ArticlebioRxiv : the preprint server for biology2024
A WORLDWIDE ENIGMA STUDY ON EPILEPSY-RELATED GRAY AND WHITE MATTER COMPROMISE ACROSS THE ADULT LIFESPAN.
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88 authors at 20 institutions in 15 countries.
Judy ChenMultimodal Imaging and Connectome Analysis Laboratory, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, QC, Canada.ORCID 0009-0004-6332-9935
Alexander NgoMultimodal Imaging and Connectome Analysis Laboratory, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, QC, Canada.ORCID 0000-0002-8999-9388
Raúl Rodríguez-CrucesMultimodal Imaging and Connectome Analysis Laboratory, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, QC, Canada.ORCID 0000-0002-2917-1212
Jessica RoyerMultimodal Imaging and Connectome Analysis Laboratory, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, QC, Canada.ORCID 0000-0002-4448-8998
Maria Eugenia CaligiuriNeuroscience Research Center, University Magna Græcia, Catanzaro, CZ, Italy.ORCID 0000-0002-2030-5552
Antonio GambardellaNeuroscience Research Center, University Magna Græcia, Catanzaro, CZ, Italy.ORCID 0000-0001-7384-3074
Luis ConchaInstitute of Neurobiology, Universidad Nacional Autónoma de México, Querétaro, México.ORCID 0000-0002-7842-3869
Simon S KellerInstitute of Systems, Molecular and Integrative Biology, University of Liverpool, Liverpool, United Kingdom.ORCID 0000-0001-5247-9795
Fernando CendesDepartment of Neurology, University of Campinas--UNICAMP, Campinas, São Paulo, Brazil.ORCID 0000-0001-9336-9568
Clarissa L YasudaDepartment of Neurology, University of Campinas--UNICAMP, Campinas, São Paulo, Brazil.ORCID 0000-0001-9084-7173
Marina K M AlvimDepartment of Neurology, University of Campinas--UNICAMP, Campinas, São Paulo, Brazil.ORCID 0000-0002-6780-0761
Leonardo BonilhaDepartment of Neurology, Emory University, Atlanta, GA, USA.ORCID 0000-0002-6153-8942
Ezequiel GleichgerrchtDepartment of Neurology, Emory University, Atlanta, GA, USA.ORCID 0000-0002-4212-4146
Niels K FockeDepartment of Neurology, University of Medicine Göttingen, Göttingen, Germany.ORCID 0000-0001-5486-6289
Barbara KreilkampDepartment of Neurology, University of Medicine Göttingen, Göttingen, Germany.ORCID 0000-0001-6881-5191
Martin DominInstitute of Diagnostic Radiology and Neuroradiology, Functional Imaging Unit, University Medicine Greifswald, Greifswald, Germany.ORCID 0000-0002-8620-966X
Felix von PodewilsDepartment of Neurology, University Medicine Greifswald, Epilepsy Center, Greifswald, Germany.ORCID 0000-0002-3134-8697
Soenke LangnerInstitute of Diagnostic Radiology and Neuroradiology, University Medicine Greifswald, Greifswald, Germany.ORCID 0000-0001-7241-1173
Christian RummelSupport Center for Advanced Neuroimaging (SCAN), University Institute of Diagnostic and Interventional Neuroradiology, University Hospital Bern, Bern, Switzerland.ORCID 0000-0003-2345-7938
Roland WiestSupport Center for Advanced Neuroimaging (SCAN), University Institute of Diagnostic and Interventional Neuroradiology, University Hospital Bern, Bern, Switzerland.ORCID 0000-0001-7030-2045
Pascal MartinDepartment of Neurology and Epileptology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.
Raviteja KotikalapudiDepartment of Neurology and Epileptology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.ORCID 0000-0003-4604-3367
Benjamin BenderDiagnostic and Interventional Neuroradiology, University Hospital Tübingen, Germany.ORCID 0000-0002-3205-4631
Terence J O'BrienDepartment of Neuroscience, Central Clinical School, Alfred Hospital, Monash University, Melbourne, Victoria, Australia.ORCID 0000-0002-7198-8621
Benjamin SinclairDepartment of Neuroscience, Central Clinical School, Alfred Hospital, Monash University, Melbourne, Victoria, Australia.
