Ponce C, 2007. Current situation of Chagas disease in Central America. Mem Inst Oswaldo Cruz 102 (Suppl 1): 41–44.
Hashimoto K, Cordon-Rosales C, Trampe R, Kawabata M, 2006. Impact of single and multiple residual sprayings of pyrethroid insecticides against Triatoma dimidiata (Reduviidae; Triatominae), the principal vector of Chagas disease in Jutiapa, Guatemala. Am J Trop Med Hyg 75: 226–230.
Dumonteil E, Ruiz-Pina H, Rodriguez-Felix E, Barrera-Perez M, Ramirez-Sierra MJ, Rabinovich JE, Menu F, 2004. Re-infestation of houses by Triatoma dimidiata after intra-domicile insecticide application in the Yucatan peninsula, Mexico. Mem Inst Oswaldo Cruz 99: 253–256.
Monroy C, Castro X, Bustamante DM, Pineda SF, Rodas A, Moguel B, Ayala V, Quiñonez J, 2012. An ecosystem approach for the prevention of Chagas disease in rural Guatemala. Charron DF, ed. Ecohealth Research in Practice: Innovative Applications of an Ecosystem Approach to Health. New York: Springer, 153–162.
Monroy C, Bustamante DM, Pineda S, Rodas A, Castro X, Ayala V, Quinones J, Moguel B, 2009. House improvements and community participation in the control of Triatoma dimidiata re-infestation in Jutiapa, Guatemala. Cad Saude Publica 25 (Suppl 1): S168–S178.
Starr MD, Rojas JC, Zeledon R, Hird DW, Carpenter TE, 1991. Chagas' disease: risk factors for house infestation by Triatoma dimidiata, the major vector of Trypanosoma cruzi in Costa Rica. Am J Epidemiol 133: 740–747.
Bustamante DM, Monroy C, Pineda S, Rodas A, Castro X, Ayala V, Quinones J, Moguel B, Trampe R, 2009. Risk factors for intradomiciliary infestation by the Chagas disease vector Triatoma dimidiata in Jutiapa, Guatemala. Cad Saude Publica 25 (Suppl 1): S83–S92.
Lucero DE, Morrissey LA, Rizzo DM, Rodas A, Garnica R, Stevens L, Bustamante DM, Monroy MC, 2013. Ecohealth interventions limit triatomine reinfestation following insecticide spraying in La Brea, Guatemala. Am J Trop Med Hyg 88: 630–637.
World Health Organization, 2002. Control of Chagas disease (Second Report). WHO, ed. WHO Technical Report Series 905. Geneva: World Health Organization, 109.
Pizarro JC, Stevens L, 2008. A new method for forensic DNA analysis of the blood meal in Chagas disease vectors demonstrated using Triatoma infestans from Chuquisaca, Bolivia. PLoS ONE 3: e3585.
Walker JA, Hughes DA, Anders BA, Shewale J, Sinha SK, Batzer MA, 2003. Quantitative intra-short interspersed element PCR for species-specific DNA identification. Anal Biochem 316: 259–269.
Walker JA, Hughes DA, Hedges DJ, Anders BA, Laborde ME, Shewale J, Sinha SK, Batzer MA, 2004. Quantitative PCR for DNA identification based on genome-specific interspersed repetitive elements. Genomics 83: 518–527.
Walker JA, Kilroy GE, Xing J, Shewale J, Sinha SK, Batzer MA, 2003. Human DNA quantitation using Alu element-based polymerase chain reaction. Anal Biochem 315: 122–128.
Dorn P, Perniciaro L, Yabsley M, Roellig D, Balsamo G, Diaz J, Wesson DM, 2007. Autochthonous transmission of Trypanosoma cruzi, Louisiana. Emerg Infect Dis 13: 605–607.
Moser DR, Kirchhoff LV, Donelson JE, 1989. Detection of Trypanosoma cruzi by DNA amplification using the polymerase chain reaction. J Clin Microbiol 27: 1477–1482.
R Development Core Group, 2010. The R Project for Statistical Computing. Available at: http://www.r-project.org/. Accessed January 15, 2011.
Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM, 2009. Mixed Effects Models and Extensions in Ecology with R. New York: Springer.
Monroy C, MejĂa M, Rodas A, Rosales R, Horio M, Tabaru Y, 1998. Comparison of indoor searches with whole house demolition collections of the vectors of Chagas disease and their indoor distribution. Med Entomol Zool 49: 195–200.
