Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-19T17:30:01.777Z Has data issue: false hasContentIssue false
  • English
  • Français

Behavioural, endocrine and immune responses to repeated social stress in pregnant gilts

Published online by Cambridge University Press:  01 January 2009

D. Couret ,
W. Otten ,
B. Puppe ,
A. Prunier  and
E. Merlot
D. Couret*
Affiliation:
INRA, UMR1079, Systèmes d’Elevage Nutrition Animale et Humaine, F-35000 Rennes, France Agrocampus Rennes, UMR1079, SENAH, F-35000 Rennes, France
W. Otten
Affiliation:
Behavioural Physiology Research Unit, Research Institute for the Biology of Farm Animals, Wilhelm-Stahl-Allee 2, 18196 Dummerstorf, Germany
B. Puppe
Affiliation:
Behavioural Physiology Research Unit, Research Institute for the Biology of Farm Animals, Wilhelm-Stahl-Allee 2, 18196 Dummerstorf, Germany
A. Prunier
Affiliation:
INRA, UMR1079, Systèmes d’Elevage Nutrition Animale et Humaine, F-35000 Rennes, France Agrocampus Rennes, UMR1079, SENAH, F-35000 Rennes, France
E. Merlot
Affiliation:
INRA, UMR1079, Systèmes d’Elevage Nutrition Animale et Humaine, F-35000 Rennes, France Agrocampus Rennes, UMR1079, SENAH, F-35000 Rennes, France
*
E-mail: [email protected]
Get access

Abstract

Pregnant sows are exposed to various stressors in intensive pig husbandry that may have negative consequences on their health, reproductive performances and welfare. Social stress is one of these challenges, because gestating sows have to be housed in groups according to EU guidelines (2001/88/CE). The purpose of this study was to determine the consequences of repeated social stress in pregnant female pigs on their behavioural, endocrine and immunological responses and on pregnancy outcome. Pregnant gilts were submitted to a repeated social stress procedure induced by housing unfamiliar gilts in pairs changed twice a week between days 77 and 105 of gestation (S group, n = 18). Control gilts were housed in stable pairs during the same period (C group, n = 18). Agonistic behaviour was observed during the first 3 h after each grouping. Skin lesions were numbered 2 h after each grouping. Salivary cortisol was measured before and repeatedly during the 4 weeks of grouping. Gilts were immunized against keyhole limpet haemocyanin (KLH) on days 81 and 95 of gestation. Immunoglobulins G against KLH, proliferative responses to concanavalin A, lipopolysaccharide, pokeweed mitogen and KLH and peripheral blood leukocyte numbers were evaluated 1 week before the first grouping and 3 days after the last one. Agonistic interactions and skin lesions were observed in S gilts at each grouping, although there was a decline between the first and the last grouping (P < 0.05). The repeated social stress induced a sustained endocrine response as shown by elevated salivary cortisol levels from 1 to 48 h after grouping in S gilts compared to C gilts. The cellular as well as the humoral immunity and the leukocyte numbers were not influenced by social stress. Gestation length tended to be shorter in S gilts (P = 0.09), but litter size, piglet weight or mortality at birth were not affected. Variability of the response of S gilts to groupings was partly explained by their average success value determined according to the outcome (defeat or win) of all the groupings. In conclusion, our study demonstrates that the application of repeated social stress to pregnant gilts during the last third of their gestation repeatedly activates their hypothalamo–pituitary–adrenal axis but does not impair their immune function and pregnancy outcome.

