Disease detection and classification in temporal lobe epilepsy: step-wise versus simultaneous AI decision models in a multisite neuroimaging study.
Authors
Affiliations (68)
Affiliations (68)
- Department of Radiation Medicine and Applied Sciences, University of California, San Diego, La Jolla, CA 92037, USA.
- Halıcıoğlu Data Science Institute, University of California, San Diego, La Jolla, CA 92093, USA.
- Department of Mathematics and Statistics, San Diego State University, San Diego, CA 92182, USA.
- Department of Neurology, Emory University, Atlanta, GA 30322, USA.
- Department of Neurosciences, University of California, San Diego, La Jolla, CA 92093, USA.
- GSU/GATech/Emory Center for Translational Research in Neuroimaging and Data Science (TReNDS), Atlanta, GA 30303, USA.
- Electrical and Computer Engineering, Georgia Institute of Technology, Atlanta, GA 30332, USA.
- Center for Translational Research in Neuroimaging and Data Science, Georgia State University, Atlanta, GA 30303, USA.
- Imaging Genetics Center, Mark and Mary Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, Marina del Rey, CA 90292, USA.
- Brazilian Institute of Neuroscience and Neurotechnology (BRAINN), Campinas, SP 13083-970, Brazil.
- Department of Neurology, University of Campinas (UNICAMP), Campinas, SP 13083-888, Brazil.
- Neuroimaging Laboratory, University of Campinas (UNICAMP), Campinas, SP 13083-888, Brazil.
- Department of Clinical and Experimental Epilepsy, UCL Queen Square Institute of Neurology, London WC1N 3BG, UK.
- Dublin Neurological Institute, Mater Misericordiae University Hospital, Dublin D07 W7XF, Ireland.
- School of Medicine, University College Dublin, Dublin D04 V1W8, Ireland.
- Centre for Medical Image Computing, Department of Medical Physics and Biomedical Engineering, University College London, London WC1E 6BT, UK.
- Department of Neurology, University Medical Center Göttingen, Göttingen 37075, Germany.
- Department of Psychiatry and Psychotherapy, University of Cologne, Cologne 50937, Germany.
- Department of Neurology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
- Department of Biomedical, Metabolic and Neural Sciences, University of Modena and Reggio Emilia, Baggiovara 41126, Italy.
- Department of Radiology, CUB Erasme Hospital, Hôpital Universitaire de Bruxelles, Université Libre de Bruxelles, Brussels 1070, Belgium.
- Department of Medical Imaging and Radiation Sciences, Faculty of Medicine and Health Sciences, Université de Sherbrooke, Sherbrooke, QC J1H 5N4, Canada.
- Department of Neurology, Clinical Neuroscience Center, University Hospital and University of Zurich, Zurich 8091, Switzerland.
- Department of Neurology, University Hospital Zurich, Zurich 8091, Switzerland.
- Epilepsy and Clinical Neurophysiology Unit, Scientific Institute IRCCS E. Medea, Conegliano 31015, Italy.
- Department of Neurology, University of California SanFrancisco, San Francisco, CA 94158, USA.
- Department of Neuroscience and Human Genetics, Meyer Children's Hospital IRCCS, Florence 50139, Italy.
- Department of Neuroscience, Pharmacology and Child Health, University of Florence, Florence 50139, Italy.
- Department of Neuroradiology, University Hospital Bonn, Bonn 53127, Germany.
- Department of Epileptology, University Hospital Bonn, Bonn 53127, Germany.
- German Center for Neurodegenerative Diseases (DZNE), Bonn 53127, Germany.
- Center for Medical Data Usability and Translation, University of Bonn, Bonn 53127, Germany.
- Department of Neuroscience, School of Translational Medicine, Alfred Health, Monash University, Melbourne, VIC 53127, Australia.
- Department of Neurology, Alfred Health, Melbourne, VIC 3004, Australia.
- Neurophysiopathology and Movement Disorders Clinic, University of Messina, Messina 98125, Italy.
- IRCCS G. Gaslini, Full Member of Epicare, Genova 16147, Italy.
- Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, University of Genova, Genova 16132, Italy.
- Departments of Medicine and Neurology, the Royal Melbourne Hospital, The University of Melbourne, Parkville, VIC 3050, Australia.
- Department of Radiology, AOU Cagliari and University of Cagliari, Cagliari 09042, Italy.
- Children's National Hospital (CNH), Washington, DC 20010, USA.
- Department of Developmental Neuroscience, IRCCS Foundation Stella Maris, Pisa 56128, Italy.
- Department of Psychiatry, Neuroscience Institute, University of Cape Town, Cape Town 7925, South Africa.
- Centre of Excellence in Epilepsy at the Neuro and McConnell Brain Imaging Centre, Montreal Neurological Institute, McGill University, Montreal, QC H3A 2B4, Canada.
- Department of Neurology and Epileptology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen 72076, Germany.
- Department of Neurology, CUB Erasme Hospital, Hôpital Universitaire de Bruxelles, Université Libre de Bruxelles, Brussels 1070, Belgium.
