Ahead of Print -Residual Infestation and Recolonization during Urban Triatoma infestans Bug Control Campaign, Peru1 - Volume 20, Number 12—December 2014 - Emerging Infectious Disease journal - CDC
Volume 20, Number 12—December 2014
Research
Residual Infestation and Recolonization during Urban Triatoma infestans Bug Control Campaign, Peru1
On This Page
Corentin M. Barbu , Alison M. Buttenheim, Maria-Luz Hancco Pumahuanca, Javier E. Quintanilla Calderón, Renzo Salazar, Malwina Carrión, Andy Catacora Rospigliossi, Fernando S. Malaga Chavez, Karina Oppe Alvarez, Juan Cornejo del Carpio, César Náquira, and Michael Z. Levy
Abstract
Chagas disease vector control campaigns are being conducted in Latin America, but little is known about medium-term or long-term effectiveness of these efforts, especially in urban areas. After analyzing entomologic data for 56,491 households during the treatment phase of a Triatoma infestans bug control campaign in Arequipa, Peru, during 2003–2011, we estimated that 97.1% of residual infestations are attributable to untreated households. Multivariate models for the surveillance phase of the campaign obtained during 2009–2012 confirm that nonparticipation in the initial treatment phase is a major risk factor (odds ratio [OR] 21.5, 95% CI 3.35–138). Infestation during surveillance also increased over time (OR 1.55, 95% CI 1.15–2.09 per year). However, we observed a negative interaction between nonparticipation and time (OR 0.73, 95% CI 0.53–0.99), suggesting that recolonization by vectors progressively dilutes risk associated with nonparticipation. Although the treatment phase was effective, recolonization in untreated households threatens the long-term success of vector control.
Chagas disease, an often deadly disease widespread in the Americas, is caused by the protozoan parasiteTrypanosoma cruzi (1,2) and transmitted by hematophageous triatomine insects (3). In southern South AmericaTriatoma infestans bugs are the primary vector (2). In 1991, the nations of this region created the Southern Cone Initiative to coordinate control efforts against T. infestans bugs. During the first decade of this initiative, 2.5 million households were treated with insecticide (4), which led to disruption of transmission of T. cruzi by T. infestans bugs in several countries and states (2). However, vector control efforts have at times failed unexpectedly and repeatedly in some areas (5,6).
Across most of its range, T. infestans bugs are found predominantly in rural areas (2). However, the vector has become an urban problem in Arequipa, Peru, a city of 850,000 inhabitants (7–9) where infected vectors have been observed since 1952 (10). Since 2003, municipal authorities and the regional ministry of health, in collaboration with the Pan American Health Organization, have worked to eliminate the vector from this city. The challenges to elimination in an urban area potentially differ from those in rural settings. Urban households have smaller peridomestic areas, fewer sources of blood, and fewer hiding places for the vector, thus mitigating some of the difficulties encountered in rural environments (7,11–13). However, although participation in control campaigns in rural areas is typically high (5,7), more affluent urban populations (14) might be more reluctant to participate (15). Thus, household level control might be easier in an urban household than in a rural household. However, at the community level, sustained control in an urban community might be more difficult.
We explored this hypothesis by using data obtained in Arequipa during the initial treatment phase or attack phase of the vector campaign and during the subsequent surveillance phase after insecticide application. We evaluated the effectiveness of the treatment phase in 3 ways. First, we estimated the reduction in the infestation prevalence resulting from the 2 insecticide applications of the treatment phase. Second, we modeled recolonization (the colonization of new households after the initial treatment) as a function of treatment phase factors. Third, during the surveillance phase, we tested insects captured from households treated during the treatment phase for resistance to insecticide. We discuss converging results of these approaches in terms of their implications for continued efforts of the control campaign in Arequipa and, more generally, for design of strategies to control Chagas disease vectors in urban environments.
Dr Barbu is a postdoctoral fellow in epidemiology at the University of Pennsylvania, Philadelphia, Pennsylvania. His primary research interest is applying computational and statistical methods to understand and control populations of Chagas disease vectors.