Keywords

cortisolimmunitypigsocial stresspregnancy
Type
Full Paper
Information
animal , Volume 3 , Issue 1 , January 2009 , pp. 118 - 127
Copyright
Copyright © The Animal Consortium 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Arck, PC 2001. Stress and pregnancy loss: role of immune mediators, hormones and neurotransmitters. American Journal of Reproductive Immunology 46, 117–123.CrossRefGoogle ScholarPubMed
Barbazanges, A, Piazza, PV, Le Moal, M, Maccari, S 1996. Maternal glucocorticoid secretion mediates long-term effects of prenatal stress. Journal of Neuroscience 16, 3943–3949.CrossRefGoogle ScholarPubMed
Bartolomucci, A 2007. Social stress, immune functions and diseases in rodents. Frontiers in Neuroendocrinology 28, 28–49.CrossRefGoogle ScholarPubMed
Bohus, B, Koolhaas, JM, De Ruiter, AJH, Heijnen, CJ 1991. Stress and differential alterations in immune system functions: conclusions from social stress studies in animals. Netherlands Journal of Medicine 39, 306–315.Google ScholarPubMed
Bolhuis, JE, Schouten, WG, De Leeuw, JA, Schrama, JW, Wiegant, VM 2004. Individual coping characteristics, rearing conditions and behavioural flexibility in pigs. Behavioural Brain Research 152, 351–360.CrossRefGoogle ScholarPubMed
Coussons-Read, ME, Okun, ML, Nettles, CD 2007. Psychosocial stress increases inflammatory markers and alters cytokine production across pregnancy. Brain, Behaviour, and Immunity 21, 343–350.CrossRefGoogle ScholarPubMed
Coutellier, L, Arnould, C, Boissy, A, Orgeur, P, Prunier, A, Veissier, I, Meunier-Salaün, MC 2007. Pig’s responses to repeated social regrouping and relocation during the growing-finishing period. Applied Animal Behaviour Science 105, 102–115.CrossRefGoogle Scholar
De Groot, J, Ruis, MAW, Scholten, JW, Koolhaas, JM, Boersma, WJA 2001. Long-term effects of social stress on antiviral immunity in pigs. Physiology and Behavior 73, 145–158.CrossRefGoogle ScholarPubMed
Elenkov, IJ 2004. Glucocorticoids and the Th1/Th2 balance. Annals of the New York Academy of Sciences 1024, 138–146.CrossRefGoogle ScholarPubMed
Ewbank, R, Meese, GB 1971. Aggressive behaviour in groups of domesticated pigs on removal and return of individuals. Animal Production 13, 685–693.Google Scholar
Fowden, AL, Dino, AG, Forhead, AJ 2006. Intrauterine programming of physiological systems: causes and consequences. Physiology 21, 29–37.CrossRefGoogle ScholarPubMed
Giersing, M, Andersson, A 1998. How does former acquaintance affect aggressive behaviour in repeatedly mixed male and female pigs? Applied Animal Behaviour Science 59, 297–306.CrossRefGoogle Scholar
Haussmann, MF, Carroll, JA, Weesner, GD, Daniels, MJ, Matteri, RL, Lay, DC 2000. Administration of ACTH to restrained, pregnant sows alters their pigs’ hypothalamic-pituitary-adrenal (HPA) axis. Journal of Animal Science 78, 2399–2411.CrossRefGoogle ScholarPubMed
Jarvis, S, Moinard, C, Robson, SK, Baxter, E, Ormandy, E, Douglas, AJ, Seckl, JR, Russell, JA, Lawrence, AB 2006. Programming the offspring of the pig by prenatal social stress: neuroendocrine activity and behaviour. Hormones and Behavior 49, 68–80.CrossRefGoogle ScholarPubMed
Joachim, R, Zenclussen, AC, Polgar, B, Douglas, AJ, Fest, S, Knackstedt, M, Klapp, BF, Arck, PC 2003. The progesterone derivative dydrogesterone abrogates murine stress-triggered abortion by inducing a Th2 biased local immune. Steroids 68, 931–940.CrossRefGoogle ScholarPubMed
