Domestic (re)infestation risk with the main vector Triatoma infestans increases with surrounding green vegetation and social vulnerability in the Argentine Chaco.

BACKGROUND: Chagas disease, caused by Trypanosoma cruzi, is still a public health problem in Latin America and in the Southern Cone countries, where Triatoma infestans is the main vector. We evaluated the relationships among the density of green vegetation around rural houses, sociodemographic characteristics, and domestic (re)infestation with T. infestans while accounting for their spatial dependence in the municipality of Pampa del Indio between 2007 and 2016. METHODS: The study comprised sociodemographic and ecological variables from 734 rural houses with no missing data. Green vegetation density surrounding houses was estimated by the normalized difference vegetation index (NDVI). We used a hierarchical Bayesian logistic regression composed of fixed effects and spatial random effects to estimate domestic infestation risk and quantile regressions to evaluate the association between surrounding NDVI and selected sociodemographic variables. RESULTS: Qom ethnicity and the number of poultry were negatively associated with surrounding NDVI, whereas overcrowding was positively associated with surrounding NDVI. Hierarchical Bayesian models identified that domestic infestation was positively associated with surrounding NDVI, suitable walls for triatomines, and overcrowding over both intervention periods. Preintervention domestic infestation also was positively associated with Qom ethnicity. Models with spatial random effects performed better than models without spatial effects. The former identified geographic areas with a domestic infestation risk not accounted for by fixed-effect variables. CONCLUSIONS: Domestic infestation with T. infestans was associated with the density of green vegetation surrounding rural houses and social vulnerability over a decade of sustained vector control interventions. High density of green vegetation surrounding rural houses was associated with households with more vulnerable social conditions. Evaluation of domestic infestation risk should simultaneously consider social, landscape and spatial effects to control for their mutual dependency. Hierarchical Bayesian models provided a proficient methodology to identify areas for targeted triatomine and disease surveillance and control.

Human Trypanosoma cruzi infection in the Argentinean Chaco: risk factors and identification of households with infected children for treatment.

BACKGROUND: Chagas disease is a neglected tropical disease (NTD). Cost-effective strategies for large-scale implementation of diagnosis and etiological treatment are urgently needed to comply with NTD control goals. We determined the seroprevalence of Trypanosoma cruzi infection and associated risk factors in a well-defined rural population of Pampa del Indio municipality including creole and indigenous (Qom) households and developed two indices to identify houses harboring infected children. METHODS: We serodiagnosed and administered a questionnaire to 1337 residents (48.2% of the listed population) in two sections of the municipality (named Areas II and IV) 6-9 years after deploying sustained vector control interventions. Multiple logistic regression models were used to evaluate the relationship between human infection and a priori selected predictors. Two risk indices were constructed based on environmental and serostatus variables, and we used spatial analysis to test whether households harboring T. cruzi-seropositive children were randomly distributed. RESULTS: The global seroprevalence of T. cruzi infection was 24.8%. Human infection was positively and significantly associated with exposure time to triatomines, the household number of seropositive co-inhabitants, maternal seropositivity for T. cruzi, recent residence at the current house and the presence of suitable walls for triatomine colonization in the domicile. The pre-intervention mean annual force of infection (FOI) was 1.23 per 100 person-years. Creoles from Area IV exhibited the highest seroprevalence and FOI; Qom people from both areas displayed intermediate ones and creoles from Area II the lowest. Three hotspots of infected children were spatially associated with hotspots of triatomine abundance at baseline and persistent house infestation. No child born after vector control interventions was T. cruzi seropositive except for one putative transplacental case. Two simple risk indices (based on self-reported inhabiting an infested house and suitable walls for triatomines or maternal serostatus) identified 97.3-98.6% of the households with at least one T. cruzi-seropositive child. CONCLUSIONS: We showed strong heterogeneity in the seroprevalence of T. cruzi infection within and between ethnic groups inhabiting neighboring rural areas. Developed indices can be used for household risk stratification and to improve access of rural residents to serodiagnosis and treatment and may be easily transferred to primary healthcare personnel.

Population structure and migration in Triatoma infestans (Hemiptera: Reduviidae) from the Argentine Chaco: An integration of genetic and morphometric data.

