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The resilience of Triatoma dimidiata: An analysis of reinfestation in the Nicaraguan Chagas disease vector control program (2010-2016).

ABSTRACT: BACKGROUND:The control of Triatoma dimidiata, a major vector of Chagas disease, was believed to eliminate Trypanosoma cruzi transmission in Central America. This vector was known for its ability to repeatedly reinfest human dwellings even after initial insecticide spraying. Current vector control programs assume that community-based surveillance can maintain low levels of infestation over many years, despite a lack of evidence in the literature to corroborate this assumption. This study aims to evaluate long-term reinfestation risk in the Nicaraguan vector control program from 2010 to 2016. METHODS:We collected data from a cohort of 395 houses in Pueblo Nuevo, Nicaragua. Primary data were collected through a field survey to assess post-intervention levels of T. dimidiata house infestation in 2016, two years after the large-scale insecticide spraying. We obtained secondary data from the records about past infestation levels and control activities between 2010 and 2015. Multilevel mixed-effects logistic regression analyses were used to identify factors associated with post-intervention house infestation. RESULTS:The control program effectively reduced the infestation level from 2010 to 2014. Community-based surveillance was introduced in 2013; however, post-intervention infestation in 2016 had nearly reached pre-intervention levels in rural villages. Post-intervention house infestation was positively associated with poor wall construction, roofing tiles piled in the peri-domestic areas or the presence of dogs. Interestingly, the odds of post-intervention house infestation were one-fifth less when villagers sprayed their own houses regularly. Past infestation levels and the intensity of government-led insecticide spraying did not explain post-intervention house infestation. CONCLUSIONS:The vector control program failed to offer sustained reductions in T. dimidiata house infestation. This experience would suggest that community-based surveillance is an insufficient approach to suppressing T. dimidiata house infestation over many years. This study provides evidence to suggest that control policies for T. dimidiata should be reconsidered throughout Central America.

SUBMITTER: Yoshioka K

PROVIDER: S-EPMC6107243 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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The resilience of Triatoma dimidiata: An analysis of reinfestation in the Nicaraguan Chagas disease vector control program (2010-2016).

Yoshioka Kota K Yoshioka Kota K Provedor Ezequiel E Manne-Goehler Jennifer J

PloS one 20180823 8

<h4>Background</h4>The control of Triatoma dimidiata, a major vector of Chagas disease, was believed to eliminate Trypanosoma cruzi transmission in Central America. This vector was known for its ability to repeatedly reinfest human dwellings even after initial insecticide spraying. Current vector control programs assume that community-based surveillance can maintain low levels of infestation over many years, despite a lack of evidence in the literature to corroborate this assumption. This study ...[more]

PMID: 30138377

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Project description:BackgroundChagas disease is a major neglected tropical disease with deep socio-economical effects throughout Central and South America. Vector control programs have consistently reduced domestic populations of triatomine vectors, but non-domiciliated vectors still have to be controlled efficiently. Designing control strategies targeting these vectors is challenging, as it requires a quantitative description of the spatio-temporal dynamics of village infestation, which can only be gained from combinations of extensive field studies and spatial population dynamic modelling.Methodology/principal findingsA spatially explicit population dynamic model was combined with a two-year field study of T. dimidiata infestation dynamics in the village of Teya, Mexico. The parameterized model fitted and predicted accurately both intra-annual variation and the spatial gradient in vector abundance. Five different control strategies were then applied in concentric rings to mimic spatial design targeting the periphery of the village, where vectors were most abundant. Indoor insecticide spraying and insect screens reduced vector abundance by up to 80% (when applied to the whole village), and half of this effect was obtained when control was applied only to the 33% of households closest to the village periphery. Peri-domicile cleaning was able to eliminate up to 60% of the vectors, but at the periphery of the village it has a low effect, as it is ineffective against sylvatic insects. The use of lethal traps and the management of house attractiveness provided similar levels of control. However this required either house attractiveness to be null, or ? 5 lethal traps, at least as attractive as houses, to be installed in each household.Conclusion/significanceInsecticide and insect screens used in houses at the periphery of the village can contribute to reduce house infestation in more central untreated zones. However, this beneficial effect remains insufficient to allow for a unique spatially targeted strategy to offer protection to all households. Most efficiently, control should combine the use of insect screens in outer zones to reduce infestation by both sylvatic and peri-domiciliated vectors, and cleaning of peri-domicile in the centre of the village where sylvatic vectors are absent. The design of such spatially mixed strategies of control offers a promising avenue to reduce the economic cost associated with the control of non-domiciliated vectors.

