Parasitology

Donkeys have different nutritional requirements and natural behaviours compared to horses and ponies. When donkeys are kept as companion animals in temperate climates they can become obese if allowed free grazing access. Grazing should therefore be restricted for much of the year, with donkeys commonly grazed at 0.1—0.2 ha/animal. Working donkeys are often kept on small areas of land in high densities to prevent roaming or to facilitate working needs.

Such stocking densities mean that larval contamination can become high on land that is not effectively managed. The donkey is a selective grazer and will not by choice graze areas soiled with dung. However, when enclosed in small areas they may graze close to or inside dunging areas, with resultant exposure to high levels of parasite challenge.

The modern anthelmintics that are available for administration to horses and ponies have been shown to be effective in donkeys, although it is important to note that resistance has been recorded to the majority of the drugs. They should be administered at doses determined for the horse and pony.

Many products are not licensed for use in donkeys and owners must be informed accordingly. The use of these drugs must be in accordance with local regulations for prescription of unlicensed medication.

ECTOPARASITES

Donkeys can be affected by the same parasites as horses and ponies and are diagnosed and treated similarly.

Pediculosis, flies, pinworm, mites, stomach bots, ticks and habronemiasis are discussed in detail in the chapter on skin.

ENDOPARASITES

Although donkeys can be infested by the same parasites as horses and ponies, it is important to note that there are some differences in parasite dynamics and in treatment regimes.

Co-grazing horses, ponies and donkeys can infect each other and this is an important consideration in the management of parasitic infestation and prevention.

Small strongyles (Cyathostomins)

As in horses and ponies, these are some of the most commonly found parasitic nematodes in donkeys globally. The donkey may not demonstrate clinical disease, particularly in populations where anthelmintics are being used.

• Small strongyles are typically less than 1.5cm in length and excrete eggs in the faeces.
• The lifecycle of the small strongyle in donkeys is the same as in horses and ponies; the eggs develop into larvae in the soil and are then ingested and invade the wall of the large intestine.
• The period of larval encystment in the large intestinal wall plays an important role in the epidemiology and pathogenicity of infection and, because they will infect all co-grazing equids, this is an important consideration for grassland management.
• In some donkeys, encysted larvae build up in large numbers and can emerge synchronously which may cause clinical or subclinical larval cyathostominosis.
• Encysted larvae can persist for many months and at certain points in the year the larvae can comprise the majority of the small strongyle burden.
• Encystment is generally at a peak during the winter months in temperate climates and during the dry season in tropical climates.
• Donkeys can harbour considerable levels of infection but the parasites (encysted larvae) are not detectable by routine faecal worm egg count (FWEC) analysis.

Donkeys do not appear to show the classical clinical signs of larval cyathostominosis and are more likely to present with weight loss, colitis and abnormally low blood proteins. It may result in colic but rarely causes diarrhoea. Mortality appears to be lower than is recorded in horses and ponies.

The impact of small strongyle 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. Other studies show no correlation between FWEC and body condition score. Many donkeys appear to remain ‘healthy’ when high levels of small strongyles are present, as long as their health is not otherwise compromised and they are not underfed or overworked.
 

Epidemiology and management is similar to that seen in horses and ponies, where individual animals vary in susceptibility to small strongyles. Generally, in well managed populations, the majority control their level of infection relatively well. This is demonstrated by a negative or low FWEC. Frequently, a few animals will harbour high levels of infection and will excrete moderate to high numbers of eggs into the environment. It is these individual donkeys that act as the main source of contamination with infective small strongyle larvae. It is thought, but not proven, that each donkey’s relative susceptibility to small strongyle infection is maintained through life.

Small strongyle infections tend to be higher in younger donkeys, especially those grazed on permanent pastures. Mature donkeys can harbour substantial infections and therefore contribute to pasture contamination or develop disease.

The role of mature donkeys as contributors to contamination should be assessed carefully when managing foals, immunocompromised animals or mixed equine herds.

