. 2018 Feb 1;141(2):391-408.

doi: 10.1093/brain/awx341.

Structural brain abnormalities in the common epilepsies assessed in a worldwide ENIGMA study

Christopher D Whelan^{1

2}, Andre Altmann³, Juan A Botía⁴, Neda Jahanshad¹, Derrek P Hibar¹, Julie Absil⁵, Saud Alhusaini^{2

6}, Marina K M Alvim⁷, Pia Auvinen^{8

9}, Emanuele Bartolini^{10

11}, Felipe P G Bergo⁷, Tauana Bernardes⁷, Karen Blackmon^{12

13}, Barbara Braga⁷, Maria Eugenia Caligiuri¹⁴, Anna Calvo¹⁵, Sarah J Carr¹⁶, Jian Chen¹⁷, Shuai Chen^{18

19}, Andrea Cherubini¹⁴, Philippe David⁵, Martin Domin²⁰, Sonya Foley²¹, Wendy França⁷, Gerrit Haaker^{22

23}, Dmitry Isaev¹, Simon S Keller²⁴, Raviteja Kotikalapudi^{25

26}, Magdalena A Kowalczyk²⁷, Ruben Kuzniecky¹², Soenke Langner²⁰, Matteo Lenge¹⁰, Kelly M Leyden^{28

29}, Min Liu³⁰, Richard Q Loi^{28

29}, Pascal Martin²⁵, Mario Mascalchi^{31

32}, Marcia E Morita⁷, Jose C Pariente¹⁵, Raul Rodríguez-Cruces³³, Christian Rummel³⁴, Taavi Saavalainen^{9

35}, Mira K Semmelroch²⁷, Mariasavina Severino³⁶, Rhys H Thomas^{37

38}, Manuela Tondelli³⁹, Domenico Tortora³⁶, Anna Elisabetta Vaudano³⁹, Lucy Vivash^{40

41}, Felix von Podewils⁴², Jan Wagner^{43

44}, Bernd Weber^{43

45}, Yi Yao⁴⁶, Clarissa L Yasuda⁷, Guohao Zhang⁴⁷, Nuria Bargalló^{15

48}, Benjamin Bender²⁶, Neda Bernasconi³⁰, Andrea Bernasconi³⁰, Boris C Bernhardt^{30

