Background
Malaria is still a major public health emergency across the sub-Saharan Africa [
1]. The Senegalese Malaria Control Programme has made unprecedented progresses against the disease, and is now targeting malaria pre-elimination/elimination in eligible areas. However, despite the encouraging results, malaria stills endemic in the most parts of the country, including Dakar and its suburbs where the epidemiology of the disease has been locally complicated by recurrent flooding since 2005. Indeed, floods have created suitable conditions for the persistence of
Anopheles arabiensis larval habitats year-round [
2‐
6]. In this context, the subsequent upsurge of vector populations’ densities increases the risk of malaria transmission in such a high-density of non-immune population. Moreover, the above-mentioned successes were made possible by scaling-up effective malaria control interventions, including the two core malaria vectors control tools: long-lasting insecticide-treated nets (LLIN) and indoor residual spraying (IRS). Indeed, across the sub-Saharan Africa, the proportion of the population at risk sleeping under an insecticide-treated net or protected by IRS increased from 37% in 2010 to 57% in 2015 [
7].
In Senegal, as part of the malaria control effort with the U.S. President’s Malaria Initiative (PMI), the IRS programme has been introduced then scaled-up in different eco-epidemiological areas of the country [
8,
9]. High reliance on these insecticide-based interventions has subjected the targeted vectors populations to an increasing insecticide pressure for the selection of the resistance phenotypes. The spread of the resistance to the main insecticide classes approved by the World Health Organization (WHO) for use in public health threatens the success of the pre-elimination and elimination programmes in Senegal [
8]. In areas such as the western coastal areas, where the impact of climate change is most felt, the conjunction of climate hazards and insecticide resistance will increase the risk and the heterogeneity of malaria epidemiology [
10]. Therefore, monitoring insecticide resistance in the main urban malaria vector,
An. arabiensis, is essential for planning and implementing an effective vector control programme in this area.
This study was undertaken to characterize insecticide resistance and underlying mechanisms among the urban An. arabiensis populations across the flooded areas of the Dakar suburbs, the capital of Senegal.
Discussion
During this study,
An. arabiensis was the sole member of the Gambiae complex encountered in all the surveyed sites. This confirms this species as the unique or main representant of the Gambiae complex in Dakar [
2,
5,
6,
19]. No specimen of
Anopheles melas or
Anopheles coluzzii, previously reported [
6,
20] was found over the study period. During their study Gadiaga et al. [
6] collected
An. melas both at the larval and adult stages.
Anopheles melas larvae were often collected in association with
An. arabiensis from a variate breeding sites located in Cafeteriat, Pikine and Zone A, in Dakar suburb. The absence of
An. melas from the larval collection may be explained by the lower sampling effort compared to the previous study. A recent study carried-out in the same geographical area reported also only the presence of
An. arabiensis in both larval and adult anopheline populations [
2,
3].
Historically,
An. arabiensis is considered as the main malaria vector in the Cap Vert Peninsula where it is found all the year-round [
21,
22]. Robert et al. [
21] attributed this to the presence of permanent larval habitats formed by the so-called “Ceane” gardening pits which served as breeding site, especially during the dry season. Gadiaga et al. [
6] found significant difference in larval habitats conductivity between breeding sites containing both
An. melas and
An. arabiensis (5.03) and those exclusive for
An. arabiensis (1.75), with the conductivity of the water being the highest when
An. melas was present.
WHO susceptibility tests showed that
An. arabiensis populations were resistant to three classes of insecticides, but susceptible to organophosphates. The pronounced resistance to pyrethroids in the study populations is consistent with the overall situation reported for malaria vectors to this chemical family across the sub-Saharan Africa [
1].
The study populations were more susceptible to organophosphate compared to carbamate. Indeed, all
An. arabiensis populations were resistant to the bendiocarb except in Yeumbeul during the 2013 rainy season. Similar results were previously reported in the country including the study area [
23]. This situation may be explained by an extensive use of insecticide for crops protection in the market gardening activities in the Niayes area [
24,
25]. Moreover, Faye et al. [
26] have previously reported a resistance of
An. gambiae s.l. to DDT in the Niayes. The current cross-resistance of
An. arabiensis populations to pyrethroids and DDT may be an heritage of an extensive agricultural used of DDT in the past as hypothesized in Burkina Faso [
27]. However, Padonou et al. [
28] attributed it rather to the use of pyrethroids in public health.
Both the L1014F (
kdr-
West or
kdr-
w) and the L1014S (
kdr-
East or
kdr-
e) mutations, the two target site mechanisms conferring a cross-resistance to DDT and pyrethroids were found in almost all the study sites. Previous studies have reported the presence of the L1014F mutation nationwide with variable frequencies across the country and between studies [
10,
25]. Indeed, the
kdr-
w mutation was previously reported in the study area by Pagès et al. [
20]; and, as shown here, its frequencies have increased since this first description. During this study, the
kdr-
e mutation also found in study populations, was the most widespread and the most frequent
kdr allele. Therefore, more investigations are necessary to assess the contribution of each mutations to the resistance level of
An. arabiensis across its distribution range. Soderlund and Knipple [
29] have reported that the
kdr-
w mutation confers a highest resistance level, while the
kdr-
e gives a selective advantage to the individual that carries it [
30].
The ~ 20% co-occurrence of the two mutations in
An. arabiensis as observed here is similar to previous observations from several other sub-Saharan African countries, including Burkina Faso [
31], Tanzania [
32], Cameroon [
33,
34], Gabon [
35] and Uganda [
36].
The absence of organophosphates-carbamates cross-resistance suggests the absence of the
ace-
1R mutation gene [
37], which was not investigated during this study. However, there is an urgent need to investigate all potential insecticide resistance mechanisms for a suitable insecticide management system.
During this study, a proportion of mosquitoes did not harbour the
kdr alleles while the populations were fully resistant, suggesting the existence of other resistance mechanisms. Further analysis revealed the involvement of metabolic resistance mechanisms implying GST and
CYP450 detoxification genes families. Indeed, the susceptibility of studied populations to DDT and permethrin was fully restored following a pre-exposure to the PBO or EA. Similar results have been previously reported in different places in Dakar, including Fass and Colobane [
38], in Benin [
39,
40] and in Cameroon [
41]. However, data presented in both studies are limited and need to be completed and updated to fully characterize the resistance of
An. arabiensis populations to insecticide and underlying mechanisms.
Authors’ contributions
DAK, GOK and KA undertook the field and laboratory work. DAK, NEA and GOK analysed the results. DAK and NEA drafted the manuscript. KL and FO designed the study. NEA, DA, SB, DSM and SMD reviewed the manuscript. All authors read and approved the final manuscript.