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Nonlinear analysis of heart rate variability for evaluating the growing pig stress response to an acute heat episode

Published online by Cambridge University Press:  12 July 2019

C. J. Byrd Open the ORCID record for C. J. Byrd [Opens in a new window] ,
J. S. Johnson ,
J. S. Radcliffe ,
B. A. Craig ,
S. D. Eicher  and
D. C. Lay Jr.
C. J. Byrd
Affiliation:
Department of Animal Sciences, Purdue University, West Lafayette, IN 47907, USA
J. S. Johnson
Affiliation:
USDA-ARS Livestock Behavior Research Unit, West Lafayette, IN 47907, USA
J. S. Radcliffe
Affiliation:
Department of Animal Sciences, Purdue University, West Lafayette, IN 47907, USA
B. A. Craig
Affiliation:
Department of Statistics, Purdue University, West Lafayette, IN 47907, USA
S. D. Eicher
Affiliation:
USDA-ARS Livestock Behavior Research Unit, West Lafayette, IN 47907, USA
D. C. Lay Jr.
Affiliation:
USDA-ARS Livestock Behavior Research Unit, West Lafayette, IN 47907, USA
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Abstract

Heart rate variability (HRV) is a proxy measure of autonomic function and can be used as an indicator of swine stress. While traditional linear measures are used to distinguish between stressed and unstressed treatments, inclusion of nonlinear HRV measures that evaluate data structure and organization shows promise for improving HRV interpretation. The objective of this study was to evaluate the inclusion of nonlinear HRV measures in response to an acute heat episode. Twenty 12- to 14-week-old growing pigs were individually housed for 7 days and acclimated to thermoneutral conditions (20.35°C ± 0.01°C; 67.6% ± 0.2% RH) before undergoing one of the two treatments: (1) thermoneutral control (TN; n = 10 pigs) or (2) acute heat stress (HS; n = 10 pigs; 32.6°C ± 0.1°C; 26.2% ± 0.1% RH). In Phase 1 of the experimental procedure (P1; 60 min), pigs underwent a baseline HRV measurement period in thermoneutral conditions before treatment [Phase 2; P2; 60 min once gastrointestinal temperature (Tg) reached 40.6°C], where HS pigs were exposed to heated conditions and TN pigs remained in thermoneutral conditions. After P2, all pigs were moved back to thermoneutral conditions (Phase 3; P3; 60 min). During each phase, Tg data were collected every 5 min and behavioural data were collected to evaluate the amount of time each pig spent in an active posture. Additionally, linear (time and frequency domain) and nonlinear [sample entropy (SampEn), de-trended fluctuation analysis, percentage recurrence, percentage determinism (%DET), mean diagonal line length in a recurrence plot] HRV measures were quantified. Heat stressed pigs exhibited greater Tg (P = 0.002) and spent less time in an active posture compared to TN pigs during P2 (P = 0.0003). Additionally, low frequency to high frequency ratio was greater in HS pigs during P3 compared to TN pigs (P = 0.02). SampEn was reduced in HS pigs during P2 (P = 0.01) and P3 (P = 0.03) compared to TN pigs. Heat stressed pigs exhibited greater %DET during P3 (P = 0.03) and tended to have greater %DET (P = 0.09) during P2 than TN pigs. No differences between treatments were detected for the remaining HRV measures. In conclusion, linear HRV measures were largely unchanged during P2. However, changes to SampEn and %DET suggest increased heat stress as a result of the acute heat episode. Future work should continue to evaluate the benefits of including nonlinear HRV measures in HRV analysis of swine heat stress.

Keywords

animal welfareheat stressstress physiologyswine
Type
Research Article
Information
animal , Volume 14 , Issue 2 , February 2020 , pp. 379 - 387
Creative Commons
This is a work of the U.S. Government and is not subject to copyright protection in the United States.
Copyright
© The Animal Consortium 2019

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Footnotes

†

Present address: Department of Animal Sciences, North Dakota State University, Fargo, ND 58108, USA. E-mail: christopher.byrd@ndsu.edu