49}, Ingmar Blümcke²³, Chad Carlson^{12

50}, Gianpiero L Cavalleri^{2

51}, Fernando Cendes⁷, Luis Concha³³, Norman Delanty^{2

51

52}, Chantal Depondt⁵³, Orrin Devinsky¹², Colin P Doherty^{51

54}, Niels K Focke^{25

55}, Antonio Gambardella^{14

56}, Renzo Guerrini^{10

11}, Khalid Hamandi^{37

38}, Graeme D Jackson^{27

57}, Reetta Kälviäinen^{8

9}, Peter Kochunov⁵⁸, Patrick Kwan⁴¹, Angelo Labate^{14

56}, Carrie R McDonald^{28

29}, Stefano Meletti³⁹, Terence J O'Brien^{41

59}, Sebastien Ourselin³, Mark P Richardson^{16

60}, Pasquale Striano⁶¹, Thomas Thesen^{12

13}, Roland Wiest³⁴, Junsong Zhang^{18

19}, Annamaria Vezzani⁶², Mina Ryten^{4

63}, Paul M Thompson¹, Sanjay M Sisodiya^{64

65}

Affiliations

¹ Imaging Genetics Center, Mark and Mary Stevens Neuroimaging and Informatics Institute, University of Southern California, Los Angeles, California, USA.
² Department of Molecular and Cellular Therapeutics, Royal College of Surgeons in Ireland, Dublin, Ireland.
³ Translational Imaging Group, Centre for Medical Image Computing, University College London, London, UK.
⁴ Reta Lila Weston Institute and Department of Molecular Neuroscience, UCL Institute of Neurology, London WC1N 3BG, UK.
⁵ Department of Radiology, Hôpital Erasme, Universite Libre de Bruxelles, Brussels 1070, Belgium.
⁶ Department of Neurology and Neurosurgery, Montreal Neurological Institute, McGill University, Montreal, Quebec, Canada.
⁷ Department of Neurology, University of Campinas, Campinas, Brazil.
⁸ Epilepsy Center, Department of Neurology, Kuopio University, Kuopio, Finland.
⁹ Institute of Clinical Medicine, Neurology, University of Eastern Finland, Kuopio, Finland.
¹⁰ Pediatric Neurology Unit, Children's Hospital A. Meyer-University of Florence, Italy.
¹¹ IRCCS Stella Maris Foundation, Pisa, Italy.
¹² Comprehensive Epilepsy Center, Department of Neurology, New York University School of Medicine, New York, USA.
¹³ Department of Physiology, Neuroscience and Behavioral Science, St. George's University, Grenada, West Indies.
¹⁴ Institute of Molecular Bioimaging and Physiology of the National Research Council (IBFM-CNR), Catanzaro, Italy.
¹⁵ Magnetic Resonance Image Core Facility, IDIBAPS, Barcelona, Spain.
¹⁶ Department of Basic and Clinical Neuroscience, Institute of Psychiatry, Psychology and Neuroscience, King's College London, UK.
¹⁷ Department of Computer Science and Engineering, The Ohio State University, USA.
¹⁸ Cognitive Science Department, Xiamen University, Xiamen, China.
¹⁹ Fujian Key Laboratory of the Brain-like Intelligent Systems, China.
²⁰ Functional Imaging Unit, Institute of Diagnostic Radiology and Neuroradiology, University Medicine Greifswald, Greifswald, Germany.
²¹ Cardiff University Brain Research Imaging Centre, School of Psychology, Wales, UK.
²² Department of Neurosurgery, University Hospital, Freiburg, Germany.
²³ Department of Neuropathology, University Hospital Erlangen, Germany.
²⁴ Department of Molecular and Clinical Pharmacology, Institute of Translational Medicine, University of Liverpool, UK.
²⁵ Department of Neurology and Epileptology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.
²⁶ Department of Diagnostic and Interventional Neuroradiology, University of Tübingen, Tübingen, Germany.
²⁷ The Florey Institute of Neuroscience and Mental Health, Austin Campus, Melbourne, VIC, Australia.
²⁸ Multimodal Imaging Laboratory, University of California San Diego, San Diego, California, USA.
