CHICKEN COOPS, Triatoma dimidiata INFESTATION AND ITS INFECTION WITH Trypanosoma cruzi IN A RURAL VILLAGE OF YUCATAN, MEXICO

Gallineros, la infestación por Triatoma dimidiata y su infección con Trypanosoma cruzi en una localidad rural de Yucatán, México

Edgar KOYOC-CARDEÑA Anuar MEDINA-BARREIRO Francisco Javier ESCOBEDO-ORTEGÓN Jorge Carlos RODRÍGUEZ-BUENFIL Mario BARRERA-PÉREZ Enrique REYES-NOVELO Juan CHABLÉ-SANTOS Celia SELEM-SALAS Gonzalo VAZQUEZ-PROKOPEC Pablo MANRIQUE-SAIDE About the authors

Abstracts

This study longitudinally investigated the association between Triatoma dimidiata infestation, triatomine infection with Trypanosoma cruzi and household/backyard environmental characteristics in 101 homesteads in Molas and Yucatan, Mexico, between November 2009 (rainy season) and May 2010 (dry season). Logistic regression models tested the associations between insect infestation/infection and potential household-level risk factors. A total of 200 T. dimidiata were collected from 35.6% of the homesteads, mostly (73%) from the peridomicile. Of all the insects collected, 48% were infected with T. cruzi. Infected insects were collected in 31.6% of the homesteads (54.1% and 45.9% intra- and peridomiciliary, respectively). Approximately 30% of all triatomines collected were found in chicken coops. The presence of a chicken coop in the backyard of a homestead was significantly associated with both the odds of finding T. dimidiata (OR = 4.10, CI 95% = 1.61-10.43, p = 0.003) and the presence of triatomines infected with T. cruzi (OR = 3.37, CI 95% = 1.36-8.33, p = 0.006). The results of this study emphasize the relevance of chicken coops as a putative source of T. dimidiata populations and a potential risk for T. cruzi transmission.

Peridomicile; Triatoma dimidiata; Trypanosoma cruzi; Chagas disease


Investigamos longitudinalmente la asociación entre la infestación por Triatoma dimidiata, su infección con Trypanosoma cruzi y las características ambientales de los domicilios/peridomicilios en 101 viviendas de Molas, Yucatán, México entre Noviembre de 2009 (temporada lluviosa) y Mayo de 2010 (temporada seca). Mediante modelos de regresión logística se probaron asociaciones entre la infestación/infección de T. dimidiatay factores de riesgo potenciales a nivel de las viviendas. Se colectó un total de 200 individuos de T. dimidiata en el 35.6% de las viviendas, mayormente del peridomicilio (73%). De todos los triatominos colectados el 48% se encontraron infectados con T. cruzi. Los triatomas infectados fueron colectados en el 31.6% de las viviendas (54.1% y 45.9% en intra y peridomicilio respectivamente). Aproximadamente el 30% de todos los triatominos colectados, fueron encontrados en gallineros. La presencia de un gallinero en el peridomicilio de una vivienda se asoció significativamante tanto con las posibilidades de encontrar T. dimidiata (OR = 4.10, CI 95% = 1.61-10.43, p = 0.003) como con la presencia de triatominos infectados con T. cruzi (OR = 3.37, CI 95% = 1.36-8.33, p = 0.006). Los resultados de este estudio enfatizan la relevancia de los gallineros como fuente putativa de poblaciones de T. dimidiata y como una fuente potencial de riesgo de transmisión de T. cruzi.


In the Mexican state of Yucatan, Chagas disease is an endemic zoonosis transmitted domestically by Triatoma dimidiata Latreille 1811 (Hemiptera: Reduviidae), the only locally proven vector. T. dimidiata can be collected in domestic, peridomestic and sylvatic habitats of Yucatan. House infestation is described as seasonal, occurring mainly due to the dispersal of adult insects from peridomestic and sylvatic habitats during the late dry season with non-apparent or limited colonization2Dumonteil E, Gourbiere S, Barrera-Pérez M, Rodríguez-Félix E, Ruíz-Piña H, Baños-López O, et al. Geographic distribution of Triatoma dimidiata and transmission dynamics of Trypanosoma cruziin the Yucatan peninsula of Mexico. Am J Trop Med Hyg. 2002;67:176-83.,5Dumonteil E, Nouvellet P, Rosecrans K, Ramírez-Sierra MJ, Gamboa-León MR, Cruz-Chan JV, et al. Eco-Bio-Social determinants for house infestation by non-domiciliated Triatoma dimidiata in the Yucatan peninsula, Mexico. PLOS Negl Trop Dis. 2013;7:e2466..

