Fertility, Gestation Outcome and Parasite Congenital Transmissibility in Mice Infected with TcI, TcII and TcVI Genotypes of Trypanosoma cruzi

PLoS Neglected Tropical Diseases

Volumn 7, Issue 6, 2013, Pages

  Cencig, Sabrina ^a   Coltel, Nicolas ^a   Truyens, Carine ^a   Carlier, Yves ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPHOSPHAMIDE; PARASITE ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST FEEDING; CHAGAS DISEASE; CONGENITAL INFECTION; CONTROLLED STUDY; DNA EXTRACTION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FERTILITY; GENOTYPE; MALE; MOUSE; NONHUMAN; PARASITE TRANSMISSION; PARASITE VIRULENCE; PARASITEMIA; PREGNANCY OUTCOME; PUP (RODENT); REAL TIME POLYMERASE CHAIN REACTION; REINFECTION; REPRODUCTION; TRYPANOSOMA CRUZI; ANIMAL; BAGG ALBINO MOUSE; CLASSIFICATION; DISEASE MODEL; GENETICS; PARASITOLOGY; PREGNANCY; RODENT DISEASES; SURVIVAL; TRANSMISSION; VERTICAL TRANSMISSION;

ANIMALS; CHAGAS DISEASE; DISEASE MODELS, ANIMAL; FEMALE; FERTILITY; GENOTYPE; INFECTIOUS DISEASE TRANSMISSION, VERTICAL; MALE; MICE; MICE, INBRED BALB C; PREGNANCY; RODENT DISEASES; SURVIVAL ANALYSIS; TRYPANOSOMA CRUZI;

EID: 84879540196     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0002271     Document Type: Article

References (76)

1. Rassi A Jr, Rassi A, Marin-Neto JA, (2010) Chagas disease. Lancet 375: 1388-1402.
2. Coura JR, Vinas PA, (2010) Chagas disease: a new worldwide challenge. Nature Jun 24;465 (7301):: S6-S7.
3. Carlier Y., Truyens C. (2010) Maternal-Fetal Transmission of Trypanosoma cruzi. In: Telleria J., Tibayrenc M., editors. American Trypanosomiasis, Chagas Disease: One Hundred Years of Research. Elsevier. pp. 539-581.
4. Pan American Health Organization (2006) Estimación cuantitativa de la enfermedad de Chagas en las Americas (Quantitative Estimation of Chagas disease in the Americas). OPS/HDM/CD/425-06. Washington, DC.
5. Munoz J, Coll O, Juncosa T, Verges M, del Pino M, et al. (2009) Prevalence and vertical transmission of Trypanosoma cruzi infection among pregnant Latin American women attending 2 maternity clinics in Barcelona, Spain. Clin Infect Dis 48: 1736-1740.
6. Jackson Y, Myers C, Diana A, Marti HP, Wolff H, et al. (2009) Congenital transmission of Chagas disease in Latin American immigrants in Switzerland. Emerg Infect Dis 15: 601-603.
7. Lazarte RA, Litman-Mazo F, Crewalk JA, Keim DE, Baram M, et al. (2012) Congenital Transmission of Chagas Disease- Virginia, 2010. Morbidity and mortality weekly report 61: 477-479.
8. Oliveira FC, Chapadeiro E, Alonso MT, Lopes ER, Pereira FE, (1966) [Chagas disease and pregnancy. I. Incidence of trypanosomiasis and spontaneous abortion in pregnant women with chronic Chagas disease]. Rev Inst Med Trop Sao Paulo 8: 184-185.
9. Teruel JR, Nogueira JL, (1970) [Fetal losses in a high prevalence area of chronic Chagas' disease]. Rev Inst Med Trop Sao Paulo 12: 239-244.
10. Hernandez-Matheson IM, Frankowski RF, Held B, (1983) Foeto-maternal morbidity in the presence of antibodies to Trypanosoma cruzi. Trans R Soc Trop Med Hyg 77: 405-411.
