Effects of tail docking and castration on stress responses in lambs and the influence of prenatal glucocorticoid treatment
Shaofu Li A B E , Ilias Nitsos A D , Graeme R. Polglase A D , John P. Newnham A B , John R. G. Challis A C and Timothy J. M. Moss A D
+ Author Affiliations
- Author Affiliations
A School of Women’s and Infants’ Health, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
B Women and Infants Research Foundation of Western Australia, 374 Bagot Road, Subiaco, WA 6008, Australia.
C Departments of Physiology and Obstetrics and Gynecology, University of Toronto, 1 King’s College Circle, Toronto, ON M5S 1A8, Canada.
D The Ritchie Centre, Monash Institute of Medical Research and Department of Obstetrics and Gynaecology, Monash University, 27–31 Wright Street, Clayton, Vic. 3800, Australia.
E Corresponding author. Email: shaofu.li@uwa.edu.au
Reproduction, Fertility and Development 25(7) 1020-1025 https://doi.org/10.1071/RD12229
Submitted: 25 May 2012 Accepted: 21 September 2012 Published: 15 October 2012
Abstract
It is common practice in Australian agriculture to remove the tails of lambs to prevent infection and to castrate males to prevent behavioural problems and unwanted reproduction. We have studied the pain and stress responses to these interventions by measuring changes in the hypothalamic–pituitary–adrenal (HPA) axis and β-endorphin levels. Further, we have evaluated the effects of prenatal exposure to dexamethasone, which is known to affect the developing HPA axis. In control animals that had received prenatal saline treatment, plasma cortisol and adrenocorticotrophin (ACTH) levels increased after the interventions in both females and males. Plasma β-endorphin levels also increased after the interventions, but the responses were less consistent. Prenatal dexamethasone exposure early in pregnancy (dexamethasone 0.14 mg kg–1 ewe weight injection commenced on day 40 of pregnancy for four consecutive intramuscular injections at 12-hourly intervals) blunted the cortisol response to tail docking in female offspring, but not to combined tail docking and castration in males. It had no effect on ACTH or β-endorphin responses in either sex. These findings describe the stress responses to these common agricultural interventions and suggest that long-term development of the HPA axis in females is altered by prenatal exposure to dexamethasone.
Additional keywords : adrenal gland, fetal programming, hormone.
References
Braun, T., Li, S., Sloboda, D. M., Li, W., Audette, M. C., Moss, T. J. M., Matthews, S. G., Polglase, G., Nitsos, I., Newnham, J. P., and Challis, J. R. G. (2009). Effects of maternal dexamethasone treatment in early pregnancy on pituitary–adrenal axis in fetal sheep. Endocrinology 150, 5466–5477.| Effects of maternal dexamethasone treatment in early pregnancy on pituitary–adrenal axis in fetal sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFGqtb3L&md5=ea7b13b8c3395648b6c06a20cba93713CAS | 19846612PubMed |
Corner, R. A., Kenyon, P. R., Stafford, K. J., West, D. M., and Oliver, M. H. (2007). The effect of mid-pregnancy shearing and litter size on lamb birth weight and postnatal plasma cortisol response. Small Rumin. Res. 73, 115–121.
| The effect of mid-pregnancy shearing and litter size on lamb birth weight and postnatal plasma cortisol response.Crossref | GoogleScholarGoogle Scholar |
de Vries, A., Holmes, M. C., Heijnis, A., Seier, J. V., Heerden, J., Louw, J., Wolfe-Coote, S., Meaney, M. J., Levitt, N. S., and Seckl, J. R. (2007). Prenatal dexamethasone exposure induces changes in nonhuman primate offspring cardiometabolic and hypothalamic–pituitary–adrenal axis function. J. Clin. Invest. 117, 1058–1067.
| Prenatal dexamethasone exposure induces changes in nonhuman primate offspring cardiometabolic and hypothalamic–pituitary–adrenal axis function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktVOit7w%3D&md5=838c8221b02808f556787c040dadfb09CAS | 17380204PubMed |
Diaz Heijtz, R., Fuchs, E., Feldon, J., Pryce, C. R., and Forssberg, H. (2010). Effects of antenatal dexamethasone treatment on glucocorticoid receptor and calcyon gene expression in the prefrontal cortex of neonatal and adult common marmoset monkeys. Behav. Brain Funct. 6, 18.
| Effects of antenatal dexamethasone treatment on glucocorticoid receptor and calcyon gene expression in the prefrontal cortex of neonatal and adult common marmoset monkeys.Crossref | GoogleScholarGoogle Scholar | 20307270PubMed |
Dodic, M., Abouantoun, T., O’Connor, A., Wintour, E. M., and Moritz, K. M. (2002a). Programming effects of short prenatal exposure to dexamethasone in sheep. Hypertension 40, 729–734.
