Equine Lungworm
Scott M. Austin
Dictyocaulus arnfieldi is a nematode parasite that affects donkeys, mules, horses, and asses. Infection occurs most frequently in cold, damp climates. This parasite appears to be well adapted to the donkey, as large numbers of parasites are associated with minimal clinical signs.1 In contrast, infections in horses produce intense tissue reaction to parasites, resulting in clinical signs of a cough and arrested development of the adult worms.
It has been suggested that donkeys are the natural host and that horses require cohabitation with donkeys to acquire the infections. Although it is true that patent infections are rare in the horse, horses may be infected without any history of exposure to infected donkeys.2,3 D. arnfieldi has a direct life cycle. Infection begins with the ingestion of infective L3 larvae from contaminated pastures. Larvae migrate from the intestines to the lungs via the lymphatics and then infiltrate the alveoli. Adult worms may reach 8 cm in length and can block smaller airways. There is no evidence that links infection in donkeys to pulmonary fibrosis; however, lungworm infections may exacerbate other coexisting pulmonary disease.1 The lungworms have a prepatent period of about 8 to 13 weeks.3,4 Embryonated eggs produced from patent infections are coughed up, swallowed, and passed in the feces. The eggs hatch into first-stage larvae in the feces and spread onto pastures with the assistance of the fungus Philbolus.1 The larvae congregate on or in the sporangiophore of this fungus, which colonizes the surface of the manure. Fluid within the sporangiophore increases in pressure until it explodes at midday, spreading parasitic larvae up to 3 meters from the site of origin. The dispersion of larvae away from feces increases the odds of ingestion by a susceptible host. The L1 larvae can survive for up to 7 weeks in the environment with suitable warmth and moisture but die rapidly in the cold.5,6 Maturation of L1 larvae into infective L3 larvae can happen in as little as 5 to 7 days under permissive conditions. In contrast to infections in donkeys, larval development is usually arrested in the early fifth stage in horses, and patent infections are rare.7,8 In horses, infections are more frequently encountered when pastured with donkeys, but infections have been identified in closed horse herds without exposure to donkeys or mules.1,6,9,10Although D. arnfieldi infections have been common in donkeys, more recent surveys indicate a significant decline in the prevalence of this parasite.11 Three decades ago, a survey of horses and donkeys in central Kentucky identified an infection rate of 54% for donkeys and 25% for horses.9 In a separate study of a single Kentucky farm, lungworm larvae were found in 93% of donkeys and 50% of Thoroughbreds.12 A more recent survey of 735 new donkeys at admission to a sanctuary in the United Kingdom (2004-2008) demonstrated a prevalence of only 4% in donkeys.11 Necropsy surveys of horses in central Kentucky from 2000 to 2001 failed to identify any D. arnfieldi infections.13 The macrocyclic lactones, which are highly effective against D. arnfieldi, were introduced after these initial studies and are probably responsible for the decline in incidence of this parasite.1
Donkeys rarely show clinical signs associated with infection, and pathology is usually limited to areas of overinflation surrounding affected bronchi and to the tip of the caudal lung lobe. In contrast, more significant lesions are seen in infected horses and are associated with a more robust inflammatory response to lungworm infections.1 In the horse, larvae within the bronchi stimulate a marked eosinophilic and lymphocytic exudate.14 Damage from the adult worms causes focal edema and hemorrhage and results in hyperplasia and thickening of occupied bronchi.15 The adult parasites also impair local defenses as they disrupt the mucociliary apparatus and cause a decrease in alveolar macrophage numbers, allowing for opportunist bacterial infections.7 Exudate, adult parasites, and airway hyperplasia cause obstruction of small bronchioles and secondary air trapping. Examination of affected lungs demonstrates interstitial pneumonia, focal necrosis, and areas of pulmonary overinflation in the lung periphery.4,14
Parasitic pneumonitis can affect horses of any age, but clinical signs are most frequent in horses between 5 and 8 years of age.9 Clinical signs can develop as rapidly as 12 days after ingestion of infective larvae.7 Chronic cough is the most common manifestation in the horse, along with exercise intolerance and mucopurulent nasal discharge.10 Affected horses are rarely inappetant or dull.
Diagnosis in donkeys relies on the modified Baermann technique to detect larvae in the feces. Fifty grams of feces are required for this test. Accurate results require the feces to be evaluated quickly or to be kept cool, as temperatures greater than 16o C are associated with the loss of 50% of the larvae in 24 hours and the loss of 80% in 48 hours.15 Since patent infections are rare in horses, endoscopic or transtracheal examination for larvae or proof of eosinophilic inflammation may be required to make a diagnosis. Hematologic and serum chemistry results are frequently normal in horses with uncomplicated parasitic pneumonitis. Mature neutrophilia and hyperfibrinogenemia are usually seen only when there is a secondary bacterial infection.16 Supportive evidence for parasitic pneumonia can be obtained by transtracheal wash, BAL, and possibly direct visualization through an endoscope. Cytology of aspirates demonstrates abnormally elevated eosinophil counts (greater than 2%). Eosinophil percentages as high as 88% have been recovered from horses with Dictyocaulus infections. Larvae or eggs can be found during examination of the fluid.16 Radiographic examination is nonspecific and may reveal a mixed bronchointerstitial pattern.5,16 Centrifugal flotation, modified McMaster technique, and Baermann technique have all been used to identify eggs or larvae in the feces of infected animals. Confirmation of infections in horses is difficult, as patent infection is rare.
Historically, thiabendazole (440 mg/kg/day for 2 days) and mebendazole (20 mg/kg/day for 5 days) were effective in reducing parasite load and larval shedding, but neither product is currently available.17 Fenbendazole, a benzimidazole that is still available, only reduces larval numbers in feces of donkeys by 50% to 70% when administered at 15 mg/kg PO once.18 The larvicidal dose of fenbendazole (10 mg/kg/day for 5 consecutive days) is not effective against adult D. arnfieldi.18 Macrocyclic lactones such as moxidectin (400 μgZkg) or ivermectin (200 μgZkg) have been demonstrated to be effective against mature and immature stages of Dictyocaulus spp., and these drugs are the most frequently used products to treat parasitic pneumonia.19 It is recommended that new donkeys be tested for Dictyocaulus and treated accordingly before introduction to a herd. Horses that graze pastures shared with donkeys are more likely to acquire infections, so it is important to control infections in donkeys and limit exposure of horses to the parasite.20