Few studies in Yucatan have examined the importance of household and backyard characteristics in the prevalence of triatomine infestations and their infection rates with T. cruzi in and around houses. GUZMÁN-MARÍN et al. 8Guzmán-Marín E, Barrera-Perez M, Rodríguez-Felix ME, Escobedo-Ortegon F, Zavala-Velázquez J. Índices entomológicos de Triatoma dimidiata en el estado de Yucatán. Rev Biomed. 1991;2:20-9. reported that household triatomine infestation in rural communities was associated with the type/quality of housing, e.g. construction with natural materials, thatched roofs, unplastered walls or walls with adobe plastering and the lack of cemented floors. However, other studies have reported that the location of a house within a community (especially if located on the periphery) is a significant risk factor for infestation and the invasion of dispersing adult insects2Dumonteil E, Gourbiere S, Barrera-Pérez M, Rodríguez-Félix E, Ruíz-Piña H, Baños-López O, et al. Geographic distribution of Triatoma dimidiata and transmission dynamics of Trypanosoma cruziin the Yucatan peninsula of Mexico. Am J Trop Med Hyg. 2002;67:176-83.,5Dumonteil E, Nouvellet P, Rosecrans K, Ramírez-Sierra MJ, Gamboa-León MR, Cruz-Chan JV, et al. Eco-Bio-Social determinants for house infestation by non-domiciliated Triatoma dimidiata in the Yucatan peninsula, Mexico. PLOS Negl Trop Dis. 2013;7:e2466.,1313 Ramírez-Sierra MJ, Herrera-Aguilar M, Gourbiere S, Dumonteil E. Patterns of house infestation dynamics by non-domiciliated Triatoma dimidiatareveal a spatial gradient of infestation in rural villages and potential insect manipulation by Trypanosoma cruzi. Trop Med Int Health. 2010;15:77-86.. REYES-NOVELO et al.1414 Reyes-Novelo E, Ruiz-Piña HA, Escobedo-Ortegon J, Barrera-Perez M, Manrique-Saide P, Rodríguez-Vivas RI. Triatoma dimidiata (Latreille) abundance and infection with Trypanosoma cruzi in a rural community of Yucatan, Mexico. Neotrop Entomol. 2013;42:317-24. showed that T. dimidiata did colonize animal shelters (e. g. chicken and dove coops, dog houses and opossum nests). More recently, DUMONTEIL et al.5Dumonteil E, Nouvellet P, Rosecrans K, Ramírez-Sierra MJ, Gamboa-León MR, Cruz-Chan JV, et al. Eco-Bio-Social determinants for house infestation by non-domiciliated Triatoma dimidiata in the Yucatan peninsula, Mexico. PLOS Negl Trop Dis. 2013;7:e2466.quantified that the number of dogs in a house and keeping chickens in a corral were strong determinants for house infestation in rural communities. Such findings from Yucatan agree with reports of house infestation and colonization by T. dimidiata in Guatemala1111 Monroy CM, Bustamante DM, Rodas A, Enriquez ME, Rosales R. Habitats, dispersion and invasion of sylvatic Triatoma dimidiata (Hemiptera: Reduviidae: Triatominae) in Peten, Guatemala. J Med Entomol. 2003;40:800-6.. This study confirms the significance of the peridomicile environment, and particularly of chicken coops, as a source of T. dimidiata populations and a potential risk factor for T. cruzi transmission in a rural village in Yucatan, Mexico.

Fieldwork was carried out between November 2009 and May 2010 in a sample of 101 homesteads (each homestead including the house and all peridomestic structures found in the front and backyard) from Molas, a rural village located in the Southeast of Mexico (20º 48'58'' N and 089º 37'54' W). The community has a population of 2,014 inhabitants, living in 553 houses and surrounded by a subtropical deciduous forest within the Cuxtal ecological reserve. Altitude is 10 m. a. s. l. Climate is characterized by an average annual temperature of 25.9 ºC, with an annual rainfall of 800-1000 mm, occurring mainly between June and November. Molas is located within the highest risk area for Chagas disease in the state of Yucatan2Dumonteil E, Gourbiere S, Barrera-Pérez M, Rodríguez-Félix E, Ruíz-Piña H, Baños-López O, et al. Geographic distribution of Triatoma dimidiata and transmission dynamics of Trypanosoma cruziin the Yucatan peninsula of Mexico. Am J Trop Med Hyg. 2002;67:176-83.,3Dumonteil E, Gourbiere S. Predicting Triatoma dimidiataabundance and infection rate: a risk map for natural transmission of Chagas disease in the Yucatan peninsula of Mexico. Am J Trop Med Hyg. 2004;70:514-9..

