In utero heat stress alters the postnatal innate immune response of pigs

Authors: Johnson, Jay; MASKAL, JACOB - Purdue University; DUTTLINGER, ALAN - Purdue University; KPODO, KOUASSI - Purdue University; MCCONN, BETTY - Orise Fellow; BYRD, CHRISTOPHER - Purdue University; RICHERT, BRIAN - Purdue University; Marchant, Jeremy; Lay Jr, Donald; PERRY, SHELBY - University Of Missouri; LUCY, MATTHEW - University Of Missouri; SAFRANSKI, TIM - University Of Missouri

Submitted to: Journal of Animal Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/30/2020
Publication Date: 11/7/2020
Citation: Johnson, J.S., Maskal, J.M., Duttlinger, A.W., Kpodo, K.R., Mcconn, B.R., Byrd, C.J., Richert, B.T., Marchant Forde, J.N., Lay Jr, D.C., Perry, S.D., Lucy, M.C., Safranski, T.J. 2020. In utero heat stress alters the postnatal innate immune response of pigs. Journal of Animal Science. 98(12). https://doi.org/10.1093/jas/skaa356.
DOI: https://doi.org/10.1093/jas/skaa356

Interpretive Summary: In utero heat stress is associated with a variety of negative outcomes for pigs and is a growing concern for swine producers worldwide. The negative effects of in utero heat stress may be observed immediately at birth whereby piglets born to heat-stressed mothers have reduced birth weight and greater stress hormone concentrations. In addition, in utero heat stress reduces future offspring productivity, health, and welfare. Taken together, in utero heat stress may be a significant source of economic loss for the swine industry and may contribute to poor animal welfare outcomes. Although studies in pigs and cattle have described altered offspring immune function resulting from in utero heat stress, little is known regarding the impact of early gestation in utero heat stress and the immune response of pigs later in life. Therefore, the study objective was to determine the effects of early gestation in utero heat stress on the immune response of pigs subjected to an immune challenge during postnatal life. Based on previous research, our alternative hypothesis was that in utero heat stressed pigs would have a negatively altered immune response compared to controls when subjected to an immune challenge later in life. It was determined that the immune response was greater and more sensitive for in utero heat stressed pigs compared to controls. In addition, stress hormone levels and fat mobilization was greater for in utero heat stressed pigs compared to controls. In conclusion, in utero heat stress altered the postnatal cytokine, metabolic, and physiological stress response of pigs later in life, which may have negative implications towards the response of in utero heat stressed pigs to pathogens.

Technical Abstract: The effects of in utero heat stress (IUHS) range from decreased growth performance to altered behavior, but the long-term impact of IUHS on postnatal innate immune function in pigs is unknown. Therefore, the study objective was to determine the effects of early gestation IUHS on the immune, metabolic, and stress response of pigs subjected to an 8 h lipopolysaccharide (LPS) challenge during postnatal life. Twenty-four pregnant gilts were exposed to thermoneutral (TN; n = 12; 17.5 ± 2.1°C) or heat stress (HS; n = 12; cyclic 26°C to 36°C) conditions from d 6 to 59 of gestation, and then TN conditions (20.9 ± 2.3°C) from d 60 of gestation to farrowing. At 12 wks of age, 16 IUHS and 16 in utero thermoneutral (IUTN) pigs were selected, balanced by sex and given an intravenous injection of LPS (2 µg/kg BW mixed with saline and injected at 2 µl/kg BW) or saline (SAL; 2 µl/kg BW). Body temperature was monitored every 30 min and blood was obtained at 0, 1, 2, 3, 4, 6, and 8 h following the LPS challenge. Blood samples were analyzed for glucose, insulin, non-esterified fatty acids (NEFA), cortisol, and cytokine concentrations. In addition, white blood cell counts were determined at 0 h and 4 h. Hour 0 data were used as covariates in all analyses. Body temperature was increased (P < 0.01) in LPS (40.88 ± 0.08°C) versus SAL (39.83 ± 0.08°C) pigs. Eosinophils tended to be decreased (P = 0.09; 43.9%) in IUHS versus IUTN pigs, regardless of LPS treatment. Glucose concentrations were reduced overall (P = 0.05; 5.9%) in IUHS versus IUTN pigs. The NEFA concentrations tended to be greater (P = 0.07; 143.4%) in IUHS-LPS pigs compared to all other treatments, and IUTN-LPS pigs tended to have greater (127.4%) circulating NEFA concentrations compared to IUTN-SAL and IUHS-SAL pigs. Cortisol was increased (P = 0.04) in IUHS-LPS compared to IUTN-LPS pigs at 3 h (21.5%) and 4 h (64.3%). At 1 h, TNFa was increased (P = 0.01; 115.1%) in IUHS-LPS compared to IUTN-LPS pigs. Overall, IL-1ß and IL-6 were greater (P < 0.04; 281.3 and 297.8%, respectively) in IUHS-LPS pigs compared to all other treatments, and IUTN-LPS pigs had increased IL-1ß and IL-6 concentrations compared to IUTN-SAL and IUHS-SAL pigs. In summary, IUHS altered the postnatal cytokine, metabolic, and physiological stress response of pigs during postnatal life, which may have negative implications towards the response of IUHS pigs to pathogens.