Journal of Neural Transmission

, Volume 122, Issue 3, pp 419–425 | Cite as

Time- and frequency-domain parameters of heart rate variability and sympathetic skin response in Parkinson’s disease

  • Walter Maetzler
  • Marie Karam
  • Monika Fruhmann Berger
  • Tanja Heger
  • Corina Maetzler
  • Heinz Ruediger
  • Juliana Bronzova
  • Patricia Pita Lobo
  • Joaquim J. Ferreira
  • Tjalf Ziemssen
  • Daniela Berg
Neurology and Preclinical Neurological Studies - Original Article

Abstract

The autonomic nervous system (ANS) is regularly affected in Parkinson’s disease (PD). Information on autonomic dysfunction can be derived from e.g. altered heart rate variability (HRV) and sympathetic skin response (SSR). Such parameters can be quantified easily and measured repeatedly which might be helpful for evaluating disease progression and therapeutic outcome. In this 2-center study, HRV and SSR of 45 PD patients and 26 controls were recorded. HRV was measured during supine metronomic breathing and analyzed in time- and frequency-domains. SSR was evoked by repetitive auditory stimulation. Various ANS parameters were compared (1) between patients and healthy controls, (2) to clinical scales (Unified Parkinson’s disease rating scale, Mini-Mental State Examination, Becks Depression Inventory), and (3) to disease duration. Root mean square of successive differences (RMSSD) and low frequency/high frequency (LF/HF) ratio differed significantly between PD and controls. Both, HRV and SSR parameters showed low or no association with clinical scores. Time-domain parameters tended to be affected already at early PD stages but did not consistently change with longer disease duration. In contrast, frequency-domain parameters were not altered in early PD phases but tended to be lower (LF, LF/HF ratio), respectively higher (HF) with increasing disease duration. This report confirms previous results of altered ANS parameters in PD. In addition, it suggests that (1) these ANS parameters are not relevantly associated with motor, behavioral, and cognitive changes in PD, (2) time-domain parameters are useful for the assessment of early PD, and (3) frequency-domain parameters are more closely associated with disease duration.

Keywords

Autonomic nervous system Heart rate variability Neurodegeneration Parkinson’s disease Progression Sympathetic skin response 

Supplementary material

702_2014_1276_MOESM1_ESM.docx (21 kb)
Supplementary material 1 (DOCX 20 kb)

