Trypanosoma cruzi: Genetic structure of populations and relevance of genetic variability to the pathogenesis of chagas disease

Memorias do Instituto Oswaldo Cruz

Volumn 99, Issue 1, 2004, Pages 1-12

  Macedo, Andréa M ^a   Machado, Carlos R ^a   Oliveira, Riva P ^b   Pena, Sérgio D J ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Chagas disease; Genetic variability; Mismatch repair; Pathogenesis; Population structure; Trypanosoma cruzi

Indexed keywords

MICROSATELLITE DNA; RIBOSOME DNA;

CELL LINEAGE; CHAGAS DISEASE; DISEASE ACTIVITY; DISEASE COURSE; DISEASE SEVERITY; DNA POLYMORPHISM; EXON; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GENOMICS; HOST PARASITE INTERACTION; HUMAN; KARYOTYPING; MISMATCH REPAIR; NONHUMAN; PARASITE VIRULENCE; PATHOGENESIS; POLYMERASE CHAIN REACTION; POPULATION GENETIC STRUCTURE; PROTOZOAL GENETICS; RANDOM AMPLIFIED POLYMORPHIC DNA; REVIEW; STATISTICAL SIGNIFICANCE; STRAIN IDENTIFICATION; SYMPTOMATOLOGY; TRYPANOSOMA CRUZI;

PROTOZOA; TRYPANOSOMA; TRYPANOSOMA CRUZI;

EID: 1642444868     PISSN: 00740276     EISSN: None     Source Type: Journal    
DOI: 10.1590/S0074-02762004000100001     Document Type: Review

References (111)

1. Adad SJ, Andrade DCS, Lopes ER 1991. Contribuição ao estudo da anatomia patológica do megaesôfago chagásico. Rev Inst Med Trop São Paulo 33: 443-450.
2. Alves AM, de Almeida DF, von Kruger WM 1996. Genomic variation in Trypanosoma cruzi clonal cultures. Parasitol Res 82: 410-415.
3. Amato Neto V, Pasternak J, Matsubara L, Hammerschlak N, Carignani FL 1996. Trials for the use of gamma rays in the prevention of Trypanosoma cruzi transfusion infection. Rev Soc Bras Med Trop 29: 613-614.
4. Andrade LO, Machado CRS, Chiari E, Pena SDJ, Macedo AM 1999. Genetic variability of Trypanosoma cruzi implications for the pathogenesis of Chagas disease. Mol Bioch Parasitol 100: 163-172.
5. Andrade SG 1974. Caracterização de cepas de Trypanosoma cruzi isoladas no Recôncavo Baiano. Ver Patol Trop 3: 65-121.
6. Andrade SG, Magalhães JB 1997. Biodemes and zymodemes of Trypanosoma cruzi strains: correlations with clinical data and experimental pathology. Rev Soc Bras Med Trop 30: 27-35.
7. Arruda MV, Reinach FC, Colli W, Zingales B 1990. Sequence of 24S ribosomal RNA gene and characterization of a corresponding pseudogene from Trypanosoma cruzi. Mol Biochem Parasitol 40: 35-42.
8. Augusto-Pinto L, Pimenta JR, Teixeira SMR, Fernandes O, Chiari E, Pena SDJ, Macedo AM, Machado CR 2003. Multilocus genotype data provide evidences that hybrid Trypanosoma cruzi strains constitute a third major lineage. Int J Parasitol in press.
9. Ayala FJ 1993. Trypanosoma and Leishmania have clonal population structures of epidemiological significance. Biol Res 26: 47-63.
10. Barret TV, Hoff RH, Mott KE, Miles MA, Godfrey DG, Teixeira R, Almeida de Souza JA, Sherlock IA 1980. Epidemiological aspects of tree Trypanosoma cruzi: two types of parsite populations presenting distinct characteristics. PAHO Scientific Pub 347: 11-21.
11. Bogliolo AR, Lauria-Pires L, Gibson WC 1996. Polymorphisms in Trypanosoma cruzi: evidence of genetic recombination. Acta Trop 61: 31-40.
