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Direct molecular identification of Trypanosoma cruzi Discrete Typing Units in domestic and peridomestic Triatoma infestans and Triatoma sordida from the Argentine Chaco

Published online by Cambridge University Press:  19 July 2012

L. MAFFEY ,
M. V. CARDINAL ,
P. C. ORDÓÑEZ-KRASNOWSKI ,
L. A. LANATI ,
M. A. LAURICELLA ,
A. G. SCHIJMAN  and
R. E. GÜRTLER
L. MAFFEY
Affiliation:
Laboratorio de Eco-Epidemiología, Departamento de Ecología, Genética y Evolución, Universidad de Buenos Aires, Buenos Aires, Argentina
M. V. CARDINAL*
Affiliation:
Laboratorio de Eco-Epidemiología, Departamento de Ecología, Genética y Evolución, Universidad de Buenos Aires, Buenos Aires, Argentina
P. C. ORDÓÑEZ-KRASNOWSKI
Affiliation:
Laboratorio de Eco-Epidemiología, Departamento de Ecología, Genética y Evolución, Universidad de Buenos Aires, Buenos Aires, Argentina
L. A. LANATI
Affiliation:
Laboratorio de Eco-Epidemiología, Departamento de Ecología, Genética y Evolución, Universidad de Buenos Aires, Buenos Aires, Argentina
M. A. LAURICELLA
Affiliation:
Instituto Nacional de Parasitología‘‘Dr. Mario Fatala Chabén’’-ANLIS, Buenos Aires, Argentina
A. G. SCHIJMAN
Affiliation:
Laboratorio de Biología Molecular de la Enfermedad de Chagas, Instituto de Investigaciones en Ingeniería Genética y Biología Molecular (INGEBI-CONICET), Vuelta de Obligado 2490, Buenos Aires, Argentina
R. E. GÜRTLER
Affiliation:
Laboratorio de Eco-Epidemiología, Departamento de Ecología, Genética y Evolución, Universidad de Buenos Aires, Buenos Aires, Argentina
*
*Corresponding author: Laboratorio de Eco-Epidemiología, Departamento de Ecología, Genética y Evolución, Universidad de Buenos Aires, Ciudad Universitaria, 1428 Buenos Aires, Argentina. Tel/Fax: +54 11 4576 3318. E-mail:mvcardinal@ege.fcen.uba.ar
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Summary

We assessed the distribution of Trypanosoma cruzi Discrete Typing Units (DTUs) in domestic and peridomestic Triatoma infestans and Triatoma sordida specimens collected in a well-defined rural area in Pampa del Indio, northeastern Argentina. Microscopically-positive bugs were randomly selected with a multi-level sampling design, and DTUs were identified using direct PCR strategies. TcVI predominated in 61% of 69 T. infestans and in 56% of 9 T. sordida. TcV was the secondary DTU in T. infestans (16%) and was found in 1 T. sordida specimen (11%). Three T. sordida (33%) were found infected with TcI, a DTU also identified in local Didelphis albiventris opossums. Mixed DTU infections occurred rarely (5%) and were detected both directly from the bugs' rectal ampoule and parasite cultures. The identified DTUs and bug collection sites of T. infestans were significantly associated. Bugs infected with TcV were almost exclusively captured in domiciles whereas those with TcVI were found similarly in domiciles and peridomiciles. All mixed infections occurred in domiciles. TcV-infected bugs fed more often on humans than on dogs, whereas TcVI-infected bugs showed the reverse pattern. T. sordida is a probable sylvatic vector of TcI linked to D. albiventris, and could represent a secondary vector of TcVI and TcV in the domestic/peridomestic cycle.

