Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-19T23:19:29.891Z Has data issue: false hasContentIssue false

Interleukin-1ra increases growth performance and body protein accretion and decreases the cytokine response in a model of subclinical disease in growing pigs

Published online by Cambridge University Press:  09 March 2007

L. Dionissopoulos
Affiliation:
Department of Animal and Poultry Science, University of Guelph, Guelph, Ontario N1G 2W1, Canada
C.E. Dewey
Affiliation:
Department of Population Medicine, University of Guelph, Guelph, Ontario N1G 2W1, Canada
H. Namkung
Affiliation:
Department of Animal and Poultry Science, University of Guelph, Guelph, Ontario N1G 2W1, Canada
C.F.M. De Lange*
Affiliation:
Department of Animal and Poultry Science, University of Guelph, Guelph, Ontario N1G 2W1, Canada
*
Corresponding author: E-mail: [email protected]
Get access

Abstract

There is a growing body of evidence to suggest direct involvement of the cytokines interleukin-1 (IL-1), interleukin-6 (IL-6) and tumour necrosis factor-α (TNF-α) in the initiation of skeletal muscle catabolism and depressions in growth performance as a result of diseases, while TNF-α and IL-6 are presumably under the control of IL-1. An experiment was conducted to investigate whether an interleukin-1 receptor antagonist (IL-1ra) could reduce growth depressions in a model of subclinical disease in growing pigs. In this study, 24 crossbred barrows and gilts were randomly assigned to three treatments: (1) healthy control (HC), saline infusion; (2) sick control (SC), infection with Mycoplasma hyopneumoniae and vaccination with porcine reproductive and respiratory syndrome modified live virus (PRRSV) vaccine and saline infusion; (3) SC plus infusion with IL-1ra (SC+IL-1ra). An additional six pigs were killed at the initiation of the trial to determine initial body composition for estimation of carcass nutrient retention rates. During the 28-day experimental period, the SC pigs had growth performance similar to that of the HC pigs and the highest levels of plasma cytokines (P<0·10). The SC+IL-1ra pigs had growth performance similar to the HC pigs, but the SC+Il-1ra pigs tended to have higher growth rates than the SC pigs (P<0·10), the highest carcass protein accretion rate (P<0·10) and similar levels of plasma cytokines compared with the HC pigs. Plasma levels of insulin-like growth factor-1 (IGF-1) on day 22 tended to be higher (P<0·10) in the HC pigs compared with the SC or SC+IL-1ra pigs and treatment×sex interaction was observed on day 29; the IGF-1 levels tended to be higher in SC+IL-1ra gilts and SC barrows (P<0·10). These results indicate that infusion with IL-1ra in a model of subclinical disease helps attenuate the catabolic effects of immune system stimulation.

Type
Research Article
Copyright
Copyright © British Society of Animal Science 2006

