JPC SYSTEMIC PATHOLOGY

DIGESTIVE SYSTEM

October 2024

D-P12 (NP)

 

SLIDE A: Signalment (JPC #1699088): A chimpanzee (Pan troglodytes)

 

HISTORY: This animal lived for many years in a large southwestern zoo and died from disseminated tuberculosis. This was an incidental finding.

 

HISTOPATHOLOGIC DESCRIPTION: 

Colon: Circumferentially, there is mucosal erosion and a diffuse, marked decrease in the number of colonic crypts. The lamina propria is infiltrated and expanded by abundant inflammatory infiltrates composed of variably sized aggregates of lymphocytes, plasma cells, and eosinophils as well as edema that surround and separate remaining crypts. These inflammatory cells multifocally occasionally extend through the muscularis mucosa into the submucosa and surround submucosal vessels. Several submucosal arteries are lined by hypertrophied endothelial cells, with occasional transmigrating eosinophils within the tunica media. Within the colonic lumen, there are few cross and tangential sections of a 90-150 µm diameter nematode with a 5 µm thin cuticle with lateral alae, platymyarian-meromyarian musculature, a pseudocoelom, a digestive tract with a muscular esophagus with a triradiate lumen, and a male or female reproductive tract.

 

Small intestine: Multifocally many eosinophils, lymphocytes, and plasma cells expand the lamina propria and submucosa. Admixed with enterocytes are increased numbers of goblet cells (hyperplasia). There are longitudinal and cross-sections of nematodes as described above embedded at various depths within the mucosa and within the lumen.

 

MORPHOLOGIC DIAGNOSIS: Colon; small intestine: Colitis and enteritis, lymphoplasmacytic and eosinophilic, circumferential, moderate, with goblet cell hyperplasia and few Oxyurid nematodes, etiology consistent with Enterobius sp., chimpanzee (Pan troglodytes), nonhuman primate.

 

CAUSE: Enterobius sp.

 

ETIOLOGIC DIAGNOSIS: Intestinal enterobiasis

 

CONDITION: Pinworm infection

 

SLIDE B: Signalment (JPC #4203282-00): Adult male albino mouse

 

HISTORY: This animal presented for necropsy with a history of “damaged eye.” Gross findings included a moderate amount of adipose tissue, a closed right eye with mild red crusting on the eyelids, several 1-3 mm scabs and ulcers on the right side of the muzzle and nose, and a normal amount of ingesta within the digestive tract with formed feces in the colon. 

 

HISTOPATHOLOGIC DESCRIPTION: Colon: The lamina propria is multifocally infiltrated and expanded by lymphocytes and plasma cells, with fewer neutrophils and eosinophils admixed. There are increased numbers of goblet cells diffusely throughout the mucosa. Within the lumen, there are numerous longitudinal and cross sections of up to 2.2 mm by 200 µm adult nematodes with prominent lateral alae, a 5 µm thin eosinophilic cuticle, lateral chords, platymyarian-meromyarian musculature, a pseudocoelom, a digestive tract lined by cuboidal uninucleate cells that occasionally shows a triradiate lumen in cross-section, and often a male or female reproductive tract. 

 

Testicle and small intestine: No significant findings.

 

MORPHOLOGIC DIAGNOSIS: Colon: Colitis, lymphoplasmacytic, multifocal, mild, with goblet cell hyperplasia and numerous intraluminal oxyurid nematodes, mouse, rodent. 

 

CAUSE: Oxyurid nematodes 

 

ETIOLOGIC DIAGNOSIS: Intestinal oxyuridiasis

 

CONDITION: Pinworm infection

 

GENERAL DISCUSSION:

• Family Oxyuridae (pinworms)
• Oxyurids are among the most host specific of nematodes
  1. Enterobius anthropopitheci: Chimpanzees, prosimian primates
  2. Enterobius vermicularis: Human pinworm; can infect chimpazees, Old World monkeys, and great apes
  3. Trypanoxyuris and Oxyuronema species: New World monkeys
• Usually innocuous in the chimpanzee, although heavy infections are common due to coprophagic habits; serious and even fatal infections have been reported
• Pathogenicity may be related to severity of infection and immunological status of host

• Inhabits colon and cecum of nonhuman primates

 

LIFE CYCLE:

• Direct; fecal-oral infection
• Ingested embryonated eggs hatch in the small intestine and undergo two or more molts
• Adult Enterobius in the ileocecocolic region
• Gravid females migrate to the perianal skin and lay embryonated eggs; eggs become infectious within a few hours

 

PATHOGENESIS:

• Pinworms have been found within all layers of the intestine and in lymph nodes of the chimpanzee
• There is controversy over whether mucosal attachment of larvae or adults is a normal part of the life cycle, and whether Enterobius is able to penetrate normal tissues:
  • Heavy infections may cause ulcerative colitis, allowing larva and adults to migrate into the mucosa
  • Mechanical mucosal damage with secondary bacterial infection
  • Parasites invade tissue damaged by some other process
• Inflammation and necrosis may occur when aberrantly migrating larvae die