Genetic and morphological structure of vector populations are useful to identify panmictic groups, reinfestation sources and minimal units for control interventions. Currently, no studies have integrated genetic and morphometric data in Triatoma infestans (Hemiptera: Reduviidae), one of the main vectors of Trypanosoma cruzi. We characterized the genetic and phenotypic structure of T. infestans at a small spatial scale (2-8 km), identified potential migrants and compared flight-related traits among genetic groups and between migrant and non-migrant insects in a well-defined area without insecticide spraying in the previous 12 years. We obtained microsatellite genotypes (N = 303), wing shape and size (N = 164) and body weight-to-length ratios (N = 188) in T. infestans from 11 houses in Pampa del Indio, Argentine Chaco. The uppermost level of genetic structuring partially agreed with the morphological groups, showing high degrees of substructuring. The genetic structure showed a clear spatial pattern around Route 3 and one genetic group overlapped with an area of persistent infestation and insecticide resistance. Females harboured more microsatellite alleles than males, which showed signs of isolation-by-distance. Wing shape discriminant analyses of genetic groups revealed low reclassification scores whereas wing size differed among genetic groups for both sexes. Potential migrants (8%) did not differ from non-migrants in sex, ecotope, wing shape and size. However, male migrants had lower W/L than non-migrants suggesting poorer nutritional state. Our findings may contribute to the understanding of population characteristics, dispersal dynamics and ongoing elimination efforts of T. infestans.

Extended stage duration and diminished fecundity in deltamethrin-resistant Triatoma infestans (Klug, 1834) of the Argentinean Chaco.

Pyrethroid-resistance is an emergent trait in populations of various insect species. For Triatoma infestans (Klug, 1834) (Heteroptera: Reduviidae), the major vector of Chagas disease in the southern part of South America, hotspot areas of pyrethroid-resistance have recently been found in the Chaco Province of Argentina. Resistant condition can reduce fitness of individuals in the absence of insecticide exposure, that is, fitness costs. We evaluated the existence of developmental and/or reproductive costs in T. infestans collected from two areas of pyrethroid-resistance in Chaco Province, Argentina. Three toxicological groups were defined from field-collected insects: susceptible (survival <20%), moderately resistant (survival between 20% and 80%) and highly resistant (survival >80%). Cohorts of the three toxicological groups were followed-up to study life cycle and reproductive parameters. Additionally, we parameterized matrix population growth models. First and IV nymphal stages of the resistant groups exhibited a longer stage duration than susceptible ones. The reproductive days and hatching success showed significant lower values revealing reproductive costs for the resistant groups. Matrix analysis showed lower population growth rates for the resistant groups. Our results support developmental and reproductive costs for pyrethroid-resistant individuals. This trait could be interpreted as lower population recovery ability for pyrethroid-resistant individuals compared to susceptible insects after alternative vector control actions.

Impacts of residual insecticide spraying on the abundance and habitat occupancy of Triatoma sordida and co-occurrence with Triatoma infestans: A three-year follow-up in northeastern Argentina.

Triatoma infestans, the main vector in the Gran Chaco region, may competitively displace other sympatric species such as Triatoma sordida. We conducted a three-year longitudinal study of site- and house-level infestation and abundance of triatomine bugs before and after an area-wide insecticide spraying campaign followed by sustained vector surveillance in a well-defined rural section of the Argentine Chaco encompassing 368-411 houses. Here, we tested whether insecticide applications targeting and virtually suppressing T. infestans reduced the abundance of T. sordida and modified its habitat occupancies, and whether their joint spatial distribution was random, aggregated or uniform, and varied over time. Systematic timed-manual searches of 18,031 sites yielded 2,226 T. sordida over seven postintervention surveys. Triatoma sordida failed to colonize human sleeping quarters after interventions, and its prime and secondary habitats remained virtually unmodified. Residual insecticide spraying and seasonality best described variations in the house-level abundance of T. sordida as determined using a generalized estimating equation model. Two-species foci occurred in 3.2% of sites ever positive for any species. The habitat-adjusted relative odds of catching one species was 10.8 times greater when the other species was present, with no evidence of heterogeneity among ORs, suggesting no antagonistic interactions throughout the follow-up. The spatial occurrence of both species was significantly aggregated within 300-500 m before and after interventions, and was random at broader spatial scales. The habitat occupancies of T. sordida may be used as a proxy for potential infestation with T. infestans and to guide targeted vector control actions.

Beating the odds: Sustained Chagas disease vector control in remote indigenous communities of the Argentine Chaco over a seven-year period.

