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ABSTRACT |
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES |
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES |
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Triatoma infestans can be controlled through application of residual insecticides to households in affected areas. Since 1991, a concerted vector control campaign, known as the Southern Cone initiative, has successfully eliminated transmission of T. cruzi by T. infestans in Chile,9 Brazil,10 and Uruguay.1 However, T. infestans control efforts are challenged, even in rural areas, by the return of the vector as the residual effect of insecticide diminishes.11,12 In the city of Arequipa, where household density is very high,6 and the vector can easily walk from one house to the next, re-dispersion of the vector may be faster than in rural areas. Residual vector populations have been found in 2–3% of households within 1 year of completion of insecticide application in Arequipa (Ministry of Health, unpublished data). Additional measures may be necessary to prevent reinfestation by T. infestans after insecticide application in the urban environment and to thereby prevent the re-establishment of vector-borne T. cruzi transmission.
Insecticide-treated nets (ITNs) have been shown to be effective in malaria control13 and potentially in the control of leishmaniasis.14 ITNs kill triatomines,15,16 but no study has yet evaluated their use to prevent vector infestation and aid in the T. infestans elimination campaign. Vector infestation typically begins in peri-domestic animal enclosures,17 and in Arequipa, guinea pig enclosures are particularly susceptible.6
We performed a longitudinal field trial to measure the rate of vector infestation in sentinel enclosures housing two guinea pigs with and without protective covers made of delta-methrin-impregnated netting. We use novel statistical methods to simultaneously estimate the effect of the netting on the rate of infestation while controlling for the effect of surrounding vector populations, taking into account both the density of these populations and their distance from the sentinel enclosures.
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MATERIALS AND METHODS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES |
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Study design. The study was conducted in coordination with the vector control program of the Arequipa Ministry of Health. The use of vertebrate animals in the study was approved by the Johns Hopkins IACUC committee. In July 2006, 5 months before the initiation of vector control activities, trained entomologic collectors visited all households in the community. After receiving consent, collectors searched for triatomines with the aid of an aerosol insecticide spray containing tetramethrin (Sapolio "Mata Moscas" tet-ramethrin 0.15%), a flushing out agent for T. infestans.19 Search was limited to the peri-domestic area of households, including all external walls and animal enclosures, and aimed only to establish whether there were vectors present. Collected vectors were removed from the household, but no attempt was made to control their population during the search. Households in which live T. infestans of any stage were encountered were invited to participate in the longitudinal sentinel enclosure study.
We took advantage of the grid structure of the city blocks in Nueva Alborada and assigned each block sequentially to one of three groups, following the numbering of the blocks that was assigned geographically by the Ministry of Health. The first group received a newly constructed guinea pig enclosure over which we placed a specially made long-lasting deltamethrin-impregnated net (PermaNet 2.0, 55 mg/m2 target deltamethrin concentration, 25 holes/cm2 mesh size; Vestergaard Frandsen, Lausanne, Switzerland). The second group received an identical new enclosure without a net; this group served as the control group. The final group of blocks did not receive anything and is not included in this study. In total, nine city blocks participated in the study: four in the intervention group and five in the control group.
Newly constructed guinea pig enclosures measured 1.4 x 0.8 m. The walls were constructed of metallic wire shown previously to be refractory to T. infestans colonization,6 and the roof was of corrugated rubber. Impregnated nets measured 1.5 x 1.0 m (Figure 1
). Enclosures were placed in the yards or roofs of participating households. Care was taken to place sentinel enclosures at least 2 m from sites of vector infestation, and the area surrounding the enclosures was reexamined at the time of placement of the enclosure for signs of triatomines. We placed two guinea pigs into each enclosure along with 25 bricks, which provide a habitat for T. infestans. Bricks were stacked loosely in the form of a "U" at one end of the enclosure. We visited participating houses every 2 weeks for 4 months and carefully examined the 25 bricks, the netting if present, and the area under the new enclosures for the presence of T. infestans and T. infestans eggs. All insects encountered were removed from the enclosures, staged, and sexed (for adults) at the National University of San Agustin.
