7
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 Roundworms and flatworms that affect donkeys can cause disease. All common helminth parasites that affect horses also infect donkeys, so animals that co-graze can act as a source of infection for either species. Of the gastrointestinal nematodes, those belonging to the cyathostomin (small strongyle) group are the most problematic in UK donkeys. Most grazing animals are exposed to these parasites and some animals will be infected all of their lives. Control is threatened by anthelmintic resistance: resistance to all 3 available anthelmintic classes has now been recorded in UK donkeys. The lungworm, Dictyocaulus arnfieldi, is also problematical, particularly when donkeys co-graze with horses. Mature horses are not permissive hosts to the full life cycle of this parasite, but develop clinical signs on infection. In contrast, donkeys are permissive hosts without displaying overt clinical signs and act as a source of infection to co-grazing horses. Donkeys are also susceptible to the fluke, Fasciola hepatica. This flatworm can be transmitted, via snails and the environment, from ruminants. As with cyathostomins, anthelmintic resistance is increasing in fluke populations in the UK. A number of the anthelmintic products available for horses do not have a licence for use in donkeys, and this complicates the design of parasite control programmes. As no new equine anthelmintic classes appear to be near market, it is important that the efficacy of currently effective drugs is maintained. It is important that strategies are used that attempt to preserve anthelmintic efficacy. These strategies should be based on the concept that the proportion of worms in a population not exposed to anthelmintic at each treatment act as a source of ‘refugia’. The latter is an important factor in the rate at which resistance develops. Thus, it is imperative that parasite control programmes take into account the need to balance therapy to control helminth-associated disease with the requirement to preserve anthelmintic effectiveness. Introduction Perhaps one of the biggest challenges when managing helminths in donkeys is that of clinical assessment. Donkeys with significant helminth burdens may appear healthy and it is rare to observe the type of clinical signs (diarrhoea, weight loss, colic or poor condition) that are more common in horses. Morrow et al. (2011) determined that, of 1444 donkeys that presented at post mortem, 16% harboured helminth infections that were considered to be of a moderate to high cyathostomin or mixed species burden. The importance of parasites as a significant cause of morbidity and mortality in otherwise healthy donkeys is as yet undetermined; however, extrapolation of data from horses would suggest that management of helminths in donkeys is of general importance to their wellbeing and to that of co-grazing animals. Nematodes that commonly affect donkeys Cyathostomins In donkey populations in which all animals are administered anthelmintics on a regular basis, most harbour low burdens of parasitic nematode infections and do not exhibit overt signs of disease. As in horses and ponies, the most common parasitic nematodes are the cyathostomin species. The life cycle of these nematodes is the same as in other equids, with a period of larval encystment in the large intestinal wall playing an important role in the epidemiology and pathogenicity of infection. In some donkeys, encysted larvae build up in large numbers and can emerge synchronously to cause larval cyathostominosis. The latter is associated with one, or all, of the following: sudden onset weight loss, colic and, rarely in donkeys, diarrhoea. The case fatality rate of larval cyathostominosis in donkeys is not known, although, in this species, it would appear to be lower than observed in other equids, which, in some reports, approaches 50% (Giles et al. 1985). Encysted larvae can persist for many months and, during autumn/winter in the UK, the larvae can comprise the majority of the cyathostomin burden. This being the case, donkeys can harbour considerable levels of infection but the parasites (encysted larvae) are not detectable by routine faecal egg count (FEC) analysis. The impact of cyathostomin infections on working donkeys is unclear; some studies indicate that they have a negative effect on body condition score and are associated with the presence of anaemia (Matthee et al. 2002). Other studies show no correlation between FEC and body condition score (Getachew 2006; Burden et al. 2010). Donkeys do appear to 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 randomised blinded control study carried out in Morocco by Crane et al. (2011) showed significant increases in body condition score in those equids that received anthelmintic treatment when compared to those that were administered a placebo; however, no significant change in bodyweight was noted. Further research is needed in this area, particularly in light of the significant expenditure required to maintain the mass deworming programmes that are commonly a mainstay of charities working with equids in the developing world. Like other equids, individual donkeys vary in susceptibility to cyathostomins. Generally, in well managed populations, within a group, the majority control their level of infection relatively well. This is manifest as a negative or low FEC. Often, a few 461 © 2013 EVJ Ltd EQUINE VETERINARY EDUCATION / AE / SEPTEMBER 2013

Review Article Common helminth infections of donkeys and

  • Upload
    others

  • View
    4

  • Download
    0

Embed Size (px)

Citation preview

Page 1: Review Article Common helminth infections of donkeys and

Review Article

Common helminth infections of donkeys and their control intemperate regionsJ. 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

SummaryRoundworms and flatworms that affect donkeys can causedisease. All common helminth parasites that affect horses alsoinfect donkeys, so animals that co-graze can act as a sourceof infection for either species. Of the gastrointestinalnematodes, those belonging to the cyathostomin (smallstrongyle) group are the most problematic in UK donkeys. Mostgrazing animals are exposed to these parasites and someanimals will be infected all of their lives. Control is threatenedby anthelmintic resistance: resistance to all 3 availableanthelmintic classes has now been recorded in UK donkeys.The lungworm, Dictyocaulus arnfieldi, is also problematical,particularly when donkeys co-graze with horses. Maturehorses are not permissive hosts to the full life cycle of thisparasite, but develop clinical signs on infection. In contrast,donkeys are permissive hosts without displaying overt clinicalsigns and act as a source of infection to co-grazing horses.Donkeys are also susceptible to the fluke, Fasciola hepatica.This flatworm can be transmitted, via snails and theenvironment, from ruminants. As with cyathostomins,anthelmintic resistance is increasing in fluke populations in theUK. A number of the anthelmintic products available for horsesdo not have a licence for use in donkeys, and this complicatesthe design of parasite control programmes. As no new equineanthelmintic classes appear to be near market, it is importantthat the efficacy of currently effective drugs is maintained. It isimportant that strategies are used that attempt to preserveanthelmintic efficacy. These strategies should be based on theconcept that the proportion of worms in a population notexposed to anthelmintic at each treatment act as a source of‘refugia’. The latter is an important factor in the rate at whichresistance develops. Thus, it is imperative that parasite controlprogrammes take into account the need to balance therapyto control helminth-associated disease with the requirement topreserve anthelmintic effectiveness.