Homestead infestation with triatomines was evaluated through: i) active collections both intra- and peridomiciliary and; ii) householders' participatory collections within the houses. Two cross-sectional timed manual active searches for triatomines (described by Gürtler et al. 1999) were performed, one during the 2009 rainy season (November) and the other one during the 2010 dry season (May).

Collections were performed inside houses (interdomiciliary) and in front/backyards (peridomiciliary) by teams of two trained research personnel (30 min in each ecotope to complete one man/hour/homestead between 8:00 a.m. and 1:00 p.m. ). Intradomiciliary searches included inside walls, the base of the roof and furniture. Peridomiciliary searches focused on animal housing, rock and woodpiles, tree trunks, and any other potential triatomine refuges. In addition, householders were invited to take part in a six-month participatory vector surveillance strategy4Dumonteil E, Ramírez-Sierra MJ, Ferral J, Euán-Garcia M, Chavez-Nuñez L. Usefulness of community participation for the fine temporal monitoring of house infestation by non-domiciliated triatomines. J Parasitol. 2009;95:469-71. between December and March, 2010.

Trypanosoma cruzi DNA extraction from individual triatomines and PCR amplification of T. cruzi kinetoplast DNA were performed as described by REYES-NOVELO et al.1414 Reyes-Novelo E, Ruiz-Piña HA, Escobedo-Ortegon J, Barrera-Perez M, Manrique-Saide P, Rodríguez-Vivas RI. Triatoma dimidiata (Latreille) abundance and infection with Trypanosoma cruzi in a rural community of Yucatan, Mexico. Neotrop Entomol. 2013;42:317-24. based on the EDWARDS et al.6Edwards K, Johnstone C, Thompson C. A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acid Res. 1991;19:1349. and MOSER et al.1212 Moser D, Kirchoff LV, Donelson JE. Detection of Trypanosoma cruzi by DNA amplification using the polymerase chain reaction. J Clin Microbiol. 1989;27:1477-82. protocols. The primers used were TcZ1: 5'-CGAGCTCTTGCCCACACGGGTGCT-3'- and TcZ2 5'-CCTCCAAGCAGCGGATAGTTCAGG-3'. Amplification was performed in a Techne TC132 (Barloworld Scientific LTD, Staffordshire, UK) thermal cycler. A 188bp fragment identified the presence of T. cruziDNA following the electrophoresis of a percentage of PCR product in a 2% agarose-TBE stained with ethidium bromide (10 µg/mL) and further documentation in an EDAS 290 gel documentation system (Kodak, Rochester, USA). Local strains of T. cruzi were used as positive controls, whereas the whole mixture minus DNA was used as a negative control.

A household survey was performed to investigate a range of household/backyard characteristics previously reported as significant in the infestation of T. dimidiata and other triatomines1Cohen JM, Wilson ML, Cruz-Celis A, Ordoñez R, Ramsey JM. Infestation by Triatoma pallidipennis (Hemiptera: Reduviidae: Triatominae) is associated with housing characteristics in rural Mexico. J Med Entomol. 2006;43:1252-60.,1010 Guzmán-Tapía Y, Ramírez-Sierra M, Dumonteil E. Urban infestation of Triatoma dimidiata in the city of Mérida, Yucatán, México. Vector Borne Zoonotic Dis. 2007;7:597-606.,1515 Starr MD, Rojas JC, Zeledón R, Hird DW, Carpenter TE. Chagas' disease: risk factors for house infestation by Triatoma dimidiata, the major vector of Trypanosoma cruzi in Costa Rica. Am J Epidemiol. 1991;133:740-7. - type/material of the house (roof, walls, floor); use of window screening; presence of rubbish, rock/wood piles, stone walls, abandoned lots on the sides; the presence of domestic animals e. g. dogs, cats, poultry, horses, sheep, cattle, and the presence of animal housing structures (organized by species) e. g. chicken coops, pig corrals, house stables and kennels.

