Automated Analysis of Risk Factors for Postictal Generalized EEG Suppression

Rationale: Currently, there is some ambiguity over the role of postictal generalized electro-encephalographic suppression (PGES) as a biomarker in sudden unexpected death in epilepsy (SUDEP). Visual analysis of PGES, known to be subjective, may account for this. In this study, we set out to perform...

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Main Authors: Xiuhe Zhao, Laura Vilella, Liang Zhu, M. R. Sandhya Rani, Johnson P. Hampson, Jaison Hampson, Norma J. Hupp, Rup K. Sainju, Daniel Friedman, Maromi Nei, Catherine Scott, Luke Allen, Brian K. Gehlbach, Stephan Schuele, Ronald M. Harper, Beate Diehl, Lisa M. Bateman, Orrin Devinsky, George B. Richerson, Guo-Qiang Zhang, Samden D. Lhatoo, Nuria Lacuey
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-05-01
Series:Frontiers in Neurology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fneur.2021.669517/full
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record_format Article
collection DOAJ
language English
format Article
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author Xiuhe Zhao
Laura Vilella
Laura Vilella
Liang Zhu
M. R. Sandhya Rani
M. R. Sandhya Rani
Johnson P. Hampson
Johnson P. Hampson
Jaison Hampson
Jaison Hampson
Norma J. Hupp
Norma J. Hupp
Rup K. Sainju
Rup K. Sainju
Daniel Friedman
Daniel Friedman
Maromi Nei
Maromi Nei
Catherine Scott
Catherine Scott
Luke Allen
Luke Allen
Brian K. Gehlbach
Brian K. Gehlbach
Stephan Schuele
Stephan Schuele
Ronald M. Harper
Ronald M. Harper
Beate Diehl
Beate Diehl
Lisa M. Bateman
Lisa M. Bateman
Orrin Devinsky
Orrin Devinsky
George B. Richerson
George B. Richerson
Guo-Qiang Zhang
Guo-Qiang Zhang
Samden D. Lhatoo
Samden D. Lhatoo
Nuria Lacuey
Nuria Lacuey
spellingShingle Xiuhe Zhao
Laura Vilella
Laura Vilella
Liang Zhu
M. R. Sandhya Rani
M. R. Sandhya Rani
Johnson P. Hampson
Johnson P. Hampson
Jaison Hampson
Jaison Hampson
Norma J. Hupp
Norma J. Hupp
Rup K. Sainju
Rup K. Sainju
Daniel Friedman
Daniel Friedman
Maromi Nei
Maromi Nei
Catherine Scott
Catherine Scott
Luke Allen
Luke Allen
Brian K. Gehlbach
Brian K. Gehlbach
Stephan Schuele
Stephan Schuele
Ronald M. Harper
Ronald M. Harper
Beate Diehl
Beate Diehl
Lisa M. Bateman
Lisa M. Bateman
Orrin Devinsky
Orrin Devinsky
George B. Richerson
George B. Richerson
Guo-Qiang Zhang
Guo-Qiang Zhang
Samden D. Lhatoo
Samden D. Lhatoo
Nuria Lacuey
Nuria Lacuey
Automated Analysis of Risk Factors for Postictal Generalized EEG Suppression
Frontiers in Neurology
PGES
generalized convulsive seizure
epilepsy
SUDEP
mortality
post-ictal generalized EEG suppression
author_facet Xiuhe Zhao
Laura Vilella
Laura Vilella
Liang Zhu
M. R. Sandhya Rani
M. R. Sandhya Rani
Johnson P. Hampson
Johnson P. Hampson
Jaison Hampson
Jaison Hampson
Norma J. Hupp
Norma J. Hupp
Rup K. Sainju
Rup K. Sainju
Daniel Friedman
Daniel Friedman
Maromi Nei
Maromi Nei
Catherine Scott
Catherine Scott
Luke Allen
Luke Allen
Brian K. Gehlbach
Brian K. Gehlbach
Stephan Schuele
Stephan Schuele
Ronald M. Harper
Ronald M. Harper
Beate Diehl
Beate Diehl
Lisa M. Bateman
Lisa M. Bateman
Orrin Devinsky
Orrin Devinsky
George B. Richerson
George B. Richerson
Guo-Qiang Zhang
Guo-Qiang Zhang
Samden D. Lhatoo
Samden D. Lhatoo
Nuria Lacuey
Nuria Lacuey
author_sort Xiuhe Zhao
title Automated Analysis of Risk Factors for Postictal Generalized EEG Suppression
title_short Automated Analysis of Risk Factors for Postictal Generalized EEG Suppression
title_full Automated Analysis of Risk Factors for Postictal Generalized EEG Suppression
title_fullStr Automated Analysis of Risk Factors for Postictal Generalized EEG Suppression
title_full_unstemmed Automated Analysis of Risk Factors for Postictal Generalized EEG Suppression
title_sort automated analysis of risk factors for postictal generalized eeg suppression
publisher Frontiers Media S.A.
