An infection of the lower respiratory tract, usually resulting in bronchitis or pneumonia, can be caused by any of several parasitic nematodes, including Dictyocaulus viviparus in cattle, llamas, and alpacas; D filaria in goats, sheep, llamas, and alpacas; D eckerti in deer; D arnfieldi in donkeys and horses; Protostrongylus rufescens and Muellerius capillaris in sheep and goats; Metastrongylus apri, M pudendotectus, and M salmi in pigs; Oslerus osleri, Crenosoma vulpis, and Eucoleus aerophilus in dogs; and Aelurostrongylus abstrusus and E aerophilus in cats. Other lungworm infections occur but are less common.
Species of Dictyocaulus belong to the superfamily Trichostrongyloidea and have direct life cycles. E aerophilus belongs to the Trichuroidea and is thought to have a direct life cycle. The others belong to the Metastrongyloidea and, except for O osleri, have indirect life cycles.
Some nematodes that inhabit the right ventricle and pulmonary circulation, eg, Angiostrongylus vasorum and Dirofilaria immitis, both found in dogs in certain areas of the world, may be associated with pulmonary disease. Clinical signs relating to a cardiac or a pulmonary syndrome or to a combination of both may occur.
Diseases caused by the ruminant Dictyocaulus spp are of most economic importance. The cattle lungworm D viviparus is common in northwest Europe and is the cause of severe outbreaks of “husk” or “hoose” in young (and more recently, older) grazing cattle. The lungworm of goats and sheep, D filaria, is comparatively less pathogenic but does cause losses, especially in Mediterranean countries, although it is also recognized as a pathogen in Australia, Europe, and North America. D filaria and D viviparus are less pathogenic in alpacas and llamas, although severe infections can cause coughing, dyspnea, depression, and loss of condition. D arnfieldi can cause severe coughing in horses and, because patency is unusual in horses (but not in donkeys), differential diagnosis with disease due to other respiratory diseases can be difficult. M capillaris is prevalent worldwide and, although usually nonpathogenic in sheep, can cause severe signs in goats. Other lungworm infections cause sporadic infections in various animal species in many countries.
Adult females in the bronchi lay larvated eggs that hatch either in the bronchi (D viviparus, D filaria) or in host feces (D arnfieldi) after being coughed up and swallowed. The infective third-stage larvae can develop on pasture within 5–7 days in warm, moist conditions, but typically in summer in temperate northern climates will require 2–3 wk. Once larvae are infective, transmission depends on their dispersal away from the fecal pats. Dispersal mechanisms are, primarily, mechanical and include rain or, in the case of D viviparus and possibly D arnfieldi, by the sporangia of the fungus Pilobolus. A proportion of infective larvae survive on pasture throughout the winter until the following year but, in very cold conditions, most become nonviable. The principal source of new infections each year is from infected carrier animals, with overwintered larvae providing a secondary but not unimportant contribution in some countries. In the case of D arnfieldi, donkeys are the prime source of pasture contamination for horses. Clinical disease in ruminants usually develops on first exposure to sufficient infective larvae; the severity of disease and stimulation of an immune response is related to the number of larvae ingested. In cattle and sheep, this usually occurs during their first season at pasture; however, an increase in the number of older cattle affected has been reported and is attributed to the efficiency of some prophylactic anthelmintic regimens, which eliminates infection and prevents development of a protective immune response. Because transmission of infection to horses requires infected donkeys (patent infections rarely occur in adult horses but may occur in foals and yearlings), first infections can occur at any age in that species. Once infected, adult ruminants generally become immune to further disease, but a proportion maintain subclinical infections during which they act as a source of further pasture contamination. Occasionally, when previously infected adults or groups that have not been exposed to reinfection for >1 yr, and in which immunity may have waned, are exposed to an overwhelming level of infection, clinical disease may recur. In areas of Europe in which cattle are housed during winter and first grazing season calves turned out in late April or May, the first infections can be seen between mid June and late July, but most severe infections generally occur in previously unexposed calves after development of the second generation of infective larvae on pasture between August and early October.
