Patterns of human exposure to early evening and outdoor biting mosquitoes and residual malaria transmission in Ethiopia

Ethiopia has shown a notable progress in reducing malaria burden over the past decade, mainly due to the scaleup of vector control interventions such as long-lasting insecticidal nets (LLINs) and indoor residual spraying (IRS). Based on the progress, the country has set goals to eliminate malaria by 2030. However, residual malaria transmission due to early evening and outdoor biting vectors could pose a challenge to malaria elimination efforts. This study assessed vector behavior, patterns of human exposure to vector bites and residual malaria transmission in southwestern Ethiopia. Anopheles mosquitoes were collected monthly from January to December 2018 using human landing catches (HLCs), human-baited double net traps, CDC light traps and pyrethrum spray catches. Human behavior data were collected using questionnaire to estimate the magnitude of human exposure to mosquito bites occurring indoors and outdoors at various times of the night. Enzyme-linked immunosorbent assay (ELISA) was used to determine mosquito blood meal sources and sporozoite infections. A total of 2,038 female Anopheles mosquitoes comprising Anopheles arabiensis (30.8%), An. pharoensis (40.5%), An. coustani (28.1%), An. squamosus (0.3%) and An. funestus group (0.2%) were collected. Anopheles arabiensis and An. pharoensis were 2.4 and 2.5 times more likely to seek hosts outdoors than indoors, respectively. However, 66% of human exposure to An. arabiensis and 39% of exposure to An. pharoensis bites occurred indoors for LLIN non-users. For LLIN users, 75% of residual exposure to An. arabiensis bites occurred outdoors while 23% occurred indoors before bed time. Likewise, 84% of residual exposure to An. pharoensis bites occurred outdoors while 15% occurred indoors before people retired to bed. Anopheles arabiensis and An. pharoensis were 4.1 and 4.8 times more likely to feed on bovine than humans, respectively. Based on the HLC, an estimated indoor and outdoor EIR of An. arabiensis was 6.2 and 1.4 infective bites/person/year, respectively, whereas An. pharoensis had an estimated outdoor EIR of 3.0 infective bites/person/year. In conclusion, An. arabiensis and An. pharoensis showed exophagic and zoophagic behavior. Human exposure to An. arabiensis bites occurred mostly indoors for LLIN non-users, while most of the exposure to both An. arabiensis and An. pharoensis bites occurred outdoors for LLIN users. Malaria transmission by An. arabiensis occurred both indoors and outdoors, whereas An. pharoensis contributed exclusively to outdoor transmission. Additional control tools targeting early-evening and outdoor biting malaria vectors are required to complement the current control interventions to control residual transmission and ultimately achieve malaria elimination.