Fiona Kenyon

The role of targeted selective treatments in the development of refugia-based approaches to the control of gastrointestinal nematodes of small ruminants

Anthelmintic resistance is recognised as a major problem affecting small ruminant production worldwide and now threatens the sustainability of many of these systems. One method that has been proposed to prolong the efficacy of our current anthelmintics is the maintenance of a parasite population in refugia (unexposed to a drug) which will maintain the genes for susceptibility within the parasite population. Management strategies that employ refugia-based methods include targeted or strategically timed whole flock treatments, targeted selective treatments (TST), whereby only a proportion of the flock is treated at any one time, and the dilution of resistant with susceptible parasites. The ability to effectively target anthelmintic use relies on the identification of those animals that will most benefit from treatment. This review explains the concept of refugia, describes the role of refugia-based approaches to the management of anthelmintic resistance and reviews the markers that have been studied as indicators for TSTs as well as the implementation of refugia-based strategies. Recent results suggest that targeting anthelmintic treatment on the basis of anaemia, milk production and liveweight gain may offer a means of reducing anthelmintic usage whilst still maintaining animal performance.

Climate change and infectious disease: helminthological challenges to farmed ruminants in temperate regions

In the UK, recent mean temperatures have consistently increased by between 1°C and 4°C compared to the 30-year monthly averages. Furthermore, all available predictive models for the UK indicate that the climate is likely to change further and feature more extreme weather events and a trend towards wetter, milder winters and hotter, drier summers. These changes will alter the prevalence of endemic diseases spatially and/or temporally and impact on animal health and welfare. Most notable among these endemic parasites are the helminths, which have been shown to be very strongly influenced by both the short-term weather and climate through effects on their free-living larval stages on pasture. In this review, we examine recent trends in prevalence and epidemiology of key helminth species and consider whether these could be climate-related. We identify likely effects of temperature and rainfall on the free-living stages and some key parasite traits likely to determine parasite abundance under changed climatic conditions. We find clear evidence that climate change, especially elevated temperature, has already changed the overall abundance, seasonality and spatial spread of endemic helminths in the UK. We explore some confounders and alternative explanations for the observed patterns. Finally, we explore the implications of these findings for policy makers and the livestock industry and make some recommendations for future research priorities.

Sheep helminth parasitic disease in south eastern Scotland arising as a possible consequence of climate change

The climate in the UK is changing, with a trend towards increased rainfall in the autumn and winter and warmer average temperatures throughout the year. There has also been a 4-week extension of the herbage growing season over the past 40 years. These changes may have implications for the epidemiology of sheep helminth parasites. Here, we describe production-limiting disease outbreaks caused by Haemonchus contortus, Nematodirus battus, Teladorsagia circumcincta and Fasciola hepatica in sheep flocks in south eastern Scotland. The occurrence and timing of these disease outbreaks could not have been predicted in this region highlighting changes in the epidemiology of helminth infections from the patterns historically described. These cases are used to introduce discussion regarding the potential effects of climate change on the epidemiology of helminth parasites and the implications for sheep farming in the UK.

Chasing helminths and their economic impact on farmed ruminants

Global agriculture will be required to intensify production from a shrinking natural resource base. Helminth infections of ruminants are a major constraint on efficient livestock production. The current challenge is to develop diagnostic methods that detect the production impact of helminth infections on farms in order to target control measures and contribute to the global challenge of preserving food security. We review here our understanding of the effects of helminth infections and control practices on productivity and the diagnostic tools that can inform on this. By combining advances in helminth laboratory diagnostics and animal health economics, sustainable management of helminth infections can be integrated into the whole-farm economic context.

