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December 02, 2022Research Article

Interrater Reliability of Expert Electroencephalographers Identifying Seizures and Rhythmic and Periodic Patterns in Electroencephalograms

View ORCID ProfileJin Jing, Wendong Ge, Aaron F. Struck, Marta Bento Fernandes, View ORCID ProfileShenda Hong, Sungtae An, Safoora Fatima, 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 December 2, 2022, DOI: https://doi.org/10.1212/WNL.0000000000201670
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
  • For correspondence: jjing@mgh.harvard.edu
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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  • For correspondence: wendong.ge@mgh.harvard.edu
Aaron F. Struck
3University of Wisconsin-Madison Department of Neurology
4William S Middleton Memorial Veterans Hospital Madison, WI
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  • For correspondence: struck@neurology.wisc.edu
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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  • For correspondence: mbentofernandes@mgh.harvard.edu
Shenda Hong
5National Institute of Health Data Science, Peking University, Beijing, China
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  • ORCID record for Shenda Hong
  • For correspondence: sdhong1503@gmail.com
Sungtae An
6Georgia Institute of Technology, College of Computing, Atlanta, GA
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  • For correspondence: sungtae.an@cc.gatech.edu
Safoora Fatima
3University of Wisconsin-Madison Department of Neurology
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  • For correspondence: sfatima2@wisc.edu
Aline Herlopian
7Yale University-Yale New Haven Hospital, CT
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  • ORCID record for Aline Herlopian
  • For correspondence: aline.herlopian@yale.edu
Ioannis Karakis
8Emory University School of Medicine, GA
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  • For correspondence: ioannis.karakis@emory.edu
Jonathan J. Halford
9Medical University of South Carolina, SC
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  • For correspondence: halfordj@musc.edu
Marcus C. Ng
10University of Manitoba, Canada
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  • For correspondence: marcus.ng@umanitoba.ca
Emily L. Johnson
11Johns Hopkins School of Medicine, MD
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  • For correspondence: ejohns92@jhmi.edu
Brian L. Appavu
12University of Arizona College of Medicine, AZ
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  • For correspondence: bappavu@phoenixchildrens.com
Rani A. Sarkis
13Brigham and Women's Hospital, MA
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  • For correspondence: rsarkis@bwh.harvard.edu
Gamaleldin Osman
14Mayo Clinic-Rochester, MN
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Peter W. Kaplan
11Johns Hopkins School of Medicine, MD
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  • For correspondence: pkaplan@jhmi.edu
Monica B. Dhakar
15Warren Alpert School of Medicine of Brown University, Providence, RI
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  • For correspondence: monica_dhakar@brown.edu
Lakshman Arcot Jayagopal
16University of Nebraska Medical Center, NE
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Zubeda Sheikh
17West Virginia University Hospitals, WV
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  • For correspondence: zubeda.karim@gmail.com
Olga Taraschenko
16University of Nebraska Medical Center, NE
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  • For correspondence: olha.taraschenko@unmc.edu
Sarah Schmitt
9Medical University of South Carolina, SC
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  • For correspondence: schmitts@musc.edu
Hiba A. Haider
18University of Chicago, Chicago, IL
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  • For correspondence: hibahaider@bsd.uchicago.edu
Jennifer A. Kim
7Yale University-Yale New Haven Hospital, CT
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Christa B. Swisher
19Atrium Health, NC
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Nicolas Gaspard
20Université Libre de Bruxelles - Hôpital Erasme, Belgium
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Mackenzie C. Cervenka
11Johns Hopkins School of Medicine, MD
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Andres A. Rodriguez Ruiz
8Emory University School of Medicine, GA
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Jong Woo Lee
13Brigham and Women's Hospital, MA
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  • For correspondence: jlee38@bwh.harvard.edu
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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  • For correspondence: mohammad.tabaeizadeh@gmail.com
Emily J. Gilmore
7Yale 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
21Icahn School of Medicine, Mount Sinai, NY
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Manisha G. Holmes
22New York University (NYU) Grossman School of Medicine, NY
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  • For correspondence: manisha.holmes@nyulangone.org
Susan T. Herman
23Barrow Neurological Institute, Phoenix, AZ
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Jennifer A. Williams
24Mater Misericordiae University Hospital, Dublin, Ireland.
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Jay Pathmanathan
25University of Pennsylvania, PA
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  • For correspondence: jay.pathmanathan@pennmedicine.upenn.edu
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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  • For correspondence: nascimento.fabio.a@gmail.com
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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  • For correspondence: zwwingfan@gmail.com
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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  • For correspondence: snasiri@mgh.harvard.edu
Mouhsin M. Shafi
26Beth Israel Deaconess Medical Center/Harvard Medical School, MA
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  • For correspondence: mshafi@bidmc.harvard.edu
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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  • For correspondence: scash@mgh.harvard.edu
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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  • For correspondence: dhoch@mgh.harvard.edu
Andrew J. Cole
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: cole.andrew@mgh.harvard.edu
Eric S. Rosenthal
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 Eric S. Rosenthal
  • For correspondence: erosenthal@mgh.harvard.edu
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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  • For correspondence: sfzafar@mgh.harvard.edu
Jimeng Sun
27University of Illinois at Urbana-Champaign, College of Computing, Champaign, IL
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  • For correspondence: jimeng@illinois.edu
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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  • ORCID record for M. Brandon Westover
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Citation
Interrater Reliability of Expert Electroencephalographers Identifying Seizures and Rhythmic and Periodic Patterns in Electroencephalograms
Jin Jing, Wendong Ge, Aaron F. Struck, Marta Bento Fernandes, Shenda Hong, Sungtae An, Safoora Fatima, 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 Dec 2022, 10.1212/WNL.0000000000201670; DOI: 10.1212/WNL.0000000000201670

