Volume 98, Issue 2
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



Chagas disease affects between six and seven million people. Its etiological agent, , is classified into six discrete typing units (DTUs). The biological study of 11 strains presented here included four parameters: growth kinetics, parasitemia curves, rate of macrophage infection, and serology to evaluate IgM, total IgG, IgG1, IgG2a, and IgG3. Sequencing of small subunit of ribosomal RNA (SSU rRNA)was performed and the strains were classified into three DTUs. When their growth in liver infusion tryptose medium was represented in curves, differences among the strains could be noted. The parasitemia profile varied among the strains from the TcI, TcII, and TcIII groups, and the 11 strains produced distinct parasitemia levels in infected BALB/c. The TcI group presented the highest rate of macrophage infection by amastigotes, followed by TcII and TcIII. Reactivity to immunoglobulins was observed in the TcI, TcII, and TcIII; all the animals infected with the different strains of showed anti- antibodies. The molecular study presented here resulted in the classification of the strains into the TcI (Bolivia, T lenti, Tm, SC90); TcII (Famema, SC96, SI8, Y); and TcIII (QMM3, QMM5, SI5) groups. These biological and molecular results from 11 strains clarified the factors involved in the biology of the parasite and its hosts. The collection of triatomine (vector) species, and the study of geographic distribution, as well as biological and molecular characterization of the parasite, will contribute to the reporting and surveillance measures in Brazilian states.


Article metrics loading...

The graphs shown below represent data from March 2017
Loading full text...

Full text loading...



