JPC SYSTEMIC PATHOLOGY
DIGESTIVE SYSTEM
September 2021
D-P09

Signalment (JPC #1640180):  Moustached tamarin (Saguinus mystax)

 

HISTORY:  None

 

HISTOPATHOLOGIC DESCRIPTION:  Ileum, two sections: Multifocally, expanding the serosa in one section, and disrupting and expanding the submucosa, tunica muscularis, and serosa and elevating the overlying ulcerated mucosa in the other section are multiple pyogranulomas centered on a cross section of an adult acanthocephalid and/or a central area of eosinophilic cellular and karyorrhectic necrotic debris and numerous viable and necrotic neutrophils and eosinophils. The adult acanthocephalid is 1 X 1.75 mm in diameter, has a thin, ridged, outer cuticle and a thick hypodermis (up to 150 um) composed of an outer felted layer and cross fibers containing lacunae, outer circular and inner longitudinal muscle layers, and a pseudocoelom containing lemnisci with compressor muscles.  The acanthacephalid is surrounded by a thin layer of degenerate neutrophils and eosinophils.  The pyogranulomas are further surrounded by a zone of epithelioid macrophages, neutrophils, eosinophils, lymphocytes, and plasma cells that are enmeshed in thick, concentric bands of mature fibrous connective tissue and fibroblasts. Fibrous connective tissue within the submucosa is multifocally, mildly separated by increased clear space (edema) and a mixed population of inflammatory cells.  A partial cross section of an adult acanthocephalid is located on the luminal aspect of the mucosa associated with a focal area of mucosal ulceration characterized by loss and replacement of enterocytes by karyorrhectic and cellular necrotic debris and degenerate neutrophils. 

 

MORPHOLOGIC DIAGNOSIS:  Ileum:  Enteritis, pyogranulomatous, chronic, multifocal, moderate, with focal ulceration, and adult acanthocephalid parasites, moustached tamarin (Saguinus mystax), nonhuman primate.

 

ETIOLOGIC DIAGNOSIS:  Intestinal acanthocephaliasis

 

CAUSE:  Prosthenorchis elegans

 

GENERAL DISCUSSION:

• Phylum Acanthocephala includes parasites in the genera of Prosthenorchis, Macracanthorhynchus, Moniliformis, and Oncicola, which are intestinal parasites of vertebrates with various invertebrates (crustaceans, annelids and larval insects) as intermediate hosts
• Most frequently associated with two parasites in the genus Prosthenorchis:
  • elegans – cecum or colon
  • spirula – terminal ileum
• Reported in a variety of New World monkeys, but Prosimians, Old World primates, and great apes can become infected under laboratory or captive conditions
• elegans is most common than P. spirula
• Intermediate host: Several species of cockroaches and certain beetles
• Acanthocephala characteristics:
• No digestive tract
• Hypodermis thicker than muscle layer
• Lacunar channels
• Proboscis and lemnisci

 

PATHOGENESIS:

• Ulcers and pyogranulomas form around the proboscis embedded in the gut wall
• Deep ulcers may perforate the bowel causing peritonitis
• Diarrhea may result from hypermotility and interference with the absorptive function of the large intestine
• Large numbers may cause complete obstruction of the bowel
• Most often the parasite creates lesions that allow for the establishment of secondary pathogens that are the cause of debilitation and death

 

LIFE CYCLE:

• Indirect life cycle: Eggs are passed in the feces of monkeys and must be ingested by a cockroach or beetle (intermediate host; varies by species) to develop> larvae hatch, develop, and encyst in the intermediate host> this stage is infective to the definitive host
• Adults have a retractable spiny proboscis used to attach itself to intestinal wall
  

TYPICAL CLINICAL FINDINGS:

• Fecal smear or sedimentation (fecal flotation not effective): Brown, thick double-walled embryonated eggs; hook-laden proboscis evident in adults passed in feces
• Can have no overt signs of disease
• Chronic course – diarrhea, normal appetite, weakness, progressive emaciation, debilitation, and death; all of these symptoms may be due to secondary infection
• Large parasite burden can lead to obstruction +/- scant amounts of hemorrhagic feces
• Acute course – perforation of intestinal wall by the proboscis leading to acute abdominal pain, peritonitis, and death

 

TYPICAL GROSS FINDINGS:

