• Users Online: 257
  • Home
  • Print this page
  • Email this page
Home About us Editorial board Ahead of print Current issue Search Archives Submit article Instructions Subscribe Contacts Login 

Table of Contents
Year : 2022  |  Volume : 59  |  Issue : 3  |  Page : 275-284

High vectorial transmission of malaria in urban and rural settings in the northern, western and eastern regions of Côte d’Ivoire

1 Institut Pierre Richet (IPR)/ Institut National de Santé Publique (INSP), Bouaké; Université Félix Houphouët-Boigny, Cocody, Abidjan, Côte d’Ivoire
2 Institut Pierre Richet (IPR)/ Institut National de Santé Publique (INSP), Bouaké; Programme National de Lutte contre le Paludisme, Abidjan, Côte d’Ivoire
3 Université Félix Houphouët-Boigny, Cocody, Abidjan, Côte d’Ivoire
4 Centre d’Entomologie Médicale et Vétérinaire, Abidjan, Côte d’Ivoire
5 Institut Pierre Richet (IPR)/ Institut National de Santé Publique (INSP), Bouaké, Côte d’Ivoire; MIVEGEC, Institut de Recherche pour le Développement, Montpellier, France
6 Programme National de Lutte contre le Paludisme, Abidjan, Côte d’Ivoire

Date of Submission22-Nov-2020
Date of Acceptance12-Jul-2022
Date of Web Publication08-Dec-2022

Correspondence Address:
Konan F Assouho
Institut Pierre Richet (IPR)/Institut National de Santé Publique (INSP), Bouaké Côte d’Ivoire, Université Félix Houphouët-Boigny, Cocody, Abidjan, Côte d’Ivoire

Login to access the Email id

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0972-9062.355967

Rights and Permissions

Background & objectives: Malaria remains a public health problem in Côte d’Ivoire. To cope with this issue, the Ministry of Health established strategies through Long-Lasting Insecticidal Nets (LLINs) and artemisinin-based medicines. To better understand the influence of periodic mass distribution of LLINs on malaria transmission, this entomological survey was conducted in three regions of Côte d’Ivoire.
Methods: Mosquitoes were sampled by Human Landing Catches (HLC) in urban and rural settings of Korhogo, Man and Abengourou. Mosquitoes were identified morphologically and by molecular methods. Plasmodium falciparum infection was assessed by ELISA, and the Entomological Inoculation Rates (EIR) were calculated for each species and setting.
Results: Only An. gambiae s.l. was identified in Korhogo and in Abengourou while An. gambiae s.l. and An. funestus s.l. was reported in Man. An. coluzzii was the most abundant species of the An. gambiae siblings collected in Abengourou, and in Man while An. gambiae was most abundant in Korhogo. In urban settings, malaria vectors showed high aggressiveness (>11 bites per person per night) and the annual EIR was high (83.22-438.44 infectious bites per person per year). In rural settings, malaria vectors showed also high aggressiveness (19-52 b/p/n). The annual EIR is very high (>94 ib/p/yr). However, the weakest EIR was recorded in the northern region with 94.90 ib/p/yr.
Interpretation & conclusion: This work indicates that malaria transmission remains high and heterogeneous across Côte d’Ivoire, despite repeated mass distribution of LLINs. Also, in Man, malaria transmission is more intense with the involvement of two main vectors. Furthermore, in the village of Korhogo, the EIR remained relatively low.

Keywords: Anopheles gambiae; Anopheles funestus; urban; rural; Côte d’Ivoire

How to cite this article:
Adja AM, Assouho KF, Assi SB, Guindo-Coulibaly N, Tia E, Sagna AB, Zoh DD, Moro AC, Yapi A. High vectorial transmission of malaria in urban and rural settings in the northern, western and eastern regions of Côte d’Ivoire. J Vector Borne Dis 2022;59:275-84

How to cite this URL:
Adja AM, Assouho KF, Assi SB, Guindo-Coulibaly N, Tia E, Sagna AB, Zoh DD, Moro AC, Yapi A. High vectorial transmission of malaria in urban and rural settings in the northern, western and eastern regions of Côte d’Ivoire. J Vector Borne Dis [serial online] 2022 [cited 2023 Feb 2];59:275-84. Available from: http://www.jvbd.org//text.asp?2022/59/3/275/355967

  Introduction Top

Malaria continues to have a devastating impact on public health and welfare in the African continent. This disease, transmitted by the bite of infected female Anopheles mosquitoes, is a major health burden in Côte d’Ivoire[1][2]. The dominant parasite in this country is Plasmodium falciparum and this disease remains the leading cause of con-sultation in health services[2][3]. In the country, four species of Anopheles are responsible of malaria transmission[4][6] (Anopheles gambiae s.s., Anopheles coluzzii, Anopheles funestus s.s. and Anopheles nili s.s.).

