Common Helminth Infections of Donkeys and Their Control in Temperate Regions J

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EQUINE VETERINARY EDUCATION / AE / SEPTEMBER 2013 461

Review Article Common helminth infections of donkeys and their control in temperate regions J. B. Matthews* and F. A. Burden† Disease Control, Moredun Research Institute, Edinburgh; and †The Donkey Sanctuary, Sidmouth, Devon, UK. *Corresponding author email: [email protected]

Keywords: horse; donkey; helminths; anthelmintic resistance

Summary management of helminths in donkeys is of general importance Roundworms and flatworms that affect donkeys can cause to their wellbeing and to that of co-grazing animals. disease. All common helminth parasites that affect horses also infect donkeys, so animals that co-graze can act as a source Nematodes that commonly affect donkeys of infection for either species. Of the gastrointestinal nematodes, those belonging to the cyathostomin (small Cyathostomins strongyle) group are the most problematic in UK donkeys. Most In donkey populations in which all animals are administered grazing animals are exposed to these parasites and some anthelmintics on a regular basis, most harbour low burdens of animals will be infected all of their lives. Control is threatened parasitic nematode infections and do not exhibit overt signs of by anthelmintic resistance: resistance to all 3 available disease. As in horses and ponies, the most common parasitic anthelmintic classes has now been recorded in UK donkeys. nematodes are the cyathostomin species. The life cycle of The lungworm, Dictyocaulus arnfieldi, is also problematical, these nematodes is the same as in other equids, with a period particularly when donkeys co-graze with horses. Mature of larval encystment in the large intestinal wall playing an horses are not permissive hosts to the full life cycle of this important role in the epidemiology and pathogenicity of parasite, but develop clinical signs on infection. In contrast, infection. In some donkeys, encysted larvae build up in large donkeys are permissive hosts without displaying overt clinical numbers and can emerge synchronously to cause larval signs and act as a source of infection to co-grazing horses. cyathostominosis. The latter is associated with one, or all, of the Donkeys are also susceptible to the fluke, Fasciola hepatica. following: sudden onset weight loss, colic and, rarely in This flatworm can be transmitted, via snails and the donkeys, diarrhoea. The case fatality rate of larval environment, from ruminants. As with cyathostomins, cyathostominosis in donkeys is not known, although, in this anthelmintic resistance is increasing in fluke populations in the species, it would appear to be lower than observed in other UK. A number of the anthelmintic products available for horses equids, which, in some reports, approaches 50% (Giles et al. do not have a licence for use in donkeys, and this complicates 1985). Encysted larvae can persist for many months and, the design of parasite control programmes. As no new equine during autumn/winter in the UK, the larvae can comprise the anthelmintic classes appear to be near market, it is important majority of the cyathostomin burden. This being the case, that the efficacy of currently effective drugs is maintained. It is donkeys can harbour considerable levels of infection but the important that strategies are used that attempt to preserve parasites (encysted larvae) are not detectable by routine anthelmintic efficacy. These strategies should be based on the faecal egg count (FEC) analysis. concept that the proportion of worms in a population not The impact of cyathostomin infections on working donkeys exposed to anthelmintic at each treatment act as a source of is unclear; some studies indicate that they have a negative ‘refugia’. The latter is an important factor in the rate at which effect on body condition score and are associated with the resistance develops. Thus, it is imperative that parasite control presence of anaemia (Matthee et al. 2002). Other studies programmes take into account the need to balance therapy show no correlation between FEC and body condition score to control helminth-associated disease with the requirement to (Getachew 2006; Burden et al. 2010). Donkeys do appear to preserve anthelmintic effectiveness. remain ‘healthy’ when high levels of cyathostomin infection are