Signalment:  

Red fox (Vulpes vulpes), juvenile, femaleThis red fox was found alive at a golf course in late July. It was showing signs of illness: weak, heaving, breathing heavily, not scared of humans. This was the second fox in one week from the same golf course with similar signs. The animal was shot in the head with a .22-caliber rifle and submitted for necropsy.

Gross Description:  

This female red fox was considered to be a young of the year (approximately 3-4 months old), based on its small size. It was in poor body condition (no fat in subcutis, only a small amount of fat around the base of the heart and in the mesentery). Both lungs were very emphysematous. The mucosa of the caudal region of the trachea was covered by a small to moderate amount of creamy whitish material and contained a few slightly raised plaques, about 2-3 mm in diameter. Almost the entire bronchial tree of both lungs was filled with creamy yellow material suggestive of pus (1-1). The stomach was empty. The large intestine contained a moderate amount of fecal material.

Histopathologic Description:

Lesions were confined to the respiratory tract and, in the lungs, were centered around the bronchial tree. Several cross and oblique sections of small nematodes, mixed with numerous ova (1-2) (often with an operculum evident at both ends), large numbers of macrophages and some neutrophils, rested on the mucosal epithelium of small and large bronchi or were embedded within it. Much of this epithelium was markedly hyperplastic, particularly in the larger bronchi, although areas of epithelial loss were also evident. The submucosa of the larger intrapulmonary bronchi was infiltrated by numerous plasma cells and some eosinophils. Many ova, several of them degenerated, could be found within bronchioles and alveoli where they were associated with a pyogranulomatous reaction, including multinucleated giant cells that had phagocytized some of these ova. Lesions similar to those within the lungs were in the main bronchi and in the caudal region of the trachea, together with fibrosis, necrosis and fibrin accumulation (tissues not included). The pulmonary nematodes were identified in tissue sections as Eucoleus aerophilus(1-3) (formerly Capillaria aerophila).³

Morphologic Diagnosis:  

Severe chronic pyogranulomatous verminous bronchopneumonia

Lab Results:  

Streptococcus species (group G), was isolated in large numbers from a bronchial swab.

Condition:  

Eurocoleus aerophilus (Capillaria aerophila)

Contributor Comment:  

This young red fox had a severe pulmonary parasitic infection, likely complicated by a secondary bacterial infection. The nematode Eucoleus aerophilus belongs to the superfamily Trichinelloidea, whose members typically parasitize epithelial surfaces of vertebrates.⁴ Eucoleus aerophilus has been reported at a low prevalence in most fecal surveys of dogs and cats and is enzootic in wild foxes in many parts of the world.^4,9 In the three Maritime provinces of Canada (Prince Edward Island, New Brunswick, Nova Scotia), more than 65% of wild red foxes that have been examined were infected by this parasite.⁹ The life cycle of E. aerophilus is mainly direct through the fecal-oral route, although earthworms that have ingested the ova with soil can also act as facultative intermediate or, more likely, paratenic hosts.⁴

Clinical signs in infected dogs and cats are generally characterized by a low-grade chronic cough. The disease among foxes raised in earthen runs on fur farms, however, used to be much more severe, with poor growth, decreased fur quality, and substantial mortality from bronchopneumonia, particularly among young animals.⁷ Control of the disease was achieved by shifting the animals to raised cages with wire bottoms. In free-living wild red fox, the degree of infection may vary among animals but is probably generally higher in young-of-the-year because of their immature immune system. It is conceivable that, every year, a number of young fox die from pneumonia caused by this parasite, either because their immune system is particularly inefficient or because they are exposed to a very large number of eggs. In this case, secondary infection by Streptococcus species group G had likely contributed to the animals death. Most bacteria of this group isolated from animals are S. canis. This bacterium can be isolated from mucous membranes of asymptomatic domestic carnivores, but it can also cause opportunistic infections, including suppurative bronchopneumonia and septicemia.¹⁰

The nematode Crenosoma vulpis is another common pulmonary parasite in the red fox population of the Canadian Maritime provinces and often occurs concurrently with E. aerophilus.⁹ This parasite may also be a common cause of respiratory disease in domestic dogs presented with clinical signs of chronic cough.¹ Crenosoma vulpis has an indirect life cycle, using snails and slugs as intermediate hosts.¹¹ Eucoleus aerophilus is longer but more slender than C. vulpis (Table 1).⁸ Whereas E. aerophilus is oviparous, C. vulpis is ovoviviparous, and it also tends to inhabit deeper regions of the bronchial tree.⁹ Adults and first stage larvae of Crenosoma vulpis were not identified in the lungs of this fox.