- Department of Neurological Sciences, Rush University Medical Center, Chicago, IL 60612, USA.
- Department of Biomedical, Metabolic and Neuronal Science, University of Modena and Reggio Emilia, Modena 41125, Italy.
- Neurophysiology Unit and Epilepsy Centre, AOU Modena, Modena 41126, Italy.
- Department of Neurology, School of Medicine at Hofstra/Northwell, Hempstead, NY 11549, USA.
- Institute of Neurobiology, Universidad Nacional Autónoma de México, Querétaro 76230, Mexico.
- University of Pittsburgh Comprehensive Epilepsy Center (UPCEC), Department of Neurology, School of Medicine, University of Pittsburgh, Pittsburgh, PA 15213, USA.
- Center for Neuroengineering and Therapeutics, University of Pennsylvania, Philadelphia, PA 19104, United States.
- Department of Neurology, David Geffen School of Medicine at UCLA, Los Angeles, CA 90095, USA.
- Clinic for Neurology, University Medical Center Göttingen, Göttingen 37075, Germany.
- Department of Neurology, NYU Grossman School of Medicine, NewYork, NY 10016, USA.
- Florey Institute of Neuroscience and Mental Health, Heidelberg, VIC 3084, Australia.
- NYU Comprehensive Epilepsy Center, NewYork, NY 10016, USA.
- Department of Neurology, Langone School of Medicine, NewYork University, New York, NY 10016, USA.
- Department of Radiology, Jinling Hospital, Affiliated Hospital of Medical School, Nanjing University, Nanjing 210002, China.
- Institute of Neurology, Magna Græcia University, Catanzaro 88100, Italy.
- Neuroscience Research Center, Magna Græcia University, Catanzaro 88100, Italy.
- Department of Neurology, Medical University of South Carolina, Charleston, SC 29425, USA.
- Department of Neurology, FCM, University of Campinas-UNICAMP, Campinas, SP 13083-888, Brazil.
- Brazilian Institute of Neuroscience and Neurotechnology, Campinas, SP 13083-970, Brazil.
- Chalfont Centre for Epilepsy, Chalfont St Peter, Bucks SL9 0RJ, UK.
- Tri-institutional Center for Translational Research in Neuroimaging and Data Science (TReNDS), Georgia State, Georgia Tech, Emory, Atlanta, GA 30303, USA.
- Department of Neurology, University of South Carolina, Columbia, SC 29203, USA.
- Department of Psychiatry, University of California, San Diego, La Jolla, CA 92037, USA.
Abstract
Diagnostic MRI evaluation of temporal lobe epilepsy (TLE) depends on the subjective visual interpretation of MRI images. These interpretations could be enhanced by quantitative artificial intelligence (AI) support tools. Humans often make sequential and conditional decisions during their radiological interpretations, such as whether an abnormality is present and, if present, characterizing the abnormality. It is not known whether it is superior to train AI to treat every decision separately in a similar step-wise manner or to train a model holistically on all decisions simultaneously. Here, we analysed three large epilepsy MRI datasets [<i>n</i> = 3676, 2320 people with epilepsy and 1356 healthy controls (HC)] to perform two tasks: (i) establish the presence of a TLE pattern on MRI and (ii) determine TLE pattern lateralization. We compared Step-wise models that independently classify TLE versus HC and lateralize patients as left TLE (L-TLE) or right TLE (R-TLE), against a simultaneous model trained to distinguish all three classes in a single step. To do this, 3D volumetric T1-weighted images were input into an EfficientNetV2 model multiple times to ensure reproducibility of results. Class prediction, model classification confidence and saliency maps were output for interpretability. Step-wise models outperformed the Simultaneous model on both tasks (both <i>P</i>s < 0.001), with an average ∼2.8% accuracy increase for discriminating HC from TLE and an average 12.7% accuracy increase for distinguishing L-TLE from R-TLE. For both the Step-wise and Simultaneous models, important features discriminating TLE from HC included the known TLE limbic pattern involving the hippocampus, parahippocampal cortical regions, cingulate cortex and lateral temporal regions. However, there was less concordance between the Step-wise and Simultaneous models for the L-TLE versus R-TLE task (all Fisher's <i>Z</i>s > 10.5, <i>P</i>s < 0.001); the Step-wise model focused less on subcortical regions such as the thalamus and hippocampus and focused more on distributed cortical pathology. Across the two Step-wise models, 95.1% of TLE patients had accurate classifications in either HC versus TLE and/or L-TLE versus R-TLE tasks. These results included 69.6% of patients being both correctly labelled as TLE and lateralized, 13.9% being correctly labelled TLE but lateralized incorrectly and 11.6% being lateralized correctly but not detected as TLE. These findings provide evidence that diagnostic tasks with simpler, Step-wise AI models may enhance diagnostic performance and interpretability in clinical workflows. Future AI clinical support tools can leverage this step-wise approach in the early identification of TLE-related structural patterns, supporting timely diagnosis and treatment decisions.