Insecticide resistance levels and mechanisms in Aedes aegypti populations in and around Ouagadougou, Burkina Faso

Abstract

Background Recent outbreaks of dengue and other Aedes aegypti -borne arboviruses highlight the importance of a rapid response for effective vector control. Data on insecticide resistance and underlying mechanisms are essential for outbreak preparedness, but are sparse in much of Africa. We investigated the levels and heterogeneity of insecticide resistance and mechanisms of Ae . aegypti from contrasting settings within and around Ouagadougou, Burkina Faso. Methodology/Principal findings Bioassays were performed on larvae and adults to diagnose prevalence of resistance, and to assess levels where resistance was detected. Investigation of resistance mechanisms was performed using synergist bioassays, knockdown resistance ( kdr ) target site mutation genotyping and quantitative PCR expression analysis of candidate P450 genes. Larval dose-response assays indicated susceptibility to the organophosphates tested. Adult females were also susceptible to organophosphates, but resistance to carbamates was suspected in urban and semi-urban localities. Females from all localities showed resistance to pyrethroids but resistance prevalence and level were higher in urban and especially in semi-urban areas, compared to the rural population. Environment was also associated with susceptibility: adults reared from larvae collected in tires from the semi-urban site were significantly less resistant to pyrethroids than those collected from large outdoor drinking water containers (‘drums’). Susceptibility to both pyrethroids tested was largely restored by pre-exposure to Piperonyl Butoxide (PBO), suggesting a strong metabolic basis to resistance. The 1534C kdr mutation was nearly fixed in semi-urban and urban areas but was far less common in the rural area, where the 1016I kdr mutation frequency was also significantly lower. P450 gene analysis detected limited over-expression of single candidates but significantly elevated average expression in the semi-urban site compared to both a susceptible laboratory colony, and females from the other collection sites. Conclusions/Significance Our results reveal pyrethroid resistance and paired kdr mutations in both urban and semi-urban sites at levels that are unprecedented for mainland Africa. The combination of target site and metabolic mechanisms is common in Ae . aegypti populations from other continents but is a worrying finding for African populations. However, organophosphate insecticides are still active against both larvae and adults of Ae . aegypti , providing useful insecticidal options for control and resistance management.

Metabolic resistance mechanism in Aedes aegypti from Lagos State, Nigeria

“…In this study, susceptibility to bendiocarb was recorded in three of the four surveyed LGAs namely; Kosofe, Badgry and Ibeju-Lekki while suspected resistance was reported in Alimosho LGA. Similar studies have reported Aedes aegypti susceptibility to carbamates in Umudike, southeastern Nigeria (Ukpai & Ekedo, 2018) and Cameroon (Kamgang et al, 2011) while carbamates resistance has been previously reported in Kwara State, Nigeria (Oduola et al, 2016), Burkina Faso (Badolo et al, 2019), Indonesia (Hamid et al, 2018), and Sri Lanka (Leong, Vythilingam, Wee, Liew, & Wong, 2019). PBO synergist was able to significantly increase the 24-h percentage and also reduce the knockdown time of Aedes aegypti to DDT and permethrin in this study; previous studies in different parts of the world have demonstrated the efficacy of PBO synergists in the management of insecticides resistant vectors.…”

“…Pyrethroid resistance was recorded in all the study areas in this study, similar to previous studies in Lagos and Kwara States, Nigeria, reported susceptibility of Aedes aegypti to permethrin (Ayorinde et al, 2015;Oduola, Obembe, Adelaja, & Ande, 2016), though suspected resistance to deltamethrin has been reported in Lagos (Ayorinde et al, 2015) and Umudike, (Ukpai & Ekedo, 2018) both in the southern part of Nigeria. Pyrethroids resistance in Aedes aegypti has also been previously reported in Cameroon (Kamgang et al, 2011;, Burkina Faso (Badolo et al, 2019), Malaysia (Ishak et al, 2017), and several other parts of the world. Selection pressure as a result of indiscriminate usage of insecticides for agricultural, domestic, and public health purposes has been associated with DDT and pyrethroids resistance in mosquitoes (Awolola et al, 2007;Fagbohun, Oyeniyi, Idowu, Otubanjo, & Awolola, 2019;Kamgang et al, 2011).…”

First detection of F1534C knockdown resistance mutation in Aedes aegypti (Diptera: Culicidae) from Cameroon

“…aegypti from two locations (Edéa and Douala) of Cameroon. This kdr mutation was previously reported in Africa in Ghana [ 21 ] and Burkina Faso [ 29 , 35 ]. The allelic frequency of this mutation observed in Cameroon (3.3–33.3%) is low compared to those found in Ghana for example (33.3–68.42%) [ 21 ].…”

“…In addition, it will be interesting to genotype other mutations such as 1016 and 410 which have been found implicated in kdr resistance in Ae. aegypti [ 22 , 28 – 30 ] and investigate the genes involved in metabolic resistance such as CYP9 overexpressed in several regions worldwide including in Africa [ 35 ].…”

“…As previous study in Central Africa [ 18 ] had not reported any mutation associated to pyrethroid resistance, we decided to focus our analysis in F1534C mutation which is mostly found worldwide including in West Africa [ 21 , 35 ]. For this purpose, genomic DNA of 30 individual mosquitoes per populations was extracted using Livak protocol [ 36 ].…”