Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-10T09:01:47.416Z Has data issue: false hasContentIssue false

A mechanistic model of developing immunity to Teladorsagia circumcincta infection in lambs

Published online by Cambridge University Press:  15 October 2010

D. R. SINGLETON*
Affiliation:
The Boyd Orr Centre for Population and Ecosystem Health, Institute of Comparative Medicine, Faculty of Veterinary Medicine, University of Glasgow, Bearsden Road, Glasgow G61 1QH, Scotland
M. J. STEAR
Affiliation:
The Boyd Orr Centre for Population and Ecosystem Health, Institute of Comparative Medicine, Faculty of Veterinary Medicine, University of Glasgow, Bearsden Road, Glasgow G61 1QH, Scotland
L. MATTHEWS
Affiliation:
The Boyd Orr Centre for Population and Ecosystem Health, Institute of Comparative Medicine, Faculty of Veterinary Medicine, University of Glasgow, Bearsden Road, Glasgow G61 1QH, Scotland
*
*Corresponding author: E-mail: darran.singleton@glasgow.ac.uk

Summary

Acquired immunity influences the severity of parasitic disease, but modelling the effects of acquired immunity in helminth infections has proved challenging. This may be due to a lack of suitable immunological data, or to the perceived complexity of modelling the immune response. We have developed a model of T. circumcincta infection in domestic sheep that incorporates the effects of acquired immunity on parasite establishment and fecundity. A large data set from commercially managed populations of Scottish Blackface sheep was used, which included relationships between IgA activity and worm length, and between worm length and fecundity. Use was also made of a recently published meta-analysis of parasite establishment rates. This realistic but simple model of nematode infection emulates observed patterns of faecal egg counts. The end-of-season faecal egg counts are remarkably robust to perturbations in the majority of the parameters, possibly because of priming of the immune system early in the season, reducing parasite establishment and growth and, therefore, faecal egg counts. Lowering the amount of early infection leads to higher end-of-season egg counts. The periparturient rise in egg counts in ewes appears to have an important role in supplying infection for the priming of the immune response. This feedback in the immune priming suggests that nematode infections may be difficult to eliminate.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2010

