Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-26T23:06:49.717Z Has data issue: false hasContentIssue false
  • English
  • Français

The molecular epidemiology and phylogeography of Trypanosoma cruzi and parallel research on Leishmania: looking back and to the future

Published online by Cambridge University Press:  20 August 2009

M. A. MILES ,
M. S. LLEWELLYN ,
M. D. LEWIS ,
M. YEO ,
R. BALEELA ,
S. FITZPATRICK ,
M. W. GAUNT  and
I. L. MAURICIO
M. A. MILES*
Affiliation:
Pathogen Molecular Biology Unit, Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UK
M. S. LLEWELLYN
Affiliation:
Pathogen Molecular Biology Unit, Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UK
M. D. LEWIS
Affiliation:
Pathogen Molecular Biology Unit, Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UK
M. YEO
Affiliation:
Pathogen Molecular Biology Unit, Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UK
R. BALEELA
Affiliation:
Pathogen Molecular Biology Unit, Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UK
S. FITZPATRICK
Affiliation:
Pathogen Molecular Biology Unit, Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UK
M. W. GAUNT
Affiliation:
Pathogen Molecular Biology Unit, Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UK
I. L. MAURICIO
Affiliation:
Pathogen Molecular Biology Unit, Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UK
*
*Tel: +44 20 7927 2340. Fax: +44 20 7636 8739. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Trypanosoma cruzi is the protozoan agent of Chagas disease, and the most important parasitic disease in Latin America. Protozoa of the genus Leishmania are global agents of visceral and cutaneous leishmaniasis, fatal and disfiguring diseases. In the 1970s multilocus enzyme electrophoresis demonstrated that T. cruzi is a heterogeneous complex. Six zymodemes were described, corresponding with currently recognized lineages, TcI and TcIIa-e – now defined by multiple genetic markers. Molecular epidemiology has substantially resolved the phylogeography and ecological niches of the T. cruzi lineages. Genetic hybridization has fundamentally influenced T. cruzi evolution and epidemiology of Chagas disease. Genetic exchange of T. cruzi in vitro involves fusion of diploids and genome erosion, producing aneuploid hybrids. Transgenic fluorescent clones are new tools to elucidate molecular genetics and phenotypic variation. We speculate that pericardial sequestration plays a role in pathogenesis. Multilocus sequence typing, microsatellites and, ultimately, comparative genomics are improving understanding of T. cruzi population genetics. Similarly, in Leishmania, genetic groups have been defined, including epidemiologically important hybrids; genetic exchange can occur in the sand fly vector. We describe the profound impact of this parallel research on genetic diversity of T. cruzi and Leishmania, in the context of epidemiology, taxonomy and disease control.

Keywords

Trypanosoma cruziChagas diseasemolecular epidemiologypericardial effusionphylogeographyLeishmaniagenetic exchangemicrosatellitesmultilocus sequence typingtaxonomy
Type
Research Article
Information
Parasitology , Volume 136 , Special Issue 12: Special Centenary Issue – Parasitology 1908–2008 , October 2009 , pp. 1509 - 1528
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Aanensen, D. M. and Spratt, B. G. (2005). The multilocus sequence typing network: mlst.net. Nucleic Acids Research 33, 728–733.CrossRefGoogle ScholarPubMed
Acquatella, H. (2007). Echocardiography in Chagas heart disease. Circulation 115, 1124–1131.CrossRefGoogle ScholarPubMed
Aguilar, H. M., Abad-Franch, F., Dias, J. C., Junqueira, A. C. and Coura, J. R. (2007). Chagas disease in the Amazon Region. Memórias do Instituto Oswaldo Cruz 102 (Suppl 1), 47–56.CrossRefGoogle ScholarPubMed
Akopyants, N. S., Kimblin, N., Secundino, N., Patrick, R., Peters, N., Lawyer, P., Dobson, D. E., Beverley, S. M. and Sacks, D. L. (2009). Demonstration of genetic exchange during cyclical development of Leishmania in the sand fly vector. Science 324, 265–268.CrossRefGoogle ScholarPubMed
Al-Jawabreh, A., Diezmann, S., Muller, M., Wirth, T., Schnur, L. F., Strelkova, M. V., Kovalenko, D. A., Razakov, S. A., Schwenkenbecher, J., Kuhls, K. and Schonian, G. (2008). Identification of geographically distributed sub-populations of Leishmania (Leishmania) major by microsatellite analysis. BMC Evolutionary Biology 8, 183.CrossRefGoogle ScholarPubMed
