The Causes of Epilepsy: Common and Uncommon Causes in Adults and Children Edited by Simon D

Cambridge University Press 978-0-521-11447-9 - The Causes of Epilepsy: Common and Uncommon Causes in Adults and Children Edited by Simon D. Shorvon, Frederick Andermann and Renzo Guerrini Frontmatter More information

The Causes of Epilepsy

© in this web service Cambridge University Press www.cambridge.org Cambridge University Press 978-0-521-11447-9 - The Causes of Epilepsy: Common and Uncommon Causes in Adults and Children Edited by Simon D. Shorvon, Frederick Andermann and Renzo Guerrini Frontmatter More information

The Causes of Epilepsy

Common and Uncommon Causes in Adults and Children Edited by: Simon D. Shorvon MA MD FRCP Professor in Clinical Neurology, UCL Institute of Neurology, University College London; Consultant Neurologist, National Hospital for Neurology and Neurosurgery, London, UK Frederick Andermann OC MD FRCPC Professor, Departments of Neurology and Neurosurgery and Pediatrics, McGill University; Director, Epilepsy Service, Montreal Neurological Institute and Hospital, Montreal, Quebec, Canada Renzo Guerrini MD Professor of Child Neurology and Psychiatry, University of Florence; Director, Pediatric Neurology Unit and Laboratories, Children’s Hospital A. Meyer, Florence, Italy

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Library of Congress Cataloging-in-Publication Data The causes of epilepsy / edited by Simon D. Shorvon, Frederick Andermann, Renzo Guerrini. p. ; cm. Includes bibliographical references. ISBN 978-0-521-11447-9 (Hardback) 1. Epilepsy–Etiology. I. Shorvon, S. D. (Simon D.) II. Andermann, Frederick. III. Guerrini, Renzo. [DNLM: 1. Epilepsy–etiology. 2. Epilepsy–diagnosis. 3. Epilepsy–therapy. WL 385] RC372.C38 2011 616.8053071–dc22 2010030379 ISBN 978-0-521-114479 Hardback

Cambridge University Press has no responsibility for the persistence or accuracy of URLs for external or third-party internet websites referred to in this publication, and does not guarantee that any content on such websites is, or will remain, accurate or appropriate.

Every effort has been made in preparing this book to provide accurate and up-to-date information which is in accord with accepted standards and practice at the time of publication. Although case histories are drawn from actual cases, every effort has been made to disguise the identities of the individuals involved. Nevertheless, the authors, editors, and publishers can make no warranties that the information contained herein is totally free from error, not least because clinical standards are constantly changing through research and regulation. The authors, editors, and publishers therefore disclaim all liability for direct or consequential damages resulting from the use of material contained in this book. Readers are strongly advised to pay careful attention to information provided by the manufacturer of any drugs or equipment that they plan to use.

Contents

List of contributors ix Foreword xvii Preface xix Section 1 – Introduction Subsection 2.2 – Pure epilepsies with 1 Historical introduction: the causes of epilepsy presumed complex in the pre-molecular era (1860–1960) 1 inheritance Simon D. Shorvon 12 Idiopathic generalized epilepsies 91 2 The etiological classification of epilepsy 21 Carla Marini and Renzo Guerrini Simon D. Shorvon 13 Benign partial epilepsies of childhood 104 3 Epileptogenesis in idiopathic epilepsy 24 Roberto H. Caraballo and Natalio Fejerman Snezana Maljevic and Holger Lerche 4 Mechanisms of epileptogenesis in symptomatic epilepsy 35 Section 3 – Symptomatic epilepsy Philip A. Schwartzkroin 14 Introduction to the concept of symptomatic epilepsy 113 Simon D. Shorvon Section 2 – Idiopathic epilepsy 5 Introduction to the concept of genetic epilepsy 43 Subsection 3.1 – Epilepsy syndromes Renzo Guerrini, Simon D. Shorvon, Frederick Andermann, and Eva Andermann 15 West syndrome and Lennox–Gastaut syndrome 119 Renzo Guerrini and Carla Marini 6 The genetic contribution to epilepsy: the known and missing heritability 62 Michael R. Johnson Subsection 3.2 – Progressive myoclonic epilepsies – Subsection 2.1 Pure epilepsies due to 16 Unverricht–Lundborg disease 135 single-gene disorders Maria K. Lehtinen, Anna-Elina Lehesjoki, and Reetta Kälviäinen 7 Benign familial neonatal seizures 67 Perrine Plouin 17 Dentato-rubro-pallido-luysian atrophy 139 Teiichi Onuma 8 Autosomal dominant nocturnal frontal lobe epilepsy 70 Paolo Tinuper and Francesca Bisulli 18 Lafora body disease 143 Anna C. Jansen 9 Genetic epilepsy with febrile seizures plus 74 Ingrid E. Scheffer and Yue-Hua Zhang 19 Mitochondrial cytopathies 147 Laurence A. Bindoff and Bernt A. Engelsen 10 Severe myoclonic epilepsy of infancy or Dravet syndrome 78 20 Neuronal ceroid lipofuscinoses 158 Carla Marini and Renzo Guerrini Ruth E. Williams 11 Benign adult familial myoclonic epilepsy 85 21 Sialidosis and Gaucher disease 164 Teiichi Onuma Silvana Franceschetti and Laura Canafoglia

