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Hosts and vectors of Trypanosoma cruzi discrete typing units in the Chagas disease endemic region of the Paraguayan Chaco

  • NIDIA ACOSTA (a1), ELSA LÓPEZ (a1), MICHAEL D. LEWIS (a2), MARTIN S. LLEWELLYN (a2), ANA GÓMEZ (a3), FABIOLA ROMÁN (a3), MICHAEL A. MILES (a2) and MATTHEW YEO (a2)...

Summary

Active Trypanosoma cruzi transmission persists in the Gran Chaco region, which is considered hyperendemic for Chagas disease. Understanding domestic and sylvatic transmission cycles and therefore the relationship between vectors and mammalian hosts is crucial to designing and implementing improved effective control strategies. Here we describe the species of triatomine vectors and the sylvatic mammal reservoirs of T. cruzi, in different localities of the Paraguayan and Bolivian Chaco. We identify the T. cruzi genotypes discrete typing units (DTUs) and provide a map of their geographical distribution. A total of 1044 triatomines and 138 sylvatic mammals were captured. Five per cent of the triatomines were microscopically positive for T. cruzi (55 Triatoma infestans from Paraguay and one sylvatic Triatoma guasayana from Bolivia) and 17 animals (12·3%) comprising eight of 28 (28·5%) Dasypus novemcinctus, four of 27 (14·8%) Euphractus sexcinctus, three of 64 (4·7%) Chaetophractus spp. and two of 14 (14·3%) Didelphis albiventris. The most common DTU infecting domestic triatomine bugs was TcV (64%), followed by TcVI (28%), TcII (6·5%) and TcIII (1·5%). TcIII was overwhelmingly associated with armadillo species. We confirm the primary role of T. infestans in domestic transmission, armadillo species as the principal sylvatic hosts of TcIII, and consider the potential risk of TcIII as an agent of Chagas disease in the Chaco.

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      Hosts and vectors of Trypanosoma cruzi discrete typing units in the Chagas disease endemic region of the Paraguayan Chaco
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This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.

Corresponding author

*Corresponding author: Department of Pathogen Molecular Biology, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UK. E-mail: Matthew.Yeo@lshtm.ac.uk

References

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Acevedo, R., Aguilera, M., Miers, R., Velázquez, G. and Canese, J. (2002). Prevalencia de la enfermedad de Chagas en una población del Chaco Paraguayo. Revista Paraguaya de Microbiologia 22, 2627.
Acosta, N., Samudio, M., López, E., Vargas, F., Yaksic, N., Brenière, S. F. and Rojas de Arias, A. (2001). Isoenzyme profiles of Trypanosoma cruzi stocks from different areas of Paraguay. Memorias do Instituto Oswaldo Cruz 96, 527533.
Acosta, N., Miret, J., López, E. and Schinini, A. (2016). First report of Sapajus cay naturally infected by Trypanosoma cruzi in San Pedro Department, Paraguay. Revista Brasileira de Parasitologia Veterinária 25, 327332.
Almeida, C. E., Vinhaes, M. C., de Almeida, J. R., Silveira, A. C. and Costa, J. (2000). Monitoring the domiciliary and peridomiciliary invasion process of Triatoma rubrovaria in the State of Rio Grande do Sul, Brazil. Memorias do Instituto Oswaldo Cruz 95, 761768.
Alvarado-Otegui, J. A., Ceballos, L. A., Orozco, M. M., Enriquez, G. F., Cardinal, M. V., Cura, C., Schijman, A. G., Kitron, U. and Gürtler, R. E. (2012). The sylvatic transmission cycle of Trypanosoma cruzi in a rural area in the humid Chaco of Argentina. Acta Tropica 124, 7986.
Bacigalupo, A., Segura, J. A., García, A., Hidalgo, J., Galuppo, S. and Cattan, P. E. (2006). First finding of Chagas disease vectors associated with wild bushes in the Metropolitan Region of Chile. Revista médica de Chile 134, 12301236.
Bar, M. E. and Wisnivesky-Colli, C. (2001). Triatoma sordida Stal 1859 (Hemiptera, Reduviidae: Triatominae) in Palms of Northeastern Argentina. Memorias do Instituto Oswaldo Cruz 96, 895899.