²⁹ Department of Psychiatry, University of California San Diego, San Diego, California, USA.
³⁰ Neuroimaging of Epilepsy Laboratory, Montreal Neurological Institute and Hospital, Mcgill University, Montreal, Quebec, Canada.
³¹ Neuroradiology Unit, Children's Hospital A. Meyer, Florence, Italy.
³² "Mario Serio" Department of Experimental and Clinical Biomedical Sciences, University of Florence, Italy.
³³ Instituto de Neurobiología, Universidad Nacional Autónoma de México. Querétaro, Querétaro, México.
³⁴ Support Center for Advanced Neuroimaging (SCAN), University Institute for Diagnostic and Interventional Neuroradiology, Inselspital, University of Bern, Bern, Switzerland.
³⁵ Central Finland Central Hospital, Medical Imaging Unit, Jyväskylä, Finland.
³⁶ Neuroradiology Unit, Department of Head and Neck and Neurosciences, Istituto Giannina Gaslini, Genova, Italy.
³⁷ Institute of Psychological Medicine and Clinical Neurosciences, Hadyn Ellis Building, Maindy Road, Cardiff, UK.
³⁸ Department of Neurology, University Hospital of Wales, Cardiff, UK.
³⁹ Department of Biomedical, Metabolic, and Neural Science, University of Modena and Reggio Emilia, NOCSE Hospital, Modena, Italy.
⁴⁰ Melbourne Brain Centre, Department of Medicine, University of Melbourne, Parkville, VIC, 3052, Australia.
⁴¹ Department of Neurology, Royal Melbourne Hospital, Parkville, 3050, Australia.
⁴² Department of Neurology, University Medicine Greifswald, Greifswald, Germany.
⁴³ Department of Epileptology, University Hospital Bonn, Bonn, Germany.
⁴⁴ Department of Neurology, Philips University of Marburg, Marburg Germany.
⁴⁵ Department of Neurocognition / Imaging, Life&Brain Research Centre, Bonn, Germany.
⁴⁶ The Affiliated Chenggong Hospital of Xiamen University, Xiamen, China.
⁴⁷ Department of Computer Science and Electrical Engineering, University of Maryland, Baltimore County, USA.
⁴⁸ Centre de Diagnostic Per la Imatge (CDIC), Hospital Clinic, Barcelona, Spain.
⁴⁹ Multimodal Imaging and Connectome Analysis Lab, Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada.
⁵⁰ Medical College of Wisconsin, Department of Neurology, Milwaukee, WI, USA.
⁵¹ FutureNeuro Research Centre, RCSI, Dublin, Ireland.
⁵² Division of Neurology, Beaumont Hospital, Dublin 9, Ireland.
⁵³ Department of Neurology, Hôpital Erasme, Universite Libre de Bruxelles, Brussels 1070, Belgium.
⁵⁴ Neurology Department, St. James's Hospital, Dublin 8, Ireland.
⁵⁵ Department of Clinical Neurophysiology, University Medicine Göttingen, Göttingen, Germany.
⁵⁶ Institute of Neurology, University "Magna Græcia", Catanzaro, Italy.
⁵⁷ Florey Department of Neuroscience and Mental Health, The University of Melbourne, Melbourne, VIC, Australia.
⁵⁸ Maryland Psychiatric Research Center, Department of Psychiatry, University of Maryland School of Medicine, Maryland, USA.
⁵⁹ Department of Medicine, University of Melbourne, Parkville, VIC, 3052, Australia.
⁶⁰ Department of Neurology, King's College Hospital, London, UK.
⁶¹ Pediatric Neurology and Muscular Diseases Unit, Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, University of Genoa, Genova, Italy.
⁶² Dept of Neuroscience, Mario Negri Institute for Pharmacological Research, Via G. La Masa 19, 20156 Milano, Italy.
⁶³ Department of Medical and Molecular Genetics, King's College London, London SE1 9RT, UK.
⁶⁴ Department of Clinical and Experimental Epilepsy, UCL Institute of Neurology, London, UK.
⁶⁵ Chalfont Centre for Epilepsy, Bucks, UK.