Contents

22 Action myoclonus–renal failure syndrome 169 37 Disorders of cobalamin and folate Eva Andermann metabolism 252 Michael Shevell, David Watkins, and 23 Progressive myoclonus epilepsies: David Rosenblatt other rare causes 172 Frederick Andermann and Eva Andermann 38 Other single-gene disorders 258 Vincent Navarro and Frédéric Sedel Subsection 3.3 – Neurocutaneous syndromes Subsection 3.5 – Disorders of chromosome 24 Tuberous sclerosis complex 177 structure Catherine J. Chu-Shore and Elizabeth A. Thiele 39 Down syndrome 265 25 Neurofibromatoses 183 Nadia Bahi-Buisson, Monika Eisermann, Rosalie E. Ferner and Margaret J. Jackson and Olivier Dulac 26 Sturge–Weber syndrome 189 40 Fragile X syndrome 272 Alexis Arzimanoglou and Eleni Panagiotakaki Irissa M. Devine and Carl E. Stafstrom – 27 Other neurocutaneous syndromes 196 41 4p (Wolf Hirschhorn) syndrome 277 Ignacio Pascual-Castroviejo Agatino Battaglia 42 Inverted duplicated chromosome 15 (isodicentric chromosome 15) 281 Subsection 3.4 – Other single-gene disorders Agatino Battaglia with epilepsy as a prominent 43 Ring chromosome 20 285 symptom Geneviève Bernard and Frederick Andermann 28 Angelman syndrome 201 Bernard Dan and Stewart G. Boyd Subsection 3.6 – Developmental anomalies 29 Lysosomal disorders and Menkes syndrome 206 of cerebral structure Edwin H. Kolodny and Swati Sathe (cortical dysplasias) 30 Neuroacanthocytosis 212 Anna C. Jansen 44 Hemimegalencephaly 289 M. Scott Perry and Michael Duchowny 31 Organic acid, amino acids, and peroxisomal disorders 216 45 Focal cortical dysplasia and related variants 293 Maria Alice Donati, Serena Gasperini, Ruben I. Kuzniecky and Renzo Guerrini 46 Agyria–pachygyria band spectrum 298 32 Porphyria 231 Elena Parrini and Renzo Guerrini Geoffrey Dean and Simon D. Shorvon 47 Agenesis of the corpus callosum 305 33 Pyridoxine-dependent epilepsy 237 Dorothy Jones-Davis, Yolanda Lau, Sidney M. Gospe, Jr. and Elliott H. Sherr 34 Rett syndrome and MECP2 48 Polymicrogyria and schizencephaly 311 and CDKL5 genotypes 242 Renzo Guerrini and Carmen Barba Daniel G. Glaze 49 Periventricular nodular heterotopia 322 35 Urea cycle disorders 246 Rahul Rathakrishnan, Yahya Aghakhani, Linda Huh and Kevin Farrell and François Dubeau 36 Wilson disease 249 50 Microcephaly 330 J. M. Walshe M. Elizabeth Ross

Contents

51 Arachnoid cysts 341 66 Metastatic disease 459 Concezio Di Rocco and Gianpiero Tamburrini Rolando F. Del Maestro, Abdulrahman Sabbagh, Ahmed Lary, and Marie-Christine 52 Malformations of human cerebral cortex 346 Guiot Waney Squier

Subsection 3.7 – Hippocampal sclerosis and Subsection 3.10 – Cerebral infection prenatal and perinatal 67 Viral encephalitis 467 injury Jane E. Adcock 68 Bacterial meningitis and focal suppurative 53 Hippocampal sclerosis 363 intracranial infections in children 475 Fernando Cendes and Márcia Elisabete Morita Suresh S. Pujar and Richard F. M. Chin 54 Neonatal seizures and postneonatal 69 Bacterial meningitis and pyogenic abscess – epilepsy causes 373 in adults 482 Eli M. Mizrahi and Kevin E. Chapman Lina Nashef and Fahmida A. Chowdhury 55 Cerebral palsy 382 70 Malaria 492 Sameer M. Zuberi and Andreas Brunklaus Charles R. J. C. Newton 56 Vaccination and immunization 388 71 Neurocysticercosis 495 Simon D. Shorvon Hector H. Garcia 72 Other parasitic diseases 501 Subsection 3.8 – Cerebral trauma Manish Modi and Gagandeep Singh 57 Open head injury 393 73 Tuberculosis 511 Flavio Giordano, Barbara Spacca, and Lorenzo Genitori Nadir E. Bharucha, Roberta H. Raven, and Vivek Nambiar 58 Closed head injury 400 Manuel Murie-Fernandez, Jorge G. Burneo, and Robert 74 HIV infection 520 W. Teasell P. Satishchandra and S. Sinha 59 De novo epilepsy after neurosurgery 407 75 Emerging and less common central nervous Charles E. Polkey system viral encephalitides 528 H. T. Chong and C. T. Tan 60 Epilepsy after epilepsy surgery 413 Andre Palmini 61 Non-accidental brain injury 425 Subsection 3.11 – Cerebrovascular disease Renzo Guerrini and Alessio De Ciantis 76 Cerebral hemorrhage 537 Henry B. Dinsdale Subsection 3.9 – Cerebral tumor 77 Cerebral infarction and occult degenerative cerebrovascular disease 544 62 Glioma 433 Ruth E. Nemire and R. Eugene Ramsay William P. Gray and Harry Bulstrode 78 Arteriovenous malformations 551 63 Ganglioglioma, dysembryoplastic neuroepithelial tumor, and related tumors 441 Suzanne A. Tharin, Autumn Marie Klein, and Robert M. Friedlander Thomas S. Jacques and William Harkness 79 Cavernous malformations 559 64 Hypothalamic hamartoma and gelastic epilepsy 449 Adrian M. Siegel John F. Kerrigan 80 Other vascular disorders 565 65 Meningioma 454 Leif Gjerstad and Erik Taubøll Sumeet Vadera and William Bingaman

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Contents

Subsection 3.12 – Cerebral immunological Subsection 4.2 – Reflex seizures disorders 96 How reflex mechanisms cause epilepsy 683 Benjamin Zifkin and Frederick Andermann 81 Rasmussen encephalitis and related conditions 573 Antonio Gambardella and Frederick Andermann 97 Visual stimuli, photosensitivity, and photosensitive epilepsy 687 82 Systemic lupus erythematosus and other collagen Dorothée Kasteleijn-Nolst Trenité, Laura Cantonetti, and vascular diseases 579 Pasquale Parisi Rolando Cimaz and Andrea Taddio 98 Startle-induced (and other sensory-induced) 83 Inflammatory and immunological diseases of the epilepsy 695 nervous system 585 Jean-Pierre Vignal, Sandrine Aubert, and Patrick Chauvel Michael P. T. Lunn 99 Primary reading epilepsy 700 Subsection 3.13 – Other cerebral disorders Matthias Koepp 100 Auditory-induced epilepsy 704 84 Psychiatric disorders 593 Carlo Di Bonaventura and Frederick Andermann Brent Elliott and John O’Donavan 101 Focal reflex seizures – with emphasis on seizures 85 Multiple sclerosis and other acquired demyelinating triggered by eating 709 diseases 607 Benjamin Zifkin, Guy M. Rémillard, and Frederick Mark R. Manford Andermann 86 Hydrocephalus and porencephaly 612 102 Hot-water epilepsy 713 Pierangelo Veggiotti and Federica Teutonico P. Satishchandra, S. Sinha, and A. Anand 87 Alzheimer disease and other neurodegenerative 103 Reflex epilepsy with higher-level processing 720 diseases 618 Benjamin Zifkin and Frederick Andermann Sigmund Jenssen and Kandan Kulandaivel

