History

Toulouse – 1yr 6 month Male neutered Corsac Fox.
History of chronic coughing and weight loss with intermittent diarrhoea. Toulouse had previously been treated with 4 x weekly milbemycin. Chronic cough persisted. Previous faecal testing negative.

Xrays, blood profile and BAL performed. Bloods showed increase in ALT, BUN and Phos with evidence for haemoconcentration.

 

 

Figure 1:
X-rays revealed a diffuse bronchial pattern, possibly more alveolar pattern in cranial lung fields.

 

Clinical Approach

Cytology reveals marked, predominantly eosinophilic inflammation with the presence of parasitic ova. Ova were ellipsoid and generally 60-65 µm in length. Occasionally the ova had distinct bipolar caps. Morphology raised significant suspicion for Eucoleus (Capillaria) spp. Given the location of the inflammation in the lower airways, presence of ova in the airways and morphology of the ova – Eucoleus (Capillaria) aerophila was suspected.

 

 

Figure 2: BAL cytology preparation showing high numbers of inflammatory cells which are mainly eosinophils with lesser numbers of neutrophils and occasional macrophages.

 

 

Figure 3: BAL cytology preparation showing marked predominantly eosinophilic inflammation and embedded helminth ova.

 

 

Figure 4: Eucoleus (Capillaria) aerophila egg in BAL from this case (left), and from a dog right (5)

 

Samples sent for PCR confirmed the presence of Eucoleus (Capillaria) aerophila. Culture also revealed a pure profuse growth of Bacillus which is generally considered of low pathogenicity. However, in the context of a small neutrophilic component to inflammation, absence of oropharyngeal contamination and noting this is a pure growth, the finding may be significant in this case.

Eucoleus (Capillaria) aerophila is a parasitic helminth found in the lower respiratory tract, primarily affecting wild carnivores however, it can also infect dogs and cats. Infections are often asymptomatic in otherwise healthy individuals but in young animals or immunosuppressed individuals, the disease can be more severe and can lead to cough, nasal discharge, dyspnoea, anorexia and debilitation.

 

 

Figure 5: Adult female Eucoleus aerophilus on the mucosa of the opened trachea of a fox  (1)

 

Life cycle

Eggs are released from infected animals in faeces and remain viable in the environment for up to 1 year. Earthworms may act as paratenic hosts. Infection is faecal oral or via ingestion of infected earthworms and ingested ova hatch in the small intestine, penetrate the mucosa and migrate via the blood or lymphatics to the lungs. Here they enter the alveoli and migrate up to the trachea, bronchi and bronchioles where they live beneath the epithelium and release eggs to be coughed up and swallowed (2).

 

 

Figure 6: Eucoleus (Capillaria) aerophile life cycle. Source VPG

 

Diagnosis

Diagnosis is either by detection of ova in BAL or sputum or in faecal analysis. Larvae are rarely seen allowing differentiation from other respiratory helminth infections. Main differentials for the ova are Eucoleus boehmi and if found in faeces, Trichuris vulpis (whipworm). Other lungworm species are generally seen as larvae rather than ova aiding identification.  Eucolues boehmi, Truchuris vulpis and Eucoleus aerophilia all have very similar appearing ova but location is important. Eucoleus boehmi is mainly nasal cavity and paranasal sinuses and Trichuris vulpis is an intestinal parasite.

 

Prevalence

Very wide geographical distribution virtually worldwide and across Europe and it primarily infects wild carnivores (foxes) but can infect domestic carnivores. It is also a potential zoonosis with occasional cases reported in humans (3). In UK, High prevalence in lungs of red fox population, average of 31%. No current studies to determine prevalence in UK cat and dog population but worldwide an average of 3% in dogs and up to 8% in cats (4).

 

(1) Lalošević, V., Lalošević, D., Čapo, I., Simin, V., Galfi, A. & Traversa, D. – Lalošević, V., Lalošević, D., Čapo, I., Simin, V., Galfi, A. & Traversa, D. (2013). High infection rate of zoonotic Eucoleus aerophilus infection in foxes from Serbia. Parasite 20: 3. doi:10.1051/parasite/2012003

(2) Traversa D, Di Cesare A, Lia RP, Castagna G, Meloni S, Heine J, et al. New insights into morphological and biological features of Capillaria aerophila (Trichocephalida, Trichuridae) Parasitol Res. 2011;109:S97–104. doi: 10.1007/s00436-011-2406-4. [DOI] [PubMed] [Google Scholar]

(3) Lalosević D, Lalosević V, Klem I, Stanojev-Jovanović D, Pozio E. Pulmonary capillariasis miming bronchial carcinoma. Am J Trop Med Hyg. 2008;78:14–16. doi: 10.4269/ajtmh.2008.78.14. [DOI] [PubMed] [Google Scholar]

(4) Samorek-Pieróg M, Cencek T, Łabuć E, Pac-Sosińska M, Pieróg M, Korpysa-Dzirba W, Bełcik A, Bilska-Zając E, Karamon J. Occurrence of Eucoleus aerophilus in wild and domestic animals: a systematic review and meta-analysis. Parasit Vectors. 2023 Jul 20;16(1):245. doi: 10.1186/s13071-023-05830-0. PMID: 37475031; PMCID: PMC10360280.

(5) Di Cesare, Angela & Castagna, Giuseppe & Otranto, Domenico & Meloni, Silvana & Milillo, Piermarino & Latrofa, Maria & Paoletti, Barbara & Bartolini, Roberto & Traversa, Donato. (2012). Molecular Detection of Capillaria aerophila, an Agent of Canine and Feline Pulmonary Capillariosis. Journal of clinical microbiology. 50. 1958-63. 10.1128/JCM.00103-12.

 

 

Thank you to Holly Faulkner at Ark Veterinary centre for collaborating on this case.