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Parasitic Airway Disease
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Overview
The disease that will be described here is Dictyocaulosis associated with infection by the nematode, Dictyocaulus arnfieldi. This parasite infects the respiratory tract of horses, donkeys, mules, hinnies and zebras and has been found throughout the world. D. arnfieldi is most commonly found in donkeys in which it is rarely associated with clinical disease. In contrast, in adult horses and ponies D. arnfieldi rarely develop to mature infections, however the parasite does cause clinical signs, most commonly coughing. It is generally believed that donkeys are the natural hosts of D. arnfieldi and that horses only become infected following grazing with donkeys. However, several reports have shown that patent infections can exist in horses and D. arnfieldi infections have been found in horses with no previous history of donkey contact [1]. Please note that the general features of D. arnfieldi infections observed in donkeys and horses are compared in Table 1.
Table 1. Summary table of the general features of D. arnfieldi infections in horses and donkeys | |||||
| Patency | Clinical Signs | Persistent Infections | Diagnosis | Treatment |
Horses | uncommon | usually | uncommon | clinical signs RS sampling response to treatment | macrocyclic lactone |
Donkeys | common | uncommon | common | fecal analysis (Baermannisation) | macrocyclic lactone |
RS = respiratory secretion Please note that the features listed here are what are most commonly encountered in each species. It is important to remember that there is some overlap in these features, for example some horses can have patent infections (particularly as foals). |
Parasite Life Cycle
The life cycle is not fully known, but it is thought to be similar to that of the bovine lungworm, Dictyocaulus viviparus. The infective stage is the third stage larva (L3) which is ingested from contaminated pasture. It appears that migration in the equine host occurs via the mesenteric lymph nodes and that larvae reach the heart via the thoracic duct [1]. Experimental infections in helminth-free donkey foals have indicated that the pre-patent period is approximately 13 weeks [2], after which the adult parasitic stage is found in the small bronchi. This is a different predilection site to that of D. viviparus adult worms, which are found in the main stem bronchi and trachea. The adult female D. arnfieldi lay eggs, which hatch quickly so that first stage larvae (L1) are recovered in the feces (Fig. 1). Early experiments showed that L1 develops through to L3 in as short as three days under optimal conditions and that the L3 survives a maximum of 14 days when in direct sunlight, but this extends to between 24 and 42 days when they are incubated in shade [3].
Donkeys are the most common source of contamination with counts of up to 1,400 L1/g being recorded [2]. Patent infections in donkeys are known to persist for at least five years and these infections probably last throughout the lives of most untreated donkeys. Nothing is known of the mechanism of persistent infection in donkeys and whether this is associated with prolonged longevity of the adult worms or, more likely, sequential re-infections. Patency in horses appears to be much shorter than that in the donkey and has been recorded from six weeks (in foals) to eight months (in older horses), although this was extended to 21 months in horses that were in poor condition [2].
Figure 1. D. arnfieldi L1 larva. (Courtesy of Professor B. Losson).
Prevalence
Several prevalence studies relating to D. arnfieldi have been performed on both horses and donkeys. In a study in the Netherlands, 51% of donkeys tested that were over 5 months old were found to excrete L1 in their feces [4]. Interestingly, levels of excretion were found to increase with age, suggesting that donkeys do not develop immunity to D. arnfieldi. In a separate postmortem study performed on the lungs of 423 Moroccan donkeys, D. arnfieldi was found to be present in 47% of the donkeys [5]. Here, adult parasites were detected in the lungs throughout the year with up to 1,000 parasites recovered from one donkey. The ratio of lung worms to L1 per gram of feces varied from 1:0.57 to 1:1.33 over the course of the year.
In a Danish study where prevalence of D. arnfieldi in horses (n = 140) and donkeys (n = 176) was investigated, 87.5% of donkeys were shown to excreted L1, often in high numbers and in the absence of overt clinical signs [6]. In this study, 106 of the horses grazed on establishments where donkeys were present and 10.4% of these horses passed D. arnfieldi L1 in their feces. A further 34 horses, that were hospitalized with dyspnea and coughing, were also coprologically tested for D. arnfieldi L1 and 8.8% of these were observed to be positive for infection. In fact, all horses in this study that had patent infections of D. arnfieldi had some degree of dyspnea or coughing. In a German study where horses and donkeys were examined coprologically at regular intervals over 15 months, D. arnfieldi was detected in only 16.2% donkeys (n = 37), whilst the horses (n = 23) that were examined, had no larvae detected in their feces [7]. The difference observed in levels of infection between these two studies may be due to the lower numbers of animals examined in the latter study or differences in environmental conditions that may have affected pre-parasitic larval development. Alternatively, it could be that a higher level of usage of macrocyclic lactones, such as ivermectin, in the later study reduced the overall prevalence of infection as D. arnfieldi are susceptible to this class of anthelmintics (see below).