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Triatomines captured from each site were stored separately on ice packs until processing at the National University of San Agustin. Vectors were counted by site, stage, and sex (for adults). Live and moribund third-, fourth-, and fifth-instar and adult triatomines were examined for T. cruzi as described by Gurtler and others.21 Briefly, intestinal contents of the insects were extracted by applying pressure to the lower abdomen of the triatomine with forceps. Extracted material was diluted in one drop of saline solution and examined under a microscope at x400 magnification. We examined insects consecutively for each site until 1 positive insect was found, 10 negative insects had been examined, or all available insects had been examined, as described previously.6
Data analysis. The latitude and longitude of all sites of collection and sentinel enclosures were determined from GoogleEarth and entered into a Geographic Information System (ArcView 3.3; ESRI, Redlands, CA). The distances from sites of collection to sentinel enclosures were calculated in ArcView. Comparison between distances determined through GoogleEarth and ArcView and those taken by tape measure showed a median discrepancy of 1.43 m; 90% of measures were within 3.6 m. When both computer-generated and manual measures of distance were available, the manual measures were used.
We calculated the total rate of infestation of sentinel enclosures by T. infestans as the number of insects collected in the enclosure per time in which the enclosure was exposed in the household (sentinel enclosure days). We compared the infestation rates in enclosures with and without impregnated netting using the 
2 test. We also calculated the stage-specific estimated reproductive value of insects encountered in each type of enclosure. The reproductive value for each stage of insect is the product of the probability that the insect survives until adulthood and the expected number of eggs produced as an adult. We followed custom and only considered female insects. Sex was not determined for nymphs, so we divided the number of nymphs captured by 2 to calculate the reproductive value. For adult female insects, reproductive value decreases with time as an adult, which we could not measure. We therefore also halved the reproductive value of females, assuming all were at the middle of their reproductive lives on migration. All stage-specific survival values and adult fecundity were derived from life table statistics of T. infestans in the experimental colonies reported by Rabinovich.22
We used log-linear models to estimate the effect of netting on the infestation rate of vectors controlling for the density and distance of potential source populations. Because the variance of the log of infestation rates between enclosures was much greater than the mean, overdispersed Poisson log-linear models fit the data better than simple Poisson log-linear models based on the likelihood ratio test. We fit the overdispersed Poisson log-linear models following the methods described in Breslow23 and implemented in the dispmod library of the R statistical package (R 2.1, www.r-project.org).
There were multiple potential sources of triatomines around all sentinel enclosures. We assumed that the effect of these populations on the rate of infestation of sentinel enclosures to be a function of both the density of each source population (Sj), and the distance between the source population and the sentinel enclosure (dij). We used kernel density estimators to summarize the distance and population density of all vector populations surrounding sentinel enclosures. Biologically, these kernel density functions represent the sum of the products of vector density of each source population and the probability of migration from that source to the sentinel enclosure. We assumed the probability of T. infestans migration to decrease with increasing distance and modeled this decrease with different one-parameter kernel functions. We considered the exponential, Cauchy, and Gaussian kernels. We included the kernel density estimates into the over-dispersed Poisson log-linear models as a covariate. The full log-linear models take the following forms:
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We identified the best fit model across a wide range of possible parameters of the spatial kernel estimators (for the exponential, the parameter is denoted as a; for the Gaussian, the parameter is called the bandwidth and is denoted as b; the parameter for the Cauchy kernel is c) for each type of model. We compared the fit of the models using the Akaike information criterion (AIC). The model with the lowest AIC was accepted as the best fit.26
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
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). No triatomines (0% of 1,460; one-sided 97.5% confidence interval [CI], 0%, 0.25%) were infected with T. cruzi.
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The great majority of live insects collected were early-stage nymphs. Triatomine eggs, which are white or pink and fairly easy to spot, were encountered in only one enclosure, which did not have a net. The proportion of each stage of insect captured in the sentinel enclosures without netting very closely resembled the stable stage distribution of T. infestans measured in laboratory conditions (Figure 3).22 In the netted enclosures, many more adult insects than immature stages were found dead or moribund. The average expected reproductive value of insects per enclosure was 10.9 times higher in control enclosures than netted enclosures (443.6 compared with 40.5). The majority of the reproductive value across all control enclosures could be attributed to first-instar nymphs (51.7%). Adults and fifth-instar nymphs contributed only 4.83% and 2.50% of the total reproductive value, respectively (Table 1).