Infestation can be managed by:

• using a treatment programme that includes a once yearly larvicidal treatment – for example, moxidectin
• using seasonal FWEC to identify new infections and to assist with reducing pasture contamination.

However a FWEC does not provide any information on the presence of encysted larvae, so should not be relied upon for this purpose.

The decision to treat for small strongyles (other than a once yearly treatment for encysted larvae) should be based upon a FWEC. There is no universally agreed threshold for treatment. In the majority of cases, treatment of individuals with a FWEC equal to or greater than 300epg is reasonable.

When individual animals are routinely presenting with high FWECs, it is recommended that screening for Pars Pituitary Intermedia Dysfunction (PPID) is undertaken, because there appears to be an association with high FWECs.

When choosing drugs for treatment consider:

• all classes of drug licensed for small strongyles appear to be safe in donkeys; dose according to guidelines developed for horses and ponies
• moxidectin should be reserved for targeted use against encysted larvae only
• other drugs – for example, ivermectin and pyrantel embonate – should be considered when treatment is indicated by a FWEC
• it should be noted that high levels of resistance to fenbendazole have been noted in the global equine population
• lower levels of resistance to ivermectin, moxidectin and pyrantel embonate have also been detected in donkeys parasites
• some classes – for example, moxidectin – are not licensed for use in donkeys and must only be prescribed according to the relevant local regulations.

A serum enzyme-linked immunosorbent assay (ELISA) has been developed for encysted cyathostomins (Tzelos et al, 2020) This is not currently validated for donkeys.

Large strongyles (Strongylus equinus, S. vulgaris and S. edentatus)

Donkeys are susceptible to large strongyles with a similar lifecycle to those seen in horses.

Like small strongyles, adult worms are found in the large intestine, but the parasitic larval stages are migratory. The time from infestation to detection of eggs in faeces is in the region of 6–12 months. Otherwise, the lifecycle and epidemiology are similar to small strongyles.

Large strongyle infestations remain a real threat to working donkeys and mules where administration of macrocyclic lactone anthelmintics (moxidectin and ivermectin) is erratic or absent. In a study on working donkeys in Ethiopia, Strongylus spp. were identified in over 90% of pooled faecal samples obtained from donkeys and in 100% of donkeys that were examined post-mortem (Getachew et al. 2010a).

When choosing the drugs for treatment, consider:

• once-yearly administration of moxidectin for encysted small strongyles should be sufficient to control large strongyles in most populations
• at present there is no indication of resistance to anthelmintics in the large strongyles
• in populations where administration of anthelmintics is unknown, erratic or absent, treatment should be undertaken as a precaution.
   

Roundworm (Parascaris equorum)

Horses and ponies acquire immunity to this small intestinal nematode relatively quickly with age and exposure. Patent infections (as detected by the observation of round, thick-shelled eggs in faeces) are usually only seen in horse and pony foals.

In donkeys, mature animals harbour patent infections and otherwise healthy, mature donkeys may be important sources of pasture contamination. When compromised through overwork, ill health or poor nutrition, they may be at risk of Parascaris related disease.

The life cycle of the roundworm is migratory and infection is in the form of an environmentally resistant egg containing a second stage larva. Time from infestation to detection of eggs in faeces is approximately 10 weeks. The parasite is relatively common, especially in large populations where animals graze permanent pastures, and can cause clinical problems when infection intensity is high.

Roundworm eggs are extremely tolerant of environmental challenges and are known to survive for years on pastures. Assessment and treatment of new donkeys is essential. Collection and proper composting of dung is especially important on premises known to have roundworm present.

Because the migratory pattern is hepato-tracheal, respiratory signs may be observed in donkeys under high levels of challenge. Other signs include failure to thrive, whole adult worms in faeces and, in cases where infection intensity is high, direct effects on the intestine. The latter effect is rare but carries a poor prognosis.