IntroductionPerhaps one of the biggest challenges when managinghelminths in donkeys is that of clinical assessment. Donkeyswith significant helminth burdens may appear healthy and it israre to observe the type of clinical signs (diarrhoea, weightloss, colic or poor condition) that are more common in horses.Morrow et al. (2011) determined that, of 1444 donkeys thatpresented at post mortem, 16% harboured helminth infectionsthat were considered to be of a moderate to highcyathostomin or mixed species burden. The importance ofparasites as a significant cause of morbidity and mortality inotherwise healthy donkeys is as yet undetermined; however,extrapolation of data from horses would suggest that

management of helminths in donkeys is of general importanceto their wellbeing and to that of co-grazing animals.

Nematodes that commonly affect donkeys

CyathostominsIn donkey populations in which all animals are administeredanthelmintics on a regular basis, most harbour low burdens ofparasitic nematode infections and do not exhibit overt signs ofdisease. As in horses and ponies, the most common parasiticnematodes are the cyathostomin species. The life cycle ofthese nematodes is the same as in other equids, with a periodof larval encystment in the large intestinal wall playing animportant role in the epidemiology and pathogenicity ofinfection. In some donkeys, encysted larvae build up in largenumbers and can emerge synchronously to cause larvalcyathostominosis. The latter is associated with one, or all, of thefollowing: sudden onset weight loss, colic and, rarely indonkeys, diarrhoea. The case fatality rate of larvalcyathostominosis in donkeys is not known, although, in thisspecies, it would appear to be lower than observed in otherequids, which, in some reports, approaches 50% (Giles et al.1985). Encysted larvae can persist for many months and,during autumn/winter in the UK, the larvae can comprise themajority of the cyathostomin burden. This being the case,donkeys can harbour considerable levels of infection but theparasites (encysted larvae) are not detectable by routinefaecal egg count (FEC) analysis.

The impact of cyathostomin infections on working donkeysis unclear; some studies indicate that they have a negativeeffect on body condition score and are associated with thepresence of anaemia (Matthee et al. 2002). Other studiesshow no correlation between FEC and body condition score(Getachew 2006; Burden et al. 2010). Donkeys do appear toremain ‘healthy’ when high levels of cyathostomin infectionare present, as long as they are not nutritionally compromisedor overworked (Getachew 2006; Burden et al. 2010). A recentrandomised blinded control study carried out in Morocco byCrane et al. (2011) showed significant increases in bodycondition score in those equids that received anthelmintictreatment when compared to those that were administered aplacebo; however, no significant change in bodyweight wasnoted. Further research is needed in this area, particularly inlight of the significant expenditure required to maintain themass deworming programmes that are commonly a mainstayof charities working with equids in the developing world.

Like other equids, individual donkeys vary in susceptibility tocyathostomins. Generally, in well managed populations, withina group, the majority control their level of infection relativelywell. This is manifest as a negative or low FEC. Often, a few

461

© 2013 EVJ Ltd

EQUINE VETERINARY EDUCATION / AE / SEPTEMBER 2013

Page 2: Review Article Common helminth infections of donkeys and

animals will harbour high levels of infection and will excretemoderate to high numbers of eggs into the environment. It isthese individual donkeys that act as the main source ofpasture contamination with infective cyathostomin larvae andit is thought, but not proven, that each donkey’s relativesusceptibility to cyathostomin infection is maintained throughlife. Cyathostomin infections tend to be higher in youngerdonkeys, especially those grazed on permanent pastures;however, mature donkeys can harbour substantial infectionsand therefore contribute to pasture contamination or developdisease. An exemplar dataset derived from 2 populations ofdonkeys based on 2 farms at the UK Donkey Sanctuary(Devon) with mixed age populations is shown in Figure 1. Thisdemonstrates that young (age <3 years) and old (age>26 years) donkeys may not always be the highest strongyleegg shedders and, in fact, in both instances, mature donkeyscan contribute substantially to pasture contamination. Clearly,the role of mature donkeys as contributors to contaminationshould be assessed carefully when managing foals,immunocompromised animals or mixed equine herds.

Large strongylesDonkeys are susceptible to large strongyle (Strongylus) species.Like cyathostomins, adult worms are found in the largeintestine, but the parasitic larval stages are migratory with timefrom infection to detection of eggs in faeces in the region of6–12 months. Apart from this, the life cycle and epidemiologyare similar to cyathostomins and currently control strategies forthese parasitic nematodes are handled as one. Thepathogenicity of large strongyles is related to the migratorypattern of the larvae and tissue feeding habit of the adults. Theavailability of macrocyclic lactones (ML), ivermectin and,later, moxidectin, led to substantial reductions in theprevalence of large strongyle infections in managed equinepopulations as these anthelmintics are highly effective againstthe pathogenic larval stages. No reports of anthelminticresistance have been reported in these species. Largestrongyle infections remain a real threat to working donkeysand mules in developing regions where administration of MLanthelmintics is erratic or absent (Getachew et al. 2010a); forexample, Strongylus spp. were identified in over 90% of pooled

faecal samples obtained from donkeys tested in Ethiopia andin 100% of donkeys that were examined post mortem.

