Analysis of heart rate variability in corn snakes (Pantherophis guttatus)
DOI:
https://doi.org/10.33448/rsd-v10i11.19781Keywords:
Autonomic regulationAbstract
The assessment of heart rate variability (HRV) by linear methods in conjunction with Poincaré plots can be useful for evaluating cardiac regulation by the autonomic nervous system and for the diagnosis and prognosis of heart disease in snakes. In this report, we describe an analysis of HRV in conscious adult corn snakes Pantherophis guttatus (P. guttatus). The electrocardiogram (ECG) parameters were determined in adult corn snakes (8 females, 13 males) and used for HRV analysis, and the RR interval was analyzed by linear methods in the time and frequency domains. There was no sex-related difference in heart rate. However, significant differences were seen in the duration of the P, PR, and T waves and QRS complex; there was no difference in the QT interval. The values for the RR interval varied by 15.3% and 18.8% in male and female snakes, respectively, and there was considerable variation in the values for the high and low frequency domains. The changes in the time domain were attributed to regulation by the parasympathetic branch of the autonomic nervous system, in agreement with variations in the high and low frequency domains. The values for standard deviations 1 and 2 in Poincaré plots, as well as the values of the frequency domain, provide useful parameters for future studies of cardiac function in P. guttatus.
References
Arita, M., Saeki, K., Tanoue, M., Fukushima, I. & Ito, M. (1967) Effects of catecholamines, propranolol, acetylcholine and ouabain on the transmembrane action potentials and contractility of the isolated venae cavae proximal to the heart of the rabbit. Jpn J Physiol. 17(2):158-73.
Armelin, V.A., Braga, V. H. S., Guagnoni, J. N., Crestani, A. M., Abe, A. S. & Florindo, L. H. (2019) Autonomic control of cardiovascular adjustments associated with orthostasis in the scansorial snake Boa constrictor. J Exp Biol. 222:jeb197848.
Bird, W. M., Peak, P. & Baxley, D. L. (2015) Natural history and meristics of an allopatric population of red cornsnakes, Pantherophis guttatus (Linnaeus, 1766) in central Kentucky, USA. J North Am Herpetol. (1):6-11.
Campbell, H. A., Leite, C. A. C., Wang, T., Skals, M., Abe, A. S., Egginton, S., Rantin, F. T., Bishop, C. M. & Taylor, E. W. (2006) Evidence for a respiratory component, similar to mammalian respiratory sinus arrhythmia, in the heart rate variability signal from the rattlesnake, Crotalus durissus terrificus. J Exp Biol. 209:2628-36.
Conant, R. & Collins, T. J. (1998) A field guide to the amphibians and reptiles of Eastern and Central North America. 3rd ed. Boston:Houghton Mifflin Co.
Conceição, M. E. B. A. M., Monteiro, F. O. B., Andrade, R. S. & Melchert, A. (2014) Effect of biometric variables on two-dimensional echocardiographic measurements in the red-tailed boa (Boa constrictor constrictor). J Zoo Wildl Med. 45(3):672-77.
Cruz, J. G. P. & Junkes, L. (2008) Controle autonômico da frequência cardíaca em Spilotes pullatus (Colubridae) como determinante das respostas de medo. Arq Bras Med Vet Zootec. 60(6):1468-71.
Freitas, A. F. (2000) Sistema nervoso autônomo e aparelho cardiovascular: um paradigma de auto-organização, complexidade e caos. Rev Port Cardiol. 19:161-91.
Gil, A. C. (2010) Como elaborar projetos de pesquisa. 4. ed. São Paulo: Atlas.
Gemer, C. M. (2016) Eletrocardiograma, movimento contrátil cardíaco e frequência cardíaca da lagartixa, Hemidactylus mabouia (Moreau de Jonnès, 1818). Dissertação de Mestrado, Faculdade de Engenharia Elétrica e de Computação, Universidade Estadual de Campinas (UNICAMP).
Hoshi, T. & Armstrong, C. M. (2013) C-Type inactivation of voltage-gated K+ channels: pore constriction or dilation? J Gen Physiol. 141(2):151-60.