Project description:Chagas disease, considered a neglected disease by the World Health Organization, is caused by the protozoan parasite Trypanosoma cruzi, and transmitted by >140 triatomine species across the Americas. In Central America, the main vector is Triatoma dimidiata, an opportunistic blood meal feeder inhabiting both domestic and sylvatic ecotopes. Given the diversity of interacting biological agents involved in the epidemiology of Chagas disease, having simultaneous information on the dynamics of the parasite, vector, the gut microbiome of the vector, and the blood meal source would facilitate identifying key biotic factors associated with the risk of T. cruzi transmission. In this study, we developed a RADseq-based analysis pipeline to study mixed-species DNA extracted from T. dimidiata abdomens. To evaluate the efficacy of the method across spatial scales, we used a nested spatial sampling design that spanned from individual villages within Guatemala to major biogeographic regions of Central America. Information from each biotic source was distinguished with bioinformatics tools and used to evaluate the prevalence of T. cruzi infection and predominant Discrete Typing Units (DTUs) in the region, the population genetic structure of T. dimidiata, gut microbial diversity, and the blood meal history. An average of 3.25 million reads per specimen were obtained, with approximately 1% assigned to the parasite, 20% to the vector, 11% to bacteria, and 4% to putative blood meals. Using a total of 6,405 T. cruzi SNPs, we detected nine infected vectors harboring two distinct DTUs: TcI and a second unidentified strain, possibly TcIV. Vector specimens were sufficiently variable for population genomic analyses, with a total of 25,710 T. dimidiata SNPs across all samples that were sufficient to detect geographic genetic structure at both local and regional scales. We observed a diverse microbiotic community, with significantly higher bacterial species richness in infected T. dimidiata abdomens than those that were not infected. Unifrac analysis suggests a common assemblage of bacteria associated with infection, which co-occurs with the typical gut microbial community derived from the local environment. We identified vertebrate blood meals from five T. dimidiata abdomens, including chicken, dog, duck and human; however, additional detection methods would be necessary to confidently identify blood meal sources from most specimens. Overall, our study shows this method is effective for simultaneously generating genetic data on vectors and their associated parasites, along with ecological information on feeding patterns and microbial interactions that may be followed up with complementary approaches such as PCR-based parasite detection, 18S eukaryotic and 16S bacterial barcoding.

Project description:Among Chagas disease triatomine vectors, the largest genus, Triatoma, includes species of high public health interest. Triatoma dimidiata, the main vector throughout Central America and up to Ecuador, presents extensive phenotypic, genotypic, and behavioral diversity in sylvatic, peridomestic and domestic habitats, and non-domiciliated populations acting as reinfestation sources. DNA sequence analyses, phylogenetic reconstruction methods, and genetic variation approaches are combined to investigate the haplotype profiling, genetic polymorphism, phylogeography, and evolutionary trends of T. dimidiata and its closest relatives within Triatoma. This is the largest interpopulational analysis performed on a triatomine species so far.Triatomines from Mexico, Guatemala, Honduras, Nicaragua, Panama, Cuba, Colombia, Ecuador, and Brazil were used. Triatoma dimidiata populations follow different evolutionary divergences in which geographical isolation appears to have had an important influence. A southern Mexican-northern Guatemalan ancestral form gave rise to two main clades. One clade remained confined to the Yucatan peninsula and northern parts of Chiapas State, Guatemala, and Honduras, with extant descendants deserving specific status. Within the second clade, extant subspecies diversity was shaped by adaptive radiation derived from Guatemalan ancestral populations. Central American populations correspond to subspecies T. d. dimidiata. A southern spread into Panama and Colombia gave the T. d. capitata forms, and a northwestern spread rising from Guatemala into Mexico gave the T. d. maculipennis forms. Triatoma hegneri appears as a subspecific insular form.The comparison with very numerous Triatoma species allows us to reach highly supported conclusions not only about T. dimidiata, but also on different, important Triatoma species groupings and their evolution. The very large intraspecific genetic variability found in T. dimidiata sensu lato has never been detected in a triatomine species before. The distinction between the five different taxa furnishes a new frame for future analyses of the different vector transmission capacities and epidemiological characteristics of Chagas disease. Results indicate that T. dimidiata will offer problems for control, although dwelling insecticide spraying might be successful against introduced populations in Ecuador.

Dataset Information

The resilience of Triatoma dimidiata: An analysis of reinfestation in the Nicaraguan Chagas disease vector control program (2010-2016).

Publications

The resilience of Triatoma dimidiata: An analysis of reinfestation in the Nicaraguan Chagas disease vector control program (2010-2016).

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