Parascaris equorumHorses and ponies acquire immunity to this small intestinalnematode relatively quickly with age and exposure: patentinfections (as detected by the observation of round,thick-shelled eggs in faeces) are usually only seen inhorse/pony foals. In donkeys, however, mature animalsharbour patent infections (Getachew et al. 2010b). Hence,otherwise healthy, mature donkeys may be important sourcesof pasture contamination and, when compromised throughoverwork, ill health or poor nutrition, may be at risk of disease.The life cycle of P. equorum is migratory and infection is in theform of an environmentally resistant egg containing a secondstage larva. Time from infection to detection of eggs in faecesis approximately 10 weeks. The parasite is relatively common,especially on large operations where animals grazepermanent pastures and can cause clinical problems wheninfection intensity is high. Because the migratory pattern ishepato-tracheal, respiratory signs are observed in animalsunder high levels of challenge. Other signs include failure tothrive, whole adult worms in faeces and, in cases whereinfection intensity is high, direct effects on the intestine. Thelatter effect is rare but holds a poor prognosis. There havebeen a number of reports of treatment failure of anthelmintics(primarily, ivermectin) against P. equorum in horse foals(von Samson-Himmelstjerna 2012) and the authors haveexperienced treatment failure against P. equorum withivermectin, moxidectin and pyrantel embonate when used indonkeys. Therefore, anthelmintic resistance in this nematodespecies should be considered when designing controlprogrammes.

Oxyuris equiOxyuris equi (pinworm) is relatively common in horses andponies, but not as common as the cyathostomins (Bucknellet al. 1995; Upjohn et al. 2010). Oxyuris equi are primarilyconsidered a nuisance or irritant, but in some animalspersistent infection can lead to damage around the perineumand tail head. The nematodes are found in the terminalportion of the large intestine. Female worms are found inhigher numbers than males and when gravid, pass out of therectum to lay eggs, which stick to the skin. These are observedas yellow, crusty masses and eggs containing L3 becomeinfective in 4–5 days. Time from infection to the release of eggsis in the region of 5 months. Adult pinworms cause perinealirritation in horses leading to rubbing with broken hairs andbare patches on the perineum and tail head. Donkeys do not,however, appear to demonstrate this behaviour as frequently(F.A. Burden, unpublished observations). Identification ofinfection in donkeys is often by the observation of adult wormspassed in faeces. Faecal examination may not revealinfection and samples should be collected from around theperineal region. Anthelmintics that have demonstratedefficacy against larval and adult O. equi in horses includeivermectin, moxidectin and fenbendazole, although not allbrands have a licence for this activity. Pyrantel hasdemonstrated efficacy against adult stages only. Nopublished studies are available describing efficacy of theseproducts against O. equi in donkeys. Recently, there havebeen a number of unpublished reports of reduced

500

400

300

200

100

450

350

250

Ave

rag

e F

EC o

ver 1

2 m

on

ths

150

50

00–3 4–6 7–20

Age group (years)

Ave FEC Farm A

Ave FEC Farm B

21–25 26–35 36+

Fig 1: Graph showing average strongyle faecal egg count over a12-month period (2011) at the UK Donkey Sanctuary for residentpopulations of donkeys present on Farm A (n = 348 donkeys) orFarm B (n = 225 donkeys). These donkeys were on a targetedtreatment programme and were administered anthelmintics whentheir faecal egg count exceeded 1000 eggs/g.

© 2013 EVJ Ltd

462 EQUINE VETERINARY EDUCATION / AE / SEPTEMBER 2013

Page 3: Review Article Common helminth infections of donkeys and

anthelmintic efficacy against O. equi in horses (Reinemeyer2012) and the authors have experienced a lack of response totreatment with both ivermectin and pyrantel in donkeys. It isimportant that good hygiene is practiced to reduce the levelsof infective eggs in the environment. Thorough cleaning with astrong disinfectant after removal of all bedding will reduce therisk of infection from the environment. Although there are nopublished studies detailing efficacy of disinfectants againstO. equi eggs, extrapolation from studies on human pinwormswould indicate that better levels of personal hygiene lead to alower the risk of infection to individuals (Mazhilene 1991; Wanget al. 2010).

Dictyocaulus arnfieldiThis is relatively common in donkeys, which, in contrast tomature horses, are permissive of the entire life cycle. However,the availability of MLs has reduced the number of donkeysinfected with D. arnfieldi: in a recent study, only 4% of animalsentering the UK Donkey Sanctuary for the first time were positiveon coprological examination (F.A. Burden, unpublished data).Adult worms are found in the respiratory passages and eggsare coughed up and swallowed and passed out in the faeces.Note that this is different to lungworms of other host species inwhich first stage larvae (L1) are usually detected in faecalsamples. D. arnfieldi eggs hatch quickly, so diagnostic analysisshould include examination for eggs by standard FECmethods, particularly if samples are fresh and have beenstored anaerobically, as well as by Baermanisation (Rode andJørgensen 1989) for L1. Donkeys do not often exhibit clinicalsigns of infection, yet may excrete large numbers of eggs intheir faeces. Donkeys most at risk of developing disease relatedto high infection intensity are those that are geriatric and/orimmunocompromised. The administration of corticosteroids orpars pituitary intermedia dysfunction appear to be correlatedwith higher lungworm burdens (F.A. Burden, unpublished data)and the screening of such donkeys for D. arnfieldi infection isrecommended. Co-grazing horses are more likely to developclinical signs (for example, coughing), so care must be takento control for lungworms in resident donkeys. Mules appearto be able to support the full life cycle (Solomon et al.2012), although less commonly than observed in donkeys,and, so, may be more susceptible to disease. Most broadspectrum anthelmintics have a label claim for lungworm indonkeys (please refer to http://www.noahcompendium.co.uk/Compendium/Overview).

