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Trypanosoma cruzi TcI and TcII transmission among wild carnivores, small mammals and dogs in a conservation unit and surrounding areas, Brazil

Published online by Cambridge University Press:  12 October 2012

FABIANA LOPES ROCHA ,
ANDRÉ LUIZ RODRIGUES ROQUE ,
RICARDO CORASSA ARRAIS ,
JEAN PIERRE SANTOS ,
VALDIRENE DOS SANTOS LIMA ,
SAMANTA CRISTINA DAS CHAGAS XAVIER ,
PEDRO CORDEIR-ESTRELA ,
PAULO SÉRGIO D'ANDREA  and
ANA MARIA JANSEN
FABIANA LOPES ROCHA
Affiliation:
Laboratório de Biologia de Tripanosomatídeos, Fundação Oswaldo Cruz, FIOCRUZ. Av. Brasil 4365. Pav. Rocha Lima 516. Rio de Janeiro-RJ. CEP: 21045-900, Brazil Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Fundação Oswaldo Cruz, FIOCRUZ. Av. Brasil 4365. Rio de Janeiro-RJ. CEP: 21045-900, Brazil Tríade – Instituto Brasileiro para Medicina da Conservação – Rua Silveira Lobo, 32, Caixa Postal 48, Bairro Casa Forte. Recife-PE. CEP: 52061-030, Brazil
ANDRÉ LUIZ RODRIGUES ROQUE
Affiliation:
Laboratório de Biologia de Tripanosomatídeos, Fundação Oswaldo Cruz, FIOCRUZ. Av. Brasil 4365. Pav. Rocha Lima 516. Rio de Janeiro-RJ. CEP: 21045-900, Brazil
RICARDO CORASSA ARRAIS
Affiliation:
Departamento de Medicina Preventiva e Saúde Animal. Universidade de São Paulo, USP. Av. Prof. Orlando Marques de Paiva, 87. Cidade Universitária. São Paulo – SP. CEP: 05508-270, Brazil
JEAN PIERRE SANTOS
Affiliation:
Instituto Pró-carnívoros. Av. Horácio Neto, 1030 – Parque Edmundo Zanoni. Atibaia-SP – CEP: 12945-010, Brazil
VALDIRENE DOS SANTOS LIMA
Affiliation:
Laboratório de Biologia de Tripanosomatídeos, Fundação Oswaldo Cruz, FIOCRUZ. Av. Brasil 4365. Pav. Rocha Lima 516. Rio de Janeiro-RJ. CEP: 21045-900, Brazil
SAMANTA CRISTINA DAS CHAGAS XAVIER
Affiliation:
Laboratório de Biologia de Tripanosomatídeos, Fundação Oswaldo Cruz, FIOCRUZ. Av. Brasil 4365. Pav. Rocha Lima 516. Rio de Janeiro-RJ. CEP: 21045-900, Brazil
PEDRO CORDEIR-ESTRELA
Affiliation:
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Fundação Oswaldo Cruz, FIOCRUZ. Av. Brasil 4365. Rio de Janeiro-RJ. CEP: 21045-900, Brazil
PAULO SÉRGIO D'ANDREA
Affiliation:
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Fundação Oswaldo Cruz, FIOCRUZ. Av. Brasil 4365. Rio de Janeiro-RJ. CEP: 21045-900, Brazil
ANA MARIA JANSEN*
Affiliation:
Laboratório de Biologia de Tripanosomatídeos, Fundação Oswaldo Cruz, FIOCRUZ. Av. Brasil 4365. Pav. Rocha Lima 516. Rio de Janeiro-RJ. CEP: 21045-900, Brazil
*
*Corresponding author: Laboratório de Biologia de Tripanosomatídeos, Fundação Oswaldo Cruz, FIOCRUZ. Av. Brasil 4365. Pav. Rocha Lima 516. Rio de Janeiro-RJ. CEP: 21045-900, Brazil. Fax: +55 21 2560 6572. E-mail: [email protected]
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Summary

Aiming to better understand the ecological aspects of Trypanosoma cruzi transmission cycles, wild carnivores, small mammals and dogs were examined for T. cruzi infection in the Serra da Canastra National Park region, Brazil. Isolates were genotyped using mini-exon gene and PCR-RFLP (1f8 and H3) genomic targets. Trypanosoma cruzi transmission was well established in the area and occurred in both wild and peridomestic environments. Dog seroprevalence was 29·4% (63/214) and TcI and TcII genotypes, besides mixed infections were observed. Only TcI was detected in wild mammals. Marsupials displayed lower relative abundance, but a high prevalence of positive haemocultures (4/22), whereas rodents displayed positive haemocultures (9/113) mainly in the abundant Akodon montensis and Cerradomys subflavus species. The felid Leopardus pardalis was the only carnivore to display positive haemoculture and was captured in the same region where the small mammal prevalence of T. cruzi infection was high. Two canid species, Chrysocyon brachyurus and Cerdocyon thous, were serologically positive for T. cruzi infection (4/8 and 8/39, respectively), probably related to their capacity to exploit different ecological niches. Herein, dog infection not only signals T. cruzi transmission but also the genotypes present. Distinct transmission strategies of the T. cruzi genotypes are discussed.

