Pulmonary capillariasis, caused by Capillaria aerophila (also known as Eucoleus aerophilus) is a parasitic disease that typically occurs in wild carnivores (e.g., mustelids and foxes). However, C. aerophila, a Trichuroidea nematode, can also infest dogs and cats and, sporadically, even humans. The adult stages of the parasite live in the mucosa of the trachea, bronchi, bronchioles and, sometimes, nasal and frontal sinuses of the host.
This is a poorly known and underestimated disease because it is generally thought that the parasite is weakly pathogenic and that infestation of pets is only occasional. Furthermore, it is a diagnostically challenging disease and, since it is often not possible to make a definite diagnosis easily, it is also difficult to acquire exhaustive information on the spread of the nematode and on the correlation between C. aerophila and the clinical respiratory picture. For this reason, information on pulmonary capillariasis in the dog and cat is very limited and only in the last few years has the interest of the scientific community focused on this infection, in the light of new data suggesting the emergence of the parasite.
THE PARASITE
The adult stages are whitish and about 2.4-3 cm long. After mating, the females lay eggs that reach the upper airways in the mucus and through the effect of coughing. After having reached the pharynx they are swallowed. The eggs, which are non-embryonated (Fig. 1) and, therefore, not infesting, transit unharmed through the whole gastrointestinal tract and are eliminated with the faeces. These eggs mature in the external environment in about 20-45 days, with the formation of an internal larva (Fig. 2) that can infest receptive vertebrate hosts. Facultative intermediate hosts can also be included in the life cycle of C. aerophila;such hosts are earthworms that eat the eggs present in the environment, within which the infesting larvae form. The cycle continues when the receptive vertebrate host is infested by ingesting embryonated eggs or earthworms. The larvae, after having hatched from the eggs, cross the gastrointestinal mucosa and reach the lung parenchyma through the lymphatic system. Once settled in the parenchyma, the parasite reaches sexual maturity about 1-2 months after the infestation.
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As said, infestation by C. aerophila is considered to occur only occasionally in dogs and cats and is more common among wild animals such as foxes and mustelids; nevertheless, in recent years this parasitic infection has been repeatedly reported in various areas of the world, also in domestic animals. The parasite has a cosmopolitan distribution, although the data published on its spread in Italy, like those for other countries, are very limited. Until a few years ago the only reports of C. aerophila infection in Italian animal populations were limited to those of finding the parasite in post-mortem examinations carried out during studies of helminth fauna in wild carnivores. A report published in 2008 described finding C. aerophila in the context of a study carried out to evaluate the spread of Aelurostrongylus abstrusus in populations of cats in the centre and south of Italy. Subsequent studies showed that the rates of infections are ~3% in dogs and ~5-6% in cats, in the centre of Italy.
The possibility that a cat or dog becomes infested by C. aerophila depends not only on the existence of the facultative vector, but also on the presence of eggs capable of surviving, alive and infestant, in the external environment for many months. The spread of the parasite in different geographic areas is guaranteed by the ubiquity of earthworms as well as its direct life cycle. The interaction between the parasite, its hosts and the environment plays an important role in the apparently increased risk of capillariasis and the recognition of the parasite as an aetiological agent of respiratory disease in companion animals. One factor suggested to be a cause of the growing diffusion of pulmonary capillariasis is the increase in fox populations in peri-urban or even urban zones. In particular, it has been hypothesised that cases of scabies in foxes could make these animals more sensitive to other parasitic infections, such as angiostrongylosis and pulmonary capillariasis. The theory is that C. aerophila would find conditions favourable for its biological cycle and would, therefore, have the possibility of infecting a broad range of receptive hosts, including domestic animals, in peri-urban and urban zones given the dispersion of eggs in the environment. The finding of concomitant infection by Sarcoptes scabiei and pulmonary nematodes in populations of foxes supports this hypothesis but, at the moment, the real role played by the reservoir of pathogens in the wild in favouring the spread of pulmonary capillariasis in dogs and cats has yet to be determined.
PATHOGENIC ROLE AND CLINICAL MANIFESTATIONS
The adult stages of C. aerophila live on the surface of bronchioles, bronchi and the trachea, fixed completely or partially to the mucosa, and cause damage to the epithelium and lung parenchyma. The parasite can also be found, rarely, in the mucosa of the nasal cavities, and the nasal and frontal sinuses.
The pathogen stimulates an inflammatory process in the respiratory tissues, with consequent rhinitis, tracheitis and/or bronchitis which, in most cases, become chronic. The signs, which are not always evident, range from minimal respiratory disturbances (e.g. loud vescicular murmurs) to a more substantial clinical picture with a catarrhal nasal discharge and dry cough. During the night, the cough is sibilant and deep. The animal develops chronic bronchitis with bronchovescicular breath sounds, wheezing and sneezing and, particularly when secondary bacterial infections become established, a moist, productive cough. The mucus in the lumen of the trachea and bronchi decreases and areas of emphysema appear. In those cases in which the parasite load is high, abscesses of pulmonary parenchyma can develop and the animal breathes with an open mouth and has severe dyspnoea. The infested animal, particularly if young, can die of bronchopneumonia or respiratory failure.
A study recently carried out in Italy on the spread and clinical impact of pulmonary capillariasis in pets showed that the most common clinical picture was a general difficulty with breathing with a dry or productive cough in 70-80% of the infested animals. Furthermore, the animals could have dyspnoea and respiratory wheezes and, particularly in cats, a nasal discharge and sneezing.
