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Living with parasites: exploiting tolerance of infection to reduce the impact of gastrointestinal nematodes in sheep

02 July 2024
12 mins read
Volume 29 · Issue 4

Abstract

Gastrointestinal nematodes are among the most prevalent and damaging infections faced by ruminant livestock. Anthelmintic resistance means that sustainable control is essential and selective breeding has been part of this for decades. Breeding, however, has focused on promoting resistance to infection, yet almost no empirical work has been done on the other means by which hosts mitigate the impact of parasites, namely tolerance of infection. This review defines the concepts of resilience, resistance and tolerance, with particular attention to gastrointestinal nematode infections of sheep. How selection has thus far been implemented is discussed, and the pros and cons of each trait are evaluated. Tolerance has been almost completely neglected in livestock science, and its potential mechanisms with regard to gastrointestinal nematodes in sheep are discussed. The authors' work to understand more about tolerance to gastrointestinal nematodes and its potential role in sustainable control of gastrointestinal nematodes in the future is also disscussed.

Gastrointestinal nematodes are a major challenge to the UK livestock industry, and particularly to sheep farming, as a result of their impact on many aspects of animal performance (Mavrot et al, 2015). A recent estimate suggests that helminth infection costs the UK meat sheep industry £41 million annually, £15 million of which is because of the effects on production and £26 million of which is because of treatments with anthelminthic drugs (Charlier et al, 2020). Gastrointestinal nematodes also have an environmental impact, since lambs infected with gastrointestinal nematodes have higher greenhouse gas emissions than uninfected lambs (Kenyon et al, 2013; Fox et al, 2018). These impacts on economic and environmental sustainability have largely been managed with anthelmintic drugs for the past several decades, but reports of resistance to these drugs in worm populations are becoming more widespread and their efficacy is declining (Sargison et al, 2007; Rose Vineer et al, 2020). Anthelmintic residues excreted by sheep also have downstream negative effects on invertebrates, such as pollinators and dung beetles, which are essential to ecosystem health (Vokřál et al, 2023). A general reduction in anthelmintic use is therefore required, to reduce these environmental impacts and maintain refugia where susceptible gastrointestinal nematodes reside (Hodgkinson et al, 2019), increasing the lifespan of anthelmintics and ensuring they can continue to be used as part of integrated parasite management. While there is a need to reduce anthelmintic use, the publication of the Animal Health and Welfare Pathway for England (Department for Enivronment, Food and Rural Affairs, 2024) highlighted internal parasites as a priority for sheep farmers, and it is almost needless to say that their impact must be controlled. It is therefore essential to develop sustainable means of controlling gastrointestinal nematodes that do not rely heavily on anthelmintics (Jackson et al, 2009; Abbott et al, 2012; Forbes, 2023). Developing sustainable parasite control strategies is now, more than ever, an active area of research, although it is not the purpose of this article to discuss them all. Nevertheless, vaccines, grazing management and nutrition are all likely to play a role. Selective breeding to ensure that gastrointestinal nematodes have as little impact on sheep as possible has been an important tool for decades, yet has not been as widely exploited as it could be. Ultimately, breeding acts by altering the biology of the sheep, and as such it is necessary to understand the mechanisms by which sheep naturally fight infection.

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