Various factors contribute to differing malaria epidemiological profiles, including altitude, topography, hydrology and land use/land cover types[7][8]. Specifically, changes in environmental factors can impact malaria transmission by altering the microclimate of the immature stages and adult mosquitoes[9], as it has been observed that shortening of Plasmodium sporogony and vector gonotrophic cycle leads to an increase of malaria transmission risk across a highland environment in Kenya[10]. The level of malaria transmission is determined by the interactions between Plasmodium parasites, the Anopheles vectors and the human host. Understanding adult vector population dynamics by identifying the different species, their abundance, biting behaviour and entomological inoculation rates are important steps towards effective control of malaria, with vector abundance being a key determinant of malaria transmission force[11]. Potential reductions of the malaria burden in endemic and epidemic regions depend on the knowledge of malaria-transmitting mosquito species, populations and behavioral characteristics, and malaria exposure risks. In fact, in Côte d’Ivoire, entomological inoculation rates (EIR) of 158 and 339 infectious bites/ person/year were respectively observed in Korhogo, in the North region[12] and in Bouaké in the Center[13], mainly due to An. gambiae s.l. Similarly, in the mountainous West region, 289 and 303 infectious bites/ person/ night were recorded respectively in the localities of Gbatta and Gouin Houyé[4]. In the latter region, malaria transmission is ensured by two major vectors: An. gambiae s.l. and An. funestas s.l. Moreover, in 2002, the entomological inoculation rate (EIR) of 789 and 249 infectious bites/ person/ year were respectively observed in Yamoussoukro and Dimbokro in the central region[14], due to An, gambiae s.I. and An, funestas s.l. Finally, an entomological inoculation rate due to An. gambiae s.l. of6.2 infectious bites/ person/ year was observed in Allaba in southern Côte d’Ivoire[15]. So, the annual Entomological Inoculation Rate, which measures the exposure to P. falciparum-infected mosquitoes annually, was very heterogeneous across the country. To fight this disease, the National Malaria Control Program (NMCP) of Côte d’Ivoire periodically organizes, since 2008, nationwide distributions of LLINs to achieve 100% coverage and 80% utilization combined with a wider availability of RDTs and ACTs for the diagnosis, and treatment of malaria cases. Between 2013 and 2014, e.g., more than 14 million LLINs were distributed to the population (unpublished data from the NMCP). The massive distribution of these control methods recommended by the NMCP should act on the malaria transmission, reducing host-vector contact and human biting rate. To better understand the influence of these large-scale malaria control means on the level of vector transmission, an entomological survey was conducted in urban and rural settings from July 2015 to March 2016 in three regions of Côte d’Ivoire. In fact, this work is a study requested by NMCP after the first distribution campaign, in order to have the status of the situation at the time of the study. These data were used as the basis to follow the trends of the situation.

  Material & Methods Top

Study area

Mosquitoes were collected from three localities in urban area and rural settings: Korhogo (9° 27'28" N, 5° 37'46" W) in the northern savannah zone, Man (7° 2445" N, 7° 33Ί3" W) in the western forest zone and Abengourou (6° 43'46" N, 3° 29'47" W) in the eastern forest zone. These localities were chosen because they are part of the sentinel sites of the NMCP and therefore included in the malaria epidemiological surveillance programme. In addition, they are tourist and trade towns and therefore places with high human traffic and activity. Moreover, according to the NMCP, the coverage rate in these localities is over 80%. In fact, in Abengourou, 89,298 households were counted, 73,305 households had at least one LLIN and 207,630 LLINs were distributed, with a coverage rate of 82.09%. In the mountainous zone of Man, 83,660 households were counted, 78,142 households had at least one LLIN and 234,904 LLINs were distributed, suggesting a coverage rate of 93.45%. Finally, in the savannah zone of Korhogo, 198,679 households were counted and 163,302 LLINs were distributed with a coverage rate of 90%.