Common cestodes that affect donkeys

Anoplocephala perfoliataThis parasite has an indirect life cycle involving an oribatidmite. Information on this parasite in donkeys is scant. APubmed search of publicly available databases reveals thatfew papers detail the prevalence of ‘cestode infections’ indonkeys. In one, ‘cestodes’, including A. perfoliata (thecommonest tapeworm found in horses in the UK), wereidentified in 8% of working donkeys examined in Ethiopia(Getachew et al. 2010a) and, in another in Burkina Faso(Vercruysse et al. 1986), the presence of Anoplocephalamagna was reported in varying numbers. Proudman and Ellis(1995) identified infection rates of A. perfoliata of 27% bycoprology and 40% by antigen specific antibody ELISA in agroup of donkeys studied in the Welsh borders. Serology alsoindicated a 34% infection rate in donkeys in Ethiopia

(Getachew et al. 2012). A low prevalence (~3%) of infectionhas been identified by coprology in donkeys entering theUK Donkey Sanctuary (F.A. Burden, unpublished data). In thiscase, most tapeworm egg-positive donkeys originated fromIreland or Wales.

In horses, a number of studies have described the effectsof A. perfoliata at the attachment site, the ileo-caecaljunction (Proudman and Trees 1999); however, nothing isreported about the clinical effect on donkeys. A post mortemsurvey (n = 1617) at the UK Donkey Sanctuary indicated <0.5%prevalence of tapeworm infection, with only one tapeworm-associated clinical case reported over a 5-year period (F.A.Burden, unpublished data). A. perfoliata infection is thought tooccur all year round; however, recent studies in horses inGermany indicated a peak in late summer/autumn (Roelfstraet al. 2006). Specific treatment with a product with licensedefficacy against A. perfoliata is recommended at this time ofyear. Praziquantel is not licensed for use in donkeys in the UK.

Common trematodes that affect donkeys

Fasciola hepaticaFasciola hepatica affects mainly cattle and sheep, but caninfect all grazing animals. It is common in the wetter, westernareas of UK and in Ireland, but infection is spreadinggeographically, probably associated with changes in climateand the difficulty of controlling this parasite due to increasingresistance to the commonly used anthelmintic,triclabendazole (Fairweather 2011). The adult fluke is found inthe bile ducts and overt clinical signs are not usually observedin infected donkeys; however, thickened bile ducts and raisedlevels of liver enzymes in serum may occasionally be noted inheavily infected animals (Collins 1961). Little is known of theoverall prevalence of F. hepatica in donkeys in the UK: arecent coprological survey (n = 735) of new relinquishments tothe UK Donkey Sanctuary indicated an infection prevalenceof 4%, the majority of positive animals originating from Walesand Ireland (F.A. Burden, unpublished data). Another study atthe UK Donkey Sanctuary indicated that, of 60 post mortemexaminations performed on donkeys transferred from Ireland,F. hepatica was identified in 17% of livers examined and, of 200faecal samples assessed, 8.5% were positive for F. hepaticaeggs (Trawford and Tremlett 1996). In the latter study, it wasnoted that there was little reaction to the flukes in the liver. Arecent study in working donkeys in Ethiopia indicated thatFasciola spp. (F. hepatica and F. gigantica) were common indonkeys of all ages: prevalence rates identified at postmortem (n = 112) and coprologically (n = 803) were in theregion of 40–45% (Getachew et al. 2010b). In this study,infection intensity was significantly higher in donkeys that wereaged 8 years or older. For these reasons, where Fasciolaspecies are known to be present in other hosts, controlprogrammes must address the exclusion of snail habitats (byfencing or drainage), which will help break the life cycle. Noproducts are licensed specifically for use against flukes indonkeys: in the UK, triclabendazole and other flukicides canbe used under the ‘Cascade’ (http://www.noah.co.uk/issues/briefingdoc/24-cascade.htm). The latter is a legal flexibilitythat allows a rational balance between the legislativerequirement for veterinary surgeons to prescribe and useauthorised medicines where available and the need forprofessional freedom to prescribe other products where theyare not and is intended to increase the choice of medicines

© 2013 EVJ Ltd

463EQUINE VETERINARY EDUCATION / AE / SEPTEMBER 2013

Page 4: Review Article Common helminth infections of donkeys and

available for specific conditions. Please note that a risk oftriclabendazole resistance must be taken into account. Wheretriclabendazole is not effective, closantel may be considered;however, due to this chemical only being effective againstadult stage fluke, repeat dosing is necessary.