Bar, M. E., Pieri Damborsky, M., Oscherov, E. B., Milano, A., Francisco, M., Avalos, G. and Wisnivesky-Colli, C. (2002). Triatomines involved in domestic and wild Trypanosoma cruzi transmission in Concepción, Corrientes, Argentina. Memorias do Instituto Oswaldo Cruz 97, 4346.
Barnabé, C., Mobarec, H. I., Jurado, M. R., Cortez, J. A. and Brenière, S. F. (2016). Reconsideration of the seven discrete typing units within the species Trypanosoma cruzi, a new proposal of three reliable mitochondrial clades. Infection, Genetics and Evolution 39, 176186.
Bento, D. N., Farias, L. M., Godoy, M. F. and Araújo, J. F. (1992). The epidemiology of Chagas’ disease in a rural area of the city of Teresina, Piauí, Brazil. Revista da Sociedade Brasileira de Medicina Tropical 25, 5158.
Bhattacharyya, T., Mills, E. A., Jansen, A. M. and Miles, M. A. (2015). Prospects for T. cruzi lineage-specific serological surveillance of wild mammals. Acta Tropica 151, 182186.
Brenière, S. F., Morochi, W., Bosseno, M. F., Ordoñez, J., Gutierrez, T., Vargas, F., Yaksic, N. and Noireau, F. (1998). Trypanosoma cruzi genotypes associated with domestic Triatoma sordida in Bolivia. Acta Tropica 71, 269283.
Brenière, S. F., Aliaga, C., Waleckx, E., Buitrago, R., Salas, R., Barnabé, C., Tibayrenc, M. and Noireau, F. (2012). Genetic characterization of Trypanosoma cruzi DTUs in wild Triatoma infestans from Bolivia: predominance of TcI. PLoS Neglected Tropical Diseases 6, e1650.
Brenière, S. F., Waleckx, E. and Barnabé, C. (2016). Over six thousand Trypanosoma cruzi strains classified into discrete typing units (DTUs): attempt at an inventory. PLoS Neglected Tropical Diseases 10, e0004792.
Brisse, S., Barnabé, C. and Tibayrenc, M. (2000). Identification of six Trypanosoma cruzi phylogenetic lineages by random amplified polymorphic DNA and multilocus enzyme electrophoresis. International Journal for Parasitology 30, 3544.
Canese, J. and Brice, E. (1977). Diagnóstico de la enfermedad de Chagas en aborígenes del Chaco paraguayo. Revista Paraguaya de Microbiologia 12, 910.
Ceballos, L. A., Piccinali, R. V., Berkunsky, I., Kitron, U. and Gürtler, R. E. (2009). First finding of melanic sylvatic Triatoma infestans (Hemiptera: Reduviidae) colonies in the Argentine Chaco. Journal of Medical Entomology 46, 11951202.
Ceballos, L. A., Piccinali, R. V., Marcet, P. L., Vazquez-Prokopec, G. M., Cardinal, M. V., Schachter-Broide, J., Dujardin, J. P., Dotson, E. M., Kitron, U. and Gürtler, R. E. (2011). Hidden sylvatic foci of the main vector of Chagas disease Triatoma infestans: threats to the vector elimination campaign? PLoS Neglected Tropical Diseases 5, e1365.
Cécere, M. C., Vázquez-Prokopec, G. M., Ceballos, L. A., Boragno, S., Zárate, J. E., Kitron, U. and Gürtler, R. E. (2013). Improved chemical control of Chagas disease vectors in the dry Chaco region. Journal of Medical Entomology 50, 394403.
Chapman, M. D., Baggaley, R. C., Godfrey-Fausset, P. F., Malpas, T. J., White, G., Canese, J. and Miles, M. A. (1984). Trypanosoma cruzi from the Paraguayan Chaco: isoenzyme profiles of strains isolated at Makthlawaiya. The Journal of Protozoology 31, 482486.
Corrales, R. M., Mora, M. C., Negrette, O. S., Diosque, P., Lacunza, D., Virreira, M., Brenière, S. F. and Basombrio, M. A. (2009). Congenital Chagas disease involves Trypanosoma cruzi sub-lineage IId in the northwestern province of Salta, Argentina. Infection, Genetics and Evolution 9, 278282.