Anez, N., Crisante, G., Silva, F. M. D., Rojas, A., Carrasco, H., Umezawa, E. S., Stolf, A. M. S., Ramirez, J. L. and Teixeira, M. M. G. (2004). Predominance of lineage I among Trypanosoma cruzi isolates from Venezuelan patients with different clinical profiles of acute Chagas disease. Tropical Medicine & International Health 9, 1319–1326.CrossRefGoogle ScholarPubMed
Anon, A. (1999). Recommendations from a satellite meeting. Memórias do Instituto Oswaldo Cruz 94, 429–432.Google Scholar
Ashford, R. W. (2000). The leishmaniases as emerging and reemerging zoonoses. International Journal for Parasitology 30, 1269–1281.CrossRefGoogle ScholarPubMed
Barnabe, C., Brisse, S. and Tibayrenc, M. (2000). Population structure and genetic typing of Trypanosoma cruzi, the agent of Chagas disease: a multilocus enzyme electrophoresis approach. Parasitology 120, 513–526.CrossRefGoogle ScholarPubMed
Barnabé, C., Neubauer, K., Solari, A. and Tibayrenc, M. (2001 a). Trypanosoma cruzi: presence of the two major phylogenetic lineages and of several lesser discrete typing units (DTUs) in Chile and Paraguay. Acta Tropica 78, 127–137.CrossRefGoogle ScholarPubMed
Barnabé, C., Yaeger, R., Pung, O. and Tibayrenc, M. (2001 b). Trypanosoma cruzi: a considerable phylogenetic divergence indicates that the agent of Chagas Disease is indigenous to the native fauna of the United States. Experimental Parasitology 99, 73–79.CrossRefGoogle Scholar
Belli, A., Miles, M. and Kelly, J. (1994). A putative Leishmania panamensis/Leishmania braziliensis hybrid is a causative agent of human cutaneous leishmaniasis in Nicaragua. Parasitology 109, 435–442.CrossRefGoogle ScholarPubMed
Bosseno, M. F., Telleria, J., Vargas, F., Yaksic, N., Noireau, F., Morin, A. and Breniere, S. F. (1996). Trypanosoma cruzi: study of the distribution of two widespread clonal genotypes in Bolivian Triatoma infestans vectors shows a high frequency of mixed infections. Experimental Parasitology 83, 275–282.CrossRefGoogle Scholar
Botilde, Y., Laurent, T., Quispe Tintaya, W., Chicharro, C., Canavate, C., Cruz, I., Kuhls, K., Schonian, G. and Dujardin, J. C. (2006). Comparison of molecular markers for strain typing of Leishmania infantum. Infection, Genetics and Evolution 6, 440–446.CrossRefGoogle ScholarPubMed
Breniere, S. F., Carrasco, R., Revollo, S., Aparicio, G., Desjeux, P. and Tibayrenc, M. (1989). Chagas' disease in Bolivia: clinical and epidemiological features and zymodeme variability of Trypanosoma cruzi strains isolated from patients. American Journal of Tropical Medicine and Hygiene 41, 521–529.CrossRefGoogle ScholarPubMed
Brisse, S., Henriksson, J., Barnabe, C., Douzery, E. J. P., Berkvens, D., Serrano, M., De Carvalho, M. R. C., Buck, G. A., Dujardin, J.-C. and Tibayrenc, M. (2003). Evidence for genetic exchange and hybridization in Trypanosoma cruzi based on nucleotide sequences and molecular karyotype. Infection, Genetics and Evolution 2, 173–183.CrossRefGoogle ScholarPubMed
Brisse, S., Verhoef, J. and Tibayrenc, M. (2001). Characterisation 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
Broutin, H., Tarrieu, F., Tibayrenc, M., Oury, B. and Barnabe, C. (2006). Phylogenetic analysis of the glucose-6-phosphate isomerase gene in Trypanosoma cruzi. Experimental Parasitology 113, 1–7.CrossRefGoogle ScholarPubMed
Burgos, J. M., Begher, S., Silva, H. M., Bisio, M., Duffy, T., Levin, M. J., Macedo, A. M. and Schijman, A. G. (2008). Molecular identification of Trypanosoma cruzi I tropism for central nervous system in Chagas reactivation due to AIDS. American Journal of Tropical Medicine and Hygiene 78, 294–297.CrossRefGoogle ScholarPubMed
Butler, G., Rasmussen, M. D., Lin, M. F., Santos, M. A., Sakthikumar, S., Munro, C. A., Rheinbay, E., Grabherr, M., Forche, A., Reedy, J. L., Agrafioti, I., Arnaud, M. B., Bates, S., Brown, A. J., Brunke, S., Costanzo, M. C., Fitzpatrick, D. A., De Groot, P. W., Harris, D., Hoyer, L. L., Hube, B., Klis, F. M., Kodira, C., Lennard, N., Logue, M. E., Martin, R., Neiman, A. M., Nikolaou, E., Quail, M. A., Quinn, J., Santos, M. C., Schmitzberger, F. F., Sherlock, G., Shah, P., Silverstein, K. A., Skrzypek, M. S., Soll, D., Staggs, R., Stansfield, I., Stumpf, M. P., Sudbery, P. E., Srikantha, T., Zeng, Q., Berman, J., Berriman, M., Heitman, J., Gow, N. A., Lorenz, M. C., Birren, B. W., Kellis, M. and Cuomo, C. A. (2009). Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature, London 459, 657–662.CrossRefGoogle ScholarPubMed