BACKGROUND: Rapid reinfestation of insecticide-treated dwellings hamper the sustained elimination of Triatoma infestans, the main vector of Chagas disease in the Gran Chaco region. We conducted a seven-year longitudinal study including community-wide spraying with pyrethroid insecticides combined with periodic vector surveillance to investigate the house reinfestation process in connection with baseline pyrethroid resistance, housing quality and household mobility in a rural section of Pampa del Indio mainly inhabited by deprived indigenous people (Qom). METHODOLOGY/PRINCIPAL FINDINGS: Despite evidence of moderate pyrethroid resistance in local T. infestans populations, house infestation dropped from 31.9% at baseline to 0.7% at 10 months post-spraying (MPS), with no triatomine found at 59 and 78 MPS. Household-based surveillance corroborated the rare occurrence of T. infestans and the house invasion of other four triatomine species. The annual rates of loss of initially occupied houses and of household mobility were high (4.6-8.0%). Housing improvements did not translate into a significant reduction of mud-walled houses and refuges for triatomines because most households kept the former dwelling or built new ones with mud walls. CONCLUSIONS/SIGNIFICANCE: Our results refute the assumption that vector control actions performed in marginalized communities of the Gran Chaco are doomed to fail. The larger-than-expected impacts of the intervention program were likely associated with the combined effects of high-coverage, professional insecticide spraying followed by systematic vector surveillance-and-response, broad geographic coverage creating a buffer zone, frequent housing replacement and residential mobility. The dynamical interactions among housing quality, mobility and insecticide-based control largely affect the chances of vector elimination.

Habitat-Specific Occupancy and a Metapopulation Model of Triatoma sordida (Hemiptera: Reduviidae), a Secondary Vector of Chagas Disease, in Northeastern Argentina.

Triatoma sordida Stål (Hemiptera: Reduviidae), a secondary vector of Trypanosoma cruzi Chagas (Kinetoplastida: Trypanosomatidae), occasionally colonizes human sleeping quarters in Paraguay, Bolivia, and Brazil, whereas only sylvatic and peridomestic populations are found in Argentina. We carried out a cross-sectional survey of house infestation in a well-defined rural area of northeastern Argentina to identify the key habitats of T. sordida; describe its spatial distribution in an apparently undisturbed setting under no recent insecticide treatment and use metapopulation theory to investigate these spatially structured populations. Timed-manual searches in 2,177 georeferenced sites from 368 houses yielded T. sordida in 78 sites (house infestation prevalence, 19.9%). Most triatomines occurred in chicken nests, chicken coops, and trees where chickens roosted (prime habitats). Goat or sheep corrals and pig corrals had a lower fraction of occupied sites (occupancies) and abundance. Both occupancy and catch increased with increasing refuge availability according to multimodel inference with model averaging. The majority of suitable habitats were unoccupied despite their proximity to occupied sites. The site-specific occurrence of T. sordida and Triatoma infestans Klug (Hemiptera: Reduviidae) was positively and homogeneously associated over ecotopes, showing no evidence of interspecific interference. An incidence function metapopulation model (including intersite distances and vector carrying capacity) predicted a fivefold greater occupancy relative to the observed pattern, suggesting the latter represented a transient state. T. sordida failed to colonize human sleeping quarters, thrived in peridomestic habitats occupied by chickens, and had a limited occupancy likely related to a poor colonizing ability and the relative instability of its prime habitats.

House Reinfestation With Triatoma infestans (Hemiptera: Reduviidae) After Community-Wide Spraying With Insecticides in the Argentine Chaco: A Multifactorial Process.

We investigated the dynamics and underlying causes of house (re)infestation with Triatoma infestans (Klug 1834) after a community-wide residual spraying with pyrethroids in a well-defined rural section of Pampa del Indio municipality (northeastern Argentina) over a 4-yr period. House infestation was assessed by timed manual searches, during insecticide applications, and by opportunistic householders' bug collections. All reinfested houses were selectively re-sprayed with insecticides. The resident population comprised Qom (66.6%) and Creole (33.4%) households, whose sociodemographic profiles differed substantially. The prevalence of house infestation dropped, less than expected, from 20.5% at baseline to 5.0% at 14 months postspraying (MPS), and then fluctuated between 0.8 and 4.2% over 21-51 MPS. Postspraying house infestation was positively and highly significantly associated with prespraying infestation. Most of the foci detected over 14-21 MPS were considered persistent (residual), some of which were moderately resistant to pyrethroids and were suppressed with malathion. Infestation patterns over 27-51 MPS suggested bug invasion from internal or external foci, but the sources of most findings were unaccounted for. Local spatial analysis identified two hotspots of postspraying house infestation. Using multimodel inference with model averaging, we corroborated that baseline domestic infestation was closely related to refuge availability, housing quality, and occurrence of peridomestic infestation. The diminished effectiveness of single pyrethroid treatments, partly attributable to moderate resistance compounded with rather insensitive vector detection methods and poor housing conditions, contributed to vector persistence. Improved control strategies combined with broad social participation are needed for the sustainable elimination of vector-borne human Chagas disease from the Gran Chaco.

