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.

The Pampa del Indio project: sustainable vector control and long-term declines in the prevalence and abundance of Triatoma infestans infected with Trypanosoma cruzi in the Argentine Chaco.

BACKGROUND: The Gran Chaco region is a major hotspot of Chagas disease. We implemented a 9-year program aimed at suppressing house infestation with Triatoma infestans and stopping vector-borne transmission to creole and indigenous (Qom) residents across Pampa del Indio municipality (Argentine Chaco). The aim of the present study was to assess the intervention effects on parasite-based transmission indices and the spatial distribution of the parasite, and test whether house-level variations in triatomine infection with Trypanosoma cruzi declined postintervention and were influenced by household ethnicity, persistent infestation linked to pyrethroid resistance and other determinants of bug infection. METHODS: This longitudinal study assessed house infestation and bug infection with T. cruzi before and after spraying houses with pyrethroids and implemented systematic surveillance-and-response measures across four operational areas over the period 2007-2016. Live triatomines were individually examined for infection by optical microscopy or kinetoplast DNA (kDNA)-PCR and declared to be infected with T. cruzi when assessed positive by either method. RESULTS: The prevalence of infection with T. cruzi was 19.4% among 6397 T. infestans examined. Infection ranged widely among the study areas (12.5-26.0%), household ethnicity (15.3-26.9%), bug ecotopes (1.8-27.2%) and developmental stages (5.9-27.6%), and decreased from 24.1% (baseline) to 0.9% (endpoint). Using random-intercept multiple logistic regression, the relative odds of bug infection strongly decreased as the intervention period progressed, and increased with baseline domestic infestation and bug stage and in Qom households. The abundance of infected bugs and the proportion of houses with ≥ 1 infected bug remained depressed postintervention and were more informative of area-wide risk status than the prevalence of bug infection. Global spatial analysis revealed sharp changes in the aggregation of bug infection after the attack phase. Baseline domestic infestation and baseline bug infection strongly predicted the future occurrence of bug infection, as did persistent domestic infestation in the area with multiple pyrethroid-resistant foci. Only 19% of houses had a baseline domestic infestation and 56% had ever had ≥ 1 infected bug. CONCLUSIONS: Persistent bug infection postintervention was closely associated with persistent foci generated by pyrethroid resistance. Postintervention parasite-based indices closely agreed with human serosurveys at the study endpoint, suggesting transmission blockage. The program identified households and population subgroups for targeted interventions and opened new opportunities for risk prioritization and sustainable vector control and disease prevention.

The Pampa del Indio project: District-wide quasi-elimination of Triatoma infestans after a 9-year intervention program in the Argentine Chaco.

BACKGROUND: The elimination of Triatoma infestans, the main domestic vector of Trypanosoma cruzi, is lagging behind expectations in the Gran Chaco region. We implemented an insecticide-based intervention program and assessed its long-term effects on house infestation and bug abundance in a resource-constrained municipality (Pampa del Indio, northeastern Argentina) inhabited by creole and the Qom indigenous people (2007-2016). Key questions were whether district-wide data integration revealed patterns concealed at lower spatial levels; to what extent preintervention infestation and pyrethroid resistance challenged the effectiveness of insecticide-based control efforts, and how much control effort was needed to meet defined targets. METHODS: Supervised vector control teams i) georeferenced every housing unit at baseline (1,546); ii) evaluated house infestation using timed-manual searches with a dislodging aerosol across four rural areas designated for district-wide scaling up; iii) sprayed with pyrethroid insecticide 92.7% of all houses; iv) periodically monitored infestation and promoted householder-based surveillance, and v) selectively sprayed the infested houses, totaling 1,823 insecticide treatments throughout the program. RESULTS: Baseline house infestation (mean, 26.8%; range, 14.4-41.4%) and bug abundance plummeted over the first year postintervention (YPI). Timed searches at baseline detected 61.4-88.0% of apparent infestations revealed by any of the methods used. Housing dynamics varied widely among areas and between Qom and creole households. Preintervention triatomine abundance and the cumulative frequency of insecticide treatments were spatially aggregated in three large clusters overlapping with pyrethroid resistance, which ranged from susceptible to high. Persistent foci were suppressed with malathion. Aggregation occurred mainly at house compound or village levels. Preintervention domestic infestation and abundance were much greater in Qom than in creole households, whereas the reverse was recorded in peridomestic habitats. House infestation, rare (1.9-3.7%) over 2-6 YPI, averaged 0.66% (95% confidence interval, 0.28-1.29%) at endpoint. CONCLUSIONS: Upscale integration revealed multiple coupled heterogeneities (spatial, sociodemographic and biological) that reflect large inequalities, hamper control efforts, and provide opportunities for targeted, sustainable disease control. High-coverage, professional insecticide spraying combined with systematic surveillance-and-response were essential ingredients to achieve the quasi-elimination of T. infestans within 5 YPI and concomitant transmission blockage despite various structural threats and constraints.

Evaluation of Mansonia spp. Infestation on Aquatic Plants in Lentic and Lotic Environments of the Madeira River Basin in Porto Velho, Rondônia, Brazil.