12. Borst P, Greaves D 1986. Discontinuous transcription and antigenic variation in trypanosomes. Annu Rev Biochem 55: 701-732.
13. Brandariz S, Schijman A, Vigliano C, Arteman P, Viotti R, Beldjord C, Levin MJ 1995. Detection of parasite DNA in Chagas' heart disease. Lancet 346: 1370-1371.
14. Brener Z 1987. Pathogenesis and immunopathology of chronic Chagas disease. Mem Inst Oswaldo Cruz 82: 205-212.
15. Brener Z 1992. Immune Response and Immunopathology in Trypanosoma cruzi Infection Chagas Disease (American Trypanosomiasis): its Impact on Transfusion and Clinical Medicine, ISBT Brazil'92, São Paulo, p. 31-47.
16. Briones MR, Souto RP, Stolf BS, Zingales 1999. The evolution of the two Trypanosoma cruzi subgroups inferred from rRNA genes can be correlated with the interchange of American mammalian faunas in the cenozoic and has implications to pathogenicity and host specificity. Mol Biochem Parasotol 104: 219-232.
17. Brisse S, Dujardin JC, Tibayrenc M 2000. Identification of six Trypanosoma cruzi lineages by sequence-characterised amplified region markers. Mol Biochem Parasitol 111: 95-105.
18. Brisse S, Verhoef J, Tibayrenc M 2001. Characterisation of large and small subunit rRNA and mini-exon genes further supports the distinction of six Trypanosoma cruzi lineages. Int J Parasitol 31: 1218-26.
19. Buscaglia CA, Di Noia JM 2003. Trypanosoma cruzi clonal diversity and the epidemiology of Chagas disease. Microbes Infect 5: 419-421.
20. Carneiro M, Chiari E, Gonçalves AM, Pereira AAS, Morel C, Romanha AJ 1990. Changes in the isoenzyme and kinetoplast DNA patterns of Trypanosoma cruzi strains induced by maintenance in mice. Acta Trop 47: 35-45.
21. Carrasco HJ, Frame IA, Valente SA, Miles MA 1996. Genetic exchange as a possible source of genomic diversity in sylvatic populations of Trypanosoma cruzi. Am J Trop Med Hyg 54: 418-424.
22. Clark CG, Pung OJ 1994. Host specificity of ribosomal DNA variation in sylvatic Trypanosoma cruzi from North America. Mol Biochem Parasitol 66: 175-179.
23. Deane MP, Sousa MA, Pereira NP, Gonçalves AM, Momen H, Morel C 1984. Trypanosoma cruzi: inoculation schedules and re-isolation methods selected individual strains from doubly infected mice, as demonstrated by schizodeme and zymodeme analyses. J Protozool 31: 276-280.
24. Devera R, Fernandes O, Coura JR 2003. Should Trypanosoma cruzi be called "cruzi" complex? A review of the parasite diversity and the potential of selecting population after in vitro culturing and mice infection. Mem Inst Oswaldo Cruz 98: 1-12.
25. Dias JCP 1992. Epidemiology of Chagas disease. In S Wendel, Z Brener, M S Camargo, A Rassi (eds), Chagas Disease (American Trypanosomiasis): its Impact on Transfusion and Clinical Medicine, ISBTBrazil'92, São Paulo, p. 49-80.
26. Dias Neto E, Steindel M, Passos LK, de Souza CP, Rollinson D, Katz N, Romanha AJ, Pena SD, Simpson AJ 1993. The use of RAPDs for the study of the genetic diversity of Schistosoma mansoni and Trypanosoma cruzi. EXS 67: 339-345.
27. Dujardin JC, Dujardin JP, Tibayrenc M, Timperman G, De Doncker S, Jacquet D, Arevalo J, Llanos-Cuentas A, Guerra H, Bermudez H 1995. Karyotype plasticity in neotropical Leishmania: an index for measuring genomic distance among L. (V.) peruviana and L. (V.) braziliensis populations. Parasitology 110: 21-30.
