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

Parasitology

Volumn 136, Issue 12, 2009, Pages 1509-1528

  Miles, M A ^a   Llewellyn, M S ^a   Lewis, M D ^a   Yeo, M ^a   Baleela, R ^a   Fitzpatrick, S ^a   Gaunt, M W ^a   Mauricio, I L ^a  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

Author keywords

Chagas disease; Genetic exchange; Leishmania; Microsatellites; Molecular epidemiology; Multilocus sequence typing; Pericardial effusion; Phylogeography; Taxonomy; Trypanosoma cruzi

Indexed keywords

MICROSATELLITE DNA; PLASMID VECTOR;

BRAZIL; CHAGAS DISEASE; CLONAL VARIATION; COMPARATIVE GENOMIC HYBRIDIZATION; DISEASE ASSOCIATION; DISEASE CONTROL; DISEASE TRANSMISSION; GENE SEQUENCE; GENETIC HETEROGENEITY; GENETIC MARKER; GENETIC RECOMBINATION; GENETIC VARIABILITY; GENETICS; GENOMICS; GEOGRAPHIC DISTRIBUTION; KARYOTYPE; LEISHMANIA; MARKER GENE; MOLECULAR EPIDEMIOLOGY; MOLECULAR GENETICS; NOMENCLATURE; NONHUMAN; PANDEMIC; PARASITOLOGY; PATHOGENESIS; PERICARDIAL EFFUSION; PHYLOGEOGRAPHY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; REVIEW; SKIN LEISHMANIASIS; TAXONOMY; TRANSGENIC ORGANISM; TRANSGENICS; TRYPANOSOMA CRUZI; VENEZUELA; VISCERAL LEISHMANIASIS; ZOONOSIS;

ANIMALS; CHAGAS DISEASE; ECOSYSTEM; LEISHMANIA; LEISHMANIASIS; MOLECULAR EPIDEMIOLOGY; PHYLOGENY; SOUTH AMERICA; TRYPANOSOMA CRUZI;

PHLEBOTOMINAE; PROTOZOA; TRYPANOSOMA CRUZI;

EID: 70350439244     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182009990977     Document Type: Review

References (119)

