Human behavioural determinants of exposure to infective Anopheles gambiae s.l. bites in communities under indoor residual spraying (IRS) in northern Benin

Despite high community coverage with insecticide-treated nets (ITNs) and indoor residual spraying (IRS), residual malaria transmission remains a major obstacle to malaria elimination. No study has thoroughly assessed human behaviour over multiple nights and its influence on residual transmission in northern Benin. This study aims to identify the key behavioural and vector bionomic determinants of residual malaria transmission in two IRS-implementing regions in northern Benin. This cross-sectional study was conducted from June to August 2019 in four IRS districts, Kandi and Gogounou (Alibori region) and Djougou and Copargo (Donga region), and two adjacent control districts, Kouandé and Bembèrèkè. Human landing catches (HLC) were performed indoors and outdoors from 7:00 p.m. to 7:00 a.m. over two consecutive nights each month. The head-thoraces of Anopheles gambiae s.l. were analysed by enzyme-linked immunosorbent assay targeting the circumsporozoite protein (ELISA-CSP) to estimate the entomological inoculation rate (EIR). In July, a socio-anthropological survey was conducted in 64 households across the IRS districts over five consecutive nights per district, two of which coincided with the two monthly nights of mosquito collection. During these nights, human activities and locations were recorded every 30 min from 7:00 p.m. to 7:00 a.m. A total of 320 individuals were monitored across 64 households, with a mean household size of 5 individuals (95% CI 4–6). Between 7:00 p.m. and 11:00 p.m., a mean of 39.2% (95% CI 13.5–67.1%) of people were found inside IRS-treated houses. Among them, a mean of 25.5% (95% CI 13.5–31.8%) were not sleeping under an ITN and received 0.8 An. gambiae s.l. bites/night (b/n), compared to 0.5 b/nt among the 11.3–51.3% found outdoors without ITNs. During this period, the outdoor EIR reached 0.3 infective bites/person/month (ib/p/m) in treated areas, while the indoor EIR was null. Between 11:00 p.m. and 7:00 a.m., 5.6% (95% CI 4.2–26.7%) of people outside treated houses were exposed to 7.4 An. gambiae s.l. b/n, while 30.6% (95% CI 27.8–31.7%) of individuals not using bed nets indoors received 4.8 b/n. The outdoor EIR remained twice as high as the indoor EIR throughout this period. IRS induced a 96% reduction in the overall EIR (0.6 ib/p/m in the IRS zone vs. 15.6 ib/p/m in the control zone), and in treated areas, 75.2% of the residual transmission occurred outdoors (0.9 ib/p/m outdoors vs. 0.3 ib/p/m indoors). IRS substantially reduced malaria transmission in northern Benin. Nevertheless, residual transmission persisted particularly outdoors, driven by the exophagic feeding behaviour of An. gambiae s.l. and the prolonged outdoor presence of community members during peak vector activity hours. Integrated approaches combining IRS, ITNs, and complementary outdoor-targeting interventions are essential to accelerate progress toward malaria elimination.