Standardization of the larval migration inhibition test for the detection of resistance to ivermectin in gastro intestinal nematodes of ruminants

Resistance to anthelmintics is an increasing problem in sheep, goat and cattle industries worldwide. For parasite management on farms reliable methods for the detection of resistance are required and it is important that tests give comparable, reproducible and reliable results in different laboratories. The ability of the larval migration inhibition test (LMIT), to detect ivermectin resistance in cattle and sheep nematodes has been evaluated through ring testing in up to six different laboratories in Europe, supported by an EU sixth Framework Project (PARASOL). Third stage larvae of Ostertagia ostertagi, Cooperia oncophora, and Haemonchus contortus with a known resistance status were obtained from faecal cultures of experimentally infected calves and sheep. Following a series of ring tests using identical protocols, reproducible results were obtained within and between participating laboratories. In all tests dose-response curves with R(2) values >0.90 were obtained by all laboratories. Resistance ratios of 8.3 and 8.4 were found when susceptible and IVM-resistant isolates of C. oncophora and H. contortus were compared and differences in the EC(50) values were highly significant (p<0.0001). Protocols for the LMIT and the preparation of ivermectin solutions are described in a supplementary file.

Development and field evaluation of a decision support model for anthelmintic treatments as part of a targeted selective treatment (TST) regime in lambs.

The recent focus of strategies to slow the rate of development of anthelmintic resistance in gastro-intestinal parasites has centred on the need to better manage the parasite population that is unexposed to the drug, i.e. in refugia. One strategy involves the use of targeted selective treatments (TST) where anthelmintics are only administered to those individuals that are likely to benefit from it, rather than to the whole flock. However, there are few TST indicators currently available for farmers in temperate environments. Here we describe the development and field evaluation of a performance-based decision support model to identify individual animals whose performance is suffering from nematodoses, and thus, likely to benefit from an anthelmintic treatment. One hundred and ninety two twin-suckled lambs were separated into eight groups and each grazed on a one-hectare paddock and exposed to one of four anthelmintic treatment regimes. Groups of lambs received either: a whole flock anthelmintic treatment either every four weeks (neo-suppressive treatment, NST); when clinical signs of disease were evident (metaphylactic/therapeutic treatment, MT); at pre-determined times throughout the grazing season (strategic treatment, SPT) or treatment on an individual animal basis as determined by a performance-based decision support model that relied on a calculation of the efficiency of nutrient utilization (targeted selective treatment, TST). Animal performance and parasitological data were recorded every two weeks. Mean faecal egg counts were low throughout the season for the NST group and moderate for the MT, SPT and TST groups. During the entire grazing season the NST, MT, SPT and TST animals each received on average 5.0, 2.0, 3.0 and 2.6 anthelmintic treatments, respectively. Compared to the NST animals, cumulative weight gains were 11% lower at the end of the grazing season in MT animals, whereas no reduction was observed in either the SPT or TST groups. The proposed decision support system appeared to be successful in discriminating between animals which were likely to respond favourably to anthelmintic treatment and those that were not and provided a quantitative estimate of the likely response. Furthermore, 87% of animals that had a pre-treatment efficiency of nutrient utilization value lower than the suggested threshold of the model responded positively to treatment. The potential benefits of using the decision support model as a TST indicator for managing the parasite population in refugia in temperate environments are discussed.

Practices to optimise gastrointestinal nematode control on sheep, goat and cattle farms in Europe using targeted (selective) treatments

Due to the development of anthelmintic resistance, there have been calls for more sustainable nematode control practices. Two important concepts were introduced to study and promote the sustainable use of anthelmintics: targeted treatments (TT), where the whole flock/herd is treated based on knowledge of the risk, or parameters that quantify the severity of infection; and targeted selective treatments (TST), where only individual animals within the grazing group are treated. The aim of the TT and TST approaches is to effectively control nematode-induced production impacts while preserving anthelmintic efficacy by maintaining a pool of untreated parasites in refugia. Here, we provide an overview of recent studies that assess the use of TT/TST against gastrointestinal nematodes in ruminants and investigate the economic consequences, feasibility and knowledge gaps associated with TST. We conclude that TT/TST approaches are ready to be used and provide practical benefits today. However, a major shift in mentality will be required to make these approaches common practice in parasite control.

