Background
After decades of efforts to malaria control, this disease is still a major public health concern in sub-Saharan Africa, responsible for an estimated of 219 million cases and 435,000 deaths in 2017 [
1]. Burkina Faso is a malaria endemic country with 19 million inhabitants, where nearly 12 million malaria cases were reported in 2017 with 4144 resulting in death [
2]. In Burkina Faso, malaria prevention primarily relies on insecticide-treated bed nets. In 2010, 2013 and 2016 combined, approximately 36 million long-lasting insecticide-treated nets (LLINs) were freely distributed through mass distribution campaigns. Additional sporadic measures such as Indoor Residual Spraying (IRS) with bendiocarb were introduced in 2010 in Diébougou, a locality situated in the southwestern part of Burkina Faso but this pilot programme was terminated in 2011 (
http://www.africairs.net/where-we-work/burkina-faso/). A larviciding pilot programme using
Bacillus thuringiensis was also implemented for 1 year in 2012 to control malaria in Ouagadougou the capital city of Burkina Faso.
Anopheles gambiae,
Anopheles coluzzii,
Anopheles arabiensis and
Anopheles funestus are the most important malaria vectors in Burkina Faso [
3,
4]. Members of the
An. gambiae complex are sympatric species with different ecological niches [
5,
6]. Previous studies showed that the species composition of the
An. gambiae complex varied across Burkina Faso climatic conditions. Whilst
Anopheles arabiensis and
An. coluzzii are distributed with equal frequency in central and eastern regions of the country [
7], the western regions, where rainfall is abundant, are dominated by
An. gambiae sensu stricto (s.s) [
5,
8].
Anopheles arabiensis is the most abundant species found in urban compared to rural areas [
6]. Recently a new cryptic sub-group inside
An. gambiae, named Goundry, was identified in Burkina Faso [
9] with an exophilic behaviour.
The development of resistance to insecticides in malaria vectors is one of the main concerns for malaria control as to date major vector tools rely on insecticide use. In Burkina Faso, resistance to the four major classes of insecticides (organochlorides, organophosphates, pyrethroids and carbamates) used in public health has recently increased throughout the country. The resistance level to pyrethroids is particularly high in the Western region of the country [
10‐
12], which may affect bed nets efficacy [
13]. Four mechanisms of insecticide resistance have been described in West Africa [
14,
15]. One of the most widespread mechanisms is target site mutation associated with resistance to pyrethroids and DDT [
16] in the voltage-gated sodium channel, associated with knock down resistance (
kdr) alleles. Three
kdr mutations have been reported in the
An. gambiae complex: L1014F, L1014S and N1575Y [
17‐
19]. There is increasing evidence that insecticide pressure used in public health and agriculture is leading to the selection of insecticide resistance in malaria vectors [
13]. The 1014F
kdr allele frequency is very high in
An. gambiae and
An. coluzzii in Burkina Faso, while the 1014S is very common in
An. arabiensis [
10,
12,
20].
There is little empirical data on the impact of insecticide resistance on malaria transmission but modeling has predicted that widespread resistance to pyrethroids will result in additional 260,000 deaths in children under 5 years of age [
21] in the WHO African Regions. Insecticide resistance is assumed to increase the likelihood of mosquito-borne disease transmission by increasing the vector population size and allowing mosquitoes a long period of life even the presence of insecticides [
22]. On the other hand, resistance may reduce the vectorial capacity by imposing a major fitness cost to mosquitoes [
22], but laboratory experiments have suggested that mosquito strains with the
kdr mutation were more susceptible to
Plasmodium infection [
23]. However, it has also been reported that older
Anopheles mosquitoes are more susceptible to insecticides than newly-emerged ones [
24‐
27]. Hence, if insecticide resistant mosquitoes are more susceptible to infection with the malaria parasite, then the chances to transmit malaria parasite in areas with intensive insecticide exposure may be diminished, according to Viana et al. [
28]. In contrast, a previous laboratory experiments showed that mosquitoes resistant to pyrethroids may be more susceptible to
P. falciparum infection, and thus could potentially be more efficient malaria vectors [
29]. Thus, field studies are needed to establish whether there is any association between insecticide resistance and the ability of the mosquito to transmit the malaria parasite (i.e. the presence of sporozoites in the mosquito’s salivary glands).
A three-year longitudinal study was conducted in Burkina Faso between 2008 and 2010 to assess for longitudinal changes in insecticide resistance from larval collections and results were published in Badolo et al. [
10]. In addition, during this study, adult mosquitoes were also collected indoor and outdoor in different ecological settings with different levels of insecticide resistance. The objectives of this work were to report on the species diversity of malaria vectors in these different ecological settings of Burkina Faso and the association between insecticide resistance and the mosquito’s ability to transmit malaria. Due to the sample size it was not possible to investigate the association between L1014F-mutation and sporozoite infection. Instead, this study assessed the association between L1014F-genotype with the sporozoite infection.
