• View in gallery

    Timetable of large-scale insecticide spraying and entomological evaluation by municipality, 2010–2014. Numbers I–IV represent quarters: I, January–March; II, April–June; III, July–September; and IV, October–December. Letters in the table represent type of activity: S1, first round spraying; S2, second round spraying; E1, first entomological evaluation; and E2, second entomological evaluation. In the municipality of Jinotega, first round spraying was discontinued owing to financial reasons.

  • View in gallery

    Data flow of entomological evaluation to assess effectiveness of two rounds of insecticide spraying. Paired data linked by two-way arrows were statistically analyzed. I.I. represents house infestation index (number of houses infested by Triatoma dimidiata/number of houses examined).

  • View in gallery

    Trends of Triatoma dimidiata house infestation index before and after spraying in 293 communities with a single or double spraying round. Numbers in graph area are number of houses infested/investigated.

  • View in gallery

    Geographical distribution of 279 communities where (A) baseline survey (2010), (B) first entomological evaluation (2011–2013), and (C) second entomological evaluation (2012–2014) were conducted for Triatoma dimidiata. The red circles in the map (A) are the clusters identified by space–time analysis (P value < 0.05). Only clusters smaller than a circle with a 10-km radius are reported.

  • 1.

    Coura JR, 2015. The main sceneries of Chagas disease transmission. The vectors, blood and oral transmissions—a comprehensive review. Mem Inst Oswaldo Cruz 110: 277282.

    • Search Google Scholar
    • Export Citation
  • 2.

    PAHO, 2006. Estimación cuantitativa de la Enfermedad de Chagas en las Américas. OPS/HDM/CD/425-06. Department of Control of Neglected Tropical Diseases, Innovative and Intensified Disease Management, Pan American Health Organization, 29.

    • Search Google Scholar
    • Export Citation
  • 3.

    WHO, 2015. Chagas disease in Latin America: an epidemiological update based on 2010 estimates. Wkly Epidemiol Rec 90: 3344.

  • 4.

    Hashimoto K, Yoshioka K, 2012. Review: surveillance of Chagas disease. Adv Parasitol 79: 375428.

  • 5.

    Moncayo A, Silveira AC, 2010. Current trends and future prospects for control of Chagas disease. Talleria J, Tibayrenc M, eds. American Trypanosomiasis Chagas Disease—One Hundred Years of Research. Burlington, MA: Elsevier Inc., 5582.

    • Search Google Scholar
    • Export Citation
  • 6.

    Dias JCP, 2007. Southern Cone Initiative for the elimination of domestic populations of Triatoma infestans and the interruption of transfusional Chagas disease. Historical aspects, present situation, and perspectives. Mem Inst Oswaldo Cruz 102 (Suppl 1): 1118.

    • Search Google Scholar
    • Export Citation
  • 7.

    Hashimoto K, Álvarez H, Nakagawa J, Juarez J, Monroy C, Cordón-Rosales C, Gil E, 2012. Vector control intervention towards interruption of transmission of Chagas disease by Rhodnius prolixus, main vector in Guatemala. Mem Inst Oswaldo Cruz 107: 877887.

    • Search Google Scholar
    • Export Citation
  • 8.

    Hashimoto K, Schofield CJ, 2012. Elimination of Rhodnius prolixus in Central America. Parasit Vectors 5: 45.

  • 9.

    IPCA, 2013. Recomendaciones: Conclusiones. XVa Reunión de la Comisión Intergubernamental de la Iniciativa de los Países de Centroamérica (IPCA) para la Interrupción de la Transmisión Vectorial, Transfusional y Atención Médica de la Enfermedad de Chagas, 22–23 de octubre de 2013, Ciudad de México, México.

    • Search Google Scholar
    • Export Citation
  • 10.

    Waleckx E, Gourbière S, Dumonteil E, 2015. Intrusive versus domiciliated triatomines and the challenge of adapting vector control practices against Chagas disease. Mem Inst Oswaldo Cruz 110: 324338.

    • Search Google Scholar
    • Export Citation
  • 11.

    Bustamante DM, Monroy C, Pineda S, Rodas A, Castro X, Ayala V, Quiñónes J, Moguel B, Trampe R, 2009. Risk factors for intradomiciliary infestation by the Chagas disease vector Triatoma dimidiata in Jutiapa, Guatemala. Cad Saúde Pública 25 (Suppl 1): S83S92.

    • Search Google Scholar
    • Export Citation
  • 12.

    Tabaru Y, Monroy C, Rodas A, Mejia M, Rosales R, 1998. Chemical control of Triatoma dimidiata and Rhodnius prolixus (Reduviidae: Triatominae), the principal vectors of Chagas' disease in Guatemala. Med Entomol Zool 49: 8792.

    • Search Google Scholar
    • Export Citation
  • 13.

    Nakagawa J, Cordón-Rosales C, Juárez J, Itzep C, Nonami T, 2003. Impact of residual spraying on Rhodnius prolixus and Triatoma dimidiata in the department of Zacapa in Guatemala. Mem Inst Oswaldo Cruz 98: 277281.

    • Search Google Scholar
    • Export Citation
  • 14.

    Nakagawa J, Hashimoto K, Cordón-Rosales C, Juárez JA, Trampe R, Marroquín L, 2003. The impact of vector control on Triatoma dimidiata in the Guatemalan department of Jutiapa. Ann Trop Med Parasitol 97: 289298.

    • Search Google Scholar
    • Export Citation
  • 15.

    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: 226230.

    • Search Google Scholar
    • Export Citation
  • 16.

    Manne J, Nakagawa J, Yamagata Y, Goehler A, Brownstein JS, Castro MC, 2012. Triatomine infestation in Guatemala: spatial assessment after two rounds of vector control. Am J Trop Med Hyg 86: 446454.

    • Search Google Scholar
    • Export Citation
  • 17.

    Lugo E, Marín F, 2005. Results of an entomological survey of triatomine (Heteroptera: Reduviidae: Triatominae) in 15 departments of Nicaragua, 1998–1999 [in Spanish]. Rev Nica Ent 65: 112.

    • Search Google Scholar
    • Export Citation
  • 18.

    Yoshioka K, Tercero D, Pérez B, Lugo E, 2011. Rhodnius prolixus in Nicaragua: geographical distribution, control, and surveillance, 1998–2009 [in Spanish]. Rev Panam Salud Publica 30: 439444.

    • Search Google Scholar
    • Export Citation
  • 19.

    IPCA, 2011. Conclusiones, recomendaciones y resoluciones. Décimo tercera reunión de la Comisión Intergubernamental de la Iniciativa de los Países de Centroamérica (IPCA) para la interrupción de la transmission vectorial, transfusional y atención médica de la Enfermedad de Chagas, 17–19 de agosto de 2011, Tegucigalpa, Honduras.

    • Search Google Scholar
    • Export Citation
  • 20.

    MoH, 2012. Informe final: encuesta basal de la Enfermedad de Chagas en 5 SILAIS, Nicaragua, 2010. Managua, Nicaragua: Ministerio de Salud de Nicaragua, Organización Panamericana de la Salud, Agencia de Cooperación Internacional del Japón.

    • Search Google Scholar
    • Export Citation
  • 21.

    Yamagata Y, Nakagawa J, 2006. Control of Chagas disease. Adv Parasitol 61: 129165.

