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The effect of concurrent corticosteroid induced immuno-suppression and infection with the intestinal parasite Trichostrongylus colubriformis on food intake and utilization in both immunologically naïve and competent sheep

Published online by Cambridge University Press:  09 March 2007

A. W. Greer ,
M. Stankiewicz ,
N. P. Jay ,
R. W. McAnulty  and
A. R. Sykes
A. W. Greer*
Affiliation:
Agriculture and Life Sciences Division, PO Box 84, Lincoln University, Canterbury, New Zealand
M. Stankiewicz
Affiliation:
Agriculture and Life Sciences Division, PO Box 84, Lincoln University, Canterbury, New Zealand
N. P. Jay
Affiliation:
Agriculture and Life Sciences Division, PO Box 84, Lincoln University, Canterbury, New Zealand
R. W. McAnulty
Affiliation:
Agriculture and Life Sciences Division, PO Box 84, Lincoln University, Canterbury, New Zealand
A. R. Sykes
Affiliation:
Agriculture and Life Sciences Division, PO Box 84, Lincoln University, Canterbury, New Zealand
*
†E-mail: Greera1@lincoln.ac.nz
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Abstract

The nutritional cost of both the acquisition and maintenance of immunity to gastro-intestinal nematodes was investigated using immunologically naïve 5-month-old lambs and immunologically competent 17-month-old ewes. Within each age cohort, animals were either infected with the equivalent of 80 L3 Trichostrongylus colubriformis larvae per kg live weight (LW) per day (IF), similarly infected and concurrently immuno-suppressed with weekly injections of 1·3 mg/kg LW of the glucocorticoid methylprednisolone acetate (ISIF), immuno-suppressed only (IS) or remained as controls (C). Body composition of all animals was estimated using X-ray computer tomography on days -14 and 76 relative to the start of infection. Body weight and faecal nematode egg counts (FEC; eggs per gram of fresh faeces (e.p.g.)) were taken weekly and blood samples for serum proteins and antibodies were obtained every 2 weeks. FEC in IF lambs peaked at 1250 e.p.g. before a typical decline as immunity developed to less than 100 e.p.g. by day 75. FEC of less than 100 e.p.g. in IF ewes indicated immunity was maintained. Successful immuno-suppression in ISIF lambs and ewes was indicated by FEC of 4000 e.p.g. on day 75 and was confirmed by comparative worm burdens and serum antibody titres. The typical reduction in voluntary food intake (VFI) as a consequence of infection was observed in IF lambs (proportionately 0·30, P < 0·001) but not in IF ewes, ISIF lambs or ISIF ewes. Gross efficiency of use of metabolizable energy for net energy deposition was reduced by proportionately 0·20 in lambs during acquisition of immunity and by 0·16 in ewes maintaining an established immunity. Infection in immuno-suppressed animals reduced efficiency by 0·05 and 0·15 for lambs and ewes, respectively. These findings allowed the hypothesis that the reduction in VFI and loss in performance in young parasitised sheep is caused by physiological signalling associated with the acquisition phase of the host immune response to infection, rather than simply the damage caused by the parasite per se.

Keywords

energy consumptionfood intakeimmunitynematodasheep
Type
Research Article
Information
Animal Science , Volume 80 , Issue 1 , February 2005 , pp. 89 - 99
Copyright
Copyright © British Society of Animal Science 2005

