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Am. J. Trop. Med. Hyg., 75(2), 2006, pp. 226-230
Copyright © 2006 by The American Society of Tropical Medicine and Hygiene

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IMPACT OF SINGLE AND MULTIPLE RESIDUAL SPRAYINGS OF PYRETHROID INSECTICIDES AGAINST TRIATOMA DIMIDIATA (REDUVIIADE; TRIATOMINAE), THE PRINCIPAL VECTOR OF CHAGAS DISEASE IN JUTIAPA, GUATEMALA

KEN HASHIMOTO*, CELIA CORDON-ROSALES, RANFERY TRAMPE, AND MASATO KAWABATA
International Center for Medical Research and Treatment, Kobe University School of Medicine, Kobe, Japan; Center for Health Studies, Institute for Research, and Medical Entomology Research and Training Unit-Guatemala/Centers for Disease Control and Prevention, Universidad del Valle de Guatemala; Vector-Borne Diseases, Health Area of Jutiapa, Ministry of Health, Guatemala


ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
This study investigated the impact of single, double, and triple insecticide sprayings on indoor infestation of Triatoma dimidiata in Jutiapa, Guatemala. Up to three successive insecticide sprayings were applied in villages, where the indoor infestation index was > 5% before each spraying round or located adjacent to the persistently infested villages. Among 64 villages with single spraying, the mean indoor infestation index reduced from 20.8% to 1.4% after 12 months, but rose to 8.1% after 33 months. In 40 double-sprayed villages, it decreased from 41.9% to 11.9% by the first spraying and to 4.8% by the second spraying. For 12 villages with triple spraying, it reduced from 40.6% to 13.2%, 10.9%, and 4.1% through each spraying round. Geographic analysis showed that originally highly infested villages were spatially clustered and were likely to remain infested after the sprayings. Indoor infestation of T. dimidiata can be controlled with less than three rounds of spraying.


INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Effective control interventions in South America in the last few decades decreased the number of people infected by Cha-gas disease from 16–18 to 10–12 million.1,2 Since > 80% of the infection occurred through vector transmission, the principal strategy consisted of residual insecticide spraying of houses, combined with community based vector surveillance.3

After the success in South America, the Central American countries formed the Initiative for Chagas Disease Control in 1997, with the goal of eliminating Chagas disease transmission by 2010. In Central America and Mexico, 2.3 million people were thought to be infected, with an estimated annual incidence of > 70,000.4 The vector control methods followed the strategies established in South America, although the vectors are different. The two important vectors in Central America are Triatoma dimidiata, an indigenous species, and Rhodnius prolixus, an imported species.5,6

In Guatemala, the estimated number of infected people was 730,000, with an annual incidence estimated at 30,000—representing ~7.3% and 0.3% of the national population, respectively.4 T. dimidiata is the most widespread domestic vector, reported from 21 of the 22 departments, whereas R. prolixus is reported in 9 departments.57 A national entomological survey conducted in the mid-1990s showed that the vector distribution was concentrated in the center and east of the country, in which the department of Jutiapa showed the highest infestation index of 34.5% for T. dimidiata.7 In 1999, serological investigation of school children in Jutiapa indicated seroprevalence of 4.2%.8

Although R. prolixus seems to be exclusively domestic in Central America, T. dimidiata occupies domestic, peri-domestic, and silvatic habitats. Because of this difference, R. prolixus can probably be eliminated by indoor residual spraying, whereas T. dimidiata may be able to re-colonize treated houses in some areas. Previous studies showed that one cycle of residual insecticide spraying could reduce the indoor infestation rate of T. dimidiata from > 30% to < 10% or 5% and from 5.3% to 0.5%.911 In Mexico, three cycles of spraying decreased the indoor infestation rate from > 90 to 0%.12 While some cases could be treated with single insecticide spaying, others required multiple insecticide spraying. This study investigated the long-term effectiveness of single insecticide spraying and the impact of double and triple insecticide spraying on the infestation and colonization of T. dimidiata with reference to the geographical distribution of the target villages.


MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Study site. The department of Jutiapa consists of 17 municipalities and is in the southeast of the country, bordering the Republic of El Salvador. The population of 389,085 live in 94,807 houses of 696 villages dispersed over a surface area of 3,219 km2.13 The department is located between 89°38' W and 90°42' W and between 13°69' N and 14°60' N.

