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June 14, 2022; 98 (24) Research Article

Clinical Yield of Electromagnetic Source Imaging and Hemodynamic Responses in Epilepsy

Validation With Intracerebral Data

Chifaou Abdallah, Tanguy Hedrich, Andreas Koupparis, Jawata Afnan, Jeffrey Alan Hall, Jean Gotman, Francois Dubeau, Nicolas von Ellenrieder, Birgit Frauscher, Eliane Kobayashi, Christophe Grova
First published April 26, 2022, DOI: https://doi.org/10.1212/WNL.0000000000200337
Chifaou Abdallah
From the Multimodal Functional Imaging Lab (C.A., T.H., J.A., C.G.), Biomedical Engineering Department, Montreal Neurological Institute and Hospital (C.A., A.K., J.A., J.A.H., J.G., F.D., N.v.E., B.F., E.K., C.G.), Neurology and Neurosurgery Department, and Analytical Neurophysiology Lab (T.H., B.F.), McGill University; and Multimodal Functional Imaging Lab (C.G.), PERFORM Centre, Department of Physics, Concordia University, Montreal, Quebec, Canada.
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Tanguy Hedrich
From the Multimodal Functional Imaging Lab (C.A., T.H., J.A., C.G.), Biomedical Engineering Department, Montreal Neurological Institute and Hospital (C.A., A.K., J.A., J.A.H., J.G., F.D., N.v.E., B.F., E.K., C.G.), Neurology and Neurosurgery Department, and Analytical Neurophysiology Lab (T.H., B.F.), McGill University; and Multimodal Functional Imaging Lab (C.G.), PERFORM Centre, Department of Physics, Concordia University, Montreal, Quebec, Canada.
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Andreas Koupparis
From the Multimodal Functional Imaging Lab (C.A., T.H., J.A., C.G.), Biomedical Engineering Department, Montreal Neurological Institute and Hospital (C.A., A.K., J.A., J.A.H., J.G., F.D., N.v.E., B.F., E.K., C.G.), Neurology and Neurosurgery Department, and Analytical Neurophysiology Lab (T.H., B.F.), McGill University; and Multimodal Functional Imaging Lab (C.G.), PERFORM Centre, Department of Physics, Concordia University, Montreal, Quebec, Canada.
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Jawata Afnan
From the Multimodal Functional Imaging Lab (C.A., T.H., J.A., C.G.), Biomedical Engineering Department, Montreal Neurological Institute and Hospital (C.A., A.K., J.A., J.A.H., J.G., F.D., N.v.E., B.F., E.K., C.G.), Neurology and Neurosurgery Department, and Analytical Neurophysiology Lab (T.H., B.F.), McGill University; and Multimodal Functional Imaging Lab (C.G.), PERFORM Centre, Department of Physics, Concordia University, Montreal, Quebec, Canada.
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Jeffrey Alan Hall
From the Multimodal Functional Imaging Lab (C.A., T.H., J.A., C.G.), Biomedical Engineering Department, Montreal Neurological Institute and Hospital (C.A., A.K., J.A., J.A.H., J.G., F.D., N.v.E., B.F., E.K., C.G.), Neurology and Neurosurgery Department, and Analytical Neurophysiology Lab (T.H., B.F.), McGill University; and Multimodal Functional Imaging Lab (C.G.), PERFORM Centre, Department of Physics, Concordia University, Montreal, Quebec, Canada.
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Jean Gotman
From the Multimodal Functional Imaging Lab (C.A., T.H., J.A., C.G.), Biomedical Engineering Department, Montreal Neurological Institute and Hospital (C.A., A.K., J.A., J.A.H., J.G., F.D., N.v.E., B.F., E.K., C.G.), Neurology and Neurosurgery Department, and Analytical Neurophysiology Lab (T.H., B.F.), McGill University; and Multimodal Functional Imaging Lab (C.G.), PERFORM Centre, Department of Physics, Concordia University, Montreal, Quebec, Canada.
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Francois Dubeau
From the Multimodal Functional Imaging Lab (C.A., T.H., J.A., C.G.), Biomedical Engineering Department, Montreal Neurological Institute and Hospital (C.A., A.K., J.A., J.A.H., J.G., F.D., N.v.E., B.F., E.K., C.G.), Neurology and Neurosurgery Department, and Analytical Neurophysiology Lab (T.H., B.F.), McGill University; and Multimodal Functional Imaging Lab (C.G.), PERFORM Centre, Department of Physics, Concordia University, Montreal, Quebec, Canada.
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Nicolas von Ellenrieder
From the Multimodal Functional Imaging Lab (C.A., T.H., J.A., C.G.), Biomedical Engineering Department, Montreal Neurological Institute and Hospital (C.A., A.K., J.A., J.A.H., J.G., F.D., N.v.E., B.F., E.K., C.G.), Neurology and Neurosurgery Department, and Analytical Neurophysiology Lab (T.H., B.F.), McGill University; and Multimodal Functional Imaging Lab (C.G.), PERFORM Centre, Department of Physics, Concordia University, Montreal, Quebec, Canada.
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Birgit Frauscher
From the Multimodal Functional Imaging Lab (C.A., T.H., J.A., C.G.), Biomedical Engineering Department, Montreal Neurological Institute and Hospital (C.A., A.K., J.A., J.A.H., J.G., F.D., N.v.E., B.F., E.K., C.G.), Neurology and Neurosurgery Department, and Analytical Neurophysiology Lab (T.H., B.F.), McGill University; and Multimodal Functional Imaging Lab (C.G.), PERFORM Centre, Department of Physics, Concordia University, Montreal, Quebec, Canada.
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Eliane Kobayashi
From the Multimodal Functional Imaging Lab (C.A., T.H., J.A., C.G.), Biomedical Engineering Department, Montreal Neurological Institute and Hospital (C.A., A.K., J.A., J.A.H., J.G., F.D., N.v.E., B.F., E.K., C.G.), Neurology and Neurosurgery Department, and Analytical Neurophysiology Lab (T.H., B.F.), McGill University; and Multimodal Functional Imaging Lab (C.G.), PERFORM Centre, Department of Physics, Concordia University, Montreal, Quebec, Canada.
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Christophe Grova
From the Multimodal Functional Imaging Lab (C.A., T.H., J.A., C.G.), Biomedical Engineering Department, Montreal Neurological Institute and Hospital (C.A., A.K., J.A., J.A.H., J.G., F.D., N.v.E., B.F., E.K., C.G.), Neurology and Neurosurgery Department, and Analytical Neurophysiology Lab (T.H., B.F.), McGill University; and Multimodal Functional Imaging Lab (C.G.), PERFORM Centre, Department of Physics, Concordia University, Montreal, Quebec, Canada.
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Citation
Clinical Yield of Electromagnetic Source Imaging and Hemodynamic Responses in Epilepsy
Validation With Intracerebral Data
Chifaou Abdallah, Tanguy Hedrich, Andreas Koupparis, Jawata Afnan, Jeffrey Alan Hall, Jean Gotman, Francois Dubeau, Nicolas von Ellenrieder, Birgit Frauscher, Eliane Kobayashi, Christophe Grova
Neurology Jun 2022, 98 (24) e2499-e2511; DOI: 10.1212/WNL.0000000000200337