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). In this model, the rate of infestation in enclosures with nets was less than a quarter of that in control enclosures (P = 0.018) after adjusting for the effect of the surrounding source populations. The estimated dispersion term in the model was 1.59, confirming that the data were indeed overdispersed. Similar overdis-persed Poisson models with a Cauchy or exponential kernel density functions fit the models nearly as well (Cauchy: AIC = 36.540, parameter = 28; exponential: AIC = 36.315, decay parameter = 0.035). The choice of kernel density function did not greatly alter the estimate of the effect of the nets nor the significance level of that estimate. Plots of the AIC of the full overdispersed Poisson models over all the parameters of the Gaussian, Cauchy, and exponential kernel density functions considered were continuous and had clear minima in all three cases (Figure 4). The estimated relation between migration rate and distance are shown in Figure 5.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES |
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Using log-linear models including kernel estimates of vector density of surrounding vector populations, we estimated the relationship between vector migration rate and distance. A Gaussian function fit the data better than an exponential function, suggesting a more gradual decrease in migration rate per meter of distance over short distances, especially when source populations are within 10 m of sentinel enclosures. Our estimated function is qualitatively in line with data from light-trapping experiments, in which nymphs were observed to walk up to 42 m,27 as well as evidence from blood meal analyses that nymphs can walk even greater distances.28 We cannot compare the actual estimated rates of migration observed here to estimates from light trap studies because such studies to date have been limited to nights of high probability of vector flight. T. infestans adults have been observed to fly up to 2 km,29 but such long-range flight was probably a negligible factor in vector migration on the scale of our study. The Cauchy function, which is "long-tailed," may be a more appropriate model of the relation between vector migration and distance when long-distance migration is more important.
Surprisingly, the great majority of insects collected from sentinel enclosures were early-stage nymphs. Vazquez-Prokopec27 collected fifth-instar nymphs in light traps in northwestern Argentina and suggested that larger nymphs may play an important role in the local propagation of T. infestans within households, but no nymph below the fifth stage was collected in light traps. Our results suggest that, in terms of numbers and reproductive value, the early-stage nymphs are the most important agents of local dispersion of T. infestans. Unfed first-instar nymphs are very unlikely to be infected with T. cruzi. Thus, local propagation of vectors likely occurs before the spread of the parasite.
We observed no increased rate of infestation among adult insects compared with nymphs. The structure of the population in the control sentinel enclosures closely paralleled that of the stable stage distribution of T. infestans as measured in laboratory conditions.22 Our results suggest that migration propensity is equal across all stages in T. infestans, even though only the adults are winged. The impregnated nets were especially effective against adult insects. Presumably, the larger insects were less able to fit through or under the mesh. Adult and late-stage nymphs have higher reproductive values.22 Taking into account the difference in population structure of insects caught in the netted enclosures, we calculated that the nets decrease the reproductive value of T. in-festans > 10-fold. More data are needed on mortality of insects in enclosures with and without nets to fully estimate the effect of nets on T. infestans colonization potential and population growth in these enclosures.
The ultimate goal of the Southern Cone initiative is the elimination of T. infestans. Infestation by T. infestans typically begins in peridomestic structures,17 and decreasing the susceptibility of these structures with impregnated netting or through other interventions might aid in the elimination of the vector. More complete analysis is necessary to determine the effect that netting might have on the number of sites a residual population of triatomines would infest, a measure known as the "R0"30 of the vector in the community. A key determinate of the potential decrease in R0 is the decrease in migration from enclosures with nets. Future work is also needed to estimate the duration of the effect of ITNs against T. infestans in field conditions. Nets were damaged over the course of the study. Tougher insecticide-impregnated materials may be needed for use in the peri-domestic habitat.
Previous studies have suggested that deltamethrin-impregnated nets might prevent T. cruzi transmission to humans.15,16 Our results show that such protection would be partial, because vectors can navigate past the nets. However, in our study, most vectors that traversed the nets were early-stage nymphs, which are less likely to carry T. cruzi. Nets might thereby substantially decrease the force of infection to humans, even if they do not fully block the vector’s access to its blood meal. Bednets might be especially effective against T. infestans because bugs would face the double jeopardy of passing the net as they approach their host to feed and again as they return to their colony. Bednets might thereby decrease domestic populations of triatomines.