References

Batchinsky, AI, Cooke, WH, Kuusela, T and Cancio, C 2007. Loss of complexity characterizes the heart rate response to experimental hemorrhagic shock in swine. Critical Care Medicine 35, 519–525.10.1097/01.CCM.0000254065.44990.77CrossRefGoogle ScholarPubMed
Becker, BA, Klie, JJ, Matteri, RL, Spiers, DE, Ellersiek, M and Misfeldt, ML 1997. Endocrine and thermoregulatory responses to acute thermal exposures in 6-month-old pigs reared in different neonatal environments. Journal of Thermal Biology 22, 87–93.10.1016/S0306-4565(96)00036-8CrossRefGoogle Scholar
Billman, GE 2013. The LF/HF ratio does not accurately measure cardiac sympatho-vagal balance. Frontiers in Physiology 4, 26.10.3389/fphys.2013.00026CrossRefGoogle Scholar
Brown, TE, Beightol, LA, Koh, J and Eckberg, DL 1993. Important influence of respiration on human R-R interval power spectra is largely ignored. Journal of Applied Physiology 75, 2310–2317.10.1152/jappl.1993.75.5.2310CrossRefGoogle Scholar
Buckingham, JC 2006. Glucocorticoids: exemplars of multi-tasking. British Journal of Pharmacology 147, S258–S268.10.1038/sj.bjp.0706456CrossRefGoogle ScholarPubMed
Byrd, CJ, Craig, BA, Eicher, SD, Radcliffe, JS and Lay, DC Jr 2019. Short Communication: assessment of disbudding pain in dairy calves using nonlinear measures of heart rate variability. Journal of Dairy Science. In Press.10.3168/jds.2018-15948CrossRefGoogle Scholar
Byrd, CJ, Johnson, JS and Lay, DC Jr. 2017. Who’s stressed? Nonlinear measures of heart rate variability may provide new clues for evaluating the swine stress response. In Proceedings of the 51st Congress of the International Society for Applied Ethology, 7–10 August 2017, Aarhus, Denmark, p. 132.Google Scholar
Collin, A, Lebreton, Y, Fillaut, M, Vincent, A, Thomas, F and Herpin, P 2001. Effects of exposure to high temperature and feeding level on regional blood flow and oxidative capacity of tissues in piglets. Experimental Physiology 86, 83–91.10.1113/eph8602102CrossRefGoogle ScholarPubMed
Eckmann, JP, Oliffson Kamphorst, S and Ruelle, D 1987. Recurrence plots of dynamical systems. Europhysics Letters 4, 973–977.10.1209/0295-5075/4/9/004CrossRefGoogle Scholar
Federation of Animal Science Societies 2010. Guide for the care and use of agricultural animals in research and teaching, 3rd edition. Federation of Animal Science Societies, Champaign, IL, USA.Google Scholar
Frondelius, L, Järvenrant, K, Koponen, T and Mononen, J 2015. The effects of body posture and temperament on heart rate variability in dairy cows. Physiology & Behavior 139, 437–441.10.1016/j.physbeh.2014.12.002CrossRefGoogle ScholarPubMed
Goldberger, AL, Peng, C-K and Lipsitz, LA 2002. What is physiological complexity and how does it change with aging and disease? Neurobiology of Aging 23, 23–26.10.1016/S0197-4580(01)00266-4CrossRefGoogle ScholarPubMed
Hicks, TA, McGlone, JJ, Whisnant, CS, Kattesh, HG and Norman, RL 1998. Behavioral, endocrine, immune, and performance measures for pigs exposed to acute stress. Journal of Animal Science 76, 474–483.10.2527/1998.762474xCrossRefGoogle ScholarPubMed
Kawada, T, Sugimachi, M, Shishido, T, Miyano, H, Sato, T, Yoshimura, R, Miyashita, H, Nakahara, T, Alexander, J Jr. Sunagawa, K 1999. Simultaneous identification of static and dynamic vagosympathetic interactions in regulating heart rate. American Journal of Physiology – Regulatory Integrative and Comparative Physiology 276, R782–R789.CrossRefGoogle ScholarPubMed
Koh, J, Nakamura, Y, Tanaka, A and Kosaka, Y 1995. Spontaneous respiration should be avoided in frequency domain analysis of heart rate variability. Journal of Anesthesia 9, 229–234.10.1007/BF02479869CrossRefGoogle ScholarPubMed
Kovács, L, Kézér, FL, Jurkovich, V, Kulcsár-Huszenicza, M and Tőzsér, J 2015. Heart rate variability as an indicator of chronic stress caused by lameness in dairy cows. PLoS ONE 10, e0134792.10.1371/journal.pone.0134792CrossRefGoogle ScholarPubMed
Kuwahara, M, Yayou, K, Ishii, K, Hashimoto, S, Tsubone, H and Sugano, S 1994. Power spectral analysis of heart rate variability as a new method for assessing autonomic activity in the rat. Journal of Electrocardiology 27, 333–337.10.1016/S0022-0736(05)80272-9CrossRefGoogle ScholarPubMed
Lake, DE, Richman, JS, Griffin, MP and Moorman, JR 2002. Sample entropy analysis of neonatal heart rate variability. American Journal of Physiology – Regulatory Integrative and Comparative Physiology 283, R789–R797.10.1152/ajpregu.00069.2002CrossRefGoogle ScholarPubMed