series Frontiers in Neurology
issn 1664-2295
publishDate 2021-05-01
description Rationale: Currently, there is some ambiguity over the role of postictal generalized electro-encephalographic suppression (PGES) as a biomarker in sudden unexpected death in epilepsy (SUDEP). Visual analysis of PGES, known to be subjective, may account for this. In this study, we set out to perform an analysis of PGES presence and duration using a validated signal processing tool, specifically to examine the association between PGES and seizure features previously reported to be associated with visually analyzed PGES.Methods: This is a prospective, multicenter epilepsy monitoring study of autonomic and breathing biomarkers of SUDEP in adult patients with intractable epilepsy. We studied videoelectroencephalogram (vEEG) recordings of generalized convulsive seizures (GCS) in a cohort of patients in whom respiratory and vEEG recording were carried out during the evaluation in the epilepsy monitoring unit. A validated automated EEG suppression detection tool was used to determine presence and duration of PGES.Results: We studied 148 GCS in 87 patients. PGES occurred in 106/148 (71.6%) seizures in 70/87 (80.5%) of patients. PGES mean duration was 38.7 ± 23.7 (37; 1–169) seconds. Presence of tonic phase during GCS, including decerebration, decortication and hemi-decerebration, were 8.29 (CI 2.6–26.39, p = 0.0003), 7.17 (CI 1.29–39.76, p = 0.02), and 4.77 (CI 1.25–18.20, p = 0.02) times more likely to have PGES, respectively. In addition, presence of decerebration (p = 0.004) and decortication (p = 0.02), older age (p = 0.009), and hypoxemia duration (p = 0.03) were associated with longer PGES durations.Conclusions: In this study, we confirmed observations made with visual analysis, that presence of tonic phase during GCS, longer hypoxemia, and older age are reliably associated with PGES. We found that of the different types of tonic phase posturing, decerebration has the strongest association with PGES, followed by decortication, followed by hemi-decerebration. This suggests that these factors are likely indicative of seizure severity and may or may not be associated with SUDEP. An automated signal processing tool enables objective metrics, and may resolve apparent ambiguities in the role of PGES in SUDEP and seizure severity studies.