present, as long as they are not nutritionally compromised or overworked (Getachew 2006; Burden et al. 2010). A recent Introduction randomised blinded control study carried out in Morocco by Perhaps one of the biggest challenges when managing Crane et al. (2011) showed significant increases in body helminths in donkeys is that of clinical assessment. Donkeys condition score in those equids that received anthelmintic with significant helminth burdens may appear healthy and it is treatment when compared to those that were administered a rare to observe the type of clinical signs (diarrhoea, weight placebo; however, no significant change in bodyweight was loss, colic or poor condition) that are more common in horses. noted. Further research is needed in this area, particularly in Morrow et al. (2011) determined that, of 1444 donkeys that light of the significant expenditure required to maintain the presented at post mortem, 16% harboured helminth infections mass deworming programmes that are commonly a mainstay that were considered to be of a moderate to high of charities working with equids in the developing world. cyathostomin or mixed species burden. The importance of Like other equids, individual donkeys vary in susceptibility to parasites as a significant cause of morbidity and mortality in cyathostomins. Generally, in well managed populations, within otherwise healthy donkeys is as yet undetermined; however, a group, the majority control their level of infection relatively extrapolation of data from horses would suggest that well. This is manifest as a negative or low FEC. Often, a few

500 faecal samples obtained from donkeys tested in Ethiopia and 450 in 100% of donkeys that were examined post mortem. 400 350 Parascaris equorum 300 Horses and ponies acquire immunity to this small intestinal 250 nematode relatively quickly with age and exposure: patent Ave FEC Farm A 200 infections (as detected by the observation of round, thick-shelled eggs in faeces) are usually only seen in 150 Ave FEC Farm B horse/pony foals. In donkeys, however, mature animals 100 harbour patent infections (Getachew et al. 2010b). Hence, 50 Average FEC over 12 months Average otherwise healthy, mature donkeys may be important sources 0 of pasture contamination and, when compromised through 0–3 4–6 7–20 21–25 26–35 36+ overwork, ill health or poor nutrition, may be at risk of disease. Age group (years) The life cycle of P. equorum is migratory and infection is in the Fig 1: Graph showing average strongyle faecal egg count over a form of an environmentally resistant egg containing a second 12-month period (2011) at the UK Donkey Sanctuary for resident stage larva. Time from infection to detection of eggs in faeces populations of donkeys present on Farm A (n = 348 donkeys) or is approximately 10 weeks. The parasite is relatively common, Farm B (n = 225 donkeys). These donkeys were on a targeted especially on large operations where animals graze treatment programme and were administered anthelmintics when permanent pastures and can cause clinical problems when their faecal egg count exceeded 1000 eggs/g. infection intensity is high. Because the migratory pattern is hepato-tracheal, respiratory signs are observed in animals animals will harbour high levels of infection and will excrete under high levels of challenge. Other signs include failure to moderate to high numbers of eggs into the environment. It is thrive, whole adult worms in faeces and, in cases where these individual donkeys that act as the main source of infection intensity is high, direct effects on the intestine. The pasture contamination with infective cyathostomin larvae and latter effect is rare but holds a poor prognosis. There have it is thought, but not proven, that each donkey’s relative been a number of reports of treatment failure of anthelmintics susceptibility to cyathostomin infection is maintained through (primarily, ivermectin) against P. equorum in horse foals life. Cyathostomin infections tend to be higher in younger (von Samson-Himmelstjerna 2012) and the authors have donkeys, especially those grazed on permanent pastures; experienced treatment failure against P. equorum with however, mature donkeys can harbour substantial infections ivermectin, moxidectin and pyrantel embonate when used in and therefore contribute to pasture contamination or develop donkeys. Therefore, anthelmintic resistance in this nematode