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Protein supply influences the nutritional penalty associated with the development of immunity in lambs infected with Trichostrongylus colubriformis

Published online by Cambridge University Press:  01 March 2009

A. W. Greer ,
R. J. Sedcole ,
N. P. Jay ,
R. W. McAnulty ,
R. S. Green ,
M. Stankiewicz  and
A. R. Sykes
A. W. Greer*
Affiliation:
Agriculture and Life Sciences Division, Lincoln University, P.O. Box 84, Canterbury, New Zealand
R. J. Sedcole
Affiliation:
Agriculture and Life Sciences Division, Lincoln University, P.O. Box 84, Canterbury, New Zealand
N. P. Jay
Affiliation:
Agriculture and Life Sciences Division, Lincoln University, P.O. Box 84, Canterbury, New Zealand
R. W. McAnulty
Affiliation:
Agriculture and Life Sciences Division, Lincoln University, P.O. Box 84, Canterbury, New Zealand
R. S. Green
Affiliation:
Wallaceville Animal Research Centre, Upper Hutt, New Zealand
M. Stankiewicz
Affiliation:
Agriculture and Life Sciences Division, Lincoln University, P.O. Box 84, Canterbury, New Zealand
A. R. Sykes
Affiliation:
Agriculture and Life Sciences Division, Lincoln University, P.O. Box 84, Canterbury, New Zealand
*
E-mail: Andy.Greer@lincoln.ac.nz
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Abstract

The influence of dietary protein supply on the nutritional penalty associated with the acquisition phase of the immune response to gastrointestinal nematodes in lambs was investigated. Groups of lambs were offered either a low-protein diet (L; 62 g metabolizable protein (MP)/kg dry matter (DM)) or high-protein diet (H; 95 g MP/kg DM) while being either infected with the equivalent of 2.000 L3 Trichostrongylus colubriformis/day (IF), similarly infected and concurrently immuno-suppressed with methylprednisolone acetate (ISIF), immuno-suppressed only (IS) or kept as uninfected controls (C). Body composition of all animals was measured on days −8 and 76 of infection using X-ray computed tomography. Temporal changes in serum phosphate and serum albumin concentrations, which provided an indicator of pathological damage, in addition to patterns of total daily nematode egg excretion and comparative worm burdens at slaughter indicated that a protective immune response was developed in H-IF, but not L-IF, H-ISIF or L-ISIF groups. Compared to their respective non-infected controls, the gross efficiency of use of metabolizable energy (ME) for net energy (NE) deposition in the carcass was reduced by 0.23 in H-IF (P < 0.05), 0.13 in H-ISIF (P > 0.05), 0.49 in L-IF (P < 0.01) and 0.23 in L-ISIF (P > 0.05). It is concluded that the reduction in ME utilization and reduced performance, which can be attributed to the immunological response, are lessened in animals offered a high-protein diet. Furthermore, evidence is presented to indicate a possible association between T. colubriformis L3 IgA antibody production and loss of performance in lambs infected with this nematode.

Keywords

nematodaimmuno-suppressionintakesheeputilization of energy
Type
Full Paper
Information
animal , Volume 3 , Issue 3 , March 2009 , pp. 437 - 445
Copyright
Copyright © The Animal Consortium 2008