Jensen, B., Boukens, B. J. D., Postma, A. V., Gunst, Q. D., van den Hoff, M. J. B., Moorman, A. F. M., Wang, T. & Christoffels, V. M. (2012) Identifying the evolutionary building blocks of the cardiac conduction system. PLoS One 7(9):e44231.
Jensen, B., Moorman, A. F. M. & Wang, T. (2014) Structure and function of the hearts of lizards and snakes. Biol Rev Camb Philos Soc. 89(2):302-36.
Jensen, B., van den Berg, G, van den Deol, R., Oostra, R. J., Wang, T. & Moorman, A. F. M. (2013) Development of the hearts of lizards and snakes and perspectives to cardiac evolution. PLoS One 8(6):e63651.
Jensen, D. D., Lieu, T., Halls, M. L., Veldhuis, N. A., Imlach, W. L., Mai, Q. N., Poole, D. P., Quach, T., Aurelio, L., Conner, J., Herenbrink, C. K., Barlow, N., Simpson, J. S., Scanlon, M. J., Graham, B., McCluskey, A., Robinson, P. J., Escriou, V., Nassini, R., Materazzi, S., Geppetti, P., Hicks, G. A., Christie, M. J., Porter, C. J. H., Canals, M. & Bunnett, N. W. (2017) Neurokinin 1 receptor signaling in endosomes mediates sustained nociception and is a viable therapeutic target for prolonged pain relief. Sci Transl Med. May 31;9(392):eaal3447. doi: 10.1126/scitranslmed.aal3447. PMID: 28566424; PMCID: PMC6034632.
Kik, M. J. L. & Mitchell, M. A. (2005) Reptile cardiology: a review of anatomy and physiology, diagnostic approaches and clinical disease. Semin Avian Exotic Pet Med. 14(1):52-60.
La Rovere, M. T., Pinna, G. D., Maestri, R., Barlera, S., Bernardinangeli, M., Veniani, M., Nicolosi, G. L., Marchioli, R., Tavazzi, L. & GISSI-HF Investigators. (2012) Autonomic markers and cardiovascular and arrhythmic events in heart failure patients: still a place in prognostication? Data from the GISSI-HF trial. Eur J Heart Fail. 14(12):1410-19.
Lewis, M., Bouvard, J., Eatwell, K. & Culshaw, G. (2020) Standardisation of electrocardiographic examination in corn snakes (Pantherophis guttatus). Vet Rec.186:e29.
Lillywhite, H. B., Albert, J. S., Sheehy, C. M. & Seymour, R. S. (2012) Gravity and the evolution of cardiopulmonary morphology in snakes. Comp Biochem Physiol A Mol Integr Physiol. 161(2):230-42.
Lillywhite, H. B., Zippel, K. C. & Farrell, A. P. (1999) Resting and maximal heart rates in ectothermic vertebrates. Comp Biochem Physiol A Mol Integr Physiol. 124(4):369-82.
Liu, R., Feng, H. Z. & Jin, J. P. (2014) Physiological contractility of cardiomyocytes in the wall of mouse and rat azygos vein. Am J Physiol Cell Physiol. 306(7):697-704.
Lopes, P. F. F., Oliveira, M. I. B., André, S. M. S., Nascimento, D. L. A., Silva, C. S. S., Rebouças, G. M., Felipe, T. R., Albuquerque Filho, N. J. B. & Medeiros, H. J. (2013) Aplicabilidade clínica da variabilidade da frequência cardíaca. Rev Neurocienc.21(2):600-03.
Malik, M. & Camm, A. J. (1995) Heart rate variability. 1st ed. Armonk:Futura.
Mullen, R. K. (1967) Comparative electrocardiography of the Squamata. Physiol Zool. 40(2):114-26.
Nijsen, M. J. M. A., Croiset, G., Diamant, M., Broekhoven, M. H., Wied, D. De. & Wiegant, V. M. (1998) Vagal activation in novelty-induced tachycardia during the light phase in the rat. Physiol Behav. 63(2):233-9.
