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March 06, 2023Research Article

Development of Expert-Level Classification of Seizures and Rhythmic and Periodic Patterns During EEG Interpretation

View ORCID ProfileJin Jing, Wendong Ge, View ORCID ProfileShenda Hong, Marta Bento Fernandes, Zhen Lin, Chaoqi Yang, Sungtae An, Aaron F. Struck, View ORCID ProfileAline Herlopian, Ioannis Karakis, View ORCID ProfileJonathan J. Halford, Marcus C. Ng, Emily L. Johnson, View ORCID ProfileBrian L. Appavu, View ORCID ProfileRani A. Sarkis, Gamaleldin Osman, Peter W. Kaplan, Monica B. Dhakar, View ORCID ProfileLakshman Arcot Jayagopal, Zubeda Sheikh, Olga Taraschenko, Sarah Schmitt, Hiba A. Haider, View ORCID ProfileJennifer A. Kim, Christa B. Swisher, Nicolas Gaspard, Mackenzie C. Cervenka, Andres A. Rodriguez Ruiz, View ORCID ProfileJong Woo Lee, Mohammad Tabaeizadeh, Emily J. Gilmore, Kristy Nordstrom, Ji Yeoun Yoo, View ORCID ProfileManisha G. Holmes, Susan T. Herman, Jennifer A. Williams, View ORCID ProfileJay Pathmanathan, View ORCID ProfileFábio A. Nascimento, Ziwei Fan, Samaneh Nasiri, Mouhsin M. Shafi, View ORCID ProfileSydney S. Cash, Daniel B. Hoch, Andrew J. Cole, View ORCID ProfileEric S. Rosenthal, Sahar F. Zafar, Jimeng Sun, View ORCID ProfileM. Brandon Westover
First published March 6, 2023, DOI: https://doi.org/10.1212/WNL.0000000000207127
Jin Jing
1Massachusetts General Hospital/Harvard Medical School Department of Neurology, MA
2Massachusetts General Hospital Clinical Data Animation Center (CDAC), MA
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  • ORCID record for Jin Jing
Wendong Ge
1Massachusetts General Hospital/Harvard Medical School Department of Neurology, MA
2Massachusetts General Hospital Clinical Data Animation Center (CDAC), MA
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Shenda Hong
3National Institute of Health Data Science, Peking University, Beijing, China
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Marta Bento Fernandes
1Massachusetts General Hospital/Harvard Medical School Department of Neurology, MA
2Massachusetts General Hospital Clinical Data Animation Center (CDAC), MA
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Zhen Lin
4University of Illinois at Urbana-Champaign, College of Computing, Champaign, IL
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Chaoqi Yang
4University of Illinois at Urbana-Champaign, College of Computing, Champaign, IL
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Sungtae An
5Georgia Institute of Technology, College of Computing, Atlanta, GA
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Aaron F. Struck
6University of Wisconsin-Madison Department of Neurology
7William S Middleton Memorial Veterans Hospital Madison, WI
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Aline Herlopian
8Yale University-Yale New Haven Hospital, CT
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Ioannis Karakis
9Emory University School of Medicine, GA
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Jonathan J. Halford
10Medical University of South Carolina, SC
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Marcus C. Ng
11University of Manitoba, Canada
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Emily L. Johnson
12Johns Hopkins School of Medicine, MD
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Brian L. Appavu
13University of Arizona College of Medicine Phoenix, AZ
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Rani A. Sarkis
14Brigham and Women's Hospital, MA
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Gamaleldin Osman
15Mayo Clinic-Rochester, MN
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Peter W. Kaplan
12Johns Hopkins School of Medicine, MD
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Monica B. Dhakar
16Warren Alpert School of Medicine of Brown University, Providence, RI
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Lakshman Arcot Jayagopal
17University of Nebraska Medical Center, Omaha, NE
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Zubeda Sheikh
18West Virginia University Hospitals, WV
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Olga Taraschenko
17University of Nebraska Medical Center, Omaha, NE
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Sarah Schmitt
10Medical University of South Carolina, SC
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Hiba A. Haider
19University of Chicago, Chicago, IL
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Jennifer A. Kim
8Yale University-Yale New Haven Hospital, CT
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Christa B. Swisher
20Atrium Health, NC
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Nicolas Gaspard
21Université Libre de Bruxelles - Hôpital Erasme, Belgium
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Mackenzie C. Cervenka
12Johns Hopkins School of Medicine, MD
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Andres A. Rodriguez Ruiz
9Emory University School of Medicine, GA
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Jong Woo Lee
14Brigham and Women's Hospital, MA
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Mohammad Tabaeizadeh
1Massachusetts General Hospital/Harvard Medical School Department of Neurology, MA
2Massachusetts General Hospital Clinical Data Animation Center (CDAC), MA
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Emily J. Gilmore
8Yale University-Yale New Haven Hospital, CT
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Kristy Nordstrom
1Massachusetts General Hospital/Harvard Medical School Department of Neurology, MA
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Ji Yeoun Yoo
22Icahn School of Medicine, Mount Sinai, NY
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Manisha G. Holmes
23New York University (NYU) Grossman School of Medicine, NY
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Susan T. Herman
24Barrow Neurological Institute, Phoenix, AZ
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Jennifer A. Williams
25Mater Misericordiae University Hospital, Dublin, Ireland
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Jay Pathmanathan
26University of Pennsylvania, PA
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Fábio A. Nascimento
1Massachusetts General Hospital/Harvard Medical School Department of Neurology, MA
2Massachusetts General Hospital Clinical Data Animation Center (CDAC), MA
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Ziwei Fan
1Massachusetts General Hospital/Harvard Medical School Department of Neurology, MA
2Massachusetts General Hospital Clinical Data Animation Center (CDAC), MA
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Samaneh Nasiri
1Massachusetts General Hospital/Harvard Medical School Department of Neurology, MA
2Massachusetts General Hospital Clinical Data Animation Center (CDAC), MA
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Mouhsin M. Shafi
27Beth Israel Deaconess Medical Center/Harvard Medical School, MA.
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Sydney S. Cash
1Massachusetts General Hospital/Harvard Medical School Department of Neurology, MA
2Massachusetts General Hospital Clinical Data Animation Center (CDAC), MA
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Daniel B. Hoch
1Massachusetts General Hospital/Harvard Medical School Department of Neurology, MA
2Massachusetts General Hospital Clinical Data Animation Center (CDAC), MA
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Andrew J. Cole
1Massachusetts General Hospital/Harvard Medical School Department of Neurology, MA
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Eric S. Rosenthal
1Massachusetts General Hospital/Harvard Medical School Department of Neurology, MA
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Sahar F. Zafar
1Massachusetts General Hospital/Harvard Medical School Department of Neurology, MA
2Massachusetts General Hospital Clinical Data Animation Center (CDAC), MA
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Jimeng Sun
4University of Illinois at Urbana-Champaign, College of Computing, Champaign, IL
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M. Brandon Westover
1Massachusetts General Hospital/Harvard Medical School Department of Neurology, MA
2Massachusetts General Hospital Clinical Data Animation Center (CDAC), MA
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  • For correspondence: mwestover@mgh.harvard.edu
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Citation
Development of Expert-Level Classification of Seizures and Rhythmic and Periodic Patterns During EEG Interpretation
Jin Jing, Wendong Ge, Shenda Hong, Marta Bento Fernandes, Zhen Lin, Chaoqi Yang, Sungtae An, Aaron F. Struck, Aline Herlopian, Ioannis Karakis, Jonathan J. Halford, Marcus C. Ng, Emily L. Johnson, Brian L. Appavu, Rani A. Sarkis, Gamaleldin Osman, Peter W. Kaplan, Monica B. Dhakar, Lakshman Arcot Jayagopal, Zubeda Sheikh, Olga Taraschenko, Sarah Schmitt, Hiba A. Haider, Jennifer A. Kim, Christa B. Swisher, Nicolas Gaspard, Mackenzie C. Cervenka, Andres A. Rodriguez Ruiz, Jong Woo Lee, Mohammad Tabaeizadeh, Emily J. Gilmore, Kristy Nordstrom, Ji Yeoun Yoo, Manisha G. Holmes, Susan T. Herman, Jennifer A. Williams, Jay Pathmanathan, Fábio A. Nascimento, Ziwei Fan, Samaneh Nasiri, Mouhsin M. Shafi, Sydney S. Cash, Daniel B. Hoch, Andrew J. Cole, Eric S. Rosenthal, Sahar F. Zafar, Jimeng Sun, M. Brandon Westover
Neurology Mar 2023, 10.1212/WNL.0000000000207127; DOI: 10.1212/WNL.0000000000207127

