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In horses that graze contaminated pasture and that are not treated with appropriate anthelmintics, large numbers of intestinal nematodes can accumulate. Anthelmintic resistance (AR) is a real threat to welfare because, when worm burdens cannot be controlled, serious disease can occur [1]. The nematodes whose management should be at the foremost of all control programmes are the strongyles, in particular, the cyathostomins (small strongyles). These worms are ubiquitous, have the potential to cause severe, sometimes fatal, disease and have a relatively high propensity to develop resistance to the anthelmintics licensed for their control [2]. For decades, equine helminth control has followed interval treatment regimens. These involve regular deworming of all horses at intervals based on the strongyle egg reappearance period of each anthelmintic defined at product licensing [3]. Frequent anthelmintic administrations have led to substantial reductions in the incidence of large strongyle (i.e. Strongylus vulgaris) associated disease, but have made a fundamental contribution to the development of AR in cyathostomins. Resistance to 2 of the 3 available anthelmintic classes is now widespread in cyathostomins, with resistance to both classes in single populations reported [2]. Reduced efficacy of the commonly used macrocyclic lactone compounds (moxidectin, ivermectin), primarily measured by a shortened egg reappearance period after treatment, is emerging [4-6]. Should resistance to all 3 anthelmintic classes become widespread, there will be no options left for control of these common infections as no new compounds appear to be under development for use in horses in the short to medium term. Consequently, strategies that delay the development and spread of AR need to be deployed.

Faecal egg count (FEC) testing is often recommended as a tool to support targeted approaches to control, with only those horses with moderate to high FEC results dewormed to reduce pasture contamination at certain times of year [7]. The high level of over dispersion in strongyle egg excretion patterns observed in equids [8], means that it should be relatively straightforward to target a small number of animals that excrete moderate to high numbers of eggs in their faeces, hence reducing the number of treatments applied per population. This approach has been proposed to protect a proportion of the worm population from selection pressure for AR [9]. It is important that those who deliver targeted treatment programmes have access to up-to-date knowledge on which to base them; this would include information on the likely prevalence and distribution of helminths in populations, the accuracy of available diagnostic tools and the probable status of efficacy of the various anthelmintic compounds.

Anthelmintic efficacy testing should be implemented in practice; the de facto test for this is the FEC reduction test, but clear recommendations for this currently only exist for small ruminants. There is a real need for well-validated, standardised and easily computable methods of analysis that can be implemented in equine practice [10]. This is an area where veterinary parasitologists now need to deliver tools (preferably, free and online) that will facilitate improved interpretation of the FEC reduction tests in the field. Recent studies have sought to use more appropriate anthelmintic sensitivity thresholds for use in equids; these have identified the prevalence of benzimidazole resistance in strongyles to approach 100% [11-13]. In the EU, in terms of reducing strongyle FEC, pyrantel efficacy has been observed to vary from farm to farm [11-13] and levels of resistance do not appear to be as high as those reported in the USA [2]. In the UK at least, pyrantel could be used strategically for strongyle control for reducing FEC and to reduce reliance on macrocyclic lactone compounds, but with the caveat that efficacy should be tested regularly. There is frequent, extensive use of ivermectin and moxidectin [14, 15]: unsurprising perhaps, given their wide spectrum of activity and lack of reported resistance in cyathostomins. Moxidectin is the only product licensed for efficacy against cyathostomin encysted larvae for which widespread resistance has not yet been reported (viz. fenbendazole), so it could be argued that its use should be preserved for this purpose. Although horse owners seem to be aware of the spectrum of the nematocidal activity of moxidectin, they are not generally reserving it specifically for treatment of cyathostomin encysted larvae [14]. More judicious application of this compound is warranted as resistance measured as a reduction in the standard strongyle egg reappearance period after moxidectin treatment has been reported [6].

As horses are most often treated as individuals, it should be a relatively straightforward step for owners to base control programmes around targeted strategies driven by regular FEC analysis. As alluded to above, published studies cite high levels of aggregation in strongyle FEC patterns in managed equines with <20% of the total population excreting >80% strongyle eggs in their faeces at any given point in time [8] with a degree of individual shedding consistency across time [16, 17]. Recent results [14] indicate that FEC-based targeted programmes are becoming more established in the UK and in some EU member states these protocols have been standard practice for more than a decade due to prescribing laws [18]. It is of the essence that messages regarding sustainable control are coherent. In a recent Scottish study [14], there appeared a disconnect in client perception of ‘targeted treatments’, with 40% of respondents confusing ‘targeted’ administration, based on use of diagnostic tools such as FEC, with targeting for species or developmental stage of worm. This is where veterinarians, suitably qualified persons and pharmaceutical companies could improve communication by using clear and consistent terminology. Also in the Scottish study [14], it was not apparent that deploying FEC-based targeted treatments led to obvious reductions in treatment intervals compared with those in traditional interval-based programmes despite the fact that over 50% of respondents engaged in ‘diagnostic’ FEC analysis.

