Interpretable surface-based detection of focal cortical dysplasias: a Multi-centre Epilepsy Lesion Detection study.


Journal

Brain : a journal of neurology
ISSN: 1460-2156
Titre abrégé: Brain
Pays: England
ID NLM: 0372537

Informations de publication

Date de publication:
21 11 2022
Historique:
received: 14 12 2021
revised: 22 04 2022
accepted: 26 05 2022
pubmed: 12 8 2022
medline: 24 11 2022
entrez: 11 8 2022
Statut: ppublish

Résumé

One outstanding challenge for machine learning in diagnostic biomedical imaging is algorithm interpretability. A key application is the identification of subtle epileptogenic focal cortical dysplasias (FCDs) from structural MRI. FCDs are difficult to visualize on structural MRI but are often amenable to surgical resection. We aimed to develop an open-source, interpretable, surface-based machine-learning algorithm to automatically identify FCDs on heterogeneous structural MRI data from epilepsy surgery centres worldwide. The Multi-centre Epilepsy Lesion Detection (MELD) Project collated and harmonized a retrospective MRI cohort of 1015 participants, 618 patients with focal FCD-related epilepsy and 397 controls, from 22 epilepsy centres worldwide. We created a neural network for FCD detection based on 33 surface-based features. The network was trained and cross-validated on 50% of the total cohort and tested on the remaining 50% as well as on 2 independent test sites. Multidimensional feature analysis and integrated gradient saliencies were used to interrogate network performance. Our pipeline outputs individual patient reports, which identify the location of predicted lesions, alongside their imaging features and relative saliency to the classifier. On a restricted 'gold-standard' subcohort of seizure-free patients with FCD type IIB who had T1 and fluid-attenuated inversion recovery MRI data, the MELD FCD surface-based algorithm had a sensitivity of 85%. Across the entire withheld test cohort the sensitivity was 59% and specificity was 54%. After including a border zone around lesions, to account for uncertainty around the borders of manually delineated lesion masks, the sensitivity was 67%. This multicentre, multinational study with open access protocols and code has developed a robust and interpretable machine-learning algorithm for automated detection of focal cortical dysplasias, giving physicians greater confidence in the identification of subtle MRI lesions in individuals with epilepsy.

Identifiants

pubmed: 35953082
pii: 6659752
doi: 10.1093/brain/awac224
pmc: PMC9679165
doi:

Types de publication

Multicenter Study Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

3859-3871

Subventions

Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/W006251/1
Pays : United Kingdom
Organisme : NINDS NIH HHS
ID : R01 NS109439
Pays : United States

Informations de copyright

© The Author(s) 2022. Published by Oxford University Press on behalf of the Guarantors of Brain.

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Auteurs

Hannah Spitzer (H)

Institute of Computational Biology, Helmholtz Center Munich, Munich 85764, Germany.

Mathilde Ripart (M)

Department of Developmental Neuroscience, UCL Great Ormond Street Institute for Child Health, London WC1N 1EH, UK.

Kirstie Whitaker (K)

The Alan Turing Institute, London NW1 2DB, UK.

Felice D'Arco (F)

Great Ormond Street Hospital NHS Foundation Trust, London WC1N 3JH, UK.

Kshitij Mankad (K)

Great Ormond Street Hospital NHS Foundation Trust, London WC1N 3JH, UK.

Andrew A Chen (AA)

Penn Statistics in Imaging and Visualization Center, Department of Biostatistics, Epidemiology, and Informatics, University of Pennsylvania, Philadelphia, PA 19104, USA.
Center for Biomedical Image Computing and Analytics, University of Pennsylvania, Philadelphia, PA 19104, USA.

Antonio Napolitano (A)

Medical Physics Department, Bambino Gesù Children's Hospital, Rome 00165, Italy.

Luca De Palma (L)

Rare and Complex Epilepsies, Department of Neurosciences, Bambino Gesù Children's Hospital, IRCCS, Rome 00165, Italy.

Alessandro De Benedictis (A)

Neurosurgery Unit, Department of Neurosciences, Bambino Gesù Children's Hospital, IRCCS, Rome 00165, Italy.

Stephen Foldes (S)

Barrow Neurological Institute at Phoenix Children's Hospital, Phoenix, AZ 85016, USA.

Zachary Humphreys (Z)

Barrow Neurological Institute at Phoenix Children's Hospital, Phoenix, AZ 85016, USA.

Kai Zhang (K)

Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing 100054, China.

Wenhan Hu (W)

Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing 100054, China.

Jiajie Mo (J)

Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing 100054, China.

Marcus Likeman (M)

Bristol Royal Hospital for Children, Bristol BS2 8BJ, UK.

Shirin Davies (S)

School of Psychology, Cardiff University Brain Research Imaging Centre, Cardiff CF24 4HQ, UK.
The Welsh Epilepsy Unit, Cardiff and Vale University Health Board, University Hospital of Wales, Cardiff CF14 4XW, UK.

Christopher Güttler (C)

Charité University Hospital, Berlin 10117, Germany.

Matteo Lenge (M)

Neuroscience Department, Children's Hospital Meyer-University of Florence, Florence 50139, Italy.

