J Vet Sci.  2011 Jun;12(2):151-157. 10.4142/jvs.2011.12.2.151.

The stress of weaning influences serum levels of acute-phase proteins, iron-binding proteins, inflammatory cytokines, cortisol, and leukocyte subsets in Holstein calves

• Kim MH
• Yang JY
• Upadhaya S
• Lee HJ
• Yun CH
• Ha JK

• KMID: 1106557
• DOI: http://doi.org/10.4142/jvs.2011.12.2.151

Abstract

The purpose of our study was to investigate changes in immunological parameters induced by weaning stress (including milk restriction) in calves. Fifteen Holstein calves were subjected to weaning at 6 weeks of age. Blood samples were collected at -14, -7, -2, 1, 3, and 5 days post-weaning (DPW; 0 DPW = 42 days). Weaning caused significant (p < 0.01) increases in the neutrophil (NE):lymphocyte (LY) ratio at 5 DPW with a significant (p < 0.05) reduction of LYs. The concentration of acute-phase proteins (haptoglobin and serum amyloid A) also increased significantly (p < 0.05) at 3 and 5 DPW compared to -2 DPW. Levels of the iron-binding protein lactoferrin decreased significantly (p < 0.05) after weaning. Serum tumor necrosis factor-alpha and cortisol levels were elevated (p < 0.05) at 3 DPW, while those of serum interferon-gamma decreased (p < 0.05) at 1 and 3 DPW compared to levels observed before weaning. Weaning significantly (p < 0.05) decreased the percentage of CD25+ T cells in the peripheral blood. In conclusion, weaning stress affected the NE:LY ratio along with the levels of acute phase proteins, lactoferrin, cortisol, and inflammatory cytokines in the peripheral blood of calves. Weaning stress may induce an acute phase response possibly through the elevation of cortisol production and modulation of inflammatory cytokines.

Keyword

acute phase protein; immune response; inflammatory cytokines; stress; weaning

MeSH Terms

Acute-Phase Proteins/*immunology/metabolism
Acute-Phase Reaction/immunology/*veterinary
Animals
Cattle/*immunology
Female
Flow Cytometry
Haptoglobins/analysis/immunology
Hydrocortisone/blood/immunology
Interferon-gamma/blood/immunology
Lactoferrin/analysis/immunology
Leukocyte Count/veterinary
Leukocytes/cytology/*immunology
Male
Serum Amyloid A Protein/analysis/immunology
Stress, Physiological/*physiology
Tumor Necrosis Factor-alpha/blood/immunology
Weaning

Reference

1. Anderson BH, Watson DL, Colditz IG. The effect of dexamethasone on some immunological parameters in cattle. Vet Res Commun. 1999. 23:399–413.

2. Arthington JD, Eicher SD, Kunkle WE, Martin FG. Effect of transportation and commingling on the acute-phase protein response, growth, and feed intake of newly weaned beef calves. J Anim Sci. 2003. 81:1120–1125.

3. Blecha F, Baker PE. Effect of cortisol in vitro and in vivo on production of bovine interleukin 2. Am J Vet Res. 1986. 47:841–845.

4. Burton JL, Kehrli ME Jr. Regulation of neutrophil adhesion molecules and shedding of Staphylococcus aureus in milk of cortisol- and dexamethasone-treated cows. Am J Vet Res. 1995. 56:997–1006.

5. Church JS, Hudson RJ. Comparison of the stress of abrupt and interval weaning of farmed wapiti calves (Cervus elaphus). Small Rumin Res. 1999. 32:119–124.

6. Conner JG, Eckersall PD, Ferguson J, Douglas TA. Acute phase response in the dog following surgical trauma. Res Vet Sci. 1988. 45:107–110.

7. Cunnick JE, Lysle DT, Kucinski BJ, Rabin BS. Evidence that shock-induced immune suppression is mediated by adrenal hormones and peripheral β-adrenergic receptors. Pharmacol Biochem Behav. 1990. 36:645–651.

8. Fike K, Spire MF. Transportation of cattle. Vet Clin North Am Food Anim Pract. 2006. 22:305–320.

9. Foote MR, Nonnecke BJ, Fowler MA, Miller BL, Beitz DC, Waters WR. Effects of age and nutrition on expression of CD25, CD44, and L-selectin (CD62L) on T-cells from neonatal calves. J Dairy Sci. 2005. 88:2718–2729.

10. Grandin T. Assessment of stress during handling and transport. J Anim Sci. 1997. 75:249–257.

11. Herzog KR. The effects of weaning stress on the serum protein profile of calves: a proteomic analysis. 2007. Saskatoon: University of Saskatchewan;Master thesis.

12. Hickey MC, Drennan M, Earley B. The effect of abrupt weaning of suckler calves on the plasma concentrations of cortisol, catecholamines, leukocytes, acute-phase proteins and in vitro interferon-gamma production. J Anim Sci. 2003. 81:2847–2855.

13. Johnson JD, Campisi J, Sharkey CM, Kennedy SL, Nickerson M, Greenwood BN, Fleshner M. Catecholamines mediate stress-induced increases in peripheral and central inflammatory cytokines. Neuroscience. 2005. 135:1295–1307.

