Machine learning approaches for imaging‐based prognostication of the outcome of surgery for mesial temporal lobe epilepsy

Objectives Around 30% of patients undergoing surgical resection for drug‐resistant mesial temporal lobe epilepsy (MTLE) do not obtain seizure freedom. Success of anterior temporal lobe resection (ATLR) critically depends on the careful selection of surgical candidates, aiming at optimizing seizure f...

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Veröffentlicht in:Epilepsia (Copenhagen) 2022-05, Vol.63 (5), p.1081-1092
Hauptverfasser: Sinclair, Benjamin, Cahill, Varduhi, Seah, Jarrel, Kitchen, Andy, Vivash, Lucy E., Chen, Zhibin, Malpas, Charles B., O'Shea, Marie F., Desmond, Patricia M., Hicks, Rodney J., Morokoff, Andrew P., King, James A., Fabinyi, Gavin C., Kaye, Andrew H., Kwan, Patrick, Berkovic, Samuel F., Law, Meng, O'Brien, Terence J.
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container_issue 5
container_start_page 1081
container_title Epilepsia (Copenhagen)
container_volume 63
creator Sinclair, Benjamin
Cahill, Varduhi
Seah, Jarrel
Kitchen, Andy
Vivash, Lucy E.
Chen, Zhibin
Malpas, Charles B.
O'Shea, Marie F.
Desmond, Patricia M.
Hicks, Rodney J.
Morokoff, Andrew P.
King, James A.
Fabinyi, Gavin C.
Kaye, Andrew H.
Kwan, Patrick
Berkovic, Samuel F.
Law, Meng
O'Brien, Terence J.
description Objectives Around 30% of patients undergoing surgical resection for drug‐resistant mesial temporal lobe epilepsy (MTLE) do not obtain seizure freedom. Success of anterior temporal lobe resection (ATLR) critically depends on the careful selection of surgical candidates, aiming at optimizing seizure freedom while minimizing postoperative morbidity. Structural MRI and FDG‐PET neuroimaging are routinely used in presurgical assessment and guide the decision to proceed to surgery. In this study, we evaluate the potential of machine learning techniques applied to standard presurgical MRI and PET imaging features to provide enhanced prognostic value relative to current practice. Methods Eighty two patients with drug resistant MTLE were scanned with FDG‐PET pre‐surgery and T1‐weighted MRI pre‐ and postsurgery. From these images the following features of interest were derived: volume of temporal lobe (TL) hypometabolism, % of extratemporal hypometabolism, presence of contralateral TL hypometabolism, presence of hippocampal sclerosis, laterality of seizure onset volume of tissue resected and % of temporal lobe hypometabolism resected. These measures were used as predictor variables in logistic regression, support vector machines, random forests and artificial neural networks. Results In the study cohort, 24 of 82 (28.3%) who underwent an ATLR for drug‐resistant MTLE did not achieve Engel Class I (i.e., free of disabling seizures) outcome at a minimum of 2 years of postoperative follow‐up. We found that machine learning approaches were able to predict up to 73% of the 24 ATLR surgical patients who did not achieve a Class I outcome, at the expense of incorrect prediction for up to 31% of patients who did achieve a Class I outcome. Overall accuracies ranged from 70% to 80%, with an area under the receiver operating characteristic curve (AUC) of .75–.81. We additionally found that information regarding overall extent of both total and significantly hypometabolic tissue resected was crucial to predictive performance, with AUC dropping to .59–.62 using presurgical information alone. Incorporating the laterality of seizure onset and the choice of machine learning algorithm did not significantly change predictive performance. Significance Collectively, these results indicate that "acceptable" to "good" patient‐specific prognostication for drug‐resistant MTLE surgery is feasible with machine learning approaches utilizing commonly collected imaging modalities, but that informa