Gürtler RE, Chuit R, Cecere MC, Castanera MB, 1995. Detecting domestic vectors of Chagas disease: a comparative trial of six methods in north-west Argentina. Bull World Health Organ 73: 487–494.
Piesman J, Sherlock IA, Mota E, Todd CW, Hoff R, Weller TH, 1985. Association between household triatomine density and incidence of Trypanosoma cruzi infection during a nine-year study in Castro Alves, Bahia, Brazil. Am J Trop Med Hyg 34: 866–869.
Aiga H, Sasagawa E, Hashimoto K, Nakamura J, Zuniga C, Chevez JE, Hernandez HM, Nakagawa J, Tabaru Y, 2012. Chagas disease: assessing the existence of a threshold for bug infestation rate. Am J Trop Med Hyg 86: 972–979.
Dorn PL, Melgar S, Rouzier V, Gutierrez A, Combe C, Rosales R, Rodas A, Kott S, Salvia D, Monroy CM, 2003. The Chagas vector, Triatoma dimidiata (Hemiptera: Reduviidae), is panmictic within and among adjacent villages in Guatemala. J Med Entomol 40: 436–440.
Oliveira Filho A, 1997. Using new tools to control triatomines in different entomological situations in the Americas. Rev Soc Bras Med Trop 30: 41–46.
Tabaru Y, Monroy C, Rodas A, MejĂa M, Rosales R, 1998. Chemical control of Triatoma dimidiata and Rhodnius prolixus (Reduviidae: Triatominae), the principal vectors of Chagas Disease in Guatemala. Med. Entomol. Zoo. 49: 87–92.
Gürtler RE, Canale DM, Spillmann C, Stariolo R, Salomon OD, Blanco S, Segura EL, 2004. Effectiveness of residual spraying of peridomestic ecotopes with deltamethrin and permethrin on Triatoma infestans in rural western Argentina: a district-wide randomized trial. Bull World Health Organ 82: 196–205.
Stevens L, Dorn PL, Schmidt JO, Klotz JH, Lucero D, Klotz SA, 2011. Kissing bugs. The vectors of chagas. Adv Parasitol 75: 169–192.
Sasaki H, Rosales R, Tabaru Y, 2003. Host feeding profiles of Rhodnius prolixus and Triatoma dimidiata in Guatemala (Hemiptera: Reduviidae: Triatominae). Med. Entomol. and Zoo. 54: 283–289.
Gürtler RE, Cohen JE, Cecere MC, Lauricella MA, Chuit R, Segura EL, 1998. Influence of humans and domestic animals on the household prevalence of Trypanosoma cruzi in Triatoma infestans populations in northwest Argentina. Am J Trop Med Hyg 58: 748–758.
Zeledon R, Solano G, Zuniga A, Swartzwelder JC, 1973. Biology and ethology of Triatoma dimidiata (Latreille, 1811). 3. Habitat and blood sources. J Med Entomol 10: 363–370.
Christensen HA, Sousa OE, de Vasquez AM, 1988. Host feeding profiles of Triatoma dimidiata in peridomestic habitats of western Panama. Am J Trop Med Hyg 38: 477–479.
Torres-Montero J, Lopez-Monteon A, Dumonteil E, Ramos-Ligonio A, 2012. House infestation dynamics and feeding sources of Triatoma dimidiata in central Veracruz, Mexico. Am J Trop Med Hyg 86: 677–682.
Gürtler RE, Cecere MC, Castanera MB, Canale D, Lauricella MA, Chuit R, Cohen JE, Segura EL, 1996. Probability of infection with Trypanosoma cruzi of the vector Triatoma infestans fed on infected humans and dogs in northwest Argentina. Am J Trop Med Hyg 55: 24–31.
Breniere SF, Pietrokovsky S, Gastelum EM, Bosseno MF, Soto MM, Ouaissi A, Kasten FL, Wisnivesky-Colli C, 2004. Feeding patterns of Triatoma longipennis Usinger (Hemiptera, Reduviidae) in peridomestic habitats of a rural community in Jalisco State, Mexico. J Med Entomol 41: 1015–1020.
Stevens L, Dorn PL, Hobson J, de la Rua NM, Lucero DE, Klotz JH, Schmidt JO, Klotz SA, 2012. Vector blood meals and Chagas disease transmission potential, United States. Emerg Infect Dis 18: 646–649.
GĂĽrtler RE, Ceballos LA, Ordonez-Krasnowski P, Lanati LA, Stariolo R, Kitron U, 2009. Strong host-feeding preferences of the vector Triatoma infestans modified by vector density: implications for the epidemiology of Chagas disease. PLoS Negl Trop Dis 3: e447.