In a large USA study performed on 5,437 live horses, ponies, mules and donkeys on 91 farms [8], fecal samples were examined and D. arnfieldi L1 were detected in 2% of 5,379 horses. These infected horses were present on 38% of the 90 farms investigated in the study. In comparison, 54% of donkeys and mules had L1 positive samples and these animals represented samples sent from 80% of the 10 farms included that had donkeys present.
In a Dutch hospital study [9], the feces of 3,791 horses and ponies were examined for a range of endoparasites. A total of 0.2% of the horses were positive for D. arnfieldi L1. In a separate hospital survey on 300 adult horses, admitted specifically for examination of the respiratory tract [10], 2.6% horses were found to harbour lungworm infection, based on respiratory secretion analysis and endoscopy. In this survey, six out of 12 horses that had a history of grazing with donkeys had lungworm infection [11].
In a Kentucky study in which the lungs of horses were examined postmortem, D. arnfieldi was recovered from 11% of 488 horses [12]. Most of the horses that were positive for lungworm had less than five worms recovered from their lungs and the majority of these parasites were sexually immature fifth stage larvae (L5). Examination of feces from 54 of the 56 positive horses showed that 30% had lungworm L1 present. In another Kentucky study [13], 89 Thoroughbred youngsters ranging from 14 to 333 days old were examined and D. arnfieldi was detected in 1 or 2 horses in a month during the study. In another coprological study, an annual incidence of 2.5 to 12.7% was found in horse feces submitted specifically for lungworm examination in Newmarket from 1967 to 1970 [1].
The results of these studies indicate that many donkeys are infected, in the absence of clinical signs, and pass L1 in their feces. In contrast, few horses have patent infections and those horses that are infected tend to show clinical signs of respiratory disease. These animals usually, but not always, have a history of contact with grazing donkeys.
Pathology of Lungworm Infections
Whether or not D. arnfieldi causes pathological lesions in donkeys is controversial. In cases where lungworm was thought to have caused severe disease in donkeys, other pathological agents, e.g., viruses, may have been involved [1]. Many other studies have reported the presence of patent infections in healthy donkeys. The lesions that are induced by D. arnfieldi were studied in a group of six naturally infected donkeys and, clinically, five of these animals showed very mild signs of respiratory insult [14]. The remaining animal was observed to have few parasites but had pneumonia and pulmonary edema (Fig. 2). The five donkeys with mild signs were necropsied and their worm burdens enumerated and pathology assessed at the gross and histological levels. Varying numbers of adult worms were harvested from the individuals. The most obvious pathological changes were discrete circular areas of over-inflation, which ranged in size from three to five cm in diameter, surrounding affected bronchi. These lesions were more frequent in the caudal lung lobe, particularly at the distal tip, the lateral edge and mediastinal border. On histological sectioning, the raised areas consisted of over-inflated tissue at the centre of which was a small bronchus packed with coiled nematodes. The small airways in these areas had a greenish appearance and were often occluded with exudate. Adult worms were seen lying in the main bronchi in mucus that was not copious. Histologically, little cellular or mucoid reaction occurred around the adult worms, but when L1 were found in the lumen they were completely surrounded by an intense muco-purulent reaction. There was marked bronchiolitis with goblet cell hyperplasia and an inflammatory infiltrate, which primarily consisted of lymphocytes. The areas of lung not showing gross parasitological changes were normal in appearance except for a diffuse eosinophilia. Although alveolar over-inflation was observed, true emphysema was not present. In a horse that presented with multiple parasitic infection, including D. arnfieldi, similar lung lesions were observed. Histologically, there was an intense immunological reaction evidenced by the presence of large "cuffs" of lymphoid tissue surrounding many bronchi [15]. Many immature parasites were observed in smaller bronchi and there was bronchial epithelial hyperplasia with large amounts of mucus and pus and many areas of alveolar hemorrhage and edema. Again, alveoli were over-inflated especially around the smaller bronchi, which were plugged with mucus.
Figure 2. D. arnfieldi adult worms in a donkey trachea. (Courtesy of Professor B. Losson).