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Success of anterior temporal lobe resection (ATLR) critically depends on the careful selection of surgical candidates, aiming at optimizing seizure freedom while minimizing postoperative morbidity. Structural MRI and FDG‐PET neuroimaging are routinely used in presurgical assessment and guide the decision to proceed to surgery. In this study, we evaluate the potential of machine learning techniques applied to standard presurgical MRI and PET imaging features to provide enhanced prognostic value relative to current practice. Methods Eighty two patients with drug resistant MTLE were scanned with FDG‐PET pre‐surgery and T1‐weighted MRI pre‐ and postsurgery. From these images the following features of interest were derived: volume of temporal lobe (TL) hypometabolism, % of extratemporal hypometabolism, presence of contralateral TL hypometabolism, presence of hippocampal sclerosis, laterality of seizure onset volume of tissue resected and % of temporal lobe hypometabolism resected. These measures were used as predictor variables in logistic regression, support vector machines, random forests and artificial neural networks. Results In the study cohort, 24 of 82 (28.3%) who underwent an ATLR for drug‐resistant MTLE did not achieve Engel Class I (i.e., free of disabling seizures) outcome at a minimum of 2 years of postoperative follow‐up. We found that machine learning approaches were able to predict up to 73% of the 24 ATLR surgical patients who did not achieve a Class I outcome, at the expense of incorrect prediction for up to 31% of patients who did achieve a Class I outcome. Overall accuracies ranged from 70% to 80%, with an area under the receiver operating characteristic curve (AUC) of .75–.81. We additionally found that information regarding overall extent of both total and significantly hypometabolic tissue resected was crucial to predictive performance, with AUC dropping to .59–.62 using presurgical information alone. Incorporating the laterality of seizure onset and the choice of machine learning algorithm did not significantly change predictive performance. Significance Collectively, these results indicate that "acceptable" to "good" patient‐specific prognostication for drug‐resistant MTLE surgery is feasible with machine learning approaches utilizing commonly collected imaging modalities, but that information on the surgical resection region is critical for optimal prognostication.</description><identifier>ISSN: 0013-9580</identifier><identifier>EISSN: 1528-1167</identifier><identifier>DOI: 10.1111/epi.17217</identifier><identifier>PMID: 35266138</identifier><language>eng</language><publisher>United States: Wiley Subscription Services, Inc</publisher><subject>Choice learning ; Convulsions &amp; seizures ; Drug resistance ; Drug Resistant Epilepsy - diagnostic imaging ; Drug Resistant Epilepsy - surgery ; Epilepsy ; Epilepsy, Temporal Lobe - diagnostic imaging ; Epilepsy, Temporal Lobe - surgery ; FDG‐PET ; Fluorodeoxyglucose F18 ; Hippocampus ; Humans ; Learning algorithms ; Machine Learning ; Magnetic Resonance Imaging ; Morbidity ; Neural networks ; Neuroimaging ; Patients ; Positron emission tomography ; Sclerosis ; Seizures ; Surgery ; Temporal lobe ; Treatment Outcome</subject><ispartof>Epilepsia (Copenhagen), 2022-05, Vol.63 (5), p.1081-1092</ispartof><rights>2022 The Authors. published by Wiley Periodicals LLC on behalf of International League Against Epilepsy</rights><rights>2022 The Authors. Epilepsia published by Wiley Periodicals LLC on behalf of International League Against Epilepsy.</rights><rights>2022. This article is published under http://creativecommons.org/licenses/by-nc/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3887-548c0f092a6ab0273ae0472df6d173e97c5fa2e8a396c034bb08b575bcd7c4cd3</citedby><cites>FETCH-LOGICAL-c3887-548c0f092a6ab0273ae0472df6d173e97c5fa2e8a396c034bb08b575bcd7c4cd3</cites><orcidid>0000-0002-0850-3644 ; 0000-0002-7198-8621 ; 0000-0003-0534-3718 ; 0000-0003-4580-841X ; 0000-0002-1182-0907 ; 0000-0001-7310-276X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fepi.17217$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fepi.17217$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>314,776,780,1411,27903,27904,45553,45554</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35266138$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Sinclair, Benjamin</creatorcontrib><creatorcontrib>Cahill, Varduhi</creatorcontrib><creatorcontrib>Seah, Jarrel</creatorcontrib><creatorcontrib>Kitchen, Andy</creatorcontrib><creatorcontrib>Vivash, Lucy E.</creatorcontrib><creatorcontrib>Chen, Zhibin</creatorcontrib><creatorcontrib>Malpas, Charles B.</creatorcontrib><creatorcontrib>O'Shea, Marie F.</creatorcontrib><creatorcontrib>Desmond, Patricia M.</creatorcontrib><creatorcontrib>Hicks, Rodney J.