Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-23T08:25:15.495Z Has data issue: false hasContentIssue false
  • English
  • Français

Immune-mediated pathology of nematode infection in sheep – is immunity beneficial to the animal?

Published online by Cambridge University Press:  28 January 2011

ANDREW R. WILLIAMS
ANDREW R. WILLIAMS*
Affiliation:
School of Animal Biology, University of Western Australia, Crawley, WA, 6009, Australia
*
*Corresponding author, present address: The Jenner Institute, University of Oxford, Oxford, OX3 7DQ, UK. Tel: +44 1865 617637. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Nematode parasitism is a severe impediment to sustainable and profitable sheep production in many countries in the world. Parasite resistance to anthelmintic treatment and consumer demand for organic agricultural products has led to much research into harnessing natural immunity as a long-term control measure. However, there is evidence that many of the clinical signs of nematode infection in sheep are due to immune-mediated pathology rather than direct effects of the parasite. Therefore, the desirability of promoting a strong natural immunity in sheep has been questioned. This review attempts to clarify some of the arguments for and against promoting strong natural immunity, particularly through selective breeding of parasite-resistant animals. It is concluded that the detrimental effects of immune-mediated pathology are outweighed by epidemiological and welfare benefits. Thus, control of nematode parasites through selection of naturally resistant sheep is a sustainable and desirable objective.

Keywords

immunitypathologysheepnematode infectionresistancebreeding
Type
Review Article
Information
Parasitology , Volume 138 , Issue 5 , April 2011 , pp. 547 - 556
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Albers, G. A. A., Gray, G. D., Piper, L. R., Barker, J. S. F., 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
Balic, A., Bowles, V., Liu, Y. and Meeusen, E. (2003). Local immune responses in sensitized sheep following challenge infection with Teladorsagia circumcincta. Parasite Immunology 25, 375–381.CrossRefGoogle ScholarPubMed
Balic, A., Bowles, V. M. and Meeusen, E. N. T. (2002). Mechanisms of immunity to Haemonchus contortus infection in sheep. Parasite Immunology 24, 39–46.CrossRefGoogle ScholarPubMed
Barger, I. A. (1993). Influence of sex and reproductive status on the susceptibility of ruminants to nematode infection. International Journal for Parasitology 23, 463–469.CrossRefGoogle Scholar
Bendixsen, T., Emery, D. L. and Jones, W. O. (1995). The sensitisation of mucosal mast cells during infections with Trichostrongylus colubriformis or Haemonchus contortus in sheep. International Journal for Parasitology 25, 741–748.CrossRefGoogle ScholarPubMed
Bendixsen, T., Windon, R. G., Huntley, J. F., MacKellar, A., Davey, R. J., McClure, S. J. and Emery, D. L. (2004). Development of a new monoclonal antibody to ovine chimeric IgE and its detection of systemic and local IgE antibody responses to the intestinal nematode Trichostrongylus colubriformis. Veterinary Immunology and Immunopathology 97, 11–24.CrossRefGoogle Scholar
Bishop, S. C., Bairden, K., McKellar, Q. A., Park, M. and Stear, M. J. (1996). Genetic parameters for faecal egg count following mixed, natural, predominantly Ostertagia circumcincta infection and relationships with liveweight in young lambs. Animal Science 63, 463–468.CrossRefGoogle Scholar
Bishop, S. C., Jackson, F., Coop, R. L. and Stear, M. J. (2004). Genetic parameters for resistance to nematode infections in Texel lambs and their utility in breeding programmes. Animal Science 78, 185–194.CrossRefGoogle Scholar