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.
Gürtler RE, Cecere MC, Lauricella MA, Cardinal MV, Kitron U, Cohen JE, 2007. Domestic dogs and cats as sources of Trypanosoma cruzi infection in rural northwestern Argentina. Parasitology 134: 69–82.
Rabinovich JE, Kitron UD, Obed Y, Yoshioka M, Gottdenker N, Chaves LF, 2011. Ecological patterns of blood-feeding by kissing-bugs (Hemiptera: Reduviidae: Triatominae). Mem Inst Oswaldo Cruz 106: 479–494.
Cohen JE, Gurtler RE, 2001. Modeling household transmission of American trypanosomiasis. Science 293: 694–698.
Gürtler RE, Ceballos LA, Stariolo R, Kitron U, Reithinger R, 2009. Effects of topical application of fipronil spot-on on dogs against the Chagas disease vector Triatoma infestans. Trans R Soc Trop Med Hyg 103: 298–304.
Cecere MC, Canale DM, Gürtler RE, 2003. Effects of refuge availability on the population dynamics of Triatoma infestans in central Argentina. J Appl Ecol 40: 742–756.
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A novel method using vector blood meal sources to assess the impact of control efforts on the risk of transmission of Chagas disease was tested in the village of El Tule, Jutiapa, Guatemala. Control used Ecohealth interventions, where villagers ameliorated the factors identified as most important for transmission. First, after an initial insecticide application, house walls were plastered. Later, bedroom floors were improved and domestic animals were moved outdoors. Only vector blood meal sources revealed the success of the first interventions: human blood meals declined from 38% to 3% after insecticide application and wall plastering. Following all interventions both vector blood meal sources and entomological indices revealed the reduction in transmission risk. These results indicate that vector blood meals may reveal effects of control efforts early on, effects that may not be apparent using traditional entomological indices, and provide further support for the Ecohealth approach to Chagas control in Guatemala.
Financial support: This research was funded by the International Development Research Center (Canada) Grants 101812 and 103696-005, by Network for Research and Training in Tropical Diseases in Central America (Sweden) Grant RO7-008, and the National Institutes of Health (USA) Grant 1R15 A1079672-01A.
Authors' addresses: Mariele J. Pellecer, Dulce M. Bustamante, and M. Carlota Monroy, Laboratorio de EntomologĂa Aplicada y ParasitologĂa, Escuela de BiologĂa, Facultad de Ciencias QuĂmicas y Farmacia, Universidad de San Carlos, Ciudad de Guatemala, Guatemala, E-mails: marielepellecer@gmail.com, dulce_mariab@hotmail.com, and mcarlotamonroy@gmail.com. Patricia L. Dorn, Department of Biological Sciences, Loyola University New Orleans, New Orleans, LA, E-mail: dorn@loyno.edu. Antonieta Rodas, Lcda, Laboratorio de EntomologĂa Aplicada y ParasitologĂa, Escuela de BiologĂa, Facultad de Ciencias QuĂmicas y Farmacia, Universidad de San Carlos, Ciudad de Guatemala, Guatemala, E-mail: antonieta55@yahoo.com.
Ponce C, 2007. Current situation of Chagas disease in Central America. Mem Inst Oswaldo Cruz 102 (Suppl 1): 41–44.
Hashimoto K, Cordon-Rosales C, Trampe R, Kawabata M, 2006. Impact of single and multiple residual sprayings of pyrethroid insecticides against Triatoma dimidiata (Reduviidae; Triatominae), the principal vector of Chagas disease in Jutiapa, Guatemala. Am J Trop Med Hyg 75: 226–230.
Dumonteil E, Ruiz-Pina H, Rodriguez-Felix E, Barrera-Perez M, Ramirez-Sierra MJ, Rabinovich JE, Menu F, 2004. Re-infestation of houses by Triatoma dimidiata after intra-domicile insecticide application in the Yucatan peninsula, Mexico. Mem Inst Oswaldo Cruz 99: 253–256.
Monroy C, Castro X, Bustamante DM, Pineda SF, Rodas A, Moguel B, Ayala V, Quiñonez J, 2012. An ecosystem approach for the prevention of Chagas disease in rural Guatemala. Charron DF, ed. Ecohealth Research in Practice: Innovative Applications of an Ecosystem Approach to Health. New York: Springer, 153–162.