The proteinases of Psoroptes ovis, the sheep scab mite: their diversity and substrate specificity

The sheep scab mite, Psoroptes ovis, causes severe dermatitis in infected sheep with severe welfare and production implications. The dermatitis has the characteristics of an immediate hypersensitivity type reaction which, by analogy to other mite species, including the house dust mites (Dermatophagoides spp.), is likely to be invoked by a variety of allergens including mite-derived proteinases. Here, the proteinases in P. ovis extracts were characterised using substrate gel analysis, inhibitor sensitivity and their ability to degrade a variety of potential natural protein substrates. These analyses showed that mites contain several proteinases which could be differentiated on the basis of molecular size and inhibitor sensitivity with cysteine, metalloproteinases and aspartyl proteinases predominating. These proteinases degraded collagen and fibronectin, possibly indicative of a role in lesion initiation, they degraded several blood proteins, a property which may aid mite feeding and they degraded immunoglobulin G, possibly aiding immuno-evasion. Because proteinases, particularly the cysteine class, are demonstrably allergenic in other mite infestations, these proteinases clearly merit further immunological and biochemical definition.

Production impact of a targeted selective treatment system based on liveweight gain in a commercial flock

The sustainability of sheep production is hindered by anthelmintic resistance. Options to slow down or prevent resistance have been widely studied but their application in the field is still limited. In this study, the practical application and effect of a targeted selective treatment (TST) approach for the treatment of parasitic gastroenteritis was investigated in lambs (n = 385) over a 2 year period. At 14-day intervals during the grazing season, liveweight, breech soiling and anthelmintic treatments were individually recorded. Selection of lambs for anthelmintic treatment in the TST group was based on pre-calculated individual growth rates, with a matched cohort routinely treated (RT) with anthelmintic drug every 6 weeks. The adoption of a TST approach had no negative effect on the liveweight gains of the lambs, time to finishing or breech soiling measures compared to RT lambs; however a 50% decrease in anthelmintic treatment was observed in the TST group. The time to implement this system averaged 2 min per lamb. It is concluded that the TST could be suitable for commercial sheep farms, in association with automated weighing systems, potentially reducing selection for anthelmintic resistance, while having no negative effect on production.

Mind the gaps in research on the control of gastrointestinal nematodes of farmed ruminants and pigs

Gastrointestinal (GI) nematode control has an important role to play in increasing livestock production from a limited natural resource base and to improve animal health and welfare. In this synthetic review, we identify key research priorities for GI nematode control in farmed ruminants and pigs, to support the development of roadmaps and strategic research agendas by governments, industry and policymakers. These priorities were derived from the DISCONTOOLS gap analysis for nematodes and follow-up discussions within the recently formed Livestock Helminth Research Alliance (LiHRA). In the face of ongoing spread of anthelmintic resistance (AR), we are increasingly faced with a failure of existing control methods against GI nematodes. Effective vaccines against GI nematodes are generally not available, and anthelmintic treatment will therefore remain a cornerstone for their effective control. At the same time, consumers and producers are increasingly concerned with environmental issues associated with chemical parasite control. To address current challenges in GI nematode control, it is crucial to deepen our insights into diverse aspects of epidemiology, AR, host immune mechanisms and the socio-psychological aspects of nematode control. This will enhance the development, and subsequent uptake, of the new diagnostics, vaccines, pharma-/nutraceuticals, control methods and decision support tools required to respond to the spread of AR and the shifting epidemiology of GI nematodes in response to climatic, land-use and farm husbandry changes. More emphasis needs to be placed on the upfront evaluation of the economic value of these innovations as well as the socio-psychological aspects to prioritize research and facilitate uptake of innovations in practice. Finally, targeted regulatory guidance is needed to create an innovation-supportive environment for industries and to accelerate the access to market of new control tools.