1. Aanensen, D. M. and Spratt, B. G. (2005). The multilocus sequence typing network: mlstfinet. Nucleic Acids Research 33, 728-733.
2. Acquatella, H. (2007). Echocardiography in Chagas heart disease. Circulation 115, 1124-1131.
3. 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.
4. 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 .y vector. Science 324, 265-268.
5. 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.
6. 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.
7. Anon, A. (1999). Recommendations from a satellite meeting. Memórias do Instituto Oswaldo Cruz 94, 429-432.
8. Ashford, R. W. (2000). The leishmaniases as emerging and reemerging zoonoses. International Journal for Parasitology 30, 1269-1281.
9. 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.
10. Barnabé , C., Neubauer, K., Solari, A. and Tibayrenc, M. (2001a). 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.
11. Barnabé , C., Yaeger, R., Pung, O. and Tibayrenc, M. (2001b). 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.
12. 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.
13. 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.
14. 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.
15. 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.
16. 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.
17. 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.
18. 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.
19. 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.
20. 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.
21. Campbell, D., Westenberger, S. and Sturm, N. (2004). The determinants of Chagas disease: connecting parasite and host genetics. Current Molecular Medicine 4, 549-562.
22. Cardinal, M. V., Lauricella, M. A., Ceballos, L. A., Lanati, L., Marcet, P. L., Levin, M. J., Kitron, U., Gü rtler, 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.
23. 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.
24. 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.
25. Chapman, M., Baggaley, R., Godfrey-Fausset, P., Malpas, T., White, G., Canese, J. and Miles, M. (1984). Trypanosoma cruzi from the Paraguayan Chaco: isoenzyme pro.les of strains isolated at Makthlawaiya. Journal of Protozoology 31, 482-486.
26. 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.
27. 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.
28. 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.
29. 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.
30. 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.
31. 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.
32. 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.
33. 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.
34. 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.
35. 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.
36. 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.
37. Evans, D., Kennedy, W., Elbihari, S., Chapman, C., Smith, V. and Peters, W. (1987). Hybrid formation within the genus Leishmania? Parassitologia 29, 165-173.
38. 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.
39. 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.
40. 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.
41. 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.
42. Heitman, J. (2006). Sexual reproduction and the evolution of microbial pathogens. Current Biology 16, R711-R725.
43. 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.
44. 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.
45. 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.
46. Ko., 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.
47. 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 .ow among European populations of Leishmania infantum MON-1. PLoS Neglected Tropical Diseases 2, e261.
48. 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.
49. 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.
50. 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).
51. 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.
52. 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. (2009a). 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.
53. 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. (2009b). 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).
54. 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.
55. 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.
56. 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.
57. 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. (2009a). 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.
58. 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. (2009b). Comparative phylogeography of Trypanosoma cruzi TCIIc: new hosts, association with terrestrial ecotopes, and spatial clustering. Infection, Genetics and Evolution (in the Press).
59. Marcili, A., Valente, V. C., Valente, S. A., Junqueira, A. C., Da Silva, F. M., Pinto, A. Y., Nai., R. D., Campaner, M., Coura, J. R., Camargo, E. P., Miles, M. A. and Teixeira, M. M. (2009c). 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.
60. 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 ampli.ed gp63 intergenic regions. Parasitology 122, 393-403.
61. 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.
62. 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.
63. Mauricio, I. L., Stothard, J. R. and Miles, M. A. (2000). The strange case of Leishmania chagasi. Parasitology Today 16, 188-189.
64. 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.
65. 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 .ve polymorphic metabolic enzymes (ASAT, GPI, NH1, NH2, PGD). International Journal for Parasitology 36, 757-769.
66. Miles, M. A. (1972). Trypanosoma cruzi - milk transmission of infection and immunity from mother to young. Parasitology 65, 1-9.
67. 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.
68. Miles, M. A. (1982). Trypanosoma cruzi: epidemiology. In Perspectives in Trypanosomiasis Research (ed. Baker, J. R.), pp. 1-15. John Wiley & Sons, London, UK.
69. Miles, M. A. (2004). The discovery of Chagas disease: progress and prejudice. Infectious Disease Clinics of North America 18, 247-260.
70. 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.
71. Miles, M. A., Apt, B. W., Widmer, G., Povoa, M. M. and Scho.eld, 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.
72. Miles, M. A., Arias, J. R., Valente, S. A. S., Nai., 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.
73. Miles, M., Cedillos, R., Povoa, M., De Souza, A., Prata, A. and Macedo, V. (1981b). Do radically dissimilar Trypanosoma cruzi strains (zymodemes) cause Venezuelan and Brazilian forms of Chagas disease? The Lancet 317, 1338-1340.
74. Miles, M., de Souza, A. and Povoa, M. (1981a). Mammal trapping and nest location in Brazilian forest with an improved spool and line. Journal of Zoology 195, 331-347.
75. Miles, M. A., de Souza, A. A. and Povoa, M. (1981c). 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.
76. 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.
77. 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.
78. Miles, M. A., Lainson, R., Shaw, J. J., Povoa, M. and De Souza, A. A. (1981d). 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.
79. 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.
80. Miles, M. A., Yeo, M. and Mauricio, I. L. (2009). Genetics. Leishmania exploit sex. Science 324, 187-189.
81. Momen, H. (1999). Taxonomy of Trypanosoma cruzi: a commentary on characterization and nomenclature. Memórias do Instituto Oswaldo Cruz 94, 181-184.
82. 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 DNAminicircles. Proceedings of the National Academy of Sciences, USA 77, 6810-6814.
83. 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.
84. 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.
85. 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.
86. Odds, F. C. and Jacobsen, M. D. (2008). Multilocus sequence typing of pathogenic Candida species. Eukaryotic Cell 7, 1075-1084.
87. 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.
88. 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.
89. Póvoa, M., De Souza, A., Nai., R., Arias, J., Nai., 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.
90. 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.
91. 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.
92. 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.
93. 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.
94. 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.
95. 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.
96. 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.
97. 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.
98. 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.
99. 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.
100. 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.
101. Souto, R. P., Fernandes, O., Macedo, A. M., Campbell, D. A. and Zingales, B. (1996). DNA markers de.ne two major phylogenetic lineages of Trypanosoma cruzi. Molecular and Biochemical Parasitology 83, 141-152.
102. 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.
103. 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.
104. Tibayrenc, M. and Ayala, F. J. (1991). Towards a population genetics of microorganisms: The clonal theory of parasitic protozoa. Parasitology Today 7, 228-232. (Pubitemid 121003512)
105. 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.
106. 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.
107. 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.
108. 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.
109. Valadares, H. M., Pimenta, J. R., De Freitas, J. M., Du.y, 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 pro.ling of Trypanosoma cruzi directly in infected tissues using nested PCR of polymorphic microsatellites. International Journal for Parasitology 38, 839-850.
110. 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.
111. 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.
112. Virreira, M., Alonso-Vega, C., Solano, M., Jijena, J., Brutus, L., Bustamante, Z., Truyens, C., Schneider, D., Torrico, F., Carlier, Y. and Svoboda, M. (2006a). Congenital chagas disease in Bolivia is not associated with DNA polymorphism of Trypanosoma cruzi. American Journal of Tropical Medicine and Hygiene 75, 871-879.
113. Virreira, M., Serrano, G., Maldonado, L. and Svoboda, M. (2006b). Trypanosoma cruzi: typing of genotype (sub)lineages in megacolon samples from Bolivian patients. Acta Tropica 100, 252-255.
114. Volf, P. and Sadlova, J. (2009). Sex in Leishmania. Science 324, 1644.
115. Weatherly, D. B., Boehlke, C. and Tarleton, R. L. (2009). Chromosome level assembly of the hybrid Trypanosoma cruzi genome. BMC Genomics 10, 255.
116. 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.
117. Westenberger, S. J., Barnabe, C., Campbell, D. A. and Sturm, N. R. (2005). Two Hybridization events de.ne the population structure of Trypanosoma cruzi. Genetics, 171, 527-543.
118. 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.
119. Zemanova, E., Jirku, M., Mauricio, I. L., Horak, A., Miles, M. A. and Lukes, J. (2007). The Leishmania donovani complex: genotypes of .ve metabolic enzymes (ICD, ME, MPI, G6PDH, and FH), new targets for multilocus sequence typing. International Journal for Parasitology 37, 149-160.