  • 22.

    WHO, 2006. Pesticides and Their Application: For the Control of Vectors and Pests of Public Health Importance, 6th edition. WHO/CDS/NTD/WHOPES/GCDPP/2006.1. Geneva, Switzerland: World Health Organization.

    • Search Google Scholar
    • Export Citation
  • 23.

    WHO, 2007. Manual for Indoor Residual Spraying: Application of Residual Sprays for Vector Control, 3rd edition. WHO/CDS/NTD/WHOPES/GCDPP/2007.3. Geneva, Switzerland: World Health Organization.

    • Search Google Scholar
    • Export Citation
  • 24.

    Monroy C, Mejía 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: 195200.

    • Search Google Scholar
    • Export Citation
  • 25.

    Schofield CJ, 2001. Field Testing and Evaluation of Insecticides for Indoor Residual Spraying against Domestic Vectors of Chagas Disease. Global collaboration for development of pesticides for public health. WHO/CDS/WHOPES/GCDPP/2001.1. Geneva, Switzerland: World Health Organization, 62.

    • Search Google Scholar
    • Export Citation
  • 26.

    Monroy C, Mejía M, Rodas A, Hashimoto T, Tabaru Y, 1998. Assessing methods for the density of Triatoma dimidiata, the principal vector of Chagas' disease in Guatemala. Med Entomol Zool 49: 301307.

    • Search Google Scholar
    • Export Citation
  • 27.

    Kulldorff M, 1997. A spatial scan statistic. Commun Stat Theory Methods 26: 14811496.

  • 28.

    Monroy C, Bustamante DM, Pineda S, Rodas A, Castro X, Ayala V, Quiñónes J, Moguel B, 2009. House improvements and community participation in the control of Triatoma dimidiata re-infestation in Jutiapa, Guatemala. Cad Saúde Pública 25 (Suppl 1): S168S178.

    • Search Google Scholar
    • Export Citation
  • 29.

    Guzman-Tapia Y, Ramirez-Sierra MJ, Escobedo-Ortegon J, Dumonteil E, 2005. Effect of hurricane Isidore on Triatoma dimidiata distribution and Chagas disease transmission risk in the Yacatán Peninsula of Mexico. Am J Trop Med Hyg 73: 10191025.

    • Search Google Scholar
    • Export Citation
  • 30.

    Dumonteil E, Ruiz-Piña H, Rodriguez-Félix E, Barrera-Pérez M, Ramirez-Sierra MJ, Rabinovich JE, Menu F, 2004. Re-infestation of houses by Triatoma dimidiata after intradomicile insecticide application in the Yucatán Peninsula, Mexico. Mem Inst Oswaldo Cruz 99: 253256.

    • Search Google Scholar
    • Export Citation
  • 31.

    Picollo MI, Vassena C, Santo Orihuela P, Barrios S, Zaidemberg M, Zerba E, 2005. High resistance to pyrethroid insecticides associated with ineffective field treatments in Triatoma infestans (Hemiptera: Reduviidae) from northern Argentina. J Med Entomol 42: 637642.

    • Search Google Scholar
    • Export Citation
  • 32.

    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: 436440.

    • Search Google Scholar
    • Export Citation
  • 33.

    Stevens L, Monroy MC, Rodas AG, Hicks RM, Lucero DE, Lyons LA, Dorn PL, 2015. Migration and gene flow among domestic populations of the Chagas insect vector Triatoma dimidiata (Hemiptera: Reduviidae) detected by microsatellite loci. J Med Entomol 52: 419428.

    • Search Google Scholar
    • Export Citation
  • 34.

    Dorn PL, Monroy C, Curtis A, 2007. Triatoma dimidiata (Latreille, 1811): a review of its diversity across its geographic range and the relationship among populations. Infect Genet Evol 7: 343352.

    • Search Google Scholar
    • Export Citation
  • 35.

    Gaspe MS, Provecho YM, Piccinali RV, Gürtler RE, 2015. Where do these bugs come from? Phenotypic structure of Triatoma infestans populations after control interventions in the Argentine Chaco. Mem Inst Oswaldo Cruz 110: 310318.

    • Search Google Scholar
    • Export Citation
  • 36.

    Nieto-Sanchez C, Baus EG, Guerrero D, Grijalva MJ, 2015. Positive deviance study to inform a Chagas disease control program in southern Ecuador. Mem Inst Oswaldo Cruz 110: 299309.

    • Search Google Scholar
    • Export Citation
  • 37.

    Hashimoto K, Zúniga C, Nakamura J, Hanada K, 2015. Integrating an infectious disease programme into the primary health care service: a retrospective analysis of Chagas disease community-based surveillance in Honduras. BMC Health Serv Res 15: 116.

    • Search Google Scholar
    • Export Citation
  • 38.

    Hashimoto K, Yoshioka K, 2014. Certifying achievement in the control of Chagas disease native vectors: what is a viable scenario? Reader's opinion. Mem Inst Oswaldo Cruz 109: 834837.

    • Search Google Scholar
    • Export Citation

 

 

 

 

Effectiveness of Large-Scale Chagas Disease Vector Control Program in Nicaragua by Residual Insecticide Spraying Against Triatoma dimidiata

View More View Less
  • School of Tropical Medicine and Global Health, Nagasaki University, Nagasaki, Japan; Chagas Disease Control Project in Nicaragua, Japan International Cooperation Agency, Managua, Nicaragua; Department of Disease Prevention, Ministry of Health, Managua, Nicaragua; Fuji Environmental Service Inc., Saitama, Japan

Chagas disease is one of the most serious health problems in Latin America. Because the disease is transmitted mainly by triatomine vectors, a three-phase vector control strategy was used to reduce its vector-borne transmission. In Nicaragua, we implemented an indoor insecticide spraying program in five northern departments to reduce house infestation by Triatoma dimidiata. The spraying program was performed in two rounds. After each round, we conducted entomological evaluation to compare the vector infestation level before and after spraying. A total of 66,200 and 44,683 houses were sprayed in the first and second spraying rounds, respectively. The entomological evaluation showed that the proportion of houses infested by T. dimidiata was reduced from 17.0% to 3.0% after the first spraying, which was statistically significant (P < 0.0001). However, the second spraying round did not demonstrate clear effectiveness. Space–time analysis revealed that reinfestation of T. dimidiata is more likely to occur in clusters where the pre-spray infestation level is high. Here we discuss how large-scale insecticide spraying is neither effective nor affordable when T. dimidiata is widely distributed at low infestation levels. Further challenges involve research on T. dimidiata reinfestation, diversification of vector control strategies, and implementation of sustainable vector surveillance.

