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Review ArticleRespiratory disease in the donkeyA. K. ThiemannThe Donkey Sanctuary, Sidmouth, Devon, UK.

Keywords: horse; donkey; respiratory; anatomy; physiology; pathology; equine influenza; equine herpesvirus; trachealcollapse; pulmonary fibrosis

Summary

The donkey suffers from a similar range of respiratorydiseases as the horse; however, there are a number ofsubtle variations, knowledge of which can influence thesuccess of treatment. As an animal adapted to a semi-aridterrain, there are variations in physiology, anatomy anddisease susceptibility. The nonathletic nature of the donkeymeans that delayed presentation is common with manydiseases and, while there may be enhanced resistance tosome transboundary and parasitic diseases, there may beequal or increased severity of illness to some endemicdiseases, e.g. equine influenza. Donkeys frequently live togeriatric ages and the clinician should be aware of theincreased risk of conditions such as tracheal collapse,fibrosing pneumonia and neoplasia in this age group. Aswith any condition that causes stress and inappetance,respiratory disease in the donkey may be complicatedby hyperlipaemia and good nursing care is an essentialcomponent of treatment.

Introduction

The most obvious manifestation of the difference in therespiratory system between the donkey and horse is theoften ear-shattering bray. This loud communication signalcarries across many kilometres in the natural semi-aridenvironment to which the donkey is adapted. Thedomestic donkey exhibits what is known as type II socialbehaviour (Goodwin 2007), in common with Grevy’s zebra,African and Asiatic wild asses. These species have territorialmales with females ranging over several male territories.The bray serves to keep donkeys in contact with othergroup members, advertise status and possession of a mate.When domestic donkeys are separated from a group(including their human social group) or when jennies are inheat, the bray is a potent reminder of the donkey’spresence. In contrast, the domestic horse, Prezwalski horse,

Burchell’s and Mountain zebra exhibit a harem type socialorganisation with one stallion and a small group of maresthat range over a wide area.

The bray is a clue to the difference in anatomy,function and disease susceptibility with respect torespiratory disease in the donkey compared to the horse.

Anatomical considerations

For interested readers, a detailed account of anatomicaldifferences between the donkey and horse can be foundin Herman (2009) and Lindsay and Clayton (1986). Thisreview will concentrate on clinically important aspects ofthe anatomy.

Working from the external nares inwards, the firstdifference is in the positioning of the nasolacrimal ductopening. This is not to be found on the floor of the nares butin a dorsolateral position often very near the junction withthe false nostril. The opening can be hard to visualise and,in some cases, it is extremely small. This position may helpavoid obstruction of the ostia in the natural dusty andsandy environment of the wild ancestors of the domesticdonkey. In the UK this duct rarely becomes blocked but, incountries where habronemiasis is more common, parasitesmay damage the nasolacrimal duct resulting in tearoverflow and a moist nonhealing wound (Mohamed et al.1990) (Fig 1).

The nasal passages in the donkey are narrow despitethe relatively large head size and care is needed to avoidcausing bleeding when performing nasogastric intubationor endoscopy.

Various features in the nasopharyngeal area of thedonkey help with forming the resonance of the bray. Thepharyngeal airway is more constricted in the middle andmore flared both dorsally and ventrally than in the horse.The nasopharyngeal recess is a diverticulum of thepharyngeal mucosa lying between the guttural pouchopenings; in donkeys it forms a deep membranous pouch2–3 cm diameter extending 4–6 cm caudally, the mucosaof which bulges into the airway during the inspiratoryphase of braying. This deep recess can be confusing when

Corresponding author email: [email protected]

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endoscoping donkeys; in the horse the recess is shallow atabout 2.5 cm in length.

The pharyngeal openings to the guttural pouches aredescribed by some authors as lying more horizontally thanvertically; however, entering, visualising and catheterisingthe guttural pouches is accomplished as in the horse.Variable amounts of deep pigmentation in the larynx andupper oesophagus can be considered a normal variationin the donkey.