Keywords

transmission cyclestrophic networkreservoirDiscrete Typing UnitsChagas diseaseSerra da Canastra National ParkBrazil
Type
Research Article
Information
Parasitology , Volume 140 , Issue 2 , February 2013 , pp. 160 - 170
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Andrade, S. G. and Magalhaes, J. B. (1996). Biodemes and zymodemes of Trypanosoma cruzi strains: correlations with clinical data and experimental pathology. Revista da Sociedade Brasileira de Medicina Tropical 30, 27–35.CrossRefGoogle Scholar
Araujo, C. A., Waniek, P. J., Xavier, S. C. and Jansen, A. M. (2011). Genotype variation of Trypanosoma cruzi isolates from different Brazilian biomes. Experimental Parasitology 127, 308–312. doi: 10.1016/j.exppara.2010.07.013.CrossRefGoogle ScholarPubMed
Ashford, R. W. (1996). Leishmaniasis reservoirs and their significance in control. Clinics in Dermatology 14, 523–532. doi: 0738–081X(96)00041-7CrossRefGoogle ScholarPubMed
Bizerril, M. X. A., Soares, C. C. and Santos, J. P. (2011). Linking community communication to conservation of the maned wolf in central Brazil. Environmental Education Research 17, 815–827.CrossRefGoogle Scholar
Bonvicino, C. R., Lemos, B. and Weksler, M. (2005). Small mammals of Chapada dos Veadeiros National Park (Cerrado of Central Brazil): ecologic, karyologic, and taxonomic considerations. Brazilian Journal of Biology 65, 395–406. doi: S1519-69842005000300004.CrossRefGoogle ScholarPubMed
Brown, E. L., Roellig, D. M., Gompper, M. E., Monello, R. J., Wenning, K. M., Gabriel, M. W. and Yabsley, M. J. (2010). Seroprevalence of Trypanosoma cruzi among eleven potential reservoir species from six states across the southern United States. Vector-Borne and Zoonotic Diseases 10, 757–763. Doi: 10.1089/vbz.2009.0009CrossRefGoogle ScholarPubMed
Camargo, M. E. (1966). Fluorescent antibody test for the serodiagnosis of American trypanosomiasis. Technical modification employing preserved culture forms of Trypanosoma cruzi in a slide test. Revista do Instituto de Medicina Tropical São Paulo 8, 227–235.Google Scholar
Cleaveland, S., Meslin, F. X. and Breiman, R. (2006). Dogs can play useful role as sentinel hosts for disease. Natur, Londone 440, 605. Doi: 10.1038/440605bCrossRefGoogle ScholarPubMed
Fernandes, O., Santos, S. S., Cupolillo, E., Mendonca, B., Derre, R., Junqueira, A. C., Santos, L. C., Sturm, N. R., Naiff, R. D., Barret, T. V., Campbell, D. A. and Coura, J. R. (2001). A mini-exon multiplex polymerase chain reaction to distinguish the major groups of Trypanosoma cruzi and T. rangeli in the Brazilian Amazon. Transactions of the Royal Society of Tropical Medicine and Hygiene 95, 97–99.CrossRefGoogle Scholar
Gurtler, R. E., Cecere, M. C., Lauricella, M. A., Cardinal, M. V., Kitron, U. and Cohen, J. E. (2007). Domestic dogs and cats as sources of Trypanosoma cruzi infection in rural northwestern Argentina. Parasitology 134, 69–82. Doi: http://dx.doi.org/10.1017/S0031182006001259.CrossRefGoogle ScholarPubMed