</creatorcontrib><creatorcontrib>Morokoff, Andrew P.</creatorcontrib><creatorcontrib>King, James A.</creatorcontrib><creatorcontrib>Fabinyi, Gavin C.</creatorcontrib><creatorcontrib>Kaye, Andrew H.</creatorcontrib><creatorcontrib>Kwan, Patrick</creatorcontrib><creatorcontrib>Berkovic, Samuel F.</creatorcontrib><creatorcontrib>Law, Meng</creatorcontrib><creatorcontrib>O'Brien, Terence J.</creatorcontrib><title>Machine learning approaches for imaging‐based prognostication of the outcome of surgery for mesial temporal lobe epilepsy</title><title>Epilepsia (Copenhagen)</title><addtitle>Epilepsia</addtitle><description>Objectives Around 30% of patients undergoing surgical resection for drug‐resistant mesial temporal lobe epilepsy (MTLE) do not obtain seizure freedom. Success of anterior temporal lobe resection (ATLR) critically depends on the careful selection of surgical candidates, aiming at optimizing seizure freedom while minimizing postoperative morbidity. Structural MRI and FDG‐PET neuroimaging are routinely used in presurgical assessment and guide the decision to proceed to surgery. In this study, we evaluate the potential of machine learning techniques applied to standard presurgical MRI and PET imaging features to provide enhanced prognostic value relative to current practice. Methods Eighty two patients with drug resistant MTLE were scanned with FDG‐PET pre‐surgery and T1‐weighted MRI pre‐ and postsurgery. From these images the following features of interest were derived: volume of temporal lobe (TL) hypometabolism, % of extratemporal hypometabolism, presence of contralateral TL hypometabolism, presence of hippocampal sclerosis, laterality of seizure onset volume of tissue resected and % of temporal lobe hypometabolism resected. These measures were used as predictor variables in logistic regression, support vector machines, random forests and artificial neural networks. Results In the study cohort, 24 of 82 (28.3%) who underwent an ATLR for drug‐resistant MTLE did not achieve Engel Class I (i.e., free of disabling seizures) outcome at a minimum of 2 years of postoperative follow‐up. We found that machine learning approaches were able to predict up to 73% of the 24 ATLR surgical patients who did not achieve a Class I outcome, at the expense of incorrect prediction for up to 31% of patients who did achieve a Class I outcome. Overall accuracies ranged from 70% to 80%, with an area under the receiver operating characteristic curve (AUC) of .75–.81. We additionally found that information regarding overall extent of both total and significantly hypometabolic tissue resected was crucial to predictive performance, with AUC dropping to .59–.62 using presurgical information alone. Incorporating the laterality of seizure onset and the choice of machine learning algorithm did not significantly change predictive performance. Significance Collectively, these results indicate that "acceptable" to "good" patient‐specific prognostication for drug‐resistant MTLE surgery is feasible with machine learning approaches utilizing commonly collected imaging modalities, but that information on the surgical resection region is critical for optimal prognostication.</description><subject>Choice learning</subject><subject>Convulsions &amp; seizures</subject><subject>Drug resistance</subject><subject>Drug Resistant Epilepsy - diagnostic imaging</subject><subject>Drug Resistant Epilepsy - surgery</subject><subject>Epilepsy</subject><subject>Epilepsy, Temporal Lobe - diagnostic imaging</subject><subject>Epilepsy, Temporal Lobe - surgery</subject><subject>FDG‐PET</subject><subject>Fluorodeoxyglucose F18</subject><subject>Hippocampus</subject><subject>Humans</subject><subject>Learning algorithms</subject><subject>Machine Learning</subject><subject>Magnetic Resonance Imaging</subject><subject>Morbidity</subject><subject>Neural networks</subject><subject>Neuroimaging</subject><subject>Patients</subject><subject>Positron emission tomography</subject><subject>Sclerosis</subject><subject>Seizures</subject><subject>Surgery</subject><subject>Temporal lobe</subject><subject>Treatment Outcome</subject><issn>0013-9580</issn><issn>1528-1167</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><recordid>eNp1kb1OwzAUhS0EglIYeAFkiQWGtHYcx86IqgKVimCAOXKcmzYoiYOdCFUsPALPyJPg_sCAhBfb1989Or4HoTNKRtSvMbTliIqQij00oDyUAaWx2EcDQigLEi7JETp27oUQImLBDtER42EcUyYH6P1e6WXZAK5A2aZsFli1rTW-CA4XxuKyVgtf_vr4zJSDHPvHRWNcV2rVlabBpsDdErDpO21qWF9dbxdgV5vuGlypKtxB3RrrD5XJAHu7FbRudYIOClU5ON3tQ_R8M32a3AXzh9vZ5HoeaCalCHgkNSlIEqpYZSQUTAGJRJgXcU4Fg0RoXqgQpGJJrAmLsozIjAue6VzoSOdsiC63ut77aw-uS-vSaagq1YDpXRrGTBIaMcE9evEHfTG9bbw7T_Ek4SKRxFNXW0pb45yFIm2tn5NdpZSk60RS_8V0k4hnz3eKfVZD_kv-ROCB8RZ481NZ_a-UTh9nW8lvlqmX0Q</recordid><startdate>202205</startdate><enddate>202205</enddate><creator>Sinclair, Benjamin</creator><creator>Cahill, Varduhi</creator><creator>Seah, Jarrel</creator><creator>Kitchen, Andy</creator><creator>Vivash, Lucy E.