Slow recovery rates and spatial aggregation of Triatoma infestans populations in an area with high pyrethroid resistance in the Argentine Chaco.

The emergence of pyrethroid resistance has threatened the elimination of Triatoma infestans from the Gran Chaco ecoregion. We investigated the status and spatial distribution of house infestation with T. infestans and its main determinants in Castelli, a municipality of the Argentine Chaco with record levels of triatomine pyrethroid resistance, persistent infestation over 2005-2014, and limited or no control actions over 2015-2020. We conducted a 2-year longitudinal survey to assess triatomine infestation by timed manual searches in a well-defined rural section of Castelli including 14 villages and 234 inhabited houses in 2018 (baseline) and 2020, collected housing and sociodemographic data by on-site inspection and a tailored questionnaire, and synthetized these data into three indices generated by multiple correspondence analysis. The overall prevalence of house infestation in 2018 (33.8%) and 2020 (31.6%) virtually matched the historical estimates for the period 2005-2014 (33.7%) under recurrent pyrethroid sprays. While mean peridomestic infestation remained the same (26.4-26.7%) between 2018 and 2020, domestic infestation slightly decreased from 12.2 to 8.3%. Key triatomine habitats were storerooms, domiciles, kitchens, and structures occupied by chickens. Local spatial analysis showed significant aggregation of infestation and bug abundance in five villages, four of which had very high pyrethroid resistance approximately over 2010-2013, suggesting persistent infestations over space-time. House bug abundance within the hotspots consistently exceeded the estimates recorded in other villages. Multiple regression analysis revealed that the presence and relative abundance of T. infestans in domiciles were strongly and negatively associated with indices for household preventive practices (pesticide use) and housing quality. Questionnaire-derived information showed extensive use of pyrethroids associated with livestock raising and concomitant spillover treatment of dogs and (peri) domestic premises. Triatoma infestans populations in an area with high pyrethroid resistance showed slow recovery and propagation rates despite limited or marginal control actions over a 5-year period. Consistent with these patterns, independent experiments confirmed the lower fitness of pyrethroid-resistant triatomines in Castelli compared with susceptible conspecifics. Targeting hotspots and pyrethroid-resistant foci with appropriate house modification measures and judicious application of alternative insecticides with adequate toxicity profiles are needed to suppress resistant triatomine populations and prevent their eventual regional spread.

Cecere MC ，Gaspe MS ，Macchiaverna NP ，Enriquez GF ，Alvedro A ，Laiño MA ，Alvarado-Otegui JA ，Cardinal MV ，Gürtler RE ... -  《Parasites & Vectors》

Improved vector control of Triatoma infestans limited by emerging pyrethroid resistance across an urban-to-rural gradient in the Argentine Chaco.

The sustainable elimination of Triatoma infestans in the Gran Chaco region represents an enduring challenge. Following the limited effects of a routine pyrethroid insecticide spraying campaign conducted over 2011-2013 (first period) in Avia Terai, an endemic municipality with approximately 2300 houses, we implemented a rapid-impact intervention package to suppress house infestation across the urban-to-rural gradient over 2015-2019 (second period). Here, we assess their impacts and whether persisting infestations were associated with pyrethroid resistance. The 2011-2013 campaign achieved a limited detection and spray coverage across settings (< 68%), more so during the surveillance phase. Following community mobilization and school-based interventions, the 2015-2019 program assessed baseline house infestation using a stratified sampling strategy; sprayed all rural houses with suspension concentrate beta-cypermethrin, and selectively sprayed infested and adjacent houses in urban and peri-urban settings; and monitored house infestation and performed selective treatments over the follow-up. Over the first period, house infestation returned to pre-intervention levels within 3-4 years. The adjusted relative odds of house infestation between 2011-2013 and 2015-2016 differed very little (adj. OR: 1.17, 95% CI 0.91-1.51). Over the second period, infestation decreased significantly between 0 and 1 year post-spraying (YPS) (adj. OR: 0.36, 95% CI 0.28-0.46), with heterogeneous effects across the gradient. Mean bug abundance also dropped between 0 and 1 YPS and thereafter remained stable in rural and peri-urban areas. Using multiple regression models, house infestation and bug abundance at 1 YPS were 3-4 times higher if the house had been infested before treatment, or was scored as high-risk or non-participating. No low-risk house was ever infested. Persistent foci over two successive surveys increased from 30.0 to 59.3% across the gradient. Infestation was more concentrated in peridomestic rather than domestic habitats. Discriminating-dose bioassays showed incipient or moderate pyrethroid resistance in 7% of 28 triatomine populations collected over 2015-2016 and in 83% of 52 post-spraying populations. The intervention package was substantially more effective than the routine insecticide spraying campaign, though the effects were lower than predicted due to unexpected incipient or moderate pyrethroid resistance. Increased awareness and diagnosis of vector control failures in the Gran Chaco, including appropriate remedial actions, are greatly needed.

