NeuroImage: Clinical (Jan 2021)
Artificial intelligence for classification of temporal lobe epilepsy with ROI-level MRI data: A worldwide ENIGMA-Epilepsy study
- Ezequiel Gleichgerrcht,
- Brent C. Munsell,
- Saud Alhusaini,
- Marina K.M. Alvim,
- Núria Bargalló,
- Benjamin Bender,
- Andrea Bernasconi,
- Neda Bernasconi,
- Boris Bernhardt,
- Karen Blackmon,
- Maria Eugenia Caligiuri,
- Fernando Cendes,
- Luis Concha,
- Patricia M. Desmond,
- Orrin Devinsky,
- Colin P. Doherty,
- Martin Domin,
- John S. Duncan,
- Niels K. Focke,
- Antonio Gambardella,
- Bo Gong,
- Renzo Guerrini,
- Sean N. Hatton,
- Reetta Kälviäinen,
- Simon S. Keller,
- Peter Kochunov,
- Raviteja Kotikalapudi,
- Barbara A.K. Kreilkamp,
- Angelo Labate,
- Soenke Langner,
- Sara Larivière,
- Matteo Lenge,
- Elaine Lui,
- Pascal Martin,
- Mario Mascalchi,
- Stefano Meletti,
- Terence J. O'Brien,
- Heath R. Pardoe,
- Jose C. Pariente,
- Jun Xian Rao,
- Mark P. Richardson,
- Raúl Rodríguez-Cruces,
- Theodor Rüber,
- Ben Sinclair,
- Hamid Soltanian-Zadeh,
- Dan J. Stein,
- Pasquale Striano,
- Peter N. Taylor,
- Rhys H. Thomas,
- Anna Elisabetta Vaudano,
- Lucy Vivash,
- Felix von Podewills,
- Sjoerd B. Vos,
- Bernd Weber,
- Yi Yao,
- Clarissa Lin Yasuda,
- Junsong Zhang,
- Paul M. Thompson,
- Sanjay M. Sisodiya,
- Carrie R. McDonald,
- Leonardo Bonilha,
- Andre Altmann,
- Chantal Depondt,
- Marian Galovic,
- Sophia I. Thomopoulos,
- Roland Wiest
Affiliations
- Ezequiel Gleichgerrcht
- Department of Neurology, Medical University of South Carolina, Charleston, SC, USA; Corresponding author.
- Brent C. Munsell
- Department of Psychiatry, University of North Carolina at Chapel Hill, NC, USA; Department of Computer Science, University of North Carolina at Chapel Hill, NC, USA
- Saud Alhusaini
- Neurology Department, Yale University School of Medicine, New Haven, CT, USA; Department of Molecular and Cellular Therapeutics, The Royal College of Surgeons in Ireland, Dublin, Ireland
- Marina K.M. Alvim
- Department of Neurology and Neuroimaging Laboratory, University of Campinas - UNICAMP, Campinas, SP, Brazil
- Núria Bargalló
- Magnetic Resonance Image Core Facility, Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Universitat de Barcelona, Barcelona, Spain; Department of Radiology of Center of Image Diagnosis (CDIC), Hospital Clinic de Barcelona, Barcelona, Spain
- Benjamin Bender
- Department of Diagnostic and Interventional Neuroradiology, University Hospital Tübingen, Tübingen, Germany
- Andrea Bernasconi
- Neuroimaging of Epilepsy Laboratory, Montreal Neurological Institute, McGill University, Montreal, QC, Canada
- Neda Bernasconi
- Neuroimaging of Epilepsy Laboratory, Montreal Neurological Institute, McGill University, Montreal, QC, Canada
- Boris Bernhardt
- McConnell Brain Imaging Center, Montreal Neurological Institute, McGill University, Montreal, QC, Canada
- Karen Blackmon
- Psychiatry and Psychology, Mayo Clinic, Jacksonville, FL, USA
- Maria Eugenia Caligiuri
- Neuroscience Research Center, Department of Medical and Surgical Sciences, University “Magna Græcia“ of Catanzaro, Catanzaro, Italy
- Fernando Cendes
- Department of Neurology and Neuroimaging Laboratory, University of Campinas - UNICAMP, Campinas, SP, Brazil
- Luis Concha
- Instituto de Neurobiología, Universidad Nacional Autónoma de México, Querétaro, Mexico
- Patricia M. Desmond
- Department of Radiology, Royal Melbourne Hospital, University of Melbourne, Melbourne, VIC, Australia
- Orrin Devinsky
- Department of Neurology, Langone School of Medicine, New York University, New York, NY, USA
- Colin P. Doherty
- Trinity College Dublin, School of Medicine, Dublin, Ireland; FutureNeuro SFI Research Centre for Rare and Chronic Neurological Diseases, Dublin, Ireland
- Martin Domin
- Functional Imaging Unit, Department of Diagnostic Radiology and Neuroradiology, University Medicine Greifswald, Greifswald, Germany
- John S. Duncan
- Department of Clinical and Experimental Epilepsy, UCL Queen Square Institute of Neurology, London, UK
- Niels K. Focke
- University Medicine Göttingen, Clinical Neurophysiology, Göttingen, Germany
- Antonio Gambardella
- Neuroscience Research Center, Department of Medical and Surgical Sciences, University “Magna Græcia“ of Catanzaro, Catanzaro, Italy; Institute of Neurology, University “Magna Græcia“ of Catanzaro, Catanzaro, Italy
- Bo Gong
- Department of Radiology, BC Children’s Hospital, University of British Columbia, Vancouver, BC, Canada
- Renzo Guerrini
- Neuroscience Department, University of Florence, Florence, Italy