Cura, C. I., Mejía-Jaramillo, A. M., Duffy, T., Burgos, J. M., Rodriguero, M., Cardinal, M. V., Kjos, S., Gurgel-Gonçalves, R., Blanchet, D., De Pablos, L. M., Tomasini, N., da Silva, A., Russomando, G., Cuba, C. A., Aznar, C., Abate, T., Levin, M. J., Osuna, A., Gürtler, R. E., Diosque, P., Solari, A., Triana-Chávez, O. and Schijman, A. G. (2010). Trypanosoma cruzi I genotypes in different geographical regions and transmission cycles based on a microsatellite motif of the intergenic spacer of spliced-leader genes. International Journal for Parasitology 40, 15991607.
Cura, C. I., Lucero, R. H., Bisio, M., Oshiro, E., Formichelli, L. B., Burgos, J. M., Lejona, S., Brusés, B. L., Hernández, D. O., Severini, G. V., Velázquez, E., Duffy, T., Anchart, E., Lattes, R., Altcheh, J., Freilij, H., Diez, M., Nagel, C., Vigliano, C., Favaloro, L., Favaloro, R. R., Merino, D. E., Sosa-Estani, S. and Schijman, A. G. (2012). Trypanosoma cruzi discrete typing units in Chagas disease patients from endemic and non-endemic regions of Argentina. Parasitology 139, 516521.
Damborsky, M. P., Bar, M. E. and Oscherov, E. B. (2001). Detection of triatomines (Hemiptera: Reduviidae) in domiciliary and extra-domiciliary ecotopes. Corrientes, Argentina. Cadernos de Saúde Pública 17, 843849.
de Freitas, J. M., Augusto-Pinto, L., Pimenta, J. R., Bastos-Rodrigues, L., Gonçalves, V. F., Teixeira, S. M., Chiari, E., Junqueira, A. C., Fernandes, O., Macedo, A. M., Machado, C. R. and Pena, S. D. (2006). Ancestral genomes, sex, and the population structure of Trypanosoma cruzi . PLoS Pathogens 2, e24.
del Puerto, F., Sánchez, Z., Nara, E., Meza, G., Paredes, B., Ferreira, E. and Russomando, G. (2010). Trypanosoma cruzi lineages detected in congenitally infected infants and Triatoma infestans from the same disease-endemic region under entomologic surveillance in Paraguay. The American Journal of Tropical Medicine and Hygiene 82, 386390.
de Luca D'oro, G. M., Gardenal, C. N., Perret, B., Crisci, J. V. and Montamat, E. E. (1993). Genetic structure of Trypanosoma cruzi populations from Argentina estimated from enzyme polymorphism. Parasitology 107, 405410.
Dereure, J., Barnabé, C., Vie, J. C., Madelenat, F. and Raccurt, C. (2001). Trypanosomatidae from wild mammals in the neotropical rainforest of French Guiana. Annals of Tropical Medicine and Parasitology 95, 157166.
Diotaiuti, L., Pereira, A. S., Loiola, C. F., Fernandes, A. J., Schofield, J. C., Dujardin, J. P., Dias, J. C. and Chiari, E. (1995). Inter-relation of sylvatic and domestic transmission of Trypanosoma cruzi in areas with and without domestic vectorial transmission in Minas Gerais, Brazil. Memorias do Instituto Oswaldo Cruz 90, 443448.
Enriquez, G. F., Cardinal, M. V., Orozco, M. M., Lanati, L., Schijman, A. G. and Gürtler, R. E. (2013). Discrete typing units of Trypanosoma cruzi identified in rural dogs and cats in the humid Argentinean Chaco. Parasitology 140, 303308.
Feliciangeli, M. D., Campbell-Lendrum, D., Martinez, C., Gonzalez, D., Coleman, P. and Davies, C. (2003). Chagas disease control in Venezuela: lessons for the Andean region and beyond. Trends in Parasitology 19, 4449.
Fernandes, O., Mangia, R. H., Lisboa, C. V., Pinho, A. P., Morel, C. M., Zingales, B., Campbell, D. A. and Jansen, A. M. (1999). The complexity of the sylvatic cycle of Trypanosoma cruzi in Rio de Janeiro state (Brazil) revealed by the non-transcribed spacer of the mini-exon gene. Parasitology 118, 161166.
Gaspe, M. S., Provecho, Y. M., Piccinali, R. V. and Gürtler, R. E. (2015). Where do these bugs come from? Phenotypic structure of Triatoma infestans populations after control interventions in the Argentine Chaco. Memorias do Instituto Oswaldo Cruz 110, 310318.
Gracey, M. and King, M. (2009). Indigenous health part 1: determinants and disease patterns. The Lancet 374, 6575.