Anthelmintic use in donkeysFew products have specific label indications for donkeys andmedicines are often administered based on dose ratesoptimised for use in horses. Donkeys are adapted to living inarid areas and thrive on poor quality fodder and, because ofphysiological differences associated with these adaptations,donkeys differ from horses and ponies in how they distribute,metabolise and excrete xenobiotics. This has implications forwater compartment partitioning which affects drugdistribution (Grosenbaugh et al. 2011). All 3 modernanthelmintic classes (Table 1) available for administration tohorses have been shown to be effective in donkeys whenadministered at doses determined for the former (Malan andReinecke 1979; Taylor and Craig 1993; Crane et al. 2011);however, a number of products are not licensed for use indonkeys and care must be taken to acknowledge theappropriate label claim for each active ingredient or brand.Early studies with moxidectin indicated shorter strongyle eggreappearance periods in donkeys than was observed at thetime in horses (Matthee et al. 2002). Indeed, the first report ofmoxidectin resistance in cyathostomins was observed indonkeys (Trawford et al. 2005). This anthelmintic is not licensedfor donkeys and this presents difficulties for cyathostomincontrol when treatments for encysted larvae are required. Inthe UK, only a 5-day course of fenbendazole has licensedefficacy against cyathostomin encysted larvae, but there iswidespread resistance in these nematodes to this anthelmintictype.

Helminth control in donkeysDonkeys have different nutritional requirements and naturalbehaviour compared to other equids. When donkeys are keptin temperate climates, they can become obese if allowed freegrazing access. Thus, grazing is often restricted for much of theyear, with donkeys commonly grazed at 0.1–0.2 ha/animal.Such stocking densities mean that larval contamination canbecome high on land that is not effectively managed.Although donkeys are selective grazers that will not, by choice,graze areas soiled by dung, when enclosed on small areas,they graze close to or inside dunging areas, with resultant

exposure to high levels of parasite challenge. To restrictgrazing, they are often enclosed using electric fencing toencourage strip grazing; although of benefit to weight control,this can lead to abnormal dunging behaviour, with lack ofestablishment of natural latrine areas away from grazing andso parasite challenge may be high. In these cases, goodpasture hygiene is paramount; dung should be lifted at leasttwice per week and consideration should be given to methodsof pasture restriction that enable animals to establish latrineareas. Studies at the UK Donkey Sanctuary have shownsubstantially reduced strongyle FEC in donkeys grazingpastures where dung was lifted mechanically or manuallytwice a week compared to pastures with no dung removal atall (Fig 2). Management of manure is important; it should becomposted with temperatures reaching a minimum of50–70°C maintained for over 8 h (Hébert et al. 2010).Generally, compost heaps require turning and maintenanceat these levels for a minimum of 3 weeks to ensure destructionof helminth eggs throughout the heap. If possible, alternativemeans of disposal should be sought or manure heaps sited sothat they are not accessible and run-off will not contaminategrazing land.

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

Anthelmintic class Active ingredient Indication Dose rate

Macrocyclic lactones IvermectinMoxidectin*

GI nematodes, Dictyocaulus arnfieldiAs above + encysted cyathostomin larvae

0.2 mg/kg bwt per os0.4 mg/kg bwt per os

Benzimidazoles Fenbendazole†

Triclabendazole*GI nematodes,D. arnfieldiImmature and mature Fasciola hepatica

7.5 mg/kg bwt per os or 7.5 mg/kg bwtper os for 5 days for cyathostominencysted larvae

18 mg/kg bwtTetrahydropyrimidines Pyrantel embonate Gastrointestinal nematodes

Anoplocephala perfoliatia19 mg/kg bwt38 mg/kg bwt

Pyrozinoisoquinolines Praziquantel* A. perfoliatia and other tapeworms 2.5 mg/kg bwtSalicylanilides 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.

1000

500

May JuneAutomatedManualNo Removal

July AugustSeptember October

Me

an

FW

EC

Fig 2: The average number of strongyle eggs/g/group calculatedin 3 groups of donkeys grazing land with different pasturemanagement protocols over a grazing season. Automated (blueline) or manual (pink line) collections of faeces were carried outtwice per week throughout the grazing season for 2 of the groups.For the remaining group (green), faeces were not lifted frompasture. Data courtesy of Dr M.L. Denwood and Professor S. Love,University of Glasgow, 2011. FWEC, faecal worm egg count.

© 2013 EVJ Ltd

464 EQUINE VETERINARY EDUCATION / AE / SEPTEMBER 2013

Page 5: Review Article Common helminth infections of donkeys and

Grazing with livestock other than equids is to beencouraged; sheep and cattle may act as biological vacuumcleaners, with few parasite species being shared between thedifferent host types. In areas with high fluke prevalence andwhere the environment may support snails, fluke infectionstatus of sheep should be assessed before allowing them tograze donkey pasture. It is not advisable to graze sheep withdonkeys that are unaccustomed to them, as donkeys mayexhibit aggressive behaviour towards unknown livestock(Burden and Trawford 2006); sheep are best employed tograze after donkeys before a period of pasture rest. Ideally,grazing should be allowed at least 6 months to reduce parasitepopulations (Kuzmina et al. 2006).

Individual donkeys differ in susceptibility to strongyleinfections; this is likely to result in over-dispersed patterns offaecal egg excretion, which, at the appropriate time of year,provides an opportunity for control via targeted therapy(Sangster 2003). In horses and ponies, ‘high egg shedders’generally maintain higher lifelong FEC patterns, despite similarexposure levels (Becher et al. 2010). Temporal data indicatingsuch patterns in donkeys are lacking. As indicated above, theclear effect of age on strongyle egg output, in part explainedby the acquisition of immunity in horses (von Samson-Himmelstjerna et al. 2009), does not appear to be as clear cutin donkeys. Despite recommendations being described fortargeted therapy in equids over 20 years ago (Duncan andLove 1991), there has been relatively poor implementationof this strategy in the field. The principal objective is todecrease selection pressure for anthelmintic resistance, whilstmaintaining health by reducing infection intensity (Stratfordet al. 2011). Variation in environmental conditions, pasturemanagement and herd dynamics mean that no one protocolcan be applied uniformly; an understanding of the targethelminth species, appropriate diagnostic tests (and theirlimitations), along with a knowledge of anthelmintic sensitivityprovide the concepts on which to base best practice control.When low faecal egg shedders are left untreated, helmintheggs in their faeces are thought to provide ‘refugia’, whichserve to dilute eggs laid by worms that have survived inanthelmintic treated animals. As parasite refugium isconsidered to be the most influential factor in thedevelopment of anthelmintic resistance and the rate at whichit increases (van Wyk 2001), repeated, simultaneoustreatments of all animals, irrespective of FEC, are notrecommended.

