1921
Volume 68, Issue 6
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Severe chronic damage to the heart and gastrointestinal tract in patients with Chagas’ disease are often observed 10–20 years after the acute phase. The course of long-lasting infection with the Colombian strain of was studied in seven rhesus monkeys infected for 15–19 years. Subpatent parasitemia was detected in all studied animals, using hemoculture (two of seven), artificial xenodiagnosis (three of seven), and a polymerase chain reaction PCR (six of six). High titers of specific IgG antibody to persisted throughout the chronic phase of infection. Abnormal electrocardiographic (three of six) and echocardiographic (one of six) patterns detected in the -infected monkeys were possibly related to parasite-triggered myocardial damage. The results suggest that rhesus monkeys experimentally infected with , besides reproducing the acute phase of Chagas’ disease, also develop chronic chagasic cardiomyopathy.

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References

  1. WHO, 1997. Interruption of transmission, Brazil. World Health Organ Wkly Epidemiol Rec 72 : 1–5. [Google Scholar]
  2. Clarkson TB, 1988. Nonhuman primate models of atherosclerosis. Lab Anim Sci 48 : 569–572. [Google Scholar]
  3. Weingand KW, 1989. Recent advances in molecular pathology: Atherosclerosis research in cynomolgus monkeys (Macaca fascicularis). Exp Mol Pathol 50 : 1–15. [Google Scholar]
  4. Cefalu WT, Wagner JD, 1997. Aging and atherosclerosis in human and nonhuman primates. Age 20 : 15–28. [Google Scholar]
  5. Kastello MD, Spertzel RO, 1973. The rhesus monkey as a model for the study of infectious disease. Am J Phys Anthropol 38 : 501–504. [Google Scholar]
  6. Barker LF, Maynard JE, Purcell RH, Hoofnagle JH, Berquist KR, London WT, 1975. Viral hepatitis, type B, in experimental animals. Am J Med Sci 270 : 189–195. [Google Scholar]
  7. Roberts ED, Bohm RP Jr, Cogswell FB, Lanners HN, Lowrie RC Jr, Povinelli L, Piesman J Philipp MT, 1995. Chronic Lyme disease in the rhesus monkey. Lab Invest 72 : 146–160. [Google Scholar]
  8. Boche D, Gray F, Khatissian E, Hurtrel M, Montagnier L, Hurtrel B, 1997. Arch Anat Cytol Pathol 45 : 75–85. [Google Scholar]
  9. Durbin AP, Elkins WR, Murphy BR, 2000. African green monkeys provide a useful nonhuman primate model for the study of human parainfluenza virus types-1, -2, and -3 infection. Vaccine 18 : 2462–2469. [Google Scholar]
  10. Nehete PN, Chitta S, Hossain MM, Hill L, Bernacky BJ, Baze W, Arlinghaus RB, Sastry KJ, 2001. Protection against chronic infection and AIDS by an HIV envelope peptide-cocktail vaccine in a pathogenic SHIV-rhesus model. Vaccine 20 : 813–825. [Google Scholar]
  11. Marsden PD, Voller A, Seah SKK, Hawkey C, Green D, 1970. Behavior of a Peru strain of Trypanosoma cruzi in rhesus monkeys. Rev Soc Bras Med Trop 4 : 178–182. [Google Scholar]
  12. Seah SKK, Marsden PD, Voller A, Pettitt LE, 1974. Experimental Trypanosoma cruzi infection in rhesus monkeys: the acute phase. Trans R Soc Trop Med Hyg 68 : 63–69. [Google Scholar]
  13. Bonecini-Almeida MG, Galvão-Castro B, Pessoa MHR, Pirmez C, Laranja FS, 1990. Experimental Chagas’ disease in rhesus monkeys. I Clinical, parasitological, hematological and anatomopathological studies in the acute and indeterminate phase of the disease. Mem Inst Oswaldo Cruz 85 : 163–171. [Google Scholar]
  14. Meirelles MNL, Bonecini-Almeida MG, Pessoa MHR, Galvão-Castro B, 1990. Trypanosoma cruzi: Experimental Chagas’ disease in rhesus monkeys. II Ultrastructural and Cytochemical studies of peroxidase and acid phosphatase activities. Mem Inst Oswaldo Cruz 85 : 173–181. [Google Scholar]
  15. WHO, 1996. Chagas disease: progress towards elimination of transmission, Argentina. World Health Organ Wkly Epidemiol Rec 76 : 12–15. [Google Scholar]
  16. Federici EE, Abelmann WH, Neva FA, 1964. Chronic and progressive myocarditis and myositis in C3H mice infected with Trypanosoma cruzi. Am J Trop Med Hyg 13 : 272–280. [Google Scholar]
  17. Guidelines on the Care of Laboratory Animals and Their Use for Scientific Purposes. II, Pain, Analgesia and Anaesthesia, 1989. London: The Royal Society and Universities Federation for Animal Welfare.