Introduction

Chagas disease is one of the most serious public health problems in Latin American countries. Its etiological agent, Trypanosoma cruzi, is mostly transmitted by hematophagous triatomine insects, followed by blood transfusion and oral intake.1 The estimated prevalence of Chagas disease in 18 Latin American countries has gradually decreased in recent years from 1.448% in 2005 to 1.055% in 2010.2,3 The reductions in prevalence are considered to be mainly owing to advances in large-scale vector control and screening of blood transfusions in both South and Central America.4

The classical vector control strategy has three phases: 1) preparatory phase for risk mapping and general programming, 2) attack phase for conducting multiple rounds of large-scale insecticide spraying of houses, and 3) surveillance phase for detecting residual foci of triatomine insects after large-scale spraying.5 In South America, this vector control strategy has drastically reduced the house infestation level of Triatoma infestans, and has consequently led to the interruption of vector-borne transmission of Chagas disease.6 After this success in South America, Central American countries also implemented similar vector control programs for eliminating Rhodnius prolixus and reducing Triatoma dimidiata. Effectiveness of the vector control program was proven in Guatemala with respect to interrupting T. cruzi transmission by R. prolixus.7 Neighboring countries followed the same vector control scheme, and R. prolixus is considered to be nearly eliminated in Central America.8 Currently, Central American countries are addressing interruption of T. cruzi transmission by T. dimidiata.9

Triatoma dimidiata is considered a species complex. Its level of adaptation to human dwellings seems to vary widely among regions, from non-domiciled populations in the Yucatan Peninsula and Belize to highly domestic populations in Guatemala.10 In locations where domestic populations of T. dimidiata are predominant, house infestation by this vector is strongly associated with poor housing conditions and the presence of animals in sleeping areas of the dwelling.11 Triatoma dimidiata is susceptible to pyrethroid insecticides. A small-scale field test showed that house infestation by this species could be prevented for 4 months after indoor residual spraying.12 Large-scale operations in eastern Guatemala also showed that large-scale insecticide spraying was effective in substantially reducing house infestation by T. dimidiata.1315 However, unlike R. prolixus, eliminating domestic populations of T. dimidiata is difficult because of its capacity of reinfesting human dwellings after insecticide spraying. Such reinfestation by T. dimidiata is likely to occur with the passage of time after spraying and in geographical hot spots.16

In Nicaragua, the first national entomological survey was conducted in 1998–1999. Among 15 departments surveyed, R. prolixus and T. dimidiata were found in 6 and 15 departments, respectively. By department, the house infestation index (number of houses infested/number of houses investigated × 100) of T. dimidiata ranged from 0.1% to 10.6%.17 Based on this first survey, the Nicaraguan Ministry of Health (MoH) began a vector control program, mainly for R. prolixus. Despite limited geographic coverage, chemical control was successfully implemented toward elimination of R. prolixus.18 Consequently, the interruption of T. cruzi transmission by R. prolixus was certified in 2011.19

Control of T. dimidiata began systematically in 2010, when the MoH conducted a baseline entomological survey with technical and financial support from the Japan International Cooperation Agency (JICA) and Pan American Health Organization (PAHO). This survey, in five departments in northern Nicaragua, determined that the house infestation index of T. dimidiata at municipality level ranged from 0.4% to 19.1%.20 After this baseline survey, the MoH planned large-scale insecticide spraying to reduce indoor populations of T. dimidiata. In this article, we report results of the large-scale spraying program and evaluate its effectiveness in controlling domestic T. dimidiata in Nicaragua. Further challenges are also discussed.

Methods

Site.

The large-scale spraying program was implemented in five departments of northern Nicaragua, namely, Estelí, Jinotega, Madriz, Matagalpa, and Nueva Segovia. In terms of public health administration, these departments cover 49 municipalities in which approximately 3,500 communities are distributed geographically. The total population of the five departments as a whole is 1,700,000, and there are approximately 315,000 dwellings.

Insecticide spraying strategy.

The operational goal of the large-scale spraying program was set to reduce the house infestation index of T. dimidiata to less than 5%. The transmission risk of T. cruzi is considered rare when the house infestation index is below 5%. We applied this same value because although this cutoff value is not based on robust scientific evidence, it has been used conventionally in the control of T. dimidiata.21

Initially, we selected 24 municipalities to conduct large-scale insecticide spraying, in which the house infestation index of T. dimidiata was more than 5% in the baseline entomological survey of 2010.20 After the spraying program was initiated in 2011, we obtained more funding, which enabled us to expand the target areas. By involving municipalities adjacent to those initially selected, the spraying program eventually reached 34 municipalities in total.

The spraying program was carried out in two rounds. For the first round, we prioritized communities with official records of detected T. dimidiata during the period 1998–2010. In the selected communities, all existing dwellings were targeted to be sprayed. In urban areas, exceptionally, only houses with known vector infestation were sprayed. At the end of the spraying activities, the sprayers roughly assessed house infestation levels, namely, flushed-out triatomine bugs were searched for 10 minutes after spraying in each sprayed house. When T. dimidiata was confirmed in more than 5% of sprayed houses in a community, that community was selected for the second round of spraying. As the first round of spraying, the second round targeted all houses to be sprayed in the selected communities.

The Nicaraguan MoH organized one or two field teams in each target municipality to conduct spraying activities. The field team was composed of one supervisor and five or six sprayers. The supervisors were MoH vector control technicians with 10–30 years' experience working in vector control activities. The sprayers were contracted temporarily and trained in spraying techniques and data collection. In target communities, the supervisor assigned up to six houses per day to each sprayer. The quality of spraying techniques was checked daily by the supervisor on site.

Insecticide and spraying technique.

In this spraying program, we used two kinds of pyrethroid-derivative insecticide: etofenprox (20% wettable powder at 0.250 g active ingredient (a.i)/m2) and alpha-cypermethrin (10% wettable powder at 0.030 g a.i/m2). Both are recommended for triatomine control.22 Pyrethroid derivatives have residual vector-controlling effects for several months after application. We principally followed the standardized spraying technique for malaria control, using 8-L Hudson X-pert professional spray tanks (H. D. Hudson Manufacturing Co., Chicago, IL).23 This standard technique allows sprayers to apply solutions of insecticide diluted in water at a rate of 40 mL/m2 on target surfaces.

After explaining the objective of the spraying program to householders, sprayers began the application of insecticide. In intradomestic areas under the house's ceiling, the inner walls, wooden furniture, and wooden beams were sprayed. Bedrooms and sleeping areas were prioritized for spraying because T. dimidiata bugs are often found around beds.24 Kitchens were not sprayed, to avoid contamination of stored food or water with insecticide. In particular, larger amounts of insecticide were deposited within cracks in walls, if present, for improved effectiveness against T. dimidiata hidden inside the cracks. Insecticide was also sprayed in peridomestic areas, especially if chicken coops or pig pens were present, or any other kind of potential refuge for triatomine bugs such as piles of firewood, bricks, adobe, or tiles in courtyards.

For data collection, sprayers registered the following data in paper format: date of spraying, name of community, geographic coordinates, family name, amount of insecticide used, and number of vectors found. Supervisors checked the data quality and aggregated house-level data into community level. In rural communities where 100% of existing houses were targeted, the spraying coverage (% of existing houses sprayed in a target community) was calculated. Community-level data were sent to MoH departmental health offices and entered into a digital database. Triatomine bugs found by sprayers were also sent to these departmental offices for taxonomical identification. In cases of bug misidentification by sprayers, the information was corrected in the database.

Cost estimation.

We collected financial data, to estimate the cost of insecticide spraying. The spraying program was financed by multiple sources including the PAHO and the JICA project, and collateral funding was provided by the Non-Project Grant Aid from the Japanese government. All funds were centrally managed by the Nicaraguan MoH. To estimate the insecticide cost, we used JICA project financial reports, which recorded the price of insecticide in 2010–2013. Combined with the spraying activity database, which provided the average amount of insecticide used per house, we calculated the cost of insecticide per house. For operational costs, including fuel and daily allowance, we used MoH financial records containing the 2012 budgetary disbursements for spraying activities during the first semester of 2013. The operational cost per house was also estimated.

