Association between postictal EEG suppression, postictal autonomic dysfunction, and sudden unexpected death in epilepsy: Evidence from intracranial EEG

Behnaz Esmaeili; Daniel Weisholtz; Steven Tobochnik; Barbara Dworetzky; Daniel Friedman; Farhad Kaffashi; Sydney Cash; Brannon Cha; Juliana Laze; Dustine Reich; Pue Farooque; Taha Gholipour; Michael Singleton; Kenneth Loparo; Mohamad Koubeissi; Orrin Devinsky; Jong Woo Lee

doi:10.1016/j.clinph.2022.12.002

Association between postictal EEG suppression, postictal autonomic dysfunction, and sudden unexpected death in epilepsy: Evidence from intracranial EEG

Clin Neurophysiol. 2023 Feb:146:109-117. doi: 10.1016/j.clinph.2022.12.002. Epub 2022 Dec 16.

Authors

Behnaz Esmaeili¹, Daniel Weisholtz², Steven Tobochnik², Barbara Dworetzky², Daniel Friedman³, Farhad Kaffashi⁴, Sydney Cash⁵, Brannon Cha², Juliana Laze³, Dustine Reich², Pue Farooque⁶, Taha Gholipour⁷, Michael Singleton⁸, Kenneth Loparo⁴, Mohamad Koubeissi⁷, Orrin Devinsky³, Jong Woo Lee²

Affiliations

¹ Department of Neurology, University of Washington, Seattle, WA, USA; Department of Neurology, Brigham and Women's Hospital, Boston, MA, USA. Electronic address: Behnaz.esmaeili@gmail.com.
² Department of Neurology, Brigham and Women's Hospital, Boston, MA, USA.
³ Department of Neurology, New York University School of Medicine, New York, NY, USA.
⁴ Department of Electrical, Computer and Systems Engineering, Case Western Reserve University, Cleveland, OH, USA.
⁵ Department of Neurology, Massachusetts General Hospital, Boston, MA, USA.
⁶ Department of Neurology, Yale School of Medicine, New Haven, CT, USA.
⁷ Department of Neurology, George Washington University, Washington, DC, USA.
⁸ Institute of Translational Health Sciences, University of Washington, Seattle, WA, USA.

PMID: 36608528
DOI: 10.1016/j.clinph.2022.12.002

Abstract

Objective: The association between postictal electroencephalogram (EEG) suppression (PES), autonomic dysfunction, and Sudden Unexpected Death in Epilepsy (SUDEP) remains poorly understood. We compared PES on simultaneous intracranial and scalp-EEG and evaluated the association of PES with postictal heart rate variability (HRV) and SUDEP outcome.

Methods: Convulsive seizures were analyzed in patients with drug-resistant epilepsy at 5 centers. Intracranial PES was quantified using the Hilbert transform. HRV was quantified using root mean square of successive differences of interbeat intervals, low-frequency to high-frequency power ratio, and RR-intervals.

Results: There were 64 seizures from 63 patients without SUDEP and 11 seizures from 6 SUDEP patients. PES occurred in 99% and 87% of seizures on intracranial-EEG and scalp-EEG, respectively. Mean PES duration in intracranial and scalp-EEG was similar. Intracranial PES was regional (<90% of channels) in 46% of seizures; scalp PES was generalized in all seizures. Generalized PES showed greater decrease in postictal parasympathetic activity than regional PES. PES duration and extent were similar between patients with and without SUDEP.

Conclusions: Regional intracranial PES can be present despite scalp-EEG demonstrating generalized or no PES. Postictal autonomic dysfunction correlates with the extent of PES.

Significance: Intracranial-EEG demonstrates changes in autonomic regulatory networks not seen on scalp-EEG.

Keywords: Heart rate variability; Intracranial EEG; Postictal EEG suppression; SUDEP; Scalp EEG; Sudden Unexpected Death in Epilepsy.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Death, Sudden / etiology
Electrocorticography
Electroencephalography
Epilepsy*
Humans
Primary Dysautonomias*
Seizures / diagnosis
Sudden Unexpected Death in Epilepsy*