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Interactive effects of protein nutrition, genetic growth potential and Heligmosomoides bakeri infection pressure on resilience and resistance in mice

Published online by Cambridge University Press:  18 July 2011

JENNIFER C. COLTHERD ,
SIMON A. BABAYAN ,
LUTZ BÜNGER ,
ILIAS KYRIAZAKIS ,
JUDITH E. ALLEN  and
JOS G. M. HOUDIJK
JENNIFER C. COLTHERD*
Affiliation:
Animal Health, SAC, West Mains Road, Edinburgh EH9 3JG, UK
SIMON A. BABAYAN
Affiliation:
Centre for Immunity, Infection & Evolution and Institute of Immunology and Infection Research, Ashworth Laboratories, King's Buildings, West Mains Road, Edinburgh EH9 3JT, UK
LUTZ BÜNGER
Affiliation:
Sustainable Livestock Systems, SAC, West Mains Road, Edinburgh EH9 3JG, UK
ILIAS KYRIAZAKIS
Affiliation:
Animal Health, SAC, West Mains Road, Edinburgh EH9 3JG, UK
JUDITH E. ALLEN
Affiliation:
Centre for Immunity, Infection & Evolution and Institute of Immunology and Infection Research, Ashworth Laboratories, King's Buildings, West Mains Road, Edinburgh EH9 3JT, UK
JOS G. M. HOUDIJK
Affiliation:
Animal Health, SAC, West Mains Road, Edinburgh EH9 3JG, UK
*
*Corresponding author: Disease Systems Team, SAC, West Mains Road, Edinburgh EH9 3JG, UK. Tel: +44 (0) 131 5353058. Fax: +44 0 131 5353121. E-mail: jcoltherd@hotmail.com
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Summary

The ability of animals to cope with an increasing parasite load, in terms of resilience and resistance, may be affected by both nutrient supply and demand. Here, we hypothesized that host nutrition and growth potential interact and influence the ability of mice to cope with different parasite doses. Mice selected for high (ROH) or low (ROL) body weight were fed a low (40 g/kg; LP) or high (230 g/kg; HP) protein diet and infected with 0, 50, 100, 150, 200 or 250 L3 infective Heligmosomoides bakeri larvae. ROH-LP mice grew less at doses of 150 L3 and above, whilst growth of ROH-HP and of ROL mice was not affected by infection pressure. Total worm burdens reached a plateau at doses of 150L3, whilst ROH mice excreted fewer worm eggs than ROL mice. Serum antibodies increased with infection dose and ROH mice were found to have higher parasite-specific IgG1 titres than ROL mice. In contrast, ROL had higher total IgE titres than ROH mice, only on HP diets. The interaction between host nutrition and growth potential appears to differentially affect resilience and resistance in mice. However, the results support the view that parasitism penalises performance in animals selected for higher growth.

Keywords

minimum level of parasitismHeligmosomoides bakeriprotein nutritiongrowth potentialresilienceresistanceserum antibodymice