Entomological evaluations.

To measure the effectiveness of insecticide spraying, we designed a quasi-experimental pre–post test without a control group. To compare entomological levels before and after spraying, we intentionally targeted communities that had been assessed in the baseline entomological survey of 2010, which were included in each round of spraying. High-risk communities tended to be targeted in the entomological evaluation because we selected communities for the spraying program that had a history of vector infestation and that were within municipalities with higher infestation levels. We evaluated the same houses in these target communities that had been assessed in the 2010 baseline survey. If family members were absent during the entomological evaluation, inspectors repeatedly visited the targeted houses until examination could be completed. Abandoned or demolished houses were not inspected. Under an assumption that the residual effects of insecticide last up to 6 months, we planned to conduct the evaluations between 90 and 180 days after the first and second rounds of spraying.

We used the man-hour search method as an evaluation technique.25,26 At each target house, two trained inspectors, who were the MoH vector control technicians, searched for triatomine bugs for 30 minutes using searchlights and tweezers. Captured bugs were sent to the MoH's departmental health offices for taxonomical identification. This method was used in the 2010 baseline survey; therefore, the pre- and post-spraying data are comparable in terms of evaluation technique. Inspectors registered community-level data including number of houses examined, number of houses infested by triatomine bugs, site of bug infestation (intra- or peridomestic), and time lapse between spraying and evaluation.

Statistical analysis.

We assessed the effectiveness of insecticide spraying by comparing the entomological data obtained before and after each round of large-scale spraying. Because house-level data were unavailable for this study, we used community as the unit of analysis and calculated the house infestation index (number of houses infested by T. dimidiata/number of houses examined) for each community. Using Stata Statistical Software Release 13.1 (StataCorp LP, College Station, TX), we used the Wilcoxon signed-rank test to assess differences in house infestation indices before and after spraying. Pearson's χ2 test was applied to analyze the relationship between pretreatment house infestation levels and posttreatment reinfestation by T. dimidiata. All statistical analyses were conducted with significance level of 5%.

Mapping and space–time analysis.

To understand spatial patterns of reinfestation by T. dimidiata after insecticide spraying, we created a digital map by plotting those communities in which the two entomological evaluations had been conducted. We collected the geographic coordinates at the approximate center of each community using portable Global Positioning System (GPS) handsets. Administrative boundary maps were provided by Harvard Dataverse Network (https://thedata.harvard.edu/dvn/). Using QGIS version 2.2.0 software, we mapped the communities showing house infestation indices of T. dimidiata at the baseline survey and the two entomological evaluations. Communities with unavailable or inaccurate GPS coordinates were excluded from mapping. Then we used SaTScan version 9.4 software to detect clusters of high infestation in a space–time setting by a Bernoulli model.27 This software scans a window across time and space, noting the number of observed and expected observations inside the window at each location. The window with the maximum likelihood is the most likely cluster in which more high-risk sites are found. To adjust the length of time intervals among the baseline survey and two entomological evaluations, we assigned generic time being time 1 for the baseline survey, 2 for the first entomological evaluation, and 3 for the second entomological evaluation.

Results

A timetable of the spraying program is given in Figure 1. During the program period (2010–2014), 34 municipalities were involved, among which 23 completed two rounds of insecticide spraying and entomological evaluation. Because the spraying program was implemented gradually according to the available financial resources, the first round of spraying and entomological evaluation was conducted at different time points among the different municipalities.

Figure 1.
Figure 1.

Timetable of large-scale insecticide spraying and entomological evaluation by municipality, 2010–2014. Numbers I–IV represent quarters: I, January–March; II, April–June; III, July–September; and IV, October–December. Letters in the table represent type of activity: S1, first round spraying; S2, second round spraying; E1, first entomological evaluation; and E2, second entomological evaluation. In the municipality of Jinotega, first round spraying was discontinued owing to financial reasons.

Citation: The American Society of Tropical Medicine and Hygiene 93, 6; 10.4269/ajtmh.15-0403

Insecticide spraying.

Table 1 summarizes the results of the insecticide spraying program by department. Overall, the first spray round was implemented in 34 municipalities and covered 66,200 houses in 973 communities. Spraying coverage was 85.0% in rural communities. During the spraying activities, 4.9% of treated houses were found to be infested by T. dimidiata. The percentage of infested houses by department ranged from 3.9% in Madriz and Nueva Segovia to 6.6% in Estelí. Among the 973 communities treated, 383 communities (39.4%) had more than 5% of houses infested by T. dimidiata. These were therefore targeted for the second spraying round.

Table 1

Results of large-scale insecticide spraying programs for controlling triatomine vectors in five departments in Nicaragua, 2010–2014

DepartmentNo. of municipalities targetedNo. of communities in the targeted municipalitiesNo. of communities selectedNo. of houses in the selected communities*No. of houses sprayedNo. of houses with Triatoma dimidiataNo. of houses with Rhodnius prolixus
First round of spraying
 Estelí659026722,63915,7921,0470
 Jinotega437417921,74413,5396760
 Madriz62361007,1356,4862550
 Matagalpa871928635,02721,5499492
 Nueva Segovia105091419,9008,8353450
Total342,42897396,44566,2003,2722
Second round of spraying
 Estelí659025216,55613,6954830
 Jinotega43741019,3926,0822870
 Madriz243262,5552,288410
 Matagalpa763018519,62617,4103410
 Nueva Segovia94471006,0315,2081180
Total282,08466454,16044,6831,2700

Sum of all existing houses in urban and rural communities. Note that this sum involves urban houses that were not targeted for spraying.

During the first spray round, R. prolixus was confirmed in two houses in the municipality of San Ramon, Matagalpa, in February 2013. These houses were in close proximity, and the same construction materials were used in both houses (i.e., wooden frame, tin roofing, dried grass walls, and earthen floor). In these two houses, five specimens of R. prolixus were collected, including three adults and two nymphs that were found in the dried grass walls and in a hen's nest under the beds. Four specimens were microscopically analyzed for the presence of T. cruzi in their gut contents, but all specimens proved negative. Owing to this finding, all communities in the municipality of San Ramon were targeted for the second round of spraying, to ensure elimination of R. prolixus.

In the second spraying round involving 28 municipalities, 44,683 houses were treated in 664 communities (Table 1). Because the second round was extended to communities adjacent to those found to be highly infested in the first spray round, 221 communities were newly involved. As a result, spraying coverage in rural communities reached 89.7%. In the target communities, 2.8% of treated houses were found to be infested by T. dimidiata, with a department-level range from 1.8% in Madriz to 3.5% in Estelí. Among the 664 communities treated, more than 5% of sprayed houses were found infested by T. dimidiata in 148 (22.3%) communities. No R. prolixus was confirmed in the second spraying round.

Cost estimation of insecticide spraying.

We calculated separately the cost of insecticide and other operational costs including fuel and daily allowance for sprayers, supervisors, and drivers. According to the JICA project's financial report, etofenprox was procured at US$40.10/kg in 2010 and alpha-cypermethrin at US$94.5/kg in 2011–2013. The spraying program database registered that the average amount of these insecticides used per house in 2010–2014 was 267.5 and 64.2 g, respectively. Thus, the calculated cost of insecticide per house was US$10.73 for etofenprox and US$6.07 for alpha-cypermethrin.