The epiglottis is shorter and more pointed in the donkey(Fig 2) and the whole laryngeal opening (aditus laryngis) istilted more caudally than in the horse. These features canmake it hard to visualise the tracheal opening through thevocal folds (rima glottidis) and can also make intubation ofdonkeys for surgery unusually difficult. The average 180 kgdonkey requires an endotracheal tube of 16 mm internaldiameter but a range of 14–18 mm may be required asthe trachea of the donkey is narrower than that of acomparably sized pony.

There are documented differences in the lateralventricles and median laryngeal recess anatomy of thedonkey but these are of little clinical relevance. There islimited information on normal tracheal wash and BALcytology in the donkey. One study with 22 donkeys foundtracheal wash cytology to have a slightly higherpercentage of neutrophils and eosinophils than the horse(Delvaux et al. 2001). Another study with 10 donkeys foundBAL values to be similar to the horse except for a highermacrophage percentage (Campi et al. 2008). Forpractical purposes, normal values may be followed fromhorse values.

Pulmonary function in donkeys

A study by Delvaux et al. (2001) measured the parametersof mechanical ventilation in the donkey. They founddonkeys compared more closely to bovines than horsesin relation to pulmonary dynamics. These authorshypothesised that the differences reflect the variation inthe nature of these species - while horses are flight animals,donkeys tend to stand and confront danger.

These differences are also reflected in the nature ofwork that donkeys are suited to, being ideal as draughtand pack animals, with limited ability to sustain speed and,as such, their contribution to the agricultural economy ofmany nations should be appreciated.

In particular, donkeys have increased respiratoryfrequency (13–31 breaths/min), increased total pulmonaryresistance and a reduced dynamic compliance,compared to horses. Clinically relevant here are the slightlyhigher resting respiratory rates of donkeys (average rate 20breaths/min, range 13–31) compared to the horse and theneed to be aware of this when monitoring anaesthetiseddonkeys, when a reduction in depth and rate of respirationmust be carefully assessed.

Disease presentation

When dealing with a donkey affected by respiratorydisease, the clinician should approach the case in a similarmanner as per the horse, while being aware of certaindifferences in presentation, management and diseaserange.

Initial clinical signs may well be subtle due to the stoicalnature of the donkey, relatively insensitive cough reflex andlack of high intensity exercise to alert the owner toa lack of performance. Despite this, the disease process maybe chronic, well advanced and complicated by otherfactors. Donkeys under stress may succumb to hyperlipaemiaand it is sensible to check appetite and triglyceride levels in adonkey with respiratory disease. Conversely, donkeys withhyperlipaemia, pancreatitis and other painful conditions mayshow tachypnoea and pyrexia.

The lung sounds in the donkey may be easier to heardue to the smaller size of the thorax but, in obeseindividuals, significant fat deposits may muffle respiratory

Fig 1: Nasolacrimal duct positioning is dorsal in the donkey.

Fig 2: Endoscopic view of donkey larynx showing typical pointedshort epiglottis.

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sounds, the use of a re-breathing bag can helpaccentuate subtle sounds.

Donkeys are often kept well into old age and geriatricrespiratory disease including pulmonary fibrosis, neoplasiaand dental related sinus empyema may be seen in thisage group.

In a recent survey of post mortem findings in 1444 ageddonkeys in the UK (Morrow et al. 2010), pulmonary fibrosiswas found in 35.2% of all the donkey deaths, making thisthe most important respiratory cause of death in this herd,followed by tracheal collapse (8.7%), guttural pouchdisease (4.9%), bronchiolar/alveolar disease (4%), nasal/paranasal sinus disease (0.8%) and malignant lungneoplasia (0.4%). In addition, the presence of eithertracheal collapse or myocardial disease increased theodds ratio of having concurrent pulmonary fibrosis by 1.5and 2.3 times, respectively. While this data reflect only onepopulation of donkeys, it is helpful in giving some idea ofthe likely problems encountered in aged donkeys.

Infectious viral respiratory disease

While donkeys are reported to have a difference insusceptibility to some ‘exotic’ diseases, this review will focuson equine influenza and herpesvirus infections in donkeys.