Section 4 – Provoked epilepsies Section 5 – Status epilepticus 88 Introduction to the concept of provoked epilepsy 625 104 Introduction – how status epilepticus is caused 723 Simon D. Shorvon, Renzo Guerrini, and Frederick Andermann Karthik Rajasekaran and Howard P. Goodkin 105 Causes of status epilepticus in children 730 Subsection 4.1 – Precipitating factors Rod C. Scott 89 Fever 631 106 The causes of convulsive status epilepticus in adults 735 Thomas P. Bleck Elizabeth J. Waterhouse and Peter W. Kaplan 90 The menstrual cycle and catamenial epilepsy 635 107 Uncommon causes of status epilepticus 745 Andrew G. Herzog Simon D. Shorvon, Raymond Y. L. Tan, and Aidan Neligan 91 Sleep 643 108 Causes of non-convulsive status epilepticus in adults 752 Liborio Parrino, Giulia Milioli, Fernando De Paolis, Pierre Thomas Andrea Grassi, Gioia Gioi, and Mario Giovanni Terzano 109 Causes of epilepsia partialis continua 759 92 Metabolic and endocrine-induced seizures 650 Hirokazu Oguni and Frederick Andermann Bernhard J. Steinhoff 110 Afterword 767 93 Electrolyte and sugar disturbances 655 Simon D. Shorvon, Renzo Guerrini, and Frederick Bindu Menon and Simon D. Shorvon Andermann 94 Drug-induced seizures 664 Aidan Neligan 95 Alcohol- and toxin-induced seizures 674 Index 771 Michelle J. Shapiro and Andrew J. Cole Color plates appear between pages 236 and 237. viii

Contributors

Jane E. Adcock Nadia Bahi-Buisson Department of Clinical Neurology, Department of Pediatric Neurology and Neurophysiology, University of Oxford, Hôpital Necker Enfants Malades, John Radcliffe Hospital, Université Paris Descartes, Paris, France Oxford, UK Carman Barba Yahya Aghakhani Pediatric Neurology Unit, Section of Neurology, Anna Meyer Children’s Hospital, Department of Internal Medicine, University of Florence, Italy University of Manitoba, Winnipeg, Alberta, Canada Agatino Battaglia Department of Child Neuropsychiatry, A. Anand University of Pisa, Molecular Biology and Genetics Unit, Stella Maris Clinical Research Institute, Italy Jawaharlal Nehru Center for Advanced Sciences (JNCASR), Division of Medical Genetics, Bangalore, India Department of Pediatrics, University of Utah School of Medicine, Eva Andermann Salt Lake City, UT, USA Neurogenetics Unit, Montreal Neurological Institute and Hospital; Geneviève Bernard Departments of Neurology and Neurosurgery and Human Pediatric Neurologist and Fellow in Neurogenetics, Genetics, CHUM and Saint-Justine’s Hospital, McGill University, Montreal, Québec, Canada Montreal, Québec, Canada Nadir E. Bharucha Frederick Andermann Departments of Neurology and Neuroepidemiology, Departments of Neurology, Neurosurgery and Pediatrics, Bombay Hospital Institute of Medical Science, McGill University; Mumbai, India Epilepsy Service, Laurence A. Bindoff Montreal Neurological Institute and Hospital, Montreal, Québec, Canada Department of Neurology, Haukeland University Hospital, Alexis Arzimanoglou Bergen; Department of Clinical Medicine, Institute for Children and Adolescents with Epilepsy IDEE, University of Bergen, Norway Department of Epilepsy, William Bingaman Sleep and Pediatric Neurophysiology, University Hospitals of Lyon (HCL) and Hôpital Department of Neurosurgery, Femme Mère Enfant, Lyon, France Cleveland Clinic Foundation, Cleveland, OH, USA Sandrine Aubert Francesca Bisulli Service de Neurophysiologie Clinique, Hôpital de la Timone, Department of Neurological Sciences, APHM, Marseille, France University of Bologna, Italy

List of contributors

Thomas P. Bleck National Centre for Young People with Epilepsy, Department of Neurological Sciences, Lingfield, Surrey, UK Neurosurgery, Medicine, and Anesthesiology, Rush Medical College, H. T. Chong Chicago, IL, USA Division of Neurology, Stewart G. Boyd Faculty of Medicine, Department of Clinical Neurophysiology, University of Malaya, Great Ormond Street Hospital for Children, Kuala Lumpur, Malaysia London, UK Fahmida A. Chowdhury Andreas Brunklaus King’s College Hospital, Fraser of Allander Neurosciences Unit, London, UK Royal Hospital for Sick Children, Glasgow, UK Catherine J. Chu-Shore Instructer in Neurology, Harry Bulstrode Harvard Medical School, Division of Clinical Neurosciences, Department of Neurology, Faculty of Medicine and Health and Life Sciences, Programs in Pediatric Epilepsy and Neurophysiology, University of Southampton, UK Massachusetts General Hospital. Jorge G. Burneo Rolando Cimaz Rheumatology Unit, Department of Neurology, Department of Pediatrics, University of Western Ontario Epilepsy Programme, Anna Meyer Children’s Hospital, London, Ontario, Canada University of Florence, Italy Laura Canafoglia Unit of Neurophysiopathology, Andrew J. Cole Epilepsy Center, IRCCS Foundation C. Besta The MGH Epilepsy Service, Neurological Institute, Milan, Italy Massachusetts General Hospital, Boston, MA, USA Laura Cantonetti Bambino Gesu, Santa Marinella, Rome, Italy Bernard Dan Roberto H. Caraballo Department of Neurology, Hôpital Universitaire des Enfants Reine Fabiola, Department of Neurology, Brussels, Belgium Hospital Nacional de Pediatria “Prof. Dr. Juan P. Garrhan,” Buenos Aires, The Late Geoffrey Dean Argentina Medical Research Board, Fernando Cendes The Health Research Board, Department of Neurology, Dublin, Ireland University of Campinas – UNICAMP, Alessio De Ciantis Campinas, SP, Brazil Department of Neuroscience, ’ Kevin E. Chapman Anna Meyer Children s Hospital, Pediatric Epilepsy, Barrow Neurological Institute, University of Florence, Italy ’ St. Joseph s Hospital and Medical Center, Fernando De Paolis Phoenix, AZ, USA Sleep Disorders Center, Department of Neurosciences, University of Parma, Italy Patrick Chauvel Laboratoire de Neurophysiologie et Neuropsychologie, Rolando F. Del Maestro INSERM, Marseille, France Brain Tumor Research Centre, Department of Neurology and Neurosurgery, Richard F. M.Chin Montreal Neurological Institute and Hospital, Neuroscience Unit, McGill University, UCL Institute of Child Health, London; Montreal, Québec, Canada x

