Signalment:  

Adult, female Northern bobwhite (Colinus virginianus [no subsp.])Found dead with no premonitory signs

Gross Description:  

At gross necropsy the animal was extremely thin with no visible fat stores and severe pectoral muscle atrophy. The proventriculus was markedly distended and filled with a large amount of thick, off-white, mucoid material. The proventricular walls were severely thickened, particularly the mucosa, which was 3 mm thick, yellow white and gelatinous. Numerous short, white, coiled nematode parasites were present within and adhered to the mucosal lining of the proventriculus and the proximal ventriculus. There was a 0.7 cm diameter region of the proventricular mucosa that was thinner than the adjacent mucosa, and dark red. 

Histopathologic Description:

The section submitted is from the proventriculus near the junction with the esophagus. The superficial mucosa varies from thickened and hyperplastic (Fig. 2-1) in some sections to severely eroded in other sections. In areas of erosion there is severe necrosis of the superficial portion of the glands with fibrin deposition and hemorrhage. Both the superficial and deep portions of the proventricular glands are distended by a mixture of mucus and numerous Spirurid nematode parasites. In cross section, the nematodes vary from 200 to 600 um in diameter. All have an approximately 5 to 15 um thick cuticle, which varies from smooth to ridged, a thick layer of coelomyarian musculature, a predominantly glandular esophagus, and a prominent intestinal tract composed of cuboidal to columnar cells with a brush border. The coelom contains a small amount of eosinophilic fluid (Fig. 2-2). Female nematodes typically demonstrate a distended uterus containing numerous small (20 by 40 um), thick shelled, embryonated eggs (Fig. 2-3). Within the lamina propria there is a diffuse infiltrate of eosinophils with smaller numbers of lymphocytes and plasma cells. Dilated glands have an attenuated epithelial lining and when free of nematodes contain a large amount of mucus and sloughed necrotic epithelial cells. A thick layer of mucus admixed with similar quantities of epithelial cells and eosinophils covers the mucosal surface. Scattered colonies of mixed bacteria are present within the mucus.

Morphologic Diagnosis:  

Proventriculus: Proventriculitis, erosive to proliferative, eosinophilic, lymphocytic, plasmacytic, diffuse, moderate to severe with Spirurid nematodes (Dispharynx nasuta)

Lab Results:  

Multiple nematodes were collected and examined microscopically. The nematodes were white, between 4 and 7 mm long, less than 1 mm in diameter and typically coiled. On microscopy 4 characteristic wavy cuticular ornaments (cordons) extended from the base of the lips posteriorly. Myriad 20 x 40 micron embryonated eggs were scattered throughout the background. The parasite was identified as Dispharynx nasuta at the time of necropsy and later confirmed by the Cornell University, College of Veterinary Medicine, Animal Health Diagnostic Center.

Condition:  

Dyspharynx nasuta

Contributor Comment:  

Dispharynx nasuta (syn. Dispharynx (Acuaria) spiralis), also known as the -�-�proventricular worm, is a spirurid nematode parasite of the proventriculus of many passerine, columbiform and free ranging gallinaceous birds.(5,11) It has been identified in a variety of game birds (ruffed grouse, blue grouse, American woodcock) including the bobwhite quail.(5,7,8) There is a single case report of infection in a captive princess parrot.(11) The highest prevalence and levels of infection are seen in juvenile birds, with infection occurring by 3 to 4 days of age in regions of high incidence.(5,7)

The life cycle of Dispharynx is indirect utilizing an intermediate terrestrial isopod host. Adult female D. nasuta pass embryonated eggs into the lumen of the proventriculus, which are later shed in the feces.(11) The eggs are consumed by the intermediate host, wood lice (Armadillidium vulgare) or sow bugs (Porcellio scaber), in which the larvae subsequently hatch and penetrate the host tissues. First stage larvae (L1) develop into the infective third stage (L3) within 26 days. The third stage larvae (L3) can survive in the infected intermediate host for up to 6 months. Once the intermediate host is consumed by a susceptible bird the third stage larvae (L3) further develop, reaching sexual maturity in 27 days.(7)

Sexually mature adults primarily infect the proventriculus, though in severe cases they can also infect the adjacent esophagus and ventriculus. The nematodes attach by their anterior end to the mucosal epithelial cells initially causing ulceration at the site of attachment. In most avian species these worms cause only a mild nodular reaction in the mucosa and a small amount of inflammation. However in some species (American wood cock, ruffed grouse, blue grouse) D. nasuta acts as a primary pathogen.(5,7) When present in large numbers (10 or more), the infection causes severe hyperplasia of the proventricular glands. Associated with the glandular proliferation is an increase in mucus production, as well as excessive sloughing of mucosal epithelial cells. As a result, the lumen of the proventriculus becomes distended by a thick, white, coagulum of mucus and sloughed cells which creates a functional obstruction of the proventriculus and secondary starvation.(5,7)