28. Ebert F 1982. The identication of two main-groups of Trypanosoma cruzi stocks from Brazil by their isoenzyme patterns of isoelectrofocusing. Tropenmed Parasitol 33: 140-146.
29. Fernandes O, Mangia RH, Lisboa CV, Pinho AP, Morel CM, Zingales B, Campbell DA, Jansen AM 1999. The complex-ity 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: 161-166.
30. Fernandes O, Santos SS, Cupolillo E, Mendonça B, Derre R, Junqueira ACV, Santos LC, Sturm NR, Naiff RD, Barrett TB, Campbell DA, Coura JR 2001. A mini-exon multiplex polymerase chain reaction to distinguish the major groups of Trypanosoma cruzi and T rangeli in the Brazilian Amazon. Trans R Soc Trop Med Hyg 95: 97-99.
31. Fernandes O, Sturm NR, Derre R, Campbell DA 1998. The mini-exon gene: a genetic marker for zymodeme III of Trypanosoma cruzi. Mol Biochem Parasitol 95: 129-133.
32. Fujieda S, Tanaka N, Sunaga H, Noda I, Sugimoto C, Tsuzuki H, Saito H 1998. Expression of hMSH2 correlates with in vitro chemosensitivity to CDDP cytotoxicity in oral and oropharyngeal carcinoma. Cancer Lett 132: 37-44.
33. Gaunt MW, Yeo M, Frame IA, Stothard JR, Carrasco HJ, Taylor MC, Mena SS, Veazey P, Miles GA, Acosta N, de Arias AR, Miles MA 2003. Mechanism of genetic exchange in American trypanosomes. Nature 421: 936-939.
34. Gibson W, Stevens J 1999. Genetic exchange in the trypanosomatidae. Adv Parasitol 43: 1-46
35. Henriksson J, Dujardin JC, Barnabe C, Brisse S, Timperman G, Venegas J, Pettersson U, Tibayrenc M, Solari A 2002. Chromosomal size variation in Trypanosoma cruzi is mainly progressive and is evolutionarily informative. Parasitology 124: 277-286.
36. Henriksson J, Porcel B, Rydaker M, Ruiz A, Sabaj V, Galanti N, Cazzulo JJ, Frasch AC, Pettersson U 1995. Chromosome specific markers reveal conserved linkage groups in spite of extensive chromosomal size variation in Trypanosoma cruzi. Mol Biochem Parasitol 73: 63-74.
37. Henriksson J, Solari A, Rydaker M, Sousa OE, Pettersson U 1996. Karyotype variability in Trypanosoma rangeli. Parasitology 112: 385-391.
38. Hernandez R, Rios P, Valdes AM, Pinero D R 1990. Primary structure of Trypanosoma cruzi small-subunit RNA coding region: comparison with other trypanosomatids. Mol Biochem Parasitol 41: 207-212.
39. Higo H, Yanagi T, Matta V, Agatsuma, Cruz-Reyes A, Uyema N, Monroy C, Kanbara H, Tada I 2000. Genetic structure of Trypanosoma cruzi in american continents: special emphasis on sexual reproduction in Central America. Parasitology 121: 403-408.
40. Higuchi ML, Gutierrez PS, Aiello VD, Palomino S, Bocchi E, Kalil J, Bellotti G, Pileggi F 1993. Correlation between Trypanosoma cruzi parasitism and myocardial inflammatory infiltrate in human chronic chagasic myocarditis: light microscopy and immunohistochemical findings. Cardiovasc Pathol 2: 101-105.
41. Hsieh P 2001. Molecular mechanisms of DNA mismatch repair. Mutat Res 486: 71-87.
42. Jones EM, Colley DJ, Tostes S, Lopes ER, Vnencak-Jones CL, McCurley TL 1993. Amplification of a Trypanosoma cruzi DNA sequence from inflammatory lesions in human chagasic cardiomyopathy. Am J Trop Med Hyg 48: 348-357.
43. Kalil J, Cunha-Neto E 1996. Autoimmunity in Chagas disease cardiomyopathy: fulfilling the criteria at last? Parasitol Today 12: 396-399.
