Skip to main content
SpringerLink
Log in

Short-term deceleration capacity of heart rate: a sensitive marker of cardiac autonomic dysfunction in idiopathic Parkinson’s disease

Clinical Autonomic Research Aims and scope Submit manuscript

Cite this article

Abstract

Purpose

Cardiac autonomic dysfunction in idiopathic Parkinson’s disease (PD) manifests as reduced heart rate variability (HRV). In the present study, we explored the deceleration capacity of heart rate (DC) in patients with idiopathic PD, an advanced HRV marker that has proven clinical utility.

Methods

Standard and advanced HRV measures derived from 7-min electrocardiograms in 20 idiopathic PD patients and 27 healthy controls were analyzed. HRV measures were compared using regression analysis, controlling for age, sex, and mean heart rate.

Results

Significantly reduced HRV was found only in the subcohort of PD patients older than 60 years. Low- frequency power and global HRV measures were lower in patients than in controls, but standard beat-to-beat HRV markers (i.e., rMSSD and high-frequency power) were not significantly different between groups. DC was significantly reduced in the subcohort of PD patients older than 60 years compared to controls.

Conclusions

Deceleration-related oscillations of HRV were significantly reduced in the older PD patients compared to healthy controls, suggesting that short-term DC may be a sensitive marker of cardiac autonomic dysfunction in PD. DC may be complementary to traditional markers of short-term HRV for the evaluation of autonomic modulation in PD. Further study to examine the association between DC and cardiac adverse events in PD is needed to clarify the clinical relevance of DC in this population.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

References

  1. Poewe W et al (2017) Parkinson disease. Nat Rev Dis Primers 3(1):17013

    Article  PubMed  Google Scholar 

  2. Kallio M et al (2000) Heart rate variability in patients with untreated Parkinson’s disease. Eur J Neurol 7(6):667–672

    Article  CAS  PubMed  Google Scholar 

  3. Rodriguez M, Sabate M, Troncoso E (1996) Time and frequency domain analysis for the assessment of heart autonomic control in Parkinson’s disease. J Neural Transm (Vienna) 103(4):447–454

    Article  CAS  Google Scholar 

  4. Turkka JT, Tolonen U, Myllyla VV (1987) Cardiovascular reflexes in Parkinson’s disease. Eur Neurol 26(2):104–112

    Article  CAS  PubMed  Google Scholar 

  5. Oka H et al (2011) Cardiovascular dysautonomia in de novo Parkinson’s disease without orthostatic hypotension. Eur J Neurol 18(2):286–292

    Article  CAS  PubMed  Google Scholar 

  6. Rahman F et al (2011) Low frequency power of heart rate variability reflects baroreflex function, not cardiac sympathetic innervation. Clin Auton Res 21(3):133–141

    Article  PubMed  PubMed Central  Google Scholar 

  7. Haapaniemi TH et al (2001) Ambulatory ECG and analysis of heart rate variability in Parkinson’s disease. J Neurol Neurosurg Psychiatry 70(3):305–310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Kallio M et al (2002) Comparison of heart rate variability analysis methods in patients with Parkinson’s disease. Med Biol Eng Comput 40(4):408–414

    Article  CAS  PubMed  Google Scholar 

  9. Mihci E et al (2006) Orthostatic heart rate variability analysis in idiopathic Parkinson’s disease. Acta Neurol Scand 113(5):288–293

    Article  CAS  PubMed  Google Scholar 

  10. Buob A et al (2010) Parasympathetic but not sympathetic cardiac dysfunction at early stages of Parkinson’s disease. Clin Res Cardiol 99(11):701–706

    Article  PubMed  Google Scholar 

  11. Kang P, Kloke J, Jain S (2012) Olfactory dysfunction and parasympathetic dysautonomia in Parkinson’s disease. Clin Auton Res 22(4):161–166

    Article  PubMed  PubMed Central  Google Scholar 

  12. Barbic F et al (2007) Early abnormalities of vascular and cardiac autonomic control in Parkinson’s disease without orthostatic hypotension. Hypertension 49(1):120–126

    Article  CAS  PubMed  Google Scholar 

  13. Asahina M et al (2014) Sudomotor and cardiovascular dysfunction in patients with early untreated Parkinson’s disease. J Parkinsons Dis 4(3):385–393