Campbell, D., Westenberger, S. and Sturm, N. (2004). The determinants of Chagas disease: connecting parasite and host genetics. Current Molecular Medicine 4, 549–562.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
Carranza, J. C., Valadares, H. M., D'avila, D. A., Baptista, R. P., Moreno, M., Galvao, L. M., Chiari, E., Sturm, N. R., Gontijo, E. D., Macedo, A. M. and Zingales, B. (2009). Trypanosoma cruzi maxicircle heterogeneity in Chagas disease patients from Brazil. International Journal for Parasitology 39, 963–973.CrossRefGoogle ScholarPubMed
Carrasco, H. J., Frame, I. A., Valente, S. A. and Miles, M. A. (1996). Genetic exchange as a possible source of genomic diversity in sylvatic populations of Trypanosoma cruzi. American Journal of Tropical Medicine and Hygiene 54, 418–424.CrossRefGoogle ScholarPubMed
Chapman, M., Baggaley, R., Godfrey-Fausset, P., Malpas, T., White, G., Canese, J. and Miles, M. (1984). Trypanosoma cruzi from the Paraguayan Chaco: isoenzyme profiles of strains isolated at Makthlawaiya. Journal of Protozoology 31, 482–486.CrossRefGoogle ScholarPubMed
Chagas, C. (1909). Nova tripanosomiase humana. Estudos sobre a morfologia e o ciclo evolutivo do Schizotrypanum cruzi n. gen., n. sp. agente etiologico de nova entidade morbida do homem. Memórias do Instituto Oswaldo Cruz 1, 159–218.CrossRefGoogle Scholar
Clark, C. G. and Pung, O. J. (1994). Host specificity of ribosomal DNA variation in sylvatic Trypanosoma cruzi from North America. Molecular and Biochemical Parasitology 66, 175–179.CrossRefGoogle ScholarPubMed
Corrales, R. M., Mora, M. C., Negrette, O. S., Diosque, P., Lacunza, D., Virreira, M., Breniere, 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, 278–282.CrossRefGoogle ScholarPubMed
Cortez, M. R., Pinho, A. P., Cuervo, P., Alfaro, F., Solano, M., Xavier, S. C., D'andrea, P. S., Fernandes, O., Torrico, F., Noireau, F. and Jansen, A. M. (2006). Trypanosoma cruzi (Kinetoplastida Trypanosomatidae): ecology of the transmission cycle in the wild environment of the Andean valley of Cochabamba, Bolivia. Experimental Parasitology 114, 305–313.CrossRefGoogle ScholarPubMed
Coura, J. R., Junqueira, A. C., Fernandes, O., Valente, S. A. and Miles, M. A. (2002). Emerging Chagas disease in Amazonian Brazil. Trends in Parasitology 18, 171–176.CrossRefGoogle ScholarPubMed
Cupolillo, E., Grimaldi, G. Jr. and Momen, H. (1994). A general classification of New World Leishmania using numerical zymotaxonomy. American Journal of Tropical Medicine and Hygiene 50, 296–311.CrossRefGoogle ScholarPubMed
De Freitas, J. M., Augusto-Pinto, L., Pimenta, J. R., Bastos-Rodrigues, L., Goncalves, V. F., Teixeira, S. M. R., Chiari, E., Junqueira, A. C. V., Fernandes, O., Macedo, A. M., Machado, C. R. and Pena, S. D. J. (2006). Ancestral genomes, sex, and the population structure of Trypanosoma cruzi. PLoS Pathogens 2, e24.CrossRefGoogle ScholarPubMed
Delgado, O., Cupolillo, E., Bonfante-Garrido, R., Silva, S., Belfort, E., Grimaldi Junior, G. and Momen, H. (1997). Cutaneous leishmaniasis in Venezuela caused by infection with a new hybrid between Leishmania (Viannia) braziliensis and L. (V.) guyanensis. Memórias do Instituto Oswaldo Cruz 92, 581–582.CrossRefGoogle ScholarPubMed
Dujardin, J.-C., Banuls, A.-L., Llanos-Cuentas, A., Alvarez, E., Dedoncker, S., Jacquet, D., Le Ray, D., Arevalo, J. and Tibayrenc, M. (1995). Putative Leishmania hybrids in the Eastern Andean valley of Huanuco, Peru. Acta Tropica 59, 293–307.CrossRefGoogle ScholarPubMed
Dvorak, J., Hall, T., Crane, M., Engel, J., Mcdaniel, J. and Uriegas, R. (1982). Trypanosoma cruzi: flow cytometric analysis. I. Analysis of total DNA/organism by means of mithramycin-induced fluorescence. Journal of Protozoology 29, 430–437.CrossRefGoogle ScholarPubMed
