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March 24, 2023Research Article

Intracerebral Correlates of Scalp EEG Ictal Discharges Based on Simultaneous Stereo-EEG Recordings

View ORCID ProfileMickaël Ferrand, Cédric Baumann, Olivier Aron, Jean-Pierre Vignal, Jacques Jonas, Louise Tyvaert, Sophie Colnat-Coulbois, Laurent Koessler Doctor, Louis Maillard
First published March 24, 2023, DOI: https://doi.org/10.1212/WNL.0000000000207135
Mickaël Ferrand
1Departments of Neurology, and University Hospital of Nancy, Lorraine University, Nancy, France
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  • ORCID record for Mickaël Ferrand
Cédric Baumann
2Department of Epidemiology and Clinical Evaluation, INSERM CIC-EC CIE6, Lorraine University, Vandoeuvre, France
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Olivier Aron
1Departments of Neurology, and University Hospital of Nancy, Lorraine University, Nancy, France
3Neurosciences of Systems and Cognition Project, BioSiS Department (Department Biologie, Signaux et Systèmes en Cancérologie et Neurosciences), Research Center for Automatic Control of Nancy (CRAN), Lorraine University, CNRS, UMR 7039, Vandoeuvre, France
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Jean-Pierre Vignal
1Departments of Neurology, and University Hospital of Nancy, Lorraine University, Nancy, France
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Jacques Jonas
1Departments of Neurology, and University Hospital of Nancy, Lorraine University, Nancy, France
3Neurosciences of Systems and Cognition Project, BioSiS Department (Department Biologie, Signaux et Systèmes en Cancérologie et Neurosciences), Research Center for Automatic Control of Nancy (CRAN), Lorraine University, CNRS, UMR 7039, Vandoeuvre, France
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Louise Tyvaert
1Departments of Neurology, and University Hospital of Nancy, Lorraine University, Nancy, France
3Neurosciences of Systems and Cognition Project, BioSiS Department (Department Biologie, Signaux et Systèmes en Cancérologie et Neurosciences), Research Center for Automatic Control of Nancy (CRAN), Lorraine University, CNRS, UMR 7039, Vandoeuvre, France
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Sophie Colnat-Coulbois
4Department of Neurosurgery, University Hospital of Nancy, Lorraine University, Nancy, France
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Laurent Koessler Doctor
3Neurosciences of Systems and Cognition Project, BioSiS Department (Department Biologie, Signaux et Systèmes en Cancérologie et Neurosciences), Research Center for Automatic Control of Nancy (CRAN), Lorraine University, CNRS, UMR 7039, Vandoeuvre, France
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Louis Maillard
1Departments of Neurology, and University Hospital of Nancy, Lorraine University, Nancy, France
3Neurosciences of Systems and Cognition Project, BioSiS Department (Department Biologie, Signaux et Systèmes en Cancérologie et Neurosciences), Research Center for Automatic Control of Nancy (CRAN), Lorraine University, CNRS, UMR 7039, Vandoeuvre, France
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  • For correspondence: l.maillard@chru-nancy.fr
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Intracerebral Correlates of Scalp EEG Ictal Discharges Based on Simultaneous Stereo-EEG Recordings
Mickaël Ferrand, Cédric Baumann, Olivier Aron, Jean-Pierre Vignal, Jacques Jonas, Louise Tyvaert, Sophie Colnat-Coulbois, Laurent Koessler Doctor, Louis Maillard
Neurology Mar 2023, 10.1212/WNL.0000000000207135; DOI: 10.1212/WNL.0000000000207135

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Abstract

Background and Objectives: It remains unknown to what extent ictal scalp EEG can accurately predict the localization of the intra-cerebral seizure onset in pre-surgical evaluation of drug resistant epilepsies. In this study, we aimed to define homogeneous ictal scalp EEG profiles (based on their first ictal abnormality) and assess their localizing value using simultaneously recorded scalp EEG and Stereo-EEG.

Methods: We retrospectively included consecutive patients with drug-resistant focal epilepsy who had simultaneous stereo-EEG and scalp EEG recordings of at least one seizure, in the epileptology unit in Nancy, France. We analyzed one seizure per patient and used hierarchical cluster analysis to group similar seizure profiles on scalp EEG and then performed a descriptive analysis of their intra-cerebral correlates.

Results: We enrolled 129 patients in this study. The hierarchical cluster analysis showed six profiles on scalp EEG first modification. None was specific to a single intra-cerebral localization. The “normal EEG” and “blurred EEG” clusters (early muscle artifacts) comprised only five patients each and corresponded to no preferential intra-cerebral localization. The “temporal discharge” cluster (n=46) was characterized by theta or delta discharges on ipsilateral anterior temporal scalp electrodes and corresponded to a preferential mesial temporal intra-cerebral localization. The “posterior discharge” cluster (n=42) was characterized by posterior ipsilateral or contralateral rhythmic alpha discharges or slow waves on scalp and corresponded to a preferential temporal localization. However, this profile was the statistically most frequent scalp EEG correlate of occipital and parietal seizures. The “diffuse suppression” cluster (n=9) was characterized by a bilateral and diffuse background activity suppression on scalp and corresponded to mesial, and particularly insulo-opercular, localization. Finally, the “frontal discharge” cluster (n=22) was characterized by bilateral frontal rhythmic fast activity or pre-ictal spike on scalp and corresponded to preferential ventrodorsal frontal intra-cerebral localizations.

Discussion: Hierarchical cluster analysis identified six seizure profiles regarding the first abnormality on scalp EEG. None of them was specific of a single intra-cerebral localization. Nevertheless, the strong relationships between the “temporal”, “frontal”, “diffuse suppression” and “posterior” profiles and intra-cerebral discharges localizations may contribute to hierarchize hypotheses derived from ictal scalp EEG analysis regarding intra-cerebral seizure onset.

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  • Received August 22, 2022.
  • Accepted in final form January 18, 2023.
  • © 2023 American Academy of Neurology

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