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Abstract

Background and Objectives Accurate delineation of the seizure-onset zone (SOZ) in focal drug-resistant epilepsy often requires stereo-EEG (SEEG) recordings. Our aims were to propose a truly objective and quantitative comparison between EEG/magnetoencephalography (MEG) source imaging (EMSI), EEG/fMRI responses for similar spikes with primary irritative zone (PIZ) and SOZ defined by SEEG and to evaluate the value of EMSI and EEG/fMRI to predict postsurgical outcome.

Methods We identified patients with drug-resistant epilepsy who underwent EEG/MEG, EEG/fMRI, and subsequent SEEG at the Epilepsy Service from the Montreal Neurological Institute and Hospital. We quantified multimodal concordance within the SEEG channel space as spatial overlap with PIZ/SOZ and distances to the spike-onset, spike maximum amplitude and seizure core intracerebral channels by applying a new methodology consisting of converting EMSI results into SEEG electrical potentials (EMSIe–SEEG) and projecting the most significant fMRI response on the SEEG channels (fMRIp–SEEG). Spatial overlaps with PIZ/SOZ (AUCPIZ, AUCSOZ) were assessed by using the area under the receiver operating characteristic curve (AUC). Here, AUC represents the probability that a randomly picked active contact exhibited higher amplitude when located inside the spatial reference than outside.

Results Seventeen patients were included. Mean spatial overlaps with the PIZ and SOZ were 0.71 and 0.65 for EMSIe–SEEG and 0.57 and 0.62 for fMRIp–SEEG. Good EMSIe–SEEG spatial overlap with the PIZ was associated with smaller distance from the maximum EMSIe–SEEG contact to the spike maximum amplitude channel (median distance 14 mm). Conversely, good fMRIp–SEEG spatial overlap with the SOZ was associated with smaller distances from the maximum fMRIp–SEEG contact to the spike-onset and seizure core channels (median distances 10 and 5 mm, respectively). Surgical outcomes were correctly predicted by EEG/MEG in 12 of 15 (80%) patients and EEG/fMRI in 6 of 11(54%) patients.

Discussion With the use of a unique quantitative approach estimating EMSI and fMRI results in the reference SEEG channel space, EEG/MEG and EEG/fMRI accurately localized the SOZ and the PIZ. Precisely, EEG/MEG more accurately localized the PIZ, whereas EEG/fMRI was more sensitive to the SOZ. Both neuroimaging techniques provide complementary localization that can help guide SEEG implantation and select good candidates for surgery.

Glossary

AUC=
area under the receiver operating characteristic curve;
BOLD=
blood oxygen level–dependent;
cMEM=
coherent maximum entropy on the mean;
EMSI=
EEG/MEG source imaging;
EZ=
epileptogenic zone;
MEG=
magnetoencephalography;
MSI=
magnetic source imaging;
PIZ=
primary irritative zone;
SEEG=
stereo-EEG;
SNR=
signal to noise ratio;
SOZ=
seizure-onset zone

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.

  • Received August 13, 2021.
  • Accepted in final form February 21, 2022.
  • © 2022 American Academy of Neurology
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