11. Schenone H, Contreras MC, Borgono JM, Rojas A, Villarroel F, (1985) [Congenital Chagas' disease in Chile. Longitudinal study of the reproductivity of women with or without Chagas' disease and of some parasitological and clinical parameters of them and their corresponding children]. Bol Chil Parasitol 40: 24-29.
12. Bittencourt AL (1988) American trypanosomiasis (Chagas'diseases). In: McLeod C., editors. Parasitic infections in pregnancy and the newborn. Oxford: Oxford University Press. pp. 62-86.
13. Torrico F, Alonso-Vega C, Suarez E, Rodriguez P, Torrico MC, et al. (2004) Maternal Trypanosoma cruzi infection, pregnancy outcome, morbidity, and mortality of congenitally infected and non-infected newborns in Bolivia. Am J Trop Med Hyg 70: 201-209.
14. Zingales B, Miles MA, Campbell DA, Tibayrenc M, Macedo AM, et al. (2012) The revised Trypanosoma cruzi subspecific nomenclature: rationale, epidemiological relevance and research applications. Infect Genet Evol 12: 240-253.
15. Bittencourt AL, Mota E, Povoa M, (1985) Isoenzyme characterization of Trypanosoma cruzi from congenital cases of Chagas' disease. Ann Trop Med Parasitol 79: 393-396.
16. Virreira M, Alonso-Vega C, Solano M, Jijena J, Brutus L, et al. (2006) Congenital Chagas disease in Bolivia is not associated with DNA polymorphism of Trypanosoma cruzi. Am J Trop Med Hyg 75: 871-879.
17. Burgos JM, Altcheh J, Bisio M, Duffy T, Valadares HM, et al. (2007) Direct molecular profiling of minicircle signatures and lineages of Trypanosoma cruzi bloodstream populations causing congenital Chagas disease. Int J Parasitol 37: 1319-1327.
18. Falla A, Herrera C, Fajardo A, Montilla M, Vallejo GA, et al. (2009) Haplotype identification within Trypanosoma cruzi I in Colombian isolates from several reservoirs, vectors and humans. Acta Trop 110: 15-21.
19. Corrales RM, Mora MC, Negrette OS, Diosque P, Lacunza D, et al. (2009) Congenital Chagas disease involves Trypanosoma cruzi sub-lineage IId in the northwestern province of Salta, Argentina. Infect Genet Evol 9: 278-282.
20. del Puerto F, Sanchez Z, Nara E, Meza G, Paredes B, et al. (2010) Trypanosoma cruzi lineages detected in congenitally infected infants and Triatoma infestans from the same disease-endemic region under entomologic surveillance in Paraguay. Am J Trop Med Hyg 82: 386-390.
21. Ortiz S, Zulantay I, Solari A, Bisio M, Schijman A, et al. (2012) Presence of Trypanosoma cruzi in pregnant women and typing of lineages in congenital cases. Acta Trop 124 (3):: 243-6.
22. Mjihdi A, Lambot MA, Stewart IJ, Detournay O, Noel JC, et al. (2002) Acute Trypanosoma cruzi infection in mouse induces infertility or placental parasite invasion and ischemic necrosis associated with massive fetal loss. Am J Pathol 161: 673-680.
23. Solana ME, Celentano AM, Tekiel V, Jones M, Gonzalez Cappa SM, (2002) Trypanosoma cruzi: effect of parasite subpopulation on murine pregnancy outcome. J Parasitol 88: 102-106.
24. Shaw GL, Quadagno D, (1975) Trypanosoma lewisi and T. cruzi: effect of infection on gestation in the rat. Exp Parasitol 37: 211-217.
25. Davila HO, Revelli SS, Moreno HS, Valenti JL, Musso OC, et al. (1994) Infection with Trypanosoma cruzi during pregnancy in rats and a decrease in chronic myocardial lesions in their infected offspring. Am J Trop Med Hyg 50: 506-511.