  18. Novy FG, Macneal WJ, 1904. On the cultivation of Trypanosoma brucei. J Infect Dis 1 : 1–30. [Google Scholar]
  19. Nicole CH, 1908. Culture du parasite du bouton d’orient. Comp R Hebdomaire Sci Acad (Paris) 146 : 842–843. [Google Scholar]
  20. Camargo EP, 1964. Growth and differentiation in Trypanosoma cruzi. I. Origin of metacyclic trypanosomes in liquid media. Rev Inst Med Trop Sao Paulo 6 : 93–100. [Google Scholar]
  21. Chiari E, Pinto Dias JC, Lana M, Chiari CA, 1989. Hemocultures for the parasitological diagnosis of human chronic Chagas’ disease. Rev Soc Bras Med Trop 22 : 19–23. [Google Scholar]
  22. Nussenzweig B, Sonntag R, 1952. Xenodiagnóstico artificial. Novo processo. Primeiros resultados positivos. Rev Paul Med 40 : 41–43. [Google Scholar]
  23. Avila HA, Sigman DS, Cohen LM, Millikan RC, Simpson L, 1991. Polymerase chain reaction amplification of Trypanosoma cruzi kinetoplast minicircle DNA isolated from whole blood lysates: diagnosis of chronic Chagas’ disease. Mol Biochem Parasitol 48 : 211–222. [Google Scholar]
  24. Britto C, Cardoso MA, Wincker P, Morel CM, 1993. A simple protocol for the physical cleavage of Trypanosoma cruzi kinetoplast DNA present in blood samples and its use in polymerase chain reaction (PCR)-based diagnosis of chronic Chagas disease. Mem Inst Oswaldo Cruz 88 : 171–172. [Google Scholar]
  25. Saiki RK, Scharf S, Fallona F, Mullis KB, Horn GT, Erlich HA, Arnheim N, 1985. Enzymatic amplification of β-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science 230 : 1350–1354. [Google Scholar]
  26. Falasca A, Grana D, Buccolo J, Gili M, Merlo A, Zoppi J, Mareso E, 1986. Susceptibility of Cebus apella monkey to different strains of Trypanosoma cruzi after single or repeated inoculations. Bull Pan Am Health Organ 20 : 117–137. [Google Scholar]
  27. Sahn DJ, DeMaria A, Kisslo J, Weyman A, 1978. Recommendations regarding quantitation in M-mode echocardiography: results of a survey of echocardiographic measurements. Circulation 58 : 1072–1083. [Google Scholar]
  28. Amico AF, Lichtenberg GS, Reisner AS, Stone CK, Schwartz RG, Meltzer RS, 1989. Superiority of visual versus computerized echocardiographic estimation of radionuclide left ventricular ejection fraction. Am Heart J 118 : 1259–1265. [Google Scholar]
  29. Kasa TJ, Lathrop GD, Dupuy HJ, Bonney CH, Toft JD, 1977. An endemic foucus of Trypanosoma cruzi infection in a subhuman primate research colony. J Am Vet Med Assoc 171 : 850–854. [Google Scholar]
  30. Chiari E, Brener Z, 1966. Contribuição ao diagnóstico parasitológico da doença de Chagas na fase crônica. Rev Inst Med Trop Med Sao Paulo 8 : 134–138. [Google Scholar]
  31. Marsden PD, Mott KE, Prata AR, 1969. Prevalencia de parasitemia de Trypanosoma cruzi em 8 familias de uma zona endemica. Gaz Med Bahia 69 : 65–69. [Google Scholar]
  32. Bronfen E, Alvarenga NJ, 1991. Xenodiagnosis and criteria to assess the level of parasitemia in chronic chagasic patients. Rev Soc Bras Med Trop 24 : 37–42. [Google Scholar]
  33. Marsden PD, Seah SKK, Draper CC, Pettitt LE, Miles MA, Voller A, 1976. Experimental Trypanosoma cruzi infections in rhesus monkeys. II. The early chronic phase. Trans R Soc Trop Med Hyg 70 : 247–251. [Google Scholar]