Monroy C, Bustamante DM, Pineda S, Rodas A, Castro X, Ayala V, Quinones J, Moguel B, 2009. House improvements and community participation in the control of Triatoma dimidiata re-infestation in Jutiapa, Guatemala. Cad Saude Publica 25 (Suppl 1): S168–S178.
Starr MD, Rojas JC, Zeledon R, Hird DW, Carpenter TE, 1991. Chagas' disease: risk factors for house infestation by Triatoma dimidiata, the major vector of Trypanosoma cruzi in Costa Rica. Am J Epidemiol 133: 740–747.
Bustamante DM, Monroy C, Pineda S, Rodas A, Castro X, Ayala V, Quinones J, Moguel B, Trampe R, 2009. Risk factors for intradomiciliary infestation by the Chagas disease vector Triatoma dimidiata in Jutiapa, Guatemala. Cad Saude Publica 25 (Suppl 1): S83–S92.
Lucero DE, Morrissey LA, Rizzo DM, Rodas A, Garnica R, Stevens L, Bustamante DM, Monroy MC, 2013. Ecohealth interventions limit triatomine reinfestation following insecticide spraying in La Brea, Guatemala. Am J Trop Med Hyg 88: 630–637.
World Health Organization, 2002. Control of Chagas disease (Second Report). WHO, ed. WHO Technical Report Series 905. Geneva: World Health Organization, 109.
Pizarro JC, Stevens L, 2008. A new method for forensic DNA analysis of the blood meal in Chagas disease vectors demonstrated using Triatoma infestans from Chuquisaca, Bolivia. PLoS ONE 3: e3585.
Walker JA, Hughes DA, Anders BA, Shewale J, Sinha SK, Batzer MA, 2003. Quantitative intra-short interspersed element PCR for species-specific DNA identification. Anal Biochem 316: 259–269.
Walker JA, Hughes DA, Hedges DJ, Anders BA, Laborde ME, Shewale J, Sinha SK, Batzer MA, 2004. Quantitative PCR for DNA identification based on genome-specific interspersed repetitive elements. Genomics 83: 518–527.
Walker JA, Kilroy GE, Xing J, Shewale J, Sinha SK, Batzer MA, 2003. Human DNA quantitation using Alu element-based polymerase chain reaction. Anal Biochem 315: 122–128.
Dorn P, Perniciaro L, Yabsley M, Roellig D, Balsamo G, Diaz J, Wesson DM, 2007. Autochthonous transmission of Trypanosoma cruzi, Louisiana. Emerg Infect Dis 13: 605–607.
Moser DR, Kirchhoff LV, Donelson JE, 1989. Detection of Trypanosoma cruzi by DNA amplification using the polymerase chain reaction. J Clin Microbiol 27: 1477–1482.
R Development Core Group, 2010. The R Project for Statistical Computing. Available at: http://www.r-project.org/. Accessed January 15, 2011.
Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM, 2009. Mixed Effects Models and Extensions in Ecology with R. New York: Springer.
Monroy C, MejĂa M, Rodas A, Rosales R, Horio M, Tabaru Y, 1998. Comparison of indoor searches with whole house demolition collections of the vectors of Chagas disease and their indoor distribution. Med Entomol Zool 49: 195–200.
Gürtler RE, Chuit R, Cecere MC, Castanera MB, 1995. Detecting domestic vectors of Chagas disease: a comparative trial of six methods in north-west Argentina. Bull World Health Organ 73: 487–494.
Piesman J, Sherlock IA, Mota E, Todd CW, Hoff R, Weller TH, 1985. Association between household triatomine density and incidence of Trypanosoma cruzi infection during a nine-year study in Castro Alves, Bahia, Brazil. Am J Trop Med Hyg 34: 866–869.
Aiga H, Sasagawa E, Hashimoto K, Nakamura J, Zuniga C, Chevez JE, Hernandez HM, Nakagawa J, Tabaru Y, 2012. Chagas disease: assessing the existence of a threshold for bug infestation rate. Am J Trop Med Hyg 86: 972–979.
Dorn PL, Melgar S, Rouzier V, Gutierrez A, Combe C, Rosales R, Rodas A, Kott S, Salvia D, Monroy CM, 2003. The Chagas vector, Triatoma dimidiata (Hemiptera: Reduviidae), is panmictic within and among adjacent villages in Guatemala. J Med Entomol 40: 436–440.
Oliveira Filho A, 1997. Using new tools to control triatomines in different entomological situations in the Americas. Rev Soc Bras Med Trop 30: 41–46.