Equine influenza

Donkeys display similar clinical signs to horses wheninfected by equine influenza, with pyrexia, harsh coughing,nasal discharge, lymphadenopathy and depression. Thereare reports that naturally infected donkeys suffer morethan horses and, in the past, this was partly attributed tothe likelihood of donkeys harbouring high burdens ofDictyocaulus arnfieldii (Rose et al. 1970); however, inexperimental trials when seronegative donkeys wereinfected with the virus, the disease progression was moresevere than in horses and the donkeys required antibioticand anti-inflammatory therapy. Due to the risk of donkeyscontracting bronchopneumonia secondary to influenza, itis recommended that antibiotic therapy is instituted early inthe course of the disease (Holland et al. 1999). Goodnursing and monitoring the appetite in sick donkeys plays asignificant factor in aiding recovery.

Unfortunately, many donkeys are still not routinelyvaccinated against influenza and veterinarians shouldencourage better vaccine compliance among donkeyowning clients.

In 2010 during an outbreak of highly pathogenic avianinfluenza H5N1 among backyard poultry in Egypt, anumber of donkeys were found to be suffering fromrespiratory distress which was isolated as being due to theH5N1 virus. This was the first time that this virus had beenshown to jump to a member of the equidae family anddemonstrates the importance of surveillance of a number

of animal species when considering epidemic influenzaoutbreaks (Abdel-Moneim et al. 2010).

Equine/asinine herpesvirus

A range of herpesviruses have been isolated from donkeyseither in natural infections or by experimentalsteroid-induced shedding. The most important pathogensare the alpha herpesviruses that cause respiratory,neurological and reproductive pathology and the donkeyis susceptible to EHV-1 and -4, with reported cases ofrespiratory disease and abortion. In addition, the donkeyalso has a range of host adapted asinine herpesviruses(Browning et al. 1988; Gupta et al. 2000). The asinineherpesvirus-3 (AHV-3) is considered to be the progenitorof EHV-1. Asinine herpesvirus-3 is host adapted andexperimental infection into naïve donkeys produced amild transient rhinitis.

Somewhat confusingly, lesions identical to coitalexanthema are frequently identified in donkeys, bothmales and females, and can be due to EHV-3 or its asinineequivalent (though genetically distinct) AHV-1.

AHV-2 has been isolated from a clinically healthydonkey and shares most similarity to the gammaherpesviruses EHV-2 and -5 (Browning et al. 1996).

Recently 2 new gamma herpesviruses designatedAHV-4 and AHV-5 were isolated from the lungs of donkeyswith interstitial pneumonia. These viruses are most closelyrelated to zebra herpesvirus, wild ass herpesvirus and EHV-2and -5 (Kleiboeker et al. 2002). A gamma herpesvirussimilar to these has been identified in a donkey withneurological disease (Vengust et al. 2008). In conclusion,the exact virus identified in donkeys with herpesvirusinfection may be different from that in the horse but similarguidelines to diagnosis, treatment and control should beinstituted.

In clinical practice at The Donkey Sanctuary (A.Thiemann, personal observation), there have been severalserologically positive results for the alpha herpesvirusesEHV-1 and -4 from donkeys showing respiratory andneurological signs (Anon 2010). In the experience of theDonkey Sanctuary, donkeys subjected to stress, such astravelling and social mixing, are at particular risk ofrecrudescence of latent infections, which may be via asimilar mechanism to that in the horse (Edington et al. 1985;Wood et al. 1997). Clinical signs are similar to the horse withtypically a harsh cough, pyrexia and serous nasaldischarge. Older donkeys can become very depressedwhen infected and require careful monitoring.Neurological cases have been seen with rapidlydeveloping variable ataxia and paresis. Treatment ofthese cases is primarily symptomatic, relying onanti-inflammatories, antibiotics in cases with secondaryinfections, monitoring the appetite and good nursing care.

While there is a vaccine available to reduce theincidence of EHV-1 and -4 infections in horses there is nodata available on its use in the donkey.