The northern zone is characterized by two seasons: one long rainy season (March–October) and a short dry season (November–February) with a mean annual temperature of 27°C and more than 1273 mm of water per year. The western and eastern zones are also characterized by two seasons: a long rainy season (March–November) and a short dry season (December–February). It has the mean temperature of 25°C and more than 1345 mm of water per year in these two sites. For a better appreciation of the realities of the field and a good interpretation of the results, two catch areas were chosen in each of the sentinel sites, one in an urban area and the other in a rural area. Thus, the neighborhoods of Logokaha (9° 27' 41" N, 5° 38' 19" W), Camp sea (7° 32' 48" N, 5° 32' 49" W) and H.K.B (6°43'46" N, 3°29'47" W) were chosen in urban area of Korhogo, Man and Abengourou, respectively. The villages of Kaforo, Kassiapleu (7°21’18» N, 7°48’47» W) and Assekro were chosen in rural areas of Korhogo, Man and Abengourou respectively [Figure 1].
Figure 1: Map of Cote d’Ivoire, showing the locations of the three study sites (the green and brown colors represent the forest and the savannah respectively).

Click here to view

Study design and adult mosquito sampling

Repeated cross-sectional surveys were carried out to conduct this study every three months. Although data were collected during four months of the year, we considered the climatic seasons (rainy and dry). Two entomological surveys were carried out during the short and long seasons of each climate. However, there is no statistical variation in any of the season sections and these data are sufficient to translate the whole year, hence the extrapolation of the data from the four months of collection for the whole year. Mosquito collections were undertaken using Human Landing Catches (HLC) from July 2015 to March 2016. During two consecutive nights (from 17:00 h to 08:00 h), HLCs were performed in three houses per community with one collector indoor and one outdoor selected household. Householders were asked to assist designated mosquito collectors in each community for two days per study site. These catches were done by two teams of volunteers (local residents). The first team worked from 17:00 h to midnight and the second from midnight to 8:00 h. The captured mosquitoes were grouped on an hourly basis per site and kept in separate sacks. Using this strategy, the Human Biting Rate (HBR) or Anopheles density per person per time unit (night) was estimated and used for the calculation of the entomological inoculation rates (EIR). All mosquitoes collected were placed in holding cups labelled by hour until they were processed for morphological identification.

Morphological identification of anopheles species and age-grading methods

After being differentiated at the level of genus as Culex, Anopheles, Aedes or Mansonia, Anopheles, mosquitoes were identified to species level using the taxonomy and identification key to female Afrotropical anophelines[16][17]. We dissected the ovaries of the females of Anopheles vectors (An. gambiae s.l. and An. funestus s.l.) and observed the degree of coiling of ovarian tracheoles to determine their parity status based on the ovary tracheation method of Dotinova[18]. All collected anopheline females were stored individually in Eppendorf tubes containing desiccant, labelled with the study site, point and date of collection, and stored at -20°C for further molecular analysis in the laboratory at the Institut Pierre Richet of Bouaké, Côte d’Ivoire.

Determination of sporozoite rates in An. gambiae s.l. and molecular identication of An. gambiae s.l. complex members

The anopheline mosquitoes collected were tested for the circumsporozoite (CSP) protein of Plasmodium falciparum using an Enzyme-Linked Immunosorbent Assay (ELISA). The head and thorax portion of each anopheles female were separated from the rest of the body. This portion was homogenized in blocking buffer (0.5% Casein, 0.1 N NaOH, 1 × PBS) and examined for the presence of Plasmodium falciparum CSP protein, using the method of Burkot et al.,[19] as modified by Wirtz et al.,[20], which is a reference technique for the detection of plasmodial species. All positive samples were extracted and disliked on new plates in subsequent tests for confirmation. Amosquito sample was considered positive if the optical density (OD) value was higher than twice the mean OD of 4 negative control wells (uninfected mosquitoes) on the ELISA plate. 90 specimens belonging to the An. gambiae s.l. siblings were further identified using molecular assays. DNA from the legs and wings of each individual specimen was extracted[21] and Polymerase Chain Reaction (PCR) was conducted to determine species[22].

