of the Shadows’, which was launched in 1997 ‘to improve acceptability, treatment, services and prevention of epilepsy worldwide in order to address discrimination against people with epilepsy and to diminish the treatment gap in the developing regions of the world.’1 Three other institutions can efficiently help epilepsy programs in Africa: The World Federation of Neurosurgical Societies (WFNS), the World Federation of Neurology (WFN),
and the Pan-African Association of Neurological Sciences (PAANS).30 These institutions can help at different levels: at the information level by sending reports on the epilepsy care situation in Africa to governments and universities in African countries; at the training and research levels by organizing courses, seminars, and granting fellowships to young African doctors to be trained in neurology and neurosurgery. In 1998 the WFNS initiated the creation of the ‘WHO Africa Sub-Committee in Neurosurgery,’ which prepared a report on the state of neurosurgery in Africa, which was presented to the WFNS and the WHO working group in Neurosurgery in 1999,20 resulting in the creation of the ‘WFNS Foundation For Training Young Neurosurgeons from developing countries’ in 2002. It also created the first reference center in the Department of Neurosurgery at the University Hospital in Rabat to train young African doctors, and the Mohamed V University of Rabat arranges and insures their training.
Conclusion Epilepsy remains an important public health problem in Africa. With its high prevalence and the lack of appropriate diagnostic and therapeutic facilities it represents an important economic and social burden in the majority of African countries. The main constraints widening the treatment gap in epilepsy include lack of knowledge about epilepsy, cultural attitudes especially in rural people, poor advocacy for neurosurgery at governmental level, and the limited human and material resources in the majority of African countries. The optimistic element, however, is the existence of neurosurgical centers of excellence at the two extreme parts of the continent, namely North and South Africa. Neurosurgeons in these areas can integrate epilepsy surgery in a fairly rapid way in their centers, using non-invasive pre-surgical investigations to successfully select the patients with intractable epilepsy. With the combined effort of North Africa and South Africa and substantial support for African neurosurgery from the international community, the development of neurology and neurosurgery in Sub-Saharan Africa can be improved and the treatment gap in epilepsy can be filled.
REFERENCES 1. 2. 3. 4. 5. 6. 7. 8.
Scott RA, Lhatoo SD, Sander JWAS. The treatment of epilepsy in developing countries: where do we go from here? Bulletin of the World Health Organization 2001;79:344–51. Kalangu KKN. Pediatric neurosurgery in Africa–present and future. Child’s Nervous System 2000;16:770–5. Commission on Tropical Diseases of the International League Against Epilepsy. relationship between epilepsy and tropical diseases. Epilepsia 1994;35:344–51. Moodley M, Moosa A. Treatment of neurocysticercosis. “Is Praziquantel the New Hope.” Lancet 1989;(8632):262–3. Moodley M, Bullock MRR. Severe neurological sequelae of childhood bacterial meningitis: S Afr. Med. J 1985;68(8):566–70. Leary PM, Morris S. Recurrent seizures in childhood: western cape profile. South Afr. Med J 1998;74:579–81. Dawood AA, Moosa A. Cerebral cysticercosis in children. J Trop Pediatr 1984; June 30(3):136–9. Marie-Preux P, Druet-Cabanac M. Epidemiology and etiology of epilepsy in Sub-Saharan Africa. Lancet – Neurology 2005;4:21–31.
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Engel J Jr. et al. Alternative treatments in epilepsy: global issues for the practicing neurologist. World Federation of Neurology Seminars in Clinical Neurology. New York, NY. Demos 2005:95–105. Wieser HG, Silfvenius H. Overview: epilepsy surgery in developing countries. Epilepsia 2000;41(Suppl 4):S3–S9. Kinnier Wilson JV, Reynolds EH. Translation and analysis of a cuneiform text forming part of a Babylonian treatise on epilepsy. Medical History 1990;34:185–98. Ammar S. En souvinir de la medecine arabe. Quelques-uns de ses grand noms. Ed Soc. Tunisienne de diffusion. Tunis 1965. Ibn Sina AH. Al Kunun FiTib, Tome 2, 76–89 (in Arabic). El Khamlichi A. African neurosurgery. Part 1: Historical outline. Surgical Neurology 1998;49:222–7. Dar J. Perspectives of international neurosurgery: neurosurgery in Kenya: Neurosurgery 1985;16:267–9. Peter JC. Pediatric neurosurgery–a South African perspective. Child’s Nervous System 2003;19:133–6.
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Peter JC. The Department of Neurosurgery of the University of Cape Town: a brief historical overview. Neurosurgery 1999; 45(S):1228–36. Krynauw RA. Infantile hemiplegia treated by removing one cerebral hemisphere. J Neurol Neurosurg Psychiat 1950;13:243–67. WHO: Atlas Epilepsy Care in the World 2005. El Khamlichi A. African neurosurgery: current situation, priorities and needs. Report presented to the WHO Working Group on Neurosurgery, Geneva, February 20, 1999. El Khamlichi A. African neurosurgery: current situation, priorities, and needs [Special Reports]. Neurosurgery 2001;48(6);1344–7. El Khamlichi A. Contribution à l’étude de l’épilepsie en milieu marocan. 1974; Thése de doctorat, Université Mohamed V, Rabat. Danesi MA, Adetunji JB. Use of alternative medicine by patients with epilepsy: a survey of 265 epilepsy patients in a developing country. Epilepsia 1994;35:344–51.
24. 25. 26. 27. 28. 29. 30.
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Reis R. Evil in the body, disorder of the brain; interpretations of epilepsy and the treatment gap in swaziland. Trop Geogr Med 1994;46:S40–3. Kissani N, Belaidi H, Bennani Othmani M. et al. Comparison du profil des patients épileptiques au Maroc à plusieurs années d’intervalle. Epilepsies 2001;13:251–7. Engle J Jr. Surgery for seizures. N Engl J Med 1996;334:647–52. Williamson PD, Jobst BC. Epilepsy surgery in developing countries. Epilepsia 2000;41 (Suppl 4):S45–50. Jallon P. Epilepsy in developing countries. Epilepsia 1997;38: 1143–51. Meinardi H. et al. on Behalf of the ILAE Commission on the Developing World. The treatment gap in epilepsy: the current situation and ways forward. Epilepsia 2001;42:136–49. Bower JH, Zenebe G. Neurologic services in the nations of Africa. Neurology 2005;64:412–15.
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History of epilepsy surgery in Southeast Asia S-H Lim
Overview of epilepsy surgery in Southeast Asia Southeast Asia (SEA) covers an area of about 4 100 000 square kilometers containing the following countries: Brunei, Cambodia, Indonesia, Laos, Malaysia, Myanmar, Philippines, Singapore, Thailand, and Vietnam. As of 2007, there are more than 580 million people living in this region. If the epilepsy prevalence rate is 5 per 1000 population, SEA would have around 2.9 million people with epilepsy (PWE). If a quarter of these PWE are medically refractory, more than 700 000 of them could be evaluated for epilepsy surgery. However the epilepsy surgery treatment gap is huge in SEA. An informal survey conducted by the author in 2003 (unpublished data) showed that selective amygdalo-hippocampectomy) while the rest were lesionectomy, neocortical resection, corpus callosotomy, hemispherectomy, and implantation of vagus nerve stimulator (VNS). Similar to the results in countries belonging with developing economies, 60–70% of temporal lobectomy patients achieved Engel Class I seizure outcome, while another 10–15% had rare seizures or worthwhile improvement. These surgeries were performed at tertiary referral centers, established in the late 1980s in Thailand, early 1990s in Singapore, and in the second half of the 1990s in Malaysia, Philippines, and Indonesia. There are currently 1–4 centers per country, located in capital cities. Each centre has 1–5 epileptologists and 1–2 neurosurgeons with special interest and/or trained in epilepsy surgery. Many centers perform long-term video-EEG monitoring and structural MRI routinely. The usage of SPECT, Wada Test, MRS, neuropsychological testing, and psychiatric assessment is variable. Intracranial EEG recordings are rarely performed and PET study is only available in two countries. To date, there is no epilepsy surgery program in Brunei, Cambodia, Laos, Myanmar, or Vietnam. There are common issues in SEA that continue to retard the development of epilepsy surgery in this region. Costs of evaluations and surgery are relatively high in most countries. Socially and culturally, many patients were reluctant to undergo cranial surgery for a condition not considered immediately life-threatening by these patients and their 130
family. This tied in with the perception by the lay that cranial surgery is oftentimes morbid and considered an extreme intervention. Family support in SEA was relatively strong, thereby obviating the need for independence and selfsupport. Many patients in the rural areas are still probably undiagnosed and not informed of the epilepsy services available in the country. Public transport services in big cities are fairly prevalent and convenient. The need to be seizure free to drive was not as pressing as in other countries like the United States. The following sections describe the development of epilepsy surgery in Indonesia, Malaysia, Philippines, and Singapore. The epilepsy surgery programe in Thailand is briefly mentioned here as the details are described in Chapter 19.
History of epilepsy surgery in Indonesia Indonesia is the largest country in Southeast Asia with a population of 224 millions and has the largest pool of epilepsy patients who require epilepsy surgery. However, there was no epilepsy surgery program till the end of the 1990s. Unlike other SEA countries where epilepsy surgeries are driven by trained epileptologists, surgery for epilepsy in Indonesia was initiated by a neurosurgeon, Dr Zainal Muttaqin from Semarang, Indonesia. Dr Muttaqin, influenced by the blooming of epilepsy surgeries in other parts of the world, developed an increasing interest in epilepsy surgery in the middle of the 1990s. To increase the awareness of clinicians and lay-public in epilepsy surgeries, he organized an epilepsy surgery symposia at national and regional neurology scientific meetings, at which Prof T Hori from Japan was a keynote speaker. He also started writing review articles on surgery for epilepsy in Indonesian language medical journals. He then decided to acquire the skills of epilepsy surgery and traveled to Hiroshima, Japan many times between 1996 and 2001 to learn epilepsy surgery from Dr Kazunori Arita and Prof Kaoru Kurisu, at the Hiroshima University. With their help, the first case of left temporal lobectomy was performed in 1999. Surgery was performed based on clinical information suggestive of temporal lobe seizures and MRI evidence of left temporal sclerosis. Another 10 cases were operated in 2000–2001, all based on clinical history suggestive of TLE semiology and unilateral hippocampal structural abnormality on MRI.
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History of epilepsy surgery in Southeast Asia Due to the limitation of financial resourses, most of the MRI machines were of 0.5 Tesla in strength, including the only centre (Diponegoro University Hospital) that performed epilepsy surgery. Only a few hospitals affiliated to universities had acquired 1.5 Tesla machines which are not used for presurgical evaluation. Prolonged EEG recording with video monitoring facility is still lacking, thus it is not part of presurgical evaluation protocol. Even for routine EEG recording, most of the machines were 10 channels, though a few of the nonepilepsy surgery centers have acquired 20–32-channel EEG machines with video recording capability. There is also a lack of trained electroencephalographers (EEGers) in Indonesia. Between 2000 and 2006, there were three adult neurologists who received 6–12 months of training, mainly in routine and noninvasive long-term EEG monitoring and clinical epileptology. Other issues included inconsistent presurgical evaluation protocols, postoperative follow-up mainly by neurosurgeon, no other trained neurosurgeon, as well as late identification and referral of intractable cases. As such, decision for surgery was made mainly by Dr Muttaqin, very often based mainly on the findings obtained from low-resolution MRI imaging. Despite the above-mentioned limitations, more than 100 patients had epilepsy surgery between 1999 and 2006. Over 90% had temporal lobectomy with removal of mesial structures, mainly for patients with mesial temporal sclerosis. A few patients had a Wada test and subdural grid recording (in those with normal MRI). One patient had intraoperative ECoG. For those with temporal lobectomy that had 12–82 months of follow-up, about 75% had Engel’s class I seizure outcome and two-thirds of these patients could have their AEDs withdrawn. A few patients had lesionectomy, multiple subpial transaction, functional hemispherectomy and corpus callosotomy.
History of epilepsy surgery in Malaysia Malaysia has a population of 28 million people but only had one ‘one-stop’ epilepsy surgery center in the 1990s and early 2000s. The adult epileptologist who pioneered the epilepsy surgery programme in Malaysia was Professor Raymond Azman Ali. He was trained by Prof David Fish in video-EEG monitoring, presurgical evaluation, and neuroimaging at the Institute of Neurology, Queen Square, London, from 1992 to 1994. At the same time, a neurosurgeon, Prof Benedict Selladurai, was also trained at the institute by Prof David Thomas and Mr. William Harkness in epilepsy surgery. Upon returning to Malaysia in 1994, they together started the epilepsy surgery programme in 1995 at the Universiti Kebangsann Malaysia Hospital. The first operation was performed on an 11-year-old boy with a dysembryoplastic neuroepithelial tumor in the mesial temporal region, who became seizure free. When they announced the successful operation in one of the national newspapers, interest in epilepsy surgery amongst PWE increased tremendously. Not all surgical patients were from the same hospital, as many were referred from other major hospitals, including Kuala Lumpur Hospital and University Malaya Medical Centre. The hospital was supportive in upgrading the neurophysiology laboratory and neuroimaging service. However, they did not have a stand-alone
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epilepsy surgery centre, in-patient ward or epilepsy nursing staff. They also employed neuropsychologists interested in epilepsy. One of the psychiatrists went on to subspecialize in neuropsychiatry. In 2000, Prof Lai-Choo Ong, a pediatric neurologist, received training in Royal Melbourne Children’s Hospital under the supervision of Dr Simon Harvey. Another adult neurologist, Dr Hui-Jin Tan, is currently being trained in clinical epilepsy. EEG facilities included a video-EEG monitoring unit using scalp and sphenoidal electrodes. A few patients had intraoperative ECoG. They have not developed intracranial EEG capability. As for neuro-imaging capability, they have 1.5 T MRI machine and are able to add MRS to their evaluation protocol. Ictal SPECT was rarely performed. Neuropsychological evaluation was routine, but there was no expertise in performing WADA tests. Standard anterior temporal lobectomy was started in 1996, followed by selective amygdalohippocampectomy and lesionectomy in 1999. Hemispherectomy, corpus callosotomy, and implantation of vagus nerve stimulator were started in 2001. Between 1996 and 2006 around 75 cases of anterior temporal lobectomy and 15 cases of selective amygdalohippocampectomy were performed with 70% of these patients achieving Engel’s Class I seizure outcome. Two patients had hemispherectomy and both became seizure free. Twelve patients had lesionectomy and 55% achieved Class I seizure outcome. There were three cases of corpus callosotomy and one VNS and all had Class IV seizure outcome. The main challenges encountered in developing the epilepsy surgery programme were lack of full-time staff (epileptologists, epilepsy neurosurgeons, neuroradiologists, neuropsychologists, nurses, and neuroanaesthesiologists). Currently only one centre performs a consistent number of epilepsy surgeries. Even then, the infrastructure for this ‘one-stop’ centre is underdeveloped.
History of epilepsy surgery in the Philippines The Philippines have a population of 87 millions. There are 3–4 hospitals offering epilepsy surgery since the late 1990s. With the continued return of clinicians trained in epileptology and subsequently in epilepsy surgery, the comprehensive epilepsy program was established in 1997 at the St. Luke’s Medical center. This center is one of the premier private hospitals in the country with the necessary resources to support the epilepsy surgery program. The center had a ‘multidisciplinary team’ composed of the following members: epileptologists, an epilepsy surgeon (Dr Annabelle Chua), neurophysiologists, psychiatrist, nurses, EEG technicians, and dieticians. The objective of the program was not only to evaluate patients and their suitability for epilepsy surgery, but also to offer overall better management and control of patients with difficult to control seizures. The Epilepsy Monitoring Unit at the St. Luke’s Medical Center is a three-bed unit capable of offering 2-hour and prolonged video-EEG monitoring. In addition, there are three other one-bed units in other hospitals with in-house epileptologists trained in video-EEG monitoring, namely the University of the Philippines-Philippine General Hospital, the Philippine Children’s Medical Center, and the Makati Medical
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Center. Epilepsy clinics were established in two training hospitals: the University of the Philippines-Philippine General Hospital and the University of the East-Ramon Magsaysay Medical Center. Presurgical evaluation included CT scan, MRI, PET scan, video-EEG, neuropsychological evaluation and WADA test. For the latter, this is being done only at St. Luke’s Medical Center, with its performance being limited by the difficulty in procuring amobarbital from the United States. There was also intracranial electrode placement, extraoperative monitoring, intraoperative ECoG, and mapping of eloquent cortex. Most patients who had resective surgery had either hippocampal sclerosis or lesion such as tumors and vascular malformations. Detailed information on the number and types of surgery, as well as seizure outcome were not available.
History of epilepsy surgery in Singapore Singapore is the smallest country that provides epilepsy surgery in SEA. It has a population of 3.6 million, and thus the number of potential surgical candidates is considered relatively low. An epilepsy surgery programme was established in Singapore in 1992 after the return of an adult neurologist, Dr Shih-Hui Lim, from the Cleveland Clinic Foundation (CCF). With the sponsorship of the Ministry of Health, Singapore, Dr Lim completed a formal clinical fellowship in epilepsy and clinical neurophysiology under the supervision of Prof Hans O Lüders from 1989 to 1991. He also obtained board certification by the American Board of Clinical Neurophysiology. A year later, another adult neurologist, Dr Michael WL Chee, also sponsored by the Ministry, completed similar training at CCF from 1990 to 1992. In addition, Dr Prem Kumar Pillay, a Singaporean doctor receiving his neurosurgery residency training at CCF in the late 1980s and early 1990s, was trained in epilepsy surgery by Dr Isam Awad. In the early 1990s, a pediatric neurologist, Dr Wei-Ling Lee received pediatric epilepsy training at Toronto Children’s Hospital in Canada as well as at the CCF. In the mid-1990s, Dr Ngai-Kun Loh, an adult neurologist spent a year and Dr Kheng-Kooi Tan, a neurosurgeon, spent a few months at CCF. Dr Andrew Pan, an adult neurologist, was sent by Ministry of Health to CCF from 1999 to 2001 to be trained in Epileptology and Sleep Disorders. Thus the epilepsy surgery programe in Singapore in the first 10 years was considerably influenced by the philosophy of Dr Lüders. In 2003, Dr Nigel Tan received his epilepsy training with Prof Sam Berkovic at the Comprehensive Epilepsy Program at Austin Health. His return added value to the existing epilepsy surgery programme. One-Bed video-EEG monitoring unit was first set up at Tan Tock Seng Hospital in 1992 and at Singapore General Hospital in 1993. Scalp and sphenoidal electrodes were used routinely. Most patients were monitored for 4–5 days after stopping medication, with an aim of recording at least three seizures. Due to administrative and logistic reasons, early postictal SPECT was carried out during office hours at the Singapore General Hospital. For those who had postictal SPECT had interictal SPECT during the monitoring period. All patients had structural MRI (1.5 T) which included oblique coronal
images with flash/gradient echo, T2-weighted, and FLAIR sequences. Volumetric study was performed as part of the research. MRS was introduced towards the end of the 1990s. FMRI for language lateralization was started in the early 2000s, mainly for research purposes. From 2005, structural MRI using a 3.0 T MRI machine became more common. WADA tests were performed routinely in the 1990s and infrequently in the 2000s. Neuropsychological and psychiatric assessments were routine. Decision for surgery was made mainly based on structural MRI findings, scalp EEG data, and analysis of semiology of recorded seizures. As long as there was no discordant information, good candidates would proceed with resective surgery. Depth electrodes implantation was performed only once in 1994 to lateralize seizure onset. Chronically implanted subdural grid electrodes and extraoperative cortical mapping were carried out in four patients with nonlesional extratemporal lobe epilepsy in 1994 and 1995. Due to the poor seizure outcome from these cases, better MRI imaging facilities, avoidance of performing resective surgery in patients with no lesion on MRI, as well as constraint of doctors’ time, invasive intracranial EEG recordings were rarely performed in the 2000s. As expected from a center conducting mainly noninvasive presurgical evaluation, temporal lobe surgeries (standard anterior temporal lobectomy cases were more than selective amygdalohippocampectomy) and to a lesser extent, lesionectomy, were the most commonly performed surgeries. Corpus callosotomy, extratemporal resective surgery, hemispherectomy and implantation of vagus nerve stimulator were much less frequently performed. Between 1992 and 2002, more than 110 patients had temporal lobectomy, 12 had lesionectomy, four had corpus callosotomy, three had extratemporal resection, two had hemispherectomy and seven had VNS implanted. They have been followed-up for an average of 8.5 years (range 5–15 years). There was no death or irreversible complications from surgery or intracranial EEG recording. Of those who had temporal lobe surgeries, about 66% had Class I seizure outcome (including 2 patients who had re-operation), 20% had worthwhile improvement (>90% seizure reduction) and the rest had no significant change (300) in the last 10 years. As described in Chapter __, the were two eras of epilepsy surgery in Thailand: the era of general neurosurgery before the 1990s and the era of epilepsy surgery as a specialty after the 1990s. For the latter, detailed neuroimaging and clinical neurophysiology information became an integral part of the presurgical evaluation process. Professor Sira Bunyaratavej and Professor Pongsakdi Visudhipan from Ramathibodi Hospital played an important role in the development of the new epilepsy surgery era in the 1990s.
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History of epilepsy surgery in Southeast Asia The major epilepsy surgery center in Thailand is the Chulalongkorn Comprehensive Epilepsy Program (CCEP) at Chulalongkorn University Hospital, Bangkok, Thailand, led by Dr Chaichon Locharernkul, an adult epileptologist and Dr Teeradej Srikijvilaikul, an adult and pediatric neurosurgeon. Dr Chaichon was trained in presurgical evaluation by Prof GA Ojemann and Prof GE Chatrain at University of Washington at Seattle, USA and by Dr A Ebner at the Bethel Epilepsy Center in Germany. Dr Srikijvilaikul was trained by Dr WE Bingaman at CCF. Other team members included Drs Tayard Desudchit, Krishnapundha Bunyaratavej, Chusak Limotai, and Jakrin Loplumlert, all had formal training in USA (three at CCF). Together, they offered the most comprehensive presurgical evaluation, including the routine use of SISCOM and 3.0 T MRI. Other centers providing epilepsy surgery programme were located at Pramongkutklao Hospital and Bangkok General
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Hospital. Both centers were established by Dr Yotin Chinvarun in 2001 and 2002, respectively. Dr Chinvarun was an adult epileptologist trained by Prof Sam Berkovic in Australia. Members in his team included Dr Siraruj Sakoolnamarka and Dr Dittapong Boonnampol (both were adult and pediatric neurosurgeons), as well as Dr Chachrine Nabangchang (a pediatric epileptologist). This is the only center in SEA that provided gamma knife surgery for epilepsy. Acknowledgments The author greatly appreciates the following persons who have given the above information: Dr Zainal Muttaqin from Indonesia, Dr Raymond Azman Ali from Malaysia, Dr Annabelle Chua from the Philippines, Drs Pongsakdi Visudhipan, Chaichon Locharernkul, and Yotin Chinvarun from Thailand.
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Epilepsy surgery in India DK Lachhwani and K Radhakrishnan
Although trephination as a treatment for epilepsy might have been practiced in ancient India more than 4000 years ago,1 the first modern epilepsy surgery in India was undertaken in the year 1952.2 As has happened elsewhere in the world,3 surgical treatment of epilepsy in India went through three phases: an initial enthusiasm (1951–1970), followed by a period of decline and a recent resurgence (from 1995). In this chapter, we intend to trace the evolution of epilepsy surgery in India along with a brief biographical sketch of the pioneers who contributed to its early development, and discuss in detail its present state and future perspectives.
The beginning The modern era of neurosurgery in India commenced with the establishment of the first department of neurosurgery by Dr. Jacob Chandy (Figure 16b.1a) in 1949 at the Christian Medical College, Vellore, in the erstwhile state of Madras (present Tamil Nadu) in southern India.4 After completing his medical education at Madras Medical College, Madras and Masters in Surgery at the University of Pennsylvania, Philadelphia, Chandy underwent neurosurgical training at the Montreal Neurological Institute during 1945–1948 under Dr. Wilder Penfield. After a brief assignment with Dr. Theodore Rasmussen, who was then setting up a neurosurgery department at Chicago, Chandy returned to India and joined the Christian Medical College, Vellore in 1949. One year later, Dr. Baldev Singh (Figure 16b.1b) joined Chandy as a neurologist. After completing his medical graduation, Singh joined King Edward Medical College, Lahore in 1922, where his initial interest in neuroanatomy developed. During his training in neurology at the National Hospital, Queen Square, London, Singh was fortunate to work with Kinnear Wilson, Lord Brain and McDonald Critchley. Reading about Berger’s rhythm, stimulated Singh to undergo a training course in electronics and construct an indigenous apparatus in the 1940s to record the electrical activity of the brain of experimental animals. Singh went over to Gibbs’s laboratory at Chicago in 1950 and spent the year, where he met Dr. Percival Bailey and participated in EEG recording on epilepsy patients on whom Bailey operated. This training proved useful to Singh to develop an epilepsy surgery program at Christian Medical College, Vellore. Coinciding with Penfield’s visit to Christian Medical College, Vellore, the first epilepsy surgery in India was performed on Aug 25, 1952 by Chandy on a 19-year old male patient with infantile right hemiplegia. Singh was in the operation theater supervising the EEG recording. 134
At that time, 150 km north of Vellore, in the city of Madras, the second department of neurosurgery in India was being developed by Dr. B. Ramamurthi (Figure. 16b.1c). After a brilliant undergraduate education, he secured Master of Surgery and Fellowship of the Royal College of Surgeons of Edinburgh in 1947. Ramamurthi received his initial training in neurosurgery at Newcastle, UK. He subsequently visited various neurosurgical centers in Europe and spent four months with Penfield at the Montreal Neurological Institute. In October 1950, Ramamurthi joined the Madras General Hospital and Madras Medical College and started the department of neurosurgery, which he later developed into the Institute of Neurology, Madras.5 Ramamurthi was helped with the EEG recording by Dr. T. S. Narasimhan (Figure 16b.1d), a neurosurgeon and electroencephalographer practicing in the city of Madras, who also held an honorary attachment in the Madras General Hospital. The first epilepsy surgery at the Madras General Hospital was done by Ramamurthi in 1954. Incidentally, the four pioneers who were involved with the early development of epilepsy surgery in India – Chandy, Singh, Ramamurthi, and Narasimhan – started the Neurological Society of India in 1951 at Madras.5 While three of them passed away, (Narasimhan in 1959, Singh in 1998, and Ramamurthi in 2003), Chandy expired on June 23, 2007.
Initial enthusiasm During the 1950s, 1960s, and the first half of the 1970s, several patients with uncontrolled epilepsies were operated at Christian Medical College, Vellore,2,6,7 and Institute of Neurology, Madras.8–10 The localization of the epileptogenic focus was based on seizure semiology as obtained by history, and data from scalp interictal EEG and radiological investigations available then such as skull radiograph, pneumoencehalogram, and carotid angiogram. At the Christian Medical College, Vellore, while local anesthesia was favored during the first decade and half, most of the subsequent surgeries were performed under general anesthesia.6,7 Pre- and post-resection electrocorticogram (ECoG) was routinely done using surface and depth electrodes. Cortical stimulation to map motor and language areas and induction of seizures intraoperatively were practiced when indicated. In a recent retrospective analysis of the clinical profile and outcome of 141 patients operated for intractable epilepsy at Christian Medical College, Vellore (a majority of them during 1950s, 1960s, and first half of the 1970s), 102 (73%) had temporal
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Figure 16b.1 The pioneers who contributed to early development of epilepsy surgery in India. (a) Professor Jacob Chandy (1910–2007). (b) Professor Baldev Singh (1904–1998). (c) Professor B. Ramamurthi (1922–2003). (d) Dr. T. S. Narasimhan (1913–1959).
lobe, 23 (16%) had extratemporal, and 16 (11%) had multifocal seizures.11 The surgical procedures undertaken for TLE were lesionectomy (28 patients), temporal lobectomy with amygdalotomy (25 patients), temporal lobectomy with amygdalotomy and hippocampectomy (10 patients), amygdalotomy alone (15 patients), and lesionectomy with amygdalotomy in one case. For extratemporal epilepsies, lesionectomy was done in 24 patients and lobectomy for 2 patients. For multififocal epilepsy, 12 hemispherectomies and 4 stereotactic anosotomies were performed. The overall outcome was assessed as total or near total seizure control in 53% of patients and a worthwhile improvement in 20% of patients.11 In the mid-sixties, functional neurosurgery was established in the Institute of Neurology, Madras and stereotactic procedures for focal and generalized seizures were practiced.5 Stereotactic lesions were made in the amygdalohippocampal region for TLE and in the central medial nucleus of the thalamus, the field of Forel, and in the internal capsule for generalized seizures and infantile spasms.8–10
The decline In the mid-seventies, epilepsy surgery took a dramatic downward trend in the country. Thus, 100 out of the 102 patients with intractable TLE operated on at Christian Medical College, Vellore, until 1990,11 were performed before 1980.7 The retirement from active service of Chandy and Ramamurthi from the centers they almost single-handedly developed, less than expected post-operative seizure outcome, availability of more effective antiepileptic drugs, and stigma associated with epilepsy surgery due to its mistaken identity with psychosurgery collectively contributed to this decline.
The resurgence The recognition in the 1990s that a majority of patients with medically refractory partial seizures have surgically remediable lesions that can be identified by relatively simple non-invasive studies such as magnetic resonance imaging (MRI) and scalp recorded interictal and ictal EEG has resulted in the evolution
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of epilepsy surgery programs in developing countries with results comparable to that of developed countries.12,13 A recent survey revealed that, in 26 of 142 (18.3%) developing nations, at least one center regularly conducted epilepsy surgery.14 One of the authors (KR) returned to India in 1994 after having had training at the Epilepsy Program, Mayo Clinic, Rochester, MN and developed the R. Madhavan Nayar Center for Comprehensive Epilepsy Care at the Sree Chitra Tirunal Institute for Medical Sciences and Technology, a tertiary referral center, situated at Trivandrum, the capital city of the South Indian state of Kerala.15 Since mid-1995, this center has undertaken, on average, 66 epilepsy surgeries per year. Almost simultaneously, epilepsy surgery programs were started at the All India Institute of Medical Sciences, New Delhi, and National Institute of Mental Health and Neurosciences, Bangalore. During the last decade, these three centers together have undertaken nearly 1000 epilepsy surgeries, which is five times more than the epilepsy surgeries performed in India during the previous four and half decades.
Present state The success of epilepsy surgery is dependent upon the early identification of potential surgical candidates, and selecting from them, ideal candidates destined to have a postoperative seizure-free outcome.16 Two basic requirements must be fulfilled before an epilepsy surgery program can be introduced in any geographical region: existence of a level of medical infrastructure to identify epilepsy patients with medical refractoriness, and a comprehensive epilepsy care organization where such patients can be subjected to a multidisciplinary evaluation to decide about surgical candidacy. There are only about 800 neurologists for the 5–10 million persons with epilepsy in India. While 70% of the people with epilepsy in India reside in rural areas, almost all the neurologists practice in urban areas.17 A majority of patients with epilepsy in India and other developing countries are therefore treated and followed-up by primary- and secondary-care physicians, who have little knowledge about the recent trends in the management of epilepsies. To many of them, epilepsy is still an incurable chronic disorder. Epilepsy clinics in a developing country set-up have to cater to a large number of patients with very limited skilled personnel. Overcrowding with patients and the consequent overburdening of the service providers, make time available for clinical assessment of individual patients very limited.18 A frequent difficulty encountered in identifying medical refractoriness among patients with chronic epilepsy in developing countries is that, although many drugs have been used, none were given for sufficiently long periods and in adequate dosages, either alone or in proper combinations.19 These factors contribute to considerable delay in the identification of prospective surgical candidates. Epilepsy surgery centers in developing countries will lack the full range of state-of-the-art technologies such as single photon emission tomography (SPECT), positron emission tomography (PET), and magnetoencephalography usually available in centers in the developed world to perform noninvasive presurgical evaluation.20 In India, patients or their families will have to bear the cost of epilepsy care. Although the
total direct cost of presurgical evaluation and surgery in developing countries amounts to a small fraction of the cost incurred in the Industrialized World, this expenditure is beyond the reach of the majority.21 Very few patients in India can afford the cost of intracranial electrodes used for invasive evaluation. In order to become cost-effective, epilepsy surgery centers in developing countries will have to achieve excellent results by selecting candidates destined to have a seizure-free outcome using locally available limited technology and expertise, without compromising on patient safety.21 Because of these reasons, the process of selection of patients for epilepsy surgery in India to some extent differs from that of developed countries. Patients with medical refractory epilepsy belong to different categories depending upon the degree of complexity involved in presurgical evaluation and the post-operative seizure outcome.22 The prototype of a surgically remediable syndrome is mesial TLE with hippocampal sclerosis (MTLEHS), which constitutes more than half of those patients with medically refractory epilepsy worldwide.23 Non-invasive evaluation utilizing history, high resolution MRI, scalp videoEEG, and neuropsychological findings can identify patients with mesial temporal lobe epilepsy and those with other circumscribed, potentially epileptogenic lesions, 70–90% of whom become seizure-free following resective surgery.16,24 Selected mesial temporal lobe epilepsy patients with consistent unilateral temporal interictal epileptiform abnormalities may not even require ictal video-EEG recordings.25 Patients with large epileptogenic lesions involving primarily one hemisphere, and those with diffuse epileptic encephalopathies and multifocal disease can be selected for functional hemispherectomy or hemispherotomy and corpus callosotomy, respectively, based on non-invasive data.22 Patients with extratemporal partial seizures, disorders of cortical development, and those with normal MRI will require extensive, sometimes repetitive studies with PET, SPECT, and intracranial electrode placement, which escalate enormously the cost of presurgical evaluation.20 Even with these expensive evaluations, in this group of patients, the postoperative outcome is often not favorable.26,27 A stepwise approach by initially operating on best outcome patients and reserving more difficult to treat patients to a later date as experience develops will help each center to understand its capabilities and limitations and to move forward.21 As detailed below, in evolving the most productive epilepsy surgery program in India today, the R. Madhavan Nayar Center for Comprehensive Epilepsy Care, Trivandum, has given due emphasis to address the above special issues relevant to epilepsy care in developing countries. R. Madhavan Nayar Center for Comprehensive Epilepsy Care, Trivandum The center is named after the late R. Madhavan Nayar, a pioneering industrialist of Kerala, who donated a generous sum of money to start a comprehensive epilepsy care program.15 Three neurologists, two neurosurgeons, two neuroradiologists, a psychologist, a psychiatrist, and a medical social worker spend 25–50% of their working time with the epilepsy program. A three-patient video-EEG monitoring facility performs on an average 300 long-term monitoring studies
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Epilepsy surgery in India annually. A facility to do functional studies, spectroscopy, and T2 relaxometry was added recently to the 1.5 Tesla MRI already available. Patients are classified according to their income into four categories; while the poorest group (~15% of patients) receives totally free treatment, the richest group (~30%) will have to bear the total hospital charges, and the intermediate groups pays 50–75% of the incurred actual cost. The center is sustained by the income generated through patient charges and by the financial support received from the Government of India for caring for the underprivileged. In addition, a local patient organization, Epilepsy Self Help Group, chips in with financial assistance for the needy through the donations it receives.15 The first epilepsy surgery (anterior temporal lobectomy with amygdalohippocampectomy) at the R. Madhavan Nayar Center for Comprehensive Epilepsy Care was undertaken on March 20, 1995. The patient was a 25-year-old gentleman with left mesial temporal sclerosis and medically refractory complex partial seizures. The important milestones of the surgical program and the break up of 706 epilepsy surgeries performed upto December 31, 2005 are provided in Tables 16b.1 and 16b.2, respectively. prior to September 2001, all the candidates were selected by noninvasive protocol utilizing history, clinical examination, interictal and ictal scalp EEG, high resolution MRI, and neuropsychological evaluation data, and all surgeries were done under general anesthesia. Nearly 90% of the patients operated during this period had MTLE-HS or MRI identified other focal lesions not adjacent to eloquent areas. Sphenoidal electrodes were inserted during long-term video-EEG monitoring of patients with suspected TLE only
Table 16b.1 Major milestones of the R. Madhavan Nayar Center for Comprehensive Epilepsy Care, Trivandrum 1st epilepsy surgery 100th epilepsy surgery 200th epilepsy surgery 300th epilepsy surgery 400th epilepsy surgery 500th epilepsy surgery 600th epilepsy surgery 700th epilepsy surgery
March 20, 1995 October 28, 1997 April 22, 1999 October 5, 2000 March 25, 2002 August 1, 2003 September 24, 2004 November 24, 2005
Table 16b.2 Epilepsy surgeries undertaken at the R. Madhavan Nayar Center for Comprehensive Epilepsy Care, Trivandrum from March 1995 through December 2005 Procedure Temporal lobe resections Extratemporal resections Corpus callosotomy Hemispherectomy/hemispherotomy Total
No. 588 70 18 30 706
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when initial scalp recorded ictal EEG pattern is poorly visualized or contaminated by movement artifacts.28 Wada test was undertaken only in those patients in whom dominant extended temporal lobe resection is planned and in whom neuropsychological testing has revealed bilateral or discordant memory dysfunction. Even in patients with apparent TLE and normal MRI, careful analysis of the non-invasive data could identify favorable surgical candidates.29 Such strategies prevented unnecessary escalation of the cost of temporal lobe epilepsy surgery. The non-invasive presurgical evaluation data of every patient is thoroughly discussed in the weekly patient management conference to collectively decide about surgical candidacy and to decide about further evaluation strategy in those with discordant features (Figure 16b.2). With the experience gained through the initial five years, intraoperative ECoG, subdural and depth electrode placements, and intraoperative and extraoperative cortical stimulation and mapping was started in 2001. These procedures have helped us to select patients whose epileptogenic zone could not be localized by non-invasive means and those with lesions such as malformations of cortical development close to eloquent areas. The R. Madhavan Nayar Center for Comprehensive Epilepsy Care is presently the only center in the country performing invasive presurgical evaluation. Upto December 31, 2005, 18 patients underwent long-term monitoring with bilateral temporal depth electrodes and 25 patients with subdural grid and strip electrodes placements. The Wada test is being replaced by functional MRI. During the last year, more restricted resective procedures such as selective amygdalohippocampectomy through subtemporal approach were being increasingly undertaken. Functional hemispherotomy is preferred to hemispherectomy for extensive unihemispherical lesions. The step-wise evolution of the epilepsy surgery program at the R. Madhavan Nayar Center for Comprehensive Epilepsy Care as outlined above is illustrated through some case scenarios in Figure 16b.3. Out of 351 patients with MTLE-HS operated on between March 1995 and March 2002 and have completed 2 years or more of post-operative follow-up, 286 (81.5%) are seizurefree, and 132 (37.7%) of them have been completely weaned off the antiepileptic drugs. During the median follow-up period of 4 years following surgery, out of 34 patients with tumoral TLE, 27 (79%) achieved a completely seizure-free state. Out of 46 patients with lesional extratemporal lobe epilepsies, 25 (55.6%) were seizure free during a median postsurgery follow-up of 4 years. Of the 6 patients operated for hypothalamic hamartoma through a transcallosal interforniceal approach, two were completely seizure free and three had more than 75% reduction of the seizures. Out of the 21 patients who completed ≥1 year of follow up following hemispherectomy/hemispherotomy, 18 patients (90%) became seizure free and 2 patients had more than 75% seizure freedom. One patient died a few hours following an uneventful anterior temporal lobectomy, the cause of which remained obscure. Three patients, following anterior temporal lobectomy, developed disabling hemiplegia due to vascular injury. An abscess at the site of an intracranial grid electrode occurred in one patient, who made a recovery without sequel following
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(a)
(b) Figure 16b.2
Discussion on (a) clinical, (b) radiological and
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(c) Figure 16b.2 cont’d (c) video-EEG data in progress during the weekly patient management conference at the R. Madhavan Nayar Center for Comprehensive Epilepsy Care, Trivandrum.
surgical drainage and antibiotic therapy. The rest of the complications were either minor or transient. Other epilepsy surgery centers The All India Institute of Medical Sciences, New Delhi has undertaken 273 epilepsy surgeries from April 1995 through December 2005, the break-up of which is given in Table 16b.3. Among the 121 patients operated for refractory epilepsy at the National Institute of Mental Health and Neurosciences, Bangalore, between 1998 and December 2005, 90 had anterior temporal lobectomy, 30 had lesionectomy, and 1 had corpus callosotomy. Detailed post-operative outcome data from these centers are not yet available, although preliminary results are comparable to those from the R. Madhavan Nayar Center for Comprehensive Epilepsy Care, Trivandrum.30,31 The following centers in India have performed less than 50 epilepsy surgeries, during the last five years, Nizam’s Institute of Medical Sciences, Hyderabad, CARE Hospital, Hyderabad, KEM Hospital, Mumbai, Jaslok Hospital, Mumbai, Poona Neurological Institute, Poona, Jahanghir Hospital, Poona, Postgraduate Institute of Medical Education and Research, Chandigarh, and Lourdes Hospital, Kochi. The National Hospital, Colombo, Sri Lanka has a very successful epilepsy surgery program and has offered surgery to nearly 60 patients in the last 3 years. The R Madhavan Nayar Center for Comprehensive Epilepsy Care, Trivandrum has actively participated in the development of the Sri Lankan program.
Future perspectives In India, with over one billion inhabitants, there are approximately one million persons with medically refractory epilepsy; among them as many as one-quarter to one-half are potential surgical candidates. However, no more than 150 epilepsy surgeries are currently being performed per year in India. Thus, only a minuscule of potential surgical candidates in India and other developing countries ever get a chance to undergo presurgical evaluation. The lack of availability and affordability has resulted in an enormous gap in developing countries between number of patients who could be benefited from epilepsy surgery and those who actually receive this treatment, which can only be minimized by developing more centers in the country, where epilepsy surgery can be undertaken. The out-of-pocket payment for epilepsy surgery (including non-invasive presurgical evaluation) at the R. Madhavan Nayar Center for Comprehensive Epilepsy Care is Rs. 50,000 (US$1200).21 With invasive evaluation the cost would escalate to two to threefold of this amount. The computed direct total cost for caring a patient with refractory temporal lobe epilepsy from age 26 to 60 years works out to be Rs. 200,000 (US$5000).21 The results from R. Madhavan Nayar Center for Comprehensive Epilepsy Care, Trivandrum and other epilepsy surgery centers in India show that over 70% of patients will be seizure-free following surgery for temporal lobe epilepsy, and there is a 30% chance that they will be
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(a)
(b)
(c)
(d)
(a)
(b)
Figure 16b.3 Case scenarios from R. Madhavan Nayar Center for Comprehensive Epilepsy Care, Trivandrum, to illustrate step-wise progress with time from straightforward to more complicated and advanced presurgical evaluation and surgical strategy. (i) Selection for epilepsy surgery by noninvasive evaluation: (a) right temporal spike discharges on scalp EEG, (b) right hippocampal atrophy on T1 weighted coronal MRI, (c) left upper extremity dystonic posturing during a complex partial seizure, and (d) rhythmic EEG activity during the seizure. Patient is seizure-free since right anterior temporal lobectomy with amygdalohippocampectomy on May 1997. (ii) A 14-year-old boy with refractory partial seizures with inconclusive scalp EEG data: (a) left occipital gliotic lesion in T1 weighted MRI, (b) left occipital-parietal grid electrode, and
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Epilepsy surgery in India LOG1-FPZ
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11:29:37
LOG2-FPZ LOG3-FPZ LOG4-FPZ LOG5-FPZ LOG6-FPZ LOG9-FPZ LO10-FPZ LO11-FPZ LO12-FPZ LO13-FPZ LO14-FPZ LO17-FPZ LO18-FPZ LO19-FPZ LO20-FPZ LO21-FPZ LO25-FPZ LO26-FPZ LO27-FPZ LO28-FPZ LO29-FPZ LO30-FPZ ROS1-FPZ ROS2-FPZ ROS3-FPZ ROS4-FPZ ROS1-FPZ ROS2-FPZ ROS3-FPZ ROS4-FPZ FPZ
(c)
Figure 16b.3, cont’d (c) seizure origin from left occipital region. Seizure free since left occipital lobectomy on January 2002. (iii) A 42-year old male with inconclusive scalp EEG data. Inset shows stereotactically placed bilateral temporal depth electrodes. Seizure origin from anterior contacts of right hippocampal depth electrode. Seizure-free since right anterior temporal lobectomy with amygdalohippocampectomy on April 2003. Continued
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(a)
(b)
Figure 16b.3, cont’d (iv) A 20-year-old female with (a) left frontal cortical dysplasia close to motor and speech areas in T2 weighted MRI, (b) awake craniotomy and cortical stimulation mapped motor cortex (m), sensory cortex (s), Broca’s area (l), and central sulcus (c). Area R was resected without any neurological deficit on June 2004. After a complete seizure freedom during first post-operative year, she had had recurrence with few non-disabling seizures.
(a) Figure 16b.3, cont’d (v) A 13-year-old left handed boy with refractory focal seizures and mild right hemiparesis due to hemorrahagic disease of new born. (a) axial MRI FLAIR sequences shows marked gliosis and atrophy of the left hemisphere with relative preservation of the primary sensory-motor cortex (arrow).
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(b)
Figure 16b.3, cont’d (b) inline BOLD MRI right finger tapping versus rest shows left motor cortex activation, and (c) inline BOLD MRI verbal fluency versus silence shows strongly right hemisphrere lateralized language distribution. Based on the information, left motor strip was spared during hemispherotomy performed on July 2005 with little post-operative weakness of right-sided extremities. No seizure recurrence during six months’ follow-up.
Table 16.3 Epilepsy surgeries undertaken at the All India Institute of Medical Sciences, New Delhi, from April 1995 through December 2005 Procedure Temporal lobe resctions Extratemporal resections Corpus callosotomy Hemispherectomy/hemispherotomy Total
No. 204 51 12 6 273
employed, achieve an improved quality of life, and often becomes a productive member of society. Therefore, surgical treatment of refractory temporal lobe epilepsy is definitely a better cost-effective option than continued medical treatment even in developing countries. Epilepsy centers in developing countries could effectively use these statistics to obtain governmental subsidies and non-governmental financial supports for implementing and sustaining epilepsy surgery programs.
Conclusions completely off antiepileptic drugs within 2 years following surgery.12,30 Even with new antiepileptic drugs, complete seizure freedom occurs in only less than 10% of temporal lobe epilepsy patients.32 A seizure-free person could be better
In order to become cost-effective, epilepsy surgery centers in India will have to achieve excellent results by selecting candidates destined to have a seizure-free outcome using locally available limited technology and expertise, without compromising on patient safety. The recent experience from epilepsy
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surgery centers in India illustrates that this goal can be accomplished by selecting patients whose epileptogenic zone can be unquestionably established, based on history, high resolution MRI, and interictal and ictal scalp EEG findings such as those with MTLE-HS, and those with circumscribed potentially epileptogenic lesions. A stepwise approach by reserving more difficult to treat patients at a later date as experience develops,
or by referring them to a better-equipped center, will help each center to understand its capabilities and limitations and to move forward. It is encouraging to note that, despite major challenges, in the last decade, several epilepsy centers in India have not only successfully implemented epilepsy surgery programs, but have also produced results comparable to that from developed countries at a fractional cost.
REFERENCES 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15.
16. 17. 18.
Sankhyan AR, Weber GHJ. Evidence of surgery in ancient India: Trepanation at Burzahom (Kashmir) over 4000 years ago. Int J Osteoarchaeol 2001;11:375–80. Chandy J. Surgical treatment of epilepsy. Neurol India 1954;2:37–41. Wolf P. History of epilepsy surgery: introduction. In: Lüders HO, Comair YG, eds. Epilepsy Surgery, Second Edition. Philadelphia: Lippincott Williams & Wilkins, 2001:19–21. Karpurkar AP, Pandya SK. Neurosurgery in India. Neurosurg Rev 1983;6:85–92. Ramamurthi B. Uphill All the Way. An Autobiography. Chennai: Guardian Press, 2000. Mathai KV, Chandy J. Surgical treatment of temporal lobe seizures. Neurol India 1970;18:158–64. Abraham J. Surgery for temporal lobe epilepsy. Neurol India 1980;28:175–9. Ramamurthi B. Focal fits. Arch Neurol 1965;13:545–6. Ramamurthi B, Balasubramaniam V, Kalyanaraman S, Arjundas G, Jagannathan K. Stereotaxic ablation of the irritable focus in temporal lobe epilepsy. Confin Neurol 1970;32:316–21. Ramamurthi B. Myoclonic epilepsy treated by combined stereotactic lesions (a case report). Neurol India 1972;20:158–60. Daniel RT, Chandy MJ. Epilepsy surgery. Overview of forty years experience. Neurol India 1999;47:98–103. Rao MB, Radhakrishnan K. Is epilepsy surgery possible in countries with limited resources? Epilepsia 2000;41(Suppl. 4):S31–4. Özkara Ç, Özurt E, Hanoglu L, et al. Surgical outcome of epilepsy patients evaluated with a noninvasive protocol. Epilepsia 2000;41(Suppl. 4):S41–4. Wieser H-G, Silfvenius H. Overview: epilepsy surgery in developing countries. Epilepsia 2000;41 (Suppl. 4):S3–9. Radhakrishnan K. The R. Madhavan Nayar Center for Comprehensive Epilepsy Care. In: Radhakrishnan K, ed. Silver Lines. Trivandrum: Sree Chitra Tirunal Institute for Medical Sciences and Technology 2004:163–89. Engel J Jr. Surgery for seizures. N Engl J Med 1996;334:647–52. Mani KS. Global campaign against epilepsy. Agenda for IEA/IES. Neurol India 1998;46:1–4. Gopinath B, Radhakrishnan K, Sarma PS, Jayachandran D, Alexander A. A questionnaire survey about doctor-patient communication, compliance and locus of control among South Indian people with epilepsy. Epilepsy Res 2000;39:73–82.
19.
20. 21. 22. 23. 24. 25. 26. 27. 28. 29.
30. 31. 32.
Radhakrishnan K, Nayak SD, Kumar SP, Sarma PS. Profile of antiepileptic pharmacotherapy in a tertiary referral center in South India: a pharmacoepidemiologic and pharmacoeconomic study. Epilepsia 1999;40:179–85. Engel J Jr. Multimodal approaches in the evaluation of patients for epilepsy surgery. Clin Neurophysiol 1999;50(Suppl):40–52. Sylaja PN, Radhakrishnan K. Surgical management of epilepsy. Problems and pitfalls in developing countries. Epilepsia 2003;44 (Suppl. 1):48–50. Radhakrishnan K. Medically refractory epilepsy. In: Radhakrishnan K, ed. Medically Refractory Epilepsy. Trivandrum, India: Sree Chitra Tirunal Institute for Medical Sciences and Technology, 1999:1–39. ILAE Commission Report. Mesial temporal lobe epilepsy with hippocampal sclerosis. Epilepsia 2004;45:695–714. Radhakrishnan K, So EL, Silbert PL et al. Predictors of outcome of anterior temporal lobectomy for intractable epilepsy. A multivariate study. Neurology 1998;51:465–71. Holmes MD, Dodrill CB, Ojemann LM, Ojemann LM. Five-year outcome after epilepsy surgery in nonmonitored and monitored surgical candidates. Epilepsia 1996;37:748–52. Zentner J, Hufnagel A, Ostertun B, et al. Surgical treatment of extratemporal epilepsy:clinical, radiologic, and histopathologic findings in 60 patients. Epilepsia 1996;37:1972–80. Edwards JC, Wyllie E, Ruggeri PM, et al. Seizure outcome after surgery for epilepsy due to malformations of cortical development. Neurology 2000;55:1110–4. Sylaja PN, Radhakrishnan K. The role of scalp EEG in the presurgical evaluation of patients with medically refractory temporal lobe epilepsy. Am J END Technol 2001;41:116–35. Sylaja PN, Radhakrishnan K, Kesavadas C, Sarma PS. Seizure outcome after anterior temporal lobectomy and its predictors in patients with apparent temporal lobe epilepsy and normal MRI. Epilepsia 2004;45:803–8. Bhatia M, Singh VP, Jain S, et al. Epilepsy surgery in India: All India Institute of Medical Sciences experience. J Assoc Physicians India 1999;47:492–5. Shukla G, Bhatia M, Singh VP, et al. Successful selection of patients with intractable extratemporal epilepsy using non-invasive investigations. Seizure 2003;12:573–6. Walker MC, Sander JWAS. The impact of new antiepileptic drugs on the prognosis of epilepsy: seizure freedom should be the ultimate goal. Neurology 1996:46:912–14.
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Treatment of epilepsy in Australia A Mohamed
Introduction Despite a relatively small population, Australia is the sixth largest nation in area following Russia, Canada, China, the United States of America, and Brazil. It is a very dry continent with most of the population living in its coastal margins. It is a federation of six states and two territories. The largest state, Western Australia, is about the same size as Western Europe. Over 60,000 years before the arrival of European settlers in 1788, Aboriginal and Torres Strait Islander peoples inhabited most areas of the Australian continent. There were an estimated 300,000 Indigenous Australians living on the continent. Today, the population of Australia is slightly over 20 million and concentrated in large cities around the coast (Table 17.1).
Epilepsy and illness in the indigenous population Aboriginal groups prior to European settlement were traditional hunter and gatherer communities and had enviable health in terms of nutrition and leisure. They lived in small closed groups of kin. The population numbers depended on availability of water and other essential resources. These groups followed up a more or less nomadic lifestyle. Most aboriginal groups were spread sparsely over the continent that mitigated against the spread of disease. These small groups followed a seasonal pattern of movement within a defined territory to which they had spiritual ties. Periodically, they would congregate in large numbers for ceremonial purposes or seasonal abundance of some food store at a particular site.1 In aboriginal culture prior to European settlement, sorcery or black magic provided an explanation of illness, pain, or death where the cause was not known or obvious. The explanations were always personal or spiritual. Someone or some spiritual powers performed black magic on the victim because of animosity or because the victim had broken a taboo. Aboriginal healers were able either to restore health or at least the group, via sorcery, could retain equilibrium. Not to know the cause of the illness or death was a disturbing factor in the psychological and social life of the group – therefore an acceptable explanation was necessary to enable the community to readjust itself to the events and go about its business.2 The sick were kept tranquil in a familiar environment with their own people about them hearing familiar voices and passed away in peace with their own kind when death was upon them.1 The aboriginal healer symbolically extracted a bone, quartz, or other stone from the patient’s body or would bring back the
wandering soul through rituals, and all was well. If the patient could not be healed, both the patient and group would prepare for death. The patient was also in a condition of high suggestibility and was ready to realize the idea suggested by the aboriginal healer. If told that he was healed, he would be reassured and prepare for improvement. Likewise, if a doctor suggested that death was inevitable, the patient would think of the spirits of the departed, turn his face to the wall, and prepare for death.2 There is no evidence that aboriginal culture placed a premium on abnormality or the epileptic. There was no reverence for epileptic patients as found in other cultures.2 Aboriginal medicine men, far from being charlatans, were men of high degree and had degrees in the secret of life beyond that taken by most adults. This required discipline, mental training, courage and confidence. Their positions commanded respect, and they were men of outstanding personality. In addition, the psychological health of the group largely depended on their powers, and they specialized in the working of the human mind.2 Despite some notable improvements in the past 20 years, the health status of aboriginal people remains of great concern. They carry a double burden of disease – not only disease of poverty but increasingly disease characteristic of a Western lifestyle. Leading causes of death includes cardiorespiratory diseases, accidents and to moving trauma, suicide, violence, and cancer.1 Incidence of epilepsy existing in the Aboriginal community is at least of the same proportion as the rest of Australia (1–2%). However this is probably an underestimate due to lifestyle factors such as alcoholism, substance abuse, and injury.
History of epilepsy in Australia after European settlement The early history of the treatment of epilepsy in Australia closely followed the path paved in the UK because of the close relationship between the two countries. Australia’s geographical isolation and low population density were compensated for by a tradition of overseas travel by doctors to undertake postgraduate studies in Europe. As with many European countries, during the 19th century, it was customary for epileptics to be institutionalized as they were thought as unfit to be at large. Epilepsy was thought to be a precursor of insanity. Many with brain disorders were institutionalized in prisons side-by-side with felons. In early Australian European settlements, the incidence of epilepsy in the prison population varied from 7 to 13%.3 The conditions in the prisons were grim and poor and it was not until later in 145
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Population and area of Australian state and territories
State or territory Queensland New South Wales Australian Capital Territory Victoria Tasmania South Australia Western Australia Northern Territory Australia
Area (square km) 1,723,936 800,628 2,358 227,010 64,519 978,810 2,526,786 1,335,742 7,659,861
Population
Capital city
3.64 m 6.61 m 0.32 m 4.82 m 0.47 m 1.51 m 1.9 m 0.2 m 19.47 m
Brisbane (1.65 m) Sydney (4.15 m) Canverra (0.32 m) Melbourne (3.49 m) Hobart (0.20 m) Adelaide (1.11 m) Perth (1.38 m) Darwin (0.11 m) 12.41 m
Source: Australian Bureau of Statistics Census 2001. Estimated June 30 2001.
the 19th century where most people with epilepsy were managed in asylums for the mentally ill.3 Towards the end of the 19th century, in the two large colonies of the time, New South Wales and Victoria, the decision was made to manage epileptics in institutions for the mentally ill.3,4 The very first asylum was created in 1811 in Castle Hill in the outskirts of Sydney. The second asylum outside New South Wales opened in 1848 at Yarra Bend in Victoria, although many sufferers were still managed at home by family and local doctors.5 Poverty, strained family relationships, and unemployment often played in large part in incarceration of these patients. Conditions in these asylums were very poor. Many of these patients suffered from a large number of physical illnesses including tuberculosis.6 In Sydney, patients in one institution (Galdesville Hospital) were dying from typhoid and infectious diseases due to inadequate sewerage.4 Early in the 20th century, there was a shift of attitudes that allowed the liberation of epileptics to asylums. This change in attitude together with campaigns by medical practitioners and activists led to a number of government inquiries4 that in turn led to the development of epileptic colonies in Sydney and Melbourne. In Sydney, moral therapists spearheaded these reforms. Work was created for epileptics and seen as a therapeutic instrument.3 Attendance of church was encouraged and libraries and newspapers were furnished for the patients. Prior to Hughlings Jackson’s postulate that epilepsy was disease of the cortex, a variety of causes were hypothesized for seizures. These included alcohol, worms, anxiety, and masturbation.3 In the late 18th century, medical treatments of epilepsy in Australia included:3 ● ● ● ●
● ● ● ● ● ● ●
Quiet rest, the feet placed in hot water and mustard bath Shaving of the scalp Mustard plaster to the back of the head Cooling of the head by a mixture of spirit of vinegar and water Bleeding in letting five fluid ounces of blood at a time Leeches to the temples Blister to the nape of the neck Use of prolonged chloroform anaesthesia Morphia Bromides introduced by Dr. Smith in 1873 Blistering where local limb auras occurred.
At this time the treatment for epilepsy in the USA included bromides, arsenic, quinine, cod liver oil, iron, and hysterectomies.7 The concept of epilepsy as a disease of the cortex was introduced to Australia in a paper in 1886 by John Springthorpe.8 He also recommended a systematic approach to treatment. This included removal of any irritants: bromides, zinc oxide, belladonna, atropine, cannabis, digitalis, and a Seton tie at the back of the neck. The Seton tie was a silk or cotton twine that was inserted through a large flap of skin and left there until a chronic running sore was created with drainage of pus from around the seton.9 The surgical treatment of epilepsy was first detailed by Dr. John Maund10 in 1856 and later by Dr. Poulton in 1890.11 In 1856 a patient with post-traumatic epilepsy who had an old depressed skull fracture and had failed medical therapy was treated successfully with trephining and removal of the bone at the side of the fracture – this occurred prior to the introduction of antiseptic techniques in cranial surgery by Horsely in 1880s.3
The beginnings of epilepsy surgery in Australia Peter Bladin created the first epilepsy center in 1969 at the Austin Hospital in Melbourne. This was a nationwide service that provided the first comprehensive epilepsy program in Australia. Between 1969 and 1991 this program performed over 200 temporal lobectomies for refractory epilepsy.12 In the late 1970s and early 1980s epilepsy centers were also established in three other Melbourne hospitals. In the early 1970s in Sydney, a lavishly equipped and staffed Brain Research Institute at Rozelle Hospital was established, where psychiatrists, neurologists, and neurosurgeons worked together to select patients for psychosurgery. Part of the workup involved the insertion, under stereotactic guidance, of recording electrodes into the hippocampus and amygdala. They were particularly interested in rage attacks, and whether these were due to epileptic activity in the amygdala. In the late 1970s there was public disquiet over such surgery (Figure 17.1). A royal commission was called that led to the shut down of this unit. The first comprehensive epilepsy center in Sydney was established in 1977 in Royal Prince Alfred Hospital13 (Figure 17.2) with centers at Prince Henry
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(a)
Figure 17.1 A Sydney tabloid reports on psychosurgery in 1977 (copyright permission).
and Westmead Hospitals being established soon after. Between the years 1990 and 1997, 226 temporal lobectomies and 40 extra temporal lobe surgeries were performed at the three adult epilepsy centers in Sydney (personal communication). Epilepsy surgery for refractory epilepsy in children were first performed at The Royal Children’s Hospital in Melbourne in 1979 and in Sydney in 1988. An epilepsy surgery center was established in Western Australia in 1989 and by 2002, 122 patients were assessed for surgery.
Conclusion There is little known of the treatment of epilepsy by the aboriginal population prior to European settlement.
(b) Figure 17.2 Epilepsy monitoring unit at Royal Prince Alfred Hospital in 1990.
However, various sources suggest that the aboriginal had good health and a spiritualistic approach to illness. The treatment of epilepsy in Australia after 1788 paralleled that seen in Europe and in particular in the UK due to the close ties between the two countries. Epilepsy surgery, first pioneered in Melbourne, has become available at a number of epilepsy centers in a country with a large geographical area, and its population concentrated in large coastal cities.
REFERENCES 1. 2. 3.
4. 5. 6. 7.
Bates D. The Passing of the Aborigines. London: Granada Publishing Ltd., 1972. Pelkin AP. Aboriginal Men of High degree. St. Lucia: University of Queensland Press, 1945. Bladin PF. A Century of Prejudice and Progress: A Paradigm of Epilepsy in a Developing Society, Medical and Social Aspects, Victoria, Australia, 1835–1950. Camberwell [Australia]: Epilepsy Australia, 2001. Garton S. Palaces for the unfortunate: lunatic asylums in New South Wales 1880–1940. Journal of the Royal Australian Historical Society 1991;76(4):297–312. Springthorpe JW. Notes on 21 cases of epilepsy. AMJ 1886: 101–105. Chesters J. ‘Not under proper care and control’: researching mental illness in East Gippsland. In: Gippsland Heritage Journal 1996:15–20. Mills CK. The treatment of epilepsy. JAMA 1886;154.
