Why does malaria transmission continue at high levels despite universal vector control? Quantifying persistent malaria transmission by Anopheles funestus in Western Province, Zambia

Abstract

Background Some settings continue to experience a high malaria burden despite scale-up of malaria vector control to high levels of coverage. Characterisation of persistent malaria transmission in the presence of standard control measures, also termed residual malaria transmission, to understand where and when individuals are exposed to vector biting is critical to inform refinement of prevention and control strategies. Methods Secondary analysis was performed using data collected during a phase III cluster randomized trial of attractive targeted sugar bait stations in Western Province, Zambia. Two seasonal cohorts of children aged 1–14 years were recruited and monitored monthly during the malaria transmission season, concurrent with entomological surveillance using a combination of human landing collection (HLC) and UV light traps at randomly selected households in study clusters. Behavioural data from cohort participants were combined with measured Anopheles funestus landing rates and sporozoite positivity to estimate the human behaviour-adjusted entomological inoculation rate (EIR). Results Behavioural data from 1237 children over 5456 child-visits in 20 entomology surveillance clusters were linked with hourly landing rates from 8131 female An. funestus trapped by HLC. Among all An. funestus tested by ELISA, 3.3% were sporozoite-positive. Mean EIR directly measured from HLC was 0.07 infectious bites per person per night (ib/p/n). When accounting for child locations over the evening and night, the mean behaviour-adjusted EIR was 0.02 ib/p/n. Children not sleeping under insecticide-treated nets (ITNs) experienced 13.6 infectious bites per person per six-month season, 8% of which occurred outdoors, while ITN users received 1.3 infectious bites per person per six-month season, 86% of which were received outdoors. Sleeping under an ITN can prevent approximately 90% of potential An. funestus bites among children. Conclusions In this setting ITNs have a high personal protective efficacy due to peak An. funestus biting occurring indoors while most individuals are asleep. However, despite high household possession of ITNs (> 90%) and high individual use (> 70%), people in this setting experience more than one infectious bite per person per six-month transmission season, sufficient to maintain high malaria transmission and burden. New tools and strategies are required to reduce the malaria burden in such settings.