Using a Fisher's exact test, statistical analyses compared the sex and stage of development of T. dimidiata between locations (intra- and peridomicile). Comparisons of infection by sex between seasons were not performed because of the low number of insects collected. Tests were carried out to study the association between triatomine infestation (positive homesteads) and T. cruzi infection with household-level potential risk factors. Variables of interest were analyzed using χ2 to reduce the model, by comparing percentages in contingency tables. Those with p < 0.25 were included in a logistic regression analysis. Adjusted Odds Ratio and Confidence Intervals (α = 0.05) were calculated with SPSS® (v17.0).

A total of 200 T. dimidiata specimens were collected from 35.6% (36/101) homesteads throughout the study period (Table 1). Overall, a greater number of adults were collected than nymphs (p < 0.05), with a higher male:female abundance ratio (p < 0.05) between ecotopes (Table 1). The majority of specimens (73%) - both adults and nymphs - were collected in the peridomicile environment; nevertheless, 22.5% of the adults and 4.5% of the nymphs collected were reported to have been found intradomiciliary.

Table 1
Triatoma dimidiata infestation (by stage of development, sex and location) and infection with Trypanosoma cruzi in homesteads in the rural community of Molas, Yucatan, Mexico

Collection methods were complementary. Active collections yielded more specimens (65%) than participatory collections. 130 T. dimidiata specimens were captured by active collection, mostly peridomiciliary (97.7%), with a sample composed by adults and nymphs in a similar ratio. 70 specimens of T. dimidiata were captured through householders' collections, mostly reported as intradomiciliary (74.3%) and consisting mostly of adult triatomines (77%).

Overall, 48% (96/200) of the T. dimidiata specimens collected tested positive for T. cruzi (Table 1) and were found in 31.6% (32/101) of homesteads. The infected specimens were mostly adults (p < 0.05); but the proportion of nymphs infected was high (37.5%). Slightly more infected T. dimidiata were found intradomiciliary (54.1%) than in the peridomicile environment (45.9%). Infection prevalence detection was higher in participatory collections (59/70) than in active collections (37/130) (p< 0.05).

Three housing/backyard characteristics initially had p < 0.25: the presence of a chicken coop in the backyard, the type of walls in the house and wood storage; but only the presence of a chicken coop was significantly and positively associated with the presence of T. dimidiata (OR = 4.10, p = 0.003; 95% CI = 1.61-10.43) in the final model. The presence of a chicken coop was also positively associated with T. dimidiata infected with T. cruzi (OR = 3.37, p = 0.006; 95% CI = 1.36-8.33).

Fifty-four homesteads were found in the area with at least one chicken coop. The general structure of local chicken coops consists of cages of 1.30 - 1.50m in height, square in shape, and with sides of 2 - 3m in length. Coops are built on a 4-log base, one on each corner, holding a roof made of either zinc or cardboard and surrounded by a chicken wire fence. The ground is commonly covered with compacted dirt and small stones. Approximately 26% (14/54) of the chicken coops had T. dimidiata, and 64.3% (9/14) had triatomines infected with T. cruzi. Of all peridomestic triatomines, 45.9% (67/146) were collected from chicken coops, with nymphs and adults found in a similar ratio (36:31, respectively. 44.8% of all specimens collected from chicken coops were infected (30/67), with a higher percentage of infected nymphs (76.7% compared to 23.3% in adults).

Triatomine specimens collected from chicken coops were obtained exclusively by active collection and were found on the floor and under stones. During the sectional-active collection in the rainy season, 9.3% (5/54) of homesteads with chicken coops were positive for triatomines. During the second active collection in the following dry season, 16.7% (9/54) of homesteads with chicken coops were positive for triatomines (the majority identified positive for the first time and only two were consistent from the collection four months earlier (Table 2).

