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January 19, 2021; 96 (3) Article

Association of Peri-ictal Brainstem Posturing With Seizure Severity and Breathing Compromise in Patients With Generalized Convulsive Seizures

View ORCID ProfileLaura Vilella, View ORCID ProfileNuria Lacuey, Johnson P. Hampson, Liang Zhu, Shirin Omidi, Manuela Ochoa-Urrea, Shiqiang Tao, M.R. Sandhya Rani, Rup K. Sainju, View ORCID ProfileDaniel Friedman, View ORCID ProfileMaromi Nei, Kingman Strohl, View ORCID ProfileCatherine Scott, View ORCID ProfileLuke Allen, View ORCID ProfileBrian K. Gehlbach, View ORCID ProfileNorma J. Hupp, Jaison S. Hampson, Nassim Shafiabadi, Xiuhe Zhao, Victoria Reick-Mitrisin, Stephan Schuele, Jennifer Ogren, Ronald M. Harper, View ORCID ProfileBeate Diehl, Lisa M. Bateman, Orrin Devinsky, George B. Richerson, Philippe Ryvlin, Guo-Qiang Zhang, Samden D. Lhatoo
First published December 2, 2020, DOI: https://doi.org/10.1212/WNL.0000000000011274
Laura Vilella
From the NINDS Center for SUDEP Research (L.V., N.L., S.O., M.O.-U., S.T., M.R.S.R., R.K.S., D.F., M.N., C.S., L.A., B.K.G., J.S.H., S.S., J.O., R.M.H., B.D., L.M.B., O.D., G.B.R., P.R., G.-Q.Z., S.D.L.) and Department of Neurology (L.V., N.L., J.P.H., S.O., M.O.-U., S.T., M.R.S.R., N.J.H., J.S.H., G.-Q.Z., S.D.L.), McGovern Medical School, and Biostatistics and Epidemiology Research Design Core (L.Z., G.B.R.), Division of Clinical and Translational Sciences, University of Texas Health Science Center at Houston; Departament de Medicina (L.V.), Universitat Autonoma de Barcelona, Spain; University of Iowa Carver College of Medicine (R.K.S., B.K.G.), Iowa City; NYU Langone School of Medicine (D.F., O.D.), New York; Sidney Kimmel Medical College (M.N.), Thomas Jefferson University, Philadelphia, PA; Division of Pulmonary (K.S.), Critical Care and Sleep Medicine, University Hospitals Medical Center, Cleveland, OH; Institute of Neurology (C.S., L.A., B.D.), University College London, UK; Case Western Reserve University (N.S., X.Z., V.R.-M.), Cleveland, OH; Feinberg School of Medicine (S.S.), Northwestern University, Chicago, IL; Department of Neurobiology and the Brain Research Institute (J.O., R.M.H.), University of California, Los Angeles; Department of Neurology (L.M.B.), Columbia University, New York, NY; and Department of Clinical Neuroscience (P.R.), Centre Hospitalier Universitaire Vaudois, Lausanne, Switzerland.
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Nuria Lacuey
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Johnson P. Hampson
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Liang Zhu
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Shirin Omidi
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Manuela Ochoa-Urrea
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Shiqiang Tao
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M.R. Sandhya Rani
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Rup K. Sainju
MBBS
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Daniel Friedman
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Maromi Nei
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Kingman Strohl
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Catherine Scott
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Luke Allen
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Brian K. Gehlbach
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Norma J. Hupp
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Jaison S. Hampson
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Nassim Shafiabadi
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Xiuhe Zhao
MD
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Victoria Reick-Mitrisin
MS
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Stephan Schuele
MD, MPH
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Jennifer Ogren
PhD
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Ronald M. Harper
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Beate Diehl
MD, PhD, FRCP
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Lisa M. Bateman
MD
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Orrin Devinsky
MD
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George B. Richerson
MD, PhD
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Philippe Ryvlin
MD, PhD
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Guo-Qiang Zhang
MS, PhD
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Samden D. Lhatoo
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Citation
Association of Peri-ictal Brainstem Posturing With Seizure Severity and Breathing Compromise in Patients With Generalized Convulsive Seizures
Laura Vilella, Nuria Lacuey, Johnson P. Hampson, Liang Zhu, Shirin Omidi, Manuela Ochoa-Urrea, Shiqiang Tao, M.R. Sandhya Rani, Rup K. Sainju, Daniel Friedman, Maromi Nei, Kingman Strohl, Catherine Scott, Luke Allen, Brian K. Gehlbach, Norma J. Hupp, Jaison S. Hampson, Nassim Shafiabadi, Xiuhe Zhao, Victoria Reick-Mitrisin, Stephan Schuele, Jennifer Ogren, Ronald M. Harper, Beate Diehl, Lisa M. Bateman, Orrin Devinsky, George B. Richerson, Philippe Ryvlin, Guo-Qiang Zhang, Samden D. Lhatoo
Neurology Jan 2021, 96 (3) e352-e365; DOI: 10.1212/WNL.0000000000011274

