CC BY 4.0 · Arq Neuropsiquiatr 2023; 81(01): 009-018
DOI: 10.1055/s-0042-1758862
Original Article

Is there a link between heart rate variability and cognitive decline? A cross-sectional study on patients with mild cognitive impairment and cognitively healthy controls

Existe uma ligação entre a variabilidade da frequência cardíaca e o declínio cognitivo? Um estudo transversal em pacientes com deficiência cognitiva leve e controles cognitivos saudáveis
1   Otto von Guericke University, Institute of Sport Science, Magdeburg, Germany.
,
2   German Center for Neurodegenerative Diseases, Neuroprotection Research Group, Magdeburg, Germany.
3   Otto von Guericke University, Department of Neurology, Medical Faculty, Magdeburg, Germany.
4   University of Potsdam, Faculty of Health Sciences, Degenerative and Chronic Diseases Research Group, Movement, Potsdam, Germany.
,
5   Otto von Guericke University, Faculty of Medicine, Department of Occupational Medicine, Magdeburg, Germany.
,
2   German Center for Neurodegenerative Diseases, Neuroprotection Research Group, Magdeburg, Germany.
3   Otto von Guericke University, Department of Neurology, Medical Faculty, Magdeburg, Germany.
4   University of Potsdam, Faculty of Health Sciences, Degenerative and Chronic Diseases Research Group, Movement, Potsdam, Germany.
,
6   Sapienza Università di Roma, Dipartimento di Psicologia, Rome, Italy.
7   IRCCS Fondazione Santa Lucia, Action and Body Lab, Rome, Italy.
,
1   Otto von Guericke University, Institute of Sport Science, Magdeburg, Germany.
,
1   Otto von Guericke University, Institute of Sport Science, Magdeburg, Germany.
,
2   German Center for Neurodegenerative Diseases, Neuroprotection Research Group, Magdeburg, Germany.
3   Otto von Guericke University, Department of Neurology, Medical Faculty, Magdeburg, Germany.
8   Otto- von- Guericke University Magdeburg, Institute of Cognitive Neurology and Dementia Research, Magdeburg, Germany.
,
9   German Research Group Neuroprotection Center for Neurodegenerative Diseases, Magdeburg, Germany.
,
10   Universidade Federal do Estado do Rio de Janeiro, Programa de Pós- Graduação em Enfermagem e Biociências, Rio de Janeiro RJ, Brazil.
11   Universidade Tiradentes, Programa de Pós- Graduação em Saúde e Ambiente, Aracaju SE, Brazil.
,
5   Otto von Guericke University, Faculty of Medicine, Department of Occupational Medicine, Magdeburg, Germany.
,
2   German Center for Neurodegenerative Diseases, Neuroprotection Research Group, Magdeburg, Germany.
3   Otto von Guericke University, Department of Neurology, Medical Faculty, Magdeburg, Germany.
4   University of Potsdam, Faculty of Health Sciences, Degenerative and Chronic Diseases Research Group, Movement, Potsdam, Germany.
12   Center Research Group Neuroprotection for Behavioral Brain Sciences, Magdeburg, Germany.
,
1   Otto von Guericke University, Institute of Sport Science, Magdeburg, Germany.
› Author Affiliations

Abstract

Background Given that, up to date, there is no effective strategy to treat dementia, a timely start of interventions in a prodromal stage such as mild cognitive impairment (MCI) is considered an important option to lower the overall societal burden. Although autonomic functions have been related to cognitive performance, both aspects have rarely been studied simultaneously in MCI.

Objective The aim of the present study was to investigate cardiac autonomic control in older adults with and without MCI.

Methods Cardiac autonomic control was assessed by means of heart rate variability (HRV) at resting state and during cognitive tasks in 22 older adults with MCI and 29 healthy controls (HCs). Resting HRV measurement was performed for 5 minutes during a sitting position. Afterwards, participants performed three PC-based tasks to probe performance in executive functions and language abilities (i.e., Stroop, N-back, and a verbal fluency task).

Results Participants with MCI showed a significant reduction of HRV in the frequency-domain (high frequency power) and nonlinear indices (SD2, D2, and DFA1) during resting state compared to HCs. Older individuals with MCI exhibited decreases in RMSSD and increases in DFA1 from resting state to Stroop and N-back tasks, reflecting strong vagal withdrawal, while this parameter remained stable in HCs.

Conclusion The results support the presence of autonomic dysfunction at the early stage of cognitive impairment. Heart rate variability could help in the prediction of cognitive decline as a noninvasive biomarker or as a tool to monitor the effectiveness of therapy and prevention of neurodegenerative diseases.

Resumo

Antecedentes Como não existe até o momento uma estratégia eficaz para tratar a demência de comprometimento cognitivo leve (MCI, na sigla em inglês), as intervenções em um estágio prodrômico são consideradas uma opção. Embora as funções autonômicas tenham sido relacionadas ao desempenho cognitivo, ambos os aspectos raramente foram estudados simultaneamente no MCI.

Objetivo Investigar o controle autonômico cardíaco em idosos com e sem MCI.