  34. WHO, 1974. Immunology of Chagas’ disease. Bull World Health Organ 50 : 459–472. [Google Scholar]
  35. Perlowagora-Szumlewicz A, Moreira CJM, 1994. In vivo differentiation of Trypanosoma cruzi. 1. Experimental evidence of the influence of vector species on metacyclogenesis. Mem Inst Oswaldo Cruz 89 : 603–618. [Google Scholar]
  36. Perlowagora-Szumlewicz A, Muller CA, Moreira CJM, 1988. Studies in search of a suitable experimental insect model for xenodiagnosis of hosts with Chagas’ disease. 3, On the interaction of vector species and parasite strain in the reaction of bugs to infection by Trypanosoma cruzi. Rev Saude Publica 22 : 390–400. [Google Scholar]
  37. Miles MA, Patterson JW, Marsden PD, Minter DM, 1975. A comparison of Rhodnius prolixus, Triatoma infestans and Panstrongylus megistus in the xenodiagnosis of a chronic Trypanosoma (Schizotrypanum) cruzi infection in a rhesus monkey (Macaca mullatta). Trans R Soc Trop Med Hyg 69 : 377–382. [Google Scholar]
  38. Avila HA, Borges-Pereira J, Thiemann O, Paiva E, Degrave W, Morel CM, Simpson L, 1993. Detection of Trypanosoma cruzi in blood specimens of chronic chagasic patients by polymerase chain reaction amplification of kinetoplas minicircle DNA: comparison with serology and xenodiagnosis. J Clin Microbiol 31 : 2421–2426. [Google Scholar]
  39. Wincker P, Britto C, Pereira JB, Cardoso MA, Oelemann W, Morel CM, 1994. Use of a simplified polymerase chain reaction procedure to detect Trypanosoma cruzi in blood samples from chronic chagasic patients in a rural endemic area. Am J Trop Med Hyg 51 : 771–777. [Google Scholar]
  40. Lane MA, 2000. Nonhuman primate models in biogerontology. Exp Gerontol 35 : 533–541. [Google Scholar]
  41. Brener Z, Gazzinelli RT, 1997. Immunological control of Trypanosoma cruzi infection and pathogenesis of Chagas’ disease. Int Arch Allergy Immunol 114 : 103–110. [Google Scholar]
  42. Szarfman A, Laranja FS, De Souza W, Galvão-Quintão L, Gerecht D, Shmunis GA, 1978. Tissue reacting antibodies in a rhesus monkey with long-term Trypanosoma cruzi infection. Am J Trop Med Hyg 27 : 832–834. [Google Scholar]
  43. Silveira JF, Umezawa ES, Luquetti AO, 2001. Chagas’ disease: recombinant Trypanosoma cruzi antigens for serological diagnosis. Trends Parasitol 17 : 286–291. [Google Scholar]
  44. Samudio M, Montenegro-James S, Kasamatsu E, Cabral M, Schinini A, Arias AR, James MA, 1999. Local and systemic cytokine expression during experimental chronic Trypanosoma cruzi infection in a Cebus monkey model. Parasite Immunol 21 : 451–460. [Google Scholar]
  45. Pless M, Juranek D, Kozarsky P, Steurer F, Tapia G, Bermudez H, 1992. The epidemiology of Chagas’ disease in a hyperendemic area of Cochabamba, Bolivia: a clinical study including electrocardiography, seroreactivity to Trypanosoma cruzi, xenodiagnosis, and domiciliary triatomine distribution. Am J Trop Med Hyg 47 : 539–546. [Google Scholar]
  46. Andrade ALS, Martelli CMT, Luquetti AO, Oliveira OS, Almeida e Silva S, Zicker F, 1992. Serologic screening for Trypanosoma cruzi among blood donors in Central Brazil. Bull Pan Am Health Organ 26 : 157–163. [Google Scholar]