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Diagnosis may be made by virus isolation fromnasopharyngeal swabs or whole blood. In the laboratory,virus positive samples are identified by the cytopathogeniceffect (cpe) on cell culture monolayers and then furthertested by PCR. Those which produce cpe but are negativefor EHV-1 are identified as presumptive asinineherpesvirus-3.

Serological testing by the complement fixation test(CFT) for antibody titres to EHV may be complicated byanti-complementary activity in most donkey serum. Thisactivity produces a positive result despite the absence ofvirus induced complement fixing antibody and artificiallyincreases the EHV titre measured. False positives can bedetected by running the CFT without addition of theantigen; a positive control indicates anti-complementaryactivity. In practice, seroconversion to values of 80 withoutevidence of vaccination are considered borderlinesignificant, while 160–320 are more serious evidence ofrecent exposure. A 4-fold rise in titre between samplestaken 2 weeks apart indicates recent exposure to the virus(Animal Health Trust, personal communication) and helpsto minimise the effect of complementary activity as arelative rise is what is being looked for. Virus neutralisationantibody (VN) test could be used in place of the CFT butthis test is considered unreliable due to the longpersistence of VN antibodies in serum.

In the future, specific asinine herpesvirus PCR testingmay become a possibility.

Parasitic respiratory disease

The donkey has long been considered to be a source ofinfection to horses with the parasite Dictyocaulus arnfieldiiand certainly this parasite seems well adapted to thedonkey where it can grow to maturity and cause minimalclinical signs in the host, even when present in high numbers(Fig 3). By contrast, in the horse, infection tends to beassociated with chronic coughing, dyspnoea and severe

tissue reaction which prevents the development of theadult worms. However, this is probably an oversimplification;a number of reports and studies indicate that patentinfections can exist in horses and infections can be found inhorses with no history of donkey contact (Matthews 2002).

A survey of 735 new donkey intakes to the DonkeySanctuary from across the UK between 2004–2008, showeda relatively low prevalence of infection with lungworm at4%, compared to a strongyle infection prevalence of 73%(Burden and Trawford 2009). This suggests that donkeysmay not be as much of a risk factor to co-grazing equinesas previously thought.

The lungs of donkeys infected with lungworm typicallyshow most changes in the tip of the caudal lung lobewhere areas of over inflation surround affected bronchi.The pathology in the horse is more severe with intenseimmunological reactions present. There is no evidence thatlinks lungworm infection in the donkey with pulmonaryfibrosis, although high burdens could exacerbate otherco-existing respiratory conditions.

The life cycle of the lungworm is direct with infective L3being ingested from contaminated pasture, larvaemigrate to the lungs via the lymphatics and then infiltratethe alveoli. The adult worms can grow up to 8 cm andblock the small airways, eggs produced are coughed up,swallowed and passed in the faeces. The prepatent periodis between 8–13 weeks and, in moist conditions, infective L3can remain viable for extended periods on pasture andspread can be aided by the fungus Pilobolus.

Diagnosis in the donkey relies mostly upon faecalexamination by the modified Baermann technique, using50 g of faeces per test. Samples should be examinedquickly or kept cool as temperatures of 16–20°C can causeloss of up to 50% larvae in 24 h and up to 80% after 48 h.

In the horse, definitive diagnosis may requiretranstracheal or endoscopic examination for larvaeand/or eosinophilic inflammation.

The treatment of choice is ivermectin at 200 mg/kg bwtper os. Moxidectin at 400 mg/kg bwt has been shown to beeffective in a small study; however, this is not currently licensedfor use in the donkey. Pyrantel has no licensed efficacyagainst lungworm, Benzimidazoles have poor efficacy andgenerally require higher dose rates than for treating strongyleinfection; given the level of resistance to these drugsthroughout the UK, their use is not advised. It is recommendedthat new donkeys should be coprologically tested for thepresence of lungworm and treated accordingly. Dungcollection may not be sufficient to ensure pasture removal ofparasites if infected donkeys have been present, due to theaction of Pilobolus fungi in aiding widespread larvaldistribution from the faecal matter. Larvae also showprolonged survival in cool, moist conditions.