Discussion
The present study shows that
An. gambiae s.l. is the most predominant malaria vector within the study area. Molecular identification showed that
An. gambiae s.l. consists of the three species
An. gambiae sensu stricto
, An. coluzzii and
An arabiensis and that there is a significant difference in their proportion between the sites within the study area.
Anopheles arabiensis was the most abundant species occurring in Goundry, but found at the similar frequency as
An. Coluzzii in Koupela. In the southern areas (Kuinima and Soumousso)
An. gambiae s.s was the most predominant species followed by
An. arabiensis. These findings are in agreement with previous studies suggesting that
An. gambiae s.s
., An coluzzii and
An. arabiensis are the most widespread malaria vectors across Burkina Faso [
6,
7]. However, the relative frequency of these species varied according to ecological settings. Furthermore, a significant reduction was found in the
An. arabiensis proportion in 2008 from sample collected as adults within all sites particularly in Koupela, Kuinima and Soumousso compare to proportion from sample collected as larvae and reared to adulthood in laboratory conditions and described in Badolo et al. [
10]. The missing proportion of
An. arabiensis was subsequently filled mainly by
An. gambiae s.s. in Soumousso and Kuinima and by
An. coluzzii in Koupela and Goundry. The observed variation in species composition between larvae and adult populations may be partially due to the high susceptibility of
An. arabiensis to insecticides as also suggested by the bioassay results described elsewhere showing an association between the 1014F-genotype and mosquito survival to permethrin and DDT [
10]. This may be indicative of the effect of insecticide resistance on species composition according to insecticide use within a given area.
Complementary trapping methods were used to collect a representative sample of
Anopheles gambiae complex mosquitoes with reference to resting behaviour. The results show a significant difference in species composition between these collection methods. In most cases, the three species from the
An. gambiae complex were abundantly caught inside houses. An important fraction of this population was also found in exit traps and pit shelters. More specifically,
An. arabiensis predominated in outdoor collection (window exit trap and pit shelters). This behaviour of
An. arabiensis is consistent with previous studies showing that
An. arabiensis are more generalist in terms of host choice and resting behaviour due to phenotypic plasticity [
38].
Vector species with a relatively broad host range, like
An. arabiensis, are thought to be better able to persist in areas of high indoor insecticide use. In contrast,
An. coluzzii was caught in higher abundances in PSC. The PSC is intended to collect mosquitoes that feed and rest indoors or feed outdoors and indoors (endophilic mosquitoes), therefore, it may be less sensitive in collecting species that predominantly rest outdoors [
39], compared to exit traps and pit shelters that target outdoor-resting mosquitoes.
Anopheles funestus was highly caught indoor using PSC and outdoor in pit shelters. This finding is in agreement with previous studies on
An. funestus population from Burkina Faso describing two chromosomal forms with different resting behaviour patterns: one form was mainly exophilic and the second endophilic [
40].The current study shows significant difference in resting behaviour between
An. arabiensis and the two other species,
An. coluzzii and
An. gambiae s.s., depending on the geographical location. Meanwhile the efficacy of vector control intervention based on IRS may be affected by this behaviour. This result is aligned with previous findings showing that
An. arabiensis was more exophilic, exophagic and zoophilic than
An. gambiae s.s [
41].
Following Badolo et al. [
10], one of the aims of this study was also to investigate the association between the
kdr 1014F-genotype and the infection status. The results from this study showed that
P.
falciparum sporozoite rate varied significantly between the four study sites [
10]. Based on laboratory experiments, Ndiath et al. [
42] suggested that
An. coluzzii was less susceptible to
P. falciparum infection than
An. gambiae s.s, while Gneme et al. [
43] found that in Burkina Faso
An. gambiae s.s. and
An.
coluzzii were equally susceptible to
P.
falciparum infection. Additionally, previous field studies from Burkina Faso [
6] and Senegal [
44] reported no difference in sporozoite rate between
An. gambiae s.s. and
An. coluzzii confirming the findings of the present study. Furthermore, a high proportion of homozygote mosquito to 1014F-genotype was found here in the sporozoite-infected mosquito sub-group compared to uninfected group, but there was no statistical difference suggesting that variation in resistance genotype proportion is not associated with the infection status. The current findings do not support the work from Alout et al. [
23], who showed that
An. gambiae mosquitoes with
kdr alleles are more susceptible to
Plasmodium than insecticide susceptible mosquitoes, and also contrast with the findings in Senegal, Burundi and Tanzania, which reported a significant correlation between the 1014F-genotype and the infection with
P. falciparum [
45‐
47]. This disagreement could be explained by the small sample size of this study which may limit the power to infer this relationship. The small sample size in this study also limited the comparison of the 1014F-genotype frequencies from mosquito collected as larvae versus those collected as adults. So, the results may have been different when increasing the samples size to those of Kabula et al. [
47], who tested 526 specimens.
Authors’ contributions
HR and NFS conceived and designed the study. AT, SA, AB, NFS and HR drafted the manuscript. MV, LN, AS and AT analysed the data. AT, AB, AS, MWG, ZS and HKT oversaw field collection and laboratory work. All authors read and approved the final manuscript.