Baseline survey. From July 2000 to April 2001, teams from Del Valle University and the Vector Control Program of the Health Area of Jutiapa investigated a total of 2,405 houses chosen at random in 178 villages of the department. The villages and houses were randomly selected within each municipality to provide an estimation of domestic infestation by municipality. The house sample size was estimated based on the 1994 National Census and on the parameters of an estimated infestation level of 30%, 5% precision, 95% CI, and 80% statistical power. The survey covered an average of 13.5 (varying from 5 to 53) houses per village or 141.5 (varying from 33 to 174) houses per municipality. Two entomology technicians searched the interior of each house (walls, roofs, floor, beds, and firewood) and peri-domestic areas (chicken coops and corrals located ~2–30 m from the house) during a total of 15–30 minutes, depending on the size of the house.

Vector distribution was expressed using standard indicators: principally, the infestation index ([number of infested houses/number of houses investigated] x 100), and additionally, the density index (number of triatomines captured/number of houses investigated), dispersion index ([number of infested villages/number of villages investigated] x 100), and natural infection index ([number of triatomines infected with Trypanosoma cruzi/number of triatomines examined] x 100).14 This last index was based on microscopic examination of triatomine rectal puncture.

Insecticide spraying. The first round of insecticide spraying (between September 2000 and May 2003) was carried out in 116 villages where the infestation index of T. dimidiata was > 5% at the baseline survey. Of all existing 12,260 houses in the 116 villages, 8,187 houses with mud walls and/or thatched roofs were programmed for spraying, and 8,096 houses were sprayed.

The second round was conducted from April 2002 to October 2003, 17 months (range: 5–20 months) after the first spraying in the villages, where the indoor infestation index remained > 5% after the first spraying or where located adjacent to the persistently infested villages. Eight villages were considered as adjacent, because the distance between the villages were less than ~20 m, for instance, divided only by a path or a road. This spraying round covered 4,259 of 4,319 houses programmed in 52 villages, which consisted of a total of 5,592 houses.

The third round of spraying focused on 12 villages with a total of 1,718 houses, where the indoor infestation index persisted above 5% after the second spraying. All 12 villages were located in the eastern area of the department. This spraying round was applied in 1,513 of 1,556 houses programmed from July 2003 to November 2003 or after 15 months (range: 9–18 months) of the second round.

The spray team of the Vector Control Program of Jutiapa consisted of four sprayers, who covered seven to eight houses per person per day, and one coordinator, who gave notice to the houses to spray on the following day and monitored the quality of spraying. Their senior coordinators of the Vector Control Program of Jutiapa also supervised the operative group for quality control of the spraying techniques on a monthly basis.

Three types of insecticide were used, depending on their availability at the time of spraying. Deltamethrin (5% wettable powder, at 25 mg active ingredient/m2) was sprayed in 41 villages for the first round and 31 villages in the second round of spraying. Lambda-cyhalothrin (10% wettable powder, at 25 mg active ingredient/m2) was used in 15 villages for the first round and 21 villages in the second round of spraying. Beta-cyfluthrin (12.5% suspension concentrate, at 25 mg active ingredient/m2) was applied in 60 villages for the first round and 12 villages for the third round of spraying. The diluted solution of each insecticide was sprayed focusing on cracks and crevices of dried mud walls of the houses and peri-domestic areas, using the pressurized Hudson sprayer. Approximately 8 L of solution was applied in each house.

Evaluation of insecticide spraying. The Vector Control Program evaluated the impact of the first insecticide spraying from April 2002 to August 2003, of the second spraying from March 2003 to August 2004, and of the third spraying from November 2003 to March 2004. The villages intervened with a single spraying were evaluated for the second time between March 2003 and August 2004. Accordingly, the evaluation was conducted twice in the villages with single and double spraying and three times in those with triple spraying.

The bug capturing technique was the same as the baseline survey, searching the interior of each house (walls, roofs, floor, beds, and firewood) and peri-domestic areas (chicken coops and corrals) for a total of 15–30 minutes, depending on the size of the house. However, the sampling number was standardized to 20 houses with mud walls and/or thatched roofs per village or all houses if the village had < 20 houses. This standardization aimed to ensure the coverage of the field evaluation with limited resources of the Vector Control Program and was implemented nationally in 2003 by the National Vector Control Program.15 Further analysis included the colonization index ([number of houses infested by nymphs/number of houses examined] x 100).14

Mapping. To analyze the distribution patterns of infested villages, each village was plotted on a map with the infestation level. A digital map issued by the National Geography Institute of Guatemala was used as a template of the Department of Jutiapa. Coordinates of the villages were codified from the UTM 1/50,000 scale paper map. Using a software ArcView GIS 3.2, the villages were plotted on the template with symbols indicating different degrees of indoor infestation index before and after insecticide sprayings and the number of insecticide applications.


RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Baseline survey. Triatoma dimidiata were found in 524 of 2,405 houses (infestation index = 21.8%) in 128 of 178 villages investigated (dispersion index = 71.9%). Of 2,752 bugs captured (density index = 1.14), 1,806 were dissected and 491 were found infected with T. cruzi (natural infection index = 27.2%). All 128 infested villages were found on the altitude between 400 and 1,600 m above the sea level.

Impact of insecticide spraying. As Figure 1Go shows, the first round of spraying resulted in reduction of the indoor infestation index to < 5% in 64 of the 116 villages, according to the first evaluation after 12 months (range: 3–21 months). The reduction of the mean infestation index of the 64 villages from 20.8% to 1.4% accounts for the control efficiency of 93%. Although a slight increase was observed in the second evaluation after 33 months (range: 20–45 months), the control efficiency remained 61% (20.8–8.1%).


Figure 1
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    FIGURE 1. Changes of indoor infestation index for the single, double, and triple spraying.

 
By application of the second spraying, the mean indoor infestation of the remaining 52 villages decreased from 12.2% to 6.3%, when evaluated after 5 months (range: 3–10 months). Among the 52 villages, 40 villages received double spraying and 12 villages required triple spraying. For the 40 villages, the mean infestation index reduced from 41.9% at the baseline survey to 4.8% at the evaluation of the second spraying (control efficiency = 89%).

The third spraying in the 12 persistently infested villages reduced the mean indoor infestation index from 10.9% to 4.1% in the evaluation after 4 months (range: 3–5 months). The mean indoor infestation index of the 12 villages decreased by 90% between the baseline survey (40.6%) and the evaluation of the third spraying (4.1%). Although the second spraying round hardly decreased the indoor infestation index and showed no effects on the indoor colonization, it halved indoor density index (Table 1Go).


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TABLE 1
Changes of dispersion, infestation, colonization, and density indices on T. dimidiata after single and multiple insecticide sprayings
 
In all evaluations except in the first round of the triple spraying group, the indoor infestation index was significantly related to both indoor colonization and indoor density indices (r > 0.65, P < 0.03). Close association between the indoor infestation and indoor colonization was illustrated especially after all interventions. When 2,184 houses were investigated, a total of 144 houses were found infested, of which 107 houses (74.3%) were with nymphs in the indoor environment and 23 houses (16.0%) were with peri-domestic populations.

The indoor infestation index showed no significant relationship with peri-domestic infestation or peri-domestic colonization indices within and between evaluations. Both peri-domestic infestation and colonization indices remained constant throughout the operations, in which the villages with the double and triple spraying showed slightly larger value than those with the single spraying (Table 1Go). The types of insecticide did not affect the infestation or colonization indices.

Both at the baseline survey and at the evaluation of the first spraying, the indoor infestation index was significantly higher in the multiple spraying villages than the single spraying villages (P < 0.01, by one-way ANOVA). Whereas the indoor infestation indexes showed a moderate relationship (r > 0.40, P < 0.01) between the baseline survey and the evaluation after the first spraying, it did not show any significant relationships after the second or third spraying. Also, the time period between the sprayings and the following evaluations was not related to entomological indexes at all evaluations.

Geographical pattern. Geographical distribution of the infested villages in Figure 2Go shows that originally highly infested villages were located close to one another and were likely to be persistently infested after the sprayings. In Figure 2Go, clusters of such villages are indicated with three circles. The first spraying reduced the indoor infestation of T. dimidiata throughout the department and identified the villages requiring multiple spraying rounds.16 The second and third rounds of spraying further reduced the indoor infestation of the villages of the target areas.


Figure 2
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    FIGURE 2. Distribution of the 116 villages of the department of Jutiapa indicated with the indoor infestation index before and after one, two, or three rounds of insecticide applications.