44. Kawashita SY, Sanson GF, Fernandes O, Zingales B, Briones MR 2001. Maximum-likelihood divergence date estimates based on rRNA gene sequences suggest two scenarios of Trypanosoma cruzi intraspecific evolution. Mol Biol Evol 18: 2250-2259.
45. Köeberle F 1968. Chagas disease and Chagas syndromes: the pathology of American trypanosomiasis. Adv Parasitol 6: 63-116.
46. Lambrech FL 1965. Biological variations in trypanosomes and their relation to the epidemiology of Chagas' disease. Rev Inst Med Trop São Paulo 7: 346-352.
47. LeClerc JE, Li B, Payne WL, Cebula TA 1996. High mutation frequencies among Escherichia coli and Salmonella pathogens. Science 274: 1208-1211.
48. Leon W, Foutz DL, Manning J 1978. Sequence arrangement of 16S and 26S rRNA genes in the pathogenic haemoflagellate Leishmania donovani. Nucleic Acids Res 5: 491-504.
49. Lopes ER, Rocha A, Meneses AC, Lopes MAB, Fatureto MC, Lopes GP, Chapadeiro E 1989. Prevalência de megas em necrópsias realizadas no Triângulo Mineiro no período de 1954 a 1988. Rev Soc Bras Med Trap 22: 211-215.
50. Luquetti AO, Miles MA, Rassi A, de Rezende JM, de Souza AA, Povoa MM, Rodrigues I 1986. Trypanosoma cruzi: zymodemes associated with acute and chronic Chagas' disease in central Brazil. Trans R Soc Trop Med Hyg 80: 462-470.
51. Macedo AM, Martins MS, Chiari E, Pena SDJ 1992. DNA finger-printing of Trypanosoma cruzi: a new tool for characterization of strains and clones. Mol Biochem Parasitol 55: 147-154.
52. Macedo AM, Pena SDJ 1998. Genetic variability of Trypanosoma cruzi: implications for the pathogenesis of Chagas disease. Parasitol Today 14: 119-123.
53. Macedo AM, Pimenta JR, Aguiar RS, Melo AI, Chiari E, Zingales B, Pena SD, Oliveira RP AM 2001. Usefulness of Microsatellite Typing in Population Genetic Studies of Trypanosoma cruzi. Mem Inst Oswaldo Cruz 96: 407-413.
54. Machado CA, Ayala FJ 2001. Nucleotide sequences provide evidence of genetic exchange among distantly related lineages of Trypanosoma cruzi. Proc Natl Acad Sci USA 98: 7396-7401
55. Machado CA, Ayala FJ 2002. Sequence variation in the dihydrofolate reductase-thymidylate synthase (DHFR-TS) and trypanothione reductase (TR) genes of Trypanosoma cruzi. Mol Biochem Parasitol 121: 33-47.
56. Marques-Araújo, Chiari E 1988. Caracterização biológica de clones das cepas Y, CL e MR de Trypanosoma cruzi em camun-dongos C3H isogênicos. Mem Inst Oswaldo Cruz 83: 175-181.
57. Miles MA, Apt BW, Widmer G, Povoa MM, Schofield CJ 1984. Isoenzyme heterogeneity and numerical taxonomy of Trypanosoma cruzi stocks from Chile. Trans R Soc Trop Med Hyg 78: 526-535.
58. Miles MA, Lanhan SM, de Souza AA, Povoa DG 1980. Further enzymic characters of Trypanosoma cruzi and their evaluation for strain identification. Trans R Soc Trop Med Hyg 74: 221-242.
59. Miles MA, Souza AA, Povoa M, Shaw JJ, Lainson R, Toye PJ 1978. Isozymic heterogeneity of Trypanosoma cruzi in the first autochthonous patients with Chagas' disease in Amazonian Brazil. Nature 272: 819-821.