Hanf, M., Adenis, A., Nacher, M. and Carme, B. (2011). The role of El Nino Southern Oscillation (ENSO) on variations of monthly Plasmodium falciparum malaria cases at the Cayenne General Hospital, 1996–2009, French Guiana. Malaria Journal 10, 100. doi: 10.1186/1475-2875-10-100.CrossRefGoogle Scholar
Herrera, H. M., Lisboa, C. V., Pinho, A. P., Olifiers, N., Bianchi, R. C., Rocha, F. L., Mourao, G. M. and Jansen, A. M. (2008). The coati (Nasua nasua, Carnivora, Procyonidae) as a reservoir host for the main lineages of Trypanosoma cruzi in the Pantanal region, Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 102, 1133–1139. doi: 10.1016/j.trstmh.2008.04.041.CrossRefGoogle ScholarPubMed
Herrera, H. M., Rocha, F. L., Lisboa, C. V., Rademaker, V., Mourao, G. M. and Jansen, A. M. (2011). Food web connections and the transmission cycles of Trypanosoma cruzi and Trypanosoma evansi (Kinetoplastida, Trypanosomatidae) in the Pantanal Region, Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 105, 380–387. doi: 10.1016/j.trstmh.2011.04.008.CrossRefGoogle ScholarPubMed
Herrera, L., D'Andrea, P. S., Xavier, S. C., Mangia, R. H., Fernandes, O. and Jansen, A. M. (2005). Trypanosoma cruzi infection in wild mammals of the National Park ‘Serra da Capivara’ and its surroundings (Piaui, Brazil), an area endemic for Chagas disease. Transactions of the Royal Society of Tropical Medicine and Hygiene 99, 379–388. doi: 10.1016/j.trstmh.2004.07.006.CrossRefGoogle Scholar
IBAMA. Instituto Brasileiro do Meio Ambiente e Recursos Naturais Renováveis (2005). Plano de manejo do Parque Nacional da Serra da Canastra. IBAMA, Brasília.Google Scholar
Jacomo, A. T. D., Kashivakura, C. K., Ferro, C., Furtado, M. M., Astete, S. P., Torres, N. M., Sollmann, R. and Silveira, L. (2009). Home range and spatial organization of maned wolves in the Brazilian grasslands. Journal of Mammalogy 90, 150–157. Doi: http://dx.doi.org/10.1644/07-MAMM-A-380.1.CrossRefGoogle Scholar
Jansen, A. M., Leon, L., Machado, G. M., da Silva, M. H., Souza-Leao, S. M. and Deane, M. P. (1991). Trypanosoma cruzi in the opossum Didelphis marsupialis: parasitological and serological follow-up of the acute infection. Experimental Parasitology 73, 249–259. doi: 0014-4894(91)90096-F.CrossRefGoogle ScholarPubMed
Juarez, K. M. and Marinho, J. (2002). Diet, habitat use, and home ranges of sympatric canids in central Brazil. Journal of Mammalogy 83, 925–933. doi: http://www.jstor.org/stable/1383498.2.0.CO;2>CrossRefGoogle Scholar
Kribs-Zaleta, C. (2010). Estimating contact process saturation in sylvatic transmission of Trypanosoma cruzi in the United States. PLoS Neglected Tropical Diseases 4, e656. doi: 10.1371/journal.pntd.0000656.CrossRefGoogle ScholarPubMed
Lisboa, C. V., Mangia, R. H., Luz, S. L., Kluczkovski, A. Jr., Ferreira, L. F., Ribeiro, C. T., Fernandes, O. and Jansen, A. M. (2006). Stable infection of primates with Trypanosoma cruzi I and II. Parasitology 133, 603–611. doi: 10.1017/S0031182006000722.CrossRefGoogle ScholarPubMed
Lisboa, C. V., Pinho, A. P., Herrera, H. M., Gerhardt, M., Cupolillo, E. and Jansen, A. M. (2008). Trypanosoma cruzi (Kinetoplastida, Trypanosomatidae) genotypes in neotropical bats in Brazil. Veterinary Parasitology 156, 314–318. doi: 10.1016/j.vetpar.2008.06.004.CrossRefGoogle ScholarPubMed