The Donkey Sanctuary is aware of treatment failures against P. equorum when using ivermectin, moxidectin and pyrantel embonate in donkeys. Anthelmintic resistance should therefore be considered when designing control programmes.
 

Pinworm (Oxyuris equi)

In most cases pinworm produces few or no clinical signs but persistent infestation can lead to damage around the perineum and tail head.

The lifecycle and epidemiology of the pinworm in donkeys is the same as that seen in horses and ponies, but treatment will vary.

• Anthelmintics that have demonstrated efficacy against larval and adult pinworm in horses and ponies include ivermectin, moxidectin and fenbendazole, although not all brands have a licence for this activity. Pyrantel embonate has demonstrated efficacy against adult stages only.
• Pinworm appears increasingly refractory to anthelmintic treatment and The Donkey Sanctuary has reported a lack of response to treatment with both ivermectin and pyrantel embonate in donkeys. Licensed treatments include ivermectin, moxidectin and pyrantel embonate.
• It is important that good hygiene is practiced to reduce the levels of infective eggs in the environment. Thorough cleaning with a suitable disinfectant after removal of all bedding will reduce the risk of infection from the environment.
• The Donkey Sanctuary uses pyrantel embonate at double the normal dose and pays particular attention to pasture, housing and animal hygiene. A second treatment with pyrantel embonate may be required as this drug is only licensed for adult pinworm.

Tapeworm (Anoplocephala magna and A. perfoliata)

Tapeworm does not appear to be common in donkeys in temperate climates and reports of clinical disease in donkeys associated with this parasite are rare. A study identified A. perfoliata in 8% of working donkeys examined in Ethiopia (Getachew et al. 2010a).

This parasite has an indirect lifecycle involving an oribatid mite.

Where clinicians are aware that tapeworm is common in the local equine population, or if tapeworm eggs and/or segments are seen on faecal tests, then treatment once per year is recommended.

Faecal counts are insensitive for tapeworm and should not be relied upon for diagnosis. Similarly, ELISA-based tests have not been validated in donkeys.

When choosing drugs for treatment in donkeys specific considerations are necessary.

• Treatment should be undertaken in late autumn or winter in temperate climates or as indicated in other climates.
• Products specifically licensed for tapeworm should be used. Pyrantel embonate should be given at an increased dose (‘double dose’).
• Praziquantel is not licensed for use in donkeys. It should be used where appropriate and according to relevant local regulations when pyrantel embonate is not available.
• No data is available for the use of combination de-wormers in donkeys. For example, ivermectin + praziquantel or moxidectin + praziquantel. The Donkey Sanctuary does not recommend their use.
   

Threadworm (Strongyloides westeri)

The lifecycle and epidemiology of the threadworm in donkeys is the same as in horses and ponies.

Lungworm (Dictyocaulus arnfieldi)

Mature horses are not permissive hosts to the full lifecycle of this parasite, but develop clinical signs on infection. In contrast, the donkey is permissive of the entire lifecycle of the lungworm but rarely displays overt clinical signs, and also acts as a source of infection to co-grazing horses.

Adult worms are found in the respiratory passages and eggs are coughed up and swallowed and passed out in the faeces. Note that this is different to lungworms of other equine host species, in which first stage larvae (L1) are usually detected in faecal samples.

Donkeys do not often exhibit clinical signs of infection, yet may excrete large numbers of eggs in their faeces. Infection in horses can cause severe coughing.

Donkeys most at risk of developing disease are those that are geriatric or immunocompromised through disease or overwork. The administration of corticosteroids or the presence of PPID appears to be correlated with higher lungworm burdens and the screening of such donkeys for lungworm infection is recommended.

Lungworm eggs hatch quickly, so diagnostic analysis should include examination for eggs by standard FWEC methods, particularly if samples are fresh and have been stored anaerobically, as well as by the Baermann technique for L1.

