Gross Findings: On postmortem examination, the chick was an 870 g female in poor body condition with diminished fat stores. Body feathers were downy and flight feathers were 2-3 cm exsheathed. The proventriculus was enlarged (45 x 30 x 25 mm) with a 5-mm thick wall. On the serosal aspect of the proventriculus were many raised serpentine tracts up to ~15 x 2 x 2 mm (Fig. 1A). The left liver lobe was compressed by the enlarged proventriculus. The upper gastrointestinal tract contained a few crickets.

Histopathological Findings: The muscular wall of the proventriculus is multifocally expanded by cavitations containing large nematodes. Cavitations are lined by epithelioid macrophages and contain variable amounts of hypereosinophilic (necrotic) debris, hemorrhage, and bacteria (Fig. 1B).  Nematodes have a thick, smooth cuticle, coelomyarian-polymyarian musculature, a pseudomembrane, prominent ventral nerve chords, and ~ 50 x 30 µm operculated eggs (Fig. 1B, 1C, 1D). Other microscopic findings include intestinal trematodes (Strigeidae and Diplostomidae), multifocal intestinal mucosal necrosis with intralesional bacteria, splenic lymphoid depletion, and renal urate stasis.

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Morphologic Diagnosis:

1. Proventriculus: Proventriculitis, granulomatous, marked, with intralesional nematodes and bacteria

Disease: Eustrongylidosis

Etiology: Eustrongylides sp. (including E. ignotus, E. tubifex, and E. excisus)

Distribution: Worldwide; E. ignotus and E. tubifex are found in North America

Seasonality: Infections can occur year-round, but mortality in young birds usually occurs in spring or summer.

Host range: Fish-eating birds, including Pelicaniformes (especially herons and egrets), Gaviiformes (loons), Suliformes (cormorants), Anseriformes (mergansers), Gruiformes (cranes), Podicipediformes (grebes), Chardriiformes (gulls), and Accipitriformes (eagles)

Transmission: The life cycle is indirect and complex, requiring four nematode larval stages and two intermediate hosts. The first larval stage of the nematode develops within eggs shed in avian host feces and ingested by aquatic oligochaetes, the first intermediate host. In the worm, the eggs hatch and develop into second and third-stage larvae, which are then ingested by small fish, the second intermediate host. The larvae encapsulate within the fish and develop into fourth-stage larvae, which are ingested by birds upon consuming the fish.  Amphibians and reptiles may also serve as second intermediate hosts. Predatory fish, amphibians, and reptiles can also serve as transport or paratenic hosts. Once ingested by the bird, larvae in fish penetrate the proventriculus within 3-5 hours and reach sexual maturity, releasing eggs into the gastrointestinal tract, within 10-17 days.

Clinical signs: Infections range from asymptomatic to fatal; fatal infections are more common in young birds. Clinical signs can include dyspnea, anorexia, difficulty swallowing, and regurgitation. Death is often due to bacterial coelomitis and sepsis caused by penetration of the nematodes through the gastrointestinal tract.

Pathology: In acute infections, raised tracts or tunnels may be grossly visible on the proventricular, ventricular, or intestinal serosa. There may be an accompanying fibrinous coelomitis or associated hemorrhage. Adult worms are red and can grow to 15 cm long and 4 mm wide. In chronic infections, raised tracts may be less conspicuous. Microscopically, nematodes are present within cavities in the wall of the gastrointestinal tract surrounded by granulomatous inflammation, hemorrhage, and necrosis. Concurrent findings may include bacterial coelomitis and airsacculitis.

Diagnosis: In live birds, the raised tunnels on the proventriculus may be palpated through the skin. A postmortem diagnosis is made through typical gross and microscopic lesions, with speciation of the nematodes possible by morphology of the adult worms and for some species.

Public health concerns: Infections can occur in humans and domestic animals who ingest raw or undercooked fish.

Wildlife population impacts: Eustrongylides ignotus have been reported to cause large epizootics of young birds in rookeries of colonial nesting species.

Management: Management is difficult due to persistence of the nematode eggs in the environment (over 2 years in experimental studies) and a prolonged infective period (over 1 year) of the intermediate hosts. Eutrophication and warm water temperatures promote the persistence of Eustrongylides sp. in the intermediate hosts and improvement in water quality may serve as a means of disease prevention.

References:

• Fenton H, McManamon R,  Howerth EW. 2018. Chapter 29: Anseriformes, Ciconiiformes, Charadriiformes, and Gruiformes. In: Pathology of Wildlife and Zoo Animals, Terio KA, McAloose D, St. Leger J, eds. Academic Press, San Diego, California, pp. 697–721.
• The Joint Pathology Center. 2008. Conference 16 Case 2. Eustrongylidosis in a great blue heron (Ardea herodias), https://www.askjpc.org/wsco/wsc_showcase2.php?id=c2tZV3N4dUxvSUxTS0dKQitJQVhmQT09 Accessed November 2022.
• PennVet News. 2021. Eustrongylidosis, https://www.vet.upenn.edu/about/news-room/news-stories/news-story-detail/eustrongylidosis Accessed November 2022.
• United States Geological Survey. 1999. Field manual of wildlife diseases: general field procedures and diseases of birds, https://pubs.usgs.gov/itr/1999/field_manual_of_wildlife_diseases.pdf#page=235 Accessed November 2022.