JPC SYSTEMIC PATHOLOGY
ENDOCRINE SYSTEM
February 2022
E-P02 (NP)

Signalment (JPC #1783252):  6-year-old cynomolgus macaque (Macaca fascicularis)

HISTORY:  Incidental finding

HISTOPATHOLOGIC DESCRIPTION:  Adipose tissue, periadrenal:  Expanding the periadrenal adipose tissue are two cross-sections of a 2 x 1.5 mm degenerate pentastome nymph with a 5 um thick chitinous cuticle that contains pit-like, sclerotized openings to skin glands, a pseudosegmented body wall, prominent body cavity, metamerically arranged (i.e arranged in regular segments) striated muscle, numerous acidophilic glands that surround the intestine and a digestive tract with villi lined by columnar epithelium.  The pentastome cross sections are surrounded by a 7 um layer of amorphous, eosinophilic material that contains sclerotized openings (previous molt) and a small amount of hemorrhage, fibrin, and edema.

Adrenal gland:  No significant findings.

MORPHOLOGIC DIAGNOSIS:  Adipose tissue, periadrenal:  Pentastome nymph, with mild hemorrhage, cynomolgus monkey (Macaca fascicularis), nonhuman primate.

ETIOLOGIC DIAGNOSIS:  Periadrenal pentastomiasis

CAUSE:  Armillifer armillatus (most likely)

GENERAL DISCUSSION:

• Pentastomes, often called tongue worms, are highly specialized crustaceans and are usually incidental postmortem findings of little pathogenic significance
• Pentastomes have two pairs of hooks surrounding the mouth; this led early researches to believe they had five ("penta") mouths ("stoma")
• Parasitic in all stages of their life cycle
• Armillifer armillatus occurs naturally only in tropical Africa
• Adults infect the respiratory tracts of large African snakes (pythons, Bitis vipers)
• Nymphs are common in macaques and other Old World monkeys (particularly wild-caught), prosimians, and great apes, and in other species such as cattle, swine, and humans

PATHOGENESIS:

• Nymphs encyst in the peritoneal cavity or beneath the liver capsule; usually cause little or no inflammation
• Migrating nymphs cause mild traumatic tissue damage and hemorrhage with infiltration of eosinophils, macrophages, and lymphocytes; peritonitis is rare
• Dead nymphs evoke a granulomatous response

LIFE CYCLE:

• Indirect
• Intermediate host (IH) infected by eating food contaminated by snake feces or saliva that contains infective eggs > larvae hatch in the IH’s gut > burrow into intestinal wall > travel through bloodstream or body cavity to the viscera or peritoneum > lose appendages > encyst and become a mature nymph
• Definitive host (DH) infected by eating IH containing nymphs > mature to adult > female deposits thin-shelled eggs containing infective larvae with clawed legs

TYPICAL CLINICAL FINDINGS:

• Usually asymptomatic
• Eggs are large (100-200 um) with a thin external shell that contains what appears to be a developing mite
• It is difficult to determine if the egg is from a pentostome or an ingested mite egg
• Within the egg, pentastomes have 4-6 small claws which allows differentiation from a mite

TYPICAL GROSS FINDINGS:

• Nymphs: C-shaped with coiling and pseudosegmentation; white and legless; 13-23 mm long
• Adults: Resemble nymphs, but are larger; cylindrical, annulated organism in the lungs of snakes with little to no tissue reaction

TYPICAL LIGHT MICROSCOPIC FINDINGS:

• Encysted parasite with little to no inflammation
• Nymph migration can cause necrosis, hemorrhage, and eosinophilic and mononuclear inflammation; dead nymphs evoke granulomatous inflammation
• Parasite features
• Pseudosegmented body
• Striated, metamerically arranged musculature
• Acidophilic glands that border the intestine
• Cuticle with sclerotized pit-like openings (unique feature of pentastomes) in body wall that are associated with production of new cuticle during molts
• Intestine with numerous villi

DIFFERENTIAL DIAGNOSIS:

Other pentastomes that infect nonhuman primates:

• Linguatula serrata
• Adults in the nasal passages of dogs and other canids, rarely domestic farm animals and humans; may cause catarrhal rhinitis and epistaxis in canids
• Nymphs in the mesenteric lymph nodes and viscera of herbivorous mammals and Old World and New World monkeys
• Porocephalus clavatus
• Adults in respiratory tract of snakes
• Nymphs common in wild-caught tamarins and in marmosets, deer mice, and cotton rats
• In nonhuman primates, nymphs encyst in many tissues, including liver, lung, peritoneum, and meninges, but cause little or no inflammatory reaction
• In rodents, nymphs encyst in viscera and produce few or no lesions
• Porocephalus subulifer: Adults in respiratory tract of snakes; encyst in the viscera of prosimians and Old World monkeys
• Porocephalus crotali: Adults in respiratory tract of snakes; encyst in the peritoneal cavity of New World monkeys
• Gigliolella brumpti: Adults in respiratory tract of snakes; encyst in the mesentery of prosimians and Old World monkeys
• Armillifer moniliformis: Adults in respiratory tract of snakes; encyst in the viscera and peritoneal cavity of Old World monkeys
• Nephridiacanthus: Adults in respiratory tract of snakes; encyst in the rectal wall of Old World monkeys

COMPARATIVE PATHOLOGY:

Armillifer armillatus in other species:

• Recent report of visceral pentastomiasis (Armillifer armillatus) in a striped hyena (Dechkajorn, Parasitol Int. 2016)

Other pentastomes:

• Reighardia : Adults in the air sacs of gulls and terns
• Raillietielia: Ophidians (snakes), lacertilians (lizards) and birds; may have direct life cycle
• Leiperia , Sebekia sp. and Subtriquetra sp.: Adults in crocodiles and alligators; nymphs in various fish

REFERENCES:

1. Bowman DD. Diagnostic parasitology. In: Bowman DD, ed. Georgis’ Parasitology for Veterinarians. St. Louis, MO: Elsevier; 2014:337.
2. Caswell JL, Williams KJ. Respiratory system. In: Maxie MG, ed. Jubb, Kennedy, and Palmer’s Pathology of Domestic Animals. Vol 2. 6th ed. St. Louis: Elsevier; 2016:585.
3. Dechkajorn S, Nomsiri R, Boonsri K, et al. Visceral pentastomiasis caused by Armillifer armillatus in a captive striped hyena (Hyaena hyaena) in Chiang Mai Night Safari, Thailand. Parasitol Int. 2016;65(1):58-61.
4. Eberhard ML. Histopathologic diagnosis. In: Bowman DD, ed. Georgis’ Parasitology for Veterinarians. St. Louis, MO: Elsevier; 2014:401-402.
5. Flynn RJ. Pentastomids. In: Flynn RJ, ed. Parasites of Laboratory Animals. Ames: The Iowa State University Press;1973:493-499.
6. Gardiner CH, Poynton SL. Morphological characteristics of pentastomes in tissue section. In: Gardiner CH, Poynton SL, ed. An Atlas of Metazoan Parasites in Animal Tissues. Washington, D.C; Armed Forces Institute of Pathology; 1999:59-60.
7. Strait K, Else JG, Eberhard ML. Parasitic diseases of nonhuman primates. In: Abee CR, Mansfield K, Tardif S, Morris T, eds. Nonhuman Primates in Biomedical Research: Diseases. Vol. 2. 2nd ed. San Diego: Academic Press; 2012:271-272.
8. Tappe D, Meyer M, Oesterlein A. Transmission of Armillifer armillatus ova at snake farm, The Gambia, West Africa. Emerg Infect Dis. 2011;17(2):251-254.

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