Grisard, E. C., Carvalho-Pinto, C. J., Scholz, A. F., Toma, H. K., Schlemper, B. R. and Steindel, M. (2000). Trypanosoma cruzi infection in Didelphis marsupialis in Santa Catarina and Arvoredo Islands, southern Brazil. Memorias do Instituto Oswaldo Cruz 95, 795800.
Gurevitz, J. M., Ceballos, L. A., Gaspe, M. S., Alvarado-Otegui, J. A., Enríquez, G. F., Kitron, U. and Gürtler, R. E. (2011). Factors affecting infestation by Triatoma infestans in a rural area of the humid Chaco in Argentina: a multi-model inference approach. PLoS Neglected Tropical Diseases 5, e1349.
Gurevitz, J. M., Gaspe, M. S., Enríquez, G. F., Vassena, C. V., Alvarado-Otegui, J. A., Provecho, Y. M., Cueto, G. A., Picollo, M. I., Kitron, U. and Gürtler, R. E. (2012). Unexpected failures to control Chagas disease vectors with pyrethroid spraying in northern Argentina. Journal of Medical Entomology 49, 13791386.
Gürtler, R. E. (2009). Sustainability of vector control strategies in the Gran Chaco region: current challenges and possible approaches. Memorias do Instituto Oswaldo Cruz 104, 5259.
Gürtler, R. E., Chuit, R., Cécere, M. C., Castañera, M. B., Cohen, J. E. and Segura, E. L. (1998). Household prevalence of seropositivity for Trypanosoma cruzi in three rural villages in northwest Argentina: environmental, demographic, and entomologic associations. The American Journal of Tropical Medicine and Hygiene 59, 741749.
Gürtler, R. E., Kitron, U., Cécere, M. C., Segura, E. L. and Cohen, J. E. (2007). Sustainable vector control and management of Chagas disease in the Gran Chaco, Argentina. Proceedings of the National Academy of Sciences of the United States of America 104, 1619416199.
Hotez, P. J. (2014 a). Ten global “hotspots” for the neglected tropical diseases. PLoS Neglected Tropical Diseases 8, e2496.
Hotez, P. J. (2014 b). Aboriginal populations and their neglected tropical diseases. PLoS Neglected Tropical Diseases 8, e2286.
Kawashita, S. Y., Sanson, G. F., Fernandes, O., Zingales, B. and Briones, M. R. (2001). Maximum-likelihood divergence date estimates based on rRNA gene sequences suggest two scenarios of Trypanosoma cruzi intraspecific evolution. Molecular Biology and Evolution 18, 22502259.
Lardeux, F., Depickère, S., Duchon, S. and Chávez, T. (2010). Insecticide resistance of Triatoma infestans (Hemiptera, Reduviidae) vector of Chagas disease in Bolivia. Tropical Medicine and International Health 15, 10371048.
Lauricella, M. A., Stariolo, R. L., Riarte, A. R., Segura, E. L. and Gürtler, R. E. (2005). Distribution and pathogenicity of Trypanosoma cruzi isolated from peridomestic populations of Triatoma infestans and Triatoma guasayana from rural Western Argentina. Memorias do Instituto Oswaldo Cruz 100, 123129.
Lauthier, J. J., Tomasini, N., Barnabé, C., Rumi, M. M., D'Amato, A. M., Ragone, P. G., Yeo, M., Lewis, M. D., Llewellyn, M. S., Basombrío, M. A., Miles, M. A., Tibayrenc, M. and Diosque, P. (2012). Candidate targets for multilocus sequence typing of Trypanosoma cruzi: validation using parasite stocks from the Chaco Region and a set of reference strains. Infection, Genetics and Evolution 12, 350358.
Lent, H. and Wygodzinsky, P. (1979). Revision of the Triatominae (Hemiptera, Reduviidae), and their significance as vectors of Chagas disease. Bulletin of the American Museum of Natural History 163, 123520.
Lewis, M. D., Ma, J., Yeo, M., Carrasco, H. J., Llewellyn, M. S. and Miles, M. A. (2009). Genotyping of Trypanosoma cruzi: systematic selection of assays allowing rapid and accurate discrimination of all known lineages. The American Journal of Tropical Medicine and Hygiene 81, 10411049.
Lewis, M. D., Llewellyn, M. S., Yeo, M., Acosta, N., Gaunt, M. W. and Miles, M. A. (2011). Recent, independent and anthropogenic origins of Trypanosoma cruzi hybrids. PLoS Neglected Tropical Diseases 5, e1363.