  1. Organização Pan-Americana da Saúde, 2017. Neglected Infectious Diseases. Available at: http://www.paho.org/hq/index.php?option=com_topics&view=article&id=10&Itemid=40743. Accessed February 21, 2017. [Google Scholar]
  2. Zingales B, 2009. A new consensus for Trypanosoma cruzi intraspecific nomenclature: second revision meeting recommends TcI to TcVI. Mem Inst Oswaldo Cruz 104: 10511054. [Google Scholar]
  3. Lewis MD, Ma J, Yeo M, Carrasco HJ, Llewellyn MS, Miles MA, , 2009. Genotyping of Trypanosoma cruzi: systematic selection of assays allowing rapid and accurate discrimination of all known lineages. Am J Trop Med Hyg 81: 10411049. [Google Scholar]
  4. Obara MT, Rosa JA, Silva NN, Ceretti W, Jr Urbinatti PR, Barata JMS, Jurberg J, Galvão C, , 2007. Estudo morfológico e histológico dos ovos de seis espécies do gênero Triatoma (Hemiptera:Reduviidae). Neotrop Entomol 36: 798806. [Google Scholar]
  5. Araujo CAC, Waniek PJ, Jansen AM, , 2009. An overview of Chagas disease and the role of triatomines on its distribution in Brazil. Vector Borne Zoonotic Dis 9: 227234. [Google Scholar]
  6. World Health Organization, 2017. Chagas Disease (American Trypanosomiasis). Available at: http://www.who.int/mediacentre/factsheets/fs340/en/. Accessed February, 21, 2017. [Google Scholar]
  7. Galvão C, , (Organizador), 2014. Vetores da doença de chagas no Brasil [online]. Zoologia: Guias e Manuais de Identificação Series. Curitiba, Paraná: Sociedade Brasileira de Zoologia, 289. ISBN 978-85-98203-09-6. Available at: http://books.scielo.org. Accessed February 21, 2017. [Google Scholar]
  8. Almeida CE, Vinhaes MC, Almeida JR, Silveira AC, Costa J, , 2000. Monitoring the domiciliary and peridomiciliary invasion process of Triatoma rubrovaria in the state of Rio Grande do Sul, Brazil. Mem Inst Oswaldo Cruz 95: 761768. [Google Scholar]
  9. Carvalho DB, Almeida CE, Rocha CS, Gardim S, Mendonça VJ, Ribeiro AR, Alves ZC, Ruellas KT, Vedoveli A, Rosa JA, , 2014. A novel association between Rhodnius neglectus and the Livistona australis palm tree in an urban center foreshadowing the risk of Chagas disease transmission by vectorial invasions in Monte Alto City, São Paulo, Brazil. Acta Trop 130: 3538. [Google Scholar]
  10. Coura JR, Viñas PA, , 2010. Chagas disease: a new worldwide challenge. Nature 465: S6S7. [Google Scholar]
  11. Dias JCP, , 2000. Epidemiological surveillance of Chagas disease. Cad Saude Publica 16: 4359. [Google Scholar]
  12. Ribeiro AR, Mendonça VJ, Alves RT, Martinez I, Araújo RF, Mello F, Rosa JA, , 2014. Trypanosoma cruzi strains from triatomine collected in Bahia and Rio Grande do Sul, Brazil. Rev Saude Publica 48: 295302. [Google Scholar]
  13. Rosa JA, Barata JMS, Santos JLF, Cilense M, , 2000. Morfologia de ovos de Triatoma circummaculata e Triatoma rubrovaria (Hemiptera, Reduviidae). Rev Saude Publica 34: 538542. [Google Scholar]
  14. Rosa JA, 2012. Description of Rhodnius montenegrensis n. sp. (Hemiptera: Reduviidae: Triatominae) from the state of Rondônia, Brazil. Zootaxa 3478: 6276. [Google Scholar]
  15. Ramírez JD, Duque MC, Montilla M, Cucunubá Z, Guhl F, , 2012. Natural and emergent Trypanosoma cruzi I genotypes revealed by mitochondrial (Cytb) and nuclear (SSU rDNA) genetic markers. Exp Parasitol 132: 487494. [Google Scholar]
  16. Souto RP, Fernandes O, Macedo AM, Campbell DA, Zingales B, , 1996. DNA markers define two major phylogenetic lineages of Trypanosoma cruzi . Mol Biochem Parasitol 83: 141152. [Google Scholar]
  17. Westenberger SJ, Barnabé C, Campbell DA, Sturm NR, , 2005. Two hybridization events define the population structure of Trypanosoma cruzi . Genetics 171: 527543. [Google Scholar]
  18. Zingales B, 2012. The revised Trypanosoma cruzi subspecific nomenclature: rationale, epidemiological, relevance and research applications. Infect Genet Evol 12: 240253. [Google Scholar]
  19. Freitas JM, 2006. Ancestral genomes, sex, and the population structure of Trypanosoma cruzi . PLoS Pathog 2: e24. [Google Scholar]
  20. Herrera C, Bargues MD, Fajardo A, Montilla M, Triana O, Vallejo GA, Guhl F, , 2007. Identifying four Trypanosoma cruzi I isolate haplotypes from different geographic regions in Colombia. Infect Genet Evol 7: 535539. [Google Scholar]
  21. Llewellyn MS, 2009. Genome-Scale multilocus microsatellite typing of Trypanosoma cruzi discrete typing unit I reveals phylogeographic structure and specific genotypes linked to human infection. PLoS Pathog 5: e1000410. [Google Scholar]
  22. Guhl F, Ramírez JD, , 2011. Trypanosoma cruzi I diversity: towards the need of genetic subdivision? Acta Trop 119: 14. [Google Scholar]
  23. Ocaña-Mayorga S, Llewellyn MS, Costales JA, Miles MA, Grijalva MJ, , 2010. Sex, subdivision, and domestic dispersal of Trypanosoma cruzi lineage I in Southern Ecuador. PLoS Negl Trop Dis 4: 18. [Google Scholar]