Lucy VivashDepartment of Neuroscience, Central Clinical School, Alfred Hospital, Monash University, Melbourne, Victoria, Australia.ORCID 0000-0002-1182-0907
Patrick KwanDepartments of Medicine and Radiology, The Royal Melbourne Hospital, The University of Melbourne, Parkville, Victoria, Australia.ORCID 0000-0001-7310-276X
Patricia M DesmondDepartments of Medicine and Radiology, The Royal Melbourne Hospital, The University of Melbourne, Parkville, Victoria, Australia.ORCID 0000-0002-4803-6323
Elaine LuiDepartments of Medicine and Radiology, The Royal Melbourne Hospital, The University of Melbourne, Parkville, Victoria, Australia.ORCID 0000-0001-6955-1140
Gian Marco DumaScientific Institute IRCCS E.Medea, Epilepsy Unit, Conegliano (TV), Italy.ORCID 0000-0002-0778-3920
Paolo BonanniScientific Institute IRCCS E.Medea, Epilepsy Unit, Conegliano (TV), Italy.
Alice BalleriniDepartment of Biomedical, Metabolic and Neural Science, University of Modena and Reggio Emilia, Modena, Italy.ORCID 0000-0002-0544-1599
Anna Elisabetta VaudanoNeurology Unit, OCB Hospital, Azienda Ospedaliera-Universitaria, Modena, Italy.ORCID 0000-0002-6280-7526
Stefano MelettiNeurology Unit, OCB Hospital, Azienda Ospedaliera-Universitaria, Modena, Italy.ORCID 0000-0003-0334-539X
Manuela TondelliDepartment of Biomedical, Metabolic and Neural Science, University of Modena and Reggio Emilia, Modena, Italy.ORCID 0000-0001-6698-5437
Saud AlhusainiDepartment of Molecular and Cellular Therapeutics, The Royal College of Surgeons in Ireland, Dublin, Ireland.ORCID 0000-0002-6869-3830
Colin P DohertyDepartment of Neurology, St James' Hospital, Dublin, Ireland.ORCID 0000-0002-8869-8567
Gianpiero L CavalleriDepartment of Molecular and Cellular Therapeutics, The Royal College of Surgeons in Ireland, Dublin, Ireland.ORCID 0000-0002-9802-0506
Norman DelantyDepartment of Molecular and Cellular Therapeutics, The Royal College of Surgeons in Ireland, Dublin, Ireland.
Reetta KälviäinenEpilepsy Center, Neuro Center, Kuopio University Hospital, Member of the European Reference Network for Rare and Complex Epilepsies EpiCARE, Kuopio, Finland.
Graeme D JacksonFlorey Institute of Neuroscience and Mental Health, University of Melbourne, Melbourne VIC 3010, Australia.ORCID 0000-0002-5378-5003
Magdalena KowalczykFlorey Institute of Neuroscience and Mental Health, University of Melbourne, Melbourne VIC 3010, Australia.
Mario MascalchiNeuroradiology Research Program, Meyer Children Hospital of Florence, University of Florence, Florence, Italy.
Mira SemmelrochFlorey Institute of Neuroscience and Mental Health, University of Melbourne, Melbourne VIC 3010, Australia.ORCID 0000-0002-9660-775X
Rhys H ThomasTransitional and Clinical Research Institute, Newcastle University, Newcastle upon Tyne, UK.ORCID 0000-0003-2062-8623
Hamid Soltanian-ZadehContol and Intelligent Processing Center of Excellence (CIPCE), School of Electrical and Computer Engineering, University of Tehran, Tehran, Iran.ORCID 0000-0002-7302-6856
Esmaeil Davoodi-BojdDepartment of Neurology, Henry Ford Health System, Detroit, MI, USA.ORCID 0000-0003-3122-3891
Junsong ZhangCognitive Science Department, Xiamen University, Xiamen, China.
Matteo LengeChild Neurology Unit and Laboratories, Neuroscience Department, Meyer Children's Hospital IRCCS, Florence, Italy.ORCID 0000-0003-2848-621X
Renzo GuerriniChild Neurology Unit and Laboratories, Neuroscience Department, Meyer Children's Hospital IRCCS, Florence, Italy.ORCID 0000-0002-7272-7079
Emanuele BartoliniIRCCS Stella Maris Foundation, Pisa, Italy.ORCID 0000-0002-5683-1941
Khalid HamandiCardiff University Brain Research Imaging Centre (CUBRIC), College of Biomedical and Life Sciences, Cardiff University, Cardiff, UK.ORCID 0000-0001-7116-262X
Sonya FoleyCardiff University Brain Research Imaging Centre (CUBRIC), College of Biomedical and Life Sciences, Cardiff University, Cardiff, UK.ORCID 0000-0002-8390-2709
Theodor RüberDepartment of Neuroradiology, University Hospital Bonn, Bonn, Germany.ORCID 0000-0002-6180-7671
Tobias BauerDepartment of Neuroradiology, University Hospital Bonn, Bonn, Germany.ORCID 0000-0002-0555-6214
Bernd WeberInstitute of Experimental Epileptology and Cognition Research, University Hospital Bonn, Bonn, Germany.ORCID 0000-0002-7811-9605
Benoit CaldairouNeuroimaging of Epilepsy Laboratory, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, QC, Canada.ORCID 0000-0002-2065-4859
Chantal DepondtDepartment of Neurology, Hôpital Erasme, Hôpital Universitaire de Bruxelles (HUB), Université Libre de Bruxelles, Brussels, Belgium.
