Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-19T23:36:38.476Z Has data issue: false hasContentIssue false
  • English
  • Français

Nutrient partitioning between reproductive and immune functions in animals

Published online by Cambridge University Press:  28 February 2007

Jos G. M. Houdijk ,
Neil S. Jessop  and
Ilias Kyriazakis
Jos G. M. Houdijk*
Affiliation:
Animal Nutrition and Health Department, Animal Biology Division, Scottish Agricultural College, West Mains Road, Edinburgh EH9 3JG, UK
Neil S. Jessop
Affiliation:
Institute of Ecology and Resource Management, The University of Edinburgh, West Mains Road, Edinburgh EH9 3JG, UK
Ilias Kyriazakis
Affiliation:
Animal Nutrition and Health Department, Animal Biology Division, Scottish Agricultural College, West Mains Road, Edinburgh EH9 3JG, UK
*
Corresponding Author: Dr J. G. M. Houdijk, fax +44 131 535 3121, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

The physiological processes that underlie the reproductive cycle impose considerable metabolisable protein (MP) demands on a female, especially during the periparturient period. When MP supply falls short of MP demand (i.e. MP becomes scarce), certain, if not all, bodily functions are expected to be penalised. It has been proposed that partitioning of scarce MP is prioritised to reproductive rather than to immune functions. In other words, at times of MP scarcity, the penalty on expression of immunity would be expected to be greater than that on reproduction. This hypothesis forms a nutritional basis for the occurrence of periparturient breakdown of immunity to parasites (BIP), which can be observed in many host–parasite systems. In the present review we explore this nutritional basis, using periparturient sheep infected with the abomasal nematode Teladorsagia circumcincta as an example, and attempt to quantify its occurrence. Evidence supporting the nutritional basis of periparturient BIP is reviewed, covering experiments in which nutrient supply (from both exogenous and endogenous sources) and/or nutrient demand were manipulated. Quantitatively, MP requirements for expression of immunity to T. circumcincta were estimated to be about 1 g/kg metabolic body weight (body weight0·75) per d, approximately 5 % of the maximum MP requirements of periparturient sheep. The major component of this requirement was assumed to be for replenishing irreversible plasma protein losses into the gastrointestinal tract. Although confirmation of this estimate is required, such estimates may be used to improve the known MP requirements of periparturient animals, enabling the extent and the consequences of periparturient BIP to be minimised.

Keywords

Nutrient partitioning around parturitionImmunity to parasitesProtein requirements of sheep
Type
Symposium on ‘Nutritional adaptation to pregnancy and lactation’
Information
Proceedings of the Nutrition Society , Volume 60 , Issue 4 , November 2001 , pp. 515 - 525
Copyright
Copyright © The Nutrition Society 2001

References

Agricultural and Food Research Council (1993). Energy and Protein Requirements of Ruminants. Wallingford, Oxon: CAB International.Google Scholar
Appleby, BM, Anwar, MA & Petty, SJ (1999) Short-term and long-term effects of food supply on parasite burdens in tawny owls,. Strix aluco. Functional Ecology 13, 315–321.CrossRefGoogle Scholar
Baker, RL, Mwamachi, DM, Audho, JO, Aduda, EO & Thorpe, W (1998) Resistance of Galla and Small East African goats in the sub-humid tropics to gastrointestinal nematode infections and the peri-parturient rise in faecal egg counts. Veterinary Parasitology 79, 53–64.CrossRefGoogle ScholarPubMed
Barger, IA (1993) Influence of sex and reproductive status on susceptibility of ruminants to nematode parasitism. International Journal for Parasitology 23, 463–469.CrossRefGoogle ScholarPubMed