Metastrongylus spp in pigs require an earthworm intermediate host; thus, infection is confined to pigs with access to pasture and may become more common in previously uncommon areas as a result of organic farming methods. M capillaris and P rufescens in sheep and goats require slugs or snails as intermediate hosts, which must be eaten for infection to occur. C vulpis is acquired by dogs through ingestion of an infected terrestrial snail or slug intermediate host. A abstrusus is normally acquired by cats after ingestion of a paratenic host such as a bird or rodent that has previously eaten the infected slug or snail intermediate host. Adults of O osleri live in nodules in the trachea of dogs, and larvated eggs laid by adults hatch there. Larvae migrate up the bronchial tree and may pass in the feces; however, these are not active, are often dead or degenerating, and are not an important route of transmission. Infection in domestic dogs is mainly through saliva as the dam cleans her pups. E aerophilus in dogs likely has a direct cycle, with larvated eggs being ingested with food or water.
The pathogenic effect of lungworms depends on their location within the respiratory tract, the number of infective larvae ingested, and the animal’s immune state. During the prepatent phase of D viviparus infection, the main lesion is blockage of bronchioles by an infiltrate of eosinophils in response to the developing larvae; this results in obstruction of the airways and collapse of alveoli distal to the block. Clinical signs are moderate unless large numbers of larvae are ingested, in which case the animal may die in the prepatent phase with severe interstitial emphysema and pulmonary edema.
In the patent phase, the adults in the segmental and lobar bronchi cause a bronchitis, with eosinophils, plasma cells, and lymphocytes in the bronchial wall; a cellular exudate, frothy mucus, and adult nematodes are found in the lumen. The bronchial irritation causes marked coughing, and the entire reaction leads to increased airway resistance. A major component of the patent stage is development of a chronic, nonsuppurative, eosinophilic, granulomatous pneumonia in response to eggs and first-stage larvae aspirated into alveoli and bronchioles. This is usually in the caudal lobes of the lungs and is severe when widespread; in combination with the bronchitis, death may result. Interstitial emphysema, pulmonary edema, and secondary bacterial infection are complications that increase the likelihood of death. Survivors may suffer considerable weight loss.
If the animal survives until the end of patency (2–3 mo for D viviparus), most or even all of the adult worms are expelled, and the cellular exudate resolves over the ensuing 4 wk. Most animals recover unless secondary infection develops in the damaged lungs during the postpatent phase. In a few animals, clinical signs are exacerbated in the postpatent phase due to development of a diffuse, proliferative alveolitis characterized by hyperplasia of the type II alveolar epithelial cells. The cause is unknown, but it is seen much less often in cattle treated with anthelmintics with a persistent action against D viviparus such as the macrocyclic lactones ivermectin, doramectin, eprinomectin, and moxidectin.
D filaria is similar to D viviparus, but interstitial emphysema is not a common complication. Bronchial lesions predominate in D arnfieldi infections; when an alveolar reaction occurs, as in donkeys or foals, there are lobular areas of overinflation due to intermittent obstruction of small bronchi.
The pathogenic effect of the other lungworms has a similar basis, but frequently such severe clinical signs are not produced, perhaps because of a more restricted localization in the lungs and less severe infections. The patent phase and the associated lesions last >4 mo for some lungworms (M apri and A abstrusus) but can be >2 yr (M capillaris). The lesions in pigs with metastrongylosis are a combination of localized bronchitis and bronchiolitis with overinflation of related alveoli, usually at the tips and midway along the diaphragmatic lobes. Associated with the mass of nematodes in the lumen is hypertrophy and hyperplasia of bronchiolar and alveolar duct smooth muscle with marked mucous cell hyperplasia. Near the end of the patent period (as adult worms are killed), gray-green lymphoid nodules (2–4 mm) are formed; fragments of dead worms may be seen microscopically in these nodules composed of lymphocytes and plasma cells surrounding a central zone of eosinophils.
