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Machine Learning-Derived Multimodal Neuroimaging of Presurgical Target Area to Predict Individual's Seizure Outcomes After Epilepsy Surgery

Objectives: Half of the patients who have tailored resection of the suspected epileptogenic zone for drug-resistant epilepsy have recurrent postoperative seizures. Although neuroimaging has become an indispensable part of delineating the epileptogenic zone, no validated method uses neuroimaging of p...

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Autores principales: Tang, Yongxiang, Li, Weikai, Tao, Lue, Li, Jian, Long, Tingting, Li, Yulai, Chen, Dengming, Hu, Shuo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8814443/
https://www.ncbi.nlm.nih.gov/pubmed/35127691
http://dx.doi.org/10.3389/fcell.2021.669795
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author Tang, Yongxiang
Li, Weikai
Tao, Lue
Li, Jian
Long, Tingting
Li, Yulai
Chen, Dengming
Hu, Shuo
author_facet Tang, Yongxiang
Li, Weikai
Tao, Lue
Li, Jian
Long, Tingting
Li, Yulai
Chen, Dengming
Hu, Shuo
author_sort Tang, Yongxiang
collection PubMed
description Objectives: Half of the patients who have tailored resection of the suspected epileptogenic zone for drug-resistant epilepsy have recurrent postoperative seizures. Although neuroimaging has become an indispensable part of delineating the epileptogenic zone, no validated method uses neuroimaging of presurgical target area to predict an individual’s post-surgery seizure outcome. We aimed to develop and validate a machine learning-powered approach incorporating multimodal neuroimaging of a presurgical target area to predict an individual’s post-surgery seizure outcome in patients with drug-resistant focal epilepsy. Materials and Methods: One hundred and forty-one patients with drug-resistant focal epilepsy were classified either as having seizure-free (Engel class I) or seizure-recurrence (Engel class II through IV) at least 1 year after surgery. The presurgical magnetic resonance imaging, positron emission tomography, computed tomography, and postsurgical magnetic resonance imaging were co-registered for surgical target volume of interest (VOI) segmentation; all VOIs were decomposed into nine fixed views, then were inputted into the deep residual network (DRN) that was pretrained on Tiny-ImageNet dataset to extract and transfer deep features. A multi-kernel support vector machine (MKSVM) was used to integrate multiple views of feature sets and to predict seizure outcomes of the targeted VOIs. Leave-one-out validation was applied to develop a model for verifying the prediction. In the end, performance using this approach was assessed by calculating accuracy, sensitivity, and specificity. Receiver operating characteristic curves were generated, and the optimal area under the receiver operating characteristic curve (AUC) was calculated as a metric for classifying outcomes. Results: Application of DRN–MKSVM model based on presurgical target area neuroimaging demonstrated good performance in predicting seizure outcomes. The AUC ranged from 0.799 to 0.952. Importantly, the classification performance DRN–MKSVM model using data from multiple neuroimaging showed an accuracy of 91.5%, a sensitivity of 96.2%, a specificity of 85.5%, and AUCs of 0.95, which were significantly better than any other single-modal neuroimaging (all p ˂ 0.05). Conclusion: DRN–MKSVM, using multimodal compared with unimodal neuroimaging from the surgical target area, accurately predicted postsurgical outcomes. The preoperative individualized prediction of seizure outcomes in patients who have been judged eligible for epilepsy surgery could be conveniently facilitated. This may aid epileptologists in presurgical evaluation by providing a tool to explore various surgical options, offering complementary information to existing clinical techniques.