Conditions of the upper respiratory tract

A number of conditions identical to those found in thehorse are seen in the donkey, such as false nostril

Fig 3: Patent lungworm infection, post mortem from lungs of adonkey with minimal respiratory signs.

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atheroma, progressive ethmoidal haematoma, sinusdisease, soft palate ulceration, laryngeal paralysissecondary to liver failure, guttural pouch disease andtracheal collapse/stenosis; however, literature on donkeyspecific features of these conditions is lacking. Availableinformation is presented below.

Congenital defects have been described in donkeysincluding choanal atresia and laryngeal deformity (Bartonand Ohnesorge 2009), defects of the lower lip andmandible (Farmand and Stohler 1990) and bifid tongueand mandibular cleft in mules (Bouayad et al. 2006). Theauthor has seen an adult donkey with a minor cleft of thepalate, showing some nasal return of food but otherwise ingood condition.

Sinus conditions

The paranasal sinuses are smaller in the donkey and do notextend as far rostrally as in the horse. The maxillary sinus isdivided into rostral and caudal compartments by aventrally located low bony ridge; this incomplete bonyseptum is in contrast to the horse where there is a completeoblique bony septum. Sinus disorders are similar to thehorse with sinusitis due to fungal infection, cysts orneoplasia being less common than sinusitis secondary todental disease. Typical clinical signs include unilateralnasal discharge with lymphadenopathy of the affectedside, and in cases of neoplasia there may be distortion ofthe overlying bone. Diagnosis is made through acombination of radiography and endoscopy.

Dental disease is particularly prevalent in aged donkeys(Morrow et al. 2010; du Toit and Dixon 2011) and careshould be taken when formulating radical treatment plansin these patients. Aged donkeys and those with dentaldisease were found to have an increased risk ofhyperlipaemia, a potentially life threatening complication(Burden et al. 2011).

Guttural pouch disease

Clinical observations by the author suggest that gutturalpouch disease in donkeys is not uncommon and thatendoscopic observation and treatment protocols aresimilar to those in the horse.

Empyema may be a sequel to bacterial invasion of thepouch and, at The Donkey Sanctuary, Streptococcuszooepidemicus is the most common bacterial isolate.Streptococcus equi has also been recovered but has notbeen seen following a ‘classic’ history of strangles. Theclinical signs are usually that of a mild nasal discharge thatpersists despite symptomatic therapy. Radiography andendoscopy are required for a definitive diagnosis. The puswithin the pouch may vary from semi-liquid through tochondroid formation. Neglected cases of empyema canprogress unnoticed to cause acute airway obstruction andit is advisable to investigate persistent nasal discharges inthe donkey with the same thoroughness as in the horse.

Guttural pouch empyema can be hard to treatsurgically in donkeys due to the limited surgical access;however, in extreme circumstances good results havebeen achieved. Figures 4 and 5 show donkey foals inEthiopia before and after surgical drainage of empyema.

Guttural pouch mycosis has only been described in onecase report recently in a Martina Franca donkey in Italy(Laus et al. 2010). This donkey presented with acutedyspnoea and epistaxis and was successfully managed bymedical therapy. The authors speculate that the unusualpresentation of dyspnoea could be due to the anatomicalfeatures of the donkey with relative nasopharyngealconstriction and the short aryepiglottic folds that bring theepiglottis closer to the arytenoids, combined with thetendency to partial collapse of the pharynx seen in manynormal donkeys when endoscoped (Delvaux et al. 2001);these features, together with the inflammation, may haveresulted in the excessive pharyngeal narrowing anddyspnoea, which is an uncommon presentation in cases ofguttural pouch mycosis in horses.

Fig 4: Guttural pouch swelling in a donkey foal in Ethiopia.

Fig 5: Three donkey foals after surgical treatment of guttural pouchempyema in Ethiopia.

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An anatomical study using 26 donkey cadaver headsfound differences in the carotid arterial tree both betweendonkeys and between the donkey and horse. The authorssuggest that this may play a role in the apparently lowincidence of guttural pouch mycosis in this species (Hayahet al. 2010).