Machado, E. M., Fernandes, A. J., Murta, S. M., Vitor, R. W., Camilo, D. J. Jr., Pinheiro, S. W., Lopes, E. R., Adad, S. J., Romanha, A. J. and Pinto Dias, J. C. (2001). A study of experimental reinfection by Trypanosoma cruzi in dogs. The American Journal of Tropical Medicine and Hygiene 65, 958–965.CrossRefGoogle ScholarPubMed
May-Junior, J. A., Songsasen, N., Azevedo, F. C., Santos, J. P., Paula, R. C., Rodrigues, F. H., Rodden, M. D., Wildt, D. E. and Morato, R. G. (2009). Hematology and blood chemistry parameters differ in free-ranging maned wolves (Chrysocyon brachyurus) living in the Serra da Canastra National Park versus adjacent farmlands, Brazil. Journal of Wildlife Diseases 45, 81–90.CrossRefGoogle Scholar
Mazzocchi, F. (2008). Complexity in biology. Exceeding the limits of reductionism and determinism using complexity theory. EMBO Reports 9, 10–14. doi: 10.1038/sj.embor.7401147.CrossRefGoogle ScholarPubMed
Michalski, F., Crawshaw, P. G., de Oliveira, T. G. and Fabian, M. E. (2006). Notes on home range and habitat use of three small carnivore species in a disturbed vegetation mosaic of southeastern Brazil. Mammalia 70, 52–57. Doi: 10.1515/MAMM.2006.004.CrossRefGoogle Scholar
Noireau, F., Diosque, P. and Jansen, A. M. (2009). Trypanosoma cruzi: adaptation to its vectors and its hosts. Veterinary Research 40, 26. doi: 10.1051/vetres/2009009.CrossRefGoogle ScholarPubMed
Nowak, R. M. (2005). Walker's Carnivores of the World. The John Hopkins University Press, Baltimore, MD, USA.Google Scholar
Pineda, V., Saldana, A., Monfante, I., Santamaria, A., Gottdenker, N. L., Yabsley, M. J., Rapoport, G. and Calzada, J. E. (2011). Prevalence of trypanosome infections in dogs from Chagas disease endemic regions in Panama, Central America. Veterinary Parasitology 178, 360–363. doi: 10.1016/j.vetpar.2010.12.043.CrossRefGoogle ScholarPubMed
Rocha-mendes, F., Mikich, S. B., Quadros, J. and Pedro, W. A. (2010). Feeding ecology of carnivores (Mammalia, Carnivora) in Atlantic Forest remnants, Southern Brazil. Biota neotropical 10, 1–10.Google Scholar
Roque, A. L., Xavier, S. C., da Rocha, M. G., Duarte, A. C., D'Andrea, P. S. and Jansen, A. M. (2008). Trypanosoma cruzi transmission cycle among wild and domestic mammals in three areas of orally transmitted Chagas disease outbreaks. The American Journal of Tropical Medicine Hygiene 79, 742–749.CrossRefGoogle ScholarPubMed
Rozas, M., De, D. S., Adaui, V., Coronado, X., Barnabe, C., Tibyarenc, M., Solari, A. and Dujardin, J. C. (2007). Multilocus polymerase chain reaction restriction fragment–length polymorphism genotyping of Trypanosoma cruzi (Chagas disease): taxonomic and clinical applications. The Journal of Infectious Diseases 195, 1381–1388. doi: 10.1086/513440.CrossRefGoogle ScholarPubMed
Shikanai-Yasuda, M. A. and Carvalho, N. B. (2012). Oral transmission of Chagas disease. Clinical Infectious Diseases 54, 845–852. doi: 10.1093/cid/cir956.CrossRefGoogle ScholarPubMed