Table 1: Comparison of the dimensions of adult specimens of Eucoleus aerophilus and Crenosoma vulpis.⁶

	length		Diameter
	male	female	male	female
E. aerophilus	15-25 mm	20-40 mm	60-100 μ	100-180 μ
C. vulpis	3.5-8 mm	12-16 mm	280-320 μ	300-480 μ

Other potential nematode parasites of the respiratory system of red fox in this country include Oslerus (Filaroides) osleri, Dirofilaria immitis, and Angyostrongylus vasorum. Infection by O. osleri is characterized by the formation of discrete nodules typically found near the bifurcation of the main bronchi, whereas both D. immitis and A. vasorum are parasites of the pulmonary arterial tree rather than of the airways.³ Moreover, the North American distribution of A. vasorum is currently confined to the Atlantic Canadian province of Newfoundland.²

JPC Diagnosis:  

Lung: Bronchopneumonia, pyogranulomatous and eosinophilic, multifocal, severe, with bronchiolar epithelial hyperplasia, aphasmids and eggs, etiology consistent with Eucoleus aerophilus, red fox (Vulpes vulpes), canine.

Conference Comment:  

The capillarids are a large group of parasites that have been divided into numerous different genera on more than one occasion. The former Capillaria affecting dogs and cats is now primarily divided into three genera:³ Eucoleus, which is found in the airways; Aonchotheca, which is found in the intestinal tract; and Pearsonema, which is found in the urinary bladder. Other genera of veterinary importance include Calodium, which is found in the liver of rats and other mammals.³ The division into these genera is not universally accepted as some researchers prefer the previous genus name Capillaria.⁶

The life cycle of Eucoleus (Capillaria) aerophilus can be either primarily direct or less commonly indirect involving an earthworm as an intermediate paratenic host. Eggs are deposited in the pseudostratified ciliated epithelium, work their way up the respiratory tree, are swallowed, and are then passed out with the feces.⁴

Physical characteristics of E. aerophilus are similar to those of other aphasmid nematodes.⁵ Aphasmids lack a pair of sensory papillae on their caudal end. They lack the prominent lateral cords seen in phasmid nematodes. They have a hypodermal band and one genital tract in the female.⁵

References:

1. Bihr T, Conboy G: Lungworm (Crenosoma vulpis) infection in dogs on Prince Edward Island. Can Vet J 40:555-559, 1999
2. Bourque A, Whitney H, Conboy G: Angiostrongylus vasorum infection in a coyote (Canis latrans) from Newfoundland and Labrador, Canada. J Wildl Dis 41:816-819, 2005
3. Bowman DD, Lynn RC, Eberhard ML: Georgis Parasitology for Veterinarians, 8th ed., pp. 190-196, 216-222, 229-233. Elsevier Science, St. Louis, MO, 2003
4. Campbell BG: Trichuris and other Trichinelloid nematodes of dogs and cats in the United States. Comp Cont Educ Pract Vet 13:769-778, 1991
5. Gardiner CH, Poynton SL: Morphological characteristics of trematodes in tissue section. In: An Atlas of Metazoan Parasites in Animal Tissues. pp. 40-42. Armed Forces Institute of Pathology, Washington, D.C., 2006
6. Hamier AN, Rupprechtt CE: A retrospective histopathologicla survey of capillariasis in raccoons from the eastern United States. J Parasitol 84:180-181, 1998
7. Hanson KB: Tests of the efficacy of single treatments with tracheal brushes in the mechanical removal of lungworms from foxes. J Am Vet Med Assoc 82:12-33, 1933
8. Levine ND: Nematode Parasites of Domestic Animals and of Man, pp. 292, 543. Burgess Publishing Company, Minneapolis, MN, 1968
9. Nev+�-�rez A, L³pez A, Conboy G, Ireland W, Sims D: Distribution of Crenosoma vulpis and Eucoleus aerophilus in the lung of free-ranging red foxes (Vulpes vulpes). J Vet Diagn Invest 17:486-489, 2005
10. Songer JG, Post KW: Veterinary Microbiology: Bacterial and Fungal Agents of Animal Disease, pp. 43-53. Elsevier Inc., St. Louis, MO, 2005
11. Soulsby EJL: Helminths, Arthropods and Protozoa of Domesticated Animals, 7th ed., pp. 282-283, 340-341. Lea & Febiger, Philadelphia, PA, 1982

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