Acknowledgments
We thank the Ministerio de Salud del Peru, the Dirección General de Salud de las Personas through the Estrategia Sanitaria Nacional de Prevención y Control de Enfermedades Metaxénicas y Otras Transmitidas por Vectores, the Dirección General de Salud Ambiental, the Gobierno Regional de Arequipa, the Gerencia Regional de Salud de Arequipa, the Red de Salud Arequipa Caylloma, the Pan American Health Organization, the Canadian International Development Agency, and the Gobierno Regional de Arequipa for organizing and conducting the Chagas disease control campaign in Arequipa; and Sébastien Gourbière, Yage Wu, Daniel Rivera Lana, Karthik Sethuraman, and Dylan Tracy for providing editing suggestions for the manuscript.
This study was supported by National Institutes of Health grants NIH-NIAID R01AI101229, P50 AI074285, and K01 AI079162, and a University of Pennsylvania Global Engagement grant.
References
- Maguire JH, Hoff R, Sherlock I, Guimarães AC, Sleigh AC, Ramos NB, Cardiac morbidity and mortality due to Chagas’ disease: prospective electrocardiographic study of a Brazilian community. Circulation. 1987;75:1140–5. DOIPubMed
- Moncayo A. Chagas disease: current epidemiological trends after the interruption of vectorial and transfusional transmission in the Southern Cone countries. Mem Inst Oswaldo Cruz. 2003;98:577–91. DOIPubMed
- Gourbière S, Dorn P, Tripet F, Dumonteil E. Genetics and evolution of triatomines: from phylogeny to vector control. Heredity. 2012;108:190–202.DOIPubMed
- Levine R. Case 12: controlling Chagas disease in the southern cone of South America. In: Center for global development, editor. Case studies in global health. Millions saved case studies. Burlington (MA): Jones & Bartlett Learning; 2007. p. 95–102.
- Porcasi X, Catalá S, Hrellac H, Scavuzzo M, Gorla D. Infestation of rural houses by Triatoma infestans (Hemiptera: Reduviidae) in southern area of Gran Chaco in Argentina. J Med Entomol. 2006;43:1060–7. DOIPubMed
- Gurevitz JM, Gaspe MS, Enriquez GF, Provecho YM, Kitron U, Gürtler RE. Intensified surveillance and insecticide-based control of the Chagas disease vector Triatoma infestans in the Argentinean Chaco. PLoS Negl Trop Dis. 2013;7:e2158. DOIPubMed
- Levy MZ, Bowman NM, Kawai V, Waller LA, Cornejo del Carpio JG, Benzaquen EC, Periurban Trypanosoma cruzi–infected Triatoma infestans, Arequipa, Peru. Emerg Infect Dis. 2006;12:1345–52 . DOIPubMed
- Bayer AM, Hunter GC, Gilman RH, Cornejo del Carpio JG, Naquira C, Bern C, Chagas disease, migration and community settlement patterns in Arequipa, Peru. PLoS Negl Trop Dis. 2009;3:e567. DOIPubMed
- Oficina Técnica de Difusión INEI. IV Censo nacional agropecuario, nota de prensa. Lima, Peru: Instituto Nacional de Estadística e Informática. July 10,2012 [cited 2013 Jul 8]. http://www.inei.gob.pe/web/NotaPrensa/Attach/14584.pdf
- Lumbreras Cruz H. Epidemiology of Chagas disease during the urbanization of Miraflores de Arequipa [in Spanish]. Arch Pathol. 1952;6:191–200.
