JPC SYSTEMIC PATHOLOGY

DIGESTIVE SYSTEM

October 2024

D-P16 (NP)

 

SIGNALMENT (JPC# 1852297): Adult wild-caught female Cebus monkey (Cebus sp.)

 

HISTORY: Incidental necropsy finding with numerous 0.5 to 2.5 cm diameter grayish-tan nodules on the serosal surface of the duodenum and jejunum

 

HISTOPATHOLOGIC DESCRIPTION: Small intestine: Markedly expanding and compressing the tunica muscularis and elevating the overlying serosa or expanding the adjacent mesenteric adipose tissue are multifocal, 4 to 5 mm diameter, well-demarcated granulomas characterized by a discontinuous fibrous capsule surrounding a rim of numerous epithelioid macrophages, eosinophils, degenerate and viable neutrophils, and few lymphocytes and plasma cells, which are centered on and surround multiple cross and tangential sections of adult nematodes and eggs, fibrin, eosinophilic homogenous material, and necrotic debris. Nematodes are up to 120 µm in diameter, have a 5 µm thick eosinophilic hyaline cuticle with evenly spaced longitudinal cuticular ridges, a pseudocoelom, platymyarian-meromyarian musculature, a prominent digestive tract lined by few multinucleate cells with a low brush border, and a female or male reproductive tract. Eggs are 30-50 µm in diameter, thin-shelled, and contain morula or larvae. Lymphocytes, plasma cells, eosinophils, and occasionally hemosiderin-laden macrophages extend into the adjacent serosa, submucosa, and into the lamina propria. The tunica muscularis adjacent to the granulomas is often lost and replaced by fibrous connective tissue. The majority of the intestinal mucosa is autolytic, but the lamina propria contains mildly increased numbers of lymphocytes and plasma cells.

 

MORPHOLOGIC DIAGNOSIS: Small intestine, serosa and mesentery: Granulomas, eosinophilic, chronic, multifocal, moderate, with multiple adult trichostrongyle nematodes and eggs, Cebus monkey (Cebus sp.), nonhuman primate.

 

ETIOLOGY: Molineus torulosus

 

ETIOLOGIC DIAGNOSIS: Enteric trichostrongyliasis

 

GENERAL DISCUSSION:

• Class Secernentea, order Strongylida, suborder Trichostrongylida

• Molineus sp. are small, slender, pale red nematodes of the upper digestive tract, pylorus, and occasionally pancreas and mesentery of nonhuman primates; these nematodes are not found in the terminal jejunum or ileum; found lying on the mucosa, not attached
• Molineus torulosus is the only pathogenic species; causes hemorrhagic or nodular ulcerative enteritis

• Unknown life cycle and transmission. 

 

PATHOGENESIS:

• Infective L3 penetrates mucosal epithelium and burrows into the submucosa > larvae mature and deposit eggs > formation of submucosal granulomas > eggs are expelled through channels from granuloma into the intestinal lumen
• Invasion of the host’s vascular system > fibrin thrombi or direct penetration or dissemination via portal vein > pancreatic ducts > chronic pancreatitis

 

TYPICAL CLINICAL FINDINGS: 

 

TYPICAL GROSS FINDINGS:

• Duodenum and proximal jejunum; occasionally pancreas

• Chronic pancreatitis associated with worms and eggs in inflamed pancreatic ducts

• 2-6 mm gray-green/black-brown serosal nodules, marbled on cut surface

• Nodules communicate with the lumen by 1 mm brownish-red ulcers and often contain a mass of sexually mature, 1 cm long, hair-like worms 

• Mesenteric lymph nodes enlarged and reddish

TYPICAL LIGHT MICROSCOPIC FINDINGS:

• Progression of three types of cysts:

• Newly formed cysts with predominately neutrophils; numerous nematodes
• Advanced cysts with fewer neutrophils and more macrophages, eosinophils, and lymphocytes (eosinophilic granuloma); fibrotic strands penetrate cyst lumen; fewer nematodes
• Chronic cyst with almost complete replacement by fibrosis; no nematodes

• Parasitic granulomas associated with large mesenteric blood vessels and vessels at the periphery of the granuloma; nematodes and eggs possibly intravascular within fibrin thrombi 
• Neutrophilic and lymphocytic periductular pancreatitis with intraductular nematodes and eggs; chronic – pancreatic fibrosis 
• Subacute mesenteric and pancreatic lymphadenitis may be present
• Molineus torulosus has the following characteristics: Conspicuous external longitudinal ridges projecting from the cuticle; platymyarian-meromyarian musculature; intestine composed of few multinucleate cells with shorter, thinner microvillar layer and fewer nuclei than strongylids; large paired excretory gland cells; copulatory bursa in males

DIFFERENTIAL DIAGNOSIS:

• Oesophagostomum sp. (D-P29): Cause serosal nodules predominantly in the colon of Old World monkeys; very rare in New World species; histologically only larvae present in nodules
• Nochtia nochti (D-P14): Trichostrongyle; produces papillomatous mucosal nodules in the stomach of Old World monkeys; cuticular ridges external to the lateral cords fused and divergent from one another, a unique feature of Nochtia 
• Prosthenorchis sp. (D-P09): Acanthocephalan; produces serosal nodules in the large intestine, occasionally the terminal ileum or ileocecal region, of New World monkeys; attached to the mucosal surface; lemnisci and a thick hypodermis are unique microscopic features
• Intramural granulomas caused by schistosomes may appear as intestinal nodules, but can be easily differentiated histologically
• Pancreatic lesions must be differentiated from similar lesions caused by other nematodes such as the spirurid Trichospirura leptostoma (D-P26)

REFERENCES:

1. Gardiner C.H., Fayer R., Dubey J.P., An Atlas of Metazoan Parasites in Tissue Section: Second Edition. Washington D.C.: American Registry of Pathology; 1998: 25
2. Matz-Rensing K, Lowenstine LJ. New World and Old World Monkeys. In: Terio KA, McAloose D, St. Leger J, eds. Pathology of Wildlife and Zoo Animals. London, UK: Academic Press; 2018:368.e9 
3. Miguel MP, Duarte SC, Santos AS. Mortality of Cebus apella by Molineus torulosus parasitism in midwestern Brazil. Acta Scientiae Veterinariae. 2013; 41(1):1-4.
4. Strait K, Else JG, Eberhard ML. Parasitic Diseases of Nonhuman Primates. In: Abee CR, Mansfield K, Tardif S, Morris T. Nonhuman Primates in Biomedical Research: Volume 2: Diseases. 2^nd ed. San Diego, CA: Elsevier; 2012: 233 – 234.

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