Keywords

Trypanosoma cruziDiscrete Typing UnitsPCRTriatoma infestansTriatoma sordidaChagas disease
Type
Research Article
Information
Parasitology , Volume 139 , Issue 12 , October 2012 , pp. 1570 - 1579
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Alvarado-Otegui, J. A., Ceballos, L. A., Orozco, M. M., Enriquez, G. F., Cardinal, M. V., Schiman, A. G., Kitron, U. and Gürtler, R. E. (2012). The sylvatic transmission cycle of Trypanosoma cruzi in the humid Chaco of Argentina. Acta Tropica (in the Press).CrossRefGoogle ScholarPubMed
Bar, M. E. and Wisnivesky-Colli, C. (2001). Triatoma sordida Stål 1859 (Hemiptera, Reduviidae: Triatominae) in palms of Northeastern Argentina. Memorias do Instituto Oswaldo Cruz 96, 895–899.CrossRefGoogle ScholarPubMed
Bosseno, M. F., Yacsik, N., Vargas, F. and Brenière, S. F. (2000). Selection of Trypanosoma cruzi clonal genotypes (Clonet 20 and 39) isolated from Bolivian triatomines following subculture in liquid medium. Memorias do Instituto Oswaldo Cruz 95, 601–607.CrossRefGoogle ScholarPubMed
Brenière, S. F., Bosseno, M. F., Noireau, F., Yacsik, N., Liegeard, P., Aznar, C. and Hontebeyrie, M. (2002). Integrated study of a Bolivian population infected by Trypanosoma cruzi, the agent of Chagas Disease. Memorias do Instituto Oswaldo Cruz 97, 289–295.CrossRefGoogle ScholarPubMed
Brisse, S., Verhoef, J. and Tibayrenc, M. (2001). Characterization of large and small subunit rRNA and mini-exon genes further supports the distinction of six Trypanosoma cruzi lineages. International Journal for Parasitology 31, 1218–1226.CrossRefGoogle ScholarPubMed
Burgos, J. M., Altcheh, J., Bisio, M., Duffy, T., Valadares, H. M. S., Seidenstein, M. E., Piccinali, R., Freitas, J. M., Levin, M. J., Machi, L., Macedo, A. M., Freilij, H. and Schijman, A. G. (2007). Direct molecular profiling of minicircle signatures and lineages of Trypanosoma cruzi bloodstream populations cuasing congenital Chagas disease. International Journal for Parasitology 37, 1319–1327.CrossRefGoogle Scholar
Cardinal, M. V., Castañera, M. B., Lauricella, M. A., Cecere, M. C., Ceballos, A. L., Vazquez-Prokopec, G. M., Kitron, U. and Gürtler, R. E. (2006). A prospective study of the effects of sustained vector surveillance following community-wide insecticide application on Trypanosoma cruzi of dogs and cats in rural northwestern Argentina. American Journal of Tropical Medicine and Hygiene 75, 753–761.CrossRefGoogle ScholarPubMed
Cardinal, M. V., Lauricella, M. A., Ceballos, L. A., Lanati, L., Marcet, P. L., Levin, M. J., Kitron, U., Gürtler, R. E. and Schijman, A. G. (2008). Molecular epidemiology of domestic and sylvatic Trypanosoma cruzi infection in rural northwestern Argentina. International Journal for Parasitology 38, 1533–1543.CrossRefGoogle ScholarPubMed
Cardinal, M. V., Lauricella, M. A., Marcet, P. L., Orozco, M. M., Kitron, U. and Gürtler, R. E. (2007). Impact of community-based vector control on house infestation and Trypanosoma cruzi infection in Triatoma infestans, dogs and cats in the Argentine Chaco. Acta Tropica 103, 201–211.CrossRefGoogle ScholarPubMed
Ceballos, L. A., Cardinal, M. V., Vazquez-Prokopec, G. M., Lauricella, M. A., Orozco, M. M., Cortinas, R., Schijman, A. G., Levin, M. J., Kitron, U. and Gürtler, R. E. (2006). Long-term reduction of Trypanosoma cruzi infection in sylvatic mammals following deforestation and sustained vector surveillance in northwestern Argentina. Acta Tropica 98, 286–296.CrossRefGoogle ScholarPubMed
Cohen, J. E. and Gürtler, R. E. (2001). Modeling household transmission of American Trypanosomiasis. Science 293, 694–698.CrossRefGoogle ScholarPubMed