- Cecere MC, Canale DM, Gürtler RE. Effects of refuge availability on the population dynamics of Triatoma infestans in central Argentina. J Appl Ecol.2003;40:742–56. DOI
- Gürtler RE, Kitron U, Cecere MC, Segura EL, Cohen JE. Sustainable vector control and management of Chagas disease in the Gran Chaco, Argentina.Proc Natl Acad Sci U S A. 2007;104:16194–9 . DOIPubMed
- Saunders M, Small A, Dedicoat M, Roberts L. The development and validation of a risk score for household infestation by Triatoma infestans, a Bolivian vector of Chagas disease. Trans R Soc Trop Med Hyg. 2012;106:677–82. DOIPubMed
- Escobal J. The determinants of nonfarm income diversification in rural Peru. World Dev. 2001;29:497–508. DOI
- Buttenheim AM, Paz-Soldan V, Barbu C, Skovira C, Calderón JQ, Riveros LM, Is participation contagious? Evidence from a household vector control campaign in urban Peru. J Epidemiol Community Health. 2014;68:103–9. DOIPubMed
- Google Earth. Arequipa, Peru, metropolis. Mountain View (CA): Google Inc. Aug 17, 2009 [cited 2010 Apr 1].http://www.google.com/earth/index.html.
- Delgado S, Ernst KC, Pumahuanca ML, Yool SR, Comrie AC, Sterling CR, A country bug in the city: urban infestation by the Chagas disease vectorTriatoma infestans in Arequipa, Peru. Int J Health Geogr. 2013;12:48 and. DOIPubMed
- Palomino M, Villaseca P, Cárdenas F, Ancca J, Pinto M. Efficiency and residuality of two insecticide pyrethroids against Triatoma infestans in three types of housing: field evaluation in Arequipa, Peru [in Spanish]. Perú Revista Peruana de Medicina Experimental y Salud Publica. 2008;25:9–16.
- Bates D, Maechler M, Bolker B. lme4: linear mixed-effects models using S4 classes, 2013. R package version 0.999999–2 [cited 2014 Jul 25].http://CRAN.R-project.org/package=lme4.
- Levy MZ, Barbu CM, Castillo-Neyra R, Quispe-Machaca VR, Ancca-Juarez J, Escalante-Mejia P, Urbanization, land tenure security and vector-borne Chagas disease. Proc Biol Sci. 2014;281:20141003. DOIPubMed
- Hong A, Barbu C, Small D, Levy M. Mapping the spatial distribution of a disease transmitting insect in the presence of surveillance error and missing data. J R Stat Soc [Ser A]. 2014 [cited 2014 Sep 22]. http://onlinelibrary.wiley.com/enhanced/doi/10.1111/rssa.12077/
- Nagelkerke NJ. A note on a general definition of the coefficient of determination. Biometrika. 1991;78:691–2. DOI
- R Core Team. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing, 2014 [cited 2014 Jul 25].http://www.R-project.org.
- Centro de Investigaciones de Plagas e Insecticidas/ Centro Institucional de Investigaciones Cientificas y Técnicas de las Fuerzas Armadas/Consejo Nacional de Investigaciones Científicas y Técnicas (CIPEIN/CITEFA/CONICET). Protocolo de evaluación de efecto insecticida en Triatoma infestans. Buenos Aires, Argentina: CIPEIN/WHO/TDR, 2005 [cited 2013 Jul 15]. http://www.anmat.gov.ar/webanmat/Protocolo_Traitoma.asp.