8. 9. 10. 11. 12. 13.
Bladin PF. John William Springthorpe, 1855–1933: Early Australian epileptologist and keeper of the flame for neurosciences. Journal of Clinical Neuroscience 2004;11(1):8–15. Bladin PF. A seton tried in the back of the neck: chronic suppuration in the treatment of epilepsy. Journal of Clinical Neuroscience 1998;5(1):17–19. Maund J. Epilepsy produced by pressure on the brain. AMJ 1856; 1:97–9. Poulton B. The case of trephining for epilepsy. Australasia Medical Gazette 1890:88–9. Popovic EA, Fabinyi GCA, Brazenor GA, Berkovic SF, Bladin PF. Temporal Iobectomy for epilepsy – complications in 200 patients. Journal of Clinical Neuroscience 1995;2(3):238–44. Radmanovich A, McMahon C, Noakes P, Healy L. The programme for the surgical treatment of epilepsy at the Royal Prince Alfred Hospital, Sydney, NSW. Australasian Journal of Neuroscience 1991;4(2):13–18.
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Epilepsy surgery in Korea BI Lee
Traditional oriental medicine Historically, Korean traditional medicine largely adopted the Chinese medicine since its beginning about 5,000 years ago. ‘Fifty-two Diseases’, the earliest Chinese medical record written 3,000 years ago, described symptoms of epilepsy and its treatment consisting of ‘repeat bathing with fluid containing a brain pill’ called ‘ ( : brain, : tablet, : drug)’. This indicated that ancient Chinese doctors had already known that epilepsy was originating from the brain. Despite their clear insight on the origin of epilepsy there has been no record describing any surgical treatment of epilepsy throughout the prolonged history of Chinese medicine. The major treatment modality of epilepsy in Chinese medicine consisted of various prescriptions using herbs, minerals, and materials from animals, and various procedures such as acupunctures, massages, and moxacautery. In the early 16th century, Dr. Joon Huh, the father of Korean traditional medicine, wrote a book called ‘ ( : east, : medicine, : gems, : book)’, which had summarized his clinical experiences as well as previous medical knowledge available in Korean and Chinese medical literature. He classified epilepsy into eight types based on charateristic symptoms, age of onset, and the traditional concept of etiopathogenesis. The book, which is still regarded as the textbook of Korean traditional doctors, has described more than 300 prescriptions and various procedures applicable to different types of seizures but none for the surgical treatment of epilepsies.1
Severance Medical School was united with Yonhee University to form Yonsei University.2 Korea was colonized by Japan from 1910 to 1945 and the Korean War occurred from 1950 to 1953. During the period, Korean society was seriously abandoned and most post-war medical activities were heavily dependent upon US aid. The modern medical management of epilepsy was initiated by Dr. L. Robinson (Figure 18.4) who was also an American medical missionary. She treated a girl suffering from epilepsy with phenytoin in 1963 and organized a mobile epilepsy clinic in association with Korean neurosurgeons and psychiatrists in 1964. These activities generated great hope among many patients and their families to organize the ‘Rose Club’, which did take initiatives of social movement as well as medical care for epilepsy. The rising phase of the Rose Club reached its peak during the 1970s and the first International Bureau Workshop for Epilepsy was held in the Severance Hospital on December, 1974. The Rose Club had grown to a huge social organization holding approximately 100,000 patients and their families and became a local chapter of IBE in 1979. Starting from 1980, the Korean economy had risen rapidly and most antiepileptic drugs became widely available in community hospitals. During this transitional period, the epilepsy care in Korea has gradually shifted from the Rose Club to community hospitals and the activities of the Rose club had gradually transformed into that of a lay
Era of Western medicine Western medicine was first introduced by Dr. H.N. Allen (Figure 18.1) in 1884, who was the medical missionary from the North Presbyterian Denomination. He built a Royal Hospital called ‘ ’ (House of Universal Helpfulness, Figure 18.2) in 1885 by the sponsorship of King Kojong of Lee Dynasty. which was the first hospital practicing western medicine in Korea. In 1886, Dr. Allen started his medical education which was succeeded by Dr. Avison. He was the first principal of (Chejungwon Medical School) and trained several assistant students. Among these, seven students had graduated in 1908 who were the first Korean medical doctors. In 1900, Mr. Severance in Cleveland, Ohio, donated $15,000 for the construction of a modern medical school and hospital which was opened in 1904 (Figure 18.3). The new medical complex was named the Severance Hospital and Medical School in memory of his generous contribution. In 1959, 148
Figure 18.1 Dr. Horace Newton Allen (1858–1932). He founded the first hospital practicing western medicine (Chejungwon) in 1885 with the support of King Kojong of Lee dynasty.
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Figure 18.2 (House of Universal Helpfulness). The first hospital practicing western medicine, which was established by Dr. H.N. Allen in 1885. The hospital was located in Che-dong, Seoul.
people’s organization. In 1982, the Korean Neurology Association was established to start a nationwide training program of neurology residents. In 1988, an epilepsy clinic was opened at Yonsei University Medical Center (Severance Hospital), which was the beginning of a specialized program for the care of epilepsy in Korea. In 1996, the Korean Epilepsy Society was organized and the major part of the Rose Club became the Korean Epilepsy Association, which has greately promoted the quality of epilepsy care in Korea.
Era of epilepsy surgery Dr. C.K. Lee (Figure 18.5), a neurosurgeon who had a postdoctoral training at the Montreal Neurological Institute in Canada, started epilepsy surgery from 1966 and published his surgical experiences of 51 cases suffering from intractable epilepsies in 1972.3 His surgical technique was the electrocoagulation of the
Figure 18.3 Severance Hospital and Medical School in 1904, which was built with the generous donation of Mr. Severance in Cleveland, Ohio. This building was located in Do-dong, Seoul. In 1995, this building was replaced by a 20-storey office building (Yonsei Severance Building) for the purpose of finacially supporting Yonsei University.
149
Figure 18.4 Dr. Lennabelle Robinson (1904–) in the center, who is discussing with Korean doctors (Dr. M.H. Kim in the left and Dr. W.S. Kang on the right) about the activities of the Rose Club.
preoccipital cortex. He considered that the preoccipital cortex was the main pathway of spreading ictal discharges and its interruption by electrocoagulation should be beneficial for the amelioration of seizures. He recorded electrocorticography (ECoG) before the electrocoagulation and observed its change after intracortical injection of procainamide to predict surgical outcome (Figure 18.6). Among 51 patients, 3 patients became seizure free and 26 patients achieved a significant improvement after the procedure. In 1980, Dr. D.S. Chung and his colleagues at Catholic University started epilepsy surgery and published their surgical experience consisting of seven cases of corpus callosotomy and eight cases of selective amygdalohippocampectomy in 1989.4 Nine patients showed significant improvement and none got worse. In this series, they did not perform any dedicated presurgical evaluations but their surgery was undertaken on the basis of clinical judgment, routine scalp EEG, and CT scan. The modern epilepsy surgery program employing the protocol of advanced presurgical evaluation was initiated at the Severance Hospital of Yonsei University Medical
Figure 18.5 Dr. Chu Kul Lee (1914–) is the first neurosurgeon to perform epilepsy surgery in Korea.
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4 5 6
(a) 1 2 3
4 5 6
(b)
(c)
1 2 3
4 5 6
(d)
(e)
Figure 18.6 The first publication of epilepsy surgery in Korea (1972). Baseline electocorticogram of a patient showing multiple spikes at both preoccipital (leads 1, 2 and 3) and motor (leads 4, 5 and 6) areas (a) electrocorticograms showed no suppression of epileptiform discharges from the preoccipital region during (b) and after (c) procainization of the motor cortex. Electrocorticograms from the motor cortex showed the clear response during (d) and after (e) the procainization of the preoccipital cortex.
Center in 1988 by Dr. B.I. Lee and K. Huh who had returned to Korea after their completion of training in neurology (University of Minnesota) and epileptology (Cleveland Clinic and University of Georgia) in the USA. In the early 1990s many young neurologists and neurosurgeons with an interest in epilepsy surgery started to have fellowship trainings abroad and established surgery programs in major university hospitals upon their return to Korea.
Current status of epilepsy surgery With the opening of a specialized epilepsy care program at Yonsei University Medical Center in 1988, epilepsy sugery has
become rapidly recognized as an effective therapeutic measure for patients suffering from medically intractable epilepsies. In addition, the wide availability of MRI and EEG telemetry systems encouraged the organization of surgery programs in major university hospitals in Korea. During the late 1990s, 12 centers performed about 500 cases of epilepsy surgery annually and their surgical experiences started to appear in international epilepsy journals. However, the flourishing activities of many surgical centers had gradually declined from the year 2000, largely relating to the emergence of failure cases, shortage of patients requiring only basic presurgical evaluations, tough competitions among centers, and financial restrictions of presurgical evaluations imposed by National Health Insurance. As PET, SYSCOM, and advanced MR
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Table 18.1 Surgical cases performed by epilepsy surgery centers during 2005 in Korea Epilepsy surgery centers Procedures ATL/SAH CS: lesional Non-lesional HS/MLR Corpus callosotomy MST only VNS DBS r-Knife surgery Total
AMC
CBUH
DSMC
24 6 1 1 3 4 1 2 4 46
16 3 2 – 6 – – – – 27
12 5 3 – – – 5 – – 25
PHIU 1 2 3 4 4 – 5 – – 19
SNUH 29 56 14 1 2 – 6 – 2 111
SMC
YUMC
26 18 6 4 2 – 6 2 3 67
35 15 2 3 16 – 24 1 – 96
ATL/SAH, anterior temporal lobectomy/selective amygdalohippocampectomy; CS, cortisectomy; HS/MLR, hemisperectomy/multilobar resection, MST, multiple subpial transection; VNS, vagus nerve stimulation; DBS, deep brain stimulation; AMC, Asan Medical Center of Ulsan University (Seoul); CBUH, Chonbuk University Hospital (Cheonju); DSMC, Dongsan Medical Center of Kyemyung University (Daegu); PHIU, Paik’s Hospital of Inje University (Seoul); SNUH, Seoul National University Hospital (Seoul); SMC, Samsung Medical Center of Sungyunkwan University (Seoul); YUMC, Yonsei University Medical Center (Seoul).
technologies became available in the late 1990s, advanced imaging technologies became the forerunner of interhospital competitions and centers not equipped with these facilities faced great restrictions in their activities to close their surgical programs. At present, seven centers are mantaining their surgical activities and the number of surgical cases has diminished to around 350 cases per year (Table 18.1). Compared to the
gradual decrease in the number of resective surgeries, there has been a trend to increase implant of vagus nerve stimulation (VNS) for its simplicity, safety, and broad indications as well as its coverage by National Health Insurance. Deep brain stimulations (DBS) is also applied in a few centers despite its experimental stage of develop-ment. Magnetoencephalography (MEG) has become available recently.
REFERENCES 1. 2. 3.
Duk Gon Kim. Epileptology of Oriental Medicine, Seowondang Publisher, 1998. History of 100 years of Yonsei University (1885–1985) Yonsei University Press. 1985: Volume 1. Lee CK. Surgical treatment of epilepsy: preoccipital coagulation. J Kor Neurosurg Ass 1972;1:1–14.
4.
Chung DS, Sung KW, Lee JS, Choi CR, Song JU. The clinical analysis of surgical treatment in the medically intractable seizure. J Kor Neurosurg Ass. 1989;18(6):910–5.
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Epilepsy surgery in Thailand T Srikijvilaikul, C Locharernkul, and A Boongird
The history of epilepsy surgery in Thailand can be divided into the era before and after 1990. Before 1990 was the time of modern neurosurgery establishment by Thai pioneer neurosurgeons. After 1990, advanced epilepsy surgery has been established in Thailand in parallel with the development of a comprehensive epilepsy program with standard and state-of-the-art clinical practice.
History of epilepsy surgery in Thailand before 1990s Modern neurosurgery in Thailand began after a number of neurosurgeons returned from formal training in the USA in the late 1960s and established neurosurgical services at Siriraj and Chulalongkorn hospitals, the first two medical schools in Thailand. Pioneers on epilepsy surgery in the country were distinguished neurosurgeons, namely Professor Sira Bunyaratavej and Professor Charas Suwanwela. Due to the lack of computer technology and advanced imaging at that time, localization mainly relied upon clinical information, namely detailed history taking, highly precise neurological examination (Figure 19.1) and surface electroencephalogram (EEG) (Figure 19.2). Early imaging included skull series, scintigraphy or isotope brain scan, cerebral angiography, pneumoencephalograhy, and after the mid1970s, computerized tomography (CT). The surgical outcomes varied among patients. Surgical treatment of epilepsy was mainly resection of structural lesions causing seizures such as tumors, abscesses, vascular malformations, and depressed skull fracture scars. However, a few operations for intractable epilepsy were also performed. Hemispherectomy for a Sturge–Weber patient was first done by Professor Sira Bunyaratavej in 1966 (Bunyaratavej S, personal communication). Stereotactic amygdalotomy was performed in a case of temporal lobe epilepsy by Professor Charas Suwanwela in 1977 (Suwanwela C, operative record). At King Chulalongkorn Memorial Hospital, modern surgery of the brain was first established in 1963 by Professor Charas Suwanwela. Granted by the prestigious Anandamahidol Foundation under His Majesty King Bhumibol Adulyadej of Thailand, he finished his neurosurgical residency training from North Carolina and certified American Board of Neurological Surgery in 1961. He began modern neurosurgical therapy for Thai people at the Bangkok Bank Building (Figure 19.3). Early brain surgeries regarding epilepsy were mainly surgical removal of intracranial space occupying lesions producing seizures as 152
well as other neurological symptoms. However, the number of brain operations directed toward the correction of epileptic seizures was modestly reported. There were at least three patients who received cicatrectomy for their long-standing epilepsy. Two cases had refractory seizures from undiagnosed depressed skull fractures long after their head injuries. One of the two was a hospital worker who had become seizure free after the cortical scar was completely removed and with antiepileptic drugs maintained. Another patient suffered from a brain abscess close to the motor area. Intractable epilepsy developed one year after the abscess was drained.1 After the fibrous wall of the healed abscess was removed, his seizures were abolished without any post-operative neurological deficit. One hemispherectomy was performed on 13 November, 1989 by Professor Charas Suwanwela on a patient with cerebral hemiatrophy (Davidoff–Dyke syndrome) (Suwanwela C, personal communication). A 9-year-old boy suffered from very frequent desperate seizures and mental deterioration. Left hemiatrophic limbs with good motor powers were noted on examination. His CT scan revealed small right hemicranium with dilated ventricles. After one year of unsuccessful antiepileptic drug therapy, modified anatomical hemispherectomy was performed on the right cerebral hemisphere. Post-operatively, his seizures decreased significantly to 1–2 attacks per month resulting in much relief of his caregivers. Although left-sided hemiparesis was acquired from surgery and a wheelchair was
Figure 19.1 Professor Charas Suwanwela, a distinguished physician of early modern neurosurgery in Thailand, performing a highly precise neurological examination on a Thai patient in the 1970s.
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Development of epilepsy surgery after the 1990s
Figure 19.2 Professor Tongchan Hongsaladarom, a pioneer neurologist and electroencephalographer of Thailand, with the first ‘Grass’ paper EEG machine at EEG laboratory, Chulalongkorn University Hospital in the early 1960s.
needed, his postoperative reduction in seizures was greatly appreciated by his family. His condition has remained the same during the regular follow-up period of over 10 years. There was a study on focal convulsions from small cortical lesions by Suwanwela C et al. (unpublished data). Twenty-two patients who had epileptic attacks from lesions within the cerebral cortex were analyzed. Lesions larger than 2 cm in diameter were surgically removed. Among these cases, brain abscess were found in two patients and cysticercosis in one patient. However, conservative treatment was found to be the option in most patients since periodic brain CT disclosed spontaneous resolution in many cases and cysticercosis was postulated to be the cause of these vanishing granulomas. The authors recommended observation and follow-up instead of doing resective surgery in these epileptogenic infectious lesions.
The era of comprehensive epilepsy surgery program starts from early 1990, after a few young Thai neurologists and neurosurgeons returned from their full epilepsy trainings in distinguished western epilepsy centers. Brought back were the technical knowhow in modern epilepsy presurgical evaluation, state-of-the-art in surgical techniques and their enthusiasm in relieving epilepsy burden in Thai epileptics. A group of clinicians established the first comprehensive epilepsy program under a university hospital environment in 1994 known as Chulalongkorn Comprehensive Epilepsy Program, or CCEP (Table 19.1) with the second author being the founder and the director of the program. During this period, surgical treatment for epilepsy relied upon neurophysiologic data and advanced imagings. The first temporal lobectomy series for intractable epilepsy was introduced by Professor Sira Bunyaratavej and Professor Pongsakdi Visudhipan in July 1993.2 The epilepsy society of Thailand has been established by Professor Pongsakdi Visudhiphan and committee since 1996. The aim of the organization has focused on identification of surgical candidates for intractable epilepsy and educated both clinician and non-clinician workers to understand the options of epilepsy surgery and other medical aspects of epileptic patients care. This organization has consistently maintained policy and enrolled as a member of the International League Against Epilepsy (ILAE) in 1997 and the International Bureau for Epilepsy in 2004. The organization was honored to host the 5th Asian and Oceanean Epilepsy Congress in 2004. Other than CCEP and Ramathibodi hospital, there have been other epilepsy surgery services established in Bangkok, namely the Phramongkutklao Hospital and the Prasat Neurological Institute. However, CCEP has been considered the only advanced comprehensive epilepsy surgery center in Thailand since 1994.3,4 The details of CCEP development will be described in this chapter.
The strategies
Figure 19.3 The Bangkok Bank Building, ideally designed for neurology, neurosurgery, and psychiatry services on each floor in its three-storied structure was opened in 1960. Early neurosurgery, of the 1960s to modern epilepsy surgery of the 21st century took place here in its long evolutionary history. Now the location of the Chulalongkorn Comprehensive Epilepsy Program.
Thailand, as a developing country, has adapted its own pattern of epilepsy surgery development. Due to its 64 millions population in 2004, with accordingly high numbers of epilepsy cases, low average income per capita, and limited resources (Human Development Index rank 74 by United Nations Development Programme’s Human Development Report 2006), the surgical program development has aimed to serve most patients under cost-effective, sustainable, and selfsufficient economic strategies. In order to utilize resources as effective as possible, CCEP has been developed in four progressing phases, starting from the optimizing medical treatment phase (phase I, 1994–1996), the presurgical evaluation development phase (phase II, 1997–2000), the basic epilepsy surgery phase (phase III, 2001–2003) to the phase of surgery using advanced techniques (phase IV, 2004–present). The presurgical work-up using minimal standard procedures was developed step-by-step as necessary, to reach the target of rationale and economic practices.
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Table 19.1 Milestones of epilepsy surgery development at CCEP, Bangkok, Thailand The medical-technology arm 1994 1996
1997
1998 1999
2000
2001
2002
2003
2004
2005
Epilepsy Clinic* New AED trial
The public arm and the Royal patronage
Phase I (1994–1996) – Optimizing medical treatment 1996 Home visit program to improve patients’ compliance by CCEP and Thai Red Cross Society volunteers
Phase II (1997–2000) – Developing epilepsy presurgical evaluations 24-hour video EEG telemetry* 1997 Media and magazine campaigns on Epilepsy presurgical conference* epilepsy and epilepsy surgery First lesionectomy (temporal ganglioglioma) MRI using epilepsy protocol* 1998 Epilepsy patients working as volunteers Ictal SPECT* and employees in the epilepsy program Sphenoidal electrodes* 1999 ‘Light for Life Foundation for Epilepsy’ Wada test –Thai language version* established under HRH’s patronage for First anterior temporal resection for HS financial support of low-income patients for epilepsy treatment MRS 2000 CCEP website, www.thaiepilepsy.org fMRI for motor area for patient and public information as Intraoperative ECoG* well as medical consultation Phase III (2001–2003) – Surgery for high-yield remediable syndromes Short course in epileptology for Thai 2001 The ‘New Life’ social events performed physicians by seizure-free patients under Royal Textbook of Comprehensive attendance Epileptology (Thai) Mobile epilepsy training for rural doctors Neuropathology of epilepsy in the 4 main parts of Thailand in cooperation with Thailand Ministry of Public Health (MOPH) Seizure free patients worked as volunteers and CCEP staffs Clinical practice guideline (CPG) for 2002 Financial support for referred epilepsy epilepsy & epilepsy surgery (Thai) surgery to the program by Thailand First Surgery of hypothalamic MOPH hamartoma First Corpus callosotomy 2003 The ‘Nom Klao’ vocational rehabilitation CCEP-Bethel epilepsy management program under HRH’s patronage conference A Thai novel based on a story of a seizure Subtraction-coregistration SPECT to free surgical case by a renounced MRI (SISCOM) * author NPT, WPSI-Thai language version* Personnel training and development in invasive EEG and advanced epilepsy surgery in Germany and U.S.A. Phase IV (2004–) – Epilepsy Surgery using Advanced Techniques Stereotactic frameless guidance 2004 Government financial support for VNS Awake operation and intraoperative devices cortical stimulation First Functional hemispherectomy* First VNS implantation* First invasive EEG (SDE) monitoring and cortical stimulation mapping* First propofol Wada test* Multilobar resection Re-evaluation and re-operation for 2005 ‘Princess Epilepsy Congress 2005’ – relapse after surgery Scientific and Public Congress on Expanding video/EEG monitoring advanced epilepsy surgery on the facilities; using of digital video/EEG auspicious occasion of HRH’s 48th Epilepsy fellowship training,* approved Birthday Anniversary by The Royal College of Medicine, Issues on epilepsy and the law, literatures, Thailand and arts liberated to public and media First frameless DBS (for PD and The ‘New Life Project ‘under Thai movement disorders)† government’s support – providing 300 First multiple subpial transection epilepsy surgeries free of charges from (MST)* 2005 to 2008, to cerebrate HRH’s 48–50th Birthday Anniversary
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Table 19.1 cont’d The medical-technology arm 2006
First FDG-PET for epilepsy presurgical evaluation* First depth electrode implantation* Textbook of Comprehensive Epileptology vol. II (Thai) Genetic studies in Thai epileptic patients with AED allergy
The public arm and the Royal patronage 2006
CCEP, King Chulalongkorn Memorial Hospital, MOPH and National Health Security Office signed MOU on development of epilepsy clinics in main hospitals throughout Thailand using CCEP as a training model, establishing online epilepsy registration and referral system for epilepsy surgery Implementation of the issue ‘Epilepsy and the Law’ in Thailand
* First time developed in Thailand. † First time performed in Asia.
Only international standard presurgical and surgical techniques have been used at the CCEP. Experimental therapeutic procedures and those unproven efficacy by evidence-based reviews were not used during the program development. The optimization of medical treatment at the initial phase has reflected pictures of inappropriate medical treatment of epilepsy long being practiced among Thai general practitioners. Among the most common examples were inadequate adjustment of antiepileptic drug (AED) types and doses to reach the maximal effectiveness (40.9%), inappropriate choice of AEDs due to unclassified seizure types (17.4%), and early AED polytherapy (10.8%). Continuing use of failed drugs was found in a small proportion (2.4%) since sub-therapeutic dosing has been acquainted in most clinical practices.5 After phase I, the burden of truly medically intractable epilepsy was able to be determined. At phase II when needs have been clearly realized, standard presurgical diagnostic facilities have been successively developed. The introduction of surgery for high-yield remediable syndromes at phase III has eliminated fear and doubt of this new approach among Thai epileptics. The good surgical outcomes have gained dramatic acceptance and subsequent yearning for surgery from patients all over the country. The success of surgery has also brought public attention and continuing donation to the program. When discordant cases from basic evaluations have accumulated, advanced techniques have been developed at phase IV. Epilepsy surgery dealing with incongruent cases then began using relevant high cost, invasive diagnostic or intraoperative techniques. Many epilepsy presurgical and surgical techniques developed at CCEP have been considered for the first time ever in the medical history of Thailand.
The medical technology arm development A specialized epilepsy clinic was first established in September 1994. The clinic provided evidence-based medical treatment for epilepsy out-patients to achieve the best seizure control and to define medically intractable cases. Subsequently, standard presurgical evaluation facilities have been developed. A well-equipped two-bed epilepsy monitoring unit (EMU) comprised of 24-hour video EEG telemetry was first established in 1997 (Figure 19.4). Special electrode placement over true anterior temporal regions according to the international 10–10 system (T9T10, FT9FT10, F9F10)6 has been routinely used in adults since late 1997. Sphenoidal electrode placement was first performed in January 1999. The first epilepsy case management conference for surgical selection was conducted in June 1997 followed shortly by the first CCEP epilepsy surgery. Lesionectomy for right temporal ganglioglioma was performed on 16 June, 1997 by Professor Charas Suwanwela, rendering the patient seizure free for more than 9 years and AED totally discontinued for more than 7 years.
The structure CCEP, located at Bangkok Bank Building, King Chulalongkorn Memorial Hospital, Thai Red Cross Society is run as a charitable organization under the university hospital environment. CCEP comprises multidisciplinary medical staff of the Faculty of Medicine, Chulalongkorn University. CCEP has a structure of two arms developed in parallel, namely the medical technology arm and the community arm, with one heart, i.e. the program has been privileged to be under Royal patronage.
Figure 19.4 Epilepsy monitoring unit (EMU) equipped with long-term video/EEG telemetry was established in 1997. A 128channel digital video/EEG analogue for cortical stimulation mapping and the four-bed facility were completed in 2004.
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Figure 19.5 The first anterior temporal resection with amygdalo-hippocampectomy in a Thai MTLE patient (drawing by Professor Charas Suwanwela, the CCEP senior neurosurgeon, October 1999).
A 1.5 tesla high resolution MRI was first used for epilepsy in 1998.7 Epilepsy protocol (thin cut on temporal lobes with planes parallel and perpendicular to hippocampal long axis) has been used. Fluid attenuation inversion recovery (FLAIR) technique has been added to routine epilepsy protocol since January 1999. Three-dimensional and reformatted software was developed in 2000 for detection of subtle cortical dysplasia. Magnetic resonance spectroscopy (MRS) and functional MRI (fMRI) for hand motor function were also developed in 2000. Single photon emission tomography (SPECT) began in May 1998.8 99mTc-Ethyl Cysteinate Dimer (ECD) has been used for ictal and interictal injections. Ictal SPECT was limited only to official hours when ECD and scanner were available. A 3-head gamma camera scanner was first used in January 1999 which produced satisfactory high resolution images. Thai language Wada test was invented by Tayard Desudchit et al.9 Intracarotid amytal injection was, for the first time, performed to lateralize memory and speech functions in a Thai TLE patient in September 1999. All epilepsy presurgical evaluations were completed and the first temporal lobectomy on intractable epilepsy from hippocampal sclerosis (HS) was performed at CCEP on 14 October 1999 by Professor Charas Suwanwela (Figure 19.5) which rendered the patient seizure free for over 7 years. Surgical series that followed were the most prevalent and the most beneficial surgically remediable syndromes. These mainly included concordant temporal lobe epilepsy (TLE) with unilateral HS and localization related (focal) epilepsies from circumscribed tumors. Almost every candidate underwent the multidisciplinary presurgical evaluation and epilepsy conference. Mesial temporal lobe epilepsy (MTLE) is the most common adult epileptic syndrome operated, comprised of up to two-thirds of medically intractable cases, from which good surgical candidates can be found in 68% of cases.10 The yield of excellent surgical outcome (>90% seizure freedom) in early surgical series had gained wide public acceptance. Subsequently, patients came to CCEP for surgical evaluation by information from others rather than by public information or referral system. The success in surgery obviously improved post-operative quality of life and relieved psychosocial stigmas of seizure-free patients. Many have become helpful volunteers of the program or even CCEP staffs in the expanding epilepsy service. Unfortunately, in early 2000, such success was acknowledged among the patient themselves rather than among medical personnel. In 2001, a short course on epileptology was held by CCEP in Bangkok for education and training of general practitioners and physicians in related fields. The first book on
epileptology was published in Thai to distribute recent advances and CCEP experiences in intractable epilepsy management to medical professions. A mobile epilepsy training module on epilepsy for rural doctors was conducted in 2001 in four main regions of Thailand, with partial funding from the Thai Ministry of Public Health (MOPH). In 2002, the first Clinical Practice Guideline (CPG) in Epilepsy and Manual on Epilepsy Surgery were published for Thai medical personnel for awareness and early referral to an epilepsy surgical center. Surgeries were later performed in highly concordant TLE by using fewer resources as well as in less concordant cases. MRI and 24-hour video/EEG monitoring remains the minimal standard for presurgical evaluation of concordant right mesial TLE. The duration of hospital stay for monitoring was shortened significantly as skills in video/EEG recording and interpretation increased. Unnecessary SPECT and Wada tests were limited. The average scalp video/EEG monitoring period of 9 days in 1999 was reduced to 7.7 days in 2003 and 5.5 days in 2005. Personnel training as well as technology development for advanced surgery have been conducted according to the CCEP plan. The Cleveland Clinic Foundation (CCF) Cleveland, Ohio, the University of Washington Regional Epilepsy Center, Seattle, USA, and the Bethel Epilepsy Center (BEZ), Bielefeld, Germany have contributed greatly to CCEP in such objectives and have created strong collaboration between the centers until now. The Chulabhorn Foundation under Professor Doctor Her Royal Highness Princess Chulabhorn’s patronage has, for the first time, granted a qualified neurosurgeon (the first author) for 2-year epilepsy surgery fellowship training at CCF in 2001 to 2003. Invasive monitoring, cortical functional mapping as well as some aspects on neuropsychological tests, are among the transferred technology from BEZ to an adult epileptologist and two technicians from CCEP in late 2003. Since then, expansion of advanced techniques has taken place at CCEP, most of which is the first time in Thailand. The first transcallosal resection of hypothalamic hamartoma was successfully done in September 2002.11 Vagal nerve stimulation (VNS) was first implanted on 12 May, 2004 in a patient with Lennox–Gastaut syndrome. The first invasive EEG monitoring (IEM) and cortical stimulation mapping using subdural grid and strip electrodes was performed on 15 November, 2004, in a refractory TLE patient who had failed gamma knife radiosurgery at a private hospital, resulting in seizure freedom for more than 2 years.12 The worldwide shortage of sodium amytal in 2003 urged CCEP to study the use of propofol for the Wada test. The first intracarotid propofol procedure was performed on 22 October, 2004 with good results.13 Digital video/EEG
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Numbers and Types of Epilepsy Surgery at CCEP
120 100 2
9 8
1
9
12 7
23
80 60
10 4 2 24
40 1 20 0
4
1
3
2
2
3
3
9
57
55
2 23
43 Year
1999
2000
ATL for HS
2001
2002
Lesionectomy for tumors
2003
2004
Other surgeries
2005
2006
Invasive EEG
VNS
Figure 19.6 Numbers and types of epilepsy surgery at CCEP from 1999 to 15 December, 2006. The total numbers have reached 325 cases. The surgeries have been greatly increased since 2004, including cases receiving invasive EEG implantation.
telemetry, subtraction of ictal and interictal SPECT co-registered to MRI (SISCOM) and neuropsychological testing in Thai language are among other diagnostic facilities developed in parallel to the above advanced surgical techniques. First multiple subpial transection (MST) was performed on 26 December, 2005 in a case of left insular cortical dysplasia with diffuse ictal onsets over eloquent frontotemporal regions. 18 FDG-PET was first used as a part of presurgical evaluations in July 2006. First depth electrode implantation was done on 21 August 2006 in a discordant unilateral MTLE patient. Neurosurgical pathology also revealed many interesting epilepsy substrates from CCEP series. Many cases such as Rasmussen’s encephalitis and desmoplastic infantile ganglioglioma (DIG tumor) were first reported in Thailand.14 A case of low-grade hypothalamic neuronal tumor with gelastic/dacrystic seizure found at CCEP has never been reported in the world medical literature. The number of surgical cases has tripled in 2004 (Figure 19.6). Anterior temporal lobectomy for HS is the most performed operation until now. Surgery on difficult cases with poorly defined epileptogenic zones such as cortical dysplasia (CD), bitemporal disease, and non-lesional epilepsy have increased in 2005. Moreover, the time after video/EEG monitoring to surgery, as well as the duration of hospital stay after surgery, has been reduced significantly in the last 3 years.
The community arm Public activities have developed in parallel to medical technology. Serial public campaigns via media and magazines along with initial excellent surgical outcomes have dramatically converted initial fear and doubt in epilepsy surgery among the Thai population into the voluntary seeking of surgical therapy at the CCEP. The number of patients registered to the center has been increasing continuously to reach 3000 patients in 2006.
The ‘Light for Life Foundation for Epilepsy’ was founded in August 1999 as a charitable organization giving continuous financial support to low-income epilepsy patients. The foundation provides expenses for new AEDs, transportation, presurgical and surgical interventions including VNS supplies. Additional support was provided by the Thai MOPH with CCEP negotiation, i.e. funding for some anterior temporal lobectomy individuals from 2002 to 2004 and for VNS from 2004 to the present time. A study from CCEP has shown that epilepsy surgery has magnificent impacts on the patients’ QOL after surgery, when evaluated by occupational achievement and income acquisition.15 Of the 111 adult epileptic patients operated between January 2002 and December 2004, an overall seizure free rate of 83% was obtained. There were 62% reduction of the unemployment rate, 43% increase of the postoperative professional achievement, and 48% increase of the average annual income per capita, when compared to the preoperative period (p80 years) have
200 180 Annual incidence per 100,000
9781841845760-Ch26
160 140 120 100 80 60 40
Iceland Rochester
20 0 0
10
20
30
40 50 Age(years)
60
70
80
90
Figure 26.1 Incidence of epilepsy by age in Rochester, MN, US and Iceland. Data adapted from the original articles.26, 27
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Epidemiology of the intractable generalized epilepsies
209
incident rates considerably higher than those seen in infants.25–28
Relative frequency of catastrophic epilepsies
Age and type of epilepsy Part of the age-related pattern for the incidence of epilepsy is due to the occurrence of generalized seizures and epilepsies, many specific forms of which occur almost exclusively in infants, children, and young adolescents. This can be clearly seen in the Icelandic study where, for generalized seizures other than generalized tonic-clonic, the incidence is very high in infancy and drops precipitously in childhood, practically to disappear in adults.27 The CAROLE study from France provides some of the most stable estimates of the relative occurrence of syndromes throughout the age span.29 New onset generalized epilepsies of any kind account for little of epilepsy beginning in adults but are quite common in children and intermediate in adolescents and young adults.
The incidence figures provide a rough idea of how often some of the more common catastrophic epilepsies occur in the population. For understanding how common they are in the epilepsy clinic, other sources of information are more revealing. The CAROLE study as well as other community- and population-based studies provide the distribution of types of epilepsy at initial diagnosis (incident cases) as well as in crosssection (prevalent samples). While these are not always strictly speaking ‘population-based studies’ and therefore precise incidence estimates cannot be obtained from them, the studies are representative of patients seen in the populations from which they come and can be reasonably used to estimate relative frequencies of different forms of epilepsy. In children, the encephalopathic disorders as a whole represent between 10 and 21% of epilepsies 29,41–43 although the highest estimate was based on the most clinic-based (referral center) of the reports.43 Syndromes such as West, Lennox-Gastaut, and MAE account for the majority of the children who have catastrophic epilepsies. Individually, each may account for 1–5% of pediatric epilepsy cases. Estimates from the rare syndromes are harder to come by. In a US study, Dravet was found in 0.5% of children recruited at the initial diagnosis of epilepsy. 38 Another study from Israel reported that syndromes such as Ohtahara and Landau-Kleffner accounted for 0.2% each of pediatric epilepsy.44 Generally, such estimates are based on one or a few cases out of several hundred. In all, what is apparent is that those forms of generalized epilepsies most likely to be intractable occur relatively rarely in absolute terms and represent a relatively small proportion of all individuals with epilepsy in the population although they represent an important minority of children.
Incidence of the catastrophic epilepsies The Icelandic data provide incident rates by age and overall category of epilepsy.27 The category for cryptogenic and symptomatic generalized epilepsy (dominated by West and Lennox-Gastaut syndromes) has an overall incidence of 0.7/100,000 per year in the general population; however, all cases observed in that population occurred in infants, and among infants ( Rt, max Lt Anterior/ Lateral FrontalECoG: Sporadic Spikes near the cicatrix on orbital surface & rhythmic sharp and slow complexes on adjacent gyrus Automatisms - Scalp EEG: -B/L Frontal SD (throat discharge in grids: clutching, the Frontal discharge tearing lobe (uncertain across Lt clothing) w/ if Rt/Lt)-B/L OFC w/out occasional Frontal SDG clinical
Perceptual N/A (only illusion ‘slow aura motion reported) sensation’: slowing down of moving objects or of person’s speech; impression that walking person is suspended in air ‘indescribable weak feeling terrible feeling’; in Lt arm/ ‘things going leg → LOC away’
Aura
4:10 PM
14
N/A
Onset (yrs)
3/19/08
Case #2 (D.Tr.) 18M/-
Age/ Sex/Han dedness
A compendium of published cases of presumed orbitofrontal epilepsy (from 1951–2005)
Authors/ Year/ Center
Table 37.1
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291
30F/Rt
22M/-
11M/-
Schneider 1961 Ann Arbor, MI Neurology Case #1
Niedermeyer* 1971 Baltimore, MD
Tharp* 1972 Stanford, CA Epilepsia
6
20
No
No
(total of 4) i Rt/Lt Mesial Frontal ii. Rt/Lt OFC
IED
Imaging
Resection
surgeries: i) resection of area w/ max ECoG abnormality ii) Rt Frontal
Rt Frontal lobectomy
Nl skull X-rays, 2 Pneumoencephalo gram & B/L carotid arteriograms
N/A
change, then 2:40min later spread to Rt Hemisphere w/ Rt head/ eye turning & Rt arm jerk - eCS of Lt - Skull X-rays Complete Temporal lobe: Nl; - Carotid excision of no auras were arteriogram: firm 2.5cm elicited Rt shift of mass at the (Lt Frontal Lt ACA tip of Lt lobe not - Ventriculogram: Frontal pole stimulated; Rt shift of w/ firm pt became ventricular stalk uncooperative) system w/ projecting posterior from track displacement originating of Lt frontal in roof Lt horn c/w Lt orbit w/ frontal spaceosteomyelitis occupying of Lt orbital lesion inferior bone (*) to the lateral ventricles
IOZ
- Scalp: B/L highvoltage delta in prefrontal regions, also Lt Anterior & mid Temporal - Subcortical electrodes in i) Superior Temporal: few slow waves ii) Superior Frontal ‘Nl alpha’ iii) Anterior Midfrontal gyrus: slow waves at 2cm level; no waves at 4cm (mass on palpation) Oroalimentary - Scalp: Depth: lowest automatisms; Generalized, ADT in Rt occasionally irregular slow OFC tonic body SWC 1-2.5Hz, posturing or max Lt Frontal, ‘grand mal’ Lt Frontopolar & Anterior Temporal - Depth: Spikes Rt Orbito-Frontal, Rt Caudate Nucleus & B/L Amygdala; also Lt OFC during sleep Facial flushing, Scalp: Periodic, 2 surgeries: piloerection, asymmetrical i) I/Op ECoG: frightened B/L Sharp/Slow Multifocal look → wave complexes Spikes & Complex Rt>Lt (Fp2> Polyspikes motor w/ Fp1& F4>F3) over
Rt head/eye deviation & Rt arm jerks → amnesia, confusion
Ictal Semiology
Rt lateral OFC Clusters ≥ 50/day, for several months w/ long sz-free intervals
Nl cortex & Class 1 >2 yrs dural vein (varix) → reop: Firm ‘gliotic’ tissue in the Rt lateral
(*) Postop course complicated by extradural abscess requiring bone flap removal, abscess evacuation, debridement & delayed cranioplasty
Ηx of MVA 5 yrs prior a/w Lt eye injury requiring enucleation & Lt orbital prosthesis
for ‘peculiar behavior’
Location/ Comments
Hx of Rt FrontoParietal skull fracture at 20yrs s/p removal of extradural hematoma & debridement of Rt Frontal lobe
Class 1(f-up = 10 months)
Outcome
Encephalomal ‘much acia & improved’ sz multiple cystic frequency but cavities and developed calcifications marked within area of hyperdisorganized sexuality & gliotic post-op cortex
Encapsulated brain abscess w/ purulent exudate of coagulase (+) hemolytic Staph aureus
Histopathology
4:10 PM
Hallucinations: Auras only -Visual formed in Rt field: headless persons, circles, bars, colored butterflie Auditory: whistling like sound of wind Olfactory: odor of foul cigar smoke
Aura
3/19/08
30
Age/ Sex/Han Onset dedness (yrs)
cont’d
292
Authors/ Year/ Center
Table 37.1
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32M/Lt 9
#2. I/Op ECoG: Lateral Inferior TG w/ eCSinduced Automatism → Rt Temporal lobectomy
#1. Rt posterior OFC
N/A
#2. Class 4
#1. Class 4
Continued
Initial invasvive evaluation w/ bitemporal superficial & depth electrodes: no epileptiform activity even during clinical sz
At onset given diagnosis of ‘psychoneurotic hysteria’ and treated w/ ECT
Duration: few sec to min
4:10 PM
No ECoG discharges postresection
N/A ‘recently operated’
at surgery (no histological examination)
Resection of N/A posterior OFC & Gyrus rectus, Amygdala & Hipocampus, 3cm of Superior TG & 5cm of Middle, TG + Inferior TG
lobe resection anterior to precentral gyrus including mesial frontal & anterior cingukate
3/19/08
Case #2
Ludwig* 1975 38M/Lt 18 NINDS, MD Epilepsia Case #1
every 0.5– 6 sec resembling SSPE, enhanced by sleep
Anterolateral Rt Frontal lobe ii) I/Op Depth in orbital: Active spiking lateral OFC; also sharp-slow waves, but no seizures recorded Cephalic Sudden loss of -Scalp: 1. SWC or - Scalp: Pneumoencepha aura = responsiveness Sharp/Slow over 1. Obscured logram: mild ‘unusual’ w/ staring → Lt Anterior + or Nonlocalizable symmetric feeling Automatisms Middle 2. Rhythmical dilatation of (fumbling, Temporal 10Hz Sharp ventricular blinking, 2. Spikes Lt >> Rt Waves Lt system sitting up from Basal leads Frontal) recumbent) 3. Bisynchronous -Extradural flaps sometimes a/w Sharp/Slow (Temporal & Frontal pallor, lasting Frontopolar, & Depth for 30 sec → max Lt (Hippocampus + oriented & - Extradural flaps posterior OFC): fluent Depths: Spikes build- up of but amnestic independent & Spikes in posterior equal Posterior OFC → rhymical OFC & 15MH → 25–30Hz Hippocampus for 15sec exquisitely I/Op ECoG: localized to OFC Spikes in - eCS-induced posterior OFC Automatisms in Hippocampus; No AD or clinical changes in OFC Feeling ‘off Unresponsiveness - Scalp: - Scalp: 1. No EEG Pneumoencepha balance’, → kicking & 1. Intermittent Rt changes logram: slight ‘choking’ cursing (rarely Temporal theta concomitant w/ dilatation of or feeling hears voices or 2. Rare sharp spontaneous szs. lateral the room sees faces) transients Rt - PTZ-induced sz: ventricles ‘closing in’ lasting Rt; N1 B/L oriented & bisynchronous SWC carotid fluent but - Epidural electrodes arteriograms amnestic Rt Frontal, Temporal: Low-voltage fast 25Hz Rt Frontal - Flap, Needle & Cortical electrodes: rhythmic 20Hz trains exclusively Spike to posterior OFC flap
screaming. Able to follow simple commands, but amnestic of events
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Basal frontal lobe epilepsy 293
13M/Lt
Case #4
N/A
7
6
Unresponsi veness w/ facial pallor → Complex motor (foot stamping, kicking, running) ± Lt oculocephalic deviation, lasting induced w/ brief for speech Lt Anterior flattening → Temporal 2–3Hz SWC over Lt OFC w/ spread to Rt OFC - I/Op ECoG: Anterior parts of Lt Middle + Inferior TG & middle FG Visual Upward mouth - Scalp: B/L - Scalp: PTZPneumoencehallucination movement synchronous induced ‘diffuse Rtphalogram: or Perceptual (either side) w/ Sharp/Slow & sided activation’ moderate illusion ‘silly laugh’ SWC over - Rt-sided SD: dilatation of (feels as if → unresponsiFrontal + OFC, Superior + entire smiling/ veness w/ Lt Frontopolar, Inferior Frontal & ventricular unable to head turning & max Rt (F4/ Midparasagittal: system speak) Lt arm waving Fp2) - SD: No spontaneous purposelessly Mesial Rt OFC szs * eCS-induced → Complex rhythmical typical sz only w/ motor (moves 2Hz waves & Rt OFC stimuation* about, independent * PTZ-induced: undresses Sharp waves flattening → self ) Rare from Rt rhythmical 2.5–3Hz generalized superior SWC Rt OFC w/ motor szs Frontal spread to Lt OFC convexity → rhythmic SWC well localized over Rt Superior frontal (F4) ‘buzzing noise Staring → Complex ** Depth: Rt OFC ** & visceral motor (kicking, localization sensation’ thrashing, pelvic thrusting) w/ genital manipulation & alleged retention of awareness, lasting ~15sec
No
Aura
Histopathology
Rt Frontal lobectomy
Felt to have ‘at least two independent epileptogenic foci’
‘dense orbitofrontal gliosis’
No resection N/A (aborted because of Suspicion of skull infection)
extensive Lt N/A Temporal lobectomy: 7 cm along Middle + Inferior TG & 5.5cm along Superior TG & Hippocampus 2.5cm
Resection
Location/ Comments
Class 4 ** Sz-free × 1yr, then recurred w/ frequency of 8/yr
No resection History of purulent Rt ear infection at 6yrs
Class 3 ‘very few’ seizures ‘short follow-up’
Outcome
4:10 PM
-/-
26M/Lt
Case #3
Onset (yrs)
3/19/08
Williamson 1985 Yale, CT Ann Neurol
Age/ Sex/Han dedness
cont’d
294
Authors/ Year/ Center
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Munari 25M/Rt 6 1995 Grenoble, FL France Adv. Neurol.
Rare: Sensation of cold & Piloerection on Back & Thorax or feeling as if ‘my brain is being crushed’
Sudden loss of contact → Ambulation & Automatisms: Oral / Gestural (‘as if trying to catch things in the air’) / Verbal (incomprehensible utterances) → rotation of trunk Lt > Rt & eyes rolling to the Lt → rare GTC
Scalp EEG: Rt Large signal anterior onset; change on Rt evolution c/w Frontopolar & initial Frontobasal Frontobasal onset → very regions, w/out rapid spread to evidence of anterior & midprogression temporal regions - sEEG: Lowvoltage fast on Rt mesial & lateral OFC w/out clinical signs for first 35sec except for some bradycardia (from 77 to 63 beats /min); szs
CT: Nl
Gliosis & areas w/ Intracytoplasmic neuronal inclusions of PAS(+) granules c/w focal lipofuscinosis
- Inferior Frontal N/A region including Forntal pole - Temporal pole & uncus - Anterior & mid-Temporal neocortex (including first, second & third temporal gyri)
-Postresection ECoG: some Frontal discharges Superior & Posterior to the excision considered insignificant
Tailored resection of Rt OFC & adjacent portion of Rt Lateral Frontal
Rt OFC / clusters 5–10/d w/ sz-free intervals up to 1–2 weeks Initial sEEG w/ depths in Rt mesial Frontal, mesial Temporal & Anterior Cingulate (failed to identify area of ictal onset)
Basal frontal lobe epilepsy Continued
Class 1 * Hx of Rt Frontal (26 months) Frontal tumor s/p resection at age 7 (details N/A) followed by chemo- & radiotherapy;
Class 1>Positive FH of 6 yrs seizures -off AEDs Psychiatric for > 5 yrs comorbidity: -apparent - Depression resolution - Violent outbursts of premorbid psychiatric problems
Rt Orbital gyri, No abnormal- Class 1 gyrus rectus ities 18 months & subcallosal area
4:10 PM
&
Scalp EEG: Obscured by artifact (only one Aura w/ Rt Temporal rhythmic theta) SD strips (B/L Temporal; & Medial + Lateral Frontal): Rt Infraorbital rhythmic fast activity w/ attenuation in all contacts
- Scalp EEG: Sudden CT: Nl attenuation of (also N1 background Ventrifollowed by culography movement & Carotid artifact angiogram) - sEEG: Repetitive Spikes localized to Rt OFC only
- Scalp EEG: 1.Bisynchronous asymmetric IEDs anteriorly w/ shifting Rt or Lt preponderance; 2. IEDs widely distributed over Rt Frontotemporal - Sphenoidal: Bisynchronous Basal IEDs maximal Rt - Infraorbital: IEDs maximal infraorbitally strips: Spikes Rt Infraorbital - I/Op ECoG: Spikes in entire Rt OFC & Anterior portion of Inferomedial Temporal Scalp-EEG: Thetadelta activity & occasional Spikes over Rt Fronto-temporal region
- Scalp EEG: Sharp waves Rt Frontotemporal (F8-T4) - sEEG: Spikes localized to Rt OFC (w/ occasional propagation to contralateral Lt OFC)
3/19/08
or
8
Chang 1991 36M/Seattle, WA Epilepsia
- Staring w/ semipurposeful & thrashing movements; shouting incoherent words (occasional laughter) & amnesia for events - Occasional GTC out of sleep Sensation of - Cessation of whole body activity areas w/ numbness → Right body/ starting in the head turning → feet → flash Complex motor backs from behavior past/butterflies (struggling, in stomach kicking) & or feelings vocalizations of fear indicating fear, lasting ~30 sec w/ abrupt return of consciousness - GTC out of sleep
10 No
Rougier and 29M/Loiseau 1988 Bordeaux, France JNNP
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295
28F/Rt
Shihabuddin 2001 Vanderbilt, TN Seizure
19
34M/Rt 13
Case #3
unrelated
13
42F/Rt
Case #2
IED
IOZ
Imaging
Resection
Histopathology
Outcome
Spikes in Lt OFC + Lt posterior mesial Temporal
Rt mesial OFC Lesionectomy
-
Rt OFC
posterior OFC
-Uncus & lateral
Class 1 19 months
surgery 11 months post-op (gliosis w/ out cell loss), age 16 → sz-free × 6yrs age w/ recurrence of habitual szs
Single seizure type w/ respect to ictal semiology Mild word-finding difficulties postop Only 2 szs on day of
No significant post-op neuropsychologyical deficits
Location/ Comments
Pilocytic Class 3 Positive FH of szs astrocytoma - Cluster of in 1st degree habitual cousin Sz szs post-op frequency: day#1 - sz -CPS: 20/month free × 1yr- - 2∞ GTC:10/mo then 3 ‘atypical’ szs in
‘unremarkable’
- OFC: NI amygdala 2×3
become symptomatic after spread to inferior frontal, temporal pole, anterior & mid-temporal neocortex Staring w/ occasi- - Scalp/sphenoidal - Scalp/sphenoidal MRI: Nl Both the central Maloriented Class 1 onal manual EEG: Spikes Rt EEG: 2Hz δ at F4 hippocampal OFC (SD cells 17 months automatisms mesial (Sp2) & & T8 → bifrontal volumetry strip) + of glial & midtemporal (T8) & Rtmidtemporal δ lateral OFC neuronal - I/op ECoG: w/ Sharp waves at Sp2 (ECoG origin c/w Spikes localized - B/L SD: Central abnormality) focal MCD to lateral OFC & Lateral contacts w/ firm mass of portion of Rt OFC strip slightly w/spread discolored to Rt subtemporal tissue Staring w/ - Scalp/sphe- Scalp/sphenoidal MRI: Nl including - 4cm lateral - Hippocam- Class 3 unresponsivenoidal EEG: EEG: (i) Bi- frontohippocampal temporal pus: no 15 months ness & oral autoIndependent temporal 3/6 volumetry; neocortex evidence matisms mostly bitemporal (ii) Lt mesial PET:↓10% FDG -3cm of of sclerosis out of sleep Spikes Lt >> temporal -B/L SD & in Lt Temporal hippocampus & but missing Rt (20:1) Depth: parahippocampal portions - I/op including ECoG: (i) Focal Lt gyrus of CA3
Ictal Semiology
hippocampal 4/8 & (ii) Central contacts of Lt OFC strip w/ spread to Rt OFC ‘feeling of N/A (only aura None reported - Scalp/sphenoidal MRI: ATL defect déjà vu’ → reported) EEG: Rt Fronto4.5cm from sensation of Temporal tip w/ disorientation - Unilateral SD (Rt complete Fronto- temporal): resection of Medial contacts Mesial of OFC SD strip structures w/ spread to Dorsolateral Frontal feeling of Restless, - Scalp/sphenoidal - Scalp/sphenoidal - MRI: Lesion ‘butterflies hyperkinetic w/ EEG: Rt EEG: Regional, Rt 20 × 8mm2 in in the UE automatism Inferomesial Inferomesial Rt mesial OFC stomach’ a/w (Rt >Lt), drinking, Temporal Spikes Temporal (Nl hippocampi) fear dressing, & later (Sp2) & ‘atypical (rhythmic theta) - PET: ↓FDG in oroalimentary trains of Spikes & Rt Temporal automatisms polyspikes’ Polyspike- SDG: (both mesial + a/w LOA + ictal (Sp2) postictally(i) Clinical szs: lateral) speech → SDG: frequent Rt mesial Frontal - SPECT: ≠uptake
None reported
Bad taste or smell & awareness of accelerated heart rate
Aura
4:10 PM
15
Onset (yrs)
3/19/08
Roper and 17F/Rt Gilmore 1995 Gainesville, FL J Epilepsy Case #1
Age/ Sex/Han dedness
cont’d
296
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21F/Rt 9
Rheims 2005 Lyon, France Epil Disord
Image- guided Rt Substantial Inferior Frontal diffuse resection gliosis w/ astrocytosis (predominantly in the white matter w/ mild intracortical gliosis w/out dysgenesis) Metallic taste, Unresponsiveness - Scalp: Lt Frontal -Scalp: Nonlocalized MRI: Nl Complete Gliosis in the head tingle, or arrest of convexity tF3) - Depth: ‘nonlesional’ resection molecular ‘déjàvu’ activity → ‘Electrodecremental’ ictal + layer + vocalization Lt posterior OFC interictal focus white matter (shouting, w/out clinical as defined w/ mild & laughing) change for ~16sec by Depths = patchy gliosis until spread to B/L posterior in other Mesial Temporal 3.5cm OFC layers No Unresponsiveness - Scalp: ‘Diffuse -Scalp: Nonlocalized MRI- identifiable Complete Old posttraumor arrest discharges’ (No invasive lesion resection old atic hematoma activity → studies) (posttraumatic) posttraumatic cavity w/ oromanual cavity & surrounding automatisms surrounding sclerotic sclerotic tissue tissue Lt TemporoBehavioral - Scalp EEG: Lt -scalp EEG: lowMRI: circumscribed Lt Frontopolar Cortical parietal arrest → Lt & Frontal Spikes & voltage fast MCD Lt Fronto& OFC Dysplasia cephalgia downward slow waves Lt Frontal → polar suggesting (resection ‘typical of oculocephalic - sEEG: active B/L Frontal ‘minor form’ of sEEGthose seen deviation w/ Spike focus Lt SWC of TSC defined area) in TSC’ grimacing & Frontopolar - sEEG: (i) Localized Lt vocalization→ Frontopolar hypermotor onset w/ spread to Lt OFC (ii) Onset & predominant evolution in Lt OFC
No
Class 1 > 2 yrs
Class 1
Class 1
Class 4 Recurrence after 6 mos sz-free → ‘shorter & less disabling’ ‘Engel IIA’
Mother w/ TSC & epilepsy Patient w/out TSC stigmata
No identifiable risk factors
Abbreviations: AD = Afterdischarge; AEDs = Antiepileptic Drugs; Angio = Angiography; ATL = Anterior Temporal Lobectomy; a/w = associated with; B/L = Bilateral; c/w = consistent with; eCS = Electrical Cortical Stimulation; ECoG = Electrocorticography; ECT = Electroconvulsive therapy; EEG = Electroencephalography; F = Female; FG = Frontal Gyrus; FH = Family History; f-up = follow-up; GTC = Generalized Tonic-Clonic; Hx = History; IEDs = Interictal Epileptiform Discharges; I/Op = Intraoperative; IOZ = Ictal Onset Zone; Lt = Left; LOA = Loss of awareness; LOC = Loss of consciousness; M = Male; max = maximum; max = maximum; MCD = Malformation of Cortical Development; min = minutes: mo = month; MRI = Magnetic Resonance Imaging; MVA = Motor Vehicle Accident; N/A = Not available; Nl = Normal; post-op = postoperatively; Rt = Right; s/p = status post; sec = seconds; sEEG = stereo-encephalography; OFC = Orbitofrontal cortex; PAS(+) = Periodic Acid-Schiff positive; post-op = postoperatively; PTZ = Pentylenetetrazol; SD = Subdural; SDG = Subdural Grid; s/p = status post; SSPE = Subacute Sclerosing PanEncephalitis; SWC = Spike & Wave Complex; sz = seizure; TSC = Tuberous Sclerosis Complex; TG = Temporal Gyrus; UE = Upper Extremity; w/ = with; w/out = without; yrs = years; 2∞ = Secondarily; -/= not provided; δ = delta
N/A
-/-
Case #2
23
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N/A
36F/-
1mo & sz-free for another 6 months
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Rugg-Gunn FJ 2002 London, U.K. Lancet
Spikes Rt (inferior/anteri Rt Temporal mesial OFC; or aspect) (injection also Spikes Rt (ii) Subclinical 15sec after sz Lateral & Basal szs: Rt OFC onset) Temporal (mesial aspect) Sudden LOA a/w - Scalp: Rt F-T -Scalp: Regional Rt -Conventional truncal rocking slow waves Frontalhigh-resolution mvts, reperated -Intracranial: 4 MRI: Normal grabbing hand typical & 10 -DTI: Area of ≠ mvts & aimless subclinical szs w/ Diffusivity in wandering Rt OFC onset Rt OFC
GTC sz
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respect to seizures following epilepsy surgery.54 Careful review of these cases, with the above criteria in mind, reveals that in most instances localization of the epileptogenic zone within the OFR is either presumed or unconfirmed. Our inability to determine the extent of the epileptogenic zone and its relationship to the OFR, when surgical resection involves extra-orbital areas adjacent to the basal frontal lobe or when an extensive frontal lobectomy has been performed reflects a well-recognized inherent limitation of most human surgical studies.35 Seizure (clinical) semiology The most widely used system for classification of epilepsies was revised in 1989 by the Commission on Classification and Terminology of the International League Against Epilepsy (ILAE).55,56 The 1989 Proposal for the Classification of the Epilepsies and Epileptic syndromes describes a separate anatomically defined seizure pattern in regards to the orbitofrontal area: ‘The orbitofrontal seizure pattern is one of complex partial seizures with initial motor and gestural automatisms, olfactory hallucinations and illusions, and autonomic signs’.55 The commission prefaces the 1989 report with a cautionary note: ‘... inferences regarding anatomical localization must be drawn carefully’. Attempts to classify seizures according to location (anatomic lobes or sublobar regions) are confounded by the fact that seizures usually give rise to ictal manifestations by virtue of propagation to eloquent areas of cortex. Large cortical areas in the anterior neocortex such as the prefrontal cortex may be clinically silent, when activated by seizure discharges or electrical stimulation. Consequently, the first clinical evidence of a seizure may reflect propagation to areas remote from the region of seizure origin.57 Seizures arising from a distinct focus within the frontal lobe may rapidly involve multiple frontal lobe regions concealing specific seizure patterns.58 On the other hand, extensive, nondiscrete, or multifocal epileptogenic zones and rapid spread patterns within the ipsilateral or contralateral frontal lobe will lead to overlapping, coincidental clinical phenomena. As a result of these limitations, attempts to classify frontal lobe seizures on the basis of distinct anatomic subdivisions may be restrictive and potentially misleading.35,59 Moreover, only a handful of patients with unequivocal focal epilepsy arising from the orbitofrontal area have been reported in the literature, as is evident from the earlier discussion and the cases listed in Table 37.1. In their comprehensive review of ‘complex partial seizures of extratemporal lobe origin’ Swartz and Delgado-Escueta remarked that only eleven cases of ‘orbitofrontal complex partial seizures’ existed in the literature in a period spanning almost 20 years (from 1957–1975; all 11 cases are included in Table 37.1). And only nine of these were thought to carry ‘strong proof ’.60 Electrical stimulation studies Direct electrical stimulation of the cortex has been used to study the results of epileptic activation of various cortical sites.61 Stimulation studies with an effective stimulus intensity reveal that the majority of human cortex is symptomatically silent, and provide further evidence to suggest that cortical activation by epileptiform discharges will not produce symptoms, unless the electrical activity spreads to adjacent eloquent cortical sites.34
Stimulation of the OFR has been reported to produce a variety of responses. Smith and co-workers report that stimulation of the lateral and mesial posterior OFR (including the apparent ictal onset zone in a patient with pharmacoresistant focal epilepsy) did not produce any observable clinical phenomena. Such findings lend support to the hypothesis that clinical manifestations of basal frontal epilepsies may in fact begin outside the basal frontal area.51 The same group stimulated 13 posterior orbitofrontal sites using laterally placed depth electrodes in nine patients, who did not have evidence of focal epilepsy arising from the OFR. An assortment of sensations were elicited in this group including ‘body tingling’ on six occasions, and ‘a spacedout, confused feeling’ on four; ‘an unpleasant feeling’, an illdefined smell, an olfactory hallucination, a cephalic sensation, lightheadedness, and ‘fuzzy vision’ were reported on one occasion each.51 In their series of orbitofrontal stereo-EEG depth electrode investigations Munari and Bancaud report that an olfactory hallucination can be elicited in the presence or absence of ‘a localized afterdischarge’ following posterior orbitofrontal stimulation.36 Smith and co-workers postulate that such provoked olfactory symptoms may actually reflect activation of the adjacent lateral olfactory striae,51 which is possible, given that afterdischarges related to electrical stimulation often activate a more extensive cortical region beyond the cerebral tissue surrounding the directly stimulated electrode.61 Lastly, autonomic responses resulting from OFR stimulation in humans were reported in older studies;62,63 these include blood pressure elevation or bradycardia,64 respiratory arrest or increased amplitude of respiration, and increased esophageal contractions or decreased gastrointestinal motility. Ictal manifestations As discussed earlier, the large prefrontal cortical region can be viewed as a collection of heteromodal association areas, which share elaborate connections with other frontal and extrafrontal cortical and subcortical structures.65 Hence, seizures arising from several regions within the anterior part of the frontal lobe – including the orbitofrontal, frontopolar, anterior cingulate, and medial intermediate frontal regions – may display overlapping clinical characteristics as a result of the rapid and simultaneous activation of cortical sites within the PFC and its connections.58,66 In general, seizures arising from the frontal lobe may start and end abruptly with little if any postictal confusion, and tend to have a shorter duration (lasting less than 30 seconds) and higher frequency (oftentimes occurring in clusters) compared to seizures of temporal lobe origin.35 Ictal behavior is commonly characterized by prominent and often complex motor manifestations. Because of their bizarre appearance at times, frontal lobe seizures are not infrequently mistaken for nonepileptic, psychogenic events.67 The somewhat circuitous and dichotomous term ‘frontal lobe complex partial seizures’ has been proposed by some authors to describe these events.53,68,69 Stereotypic recurrence of the various clinical components in individual patients is key in establishing the correct diagnosis of seizures arising from the frontal lobe.53,67 Again, it is important to recognize that the observed seizure semiology reflects epileptic activation of the symptomatogenic zone.34 When seizures originate from silent areas of the brain there will be no outward manifestations without propagation of seizure activity to the symptomatogenic zone. Studies with
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Basal frontal lobe epilepsy depth electrodes have shown that ictal onset within the OFR may precede the onset of clinical manifestations by as much as 60 seconds suggesting asymptomatic activation of this area.37,51,70 Two separate groups of investigators have observed that patients may in fact remain completely asymptomatic, when the epileptic discharge stays localized within the OFR.37,47 Summarizing their experience of more than 150 patients, in whom the orbitofrontal region was investigated using stereoEEG, Munari and co-workers concluded that ‘the only clinical from characteristic of well-limited discharges in the orbital cortex was the absence of any objective clinical symptomatology’.71 Based on these observations, the limited number of welldocumented published cases, and the functional heterogeneity of the OFR, it is difficult to assume a unique seizure semiology that is characteristic for this part of the frontal lobe. A review of reported cases reveals some common themes: lack of aura or nonspecific auras, autonomic changes, behavioral arrest and/or impaired awareness, complex motor and ‘hypermotor’ activity, vocalization, oculocephalic deviation, olfactory or gustatory hallucinations, occasional secondary generalization.55,66,72 Occurrence in clusters, nocturnal preponderance, relatively brief duration and brief if any postictal confusion are also observed. Based on the cases reported by Ludwig41 (see Table 37.1) Bancaud and Talairach identified two ‘recognizable seizure patterns’ associated with seizures of orbitofrontal origin,73 as follows: (1) Olfactory auras, defined as seizures beginning with an olfactory hallucination or illusion. The olfactory symptoms may be accompanied by gustatory auras, autonomic changes, oroalimentary and/or gestural automatisms and ‘thymic alterations’. These associated symptoms have been attributed to propagation of ictal discharges to the adjacent opercular-insular-amygdalar region (autonomic manifestations, gustatory hallucinations or illusions, and oroalimentary activity) and/or to anterior cingulate region (complex gestural activity ‘automatic gesticulations’, and mood changes).36 Other studies have shown that olfactory auras usually point to seizures originating from the limbic mesial temporal structures, which are also involved in olfactory function.74,75 In fact, published reports suggest that olfactory auras constitute an uncommon manifestation of seizures arising from the basal frontal region.76 (2) Autonomic seizures, defined as seizures of prevalent ‘vegetative components’. They present with a variety of paroxysmal autonomic disorders including cardiovascular (heart rate changes, facial flushing, pallor), respiratory (apnea), digestive (sensation of hunger and/or thirst), urogenital (urge to urinate and periictal urination) and thermoregulatory disturbances (sensation of cold with piloerection and/or sensation of heat). Ictal ‘vegetative’ manifestations are thought to result from activation of the orbitofrontal and opercular insular regions.35,73 The so-called ‘hypermotor seizures’ constitute another ictal pattern commonly associated with this region. According to the Semiologic Seizure Classification hypermotor, seizures are defined as seizures manifesting with complex motor automatisms – organized motor activity, which primarily affects the proximal body segments and results in relatively large amplitude movements.77 The term ‘organized’ refers to movements
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that imitate natural movements as opposed to dystonic, tonic or clonic movements, but does not specify whether they are voluntary, involuntary or semipurposeful (e.g., evoked in response to environmental stimuli).78 When rapidly executed these movements may appear violent, for example thrashing, bicycling, vigorous kicking, frenetic striking or flailing of limbs and other rather peculiar motor behaviors.76 The repetitive character of these motions has been attributed to the central role of the prefrontal and premotor areas of the frontal lobe in the sequential design of movements.79 In a large series of suspected frontal or temporal lobe epilepsies Manford and co-workers identified 13 patients with a CT and/or MRI-demonstrable lesion (‘lesional focal epilepsy’) and hypermotor seizures, characterized by early ‘motor agitation’. The authors noted that the structural lesions involved the OFR in the majority of cases (7 out of 13). Lesions extended to the frontopolar cortex in Six of these Seven patients.80 The remaining Six cases with early motor agitation showed no consistent lesion localization (their lesions resided in various other frontal or temporal areas). Such observations may support the 1989 ILAE classification of anatomically defined seizure types of possible orbitofrontal origin. It should be noted however, that this was not a series of patients undergoing resective epilepsy surgery, and that the definition of the presumed epileptogenic focus was based on somewhat loose and often discordant clinical, EEG and MRI/CT localization criteria. In his review of structural lesions in the frontal lobe Goldensohn found ‘… too few cases with discrete lesions with sufficiently detailed seizure descriptions of possible orbitofrontal and cingulate origin to allow separate categorizations’.66 The author concluded that symptoms and signs commonly linked to orbitofrontal and/or cingulate epilepsy (such as autonomic or mood and affect changes, gestural automatisms, and versive movements preceding automatisms) do not appear to differentiate between lesion cases involving the orbitofrontal, anterior cingulate or other areas of the anterior third of the frontal lobe.66 Finally, it should be emphasized that epileptogenic foci within the OFR can give rise to seizures, which are electroclinically indistinguishable from temporal lobe seizures given the widespread connections between the limbic system and the OFR.39,47,50 In other words, basal frontal epilepsy may manifest itself with seizure spread outside the lobe of origin, as illustrated by Shihabuddin and colleagues in their case of a small right orbitofrontal pilocytic astrocytoma. Invasive recordings demonstrated seizure generation in the right OFR with spread to the ipsilateral mesial-basal temporal region – seizures were eliminated almost completely following right mesial orbitofrontal lesionectomy.50 Electroencephalography Surface EEG The ability of the scalp EEG to detect interictal activity depends on the extent of the irritative zone, the location and proximity of the generator in relation to the scalp and the orientation of the dipole.81 In general, interictal or ictal surface EEG studies are not very helpful in identifying epileptogenic foci residing in the basal frontal lobe because of the hidden, distant location of this part of the cortex with relation to scalp electrodes. Even long-term sleep-deprived interictal EEG
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recordings may be completely normal despite activation procedures. This apparent lack of interictal and/or ictal EEG abnormalities is a well-known weakness of electroencephalography.74 When detected on scalp EEG, interictal epileptiform discharges are helpful in establishing the diagnosis of epilepsy. Prolonged daytime EEG studies with recordings of 1–2 hours of sleep, as well as nocturnal sleep recordings increase the yield of interictal epileptiform abnormalities in individuals with epilepsy.82–84 Increased sampling using special electrodes (such as sphenoidal, anterior temporal or ear electrodes)85,86 and closely spaced additional scalp electrodes87–89 may be helpful in distinguishing temporal from frontal lobe foci. Home videotape recordings, when available, can provide valuable diagnostic information by capturing ictal manifestations. Prolonged inpatient video-EEG monitoring is indicated in patients with pharmacoresistant epilepsy as well as patients with paroxysmal events of unclear etiology. Careful video analysis of ictal semiology may lend support to the diagnosis of frontal lobe epilepsy, even in some cases where EEG is inconclusive. Polysomnographic recordings with additional EEG montages should be considered, in cases of predominantly nocturnal paroxysmal phenomena.90,91 Typically, abnormalities that are detectable on scalp EEG do not allow for topographic localization of foci residing in the basal frontal lobe. When present, spikes or sharp waves may have a regional distribution or appear generalized as a result of secondary bilateral synchrony.87 False localization to the anterior temporal region is not uncommon in patients with basal frontal epilepsies, who present with anterior temporal interictal epileptiform discharges (Figure 37.6) on their scalp EEG.57 Occasionally, propagated epileptiform activity can be present over central or frontolateral regions.76 Moreover, epileptiform
abnormalities may have a misleadingly widespread appearance, because of the large distance and intervening cortical area that separates the epileptogenic zone from the scalp EEG electrodes.81,92 Interictal sharp waves may be reflected over a wide bifrontal region as a result of volume conduction (Figure 37.7) such bilateral discharges may sometimes exhibit a shifting right or left preponderance or a misleading contralateral maximum.35 The inaccessibility of the basal frontal surface and other areas of the frontal lobe to scalp electrodes, the widespread connectivity of the OFR, the variable size and location of epileptogenic foci within this region and the potential for bilateral epileptogenicity as a result of bifrontal injuries are among the factors accounting for the lack of adequate topographic scalp EEG localization in basal frontal lobe epilepsies.33 Large and somewhat blunted sharp waves were demonstrated by Tharp in his patients with presumed orbitofrontal epilepsy.52 Case reports by Ludwig and co-workers highlighted the occurrence of bilaterally synchronous, paroxysmal epileptiform discharges, with a bifrontal or frontopolar maximum, as well as discharges involving one anterior quadrant, with or without evidence of additional temporal lobe involvement.41 In the single patient described by Chang and colleagues sphenoidal recordings exhibited a consistent preponderance on the side of the epileptogenic OFR. In this well-documented case report the addition of sphenoidal and infraorbital scalp electrodes revealed that the observed bisynchronous discharges had a more basal distribution with a maximum in the infraorbital regions.39 The close anatomical connections between the mesial temporal and orbitofrontal regions have already been discussed. In their classic (1958) paper, Kendrick and Gibbs used the technique of strychnine neuronography in the course of temporal
Spike, Maximum Sp1 Fp1–F7 50 uv
F7–SP1 SP1–T7 T7–P7 P7–O1 Fp2–F8 F8–SP2 SP2–T8 T8–P8 P8–O2 SP1–SP2 TP9–TP10 Fp1–F3 F3–C3 C3–P3 P3–O1 FP2–F4 F4–C4 C4–P4 P4–O2 EKG1–EKG2 2000 uV
Figure 37.6 Interictal scalp EEG tracing. Predominant spike focus in the left anterior temporal region, maximum in the left sphenoidal electrode (Sp1), as seen on this longitudinal bipolar montage (the temporal chains have been extended to include the left and right sphenoidal electrodes).