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

Anderson, R. M. and May, R. M. (1978). Regulation and stability of host-parasite population interactions: I. regulatory processes. Journal of Animal Ecology 47, 219247.Google Scholar
Anderson, R. M. and May, R. M. (1985). Herd immunity to helminth infection and implications for parasite control. Nature, London 315, 493496.Google Scholar
Bartley, D. J., Jackson, F., Jackson, E. and Sargison, N. (2004). Characterisation of two triple resistant field isolates of Teladorsagia from Scottish lowland sheep farms. Veterinary Parasitology 123, 189199.Google 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 live weight in young lambs. Animal Science 63, 423428.Google Scholar
Bishop, S. C. and Stear, M. J. (1997). Modelling responses to selection for resistance to gastro-intestinal parasites in sheep. Animal Science 64, 469478.Google Scholar
Bishop, S. C. and Stear, M. J. (2001). Inheritance of faecal egg counts during early lactation in Scottish Blackface ewes facing mixed, natural nematode infections. Animal Science 73, 389395.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, 325330.Google Scholar
Cornell, S. (2005). Modelling nematode populations: 20 years of progress. Trends in Parasitology 21, 542545.Google Scholar
Gaba, S., Gruner, L. and Cabaret, J. (2006). The establishment rate of a sheep nematode: revisiting classics using a meta-analysis of 87 experiments. Veterinary Parasitology 140, 302311.Google Scholar
Gibson, T. E. and Everett, G. (1972). The ecology of the free-living stages of Ostertagia circumcincta. Parasitology 64, 451460.Google Scholar
Githigia, S. M., Thamsborg, S. M. and Larsen, M. (2001). Effectiveness of grazing management in controlling gastrointestinal nematodes in weaner lambs on pasture in Denmark. Veterinary Parasitology 99, 1527.Google Scholar
Hein, W. R. and Harrison, G. B. L. (2005). Vaccines against veterinary helminths. Veterinary Parasitology 132, 217222.Google Scholar
Henderson, N. G. (2002). Immunity to Teladorsagia circumcincta infection in Scottish Blackface sheep: an investigation into the kinetics of the immune response, antigen recognition and the MHC. Ph.D. thesis, University of Glasgow.Google Scholar
Henderson, N. G. and Stear, M. J. (2006). Eosinophil and IgA responses in sheep infected with Teladorsagia circumcincta. Veterinary Immunology and Immunopathology 112, 6266.Google Scholar
Hong, C., Michel, J. F. and Lancaster, M. B. (1986). Populations of Ostertagia circumcincta in lambs following a single infection. International Journal for Parasitology 16, 6367.Google Scholar
Houdijk, J. G. M., Kyriazakis, I., Jackson, F., Huntley, J. F. and Coop, R. L. (2005). Effects of protein supply and reproductive status on local and systemic immune responses to Teladorsagia circumcincta in sheep. Veterinary Parasitology 129, 105117.Google Scholar
Jackson, F., Jackson, E. and Williams, J. T. (1988). Susceptibility of the pre-parturient ewe to infection with Trichostrongylus vitrinus and Ostertagia circumcincta. Research in Veterinary Science 45, 213218.Google Scholar
Kao, R. R., Leathwick, D. M., Roberts, M. G. and Sutherland, I. A. (2000). Nematode parasites of sheep: a survey of epidemiological parameters and their application in a simple model. Parasitology 121, 85103.Google Scholar
Knox, D. P., Redmond, D. L., Newlands, G. F., Skuce, P. J., Pettit, D. and Smith, W. D. (2003). The nature and prospects for gut membrane proteins as vaccine candidates for Haemonchus contortus and other ruminant trichostrongyloids. International Journal for Parasitology 33, 11291137.Google Scholar
Learmount, J., Taylor, M. A., Smith, G. and Morgan, C. (2006). A computer model to simulate control of parasitic gastroenteritis in sheep on UK farms. Veterinary Parasitology 142, 312329.Google Scholar
Louie, K., Vlassoff, A. and Mackay, A. D. (2007). Gastrointestinal nematode parasites of sheep: a dynamic model for their effect on liveweight gain. International Journal for Parasitology 37, 233241.Google Scholar
Macciotta, N. P. P., Cappio-Borlino, A. and Pulina, G. (2004). Growth and lactation curves. In Genetic Analysis of Complex Traits Using SAS (ed. Saxton, A. M.), pp. 97147. SAS Publishing, Cary, NC, USA.Google Scholar
Nieuwhof, G. J. and Bishop, S. C. (2005). Costs of the major endemic diseases of sheep in Great Britain and the potential benefits of reduction in disease impact. Animal Science 81, 2329.Google Scholar
Niezen, J. H., Charleston, W. A. G., Hodgson, J., Miller, C. M., Waghorn, T. S. and Robertson, H. A. (1998). Effect of plant species on the larvae of gastrointestinal nematodes which parasitise sheep. International Journal for Parasitology 28, 791803.Google Scholar
Niven, P., Anderson, N. and Vizard, A. L. (2002). The integration of grazing management and summer treatments for the control of trichostrongylid infections in Merino weaners. Australian Veterinary Journal 80, 559566.Google Scholar
