The interplay between malaria vectors and human activity accounts for high residual malaria transmission in a Burkina Faso village with universal ITN coverage

Abstract

Background: Mosquito and human behaviour interaction is a key determinant of the maximum level of protection against malaria that can be provided by insecticide treated nets (ITNs). Nevertheless, scant literature focuses on this interaction, overlooking a fundamental factor for efficient malaria control. This study aims to estimate malaria transmission risk in a Burkina Faso village by integrating vector biting rhythms with some key information about human habits. Methods: Indoors/outdoors Human Landing Catches were conducted for 16 hours (16:00-08:00) during 8 nights (September 2020) in Goden village. A survey about net usage and sleeping patterns was submitted to half the households (October-December 2020). A subsample of A. gambiae s.l. collected specimens was molecularly processed for: species identification, Plasmodium detection from head-thoraxes, and L1014F pyrethroid-resistance allele genotyping. Hourly mosquito abundance was statistically assessed by GLM/GAM and the entomological inoculation rate (EIR) was corrected for the actual ITN usage retrieved from the questionnaire. Results: Malaria transmission was mainly driven by Anopheles coluzzii (68.7%), followed by Anopheles arabiensis (26.2%). The overall sporozoite rate was 2%, and L1014F estimated frequency of 0.68 (N=1,070 out of 15,201 A. gambiae s.l. collected). No major shift in mosquito biting rhythms in response to ITN, nor differences between indoor and outdoor, were detected. Impressive high biting pressure (mean 30.3 mosquitoes/person/hour) was exerted from 20:00 to 06:00 with a peak at 4:00. Human survey revealed that nearly all inhabitants were awake before 20:00 and after 7:00 and at least 8.7% had no access to bednets. Adjusting for anthropological data, the EIR dropped from 6.7 to 1.2 infective bites/person/16h. In a scenario of full net coverage and accounting only for the human sleeping patterns, the daily malaria transmission risk not targetable by ITNs was 0.69 infective bites. Conclusions: The high mosquito densities and the interplay between human/vector activities means that an estimated 10% of residual malaria transmission cannot be prevented by ITNs in the village. Locally-tailored studies, as the current one, are essential to explore the heterogeneity of human exposure to infective bites and, by consequence, to instruct the adoption of new vector control tools strengthening individual and community protection.