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Spike, Generalized Fp1–F7 50 uV
F7–T7 T7–P7 P7–O1 Fp2–F8 F8–T8 T8–P8 P8–O2 Fp1–F3 F3–C3 C3–P3 P3–O1 Fp2–F4 F4–C4 C4–P4 P4–O2 F7–Cz Cz–Pz EKG1–EKG2 2000 uV
Figure 37.7 Interictal scalp EEG tracing. Less frequently, generalized epileptiform discharges (with a shifting bifrontal maximum; higher on the right side in this instance) were seen during prolonged video-EEG recordings, as illustrated on this routine longitudinal bipolar montage.
lobectomies to demonstrate the bidirectional interrelationship between these two regions in humans.93 Local application of strychnine through needle electrodes produced ‘artificial’ spike foci in the frontal and temporal lobes of 34 patients. The authors observed that strychnine-induced spikes in the mesial temporal region commonly spread to the mesial orbital surface of the ipsilateral frontal lobe as well as to the tip of the ipsilateral temporal lobe. On the other hand, strychnine injected into the mesial OFR resulted in spike discharges that propagated first to the ipsilateral mesial temporal cortex, and later to the contralateral mesial OFR and to a lesser extent to the frontal poles. The authors concluded that discharges may spread in either direction – depending upon whether strychnine is first applied in the mesial temporal or orbitofrontal area – and implicated the ‘pathway afforded by the uncinate fasciculus’ to explain the observed spread patterns. Ictal scalp EEG recordings (Figure 37.8) during seizures of frontal lobe origin, as a whole, may provide poorly localizing94,95 or misleading information.96 Seizure duration is usually short and muscle artifact often obscures ictal EEG activity. Furthermore, observed patterns and frequency of activity at the time of electroencephalographic seizure onset do not correlate with the cortical area generating seizures.97 When ictal EEG is inconclusive or normal, diagnosis will rely on the history and ictal semiology. In cases where the clinical pattern does not provide additional clues with respect to lateralization to one hemisphere, detailed analysis of clinical seizure onset may be helpful in disclosing a clearly defined focal symptomatology.98 The localizing value of ictal scalp EEG is generally inferior in extra-temporal epilepsies.33,99 Using lateralized rhythmic discharges, postictal slowing and EEG activity at seizure onset
only 47–65% of extratemporal seizures are correctly lateralized, as opposed to 76–83% of temporal lobe seizures.99 Surface ictal EEG recordings were retrospectively analyzed in a recent series of 46 patients with neocortical focal epilepsy, who became seizure free after surgical resection of a single lobe (lateral frontal=15, mesial frontal=8, neocortical temporal=10, parietal=7 and occipital = 6). In this series, virtually all seizures that were either obscured by artifact or had no identifiable EEG change had a frontal lobe origin.33 Localized EEG patterns were more common with seizures arising from the dorsolateral frontal region. Intracranial EEG Patients with suspected pharmacoresistant focal epilepsy should be referred to a comprehensive epilepsy center for a thorough presurgical evaluation, which includes prolonged video-EEG recordings, high-resolution structural and functional imaging and neuropsychological assessment. When results of presurgical studies are inconclusive or incongruent and epilepsy surgery is being considered, invasive EEG recordings with subdural grid and/or depth electrodes may be necessary to delineate the epileptic focus. Invasive approaches to verify the location of the epileptogenic focus include: intraoperative electrocorticography, extraoperative invasive electrode recordings (using extradural, subdural and/or intracerebral electrodes), and stereo-electroencephalography.60 It is important to emphasize that invasive electrodes record from limited parts of the cortex only, and do not provide the global picture of brain activity afforded by scalp electrodes.100,101 Hence, intracranial electrode monitoring should only be utilized, once a reasonable hypothesis
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Textbook of epilepsy surgery EEG_ONSET Rhythmic change in Lt hemisphere
Fp1–F7 20 uV
F7–SP1 SP1–T7 T7–P7 P7–O1 Fp2–F8 F8–SP2 SP2–T8 T8–P8 P8–O2 SP1–SP2 TP9–TP10 FP1–F3 F3–C3 C3–P3 P3–O1 Fp2–F4 F4–C4 C4–P4 P4–O2 EKG1–EKG2 1000 uV
Fp1–F7
> HR increases to 84bpm
>
> > 20s + EEG onset
50 uV
F7–SP1 SP1–T7 T7–P7 P7–O1 Fp2–F8 F8–SP2 SP2–T8 T8–P8 P8–O2 SP1–SP2 TP9–TP10 Fp1–F3 F3–C3 C3–P3 P3–O1 Fp2–F4 F4–C4 C4–P4 P4–O2 EKG–EKG2 1000 uV
Figure 37.8 Ictal scalp EEG tracings on a routine longitudinal bipolar montage during a typical nocturnal seizure: (a) The electrographic onset (EEG onset) is punctuated by the appearance during sleep of an initial low voltage semi-rhythmic activity, which gradually evolves into more rhythmic and sharply contoured delta slowing over the left hemisphere; (b) 20 seconds later repetitive spikes within the ill-defined slowing.
about the possible location(s) of the epileptogenic zone has been made based on the results of a detailed presurgical evaluation.102 When epileptogenicity involving the basal frontal lobe is suspected, electrode coverage of both the frontal and the temporal lobe may be necessary, to better localize the epileptogenic zone and differentiate between frontal and temporal involvement (Figures 37.9 and 37.10). Furthermore, use of bilateral frontal electrodes may be contemplated as a means
of improving the investigators’ ability to study lateralization and mode of propagation of ictal discharges.103 Stereotactically placed depth electrodes are useful in accurately targeting/evaluating deep structures, but sample only a restricted area. On the other hand, subdural electrodes provide better spatial resolution and can sample a larger expanse of cortex as they record directly from the cortical surface that underlies the pia matter. However, only about one-third of the
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Basal frontal lobe epilepsy CLIN_ONSET Elevate Rt arm
Fp1–F7
> > Rhythmic theta max sp1 40s + onset
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SEIZURE seizure button
100 uV
F7–SP1 SP1–T7 T7–P7 P7–O1 Fp2–F8 F8–SP2 SP2–T8 T8–P8 P8–O2 SP1–SP2 TP9–TP10 Fp1–F3 F3–C3 C3–P3 P3–O1 Fp2–F4 F4–C4 C4–P4 P4–O2 EKG–EKG2 1000 uV
Fp1–F7
> Head turn to Rt
> > Vocalize, extend Rt arm forward Eyes to Lt",
Sign of four,
quickly
followed by
200 uV
F7–SP1 SP1–T7 T7–P7 P7–O1 Fp2–F8 F8–SP2 SP2–T8 T8–P8 P8–O2 SP1–SP2 TP9–TP10 FP1–F3 F3–C3 C3–P3 P3–O1 Fp2–F4 F4–C4 C4–P4 P4–O2 EKG1–EKG2 1000 uV
Figure 37.8, (c) low-amplitude repetitive spiking (~5–7Hz) seen over the left temporal region at the time of clinical onset, which occurs approximately 40 seconds following EEG onset. (d) muscle artifact obscuring EEG activity at the beginning of secondary generalization, which occurs approximately 50 seconds following EEG onset.
cortex is exposed, and generators located within the depth of a sulcus cannot be sampled adequately unless they extend to the cortical surface or crown.104 Subdural grid or strip electrode arrays are inserted under general anesthesia following craniotomy and incision of the dura. Such arrays are usually slid under the edges of the exposed dura, in contact with the brain surface, without direct visualization for the purposes of recording from the orbitofrontal and adjacent inferior temporal areas.105 The current approach at both the Cleveland Clinic Epilepsy Center and at the Texas Comprehensive Epilepsy Program is to sample the basal frontal region using a 4 × 4 subdural electrode array (Figure 37.9); made of four rows and four columns of platinum-iridium disk electrodes, each of
which has a 4mm diameter and is separated from neighboring electrodes by a center-to-center distance of 1cm.106 As described above, the OFR has widespread connections with the anterior and mesial temporal regions, the insula, opercular areas and cingulate gyrus. Adequate sampling of these areas is recommended during invasive recordings in patients with suspected basal frontal epilepsies.107,108 Good communication between the neurosurgeon and the epileptologist/neurophysiologist involved in the clinical management and interpretation of presurgical studies is essential during the planning stage. In addition, functional mapping by means of electrical cortical stimulation may be necessary to identify eloquent cortex such as language areas and motor cortex.
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Brain Map-Left
A
DSF
B
DIF D
E
E
F
C
Figure 37.9 Invasive EEG evaluation using a combination of multiple subdural electrodes covering the left frontal and temporal lobes along with two intracerebral depth electrodes targeting the area of encephalomalacia. Subdural electrode arrays: A = 8×8 plate, covering the left perirolandic region; B = 4×6 plate, covering the left dorsolateral frontal region, anterior to the A plate; C = 4 ×4 plate, covering the orbitofrontal area; D = 2×6 plate, covering the lateral aspect of the temporal lobe; E and F = 1×6 strips, covering the anterior and mid subtemporal regions. Intracerebral depth electrodes targeting the encephalomalacic area: DSF with entry point in the superior frontal gyrus, and DIF with entry point in the inferior frontal gyrus, as seen in this schematic representation.
Roper and Gilmore used a single subdural strip electrode to sample the orbitofrontal cortex in all cases of limbic epilepsy referred for invasive monitoring during a period of 1 year.46 A total of 15 patients underwent invasive evaluations during this period (unilateral investigations with temporal, frontal, and orbitofrontal subdural electrodes were performed in eight and bilateral studies using bitemporal depth electrodes along with bilateral inferolateral temporal and orbitofrontal subdural electrodes were performed in seven patients). Three patients out of the 15 patients with intractable limbic seizures were found to have seizures originating from within the OFR (see Table 37.1). Subdural strip electrodes identified the OFR as the site of seizure origin (ictal onset zone), but were insufficient to define the actual boundaries of the epileptogenic zone. To better delineate the boundaries of the epileptogenic area the authors supplemented their investigations with the use of intraoperative electrocorticography (ECoG). These investigations and subsequent surgical excisions led the authors to conclude that unilateral OFR resections can be beneficial in a subset of patients with orbitofrontal epilepsy and can be performed without significant neuropsychologic impairment. Stereo-electro-encephalography (stereo-EEG, sEEG) refers to the methodology of stereotactically-guided depth electrode recordings, which was originally developed by Bancaud and Talairach in France. Ictal anatomo-electro-clinical correlations based on sEEG recordings are utilized in identifying the cortical area(s) primarily involved in the generation of spontaneous ictal discharges, and provide a guide to tailored cortical resection.109 For the school of stereo-EEG investigations individualized planning of electrode implantation
is critical. The surgical team is assigned with the task of finding the best compromise between the ‘ideal’ position of the electrode and the constraints introduced by the various vascular segments, which the electrode may encounter along the length of its trajectory from the surface to the deeper brain targets.103,110 In their review of the electroclinical features of orbitofrontal seizures Munari and Bancaud summarized their experience in a series of 60 patients, who underwent stereo-EEG investigations with at least one orbitofrontal depth electrode. The majority of these stereotactically implanted multilead electrodes (total of 10 contacts, each 2mm in size and 1.5mm apart) were inserted via an orthogonal, lateral approach and aimed to explore both the medial and lateral aspects of the OFR.36 An oblique approach was used in a few cases and a vertical approach was utilized in a single patient. Spread between OFR and temporal lobe may occur extremely rapidly via the uncinate fasciculus as documented by stereo-EEG investigations of spontaneous seizures arising from the basal frontal lobe.36 Other investigators have observed that ‘orbitofrontal seizures’ propagate more slowly compared to seizures arising from other extratemporal locations.101 This observation comes out of a fairly small study of 10 patients with extratemporal neocortical epilepsy. A total of 25 seizures were studied with intracranial recordings using a combination of subdural strips, subdural grids, and depth electrodes implanted ‘as clinically indicated’. Two patients in this group were thought to have seizures arising from the OFR and both underwent bilateral intracranial EEG investigations. A total of eight ‘orbitofrontal seizures’ were studied, although details on individual seizures were not provided. The authors defined the ipsilateral and contralateral propagation time as the time elapsed from electrographic seizure onset to first spread either to an adjacent ipsilateral lobe or to the contralateral hemisphere. For ‘orbitofrontal seizures’ spread to the ipsilateral temporal lobe occurred within a period ranging from 12.5 to 85 seconds, and to the contralateral frontal lobe within a period ranging from 9.8 to 92 seconds (compared to a more rapid ipsilateral or contralateral spread, as early as within 0 to 0.4 seconds, in some seizures arising from other frontal or parieto-occipital locations).101 The small patient number and the potential spatial sampling limitations of invasive recordings need to be taken into account, when interpreting these results. Structural and functional imaging Structural imaging High resolution anatomical MRI should be performed to search for focal intracerebral lesions, and ideally interpreted by expert radiologists, experienced in imaging of the epilepsies.111 Identification of a structural abnormality by MRI adds substantially to the process of localizing the site of seizure onset and selecting favorable candidates for resective epilepsy surgery.112 Structural abnormalities may be found in up to 80% of patients with refractory focal epilepsy using optimal anatomical MRI imaging.113 Structural MRI can provide reliable information about the pathology of the suspected epileptogenic lesion. Common MRI-identifiable pathologies include disorders of cortical development and foreign-tissue lesions (such as
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EEG_ONSET SC1–Ref
500 uV
SC2–Ref SC3–Ref SC4–Ref SC5–Ref SC6–Ref SC7–Ref SC8–Ref SC9–Ref SC10–Ref SC11–Ref SC12–Ref SC13–Ref SC14–Ref SC15–Ref SC16–Ref SD1–Ref SD2–Ref SD3–Ref SD4–Ref SD5–Ref SD6–Ref SD7–Ref SD8–Ref SD10–Ref SD11–Ref SD12–Ref
EEG onset + 10 sec. SC1–Ref 500 uV
SC2–Ref SC3–Ref SC4–Ref SC5–Ref SC6–Ref SC7–Ref SC8–Ref SC9–Ref SC10–Ref SC11–Ref SC12–Ref SC13–Ref SC14–Ref SC15–Ref SC16–Ref SD1–Ref SD2–Ref SD3–Ref SD4–Ref SD5–Ref SD6–Ref SD7–Ref SD8–Ref SD10–Ref SD11–Ref SD12–Ref
Figure 37.10 Ictal invasive EEG recordings on a referential montage displaying the electrode contacts on the C (orbitofrontal) and D (lateral temporal) plates: The electrographic onset is punctuated by the appearance of focal repetitive spiking involving the mesial, posterior corner of the orbitofrontal plate (electrodes C1 followed by electrodes C2 and C5). This activity remains confined to the orbitofrontal area without evidence of concurrent involvement of other electrodes for several (~25) seconds.
tumors and vascular malformations). Furthermore, findings on MRI help tailor the surgical procedure and assess the extent of resection postoperatively.112 A particular challenge for T2 weighted MRI sequences investigating the human OFR using is the potential for susceptibility artifacts resulting in signal dropout or geometric distortion as a result of the close proximity of the OFR to the air-filled sinuses.7 When MRI is negative but EEG or other testing points to a potential area of focal epileptogenicity, dedicated MRI
sequences114 with thin cuts through the region(s) of interest should be obtained. Imaging with higher magnetic fields or three-dimensional MRI techniques may further increase the yield and allow for presurgical identification of epileptogenic lesions.115 As illustrated in the case reported by Rugg-Gunn and colleagues48 the use of diffusion tensor imaging and advanced postacquisition processing analyses can enhance the detection rate of subtle abnormalities in patients with so-called ‘nonlesional’ focal epilepsies.116,117
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Functional imaging Functional imaging with interictal PET and/or ictal SPECT studies may be employed as a means of identifying seizure foci in the basal frontal lobe and guiding surgical resection. Interictal studies of brain metabolism using 18FDG-PET (fluoro-deoxyglucose positron emission tomography) may disclose areas of hypometabolism in up to 60% of patients with frontal lobe epilepsy. However, almost 90% of these patients will have an underlying MRI-identifiable structural abnormality.118 In neocortical epilepsy it is often difficult to interpret small or subtle focal areas of hypometabolism of questionable clinical relevance in the absence of a structural lesion.119 Consequently, 18FDG-PET studies may be of limited value in nonlesional frontal lobe epilepsies. Single photon emission computed tomography (SPECT) has been used in patients with focal epilepsy to assess alterations of cerebral perfusion that may reflect the approximate location of the epileptic focus. Ictal SPECT is the only available, noninvasive modality practically suited for functional brain imaging during an actual seizure.119 Digital subtraction techniques allow for comparison of an individual patient’s interictal (baseline) and ictal SPECT images. The relatively low-resolution subtraction images afforded by SPECT can then be coregistered to the patient’s anatomical MRI for more precise localization.119 This computer-aided process was found to be diagnostically superior, when compared to routine side-by-side visual inspection of ictal and interictal SPECT scans.120 Recent studies suggest that subtraction SPECT images are useful in guiding the location and extent of surgical resection in patients with extratemporal epilepsy.121 There have been no specific reports related to subtraction/ictal SPECT imaging in patients with seizures arising from the basal frontal lobe. Because of their sometimes brief duration and propensity of frontal lobe seizures for rapid secondary generalization it may particularly difficult to obtain and interpret ictal SPECT studies. In contrast to the aforementioned nuclear imaging techniques, magnetoencephalography (MEG) is a neurophysiological method with high temporal and spatial resolution. Results of MEG source localization can be co-registered to structural MRI data and produce the so-called magnetic source imaging (MSI), which is currently explored as a means of improving noninvasive localization of epileptogenic foci. The conjugation of noninvasive neurophysiology and anatomical neuroimaging using MEG/EEG along with MRI can provide important insights into the generation and spatiotemporal evolution of neocortical discharges. However, the results obtained require careful clinical analysis, integration and comparison with available preoperative testing and further validation.122 MSI123 along with ictal SPECT studies124 may play an increasingly important role in directing placement of electrodes in patients with suspected frontal lobe epilepsy, being considered for resective surgery.125 At this time, however, the role of MSI in the presurgical evaluation of patients with suspected basal frontal lobe epilepsies remains unclear. Etiologies of basal frontal lobe epilepsy Out of the 23 cases assembled in Table 37.1, a brain abscess was identified in two patients, and a tumor in another two (one had a pilocytic astrocytoma; the tumor type was unknown in the second case). Two more patients were found
to have cortical dysplasia, while four patients were suspected to have a posttraumatic etiology. Histo-pathological examination showed nonspecific ‘gliosis’ in five patients and no abnormalities in three. Details on histopathology of resected tissue were not provided/not known in the remaining five cases. The OFR is a common site for closed-head injury. Nonpenetrating head traumas may produce forces that move the basal frontal brain parenchyma across the underlying uneven surface of the orbital roof.126 Falls or blows on the front of the head produce direct frontal lobe damage, while trauma to the occipital region produce basal frontal and fronto-polar injury by a contre-coup mechanism. Hence, posttraumatic epilepsy following closed head injury often involves the frontal and/or temporal lobes. The diffuse nature of nonpenetrating head injuries often limits localization of the epileptogenic focus, especially in patients without distinct, MRI-identifiable focal lesions.127 It should also be noted that extensive cortical abrasions and/or lacerations in the orbitofrontal region may not be easily detected by CT and/or MRI because of the relatively limited three-dimensional volume of these lesions and the artifacts introduced by the surrounding bony irregularities of the cribriform plate.128 The prognosis and risk of later epilepsy depends on the severity of the trauma and concomitant cerebral complications.129,130 Post-traumatic epilepsy refers to the recurrent, unprovoked seizures developing more than one week after penetrating or closed head injury.131 Nearly 40% of seizures appear within the first 6 months, and 70–80% by the first 2 years after the injury.132 The risk of posttraumatic epilepsy falls rapidly as the post-injury seizure-free interval increases, but does persist for more than 15 years after the injury, especially in cases of moderate to severe trauma.130 The olfactory nerves are located immediately below the OFR and are similarly susceptible to injury following closed head trauma. Post-traumatic anosmia usually results from shearing of the olfactory nerve fascicles as they traverse the cribriform plate to enter the olfactory bulb.133 Because of this shared mechanism of injury posttraumatic anosmia may serve as an important clinical sign of concomitant orbitofrontal damage. Significant hypoperfusion in the OFR has been demonstrated with the use of HMPAO-SPECT in a series of 18 patients, who had been rendered completely anosmic as a result of a remote head injury.134 In a similar study of 11 anosmic patients with a history of prior head injury quantitative PET studies showed evidence of hypometabolism in the OFR as well as in the medial temporal region compared with controls.135 In a similar series of 20 head-injury patients the finding of marked post-traumatic anosmia was taken as a strong indication of damage to the OFR.128 Most of these patients appeared intact on psychometric neuropsychological testing and were generally preserved in areas such as intelligence, memory and language. Nevertheless, they faced major psychosocial difficulties; most of them were unemployed and showed evidence of poor empathy, poor judgment and absent-mindedness. It is not uncommon for patients with OFR injuries to perform normally on a variety of standard neuropsychological tests.128,136 More specialized testing is required to expose deficits related to decision making and executive planning. The authors concluded that posttraumatic anosmia has a close and specific relationship with a particular locus of injury (OFR) and a
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Basal frontal lobe epilepsy specific set of neurobehavioral symptoms that constitute the so-called ‘orbitofrontal syndrome’. Another common insult with predominant temporal and/or orbitofrontal localization that deserves mentioning in this section is herpes simplex encephalitis. Herpes simplex virus (HSV) is the cause of the most common sporadic viral encephalitis in adults and children older than 6 months.137 Encephalitis due to HSV infection (both primary and recurrent infection) is a serious disease with an untreated mortality approaching 70% and substantial morbidity despite antiviral therapy.138 Pathological studies of HSV encephalitis have shown predominant viral-related damage in limbic structures as well as neighboring areas including the mesial temporal lobe (hippocampal formation, amygdala, parahippocampal gyrus, and perirhinal cortex), orbitofrontal region, insula and cingulate gyrus.139 The selective and often remarkably segregated involvement of temporal and orbitofrontal locations may in part reflect the route of entry of the virus into the host. In primary infection HSV may gain access to the brain via an olfactory route reaching the olfactory bulbs through the cribriform and subsequently spreading along the base of the frontal lobe. In reactivation of latent HSV infection the virus may spread from the trigeminal ganglion along meningeal branches of the trigeminal nerve.137,140 The long-term sequelae of rigorously confirmed HSV encephalitis in the era of antiviral therapy (with acyclovir) were investigated in a retrospective study from New Zealand, in which a total of 42 acyclovir-treated patients were followed for a period of up to 11 years.141 The mortality rate was 12% at 1 month and 14% at 6 months. All but one of the surviving patients had persistent neurological impairment. The most common and most disabling complication was that of memory dysfunction (especially short-term memory). Personality and behavioral disorders occurred in almost half of the long-term survivors, albeit less severe compared to reported disability before the introduction of acyclovir. Epilepsy was present in 24% of surviving patients. Of note, two-thirds of survivors were found to have unilateral or bilateral anosmia, although may of these patients were unaware of the deficit.141 Other common substrates of extratemporal focal epilepsy include tumors, vascular anomalies and developmental disorders. The importance of MRI-identifiable lesions involving the deeply situated orbitofrontal region should not be underestimated. Studies of anatomically defined lesions in various locations of the brain cortex indicate that these lesions will more often than not harbor the site of the epileptogenic focus.142 In this case complete excision of the lesion along with the surrounding ‘epileptogenic tissue’ provides an excellent chance for a seizure-free outcome.38,66 Studies have shown that one of the best prognostic factors in epilepsy surgery is in fact the completeness of such lesionectomies.143 Poor surgical results are more common in cases, where postoperative MRI provides evidence of incomplete resection of the lesional pathology.144 With improvements in neuroimaging, cortical dysplasias and other developmental disorders are increasingly recognized as causes of pharmacoresistant focal epilepsy. It is estimated that nearly 30% of surgical specimens from patients with neocortical epilepsy contain some type of malformation of cortical development.145 In fact, dysplastic lesions (ranging
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from heterotopias to subtle cytoarchitectural abnormalities) are the most common histopathological finding in some surgical series of frontal lobe epilepsies.38 Among the various vascular anomalies, cavernous angiomas (cavernous malformations, CM) and arteriovenous malformations (AVM), are more likely to cause seizures. The epileptogenicity of these lesions is believed to result from pathological changes imparted on tissue surrounding the vascular malformation due to ongoing microhemorrhage and hemosiderin deposition.146 Therefore, surgical excision should not only target the lesion but extend to the adjacent hemosiderin-stained tissue.147 Frequently encountered tumoral pathologies associated with pharmacoresistant epilepsy include gangliogliomas, dysembryoplastic neuroepithelial tumors (DNETs) and lowgrade gliomas. In cases involving the basal frontal lobe, a gross total resection to clear margins provides the best chance for control from both the oncology and epilepsy standpoint.148 Gliosis as a result of previous anoxia, head trauma, or other unknown causes may be the only identifiable in pathology in surgical specimens obtained from patients with focal epilepsy. Lastly, a curious clinicopathologic entity of intracranial choristomas involving the gyrus rectus has been reported recently in two adult patients with seizures. In both cases the epileptogenic lesions were composed of heterotopic epithelial, glial and mesenchymal components. The histogenesis of these lesions is unclear, but the preferential involvement of the gyrus rectus, which is in close proximity to the frontal bone, led the authors to speculate a common origin from neural crest progenitors.149 Medical therapy Seizures arising from the basal frontal region may respond to standard anticonvulsant agents (AEDs). As the seizures are focal in origin carbamazepine (or phenytoin) has been recommended as first line of treatment.150 Alternatively monotherapy with a newer AED such as lamotrigine, oxcarbazepine, topiramate or gabapentin could be considered based on drugdrug interactions and side-effect profile.151 If patients do not respond to monotherapy trials at maximum tolerated doses a second agent may be added. Valproic acid may have a role in preventing secondarily generalized seizures. Other adjunctive agents include levetiracetam, zonisamide and tiagabine.152 Approximately 65% of patients with focal epilepsy respond to appropriate anticonvulsant therapy.153,154 When medical therapy provides inadequate control of seizures or unacceptable side effects, the possibility of resective surgery should be explored. Patients with evidence of pharmacoresistant focal epilepsy should be referred to a specialized epilepsy center for presurgical evaluation and management. Patients who are not favorable surgical candidates or have failed surgical resection may be considered for implantation of a vagus nerve stimulator (VNS). Unfortunately, it has not been possible to predict which patients will benefit from chronic VNS before implanting the device.155 Surgical approaches to the OFR The surgical anatomy of and surgical approaches to the orbitofrontal region have not been well characterized in the published literature. One possible reason for this may be
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the fact that prior to the widespread application of invasive electrophysiology in surgical epilepsy programs the OFR has generally not been viewed as a target for resection. While portions of the basal frontal lobe are routinely retracted during neurosurgical procedures for vascular or neoplastic abnormalities, resections of the OFR itself are uncommon. A notable exception is the resection of the gyrus rectus that is carried out to facilitate exposure during pterional/subfrontal approaches to aneurysms involving the anterior communicating artery and proximal A2 segment of the anterior cerebral artery. The epilepsy surgeon accessing the OFR should, therefore, familiarize him/herself with the anatomy of the region and discuss the goals of the planned procedure with the treating epileptologist. Invasive monitoring of the OFR The investigation of nonlesional basal frontal lobe epilepsy is challenging, yet necessary, given the ‘buried’ nature of the cortex in this region. We prefer the use of subdural electrodes to depth electrodes to investigate the OFR. If a fronto-temporal craniotomy is planned, it is extended anteriorly to expose most of the frontal operculum; if burr holes and strip electrodes are planned, one burr hole is placed over the pterion (‘the keyhole’). In the case of a craniotomy, a 4×4 electrode array, with its lead situated laterally, is placed over the orbital roof, to cover a significant portion of the OFR. If burr holes are used, a 4-contact strip electrode is placed over the posterior portion of the OFR. Resections of the OFR The surgical approach to the OFR is dictated by the surgeon’s familiarity with a particular approach, the pathologic process being treated (lesion resection versus regional OFR excision for intractable epilepsy), the location of the lesion, and whether or not the resection involves the (presumed or apparent) dominant hemisphere. Another important consideration during surgical planning should be the connections of this region with the anterior and medial temporal lobe and the cingulate gyrus. Incomplete resection of epileptogenic cortex left attached to these structures, may compromise surgical outcome. Given that these connections extend from the posterior edge of the OFR, and that the posterior boundary is intimately linked to multiple structures (anterior perforated substance, optic nerve and anterior cerebral artery) – damage of which can result in significant deficits – an intimate knowledge of the anatomy of the OFR is crucial to successful surgical outcomes. Prior descriptions of surgery in the OFR have variously delineated the posterior extent of orbito-frontal excisions as being about 1–2cm in front of Broca’s area in the languagedominant hemisphere or extending posteriorly to the ipsilateral internal carotid artery156 and the intersection of the optic and olfactory nerves.107 We find a subpial approach combined with intraoperative frameless stereotactic navigation to be safer, and prefer to use the proximal anterior and middle cerebral arteries (viewed through intact pia) to delimit the resection margins (Figure 37.2). The OFR may be approached using three possible trajectories, depending on the nature and location of the lesion (Figure 37.3): ● ● ●
Lateral frontal; Anterior frontal; and Intermediate or anterolateral approach, which may be combined with orbito-zygomatic osteotomy.
The lateral frontal is by far the commonest approach for an OFR resection in the context of epilepsy surgery. This is because many such resections occur in the context of a large fronto-temporo-parietal craniotomy performed for placement of subdural electrodes for invasive electrophysiology. The resection is usually carried out at the time of electrode removal, and the orbital cortex is therefore approached from its lateral aspect. An en bloc resection of all, except the most posterior aspect, of the lateral, posterior and medial orbital gyri, and a portion of the anterior inferior frontal gyrus is carried out. This is followed by subpial aspiration of gyrus rectus. The ipsilateral anterior cerebral artery (ACA) is identified and traced posteriorly to the rostrum of the corpus callosum. Finally, the posterior limits of the orbital gyri and the subcallosal (rostral) cingulate gyrus are aspirated using a subpial technique (Figures 37.4 and 37.5). Identification of the ACA helps determine the posterior extent of the medial resection. The M1 segment of the middle cerebral artery (MCA) may be used to define the posterior edge of the resection. Use of a subpial technique during the medial and posterior aspect of the resection is crucial in minimizing risks to the anterior perforated substance, olfactory tract, and optic nerves. The anterior approach is principally used for excisions of overt OFR lesions and resections in the context of depth electrode recordings. Preoperative placement of a lumbar drain minimizes the need for retraction. A bicoronal scalp incision is made, following which a frontal craniotomy bone flap is elevated – from just above the frontal sinus, just lateral to the midline (and anterior sagittal sinus) and extending laterally to the anterior attachment of the temporalis muscle. A frameless stereotactic system may be used to demarcate the edges of the craniotomy and facilitate approach to the lesion. The dura is opened, with its base on the sagittal sinus, following which the lesion is resected. Subpial techniques should be used when there is a need to remove abnormal (gliotic, hemosiderin stained etc.) cortex surrounding the lesion. A principal advantage of the anterior and antero-lateral approaches is that the inferior frontal gyrus is more easily spared (Figure 37.7). The antero-lateral approach, combined with an orbitozygomatic osteotomy may be useful in cases where a large lesion is situated in the postero-medial OFR, and the intention is to minimize dissection and retraction of uninvolved cortex. A frontal craniotomy incision extending to the contralateral midpupillary line is used, following which a frontal craniotomy and orbito-zygomatic osteotomy are carried out. The dura is then opened with its base on the orbital contents, and resection of the lesion is performed. A lumbar drain placed prior to the craniotomy further helps in minimizing retraction. Occasionally invasive recordings may suggest independent ictal onsets originating from both the medial temporal and orbitofrontal regions. These cases can be managed with concurrent resections, possibly guided by the judicious use of intra-operative electro-corticography (ECoG) to measure the impact on electric activity in one region after the other is resected. Routine resection of the OFR concurrent with a temporal lobectomy is not recommended – although some authors have adopted a combined approach guided solely by the apparent location of interictal abnormalities.157
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Basal frontal lobe epilepsy Possible complications related to surgery in the OFR include: infection of the surgical site, osteomyelitis and/or CSF fistulae from opening the frontal sinus mucosa during craniotomy; hemorrhage from injuring the anterior sagittal sinus; venous infarcts when sacrificing veins leading into the sinus; visual deficits following injury to the optic nerve; ischemic events following injury to perforating vessels in the anterior perforating substance; CSF rhinorrhea through the cribriform plate and anosmia if the olfactory nerve and tracts are destroyed; and inadvertent injury to the contralateral frontal lobe if the medial frontal pial layer is not recognized and respected. In addition, there may be impacts upon personality and social behavior following OFR resections – such deficits are not adequately assessed with the current, standard neuropsychological measures employed in patients undergoing epilepsy surgery. Outcome There is no systematic study of outcomes related to resections for the treatment of basal frontal lobe epilepsy, and studies examining neuropsychological function in patients with epilepsy arising from this region are lacking. In general, just as for other extratemporal epilepsies, outcomes following resective epilepsy surgery anywhere in the frontal lobe are considered to be ‘not as good’ as those after temporal lobectomy.121,144 The presence of a lesion on neuroimaging increases the chances for seizure-freedom or significant improvement.35 Cumulative results of surgical treatment for various frontal lobe epilepsies in the pre-MRI era have been characterized as ‘unsatisfactory’ or ‘mediocre’.103 As a rule, results following removal of discrete frontal lesions are superior to those with more diffuse lesions or without demonstrable lesions.66 In a study of 68 consecutive patients, who underwent epilepsy surgery involving the frontal lobe good outcome at last follow-up was reported in 72% of patients with evidence of a lesion on neuroimaging, as compared to only 41% of the ‘nonlesional’ cases.158 We recently performed a retrospective review of all frontal lobe resections performed by a single neurosurgeon for the treatment of pharmacoresistant focal epilepsy at the Cleveland Clinic Foundation during a 6-year period (from 1998 to 2004). All cases had undergone a comprehensive presurgical evaluation including high-resolution preoperative MR imaging and presentation at a multidisciplinary patient management conference. Out of a total of 130 patients, who had frontal resections during the study period, basal frontal lobe epilepsy was suspected in eight patients.159 In these patients, MRI demonstrated a lesion restricted to the OFR, and/or invasive recordings provided clear evidence for ictal onset within the OFR. Patients with more extensive MRI lesions were excluded. Only two cases were nonlesional (i.e., there was no identifiable structural abnormality on high-resolution anatomical MRI); in three of the six ‘lesional’ cases the MRI detected blurring of the gray-white junction in the medial OFR. Histopathology revealed malformations of cortical development in the majority of patients (5 of 8); cavernomas were found in two, and gliosis in one patient. Resections were restricted to the OFR only in four of the eight patients; the other four underwent larger resections that extended into the lateral frontal region. In this study median follow-up was only 14 months. Seven patients were seizure free, while one had rare seizures postoperatively (Wieser class 3).54
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Illustrative case presentation The patient is a 33-year-old, right-handed young man with frequent pharmaco-resistant seizures dating back to the age of 26 years. The patient has a history of a motor vehicle accident at the age of 21 years, when he drove into a telephone pole. He lost consciousness upon impact, and had peritraumatic amnesia and a left-sided skull fracture. He did not require neurosurgical intervention and did not experience seizures at the time of the accident. Seizures started approximately 5 years later. Initial seizures were primarily nocturnal occurring out of sleep. Family members described ‘whole body convulsions’ followed by stertorous respirations and loss of urine control lasting for less than 1–2 minutes. Postictally the patient reported tiredness, muscle soreness and occasional tongue biting. These seizures have been disabling and have persisted despite several trials of antiepileptic agents with an average frequency of at least one to four per month. A second ‘mild seizure type’ was reported. During wakefulness he would have a warning described as ‘feeling unwell’ or having ‘a funny feeling in the head’ lasting for a few seconds, and followed by loss of awareness. Family members described staring and unresponsiveness for 2–3 minutes. During this period the patient had been observed to have complex movements involving the legs and hands. Patient was not sure as to the frequency of this second seizure type. He reported having auras at least once a month. He had no history of prolonged, unremitting seizures or physical injury as a result of seizures. He has been unable to work for the last 7 years, because of seizures. Examination and investigations Physical and neurological examinations were normal. Routine outpatient EEG was normal. Magnetic resonance imaging revealed an area of focal encephalomalacia in the ventral and basal aspects of the left anterior frontal lobe abutting the roof of the left orbit. The patient was admitted for video-EEG monitoring. Background EEG was normal. Interictal epileptiform activity was recorded predominantly arising from the left temporal region (maximum at the left sphenoidal electrode (Figure 37.6). Less frequent generalized epileptiform discharges with a shifting bifrontal maximum were also present (Figure 37.7). In addition, rare right temporal sharp waves were described. Three typical nocturnal seizures were recorded during sleep. They were characterized by an early change in facial expression and unresponsiveness, followed by tonic stiffening and elevation of the right arm (sign of four, right arm extended with the left arm flexed at the elbow), and right head turning preceding the onset of the secondarily generalized tonic-clonic seizure. Interictal FDG-PET showed mild decrease of FDG uptake in the left orbitofrontal region, corresponding to the area of MRI abnormality. Wada testing (with intracarotid administration of methohexital) demonstrated left hemispheric dominance for language and bilateral memory representation. Baseline neuropsychological evaluation suggested bilateral frontotemporal dysfunction. The patient appeared to have greater difficulties with verbal than visuospatial intellectual measures. He exhibited evidence of compromised executive function in the course
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of problem solving, impaired verbal memory performance and some deficiencies in vocabulary, naming and reading. The case and results of presurgical studies were discussed in a weekly, interdisciplinary patient management conference attended by experts in clinical epileptology, electroencephalography, structural and functional neuroimaging and neuropsychology. The impression was that the patient’s epilepsy may be arising from the left orbitofrontal region ‘perhaps deep in the area of encephalomalacia’. A temporal onset could not be excluded. An invasive evaluation with a combination of chronically implanted subdural and depth electrodes was recommended to further delineate the seizure onset zone, and its relationship to the encephalomalacic lesion (Figure 37.9). In addition, this approach would allow functional mapping of adjacent eloquent cortex (anterior language area) by means of extraoperative electrical cortical stimulation. Six typical nocturnal seizures were recorded in the span of 8 days of invasive recordings. All seizures were characterized by focal EEG changes restricted to the mesial, posterior edge of the orbitofrontal plate (Figure 37.10). Based on three-dimensional MRI reconstructions of the electrode location and underlying epileptogenic lesion the area of seizure onset was found to correspond to the posterior edge of the encephalomalacia. Treatment and outcome A resection of the left orbitofrontal and anterior ventral frontal regions was performed. Postoperatively the patient experienced a single breakthrough seizure at 3 months and a cluster of three seizures within one day (in the context of a flulike illness) at approximately 6 months. At his last follow-up
the patient has been seizure-free since for more than a year on a stable combination of lamotrigine and levetiracetam.
Summary The basal frontal lobe is perhaps one of the least explored and least understood regions of the human cerebral cortex. This highly multimodal area is characterized by its functional heterogeneity and widespread connections within the frontal lobes and limbic system. The anterior part of the OFR has the appearance of granular isocortex and is connected to the heteromodal prefrontal cortex. The posterior OFR has a more primitive, dysgranular architectonic appearance and is intimately connected with the limbic system. Localization of epileptogenicity arising from the basal frontal lobe is particularly difficult because of the absent or potentially misleading information derived from scalp EEG recordings, and the lack of distinct ictal manifestations. The advent of sophisticated neuroimaging techniques (especially high-resolution anatomical MRI) and the increasing capability to perform invasive recordings from the OFR has made it possible to delineate epileptogenic foci within this region. A limited number of patients with identifiable lesions in the orbitofrontal area and very few patients without evidence of MRI abnormalities have been reported to be seizure free after localized surgical resections. The intimate spatial and functional relationship of the OFR with limbic structures and the reported successes following targeted resections underscore the utility of evaluating this region closely in cases of focal epilepsy presumed to originate in the frontal or temporal lobes.
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Parieto-occipital lobe epilepsy V Salanova
Introduction Occipital lobe epilepsy was first recognized by Gowers in 18791 when he described a 30-year-old man with ‘epileptoid attacks with visual aura’. The patient described a very brilliant image before him ‘like a gold serpent’. This patient at other times had episodes of transient blindness. The patient was found to have an occipito-parietal tumor at autopsy. Gowers interpreted the aura as follows: ‘at first there was apparently an over action of the center – a bright light; afterwards paroxysmal defective action, due to temporary exhaustion or inhibition, shown in the narrowing of the field of vision’. When Gowers examined his records,2 he found that 84 of his 1000 patients with epilepsy exhibited a ‘special sensory aura’ which was referred as ‘the organ or sense of sight’, he subdivided these ‘ocular and visual warnings’ into five categories: a sensation in the eyeball itself, diplopia, an apparent increase or diminution in the size of the objects, loss of sight, and distinct visual sensations such as elementary visual hallucinations. The symptomatology of occipital epilepsy was further defined in 1927 by Gordon Holmes3 when he studied patients who had sustained gunshot wounds to the occipital region who exhibited occipital auras, characterized by elementary visual hallucinations or transient blindness, and in 1941 by Penfield and Erickson,4 who described the clinical manifestations of several patients with ‘visual seizures’, including blindness, and coloured moving lights, and were able to elicit the auras by cortical stimulation. In 1951 Penfield and Kristiansen5 reported that 11 of 222 patients with focal epilepsy treated surgically had ‘visual sensations’ as the first manifestation of their seizures, characterized as sensations of lights, darkness of colour, and five patients reported that the visual image was ‘revolving’ or ‘rotating’. Penfield and Jasper,6 described several patients with ‘visual seizures’, including the patient C.Fr. with a traumatic scar of the pole of the right occipital lobe who had an incomplete left homonymous hemianopia. The patient felt that the seizures were induced by a bright light, to the point that he refused to have the examiner shine a light in his eye. Wilder Penfield stated that ‘This is an example of sensory precipitation of a visual seizure’. The patient described lights followed by blurring of the vision progressing to complete blindness and then a sensation of stiffness in the left hand, and right hand, followed by a generalized seizure. Penfield stated ‘The somatic sensation in both hands suggests that the spread of discharge was from the calcarine cortex to the supplementary area 314
within the sagittal fissure. At the onset of the generalized seizure the head and body turned to the left’. Penfield and Jasper7 also reported two patients whose spontaneous seizures began with elementary visual hallucinations, followed by complex visual images. In both patients the habitual complex visual hallucinations were elicited at surgery by stimulation of the right posterior temporal region, suggesting that during the spontaneous attacks the hallucinations probable represented spread of the ictal discharge to the temporal lobe. Ludwig and Ajmone Marsan7 reported the clinical manifestations in 55 patients with electrographic evidence of occipital lobe involvement, and noted that as many as two-thirds had lateralized visual manifestations, Blume et al.8 found that in 13 of 19 (68%) of their patients the most common initial ictal symptoms were visual phenomena, and Williamson et al.9 reported that in 22 of 25 patients (88%) with occipital lobe epilepsy, early signs or symptoms ‘would had provided clues for the correct diagnosis’. In the series from the Montreal Neurological Institute10 in more than two-thirds of the patients the clinical manifestations indicated the occipital onset of the seizures. Functional anatomy Von Economo11 divided the occipital cortex into striate, peristriate, and parastriate regions. The striate cortex contained within the walls of the calcarine fissure, constitutes Brodmann’s area 17, and it is recognized by the thick strip of granular cells in layer IV that is split by the geniculocalcarine band of Gennari. All layers of this cortex reveal marked granularization. All six layers of cortex are delineated in the peristriate and parastriate cortices (areas 18 and 19). Numerous pyramidal cells are found in layers II, III, and V and giant pyramidal cells populate area 18, immediately bordering on the striate cortex. Jones and Powell12 studied the distribution of projection pathways emanating from areas 17, 18, and 19 by selectively ablating these areas in adult rhesus monkeys. The striate cortex projected to areas 18 and 19, whereas areas 18 and 19 projected fibers to area 8 in the frontal lobe and the adjacent temporal and parietal association cortices. The pathways include the superior longitudinal, the inferior longitudinal and the fronto-occipital fasciculus. Areas 18 and 19 also project deep fibers to the midbrain tegmentum. Further elucidation of the occipital lobe functional anatomy arose from electrical cortical stimulation studies in
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Parieto-occipital lobe epilepsy humans undergoing epilepsy surgery. Wilder Penfield and Theodore Rasmussen in the Cerebral Cortex of Man,13 found that 22 patients reported gross visual sensations as the result of stimulation. These visual responses were elementary sensations of light, darkness, and color. They also reported that ‘complicated visual hallucinations do occasionally result from epileptic or electrical stimulation, but these are phenomena of another order and are associated with activation of the temporal lobes’. They observed that ‘the visual responses appear in the secondary visual areas of Brodman (18 and 19) as well as in the primary calcarine area 17. They noted that ‘in general, it would appear that the calcarine image was more often colored while images produced from the secondary visual zone more often consisted of colorless light’. Symptomatology and pathophysiology of occipital lobe seizures An analysis of 42 patients with refractory occipital lobe epilepsy treated surgically at the Montreal Neurological Institute (MNI) between 1930 and 199110 showed that the clinical features of occipital lobe epilepsy can be divided into those representing seizure phenomena of occipital lobe origin, which include elementary visual hallucinations, ictal blindness, blinking and ocular movements and those resulting from ictal spread to adjacent cortical areas. Fifty-nine percent had visual field deficits. Seventy-three percent of the patients had visual auras. In those patients where the data were available, the elementary visual hallucinations were contralateral to the epileptogenic area. One patient with left occipital microgyria and a right homonymous hemianopsia described ‘dancing lights, whirling lights to the right’ followed by right head and eye deviation, and right head and eye clonic activity. Another patient with left occipital microgyria and a right homonymous hemianopsia described a slowly rotating disk of light in the right visual field. Others described flashing colors, and change in perception of shapes and colors. Another patient with left occipital cortical dysplasia and right upper quadrantanopsia described ‘circles, triangles squares, all colors’, and a visual sensation of movement, followed by conscious right head and eye deviation and right arm posturing. A patient with left occipital gliosis described ‘colored squares of light’ followed by blindness, right head and eye deviation and postictal dysphasia. Four patients had elementary visual hallucinations followed by complex visual hallucinations: a 12-year-old with a history of birth trauma and right occipital gliosis had elementary visual aura characterized by colored triangles followed by a complex hallucination in which he saw a robber, or a man with a gun; sinister characters from comic books, followed by conscious adversion to the left, nystagmoid eye movements, left arm clonic activity and postictal left hemiparesis. Another patient with a left hemianopia described ‘a square with a circle in it’, faces, pictures like Rembrandt’s self portrait. The reason for these complex visual hallucinations is most likely ictal spread to the posterior temporal region, as Penfield and Perot14 found that complex visual hallucinations could be elicited by posterior temporal stimulation near the occipital cortex, and Gloor et al.15 reported that experiential phenomena (visual and auditory) ‘did not occur unless a seizure discharge or electrical stimulation involved limbic structures’.
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Ictal blindness has been a consistent symptom of patients with occipital lobe epilepsy. Twenty-eight percent of patients from the MNI had ictal blindness as an initial manifestations of their seizures which lasted as long as a few minutes. A 24year-old patient with left occipital gliosis described a shadow moving to the right, ‘ombrage’ followed by blindness, and conscious adversion to the right. Russel and Whitty16 reported blurring or extinction of vision in 40% of their patients with traumatic occipital lobe epilepsy, and Williamson et al.9 reported that 10 of 25 (40%) of their patients with occipital lobe epilepsy exhibited ictal amaurosis. Barry et al.17 reported five patients with ictal blindness and electrographic (EEG) monitoring revealed that complete blindness occurred with ictal spread to the contralateral occipital lobe, demonstrating that ictal blindness is caused by seizure induced bilateral occipital lobe dysfunction. Other authors have also reported lateralized visual auras in patients with occipital lobe epilepsy, Sveinbjornsdottir and Duncan,18 Aarli and Engelsen,19 Geller et al.,20 Boesebeck et al.,21 Taylor et al.,22 and Blume et al.23 Other occipital manifestations in the MNI series included eye pulling or moving sensations, blinking, nystagmoid eye movement and contralateral eye movements. Nineteen percent of the MNI patients exhibited blinking and 7% had contralateral nystagmoid eye movements. In one patient, studied with depth electrodes, the nystagmoid eye movements were contralateral to the seizure discharge. Munari et al.24 described 16 patients with stereo EEG who had seizures with ocular deviation within the first 10 seconds of the seizure onset. In 14 patients the ocular deviation was tonic and in all was contralateral to the ictal discharge, which generally originated in the medial occipital structures. Cortical stimulation studies in animals and humans demonstrate that eye movements can be initiated by occipital mechanisms.25,26 Contralateral head and eye deviation was present in half of the MNI patients. Two of these patients were studied with depth electrodes and had contralateral head and eye deviation while the seizure remained localized to the occipital lobe. Ludwig and Ajmone-Marsan7 reported contraversive movements of head and eyes in 29% of their 55 patients. Automatisms similar to those from patients with temporal lobe epilepsy occurred in 50%, and focal motor activity in 38% of the MNI patients, and one-third of the patients had more than one seizure type. Ajmone-Marsan and Ralston27 suggested that seizures originating in the occipital lobe could have multiple spread patterns. Subsequently this was confirmed by intracranial recordings in humans28,29 and animal experimental data.30 The inferior longitudinal, superior longitudinal and the fronto-occipital fasciculus are involved in this spread. Etiologies of occipital lobe epilepsy Rasmussen,31 identified the etiology of refractory occipital lobe epilepsy, established by history and pathological findings in 23 patients; one-third had a history of head trauma or anoxia; 9% had gliomas and 13% postinflamatory brain scarring. In 26% of patients no cause could be determined. The remaining patients had other lesions including pial angiomatosis. In the updated series of 42 patients from the
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MNI, 21% had a history of significant head trauma with loss of consciousness, 24% had a history suuggestive of birth trauma or hypoxia, 7% had a history suggestive of encephalitis, and 10% had slow growing glial tumors. Others had focal cortical dysplasia. Ludwig and Ajmone-Marsan7 reported that 24% of their patients had a history of birth injury, hypoxia, and severe head trauma; 13% had a history of encephalitis or meningitis; 14% vascular lesions, and 7% expanding lesions. In 25% the etiology was unknown. A recent series from the Yale Epilepsy Center, of 35 patients with intractable occipital lobe epilepsy treated between 1986 and 1995, reported that most of their patients had developmental abnormalities or tumors,32 and Lee et al.33 reported that 20 of 26 of their patients with occipital lobe epilepsy had a pathological diagnosis of cortical dysplasia. EEG findings in occipital epilepsy In the MNI series, the most common location of interictal epileptiform discharges was the posterior temporal-occipital region (46%). Interictal epileptiform discharges were localized to the occipital lobe in only 18% of patients. One-third of the patients had synchronous lower amplitude epileptiform discharges from the contralateral homologous head regions, suggesting secondary bilateral synchrony. Bitemporal interictal epileptiform discharges were recorded, in 24% of the patients. This is probably a manifestation of secondary bilateral synchrony and/or secondary epileptogenesis.34,35 The most common type of surface ictal onset was regional involving the posterior temporal occipital region. Ictal onsets on surface recordings restricted to the occipital lobe were seen in only four out of 24 patients (17%). Six patients had intracranial recordings with depth electrodes. Ictal onsets were predominantly regional rather than focal and involved widespread areas of the mesial and lateral occipital cortex, often involving the supra and infracalcarine structures and, in some seizures, the posterior temporal region. The most common pattern of spread involved the ipsilateral temporol-mesial structures. Aykut-Bingol et al.32 found that of 35 patients who had occipital lobe epilepsy surgery between 1986 and 1995, interictal scalp EEG was localized to the occipital, temporal, and occipitotemporal regions in 17%, 27%, and 24% of patients, respectively. Ictal events were recorded in 30 patients. Ictal onset was localized to the occipital lobe in 30%, and temporal and occipitotemporal in 27%; in the rest it was more diffuse. Nineteen patients underwent intracranial EEG studies. Foldvary et al.36 analyzed the localizing value of ictal EEG in focal epilepsy, and found that ‘false localization/ lateralization occurred in 28% of occipital seizures.’