disease. An exemplar dataset derived from 2 populations of species should be considered when designing control donkeys based on 2 farms at the UK Donkey Sanctuary programmes. (Devon) with mixed age populations is shown in Figure 1. This < demonstrates that young (age 3 years) and old (age Oxyuris equi > 26 years) donkeys may not always be the highest strongyle Oxyuris equi (pinworm) is relatively common in horses and egg shedders and, in fact, in both instances, mature donkeys ponies, but not as common as the cyathostomins (Bucknell can contribute substantially to pasture contamination. Clearly, et al. 1995; Upjohn et al. 2010). Oxyuris equi are primarily the role of mature donkeys as contributors to contamination considered a nuisance or irritant, but in some animals should be assessed carefully when managing foals, persistent infection can lead to damage around the perineum immunocompromised animals or mixed equine herds. and tail head. The nematodes are found in the terminal portion of the large intestine. Female worms are found in Large strongyles higher numbers than males and when gravid, pass out of the Donkeys are susceptible to large strongyle (Strongylus) species. rectum to lay eggs, which stick to the skin. These are observed Like cyathostomins, adult worms are found in the large as yellow, crusty masses and eggs containing L3 become intestine, but the parasitic larval stages are migratory with time infective in 4–5 days. Time from infection to the release of eggs from infection to detection of eggs in faeces in the region of is in the region of 5 months. Adult pinworms cause perineal 6–12 months. Apart from this, the life cycle and epidemiology irritation in horses leading to rubbing with broken hairs and are similar to cyathostomins and currently control strategies for bare patches on the perineum and tail head. Donkeys do not, these parasitic nematodes are handled as one. The however, appear to demonstrate this behaviour as frequently pathogenicity of large strongyles is related to the migratory (F.A. Burden, unpublished observations). Identification of pattern of the larvae and tissue feeding habit of the adults. The infection in donkeys is often by the observation of adult worms availability of macrocyclic lactones (ML), ivermectin and, passed in faeces. Faecal examination may not reveal later, moxidectin, led to substantial reductions in the infection and samples should be collected from around the prevalence of large strongyle infections in managed equine perineal region. Anthelmintics that have demonstrated populations as these anthelmintics are highly effective against efficacy against larval and adult O. equi in horses include the pathogenic larval stages. No reports of anthelmintic ivermectin, moxidectin and fenbendazole, although not all resistance have been reported in these species. Large brands have a licence for this activity. Pyrantel has strongyle infections remain a real threat to working donkeys demonstrated efficacy against adult stages only. No and mules in developing regions where administration of ML published studies are available describing efficacy of these anthelmintics is erratic or absent (Getachew et al. 2010a); for products against O. equi in donkeys. Recently, there have example, Strongylus spp. were identified in over 90% of pooled been a number of unpublished reports of reduced

anthelmintic efficacy against O. equi in horses (Reinemeyer (Getachew et al. 2012). A low prevalence (~3%) of infection 2012) and the authors have experienced a lack of response to has been identified by coprology in donkeys entering the treatment with both ivermectin and pyrantel in donkeys. It is UK Donkey Sanctuary (F.A. Burden, unpublished data). In this important that good hygiene is practiced to reduce the levels case, most tapeworm egg-positive donkeys originated from of infective eggs in the environment. Thorough cleaning with a Ireland or Wales. strong disinfectant after removal of all bedding will reduce the In horses, a number of studies have described the effects risk of infection from the environment. Although there are no of A. perfoliata at the attachment site, the ileo-caecal published studies detailing efficacy of disinfectants against junction (Proudman and Trees 1999); however, nothing is O. equi eggs, extrapolation from studies on human pinworms reported about the clinical effect on donkeys. A post mortem would indicate that