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References

Adams, N. R. and Sanders, M. R. 1992. Improved feed intake and body weight change in sheep treated with dexamethasone at entry into pens or feedlots. Australian Veterinary Journal 69: 209–213CrossRefGoogle ScholarPubMed
Agriculture and Food Research Council. 1993. Energy and protein requirements of ruminants. An advisory manual prepared by the AFRC Technical Committee on Responses to Nutrients. CAB International, Wallingford.Google Scholar
Barger, I. A. and Southcott, W. H. 1975. Trichostrongylosis and wool growth. 3. The wool growth response of resistant grazing sheep to larval challenge. Australian Journal of Experimental Agriculture and Animal Husbandry 15: 167–172.CrossRefGoogle Scholar
Bertozzi, C., Portetelle, D., Massart, S., Prandi, A., Darras, V., Room, G., Tassinari, M., Vleurick, L., Parmentier, I., Haezebroeck, V., Decuypere, E., Burny, A. and Renaville, R. 2000. Dexamethasone ester treatment alters insulin-like growth factor-1, its binding proteins and thyroid status in finishing calves. Canadian Journal of Animal Science 80: 329–335.CrossRefGoogle Scholar
Blaxter, K. L. and Rook, A. J. F. 1953. The heat of combustion of the tissues of cattle in relation to their chemical composition. British Journal of Nutrition 7: 83–91Google Scholar
Bown, M. D., Poppi, D. P. and Sykes, A. R. 1991. The effect of post-ruminal infusion of protein or energy on the pathophysiology of Trichostrongylus colubriformis infection and body composition in lambs. Australian Journal of Agricultural Research 42: 253–267.Google Scholar
Calder, P. and Newsholme, P. 2002. Glutamine and the immune system. In Nutrition and immune function(ed. Calder, P. Field, C. and Gill, H.), pp. 109–132. CAB International, Wallingford.CrossRefGoogle Scholar
Colditz, I. G. 2002. Effects of the immune system on metabolism: implications for production and disease resistance in livestock. Livestock Production Science 75: 257–268.Google Scholar
Coop, R. L. and Holmes, P. H. 1996. Nutrition and parasite interaction. International Journal for Parasitology 26: 951–962.CrossRefGoogle ScholarPubMed
Coop, R. L. and Kyriazakis, I. 1999. Nutrition-parasite interaction. Veterinary Parasitology 84: 187–204.CrossRefGoogle ScholarPubMed
Corah, T. J., Tatum, J. D., Morgan, J. B., Mortimer, R. G. and Smith, G. C. 1995. Effects of a dexamethasone implant on deposition of intramuscular fat in genetically identical cattle. Journal of Animal Science 73: 3310–3316.Google Scholar
Dicke, B. D., Farlin, S. D. and Arthaud, V. H. 1975. Effect of dexamethasone on intramuscular fat content. Journal of Animal Science 39: 168.Google Scholar
Donaldson, J., Houtert van, M. J. F. and Sykes, A. R. 2001. The effect of dietary fish-meal supplementation on parasite burdens of periparturient sheep. Animal Science 72: 149–158.CrossRefGoogle Scholar
Farthing, M. J. G. and Ballinger, A. B. 2001. Anorexia and cytokines in the acute phase response to infection. In Nutrition, immunity and infection in infants and children. Nestle nutrition workshop series, paediatric program, Nestec Ltd(ed. Suskind, R. M. and Tontisirin, K.), pp. 303–317. Lippincott Williams and Wilkins, Philadelphia.Google Scholar
Fourie, P. D., Kirton, A. H. and Jury, K. E. 1970. Growth and development of sheep. II. Effect of breed and sex on the growth and carcass composition of the Southdown and Romney and their cross. New Zealand Journal of Agricultural Research 13: 753–770.CrossRefGoogle Scholar
Gunderson, H. J. G., Bendtsen, T. F., Korbo, L., Marcussen, N., Moller, A., Neilsen, K., Nyengaard, U. R., Pakkenberg, B., Sorensen, F. B., Vesterby, A. and West, M. J. 1988. Some new, simple and ef. cient stereological methods and their use in pathological research and diagnoses. Acta Pathologica, Microbiologica et Immunologica Scandinavica 96: 379–394.CrossRefGoogle Scholar
Hein, W. R., Shoemaker, C. B. and Heath, A. C. G. 2001. Future technologies for control of nematodes of sheep. New Zealand Veterinary Journal 49: 247–251.CrossRefGoogle ScholarPubMed
Houtert, M. F. J. and van Sykes, A. R. 1996. Implications of nutrition for the ability ruminants to withstand gastrointestinal nematode infections. International Journal for Parasitology 26: 1151–1158.CrossRefGoogle ScholarPubMed
Howse, S. W., Blair, H. T., Garrick, D. J. and Pomroy, W. E. 1992. A comparison of internal parasitism in . eeceweight-selected and control Romney sheep. Proceedings of the New Zealand Society of Animal Production 52: 57–60.Google Scholar
Huang, H., Gazzola, C., Pegg, G. G. and Sillence, M. N. 1998. Effect of corticosterone on β-adrenoceptor density in rat skeletal muscle. Journal of Animal Science 76: 999–1003.CrossRefGoogle ScholarPubMed
Husband, A. J. and Bryden, W. J. 1996. Nutrition, stress and immune activation. Proceedings of the Nutrition Society of Australia 20: 60–70.Google Scholar
Johnson, R. W. 1997. Inhibition of growth by pro-in. ammatory cytokines: an integrated view. Journal of Animal Science 75: 1244–1255.Google Scholar
Kahn, L. P., Knox, M. R., Gray, G. D., Lea, J. M. and Walkden-Brown, S. W. 2003. Enhancing immunity to nematode parasites in single-bearing Merino ewes through nutrition and genetic selection. Veterinary Parasitology 112: 211–225.Google Scholar