    Article  CAS  PubMed  Google Scholar 

  14. Arnao V et al (2020) Impaired circadian heart rate variability in Parkinson’s disease: a time-domain analysis in ambulatory setting. BMC Neurol 20(1):152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Visanji NP et al (2017) Heart rate variability in leucine-rich repeat kinase 2-associated Parkinson’s disease. Mov Disord 32(4):610–614

    Article  CAS  PubMed  Google Scholar 

  16. Carricarte Naranjo C et al (2019) Increased markers of cardiac vagal activity in leucine-rich repeat kinase 2-associated Parkinson’s disease. Clin Auton Res 29(6):603–614

    Article  PubMed  Google Scholar 

  17. Müller MLTM, Bohnen NI (2013) Cholinergic dysfunction in Parkinson’s disease. Curr Neurol Neurosci Rep 13(9):377–377

    Article  PubMed  PubMed Central  Google Scholar 

  18. Bauer A et al (2006) Deceleration capacity of heart rate as a predictor of mortality after myocardial infarction: cohort study. Lancet 367(9523):1674–1681

    Article  PubMed  Google Scholar 

  19. Pan Q et al (2016) Do the deceleration/acceleration capacities of heart rate reflect cardiac sympathetic or vagal activity? A model study. Med Biol Eng Comput 54(12):1921–1933

    Article  PubMed  Google Scholar 

  20. Rizas KD et al (2018) Bedside autonomic risk stratification after myocardial infarction by means of short-term deceleration capacity of heart rate. Europace 20(Fi1):f129–f136

    Article  PubMed  Google Scholar 

  21. Sassi R et al (2015) 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 17(9):1341–1353

    Article  PubMed  Google Scholar 

  22. Hughes AJ et al (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55(3):181–184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Machado A et al (2000) Automatic filtering of R-R intervals for heart rate variability analysis. Ann Noninvasive Electrocardiol 5(3):255–261

    Article  Google Scholar 

  24. Cornforth D, Jelinek HF, Tarvainen M (2015) A comparison of nonlinear measures for the detection of cardiac autonomic neuropathy from heart rate variability. Entropy 17(3):1425–1440

    Article  Google Scholar 

  25. Parlitz U et al (2012) Classifying cardiac biosignals using ordinal pattern statistics and symbolic dynamics. Comput Biol Med 42(3):319–327

    Article  CAS  PubMed  Google Scholar 

  26. Carricarte-Naranjo C et al (2018) Rényi and permutation entropy analysis for assessment of cardiac autonomic neuropathy. In: Eskola H, Väisänen O, Viik J, Hyttinen J (eds) EMBEC & NBC 2017. EMBEC 2017, NBC 2017. IFMBE proceedings, vol 65. Springer, Singapore. https://doi.org/10.1007/978-981-10-5122-7_189

  27. Huikuri HV et al (1996) Sex-related differences in autonomic modulation of heart rate in middle-aged subjects. Circulation 94(2):122–125

    Article  CAS  PubMed  Google Scholar 

  28. Tsuji H et al (1996) Determinants of heart rate variability. J Am Coll Cardiol 28(6):1539–1546

    Article  CAS  PubMed  Google Scholar 

  29. Voss A et al (2015) Short-term heart rate variability–influence of gender and age in healthy subjects. PLoS ONE 10(3):e0118308–e0118308

    Article  PubMed  PubMed Central  Google Scholar 

  30. Delgado G et al (2014) Cardiovascular variability in Mexican patients with Parkinson’s disease. Arq Neuropsiquiatr 72(10):762–767

    Article  PubMed  Google Scholar 

  31. Maetzler W et al (2015) Time- and frequency-domain parameters of heart rate variability and sympathetic skin response in Parkinson’s disease. J Neural Transm (Vienna) 122(3):419–425

    Article  CAS  Google Scholar 

  32. Szili-Török T et al (1999) Abnormal cardiovascular autonomic regulation in Parkinson’s disease. J Clin Basic Cardiol 2(2):245–247

    Google Scholar 

  33. Estévez-Báez M et al (2016) A procedure to correct the effect of heart rate on heart rate variability indices: description and assessment. Int J Disabil Hum Dev 15(3):277–292

