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December 14, 2021; 97 (24) Research Article

Association of Short-term Heart Rate Variability and Sudden Unexpected Death in Epilepsy

View ORCID ProfileShobi Sivathamboo, Daniel Friedman, Juliana Laze, View ORCID ProfileRussell Nightscales, View ORCID ProfileZhibin Chen, Levin Kuhlmann, View ORCID ProfileSasha Devore, View ORCID ProfileVaughan Macefield, Patrick Kwan, Wendyl D'Souza, View ORCID ProfileSamuel F. Berkovic, View ORCID ProfilePiero Perucca, Terence J. O'Brien, View ORCID ProfileOrrin Devinsky, on behalf of the MS-BioS Study Group
First published October 14, 2021, DOI: https://doi.org/10.1212/WNL.0000000000012946
Shobi Sivathamboo
From the Department of Neuroscience, Central Clinical School (S.S., R.N., Z.C., M.B., V.M., P.K., P.P., T.J.O.), Clinical Epidemiology, School of Public Health and Preventive Medicine (Z.C., M.B.), and Department of Data Science and AI, Faculty of Information Technology (L.K.), Monash University; Department of Medicine (The Royal Melbourne Hospital) (S.S., R.N., Z.C., M.B., P.K., P.P., T.J.O.), The University of Melbourne; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), The Royal Melbourne Hospital; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), Alfred Health, Melbourne, Australia; Department of Neurology (D.F., J.L., S.D., O.D.), New York University Grossman School of Medicine, New York; Human Autonomic Neurophysiology (V.M.), Baker Heart and Diabetes Institute, Melbourne; Department of Medicine (W.D., M.D.C.B.), St. Vincent's Hospital, The University of Melbourne, Fitzroy; and Department of Medicine (S.F.B.), Austin Health, The University of Melbourne, Heidelberg, Australia.
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Daniel Friedman
From the Department of Neuroscience, Central Clinical School (S.S., R.N., Z.C., M.B., V.M., P.K., P.P., T.J.O.), Clinical Epidemiology, School of Public Health and Preventive Medicine (Z.C., M.B.), and Department of Data Science and AI, Faculty of Information Technology (L.K.), Monash University; Department of Medicine (The Royal Melbourne Hospital) (S.S., R.N., Z.C., M.B., P.K., P.P., T.J.O.), The University of Melbourne; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), The Royal Melbourne Hospital; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), Alfred Health, Melbourne, Australia; Department of Neurology (D.F., J.L., S.D., O.D.), New York University Grossman School of Medicine, New York; Human Autonomic Neurophysiology (V.M.), Baker Heart and Diabetes Institute, Melbourne; Department of Medicine (W.D., M.D.C.B.), St. Vincent's Hospital, The University of Melbourne, Fitzroy; and Department of Medicine (S.F.B.), Austin Health, The University of Melbourne, Heidelberg, Australia.
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Juliana Laze
From the Department of Neuroscience, Central Clinical School (S.S., R.N., Z.C., M.B., V.M., P.K., P.P., T.J.O.), Clinical Epidemiology, School of Public Health and Preventive Medicine (Z.C., M.B.), and Department of Data Science and AI, Faculty of Information Technology (L.K.), Monash University; Department of Medicine (The Royal Melbourne Hospital) (S.S., R.N., Z.C., M.B., P.K., P.P., T.J.O.), The University of Melbourne; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), The Royal Melbourne Hospital; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), Alfred Health, Melbourne, Australia; Department of Neurology (D.F., J.L., S.D., O.D.), New York University Grossman School of Medicine, New York; Human Autonomic Neurophysiology (V.M.), Baker Heart and Diabetes Institute, Melbourne; Department of Medicine (W.D., M.D.C.B.), St. Vincent's Hospital, The University of Melbourne, Fitzroy; and Department of Medicine (S.F.B.), Austin Health, The University of Melbourne, Heidelberg, Australia.
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Russell Nightscales