Faecal egg count should be used regularly to targethelminth adulticidal treatments and can be performed‘in-house’ as they require little specialised equipment orparticularly advanced skills. Alternatively, a number oflaboratories offer a commercial FEC service. The McMaster (ormodified McMaster) test, based on a flotation/dilutionprinciple, is the most commonly used technique. Acentrifugal-flotation technique is more sensitive, particularly atlow egg numbers (Bello and Allen 2009). Faecal samplesshould be collected as fresh as possible and placed intosealable bags, excluding as much air as possible to reduceegg development. Samples collected in this way can berefrigerated in airtight containers for up to 120 h without asignificant change in nematode egg numbers (Nielsen et al.2010). FEC do not provide a gauge of total nematodeburdens; especially during autumn and winter in the UK whencyathostomin encysted larval levels can be high. For thisreason, FEC are of most use in targeted therapy strategies

during the grazing season when they can be used to identifythe relative contribution that individuals make to pasturecontamination (Matthews 2010). All co-grazers should betested simultaneously after the effective refractory period ofthe previously administered anthelmintic has elapsed.Individuals with a FEC in excess of a set threshold should betreated with a licensed anthelmintic, (ideally, shown previouslyto be effective), at a dose rate of 100–110% bodyweightestimated by weight tape or scale. The most frequently citedFEC cut-off for determining treatment is 200–500 eggs/g(Matthews 2008). Subsequently, FEC may be performed at 2–3monthly intervals depending on the product used. Since FECdo not detect cyathostomin encysted larvae, larvicidaltreatments can be administered when considered mostappropriate (for example, late autumn or winter in the UK).

A total reduction in administration of some anthelminticclasses (for example MLs) could potentially lead to theincreased prevalence of parasite species or stages (forexample Strongylus spp. or P. equorum). Following a decadeof targeted treatment application in Denmark, it was initiallynoted that the prevalence of S. vulgaris had remained similarto that observed in Sweden, where such treatment regimeshad not been instituted to the same degree (Nielsen 2009). Ina further Danish study in which larval culture analysis wasperformed to identify strongylid nematodes in faecal samplesfrom farms that instituted targeted treatments based on FECanalysis compared to those that treated without using FEC,S. vulgaris prevalence was significantly higher where targetedtherapy had been applied (Nielsen et al. 2012). Donkeys newlyrelinquished and resident at the UK Donkey Sanctuary havebeen rarely found to harbour large strongyles (<0.1% ofdonkeys at post mortem over a 5-year period; F.A. Burden,unpublished data). However, further research is requiredand baseline prevalence data are essential to assess theimpact of changes in parasite management regimes overtime.

In terms of quarantine, the UK Donkey Sanctuary screens allrelinquishments for strongyles, P. equorum (regardless of age),liver fluke and lungworm coprologically. Coprologicalassessment is also carried out for tapeworm. Althoughsensitivity is low (Meana et al. 1998), unless there is a specificconcern, tapeworm serology is not carried out asthe available ELISA (Diagnosteq, http://www.liv.ac.uk/diagnosteq/) has not been validated for donkey serum IgG(T).Donkeys or mules whose test results indicate a patent infectionwith P. equorum, liver fluke, lungworm or tapeworm aretreated appropriately and follow-up FEC are analysed 14–21days post treatment to gauge efficacy of treatment. Donkeyswith positive strongyle FEC may be treated above 300 eggs/gdependent upon the clinical picture. If there is concern that anewly acquired donkey or mule entering a group harbourslungworm or P. equorum that may not have reached patency,ivermectin is administered immediately and the animalquarantined from grazing for 48 h.

Assessing anthelmintic efficacyAnthelmintic resistance may be suspected following a FECreduction test, a reduction in the expected effectiverefractory period after anthelmintic treatment, or by clinicalsigns of disease where appropriate dosing is thought to haveoccurred. The FEC reduction test compares FEC before (Day 0)and 10–14 days after anthelmintic treatment. It is simple to

© 2013 EVJ Ltd

465EQUINE VETERINARY EDUCATION / AE / SEPTEMBER 2013

Page 6: Review Article Common helminth infections of donkeys and

perform, can be applied to all classes of anthelmintic and isthe most widely used screening test for resistance. Efficacy iscalculated using the formula:

Reduction

Day mean FEC day post treatment mean FE

(%)