  47. Carvalho MR, Krieger MA, Almeida E, Oelemann W, Shikanai-Yasuda MA, Ferreira AW, Pereira JB, Sáez-Alquezar A, Dorlhiac-Llacer PE, Chamone DF, 1993. Chagas’ disease diagnosis: evaluation of several tests in blood bank screening. Transfusion 33 : 830–834. [Google Scholar]
  48. Salles NA, Sabino EC, Cliquet MC, Eluf-Neto J, Mayer A, Almeida Neto C, Mendonça MC, Doraliach-Llacer P, Chamone DF, Sáez-Alquezar A, 1996. Risk of exposure to Chagas’ disease among seroreactive Brazilian blood donors. Transfusion 36 : 969–973. [Google Scholar]
  49. Arteaga-Fernandez E, Barreto ACP, Ianni BM, Mady C, Bellotti G, Pileggi F, 1988. Variação temporal dos títulos das reações sorológicas na fase crônica da doença de Chagas e sua possível correlação clínica. Arq Bras Cardiol 51 : 143–146. [Google Scholar]
  50. Tarleton RL, Zhang L, 1999. Chagas disease etiology: autoimmunity or parasite persistence? Parasitol Today 15 : 94–99. [Google Scholar]
  51. Kumar R, Kline IK, Abelman WH, 1969. Experimental Trypanosoma cruzi myocarditis. Relative effects upon the right and left ventricles. Am J Pathol 57 : 31–48. [Google Scholar]
  52. dos Santos PVA, Roffê E, Santiago HC, Torres RA, Marino APMP, Paiva CN, Silva AA, Gazzinelli RT, Lannes-Vieira J, 2001. Prevalence of CD8+alpha beta T cells in Trypanosoma cruzielicited myocarditis is associated with acquisition of CD62LLowLFA-1HighVLA-4High activation phenotype and expression of IFN-γ-inducible adhesion and chemoattractant molecules. Microbes Infection 3 : 971–984. [Google Scholar]
  53. Andrade SG, 1990. Influence of Trypanosoma cruzi strain on the pathogenesis of chronic myocardiopathy in mice. Mem Inst Oswaldo Cruz 85 : 17–27. [Google Scholar]
  54. Dias E, Laranja FS, Nobrega G, 1945. Doença de Chagas. Mem Inst Oswaldo Cruz 43 : 495–581. [Google Scholar]
  55. Rosenbaum MB, Alvarez AJ, 1955. The electrocardiogram in chronic chagasic myocarditis. Am Heart J 50 : 492–527. [Google Scholar]
  56. Sanchez G, Duarte CA, Araujo J, D’Alessandro A, 1971. Infection by Trypanosoma cruzi in man versus Chagas’ disease in Tibu, north of Santander, Colombia. Bol Oficina Sanit Panam 70 : 463–471. [Google Scholar]
  57. Mello de Oliveira JA, Meira Oliveira JS, Koberle F, 1972. Pathologic anatomy of the His-Tawara system and electrocardiographic abnormalities in chronic Chagas’ heart disease. Arq Bras Cardiol 25 : 17–25. [Google Scholar]
  58. Rofeld A, Fernandes MAOC, Camargo NB, Moraes AP, Nero E Jr, Tranchesi J, Decourt LV, 1978. Eletrocardiograma em indivíduos com reação de Guerreiro-Machado positiva. Arq Bras Cardiol 31 : 191–194. [Google Scholar]
  59. Bestetti RB, Dalbo CMR, Freitas OC, Teno LAC, Castilho OT, Oliveira JSM, 1994. Noninvasive predictors of mortality for patients with Chagas’ heart disease: a multivariate stpewise logistic regression study. Cardiology 84 : 261–267. [Google Scholar]
  60. Rocha A, Lima Filho JL, Silva Z, Heredita RAG, Lopes ER, 1994. Histopatologia da porção trabecular do ramo direito do feixe de His em chagásicos crônicos com bloqueio de ramo direito. Arq Bras Cardiol 63 : 97–100. [Google Scholar]