Low, DA, Keller, DM, Wingo, JE, Brothers, RM and Crandall, CG 2011. Sympathetic nerve activity and whole body heat stress in humans. Journal of Applied Physiology 111, 1329–1334.10.1152/japplphysiol.00498.2011CrossRefGoogle ScholarPubMed
Marchant-Forde, RM, Marlin, DJ and Marchant-Forde, JN 2004. Validation of a cardiac monitor for measuring heart rate variability in adult female pigs: accuracy, artefacts and editing. Physiology & Behavior 80, 449–458.10.1016/j.physbeh.2003.09.007CrossRefGoogle ScholarPubMed
Mohr, E, Langbein, J and Nürnberg, G 2002. Heart rate variability: a noninvasive approach to measure stress in calves and cows. Physiology & Behavior 75, 251–259.10.1016/S0031-9384(01)00651-5CrossRefGoogle ScholarPubMed
Nkurikiyeyezu, KN, Suzuki, Y and Lopez, GF 2018. Heart rate variability as a predictive biomarker of thermal comfort. Journal of Ambient Intelligence and Humanized Computing 9, 1465–1477.10.1007/s12652-017-0567-4CrossRefGoogle Scholar
NRC 2012. Nutrient Requirements of Swine, 11th revised edition. Natl. Acad. Press, Washington, DC, USA Google Scholar
Parois, SP, Cabezón, FA, Schinckel, AP, Johnson, JS, Stwalley, RM and Marchant-Forde, JN 2018. Effect of floor cooling on behavior and heart rate of late lactation sows under acute heat stress. Frontiers in Veterinary Science 5, 223.CrossRefGoogle ScholarPubMed
Pincus, S 1995. Approximate entropy (ApEn) as a complexity measure. Chaos 5, 110–117.10.1063/1.166092CrossRefGoogle Scholar
Poletto, R, Janczak, AM, Marchant-Forde, RM, Marchant-Forde, JN, Matthews, DL, Dowell, CA, Hogan, DF, Freeman, LJ and Lay, DC Jr. 2011. Identification of low and high frequency ranges for heart rate variability and blood pressure analyses using pharmacological autonomic blockade with atropine and propranolol in swine. Physiology & Behavior 103, 188–196.10.1016/j.physbeh.2011.01.019CrossRefGoogle ScholarPubMed
Ross, JW, Hale, BJ, Gabler, NK, Rhoads, RP, Keating, AF and Baumgard, LH 2015. Physiological consequences of heat stress in pigs. Animal Production Science 55, 1381–1390.CrossRefGoogle Scholar
Ruis, MAW, de Groot, J, te Brake, JHA, Ekkel, ED, van de Burgwal, JA, Erkens, JHF, Engel, B, Buist, WG, Blokhuis, HJ and Koolhaas, JM 2001. Behavioural and physiological consequences of acute social defeat in growing gilts: effects of the social environment. Applied Animal Behaviour Science 70, 201–225.10.1016/S0168-1591(00)00150-7CrossRefGoogle ScholarPubMed
Sapkota, A, Herr, A, Johnson, JS and Lay, DC 2016. Core body temperature does not cool down with skin surface temperature during recovery at room temperature after acute heat stress exposure. Livestock Science 191, 143–147.10.1016/j.livsci.2016.07.010CrossRefGoogle Scholar
Sassi, R, Cerutti, S, Lombardi, F, Malik, M, Huikuri, HV, Peng, CK, Schmidt, G and Yamamoto, Y 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. EP Europace 17, 1341–1353.10.1093/europace/euv015CrossRefGoogle Scholar
Shaffer, F, McCraty, R and Zerr, CL 2014. A healthy heart is not a metronome: an integrative review of the heart’s anatomy and heart rate variability. Frontiers in Psychology 5, 1040.CrossRefGoogle Scholar
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. European Heart Journal 17, 354–381.10.1093/oxfordjournals.eurheartj.a014868CrossRefGoogle Scholar
von Borell, E, Langbein, J, Després, G, Hansen, S, Leterrier, C, Marchant-Forde, J, Marchant-Forde, R, Minero, M, Mohr, E, Prunier, A, Valance, D and Veissier, I 2007. Heart rate variability as a measure of autonomic regulation of cardiac activity for assessing stress and welfare in farm animals – a review. Physiology & Behavior 92, 293–316.10.1016/j.physbeh.2007.01.007CrossRefGoogle ScholarPubMed
Wallott, S 2017. Recurrence quantification analysis of processes and products of discourse: a tutorial in R. Discourse Processes 54, 382–405.10.1080/0163853X.2017.1297921CrossRefGoogle Scholar
Young, H and Benton, D 2015. We should be using nonlinear indices when relating heart-rate dynamics to cognition and mood. Scientific Reports 5, 16619.10.1038/srep16619CrossRefGoogle Scholar
Zhao, L, Wei, S, Zhang, C, Jiang, X, Liu, F and Liu, C 2015. Determination of sample entropy and fuzzy measure entropy parameters for distinguishing congestive heart failure from normal sinus rhythm subjects. Entropy 17, 6270–6288.CrossRefGoogle Scholar
Zupan, M, Framstad, T and Zanella, AJ 2016. Behaviour, heart rate, and heart rate variability in pigs exposed to novelty. Revista Brasileira De Zootecnia 45, 121–129.10.1590/S1806-92902016000300006CrossRefGoogle Scholar