C. aerophilacan infect humans, albeit only occasionally; this zoonosis is characterized by fever, bronchitis, cough with a catarrhal expectorate, haemoptysis and dyspnoea. The last case described in Serbia is particularly interesting: a woman with C. aerophila infection was initially thought to have a bronchial carcinoma. The patient presented with a productive cough and purulent expectorate and computed tomography scans showed bronchopulmonary shadows and nodular, partially confluent, infiltrating lesions of the parenchyma. The finding of C. aerophila eggs in the pulmonary biopsies clarified that these tumour-like lesions were nothing other than abscesses caused by the presence of dead parasites in the bronchi, highlighting the diagnostic challenge that can be posed by C. aerophila infection in human medicine.
DIAGNOSIS
C. aerophilainfection cannot be diagnosed on clinical grounds because the manifestations are non-specific. Clinical signs such as fatigue with cough, sneezing, mucopurulent nasal discharge and open-mouthed breathing should lead the veterinarian to include pulmonary capillariasis among the differential diagnoses, although this clinical picture is similar to that of many other diseases. For example, in the cat, pulmonary capillariasis must be distinguished from parasitosis caused by Dirofilaria immitis or A. abstrusus, from bacterial or viral infections, and from allergies, fungal infections or nasopharyngeal polyps. In dogs, signs similar to those caused by C. aerophila are present in parasite infections by D. immitis, Angiostrongylus vasorum, Crenosoma vulpis and Filaroides spp., and during many other disorders, such as other infectious diseases, nasopharyngeal polyps, allergic bronchitis, foreign bodies and tumours.
Diagnostic imaging is not useful for the diagnosis of capillariasis because the radiographic findings are variable, non-specific interstitial and/or alveolar changes.
The definitive diagnosis of pulmonary capillariasis is made from the finding and recognition of the typical eggs of the parasite in the mucus, bronchial lavage fluid or faeces of an infected animal. A flotation method with sucrose, sodium chloride or zinc sulphate can be used to look for the eggs of the nematode in the faeces of animals; solutions with a specific gravity of 1200-1350 generally provide the best results.
The operculated, lemon-shaped eggs of C. aerophila (Fig. 1), are 60-80 mm long and 25-40 mm wide, have axially asymmetrical poles, a densely striated wall and numerous anastomoses. They can, however, be confused with the eggs of other better known, more widely spread parasites with similar morphology, such as the nasal parasite Eucoleus bohmi and, more often, intestinal parasites of the genus Trichuris. Indeed, when lemon-shaped eggs are found in faecal specimens, especially from dogs, in most cases they are mistaken for the better known Trichuris vulpis eggs. However, the eggs of Trichuris are larger (70-80 mm long, 30-50 mm wide), have a smooth wall, symmetrical poles that are in axis, and a ring-like thickening at the base. Furthermore, T. vulpis does not infect cats, although felines can be infested by other species of Trichuris not present in Europe. The eggs of E. bohmi are smaller (50-60 mm long, 30-35 mm wide) than those of C. aerophila and have minuscule fissures on the external surface.
TREATMENT
There is very little information available on the treatment of pulmonary capillariasis in pets and what there is, has been derived from individual case reports. Daily oral administration of fenbendazole at a dose of 50 mg/kg for 2 weeks has shown a certain efficacy in the treatment of pulmonary capillariasis in dogs. Levamisole, administered at the dose of 5 mg/kg for 5 consecutive days in three cycles separated by intervals of 9 days, has also been reported to be effective. Treatment with two doses of subcutaneous abamectin 0.3 mg/kg, administered 2 weeks apart, has been used in cats.
Suggested readings
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- Burgess H., Ruotsalo K., Peregrine A.S., Hanselman B., Abrams-Ogg A. 2008. Eucoleus aerophilus respiratory infection in a dog with Addison's disease. Canadian Veterinary Journal 49, 389-392.
- Lalosević D., Lalosević V., Klem I., Stanojev-Jovanović D., Pozio E. 2008. Pulmonary capillariasis miming bronchial carcinoma. American Journal of Tropical Medicine and Hygiene 78, 14-16.
- Traversa D., Di CesareA., IorioR., Avolio S., Pampurini F., Bartolini R., Milillo P., Schaper R., Heine J. 2008. Eucoleus aerophilusand Aelurostrongylus abstrusus: two neglected lungworms affecting cats in central Italy. Atti XXV Congresso della Società Italiana di Parassitologia (SO.I.PA.), Pisa 18-21/6/2008, Parassitologia 50 (1), p. 217.
- Traversa D., Di Cesare A., Milillo P., Iorio R., Otranto D. 2009. Infection by zoonotic Eucoleus aerophilus in dogs and cats: is another extra-intestinal parasitic nematode of pets emerging in Italy? Research in Veterinary Science 87, 270-272.
- Traversa D., Milillo P., Iorio R., Di Cesare A., Bartolini R., Avolio S., Paoletti B. 2009. Diffusione di Capillaria aerophila (sin. Eucoleus aerophilus) nel cane e nel gatto in centro Italia. SUMMA 5, 39-43.
- Traversa D., Di Cesare A., Conboy G., 2010. Canine and feline cardiopulmonary parasitic nematodes in Europe: emerging and underestimated. Parasites & Vectors2010, 3:62.

