Quantitative analysis of visually reviewed normal scalp EEG predicts seizure freedom following anterior temporal lobectomy.


Journal

Epilepsia
ISSN: 1528-1167
Titre abrégé: Epilepsia
Pays: United States
ID NLM: 2983306R

Informations de publication

Date de publication:
07 2022
Historique:
revised: 10 04 2022
received: 17 08 2021
accepted: 11 04 2022
pubmed: 14 4 2022
medline: 15 7 2022
entrez: 13 4 2022
Statut: ppublish

Résumé

Anterior temporal lobectomy (ATL) is a widely performed and successful intervention for drug-resistant temporal lobe epilepsy (TLE). However, up to one third of patients experience seizure recurrence within 1 year after ATL. Despite the extensive literature on presurgical electroencephalography (EEG) and magnetic resonance imaging (MRI) abnormalities to prognosticate seizure freedom following ATL, the value of quantitative analysis of visually reviewed normal interictal EEG in such prognostication remains unclear. In this retrospective multicenter study, we investigate whether machine learning analysis of normal interictal scalp EEG studies can inform the prediction of postoperative seizure freedom outcomes in patients who have undergone ATL. We analyzed normal presurgical scalp EEG recordings from 41 Mayo Clinic (MC) and 23 Cleveland Clinic (CC) patients. We used an unbiased automated algorithm to extract eyes closed awake epochs from scalp EEG studies that were free of any epileptiform activity and then extracted spectral EEG features representing (a) spectral power and (b) interhemispheric spectral coherence in frequencies between 1 and 25 Hz across several brain regions. We analyzed the differences between the seizure-free and non-seizure-free patients and employed a Naïve Bayes classifier using multiple spectral features to predict surgery outcomes. We trained the classifier using a leave-one-patient-out cross-validation scheme within the MC data set and then tested using the out-of-sample CC data set. Finally, we compared the predictive performance of normal scalp EEG-derived features against MRI abnormalities. We found that several spectral power and coherence features showed significant differences correlated with surgical outcomes and that they were most pronounced in the 10-25 Hz range. The Naïve Bayes classification based on those features predicted 1-year seizure freedom following ATL with area under the curve (AUC) values of 0.78 and 0.76 for the MC and CC data sets, respectively. Subsequent analyses revealed that (a) interhemispheric spectral coherence features in the 10-25 Hz range provided better predictability than other combinations and (b) normal scalp EEG-derived features provided superior and potentially distinct predictive value when compared with MRI abnormalities (>10% higher F1 score). These results support that quantitative analysis of even a normal presurgical scalp EEG may help prognosticate seizure freedom following ATL in patients with drug-resistant TLE. Although the mechanism for this result is not known, the scalp EEG spectral and coherence properties predicting seizure freedom may represent activity arising from the neocortex or the networks responsible for temporal lobe seizure generation within vs outside the margins of an ATL.

Identifiants

pubmed: 35416285
doi: 10.1111/epi.17257
pmc: PMC9283304
mid: NIHMS1821814
doi:

Types de publication

Journal Article Multicenter Study Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

1630-1642

Subventions

Organisme : NINDS NIH HHS
ID : R01 NS092882
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS097719
Pays : United States

Informations de copyright

© 2022 The Authors. Epilepsia published by Wiley Periodicals LLC on behalf of International League Against Epilepsy.

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Auteurs

Yogatheesan Varatharajah (Y)

Department of Bioengineering, University of Illinois at Urbana Champaign, Urbana, Illinois, USA.
Departments of Neurology and Physiology & Biomedical Engineering, Mayo Clinic, Rochester, Minnesota, USA.

Boney Joseph (B)

Departments of Neurology and Physiology & Biomedical Engineering, Mayo Clinic, Rochester, Minnesota, USA.

Benjamin Brinkmann (B)

Departments of Neurology and Physiology & Biomedical Engineering, Mayo Clinic, Rochester, Minnesota, USA.

Marcia Morita-Sherman (M)

Epilepsy Center, Cleveland Clinic, Cleveland, Ohio, USA.

Zachary Fitzgerald (Z)

Epilepsy Center, Cleveland Clinic, Cleveland, Ohio, USA.

Deborah Vegh (D)

Epilepsy Center, Cleveland Clinic, Cleveland, Ohio, USA.

Dileep Nair (D)

Epilepsy Center, Cleveland Clinic, Cleveland, Ohio, USA.

Richard Burgess (R)

Epilepsy Center, Cleveland Clinic, Cleveland, Ohio, USA.

Fernando Cendes (F)

Department of Neurology, University of Campinas UNICAMP, Campinas, Brazil.

Lara Jehi (L)

Epilepsy Center, Cleveland Clinic, Cleveland, Ohio, USA.

Gregory Worrell (G)

Departments of Neurology and Physiology & Biomedical Engineering, Mayo Clinic, Rochester, Minnesota, USA.

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