Bauman, DE (2000) Regulation of nutrient partitioning during lactation: homeostasis and homeorhesis revisited. In Ruminant Physiology: Digestion, Metabolism, Growth and Reproduction, pp. 311–328 [Cronjé, PB, editor]. Wallingford, Oxon: CAB International.CrossRefGoogle Scholar
Berghen, P, Dorny, P, Hilderson, H, Vercruysse, J & Hollanders, W (1990) Observations on parasitic gastroenteritis and parasitic bronchitis in calves over two grazing seasons. Veterinary Record 127, 426–430.Google ScholarPubMed
Blaxter, KL (1989) Energy Metabolism in Animals and Man. Cambridge: Cambridge University Press.Google Scholar
Botts, RL, Hemken, RW & Bull, LS (1979) Protein reserves in the lactating dairy cow. Journal of Dairy Science 62, 433–440.CrossRefGoogle ScholarPubMed
Boulay, M, Scott, ME, Conly, SL, Stevenson, MM & Koski, KG (1998) Dietary protein and zinc restrictions independently modify a Heligmosomoides polygyrus (Nematoda) infection in mice. Parasitology 116, 449–462.CrossRefGoogle ScholarPubMed
Bown, MD, Poppi, DP & Sykes, AR (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, PC (1995) Fuel utilisation by cells of the immune system. Proceedings of the Nutrition Society 54, 65–82.CrossRefGoogle ScholarPubMed
Calder, PC & Jackson, AA (2000) Undernutrition, infection and immune function. Nutrition Research Reviews 13, 3–29.CrossRefGoogle ScholarPubMed
Chandra, RK (1991) Nutrition and immunity in the elderly. Nutrition Research Reviews 4, 83–95.CrossRefGoogle ScholarPubMed
Chandra, RK (1997) Nutrition and the immune system: an introduction. American Journal of Clinical Nutrition 66, 460S–463S.CrossRefGoogle ScholarPubMed
Chartier, C, Etter, E, Hoste, H, Pors, I, Mallereau, M-P,, Broqua, C, Mallet, S, Koch, C & Massé, A (2000) Effects of the initial level of milk production and of the dietary protein intake on the course of natural nematode infection in dairy goats. Veterinary Parasitology 92, 1–13.CrossRefGoogle ScholarPubMed
Claerebout, E & Vercruysse, J (2000) The immune response and the evaluation of acquired immunity against gastrointestinal nematodes in cattle: a review. Parasitology 120, S25–S42.CrossRefGoogle ScholarPubMed
Connan, RM (1967) Observations on the epidemiology of parasite gastro-enteritis due to Oesophagostomum spp. and Hydrostrongylus ribidus in the pig. Veterinary Record 80, 424–429.CrossRefGoogle ScholarPubMed
Connan, RM (1972) The effect of host lactation on a second infection of Nippostrongylus brasiliensis in rats. Parasitology 64, 229–233.CrossRefGoogle ScholarPubMed
Coop, RL & Holmes, PH (1996) Nutrition and parasite interaction. International Journal for Parasitology 26, 951–962.CrossRefGoogle ScholarPubMed
Coop, RL & Kyriazakis, I (1999) Nutrition-parasite interaction. Veterinary Parasitology 84, 187–204.CrossRefGoogle ScholarPubMed
Coop, RL & Kyriazakis, I (2001) Influence of host nutrition on the development and consequences of nematode parasitism in ruminants. Trends in Parasitology 17, 325–330.CrossRefGoogle ScholarPubMed
Crofton, HD (1954) Nematode parasite populations in sheep on lowland farms. 1. Worm egg counts in ewes. Parasitology 44, 465–477.CrossRefGoogle ScholarPubMed
Cummins, AG, Duncombe, VM, Bolin, TD, Davis, AE & Yong, J (1987) The response of the small intestine of the protein-deficient rat to infection with Nippostrongylus brasiliensis. International Journal for Parasitology 17, 1445–1450.CrossRefGoogle ScholarPubMed
Donaldson, J, Van Houtert, MFJ & Sykes, AR (1998) The effect of nutrition on the periparturient parasite status of mature ewes. Animal Science 67, 523–533.CrossRefGoogle Scholar
Dröge, W & Breitkreutz, R (2000) Glutathione and immune function. Proceedings of the Nutrition Society 59, 595–600.CrossRefGoogle ScholarPubMed
