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

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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.

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Most cited references 53

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The revised Trypanosoma cruzi subspecific nomenclature: rationale, epidemiological relevance and research applications.

Bianca Zingales, Michael Miles, David A. Campbell … (2012)

The protozoan Trypanosoma cruzi, its mammalian reservoirs, and vectors have existed in nature for millions of years. The human infection, named Chagas disease, is a major public health problem for Latin America. T. cruzi is genetically highly diverse and the understanding of the population structure of this parasite is critical because of the links to transmission cycles and disease. At present, T. cruzi is partitioned into six discrete typing units (DTUs), TcI-TcVI. Here we focus on the current status of taxonomy-related areas such as population structure, phylogeographical and eco-epidemiological features, and the correlation of DTU with natural and experimental infection. We also summarize methods for DTU genotyping, available for widespread use in endemic areas. For the immediate future multilocus sequence typing is likely to be the gold standard for population studies. We conclude that greater advances in our knowledge on pathogenic and epidemiological features of these parasites are expected in the coming decade through the comparative analysis of the genomes from isolates of various DTUs. Copyright © 2012 Elsevier B.V. All rights reserved.

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Effects of environmental change on emerging parasitic diseases.

Jonathan A. Patz, Thaddeus K. Graczyk, Nina L Geller … (2000)

Ecological disturbances exert an influence on the emergence and proliferation of malaria and zoonotic parasitic diseases, including, Leishmaniasis, cryptosporidiosis, giardiasis, trypanosomiasis, schistosomiasis, filariasis, onchocerciasis, and loiasis. Each environmental change, whether occurring as a natural phenomenon or through human intervention, changes the ecological balance and context within which disease hosts or vectors and parasites breed, develop, and transmit disease. Each species occupies a particular ecological niche and vector species sub-populations are distinct behaviourally and genetically as they adapt to man-made environments. Most zoonotic parasites display three distinct life cycles: sylvatic, zoonotic, and anthroponotic. In adapting to changed environmental conditions, including reduced non-human population and increased human population, some vectors display conversion from a primarily zoophyllic to primarily anthrophyllic orientation. Deforestation and ensuing changes in landuse, human settlement, commercial development, road construction, water control systems (dams, canals, irrigation systems, reservoirs), and climate, singly, and in combination have been accompanied by global increases in morbidity and mortality from emergent parasitic disease. The replacement of forests with crop farming, ranching, and raising small animals can create supportive habitats for parasites and their host vectors. When the land use of deforested areas changes, the pattern of human settlement is altered and habitat fragmentation may provide opportunities for exchange and transmission of parasites to the heretofore uninfected humans. Construction of water control projects can lead to shifts in such vector populations as snails and mosquitoes and their parasites. Construction of roads in previously inaccessible forested areas can lead to erosion, and stagnant ponds by blocking the flow of streams when the water rises during the rainy season. The combined effects of environmentally detrimental changes in local land use and alterations in global climate disrupt the natural ecosystem and can increase the risk of transmission of parasitic diseases to the human population.

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adephylo: new tools for investigating the phylogenetic signal in biological traits.

Thibaut Jombart, Thibaut Jombart, Stéphane Dray (2010)

adephylo is a package for the R software dedicated to the analysis of comparative evolutionary data. Phylogenetic comparative methods initially aimed at accounting for or removing the effects of phylogenetic signal in the analysis of biological traits. However, recent approaches have shown that considerable information can be gathered from the study of the phylogenetic signal. In particular, close examination of phylogenetic structures can unveil interesting evolutionary patterns. For this purpose, we developed the package adephylo that provides tools for quantifying and describing the phylogenetic structures of biological traits. adephylo implements tests of phylogenetic signal, phylogenetic distances and proximities, and novel methods for describing further univariate and multivariate phylogenetic structures. These tools open up new perspectives in the analysis of evolutionary comparative data. The stable version is available from CRAN: http:/cran.r-project.org/web/packages/adephylo/. The development version is hosted by R-Forge: http://r-forge.r-project.org/projects/adephylo/. Both versions can be installed directly from R. adephylo is distributed under the GNU General Public Licence (> or =2).

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Author and article information

Contributors

Érika Martins Braga: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, USA )

ISSN (Electronic): 1932-6203

Publication date Collection: 2013

Publication date (Electronic): 4 July 2013

Volume: 8

Issue: 7

Electronic Location Identifier: e67463

Affiliations

[1 ]Laboratório de Biologia de Tripanosomatídeos, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil

[2 ]Instituto Brasileiro para Medicina da Conservação, TRÍADE, Recife, Pernambuco, Brazil

[3 ]Programa de Conservação Mamíferos do Cerrado, PCMC, Araguari, Minas Gerais, Brazil

[4 ]Programa de Pós-graduação em Ecologia e Conservação, Universidade Federal de Mato Grosso do Sul, UFMS, Campo Grande, Mato Grosso do Sul, Brazil

[5 ]Programa de Pesquisa em Vida Selvagem/Projeto Carnívoros, Instituto de Pesquisas Cananéia (IPeC), Cananéia, São Paulo, Brazil

[6 ]Departamento de Ciências Biológicas, Universidade Federal de Goiás, UFG, Catalão, Goiás, Brazil

[7 ]Departamento de Medicina Preventiva e Saúde Animal, Universidade de São Paulo, USP, São Paulo, Brazil

[8 ]Universidade Católica Dom Bosco, UCDB, Campo Grande, Mato Grosso do Sul, Brazil

[9 ]Laboratório de Vida Selvagem, Empresa Brasileira de Pesquisa Agropecuária, Embrapa Pantanal, Corumbá, Mato Grosso do Sul, Brazil

Universidade Federal de Minas Gerais, Brazil

Author notes

* E-mail: jansen@ 123456ioc.fiocruz.br

Competing Interests: The authors have declared that no competing interests exist.

Conceived and designed the experiments: FLR GM AMJ. Performed the experiments: FLR JSL CCC FGL FCA RCA DB HMH. Analyzed the data: FLR ALR GM AMJ. Wrote the paper: FLR ALR AMJ.

Article

Publisher ID: PONE-D-13-05812

DOI: 10.1371/journal.pone.0067463

PMC ID: 3701642

PubMed ID: 23861767

SO-VID: 50e561ba-045a-4484-a1ba-c66b245b3585

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 6 February 2013

Date accepted : 18 May 2013

Page count

Pages: 12

Funding

This study was funded by ChagasEpiNet 223034. Fundação de Apoio ao Desenvolvimento do Ensino, Ciência e Tecnologia do Estado de Mato Grosso do Sul (FUNDECT) - 9777.256.476.13022008. National Research Center for the Conservation of Natural Predators – CENAP/ICMBio. Wildlife Conservation Society – OWOH 2008_001. Consórcio Capim Branco de Energia. CNPq Edital Universal 014/2008. PDJ-CNPq 150608/2013-6. Smithsonian Institution. Neotropical Grassland Conservancy. Idea Wild. U.S. Fish and Wildlife Service. A doctoral grant was provided by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) to FLR and CCC. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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

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Decoding Infection and Transmission

Most cited references 53

The revised Trypanosoma cruzi subspecific nomenclature: rationale, epidemiological relevance and research applications.

Effects of environmental change on emerging parasitic diseases.

adephylo: new tools for investigating the phylogenetic signal in biological traits.

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