Hidden sylvatic foci of the main vector of chagas disease Triatoma infestans: Threats to the vector elimination Campaign?

PLoS Neglected Tropical Diseases

Volumn 5, Issue 10, 2011, Pages

  Ceballos, Leonardo A ^a   Piccinali, Romina V ^a   Marcet, Paula L ^b   Vazquez Prokopec, Gonzalo M ^c,d   Cardinal, M Victoria ^a   Schachter Broide, Judith ^a   Dujardin, Jean Pierre ^e   Dotson, Ellen M ^b   Kitron, Uriel ^c,d   Gürtler, Ricardo E ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^c EMORY UNIVERSITY   (United States)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

^e CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA; PYRETHROID; INSECTICIDE;

ANIMAL EXPERIMENT; ARGENTINA; ARTICLE; CHAGAS DISEASE; CONTROLLED STUDY; FEMALE; GENE FLOW; HABITAT FRAGMENTATION; HABITAT QUALITY; HAPLOTYPE; HEALTH PROGRAM; INFECTION CONTROL; INSECTICIDAL ACTIVITY; MALE; MICROSATELLITE MARKER; MITOCHONDRIAL GENE; MORPHOMETRICS; NONHUMAN; ORGANISM COLONY; PARASITE VECTOR; PESTICIDE SPRAYING; POLYMORPHIC LOCUS; POPULATION ABUNDANCE; RURAL AREA; SPECIES HABITAT; TRIATOMA INFESTANS; VECTOR CONTROL; ANIMAL; CHEMISTRY; CLASSIFICATION; DISEASE CARRIER; DISEASE TRANSMISSION; DNA SEQUENCE; ECOSYSTEM; FAMILY SIZE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; INSECT CONTROL; METHODOLOGY; PHYLOGENY; SOUTH AMERICA; TREE; TRIATOMA;

ANIMALS; CHAGAS DISEASE; DISEASE VECTORS; DNA, MITOCHONDRIAL; ECOSYSTEM; FAMILY CHARACTERISTICS; FEMALE; INSECT CONTROL; INSECTICIDES; PHYLOGENY; PYRETHRINS; SEQUENCE ANALYSIS, DNA; SOUTH AMERICA; TREES; TRIATOMA;

EID: 80055088593     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0001365     Document Type: Article

References (82)

