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Modelling gastrointestinal parasitism infection in a sheep flock over two reproductive seasons: in silico exploration and sensitivity analysis

  • M. SACCAREAU (a1), C. R. MORENO (a1), I. KYRIAZAKIS (a2), R. FAIVRE (a3) and S. C. BISHOP (a4)...

Summary

In reproducing ewes, a periparturient breakdown of immunity is often observed to result in increased fecal egg excretion, making them the main source of infection for their immunologically naive lambs. In this study, we expanded a simulation model previously developed for growing lambs to explore the impact of the genotype (performance and resistance traits) and host nutrition on the performance and parasitism of both growing lambs and reproducing ewes naturally infected with Teladorsagia circumcincta. Our model accounted for nutrient-demanding phases, such as gestation and lactation, and included a supplementary module to manage the age structure of the ewe flock. The model was validated by comparison with published data. Because model parameters were unknown or poorly estimated, detailed sensitivity analysis of the model was performed for the sheep mortality and the level of infection, following a preliminary screening step. The parameters with the greatest effect on parasite-related outputs were those driving animal growth and milk yield. Our model enables different parasite-control strategies (host nutrition, breeding for resistance and anthelmintic treatments) to be assessed on the long term in a sheep flock. To optimize in silico exploration, the parameters highlighted by the sensitivity analysis should be refined with real data.

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This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.

Corresponding author

*Corresponding author: GenPhySE, INRA, INPT, INP-ENVT, Université de Toulouse, Castanet Tolosan, France. E-mail: mathilde.saccareau@toulouse.inra.fr