Métodos O controle autonômico cardíaco foi avaliado por meio da variabilidade da frequência cardíaca (HRV, na sigla em inglês) em repouso e durante tarefas cognitivas, em 22 idosos com MCI e 29 controles saudáveis (HCs, na sigla em inglês). A medida da HRV de repouso foi realizada por 5 minutos na posição sentada. Os participantes realizaram três tarefas executadas em computador para testar o desempenho em funções executivas e habilidades de linguagem (o teste de cores e palavras - Stroop, Tarefa N-back auditiva e uma tarefa de fluência verbal).

Resultados Em pacientes com MCI, observou-se uma redução significativa da HRV no domínio da frequência (potência de alta frequência) e índices não lineares (SD2, D2 e DFA1) durante o estado de repouso em comparação com os HCs. Indivíduos mais velhos com MCI exibiram diminuições em RMSSD e aumentos em DFA1 do estado de repouso para Stroop e tarefas N-back, refletindo forte recessão vagal, enquanto este parâmetro permaneceu estável em HC.

Conclusão Observou-se disfunção autonômica na fase inicial da neurodegeneração. A HRV pode ajudar na previsão do declínio cognitivo, como um biomarcador não invasivo, ou como uma ferramenta para monitorar a eficácia da terapia e prevenção de doenças neurodegenerativas.

Authors' Contributions

BG: writing – original draft; BG, MD, SD, FH, GF, CL, NH, PM, WG, IB, NM, AH, ED: writing – review and editing; BG, MD, CL, NHH, PM, WG, NM: data collection; BG, MD, SD, ED: data analysis; BG, MD, FH, CL: conception and study design; NM, AH: funding acquisition, supervision, and project administration. All authors revised and reviewed the manuscript. All authors have read and approved the final submitted manuscript.


Support

The present study was supported by the European Regional Development Fund (grant number: ZS/2018/08/94206).


European Regional Development Fund.


Grant number: ZS/2018/08/94206.




Publication History

Received: 14 November 2021

Accepted: 02 May 2022

Article published online:
14 March 2023

© 2023. Academia Brasileira de Neurologia. This is an open access article published by Thieme under the terms of the Creative Commons Attribution 4.0 International License, permitting copying and reproduction so long as the original work is given appropriate credit (https://creativecommons.org/licenses/by/4.0/)

Thieme Revinter Publicações Ltda.
Rua do Matoso 170, Rio de Janeiro, RJ, CEP 20270-135, Brazil