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

Arend, W. P., Welgus, H. G., Thompson, R. C. and Eisenberg, S. P. 1990. Biological properties of recombinant human interleukin-1 receptor antagonist. Journal of Clinical Investigation 85: 16941697.CrossRefGoogle Scholar
Bateman, A., Singh, A., Kral, T. and Solomon, S. 1989. The immune-hypothalamic-pituitary-adrenal axis. Endocrinology Reviews 10: 92112.CrossRefGoogle ScholarPubMed
Breuillé, D., Farge, M. C., Rosé, F., Arnal, M., Attaix, D. and Obled, C. 1993. Pentoxifylline decreases body weight loss and muscle protein wasting characteristics of sepsis. American Journal of Physiology 265: E660E666.Google ScholarPubMed
Broussard, S. R., Zhou, J. H., Venters, H. D., Bluthe, R. M., Freund, G. G., Johnson, R. W., Dantzer, R. and Kelley, K. W. 2001. At the interface of environment-immune interactions: cytokine and growth-factor receptors. Journal of Animal Science 79: E268E284.CrossRefGoogle Scholar
De Lange, C. F. M., Souffrant, W. B. and Sauer, W. C. 1990. Real ileal protein and amino acid digestibilities in feedstuffs for growing pigs as determined with the 15 N-isotope dilution technique. Journal of Animal Science 68: 409418.CrossRefGoogle Scholar
De Simoni, M. G., Del Bo, R., De Luigi, A., Simard, S. and Forloni, G. 1995. Central endotoxin induces different patterns of interleukin (IL)-1β and IL-1 messenger ribonucleic acid expression and IL-6 secretion in the brain and periphery. Endocrinology 136: 897902.CrossRefGoogle Scholar
Dionissopoulos, L., De Lange, C. F. M., Dewey, C., Maclnnes, J. I. and Friendship, R. M. 2001. Effect of healthy management strategy during rearing on grower-finisher pig performance and selected indicators of immune system stimulation. Canadian Journal of Animal Science 81: 179187.CrossRefGoogle Scholar
Elsasser, T. H., Rumsey, T. S. and Hammond, A. C. 1989. Influence of diet on basal and growth hormone stimulated plasma concentrations of IGF-1 in beef cattle. Journal of Animal Science 67: 128141.CrossRefGoogle ScholarPubMed
Fischer, E., Marano, M. A., Van Zee, K. J., Rock, C. S., Hawes, A. S., Thompson, W. A., DeForge, L., Kenney, J. S., Remick, D. G., Bloedow, D. C., Thompson, R. C., Lowry, S. F. and Moldwater, L. L. 1992. Interleukin-1 receptor blockade improves survival and hemodynamic performance in Escherichia coli septic shock, but fails to alter host responses to sublethal endotoxemia. Journal of Clinical Investigation 89: 15511557.CrossRefGoogle ScholarPubMed
Fisher, C. J., Dhainaut, J.-F. A., Opal, S. M., Pribble, J. P., Balk, R. A., Slotman, G. J., Iberti, T. J., Rackow, E. C., Shapiro, M. J., Greenman, R. L., Reines, H. D., Shelly, M. P., Thompson, B. W., LaBrecque, J. F., Catalano, M. A., Knaus, W. A. and Sadoff, J. C. 1994. Recombinant human interleukin-1 receptor antagonist in the treatment of patients with sepsis syndrome: results from a randomized, double-blind, placebo-controlled trial. Journal of the American Medical Assocation 271: 18361843.CrossRefGoogle ScholarPubMed
Frost, R. A., Fuhrer, J., Steigbigel, R., Mariuz, P., Lang, C. H. and Gelato, M. C. 1996. Wasting in the acquired immune deficiency syndrome is associated with multiple defects in the serum insulin-like growth factor system. Clinical Endocrinology 44: 501514.CrossRefGoogle ScholarPubMed
Guyton, A. C. 1991. Textbook of medical physiology. W.B. Saunders Co., Philadelphia.Google Scholar
Johnson, R. W. 1997. Inhibition of growth by pro-inflammatory cytokines: an integrated view. Journal of Animal Science 75: 12441255.CrossRefGoogle ScholarPubMed
Kakucska, I., Qi, Y., Clark, B. D. and Lechan, R. M. 1993. Endotoxin-induced corticotropin-releasing hormone gene expression in the hypothalamic paraventricular nucleus is mediated centrally by interleukin-1. Endocrinology 133: 815882.CrossRefGoogle ScholarPubMed
Klasing, K. C. 1988. Nutritional aspects of leukocytic cytokines. Journal of Nutrition 118: 14361446.CrossRefGoogle ScholarPubMed
Lang, C. H. and Dobrescu, C. 1989. Interleukin-1 induced increases in glucose utilization are insulin mediated. Life Science 45: 21272134.CrossRefGoogle ScholarPubMed
Lang, C. H., Fan, J., Cooney, R. and Vary, T. C. 1996. IL-1 receptor antagonist attenuates sepsis-induced alterations in the IGF system and protein synthesis. American Journal of Physiology 270: E430E437.Google ScholarPubMed