Diagnosis in this case was made based on the characteristic proventricular lesion, egg and adult worm identification. As stated previously, the significance of this parasite is variable. In most birds this nematode is an incidental finding. However in some species, particularly the ruffed grouse and blue grouse, these organisms are believed to be a significant cause of mortality and decline in wild populations. While not typically considered a primary pathogen of free ranging bobwhites, significant mortality has been seen in cage-reared animals.(5,7,8)

JPC Diagnosis:  

1. Proventriculus: Proventriculitis, proliferative and heterophilic, diffuse, marked with glandular ectasia and adult spirurids
2. Serosa, adipose tissue: Atrophy, diffuse, moderate

Conference Comment:  

Spirurid nematodes often have several distinguishing characteristics in histologic section. Several types of spirurids have cuticular ornamentations around the buccal cavity varying from spines to cords to collars. Eosinophilic fluid is found in the body cavity and is a distinguishing characteristic of this group of nematodes. Lateral cords can be extremely large in size and are often vacuolated. Most adult females in this group also produce thick shelled, embryonated eggs. Other examples of spirurids in domestic animals include: Physaloptera sp., Gonnglyonema sp., Draschia sp., Spirocerca sp., Thelazia sp.(4)

In a retrospective study done by Drs. Raymond, Miller, and Garner it was found that in two cases infection with D. nasuta, also known as adenomatous proliferative proventriculitis (APP), the lesions progressed to proventricular adenocarcinoma.(9) In humans and domestic animals, several parasites have been associated with subsequent neoplasia. A brief, non-comprehensive list is included.

Spirocerca lupi	Esophageal sarcoma in dogs
Opisthorchid flukes	Cholangiocarcinoma in cats and man
Cysticercus fasciolaris	Hepatic sarcoma in rats
Clonorchis sinensis	Cholangiocarcinoma in cats and man
Schistosoma haematobium	Carcinoma in bladder of humans
Trichosomoides crassicauda	Papillomas in urothelium in rats

References:

1. Bolette DP: Dispharynxiasis in a captive princess parrot. Journal of Wildlife Diseases 34:390-391, 1998
2. Brown CC, Baker DC, Barker IK: The alimentary system. In: Jubb, Kennedy and Palmers Pathology of Domestic Animals, ed. Maxie MG, 5th ed., vol. 2, p. 40-41, 256. Saunders Elsevier, Philadelphia, PA, 2007
3. Epstein JI: The lower urinary tract and male genital system. In: Robbins and Cotran Pathologic Basis of Disease, eds. V. Kumar, A. K. Abbas, N. Fausto, 7th ed., pp. 1032, Elsiever, Inc., Philadelphia, PA, 2005
4. Gardiner CH, Poynton SL: In: An Atlas of Metazoan Parasites in Animal Tissues, 2nd ed., pp. 30-34. Armed Forces Institute of Pathology, Washington, DC 1998
5. Goble FC, Kutz HL: The genus dispharynx (Nematoda: Acuariidae) in galliform and passeriform birds. Journal of Parasitology 31:323-331, 1945
6. Percy DH, Barthold SW: Pathology of Laboratory Rodents and Rabbits, 3rd ed., pp.160. Blackwell Publishing, Ames, Iowa, 2007
7. Proventricular or Stomach Worm. http://www.michigan.gov/dnr/0,1607,7-153-10370_12150_12220-27255--,00.htm
8. Purvis JR, Peterson MJ, Lichtenfels JR, Silvy NJ: Northern bobwhites as disease indicators for the endangered Attwaters prairie chicken. Journal of Wildlife Diseases 34:348-354
9. Raymond JT, Miller C, Garner MM: Adenomatous proliferative proventriculitis (APP) in birds. Journal Proceedings, AAZV Conference, Milwaukee, WI, 2002
10. Stalker MJ, Hayes MA: Liver and biliary system. In: Jubb, Kennedy and Palmers Pathology of Domestic Animals, ed. Maxie MG, 5th ed., vol. 2, pp.363. Saunders Elsevier, Philadelphia, PA, 2007
11. Urquhart GM, Armour J, Duncan JL, Dunn AM, Jennings FW: Veterinary Parasitology, pp.82 83, Churchill Livingstone Inc., 1994

Click the slide to view.

---

2-1. Proventriculus, quail. 

2-2. Proventriculus, quail.

2-3. Proventriculus, quail

---