topic PGES
generalized convulsive seizure
epilepsy
SUDEP
mortality
post-ictal generalized EEG suppression
url https://www.frontiersin.org/articles/10.3389/fneur.2021.669517/full
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spelling doaj-7789d456bc2f421d8da015094c9429de2021-05-11T04:58:49ZengFrontiers Media S.A.Frontiers in Neurology1664-22952021-05-011210.3389/fneur.2021.669517669517Automated Analysis of Risk Factors for Postictal Generalized EEG SuppressionXiuhe Zhao0Laura Vilella1Laura Vilella2Liang Zhu3M. R. Sandhya Rani4M. R. Sandhya Rani5Johnson P. Hampson6Johnson P. Hampson7Jaison Hampson8Jaison Hampson9Norma J. Hupp10Norma J. Hupp11Rup K. Sainju12Rup K. Sainju13Daniel Friedman14Daniel Friedman15Maromi Nei16Maromi Nei17Catherine Scott18Catherine Scott19Luke Allen20Luke Allen21Brian K. Gehlbach22Brian K. Gehlbach23Stephan Schuele24Stephan Schuele25Ronald M. Harper26Ronald M. Harper27Beate Diehl28Beate Diehl29Lisa M. Bateman30Lisa M. Bateman31Orrin Devinsky32Orrin Devinsky33George B. Richerson34George B. Richerson35Guo-Qiang Zhang36Guo-Qiang Zhang37Samden D. Lhatoo38Samden D. Lhatoo39Nuria Lacuey40Nuria Lacuey41Department of Neurology, Qilu Hospital of Shandong University, Jinan, ChinaNational Institute of Neurological Disorders and Stroke (NINDS) Center for Sudden Unexpected Death in Epilepsy (SUDEP) Research, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United StatesDepartment of Neurology, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United StatesBiostatistics and Epidemiology Research Design Core, Division of Clinical and Translational Sciences, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United StatesNational Institute of Neurological Disorders and Stroke (NINDS) Center for Sudden Unexpected Death in Epilepsy (SUDEP) Research, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United StatesDepartment of Neurology, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United StatesNational Institute of Neurological Disorders and Stroke (NINDS) Center for Sudden Unexpected Death in Epilepsy (SUDEP) Research, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United StatesDepartment of Neurology, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United StatesNational Institute of Neurological Disorders and Stroke (NINDS) Center for Sudden Unexpected Death in Epilepsy (SUDEP) Research, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United StatesDepartment of Neurology, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United StatesNational Institute of Neurological Disorders and Stroke (NINDS) Center for Sudden Unexpected Death in Epilepsy (SUDEP) Research, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United StatesDepartment of Neurology, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United StatesNational Institute of Neurological Disorders and Stroke (NINDS) Center for Sudden Unexpected Death in Epilepsy (SUDEP) Research, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United StatesDepartment of Neurology, University of Iowa Carver College of Medicine, Iowa City, IA, United StatesNational Institute of Neurological Disorders and Stroke (NINDS) Center for Sudden Unexpected Death in Epilepsy (SUDEP) Research, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United StatesNew York University (NYU) Grossman School of Medicine, New York, NY, United StatesNational Institute of Neurological Disorders and Stroke (NINDS) Center for Sudden Unexpected Death in Epilepsy (SUDEP) Research, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United StatesSidney Kimmel Medical College, Thomas Jefferson University, Philadelphia, PA, United StatesNational Institute of Neurological Disorders and Stroke (NINDS) Center for Sudden Unexpected Death in Epilepsy (SUDEP) Research, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United StatesDepartment of Neurology, Institute of Neurology, University College London, London, United KingdomNational Institute of Neurological Disorders and Stroke (NINDS) Center for Sudden Unexpected Death in Epilepsy (SUDEP) Research, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United StatesDepartment of Neurology, Institute of Neurology, University College London, London, United KingdomNational Institute of Neurological Disorders and Stroke (NINDS) Center for Sudden Unexpected Death in Epilepsy (SUDEP) Research, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United StatesDepartment of Neurology, University of Iowa Carver College of Medicine, Iowa City, IA, United StatesNational Institute of Neurological Disorders and Stroke (NINDS) Center for Sudden Unexpected Death in Epilepsy (SUDEP) Research, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United StatesFeinberg School of Medicine, Northwestern University, Chicago, IL, United