Parietal lobe epilepsy Historical background, and functional anatomy Wilder Penfield, Theodore Rasmussen, and their colleagues divided their patients with refractory epilepsy into those whose epileptogenic areas involved the frontal, central (sensorimotor area), parietal and occipital regions.4,6,13 Patients with epileptogenic lesions involving the pre- and post-central gyrus were grouped together, because lesions in
this cortex produced sensorimotor deficits, and as Penfield and Erickson4 stated ‘the precentral and postcentral gyri in man constitute a functional unit. Close interrelationship of motor and sensory cortical areas is established by the numerous connecting U-shaped fibers which pass under the bottom of the central fissure’. Penfield and Rasmussen,13 noted that ‘by Parietal area is meant that portion of the classical parietal lobe which lies behind the post central gyrus’, ‘if the lower parietal area which constitutes the parietal speech area on the dominant side be excluded, the superior parietal cortex could be removed with a comparatively small functional penalty’. Penfield and Erickson4 had described that ablation of the parietal association cortex left little obvious functional deficits though ‘disturbances of speech and disturbances in perception of form in the opposite homonymous visual field has been noted’. Rasmussen37 continued to use the functional division of the brain developed by Foerster and Penfield,38 since their definition of the parietal lobe differs from the generally employed in reviewing the MNI series of parietal lobe epilepsy, we refer to ‘parietal association area’ to define the region behind the postcentral gyrus and in front of the occipital lobe. Foerster and Penfield,38 described patients with epileptogenic lesions and ‘parietal field attacks’, characterized by painful sensations, vertigo, paresthesias, head and eye deviation, a sense of movement of one extremity, visual illusions, and complex movements of arms and legs, and reproduced these symptoms by faradic stimulation. Cushing39 expanded on these observations when he described 12 patients with parietal meningiomas; nine of them had a contralateral sensory aura, described as numbness, tingling, painful sensation or a feeling of warmth or heat. Since then few series of patients with parietal lobe epilepsy have been reported. Clinical manifestations and pathophysiology Patients with parietal lobe epilepsy with epileptogenic areas in the parietal cortex behind the postcentral gyrus, comprised 6% of patients operated at the Montreal Neurological Institute (MNI) between 1929 and 1980.40,41 Eighty-two patients had nontumoral parietal lobe epilepsy (Figure 38.1), with a mean age of seizure onset of 14.1 years and mean duration of epilepsy 8.1 years. Twelve patients had contralateral sensory deficits which were found during detailed examination and consisted of contralateral impaired two pointpoint discrimination, isolated diminished stereognosis, without two point discrimination, was reported in only two patients. Sixteen percent of patients had smallness of the contralateral extremities, 8% contralateral visual field deficits, most commonly inferior quadrantic defects. Impairment of spatial orientation and right–left disorientation were described in three patients, disturbance in the field of written language, and mild aphasia in two others. Ninety-four percent of patients exhibited auras. The most common were somatosensory, described by 52 patients as tingling or numbness; they were contralateral to the epileptogenic zone in 51 patients and bilateral in one; 13 of these patients described a painful, and five a thermal sensation. The second most common auras were disturbances of body
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parietal lobe to the temporo-limbic areas. This pattern of spread is supported by Reesnick et al.,44 who used subdural electrodes in the evaluation of patients with refractory epilepsy, and is a reflection of the connection of the parietal lobe with the supplementary motor area, and with the temporo-limbic region,.45,46 Other authors and recent reviews have also reported asymmetrical tonic seizures and automatisms in patients with parietal lobe epilepsy, and have emphasized that many of these patients have more than one seizure type.18,47–50
Figure 38.1 Original operative map of patient A. H. operated on by Dr Penfield in 1946. 25 year old with history of head trauma. The seizures were described as ‘does not know where he is, cannot concentrate, cannot see well’, followed by turning to the left.
image exhibited by nine patients; three patients mentioned a sensation of movement in one extremity, and another a sensation that the leg was absent. Twisting or turning sensations of the extremities were also described. Visual illusions were reported by nine patients as ‘figures look larger’ or ‘things on the wall turning’. A few patients exhibited complex visual or auditory hallucinations, suggesting ictal spread to temporo-limbic areas.15 Eighty patients underwent intraoperative cortical stimulation studies and the habitual auras were reproduced in 55% of patients. These included auras with a disturbance of body image or visual illusions, indicating an epileptogenic zone in the parietal association cortex. However, somatosensory auras also occurred in patients with lesions limited to the parietal association cortex, suggesting ictal spread to the somatosensory cortex. Thus, the symptomatogenic zones were distant from the epileptogenic zones in the parietal association cortex, Luders and Awad.43 Other seizure characteristics The other clinical manifestations were due to ictal spread. The ictal semiology indicated several dominant spread patterns, including spread to the sensorimotor cortex, the premotor eyefield, supplementary motor area, and the temporolimbic region. Twenty-eight percent had tonic posturing of the extremities, 57% had focal motor activity, 17% had oral-gestural automatisms, and 4% had complex automatisms. Fortyone percent had head deviation, 22% had Todd’s paralysis and 7% had postictal dysphasia. Many patients had more than one seizure type reflecting the different spread patterns. Sixty-one percent of patients with tonic posturing had epileptogenic zones which included the superior parietal lobule, and 79% of those with automatisms had epileptogenic zones extending into the inferior parietal lobule. This suggest preferential spread with ictal activity from the superior parietal lobule more commonly spreading to the supplementary motor area, and the one from the inferior
Etiologies of nontumoral parietal lobe epilepsy Thirty-five patients from the MNI series had a history of head trauma, and 16% had a history of birth trauma. The remaining patients had a history of encephalitis, febrile convulsions, gunshot wounds to the head, forme fruste of tuberous sclerosis, hamartomas, vascular malformations, tuberculoma, arachnoid or porencephalic cysts, microgyria and post-traumatic thrombosis of the middle cerebral artery. Tumoral parietal lobe epilepsy Thirty-four of 116 patients (29%) from the MNI series with parietal lobe epilepsy had slow growing tumors (Figure 38.2), most commonly astrocytomas (62%) and meningiomas (14%). The remaining patients had hemangiomas, oligodendrogliomas, and mixed astrocytoma and oligodendroglioma. Forty-seven percent had impaired two point discrimination in the contralateral fingers, 38% had mild contralateral weakness, 6% aphasia, 3% smaller extremities contralateral to the epileptogenic zone, one right to left disorientation and acalculia and two spatial disability. Only one patient exhibited definite astereognosis without coexisting primary sensory cortical deficit. Seventy-nine percent exhibited auras, most commonly somatosensory, contralateral to the the epileptogenic zone in
Figure 38.2 Original operative map of patient E. O’k. operated on by Dr Penfield in 1947. 25 year old with weakness of left foot and absent two-point discrimination in left leg. The seizures began by a sensation in the left great toe, tingling in the left vulva, spreading to left breast (not sexual), followed by left leg and left arm jerking.
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all except for one patient. Four described a painful sensation. Twelve percent had visual illusions, 9% aphasic aurae, 6% disturbance of body image, 3% complex auditory hallucinations, and 3% a feeling of movement in one arm. Some patients had two or more auras. The clinical manifestations indicated different spread patterns; 21% had tonic posturing of the extremities, 28% had focal clonic activity always contralateral to the epileptogenic lesion, 15% had head deviation, 9% automatisms, and 6% difficulty speaking. Thirty-two percent had Todd’s paralysis and 18% had post-ictal dysphasia.
EEG findings in parietal epilepsy Surface EEG was available in 66 patients of the nontumoral parietal lobe epilepsy MNI series and seizures were recorded in 36 patients. The interictal epileptiform discharges were recorded from the fronto-centro-parietal region in 33% of patients, parieto-posterior temporal in 14%, parietal in 14%, parieto-occipital in 9%, fronto-centro-temporal in 4.5%, fronto-temporal-parietal in 4.5%, hemispheric, maximum posterior head region in 9%, and bilateral in 4.5%. No interictal epileptiform discharges were recorded in 7.5% of patients. Secondary bilateral synchrony was described in 32% of patients. Ictal discharges were predominantly lateralized, in some patients the maximum ictal activity was recorded over the centro-parietal region and in others over the posterior head region. Localized parietal seizure onset was recorded in four patients. Williamson et al.47 and Cascino et al.48 emphasized that surface EEG monitoring is often non-localizing in parietal lobe epilepsy, and Foldvary et al.36 reported false localization/lateralization in 16% of parietal lobe seizures.
Conclusions In more than two-thirds of the patients with occipital lobe epilepsy, clinical manifestations indicated the occipital onset of the seizures. Visual auras were reported in 47–73% of patients. Most patients exhibited contralateral elementary visual auras, and a few exhibited ictal blindness. Seven to nine percent of patients exhibited nystagmoid eye movements. Many of the disabling clinical manifestations resulted from ictal spread to adjacent cortical structures, 29–88% of patients exhibited automatisms typical of temporal lobe epilepsy, and 38–47% had focal motor activity. Some patients had more than one seizure type reflecting these different spread patterns. Contralateral visual field deficits were reported in 20–59%, and abnormal imaging studies in 37–72% of patients. EEG recordings often showed posterior temporaloccipital interictal epileptiform discharges, and ictal onsets were regional often involving the posterior temporal region. A quarter of patients had bitemporal independent interictal epileptiform discharges, and one-third had bilateral synchronous epileptiform discharges over the posterior head regions. Ninety-four percent of patients with parietal lobe epilepsy exhibited auras. The most common auras were somatosensory, including painful sensations. However the auras experienced by some patients, like disturbance of body image may have indicated an epileptogenic zone in the association parietal cortex. The ictal semiology indicated several dominant spread patterns; 28% had tonic posturing of extremities, 57% focal motor clonic activity, and 17% had oral-gestural automatisms. The surface EEG was often lateralizing rather than localizing. Brain tumors are often the cause of parietal lobe epilepsy and were found in one-third of 116 MNI patients.
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Cushing H. The parietal tumors. Inaugural sensory fits. In: Cushing H, ed. Meningiomas: Their Classification, Regional Behaviours, Life History, and Surgical End Results. Springfield IL; Charles C.Thomas, 1938:632–56. Salanova V, Andermann F, Rasmussen T. et al. Parietal lobe epilepsy: clinical manifestations and outcome in 82 patients treated surgically between 1929–1988. Brain 1995;118:607–27. Salanova V, Andermann F, Rasmussen T. et al. Tumoural parietal lobe epilepsy: clinical manifestations and outcome in 34 patients treated between 1934 and 1988. Brain 1995;118:1289–304. Gloor P. Experiential phenomena of temporal lobe epilepsy. Facts and hypotheses. Brain 1990;113:1673–94 Luders HO, Awad I. Conceptual considerations. In: Lüders HO, editor. Epilepsy Surgery. New York: Raven Press, 1991:51–62. Resnick TJ, Duchowny M, Jayakar P et al. Clinical semiology of parietal lobe epilepsy (abstract). Epilepsia 1993;34 Suppl 6:29. Jones EG, Powell TPS. An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. Brain 1970; 93:793–820. Pandia DN, Yeterian EH. Architecture and connections of cortical association areas. In: Peters A, Jones EG, eds. Cerebral Cortex, Vol. 4. New York: Plenum Press, 1985:3–61 Williamson PD, Boon PA, Thadani VM. et al. Parietal lobe epilepsy: diagnostic considerations and results of surgery. Ann Neurol 1992;31:193–201. Cascino GD, Hulihan JF, Sharbrough FW et al Parietal lobe lesional epilepsy: electroclinical correlation and operative outcome. Epilepsia 1993;34:522–7. Loiseau P. Parietal lobe epilepsies. In: H Meinardi ed. Handbook of Clinical Neurology: Vol. 73(29); The Epilepsies, part II, Amsterdam: Elsevier Science B.V., 2000:97–106. Siegel AM. Parietal lobe epilepsy. In: Siegel AM, Andersen RA, Freund HJ, Spencer DD, ed. Advances in Neurology: Vol. 93. The Parietal Lobes. Philadelphia: Lippincott Williams & Wilkins, 2003:335–45.
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Insular epilepsy J Isnard, P Ryvlin, and F Mauguière
Introduction The concept of insular epilepsy was debated in the early fifties when it was observed that insular stimulation could evoke symptoms very similar to those of temporal lobe seizures. This similarity could be such that confusion between insular and temporal lobe seizures might explain some of the failures of temporal lobectomy. In ‘Historical background and basic concepts’ we review the historical background and concepts on which are grounded recent depth Stereotactic EEG (SEEG) studies aiming at identifying the actual symptoms reflecting discharges located in the insular lobe. ‘The insula as an ictal symptomatogenic area’ is devoted to the description of an ictal symptomatic sequence, which occurs in full consciousness, and is highly suggestive of an epileptic discharge in the insular lobe. Based on SEEG recordings of spontaneous seizures and stimulation data, this sequence includes an initial pharyngeal and/or laryngeal discomfort with thoracic oppression or dyspnea, unpleasant paresthesiae, warmth or pain sensation in the perioral region or spreading to a large somatic territory, followed by dysarthric or dysphonic speech and ending by focal somato-motor manifestations. Several cortical areas, with which the insula is connected, are involved in most of the focal seizures originating in, or spreading to, the insula. Based on clinical observation of ictal symptomatology, invasive EEG investigations must be targeted to explore the whole extent of the suspected epileptogenic network in order to assess the role of the insula in seizure development. ‘The insula as a mode in distributed epileptogenic networks’ provides the arguments supporting identification of three major epileptogenic networks (temporo-perisylvian, temporo-limbic and mesialorbital frontal) where the insula participates as a node in the building of ictal symptomatology, including that of nocturnal frontal hypermotor seizures where the antero-superior part of the insula can be a clinically silent seizure onset zone. The final three sections are devoted to the review of etiologies, presurgical evaluation and treatment of insular epilepsies. Most cases reported in the literature as insular epilepsies are symptomatic of a focal epileptogenic lesion located in the insula, some of which were successfully operated upon, while the few cases of cryptogenic epilepsies hitherto available are those reported in this chapter. EEG plays a minor role for investigating insular epilepsies because interictal paroxysms and seizures originating in the insula are unlikely to be detected by scalp recordings. The roles of MEG and functional interictal neuroimaging remain incertain as well as the results of insular surgical resection based on SEEG data or of SEEG-guided thermo-coagulation in cryptogenic cases. Conversely seizure 320
freedom can be obtained after surgical resection of the lesion in symptomatic cases, provided that ictal symptoms are compatible with an epileptogenic zone located close to the lesion in the insular lobe.
Historical background and basic concepts The insula as the fifth lobe of the brain In an article published in 1896 that was devoted to the comparative anatomy of the insula, Clark1 quoted 39 synonyms used in anatomical literature to name the fifth lobe of the brain buried in the lateral sulcus and covered by the opercular parts of the frontal, parietal, and temporal lobes, among which the term insula, first proposed by Reil in 1804, has prevailed. The anatomical situation of the insula and its cytoarchitectonic organization lent some substance to the view that it might be an isolated lobe of the brain mostly devoted to the processing of body and visceral sensation including gustation, pain and other emotions, and to viscero-motor and autonomic control. In monkeys the insula includes Brodmann’s areas 13 to 16 and shows a caudo-rostral sequence of distinct cytoarchitectonic areas namely; a granular cortex, at its upper and posterior part, very similar to that of the second somatosensory (SII) area and involved mostly in somatosensory, pain and auditory functions; a transitional dysgranular field localized in its antero-superior part involved in gustation and and viscero-sensitive functions; an antero-ventral agranular field, which is in continuity with the temporal pole and olfactory proisocortex, and related to olfactory and autonomic functions (see ref 2 for a review). For the past 10 years the question of insular physiology has been addressed by numerous studies using neuroimaging, evoked potentials and direct stimulation in humans as well as microelectrode studies in monkeys. These studies have confirmed the role of the insula in: ●
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Somatosensory and pain sensation as assessed by numerous anatomical,3,4 functional imaging studies5–8, as well as by our recent studies of somato-sensory and pain evoked responses9 and direct electric stimulation of the Insular cortex10, 11 Visceral sensation and viscero-motor control12–14 including processing of visceral pain15 Cardiovascular function as demonstrated by insular stimulation in epileptic patients before temporal lobectomy that produced changes in heart rate or in blood pressure
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in 50% of cases,16 thus leading to suspect a role of insular discharges in cardiac arrhythmias causing sudden death during epileptic seizures. Gustation as assessed first by the stimulation studies of Penfield and Faulk17 and further confirmed by neuroimaging studies18, 31 as well as by microelectrode recordings of a large number of insular neurons in monkeys,20 these physiological findings being consistent with the altered taste perception observed in patients with insular lesion.21 Audition and language, in particular allocation of auditory attention, tuning in to novel auditory stimuli, temporal and phonological processing of auditory stimuli.22 Furthermore several studies suggest that both right and left insulae are involved in the control of speech production.23–28
More recently, some studies suggested that the insular lobe could belong to the mirror-neuron system that characterizes regions of the brain that are able to respond when the subject performs an action and when the subject observes another individual doing a similar action (see ref 29 for a review), but also regions able to encode for a sensation (or emotion) perceived by the subject and to respond to the observation of others experiencing that sensation (or emotion). In the human insula regions involved in visceral sensation or viscero-motor responses also respond to faces expressing disgust.30,31 Similarly the human insula responds to both pain perception and empathy for others’ pain.32 From what precedes one can conclude that the insula represents a highly organized lobe with specific functions comparable to the other lobes of the brain and, therefore, consider that an epileptogenic zone located in this area will cause seizures characterized by a specific ictal symptomatology. This point is addressed in details in the second section of this chapter where we discuss the localizing value of a sequence of ictal symptoms that are highly suggestive of an epileptic discharge affecting the insula. The insula as a node in distributed cortical networks As the other lobes of the brain, the insula is characterized by anatomical borders that are defined by a limiting sulcus (the circuminsular fissure) but also by fuzzy cytoarchitectonic borders with neighboring cortical areas and by a dense network of cortico-cortical connections with adjacent or more distant cortical areas. Therefore its function, as well as its implication in epileptic seizure development, cannot be sketched as an isolated functional center, as suggested by the term ‘insula’. A complete description of insular connections is given in the review by Augustine2 showing that the insula is connected with the limbic areas, the amygdalar nucleus, the basal ganglia, and all of the cortical lobes, except the occipital lobe. Several attempts have been made to identify functional networks in which the insula could play the role of a functional node.33–35 Among these networks the perisylvian-insular, the temporolimbic-insular, and the mesial-orbito-frontal-insular networks deserve the attention of epileptologists because epileptic discharges propagating in each of them will produce seizures where the symptoms attributable to the insula will reflect only part of the ictal symptomatology. In part III of this chapter we discuss the difficulties in identifying insular epilepsy among epilepsies where the epileptogenic zone spreads outside the
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limits of the insular lobe, and the utility of the concept of epileptogenic networks for planning the depth electrodes implantation in the presurgical evaluation of these patients. The concept of insular epilepsy In the late forties and early fifties Guillaume et al.36 followed by Penfield and Jasper37 were the first authors to call attention upon the concept of insular epilepsy. Penfield and Faulk38 concluded the review of their personal experience of insular stimulation by noting that the majority of the positive responses to stimulation of the insula consisted either in sensations resembling that produced by stimulation of the superior bank of the sylvian fissure (SII area), or in abdominal feeling secondary to motor change in the gastrointestinal tract. This latter finding suggested that seizures originating in the insular cortex were able to mimic temporal lobe seizures to such a degree that confusion between the two types of seizures might explain part of temporal lobectomy failures.36 This concept was mostly based on data from electrocorticography (EcoG) carried out during the surgical treatment of patients suffering from temporal lobe epilepsy (TLE) under local anaesthesia. Moreover EcoG recordings revealed a rich interictal spiking paroxysmal activity in about half of these patients.34 However, in spite of an EcoG strategy exploring systematically the insula, Penfield and his collaborators never succeeded to record spontaneous epileptic discharges with a focal onset in the insular cortex. Furthermore they were unable to provide the argument that insular cortectomy, as a complement to conventional temporal lobectomy in TLE patients, could improve the surgical outcome.39 Thus the concept that specific symptoms could reflect insular discharges into the insular lobe fell into dereliction. More recently, several case reports showed that seizures could be stopped by the surgical removal of insular lesions40–42 and reactivated the research for identifying the insula as a symptomatogenic area in focal epilepsy.
The insula as an ictal symptomatogenic area Identification of a given cortical area as a symptomatogenic zone is mostly based on correlations between the ictal symptomatology and data from ictal discharge recordings using invasive EEG procedures.43 In the case of the insular lobe such correlations are often uneasy because, even though the insula is frequently involved during temporal lobe seizures, most insular discharges develop concomitanty in the temporal, perisylvian, or frontal cortex, so that symptoms reflecting discharges in the insular cortex are difficult to disentangle from those related to the involvement of these neighboring areas in the building of ictal symptomatology. The patients’ file of our department reflects the rarity of focal seizures involving exclusively, or preferentially, the insular lobe. Of the 180 patients with temporal lobe epilepsy (TLE) referred to our department for presurgical evaluation since 1996, 83 were explored using depth electrodes implanted in the lateral and mesial regions of the temporal lobe, of whom 50 also had depth electrodes implanted in the insular. We have been able to identify an ictal symptomatic sequence associated with a focal discharge restricted to the insula in only eight of them (16%).
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Ictal symptoms reflecting seizure activity in the insula What we know about the electroclinical manifestations of insular seizures mostly stems from SEEG data from a few patients referred mostly for TLE surgery. Electrode implantation in the insula is usually decided on the basis of ictal symptoms or scalp video-EEG data suggesting an early spread of seizures either to the suprasylvian opercular cortex, such as tonic or clonic mouvements of the face, dysarthria or motor aphasia, gustatory hallucinations, hypersalivation, post ictal facial paresis,44 or to the infrasylvian opercular cortex such as auditory hallucinations or early sensory aphasia.45 For the description of insular ictal symptoms we selected seizures that were characterized by a SEEG discharge involving selectively the insula at any moment of the seizure development. In six patients discharges originated from the insula itself (cases 3 to 8 in Figure 39.1) and in two (cases 1 and 2 in Figure 39.1) discharges originated in the hippocampus but propagated exclusively to the insular cortex without spreading to any other cortical structure. Video recordings of patients’ behavior during insular seizures are illustrated in Figure 39.1. The five ictal features that were invariant in repeated seizures in a given individual and observed when the ictal discharge selectively involved the insular cortex are the following: (a) Consciousness and contact with the environment are fully preserved (b) Paresthesiae (lines B and C in Figure 39.1) represent the second feature that is reported by all patients during insular discharges. They are described as an unpleasant sensation of electricity or warmth that can be painful (2/8). They are either restricted to peri-or intra-oral areas (line B in Figure 39.1), or distributed to a large cutaneous territory (face-shoulder-arm and trunk, upper limb-trunklower limb) most often opposite to the insular discharge (line C in Figure 39.1), or bilateral (2/8) affecting either territories close to midline, such as mouth and oral cavity
1
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(1B and 2B in Figure 39.1), or more distal somatotopic areas such as both lower limbs (3C in Figure 39.1). Although the onset site and spreading of paresthesiae can vary from one seizure to the other, there is usually no somatotopic Jacksonian march as often reported in SI somatosensory seizures.46 (c) Motor and sensory pharyngo-laryngeal symptoms are other frequent manifestations (6/8) that are accompanied by the spontaneous gesture of seizing the neck with the hand ipsi- or contralateral to the discharge, or with boths hands, as illustrated in patients 1–6 in Figure 39.1 (line A). This sensation can be isolated or preceded, or followed, by other sensations such as a retro-sternal or abdominal heaviness that can be accompanied by rumbling noises and vomiting (image 1B in Figure 39.1), or a short breath with dyspnea as reported in the early descriptions of anterior insular stimulations by Penfield and Faulk.38 Its intensity is variable according to patients and is described either as an unpleasant sensation of throat constriction, or as the sensation that the salivary glands are under pressure preceding hypersalivaltion (image 2A–5A in Figure 39.1), or even as a terrifying sensation of strangulation with suffocation (images 1A and 6A in Figure 39.1). (d) A dysphonic and dysarthric speech evolving progressively toward a complete muteness is as frequent as the laryngeal sensation described above (6/8). It may persist several tens of seconds after the end of the discharge. (e) Finally, the clinical manifestations of insular seizures often (5/8) end with motor symptoms (cases 4–8, line D in Figure 39.1) that are either lateralized and opposite to the discharge (tonic spasm of face and upper limb), or more diffuse (head and eyes rotation, generalized dystonia). In a given patient the occurrence of motor symptoms is usually inconstant from one seizure to the other.
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D Figure 39.1 Video sequence of ictal symptoms in the eight patients with insular seizures. Empty areas correspond to missing symptoms in the sequence. All illustrated seizures are simple partial seizures with complete preservation of contact during phases A, B, and C of the sequence. A brief loss of contact occurred in phase D for patients 6 and 7 in association with intense somatomotor convulsive symptoms. A: Laryngeal constriction (6 patients). B: Paresthesiae in the perioral region (6 patients). C: Lateralized somatosensory symptoms in upper limb (7 patients). D: Focal somatomotor symptoms (5 patients). *For patient 3 somatomotor symptoms(D) did not occur during the three Video-SEEG recorded seizures, while most of spontaneous seizures in patient’s history ended by this type of symptoms. Colored frames distinguish rostral (green) from caudal (red) insular seizures. Green frame: symptoms associated with anterior insular ictal discharge Red frame symptoms associated with posterior insular ictal discharge.
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Insular epilepsy When observed at any given moment in the seizure such symptoms suggest that the insular lobe is included in the symptomatogenic zone; when observed at the onset of seizures they indicate that the insula should be involved in the surgically resected area to achieve postsurgical control of seizures; when an insular lesion is present their occurrence at seizure onset suggests that the epileptogenic zone is close to the lesion. This latter statement is illustrated by the patient whose brain MRI is shown in Figure 39.2. This female patient, aged 22, had suffered since the age of 16 from seizures begining by unpleasant and intense paresthesiae that involved a large proportion of the left side of her body including face, whole upper limb and trunk followed by a ‘strange taste’ in her mouth. Her seizures ended with hypersalivation and clonic jerks in her left face. MRI showed a cavernous angioma located in the posterior insular cortex, the removal of which was followed by the disappearance of seizures. Since surgery this patient has remained free of seizures and antiepileptic drugs, with a postsurgery follow-up of two years. Localization specificity of insular ictal symptoms: data from direct electric cortical stimulations Electric stimulation of the insula in patients presenting with one or more of the above listed ictal symptoms is useful for mapping
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Figure 39.2 Sagittal (a), coronal (b) and axial (c) MRI slice showing a right posterior insular cavernous angioma in a patient with painful seizures on the left side of the body, who became seizure free after lesionnectomy (see text for details).
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the symptomatogenic area when it reproduces symptoms that are immediately identified by the patient as identical to their spontaneous ictal symptoms. Thus lateralized and widely distributed paresthesiae could be triggered by stimulation in five of the eight patients whose ictal behavior is shown in Figure 39.1 (cases 1, 3, 5, 6 and 8), focal perioral paresthesiae in four (cases 1, 2, 3, and 6), laryngeal sensation in three (cases 2, 4, and 5), dysarthric speech in one (case 5) and abdominal pain in one (case 1). More generally direct stimulation of the insula, even in patients whose seizures are of extrainsular origin, is able to elicit all of the ictal symptoms of insular seizures. In our experience, the insula is one of the most eloquent cortical areas when electrically stimulated by shocks47 or trains11 at low intensities (1–3 mA). Insular stimulation sites explored in our group of 50 consecutive patients are plotted in Figure 39.3. Of these 144 sites, 125 were clinically responsive to stimulation in the absence of any after discharge, and a total amount of 139 evoked clinical responses could be collected (Figure 39.3b). Thirty-one of them were identified by the patients as identical to one of the ictal symptoms of their spontaneous seizures, 108 were reported as unknown and not belonging to the usual ictal symptomatology. As for ictal symptoms, these responses can be subdivided into five main categories: somatosensory (Figure 39.3Ca), viscerosensitive (Figure 39.3Cb and c), auditory (Figure 39.3Cd), dysarthria and missing words (Figure 39.3Ce), others including sensation of unreality, whole body sensations, olfacto-gustatory hallucinations, and vegetative responses (Figure 39.3Cf). Somato- or viscero-sensory responses represent nearly twothirds of evoked responses, of which more than half concern the cervical-laryngeal region. There is thus converging evidence from seizure analysis and stimulation data that these somatosensory symptoms, particularly in case of warmth or pain sensation, suggest an ictal involvement of the posterior insula. Similarly the laryngeal and visceral sensations reported by our patients during their seizures, and reproduced by electric stimulation suggest an anterior insular propagation of the epileptic discharge. This conclusion contrasts with the commonly accepted view that visceral and laryngeal ictal sensations indicate a hippocampal or amygdalar origin when observed in the context of TLE seizures.48, 49 Auditory symptoms and dysarthric speech immediately follow somatic and visceral sensations, in terms of frequency, in the list of responses evoked by insular stimulation. Auditory symptoms are currently attributed to ictal discharges in the temporal operculum and first temporal gyrus. Our data suggest that they may also reflect an insular propagation of the discharge. However, there are no types of auditory illusions or hallucinations that can be considered as specific to insular ictal semiology, because stimulation of the Heschl’s gyrus can evoke auditory symptoms very similar to those produced by insular stimulation. Conversely, though dysarthria is considered to reflect frontal opercular discharges,50 we never observed this symptom in isolation when stimulating this region outside Broca’s area. Moreover, ictal dysarthria was associated with discharges in the nondominant hemisphere for language in the three patients whose insular seizures included this symptom, and it was reproduced as often in the right or left hemisphere by direct cortical stimulation. Somato-motor ictal manifestations differ from others in that they usually cannot be reproduced by insular stimulation and reflect seizure propagation outside the insular lobe. They have been considered as predictors of a bad outcome in
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VAC
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Figure 39.3 SEEG exploration of the insular lobe. A: Fusion of skull radiography and coronal MRI slice in the anterior commissure vertical plane at scale 1. This picture illustrates the positions and trajectories of the electrodes exploring the insular cortex (i1, i2, and i3) in an individual patient. The two deepest contacts of each electrode are located in the insular cortex. The more superficial contacts are located in the suprasylvian (i1) and infrasylvian opercular cortex (i2 and i3). (R: right, L: left). B: Plotting of the 144 insular contacts (yellow dots) in the 50 patients on a sagittal MRI slice of the insula. The borders of the insular lobe are drawn in red. Most of the insular surface has been explored except its most anterior part. The white lines represent the axis of the bicommissural stereotactic space of Talairach and Tournoux.97 AC-PC: anterior commissure-posterior commissure horizontal plane; VAC: vertical anterior commissure plane orthogonal to the AC-PC plane; VPC: vertical posterior commissure plane orthogonal to the AC-PC plane C: Functional mapping of the insula. This figure illustrates data from direct electrical stimulations of the insular cortex in the 50 patients of this study. In each of the six Ca to Cf insets all of the 144 stimulated points are plotted as black circles (see ref. 11 for details on stimulation procedure, safety and accuracy). The 138 responses evoked by electrical stimulations are represented according to the functional categories detailed in the results section. Ca: Somatosensory responses. Simple paresthesiae are represented in yellow, paresthesiae with warmth sensation in orange and painful paresthesiae in red. Cb: Viscero-sensitive responses are in blue, of which one was painful (in red). Cc: Sensations of laryngeal constriction are in green, of which two were painful (in red). Cd: Auditory responses (lilac). Ce: Dysarthric speech and missing words (cream white). Cf: Miscellaneous responses: Sensation of unreality (light blue); Olfacto-gustatory responses (orange); Vestibular responses (pink), Vegetative responses (purple). From Isnard et al. 2004 with permission.69 (See Color plates.)
temporal lobectomy and their occurrence makes questionable the diagnosis of TLE.51 Indeed such symptoms are exceptional in seizures originating in the mesial temporal lobe, while they occur at the end of nearly two-thirds of insular seizures. Thus, in patients whose ictal symptomatology is compatible with TL seizures, their occurrence during the development of the seizure strongly suggests a seizure onset in the insular lobe. Finally, 10% of the responses evoked by insular stimulation (Figure 39.3Cf) reproduce ictal manifestations that are only
occasionally observed in spontaneous insular seizures such as vegetative responses, feeling of unreality, olfacto-gustatory and visceral sensations. The insular origin of these rare symptoms is in agreement with the functional role of the insular lobe in the control of taste52–56 and visceral functions.31, 57 None of our patients with SEEG documented insular seizures reported vertigo or sensation of body tilting as part of their ictal symptomatology and insular stimulation exceptionally produced a vestibular sensation (3/139: 2.1%, purple points
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Insular epilepsy in Figure 39.3Cf). This finding contrasts with some observations where parieto-insular strokes manifested by such sensations.58–60 It is in line with cortical stimulation data by Penfield and Jasper37 and more recently by Kahane et al.61 showing that vestibular sensations are mostly observed after stimulation of the superior temporal neocortex and lateral aspect of the inferior parietal cortex.
cavernous angioma or a low grade tumor, is observed within the insula, invasive EEG investigations, based on clinical observation of ictal symptomatology, must be targeted to explore the whole extent of the suspected epileptogenic network in order to assess the exact role of the insula in seizure development. Three major types of epileptogenic networks involving the insula can be distinguished: ●
What, if anything, is an insular seizure? Based on the above detailed observations is it possible to add an ‘insular’ category to the list of epileptogenic zones that can be used as one of the dimensions of a patient-oriented epilepsy classification?62 In other words, is there any sequence of symptoms that are specific enough to locate the epileptogenic area in the insula and to predict that the removal of the insular cortex is necessary to make the patient seizure free? Even though SEEG-documented seizures are scarce an affirmative answer can be given to this question when, during spontaneous seizures, the patient experiences in full consciousness a symptomatic sequence made of a pharyngeal and/or laryngeal discomfort with thoracic oppression or dyspnea, unpleasant paresthesiae, warmth or pain sensation in the perioral region or spreading to a large somatic territory, followed by dysarthric or dysphonic speech and ending in focal somato-motor manifestations. Knowing that in patients illustrated in Figure 39.1, most of the antero superior quadrant of the insula has not been explored (see Figure 39.3), two variants can be distinguished according to whether the insular discharge originates from the anterior or posterior part of the insula. In rostral insular seizures viscero-motor and laryngeal symptoms are predominant (green frame in Figure 39.1), while in caudal insular seizures the ictal symptomatology is dominated by somato-sensory symptoms, which are all the more so specific that they affect a large, eventually bilateral, territory and manifest as a warm or painful sensation (red frame in Figure 39.1)! Thus most of the insular seizures can be described as a combination of vegetative and somatosensory auras according to the semiological seizure classification proposed by Lüders et al.63
The insula as a node in distributed epileptogenic networks As for any other types of partial seizures, the concept of a distributed epileptogenic network can be applied to describe insular seizures where the insular cortex is involved as a node, or as a relay in seizure propagation, and not as a single focus. This situation is likely to be more frequent than that where seizures remain confined to the insular cortex. The occurrence of a sequence of ictal symptoms reflecting the insular involvement at seizures clinical onset, as described above, proves effective to delineate the various clinical situations where epileptic discharges might originate in the insula. It must be reminded, however, that identification of these symptoms does not allow to firmly conclude on the insular origin of seizures, since they might as well follow the primary involvement of noninsular portions of a larger epileptogenic network where the seizure onset zone can keep clinically silent.64 Thus, apart from the situation where a clear-cut epileptogenic MRI lesion, such as a
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Temporo-perisylvian-insular networks that include the various brain regions bordering the sylvian fissure, i.e., the frontal, parietal and temporal operculum, together with the insula; Temporo-limbic-insular networks, which primarily involve the mesial temporal structures and/or the temporal pole; Mesial and orbito frontal-insular networks, in the context of the so-called nocturnal frontal lobe epilepsy.
This subdivision remains partly artificial, however, since some patients combine electro-clinical features that belong to at least two of these networks, as detailed below. Temporo-perisylvian-insular networks The concept of ‘perisylvian epilepsy’ was originally introduced by Munari et al.,50 in an attempt to distinguish this form of epilepsy from temporal lobe epilepsy proper. It should be noted, however, that in perisylvian the epileptogenic zone often encompasses the first temporal gyrus, accounting for the frequent presence of simple auditory hallucinations in this form of epilepsy, and explaining why the term ‘temporo-perisylvian’ is preferable to that of ‘perisylvian’. Apart from simple auditory hallucinations, temporo-perisylvian seizures are characterized by the presence of symptoms reflecting the involvement of the frontal and parietal operculum (hemifacial motor or somato-sensory symptoms, gustatory hallucinations, hypersalivation), the secondary somato-sensory area (various types of ipsilateral, contralateral or bilateral somatosensory symptoms), and the temporo-perisylvian vestibular cortex (vertigo).61 Part of the semiology initially ascribed to frontal or parietal opercular ictal discharges in the early study of Munari et al.,50 which did not benefit from the placement of depth electrodes within the insula, does in fact reflect the involvement of the insular cortex. One such example is that of gustatory hallucinations, previously thought to reflect a fronto-parietal opercular discharge,52 but that can be elicited by stimulating the insula rather than the opercular region.17 Furthermore, both the insular cortex and parietal opercular somato-sensory (SII) cortex can be responsible for similar ictal somato-sensory symptoms affecting large cutaneous territories, even though the somatotopic fields are much larger in the insula than in SII65 Finally, the tight anatomical connections and cytoarchitectonic continuum observed between the fronto-parietal and temporal perisylvian cortex on one hand, and the insula on the other, also militates for including all these brain regions within the temporo-perisylvian network that must be explored by SEEG recordings before surgery. For instance, in two of the patients presented in section II (#4 and #5), one of whom presented with a parietal cortical dysplasia (#4), the SEEG involvement of part of the
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opercular regions was judged important enough to lead to a surgical resection or a thermolesion of that structure together with the posterior insula, resulting in seizure control in both patients (class Ib of Engel). In another recent series,66 the role of the insula in a temporo-perisylvian epileptogenic network can be suspected in six patients in whom temporal lobe surgery was unsuccessful in controlling seizures despite intracranial EEG evidence that the temporal lobe participated in seizures genesis. In these patients a somato-sensory aura was interpreted as reflecting a discharge in the parietal lobe and the inferior parietal region was indeed also involved at ictal onset on intracranial EEG recordings, but its secondary removal did not result in better seizure control. The authors acknowledged that the insula might have participated to the complex epileptogenic network observed in their patients, inasmuch as one presented with an insular hyperperfusion on ictal SPECT. They could not confirm this hypothesis, however, due to the lack of intracerebral electrodes directly placed within the insula. Temporo-limbic-insular networks One major challenge in epilepsy surgery remains to understand the origin of postoperative seizure recurrence in a still significant proportion of operated patients, despite the presence of typical clinical and MRI features of mesial temporal lobe epilepsy. Part of these surgical failures might reflect the involvement of the insular cortex within a larger epileptogenic network encompassing the sclerotic mesial temporal structures.67 This issue is well illustrated by patient #6 in Figure 39.1, whose history has been further detailed in a recent review.68 Indeed, this patient fulfilled the major criteria used to define mTLE, including a rising and distressing epigastric sensation at seizure onset rapidly followed by oroalimentary automatisms, MRI signs of unilateral hippocampal sclerosis; ipsilateral temporo-limbic interictal FDG-PET hypometabolism, and an anterior temporal scalp-EEG ictal discharge. However, other ictal signs and symptoms suggested a rapid involvement of the perisylvian region, including early simple auditory hallucination and rapid occurrence of mastication and left face tonic contraction, leading to the decision of performing an invasive SEEG monitoring. The latter revealed that the patient suffered two seizure types, one arising from the sclerotic mesial temporal structures that secondarily propagated to the ipsilateral insula and opercular regions, and another arising from the posterior insula before invading the ipsilateral mesial temporal and opercular regions. Interestingly, the insular seizure type, but not that arising from the temporal lobe, selectively occurred during sleep. Resection of the epileptogenic temporal lobe controlled daytime seizures type for a few months only, whereas nocturnal seizures have continued unchanged. Overall, this case report illustrates the possibility of observing insular seizures in a patient with the major clinical and MRI features of mesial temporal lobe epilepsy, suggesting an epileptogenic zone encompassing the temporo-limbic regions and the insula. This patient also demonstrated an intense and rapid involvement of other temporo-perisylvian regions, suggesting that these different networks might be intermingled and overlapping in the same patient.
Other patients might present with comparable ictal semiology, EEG and neuroimaging data, and will eventually prove to have an epileptogenic zone limited to the temporo-limbic cortex. This alternative situation is illustrated by another patient from our series (#2 in Figure 39.1) whose intracerebral EEG recordings demonstrated a mesial temporal ictal discharge that invaded the insula very rapidly and intensively, suggesting that the insular cortex might be part of the epileptogenic zone.69 However, long-term seizure freedom was achieved after an anterior temporal lobectomy. More generally, seizures originating in the mesial temporal lobe are likely to propagate to the ipsilateral insula, though less rapidly and intensively than in the above patient, and this propagation70 does not preclude seizure freedom after temporal lobectomy. Several issues remained unsolved regarding the connections involved in the propagation of ictal discharges between the temporo-limbic system and the insula. Due to the frequent participation of the temporal pole at ictal onset,71 we prefer using the terminology ‘temporo-limbic’ rather than ‘mesial temporal’, knowing that part of this brain region is located outside the mesial aspect of the temporal lobe and is closely connected to the insula. In fact, according to Mesulam’s description of the paralimbic regions, two major belts should be considered, one including the orbito-frontal cortex, the temporal pole, and the insula, while the parahippocampal and cingulate gyrus form the other.33 Indeed, as already discussed, the insula has strong reciprocal connections with the temporal pole, but also with the entorhinal cortex and the amygdala. In addition, it projects to the anterior hippocampus but does not receive major direct afferents from this structure. It is yet unclear which of the above regions is predominantly involved in the insular propagation of temporo-limbic ictal discharge. Conversely, the posterior and anterior-inferior aspects of the insular cortex are predominantly involved in seizures propagating to the mesial temporal structures.68, 69 Mesial and orbital frontal-insular networks A recent issue concerns the role of the insula as a part of the epileptogenic network in fontal lobe epilepsies and, more precisely, in NFLE, which is is primarily characterized by seizures occurring exclusively or predominantly during sleep, the semiology of which suggests a frontal lobe origin, as for example nocturnal paroxysmal dystonia (NPD) or hypermotor seizures.72 An autosomal dominant inheritance (ADNFLE) is found in 8–43% of patients, and several mutated genes have been identified.72–76 However, many uncertainties persist regarding the neural networks underlying the cryptogenic and idiopathic forms of NFLE, inasmuch as very few patients have been investigated with intracranial EEG recordings.77, 78 We have recently reported three patients with a typical form of nocturnal hypermotor seizures suggesting cryptogenic NFLE in two, and autosomal dominant NFLE (ADNFLE) in another, whose ictal onset zone proved located in the anterosuperior portion of the insula.79 In the two patients presenting with a seemingly cryptogenic NFLE, intracerebral EEG recordings demonstrated a very focal interictal focus in that same region, consisting of frequent bursts of high frequency discharges and high amplitude spikes (Figure 39.4). In the ADNFLE patient, the epileptogenic zone appeared larger, extending to the frontal operculum.
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Figure 39.4 Intra-cerebral EEG investigation of a patient with a clinically-defined cryptogenic nocturnal frontal lobe epilepsy showing almost permanent high amplitude spikes (left EEG traces), and a high frequency discharge at ictal onset (right EEG traces) in the antero-superior portion of the left insula (i1,i2), slightly diffusing to the nearby deepest aspect of the frontal operculum (i3–4), but not to more lateral probes. Note that all leads are displayed with a similar amplification.
High frequency electrical stimulation of the antero-superior portion of the insula, but of no other region, could elicit a typical aura or full-blown seizure in two patients. However, because none of the three patients underwent epilepsy surgery, we cannot firmly conclude on the precise extent of their epileptogenic zone. Interestingly, these three patients represent 30% of all those with nocturnal hypermotor seizures and no MRI brain lesion who underwent an intracerebral EEG investigation in our study. Among the seven other patients, a mesial or anterior frontal seizure onset was demonstrated and resected, but three continued to suffer postoperative seizures. One might speculate on the role of the insula in these patients seizures, provided that it was not investigated during their intracerebral EEG recordings. Overall, an insular seizure onset zone might be responsible for a significant proportion of so-called cryptogenic NFLE, at least among those resistant to antiepileptic drugs. At the present time, no clear indicator other than intracerebral EEG recordings allows to distinguish these patients from those presenting NFLE proper. In fact, our patients with an anterosuperior insular ictal onset started their hyperkinetic behavior only when the mesial frontal cortex was invaded. The propensity for insular seizure to occur during sleep has not been previously reported. However, it is interesting to note
that this propensity was also observed in one of our patient with temporo-insular epilepsy (see previous section). The role of the insula in sleep physiology is not known, but recent functional neuroimaging studies have shown a marked deactivation of the anterior insula during sleep.80, 81 Overall, insular seizures might be associated with various types of ictal semiology, reflecting the subregion of the insular cortex primarily affected, as well as the related multilobar network: the posterior and antero-inferior aspect of the insula appears to be mostly involved in temporo-perisylvian and/or insulo-temporo-limbic epileptogenic networks mimicking the different forms of TLE; the antero-superior portion of the insula seems to play a more important role in the insulo-frontal networks mimicking NFLE. At the present time, there is no available data suggesting a primary role of the insular cortex in seizures originating from other brain areas than those listed above.
Etiology of insular epilepsy Lesional insular epilepsy The majority of cases reported in the literature as insular seizures or epilepsies derives from patients with an obvious
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epileptogenic brain lesion located in the insula, some of which were subsequently and successfully operated upon. 41,42,54, 69, 82,–85 These lesions primarily included low grade brain tumors, including gliomas and dysembryoplastic neuroepithelial tumors, cavernomas, and cortical dysplasia. However, all potentially epileptogenic brain lesions might be observed in the insula, such as stroke or encephalitis.86, 87 Cryptogenic and idiopathic epilepsy primarily involving the insula To our knowledge, the only published cases of cryptogenic epilepsy primarily involving the insula are those published by our group.68,69 They represent a very limited number of patients, none of whom underwent a surgical resection of their epileptogenic but MRI negative insula. No pathological data is thus available, but SEEG findings suggested the possibility of a MRI occult cortical dysplasia in a minority of patients. For instance, one of our patients with NFLE of insular origin presented an intracerebral SEEG pattern typical of an underlying cortical dysplasia, with very focal and permanent high amplitude spikes intermingled with bursts of high frequency discharges (Figure 39.4).79 In the same series, one who presented with a typical form of ADNFLE, but none of the known mutation of the α 4 and β 2 subunits of the nicotinic acetyl-choline receptor, should be considered to suffer an idiopathic form of partial insulo-opercular epilepsy, according to the familial inheritance of his epileptic disorder and the result of his SEEG investigation.79,88 To our knowledge, no other patient with ADNFLE has undergone an intracerebral EEG investigation, and we therefore ignore the proportion of such patients who might also demonstrate an insular epileptogenic zone.
Presurgical evaluation Noninvasive investigations EEG and MEG According to the deep location and specific gyral organisation of the insula, interictal or ictal epileptiform discharges originating in this lobe are unlikely to be detected by scalp-EEG recording, unless these discharges propagate to lateral neocortical regions. This has been shown in our first description of insular discharges70 and is also illustrated by Figure 39.4. Accordingly, neither interictal nor ictal scalp-EEG abnormality could be recorded in this patient, accounting for the fact that the epileptic origin of his seizure disorder has been strongly debated. However, scalp-EEG recordings might provide some clue regarding a temporo-perisylvian epileptogenic zone, indirectly reflecting the potential involvement of the insular cortex. In particular, both interictal and ictal EEG abnormalities will display a more widespread distribution over the infra- and suprasylvian elecrodes. To our knowledge, a single case report has assessed the diagnostic value of MEG in a patient with an insular epileptogenic DNET, and concluded that MEG could detect epileptiform abnormalities within the concealed insular cortex.82
Functional interictal neuroimaging In patients with typical TLE, [18F]FDG-PET and [11C] Flumazenil-PET studies have reported that interictal hypometabolism and decreased benzodiazepine receptor density observed in the temporal lobe could extend to the insula in some patients.89–92 At the present time, the presence of such insular abnormalities have not been clearly associated with a higher risk of postoperative seizure relapse, but this issue still needs to be addressed in larger populations. In the few well-documented cases of insular epilepsy, [18F]FDG-PET, [11C]Flumazenil-PET, and ictal SPECT did not demonstrate distinctive features from those encountered in TLE or NFLE, and in particular no clear cut insular abnormality.67,68 Finally, [18F]FDG-PET and ictal SPECT have shown abnormal findings in the insula of a few patients with uncertain epileptogenic zone, where one might speculate on the involvement of the insula.66,93,94 These include patients with nocturnal hypermotor seizures,93,94 as well as one patient with somato-sensory aura and a seemingly temporo-parietal ictal onset zone not controlled by surgery sparing the insula.66 Overall, whether functional imaging will eventually prove useful in the clinical assessment of insular epilepsy remains an open issue. Invasive investigations In the stereotactic implantation technique first described by Talairach and Bancaud,95 intracerebral electrodes are implanted perpendicular to the midsagittal plane using Talairach’s stereotactic grid and can be left in place chronically up to 15 days.96 The position of each contact can be plotted on the corresponding slice of the atlas of Talairach and Tournoux97 and by fusing the frontal skull radiography with the coronal MRI slice, both at scale 1/1, corresponding to the electrode trajectory (Figure 39.3a). Oblique electrode trajectories can be also useful to explore the insula.79 Interictal insular recordings The few available data from literature on interictal insular paroxysmal activities in surface or depth recordings were reported in the fifties.36, 98, 99 These early studies showed that spikes or spike-waves are recorded in the insula of nearly 50% of TLE patients. In SEEG recordings they are present in all patients with insular seizures. They are sporadic or intermittent in TLE and most often frequent in patients with insular seizures, particularly in those with focal dysplasia.91 Since the early study of Silfvenius et al.39 it has been acknowledged that their presence is not predictive of a poor outcome of temporal lobectomy in TLE, so that they do not indicate an insular epileptogenic zone. Spikes in the amygdala, hippocampus or temporal pole usually co-exist, and are most often asynchronous, with insular paroxysms. Contacts located in supra- or infrasylvian opercular cortex or adjacent amygdalo-hippocampal structures are often blind to insular paroxysms, which are thus unlikely to be recordable by subdural electrodes grids placed over the sylvian fissure or on the mesial surface of the temporal lobe (Figure 39.5).
Figure 39.5 SEEG recordings in patient 8 using three transopercular electrodes exploring the right insular lobe (cf Figure 39.3a). An abundant paroxysmal interictal activity made of subontinuous spikes and spike-waves is picked up by the insular contacts (A’, C’), to which which more superficial opercular contacts are blind. (i) MRI sagittal slice in the insular plane. (op) MRI sagittal slice in the opercular plane. A, B and C: postions of the insular contacts; A’, B’ and C’: positions of the opercular contacts.
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Figure 39.6 SEEG recording of an ictal discharge in patient 8 beginning in the insular cortex (Arrow 1) by a large spike-wave complex followed by a low voltage fast activity and a recruiting discharge of high frequency spikes and spike-wave affecting preferentially the posterior insula. This ictal spiking activity reaches the opercular cortex 8 seconds after the insular onset time (Arrow 2). This discharge spreads later on to the frontal (G, G’) and parietal (E, E’) ‘lobe, sparing the temporal lobe (D, D’).
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Insular epilepsy Ictal insular SEEG recordings In terms of onset site, propagation and morphology, the insular discharge patterns are very similar from one seizure to the other in a given patient, suggesting an individual organization of the insular epileptogenic neuronal network. They are made of a low voltage fast activity (LvFA) that may begin abruptly, or be preceded by changes in interictal activity. These preictal changes manifest by an increase in the frequency of spikes that become more regular or rhythmic and/or by the appearance of spikes and poly-spike-waves. Ictal LvFA can remain confined in the insula during several tens of seconds, or spread outside the insula in a few hundreds of milliseconds. During their intrainsular development LvFAs are not detectable by SEEG contacts located in neighbouring structures, in particular in the temporo-parieto-frontal opercular cortex, the activity of which is either unchanged or shows only rhythmic slow waves without sharp paroxysms during insular LvFA discharges (Figure 39.6). We have never observed an insular LvFA not spreading, either step by step to perisylvian cortical areas, or more abruptly at distance to ipsilateral amygdala, hippocampus or posterior mesial frontal cortex. Lastly, in two patients with a bilateral SEEG exploration we could observe that an insular LvFA can propagate to the contralateral insula. This anecdotal observation does not allow any conclusion as to the frequency of insular seizures bilateralization, but suggests that the insula is not only a possible relay for intrahemispheric propagation of focal seizures (see section III), but also a route for their interhemispheric transfer.
Treatment Based on electrocorticography, insular resections were attempted as early as the late forties to improve the surgical outcome of temporal lobectomy.36,39,98,99 This procedure has been abandoned because it proved to have a much greater morbidity than the usual temporal lobectomy alone without improving significantly the seizure control. Progress in surgical techniques now allows, with an acceptable risk level, the removal of focal epileptogenic lesions located in the insula, such as tumors42 and cavernous angiomas.100,101 The outcome in terms of seizures control is usually good,102 so that a lesionnectomy can be proposed, without presurgical invasive EEG recordings, whenever an insular lesion manifests clinically by seizures with insular ictal symptomatology, as in the case illustrated in Figure 39.2.
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Figure 39.7 Sagittal (1), coronal (2) and axial (3) control brain MR images after insular radio frequency thermo lesions using the SEEG electrodes contacts implanted in the epileptogenic areas of patient 5. This procedure was performed immediately before SEEG electrodes removal and thus did not entail the risk of additional electrodes implantation. These RM images acquired 15 days after this procedure show the thermo-lesions located at the insular onset site of seizures (A), and in the parietal opercular cortex (B), which was the first propagation relay of insular discharges.
Partial or subtotal resection of the insular cortex is also feasible in a patient without a space-occupying lesion (case 4 in Figure 39.1). However, this remains an aggressive procedure that necessitates the removal of part of the opercular parietofrontal or temporal cortex, and entails a lesional risk in the deep territory of the middle cerebral artery. In the absence of a lesion no tailored insular cortectomy can be undertaken without presurgical SEEG exploration of the entire cortical network suspected as epileptogenic (see the third main section), with recordings of several spontaneous seizures and insular stimulations. An alternative to cortectomy is represented by SEEG guided radio-frequency (RF) thermocoagulation.71 RF thermocoagulation is performed using adjacent contacts of SEEG electrodes in sites where discharges have been recorded. It produces focal lesions of 5–7 mm diameter with minimal risk (Figure 39.7). Two of the eight patients reported in this chapter (see the second main section) have benefited from RF thermocoagulation (# 5 and 8), with a follow up of 36 and 17 months, respectively. Both are free of disabling seizures (class Ib of Engel).
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Cingulate epilepsy E Garzon and HO Lüders
Introduction Between the 1940s and 1950s, studies on experimental animals and observations on human beings with destructive lesions led to the discovery of a possible relationship between the anterior portion of the cingulate gyrus (CG) and behavioral disorders. Those studies also led to the use of surgical ablation of the anterior portion of the CG or of cingulum disconnection for the treatment of severe behavioral illnesses. Many advances have been made in the last 20 years and, even if a clear understanding of all its connections and functions is still far in the future, the CG has been shown to be, indeed, a heterogeneous structure. Because of peculiarities of its vascular irrigation (the pericallosal artery and its branches irrigate the medial portion of the frontal lobe and part of the medial portion of the parietal lobe), ischemic or hemorrhagic lesions circumscribed to the CG are rare. Small tumors or malformative lesions relatively restricted to the CG are also uncommon. These facts limit our ability to study CG function based on lesional observations. Noninvasive neurophysiological studies provide only partial or inconclusive data because of the anatomical location of the CG (medial and distant from the cerebral surface, with significant portion of the CG buried in the depths of the pericallosal and cingulate sulci). This makes it difficult to define the ictal clinical manifestations of the CG as a symptomatogenic zone. The objective of the present chapter is to describe the clinical characteristics of epileptic seizures most probably originating in the CG. As an introduction a brief review of the cytoarchitecture, connections and functions of the CG of humans and experimental animals will be presented.