Clinical Signs
Clinical signs are not obvious in infected donkeys. On auscultation harsh lung sounds may be detected. In horses, infection is often associated with a chronic cough and tachypnea. Coughing can be seen as early as 12 days post infection and clinical signs are most severe in the third to fifth weeks of infection [1]. After this, the signs usually abate but coughing persists, especially on exercise, for several months and in some cases, if animals remain untreated, for over a year. Horses remain bright and are not usually anorexic. In one report in which eight adult horses co-grazed with an infected donkey, the horses presented with a moist cough of six-week duration and were found to have large numbers of eosinophils in tracheal washes [16]. Coughing was also observed in mature ponies in a study where four mares, two donkey mares and foals co-grazed a paddock [17]. Coughing started in two of the mares within four to six weeks of grazing infected pasture. In one of these mares, coughing continued until the end of the study over one year later. No clinical signs were observed in the pony foals, however within 11 weeks of exposure to this pasture all six foals developed patent infections. In a large case control study on respiratory disease [11], coughing was frequently present in all horses (n = 7) that presented with lungworm infection. A total of 43% of these horses presented with a nasal discharge and 83% had a history of grazing with donkeys. In this study, tracheal respiratory secretions and broncho-alveolar lavage eosinophil ratios were raised with lungworm infection [18]. Not all horses that co-graze with infected donkeys show clinical signs of respiratory disease. In fact, horses seem to vary in their response to the parasite: for example one mare, which passed 1,520 L1/g of feces and harboured 20,000 adult worms at necropsy, had no clinical signs of lungworm disease whatsoever [1].
Epidemiology
Donkeys may acquire infections when young and remain infected throughout their lives. This appeared to be the case in the Netherlands study cited above [4]. Frequent examinations made on two donkey studs over five years, showed that there was remarkable stability in larval output of individual animals [2]. In this study there were no obvious seasonal variations in fecal larval counts. There was some indication that pregnancy and lactation had an effect on worm burdens as some mares, previously negative, developed patent infections and others had increases associated with foaling.
In donkeys and horses, adult parasites have been found in lungs throughout the year [5,12]. In one study in Morocco, October, February and June were the months when the highest peaks of infections were observed [5]. In a large study performed over one year in Kentucky, lungworm infected horses were found in each month of the study and infection levels were highest in April and lowest in September [12].
The acquisition of infection by donkey foals was studied on studs in the UK over four breeding seasons [2]. The first patent infections were not detected until August in the year of birth, with 62% of foals having patent infections in the autumn. Experiments on the natural acquisition of infection by horse foals indicated that a similar pattern occurred with infections reaching patency 12 to 19 weeks after exposure to infected pasture [2], however the duration of patency was only 6 to 31 weeks in these animals.
Little is known about the development of infections in adult horses. Although donkeys are common reservoirs for infection in horses, transmission of lungworm from horse to horse has been reported. In one study, there were several instances of lungworm infections in horses where no contact with donkeys could be established [8]. There has been a dispute as to whether older horses have patent infections, but several studies have shown patent infections in animals up to 20 years of age and it can be concluded that age immunity per se does not exist in the horse. The majority of horses with lungworm in the UK do not have patent infections. In an experimental study on 49 ponies, 24 developed clinical disease but patent infections were established in only two animals [1]. Although patent infections were only found in two ponies, worms were found in all 31 ponies that were necropsied more than 13 days post infection. Most of the worms were retarded in development at L5. Ponies that were necropsied 13 months after the infection were also seen to have L5 in their lungs. In contrast to the results in the adult ponies, lungworm developed to maturity in all six foals that were grazed on the infected pasture. Thus, these results indicate that young horse foals develop patent infections more readily than adult horses.
It has also been suggested that, similar to D. viviparus infections in cattle, the fungus Pilobolus plays a role in the spread of D. arnfieldi L3. In one study, between 10 and 25% of D. arnfieldi larvae excreted in feces were harvested from fecal cultures by means of Pilobolus[19]. The larvae that were recovered were viable.
Diagnosis
D. arnfieldi eggs hatch in the large intestine or soon after being passed in the feces. Thus, D. arnfieldi L1 can be readily demonstrated in feces of infected donkeys using the modified Baermann technique [20]. This technique relies on the active migration of larvae out of the fecal mass and their subsequent sedimentation in water [21]. Fifty grams of feces should be used and the larvae recovered following overnight incubation. Method of storage can have an effect on the efficiency of larval recovery from feces. For example, L1 recovery was not affected in fecal samples kept for 48 h at 4ºC, whilst storage at 16ºC and 20ºC resulted in significant losses in the region of 40-50% after 24 h and 80% after 48 h [20]. Therefore it is important to examine the samples quickly or store them in the fridge. These workers showed that nearly half the larvae emerge into the Baermann funnel within 5 to 6 h.