In M capillaris and P rufescens infections, chronic, eosinophilic, granulomatous pneumonia seems to predominate; the reaction is in the bronchioles and alveoli that contain the parasites, their eggs, or larvae. They are surrounded by macrophages, giant cells, eosinophils, and other immunoinflammatory cells, which produce gray or beige plaques (1–2 cm) subpleurally in the dorsal border of the caudal lung lobes. Small (1–2 mm), greenish, nodular lesions may also develop. The effect of these lesions in sheep is minor, perhaps because of the predominantly subpleural location. This infection represents the lower end of the pathogenic spectrum for lungworms.
In cats, A abstrusus produces nodular areas of granulomatous pneumonia in the caudal lobes that, if sufficiently generalized, can be clinically significant and occasionally fatal; a notable feature is the hypertrophy and hyperplasia of the smooth muscle in the media of pulmonary arteries and arterioles. The nodules of O osleri, found in the mucous membrane of the trachea and large bronchi, can produce extreme airway irritation and persistent coughing. C vulpis infections result in chronic bronchitis and bronchiolitis, which leads to chronic coughing. E aerophilus infections in dogs are usually well tolerated but may cause chronic tracheitis and bronchitis.
In adult animals not previously exposed to infection, the lesions and pathogenesis are the same as in young animals. However, in adults with some degree of immunity, reexposure to the parasite (eg, husk in adult cattle) can result in different lesions. Despite the immune response, many larvae reach the lungs before they are killed in the terminal bronchioles and alveoli. Larvae not killed in the terminal bronchioles may reach the bronchi and cause a bronchitis characterized by marked eosinophilic infiltration of the bronchial walls and greenish yellow exudate in the lumen comprising eosinophils, other inflammatory cells, and parasitic debris. The reaction associated with this process can lead to severe clinical signs if the nodules are numerous and the eosinophilic bronchitis extensive; this is responsible for the reinfection phenomenon.
Signs of lungworm infection range from moderate coughing with slightly increased respiratory rates to severe persistent coughing and respiratory distress and even failure. Reduced weight gains, reduced milk yields, and weight loss accompany many infections in cattle, sheep, and goats. Patent subclinical infections can occur in all species.
The most consistent signs in cattle are tachypnea and coughing. Initially, rapid, shallow breathing is accompanied by a cough that is exacerbated by exercise. Respiratory difficulty may ensue, and heavily infected animals stand with their heads stretched forward and mouths open and drool. The animals become anorectic and rapidly lose condition. Lung sounds are particularly prominent at the bronchial bifurcation. In adult dairy cattle, milk yield drops severely, and abnormal lung sounds are heard over the caudal lobes. The reinfection phenomenon in adult dairy cattle is usually seen in the fall; although less severe than in initial infections, the signs are widespread coughing and tachypnea and a marked drop in milk yield.
The signs in llamas, alpacas, sheep, and goats infected with D filaria are similar to those in cattle. Pulmonary signs usually are not associated with M capillaris or P rufescens in sheep, but the former can affect goats similarly to D filaria. D arnfieldi is associated with coughing, tachypnea, and unthriftiness in older horses but with few if any signs in foals or donkeys.
The main clinical sign of metastrongylosis in pigs is a persistent cough that may become paroxysmal.
Coughing and dyspnea occur with A abstrusus infections in cats and O osleri or C vulpis infections in dogs. Fatalities are relatively uncommon with these lungworms, although they do occur in kittens.
