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      Confounding factors affecting faecal egg count reduction as a measure of anthelmintic efficacy Translated title: Facteurs de confusion affectant la réduction du nombre d’œufs fécaux comme mesure de l’efficacité anthelminthique

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          Abstract

          Increasing anthelmintic resistance (AR) in livestock has stimulated growing efforts to monitor anthelmintic effectiveness (AE) on livestock farms. On-farm assessment of AE relies on measuring the reduction in faecal egg count (FEC) following treatment; and if conducted rigorously, qualifies as a formal FEC reduction test (FECRT) for AR. Substantial research effort has been devoted to designing robust protocols for the FECRT and its statistical interpretation; however, a wide range of factors other than AR can affect FEC reduction on farms. These are not always possible to control, and can affect the outcome and repeatability of AE measurements and confound the on-farm classification of AR using FECRT. This review considers confounders of FEC reduction, focusing on gastrointestinal nematodes of ruminants, including host and parasite physiology and demography; pharmacokinetic variation between drugs, parasites and hosts; and technical performance. Drug formulation and delivery, host condition and diet, and seasonal variation in parasite species composition, can all affect AE and hence observed FEC reduction. Causes of variation in FEC reduction should be attenuated, but this is not always possible. Regular monitoring of AE can indicate a need to improve anthelmintic administration practices, and detect AR early in its progression. Careful interpretation of FEC reduction, however, taking into account possible confounders, is essential before attributing reduced FEC reduction to AR. Understanding of confounders of FEC reduction will complement advances in FECRT design and interpretation to provide measures of anthelmintic efficacy that are both rigorous and accessible.

          Translated abstract

          L’augmentation de la résistance aux anthelminthiques (RA) chez le bétail a stimulé des efforts croissants pour mesurer l’efficacité des anthelminthiques (EA) dans les élevages. L’évaluation à la ferme de l’EA repose sur la mesure de la réduction du nombre d’œufs dans les selles (NOS) après le traitement ; si effectué rigoureusement, celui-ci est qualifié de test formel de réduction du NOS (TFRNOS) pour la RA. Des efforts de recherche substantiels ont été consacrés à la conception de protocoles robustes pour le TFRNOS et son interprétation statistique, mais un large éventail de facteurs autres que la RA peuvent affecter la réduction du NOS dans les exploitations. Ces facteurs ne sont pas toujours contrôlables et peuvent affecter le résultat et la répétabilité des mesures de l’EA et introduire de la confusion dans la classification à la ferme de la RA à l’aide de la TFRNOS. Cette revue examine les facteurs de confusion de la réduction du NOS, en se concentrant sur les nématodes gastro-intestinaux des ruminants, et considère la physiologie et la démographie de l’hôte et du parasite, la variation pharmacocinétique entre les médicaments, les parasites et les hôtes, et les performances techniques. La formulation et l’administration de médicaments, la condition et le régime alimentaire de l’hôte, ainsi que les variations saisonnières de la composition des espèces de parasites, peuvent tous affecter l’EA et donc la réduction du NOS observé. Les causes de variation de la réduction du NOS doivent être atténuées, mais cela n’est pas toujours possible. Une surveillance régulière de l’EA peut indiquer la nécessité d’améliorer les pratiques d’administration des anthelminthiques et de détecter la RA au début de sa progression. Une interprétation prudente de la réduction du NOS, cependant, en tenant compte des facteurs de confusion possibles, est essentielle avant d’attribuer la réduction du NOS à la RA. La compréhension des facteurs de confusion d’une moindre réduction du NOS complétera les progrès sur la conception et l’interprétation du TFRNOS, pour fournir des mesures de l’efficacité des anthelminthiques à la fois rigoureuses et accessibles.

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          World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.) methods for the detection of anthelmintic resistance in nematodes of veterinary importance.