Gaspe MS ，Cardinal MV ，Fernández MDP ，Vassena CV ，Santo-Orihuela PL ，Enriquez GF ，Alvedro A ，Laiño MA ，Nattero J ，Alvarado-Otegui JA ，Macchiaverna NP ，Cecere MC ，Freilij H ，Gürtler RE ... -  《Parasites & Vectors》

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

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. 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. 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. 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.

Gürtler RE ，Gaspe MS ，Macchiaverna NP ，Enriquez GF ，Rodríguez-Planes LI ，Fernández MDP ，Provecho YM ，Cardinal MV ... -  《PLoS Neglected Tropical Diseases》

Intensified surveillance and insecticide-based control of the Chagas disease vector Triatoma infestans in the Argentinean Chaco.

The elimination of Triatoma infestans, the main Chagas disease vector in the Gran Chaco region, remains elusive. We implemented an intensified control strategy based on full-coverage pyrethroid spraying, followed by frequent vector surveillance and immediate selective insecticide treatment of detected foci in a well-defined rural area in northeastern Argentina with moderate pyrethroid resistance. We assessed long-term impacts, and identified factors and procedures affecting spray effectiveness. After initial control interventions, timed-manual searches were performed by skilled personnel in 4,053 sites of 353-411 houses inspected every 4-7 months over a 35-month period. Residual insecticide spraying was less effective than expected throughout the three-year period, mainly because of the occurrence of moderate pyrethroid resistance and the limited effectiveness of selective treatment of infested sites only. After initial interventions, peridomestic infestation prevalence always exceeded domestic infestation, and timed-manual searches consistently outperformed householders' bug detection, except in domiciles. Most of the infestations occurred in houses infested at baseline, and were restricted to four main ecotopes. Houses with an early persistent infestation were spatially aggregated up to a distance of 2.5 km. An Akaike-based multi-model inference approach showed that new site-level infestations increased substantially with the local availability of appropriate refugia for triatomine bugs, and with proximity to the nearest site found infested at one or two preceding surveys. Current vector control procedures have limited effectiveness in the Gran Chaco. Selective insecticide sprays must include all sites within the infested house compound. The suppression of T. infestans in rural areas with moderate pyrethroid resistance requires increased efforts and appropriate management actions. In addition to careful, systematic insecticide applications, housing improvement and development policies that improve material conditions of rural villagers and reduce habitat suitability for bugs will contribute substantially to sustainable vector and disease control in the Gran Chaco.

Gurevitz JM ，Gaspe MS ，Enriquez GF ，Provecho YM ，Kitron U ，Gürtler RE ... -  《PLoS Neglected Tropical Diseases》

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.

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. 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. 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. 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.

Gürtler RE ，Enriquez GF ，Gaspe MS ，Macchiaverna NP ，Del Pilar Fernández M ，Rodríguez-Planes LI ，Provecho YM ，Cardinal MV ... -  《Parasites & Vectors》