Kanitz, E, Tuchscherer, M, Puppe, B, Tuchscherer, A, Stabenow, B 2004. Consequences of repeated early isolation in domestic piglets (Sus scrofa) on their behavioural, neuroendocrine, and immunological responses. Brain, Behaviour, and Immunity 18, 35–45.CrossRefGoogle ScholarPubMed
Kanitz, E, Otten, W, Tuchscherer, M 2006. Changes in endocrine and neurochemical profiles in neonatal pigs prenatally exposed to increased maternal cortisol. Journal of Endocrinology 191, 207–220.CrossRefGoogle ScholarPubMed
Kranendonk, G, Hopster, H, Fillerup, M, Ekkel, ED, Mulder, EJH, Wiegant, VM, Taverne, MAM 2006. Lower birth weight and attenuated adrenocortical response to ACTH in offspring from sows that orally received cortisol during gestation. Domestic Animal Endocrinology 30, 218–238.CrossRefGoogle ScholarPubMed
McGlone, JJ, Salak, JL, Lumpkin, EA, Nicholson, RI, Gibson, M, Norman, RL 1993. Shipping stress and social status effects on pig performance, plasma cortisol, natural killer cell activity, and leukocyte numbers. Journal of Animal Science 71, 888–896.CrossRefGoogle ScholarPubMed
Meese, GB, Ewbank, R 1972. A note on instability of the dominance hierarchy and variations in level of aggression within groups of fattening pigs. Animal Production 14, 359–362.Google Scholar
Mendl, M, Zanella, AJ, Broom, DM 1992. Physiological and reproductive correlates of behavioural strategies in female domestic pigs. Animal Behaviour 44, 1107–1121.CrossRefGoogle Scholar
Merlot, E, Couret, D, Otten, W 2008. Prenatal stress, fetal imprinting and immunity. Brain, Behavior, and Immunity 22, 42–51.CrossRefGoogle ScholarPubMed
Neumann, ID, Johnstone, HA, Hatzinger, M, Liebsch, G, Shipston, M, Russell, JA, Landgraf, R, and Douglas, AJ 1998. Attenuated neuroendocrine responses to emotional and physical stressors in pregnant rats involve adenohypophysial changes. Journal of Physiology 508, 289–300.CrossRefGoogle ScholarPubMed
Niekamp, SR, Sutherland, MA, Dahl, GE, Salak-Johnson, JL 2007. Immune responses of piglets to weaning stress: impact of photoperiod. Journal of Animal Science 85, 93–100.CrossRefGoogle ScholarPubMed
Olsson, IAS, De Jonge, FH, Schuurman, T, Helmond, FA 1999. Poor rearing conditions and social stress in pigs: repeated social challenge and the effect on behavioural and physiological responses to stressors. Behavioural Processes 46, 201–215.CrossRefGoogle ScholarPubMed
Otten, W, Puppe, B, Stabenow, B, Kanitz, E, Schön, PC, Brüssow, KP, Nürnberg, G 1997. Agonistic interactions and physiological reactions of top- and bottom-ranking pigs confronted with a familiar and an unfamiliar group: preliminary results. Applied Animal Behaviour Science 55, 79–90.CrossRefGoogle Scholar
Otten, W, Puppe, B, Kanitz, E, Schön, PC, Stabenow, B 2002. Physiological and behavioral effects of different success during social confrontation in pigs with prior dominance experience. Physiology and Behaviour 75, 127–133.CrossRefGoogle ScholarPubMed
Puppe, B 1998. Effects of familiarity and relatedness on agonistic pair relationships in newly mixed domestic pigs. Applied Animal Behaviour Science 58, 233–239.CrossRefGoogle Scholar
Puppe, B, Langbein, J, Bauer, J, Hoy, S 2008. A comparative view on social hierarchy formation at different stages of pig production using sociometric measures. Livestock Science 113, 155–162.CrossRefGoogle Scholar