 
The increase in the mean indoor infestation index of the 64 villages with single spraying after 33 months (range: 20–45 months; Figure 1Go) was more notable in the villages inside the clusters than those outside. When the increased mean infestation index (8.1%) of the 64 villages was analyzed separately, 40 villages inside the clusters showed a mean index of 12.1%, and 24 villages outside the clusters presented a mean index of 1.4%. Similarly, the increased indoor colonization index of 5.9% was composed of 8.8% in the 40 villages inside the clusters and 0.9% in the 24 villages outside the clusters.


DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The results from this study showed that reduction of the indoor infestation index of T. dimidiata to < 5% is achievable in most villages with less than three rounds of residual spraying of pyrethroid insecticides. High initial infestation indicates the necessity of multiple insecticide sprayings. In this study, the single spraying lowered the indoor infestation index from ~40% to < 15% and from ~20% to < 5%. The highly infested villages are often located close to one another and tend to remain infested after a single spraying, forming endemic clusters. Accordingly, the first spraying is useful in identifying the target areas for multiple sprayings.16 Long-term effectiveness of single spraying may be limited in such endemic areas. The operational implication is that, although the first round spraying may dramatically reduce the indoor infestation of T. dimidiata, the villages in endemic areas should be constantly monitored for possible second or third round of insecticide spraying. Furthermore, this study found that the indoor infestation showed notable association with the indoor colonization but not with peri-domestic infestation. This suggests, in accordance with earlier work, that recolonization of houses in Jutiapa is more likely caused by residual T. dimidiata surviving or escaping the insecticide spraying rather than resulting from re-infestation from peri-domestic or silvatic habitats.9

Application of single and multiple residual sprayings may be programmed more efficiently by taking account of the degree of their effectiveness. After the first spraying, a map of the persistently infested villages with their infestation level will indicate the formation of seriously infested areas or endemic clusters. The second spraying round further reduces the indoor infestation of the majority of the persistently infested villages in the target areas to < 5%. Although a few villages remain infested, the third spraying decreases the indoor infestation of almost all villages to < 5%. The results of this study suggest that this formula of single and multiple sprayings is effective for the attack phase of vector control of T. dimidiata.

Long-term effectiveness of the multiple sprayings, however, is yet to be evaluated. Although the varied time periods of up to 25 months between the sprayings and the following evaluations did not affect the infestation or colonization levels, the effect of the single spraying in the endemic areas started to diminish at least after 33 months. However, T. dimidiata was found inside the house as early as 4 months after a spraying in Mexico.17 While colonization and re-infestation mechanisms of T. dimidiata may vary between regions, the villages in the endemic areas should be monitored by the local health service at least once a year after the insecticide sprayings.

High possibilities of colonization of T. dimidiata after sprayings indicate that colonies of the vector are likely to exist in the indoor environments. Temporary shelters of the vector may exist in stacks of dried mud bricks and firewood, inside the mud walls, chicken nests, animal beds, and other objects (e.g., cloths) in the houses and chicken coops attached to outside of the house walls.9 These places may escape from complete spraying. Furthermore, contribution of peri-domestic and silvatic populations needs to be determined. The negative results found in this study might reflect low frequency of peri-domestic structures or even greater lack of sensitivity of the bug search method to detect the peri-domestic infestation. Systematic investigations on characteristics of the indoor and peri-domestic environments of the persistently infested houses may identify the patterns of possible colonization and re-infestation of T. dimidiata.

While insecticide spraying can be intensified against the possible shelters, the residents of the houses can reduce or avoid them by tidying and ordering their housing conditions. When the impact of first insecticide spraying indicates the endemic areas on a map, the local health service should prepare for up to three rounds of spraying for the villages in the target areas. At the same time, interventions at community level should be introduced to minimize unnecessary shelters of the vector in their houses, particularly in endemic areas.


Received November 8, 2005. Accepted for publication March 30, 2006.

Acknowledgments: The authors thank the Vector Control Program of Health Area of Jutiapa for their valuable assistance and Drs. Yoichi Yamagata, Yuichiro Tabaru, Jun Nakagawa, and Chris Schofield for the technical advice and revision of the paper.

Financial support: This study was supported by the Chagas Disease Vector Control Project of the Ministry of Health of Guatemala and the Japan International Cooperation Agency from 2000 to 2005. Additional financial support for the baseline survey was provided by the Special Program on Tropical Disease Research/World Health Organization and the Medical Entomology Research and Training Unit/Guatemala, a field station of the US Centers for Disease Control and Prevention.