If FEC testing is to be the basis of evidence-based control, methodologies need to be as optimal as is practicably possible to be of value in the field. Limitations in protocols and interpretation must be appreciated. A number of factors leading to variation present difficulties in practice and could result in incorrect decisions regarding treatment administration or classification of drug sensitivity. Strongyle eggs are not distributed evenly among balls of horse dung [19] so sampling protocols need to ensure that sufficient (i.e. >10 g) representative material (selected from at least 3 dung balls) is taken for analysis [19]. Also, samples must be thoroughly mixed before taking an aliquot at the laboratory to be analysed in the test [20]. This is not rocket science, but these simple measures will enhance the value of FEC analysis. An important factor that affects outcome of the test is the multiplication factor inherent in different types of FEC methods [21]. For accuracy, FEC methods with as a high a sensitivity as is practicably possible should be used to reduce variance when reporting output data. Faecal egg count methods often used in veterinary practice laboratories have relatively low sensitivity and employ multiplication factors in calculating the final eggs/g (‘epg’) result. Recent analysis in the author's laboratory using faeces from strongyle-infected horses indicates that when FEC tests that involve a multiplication step are used to inform on the requirement for treatment, more horses were deemed to have a higher epg when compared with more sensitive FEC methods. In future, consideration should be given to adapting methodology to increase sensitivity or of changing to methodologies validated as more sensitive for counting nematode egg in faeces [22].

It is important that, in establishing FEC-based targeted protocols, helminth species and developmental stages that cannot be detected or easily differentiated by standard nematode egg counting methods must still be considered. Comparative analyses suggest an association between the occurrence of S. vulgaris on farms in Denmark and the application of targeted treatments based on regular FEC [23]. Differentiation of large and small strongyle species on the basis of egg morphology is not something that would be routinely done in practice and is an area where parasitologists or large diagnostic laboratories need to be vigilant. Standard FEC methods are also not particularly useful for detecting tapeworm infection and although an antibody-directed ELISA has been developed and is commercially available for diagnosing Anoplocephala perfoliata, its interpretation is complicated by the extended half-life of parasite-specific serum immunoglobulin [24]. A coproantigen based ELISA has shown some potential for detection of concurrent infection with tapeworm [25], but progress of the test to commercial reality is not clear at present.

Faecal egg count techniques are incapable of diagnosing prepatent infection of helminths. Cyathostomin encysted larvae can persist for extended periods and, at specific times (autumn/winter in the UK), can constitute up to 90% of the total burden [26]. In some horses, large numbers of larvae can emerge to cause severe diarrhoea, weight loss, colic and/or oedema and death in up to 50% of cases [27]. Diagnostic markers that form the basis of a serum-based ELISA for identifying infection with cyathostomin encysted larvae have been described and their specificity validated [28]. The test is currently being patented and developed for commercialisation. In contrast, attempts to develop a similar test for detection of migrating S. vulgaris larvae have been unsuccessful [29].

With current advice conveyed to horse owners to consider rotational grazing with other species to assist in the environmental control of pasture contamination, one concern is the recent increase in prevalence observed in liver fluke (Fasciola hepatica) in the UK (http://www.defra.gov.uk/ahvla-en/publication/vida12/). Liver fluke can infect equids and is a challenge to control because there are no licensed antifluke products for horses and donkeys, and resistance to the widest spectrum and safest product, triclabendazole, is being increasingly reported in sheep [30]. For these reasons, there is a need to optimise surveillance and diagnostics for fasciolosis in equids.

The challenge now is to convince horse owners to continue with evidence-based helminth control strategies, with emphasis placed on maximising the value of diagnostic tests to facilitate appropriate treatment decisions and to increase levels of efficacy testing in the field. The recent questionnaire study [14] revealed that horse owners are now engaging in evidence-based protocols; however, over reliance on some compounds was identified and continued client education in this area will be required to elicit further changes in behaviour [14]. This can be combined with dialogue on all potential benefits of these protocols, such as the inherent value in continued disease surveillance and the potential financial benefits associated with significant reductions in anthelmintic use [31].

Source of funding

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  2. Source of funding
  3. References

J.B. Matthews has been supported in the research described by the HBLB, Pilkington Trust, Donkey Sanctuary and The Horse Trust.

