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CC BY-NC-ND 4.0 · Arq Neuropsiquiatr 2020; 78(11): 724-732
DOI: 10.1590/0004-282X20200087
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Heart rate variability as an autonomic biomarker in ischemic stroke

Variabilidade da frequência cardíaca como biomarcador autonômico em pacientes com acidente vascular cerebral isquêmico
Natalia Buitrago-Ricaurte 
1   Universidade Federal de São Paulo, Department of Neurology, São Paulo SP, Brazil.
,
Fátima Cintra 
2   Universidade Federal de São Paulo, Department of Cardiology, São Paulo SP, Brazil.
,
Gisele Sampaio Silva 
1   Universidade Federal de São Paulo, Department of Neurology, São Paulo SP, Brazil.
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ABSTRACT

Stroke is one of the leading causes of mortality and disability worldwide. Autonomic dysfunction after ischemic stroke is frequently associated with cardiac complications and high mortality. The brain-heart axis is a good model for understanding autonomic interaction between the autonomic central network and the cardiovascular system. Heart rate variability (HRV) analysis is a non-invasive approach for understanding cardiac autonomic regulation. In stroke patients, HRV parameters are altered in the acute and chronic stages of the disease, having a prognostic value. In this literature review we summarize the main concepts about the autonomic nervous system and HRV as autonomic biomarkers in ischemic stroke.

RESUMO

O acidente vascular cerebral (AVC) é uma das principais causas de mortalidade e deficiência no mundo inteiro. Alterações do sistema nervoso autônomo após AVC estão frequentemente associadas a complicações cardíacas e alta mortalidade. O eixo cérebro-coração é um modelo apropriado para entender as interações entre a rede central autonômica e o sistema cardiovascular. A análise da variabilidade da frequência cardíaca (VFC) é uma aproximação não invasiva para o entendimento da regulação autonômica cardíaca. Em doentes que sofreram um AVC, os parâmetros da VFC se encontram alterados nas fases aguda e crônica da doença, com a possibilidade de valor prognóstico. Nesta revisão da literatura, apresentamos os principais conceitos sobre o sistema nervoso autônomo e a variabilidade da frequência cardíaca como biomarcador autonômico no acidente vascular cerebral isquêmico.

Keywords:

Heart Rate Determination - Autonomic Nervous System - Biomarkers - Stroke

Palavras-chave:

Determinação da Frequência Cardíaca - Sistema Nervoso Autônomo - Biomarcadores - Acidente Vascular Cerebral

Authors’ contributions:

All authors contributed to the design and implementation of the search strategy and to the writing of the manuscript.




Publication History

Received: 14 January 2020

Accepted: 18 April 2020

Article published online:
07 June 2023

© 2020. Academia Brasileira de Neurologia. This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commecial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/)