From the Department of Neuroscience, Central Clinical School (S.S., R.N., Z.C., M.B., V.M., P.K., P.P., T.J.O.), Clinical Epidemiology, School of Public Health and Preventive Medicine (Z.C., M.B.), and Department of Data Science and AI, Faculty of Information Technology (L.K.), Monash University; Department of Medicine (The Royal Melbourne Hospital) (S.S., R.N., Z.C., M.B., P.K., P.P., T.J.O.), The University of Melbourne; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), The Royal Melbourne Hospital; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), Alfred Health, Melbourne, Australia; Department of Neurology (D.F., J.L., S.D., O.D.), New York University Grossman School of Medicine, New York; Human Autonomic Neurophysiology (V.M.), Baker Heart and Diabetes Institute, Melbourne; Department of Medicine (W.D., M.D.C.B.), St. Vincent's Hospital, The University of Melbourne, Fitzroy; and Department of Medicine (S.F.B.), Austin Health, The University of Melbourne, Heidelberg, Australia.
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Zhibin Chen
From the Department of Neuroscience, Central Clinical School (S.S., R.N., Z.C., M.B., V.M., P.K., P.P., T.J.O.), Clinical Epidemiology, School of Public Health and Preventive Medicine (Z.C., M.B.), and Department of Data Science and AI, Faculty of Information Technology (L.K.), Monash University; Department of Medicine (The Royal Melbourne Hospital) (S.S., R.N., Z.C., M.B., P.K., P.P., T.J.O.), The University of Melbourne; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), The Royal Melbourne Hospital; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), Alfred Health, Melbourne, Australia; Department of Neurology (D.F., J.L., S.D., O.D.), New York University Grossman School of Medicine, New York; Human Autonomic Neurophysiology (V.M.), Baker Heart and Diabetes Institute, Melbourne; Department of Medicine (W.D., M.D.C.B.), St. Vincent's Hospital, The University of Melbourne, Fitzroy; and Department of Medicine (S.F.B.), Austin Health, The University of Melbourne, Heidelberg, Australia.
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Levin Kuhlmann
From the Department of Neuroscience, Central Clinical School (S.S., R.N., Z.C., M.B., V.M., P.K., P.P., T.J.O.), Clinical Epidemiology, School of Public Health and Preventive Medicine (Z.C., M.B.), and Department of Data Science and AI, Faculty of Information Technology (L.K.), Monash University; Department of Medicine (The Royal Melbourne Hospital) (S.S., R.N., Z.C., M.B., P.K., P.P., T.J.O.), The University of Melbourne; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), The Royal Melbourne Hospital; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), Alfred Health, Melbourne, Australia; Department of Neurology (D.F., J.L., S.D., O.D.), New York University Grossman School of Medicine, New York; Human Autonomic Neurophysiology (V.M.), Baker Heart and Diabetes Institute, Melbourne; Department of Medicine (W.D., M.D.C.B.), St. Vincent's Hospital, The University of Melbourne, Fitzroy; and Department of Medicine (S.F.B.), Austin Health, The University of Melbourne, Heidelberg, Australia.
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Sasha Devore
From the Department of Neuroscience, Central Clinical School (S.S., R.N., Z.C., M.B., V.M., P.K., P.P., T.J.O.), Clinical Epidemiology, School of Public Health and Preventive Medicine (Z.C., M.B.), and Department of Data Science and AI, Faculty of Information Technology (L.K.), Monash University; Department of Medicine (The Royal Melbourne Hospital) (S.S., R.N., Z.C., M.B., P.K., P.P., T.J.O.), The University of Melbourne; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), The Royal Melbourne Hospital; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), Alfred Health, Melbourne, Australia; Department of Neurology (D.F., J.L., S.D., O.D.), New York University Grossman School of Medicine, New York; Human Autonomic Neurophysiology (V.M.), Baker Heart and Diabetes Institute, Melbourne; Department of Medicine (W.D., M.D.C.B.), St. Vincent's Hospital, The University of Melbourne, Fitzroy; and Department of Medicine (S.F.B.), Austin Health, The University of Melbourne, Heidelberg, Australia.
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Vaughan Macefield