Bishop, S. C. and Stear, M. J. (2003). Modelling of host genetics and resistance to infectious diseases: understanding and controlling nematode infections. Veterinary Parasitology 115, 147–166.CrossRefGoogle ScholarPubMed
Bisset, S. A. and Morris, C. A. (1996). Feasibility and implications of breeding sheep for resilience to nematode challenge. International Journal for Parasitology 26, 857–868.CrossRefGoogle ScholarPubMed
Bisset, S. A., Vlassoff, A., West, C. J. and Morrison, L. (1997). Epidemiology of nematodosis in Romney lambs selectively bred for resistance or susceptibility to nematode infection. Veterinary Parasitology 70, 255–269.CrossRefGoogle ScholarPubMed
Bouix, J., Krupinski, J., Rzepecki, R., Nowosad, B., Skrzyzala, I., Roborzynski, M., Fudalewicz-Niemczyk, W., Skalska, M., Malczewski, A. and Gruner, L. (1998). Genetic resistance to gastrointestinal nematode parasites in Polish long-wool sheep. International Journal for Parasitology 28, 1797–1804.CrossRefGoogle ScholarPubMed
Clunies-Ross, I. (1932). Observations on the resistance of sheep to infestations by the stomach worm, Haemonchus contortus. Journal of the Council for Scientific and Industrial Research 5, 73–80.Google Scholar
Colditz, I. G. (2003). Metabolic effects of host defence responses during gastrointestinal parasitism in sheep. Australian Journal of Experimental Agriculture 43, 1437–1443.CrossRefGoogle Scholar
Colditz, I. G. (2008). Six costs of immunity to gastrointestinal nematode infections. Parasite Immunology 30, 63–70.CrossRefGoogle ScholarPubMed
Coltman, D., Pilkington, J. G., Kruuk, L. E. B., Wilson, K. and Pemberton, J. M. (2001). Positive genetic correlation between parasite resistance and body size in a free-living ungulate population. Evolution 55, 2116–2125.Google Scholar
Coop, R. L. 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
Dinglasan, R. R. and Jacobs-Lorena, M. (2008). Flipping the paradigm on malaria transmission-blocking vaccines. Trends in Parasitology 24, 364–370.CrossRefGoogle ScholarPubMed
Dobson, R. J., Waller, P. J. and Donald, A. D. (1990). Population dynamics of Trichostrongylus colubriformis in sheep: the effect of host age on the establishment of infective larvae. International Journal for Parasitology 20, 353–357.CrossRefGoogle ScholarPubMed
Doligalska, M., Moskwa, B. and Stear, M. J. (1999). Relationships among peripheral eosinophilia, eosinophil peroxidase activity, interluekin-5 concentration and faecal nematode egg count during natural, mixed gastrointestinal nematode infection. Veterinary Immunology and Immunopathology 70, 299–308.CrossRefGoogle Scholar
Eady, S. J., Woolaston, R. R., Lewer, R. P., Raadsma, H. W., Swan, A. A. and Ponzoni, R. W. (1998). Resistance to nematode parasites in sheep – correlation with production traits. Australian Journal of Agricultural Research 49, 1201–1211.CrossRefGoogle Scholar
Emery, D. L. (1996). Vaccination against worm parasites of animals. Veterinary Parasitology 64, 31–45.CrossRefGoogle ScholarPubMed
Greeff, J. C. and Karlsson, L. J. E. (2006). Breeding for worm resistance- whole farm benefits. International Journal of Sheep and Wool Science 54, 7–14.Google Scholar
Greeff, J. C., Karlsson, L. J. E. and Besier, R. B. (1999). Breeding sheep for resistance to internal parasites. Proceedings of the Australian Association for the Advancement of Animal Breeding and Genetics 13, 150–155.Google Scholar
Greer, A. W. (2008). Trade-offs and benefits: implications of promoting a strong immunity to gastrointestinal parasites in sheep. Parasite Immunology 30, 123–132.CrossRefGoogle Scholar