          Methods have been described to assist in the detection of anthelmintic resistance in strongylid nematodes of ruminants, horses and pigs. Two tests are recommended, an in vivo test, the faecal egg count reduction test for use in infected animals, and an in vitro test, the egg hatch test for detection of benzimidazole resistance in nematodes that hatch shortly after embryonation. Anaerobic storage for submission of faecal samples from the field for use in the in vitro test is of value and the procedure is described. The tests should enable comparable data to be obtained in surveys in all parts of the world.
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            Initial assessment of the economic burden of major parasitic helminth infections to the ruminant livestock industry in Europe

            We report a European wide assessment of the economic burden of gastrointestinal nematodes, Fasciola hepatica (common liver fluke) and Dictyocaulus viviparus (bovine lungworm) infections to the ruminant livestock industry. The economic impact of these parasitic helminth infections was estimated by a deterministic spreadsheet model as a function of the proportion of the ruminant population exposed to grazing, the infection frequency and intensity, the effect of the infection on animal productivity and mortality and anthelmintic treatment costs. In addition, we estimated the costs of anthelmintic resistant nematode infections and collected information on public research budgets addressing helminth infections in ruminant livestock. The epidemiologic and economic input data were collected from international databases and via expert opinion of the Working Group members of the European Co-operation in Science and Technology (COST) action COMbatting Anthelmintic Resistance in ruminants (COMBAR). In order to reflect the effects of uncertainty in the input data, low and high cost estimates were obtained by varying uncertain input data arbitrarily in both directions by 20 %. The combined annual cost [low estimate-high estimate] of the three helminth infections in 18 participating countries was estimated at € 1.8 billion [€ 1.0-2.7 billion]. Eighty-one percent of this cost was due to lost production and 19 % was attributed to treatment costs. The cost of gastrointestinal nematode infections with resistance against macrocyclic lactones was estimated to be € 38 million [€ 11-87 million] annually. The annual estimated costs of helminth infections per sector were € 941 million [€ 488 - 1442 million] in dairy cattle, € 423 million [€ 205-663 million] in beef cattle, € 151million [€ 90-213 million] in dairy sheep, € 206 million [€ 132-248 million] in meat sheep and € 86 million [€ 67-107 million] in dairy goats. Important data gaps were present in all phases of the calculations which lead to large uncertainties around the estimates. Accessibility of more granular animal population datasets at EU level, deeper knowledge of the effects of infection on production, levels of infection and livestock grazing exposure across Europe would make the largest contribution to improved burden assessments. The known current public investment in research on helminth control was 0.15 % of the estimated annual costs for the considered parasitic diseases. Our data suggest that the costs of enzootic helminth infections which usually occur at high prevalence annually in ruminants, are similar or higher than reported costs of epizootic diseases. Our data can support decision making in research and policy to mitigate the negative impacts of helminth infections and anthelmintic resistance in Europe, and provide a baseline against which to measure future changes.
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              Anthelmintic resistance in equine nematodes