| Programming effects of short prenatal exposure to dexamethasone in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XpsFWlsbw%3D&md5=78a84132a32fa8cfbcc584031f40e258CAS | 12411469PubMed |
Dodic, M., Hantzis, V., Duncan, J., Rees, S., Koukoulas, I., Johnson, K., Wintour, E. M., and Moritz, K. (2002b). Programming effects of short prenatal exposure to cortisol. FASEB J. 16, 1017–1026.
| Programming effects of short prenatal exposure to cortisol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltlGrsb0%3D&md5=2cc8934bea329243beb6566d939d931eCAS | 12087063PubMed |
Dodic, M., McAlinden, A. T., Jefferies, A. J., Wintour, E. M., Cock, M. L., May, C. N., Evans, R. G., and Moritz, K. M. (2006). Differential effects of prenatal exposure to dexamethasone or cortisol on circulatory control mechanisms mediated by angiotensin II in the central nervous system of adult sheep. J. Physiol. 571, 651–660.
| Differential effects of prenatal exposure to dexamethasone or cortisol on circulatory control mechanisms mediated by angiotensin II in the central nervous system of adult sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XktVCkurk%3D&md5=1837f710acb9ba4a2725044b97efa032CAS | 16423855PubMed |
Forest, M. G. (2004). Recent advances in the diagnosis and management of congenital adrenal hyperplasia due to 21-hydroxylase deficiency. Hum. Reprod. Update 10, 469–485.
| Recent advances in the diagnosis and management of congenital adrenal hyperplasia due to 21-hydroxylase deficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVSru7rK&md5=820a010b685194b777be31fd215148ecCAS | 15514016PubMed |
Graham, M. J., Kent, J. E., and Molony, V. (1997). Effects of four analgesic treatments on the behavioural and cortisol responses of 3-week-old lambs to tail docking. Vet. J. 153, 87–97.
| Effects of four analgesic treatments on the behavioural and cortisol responses of 3-week-old lambs to tail docking.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXkslagtrs%3D&md5=d9854b421587be6466cc4189e34254f7CAS | 9125361PubMed |
Hantzis, V., Albiston, A., Matsacos, D., Wintour, E. M., Peers, A., Koukoulas, I., Myles, K., Moritz, K., and Dodic, M. (2002). Effect of early glucocorticoid treatment on MR and GR in late gestation ovine kidney. Kidney Int. 61, 405–413.
| Effect of early glucocorticoid treatment on MR and GR in late gestation ovine kidney.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtlWjt78%3D&md5=bfa1da0c371946b93d3e86eb6af3513aCAS | 11849380PubMed |
Jobe, A. H., Wada, N., Berry, L. M., Ikegami, M., and Ervin, M. G. (1998). Single and repetitive maternal glucocorticoid exposures reduce fetal growth in sheep. Am. J. Obstet. Gynecol. 178, 880–885.
| Single and repetitive maternal glucocorticoid exposures reduce fetal growth in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjslOltb0%3D&md5=293c1fa82b6f8da2f6273cdcd2b2b476CAS | 9609554PubMed |
Kent, J. E., Molony, V., and Graham, M. J. (1998). Comparison of methods for the reduction of acute pain produced by rubber ring castration or tail docking of week-old lambs. Vet. J. 155, 39–51.
| Comparison of methods for the reduction of acute pain produced by rubber ring castration or tail docking of week-old lambs.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c7hs1WksA%3D%3D&md5=cddd7798589700720f1d1ce9c0297b20CAS | 9455158PubMed |
Lajic, S., Nordenstrom, A., and Hirvikoski, T. (2008). Long-term outcome of prenatal treatment of congenital adrenal hyperplasia. Endocr. Dev. 13, 82–98.
| Long-term outcome of prenatal treatment of congenital adrenal hyperplasia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhslWht7o%3D&md5=768adaaceb5814387ebff5302fb3fb8fCAS | 18493135PubMed |
Li, S., Nitsos, I., Polglase, G. R., Braun, T., Moss, T. J., Newnham, J. P., and Challis, J. R. (2012). The effects of dexamethasone treatment in early gestation on hypothalamic–pituitary–adrenal responses and gene expression at 7 months of postnatal age in sheep. Reprod. Sci. 19, 260–270.
| The effects of dexamethasone treatment in early gestation on hypothalamic–pituitary–adrenal responses and gene expression at 7 months of postnatal age in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlvFShtbk%3D&md5=e2c2982b42142be8797e1e13e5c16fabCAS | 22101239PubMed |
Liggins, G. C., and Howie, R. N. (1972). A controlled trial of antepartum glucocorticoid treatment for prevention of the respiratory distress syndrome in premature infants. Pediatrics 50, 515–525.