Tracheal collapse

Clinical signs of tracheal disease are uncommon and, dueto the sedentary nature of donkeys, gradual stenosis maygo undiagnosed. In a post mortem survey of donkeys(Morrow et al. 2010), tracheal collapse was present in 8.7%of donkeys and there was an increased probability oftracheal collapse in cases with concurrent pulmonaryfibrosis; however, it is unclear which disorder preceded theother.

In another study of the morphology of tracheal shapein 75 predominantly aged donkeys (Powell et al. 2009),abnormalities of the tracheal rings noted includeddorsoventral flattening, dorsal ligament separation andcartilage deformity (Fig 6).

The mean number of tracheal rings in the donkey is 43(range 34–50); rings 10–30 (distal cervical and rostralthoracic) contain the most dorsoventrally flattened ringsand have the lowest cross-sectional area. This wouldexplain the finding that clinically the level of the thoracicinlet is often the site of collapse and is hard to diagnose byexternal palpation.

The condition is usually seen in older donkeys either as aresult of age related degeneration in tracheal ring/cartilage or secondary to other respiratory diseases thathave caused an increase in respiratory effort; typicallycollapse occurs in animals with chronic recurrent airwayobstruction or pulmonary fibrosis.

Clinical signs are variable depending on the severityand presence or absence of lower respiratory disease.Acute cases show distress, extreme dyspnoea andsometimes attempts at mouth breathing, harsh stertorousand honking sounds may be present. Excessive trachealnoise is heard on auscultation and, in some cases, digitalpressure on the trachea can cause severe deterioration inthe dyspnoea, strong vibrations may also be palpated.Chronic cases may present with both inspiratory andexpiratory dyspnoea and frequently a chronic cough thatresponds poorly to conventional therapy (Mair and Lane1990). Differential diagnoses should include lowerrespiratory tract disease, intra- or extra-luminal masses andpharyngeal/laryngeal paralysis. Definite diagnosis may beconfirmed by endoscopy and radiography. Standinglateral radiographs will often be sufficient to demonstratesignificant tracheal narrowing; however subtle/chroniccases may require endoscopy. Endoscopy is rarelytolerated in acutely dyspnoeic donkeys but may bevaluable for confirming the diagnosis in less obvious cases.

In an acute crisis, treatment may be attempted with i.v.steroids, atropine and diuretics to reduce mucosaloedema; however, euthanasia may be necessary.

Chronic cases may be managed by reduction ofinflammation in both upper and lower respiratory tract withthe use of systemic and inhaled anti-inflammatory steroidsand bronchodilators, and maintenance of a healthydust-free environment. There are no reports of trachealstents being used in the donkey, although the procedurehas been performed in miniature horses.

Conditions of the lower respiratory tract

Donkeys suffer from recurrent airway obstruction RAO in asimilar manner to the horse, although typically delayedpresentation may lead to a poor outcome. Managementis as for the horse with a combination of medical andenvironmental management; donkeys tolerate nebuliseddrugs well and similar dosages regimes apply.

Dyspnoea in the donkey can be caused by a numberof lower respiratory conditions as in the horse; these includepneumonia, pleural effusions or haemorrhage, pulmonaryoedema, neoplasia, hydatid cysts and diaphragmaticrupture. This review will focus on the most commoncause, idiopathic pulmonary fibrosis, and mentionshydatid disease and neoplasia where there is somedonkey-specific literature available.

Pulmonary fibrosis

Chronic interstitial fibrosing pneumonia has been found inthe lungs of donkeys at post mortem examination in the UK(Thiemann and Bell 2001) and USA (Kleiboeker et al. 2002).The lesions are described as varying from mild with focaldiscrete areas of fibrosis through to severe with wholelobules diffusely fibrosed and widespread sub-pleuralfibrosis.

Fig 6: Dorsoventrally flattened tracheal rings typical of trachealcollapse.