              1 The issue of horse nematodes Horses worldwide are exposed to an array of gastrointestinal nematodes. Animals that graze contaminated pasture, and which are not treated with effective anthelmintics, can accumulate large numbers of worms. The most prevalent of these are members of the small strongyle group, the cyathostomins (Ogbourne, 1976; Bucknell et al., 1995; Gawor, 1995; Kuz’mina, 2012; Relf et al., 2013). When the total burden of cyathostomins is high, they can seriously compromise the health of affected individuals (Mair, 1994; Matthews, 2008, 2014). Substantial burdens (i.e. several million) of immature cyathostomins can encyst in the large intestinal wall and it is thought that these stages can persist for years (Murphy and Love, 1997). These stages, in particular early third stage larvae (EL3), are relatively insensitive to most anthelmintics available (Monahan et al., 1996). In temperate areas of the northern hemisphere, cyathostomin larvae encyst primarily during the autumn and winter and can comprise up to 90% of the total burden (Dowdall et al., 2002). When these larvae re-emerge in large numbers from the gut wall, a fatal colitis, larval cyathostominosis, can develop (Giles et al., 1985). Several other nematode species infect horses and other equids, but the prevalence of these species is usually lower than that of cyathostomins (Relf et al., 2013). The most important non-cyathostomin species affecting horses older than one year is Strongylus vulgaris. This nematode can cause non-strangulating intestinal infarction leading to severe colic and was the major parasitic threat to equine health before the advent of broad-spectrum anthelmintics, in particular, the macrocyclic lactones (Reinemeyer and Nielsen, 2009). In younger horses (i.e. those less than 2 years-old), the small intestinal ascarid, Parascaris equorum, can be a substantial risk, producing both respiratory and intestinal signs of disease (Cribb et al., 2006). The lungworm, Dictyocaulus arnfieldi (MacKay and Urquhart, 1979), and the liver fluke, Fasciola hepatica (Owen, 1977), can undergo life cycle development in horses and lead to clinical signs; these are a particular hazard in horses that co-graze with, or graze pastures recently populated by, more permissive hosts such as donkeys and ruminants, respectively. There are few published studies describing the factors that affect the prevalence and abundance of the various parasitic nematode species of horses. A recent publication identified that a lack of rotational grazing practices (between age groups or host species) was associated with a higher prevalence of cyathostomin egg excretion on Thoroughbred stud farms (Relf et al., 2013). In the same study, higher levels of strongyle egg shedding (i.e. >200 eggs per gram) in faeces were observed to be significantly associated with a number of factors, with a recent history of treatment with fenbendazole identified as the most significant factor. The latter observation may be linked to the fact that there is a high prevalence of benzimidazole resistance in cyathostomin populations (see below). Since the 1960s, nematode control has followed interval treatment regimens involving the frequent administration of anthelmintic products at intervals based on strongyle egg reappearance periods (ERP). These periods were defined for each chemical class of compound at the time of licensing (Parry et al., 1993; Kaplan and Nielsen, 2010). Such interval treatment programmes have been successful in substantially reducing the prevalence of strongyle infections and the incidence of large strongyle-associated disease. On the flip side, these programmes have made a substantial contribution to the development of anthelmintic resistance, particularly in cyathostomin species (Kaplan, 2004). Should anthelmintic resistance levels worsen, there will be limited scope for control, as no new classes of compound appear to be under development for use in horses in the short to medium term. Based on comparative studies on sheep nematodes (Jackson and Coop, 2000), reversion to anthelmintic sensitivity is unlikely to occur once populations are measured as anthelmintic resistant by conventional means such as the faecal egg count reduction test (FECRT). For these reasons, more sustainable methods of nematode control are now required, these being based on a requirement to treat animals predisposed to larger burdens to prevent clinical disease, balanced with a need to reduce treatment frequency to preserve anthelmintic efficacy. In the last decade, regulations in the European Union (EU) require that anthelmintics be classified as prescription-only drugs. Currently, the legislation is interpreted differently across the EU, with strictest implementation in Denmark where anthelmintic administration is based on diagnostic evidence of infection (Nielsen et al., 2012). Deployment of such diagnostic-based control strategies requires that robust and practical support tools are available. Coprological analysis for nematode eggs is central to this strategy, but this method is incapable of discriminating pre-patent infection. With the extended pre-patent period of several strongyle species, there is a requirement for diagnostic tests that detect and quantify levels of immature stages. A number of antigens are under investigation as diagnostic markers for detecting pre-patent cyathostomin (McWilliam et al., 2010) and S. vulgaris ( Andersen et al., 2013a) infections. Until these are available, FEC-directed treatments will need to be balanced with anthelmintics applied strategically to target pathogenic larvae (Matthews, 2008). 