Nilson, S. (2010) Comparative anatomy of the autonomic nervous system. Autonom Neurosci. 165(1):3-9.
Pess, M., Neal, A., Müller, K., Schmidt, V., Truen, U., Leinecker, N. & Marschang, R. (2016) Virus distribution and detection in corn snakes (Pantherophis guttatus) after experimental infection with three different ferlavirus strains. Vet Microbiol. 182:213-22
Rocha, R. M., Albuquerque, D. C. & Albanesi Filho, F. M. (2005) Variabilidade da frequência cardíaca e ritmo circadiano em pacientes com angina estável. Rev Socerj. 18(5):429-42.
Roy, B. & Ghatak, S. (2013) Métodos não-lineares para avaliar mudanças na variabilidade da frequência cardíaca em pacientes com diabetes tipo 2. Arq Bras Cardiol. 101(4):317-27.
Sá, J. C. F., Costa, E. C., Silva, E. & Azevedo, G. D. (2013) Variabilidade da frequência cardíaca como método de avaliação do sistema nervoso autônomo na síndrome dos ovários policísticos. Rev Bras Ginecol Obstet. 35(9):421-6.
Shaffer, F. & Ginsberg, J. P. (2017) An overview of heart rate variability metrics and norms. Front Public Health. 5:258.
Shoemaker, N. J. & Zandvliet, M. M. J. M. (2005) Electrocardiograms in selected species. Semin Avian Exotic Pet Med. 14(1):26-33.
Stuginski, D. R., Fernandes, W. & Grego, K. F. (2011) Parâmetros eletrocardiográficos de cascavéis (Crotalus durissus, Linnaeus, 1758) em cativeiro. Arch Vet Sci. 16(3):31-7.
Strussmann, C. & Sazima, I. (1991) Predation on avian eggs by the boid snake, Eunectes notaeus. Herpetological Review 22: 118–120.
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. Eur Heart J. 17(5):354-81.
Taylor, E. W., Leite, C. A. C., Sartori, M. R., Wang, T., Abe, A. S. & Crossley, D. A. (2014) The phylogeny and ontogeny of autonomic control of the heart and cardiorespiratory interactions in vertebrates. J Exp Biol. 217(5):690-703.
Temple, I. P., Inada, S., Dobrzynski, H. & Boyett, M. R. (2013) Connexins and the atrioventricular node. Heart Rhyth. 10(2):297-304.
Valentinuzzi, M. E., Hoff, H. E. & Geddes, M. E. (1970) Electrocardiogram of the snake: effect of vagal stimulation on the Q-T duration. J Electrocardiol. 3(1):21-8.
Vanderlei, L. C. M., Pastre, C. M., Hoshi, R. A., Carvalho, T. D., Godoy, M. F. (2009) Noções básicas de variabilidade da frequência cardíaca e sua aplicabilidade clínica. Rev Bras Cir Cardiovasc. 24(2):205-17.
Vanderlei, L. C. M., Pastre, C. M., Freitas Júnior, I. F. & Godoy, M. F. (2010) Índices geométricos de variabilidade da frequência cardíaca em crianças obesas e eutróficas. Arq Bras Cardiol. 95(1):30-40.
Veras, L. & González, J. G. (1999) Power spectral analysis of short-term RR interval and arterial blood pressure oscillations in the lizard, Gallotia galloti: effects of sympathetic blockade. J Exp Zool. 283(2):113-20.
Veras, L., González, J. G. & Pereda, E. (2000) Relationship between cortical electrical and cardiac autonomic activities in the awake lizard, Gallotia galloti. J Exp Zool. 287(1):21-8.
Wang, T., Altimiras, J., Klein, W. & Axelsson, M. (2003) Ventricular haemodynamics in Python molurus: separation of pulmonary and systemic pressures. J Exp Biol. 206:4241-45.
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Copyright (c) 2021 Antonio Gomes da Silva Neto; Daniel Souza Ferreira Magalhães; Raduan Hage; Laurita dos Santos; José Carlos Cogo
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