Cytoarchiteture Brodmann’s cytoarchitectural map of the cerebral cortex has been used as the standard for human brain research. The CG is divided into anterior and posterior parts (Figure 40.1). The anterior part consists of the perigenual portion, areas 25 and 33, and of the midcingulate portion, areas 24 and 32. The posterior cingulate consists of the posterior cingulate cortex, areas 23 and 31, of the retrosplenial portion, areas 29 and 30, and the ectosplenial portion, area 26. Areas 29, 30, and 26 are narrow and located in the isthmus of the CG.1 More recent cytoarchitecture studies have confirmed that an important part of the CG cortex is buried in the depth of the sulci (Figure 40.1). The anterior cingulate cortex (ACC) 334
is agranular, with a prominent Va layer. Not all the cortex of area 24 is exposed on the surface2 and histological differences exist between the caudal and rostral parts of area 24, which is, therefore, subdivided into 24a, 24b, 24c, and 24d.3 The main difference resides in the composition and thickness of layers Va and Vb.3 Area 24c lies primarily within the ventral bank of the cingulate sulcus.2 This area is called the cingulate motor cortex, since pyramidal Betz cells have been demonstrated in layer Va.4 Compared with the Betz cells of the primary motor field, those of the cingulate area display numerous primitive traits.5 In non-human primates, in addition to cytoarchitectural differences there are differences in inputs. While the rostral portion of area 24 receives substantial input from the amygdala, the caudal portion receives a large component of parietal lobe afferents.6 The posterior CG consists of the posterior cingulate cortex (PCC), areas 23 and 31, and the retrosplenial and ectosplenial areas 29, 30, and 26. Areas 29, 30, and 26 are buried in the depths of the pericallosal sulcus. Area 23 is located in the caudal portion of the CG and extends into the caudal part of the cingulate sulcus before it arches to form the marginal sulcus. The PCC is characterized by granular layers II and IV,2 except for area 30 whose layer IV is dysgranular.7 Area 23 is subdivided into 23a, 23b, 23c, and 23d as a function of the degree of differentiation of layer III and of the size and distribution of neurons of layers IV and Va.3
Connections The cingulate cortex is considered to be part of the limbic system and is also a component of the Papez circuit. Outputs from the amygdala, septal area, entorhinal cortex, and hippocampus travel via the fornix to the mammillary bodies of the hypothalamus; from there via the mammillothalamic tract, to the anterior thalamic nucleus (anteroventral subdivision); and via the thalamocortical fiber system to the CG, and then back to the hippocampus via the cingulum and entorhinal areas. This closed circuit of connections was described by Papez8 and became known as the Papez circuit. Studies in rhesus monkeys using retrograde tracer horseradish peroxidase have shown that both the ACC and the PCC receive thalamic inputs. Although each area of the CG receives inputs from distinct thalamic nuclei, the anterior thalamic nucleus (anteromedial subdivision) sends afferent fibers to areas 25, 24, and 23, thus forming a certain connectional link between all cingulate areas.9
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Cingulate epilepsy VCA
VCP
335
CS
6
7
9 8 12
CA-CP STG
Figure 40.1 Cingulate gyrus cytoarchitectural areas. Areas 24, 25, 23, and 31 are located on the mesial surface. Small portions of areas 24 and 23 are buried in the depth of the cingulate sulci. Areas 32, 33, 26, 29, and 30 are buried in the depth of the cingulate and pericallosal sulcus (ACG = anterior cingulate gyrus; PCG = posterior cingulate gyrus; CC = corpus callosum; CS = cingulate sulcus, MR = marginal ramus)
The ACC and PCC also receive a large contingent of afferents from the frontal lobe, especially the dorsolateral and orbital areas, and also from the parietal lobe. Most of the frontal cortical afferents reach area 24, whereas area 23 preferentially receives inputs from the parietal lobe.6 The ACC also receives afferents from the insula cortex and the PCC receives a small proportion of afferents from the occipital lobe, area 19.6 The CG also has extensive efferents connections. Studies on rhesus monkeys have shown that areas 23 and 24 have extensive and widespread projections to several regions of the cerebral cortex (Figure 40.2). Area 24 projects to the premotor region (areas 6 and 8), the orbito-frontal cortex (area 12), the rostral part of the inferior parietal lobe, the anterior insular cortex, the perirhinal cortex, and the laterobasal nucleus of the amygdala. Area 23, likewise, sends its connections to the dorsal prefrontal cortex (areas 9 and 10), the rostral orbital cortex (area 11), the parietotemporal cortex (posterior part of the inferior parietal lobule and the superior temporal sulcus), the parahippocampal gyrus, the retrosplenial region, and the presubiculum.10 The anterior cingulate cortex also sends projections to brainstem motor systems including the caudate, pontine, and red nuclei.11,12
Functions Structural lesions, surgical ablations, or functional alterations due to electrical stimulation of the CG in animals and humans shed some light on the function of the CG. These studies have been complemented by microelectrode recordings, and positron emission tomography in experimental animals and human beings. Changes in behavior can occur due to lesions in area 24, although in many of these reports on humans and experimental animals additional damage was also evident in the adjacent areas 6, 8, 9, 10, and 25 and in the corpus callosum. In monkeys, ablation of area 24 was marked by increased restlessness, hyperactivity, loss of their previous apprehension to certain aspects of their environment, apparent loss of fear, increased
24 CG
CC
23 RS PS
PHG
Figure 40.2 Cingulate gyrus simplified sketch showing efferent connections from areas 23 and 24 in the monkey’s brain (CC = corpus callosum; CG = cingulate gyrus; PHG = parahippocampal gyrus; PS = presubiculum; RS = retrosplenial area; STG = superior temporal gyrus).
tameness, and reduction of aggression.13 In animals with a longer survival time these changes tend to be reduced or to disappear. Behavioral changes such as indifference, docility, inappropriate urination, severe lack of attention, lack of social restraint, heightened sexuality, bulimia, and aggressiveness have also been reported to occur in humans as a consequence of unilateral14 or bilateral15 lesions in the anterior portion of the CG. Bilateral lesions of area 24 also cause the so-called anterior cingulate gyri syndrome which clinically manifests as apathy, akinesia, mutism, urinary incontinence, and indifference to pain.16 Structural lesions and studies of cortical stimulation have also correlated the anterior cingulate with autonomic phenomena such as piloerection,13 changes in blood pressure, tachycardia, mydriasis, and increased respiration frequency.17,18,19 The structural basis for involvement of area 25 in visceromotor activity is well known. Area 25 projects directly to the parasympathetic nucleus of the solitary tract,20 dorsal motor nucleus of the vagus, and to the sympathetic thoracic intermediolateral cell column.21 The anterior cingulate is also involved in the emotional aspects of pain perception.22,23 The ability of the anterior cingulate to participate in or execute motor functions has been studied extensively. The presence of Betz cells in area 24 supports the hypothesis of the possible existence of a motor area in the CG. In experimental animals the lower bank of the anterior cingulate sulcus is involved in self-initiated movements.24 There is also evidence
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that areas 24c and 23c send inputs to the motor and supplementary motor cortices in a somatotopic distribution.25 Additionally, there are reports that cortical stimulation of the ACC evokes motor responses in man.26–29 The nature of the responses obtained differ among the various studies, but include repetitive movements of the hands, fingers, and lips that can be classified as automatisms, tonic contractions involving the hands and arms, or an irresistible urge to grasp something. The posterior CG probably integrates visual information recognized in the visual cortex and an emotion-related substrate is processed in the anterior cingulate.30 Electrical activity of PCC is detected during eye movements in several species while assessing large visual field patterns. The activity is linked to the position of the eye in the orbit and the direction and amplitude of saccadic eye movements.31–33 Several observations have suggested that the PCC contributes to orientation of the animal in the environment and to spatial memory. Lesions of the posterior cingulate disrupt a rat’s ability to swim to a hidden platform.34 The observation of the deficits due to lesion of the retrosplenial region of rats has led to the assumption that the damage may disrupt the integration and transmission of both movement-related information and visuospatial information from cortex to hippocampal formation. The hypothesis is that the retrosplenial region is important not for memory of landmarks or other visuospatial cues, but rather the functional role of this region may be to purposefully organize the movements with respect to surrounding visual landmarks.35
Cingulate seizures Overview The semiologic characterization of epileptic seizures originating in the CG cortex is a challenge in epileptology. As mentioned before, the anatomical location of the CG makes neurophysiological studies with scalp electrodes difficult. Similar problems are encountered with invasive neurophysiological recordings. The presence of large caliber blood vessels on the medial surface of the brain and the fact that a considerable proportion of the cortex is located inside sulci make invasive evaluation of this area difficult. Ideal cases for the study of ictal clinical manifestations would be small medial epileptogenic lesions practically limited to the CG. These cases are relatively rare and literature data are limited to case reports or relatively small series. Thus, the semiologic aspects of the epileptic seizures of this region are still poorly defined. Most cases in the literature do not provide direct evidence that the epileptogenic zone was in the CG or actually limited to the CG. The gold standard would be cases in which a resection of an epileptogenic zone limited to the CG renders the patient free. Such cases do not exist in the current literature. Therefore, the following review of the literature refers to cases in which the lesion was mainly in the CG, even if there was no direct proof that the seizures originated from the CG, i.e., patients were not necessarily seizure free after surgery and/or the surgery was not limited to the cingulated gyrus. Although auras are considered rare,36 autonomic symptoms such as tachycardia, mydriasis, and changes in respiratory frequency are considerate common.37 Other descriptions are sensation of fear, dizziness,37 and painful sensations.38
In general, reports in the literature tend to stress that seizures originating from the cingualte gyrus are frequent, brief, nocturnal and do not include significant preictal or postictal alterations.36 The ictal semiology that has been related to the anterior cingulate is relatively varied. Some ictal manifestations like complex automatisms, laughter, and altered level of attention or consciousness have been described more frequently. Table 40.1 summarizes literature cases with seizures originating in the anterior portion of the cingulate, as confirmed by scalp video-EEG evaluation and/or invasive recording in lesional and non-lesional cases. Complex gestural movements,36–40 laughter,36,38,39,41 tonic contraction,36 lapses of attention, blinking, and oroalimentary automatism40 were the most common clinical manifestations. For comparative purposes, on the basis of described data, we reclassified the seizures according to the semiological seizure classification (Table 40.1).42 The most frequent types of epileptic seizures reported as originating from the anterior portion of the CG were bilateral asymmetric tonic seizures, gelastic seizures, hypermotor seizures, and complex motor seizures. In two cases the seizures were preceded by a somatosensory and autonomic aura respectively. In one case an autonomic seizure was documented (mydriasis). Dialeptic seizures were reported in only one report. This patient by history had atonic and complex motor seizures, but dialeptic seizures were documented during evaluation by video-EEG.40 Stimulation with depth electrodes have shown that continuous movements may be elicited by electrical stimulation of the anterior region of the CG. These movements were classified as automatisms and primarily involved the fingers, hands, lips, and tongue. The movements were ‘primitive’ and simple such as touching, leaning, rubbing, stretching, or sucking. The movements were frequently integrated with more complex movements that were adapted to the situation and thus represent, as a whole, what the authors called ‘types of behavior’.19,26 Cleveland clinic series In an attempt to better define the semiology of seizures originating from the CG, we reviewed the Cleveland Clinic Epilepsy database. To analyze the semiology and the electroencephalographic findings of seizures originating from the CG, patients of any age range evaluated by video-EEG and with symptomatic focal epilepsy secondary to a single structural lesion identifiable by magnetic resonance and localized in the CG, anterior, or posterior region were selected. No attempt was made here to define if the observed ictal semiology was due to direct activation of the CG (symptomatogenic zone in the CG) or due to spread an activation of extra-CG symptomatogenic areas such as, for example, the adjacent supplementary sensory-motor area. Only cases in which at least 90% of the lesion was located in the CG were included. Patients with extensive lesions with a small proportion in the CG or with extensive lesions widely involving the CG and adjacent regions as also non-lesional cases were excluded. Of patients evaluated between 1990 and 2005 who had received a diagnosis or a diagnosis of probable cingulate epilepsy, 76 were selected. The clinical data and the
Type
Case report
Case report
Review and 2 cases description
Chassagnon et al., 200338
McConachie & King, 199739
Devinsky et al., 199536
Laughter, repetition of the phrase ‘Oh my God’, small repetitive neck and trunk flexion, and bilateral arm extension, repeated touching of the forehead and mouth. Amnestic for the seizures
Grotesque facial contortions (tongue thrusting, a strangulated yell), neck and trunk flexion, bilateral arm and leg extension with side-to-side thrashing and occasional progression to a generalized tonic-clonic seizure Consciousness preserved
Male 28yrs
Male 29yrs
1. Sudden inappropriate laughter and kicking movements of the lower limbs. 2. Screaming, falling to the ground, holding his right arm in the air, thrashing his other limbs and wetting himself.
90% and one had 75% in 6/19 patients (31%) with complete disappearance in one. The authors assumed they had, at times, spectacular results in the cryptogenic LGS, with no clinical or EEG evidence of focalization, which contrasts with the results obtained by other authors. They also mentioned improvement in awareness and alertness, not attributable to changes in antiepileptic medication. In one patient, a new seizure type occurred after surgery, consisting of nocturnal focal adversive and clonic seizures. These data are consistent with the data reported by Spencer et al.27,28 on the occurrence of more intense focal seizures after callosal section. In the same way Spencer et al.29 have analyzed the EEG ictal patterns before and after CC, showing that the bilateral synchronous pattern was replaced by a unilateral or a focal onset, and that seizures newly localized to a lobe could occur, mainly in the frontal, sometimes in the parietooccipital lobe. Quattrini et al.30 observed the same changes in the postoperative ictal discharges. They also observed that after certain time, generally some months, lateralized discharges tend to generalize again, confirming that CC is replaced in discharge diffusion by other structures (brainstem, diencephalon). Ritter et al.31 reported 27 patients with LGS who underwent CC (19 complete, eight partial anterior). The selection criterion was the presence of drop attacks or frequent secondary generalized tonic-clonic seizures. Duration of follow up was 2–18 months (median 6 months). Overall, 70% of the patients had marked improvement in seizure control: tonic seizures decreased in frequency >80% in 14 of 23 patients (60%); GTC in nine of 15 (60%); atonic in seven of eight (87%), and seizures associated with dropping in 13 of 21 (61%). Repeated episodes of status epilepticus ceased in three of four patients. Provinciali et al.32 reported on the neuropsychological changes after partial CC in 15 patients with SGE, of which five were LGS. They tested memory, attention, visuo-motor ability, posture, motor dexterity, language, praxis and gnosis, as well as social behavior, one month before surgery, then 15–20 and 90–100 days postoperatively, without modifying the medical treatment. The short-term neuropsychological cost of this procedure appears to be low and seems to depend mostly on surgical parameters and brain conditions before the operation.
Nakatani et al.33 and Sakaki et al.34 reported respectively four and two patients operated upon in Japan with a satisfactory result with respect to the seizures for all, in spite of a disconnection syndrome in three patients, transient in one and lasting in two. Gates 35 reviewed three series of CC, including 17, one and five patients with LGS in the respective series. Among them 15 achieved a satisfactory outcome. Gates reported that the presence of bilateral independent foci with capacity for secondary generalization was an indicator of good outcome. Pinard et al.36 had operated on 34 patients with more than three seizures a day, among whom eight patients were diagnosed as having LGS. Patients were followed prospectively for at least 2 years after anterior CC (19 patients) and for 1 year after complete CC (15 patients). The eight patients with cryptogenic LGS improved after anterior CC. Septien et al.37 emphasized the good results obtained in children with psychiatric problems. They had performed partial anterior CC in two children with LGS and major psychiatric troubles: frontal syndrome with hyperkinesia, distractibility, aggressiveness, alexithymia, loss of planning abilities. They observed a progressive improvement of this frontal syndrome during the 2 postoperative months, with the possibility of learning new skills, without a change in IQ. Associative functions depending on the posterior third of the corpus callosum were preserved. They thought this improvement was related to the reduction of seizures. Claverie and Rougier38 studied the outcome in terms of quality of life in 20 patients submitted to CC for intractable epilepsy, including three cases of LGS. In two of these three they observed a substantial change; they became capable of independent living, and one attended a specialized school. In the whole series it appeared that the psychosocial benefits obtained in 40% of the patients were linked not only to the seizure reduction but also to the precocity of the intervention. Matsuzaka et al.39 studied 22 consecutive patients who underwent an anterior CC for intractable epilepsy. Seventeen of these patients had SGE, of whom eight had LGS. A crosscorrelation analysis and measurements of amplitude differences were performed between bilateral homologous regions pre-and postoperatively. The surgical outcome was excellent in 14 (63.6%), including a complete elimination of seizures in four; good in three (13.6%); and poor in five (22.7%) patients. After surgery, interictal generalized synchronous SW bursts in the SGE patients were disrupted and changed to unilateral SWs in 11 patients and to bilaterally independent SWs in six. The unilateral group had better surgical outcome than the bilateral independent group. Preoperatively the first group had significantly lower interhemispheric synchrony and fewer regional changes in the side leading in time and the side dominant for amplitude, suggesting unilaterally predominant epileptogenesis that triggered the secondary bilateral synchrony. These findings lead to the hypothesis that a considerable range of variation exists in the underlying condition of epileptogenesis in each hemisphere, even in SGE, affecting the postoperative EEG changes and surgical outcome. Preoperative quantitative EEG analyses enabled the authors to predict the underlying conditions of epileptogenesis and the surgical outcome. Unfortunately the authors were not precise in indicating to which group the patients with LGS belonged.
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The Lennox–Gastaut syndrome: a surgically remediable epilepsy? Kwan et al.40 analyzed findings and acute changes in electrocorticograms (EcoG) obtained during CC, in order to identify any relationships with the postoperative outcome of seizure activity, in 48 patients with LGS, all followed postoperatively for more than 4 years. Of these patients, 31 (64.6%) had significant improvement in seizure control. EcoG displayed bisynchronous discharges in 79.2% of the 48 patients, and they were blocked during CC in 69.7%, who achieved the best postoperative outcomes. But the difference did not reach statistical significance. Therefore, the changes in preoperative EcoG are not predictive. The largest series was reported by Cukiert et al.41 who performed one-stage callosal section, leaving only the splenium intact, in 76 patients with Lennox–Gastaut (n = 28) and Lennox-like (n = 48) syndromes. However, the latter is not defined by the authors. All patients were severely mentally impaired. Mean follow-up time was 4.7 years. Worthwhile improvement (>50%) was noted in 69 patients, with 90% or more seizure reduction in 52, 100% in seven. As in other series, the drop attacks were the most responsive seizure type (92%), followed by atypical absences (82%), tonic-clonic (57%), and tonic (51%) seizures. Postoperative EEGs were obtained in 56 patients. In 42 they showed complete disruption of secondary bilateral synchrony, in six only partial disruption, in eight no change. But a postoperative acute callosal disconnection syndrome appears in 72 patients (apathy, urinary incontinence, right hemineglect, low verbal input, one mutism) which lasted for 8–50 days. After this period, the attention abilities were substantially improved. Interestingly, in two patients who had LGS with reflex seizures these seizures were reduced by 60% in one (startle epilepsy) and disappeared in the second (tap epilepsy), unfortunately with a relapse after one year in the latter.42 In all series, postoperative complications and side-effects were rare. When it appears, the disconnection syndrome is transient. All the authors underline that in children CC is usually followed by an evident improvement in psychomotor development and behavior, though it is not measurable by usual assessment methods.35,37,38 At the end of this brief and incomplete survey, it appears that a number of patients with LGS can really improve with a partial anterior CC. In any case it is not a curative but a palliative treatment which can control the most ominous seizures represented by the drop attacks, mainly tonic in nature in this syndrome. Few papers give data on long-term results (more than 5 years’ follow-up) but it is never mentioned that good results were transitory. Spencer et al.26 followed patients postoperatively from 2–7 years. They indicate that ‘the stability of generalized seizure control after CC continues over many years of follow up’. The problem is not knowing the factors which could allow predicting the result of this intervention. Most authors reported better outcome in patients with a lateralized lesion or lateralized EEG anomalies, but in one series43 some cryptogenic LGS without asymmetry have been improved. Nevertheless, it is important to conduct a good preoperative EEG analysis in order to detect the type of electrogenesis in each hemisphere. The presence of a mental deficit is not a contraindication. Neuropsychological consequences are usually rare after partial section. It is recommended to perform surgery before the age of 10, in order to preserve a good intellectual outcome and to restore a good quality of life.
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Vagus nerve stimulation In the numerous publications studying the effects of VNS on epilepsy, the patients with LGS were often included in series of patients with ‘refractory’ or ‘intractable’ seizures, or with a low IQ. Few details were provided by the authors. The effect of VNS was evaluated at different times after surgery and was variable, from 50% and more seizure reduction in few patients44, 45 up to more than 90% seizure reduction.46,47 Most of the authors also indicate some degree of improvement in behavior, such as alertness and social communication. The side-effects were never disabling, consisting of change in the voice, hoarseness, sometimes coughing, at the time of the stimulation, and usually persisted only for some weeks. From the year 2000, LGS patients have been reported as a group and the conclusions are also variable. Moreover, the criteria for diagnosing LGS often lack and these groups include also cases designated as Lennox-like syndromes. The best study of VNS in patients with LGS was published by Majoie et al.,48 who gave the results of this procedure in 16 patients, aged from 7–18 years, accurately analyzed in terms of seizure and epilepsy type, frequency of the different seizure types, cognitive functions, quality of life and cost-effectiveness. This prospective, longitudinal cohort study included 16 ‘Lennox-like’ patients, among whom 12 with LGS, three with myoclonic astatic epilepsy, and one with myoclonic absences, followed from 6–12 months. The overall results showed that 25% of the patients had a reduction of seizures of 50% or more, with a mean for the individual patient of approximately 20–30%. No patient was completely seizure free. There were no significant differences between the various seizure types and for patients with drop attacks (n = 10) only one was seizure free and one had more than 50% reduction. The effects were moderate on neuropsychological functioning, a slight improvement appearing in the group with the highest mental age and not correlated with the seizure frequency reduction. The effects on EEG were not studied, but the best results were obtained in the patients with the best EEG background activity. The side-effects were low and transitory. The costeffectiveness analysis showed a decrease of 2876.06 € in the postoperative period of 6 months (1 € was approximately equivalent to 1 $). The same authors reported the results after a 2-year follow-up,49 which were substantially the same with persistence of the seizure reduction rate at the same level and no more improvement in the neuropsychological functioning. Frost et al.50 reported a multicentric retrospective study of 50 LGS patients, aged from 5 to 27 years (median = 13 years), 42% younger than 12. Data were gathered at 1, 3, and 6 months after implantation. They had multiple seizure types, 66% presenting with drop attacks. At 3 months, data were available for 43 patients. Seizures had decreased by >75% in 15 (35%), and by =50% in 24 (56%), and they have increased by >50% in 3. After 6 months, data were available for 24 patients (due to the data collection cutoff point). Seizures had decreased by >75% in 9 (38%) and by =50% in 14 (58%), and no increase was reported. No patient was seizure free. According to the authors, drop attacks and atypical absences seemed to equally respond, but it was difficult to affirm that, since there was no prolonged video recording. They also mentioned an improvement in quality of life, which requires further studies because the scales they applied were very simple. The side-effects were similar to those in previous studies, but
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hypersalivation and worsened behavior and hyperactivity were also noted in respectively 4 and 3 patients. Buoni et al 51 reported a series of 13 patients, 7 with LGS of whom 6 with atonic seizures. Three had a 50% or more seizure frequency reduction, mainly for atonic seizures, which the authors considered one good responsive seizure type, in contrast with the results by Majoie et al.48 However, their sample is small and atonic seizures are not always responsible for falls (drop attacks). Data about the effectiveness of VNS in LGS as regards other epilepsy types are unclear. Some authors 46 found a high rate of seizure reduction (from more than 50% up to more than 90%) and others seem to indicate that it is equivalent48 or lower. Labar, 52 in a survey of 269 patients with 1-year follow-up, concluded that VNS responsiveness was associated with older age, longer duration epilepsy and syndromes other than LGS. As for CC, up to now there are no outcome predictive factors allowing the selection of patients with a good chance of improvment by VNS. Janszky et al.53 conducted a study in 47 patients, with long-term ictal and interictal EEG recordings, with a 1-year follow-up. Only four patients had a symptomatic generalized epilepsy. They concluded that only two factors were predictive for a complete control of the seizures, the presence of a cortical dysplasia and the absence of bilateral interictal epileptiform discharges, the latter independently. These preliminary results would be rather discouraging for LGS patients. Another group54 also attempted to find prognostic electroclinical features and studied seizure patterns in 17 patients, mainly with focal epilepsies (16 with falls) and including four LGS patients. Only four patients had a significant seizure reduction, a better outcome occurring in those seizures with a temporal lobe onset, and the poorest outcome occurring in frontal and fronto-central seizures. In the LGS patients there were no significant improvement, except a diminution of retropulsive falls.
Conclusion In conclusion, one must underline that none of the published patients treated by VNS for a LGS has been completely seizure free, even if one seizure type could have disappeared in few of them (atonic seizures).51 For this reason, the choice between the two types of palliative surgery, CC and VNS, should be discussed case by case. It is known that a real improvement in quality of life is obtained only in patients who become seizure free and not in patients with a seizure frequency reduction 90% reduction in seizures is used.8 Difficulties arise when a Class III ‘worthwhile’ outcome is not specified either in number of seizures or percentage reduction from baseline. The substantial reduction group would also include the Duke ‘Significantly Improved’ outcome of 99% >99% 80% >99% 80% 75% >99%
89% 100% 90% >90%
Specifity
Contralateral Contralateral Contralateral Contralateral
Hemisphere of the epileptogenic zone
Localized somatosensory aura Hemifield visual aura Focal tonic/clonic activity Forced head version lateral parieto-occipital More likely occipital or temporal, but all lobes possible Basal temporal, TPO junction Basal temporal, occipito-temporal
Occipital, temporal Occipital, parietal, posterior temporal All lobes
If lateralized, contralateral
Temporal, parietal, occipital
No
More likely Heschl’s gyrus More likely auditory association cortex All lobes, more frequently temporoparietal Amygdala, insula Insula, mesial temporal
Temporal Frontal, temporal Temporal Parietal, temporal, frontal
If lateralized, contralateral
Frontal, insular, mesial temporal Temporal, insular
No If lateralized contralateral
Insula Insula, anterior cingulate, SSMA, amygdala, hippocampus, hypothalamus Insula Insula, mesial temporal, mesial frontal
Insular Temporal, (orbito-) frontal, insular
No No
Temporal, insular All lobes, most often temporal
More often ND Right, if associated with vomiting
Amygdala, hippocampus, mesial frontal Temporal Mesial > lateral temporal Lateral temporal, TPO junction TPO junction
(Mesial) temporal or frontal
No
Temporal Temporal Temporal, parietal Temporal, parietal
More often ND More often ND No No
All lobes
No
More often mesial frontal or post. temp.
No
More often frontal or temporal, but all lobes possible SS II, SSMA
More often ND
More often ND
Abbreviations: SS I: primary somatosensory area, SS II: second somatosensory area, SSMA: supplementary sensorimotor area, TPO: temporoparieto-occipital, ND: nondominant hemisphere
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Auras: localizing and lateralizing value
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Jackson JH. A study of convulsions. Transactions of the St. Andrews Medical Graduates’ Association 1869;162–204. Horsley V. Brain surgery. BMJ 1886;2:670–5. Cushing H. A note upon the faradic stimulation of the post-central gyrus in conscious patients. Brain 1909;32:44–53. Förster O. Sensible corticale Felder. In: Bumke O, Förster O, eds. Handbuch der Neurologie, Vol. 6. Berlin: Springer-Verlag, 1936:358–62. Penfield W, Jasper H. Epilepsy and the Functional Anatomy of the Human Brain. Boston: Little, Brown, 1954. Penfield W, Faulk ME. The insula: further observations on its function. Brain 1955;78:445–70. Penfield W, Perot P. The brain’s record of auditory and visual experience. A final summary and discussion. Brain 1963;86:595–696. Lüders HO, Awad I. Conceptual considerations. In: Lüders H, ed. Epilepsy Surgery. New York: Raven Press, 1991;51–62. Cooper R, Winter AL, Crow HJ, Walter WG. Comparison of subcortical, cortical and scalp activity using chronically indwelling electrodes in man. Electroencephalogr Clin Neurophysiol 1965;18:217–28. Gloor P. Neuronal generators and the problem of localization in electroencephalography: applications of volume conductor theory to electroencephalography. J Clin Neurophysiol 1985;2(4):327–54. Devinsky O, Kelley K, Porter RJ, Theodore WH. Clinical and electroencephalographic features of simple partial seizures. Neurology 1988;38(9):1347–52. Bare MA, Burnstine TH, Fisher RS et al. EEG changes during simple partial seizures. Epilepsia 1994;35:715–20. Lüders HO. Symptomatogenic areas and electrical cortical stimulation. In: Lüders HO, Noachtar S, eds. Epileptic Seizures: Pathophysiology and Clinical Semiology. Philadelphia: Churchill Livingstone, 2000;131–40. Fish DR, Gloor P, Quesney FL, Olivier A. Clinical reponses to electrical brain stimulation of the temporal and frontal lobes in patients with epilepsy. Pathophysiological implications. Brain 1993;116: 397–414. Gloor P. Experiential phenomena of temporal lobe epilepsy. Facts and hypotheses. Brain 1990;113:1673–94. Mesulam MM. Large-scale neurocognitive networks and distributed processing for attention, language, and memory. Ann Neurol 1990;28(5):597–613. Fuster JM. The cognit: a network model of cortical representation. Int J Psychophysiology 2006;60(2):125–32. Schulz R, Lüders HO, Tuxhorn I et al. Localization of epileptic auras induced on stimulation by subdural electrodes. Epilepsia 1997;38(12):1321–9. Bernier GP, Richer F, Giard N et al. Electrical stimulation of the human brain in epilepsy. Epilepsia 1990;31(5):513–20. Wieser HG, Bancaud J, Talairach J, Bonis A, Szikla G. Comparative value of spontaneous and electrically induced seizures in establishing the lateralization of temporal seizures. Epilepsia 1979;20(1):47–59. Palmini A, Gloor P. The localizing value of auras in partial seizures: a prospective and retrospective study. Neurology 1992;42:801–8. Boesebeck F, Schulz R, May T, Ebner A. Lateralizing semiology predicts the seizure outcome after epilepsy surgery in the posterior cortex. Brain 2002;125:2320–31. Lüders H, Acharya J, Baumgartner C et al. Semiological seizure classification. Epilepsia 1998;39:1006–13. Ajmone-Marsan C, Goldhammer L. Clinical ictal patterns and electrographic data in cases of parietal seizures of frontal-centralparietal origin. In: Brazier M, ed. Epilepsy: Its Phenomena in Man. New York: Academic Press 1973;235–58. Mauguiere F, Courjon J. Somatosensory epilepsy: a review of 127 cases. Brain 1978;101:307–32. Brodmann K. Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues. Leipzig: Barth, 1909. Nii Y, Uematsu S, Lesser RP, Gordon B. Does the central sulcus divide motor and sensory functions? Cortical mapping of human hand areas as revealed by electrical stimulation through subdural grid electrodes. Neurology 1996;46(2):360–7. Uematsu S, Lesser R, Fisher RS et al. Motor and sensory cortex in humans: topography studied with chronic subdural stimulation. Neurosurgery 1992;31(1):59–71; discussion 71–2. Mazzola L, Isnard J, Mauguiere F. Somatosensory and pain responses to stimulation of the second somatosensory area (SII) in humans. A comparison with SI and insular responses. Cerebral Cortex 2006;16(7):960–8.
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Lüders H, Lesser RP, Dinner DS et al. The second sensory area in humans: evoked potential and electrical stimulation studies. Ann Neurol 1985;(2):177–84. Lim SH, Dinner DS, Pillay PK et al. Functional anatomy of the human supplementary sensorimotor area: results of extraoperative electrical stimulation. Electroencephalogr Clin Neurophysiol 1994;91(3):179–93. Manford M, Fish DR, Shorvon SD. An analysis of clinical seizure patterns and their localizing value in frontal and temporal lobe epilepsies. Brain 1996;119:17–40. Salanova V, Andermann F, Rasmussen T, Olivier A, Quesney LF. Parietal lobe epilepsy. Clinical manifestations and outcome in 82 patients treated surgically between 1929 and 1988. Brain 1995;118:607–27. Blume WT, Jones DC, Young GB, Girvin JP, McLachlan RS. Seizures involving secondary sensory and related areas. Brain 1992;115:1509–20. Isnard J, Guenot M, Sindou M, Mauguiere F. Clinical manifestations of insular lobe seizures: a stereo-electroencephalographic study. Epilepsia 2004;45(9):1079–90. Tuxhorn IE. Somatosensory auras in focal epilepsy: a clinical, video-EEG and MRI study. Seizure 2005;14(4):262–8. Erickson JC, Clapp LE, Ford G, Jabbari B. Somatosensory auras in refractory temporal lobe epilepsy. Epilepsia 2006;47(1):202–6. Nair D, Najm I, Bulacio J, Lüders H. Painful auras in focal epilepsy. Neurology 2001;57:700–2. Young GB, Blume WT. Painful epileptic seizures. Brain 1983;106:537–54. Siegel AM, Williamson PD, Roberts DW, Thadani VM, Darcey TM. Localized pain associated with seizures originating in the parietal lobe. Epilepsia 1999;845–55. Sveinbjornsdottir S, Duncan JS. Parietal and occipital lobe epilepsy: a review. Epilepsia 1993;34(3):493–521. Erratum in: Epilepsia 1994;35(2):467. Kahane P, Hoffmann D, Minotti L, Berthoz A. Reappraisal of the human vestibular cortex by cortical electrical stimulation study. Ann Neurol 2003;54(5):615–24. Holtzmann RN. Sensations of ocular movement in seizures originating in occipital lobe. Neurology 1977;27:554–6. Kofman O, Tasker R. Ipsilateral and focal inhibitory seizures. Neurology 1967;17:1082–6. Horrax G, Putnam DJ. Distortions of the visual fields in cases of brain tumors: the field defects and hallucinations produced by tumors of the occipital lobe. Brain 1932;55:499–523. Richer F, Martinez M, Cohen H, Saint-Hilaire JM. Visual motion perception from stimulation of the human medial parieto-occipital cortex. Exp Brain Res 1991;87(3):649–52. Laff R, Mesad S, Devinski O. Epileptic kinetopsia: ictal illusory motion perception. Neurology 2003;61(9):1262–4. Ludwig BI, Ajmone-Marsan C. Clinical ictal patterns in epileptic patients with occipital electroencephalographic foci. Neurology 1975;25(5):463–71. Blanke O, Landis T, Seeck M. Electrical cortical stimulation of the human prefrontal cortex evokes complex visual hallucinations. Epilepsy Behav 2000;1(5):356–61. Beauvais K, Biraben A, Seigneuret E, Saikali S, Scarabin JM. Subjective signs in premotor epilepsy: confirmation by stereo-electroencephalography. Epileptic Disord 2005;7(4):347–54. Blume WT, Wiebe S, Tapsell LM. Occipital epilepsy: lateral vs mesial. Brain 2005;128:1209–25. Bien CG, Benninger FO, Urbach H et al. Localizing value of epileptic visual auras. Brain 2000;123:244–53. Salanova V, Andermann F, Olivier A, Rasmussen T, Quesney LF. Occipital lobe epilepsy: electroclinical manifestations, electrocorticography, cortical stimulation and outcome in 42 patients treated between 1930 and 1991. Brain 1992;115:1655–80. Russell WR. Whitty CW. Studies in traumatic epilepsy. 3. Visual fits. J Neurol Neurosurg Psychiatry 1955;18(2):79–96. Cohen L, Gray F, Meyrignac C, Dehaene S, Degos JD. Selective deficit of visual size perception: two cases of hemimicropsia. J Neurol Neurosurg Psychiatry 1994;57(1):73–8. Muller T, Buttner T, Kuhn W, Heinz A, Przuntek H. Palinopsia as sensory epileptic phenomenon. Acta Neurol Scand 1995;91(6): 433–6. Meadows JC, Munro SS. Palinopsia. J Neurol Neurosurg Psychiatry 1977;40(1):5–8. Mullan S, Penfield W. Illusions of comparative interpretation and emotion. Arch Neurol Psychiatry 1959;81:269–84.
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Textbook of epilepsy surgery Celesia GG. Organization of auditory cortical areas in man. Brain 1976;99(3):403–14. De Graaf JB, Liégeois-Chauvel C, Vignal J-P, Chauvel P. Electrical stimulation of the auditory cortex. In: Lüders HO, Noachtar S, eds. Epileptic Seizures: Pathophysiology and Clinical Semiology. Philadelphia: Churchill Livingstone, 2000:228–36. Foldvary N, Acharya V, Lüders HO. Auditory auras. In: Lüders HO, Noachtar S, eds. Epileptic Seizures: Pathophysiology and Clinical Semiology. Philadelphia: Churchill Livingstone, 2000: 304–12. Smith BH. Vestibular disturbances in epilepsy. Neurology 1960;10: 465–9. Lobel E, Kleine JF, Bihan DL, Leroy-Willig A, Berthoz A. Functional MRI of galvanic vestibular stimulation. J Neurophysiol 1998;80: 2699–709. Kahane P, Hoffmann D, Minotti L, Berthoz A. Reappraisal of the human vestibular cortex by cortical electrical stimulation study. Ann Neurol 2003;54(5):615–24. Brandt T, Dieterich M. The vestibular cortex. Its locations, functions, and disorders. Ann NY Acad Sci 1999;871:293–312. Kluge M, Beyenburg S, Fernandez G, Elger CE. Epileptic vertigo: evidence for vestibular representation in human frontal cortex. Neurology 2000;55:1906–8. Acharya V, Acharya J, Lüders H. Olfactory epileptic auras. Neurology 1998;51:56–60. Fried I, Spencer DD, Spencer SS. The anatomy of epileptic auras: focal pathology and surgical outcome. J Neurosurg 1995;83(1): 60–6. Jasper HH, Rasmussen T. Studies of clinical and electrical reponses to deep temporal stimulation in man with some considerations of functional anatomy. Res Publ Assoc Res Nerv Ment Dis 1958;36:316–34. Bancaud J, Talairach J. Clinical semiology of frontal lobe seizures. Adv Neurol 1992;57:3–58. Munari C, Tassi L, Di Leo M et al. Video-stereo-electroencephalographic investigation of orbitofrontal cortex. Ictal electroclinical patterns. Adv Neurol 1995;66:273–95. Greenberg MS. Olfactory hallucinations. In: Serby MJ, Chobor KL, eds. Science of Olfaction. Berlin: Springer-Verlag, 1992:467. Hausser-Hauw C, Bancaud J. Gustatory hallucinations in epileptic seizures. Electrophysiological, clinical and anatomical correlates. Brain 1987;110:339–59. Pool JL, Ransohoff H. Autonomic effects on stimulating the rostral portion of the cingulate gyrus in man. J Neurophysiol 1949;12: 385–92. Van Buren J, Ajmone-Marsan C. A correlation of autonomic and EEG components in temporal lobe epilepsy. Arch Neurol 1960;91:683–703. Halgren E, Walter RD, Cherlow DG, Crandall PH. Mental phenomena evoked by electrical stimulation of the human hippocampal formation and amygdala. Brain 1978;101:83–117.
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Ojemann GA, Van Buren JM. Respiratory, heart rate and GSR responses from human diencephalon. Arch Neurol 1967;16: 74–88. Baumgartner C, Groppel G, Leutmezer F et al. Ictal urinary urge indicates seizure onset in the nondominant temporal lobe. Neurology 2000;55(3):432–4. Loddenkemper T, Foldvary N, Raja S, Neme S, Lüders HO. Ictal urinary urge: further evidence for lateralization to the nondominant hemisphere. Epilepsia 2003;44(1):124–6. Van Buren JM. The abdominal aura. A study of abdominal sensations occurring in epilepsy and produced by depth stimulation. Electroencephalogr Clin Neurophysiol 1963;15:1–19. Bartolomei F, Barbeau E, Gavaret M et al. Cortical stimulation study of the role of rhinal cortex in déjà vu and reminiscence of memories. Neurology 2004;63:858–64. Henkel A, Noachtar S, Pfänder M, Lüders HO. The localizing value of the abdominal aura and its evolution: a study in focal epilepsies. Neurology 2002;58(2):271–6. Kotagal P, Lüders HO, Williams G, Nichols TR, McPherson J. Psychomotor seizures of temporal lobe onset: analysis of symptom clusters and sequences. Epilepsy Res 1995;20(1):49–67. Mendez MF, Cherrier MM, Perryman KM. Epileptic forced thinking from left frontal lesions. Neurology 1996;47:79–83. Stefan H, Schulze-Bonhage A, Pauli E et al. Ictal pleasant sensations: cerebral localization and lateralization. Epilepsia 2004;45(1):35–40. Janszky J, Ebner A, Szupera Z et al. Orgasmic aura – a report of seven cases. Seizure 2004;13(6):441–4. Weinand ME, Hermann B, Wyler AR et al. Long-term subdural strip electrocorticographic monitoring of ictal déjà vu. Epilepsia 1994;35(5):1054–9. Comment in: Epilepsia 1995;36(5):522. Bancaud J, Brunet-Bourgin F, Chauvel P, Halgren E. Anatomical origin of déjà vu and vivid ‘memories’ in human temporal lobe epilepsy. Brain 1994;117:71–90. Blanke O, Landis T, Spinelli L, Seeck M. Out-of-body experience and autoscopy of neurological origin. Brain 2004;127:243–58. Nair DR, Lüders HO. Cephalic and whole-body auras. In: Lüders HO, Noachtar S, eds. Epileptic Seizures: Pathophysiology and Clinical Semiology. Philadelphia: Churchill Livingstone, 2000: 355–60. Jobst BC, Siegel AM, Thadani VM et al. Intractable seizures of frontal lobe origin: clinical characteristics, localizing signs, and results of surgery. Epilepsia 2000;41(9):1139–52. Laplante P, Saint-Hilaire JM, Bouvier G. Headache as an epileptic manifestation. Neurology 1983;33(11):1493–5. Bernasconi A, Andermann F, Bernasconi N, Reutens DC, Dubeau F. Lateralizing value of peri ictal headache: a study of 100 patients with partial epilepsy. Neurology 2001;56:130–2. Wieser HG, Williamson PD. Ictal semiology. In: Engel J Jr, ed. Surgical Treatment of the Epilepsies, 2nd ed. New York: Raven Press, 1993:161–71.
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Autonomic seizures: localizing and lateralizing value V Nagaraddi and HO Lüders
Summary Autonomic symptoms are common during epileptic seizures, mainly in conjunction with other more prominent symptoms. However, in selected cases autonomic symptoms may also constitute the predominant ictal manifestation. Autonomic seizures are actually mediated by activation of the central autonomic network and are not an adjunct to motor and other manifestations of seizures. Autonomic seizures have been divided into cardiovascular, respiratory, gastrointestinal, cutaneous, papillary, and urogenital, depending upon the symptoms.1 Certain autonomic symptoms provide lateralizing and/or localizing information about the ictal onset zone, due to specific representation of the central autonomic network in the cortex. Autonomic symptoms range from subtle changes, which are apparent only with video-EEG monitoring, to severe, sometimes life-threatening events. When autonomic symptoms are the sole seizure manifestation, they can be difficult to differentiate from psychogenic non-epileptic seizures. Finally, autonomic symptoms during seizures provide a unique opportunity to study the functional organization of the central autonomic network.1
Introduction Autonomic symptoms occurring during seizures have been recognized for more than 100 years. Changes in heart rate and respiration during a generalized tonic–clonic seizure are predictable and are obvious to an observer. Autonomic symptoms during focal seizures have long been observed as well, including goose bumps, flushing, pallor, sweating, sexual sensations, and pupillary changes.2 In 1981, the commission on classification and terminology of the International League against Epilepsy included autonomic seizures as a subdivision of simple partial seizures in the revised seizure classification. This subdivision included among others, epigastric sensations, pallor, sweating, flushing, piloerection and pupillary dilation.3 Autonomic symptoms can occur either during the ictus or postictally. They may also play a role in some interictal epileptic behaviors. Autonomic symptoms are being recognized with increasing frequency. Nevertheless, autonomic seizures are still frequently under- or misdiagnosed, resulting in expensive investigations and inappropriate therapies, leaving incapacitating and potentially fatal symptoms untreated.4
Both focal and generalized seizures alter the central autonomic functioning during ictal, postictal, and interictal states. All aspects of autonomic function can be affected, including the parasympathetic, sympathetic, and adrenal medullary systems. Focal and generalized seizures typically activate the sympathetic nervous system, increasing the heart rate and blood pressure, although parasympathetic activation or sympathetic inhibition may predominate during some focal seizures.5
Neuroanatomy of the autonomic system The preganglionic sympathetic and parasympathetic efferent pathways are regulated by reciprocally interconnected cortical, subcortical, and brainstem regions. The components of the central autonomic network have been established by experimental methods, and include the insular cortex, the medial prefrontal cortex, the central nucleus of the amygdala, the nucleus of the stria terminalis, the hypothalamus, the midbrain periaqueductal gray matter, the pontine parabrachial region, the nucleus of the solitary tract and the intermediate reticular zone of the medulla.6 Anatomic and physiologic studies have defined a topographically organized visceral map in the insula, supporting the concept of the insula as a ‘visceral sensory cortex’, with localization of gustatory responsive neurons to the rostral agranular region and gastric mechanical responsive neurons to the caudal granular region. Electrical stimulation studies of the insular cortex have demonstrated heart rate, blood pressure, respiratory, piloerector, pupillary, gastrointestinal, salivatory, and adrenal responses. Intraoperative stimulation studies of the human insular cortex have suggested that tachycardia and pressor responses occur more commonly with right anterior insula stimulation, whereas bradycardia and depressor responses are more common with left anterior insular stimulation.7,8 Stimulation of the medial prefrontal cortex produces profound changes in blood pressure, heart rate, and gastrointestinal motility. A viscerotopic map of this region, which includes the anterior cingulate gyrus and the inferior and prelimbic cortices, supports the concept of the medial prefrontal cortex as a ‘visceral motor cortex.’ Intraoperative human stimulation studies of the cingulate gyrus have demonstrated changes in heart rate and blood pressure.4,9 443
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Definition of autonomic seizures Autonomic seizures have a measurable or visible autonomic symptom or manifestation, for example change in the heart rate or piloerection, which is also a prominent or predominant feature of the seizure. The symptom is usually verifiable by an observer, reproducible over several seizures and can be documented quantitatively or qualitatively. This is important in distinguishing autonomic seizures from autonomic auras, which are symptoms perceived by the patient, such as feeling hot, or cold and clammy etc., but there is no change that can be verified by observation or measurement, such as the temperature being assessed by touch or measured by a thermometer and sweating documented by either touch or observation. The limitation is that many of the autonomic symptoms in question, are not quantifiable in most routine settings, because there is no simple, practical means of measuring it, for example peristalsis, pupillary changes etc. It should also be noted that almost all epileptic seizures have some autonomic symptoms, especially cardiac and respiratory changes. Most focal and generalized tonic-clonic seizures have changes in heart rate, as measured by the EKG. In most of these cases, there is sinus tachycardia at the onset of seizure and to a lesser extent sinus bradycardia. Similarly, there are changes in the respiratory pattern and rate, which could be either due to modulation of the respiratory centers in the cortex and brainstem due to the spread of the seizure or as a result of the tonic contraction and spasms of the diaphragm and intercostal muscles. In these seizures, the predominant feature is either the alteration in consciousness and or the motor manifestations accompanying it and therefore they are not classified as true ‘autonomic seizures’.4,5
Cardiac manifestations Cardiac manifestations are the most studied autonomic alterations, partly because of trying to elucidate the pathophysiology of SUDEP and also because most EEG recordings have an EKG channel that can be easily analyzed. Ictal tachycardia An increase in the heart rate is seen in the vast majority of all epileptic seizures, including subclinical electrographic seizures.10–13 Depending upon the definition of tachycardia, usually >100 beats per minute, the incidence of ictal tachycardia varied from 33–87%.14–18 Furthermore, there is a significant preponderance of ictal tachycardia in temporal lobe epilepsy versus extratemporal lobe epilepsy (62% versus 11%, p < 0.0018)19 and in one study ictal tachycardia was seen in 98% of temporal lobe seizures.16,20,21 Within the temporal lobe, ictal tachycardia was found to be more prevalent in seizures arising from the mesial temporal lobe.15,21 The onset of tachycardia tended to precede the EEG seizure onset, more so in temporal lobe versus extratemporal lobe seizures and mesial temporal lobe versus lateral temporal lobe seizures.13,17,21 Finally, ictal tachycardia has been lateralized to the right hemisphere in several studies.17,22 This suggests that early and significant tachycardia was primarily associated with right mesial temporal lobe seizures.20
Ictal bradycardia A decrease in the heart rate is a lot less common and varied from 0-5% of seizures reported in several studies.14,16,17,20 There are mixed results to the localization and lateralization of ictal bradycardia. Most of the prior reports had shown a predilection of ictal bradycardia in left temporal lobe seizures.23–25 However, a recent study and other reports dispute this finding and suggest that there is usually bilateral involvement in seizures causing ictal bradycardia.24,26 The reason may be due to the fact that ictal bradycardia is relatively uncommon and the number of seizures with ictal bradycardia in all of the studies were small, which included several case reports. Ictal asystole The incidence of ictal asystole is extremely rare,27,28 though it may be higher than previously estimated especially in focal intractable epilepsy.29–31 It has been implicated as one of the causes of SUDEP. There are several anecdotal case reports of ictal asystole following ictal bradycardia in left hemispheric seizures, mainly left temporal and frontal lobe seizures.28,32–35 Single cases of ictal asystole in seizures arising from the left cingulate gyrus36 and right frontal lobe37have also been reported. Ictal arrhythmia High-risk or fatal cardiac arrhythmias during epileptic seizures are thought to be uncommon,38,39 however the incidence of ictal arrhythmias appears to be more common in intractable and generalized seizures.40 Various cardiac arrhythmias that have been reported during epileptic seizures include atrial fibrillation (AF), supraventricular tachycardia (SVT), premature ventricular contraction (PVC), premature atrial contraction (PAC), bundle branch block (BBB), ST depression and T-wave inversion.39,40 None of these ictal cardiac arrhythmias seem to have any localizing or lateralizing value.
Respiratory manifestations Respiratory manifestations are not as common as cardiac manifestations but is probably the second most common manifestation of autonomic seizures. Most of the studies have been done in pediatric patients as they appear to be more common in children Ictal hyperventilation Ictal hyperventilation, defined as a 10% increase in the respiratory rate from the pre-ictal baseline, was seen in 56% of focal seizures recorded from 37 children.41 In another study, hyperventilation was seen in 18% of children with autonomic seizures and was more common in temporal lobe epilepsy compared to extra temporal lobe epilepsy, but this was not statistically significant.42 A study in adults found hyperventilation in both temporal and frontal lobe epilepsies, but occurred more in mesial compared to lateral temporal lobe epilepsy.43
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Autonomic seizures: localizing and lateralizing value Ictal apnea Ictal apnea is most commonly reported in neonates and infants, typically lasting 1–2 minutes.44–51 It was seen in 20% of children,42 58% of adults52 and 30% of focal epilepsies.41 When localized, it was mostly seen in temporal lobe epilepsies,44–48,51,53 with cases lateralizing to both the left53 and right47,51 temporal regions. Ictal dyspnea and stridor This is not a well defined entity in the available literature. It was seen in 15% of children and two-third were associated with the tonic phase of epileptic seizures.42 A case report describes stereotypical episodes of dyspnea over 4 months which turned out to be due to a right mesial temporal lobe epilepsy.54 Postictal nose wiping/postictal coughing These two manifestations are thought to be due to same mechanism, which is increased parasympathetic activity, resulting in increased nasal and/or pharyngeal secretions, which then cause the patient either to wipe the nose or induce coughing. These reflexive maneuvers are usually seen postictally because during the ictus, both reflexive maneuvers are inhibited. Postictal coughing is most commonly seen in temporal lobe epilepsies, but has not been consistently lateralized to either the right or left hemisphere.42,55,56 However, the hand used in postictal nose wiping seems to lateralize and or localize to the ipsilateral temporal lobe.57–60
Gastrointestinal manifestations Gastrointestinal manifestations are the earliest autonomic symptoms to be described and studied. These symptoms generally have good lateralizing and localizing value except for ictal defecation because it is relatively rare and probably under reported. Abdominal epilepsy has been included here, even though it actually constitutes several different autonomic symptoms, but they are primarily gastrointestinal manifestations. Epigastric aura Epigastric aura is the earliest autonomic manifestation to be described61and the most commonly reported aura,62 it has significant localizing value, arising from the mesial temporal lobe structures and the insula primarily.63,64 In terms of lateralizing value, some authors claim that it is more common in nondominant hemispheric epilepsy,65,66 but it has not been confirmed by others.67–69 Abdominal epilepsy Abdominal epilepsy is the earliest autonomic seizure to be described, and was previously called visceral seizures.9,70 It is more common in children71,72 than adults.73,74 It is characterized by recurrent paroxysmal abdominal pain, usually associated with nausea, vomiting, lethargy and confusion.75–78 Abdominal epilepsy has not been consistently lateralized73 but has been localized to the temporal lobe in several reports.42,79–82 Most patients reported as abdominal epilepsy had paroxysmal
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autonomic symptoms but no objective proof that these symptoms actually were an expression of epileptic seizures. Ictal vomiting (Ictus emeticus) In contrast to abdominal epilepsy, in which vomiting usually accompanies the abdominal pain and the patient is aware of it, vomiting in ictus emeticus occurs as the sole manifestation83,84 or may be associated with other symptomatology of temporal lobe seizures, but the patient is usually amnesic of the vomiting.85–87 Ictal vomiting is a relatively rare manifestation of temporal lobe seizures in adults.84,88 It has been postulated to arise mostly from the non-dominant temporal lobe70,86–90 however there have been several reports of ictal vomiting with dominant temporal lobe epilepsy.42,91–95 On the other hand, ictal vomiting is the predominant manifestation of the early onset benign childhood occipital lobe epilepsy, which affects 13% of children aged 3-6 years.96–101 Ictal vomiting is also seen in extraoccipital benign childhood epilepsies and carries the same prognosis.102,103 Ictal vomiting is thought to occur when the epileptic discharges involve the medial and lateral aspects of the temporal lobe and the adjacent insular cortex.85–87,104,105 Even in extra-temporal lobe epilepsies, it has been shown that ictal vomiting occurs when the ictal discharge spreads to the temporal lobe from the extratemporal focus, which in most cases is the occipital lobe.104,106 Ictal spitting (Ictus exporatus) Ictal spitting is a rare manifestation of epileptic seizures, with an incidence of 0.2 to 2.2% of patients in epilepsy monitoring units.107–109 It has been lateralized and localized to the nondominant temporal lobe in most of the studies,42,108–112 but has been reported in dominant temporal lobe in a couple of studies.107,113 Ictal spitting is also thought to arise from the insular cortex.109 Ictal defecation Ictal defecation is the urge to defecate, associated with the onset of a focal seizure, which has been reported anecdotally by several authors.64,70,114,115 A.L. Reeves mentioned several cases in a review article, of patients with the urge to defecate at the onset of a seizure. A recent case report describes a 47 year old right handed woman with the urge to defecate at the onset of a seizure and the EEG was lateralized to the right hemisphere during the seizure.116
Cutaneous manifestations Cutaneous manifestations are rare autonomic expressions of focal epilepsy, that were first described by Penfield,114 Mulder70, Daly115 and Van Buren.64,64,64 They usually occur in conjunction with one another, in addition to other common manifestations of focal epilepsy. Other cutaneous manifestations, which have been cited in the literature include sweating, cyanosis and purpura, but will not be covered here because there have been no reported localizing or lateralizing value to any of these manifestations and most of these studies were case-reports.
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Ictal piloerection (goose bumps) Ictal piloerection was identified in only 0.4% of 3500 patients undergoing video-EEG monitoring in a single epilepsy center over a 7 year period.117 It has been localized to the temporal lobe in the majority of the patients reported in the literature,117–119 including confirmation with cortical stimulation.117,120 The piloerection mostly tended to occur unilaterally and often had a ‘Jacksonian march’ and in most of the cases, it was ipsilateral to the onset of the focal epilepsy.117–119,121 The etiology was diverse, and included tumors,121,122 hippocampal sclerosis,120,121,123,124 limbic encephalitis,125 hyperosmolor non-ketotic hyperglycemia,126 post-traumatic127 and cryptogenic.118,124 However, it has not been consistently lateralized to either hemisphere and with several case reports of left118–120,124,128 and right122,123,127,129 hemispheric onsets. Ictal pallor The only comprehensive study of ictal pallor was a recent study in 100 children, in whom 11 were found to have ictal pallor. In this study 11 children had left temporal lobe epilepsy.130 This has not been replicated in adults with only a handful of reports and in most of these reports, ictal pallor was usually concomitantly associated with other cutaneous manifestation. Ictal flushing In contrast to ictal pallor, ictal flushing was observed in 19 out of 100 children undergoing video-EEG monitoring. Ictal flushing showed neither lateralizing nor localizing value. Flushing was mostly facial and happened not only during simple partial (motor) seizures but also during complex partial (temporal lobe) seizures, which suggests that flushing is due to both skin hyperperfusion during motor activities but also due to central autonomic involvement.42
Pupillary manifestations Pupillary manifestations are rare autonomic manifestations, with only a handful of case reports in the literature and hence have limited localizing and lateralizing value. Ictal mydriasis Bilateral mydriasis is a common concomitant of generalized convulsive seizures, both primary and secondarily generalized, most probably due to the diffuse spread of the epileptic discharges, thus activating widespread subcortical midline structures and the central sympathetic nervous system.1,4 Unilateral mydriasis is far less common and has been reported to be ipsilateral in focal occipito-temporal seizures131 and contralateral in a young boy with a ‘ benign left frontal epileptic focus’.132 Ictal miosis Bilateral miosis has been described in a case of generalized photosensitive epilepsy along with bilateral adduction as part
of a near reflex accommodation spasm.133 Bilateral miosis has also been described with bilateral internal ophthalmoplegia in a patient with left temporo-occipital epilepsy134 and without internal ophthalmoplegia in a 3-year-old girl with rightsided mesiotemporal ganglioglioma.42 Unilateral miosis associated with ptosis has been reported in two patients with temporal lobe epilepsy, with one case presumed to be ipsilateral and the other contralateral to the unilateral miosis.135 Left miosis associated with left homonymous hemianopia and visual hallucinations has also been reported in a patient with right occipital lobe epilepsy due to a small cavernous hemangioma.136
Urogenital manifestations Urine incontinence is the most common urogenital manifestation and is a common feature of generalized tonic-clonic seizures and usually occurs after the clonic jerking stops. It is not due to increased intravesicular pressure during the seizure, but rather depends on relaxation of the vesical sphincter during the phase of muscular recovery and occurs only if the bladder is full at the time of the attack. However, urine incontinence does not have any localizing or lateralizing value. Ictal urinary urge The aura of urinary urgency during seizures has been shown to be a lateralizing sign for non-dominant temporal lobe in two studies with a total of 12 adults undergoing video-EEG monitoring.137,138 A single case of ictal urinary urge associated with confusion, oral and genital automatism has been reported in a 6-year-old boy with a left temporal lobe seizure.139 Sexual/orgasmic aura Sexual auras refer to seizures that include erotic thoughts and feelings, sexual arousal, and orgasm. They may be accompanied by genital viscerosensory phenomena, vulvovaginal secretory activity, and olfactory hallucinations. Sexual auras are reported more frequently by women and may be associated more commonly with right temporal lobe epilepsy.140–142 Orgasmic auras, a subset of sexual auras, have been lateralized to the right hemisphere in the majority of the cases reported in the literature.143 In a case series of seven patients experiencing an orgasmic aura, six had right temporal lobe epilepsy confirmed by EEG, MRI, and ictal SPECT and the remaining patient who was left hemisphere dominant as confirmed by WADA, had left temporal lobe epilepsy.144 There are, however, also isolated reports of orgasmic auras with seizures from the left hemisphere, as determined by EEG.145 Genital aura Genital auras are characterized by unpleasant, sometimes painful, frightening, or emotionally neutral somatosensory sensations in the genitals and can be accompanied by ictal orgasm. Genital auras are localized to the parasagittal postcentral gyrus, where genital sensations are represented.
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Autonomic seizures: localizing and lateralizing value When these sensations are bilateral, then the secondary somatosensory area is also thought to be involved.145–147 Sexual automatisms Sexual automatisms, characterized by hypermotor movements consisting of writhing, thrusting, and rhythmic movements of the pelvis, arms, and legs, sometimes associated with picking and rhythmic manipulation of the groin or genitalia, exhibitionism, and masturbation, are localized to seizures from the frontal lobe. In addition, sexual automatisms were seen from different subcompartments of the frontal lobe, including the frontal convexity, the orbitofrontal region, and the supplementary sensorimotor area.148–151
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Genital automatisms Genital automatisms, characterized by discrete genital automatisms such as grabbing or fondling the genitals, which can be accompanied by masturbatory activity and exhibitionistic behavior, were generally associated with temporal lobe seizures, but could not be lateralized.141,142,152–154 Several recent studies in both adults and children have not shown any localizing or lateralizing value to genital automatisms. However, genital automatisms did localize to the temporal lobe when associated with ictal urinary urge or unilateral hand automatisms in adults. In children, the hand used for genital automatisms was more frequently ipsilateral to the seizure onset zone.155,156
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Masnou P, Gagnepain JP, Fouad A, Ducreux D, Adams D. Pilomotor seizures associated with sequential changes in magnetic resonance imaging. Epileptic Disord 2006;8(3):232–237. Seo DW, Lee HS, Hong SB, Hong SC, Lee EK. Pilomotor seizures in frontal lobe epilepsy: case report. Seizure. 2003;12(4):241–4. Fogarasi A, Janszky J, Tuxhorn I. Ictal pallor is associated with left temporal seizure onset zone in children. Epilepsy Res 2005;67(3):117–21. Masjuan J, Garcia-Segovia J, Baron M, Alvarez-Cermeno JC. Ipsilateral mydriasis in focal occipitotemporal seizures. J Neurol Neurosurg Psychiatry 1997;63(6):810–11. Gadoth N, Margalith D, Bechar M. Unilateral pupillary dilatation during focal seizures. J Neurol 1981;225(3):227–30. Shahar E, Andraus J. Near reflex accommodation spasm: unusual presentation of generalized photosensitive epilepsy. J Clin Neurosci 2002;9(5):605–7. Rosenberg ML, Jabbari B. Miosis and internal ophthalmoplegia as a manifestation of partial seizures. Neurology 1991;41(5):737–9. Afifi AK, Corbett JJ, Thompson HS, Wells KK. Seizure-induced miosis and ptosis: association with temporal lobe magnetic resonance imaging abnormalities. J Child Neurol 1990;5(2):142–6. Lance JW, Smee RI. Partial seizures with visual disturbance treated by radiotherapy of cavernous hemangioma. Ann Neurol 1989;26(6):782–5. Loddenkemper T, Foldvary N, Raja S, Neme S, Luders HO. Ictal urinary urge: further evidence for lateralization to the nondominant hemisphere. Epilepsia 2003;44(1):124–6. Baumgartner C, Groppel G, Leutmezer F et al. Ictal urinary urge indicates seizure onset in the nondominant temporal lobe. Neurology 2000;55(3):432–4. Inthaler S, Donati F, Pavlincova E, Vassella F, Staldemann C. Partial complex epileptic seizures with ictal urogenital manifestation in a child. Eur Neurol 1991;31(4):212–15. Remillard GM, Andermann F, Testa GF et al. Sexual ictal manifestations predominate in women with temporal lobe epilepsy: a finding suggesting sexual dimorphism in the human brain. Neurology 1983;33(3):323–30. Currier RD, Little SC, Suess JF, Andy OJ. Sexual seizures. Arch Neurol 1971;25(3):260–4. Freemon FR, Nevis AH. Temporal lobe sexual seizures. Neurology. 1969;19(1):87–90. Janszky J, Szucs A, Halasz P et al. Orgasmic aura originates from the right hemisphere. Neurology 2002;58(2):302–4. Janszky J, Ebner A, Szupera Z et al. Orgasmic aura – a report of seven cases. Seizure 2004;13(6):441–4. Calleja J, Carpizo R, Berciano J. Orgasmic epilepsy. Epilepsia 1988; 29(5):635–9. Ruff RL. Orgasmic epilepsy. Neurology 1980;30(11):1252. York GK, Gabor AJ, Dreyfus PM. Paroxysmal genital pain: an unusual manifestation of epilepsy. Neurology 1979; 29(4):516–19. Spencer SS, Spencer DD, Williamson PD, Mattson RH. Sexual automatisms in complex partial seizures. Neurology 1983;33(5):527–33. Williamson PD, Spencer DD, Spencer SS, Novelly RA, Mattson RH. Complex partial seizures of frontal lobe origin. Ann Neurol 1985;18(4):497–504. Bancaud J, Talairach J. Clinical semiology of frontal lobe seizures. Adv Neurol 1992;57:3–58. Jobst BC, Siegel AM, Thadani VM et al. Intractable seizures of frontal lobe origin: Clinical characteristics, localizing signs, and results of surgery. Epilepsia 2000;41(9):1139–52. Hooshmand H, Brawley BW. Temporal lobe seizures and exhibitionism. Neurology 1969;19(11):1119–24. Mascia A, Di Gennaro G, Esposito V et al. Genital and sexual manifestations in drug-resistant partial epilepsy. Seizure 2005;14(2):133–8. Leutmezer F, Serles W, Bacher J et al. Genital automatisms in complex partial seizures. Neurology 1999;52(6):1188–91. Dobesberger J, Walser G, Unterberger I et al. Genital automatisms: a video-EEG study in patients with medically refractory seizures. Epilepsia 2004;45(7):777–80. Fogarasi A, Tuxhorn I, Tegzes A, Janszky J. Genital automatisms in childhood partial seizures. Epilepsy Res 2005;65(3):179–84.
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Simple motor seizures: localizing and lateralizing value S Noachtar and S Arnold
Definition of simple motor seizures
Myoclonic seizures
Simple motor seizures are characterized by unnatural, relatively simple movements that can be reproduced by electrical stimulation of the primary and supplementary sensorimotor areas.1 Simple motor seizures can be divided into the following subtypes depending on the duration of the muscle contraction, the rhythmicity of movement repetition, and the muscles involved: myoclonic seizures (negative myoclonic seizure), clonic seizures, tonic seizures, epileptic spasms, versive seizures, and tonic-clonic seizures.1–3 In contrast to simple motor seizures, during complex motor seizures the patients perform movements that imitate natural movements, are relatively complex, and tend to involve different body segments moving in different planes. These movements have also been labeled automatisms. If a given seizure cannot be classified into the following categories based on the available information the term simple motor seizure is recommended.1–3
Myoclonic seizures consist of sudden muscle jerks of short duration (less than 400 ms), which do not recur in a rhythmical fashion. They can be either bilateral (generalized) or unilateral (Figure 51.1–51.2). Generalized myoclonic seizures, which predominantly affect the shoulders and proximal arms, are typical for patients with juvenile myoclonic epilepsy4 and have already been recognized in the mid-19th century.5 Generalized myoclonic seizures are also frequently seen in patients with Lennox-Gastaut syndrome6 and the rare MERRF syndrome (myopathy, encephalopathy, ragged red fibers) (Figure 51.1) or Unverricht-Lundborg-syndrome. Electroencephalographically, generalized myoclonic seizures are frequently associated with generalized polyspikes that have a fronto-central maximum. Bilateral myoclonic seizures are rarely observed in patients with focal epilepsies (Figure 51.2). The primary motor cortex or premotor areas are most likely involved in the generation of this seizure type.
Bilateral Myoclonic Seizure Fp2–A2 F8–A2 T4–A2 T6–A2 Fp1–A1 F7–A1 T3–A1 T5–A1 F4–A2 C4–A2 P4–A2 O2–A2 F3–A1 C3–A1 P3–A1 O1–A1 Fz–A2 Cz–A1 EMG1 EMG2 EKG
Figure 51.1. The generalized polyspikes in this 28-year old patient with MERFF syndrome are consistently associated with generalized myoclonic jerks of the trunk and proximal limbs, whereas single spikes, spike-wave complexes and less dense polyspikes were not. Longitudinal bipolar montage including EMG of both legs (EMG1=left anterior tibial muscle; EMG2= right anterior tibial muscle).
