Abstract

A hatch-year Common Raven (Corvus corax) with subcutaneous and internal pseudocysts, filled with fluid, containing a pair of adult trematodes and numerous eggs consistent with Collyriclum faba, died near a riverbank in California, US. While C. faba is incidental in many Passeriformes, this case was a fatal systemic infection.

Collyriclum faba typically causes a self-limiting disease in Passeriformes worldwide, where many species harbor the trematodes but with rare fatality (Literák et al. 2003). In its host, C. faba leads to subcutaneous pseudocysts at three locations: femoral or tibial subcutis (leg ecotype), vent or abdomen (vent ecotype), or above the coccygeal gland (rump ecotype; Heneberg et al. 2011; Heneberg and Literák 2013). The pseudocysts occur less frequently in the sternal region or face (Literák et al. 2003) or, in South American passerines, in the throat region (Kirmse 1987). Each pseudocyst contains a pair of adult trematodes immersed in a fluid rich in eggs, which are released into the environment through a pore when triggered by contact with water (Parker 2009). Thick layers of fibrous connective tissue form the pseudocysts, with minimal inflammation in adjacent tissues (Blankespoor et al. 1982). Significant disease may occur when large numbers of pseudocysts are present in one location, such as obstructing the cloacal opening and leading to impaction, emaciation, and death in the vent form. Concurrent infections also can influence the extent of tissue damage (Literák et al. 2003; Grove et al. 2005). We report a systemic C. faba infection in a Common Raven (Corvus corax).

A female, <1-yr-old Common Raven with “boils” or “ulcers” on the abdomen was in debilitated condition and died on the bank of the Eel River, Humboldt County, California, US on 25 July 2013. On necropsy the bird was emaciated and the abdomen was turgid, firm, and doughy. The ventral body extending to the cloaca was diffusely alopecic and a large central area was ulcerated with crusting (Fig. 1A). The abdominal wall was severely thickened and disrupted by tightly organized clusters of 0.5–1.0-cm diameter cystic formations in the subcutis. More than 12 similar structures were spread throughout the serosa of the abdominal organs, primarily on the gastrointestinal serosa and the splenic capsule, with extensive tenacious adhesions between the intestinal loops, mesentery, and peritoneal wall (Fig. 1B). The spleen was enlarged, the air sacs were thickened and opaque. The pseudocysts had transparent walls, were filled with brown watery fluid with particulates, and contained two light brown, coiled, adult trematodes with visible vitelline sacs (Fig. 1C). On microscopy, the particulates were oval, translucent operculated eggs.

Figure 1

Systemic infection by the trematode Collyriclum faba in a hatch-year wild Common Raven (Corvus corax). (A) The raven was emaciated and the abdominal subcutaneous pseudocysts caused a swollen, thick, doughy abdomen with alopecic, ulcerated skin (arrow). (B) Internal pseudocysts (arrows) as clusters or singly throughout the gastrointestinal serosal surfaces, with adhesions, and on splenic capsule with splenomegaly (star). (C) A pseudocyst within the peritoneal cavity filled with fluid and containing two coiled adult trematodes (thick arrow) and vitelline sacs (thin arrow). (D) Histologic appearance of a pseudocyst within the peritoneal wall that contains paired C. faba trematodes (black star outline on the tegument of the trematodes) with numerous eggs filling the uterus (arrows) and free in the connective tissue (arrow head). The thick capsule of the pseudocyst is formed by dense fibroblastic proliferations in the inner portion and surrounding mature connective tissue without notable inflammation (black solid stars). Bar=100 μm.

Figure 1

Systemic infection by the trematode Collyriclum faba in a hatch-year wild Common Raven (Corvus corax). (A) The raven was emaciated and the abdominal subcutaneous pseudocysts caused a swollen, thick, doughy abdomen with alopecic, ulcerated skin (arrow). (B) Internal pseudocysts (arrows) as clusters or singly throughout the gastrointestinal serosal surfaces, with adhesions, and on splenic capsule with splenomegaly (star). (C) A pseudocyst within the peritoneal cavity filled with fluid and containing two coiled adult trematodes (thick arrow) and vitelline sacs (thin arrow). (D) Histologic appearance of a pseudocyst within the peritoneal wall that contains paired C. faba trematodes (black star outline on the tegument of the trematodes) with numerous eggs filling the uterus (arrows) and free in the connective tissue (arrow head). The thick capsule of the pseudocyst is formed by dense fibroblastic proliferations in the inner portion and surrounding mature connective tissue without notable inflammation (black solid stars). Bar=100 μm.