- Barbu CM, Hong A, Manne JM, Small DS, Quintanilla Calderón JE, Sethuraman K, The effects of city streets on an urban disease vector. PLOS Comput Biol. 2013;9:e1002801. DOIPubMed
- Gürtler RE, Petersen RM, Cecere MC, Schweigmann NJ, Chuit R, Gualtieri JM, Chagas disease in north-west Argentina: risk of domestic reinfestation by Triatoma infestans after a single community-wide application of deltamethrin. Trans R Soc Trop Med Hyg. 1994;88:27–30. DOIPubMed
- Gürtler RE, Cecere M, Canale D, Castañera M, Chuit R, Cohen J. Monitoring house reinfestation by vectors of Chagas disease: a comparative trial of detection methods during a four-year follow-up. Acta Trop. 1999;72:213–34. DOIPubMed
- Cecere MC, Vazquez-Prokopec GM, Gürtler RE, Kitron U. Spatio-temporal analysis of reinfestation by Triatoma infestans (Hemiptera: Reduviidae) following insecticide spraying in a rural community in northwestern Argentina. Am J Trop Med Hyg. 2004;71:803–10 .PubMed
- Pérez de Rosas AR, Segura EL, García BA. Microsatellite analysis of genetic structure in natural Triatoma infestans (Hemiptera: Reduviidae) populations from Argentina: its implication in assessing the effectiveness of Chagas’ disease vector control programmes. Mol Ecol.2007;16:1401–12. DOIPubMed
- Gaspe MS, Gurevitz JM, Gürtler RE, Dujardin J-P. Origins of house reinfestation with Triatoma infestans after insecticide spraying in the Argentine Chaco using wing geometric morphometry. Infect Genet Evol. 2013;17:93–100. DOIPubMed
- Levy MZ, Quíspe-Machaca VR, Ylla-Velasquez JL, Waller LA, Richards JM, Rath B, Impregnated netting slows infestation by Triatoma infestans. Am J Trop Med Hyg. 2008;79:528–34 .PubMed
- Picollo MI, Vassena C, Orihuela PS, Barrios S, Zaidemberg M, Zerba E. High resistance to pyrethroid insecticides associated with ineffective field treatments in Triatoma infestans (Hemiptera: Reduviidae) from northern Argentina. J Med Entomol. 2005;42:637–42 . DOIPubMed
- Toloza AC, Germano M, Cueto GM, Vassena C, Zerba E, Picollo MI. Differential patterns of insecticide resistance in eggs and first instars of Triatoma infestans (Hemiptera: Reduviidae) from Argentina and Bolivia. J Med Entomol. 2008;45:421–6 . DOIPubMed
- Germano MD, Acevedo GR, Cueto GA, Toloza A, Vassena C, Picollo M. New findings of insecticide resistance in Triatoma infestans (Heteroptera: Reduviidae) from the Gran Chaco. J Med Entomol. 2010;47:1077–81. DOIPubMed
- Espinoza N, Borrás R, Abad-Franch F. Chagas disease vector control in a hyperendemic setting: the first 11 years of intervention in Cochabamba, Bolivia. PLoS Negl Trop Dis. 2014;8:e2782. DOIPubMed
- Adelman ZN, Kilcullen KA, Koganemaru R, Anderson MAE, Anderson TD, Miller DM. Deep sequencing of pyrethroid-resistant bed bugs reveals multiple mechanisms of resistance within a single population. PLoS ONE. 2011;6:e26228. DOIPubMed
- Levy MZ, Kawai V, Bowman NM, Waller LA, Cabrera L, Pinedo-Cancino VV, Targeted screening strategies to detect Trypanosoma cruzi infection in children. PLoS Negl Trop Dis. 2007;1:e103. DOIPubMed
- Noireau F. Wild Triatoma infestans, a potential threat that needs to be monitored. Mem Inst Oswaldo Cruz. 2009;104:60–4. DOIPubMed
- Ceballos LA, Piccinali RV, Marcet PL, Vazquez-Prokopec GM, Cardinal MV, Schachter-Broide J, Hidden sylvatic foci of the main vector of Chagas disease Triatoma infestans: threats to the vector elimination campaign? PLoS Negl Trop Dis. 2011;5:e1365 . DOIPubMed
Figures
Tables
Suggested citation for this article: Barbu CM, Buttenheim AM, Hancco Pumahuanca ML, Quintanilla Calderón JE, Salazar R, Carrión M, et al. Residual infestation and recolonization during urban Triatoma infestans bug control campaign, Peru. Emerg Infect Dis [Internet]. 2012 Dec [date cited].http://dx.doi.org/10.3201/eid2012.131820
1A Spanish version of this article is available online (http://www.spatcontrol.net/articles/Barbu2014/traduccionEspanol.pdf).
No hay comentarios:
Publicar un comentario