In horses, confirming diagnosis by fecal analysis is more difficult as the infections do not often reach patency, particularly in adult animals. Furthermore, numbers of larvae present are often low. Thus it is important not to exclude lungworm in the differential diagnosis of chronic coughing just because L1 cannot be harvested from feces. Trans-tracheal aspirates can be useful for demonstrating increased eosinophil numbers. For example in one study, L5 were observed in tracheal mucus obtained from a 6-year old gelding, which presented with a harsh dry cough and increased expiratory effort [22]. In a large case control study on equine pulmonary disease [10], horses were diagnosed as suffering from lungworm infection if they had eosinophilic pulmonary inflammation associated with endoscopic evidence of lungworm larvae in their airway. Alternatively, horses that presented with eosinophilic pulmonary disease, which responded to anthelmintic therapy and pasture change (if necessary), were diagnosed as having lungworm infection. Thus, diagnosis in horses can be based on clinical signs, together with a history of donkey contact and a positive response to appropriate anthelmintic treatment.
Treatment
Successful treatment of both horses and donkeys has been described using moxidectin, ivermectin and benzimidazoles (at elevated dose rates).
Benzimidazoles
High dose rates of benzimidazoles are required for effective treatment of lungworm infections. In an early report, thiabendazole given twice at a 10-fold therapeutic dosage of 440 mg/kg was used successfully to treat a horse with a harsh, dry paroxysmal cough, which had eosinophils and L5 in the tracheal mucus [22]. In the outbreak described in six horses above [16], clinical signs resolved in all horses treated with two oral administrations of thiabendazole at 440 mg/kg. Thiabendazole at this dose rate has also been used successfully to treat donkeys [2] cited by [23]. However, this regime has not been evaluated in a controlled trial and some animals have shown depression and anorexia after treatment.
In a separate study where oxibendazole was used at a range of doses from 5 to 15 mg/kg, the drug was ineffective against D. arnfieldi [24]. A single dose of fenbendazole (at 7.5 mg/kg) as well as higher doses (up to 30 mg/kg) and repeated treatments (2 x 15 mg/kg) also failed to eliminate lungworm infections in donkeys [25]. In contrast to this, albendazole was used successfully to achieve full clinical recovery in several ponies and one horse when the drug was used at 25 mg/kg twice daily for five days [26].
In a controlled trial in naturally infected donkeys, mebendazole given orally for five days at elevated dose rates of 15.2 to 20 mg/kg was 75 to 100% effective in the removal of parasites from individual animals [27]. The drug was ineffective when given orally at a dose rate of 4.3 to 5.7 mg/kg for five days. A study to investigate re-establishment of patent lungworm infection in donkeys after treatment with mebendazole at 15 to 30 mg/kg per day for five days, showed that the number of animals excreting L1 fell from 66% to 23% one month after treatment [23]. Despite exposure to infected pastures throughout the summer these levels were maintained at a comparatively low level and, by October, patent infections had re-established in only 15% of the donkeys that were negative following treatment.
Ivermectin
The efficacy of orally administered ivermectin at 200 µg/kg against D. arnfieldi was assessed in a controlled study in 12 yearling ponies [28]. A single dose was 100% effective against adult and immature stages of lungworm. In the case control study of 300 cases presenting with pulmonary disease of which seven were diagnosed with lungworm infection, all animals were treated with oral ivermectin at 200 µg/kg and all were re-examined post treatment [29]. At initial re-examination two of the seven cases showed no clinical improvement, however these horses still had access to contaminate pastures. A second re-examination was performed following a further ivermectin treatment and removal from pasture and a clinical improvement was achieved. Of the seven horses, 86% showed complete improvement, whilst 14% had partial improvement. The results indicated that the combination of ivermectin treatment and pasture change was an effective treatment.
Moxidectin
In a small study on seven donkeys that were positive for lungworm larvae prior to treatment, four were treated with moxidectin orally at 400 µg/kg [30]. All animals were found to be negative for lungworm larvae up to 21 days post treatment.
Control
D. arnfieldi infection should be addressed in the routine worm control programme of all horses and ponies co-grazing with donkeys. In these cases, donkeys co-grazing with horses should be treated to reduce L1 output and hence pasture contamination. Strategic treatments with a macrocyclic lactone can be administered based on regular fecal sampling of all donkeys and treatment based on the presence of a positive L1 count. Based on their study with mebendazole quoted above, Clayton and Trawford [23] recommended that on donkey-only grazing, annual treatment of all residents for lungworm in the spring, combined with isolation and treatment of new arrivals, should result in significant reductions in pasture L3 burdens.
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Affiliation of the authors at the time of publication
Dept of Vet Clinical Science and Animal Husbandry, Division of Equine Studies, Faculty of Veterinary Science, University of Liverpool, Liverpool, UK.
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