Circadian changes in the structure of cardiac rhythm during pre-symptomatic and symptomatic stages of Parkinson’s disease

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Objective. To study circadian regulation of heart rhythm during the pre-symptomatic (PS) and early symptomatic (ESS) stages of Parkinson’s disease (PD) and determine the functionally most unfavorable periods during which there is a risk of life-threatening arrhythmias. Material and methods. The studies were performed on C57BL/6 mice. ECG monitoring was performed in online mode using a wireless telemetry system (ADInstruments Australia). Results. Characteristics of circadian changes heart rate during PS and ESS of PD were detected. During PS changes in the autonomic regulation of the heart occur at night. The increase at this time of the parasympathetic tone indicates compensatory mechanisms that prevent changes in the total power spectrum. However, they can’t prevent the high risk of life-threatening arrhythmias. The early symptomatic stage leads to the changes in mechanisms of not only sympathetic, but also parasympathetic regulation of the heart, increase in sympathetic tone and disturbed structure of the heart rhythm over most of the day. The decrease in the total power of the spectrum indicates a decrease in the adaptive capacity of the cardiovascular system. The increase in the intervals of QT, QTc and Tpeak Tend, indicates a risk of life-threatening arrhythmias. Conclusion. PD predetermines complications of circadian autonomic regulation of the heart during PS and ESS, which can become the pathogenetic basis for severe cerebrocardial disorders.

Keywords:

Parkinson’s disease

heart rate variability

life-threatening arrhythmia

autonomic balance

Authors:

Mamalyga M.L.

Kafedra anatomii i fiziologii cheloveka i zhivotnykh Moskovskogo pedagogicheskogo gosudarstvennogo universiteta, Moskva

Mamalyga L.M.

Institute of Biology and Chemistry of the Moscow Pedagogical State University, Moscow

List of references:

