Skip to main content Accessibility help
×
Home

The impact of pre-natal stress on offspring development in pigs

  • W. OTTEN (a1), E. KANITZ (a1) and M. TUCHSCHERER (a1)

Summary

In farm animals, restricted housing conditions or inadequate management practices during gestation may be potential stressors for the mother, with possible consequences on the growth, vitality, health and welfare of the dam and its offspring, and thus can have economic as well as ethical implications. The current review summarizes data from studies in pigs on the impact of maternal stress during gestation on the litter characteristics and phenotypic traits of offspring. The outcomes from the different experimental models using either maternal stress paradigms or artificially increased maternal cortisol are presented, and possible reasons for the consistent or divergent results are discussed. Maternal stress models are of particular importance, because social stress, restraint, rough handling and heat or cold stress are of practical relevance during housing of pregnant sows, whereas in other models the specific role of maternal cortisol as a mediator for pre-natal stress is studied. The data reveal that pre-natal stress in pigs can impair growth and modify the immune function, stress reactivity and behaviour of offspring. There is evidence that the materno-foetal cortisol regulation is a major determinant of the alterations in offspring. Neuroendocrine and behavioural data in the offspring indicate that pre-natally stressed pigs can express a modified phenotype characterized by increased reactivity of the hypothalamic–pituitary–adrenal axis, altered emotionality, more fearfulness in a novel environment and disturbed social and maternal behaviour. Further research is needed and should focus on the long-term consequences on immune function, reproductive traits and maternal behaviour in female offspring used as breeding animals.