 
  • References

  • 1 Shaffer F, Ginsberg JP. An Overview of Heart Rate Variability Metrics and Norms. Front Public Health 2017; 5: 258
  • 2 Billman GE. Heart rate variability - a historical perspective. Front Physiol 2011; 2: 86
  • 3 Shaffer F, McCraty R, Zerr CL. A healthy heart is not a metronome: an integrative review of the heart's anatomy and heart rate variability. Front Psychol 2014; 5: 1040
  • 4 Sammito S, Böckelmann I. Factors influencing heart rate variability. ICFJ 2016; 6: 18-22
  • 5 Thayer JF, Lane RD. The role of vagal function in the risk for cardiovascular disease and mortality. Biol Psychol 2007; 74 (02) 224-242
  • 6 Forte G, Favieri F, Casagrande M. Heart Rate Variability and Cognitive Function: A Systematic Review. Front Neurosci 2019; 13: 710
  • 7 Grässler B, Hökelmann A, Cabral RH. Resting heart rate variability as a possible marker of cognitive decline. Kinesiology (Zagreb, Online) 2020; 52 (01) 72-84
  • 8 Forte G, Morelli M, Casagrande M. Heart Rate Variability and Decision-Making: Autonomic Responses in Making Decisions. Brain Sci 2021; 11 (02) 243
  • 9 Collins O, Dillon S, Finucane C, Lawlor B, Kenny RA. Parasympathetic autonomic dysfunction is common in mild cognitive impairment. Neurobiol Aging 2012; 33 (10) 2324-2333
  • 10 Zulli R, Nicosia F, Borroni B. et al. QT dispersion and heart rate variability abnormalities in Alzheimer's disease and in mild cognitive impairment. J Am Geriatr Soc 2005; 53 (12) 2135-2139
  • 11 Nicolini P, Ciulla MM, Malfatto G. et al. Autonomic dysfunction in mild cognitive impairment: evidence from power spectral analysis of heart rate variability in a cross-sectional case-control study. PLoS One 2014; 9 (05) e96656
  • 12 Guarino A, Forte G, Giovannoli J, Casagrande M. Executive functions in the elderly with mild cognitive impairment: a systematic review on motor and cognitive inhibition, conflict control and cognitive flexibility. Aging Ment Health 2020; 24 (07) 1028-1045
  • 13 Mitchell AJ, Shiri-Feshki M. Rate of progression of mild cognitive impairment to dementia–meta-analysis of 41 robust inception cohort studies. Acta Psychiatr Scand 2009; 119 (04) 252-265
  • 14 Schapkin SA, Freude G, Gajewski PD, Wild-Wall N, Falkenstein M. Effects of working memory load on performance and cardiovascular activity in younger and older workers. Int J Behav Med 2012; 19 (03) 359-371
  • 15 Laborde S, Mosley E, Thayer JF. Heart rate variability and cardiac vagal tone in psychophysiological research - Recommendations for experiment planning, data analysis, and data reporting. Front Psychol 2017; 8 (FEB): 213
  • 16 Bélanger S, Belleville S, Gauthier S. Inhibition impairments in Alzheimer's disease, mild cognitive impairment and healthy aging: effect of congruency proportion in a Stroop task. Neuropsychologia 2010; 48 (02) 581-590
  • 17 Morris JC, Heyman A, Mohs RC. et al. The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part I. Clinical and neuropsychological assessment of Alzheimer's disease. Neurology 1989; 39 (09) 1159-1165
  • 18 Petersen RC, Smith GE, Waring SC, Ivnik RJ, Tangalos EG, Kokmen E. Mild cognitive impairment: clinical characterization and outcome. Arch Neurol 1999; 56 (03) 303-308
  • 19 Grässler B, Herold F, Dordevic M. et al. Multimodal measurement approach to identify individuals with mild cognitive impairment: study protocol for a cross-sectional trial. BMJ Open 2021; 11 (05) e046879
  • 20 Stroop JR. Studies of interference in serial verbal reactions. J Exp Psychol 1935; 18 (06) 643-662
  • 21 Kirchner WK. Age differences in short-term retention of rapidly changing information. J Exp Psychol 1958; 55 (04) 352-358
  • 22 McDonnell M, Dill L, Panos S. et al. Verbal fluency as a screening tool for mild cognitive impairment. Int Psychogeriatr 2020; 32 (09) 1055-1062
  • 23 Aschenbrenner S, Tucha O, Lange KW. Regensburger Wortflüssigkeits-Test: RWT; Handanweisung. Göttingen: Hogrefe Verl. für Psychologie; 2000. . 121 p. ger.
  • 24 Sammito S, Thielmann B, Seibt R, Klussmann A, Weippert M, Böckelmann I. Guideline for the application of heart rate and heart rate variability in occupational medicine and occupational science. ASUI 2015; 2015 (06)
  • 25 Munoz ML, van Roon A, Riese H. et al. Validity of (Ultra-)Short recordings for heart rate variability measurements. PLoS One 2015; 10 (09) e0138921
  • 26 Fernandes de Godoy M. Nonlinear Analysis of Heart Rate Variability: A Comprehensive Review. J Cardiol Ther 2016; 3 (03) 528-533
  • 27 Nussinovitch U, Elishkevitz KP, Katz K. et al. Reliability of Ultra-Short ECG Indices for Heart Rate Variability. Ann Noninvasive Electrocardiol 2011; 16 (02) 117-122
  • 28 Cohen J. Statistical power analysis for the behavioral sciences. 2nd ed. Hillsdale, NJ: Erlbaum; 1988. :567
  • 29 Mellingsæter MR, Wyller TB, Ranhoff AH, Bogdanovic N, Wyller VB. Reduced sympathetic response to head-up tilt in subjects with mild cognitive impairment or mild Alzheimer's dementia. Dement Geriatr Cogn Disord Extra 2015; 5 (01) 107-115
  • 30 Gąsior JS, Rosoł M, Młyńczak M. et al. Reliability of Symbolic Analysis of Heart Rate Variability and Its Changes During Sympathetic Stimulation in Elite Modern Pentathlon Athletes: A Pilot Study. Front Physiol 2022; 13: 829887
  • 31 Gronwald T, Rogers B, Hoos O. Fractal Correlation Properties of Heart Rate Variability: A New Biomarker for Intensity Distribution in Endurance Exercise and Training Prescription?. Front Physiol 2020; 11: 550572
  • 32 Mäkikallio TH, Høiber S, Køber L. et al. Fractal analysis of heart rate dynamics as a predictor of mortality in patients with depressed left ventricular function after acute myocardial infarction. TRACE Investigators. TRAndolapril Cardiac Evaluation. Am J Cardiol 1999; 83 (06) 836-839
  • 33 Vazan R, Filcikova D, Mravec B. Effect of the Stroop test performed in supine position on the heart rate variability in both genders. Auton Neurosci 2017; 208: 156-160
  • 34 Young H, Benton D. We should be using nonlinear indices when relating heart-rate dynamics to cognition and mood. Sci Rep 2015; 5: 16619
  • 35 Thayer JF, Hansen AL, Saus-Rose E, Johnsen BH. Heart rate variability, prefrontal neural function, and cognitive performance: the neurovisceral integration perspective on self-regulation, adaptation, and health. Ann Behav Med 2009; 37 (02) 141-153
  • 36 Dlugaj M, Gerwig M, Wege N. et al. Elevated levels of high-sensitivity C-reactive protein are associated with mild cognitive impairment and its subtypes: results of a population-based case-control study. J Alzheimers Dis 2012; 28 (03) 503-514
  • 37 Forte G, De Pascalis V, Favieri F, Casagrande M. Effects of Blood Pressure on Cognitive Performance: A Systematic Review. J Clin Med 2019; 9 (01) E34