Genetic analysis of Enterobius vermicularis isolated from a chimpanzee with lethal hemorrhagic colitis and pathology of the associated lesions

Abstract

Human pinworms, Enterobius vermicularis, are normally recognized as minor pathogens. However, a fatal case of human pinworm infection has been reported in a nonhuman primate, a zoo reared chimpanzee. Here, we histopathologically examined the lesions in tissues from the deceased chimpanzee and genetically characterized the isolated worms to investigate the pathogenicity and determine the phylogeny. We identified ulcers deep in the submucosa where many parasites were found to have invaded the lamina propria mucosa or submucous tissue. An inflammatory reaction consisting mainly of neutrophils and lymphocytes but not eosinophils was observed around the parasites, and intense hemorrhage in the lamina propria was confirmed. The parasites were morphologically similar to E. vermicularis based on the shape of the copulatory spicules. Mitochondrial cytochrome c oxidase subunit 1 gene products were amplified from worm DNA by PCR and were genetically identified as E. vermicularis based on >98.7% similarity of partial sequences. Phylogenetic analysis revealed that the sequences clustered together with other chimpanzee E. vermicularis isolates in a group which has been referred to as type C and which differs from human isolates (type A). The samples were negative for bacterial pathogens and Entamoeba histolytica indicating that E. vermicularis could be pathogenic in chimpanzees. Phylogenetic clustering of the isolates indicated that the parasite may be host specific.

A pinworm's tale: The evolutionary history of Lemuricola (Protenterobius) nycticebi

“…In the case of primate pinworms, such congruence originates from both parasite- and host-specific attributes that would seem to provide a buffer against host switching and successful exploitation of novel hosts. For instance, even though humans and chimpanzees are closely related, infection with the human pinworm E. vermicularis is usually of mild pathogenicity in humans but often results in fatalities in chimpanzees (Murata et al, 2002; Yaguchi et al, 2014). The contrasting infection outcomes in these two closely related species suggests differences in host specificity.…”

Enterobiasis in a wild captured Indian Langur

“…Though the infection can be treated with antihelminthic drugs like mebendazole, pyrantel pamoate and albendazole (Remfry 1978) [9] , the circulation of the diseases continues even in developed countries. The disease has been identified in non-human primates like monkeys, gorillas (Gorilla gorilla), Chimpanzees (Pan troglodytes) (Yaguchi et al, 2014) [10] [1,7,5,4] from and others. The role of these non-human primates in transmitting the infection to humans has not been studied.…”

Natural pathology of the captive chimpanzee (Pan troglodytes): A 35‐year review

“…Except for a few short surveys of lesions and causes of mortality, an extensive documentation of chimpanzee lesions is lacking. Most of the published studies are in the form of case series that include pathology findings related to body systems (central nervous, cardiovascular, respiratory, gastrointestinal, urinary, and integumentary), etiologies (parasitic, degenerative, and neoplastic), and individual case reports . An extensive survey of the pathological lesions is lacking in literature.…”

“…integumentary(54,4.0%), endocrine (53, 3.9%), nervous (43, 3.2%), musculoskeletal (31, 2.3%), multisystemic lesions (20, 1.5%), and lesions involving the special senses (13, 1.0).…”