References

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AFRC (1990). Nutritive Requirements of Ruminant Animals: Energy. CAB International, Wallingford, Oxon.
AFRC (1993). Energy and Protein Requirements of Ruminants. An Advisory Manual Prepared by the AFRC Technical Committee on Response to Nutrients. CAB International, Wallingford, UK.
ARC (1980). The Nutrient Requirements of Ruminant Livestock. Commonwealth Agricultural Bureau, Farnham Royal, UK.
Arranz, J. M. (2012). Changements observés dans les prairies permanentes de l'extrême sud-ouest de la France et perspectives pour les systèmes d’élevages herbivores. Journées de l'Association Française pour la Production Fourragère, 3–4 avril 2012, Paris.
Arranz, J. M. and Bocquier, F. (1995). Production et valorisation hivernale de la prairie permanente par les brebis laitières en Pyrénées-Atlantiques. Proceedings of the Rencontres Recherche Ruminants, Paris, 2, 109–112.
Astruc, J.-M., Barillet, F. and Lagriffoul, G. (2013). Report of the annual meeting of the Comité National Brebis Laitière, Toulouse, 16–17 octobre 2013.
Barger, I. A. (1993). Influence of sex and reproductive status on susceptibility of ruminants to nematode parasitism. Special Issue: Proceedings of the Joint Conference of the Australian and New Zealand Societies for Parasitology, 1992 23, 463469.
Barillet, F., Astruc, J.-M., Lagriffoul, G., Aguerre, X. and Bonaïti, B. (2008). Selecting milk composition and mastitis resistance by using a part lactation sampling design in French Manech red faced dairy sheep breed. Proceedings of International Comittee for Animal Recording, Niagara, 16–20 juin 2008.
Bishop, S. C. and Morris, C. A. (2007). Genetics of disease resistance in sheep and goats. Special Issue: the Outlook of Quantitative and Molecular Genetics Applications in Improving Sheep and Goats 70, 4859.
Bishop, S. C. and Stear, M. J. (1997). Modelling responses to selection for resistance to gastro-intestinal parasites in sheep. Animal Science 64, 469478.
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.
Boag, B., Topham, P. B. and Webster, R. (1989). Spatial distribution on pasture of infective larvae of the gastro-intestinal nematode parasites of sheep. International Journal for Parasitology 19, 681685.
Boyazoglu, J. G. (1963). Aspects quantitatif de la production laitière des brebis. I. Mise au point bibliographique. Annales de zootechnie 12, 237296.
Callinan, A. P. L., Morley, F. H. W., Arundel, J. H. and White, D. H. (1982). A model of the life cycle of sheep nematodes and the epidemiology of nematodiasis in sheep. Agricultural Systems 9, 199225.
Carnell, R. (2012). lhs: Latin Hypercube Samples. R package version 0.10.
Coffey, M. P., Emmans, G. C. and Brotherstone, S. (2001). Genetic evaluation of dairy bulls for energy balance traits using random regression. Animal Science – Glasgow 73, 2940.
Coop, R. L., Sykes, A. R. and Angus, K. W. (1982). The effect of three levels of intake of Ostertagia circumcincta larvae on growth rate, food intake and body composition of growing lambs. Journal of Agricultural Science, Cambridge 98, 247255.
Cronjé, P. B. and Smuts, M. (1994). Nutrient partitioning in Merino rams with different wool growth rates. Animal Science 59, 5560.
de Almeida, F. A., da Sobrinho, A. G. S., Endo, V., Lima, N. L. L., Columbeli, A. C., Zeola, N. M. B. L. and Barbosa, J. C. (2012). Gastrointestinal nematodes infection of primiparous and multiparous ewe in different reproductive stages. Journal of Animal and Veterinary Advances 2, 373378.
Doeschl-Wilson, A. B., Vagenas, D., Kyriazakis, I. and Bishop, S. C. (2008). Exploring the assumptions underlying genetic variation in host nematode resistance. Genetics Selection Evolution 40, 241264.
Emmans, G. C. (1994). Effective energy: a concept of energy utilization applied across species. British Journal of Nutrition 71, 801821.
Emmans, G. C. (1997). A method to predict the food intake of domestic animals from birth to maturity as a function of time. Journal of Theoretical Biology 186, 189199.
Emmans, G. C. and Fisher, C. (1986). Problems of Nutriotional theory. In Nutritional Requirements and Nutritional Theory (ed. Fisher, C. and Boorman, K. N.), pp. 957. Butterworths, London.
Emmans, G. C. and Kyriazakis, I. (1997). Models of pig growth: problems and proposed solutions. Livestock Production Science 51, 119129.
Emmans, G. C. and Kyriazakis, I. (1999). Growth and body composition. In A Quantitative Biology of the Pig (ed. Kyriazakis, I.), pp. 181197. CAB International, Wallingford, UK.
Emmans, G. C. and Kyriazakis, I. (2001). Consequences of genetic change in farm animals on food intake and feeding behaviour. Proceedings of the Nutrition Society 60, 115125.
Faivre, R. (2013). Exploration par construction de métamodèles. In Analyse de sensibilité et exploration de modèles. Applications aux modèles environnementaux (ed. Faivre, R., Iooss, B., Mahévas, S., Makowski, D. and Monod, H.), pp. 159194. Quae, Versailles.
Faivre, R., Iooss, B., Mahévas, S., Makowski, D. and Monod, H. (2013). Analyse de sensibilité et exploration de modèles. Applications aux modèles environnementaux. Quae, Versailles.
Fox, N. J., Marion, G., Davidson, R. S., White, P. C. L. and Hutchings, M. R. (2013). Modelling parasite transmission in a grazing system: the importance of host behaviour and immunity. PLoS ONE 8, e77996.
Gaba, S., Cabaret, J., Ginot, V. and Silvestre, A. (2006). The early drug selection of nematodes to anthelmintics: stochastic transmission and population in refuge. Parasitology 133, 345356.
Houdijk, J. G., Kyriazakis, I., Jackson, F., Huntley, J. and Coop, R. (2003). Is the allocation of metabolisable protein prioritised to milk production rather than to immune functions in Teladorsagia circumcincta-infected lactating ewes? International Journal for Parasitology 33, 327338.
Houdijk, J. G. M. (2008). Influence of periparturient nutritional demand on resistance to parasites in livestock. Parasite Immunology 30, 113121.