2 Anthelmintic resistance Interval-based treatment programmes, which have been used extensively in the equine industry, will be expected to select resistance alleles within nematode populations (Kaplan and Nielsen, 2010). Resistance to the earlier registered anthelmintics, the benzimidazoles and the tetrahydropyrimidines, has been reported many times in cyathostomin populations across the world, and resistance to both of these classes in single populations is a common observation in field studies (Kaplan et al., 2004; Traversa et al., 2009; Traversa et al., 2012). As fenbendazole resistance in cyathostomins is virtually ubiquitous in many regions (Osterman Lind et al., 2007; Traversa et al., 2012; Lester et al., 2013b; Relf et al., 2014; Stratford et al., 2014b), this anthelmintic should not be recommended for use in control of these infections in these areas. Perhaps surprisingly, despite the substantial reliance on ivermectin and moxidectin for equine nematode control in the last 30 years, resistance, measured as a reduction in FEC of less than 90–95% at 14–17 days after treatment, has been reported infrequently. Nevertheless, there have now been several reports of reduced strongyle egg ERP after ivermectin or moxidectin administration in a number of countries (von Samson-Himmelstjerna et al., 2007; Molento et al., 2008; Lyons et al., 2009; Lyons et al., 2010; Rossano et al., 2010; Lyons et al., 2011; Lyons and Tolliver, 2013; Canever et al., 2013; Relf et al., 2014). Reduced ERP is believed to provide an early indicator of a shift in a nematode population’s sensitivity towards resistance (Sangster, 2001) and so this provides a warning as to the likely long-term effect of macrocyclic lactone compounds in horses. Ivermectin resistance measured as low FEC reduction after treatment has been reported with regularity in P. equorum populations (Boersema et al., 2002; Hearn and Peregrine, 2003; Stoneham and Coles, 2006; Craig et al., 2007; Schougaard and Nielsen, 2007; von Samson-Himmelstjerna et al., 2007; Reinemeyer, 2012). These findings are unsurprising given the excessively frequent use of ivermectin in foals on stud farms. Control of ivermectin resistant P. equorum populations can theoretically be achieved using tetrahydropyrimidine or benzimidazole compounds; however, ivermectin resistant P. equorum populations have been shown to exhibit resistance to tetrahydropyrimidines as well (Reinemeyer, 2012). Benzimidazole resistance in P. equorum has not yet been published in the literature, but there is now anecdotal evidence of a lack of efficacy of this compound on stud farms in the UK (Matthews, unpublished observations). These reports highlight the threat of multi-class resistance in this nematode species and is a major concern for stud farmers given the potential pathogenicity of this parasite in foals. All of the aforementioned issues highlight the risk of multi-class resistance in equine nematode populations and the complexity of patterns of infection and resistance that will need to be dealt with in the field. As anthelmintic choice now needs to be more evidence based, the tools that inform on levels of infection and anthelmintic efficacy need to be robust. 3 Tools for monitoring infection and detecting anthelmintic resistance 3.1 Faecal egg count analysis The FEC test is a relatively easy method in which the number of strongyle and P. equorum eggs in equine faeces can be estimated at a specific point in time. A number of FEC techniques exist and these differ in sensitivity, speed of generation of results and the level of expertise required to perform the test. In all cases, it is essential that good practice be followed at each stage: from collection of samples at the yard or farm, to processing and analysis in the laboratory. In this way, examination of representative samples should provide a reasonable estimation of the level of egg excretion in each individual. Several studies, published in the last few years, have highlighted several factors that affect the accuracy of FEC analysis in horses and how these factors might impact the outcome of efficacy testing (Nielsen et al., 2010; Vidyashankar et al., 2012; Lester and Matthews, 2014). Generally, FEC test output is affected by differences in egg shedding at individual level (Denwood et al., 2012), the over-dispersion of nematode eggs in faeces (Lester et al., 2012), the non-uniform distribution of nematode eggs in suspension (Vidyashankar et al., 2012), the type of FEC method used (Lester and Matthews, 2014) and by sampling and storage practices (Nielsen et al., 2010). A number of recommendations have come out of these studies and are as follows. Studies on strongyle egg hatching and larval development suggest that faecal samples should be collected as fresh as possible (at most  95% was set for macrocyclic lactone anthelmintics, whilst a threshold of >90% was set for efficacy for benzimidazole and tetrahydropyrimidine anthelmintics. To give an indication of the data range inherent in these datasets, 95% lower confidence limits (LCL) were calculated (Vidyashankar et al., 2007; Lester et al., 2013b; Relf et al., 2014). In terms of the 95% LCL selected for classifying resistance, this varied depending on the class of anthelmintic tested with the percentage reduction threshold used for classifying resistance to macrocyclic lactones set at 90% and, for benzimidazoles and tetrahydropyrimidines, 80%. These cut-offs have been selected to reflect original efficacy levels reported in anthelmintic-sensitive strongyle populations soon after the products were registered for use in horses (Cornwell and Jones, 1969; Colglazier et al., 1977; Xiao et al., 1994). Maximum likelihood models, based on the negative binomial distribution for estimating FEC reduction (Torgerson et al., 2005), and Markov Chain Monte Carlo methods (Denwood et al., 2010) have also been suggested to account for the highly aggregated distribution inherent in equine FEC data. A limitation in these methodologies is that they require the ability to use advanced statistical programmes such as R. Recently, though, a web-interface has been developed to enable researchers to enter FEC datasets online, together with the detection limit of the FEC method used to generate the counts. This interface estimates the percentage of