 

TYPICAL CLINICAL FINDINGS:

• Anal pruritus and irritation; causes self mutilation, restlessness, and aggression
• Chimpanzees with severe enterobiasis develop depression, anorexia, weight loss/emaciation, dehydration, and mild to profuse watery diarrhea; death may occur within one week of the onset of diarrhea

 

TYPICAL GROSS FINDINGS:

• Fatal infections in the chimpanzee are characterized by extensive ulcerative enterocolitis, peritonitis, necrogranulomatous mesenteric lymphadenitis, and possible ileocecal nodules
• Females (6-12mm x 0.3-0.6mm) often have long pointed tails and are generally larger than males (2-5mm x 0.1-0.2mm)

 

TYPICAL LIGHT MICROSCOPIC FINDINGS:

• In severe infections there is mucosal and submucosal necrosis
• Neutrophilic and lymphoplasmacytic inflammation
• Oxyurids have a thin cuticle with cervical or lateral triangular alae (lateral in Enterobius), platymyarian-type musculature, cuboidal uninucleate intestinal cells, and a prominent rhabditiform esophagus (corpus, isthmus, and bulb)
• Nematodes in all layers of the intestine
• Ellipsoid, asymmetrical eggs, 50-60µm long; +/- embryonated when laid

 

ADDITIONAL DIAGNOSIC TESTS:

• Adult worms emerging from the anus 
• Enterobius eggs rarely passed in the feces; not detected by fecal flotation or direct fecal examination
• Antemortem diagnosis is based on visualization of adults emerging from the anus, or from identification of eggs in perianal swabs or cellophane tape preparations.

 

DIFFERENTIAL DIAGNOSIS:

• Prosthenorchis elegans: Acanthocephalid, causes pyogranulomatous enteritis with parasites
• Oesophagostomum sp.: Causes intramural nodules in the cecum, colon, and adjacent mesentery of wild-caught monkeys

 

COMPARATIVE PATHOLOGY:

• Pinworms do NOT infect the dog and cat
• Enterobius anthropopitheci: Nonhuman primates, chimpanzees, prosimian primates
• Enterobius vermicularis: Old World monkeys, great apes; associated with appendicitis, intestinal abscesses, infections of the female reproductive tract, peritonitis, and nephritis in captive chimpanzees; public health concern
• Oxyuris equi: Most common pinworm in domestic animals; distal intestine, with rectal pruritus in horses
• Skrjabinema ovis: Sheep & goats
• Passalurus ambiguus: Ceca of rabbit; heavy infections cause impaired weight gains, poor breeding performance, and death
• Syphacia obvelata, Aspicularis tetraptera, Syphacia muris: Cecum and colon of rats
• Syphacia obvelata, Aspicularis tetraptera: Common in laboratory mouse; heavy infections associated with rectal prolapse, intussusception, fecal impaction, and diarrhea
• Amphibians: Gyrinicola spp. considered to be beneficial commensal organisms

 

REFERENCES:

1. Barthold SW, Griffey SM, Percy DH. Pathology of Laboratory Rodents and Rabbits. 4th ed. Ames, Iowa: Blackwell Publishing; 2016: 84-85,152,190,205,301.
2. Gardiner CH, Poynton SL. An Atlas of Metazoan Parasites in Animal Tissues. Washington, D.C: Armed Institute of Pathology; 2006:5,17-18.
3. McAloose D, Stalis IH. Ch. 13 Prosimians In: Terio K, McAloose D, Leger J, eds. Pathology of Wildlife and Zoo Animals, San Diego, CA: Elsevier 2018:339.e16-e17.
4. Lowenstine LJ, McManamon R, Terio KA. Apes. In: Terio KA, McAloose D, St. Leger J, eds. Pathology of Wildlife and Zoo Animals. London, UK: Academic Press; 2018:397. 
5. Pessier AP. Amphibia. In: Terio KA, McAloose D, St. Leger J, eds. Pathology of Wildlife and Zoo Animals. London, UK: Academic Press; 2018:942. 
6. Radostits OM, Gray CC, Hinchcliff KW, Constable PD. Veterinary Medicine. 10th ed. Philadelphia, PA: Saunders Elselvier: 2007:1562.
7. Rensing, KM, Lowenstine, LJ. New World and Old World Monkeys. In: Terio K, McAloose D, Leger J, eds. Pathology of Wildlife and Zoo Animals, San Diego, CA: Elsevier 2018:368.e9, 403e18.
8. Spagnoli ST, Gelberg HB. Alimentary System and the Peritoneum, Omentum, Mesentery, and Peritoneal Cavity. In: Zachary JF, ed. Pathologic Basis of Veterinary Disease. 7th ed. St. Louis, MO: Elsevier; 2022:458. 
9. Strait K, Else JG, Eberhard ML. Parasitic diseases of nonhuman primates. In: Abee CR, Mansfield K, Tardiff S, Morris T, eds. Nonhuman Primates in Biomedical Research. Vol. 2. 2nd ed. San Diego, CA: Elselvier; 2012:231.

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