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May 16, 2023; 100 (20) Research 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, Louis Maillard
First published March 24, 2023, DOI: https://doi.org/10.1212/WNL.0000000000207135
Mickaël Ferrand
From the Department of Neurology (M.F., O.A., J.-P.V., J.J., L.T., L.M.), and University Hospital of Nancy, Lorraine University; Department of Epidemiology and Clinical Evaluation (C.B.), INSERM CIC-EC CIE6, Lorraine University, Vandoeuvre; Neurosciences of Systems and Cognition Project (O.A., J.J., L.T., L.K., L.M.), 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; and Department of Neurosurgery (S.C.-C.), University Hospital of Nancy, Lorraine University, Nancy, France.
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  • ORCID record for Mickaël Ferrand
Cédric Baumann
From the Department of Neurology (M.F., O.A., J.-P.V., J.J., L.T., L.M.), and University Hospital of Nancy, Lorraine University; Department of Epidemiology and Clinical Evaluation (C.B.), INSERM CIC-EC CIE6, Lorraine University, Vandoeuvre; Neurosciences of Systems and Cognition Project (O.A., J.J., L.T., L.K., L.M.), 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; and Department of Neurosurgery (S.C.-C.), University Hospital of Nancy, Lorraine University, Nancy, France.
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Olivier Aron
From the Department of Neurology (M.F., O.A., J.-P.V., J.J., L.T., L.M.), and University Hospital of Nancy, Lorraine University; Department of Epidemiology and Clinical Evaluation (C.B.), INSERM CIC-EC CIE6, Lorraine University, Vandoeuvre; Neurosciences of Systems and Cognition Project (O.A., J.J., L.T., L.K., L.M.), 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; and Department of Neurosurgery (S.C.-C.), University Hospital of Nancy, Lorraine University, Nancy, France.
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Jean-Pierre Vignal
From the Department of Neurology (M.F., O.A., J.-P.V., J.J., L.T., L.M.), and University Hospital of Nancy, Lorraine University; Department of Epidemiology and Clinical Evaluation (C.B.), INSERM CIC-EC CIE6, Lorraine University, Vandoeuvre; Neurosciences of Systems and Cognition Project (O.A., J.J., L.T., L.K., L.M.), 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; and Department of Neurosurgery (S.C.-C.), University Hospital of Nancy, Lorraine University, Nancy, France.
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Jacques Jonas
From the Department of Neurology (M.F., O.A., J.-P.V., J.J., L.T., L.M.), and University Hospital of Nancy, Lorraine University; Department of Epidemiology and Clinical Evaluation (C.B.), INSERM CIC-EC CIE6, Lorraine University, Vandoeuvre; Neurosciences of Systems and Cognition Project (O.A., J.J., L.T., L.K., L.M.), 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; and Department of Neurosurgery (S.C.-C.), University Hospital of Nancy, Lorraine University, Nancy, France.
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Louise Tyvaert
From the Department of Neurology (M.F., O.A., J.-P.V., J.J., L.T., L.M.), and University Hospital of Nancy, Lorraine University; Department of Epidemiology and Clinical Evaluation (C.B.), INSERM CIC-EC CIE6, Lorraine University, Vandoeuvre; Neurosciences of Systems and Cognition Project (O.A., J.J., L.T., L.K., L.M.), 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; and Department of Neurosurgery (S.C.-C.), University Hospital of Nancy, Lorraine University, Nancy, France.
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Sophie Colnat-Coulbois
From the Department of Neurology (M.F., O.A., J.-P.V., J.J., L.T., L.M.), and University Hospital of Nancy, Lorraine University; Department of Epidemiology and Clinical Evaluation (C.B.), INSERM CIC-EC CIE6, Lorraine University, Vandoeuvre; Neurosciences of Systems and Cognition Project (O.A., J.J., L.T., L.K., L.M.), 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; and Department of Neurosurgery (S.C.-C.), University Hospital of Nancy, Lorraine University, Nancy, France.
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Laurent Koessler
From the Department of Neurology (M.F., O.A., J.-P.V., J.J., L.T., L.M.), and University Hospital of Nancy, Lorraine University; Department of Epidemiology and Clinical Evaluation (C.B.), INSERM CIC-EC CIE6, Lorraine University, Vandoeuvre; Neurosciences of Systems and Cognition Project (O.A., J.J., L.T., L.K., L.M.), 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; and Department of Neurosurgery (S.C.-C.), University Hospital of Nancy, Lorraine University, Nancy, France.
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Louis Maillard
From the Department of Neurology (M.F., O.A., J.-P.V., J.J., L.T., L.M.), and University Hospital of Nancy, Lorraine University; Department of Epidemiology and Clinical Evaluation (C.B.), INSERM CIC-EC CIE6, Lorraine University, Vandoeuvre; Neurosciences of Systems and Cognition Project (O.A., J.J., L.T., L.K., L.M.), 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; and Department of Neurosurgery (S.C.-C.), University Hospital of Nancy, Lorraine University, Nancy, France.
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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, Louis Maillard
Neurology May 2023, 100 (20) e2045-e2059; 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 intracerebral seizure onset in presurgical 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 1 seizure in the epileptology unit in Nancy, France. We analyzed 1 seizure per patient and used hierarchical cluster analysis to group similar seizure profiles on scalp EEG and then performed a descriptive analysis of their intracerebral correlates.

Results We enrolled 129 patients in this study. The hierarchical cluster analysis showed 6 profiles on scalp EEG first modification. None were specific to a single intracerebral localization. The “normal EEG” and “blurred EEG” clusters (early muscle artifacts) comprised only 5 patients each and corresponded to no preferential intracerebral 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 intracerebral 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 preictal spike on scalp and corresponded to preferential ventrodorsal frontal intracerebral localizations.

Discussion The hierarchical cluster analysis identified 6 seizure profiles regarding the first abnormality on scalp EEG. None of them were specific of a single intracerebral localization. Nevertheless, the strong relationships between the “temporal,” “frontal,” “diffuse suppression,” and “posterior” profiles and intracerebral discharge localizations may contribute to hierarchize hypotheses derived from ictal scalp EEG analysis regarding intracerebral seizure onset.

Glossary

DNET=
dysembrioplastic neuroepithelial tumor;
EZ=
epileptogenic zone;
IQR=
interquartile range;
LVFA=
low-voltage fast activity;
M=
motor;
PF=
prefrontal;
PM=
premotor;
RFA=
rhythmic fast activity;
RSA=
rhythmic slow activity;
SEEG=
stereo-EEG

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Submitted and externally peer reviewed. The handling editor was Associate Editor Barbara Jobst, MD, PhD, FAAN.

  • Editorial, page 937

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