List of contributors

Irissa M. Devine Kevin Farrell Division of Pediatric Neurology, Division of Neurology, Department of Pediatrics, Department of Neurology, University of British Columbia and British Columbia’s University of Wisconsin, Children’s Hospital, Madison, WI, USA Vancouver, Canada

Carlo Di Bonaventura Natalio Fejerman Epilepsy Unit, Department of Neurological Sciences, Department of Neurology, “ ” La Sapienza University of Rome, Italy Hospital Nacional de Pediatria “ ” Concezio Di Rocco Prof. Dr. Juan P. Garrhan, Buenos Aires, Argentina Institute of Neurosurgery, Catholic University Medical School, Rosalie E. Ferner Rome, Italy Guy’s and St. Thomas’ NHS Foundation Trust, Henry B. Dinsdale London, UK Queen’s University, Silvana Franceschetti Kingston, Ontario, Canada Unit of Neurophysiopathology, Epilepsy Center, Maria Alice Donati IRCCS Foundation C. Besta Neurological Institute, Milan, Italy Pediatric Neurology and Metabolic and Neuromuscular Disorders Units, Neuroscience Department, Robert M.Friedlander ’ Anna Meyer Children s Hospital, Department of Neurosurgery, University of Florence, Italy Brigham and Women’s Hospital, François Dubeau Boston, MA, USA Department of Neurology and Neurosurgery, Antonio Gambardella Montreal Neurological Hospital and Institute, Institute of Neurology, University Magna Graecia, McGill University, Catanzaro, Italy Montreal, Québec, Canada Hector H. Garcia Michael Duchowny Cysticercosis Unit, Department of Microbiology, Comprehensive Epilepsy Program and the Brain Institute, School of Sciences, ’ Miami Children s Hospital, Universidad Peruana Cayetano Heredia, Miami, FL, USA Lima, Peru Olivier Dulac Serena Gasperini Department of Pediatric Neurology and Neurophysiology, Pediatric Neurology and Metabolic and Neuromuscular Hôpital Necker Enfants Malades, Disorders Units, Neuroscience Department, Université Paris Descartes, Paris, France Anna Meyer Children’s Hospital, Monika Eisermann University of Florence, Italy Department of Pediatric Neurology and Neurophysiology, Lorenzo Genitori Hôpital Necker Enfants Malades, Department of Neurosurgery, Université Paris Descartes, Anna Meyer Children’s Hospital, Paris, France University of Florence, Italy Brent Elliott Gioia Gioi Department of Neuropsychiatry, Sleep Disorders Center, National Hospital for Neurology and Neurosurgery, Department of Neurology, London, UK Policlinico Monserrato, Cagliari, Italy Bernt A. Engelsen Department of Neurology, Flavio Giordano Haukeland University Hospital, Department of Neurosurgery, Bergen; Department of Clinical Medicine, Anna Meyer Children’s Hospital, University of Bergen, Norway University of Florence, Italy xi

List of contributors

Leif Gjerstad Thomas S.Jacques Department of Neurology, Division of Clinical Neuroscience, Neural Development Unit, Rikshospitalet University Hospital, Oslo, Norway UCL Institute of Child Health and Department of Histopathology, Daniel G. Glaze Great Ormond Street Hospital, Departments of Pediatrics and Neurology, Baylor College of London, UK Medicine and Blue Bird Circle Rett Center, Texas Children’s Hospital, Houston, TX, USA Anna C. Jansen Department of Pediatric Neurology, Howard P. Goodkin UZ Brussel, Brussels, Belgium Department of Neurology, University of Virginia, Charlottesville, VA, USA Sigmund Jenssen Department of Neurology, Sidney M. Gospe,Jr. Hahnemann University Hospital, Division of Pediatric Neurology, Philadelphia, PA, USA University of Washington and Seattle Children’s Hospital, Seattle, WA, USA Michael R. Johnson Division of Neuroscience, Andrea Grassi Imperial College London, UK Sleep Disorders Center, Department of Neurosciences, Dorothy Jones-Davis University of Parma, Italy Department of Neurology, University of California, William P. Gray San Francisco, CA, USA Department of Neurosurgery, University of Southampton, UK Reetta Kälviäinen Kuopio Epilepsy Center, Renzo Guerrini Department of Neurology, Department of Child Neurology and Psychiatry, Kuopio University Hospital, University of Florence Pediatric Neurology Unit and Kuopio, Finland Laboratories, Anna Meyer Children’s Hospital, Peter W.Kaplan University of Florence, Italy Department of Neurology, Johns Hopkins University School of Medicine, Marie-Christine Guiot Baltimore, MD, USA Department of Neuropathology, Montreal Neurological Institute and Hospital, John F. Kerrigan McGill University, Montreal, Québec, Canada Department of Clinical Pediatrics and Neurology, University of Arizona College of Medicine, William Harkness Phoenix; Pediatric Epilepsy Program and Hypothalamic Department of Neurosurgery, Hamartoma Program, Great Ormond Street Hospital, London, UK Barrow Neurological Institute, Phoenix, AZ, USA Andrew G.Herzog Department of Neurology, Autumn Marie Klein Harvard Medical School, and Neuroendocrine Unit, Department of Neurosurgery, Beth Israel Deaconess Medical Center, Brigham and Women’s Hospital, Boston, MA, USA Boston, MA, USA Linda Huh Matthias Koepp Division of Neurology, Department of Pediatrics, Department of Clinical and Experimental Epilepsy, University of British Columbia and British Columbia’s UCL Institute of Neurology, London, UK Children’s Hospital, Vancouver, Canada Edwin H. Kolodny Margaret J. Jackson Department of Neurology, Department of Neurology, Newcastle-upon-Tyne New York University School of Medicine, Hospitals Trust, Newcastle-upon-Tyne, UK New York, NY, USA

