Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-25T02:56:27.890Z Has data issue: false hasContentIssue false
  • English
  • Français

Secondary infection of Nippostrongylus brasiliensis in lactating rats is sensitive to dietary protein content

Published online by Cambridge University Press:  08 March 2007

Jos G. M. Houdijk ,
Neil S. Jessop ,
David P. Knox  and
Ilias Kyriazakis
Jos G. M. Houdijk*
Affiliation:
Animal Nutrition and Health Department, Scottish Agricultural College, West Mains Road, Edinburgh, EH9 3JG, UK
Neil S. Jessop
Affiliation:
Institute of Atmospheric and Environmental Sciences, School of GeoSciences, University of Edinburgh, West Mains Road, Edinburgh, EH9 3JG, UK
David P. Knox
Affiliation:
Parasitology Division, Moredun Research Institute, Pentland Science Park, Bush Loan, Penicuik, EH26 0PZ, UK
Ilias Kyriazakis
Affiliation:
Animal Nutrition and Health Department, Scottish Agricultural College, West Mains Road, Edinburgh, EH9 3JG, UK
*
*Corresponding author: Dr Jos Houdijk, fax +44 131 535 3416, 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.

Lactating mammals usually exhibit a breakdown of immunity to parasites, i.e. they have larger worm burdens than their non-lactating counterparts. Here, we tested the hypothesis that a secondary infection with Nippostrongylus brasiliensis in lactating rats is sensitive to dietary protein content. We also tested whether this infection affects host food intake. Rats either remained uninfected throughout the study or were given a single infection before mating (primary infection) and re-infected on day 2 of lactation (secondary infection) with 1600 infective larvae. Infected rats were fed foods during lactation formulated to supply 100 (low protein; LP), 200 (medium protein; MP) or 300 (high protein; HP) g crude protein per kg DM; non-infected rats were fed either the LP or HP food. Litter size was standardized to ten pups between parturition (day 0) and secondary infection (day 2). Ten days after secondary infection, MP and HP rats had excreted fewer nematode eggs, and had fewer adult nematodes in their small intestine and nematode eggs in their colon than the LP rats. Primary infection increased food intake in late pregnancy, and increased maternal body weight and litter size at parturition. Secondary infection did not affect mean food intake, maternal and litter weight, although food intake was reduced for 1 d following infection. These results support the view that a secondary infection with N. brasiliensis is sensitive to dietary protein content, and that the latter infection does not impair lactational performance. Future studies may focus on elucidating the nutritional sensitivity of immune responses underlying the reduced secondary N. brasiliensis infection.

Keywords

Lactating ratsNippostrongylus brasiliensisNutritionImmunityProtein
Type
Research Article
Information
British Journal of Nutrition , Volume 93 , Issue 4 , April 2005 , pp. 493 - 499
Copyright
Copyright © The Nutrition Society 2005