Salak-Johnson, JL, McGlone, JJ 2007. Making sense of apparently conflicting data: stress and immunity in swine and cattle. Journal of Animal Science 85, 81–88.CrossRefGoogle ScholarPubMed
Salak-Johnson, JL, McGlone, JJ, Norman, RL 1996. In vivo glucocorticoid effects on porcine natural killer cell activity and circulating leukocytes. Journal of Animal Science 74, 584–592.CrossRefGoogle ScholarPubMed
Schouten, WG, Wiegant, VM 1997. Individual responses to acute and chronic stress in pigs. Acta Physiologica Scandinavica Supplementum 640, 88–91.Google ScholarPubMed
Schrama, JW, Schouten, JM, Swinkels, JWGM, Gentry, JL, De Vries Reilingh, G, Parmentier, HK 1997. Effect of hemoglobin status on humoral immune response of weanling pigs differing in coping styles. Journal of Animal Science 75, 2588–2596.CrossRefGoogle ScholarPubMed
Soede, NM, Van Sleuwen, MJW, Molenaar, R, Rietveld, FW, Schouten, WPG, Hazeleger, W, Kemp, B 2006. Influence of repeated regrouping on reproduction in gilts. Animal Reproduction Science 96, 133–145.CrossRefGoogle ScholarPubMed
Soede, NM, Roelofs, JB, Verheijen, RJ, Schouten, WP, Hazeleger, W, Kemp, B 2007. Effect of repeated stress treatments during the follicular phase and early pregnancy on reproductive performance of gilts. Reproduction in Domestic Animal 42, 135–142.CrossRefGoogle ScholarPubMed
Statistical Analysis Systems Institute 1999. Statistical analysis systems, released 8.01. Statistical Analysis Systems Institute Inc., Cary, NC, USA.Google Scholar
Stefansky, V, Raabe, C, Schulte, M 2005. Pregnancy and social stress in female rats: influences on blood leukocytes and corticosterone concentrations. Journal of Neuroimmunology 162, 81–88.CrossRefGoogle Scholar
Tsuma, VT, Einarsson, S, Madej, A, Kindahl, H, Lundeheim, N, Rojkittikhun, T 1996. Endocrine changes during group housing of primiparous sows in early pregnancy. Acta Veterinaria Scandinavica 37, 481–489.CrossRefGoogle ScholarPubMed
Tuchscherer, M, Puppe, B, Tuchscherer, A, Kanitz, E 1998. Effects of social status after grouping on immune, metabolic and endocrine responses in pigs. Physiology and Behavior 64, 353–360.CrossRefGoogle ScholarPubMed
Tuchscherer, M, Kanitz, E, Otten, W, Tuchscherer, A 2002. Effects of prenatal stress on cellular and humoral immune responses in neonatal pigs. Veterinary Immunology and Immunopathology 86, 195–203.CrossRefGoogle ScholarPubMed
Von Borell, E, Dobson, H, Prunier, A 2007. Stress, behaviour and reproductive performance in female cattle and pigs. Hormones and Behavior 52, 130–138.CrossRefGoogle ScholarPubMed
Wegmann, TG, Lin, H, Guilbert, L, Mosmann, TR 1993. Bidirectional cytokine interactions in the maternal–fetal relationship: is successful pregnancy a Th2 phenomenon? Immunology Today 14, 353–356.CrossRefGoogle ScholarPubMed
Weinstock, M 1997. Does prenatal stress impair coping and regulation of hypothalamo–pituitary–adrenal axis? Neuroscience and Biobehavioral Reviews 21, 1–10.CrossRefGoogle Scholar
Wiebold, JL, Stanfield, PH, Becker, WC, Hillers, JK 1986. The effect of restraint stress in early pregnancy in mice. Journal of Reproduction and Fertility 78, 185–192.CrossRefGoogle ScholarPubMed
Yang, WC, Schultz, RD 1986. Effect of corticosteroids on porcine leukocytes: age-related effects of corticosteroid inhibition on porcine lymphocyte responses to mitogens. Veterinary Immunology and Immunopathology 13, 19–29.CrossRefGoogle ScholarPubMed