McCarthy, D. O., Kluger, M. J. and Vander, A. J. 1985. Suppression of food intake during infection: is interleukin-1 involved? American Journal of Clinical Nutrition 42: 11791182.CrossRefGoogle ScholarPubMed
McHugh, K. J., Collins, S. M. and Weingarten, H. P. 1994. Central interleukin-1 receptors contribute to suppression of feeding after acute colitis in the rat. American Journal of Physiology 266: R1659R1663.Google ScholarPubMed
Möhn, S. and de Lange, C. F. M. 1998. The effect of body weight on the upper limit to protein deposition in a defined population of growing gilts. Journal of Animal Science 76: 124133.CrossRefGoogle Scholar
Moldovan, M. and May, I. 1975. Taking blood from the orbital sinus of swine. Revista de Cresterea Animalelor 25: 5863.Google Scholar
Molloy, R. G., Mannick, J. A. and Rodrick, M. L. 1993. Cytokines, sepsis, and immunomodulation. British Journal of Surgery 80: 289297.CrossRefGoogle ScholarPubMed
Mulligan, K., Grunfeld, C., Hellerstein, M. K., Neese, R. A. and Shambelan, M. 1993. Anabolic effects of recombinant human growth hormone in patients with wasting associated with human immunodeficiency virus infection. Journal of Clinical Endocrinology and Metabolism 77: 956962.Google ScholarPubMed
National Research Council. 1988. Nutrient requirements of swine. National Academy Press, Washington, DC.Google Scholar
Odink, J., Smeets, J. F. M., Visser, I. J. R., Sandman, H. and Snijders, J. M. A. 1990. Hematological and clinicochemical profiles of healthy swine and swine with inflammatory processes. Journal of Animal Science 68: 163170.CrossRefGoogle ScholarPubMed
Peisen, J. N., McDonnell, K. J., Mulroney, S. E. and Lumpkin, M. D. 1995. Endotoxin-induced suppression of the somatotropic axis is mediated by interleukin-1β and corticotropin-releasing factor in the juvenile rat. Endocrinology 136: 33783390.CrossRefGoogle Scholar
Roitt, I. 1994. Essential immunology. Blackwell Scientific Publications, Oxford.Google Scholar
Romagnani, S. 1994. Lymphokine production by human T cells in disease states. Annual Reviews in Immunology 12: 227257.CrossRefGoogle Scholar
Rowsell, H. C. 1991. The Canadian Council on Animal Care–its guidelines and policy directives: the veterinarian's responsibility. Canadian Journal of Veterinary Research Reviews 55: 205.Google ScholarPubMed
Seckinger, P., Williamson, K., Balavoine, J. F., Mach, B., Mazzei, G., Shaw, A. and Dayer, J. M. 1987. A urine inhibitor of interleukin-1 activity affects both interleukin-1α and 1β but not tumour necrosis factor-α. Journal of Immunology 139: 15411545.CrossRefGoogle Scholar
Statistical Analysis Systems Institute. 2000. SAS version 8. SAS Institute Inc., Cary, NC.Google Scholar
Steele, F. R. 1996. Growth hormone and AIDS-related wasting. Natural Medicines 2: 369370.CrossRefGoogle ScholarPubMed
Van Zee, K. J., Coyle, S. M., Calvano, S. E., Oldenburg, H. S. A., Stiles, D. M., Pribble, J., Catalano, M., Moldwater, L. L. and Lowry, S. F. 1995. Influence of IL-1 receptor blockade on the human response to endotoxemia. Journal of Immunology 154: 14991507.CrossRefGoogle ScholarPubMed
Wakabayashi, G., Gelfand, J. A., Burke, J. F., Thompson, R. C. and Dinarello, C. A. 1991. A specific receptor antagonist for interleukin-1 prevents Escherichia coli-induced shock in rabbits. Federation of American Societies for Experimental Biology Journal 5: 338343.CrossRefGoogle ScholarPubMed
Warren, E. J., Finck, B. N., Arkins, S., Kelley, K. W., Scamurra, R. W., Murtaugh, M. P. and Johnson, R. W. 1997. Coincidental changes in behaviour and plasma cortisol in unrestrained pigs after intracerebroventricular injection of tumour necrosis factor-α. Endocrinology 138: 23652371.CrossRefGoogle Scholar
Webel, D. M., Finck, B. N., Baker, D. H. and Johnson, R. W. 1997. Time course of increased plasma cytokines, cortisol, and urea nitrogen in pigs following intraperitoneal injection of lipopolysaccharide. Journal of Animal Science 75: 15141520.CrossRefGoogle ScholarPubMed
Williams, N. H., Stahly, T. S. and Zimmerman, D. R. 1997. Effect of level of chronic immune system activation on the growth and lysine needs of pigs fed from 6 to 112kg. Journal of Animal Science 75: 24812496.CrossRefGoogle Scholar