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Abstract

Objective To analyze the association between peri-ictal brainstem posturing semiologies with postictal generalized electroencephalographic suppression (PGES) and breathing dysfunction in generalized convulsive seizures (GCS).

Methods In this prospective, multicenter analysis of GCS, ictal brainstem semiology was classified as (1) decerebration (bilateral symmetric tonic arm extension), (2) decortication (bilateral symmetric tonic arm flexion only), (3) hemi-decerebration (unilateral tonic arm extension with contralateral flexion) and (4) absence of ictal tonic phase. Postictal posturing was also assessed. Respiration was monitored with thoracoabdominal belts, video, and pulse oximetry.

Results Two hundred ninety-five seizures (180 patients) were analyzed. Ictal decerebration was observed in 122 of 295 (41.4%), decortication in 47 of 295 (15.9%), and hemi-decerebration in 28 of 295 (9.5%) seizures. Tonic phase was absent in 98 of 295 (33.2%) seizures. Postictal posturing occurred in 18 of 295 (6.1%) seizures. PGES risk increased with ictal decerebration (odds ratio [OR] 14.79, 95% confidence interval [CI] 6.18–35.39, p < 0.001), decortication (OR 11.26, 95% CI 2.96–42.93, p < 0.001), or hemi-decerebration (OR 48.56, 95% CI 6.07–388.78, p < 0.001). Ictal decerebration was associated with longer PGES (p = 0.011). Postictal posturing was associated with postconvulsive central apnea (PCCA) (p = 0.004), longer hypoxemia (p < 0.001), and Spo2 recovery (p = 0.035).

Conclusions Ictal brainstem semiology is associated with increased PGES risk. Ictal decerebration is associated with longer PGES. Postictal posturing is associated with a 6-fold increased risk of PCCA, longer hypoxemia, and Spo2 recovery. Peri-ictal brainstem posturing may be a surrogate biomarker for GCS severity identifiable without in-hospital monitoring.

Classification of Evidence This study provides Class III evidence that peri-ictal brainstem posturing is associated with the GCS with more prolonged PGES and more severe breathing dysfunction.

Glossary

CI=
confidence interval;
EST=
β estimate;
GCS=
generalized convulsive seizures;
GEE=
generalized estimating equation;
ICA=
ictal central apnea;
MORTEMUS=
Mortality in Epilepsy Monitoring Unit Study;
OR=
odds ratio;
PAG=
periaqueductal gray;
PCCA=
postconvulsive central apnea;
PGES=
postictal generalized electroencephalographic suppression;
PRISM=
Prevention and Risk Identification of SUDEP Mortality;
SUDEP=
sudden unexpected death in epilepsy;
VEEG=
video-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.

  • Editorial, page 89

  • Class of Evidence: NPub.org/coe

  • Received August 18, 2019.
  • Accepted in final form August 17, 2020.
  • © 2020 American Academy of Neurology
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  • Reader response: Association of peri-ictal brainstem posturing with seizure severity and breathing compromise in patients with generalized convulsive seizures
    • Aileen McGonigal, Neurologist and epileptologist, Aix-Marseille University, France
    Submitted December 10, 2020
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