Greer, A. W., Huntley, J. F., MacKellar, A., McAnulty, R. W., Jay, N. P., Green, R. S., Stankiewicz, M. and Sykes, A. R. (2008). The effect of corticosteroid treatment on local immune responses, intake and performance in lambs infected with Teladorsagia circumcincta. International Journal for Parasitology 38, 1717–1728.CrossRefGoogle ScholarPubMed
Greer, A. W., Stankiewicz, M., Jay, N. P., McAnulty, R. W. and Sykes, A. R. (2005). The effect of concurrent corticosteroid induced immuno-suppression and infection with the intestinal parasite Trichostrongylus colubriformis on food intake and utilization in both immunologically naive and competent sheep. Animal Science 80, 89–99.CrossRefGoogle Scholar
Harrison, G. B. L., Pulford, H. D., Doolin, E. E., Pernthaner, A., Shoemaker, C. B. and Hein, W. R. (2008). Antibodies to surface epitopes of the carbohydrate larval antigen CarLA are associated with passive protection in strongylid nematode challenge infections. Parasite Immunology 30, 577–584.CrossRefGoogle ScholarPubMed
Harrison, G. B. L., Pulford, H. D., Gatehouse, T. K., Shaw, R. J., Pfeffer, A. and Shoemaker, C. B. (1999). Studies on the role of mucus and mucosal hypersensitivity reactions during rejection of Trichostrongylus colubriformis from the intestine of immune sheep using an experimental challenge model. International Journal for Parasitology 29, 459–468.CrossRefGoogle ScholarPubMed
Hurtrez-Bousses, S., Meunier, C., Durand, P. and Renaud, F. (2001). Dynamics of host–parasite interactions: the example of population biology of the liver fluke (Fasciola hepatica). Microbes and Infection 3, 841–849.CrossRefGoogle ScholarPubMed
Jackson, F., Bartley, D. J., Bartley, Y. and Kenyon, F. (2009). Worm control in sheep in the future. Small Ruminant Research 86, 40–45.CrossRefGoogle Scholar
Jacobson, C. L., Bell, K. and Besier, R. B. (2009). Nematode parasites and faecal soiling of sheep in lairage: evidence of widespread potential production losses for the sheep industry. Animal Production Science 49, 326–332.CrossRefGoogle Scholar
Kahn, L. P. (2003). Regulation of the resistance and resilience of periparturient ewes to infection with gastrointestinal nematode parasites by dietary supplementation. Australian Journal of Experimental Agriculture 43, 1477–1485.CrossRefGoogle Scholar
Karlsson, L. J. E. and Greeff, J. C. (2006). Selection response in faecal worm egg counts in the Rylington Merino parasite resistant flock. Australian Journal of Experimental Agriculture 46, 809–811.CrossRefGoogle Scholar
Karlsson, L. J. E., Pollott, G. E., Eady, S. J., Bell, A. and Greeff, J. C. (2004). Relationship between faecal worm egg counts and scouring in Australian Merino sheep. Animal Production in Australia 25, 100–103.Google Scholar
Kemp, J. M., Robinson, N. A., Meeusen, E. N. T. and Piedrafita, D. M. (2009). The relationship between the rapid rejection of Haemonchus contortus larvae with cells and mediators in abomasal tissues in immune sheep. International Journal for Parasitology 39, 1589–1594.CrossRefGoogle ScholarPubMed
Kotze, A. C., O'Grady, J., Emms, J., Toovey, A. F., Hughes, S., Jessop, P., Bennell, M., Vercoe, P. E. and Revell, D. K. (2009). Exploring the anthelmintic properties of Australian native shrubs with respect to their potential role in livestock grazing systems. Parasitology 136, 1065–1080.CrossRefGoogle ScholarPubMed
Larsen, J. W. A., Anderson, N., Vizard, A. L., Anderson, G. A. and Hoste, H. (1994). Diarrhoea in Merino ewes during winter: association with trichostrongylid larvae. Australian Veterinary Journal 71, 365–372.CrossRefGoogle ScholarPubMed
