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

María Sol Gaspe,Julián Antonio Alvarado-Otegui,Mariano Alberto Laiño,María Del Pilar Fernández,Pablo Luis Santo-Orihuela,Ricardo Esteban Gürtler,Marta Victoria Cardinal,Julieta Nattero,Natalia Paula Macchiaverna,Claudia Viviana Vassena,Gustavo Fabián Enriquez,Héctor Freilij,Alejandra Alvedro,María Carla Cecere

doi:10.1186/s13071-021-04942-9

Abstract

BackgroundThe 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.MethodsThe 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.ResultsOver 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.ConclusionsThe 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

Highlights

The sustainable elimination of Triatoma infestans in the Gran Chaco region represents an endur‐ ing challenge
The prevalence of house infestation stratified for type of environment did not differ significantly between 2011–2013 and 2015–2016, the latter taken as an outcome measure of prior interventions
Residual house spraying with pyrethroid insecticide has successfully suppressed or reduced house infestations with the major triatomine species over the last 40 years, and continues to be effective under most circumstances if applied properly in the framework of a consistent disease control program [13]

Summary

Introduction

The sustainable elimination of Triatoma infestans in the Gran Chaco region represents an endur‐ ing challenge. Ecological, socio-demographic, political and economic constraints hinder vector control success in the Gran Chaco, including the lower effectiveness of pyrethroid insecticides in peridomestic structures, limited coverage of control actions, disperse rural settlements with limited access, operational and resource limitations, occurrence of sylvatic foci, among others [12, 13]. This epidemiological scenario gained more complexity over the 1990s with the emergence of pyrethroid resistance in T. infestans and associated control failures across northern Argentina and Bolivia [14,15,16,17,18]. The issue of rapid recovery of triatomine populations following insecticide spraying campaigns cuts across the major triatomine vector species, such as Triatoma dimidiata, Triatoma brasiliensis, Rhodnius ecuadoriensis and Rhodnius prolixus (e.g., [19,20,21,22,23])

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