better levels of personal hygiene lead to a survey (n = 1617) at the UK Donkey Sanctuary indicated <0.5% lower the risk of infection to individuals (Mazhilene 1991; Wang prevalence of tapeworm infection, with only one tapeworm- et al. 2010). associated clinical case reported over a 5-year period (F.A. Burden, unpublished data). A. perfoliata infection is thought to Dictyocaulus arnfieldi occur all year round; however, recent studies in horses in This is relatively common in donkeys, which, in contrast to Germany indicated a peak in late summer/autumn (Roelfstra mature horses, are permissive of the entire life cycle. However, et al. 2006). Specific treatment with a product with licensed the availability of MLs has reduced the number of donkeys efficacy against A. perfoliata is recommended at this time of infected with D. arnfieldi: in a recent study, only 4% of animals year. Praziquantel is not licensed for use in donkeys in the UK. entering the UK Donkey Sanctuary for the first time were positive on coprological examination (F.A. Burden, unpublished data). Common trematodes that affect donkeys Adult worms are found in the respiratory passages and eggs are coughed up and swallowed and passed out in the faeces. Fasciola hepatica Note that this is different to lungworms of other host species in Fasciola hepatica affects mainly cattle and sheep, but can which first stage larvae (L1) are usually detected in faecal infect all grazing animals. It is common in the wetter, western samples. D. arnfieldi eggs hatch quickly, so diagnostic analysis areas of UK and in Ireland, but infection is spreading should include examination for eggs by standard FEC geographically, probably associated with changes in climate methods, particularly if samples are fresh and have been and the difficulty of controlling this parasite due to increasing stored anaerobically, as well as by Baermanisation (Rode and resistance to the commonly used anthelmintic, Jørgensen 1989) for L1. Donkeys do not often exhibit clinical triclabendazole (Fairweather 2011). The adult fluke is found in signs of infection, yet may excrete large numbers of eggs in the bile ducts and overt clinical signs are not usually observed their faeces. Donkeys most at risk of developing disease related in infected donkeys; however, thickened bile ducts and raised to high infection intensity are those that are geriatric and/or levels of liver enzymes in serum may occasionally be noted in immunocompromised. The administration of corticosteroids or heavily infected animals (Collins 1961). Little is known of the pars pituitary intermedia dysfunction appear to be correlated overall prevalence of F. hepatica in donkeys in the UK: a with higher lungworm burdens (F.A. Burden, unpublished data) recent coprological survey (n = 735) of new relinquishments to and the screening of such donkeys for D. arnfieldi infection is the UK Donkey Sanctuary indicated an infection prevalence recommended. Co-grazing horses are more likely to develop of 4%, the majority of positive animals originating from Wales clinical signs (for example, coughing), so care must be taken and Ireland (F.A. Burden, unpublished data). Another study at to control for lungworms in resident donkeys. Mules appear the UK Donkey Sanctuary indicated that, of 60 post mortem to be able to support the full life cycle (Solomon et al. examinations performed on donkeys transferred from Ireland, 2012), although less commonly than observed in donkeys, F. hepatica was identified in 17% of livers examined and, of 200 and, so, may be more susceptible to disease. Most broad faecal samples assessed, 8.5% were positive for F. hepatica spectrum anthelmintics have a label claim for lungworm in eggs (Trawford and Tremlett 1996). In the latter study, it was donkeys (please refer to http://www.noahcompendium.co.uk/ noted that there was little reaction to the flukes in the liver. A Compendium/Overview). recent study in working donkeys in Ethiopia indicated that Fasciola spp. (F. hepatica and F. gigantica) were common in Common cestodes that affect donkeys donkeys of all ages: prevalence rates identified at post mortem (n = 112) and coprologically (n = 803) were in the Anoplocephala perfoliata region of 40–45% (Getachew et al. 2010b). In this study, This parasite has an indirect life cycle involving an oribatid infection intensity was significantly higher in donkeys that were mite. Information on