60. Miles MA, Toye PJ, Oswald SC, Godfrey DG et al 1977. The identification by isoenzyme patterns of two distinct strain groups of Trypanosoma cruzi, circulating independently in a rural area of Brazil. Trans R Soc Trop Med Hyg 71: 217-225.
61. Momen H 1999. Taxonomy of Trypanosoma cruzi: a commentary on characterization and nomenclature. Mem Inst Oswaldo Cruz 94: 181-184.
62. Morel C, Chiari E, Camargo EP, Mattei DM, Romanha AJ, Simpson L 1980. Strains and clones of Trypanosoma cruzi can be characterized by pattern of restriction endonuclease products of kinetoplast DNA minicircles. Proc Natl Acad Sci USA 77: 6810-6814.
63. Muhlpfordt H, Berger J 1990. Characterization and grouping of Trypanosoma cruzi stocks by DNA base-specific fluorochromes and discriminate analysis. Parasitol Res 76: 319-325.
64. Murthy VK, Dibbern KM, Campbell DA 1992. PCR amplification of mini-exon genes differentiates Trypanosoma cruzi from Trypanosoma rangeli. Mol Cell Probes 6: 237-243.
65. Nunes LR, de Carvalho MR, Buck GA 1997. Trypanosoma cruzi strains partition into two groups based on the structure and function of the spliced leader RNA and rRNA gene promoters. Mol Biochem Parasitol 86: 211-224.
66. Oliveira RP 1997. Estudos Genéticos e Evolucionários do Trypanosoma cruzi, PhD Thesis, Universidade Federal de Minas Gerais, Belo Horizonte.
67. Oliveira RP, Broude NE, Macedo AM, Cantor CR, Smith CL, Pena SDJ 1998. Probing the genetic population structure of Trypanosoma cruzi with polymorphic microsatellites. Proc Natl Acad Sci USA 95: 3776-3780.
68. Oliveira RP, Macedo AM, Chiari E, Pena SDJ 1997. An alternative approach to evaluating the intraspecific genetic variability of parasites. Parasitol Today 13: 196-200.
69. Oliveira RP, Melo AIR, Macedo AM, Chiari E, Pena SDJ 1999. The population structure of Trypanosorna cruzi: expanded analysis of 54 strains using eight polymorphic CA-repeat microsatellites. Mem Inst Oswaldo Cruz 94: 65-70.
70. Palacius-Pru E, Carrasco H, Scorza C, Espinoza R 1989. Ultra-structural characteristics of different stages of human chagasic myocarditis. Am J Trop Med Hyg 41: 29-40.
71. Pedroso A, Cupolillo E, Zingales B 2003. Evaluation of Trypanosoma cruzi hybrid stocks based on chromosomal size variation. Mol Biochem Parasitol 129: 79-90.
72. Peltomaki P 2003. Role of DNA mismatch repair defects in the pathogenesis of human cancer. J Clin Oncol 21: 1174-1179.
73. Pena, SDJ, Simpson AJG 1996. Sequence-specific gene signatures produced by LSSP-PCR. In U Landegren, Laboratory Protocols for Mutation Detection, Oxford University Press, Oxford, p. 42-47.
74. Pena SD, Barreto G, Vago AR, De Marco L, Reinach FC, Dias Neto E, Simpson AJ 1994. Sequence-specific "gene signatures" can be obtained by PCR with single specific primers at low stringency. Proc Natl Acad Sci USA 91: 1946-1949.
75. Pimenta JR 2002. Análises Filogenéticas Populacionais em T. cruzi a Partir de Estudos de Microssatélites Polimórficos de DNA, PhD Thesis, Universidade Federal de Minas Gerais, Belo Horizonte.
76. Porcile PE, Santos MR, Souza RT, Verbisck NV, Brandao A, Urmenyi T, Silva R, Rondinelli E, Lorenzi H, Levin MJ, Degrave W, Franco da Silveira J 2003. A refined molecular karyotype for the reference strain of the Trypanosoma cruzi genome project (clone CL Brener) by assignment of chromosome markers. Gene 308: 53-65.
