Complexity and multi-factoriality of Trypanosoma cruzi sylvatic cycle in coatis, Nasua nasua (Procyonidae), and triatomine bugs in the Brazilian Pantanal.

BACKGROUND: Trypanosoma cruzi is dispersed in nature through many transmission mechanisms among a high diversity of vectors and mammalian species, representing particular behaviors and habitats. Thus, each locality has a unique set of conditions underlying the maintenance of this parasite in the wild. The aim of the present study was to evaluate the life-cycle of T. cruzi in free-ranging coatis from the central region of the Brazilian Pantanal using a multi-factorial approach. METHODS: Three methodological blocks were used in the present study: (i) We evaluated T. cruzi infection using serological (ELISA) and parasitological (hemoculture) tests in free-ranging coatis captured from October 2010 to March 2012. In addition, we characterized T. cruzi isolates as DTUs (Discrete Typing Units); (ii) We evaluated Trypanosoma infection in species of Triatoma and Rhodnius inhabiting coati arboreal nests from May to September 2012 using parasitological and molecular assays; and (iii) We analyzed a set of longitudinal data (from 2005 to 2012) concerning the effects of T. cruzi infection on this coati population. Herein, we investigated whether seasonality, host sex, and host age influence T. cruzi prevalence and patterns of infection. RESULTS: The 2010-2012 period presented high seroprevalence on coatis (72.0 % ELISA) and a high percentage of individuals with infectivity competence (20.5 % positive hemoculture). All isolates presented TcI band patterns, occurring in single (n = 3) and mixed infections (1 TcI/T. rangeli; 4 with undefined characterization). Both male and female individuals presented the same transmission potential, expressed as positive hemoculture, which was only detected in the summer. However, overall, the data (2005-2012) highlighted the importance of females for T. cruzi maintenance in the winter. Moreover, twenty-three (67.6 %) bugs from five coati nests (71.4 %) were infected with flagellated forms. Seventeen samples were characterized as T. cruzi (TcI and TcIII genotypes). CONCLUSION: In the Pantanal region, T. cruzi is transmitted in a complex, multifactorial, dynamic and non-linear transmission web. The coati nests might be inserted in this web, acting as important transmission foci at the arboreal stratum to different mammal species with arboreal or scansorial behavior.

Infestation of arboreal nests of coatis by triatomine species, vectors of Trypanosoma cruzi, in a large Neotropical wetland.

The coati (Nasua nasua, Carnivora) is a medium-sized mammal common in the Pantanal of Brazil. Unlike most mammals, coatis construct arboreal nests used for resting and reproduction. In this region, the coati is an important host of Trypanosoma cruzi, the causative agent of Chagas disease. There are two possible routes through coatis can be infected by T. cruzi: the oral route or the vectorial route. However, the relative importance of each of these routes in the infection of coatis and its role in the sylvatic cycle of the parasite are unknown. Our objectives were to investigate: (i) whether coati nests were infested by triatomine bugs, (ii) what species were frequent in the nests, (iii) whether the triatomines in nests were infected by T. cruzi, and (iv) what were the food resources of these triatomines. Eight of the 24 nests sampled were infested with triatomines, a total of 37 specimens of at least two species (Rhodnius stali and Triatoma sordida). In one nest, R. stali and T. sordida co-occurred and both fed on multiple resources, including coatis. This is the first report of triatomines occurring in arboreal nests of coatis. The co-occurrence of two different genera of triatomine vectors and coatis within the limited space of the coati nests provide multiple opportunities for the exchange of the protozoan parasite through both the vectorial and oral transmission routes.

Trypanosoma cruzi infection in neotropical wild carnivores (Mammalia: Carnivora): at the top of the T. cruzi transmission chain.

Little is known on the role played by Neotropical wild carnivores in the Trypanosoma cruzi transmission cycles. We investigated T. cruzi infection in wild carnivores from three sites in Brazil through parasitological and serological tests. The seven carnivore species examined were infected by T. cruzi, but high parasitemias detectable by hemoculture were found only in two Procyonidae species. Genotyping by Mini-exon gene, PCR-RFLP (1f8/Akw21I) and kDNA genomic targets revealed that the raccoon (Procyon cancrivorus) harbored TcI and the coatis (Nasua nasua) harbored TcI, TcII, TcIII-IV and Trypanosoma rangeli, in single and mixed infections, besides four T. cruzi isolates that displayed odd band patterns in the Mini-exon assay. These findings corroborate the coati can be a bioaccumulator of T. cruzi Discrete Typing Units (DTU) and may act as a transmission hub, a connection point joining sylvatic transmission cycles within terrestrial and arboreal mammals and vectors. Also, the odd band patterns observed in coatis' isolates reinforce that T. cruzi diversity might be much higher than currently acknowledged. Additionally, we assembled our data with T. cruzi infection on Neotropical carnivores' literature records to provide a comprehensive analysis of the infection patterns among distinct carnivore species, especially considering their ecological traits and phylogeny. Altogether, fifteen Neotropical carnivore species were found naturally infected by T. cruzi. Species diet was associated with T. cruzi infection rates, supporting the hypothesis that predator-prey links are important mechanisms for T. cruzi maintenance and dispersion in the wild. Distinct T. cruzi infection patterns across carnivore species and study sites were notable. Musteloidea species consistently exhibit high parasitemias in different studies which indicate their high infectivity potential. Mesocarnivores that feed on both invertebrates and mammals, including the coati, a host that can be bioaccumulator of T. cruzi DTU's, seem to take place at the top of the T. cruzi transmission chain.