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References

Abbott, EM, Parkins, JJ, Holmes, PH 1988. Influence of dietary protein on the pathophysiology of haemonchosis in lambs given continuous infections. Research in Veterinary Science 45, 41–49.CrossRefGoogle ScholarPubMed
Adams, NR, Sanders, MR 1992. Improved feed intake and body weight change in sheep treated with dexamethasone at entry into pens or feedlots. Australian Veterinary Journal 69, 209–213.CrossRefGoogle ScholarPubMed
Agriculture and Food Research Council (AFRC) 1993. Energy and protein requirements of ruminants. An advisory manual prepared by the Agriculture and Food Research Council (AFRC) technical committee on responses to nutrients. CAB International, Wallingford, UK.Google Scholar
Barger, IA, Southcott, WH, Williams, VJ 1973. Trichostrongylosis and wool growth 2. The wool growth response of infected sheep to parenteral and duodenal cysteine and cysteine supplementation. Australian Journal of Experimental Agriculture and Animal Husbandry 13, 351–359.CrossRefGoogle Scholar
Blaxter, KL, Rook, AJF 1953. The heat of combustion of the tissue in cattle in relation to their chemical composition. The British Journal of Nutrition 7, 83–91.CrossRefGoogle ScholarPubMed
Bown, MD, Poppi, DP, Sykes, AR 1991a. 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
Bown, MD, Poppi, DP, Sykes, AR 1991b. Nitrogen transactions along the digestive tract of lambs concurrently infected with Trichostrongylus colubriformis and Ostertagia circumcincta. The British Journal of Nutrition 42, 237–249.CrossRefGoogle Scholar
Coop, RL, Kyriazakis, I 1999. Nutrition–parasite interaction. Veterinary Parasitology 84, 187–204.CrossRefGoogle ScholarPubMed
Coop, RL, Huntley, JF, Smith, WD 1995. Effect of dietary protein supplementation on the development of immunity to Ostertagia circumcincta in growing lambs. Research in Veterinary Science 59, 24–29.CrossRefGoogle ScholarPubMed
Datta, FU, Nolan, JV, Rowe, JB, Gray, GD 1998. Protein supplementation improves the performance of parasitised sheep fed a straw-based diet. International Journal for Parasitology 28, 1269–1278.CrossRefGoogle ScholarPubMed
Donaldson, J, van Houtert, MJF, Sykes, AR 2001. The effect of dietary fish-meal supplementation on parasite burdens of periparturient sheep. Animal Science 72, 149–158.CrossRefGoogle Scholar
Douch, PGC, Green, RS, Risdon, PL 1994. Antibody responses of sheep to challenge with Trichostrongylus colubriformis and the effect of dexamethasone treatment. International Journal for Parasitology 24, 921–928.CrossRefGoogle ScholarPubMed
Else, KJ 2005. Have gastrointestinal nematodes outwitted the immune system. Parasite Immunology 27, 407–415.CrossRefGoogle ScholarPubMed
Greer, AW, McAnulty, RW, Stankiewicz, M, Sykes, AR 2005a. Corticosteroid treatment prevents the reduction in food intake and growth in lambs infected with the abomasal parasite Teladorsagia circumcincta. Proceedings of the New Zealand Society of Animal Production 65, 9–13.Google Scholar
Greer, AW, Stankiewicz, M, Jay, NP, McAnulty, RW, Sykes, AR 2005b. The effect of concurrent corticosteroid-induced immuno-suppression and infection with the intestinal parasite Trichostrongylus colubriformis on feed intake and utilisation in both immunologically naive and competent sheep. Animal Science 80, 89–99.CrossRefGoogle Scholar
Huang, H, Gazzola, C, Pegg, GG, Sillence, MN 1998. Effect of corticosterone on β-adrenoceptor density in rat skeletal muscle. Journal of Animal Science 76, 999–1003.CrossRefGoogle ScholarPubMed
Ing, R, Su, Z, Scott, ME, Koski, KG 2000. Suppressed T helper 2 immunity and prolonged survival of a nematode parasite in protein-malnourished mice. Proceedings of the National Academy of Sciences of the United States of America 97, 7078–7083.CrossRefGoogle ScholarPubMed
Kahn, LP, Kyriazakis, I, Jackson, F, Coop, RL 2000. Temporal effects of protein nutrition on the growth and immunity of lambs infected with Trichostrongylus colubriformis. International Journal for Parasitology 30, 193–205.CrossRefGoogle ScholarPubMed
Kimambo, AE, MacRae, JC, Walker, A, Watt, CF, Coop, RL 1988. Effect of prolonged subclinical infection with Trichostrongylus colubriformis on the performance and nitrogen metabolism of growing lambs. Veterinary Parasitology 28, 191–203.CrossRefGoogle ScholarPubMed