this parasite in donkeys is scant. A aged 8 years or older. For these reasons, where Fasciola Pubmed search of publicly available databases reveals that species are known to be present in other hosts, control few papers detail the prevalence of ‘cestode infections’ in programmes must address the exclusion of snail habitats (by donkeys. In one, ‘cestodes’, including A. perfoliata (the fencing or drainage), which will help break the life cycle. No commonest tapeworm found in horses in the UK), were products are licensed specifically for use against flukes in identified in 8% of working donkeys examined in Ethiopia donkeys: in the UK, triclabendazole and other flukicides can (Getachew et al. 2010a) and, in another in Burkina Faso be used under the ‘Cascade’ (http://www.noah.co.uk/issues/ (Vercruysse et al. 1986), the presence of Anoplocephala briefingdoc/24-cascade.htm). The latter is a legal flexibility magna was reported in varying numbers. Proudman and Ellis that allows a rational balance between the legislative (1995) identified infection rates of A. perfoliata of 27% by requirement for veterinary surgeons to prescribe and use coprology and 40% by antigen specific antibody ELISA in a authorised medicines where available and the need for group of donkeys studied in the Welsh borders. Serology also professional freedom to prescribe other products where they indicated a 34% infection rate in donkeys in Ethiopia are not and is intended to increase the choice of medicines

TABLE 1: Anthelmintics available for use in treating helminth infections in donkeys in the UK

Anthelmintic class Active ingredient Indication Dose rate

Macrocyclic lactones Ivermectin GI nematodes, Dictyocaulus arnfieldi 0.2 mg/kg bwt per os Moxidectin* As above + encysted cyathostomin larvae 0.4 mg/kg bwt per os Benzimidazoles Fenbendazole† GI nematodes, 7.5 mg/kg bwt per os or 7.5 mg/kg bwt Triclabendazole* D. arnfieldi per os for 5 days for cyathostomin Immature and mature Fasciola hepatica encysted larvae 18 mg/kg bwt Tetrahydropyrimidines Pyrantel embonate Gastrointestinal nematodes 19 mg/kg bwt Anoplocephala perfoliatia 38 mg/kg bwt Pyrozinoisoquinolines Praziquantel* A. perfoliatia and other tapeworms 2.5 mg/kg bwt Salicylanilides Closantel* Mature F. hepatica 20 mg/kg bwt

* Not licensed for use in donkeys. Prescribe under the CASCADE: refer to http://www.vmd.defra.gov.uk/pdf/vmgn/VMGNote15.pdf † High levels of resistance to this anthelmintic reported in cyathostomins, worldwide. available for specific conditions. Please note that a risk of triclabendazole resistance must be taken into account. Where triclabendazole is not effective, closantel may be considered; however, due to this chemical only being effective against adult stage fluke, repeat dosing is necessary. 1000

Anthelmintic use in donkeys FWEC Few products have specific label indications for donkeys and medicines are often administered based on dose rates Mean 500 optimised for use in horses. Donkeys are adapted to living in arid areas and thrive on poor quality fodder and, because of physiological differences associated with these adaptations, donkeys differ from horses and ponies in how they distribute, metabolise and excrete xenobiotics. This has implications for May June July AugustSeptember October Automated water compartment partitioning which affects drug Manual distribution (Grosenbaugh et al. 2011). All 3 modern No Removal anthelmintic classes (Table 1) available for administration to Fig 2: The average number of strongyle eggs/g/group calculated horses have been shown to be effective in donkeys when in 3 groups of donkeys grazing land with different pasture administered at doses determined for the former (Malan and management protocols over a grazing season. Automated (blue Reinecke 1979; Taylor and Craig 1993; Crane et al. 2011); line) or manual (pink line) collections of faeces were carried out however, a number of products are not licensed for use in twice per week throughout the grazing season for 2 of the groups. donkeys and care must be taken to acknowledge the For the remaining group (green), faeces were not lifted from pasture. Data courtesy of Dr M.L. Denwood and Professor S. Love, appropriate label claim for each active ingredient or brand. University of Glasgow, 2011. FWEC, faecal worm egg count. Early studies with moxidectin indicated shorter strongyle egg reappearance periods in donkeys than was observed