Generalized tonic-clonic seizures are accompanied by changes of interrelations within the autonomic nervous system

Solveig Vieluf; Tanuj Hasija; Peter J Schreier; Rima El Atrache; Sarah Hammond; Fatemeh Mohammadpour Touserkani; Rani A Sarkis; Tobias Loddenkemper; Claus Reinsberger

doi:10.1016/j.yebeh.2021.108321

Generalized tonic-clonic seizures are accompanied by changes of interrelations within the autonomic nervous system

Epilepsy Behav. 2021 Oct 5:124:108321. doi: 10.1016/j.yebeh.2021.108321. Online ahead of print.

Authors

Solveig Vieluf¹, Tanuj Hasija², Peter J Schreier², Rima El Atrache³, Sarah Hammond³, Fatemeh Mohammadpour Touserkani⁴, Rani A Sarkis⁵, Tobias Loddenkemper³, Claus Reinsberger⁶

Affiliations

¹ Division of Epilepsy and Clinical Neurophysiology, Boston Children's Hospital, Harvard Medical School, Boston, USA; Institute of Sports Medicine, Paderborn University, Paderborn, Germany. Electronic address: reinsberger@sportmed.upb.de.
² Signal and System Theory Group, Paderborn University, Paderborn, Germany.
³ Division of Epilepsy and Clinical Neurophysiology, Boston Children's Hospital, Harvard Medical School, Boston, USA.
⁴ Division of Epilepsy and Clinical Neurophysiology, Boston Children's Hospital, Harvard Medical School, Boston, USA; Department of Neurology, SUNY Downstate Medical Center, Brooklyn, NY, USA.
⁵ Division of Epilepsy, Dept. of Neurology, Brigham and Women's Hospital, Harvard Medical School, Boston, USA.
⁶ Institute of Sports Medicine, Paderborn University, Paderborn, Germany; Division of Epilepsy, Dept. of Neurology, Brigham and Women's Hospital, Harvard Medical School, Boston, USA.

PMID: 34624803
DOI: 10.1016/j.yebeh.2021.108321

Abstract

Purpose: A seizure is a strong central stimulus that affects multiple subsystems of the autonomic nervous system (ANS), and results in different interactions across ANS modalities. Here, we aimed to evaluate whether multimodal peripheral ANS measures demonstrate interactions before and after seizures as compared to controls to provide the basis for seizure detection and forecasting based on peripheral ANS signals.

Methods: Continuous electrodermal activity (EDA), heart rate (HR), peripheral body temperature (TEMP), and respiratory rate (RR) calculated based on blood volume pulse were acquired by a wireless multi-sensor device. We selected 45 min of preictal and 60 min of postictal data and time-matched segments for controls. Data were analyzed over 15-min windows. For unimodal analysis, mean values over each time window were calculated for all modalities and analyzed by Friedman's two-way analysis of variance.

Results: Twenty-one children with recorded generalized tonic-clonic seizures (GTCS), and 21 age- and gender-matched controls were included. Unimodal results revealed no significant effect for RR and TEMP, but EDA (p = 0.002) and HR (p < 0.001) were elevated 0-15 min after seizures. The averaged bimodal correlation across all pairs of modalities changed for 15-min windows in patients with seizures. The highest correlations were observed immediately before (0.85) and the lowest correlation immediately after seizures. Overall, average correlations for controls were higher.

Significance: Multimodal ANS changes related to GTCS occur within and across autonomic nervous system modalities. While unimodal changes were most prominent during postictal segments, bimodal correlations increased before seizures and decreased postictally. This offers a promising avenue for further research on seizure detection, and potentially risk assessment for seizure recurrence and sudden unexplained death in epilepsy.

Keywords: Autonomic network; Canonical correlation analysis; Multimodal analysis; People with epilepsy.