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Effects of prenatal restraint stress on hypothalamic-pituitary-adrenocortical and sympatho-adrenomedullary axis in neonatal pigs

Published online by Cambridge University Press:  18 August 2016

W. Often ,
E. Kanitz ,
M. Tuchscherer  and
G. Nürnberg
W. Often*
Affiliation:
Research Unit Behavioural Physiology;
E. Kanitz
Affiliation:
Research Unit Behavioural Physiology;
M. Tuchscherer
Affiliation:
Research Unit Behavioural Physiology;
G. Nürnberg
Affiliation:
Research Unit Genetics and Biometry; Research Institute for the Biology of Farm Animals, 18196 Dummerstorf Germany
*
E-mail:[email protected]
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Abstract

Studies in rodents and primates strongly indicate that prenatal stress affects the survival, behaviour and physiology of the offspring. Stressful stimuli during gestation may have a direct or hormone mediated effect on the development of stress systems in the foetal organism, resulting in an altered coping during stressful situations. The present study was conducted to elucidate prenatal stress effects in domestic pigs on the responses of the hypothalamicpituitary- adrenocortical (HPA) axis and the sympatho-adrenomedullary (SAM) system as well as on morbidity, mortality and growth of the offspring. Pregnant sows were subjected to a restraint stress for five minutes daily during the last five weeks of gestation. Endocrine reactions of the piglets were tested at 3, 7, 21 and 35 days of age using an immobilization test and an ACTH challenge test. Prenatally stressed piglets showed lower basal plasma cortisol and increased corticosteroid binding globulin (CBG) concentrations at 3 days of age, indicating decreased free cortisol concentrations after birth. Cortisol levels after ACTH stimulation and catecholamine levels after immobilization were not affected by the stress treatment of the sows. Piglets from stressed sows tended to have lower noradrenaline : adrenaline ratios at three days of age compared with the control piglets. In addition, stressed sows tended to have lower litter weights after birth. The morbidity and mortality during the suckling period was higher in the prenatally stressed litters, as shown by a higher frequency of diseased and perished piglets per litter. We suppose that prenatal stress during late gestation in pigs alters the development of the HPA system and impairs the vitality of the offspring.

Keywords

epinephrinehydrocortisonenorepinephrinepigsstress
Type
Non-ruminant, nutrition, behaviour and production
Information
Animal Science , Volume 73 , Issue 2 , October 2001 , pp. 279 - 287
Copyright
Copyright © British Society of Animal Science 2001