77. Prata A 2001. Clinical and epidemiological aspects of Chagas disease. Lancet Infec Dis 1: 92-100.
78. Romanha AJ, Pereira da Silva AA, Chiari E, Kilgour, V 1979. Isoenzyme patterns of cultured Trypanosoma cruzi: changes after prolonged subculture. Comp Biochem Physiol 62B: 139-142.
79. Santos, FR, Pandya, A, Tyler-Smith, C, Pena, SDJ, Schanfield, M, Leonard, WR, Osipova, L, Crawford, MH, Mitchell, RJ 1999. The central Siberian origin for native American chromosomes. Am J Hum Genet 64: 619-628.
80. Santos MR, Cano MI, Schijman A, Lorenzi H, Vazquez M, Levin MJ, Ramirez JL, Brandão A, Degrave WM, da Silveira JF 1997. The Trypanosoma cruzi genome project: nuclear karyotype and gene mapping of clone CL Brener. Mem Inst Oswaldo Cruz 92: 821-828.
81. Satellite Meeting 1999. Recommendations from a satellite meeting. Mem Inst Oswaldo Cruz 94: 429-432.
82. Schmuñis, GA 1987. Autoimmunity in Chagas' disease. Mem Inst Oswaldo Cruz 82: 287-310.
83. Schon I, Martens K 2003. No slave to sex. Proc R Soc Lond B Biol Sci 270: 827-833.
84. Schottelius J 1982. The identification by lecitins of two strain groups of Trypanosoma cruzi. Z Parasitenk 68: 147-154.
85. Skaletsky H, Kuroda-Kawaguchi T, Minx PJ, Cordum HS, Hillier L, Brown LG, Repping S, Pyntikova T, Ali J, Bieri T, Chinwalla A, Delehaunty A, Delehaunty K, Du H, Fewell G, Fulton L, Fulton R, Graves T, Hou SF, Latrielle P, Leonard S, Mardis E, Maupin R, McPherson J, Miner T, Nash W, Nguyen C, Ozersky P, Pepin K, Rock S, Rohlfing T, Scott K, Schultz B, Strong C, Tin-Wollam A, Yang SP, Waterston RH, Wilson RK, Rozen S, Page DC 2003. The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423: 825-837.
86. Souto RP, Zingales B 1993. Sensitive detection and strain classification of Trypanosoma cruzi by amplification of a ribosomal RNA sequence. Mol Biochem Parasitol 62: 45-52.
87. Souto RP, Fernandes O, Macedo AM, Campbell, Zingales B 1996. DNA markers define two major phylogenetic lineages of Trypanosoma cruzi. Mol Biochem Parasitol 83: 141-152.
88. Steindel M, Dias Neto E, Menezes C, Romanha A, Simpson AJG 1993. Random amplified polymorphic DNA analysis of Trypanosoma cruzi strains. Mol Biochem Parasitol 60: 71-80.
89. Stothard J, Frame I, Miles M 1999. Genetic diversity and genetic exchange in Trypanosoma cruzi: dual drug-resistant "progeny" from episomal transformants. Mem Inst Oswaldo Cruz 94: 189-193.
90. Sturm NR, Vargas NS, Westenberger SJ, Zingales B, Campbell DA 2003. Evidence for multiple hybrid groups in Trypanosoma cruzi. Int J Parasitol 33: 269-279.
91. Tait A 1980. Evidence for diploidy and mating in trypanosomes. Nature 287: 536-538.
92. Takeda GK, Campos R, Kieffer J, Moreira AA, Amato Neto V, Castilho VL, Pinto PL, Duarte MI 1986. Ação de raios gama sobre formas sanguícolas de Trypanosoma cruzi. Estudo experimental em camundongos. Rev Inst Med Trop Sao Paula 28: 15-18.
93. Tanowitz HB 1992. Chagas disease. Clin Microbiol 5: 400-419.
94. Tibayrenc M 1995. Population genetics of parasitic protozoa and other microorganisms. Adv Parasitol 36: 47-115.
95. Tibayrenc M 1998. Genetic epidemiology of parasitic protozoa and other infectious agents: the need for an integrated approach. Int J Parasitol 28: 85-104.