Perry, B. D. and Randolph, T. F. (1999). Improving the assessment of the economic impact of parasitic diseases and of their control in production animals. Veterinary Parasitology 84, 145168.Google Scholar
Roberts, M. G. (1995). A pocket guide to host-parasite models. Parasitology Today 11, 172177.Google Scholar
Roberts, M. G. and Grenfell, B. T. (1991). The population dynamics of nematode infections of ruminants: periodic perturbations as a model for management. IMA Journal of Mathematics Applied in Medicine & Biology 8, 8393.Google Scholar
Sargison, N. D., Jackson, F., Bartley, D. J., Wilson, D. J., Stenhouse, L. J. and Penny, C. D. (2007). Observations on the emergence of multiple anthelmintic resistance in sheep flocks in the south-east of Scotland. Veterinary Parasitology 145, 6576.Google Scholar
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, 159171.Google Scholar
Seaton, D. S., Jackson, F., Smith, W. D. and Angus, K. W. (1989). Development of immunity to incoming radiolabelled larvae in lambs continuously infected with Ostertagia circumcincta. Research in Veterinary Science 46, 241246.Google Scholar
Smith, G. and Grenfell, B. T. (1985). The population biology of Ostertagia ostertagi. Parasitology Today 1, 7681.Google Scholar
Stear, M. J., Abuagob, O., Benothman, M., Bishop, S. C., Innocent, G., Kerr, A. and Mitchell, S. (2006). Variation among faecal egg counts following natural nematode infection in Scottish Blackface lambs. Parasitology 132, 275280.Google Scholar
Stear, M. J., Bairden, K., Bishop, S. C., Duncan, J. L., Karimi, S. K., McKellar, Q. A. and Murray, M. (1995 a). Different patterns of faecal egg output following infection of Scottish Blackface lambs with Ostertagia circumcincta. Veterinary Parasitology 59, 2938.Google Scholar
Stear, M. J., Bairden, K., Duncan, J. L., Gettinby, G., McKellar, Q. A., Murray, M. and Wallace, D. S. (1995 b). The distribution of faecal nematode egg counts in Scottish Blackface lambs following natural, predominantly Ostertagia circumcincta infection. Parasitology 110, 573581.Google Scholar
Stear, M. J., Bairden, K., Innocent, G. T., Mitchell, S., Strain, S. and Bishop, S. C. (2004). The relationship between IgA activity against 4th-stage larvae and density-dependent effects on the number of 4th-stage larvae of Teladorsagia circumcincta in naturally infected sheep. Parasitology 129, 363369.Google Scholar
Stear, M. J. and Bishop, S. C. (1999). The curvilinear relationship between worm length and fecundity of Teladorsagia circumcincta. International Journal for Parasitology 29, 777780.Google Scholar
Stear, M. J., Bishop, S. C., Doligalska, M., Duncan, J. L., Holmes, P. H., Irvine, J., McCririe, L., McKellar, Q. A., Sinski, E. and Murray, M. (1995 c). Regulation of egg production, worm burden, worm length and worm fecundity by host responses in sheep infected with Ostertagia circumcincta. Parasite Immunology 17, 643652.Google Scholar
Stear, M. J., Bishop, S. C., Mallard, B. A. and Raadsma, H. (2001). The sustainability, feasibility and desirability of breeding livestock for disease resistance. Research in Veterinary Science 71, 17.Google Scholar
Stear, M. J., Doligalska, M. and Donskow-Schmelter, K. (2007). Alternatives to anthelmintics for the control of nematodes in livestock. Parasitology 134, 139151.Google Scholar
Stear, M. J., Park, M. and Bishop, S. C. (1996). The key components of resistance to Ostertagia circumcincta in lambs. Parasitology Today 12, 438441.Google Scholar
Strain, S. A. J., Bishop, S. C., Henderson, N. G., Kerr, A., McKellar, Q. A., Mitchell, S. and Stear, M. J. (2002). The genetic control of IgA activity against Teladorsagia circumcincta and its association with parasite resistance in naturally infected sheep. Parasitology 124, 545552.Google Scholar
Urquhart, G. M., Armour, J., Duncan, J. L., Dunn, A. M. and Jennings, F. W. (1996). Veterinary Parasitology. 2nd Edn. Blackwell Science. Oxford, UK.Google Scholar
Vagenas, D., Bishop, S. C. and Kyriazakis, I. (2007 a). A model to account for the consequences of host nutrition on the outcome of gastrointestinal parasitism in sheep: logic and concepts. Parasitology 134, 12631277.Google Scholar
Vagenas, D., Bishop, S. C. and Kyriazakis, I. (2007 b). A model to account for the consequences of host nutrition on the outcome of gastrointestinal parasitism in sheep: model evaluation. Parasitology 134, 12791289.Google Scholar
Waller, P. J., Dobson, R. J., Donald, A. D. and Thomas, R. J. (1981). Populations of strongyloid nematode infective stages in sheep pastures: comparison between direct pasture sampling and tracer lambs as estimators of larval abundance. International Journal for Parasitology 11, 359367.Google Scholar
Yue, C., Coles, G. and Blake, N. (2003). Multiresistant nematodes on a Devon farm. Veterinary Record 153, 604.Google Scholar