Tabaru Y, Monroy C, Rodas A, MejĂa M, Rosales R, 1998. Chemical control of Triatoma dimidiata and Rhodnius prolixus (Reduviidae: Triatominae), the principal vectors of Chagas Disease in Guatemala. Med. Entomol. Zoo. 49: 87–92.
Gürtler RE, Canale DM, Spillmann C, Stariolo R, Salomon OD, Blanco S, Segura EL, 2004. Effectiveness of residual spraying of peridomestic ecotopes with deltamethrin and permethrin on Triatoma infestans in rural western Argentina: a district-wide randomized trial. Bull World Health Organ 82: 196–205.
Stevens L, Dorn PL, Schmidt JO, Klotz JH, Lucero D, Klotz SA, 2011. Kissing bugs. The vectors of chagas. Adv Parasitol 75: 169–192.
Sasaki H, Rosales R, Tabaru Y, 2003. Host feeding profiles of Rhodnius prolixus and Triatoma dimidiata in Guatemala (Hemiptera: Reduviidae: Triatominae). Med. Entomol. and Zoo. 54: 283–289.
Gürtler RE, Cohen JE, Cecere MC, Lauricella MA, Chuit R, Segura EL, 1998. Influence of humans and domestic animals on the household prevalence of Trypanosoma cruzi in Triatoma infestans populations in northwest Argentina. Am J Trop Med Hyg 58: 748–758.
Zeledon R, Solano G, Zuniga A, Swartzwelder JC, 1973. Biology and ethology of Triatoma dimidiata (Latreille, 1811). 3. Habitat and blood sources. J Med Entomol 10: 363–370.
Christensen HA, Sousa OE, de Vasquez AM, 1988. Host feeding profiles of Triatoma dimidiata in peridomestic habitats of western Panama. Am J Trop Med Hyg 38: 477–479.
Torres-Montero J, Lopez-Monteon A, Dumonteil E, Ramos-Ligonio A, 2012. House infestation dynamics and feeding sources of Triatoma dimidiata in central Veracruz, Mexico. Am J Trop Med Hyg 86: 677–682.
Gürtler RE, Cecere MC, Castanera MB, Canale D, Lauricella MA, Chuit R, Cohen JE, Segura EL, 1996. Probability of infection with Trypanosoma cruzi of the vector Triatoma infestans fed on infected humans and dogs in northwest Argentina. Am J Trop Med Hyg 55: 24–31.
Breniere SF, Pietrokovsky S, Gastelum EM, Bosseno MF, Soto MM, Ouaissi A, Kasten FL, Wisnivesky-Colli C, 2004. Feeding patterns of Triatoma longipennis Usinger (Hemiptera, Reduviidae) in peridomestic habitats of a rural community in Jalisco State, Mexico. J Med Entomol 41: 1015–1020.
Stevens L, Dorn PL, Hobson J, de la Rua NM, Lucero DE, Klotz JH, Schmidt JO, Klotz SA, 2012. Vector blood meals and Chagas disease transmission potential, United States. Emerg Infect Dis 18: 646–649.
GĂĽrtler RE, Ceballos LA, Ordonez-Krasnowski P, Lanati LA, Stariolo R, Kitron U, 2009. Strong host-feeding preferences of the vector Triatoma infestans modified by vector density: implications for the epidemiology of Chagas disease. PLoS Negl Trop Dis 3: e447.
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.
Gürtler RE, Cecere MC, Lauricella MA, Cardinal MV, Kitron U, Cohen JE, 2007. Domestic dogs and cats as sources of Trypanosoma cruzi infection in rural northwestern Argentina. Parasitology 134: 69–82.
Rabinovich JE, Kitron UD, Obed Y, Yoshioka M, Gottdenker N, Chaves LF, 2011. Ecological patterns of blood-feeding by kissing-bugs (Hemiptera: Reduviidae: Triatominae). Mem Inst Oswaldo Cruz 106: 479–494.
Cohen JE, Gurtler RE, 2001. Modeling household transmission of American trypanosomiasis. Science 293: 694–698.
Gürtler RE, Ceballos LA, Stariolo R, Kitron U, Reithinger R, 2009. Effects of topical application of fipronil spot-on on dogs against the Chagas disease vector Triatoma infestans. Trans R Soc Trop Med Hyg 103: 298–304.
Cecere MC, Canale DM, Gürtler RE, 2003. Effects of refuge availability on the population dynamics of Triatoma infestans in central Argentina. J Appl Ecol 40: 742–756.
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