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References

Barbazanges, A., Piazza, P. V., Lemoal, M. and Maccari, S. 1996. Maternal glucocorticoid secretion mediates long-term effects of prenatal stress. Journal of Neuroscience 16: 3943–3949.Google Scholar
Braastad, B. O. 1998. Effects of prenatal stress on behaviour of offspring of laboratory and farmed mammals. Applied Animal Behaviour Science 61: 159–180.CrossRefGoogle Scholar
Eishi, Y., Hirokawa, K. and Hatakeyama, S. 1983. Long-lasting impairment of immune and endocrine systems of offspring induced by injection of dexamethasone into pregnant mice. Clinical Immunology and Immunopathology 26: 335–349.Google Scholar
Fameli, M., Kitraki, E. and Stylianopoulou, F. 1994. Effects of hyperactivity of the maternal hypothalamic-pituitary-adrenal (HPA) axis during pregnancy on the development of the HPA axis and brain monoamines of the offspring. International Journal of Developmental Neuroscience 12: 651–659.CrossRefGoogle ScholarPubMed
Fameli, M., Kitraki, E. and Stylianopoulou, F. 1995. Maternal behaviour of dams treated with ACTH during pregnancy. Physiology and Behavior 57: 397–400.Google Scholar
Fiedler, I., Rehfeldt, C., Albrecht, E. and Henning, M. 1998. Histophysiological features of skeletal muscle and adrenal glands in wild-type and domestic pigs during growth. Archiv für Tierzucht 41: 489–495.Google Scholar
Fiedler, I., Rehfeldt, C. and Ender, K. 1996. Histophysiologische Kriterien der Schilddrüsen- und Nebennierenaktivität neugeborener Ferkel nach Behandlung der trächtigen Sauen mit Somatotropin. Journal of Animal Physiology and Animal Nutrition 76: 199–209.Google Scholar
Fride, E., Dan, Y., Feldon, J., Halevy, G. and Weinstock, M. 1986. Effects of prenatal stress on vulnerability to stress in prepubertal and adult rats. Physiology and Behavior 37: 681–687.Google Scholar
Haussmann, M. F., Carroll, J. A., Weesner, G. D., Daniels, M. J., Matteri, R. L. and Lay Jr, D. C. 2000. Administration of ACTH to restrained, pregnant sows alters their pigs’ hypothalamic-pituitary-adrenal (HPA) axis. Journal of Animal Science 78: 2399–2411.Google Scholar
Henry, C., Kabbaj, M., Simon, H., Le Moal, M. and Maccari, S. 1994. Prenatal stress increases the hypothalamic-pituitary-adrenal axis response to stress in young and adult rats. Journal of Endocrinology 6: 341–345.Google Scholar
Jeppesen, L. L. and Heller, K. E. 1986. Stress effects on circulating eosinophil leukocytes, breeding performance, and reproductive success in ranch mink. Scientifur 10: 15–18.Google Scholar
Kanitz, E., Otten, W., Nürnberg, G. and Brüssow, K. P. 1999. Effects of age and maternal reactivity on the stress response of the pituitary-adrenocortical axis and the sympathetic nervous system in neonatal pigs. Animal Science 68: 519–526.CrossRefGoogle Scholar
Kattesh, H. G., Baumbach, G. A., Gillespie, B. B., Schneider, J. F. and Murai, J. T. 1997. Distribution between protein-bound and free forms of plasma cortisol in the gilt and fetal pig near term. Biology of the Neonate 72: 192–200.CrossRefGoogle ScholarPubMed
Kay, G., Tarcic, N., Poltyrev, T. and Weinstock, M. 1998. Prenatal stress depresses immune function in rats. Physiology and Behavior 63: 397–402.Google Scholar
Klemcke, H. G. 1995. Placental metabolism of cortisol at mid- and late gestation in swine. Biology of Reproduction 53: 1293–1301.Google Scholar
Klemcke, H. G. and 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: 99–106.CrossRefGoogle ScholarPubMed
Klemcke, H. G., Lunstra, D. D., Brown-Borg, H.M, Borg, K. E. and Christenson, R. K. 1993. Association between low birth weight and increased adrenocortical function in neonatal pigs. Journal of Animal Science 71: 1010–1018.Google Scholar
Lundström, K., Dahlberg, E., Nyberg, L., Snochowski, M., Standal, N. and Edquist, L. E. 1983. Glucocorticoid and androgen characteristics in two lines of pigs selected for rate of gain and thickness of backfat. Journal of Animal Science 56: 401–409.CrossRefGoogle Scholar
Maccari, S., Piazza, P. V., Kabbaj, M., Barbazanges, A. and Simon, H. 1995. Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. Journal of Neuroscience 15: 110–116.CrossRefGoogle ScholarPubMed
McCormick, C. M., Smythe, J. W., Sharma, S. and Meaney, M. J. 1995. Sex-specific effects of prenatal stress on hypothalamic-pituitary-adrenal responses to stress and brain glucocorticoid receptor density in adult rats. Developmental Brain Research 84: 55–61.Google Scholar
Magnusson, U., Wattrang, E., Tsuma, V. and Fossum, C. 1998. Effects of stress resulting from short-term restraint on in vitro functional capacity of leukocytes obtained from pigs. American Journal of Veterinary Research 59: 421–425.Google Scholar
Neubert, E., Gürtler, H. and Vallentin, G. 1996. Effects of snare restraint on plasma levels of catecholamines, cortisol, insulin and metabolic parameters in growing pigs. Berliner und Münchener Tierärztliche Wochenschrift 109: 409–413.Google Scholar
Otten, W., Puppe, B., Stabenow, B., Kanitz, E., Schön, P. C., Brüssow, K. P. and Nürnberg, G. 1997. Agonistic interactions and physiological reactions of top and bottom ranking pigs confronted with a familiar and unfamiliar group: preliminary results. Applied Animal Behaviour Science 55: 79–90.Google Scholar
Schneider, M. L. 1992a. The effect of mild stress during pregnancy on birth-weight and neuromotor maturation in rhesus-monkey infants (Macaca mulatta). Infant Behaviour and Development 15: 389–403.Google Scholar
Schneider, M. L. 1992b. Prenatal stress exposure alters postnatal behavioral expression under conditions of novelty challenge in rhesus-monkey infants. Developmental Psychobiology 25: 529–540.Google Scholar
Sgoifo, A., De Boer, S. F., Haller, J. and Koolhas, J. M. 1996. Individual differences in plasma catecholamine and corticosterone stress responses of wild-type rats: relation with aggression. Physiology and Behavior 60: 1403–1407.Google Scholar
Statistical Analysis Systems Institute. 1989. SAS/STAT user’s guide, version 6, 4th edition, volume 2. SAS Institute, Cary, NC.Google Scholar
Takahashi, L. K., Baker, E. W. and Kalin, N. H. 1990. Ontogeny of behavioral and hormonal responses to stress in prenatally stressed male rat pups. Physiology and Behavior 47: 357–364.Google Scholar
Takahashi, L. K., Turner, J. G. and Kalin, N. H. 1992. Prenatal stress alters brain catecholaminergic activity and potentiates stress-induced behavior in adult rats. Brain Research 574: 131–137.CrossRefGoogle ScholarPubMed
Vallée, M., Mayo, W., Dellu, F., Le Moal, M., Simon, H. and Maccari, S. 1997. Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion. Journal of Neuroscience 17: 2626–2636.Google Scholar
Ward, M. M., Mefford, I. N., Parker, S.D., Chesney, M. A., Taylor, C. B., Keegan, D. L. and Barchas, J. D. 1983. Epinephrine and norepinephrine responses in continuously collected human plasma to a series of stressors. Psychosomatic Medicine 45: 471–486.Google Scholar
Weinstock, M. 1997. Does prenatal stress impair coping and regulation of the hypothalamic-pituitary-adrenal axis? Neuroscience and Biobehavioral Reviews 21: 1–10.Google Scholar
Weinstock, M., Matlina, E., Maor, G. I., Rosen, H. and McEwen, B. S. 1992. Prenatal stress selectively alters the reactivity of the hypothalamic-pituitary-adrenal system in the female rat. Brain Research 595: 195–200.Google Scholar
Weinstock, M., Poltyrev, T., Schorer-Apelbaum, D., Men, D. and McCarty, R. 1998. Effect of prenatal stress on plasma corticosterone and catecholamines in response to footshock in rats. Physiology and Behavior 64: 439–444.Google Scholar
Wise, T., Stone, R. T. and Vernon, M. W. 1991. Relationships of serum estriol, cortisol and albumin concentrations with pig weight at 110 days of gestation and at birth. Biology of the Neonate 59: 114–119.Google Scholar
Zhang, S. H., Hennessy, D. P. and Cranwell, P. D. 1990. In vitro study of the function of adrenocortical cells from pigs of differing in vivo response to adrenocorticotropin. American Journal of Veterinary Research 51: 1016–1020.CrossRefGoogle ScholarPubMed