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List of contributors

Kandan Kulandaivel Bindu Menon Department of Neurology, Department of Neurology, Hahnemann Hospital, Narayana Medical College and Superspeciality Hospital, Drexel University College of Medicine, Nellore, Andhra Pradesh, India Philadelphia, PA, USA Giulia Milioli Ruben I. Kuzniecky Sleep Disorders Center, Department of Neurosciences, NYU Epilepsy Center, University of Parma, Italy Department of Neurology, Eli M. Mizrahi NYU School of Medicine, Peter Kellaway Section of Neurophysiology, New York, NY, USA Department of Neurology and Section of Pediatric Neurology, Ahmed Lary Department of Pediatrics, Baylor College of Medicine, Department of Neurosurgery, Houston, TX, USA Neurosciences Center, Manish Modi King Fahd Medical City, Department of Neurology, Riyadh, Saudi Arabia Postgraduate Institute of Medical Education and Research, Yolanda Lau Chandigarh, India Department of Neurology, Márcia Elisabete Morita University of California, Department of Neurology, San Francisco, CA, USA University of Campinas – UNICAMP, Campinas, SP, Brazil Anna-Elina Lehesjoki Folkhälsan Institute of Genetics, Manuel Murie-Fernandez Department of Medical Genetics Department of Physical Medicine and Rehabilitation, and Neuroscience Center, St. Joseph’s Healthcare, Biomedicum Helsinki, London, Ontario, Canada University of Helsinki, Finland Vivek Nambiar Maria K. Lehtinen Department of Neurology, Howard Hughes Medical Institute, Bombay Hospital Institute of Medical Science, Beth Israel Deaconess Medical Center, Mumbai, India Harvard Medical School, Boston, MA, USA Lina Nashef King’s College Hospital, Holger Lerche London, UK Neurological Clinic and Institute of Applied Physiology, University of Ulm, Germany Vincent Navarro Epilepsy Unit, Salpêtrière Hospital, Michael P. T. Lunn Pierre et Marie Curie University; National Hospital for Neurology and Neurosurgery, Cortex and Epilepsy Unit, London, UK Centre de Recherche de l’Institut du Cerveau et de la Moelle, Paris, France Snezana Maljevic Neurological Clinic and Institute of Applied Physiology, Aidan Neligan University of Ulm, Germany UCL Institute of Neurology, University College London, UK Mark R. Manford Department of Neurology, Addenbrooke’s Hospital, Ruth E. Nemire Cambridge, UK Touro College of Pharmacy, New York, NY, USA Carla Marini Pediatric Neurology Unit and Laboratories, Charles R. J. C. Newton Anna Meyer Children’s Hospital, The Wellcome Trust, University of Florence, Italy KEMRI Unit, Kilifi, Kenya

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List of contributors

John O’Donavan Karthik Rajasekaran Department of Neuropsychiatry, Department of Neurology, University of Virginia, The National Hospital for Neurology and Neuropsychiatry, Charlottesville, VA, USA London, UK R. Eugene Ramsey Hirokazu Oguni International Center for Epilepsy, Department of Pediatrics, University of Miami School of Medicine, Miami, FL, USA Tokyo Women’s Medical University, Tokyo, Japan Rahul Rathakrishnan Teiichi Onuma Department of Neurology and Neurosurgery, Musasinokokubunnji Clinic, Tokyo, Japan Montreal Neurological Hospital and Institute, Andre Palmini McGill University, Montreal, Neurology Service and Faculty of Medicine, Québec, Canada Hospital São Lucas, Roberta H. Raven Pontifícia Universidade Católica do Department of Neuroepidemiology, Rio Grande do Sul (PUCRS), Bombay Hospital Institute of Medical Science, Porto Alegre, RS, Brazil Mumbai, India Eleni Panagiotakaki Guy M.Rémillard Institute for Children and Adolescents with Epilepsy (IDEE), Department of Neurology, Hôpital Femme Mère Enfant, Lyon, France Hôpital du Sacré-Coeur de Montréal, Pasquale Parisi Montreal, Québec, Canada Department of Child Neurology, David Rosenblatt II Faculty of Medicine, Department of Human Genetics and Department “La Sapienza” University of Rome, Italy of Pediatrics and Medicine, McGill University, Elena Parrini Montreal, Québec, Canada Pediatric Neurology and Neurogenetics Unit and Laboratories, M.Elizabeth Ross Anna Meyer Children’s Hospital, Laboratory of Neurogenetics and Development, University of Florence, Italy Weill Medical College of Cornell University, Liborio Parrino New York, NY, USA Sleep Disorders Center, Department of Neurosciences, Abdulrahman Sabbagh University of Parma, Italy Department of Neurosurgery, Ignacio Pascual-Castroviejo Neurosciences Center, University Hospital La Paz, Madrid, Spain King Fahd Medical City, Riyadh, Saudi Arabia M. Scott Perry P. Satishchandra Comprehensive Epilepsy Program and the Brain Institute, Department of Neurology, Miami Children’s Hospital, Miami, FL, USA National Institute of Mental Health and Neurosciences (NIMHANS), Bangalore, India Perrine Plouin Clinical Neurophysiology Unit, Swati Sathe Hôpital Necker Enfants Malades, Department of Neurology, Université Paris Descartes, Paris, France New York University School of Medicine, New York, NY, USA Charles E. Polkey Department of Clinical Neurosciences, Ingrid E. Scheffer Institute of Psychiatry, King’s College, Department of Medicine, London, UK The University of Melbourne, Victoria; Suresh S.Pujar Department of Pediatrics, Neuroscience Unit, UCL Institute of Child Health, The University of Melbourne, London; National Centre for Young People with Epilepsy, Royal Children’s Hospital, Lingfield, Surrey, UK Melbourne, Victoria, Australia xiv