at the exposure to high levels of parasite challenge. To restrict time in horses (Matthee et al. 2002). Indeed, the first report of grazing, they are often enclosed using electric fencing to moxidectin resistance in cyathostomins was observed in encourage strip grazing; although of benefit to weight control, donkeys (Trawford et al. 2005). This anthelmintic is not licensed this can lead to abnormal dunging behaviour, with lack of for donkeys and this presents difficulties for cyathostomin establishment of natural latrine areas away from grazing and control when treatments for encysted larvae are required. In so parasite challenge may be high. In these cases, good the UK, only a 5-day course of fenbendazole has licensed pasture hygiene is paramount; dung should be lifted at least efficacy against cyathostomin encysted larvae, but there is twice per week and consideration should be given to methods widespread resistance in these nematodes to this anthelmintic of pasture restriction that enable animals to establish latrine type. areas. Studies at the UK Donkey Sanctuary have shown substantially reduced strongyle FEC in donkeys grazing Helminth control in donkeys pastures where dung was lifted mechanically or manually Donkeys have different nutritional requirements and natural twice a week compared to pastures with no dung removal at behaviour compared to other equids. When donkeys are kept all (Fig 2). Management of manure is important; it should be in temperate climates, they can become obese if allowed free composted with temperatures reaching a minimum of grazing access. Thus, grazing is often restricted for much of the 50–70°C maintained for over 8 h (Hébert et al. 2010). year, with donkeys commonly grazed at 0.1–0.2 ha/animal. Generally, compost heaps require turning and maintenance Such stocking densities mean that larval contamination can at these levels for a minimum of 3 weeks to ensure destruction become high on land that is not effectively managed. of helminth eggs throughout the heap. If possible, alternative Although donkeys are selective grazers that will not, by choice, means of disposal should be sought or manure heaps sited so graze areas soiled by dung, when enclosed on small areas, that they are not accessible and run-off will not contaminate they graze close to or inside dunging areas, with resultant grazing land.

Grazing with livestock other than equids is to be during the grazing season when they can be used to identify encouraged; sheep and cattle may act as biological vacuum the relative contribution that individuals make to pasture cleaners, with few parasite species being shared between the contamination (Matthews 2010). All co-grazers should be different host types. In areas with high fluke prevalence and tested simultaneously after the effective refractory period of where the environment may support snails, fluke infection the previously administered anthelmintic has elapsed. status of sheep should be assessed before allowing them to Individuals with a FEC in excess of a set threshold should be graze donkey pasture. It is not advisable to graze sheep with treated with a licensed anthelmintic, (ideally, shown previously donkeys that are unaccustomed to them, as donkeys may to be effective), at a dose rate of 100–110% bodyweight exhibit aggressive behaviour towards unknown livestock estimated by weight tape or scale. The most frequently cited (Burden and Trawford 2006); sheep are best employed to FEC cut-off for determining treatment is 200–500 eggs/g graze after donkeys before a period of pasture rest. Ideally, (Matthews 2008). Subsequently, FEC may be performed at 2–3 grazing should be allowed at least 6 months to reduce parasite monthly intervals depending on the product used. Since FEC populations (Kuzmina et al. 2006). do not detect cyathostomin encysted larvae, larvicidal Individual donkeys differ in susceptibility to strongyle treatments can be administered when considered most infections; this is likely to result in over-dispersed patterns of appropriate (for example, late autumn or winter in the UK). faecal egg excretion, which, at the appropriate time of year, A total reduction in administration of some anthelmintic provides an opportunity for control via targeted therapy classes (for example MLs) could potentially lead to the (Sangster 2003). In horses and ponies, ‘high egg shedders’ increased prevalence of parasite species