• Firm white nodules several millimeters in diameter in the terminal ileum, cecum, or colon; often visible from the serosal surface
• Multifocal, sharply delineated, 1-2mm deep intestinal ulcers, rimmed by connective tissue, with or without parasite attached
• Adults attached to the mucosa of the ileum, cecum, and colon are pathognomonic
• With perforation – peritonitis, fibrinous tags, adhesions, or abscesses +/- parasites free in peritoneal cavity
• Severe infections may completely occlude the lumen; can cause intussusception

 

TYPICAL LIGHT MICROSCOPIC FINDINGS:

• Morphology of acanthocephalids:
• Cylindrical pseudocoelomates; separate sexes
• Retractable proboscis armed with rows of hooks (spines)
• Hypodermis thicker than muscle layers; consists of two layers (felted layer and cross fibers containing lacunar channels)
• Two layers of somatic muscles: Outer circular and inner longitudinal
• Absent digestive tract (nutrients absorbed through thin cuticle)
• Lemnisci with compressor muscles (may function in proboscis extrusion)
• Prosthenorchis elegans:
• Females up to 50 mm long, males 18-25 mm long; trunk transversely wrinkled, not pseudosegmented; narrow neck with 6 spiral rows of 5-7 curved hooks
• Anterior end has a distinctive collar with 18-20 festoons (not in spirula)
• Eggs: Brown, double-walled shell, 42X65 um; central embryo with a central mass containing numerous nuclei
• Ileum, cecum, and colon with numerous deep ulcers containing adult parasites with a hook-laden proboscis embedded deep in the intestinal wall
• Ulcers extend into submucosa and tunica muscularis

 

DIFFERENTIAL DIAGNOSIS:

• Intramural nodules in New World monkeys:
  • Prosthenorchis spirula: Acanthecephalid, lacks a collar
  • Molineus torulosus: Strongylid nematode, characteristic strongyle intestine
• Intramural nodules in Old World monkeys:
  • Oesophagostomum (nematode): Adults extremely small; totally embedded in the parasitic nodule; eggs easily distinguishable from Prosthenorchis sp. in that they are not double shelled

 

COMPARATIVE PATHOLOGY:

• In captivity, bush babies, lemurs, pig-tailed macaques, gibbons, and chimpanzees may become infected if housed in close proximity with infected animals
• Smaller acanthocephalans:
• Polymorphus and Filicolis sp.: Waterfowl and fishes; intermediate host is crustacean; lesions similar to Prosthenorchis in NHP
• Other acanthocephalans that parasitize mammals:
• Moniliformis moniliformis: Wild rodents and great apes; cockroach intermediate host; very long (up to 32 cm); pseudosegmented (easy to misdiagnose as a cestode); no distinctive scalloped collar in the neck region
• Macracanthorhynchus hirudinaceus (thorny-headed worm of swine): Wild and domestic swine; dung beetle intermediate host; affects small intestine; penetrates to tunica muscularis and may cause peritonitis; granulomatous nodule forms at attachment site, called strawberry mark
• Macracanthorhynchus catalinum and ingens: Foxes, wolves, badgers, skunk, raccoons, mink, moles, occasionally the dog
• Oncicola canis: Dog, coyote, domestic cat, lynx, bobcat; arthropod intermediate host; armadillo paratenic host; affects small intestine; rarely causes disease
• Oncicola campanulutus: Domestic cats
• Unknown acanthocephalan causing hepatic abscess and granulomatous myositis reported in adult bush baby

 

REFERENCES:

1. Gardiner CH, Poynton SL. An Atlas of Metazoan Parasites in Animal Tissues, American Registry of Pathology. Washington, DC, 1999:44-45.
2. Matz-Rensing K, Lownestine LJ. New World and Old World Monkeys. In: Terio KA, McAloose D, St. Leger J, ed. Pathology of Wildlife and Zoo Animals, Cambridge, MA Academic Press; 2018: 368.
3. Strait K, Else JG, Eberhard ML. Parasitic disease of nonhuman primates. In: Abee CR, Mansfield K, Tardif S, Morris T, eds. Nonhuman Primates in Biomedical Research. Vol 2. Diseases. 2nd ed. San Diego, CA: Elsevier, Inc. 2012: 258-260.
4. Uzal FA, Plattner BL, Hostetter JM. Alimentary system. In: Maxie MG, ed. Jubb, Kennedy and Palmer’s Pathology of Domestic Animals. Vol 2. 6th ed. St. Louis, MO: Elsevier Ltd; 2016:116, 227.

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