PMID: 29365066
PMCID: PMC5837616
DOI: 10.1093/brain/awx341

Structural brain abnormalities in the common epilepsies assessed in a worldwide ENIGMA study

Christopher D Whelan et al. Brain. 2018.

. 2018 Feb 1;141(2):391-408.

doi: 10.1093/brain/awx341.

Authors

Affiliations

¹ Imaging Genetics Center, Mark and Mary Stevens Neuroimaging and Informatics Institute, University of Southern California, Los Angeles, California, USA.
² Department of Molecular and Cellular Therapeutics, Royal College of Surgeons in Ireland, Dublin, Ireland.
³ Translational Imaging Group, Centre for Medical Image Computing, University College London, London, UK.
⁴ Reta Lila Weston Institute and Department of Molecular Neuroscience, UCL Institute of Neurology, London WC1N 3BG, UK.
⁵ Department of Radiology, Hôpital Erasme, Universite Libre de Bruxelles, Brussels 1070, Belgium.
⁶ Department of Neurology and Neurosurgery, Montreal Neurological Institute, McGill University, Montreal, Quebec, Canada.
⁷ Department of Neurology, University of Campinas, Campinas, Brazil.
⁸ Epilepsy Center, Department of Neurology, Kuopio University, Kuopio, Finland.
⁹ Institute of Clinical Medicine, Neurology, University of Eastern Finland, Kuopio, Finland.
¹⁰ Pediatric Neurology Unit, Children's Hospital A. Meyer-University of Florence, Italy.
¹¹ IRCCS Stella Maris Foundation, Pisa, Italy.
¹² Comprehensive Epilepsy Center, Department of Neurology, New York University School of Medicine, New York, USA.
¹³ Department of Physiology, Neuroscience and Behavioral Science, St. George's University, Grenada, West Indies.
¹⁴ Institute of Molecular Bioimaging and Physiology of the National Research Council (IBFM-CNR), Catanzaro, Italy.
¹⁵ Magnetic Resonance Image Core Facility, IDIBAPS, Barcelona, Spain.
¹⁶ Department of Basic and Clinical Neuroscience, Institute of Psychiatry, Psychology and Neuroscience, King's College London, UK.
¹⁷ Department of Computer Science and Engineering, The Ohio State University, USA.
¹⁸ Cognitive Science Department, Xiamen University, Xiamen, China.
¹⁹ Fujian Key Laboratory of the Brain-like Intelligent Systems, China.
²⁰ Functional Imaging Unit, Institute of Diagnostic Radiology and Neuroradiology, University Medicine Greifswald, Greifswald, Germany.
²¹ Cardiff University Brain Research Imaging Centre, School of Psychology, Wales, UK.
²² Department of Neurosurgery, University Hospital, Freiburg, Germany.
²³ Department of Neuropathology, University Hospital Erlangen, Germany.
²⁴ Department of Molecular and Clinical Pharmacology, Institute of Translational Medicine, University of Liverpool, UK.
²⁵ Department of Neurology and Epileptology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.
²⁶ Department of Diagnostic and Interventional Neuroradiology, University of Tübingen, Tübingen, Germany.
²⁷ The Florey Institute of Neuroscience and Mental Health, Austin Campus, Melbourne, VIC, Australia.
²⁸ Multimodal Imaging Laboratory, University of California San Diego, San Diego, California, USA.
²⁹ Department of Psychiatry, University of California San Diego, San Diego, California, USA.
³⁰ Neuroimaging of Epilepsy Laboratory, Montreal Neurological Institute and Hospital, Mcgill University, Montreal, Quebec, Canada.
³¹ Neuroradiology Unit, Children's Hospital A. Meyer, Florence, Italy.
³² "Mario Serio" Department of Experimental and Clinical Biomedical Sciences, University of Florence, Italy.
³³ Instituto de Neurobiología, Universidad Nacional Autónoma de México. Querétaro, Querétaro, México.
³⁴ Support Center for Advanced Neuroimaging (SCAN), University Institute for Diagnostic and Interventional Neuroradiology, Inselspital, University of Bern, Bern, Switzerland.
³⁵ Central Finland Central Hospital, Medical Imaging Unit, Jyväskylä, Finland.
³⁶ Neuroradiology Unit, Department of Head and Neck and Neurosciences, Istituto Giannina Gaslini, Genova, Italy.
³⁷ Institute of Psychological Medicine and Clinical Neurosciences, Hadyn Ellis Building, Maindy Road, Cardiff, UK.
³⁸ Department of Neurology, University Hospital of Wales, Cardiff, UK.
³⁹ Department of Biomedical, Metabolic, and Neural Science, University of Modena and Reggio Emilia, NOCSE Hospital, Modena, Italy.
⁴⁰ Melbourne Brain Centre, Department of Medicine, University of Melbourne, Parkville, VIC, 3052, Australia.
⁴¹ Department of Neurology, Royal Melbourne Hospital, Parkville, 3050, Australia.
⁴² Department of Neurology, University Medicine Greifswald, Greifswald, Germany.
⁴³ Department of Epileptology, University Hospital Bonn, Bonn, Germany.
⁴⁴ Department of Neurology, Philips University of Marburg, Marburg Germany.
⁴⁵ Department of Neurocognition / Imaging, Life&Brain Research Centre, Bonn, Germany.
⁴⁶ The Affiliated Chenggong Hospital of Xiamen University, Xiamen, China.
⁴⁷ Department of Computer Science and Electrical Engineering, University of Maryland, Baltimore County, USA.
⁴⁸ Centre de Diagnostic Per la Imatge (CDIC), Hospital Clinic, Barcelona, Spain.
⁴⁹ Multimodal Imaging and Connectome Analysis Lab, Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada.
⁵⁰ Medical College of Wisconsin, Department of Neurology, Milwaukee, WI, USA.
⁵¹ FutureNeuro Research Centre, RCSI, Dublin, Ireland.
⁵² Division of Neurology, Beaumont Hospital, Dublin 9, Ireland.
⁵³ Department of Neurology, Hôpital Erasme, Universite Libre de Bruxelles, Brussels 1070, Belgium.
⁵⁴ Neurology Department, St. James's Hospital, Dublin 8, Ireland.
⁵⁵ Department of Clinical Neurophysiology, University Medicine Göttingen, Göttingen, Germany.
⁵⁶ Institute of Neurology, University "Magna Græcia", Catanzaro, Italy.
⁵⁷ Florey Department of Neuroscience and Mental Health, The University of Melbourne, Melbourne, VIC, Australia.
⁵⁸ Maryland Psychiatric Research Center, Department of Psychiatry, University of Maryland School of Medicine, Maryland, USA.
⁵⁹ Department of Medicine, University of Melbourne, Parkville, VIC, 3052, Australia.
⁶⁰ Department of Neurology, King's College Hospital, London, UK.
⁶¹ Pediatric Neurology and Muscular Diseases Unit, Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, University of Genoa, Genova, Italy.
⁶² Dept of Neuroscience, Mario Negri Institute for Pharmacological Research, Via G. La Masa 19, 20156 Milano, Italy.
⁶³ Department of Medical and Molecular Genetics, King's College London, London SE1 9RT, UK.
⁶⁴ Department of Clinical and Experimental Epilepsy, UCL Institute of Neurology, London, UK.
⁶⁵ Chalfont Centre for Epilepsy, Bucks, UK.