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  • References

  • 1 Ministério da Saúde do Brasil. Análise situação em saúde e desafios nos Objetivos do Desenvolvimento Sustentável. Brasília: Secretaria de Vigilância da Saúde; 2017. Available from: http://bvsms.saude.gov.br/bvs/publicacoes/saude_brasil_2017_analise_situacao_saude_desafios_objetivos_desenvolvimento_sustetantavel.pdf.
  • 2 Katan M, Luft A. Global burden of stroke. Semin Neurol. 2018 Apr;38(2):208-11. https://doi.org/10.1055/s-0038-1649503
  • 3 Brouns R, De Deyn PP. The complexity of neurobiological processes in acute ischemic stroke. Clin Neurol Neurosurg. 2009 Jul;111(6):483-95. https://doi.org/10.1016/j.clineuro.2009.04.001
  • 4 Benarroch EE. The central autonomic network: functional organization, dysfunction, and perspective. Mayo Clin Proc. 1993 Oct;68(10):988-1001. https://doi.org/10.1016/s0025-6196(12)62272-1
  • 5 Manea MM, Comsa M, Minca A, Dragos D, Popa C. Brain-heart axis–Review Article. J Med Life. Jul-Sep 2015;8(3):266-71.
  • 6 Daniele O, Caravaglios G, Fierro B, Natalè E. Stroke and cardiac arrhythmias. J Stroke Cerebrovasc Dis. Jan-Feb 2002;11(1):28-33. https://doi.org/10.1053/jscd.2002.123972
  • 7 Freeman R, Chapleau MW. Testing the autonomic nervous system. Handb Clin Neurol. 2013;115:115-36. https://doi.org/10.1016/B978-0-444-52902-2.00007-2
  • 8 Seifert F, Kallmünzer B, Gutjahr I, Breuer L, Winder K, Kaschka I, et al. Neuroanatomical correlates of severe cardiac arrhythmias in acute ischemic stroke. J Neurol. 2015 May;262(5):1182-90. https://doi.org/10.1007/s00415-015-7684-9
  • 9 Ruthirago D, Julayanont P, Tantrachoti P, Kim J, Nugent K. Cardiac arrhythmias and abnormal electrocardiograms after acute stroke. Am J Med Sci. 2016 Jan;351(1):112-8. https://doi.org/10.1016/j.amjms.2015.10.020
  • 10 Wehrwein EA, Orer HS, Barman SM. Overview of the anatomy, physiology, and pharmacology of the autonomic nervous system. Compr Physiol. 2016 Jun;6(3):1239-78. https://doi.org/10.1002/cphy.c15003
  • 11 Cannon WB. the interrelations of emotions as suggested by recent physiological researches. Am J Psychol. 1914 Apr;25(2):256-82. https://doi.org/10.2307/1413414
  • 12 Hall JE, Guyton AC. Guyton and Hall textbook of medical physiology. 12. ed. Philadelphia, PA: Saunders/Elsevier; 2011.
  • 13 Beissner F, Meissner K, Bär K-J, Napadow V. The autonomic brain: an activation likelihood estimation meta-analysis for central processing of autonomic function. J Neurosci. 2013 Jun 19;33(25):10503-11. https://doi.org/10.1523/JNEUROSCI.1103-13.2013
  • 14 Sklerov M, Dayan E, Browner N. Functional neuroimaging of the central autonomic network: recent developments and clinical implications. Clin Auton Res. 2019 Dec;29(6):555-66. https://doi.org/10.1007/s10286-018-0577-0
  • 15 Karemaker JM. An introduction into autonomic nervous function. Physiol Meas. 2017 May;38(5):R89-R118. https://doi.org/10.1088/1361-6579/aa6782
  • 16 Ziemssen T, Siepmann T. The investigation of the cardiovascular and sudomotor autonomic nervous system – a review. Front Neurol. 2019 Feb;10:53. https://doi.org/10.3389/fneur.2019.00053
  • 17 Sletten DM, Suarez GA, Low PA, Mandrekar J, Singer W. COMPASS 31: a refined and abbreviated composite autonomic symptom score. Mayo Clin Proc. 2012 Dec;87(12):1196-201. https://doi.org/10.1016/j.mayocp.2012.10.013
  • 18 Macey PM, Ogren JA, Kumar R, Harper RM. Functional imaging of autonomic regulation: methods and key findings. Front Neurosci. 2016 Jan;9:513. https://doi.org/10.3389/fnins.2015.00513
  • 19 Boylan M. Galen: on blood, the pulse, and the arteries. J Hist Biol. Summer 2007;40(2):207-30. https://doi.org/10.1007/s10739-006-9116-2
  • 20 AlGhatrif M, Lindsay J. A brief review: history to understand fundamentals of electrocardiography. J Community Hosp Intern Med Perspect. 2012 Apr 30;2(1). https://doi.org/10.3402/jchimp.v2i1.14383