Diagnosis is based on clinical signs, epidemiology, presence of first-stage larvae in feces, and necropsy of animals in the same herd or flock. Bronchoscopy and radiography may be helpful. Larvae are not found in the feces of animals in the prepatent or postpatent phases and usually not in the reinfection phenomenon (D viviparus). ELISA tests are available in some countries. The test is mainly of use in detecting cattle that have not been exposed, rather than as a differential diagnostic tool in acute respiratory disease. In the early stages of an outbreak, larvae may be few in number. First-stage larvae or larvated eggs can be recovered using most fecal flotation techniques with the appropriate salt solutions; however, larvae will crenate if allowed to sit for a long time on the slide before examination, making identification difficult. Bronchial lavage can reveal D arnfieldi infections in horses. A convenient method to recover larvae is a modification of the Baermann technique, in which large fecal samples (25–30 g) are wrapped in tissue paper or cheese cloth and suspended or placed in water contained in a beaker. The water at the bottom of the beaker is examined for larvae after 4 hr; in heavy infections, larvae may be present within 30 min.
In domestic pets, detection of first-stage larvae in the feces, either on flotation or with the Baermann technique, is still the diagnostic technique of choice. However, in dogs, cats, and horses, because of the relative infrequency of infection in many areas, lungworms may be considered only after failure of antibiotic therapy to ameliorate the condition. Adults of Dictyocaulus spp and M apri are readily visible in the bronchi during the patent phases of infection. However, examination of smears from bronchial mucus or histologic sections from lesions may be necessary to confirm the diagnosis during other stages of lungworm infection (and also for other lungworms).
Bronchoscopy can be used to detect nodules of O osleri or to collect tracheal washings (dogs and horses) to examine for eggs, larvae, and eosinophils.
Necropsy should include examination of the trachea, particularly at the bifurcation, for O osleri and the lesions they induce.
Several drugs are useful to treat lungworms (see Table: Recommended Treatments for Lungworms a). The benzimidazoles (fenbendazole, oxfendazole, and albendazole) and macrocyclic lactones (ivermectin, doramectin, eprinomectin, and moxidectin) are frequently used in cattle and are effective against all stages of D viviparus. These drugs are also effective against lungworms in sheep, horses, and pigs. Levamisole is used in cattle, sheep, and goats, but treatment may need to be repeated 2 wk later because it is less effective against larvae during the early stages. Topical formulations containing moxidectin, selamectin, or emodepside and oral fenbendazole have been used successfully in cats for A abstrusus. O osleri in dogs is a problem, but there is evidence that fenbendazole and ivermectin are effective if treatment is prolonged (fenbendazole). Injectible doramectin along with removal of as many nodules as possible is the current treatment of choice. E aerophilus in dogs and cats is similarly difficult to treat, but success has been reported with ivermectin, fenbendazole, or selamectin.
Recommended Treatments for Lungworms a
Animals at pasture should be moved off infected pasture, and supportive therapy may be needed for complications that can arise in all species.
Lungworm infections in herds or flocks are controlled primarily by vaccination or anthelmintics. Oral vaccines are available in Europe for D viviparus (northeastern areas) and D filaria (southeast). Two doses of irradiated infective larvae are given 4 wk apart, with the second dose given at least 2 wk before the start of grazing or exposure to probable infection. Used properly, they prevent clinical disease, but some vaccinated animals may become mildly infected to the extent that larvae are excreted and perpetuate further infection.
Anthelmintic prophylaxis has become feasible with the advent of anthelmintics with prolonged activity (eg, ivermectin, doramectin, moxidectin, eprinomectin). With persistent anthelmintics, two or three treatments during the grazing season, the timing of which depends on local grazing practice and epidemiology, are effective and may, by disrupting developing infections, stimulate immunity to the parasite. The use of multiple treatments may delay immunity to D viviparus until the animal is adult, when infection (albeit usually less severe) can occur. However, these methods have become popular in that GI parasites are controlled simultaneously.
Other more sporadic infections can be controlled more easily by management, eg, avoidance of grazing horses with donkeys, indoor husbandry of pigs, and by not mixing sheep and goats on the same grazing.