Vector-borne transmission of Trypanosoma cruzi among captive Neotropical primates in a Brazilian zoo

Abstract

BackgroundNeotropical primates are important sylvatic hosts of Trypanosoma cruzi, the etiological agent of Chagas disease. Infection is often subclinical, but severe disease has been described in both free-ranging and captive primates. Panstrongylus megistus, a major T. cruzi vector, was found infesting a small-primate unit at Brasília zoo (ZooB), Brazil. ZooB lies close to a gallery-forest patch where T. cruzi circulates naturally. Here, we combine parasitological and molecular methods to investigate a focus of T. cruzi infection involving triatomine bugs and Neotropical primates at a zoo located in the Brazilian Savannah.MethodsWe assessed T. cruzi infection in vectors using optical microscopy (n = 34) and nested PCR (n = 50). We used quantitative PCR (qPCR) to examine blood samples from 26 primates and necropsy samples from two primates that died during the study. We determined parasite lineages in five vectors and two primates by comparing glucose-6-phosphate isomerase (G6pi) gene sequences.ResultsTrypanosoma cruzi was found in 44 vectors and 17 primates (six genera and eight species); one Mico chrysoleucus and one Saguinus niger had high parasitaemias. Trypanosoma cruzi DNA was detected in three primates born to qPCR-negative mothers at ZooB and in the two dead specimens. One Callithrix geoffroyi became qPCR-positive over a two-year follow-up. All G6pi sequences matched T. cruzi lineage TcI.ConclusionsOur findings strongly suggest vector-borne T. cruzi transmission within a small-primate unit at ZooB – with vectors, and perhaps also parasites, presumably coming from nearby gallery forest. Periodic checks for vectors and parasites would help eliminate T. cruzi transmission foci in captive-animal facilities. This should be of special importance for captive-breeding programs involving endangered mammals, and would reduce the risk of accidental T. cruzi transmission to keepers and veterinarians.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-016-1334-7) contains supplementary material, which is available to authorized users.

First report of Sapajus cay naturally infected by Trypanosoma cruzi in San Pedro Department, Paraguay

“…Fernandes et al (1999) also reported specimens of L. rosalia infected with 'TcII' (without determination of TcIIa-e subgroup) in Rio de Janeiro state (Brazil). Recently, among captive Neotropical primates in a Brazilian zoo, TcI was reported associated with Panstrongylus species transmission (MINUZZI-SOUZA et al, 2016). T. cruzi isolates from lemurs in the United States were assigned to TcIV (HALL et al, 2007;ROELLIG & YABSLEY, 2010) as well as isolates from wild primates in Bolivia and Venezuela (WESTENBERGER et al, 2006).…”

Lineage-specific serology confirms Brazilian Atlantic forest lion tamarins, Leontopithecus chrysomelas and Leontopithecus rosalia, as reservoir hosts of Trypanosoma cruzi II (TcII)

“…The lack of more severe changes may be due to a lesser pathology produced by the parasite as a result of the longer evolutionary relationship between parasite and primate host, but may also be related to a fitness cost for the animals, causing them to die before these changes are detected, either by predation or by an inability to cope in nature [45]. In the course of conservation programmes wild species are frequently translocated and, in light of the findings here indicative of both TcII and TcV/VI infection in lion tamarins, it is important to do this in a responsible manner to avoid introducing new parasite populations to non-endemic regions [34, 46]. Infections have also been recorded in captive populations, with an active transmission cycle involving Panstrongylus megistus being identified in a Brazilian Zoo, which is probably an extension of that of a neighbouring intact forest fragment [46].…”

“…In the course of conservation programmes wild species are frequently translocated and, in light of the findings here indicative of both TcII and TcV/VI infection in lion tamarins, it is important to do this in a responsible manner to avoid introducing new parasite populations to non-endemic regions [34, 46]. Infections have also been recorded in captive populations, with an active transmission cycle involving Panstrongylus megistus being identified in a Brazilian Zoo, which is probably an extension of that of a neighbouring intact forest fragment [46]. This not only highlights the potential for primates to act as sources of infection for humans, but also the potential for sylvatic triatomines to invade other settings where they are in close contact, such as human settlements at forest edges.…”

Synanthropic triatomines as potential vectors of Trypanosoma cruzi in Central Brazil

“…Trypanosoma cruzi infection was investigated by optical microscopy in live bugs at the laboratory as described by Minuzzi-Souza et al 8 . Bugs from LACEN in Goiás were brought dead to MPVBL, precluding fresh-slide examination.…”

“…House invasion and colonization by P. megistus must hence be closely monitored in areas with gallery forest remnants -and particularly over the early rainy season, when the records of the species in human environments peak 6 . Autochthonous T. cruzi transmission mediated by P. megistus was recently reported in primate units at the Brasília zoo 8 . In spite of the presence of T. cruzi-infected triatomines inside houses, no autochthonous cases of human Chagas disease have so far been reported from the Federal District.…”