El-Sayed, N. M., Myler, P. J., Bartholomeu, D. C., Nilsson, D., Aggarwal, G., Tran, A. N., Ghedin, E., Worthey, E. A., Delcher, A. L., Blandin, G., Westenberger, S. J., Caler, E., Cerqueira, G. C., Branche, C., Haas, B., Anupama, A., Arner, E., Aslund, L., Attipoe, P., Bontempi, E., Bringaud, F., Burton, P., Cadag, E., Campbell, D. A., Carrington, M., Crabtree, J., Darban, H., Da Silveira, J. F., De Jong, P., Edwards, K., Englund, P. T., Fazelina, G., Feldblyum, T., Ferella, M., Frasch, A. C., Gull, K., Horn, D., Hou, L., Huang, Y., Kindlund, E., Klingbeil, M., Kluge, S., Koo, H., Lacerda, D., Levin, M. J., Lorenzi, H., Louie, T., Machado, C. R., Mcculloch, R., Mckenna, A., Mizuno, Y., Mottram, J. C., Nelson, S., Ochaya, S., Osoegawa, K., Pai, G., Parsons, M., Pentony, M., Pettersson, U., Pop, M., Ramirez, J. L., Rinta, J., Robertson, L., Salzberg, S. L., Sanchez, D. O., Seyler, A., Sharma, R., Shetty, J., Simpson, A. J., Sisk, E., Tammi, M. T., Tarleton, R., Teixeira, S., Van Aken, S., Vogt, C., Ward, P. N., Wickstead, B., Wortman, J., White, O., Fraser, C. M., Stuart, K. D. and Andersson, B. (2005). The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309, 409–415.CrossRefGoogle ScholarPubMed
Evans, D., Kennedy, W., Elbihari, S., Chapman, C., Smith, V. and Peters, W. (1987). Hybrid formation within the genus Leishmania? Parassitologia 29, 165–173.Google ScholarPubMed
Feliciangeli, M. D., Carrasco, H., Patterson, J. S., Suarez, B., Martinez, C. and Medina, M. (2004). Mixed domestic infestation by Rhodnius prolixus Stal, 1859 and Panstrongylus geniculatus Latreille, 1811, vector incrimination, and seroprevalence for Trypanosoma cruzi among inhabitants in El Guamito, Lara State, Venezuela. American Journal of Tropical Medicine and Hygiene 71, 501–505.CrossRefGoogle ScholarPubMed
Fitzpatrick, S., Feliciangeli, M. D., Sanchez-Martin, M. J., Monteiro, F. A. and Miles, M. A. (2008). Molecular genetics reveal that silvatic Rhodnius prolixus do colonise rural houses. PLoS Neglected Tropical Diseases 2, e210.CrossRefGoogle ScholarPubMed
Gaunt, M. and Miles, M. (2000). The ecotopes and evolution of triatomine bugs (Triatominae) and their associated trypanosomes. Memórias do Instituto Oswaldo Cruz 95, 557–565.CrossRefGoogle ScholarPubMed
Gaunt, M. W., Yeo, M., Frame, I. A., Stothard, J. R., Carrasco, H. J., Taylor, M. C., Mena, S. S., Veazey, P., Miles, G. A., Acosta, N., De Arias, A. R. and Miles, M. A. (2003). Mechanism of genetic exchange in American trypanosomes. Nature, London 421, 936–939.CrossRefGoogle ScholarPubMed
Heitman, J. (2006). Sexual reproduction and the evolution of microbial pathogens. Current Biology 16, R711–R725.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
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.CrossRefGoogle Scholar
Kelly, J., Law, J., Chapman, C., Van Eys, G. and Evans, D. (1991). Evidence of genetic recombination in Leishmania. Molecular and Biochemical Parasitology 46, 253–263.CrossRefGoogle ScholarPubMed
Koffi, M., De Meeus, T., Bucheton, B., Solano, P., Camara, M., Kaba, D., Cuny, G., Ayala, F. J. and Jamonneau, V. (2009). Population genetics of Trypanosoma brucei gambiense, the agent of sleeping sickness in Western Africa. Proceedings of the National Academy of Sciences, USA 106, 209–214.CrossRefGoogle ScholarPubMed
Kuhls, K., Chicharro, C., Canavate, C., Cortes, S., Campino, L., Haralambous, C., Soteriadou, K., Pratlong, F., Dedet, J. P., Mauricio, I., Miles, M., Schaar, M., Ochsenreither, S., Radtke, O. A. and Schonian, G. (2008). Differentiation and gene flow among European populations of Leishmania infantum MON-1. PLoS Neglected Tropical Diseases 2, e261.CrossRefGoogle ScholarPubMed
Kuhls, K., Keilonat, L., Ochsenreither, S., Schaar, M., Schweynoch, C., Presber, W. and Schonian, G. (2007). Multilocus microsatellite typing (MLMT) reveals genetically isolated populations between and within the main endemic regions of visceral leishmaniasis. Microbes and Infection 9, 334–343.CrossRefGoogle ScholarPubMed
Leiby, D. A., Herron, R. M. Jr., Garratty, G. and Herwaldt, B. L. (2008). Trypanosoma cruzi parasitemia in US blood donors with serologic evidence of infection. The Journal of Infectious Diseases 198, 609–613.CrossRefGoogle ScholarPubMed
Lewis, M. D., Llewellyn, M. S., Gaunt, M. W., Yeo, M., Carrasco, H. J. and Miles, M. A. (2009). Flow cytometric analysis and microsatellite genotyping reveal extensive DNA content variation in Trypanosoma cruzi populations and expose contrasts between natural and experimental hybrids. International Journal for Parasitology (in the Press).CrossRefGoogle ScholarPubMed