References

  1. Top of page
  2. Source of funding
  3. References
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    Nielsen, M.K. (2012) Sustainable equine parasite control: perspectives and research needs. Vet. Parasitol. 185, 32-44.
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    Molento, M.B., Nielsen, M.K. and Kaplan, R.M. (2012) Resistance to avermectin/milbemycin anthelmintics in equine cyathostomins – current situation. Vet. Parasitol. 185, 16-24.
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    Rossano, M.G., Smith, A.R. and Lyons, E.T. (2010) Shortened strongyle-type egg reappearance periods in naturally infected horse treated with moxidectin and failure of a larvicidal dose of fenbendazole to reduce faecal egg counts. Vet. Parasitol. 173, 349-352.
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    Relf, V.E., Morgan, E.R., Hodgkinson, J.E. and Matthews, J.B. (2013) Helminth egg excretion with regard to age, gender and management practices on UK Thoroughbred studs. Parasitology 140, 641-652.
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    Nielsen, M.K., Kaplan, R.M., Thamsborg, S.M., Monrad, J. and Olsen, S.N. (2007) Climatic influences on development and survival of free-living stages of equine strongyles: implications for worm control strategies and managing anthelmintic resistance. Vet. J. 174, 23-32.
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    Stratford, C.H., Lester, H.E., Pickles, K.J., McGorum, B.C. and Matthews, J.B. (2014) An investigation of anthelmintic efficacy against strongyles on equine yards in Scotland. Equine Vet. J. 46, 17-24.
  • 13
    Traversa, D., Castagna, G., von Samson-Himmelstjerna, G., Meloni, S., Bartolini, R., Geurden, T., Pearce, M.C., Woringer, E., Besognet, B., Milillo, P. and D'Espois, M. (2012) Efficacy of major anthelmintics against horse cyathostomins in France. Vet. Parasitol. 188, 294-300.
  • 14
    Stratford, C.H., Lester, H.E., Morgan, E.R., Pickles, K.J., Relf, V., McGorum, B.C. and Matthews, J.B. (2014) A questionnaire study of equine gastrointestinal parasite control in Scotland. Equine Vet. J. 46, 25-31.
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    Relf, V.E., Morgan, E.R., Hodgkinson, J.E. and Matthews, J.B. (2012) A questionnaire study on parasite control practices on UK breeding Thoroughbred studs. Equine Vet. J. 44, 466-471.
  • 16
    Becher, A.M., Mahling, M., Nielsen, M.K. and Pfister, K. (2010) Selective anthelmintic therapy of horses in the Federal states of Bavaria (Germany) and Salzburg (Austria): an investigation into strongyle egg shedding consistency. Vet. Parasitol. 171, 116-122.
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  • 19
    Lester, H.E., Bartley, D.J., Morgan, E.R., Hodgkinson, J.E. and Matthews, J.B. (2012) The spatial distribution of strongyle eggs in horse faeces. J. Eq. Vet. Sci. 32, S33-S34.
  • 20
    Denwood, M.J., Love, S., Innocent, G.T., Matthews, L., McKendrick, I.J., Hillary, N., Smith, A. and Reid, S.W. (2012) Quantifying the sources of variability in equine faecal egg counts: implications for improving the utility of the method. Vet. Parasitol. 188, 120-126.
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    Nielsen, M.K., Olsen, S.N., Lyons, E.T., Monrad, J. and Thamsborg, S.M. (2012) Real-time PCR evaluation of Strongylus vulgaris in horses on farms in Denmark and Central Kentucky. Vet. Parasitol. 190, 461-466.
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  • 26
    Dowdall, S.M.J., Matthews, J.B., Mair, T., Murphy, D., Love, S. and Proudman, C.J. (2002) Antigen-specific IgG(T) responses in natural and experimental Cyathostominae infection in horses. Vet. Parasitol. 106, 225-242.
  • 27
    Giles, C.J., Urquhart, K.A. and Longstaffe, J.A. (1985) Larval cyathostomiasis (immature trichonema-induced enteropathy): a report of 15 clinical cases. Equine Vet. J. 17, 196-201.
  • 28
    McWilliam, H.E., Nisbet, A.J., Dowdall, S.M., Hodgkinson, J.E. and Matthews, J.B. (2010) Identification and characterisation of an immunodiagnostic marker for cyathostomin developing stage larvae. Int. J. Parasitol. 40, 265-275.
  • 29
    Andersen, U.V., Howe, D.K., Olsen, S.N. and Nielsen, M.K. (2013) Recent advances in diagnosing pathogenic equine gastrointestinal helminths: the challenge of prepatent detection. Vet. Parasitol. 192, 1-9.
  • 30
    Cabada, M.M. and White, A.C. Jr (2012) New developments in epidemiology, diagnosis, and treatment of fascioliasis. Curr. Opin. Infect. Dis. 25, 518-522.
  • 31
    Lester, H.E., Bartley, D.J., Morgan, E.R., Hodgkinson, J.E., Stratford, C.H. and Matthews, J.B. (2013) A cost comparison of targeted anthelmintic treatments in horses in the UK. Vet. Rec. 173, 371.