Table 2
Active collection and Trypanosoma cruzi infection of Triatoma dimidiata from peridomicilary chicken coops in homesteads in the rural community of Molas, Yucatan, Mexico

Chicken coops are known to play an important role in the maintenance of T. dimidiata populations, both as a refuge for invading insects1111 Monroy CM, Bustamante DM, Rodas A, Enriquez ME, Rosales R. Habitats, dispersion and invasion of sylvatic Triatoma dimidiata (Hemiptera: Reduviidae: Triatominae) in Peten, Guatemala. J Med Entomol. 2003;40:800-6.,1616 Zeledón R, Montenegro VM, Zeledón O. Evidence of colonization of man-made ecotopes by Triatoma dimidiata (Latreille, 1811) in Costa Rica. Mem Inst Oswaldo Cruz. 2001;96:659-60.and as a primary source of blood for triatomines9Guzmán-Marín E, Barrera-Perez M, Rodríguez-Félix ME, Zavala-Velázquez J. Hábitos biológicos de Triatoma dimidiata en Yucatán, México. Rev Bioméd. 1992;3:125-31.. All coops that tested positive in Molas had chickens, except for one, where chickens were removed two weeks before the survey. Among the total homesteads sampled in the locality, only two other sites were found to be used by triatomines as refuges: a rabbit hutch and a pile of rocks and wood. Although the rabbit hutch had a large population of triatomines, this type of refuge was not as commonly found in the peridomiciles as chicken coops. Piles of rocks and wood were quite common, but only one was found to be infested with triatomines.

While the debate concerning whether house infestation by triatomines is influenced by the peridomicile and/or the sylvatic habitats continues4Dumonteil E, Ramírez-Sierra MJ, Ferral J, Euán-Garcia M, Chavez-Nuñez L. Usefulness of community participation for the fine temporal monitoring of house infestation by non-domiciliated triatomines. J Parasitol. 2009;95:469-71.,1313 Ramírez-Sierra MJ, Herrera-Aguilar M, Gourbiere S, Dumonteil E. Patterns of house infestation dynamics by non-domiciliated Triatoma dimidiatareveal a spatial gradient of infestation in rural villages and potential insect manipulation by Trypanosoma cruzi. Trop Med Int Health. 2010;15:77-86.,1414 Reyes-Novelo E, Ruiz-Piña HA, Escobedo-Ortegon J, Barrera-Perez M, Manrique-Saide P, Rodríguez-Vivas RI. Triatoma dimidiata (Latreille) abundance and infection with Trypanosoma cruzi in a rural community of Yucatan, Mexico. Neotrop Entomol. 2013;42:317-24., the results of this study expose the significance of chicken coops located in the peridomicile as a potential source of T. dimidiata populations. Preceding studies in Yucatan report that T. dimidiata infestations occur seasonally but transiently, i.e. with a limited capacity for colonizing households in Yucatan2Dumonteil E, Gourbiere S, Barrera-Pérez M, Rodríguez-Félix E, Ruíz-Piña H, Baños-López O, et al. Geographic distribution of Triatoma dimidiata and transmission dynamics of Trypanosoma cruziin the Yucatan peninsula of Mexico. Am J Trop Med Hyg. 2002;67:176-83.,7Gourbiere S, Dumonteil E, Rabinovich JE, Minkoue R, Menu F. Demographic and dispersal constraints for domestic infestation by non-domicilated Chagas disease vectors in the Yucatan Peninsula, Mexico. Am J Trop Med Hyg. 2008;78:133-9.. These findings indicate the existence of peri- and intradomiciliary infestation and the high prevalence of infected triatomines not only during the dry season, but also in the rainy season. Colonization in houses (based on the collection of nymphs) is indeed uncommon during the rainy season, but increases during the dry season.

This study shows that chicken coops are a risk factor for insect infestation and parasite infection. Nonetheless these findings should be re-evaluated in other communities infested by T. dimidiata.

ACKNOWLEDGEMENTS

This study was funded by the project "Estudio multidisciplinario para la identificación de variables asociadas a la transmisión de enfermedades zoonóticas y enfermedades transmitidas por vector en Yucatán" of the Red epidemiológica de Enfermedades Zoonóticas y Transmitidas por Vector (ETV's) de Importancia en Salud Pública (PROMEP 2008-103.5/09/12.58. SISTPROY CIRB-2009-0006).