26. Werner H, Egger I, (1971) [Congenital chagas-influence of Trypanosoma cruzi infection on embryonic development in pregnant mice]. Z Tropenmed Parasitol 22: 224-234.
27. Cabeza MP, Chambo GJ, Laguens RP, (1980) [Congenital disease secondary to the chronic infection of mice with Trypanosoma cruzi. Experimental model of congenital Chagas disease]. Medicina (B Aires) 40 (Suppl 1):: 40-44.
28. Sala MA, Lopes RA, Carraro Abrahao AA, Meneguette C, (2006) Efecto de la infeccion aguda por diferentes cepas de Trypanosoma cruzi sobre el crecimiento intrauterino de fetos de raton. Parasitol Latinoam 61: 69-73.
29. Carlier Y, Rivera MT, Truyens C, Puissant F, Milaire J, (1987) Interactions between chronic murine Trypanosoma cruzi infection and pregnancy: fetal growth retardation. Am J Trop Med Hyg 37: 534-540.
30. Apt W, Naquira C, Strozzi L, (1968) [Congenital transmission of trypanosomiasis cruzi. 3. In mice with acute and chronic infection]. Bol Chil Parasitol 23: 15-19.
31. de Cunio RW, Olmos JA, de Mercau GTN, Ontivero MI, de Budeguer MV, (1980) Chagas Mazza congenito experimental. Medicina (Buenos Aires) 40: 50-55.
32. Apt W, Naquira C, Tejada A, Strozzi L, (1968) [Congenital transmission of Trypanosoma cruzi. II. In rats with acute and chronic infections]. Bol Chil Parasitol 23: 9-15.
33. Andrade SG, (1982) The influence of the strain of Trypanosoma cruzi in placental infections in mice. Trans R Soc Trop Med Hyg 76: 123-128.
34. Moreno EA, Rivera IM, Moreno SC, Alarcon ME, Lugo-Yarbuh A, (2003) [Vertical transmission of Trypanosoma cruzi in Wistar rats during the acute phase of infection]. Invest Clin 44: 241-254.
35. Alarcon M, Perez MC, Villarreal J, Araujo S, Goncalves L, et al. (2009) [Detection of Trypanosoma cruzi DNA in the placenta and fetuses of mice with Chagasic acute infection]. Invest Clin 50: 335-345.
36. Werner H, Kunert H, (1958) Uber die ursache von congenitalen protozoen-infektionen. Z Tropenmed Parasit 8: 17-27.
37. Delgado MA, Santos-Buch CA, (1978) Transplacental transmission and fetal parasitosis of Trypanosoma cruzi in outbred white Swiss mice. Am J Trop Med Hyg 27: 1108-1115.
38. Hall CA, Pierce EM, Wimsatt AN, Hobby-Dolbeer T, Meers JB, (2010) Virulence and vertical transmission of two genotypically and geographically diverse isolates of Trypanosoma cruzi in mice. J Parasitol 96: 371-376.
39. Alkmim-Oliveira SM, Costa-Martins AG, Borges Kappel H, Correia D, Ramirez LE, et al. (2013) Trypanosoma cruzi experimental congenital transmission associated with TcV and TcI subpatent maternal parasitemia. Parasitol Res 112: 671-678.
40. Vray B, De Baetselier P, Ouaissi A, Carlier Y, (1991) Trypanosoma cruzi but not Trypanosoma brucei fails to induce a chemiluminescent signal in a macrophage hybridoma cell line. Infect Immun 59: 3303-3308.
41. Castanys S, Osuna A, Gamarro F, Ruiz-Perez LM, (1984) Purification of metacyclic forms of Trypanosoma cruzi by Percoll discontinuous gradient centrifugation. Z Parasitenkd 70: 443-449.
42. Carlier Y, Rivera MT, Truyens C, Ontivero M, Flament J, et al. (1992) Chagas' disease: decreased resistance to Trypanosoma cruzi acquired infection in offspring of infected mice. Am J Trop Med Hyg 46: 116-122.