(

= −0

14 CCDay FEC

)×1000

Accuracy can be affected by inherent variability in FEC withinand between donkeys, and it can be difficult to interpret dataderived from populations where there are large proportions ofanimals that have low or zero FEC (Matthews 2011). Pre- andposttreatment samples should be handled and processedsimilarly. Performing the test on a large proportion of thepopulation will provide the most accurate representation ofsensitivity. Different FEC reduction percentage cut-offs arerecommended for different classes of anthelmintic; recentrecommendations state these as 90% for BZs andtetrahydropyrimidines and 95% for MLs (Kaplan and Nielsen2010). These threshold percentages take into accountvariation in efficacy when the anthelmintics were initiallytested for licensing. A population mean FEC reduction abovethese cut-offs represents acceptable efficacy, whilst a lowermean FEC reduction is indicative of resistance. Ideally, in casesof suspected resistance, the test should be repeated: asecond observed lower efficacy confirms resistance, whereasa mean FEC reduction above the accepted thresholdindicates possible under-dosing or administration error in thefirst test. It is important to consider the number of animalstested, the age distribution of the population and averagepretreatment FEC to determine whether the result is likely to betruly representative of the entire population. Higher levels ofsensitivity (i.e. tests with detection limits of <50 eggs/g) will moreaccurately determine anthelmintic sensitivity, especially whenthere are a high proportion of low FEC in the test population. Itis important to investigate all suspected cases of resistance. Inthe UK, confirmed anthelmintic resistance should be reportedto the Veterinary Medicines Directorate as a ‘SuspectedAdverse Reaction’ (http://www.vmd.defra.gov.uk/adversereactionreporting/).

Authors’ declaration of interestsNo conflicts of interest have been declared.

ReferencesBecher, 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 strongyleegg shedding consistency. Vet. Parasitol. 171, 116-122.

Bello, T.R. and Allen, T.M. (2009) Comparison of two fecal egg recoverytechniques and larval culture for cyathostomins in horses. Am. J. Vet.Res. 70, 571-573.

Bucknell, D.G., Gasser, R.B. and Beveridge, I. (1995) The prevalence andepidemiology of gastrointestinal parasites of horses in Victoria,Australia. Int. J. Parasitol. 25, 711-724.

Burden, F. and Trawford, A. (2006) Equine interspecies aggression. Vet.Rec. 159, 859-860.

Burden, F.A., Du Toit, N., Hernandez-Gil, M., Prado-Ortiz, O. and Trawford,A.F. (2010) Selected health and management issues facing workingdonkeys presented for veterinary treatment in rural Mexico: somepossible risk factors and potential intervention strategies. Trop. Anim.Health Prod. 42, 597-605.

Collins, D.R. (1961) Fascioliasis in a Mexican burro. J. Am. Vet. Med. Ass.139, 1321-1323.

Crane, M.A., Khallaayoune, K., Scantlebury, C. and Christley, R.M.(2011) A randomized triple blind trial to assess the effect of ananthelmintic programme for working equids in Morocco. BMC Vet.Res. 7, 1.

Duncan, J.L. and Love, S. (1991) Preliminary observations on analternative strategy for the control of horse strongyles. Equine Vet. J.23, 226-228.

Fairweather, I. (2011) Reducing the future threat from (liver) fluke:realistic prospect or quixotic fantasy? Vet. Parasitol. 180, 133-143.

Getachew, M. (2006) Endoparasites of working donkeys in Ethiopia:epidemiological study and mathematical modelling. PhD thesis,University of Glasgow.

Getachew, M., Trawford, A., Feseha, G. and Reid, S.W. (2010a)Gastrointestinal parasites of working donkeys of Ethiopia. Trop. Anim.Health Prod. 42, 27-33.

Getachew, M., Innocent, G.T., Trawford, A.F., Reid, S.W. and Love, S.(2010b) Epidemiological features of fasciolosis in working donkeys inEthiopia. Vet. Parasitol. 169, 335-339.

Getachew, A.M., Innocent, G., Proudman, C.J., Trawford, A., Feseha,G., Reid, S.W., Faith, B. and Love, S. (2012) Equine cestodosis: asero-epidemiological study of Anoplocephala perfoliata infection inEthiopia. Vet. Res. Commun. 36, 93-98.

Giles, C.J., Urquhart, K.A. and Longstaffe, J.A. (1985) Larvalcyathostomiasis (immature trichonema-induced enteropathy): areport of 15 clinical cases. Equine Vet. J. 17, 196-201.

Grosenbaugh, D.A., Reinemeyer, C.R. and Figueiredo, M.D. (2011)Pharmacology and therapeutics in donkeys. Equine Vet. Educ. 23,523-531.

Hébert, L., Cauchard, J., Doligez, P., Quitard, L., Laugier, C. and Petry, S.(2010) Viability of Rhodococcus equi and Parascaris equorum eggsexposed to high temperatures. Curr. Microbiol. 60, 38-41.

Kaplan, R.M. and Nielsen, M.K. (2010) An evidence-based approach toequine parasite control: it ain’t the 60s anymore. Equine Vet. Educ.22, 306-316.

Kuzmina, T.A., Kuzmin, Y.I. and Kharchenko, V.A. (2006) Field study on thesurvival, migration and overwintering of infective larvae of horsestrongyles on pasture in central Ukraine. Vet. Parasitol. 141, 264-272.

Malan, F.S. and Reinecke, R.K. (1979) Anthelmintic efficiency offenbendazole in equines. J. S. Afr. Vet. Ass. 50, 255-258.

Matthee, S., Krecek, R.C., Milne, S.A., Boshoff, M. and Guthrie, A.J. (2002)Impact of management interventions on helminth levels, and bodyand blood measurements in working donkeys in South Africa. Vet.Parasitol. 107, 103-113.

Matthews, J.B. (2008) An update on cyathostomins: anthelminticresistance and worm control. Equine Vet. Educ. 20, 552-560.

Matthews, J.B. (2010) Clinical forum: drug resistance in cyathostomins.Companion Anim. 15, 9-17.

Matthews, J.B. (2011) Facing the threat of equine parasitic disease.Equine Vet. J. 43, 126-132.

Mazhilene, O.K. (1991) The practical aspects of the enterobiasisproblem in Lithuania. Med. Parazitol. (Mosk). 4, 31-34.