Liu, S. M., Masters, D. G. and Adams, N. R. (2003). Potential impact of nematode parasitism on nutrient partitioning for wool production, growth and reproduction in sheep. Australian Journal of Experimental Agriculture 43, 1409–1417.CrossRefGoogle Scholar
Liu, S. M., Smith, T. L., Briegel, J., Murray, A., Masters, D. G., Karlsson, L. J. E., Palmer, D. G., Greeff, J. C., Besier, R. B. and Gao, S. B. (2005 a). Comparing productive performance of nematode resistant Merino sheep with non-selected control. Livestock Production Science 97, 117–129.CrossRefGoogle Scholar
Liu, S. M., Smith, T. L., Karlsson, L. J. E., Palmer, D. G. and Besier, R. B. (2005 b). The costs for protein and energy requirements by nematode infection and resistance in Merino sheep. Livestock Production Science 97, 131–139.CrossRefGoogle Scholar
McClure, S. J. (2009). Mucosal delivery of native and recombinant protein vaccines against Trichostrongylus colubriformis. International Journal for Parasitology 39, 599–606.CrossRefGoogle ScholarPubMed
McEwan, J. C., Mason, P. C. and Baker, R. L. (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
Meeusen, E. N. T. (1999). Immunology of helminth infections, with special reference to immunopathology. Veterinary Parasitology 84, 259–273.CrossRefGoogle ScholarPubMed
Meeusen, E. N. T., Balic, A. and Bowles, V. (2005). Cells, cytokines and other molecules associated with rejection of gastrointestinal nematode parasites. Veterinary Immunology and Immunopathology 108, 121–125.CrossRefGoogle ScholarPubMed
Miller, H. R. P. (1996). Prospects for the immunological control of ruminant gastrointestinal nematodes: natural immunity, can it be harnessed? International Journal for Parasitology 26, 801–811.CrossRefGoogle ScholarPubMed
Morris, C. A., Vlassoff, A., Bisset, S. A., Baker, R. L., Watson, T. G., West, C. J. and Wheeler, M. (2000). Continued selection of Romney sheep for resistance or susceptibility to nematode infection: estimates of direct and correlated responses. Animal Science 70, 17–28.CrossRefGoogle Scholar
Mulcahy, G., O'Neill, S., Donnelly, S. and Dalton, J. P. (2004). Helminths at mucosal barriers – interaction with the immune system. Advanced Drug Delivery Reviews 56, 853–868.CrossRefGoogle ScholarPubMed
Pernthaner, A., Cole, S., Morrison, L. and Hein, W. R. (2005). Increased expression of Interleukin-5 (IL-5), IL-13, and tumor necrosis factor alpha genes in intestinal lymph cells of sheep selected for enhanced resistance to nematodes during Infection with Trichostrongylus colubriformis. Infection and Immunity 73, 2175–2183.CrossRefGoogle ScholarPubMed
Pollott, G. E. and Greeff, J. C. (2004). Genetic relationships between faecal egg count and production traits in commercial Merino sheep flocks. Animal Science 79, 21–32.CrossRefGoogle Scholar
Pollott, G. E., Karlsson, L. J. E., Eady, S. J. and Greeff, J. C. (2004). Genetic parameters for indicators of host resistance to parasites from weaning to hogget age in Merino sheep. Journal of Animal Science 82, 2852–2864.CrossRefGoogle ScholarPubMed
Riley, E. M., Wahl, S., Perkins, D. J. and Schofield, L. (2006). Regulating immunity to malaria. Parasite Immunology 28, 35–49.CrossRefGoogle ScholarPubMed
Sayers, G. and Sweeney, T. (2005). Gastrointestinal nematode infection in sheep – a review of the alternatives to anthelmintics in parasite control. Animal Health Research Reviews 6, 159–171.CrossRefGoogle ScholarPubMed
Shaw, R. J., Morris, C. A., Green, R. S., Wheeler, M., Bisset, S. A., Vlassoff, A. and Douch, P. G. C. (1999). Genetic and phenotypic relationships among Trichostrongylus colubriformis-specific immunoglobulin E, anti-Trichostrongylus colubriformis antibody, immunoglobulin G, faecal egg count and body weight traits in grazing Romney lambs. Livestock Production Science 58, 25–32.CrossRefGoogle Scholar
