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      MRI-based deep learning can discriminate between temporal lobe epilepsy, Alzheimer’s disease, and healthy controls

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          Abstract

          Background

          Radiological identification of temporal lobe epilepsy (TLE) is crucial for diagnosis and treatment planning. TLE neuroimaging abnormalities are pervasive at the group level, but they can be subtle and difficult to identify by visual inspection of individual scans, prompting applications of artificial intelligence (AI) assisted technologies.

          Method

          We assessed the ability of a convolutional neural network (CNN) algorithm to classify TLE vs. patients with AD vs. healthy controls using T1-weighted magnetic resonance imaging (MRI) scans. We used feature visualization techniques to identify regions the CNN employed to differentiate disease types.

          Results

          We show the following classification results: healthy control accuracy = 81.54% (SD = 1.77%), precision = 0.81 (SD = 0.02), recall = 0.85 (SD = 0.03), and F1-score = 0.83 (SD = 0.02); TLE accuracy = 90.45% (SD = 1.59%), precision = 0.86 (SD = 0.03), recall = 0.86 (SD = 0.04), and F1-score = 0.85 (SD = 0.04); and AD accuracy = 88.52% (SD = 1.27%), precision = 0.64 (SD = 0.05), recall = 0.53 (SD = 0.07), and F1 score = 0.58 (0.05). The high accuracy in identification of TLE was remarkable, considering that only 47% of the cohort had deemed to be lesional based on MRI alone. Model predictions were also considerably better than random permutation classifications ( p < 0.01) and were independent of age effects.

          Conclusions

          AI (CNN deep learning) can classify and distinguish TLE, underscoring its potential utility for future computer-aided radiological assessments of epilepsy, especially for patients who do not exhibit easily identifiable TLE associated MRI features (e.g., hippocampal sclerosis).

          Plain language summary

          In people with temporal lobe epilepsy, seizures start in a particular part of the brain positioned behind the ears called the temporal lobe. It is difficult for a doctor to detect that a person has temporal lobe epilepsy using brain scans. In this study, we developed a computer model that was able to identify people with temporal lobe epilepsy from scans of their brain. This computer model could be used to help doctors identify temporal lobe epilepsy from brain scans in the future.

          Abstract

          Chang et al. classify people with Temporal Lobe Epilepsy (TLE), Alzheimer’s disease and healthy controls using a convolutional neural network algorithm applied to magnetic resonance imaging (MRI) scans. People with TLE can be distinguished, including those without easily identifiable TLE-associated MRI features.

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          Most cited references37

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          Revised terminology and concepts for organization of seizures and epilepsies: report of the ILAE Commission on Classification and Terminology, 2005-2009.

          The International League Against Epilepsy (ILAE) Commission on Classification and Terminology has revised concepts, terminology, and approaches for classifying seizures and forms of epilepsy. Generalized and focal are redefined for seizures as occurring in and rapidly engaging bilaterally distributed networks (generalized) and within networks limited to one hemisphere and either discretely localized or more widely distributed (focal). Classification of generalized seizures is simplified. No natural classification for focal seizures exists; focal seizures should be described according to their manifestations (e.g., dyscognitive, focal motor). The concepts of generalized and focal do not apply to electroclinical syndromes. Genetic, structural-metabolic, and unknown represent modified concepts to replace idiopathic, symptomatic, and cryptogenic. Not all epilepsies are recognized as electroclinical syndromes. Organization of forms of epilepsy is first by specificity: electroclinical syndromes, nonsyndromic epilepsies with structural-metabolic causes, and epilepsies of unknown cause. Further organization within these divisions can be accomplished in a flexible manner depending on purpose. Natural classes (e.g., specific underlying cause, age at onset, associated seizure type), or pragmatic groupings (e.g., epileptic encephalopathies, self-limited electroclinical syndromes) may serve as the basis for organizing knowledge about recognized forms of epilepsy and facilitate identification of new forms.
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            The Epidemiology of Epilepsy