Meana, A., Luzon, M., Corchero, J. and Gómez-Bautista, M. (1998)Reliability of coprological diagnosis of Anoplocephala perfoliatainfection. Vet. Parasitol. 74, 79-83.

Morrow, L.D., Smith, K.C., Piercy, R.C., du Toit, N., Burden, F.A., Olmos, G.,Gregory, N.G. and Verheyen, K.L.P. (2011) Retrospective analysis ofpost mortem findings in 1,444 aged donkeys. J. Comp. Pathol. 144,145-156.

Nielsen, M.K. (2009) Restrictions of anthelmintic usage: perspectives andpotential consequences. Parasit. Vectors 2, Suppl. 2, S7.

Nielsen, M.K., Vidyashankar, A.N., Andersen, U.V., Delisi, K., Pilegaard, K.and Kaplan, R.M. (2010) Effects of fecal collection and storagefactors on strongylid egg counts in horses. Vet. Parasitol. 167, 55-61.

Nielsen, M.K., Vidyashankar, A.N., Olsen, S.N., Monrad, J. andThamsborg, S.M. (2012) Strongylus vulgaris associated with usage ofselective therapy on Danish horse farms – is it reemerging?Vet. Parasitol. 189, 260-266.

Proudman, C.J. and Ellis, R.N. (1995) Tapeworm infection in donkeys.Vet. Rec. 136, 475.

Proudman, C.J. and Trees, A.J. (1999) Tapeworms as a cause ofintestinal disease in horses. Parasitol. Today 15, 156-159.

© 2013 EVJ Ltd

466 EQUINE VETERINARY EDUCATION / AE / SEPTEMBER 2013

Page 7: Review Article Common helminth infections of donkeys and

Reinemeyer, C.R. (2012) Anthelmintic resistance in non-strongylidparasites of horses. Vet. Parasitol. 185, 9-15.

Rode, B. and Jørgensen, R.J. (1989) Baermannization of Dictyocaulusspp. from faeces of cattle, sheep and donkeys. Vet. Parasitol. 30,205-211.

Roelfstra, L., Betschart, B. and Pfister, K. (2006) A study on the seasonalepidemiology of Anoplocephala spp. infection in horses and theappropriate treatment using a praziquantel gel (Droncit 9% oralgel). Berl. Munch. Tierarztl. Wochenschr. 119, 312-315.

Sangster, N. (2003) A practical approach to anthelmintic resistance.Equine Vet. J. 35, 218-219.

Solomon, T., Basaznew, B., Mersha, C. and Melaku, A. (2012)Occurrence of lungworm infection in equines and their associatedrisk factors. Glob. Vet. 8, 35-38.

Stratford, C.H., McGorum, B.C., Pickles, K.J. and Matthews, J.B. (2011)An update on cyathostomins: anthelmintic resistance anddiagnostic tools. Equine Vet. J. 43, 133-139.

Taylor, T.S. and Craig, T.M. (1993) Lungworms in donkeys: evaluation ofanthelmintics under field conditions. J. Equine Vet. Sci. 13, 150-152.

Trawford, A.F., Burden, F. and Hodgkinson, J.E. (2005) Suspectedmoxidectin resistance in cyathostomes in two donkey herds at theDonkey Sanctuary, UK. In: 20th International Conference of theWorld Association for the Advancement of Veterinary Parasitology,New Zealand. pp 196.

Trawford, A.F. and Tremlett, J.G. (1996) Efficacy of triclabendazoleagainst Fasciola hepatica in the donkey (Equus asinus). Vet. Rec.139, 142-143.

Upjohn, M.M., Shipton, K., Lerotholi, T., Attwood, G. and Verheyen, K.L.(2010) Coprological prevalence and intensity of helminth infectionin working horses in Lesotho. Trop. Anim. Health Prod. 42, 1655-1661.

Van Wyk, J.A. (2001) Refugia: overlooked as perhaps the most potentfactor concerning the development of anthelmintic resistance.Onderstepoort J. Vet. Res. 68, 55-67.

Vercruysse, J., Harris, E.A., Kaboret, Y.Y., Pangui, L.J. and Gibson, D.I.(1986) Gastrointestinal helminths of donkeys in Burkina Faso. Z.Parasitenkd. 72, 821-825.

Von Samson-Himmelstjerna, G. (2012) Anthelmintic resistance in equineparasites - detection, potential clinical relevance and implicationsfor control. Vet. Parasitol. 185, 2-8.

Von Samson-Himmelstjerna, G., Traversa, D., Demeler, J., Rohn, K., Milillo,P., Schurmann, S., Lia, R., Perrucci, S., di Regalbono, A.F., Beraldo, P.,Barnes, H., Cobb, R. and Boeckh, A. (2009) Effects of worm controlpractices examined by a combined faecal egg count andquestionnaire survey on horse farms in Germany, Italy and the UK.Parasit. Vectors 2, Suppl. 2, S3.

Wang, L.C., Hwang, K.P. and Chen, E.R. (2010) Enterobius vermicularisinfection in schoolchildren: a large-scale survey 6 years after apopulation-based control. Epidemiol. Infect. 138, 28-36.

© 2013 EVJ Ltd

467EQUINE VETERINARY EDUCATION / AE / SEPTEMBER 2013

SCAN TO VISIT WEBSITE© 2013 Thorovet, L.L.C. fb.com/ThoroVetLLC @ThoroVet

The first true mobile equine veterinary software system is here.

Available now at www.thorovet.comVisit us at the AAEP Convention in Nashville at Booth 1867

www.thorovet.com | [email protected] | 877-989-VETS (8387)

Game-ChangersThe Revolution Is Here!

creo