Lisboa, C. V., Xavier, S. C., Herrera, H. M. and Jansen, A. M. (2009). The ecology of the Trypanosoma cruzi transmission cycle: dispersion of zymodeme 3 (Z3) in wild hosts from Brazilian biomes. Veterinary Parasitology 165, 1924.
Lisboa, C. V., Monteiro, R. V., Martins, A. F., Xavier, S. C., Lima, V. D. and Jansen, A. M. (2015). Infection with Trypanosoma cruzi TcII and TcI in free-ranging population of lion tamarins (Leontopithecus spp): an 11-year follow-up. Memorias do Instituto Oswaldo Cruz 110, 394402.
Llewellyn, M. S., Lewis, M. D., Acosta, N., Yeo, M., Carrasco, H. J., Segovia, M., Vargas, J., Torrico, F., Miles, M. A. and Gaunt, M. W. (2009). Trypanosoma cruzi IIc: phylogenetic and phylogeographic insights from sequence and microsatellite analysis and potential impact on emergent Chagas disease. PLoS Neglected Tropical Diseases 3, e510.
Lucero, R. H., Brusés, B. L., Cura, C. I., Formichelli, L. B., Juiz, N., Fernández, G. J., Bisio, M., Deluca, G. D., Besuschio, S., Hernández, D. O. and Schijman, A. G. (2016). Chagas’ disease in aboriginal and Creole communities from the Gran Chaco Region of Argentina: seroprevalence and molecular parasitological characterization. Infection, Genetics and Evolution 41, 8492.
Macchiaverna, N. P., Gaspe, M. S., Enriquez, G. F., Tomassone, L., Gürtler, R. E. and Cardinal, M. V. (2015). Trypanosoma cruzi infection in Triatoma sordida before and after community-wide residual insecticide spraying in the Argentinean Chaco. Acta Tropica 143, 97102.
Maffey, L., Cardinal, M. V., Ordóñez-Krasnowski, P. C., Lanati, L. A., Lauricella, M. A., Schijman, A. G. and Gürtler, R. E. (2012). Direct molecular identification of Trypanosoma cruzi discrete typing units in domestic and peridomestic Triatoma infestans and Triatoma sordida from the Argentine Chaco. Parasitology 139, 15701579.
Marcili, A., Lima, L., Cavazzana, M., Junqueira, A. C., Veludo, H. H., Maia Da Silva, F., Campaner, M., Paiva, F., Nunes, V. L. and Teixeira, M. M. (2009 a). A new genotype of Trypanosoma cruzi associated with bats evidenced by phylogenetic analyses using SSU rDNA, cytochrome b and Histone H2B genes and genotyping based on ITS1 rDNA. Parasitology 136, 641655.
Marcili, A., Lima, L., Valente, V. C., Valente, S. A., Batista, J. S., Junqueira, A. C., Souza, A. I., da Rosa, J. A., Campaner, M., Lewis, M. D., Llewellyn, M. S., Miles, M. A. and Teixeira, M. M. (2009 b). Comparative phylogeography of Trypanosoma cruzi TCIIc: new hosts, association with terrestrial ecotopes, and spatial clustering. Infection, Genetics and Evolution 9, 12651274.
Martins, L. P., Marcili, A., Castanho, R. E., Therezo, A. L., de Oliveira, J. C., Suzuki, R. B., Teixeira, M. M., da Rosa, J. A. and Sperança, M. A. (2008). Rural Triatoma rubrovaria from southern Brazil harbors Trypanosoma cruzi of lineage IIc. The American Journal of Tropical Medicine and Hygiene 79, 427434.
Messenger, L. A., Miles, M. A. and Bern, C. (2015). Between a bug and a hard place: Trypanosoma cruzi genetic diversity and the clinical outcomes of Chagas disease. Expert Review of Anti-Infective Therapy 13, 9951029.
Miles, M., Feliciangeli, D. and Rojas de Arias, A. (2003). American tripanosomiasis (Chagas disease) and the role of molecular epidemiology in guiding control strategies. British Medical Journal 326, 14441448.
Miles, M. A. (1993). Culturing and biological cloning of Trypanosoma cruzi . In Protocols in Molecular Parasitology, vol. 21 (ed. Hyde, J. E.), pp. 1528. Springer, London.