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Bilateral Myoclonic Seizure fc2–P8 c2–P8 cp2–P8 Fz–P8 fcz–P8 Cz–P8 cpz–P8 Pz–P8 f1–P8 fc1–P8 c1–P8 cp1–P8 F3–P8 fc3–P8 C3–P8 cp3–P8 F7–P8 T7–P8 fc5–P8 c5–P8 cp5–P8 P3–P8 F4–P8 C4–P8 ali bli are bre
R
L
100 µV 1 sec
Figure 51.2. This 53-year-old patient has myoclonic seizures of both legs with a right zentral perinatal lesion. EEG is referenced to the electrode P8. ali= left brachioradial muscle EMG; bli=left anterior tibial muscle EMG; are=right brachioradial muscle EMG; bre=right anterior tibial muscle EMG.
Unilateral myoclonic seizures are very rare and occur contralateral or predominantly contralateral to the epileptogenic zone. Figure 51.2 shows the rare occasion that left central polyspikes in the EEG were consistently associated with myoclonic jerks of the both legs in a patient with a left central perinatal lesion. Some patients with juvenile myoclonic epilepsy report unilateral myoclonic jerks although video recording usually establishes the bilateral character of the myoclonic jerks. These patients typically favor the dominant arm.7
Negative myoclonic seizures Negative myoclonus is a rare epileptic seizure type which is characterized by brief periods (20–400 ms) muscle atonia (Figure 51.3).8 Negative myoclonus occurs only if muscle activity is exerted and the sujdden muscle atonia leads to the drop of the limb. Polygraphic recordings are helpful to document muscle atonia in the EMG associated with negative myoclonic seizures and epileptiform discharges in the EEG
Right Arm Epileptic Negative Myoclonus M. abd. dig. I M. deltoideus F7–F3 F3–Fz Fz–F4 F4–F8 A1–T3 T3–C3 C3–Cz Cz–C4 C4–T4 T4–A2
1 sec
Figure 51.3. The transverse bipolar EEG montage shows that the left central sharp wave elicited a atonia of muscle activity in the right abductor digiti minimi and the right delta muscle, which documents an epileptic negative myoclonus. The MRI of this patient showed diffuse left hemisphere perinatal lesion and atrophy.
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and distinguish negative myoclonus from myoclonic seizures, which may be difficult visually (Figure 51.3). Negative epileptic myoclonus has been described in patients with frontal and paracentral epilepsies.9,10 Bilateral negative myoclonus also occurs in different encephalopathies.8 In unilateral negative myoclonus, the epileptogenic region is contralateral to the affected limb. The central primary somatosensory cortex is considered responsible for the generation of negative myoclonus but there is very little data available.11 The cortex in the postcentral gyrus has been shown to generate contralateral negative myoclonus.10
Clonic seizures Clonic seizures consist of repeated, short contractions of various muscle groups (agonists and antagonists) usually characterized by jerking or twitching movements recurring at a regular interval between 0.2 and 5 per second (Figure 51.4). The jerks seen with myoclonic and clonic seizures are the same except that myoclonic seizures consist of single jerks which repeat in an irregular fashion whereas with clonic seizures the jerks have a regular rate. In other words, clonic seizures consist of ‘myoclonic jerks’ recurring at a regular repetition rate. The movements may affect any part of the body. Generally they are an expression of epileptic activation of the primary motor or the premotor areas.12 Focal clonic seizures mostly affect the distal segments of the extremities, e.g., the hand or the face. Clonic activity may show a ‘march’ from the distal to the proximal parts of the extremities, reflecting the spreading activation of the primary motor cortex. Electrical stimulation of the supplementary sensorimotor area can elicit distal clonic movements, but only very rarely.13 Typically clonic seizures start with a tonic phase, which frequently is not clinically
detected unless polygraphic recordings reveal that the frequency of muscle contraction is higher in the beginning of the seizure and gets gradually slower, thus leading to recognizable clonic jerks.14 Unilateral clonic seizures typically involve the face or hand area and less frequently the leg or trunk15–17. Clonic seizures were first systematically described in 1827 by Bravais18 who distinguished facial, brachial, and crural onset clonic seizures and described the typical unilateral march of the convulsion which was later associated with Hughlings Jackson’s name. In a large series of 8938 epileptic patients clonic seizures have been found to be rare occurring in only 2.2% of the patients.19 However, clonic seizures were relatively frequent in those 127 patients who had somatosensory auras. One third (34.3%) of these patients had clonic seizures.19 Of 52 patients reported by Hallen in 1952, clonic seizures started in the hand in 16, in the face in 14, in the foot in ten, in the shoulder in four, in the leg in four, in the head in two, in the thorax in one and in the neck in another patient. The seizures types preceding and following clonic seizures are very variable. We analyzed all patients in whom clonic seizures were recorded at the Epilepsy Monitoring Units of the Bethel Epilepsy Center from 1991–1994 and the University of Munich Epilepsy Program from 1994–1995. We identified 127 patients with clonic seizures occurring in 162 different seizure evolutions from the data bases (Figure 51.5). Thus, some patients had more than one seizure evolution. Clonic seizures were the initial seizures in 33 patients. In the remaining 129 seizure sequences usually automotor (n=45) and tonic (n=45) seizures preceded the clonic seizures. The different seizure types preceding clonic seizures are listed in Figure 51.5. The clonic seizures evolved typically into generalized tonic-clonic seizures (n=58) and less frequently into other seizure types such as tonic or versive seizures (Figure 51.5). No following seizure types were observed in 42 patients.
Right shoulder clonic seizure fcz–poz cz–poz cpz–poz Pz–poz fcI–poz CI–poz cpI–poz fc2–poz c2–poz cp2–poz R
EMG–RSH
L
70 µV 1 sec
Figure 51.4. This 14-year-old boy had clonic seizures of the right shoulder secondary to a low-grade glioma, which were consistently associated with left central spikes in the surface EEG. Selection of ten EEG channels in a referential montage to the electrode POZ. EMG-RSH=EMG of the left delta muscle.
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Simple motor seizures: localizing and lateralizing value Seizure Evolutions 127 Patients with Focal Clonic Seizures Preceding seizure types
Following seizure types
automotor sz. (45) tonic sz. (45)
gen.tonic-clonic sz. (58
no preceding sz. (33) versive sz. (11) som.sens. aura(9)
no following sz. (42)
other aura(8) hypermotor sz. (4) hypomotor sz. (3) myoclonic sz. (3)
tonic sz. (9) Clonic seizure 162
versive sz. (9) automotor sz. (5) gen.clonicsz. (4) hypermotor sz. (2)
atonic sz. (1)
Figure 51.5. Seizure types preceding and following clonic seizures in 162 seizure evolutions of 127 patients who underwent EEG-video monitoring. Clonic seizures were the initial seizure manifestation in 33 seizure evolutions. The frequency of preceding and following seizure types are given in parenthesis. Clonic seizures were preceded by other seizure types in 129 seizure evolutions.
Clonic seizures may represent the initial seizure symptomatology but may be preceded by other seizure types such as auras, automotor or tonic seizures (Figure 51.5). Clonic seizures can evolve into other seizure types most commonly into generalized tonic clonic seizures (Figure 51.5–6). Unilateral clonic seizures are present in several focal epilepsies. In patients with frontal lobe epilepsy, clonic seizures tend to occur early in the seizure evolution and the patient is usually conscious at the time the clonic activity begins (Figure 51.6).12,20 When clonic seizures are the result of spread of epileptiform activity into the frontal lobe from the occipital or temporal lobe, consciousness is usually altered at the onset of unilateral clonic seizures. Generalized clonic seizures only very rarely occur with preserved consciousness.21
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Fincher and Dowman22 reported on a series of 130 patients with ‘Jacksonian’ seizures. Eighty-four patients had ‘purely motor’ seizures. In 20 patients somatosensory auras were followed by motor seizures and in nine patients motor features immediately preceded sensory ‘attacks’. In 17 instances there were sensory and motor ‘attacks’ occurring simultaneously. The authors mention two patients, in whom generalized jerkings were not associated with loss of consciousness. Consciousness is usually preserved if unilateral clonic activity is the initial seizure manifestation. If an automotor seizure precedes a clonic seizure, which we observed only in temporal lobe epilepsy and not in frontal lobe epilepsy consciousness will typically be disturbed during the clonic seizure.23 A series of ‘pure’ frontal lobe epilepsies of the Montreal Neurological Institute showed focal ‘sensorimotor seizures’ in 27% of the patients.24 Automotor seizures were as common in this series (30%). Geier et al.25 found ‘clonic and/or tonic seizures’ which were not further specified in 77.3% of 22 patients with frontal lobe epilepsies. Disturbance of consciousness (100%), deviation of head and eyes (86.4%), vocalisation (86.4%), and falling (81.8%) were more common in this study than clonic seizures. In a recent study of 252 patients with focal epilepsies 14 patients had clonic seizures.20 In the 14 patients with clonic seizures a structural lesion could be demonstrated in the primary motor cortex in seven patients, in the premotor region in one patient and in the parietal cortex in another patient. Clonic seizures occurred both in temporal and frontal lobe epilepsies but the seizure evolution was different: if the clonic seizures occurred early in the seizure evolution there was a significant association with frontal lobe epilepsy.20 In a series of 40 patients with frontal lobe epilepsies who underwent selective epilepsy surgery of the parasagittal convexity of the frontal lobes (PSC) or anterolaterodorsal convexity (ALDC) and remained seizure free, seizure onset in the PSC (eight of ten patients) was more frequently associated
Clonic Seizures in Frontal Lobe Epilepsies Preceding seizure types
Following seizure types
no preceding sz. type (6) 6 aura (3) 1 2 no aura (10)10 abdominal aura (1) 1
focal tonic sz. (14)
somato– sensory 1 aura (2) dialeptic 1 sz. (4)
1
hypermotor seizure (1)
4 7 2 1 1 1
no following sz. type (8) focal clonic sz. head (6)
3
arm (9)
4
arm & leg (3)
1
1
gen. ton.–clon. sz. (9)
leg (2) non– spec. (2)
versive seizure (1)
8
1 1 gen. clon. sz. (2)
Figure 51.6. Seizure types preceding and following clonic seizures as documented by EEG-video monitoring in 19 patients with frontal lobe epilepsies. Clonic seizures were the initial seizure manifestation in seven seizure evolutions. Focal clonic seizures evolved further either into generalized tonic-clonic or generalized clonic seizures.
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with focal motor seizures than seizure onset in the ALDC (15 of 30 patients).26 In a later report of the same group 29% to 60% of the patients with ‘dorsolateral frontal lobe epilepsies’ had clonic seizures.27 The authors concluded that clonic seizures occur in patients with epilepsy of different frontal compartments and are not a reliable indicator of seizure onset location.27 A neuroimaging study using FDG-PET in patients with probable frontal lobe epilepsy reported clonic seizures in nine of 22 patients. In six patients clonic activity was the initial seizure symptom. Precentral seizure onset was assumed in three, premotor onset also in three, and mesial onset in another three patients.28 A study of ten patients with medial frontal or orbitofrontal seizure onset did not describe clonic seizures.29 These patients had seizures characterized by complex motor automatisms with kicking and trashing movements and a bizarre appearance frequently leading to erroneous diagnosis of non-epileptic psychogenic seizures. Data about seizure evolution of focal clonic seizures is sparse. Thirty percent of 24 patients with frontal lobe epilepsy have been described to have clonic seizures.30 In three of these patients the clonic seizures were preceded by conscious contralateral version. The clonic seizures were followed by tonic seizures consisting of tonic posturing of all extremities in three patients. Harvey et al.31 reported clinical seizures characteristics in 22 children with frontal lobe epilepsies who underwent ictal SPECT studies. Ten children had clonic seizures. Seizure evolution commenced most frequently with behavioral arrest (n=13) or auras (n=6) which evolved into tonic seizures (n=11), hypermotor (n=6), or automotor seizures (n=2). The clonic seizures were preceded by tonic seizures in seven patients, by an aura in one patient, by behavioral arrest in one patient, and by an automotor seizure in another patient. Only one patient had clonic seizures as the inital seizure manifestation. In one child the clonic seizures further evolved into generalized tonic-clonic seizures. We identified 19 patients of the above mentioned series of 129 patients with clonic seizures who had a frontal lobe epilepsy. The seizure evolutions in these cases are shown in Figure 51.6. Only in six patients the seizures started with clonic activity. More commonly, the clonic seizures were preceded by one or two other seizure types such as auras and tonic seizures. In conclusion, the occurrence and frequency of clonic seizures in frontal lobe epilepsy varies considerably between studies. It seems that the occurrence of clonic seizures depends on different locations of seizure onset in the frontal lobe and individually different seizure spread patterns. In our series, tonic seizures typically preceded clonic seizures and only a minority of the patients had clonic seizures as the initial seizure type. In temporal lobe epilepsy, complex motor activity like oral automatisms was seen most frequently (10%) whereas simple motor activity like facial and brachial twitching without Jacksonian march occurred ‘less commonly’ (4%).32 Another study only mentions automatisms as the ictal symptomatology of seizures in patients with temporal lobe epilepsies.33 In a cluster analysis of 59 patients of ‘primary psychomotor epilepsy’ unilateral and bilateral tonic, clonic, and versive activity was described.34 Most commonly the face area was involved unilaterally (about 30–50% of the seizures), followed by the hand (20%) and the leg (7%). In this report tonic, clonic, and versive seizures were all lumped together.34
A recent study of seizures in 31 patients with temporal lobe epilepsy who underwent epilepsy surgery and were seizure free reported unilateral clonic activity in the face in eight and in the arm in three patients.35 Bilateral clonic activity of the arms was observed in 14 patients and of the legs in one patient.35 These findings are in agreement with the study of Abou-Khalil et al.36 who observed focal clonic activity in eight of their 32 patients with unilateral temporal lobe epilepsies documented by EEG-video recordings. In three of these patients the clonic activity was concomitant with head turning to one side. However, the study did not distinguish between head turning that looks like a normal movement and the forceful ‘version’ frequently associated with unilateral clonic movements which is almost pathognomonic of regional contralateral epilepsy.37 The study of Manford et al.20 reported on clonic movements in 17 of 58 ‘temporal seizures’ in 42 patients with temporal lobe lesions. Clonic movements were observed more frequently in patients with frontal lobe lesions (35 of 61 seizures of 49 patients). However, clonic movements are only suggestive of frontal lobe epilepsy when they occur early in the evolution of a seizure.20 We evaluated the seizure sequences in our series of 24 patients with temporal lobe epilepsies who demonstrated clonic seizures during EEG-video recordings (Figure 51.7). All 24 patients had automotor seizure preceding the clonic seizures and in no case did the clonic seizures involve primarily the leg. In three patients, automotor seizures first evolved into versive seizures and then eventually into clonic seizures. All patients had generalized tonic-clonic seizures following the clonic seizures. We recently found statistically significant differences in the seizure evolutions of mesial and neocortical temporal lobe epilepsy.38 Abdominal auras and contralateral dystonic posturing were more frequent in patients with mesial temporal lobe epilepsy whereas early clonic seizures occurred more frequently in patients with neocortical temporal lobe epilepsy. This might reflect different cortical spread of seizure activity.38 In conclusion, clonic seizures are usually preceded by automotor and followed by generalized tonic-clonic seizures in temporal lobe epilepsy. Thus, the seizure sequences of clonic seizures in temporal lobe epilepsy is clearly different from the seizure sequences in frontal lobe epilepsy (Figure 51.6–7). It is well known that tumors in the paracentral (perirolandic) region are frequently associated with epilepsy.39 Most studies about focal epilepsy syndromes distinguish frontal and parietal lobe epilepsies. However, in a considerable number of patients the seizure anatomically involves both, the frontal and the parietal lobe. The observation that seizures arising from the frontal and parietal lobes outside the perirolandic region behave differently both, clinically and pathophysiologically to seizures arising from the perirolandic (paracentral) region has been recognized for decades and is reflected in the studies of the Montreal school.30, 40 About one third (34.3%) of 127 patients who had somatosensory auras had also had clonic seizures.19 Fifty percent of the lesions of these patients were located in the contralateral central region.19 In a series of 28 patients in whom extratemporal seizure onset had been documented by means of invasive EEG recordings, nine patients had clonic seizures and two of them had epilepsia partialis continua.41 The seizure onset
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Clonic Seizures in Temporal Lobe Epilepsy preceding seizure types
abdominal aura (15)
following seizure types
no preceding sz. type (0)
psychic aura (3) no aura (1) abdominal & psychic aura (2)
clonic sz. automotor 11 4 seizure sz. 5 1 3
other aura (2) visual autonomic psychic aura (1)
no following sz. type (0)
face 11
11
face & arm 5
5
arm 7 lateralized 1
versive 1 sz. 2
gen. ton.–clon. sz. (24)
7 1
Figure 51.7. Seizure types preceding and following clonic seizures as documented by EEG-video monitoring in 24 patients with temporal lobe epilepsies. All clonic seizures of this series were preceded by other seizure types. Most commonly clonic seizures involved the face and were preceded by automotor seizures. All patients showed an evolution to generalized tonic-clonic seizures.
was perirolandic in six of these nine cases and six patients had auras preceding the clonic seizures. Of 34 patients with parietal lobe tumors who underwent surgical resection at the Montreal Neurological Institute between 1934 and 1988, 82% had focal clonic activity in the course of their seizures.42 In a greater series of 82 patients with parietal lobe epilepsy of the same institution 57% had clonic seizures.40 However, as mentioned above, in the MNI series parietal lobe epilepsy usually refers to the parietal lobe posterior to the postcentral sulcus and does not include the postcentral gyrus.40 In another series, clonic seizures occurred in three of ten patients with lesions in the parietal lobe (including the postcentral gyrus).43 One patient had ‘focal motor seizures’ which were preceded by a somatosensory aura of the right hand. In two patients somatosensory auras preceded the clonic seizures, in one patient clonic seizures were the initial seizure manifestation. In another study of 11 patients with parietal lesions most probably also involving the postcentral gyrus, clonic seizures were reported in 4 patients.44 Somatosensory auras were present in 7 patients of this series. In a recent report of 11 patients with seizures involving the supplementary sensorimotor area, all patients showed clonic movements present in one or more extremities following tonic posturing which usually lasted 10–30 seconds.45 The clonic movements and the tonic posturing are usually bilateral, but unilateral clonic activity is an excellent lateralizing sign.26,46 Seizures involving the supplementary sensorimotor area are typically either tonic or less frequently hypermotor seizures,23 e.g., consisting of bizarre and violent movements predominantly of the trunk and the proximal extremities.45,47–49 Tonic and clonic seizures have been described in patients with occipital lobe epilepsy.50,51 The initial seizure symptomatology most frequently includes visual auras and other signs such as eye blinking or eye deviation. Spread to the frontal lobes is usually associated with tonic and/or clonic activity. This has been reported in three of 25 patients as the only spread pattern. In another 11 patients of this series, a combination of
‘frontal’ and ‘temporal lobe type’ seizure was observed.51 However, no data were available in this study regarding the exact seizure semiology and frequency of tonic or clonic seizures.51 In another study of eight patients in whom occipitotemporal seizure onset was documented by invasive EEG studies, no patient had clonic seizures of the extremities.52 One patient had jerking eye movements to the right. In the series of 42 patients with occipital lobe epilepsies of the MNI treated between 1930 and 1991, 13 patients had unilateral clonic seizures of the arm or face.50 In ten patients versive head and/or eye deviation preceded the clonic seizures.50 The detailed evolution of the clonic seizures is not mentioned. Since the early reports it has been recognized that children with benign focal epilepsy of childhood frequently have clonic seizures.53 Characteristic seizures consist of tonic, tonic-clonic, or clonic seizures involving the face area. Usually this is preceded by an unilateral somatosensory aura of the face.54 Spreading of the clonic activity to the ipsilateral hand or arm (‘Jacksonian march’) occurs only infrequently. Usually the seizures occur during sleep and evolve into generalized tonic-clonic seizures. In these cases a focal seizure onset may be overlooked. Rasmussen’s encephalitis almost invariably is associated with clonic status which usually is restricted to the arm and less frequently to the face and leg of one side.55 Clonic status usually occurs with the progression of this syndrome which typically includes hemiparesis of the affected limbs (Figure 51.8). Generalized clonic seizures are frequently seen following generalized tonic seizures in grand mal epilepsy. This type of seizures (generalized tonic-clonic seizures) will be discussed in detail in another chapter. Isolated generalized clonic seizures are rare in adults but may, for instance, occur in patients with progressive myoclonic epilepsies.7 These patients typically have generalized myoclonic seizures which are not as repetitive and rhythmic as clonic seizures. In newborns, generalized clonic seizures are more frequently observed but may still have a focal seizure onset in the EEG.56 We identified two patients who had generalized clonic seizures in our series of frontal
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Textbook of epilepsy surgery Left leg clonic status
A1–T7 T7–C3 C3–CZ CZ–C4 C4–T8 T8–A2 P7–P3 P3–PZ PZ–P4 P4–P8 EMG L M.TIB. ANT.
50 µV 1 sec
Figure 51.8. Sixty-nine-year old man with continual jerking of the left foot and leg for several weeks, without loss of consciousness. Electromyography from the left anterior tibial muscle showed that jerks occurred synchronously with each burst of polyspikes on EEG. Polyspikes were maximum at left vertex electrodes, presumably as a result of paradoxical lateralization of the discharge from the right interhemispheric region.
lobe epilepsies. Both patients had focal tonic seizures preceding the generalized clonic seizures. Jackson’s clinico-pathological observations showed that motor seizures are associated with lesions of the motor cortex.57 Electrical stimulation of the primary motor area (Brodmann’s area 4) or the premotor areas (area 6) can elicit clonic movements.58–60 It is therefore reasonable to conclude that clonic seizures are an expression of epileptic activation of the motor cortex. Electrical stimulation of the supplementary sensorimotor area can elicit clonic movements, but this occurs only very rarely and typically not at seizure onset but later in the seizure evolution.13,62 The fact that the hand and face area are most commonly involved in clonic seizures is usually attributed to the large cortical representation of these parts of the body. In contrast, the rare occurrence of clonic seizures limited to the trunk reflects its small cortical representation.17 Spread of clonic seizures may reflect the cortical representation of the body in the motor cortex. It has been speculated that the variability of the observed spread patterns may reflect interindividual variability of the cortical representation.15 It is important to remember also that clonic seizures can only be elicited when the epileptic discharge is strong enough to produce suprathreshold activation of a given region of motor cortex. Experimental studies have shown that different regions of the motor cortex have also different thresholds to electrical stimulation.63 It is important to point out that high-frequency electrical stimulation (50–60 Hz) of the primary motor area in wake humans ictally causes tonic contractions, which evolve into clonic twitching of the affected muscles at a frequency of ca. 1–2 Hz.14 The epileptic clonus consists of simultaneous contractions of agonistic and antagonistic muscles at regular intervals and is separated by periods of complete muscle relaxation. Epileptic clonic muscle contractions are generated by localized polyspike-wave activity in cortical primary motor areas. The periods of muscle relaxation occur during the EEG slow waves. The study of Hamer et al.14 suggests that focal
clonic seizures are focal tonic-clonic seizures. It is known that single or short series of electrical stimuli only elicit muscle responses if relatively high intensities are used.60,64 Temporal and spatial summation of the stimuli were needed for clonus generation.65 This principle is illustrated in the patient with the left calf clonic status shown in Figure 51.8. This explains why single spikes or slow, repetitive spikes frequently do not elicit muscle twitching, whereas polyspikes or runs of paroxysmal fast activity are usually associated with muscle responses. Most probably temporal facilitation elicited by repetitive stimulation is necessary to exceed the threshold of the motor cortex. Jerking of the left calf was always accompanied by polyspikes in the EEG (Figure 51.8), whose potential field extended from the vertex to the left central region. Conversely, individual spikes that did not correlate with jerking of the foot had a slightly different potential field extending to the right centroparietal area. The polyspikes in this case have a maximum ipsilateral to the affected leg. This is an example of paradoxical lateralization.66–68 The EEG of generalized clonic seizures shows generalized epileptiform discharges. There is typically a 1:1 relationship between muscle twitch and epileptic discharge, and the background activity between the discharges is generally suppressed. Generalized fast activity usually leads to tonic ‘posturing seizures’ and only exceptionally to clonic movements. Generalized clonic seizures are assumed to be the result of intermittent generalized epileptic activation of the motor region of the cortex (Brodman areas 4 and 6). We have also observed cases in which epileptic seizures originating in the supplementary sensorimotor area led to bilateral clonic movements of the upper extremities without any clouding of consciousness. In these cases no generalized spike-and-wave discharges occurred. It is quite probable that the generalized clonic seizures in these cases are caused by restricted activation of one or both of the supplementary sensorimotor areas.
Tonic seizures Tonic seizures consist of a sustained contraction of one or more muscle groups usually lasting at least 3 sec leading to posturing of the limbs or whole body.3,23,69 Tonic seizures in patients with focal epilepsy preferentially affect proximal muscle groups on both sides of the body. However, they predominate most often in the contralateral body, leading to an asymmetric posture.70 In most patients with focal epilepsy, consciousness is unclouded, at least at the onset of such unilateral or asymmetric seizures.25,71,72 If clearly unilateral, tonic seizures have a high lateralizing significance, pointing to a contralateral seizure onset. Ictal EEG in frontal epilepsies shows a low-amplitude high-frequency pattern (‘recruitment pattern’) (Figure 51.9). Consciousness is disturbed from the beginning of generalized tonic seizures, which are common in patients with Lennox-Gastaut syndrome.6 Generalized tonic seizures usually last from 3–10 sec. The ictal EEG of generalized tonic seizures in patients with Lennox-Gastaut syndrome is similar to the ictal EEG in frontal lobe epilepsies showing a diffuse low-amplitude high-frequency recruiment pattern (Figure 51.9). Tonic seizures in focal epilepsies are more commonly bilateral (76%) than unilateral (24%).73 The majority of bilateral tonic seizures involve the whole body (both arms
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Bilateral asymmetric tonic seizure F7–F3 F3–Fz Fz–F4 F4–F8 A1–T7 T7–C3 C3–Cz Cz–C4 C4–T8 R
L
T8–A2 100 µV 1 sec
Figure 51.9. This transverse bipolar EEG montage of a 17-year old female with a low grade glioma in the medium frontal gyrus shows a typical EEG seizure pattern during a bilateral asymmetrical tonic seizure. After a high amplitude midline sharp wave the EEG shows low amplitude high frequency activity with a midline frontocentral maximum (recruitment pattern). The arrow marks the clinical seizure onset.
and legs and trunk).73 Unilateral tonic seizures affected most commonly one arm (56%) or one side of the body (20%).73 Tonic seizures occur most commonly in frontal lobe epilepsy (62.2%) and very rarely in temporal lobe epilepsy (1.7%). In the latter only unilateral tonic seizures occurred, whereas 32% of the tonic seizures in frontal lobe epilepsies were bilateral.73 Focal tonic seizures most probably originate in the cortical motor areas, i.e., the primary motor and the supplementary sensorimotor areas. However, the reticular formation of the brain stem and the thalamus were reported to be involved in the generation of tonic seizures in patients with LennoxGastaut syndrome.74 Phonatory seizures could be considered tonic seizures of the phonatory muscle system. They result from activation by the ictal discharge of the primary motor cortex or the SMA.75 Phonatory movements have been elicited on stimulation of the SMA or the primary motor cortex below the tongue or lip area. Vocalization in SMA seizures is more often sustained than interrupted, whereas seizures involving the primary motor area tend to produce interrupted sounds. Paroxysmal dystonia resulting from subcortical pathology such as brainstem dysfunction or multiple sclerosis has to be considered in the differentialdiagnosis of focal tonic seizures.
to flexion of the neck (and legs) and abduction of both arms. Less frequently myoclonic or tonic extension may lead to an opisthotonic posture. Epileptic spasms usually last 2–10 seconds and frequently occur in clusters. Short myoclonic contractions may mix with tonic contractions in one cluster. The ictal EEG of patients with West syndrome during epileptic spasms typically shows an attenuation of the background activity and depending on the resolution of the EEG system a low-amplitude high-frequency pattern (Figure 51.10). This seizure type is age specific and also occurs in focal epilepsies with different epileptogenic zones. Well established examples have been published like for instance an 11-month-old with epileptic spasms secondary to a right temporal hamartoma which was seizure free postoperatively.23 Consequently, Epileptic Spasm West–Syndrome Fp1–F3 F3–C3 C3–P3 P3–O1 FP2–F4 F4–C4 C4–P4
Epileptic spasms
P4–O2 FZ–CZ
Epileptic spasms typically occur between 3–12 months of age. They are a frequent seizure type in children with West syndrome and in this context have also been called ‘infantile spasms’.76 Epileptic spasms consist of relatively symmetric tonic and myoclonic features, which may vary in the same patient from one seizure to another. The muscle contractions predominantly affect the proximal and axial muscles and typically lead
CZ–PZ EKG
1 sec
100 µV
Figure 51.10. The epileptic spasm of this 8-month-old child with West syndrome is electroencephalographically associated with a diffuse attenuation of the hypsarrhythmia during the seizure.
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epileptic spasms do not allow localization. Children with epileptic spasms typically develop other seizure types after the age of 3–5 years77 as in the above-mentioned case, in whom at the age of 2 1/2 years mild automatisms occurred.23
Versive seizures Versive seizures consist of a sustained, unnatural turning of the eyes and head to one side.37 The version usually consists of a smooth, tonic lateral deviation of the eyes with, not infrequently, a clonic superimposed component. Often the angle of the mouth is also deviated to the same side and the neck is extended. These seizures are the expression of epileptic activation of the frontal eye field (inferior/medial frontal gyrus) that is contralateral to the side to which the eyes turn.60,78 Epileptic activation from the temporal lobe or other structures distant from the frontal eye fields may spread into the frontal eye field, giving rise to versive seizures.37 In temporal lobe epilepsy, version occurs when the patient has already lost consciousness and the version is frequently preceded by oral and maunal automatisms (automotor seizure). A study of patients with extratemporal and temporal epilepsies showed that version occurred earlier than 18 seconds in seizures with an extratemporal onset and later than 18 seconds in the vast majority of temporal lobe epilepsies,79 which reflects faster spread to the frontal eye fields from extratemporal particularly
frontal lobe regions than from the temporal lobes. Patients may be unconscious (n=16) or conscious (n=7) depending from which region of the cortex the seizures originated in 222 patients considered for epilepsy surgery at the Montreal Neurological Institute.80 The early 1980s witnessed a controversy surrounding the lateralizing value of versive seizures in temporal epilepsy.81,82 Then Wyllie et al. defined version as a forced, sustained, and unnatural movement. On the basis of this definition, versive seizures have a high lateralizing significance to seizure onset in the contralateral hemisphere, particularly when they occur immediately before a generalized tonic-clonic seizure.46 The mechanisms involved in the contralateral head version is not well understood considering that for a version of the head to the contralateral side the ipsilateral sternocleidomastoid muscle needs to be activated.83 Quantitative movement analysis was able to demonstrate that in temporal lobe epilepsy there is a initial ipsilateral head turning followed by a contralateral head version which last longer and occurs prior to secondary generalization.78
Tonic-clonic seizures Tonic-clonic seizures are characterized by a typical sequence of a generalized tonic contraction followed by clonic contractions. Grand mal (= ‘the great evil’) is a synonym for generalized
EMG Artifactduring a Generalized Tonic-Clonic Seizure FP2–F8 50 uV F8–T8 T8–P8 P8–O2 FP1–F7 F7–T7 T7–P7 P7–O1 FP2–F4 F4-C4 C4–P4 P4–O2 FP1–F3 F3–C3 C3–P3 P3–O1 FZ–CZ CZ–PZ EKG1–EKG2
(a) FP2–F8 50 uV F8–T8 T8–P8 P8–O2 FP1–F7 F7–T7 T7–P7 P7–O1 FP2–F4 F4-C4 C4–P4 P4–O2 FP1–F3 F3–C3 C3–P3 P3–O1 FZ–CZ CZ–PZ EKG1–EKG2
(c)
FP2–F8 50 uV F8–T8 T8–P8 P8–O2 FP1–F7 F7–T7 T7–P7 P7–O1 FP2–F4 F4-C4 C4–P4 P4–O2 FP1–F3 F3–C3 C3–P3 P3–O1 FZ–CZ CZ–PZ EKG1–EKG2
(b) FP2–F8 50 uV F8–T8 T8–P8 P8–O2 FP1–F7 F7–T7 T7–P7 P7–O1 FP2–F4 F4-C4 C4–P4 P4–O2 FP1–F3 F3–C3 C3–P3 P3–O1 FZ–CZ CZ–PZ EKG1–EKG2
(d)
1sec
Figure 51.11. Typical EMG artifact illustrating the course of a generalized tonic-clonic seizure. Initially the tonic activity increases in amplitude (a–b) followed by gradually increasing clonic activity with periods of reduced EMG artifact (c–d). The duration of the pauses inbetween the clonic activity increases towards the end of the clonic activity. This EMG artifact is very typical for generalized tonic-clonic seizures and may even help to distinguish them from non-epileptic pseudoseizures.
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Figure 51.12. The increased intrathoracal pressure during the tonic phase may lead to subcutan petechial bleeding, which can be seen in the periorbital region of this 16-year-old male. He had his first generalized tonic-clonic seizure the day before. This phenomenon is typical for generalized tonic-clonic seizures.
tonic-clonic seizure, which is the only seizure type in grand mal epilepsies (Epilepsy with grand mal [generalized tonicclonic] seizures on awakening) (Commission on Classification and Terminology of the International League Against Epilepsy.84 The seizures have a typical evolution, initially occurring with tonic posturing, adduction with extension of all four extremities, and flexion of the wrist and fingers. This phase lasts for approximately 5 (to 12) seconds and then evolves into a ‘tremor-like’ twitching.85 The ictal EEG shows a typical EMG artifact (Figure 51.11). The repetition rate of the twitches gradually becomes slower and the amplitude increases, giving rise to the clonic phase (Figure 51.12). The clonic phase consists predominantly of flexion myoclonic
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jerks of the elbow, hip, and knee. The duration of the tonicclonic seizures varies between 1–2 minutes.85 Consciousness is always disturbed with the beginning of the tonic phase. Generalized tonic-clonic seizures are followed by a prolonged postictal coma and confusion. During the tonic phase increased intrathoracal pressure may lead to petechial subcutan bleeding in the periorbital region (Figure 51.12). Generalized tonic-clonic seizures may occur in generalized and focal epilepsy syndromes. Occasionally other generalized seizure types may evolve into generalized tonic-clonic seizures (i.e., generalized myoclonic seizure → generalized tonic-clonic seizure or dialeptic seizure → generalized tonic-clonic seizure). The evolution of generalized myoclonic seizures into generalized tonic-clonic seizures is typical for juvenile myoclonic epilepsy. In focal epilepsies, generalized tonic-clonic seizures usually constitute the end of a seizure evolution. The focal seizure types preceding a generalized tonic-clonic seizure depend on the cortical region, which gives rise to the seizure. Secondarily generalized tonic-clonic seizures may infrequently evolve into a short (2–10 sec) focal motor seizure that may be generated by persisting epileptiform discharges in the hemisphere of origin or may involve the contralateral hemsiphere (paradoxical version).86,87 The clonic phase of generalized tonicclonic seizures may end asymmetrically, showing clonic jerks persisting in the limbs ipislateral to the hemisphere of seizure onset.85 It is speculated that this seizure evolution reflects earlier seizure cessation in the hemisphere of seizure onset, whereas the contralateral hemisphere still continues to seize. Patients with juvenile myoclonic epilepsy may have generalized myoclonic seizure preceding the generalized tonic-clonic seizures, particularly after sleep deprivation. Clinical experience shows that there are some patients with clonic-tonic-clonic seizures but there are only anecdotal reports on this observation.7 The pathophysiological considerations on the origin of generalized tonic-clonic seizures are the same as discussed above for generalized tonic and generalized clonic seizures.
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Complex motor seizures: localizing and lateralizing value MM Bianchin and AC Sakamoto
Introduction Clinical signs and symptoms expressed during epileptic seizures are thought to be generated by widespread neuronal matrices, linked together by anatomic connections, and further strengthened through repeated use.1–4 Although presenting great interindividual variability such neural networks share similarities among different patients, permitting the expression of stereotyped ictal behaviors that might indicate the underlying neural substrates. When motor networks are activated during seizures, patients may exhibit motor behaviors that can be classified as simple motor seizures (reproducible by direct stimulation of the primary motor cortex) or complex motor seizures.5,6 Classifying seizures according to semiological ictal findings, and particularly according to motor behavior is especially useful during presurgical videoEEG evaluations. This semiological-oriented classification was first proposed by Lüders and colleagues as an alternative classification to that of ILAE.5,6 Semiologic Seizure Classification (SSC) might provide a more comprehensive picture of epileptic seizures, notably in patients with focal epilepsy, being very useful for both, everyday clinical practice and more specialized evaluations in epilepsy centers.7–9 The relevance of this semiological-based approach is well demonstrated by Chee and colleagues10 who reported that the epileptogenic region can be correctly lateralized by semiological analysis in 78% of patients, with positive predictive value of 94%, and very good interobserver reliability. When combined with video-EEG analysis, semiological findings might allow lateralization and/or localization of epileptogenic and symptomatogenic zone in most patients.11–13 According to the SSC complex motor seizures encompass three main seizure types: (1) automotor seizures; (2) hipermotor seizures; and (3) gelastic seizures. Automotor and hypermotor seizures are more frequently associated to temporal or frontal lobe epilepsies, respectively,5 while gelastic seizures are usually related to hypothalamic hamartoma.5,14 Complex motor behaviors may also be observed in the late course of posterior cortex seizures, once these might propagate to more anterior regions.15–18 The reader must observe four important points regarding this classification. First, the complex motor behaviors observed during seizures are usually similar to complex movements executed during common life diary activities (e.g., coughing, swallowing, lip smacking, clapping hands, among many others), or alternatively, can resemble motor behaviors 462
observed in movement disorders (e.g., limb dystonic posturing), suggesting they share common functional anatomic substrates.5 Second, the ictal motor behavior can be qualified as ipsi- or contralateral, according to the lateralization of the epileptogenic zone. Third, distinct from ILAE’s classification,19 in the SSC the term ‘complex’ refers to the complexity of the movement, and not to the patients’ state of consciousness.5 Forth, classifying seizures according to ictal motor behavior is a purely semiological concept, and therefore, based exclusively on clinical manifestations observed during seizures.5 When these ictal signs and symptoms are sequentially considered, they may additionally indicate specific propagation patterns and reflect the anatomical sites involved during seizure propagation, the sequences of these involvements, and some mechanisms of ictal spreading. The assessment of symptomatogenic motor regions and networks through ictal semiology is of paramount importance for the process of epileptogenic and symptomatogenic zone localization. In addition, ictal semiology might also hold postsurgical prognostic significance. In this chapter we will address the complex motor seizures, mainly emphasizing motor components and localizing and/or lateralizing features. Periictal complex motor phenomena, when common, stereotyped, and consistently associated with complex motor seizures will also be described, since they might also carry valuable localizing and lateralizing information. In addition, we will briefly review the existing evidences on the mechanisms and anatomic areas possibly involved in the production of complex motor seizures and associated common behaviors. Table 52.1 summarizes existing data on complex motor seizures. Preliminarily, however, a brief consideration about auras will be presented, once auras antecede complex motor behaviors in most patients.
Auras Auras are reported by most patients with automotor or hypermotor seizures. Automotor seizures are more frequently associated to temporal lobe epilepsy, and by far epigastric aura with raising sensation is the most common type of aura anteceding these seizures. Epigastric aura might also occur in association with frontal lobe epilepsy, although much less frequently.20–26 Also common in automotor seizures are auras of fear, anxiety, or other related symptoms.20,24–26 Other types of auras common to automotor seizures but less frequently
Most patients.
Very common.
10% of patients with FLE or TLE.
15–70% of patients with TLE or FLE.
50% of FLE patients. 15–20% of TLE patients. 5–28% of patients with TLE. Less than 1% of patients.
Limb automatisms
Oral automatism
Genital and sexual automatisms
Unilateral dystonic limb posturing
Unilateral tonic posturing
24% of FLE patients. 6% of TLE patients.
75% of TLE patients. 50% of FLE patients.
35% of TLE patients. 20–60% of FLE patients.
15–20% of secondary generalized seizures.
0.8–1.5% of patients.
Pelvic thrusting
Non-versive head turning
Head version
Head and eye ipsiversion at the end of generalized seizure
Unilateral eye blinking
Postictal palsy
Ipsialateral in 80% of patients.
Ipsilateral if initial head version vanish during generalization.
Contralateral in more than 90% of patients.
Usually ipsilateral (see text for details).
None.
Contralateral in most patients with automotor seizures. Contralateral in all patients.
Contralateral in 40–90% of patients.
Contralateral in more than 90% of patients.
Mostly temporal in automotor seizures.
Frontal or temporal.
Not determined. Basal ganglia (striatum) might be involved. Frontal or temporal.
Usually frontal, may be temporal.
Frontal or temporal.
Temporal.
Temporal or frontal.
Temporal or frontal.
Highly suggestive of MTLE when associated with contralateral dystonic posturing. Suggests temporal lobe. May be observed in seizures originating in frontal lobe. Frontal or temporal.
Epileptogenic zone
Not determined.
Cotralateral Boardman’s area 6 and 8.
Broadmann’s area 6 and 8.
Unknown.
Possible exhaustion or inhibition of Brodmann area 4 and 6. Unknown.
Temporal, frontal, parietal and basal ganglia (Putamen). Supplementary motor area, basal ganglia, other frontal areas cannot be excluded. Contralateral frontal lobe.
Unknown.
Limbic system.
Variable. Frontal or temporal activation. May correspond to releasing phenomena.
Simptomatogenic zone
Complex motor seizures: localizing and lateralizing value Continued
Associated with conjugate eye versions to the same side and preceding (10 seconds or less) secondary generalizations. If initial head version is maintained during seizure, late head version still contralateral to epileptogenic zone. Involvement of inferior postcentral area has been suggested.
May be observed in pseudoseizures (17% of patients). Lateralizatory value is controversial.
In hypermotor seizures, suggest frontal lobe. In automotor seizures, suggest temporal lobe. When associated with unilateral automatisms suggests mesial temporal epilepsy. May be differentiated from dystonic posturing by absence of rotational components. Probably a negative motor phenomenon. Should be differentiated from ictal unilateral immobile limb.
When automotor and associated with preserved responsiveness suggest nondominant temporal lobe (6% of TLE). Positive ictal activation or releasing phenomena.
Observation
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Poor. Lateralizatory value on depending other signs.
Usually ipsilateral in MTLE, contralateral in NTLE, and nonlateralizing in frontal lobe seizures. Nonlateralizing.
Lateralizing value
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Unilateral immobile limb
Frequency
Selected motor behaviors observed in association with complex motor seizures
Motor characteristics findings
Table 52.1
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cont’d
2% of TLE patients.
Less then 1% of patients.
2.5% of TLE patients. are in other Epilepsies.
15% of TLE patients.
9–40% of patients.
Rare.
More then 50% of FLE patients. 2–3% of TLE patients.
Rare
Ictal vomiting
Ictal spitting
Ictal urinary urge
Periictal water drinking
Periictal cough
Unilateral ear-plugging
Complex hypermotor ictal behaviors
Gelastic seizures
Nonlateralizing.
Nonlateralizing.
Suggests contralateral epileptogeni c zone.
Nonlateralizing.
Suggest nondominant epileptogenic zone.
Suggests nondominat epileptogenic zone.
Simptomatogenic zone
Highly suggestive of frontal lobe. Might be observed in seizures from other regions due to ictal propagation. Highly suggesive of hypothalamic hamartomas. Other lesions also possible, mostly frontal or temporal.
Anterior cingulated regions inolved in motor aspects of laughter. Temporal lobes involved in mirth.
Frontal lobe.
Suggest mesial temporal Unknow. Might reflect epileptogenic zone. olfactory hallucinations, Might be extratemporal. nasal secretion or abnormal amygdalar network functioning. Suggests nondominant Activation of limbic structures, temporal lobe. insula, and mesial frontal regions. Suggests nondominant Cortical activation or releasing temporal lobe or phenomena of unknown hemisphere. networks. Suggests nondominant Insular cortex, mesial frontal temporal lobe. region, medial temporal gyrus, and operculum. Suggests nondominant Amigdala, hippocampus, temporal lobe. and parahippocampal gyrus. Hypothalamus? Suggests temporal lobe. Unknown. Might be due to activation of central autonomic pathway. Suggests neocortical Auditory cortex, on superior temporal cortex. temporal gyrus.
Epileptogenic zone
Mirth is only possible with conscience preservation during at least part of the seizure.
Multiple mechanisms. Increased respiratory secretion might have a role. Probably a stereotyped response to annoying auditory phenomena. There is no consensus on the specific localization of epileptogenic or symptomatogenic zones in frontal lobes.
It is not due to bad mouth sensation, excessive salivation, or drooling. Suggests activation of specific nondominant hemispheric bladder control centers. Unknow. Propagation of ictal activity to hypothalamus has been suggested.
Unknown mechanisms.
May reflect contralateral postictal movement abnormalities or neglect.
Observation
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Suggests nondominant epileptogenic zone.
Suggests nondominant epileptogenic zone.
Ipsilateral to temporal lobe epileptogenic zone in 70–90%. Nonlateralizing in frontal lobe seizures.
Lateralizing value
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Observations: Data regarding adult patients. Motor symptoms might be observed in posterior cortex epilepsy due to seizure propagation. The general predominance of central autonomic networks in nondominant or right hemisphere might account for nondominant (right) periictal-related behaviors. Frequencies are taken from reports on different series of video-EEG monitoring. For references, consult text. Ipsilateral or contralateral refers to the epileptogenic zone. Legends: FLE = frontal lobe epilepsy; TLE = temporal lobe epilepsy, MTLE = mesial temporal lobe epilepsy; NTLE = neocortical temporal lobe epilepsy. ETLE = extra-temporal lobe epilepsy.
50–85% of MTLE patients. 10–33% of extratempor al patients.
Nosewiping
Frequency
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Motor characteristics findings
Table 52.1
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Complex motor seizures: localizing and lateralizing value observed are déjà vu, jamais vu, olfactory auras, feelings of depersonalization.20,24 Some auras preceding automotor seizures are difficult to be characterized by patients and neurologists because they consist of complex subjective symptoms exclusively felt during seizures, and not usually experienced in other contexts. It is not uncommon that patients with automotor seizures and mesial temporal lobe epilepsy have history of auras in the past that no longer exist. This should be specifically asked to patients, once past or present history of auras is an important aspect of automotor seizures. Depending on the series, 15–69% of patients have auras preceding complex motor seizures of frontal lobe origin, a region more often associated with hypermotor seizures. 21,23,27–29 These auras consist of feelings of tightness or tingling of certain body parts, auras of whole body sensation, cephalic sensation, and other nonspecific feelings.21,23,27–31 Palpitations, fear, anxiety, and even panic have also been reported, although much less frequently.21,23,27–29,32,33 When comparing seizures of temporal lobe origin with those emanating from frontal lobes, psychic, gustatory, olfactory, fear, auditory, visual, or experiential auras suggest temporal lobe seizure onset and therefore are more frequently associated with automotor seizures.24 A nonspecific general body sensation is much more suggestive of frontal lobe epilepsy, frequently preceding hypermotor seizures.23,33 Cephalic sensations or other vague complaints are nonspecific and might occur in both, automotor and hypermotor seizures. Because auras are among the first clinical seizure symptoms, they might reflect initial and more circumscribe regional alterations, having diagnostic and prognostic significances.31,34 For these reasons, detailed evaluation of auras should not be forgotten during complex motor seizures evaluations. The reader should review the chapter about auras for a more detailed discussion.
Automotor seizures Automotor seizures (SSC) or complex partial seizures (ILAE’s classification) are by far the commonest type of complex motor seizures observed in video-EEG units. Automotor seizures are more commonly observed in association with temporal lobe epilepsy. These seizures are usually preceded by auras and their most remarkable characteristics are the impairment of consciousness and the presence of automatisms (e.g., oral automatisms, and limb automatism) and/or stereotyped motor behaviors (e.g., dystonic posturing), involving mainly hands, mouth, or tongue.5 The lateralizing and localizing semiological findings in automotor seizures are rich, especially when observed in association with temporal lobe epilepsy, where the number of clinical symptoms per seizures and duration of the seizures are usually higher than in other complex motor seizures.23 Consciousness is affected, but can be preserved in variable degrees, especially when seizures originate and remain restricted to the nondominant hemisphere.10,12,35–37 In the following sections we will review in detail these automatisms and most common associated periictal motor behaviors. A short discussion about mechanisms of all these ictal or periictal motor behaviors is also presented.
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Automatisms Oral or alimentary automatisms and automatisms of limbs usually more exuberant in the upper limbs are commonly observed in automotor seizures. These automatisms are significantly more observed in temporal lobe epilepsy but can be also seen in extratemporal seizures.16,23,33,38,39 Typical automatisms observed in automotor seizures can be discrete, consisting of repetitive and stereotyped involuntary actions as is the case of oral automatisms,10,40,41 or more complex, characterized by involuntary, learned and semipurposeful complex motor acts, like fumbling, picking, or gesticulating movements.24,40,42–45 By comparing automatisms between patients with ‘pure culture’ of temporal and frontal lobe epilepsies, Kotagal and colleagues23 observed that alimentary automatisms, repetitive upper limb automatisms, perseverative automatisms, looking around and complex gestures were much more commonly seen in temporal lobe epilepsy, while hypermotor seizures were much more frequent in frontal lobe epilepsy. Indeed, although in surgical series of frontal lobe epilepsies up to 77% of patients might present some type of automatism during seizures, they are usually hyperkinetic and qualitatively distinct from automotor automatisms. These aspects will be discussed further in hypermotor seizures.21,23 Automatisms in automotor seizures may be interpreted as release phenomenon and/or the result of activation or disruptions caused by seizure propagation to limbic system, subcortical structures, and/or other cortical regions.40,45–47 In the following sections we will better characterize the most common types of automatisms associated with automotor seizures, namely, oral and gestural automatisms, and discuss their underlying mechanisms. Oral automatisms Automatisms involving the oral region including masticator movements, swallowing, lip smacking, kissing or other tongue movements are classically observed in automotor seizures from temporal lobe origin.33,40,48 However, they can also occur in extratemporal seizures, especially when ictal discharges spread and secondarily involve the temporal lobes.16,18,21,38,39,49,50 When occurring in frontal lobe epilepsy, these automatisms are more common in association with orbito-frontal seizures.21 Precise mechanisms of oral automatisms are still poorly elucidated. They may represent release phenomenon or positive activation of the limbic system.40 Electrical stimulation of limbic structures, and particularly of amygdala, can induce oral automatisms, but only when associated to clinical seizures or widespread afterdischarges.2 In line with this observation, Maillard and colleagues45 observed that oral automatisms occur relatively early during seizures initiated in medial-lateral temporal structures, but only late in medial temporal seizures, suggesting that oral automatisms require widespread dysfunction of medial and neocortical temporal lobe structures for their expression.45,51 Gestural automatisms Gestural automatisms observed in automotor seizures are far more prominent in upper limbs and face. Lower limb automatisms although less frequent and more discrete share similar mechanisms and significances.52 In unilateral temporal lobe automotor seizures, while the contralateral limb is usually tonic, dystonic, or immobile, the ipsilateral limb may present
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several different patterns of gestural automatisms.10,40,41,53–57 Depending on the series, limb automatisms are reported in more than 80% of temporal lobe epilepsy patients,10,57,58 being exclusively unilateral in more than 50% of the patients.58 Gestural automatisms are usually observed after the initial instants of the seizure, which seems to be the time necessary for the ictal spread to limbic-neocortical structures.45 During video-EEG it is useful to observe that limb automatisms are predominantly ipsilateral to the epileptogenic zone in patients with mesial temporal lobe epilepsy, but contralateral in patients with neocortical temporal lobe epilepsy.57,59 In mesial temporal lobe epilepsy, automatisms occur just before or simultaneously to dystonic posturing. This pattern suggests that ictal activity spreads from mesial temporal lobe structures sequentially to medial frontal cortex and then to striatopallidal complex, or that it spreads to medial frontal cortex and basal ganglia simultaneously.57 Unilateral ictal automatisms associated with contralateral dystonic posturing are highly suggestive of mesial temporal lobe epilepsy.58,60 However, the lateralizing value of unilateral automatisms not associated with dystonic posture has limited lateralizing value.58 When occurring isolated and left-sided, they might indicate ipsilateral epileptogenic zone. When observed right-sided, without contralateral dystonia, they have no lateralizing value.58 It is interesting to note that unilateral automatisms in automotor seizures of mesial temporal lobe origin might correspond in fact to bilateral automatisms, being the automatisms contralateral to the epileptogenic zone overridden by dystonic or tonic posture, or by ictal paresis.58,60 With very rare exceptions, automatisms observed in automotor seizures with preserved responsiveness are characteristic of epileptogenic zone in the nondominant temporal lobe.35–37,61 Gestural automatisms have complex mechanisms, most of them not elucidated yet. By stimulating the anterior gyrus cinguli and mesiotemporal structures, oral and hand automatisms can be evoked,62–64 thus suggesting that these automatisms can be caused by ictal spreading activity. However, other authors have suggested also that at least some automatisms may correspond to releasing phenomenon, not being caused by direct ictal activation.35,58,65 Genital and sexual automatisms Genital automatisms are defined as repeated ictal fondling, grabbing, scratching or other genital manipulations. They must be differentiated from other genital or seizure manifestations, like sexual or orgasmic auras, genital sensory phenomena, or hypermotor sexual automatisms.66–70 Genital and sexual automatisms are observed in about 10% of the patients referred for epilepsy surgery.71 While orgasmic auras originate from the nondominant temporal lobe,70,72,73 genital and sexual automatisms are essentially nonlateralizing, and may be seen in seizures originating from frontal as well as temporal lobes.69,71,72,74–76 According to Leutmezer and colleagues,76 the term ‘sexual’ refers to symptoms or signs with erotic components while the term ‘genital’ refers to symptoms or signs involving the genitalia but without erotic components. The quality of genital or sexual automatisms might indicate the lobe of seizure origin. Aggressive sexual pelvic or truncal movements are usually automatisms appearing in the context of hypermotor seizures associated with frontal lobe epilepsy,71,75,76 while subtle genital automatisms like fondling or grabbing the genitals are more commonly observed in
temporal lobe seizures.69,71,76 The latter occur more frequently in men and may localize the seizure onset to the ipsilateral temporal lobe only when associated to unilateral hand automatisms (70% of patients), or to the nondominant temporal lobe when associated with periictal urinary urge (in 22% of patients).69 Pelvic thrusting is a complex motor behavior that needs some consideration because it might be observed in a moderate number of patients, with different meanings. Geyer and colleagues reported that pelvic thrusting is more commonly observed in frontal lobe seizures (24% of the patients) or in pseudoseizures (17% of the patients),77 but it can be also observed in temporal lobe seizures, in a smaller percentage of cases (6% of the patients). It does not have any lateralizing value.77 The mechanisms underlying sexual and genital automatisms are also not well understood. A transitory Klüver and Bucy syndrome-like phenomenon caused by bi-temporal lobe dysfunction, a nonspecific behavioral pattern, or even a specific behavior related to limbic activation, or a reaction to other internal stimuli were all hypothesized mechanisms, but so far not corroborated by electro-clinical supportive data.69,78 Stereotyped ictal or periictal motor behaviors Prominent stereotyped motor behaviors are integrant components of complex motor seizures, mainly automotor seizures. The assessment of their semiological characteristics is of diagnostic importance since they frequently carry useful and reliable information for the localization of the epileptogenic zone. The main clinical features of the most common types of ictal stereotyped motor behaviors are described in the following sections. Dystonic limb posturing Dystonic limb posturing consists of a sustained limb posturing similar to that observed in movement disorders, very often occurring in the course of automotor seizures. Unilateral or predominantly unilateral dystonic posturing of the upper limb is perhaps the most reliable lateralizing sign in temporal lobe automotor seizures.10,54,55,57,79–84 Although less frequently it can also occur in frontal lobe epilepsy, where it might be observed latter in the course of the seizures. Depending on the series and on the clinical criteria of inclusion, dystonic posturing can be observed in 15–70% of the patients.10,40,55,57,81,82,84–86 When present, unilateral dystonic posturing is usually observed several seconds after seizure onset, suggesting that seizure propagation is necessary for producing it.87 Dystonic posturing occurs contralateral to the epileptogenic zone in more than 90% of the patients with temporal or extratemporal seizures.54,82,84,88 Contralateral dystonic posturing associated with head turning and automatisms ipsilateral to the epileptogenic zone are findings highly suggestive of mesial temporal lobe epilepsy.55,57,79,81,89 Rusu and colleagues also associated dystonic posturing with hypersalivation, somatomotor manifestations, secondary generalization, profound clouding of conscience, and prolongued postictal confusion to mesial temporal lobe epilepsy.84 Dystonic posturing may occur in different degrees of complexity and duration, and has been correlated with different seizure patterns of propagation to temporal, frontal, and parietal lobes.84,87,90,91 However, most
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Complex motor seizures: localizing and lateralizing value authors agree that direct or indirect basal ganglia activation,87,90,91 and more specifically, the putamen seems to be necessary for ictal dystonic posturing.87,92,93 PET and SPECT findings are in line with these evidences,94 and additionally revealed alterations in insula, inferior and superior frontal gyri, cingulated gyri, as well as in parietal areas.84,94 Taken together, these findings suggest that dystonic posturing results from widespread subcortical and cortical involvement of different neural networks. This observation agrees with those suggesting that dystonic posturing might be a negative predictor for good surgical outcome in mesial temporal lobe epilepsy,84,95 once broad spread of ictal activity has been previously reported to be accompanied by worse post-surgical outcome.96 Unilateral tonic posturing Contralateral tonic limb posturing, although less frequent and less specific, is also considered an important lateralizing sign in temporal lobe automotor seizures. It is observed in about 17% of temporal lobe epilepsy patients, being contralateral to the epileptogenic zone in 40 to 86% of them.54,82 Unilateral tonic limb posturing may be also observed in up to 15% of extratemporal seizures,54 being contralateral to the seizure focus in 67–89% of these patients.54,85 Tonic posturing has been differentiated from dystonic posturing by the absence of rotational or torsion components. However, it can be observed co-occurring with dystonic posturing and it has been considered as a muted expression of more classical dystonic posturing by some authors.54,84 Unilateral tonic posturing are most likely due to the activation of the supplementary motor area (SMA), although basal ganglia, cingulate gyrus, and primary motor area cannot be ruled out in the generation of tonic posturing.65,97 Unilateral immobile limb Unilateral immobile limb or unilateral ictal akinesia was initially described as ‘ictal paresis’ or ‘ictal paralysis’ and can be defined as a sudden loss of tone in one upper limb while the opposite side expresses automatisms. It is often observed during temporal lobe seizures, being considered as highly specific for lateralizing the epileptogenic zone.54 Ictal immobile limb is reported in about 5–28% of the patients, being contralateral to the epileptic focus in virtually all patients.54,98,99 It is frequently associated to ipsilateral limb automatisms, usually occurring immediately after the initial symptoms.99 In some seizures it occurs after patients had already initiated bilateral automatisms, while in others it may appear concomitantly with the onset of the ipsilateral automatisms. In about 70% of the seizures, unilateral immobile limb may precede typical ictal dystonia. In the other 30%, it may be followed by more complex automatisms, other signs of frontal lobe involvement, or secondary generalization. Authors have excluded tonic posturing as cause of upper limb immobility, despite the fact that muscle tonus had been tested in only few patients.98 Ictal paresis should be differentiated from postictal paresis or Todd’s palsy, a transient focal motor deficit that might occur after a seizure in 0.5–13.4% of the patients, depending on the series.100,101 It lasts about 3 minutes, ranging from 11 seconds to 22 minutes, usually being unilateral and contralateral to the seizure focus.101 Bilateral postictal paresis has also been described.101,102 Postictal limb paresis might be
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associated with ictal unilateral clonic activity (55.6% of seizures), dystonic posturing (47.9% of seizures), and ictal limb paresis (24.6% of seizures).100 The mechanisms underlying ictal unilateral immobile limb are not completely elucidated, corresponding probably to a negative motor sign. Ictal invasive recordings performed in few patients suggested epileptic activation of the contralateral premotor cortex, prefrontal cortex, anterior cingulate gyrus and orbitofrontal cortex as the neural substrates involved in this motor behavior.99 Congruent with these findings, negative motor responses can be elicited by stimulation of mesial and lateral frontal lobe regions.103–105 Eyes motor behaviors Conjugated and sustained tonic versive eye movement occurring shortly before generalization is the most reliable ocular sign for seizure lateralization. It usually occurs associated to head version. Both, head and eyes version, frequently appear contralaterally to the epileptogenic zone,106,106,107 due to seizure propagation to Broadman’s area 8. Although they are simple motor phenomena, they were included here because head and eyes version may be observed in the context of complex motor seizures. Unilateral eye blinking is rare and may be observed in about 0.8 to 1.5% of seizures from patients referred to video-EEG, being ipsilateral to the epileptogenic area in about 80% of the patients.65,108,109 The mechanisms underlying ipsilateral ictal eye blinking are still unclear. Nistagmus is another eye motor sign, observed in less then 1% of patients during video-EEG and reviewed here because it is a motor sign with lateralizing properties. Nistagmus is usually observed in association with posterior cortex epilepsy, the fast phase being contralateral to the epileptogenic zone in all well-documented cases.110–117 Mechanisms of ictal nistagmus are complex and still not elucidated. Intermitent, but periodic activation of cortical saccade areas by ictal activity, activation of slow ipsiversive smooth pursuit region, or even activation of cortical optokinetic regions and subsequently subcortical structures were all mechanism hypothesized.117 Head turning and head version Versive and nonversive head turnings are common signs of automotor seizures. Version classically defines a tonic, unnatural, and forced lateral gyratory movement while head deviation or head turning refers to other head gyratory movements with more natural and unforced components. While some controversy exists about the significance and reliability of ictal nonversive head turning as a lateralizing sign, authors agree that forced versive head movements are contralateral to the epileptogenic zone in more then 90% of cases, especially when associated to conjugated eyes version and occurring shortly (usually 10 seconds or less) before secondary generalization.10,21,43,81,85,106,107,118–121 When contralateral to epileptogenic zone, head versions are sometimes referred as adversion or contraversion. Depending on the series, head version is observed in approximately 35% of patients with temporal lobe epilepsy and in 20–60% of patients with extratemporal epilepsies, mainly frontal lobe epilepsies.10,21,43,81,85,106,107,118–121 Nonversive head turning occurs in up to 73% of the temporal lobe seizures, but its value as a lateralizing sign has been controversial.120 In focal seizures without generalization, when a single head turning occur, it is ipsilateral to the epileptogenic
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focus in up to 94% of the seizures.120 When two head turnings occur to the same direction (19% of the seizures), they are usually ipsilateral to the seizure focus. However, in focal seizures with secondary generalization, when two head turnings occur, the first is usually ipsilateral to the seizure onset and the second is contralateral to the epileptogenic zone, usually appearing shortly before generalization.81,120 Head turning or deviation can be observed in about 50% of patients with frontal lobe seizures, being also ipsilateral to the epileptogenic zone in most cases. When patients show both sides head gyratory movements, ipsilateral head turning usually occurs earlier and precedes contralateral head turning. Late ipsiversion of head and eye at the end of a generalized tonic-clonic seizure might be observed in 15–20% of patients. When initial contraversion persists during the generalization phase, late head deviation is usually contralateral. When initial contraversion vanish during the generalized phase, late version is usually ipsilateral.10,106 Head version can be elicted by direct electric stimulation of the premotor areas (Broadman’s areas 6 and 8). Thus, propagation of seizures to these areas might underlie this behavior shortly before generalization. This seems to be also the mechanism of late ipsiversion, when activation of contralateral nonepileptogenic hemisphere predominates, after the initial ictal activity in the epileptogenic hemisphere is already exhausted or inhibited.10,106,117 The mechanisms of other nonversive head turning are less well understood. The association of ipsilateral head turning with contralateral dystonic limb posturing has led some authors to associate ipsilateral head turning with seizure spreading to the basal ganglia, and more specifically to the striatum.81,120,121 However, other authors have suggested neglect of the contralateral space as the possible mechanism involved in ipsilateral head turning.107,121 Facial alterations Facial expression changes occur in virtually all types of complex motor seizures. In automotor seizures, most patients exhibit neutral facial expression and staring, but emotional facial changes (e.g., disgust, happiness, and sadness) may also be observed.122–124 Expressions of anger, surprise, or fear are not commonly seen in automotor seizures, but frequently occur in hypermotor seizures.122,124–126 Although emotional facial asymmetry is not a specific ictal motor abnormality, it deserves a brief mention here because it might help in lateralizing the epileptogenic zone. Observed in about 70% of temporal lobe epilepsy patients, inferior facial weakness is usually, but not always, contralateral to the epileptogenic zone.127–130 Ictal smile was reported in children, occurring in 11% of frontal lobe seizures, in 3% of temporal lobe seizures, and in 26% of posterior cortex seizures, where it is significantly more common. This finding might lateralize the epileptogenic zone to the nondominant hemisphere.131 Rarely, ictal cry may be observed in patients with temporal or medial frontal lobe epilepsy.132,133 Mechanisms involved in ictal facial expression changes are multiple and complex. Facial alterations might be caused by direct seizure activation or disconnections of cortical or subcortical motor areas involved in facial muscle control,122,134–139 or be provoked by ictal alterations in emotion-regulation networks. Seizures originating from or involving limbic and related structures may also activate or disrupt regions involved
in the modulation of emotional responses, provoking emotional facial alterations that can appear associated to complex motor behaviors, like fear or anger, sometimes being quite dramatic and resembling panic attacks.124,126,140 Associated emotional behavior may be observed in temporal lobe epilepsy, but extreme emotional ictal behaviors (usually intense agitation, screaming, facial expression of rage, fear, or anger) are more commonly observed in frontal lobe seizures.125,126 The analysis of the neural substrates underlying emotional responses is particularly complex, once emotions and related behaviors are difficult to be reproduced and studied under controlled situations. Nevertheless, an increasing body of evidence has pointed amygdala, prefrontal cortex, hypothalamus, cingulate cortex, orbitofrontal cortex, insular cortex, and the ventral striatum as components of a complex neural emotional network.141–144 More complex emotional motor behaviors might be related to seizure propagation to rostral cingulate (M3) or caudal cingulate areas (M4), regions that might be responsible for ‘emotional facial movements’.46,136,139 Nosewiping or nose-rubbing Many epileptic patients wipe or rub their nose during or shortly after ictal period (less then 60 secounds) and this motor behavior appears to have localizatory and lateralizing value.117,145,146 Nosewiping is significantly more frequent in mesial temporal lobe seizures than in other temporal lobe or extratemporal lobe seizures.147,148 In temporal lobe epilepsy, ictal or postictal nosewiping might be observed in 50–85% of the patients and in 43% of the seizures, while it might be observed in only 10–33% of all patients with extratemporal epilepsy.145,148,149 In automotor temporal lobe seizures, nosewiping has lateralizing properties, being performed with the hand ipsilateral to the epileptogenic zone in about 75–90% of patients.145,146,148,149 In extratemporal epilepsies nosewiping might be observed in about 50% of the patients.149 Nosewiping is uncommon in patients with generalized epilepsy, after secoundarily generalized seizures or during nonepileptic events.146 Nose wiping is hardly lateralizatory in frontal lobe epilepsy.150 The pathophysiology of ictal and postictal nose wiping remains uncertain but it might reflect ictal olfactory hallucinations or increased nasal secretions.148 Earlier ictal amygdala involvement is more common in nosewiping. This finding together with observations that amygdala has a particular role in the olfactory system2,148 might suggest that direct amygdala ictal activation or disorganization of amygdale-related neural network might play an important role in the genesis of ictal or postictal nosewiping.2,148 The use of the ipsilateral hand may be related to contralateral postictal movement abnormalities or neglect.151–153 Other stereotyped motor behaviors Some ictal or periictal complex motor behaviors may be determined by special and well-characterized physiological states that can cause stereotyped and well-defined clinical situations such as cough, urinary urgency, thirst, vomiting, spitting, orgasmic related behaviors, among others. These periictal complex motor behaviors possibly have some common points that might allow them to be grouped together. In this venue, it is interesting to note that many of these behaviors are more
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Complex motor seizures: localizing and lateralizing value commonly observed in patients with nondominant temporal lobe epilepsy. Although several mechanisms could be involved, it is tempting to hypothesize that some of these abnormal behaviors can only be observed because patients keep some degree of awareness about their own feelings, about themselves, and about the surrounding ambient during seizures. Moreover, some of these behaviors correspond to autonomic responses, and the predominance of autonomic functions in the nondominant temporal lobe has also been advocated.154 Ictal vomiting Ictal vomiting is an unusual manifestation, observed in about 2% of patients submitted to video-EEG.89,155,156 Frequently associated with nondominant temporal lobe epilepsy, it might be also observed in language-dominant temporal lobe epilepsy.155,157–163 The mechanisms of ictal vomiting are not yet completely elucidated. However, seizure activity in mesial temporal structures, other limbic structures, insula, and mesial frontal regions seems to be necessary. This association is supported by several clinical-electrografic correlations,155,158–163 direct electrical stimulation157 and evidences obtained from SPECT studies.159 Ictal spitting Ictal spitting is another uncommon ictal behavior, occurring in less than 1% of the patients referred for video-EEG monitoring.164,165 It is usually observed in seizures involving nondominant temporal lobe epilepsy,164,165 but seizures of language-dominant temporal lobe and extratemporal lobes were also reported.166 The mechanisms underlying ictal spitting remain largely unknown. Increased salivation, a rare finding also associated with nondominant temporal lobe epilepsy has not been associated with spitting in most patients.167 It appears that spitting corresponds to complex automatisms similar to other oroalimentary automatisms. The association of ictal spitting with nondominant hemisphere further suggests involvement of autonomic mechanisms. However, ictal spiting is hardly explained by bad mouth sensations, excessive salivation or drooling, as one could intuitively suppose.166,167 Ictal urinary urge Ictal urinary urge provokes characteristic motor behavior in association with seizures,168,169 usually with epileptic focus located in the nondominant hemisphere.168,169 It might be observed in 0.2–2.5% of patients during video-EEG, being more common in temporal lobe epilepsy.65,168,169 The lateralizing significance of this sign can be explained by a hemispheric specific representation of central bladder control. PET studies on brain activation during micturition in normal subjects suggested a predominance of the right hemisphere in central bladder control.170,171 The symptomatogenic zone probably involves the insular cortex, mesial frontal region or the medial temporal gyrus and operculum.168–172 Periictal water drinking Water drinking is also a characteristic behavior occasionally observed during or up to 2 minutes after an automotor seizure.154,173,174 It occurs in about 15% of patients and it is usually associated with nondominant temporal lobe epileptogenic zone. Depth electrodes recordings have evidenced
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seizures starting in the amygdala, hippocampus, and parahippocampal gyrus.153,154,174 Propagation of seizures from these structures to hypothalamus was suggested as the cause for water drinking.154 As in other nondominant temporal lobe seizures, the general predominance of central autonomic networks functioning in the nondominant hemisphere has been also advocated,154 but more specific mechanisms remain uncertain. Ictal or periictal cough Cough is a relatively common ictal or periictal finding in epilepsy, being observed in 9–40% of patients during videoEEG.175–177 Coughing may be observed in temporal lobe seizures as well as in extratemporal seizures, but it is rare in pseudoseizures. Some authors have suggested that periictal coughing is more often observed in temporal lobe epilepsy, although without lateralising properties.175–177 Mechanisms of periictal cough are complex and might differ between temporal and extratemporal lobe seizures.176,177 Nevertheless, perictal coughing is thought to be consequence of increased respiratory secretion or provoked by direct activation of the central autonomic pathways.177 Unilateral ear plugging Ear plugging may be observed in some epileptic patients, probably representing a stereotyped response to an annoying auditory phenomenon. It is usually observed in children with epilepsy and learning disabilities or poor communication skills.178 Similar to nose rubbing, ear plugging is not a primary motor seizure, but a motor behavior probably performed in response to an auditory hallucination provoked by seizures involving the contralateral superior temporal gyrus.178 Thus, this behavior may occasionally be helpful in indicating the localization of the epileptogenic zone in the contralateral auditory cortex, on the superior temporal gyrus.178
Hypermotor seizures Hypermotor (Semiological Classification) or hyperkinetic seizures (ILAE Classification) were first defined as hypermotoric turning movements and postures,42 and further detailed by Lüders and colleagues as seizures in which the main clinical manifestations consist of complex movements involving the proximal segments of limbs and trunk. These characteristics result in large movements that might appear violent when occurring in high speed.5 These seizures are commonly refereed as complex gestural automatisms, gestural motor symptoms, hyperkinetic or hypermotoric behavior.166 Motor activity includes axial motor components like trashing, jumping, or body rocking. It might involve lower or upper extremities like thrashing of the extremities, bicycling leg movements, stepping, pedaling, hand flapping, clapping, slamming, pounding, fist clenching, grasping, shaking or playing with objects. Sexual automatisms are common and characterized mainly by pelvic thrusting and aggressive genital manipulations. Vocalization, laughing, shouting, or crying are frequently associated, but considered not specific findings of hypermotor seizures.21,23,32,75,179–181 Not only the pattern of motor behavior, but also its quality, i.e., agitated, frenetic, and hyperkinetic, characterizes seizures as hypermotor seizures.