1. World Health Organization (2004) World Health Report 2004: Changing history (World Health Organization, Geneva). Available: www.who.int/whr/2004/en/report04_en.pdf. Accessed 2011 April 11.
2. Diotaiuti L, Faria Filho OF, Carneiro FCF, Dias JCP, Pires HHR, et al. (2000) Aspectos operacionais do controle do Triatoma brasiliensis. Cad Saúde Públ 16: 7-14.
3. Ramsey JM, Cruz-Celis A, Salgado L, Espinosa L, Ordonez R, et al. (2003) Efficacy of pyrethroid insecticides against domestic and peridomestic populations of Triatoma pallidipennis and Triatoma barberi (Reduviidae: Triatominae) vectors of Chagas' disease in Mexico. J Med Entomol 40: 912-920.
4. Dumonteil E, Ruiz-Pina H, Rodriguez-Felix E, Barrera-Perez M, Ramirez-Sierra MJ, et al. (2004) Re-infestation of houses by Triatoma dimidiata after intradomicile insecticide application in the Yucatan Peninsula, Mexico. Mem Inst Oswaldo Cruz 99: 253-266.
5. Matias A, de la Riva J, Martínez E, Torrez M, Dujardin JP, (2003) Domiciliation process of Rhodnius ståli (Hemiptera: Reduviidae) in Alto Beni, La Paz, Bolivia. Trop Med Int Health 8: 264-268.
6. Sánchez-Martin MJ, Feliciangeli MD, Campbell-Lendrum D, Davies CR, (2006) Could the Chagas disease elimination programme in Venezuela be compromised by reinvasion of houses by sylvatic Rhodnius prolixus bug populations? Trop Med Int Health 11: 1585-1593.
7. Silveira AC, (2002) O controle da doença de Chagas nos países do Cone Sul da America. História de uma iniciativa internacional. 1991-2001. In: Silveira AC, Rojas de Arias A, Guillén G, Russomando G, Schenone H, editors. El control de la enfermedad de Chagas en los países del Cono Sur de América pp. 15-43 Historia de una iniciativa internacional. 1991-2001. Facultad de Medicina do Triangulo Mineiro, Uberaba, Brazil.
8. Gürtler RE, Kitron U, Cecere MC, Segura EL, Cohen JE, (2007) Sustainable vector control and management of Chagas disease in the Gran Chaco, Argentina. Proc Natl Acad Sci USA 104: 16194-16199.
9. Gürtler RE, (2009) Sustainability of vector control strategies in the Gran Chaco region: current challenges and possible approaches. Mem Inst Oswaldo Cruz 104 (Suppl 1): 52-59.
10. Gürtler RE, Cecere MC, Canale D, Castañera MB, Chuit R, et al. (1999) Monitoring house reinfestation by vectors of Chagas disease: a comparative trial of detection methods during a four-year follow-up. Acta Trop 72: 213-234.
11. Gürtler RE, Cecere MC, Lauricella MA, Petersen RM, Canale D, et al. (2005) Incidence of Trypanosoma cruzi infection among children following domestic reinfestation after insecticide spraying in rural northwestern Argentina. Am J Trop Med Hyg 73: 95-103.
12. Cecere MC, Vazquez-Prokopec GM, Gürtler RE, Kitron U, (2006) Reinfestation sources for Chagas disease vector, Triatoma infestans, Argentina. Emerg Infect Dis 12: 1096-1102.
13. Gorla DE, Porcasi X, Hrellac H, Catalá SS, (2009) Spatial stratification of house infestation by Triatoma infestans in La Rioja, Argentina. Am J Trop Med Hyg 80: 405-409.
14. Schmunis GA, Zicker F, Moncayo A, (1996) Interruption of Chagas' disease transmission through vector elimination. Lancet 348: 1171.
15. Schofield CJ, Dias JC, (1999) The Southern Cone Initiative against Chagas disease. Adv Parasit 42: 1-27.
16. Abalos JW, Wygodzinsky P, (1951) Las Triatominae Argentinas (Reduviidae, Hemiptera). Tucumán: Universidad Nacional de Tucumán. Publicación 601. Monografía N° 2: 179.
17. Usinger RL, Wygodzinsky P, Ryckman RE, (1966) The biosystematics of Triatominae. Annu Rev Entomol 11: 309-330.
18. Schofield CJ, (1988) Biosystematics of the Triatominae. In: Service MW, editors. Biosystematics of Haematophagous Insects Oxford Clarendon Press pp. 284-312.
19. Lent H, Wygodzinsky P, (1979) Revision of the Triatominae (Hemiptera: Reduviidae) and their significance as vectors of Chagas' disease. Bull Am Mus Nat Hist 163: 185-199.
20. Dujardin JP, Tibayrenc M, Venegas E, Maldonado L, Desjeux P, et al. (1987) Isozyme evidence of lack of speciation between wild and domestic Triatoma infestans (Heteroptera: Reduviidae) in Bolivia. J Med Entomol 24: 40-45.