Kimambo, A. E., MacRae, J. C., Walker, A., Watt, C. F. and Coop, R. L. 1988. Effect of prolonged subclinical infection with Trichostrongylus colubriformis on the performance and nitrogen metabolism of growing lambs. Veterinary Parasitology 28: 191–203.Google Scholar
Kyriazakis, I., Anderson, D. H., Oldham, J. D., Coop, R. L. and Jackson, F. 1996. Long-term subclinical infection with Trichostrongylus colubriformis: effects on food intake, diet selection and performance of growing lambs. Veterinary Parasitology 61: 297–313.Google Scholar
Kyriazakis, I., Tolkamp, B. J. and Hutchings, M. R. 1998. Towards a functional explanation for the occurrence of anorexia during parasitic infections. Animal Behaviour 56: 265–274.Google Scholar
Langhans, W. 2000. Anorexia of infection: current prospects. Nutrition 16: 996–1005.Google Scholar
Lawes Agricultural Trust. 2001. GENSTAT fifth edition, release 4. 22. Rothamsted Experimental Station, Harpenden.Google Scholar
Lawrence, C. E., Kennedy, M. W. and Garside, P. 2001. Gut immunopathology in helminth infections–paradigm lost? In Parasitic nematodes(ed. Harnett, W. and Kennedy, M. W.), pp. 373–397. CAB International, Wallingford.Google Scholar
Leyva, V., Henderson, A. E. and Sykes, A. R. 1982. Effect of daily infection with Ostertagia circumcincta larvae on food intake, milk production and wool growth in sheep. Journal of Agricultural Science, Cambridge 99: 249–259.CrossRefGoogle Scholar
McEwan, J. C., Mason, P., Baker, R. L., Clarke, J. N., Hickey, S. M. and Turner, K. 1992. Effect of selection for productive traits on internal parasite resistance in sheep. Proceedings of the New Zealand Society of Animal Production 52: 53–56.Google Scholar
MacRae, J. C. 1993. Metabolic consequences of intestinal parasitism. Proceedings of the Nutrition Society 52: 121–130.Google Scholar
Ministry of Agriculture, Fisheries and Food. 1979. Manual of veterinary parasitological laboratory techniques. Ministry of Agriculture, Fisheries and Food, Agricultural Development and Advisory Service technical bulletin no. 18. Her Majesty's Stationery Office, London.Google Scholar
Morris, C. A., Bisset, S. A., Vlassoff, A., MacKay, A. D.,Betterridge, K., Alderton, M. J., West, C. J. and Devantier, B. P. 2001. Genetic studies of resilience of Romney sheep to nematode challenge in New Zealand. Proceedings of the New Zealand Society of Animal Production 61: 92–95.Google Scholar
Nagasinha, C. 1999. Effects of Trichostrongylus colubriformis on phosphorus and protein metabolism in sheep. Ph. D. thesis, Lincoln University, Canterbury, New Zealand.Google Scholar
Panaretto, B. A. 1979. Comparisons of the plasma steroid concentration profiles and wool growth responses after administration of two forms of dexamethasone to sheep. Australian Journal of Biological Sciences 32: 343–351.CrossRefGoogle ScholarPubMed
Pernanther, A., Vlassoff, A., Douch, P. G. C. and Maass, D. R. 1997. Cytokine mRNA expression and IFN-γ. production in nematode resistant and susceptible line lambs artificially infected with gastro-intestinal nematodes. Acta Parasitologica 42: 55–61.Google Scholar
Radcliffe, J. and Webster, A. 1976. Regulation of food intake during growth in fatty and lean female Zucker rats given diets of different protein content. British Journal of Nutrition 36: 457–469.CrossRefGoogle ScholarPubMed
Spurlock, M. E. 1997. Regulation of metabolism and growth during immune challenge: an overview of cytokine function. Journal of Animal Science 75: 1773–1783.Google Scholar
Sykes, A. R. 1994. Parasitism and production in farm animals. Animal Production 59: 155–172.Google Scholar
Sykes, A. R. and Coop, R. L. 1976. Intake and utilisation of food by growing lambs with parasitic damage to the small intestine caused by daily dosing with Trichostrongylus colubriformis larvae. Journal of Agricultural Science, Cambridge 86: 507–515.Google Scholar
Thompson, K., Coleman, E. S., Hudmon, A., Kemppainen, R. J., Soyoola, E. O. and Sartin, J. L. 1995. Effects of short-term cortisol infusion on growth hormonereleasing hormone stimulation of growth hormone release in sheep. American Journal of Veterinary Research 56: 1228–1231.Google Scholar
Turini, M. E., Boza, J. J., Gueissaz, N., Moennoz, D., Montigon, F., Vuichoud, J., Gremaud, G., Pouteau, E., Piguet, C., Perrin, I., Verguet, C., Finot, P. A. and German, B. 2003. Short-term dietary conjugated linoleic acid supplementation does not enhance the recovery of immunodepleted dexamethasone-treated rats. European Journal of Nutrition 42: 171–179.Google Scholar
Xie, H. L., Stankiewicz, M. and Huntley, J. F., Sedcole, J. R., McAnulty, R. W., Green, R. S. and Sykes, A. R. 2004. The effects of cold exposure, food allowance and litter size on immunity of periparturient sheep to Teladorsagia circumcincta and Trichostrongylus colubriformis. Animal Science 78: 149–158.CrossRefGoogle Scholar
Young, M. J., Nsoso, S. J., Logan, C. M. and Beatson, P. R. 1996. Prediction of carcass tissue weight in vivo using liveweight, ultrasound or X-ray CT measurements. Proceedings of the New Zealand Society of Animal Production 56: 205–211.Google Scholar
Yu, F., Bruce, L. A. and Calder, A. G., Milne, E., Coop, R. L., Jackson, F., Horgan, G. W. and MacRae, J. C. 2000. Subclinical infection with the nematode Trichostrongylus colubriformis increases gastrointestinal tract leucine metabolism and reduces availability of leucine for other tissues. Journal of Animal Science 78: 380–390.Google Scholar