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Interictal magnetoencephalography abnormalities to guide intracranial electrode implantation and predict surgical outcome

Intracranial EEG is the gold standard technique for epileptogenic zone localization but requires a preconceived hypothesis of the location of the epileptogenic tissue. This placement is guided by qualitative interpretations of seizure semiology, MRI, EEG and other imaging modalities, such as magneto...

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Autores principales: Owen, Thomas W, Janiukstyte, Vytene, Hall, Gerard R, Chowdhury, Fahmida A, Diehl, Beate, McEvoy, Andrew, Miserocchi, Anna, de Tisi, Jane, Duncan, John S, Rugg-Gunn, Fergus, Wang, Yujiang, Taylor, Peter N
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10636564/
https://www.ncbi.nlm.nih.gov/pubmed/37953844
http://dx.doi.org/10.1093/braincomms/fcad292
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author Owen, Thomas W
Janiukstyte, Vytene
Hall, Gerard R
Chowdhury, Fahmida A
Diehl, Beate
McEvoy, Andrew
Miserocchi, Anna
de Tisi, Jane
Duncan, John S
Rugg-Gunn, Fergus
Wang, Yujiang
Taylor, Peter N
author_facet Owen, Thomas W
Janiukstyte, Vytene
Hall, Gerard R
Chowdhury, Fahmida A
Diehl, Beate
McEvoy, Andrew
Miserocchi, Anna
de Tisi, Jane
Duncan, John S
Rugg-Gunn, Fergus
Wang, Yujiang
Taylor, Peter N
author_sort Owen, Thomas W
collection PubMed
description Intracranial EEG is the gold standard technique for epileptogenic zone localization but requires a preconceived hypothesis of the location of the epileptogenic tissue. This placement is guided by qualitative interpretations of seizure semiology, MRI, EEG and other imaging modalities, such as magnetoencephalography. Quantitative abnormality mapping using magnetoencephalography has recently been shown to have potential clinical value. We hypothesized that if quantifiable magnetoencephalography abnormalities were sampled by intracranial EEG, then patients’ post-resection seizure outcome may be better. Thirty-two individuals with refractory neocortical epilepsy underwent magnetoencephalography and subsequent intracranial EEG recordings as part of presurgical evaluation. Eyes-closed resting-state interictal magnetoencephalography band power abnormality maps were derived from 70 healthy controls as a normative baseline. Magnetoencephalography abnormality maps were compared to intracranial EEG electrode implantation, with the spatial overlap of intracranial EEG electrode placement and cerebral magnetoencephalography abnormalities recorded. Finally, we assessed if the implantation of electrodes in abnormal tissue and subsequent resection of the strongest abnormalities determined by magnetoencephalography and intracranial EEG corresponded to surgical success. We used the area under the receiver operating characteristic curve as a measure of effect size. Intracranial electrodes were implanted in brain tissue with the most abnormal magnetoencephalography findings—in individuals that were seizure-free postoperatively (T = 3.9, P = 0.001) but not in those who did not become seizure-free. The overlap between magnetoencephalography abnormalities and electrode placement distinguished surgical outcome groups moderately well (area under the receiver operating characteristic curve = 0.68). In isolation, the resection of the strongest abnormalities as defined by magnetoencephalography and intracranial EEG separated surgical outcome groups well, area under the receiver operating characteristic curve = 0.71 and area under the receiver operating characteristic curve = 0.74, respectively. A model incorporating all three features separated surgical outcome groups best (area under the receiver operating characteristic curve = 0.80). Intracranial EEG is a key tool to delineate the epileptogenic zone and help render individuals seizure-free postoperatively. We showed that data-driven abnormality maps derived from resting-state magnetoencephalography recordings demonstrate clinical value and may help guide electrode placement in individuals with neocortical epilepsy. Additionally, our predictive model of postoperative seizure freedom, which leverages both magnetoencephalography and intracranial EEG recordings, could aid patient counselling of expected outcome.
