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

Abstract

Background 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. Methods 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. Results 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. Conclusions 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. Graphical abstract

Urban vectors of Chagas disease in the American continent: A systematic review of epidemiological surveys

“…Numerous studies approach the problem of triatomine infestation and its infection by T. cruzi in peri or suburban areas [75][76][77]. However, the urban area concept is controversial since there are no unified criteria for its characterization.…”

Towards environmental detection of Chagas disease vectors and pathogen

“…In Casanare (eastern Colombia), traditional methods are still used for entomological surveillance of R. prolixus and T. cruzi . Together these observations highlight the potential for this technique to accurately identify foci of residual triatomine infestation, which are important sources of operational failure of current Chagas disease vector control programmes 59 , 60 . In terms of implementation, the COVID-19 pandemic increased the molecular diagnostic capabilities of several laboratories nationwide, including the Casanare department (Secretaria Departamental de Salud y Unitropico).…”

New Cell Lines Derived from Laboratory Colony Triatoma infestans and Rhodnius prolixus, Vectors of Trypanosoma cruzi, Do Not Harbour Triatoma Virus

“…The environmental costs of insecticides and the increase in reports of insecticide resistance among triatomine bug populations across South America [ 2 , 49 , 50 ] underline the need for new approaches to vector control. Bio-control, exploiting natural pathogens of triatomines such as TrV as control tools, is an attractive approach; however, the experience with the fungal pathogen Metarhizium anisopliae , which took longer to kill bugs infected with T. cruzi than uninfected bugs [ 51 ] indicates the need for caution.…”