  61. Silva MAD, Costa JM, Barbosa JM, Cabral F, Fragata Filho AA, Correa EB, Borges Filho R, Sousa JEMR, 1994. Fase crônica da doença de Chagas. Aspectos clínicos e evolutivos. Arq Bras Cardiol 63 : 281–285. [Google Scholar]
  62. Andrade ALSS, Zicker F, Rassi A, Rassi AG, Oliveira RM, Silva AS, Andrade SS, Martelli CMT, 1998. Early electrocardiographic abnormalities in Trypanosoma cruzi-seropositive children. Am J Trop Med Hyg 59 : 530–534. [Google Scholar]
  63. Bar ME, Pozzer DL, Alvarez BM, Vallejos JÁ, Storino RA, 1998. Estudio transversal clínico y epidemiológico de la enfermedad de Chagas em uma área rural del nordeste argentino. Rev Soc Bras Med Trop 31 : 199–206. [Google Scholar]
  64. Castro C, Prata A, Macedo V, 2001. Estudo clínico durante 13 anos de 190 chagásicos crônicos de Mambaí, Goiás, Brasil. Rev Soc Bras Med Trop 34 : 309–318. [Google Scholar]
  65. Torres CM, Tavares BM, 1958. Miocardite no macaco Cebus após inoculações repetidas com Schizotrypanum cruzi. Mem Inst Oswaldo Cruz 56 : 85–119. [Google Scholar]
  66. Bolomo N, Milei J, Cossio P, Segura EL, Laguens RP, Fernández L, Arana RM, 1980. Enfermedad de Chagas experimental en un primate sulamericano (Cebus sp.). Medicina (B Aires) 40 : 667–672. [Google Scholar]
  67. Rosner IM, Schinini A, Rovira T, de Arias A, Velásquez G, Monzón MI, Maldonado M, Ferro EA, Gateano R, 1988. Acute Chagas’ disease in non-human primates. 1. Chronology of clinical events, clinical chemistry, ECG, radiology, parasitemia and immunological parameters in Cebus apella monkey. Trop Med Parasitol 39 : 51–55. [Google Scholar]
  68. Almeida EA, Navarro MR, Guariento ME, Carvalhal SS, 1992. Infecção experimental de macacos Cebus apella sp pelo Trypanosoma cruzi. Avaliação clínica, eletrocardiográfica e anatomopatológica. Rev Soc Bras Med Trop 25 : 7–12. [Google Scholar]
  69. Riarte R, Sinagra A, Lauricella M, Bolomo N, Moreno M, Cossio P, Arana R. Segura EL, 1995. Chronic experimental infection by Trypanosoma cruzi in Cebus apella monkeys. Mem Inst Oswaldo Cruz 90 : 733–740. [Google Scholar]
  70. Pung OJ, Hulsebos LH, Kuhn RE, 1988. Experimental Chagas’ disease (Trypanosoma cruzi) in the Brazilian squirrel monkey (Saimiri sciureus): hematology, cardiology, cellular and humoral immune responses. Int J Parasitol 18 : 115–120. [Google Scholar]
  71. Miles MA, Marsden PD, Pettitt LE, Draper CC, Watson S, Seah SKK, Hutt MSR, Fowler JM, 1979. Experimental Trypanosoma cruzi infection in rhesus monkeys. III. Electrocardiographic and histopathological findings. Trans R Soc Trop Med Hyg 73 : 528–532. [Google Scholar]
  72. Teixeira AR, Figueiredo F, Rezende Filho J, Macedo V, 1983. Chagas’ disease: a clinical, parasitological, immunological, and pathological study in rabbits. Am J Trop Med Hyg 32 : 258–272. [Google Scholar]
  73. Postan M, Bailey JJ, Dvorak JÁ, McDaniel JP, Pottala EW, 1987. Studies of Trypanosoma cruzi clones in inbred mice. III. Histopathological and electrocardiographical responses to chronic infection. Am J Trop Med Hyg 37 : 541–549. [Google Scholar]