43. Cross JC, Werb Z, Fisher SJ, (1994) Implantation and the placenta: key pieces of the development puzzle. Science 266: 1508-1518.
44. Id Boufker H, Alexandre H, Carlier Y, Truyens C, (2006) Infertility in murine acute Trypanosoma cruzi infection is associated with inhibition of pre-implantation embryo development. Am J Pathol 169: 1730-1738.
45. Bustamante JM, Bixby LM, Tarleton RL, (2008) Drug-induced cure drives conversion to a stable and protective CD8+ T central memory response in chronic Chagas disease. Nat Med 14: 542-550.
46. Cencig S, Coltel N, Truyens C, Carlier Y, (2011) Parasitic loads in tissues of mice infected with Trypanosoma cruzi and treated with AmBisome. PLoS Negl Trop Dis 5: e1216.
47. Carlier Y, Truyens C, (1995) Influence of maternal infection on offspring resistance towards parasites. Parasitol Today 11: 94-99.
48. Cummings KL, Tarleton RL, (2003) Rapid quantitation of Trypanosoma cruzi in host tissue by real-time PCR. Mol Biochem Parasitol 129: 53-59.
49. el 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: 69-76.
50. Solana ME, Alba Soto CD, Fernandez MC, Poncini CV, Postan M, et al. (2009) Reduction of parasite levels in blood improves pregnancy outcome during experimental Trypanosoma cruzi infection. Parasitology 136: 627-639.
51. Bustamante JM, Rivarola HW, Fernandez AR, Enders JE, Fretes R, et al. (2002) Trypanosoma cruzi reinfections in mice determine the severity of cardiac damage. Int J Parasitol 32: 889-896.
52. Torrico F, Alonso-Vega C, Suarez E, Tellez T, Brutus L, et al. (2006) Are maternal re-infections with Trypanosoma cruzi associated with higher morbidity and mortality of congenital Chagas disease? Trop Med Int Health 11: 628-635.
53. Vacchina P, Valdez RA, Gomez Y, Revelli S, Romano MC, (2008) Steroidogenic capacity of Trypanosoma cruzi trypomastigotes. J Steroid Biochem Mol Biol 111: 282-286.
54. Calabrese KS, Lagrange PH, da Costa SC, (1994) Trypanosoma cruzi: histopathology of endocrine system in immunocompromised mice. Int J Exp Pathol 75: 453-462.
55. Lenzi HL, Castelo-Branco MT, Pelajo-Machado M, Oliveira DN, Gattass CR, (1998) Trypanosoma cruzi: compromise of reproductive system in acute murine infection. Acta Trop 71: 117-129.
56. Rivera MT, Marques de AS, Lucas R, Deman J, Truyens C, et al. (1995) High tumor necrosis factor alpha (TNF-alpha) production in Trypanosoma cruzi-infected pregnant mice and increased TNF-alpha gene transcription in their offspring. Infect Immun 63: 591-595.
57. Mjihdi A, Truyens C, Detournay O, Carlier Y, (2004) Systemic and placental productions of tumor necrosis factor contribute to induce fetal mortality in mice acutely infected with Trypanosoma cruzi. Exp Parasitol 107: 58-64.
58. Marinho CR, Nunez-Apaza LN, Martins-Santos R, Bastos KR, Bombeiro AL, et al. (2007) IFN-gamma, but not nitric oxide or specific IgG, is essential for the in vivo control of low-virulence Sylvio X10/4 Trypanosoma cruzi parasites. Scand J Immunol 66: 297-308.
59. Rodrigues AA, Saosa JS, da Silva GK, Martins FA, da Silva AA, et al. (2012) IFN-gamma plays a unique role in protection against low virulent Trypanosoma cruzi strain. PLoS Negl Trop Dis 6: e1598.
60. Storni P, Bolsi FL, (1979) [Pregnancy and Trypanosoma cruzi parasitism]. Medicina (B Aires) 39: 193-197.
61. Menezes CA, Bitterncourt AL, Mota E, Sherlock I, Ferreira J, (1992) [The assessment of parasitemia in women who are carriers of Trypanosoma cruzi infection during and after pregnancy]. Rev Soc Bras Med Trop 25: 109-113.
