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

Authors: BYRD, CHRISTOPHER - PURDUE UNIVERSITY; Johnson, Jay; RADCLIFFE, JOHN - PURDUE UNIVERSITY; CRAIG, BRUCE - PURDUE UNIVERSITY; EICHER, SUSAN; LAY JR, DONALD

Submitted to: Journal of Animal Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/20/2019
Publication Date: 7/12/2019
Citation: Byrd, C.J., Johnson, J.S., Radcliffe, J.S., Craig, B.A., Eicher, S.D., Lay Jr, D.C. 2019. Nonlinear analysis of heart rate variability for evaluating the growing pig stress response to an acute heat episode. Journal of Animal Science. https://doi.org/10.1017/S1751731119001630.
DOI: https://doi.org/10.1017/S1751731119001630

Interpretive Summary: Heart rate variability, or the variation in time between adjacent heart beats, is an established proxy for measuring nervous system function and is useful for evaluating the nervous system response to various stressors in livestock species. One drawback to the use of linear measures of heart rate variability stems from their inability to evaluate the nonlinear processes involved in heart rate modulation. Nonlinearity in heart rate modulation arises from the multiple physiological processes that act concurrently via the nervous system or directly on the heart to alter heart rate. As a result, the branches of the nervous system can interact with each other in a nonlinear manner (i.e. input from both branches may increase or decrease at the same time, or act in an antagonistic manner), resulting in changes to the overall structure of the heart rate signal that cannot be explained by a simple linear model of balance between the branches of the nervous system. To evaluate these nonlinear properties, nonlinear heart rate measures attempt to quantify how a stressor affects correlational and structural properties of the heart rate signal instead of linear measures such as mean or standard deviation. Several nonlinear measures have been used in human studies with varying degrees of success, and investigation of robust nonlinear measures for inclusion in heart rate variability analysis has been recommended for measuring the physiological stress response. For the swine industry, increased environmental temperature is a major source of physiological stress that negatively affects swine welfare and economic return for the producer. Specifically, increased heat load results in decreased feed intake, reduced intestinal integrity, decreased reproductive performance, and an altered immune response. Accordingly, losses due to heat stress have been estimated to reach approximately $300 million annually. With increases in global temperatures expected to continue, tools to measure the stress caused by heat are as pertinent as ever if further mitigation strategies are to be developed. Therefore, the objective of this study was to evaluate heart rate variability in response to an acute heat stress episode with particular emphasis placed on the usefulness of nonlinear measures. In response to an acute heat stress period, heat stress pigs experienced higher body temperatures and were less active than pigs housed in thermal neutral conditions. However, stress hormones and linear measures of heart rate variability were largely unaffected by acute heat exposure. Heat stressed pigs exhibited a change in some nonlinear measures of heart rate variability indicative of an increase stress response following the acute heat episode compared to pigs in thermal neutral environments. Inclusion of nonlinear heart rate variability measures may be beneficial for inclusion in studies on animal welfare and help welfare scientists to develop effective intervention strategies.

Technical Abstract: Heart rate variability (HRV) is a proxy measure of autonomic function and is commonly used as an indicator of stress in both humans and animals. While traditional linear measures are commonly used to distinguish between stressed and unstressed treatments, inclusion of additional nonlinear HRV measures that evaluate data structure and organization show promise for improving HRV interpretation following exposure to a stressor. Therefore, the objective of this study was to evaluate the inclusion of nonlinear HRV measures in response to an acute heat stress episode. Twenty, 12 to 14 wk-old growing pigs were individually housed in thermoneutral conditions and randomly allocated to 1 of 2 treatments: 1) Thermoneutral control (TN; n = 10) or 2) acute heat stress (HS; n = 10). In Phase 1 of the experimental procedure (P1), all pigs underwent a baseline HRV measurement period in thermoneutral conditions before undergoing treatment (Phase 2; P2), where HS pigs were exposed to heated conditions and TN pigs remained in thermoneutral conditions. After P2, all pigs were moved back to their home pens in thermoneutral conditions (Phase 3; P3). Gastrointestinal temperature (Tg) data were collected for each pig every 5 min. Behavioral data were collected to evaluate the amount of time each pig time spent in an active posture (sitting or standing; %). Heart rate variability measures in the time domain (RR, SDNN, RMSSD), frequency domain (LF/HF), and nonlinear measures (SampEn, DFA a1, % REC, % DET, Lmean) were quantified. Data were analyzed using Proc Glimmix in SAS 9.4. Heat stressed pigs exhibited higher Tg (P = 0.001) and were less active than TN pigs during P2 (P = 0.0003). Heat Stressed pigs exhibited higher LF/HF during P3 compared to TN pigs (P = 0.02). Sample Entropy (SampEn) was reduced in HS pigs during P2 (P = 0.007) and P3 (P = 0.03) compared to TN pigs. Overall, HS pigs exhibited higher % DET during P3 (P = 0.03) and tended to have higher % DET (P = 0.09) during phase 2 compared to TN pigs, indicating increased HR periodicity. No other differences between treatments were detected for the remaining HRV measures. In conclusion, linear HRV measures were largely unchanged as a result of acute heat exposure. However, changes to SampEn and % DET suggest increased stress as a result of the acute heat episode. Future work should continue to focus on nonlinear measures such as SampEn and % DET for regular inclusion in HRV studies on swine heat stress.