The peri-urban interface and house infestation with Triatoma infestans in the Argentine Chaco: an underreported process?

Peri-urban infestations with triatomine bugs, their sources and their dynamics have rarely been investigated. Here, we corroborated the reported occurrence of Triatoma infestans in a peri-urban area and in neighbouring rural houses in Pampa del Indio, in the Argentine Chaco, and identified its putative sources using spatial analysis and demographic questionnaires. Peri-urban householders reported that 10% of their premises had triatomines, whereas T. infestans was collected by timed manual searches or community-based surveillance in only nine (3%) houses. Trypanosoma cruzi-infected T. infestans and Triatoma sordida were collected indoors only in peri-urban houses and were infected with TcV and TcI, respectively. The triatomines fed on chickens, cats and humans. Peri-urban infestations were most frequent in a squatter settlement and particularly within the recently built mud houses of rural immigrants, with large-sized households, more dogs and cats and more crowding. Several of the observed infestations were most likely associated with passive bug transport from other sources and with active bug dispersal from neighbouring foci. Thus, the households in the squatter settlement were at a greater risk of bug invasion and colonisation. In sum, the incipient process of domestic colonisation and transmission, along with persistent rural-to-urban migratory flows and unplanned urbanisation, indicate the need for active vector surveillance and control actions at the peri-urban interface of the Gran Chaco.

The peri-urban interface and house infestation with Triatoma infestans in the Argentine Chaco: an underreported process?

Peri-urban infestations with triatomine bugs, their sources and their dynamics have rarely been investigated. Here, we corroborated the reported occurrence of Triatoma infestans in a peri-urban area and in neighbouring rural houses in Pampa del Indio, in the Argentine Chaco, and identified its putative sources using spatial analysis and demographic questionnaires. Peri-urban householders reported that 10% of their premises had triatomines, whereas T. infestans was collected by timed manual searches or community-based surveillance in only nine (3%) houses. Trypanosoma cruzi-infected T. infestans and Triatoma sordida were collected indoors only in peri-urban houses and were infected with TcV and TcI, respectively. The triatomines fed on chickens, cats and humans. Peri-urban infestations were most frequent in a squatter settlement and particularly within the recently built mud houses of rural immigrants, with large-sized households, more dogs and cats and more crowding. Several of the observed infestations were most likely associated with passive bug transport from other sources and with active bug dispersal from neighbouring foci. Thus, the households in the squatter settlement were at a greater risk of bug invasion and colonisation. In sum, the incipient process of domestic colonisation and transmission, along with persistent rural-to-urban migratory flows and unplanned urbanisation, indicate the need for active vector surveillance and control actions at the peri-urban interface of the Gran Chaco.

Origins of house reinfestation with Triatoma infestans after insecticide spraying in the Argentine Chaco using wing geometric morphometry.

Identifying the origins of insect vectors collected after community-wide residual insecticide applications is a relevant challenge in the Gran Chaco region where the main vector of Chagas disease Triatoma infestans usually reinfests human dwellings. Wing geometric morphometry was used to compare the right wings of 63 males and 54 females collected at 4 months post-spraying (MPS) with those from 165 males and 111 females collected before full-coverage spraying with pyrethroids in a well-defined rural area in Northeastern Argentina. Male and female wing centroid size resulted significantly larger at 4MPS than before interventions, but no significant changes in shape were detected. Metric disparity (variance of shape) varied significantly in males but not in females. Using shape variables, a relatively large fraction of post-spraying males (70%) and females (54%) could not be differentiated from those collected at the same source house or at the nearest infested house before interventions. Bugs collected at 4 and 8MPS in a persistently infested house were mainly assigned to the source house. These results support the hypothesis of persistent bug populations that survived the insecticide application at local spatial scales, and are consistent with the occurrence of vector control failures most likely related to moderate pyrethroid resistance. Wing geometric morphometry is a useful tool for identifying sources of reinfestation, but it is limited by the spatial structure found in the reference populations. Combined with field and genetic data, this approach may contribute to the understanding of the reinfestation process and improvement of vector control strategies.