REFERENCES

  • 1
    Cohen JM, Wilson ML, Cruz-Celis A, Ordoñez R, Ramsey JM. Infestation by Triatoma pallidipennis (Hemiptera: Reduviidae: Triatominae) is associated with housing characteristics in rural Mexico. J Med Entomol. 2006;43:1252-60.
  • 2
    Dumonteil E, Gourbiere S, Barrera-Pérez M, Rodríguez-Félix E, Ruíz-Piña H, Baños-López O, et al. Geographic distribution of Triatoma dimidiata and transmission dynamics of Trypanosoma cruziin the Yucatan peninsula of Mexico. Am J Trop Med Hyg. 2002;67:176-83.
  • 3
    Dumonteil E, Gourbiere S. Predicting Triatoma dimidiataabundance and infection rate: a risk map for natural transmission of Chagas disease in the Yucatan peninsula of Mexico. Am J Trop Med Hyg. 2004;70:514-9.
  • 4
    Dumonteil E, Ramírez-Sierra MJ, Ferral J, Euán-Garcia M, Chavez-Nuñez L. Usefulness of community participation for the fine temporal monitoring of house infestation by non-domiciliated triatomines. J Parasitol. 2009;95:469-71.
  • 5
    Dumonteil E, Nouvellet P, Rosecrans K, Ramírez-Sierra MJ, Gamboa-León MR, Cruz-Chan JV, et al. Eco-Bio-Social determinants for house infestation by non-domiciliated Triatoma dimidiata in the Yucatan peninsula, Mexico. PLOS Negl Trop Dis. 2013;7:e2466.
  • 6
    Edwards K, Johnstone C, Thompson C. A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acid Res. 1991;19:1349.
  • 7
    Gourbiere S, Dumonteil E, Rabinovich JE, Minkoue R, Menu F. Demographic and dispersal constraints for domestic infestation by non-domicilated Chagas disease vectors in the Yucatan Peninsula, Mexico. Am J Trop Med Hyg. 2008;78:133-9.
  • 8
    Guzmán-Marín E, Barrera-Perez M, Rodríguez-Felix ME, Escobedo-Ortegon F, Zavala-Velázquez J. Índices entomológicos de Triatoma dimidiata en el estado de Yucatán. Rev Biomed. 1991;2:20-9.
  • 9
    Guzmán-Marín E, Barrera-Perez M, Rodríguez-Félix ME, Zavala-Velázquez J. Hábitos biológicos de Triatoma dimidiata en Yucatán, México. Rev Bioméd. 1992;3:125-31.
  • 10
    Guzmán-Tapía Y, Ramírez-Sierra M, Dumonteil E. Urban infestation of Triatoma dimidiata in the city of Mérida, Yucatán, México. Vector Borne Zoonotic Dis. 2007;7:597-606.
  • 11
    Monroy CM, Bustamante DM, Rodas A, Enriquez ME, Rosales R. Habitats, dispersion and invasion of sylvatic Triatoma dimidiata (Hemiptera: Reduviidae: Triatominae) in Peten, Guatemala. J Med Entomol. 2003;40:800-6.
  • 12
    Moser D, Kirchoff LV, Donelson JE. Detection of Trypanosoma cruzi by DNA amplification using the polymerase chain reaction. J Clin Microbiol. 1989;27:1477-82.
  • 13
    Ramírez-Sierra MJ, Herrera-Aguilar M, Gourbiere S, Dumonteil E. Patterns of house infestation dynamics by non-domiciliated Triatoma dimidiatareveal a spatial gradient of infestation in rural villages and potential insect manipulation by Trypanosoma cruzi Trop Med Int Health. 2010;15:77-86.
  • 14
    Reyes-Novelo E, Ruiz-Piña HA, Escobedo-Ortegon J, Barrera-Perez M, Manrique-Saide P, Rodríguez-Vivas RI. Triatoma dimidiata (Latreille) abundance and infection with Trypanosoma cruzi in a rural community of Yucatan, Mexico. Neotrop Entomol. 2013;42:317-24.
  • 15
    Starr MD, Rojas JC, Zeledón R, Hird DW, Carpenter TE. Chagas' disease: risk factors for house infestation by Triatoma dimidiata, the major vector of Trypanosoma cruzi in Costa Rica. Am J Epidemiol. 1991;133:740-7.
  • 16
    Zeledón R, Montenegro VM, Zeledón O. Evidence of colonization of man-made ecotopes by Triatoma dimidiata (Latreille, 1811) in Costa Rica. Mem Inst Oswaldo Cruz. 2001;96:659-60.

Publication Dates

  • Publication in this collection
    May-Jun 2015

History

  • Received
    23 Apr 2014
  • Accepted
    16 Sept 2014
Instituto de Medicina Tropical de São Paulo Av. Dr. Enéas de Carvalho Aguiar, 470, 05403-000 - São Paulo - SP - Brazil, Tel. +55 11 3061-7005 - São Paulo - SP - Brazil
E-mail: revimtsp@usp.br