14. Kelley KW. Stress and immune function: a bibliographic review. Ann Rech Vet. 1980. 11:445–478.

15. Kelley KW, Johnson RW, Dantzer R. Immunology discovers physiology. Vet Immunol Immunopathol. 1994. 43:157–165.

16. Khan MA, Lee HJ, Lee WS, Kim HS, Kim SB, Ki KS, Ha JK, Lee HG, Choi YJ. Pre- and postweaning performance of Holstein female calves fed milk through step-down and conventional methods. J Dairy Sci. 2007. 90:876–885.

17. Kurash JK, Shen CN, Tosh D. Induction and regulation of acute phase proteins in transdifferentiated hepatocytes. Exp Cell Res. 2004. 292:342–358.

18. Lee HJ, Khan MA, Lee WS, Kim HS, Ki KS, Kang SJ, Hur TY, Khan MS, Choi YJ. Growth, blood metabolites, and health of Holstein calves fed milk replacer containing different amounts of energy and protein. Asian-Australas J Anim Sci. 2008. 21:198–203.

19. Leonard BE. The HPA and immune axes in stress: the involvement of the serotonergic system. Eur Psychiatry. 2005. 20:Suppl 3. S302–S306.

20. Marinkovic S, Jahreis GP, Wong GG, Baumann H. IL-6 modulates the synthesis of a specific set of acute phase plasma proteins in vivo. J Immunol. 1989. 142:808–812.

21. Murata H, Miyamoto T. Bovine haptoglobin as a possible immunomodulator in the sera of transported calves. Br Vet J. 1993. 149:277–283.

22. Murata H. Stress and acute phase protein response: an inconspicuous but essential linkage. Vet J. 2007. 173:473–474.

23. Heegaard PMH, Godson DL, Toussaint MJM, Tjørnehøj K, Larsen LE, Viuff B, Rønsholt L. The acute phase response of haptoglobin and serum amyloid A (SAA) in cattle undergoing experimental infection with bovine respiratory syncytial virus. Vet Immunol Immunopathol. 2000. 77:151–159.

24. Phillips WA, Juniewicz PE, Zavy MT, Von Tungeln DL. The effect of the stress of weaning and transport on white blood cell patterns and fibrinogen concentration of beef calves of different genotypes. Can J Anim Sci. 1989. 69:333–340.

25. Richards DF, Fernandez M, Caulfield J, Hawrylowicz CM. Glucocorticoids drive human CD8⁺ T cell differentiation towards a phenotype with high IL-10 and reduced IL-4, IL-5 and IL-13 production. Eur J Immunol. 2000. 30:2344–2354.

26. Salak-Johnson JL, McGlone JJ, Norman RL. In vivo glucocorticoid effects on porcine natural killer cell activity and circulating leukocytes. J Anim Sci. 1996. 74:584–592.

27. Schaefer AL, Jones SD, Stanley RW. The use of electrolyte solutions for reducing transport stress. J Anim Sci. 1997. 75:258–265.

28. Shawhat Ali MD, Kang GH, Joo ST. A review: influence of pre-slaughter stress on poultry meat quality. Asian-Australas J Anim Sci. 2008. 21:912–916.

29. Shinde PL, Dass RS, Garg AK, Chaturvedi VK. Immune response and plasma alpha tocopherol and selenium status of male buffalo (Bubalus bubalis) calves supplemented with vitamin E and selenium. Asian-Australas J Anim Sci. 2007. 20:1539–1545.

30. Sivakumar AVN, Singh G, Varshney VP. Antioxidants supplementation on acid base balance during heat stress in goats. Asian-Australas J Anim Sci. 2010. 23:1462–1468.

31. Sunil Kumar BV, Singh G, Meur SK. Effects of addition of electrolyte and ascorbic acid in feeding during heat stress in bufalloes. Asian-Australas J Anim Sci. 2010. 23:880–888.

32. Tizard IR. Veterinary Immunology: an Introduction. 2004. 7th ed. Philadelphia: Saunders.

33. Wakabayashi H, Yamauchi K, Takase M. Lactoferrin research, technology and applications. Int Dairy J. 2006. 16:1241–1251.

34. Wallgren P, Wilén IL, Fossum C. Influence of experimentally induced endogenous production of cortisol on the immune capacity in swine. Vet Immunol Immunopathol. 1994. 42:301–316.

35. Warren EJ, Finck BN, Arkins S, Kelley KW, Scamurra RW, Murtaugh MP, Johnson RW. Coincidental changes in behavior and plasma cortisol in unrestrained pigs after intracerebroventricular injection of tumor necrosis factor-α. Endocrinology. 1997. 138:2365–2371.

36. Westly HJ, Kelley KW. Physiologic concentrations of cortisol suppress cell-mediated immune events in the domestic pig. Proc Soc Exp Biol Med. 1984. 177:156–164.

37. Yamane H, Kurauchi I, Denbow DM, Furuse M. Central functions of amino acids for the stress response in chicks. Asian-Australas J Anim Sci. 2009. 22:296–304.