Haapaniemi TH, Pursiainen V, Korpelainen JT, Huikuri HV, Sotaniemi KA, Myllylä VV. Ambulatory ECG and analysis of heart rate variability in Parkinson’s disease. J Neurol Neurosurg Psychiatry. 2001;70(3):305-310. https://doi.org/10.1136/jnnp.70.3.305
Pursiainen V. Autonomic dysfunction in early and advanced Parkinson’s disease. University of Oulu, Finland. 2007. http://jultika.oulu.fi/files/isbn9789514283888.pdf
Politis M, Piccini P, Pavese N, Koh SB, Brooks DJ. Evidence of dopamine dysfunction in the hypothalamus of patients with Parkinson’s disease: An in vivo 11C-raclopride PET study. Experimental Neurology. 2008;214(1):112-116. https://doi.org/10.1016/j.expneurol.2008.07.021
Seifried C, Boehncke S, Heinzmann J, Baudrexel S, Weise L, Gasser T, Eggert K, Fogel W, Baas H, Badenhoop K, Steinmetz H, Hilker R. Diurnal Variation of Hypothalamic Function and Chronic Subthalamic Nucleus Stimulation in Parkinson’s Disease. Neuroendocrinology. 2013;97(3):283-290. https://doi.org/10.1159/000343808
Rieu I, Boirie Y, Morio B, Derost P, Ulla M, Marques A, Debilly B, Bannier S, Durif F. The Idiopathic Parkinson’s disease: A metabolic disease? Rev Neurol (Paris). 2010;166(10):822-828. https://doi.org/10.1016/j.neurol.2010.08.001
Deguchi K, Sasaki I, Tsukaguchi M, Kamoda M, Touge T, Takeuchi H, Kuriyama S. Abnormalities of rate-corrected QT intervals in Parkinson’s disease — a comparison with multiple system atrophy and progressive supranuclear palsy. Journal of the Neurological Sciences. 2002;199(1-2):31-37. https://doi.org/10.1016/S0022-510X(02)00079-5
Mokhles MM, Trifirò G, Dieleman JP, Haag MD, van Soest EM, Verhamme KM, Mazzaglia G, Herings R, Luise Cd, Ross D, Brusselle G, Colao A, Haverkamp W, Schade R, Camp Gv, Zanettini R, Sturkenboom MC. The risk of new onset heart failure associated with dopamine agonist use in Parkinson’s disease. Pharmacological Research. 2012;65(3):358-364. https://doi.org/10.1016/j.phrs.2011.11.009
Oeda T, Masaki M, Yamamoto K, Mizuta E, Kitagawa N, Isono T, Taniguchi S, Doi K, Yaku H, Yutani C, Kawamura T, Kuno S, Sawada H. High risk factors for valvular heart disease from dopamine agonists in patients with Parkinson’s disease. J Neural Transm. 2009;116(2):171-178. https://doi.org/10.1007/s00702-008-0160-2
Ritz B, Rhodes SL, Qian L, Schernhammer E, Olsen JH, Friis S. L-type calcium channel blockers and Parkinson disease in Denmark. Ann Neurol. 2010;67(5):600-606. https://doi.org/10.1002/ana.21937
Mamalyga ML. Cardiovascular dysfunctions in brain disorders and their treatment. Saarbrücken, Germany: Academic Publishing. 2017.
Videnovic A, Willis GL. Circadian System — A Novel Diagnostic and Therapeutic Target in Parkinson’s Disease? Movement Disorders. 2016;31(3):260-269. https://doi.org/10.1002/mds.26509
Khaindrava VG, Kozina EA, Kucherianu VG, Kryzhanovskiĭ GN, Kudrin VS, Klodt PD, Bocharov EV, Raevskiĭ KS, Ugriumov MV. Modeling of preclinical and early clinical stages of Parkinson’s disease. Zhurnal nevrologii i psikhiatrii im. S.S. Korsakova. 2010;110(7):41-47. (In Russ.)
Khakimova GR, Kozina EA, Sapronova AYa, Ugryumov MV. Dopamine release in the substantia nigra and striatum at presymptomatic and early symptomatic stages in parkinsonian mice. Neurochemical Journal. 2011;5(1):35-41. (In Russ.) https://doi.org/10.1134/S1819712411010041
Ugrumov MV, Khaindrava VG, Kozina E.A, Kucheryanu VG, Bocharov EV, Kryzhanovsky GN, Kudrin VS, Narkevich VB, Klodt PM, Rayevsky KS, Pronina TS. Modeling of presymptomatic and symptomatic stages of parkinsonism in mice. Neuroscience. 2011;181(5):175-188. https://doi.org/10.1016/j.neuroscience.2011.03.007
Jost WH. Autonomic dysfunction in idiopathic Parkinson’s disease. J Neurol. 2003;250(1):128-130. https://doi.org/10.1007/s00415-003-1105-z
Korchounov A, Kessler KR, Yakhno NN, Damulin IV, Schipper HI. Determinants of autonomic dysfunction in idiopathic Parkinson’s disease. J Neurol. 2005;252(12):1530-1536. https://doi.org/10.1007/s00415-005-0909-6
Magenkurth C, Schnitzer R, Braune S. Symptoms of autonomic failure in Parkinson’s disease: prevalence and impact on daily life. Clin Auton Res. 2005;15(2):76-82. https://doi.org/10.1007/s10286-005-0253-z
Ugryumov MV. Expression of the enzymes of dopamine synthesis in mediumenergy neurons: functional significance and regulation. Uspekhi fiziologicheskih nauk. 2007;38(4):3-20. (In Russ.) http://www.fesmu.ru/elib/Article.aspx?id=171972