Copyright

Corresponding author

*To whom all correspondence should be addressed. Email: otten@fbn-dummerstorf.de

References

Hide All
Ashworth, C. J., Hogg, C. O., Hoeks, C. W., Donald, R. D., Duncan, W. C., Lawrence, A. B. & Rutherford, K. M. (2011). Pre-natal social stress and post-natal pain affect the developing pig reproductive axis. Reproduction 142, 907914.
Backus, B. L., Bryer, P. J. & Sutherland, M. A. (2013). Prenatal stress and ketamine affect the behavioural and physiological responsiveness of early adolescent pigs to a novel arena and social confrontation test. Applied Animal Behaviour Science 145, 6069.
Barbazanges, A., Piazza, P. V., Le Moal, M. & Maccari, S. (1996). Maternal glucocorticoid secretion mediates long-term effects of prenatal stress. Journal of Neuroscience 16, 39433949.
Bate, L. A. & Hacker, R. R. (1985 a). The influence of the sow's adrenal activity on the ability of the piglet to absorb IgG from colostrum. Canadian Journal of Animal Science 65, 7785.
Bate, L. A. & Hacker, R. R. (1985 b). Influence of environmental temperature during late gestation and soon after birth on IgG absorption by newborn piglets. Canadian Journal of Animal Science 65, 8793.
Bate, L. A., Ireland, W., Connell, B. J. & Grimmelt, B. (1991). Development of the small intestine of piglets in response to prenatal elevation of glucocorticoids. Histology and Histopathology 6, 207216.
Baxter, E. M., Jarvis, S., Palarea-Albaladejo, J. & Edwards, S. A. (2012). The weaker sex? The propensity for male-biased piglet mortality. PLoS ONE 7, e30318.
Brüssow, K. P., Schneider, F., Kanitz, E., Otten, W. & Tuchscherer, M. (2005). Alteration of reproductive hormone levels in pregnant sows induced by repeated ACTH application and its possible influence on pre- and post-natal hormone secretion of piglets. Journal of Reproduction and Development 51, 133142.
Collier, C. T., Williams, P. N., Carroll, J. A., Welsh, T. H. Jr. & Laurenz, J. C. (2011). Effect of maternal restraint stress during gestation on temporal lipopolysaccharide-induced neuroendocrine and immune responses of progeny. Domestic Animal Endocrinology 40, 4050.
Couret, D., Otten, W., Puppe, B., Prunier, A. & Merlot, E. (2009 a). Behavioural, endocrine and immune responses to repeated social stress in pregnant gilts. Animal 3, 118127.
Couret, D., Prunier, A., Mounier, A. M., Thomas, F., Oswald, I. P. & Merlot, E. (2009 b). Comparative effects of a prenatal stress occurring during early or late gestation on pig immune response. Physiology and Behavior 98, 498504.
Couret, D., Jamin, A., Kuntz-Simon, G., Prunier, A. & Merlot, E. (2009 c). Maternal stress during late gestation has moderate but long-lasting effects on the immune system of the piglets. Veterinary Immunology and Immunopathology 131, 1724.
De Groot, J., Kranendonk, G., Fillerup, M., Hopster, H., Boersma, W., Hodgson, D., Van Reenen, K. & Taverne, M. (2007). Response to LPS in female offspring from sows treated with cortisol during pregnancy. Physiology and Behavior 90, 612618.
English, P. R., Smith, W. J. & MacLean, A. (1977). The Sow – Improving her Efficiency. Ipswich: Farming Press.
Fowden, A. L. & Forhead, A. J. (2004). Endocrine mechanisms of intrauterine programming. Reproduction 127, 515526.
Fowden, A. L., Giussani, D. A. & Forhead, A. J. (2006). Intrauterine programming of physiological systems: causes and consequences. Physiology 21, 2937.
Gu, W. & Jones, C. T. (1986). The effect of elevation of maternal plasma catecholamines on the fetus and placenta of the pregnant sheep. Journal of Developmental Physiology 8, 173186.
Harris, A. & Seckl, J. (2011). Glucocorticoids, prenatal stress and the programming of disease. Hormones and Behavior 59, 279289.
Haussmann, M. F., Carroll, J. A., Weesner, G. D., Daniels, M. J., Matteri, R. L. & Lay, D. C. Jr. (2000). Administration of ACTH to restrained, pregnant sows alters their pigs’ hypothalamic-pituitary-adrenal (HPA) axis. Journal of Animal Science 78, 23992411.
Ison, S. H., D'Eath, R. B., Robson, S. K., Baxter, E. M., Ormandy, E., Douglas, A. J., Russell, J. A., Lawrence, A. B. & Jarvis, S. (2010). ‘Subordination style’ in pigs? The response of pregnant sows to mixing stress affects their offspring's behaviour and stress reactivity. Applied Animal Behaviour Science 124, 1627.
Ison, S. H., Donald, R. D., Jarvis, S., Robson, S. K., Lawrence, A. B. & Rutherford, K. M. D. (2014). Behavioral and physiological responses of primiparous sows to mixing with older, unfamiliar sows. Journal of Animal Science 92, 16471655.
Jarvis, S., Moinard, C., Robson, S. K., Baxter, E., Ormandy, E., Douglas, A. J., Seckl, J. R., Russell, J. A. & Lawrence, A. B. (2006). Programming the offspring of the pig by prenatal social stress: neuroendocrine activity and behaviour. Hormones and Behavior 49, 6880.
