Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-24T15:30:30.299Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of neonatal surgical castration and immunocastration in male pigs on blood T lymphocytes and health markers

Published online by Cambridge University Press:  17 April 2014

C. Leclercq ,
A. Prunier  and
E. Merlot
C. Leclercq
Affiliation:
INRA, UMR1348 PEGASE, F-35590 Saint-Gilles, France Agrocampus Ouest, UMR1348 PEGASE, F-35000 Rennes, France
A. Prunier
Affiliation:
INRA, UMR1348 PEGASE, F-35590 Saint-Gilles, France Agrocampus Ouest, UMR1348 PEGASE, F-35000 Rennes, France
E. Merlot*
Affiliation:
INRA, UMR1348 PEGASE, F-35590 Saint-Gilles, France Agrocampus Ouest, UMR1348 PEGASE, F-35000 Rennes, France
*
† E-mail: [email protected]
Get access

Abstract

Surgical castration in pig husbandry is criticized for welfare reasons. Thus, it is necessary to evaluate alternative ways of rearing male pigs, such as entire or immunocastrated animals. Immunocastration is a vaccination directed against gonadotropin-releasing hormone (GnRH) to suppress the production of sexual hormones. This study aimed at investigating the effects of these two methods of castration in comparison with intact male pigs on blood T-lymphocyte subsets and function, the immunoglobulin (Ig) response to an influenza vaccine and health markers during sexual development. A total of 70 animals were allocated to three experimental groups: entire (E), surgically castrated at 5 to 6 days of age (SC), and immunized against GnRH at 3 and 4 months of age (IC). Blood samples were collected at 3, 4 and 5 months. At slaughter, global health status and body and spleen weights were measured. Results showed that SC male pigs had fewer blood lymphocytes than E pigs at 4 and 5 months (P<0.05), whereas IC pigs did not differ significantly from E pigs. The percentages of CD3+, CD3+CD4+ and CD3+CD8+ lymphocytes were not altered by treatment (P>0.1). Compared with E pigs, the SC pigs had a higher percentage of CD3+CD4+CD8+ cells at 4 months, whereas the IC pigs had a higher percentage at 5 months (P<0.05). Regarding γδT cells, SC pigs had a lower percentage than E pigs at 4 and 5 months (P<0.05), whereas IC pigs did not differ significantly from E pigs at any age. However, there were no consequences on T-lymphocyte proliferation and total IgG or anti-influenza Ig. At slaughter, relative spleen weight was decreased in IC pigs, whereas pneumonia score was decreased in SC pigs relatively to E pigs. Overall, no clear functional consequences of either method on commercial pig immune abilities were demonstrated, but more investigations are required to ascertain this conclusion.

Keywords

pigsurgical castrationimmunocastrationtestosteroneT cells
Type
Full Paper
Information
animal , Volume 8 , Issue 5 , May 2014 , pp. 836 - 843
Copyright
© The Animal Consortium 2014 

