Insecticide resistance and behavioural adaptation as a response to long-lasting insecticidal net deployment in malaria vectors in the Cascades region of Burkina Faso

Abstract

The decline in malaria across Africa has been largely attributed to vector control using long-lasting insecticidal nets (LLINs). However, this intervention has prompted widespread insecticide resistance (IR) and been associated with changes in mosquito behaviour that reduce their contact with LLINs. The relative importance and rate at which IR and behavioural adaptations emerge are poorly understood. We conducted surveillance of mosquito behaviour and IR at 12 sites in Burkina Faso to assess the magnitude and temporal dynamics of insecticide, biting and resting behaviours in vectors in the 2-year period following mass LLIN distribution. Insecticide resistance was present in all vector populations and increased rapidly over the study period. In contrast, no longitudinal shifts in LLIN-avoidance behaviours (earlier or outdoor biting and resting) were detected. There was a moderate but statistically significant shift in vector species composition from Anopheles coluzzii to Anopheles gambiae which coincided with a reduction in the proportion of bites preventable by LLINs; possibly driven by between-species variation in behaviour. These findings indicate that adaptations based on insecticide resistance arise and intensify more rapidly than behavioural shifts within mosquito vectors. However, longitudinal shifts in mosquito vector species composition were evident within 2 years following a mass LLIN distribution. This ecological shift was characterized by a significant increase in the exophagic species (An. gambiae) and coincided with a predicted decline in the degree of protection expected from LLINs. Although human exposure fell through the study period due to reducing vector densities and infection rates, such ecological shifts in vector species along with insecticide resistance were likely to have eroded the efficacy of LLINs. While both adaptations impact malaria control, the rapid increase of the former indicates this strategy develops more quickly in response to selection from LLINS. However, interventions targeting both resistance strategies will be needed.

Risk of Plasmodium falciparum infection in south-west Burkina Faso - potential impact of expanding eligibility for seasonal malaria chemoprevention

“…Human landing catches were carried out inside houses twice a month during the 2017 transmission season in each of the 10 villages 14 . Four households were sampled on one night every month, with a different group of households selected the following month to maximise spatial coverage.…”

“…coluzzii and, to a lesser extent, An. arabiensis 14,18 . The site has an entomological inoculation rate (EIR) of 80 infective bites per child during the transmission season 8 , with another study suggesting up to 52 infective bites per person per night during the peak transmission season in October 19 .…”

“…PBO is an insecticide synergist which inhibits the action of resistance-associated metabolic enzymes of the cytochrome P450 family and improves control of pyrethroid-resistant anopheline mosquitoes. The added advantage of pyrethroid-PBO ITNs over pyrethroid-only ITNs is estimated from a meta-analyses of experimental hut trial data 32 and the level of resistance for the region estimated using discriminating dose bioassay 14 . The impact of changing SMC is assessed using the same method as outlined previously 33 , either halting SMC, maintaining the existing age range of 0-5 year olds or extending the upper age limit to 10 or 15 years.…”

“…SMC requires the administration of the anti-malarial drugs sulfadoxine-pyrimethamine (SP) and amodiaquine (AQ) monthly for four months during the high transmission season to prevent malaria and is recommended by WHO across the Sahel Region 7 . Potential explanations for the stagnating progress in malaria control include low ITN usage or lack of ITN bioe cacy and durability [8][9][10][11] , a rise in the resistance of vectors to pyrethroid insecticides used to treat ITNs [12][13][14] , and an increase in outdoor vector biting 14 .…”

“…(Lambert et al, unpublished) which is parameterised with local epidemiological 8 and entomological data14,19 and tted to estimates of malaria prevalence (assessed by microscopy) across the Cascades region collated by the Malaria Atlas Project (https://malariaatlas.org/). It is used to predict the number of clinical cases per person in the whole population between 2019 and 2022 following the mass ITN campaign in 2019.…”