or stages (for generally maintain higher lifelong FEC patterns, despite similar example Strongylus spp. or P. equorum). Following a decade exposure levels (Becher et al. 2010). Temporal data indicating of targeted treatment application in Denmark, it was initially such patterns in donkeys are lacking. As indicated above, the noted that the prevalence of S. vulgaris had remained similar clear effect of age on strongyle egg output, in part explained to that observed in Sweden, where such treatment regimes by the acquisition of immunity in horses (von Samson- had not been instituted to the same degree (Nielsen 2009). In Himmelstjerna et al. 2009), does not appear to be as clear cut a further Danish study in which larval culture analysis was in donkeys. Despite recommendations being described for performed to identify strongylid nematodes in faecal samples targeted therapy in equids over 20 years ago (Duncan and from farms that instituted targeted treatments based on FEC Love 1991), there has been relatively poor implementation analysis compared to those that treated without using FEC, of this strategy in the field. The principal objective is to S. vulgaris prevalence was significantly higher where targeted decrease selection pressure for anthelmintic resistance, whilst therapy had been applied (Nielsen et al. 2012). Donkeys newly maintaining health by reducing infection intensity (Stratford relinquished and resident at the UK Donkey Sanctuary have et al. 2011). Variation in environmental conditions, pasture been rarely found to harbour large strongyles (<0.1% of management and herd dynamics mean that no one protocol donkeys at post mortem over a 5-year period; F.A. Burden, can be applied uniformly; an understanding of the target unpublished data). However, further research is required helminth species, appropriate diagnostic tests (and their and baseline prevalence data are essential to assess the limitations), along with a knowledge of anthelmintic sensitivity impact of changes in parasite management regimes over provide the concepts on which to base best practice control. time. When low faecal egg shedders are left untreated, helminth In terms of quarantine, the UK Donkey Sanctuary screens all eggs in their faeces are thought to provide ‘refugia’, which relinquishments for strongyles, P. equorum (regardless of age), serve to dilute eggs laid by worms that have survived in liver fluke and lungworm coprologically. Coprological anthelmintic treated animals. As parasite refugium is assessment is also carried out for tapeworm. Although considered to be the most influential factor in the sensitivity is low (Meana et al. 1998), unless there is a specific development of anthelmintic resistance and the rate at which concern, tapeworm serology is not carried out as it increases (van Wyk 2001), repeated, simultaneous the available ELISA (Diagnosteq, http://www.liv.ac.uk/ treatments of all animals, irrespective of FEC, are not diagnosteq/) has not been validated for donkey serum IgG(T). recommended. Donkeys or mules whose test results indicate a patent infection Faecal egg count should be used regularly to target with P. equorum, liver fluke, lungworm or tapeworm are helminth adulticidal treatments and can be performed treated appropriately and follow-up FEC are analysed 14–21 ‘in-house’ as they require little specialised equipment or days post treatment to gauge efficacy of treatment. Donkeys particularly advanced skills. Alternatively, a number of with positive strongyle FEC may be treated above 300 eggs/g laboratories offer a commercial FEC service. The McMaster (or dependent upon the clinical picture. If there is concern that a modified McMaster) test, based on a flotation/dilution newly acquired donkey or mule entering a group harbours principle, is the most commonly used technique. A lungworm or P. equorum that may not have reached patency, centrifugal-flotation technique is more sensitive, particularly at ivermectin is administered immediately and the animal low egg numbers (Bello and Allen 2009). Faecal samples quarantined from grazing for 48 h. should be collected as fresh as possible and placed into sealable bags, excluding as much air as possible to reduce egg development. Samples collected in this way can be Assessing anthelmintic efficacy refrigerated in airtight containers for up to 120 h without a Anthelmintic resistance may be suspected following a FEC significant change in nematode egg numbers (Nielsen et al. reduction test, a reduction in the expected effective 2010). FEC do not provide a gauge of total nematode refractory period after anthelmintic treatment, or by clinical burdens; especially during autumn and winter in the UK when signs of disease where appropriate dosing is thought to have cyathostomin encysted larval levels can be high. For this occurred. The FEC reduction test compares FEC before (Day 0) reason, FEC are of most use in targeted therapy strategies and 10–14 days after anthelmintic treatment. It is simple to