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spelling pubmed-106365642023-11-11 Interictal magnetoencephalography abnormalities to guide intracranial electrode implantation and predict surgical outcome Owen, Thomas W Janiukstyte, Vytene Hall, Gerard R Chowdhury, Fahmida A Diehl, Beate McEvoy, Andrew Miserocchi, Anna de Tisi, Jane Duncan, John S Rugg-Gunn, Fergus Wang, Yujiang Taylor, Peter N Brain Commun Original Article Intracranial EEG is the gold standard technique for epileptogenic zone localization but requires a preconceived hypothesis of the location of the epileptogenic tissue. This placement is guided by qualitative interpretations of seizure semiology, MRI, EEG and other imaging modalities, such as magnetoencephalography. Quantitative abnormality mapping using magnetoencephalography has recently been shown to have potential clinical value. We hypothesized that if quantifiable magnetoencephalography abnormalities were sampled by intracranial EEG, then patients’ post-resection seizure outcome may be better. Thirty-two individuals with refractory neocortical epilepsy underwent magnetoencephalography and subsequent intracranial EEG recordings as part of presurgical evaluation. Eyes-closed resting-state interictal magnetoencephalography band power abnormality maps were derived from 70 healthy controls as a normative baseline. Magnetoencephalography abnormality maps were compared to intracranial EEG electrode implantation, with the spatial overlap of intracranial EEG electrode placement and cerebral magnetoencephalography abnormalities recorded. Finally, we assessed if the implantation of electrodes in abnormal tissue and subsequent resection of the strongest abnormalities determined by magnetoencephalography and intracranial EEG corresponded to surgical success. We used the area under the receiver operating characteristic curve as a measure of effect size. Intracranial electrodes were implanted in brain tissue with the most abnormal magnetoencephalography findings—in individuals that were seizure-free postoperatively (T = 3.9, P = 0.001) but not in those who did not become seizure-free. The overlap between magnetoencephalography abnormalities and electrode placement distinguished surgical outcome groups moderately well (area under the receiver operating characteristic curve = 0.68). In isolation, the resection of the strongest abnormalities as defined by magnetoencephalography and intracranial EEG separated surgical outcome groups well, area under the receiver operating characteristic curve = 0.71 and area under the receiver operating characteristic curve = 0.74, respectively. A model incorporating all three features separated surgical outcome groups best (area under the receiver operating characteristic curve = 0.80). Intracranial EEG is a key tool to delineate the epileptogenic zone and help render individuals seizure-free postoperatively. We showed that data-driven abnormality maps derived from resting-state magnetoencephalography recordings demonstrate clinical value and may help guide electrode placement in individuals with neocortical epilepsy. Additionally, our predictive model of postoperative seizure freedom, which leverages both magnetoencephalography and intracranial EEG recordings, could aid patient counselling of expected outcome. Oxford University Press 2023-10-25 /pmc/articles/PMC10636564/ /pubmed/37953844 http://dx.doi.org/10.1093/braincomms/fcad292 Text en © The Author(s) 2023. Published by Oxford University Press on behalf of the Guarantors of Brain. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Article
Owen, Thomas W
Janiukstyte, Vytene
Hall, Gerard R
Chowdhury, Fahmida A
Diehl, Beate
McEvoy, Andrew
Miserocchi, Anna
de Tisi, Jane
Duncan, John S
Rugg-Gunn, Fergus
Wang, Yujiang
Taylor, Peter N
Interictal magnetoencephalography abnormalities to guide intracranial electrode implantation and predict surgical outcome
title Interictal magnetoencephalography abnormalities to guide intracranial electrode implantation and predict surgical outcome
title_full Interictal magnetoencephalography abnormalities to guide intracranial electrode implantation and predict surgical outcome
title_fullStr Interictal magnetoencephalography abnormalities to guide intracranial electrode implantation and predict surgical outcome
title_full_unstemmed Interictal magnetoencephalography abnormalities to guide intracranial electrode implantation and predict surgical outcome
title_short Interictal magnetoencephalography abnormalities to guide intracranial electrode implantation and predict surgical outcome
title_sort interictal magnetoencephalography abnormalities to guide intracranial electrode implantation and predict surgical outcome
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10636564/
https://www.ncbi.nlm.nih.gov/pubmed/37953844
http://dx.doi.org/10.1093/braincomms/fcad292
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