Longitudinal field evaluation of outdoor Anopheles and non-Anopheles host-seeking in response to a volatile pyrethroid spatial emanator (SE) product among forest-dwelling indigenous residents of Sumatra, Indonesia

Abstract

Background: Interventions against adult Anopheles mosquitoes responsible for malaria transmission have traditionally been aimed at indoor spaces and biting behaviours. However, no globally recommended intervention exists which directly interrupt or target outdoor biting behaviours. A volatile pyrethroid spatial emanator (SE) containing transfluthrin aims to address this gap in protection via a simple-to-use, readily deployable device to provide multiple weeks of protection. The device was tested in open-walled households of the forest-dwelling Orang Rimba people in Sumatra, Indonesia, over the course of sixteen weekly entomological visits.

Methods: Double-net traps were used for all mosquito collections. Collections occurred near Bukit Duabelas National Park in central Sumatra, an area characterized by secondary forests undergoing widespread conversion to palm and rubber plantations. Four collections occurred per collection night within ten geographically separated small familial groups for a total of 40 trap-nights per week. Groups were assigned the SE or a control device after a seven-week baseline trapping period. Devices were replaced every four weeks. Results were compared using generalized linear models, incorporating treatment, weather, and landscape parameters as fixed effects, with date and location included as random effects.

Results: Anopheles mosquitoes were captured on 63.2% of all collection nights. Overall nightly Anopheles host-seeking activity was lower in the presence of SE devices (RR: 0.29 [0.19-0.45], p < 0.001). Non-Anopheles mosquitoes experienced a smaller nightly decline in behaviour (RR: 0.78 [0.64-0.93], p = 0.007). The age of the device (1 month) did not impact modeled efficacy. Anopheles host-seeking activity was also positively correlated with humidity, topographic wetness, and local human structure density.

Conclusions: The SE device evaluated in this field trial was effective in reducing outdoor human exposure to Anopheles and non-Anopheles mosquito host-seeking activity. The effect was not found to depend upon the age of the device, suggesting that the protection was persistent over the 4-week replacement period during this study. There was an association between hour of collection and intervention efficacy, suggesting the possibility of species-specific effects which were not further investigated. The SE device is a promising, low-cost, easily deployable, and distributable intervention that reduces exposure to mosquitoes with consequent impacts on transmission in outdoor environments.

Fig. 1

Typical structures and local environment inhabited by Orang Rimba study participants in the study area in Jambi, Indonesia

Fig. 2

Map of the study area displaying cluster locations. The national park is in the center of the study area, bordered closely by clusters 1–3, 4, and 8–10. The national park consists of secondary forest, while the surrounding forest has been converted to palm or rubber plantations. Clusters are denoted by their number, with an arrow connecting cluster sites for the two clusters which moved during the follow-up period of the study

Fig. 3

Proportional hourly host seeking activity in control and treatment clusters. Lines refer to the mean proportion of host seeking activity which occurred in each hour across all study nights in each cluster and study period, with the 95% confidence interval ribbons displayed

Fig. 4

Cumulative capture of Anopheles mosquitoes by study cluster over weekly entomological visits. Untreated clusters are displayed in panel A (left) with treated clusters in panel B (right). Each cluster is displayed as separate, colored lines, with mean values within the two treatment arms displayed in each panel as gray dashed lines. The baseline period is denoted by a gray box between weekly visits 1 and 7. Cluster movement occurred in two treatment clusters and is denoted by arrows. Vertical dotted lines represent device replacement

Fig. 5

Cumulative capture of Anopheles mosquitoes in treatment and placebo clusters. The number of mosquitoes is displayed cumulatively by visit on the x-axis by study arm. The baseline period is denoted by a gray background between visits 1 and 7