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

Allrich, RD, Christenson, RK, Ford, JJ and Zimmerman, DR 1982. Pubertal development of the boar -testosterone, estradiol-17-beta, cortisol and LH concentrations before and after castration at various ages. Journal of Animal Science 55, 1139–1146.CrossRefGoogle ScholarPubMed
Azad, N, LaPaglia, N, Agrawal, L, Steiner, J, Uddin, S, Williams, DW, Lawrence, AM and Emanuele, NV 1998. The role of gonadectomy and testosterone replacement on thymic luteinizing hormone-releasing hormone production. Journal of Endocrinology 158, 229–235.CrossRefGoogle ScholarPubMed
Bouman, A, Heineman, MJ and Faas, MM 2005. Sex hormones and the immune response in humans. Human Reproduction Update 11, 411–423.CrossRefGoogle ScholarPubMed
Brunius, C, Zamaratskaia, G, Andersson, K, Chen, G, Norrby, M, Madej, A and Lundstrom, K 2011. Early immunocastration of male pigs with Improvac (R) – effect on boar taint, hormones and reproductive organs. Vaccine 29, 9514–9520.CrossRefGoogle Scholar
Caccamo, N, Dieli, F, Wesch, D, Jomaa, H and Eberl, M 2006. Sex-specific phenotypical and functional differences in peripheral human V gamma 9/V delta 2 T cells. Journal of Leukocyte Biology 79, 663–666.CrossRefGoogle Scholar
Chen, A, Ganor, Y, Rahimipour, S, Ben-Aroya, N, Koch, Y and Levite, M 2002. The neuropeptides GnRH-II and GnRH-I are produced by human T cells and trigger laminin receptor gene expression, adhesion, chemotaxis and homing to specific organs. Nature Medicine 8, 1421–1426.CrossRefGoogle Scholar
Claus, R, Lacorn, M, Danowski, K, Pearce, MC and Bauer, A 2007. Short-term endocrine and metabolic reactions before and after second immunization against GnRH in boars. Vaccine 25, 4689–4696.CrossRefGoogle ScholarPubMed
Colenbrander, B, Dejong, FH and Wensing, CJG 1978. Changes in serum testosterone concentrations in male pig during development. Journal of Reproduction and Fertility 53, 377–380.Google Scholar
Colenbrander, B, Meijer, JC, Macdonald, AA, Vandewiel, DFM, Engel, B and de Jong, FH 1987. Feedback-regulation of gonadotropic hormone secretion in neonatal pigs. Biology of Reproduction 36, 871–877.CrossRefGoogle ScholarPubMed
Couret, D, Jamin, A, Kuntz-Simon, G, Prunier, A and Merlot, E 2009. Maternal stress during late gestation has moderate but long-lasting effects on the immune system of the piglets. Veterinary Immunology Immunopathology 131, 17–24.CrossRefGoogle ScholarPubMed
Ellis, TM, Moser, MT, Le, PT, Flanigan, RC and Kwon, ED 2001. Alterations in peripheral B cells and B cell progenitors following androgen ablation in mice. Internal Immunology 13, 553–558.CrossRefGoogle Scholar
Gould, KG, Akinbami, MA and Mann, DR 1998. Effect of neonatal treatment with a gonadotropin releasing hormone antagonist on developmental changes in circulating lymphocyte subsets: a longitudinal study in male rhesus monkeys. Developmental and Comparative Immunology 22, 457–467.CrossRefGoogle ScholarPubMed
Henry, Y, Dauloudet, C, Kerisit, R, Lefeuve, P, Gaye, A, Denechaud, MF and Bourdon, D 1970. Effets nutritionnels de l’incorporation de cellulose purifiée dans le régime du porc en croissance-finition. III-Incidence sur le développement des ulcères gastro-oesophagiens. Annales de Zootechnie 19, 117–141.CrossRefGoogle Scholar
Hirakata, A, Okumi, M, Griesemer, AD, Shimizu, A, Nobori, S, Tena, A, Moran, S, Arn, S, Boyd, RL, Sachs, DH and Yamada, K 2010. Reversal of age-related thymic involution by an LHRH agonist in miniature swine. Transplant Immunology 24, 76–81.CrossRefGoogle ScholarPubMed
Jacobson, JD and Ansari, MA 2004. Immunomodulatory actions of gonadal steroids may be mediated by gonadotropin-releasing hormone. Endocrinology 145, 330–336.CrossRefGoogle ScholarPubMed
Jacobson, JD, Crofford, LJ, Sun, LH and Wilder, RL 1998. Cyclical expression of GnRH and GnRH receptor mRNA in lymphoid organs. Neuroendocrinology 67, 117–125.CrossRefGoogle ScholarPubMed
Kanda, N, Tsuchida, T and Tamaki, K 1996. Testosterone inhibits immunoglobulin production by human peripheral blood mononuclear cells. Clinical and Experimental Immunology 106, 410–415.CrossRefGoogle ScholarPubMed
Leposavic, G, Perisic, M, Kosec, D, Arsenovic-Ranin, N, Radojevic, K, Stojic-Vukanic, Z and Pilipovic, I 2009. Neonatal testosterone imprinting affects thymus development and leads to phenotypic rejuvenation and masculinization of the peripheral blood T-cell compartment in adult female rats. Brain, Behavior, and Immunity 23, 294–304.CrossRefGoogle ScholarPubMed
Madec, F and Kobish, M 1982. A survey of pulmonary-lesions in bacon pigs (observations made at the slaughterhouse). Annales de Zootechnie 31, 341.CrossRefGoogle Scholar
Merlot, E, Thomas, F and Prunier, A 2013. Comparison of immune and health markers in intact and neonatally castrated male pigs. Veterinary Record 173, 317.CrossRefGoogle ScholarPubMed
Odink, J, Smeets, JFM, Visser, IJR, Sandman, H and Snijders, JMA 1990. Hematological and clinicochemical profiles of healthy swine and swine with inflammatory processes. Journal of Animal Science 68, 163–170.CrossRefGoogle ScholarPubMed
Pescovitz, MD, Sakopoulos, AG, Gaddy, JA, Husmann, RJ and Zuckermann, FA 1994. Porcine peripheral-blood CD4(+) CD8(+) dual expressing T-cells. Veterinary Immunology Immunopathology 43, 53–62.Google Scholar
Radojevic, K, Arsenovic-Ranin, N, Kosec, D, Pesic, V, Pilipovic, I, Perisic, M, Plecas-Solarovic, B and Leposavic, G 2007. Neonatal castration affects intrathymic kinetics of T-cell differentiation and the spleen T-cell level. Journal of Endocrinology 192, 669–682.Google Scholar
Shioya, N, Inomata, T, Ninomiya, W and Nakamura, T 2000. Influence of castration on development of the thymus in neonatal male rats. Experimental Animals 49, 57–60.CrossRefGoogle ScholarPubMed
Sutherland, JS, Goldberg, GL, Hammett, MV, Uldrich, AP, Berzins, SP, Heng, TS, Blazar, BR, Millar, JL, Malin, MA, Chidgey, AP and Boyd, RL 2005. Activation of thymic regeneration in mice and humans following androgen blockade. Journal of Immunology 175, 2741–2753.CrossRefGoogle ScholarPubMed
Tallet, C, Brillouet, A, Paulmier, V, Meunier-Salaun, M-C, Bonneau, M and Prunier, A 2011. Conséquences de l'enrichissement du milieu sur le développement sexuel et l'agressivité des porcs mâles entiers et castrés. Journées de la Recherche Porcine 43, 187–188.Google Scholar
Tallet, C, Brillouet, A, Meunier-Salaun, MC, Paulmier, V, Guerin, C and Prunier, A 2013. Effects of neonatal castration on social behaviour, human-animal relationship and feeding activity in finishing pigs reared in a conventional or an enriched housing. Applied Animal Behaviour Science 145, 70–83.CrossRefGoogle Scholar
Viselli, SM, Stanziale, S, Shults, K, Kovacs, WJ and Olsen, NJ 1995. Castration alters peripheral immune function in normal-male mice. Immunology 84, 337–342.Google ScholarPubMed
Zuckermann, FA and Husmann, RJ 1996. Functional and phenotypic analysis of porcine peripheral blood CD4/CD8 double-positive T cells. Immunology 87, 500–512.Google ScholarPubMed