References

  1. Beck AT, Steer RA, Ball R, Ranieri W (1996) Comparison of Beck depression inventories -IA and -II in psychiatric outpatients. J Pers Assess 67:588–597CrossRefPubMedGoogle Scholar
  2. Braune HJ, Korchounov AM, Schipper HI (1997) Autonomic dysfunction in Parkinson’s disease assessed by sympathetic skin response: a prospective clinical and neurophysiological trial on 50 patients. Acta Neurol Scand 95:293–297CrossRefPubMedGoogle Scholar
  3. Brisinda D, Sorbo AR, Di Giacopo R, Venuti A, Bentivoglio AR et al (2014) Cardiovascular autonomic nervous system evaluation in Parkinson disease and multiple system atrophy. J Neurol Sci 336:197–202. doi:10.1016/j.jns.2013.10.039 CrossRefPubMedGoogle Scholar
  4. Choi BO, Bang OY, Sohn YH, Sunwoo IN (1998) Sympathetic skin response and cardiovascular autonomic function tests in Parkinson’s disease. Yonsei Med J 39:439–445CrossRefPubMedGoogle Scholar
  5. Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198CrossRefPubMedGoogle Scholar
  6. Friedrich C, Rudiger H, Schmidt C, Herting B, Prieur S et al (2008) Baroreflex sensitivity and power spectral analysis in different extrapyramidal syndromes. J Neural Transm 115:1527–1536CrossRefPubMedGoogle Scholar
  7. Friedrich C, Rudiger H, Schmidt C, Herting B, Prieur S et al (2010) Baroreflex sensitivity and power spectral analysis during autonomic testing in different extrapyramidal syndromes. Mov Disord 25:315–324CrossRefPubMedGoogle Scholar
  8. Gibb WR, Lees AJ (1988) A comparison of clinical and pathological features of young- and old-onset Parkinson’s disease. Neurology 38:1402–1406CrossRefPubMedGoogle Scholar
  9. Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S et al (2008) Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord 23:2129–2170CrossRefPubMedGoogle Scholar
  10. Haapaniemi TH, Korpelainen JT, Tolonen U, Suominen K, Sotaniemi KA et al (2000) Suppressed sympathetic skin response in Parkinson disease. Clin Auton Res 10:337–342CrossRefPubMedGoogle Scholar
  11. Haapaniemi TH, Pursiainen V, Korpelainen JT, Huikuri HV, Sotaniemi KA et al (2001) Ambulatory ECG and analysis of heart rate variability in Parkinson’s disease. J Neurol Neurosurg Psychiatry 70:305–310CrossRefPubMedCentralPubMedGoogle Scholar
  12. Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17:427–442CrossRefPubMedGoogle Scholar
  13. Jain S, Ton TG, Perera S, Zheng Y, Stein PK et al (2012) Cardiovascular physiology in premotor Parkinson’s disease: a neuroepidemiologic study. Mov Disord 27:988–995CrossRefPubMedCentralPubMedGoogle Scholar
  14. Kallio M, Haapaniemi T, Turkka J, Suominen K, Tolonen U et al (2000) Heart rate variability in patients with untreated Parkinson’s disease. Eur J Neurol 7:667–672CrossRefPubMedGoogle Scholar
  15. Lanfranchi PA, Fradette L, Gagnon J-F, Colombo R, Montplaisir J (2007) Cardiac autonomic regulation during sleep in idiopathic REM sleep behavior disorder. Sleep 30:1019–1025PubMedCentralPubMedGoogle Scholar
  16. Linden D, Diehl RR, Berlit P (1997) Sympathetic cardiovascular dysfunction in long-standing idiopathic Parkinson’s disease. Clin Aut Res 7:311–314CrossRefGoogle Scholar
  17. Maetzler W, Liepelt I, Berg D (2009) Progression of Parkinson’s disease in the clinical phase: potential markers. Lancet Neurol 8:1158–1171CrossRefPubMedGoogle Scholar
  18. Mesec A, Sega S, Trost M, Pogacnik T (1999) The deterioration of cardiovascular reflexes in Parkinson’s disease. Acta Neurol Scand 100:296–299CrossRefPubMedGoogle Scholar
  19. Niwa F, Kuriyama N, Nakagawa M, Imanishi J (2011) Circadian rhythm of rest activity and autonomic nervous system activity at different stages in Parkinson’s disease. Aut Neurosci 165:195–200CrossRefGoogle Scholar
  20. Orimo S, Ozawa E, Nakade S, Sugimoto T, Mizusawa H (1999) (123)I-metaiodobenzylguanidine myocardial scintigraphy in Parkinson’s disease. J Neurol Neurosurg Psychiatry 67:189–194CrossRefPubMedCentralPubMedGoogle Scholar