From the Department of Neuroscience, Central Clinical School (S.S., R.N., Z.C., M.B., V.M., P.K., P.P., T.J.O.), Clinical Epidemiology, School of Public Health and Preventive Medicine (Z.C., M.B.), and Department of Data Science and AI, Faculty of Information Technology (L.K.), Monash University; Department of Medicine (The Royal Melbourne Hospital) (S.S., R.N., Z.C., M.B., P.K., P.P., T.J.O.), The University of Melbourne; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), The Royal Melbourne Hospital; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), Alfred Health, Melbourne, Australia; Department of Neurology (D.F., J.L., S.D., O.D.), New York University Grossman School of Medicine, New York; Human Autonomic Neurophysiology (V.M.), Baker Heart and Diabetes Institute, Melbourne; Department of Medicine (W.D., M.D.C.B.), St. Vincent's Hospital, The University of Melbourne, Fitzroy; and Department of Medicine (S.F.B.), Austin Health, The University of Melbourne, Heidelberg, Australia.
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Patrick Kwan
From the Department of Neuroscience, Central Clinical School (S.S., R.N., Z.C., M.B., V.M., P.K., P.P., T.J.O.), Clinical Epidemiology, School of Public Health and Preventive Medicine (Z.C., M.B.), and Department of Data Science and AI, Faculty of Information Technology (L.K.), Monash University; Department of Medicine (The Royal Melbourne Hospital) (S.S., R.N., Z.C., M.B., P.K., P.P., T.J.O.), The University of Melbourne; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), The Royal Melbourne Hospital; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), Alfred Health, Melbourne, Australia; Department of Neurology (D.F., J.L., S.D., O.D.), New York University Grossman School of Medicine, New York; Human Autonomic Neurophysiology (V.M.), Baker Heart and Diabetes Institute, Melbourne; Department of Medicine (W.D., M.D.C.B.), St. Vincent's Hospital, The University of Melbourne, Fitzroy; and Department of Medicine (S.F.B.), Austin Health, The University of Melbourne, Heidelberg, Australia.
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Wendyl D'Souza
From the Department of Neuroscience, Central Clinical School (S.S., R.N., Z.C., M.B., V.M., P.K., P.P., T.J.O.), Clinical Epidemiology, School of Public Health and Preventive Medicine (Z.C., M.B.), and Department of Data Science and AI, Faculty of Information Technology (L.K.), Monash University; Department of Medicine (The Royal Melbourne Hospital) (S.S., R.N., Z.C., M.B., P.K., P.P., T.J.O.), The University of Melbourne; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), The Royal Melbourne Hospital; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), Alfred Health, Melbourne, Australia; Department of Neurology (D.F., J.L., S.D., O.D.), New York University Grossman School of Medicine, New York; Human Autonomic Neurophysiology (V.M.), Baker Heart and Diabetes Institute, Melbourne; Department of Medicine (W.D., M.D.C.B.), St. Vincent's Hospital, The University of Melbourne, Fitzroy; and Department of Medicine (S.F.B.), Austin Health, The University of Melbourne, Heidelberg, Australia.
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Samuel F. Berkovic
From the Department of Neuroscience, Central Clinical School (S.S., R.N., Z.C., M.B., V.M., P.K., P.P., T.J.O.), Clinical Epidemiology, School of Public Health and Preventive Medicine (Z.C., M.B.), and Department of Data Science and AI, Faculty of Information Technology (L.K.), Monash University; Department of Medicine (The Royal Melbourne Hospital) (S.S., R.N., Z.C., M.B., P.K., P.P., T.J.O.), The University of Melbourne; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), The Royal Melbourne Hospital; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), Alfred Health, Melbourne, Australia; Department of Neurology (D.F., J.L., S.D., O.D.), New York University Grossman School of Medicine, New York; Human Autonomic Neurophysiology (V.M.), Baker Heart and Diabetes Institute, Melbourne; Department of Medicine (W.D., M.D.C.B.), St. Vincent's Hospital, The University of Melbourne, Fitzroy; and Department of Medicine (S.F.B.), Austin Health, The University of Melbourne, Heidelberg, Australia.
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Piero Perucca