  • 21 Task Force. Heart rate variability. Standards of measurement, physiological interpretation, and clinical use. Task Force of The European Society of Cardiology and the North American Society for Pacing and Electrophysiology. Eur Heart J. 1996;17(3):354-81.
  • 22 Cygankiewicz I, Zareba W. Heart rate variability. Handb Clin Neurol. 2013;117:379-93. https://doi.org/10.1016/B978-0-444-53491-0.00031-6
  • 23 Moorman JR, Delos JB, Flower AA, Cao H, Kovatchev BP, Richman JS, et al. Cardiovascular oscillations at the bedside: early diagnosis of neonatal sepsis using heart rate characteristics monitoring. Physiol Meas. 2011 Nov;32(11):1821-32. https://doi.org/10.1088/0967-3334/32/11/S08
  • 24 Fairchild KD, Schelonka RL, Kaufman DA, Carlo WA, Kattwinkel J, Porcelli PJ, et al. Septicemia mortality reduction in neonates in a heart rate characteristics monitoring trial. Pediatr Res. 2013 Nov;74(5):570-5. https://doi.org/10.1038/pr.2013.136
  • 25 Singh N, Moneghetti KJ, Christle JW, Hadley D, Plews D, Froelicher V. Heart rate variability: an old metric with new meaning in the era of using mHealth technologies for health and exercise training guidance. Part One: Physiology and Methods. Arrhythm Electrophysiol Rev. 2018 Aug;7(3):193-8. https://doi.org/10.15420/aer.2018.27.2
  • 26 Gordan R, Gwathmey JK, Xie L-H. Autonomic and endocrine control of cardiovascular function. World J Cardiol. 2015 Apr;7(4):204-14. https://doi.org/10.4330/wjc.v7.i4.204
  • 27 Mendelowitz D. Advances in parasympathetic control of heart rate and cardiac function. News Physiol Sci. 1999 Aug;14:155-61. https://doi.org/10.1152/physiologyonline.1999.14.4.155
  • 28 Kumar KR, Kirsch RE, Hornik CP. Cardiovascular physiology for intensivists. In: Critical heart disease in infants and children. 3. ed. Elsevier; 2019. p. 111-133.e5. Available from: https://linkinghub.elsevier.com/retrieve/pii/B9781455707607000139
  • 29 Sassi R, Cerutti S, Lombardi F, Malik M, Huikuri HV, Peng C-K, et al. Advances in heart rate variability signal analysis: joint position statement by the e-Cardiology ESC Working Group and the European Heart Rhythm Association co-endorsed by the Asia Pacific Heart Rhythm Society. Europace. 2015 Sep;17(9):1341-53. https://doi.org/10.1093/europace/euv015
  • 30 Trimmel K, Sacha J, Huikuri HV, editors. Heart rate variability: clinical applications and interaction between HRV and heart rate. Frontiers Media SA; 2015. (Frontiers Research Topics). Available from: http://www.frontiersin.org/books/Heart_Rate_Variability_Clinical_Applications_and_Interaction_between_HRV_and_Heart_Rate/698
  • 31 Dutsch M, Burger M, Dorfler C, Schwab S, Hilz MJ. Cardiovascular autonomic function in poststroke patients. Neurology. 2007 Dec;69(24):2249-55. https://doi.org/10.1212/01.wnl.0000286946.06639.a7
  • 32 McCraty R, Shaffer F. Heart rate variability: new perspectives on physiological mechanisms, assessment of self-regulatory capacity, and health risk. Glob Adv Health Med. 2015 Jan;4(1):46-61. https://doi.org/10.7453/gahmj.2014.073
  • 33 Li K, Rüdiger H, Ziemssen T. Spectral analysis of heart rate variability: time window matters. Front Neurol. 2019 May;10:545. https://doi.org/10.3389/fneur.2019.00545
  • 34 Germán-Salló Z, Germán-Salló M. Non-linear methods in HRV analysis. Procedia Technol. 2016;22:645-51. https://doi.org/10.1016/j.protcy.2016.01.134
  • 35 Ernst G. Hidden signals — the history and methods of heart rate variability. Front Public Health. 2017 Oct;5:265. https://doi.org/10.3389/fpubh.2017.00265
  • 36 Shaffer F, Ginsberg JP. An overview of heart rate variability metrics and norms. Front Public Health. 2017;5:258. https://doi.org/10.3389/fpubh.2017.00258