Else, KJ & Finkelman, FD (1998) Intestinal nematode parasites, cytokines and effector mechanisms. International Journal for Parasitology 28, 1145–1158.CrossRefGoogle ScholarPubMed
Emmans, GE & Fisher, C (1986) Problems in nutritional theory. In Nutrient Requirements of Poultry and Nutritional Research, pp. 9–39 [Fisher, C and Boorman, N, editors]. London: Butterworths.Google Scholar
Fell, BF, Campbell, RM, Mackie, WS & Weekes, TEC (1972) Changes associated with pregnancy and lactation in some extra-reproductive organs of the ewe. Journal of Agricultural Science, Cambridge 79, 397–407.CrossRefGoogle Scholar
Frandson, RD, (1986) Anatomy and Physiology of Farm Animals. Philadelphia, PA: Lea & Febiger.Google Scholar
Gibbs, HC & Barger, IA (1986) Haemonchus contortus and other trichostrongylid infections in parturient, lactating and dry ewes. Veterinary Parasitology 22, 57–66.CrossRefGoogle ScholarPubMed
Goodwill, M, Jessop, NS & Oldham, JD (1996) Mammary sensitivity to protein and energy intakes during lactation. Journal of Dairy Science 79, Suppl. 1, 154.Google Scholar
Groenewald, PCN, Ferreira, AV, van der Merwe, HJ & Slippers, SC (1996) Application of Bayesian inference in the comparison of lactation curves of Merino ewes. Animal Science 62, 63–69.CrossRefGoogle Scholar
Hammond, KA & Diamond, J (1992) An experimental test for a ceiling on sustained metabolic rate in lactating mice. Physiological Zoology 65, 952–977.CrossRefGoogle Scholar
Holmes, PH (1993) Interactions between parasites and animal nutrition: the veterinary consequences. Proceedings of the Nutrition Society 52, 113–120.CrossRefGoogle ScholarPubMed
Hoste, H & Chartier, C (1993) Comparison of the effects on milk production of concurrent infection with Haemonchus contortus and Trichostrongylus colubriformis in high- and low-producing dairy goats. American Journal of Veterinary Research 54, 1886–1893.CrossRefGoogle ScholarPubMed
Houdijk, JGM, Kyriazakis, I, Jackson, F & Coop, RL (2001 a) The relationship between protein nutrition, reproductive effort and breakdown in immunity to Teladorsagia circumcincta in periparturient ewes. Animal Science 72, 595–606.CrossRefGoogle Scholar
Houdijk, JGM, Kyriazakis, I, Jackson, F & Coop, RL (2001 b) The expression of immunity to Teladorsagia circumcincta and its relationship to protein nutrition depend on body protein reserves. Parasitology 122, 661–672.CrossRefGoogle ScholarPubMed
Houdijk, JGM, Kyriazakis, I, Jackson, F, Huntley, JF & Coop, RL (2000) Can an increased metabolizable protein intake affect the periparturient relaxation in immunity against Teladorsagia circumcincta in sheep? Veterinary Parasitology 91, 43–62.CrossRefGoogle ScholarPubMed
Huntley, JF, Gibson, S, Brown, D, Smith, WD, Jackson, F & Miller, HRP (1987) Systemic release of a mast cell proteinase following nematode infections in sheep. Parasite Immunology 9, 603–614.CrossRefGoogle ScholarPubMed
Ilmonen, P, Hakkarainen, H, Koivunen, V, Korpimaki, E, Mullie, A & Shutler, D (1999) Parental effort and blood parasitism in Tengmalm's owl: effects of natural and experimental variation in food abundance. Oikos 86, 79–86.CrossRefGoogle Scholar
Jackson, AA (1998) Salvage of urea-nitrogen in the large bowel: functional significance in metabolic control and adaptation. Biochemical Society Transactions 26, 231–236.CrossRefGoogle ScholarPubMed
Jackson, F, Jackson, E & Williams, JT (1988) Susceptibility of the pre-parturient ewe to infection with Trichostrongylus vitrinus and Ostertagia circumcincta. Research in Veterinary Science 45, 213–218.CrossRefGoogle ScholarPubMed
Jessop, NS (1997) Protein metabolism during lactation. Proceedings of the Nutrition Society 56, 169–175.CrossRefGoogle ScholarPubMed