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Clinically the signs vary depending on how soon thecondition is detected. In mild cases tachypnoea,increased respiratory effort and variable adventitious lungsounds are present. The condition can initially be difficult todifferentiate from RAO and other causes of lower airwaydisease. The response to conventional treatment is usuallypoor due to the fibrosing nature of the condition. Inlongstanding cases there will be more marked inspiratorydyspnoea as the patient attempts to lengthen theinspiratory phase to counteract the restrictive nature of thefibrosis. It is important to note the pattern of breathingcarefully and differentiate inspiratory from expiratorydyspnoea. The latter is more indicative of RAO. There maybe episodes of pyrexia and nasal discharge which usuallycorrespond to a secondary bacterial lower airwayinfection. Auscultation at this stage typically reveals anabsence of lung sounds in many areas where fibrosis ispresent and is a poor prognostic sign; there will also bedullness on percussion of the affected lung. Ultrasoundprovides a useful diagnostic aid; pleural thickening andareas of sub-pleural fibrosis can be seen as ‘comet-tails’(Fig 7).

At present, there is minimal information on normalvalues for BAL/tracheal wash in the donkey and no studieson the likely changes secondary to pulmonary fibrosis.Endoscopy may be useful to rule out other conditionscausing dyspnoea but cannot be used to confirma diagnosis of IPF. Radiography (if available) willdemonstrate a primarily interstitial pattern and can beused to evaluate the cardiac silhouette, which may behypertrophic in cases of chronic respiratory disease. Thereis usually no pleural effusion and no value in attempting toobtain pleural fluid samples.

Due to the nonathletic nature of donkeys, acute casessometimes present with severe dyspnoea, tachypnoeaand marked respiratory effort, particularly on inspirationand stertorous noises often reflect concurrent trachealcollapse. These acutely presented severe cases have avery poor prognosis as there is so little unaffected lung left.

Treatment is palliative, aimed at reducing ongoinginflammation and maintaining clear airways, with acombination of oral or inhaled steroids, bronchodilators,antibiotics and mucolytics. A decision to subject suchcases to euthanasia is difficult as donkeys can cope wellwith reduced lung function for a number of years. The rateand depth of respiration should be assessed regularly andthe donkey’s general condition score, appetite andfrequency of concurrent infections noted. The aim is tosubject such cases to euthanasia before acute dyspnoeaoccurs and so prevent an obstructive respiratory crisis.Owners need to understand the hopeless long-termprognosis of this condition.

Typical post mortem changes are demonstrated inFigs 8 and 9. There is pleural, sub-pleural and interstitialfibrosis, which present as white lesions in these areas. Theremay be focal or diffuse lesions and affected lungs areheavy due to the lack of aeration. Pleural effusion is not a

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Fig 7: Transcutaneous ultrasound image showing characteristicpleural lesions evident as ‘comet tail’ lesions.

Fig 8: Severe lung fibrosis evident as white lesions in a post mortemlung specimen.

Fig 9: Severe pulmonary fibrosis visible as dark areas in inflatedlung of a fresh post mortem specimen.

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feature of the condition. In the examples shown here, theaffected lungs weighed twice as much (4 kg) as controllungs. Histological changes (Fig 10) include a combinationof inflammation, consolidation and fibrosis. A CT scan ofaffected lung tissue is shown (Fig 11) which clearlydemonstrated the demarcation between normal andunaffected tissue.

Kleiboeker et al. (2002) isolated asinine herpesvirus-4 and-5 from the lungs of donkeys with interstitial pneumonia andpostulated that these viruses may be the underlying cause ofthe pathology. This is notable for syncytial cell formation,lymphohistiocytic and suppurative bronchiolitis and withareas of interstitial fibrosis. At present, work is ongoing to

understand the relationship between herpes virus infectionand the fibrosing lung disease (The Donkey Sanctuary).

Williams et al. (2007) described a fibrotic lung disease inhorses associated with equine herpesvirus-5. In these horsesthe fibrosis was more nodular than diffuse. It is not knownhow herpesvirus infections drive fibrosis and, at present,there is no possibility of prevention, although in the futuremore specific antivirals may become available(Niedermaier et al. 2010).