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Although movements might seems violent, emotional or affective signs are reported as minimal and rare.126,182 Nevertheless some patients might exhibit emotional components associated with hypermotor seizures,126 but these aspects cannot be easily characterized and as a consequence, they are far less studied. The combination of all these components results in the large clinical variability of hypermotor seizures and unique and very bizarre-appearing seizures, sometimes suggesting pseudoseizures for those not habituated with video-EEG. For those habituated, hypermotor seizures are perhaps too bizarre for pseudoseizures.181,183 Hypermotor seizures usually originate in the frontal lobes,42,184 but it may also begin in the temporal lobes, posterior cortex, and insula.18,39,185,186 In the next sessions we discuss hypermotor seizures and other complex motor ictal behaviors related with frontal, temporal, and insular regions, pointing some important clinical differences of these seizures. Hypermotor seizures and frontal lobe Frontal lobe seizures express one of its main function: triggering, organizing, and performing most diverse motor activity. Except for ‘frontal lobe absences’ where little or no motor activity is observed, some form of motor activity is observed in virtually all patients with frontal lobe epilepsy and more complex motor ictal behaviors are very common.21–23,32,33,38,97,166,179,181,187–192 However, it is important to remember that these seizures are not exclusively characterized by motor activity. In fact, many patients may have auras preceding complex motor ictal behaviors of frontal lobe origin.21,23,28,166,183,193 Moreover, in spite of being much less evident, motor behavior is preceded or followed by tonic muscle activity of limbs. Mainly due to the exuberance of the hypermotoric behaviors and short duration of episodes, auras and other periictal subtle muscle activities are usually underestimated, and specific efforts in their identification may be necessary. During hypermotor seizures, conscience may be preserved to some degree in many patients and this aspect, associated with the brevity of seizures might account for minimal postictal confusion.179 Considering all types of automatisms observed in surgical series of frontal lobe epilepsy, hyperkinetic automatisms seems to be the most common type of automatisms, occurring in more than 50% of these patients.21 They are usually observed early (first half) in the seizure.184 When paroxysmal dystonic movements are observed in association with nocturnal hypermotor seizures, autosomal dominant nocturnal frontal lobe epilepsy should be suspected.194–196 When associated with hyperkinetic automatisms, some other clinical characteristics classically suggest seizures originating in frontal lobe. These findings are brief seizures, seizures of sudden onset and termination, early motor signs, minimal post ictal confusion, seizures that occur in cluster, seizures occurring during sleep, and seizure with tendency to rapid generalization, although not as frequent as previously suggested.21,23,32,179–181 More recently, authors have been observing that some of these associations might be clinically nonelevant or even controversial.21,181,184,197 Nevertheless, some of these characteristics seem to be a direct consequence of seizure spreading properties in the frontal lobe. Indeed, it is interesting to note that in spite of the intense interconnections of frontal lobes with other brain regions, ictal activity of
complex motor seizures remains restricted to the frontal lobe where it originates. When propagating outside the frontal lobe of origin, it usually spreads to the contralateral frontal lobe. Because of the limited ictal spreading for an appreciable period of time, some authors were able to lateralize clinical seizure findings in up to 75% of patients with frontal lobe epilepsy.198,199 However, it is also interesting to note that the variable and often bilateral limb motor phenomena observed in hypermotor seizures of frontal lobe origin may reflect prominent multiple target corticofugal projections from the epileptogenic zone and significant projections to proximal limbs.199,200 Thus, bilaterality of clinical expression of motor components observed in hypermotor seizures from frontal lobe origin does not necessarily reflect bilateral cortical spread. When seizures spread to other brain regions outside frontal lobes, ictal activity frequently invades the temporal lobes, leading to false impression of temporal lobe seizures.181,192,201–203 Differences between complex ictal motor behaviors in frontal lobe epilepsy and temporal lobe epilepsy have been observed since Penfield and Jasper.23 Even when limited to the frontal lobe of origin, hypermotor seizures are characterized by involvement of all limbs, being bilateral, like thrashing or hitting, and include the lower limbs in movements resembling running, kicking, crossing and uncrossing the legs, or pedaling movements. They might be frenetic and bizarre, and patient may vigorously rock to and from, pound the bed or other objects with their hands, and jump or scramble about. It might be associated with pelvic trust and aggressive genital manipulation.23,75,180,204 It is not uncommon that patients yell, growl, shout expletives, bark, laugh, whistle, or hum. Head and eyes deviation are frequently observed during hypermotor seizures but are of lesser lateralizing or localizatory value, except when versive, sustained and occurring late in seizures, shortly before generalization, being in this case contralateral to the epileptogenic zone. These patients might have poor surgical prognostic.21,85,205 Conscience might be preserved during episodes, in spite of patients not being able to cooperate with test performed during the ictal period. Depending on the authors, some complex motoric behaviors observed in frontal lobe epilepsy may be seen as adapted behaviors to the environment or active interactions with surrounding objects, an observation in line with findings of some conscience maintenance during hypermotor seizures.179 When frontal lobe and temporal lobe ictal automatisms are compared, differences are indeed quite evident and should be stressed here. Perseverative automatisms and complex gestures occurring in more homogeneous and stereotyped clinical patterns are usually observed in association with temporal lobe seizures. Upper extremities automatism observed in MTLE involve the distal segments of the fingers and hands and are discrete, repetitive and stereotyped, characterizing automotor seizures.184 By contrast, upper extremity automatisms observed in most frontal lobe seizures present great clinical variability, being coarse, irregular, complex, semi-purposive, and involving more proximal muscles of shoulder, elbows, as well the hands, characterizing hypermotor seizures.184,206 Alimentary automatisms might occur in both type of epilepsy, but are more frequent and occur early in temporal lobe epilepsy.33,184 When observed in frontal lobe seizures, ‘automotor-type’ automatisms have been associated with seizure origin in orbito-frontal regions and as stated before, it might
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Complex motor seizures: localizing and lateralizing value reflect seizure propagation from frontal to temporal lobe, leading to false localization of the epileptogenic zone localizing in the temporal lobe.202,203,206 This situation might be particularly tricky in presurgical evaluation of patients with normal neuroimaging findings, where extra-caution is necessary. When multiple motor symptoms are considered together, complex motor seizures might be better characterized and understood. Differences between complex motor seizures of frontal and temporal lobe origin might be also better appreciated. In this venue, Kotagal and colleagues23 demonstrated that complex motor seizures of frontal lobe origin are characterized by a cluster of repetitive proximal upper extremity movements, complex motor activity, and hypermotor activity. In contrast, complex motor seizures of temporal lobe origin are better characterized by a cluster of oroalimentar automatisms and repetitive distal upper extremity movements. Usually but not always, alteration of conscience is associated with both seizure patterns.23 Although infrequent, mixed semiology might suggest propagation from one lobe to another. In these situations, a very careful analysis of initial symptoms and the sequence of appearance of ictal motor findings are particularly important. Such approach might indicate more precisely the initial symptomatogenic zone and the patterns of seizure propagation. When clustered together, some clinical seizure patterns may indicate the ictal activation of functionally and/or anatomically related areas, an observation that might help during clinical evaluation of patients, especially in those with normal neuroimaging findings.23 Origin of hypermotor seizures in frontal lobe Although the association between hypermotor seizures and frontal lobes overall is well accepted, there is no consensus on the specific localization of the symptomatogenic zone responsible for complex motor behavior observed in frontal lobe seizures. This fact reflects mainly the relative few studies on ‘pure culture’ frontal lobe epilepsy and series with limited number of patients included. Also account for these difficulties, the intrinsic proprieties of frontal lobe, such as its large volume as well as the complexity of connections of its neural networks, leading to rapid seizure propagation in variable spreading patterns within the frontal lobes. According to Bancaud and Tailarach, there are five different frontal regions from which complex motor seizures might originate: anterior cingulated gyrus, frontopolar cortex, orbito-frontal cortex, opercular-insular cortex, and medialintermediate region.207 More recently, hypermotor seizures have been associated with seizures originating from medial or orbitofrontal regions,206 an association further confirmed by SPECT findings in few patients.208,209 Also in hypermotor seizures, PET revealed interictal hypometabolism involving frontomesial, anterior cingulate, perirolandic, and anterior insular/frontal opercular areas.210 However, none of ictal complex motor behavioral patterns were observed to be exclusive from these regions, once there are well-documented examples of such seizures initiating in other frontal lobe regions as well.21,181,188,208 Other authors have further differentiating prefrontal seizures in ventro-medial prefrontal seizures or dorsolateral prefrontal seizures. Seizures arising from ventral or ventro-medial regions appear to correspond to those initially described as ‘complex partial seizures of frontal origin’. 179,180 Some of these patients exhibit hypermotor seizures resembling
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intense and dramatic behavioral reaction to fear, with semipurposeful gesticulation, like kicking or punching, bipedal cycling movements or attempts to escape. On its turns, seizure originating in dorso-lateral prefrontal regions might be characterized by tonic eye deviation preceding head version and complex semi-purposeful gestural automatisms that might be directed toward the same location as the gaze.179 However, as stated before, the origin of hypermotor complex behaviors within the frontal lobe is a matter of ongoing research. In spite of some seizure patterns being associated with specific frontal lobe regions by some authors, others could not observe such associations. On the contrary, they simply concluded that hyperactive seizures with frenetic automatisms, characteristic of hypermotor frontal lobe epilepsy, do not seem to be associated with any specific sublobar region within the frontal lobes.181,206 In line with this last hypothesis, a mechanism proposed for complex ictal motor behaviors observed in frontal lobe epilepsy is that epileptic activity may simply disrupt the control normally exerted by higher brain centers over other regions, allowing release phenomena or disinhibition of more primitive and stereotyped behaviors.179 It is possible that frontal lobe seizures might leads to an imbalance between internally generated control of movement and response to environmental cues.179 This phenomenon would be the basis of the complex motor behaviors observed in frontal lobe epilepsy. Nevertheless, frontal lobe epilepsy remains the next frontier.191 Whether hypermotor seizure or complex ictal motor phenomena have origin in specific subregions within the frontal lobe or not is still unknown. Studies with larger groups of patients with pure frontal lobe epilepsy, evaluated with modern neuroimaging appropriately combined with electrophysilogical techniques and proven seizure free after surgery, are necessary to solve this problem. Hypermotor seizures in temporal lobe epilepsy Much less frequently, hypermotor seizures are observed in seizures originating in the temporal lobes, even if sleeprelated.185,197 This should not be a surprise if one considers that temporal and frontal structures are highly interconnected and under certain aspects, some of these regions might be considered as a physiological continuum, as is the case of limbic and para-limbic structures. In this venue, Carreno and colleagues,185 analyzing a series of 502 patients with temporal lobe epilepsy identified only 12 individuals (2.4%) with seizures originating from mesial or neocortical temporal lobes, who exhibited complex motor behaviors similar to those observed during frontal lobe seizures. Large amplitude movements mainly involving the proximal segments of the limbs were observed in six of these patients, four other patients presented unilateral hemiballismus-like movements and the remaining two had movements affecting all four members, resembling rowing or bicycling (one patient) and violent and disorganized thrashing (the other patient). As observed by those authors, these patients might present ‘temporal lobe’ auras preceding the hypermotor phase, a finding that although far from being specific, might help differentiate hypermotor temporal lobe seizures from frontal lobe seizures. It is also possible that careful evaluation of the very early symptoms in these patients might provide additional clues for temporal lobe seizure onset, with rapid, but latter propagation
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to frontal lobes. Indeed, although the epileptogenic zone in those cases is located in the temporal lobe, there are growing evidences suggesting that the symptomatogenic zones are in fact located in the anterior cingulated cortex and/or the orbitofrontal cortex.125,126,211 This pattern of propagation with ictal discharges spreading to frontal lobe structures would explain the frontal-like symptomatology presented by this particular group of temporal lobe epilepsy patients. Surgical results in these patients are mainly dependent on the etiology of the epilepsy (mesial temporal sclerosis, malformations of cortical development, tumors, among others), being similar to those observed in patients with typical temporal lobe seizure semiology.185 Hypermotor seizures in insular lobe Ryvlin and colleges186 recently reported on three patients with medically intractable nocturnal hypermotor seizures whose depth electrodes investigation had demonstrated non-equivocal insular origin, more specifically in its anterosuperior portion. This observation was further corroborated by additional findings, with patient’s habitual seizures being triggered by electrical stimulation in one patient, and interictal spikes over the insular region in the other two patients (suggesting its involvement in the origin of the hypermotor seizures). Thus, as in the case of seizures emanating from temporal lobes, seizures originating in insular regions might be associated with hypermotor behaviors as well. Epileptogenic zone in bimanual-bipedal automatisms Bimanual-bipedal automatisms are one of many automatisms observed during hypermotor seizures. However, because it is frequent, better characterized in literature, stereotyped, and easily recognizable during video-EEG, it deserves additional comments. Although usually seen as a frontal lobe clinical finding, it might be observed in few patients with seizures originating in temporal lobes as well.212,213 Swartz212 reported that bimanual-bipedal automatisms occur in 27% of patients with frontal lobe seizure onset and in 7% of patients with temporal lobe epilepsy. Disputing this, other authors report these behaviors as being exclusive of frontal lobe epilepsy semiology.23 According to Swartz mesio and/or latero-temporal plus orbital areas seem to be activated in seizures originating from temporal lobes, while dorsolateral and mesiofrontal areas were more commonly activated in seizures originating from the frontal lobes.212 Thus, although symptomatic areas of bipedalbimanual automatisms are frontal lobes, epileptogenic areas might be frontal or temporal. Gyratory ictal behavior Gyratory ictal behavior, commonly refereed as gyratory seizures, is characterized by ictal rotation usually around the body axis for at least 180 degrees.214 It was included here because gyratory ictal behaviors might be observed as integrant components of complex motor seizures. It is a non usual ictal clinical finding, observed in about 4% of patients referred to epilepsy surgery and hardly observed in pseudoseizures.183 Gyratory ictal behaviors are more commonly observed in
seizures originating from frontal lobes, but it might be also observed in seizures originating from the temporal lobes.214 Gyratory ictal behaviors might have localizatory and lateralizing value. When following a forced head version, the rotation side is usually contralateral to the epileptogenic zone. Conversely, when not preceded by a forced head version, the direction of rotation is usually toward the side of seizure onset.214 The mechanisms involved in the genesis of these behaviors are unknown.
Gelastic seizures Gelastic seizures are seizures whose main characteristics are brief periods of laughter or grimaces, accompanied or not by subjective feelings of mirth. The term ‘gelastic’ is originated from the Greek word gelos which means joy, an expression referring to the observation of laughter during seizures.14,215–219 Gelastic seizures are uncommon type of seizures, better classified apart from other complex motor seizures due to their peculiar characteristics. Although this semiological finding strongly suggests hypothalamic hamartoma as the cause of the seizures, rare patients might experience gelastic seizures due to other types of brain lesions, located in diverse brain areas.14,14,215–224 Hypothalamic hamartomas are rare but well-recognized developmental malformations of the tuber cinereum, associated with precocious puberty and gelastic seizures. Although there is a spectrum of epilepsy severity associated with hypothalamic hamartomas, patients with hypothalamic hamartomas who present the classical form of the disease develop gelastic seizures during infancy or early childhood, followed by appearance of generalized seizures associated with broad cognitive and behavioral deterioration. Endocrine disorders are also observed, leading to precocious puberty.14,14,215–219 Rare patients might experience milder forms of the disease, with seizures only characterized by pressure to laugh.225 Typically, gelastic seizures might be difficult to recognize as epileptic events until an average of 4 years. These patients are poorly responsive to pharmachological treatments. Alternatives therapies, such as vagal nerve stimulation and the ketogenic diet have not shown clear benefits. However, because gelastic seizures originate and propagate from hypothalamic hamartomas, surgical seizure control is possible. Advances in surgical techniques have allowed safe resections of hypothalamic hamartomas, leading to drastic improvements in seizure control.14,220–223,226–231 Surgical treatment is also possible in refractory cases associated with lesions other than hypothalamic hamartoma.215,217,224,232–235 In these cases the prognosis is mainly dependent on the local and extension of the lesion. As is the rule in epilepsy surgery, small epileptogenic lesions located outside the eloquent cortical areas, and whose epileptogenic zone can be completely excised, carry good surgical prognosis. The pathophysiology of gelastic seizures remains undefined but it is mainly dependent on the lesion from where seizures emanate. In the case of hypothalamic hamartomas, investigations involving ictal recordings from implanted electrodes, including electrode contacts placed directly into the hypothalamic hamartoma, suggested that gelastic seizures arise directly form these lesions.14,236 Recently, Wu and collegues237
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Complex motor seizures: localizing and lateralizing value have demonstrated that hypothalamic hamartoma cells exhibit intrinsic pacemaker-like activity, a finding suggesting these cells might underlay the genesis of epileptic activity. Although this finding might provide evidences for seizure generation, less is known about the microcellular network associated with these cells or the hypothalamic hamartoma neural network involved in seizure spreading.237–244 Although seizures seem to originate in the hypothalamic hamartoma itself, the neural networks and pathways which are activated during seizure propagation seem to be directly responsible for promoting the laughter or joy and different patterns of propagation might account for some clinical variability of gelastic seizures. These circuits are still not completely defined. Circuits involved in physiological laughter and/or mirth seem to be activated during seizure propagation in these patients, resulting in the gelastic seizures. The same brain networks might be activated during gelastic seizures originated from other brain lesions that not hypothalamic hamartomas. Although various anatomical regions may elicit laughter, it seems that the anterior cingulate regions are involved in the motor aspects of laughter, while temporal lobes, and particularly its basal regions, seem to be mainly involved in the processing of mirth.217,233,238,245 Although laughter is quite evident in these patients, mirth is a subjective sensation and patients need to keep some degree of awareness of the seizures in order to be able to report it.
Complex motor seizures in children Clinical features of complex motor seizures are distinct in children. Not only the etiological profile and associated pathologies are diverse246–249 but differences in brain maturation also seem to influence seizure semiology.41,42,246–248,250–256 Adapting Gloor’s concepts,1 it is probably appropriate to consider that clinical phenomenology of seizures in children is generated by widespread immature neuronal matrices, not fully specialized, linked together by still in-development anatomical connections that are just beginning to become strengthened through repeated use.1,2 Indeed, it is during brain maturation that neuronal matrices are formed and wired together, creating the organized and specific neuronal networks characteristic of adult life. In immature neural matrices, the epileptic electrical activity seems to evolve according to patterns of propagation distinct from those observed during adulthood.251,257 Differences in propagation patterns seem to be influential to the clinical course of complex motor seizures in children. These theoretical considerations are important once they might help to explain the occurrence of a certain gradient of motor findings between childhood and adulthood, evolving from more simple, prominent and broader, to more elaborate, discrete, and focal complex motor patterns. In children under 3–4 years old with temporal lobe epilepsy, seizures tend to manifest with prominent tonic, clonic, or myoclonic patterns that are sometimes bilateral and symmetrical, with ictal characteristics closer to seizures from generalized epilepsy syndromes. Although lateralising signs might be observed with very good interobserver agreement in up to 75% of children under 13 years old, the lack of specific clinical lateralizing signs, especially unilateral automatisms,
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dystonic posturing, version, postictal dysphasia, and postictal facial wiping is not unusual in young children.256 Postictal nose wiping, unilateral tonic seizures, Todd’s paralysis, unilateral clonic seizures, and ictal nistagmus are among lateralising signs observed earlier.42,246,248,251,258–262 When automatisms are observed, they tend to be less elaborated and are usually restricted to oroalimentar automatisms.251 These features may be also seen in focal epilepsies originating in other brain areas.249,258–261 As the child grows, the motor manifestations become more elaborated. These modifications seem to become clinically evident after 3.5–4 years of life, probably coinciding with more advanced stages of brain maturation.251 At these later stages, motor signs become progressively less prominent, giving room to more complex automatisms that increases in complexity as the child grows. At this age, many children might also show dystonic posture or versive movements.42,246 After six years of age, motor phenomenology of temporal lobe seizures become similar to that observed in adults.42,246,248,256 As can be concluded from above, complex motor seizure analysis is particularly challenging in young children, once they present less frequently lateralizing and localizing signs, and they are usually unable to give reliable information about auras or other subjective symptoms. Oller-Daurella and Oller,263 studying focal seizures in 154 children during the first 3 years of life observed that only 23% of them had focal ictal signs suggestive of focal pathologies. All the others had nonfocal seizures. In a postsurgical retrospective analysis, Loddenkemper and colleges262 studied ictal lateralizing findings in infants from 1 to 32 months of age with focal epilepsy. They observed reliable lateralizing motor signs in only 58% of the seizures, in 63% of the children, mostly consisting of lateralized simple motor seizures. Complex motor behaviors were not observed or were not reliable for focus localization.262 Head and eye version were common, but shifted laterality, consequently being nonreliable as lateralizing signs.262 In young children, temporal, temporo-parietal, or occipital lobe seizures are more commonly characterized by impaired responsiveness and awareness (difficult to evaluate in very young children) and decreased motor activity. This pattern is usually referred as hypomotor seizures. Hypermotor seizures might occur, but it is sporadic.56,252,264 These seizures are clearly distinct from seizures initiating in frontal, central, fronto-central or fronto-parietal regions, that are characterized by motor alterations consisting of tonic, atonic, or clonic movements.56,264 Pediatric frontal lobe epilepsy might be especially challenging for epilepsy surgery. When compared with those children with temporal lobe epilepsy, children with frontal lobe epilepsy had more frequent seizures, seizures of brief duration, and seizures occurring more often during sleep. Other characteristics of pediatric frontal lobe epilepsy are seizures of explosive onset with scream or cry, marked agitation during seizures, stiffening, kicking, or bicycling of legs, incontinence, and rapid recovery, with only brief postictal phase.265,266 In older children, seizures assume patters of adulthood epilepsy. In mesial temporal lobe epilepsy seizures are usually of automotor type while in patients with frontal lobe epilepsy seizures might be complex hypermotor seizures or simple motor seizures, like asymmetric tonic seizures or focal clonic signs.265 Epileptic spasms are nonspecific findings
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regarding lateralization, once it can be observed in association with focal lesions in all regions cited above.264
Final comments The reader must keep in mind that, although several aspects of complex motor seizures might help in localize and lateralize the seizure onset zone, semiological findings cannot be 100% accurate. Some discrepancy should always be expected between the epileptogenic and symptomatogenic zone once these zones are conceptually distinct, and although overlapping is common, there exist considerable intra- and interpatient variability. Also because of this variability, exceptions in the lateralizing and localizatory value of many signs may be expected. Nevertheless, careful descriptions of the complex motor findings observed during ictal periods are accurate enough for correct semiological seizure classification, frequently providing useful evidences supporting surgical decisions.7–9 In this venue, besides studying isolated clinical signs
and describing them in detail, epileptologists should also concentrate research efforts in specifying common patterns of composed motor behaviors, as well as in the establishment of common patterns of temporal and sequential evolution of these behaviors. Although not practical during actual routine presurgical evaluation, it is however possible that such analysis might be particularly relevant in near future. For example, combining two motor signs might improve the diagnostic power of the epileptogenic zone, as is the case of ipsilateral automatism associated with contralateral dystonic posturing in automotor seizures. Also, some patterns might have prognostic significances, as is the case of patients that evolve to generalization during ictal spreading of mesial temporal lobe seizures.95 For these matters, cluster analysis,184,267 neuroetholgy,268 or other techniques developed in order to group common events together and establish timerelated sequences of behaviors might add further insights to clinical analysis of isolated signs. We believe such approaches might help planning more tailored surgical resections in future.
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Leutmezer F, Baumgartner C. Postictal signs of lateralizing and localizing significance. Epileptic Disord 2002;4:43–8. Loddenkemper T, Kotagal P. Lateralizing signs during seizures in focal epilepsy. Epilepsy Behav 2005;7:1–17. Trinka E, Walser G, Unterberger I et al. Peri-ictal water drinking lateralizes seizure onset to the nondominant temporal lobe. Neurology 2003;60:873–6. Kramer RE, Lüders H, Goldstick LP et al. Ictus emeticus: an electroclinical analysis. Neurology 1988;38:1048–52. Panayiotopoulos CP. Vomiting as an ictal manifestation of epileptic seizures and syndromes. J Neurol Neurosurg Psychiatry 1988;51:1448–51. Van Burn JM. The abdominal aura. A study of abdominal sensations occurring in epilepsy and produced by depth stimulation. Electroencephalogr Clin Neurophysiol 1963;15:1–19. Devinsky O, Frasca J, Pacia SV et al. Ictus emeticus: further evidence of nondominant temporal involvement. Neurology 1995;45:1158–60. Baumgartner C, Olbrich A, Lindinger G et al. Regional cerebral blood flow during temporal lobe seizures associated with ictal vomiting: an ictal SPECT study in two patients. Epilepsia 1999;40:1085–91. Chen C, Yen DJ, Yiu CH et al. Ictal vomiting in partial seizures of temporal lobe origin. Eur Neurol 1999;42:235–9. Schauble B, Britton JW, Mullan BP et al. Ictal vomiting in association with left temporal lobe seizures in a left hemisphere language-dominant patient. Epilepsia 2002;43:1432–5. Shuper A, Goldberg-Stern H. Ictus emeticus (ictal vomiting). Pediatr Neurol 2004;31:283–6. Schindler K, Wieser HG. Ictal vomiting in a left hemisphere language-dominant patient with left-sided temporal lobe epilepsy. Epilepsy Behav 2006;8:323–7. Voss NF, Davies KG, Boop FA et al. Spitting automatism in complex partial seizures: a nondominant temporal localizing sign? Epilepsia 1999;40:114–16. Kellinghaus C, Loddenkemper T, Kotagal P. Ictal spitting: clinical and electroencephalographic features. Epilepsia 2003;44: 1064–9. Kellinghaus C, Lüders HO. Frontal lobe epilepsy. Epileptic Disord 2004;6:223–9. Shah J, Zhai H, Fuerst D et al. Hypersalivation in temporal lobe epilepsy. Epilepsia 2006;47:644–51. Baumgartner C, Groppel G, Feucht M et al. Peri-ictal urinary urge – a new lateralizing sign indicating seizure onset in the non-dominant temporal lobe. Epilepsia 1999;40:29. Loddenkemper T, Foldvary N, Raja S et al. Ictal urinary urge: further evidence for lateralization to the nondominant hemisphere. Epilepsia 2003;44:124–6. Blok BF, Willemsen AT, Holstege G. A PET study on brain control of micturition in humans. Brain 1997;120 (Pt 1):11–21. Blok BF, Sturms LM, Holstege G. Brain activation during micturition in women. Brain 1998;121 (Pt 11):2033–42. Loddenkemper T, Wyllie E, Neme S et al. Lateralizing signs during seizures in infants. J Neurol 2004;251:1075–79. Remillard GM, Andermann F, Gloor P et al. Water-drinking as ictal behavior in complex partial seizures. Neurology 1981;31:117–24. Bauer G, Dobesberger J, Bauer R et al. Prefrontal disturbances as the sole manifestation of simple partial nonconvulsive status epilepticus. Epilepsy Behav 2006;8:331–5. Gil-Nagel A, Risinger MW. Ictal semiology in hippocampal versus extrahippocampal temporal lobe epilepsy. Brain 1997;120 (Pt 1):183–92. Wennberg R. Postictal coughing and noserubbing coexist in temporal lobe epilepsy. Neurology 2001;56:133–4. Fauser S, Wuwer Y, Gierschner C et al. The localizing and lateralizing value of ictal/postictal coughing in patients with focal epilepsies. Seizure 2004;13:403–10. Clarke DF, Otsubo H, Weiss SK et al. The significance of ear plugging in localization-related epilepsy. Epilepsia 2003;44: 1562–7. McGonigal A. and Chauvel P. Frontal lobe epilepsy: seizure semiology and presurgical evaluation. Practical Neurology 2004;10:260–73. Williamson PD, Spencer DD, Spencer SS et al. Complex partial seizures of frontal lobe origin. Ann Neurol 1985;18:497–504. Williamson PD, Jobst BC. Frontal lobe epilepsy. Adv Neurol 2000;84:215–42. Geier S, Bancaud J, Talairach J et al. The seizures of frontal lobe epilepsy. A study of clinical manifestations. Neurology 1977;27:951–8.
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Saygi S, Katz A, Marks DA et al. Frontal lobe partial seizures and psychogenic seizures: comparison of clinical and ictal characteristics. Neurology 1992;42:1274–7. Kotagal P, Arunkumar G, Hammel J et al. Complex partial seizures of frontal lobe onset statistical analysis of ictal semiology. Seizure 2003;12:68–81. Carreno M, Donaire A, Perez Jimenez MA et al. Complex motor behaviors in temporal lobe epilepsy. Neurology 2005;65: 1805–7. Ryvlin P, Minotti L, Demarquay G et al. Nocturnal hypermotor seizures, suggesting frontal lobe epilepsy, can originate in the insula. Epilepsia 2006;47:755–65. Broglin D, Delgado-Escueta AV, Walsh GO et al. Clinical approach to the patient with seizures and epilepsies of frontal origin. Adv Neurol 1992;57:9–88. Chauvel P, Kliemann F, Vignal JP et al. The clinical signs and symptoms of frontal lobe seizures. Phenomenology and classification. Adv Neurol 1995;66:115–25. Geier S, Bancaud J, Talairach J et al. The seizures of frontal lobe epilepsy. A study of clinical manifestations. Neurology 1977;27: 951–8. Kramer U, Riviello JJ Jr, Carmant L et al. Clinical characteristics of complex partial seizures: a temporal versus a frontal lobe onset. Seizure 1997;6:57–61. Niedermeyer E. Frontal lobe epilepsy: the next frontier. Clin Electroencephalogr 1998;29:163–9. Williamson PD. Frontal lobe epilepsy. Some clinical characteristics. Adv Neurol 1995;66:127–50. Kramer U, Riviello JJ Jr, Carmant L et al. Clinical characteristics of complex partial seizures: a temporal versus a frontal lobe onset. Seizure 1997;6:57-61. Scheffer IE, Bhatia KP, Lopes-Cendes I et al. Autosomal dominant frontal epilepsy misdiagnosed as sleep disorder. Lancet 1994;343:515–17. Scheffer IE, Bhatia KP, Lopes-Cendes I et al. Autosomal dominant nocturnal frontal lobe epilepsy. A distinctive clinical disorder. Brain 1995;118 (1):61–73. Hayman M, Scheffer IE, Chinvarun Y et al. Autosomal dominant nocturnal frontal lobe epilepsy: demonstration of focal frontal onset and intrafamilial variation. Neurology 1997;49:969–75. Mai R, Sartori I, Francione S et al. Sleep-related hyperkinetic seizures: always a frontal onset? Neurol Sci 2005;26(Suppl 3): S220–4. Toczek MT, Morrell MJ, Risinger MW et al. Intracranial ictal recordings in mesial frontal lobe epilepsy. J Clin Neurophysiol 1997;14:499–506. Blume WT, Ociepa D, Kander V. Frontal lobe seizure propagation: scalp and subdural EEG studies. Epilepsia 2001;42:491–503. Williamson PD. Frontal lobe seizures. Problems of diagnosis and classification. Adv Neurol 1992;57:289–309. Quesney LF, Constain M, Rasmussen T. Seizures from the dorsolateral frontal lobe. Adv Neurol 1992;57:233–43. Munari C, Tassi L, Di Leo M et al. Video-stereo-electroencephalographic investigation of orbitofrontal cortex. Ictal electroclinical patterns. Adv Neurol 1995;66:273–95. Shihabuddin B, Abou-Khalil B, Delbeke D et al. Orbito-frontal epilepsy masquerading as temporal lobe epilepsy – a case report. Seizure 2001;10:134–8. Williamson PD, Spencer DD, Spencer SS et al. Complex partial status epilepticus: a depth-electrode study. Ann Neurol 1985;18: 647–54. Ferrier CH, Engelsman J, Alarcon G et al. Prognostic factors in presurgical assessment of frontal lobe epilepsy. J Neurol Neurosurg Psychiatry 1999;66:50–6. Jobst BC, Siegel AM, Thadani VM et al. Intractable seizures of frontal lobe origin: clinical characteristics, localizing signs, and results of surgery. Epilepsia 2000;41:1139–52. Kellinghaus C, Luders HO. Frontal lobe epilepsy. Epileptic Disord 2004;6:223–39. Harvey AS, Hopkins IJ, Bowe JM et al. Frontal lobe epilepsy: clinical seizure characteristics and localization with ictal 99mTcHMPAO SPECT. Neurology 1993;43:1966–80. Vera P, Habert MO, Landre E et al. Inter-ictal brain SPET in frontal epilepsy: correlations with stereo-electroencephalography. Nucl Med Commun 1995;16:591–8. Schlaug G, Antke C, Holthausen H et al. Ictal motor signs and interictal regional cerebral hypometabolism. Neurology 1997;49:341–50. San Pedro EC, Mountz JM, Ojha B et al. Anterior cingulate gyrus epilepsy: the role of ictal rCBF SPECT in seizure localization. Epilepsia 2000;41:594–600.
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Kerrigan JF, Ng YT, Chung S et al. The hypothalamic hamartoma: a model of subcortical epileptogenesis and encephalopathy. Semin Pediatr Neurol 2005;12:119–31. Leal AJ, Passao V, Calado E et al. Interictal spike EEG source analysis in hypothalamic hamartoma epilepsy. Clin Neurophysiol 2002;113:1961–9. Leal AJ, Moreira A, Robalo C et al. Different electroclinical manifestations of the epilepsy associated with hamartomas connecting to the middle or posterior hypothalamus. Epilepsia 2003;44:1191–5. Leal AJ, Dias AI, Vieira JP. Analysis of the EEG dynamics of epileptic activity in gelastic seizures using decomposition in independent components. Clin Neurophysiol 2006;117:1595–601. Iwasa H, Shibata T, Mine S et al. Different patterns of dipole source localization in gelastic seizure with or without a sense of mirth. Neurosci Res 2002;43:23–9. Wyllie E, Chee M, Granstrom ML et al. Temporal lobe epilepsy in early childhood. Epilepsia 1993;34:859–68. Ray A, Kotagal P. Temporal lobe epilepsy in children: overview of clinical semiology. Epileptic Disord 2005;7:299–307. Terra-Bustamante VC, Inuzuca LM, Fernandes RM et al. Temporal lobe epilepsy surgery in children and adolescents: clinical characteristics and post-surgical outcome. Seizure 2005;14:274–81. Terra-Bustamante VC, Fernandes RM, Inuzuka LM et al. Surgically amenable epilepsies in children and adolescents: clinical, imaging, electrophysiological, and post-surgical outcome data. Childs Nerv Syst 2005;21:546–51. Fogarasi A, Janszky J, Faveret E et al. A detailed analysis of frontal lobe seizure semiology in children younger than 7 years. Epilepsia 2001;42:80–5. Fogarasi A, Jokeit H, Faveret E et al. The effect of age on seizure semiology in childhood temporal lobe epilepsy. Epilepsia 2002;43:638–43. Fogarasi A, Boesebeck F, Tuxhorn I. A detailed analysis of symptomatic posterior cortex seizure semiology in children younger than seven years. Epilepsia 2003;44:89–96. Loddenkemper T, Wyllie E, Neme S et al. Lateralizing signs during seizures in infants. J Neurol 2004;251:1075–9. Fogarasi A, Janszky J, Tuxhorn I. Ratio of motor seizure components in childhood temporal lobe epilepsy. J Child Neurol 2005;20(11):932–932. Fogarasi A, Tuxhorn I, Hegyi M et al. Predictive clinical factors for the differential diagnosis of childhood extratemporal seizures. Epilepsia 2005;46:1280–5. Fogarasi A, Janszky J, Tuxhorn I. Peri-ictal lateralizing signs in children: blinded multiobserver study of 100 children < or =12 years. Neurology 2006;66:271–4. Holmes GL. Epilepsy in the developing brain: lessons from the laboratory and clinic. Epilepsia 1997;38:12–30. Fogarasi A, Janszky J, Faveret E et al. A detailed analysis of frontal lobe seizure semiology in children younger than 7 years. Epilepsia 2001;42:80–85. Fogarasi A, Boesebeck F, Tuxhorn I. A detailed analysis of symptomatic posterior cortex seizure semiology in children younger than seven years. Epilepsia 2003;44:89–96. Fogarasi A, Tuxhorn I, Hegyi M et al. Predictive clinical factors for the differential diagnosis of childhood extratemporal seizures. Epilepsia 2005;46:1280–5. Fogarasi A, Janszky J, Tuxhorn I. Peri-ictal lateralizing signs in children: blinded multiobserver study of 100 children < or =12 years. Neurology 2006;66:271–74. Loddenkemper T, Wyllie E, Neme S et al. Lateralizing signs during seizures in infants. J Neurol 2004;251:1075–9. Oller-Daurella L, Oller LF. Partial epilepsy with seizures appearing in the first three years of life. Epilepsia 1989;30:820–6. Acharya JN, Wyllie E, Lüders HO et al. Seizure symptomatology in infants with localization-related epilepsy. Neurology 1997;48:189–96. Lawson JA, Cook MJ, Vogrin S et al. Clinical, EEG, and quantitative MRI differences in pediatric frontal and temporal lobe epilepsy. Neurology 2002;58:723–9. Sinclair DB, Wheatley M, Snyder T. Frontal lobe epilepsy in childhood. Pediatr Neurol 2004;30:169–76. Wieser HG, Meles HP, Bernoulli C et al. Clinical and chronotopographic psychomotor seizure patterns (SEEG study with reference to postoperative results). Acta Neurochir Suppl 1980;30:103–12. Dal Col ML, Terra-Bustamante VC, Velasco TR et al. Neuroethology application for the study of human temporal lobe epilepsy: from basic to applied sciences. Epilepsy Behav 2006;8:149–60.
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Dialeptic seizures: localizing and lateralizing value S Noachtar
Definition Definition of dialeptic seizure The term dialeptic seizure has been introduced by us to allow for a seizure classification which is purely based on ictal seizure semiology.1,2 Dialeptic seizure refers to a seizure whose predominant ictal features are alteration of consciousness, staring and loss, or minimal motor activity. The term absence seizures, on the other hand, describes a subgroup of dialeptic seizures but also includes EEG findings in the seizure classification.3 It was the pioneering work of Gibbs and co-workers who demonstrated that in patients with absence epilepsies dialeptic seizures were associated with generalized 3 Hz spikewave complexes in the EEG.4 Ever since the term absence has been defined as an electroclinical syndrome consisting of loss of consciousness, arrest of activity and an EEG showing generalized spike-wave complexes. It seems therefore appropriate to introduce a new term which describes the ictal loss of consciousness and the arrest of motor activity emphazising a purely clinical seizure classification independent of associated EEG findings. The verb διαλειπειν is old Greek and means to interrupt, stand still, or pass out. Definitions of consciousness are subject to controversy.5,6 A clinically applicable definition of consciousness has to be restricted to awareness and responsiveness which is actually included in the proposal of the International Classification of Epileptic Seizures (ICES).3 However, there are not infrequently limitations and exceptions to this concept. Patients may not infrequently recall the command to push a button during a seizure but may have been unable to do so.7,8 Awareness and responsiveness may be disturbed differently. It has been shown recently, that patients may be fully responsive during focal seizures associated with automatisms and yet not be able to recall the events during the seizure. We could observe this phenomenon prospectively in 10% of the patients with right temporal lobe epilepsies.9 Even with simultaneous Video-EEG recordings it may be impossible to exclude that the patients failure to respond was not caused by an arrest of activity due to epileptic activation of the speech areas. Thus, assessment of consciousness during an epileptic seizure may well not be trivial and remains conceptually difficult.5 For the purpose of the present chapter we will consider that an impairment of consciousness occurred during a dialeptic seizure if either responsiveness or recall were disturbed. Clinically, dialeptic seizures frequently are associated with minimal motor activity such as eyelid myoclonia and upward
eye movements. To classify seizures in children or mentally retarded adults in whom it is sometimes impossible to assess ictal consciousness the term hypomotor seizure has been introduced.10,11 Loss of voluntary tonic motor activity may be present during dialeptic seizures and is clearly distinct from atonia of postural tone leading to drop or fall. If the predominant feature of a seizure is an inability to follow a motor command such as pressing a button with full recall of the event, the seizure should be classified as an akinetic seizure (see Chapter 54a). If motor activity is present during a dialeptic seizure it is usually restricted to some minor motor movements like eye blinking. If motor activity predominates the seizure semiology the seizure will be classified according to the specific motor activity (e.g., automotor seizure, if automatisms occur or clonic seizure left arm, if the left arm is jerking). Subgroups of dialeptic seizures A subclassification of dialeptic seizures seems justified since the above mentioned definition is quite broad. Some patients have very brief dialeptic seizures characterized by an abrupt onset and offset. These seizures when associated with bursts of generalized 3 Hz spike-wave complexes have been classified as typical absences and are usually seen in patients with absence epilepsies.3 On the other hand, the ICES identifies as atypical absences dialeptic seizures in which changes in muscle tone are more pronounced and which usually do not begin and end abruptly and are accompanied by generalized irregular slow spike-wave complexes with a repetition rate of 2.5 Hz or less.3 It has also been proposed to distinguish between ‘simple’ absences and ‘complex’ absences basically depending on the degree of motor activity associated.12,13 Clinically, this subclassification overlaps somewhat with the distinction between ‘typical’ and ‘atypical’ absences which has been proposed by the ICES.3 However, there is evidence to suggest that the distinction between typical and atypical absences depends mainly on the EEG abnormalities associated with the dialeptic seizures.14 Holmes et al.14 analyzed a total of 926 dialeptic seizures in 54 patients with generalized epilepsies and found automatisms more frequently in ‘typical absences’ and more loss of muscle tone in ‘atypical absences’. Both subtypes of dialeptic seizures usually had a sudden onset and end. The authors concluded that typical and atypical ‘absence’ seizures are not discrete entities but rather form a continuum.14 Based on the associated motor or automotor activity dialeptic seizures occurring in patients with generalized epilepsies 479
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(absences) have been subdivided in six subtypes by Penry and co-workers.15 Only about 10% of all absence seizures are characterized by lapse of consciousness usually associated with a change in facial expression (staring) and cessation of motor activity, according to Penry et al.15 Of the patients with absence seizures, 71% showed at least some clonic components.15 Dialeptic seizures with tonic components are rare (3%),15 and show an increase of muscle tone which may cause a backward movement of the head and trunk (‘retropulsiv petit mal’).16 The tonic postural movements usually include both flexor and extensor muscles of the trunk or head, but extensors typically dominate. They can be asymmetric, leading to brief versive movements. Atonic components during dialeptic seizures are usually gradual causing the head to drop slightly or objects fall of the hands. An asymmetry of the decrease of muscle tone may occur. Myoclonic jerks may intermix leading to a rhythmic appearance of a head drop. Rarely the atonia is as severe and lasts long enough to cause the patient fall. Seizures in which the loss of tone is the predominant feature should be classified as atonic seizures or astatic seizures when the patients actually falls. An atonic component occurred in about half of the patients in at least one absence seizure.15 Most patients with dialeptic seizures present some mild automatisms in at least some of their seizures. The automatisms may reflect a continuation of what the patient was doing prior to the seizure onset. The patient may, for instance, continue moving the fork or spoon or chewing if a seizure occurs while eating or continue to walk if a seizure commences while walking. However, the movements will usually be slower and not as elaborate. De novo automatisms typically include simple movements such as lip licking, grimacing, yawning, swallowing, scratching or fumbling. About 88% of the patients of Penry et al. showed some kind of automatisms during their dialeptic seizures,15 and 28% of all dialeptic seizures were subclassified as dialeptic seizures with automatisms. The occurrence of automatisms increases with seizure duration and usually oral automatisms occur first followed by manual automatisms.17 At a seizure duration of 3 seconds in 22% of the seizures automatisms were present, whereas at a seizure duration of 18 seconds in 95% of the seizures automatisms occurred.15 Seizures in which the automatisms constitute a prominent part of the seizure should be classified as automotor seizures. Some dialeptic seizures are accompanied with autonomic components such as pallor of the face, flushing, mydriasis, salivation, tachycardia, piloerection and rarely urinary incontinence. It is important to notice that in 40% of the dialeptic seizures of patients with generalized epilepsies several of the above-mentioned features occurred.15 There was a considerable overlap of the subtypes from one seizure to another in the same individual.15 Fifty percent of the patients evaluated have had only one of the above-mentioned subtypes of absence seizures.15 There are reports which will be discussed later that describe dialeptic seizures in patients with focal epilepsies. However, subtypes of dialeptic seizures are not systematically studied in these patients.18–21 Further studies are currently being undertaken to gain more insight into the semiology of dialeptic seizures in focal epilepsies.22
Relationship of dialeptic seizures with ‘absence seizures’ and ‘complex-partial’ seizures As mentioned above the term dialeptic seizure exclusively refers to an ictal seizure semiology. The ICES, however, is based on both, clinical symptomatology and EEG.3 Therefore, a seizure consisting of lapse of consciousness and minimum of motor activity, i.e., would be classified as ‘complex-partial’ seizure according to the ICES if the EEG reveals focal epileptiform activity.23–24 A seizure with essentially identical seizure semiology would be classified as an absence seizure in ICES, if the EEG showed generalized spike-wave complexes. Thus, absence seizures define an electroclinical syndrome consisting of dialeptic seizures, and less frequently other semiological seizure types like automotor seizures or akinetic seizures, occurring in association with generalized spike-wavecomplexes. Complex partial seizures of the ICES define any seizure occurring in association with an alteration of consciousness and focal epileptiform EEG discharges (or normal EEG) and clinical or imaging features suggesting a focal epilepsy. Dialeptic seizures associated with a focal EEG pattern are actually one type of complex partial seizures of the ICES. The main difference between these terms is that dialeptic seizures refer exclusively to the clinical semiology of the seizures whereas absence seizures and complex partial seizures define electroclinical complexes, i.e., the definition of the terms includes clinical semiology and a specific EEG seizure pattern. In this chapter we will use the above-mentioned clinical definition of dialeptic seizures. This will allow us to use the term dialeptic seizure independently of the EEG. Such an approach may enable us to better assess the mode of appearance and frequency of dialeptic seizures in different epilepsy syndromes and allow us to better investigate the evolution and spread of epileptic seizures.24 Relationship of dialeptic seizures with epilepsy syndromes Dialeptic seizures can occur in different epilepsy syndromes (Figure 53.1). Most patients with dialeptic seizures have generalized epilepsies such as absence epilepsy and Lennox-Gastaut syndrome. Dialeptic seizures also occur even if less frequently in other generalized epilepsies such as generalized myoclonic epilepsy and probably even less frequently in focal epilepsies.18,25–28 We recently reviewed the electronic data files of the Epilepsy Program of the Cleveland Clinic Foundation and identified 34 patients with unequivocal EEG-video documented dialeptic seizures in patients with focal epilepsies (Figure 53. 2).
Clinical characteristics of dialeptic seizures Clinical symptomatology Dialeptic seizures are seen in different epileptic syndromes and tend to vary considerably in their clinical semiology. In the literature there is no good semiological study studying systematically the differences of dialeptic seizures in different epileptic syndromes. Particularly, there is little data on dialeptic seizures in focal epilepsies. Because of this limitation it is necessary to describe the characteristics of dialeptic seizures independently for each epileptic syndrome.
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focal epilepsies
Lennox-Gastaut syndrome
DIALEPTIC SEIZURES
absence epilepsy
juvenile myoclonic epilepsy
Figure 53.1 Dialeptic seizures occur in absence epilepsy, juvenile myoclonic epilepsy, Lennox-Gastaut syndrome and in focal epilepsies.
Dialeptic seizures in patients with absence epilepsy The hallmark of dialeptic seizures in these patients is a sudden lapse of consciousness with amnesia and an arrest of volitional movements. Usually the seizures are brief, lasting about 4–10 seconds.29 Rarely (3%), dialeptic seizures last up to one minute.15–17,30 The seizures may be subtle and go unnoticed by the surrounding. The patient will typically show an arrest of whatever they were doing at the onset of the seizure. A preexisting movement like walking may however sometimes be continued for some time. If a dialeptic seizure occurs while talking, the patient may realize an interruption of the conversation but may otherwise be unaware of having had a seizure. During an dialeptic seizure the patient is unresponsive, but may grunt in reply to a question or verbal commands. Reactivity is frequently disturbed at the beginning of the seizure and is less pronounced after a few seconds.7 Browne et al.7 could demonstrate, that 4 seconds after onset of the spikewave discharges, 52% of their patients with generalized epilepsies had normal reaction time. This can be nicely documented when asking the patient to press a button using the ‘clicker test’. The patients are usually unable to follow the command to press the button but some may recall the command later8.
DIALEPTIC SEIZURES focal epilepsy syndromes __________________________________ frontal
parieto-occipital 6
11
2
15
temporal
unclassified focal
n=34
Figure 53.2 Focal epilepsies in which video-EEG documented dialeptic seizures were seen in 34 patients recorded at the Cleveland Clinic Foundation.