With respect to operational costs, the MoH appropriated 30 Nicaraguan córdoba (C$) per 1-L diesel. The daily allowance for sprayers, supervisors, and drivers was C$150 per day, according to MoH regulations. When accommodation was necessary, C$200 was added to the daily allowance. For spraying activities in the first semester of 2013, in which 41,493 houses were to be sprayed, the MoH disbursed a total of C$180,000 for fuel. Total daily allowance was C$3,011,400, C$501,900, and C$90,000 for sprayers, supervisors, and drivers, respectively. Thus, the operational cost per house was estimated to be C$91.20, that is, US$3.80 at the 2012 average exchange rate. In sum, the total cost per house, including insecticide, fuel, and daily allowance, was US$14.53 for etofenprox and US$9.87 for alpha-cypermethrin.

Entomological evaluation.

Figure 2 shows the data flow for entomological evaluation. We identified 307 communities that were assessed in the 2010 baseline survey and then targeted for the first round of the spraying program. The pretreatment house infestation index of T. dimidiata in these 307 communities was 17.0% (725/4,248 houses). During the first spray round, 14 communities dropped out, that is, spraying activities or entomological evaluation were not conducted. Among 293 communities included in the first treatment round, 172 communities proceeded to the second round and no communities dropped out. Thus, among 307 communities selected for entomological evaluation, 172 were sprayed twice, 121 were sprayed only once, and 14 were dropped out.

Figure 2.
Figure 2.

Data flow of entomological evaluation to assess effectiveness of two rounds of insecticide spraying. Paired data linked by two-way arrows were statistically analyzed. I.I. represents house infestation index (number of houses infested by Triatoma dimidiata/number of houses examined).

Citation: The American Society of Tropical Medicine and Hygiene 93, 6; 10.4269/ajtmh.15-0403

After the first spray round, we observed a substantial decrease in the T. dimidiata house infestation index (Figure 2). In the communities targeted for the first entomological evaluation, this index was dramatically reduced from 17.0% to 3.0% (122/4,049). The difference in house infestation index before and after first round spraying was statistically significant (P < 0.0001). In contrast, the second entomological evaluation in 172 communities revealed that the house infestation index of T. dimidiata had increased slightly from 3.4% (80/2,346) to 4.4% (102/2,324). However, the difference was not statistically significant (P = 0.21). A similar increase in this index was also seen at the second entomological evaluation in those communities where a second spray treatment was not applied (Figure 3).

Figure 3.
Figure 3.

Trends of Triatoma dimidiata house infestation index before and after spraying in 293 communities with a single or double spraying round. Numbers in graph area are number of houses infested/investigated.

Citation: The American Society of Tropical Medicine and Hygiene 93, 6; 10.4269/ajtmh.15-0403

Table 2 provides details of the entomological evaluation by department. Although this evaluation is not designed for cross-departmental comparison, the infestation level of T. dimidiata in Jinotega was found to be higher than the other four departments for pre-spray as well as post-spray indices. Longitudinal trends of infestation indices were similar among the five departments over time. In the first entomological evaluation, we observed that the house infestation index was reduced from 11.7–23.8% to 2.1–5.6%. In the second evaluation, the house infestation index increased slightly, except in Nueva Segovia. In both the first and second entomological evaluation, intradomestic areas were found to be more infested by T. dimidiata than peridomestic areas. The average time lapse between insecticide spraying and entomological evaluation was about 4 months in both rounds.

Table 2

House infestation index of Triatoma dimidiata before and after insecticide spraying, by department in Nicaragua, 2010–2014

DepartmentBaseline survey (307 communities)Evaluation 1 (293 communities sprayed in the first spray round)Evaluation 2 (172 communities sprayed in the second spray round)
No. of houses examinedOverall infestation index (%)No. of houses examinedInfestation index (%)Mean time lapse in days (range)*No. of houses examinedInfestation index (%)Mean time lapse in days (range)*
DomesticPeridomesticOverallDomesticPeridomesticOverall
Estelí1,63815.71,6241.80.42.3131.1 (61–292)8083.51.44.8118.6 (41–166)
Jinotega60923.84624.11.55.6186.8 (44–417)3114.82.97.7160.2 (103–219)
Madriz39311.73741.60.52.1141.9 (99–192)3431.51.52.9239.2 (79–372)
Matagalpa92418.09052.40.32.8120.5 (79–170)5473.30.43.7102.4 (63–145)
Nueva Segovia68416.16842.61.23.8123.5 (92–201)3152.20.62.9109.2 (92–131)
Total4,24817.04,0492.30.73.0136.3 (44–417)2,3243.11.24.4131.6 (41–372)

Time lapse in days between insecticide spraying and entomological evaluation.

Space–time analysis.

In Figure 4, we plotted 279 communities where baseline, first, and second entomological evaluations were conducted. We could not represent 14 communities owing to missing or inaccurate geographical coordinates. The left map (Figure 4A) shows all plotted communities that were infested by T. dimidiata at the baseline survey, among which some had a house infestation index of more than 25%. The middle and right maps (Figure 4B and C) show the geographic distribution of communities with T. dimidiata infestation index at the post-spray evaluations. The space–time analysis identified eight clusters (demonstrated as red circles in the map [Figure 4A]) where the house infestation of T. dimidiata are most likely to happen across space and time. These clusters are located around the communities with high pre-spray infestation level. The χ2 test confirmed the same trends (Tables 3 and 4): initial house infestation of more than 25% is significantly associated with reinfestation at the first entomological evaluation (P = 0.030); reinfestation at the first entomological evaluation is also associated with reinfestation at the second evaluation (P = 0.014).

Figure 4.
Figure 4.

Geographical distribution of 279 communities where (A) baseline survey (2010), (B) first entomological evaluation (2011–2013), and (C) second entomological evaluation (2012–2014) were conducted for Triatoma dimidiata. The red circles in the map (A) are the clusters identified by space–time analysis (P value < 0.05). Only clusters smaller than a circle with a 10-km radius are reported.

Citation: The American Society of Tropical Medicine and Hygiene 93, 6; 10.4269/ajtmh.15-0403

Table 3

Relationship between pre-spraying Triatoma dimidiata house infestation index and reinfestation at the first entomological evaluation

No. of communitiesReinfestation at the first entomological evaluationTotal
Not confirmedConfirmed
Pre-spray house infestation index< 25%15651207
≥ 25%543286
Total21083293
  χ2 test P = 0.030
Table 4

Relationship between reinfestation at the first and second entomological evaluations

No. of communitiesReinfestation at the second entomological evaluationTotal
Not confirmedConfirmed
Reinfestation at the first entomological evaluationNot confirmed14862210
Confirmed463783
Total19499293
  χ2 test P = 0.014

Discussion

The spraying program described here was implemented systematically at large scale with an expected result of reduced vector infestation. Although the first spray treatment and entomological evaluation were conducted at different points in time owing to limited financial resources during 2010–2012, spraying ultimately covered 34 municipalities among which 23 completed two rounds each of spraying and entomological evaluation. A total of 78,623 houses were sprayed at least once, and the cumulative total of treated dwellings reached 110,883 in the two rounds of spraying. Considering the risk-driven strategy to identify treatment needs and the results of entomological evaluation in the selected communities, we can definitely assume that the spraying program had a strong impact on controlling indoor populations of T. dimidiata and reducing the transmission risk of Chagas disease in these five departments of Nicaragua.