Kahn, LP, Knox, MR, Gray, GD & Corbett, JL (1999) Enhancing immunity to nematode parasites in pregnant and lactating sheep through nutrition and genetic selection. Recent Advances in Animal Nutrition, Australia 12, 15–22.Google Scholar
Kimambo, AE, MacRae, JC & Dewey, PJS (1988) The effect of daily challenge with Trichostrongylus colubriformis larvae on the nutrition and performance of immunologically-resistant sheep. Veterinary Parasitology 28, 205–212.CrossRefGoogle ScholarPubMed
Klasing, KC & Calvert, CC (1999) The care and feeding of an immune system: an analysis of lysine needs. In Protein Metabolism and Nutrition, pp. 253–264 [Lobley, GE, White, A and MacRae, JC, editors]. Wageningen, The Netherlands: Wageningen Press.Google Scholar
Kloosterman, A, Borgsteede, F & Eysker, M (1984) The effect of experimental. Ostertagia ostertagi infections in stabled milking cows on egg output, serum pepsinogen levels, antibody titres and milk production. Veterinary Parasitology 17, 299–308.CrossRefGoogle Scholar
Lancaster, MB & Andrews, SJ (1991) Observations on the output of nematode eggs in faeces and on the subsequent pasture infestation with third stage larvae produced by a herd of farmed red deer (Cervus elaphus). Veterinary Record 129, 549–551.Google ScholarPubMed
Lewis, RA & Austin, KF (1981) Mediation of local homeostasis and inflammatory by leukotrienes and other mast cell-dependent compounds. Nature 293, 103–108.CrossRefGoogle Scholar
Leyva, V, Henderson, AE & Sykes, AR (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
Lloyd, S (1983) Effect of pregnancy and lactation upon infection. Veterinary Immunology and Immunopathology 4, 153–176.CrossRefGoogle ScholarPubMed
Lloyd, S, Amerasinghe, PH & Soulsby, EJL (1983) Periparturient immunosuppression in the bitch and its influence on infection with Toxocara canis. Journal of Small Animal Practice 24, 237–247.CrossRefGoogle Scholar
MacRae, JC (1993) Metabolic consequences of intestinal parasitism. Proceedings of the Nutrition Society 52, 121–130.CrossRefGoogle ScholarPubMed
Miles, EA & Calder, PC (1998) Modulation of immune function by dietary fatty acids. Proceedings of the Nutrition Society 57, 277–292.CrossRefGoogle ScholarPubMed
Miller, HRP (1984) The protective mucosal response against gastrointestinal nematodes in ruminants and laboratory animals. Veterinary Immunology and Immunopathology 6, 167–259.CrossRefGoogle ScholarPubMed
Miller, HRP (1996) Mucosal mast cells and the allergic response against nematode parasites. Veterinary Immunology and Immunopathology 54, 331–336.CrossRefGoogle ScholarPubMed
Molina, X, Casanova, JC & Feliu, C (1999) Influence of host weight, sex and reproductive status on helminth parasites of the wild rabbit, Oryctolagus cuniculus, in Navarra, Spain. Journal of Helminthology 73, 221–225.CrossRefGoogle ScholarPubMed
Motil, KJ, Montandon, CM, Hachey, DL, Boutbon, TW, Klein, PD & Garza, C (1989) Relationships among lactational performance, maternal diet and body protein metabolism in humans. European Journal of Clinical Nutrition 43, 681–691.Google ScholarPubMed
Naismith, DJ & Morgan, BLG (1976) The biphasic nature of protein metabolism during pregnancy in the rat. British Journal of Nutrition 36, 563–566.CrossRefGoogle ScholarPubMed
Naismith, DJ, Richardson, DP & Pritchard, AE (1982) The utilization of protein and energy during lactation in the rat, with particular regard to the use of that accumulated in pregnancy. British Journal of Nutrition 48, 433–441.CrossRefGoogle Scholar
Ngwenya, BZ (1977) Response of nonsensitized and sensitized lactating mice to infection with Trichinella spiralis. International Journal for Parasitology 7, 41–45.CrossRefGoogle ScholarPubMed
Nordling, D, Andersson, M, Zohari, S & Gustafsson, L (1998) Reproductive effort reduces specific immune response and parasite resistance. Proceedings of the Royal Society of London 265, 1291–1298.CrossRefGoogle Scholar
