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Common Helminth Infections of Donkeys and Their Control in Temperate Regions J 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 © 2013 EVJ Ltd 462 EQUINE VETERINARY EDUCATION / AE / SEPTEMBER 2013 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
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