  • 37 El Husseini N, Laskowitz DT. The role of neuroendocrine pathways in prognosis after stroke. Expert Rev Neurother. 2014 Feb;14(2):217-32. https://doi.org/10.1586/14737175.2014.877841
  • 38 Fu Y, Liu Q, Anrather J, Shi F-D. Immune interventions in stroke. Nat Rev Neurol. 2015 Sep;11(9):524-35. https://doi.org/10.1038/nrneurol.2015.144
  • 39 Kumar S, Selim MH, Caplan LR. Medical complications after stroke. Lancet Neurol. 2010 Jan;9(1):105-18. https://doi.org/10.1016/S1474-4422(09)70266-2
  • 40 Maaijwee NA, Rutten-Jacobs LC, Schaapsmeerders P, van Dijk EJ, de Leeuw F-E. Ischaemic stroke in young adults: risk factors and long-term consequences. Nat Rev Neurol. 2014 Jun;10(6):315-25. https://doi.org/10.1038/nrneurol.2014.72
  • 41 Scheitz JF, Nolte CH, Doehner W, Hachinski V, Endres M. Stroke–heart syndrome: clinical presentation and underlying mechanisms. Lancet Neurol. 2018 Dec;17(12):1109-20. https://doi.org/10.1016/S1474-4422(18)30336-3
  • 42 Chen Z, Venkat P, Seyfried D, Chopp M, Yan T, Chen J. Brain-heart interaction: cardiac complications after stroke. Circ Res. 2017 Aug;121(4):451-68. https://doi.org/10.1161/CIRCRESAHA.117.311170
  • 43 Dorrance AM, Fink G. Effects of stroke on the autonomic nervous system. In: Terjung R, editor. Comprehensive physiology. Hoboken, NJ, USA: John Wiley & Sons, Inc.; 2015. p. 1241-63. Available from: http://doi.wiley.com/10.1002/cphy.c140016
  • 44 Yperzeele L, van Hooff R-J, Nagels G, De Smedt A, De Keyser J, Brouns R. Heart rate variability and baroreceptor sensitivity in acute stroke: a systematic review. Int J Stroke. 2015 Aug;10(6):796-800. https://doi.org/10.1111/ijs.12573
  • 45 Palamarchuk I, Kimpinski K, Lippert C, Hachinski V. Nocturnal deterioration after ischemic stroke and autonomic dysfunction: hypothesis and implications. Cerebrovasc Dis. 2013;36(5-6):454-61. https://doi.org/10.1159/000356093
  • 46 Raghu ALB, Parker T, van Wyk A, Green AL. Insula stroke: the weird and the worrisome. Postgrad Med J. 2019 Sep;95(1127):497-504. http://dx.doi.org/10.1136/postgradmedj-2019-136732
  • 47 Sposato LA, Riccio PM, Hachinski V. Poststroke atrial fibrillation: cause or consequence? Critical review of current views. Neurology. 2014 Apr;82(13):1180-6. https://doi.org/10.1212/WNL.20200087202000870265
  • 48 Grilletti J, Scapini K, Bernardes N, Spadari J, Bigongiari A, Mazuchi F, et al. Impaired baroreflex sensitivity and increased systolic blood pressure variability in chronic post-ischemic stroke. Clinics. 2018 Oct;73:e253. https://doi.org/10.6061/clinics/2018/e253
  • 49 Lees T, Shad-Kaneez F, Simpson AM, Nassif NT, Lin Y, Lal S. Heart rate variability as a biomarker for predicting stroke, post-stroke complications and functionality. Biomark Insights. 2018;13:1177271918786931. https://doi.org/10.1177/1177271918786931
  • 50 Tobaldini E, Proserpio P, Oppo V, Figorilli M, Fiorelli EM, Manconi M, et al. Cardiac autonomic dynamics during sleep are lost in patients with TIA and stroke. J Sleep Res. 2019 Jun;29(3):e12878. https://doi.org/10.1111/jsr.12878
  • 51 Binici Z, Mouridsen MR, Køber L, Sajadieh A. Decreased nighttime heart rate variability is associated with increased stroke risk. Stroke. 2011 Nov;42(11):3196-201. https://doi.org/10.1161/STROKEAHA.110.607697
  • 52 Oka H. Heart rate variability and neurological disorders. In: Iwase S, Hayano J, Orimo S, editors. Clinical assessment of the autonomic nervous system. Tokyo: Springer Japan; 2017. p.179-97. Available from: http://link.springer.com/10.1007/978-4-431-56012-8_11
  • 53 Pandian JD, Gall SL, Kate MP, Silva GS, Akinyemi RO, Ovbiagele BI, et al. Prevention of stroke: a global perspective. Lancet. 2018 Oct;392(10154):1269-78. https://doi.org/10.1016/S0140-6736(18)31269-8
  • 54 Ghandehari K. Barriers of thrombolysis therapy in developing countries. Stroke Res Treat. 2011;2011:686797. https://doi.org/10.4061/2011/686797