List of contributors

PhilipA.Schwartzkroin Bernhard J. Steinhoff Department of Neurological Surgery, Kork Epilepsy Centre, University of California–Davis, Kehl-Kork, Germany Davis, CA, USA Andrea Taddio Rod C. Scott Department of Pediatrics, UCL Institute of Child Health, London, UK IRCCS Burlo Garofolo, Trieste, Italy Frédéric Sedel Gianpiero Tamburrini Federation of Nervous System Diseases, Institute of Neurosurgery, Reference Center for Lysosomal Diseases, Catholic University Medical School, Assistance Publique-Hôpitaux de Paris, Paris, France Rome, Italy Michelle J. Shapiro C. T. Tan McMaster University, Hamilton General Hospital, Division of Neurology, Faculty of Medicine, Hamilton, Ontario, Canada University of Malaya, Kuala Lumpur, Malaysia Elliott H. Sherr Department of Neurology, Raymond Y. L. Tan University of California, National Hospital for Neurology and Neurosurgery, San Francisco, CA, USA London, UK Michael Shevell Erik Taubøll Departments of Neurology, Neurosurgery and Pediatrics, Department of Neurology, McGill University, Montreal, Québec, Canada Division of Clinical Neuroscience, Rikshospitalet University Hospital, Simon D. Shorvon Oslo, Norway UCL Institute of Neurology, London; National Hospital for Neurology and Neurosurgery, London, UK Robert W.Teasell Department of Physical Medicine and Rehabilitation, Adrian M. Siegel St. Joseph’s Healthcare, Department of Neurology, London, Ontario, Canada Zuger Kantonsspital, Baar, Switzerland Mario Giovanni Terzano Gagandeep Singh Sleep Disorders Center, Department of Neurology, Department of Neurosciences, Dayanand Medical College and Hospital, University of Parma, Italy Ludhiana, India Federica Teutonico S. Sinha Department of Child Neurology Department of Neurology, and Psychiatry, “C. Mondino” Foundation, National Institute of Mental Health and Neurosciences University of Pavia, Italy (NIMHANS), Bangalore, India Suzanne A. Tharin Barbara Spacca Department of Neurosurgery, Department of Neurosurgery, Brigham and Women’s Hospital, Royal Liverpool Children’s Hospital NHS Trust, Harvard Medical School, Liverpool, UK Boston, MA, USA Waney Squier Elizabeth A. Thiele Department of Neuropathology, Herscot Center for Tuberous Sclerosis Complex, John Radcliffe Hospital, Oxford, UK Boston, MA, USA Carl E. Stafstrom Pierre Thomas Department of Neurology, UF EEG-Epileptologie, Service de Neurologie, University of Wisconsin, Madison, WI, USA University of Nice-Sophia-Antipolis, Nice, France

List of contributors

Paolo Tinuper Elizabeth J. Waterhouse Department of Neurological Sciences, Department of Neurology, University of Bologna, Italy Medical College of Virginia Commonwealth University, Richmond, VA, USA Dorothée Kasteleijn-Nolst Trenité University of Utrecht, David Watkins The Netherlands; II Faculty of Medicine, Department of Human Genetics, McGill University, “La Sapienza” University of Rome, Italy Montreal, Québec, Canada Sumeet Vadera Ruth E. Williams Department of Neurosurgery, Cleveland Clinic Foundation, Department of Pediatric Neurology, Cleveland, OH, USA Evelina Children’s Hospital, London, UK Pierangelo Veggiotti Yue-Hua Zhang Department of Child Neurology and Psychiatry, Department of Pediatrics, “C. Mondino” Foundation, Peking University First Hospital, Beijing, China University of Pavia, Italy Benjamin Zifkin Jean-Pierre Vignal Epilepsy Clinic, Montreal Neurological Hospital, Service de Neurologie, Montreal, Québec, Canada Hopital Central CHU de Nancy, Nancy, France Sameer M.Zuberi J. M. Walshe Fraser of Allander Neurosciences Unit, Department of Neurology, Royal Hospital for Sick Children, The Middlesex Hospital, London, UK Glasgow, UK