Julie AbsilDepartment of Radiology, Hôpital Erasme, Université Libre de Bruxelles, Brussels, Belgium.ORCID 0000-0002-9420-2310
Sarah J A CarrSchool of Neuroscience, Institute of Psychiatry, Psychology and Neuroscience, King's College London, UK.ORCID 0000-0001-6641-4415
Eugenio AbelaSchool of Neuroscience, Institute of Psychiatry, Psychology and Neuroscience, King's College London, UK.
Mark P RichardsonSchool of Neuroscience, Institute of Psychiatry, Psychology and Neuroscience, King's College London, UK.ORCID 0000-0001-8925-3140
Orrin DevinskyDepartment of Neurology, NYU Grossman School of Medicine, New York, NY, United States.ORCID 0000-0003-0044-4632
Heath PardoeDepartment of Neurology, NYU Grossman School of Medicine, New York, NY, United States.ORCID 0000-0002-0123-2167
Mariasavina SeverinoIRCCS Istituto Giannina Gaslini, Genova, Italy.ORCID 0000-0003-4730-5322
Pasquale StrianoIRCCS Istituto Giannina Gaslini, Genova, Italy.ORCID 0000-0002-6065-1476
Domenico TortoraDepartment of Neurosciences, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, University of Genova, Genova, Italy.ORCID 0000-0002-5621-4046
Erik KaestnerDepartment of Radiation Medicine and Applied Sciences; Department of Psychiatry, Center for Multimodal Imaging and Genetics, University of California San Diego, La Jolla, CA, United States.ORCID 0000-0003-3252-5365
Sean N HattonDepartment of Neurosciences, Center for Multimodal Imaging and Genetics, University of California San Diego, La Jolla, CA, United States.ORCID 0000-0002-9149-8726
Donatello ArienzoDepartment of Radiation Medicine and Applied Sciences; Department of Psychiatry, Center for Multimodal Imaging and Genetics, University of California San Diego, La Jolla, CA, United States.ORCID 0000-0003-2590-6434
Sjoerd B VosDepartment of Clinical and Experimental Epilepsy, UCL Queen Square Institute of Neurology, London, UK.ORCID 0000-0002-8502-4487
Mina RytenDepartment of Clinical and Experimental Epilepsy, UCL Queen Square Institute of Neurology, London, UK.
Peter N TaylorDepartment of Clinical and Experimental Epilepsy, UCL Queen Square Institute of Neurology, London, UK.ORCID 0000-0003-2144-9838
John S DuncanDepartment of Clinical and Experimental Epilepsy, UCL Queen Square Institute of Neurology, London, UK.ORCID 0000-0002-1373-0681
Christopher D WhelanDepartment of Molecular and Cellular Therapeutics, The Royal College of Surgeons in Ireland, Dublin, Ireland.ORCID 0000-0003-0308-5583
Marian GalovicDepartment of Neurology, Clinical Neuroscience Center, University Hospital and University of Zürich, Zürich, Switzerland.ORCID 0000-0002-2307-071X
Gavin P WinstonDepartment of Clinical and Experimental Epilepsy, UCL Queen Square Institute of Neurology, London, UK.ORCID 0000-0001-9395-1478
Sophia I ThomopoulosImaging Genetics Center, Mark & Mary Stevens Institute for Neuroimaging and Informatics, Keck School of Medicine, University of Southern California, Los Angeles, CA, United States.ORCID 0000-0002-0046-4070
Paul M ThompsonImaging Genetics Center, Mark & Mary Stevens Institute for Neuroimaging and Informatics, Keck School of Medicine, University of Southern California, Los Angeles, CA, United States.ORCID 0000-0002-4720-8867
Sanjay M SisodiyaDepartment of Clinical and Experimental Epilepsy, UCL Queen Square Institute of Neurology, London, UK.ORCID 0000-0002-1511-5893
Angelo LabateNeurophysiopathology and Movement Disorders Clinic, Regional Epilepsy Center, University of Messina, Italy.ORCID 0000-0002-8827-7324
Carrie R McDonaldDepartment of Radiation Medicine and Applied Sciences; Department of Psychiatry, Center for Multimodal Imaging and Genetics, University of California San Diego, La Jolla, CA, United States.