21. Dujardin JP, Bermudez H, Schofield CJ, (1997) The use of morphometrics in entomological surveillance of silvatic foci of Triatoma infestans in Bolivia. Acta Trop 66: 145-153.
22. Dujardin JP, Schofield CJ, Tibayrenc M, (1998) Population structure of Andean Triatoma infestans: an isozymic study and its epidemiological relevance. Med Vet Entomol 12: 20-29.
23. Noireau F, Cortez MR, Monteiro FA, Jansen AM, Torrico F, (2005) Can wild Triatoma infestans foci in Bolivia jeopardize Chagas disease control efforts? Trends Parasitol 21: 7-10.
24. Ceballos LA, Piccinali RV, Berkunsky I, Kitron U, Gürtler RE, (2009) First finding of melanic sylvatic Triatoma infestans (Hemiptera: Reduviidae) in the Argentine Chaco. J Med Entomol 46: 1195-1202.
25. Noireau F, Flores R, Gutierrez T, Dujardin JP, (1997) Detection of sylvatic dark morphs of Triatoma infestans in the Bolivian Chaco. Mem Inst Oswaldo Cruz 92: 583-584.
26. Rolón M, Vega MC, Román F, Gómez A, Rojas de Arias A, (2011) First report of colonies of sylvatic Triatoma infestans (Hemiptera: Reduviidae) in the Paraguayan Chaco, using a trained dog. PLoS Negl Trop Dis 5: e1026.
27. Bacigalupo BA, Segura MJA, Garcia CA, Hidalgo CJ, Galuppo GS, et al. (2006) Primer hallazgo de vectores de la enfermedad de Chagas asociados a matorrales silvestres en la Región Metropolitana, Chile. Rev Méd Chile 134: 1230-1236.
28. Bacigalupo A, Torres-Pérez F, Segovia V, García A, Correa JP, et al. (2010) Sylvatic foci of the Chagas disease vector Triatoma infestans in Chile: description of a new focus and challenges for control programs. Mem Inst Oswaldo Cruz 105: 633-641.
29. Buitrago R, Waleckx E, Bosseno MF, Zoveda F, Vidaurre P, et al. (2010) First report of widespread wild populations of Triatoma infestans (Reduviidae, Triatominae) in the valleys of La Paz, Bolivia. Am J Trop Med Hyg 82: 574-579.
30. Bargues MD, Klisiowicz DR, Panzera F, Noireau F, Marcilla A, et al. (2006) Origin and phylogeography of the Chagas disease main vector Triatoma infestans based on nuclear rDNA sequences and genome size. Infect Genet Evol 6: 46-62.
31. Pérez de Rosas AR, Segura EL, García BA, (2007) Microsatellite analysis of genetic structure in natural Triatoma infestans (Hemiptera: Reduviidae) populations from Argentina: its implication in assessing the effectiveness of Chagas' disease vector control programmes. Mol Ecol 16: 1401-1412.
32. Piccinali RV, Marcet PL, Noireau F, Kitron U, Gürtler RE, et al. (2009) Molecular population genetics and phylogeography of the Chagas disease vector Triatoma infestans in South America. J Med Entomol 46: 796-809.
33. Piccinali RV, Marcet PL, Ceballos LA, Kitron U, Gürtler RE, et al. (2011) Genetic variability, phylogenetic relationships and gene flow in Triatoma infestans dark morphs from the Argentinean Chaco. Infect Genet Evol 11: 895-903.
34. Panzera F, Dujardin JP, Nicolini P, Caraccio MN, Rose V, et al. (2004) Genomic changes of Chagas disease vector, South America. Emerg Infect Dis 10: 438-446.
35. Picollo MI, Vassena C, Santo Orihuela P, Barrios S, Zaidenberg M, et al. (2005) High resistance to pyrethroid insecticides associated with ineffective field treatments in Triatoma infestans (Hemiptera: Reduviidae) from Northern Argentina. J Med Entomol 42: 637-642.
36. Lardeux F, Depickère S, Duchon S, Chavez T, (2010) Insecticide resistance of Triatoma infestans (Hemiptera, Reduviidae) vector of Chagas disease in Bolivia. Trop Med Int Health 15: 1037-1048.
37. Miles MA, Feliciangeli MD, Rojas de Arias A, (2003) Science, medicine, and the future: American trypanosomiasis (Chagas' disease) and the role of molecular epidemiology in guiding control strategies. BMJ 326: 1444-1448.
38. Fitzpatrick S, Feliciangeli MD, Sanchez-Martin MJ, Monteiro FA, Miles MA, (2008) Molecular genetics reveal that silvatic Rhodnius prolixus do colonise rural houses. PLoS Negl Trop Dis 2: e210.
39. Dujardin JP, Beard CB, Ryckman R, (2007) The relevance of wing geometry in entomological surveillance of Triatominae, vectors of Chagas disease. Infect Genet Evol 7: 161-167.