Norris, K, Anwar, M & Read, AF (1994) Reproductive effort influences the prevalence of haematozoan parasites in great tits. Journal of Animal Ecology 63, 601–610.CrossRefGoogle Scholar
O'Sullivan, BM & Donald, AD (1970) A field study of nematode parasite populations in the lactating ewe. Parasitology 61, 301–315.CrossRefGoogle ScholarPubMed
O'Sullivan, BM & Donald, AD (1973) Responses to infection with Haemonchus contortus and Trichostrongylus colibriformis in ewes of different reproductive status. International Journal for Parasitology 3, 521–530.CrossRefGoogle Scholar
Papadopoulos, E, Sotiraki, S, Stamataris, C, Lainas, T, Himonas, C, Katsaounis, N & Zygoyiannis, D (2000) Effect of undergradable protein on nematode parasites in growing kids and lambs. Proceedings of the 8th Hellenic Veterinary Congress, p. 191. Athens: Greek Veterinary Medical Society.Google Scholar
Parkins, JJ & Holmes, PH (1989) Effects of gastrointestinal helminth parasites on ruminant nutrition. Nutrition Research Reviews 2, 227–246.CrossRefGoogle ScholarPubMed
Pine, AP, Jessop, NS, Allan, GF & Oldham, JD (1994 a) Maternal protein reserves and their influence on lactational performance in rats. 4. Tissue protein synthesis and turnover associated with mobilization of maternal protein. British Journal of Nutrition 72, 831–844.CrossRefGoogle ScholarPubMed
Pine, AP, Jessop, NS & Oldham, JD (1994 b) Maternal protein reserves and their influence on lactational performance in the rat. British Journal of Nutrition 71, 13–27.CrossRefGoogle Scholar
Poelvoorde, J (1973) Epidemiology of an Oesophagostomum spp. infection in boars. Vlaams Diergeneeskundig Tijdschrift 42, 120–124.Google Scholar
Powanda, MC (1977) Changes in body balances of nitrogen and other key nutrients: description and underlying mechanisms. American Journal of Clinical Nutrition 30, 1254–1268.CrossRefGoogle ScholarPubMed
Rauw, WM, Kanis, E, Noordhuizen-Stassen, EN & Grommers, FJ (1998) Undesirable side effects of selection for high production efficiency in farm animals: a review. Livestock Production Science 56, 15–33.CrossRefGoogle Scholar
Reeds, PJ, Fjeld, CR & Jahoor, F (1994) Do the differences between the amino acid compositions of acute-phase and muscle proteins have a bearing on nitrogen loss in traumatic states? Journal of Nutrition 124, 906–910.CrossRefGoogle ScholarPubMed
Richner, H, Christe, P & Oppliger, A (1995) Paternal investment affects prevalence of malaria. Proceedings of the National Academy of Sciences USA 92, 1192–1194.CrossRefGoogle ScholarPubMed
Romjali, E, Dorny, P, Batubara, A, Pandey, VS & Gatenby, RM (1997) Peri-parturient rise in faecal strongyle egg counts of different genotypes of sheep in North Sumatra, Indonesia. Veterinary Parasitology 68, 191–196.CrossRefGoogle ScholarPubMed
Rothwell, TLW (1989) Immune expulsion of parasitic nematodes from the alimentary tract. International Journal for Parasitology 19, 139–168.CrossRefGoogle ScholarPubMed
Rowe, JB, Nolan, JV, Chaneet, GD, Teleni, E & Holmes, PH (1988) The effect of haemonchosis and blood loss into the abomasum on digestion in sheep. British Journal of Nutrition 59, 125–139.CrossRefGoogle ScholarPubMed
Sakanashi, TM, Brigham, HE & Rasmussen, KM (1987) Effect of dietary restriction during lactation on cardiac output, organ blood flow and organ weights of rats. Journal of Nutrition 117, 1469–1474.CrossRefGoogle ScholarPubMed
Selby, GR & Wakelin, D (1975) Suppression of the immune response to Trichuris muris in lactating mice. Parasitology 71, 77–85.CrossRefGoogle ScholarPubMed
Smith, W, Jackson, F, Jackson, E & Williams, J (1983) Local immunity and Ostertagia circumcincta: changes in the gastric lymph of immune sheep after a challenge infection. Journal of Comparative Pathology 93, 479–488.CrossRefGoogle ScholarPubMed