Kanitz, E., Otten, W., Tuchscherer, M. & Manteuffel, G. (2003). Effects of prenatal stress on corticosteroid receptors and monoamine concentrations in limbic areas of suckling piglets (Sus scrofa) at different ages. Journal of Veterinary Medicine A: Physiology, Pathology and Clinical Medicine 50, 132139.
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, 207220.
Kapoor, A. & Matthews, S. G. (2011). Testosterone is involved in mediating the effects of prenatal stress in male guinea pig offspring. Journal of Physiology 589, 755766.
Kattesh, H. G., Kornegay, E. T., Gwazdauskas, F. C., Knight, J. W. & Thomas, H. R. (1979). Peripheral plasma testosterone concentration and sexual behavior in young prenatally stressed boars. Theriogenology 12, 289305.
Kattesh, H. G., Kornegay, E. T., Knight, J. W., Gwazdauskas, F. G., Thomas, H. R. & Notter, D. R. (1980). Glucocorticoid concentrations, corticosteroid binding protein characteristics and reproduction performance of sows and gilts subjected to applied stress during mid-gestation. Journal of Animal Science 50, 897905.
Klemcke, H. G. (1995). Placental metabolism of cortisol at mid- and late gestation in swine. Biology of Reproduction 53, 12931301.
Klemcke, H. G. & Christenson, R. K. (1996). Porcine placental 11β-hydroxysteroid dehydrogenase activity. Biology of Reproduction 55, 217223.
Klemcke, H. G. & Christenson, R. K. (1997). Porcine fetal and maternal adrenocorticotropic hormone and corticosteroid concentrations during gestation and their relation to fetal size. Biology of Reproduction 57, 99106.
Kranendonk, G., Hopster, H., Van Eerdenburg, F., Van Reenen, K., Fillerup, M., De Groot, J., Korte, M. & Taverne, M. (2005). Evaluation of oral administration of cortisol as a model for prenatal stress in pregnant sows. American Journal of Veterinary Research 66, 780790.
Kranendonk, G., Hopster, H., Fillerup, M., Ekkel, E. D., Mulder, E. J., Wiegant, V. M. & Taverne, M. A. (2006 a). Lower birth weight and attenuated adrenocortical response to ACTH in offspring from sows that orally received cortisol during gestation. Domestic Animal Endocrinology 30, 218238.
Kranendonk, G., Hopster, H., Fillerup, M., Ekkel, E. D., Mulder, E. J. & Taverne, M. A. (2006 b). Cortisol administration to pregnant sows affects novelty-induced locomotion, aggressive behaviour, and blunts gender differences in their offspring. Hormones and Behavior 49, 663672.
Kranendonk, G., Van der Mheen, H., Fillerup, M. & Hopster, H. (2007). Social rank of pregnant sows affects their body weight gain and behavior and performance of the offspring. Journal of Animal Science 85, 420429.
Kranendonk, G., Mulder, E. J., Parvizi, N. & Taverne, M. A. (2008). Prenatal stress in pigs: experimental approaches and field observations. Experimental and Clinical Endocrinology and Diabetes 116, 413422.
Lay, D. C. Jr., Kattesh, H. G., Cunnick, J. E., Daniels, M. J., McMunn, K. A., Toscano, M. J. & Roberts, M. P. (2008). Prenatal stress effects on pig development and response to weaning. Journal of Animal Science 86, 13161324.
Lay, D. C. Jr., Kattesh, H. G., Cunnick, J. E., Daniels, M. J., Kranendonk, G., McMunn, K. A., Toscano, M. J. & Roberts, M. P. (2011). Effect of prenatal stress on subsequent response to mixing stress and a lipopolysaccharide challenge in pigs. Journal of Animal Science 89, 17871794.
Machado-Neto, R., Graves, C. N. & Curtis, S. E. (1987). Immunoglobulins in piglets from sows heat-stressed prepartum. Journal of Animal Science 65, 445455.
Mack, L. A., Lay, D. C. Jr., Eicher, S. D., Johnson, A. K., Richert, B. T. & Pajor, E. A. (2014). Growth and reproductive development of male piglets are more vulnerable to midgestation maternal stress than that of female piglets. Journal of Animal Science 92, 530548.
Mairesse, J., Lesage, J., Breton, C., Bréant, B., Hahn, T., Darnaudéry, M., Dickson, S. L., Seckl, J., Blondeau, B., Vieau, D., Maccari, S. & Viltart, O. (2007). Maternal stress alters endocrine function of the feto-placental unit in rats. American Journal of Physiology–Endocrinology and Metabolism 292, E1526E1533.
McPherson, R. L., Ji, F., Wu, G., Blanton, J. R. Jr. & Kim, S. W. (2004). Growth and compositional changes of fetal tissues in pigs. Journal of Animal Science 82, 25342540.
Merlot, E., Couret, D. & Otten, W. (2008). Prenatal stress, fetal imprinting and immunity. Brain, Behavior, and Immunity 22, 4251.
Mueller, B. R. & Bale, T. L. (2008). Sex-specific programming of offspring emotionality after stress early in pregnancy. Journal of Neuroscience 28, 90559065.
O'Gorman, C. W., Gonzales, E., Eaton, M. D., Collard, K. A., Reyna, M., Laurenz, J. C., Stanko, R. L., Keisler, D. H., Carroll, J. A. & Garcia, M. R. (2007). Fetal exposure to maternal stress influences leptin receptor gene expression during development and age at puberty in gilts (abstract). Journal of Animal Science 85 (Suppl. 2), 13.
Otten, W., Kanitz, E., Tuchscherer, M. & Nürnberg, G. (2001). Effects of prenatal restraint stress on hypothalamic–pituitary–adrenocortical and sympatho-adrenomedullary axis in neonatal pigs. Animal Science 73, 279287.