Miles, M. A., Póvoa, M. M., De Souza, A. A., Lainson, R., Shaw, J. J. and Ketteridge, D. S. (1981). Chagas's disease in the Amazon Basin: the distribution of Trypanosoma cruzi zymodemes 1 and 3 in Pará State, north Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 667674.
Miles, M. A., Arias, J. R., Valente, S. A., Naiff, R. D., de Souza, A. A., Póvoa, M. M., Lima, J. A. and Cedillos, R. A. (1983). Vertebrate hosts and vectors of Trypanosoma rangeli in the Amazon Basin of Brazil. The American Journal of Tropical Medicine and Hygiene 32, 12511259.
Miles, M. A., Llewellyn, M. S., Lewis, M. D., Yeo, M., Baleela, R., Fitzpatrick, S., Gaunt, M. W. and Mauricio, I. L. (2009). The molecular epidemiology and phylogeography of Trypanosoma cruzi and parallel research on Leishmania: looking back and to the future. Parasitology 136, 15091528.
Montamat, E. E., De Luca d'Oro, G., Perret, B. and Rivas, C. (1992). Characterization of Trypanosoma cruzi from Argentina by electrophoretic zymograms. Acta Tropica 51, 173.
Moretti, E., Castro, I., Franceschi, C. and Basso, B. (2010). Chagas disease: serological and electrocardiographic studies in Wichi and Creole communities of Misión Nueva Pompeya, Chaco, Argentina. Memorias do Instituto Oswaldo Cruz 105, 621627.
Morocoima, A., Carrasco, H. J., Boadas, J., Chique, J. D., Herrera, L. and Urdaneta-Morales, S. (2012). Trypanosoma cruzi III from armadillos (Dasypus novemcinctus novemcinctus) from Northeastern Venezuela and its biological behavior in murine model. Risk of emergency of Chagas’ disease. Experimental Parasitology 132, 341347.
Neris, N., Colmán, F., Ovelar, E., Sukigara, N. and Ishii, N. (2002). Guía de mamíferos medianos y grandes del Paraguay. Distribución, tendencia poblacional y utilización. Secretaría del Ambiente/Agencia de Cooperación Internacional para el Desarrollo, Asunción.
Noireau, F., Flores, R., Gutierrez, T. and Dujardin, J. P. (1997 a). Detection of sylvatic dark morphs of Triatoma infestans in the Bolivian Chaco. Memorias do Instituto Oswaldo Cruz 92, 583584.
Noireau, F., Brenière, F., Ordoñez, J., Cardozo, L., Morochi, W., Gutierrez, T., Bosseno, M. F., Garcia, S., Vargas, F., Yaksic, N., Dujardin, J. P., Peredo, C. and Wisnivesky-Colli, C. (1997 b). Low probability of transmission of Trypanosoma cruzi to humans by domiciliary Triatoma sordida in Bolivia. Transactions of the Royal Society of Tropical Medicine and Hygiene 91, 653656.
Noireau, F., Gutierrez, T., Zegarra, M., Flores, R., Brenière, F., Cardozo, L. and Dujardin, J. P. (1998). Cryptic speciation in Triatoma sordida (Hemiptera:Reduviidae) from the Bolivian Chaco. Tropical Medicine and International Health 3, 364372.
Noireau, F., Flores, R., Gutierrez, T., Abad-Franch, F., Flores, E. and Vargas, F. (2000). Natural ecotopes of Triatoma infestans dark morph and other sylvatic triatomines in the Bolivian Chaco. Transactions of the Royal Society of Tropical Medicine and Hygiene 94, 2327.
Orozco, M. M., Enriquez, G. F., Alvarado-Otegui, J. A., Cardinal, M. V., Schijman, A. G., Kitron, U. and Gürtler, R. E. (2013). New sylvatic hosts of Trypanosoma cruzi and their reservoir competence in the humid Chaco of Argentina: a longitudinal study. The American Journal of Tropical Medicine and Hygiene 88, 872882.
Pérez, E., Monje, M., Chang, B., Buitrago, R., Parrado, R., Barnabé, C., Noireau, F. and Brenière, S. F. (2013). Predominance of hybrid discrete typing units of Trypanosoma cruzi in domestic Triatoma infestans from the Bolivian Gran Chaco region. Infection, Genetics and Evolution 13, 116123.
Póvoa, M. M., de Souza, A. A., Naiff, R. D., Arias, J. R., Naiff, M. F., Biancardi, C. B. and Miles, M. A. (1984). Chagas’ disease in the Amazon basin IV. Host records of Trypanosoma cruzi zymodemes in the states of Amazonas and Rondônia, Brazil. Annals of Tropical Medicine and Parasitology 78, 479487.