Smith, W, Jackson, F, Jackson, E, Williams, J & Miller, H (1984) Manifestations of resistance to ovine ostertagiasis associated with immunological responses in the gastric lymph. Journal of Comparative Pathology 94, 591–601.CrossRefGoogle ScholarPubMed
Smith, WD, Jackson, F, Jackson, E, Dawson, AM & Burrells, C (1981) Changes in the flow and composition of gastric lymph in sheep repeatedly infected with Ostertagia circumcincta. Journal of Comparative Pathology 91, 553–564.CrossRefGoogle ScholarPubMed
Sykes, AR (2000) Environmental effects on animal production: the nutritional demands of nematode parasite exposure in sheep. Asian Australasian Journal of Animal Sciences 13, 343–350.Google Scholar
Takahashi, K, Ohta, N & Akiba, Y (1997) Influences of dietary methionine and cysteine on metabolic responses to immunological stress by Escherichia coli lipopolysaccharide injection, and mitogenic response in broiler chickens. British Journal of Nutrition 78, 815–821.CrossRefGoogle ScholarPubMed
Taylor, EL (1935) Seasonal fluctuation in the number of eggs of trichostrongylid worms in the faeces of ewes. Journal of Parasitology 21, 175–179.CrossRefGoogle Scholar
Taylor, LM, Parkins, JJ, Arour, J, Holmes, PH, Bairden, K, Ibarra-Silva, AM, Salman, SK & McWilliam, PN (1989) Pathophysiological and parasitological studies on Ostertagia ostertagi infections in calves. Research in Veterinary Science 46, 218–225.CrossRefGoogle ScholarPubMed
Thomas, RJ & Ali, DA (1983) The effect of Haemonchus contortus infection on the pregnant and lactating ewe. International Journal for Parasitology 13, 393–398.CrossRefGoogle ScholarPubMed
Trayhurn, P (1985) Brown adipose tissue thermogenesis and the energetics of lactation in rodents. International Journal of Obesity 9, 81–88.Google ScholarPubMed
Trigg, TE & Topps, JH (1981) Composition of body weight change during lactation in Hereford and Friesian cows. Journal of Agricultural Science, Cambridge 97, 147–157.CrossRefGoogle Scholar
Van Houtert, MFJ, Barger, IA, Steel, JW, Windon, RG & Emery, DL (1995) Effects of dietary protein intake on responses of young sheep to infection with Trichostrongylus colubriformis. Veterinary Parasitology 56, 163–180.CrossRefGoogle ScholarPubMed
Van Houtert, MFJ & Sykes, AR (1996) Implications of nutrition for the ability of ruminants to withstand gastrointestinal nematode infections. International Journal for Parasitology 26, 1151–1168.CrossRefGoogle ScholarPubMed
Van Zon, AAJC & Eling, WMC (1980) Depressed malarial immunity in pregnant mice. Infection and Immunity 28, 630–632.CrossRefGoogle ScholarPubMed
Waller, PJ (1993) Control strategies to prevent resistance. Veterinary Parasitology 46, 133–142.CrossRefGoogle ScholarPubMed
Wiehn, J & Korpimaki, E (1998) Resource levels, reproduction and resistance to haematozoan infections. Proceedings of the Royal Society of London 265, 1197–1201.CrossRefGoogle Scholar
Wiehn, J, Korpimaki, E & Pen, I (1999) Haematozoan infections in the Eurasian kestrel: effects of fluctuating food supply and experimental manipulation of parental effort. Oikos 84, 87–98.CrossRefGoogle Scholar
Xiao, L & Herd, RP (1994) Epidemiology of equine Cryptosporidium and Giardia infections. Equine Veterinary Journal 26, 14–17.CrossRefGoogle ScholarPubMed
Yakoob, A, Holmes, PH & Armour, J (1983) Pathophysiology of gastrointestinal trichostrongyles in sheep: plasma losses and changes in plasma pepsinogen levels associated with parasite challenge of immune animals. Research in Veterinary Science 34, 305–309.CrossRefGoogle ScholarPubMed
Yu, A, Bruce, LA, Calder, AG, Milne, E, Coop, RL, Jackson, F, Horgan, GW & MacRae, JC (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.CrossRefGoogle ScholarPubMed