JPC SYSTEMIC PATHOLOGY
DIGESTIVE SYSTEM
September 2021
D-P15

 

Signalment (JPC #3048313):  A pigeon

 

HISTORY:  None

 

HISTOPATHOLOGIC DESCRIPTION:  Proventriculus:  Multifocally, 50% of mucosal (compound tubular) glands are markedly dilated up to 2.5 x 2 mm, lined by attenuated epithelium, and contain cross sections of plump adult female nematodes.  These expanded glands compress adjacent atrophic glands (compression atrophy) and elevate the overlying mucosa. These nematodes are 1.5-mm-diameter, have a 3 um wrinkled cuticle, and have a pseudocoelom that contains abundant homogenous, brightly eosinophilic fluid; polymyarian-coelomyarian musculature; a digestive tract lined by many uninucleate cuboidal cells with a prominent brush border that contains abundant brown pigment; a tripartite esophagus; uteri containing numerous 25 x 50 um, oval, thick shelled, embryonated spirurid eggs, and variably sized ovaries with ova. Occasionally, embryonated eggs have visible polar filaments.  Multifocally within the lamina propria, submucosa, muscularis, and serosa are several small aggregates of lymphocytes and rare heterophils. There is increased mucous production in the superficial mucosa.

 

Heart; esophagus; ventriculus; great vessel; air sac; peripheral nerve; and lung:  Essentially normal tissue.

 

MORPHOLOGIC DIAGNOSIS:  Proventriculus, : Glandular ectasia, multifocal, marked, with compression atrophy, intraglandular adult spirurid nematodes, and mild lymphocytic proventriculitis, etiology consistent with Tetrameres sp., pigeon (Columba livia), avian.

 

ETIOLOGIC DIAGNOSIS:  Proventricular tetrameriasis

 

CAUSE:  Tetrameres sp. (T. americana or T. fissispina)

 

GENERAL DISCUSSION:

• Proventricular spirurid nematode affecting numerous aquatic birds, particularly Anseriformes, Ardeiformes, Gruiformes, and Charadriiformes, and less commonly affecting land birds such as Passerines and Galliformes.
• These parasites have marked sexual dimorphism; males are small, white, and filiform and either found with females in the mucosal glands or free in the lumen of the proventriculus; females are large, blood red, and either spherical (globular in tissue section ‑ Tetrameres) or coiled (lobate in tissue section ‑ Microtetrameres) in the mucosal glands

 

PATHOGENESIS:

• Females suck blood and cause moderate to severe irritation/inflammation in the proventriculus of some avian hosts
• Necrosis and degeneration of proventricular mucosa, edema, leukocytosis, and extensive blood loss may occur

 

 

LIFE CYCLE:

• Females live in the proventricular glands; males live free in the lumen or on the mucosal surface and enter the glands only temporarily to copulate
• Tetrameres require an intermediate host (water crustaceans or insects [grasshopper, earthworms, or cockroach])
• Embryonated eggs pass in feces > develop in intermediate host (grasshopper, cockroach) > eaten by a bird > infective larvae mature in the proventriculus

 

TYPICAL CLINICAL FINDINGS:

• Vary from no clinical signs to anemia, diarrhea, emaciation, and death depending on the severity of infection and susceptibility of the host species
• Tetrameres americana causes no signs in bobwhite quail but can cause death in pigeons

 

TYPICAL GROSS FINDINGS:

• Bright red female worms are embedded in the proventricular glands and can be observed through the wall of the unopened gland
• May develop thickening (due to mucosal hyperplasia) of the proventricular wall that can obliterate the proventricular lumen in some hosts

 

TYPICAL LIGHT MICROSCOPIC FINDINGS:

• Distension of glands by female nematodes with compression of adjacent tissue
• Mucosal hyperplasia with heavy infection
• americana is usually associated with mild inflammation, while T. fissispina produces degeneration, edema, and extensive leukocyte infiltration
• Nematode characteristics:  Polymyarian/coelomyarian musculature; large stalked lateral cords; esophagus divided into anterior muscular and posterior glandular portions; large intestine lined by many uninucleate columnar to cuboidal cells with a prominent (long) microvillar border; distinguishing eosinophilic fluid in the pseudocoelom (feature of most Spirurids); and small, thick-shelled embryonated eggs (characteristic of Spirurids)

 

ADDITIONAL DIAGNOSTIC TESTS:

• Fecal examination can be performed, but eggs may be indistinguishable from other spirurids.

 

DIFFERENTIAL DIAGNOSIS: 

For nematodes in the proventriculus:

• Tetrameres sp.: Fat, spherical, blood-red worms in the wall of the proventriculus that distend the glands
• Microtetrameres sp.: Lobate, wide, coiled, blood red worms in the wall of the proventriculus  ( helix:  Russian and North American crows and pigeons)
• Cyrnea sp.: Spirurids, but lack the marked sexual dimorphism of the Tetramitidae; nonpathogenic; do not suck blood; do not attach to mucosa or live in glands 
  • C. pileata: Bobwhite quail
  • C. colini: Various North American gallinaceous birds
• Dispharynx nasuta: Lives on the mucosa of the proventriculus, esophagus, and rarely the intestines of various species of pigeons, chickens, turkeys, and guinea fowl worldwide; can cause severe ulceration with chronic diffuse fibrosis; most severe in young birds and the main cause of grouse disease in the USA
• Echinuria uncinata: In the esophagus, proventriculus, gizzard, and small intestine of the duck, goose, and swan; penetrate deep into the mucosa forming large nodules with caseous centers, which can obstruct the passage of food
• Gongylonema ingluvicola: mucosa of the crop and sometimes the esophagus and proventriculus of chicken, turkey, partridge, pheasant, and quail; burrows in the mucosa, which appear as white convoluted tracks

 

COMPARATIVE PATHOLOGY:

Tetrameres spp.:

• Tetrameres americana: Chicken, quail, turkey, guinea fowl, pigeons, ducks, and geese; mainly in the USA and South Africa
• T. fissispina: Most common in ducks and geese; rare in pigeons, chickens, turkeys, and other birds; worldwide distribution
• T. crami: North American ducks
• T. pattersoni: Only in bobwhite quail 

 

REFERENCES:

1. Fenton H, McManamon R, Howerth EW. Anseriformes, Ciconiiformes, Charadriiformes, and Gruiformes. In: Terio KA, McAloose D, St. Leger J, eds. Pathology of Wild Life and Zoo Animals. Cambrige, MA, Elseveir, 2018: 717.e5.
2. Gardiner CH, Poynton SL. In: An Atlas of Metazoan Parasites in Animal Tissues. Washington DC: Armed Forces Institute of Pathology; 1999:34.
3. Kinsella JM, Forrester DJ. Tetrameridosis. In: Atkinson CT, Thomas NJ, Hunter DB, eds. Parasitic Diseases of Wild Birds. Ames, IA: John Wiley & Sons; 2008:376-383.
4. McDougald LR. Internal Parasites. In: Swayne DE, ed. Diseases of Poultry. 13th ed. Ames, IA: John Wiley & Sons; 2013:1131-1132.
5. Schmidt GD, Roberts LS. Foundations of Parasitology. Louis, MO: Mosby; 1981: 501-511.
6. Urquhart GM, Armour J, Duncan JL, Dunn AM, Jennings FW. Veterinary Parasitology. 2nd ed. Oxford, UK: Blackwell Science Limited; 1996:85.

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