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Abstract

Background and Objectives: The validity of brain monitoring using electroencephalography (EEG), particularly to guide care in patients with acute or critical illness, requires that experts can reliably identify seizures and other potentially harmful rhythmic and periodic brain activity, collectively referred to as “ictal-interictal-injury continuum" (IIIC). Prior inter-rater reliability (IRR) studies are limited by small samples and selection bias. This study was conducted to assess the reliability of experts in identifying IIIC.

Methods: This prospective analysis included 30 experts with subspecialty clinical neurophysiology training from 18 institutions. Experts independently scored varying numbers of ten-second EEG segments as: “Seizure (SZ)”, “Lateralized Periodic Discharges (LPD)”, “Generalized Periodic Discharges (GPD)”, “Lateralized Rhythmic Delta Activity (LRDA)”, “Generalized Rhythmic Delta Activity (GRDA)”, or “Other”. EEGs were performed for clinical indications at Massachusetts General Hospital between 2006 to 2020. Primary outcome measures were pairwise IRR (average percent agreement (PA) between pairs of experts) and majority IRR (average PA with group consensus) for each class; and beyond chance agreement (κ). Secondary outcomes were calibration of expert scoring to group consensus, and latent trait analysis to investigate contributions of bias and noise to scoring variability.

Results: Among 2,711 EEGs, 49% were from females, and median (IQR) age was 55 (41). In total experts scored 50,697 EEG segments; the median [range] number scored by each expert was 6,287.5 [1,002, 45,267]. Overall pairwise IRR was moderate (PA 52%, κ 42%), and majority IRR was substantial (PA 65%, κ 61%). Noise-bias analysis demonstrated that a single underlying receiver operating curve can account for most variation in experts' false positive vs true positive characteristics (median [range] of variance explained (R2): 95 [93, 98]%), and for most variation in experts’ precision vs sensitivity characteristics (R2: 75 [59, 89]%). Thus, variation between experts is mostly attributable not to differences in expertise, but rather to variation in decision thresholds.

Discussion: Our results provide precise estimates of expert reliability from a large and diverse sample, and a parsimonious theory to explain the origin of disagreements between experts. The results also establish a standard for how well an automated IIIC classifier must perform to match experts.

Classification of Evidence: This study provides Class II evidence that independent expert review reliably identifies ictal-interictal injury continuum patterns on EEG compared to expert consensus.

  • Received April 13, 2022.
  • Accepted in final form October 25, 2022.
  • © 2022 American Academy of Neurology

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