Background
Malaria remains the deadliest tropical infectious disease, with higher incidences in Africa [
1]. In 2018, malaria has caused over 228 million cases and 405,000 deaths worldwide, of which 93% has occurred in sub-Saharan Africa [
1]. In 2019, the overall number of cases increased from 228 to 229 million of malaria cases with 409,000 deaths [
2]. In Côte d’Ivoire, malaria is still a major public health challenge and the leading reason for consultations in health services. It is responsible for up to 43% of morbidity, 11.8% of mortality, 40% of school absenteeism, 50% of loss of agricultural income and 62% of hospitalizations [
3]. According to the world malaria report, the entire Ivorian population is at risk of malaria, with the most vulnerable being children under 5 years of age and pregnant women [
4].
Malaria transmission in Africa is very heterogeneous due to eco-climatic variations across the continent [
5]. Currently, five species of the
Plasmodium parasites have been identified as being responsible for malaria infection in humans [
6,
7]. Of these,
Plasmodium falciparum remains the most prevalent and most virulent species causing the deadly forms of malaria [
7,
8]. The
Plasmodium species responsible for human malaria are mainly transmitted by primary vector species, such as
Anopheles gambiae sensu lato (
s.
l.) [
9],
Anopheles funestus group and
Anopheles nili group [
10‐
12].
In West Africa, two molecular forms have been identified in
An. gambiae s.l., formerly known as M and S. Recently, they have been identified as distinct species belonging to the
An.
gambiae complex and named
Anopheles coluzzii for the M form and
An. gambiae sensu stricto (
s.s.) for the S form [
10]. These species display strong anthropophilic host-seeking behaviour and longevity, causing large numbers of malaria cases [
13].
Anopheles larvae are aquatic and found in a variety of breeding habitat types in terms of size, permanence, vegetation and water cleanliness [
14]. Overall, the larvae of
An. gambiae s.l. grow in small, shallow, relatively clean and sunny water reservoirs (puddles of water, stagnant water) [
15,
16], and is more frequent and rain-dependent.
Anopheles coluzzii is associated to permanent breeding sites and those resulting from human activity and prefers urban water collections and adapts quickly to pollution [
17,
18]. According to Mourou et al. [
19], the breeding habitats of this species are known to increase in number and productivity during the rainy season, but almost disappear during the dry season. Deploying major vector control interventions, such as the scale-up of long-lasting insecticidal nets (LLINs) and indoor residual spraying (IRS), requires detailed understanding of the species composition, distribution and behaviour dynamics of the local vectors to avoid limited impact or intervention failure [
20,
21].
In Côte d’Ivoire, the malaria vectors
An. gambiae s.s. and
An. coluzzii are widespread across the country [
22,
23], whilst
An. funestus s.l. and
An. nili act as secondary vectors [
24].
Anopheles gambiae s.s. and
An. coluzzii are well-adapted to diverse types of breeding sites (e.g., permanent breeding sites or temporary rain pools such as puddles, shallow wells, footprints, or in rice and vegetable fields), which are generally frequent in both rural and urban areas [
25]. The country shows considerable bio-climatic variations from the North to the South, leading to the subdivision of the country into different ecological zones [
26]. Thus, the South-East of Côte d’Ivoire is marked by coastal inland lagoons [
27]. The southern region, especially the South-West, is covered with dense tropical rainforest. The Guinean forest-savannah mosaic belt extends across the middle of the country from the East to the West and the northern part belongs to the Sudanian savannah. All these ecological conditions contribute to the proliferation of many malaria vector species across the country [
28]. This contributes to the stability of malaria transmission throughout the year, with peaks during the rainy season [
29]. Identifying these vector species and their involvement in malaria transmission in these different ecological zones could provide essential information that could guide the planning and implementation of vector control measures. Furthermore, limited entomological data are available on disease transmission dynamics, particularly in districts along the borders of the country. This study assessed the species diversity of
Anopheles mosquito vectors, members of the
An. gambiae complex and transmission of malaria in four health districts at the border areas of Côte d'Ivoire.
Discussion
Malaria is still a leading cause of death and poverty in the majority of the countries in sub-Saharan Africa due to country vectors specificity and even differences within ecological zones of a country implying targeted monitoring to better understand and support vector control decision-making. This study assessed
Anopheles mosquito vectors and malaria transmission in district health facilities at the borders of Côte d’Ivoire, coupled with the malaria incidence during the second semester of both 2016 and 2017 [
38]. In this study, the relative diversity and abundance of
Anopheles mosquitoes in four districts located at the borders of Côte d'Ivoire has been highlighted and assessed their implications in malaria transmission to local communities. The results have shown that
An. gambiae s.l. was most the abundant vector of malaria in the four districts. Moreover,
Plasmodium sporozoite infection rate in
An. gambiae s.l. and
An. funestus s.l. was higher in Odienné (11.0% and 8.27%, respectively) and Bloléquin (7.8% and 6.2%, respectively), compared with Aboisso (3.1% and 0%, respectively) and Ouangolodougou (2.5% and 0%, respectively). Similarly, malaria prevalence rate among people in Odienné (39.7%) and Bloléquin (37.6%) health districts was higher compared with that in Ouangolodougou (18.3%), and Aboisso (19.7%) health districts.
A diversity of
Anopheles mosquito species including seven
Anopheles species was recorded, among which three (
An. gambiae s.l.,
An. funestus s.l. and
An. nili) have previously been incriminated in malaria transmission in Côte d’Ivoire [
22,
39]. Moreover,
An. gambiae s.l. was the predominant species in all study sites, with particularly higher abundance in the northern health districts of Ouangolodougou and Odienné located in savannah zones compared with the districts of Aboisso and Bloléquin situated in forest zones. The high diversity and variation in the relative abundance of
Anopheles mosquito species might result from a combination of ecological and climatic factors favouring the larval development of some species. Indeed, permanent water sources, puddles and small dams are probably abundant in these areas [
40,
41].
