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.
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.
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.
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.
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Poewe W et al (2017) Parkinson disease. Nat Rev Dis Primers 3(1):17013
Kallio M et al (2000) Heart rate variability in patients with untreated Parkinson’s disease. Eur J Neurol 7(6):667–672
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
Turkka JT, Tolonen U, Myllyla VV (1987) Cardiovascular reflexes in Parkinson’s disease. Eur Neurol 26(2):104–112
Oka H et al (2011) Cardiovascular dysautonomia in de novo Parkinson’s disease without orthostatic hypotension. Eur J Neurol 18(2):286–292
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
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
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
Mihci E et al (2006) Orthostatic heart rate variability analysis in idiopathic Parkinson’s disease. Acta Neurol Scand 113(5):288–293
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
Kang P, Kloke J, Jain S (2012) Olfactory dysfunction and parasympathetic dysautonomia in Parkinson’s disease. Clin Auton Res 22(4):161–166
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
Asahina M et al (2014) Sudomotor and cardiovascular dysfunction in patients with early untreated Parkinson’s disease. J Parkinsons Dis 4(3):385–393
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
Visanji NP et al (2017) Heart rate variability in leucine-rich repeat kinase 2-associated Parkinson’s disease. Mov Disord 32(4):610–614
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
Müller MLTM, Bohnen NI (2013) Cholinergic dysfunction in Parkinson’s disease. Curr Neurol Neurosci Rep 13(9):377–377
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
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
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
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
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
Machado A et al (2000) Automatic filtering of R-R intervals for heart rate variability analysis. Ann Noninvasive Electrocardiol 5(3):255–261
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
Parlitz U et al (2012) Classifying cardiac biosignals using ordinal pattern statistics and symbolic dynamics. Comput Biol Med 42(3):319–327
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
Huikuri HV et al (1996) Sex-related differences in autonomic modulation of heart rate in middle-aged subjects. Circulation 94(2):122–125
Tsuji H et al (1996) Determinants of heart rate variability. J Am Coll Cardiol 28(6):1539–1546
Voss A et al (2015) Short-term heart rate variability–influence of gender and age in healthy subjects. PLoS ONE 10(3):e0118308–e0118308
Delgado G et al (2014) Cardiovascular variability in Mexican patients with Parkinson’s disease. Arq Neuropsiquiatr 72(10):762–767
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
Szili-Török T et al (1999) Abnormal cardiovascular autonomic regulation in Parkinson’s disease. J Clin Basic Cardiol 2(2):245–247
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
Hindle JV (2010) Ageing, neurodegeneration and Parkinson’s disease. Age Ageing 39(2):156–161
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
Jain S, Goldstein DS (2012) Cardiovascular dysautonomia in Parkinson disease: from pathophysiology to pathogenesis. Neurobiol Dis 46(3):572–580
Camerlingo M et al (1987) Parasympathetic assessment in Parkinson’s disease. Adv Neurol 45:267–269
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
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
Marras C, Lang A (2013) Parkinson’s disease subtypes: lost in translation? J Neurol Neurosurg Psychiatry 84(4):409–415
Bugalho P et al (2018) Heart rate variability in Parkinson disease and idiopathic REM sleep behavior disorder. Clin Auton Res 28(6):557–564
Cicero CE et al (2019) Cardiovascular autonomic function and MCI in Parkinson’s disease. Parkinsonism Relat Disord 69:55–58
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
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
Ewing DJ et al (1985) The value of cardiovascular autonomic function tests: 10 years experience in diabetes. Diabetes Care 8(5):491–498
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
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
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
Rajput AH, Rozdilsky B (1976) Dysautonomia in Parkinsonism: a clinicopathological study. J Neurol Neurosurg Psychiatry 39(11):1092–1100
Matsumoto H et al (2014) Sudden death in Parkinson’s disease: A retrospective autopsy study. J Neurol Sci 343(1–2):149–152
Scorza FA et al (2018) Cardiac abnormalities in Parkinson’s disease and Parkinsonism. J Clin Neurosci 53:1–5
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
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
Kobayashi H (2009) Does paced breathing improve the reproducibility of heart rate variability measurements? J Physiol Anthropol 28(5):225–230
Perez-Lloret S, Barrantes FJ (2016) Deficits in cholinergic neurotransmission and their clinical correlates in Parkinson’s disease. Npj Parkinson Dis 2:16001
Kim J-S et al (2016) Cardiovascular autonomic dysfunction in mild and advanced Parkinson’s disease. J Mov Dis 9(2):97–103
Porta A et al (2015) Limits of permutation-based entropies in assessing complexity of short heart period variability. Physiol Meas 36(4):755–765
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
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
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
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.
This work was supported by the Michael J. Fox Foundation for Parkinson’s Research [Grant Number MJFF 6896].
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.
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.
All participants provided written informed consent prior to their inclusion in the study.
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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