References

Barger, IA (1993) Influence of sex and reproductive status on susceptibility of ruminants to nematode parasitism. Int J Parasitol 23, 463–469.CrossRefGoogle ScholarPubMed
Bolin, TD, Davis, AE, Cummins, AG, Duncombe, VM & Kelly, JD (1977) Effect of iron and protein deficiency on the expulsion of Nippostrongylus brasiliensis from the small intestine of the rat. Gut 18, 182–186.Google Scholar
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. Austr J Agric Res 42, 253–267.Google Scholar
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. Vet Parasitol 92, 1–13.CrossRefGoogle ScholarPubMed
Chemical Rubber Company (2001) Handbook of Chemistry and Physics 82nd ed. LondonCRC PressGoogle Scholar
Coop, RL & Kyriazakis, I (1999) Nutrition–parasite interaction. Vet Parasitol 84, 187–204.Google Scholar
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. Int J Parasitol 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. Anim Sci 67, 523–533.CrossRefGoogle Scholar
Donaldson, J, van Houtert, MFJ & Sykes, AR (2001) The effect of dietary fish-meal supplementation on parasite burdens of periparturient sheep. Anim Sci 72, 149–158.CrossRefGoogle Scholar
Emmans, GC & Kyriazakis, I (2000) Issues arising from genetic selection for growth and body composition characteristics in poultry and pigs. In The Challenge of Genetic Change in Animal Production, pp. 36–53 [Hill, WG, Bishop, SC, McGuirk, B, McKay, JC, Simm, G, Webb, AJ, editors]. Edinburgh: British Society of Animal Science.Google Scholar
Friggens, NC, Hay, DEF & Oldham, JD (1993) Interactions between major nutrients in the diet and the lactational performance of rats. Br J Nutr 69, 59–71.Google Scholar
Herbert, IV & Nickson, EW (1969) Dietary factors and the production of Oesophagostomum sp. ova in breeding pigs. Vet Rec 84, 569–570.Google Scholar
Houdijk, JGM, Kyriazakis, I, Jackson, F & Coop, RL (2000) Effects of protein and energy supply on the resistance to nematodes in pregnant ewes. Proc Br Soc Anim Sci 116, 33.CrossRefGoogle Scholar
Houdijk, JGM, Jessop, NS & Kyriazakis, I (2001) Nutrient partitioning between reproductive and immune functions in animals. Proc Nutr Soc 60, 515–525.CrossRefGoogle ScholarPubMed
Houdijk, JGM, Kyriazakis, I, Coop, RL & Jackson, F (2001) The relationship between protein nutrition, reproductive effort and breakdown in immunity to Teladorsagia circumcincta in periparturient ewes. Anim Sci 72, 595–606.Google Scholar
Houdijk, JGM, Jessop, NS, Knox, DP & Kyriazakis, I (2003) Breakdown of immunity to Nippostrongylus brasiliensis in lactating rats. Br J Nutr 90, 809–814.Google Scholar
Houdijk, JGM, Kyriazakis, I, Jackson, F & Coop, RL (2003) Reducing the degree of protein scarcity rapidly increases immunity to nematodes in ewes. Proc Br Soc Anim Sci 119, 29.Google Scholar
Houdijk, JGM, Kyriazakis, I, Jackson, F, Huntley, JF & Coop, RL (2003) Is the allocation of metabolisable protein prioritised to milk production rather than to immune functions in Teladorsagia circumcincta -infected lactating ewes?. Int J Parasitol 33, 327–338.Google Scholar
Jarrett, EEE, Jarrett, WFH & Urquhart, GM (1968) Quantitative studies on the kinetics of establishment and expulsion of intestinal nematode populations in susceptible and immune hosts. Nippostrongylus brasiliensis in the rat. Parasitology 58, 625–639.Google Scholar
Jessop, NS (1997) Protein metabolism during lactation. Proc Nutr Soc 56, 169–175.Google Scholar
Johnson, NL, Kotz, S & Balakrishnan, N (1988) Continuous Univariate Distributions 2nd ed. Boston, MA: PWS-KENTGoogle Scholar
Kahn, LP, Knox, MR, Gray, GD, Lea, JM, Walkden-Brown, SW (2003) Enhancing immunity to nematode parasites in single-bearing Merino ewes through nutrition and genetic selection. Vet Parasitol 112, 211–225.Google Scholar
Koski, KG & Scott, ME (2001) Gastrointestinal nematodes, nutrition and immunity: breaking the negative spiral. Annu Rev Nutr 21, 297–321.Google Scholar
Kristan, DM (2004) Intestinal nematode infection affects host life history and offspring susceptibility to parasitism. J Anim Ecol 73, 227–238.Google Scholar
Kyriazakis, I, Tolkamp, BJ & Hutchings, MR (1998) Towards a functional explanation of the occurrence of anorexia during parasitic infections. Anim Behav 56, 265–274.CrossRefGoogle ScholarPubMed
Littel, RC, Henry, PR & Ammerman, CB (1998) Statistical analysis of repeated measures data using SAS procedures. J Anim Sci 76, 1216–1231.CrossRefGoogle Scholar
Mahan, DC & Mangan, LT (1975) Evaluation of various protein sequences on the nutritional carry over from gestation to lactation with first litter sows. J Nutr 105, 1291–1298.CrossRefGoogle ScholarPubMed
Mercer, JG, Mitchell, PI, Moar, KM, Bisset, A, Geissler, S, Bruce, K & Chappell, LH (2000) Anorexia in rats infected with the nematode Nippostrongylus brasiliensis: experimental manipulations. Parasitology 120, 641–647.Google Scholar
National Research Council (1995) Nutrient Requirements of Laboratory Animals, 4th ed. Washington, DC: National Academy Press.Google Scholar
Pearce, GP (1999) Interactions between dietary fibre, endo-parasites and Lawsonia intracellularis bacteria in grower-finisher pigs. Vet Parasitol 87, 51–61.Google Scholar
Petkevicius, S, Nansen, P, Bach, KKE & Skjoth, F (1999) The effect of increasing levels of insoluble dietary fibre on the establishment and persistence of Oesophagostomum dentatum in pigs. Parasite 6, 17–26.Google Scholar
Petkevicius, S, Knudsen, KEB, Murrell, KD & Wachmann, H (2003) The effect of inulin and sugar beet fibre on Oesophagostomum dentatum infection in pigs. Parasitology 127, 61–68.Google Scholar
Pine, AP, Jessop, NS & Oldham, JD (1994) Maternal protein reserves and their influence on lactational performance in rats. Br J Nutr 71, 13–27.Google Scholar
Rothwell, TLW (1989) Immune expulsion of parasitic nematodes from the alimentary tract. Int J Parasitol 19, 139–168.CrossRefGoogle ScholarPubMed
Taylor, EL (1935) Seasonal fluctuation in the number of eggs of trichostrongylid worms in the faeces of ewes. J Parasitol 21, 175–179.Google Scholar
Tolkamp, BJ, Dewhurst, RJ, Friggens, NC, Kyriazakis, I, Veerkamp, RF & Oldham, JD (1998) Diet choice by dairy cows. 1. Selection of feed protein content during the first half of lactation. J Dairy Sci 81, 2657–2669.CrossRefGoogle ScholarPubMed
Yaqoob, P (2004) Fatty acids and the immune system: from basic science to clinical applications. Proc Nutr Soc 63, 89–104.Google Scholar