Information

Type
Research Article
Information
Parasitology , Volume 138 , Issue 10 , September 2011 , pp. 1305 - 1315
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Albers, G. A., Gray, G. D., Piper, L. R., Barker, J. S., Le Jambre, L. F. and Barger, I. A. (1987). The genetics of resistance and resilience to Haemonchus contortus infection in young merino sheep. International Journal for Parasitology 17, 1355–1363.CrossRefGoogle ScholarPubMed
Anderson, R. M. and Michel, J. F. (1977). Density-dependent survival in populations of Ostertagia ostertagi. International Journal for Parasitology 7, 321–329.CrossRefGoogle ScholarPubMed
Athanasiadou, S., Kyriazakis, I., Jackson, F., and Coop, R. L. (2001). The effects of condensed tannins supplementation of foods with different protein content on parasitism, food intake and performance of sheep infected with Trichostrongylus colubriformis. British Journal of Nutrition 86, 697–706.CrossRefGoogle ScholarPubMed
Bansemir, A. D. and Sukhdeo, M. V. K. (1994). The food resource of adult Heligmosomoides-Polygyrus in the small-intestine. Journal of Parasitology 80, 24–28.CrossRefGoogle ScholarPubMed
Bansemir, A. D. and Sukhdeo, M. V. K. (1996). Villus length influences habitat selection by Heligmosomoides polygyrus. Parasitology 113, 311–316.Google Scholar
Behnke, J. M., Mugambi, J. M., Clifford, S., Iraqi, F. A., Baker, R. L., Gibson, J. P. and Wakelin, D. (2006). Genetic variation in resistance to repeated infections with Heligmosomoides polygyrus bakeri, in inbred mouse strains selected for the mouse genome project. Parasite Immunology 28, 85–94.CrossRefGoogle ScholarPubMed
Behnke, J. M. and Wahid, F. N. (1991). Immunological relationships during primary infection with Heligmosomoides polygyrus (Nematospiroides dubius): H-2 linked genes determine worm survival. Parasitology 103, 157–164.Google Scholar
Bell, R. G., Appleton, J. A., Negrao-Correa, D. and Adams, L. S. (1992). Rapid expulsion of Trichinella spiralis in adult rats mediated by monoclonal antibodies of distinct IgG isotypes. Immunology 75, 520–527.Google ScholarPubMed
Ben-Smith, A., Wahid, F. N., Lammas, D. A. and Behnke, J. M. (1999). The relationship between circulating and intestinal Heligmosomoides polygyrus-specific IgG1 and IgA and resistance to primary infection. Parasite Immunology 21, 383–395.CrossRefGoogle ScholarPubMed
Bishop, S. C. and Stear, M. J. (2000). The use of a gamma-type function to assess the relationship between the number of adult Teladorsagia circumcincta and total egg output. Parasitology 121, 435–440.CrossRefGoogle ScholarPubMed
Bleay, C., Wilkes, C. P., Paterson, S. and Viney, M. E. (2007). Density-dependent immune responses against the gastrointestinal nematode Strongyloides ratti. International Journal for Parasitology 37, 1501–1509.Google Scholar
Boulay, M., Scott, M. E., Conly, S. L., Stevenson, M. M. and Koski, K. G. (1998). Dietary protein and zinc restrictions independently modify a Heligmosomoides polygyrus (Nematoda) infection in mice. Parasitology 116, 449–462.CrossRefGoogle ScholarPubMed
Bransby, D. I. (1993). Effects of grazing management practices on parasite load and weight gain of beef cattle. Veterinary Parasitology 46, 215–221.CrossRefGoogle ScholarPubMed
Bünger, L., Laidlaw, A., Bulfield, G., Eisen, E. J., Medrano, J. F., Bradford, G. E., Pirchner, F., Renne, U., Schlote, W. and Hill, W. G. (2001 a). Inbred lines of mice derived from long-term growth selected lines: unique resources for mapping growth genes. Mammalian Genome 12, 678–686.CrossRefGoogle ScholarPubMed
Bünger, L., Renne, U. and Buis, R. C. (2001 b). Body weight limits in mice. In Encyclopedia of Genetics (ed. Reeve, E. C. R.), pp. 337–360. Fitzroy Dearborn Publishers, London, UK and Chicago, Il, USA.Google Scholar
Christensen, C. M., Barnes, E. H., Nansen, P., Roepstorff, A. and Slotved, H. C. (1995). Experimental Oesophagostomum dentatum infection in the pig: worm populations resulting from single infections with three doses of larvae. International Journal for Parasitology 25, 1491–1498.CrossRefGoogle ScholarPubMed
Christie, M. and Jackson, F. (1982). Specific identification of strongyle eggs in small samples of sheep feces. Research in Veterinary Science 32, 113–117.CrossRefGoogle Scholar
Coltherd, J. C., Bünger, L., Kyriazakis, I. and Houdijk, J. G. M. (2009). Genetic growth potential interacts with nutrition on the ability of mice to cope with Heligmosomoides bakeri infection. Parasitology 136, 1043–1055.CrossRefGoogle ScholarPubMed
Coop, R. L. and Kyriazakis, I. (1999). Nutrition-parasite interaction. Veterinary Parasitology 84, 187–204.Google Scholar