Provecho, Y. M., Gaspe, M. S., del Pilar Fernández, M., Enriquez, G. F., Weinberg, D. and Gürtler, R. E. (2014). The peri-urban interface and house infestation with Triatoma infestans in the Argentine Chaco: an underreported process? Memorias do Instituto Oswaldo Cruz 109, 923934.
Quisberth, S., Waleckx, E., Monje, M., Chang, B., Noireau, F. and Brenière, S. F. (2011). “Andean” and “non-Andean” ITS-2 and mtCytB haplotypes of Triatoma infestans are observed in the Gran Chaco (Bolivia): population genetics and the origin of reinfestation. Infection, Genetics and Evolution 11, 10061014.
Rabinovich, J. E., Schweigmann, N., Yohai, V. and Wisnivesky-Colli, C. (2001). Probability of Trypanosoma cruzi transmission by Triatoma infestans (Hemiptera: Reduviidae) to the opossum Didelphis albiventris (Marsupiala: Didelphidae). The American Journal of Tropical Medicine and Hygiene 65, 125130.
Ramírez, J. D., Duque, M. C. and Guhl, F. (2011). Phylogenetic reconstruction based on Cytochrome b (Cytb) gene sequences reveals distinct genotypes within Colombian Trypanosoma cruzi I populations. Acta Tropica 119, 6165.
Risso, M. G., Sartor, P. A., Burgos, J. M., Briceño, L., Rodríguez, E. M., Guhl, F., Chavez, O. T., Espinoza, B., Monteón, V. M., Russomando, G., Schijman, A. G., Bottasso, O. A. and Leguizamón, M. S. (2011). Immunological identification of Trypanosoma cruzi lineages in human infection along the endemic area. The American Journal of Tropical Medicine and Hygiene 84, 7884.
Rojas de Arias, A. (2003). Control y Vigilancia de Chagas con la participación comunitaria de etnias indígenas: Una perspectiva de la situación. XIIa. Reunión Intergubernamental INCOSUR/Chagas, Santiago, Chile, Marzo de 2003 (PAHO document), pp. 121124.
Rojas de Arias, A., Velázquez de Saldívar, G., Merlo, R., Monzón de Calabró, M., Gamarra de Galaher, P. and Keller, F. (1990). Seroepidemiología de la enfermedad de Chagas en el Paraguay: un estudio de dos localidades del Chaco Paraguayo. Memorias del Instituto de Investigaciones en Ciencias de la Salud 15, 253264.
Rojas de Arias, A., Arévalo de Guillén, I., Inchaustti, A., Samudio, M. and Schmeda-Hischmann, G. (1993). Prevalence of Chagas disease in Ayoreo communities of the Paraguayan Chaco. Tropical Medicine and Parasitology 44, 285288.
Rojas de Arias, A., Rolón, M., Vega, M. C., Gómez, A., Román, F., Sánchez, H., Acosta, C., Villalba, C., Cécere, C., Marcet, P. and Dotson, E. (2011). Molecular epidemiology and ecosystem approach of the reinfestation process by Triatoma infestans in rural communities of the Paraguayan Chaco. XV Congreso Colombiano de Parasitología y Medicina Tropical. Biomédica 31, 314315.
Rolón, M., Vega, M. C., Román, F., Gómez, A. and Rojas de Arias, A. (2011). First report of colonies of sylvatic Triatoma infestans (Hemiptera: Reduviidae) in the Paraguayan Chaco, using a trained dog. PLoS Neglected Tropical Diseases 5, e1026.
Samuels, A. M., Clark, E. H., Galdos-Cardenas, G., Wiegand, R. E., Ferrufino, L., Menacho, S., Gil, J., Spicer, J., Budde, J., Levy, M. Z., Bozo, R. W., Gilman, R. H. and Bern, C. (2013). Epidemiology of and impact of insecticide spraying on Chagas disease in communities in the Bolivian Chaco. PLoS Neglected Tropical Diseases 7, e2358.
Sánchez, Z., Russomando, G. and Guillén, R. (2012). Enfermedad de Chagas: estudio de un vector secundario. Editorial Académica Española. LAP LAMBERT Academic Publishing GmbH & Co. KG., Saabrucken, Alemania, pp. 1100. ISBN-13: 978-3-659-03664-4.