  21. Pursiainen V, Haapaniemi TH, Korpelainen JT, Huikuri HV, Sotaniemi KA et al (2002) Circadian heart rate variability in Parkinson’s disease. J Neurol 249:1535–1540CrossRefPubMedGoogle Scholar
  22. Reimann M, Friedrich C, Gasch J, Reichmann H, Rudiger H et al (2010a) Trigonometric regressive spectral analysis reliably maps dynamic changes in baroreflex sensitivity and autonomic tone: the effect of gender and age. PLoS One 5:e12187CrossRefPubMedCentralPubMedGoogle Scholar
  23. Reimann M, Schmidt C, Herting B, Prieur S, Junghanns S et al (2010b) Comprehensive autonomic assessment does not differentiate between Parkinson’s disease, multiple system atrophy and progressive supranuclear palsy. J Neural Transm 117:69–76CrossRefPubMedGoogle Scholar
  24. Rüdiger H, Klinghammer L, Scheuch K (1999) The trigonometric regressive spectral analysis–a method for mapping of beat-to-beat recorded cardiovascular parameters on to frequency domain in comparison with Fourier transformation. Comput Methods Programs Biomed 58:1–15CrossRefPubMedGoogle Scholar
  25. Sauvageot N, Vaillant M, Diederich NJ (2011) Reduced sympathetically driven heart rate variability during sleep in Parkinson’s disease: a case-control polysomnography-based study. Mov Disord 26:234–240. doi:10.1002/mds.23479 CrossRefPubMedGoogle Scholar
  26. Schestatsky P, Ehlers JA, Rieder CR, Gomes I (2006) Evaluation of sympathetic skin response in Parkinson’s disease. Park Relat Disord 12:486–491CrossRefGoogle Scholar
  27. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology (1996) Heart rate variability: standards of measurement, physiological interpretation and clinical use. Circulation 93:1043–1065Google Scholar
  28. Turkka JT, Tolonen U, Myllylä VV (1987) Cardiovascular reflexes in Parkinson’s disease. Eur Neurol 26:104–112CrossRefPubMedGoogle Scholar
  29. Van Dijk JG, Haan J, Zwinderman K, Kremer B, van Hilten BJ et al (1993) Autonomic nervous system dysfunction in Parkinson’s disease: relationships with age, medication, duration, and severity. J Neurol Neurosurg Psychiatry 56:1090–1095CrossRefPubMedCentralPubMedGoogle Scholar
  30. Visser M, van Rooden SM, Verbaan D, Marinus J, Stiggelbout AM et al (2008) A comprehensive model of health-related quality of life in Parkinson’s disease. J Neurol 255:1580–1587. doi:10.1007/s00415-008-0994-4 CrossRefPubMedGoogle Scholar
  31. Wang N, Gibbons CH, Lafo J, Freeman R (2013) α-Synuclein in cutaneous autonomic nerves. Neurology 81:1604–1610. doi:10.1212/WNL.0b013e3182a9f449 CrossRefPubMedCentralPubMedGoogle Scholar
  32. Ziemssen T, Reichmann H (2010) Cardiovascular autonomic dysfunction in Parkinson’s disease. J Neurol Sci 289:74–80CrossRefPubMedGoogle Scholar
  33. Ziemssen T, Reichmann H (2011) Cardiovascular autonomic testing in extrapyramidal disorders. J Neurol Sci 310:129–132. doi:10.1016/j.jns.2011.07.032 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Wien 2014

Authors and Affiliations

  • Walter Maetzler
    • 1
    • 2
  • Marie Karam
    • 1
    • 2
  • Monika Fruhmann Berger
    • 1
    • 2
  • Tanja Heger
    • 1
    • 2
  • Corina Maetzler
    • 1
    • 2
  • Heinz Ruediger
    • 3
  • Juliana Bronzova
    • 4
  • Patricia Pita Lobo
    • 4
  • Joaquim J. Ferreira
    • 4
  • Tjalf Ziemssen
    • 3
  • Daniela Berg
    • 1
    • 2
  1. 1.Department of Neurodegeneration, Hertie Institute for Clinical Brain ResearchUniversity of TuebingenTuebingenGermany
  2. 2.DZNE, German Center of Neurodegenerative DiseasesTüebingenGermany
  3. 3.Department of Neurology, Multiple Sclerosis Centre DresdenUniversity Clinic Carl Gustavus Carus, University of TechnologyDresdenGermany
  4. 4.Laboratory of Clinical Pharmacology and Therapeutics and Instituto de Medicina Molecular, Faculty of MedicineUniversity of LisbonLisbonPortugal

Personalised recommendations