40. Feliciangeli MD, Sanchez-Martin M, Marrero R, Davies C, Dujardin JP, (2007) Morphometric evidence for a possible role of Rhodnius prolixus from palm trees in house re-infestation in the State of Barinas (Venezuela). Acta Trop 101: 169-177.
41. Kitron U, Clennon JA, Cecere MC, Gürtler RE, King CH, et al. (2006) Upscale or downscale: applications of fine scale remotely sensed data to Chagas disease in Argentina and schistosomiasis in Kenya. Geospatial Health Applic 1: 49-58.
42. Ceballos LA, Cardinal MV, Vazquez-Prokopec GM, Lauricella MA, Orozco MM, et al. (2006) Long-term reduction of Trypanosoma cruzi infection in sylvatic mammals following deforestation and sustained vector surveillance in northwestern Argentina. Acta Trop 98: 286-296.
43. Noireau F, Flores R, Gutierrez T, Abad-Franch F, Flores E, et al. (2000) Natural ecotopes of Triatoma infestans dark morph and other wild triatomines in the Bolivian Chaco. Trans R Soc Trop Med Hyg 94: 23-27.
44. Wisnivesky-Colli C, Schweigmann NJ, Alberti A, Pietrokovsky SM, Conti O, et al. (1992) Sylvatic American trypanosomiasis in Argentina. Trypanosoma cruzi infection in mammals from the Chaco forest in Santiago del Estero. Trans R Soc Trop Med Hyg 86: 38-41.
45. Cecere MC, Castañera MB, Canale DM, Chuit R, Gürtler RE, (1999) Trypanosoma cruzi infection in Triatoma infestans and other triatomines: long-term effects of a control program in a rural area of northwestern Argentina. Rev Panam Salud Publ 5: 392-399.
46. Vazquez-Prokopec GM, Cecere MC, Kitron U, Gürtler RE, (2008) Environmental and demographic factors determining the spatial distribution of Triatoma guasayana in peridomestic and semi-sylvatic habitats of rural northwestern Argentina. Med Vet Entomol 22: 273-282.
47. Noireau F, Flores R, Vargas F, (1999) Trapping sylvatic Triatominae (Reduviidae) in hollow trees. Trans R Soc Trop Med Hyg 93: 13-14.
48. Vazquez-Prokopec GM, Ceballos LA, Marcet PL, Cecere MC, Cardinal MV, et al. (2006) Seasonal variations in active dispersal of natural populations of Triatoma infestans in rural north-western Argentina. Med Vet Entomol 20: 1-6.
49. Schofield CJ, Lehane MJ, McEwen P, Catala SS, Gorla DE, (1992) Dispersive flight by Triatoma infestans under natural climatic conditions in Argentina. Med Vet Entomol 6: 51-56.
50. Gurevitz JM, Kitron U, Gürtler RE, (2007) Flight muscle dimorphism and heterogeneity in flight initiation of field-collected Triatoma infestans (Hemiptera: Reduviidae). J Med Entomol 44: 186-191.
51. Ceballos LA, Vazquez-Prokopec GM, Cecere MC, Marcet PL, Gürtler RE, (2005) Feeding rates, nutritional status and flight dispersal potential of peridomestic populations of Triatoma infestans in rural northwestern Argentina. Acta Trop 95: 149-159.
52. Monteiro FA, Barrett TV, Fitzpatrick S, Cordon-Rosales C, Feliciangeli D, et al. (2003) Molecular phylogeography of the Amazonian Chagas disease vectors Rhodnius prolixus and R. robustus. Mol Ecol 12: 997-1006.
53. García BA, Powell JR, (1998) Phylogeny of species of Triatoma (Hemiptera: Reduviidae) based on mitochondrial DNA sequences. J Med Entomol 35: 232-238.
54. Monteiro FA, Perez R, Panzera F, Dujardin JP, Galvão C, et al. (1999) Mitochondrial DNA variation of Triatoma infestans populations and its implication on the specific status of T. melanosoma. Mem Inst Oswaldo Cruz 94: 229-238.
55. Giordano R, Pizarro Cortez JC, Paulk S, Stevens L, (2005) Genetic diversity of Triatoma infestans (Hemiptera: Reduviidae) in Chuquisaca, Bolivia based on the mitochondrial cytochrome b gene. Mem Inst Oswaldo Cruz 100: 753-760.
56. Cortez MR, Emperaire L, Piccinali RV, Gürtler RE, Torrico F, et al. (2007) Sylvatic Triatoma infestans (Reduviidae, Triatominae) in the Andean valleys of Bolivia. Acta Trop 102: 47-54.
57. Librado P, Rozas J, (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452.
58. Clement M, Posada D, Crandall KA, (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9: 1657-1660.
59. Marcet PL, Lehmann T, Groner G, Gürtler RE, Kitron U, et al. (2006) Identification and characterization of microsatellite markers in the Chagas disease vector Triatoma infestans (Heteroptera: Reduviidae). Infect Genet Evol 6: 32-37.