Lorenzo CaciagliDepartment of Clinical and Experimental Epilepsy, UCL Queen Square Institute of Neurology, London, UK.ORCID 0000-0001-7189-9699
Neda BernasconiNeuroimaging of Epilepsy Laboratory, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, QC, Canada.
Andrea BernasconiNeuroimaging of Epilepsy Laboratory, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, QC, Canada.
Sara LarivièreMultimodal Imaging and Connectome Analysis Laboratory, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, QC, Canada.ORCID 0000-0001-5701-1307
Dewi SchraderBC Children's Hospital, University of British Columbia, Vancouver, BC, Canada.ORCID 0000-0003-0173-2716
Boris C BernhardtMultimodal Imaging and Connectome Analysis Laboratory, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, QC, Canada.ORCID 0000-0001-9256-6041
Montreal Neurological Institute and Hospital · CANational Hospital for Neurology and Neurosurgery · GBThe Royal Melbourne Hospital · AURoyal College of Surgeons in Ireland · IEUniversity of California San Diego · USUniversity of Modena and Reggio Emilia · ITKing's College London · GBMeyer Children's Hospital · ITThe University of Melbourne · AUUniversidade Estadual de Campinas (UNICAMP) · BRUniversitätsmedizin Greifswald · DEUniversity Hospital Bonn · DEEmory University · USHenry Ford Health System · USHertie Institute for Clinical Brain Research · DEIRCCS Eugenio Medea · ITIstituto Giannina Gaslini · ITMagna Graecia University · ITNew York University · USUniversité Libre de Bruxelles · BE
Funding
Lifespan Epilepsy Network Signatures (LENS): Leveraging ENIGMA-Epilepsy to Predict Cognitive Aging and Surgical OutcomesR01NS122827 · NINDS · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI CARRIE R MCDONALD · 2021 to 2026
$3.8MMultimodal imaging of memory in epilepsy from whole brain networks to local neuronal responses: Implications for surgical decision-makingR01NS124585 · NINDS · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI MCDONALD, CARRIE R · 2022 to 2025
$3.3MPrediction of seizure lateralization and postoperative outcome through the use of deep learning applied to multi-site MRI/DTI data: An ENIGMA-Epilepsy studyR21NS107739 · NINDS · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI BONILHA, LEONARDO F, MCDONALD, CARRIE R · 2019 to 2019
$444kMedical Research Council MR/S00355X/1NINDS NIH HHS R01 NS122827NINDS NIH HHS R01 NS124585NINDS NIH HHS R21 NS107739
Abstract
Objectives: Temporal lobe epilepsy (TLE) is commonly associated with mesiotemporal pathology and widespread alterations of grey and white matter structures. Evidence supports a progressive condition although the temporal evolution of TLE is poorly defined. This ENIGMA-Epilepsy study utilized multimodal magnetic resonance imaging (MRI) data to investigate structural alterations in TLE patients across the adult lifespan. We charted both grey and white matter changes and explored the covariance of age-related alterations in both compartments. Methods: We studied 769 TLE patients and 885 healthy controls across an age range of 17-73 years, from multiple international sites. To assess potentially non-linear lifespan changes in TLE, we harmonized data and combined median split assessments with cross-sectional sliding window analyses of grey and white matter age-related changes. Covariance analyses examined the coupling of grey and white matter lifespan curves. Results: In TLE, age was associated with a robust grey matter thickness/volume decline across a broad cortico-subcortical territory, extending beyond the mesiotemporal disease epicentre. White matter changes were also widespread across multiple tracts with peak effects in temporo-limbic fibers. While changes spanned the adult time window, changes accelerated in cortical thickness, subcortical volume, and fractional anisotropy (all decreased), and mean diffusivity (increased) after age 55 years. Covariance analyses revealed strong limbic associations between white matter tracts and subcortical structures with cortical regions. Conclusions: This study highlights the profound impact of TLE on lifespan changes in grey and white matter structures, with an acceleration of aging-related processes in later decades of life. Our findings motivate future longitudinal studies across the lifespan and emphasize the importance of prompt diagnosis as well as intervention in patients.
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agingatrophyEpilepsylifespanmultimodaltemporal lobe epilepsy
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