  24. Ramírez JD, Duque MC, Guhl F, , 2011. Phylogenetic reconstruction based on cytochrome b (Cytb) gene sequences reveals distinct genotypes within Colombian Trypanosoma cruzi I populations. Acta Trop 119: 6165. [Google Scholar]
  25. Llewellyn MS, Rivett-Carnac JB, Fitzpatrick S, Lewis MD, Yeo M, Gaunt MW, Miles MA, , 2011. Extraordinary Trypanosoma cruzi diversity within single mammalian reservoir hosts implies a mechanism of diversifying selection. Int J Parasitol 41: 609614. [Google Scholar]
  26. Zumaya-Estrada FA, 2012. North American import? Charting the origins of an enigmatic Trypanosoma cruzi domestic genotype. Parasit Vectors 5: 19. [Google Scholar]
  27. Fernandes O, 1998. Brazilian isolates of Trypanosoma cruzi from humans and triatomines classified into two lineages using mini-exon and ribosomal RNA sequences. Am J Trop Med Hyg 58: 807811. [Google Scholar]
  28. 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 1: 159164. [Google Scholar]
  29. Lisboa CV, Pinho AP, Monteiro RV, Jansen AM, , 2007. Trypanosoma cruzi (kinetoplastida Trypanosomatidae): biological heterogeneity in the isolates derived from wild hosts. Exp Parasitol 116: 150155. [Google Scholar]
  30. Briones MRS, Souto RP, Stolf BS, Zingales B, , 1999. The evolution of 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 Parasitol 104: 219232. [Google Scholar]
  31. 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: 22502259. [Google Scholar]
  32. Machado CA, Ayala FJ, , 2001. Nucleotide sequences provide evidence of genetic exchange among distantly related lineages of Trypanosoma cruzi . Proc Natl Acad Sci USA 13: 73967401. [Google Scholar]
  33. Monteiro WM, Magalhães LK, Santana Filho FS, Borborema M, Silveira H, Barbosa Md, , 2010. Trypanosoma cruzi TcIII/Z3 genotype as agent of an outbreak of Chagas disease in the Brazilian western Amazonia. Trop Med Int Health 15: 10491051. [Google Scholar]
  34. Jansen AM, Xavier SC, Roque AL, , 2015. The multiple and complex and changeable scenarios of the Trypanosoma cruzi transmission cycle in the sylvatic environment. Acta Trop 151: 115. [Google Scholar]
  35. Miles MA, Cedillos RA, Póvoa MM, de Souza AA, Prata A, Macedo V, , 1981. Do radically dissimilar Trypanosoma cruzi strains (zymodemes) cause Venezuelan and Brazilian forms of Chagas’ disease? Lancet 20: 13381340. [Google Scholar]
  36. Zafra G, Mantilla JC, Valadares HM, Macedo AM, González CI, , 2008. Evidence of Trypanosoma cruzi II infection in Colombian chagasic patients. Parasitol Res 103: 731734. [Google Scholar]
  37. Lima VS, Xavier SCC, Maldonado IFR, Roque ALR, Vicente ACP, Jansen AM, , 2014. Expanding the knowledge of the geographic distribution of Trypanosoma cruzi TcII and TcV/TcVI Genotypes in the Brazilian Amazon. PLoS One 9: e116137. [Google Scholar]
  38. Chagas C, , 1909. Nova tripanozomase humana. Estudos sobre a morfologia e o ciclo evolutivo do Schizotrypanum cruzi n. gen. n. gen. n. sp, agente etiológico de nova entidade mórbida do homem. Mem Inst Oswaldo Cruz 1: 159218. [Google Scholar]
  39. Pena DA, Eger I, Nogueira L, Heck N, Menin Á, Báfica A, Steindel M, , 2012. Selection of TcII Trypanosoma cruzi population following macrophage infection. J Infect Dis 204: 478486. [Google Scholar]
  40. Funayama GK, Prado Júnior JC, , 1974. Estudo dos caracteres de uma amostra boliviana do Trypanosoma cruzi . Rev Soc Bras Med Trop 8: 7581. [Google Scholar]
  41. Martins LPA, Castanho REP, Rosa JA, Silva LC, Godoy CAP, Rosa RM, , 2003. Caracterização biológica, histopatológica e análise de ácido nucléico de uma cepa Trypanosoma cruzi da região de Marília, SP. Rev Soc Bras Med Trop 36: 3539. [Google Scholar]
  42. Steindel M, 2008. Characterization of Trypanosoma cruzi isolated from humans, vectors, and animal reservoirs following an outbreak of acute human Chagas disease in Santa Catarina State, Brazil. Diagn Microbiol Infect Dis 60: 2532. [Google Scholar]
  43. Silva LHP, Nussenzweig V, , 1953. Sobre uma cepa de Trypanosoma cruzi altamente virulenta para o camundongo branco. Folia Clin Biol (Sao Paulo) 20: 191208. [Google Scholar]
  44. Sambrook J, Russell DW, , 2001. Molecular Cloning: A Laboratory Manual, 3rd edition, Vols 1, 2, and 3. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press, 2100. [Google Scholar]
  45. Nicholas KB, Nicholas HBJ, Deerfield DW, , 1997. GeneDOC: Analysis and Visualization of Genetic Variation. EMBNEW News 4: 414. [Google Scholar]
  46. Thompson JD, Gibson TJ, Plewnia KF, , 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 48764882. [Google Scholar]
  47. Swofford DL, PAUP*, 2002. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sunderland, MA: Sinauer Associates. [Google Scholar]
  48. Stamatakis A, , 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 26882690. [Google Scholar]