Tissue samples were fixed in 10% neutral-buffered formalin, embedded in paraffin, cut at 5-μm sections, and stained with H&E. Multiple pseudocysts were collected in 70% ethanol for parasitology. Ancillary tests included aerobic bacterial culture of liver as well as PCR on intestinal contents for Salmonella spp., on an oropharyngeal swab for avian influenza and avian paramyxovirus-1, and on kidney tissue for West Nile virus. Toxicologic analyses involved liver tissue screening for selenium, heavy metals (lead, manganese, cadmium, copper, iron, zinc, molybdenum, arsenic, and mercury), and anticoagulant rodenticides (brodifacoum, bromadiolone, chlorophacinone, coumachlor, difethialone, diphacinone, and warfarin).

Histologically, pseudocysts with dense fibrous walls coalesced to obliterate and expand the ventral peritoneal wall up to 0.7 cm and the intestinal wall up to 0.3 cm thickness. The splenic capsule and the posterior lung parenchyma and air sacs had similar pseudocysts that contained one to two trematodes (Fig. 1D) and numerous brown-pigmented, oval eggs. Peripherally, fibrous tissue with variably hyalinized or mucinous matrix with occasional fragments of pre-existing collagen and muscle bundles separated the pseudocysts. The inner portions of the fibrous capsule contained regions with abundant eggs and were circumferentially infiltrated by densely packed fibroblasts and occasional scattered heterophils, eosinophils, or histiocytes. Numerous small-caliber vessels were within the perimeter of the fibrous walls. The hepatic capsule and air sacs were thickened with mature connective tissue. The epicardium demonstrated serous atrophy of fat. The fixed trematodes were up to 5 mm long with a subterminal dorsal oral sucker. Rows of spines were observed along the dorsal tegument with less-prominent spines along the ventrum, consistent with C. faba (Blankespoor et al. 1982; Taylor et al. 2007).

Laboratory tests were negative except for trace levels of brodifacoum in the liver; this was regarded as an incidental finding due to lack of hemorrhages.

This C. faba infection is unique with respect to the reported host species and the distribution of infection. Despite the first descriptions of this parasite over a century ago (Farner and Morgan 1944), the taxonomy, complete life cycle, and host-pathogen interactions are still being unraveled. Until recently, C. faba was classified under Gorgoderoidea and, together with Collyricloides massanae, formed the two members of the family Collyriclidae. However, in addition to morphologic differences, C. massanae forms pseudocysts in serosa of intestines rather than the subcutis and can infect mammals. Birds are the only definitive hosts for C. faba. Recent reclassification placed C. faba singly in Collyriclidae (Heneberg and Literák 2013; Kanarek et al. 2015).

Similar to the raven, most cases of C. faba are in young birds found close to water—features that pertain to birds becoming infected in the nest and the association of the trematode's life cycle with water, respectively (Stunkard 1971; Heneberg et al. 2011). The two aquatic intermediate hosts recently elucidated in Europe, a gastropod (Bythinella austriaca) and a mayfly (e.g., Ecdyonurus venosus, Rhithrogena picteti, Rhithrogena iridina), are likely the same in North America (Heneberg et al. 2015).

The majority of information on C. faba is from Europe, where the trematode is enzootic in a large number of passerines in the Carpathians (Literák et al. 2003). All reported cases in corvids are from North America (Heneberg and Literák 2013) and all had the vent form with no adverse effects except for one American Crow (Corvus brachyrhynchos) that had adhesions between the abdominal peritoneal wall and the intestinal serosa but no internal parasites (Grove et al. 2005; Parker 2009). The more-advanced disease in the crow may have been due to immunosuppression from a concurrent avian pox virus infection. The only other comparable fatal case with involvement of the lung was in a European Starling (Sturnus vulgaris; Prosl and Loupal 1985) that, similarly, had no underlying disease. These differences could represent a different or more pathogenic ecotype, or immunosuppression due to malnutrition, or an undetermined cause may be involved in this case.

We thank Julia Chapman, Dave Lancaster, and Terry Wildman for invaluable assistance.

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