Cura, C. I., Lucero, R. H., Bisio, M., Oshiro, E., Formicelli, L. B., Burgos, J. M., Lejonas, S., Brusés, B. L., Hernández, D. O., Severini, G. V., Velázquez, E., Duffy, T., Anchart, E., Latte, 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.CrossRefGoogle ScholarPubMed
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, 1599–1607.CrossRefGoogle ScholarPubMed
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, 405–410.CrossRefGoogle ScholarPubMed
Diosque, P., Barnabe, C., Padilla, A. M., Marco, J. D., Cardozo, R. M., Cimino, R. O., Nasser, J. R., Tibayrenc, M. and Basombrio, M. A. (2003). Multilocus enzyme electrophoresis analysis of Trypanosoma cruzi isolates from a geographically restricted endemic area for Chagas’ disease in Argentina. International Journal for Parasitology 33, 997–1003.CrossRefGoogle ScholarPubMed
Diosque, P., Padilla, A. M., Cimino, R. O., Marino Cardozo, R., Sanchez Negrette, O., Marco, J. D., Zacca, R., Meza, C., Juarez, A., Rojo, H., Rey, R., Corrales, R. M., Nasser, J. R. and Basombrío, M. A. (2004). Chagas disease in rural areas of Chaco province, Argentina: epidemiologic survey in humans, reservoirs, and vectors. American Journal for Tropical Medicine and Hygiene 71, 590–593.CrossRefGoogle ScholarPubMed
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, 443–448.CrossRefGoogle ScholarPubMed
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. doi:10.1371/journal.pntd.0001349.CrossRefGoogle Scholar
Gürtler, R. E., Ceballos, L. A., Ordóñez Krasnowski, P. C., Lanati, L. A., Stariolo, R. and Kitron, U. (2009). Strong host-feeding preferences of the vector Triatoma infestans modified by vector density: implications for the epidemiology of Chagas Disease. PLoS Neglected Tropical Diseases 3, e447. doi:10.1371/journal.pntd.0000447.CrossRefGoogle ScholarPubMed
Gürtler, R. E., Cecere, M. C., Lauricella, M. A., Cardinal, M. V., Kitron, U. and Cohen, J. E. (2007 b). Domestic dogs and cats as sources of Trypanosoma cruzi infection in rural northwestern Argentina. Parasitology 134, 69–82.CrossRefGoogle ScholarPubMed
Gürtler, R. E., Kitron, U., Cecere, M. C., Segura, E. L. and Cohen, J. E. (2007 a). Sustainable vector control and management of Chagas disease in the Gran Chaco, Argentina. Proceedings of the National Academy of Sciences, USA 104, 16194–16199.CrossRefGoogle ScholarPubMed
Herrera, C., Bargues, M. D., Fajardo, A., Montilla, M., Triana, O., Vallejo, G. A. and Guhl, F. (2007). Identifying four Trypanosoma cruzi I isolate haplotypes from different geographic regions in Colombia. Infection, Genetics and Evolution 7, 535–539.CrossRefGoogle ScholarPubMed
Higo, H., Miura, S., Horio, M., Mimori, T., Hamano, S., Agatsuma, T., Yanagi, T., Cruz-Reyes, A., Uyema, N., Rojas de Arias, A., Matta, V., Akahane, H., Hirayama, K., Takeuchi, T., Tada, I. and Himeno, K. (2004). Genotypic variation among lineages of Trypanosoma cruzi and its geographic aspects. Parasitology International 53, 337–344.CrossRefGoogle ScholarPubMed
Laurent, J. P., Barnabé, C., Quesney, V., Noel, S. and Tibayrenc, M. (1997). Impact of clonal evolution on the biological diversity of Trypanosoma cruzi. Parasitology 114, 213–218.CrossRefGoogle ScholarPubMed
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, 123–129.CrossRefGoogle ScholarPubMed
Llewellyn, M. S., Miles, M. A., Carrasco, H. J., Lewis, M. D., Yeo, M., Vargas, J., Torrico, F., Diosque, P., Valente, V., Valente, S. A. and Gaunt, M. W. (2009). Genome-scale multilocus microsatellite typing of Trypanosoma cruzi discrete typing unit I reveals phylogeographic structure and specific genotypes linked to human infection. PLoS Pathogens 5, e1000410.CrossRefGoogle ScholarPubMed
Llewellyn, M. S., Rivett-Carnac, J. B., Fitzpatrick, S., Lewis, M. D., Yeo, M., Gaunt, M. W. and Miles, M. A. (2011). Extraordinary Trypanosoma cruzi diversity within single mammalian reservoir hosts implies a mechanism of diversifying selection. International Journal for Parasitology 41, 609–614.CrossRefGoogle ScholarPubMed