From the Department of Neuroscience, Central Clinical School (S.S., R.N., Z.C., M.B., V.M., P.K., P.P., T.J.O.), Clinical Epidemiology, School of Public Health and Preventive Medicine (Z.C., M.B.), and Department of Data Science and AI, Faculty of Information Technology (L.K.), Monash University; Department of Medicine (The Royal Melbourne Hospital) (S.S., R.N., Z.C., M.B., P.K., P.P., T.J.O.), The University of Melbourne; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), The Royal Melbourne Hospital; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), Alfred Health, Melbourne, Australia; Department of Neurology (D.F., J.L., S.D., O.D.), New York University Grossman School of Medicine, New York; Human Autonomic Neurophysiology (V.M.), Baker Heart and Diabetes Institute, Melbourne; Department of Medicine (W.D., M.D.C.B.), St. Vincent's Hospital, The University of Melbourne, Fitzroy; and Department of Medicine (S.F.B.), Austin Health, The University of Melbourne, Heidelberg, Australia.
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Terence J. O'Brien
From the Department of Neuroscience, Central Clinical School (S.S., R.N., Z.C., M.B., V.M., P.K., P.P., T.J.O.), Clinical Epidemiology, School of Public Health and Preventive Medicine (Z.C., M.B.), and Department of Data Science and AI, Faculty of Information Technology (L.K.), Monash University; Department of Medicine (The Royal Melbourne Hospital) (S.S., R.N., Z.C., M.B., P.K., P.P., T.J.O.), The University of Melbourne; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), The Royal Melbourne Hospital; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), Alfred Health, Melbourne, Australia; Department of Neurology (D.F., J.L., S.D., O.D.), New York University Grossman School of Medicine, New York; Human Autonomic Neurophysiology (V.M.), Baker Heart and Diabetes Institute, Melbourne; Department of Medicine (W.D., M.D.C.B.), St. Vincent's Hospital, The University of Melbourne, Fitzroy; and Department of Medicine (S.F.B.), Austin Health, The University of Melbourne, Heidelberg, Australia.
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Orrin Devinsky
From the Department of Neuroscience, Central Clinical School (S.S., R.N., Z.C., M.B., V.M., P.K., P.P., T.J.O.), Clinical Epidemiology, School of Public Health and Preventive Medicine (Z.C., M.B.), and Department of Data Science and AI, Faculty of Information Technology (L.K.), Monash University; Department of Medicine (The Royal Melbourne Hospital) (S.S., R.N., Z.C., M.B., P.K., P.P., T.J.O.), The University of Melbourne; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), The Royal Melbourne Hospital; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), Alfred Health, Melbourne, Australia; Department of Neurology (D.F., J.L., S.D., O.D.), New York University Grossman School of Medicine, New York; Human Autonomic Neurophysiology (V.M.), Baker Heart and Diabetes Institute, Melbourne; Department of Medicine (W.D., M.D.C.B.), St. Vincent's Hospital, The University of Melbourne, Fitzroy; and Department of Medicine (S.F.B.), Austin Health, The University of Melbourne, Heidelberg, Australia.
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From the Department of Neuroscience, Central Clinical School (S.S., R.N., Z.C., M.B., V.M., P.K., P.P., T.J.O.), Clinical Epidemiology, School of Public Health and Preventive Medicine (Z.C., M.B.), and Department of Data Science and AI, Faculty of Information Technology (L.K.), Monash University; Department of Medicine (The Royal Melbourne Hospital) (S.S., R.N., Z.C., M.B., P.K., P.P., T.J.O.), The University of Melbourne; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), The Royal Melbourne Hospital; Department of Neurology (S.S., R.N., P.K., P.P., T.J.O.), Alfred Health, Melbourne, Australia; Department of Neurology (D.F., J.L., S.D., O.D.), New York University Grossman School of Medicine, New York; Human Autonomic Neurophysiology (V.M.), Baker Heart and Diabetes Institute, Melbourne; Department of Medicine (W.D., M.D.C.B.), St. Vincent's Hospital, The University of Melbourne, Fitzroy; and Department of Medicine (S.F.B.), Austin Health, The University of Melbourne, Heidelberg, Australia.
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Association of Short-term Heart Rate Variability and Sudden Unexpected Death in Epilepsy
Shobi Sivathamboo, Daniel Friedman, Juliana Laze, Russell Nightscales, Zhibin Chen, Levin Kuhlmann, Sasha Devore, Vaughan Macefield, Patrick Kwan, Wendyl D'Souza, Samuel F. Berkovic, Piero Perucca, Terence J. O'Brien, Orrin Devinsky, on behalf of the MS-BioS Study Group
Neurology Dec 2021, 97 (24) e2357-e2367; DOI: 10.1212/WNL.0000000000012946