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During a dialeptic seizure motor activity is normally reduced to a minimum, although some minor movements may be present the longer the seizure lasts.17 These typically include clonic or versive upward eye movements, blinking or mild clonic jerks of the face or the extremities. The muscle tone may change during such attacks either presenting an increase of tone such as in a ‘retropulsiv’ movement of the trunk 16 or rarely a decrease of tone leading to dropping of the head or slumping of the trunk. The face usually gives the impression of atonic stare. The eyes become vacant giving a trance like expression. Subtle automatisms like lip smacking, swallowing, or fumbling may also occur but should not predominate otherwise the seizure would be classified as automotor seizure. Polygraphic video-EEG studies have shown that 1.2 seconds after onset ocular movements occur followed by oral automatisms about 4 seconds later and 1 second later manual automatisms develop.17 Dialeptic seizures usually end abruptly, and the patient may commence his previous activities being amnestic for the time of the seizure. Detailed videoEEG analysis supported the clinical experience that most patients demonstrate some mild motor activity during their dialeptic seizures and only rarely lapse of consciousness and arrest of motor activity are the only ictal features.15–17 Dialeptic seizure is the predominant seizure type in absence epilepsies and best described in this epilepsy syndrome. These patients account for 10–15% of epilepsy patients in the pediatric age range.31 The dialeptic seizures in these patients usually last 3 to 10 seconds, occur daily and very frequently (‘pyknolepsy’).32 The age of onset ranges from 3 to 12 years of age and girls account for approximately two-thirds of the affected.16,30 Later in life, patients with absence epilepsies frequently suffer also from generalized tonic-clonic seizures.16,29,33 In long-term follow-up studies, the proportion of patients entering remission varied between 19% to 90%.34–42 Favorable prognostic factors include normal intelligence, lack of additional generalized tonic-clonic seizures, typical 3 Hz Spikewave-complexes and initial response to medical treatment. Generalized tonic-clonic seizures occur in 35–60% of these patients.35,37,38,41 The longer the follow-up period, the poorer seems the remission rate. However, even if the dialeptic seizures have a good prognosis, generalized tonic-clonic seizures may ensue in adulthood.43 In a long-term follow-up study over 20 to 37 years, 92% of the patients, in whom the dialeptic seizures persisted beyond the age of 30 to 61 years, eventually developed generalized tonic-clonic seizures.44 Some authors subdivide absence epilepsies into childhood absence epilepsy and juvenile absence epilepsy according to the age of onset and clinical course.16,45 The patients with juvenile absence epilepsy are reported to have less frequent dialeptic seizures (‘spanioleptic’), generalized tonic-clonic seizures may precede the dialeptic seizures more frequently and the EEG shows more irregular and fast spike-wave-complexes and a higher rate of photoparoxysmal responses 46 as compared to the childhood absence epilepsy group. These differences are considered to reflect genetically different traits.47 Others have questioned the clinical significance of this subdivision of absence epilepsies and propose a continuum of idiopathic generalized epilepsies with a great deal of overlap.48–51 The issue is at present not resolved, but subclassification of the absence epilepsies may be justified in the light of further
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genetic studies47 and possible different prognosis.42,51 Childhood absence epilepsy showed less seizure relapse after discontinuation of antiepileptic medication (19%) than juvenile absence epilepsy (33%),42 but this observation was not supported by others.51 The ictal EEG usually reveals regular spike-wave-complexes which show a repetition rate of 3 Hz. The spikes may be more blunt and the repetition rate will drop the longer the dialeptic seizures last. Patients with absence epilepsies are particularly sensitive to hyperventilation and/or photic stimulation.34,52–54 Of the 374 dialeptic seizures in the 48 patients evaluated by Penry et al., 29% occurred spontaneously. Hyperventilation which is the most potent activator in these patients, provoked 53% and photic stimulation another 18% of the dialeptic seizures.15 Both methods also activate interictal generalized spike-wavecomplexes in the EEG. The evolution of dialeptic seizures depends on the epilepsy syndrome. In generalized epilepsy syndromes the typical evolution of an dialeptic seizure is into a generalized tonic-clonic seizure.16,24 Dialeptic seizures in patients with Lennox-Gastaut syndrome It was already noticed in the early days of EEG that a slow repetition rate of generalized spike-wave-complexes at 2 Hz (‘petit mal variant’) correlates with a milder impairment of consciousness during dialeptic seizures as compared to the 3 Hz spike-wave pattern.54–55 The syndrome has been delineated later referring to patients with frequent tonic-, atonic-, myoclonic- and dialeptic seizures commencing early in childhood and being poorly responsive to medication. The patients usually have or develop mental impairment.56,57 The ICES lists these dialeptic seizures as ‘atypical’ absences (see above).3 In a pediatric age group Lennox-Gastaut syndrome accounted for 1–2%, whereas childhood absence epilepsy for 10–15% and juvenile absence epilepsy for 5%.31 In patients with LennoxGastaut syndrome the onset and end of dialeptic seizures was reported to be more gradual and not as abrupt as in the absence epilepsy patients and the attacks usually last longer. However, the video-EEG study of Holmes et al.,14 on 926 dialeptic seizures in 54 patients did not show any significant difference in the seizure onset and end between typical and atypical absence seizures. Some tonic, atonic and/or clonic movements particularly concerning the eyes and the perioral muscles and automatisms may occur. Dialeptic seizures in these patients are not precipitated by hyperventilation and photic stimulation. Hyperventilation rarely facilitates the occurrence of slow-spikes-wave complexes and photic stimulation does not have any effect.58 The evolution of dialeptic seizures in these patients has not yet been systematically evaluated but they can also evolve into generalized tonic-clonic seizures. Dialeptic seizures in patients with other generalized epilepsies Dialeptic seizures are not infrequently seen in patients with other generalized epilepsies.16,59 Juvenile myoclonic epilepsy occurs in 5% of a pediatric population.31 The frequency of
dialeptic seizures in patients with juvenile myoclonic epilepsy varies between 15–40% of the patients in different studies.16,61–63 Clinically, the dialeptic seizures in this patients group do not differ from those seen in patients with absence epilepsies. However, the ictal EEG in this older age group is not as regular as in the children with absence epilepsies and shows typically irregular spike-wave complexes with a repetition rate faster than 3 Hz. Photic stimulation seems to be particularly useful in patients with juvenile myoclonic epilepsy and elicits epileptiform activity in the EEG of 30% of these patients,46 although dialeptic are rarely provoked. Rarely, other mechanisms such as reading-induced or video-game-induced dialeptic seizures have been reported.64,65 Some authors proposed the classification of an ‘epilepsy with myoclonic absences’ describing an epilepsy syndrome with patients who they felt are inbetween the idiopathic absence epilepsies and the Lennox-Gastaut syndrome.35,66–68 ‘Myoclonic absence seizures’ represent the only or predominant seizure type in these sometimes mentally retarded patients and the myoclonic components are described to be massive as compared to the mild clonic movements recognized in typical dialeptic seizures. These seizures are refractory to medication in about 50% of these patients. This syndrome has been included in the International Classification of Epileptic Syndromes.69 However, a distinction by seizure type alone appears unjustified. Patients with neurological diseases such as Batten disease, Lafora disease, or subacute sclerotic panencephalitis are rarely reported to suffer from dialeptic seizures.70–72 Dialeptic seizures in focal epilepsies Janz73 already pointed out that dialeptic seizures consisting of pure brief lapse of consciousness may occur in epilepsy syndromes other than generalized epilepsies as well and therefore proposed the term ‘pyknoleptic petit mal’ for dialeptic seizures in patients with childhood absence epilepsy. Although several textbooks on epilepsy mention that dialeptic seizures may also occur in focal epilepsies, our knowledge at present is very limited.16,73 Only few data and scattered reports are available which mainly deal, although not exclusively, with patients with frontal lobe epilepsies.25,28 An abrupt ictal onset and end which is a typical feature of dialeptic seizures in childhood absence epilepsies seems also to occur in patients with frontal lobe epilepsies. This observation prompted the French school to coin the term ‘frontal absence’.27,74 Fronto-mesial and fronto-orbital seizure onset has been associated with this kind of seizure.27,74 ‘Complex partial seizures’ including dialeptic seizures (frontal absences) have been reported to occur in 161 seizures of medial intermediate frontal onset of 39 patients.27,74 However, the relative frequency of dialeptic seizures (frontal absences) was not specified. The symptoms observed during these ‘frontal absences’ include disturbance of consciousness (loss of contact), speech arrest, arrest of movements, simple gestures (automatisms), conjugate deviation of the eyes and head, and immediate recovery of consciousness.27,74 Patients with temporal lobe epilepsies not infrequently also have seizures consisting of an arrest of movement and lapse of consciousness without automatisms or other
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Dialeptic seizures: localizing and lateralizing value motor movements.21,78 Because these seizures resemble the dialeptic seizures (‘absences’) seen in patients with generalized epilepsies the term ‘pseudoabsence’ has been proposed.26,78,79 Karbowski et al. described this phenomenon in 5 of 12 children evaluated.80 Wieser et al. reported that ‘pseudoabsence’ seizures have been the predominant seizure type in 2 out of 25 patients evaluated.79 Shimizu et al. reported that the interictal PET regional hypometabolism was identical in 18 temporal lobe patients regardless whether they had seizures characterized by automatisms (‘automotor seizure’) or motionless staring (‘dialeptic seizures’).81 Wieser subclassified focal seizures arising from frontal and temporal lobe according to seizure onset as documented by depth recordings.82 However, no clear clinical distinction was made with regard to dialeptic seizures. Recently, a study using cluster analysis in seizures of patients with frontal and temporal lobe epilepsies concluded that dialeptic seizures may occur in both syndromes and cannot be distinguished on clinical grounds only. The distinction of dialeptic seizures consisting of an arrest of movement and lapse of consciousness arising from the temporal lobes and dialeptic seizures particularly in patients with Lennox-Gastaut syndrome (‘atypical’ absences) is sometimes impossible based on clinical semiology.83 We reviewed the database at the Epilepsy Monitoring Unit of the Cleveland Clinic Foundation from 1991 to 1995 looking for patients who underwent prolonged video-EEG Monitoring and in whom at least one unequivocal dialeptic seizure was recorded. Dialeptic seizures were defined purely on clinical grounds as seizures in which arrest of activity and lapse of consciousness were the predominant ictal features, and other features such as automatisms are not as prominent. We identified 34 patients with focal epilepsies in whom dialeptic seizures were documented by EEG and video. Fifteen of these 34 patients had focal epilepsies of one hemisphere but the epileptogenic zone could not be localized further. Eleven patients had temporal, six patients frontal and another two had parieto-occipital lobe epilepsies (Figure 53.2). The proportion of patients with temporal lobe epilepsy may be biased because these patients tend to be over-represented in epilepsy surgery centers. In focal epilepsies hyperventilation may provoke focal epileptiform discharges in up to 10% of the patients, but it is not known whether this activates dialeptic seizures. Photic stimulation is not an activator of focal seizures except rarely in parieto-occipital epilepsies. It is not known if dialeptic seizures can be triggered by photic stimulation. The semiology of the dialeptic seizures was similar independent of the lobe of seizure origin. Thus, analysis of the dialeptic seizure itself did not allow differentiation of the epileptogenic zone. However, the evolution of dialeptic seizures may provide lateralizing or localizing information (see below). Dialeptic seizures may be preceded by other seizure types such as auras24,25 (see below). In focal epilepsies the evolutions are more variable: an aura may precede a dialeptic seizure and the dialeptic seizure itself may evolve into other focal seizures such as for instance into a versive seizure. At present no representative data is available as to the evolution of dialeptic seizures. There are two main reasons for this: the term ‘absence’ is by definition of ICES a generalized seizure, and ICES does not allow for classification of seizure evolution in generalized epilepsies. Recently, a study analyzed
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seizure patterns in patients with frontal and temporal lobe epilepsies and used a purely clinically-based definition of the seizure types.84 Most dialeptic seizures (identified as ‘absence’ seizures in this study) commenced without warning, but in 13 of 57 cases auras preceded the dialeptic seizures and further evolved into versive or automotor seizures.84 Pathophysiology Generalized epilepsies The advent of electroencephalography proved the epileptic origin of dialeptic seizures in generalized epilepsies. Gibbs et al. described first that ‘absence’ seizures are associated with a generalized 3 Hz spike-wave pattern in the EEG.4 Since several experimental animal models have been established which served for both the search of the underlying mechanisms of the absence epilepsies and the development of drugs against human dialeptic seizures. Examples include, amongst others, the systemic pentylenetetrazol model,85 the feline generalized penicillin model,86 the rat ICV enkephaline model,87 the systemic gamma-hydroxybutyrate model,88 the tetrahydroxyisoxosolopyridine (THIP) model,89 and genetic models such as the photosensitive Senegalese baboon (papio papio)90 or the tottering mouse.91 The concepts proposed for the generation of dialeptic seizures occurring in generalized epilepsies have been subject to much controversy. Two contrary hypotheses have been debated for decades.92 The centrencephalic theory (Montreal school) proposed that a thalamocortical mechanisms capable of inducing spindles and recruiting responses were involved in the production of generalized spike-wave discharges and typical dialeptic seizures.93,94 It has been postulated that brain stem structures as also the thalamus may play an essential role in the pathogenesis of dialeptic seizures. A recent study using functional MRI supported this view and showed that, during absence seizures of a patient with absence epilepsy, the BOLD effect in the frontal cortex was reduced whereas it was increased in the thalamus.95 In contrast to this concept it has been stated that generalized spike-wave discharges are a cortical phenomenon.96,97 Both concepts were based on the results of experimental studies in animals. In an attempt to reconcile these apparently conflicting views, the corticoreticular hypothesis has been put forward. It postulated that generalized spike-wave discharges result from an abnormal interaction of cortical and diffusely projecting subcortical thalamic and midbrain reticular mechanisms.98,99 Based on this theory, the cortex is the primary generator of spike-wave discharges.100 It could be demonstrated that electrical stimulation of the thalamus which elicited spindles and recruiting responses in control animals elicited spike-wave complexes in cats given penicillin intramuscularly.101 On the other hand, injection of penicillin in the thalamus did not elicit spike-wave discharges, whereas diffuse application on the cortex did. Additional studies could also demonstrate a facilitating effect on spike-wave discharges through a depression of desynchronizing effects of the reticular formation.102 Several further mechanisms, such as altered properties of T-type calcium channels, increased numbers of GABA-B receptors, and changes in the subunit composition of GABA-A receptors have been postulated to be involved in the generation of dialeptic seizures in generalized epilepsies.103 Since the
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predominant clinical feature of dialeptic seizures is an inhibition of motor and cognitive function, it has been suggested that the underlying mechanisms may involve synaptic inhibition.104 It could be demonstrated in the feline generalized penicillin model, that the slow-waves of the spike-wave complexes are associated with GABA-mediated chloride-sensitive IPSPs in cortical neurons.105 Furthermore, GABA agonists like THIP can elicit ‘absence like seizures’ suggesting an effect of synaptic inhibition.89
complexes seen with dialeptic seizures in patients with generalized epilepsies points to the frontal lobes.115 Alternatively, arrest of motor activity could be an expression of the loss of consciousness. However, as mentioned before, preserved perception associated with inhibited motor activity has been documented.116 On the other hand disturbed perception with preservation of some automatic motor activity has also been observed. It therefore seems unlikely that consciousness and motor activity are disturbed by the same mechanisms.
Focal epilepsies The term ‘frontal absence’ has been coined by the French school referring to brief seizures which are clinically not distinguishable from dialeptic seizures of the generalized epilepsies. Invasive EEG recordings in these patients frequently revealed a frontal seizure onset.13,106,107 It has been suggested that epileptic discharges arising from several areas of the frontal lobe, such as intermediate frontal region, orbitofrontal region, and cingulate gyrus may elicit dialeptic seizures.20,74,79,108,109 It is intriguing that a seizure symptomatology which conceptually is so strongly associated with generalized epilepsy can have a focal seizure onset. The concept of ‘frontal absence’ was further supported by studies showing that electrical stimulation of the mesial frontal lobe can give rise to dialeptic seizures as well as to generalized spike-wave discharges at the scalp.18,26 This finding is in correspondence with the EEG observation of secondary bilateral synchrony arising from the mesial frontal lobe.28 Systematic electrical stimulation of the frontal lobe disclosed regions from which an arrest of motor activity could be elicited.110–112 Close connections between the prefrontal cortex and the nonspecific thalamic nucleus and the midline region of the intralaminar thalamic complex are known to exist.113 Seizures may arise from prefrontal cortex rapidly spread to the reticular formation causing an alteration of consciousness and generalization. Epileptic activation of the negative motor regions or the disturbance of consciousness itself may lead to an arrest of motor activity. It is not yet clear whether the frontal cortex or subcortical structures are the pacemaker of these ictal discharges, which usually involves both of them during the course of a seizure.74 Arrest of motor activity and blank staring with loss of consciousness have also been described in patients with temporal lobe epilepsies,19,80 which makes it most unlikely to be specific to a particular cortex region. Epileptic activation of limbic structures has been proposed as the pathogenesis for these dialeptic seizures but this has not yet been proven.73 Invasive recordings have shown that ictal discharges in the mesial temporal lobes may be associated with this symptomatology.82 Ictal SPECT studies in patients with temporal lobe epilepsies have shown that loss of consciousness was associated with hyperperfusion of brainstem structures as a result of spread of epileptic activity.114 Although some invasive recordings can reveal highly localized seizure onset zones, it has to be kept in mind that invasive studies only record from a very limited region of the brain. Theoretically, the degree of arrest of motor activity and loss of consciousness may be a reflection of the volume of cortex involved in the seizure discharge. It is conceivable that motor activity may be inhibited either by epileptic activity excerting an interference on the function of primary motor cortex or epileptic activation of negative motor areas which both lie within the frontal lobe. Source analysis of generalized spike-wave
Illustrative patient This 16-year-old girl has had epilepsy since the age of 14 years. The seizures were characterized by loss of responsiveness and arrest of behavior. Sometimes, her dialeptic seizures were heralded by an aura sensation of vague strangeness or familiarity (psychic aura). Postictally, she had difficulty naming objects but she could describe the use of the objects. The postictal aphasia points to seizure onset in the dominant hemisphere. Ictal EEG showed left temporal seizure pattern. Interictally, the EEG showed spikes and continuous slowing in the left temporal region. MRI showed a low grade astrocytoma in the anterior part of the left inferior temporal gyrus and ipsilateral mesial temporal sclerosis. The patient underwent a left anterior temporal resection including the tumor and remained seizure free for 5 years’ follow-up. Localizing and lateralizing significance The above-mentioned semiological features of dialeptic seizures allow to some extent to identify the epilepsy syndrome and thus the epileptogenic zone. The semiology of dialeptic seizures may provide some clues as to the epilepsy syndrome: shorter duration (< 20 s) is more likely to occur in generalized epilepsy as compared to focal epilepsy.22 Typically additional clinical factors are helpful like for instance the pyknoleptic occurrence of brief dialeptic seizures in a neurological normal child of school age which is highly suggestive of absence epilepsy. Pyknoleptic appearance was extremely rare in focal epilepsy.22 Since, by definition, little additional clinical features are associated with dialeptic seizure it is not surprising that the analysis of these phenomena provides few criteria for differentiation between different epilepsy syndromes. Blinking seems to be significantly more frequent in generalized epilepsy than focal epilepsy.22 The evolution of dialeptic seizures is important for localization and lateralization. If dialeptic seizures are preceded by an aura this fact clearly points to a focal epilepsy and the characteristics of the aura are crucial for further localization. There is scant data on which and how often lateralizing features occur during dialeptic seizures. Somatosensory auras would favor a seizure onset in the paracentral region, or abdominal auras a temporal seizure onset.117 Unilateral clonic seizures which evolved into dialeptic seizure have been reported, but the epileptogenic zone in this patient was most likely rather diffuse as documented by EEG and multiple other seizure types.24 The seizure evolution following a dialeptic seizure is also important: dialeptic seizures which evolve into hypermotor or tonic seizures are highly suggestive of a frontal seizure onset. Automotor seizures of patients with temporal lobe epilepsy frequently show some motionless stare at seizure onset.21 This evolution is typical for automotor seizures and should not be classified as dialeptic seizureÆ automotor.2,118
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Dialeptic seizures: localizing and lateralizing value Postictal phenomena, such as postictal aphasia, point to a seizure onset in the dominant hemisphere as shown in the illustrative patient. We observed a few versive seizures following dialeptic seizures which arose contralateral to the direction of the version.119 Other lateralizing phenomena, such as
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postictal coughing,120 ipsilateral nose wiping,121 sign of four,122 ictal vomiting,123 and unilateral blinking 124,125 occur probably rarely, if at all, during dialeptic seizures but no data is available of the frequency and lateralizing significance in the setting of dialeptic seizures.
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Textbook of epilepsy surgery Reutens DC, Berkovic SF. Idiopathic generalized epilepsy of adolescence: are the syndromes clinically distinct? Neurology 1995;45:1469–76. Trinka E, Baumgartner S, Unterberger I et al. Long-term prognosis for childhood and juvenile absence epilepsy. J Neurol 2004;251:1235–41. Adams DJ, Lueders H. Hyperventilation and 6-hour EEG recording in evaluation of absence seizures. Neurology 1981;31:1175–7. Sato S. Generalized seizures: absence. In: Dreifuss FE, ed. Pediatric Epileptology: Classification and Management of Seizures in the Child. Boston: Wright-PSG, 1983:65–91. Gastaut J. Clinical and electroencephalographic correlates of generalized spike-wave bursts occurring spontaneously in man. Epilepsia 1968;9:179–84. Gibbs FA, Gibbs EL, Lennox WG. Influence of blood sugar level on the wave and spike formation in petit mal epilepsy. Arch Neurol Psychiatr 1939;41:1111–16. Gastaut J, Roger J, Soulayrol R et al. Childhood epileptic encephalopathy with diffuse slow spike-waves (otherwise known as ‘petit mal variant’) or Lennnox syndrome. Epilepsia 1966;7:139–79. Lennox WG, Davis JP. Clinical correlates of the fast and slow spike-wave electroencephalogram. Pediatrics 1950;5:626–44. Blume WT. Lennox-Gastaut syndrome. In: Lüders HO, Lesser RP, eds. Epilepsy: Electroclinical Syndromes. New York: Springer, 1987:73–92. Janz D, Christian W. Impulsiv-petit mal. Dtsch Z Nervenheilk 1957;176:346–86. Panayiotopoulos CP, Obeid T, Waheed G. Absences in juvenile myoclonic epilepsy: a clinical and video-electroencephalographic study. Ann Neurol 1989;25:391–7. Asconape J, Penry JK. Some clinical and EEG aspects of benign juvenile myoclonic epilepsy. Epilepsia 1984;25:108–14. Delgado-Escueta AV, Enrile-Bacsal F. Juvenile myoclonic epilepsy of Janz. Neurology 1984;34:285–94. Loiseau P, Legroux M, Grimond P, Du Pasquier R, Henry P. Taxometric classification of myoclonic epilepsies. Epilepsia 1974;15:1–11. Ferrie CD, De Marco P, Grunewald RA, Giannakodimos S, Panayiotopoulos, CP. Video game induced seizures. (Review). J Neurol Neurosurg Psychiatry 1994;57:925–31. Singh B, Anderson L, al Gashlan M, al-Shahwan SA, Riela AR. Reading-induced absence seizures. Neurology 1995;45:1623–24. Tassinari CA, Lyagoubi S, Santo V et al. Etude des discharges de pointes ondes chez l’homme, II–Les aspects clinicques et electroencephalographiques des absences myocloniques. Rev Neurol 1969;121:379–83. Lugaresi E, Pazzaglia P, Franck L et al. Evolution and prognosis of primary generalized epilepsies of the petit mal absence type. In: Lugaresi E, Pazzaglia P, Tassinari CA, eds. Evoluation and Prognosis of Epilepsy. Bologna: Aulo Gaggi, 1973:2–22. Tassinari CA, Michelucci R. Epilepsy with myoclonic absences: a reappraisal. In: Wolf P, ed. Epileptic Seizures and Syndromes. London: John Libbey & Co, 1994:137–41. Commission on Classification and Terminology of the International League Against Epilepsy. A revised proposal for the classification of epilepsy and epileptic syndromes. Epilepsia 1989;30:389–99. Andermann F. Absence attacks and diffuse neuronal disease. Neurology 1967;17:205–12. Roger J, Pellisier JF, Bureau M et al. Le diagnostic precoce de la maladie de Lafora: importance des manifestations paroxystiques visuelles et interet de la biopsie cutanee. Rev Neurol 1983;139:115–24. Broughton R, Nelson R, Gloor P, Andermann F. Petit mal epilepsy evolving to subacute sclerosing panencephalitis. In: Lugaresi E, Pazzaglia P, Tassinari CA, eds. Evolution and Prognosis of Epilepsies. Bologna: Aulo Gaggi, 1973:63–72. Aird RB, Masland RL, Woodbury DM. The Epilepsies: A critical Review. New York: Raven Press, 1984. Bancaud J, Talairach J. Clinical semiology of frontal lobe seizures. In: Chauvel P, Delgado-Escueta AV, Halgren E, Bancaud J, eds. Frontal lobe seizures and epilepsies. Vol. 57. New York: Raven Press, 1992:3–58. Madsen JA, Bray PF. The coincidence of diffuse electroencephalograhic spike-wave paroxysms and brain tumors. Neurology 1966;16:546–55. Wieser HG, Hajek M. Frontal lobe epilepsy: compartmentalization, presurgical evaluation, and operative results. In: Jasper HH, Riggio S, Goldman-Rakic PS, eds. Epilepsy and the Functional Anatomy of the Frontal Lobe. Vol. 66. New York: Raven Press, 1995:297–320.
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Chauvel P, Kliemann F, Vignal JP et al. The clinical signs and symptoms of frontal lobe seizures: phenomenology and classification. In: Jasper HH, Riggio S, Goldman-Rakic PS, eds. Epilepsy and the Functional Anatomy of the Frontal Lobe. Vol. 66. New York: Raven Press, 1995:115–26. Karbowski K. Proceedings: Absences and absence-like seizures. Electroencephalogr Clin Neurophysiol 1975;39:531. Wieser HG, Swartz BE, Delgado-Escueta AV et al. Differentiating frontal lobe seizures from temporal lobe seizures. In: Chauvel P, Delgado-Escueta AV, Halgren E, Bancaud J, eds. Frontal Lobe Seizures and Epilepsies. Vol. 57. New York: Raven Press, 1992:267–85. Karbowski K, Vassella F, Pavlincova E, Nielsen J. Psychomotor seizures in infants and young children. (German). Z EEG-EMG 1988;19:30–4. Shimizu H, Ishijima B, Iio M. Diagnosis of temporal lobe epilepsy by positron emission tomography. ( Japanese). No to Shinkei – Brain & Nerve 1985;37:507–12. Wieser HG. Electroclinical features of the psychomotor seizure. Stuttgart: Fischer, 1983. So EL, King DW, Murvin AJ. Misdiagnosis of complex absence seizures. Arch Neurol 1984;41:640–1. Manford MR, Fish DR, Shorvon SD. An analysis of clinical seizure patterns and their localizing value in frontal and temporal lobe epilepsies. Brain 1996;119:17–40. Woodbury DM. Applications to drug evaluation. In: Purpura DP, Penry JK, Tower DB, Walter RD, eds. Experimental Models of Epilepsy – A Manual for the Laboratory Worker. New York: Raven Press, 1972:557–83. Quesney LF, Gloor P, Kratzenberg E, Zumstein H. Pathophysiology of generalized penicillin epilepsy in the cat: the role of cortical and subcortical structures. I. Systemic application of penicillin. Electroencephalogr Clin Neurophysiol 1977;42:640–55. Urca G, Frek H, Liebeskind JC, Taylor AN. Morphin and enkephalin: analgesic and epileptic properties. Science 1977;197:83–6. Snead OC. Gamma hydroxybutyrate in the monkey: effects of intravenous anticonvulsant drug. Neurology 1978;28:1173–8. Fariello RG, Golden GT. The THIP-induced model of bilateral synchronous spike and wave in rodents. Neuropharmacology 1987;26:161–5. Kiliam KF, Kiliam EK, Naquet R. An animal model of light sensitivity epilepsy. Electroenceph Clin Neurophysiol 1967;22: 497–513. Noebels JL, Sidman RL. Inherited epilepsy: spike-wave and focal motor seizures in the mutant mouse tottering. Science 1979;204:1334–6. Gloor P. Generalized epilepsy with bilateral synchronous spike and wave discharge. New findings concerning its physiological mechanisms. Electroencephalogr Clin Neurophysiol; (Suppl) 1978:245–9. Jasper H, Droogleever-Fortuyn J. Experimental studies on the functional anatomy of petit mal epilepsy. Res Publ Assoc Res Nerv Ment Dis 1947;26:272–98. Penfield W, Jasper H. Highest level seizures. Res Publ Assoc Res Nerv Ment Dis 1947;26:252–71. Aghakhani Y, Bagshaw AP, Benar CG et al. fMRI activation during spike and wave discharges in idiopathic generalized epilepsy. Brain 2004;127:1127–44. Gibbs FA, Gibbs EL. Atlas of Electroencephalography. Cambridge, MA: Addison-Wesley, 1952. Niedermeyer E, Laws ERJ, Walker AE. Depth EEG findings in epileptics with generalized spike-wave complexes. Arch Neurol 1969;21:51–8. Gloor P. Generalized cortico-reticular epilepsies. Some considerations on the pathophysiology of generalized bilaterally synchronous spike and wave discharge. Epilepsia 1968;9:249–63. Gloor P. Neurophysiological bases of generalized seizures termed centrencephalic. In: Gastaut H, Jasper H, Bancaud J, Waltregny A, eds. The Physiopathogenesis of the Epilepsies. Springfield, IL: Charles C Thomas, 1969:209–36. Fromm GH. The brainstem and seizures: summary and synthesis. In: Fromm GH, Faingold CL, Browning RL, Burnham WM, eds. Epilepsy and the Reticular Formation: The Role of the Reticular Core in Convulsive Seizures. New York: Alan R Liss, 1987:203–18. Gloor P. Generalized epilepsy with spike-and-wave discharge: a reinterpretation of its electrographic and clinical manifestations. The 1977 William G. Lennox Lecture, American Epilepsy Society. Epilepsia 1979;20:571–88.
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Gloor P, Testa G. Generalized penicillin epilepsy in the cat: effects of intracarotid and intravertebral pentylentetrazol and amobarbital injections. Electroenceph Clin Neurophysiol 1974;36:499–515. Snead OC, III. Basic mechanisms of generalized absence seizures. Ann Neurol 1995;37:146–57. Fromm GH. Role of inhibitory mechanisms in staring spells. J Clin Neurophysiol 1986;3:297–311. Giaretta D, Avoli M, Gloor P. Intracellular recordings in pericruciate neurons during spike and wave discharges of feline generalized penicillin epilepsy. Brain Res 1987;405:68–79. Geier S, Bancaud J, Talairach J et al. The seizures of frontal lobe epilepsy. A study of clinical manifestations. Neurology 1977;27:951–8. Gastaut H, Broughton R. Epileptic Seizures. Springfield, IL: Charles C Thomas, 1972. Fegersten L, Roger A. Frontal epileptogenic foci and their clinical correlations. Electroenceph Clin Neurophysiol 1961;13:905–13. Mazars G. Cingulate gyrus epileptogenic foci as an origin for generalized seizures. In: Gastaut H, Jasper H, Bancaud J, Waltregny A, eds. The Physiopathogenesis of the Epilepsies. Springfiled, IL: Charles C Thomas, 1969:186–9. Penfield W, Jasper H. Epilepsy and the functional anatomy of the human brain. Boston: Brown Little & Co, 1954. Lüders HO, Lesser RP, Dinner DS, et al. A negative motor response elicited by electrical stimulation of the human frontal cortex. In: Chauvel P, Delgado-Escueta AV, Halgren E, Bancaud J eds, Frontal lobe seizures and epilepsies. New York: Raven Press, 1992:149–58. Lüders HO, Lesser RP, Morris HH, Dinner DS. Negative motor responses elicited by stimulation of the human cortex. In: Wolf P, Dam M, Janz D, eds. Advances in Epileptology. New York: Raven Press, 1987:229–31.
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Nauta WJH. Some efferent connections of the prefrontal cortex in the monkey. In: Warren JM, Akert K, eds. The Frontal Granular Cortex and Behavior. New York: McGraw Hill, 1964:397–409. Lee KH, Meador KJ, Park YD et al. Pathophysiology of altered consciousness during seizures: Subtraction SPECT study. Neurology 2002;59:841–6. Rodin EA, Rodin MK, Thompson JA. Source analysis of generalized spike-wave complexes. 1994;7:113–19. Lüders HO, Noachtar S. Atlas and Classification of Electroencephalography. Philadelphia: W.B. Saunders, 2000. Henkel A, Noachtar S, Pfander M, Lüders HO. The localizing value of the abdominal aura and its evolution: a study in focal epilepsies. Neurology 2002;58:271–6. Noachtar S, Rosenow F, Arnold S et al. Semiologic classification of epileptic seizures. Nervenarzt 1998;69:117–26. Wyllie E, Lüders HO, Morris HH, Lesser RP, Dinner DS. The lateralizing significance of versive head and eye movements during epileptic seizures. Neurology 1986;36:606–11. Wennberg R. Postictal coughing and noserubbing coexist in temporal lobe epilepsy. Neurology 2001;56:133–4. Hirsch LJ, Lain AH, Walczak TS. Postictal nosewiping lateralizes and localizes to the ipsilateral temporal lobe. Epilepsia 1998;39:991–7. Kotagal P, Bleasel A, Geller E et al. Lateralizing value of asymmetric tonic limb posturing observed in secondarily generalized tonic-clonic seizures. Epilepsia 2000;41:457–62. Kramer RE, Lüders HO, Goldstick LP, et al. Ictus emeticus: an electroclinical analysis. Neurology 1988;38:1048–52. Benbadis SR, Kotagal P, Klem GH. Unilateral blinking: a lateralizing sign in partial seizures. Neurology 1996;46:45–8. Henkel A, Winkler PA, Noachtar S. Ipsilateral blinking: a rare lateralizing seizure phenomenon in temporal lobe epilepsy. Epileptic Disord 1999;1:195–7.
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Special seizures: localizing and lateralizing value SR Benbadis
Introduction ‘Special seizures’ are, in the semiologic seizure classification, those that cannot be classified in any of the other broad categories1 (see Chapter 34 in this volume). Thus, by definition, these seizures do not meet criteria for auras, autonomic seizures, dialeptic seizures, or motor seizures. In general, special seizures represent negative phenomena, which makes them unusual or ‘special’ among epileptic seizures. Special seizures include atonic seizures, astatic seizures, hypomotor seizures, akinetic seizures, negative myoclonic seizures, and aphasic seizures (see Chapter 32 in this book).
Astatic and hypomotor seizures These two categories of special seizures, like others in the semiologic classification, are defined by the predominant phenomenology. What they have in common is that they are also defined by the inability to characterize the mechanism of the symptoms due to lack of information. Thus, they do not represent unique or specific seizure types and do not have a clear localizing value. ●
●
Astatic seizures are seizures whose salient feature is a fall, but in which the mechanism of the fall cannot be further categorized. Thus, this category is most useful when there are incomplete data, e.g., history only or infants. If the predominant historical feature is a fall and there is no further useful information, this category (astatic seizure) is used. When more data are available, especially video-EEG recordings, more a specific seizure type should be identified in most cases. Seizure types that can result in a fall include tonic, atonic, GTC, and (more rarely) myoclonic seizures. Again, these are usually relatively easily identified with video-EEG monitoring. In occasional situations where the seizure cannot be more precisely classified even on video-EEG it is usually because they represent a ‘mixture’ of myoclonic, tonic, and atonic features2. These are usually seen in patients with symptomatic generalized epilepsies of the Lennox-Gastaut type (see tonic seizures in Chapter 53 and atonic seizures below), and in myoclonic astatic epilepsy of early childhood (Doose syndrome).2 Hypomotor seizures are those whose salient feature is immobility or a reduction in movements. As for astatic
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seizures, this category is most useful when there is incomplete data, e.g., history only. If the predominant historical feature is immobility and there is no further useful information, this category (hypomotor seizure) is used. More specific seizure types that can result in a hypomotor behavior include auras (by way of distress or distractibility), dialeptic seizures (where the predominant manifestation is an alteration of consciousness), and negative myoclonic or akinetic seizures (see below), and these can be identified more precisely with video-EEG recordings. Probably the common justified use of this category is in infants and young children where consciousness cannot be assessed. In fact, in this age group hypomotor seizures are likely a bland form of ‘complex partial’ seizures with no or minimal automatisms.3
Atonic seizures Atonic seizures are defined by loss of postural tone. This is usually abrupt and results in a fall, complete or incomplete depending on severity and the patient’s position. They frequently result in injuries. Atonic seizures are seen almost exclusively in patients with symptomatic generalized epilepsies of the Lennox-Gastaut type, so their ‘localizating value’ is that they are usually... generalized. Atonic seizures are, in fact, a type of generalized seizures in the ILAE seizure classification,4 and are typically accompanied, ictally, by generalized seizure patterns such as electrodecrement, paroxysmal fast activity, or spike-wave complexes. There is some evidence for a symptomatogenic zone in deep (nonrespectable) structures such as the brainstem reticular formation5,6 or the thalamus.7 Atonic seizures are considered relatively common in the symptomatic generalized epilepsies of the Lennox-Gastaut type because seizures that cause falls are often assumed to be atonic. However, careful video analysis shows that the majority of epileptic falls are tonic rather than atonic.6, 8 Often it is not completely clear that it is ‘atonia’ that is causing the fall, and it is instead a mixture (or sequence) of myoclonic, tonic and atonic phenomena. Atonic seizures can, rarely, be seen in focal epilepsy but this has not been clearly documented.9 However, even in patients with focal epilepsy (e.g., secondary to a focal cortical dysplasia), ictal SPECT recordings point to a strong inhibition in the bilateral motor cortexes.10 From a practical point of view,
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Special seizures: localizing and lateralizing value atonic seizures do not a have a reliable localizing value for purposes of resective surgery, and their presence should, generally, argue against pursuing resective surgery.
Akinetic seizures and negative myoclonic seizures (epileptic negative myoclonus) That electrical stimulation of the cortex can inhibit movements has been known since the seminal work of Penfield and Jasper.11 More recent studies showed that electrical stimulation of two regions in the frontal lobe elicit inability to initiate or maintain voluntary movements.12–15 The primary negative motor area lies in the inferior frontal gyrus, immediately anterior to the motor face area, close to (and often overlapping with) Broca’s area on the dominant side. The supplementary negative motor area is anterior to the face region of the supplementary sensorimotor area. Electrical activation of these negative motor areas may produce focal as well as bilateral inability to perform voluntary movements.12,13 The fact that responses to electrical stimulation are often bilateral makes these seizures difficult to lateralize on clinical (semiologic) grounds. Studies in primates support observations documenting two similar negative motor areas in the frontal lobe.12 Premotor and primary somatosensory cortex xan also produce (contralateral) negative motor responses.16,17 Epileptic myoclonus is referred to as ‘pure’ when it is not immediately preceded by positive myoclonus, enhancement of EMG, or a motor evoked potential.16 There is good evidence that the presence or absence of an antecedent positive motor phenomenon depends partly on stimulus intensity, except for the SMA where pure silent periods are obtained regardless of stimulus intensity.16 Akinetic seizures Akinetic seizures are defined, in the semiologic classification, by the inability to perform voluntary movements, not due to loss of consciousness (which would make it a dialeptic seizure), or loss of muscle tone (which would make it an atonic seizure). It should be pointed out that the term ‘akinetic seizures’ has different meanings outside of the semiologic classification. A longer duration (several seconds) differentiates it from negative myoclonic seizures, which are much briefer (see below). Akinetic seizures have been reported under other names such as ictal paresis18 and hemiparetic seizures.19 The symptomatogenic zone for akinetic seizures is most likely the primary or supplementary negative motor areas, as can be demonstrated by video-EEG recordings20 and confirmed by electrical cortical stimulation.12–15 Akinetic seizures most often affect distal (hand) muscles. Because of their proximity, the primary motor area are often simultaneously activated, producing clonic jerking of the face or tongue at the same time. Negative myoclonic seizures (epileptic negative myoclonus) Negative myoclonic seizures are brief (often 30–50 msec but by definition < 500 msec) episodes of muscle atonia, and can
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be viewed as the brief (sporadic) version of akinetic seizures. They can in fact be elicited by electrical stimulation using single or low frequency (1 Hz) stimulation.16 This is analogous, on the ‘positive’ side, to myoclonic seizures being the brief (sporadic) version of clonic seizures. They are only clinically apparent if the muscles in question are tonically used at the time (for example, outstretched hands). The muscle atonia can be documented by a silent period on EMG, which is identical whether the negative myoclonus is epileptic or nonepileptic such as asterixis. The epileptic nature of a negative myoclonus, and its symptomatogenic zone, can be documented by its time-locked association to an epileptiform EEG discharge (spike or sharp wave), which typically occurs 15–50 msec prior to the EMG inhibition.21–25 Since negative myoclonic seizures are essentially the brief (sporadic) version of akinetic seizures, their localizing value (or lack thereof) is similar, pointing to the negative motor areas mentioned above: premotor cortex16 post-central primary somatosensory,16 primary2,23 and supplementary negative motor area (dorsolateral frontal).26,27 In keeping with this, when epileptic negative myoclonus is seen in association with clear surface EEG abnormalities, the phenotype resembles benign childhood epilepsy with Rolandic spikes.28
Aphasic seizures Various speech disturbances can occur during seizures.29–31 Ictal aphasia (or dysphasia) is found in about 30% of patients with temporal lobe epilepsy.29,32 However, the term ‘aphasic seizures’ should be reserved for seizures in which aphasia is the predominant ictal symptom, and such seizures are relatively rare (the vast majority of aphasias are caused by head injury, stroke and dementia). In the International Classification of Epileptic Seizures, ‘dysphasic seizures’ are found under ‘simple partial’ seizures (with psychic symptoms), which is appropriate, since by definition aphasia requires intact consciousness. Confusingly, however, it is also stated that these seizures more commonly occur as ‘complex partial’ seizures.4 Studies of electrical cortical stimulation have identified four language areas: Broca’s, Wernicke’s and supplementary motor areas have been known since the work of Penfield and associates,33,11 while the basal temporal language area was described more recently.34–36 Identifying a language disturbance during electrical cortical stimulation requires a meticulous methodology to exclude speech impairment caused by nonspecific motor phenomena (positive, negative or apraxic).34,35 Identifying aphasia during seizures is fraught with the same difficulties, as it requires a selective impairment of language. Consciousness and awareness should be intact. If a patient has a more global impairment or is mute, aphasia may well be present but cannot be identified. As pointed out above, ictal aphasia may be difficult to elicit and diagnose in typical short-lived seizures. Thus, while some reports on ictal aphasia include cases of sporadic seizures,37–42 the majority describe cases of status epilepticus.43–51 Types of aphasia include Wernicke, conduction, anomic, and isolation (transcortical) aphasia.52 However, due to short seizure duration and concomitant symptoms, such complex classification is not possible for ictal aphasia. From a practical
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point of view, ascertaining the presence of a true language disturbances, rather than a nonspecific motor phenomenon (e.g., speech arrest) or a more global alteration in consciousness, is the crucial step. The basic dichotomy (i.e., anterior/ Broca/expressive/nonfluent vs. posterior/Wernicke/receptive/ fluent) is realistically practical for seizures, and consistent with the early reports of ictal dysphasia.32 The easiest type to identify ictally is the anterior type (Broca, nonfluent, expressive,). The posterior type (Wernicke, receptive, fluent) is more difficult to distinguish from less specific alteration of awareness. Further subtypes cannot realistically be identified ictally, which is unimportant since the type of aphasia does not reliably predict the lobe or region of seizure onset.30 The fact that subtypes of aphasia have no specific localizing value is quite consistent with the findings of cortical stimulations, where the type of aphasia may change with the stimulus intensity, and where stimulation of Broca, Wernicke, and basal temporal language areas produces relatively similar deficits.35 Localizing value Most patients with documented aphasic seizures have temporal lobe epilepsy, but this most likely reflects the predominance of such patients in monitoring units. In the only sizeable series of patients with ictal aphasia,32 30 of 34 patients (88%) had left temporal lobe epilepsy (defined preoperatively). Of 17 patients with definite localization (i.e., became seizurefree after temporal lobectomy) and ictal aphasia, 16 (94%) had left temporal
lobe seizures. Ictal aphasia can occur in seizures arising from almost any lobe, including frontal, fronto-temporal, centroparietal, parietal, temporo-parietal, posterior lateral temporal, and temporo-occipital.37,40,45,47,50,51,49,53,55 This is not surprising if one considers the four language areas defined by electrical stimulations. Furthermore, the presence of ictal aphasia in seizures of various origin is also in keeping with the important concept that distinguishes between epileptogenic zone and symptomatogenic zone56; in brief, epileptogenic zones in various locations may be in silent cortex but produce discharges which spread to one or more language areas. In additional to the ‘classical’ language areas, there is also convincing evidence incriminating the basal temporal language area.30,37,38,43 Ictal aphasia as a lateralizing sign By contrast, regardless of the lobe, the lateralizing value of ictal aphasia is excellent, with nondominant seizures being exceptional. Ictal aphasia was seen in two seizures arising from the nondominant hemisphere (in one patient) in the series of Gabr et al.,29 and in that patient aphasia was limited to paraphasia. One similar exception was reported in the series by Serafetinides and Falconer32; although the patient had ictal aphasia and proven right temporal lobe epilepsy (by seizurefreedom after temporal lobectomy), language dominance had not been determined by Wada testing, and the patient may have been right-hemisphere dominant. Thus, when present, the lateralizing value of ictal aphasia is high, and seems to be comparable to that of postictal aphasia, which is 92–100%.29,57
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Rubboli G, Parmeggiani L, Tassinari CA. Frontal inhibitory spike component associated with epileptic negative myoclonus. Electroencephalogr Clin Neurophysiol 1995;95:201–5. Baumgartner C, Poderka I, Olbrich A et al. Epileptic negative myoclonus: an EEG-single photon emission CT study indicating involvement of premotor area. Neurology 1996;46:753–8. Aicardi J, Chevrie JJ. Atypical benign partial epilepsy of childhood. Dev Med Child Neurol 1982;24:281–92. Gabr M, Lüders HO, Dinner D et al. Speech manifestations in lateralization of temporal lobe seizures. Ann Neurol 1989;25:82–7. Benbadis SR. Aphasic seizures. In: Lüders HO, Noachtar S, eds. Epileptic Seizures: Pathophysiology and Clinical Semiology. New York: Churchill Livingstone, 2000:501–5. Yen D, Su M, Yiu C et al. Ictal speech manifestations in temporal lobe epilepsy: a video-EEG study. Epilepsia 1996;37:45–9. Serafetinides EA, Falconer MA. Speech disturbance in temporal lobe seizures. A study in 100 epileptic patients submitted to anterior temporal lobectomy. Brain 1963;86:333–46. Penfield W, Rasmussen T. Vocalization and arrest of speech. Arch of Neurol Psychiatry 1949;61:21–7. Lüders HO, Lesser RP, Hahn J et al. Basal temporal language area demonstrated by electrical stimulation. Neurology 1986;36: 505–10. Lüders HO, Lesser RP, Hahn J et al. Basal temporal language area. Brain 1991;114:743–54. Schaffler L, Lüders HO, Morris HH III, Wyllie E. Anatomic distribution of cortical language sites in the basal temporal language area in patients with left temporal lobe epilepsy. Epilepsia 1994;35:525–8. Abou-Khalil B, Welch L, Blumenkopf B et al. Global aphasia with seizure onset in the dominant basal temporal region. Epilepsia 1994;35:1079–84. Suzuki I, Shimizu H, Ishijima B et al. Aphasic seizure caused by focal epilepsy in the left fusiform gyrus. Neurology 1992;42: 2207–10. Gilmore RL, Heilman KM. Speech arrest in partial seizures: evidence of an associated language disorder. Neurology 1981;31: 1016–19. Rosenbaum DH, Siegel M, Barr WB, Rowan AJ. Epileptic aphasia. Neurology 1986;36:822–5. Spatt J, Goldenberg G, Mamoli B. Simple dysphasic seizures as the sole manifestation of relapse in multiple sclerosis. Epilepsia 1994;35:1342–5.
42. 43. 44. 45. 46. 47. 48. 49. 50. 51. 52. 53. 54. 55.
56. 57.
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Smith Doody R, Hrachovy RA, Feher EP. Recurrent fluent aphasia associated with a seizure focus. Brain Lang 1992;42: 419–30. Kirshner HS, Hughes T, Fakhoury T, Abou-Khalil B. Aphasia secondary to partial status epilepticus of the basal temporal language area. Neurology 1995;45:1616–18. Wells CR, Labar DR, Solomon GE. Aphasia as the sole manifestation of simple partial status epilepticus. Epilepsia 1992;33: 84–7. De Pasquet EG, Gaudin ES, Bianchi A, De Mendilaharsu SA. Prolonged and monosymptomatic dysphasic status epilepticus. Neurology 1976;26:244–7. Racy A, Osborn MA, Vern BA, Molinari GF. Epileptic aphasia: first onset of prolonged monosymptomatic status epilepticus in adults. Arch Neurol 1980;37:419–22. Primavera A, Bo GP, Venturi S. Aphasic status epilepticus. Europ Neurol 1988;28:255–7. Boudouresques J, Roger J, Gastaut H. Crises aphasiques subintrantes chez un epileptique temporal: etude electroclinique. Rev Neurol 1962;106:381. Hamilton NG, Matthews T. Aphasia: the sole manifestation of focal status epilepticus. Neurology 1979;29:745–8. Knight RT, Cooper J. Status epilepticus manifesting as reversible Wernicke’s aphasia. Epilepsia 1986;27:301–4. Dinner DS, Lüders HO, Lederman R, Gretter TE. Aphasic status epilepticus: a case report. Neurology 1981;31:888–91. Geschwind N. Aphasia. N Engl J Med 1971;284:654–6. Obana WG, Laxer KD, Cogen PH et al. Resection of dominant opercular gliosis in refractory partial epilepsy. Report of two cases. J Neurosurg 1992;77:632–9. Commission on classification and terminology of the International League Against Epilepsy: Proposal for revised classification of epilepsy and epileptic syndromes. Epilepsia 1989;30:389–99. Salanova V, Andermann F, Rasmussen T et al. Parietal lobe epilepsy: clinical manifestations and outcome in 82 patients treated surgically between 1929 and 1988. Brain 1995;118: 607–27. Lüders HO, Awad I. Conceptual considerations. In Lüders HO, ed: Epilepsy Surgery. New York: Raven Press, 1992:51. Chee MWL, Kotagal P, Van Ness PC et al. Lateralizing signs in intractable partial epilepsy: blind multiple-observer analysis. Neurology 1993;43:2519–25.
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Secondary generalized tonic-clonic seizures SD Lhatoo and HO Lüders
Introduction Secondary generalized tonic-clonic seizures (SGTCS) are a common occurrence in the video-monitoring phase of the presurgical assessment of focal epilepsies, although in contrast to primary generalized tonic clonic seizures (PGTCS), the rather scanty literature available on their semiology and pathophysiology belies this. To date, the most authoritative work on generalized tonic clonic seizures (GTCS) has been the description provided by Gastaut and Broughton in their influential monograph Epileptic Seizures: Clinical and Electrographic Features, Diagnosis and Treatment. Modern epilepsy semiology literature is reliant on their observations and the few contemporary analyses that exist use their description as a benchmark. Gastaut and Broughton acknowledged the difficulty in distinguishing PGTCS from SGTCS when seizures were clinically generalized at onset, a conundrum that has not completely diminished since then, and thus their classical account of the generalized tonicclonic seizure appears to present a composite of mainly ‘grand mal’ primary but also secondary generalized tonic-clonic seizures. However, certain semiological features often differ and may be of critical value in the distinction of one from another. Furthermore, these features may have a lateralizing value that complements the other facets of presurgical assessment.
Semiology of the SGTCS Gastaut and Broughton’s work provides exquisite detail on the semiology and pathophysiology of GTCS with detailed descriptions of electroencephalography, electrocardiography, electrodermography, sphygmomanometry, pupillary measurement, intravesical pressure measurements, and audiometry and spirometry. They divided the various phases of the GTCS into: 1. preictal manifestations 2. the ictal phase a. the tonic phase (including an ‘intermediate vibratory period’) b. the clonic phase c. (concurrent) Autonomic changes 3. immediate postictal features 4. late postictal features It is the first two phases–the preictal phase and the ictal phase, that are of greatest semiological interest, mainly 492
because of the clinical information that they provide as an aid to seizure localization and lateralization. The later phases of the SGTCS are less likely to yield significant information. The preictal ‘myoclonic’ phase (such as occurs in juvenile myoclonic epilepsy (JME)) was thought to occur in the majority and constituted a ‘succession of brief, bilateral and massive muscle contractions which usually last a total of several seconds ... frequently accompanied by a spasmodic cry’. The tonic phase, accompanied by loss of consciousness, was characterized by a brief phase in flexion followed by a longer one in extension, in all lasting ten to twenty seconds. A typical flexion was described as one similar to the response to the command ‘Put up your hands!’ with shoulder elevation, arm elevation and the elbow semiflexion. The lower limbs were described as being less involved but often with flexion, abduction and external rotation of the thighs and legs, completing an emprosthotonic posture (Figure 54b.1). This tonic flexion was followed by tonic extension into an opisthotonic position (Figure 54b.2). Contraction of the thoraco-abdominal musculature produced the ‘tonic epileptic cry’. The arms became semiflexed in front of the chest but also at times became extended, with forearm pronation and either wrist flexion and finger extension or wrist extension and fist clenching. The legs went into forced extension, adduction and external rotation along with extension of the feet and toes into a Babinski-like posture. This ‘tetanic’ phase subsequently became less complete and the rigidity was replaced by a fine tremor that grew in amplitude and slowed in frequency from 8 per second to 4 per second because of recurrent decreases in muscle tone–a so-called ‘intermediate vibratory period’. The clonic phase lasted about 30 seconds and was said to occur when each of the recurrent muscular contractions responsible for the vibratory phase became sufficiently prolonged to completely interrupt the tonic contraction, the resultant flexor spasms of the entire body appearing to resemble an ‘an epileptic form of bilateral myoclonus’. This myoclonus progressively slowed until seizure cessation. Variations to this entire theme were considered occasional and unusual. Asynchrony between two sides during the tonic or clonic phases was one such deviation. This asynchrony could be clinical or only evident on EMG recordings when clinically unnoticed. Lateralization in the initial phase of the SGTCS Two important studies have addressed the issue of the importance of two semiological features at the onset of secondary
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Figure 54b.1
The flexion or ‘emprosthotonic’ posture.
generalization in focal epilepsies that can be an invaluable aid to lateralization. Wyllie et al.2 studied head version in 61 seizures in 27 patients and reported that this occurred contralateral to the hemisphere of seizure onset in all patients. It is important to emphasize here that the definition of head version is crucial to correct lateralization. Only forced and prolonged head turning, usually in a clonic motion with the chin pointing upwards, with eye version to the same side as head version allows precise lateralization (Figure 54b.3). Very frequently, such a version is also accompanied by pulling of the face towards the contralateral, clonic, twitching side. Kotagal et al.3 reported the ‘sign of 4’ or the ‘figure 4 sign’ where the elbow contralateral to the hemisphere of seizure onset extends and the ipsilateral elbow flexes over the chest to produce an upper limbs posture that resembles a figure 4. (Figure 54b.1). In a study that looked at 39 patients with focal epilepsy, correct lateralization with this sign was seen in 90%. Other studies have subsequently confirmed the clinical utility of this sign. However, both head version and the sign of 4 are unreliable signs once the seizure is well established and their main value is derived at the onset of generalization when they are less likely to represent symptomatology remote from the ictal onset zone. Lateralization in the SGTCS and seizure progression A few studies have since examined the progression of the SGTCS (Table 54b.1). A study from Bethesda, Maryland in
Figure 54b.2
493
The extension or (opisthotonic) posture.
19944 presented a videotape analysis of 120 SGTCS in 47 patients with focal epilepsy with an age range between 11 and 56 years. Seizure semiology analysis was carried out jointly by three observers and the generalized phase was divided into five phases that constituted onset of generalization, pretonic clonic, tonic, tremulousness and clonic phases. Eighty-four percent of the seizures had the ‘onset’ phase characterized by vocalization, head version or some form of movement, 48% had a pretonic clonic phase where patients had irregular and asymmetric jerking, 95% a tonic phase and 98% a clonic phase. Only 27% of these seizures exhibited all five phases. The authors noted that generalization was not uniform or symmetric and noted the marked heterogeneity in GTCS phenomenology. Another study that examined SGTCS progression in temporal lobe epilepsy patients in 20015 found the classically described sequence of progression in only half their patients and in a third, a clonic phase preceded the tonic and in a quarter, the progression was one of tonic to clonic to tonic. Asynchrony in the clonic phase was noted in only two patients. An unblinded videotape analysis from Nashville, Tennessee in 19996 compared ten GTCS in nine patients with idiopathic generalized epilepsy and ten GTCS in ten patients with temporal lobe epilepsy. Interestingly, (and this has been noted by subsequent studies), focal features were seen before generalization in seven idiopathic generalized seizures, most commonly comprising head turning, in one patient occurring in different directions in two different seizures. The authors noted that the tonic phase was always symmetric but that in the last generalized
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Figure 54b.3 The sign of 4 with right elbow extension indicating left hemisphere seizure onset. Also notice version of the head to the right.
clonic phase, asymmetry or asynchrony of motor activity was seen transiently in three seizures. In contrast, in the temporal lobe epilepsy patients, focal tonic activity occurred in four seizures, with variable lateralization and there was asymmetric or asynchronous activity in the clonic phase in eight seizures. Seizure progression in these patients was tonic to clonic in eight, clonic to tonic to clonic in one and only clonic in one. A 2003 study from Calgary7 attempted to distinguish primary from SGTCS in children aged 18 months to 17 years by examining 64 GTCS in 13 children with medically refractory epilepsy. The study highlighted mouth movements and motor activity following clinical and EEG seizure end as distinctive features of the SGTCS, although these conclusions and their value in clinical practice is debatable. However, these authors also noted the asymmetry in arm movements in seven out of 12 children and in leg movements in nine out of 12 children during secondary generalization. In five patients, seizure activity continued on one side, with varying lateralization. Thus, no reliable clinical features appear to lateralize the hemisphere of seizure onset once the seizure is well under way. This is not surprising, given that the seizure has propagated to areas distant from the ictal onset zone.
Table 54b.1
Lateralization in the latter phase of the SGTCS Two studies have examined lateralization during seizure termination in temporal lobe epilepsy. They found that in 80–83% of seizures that ended in an asynchronous fashion, the final clonic movements occurred on the side ipsilateral to the hemisphere of seizure onset.8,9 This may reflect on earlier seizure cessation in the hemisphere of seizure onset due to factors such as neuronal fatigue, an exhaustion of excitatory processes, or a predominance of inhibitory processes. The marked slowing usually seen on scalp-EEG during this phase in the hemisphere ipsilateral to the paradoxical movements lends support to this. Paradoxical movements are most likely to be generated in the contralateral cortex and propagated by the pyramidal tract, rather than originating in the brainstem, not least because there is a clear relationship between ipsilateral cortical discharges and strictly contralateral clonic signs. There appears to be some lateralizing value to this sign although it is important to emphasize that the seizure should always be viewed in its entirety and the value of lateralizing signs at seizure onset outweigh the importance of phenomena that occur during or towards the end of seizures. Two common themes emerge from these studies. Firstly, that there is considerable heterogeneity in seizure progression during the phase of secondary generalization as compared to Gastaut’s classical description and secondly, there is asynchrony (disparity of rhythm between the two sides) and/or asymmetry (disparity in amplitude of limb movement between the two sides) during the seizure in a substantial proportion of patients. Contrary to the caution required in interpreting late ictal phenomena, forced head version immediately prior to the onset of secondary generalization and the asymmetric ‘sign of 4’ tonic posturing at the onset of the SGTCS are known to be useful lateralizing features where head version or elbow extension in the sign of 4 occur contralateral to the hemisphere of seizure onset.3 However, there is literature to suggest that focal features also arise in the GTCS of idiopathic generalized epilepsy, although definitions of head version for example, may differ in their interpretation.10
The Cleveland Clinic experience In our own semiological analysis of 24 SGTCS in 14 patients (12 male, two female) aged 9–39 years who underwent
Studies of seizure semiology in secondary generalized tonic-clonic seizures Seizure progression – % of patientsb
Study
No of seizuresa
Theodore 1994 Niaz 1999 Jobst 2001 Trinka 2002 Leutmezer 2002 Kirton 2003
120 10 286 39 74 64
a
TÆC
CÆTÆC
TÆCÆT
80 52
48 10 31
28
Asynchronyc C
yes/no – %
10
Yes Yes Yes Yes Yes
Number of seizures specified rather than number of patients because of seizure heterogeneity in the same patient T = tonic, C = clonic c Asynchrony is used synonymously with asymmetry b
(80) (60) (43) (38.5)
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Clinical characteristics of patients with secondary generalized tonic-clonic seizures
Patient
Sex
Age
1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14.
F M M M M M F M M M M M M M
26 27 18 25 19 14 35 25 18 20 39 23 9 13
Duration of ep. 12 15 13 21 10 9 19 15 15 9 22 20 7 1
Diagnosis
Pathology
Left temporal lobe epilepsy Right temporo-parieto-occipital epilepsy Right mesial frontal lobe epilepsy Left basal temporal lobe epilepsy Left lateral temporal lobe epilepsy Right temporo-parietal epilepsy Right hemispheric epilepsy Left hemispheric epilepsy Right mesial frontal lobe epilepsy Right parieto-occipital epilepsy Right temporo-occipital epilepsy Left lateral frontal lobe epilepsy Right lateral temporal lobe epilepsy Right temporo-occipital epilepsy
Temporal hamartoma Bihemispheric MCD Remote infarct Focal subpial gliosis Focal subpial gliosis Focal cortical dysplasia Bihemispheric MCD Unknown Remote infarct/contusion Focal cortical dysplasia Bihemispheric MCD Focal subpial gliosis Unknown DNET
MCD – malformation of clinical development; DNET – dysembryoplastic neuroepithelial tumor.
video-EEG monitoring as part of their presurgical investigation for medically refractory focal epilepsy, we found confirmation of some of the clinical features described in the literature. All 14 patients had invasive evaluations with subdural grid electrodes and/or depth electrodes. The duration of epilepsy ranged from 1–22 years. Clinical details are provided in Table 54b.2. In each case, the epilepsy diagnosis was made with on the basis of semiology, MR as well as functional imaging, interictal and ictal EEG findings. Seizure semiology was studied from the point of onset of secondary generalization. We employed a practical definition for generalization as that clinical stage where there was
Table 54b.3 Pt. 1. 2. 3. 4. 5a. 5b. 5c. 5d. 6. 7. 8. 9a. 9b. 9c. 9d. 10a. 10b. 10c. 10d. 11. 12a. 12b. 13. 14.
clear evidence of bilateral motor arm and/or leg involvement along with complete loss of consciousness. Thus, we did not include head or eye version in this definition. Mode of onset, progression of generalization, duration of various motor stages, symmetry of seizures, synchrony of the clonic phase, and the presence or absence of paradoxical lateralization were all studied. Asymmetry was defined as a greater than 50% difference in amplitude of movement between the two sides of the body. Asynchrony was defined as a clear difference in the rhythm of movement between the two sides of the body. Table 54b.3 summarizes these findings.
Characteristics of Secondary Generalization in SGTCS Onset ST AST Sign of 4 – rt arm Bilat. arm clonic ST ST Sign of 4 – rt arm ST Bilat. leg clonic AST Sign of 4 – rt arm AST AST Sign of 4 – lt arm Sign of 4 – lt arm ST ST Sign of 4 – lt arm Bilat. arm clonic Sign of 4 – lt arm Sign of 4 – rt arm Bilat. arm clonic AST AST
Tonic phase S A S S S S S A No A S S S A A S S S A A S A A A
Vibratory phase S S S S S No No No No No No S A S A No S S S No No S No No
AST – asymmetric tonic; ST – symmetric tonic; S – symmetric; A – asymmetric.
Clonic phase
Asynchrony
S S S A A S S S A S A S A A A S A S A A S S A A
No Yes No No Yes No Yes Yes Yes No No No Yes Yes Yes Yes Yes Yes Yes Yes No Yes Yes Yes
Paradoxical lat. No No No No No No Yes Yes Yes No No No No No No No No No No No No Yes No Yes
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Seizure onset The sign of 4 was seen in eight (seven patients) of 24 (33%) seizures. In seven of these seizures (87.5%), it predicted the side of seizure onset correctly, with arm extension contralateral to the side of seizure onset. In one patient, two further seizures occurred without a sign of 4, suggesting that this does not consistently occur in all seizures in the same patients. In 6/24 (25%) seizures, there was an asymmetric tonic onset to the seizures that did not amount to a sign of 4. In 6/24 (25%), there was a symmetric tonic onset to the generalization. In 4/24 (17%) there was a clonic onset that was asymmetric in all.
2. Type 2 (26%) The body was held in the same position as in Type 1 but with persistent elbow extension rather than flexion (Figure 54b.4b). 3. Type 3 (9%) The body was held in the same position as in Type 1 but with hip and knee flexion rather than extension (Figure 54b.4c). 4. Type 4 (30%) The body was held in a position of bilateral asymmetric tonicity with upper and/or lower limb flexion on one side and upper and/or lower limb extension on the other (Figure 54b.4d).
Seizure progression Progression of generalization through various phases also varied. In 13/24 seizures (54%), there was a tonic phase followed by the vibratory phase, followed by a clonic phase. In 6/24 seizures (25%), there was no intervening vibratory phase. In one patient, there was progression from a tonic to a focal arm clonic phase. The clonic to tonic to clonic progression noted by Gastaut was seen in only 3/24 (13%) of seizures and in one patient, the seizure remained clonic throughout. All seizures had a clonic phase.
1. Type 1 (35%) The upper limbs were held in a position of s