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Abstract

Background and Objectives: Seizures and other seizure-like patterns of brain activity can harm the brain and contribute to in-hospital death, particularly when prolonged. However, experts qualified to interpret electroencephalography (EEG) data are scarce. Prior attempts to automate this task have been limited by small or inadequately labeled samples and have not convincingly demonstrated generalizable expert-level performance. There exists a critical unmet need for an automated method to classify seizures and other seizure-like events with expert-level reliability. This study was conducted to develop and validate a computer algorithm that matches the reliability and accuracy of experts in identifying seizures and seizure-like events, known as “ictal-interictal-injury-continuum” (IIIC) patterns on EEG, including seizures (SZ), lateralized and generalized periodic discharges (LPD, GPD), and lateralized and generalized rhythmic delta activity (LRDA, GRDA), and in differentiating these patterns from non-IIIC patterns.

Methods: We used 6,095 scalp EEGs from 2,711 patients with and without IIIC events to train a deep neural network, SPaRCNet, to perform IIIC event classification. Independent training and test datasets were generated from 50,697 EEG segments, independently annotated by 20 fellowship-trained neurophysiologists. We assessed whether SPaRCNet performs at or above the sensitivity, specificity, precision, and calibration of fellowship-trained neurophysiologists for identifying IIIC events. Statistical performance was assessed via the calibration index, and by the percentage of experts whose operating points were below the model’s receiver operating characteristic curves (ROC) and precision recall curves (PRC) for the 6 pattern classes.

Results: SPaRCNet matches or exceeds most experts in classifying IIIC events based on both calibration and discrimination metrics. For SZ, LPD, GPD, LRDA, GRDA, and “Other” classes, SPaRCNet exceeds the following percentages of 20 experts – ROC: 45%, 20%, 50%, 75%, 55%, 40%; PRC: 50%, 35%, 50%, 90%, 70%, 45%; and calibration: 95%, 100%, 95%, 100%, 100%, 80%, respectively.

Discussion: SPaRCNet is the first algorithm to match expert performance in detecting seizures and other seizure-like events in a representative sample of EEGs. With further development, SPaRCNet may thus be a valuable tool for expedited review of EEGs.

  • Received May 13, 2022.
  • Accepted in final form January 12, 2023.
  • © 2023 American Academy of Neurology

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