Otten, W., Kanitz, E., Tuchscherer, M., Schneider, F. & Brüssow, K. P. (2004). Effects of adrenocorticotropin stimulation on cortisol dynamics of pregnant gilts and their fetuses: implications for prenatal stress studies. Theriogenology 61, 16491659.
Otten, W., Kanitz, E., Tuchscherer, M., Puppe, B. & Nürnberg, G. (2007 a). Repeated administrations of adrenocorticotropic hormone during gestation in gilts: effects on growth, behaviour and immune responses of their piglets. Livestock Science 106, 261270.
Otten, W., Kanitz, E., Tuchscherer, M., Puppe, B. & Gimsa, U. (2007 b). Repeated administrations of ACTH during late gestation in pigs: effects on HPA axis, brain neurotransmitter systems, behaviour and immune responses in the offspring. Experimental Dermatology 16, 368369.
Otten, W., Kanitz, E., Tuchscherer, M., Brüssow, K. P. & Nürnberg, G. (2008). Repeated administrations of adrenocorticotropic hormone during late gestation in pigs: maternal cortisol response and effects on fetal HPA axis and brain neurotransmitter systems. Theriogenology 69, 312322.
Otten, W., Kanitz, E., Couret, D., Veissier, I., Prunier, A. & Merlot, E. (2010). Maternal social stress during late pregnancy affects hypothalamic–pituitary–adrenal function and brain neurotransmitter systems in pig offspring. Domestic Animal Endocrinology 38, 146156.
Pena, C. J., Monk, C. & Champagne, F. A. (2012). Epigenetic effects of prenatal stress on 11ß-hydroxysteroid dehydrogenase-2 in the placenta and fetal brain. PLoS ONE 7, e39791.
Ranger, M., Johnston, C. C. & Anand, K. J. S. (2007). Current controversies regarding pain assessment in neonates. Seminars in Perinatology 31, 283288.
Rault, J. L., Mack, L. A., Carter, C. S., Garner, J. P., Marchant-Forde, J. N., Richert, B. T. & Lay, D. C. Jr. (2013). Prenatal stress puzzle, the oxytocin piece: prenatal stress alters the behaviour and autonomic regulation in piglets, insights from oxytocin. Applied Animal Behaviour Science 148, 99107.
Rutherford, K. M., Robson, S. K., Donald, R. D., Jarvis, S., Sandercock, D. A., Scott, E. M., Nolan, A. M. & Lawrence, A. B. (2009). Pre-natal stress amplifies the immediate behavioural responses to acute pain in piglets. Biology Letters 5, 452454.
Rutherford, K. M. D., Piastowska-Ciesielska, A., Donald, R. D., Robson, S. K., Ison, S. H., Jarvis, S., Brunton, P. J., Russell, J. A. & Lawrence, A. B. (2014). Prenatal stress produces anxiety prone female offspring and impaired maternal behaviour in the domestic pig. Physiology and Behavior 129, 255264.
Sandercock, D. A., Gibson, I. F., Rutherford, K. M., Donald, R. D., Lawrence, A. B., Brash, H. M., Scott, E. M. & Nolan, A. M. (2011). The impact of prenatal stress on basal nociception and evoked responses to tail-docking and inflammatory challenge in juvenile pigs. Physiology and Behavior 104, 728737.
Sarkar, S., Tsai, S.-W., Nguyen, T. T., Plevyak, M., Padbury, J. F. & Rubin, L. P. (2001). Inhibition of placental 11β-hydroxysteroid dehydrogenase type 2 by catecholamines via α-adrenergic signaling. American Journal of Physiology–Regulatory, Integrative, and Comparative Physiology 281, R1966R1974.
Schwerin, M., Kanitz, E., Tuchscherer, M., Brüssow, K. P., Nürnberg, G. & Otten, W. (2005). Stress-related gene expression in brain and adrenal gland of porcine fetuses and neonates. Theriogenology 63, 12201234.
Šinkora, M. & Butler, J. E. (2009). The ontogeny of the porcine immune system. Developmental and Comparative Immunology 33, 273283.
Stevens, A. D. & Lumbers, E. R. (1995). Effects of intravenous infusions of noradrenaline into the pregnant ewe on uterine blood-flow, function, and lung liquid flow. Canadian Journal of Physiology and Pharmacology 73, 202208.
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, 195203.
Viltart, O. & Vanbesien-Mailliot, C. C. A. (2007). Impact of prenatal stress on neuroendocrine programming. Scientific World Journal 7, 14931537.
Ward, I. L. & Weisz, J. (1984). Differential effects of maternal stress on circulating levels of corticosterone, progesterone, and testosterone in male and female rat fetuses and their mothers. Endocrinology 114, 16351644.
Welsh, M., Saunders, P. T. K., Fisken, M., Scott, H. M., Hutchison, G. R., Smith, L. B. & Sharpe, R. M. (2008). Identification in rats of a programming window for reproductive tract masculinization, disruption of which leads to hypospadias and cryptorchidism. Journal of Clinical Investigation 118, 14791490.
Xiong, F. & Zhang, L. (2013). Role of the hypothalamic–pituitary–adrenal axis in developmental programming of health and disease. Frontiers in Neuroendocrinology 34, 2746.

Related content

Powered by UNSILO

The impact of pre-natal stress on offspring development in pigs

  • W. OTTEN (a1), E. KANITZ (a1) and M. TUCHSCHERER (a1)

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.