Refugia-based strategies for sustainable worm control: Factors affecting the acceptability to sheep and goat owners

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Abstract

Sustainable nematode management programs aim to minimise animal production loss and prevent parasitic disease, without increasing the level of anthelmintic resistance. Resistance management strategies are now largely based on the “refugia” concept, by which populations of nematodes not recently exposed to treatment are deliberately allowed to survive. Progeny from the unselected parasites provide a source of less-resistant worms which can dilute resistant worms surviving anthelmintics, and hence reduce the rate of resistance development. This can be achieved by either modifying strategic treatment regimens to ensure the survival of infective worm larvae on pasture, or by avoiding treatments to individual animals identified as best able to cope with parasites. These strategies include “targeted treatment” (based on estimates of worm-burdens) and “targeted selective treatment” (based on indications of parasitic effects). However, the departure from conventional anthelmintic approaches represents a major conceptual challenge to many livestock owners. Factors that may affect the wide adoption of refugia strategies include the increased risk of parasitism and production loss, the effectiveness of reducing the development of resistance, the practicality of implementation, and the direct effects on costs and labour efficiency. The acceptance of particular strategies is likely to vary considerably according to environmental effects, nematode species, animal production aims and resource availability. However, recent indications that comparatively small changes to present practices can provide substantial refugia benefits suggest that appropriate resistance management approaches can be developed for different situations.

Introduction

The importance of anthelmintic resistance management strategies in nematode control recommendations for livestock has been recognised for many years, in response to evidence of an increasing prevalence and severity of resistance (Besier and Love, 2003, Kaplan, 2004, Wolstenholme et al., 2004). Numerous studies have contributed to the theoretical basis to the development of resistance, and the major causal factors are well understood (Prichard et al., 1980, Sangster and Dobson, 2002). Changes to anthelmintic usage practices that impose significant selection pressure for resistance are essential to preserve the effectiveness of anthelmintics currently in use, and also to avoid the rapid development of resistance to newly introduced anthelmintics.

In recent years, the refugia concept has been identified as a fundamental principle in resistance management. This proposes that to reduce the selection pressure for resistance in a population of nematodes, resistant worms surviving anthelmintic treatment must be diluted by the establishment of infective larvae from a non-resistant source to reduce the relative contribution of resistant parasites to subsequent generations (van Wyk, 2001, Besier, 2008, Jackson and Waller, 2008, Leathwick et al., 2009, Kenyon et al., 2009). Worm populations in refugia from anthelmintics exist as larvae on pasture prior to the administration of anthelmintic treatments, and as worms present in animals not recently given anthelmintic treatments. Resistance management strategies for particular situations therefore require a judgement of the potential level of intake of infective larvae and their likely resistance status, and the planning of pasture movements in relation to anthelmintic treatments of grazing animals.

However, the application of the refugia concept to practical situations usually requires modifications or additions to existing control regimens, and hence an awareness of factors which may influence the applicability of different approaches to different circumstances. In addition to the effects of environment and nematode species, animal production aims, financial resources and labour availability vary between enterprise types and between individual livestock owners. Translating potential refugia strategies from experimental concepts into strategies appropriate to particular situations and acceptable to livestock owners represents a considerable challenge to parasitologists and animal health advisers. Importantly, the acceptability of the refugia concept will be most effective when integrated with appropriate anthelmintic choice and non-chemical management methods (Jackson et al., 2009).

Section snippets

Refugia strategies

Refugia-based strategies usually involve either changes to the timing and frequency of regimens by which all animals in a group are treated, or the introduction of selective treatment strategies, by which some animals are left untreated when flock treatments are given. In all cases, it is recognised that the survival of larger worm populations than normally allowed requires a balance between the effectiveness of refugia that the new approach creates, and the potential adverse consequences from

Factors influencing the adoption of refugia strategies

The concept of refugia can present a significant conceptual challenge to livestock owners, and the adoption of modified practices to combat drench resistance has been difficult to achieve. Poor anthelmintic performance due to drench resistance is often not clinically evident (other than for H. contortus) and even where the potential impact of drench resistance is understood, farmers usually find the option of moving to an alternative anthelmintic easier to implement than approaches involving

Risk of parasitism and production loss

Trade-offs between resistance management and worm control effectiveness are fundamental to refugia-based strategies. The deliberate retention of adult worm burdens may have immediate consequences due to continued parasitic effects in untreated individuals, as well as allowing further pasture larval contamination which may reduce the effectiveness of epidemiologically based control programs. The deliberate exposure of sheep with minimal existing burdens to further larval ingestion, required to

How much refugia is necessary?

The key question regarding refugia strategies is whether they can reduce the development of anthelmintic resistance by a sufficient degree to warrant changes to worm control routines and potential increased losses due to parasitism. Most recent studies have not included estimations of between-treatment changes in resistance status, largely because this is difficult to measure over short time periods, and genetic changes within worm populations cannot easily be differentiated where treatment

Practicality of application

Even when the concept of refugia is accepted, its incorporation into routine strategies depends upon the availability of adequate resources, such as time and labour. In general, less individual animal intervention will be feasible in large and lower-margin extensive enterprises such as in Australia and New Zealand compared to smaller but high-return flocks in Europe and North America, or by traditional herders in less developed countries.

A major limitation for TST occurs where frequent

Costs and efficiencies

A key question is: “what is the cost required to ensure the sustainability of anthelmintic programs?” Few studies have included a cost-benefit analysis of refugia strategies, although there is likely to be some cost to an enterprise in terms of potentially lost production and in implementation costs. The cost deemed acceptable will vary according to the attitudes and experiences of individual animal owners, and the relative risk of resistance development. For example, Mahieu et al. (2007)

Conclusion

There is general agreement that refugia-based approaches are central to the effective management of anthelmintic resistance, and investigations have confirmed the potential of a variety of implementation strategies. However, even where livestock owners are convinced of the necessity for sustainable anthelmintic management, a number of factors must be considered if these concepts are to be developed into recommendations, and if wide acceptance is to be achieved.

In particular, there is an obvious

Conflict of interest

The author declares that there is no conflict of interest.

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