</creator><creator>Chen, Zhibin</creator><creator>Malpas, Charles B.</creator><creator>O'Shea, Marie F.</creator><creator>Desmond, Patricia M.</creator><creator>Hicks, Rodney J.</creator><creator>Morokoff, Andrew P.</creator><creator>King, James A.</creator><creator>Fabinyi, Gavin C.</creator><creator>Kaye, Andrew H.</creator><creator>Kwan, Patrick</creator><creator>Berkovic, Samuel F.</creator><creator>Law, Meng</creator><creator>O'Brien, Terence J.</creator><general>Wiley Subscription Services, Inc</general><scope>24P</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7TK</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-0850-3644</orcidid><orcidid>https://orcid.org/0000-0002-7198-8621</orcidid><orcidid>https://orcid.org/0000-0003-0534-3718</orcidid><orcidid>https://orcid.org/0000-0003-4580-841X</orcidid><orcidid>https://orcid.org/0000-0002-1182-0907</orcidid><orcidid>https://orcid.org/0000-0001-7310-276X</orcidid></search><sort><creationdate>202205</creationdate><title>Machine learning approaches for imaging‐based prognostication of the outcome of surgery for mesial temporal lobe epilepsy</title><author>Sinclair, Benjamin ; Cahill, Varduhi ; Seah, Jarrel ; Kitchen, Andy ; Vivash, Lucy E. ; Chen, Zhibin ; Malpas, Charles B. ; O'Shea, Marie F. ; Desmond, Patricia M. ; Hicks, Rodney J. ; Morokoff, Andrew P. ; King, James A. ; Fabinyi, Gavin C. ; Kaye, Andrew H. ; Kwan, Patrick ; Berkovic, Samuel F. ; Law, Meng ; O'Brien, Terence J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3887-548c0f092a6ab0273ae0472df6d173e97c5fa2e8a396c034bb08b575bcd7c4cd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Choice learning</topic><topic>Convulsions &amp; seizures</topic><topic>Drug resistance</topic><topic>Drug Resistant Epilepsy - diagnostic imaging</topic><topic>Drug Resistant Epilepsy - surgery</topic><topic>Epilepsy</topic><topic>Epilepsy, Temporal Lobe - diagnostic imaging</topic><topic>Epilepsy, Temporal Lobe - surgery</topic><topic>FDG‐PET</topic><topic>Fluorodeoxyglucose F18</topic><topic>Hippocampus</topic><topic>Humans</topic><topic>Learning algorithms</topic><topic>Machine Learning</topic><topic>Magnetic Resonance Imaging</topic><topic>Morbidity</topic><topic>Neural networks</topic><topic>Neuroimaging</topic><topic>Patients</topic><topic>Positron emission tomography</topic><topic>Sclerosis</topic><topic>Seizures</topic><topic>Surgery</topic><topic>Temporal lobe</topic><topic>Treatment Outcome</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sinclair, Benjamin</creatorcontrib><creatorcontrib>Cahill, Varduhi</creatorcontrib><creatorcontrib>Seah, Jarrel</creatorcontrib><creatorcontrib>Kitchen, Andy</creatorcontrib><creatorcontrib>Vivash, Lucy E.</creatorcontrib><creatorcontrib>Chen, Zhibin</creatorcontrib><creatorcontrib>Malpas, Charles B.</creatorcontrib><creatorcontrib>O'Shea, Marie F.</creatorcontrib><creatorcontrib>Desmond, Patricia M.</creatorcontrib><creatorcontrib>Hicks, Rodney J.</creatorcontrib><creatorcontrib>Morokoff, Andrew P.</creatorcontrib><creatorcontrib>King, James A.</creatorcontrib><creatorcontrib>Fabinyi, Gavin C.</creatorcontrib><creatorcontrib>Kaye, Andrew H.</creatorcontrib><creatorcontrib>Kwan, Patrick</creatorcontrib><creatorcontrib>Berkovic, Samuel F.</creatorcontrib><creatorcontrib>Law, Meng</creatorcontrib><creatorcontrib>O'Brien, Terence J.</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Epilepsia (Copenhagen)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sinclair, Benjamin</au><au>Cahill, Varduhi</au><au>Seah, Jarrel</au><au>Kitchen, Andy</au><au>Vivash, Lucy E.</au><au>Chen, Zhibin</au><au>Malpas, Charles B.</au><au>O'Shea, Marie F.</au><au>Desmond, Patricia M.</au><au>Hicks, Rodney J.</au><au>Morokoff, Andrew P.</au><au>King, James A.</au><au>Fabinyi, Gavin C.