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Foreword

The written history of epilepsy goes back 3000 years with not only is identifying an increasing number of “epilepsy accurate descriptions of epileptic phenomena appearing in genes” responsible for specific types of epilepsy, and further the writings of ancient Mesopotamia and the Indian Ayurvedic characterizing genetic disorders associated with epilepsy, but texts. Although physicians of the Hippocratic school in Greece, also advancing the concept of susceptibility genes, which will about 400 BC, understood that epileptic seizures originated in explain variable individual predispositions to develop certain the brain, as did Galen several hundred years later, epilepsy forms of acquired epilepsies. Now, in the twenty-first century, was generally viewed as a mysterious condition attributed to we are poised to reap the benefits of these dramatic advances in supernatural causes, at least in the West, until the mid nine- our understanding of the causes of epilepsy. teenth century. At that time, the nascent disciplines of basic Methodology for characterizing different types of epileptic neuroscience and clinical neurology defined a variety of ictal seizures and the disorders associated with them, particularly manifestations, including focal seizures and absences, and through electroclinical correlations, that is the association of recognized them as part of a constellation of disorders referred particular behavioral ictal signs and symptoms with their to as epilepsy. In particular, postmortem clinical pathological unique EEG correlates, led the International League Against correlations not only revealed specific anatomic substrates for Epilepsy (ILAE) to propose international classifications for different ictal manifestations, but led directly to concepts of epileptic seizures, and for the epilepsies in 1970. These have localization of function within the human brain, and to surgical undergone several revisions, but the most recent version of the treatment for certain types of focal epilepsies. The development International Classification of Epileptic Seizures was proposed of radiology in the twentieth century further improved phys- in 1981, and the most recent International Classification of the icians’ abilities to identify “invisible” lesions as responsible for Epilepsies was proposed in 1989. These were purported to be epileptic seizures in some patients, but it was application of the purely phenomenological, because the authors felt there was, at electroencephalogram (EEG), and the subsequent field of both the time, insufficient mechanistic information on which to clinical and basic electrophysiology, that provided a means to base a classification on specific causes of epilepsy. Neverthe- begin classifying and characterizing different types of epileptic less, the inclusion of EEG characteristics permitted categoriza- seizures and epilepsy syndromes, and investigating their under- tion of ictal phenomena in a way that implied certain lying fundamental pathophysiological neuronal mechanisms. pathophysiologic differences, as well as anatomic substrates. The careful delineation of different types of ictal phenom- For instance, generalized seizures were distinguished from focal ena provided the basis for creating experimental animal seizures that appeared to originate in a part of one hemisphere. models for both in vitro and in vivo electrophysiological and Epilepsies were classified not only based on their characteristic microanatomical investigations of epilepsy. EEG localization associated seizure types, but also according to broad etiologic of the epileptogenic region greatly increased the application of categories: idiopathic, meaning epilepsy and nothing else, pre- surgical treatment for focal epilepsies, which also provided sumably primary genetic disorders; and symptomatic, meaning novel opportunities for parallel invasive in vitro and in vivo secondary to some other disease process. In addition, diseases electrophysiological and microanatomical investigations in associated with epilepsy were well described, and some epilepsy patients. Towards the end of the twentieth century, explosive diseases were recognized as conditions with a single known advances in three-dimensional neuroimaging, first with struc- cause, but most of the defined epilepsy conditions were syn- tural X-ray computerized tomography (CT), then functional dromes, characterized by specific seizure types, and other clinical positron emission tomography (PET), and finally both struc- features, such as age of onset, response to antiepileptic drugs, and tural and functional high-resolution magnetic resonance comorbidity. Using this approach, the vast majority of accepted imaging (MRI) provided intricate insights into the pathophy- epilepsy syndromes are pediatric idiopathic conditions, while the siologic mechanisms and anatomic substrates of epilepsy dis- majority of epilepsies that affect adults, most of which are symp- orders in individual patients that could be used to create more tomatic, still defy a reasonable syndromic classification. informed categorizations and classifications. These efforts For over a decade, the ILAE has attempted to revise the were joined by the burgeoning field of neurogenetics, which 1981 and 1989 classifications, with multiple reports that have xvii

Foreword

updated the list of epileptic seizure types and epilepsy syn- ultimately become a biologically based international classifi- dromes. They now recognize certain seizure types as diagnostic cation of the epilepsies. entities with associated therapeutic, prognostic, and etiologic With the hundreds of textbooks that have been published implications that can be used when a definitive syndrome or on epilepsy in the past decade or so, it is rather amazing that disease diagnosis cannot be made. These deliberations provide a none have focused specifically on the causes of epilepsy. The basis for a more scientific classification of epilepsy disorders editors have undertaken this monumental task and succeeded based on underlying genetic and pathophysiologic mechanisms, in documenting the current state of knowledge concerning the as well as anatomic substrates. Ironically, however, as the chap- genetic and pathological substrates of disorders characterized ters in this book clearly confirm, with the increasing sophistica- by epileptic seizures, as well as the situations that provoke ictal tion of our investigative methodology, the elucidation of events. This comprehensive compendium will not only serve as distinctive epilepsy conditions as diagnostic entities has become an important resource for rethinking the organization and more, rather than less, complicated. The old dichotomies of classification of epileptic phenomena and epilepsy syndromes idiopathic versus symptomatic, and generalized versus focal, and diseases, but will also provide a foundation for basic are artificial and often impossible to apply. Well-defined research attempting to identify the diverse pathophysiological classical syndromes, such as childhood absence epilepsy, are mechanisms at the subcellular, cellular, and systems levels, that not as homogeneous as once believed. Some idiopathic child- are responsible for epileptogenesis and seizure generation. hood epilepsies, such as Dravet syndrome, are not benign, Identification of these fundamental neuronal processes in turn and there appear to be several distinctly different forms of will lead to novel and more effective approaches to treatment, temporal lobe epilepsy with hippocampal sclerosis. However, cure, and prevention of epilepsy. the causes of epilepsy discussed in this textbook represent a Jerome Engel, Jr. major effort to put flesh on the bones of what hopefully will Los Angeles, California

Medicine is undergoing a remarkable transition as we move non-channel molecules and pathways associated with neural from descriptions of disease and a taxonomy based on clinical excitability. Together, these techniques are providing a crucial characteristics to a more detailed and precise understanding of framework for redefining the epilepsies based on pathophy- disease pathogenesis. This revolution has been driven by the siology and, in turn, this will have a profound impact on our adoption of a range of molecular tools and, more particularly, ability to predict, diagnose, and, ultimately, treat disease. Anti- by the application of molecular genetics to medicine. These convulsive therapy has been remarkably successful, given how approaches are providing us with insights, often for the first little we know about the pathogenic mechanisms of the disease, time, of the pathways and precise events associated with disease so it is likely that future therapeutic interventions based on a pathogenesis and this will change forever the foundations on clearer understanding of the relevant pathways will be even which we base diagnosis and treatment of disease. more effective. The developments in the molecular understanding of dis- Together, these advances have made epilepsy one of the ease are nowhere more evident than in neurological disease, most significant examples in medicine of the importance of particularly the epilepsies. These clinical syndromes, often genetic tools in clarifying pathophysiology and these disorders dramatic in their clinical characteristics, have been associated demonstrate clearly how powerful the change from pure with a range of taxonomies that have developed over many phenotypic classification of disease to one based on pathophy- centuries. The clinical characteristics of seizures and an siology can be. The authors of this important book have been understanding of the abnormal electrophysiology provided able to bring together a wide range of scientific insight and a framework on which taxonomy could be based, but clearly data on this topic into a single volume that covers the whole could not address the fundamental issue of the underpinning range of clinical syndromes. They demonstrate how powerful events in disease pathogenesis. That has had to wait until the these new genetic tools have already been in defining pathways past twenty years when the tools available for characterizing in disease and they also clearly demonstrate that, together, both families and individual patients have gradually become their observations are likely to lead to a fundamental new available. classification of these diseases. Not only is this volume timely, Initial progress in this field focused, as with other diseases, given the recent exciting developments in this field, but it also on Mendelian forms of epilepsy using family based studies. demonstrates the enormous influence that these key basic Although these studies revealed a range of interesting patho- insights will have on the way we categorize and, ultimately, physiological mechanisms, including a number of ion chan- treat individuals with disease. Epilepsy and its associated syn- nels, it has been clear that this describes only a portion of the dromes give us a clear vision of what the future of medicine is epilepsy syndromes, many of which involve more complex likely to look like. genetics. These now are increasingly tractable with the new Professor Sir John Bell, tools for genetic association and these are beginning to reveal University of Oxford, UK xviii

Preface – an act of supererogation?