- Sean N. Hatton
- Center for Multimodal Imaging and Genetics, University of California, San Diego, La Jolla, CA, USA
- Reetta Kälviäinen
- Kuopio University Hospital, Member of EpiCARE ERN, Kuopio, Finland; Institute of Clinical Medicine, Neurology, University of Eastern Finland, Kuopio, Finland
- Simon S. Keller
- Institute of Systems, Molecular and Integrative Biology, University of Liverpool, Liverpool, UK; The Walton Centre NHS Foundation Trust, Liverpool, UK
- Peter Kochunov
- Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD, USA
- Raviteja Kotikalapudi
- Department of Diagnostic and Interventional Neuroradiology, University Hospital Tübingen, Tübingen, Germany; Department of Clinical Neurophysiology, University Hospital Göttingen, Goettingen, Germany; Department of Neurology and Epileptology, Hertie Institute for Clinical Brain Research, University Hospital Tübingen, Tübingen, Germany
- Barbara A.K. Kreilkamp
- University Medicine Göttingen, Clinical Neurophysiology, Göttingen, Germany; Institute of Systems, Molecular and Integrative Biology, University of Liverpool, Liverpool, UK
- Angelo Labate
- Neuroscience Research Center, Department of Medical and Surgical Sciences, University “Magna Græcia“ of Catanzaro, Catanzaro, Italy; Institute of Neurology, University “Magna Græcia“ of Catanzaro, Catanzaro, Italy
- Soenke Langner
- Institute for Diagnostic Radiology and Neuroradiology, University Medicine Greifswald, Greifswald, Germany; Institute for Diagnostic and Interventional Radiology, Pediatric and Neuroradiology, University Medical Centre Rostock, Rostock, Germany
- Sara Larivière
- McConnell Brain Imaging Center, Montreal Neurological Institute, McGill University, Montreal, QC, Canada
- Matteo Lenge
- Pediatric Neurology, Neurogenetics and Neurobiology Unit and Laboratories, Children’s Hospital A. Meyer-University of Florence, Florence, Italy; Functional and Epilepsy Neurosurgery Unit, Neurosurgery Department, Children’s Hospital A. Meyer-University of Florence, Florence, Italy
- Elaine Lui
- Department of Radiology, Royal Melbourne Hospital, University of Melbourne, Melbourne, VIC, Australia
- Pascal Martin
- Department of Neurology and Epileptology, Hertie Institute for Clinical Brain Research, University Hospital Tübingen, Tübingen, Germany
- Mario Mascalchi
- ‘Mario Serio’ Department of Clinical and Experimental Medica Sciences, University of Florence, Florence, Italy
- Stefano Meletti
- Department of Biomedical, Metabolic, and Neural Sciences, University of Modena and Reggio Emilia, Modena, Italy; Neurology Unit, OCB Hospital, AOU Modena, Modena, Italy
- Terence J. O'Brien
- Department of Neuroscience, Monash University, Melbourne, VIC, Australia; The Department of Medicine (The Royal Melbourne Hospital), The University of Melbourne, Parkville, VIC, Australia; Department of Neurology, Alfred Health, Melbourne, VIC, Australia
- Heath R. Pardoe
- Department of Neurology, Langone School of Medicine, New York University, New York, NY, USA
- Jose C. Pariente
- Magnetic Resonance Image Core Facility, Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Universitat de Barcelona, Barcelona, Spain
- Jun Xian Rao
- Department of Psychiatry, University of California San Diego, La Jolla, CA, USA
- Mark P. Richardson
- Division of Neuroscience, King’s College London, London, UK
- Raúl Rodríguez-Cruces
- Instituto de Neurobiología, Universidad Nacional Autónoma de México, Querétaro, Mexico; Montreal Neurological Institute and Hospital, McGill University, Montreal, QC, Canada
- Theodor Rüber
- Department of Epileptology, University Hospital Bonn, Bonn, Germany
- Ben Sinclair
- Department of Neuroscience, Monash University, Melbourne, VIC, Australia; The Department of Medicine (The Royal Melbourne Hospital), The University of Melbourne, Parkville, VIC, Australia; Department of Neurology, Alfred Health, Melbourne, VIC, Australia
- Hamid Soltanian-Zadeh
- Radiology and Research Administration, Henry Ford Health System, Detroit, MI, USA; School of Electrical and Computer Engineering, College of Engineering, University of Tehran, Tehran, Iran
- Dan J. Stein
- SA MRC Unit on Risk & Resilience in Mental Disorders, Department of Psychiatry & Neuroscience Institute, University of Cape Town, Cape Town, South Africa
- Pasquale Striano
- IRCCS Istituto ‘G. Gaslini’, Genova, Italy; Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, University of Genova, Genova, Italy
- Peter N. Taylor
- Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, University of Genova, Genova, Italy; School of Computing, Newcastle University, Newcastle Upon Tyne, UK
- Rhys H. Thomas
- Institute of Translational and Clinical Research, Newcastle University, Newcastle Upon Tyne, UK
- Anna Elisabetta Vaudano
- Department of Biomedical, Metabolic, and Neural Sciences, University of Modena and Reggio Emilia, Modena, Italy; Neurology Unit, OCB Hospital, AOU Modena, Modena, Italy
- Lucy Vivash
- Department of Neuroscience, Monash University, Melbourne, VIC, Australia; The Department of Medicine (The Royal Melbourne Hospital), The University of Melbourne, Parkville, VIC, Australia; Department of Neurology, Alfred Health, Melbourne, VIC, Australia
- Felix von Podewills
- Department of Neurology, Epilepsy Center, University Medicine Greifswald, Greifswald, Germany
- Sjoerd B. Vos
- Centre for Medical Image Computing, Department of Computer Science, University College London, London, UK; Neuroradiological Academic Unit, UCL Queen Square Institute of Neurology, University College London, London, UK
- Bernd Weber
- Institute of Experimental Epileptology and Cognition Research, University of Bonn, Bonn, Germany
- Yi Yao
- Institute of Experimental Epileptology and Cognition Research, University of Bonn, Bonn, Germany
- Clarissa Lin Yasuda
- Department of Neurology and Neuroimaging Laboratory, University of Campinas - UNICAMP, Campinas, SP, Brazil
- Junsong Zhang
- Cognitive Science Department, School of Informatics, Xiamen University, Xiamen, China
- Paul M. Thompson
- Imaging Genetics Center, Mark and Mary Stevens Institute for Neuroimaging and Informatics, Keck School of Medicine, University of Southern California, Marina del Rey, CA, USA
- Sanjay M. Sisodiya
- UCL Queen Square Institute of Neurology, London, UK; Chalfont Centre for Epilepsy, Bucks, UK
- Carrie R. McDonald
- Department of Psychiatry, University of California San Diego, La Jolla, CA, USA
- Leonardo Bonilha
- Department of Neurology, Medical University of South Carolina, Charleston, SC, USA
- Andre Altmann
- Centre for Medical Image Computing, Department of Medical Physics and Biomedical Engineering, University College London, London, UK
- Chantal Depondt
- Department of Neurology, Hôpital Erasme, Université Libre de Bruxelles, Brussels, Belgium
- Marian Galovic
- Department of Clinical and Experimental Epilepsy, UCL Queen Square Institute of Neurology, London, UK; Department of Neurology, University Hospital Zurich, Zurich, Switzerland
- Sophia I. Thomopoulos
- Imaging Genetics Center, Mark and Mary Stevens Institute for Neuroimaging and Informatics, Keck School of Medicine, University of Southern California, Marina del Rey, CA, USA
- Roland Wiest
- Department of Neurology and Epileptology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany
- Journal volume & issue
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Vol. 31
p. 102765
Abstract
Artificial intelligence has recently gained popularity across different medical fields to aid in the detection of diseases based on pathology samples or medical imaging findings. Brain magnetic resonance imaging (MRI) is a key assessment tool for patients with temporal lobe epilepsy (TLE). The role of machine learning and artificial intelligence to increase detection of brain abnormalities in TLE remains inconclusive. We used support vector machine (SV) and deep learning (DL) models based on region of interest (ROI-based) structural (n = 336) and diffusion (n = 863) brain MRI data from patients with TLE with (“lesional”) and without (“non-lesional”) radiographic features suggestive of underlying hippocampal sclerosis from the multinational (multi-center) ENIGMA-Epilepsy consortium. Our data showed that models to identify TLE performed better or similar (68–75%) compared to models to lateralize the side of TLE (56–73%, except structural-based) based on diffusion data with the opposite pattern seen for structural data (67–75% to diagnose vs. 83% to lateralize). In other aspects, structural and diffusion-based models showed similar classification accuracies. Our classification models for patients with hippocampal sclerosis were more accurate (68–76%) than models that stratified non-lesional patients (53–62%). Overall, SV and DL models performed similarly with several instances in which SV mildly outperformed DL. We discuss the relative performance of these models with ROI-level data and the implications for future applications of machine learning and artificial intelligence in epilepsy care.