</au><au>Kaye, Andrew H.</au><au>Kwan, Patrick</au><au>Berkovic, Samuel F.</au><au>Law, Meng</au><au>O'Brien, Terence J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Machine learning approaches for imaging‐based prognostication of the outcome of surgery for mesial temporal lobe epilepsy</atitle><jtitle>Epilepsia (Copenhagen)</jtitle><addtitle>Epilepsia</addtitle><date>2022-05</date><risdate>2022</risdate><volume>63</volume><issue>5</issue><spage>1081</spage><epage>1092</epage><pages>1081-1092</pages><issn>0013-9580</issn><eissn>1528-1167</eissn><abstract>Objectives Around 30% of patients undergoing surgical resection for drug‐resistant mesial temporal lobe epilepsy (MTLE) do not obtain seizure freedom. Success of anterior temporal lobe resection (ATLR) critically depends on the careful selection of surgical candidates, aiming at optimizing seizure freedom while minimizing postoperative morbidity. Structural MRI and FDG‐PET neuroimaging are routinely used in presurgical assessment and guide the decision to proceed to surgery. In this study, we evaluate the potential of machine learning techniques applied to standard presurgical MRI and PET imaging features to provide enhanced prognostic value relative to current practice. Methods Eighty two patients with drug resistant MTLE were scanned with FDG‐PET pre‐surgery and T1‐weighted MRI pre‐ and postsurgery. From these images the following features of interest were derived: volume of temporal lobe (TL) hypometabolism, % of extratemporal hypometabolism, presence of contralateral TL hypometabolism, presence of hippocampal sclerosis, laterality of seizure onset volume of tissue resected and % of temporal lobe hypometabolism resected. These measures were used as predictor variables in logistic regression, support vector machines, random forests and artificial neural networks. Results In the study cohort, 24 of 82 (28.3%) who underwent an ATLR for drug‐resistant MTLE did not achieve Engel Class I (i.e., free of disabling seizures) outcome at a minimum of 2 years of postoperative follow‐up. We found that machine learning approaches were able to predict up to 73% of the 24 ATLR surgical patients who did not achieve a Class I outcome, at the expense of incorrect prediction for up to 31% of patients who did achieve a Class I outcome. Overall accuracies ranged from 70% to 80%, with an area under the receiver operating characteristic curve (AUC) of .75–.81. We additionally found that information regarding overall extent of both total and significantly hypometabolic tissue resected was crucial to predictive performance, with AUC dropping to .59–.62 using presurgical information alone. Incorporating the laterality of seizure onset and the choice of machine learning algorithm did not significantly change predictive performance. Significance Collectively, these results indicate that "acceptable" to "good" patient‐specific prognostication for drug‐resistant MTLE surgery is feasible with machine learning approaches utilizing commonly collected imaging modalities, but that information on the surgical resection region is critical for optimal prognostication.</abstract><cop>United States</cop><pub>Wiley Subscription Services, Inc</pub><pmid>35266138</pmid><doi>10.1111/epi.17217</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0002-0850-3644</orcidid><orcidid>https://orcid.org/0000-0002-7198-8621</orcidid><orcidid>https://orcid.org/0000-0003-0534-3718</orcidid><orcidid>https://orcid.org/0000-0003-4580-841X</orcidid><orcidid>https://orcid.org/0000-0002-1182-0907</orcidid><orcidid>https://orcid.org/0000-0001-7310-276X</orcidid><oa>free_for_read</oa></addata></record>
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subjects Choice learning
Convulsions & seizures
Drug resistance
Drug Resistant Epilepsy - diagnostic imaging
Drug Resistant Epilepsy - surgery
Epilepsy
Epilepsy, Temporal Lobe - diagnostic imaging
Epilepsy, Temporal Lobe - surgery
FDG‐PET
Fluorodeoxyglucose F18
Hippocampus
Humans
Learning algorithms
Machine Learning
Magnetic Resonance Imaging
Morbidity
Neural networks
Neuroimaging
Patients
Positron emission tomography
Sclerosis
Seizures
Surgery
Temporal lobe
Treatment Outcome
title Machine learning approaches for imaging‐based prognostication of the outcome of surgery for mesial temporal lobe epilepsy
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