Lisboa, C. V., Mangia, R. H., De Lima, N. R. C., Martins, A., Dietz, J., Baker, A. J., Ramon-Miranda, C. R., Ferreira, L. F., Fernandes, O. and Jansen, A. M. (2004). Distinct patterns of Trypanosoma cruzi infection in Leontopithecus rosalia in distinct Atlantic Coastal Rainforest fragments in Rio de Janeiro – Brazil. Parasitology 129, 703–711.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 a). 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., Lewis, M. D., Acosta, N., Yeo, M., Carrasco, H. J., Segovia, M., Vargas, J., Torrico, F., Miles, M. A., and Gaunt, M. W. (2009 b). Trypanosoma cruzi IIc: phylogenetic and phylogeographic insights from sequence and microsatellite analysis and potential impact on emergent Chagas disease. PLoS Neglected Tropical Diseases (in the Press).CrossRefGoogle ScholarPubMed
Lukes, J., Mauricio, I. L., Schonian, G., Dujardin, J.-C., Soteriadou, K., Dedet, J.-P., Kuhls, K., Tintaya, K. W. Q., Jirku, M., Chocholova, E., Haralambous, C., Pratlong, F., Obornik, M., Horak, A., Ayala, F. J. and Miles, M. A. (2007). Evolutionary and geographical history of the Leishmania donovani complex with a revision of current taxonomy. Proceedings of the National Academy of Sciences, USA 104, 9375–9380.CrossRefGoogle ScholarPubMed
Luquetti, A. O., Miles, M. A., Rassi, A., De Rezende, J. M., De Souza, A. A., Póvoa, M. M. and Rodrigues, I. (1986). Trypanosoma cruzi: zymodemes associated with acute and chronic Chagas disease in central Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 462–470.CrossRefGoogle ScholarPubMed
Machado, C. A. and Ayala, F. J. (2001). Nucleotide sequences provide evidence of genetic exchange among distantly related lineages of Trypanosoma cruzi. Proceedings of the National Academy of Sciences, USA 98, 7396–7401.CrossRefGoogle ScholarPubMed
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, 641–655.CrossRefGoogle ScholarPubMed
Marcili, A., Lima, L., Valente, V., Valente, S., Batista, J., Junqueira, A., Souza, A., Rosa, J., Campaner, M., Lewis, M., Llewellyn, M., Miles, M. and Teixeira, M. (2009 b). Comparative phylogeography of Trypanosoma cruzi TCIIc: new hosts, association with terrestrial ecotopes, and spatial clustering. Infection, Genetics and Evolution (in the Press).CrossRefGoogle ScholarPubMed
Marcili, A., Valente, V. C., Valente, S. A., Junqueira, A. C., Da Silva, F. M., Pinto, A. Y., Naiff, R. D., Campaner, M., Coura, J. R., Camargo, E. P., Miles, M. A. and Teixeira, M. M. (2009 c). Trypanosoma cruzi in Brazilian Amazonia: Lineages TCI and TCIIa in wild primates, Rhodnius spp. and in humans with Chagas disease associated with oral transmission. International Journal for Parasitology 39, 615–623.CrossRefGoogle ScholarPubMed
Mauricio, I. L., Gaunt, M. W., Stothard, J. R. and Miles, M. A. (2001). Genetic typing and phylogeny of the Leishmania donovani complex by restriction analysis of PCR amplified gp63 intergenic regions. Parasitology 122, 393–403.CrossRefGoogle ScholarPubMed
Mauricio, I. L., Gaunt, M. W., Stothard, J. R. and Miles, M. A. (2007). Glycoprotein 63 (gp63) genes show gene conversion and reveal the evolution of Old World Leishmania. International Journal for Parasitology 37, 565–576.CrossRefGoogle ScholarPubMed
Mauricio, I. L., Howard, M. K., Stothard, J. R. and Miles, M. A. (1999). Genomic diversity in the Leishmania donovani complex. Parasitology 119, 237–246.CrossRefGoogle ScholarPubMed
Mauricio, I. L., Stothard, J. R. and Miles, M. A. (2000). The strange case of Leishmania chagasi. Parasitology Today 16, 188–189.CrossRefGoogle ScholarPubMed
Mauricio, I. L., Stothard, J. R. and Miles, M. A. (2004). Leishmania donovani complex: genotyping with the ribosomal internal transcribed spacer and the mini-exon. Parasitology 128, 263–267.CrossRefGoogle ScholarPubMed
Mauricio, I. L., Yeo, M., Baghaei, M., Doto, D., Pratlong, F., Zemanova, E., Dedet, J.-P., Lukes, J. and Miles, M. A. (2006). Towards multilocus sequence typing of the Leishmania donovani complex: Resolving genotypes and haplotypes for five polymorphic metabolic enzymes (ASAT, GPI, NH1, NH2, PGD). International Journal for Parasitology 36, 757–769.CrossRefGoogle ScholarPubMed
Miles, M. A. (1972). Trypanosoma cruzi – milk transmission of infection and immunity from mother to young. Parasitology 65, 1–9.CrossRefGoogle ScholarPubMed
Miles, M. (1979). Transmission cycles and the heterogeneity of Trypanosoma cruzi. In Biology of the Kinetoplastida, Vol. 2 (ed. Lumsden, W. H. R. and Evans, D.), pp. 117–196. Academic Press, London, UK.Google Scholar
Miles, M. A. (1982). Trypanosoma cruzi: epidemiology. In Perspectives in Trypanosomiasis Research (ed. Baker, J. R.), pp. 1–15. John Wiley & Sons, London, UK.Google Scholar