Saper CB, Scammell TE, Lu J. Review Article Hypothalamic regulation of sleep and circadian rhythms. Nature. 2005;437(7063):1257-1263. https://doi.org/10.1038/nature04284
Chou ThC, Scammell Th E, Gooley JJ, Gaus SE, Saper CB, Lu J. Critical Role of Dorsomedial Hypothalamic Nucleus in a Wide Range of Behavioral Circadian Rhythms. Journal of Neuroscience. 2003;23(33):10691-10702. https://www.ncbi.nlm.nih.gov/pubmed/14627654
Manni R, Terzagh, M, Pacchetti C, Nappi G. Sleep disorders in Parkinson’s disease: facts and new perspectives. Neurol Sci. 2007;28(1):1-5. https://doi.org/10.1007/s10072-007-0731-2
Bhidayasiri R, Truong DD. Therapeutic strategies for nonmotor symptoms in early Parkinson’s disease: the case for a higher priority and stronger evidence. Parkinsonism Relat Disord. 2012;18(1):110-113. https://doi.org/10.1016/S1353-8020(11)70035-9
Baevsky PM, Ivanov GG. Heart rate variability: theoretical aspects and possibilities of clinical application. Ul’trazvukovaya i funkcional’naya diagnostika. 2001;3:106-127. (In Russ.) https://elibrary.ru/item.asp?id=25990135
Vein AM. Autonomic disorders: clinical picture, diagnosis, treatment. M.: MIA; 2003. (In Russ.) http://www.booksmed.com/nevrologiya/77-vegetativnye-rasstrojstva-vejn-klinika.html
Oka H, Mochio S, Onouchi K, Morita M, Yoshioka M, Inoue K. Cardiovascular dysautonomia in de novo Parkinson’s disease. Neurol Sci. 2006;241(1-2):59-65. https://doi.org/10.1016/j.jns.2005.10.014
Pursiainen V, Haapaniemi TH, Korpelainen JT, Huikuri HV, Sotaniemi KA, Myllylä VV. Circadian heart rate variability in Parkinson’s disease. J Neurology. 2002;249(11):1535-1540. https://doi.org/10.1007/s00415-002-0884-0
Mamalyga ML, Mamalyga LM. Influence of pre-symptomatic and symptomatic stages of Parkinson’s disease and its treatment upon changes of variability of cardiac rhythm. Romanian Journal of Neurology. 2017;16(1):9-14. https://view.publitas.com/amph/rjn_2017_1_art-02/page/1
Devos D, Kroumova M, Bordet R, Vodougnon H, Guieu JD, Libersa C, Destee A. Heart rate variability and Parkinson’s disease severity. J Neural Transm (Vienna). 2003;110(9):997-1011. https://doi.org/10.1007/s00702-003-0016-8
Haapaniemi T. Autonomic dysfunction in Parkinson’s disease and its correlates to medication and dopamine transporter binding. Oulu University Press. Finland. 2001. http://jultika.oulu.fi/Record/isbn951-42-5963-7
Fuller RW, Hemrick-Luecke SK, Perry KW. Deprenyl antagonizes acute lethality of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in mice. J Pharmacol Exp Ther. 1988;247(2):531-535. https://www.ncbi.nlm.nih.gov/pubmed/3141609
Algeri S, Ambrosio S, Garofalo P, Gerli P. Peripheral effects of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) and its main metabolite 1-methyl-4-phenylpyridinium ion (MPP+) in the rat. European Journal of Pharmacology. 1987;141(2):309-312. https://www.ncbi.nlm.nih.gov/pubmed/3500067
Ren J, Porter JE, Wold LE, Aberle NS, Muralikrishnan Dh, Haselton JR. Depressed contractile function and adrenergic responsiveness of cardiac myocytes in an experimental model of Parkinson disease, the MPTP-treated mouse. Neurobiology of Aging. 2004;25(1):131-138. https://doi.org/10.1016/S0197-4580(03)00035-6
Ambrosio S, Blesa R, Mintenig GM. , Palacios-Araus L, Mahy N, Gual A. Acute effects of 1-methyl-4-phenyl-1,2,3,6-tetra-hydropyridine (MPTP) on catecholamines in heart, adrenal gland, retina and caudate nucleus of the cat. Toxicology Letters. 1988;44(1-2):1-6. https://www.ncbi.nlm.nih.gov/pubmed/3263717
Korshunov KS, Blakemore LJ, Trombley PQ. Dopamine: A Modulator of Circadian Rhythms in the Central Nervous System. Front Cell Neurosci. 2017;11(2):91-110. https://doi.org/10.3389/fncel.2017.00091
Verwey M, Dhir S, Amir Sh. Circadian influences on dopamine circuits of the brain: regulation of striatal rhythms of clock gene expression and implications for psychopathology and disease. F1000Res. 2016;5:F1000 Faculty Rev-2062. https://doi.org/10.12688/f1000research.9180.1
Yujnovsky I, Hirayama J, Doi M. Borrelli E, Sassone-Corsi P. Signaling mediated by the dopamine D2 receptor potentiates circadian regulation by CLOCK: BMAL1. Proc Natl Acad Sci USA. 2006;103(16):6386-6391. https://doi.org/10.1073/pnas.0510691103

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