Nathan T Cohen (NT)

Center for Neuroscience, Children's National Hospital, Washington, DC 20012, USA.

Yingying Tang (Y)

Department of Neurology, West China Hospital of Sichuan University, Chengdu 610093, China.
Epilepsy Center, Cleveland Clinic, Cleveland, OH 44106, USA.

Shan Wang (S)

Epilepsy Center, Cleveland Clinic, Cleveland, OH 44106, USA.
Department of Neurology, Epilepsy Center, Second Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou 310058, China.

Aswin Chari (A)

Department of Developmental Neuroscience, UCL Great Ormond Street Institute for Child Health, London WC1N 1EH, UK.
Great Ormond Street Hospital NHS Foundation Trust, London WC1N 3JH, UK.

Martin Tisdall (M)

Department of Developmental Neuroscience, UCL Great Ormond Street Institute for Child Health, London WC1N 1EH, UK.
Great Ormond Street Hospital NHS Foundation Trust, London WC1N 3JH, UK.

Nuria Bargallo (N)

Department of Neuroradiology, Hospital Clinic Barcelona and Magnetic Resonance Imaging, Core Facility, IDIBAPS, Barcelona 08036, Spain.
Centro de Investigación Biomédica en Red de Salud Mental, CIBERSAM, Madrid 28029, Spain.

Estefanía Conde-Blanco (E)

Magnetic Resonance Imaging, Core Facility, IDIBAPS, Barcelona 08036, Spain.

Jose Carlos Pariente (JC)

Magnetic Resonance Imaging, Core Facility, IDIBAPS, Barcelona 08036, Spain.

Saül Pascual-Diaz (S)

Magnetic Resonance Imaging, Core Facility, IDIBAPS, Barcelona 08036, Spain.

Ignacio Delgado-Martínez (I)

Department of Neurosurgery, Hospital del Mar, Barcelona 08003, Spain.

Carmen Pérez-Enríquez (C)

Department of Neurology, Hospital del Mar, Barcelona 08003, Spain.

Ilaria Lagorio (I)

IRCCS Istituto Giannina Gaslini, Genova 16147, Italy.

Eugenio Abela (E)

Center for Neuropsychiatry and Intellectual Disability, Psychiatrische Dienste Aargau AG, Windisch 5120, Switzerland.

Nandini Mullatti (N)

Institute of Psychiatry, Psychology and Neuroscience, King's College, London SE5 8AF, UK.

Jonathan O'Muircheartaigh (J)

Institute of Psychiatry, Psychology and Neuroscience, King's College, London SE5 8AF, UK.
Department of Perinatal Imaging and Health, St. Thomas' Hospital, King's College London, London SE1 7EH, UK.

Katy Vecchiato (K)

Department of Perinatal Imaging and Health, St. Thomas' Hospital, King's College London, London SE1 7EH, UK.
Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology and Neuroscience, King's College, London SE5 8AF, UK.

Yawu Liu (Y)

Department of Neurology, University of Eastern Finland, Kuopio 70210, Finland.

Maria Eugenia Caligiuri (ME)

Department of Medical and Surgical Sciences, Magna Graecia University of Catanzaro, Catanzaro 88100, Italy.

Ben Sinclair (B)

Department of Neuroscience, Central Clinical School, Monash University, Melbourne, VIC 3004, Australia.

Lucy Vivash (L)

Department of Neuroscience, Central Clinical School, Monash University, Melbourne, VIC 3004, Australia.
Department of Neurology, Monash University, Melbourne, VIC 3004, Australia.

Anna Willard (A)

Department of Neuroscience, Central Clinical School, Monash University, Melbourne, VIC 3004, Australia.

Jothy Kandasamy (J)

Royal Hospital for Children and Young People, Edinburgh EH16 4TJ, UK.

Ailsa McLellan (A)

Royal Hospital for Children and Young People, Edinburgh EH16 4TJ, UK.

Drahoslav Sokol (D)

Royal Hospital for Children and Young People, Edinburgh EH16 4TJ, UK.

Mira Semmelroch (M)

The Florey Institute of Neuroscience and Mental Health, University of Melbourne, Parkville, VIC 3052, Australia.

Ane G Kloster (AG)

Neurobiology Research Unit, Copenhagen University Hospital-Rigshospitalet, Copenhagen 2100, Denmark.

Giske Opheim (G)

Neurobiology Research Unit, Copenhagen University Hospital-Rigshospitalet, Copenhagen 2100, Denmark.
Department of Neuroradiology, Copenhagen University Hospital-Rigshospitalet, Copenhagen 2100, Denmark.

Letícia Ribeiro (L)

Department of Neurology, University of Campinas, Campinas 13083-888, Brazil.
Brazilian Institute of Neuroscience and Neurotechnology (BRAINN), University of Campinas, Campinas 13083-888, Brazil.

Clarissa Yasuda (C)

Department of Neurology, University of Campinas, Campinas 13083-888, Brazil.
Brazilian Institute of Neuroscience and Neurotechnology (BRAINN), University of Campinas, Campinas 13083-888, Brazil.