PMID: 29365066
PMCID: PMC5837616
DOI: 10.1093/brain/awx341

Abstract

Progressive functional decline in the epilepsies is largely unexplained. We formed the ENIGMA-Epilepsy consortium to understand factors that influence brain measures in epilepsy, pooling data from 24 research centres in 14 countries across Europe, North and South America, Asia, and Australia. Structural brain measures were extracted from MRI brain scans across 2149 individuals with epilepsy, divided into four epilepsy subgroups including idiopathic generalized epilepsies (n =367), mesial temporal lobe epilepsies with hippocampal sclerosis (MTLE; left, n = 415; right, n = 339), and all other epilepsies in aggregate (n = 1026), and compared to 1727 matched healthy controls. We ranked brain structures in order of greatest differences between patients and controls, by meta-analysing effect sizes across 16 subcortical and 68 cortical brain regions. We also tested effects of duration of disease, age at onset, and age-by-diagnosis interactions on structural measures. We observed widespread patterns of altered subcortical volume and reduced cortical grey matter thickness. Compared to controls, all epilepsy groups showed lower volume in the right thalamus (Cohen's d = -0.24 to -0.73; P < 1.49 × 10-4), and lower thickness in the precentral gyri bilaterally (d = -0.34 to -0.52; P < 4.31 × 10-6). Both MTLE subgroups showed profound volume reduction in the ipsilateral hippocampus (d = -1.73 to -1.91, P < 1.4 × 10-19), and lower thickness in extrahippocampal cortical regions, including the precentral and paracentral gyri, compared to controls (d = -0.36 to -0.52; P < 1.49 × 10-4). Thickness differences of the ipsilateral temporopolar, parahippocampal, entorhinal, and fusiform gyri, contralateral pars triangularis, and bilateral precuneus, superior frontal and caudal middle frontal gyri were observed in left, but not right, MTLE (d = -0.29 to -0.54; P < 1.49 × 10-4). Contrastingly, thickness differences of the ipsilateral pars opercularis, and contralateral transverse temporal gyrus, were observed in right, but not left, MTLE (d = -0.27 to -0.51; P < 1.49 × 10-4). Lower subcortical volume and cortical thickness associated with a longer duration of epilepsy in the all-epilepsies, all-other-epilepsies, and right MTLE groups (beta, b < -0.0018; P < 1.49 × 10-4). In the largest neuroimaging study of epilepsy to date, we provide information on the common epilepsies that could not be realistically acquired in any other way. Our study provides a robust ranking of brain measures that can be further targeted for study in genetic and neuropathological studies. This worldwide initiative identifies patterns of shared grey matter reduction across epilepsy syndromes, and distinctive abnormalities between epilepsy syndromes, which inform our understanding of epilepsy as a network disorder, and indicate that certain epilepsy syndromes involve more widespread structural compromise than previously assumed.