FEC reduction using Bayesian hierarchical models via Markov Chain Monte Carlo sampling (http://www.math.uzh.ch/as/index.php?id=calc, Torgerson et al., 2014) and now provides access for the layperson to more robust methods of computing efficacy. Similar to the issues encountered with the FECRT, there are no well-defined guidelines on how to calculate and interpret strongyle ERP datasets in horses. In the main, two methods have been used: one, defined as the week of the first positive strongyle FEC after anthelmintic administration (Dudeney et al., 2008; Lyons et al., 2008; Molento et al., 2008), and the other, defined when the group arithmetic mean FEC exceeds 10% of the group arithmetic mean FEC at Day 0 (Borgsteede et al., 1993; Jacobs et al., 1995; Boersema et al., 1996; Mercier et al., 2001; Tarigo-Martinie et al., 2001; von Samson-Himmelstjerna et al., 2007; Larsen et al., 2011). The second method gives a more conservative estimate of egg reappearance with respect to the level and spread of the FEC data sampled prior to treatment and so gives a more accurate measure a population’s sensitivity to anthelmintic. More research is warranted and measurement of the ERP parameter needs to be standardized so that analysis can be made between studies. 3.3 Measuring pre-patent infections Because of the pathogenicity of immature cyathostomin and S. vulgaris larvae, diagnostic tests that detect and quantify levels of these stages are required. A number of antigens are under investigation as diagnostic markers for detecting pre-patent cyathostomin (Dowdall et al., 2002; Dowdall et al., 2004; McWilliam et al., 2010) and S. vulgaris ( Andersen et al., 2013a) infections. A cyathostomin ELISA is being developed, which is based on measurement of levels of serum IgG(T) specific to two antigens present in early and late third stage larvae and developing fourth stage larvae (Dowdall et al., 2002; Dowdall et al., 2004; McWilliam et al., 2010). IgG(T) levels specific to these antigens have been shown to increase to 20 and 25 kDa complexes in native extracts of larvae (Dowdall et al., 2004) and to recombinant versions of proteins present within these complexes (McWilliam et al., 2010) within 5–6 weeks of a primary cyathostomin infection. The recombinant proteins have now been evaluated in an indirect ELISA format as a cocktail of antigens spanning nine common cyathostomin species and this cocktail is currently under assessment as to its utility in informing on cyathostomin encysted larval burden. A number of S. vulgaris antigens that are targets of antibody responses in infected horses have been described, but most of these have not been well characterised in terms of their specificity or their predictive value in informing on larval burdens (Andersen et al., 2013b). Recently, a S. vulgaris antigen, SvSXP, was identified as a possible diagnostic marker (Andersen et al., 2013a). Similar to the cyathostomin proteins described above, this antigen was identified by immunoscreening a larval stage complimentary DNA library using rabbit serum raised against adult worm excretory/secretory products. Immunoblotting experiments and preliminary ELISA analysis indicate that serum IgG(T) responses to this protein have potential as diagnostic markers of pre-patent infection (Andersen et al., 2013a). Until these tests are developed further and become commercially available, FEC-directed treatments will need to be balanced with anthelmintic applied strategically to target pathogenic larvae for both types of infections. 4 Sustainable control Clearly, there is a real need for better management of equine nematodes, with improvement in anthelmintic use decisions the cornerstone of improved programmes that aim to avoid unnecessary or ineffective treatments. The practice of FEC-directed treatments can be highly effective in reducing anthelmintic administration frequency in horses because egg excretion is highly over dispersed amongst individuals (Relf et al., 2013; Lester et al., 2013b). A commonly quoted dogma is that 20% of the equine population excretes 80% of the parasite burden into the environment (Matthews, 2008) and recent studies have demonstrated that, in well-managed populations, the actual percentage of horses responsible for 80% excretion is lower than 20% (Relf et al., 2013; Lester et al., 2013b). In FEC-directed treatment programmes, high shedders (for example, horses excreting more than 200 eggs per gram [EPG] in faeces) are targeted with anthelmintics, whilst those identified as shedding negligible to moderate levels of eggs are left untreated (Duncan and Love, 1991). In this way, anthelmintic treatments are reduced at the same time as pasture contamination is lowered. It is assumed that nematodes in untreated horses will act as a source of ‘refugia’ (van Wyk, 2001) and that the progeny of these will act to dilute resistant alleles in offspring derived from worms that survive in horses administered with anthelmintic. There have been no quantitative studies that substantiate these principles in horses; nevertheless, the delivery of fewer anthelmintic treatments over time and the requirement to monitor nematode egg excretion profiles within populations provides the basis for more responsible control programmes. Due to the long pre-patent period of a number of strongyle worm species and, because severe disease can be caused by the larval stages of some of these species, FEC-directed treatments need to be balanced with a requirement to treat stages of nematodes that are undetectable by FEC analysis. In the absence of diagnostic tests that allow estimation of immature larvae, treatments with larvicidal anthelmintics (i.e. moxidectin) are recommended at specific times of year (Matthews, 2008; Hertzberg et al., 2014). The future availability of diagnostics that allow estimation of burden of pre-patent stages will enable specific targeting of individuals with larvicidal anthelmintics, as these tests can be used to identify horses