Coop, R. and 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
Coop, R. L., Sykes, A. R. and Angus, K. W. (1982). The Effect of 3 Levels of Intake of Ostertagia-Circumcincta Larvae on Growth-Rate, Food-Intake and Body-Composition of Growing Lambs. Journal of Agricultural Science 98, 247–255.CrossRefGoogle Scholar
Dineen, J. K. (1963). Immunological aspects of parasitism. Nature, London 197, 268–269.CrossRefGoogle ScholarPubMed
Doeschl-Wilson, A. B., Brindle, W., Emmans, G. and Kyriazakis, I. (2009). Unravelling the relationship between animal growth and immune response during micro-parasitic infections. PLoS One 4, e7508.CrossRefGoogle ScholarPubMed
Doeschl-Wilson, A. B., Vagenas, D., Kyriazakis, I. and Bishop, S. C. (2008). Exploring the assumptions underlying genetic variation in host nematode resistance (Open Access publication). Genetics Selection Evolution 40, 241–264.Google ScholarPubMed
Durett-Desset, M. C., Kinsella, J. M. and Forrester, D. J. (1972). [Arguments in favour of a double origin for neartic nematodes of the genus Heligomosomoides Hall, 1916]. Annales de Parasitologie humane et comparée 47, 365–382.Google Scholar
Ehrenford, F. (1954). Effects of dietary protein on the relationship between laboratory mice and the nematode Nematospiroides dubius. Journal of Parasitology 40, 486.CrossRefGoogle Scholar
Emmans, G. C. and 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 (ed. Hill, W. G., Bishop, S. C., McGuirk, B., McKay, J. C., Simm, G. and Webb, A. J.), pp. 36–53. British Society of Animal Science, Edinburgh, UK.Google Scholar
Falconer, D. S. and MacKay, T. F. C. (1996). Introduction to Quantitative Genetics, 4 th Edn. Longman Scientific and Technical, Harlow, UK.Google Scholar
Garside, P., Kennedy, M. W., Wakelin, D. and Lawrence, C. E. (2000). Immunopathology of intestinal helminth infection. Parasite Immunology 22, 605–612.CrossRefGoogle ScholarPubMed
Hastings, I. M. and Hill, W. G. (1989). A note on the effect of different selection criteria on carcass composition in mice. Animal Production 48, 229–233.Google Scholar
Heath, S. C., Bulfield, G., Thompson, R. and Keightley, P. D. (1995). Rates of change of genetic-parameters of body-weight in selected mouse lines. Genetical Research 66, 19–25.CrossRefGoogle ScholarPubMed
Holmes, P. H. (1993). Interactions between parasites and animal nutrition - the veterinary consequences. Proceedings of the Nutrition Society 52, 113–120.CrossRefGoogle ScholarPubMed
Houdijk, J. G. M. and Bünger, L. (2006). Selection for growth increases the penalty of parasitism on growth performance in mice. Proceedings of the Nutrition Society 65, 68A.Google Scholar
Houdijk, J. G. M. and Bünger, L. (2007). Interactive effects of selection for growth and protein supply on the consequences of gastrointestinal parasitism on growth performance in mice. Proceedings of the British Society of Animal Science, 2007 p. 92.CrossRefGoogle Scholar
Houdijk, J. G. M., Jessop, N. S., Knox, D. P. and Kyriazakis, I. (2005). Secondary infection of Nippostrongylus brasiliensis in lactating rats is sensitive to dietary protein content. British Journal of Nutrition 93, 493–499.Google Scholar
Ing, R., Su, Z., Scott, M. E. and Koski, K. G. (2000). Supressed T helper 2 immunity and prolonged survival of a nematode parasite in protein-malnourished mice. Proceedings of the National Academy of Sciences, USA 97, 7078–7083.CrossRefGoogle Scholar
Irvine, R. J., Stien, A., Dallas, J. F., Halvorsen, O., Langvatn, R. and Albon, S. D. (2001). Contrasting regulation of fecundity in two abomasal nematodes of Svalbard reindeer (Rangifer tarandus platyrhynchus). Parasitology 122, 673–681.CrossRefGoogle ScholarPubMed
Jenkins, S. N. and Behnke, J. M. (1977). Impairment of primary expulsion of Trichuris-Muris in mice concurrently infected with Nematospiroides-Dubius. Parasitology 75, 71–78.Google Scholar
Kerboeuf, D. and Jolivet, G. (1984). Heligmosomoides polygyrus: time of anthelmintic treatment and infection parameters in mice exposed to increasing doses of larvae. Experimental Parasitology 57, 307–315.CrossRefGoogle ScholarPubMed
Keymer, A. E. and Slater, A. F. (1987). Helminth fecundity: density dependence or statistical illusion? Parasitology Today 3, 56–58.Google Scholar
Keymer, A. E. and Tarlton, A. B. (1991). The population dynamics of acquired immunity to Heligmosomoides polygyrus in the laboratory mouse: strain, diet and exposure. Parasitology 103, 121–126.CrossRefGoogle ScholarPubMed