  49. Ronquist F, Huelsenbeck JP, , 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 15721574. [Google Scholar]
  50. Huson D, Bryant D, , 2006. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23: 254267. [Google Scholar]
  51. Brener Z, Chiari E, , 1963. Variações morfológicas observadas em diferentes amostras de Trypanosoma cruzi . Rev Inst Med Trop Sao Paulo 5: 220224. [Google Scholar]
  52. Muelas-Serrano S, Le-Senne A, Fernandez-Portillo C, Nogal JJ, Ochoa C, Gomez-Barrio A, , 2002. In vitro and vivo anti-Trypanosoma cruzi activity of a novel nitro-derivative. Mem Inst Oswaldo Cruz 97: 553557. [Google Scholar]
  53. Jawetz E, Melnick JL, Adelberg EA, , 1991. Microbiologia médica. In: O crescimento, a sobrevida e a morte de microorganismos, 18th edition, Vol. 1. Rio de Janeiro, Brazil: Guanabara Koogan. [Google Scholar]
  54. Burgos JM, 2010. Molecular Identification of Trypanosoma cruzi discrete typing units in end-stage chronic Chagas heart disease and reactivation after heart transplantation. Clin Infect Dis 51: 485495. [Google Scholar]
  55. Câmara AC, Lages-Silva E, Sampaio GH, D’Ávila DA, Chiari E, da Cunha Galvão LM, , 2013. Homogeneity of Trypanosoma cruzi I, II, and III populations and the overlap of wild and domestic transmission cycles by Triatoma brasiliensis in northeastern Brazil. Parasitol Res 112: 15431550. [Google Scholar]
  56. Marcili A, 2009. Comparative phylogeography of Trypanosoma cruzi TCIIc: new hosts, association with terrestrial ecotopes, and spatial clustering. Infect Genet Evol 9: 12651274. [Google Scholar]
  57. Lima L, Álvarez OEI, Hamilton PB, Neves L, Takata CSA, Campaner M, Attias M, Souza W, Camargo EFP, Teixeira MMG, , 2013. Trypanosoma livingstonei: a new species from African bats supports the bat seeding hypothesis for the Trypanosoma cruzi clade. Parasit Vectors 6: 221. [Google Scholar]
  58. Barreto MP, , 1965. Tripanossomos semelhantes ao Trypanosoma cruzi em animais silvestres e sua identificação com o agente etiológico da doença de Chagas. Rev Inst Med Trop Sao Paulo 7: 305315. [Google Scholar]
  59. Belda Neto FM, , 1973. Estudos Sobre a Existência de Correlação Entre Os Dados Biométricos e o Grau de Patogenicidade de Amostras Humanas do Trypanosoma cruzi Chagas, 1909. Tese Doutorado. Faculdade de Farmácia e Odontologia de Araraquara. São Paulo, Brasil: Universidade Estadual Júlio de Mesquita Filho, Araraquara.
  60. Andrade SG, , 1974. Caracterização de cepas do Trypanosoma cruzi isoladas no Recôncavo Baiano. Rev. Patol. Trop 3: 65121. [Google Scholar]
  61. Albuquerque S, , 2001. Considerações Relativas ao Comportamento Biológico de Amostras de Uma Cepa de Trypanosoma cruzi, Obtidas Por Centrifugação Diferencial. Tese Livre-Docente. Faculdade de Ciências Farmacêuticas de Ribeirão Preto. São Paulo, Brasil: Universidade de São Paulo, Ribeirão Preto.
  62. Yoshida N, , 2006. Molecular basis of mammalian cell invasion by Trypanosoma cruzi . An Acad Bras Cienc 78: 87111. [Google Scholar]
  63. Nogueira N, Cohn Z, , 1976. Trypanosoma cruzi: mechanism of entry and intracellular fate in mammalian cells. J Exp Med 1: 14021420. [Google Scholar]
  64. Meirelles MN, Araújo-Jorge TC, Souza W, , 1982. Interaction of Trypanosoma cruzi with macrophages in vitro: dissociation of the attachment and internalization phases by low temperature and cytochalasin B. Z Parasitenkd 68: 714. [Google Scholar]
  65. Campos Y, Briceño L, Reina K, Figarella K, Pérez JL, Mosca W, , 2009. Serological diagnosis of Chagas disease: evaluation and characterisation of a low cost antigen with high sensitivity and specificity. Mem Inst Oswaldo Cruz 104: 914917. [Google Scholar]
  66. Bouhdidi A, Truyens C, Rivera MT, Bazin H, Carlier Y, , 1994. Trypanosoma cruzi infection in mice induces a polyisotypic hypergammaglobulinaemia and parasite-specific response involving high IgG2a concentrations and highly avid IgG1 antibodies. Parasite Immunol 16: 6976. [Google Scholar]
  67. Takehara HA, Perini A, da Silva MH, Mota I, , 1981. Trypanosoma cruzi: role of different antibody classes in protection against infection in the mouse. Exp Parasitol 52: 137146. [Google Scholar]
  68. Brodskyn CI, Silva AM, Takehara HA, Mota I, , 1989. IgG subclasses responsible for immune clearance in mice infected with Trypanosoma cruzi . Immunol Cell Biol 67: 343348. [Google Scholar]
  69. Jorge TCA, Castro SL, , (orgs) 2000. Doença de chagas: manual para experimentação animal [online]. Antropologia e Saúde Collection. Rio de Janeiro, Brazil: Editora FIOCRUZ, 368. Available at: http://books.scielo.org. Accessed February 21, 2017. [Google Scholar]

Data & Media loading...

  • Received : 11 Mar 2016
  • Accepted : 29 Jan 2017
  • Published online : 08 Jan 2018

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error