Entomological evaluation demonstrated that house infestation levels of T. dimidiata were drastically reduced after the first insecticide treatment, from 17.0% to 3.0%. Although the pre–post design used does not allow us to determine exact causality, we can strongly infer that the observed reduction of T. dimidiata can be attributed mainly to the insecticide spraying. Apart from chemical control with insecticide, populations of T. dimidiata could be influenced by improvements in housing or by climate events, such as hurricanes.28,29 However, no such large-scale socioeconomic or environmental changes were seen during 2010–2014. To the best of our knowledge, the insecticide spraying program was the only intervention during this period that could contribute widely to the large reduction in domestic populations of T. dimidiata.

By contrast, we found no significant changes in T. dimidiata house infestation levels after the second spray treatment. Rather, the observed infestation levels had increased slightly in both treated and non-treated communities at the second entomological evaluation (Figure 3). The reason for the increased index could be mainly owing to the limited sensitivity of the man-hour manual search. Monroy and others compared the number of T. dimidiata found by the man-hour search method with that found after demolishing an entire house and showed that only 7.0% of the total bugs present could be found by the man-hour method.24 This manual searching technique involves technical bias owing to inspectors' motivation and skill. It is possible that in our study, those bug inspectors who performed the first entomological evaluation had improved their bug searching skills by the second evaluation.

The results of the second entomological evaluation suggest that large-scale insecticide spraying would not be effective where infestation levels are relatively low. A previous study in Guatemala showed that multiple rounds of insecticide spraying was necessary to reduce the T. dimidiata infestation index from 40% to 5% or less.15 When the initial infestation index was around 20%, a single spraying was sufficient to reduce the infestation index below 5%. In our study in Nicaragua, the initial infestation index was 17.0% on average; thus a single spray treatment would have been sufficient to reduce the infestation level below 5%. However, the long-term effect of multiple spraying should be examined. Hashimoto and others15 reported recovery of the T. dimidiata infestation index after a single spraying. Even if the second treatment is not effective in reducing the infestation index when the initial infestation level is low, it may have long-term impacts in suppressing reinfestation by T. dimidiata. Longitudinal monitoring is necessary to understand the reinfestation patterns in communities with single and multiple spray treatments.

With respect to economic aspects, the cost of insecticide spraying for Chagas disease vector control remains a financial burden in Central America. In a previous experience in Guatemala, the cost of spraying per house was US$9.12, which included the cost of insecticide (deltamethrin or beta-cyfluthrin), sprayers' salaries, fuel, and vehicle maintenance.13 A simple comparison with our cost estimates in Nicaragua is inappropriate because we included labor costs for supervisors and drivers and did not include costs for vehicle maintenance. However, the cost per house in Guatemala was similar to our cost estimation with alpha-cypermethrin, which was US$9.87 per house. In Nicaragua, the cost of large-scale spraying for Chagas disease vector control was not affordable for the MoH, and the procurement of insecticide depended entirely on external funding. As Nakagawa and others13 observed, the cost of insecticide plays a crucial role in lowering the entire cost of spraying operations.

Triatoma dimidiata has a high capacity of reinfesting human dwellings after insecticide spraying in Central America.15,30 Understanding the mechanism of reinfestation is crucial to formulating an effective post-spray control strategy for T. dimidiata. Theoretically, reinfestation can occur in two ways: 1) vectors survive the insecticide treatment or 2) vectors migrate to treated houses after spraying.25 The first option of survival is mainly owing to insufficient coverage or unskilled insecticide spraying techniques, including poor dilution of insecticide, inadequate water pH in which the insecticide is prepared, and poor penetration of insecticide in the wall cracks where T. dimidiata lives. A repellent effect of insecticide could be a reason of survival, enabling vectors to detect residues of insecticidal component and escape to sites without residues, such as deep wall cracks or ceiling. The vector's resistance to pyrethroid is another possible reason for survival, as was the case for T. infestans in northern Argentina.31 However, there is no evidence in Central America of T. dimidiata developing insecticide resistance.

Regarding the second option of reinfestation by vector migration, the pattern of reinvasion to sprayed houses by T. dimidiata could vary in sources and ways of migration. Triatoma dimidiata can come from the peridomestic ecotopes and even from other houses or adjacent communities.32,33 Sylvatic population of T. dimidiata might also be a source of reinvasion. Triatoma dimidiata can move by active transportation (i.e., flying) or passive transportation (i.e., carried by humans, animals, farming implements, or tacks). In addition, capacity of reinfestation may differ widely among subgroups of T. dimidiata.10,34 Given such complex mechanisms, the effective control of reinfestation is difficult without understanding the pattern of reinfestation of T. dimidiata in each local setting.

In this study, we also observed infestation by T. dimidiata after both the first and second rounds of spraying. The entomological evaluations found 2- to 3-fold higher numbers of infested houses in intradomestic ecotopes than in peridomestic ecotopes (Table 2). This result may suggest that more reinfestant vectors were survivors within houses evaluated prior to spraying; however, this does not exclude the possibility of vector migration after treatment. It is likely that the reinfestant vector population would be a mix of surviving and reinvading vectors, but further analysis is not possible using the available data in this study. For this problem, genetic or morphometric studies will provide valuable information, comparing the spatial patterns and population structures of vectors before and after insecticide spraying. For instance, a morphometric study in Chaco Province of Argentina suggested that reinfestant T. infestans came from external sources because they were significantly different from the pretreatment vector population.35 Similar studies should be encouraged for improving understanding of the reinfestation pattern of T. dimidiata.

Figure 4, although our data are patchy because of the limited number of communities investigated, shows that the communities where reinfestation was confirmed are not uniformly distributed. Instead, the reinfested communities seem to be gathered in some specific areas. The space–time analysis identified high-risk clusters around communities highly infested at the baseline survey. Tables 3 and 4 also suggest that communities with high pre-spray infestation indices are likely to be reinfested after spraying, and further reinfestation could occur in such communities. These results are consistent enough to lead a conclusion that the reinfestation by T. dimidiata is more likely to happen in some spatial clusters where the inherent infestation level is high. Existence of such clusters vulnerable to the T. dimidiata reinfestation is compatible with the previous spatial study in Guatemala.16 Probably in the high-risk clusters, the communities share the similar environmental or housing conditions and exchange vectors constantly among them. To address the reinfestation of T. dimidiata efficiently, the MoH's vector control program should pay more attention to the areas where some communities with high pre-spray infestation level are gathered.

The present spraying program provided strong evidence toward the elimination of R. prolixus in the targeted five departments. In Nicaragua, after large-scale spraying activities for controlling R. prolixus in 1998–2000, this species was sporadically detected in 2002–2009.18 This implies that the initial spraying program left some communities untreated and vulnerable to probable infestation with R. prolixus. The spraying program in 2010–2014 complemented the initial program to expand the geographic control coverage. As a consequence, R. prolixus was still detected in one community from the municipality of San Ramon during the first spraying round in 2013. The absence of R. prolixus was confirmed in the second round, which included all communities in this municipality. Yet it remains uncertain if the control coverage was sufficient to detect all R. prolixus in the region. Entomological surveillance must be sustained to ensure elimination of R. prolixus in Nicaragua.