Santos-Mallet, J. R., Silva, C. S., Gomes, S. A., Oliveira, D. L., Santos, C. L., Sousa, D. M., Pinheiro, N. L., Junqueira, A. C. and Gonçalves, T. C. (2008). Molecular characterization of Trypanosoma cruzi sylvatic isolates from Rio de Janeiro, Brazil. Parasitology Research 103, 10411045.
Saravia, N. G., Holguín, A. F., Cibulskis, R. E. and D'Alessandro, A. (1987). Divergent isoenzyme profiles of sylvatic and domiciliary Trypanosoma cruzi in the eastern plains, piedmont, and highlands of Colombia. The American Journal of Tropical Medicine and Hygiene 36, 5969.
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, 235253.
Souto, R. P., Fernandes, O., Macedo, A. M., Campbell, D. A. and Zingales, B. (1996). DNA markers define two major phylogenetic lineages of Trypanosoma cruzi . Molecular and Biochemical Parasitology 83, 141152.
Usinger, R. L., Wygodzinsky, P. and Ryckman, R. E. (1966). The biosystematics of Triatominae. Annual Review of Entomology 11, 309330.
Valette, E., Brenière, S. F., Le Pont, F. and Desjeux, P. (1988). Zymodemes of Trypanosoma cruzi isolated from wild mammals in Bolivia. Memorias do Instituto Oswaldo Cruz 83, 139140.
Vazquez-Prokopec, G. M., Ceballos, L. A., Marcet, P. L., Cécere, M. C., Cardinal, M. V., Kitron, U. and Gürtler, R. E. (2006). Seasonal variations in active dispersal of natural populations of Triatoma infestans in rural north-western Argentina. Medical and Veterinary Entomology 20, 273279.
Velázquez, C. J. and González, G. (1959). Aspectos de la enfermedad de Chagas en el Paraguay. Revista Goiana de Medicina 5, 357373.
Vezzani, D., Schweigmann, N. J., Pietrokovsky, S. M. and Wisnivesky-Colli, C. (2001). Characterization of Triatoma guasayana biotopes in a hardwood forest of Santiago del Estero, Argentina. Memorias do Instituto Oswaldo Cruz 96, 459466.
Vicco, M. H., Bontempi, I., Ortiz, S., Solari, A., Bottasso, O. A. and Marcipar, I. (2012). Chronic Chagas disease with cardiodigestive involvement and the TcVI infective form of Trypanosoma cruzi. A case report. Parasitology International 61, 735737.
Waleckx, E., Depickère, S., Salas, R., Aliaga, C., Monje, M., Calle, H., Buitrago, R., Noireau, F. and Brenière, S. F. (2012). New discoveries of sylvatic Triatoma infestans (Hemiptera: Reduviidae) throughout the Bolivian Chaco. The American Journal of Tropical Medicine and Hygiene 86, 455458.
Westenberger, S. J., Barnabé, C., Campbell, D. A. and Sturm, N. R. (2005). Two hybridization events define the population structure of Trypanosoma cruzi . Genetics 171, 527543.
Wisnivesky-Colli, C., Schweigmann, N. J., Pietrokovsky, S., Bottazi, V. and Rabinovich, J. E. (1997). Spatial distribution of Triatoma guasayana (Hemiptera: Reduviidae) in hardwood forest biotopes in Santiago del Estero, Argentina. Journal of Medical Entomology 34, 102109.
World Health Organization (2015). Chagas disease in Latin America: an epidemiological update based on 2010 estimates. Weekly Epidemiological Record 90, 3343.
Yeo, M., Acosta, N., Llewellyn, M., Sánchez, H., Adamson, S., Miles, G. A., López, E., González, 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, 225233.
Yeo, M., Lewis, M. D., Carrasco, H. J., Acosta, N., Llewellyn, M., da Silva Valente, S. A., de Costa Valente, V., de Arias, A. R. and Miles, M. A. (2007). Resolution of multiclonal infections of Trypanosoma cruzi from naturally infected triatomine bugs and from experimentally infected mice by direct plating on a sensitive solid medium. International Journal for Parasitology 37, 111120.
Zelada, J., Sanabria, V., Canese, A. and Canese, J. (1998). Enfermedad de Chagas en comunidades indígenas del Chaco Paraguayo. Revista Paraguaya de Microbiologia 18, 1317.
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, 240253.
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Parasitology
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