Sikes, R. S. and Gannon, W. L. (2011). Guidelines of the American Society of Mammalogists for the use of wild mammals in research. Journal of Mammalogy 92, 235–253. Doi: 10.1644/10-MAMM-F-355.1.CrossRefGoogle Scholar
Steindel, M., Kramer, P. L., Scholl, D., Soares, M., de Moraes, M. H., Eger, I., Kosmann, C., Sincero, T. C., Stoco, P. H., Murta, S. M., de Carvalho-Pinto, C. J. and Grisard, E. C. (2008). Characterization of Trypanosoma cruzi isolated from humans, vectors, and animal reservoirs following an outbreak of acute human Chagas disease in Santa Catarina State, Brazil. Diagnostic Microbiology and Infectious Disease 60, 25–32. doi: 10.1016/j.diagmicrobio.2007.07.016.CrossRefGoogle ScholarPubMed
Vallejo, G. A., Guhl, F., Chiari, E. and Macedo, A. M. (1999). Species specific detection of Trypanosoma cruzi and Trypanosoma rangeli in vector and mammalian hosts by polymerase chain reaction amplification of kinetoplast minicircle DNA. Acta Tropica 72, 203–212. doi: S0001-706X(98)00085-0.CrossRefGoogle ScholarPubMed
Westenberger, S. J., Barnabe, C., Campbell, D. A. and Sturm, N. R. (2005). Two hybridization events define the population structure of Trypanosoma cruzi. Genetics 171, 527–543. doi: 10.1534/genetics.104.038745.CrossRefGoogle ScholarPubMed
World Health Organization (2002). Control of Chagas disease. WHO Technical Report Series No 905. World Health Organization, Geneva, Switzerland.Google Scholar
Xavier, S. C., Roque, A. L., Lima, V. S., Monteiro, K. J., Otaviano, J. C., Ferreira da Silva, L. F. and Jansen, A. M. (2012). Lower richness of small wild mammal species and Chagas disease risk. Plos Neglected Tropical Diseases 6, e1647. doi: 10.1371/journal.pntd.0001647.CrossRefGoogle ScholarPubMed
Yeo, M., Acosta, N., Llewellyn, M., Sanchez, H., Adamson, S., Miles, G. A., Lopez, E., Gonzalez, N., Patterson, J. S., Gaunt, M. W., de Arias, A. R. and Miles, M. A. (2005). Origins of Chagas disease: Didelphis species are natural hosts of Trypanosoma cruzi I and armadillos hosts of Trypanosoma cruzi II, including hybrids. International Journal for Parasitology 35, 225–233. doi: 10.1016/j.ijpara.2004.10.024.CrossRefGoogle ScholarPubMed
Zingales, B., Andrade, S. G., Briones, M. R., Campbell, D. A., Chiari, E., Fernandes, O., Guhl, F., Lages-Silva, E., Macedo, A. M., Machado, C. R., Miles, M. A., Romanha, A. J., Sturm, N. R., Tibayrenc, M. and Schijman, A. G. (2009). A new consensus for Trypanosoma cruzi intraspecific nomenclature: second revision meeting recommends TcI to TcVI. Memórias do Instituto Oswaldo Cruz 104, 1051–1054. doi: S0074-02762009000700021.CrossRefGoogle ScholarPubMed
Zingales, B., Miles, M. A., Campbell, D. A., Tibayrenc, M., Macedo, A. M., Teixeira, M. M., Schijman, A. G., Llewellyn, M. S., Lages-Silva, E., Machado, C. R., Andrade, S. G. and Sturm, N. R. (2012). The revised Trypanosoma cruzi subspecific nomenclature: Rationale, epidemiological relevance and research applications. Infection, Genetics and Evolution 12, 240–253. doi: 10.1016/j.meegid.2011.12.009.CrossRefGoogle ScholarPubMed
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