Keywords: MRI; epilepsy; precentral gyrus; thalamus.

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Figures

**Figure 1**
**Study flowchart.** ILAE = International League Against Epilepsy; MOU = memorandum of understanding.

**Figure 2**
**Subcortical volume findings.** Cohen’s d effect size estimates for case-control differences in subcortical volume, across the (A) all-epilepsies, (B) mesial temporal lobe epilepsies with left hippocampal sclerosis (HS; MTLE-L), (C) mesial temporal lobe epilepsies with right hippocampal sclerosis (MTLE-R), (D) idiopathic generalized epilepsies (IGE), and (E) all-other-epilepsies groups. Cohen’s d effect sizes were extracted using multiple linear regressions, and pooled across research centres using random-effects meta-analysis. Subcortical structures with P-values < 1.49 × 10⁻⁴ are shown in heatmap colours; strength of heat map is determined by the size of the Cohen’s d (d < 0 = blue, d > 0 = yellow/red). Image generated using MATLAB, with annotations added using Adobe Photoshop. An interactive version of this figure is available online, via ‘ENIGMA-Viewer’: http://enigma-viewer.org/ENIGMA_epilepsy_subcortical.html. See Supplementary material for guidelines on how to use the interactive visualization.

**Figure 3**
**Cortical thickness findings.** Cohen’s d effect size estimates for case-control differences in cortical thickness, across the (A) all-epilepsies, (B) mesial temporal lobe epilepsies with left hippocampal sclerosis (MTLE-L), (C) mesial temporal lobe epilepsies with right hippocampal sclerosis (MTLE-R), (D) idiopathic generalized epilepsies (IGE), and (E) all-other-epilepsies groups. Cohen’s d effect sizes were extracted using multiple linear regressions, and pooled across research centres using random-effects meta-analysis. Cortical structures with P-values < 1.49 × 10⁻⁴ are shown in heatmap colours; strength of heat map is determined by the size of the Cohen’s d (d < 0 = blue, d > 0 = yellow/red). Image generated using MATLAB with annotations added using Adobe Photoshop. An interactive version of this figure is available online, via ‘ENIGMA-Viewer’: http://enigma-viewer.org/ENIGMA_epilepsy_cortical.html. See Supplementary material for guidelines on how to use the interactive visualization. HS = hippocampal sclerosis.

See this image and copyright information in PMC

Comment in

Epileptic Seizures, Brain Volume Changes, and "Brain Damage": What Do We Know So Far?
Hogan RE. Hogan RE. Epilepsy Curr. 2018 Jul-Aug;18(4):224-226. doi: 10.5698/1535-7597.18.4.224. Epilepsy Curr. 2018. PMID: 30254514 Free PMC article. No abstract available.

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Structural brain abnormalities in the common epilepsies assessed in a worldwide ENIGMA study

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Structural brain abnormalities in the common epilepsies assessed in a worldwide ENIGMA study

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