    Article  Google Scholar 

  34. Hindle JV (2010) Ageing, neurodegeneration and Parkinson’s disease. Age Ageing 39(2):156–161

    Article  PubMed  Google Scholar 

  35. Van Den Berge N et al (2021) Ageing promotes pathological alpha-synuclein propagation and autonomic dysfunction in wild-type rats. Brain 20:awab061. https://doi.org/10.1093/brain/awab061

  36. Jain S, Goldstein DS (2012) Cardiovascular dysautonomia in Parkinson disease: from pathophysiology to pathogenesis. Neurobiol Dis 46(3):572–580

    Article  CAS  PubMed  Google Scholar 

  37. Camerlingo M et al (1987) Parasympathetic assessment in Parkinson’s disease. Adv Neurol 45:267–269

    CAS  PubMed  Google Scholar 

  38. Ke JQ et al (2017) Sympathetic skin response and heart rate variability in predicting autonomic disorders in patients with Parkinson disease. Medicine (Baltimore) 96(18):e6523

    Article  CAS  Google Scholar 

  39. Erro R et al (2013) The Heterogeneity of Early Parkinson’s Disease: A Cluster Analysis on Newly Diagnosed Untreated Patients. PLoS ONE 8(8):e70244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Marras C, Lang A (2013) Parkinson’s disease subtypes: lost in translation? J Neurol Neurosurg Psychiatry 84(4):409–415

    Article  PubMed  Google Scholar 

  41. Bugalho P et al (2018) Heart rate variability in Parkinson disease and idiopathic REM sleep behavior disorder. Clin Auton Res 28(6):557–564

    Article  PubMed  Google Scholar 

  42. Cicero CE et al (2019) Cardiovascular autonomic function and MCI in Parkinson’s disease. Parkinsonism Relat Disord 69:55–58

    Article  PubMed  Google Scholar 

  43. Kiyono K et al (2012) Non-gaussianity of low frequency heart rate variability and sympathetic activation: lack of increases in multiple system atrophy and Parkinson disease. Front Physiol 3:34

    Article  PubMed  PubMed Central  Google Scholar 

  44. Campana LM et al (2010) Phase-rectified signal averaging as a sensitive index of autonomic changes with aging. J Appl Physiol 108(6):1668–1673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Ewing DJ et al (1985) The value of cardiovascular autonomic function tests: 10 years experience in diabetes. Diabetes Care 8(5):491–498

    Article  CAS  PubMed  Google Scholar 

  46. Torres McCook, A.R. (2019) Análisis de la Variabilidad de la Frecuencia Cardíaca en diferentes condiciones fisiológicas (unpublished diploma thesis). Universidad de La Habana, Havana

  47. Bigger JT et al (1993) The ability of several short-term measures of RR variability to predict mortality after myocardial infarction. Circulation 88(3):927–934

    Article  CAS  PubMed  Google Scholar 

  48. Algra A et al (1993) Heart rate variability from 24-hour electrocardiography and the 2-year risk for sudden death. Circulation 88(1):180–185

    Article  CAS  PubMed  Google Scholar 

  49. Rajput AH, Rozdilsky B (1976) Dysautonomia in Parkinsonism: a clinicopathological study. J Neurol Neurosurg Psychiatry 39(11):1092–1100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Matsumoto H et al (2014) Sudden death in Parkinson’s disease: A retrospective autopsy study. J Neurol Sci 343(1–2):149–152

    Article  PubMed  Google Scholar 

  51. Scorza FA et al (2018) Cardiac abnormalities in Parkinson’s disease and Parkinsonism. J Clin Neurosci 53:1–5

    Article  PubMed  Google Scholar 

  52. Penttilä J et al (2001) Time domain, geometrical and frequency domain analysis of cardiac vagal outflow: effects of various respiratory patterns. Clin Physiol 21(3):365–376

    Article  PubMed  Google Scholar 

  53. Gąsior JS et al (2016) Heart rate and respiratory rate influence on heart rate variability repeatability: effects of the correction for the prevailing heart rate. Front Physiol 7:356

    Article  PubMed  PubMed Central  Google Scholar 

  54. Kobayashi H (2009) Does paced breathing improve the reproducibility of heart rate variability measurements? J Physiol Anthropol 28(5):225–230

    Article  PubMed  Google Scholar 

  55. Perez-Lloret S, Barrantes FJ (2016) Deficits in cholinergic neurotransmission and their clinical correlates in Parkinson’s disease. Npj Parkinson Dis 2:16001