Knox, MR, Steel, JW 1999. The effects of urea supplementation on production and parasitological responses of sheep infected with Haemonchus contortus and Trichostrongylus colubriformis. Veterinary Parasitology 83, 123–135.CrossRefGoogle ScholarPubMed
Kyriazakis, I, Anderson, DH, Oldham, JD, Coop, RL, 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.CrossRefGoogle ScholarPubMed
Lawes Agricultural Trust 2003. GENSTAT, 7th edition, release 7.2. VSN International Ltd., Rothamstead Experimental Station, Harpenden.Google Scholar
MacRae, JC 1993. Metabolic consequences of intestinal parasitism. The Proceedings of the Nutrition Society 52, 121–130.CrossRefGoogle ScholarPubMed
Ministry of Agriculture, Fisheries and Food 1979. Manual of veterinary parasitological laboratory techniques. Ministry of Agriculture, Fisheries and Food (M.A.F.F.), Agricultural Development and Advisory Service Technical Bulletin No. 18. Her Majesty’s Stationary Office, London.Google Scholar
Morris, CA, Vlassoff, A, Bisset, SA, Baker, RL, Watson, TG, West, CJ, Wheeler, M 2000. Continued selection of Romney sheep for resistance or susceptibility to nematode infection: estimates of direct and correlated responses. Animal Science 70, 17–27.CrossRefGoogle Scholar
Morris, CA, Wheeler, M, Watson, TG, Hosking, BC, Leathwick, DM 2005. Direct and correlated responses to selection for high or low faecal nematode egg count in Perendale sheep. New Zealand Journal of Agricultural Research 48, 1–10.CrossRefGoogle Scholar
Panaretto, BA 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
Pernthaner, A, Shaw, RJ, McNeill, MM, Morrison, L, Hein, WR 2005. Total nematode-specific IgE responses in intestinal lymph of genetically resistant and susceptible sheep during infection with Trichostrongylus colubriformis. Veterinary Immunology and Immunopathology 104, 69–80.CrossRefGoogle ScholarPubMed
Pernthaner, A, Cole, SA, Morrison, L, Green, R, Shaw, RJ, Hein, WR 2006. Cytokine and antibody subclass responses in the intestinal lymph of sheep during repeated experimental infections with the nematode parasite Trichostrongylus colubriformis. Veterinary Immunology and Immunopathology 114, 135–148.CrossRefGoogle ScholarPubMed
Stear, MJ, Bishop, SC, Doligalska, M, Duncan, JL, Holmes, PH, Irvine, J, McCririe, L, McKellar, QA, Sinski, E, Murray, M 1995. Regulation of egg production, worm burden, worm length and worm fecundity by host responses in sheep infected with Ostertagia circumcincta. Parasite Immunology 17, 643–652.CrossRefGoogle ScholarPubMed
Steel, JW, Symons, LEA, Jones, WO 1980. Effects of level of larval intake on the productivity and physiological and metabolic responses of lambs infected with Trichostrongylus colubriformis. Australian Journal of Agricultural Research 31, 821–838.CrossRefGoogle Scholar
Sykes, AR, Coop, RL 1976. Intake and utilization 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.CrossRefGoogle Scholar
Turini, ME, Boza, JJ, Gueissaz, N, Moennoz, D, Montigon, F, Vuichoud, J, Gremaud, G, Pouteau, E, Piguet, C, Perrin, I, Verguet, C, Finot, PA, 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.CrossRefGoogle Scholar
van Houtert, MFJ, Sykes, AR 1996. Implications of nutrition for the ability ruminants to withstand gastrointestinal nematode infections. International Journal for Parasitology 26, 1151–1158.CrossRefGoogle ScholarPubMed
van Houtert, MFJ, Barger, IA, Steel, JW 1995. Dietary protein for young grazing sheep: interactions with gastrointestinal parasitism. Veterinary Parasitology 60, 283–295.CrossRefGoogle ScholarPubMed
Vaughan, AL, Greer, AW, McAnulty, RW, Sykes, AR 2006. Plasma protein loss in lambs during a mixed infection of Trichostrongylus colubriformis and Teladorsagia circumcincta – a consequence of the immune response? Proceedings of the New Zealand Society of Animal Production 66, 83–87.Google Scholar
Wilson, WD, Field, AC 1983. Absorption and secretion of calcium and phosphorus in the alimentary tract of lambs infected with daily doses of Trichostrongylus colubriformis or Ostertagia circumcincta larvae. Journal of Comparative Pathology 93, 61–71.CrossRefGoogle ScholarPubMed
Xie, HL, Stankiewicz, M, Huntley, JF, Sedcole, JR, McAnulty, RW, Green, RS, Sykes, AR 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
Zhou, H, Hickford, JGH, Fang, Q 2005. Polymorphism if the IGHA gene in sheep. Immunogenetics 57, 453–457.CrossRefGoogle ScholarPubMed