Further challenges for preventing vector-borne transmission of T. cruzi by T. dimidiata include implementing multilevel approaches. At the operational level, a single intervention relying only on indoor insecticide spraying is unsuitable for controlling T. dimidiata, which can repeatedly reinfest human dwellings. There is a need to seek an optimal mix of chemical and ecological approaches, such as improving dwellings with locally available materials.28 In addition, encouraging certain behaviors among community members, such as self-fumigation of dwellings or relocation of domestic animals away from the house, could offer easy anti-triatomine solutions.36 At the strategic level, the classical three-phase vector control strategy, that is, preparation, attack, and surveillance,5 is no longer appropriate in scenarios where T. dimidiata is distributed widely at low levels of infestation. The attack phase of this strategy (i.e., large-scale insecticide spraying) is not cost-effective or affordable for Central American settings. An alternative strategy is to first implement community-based vector surveillance in all areas suspected of T. dimidiata infestation. Such vector surveillance, once integrated into primary health-care services, can be administrated in a sustainable way and will enable detection of vector infestation foci.37 At the international policy level, the current common goal that emphasizes the interruption of vector-borne transmission is no longer suitable for controlling T. dimidiata. Policy change is needed, which adds weight to sustainable control rather than the interruption of disease transmission.38

In conclusion, we demonstrated substantial effectiveness of large-scale insecticide spraying to reduce house infestation levels of T. dimidiata. However, because of frequent reinfestation by T. dimidiata as well as the financial burden, such large-scale spraying is not a deliberate strategic option, particularly when house infestation levels of T. dimidiata are low. Further research will help to gain a thorough understanding of the mechanisms of T. dimidiata reinfestation. Operational, strategic, and policy innovations are necessary, to implement more cost-effective and sustainable vector control programs.

ACKNOWLEDGMENTS

We appreciate the laborious efforts of those who participated in the field operations of spraying and entomological evaluation. We also thank the householders who kindly accepted the spraying activities. Thanks to Toshihiko Sunahara for technical advices on space–time analysis.

  • 1.

    Coura JR, 2015. The main sceneries of Chagas disease transmission. The vectors, blood and oral transmissions—a comprehensive review. Mem Inst Oswaldo Cruz 110: 277282.

    • Search Google Scholar
    • Export Citation
  • 2.

    PAHO, 2006. Estimación cuantitativa de la Enfermedad de Chagas en las Américas. OPS/HDM/CD/425-06. Department of Control of Neglected Tropical Diseases, Innovative and Intensified Disease Management, Pan American Health Organization, 29.

    • Search Google Scholar
    • Export Citation
  • 3.

    WHO, 2015. Chagas disease in Latin America: an epidemiological update based on 2010 estimates. Wkly Epidemiol Rec 90: 3344.

  • 4.

    Hashimoto K, Yoshioka K, 2012. Review: surveillance of Chagas disease. Adv Parasitol 79: 375428.

  • 5.

    Moncayo A, Silveira AC, 2010. Current trends and future prospects for control of Chagas disease. Talleria J, Tibayrenc M, eds. American Trypanosomiasis Chagas Disease—One Hundred Years of Research. Burlington, MA: Elsevier Inc., 5582.

    • Search Google Scholar
    • Export Citation
  • 6.

    Dias JCP, 2007. Southern Cone Initiative for the elimination of domestic populations of Triatoma infestans and the interruption of transfusional Chagas disease. Historical aspects, present situation, and perspectives. Mem Inst Oswaldo Cruz 102 (Suppl 1): 1118.

    • Search Google Scholar
    • Export Citation
  • 7.

    Hashimoto K, Álvarez H, Nakagawa J, Juarez J, Monroy C, Cordón-Rosales C, Gil E, 2012. Vector control intervention towards interruption of transmission of Chagas disease by Rhodnius prolixus, main vector in Guatemala. Mem Inst Oswaldo Cruz 107: 877887.

    • Search Google Scholar
    • Export Citation
  • 8.

    Hashimoto K, Schofield CJ, 2012. Elimination of Rhodnius prolixus in Central America. Parasit Vectors 5: 45.

  • 9.

    IPCA, 2013. Recomendaciones: Conclusiones. XVa Reunión de la Comisión Intergubernamental de la Iniciativa de los Países de Centroamérica (IPCA) para la Interrupción de la Transmisión Vectorial, Transfusional y Atención Médica de la Enfermedad de Chagas, 22–23 de octubre de 2013, Ciudad de México, México.

    • Search Google Scholar
    • Export Citation
  • 10.

    Waleckx E, Gourbière S, Dumonteil E, 2015. Intrusive versus domiciliated triatomines and the challenge of adapting vector control practices against Chagas disease. Mem Inst Oswaldo Cruz 110: 324338.

    • Search Google Scholar
    • Export Citation
  • 11.

    Bustamante DM, Monroy C, Pineda S, Rodas A, Castro X, Ayala V, Quiñónes J, Moguel B, Trampe R, 2009. Risk factors for intradomiciliary infestation by the Chagas disease vector Triatoma dimidiata in Jutiapa, Guatemala. Cad Saúde Pública 25 (Suppl 1): S83S92.

    • Search Google Scholar
    • Export Citation
  • 12.

    Tabaru Y, Monroy C, Rodas A, Mejia M, Rosales R, 1998. Chemical control of Triatoma dimidiata and Rhodnius prolixus (Reduviidae: Triatominae), the principal vectors of Chagas' disease in Guatemala. Med Entomol Zool 49: 8792.

    • Search Google Scholar
    • Export Citation
  • 13.

    Nakagawa J, Cordón-Rosales C, Juárez J, Itzep C, Nonami T, 2003. Impact of residual spraying on Rhodnius prolixus and Triatoma dimidiata in the department of Zacapa in Guatemala. Mem Inst Oswaldo Cruz 98: 277281.

    • Search Google Scholar
    • Export Citation
  • 14.

    Nakagawa J, Hashimoto K, Cordón-Rosales C, Juárez JA, Trampe R, Marroquín L, 2003. The impact of vector control on Triatoma dimidiata in the Guatemalan department of Jutiapa. Ann Trop Med Parasitol 97: 289298.

    • Search Google Scholar
    • Export Citation
  • 15.

    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: 226230.

    • Search Google Scholar
    • Export Citation
  • 16.

    Manne J, Nakagawa J, Yamagata Y, Goehler A, Brownstein JS, Castro MC, 2012. Triatomine infestation in Guatemala: spatial assessment after two rounds of vector control. Am J Trop Med Hyg 86: 446454.

    • Search Google Scholar
    • Export Citation
  • 17.

    Lugo E, Marín F, 2005. Results of an entomological survey of triatomine (Heteroptera: Reduviidae: Triatominae) in 15 departments of Nicaragua, 1998–1999 [in Spanish]. Rev Nica Ent 65: 112.

    • Search Google Scholar
    • Export Citation
  • 18.

    Yoshioka K, Tercero D, Pérez B, Lugo E, 2011. Rhodnius prolixus in Nicaragua: geographical distribution, control, and surveillance, 1998–2009 [in Spanish]. Rev Panam Salud Publica 30: 439444.