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Abstract

Background and Objectives We compared heart rate variability (HRV) in sudden unexpected death in epilepsy (SUDEP) cases and living epilepsy controls.

Methods This international, multicenter, retrospective, nested case–control study examined patients admitted for video-EEG monitoring (VEM) between January 1, 2003, and December 31, 2014, and subsequently died of SUDEP. Time domain and frequency domain components were extracted from 5-minute interictal ECG recordings during sleep and wakefulness from SUDEP cases and controls.

Results We identified 31 SUDEP cases and 56 controls. Normalized low-frequency power (LFP) during wakefulness was lower in SUDEP cases (median 42.5, interquartile range [IQR] 32.6–52.6) than epilepsy controls (55.5, IQR 40.7–68.9; p = 0.015, critical value = 0.025). In the multivariable model, normalized LFP was lower in SUDEP cases compared to controls (contrast −11.01, 95% confidence interval [CI] −20.29 to 1.73; p = 0.020, critical value = 0.025). There was a negative correlation between LFP and the latency to SUDEP, where each 1% incremental reduction in normalized LFP conferred a 2.7% decrease in the latency to SUDEP (95% CI 0.95–0.995; p = 0.017, critical value = 0.025). Increased survival duration from VEM to SUDEP was associated with higher normalized high-frequency power (HFP; p = 0.002, critical value = 0.025). The survival model with normalized LFP was associated with SUDEP (c statistic 0.66, 95% CI 0.55–0.77), which nonsignificantly increased with the addition of normalized HFP (c statistic 0.70, 95% CI 0.59–0.81; p = 0.209).

Conclusions Reduced short-term LFP, which is a validated biomarker for sudden death, was associated with SUDEP. Increased HFP was associated with longer survival and may be cardioprotective in SUDEP. HRV quantification may help stratify individual SUDEP risk.

Classification of Evidence This study provides Class III evidence that in patients with epilepsy, some measures of HRV are associated with SUDEP.

Glossary

ASM=
antiseizure medication;
CI=
confidence interval;
EMU=
epilepsy monitoring unit;
GLM=
generalized linear model;
HFP=
high-frequency power;
HRV=
heart rate variability;
IQR=
interquartile range;
LFP=
low-frequency power;
RMSSD=
root mean square of the successive differences;
SDNN=
SD of the normal-to-normal interval;
SUDEP=
sudden unexpected death in epilepsy;
TCS=
tonic-clonic seizure;
VEM=
video-EEG monitoring;
VNS=
vagus nerve stimulator

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.

  • ↵* These authors contributed equally to this work.

  • ↵† These authors contributed equally to this work.

  • MS-BioS Study Group coinvestigators are listed in the appendix at the end of the article.

  • Class of Evidence: NPub.org/coe

  • Editorial, page 1103

  • Received May 13, 2021.
  • Accepted in final form September 29, 2021.
  • © 2021 American Academy of Neurology
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    • Appendix 1 Authors
    • Appendix 2 Coinvestigators
    • Footnotes
    • References
  • Figures & Data
  • Info & Disclosures
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