estimated to harbour above a certain threshold of larval numbers. Such targeting should facilitate further reductions in anthelmintic usage at those times of year when larvicidal treatments are indicated. Targeted treatment programmes have had variable uptake across regions and countries and between different types of management systems, with poorer uptake on Thoroughbred stud farms (Relf et al., 2013; Robert et al., 2014) and better uptake by the leisure horse sector (Lester et al., 2013a; Stratford et al., 2014a). Where targeted treatment programmes have been followed, large reductions in anthelmintic use have resulted (Lester et al., 2013a). The challenge now lies in disseminating these programmes further. Recent data from the USA indicates that stud farm owners, for example, are only willing to change to more evidence-based control measures if they are assured that such approaches would prevent anthelmintic resistance and decrease health risks significantly (Robert et al., 2014). Further research is required to provide such evidence, particularly as one recent study indicated an apparent increase in the prevalence of S. vulgaris infections on farms where reduced anthelmintic treatment intensity had been implemented over several years (Nielsen et al., 2012). Despite a gradual move towards more evidence-based anthelmintic use, the prevalence of resistance in some populations is very high, with resistance reported to every class available (Trawford and Burden, 2012). Thus, it is imperative that, alongside implementation of these strategies, other methods of control are used so that there is not sole reliance on the use of anthelmintics to break the nematode transmission cycle. One option is to reduce contamination of grazing by removal of faeces from pasture. In 1986, Herd (Herd, 1986) demonstrated that pasture management, via the removal of faeces twice a week alone, was more effective than anthelmintic therapy in reducing pasture levels of strongyle larvae. This study was performed before the widespread use of moxidectin, which has a prolonged egg suppressive effect. More recently, studies undertaken on a UK donkey sanctuary confirmed the effectiveness of faecal removal from pasture in reducing nematode transmission (Corbett et al., 2014). These studies confirmed that twice-weekly removal of faeces from pasture significantly reduced the number of strongyle eggs shed in faeces from groups of co-grazed donkeys, thus verifying this practice was a useful management tool to further reduce use of anthelmintics. Faecal removal is recommended at intervals frequent enough to prevent third stage larvae developing and translating onto pasture and this interval has been measured as approximately two weeks in warm temperate conditions (Ramsey et al., 2004), but development may be more rapid in tropical and sub-tropical regions. Alternated grazing with ruminants will also decrease levels of strongyle contamination on pasture over time, but care must be taken to monitor for helminths that can be transmitted between sheep and horses (in particular, F. hepatica). Further research is required in these areas to provide quantitative evidence on the utility of these control methods and to provide baseline values on which to build practical recommendations. 5 Final conclusions The lack of benzimidazole and tetrahydropyrimidine efficacy measured in equine nematode populations across the world, along with clear indications of emerging resistance against ivermectin and moxidectin, emphasises the need for fundamental changes in the way that nematodes are managed in horses. The macrocyclic lactone anthelmintics have the major market share globally and until recently, serious consideration had not been given to protecting efficacy of these compounds by implementing control programmes that use these medicines in a more targeted manner. Although targeted programmes are being used in some regions, the advantages of these programmes need further dissemination to ensure further uptake. Many horses are still subjected to regular blanket anthelmintic treatments with no attention paid to efficacy and a lack of uptake of evidence-based strategies may be due to the perceived complexity involved in integrating these methods in practice. It is essential that barriers be broken down so that those involved in prescribing and administering anthelmintics have confidence in delivering evidence-based protocols. This requires that stakeholders have easy access to up-to-date knowledge, as well as to robust diagnostic tests required to support decision-making. The gap between research findings and implementation at farm level is a continuing challenge for scientists working in equine parasitology. One piece of evidence to start reducing this gap is that initial feedback from horse owners indicates that by using targeted treatment strategies, considerably fewer anthelmintic treatments are applied (Lester et al., 2013a; Hertzberg et al., 2014). Furthermore, that this can lead to substantial financial savings (Lester et al., 2013a). There is still a requirement for better tools that will inform evidence-based parasite control, but new tests are on the horizon and these will need to be priced and marketed properly to ensure that they are used across the equine industry. By moving to evidence-based parasite management built on best practice (i.e. limiting use of anthelmintics and ensuring correct dose rates), combined with targeted grazing management and exploiting available diagnostic tools, the efficacy of the currently effective anthelmintics might be prolonged until new chemotherapeutics are discovered. This is paramount because reversion to anthelmintic susceptibility, in all probability, will not occur in nematode populations once they have become resistant. Conflict of interest The authors declared that there is no conflict of interest.
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                Author and article information