perform, can be applied to all classes of anthelmintic and is Crane, M.A., Khallaayoune, K., Scantlebury, C. and Christley, R.M. the most widely used screening test for resistance. Efficacy is (2011) A randomized triple blind trial to assess the effect of an anthelmintic programme for working equids in Morocco. BMC Vet. calculated using the formula: Res. 7,1. Duncan, J.L. and Love, S. (1991) Preliminary observations on an (Day 0 mean FEC alternative strategy for the control of horse strongyles. Equine Vet. J. − 14 day post treatment mean FEC) ×100 23, 226-228. Reduction (%) = Fairweather, I. (2011) Reducing the future threat from (liver) fluke: Day 0 FEC realistic prospect or quixotic fantasy? Vet. Parasitol. 180, 133-143. Getachew, M. (2006) Endoparasites of working donkeys in Ethiopia: Accuracy can be affected by inherent variability in FEC within epidemiological study and mathematical modelling. PhD thesis, University of Glasgow. and between donkeys, and it can be difficult to interpret data Getachew, M., Trawford, A., Feseha, G. and Reid, S.W. (2010a) derived from populations where there are large proportions of Gastrointestinal parasites of working donkeys of Ethiopia. Trop. Anim. animals that have low or zero FEC (Matthews 2011). Pre- and Health Prod. 42, 27-33. posttreatment samples should be handled and processed Getachew, M., Innocent, G.T., Trawford, A.F., Reid, S.W. and Love, S. similarly. Performing the test on a large proportion of the (2010b) Epidemiological features of fasciolosis in working donkeys in population will provide the most accurate representation of Ethiopia. Vet. Parasitol. 169, 335-339. sensitivity. Different FEC reduction percentage cut-offs are Getachew, A.M., Innocent, G., Proudman, C.J., Trawford, A., Feseha, recommended for different classes of anthelmintic; recent G., Reid, S.W., Faith, B. and Love, S. (2012) Equine cestodosis: a sero-epidemiological study of Anoplocephala perfoliata infection in recommendations state these as 90% for BZs and Ethiopia. Vet. Res. Commun. 36, 93-98. tetrahydropyrimidines and 95% for MLs (Kaplan and Nielsen Giles, C.J., Urquhart, K.A. and Longstaffe, J.A. (1985) Larval 2010). These threshold percentages take into account cyathostomiasis (immature trichonema-induced enteropathy): a variation in efficacy when the anthelmintics were initially report of 15 clinical cases. Equine Vet. J. 17, 196-201. tested for licensing. A population mean FEC reduction above Grosenbaugh, D.A., Reinemeyer, C.R. and Figueiredo, M.D. (2011) these cut-offs represents acceptable efficacy, whilst a lower Pharmacology and therapeutics in donkeys. Equine Vet. Educ. 23, mean FEC reduction is indicative of resistance. Ideally, in cases 523-531. of suspected resistance, the test should be repeated: a Hébert, L., Cauchard, J., Doligez, P., Quitard, L., Laugier, C. and Petry, S. (2010) Viability of Rhodococcus equi and Parascaris equorum eggs second observed lower efficacy confirms resistance, whereas exposed to high temperatures. Curr. Microbiol. 60, 38-41. a mean FEC reduction above the accepted threshold Kaplan, R.M. and Nielsen, M.K. (2010) An evidence-based approach to indicates possible under-dosing or administration error in the equine parasite control: it ain’t the 60s anymore. Equine Vet. Educ. first test. It is important to consider the number of animals 22, 306-316. tested, the age distribution of the population and average Kuzmina, T.A., Kuzmin, Y.I. and Kharchenko, V.A. (2006) Field study on the pretreatment FEC to determine whether the result is likely to be survival, migration and overwintering of infective larvae of horse strongyles on pasture in central Ukraine. Vet. Parasitol. 141, 264-272. truly representative of the entire population. Higher levels of Malan, F.S. and Reinecke, R.K. 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