  74. Barr SC, Holmes RA, Klei TR, 1992. Electrocardiographic and echocardiographic features of trypanosomiasis in dogs inoculated with North American Trypanosoma cruzi isolates. Am J Vet Res 53 : 521–527. [Google Scholar]
  75. Laranja FS, Dias E, Nobrega GC, Miranda A, 1956. Chagas’ disease. A clinical, epidemiologic and pathologic study. Circulation 14 : 1035–1060. [Google Scholar]
  76. Andrade ZA, Andrade SG, Sadigursky M, Maguire JH, 1981. Experimental Chagas’ disease in dogs: a pathological and ECG study of the chronic indeterminate phase of the infection. Arch Pathol Lab Med 105 : 450–464. [Google Scholar]
  77. Laranja FS, Dias E, Nobrega G, 1948. Clínica e terapêutica da doença de Chagas. Mem Inst Oswaldo Cruz 46 : 473–529. [Google Scholar]
  78. Acquatella H, Catalioti F, Gomez-Mancebo JR, Davalos V, Villalobos L, 1987. Long-term control of Chagas’ disease in Venezuela: effects on serologic findings, electrocardiographic abnormalities, and clinical outcome. Circulation 76 : 556–562. [Google Scholar]
  79. Acquatella H, Schiller NB, Puigbo JJ, Giordano H, Suarez JA, Casal H, Arreaza N, Valecillos R, Hirschhaut E, 1980. M-mode and two-dimensional echocardiography in chronic Chagas’ heart disease. Circulation 62 : 787–799. [Google Scholar]
  80. Combellas I, Puigbo JJ, Acquatella H, Tortoledo F, Gomez JR, 1985. Echocardiographic features of impaired left ventricular diastolic function in Chagas’ heart disease. Br Heart J 52 : 298–309. [Google Scholar]
  81. World Health Organization, 1984. Cardiomyopathies. Report of a WHO Expert Committee. World Health Organ Tech Rep Ser 697 : 7–64. [Google Scholar]
  82. Borges-Pereira J, Xavier SS, Pirmez C, Coura JR, 1998. Doença de Chagas em Virgem da Lapa, Minas Gerais, Brasil. IV. Aspectos clínicos e epidemiológicos do aneurisma ventricular esquerdo. Rev Soc Bras Med Trop 31 : 457–463. [Google Scholar]
  83. Rassi A Jr, Rassi A, Little WC, 2000. Chagas’ heart disease. Clin Cardiol 23 : 883–889. [Google Scholar]
  84. Casado J, Davila DF, Donis JH, Torres A, Payares A, Colmenares R, Gottberg CF, 1990. Electrocardiographic abnormalities and left ventricular systolic function in Chagas’ heart disease. Int J Cardiol 27 : 55–62. [Google Scholar]
  85. Araujo J, Sanchez G, Gutierrez J, Perez F, 1970. Cardiomyopathies of obscure origin in Cali, Colombia. Clinical, etiologic, and laboratory aspects. Am Heart J 80 : 162–170. [Google Scholar]
  86. Blandon R, Leandro IM, Johnson CM, 1995. Evaluacion clinica, electrocardiografica y angiografica de los reservorios naturales de la enfermedad de Chagas em la Republica de Panama. Rev Med Panama 20 : 108–115. [Google Scholar]
  87. Gutierrez R, Vera A, Luna DP, Sandoval CM, Ângulo VM, Brito C, Fernandes O, 2001. Epidemiological aspects of Chagas disease in Santander (Colombia). Annals of the XXVIII Annual Meeting on Basic Research in Chagas Disease and XVII Annual Meeting of the Brazilian Society of Protozoology, 2001. Caxambu, Minas Gerais, Brazil, 167.
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  • Received : 07 Aug 2002
  • Accepted : 05 Feb 2003

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