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spelling pubmed-88144432022-02-05 Machine Learning-Derived Multimodal Neuroimaging of Presurgical Target Area to Predict Individual's Seizure Outcomes After Epilepsy Surgery Tang, Yongxiang Li, Weikai Tao, Lue Li, Jian Long, Tingting Li, Yulai Chen, Dengming Hu, Shuo Front Cell Dev Biol Cell and Developmental Biology Objectives: Half of the patients who have tailored resection of the suspected epileptogenic zone for drug-resistant epilepsy have recurrent postoperative seizures. Although neuroimaging has become an indispensable part of delineating the epileptogenic zone, no validated method uses neuroimaging of presurgical target area to predict an individual’s post-surgery seizure outcome. We aimed to develop and validate a machine learning-powered approach incorporating multimodal neuroimaging of a presurgical target area to predict an individual’s post-surgery seizure outcome in patients with drug-resistant focal epilepsy. Materials and Methods: One hundred and forty-one patients with drug-resistant focal epilepsy were classified either as having seizure-free (Engel class I) or seizure-recurrence (Engel class II through IV) at least 1 year after surgery. The presurgical magnetic resonance imaging, positron emission tomography, computed tomography, and postsurgical magnetic resonance imaging were co-registered for surgical target volume of interest (VOI) segmentation; all VOIs were decomposed into nine fixed views, then were inputted into the deep residual network (DRN) that was pretrained on Tiny-ImageNet dataset to extract and transfer deep features. A multi-kernel support vector machine (MKSVM) was used to integrate multiple views of feature sets and to predict seizure outcomes of the targeted VOIs. Leave-one-out validation was applied to develop a model for verifying the prediction. In the end, performance using this approach was assessed by calculating accuracy, sensitivity, and specificity. Receiver operating characteristic curves were generated, and the optimal area under the receiver operating characteristic curve (AUC) was calculated as a metric for classifying outcomes. Results: Application of DRN–MKSVM model based on presurgical target area neuroimaging demonstrated good performance in predicting seizure outcomes. The AUC ranged from 0.799 to 0.952. Importantly, the classification performance DRN–MKSVM model using data from multiple neuroimaging showed an accuracy of 91.5%, a sensitivity of 96.2%, a specificity of 85.5%, and AUCs of 0.95, which were significantly better than any other single-modal neuroimaging (all p ˂ 0.05). Conclusion: DRN–MKSVM, using multimodal compared with unimodal neuroimaging from the surgical target area, accurately predicted postsurgical outcomes. The preoperative individualized prediction of seizure outcomes in patients who have been judged eligible for epilepsy surgery could be conveniently facilitated. This may aid epileptologists in presurgical evaluation by providing a tool to explore various surgical options, offering complementary information to existing clinical techniques. Frontiers Media S.A. 2022-01-21 /pmc/articles/PMC8814443/ /pubmed/35127691 http://dx.doi.org/10.3389/fcell.2021.669795 Text en Copyright © 2022 Tang, Li, Tao, Li, Long, Li, Chen and Hu. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Tang, Yongxiang
Li, Weikai
Tao, Lue
Li, Jian
Long, Tingting
Li, Yulai
Chen, Dengming
Hu, Shuo
Machine Learning-Derived Multimodal Neuroimaging of Presurgical Target Area to Predict Individual's Seizure Outcomes After Epilepsy Surgery
title Machine Learning-Derived Multimodal Neuroimaging of Presurgical Target Area to Predict Individual's Seizure Outcomes After Epilepsy Surgery
title_full Machine Learning-Derived Multimodal Neuroimaging of Presurgical Target Area to Predict Individual's Seizure Outcomes After Epilepsy Surgery
title_fullStr Machine Learning-Derived Multimodal Neuroimaging of Presurgical Target Area to Predict Individual's Seizure Outcomes After Epilepsy Surgery
title_full_unstemmed Machine Learning-Derived Multimodal Neuroimaging of Presurgical Target Area to Predict Individual's Seizure Outcomes After Epilepsy Surgery
title_short Machine Learning-Derived Multimodal Neuroimaging of Presurgical Target Area to Predict Individual's Seizure Outcomes After Epilepsy Surgery
title_sort machine learning-derived multimodal neuroimaging of presurgical target area to predict individual's seizure outcomes after epilepsy surgery
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8814443/
https://www.ncbi.nlm.nih.gov/pubmed/35127691
http://dx.doi.org/10.3389/fcell.2021.669795
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