    • Search Google Scholar
    • Export Citation
  • 19.

    IPCA, 2011. Conclusiones, recomendaciones y resoluciones. Décimo tercera reunión de la Comisión Intergubernamental de la Iniciativa de los Países de Centroamérica (IPCA) para la interrupción de la transmission vectorial, transfusional y atención médica de la Enfermedad de Chagas, 17–19 de agosto de 2011, Tegucigalpa, Honduras.

    • Search Google Scholar
    • Export Citation
  • 20.

    MoH, 2012. Informe final: encuesta basal de la Enfermedad de Chagas en 5 SILAIS, Nicaragua, 2010. Managua, Nicaragua: Ministerio de Salud de Nicaragua, Organización Panamericana de la Salud, Agencia de Cooperación Internacional del Japón.

    • Search Google Scholar
    • Export Citation
  • 21.

    Yamagata Y, Nakagawa J, 2006. Control of Chagas disease. Adv Parasitol 61: 129165.

  • 22.

    WHO, 2006. Pesticides and Their Application: For the Control of Vectors and Pests of Public Health Importance, 6th edition. WHO/CDS/NTD/WHOPES/GCDPP/2006.1. Geneva, Switzerland: World Health Organization.

    • Search Google Scholar
    • Export Citation
  • 23.

    WHO, 2007. Manual for Indoor Residual Spraying: Application of Residual Sprays for Vector Control, 3rd edition. WHO/CDS/NTD/WHOPES/GCDPP/2007.3. Geneva, Switzerland: World Health Organization.

    • Search Google Scholar
    • Export Citation
  • 24.

    Monroy C, Mejía 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: 195200.

    • Search Google Scholar
    • Export Citation
  • 25.

    Schofield CJ, 2001. Field Testing and Evaluation of Insecticides for Indoor Residual Spraying against Domestic Vectors of Chagas Disease. Global collaboration for development of pesticides for public health. WHO/CDS/WHOPES/GCDPP/2001.1. Geneva, Switzerland: World Health Organization, 62.

    • Search Google Scholar
    • Export Citation
  • 26.

    Monroy C, Mejía M, Rodas A, Hashimoto T, Tabaru Y, 1998. Assessing methods for the density of Triatoma dimidiata, the principal vector of Chagas' disease in Guatemala. Med Entomol Zool 49: 301307.

    • Search Google Scholar
    • Export Citation
  • 27.

    Kulldorff M, 1997. A spatial scan statistic. Commun Stat Theory Methods 26: 14811496.

  • 28.

    Monroy C, Bustamante DM, Pineda S, Rodas A, Castro X, Ayala V, Quiñónes J, Moguel B, 2009. House improvements and community participation in the control of Triatoma dimidiata re-infestation in Jutiapa, Guatemala. Cad Saúde Pública 25 (Suppl 1): S168S178.

    • Search Google Scholar
    • Export Citation
  • 29.

    Guzman-Tapia Y, Ramirez-Sierra MJ, Escobedo-Ortegon J, Dumonteil E, 2005. Effect of hurricane Isidore on Triatoma dimidiata distribution and Chagas disease transmission risk in the Yacatán Peninsula of Mexico. Am J Trop Med Hyg 73: 10191025.

    • Search Google Scholar
    • Export Citation
  • 30.

    Dumonteil E, Ruiz-Piña H, Rodriguez-Félix E, Barrera-Pérez M, Ramirez-Sierra MJ, Rabinovich JE, Menu F, 2004. Re-infestation of houses by Triatoma dimidiata after intradomicile insecticide application in the Yucatán Peninsula, Mexico. Mem Inst Oswaldo Cruz 99: 253256.

    • Search Google Scholar
    • Export Citation
  • 31.

    Picollo MI, Vassena C, Santo Orihuela P, Barrios S, Zaidemberg M, Zerba E, 2005. High resistance to pyrethroid insecticides associated with ineffective field treatments in Triatoma infestans (Hemiptera: Reduviidae) from northern Argentina. J Med Entomol 42: 637642.

    • Search Google Scholar
    • Export Citation
  • 32.

    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: 436440.

    • Search Google Scholar
    • Export Citation
  • 33.

    Stevens L, Monroy MC, Rodas AG, Hicks RM, Lucero DE, Lyons LA, Dorn PL, 2015. Migration and gene flow among domestic populations of the Chagas insect vector Triatoma dimidiata (Hemiptera: Reduviidae) detected by microsatellite loci. J Med Entomol 52: 419428.

    • Search Google Scholar
    • Export Citation
  • 34.

    Dorn PL, Monroy C, Curtis A, 2007. Triatoma dimidiata (Latreille, 1811): a review of its diversity across its geographic range and the relationship among populations. Infect Genet Evol 7: 343352.

    • Search Google Scholar
    • Export Citation
  • 35.

    Gaspe MS, Provecho YM, Piccinali RV, Gürtler RE, 2015. Where do these bugs come from? Phenotypic structure of Triatoma infestans populations after control interventions in the Argentine Chaco. Mem Inst Oswaldo Cruz 110: 310318.

    • Search Google Scholar
    • Export Citation
  • 36.

    Nieto-Sanchez C, Baus EG, Guerrero D, Grijalva MJ, 2015. Positive deviance study to inform a Chagas disease control program in southern Ecuador. Mem Inst Oswaldo Cruz 110: 299309.

    • Search Google Scholar
    • Export Citation
  • 37.

    Hashimoto K, Zúniga C, Nakamura J, Hanada K, 2015. Integrating an infectious disease programme into the primary health care service: a retrospective analysis of Chagas disease community-based surveillance in Honduras. BMC Health Serv Res 15: 116.

    • Search Google Scholar
    • Export Citation
  • 38.

    Hashimoto K, Yoshioka K, 2014. Certifying achievement in the control of Chagas disease native vectors: what is a viable scenario? Reader's opinion. Mem Inst Oswaldo Cruz 109: 834837.

    • Search Google Scholar
    • Export Citation

Author Notes

* Address correspondence to Kota Yoshioka, School of Tropical Medicine and Global Health, Nagasaki University, 1-12-4, Sakamoto, Nagasaki, Japan. E-mail: yoshiokakota@gmail.com

Financial support: The vector control program described in this article was conducted with financial contributions from the Embassy of Japan in Nicaragua, Japan International Cooperation Agency (JICA), and Pan American Health Organization (PAHO).

Authors' addresses: Kota Yoshioka, School of Tropical Medicine and Global Health, Nagasaki University, Nagasaki, Japan, and Chagas Disease Control Project in Nicaragua, Japan International Cooperation Agency, Managua, Nicaragua, E-mail: yoshiokakota@gmail.com. Jiro Nakamura, Byron Pérez, and Doribel Tercero, Chagas Disease Control Project in Nicaragua, Japan International Cooperation Agency, Managua, Nicaragua, E-mails: jironjp@yahoo.co.jp, byronperezr@yahoo.com, and doriter_16@yahoo.com. Lenin Pérez, Department of Disease Prevention, Ministry of Health, Managua, Nicaragua, E-mail: chagas@minsa.gob.ni. Yuichiro Tabaru, Fuji Environmental Service Inc., Saitama, Japan, E-mail: tabarito@fujikankyo.com.

Save