The control of lungworm in donkeys is particularly beneficial for co-grazing equines. It is essential to maintain a ‘zero tolerance’ approach to this parasite because once established on pasture it is extremely difficult to eradicate due to the ability of L3 to overwinter.

When choosing drugs for treatment specific considerations are necessary.

• Lungworm can be successfully treated with macrocyclic lactones.
• There is currently no indication of resistance to anthelmintics.
• A de-worming schedule that includes a once yearly larvicidal macrocyclic lactones treatment should control lungworm in closed populations.
• Newly introduced donkeys or mules should always be treated with an macrocyclic lactones and restricted from grazing for 48 hours.
   

Liver fluke (Fasciola hepatica)

Liver fluke affects mainly cattle and sheep, but can infect many mammalian species. Donkeys appear to be susceptible to liver fluke and this parasite is an increasing problem in donkeys globally. The prevalence of liver fluke infection (diagnosed by coprology) in newly admitted donkeys to The Donkey Sanctuary, UK, between 2011-2013 was 10.2%. Donkeys grazing wet, marshy paddocks are susceptible because fluke requires the water snail Lymnaea spp. to act as an intermediate host. Donkeys may be at particular risk if co-grazing with other infected livestock.

The adult fluke is found in the bile ducts and overt clinical signs are not usually observed in infected donkeys. Thickened bile ducts and raised levels of liver enzymes in serum may occasionally be noted in heavily infected animals.

Donkeys should have a faecal sample assessed using a sedimentation technique if fluke infestation is known to be a risk.

Where liver fluke are known to be present in other hosts, control programmes must address the exclusion of snail habitats (by fencing or drainage), which will help break the lifecycle.
 

There are no flukicidal products licensed for use in donkeys so treatment must be prescribed according to relevant local regulations.

• Triclabendazole has been used extensively by The Donkey Sanctuary at an increased dose rate of 18mg/kg bwt.
• There are numerous reports of lack of efficacy of triclabendazole and this has been observed in donkey infestations. To ensure treatment has been successful, a faecal sample should be analysed 14—28 days post treatment.
• Where triclabendazole is known to be ineffective, closantel (20mg/kg bwt) may be considered. It should be noted that this product is only effective against adult fluke so re-dosing is required 8—10 weeks later. Signs of closantel overdose are rare and include blindness, anorexia and ataxia. These signs have not been observed by The Donkey Sanctuary.

TREATMENT

Early studies indicate that the reappearance period for strongyle eggs are shorter in donkeys than in horses and ponies.

Moxidectin resistance in equine small strongyles has been recorded in donkeys.

PREVENTION

It is imperative that preventative programmes balance parasite control with the requirement to preserve anthelmintic effectiveness.

Environmental management

Anthelmintics reduce pasture contamination and treat clinical disease but only impact on parasites within the animal. The vast majority of parasites reside in the environment, which includes buildings or fences in some cases. Control of the environmental population is essential.

• Dung removal at least twice per week has been shown to significantly decrease the number of parasite larvae present and the requirement to treat with anthelmintics. This is especially important when equids are intensively grazed.
• Manure should be properly composted before being spread on to grazing land. Manure should be composted for a minimum of six weeks with regular turning and maintenance. A minimum temperature of 50—70°C is recommended to kill helminth eggs.
• New equines should be quarantined and treated. Treatment for lungworm with an macrocyclic lactones is recommended for any new donkey or mule entering a property before it is allowed to graze.
• Co-grazing with ruminants is useful as a ‘biological hoover’. Care should be taken grazing donkeys alongside other species as they can exhibit aggressive behaviour towards unknown animals; unless they are carefully introduced, grazing separately is recommended.
• Disinfection of stables, fencing and fomites is advisable where Parascaris or Oxyuris are present.
• Where fluke is an issue, drainage of grazing land and fencing to restrict access to wet areas plus monitoring and treatment of other livestock is strongly recommended.