Miles, M. A. (2004). The discovery of Chagas disease: progress and prejudice. Infectious Disease Clinics of North America 18, 247–260.CrossRefGoogle ScholarPubMed
Miles, M. A. (2006). New World trypanosomiasis. In Topley & Wilson's Microbiology and Microbial Infections (ed. Wakelin, D., Despommier, D. D., Gillespie, S. H. and Cox, F. E. G.), Vol. 5, pp. 376–398. London, UK.Google Scholar
Miles, M. A., Apt, B. W., Widmer, G., Povoa, M. M. and Schofield, C. J. (1984). Isozyme heterogeneity and numerical taxonomy of Trypanosoma cruzi stocks from Chile. Transactions of the Royal Society for Tropical Medicine and Hygiene 78, 526–535.CrossRefGoogle ScholarPubMed
Miles, M. A., Arias, J. R., Valente, S. A. S., Naiff, R. D., Souza, A. A., de Povoa, M. M., Lima, J. A. N., and Cedillos, R. A. (1983). Vertebrate hosts and vectors of Trypanosoma rangeli in the Amazon Basin of Brazil. American Journal of Tropical Medicine and Hygiene 32, 1251–1259.CrossRefGoogle ScholarPubMed
Miles, M., Cedillos, R., Povoa, M., De Souza, A., Prata, A. and Macedo, V. (1981 b). Do radically dissimilar Trypanosoma cruzi strains (zymodemes) cause Venezuelan and Brazilian forms of Chagas disease? The Lancet 317, 1338–1340.CrossRefGoogle Scholar
Miles, M., de Souza, A. and Povoa, M. (1981 a). Mammal trapping and nest location in Brazilian forest with an improved spool and line. Journal of Zoology 195, 331–347.CrossRefGoogle Scholar
Miles, M. A., de Souza, A. A. and Povoa, M. (1981 c). Chagas disease in the Amazon basin III. Ecotopes of ten triatomine bug species (Hemiptera: Reduviidae) from the vicinity of Belém, Pará State, Brazil. Journal of Medical Entomology 18, 266–278.CrossRefGoogle ScholarPubMed
Miles, M. A., de Souza, A., Povoa, M., Shaw, J. J., Lainson, R. and Toye, P. J. (1978). Isozymic heterogeneity of Trypanosoma cruzi in the first autochthonous patients with Chagas' disease in Amazonian Brazil. Nature, London 272, 819–821.CrossRefGoogle ScholarPubMed
Miles, M. A., Feliciangeli, M. D. and De Arias, A. R. (2003). American trypanosomiasis (Chagas disease) and the role of molecular epidemiology in guiding control strategies. British Medical Journal 326, 1444–1448.CrossRefGoogle ScholarPubMed
Miles, M. A., Lainson, R., Shaw, J. J., Povoa, M. and De Souza, A. A. (1981 d). Leishmaniasis in Brazil: XV. Biochemical distinction of Leishmania mexicana amazonensis, L. braziliensis braziliensis and L. braziliensis guyanensis – aetiological agents of cutaneous leishmaniasis in the Amazon Basin of Brazil. Transactions of the Royal Society for Tropical Medicine and Hygiene 75, 524–529.CrossRefGoogle ScholarPubMed
Miles, M., Toye, P., Oswald, S. and Godfrey, D. (1977). The identification by isoenzyme patterns of two distinct strain-groups of Trypanosoma cruzi, circulating independently in a rural area of Brazil. Transactions of the Royal Society for Tropical Medicine and Hygiene 71, 217–225.CrossRefGoogle Scholar
Miles, M. A., Yeo, M. and Mauricio, I. L. (2009). Genetics. Leishmania exploit sex. Science 324, 187–189.CrossRefGoogle ScholarPubMed
Momen, H. (1999). Taxonomy of Trypanosoma cruzi: a commentary on characterization and nomenclature. Memórias do Instituto Oswaldo Cruz 94, 181–184.CrossRefGoogle ScholarPubMed
Morel, C., Chiari, E., Camargo, E. P., Mattei, D. M., Romanha, A. J. and Simpson, L. (1980). Strains and clones of Trypanosoma cruzi can be characterized by pattern of restriction endonuclease products of kinetoplast DNA minicircles. Proceedings of the National Academy of Sciences, USA 77, 6810–6814.CrossRefGoogle ScholarPubMed
Morrison, L. J., Tweedie, A., Black, A., Pinchbeck, G. L., Christley, R. M., Schoenefeld, A., Hertz-Fowler, C., Macleod, A., Turner, C. M. and Tait, A. (2009). Discovery of mating in the major African livestock pathogen Trypanosoma congolense. PLoS ONE 4, e5564.CrossRefGoogle ScholarPubMed
Nolder, D., Roncal, N., Davies, C. R., Llanos-Cuentas, A. and Miles, M. A. (2007). Multiple hybrid genotypes of Leishmania (Viannia) in a focus of mucocutaneous leishmaniasis. American Journal of Tropical Medicine and Hygiene 76, 573–578.CrossRefGoogle Scholar
O'Connor, O., Bosseno, M. F., Barnabe, C., Douzery, E. J. and Breniere, S. F. (2007). Genetic clustering of Trypanosoma cruzi I lineage evidenced by intergenic miniexon gene sequencing. Infection, Genetics and Evolution 7, 587–593.CrossRefGoogle ScholarPubMed