60. Marcet PL, Mora MS, Cutrera AP, Jones LJ, Gürtler RE, et al. (2008) Genetic structure of Triatoma infestans populations in rural villages of Santiago del Estero, northern Argentina. Infect Genet Evol 8: 835-846.
61. Bowcock AM, Ruiz-Linares A, Tomfohrde J, Minch E, Kidd JR, et al. (1994) High resolution of human evolutionary trees with polymorphic microsatellites. Nature 368: 455-457.
62. Kumar S, Tamura K, Nei M, (2004) MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinformatics 5: 150-163.
63. Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, et al. (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95: 536-539.
64. Paetkau D, Slade R, Burden M, Estoup A, (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol Ecol 13: 55-65.
65. Jones O, Wang J, (2009) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour 10: 551-555.
66. Schachter-Broide J, Dujardin JP, Kitron U, Gürtler RE, (2004) Spatial structuring of Triatoma infestans (Hemiptera, Reduviidae) populations from northwestern Argentina using wing geometric morphometry. J Med Entomol 41: 643-649.
67. Rohlf FJ, (1996) Morphometric spaces, shape components and the effects of linear transformations. In Advances in Morphometrics. Proceedings of the 1993 NATO-ASI on Morphometrics. In: Marcus LF, Corti M, Loy A, Naylor G, Slice D, editors. pp. 117-129 New York: Plenum Publ. NATO ASI, ser. A, Life Sciences.
68. Dujardin JP, Kaba D, Henry AB, (2010) The exchangeability of shape. BMC Research Notes 3: 266.
69. Getis A, Ord JK, (1996) Local spatial statistics: an overview. In: Longley P, Batty M, editors. Spatial Analysis: Modelling in a GIS Environment Cambridge Geoinformation International pp. 261-277.
70. Chen D, Getis A, (1998) Point Pattern Analysis. San Diego State University, San Diego, CA. Available: http://www.nku.edu/~longa/cgi-bin/cgi-tcl-examples/generic/ppa/ppa.cgi. Accessed: 2011, April 11.
71. Abad-Franch F, Ferraz G, Campos C, Palomeque FS, Grijalva MJ, et al. (2010) Modeling disease vector occurrence when detection is imperfect: Infestation of Amazonian palm trees by triatomine bugs at three spatial scales. PLoS Negl Trop Dis 4: e620.
72. Piccinali RV, Canale DM, Sandoval AE, Cardinal MV, Jensen O, et al. (2010) Triatoma infestans bugs in southern Patagonia. Emerg Inf Dis 16: 887-889.
73. Torres-Pérez F, Acuna-Retamar M, Cook JA, Bacigalupo A, García A, et al. (2010) Statistical phylogeography of Chagas disease vector Triatoma infestans: Testing biogeographic hypotheses of dispersal. Infect Genet Evol 11: 167-174.
74. Richer W, Kengne P, Cortez MR, Perrineau MM, Cohuet A, et al. (2007) Active dispersal by wild Triatoma infestans in the Bolivian Andes. Trop Med Int Health 12: 759-764.
75. Lehane MJ, Schofield CJ, (1981) Field experiments of dispersive flight by Triatoma infestans. Trans R Soc Trop Med Hyg 75: 399-400.
76. Schweigmann N, Vallvé S, Muscio O, Guillini M, Alberti A, et al. (1988) Dispersal flight by Triatoma infestans in an arid area of Argentina. Med Vet Entomol 2: 401-404.
77. Ward JP, Baker PS, (1982) The tethered flight performance of a laboratory population of Triatoma infestans Klug (Hemiptera: Reduviidae). Bull Entomol Res 72: 17-28.
78. Noireau F, Gutierrez T, Flores R, Breniere F, Bosseno MF, et al. (1999b) Ecogenetics of Triatoma sordida and Triatoma guasayana (Hemiptera: reduviidae) in the Bolivian chaco. Mem Inst Oswaldo Cruz 94: 451-457.
79. Yeo M, Acosta N, Llewellyn M, Sanchez H, Adamson S, et al. (2005) Origins of Chagas disease: Didelphis species are natural hosts of Trypanosoma cruzi I and armadillos hosts of Trypanosoma cruzi II, including hybrids. Int J Parasitol 35: 225-233.
80. Cardinal MV, Lauricella MA, Ceballos LA, Lanati L, Marcet PL, et al. (2008) Molecular epidemiology of domestic and sylvatic Trypanosoma cruzi infection in rural northwestern Argentina. Int J Parasitol 3: 1533-1543.
81. Romaña CA, (1963) Enfermedad de Chagas. López Libreros Editores, Buenos Aires.
82. Minoli SA, Lazzari CR, (2006) Take-off activity and orientation of triatomines (Heteroptera: Reduviidae) in relation to the presence of artificial lights. Acta Trop 97: 324-330.