62. Hermann E, Truyens C, Alonso-Vega C, Rodriguez P, Berthe A, et al. (2004) Congenital transmission of Trypanosoma cruzi is associated with maternal enhanced parasitemia and decreased production of interferon- gamma in response to parasite antigens. J Infect Dis 189: 1274-1281.
63. Brutus L, Ernould JC, Postigo J, Romero M, Schneider D, et al. (2011) Influence of pregnancy on Trypanosoma cruzi parasitemia in chronically infected women in a rural Bolivian community. Am J Trop Med Hyg 84: 808-812.
64. Siriano LR, Luquetti AO, Avelar JB, Marra NL, de Castro AM, (2011) Chagas disease: increased parasitemia during pregnancy detected by hemoculture. Am J Trop Med Hyg 84: 569-574.
65. Somerset DA, Zheng Y, Kilby MD, Sansom DM, Drayson MT, (2004) Normal human pregnancy is associated with an elevation in the immune suppressive CD25+ CD4+ regulatory T-cell subset. Immunology 112: 38-43.
66. Fernandez-Aguilar S, Lambot MA, Torrico F, Alonso-Vega C, Cordoba M, et al. (2005) [Placental lesions in human Trypanosoma cruzi infection]. Rev Soc Bras Med Trop 38 (Suppl 2):: 84-86.
67. Pena DA, Eger I, Nogueira L, Heck N, Menin A, et al. (2011) Selection of TcII Trypanosoma cruzi population following macrophage infection. J Infect Dis 204: 478-486.
68. Diaz-Lujan C, Triquell MF, Schijman A, Paglini P, Fretes RE, (2012) Differential susceptibility of isolated human trophoblasts to infection by Trypanosoma cruzi. Placenta 33: 264-270.
69. Carlier Y, Torrico F, Sosa-Estani S, Russomando G, Luquetti A, et al. (2011) Congenital Chagas disease: recommendations for diagnosis, treatment and control of newborns, siblings and pregnant women. PLoS Negl Trop Dis 5: e1250.
70. Virreira M, Torrico F, Truyens C, Alonso-Vega C, Solano M, et al. (2003) Comparison of polymerase chain reaction methods for reliable and easy detection of congenital Trypanosoma cruzi infection. Am J Trop Med Hyg 68: 574-582.
71. Bern C, Verastegui M, Gilman RH, Lafuente C, Galdos-Cardenas G, et al. (2009) Congenital Trypanosoma cruzi transmission in Santa Cruz, Bolivia. Clin Infect Dis 49: 1667-1674.
72. Virreira M, Truyens C, Alonso-Vega C, Brutus L, Jijena J, et al. (2007) Comparison of Trypanosoma cruzi lineages and levels of parasitic DNA in infected mothers and their newborns. Am J Trop Med Hyg 77: 102-106.
73. Truyens C, Torrico F, Angelo-Barrios A, Lucas R, Heremans H, et al. (1995) The cachexia associated with Trypanosoma cruzi acute infection in mice is attenuated by anti-TNF-alpha, but not by anti-IL-6 or anti-IFN-gamma antibodies. Parasite Immunol 17: 561-568.
74. Disko R, Krampitz HE, (1971) [Occurrence of Trypanosoma cruzi in the milk of infected mice]. Z Tropenmed Parasitol 22: 56-66.
75. Martins LP, Castanho RE, Nogueira AB, Silva OT, Gusmao AS, (2011) Incidence of Trypanosoma cruzi transmission through breastfeeding during acute experimental Chagas disease. Braz J Infect Dis 15: 116-118.
76. Davila HO, Revelli SS, Uasuf C, Didoli G, Moreno H, et al. (1997) Attenuated Trypanosoma cruzi infection in young rats nursed on infected mothers undergoing interferon-gamma treatment during pregnancy. Immunopharmacology 37: 1-6.