Trypanosoma cruzi Infection in Neotropical Wild Carnivores (Mammalia: Carnivora): At the Top of the T. cruzi Transmission Chain

Abstract

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.

Ecological host fitting of Trypanosoma cruzi TcI in Bolivia: mosaic population structure, hybridization and a role for humans in Andean parasite dispersal

“…2003) and have a propensity for nonvectoral routes of infection, including oral transmission via predation of infected vectors or mammals (Jansen & Roque 2010; Rocha et al . 2013) and exposure to contaminated anal scent gland secretions (Carreira et al . 2001).…”

“…2005; Rocha et al . 2013; Lima et al . 2014), cautioning the interpretation of putative host associations.…”

“…2009a; Rocha et al . 2013; Lima et al . 2014), and genetic diversity of terrestrial TcIII appears similarly independent of host species (Llewellyn et al .…”

Triatominae (Hemiptera, Reduviidae) in the Pantanal region: association with Trypanosoma cruzi, different habitats and vertebrate hosts

“…The enzootic cycle of T. cruzi in relation to mammalian hosts in the Pantanal region has been extensively investigated over the last decade. In fact, T. cruzi infection in this wetland has been reported in small mammals (rodents and marsupials), carnivores (coatis, crab-eating fox, crab-eating raccoon and ocelot), bats, armadillos, peccaries and feral pigs (12) (13) (14) (15) (16) (17) .…”

“…The fieldwork was conducted in the Southern Pantanal region, an area that has been described as having active T. cruzi transmission cycles in the last decade (12) (13) (14) (15) (16) (17) . The investigation sites included (a) Nhumirim Ranch (NHUR), 18°59ʹ17.07″S 56°37ʹ8.65″W, which is a research station belonging to Embrapa Pantanal, along with neighboring farms with extensive cattle raising; and (b) sections of the MS-184 (67km) and MS-337 …”