96. Tibayrenc M, Ayala FJ 1987. High correlation between isoenzyme classification and kinetoplast DNA variability in Trypanosoma cruzi. C R Acad Scu III 304: 89-92.
97. Tibayrenc M, Ayala F 1988. Isoenzyme variability of Trypanosoma cruzi, the agent of Chagas' disease: genetic, taxonomic and epidemiological significance. Evolution 42: 277-292.
98. Tibayrenc M, Miles MA 1983. A genetic comparison of Brazilian and Bolivian zymodemes of Trypanosoma cruzi. Trans R Soc Trop Med Hyg 77: 76-83.
99. Tibayrenc M, Echalar L, Dujardin, P Poch O, Desjeux P 1984. The microdistribution of isoenzymic strains of Trypanosoma cruzi in Southern Bolivia: new isoenzyme profiles and futher arguments against Mendelian sexuality. Trans R Soc Trop Med Hyg 78: 519-525.
100. Tibayrenc M, Neubauer K, Barnabé C, Guerrini F, Skarecky D, Ayala F 1993. Genetic characterization of six parasitic protozoa: parity between random primer DNA typing and multilocus enzyme electrophoresis. Proc Natl Acad Sci USA 90: 1335-1339.
101. Tibayrenc M, Ward P, Moya A, Ayala FJ 1986. Natural populations of Trypanosoma cruzi, the agent of Chagas disease, have a complex multiclonal structure. Proc Natl Acad Sci USA 83: 115-119.
102. Vago AR, Andrade LO, Leite AA, d'Avila Reis D, Macedo AM, Adad SJ, Tostes S Jr, Moreira MC, Filho GB, Pena SD 2000. Genetic characterization of Trypanosoma cruzi directly from tissues of patients with chronic Chagas disease: differential distribution of genetic types into diverse organs. Am J Hum Pathol 156: 1805-1809.
103. Vago AR, Macedo AM, Adad SJ, Reis DA, Corrêa-Oliveira R 1996a. PCR detection of Trypanosoma cruzi DNA in esophageal tissues of patients with chronic Chagas disease. Lancet 348: 891-892.
104. Vago AR, Macedo AM, Oliveira RP, Andrade LO, Chiari E, Galvão LMC, Simpson AJG, Tostes S, Pena SDJ 1996b. Kinetoplast DNA signatures of Trypanosoma cruzi strains obtained directly from infected tissues. Am J Pathol 149: 2153-2159.
105. Vianna G 1911. Contribuição para o estudo da anatomia patológica da moléstia de Chagas. Mem Inst Oswaldo Cruz 3: 276-293.
106. Welch DM, Meselson M 2000. Evidence for the evolution of Bdelloid rotifers without sexual reproduction or genetic exchange. Science 288: 1211-1215.
107. Zeledon R, Rabinovich JE 1981. Chagas' disease: an ecological appraisal with special emphasis on its insect vectors. Annu Rev Entomol 26: 101-33.
108. Zhang Q, Tibayrenc M, Ayala FJ 1988. Linkage disequilibrium in natural populations of Trypanosoma cruzi (Flagellate), the agent of Chagas' disease. J Parasitol 35: 81-85.
109. Zillman U, Ebert F 1983. The characterization of Trypanosoma cruzi stocks by starch gel electrophoresis, comparison of results with those of isoeletric focusing. Tropemmed Parasitol 34: 84-88.
110. Zingales B, Souto RP, Mangia RH, Lisboa CV, Campbell DA, Coura JR, Jansen A, Fernandes O 1998. Molecular epidemiology of American trypanosomiasis in Brazil based on dimorphisms of rRNA and mini-exon gene sequences. Int J Parasitol 28: 105-112.
111. Zingales B, Stolf BS, Souto RP, Fernandes O, Briones MR 1999. Epidemiology, biochemistry and evolution of Trypanosoma cruzi lineages based on ribosomal RNA sequences. Mem Inst Oswaldo Cruz 94: 159-164.