Camilla Rossi-Espagnet (C)

Neuroradiology Unit, IRCCS Bambino Gesù Children's Hospital, Rome 00165, Italy.

Khalid Hamandi (K)

School of Psychology, Cardiff University Brain Research Imaging Centre, Cardiff CF24 4HQ, UK.
The Welsh Epilepsy Unit, University Hospital of Wales, Cardiff CF14 4XW, UK.

Anna Tietze (A)

Charité University Hospital, Berlin 10117, Germany.

Carmen Barba (C)

Neuroscience Department, Children's Hospital Meyer-University of Florence, Florence 50139, Italy.

Renzo Guerrini (R)

Neuroscience Department, Children's Hospital Meyer-University of Florence, Florence 50139, Italy.

William Davis Gaillard (WD)

Center for Neuroscience, Children's National Hospital, Washington, DC 20012, USA.

Xiaozhen You (X)

Center for Neuroscience, Children's National Hospital, Washington, DC 20012, USA.

Irene Wang (I)

Epilepsy Center, Cleveland Clinic, Cleveland, OH 44106, USA.

Sofía González-Ortiz (S)

Department of Neuroradiology, Hospital del Mar, Barcelona 08003, Spain.
Magnetic Resonance Imaging Core Facility, Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona 08036, Spain.

Mariasavina Severino (M)

IRCCS Istituto Giannina Gaslini, Genova 16147, Italy.

Pasquale Striano (P)

IRCCS Istituto Giannina Gaslini, Genova 16147, Italy.
Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, University of Genova, Genova, Italy.

Domenico Tortora (D)

IRCCS Istituto Giannina Gaslini, Genova 16147, Italy.

Reetta Kälviäinen (R)

Department of Neurology, University of Eastern Finland, Kuopio 70210, Finland.
Kuopio Epilepsy Center, Neurocenter, Kuopio University Hospital, Kuopio 70210, Finland.

Antonio Gambardella (A)

Institute of Neurology, Department of Medical and Surgical Sciences, Magna Graecia University, Catanzaro 88100, Italy.

Angelo Labate (A)

Neurology Unit, Department of BIOMORF, University of Messina, Messina 98168, Italy.

Patricia Desmond (P)

Department of Radiology, The Royal Melbourne Hospital, University of Melbourne, Parkville, VIC 3050, Australia.

Elaine Lui (E)

Department of Radiology, The Royal Melbourne Hospital, University of Melbourne, Parkville, VIC 3050, Australia.

Terence O'Brien (T)

Department of Neuroscience, Central Clinical School, Monash University, Melbourne, VIC 3004, Australia.
Department of Medicine, The Royal Melbourne Hospital, Parkville, VIC, 3052, Australia.

Jay Shetty (J)

Royal Hospital for Children and Young People, Edinburgh EH16 4TJ, UK.

Graeme Jackson (G)

The Florey Institute of Neuroscience and Mental Health, Austin Campus, Heidelberg, VIC 3071, Australia.
Department of Neurology, Austin Health, Heidelberg, VIC 3084, Australia.

John S Duncan (JS)

UCL Queen Square Institute of Neurology, London WC1N 3BG, UK.

Gavin P Winston (GP)

UCL Queen Square Institute of Neurology, London WC1N 3BG, UK.
Department of Medicine, Division of Neurology, Queen's University, Kingston, ON, Canada K7L 3N6.

Lars H Pinborg (LH)

Neurobiology Research Unit, Copenhagen University Hospital-Rigshospitalet, Copenhagen 2100, Denmark.
Epilepsy Clinic, Department of Neurology, Copenhagen University Hospital-Rigshopsitalet, Copenhagen 2100, Denmark.

Fernando Cendes (F)

Department of Neurology, University of Campinas, Campinas 13083-888, Brazil.
Brazilian Institute of Neuroscience and Neurotechnology (BRAINN), University of Campinas, Campinas 13083-888, Brazil.

Fabian J Theis (FJ)

Institute of Computational Biology, Helmholtz Center Munich, Munich 85764, Germany.
Department of Mathematics, Technical University of Munich, Garching 85748, Germany.

Russell T Shinohara (RT)

Penn Statistics in Imaging and Visualization Center, Department of Biostatistics, Epidemiology, and Informatics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

J Helen Cross (JH)

Department of Developmental Neuroscience, UCL Great Ormond Street Institute for Child Health, London WC1N 1EH, UK.
Young Epilepsy, Lingfield, Surrey RH7 6PW, UK.

Torsten Baldeweg (T)

Department of Developmental Neuroscience, UCL Great Ormond Street Institute for Child Health, London WC1N 1EH, UK.
Great Ormond Street Hospital NHS Foundation Trust, London WC1N 3JH, UK.

Sophie Adler (S)

Department of Developmental Neuroscience, UCL Great Ormond Street Institute for Child Health, London WC1N 1EH, UK.

Konrad Wagstyl (K)

Department of Developmental Neuroscience, UCL Great Ormond Street Institute for Child Health, London WC1N 1EH, UK.
Wellcome Centre for Human Neuroimaging, University College London, London WC1N 3AR, UK.

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