            Epilepsy is a chronic disease of the brain characterized by an enduring (i.e., persisting) predisposition to generate seizures, unprovoked by any immediate central nervous system insult, and by the neurobiologic, cognitive, psychological, and social consequences of seizure recurrences. Epilepsy affects both sexes and all ages with worldwide distribution. The prevalence and the incidence of epilepsy are slightly higher in men compared to women and tend to peak in the elderly, reflecting the higher frequency of stroke, neurodegenerative diseases, and tumors in this age-group. Focal seizures are more common than generalized seizures both in children and in adults. The etiology of epilepsy varies according to the sociodemographic characteristics of the affected populations and the extent of the diagnostic workup, but a documented cause is still lacking in about 50% of cases from high-income countries (HIC). The overall prognosis of epilepsy is favorable in the majority of patients when measured by seizure freedom. Reports from low/middle-income countries (LMIC; where patients with epilepsy are largely untreated) give prevalence and remission rates that overlap those of HICs. As the incidence of epilepsy appears higher in most LMICs, the overlapping prevalence can be explained by misdiagnosis, acute symptomatic seizures and premature mortality. Studies have consistently shown that about one-half of cases tend to achieve prolonged seizure remission. However, more recent reports on the long-term prognosis of epilepsy have identified differing prognostic patterns, including early and late remission, a relapsing-remitting course, and even a worsening course (characterized by remission followed by relapse and unremitting seizures). Epilepsy per se carries a low mortality risk, but significant differences in mortality rates are expected when comparing incidence and prevalence studies, children and adults, and persons with idiopathic and symptomatic seizures. Sudden unexplained death is most frequent in people with generalized tonic-clonic seizures, nocturnal seizures, and drug refractory epilepsy.
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              Brain atrophy in Alzheimer's Disease and aging.

              Thanks to its safety and accessibility, magnetic resonance imaging (MRI) is extensively used in clinical routine and research field, largely contributing to our understanding of the pathophysiology of neurodegenerative disorders such as Alzheimer's disease (AD). This review aims to provide a comprehensive overview of the main findings in AD and normal aging over the past twenty years, focusing on the patterns of gray and white matter changes assessed in vivo using MRI. Major progresses in the field concern the segmentation of the hippocampus with novel manual and automatic segmentation approaches, which might soon enable to assess also hippocampal subfields. Advancements in quantification of hippocampal volumetry might pave the way to its broader use as outcome marker in AD clinical trials. Patterns of cortical atrophy have been shown to accurately track disease progression and seem promising in distinguishing among AD subtypes. Disease progression has also been associated with changes in white matter tracts. Recent studies have investigated two areas often overlooked in AD, such as the striatum and basal forebrain, reporting significant atrophy, although the impact of these changes on cognition is still unclear. Future integration of different MRI modalities may further advance the field by providing more powerful biomarkers of disease onset and progression.
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                Author and article information

                Contributors
                leonardo.bonilha@emory.edu
                Journal
                Commun Med (Lond)
                Commun Med (Lond)
                Communications Medicine
                Nature Publishing Group UK (London )
                2730-664X
                27 February 2023
                27 February 2023
                2023
                : 3
                : 33
                Affiliations
                [1 ]GRID grid.259828.c, ISNI 0000 0001 2189 3475, Department of Neurology, , Medical University of South Carolina, ; Charleston, SC USA
                [2 ]GRID grid.189967.8, ISNI 0000 0001 0941 6502, Department of Neurology, , Emory University School of Medicine, ; Atlanta, GA USA
                [3 ]GRID grid.15090.3d, ISNI 0000 0000 8786 803X, Department of Epileptology, , University Hospital Bonn, ; Venusberg-Campus 1, 53127 Bonn, Germany
                [4 ]GRID grid.10025.36, ISNI 0000 0004 1936 8470, Department of Pharmacology and Therapeutics, Institute of Systems, Molecular and Integrative Biology, , University of Liverpool, ; Liverpool, UK
                [5 ]GRID grid.412162.2, ISNI 0000 0004 0441 5844, Department of Neurosurgery, , Emory University Hospital, ; Atlanta, GA USA
                [6 ]GRID grid.511426.5, Tri-institutional Center for Translational Research in Neuroimaging and Data Science (TReNDS), , Georgia State University, Georgia Institute of Technology, Emory University, ; Atlanta, GA USA
                [7 ]GRID grid.213917.f, ISNI 0000 0001 2097 4943, School of Electrical & Computer Engineering, , Georgia Institute of Technology, ; Atlanta, GA USA
                [8 ]GRID grid.266100.3, ISNI 0000 0001 2107 4242, Department of Psychology, , University of California, ; San Diego, CA USA
                [9 ]GRID grid.15090.3d, ISNI 0000 0000 8786 803X, Institute of Experimental Epileptology and Cognition Research, University Hospital Bonn, ; Venusberg-Campus 1, 53127 Bonn, Germany
                Author information
                http://orcid.org/0000-0001-8483-3226
                http://orcid.org/0000-0002-6180-7671
                http://orcid.org/0000-0001-9223-5314
                http://orcid.org/0000-0001-9058-0747
                Article
                262
                10.1038/s43856-023-00262-4
                9970972
                36849746
                3ffce2de-b7fc-4081-aa56-26b79aa13d87
                © The Author(s) 2023

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 11 August 2022
                : 10 February 2023
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                © The Author(s) 2023

                network models,epilepsy
                network models, epilepsy

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