Simpson, H. V. (2000). Pathophysiology of abomasal parasitism: is the host or parasite responsible? The Veterinary Journal 3, 177–191.CrossRefGoogle Scholar
Stear, M. J., Boag, B., Cattadori, I. and Murphy, L. (2009). Genetic variation in resistance to mixed, predominantly Teladorsagia circumcincta nematode infections of sheep: from heritabilities to gene identification. Parasite Immunology 31, 274–282.CrossRefGoogle ScholarPubMed
Stear, M. J., Strain, S. and Bishop, S. C. (1999). How lambs control infection with Ostertagia Circumcincta. Veterinary Immunology and Immunopathology 72, 213–218.CrossRefGoogle ScholarPubMed
Steel, J. W., Jones, W. O. and Wagland, B. M. (1990). The response of immune sheep to challenge with Trichostrongylus colubriformis: enteric plasma loss and secretion of biogenic amines. International Journal for Parasitology 20, 1067–1073.CrossRefGoogle ScholarPubMed
Sykes, A. R. (2008). Manipulating host immunity to improve nematode parasite control – Quo vadit. Parasite Immunology 30, 71–77.CrossRefGoogle ScholarPubMed
Sykes, A. R. and Greer, A. W. (2003). Effects of parasitism on the nutrient economy of sheep: an overview. Australian Journal of Experimental Agriculture 43, 1393–1398.CrossRefGoogle Scholar
Wagland, B. M., Emery, D. L. and McClure, S. J. (1996). Studies on the host-parasite relationship between Trichostrongylus colubriformis and susceptible and resistant sheep. International Journal for Parasitology 26, 1279–1286.CrossRefGoogle ScholarPubMed
Wilkie, B. N. and Mallard, B. A. (1999). Selection for high immune response: An alternative approach to animal health maintenance? Veterinary Immunology and Immunopathology 72, 231–235.CrossRefGoogle ScholarPubMed
Williams, A. R., Greeff, J. C., Vercoe, P. E., Dobson, R. J. and Karlsson, L. J. E. (2010 a). Merino ewes bred for parasite resistance reduce larval contamination onto pasture during the peri-parturient period. Animal 4, 122–127.CrossRefGoogle ScholarPubMed
Williams, A. R., Karlsson, L. J. E., Palmer, D. G., Vercoe, P. E., Williams, I. H., Greeff, J. C. and Emery, D. L. (2010 b). Relationships between faecal dry matter, worm burdens and inflammatory mediators and cells in parasite-resistant Merino rams. Veterinary Parasitology 171, 263–272.CrossRefGoogle ScholarPubMed
Williams, A. R., Karlsson, L. J. E., Palmer, D. G., Williams, I. H., Vercoe, P. E., Greeff, J. C. and Emery, D. L. (2008). Increased levels of cysteinyl leukotrienes and prostaglandin E2 in gastrointestinal tract mucus are associated with decreased faecal dry matter in Merino rams during nematode infection. Australian Journal of Experimental Agriculture 48, 873–878.CrossRefGoogle Scholar
Williams, A. R., Palmer, D. G., Williams, I. H., Vercoe, P. E., Emery, D. L. and Karlsson, L. J. E. (2010 c). Relationships between immune indicators of parasitic gastroenteritis, nematode burdens and faecal dry matter in sheep. Animal Production Science 50, 219–227.CrossRefGoogle Scholar
Williamson, J. F., Blair, H. T., Garrick, D. J., Pomroy, W. E., Douch, P. G. C. and Green, R. S. (1997). Parasitological characteristics of fleece-weight selected and control sheep. New Zealand Journal of Agricultural Research 38, 389–397.CrossRefGoogle Scholar
Wuliji, T., Dodds, K. G., Land, J. T. L., Andrews, R. N. and Turner, P. R. (2001). Selection for ultrafine Merino sheep in New Zealand: heritability, phenotypic and genetic correlations of live weight, fleece weight and wool characteristics in yearlings. Animal Science 72, 241–250.CrossRefGoogle Scholar