An inquiring mind must return again and again to the problem cause of the symptom was completely absent from the current of origin or cause.... physicians have dug away at diverse classification schemes, based as they are largely on clinical etiologic theories or facts; physical or psychic; general or individ- semiology and electroencephalography, and it is interesting ual; genetic or acquired; fundamental or contributory. When a to muse on what form the epilepsy classification might have crime is committed, everyone in the vicinity is suspect. taken if MRI scanning had preceded EEG as a clinical investi- William Lennox, Epilepsy and Related Conditions, 1960 gatory tool. We thus open this book with, in Chapter 2, the presenta- Thus Lennox opened his chapter on “The diverse sources of tion of a draft etiological classification which goes some way seizures,” and indeed he devoted a great many pages of his we hope to filling the nosological void. The main part of the famous book to the question of etiology. Yet, 50 years later, book is organized according to this classificatory scheme. We causation is an aspect of epilepsy now somewhat neglected in have divided the etiologies into four categories: idiopathic the scientific literature on epilepsy, in the classification of epilepsies, symptomatic epilepsies, cryptogenic epilepsies, and epilepsy, and in the conceptualization of epilepsy at a clinical provoked epilepsies, and these are defined in Chapter 2.In and experimental level. It was to go some way to remedying doing so, of course, we recognize, as Lennox, and many before this deficiency that this book was conceived. him, frequently reiterated, that epilepsy is in the great majority Kinnier Wilson in 1940 wrote that the listing of all causes of of cases multifactorial, and frequently has a developmental epilepsy would be an act of supererogation, but the editors of this basis with therefore a temporal dimension. The epilepsy is book beg to differ. This is the first book ever published, as far as often the result of both genetic and acquired influences and we know, which is devoted to the topic of causation in epilepsy, also influenced by provoking factors, and assignment in such and we have attempted within its 800 pages to catalog the cases to any single etiology is therefore to an extent arbitrary. known causes of epilepsy, and corral these into a single tome. The approach to the problem of etiology between 1860 Such an attempt is only possible because of the great and 1960 forms the subject of the historical introduction advances made in imaging, molecular biology, and molecular (Chapter 1) which ends with Lennox’s work, and this is genetics in the last 40 years or so, and we believe that progress included as we believe it is important to understand the evolu- has now been sufficient to permit at least a stab at a compre- tion of concepts of causation within its historical context. hensive listing of causation. The literature on epilepsy has In subsequent chapters, we have asked the authors to rapidly increased in recent years. Kinnier Wilson noted that consider their topic in a consistent fashion, dealing with the the index catalogue of the US Surgeon-General’s office (1925) phenomenon of epilepsy in each etiology, including its epidemi- contained about 3000 titles and the “Gruhle’s review for the ology, clinical features, and prognosis, and any specific aspects years 1910–1920 deals with some 1000 articles.” In the last of investigation or treatment. 10-year period, a search on PubMed® using the keyword The purpose of the book is to be a comprehensive reference epilepsy produces more than 37 000 references, many of which work, a catalog of all the important causes of epilepsy, and a deal at least tangentially with etiology. It is this literature-base clinical tool for all clinicians dealing with patients with epi- which we have asked our contributors to summarize in the lepsy. It is aimed at specialists and the interested generalist various chapters of this volume. and it is hoped provides a distillation of knowledge in a form One striking omission has been the absence of any detailed that is helpful in the clinical setting. We hope too that it will consideration of etiology in the standard classifications of act as a clinical guide to scientists probing the dark interior of epilepsy. This is partly because at the time that these schemes the subject. were being devised neither modern investigatory imaging We have attempted to take a worldwide perspective, and methods nor modern molecular biology were available – and have included chapters on the causes of epilepsy that are rare the ascertainment of “cause” in life was often simply not in the West but common in other parts of the world. To match possible. Although it was fully recognized that epilepsy was the worldwide spread of the conditions considered here, we often “a symptom” of neurological disease, the underlying have a distinguished faculty with a similar global reach, and xix

Preface – an act of supererogation?

the book has 165 contributors from 21 countries and all and a renowned medical geneticist. The book is indeed fortu- continents many of whom are the leaders in their fields. nate to have their contributions. We are also enormously The editors have exercised a heavy editorial blue pen, have grateful to Nicholas Dunton, the Senior Commissioning tried to minimize overlap or repetition, and have asked the Editor at Cambridge University Press, who has guided the authors to follow where possible a pre-assigned template. Our project since its inception with extraordinary skill and expert- contributors have responded magnificently in our opinion, ise, and without whose assistance the book would not and we extend our grateful thanks for their hard work and have made it to the shelves. We also thank Assistant Editor for their time and effort. We would like to thank also Profes- Joanna Chamberlin and Production Editor Caroline Brown sor Jerome (Pete) Engel and Professor Sir John Bell for gra- for their great efforts on behalf of the book. Finally, we would ciously agreeing to write the foreword to the book. Pete Engel like to thank all our colleagues around the world for their is a famous leader in the field of epilepsy and a prolific author, stimulating ideas and knowledge, which have informed and who has made major contributions to many fields of epilepsy. illuminated all the pages of this book. Sir John Bell is President of the Academy of Medical Sciences and Regius Professor of Medicine at the University of Oxford, Simon Shorvon, Renzo Guerrini, and Fred Andermann