The diversity and variation in
Anopheles mosquito species composition are mostly related to human activities (e.g., rice farming, vegetable crops) [
42,
43]. Odienné and Ouangolodougou are rural districts in which several crops are cultivated including rice, maize, yam, vegetable crops, cashew nuts and cotton. Rice paddies and vegetable crops were strongly associated with high densities of malaria vectors [
44,
45]. In addition,
An. gambiae s.l. exhibited high parity rates in all districts, thus suggesting that a significant proportion of the local vector populations that have sufficient lifespan allowing for the completion of
Plasmodium parasite lifecycle and transmission to humans. Similar findings have previously been reported in Côte d’Ivoire [
46,
47].
This study showed that
An. coluzzii was the predominant species in forest area, whilst
An. gambiae s.s. was the dominant species in savannah. The relative abundance of these two species is associated with specific and characteristic breeding sites as previously reported in Côte d'Ivoire [
40,
48]. The abundance of
An. coluzzii in samples from forest areas could be related to the type of breeding sites and the climatic conditions in these study sites [
49,
50]. Several studies carried out in Côte d'Ivoire have shown a predominance of
An. coluzzii in forest area especially in the western [
22] and south-eastern [
51] parts. The highest abundance of
An. gambiae s.s. was observed in the savannah area where relatively abundant precipitation provides more favorable humidity and temperature conditions [
52,
53]. The predominance of
An.
gambiae s.s. in savannah zones has been observed by Touré et al
. [
54] and Tia et al
. [
48], suggesting that environmental conditions in savannah zones are unfavourable for the reproduction and the survival of
An. coluzzii.
Understanding malaria transmission at the local level is essential for the development and implementation of effective vector control strategies. Thus, to identify potential vector species of malaria in our various study sites, individual females of
An. gambiae s.l. were tested using molecular PCR for the presence of
P. falciparum sporozoites. The finding showed that only two species were involved in malaria transmission across the four health districts, with
An. gambiae s.l. being the main malaria vector in all districts. In addition,
An. gambiae s.l. and
An. funestus s.l. were efficient vectors of
P. falciparum in these two cross-border districts. This observation is consistent with findings from previous studies showing that the high capacity of malaria vectors ensures high transmission in an ecological area is intimately related with environmental conditions [
21,
22]. Although infection rates were almost similar between study sites, the intensity of transmission was very heterogeneous. Malaria transmission is lower in Aboisso and Ouangolodougou health districts. In contrast, it remains relatively high in Bloléquin and Odienné districts where two additional
Anopheles vectors are involved in malaria transmission. This high transmission of malaria could possibly be due to the high infection rate of malaria vectors and the non-respect of vector control measures in these districts where control strategy is based mainly on the distribution of distribution of LLINs. In addition, the presence of several vectors in the same area could significantly increase the risk of malaria transmission. This study suggests that malaria vector control interventions should be strengthened in Bloléquin and Odienné in order to reduce or eliminate the burden of malaria in these districts.
The low prevalence of malaria observed (< 20%) in the health districts of Aboisso and Ouangolodougou suggests that both districts are in areas of moderate transmission [
55]. In contrast, high prevalence rates of
P. falciparum infections (ranging from 37.6 to 39.7%) in Bloléquin and Odienné may imply that these districts are areas of high malaria transmission. This variation of
Plasmodium transmission from one health district to another may be related to climatic conditions. Several previous studies have shown that
Plasmodium infections are influenced by environmental factors such as temperature, rainfall, humidity and altitude [
56,
57]. These factors directly or indirectly influence the development and appearance of
Anopheles mosquitoes and, thus, the geographical distribution of the malaria infection and disease. The heterogeneity of malaria transmission observed in the present study is consistent with previous studies [
27,
39]. This may also be the effect of differences in intervention strategies coordinated by the National Malaria Control Programme (NMCP), especially mass distribution of LLINs to vulnerable population and the use of ACT for the early treatment of malaria cases.
The country experienced already four campaigns of LLINs distribution and malaria transmission remains high and heterogeneous across cross-border health districts of Côte d’Ivoire with the presence of several vector species:
An. funestus s.l., An. nili and
An. gambiae s.l. The latter is the most species encountered. The study showed a high diversity and abundance of
Anopheles mosquitoes, which could contribute to malaria transmission persistence over time. Moreover, high sporozoite infection and parity rates were recorded in all four heath districts and highlighted the high transmission of malaria within local populations. Currently, the vector control strategy of NMCP of Côte d'Ivoire is based on LLIN distribution. Recently in August 2020, the President Malaria Initiative (PMI) through the MoH implemented IRS in pilot site (Sakassou), in order to strengthen LLINs effects that have already proven effective in individual and community protection against malaria. [
58,
59]. However, in the recent past, pyrethroids were the single insecticide class used for impregnation of LLINs, owing to their rapid action, excito-repellent effects, effectiveness at low doses and low toxicity to humans [
60]. Unfortunately, pyrethroid resistance in malaria vectors has emerged and spread rapidly in Côte d’Ivoire [
61] and several parts of Africa [
62‐
64]. Therefore, efforts should be made to evaluate the effectiveness of insecticide-treated LLINs with different modes of action to which there is no cross-resistance and to evaluate promising tools to be used in combination with LLINs in highly endemic areas. Since mosquito capture has been done indoors, it is important to rapidly roll out the implementation of IRS nationally in highly endemic districts using next generation formulations, which has already proven its effectiveness in combination with LLIN [
65].
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