* Address correspondence to Ken Hashimoto, International Center for Medical Research and Treatment, Kobe University School of Medicine, 7-5-1, Kusunoki-cho, Chuo-ku, Kobe 650-0017, Japan. E-mail: hashimok{at}gmail.com Back

Authors’ addresses: Ken Hashimoto and Masato Kawabata, International Center for Medical Research and Treatment, Kobe University School of Medicine, 7-5-1, Kusunoki-cho, Chuo-ku, Kobe 650-0017, Japan, Telephone: 81-78-382-5681, Fax: 81-78-382-5715, E-mails: hashimok{at}gmail.com and mkawabat{at}med.kobe-u.ac.jp. Celia Cordon-Rosales, Center for Health Studies, Universidad del Valle de Guatemala/Medical Entomology Research and Training Unit/Guatemala, Division of Parasitic Diseases, Centers for Disease Control and Prevention, Apartado Postal 082, Guatemala City, Guatemala, Telephone: 502-2369-0791, Fax: 502-2364-0354, E-mail: ccz{at}cdc.gov. Ranfery Trampe, Dirección de Área de Salud, Jutiapa, Guatemala, Telephone/Fax: 502-7844-1315.

Reprint requests: Ken Hashimoto and Masato Kawabata, International Center for Medical Research and Treatment, Kobe University School of Medicine, 7-5-1, Kusunoki-cho, Chuo-ku, Kobe 650-0017, Japan.


REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. World Health Organization, 1991. Control of Chagas disease. World Health Organ Tech Rep Ser 811: 95.
  2. Schmunis GA, 2004. Medical significance of American trypanosomiasis. Maudlin I, Holmes PH, Miles MA, eds. The Trypanosomiases. Wallingford: CABI Publishing, 355–368.
  3. Dias JCP, Schofield CJ, 1999. The evolution of Chagas disease (American trypanosomiasis) control after 90 years since Carlos Chagas discovery. Mem Inst Oswaldo Cruz 97: 603–612.
  4. World Health Organization, 2000. Global Collaboration for Development of Pesticides for Public Health (GCDPP)–Challenge of Chagas Disease Vector Control in Central America. Geneva: World Health Organization.
  5. Organización Panamericana de la Salud, 2002. Comisión Intergubernamental de la Iniciativa de los Países de Centroamérica para la Interrupción de la Transmisión Vectorial y Transfusional de la Enfermedad de Chagas. Taller para el Estable-cimiento de Pautas Técnicas en el Control de Triatoma dimidiata. San Salvador: Organización Panamericana de la Salud.
  6. Organización Panamericana de la Salud, 2003. Comisión Intergubernamental de la Iniciativa de los Países de Centroamérica para la Interrupción de la Transmisión Vectorial y Transfusional de la Enfermedad de Chagas. Reunión Internacional para el Establecimiento de Certificación de la Eliminación de Rhodnius prolixus. Ciudad de Guatemala: Organización Panamericana de la Salud.
  7. Tabaru Y, Monroy C, Rodas A, Mejia M, Rosales R, 1999. The geographical distribution of vectors of Chagas disease and populations at risk of infection in Guatemala. Med Entomol Zool 50: 9–17.
  8. Rizzo NR, Arana B, Diaz A, Cordón-Rosales C, Klein RE, Powell M, 2003. Seroprevalence of Trypanosoma cruzi infection among school-age children in the endemic area of Guatemala. Am J Trop Med Hyg 68: 678–682.[Abstract/Free Full Text]
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  12. Rojas Wastavino G, Cabrera-Bravo M, García de la TG, Vences-Blanco M, Ruiz Hernández A, Bucio Torres M, Guevara Gómez Y, Escobar Mesa A, Salazar Schettino PM, 2004. Insecticde and community interventions to control Triatoma dimidiata in localities of the State of Veracruz, Mexico. Mem Inst Oswaldo Cruz 99: 433–437.
  13. Guatemala Instituto Nacional de Estadística, 2002. Censos Nacoinales XI de Población y VI Habitación. Ciudad de Guatemala: Ediciones Instituto Nacional de Estadística.
  14. World Health Organization, 2002. Control of Chagas disease. World Health Organ Tech Rep Ser 905: 82–83.
  15. Guatemala Ministerio de Salud Pública y Asistencia Social, 2003. Manual Operativo de Vigilancia y Control Entomológico de la Enfermedad de Chagas. Ciudad de Guatemala: Ediciones Programa Nacional de Enfermedades Tranmitidas por Vectores, Ministerio de Salud Pública y Asistencia Social.
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