                Journal
                Parasite
                Parasite
                parasite
                Parasite
                EDP Sciences
                1252-607X
                1776-1042
                2022
                07 April 2022
                : 29
                : ( publisher-idID: parasite/2022/01 )
                : 20
                Affiliations
                [1 ] School of Biological Sciences, Queen’s University Belfast 19, Chlorine Gardens BT9 5DL Belfast United Kingdom
                [2 ] Laboratorio de Farmacología, Centro de Investigación Veterinaria de Tandil (CIVETAN) (UNCPBA-CICPBA-CONICET), Facultad de Ciencias Veterinarias, UNCPBA 7000 Tandil Argentina
                [3 ] Department of Veterinary Medicine and Animal Production, University of Naples Federico II Via Delpino, 1 80137 Naples Italy
                [4 ] Kreavet Hendrik Mertensstraat 17 9150 Kruibeke Belgium
                [5 ] Faculty of Veterinary Medicine, University of Gent Salisburylaan 133 9820 Merelbeke Belgium
                Author notes
                [* ]Corresponding author: eric.morgan@ 123456qub.ac.uk
                Article
                parasite210159 10.1051/parasite/2022017
                10.1051/parasite/2022017
                8988865
                35389336
                d04e641e-af84-422c-b6fe-9f560f6317ed
                © E.R. Morgan et al., published by EDP Sciences, 2022

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

                History
                : 29 November 2021
                : 07 March 2022
                Page count
                Figures: 2, Tables: 1, Equations: 0, References: 101, Pages: 13
                Funding
                Funded by: European Cooperation in Science and Technology, doi 10.13039/501100000921;
                Award ID: CA16230
                Funded by: Biotechnology and Biological Sciences Research Council, doi 10.13039/501100000268;
                Award ID: BBR0102501
                Categories
                Review Article
                Special Issue – Combatting Anthelmintic resistance in ruminants. Invited Editors: Johannes Charlier, Hervé Hoste, and Smaragda Sotiraki

                helminths,anthelmintic resistance,faecal egg count reduction test,drug pharmacology related therapeutic failures,pharmacokinetics,epidemiology,effectiveness

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