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. American Journal of Tropical Medicine and Hygiene 81, 1041–1049.CrossRefGoogle ScholarPubMed
Loza-Murguía, M. and Noireau, F. (2010). Vectorial capacity of Triatoma guasayana (Wygodzinsky & Abalos) (Hemiptera: Reduviidae) compared with two other species of epidemic importance. Neotropical Entomology 39, 799–809.CrossRefGoogle ScholarPubMed
Macedo, A. M. and Pena, S. D. (1998). Genetic variability of Trypanosoma cruzi: implications for the pathogenesis of Chagas disease. Parasitology Today 14, 119–123.CrossRefGoogle ScholarPubMed
Marcet, P. L., Duffy, T., Cardinal, M. V., Burgos, J. M., Lauricella, M. A., Levin, M. J., Kitron, U., Gurtler, R. E. and Schijman, A. G. (2006). PCR-based screening and lineage identification of Trypanosoma cruzi directly from faecal samples of triatomine bugs from northwestern Argentina. Parasitology 132, 57–65.CrossRefGoogle ScholarPubMed
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, 1509–1528.CrossRefGoogle ScholarPubMed
Montamat, E. E., Arauzo, S., Cazzulo, J. J. and Subias, E. (1987). Characterization by electrophoretic zymograms of 19 Trypanosoma cruzi clones derived from two chronic chagasic patients. Comparative Biochemistry and Physiology 87, 417–422.Google Scholar
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). 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, 653–656.CrossRefGoogle ScholarPubMed
Schofield, C. J., Lehane, M. J., McEwan, P., Catalá, S. S. and Gorla, D. E. (1991). Dispersive flight by Triatoma sordida. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 676–678.CrossRefGoogle ScholarPubMed
Schweigmann, N. J., Pietrokovsky, S., Bottazzi, V., Conti, O., Bujas, M. A. and Wisnivesky-Colli, C. (1999). Estudio de la prevalencia de infección por Trypanosoma cruzi en zarigüeyas (Didelphis albiventris) en Santiago del Estero, Argentina. Revista Panamericana de Salud Pública 6, 371–377.CrossRefGoogle Scholar
StataCorp (2007). Stata Statistical Software: Release 10.0. Stata Corporation, College Station, TX, USA.Google Scholar
Tibayrenc, M. (1998). Genetic epidemiology of parasitic protozoa and other infectious agents: the need for an integrated approach. International Journal for Parasitology 28, 85–104.CrossRefGoogle ScholarPubMed
Vazquez-Prokopec, G. M., Ceballos, L. A., Marcet, P. L., Cecere, 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, 273–279.CrossRefGoogle ScholarPubMed
Wisnivesky-Colli, C., Schweigmann, N. J., Alberti, A., Pietrokovsky, S. M., Conti, O., Montoya, S., Riarte, A. and Rivas, C. (1992). Sylvatic American trypanosomiasis in Argentina. Trypanosoma cruzi infection in mammals from the Chaco forest in Santiago del Estero.Transactions of the Royal Society of Tropical Medicine and Hygiene 86, 38–41.CrossRefGoogle ScholarPubMed
World Health Organization. (2007). Report of the Scientific Working Group on Chagas Disease. TDR/SWH/09. World Health Organization, Geneva, Switzerland.Google Scholar
Yeo, M., Acosta, N., Llewellyn, M., Sánchez, H., Adamson, S., Miles, G. A. J., López, E., González, N., Patterson, J. S., Gaunt, M. W., Rojas de Arias, A. 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.CrossRefGoogle ScholarPubMed
Yeo, M., Lewis, M. D., Carrasco, H. J., Acosta, N., Llewellyn, M., Aldo, S., Vera de Costa, V., Rojas de Arias, A. 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, 111–120.CrossRefGoogle ScholarPubMed
Zingales, B., Andrade, S. G., Briones, M. R. S., Campbe, 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. Memorias do Instituto Oswaldo Cruz 104, 1051–1054.CrossRefGoogle ScholarPubMed