Odds, F. C. and Jacobsen, M. D. (2008). Multilocus sequence typing of pathogenic Candida species. Eukaryotic Cell 7, 1075–1084.CrossRefGoogle ScholarPubMed
Pan American Health Organisation (2009). Guia para vigilância, prevenção, controle e manejo clinico da doença de Chagas aguda transmitida por alimentos., Rio de Janeiro, panaftosa.org.br/Comp/Documentacao/doc/n59-2009.Google Scholar
Pinto, A. Y., Valente, S. A., Valente Vda, C., Ferreira Junior, A. G. and Coura, J. R. (2008). Acute phase of Chagas disease in the Brazilian Amazon region: study of 233 cases from Pará, Amapá and Maranhão observed between 1988 and 2005. Revista da Sociedade Brasileira de Medicina Tropical 41, 602–614.CrossRefGoogle ScholarPubMed
Póvoa, M., De Souza, A., Naiff, R., Arias, J., Naiff, M., Biancardi, C. and Miles, M. (1984). Chagas' disease in the Amazon basin IV. Host records of Trypanosoma cruzi zymodemes in the states of Amazonas and Rondonia, Brazil. Annals of Tropical Medicine and Parasitology 78, 479–487.CrossRefGoogle ScholarPubMed
Ramirez, L. E., Lages-Silva, E., Soares Junior, J. M. and Chapadeiro, E. (1994). The hamster (Mesocricetus auratus) as experimental model in Chagas disease: parasitological and histopathological studies in acute and chronic phases of Trypanosoma cruzi infection. Revista da Sociedade Brasileira de Medicina Tropical 27, 163–169.CrossRefGoogle ScholarPubMed
Ravel, C., Cortes, S., Pratlong, F., Morio, F., Dedet, J.-P. and Campino, L. (2006). First report of genetic hybrids between two very divergent Leishmania species: Leishmania infantum and Leishmania major. International Journal for Parasitology 36, 1383–1388.CrossRefGoogle ScholarPubMed
Rioux, J. A., Lanotte, G., Serres, E., Pratlong, F., Bastien, P. and Perieres, J. (1990). Taxonomy of Leishmania. Use of isoenzymes. Suggestions for a new classification. Annales de Parasitologie Humaine et Comparée 65, 111–125.CrossRefGoogle ScholarPubMed
Roellig, D. M., Brown, E. L., Barnabe, C., Tibayrenc, M., Steurer, F. J. and Yabsley, M. J. (2008). Molecular typing of Trypanosoma cruzi isolates, United States. Emerging Infectious Diseases 14, 1123–1125.CrossRefGoogle ScholarPubMed
Rougeron, V., De Meeus, T., Hide, M., Waleckx, E., Bermudez, H., Arevalo, J., Llanos-Cuentas, A., Dujardin, J. C., De Doncker, S., Le Ray, D., Ayala, F. J. and Banuls, A. L. (2009). Extreme inbreeding in Leishmania braziliensis. Proceedings of the National Academy of Sciences, USA pp. 10224–10229.CrossRefGoogle ScholarPubMed
Rozas, M., Botto-Mahan, C., Coronado, X., Ortiz, S., Cattan, P. E. and Solari, A. (2007). Coexistence of Trypanosoma cruzi genotypes in wild and periodomestic mammals in Chile. American Journal of Tropical Medicine and Hygiene 77, 647–653.CrossRefGoogle ScholarPubMed
Sanchez-Guillen Mdel, C., Lopez-Colombo, A., Ordonez-Toquero, G., Gomez-Albino, I., Ramos-Jimenez, J., Torres-Rasgado, E., Salgado-Rosas, H., Romero-Diaz, M., Pulido-Perez, P. and Perez-Fuentes, R. (2006). Clinical forms of Trypanosoma cruzi infected individuals in the chronic phase of Chagas disease in Puebla, Mexico. Memórias do Instituto Oswaldo Cruz 101, 733–740.CrossRefGoogle ScholarPubMed
Schonian, G., Mauricio, I., Gramiccia, M., Canavate, C., Boelaert, M. and Dujardin, J. C. (2008). Leishmaniases in the Mediterranean in the era of molecular epidemiology. Trends in Parasitology 24, 135–142.CrossRefGoogle ScholarPubMed
Schwenkenbecher, J. M., Wirth, T., Schnur, L. F., Jaffe, C. L., Schallig, H., Al-Jawabreh, A., Hamarsheh, O., Azmi, K., Pratlong, F. and Schonian, G. (2006). Microsatellite analysis reveals genetic structure of Leishmania tropica. International Journal for Parasitology 36, 237–246.CrossRefGoogle ScholarPubMed
Seridi, N., Amro, A., Kuhls, K., Belkaid, M., Zidane, C., Al-Jawabreh, A. and Schonian, G. (2008). Genetic polymorphism of Algerian Leishmania infantum strains revealed by multilocus microsatellite analysis. Microbes and Infection 10, 1309–1315.CrossRefGoogle ScholarPubMed
Sherlock, I. A., Guittton, N. and Miles, M. A. (1977). Rhodnius paraensis, especie nova do Estado do Pará, Brasil (Hemiptera, Reduviidae, Triatominae). Acta Amazonica 7, 71–74.CrossRefGoogle Scholar
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, 141–152.CrossRefGoogle ScholarPubMed
Stothard, J., Frame, I. and Miles, M. (1999). Genetic diversity and genetic exchange in Trypanosoma cruzi: dual drug-resistant “progeny” from episomal transformants. Memórias do Instituto Oswaldo Cruz 94, 189–193.CrossRefGoogle ScholarPubMed