The females of Mansonia are voraciously hematophagous. The spiracular apparatus of the immature, larval, and pupal forms is adapted to perforate submerged aquatic vegetation, from whose aeriferous aerenchyma they obtain the oxygen necessary for breathing. The proliferation of aquatic plants, in some cases linked to anthropic modifications that reduce water flow and/or increase organic matter content, may therefore contribute to the spread of these mosquitoes. This study aims to assess the presence of immature individuals of Mansonia in different aquatic plants of the Madeira River basin in 10 lentic and lotic environments and correlate their population density with abiotic factors such as water pH, dissolved O2, conductivity, and temperature. The sampling lasted from February 2016 to June 2018, a 29-month period during which 31,287 specimens belonging to the genus Mansonia were captured. Of the 12 species of macrophytes inspected, Eichhornia crassipes made up 70.1% of the samples. Lentic environments accounted for 58.9% of the samples and lotic environments for 41.1%. Immature individuals were most commonly found on Eichhornia crassipes, with this plant accounting for an average of 96.2% of all individuals, with a percentage ranging between 58.2% and 77.1% in different breeding areas. Only at the Foz do Igarapé Jirau site was a different distribution observed, with the number of aquatic plants more nearly equal: 83.3% of the larvae were found in Eichhornia crassipes, 9.2% in Ceratopteris pteridoides, 3.6% in E. azurea, 2.0% in Salvinia sp., and 1.9% in Pistia sp. The greatest richness was found in Iguapé do Raul. Concerning the larval/plant relationship, although less frequent, E. azurea had a higher larval density of Mansonia spp. It is important to emphasize that this finding may indicate a possible selection for this plant. Egg deposition by Mansonia spp. was more abundant in sample areas with Eichhornia crassipes and Pistia sp. The number of specimens collected was positively correlated with temperature, pH, and conductivity. These correlations showed a marked increase in the rainy season. Therefore, we were able to establish preliminary parameters of how environmental changes influence the ecology of this important genus of mosquitoes, the species of which are critical disease vectors.

Urbanisation, risk stratification and house infestation with a major vector of Chagas disease in an endemic municipality of the Argentine Chaco.

BACKGROUND: The occurrence of the major vectors of Chagas disease has historically been linked to poor rural housing, but urban or peri-urban infestations are increasingly being reported. We evaluated a simple risk index to detect houses infested with Triatoma infestans and tested whether house infestation and vector abundance increased across the urban-to-rural gradient in Avia Terai, an endemic municipality of the Argentine Chaco; whether the association between infestation and selected ecological determinants varied across the gradient; and whether urban and peri-urban infestations were associated with population settlement history. METHODS: We conducted a screening survey of house infestation in 2296 urban, peri-urban and rural dwellings to identify high-risk houses based on a simple index, and then searched for triatomines in all high-risk houses and in a systematic sample of low-risk houses. RESULTS: The risk index had maximum sensitivity and negative predictive value, and low specificity. The combined number of infested houses in peri-urban and urban areas equalled that in rural areas. House infestation prevalence was 4.5%, 22.7% and 42.4% across the gradient, and paralleled the increasing trend in the frequency of domestic animals and peridomestic structures. Multiple logistic regression analysis showed that house infestation was positively and significantly associated with the availability of poultry and bug refuges in walls, and was negatively associated with domestic insecticide use. Several pieces of evidence, including absence of spatial aggregation of house infestation, support that T. infestans has been a long-established occupant of urban, peri-urban and rural settings in Avia Terai. CONCLUSIONS: An integrated vector management strategy targeting chicken coops and good husbandry practices may provide more cost-effective returns to insecticide-based vector elimination efforts.

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.

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 / Impactos da pulverização residual de inseticidas na abundância e ocupação do habitat de Triatoma sordida e co-ocorrência com Triatoma infestans: um acompanhamento de três anos no nordeste da 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 368­411 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 300­500 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.

Occurrence of domestic and intrusive triatomines (Hemiptera: Reduviidae) in sylvatic habitats of the temperate Monte Desert ecoregion of Argentina.

The eco-epidemiology of Triatominae and Trypanosoma cruzi transmission has been little studied in the Argentinean Monte ecoregion. Herein, we provide a comprehensive description of domestic and intrusive triatomines to evaluate the risk of reinfestation of rural dwellings. Triatoma infestans, T. patagonica, T. garciabesi and T. eratyrusiformis were collected by active searches or light traps. None were infected with T. cruzi. One T. infestans male was collected at 1.3 km from the nearest infested house. The finding of intrusive and domestic triatomines in sylvatic foci emphasizes the need of implementing an effective vector surveillance system.

Community-based surveillance and control of chagas disease vectors in remote rural areas of the Argentine Chaco: A five-year follow-up.

Prevention of Chagas disease vector-borne transmission mostly relies on the residual application of pyrethroid insecticide. Persistent or recurrent house infestation after insecticide spraying remains a serious challenge in remote, resource-poor rural areas where public health services face substantial constraints. Here we use generalized estimating equations and multimodel inference to model the fine-scale, time-lagged effects of a community-based vector surveillance-and-response strategy on house infestation and abundance of Triatoma infestans in four rural communities of the Argentine Chaco over a five-year period. Householders and community leaders were trained to detect triatomines and spray with insecticides their premises if infested. House infestation and vector abundance were consistently higher in peridomestic habitats than in human habitations (domiciles). Householders supplemented with sensor boxes detected infested domiciles (67%) more frequently than timed-manual searches (49%). Of all houses ever found to be infested by timed-manual searches, 76% were sprayed within six months upon detection. Domestic triatomine abundance was significantly related to house-level insecticide spraying during the previous year (inversely) and current peridomestic abundance (positively). Peridomestic triatomine abundance significantly increased with current domestic bug abundance and maximum peridomestic abundance during the previous year, and was unaffected by insecticide spraying. Our study provides new empirical evidence of the interconnection and flow between domestic and peridomestic populations of T. infestans under recurrent insecticide treatments, and supports targeting both habitats with appropriate tactics for longer-lasting, improved vector control. Community-directed efforts succeeded in controlling domestic infestations and interrupting domestic transmission, whereas persistent peridomestic infestations demand sustained control efforts to address domestic reinvasions.

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.