Pulmonary hydatidosis

The donkey and horse act as intermediate hosts in the lifecycle of Echinococcus granulosum, the tapeworm ofdomestic dogs, cats and foxes. In the equid, hydatid cystsform typically in the liver and lung, containing numerousfertile protocoleces. The cysts are slow growing and maybe asymptomatic being noted as incidental findings atpost mortem examination. However, particularly large ornumerous cysts can interfere with organ function. Figure 12shows hydatid cysts found in the liver and lungs of adonkey that presented with respiratory distress, weight lossand ventral oedema. Ultrasound can be useful todiagnose infection as the cysts are frequently near thesurface of the organ and can be clearly visualised.

Surgical treatment by excision or drainage of affectedcases may be attempted if the cysts are in ananatomically safe location and in the case described bySummerhayes and Mantell (1995), a retrobulbar cyst wassuccessfully drained. Drainage of cysts in the liver and lungmay be dangerous if cystic liquor is spilt, risking seedingnew infection and possible anaphylaxis. Medicaltreatment relies upon the long term use of albendazoleand/or praziquantel. It can be hard to decide upon theclinical significance of hydatid cysts and a number of testssuch as serum amyloid A, plasma fibrinogen and biopsyadjacent to the cyst may be required.

Fig 10: Histological section of lung with fibrosis. Mature collagenwithin alveolar walls to the right of the slide. H&E x20magnification.

Fig 11: CT image of donkey lungs (obtained post mortem) withsevere fibrosis visible as white areas.

Fig 12: Hydatid cysts in a donkey lung.

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Prevention relies upon treating domestic carnivoreswith praziquantel and preventing their access to rawinfected offal.

There is limited information about the prevalence ofhydatidosis in donkeys; at the Donkey Sanctuary, postmortem records indicate that the incidence is higher indonkeys that originate from Wales and Ireland. There aresome reports in the literature regarding the prevalence ofhydatidosis in donkeys in Jordan and Morocco, whichshow an increase in infection with age and apreponderance of liver over pulmonary cysts (Pandey1980; Mukbel et al. 2000).

Pulmonary neoplasia

Thoracic neoplasia is uncommon in the donkey and anincidence of 0.4% for pulmonary neoplasia was found inthe survey by Morrow et al. (2010). This is similar to theincidence in horses quoted by other authors (Mair et al.2004; Davis and Rush 2006).

Neoplasia should be considered as a differentialdiagnosis especially in elderly donkeys with chronicrespiratory disease that are nonresponsive to conventionaltherapy. Clinical signs may be variable depending onwhether the tumour is primary or secondary in origin, andwhere the lesion is located anatomically.

Typical signs include variable dullness, intermittentpyrexia, weight loss, lymphadenopathy, dyspnoea andtachypnoea. There may be haematological andbiochemical changes, suggesting chronic inflammatoryprocess, including anaemia, monocytosis,hyperglobulinaemia and hyperfibrinogenaemia. The fewclinical cases recorded by the author have not shownventral oedema or pleural effusion, but this may relate tothe site of tumour development. Diagnosis may be hard toconfirm and requires the use of endoscopy, radiographyand cytological analysis of any effusion or mass (Figs 13and 14).

Summary

The aim of this review has been to cover what is currentlyknown about respiratory disease in the donkey. It is clearthat much of the information comes from small case seriesand limited studies. The donkey plays an enormous role insupporting the livelihoods of those dependent on its use asan agricultural animal and in providing pleasure as acompanion animal, and because of this, it is important toshare knowledge and continue to progress in finding outhow we, as veterinary surgeons, can improve the welfareof this stoical species.

Author’s declaration of interests

No conflicts of interest have been declared.

Acknowledgements

The author wishes to acknowledge the advice and supportof her colleagues at The Donkey Sanctuary in the UK andOverseas, particularly with acquiring images. Dr TobiasSchwarz, Senior Lecturer in Diagnostic Imaging, Universityof Edinburgh, supplied Image 11, CT scan. Dr SionaghSmith, University of Edinburgh, supplied Image 10, histologysection. Amy Miele, University of Edinburgh, suppliedImage 7, pleural scan.

References

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