Our study had a number of limitations. Because of the two-phase design, we had an unequal number of netted and control enclosures. The low participation rate for the initial vector collection led to a low sample size for the longitudinal sentinel enclosure study and decreased precision in our estimates of vector migration rate over distance. We placed 25 bricks in sentinel enclosures to provide habitat to infesting insects. We cannot exclude the possibility that this habitat was incompatible to insects of certain stages, adults particularly, which may prefer other materials. We were only able to examine the sentinel enclosures biweekly; natural predators of triatomines, especially chickens and ants, probably ate many dead and moribund triatomines. We were also not able to control for the presence of vectors in neighboring communities.
There are hundreds of urban and peri-urban communities similar to Nueva Alborada in the city of Arequipa. Although T. cruzi transmission was not observed in Nueva Alborada at the time of vector control, the parasite is quite common in similar communities.6 Achieving elimination of vector-borne transmission of T. cruzi in the urban environment will not be easy and likely requires measures in addition to those shown to be successful elsewhere in rural areas covered by the Southern Cone initiative. ITNs have proven to be a low-cost and effective intervention against malaria.13 Further study is needed to establish whether they might have similar potential in the control of Chagas disease.
Received March 11, 2008. Accepted for publication June 30, 2008.
Acknowledgments: We thank the community of Nueva Alborada for participation and hospitality during this study. We especially thank Rocio Rodriguez, Amparo Toledo, and the sprayers and field collectors who worked on the study. We also thank Gregory Martin, Jeffrey Stancil, David Bentzel, Ellen Dotson, Lucy Rubio, Gena Lawrence, Linda Webb, Karina Oppe, and Fernando Malaga for assistance and support. The authors thank Torben Frandsen for fabrication and donation of the guinea pig PermaNets.
Financial support: This study received financial support from the UNICEF/UNDP/World Bank/WHO Special Program for Research and Training in Tropical Diseases (TDR Grant A50684). M.Z.L. was supported by a Howard Hughes Pre-doctoral fellowship. V.Q.M., J.L.Y.V., K.B., and B.R. were supported by a training grant from the Fogarty Center of the NIH. Additional support came from National Institutes of Health Grants U19-AI-33061 and RO1-AI047498.
* Address correspondence to Michael Z. Levy, Fogarty International Center, 31 Center Drive, MSC2220, Bethesda, MD 20892-2220. E-mail: levymz{at}yahoo.com 
Authors’ addresses: Michael Levy and F. Ellis McKenzie, Fogarty International Center, National Institutes of Health, MSC2220, Bethesda, MD 20892-2220. Victor R. Quíspe-Machaca, Jose L. Ylla-Velasquez, Jean M. Richards, Bruno Rath, and Katty Borrini-Mayori, Asociacio ' n Bene 'fica Proyectos en Informa 'tica, Salud, Me-dicina y Agricultura (AB PRISMA), 251 Carlos Gonzales, Maranga, San Miguel, Lima 32, Peru. Lance Waller, Department of Biostatistics, 1518 Clifton Rd., NE, Rollins School of Public Health, Emory University, Atlanta, GA 30322. Juan Cornejo del Carpio, Dirección Regional del Ministerio de Salud, Av. Daniel Alcides Carrión 505, Arequipa, Peru. Eleazar Cordova-Benzaquen, Universidad Nacional San Agustín, Facultad de Medicina, Arequipa, Peru. Robert A. Wirtz and Caryn Bern, Division of Parasitic Diseases, Centers for Disease Control and Prevention, Mailstop F-22, Atlanta, GA 30341. James H. Maguire, Division of Infectious Disease, Brigham and Women’s Hospital, PBBA-475 Francis Street, Boston, MA 02115. Robert H. Gil-man, Department of International Health, Bloomberg School of Public Health, 615 N. Wolfe St. rm W5515, Baltimore, MD 21205.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES |
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This article has been cited by other articles:
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  M. Z. Levy, F. S. Malaga Chavez, J. G. Cornejo del Carpio, D. A. Vilhena, F. E. McKenzie, and J. B. Plotkin Rational spatio-temporal strategies for controlling a Chagas disease vector in urban environments J R Soc Interface, January 8, 2010; (2010) rsif.2009.0479v1. [Abstract] [Full Text] [PDF]
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