    Article  CAS  Google Scholar 

  56. Kim J-S et al (2016) Cardiovascular autonomic dysfunction in mild and advanced Parkinson’s disease. J Mov Dis 9(2):97–103

    Google Scholar 

  57. Porta A et al (2015) Limits of permutation-based entropies in assessing complexity of short heart period variability. Physiol Meas 36(4):755–765

    Article  PubMed  Google Scholar 

  58. Porta A et al (2012) Short-term complexity indexes of heart period and systolic arterial pressure variabilities provide complementary information. J Appl Physiol 113(12):1810–1820

    Article  CAS  PubMed  Google Scholar 

  59. Porta A et al (2020) Comparison of symbolization strategies for complexity assessment of spontaneous variability in individuals with signs of cardiovascular control impairment. Biomed Signal Process Cont 62:102128

    Article  Google Scholar 

  60. Porta A et al (2020) Are strategies favoring pattern matching a viable way to improve complexity estimation based on sample entropy? Entropy 22(7):724

    Article  PubMed Central  Google Scholar 

Download references

Acknowledgements

This paper is dedicated to the memory of Professor Mario Estévez Báez, an outstanding scientist who devoted his life to human physiology research, through his extensive studies on the assessment of autonomic nervous system and methodological aspects of HRV analysis. The authors would like to thank all participants for their valuable contribution to this study. This work was facilitated by a travel grant awarded by the International Parkinson and Movement Disorder Society Pan American Section to CCN. The study was funded by a research grant awarded by The Michael J. Fox Foundation for Parkinson’s Research to CM and BS.

Funding

This work was supported by the Michael J. Fox Foundation for Parkinson’s Research [Grant Number MJFF 6896].

Author information

Authors and Affiliations

  1. Facultad de Biología, Universidad de La Habana, Havana, Cuba

    Claudia Carricarte Naranjo & Andrés Machado

  2. Edmond J Safra Program in Parkinson’s Disease and the Morton and Gloria Shulman Movement Disorders Clinic, Toronto Western Hospital, Toronto, ON, Canada

    Connie Marras, Naomi P. Visanji & Anthony E. Lang

  3. Member of the National Coalition of Independent Scholars (NCIS), Battleboro, VT, USA

    David J. Cornforth

  4. Department of Radiology, University of Calgary, Calgary, AB, Canada

    Lazaro Sanchez‑Rodriguez

  5. Department of Pathology, Stanford School of Medicine, Stanford, CA, USA

    Birgitt Schüle

  6. Department of Neurology, University of California, San Francisco, CA, USA

    Samuel M. Goldman

  7. Departamento de Neurofisiología Clínica, Instituto de Neurología y Neurocirugía, La Habana, Cuba

    Mario Estévez

  8. School of Medicine, Washington University, St. Louis, MO, USA

    Phyllis K. Stein

  9. Khalifa University, Abu Dhabi, UAE

    Herbert F. Jelinek

Authors
  1. Claudia Carricarte Naranjo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Connie Marras
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Naomi P. Visanji
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. David J. Cornforth
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lazaro Sanchez‑Rodriguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Birgitt Schüle
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Samuel M. Goldman
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mario Estévez
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Phyllis K. Stein
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Anthony E. Lang
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Herbert F. Jelinek
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Andrés Machado
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Claudia Carricarte Naranjo.

Ethics declarations

Conflict of interest

CM has received research grants from the Michael J. Fox Foundation, Canadian Institutes of Health Research, Parkinson’s Foundation (US), National Institutes of Health (US), and International Parkinson and Movement Disorders Society. She is a consultant for Grey Matter Technologies and receives financial compensation as a steering committee member from the Michael J. Fox Foundation. The remaining authors declare that they have no conflict of interest.

Ethical standards

The study protocol was approved by the University Health Network Research Ethics Board (Toronto) and El Camino Hospital Institutional Review Board (Parkinson’s Institute). The study was performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.

Informed consent

All participants provided written informed consent prior to their inclusion in the study.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 379 KB)

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Carricarte Naranjo, C., Marras, C., Visanji, N.P. et al. Short-term deceleration capacity of heart rate: a sensitive marker of cardiac autonomic dysfunction in idiopathic Parkinson’s disease. Clin Auton Res 31, 729–736 (2021). https://doi.org/10.1007/s10286-021-00815-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10286-021-00815-4

Keywords

search

Navigation