Houdijk, J. G. M., Jessop, N. S. and Kyriazakis, I. (2001). Nutrient partitioning between reproductive and immune functions in animals. Proceedings of the Nutrition Society 60, 515525.
Inra Tables (2007). Alimentation des bovins, ovins et caprins. Quae, Versailles, France.
Jackson, F., Greer, A. W., Huntley, J., McAnulty, R. W., Bartley, D. J., Stanley, A., Stenhouse, L., Stankiewicz, M. and Sykes, A. R. (2004). Studies using Teladorsagia circumcincta in an in vitro direct challenge method using abomasal tissue explants. Veterinary Parasitology 124, 7389.
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.
Karlsson, L. J. E. and Greeff, J. C. (2012). Genetic aspects of sheep parasitic diseases. Veterinary Parasitology 189, 104112.
Kyriazakis, I. (2014). Pathogen-induced anorexia: a herbivore strategy or an unavoidable consequence of infection? Animal Production Science 54, 11901197.
Lamboni, M., Makowski, D., Lehuger, S., Gabrielle, B. and Monod, H. (2009). Multivariate global sensitivity analysis for dynamic crop models. Field Crops Research 113, 312320.
Laurenson, Y. C. S. M. (2014). Evaluating the feasibility of developing a model to better manage nematode infections of sheep. Technical Report.
Laurenson, Y. C. S. M., Bishop, S. C. and Kyriazakis, I. (2011). In silico exploration of the mechanisms that underlie parasite-induced anorexia in sheep. British Journal of Nutrition 106, 10231039.
Laurenson, Y. C. S. M., Kyriazakis, I. and Bishop, S. C. (2012 a). In silico exploration of the impact of pasture larvae contamination and anthelmintic treatment on genetic parameter estimates for parasite resistance in grazing sheep. Journal of Animal Science 90, 21672180.
Laurenson, Y. C. S. M., Kyriazakis, I., Forbes, A. B. and Bishop, S. C. (2012 b). Exploration of the epidemiological consequences of resistance to gastro-intestinal parasitism and grazing management of sheep through a mathematical model. Veterinary Parasitology 189, 238249.
Lewis, R. M., Macfarlane, J. M., Simm, G. and Emmans, G. C. (2004). Effects of food quality on growth and carcass composition in lambs of two breeds and their cross. Animal Science 78, 355367.
Louie, K., Vlassoff, A. and MacKay, A. (2005). Nematode parasites of sheep: extension of a simple model to include host variability. Parasitology 130, 437446.
Morris, M. D. (1991). Factorial sampling plans for preliminary computational experiments. Technometrics 33, 161174.
Pujol, G., Iooss, B., Janon, A., Gilquin, L., Le Gratiet, L. and Lemaître, P. (2014). Sensitivity: Sensitivity Analysis. R package version 1.8-1.
R: A Language and Environment for Statistical Computing (2014). R Core Team, Vienna, Austria.
Sakkas, P., Houdijk, J. G. M., Athanasiadou, S. and Kyriazakis, I. (2012). Sensitivity of periparturient breakdown of immunity to parasites to dietary protein source. Journal of Animal Science 90, 39543962.
Saltelli, A., Chan, K. and Scott, E. M. (2000). Sensitivity Analysis. Wiley, Chichester, UK.
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, 15521566.
Stear, M. J. and Bishop, S. C. (1999). The curvilinear relationship between worm length and fecundity of Teladorsagia circumcincta . International Journal of Parasitology 29, 777780.
Stear, M. J., Strain, S. and Bishop, S. C. (1999). Mechanisms underlying resistance to nematode infection. Second International Conference Novel Approaches to the Control of the Helminth Parasites of Livestock 29, 5156.
Steel, J., Symons, L. and Jones, W. (1980). Effects of level of larval intake on the productivity and physiological and metabolic responses of lambs infected with Trichostrongylus colubriformis. Australian Journal of Agricultural Research 31, 821838.
Suarez, V. H., Cristel, S. L. and Busetti, M. R. (2009). Epidemiology and effects of gastrointestinal nematode infection on milk productions of dairy ewes. Parasite 16, 141147.
Sykes, A. R. (2000). Environmental effects on animal production: the nutritional demands of nematode parasite exposure in sheep. Asian-Australasian Journal of Animal Sciences 13, 343350.
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.
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.
Vagenas, D., Doeschl-Wilson, A., Bishop, S. C. and Kyriazakis, I. (2007 c). In silico exploration of the effects of host genotype and nutrition on the genetic parameters of lambs challenged with gastrointestinal parasites. International Journal for Parasitology 37, 16171630.
Wang, J., Monod, H., Faivre, R. and Richard, H. (2014). Package “mtk”: Mexico ToolKit library (MTK). R package version 1.0.
Wellock, I. J., Emmans, G. C. and Kyriazakis, I. (2003). Modelling the effects of thermal environment and dietary composition on pig performance: model logic and concepts. Animal Science 77, 255266.
Wellock, I. J., Emmans, G. C. and Kyriazakis, I. (2004). Describing and predicting potential growth in the pig. Animal Science: an International Journal of Fundamental and Applied Research 78, 379388.
White, D. H., Bowman, P. J., Morley, F. H. W., McManus, W. R. and Filan, S. J. (1983). A simulation model of a breeding ewe flock. Agricultural Systems 10, 149189.
Wood, P. D. P. (1967). Algebraic model of the lactation curve in cattle. Nature 216, 164165.
Yin, X., Goudriaan, J., Lantinga, E. A., VOS, J. and Spiertz, H. J. (2003). A flexible sigmoid function of determinate growth. Annals of Botany 91, 361371.
Zaralis, K., Tolkamp, B. J., Houdijk, J. G. M., Wylie, A. R. G. and Kyriazakis, I. (2008). Changes in food intake and circulating leptin due to gastrointestinal parasitism in lambs of two breeds. Journal of Animal Science 86, 18911903.

Keywords

Modelling gastrointestinal parasitism infection in a sheep flock over two reproductive seasons: in silico exploration and sensitivity analysis

  • M. SACCAREAU (a1), C. R. MORENO (a1), I. KYRIAZAKIS (a2), R. FAIVRE (a3) and S. C. BISHOP (a4)...

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