| 1:STN:280:DyaE3s%2FgvVCrtw%3D%3D&md5=75b16cf245f533778b55ff6cdcb1dbd0CAS | 4561295PubMed |
Mellor, D. J., Stafford, K. J., Todd, S. E., Lowe, T. E., Gregory, N. G., Bruce, R. A., and Ward, R. N. (2002). A comparison of catecholamine and cortisol responses of young lambs and calves to painful husbandry procedures. Aust. Vet. J. 80, 228–233.
| A comparison of catecholamine and cortisol responses of young lambs and calves to painful husbandry procedures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltlOrsbc%3D&md5=b007e4461e22b10d9f7e8b391f28ecc3CAS | 12054287PubMed |
Merlot, E., Couret, D., and Otten, W. (2008). Prenatal stress, fetal imprinting and immunity. Brain Behav. Immun. 22, 42–51.
| 1:CAS:528:DC%2BD2sXhsVWjtLzP&md5=dd599f23b2457a99a7dda3ad387ca8a4CAS | 17716859PubMed |
Moritz, K., Butkus, A., Hantzis, V., Peers, A., Wintour, E. M., and Dodic, M. (2002). Prolonged low-dose dexamethasone, in early gestation, has no long-term deleterious effect on normal ovine fetuses. Endocrinology 143, 1159–1165.
| Prolonged low-dose dexamethasone, in early gestation, has no long-term deleterious effect on normal ovine fetuses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XisFGju7Y%3D&md5=186a2eed1825b3e5186935977d97798cCAS | 11897667PubMed |
Morris, D. G., Kuchel, T. R., and Maddocks, S. (1994). Stress responses in lambs to different tail docking methods. Proc. Aust. Soc. Anim. Prod. 20, 202–205.
Moss, T. J., Sloboda, D. M., Gurrin, L. C., Harding, R., Challis, J. R., and Newnham, J. P. (2001). Programming effects in sheep of prenatal growth restriction and glucocorticoid exposure. Am. J. Physiol. Regul. Integr. Comp. Physiol. 281, R960–R970.
| 1:CAS:528:DC%2BD3MXmvFWju7w%3D&md5=678dadc7e0028b4eee3aaec49eefb83aCAS | 11507014PubMed |
Moss, T. J., Nitsos, I., Harding, R., and Newnham, J. P. (2003). Differential effects of maternal and fetal betamethasone injections in late-gestation fetal sheep. J. Soc. Gynecol. Invest. 10, 474–479.
| Differential effects of maternal and fetal betamethasone injections in late-gestation fetal sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXps1Oltrk%3D&md5=79e66f68ffefc835cc17c7e3145fd06cCAS |
Peers, A., Mellor, D. J., Wintour, E. M., and Dodic, M. (2002). Blood pressure, heart rate, hormonal and other acute responses to rubber-ring castration and tail docking of lambs. N. Z. Vet. J. 50, 56–62.
| Blood pressure, heart rate, hormonal and other acute responses to rubber-ring castration and tail docking of lambs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjtlWisLc%3D&md5=28efa3528f421638809b2c45b2d81551CAS | 16032211PubMed |
Ritzén, E. M. (2001). Prenatal dexamethasone treatment of fetuses at risk for congenital adrenal hyperplasia: benefits and concerns. Semin. Neonatol. 6, 357–362.
| Prenatal dexamethasone treatment of fetuses at risk for congenital adrenal hyperplasia: benefits and concerns.Crossref | GoogleScholarGoogle Scholar | 11972437PubMed |
Rizvi, Z. B., Aniol, H. S., Myers, T. F., Zeller, W. P., Fisher, S. G., and Anderson, C. L. (1992). Effects of dexamethasone on the hypothalamic–pituitary–adrenal axis in preterm infants. J. Pediatr. 120, 961–965.
| Effects of dexamethasone on the hypothalamic–pituitary–adrenal axis in preterm infants.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK383nslaitg%3D%3D&md5=3f5bf269162eeb1d5de0e78d576ebd87CAS | 1317422PubMed |
Sloboda, D. M., Moss, T. J., Li, S., Doherty, D., Nitsos, I., Challis, J. R., and Newnham, J. P. (2007). Prenatal betamethasone exposure results in pituitary–adrenal hyporesponsiveness in adult sheep. Am. J. Physiol. Endocrinol. Metab. 292, E61–E70.
| Prenatal betamethasone exposure results in pituitary–adrenal hyporesponsiveness in adult sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXisFCqsb8%3D&md5=c3c9debe699ce910eff69a68bfaa2767CAS | 16882931PubMed |
Turner, A. I., Hosking, B. J., Parr, R. A., and Tilbrook, A. J. (2006). A sex difference in the cortisol response to tail docking and ACTH develops between 1 and 8 weeks of age in lambs. J. Endocrinol. 188, 443–449.
| A sex difference in the cortisol response to tail docking and ACTH develops between 1 and 8 weeks of age in lambs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjt1Kjt7w%3D&md5=cae6a07737a013d69cbf47afd972c163CAS | 16522725PubMed |