StatesNational Institute of Neurological Disorders and Stroke (NINDS) Center for Sudden Unexpected Death in Epilepsy (SUDEP) Research, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United States0Department of Neurobiology and the Brain Research Institute, University of California, Los Angeles, Los Angeles, CA, United StatesNational Institute of Neurological Disorders and Stroke (NINDS) Center for Sudden Unexpected Death in Epilepsy (SUDEP) Research, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United StatesDepartment of Neurology, Institute of Neurology, University College London, London, United KingdomNational Institute of Neurological Disorders and Stroke (NINDS) Center for Sudden Unexpected Death in Epilepsy (SUDEP) Research, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United States1Department of Neurology, Cedars-Sinai Medical Center, Los Angeles, CA, United StatesNational Institute of Neurological Disorders and Stroke (NINDS) Center for Sudden Unexpected Death in Epilepsy (SUDEP) Research, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United StatesNew York University (NYU) Grossman School of Medicine, New York, NY, United StatesNational Institute of Neurological Disorders and Stroke (NINDS) Center for Sudden Unexpected Death in Epilepsy (SUDEP) Research, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United StatesDepartment of Neurology, University of Iowa Carver College of Medicine, Iowa City, IA, United StatesNational Institute of Neurological Disorders and Stroke (NINDS) Center for Sudden Unexpected Death in Epilepsy (SUDEP) Research, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United StatesDepartment of Neurology, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United StatesNational Institute of Neurological Disorders and Stroke (NINDS) Center for Sudden Unexpected Death in Epilepsy (SUDEP) Research, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United StatesDepartment of Neurology, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United StatesNational Institute of Neurological Disorders and Stroke (NINDS) Center for Sudden Unexpected Death in Epilepsy (SUDEP) Research, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United StatesDepartment of Neurology, McGovern Medical School, University of Texas Health Science Center at Houston, Houston, TX, United StatesRationale: Currently, there is some ambiguity over the role of postictal generalized electro-encephalographic suppression (PGES) as a biomarker in sudden unexpected death in epilepsy (SUDEP). Visual analysis of PGES, known to be subjective, may account for this. In this study, we set out to perform an analysis of PGES presence and duration using a validated signal processing tool, specifically to examine the association between PGES and seizure features previously reported to be associated with visually analyzed PGES.Methods: This is a prospective, multicenter epilepsy monitoring study of autonomic and breathing biomarkers of SUDEP in adult patients with intractable epilepsy. We studied videoelectroencephalogram (vEEG) recordings of generalized convulsive seizures (GCS) in a cohort of patients in whom respiratory and vEEG recording were carried out during the evaluation in the epilepsy monitoring unit. A validated automated EEG suppression detection tool was used to determine presence and duration of PGES.Results: We studied 148 GCS in 87 patients. PGES occurred in 106/148 (71.6%) seizures in 70/87 (80.5%) of patients. PGES mean duration was 38.7 ± 23.7 (37; 1–169) seconds. Presence of tonic phase during GCS, including decerebration, decortication and hemi-decerebration, were 8.29 (CI 2.6–26.39, p = 0.0003), 7.17 (CI 1.29–39.76, p = 0.02), and 4.77 (CI 1.25–18.20, p = 0.02) times more likely to have PGES, respectively. In addition, presence of decerebration (p = 0.004) and decortication (p = 0.02), older age (p = 0.009), and hypoxemia duration (p = 0.03) were associated with longer PGES durations.Conclusions: In this study, we confirmed observations made with visual analysis, that presence of tonic phase during GCS, longer hypoxemia, and older age are reliably associated with PGES. We found that of the different types of tonic phase posturing, decerebration has the strongest association with PGES, followed by decortication, followed by hemi-decerebration. This suggests that these factors are likely indicative of seizure severity and may or may not be associated with SUDEP. An automated signal processing tool enables objective metrics, and may resolve apparent ambiguities in the role of PGES in SUDEP and seizure severity studies.https://www.frontiersin.org/articles/10.3389/fneur.2021.669517/fullPGESgeneralized convulsive seizureepilepsySUDEPmortalitypost-ictal generalized EEG suppression