Subileau, M., Barnabe, C., Douzery, E. J., Diosque, P. and Tibayrenc, M. (2009). Trypanosoma cruzi: New insights on ecophylogeny and hybridization by multigene sequencing of three nuclear and one maxicircle genes. Experimental Parasitology, 328–337.CrossRefGoogle ScholarPubMed
Tibayrenc, M. and Ayala, F. J. (1991). Towards a population genetics of microorganisms: The clonal theory of parasitic protozoa. Parasitology Today 7, 228–232.CrossRefGoogle ScholarPubMed
Tibayrenc, M. and Miles, M. A. (1983). A genetic comparison between Brazilian and Bolivian zymodemes of Trypanosoma cruzi. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 76–83.CrossRefGoogle ScholarPubMed
Tibayrenc, M., Neubauer, K., Barnabe, C., Guerrini, F., Skarecky, D. and Ayala, F. J. (1993). Genetic characterization of six parasitic protozoa: parity between random-primer DNA typing and multilocus enzyme electrophoresis. Proceedings of the National Academy of Sciences, USA 90, 1335–1339.CrossRefGoogle ScholarPubMed
Tsukayama, P., Lucas, C. and Bacon, D. J. (2009). Typing of four genetic loci discriminates among closely related species of New World Leishmania. International Journal for Parasitology 39, 355–362.CrossRefGoogle ScholarPubMed
Vago, A. R., Andrade, L. O., Leite, A. A., D'avila Reis, D., Macedo, A. M., Adad, S. J., Tostes, S. Jr., Moreira, M. D. C. V., Filho, G. B. and Pena, S. D. J. (2000). Genetic characterization of Trypanosoma cruzi directly from tissues of patients with chronic Chagas disease: differential distribution of genetic types into diverse organs. American Journal of Pathology 156, 1805–1809.CrossRefGoogle ScholarPubMed
Valadares, H. M., Pimenta, J. R., De Freitas, J. M., Duffy, T., Bartholomeu, D. C., Oliveira Rde, P., Chiari, E., Moreira Mda, C., Filho, G. B., Schijman, A. G., Franco, G. R., Machado, C. R., Pena, S. D. and Macedo, A. M. (2008). Genetic profiling of Trypanosoma cruzi directly in infected tissues using nested PCR of polymorphic microsatellites. International Journal for Parasitology 38, 839–850.CrossRefGoogle ScholarPubMed
Valente, S. A., Da Costa Valente, V., Das Neves Pinto, A. Y., De Jesus Barbosa Cesar, M., Dos Santos, M. P., Miranda, C. O., Cuervo, P. and Fernandes, O. (2009). Analysis of an acute Chagas disease outbreak in the Brazilian Amazon: human cases, triatomines, reservoir mammals and parasites. Transactions of the Royal Society of Tropical Medicine and Hygiene 103, 291–297.CrossRefGoogle ScholarPubMed
Valente, V. C., Valente, S. A., Noireau, F., Carrasco, H. J. and Miles, M. A. (1998). Chagas disease in the Amazon Basin: association of Panstrongylus geniculatus (Hemiptera: Reduviidae) with domestic pigs. Journal of Medical Entomology 35, 99–103.CrossRefGoogle ScholarPubMed
Virreira, M., Alonso-Vega, C., Solano, M., Jijena, J., Brutus, L., Bustamante, Z., Truyens, C., Schneider, D., Torrico, F., Carlier, Y. and Svoboda, M. (2006 a). Congenital chagas disease in Bolivia is not associated with DNA polymorphism of Trypanosoma cruzi. American Journal of Tropical Medicine and Hygiene 75, 871–879.CrossRefGoogle Scholar
Virreira, M., Serrano, G., Maldonado, L. and Svoboda, M. (2006 b). Trypanosoma cruzi: typing of genotype (sub)lineages in megacolon samples from Bolivian patients. Acta Tropica 100, 252–255.CrossRefGoogle ScholarPubMed
Volf, P. and Sadlova, J. (2009). Sex in Leishmania. Science 324, 1644.CrossRefGoogle ScholarPubMed
Weatherly, D. B., Boehlke, C. and Tarleton, R. L. (2009). Chromosome level assembly of the hybrid Trypanosoma cruzi genome. BMC Genomics 10, 255.CrossRefGoogle ScholarPubMed
Wells, K., Pfeiffer, M., Lakim, M. B. and Kalko, E. K. (2006). Movement trajectories and habitat partitioning of small mammals in logged and unlogged rain forests on Borneo. Journal of Animal Ecology 75, 1212–1223.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.CrossRefGoogle ScholarPubMed
Yeo, M., Acosta, N., Llewellyn, M., Sanchez, H., Adamson, S., Miles, G. A. J., Lopez, E., Gonzalez, N., Patterson, J. S. and Gaunt, M. W. (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
Zemanova, E., Jirku, M., Mauricio, I. L., Horak, A., Miles, M. A. and Lukes, J. (2007). The Leishmania donovani complex: genotypes of five metabolic enzymes (ICD, ME, MPI, G6PDH, and FH), new targets for multilocus sequence typing. International Journal for Parasitology 37, 149–160.CrossRefGoogle ScholarPubMed