Kristan, D. M. and Hammond, K. A. (2001). Parasite infection and caloric restriction induce physiological and morphological plasticity. American Journal of Physiology-Regulatory Integrative and Comparative Physiology 281, R502–R510.Google Scholar
Kristan, D. M. and Hammond, K. A. (2006). Effects of three simultaneous demands on glucose transport, resting metabolism and morphology of laboratory mice. Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology 176, 139–151.Google Scholar
Kidane, A., Houdijk, J. G. M., Tolkamp, B. J., Athanasiadou, S. and Kyriazakis, I. (2009). Consequences of infection pressure and protein nutrition on periparturient resistance to Teladorsagia circumcincta and performance in ewes. Veterinary Parasitology 165, 78–87.Google Scholar
Kyriazakis, I. (2010). Is anorexia during infection in animals affected by food composition? Animal Feed Science and Technology 156, 1–9.CrossRefGoogle Scholar
Kyriazakis, I., Emmans, G. C. and Whittemore, C. T. (1991). The ability of pigs to control their protein intake when fed in three different ways. Physiology and Behaviour 50, 1197–1203.CrossRefGoogle ScholarPubMed
Mortimer, K., Brown, A., Feary, J., Jagger, C., Lewis, S., Antoniak, M., Pritchard, D. and Britton, J. (2006). Dose-ranging study for trials of therapeutic infection with Necator americanus in humans. American Journal of Tropical Medicine and Hygiene 75, 914–920.Google Scholar
Negrao-Correa, D., Adams, L. S. and Bell, R. G. (1999). Variability of the intestinal immunoglobulin E response of rats to infection with Trichinella spiralis, Heligmosomoides polygyrus or Nippostrongylus brasiliensis. Parasite Immunology 21, 287–297.Google Scholar
NRC. (1995). Nutrient Requirements of Laboratory Animals, 4th Edn.National Academy Press, Washington D.C., USA.Google Scholar
Paterson, S. and Viney, M. E. (2002). Host immune responses are necessary for density dependence in nematode infections. Parasitology 125, 283–292.Google Scholar
Poulin, R. (1997). Covariation of sexual size dimorphism and adult sex ratio in parasitic nematodes. Biological Journal of the Linnean Society 62, 567–580.CrossRefGoogle Scholar
Rauw, W., Kanis, E., Noordhuizen-Stassen, E. N. and Grommers, F. J. (1998). Undesirable side effects of selection for high production efficiency in farm animals: a review. Livestock Production Science 56, 15–33.CrossRefGoogle Scholar
Romagnani, S. (1991). Type-1 T-helper and type-2 T-helper cells-functions, regulation and role in protection and disease. International Journal of Clinical and Laboratory Reasearch 21, 152–158.CrossRefGoogle ScholarPubMed
Sandberg, F. B., Emmans, G. C. and Kyriazakis, I. (2006). A model for predicting feed intake of growing animals during exposure to pathogens. Journal of Animal Science 84, 1552–1566.Google Scholar
Silva, A. S., Cavalcante, L. T., Faquim-Mauro, E. L. and Macedo, M. S. (2006). Regulation of anaphylactic IgG1 antibody production by IL-4 and IL-10. International Archives of Allergy and Immunology 141, 70–78.CrossRefGoogle ScholarPubMed
Sripa, B. and Kaewkes, S. (2000). Relationship between parasite-specific antibody responses and intensity of Opisthorchis viverrini infection in hamsters. Parasite Immunology 22, 139–145.Google Scholar
Stien, A., Dallimer, M., Irvine, R. J., Halvorsen, O., Langvatn, R., Albon, S. D. and Dallas, J. F. (2005). Sex ratio variation in gastrointestinal nematodes of Svalbard reindeer; density dependence and implications for estimates of species composition. Parasitology 130, 99–107.Google Scholar
Tu, T., Koski, K. G., Wykes, L. J. and Scott, M. E. (2007). Re-feeding rapidly restores protection against Heligmosomoides bakeri (Nematoda) in protein-deficient mice. Parasitology 134, 899–909.Google Scholar
Urban, J. F., Katona, I. M. and Finkelman, F. D. (1991). Heligmosomoides-Polygyrus - Cd4+ But Not Cd8+ T-Cells regulate the IgE response and protective immunity in mice. Experimental Parasitology 73, 500–511.Google Scholar
Urban, J. F., Madden, K. B., Svetic, A., Cheever, A., Trotta, P. P., Gause, W. C., Katona, I. M. and Finkelman, F. D. (1992). The importance of Th2-cytokines in protective immunity to nematodes. Immunological Reviews 127, 205–220.CrossRefGoogle ScholarPubMed
Vercruysse, J. and Claerebout, E. (2001). Treatment vs non-treatment of helminth infections in cattle: defining the threshold. Veterinary Parasitology 98, 195–214.Google Scholar
Wahid, F. N., Behnke, J. M., Grencis, R. K., Else, K. J. and Ben-Smith, A. W. (1994). Immunological relationships during primary infection with Heligmosomoides polygyrus – Th2 cytokines and primary response phenotype. Parasitology 108, 461–471.Google Scholar