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

Author:

Owen Thomas W1,Janiukstyte Vytene1,Hall Gerard R1,Chowdhury Fahmida A23,Diehl Beate23,McEvoy Andrew23,Miserocchi Anna23,de Tisi Jane234,Duncan John S234ORCID,Rugg-Gunn Fergus23,Wang Yujiang1235,Taylor Peter N1235ORCID

Affiliation:

1. CNNP Lab, Interdisciplinary Computing and Complex BioSystems Group, School of Computing, Newcastle University , Newcastle upon Tyne NE4 5TG , UK

2. UCL Queen Square Institute of Neurology , London WC1N 3BG , UK

3. National Hospital for Neurology & Neurosurgery , London WC1N 3BG , UK

4. NIHR University College London Hospitals Biomedical Research Centre, UCL Queen Square Institute of Neurology , London WC1N 3BG , UK

5. Faculty of Medical Sciences, Newcastle University , Newcastle upon Tyne NE1 7RU , UK

Abstract

Abstract 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.

Funder

Medical Research Council

Centre for Doctoral Training in Cloud Computing for Big Data

UK Research & Innovation

National Institutes of Health National Institute of Neurological Disorders and Stroke

Center for Sudden Unexpected Death in Epilepsy Research

Epilepsy Research UK

Wellcome

National Institute for Health Research University College London Hospitals Biomedical Research Centre

UCL Queen Square Institute of Neurology

Publisher

Oxford University Press (OUP)

Subject

Neurology,Cellular and Molecular Neuroscience,Biological Psychiatry,Psychiatry and Mental health

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