Data processing and statistical analysis

Data were double entered into Microsoft Excel 2013 and transferred to STATA 14 (Stata Corp, College Station, TX, USA) for analysis. The human biting rate (HBR) (number of Anopheles per person and per night), Parous female percentages were calculated and the circumsporozoite protein (CSP) positive rate was calculated for each species in each setting. The CSP positive rate was calculated as the proportion of mosquitoes found to be positive for CSP. The EIR was defined as the Anopheles density by the CSP and estimated as the number of infectious bites per human per night. Data were analysed using STATA Statistics 14. Chi-square tests were used to compare different proportions and Kruskal-Wallis test was used to compare HBR. All tests were performed at the 5% significance level.

Ethical statement

This study received the approval of the National Research Ethics Committee of Côte d’Ivoire. This study also received an approval from health authorities of each locality. Permission was sought from households to perform collections in their rooms. In addition, community consent had been obtained beforehand in all the sites. The volunteer mosquito collectors gave their consent before participating in the study. They were also subjected to regular medical checkups with preventive malaria treatment in accordance with the recommendations of the NMCP of Côte d’Ivoire. They were all vaccinated against yellow fever.

  Results Top

Mosquitoes’ composition and anopheline fauna diversity

In total 11,490 mosquitoes were collected during the survey period by HLC. Five genera were recorded based on the morphological identification of the specimens, including 77.65% Anopheles spp, 14.43% Culex spp, 7.33% Mansonia spp, 0.58% Aedes spp. and 0.0001% Uranotaeniaspp [Table 1]. Overall, 8922Anopheles mosquitoes were morphologically identified, including 8467 An. gambiae s.l. and 338 An. funestus s.l. The remaining 1.02% (117) of the anopheline species were: An. pharoensis, An. coustani, An. ziemanni and An. wellcomei.
Table 1: Composition and abundance of mosquitoes in urban and rural settings of the three study sites from July 2015 to March 2016

Click here to view

An. gambiae s.l. was the predominant Anopheles species in all settings, both in urban and rural settings, and the only vector species identified in Korhogo (northern region) and in Abengourou (eastern region) while in rural Man (Kassiapleu), two malaria vectors were collected: An. gambiae s.l. and An. funestus s.l. analysis of An. gambiae s.l. siblings in each study sites revelated An. gambiae s.s. and An. coluzzii. In fact, An. coluzzii was predominant in the study sites except Korhogo, in the northen savannah where An. gambiae s.s. was most abundant. Thus, there were 90.32% An. gambiae s.s. and 9.68 An. coluzzii in Korhogo, 75% An. coluzzii and 25% An. gambiae s.s. in Man and finally 87.10%An. coluzzii and 12.90%An. gambiae s.s. in Abengourou [Figure 2]. Consequently An. coluzzii was the most abundant of the An. gambiae siblings collected by HLC in the study sites except Korhogo in the northern savannah where An. gambiae s.s. was abundant.
Figure 2: Distribution of members of Anopheles gambiae complex in the three study localities.

Click here to view

Biting behaviours and biting rates of malaria vectors

Estimates of the degree of endophagy and exophagy were obtained when relative proportions of vectors attempting to bite indoor and outdoor were compared. The results showed that the biting behaviour of malaria vectors was variable [Table 2]. In fact, in the urban settings, the anopheline populations feed both indoor and outdoor in Logokaha while they were exophagic in the two other neighbourhoods (Camp sea and HKB). In rural settings, the An, gambiae s.I. females in Kaforo feed both indoor and outdoor. The same behavior is observed in the village of Kassiapleu (Man). However, the An, gambiae s.I. populations remain exophagic in Assekro (Abengourou) as in urban setting. Otherwise, the An, funestas s.I. females, collected in the village of Kassiapleu (Man) were endophagic (57.73%). The HBR ofmalaria vectors was very high and varied according to species and localities [Table 3]. HLC gave an average biting rate of 26.36 An, gambiae s.I. bites per person per night in urban settings (39.08 b/p/n in Logokaha, 28.60 b/p/n in Camp sea and 11.40 b/p/n in H.K.B) and 32.44 b/p/n in rural settings (51.72 b/p/n in Kaforo, 25.92 in Kassiapleu and 19.67 b/p/n in Assekro) [Table 3]. In urban settings, Logokaha had the highest An, gambiae s.I. HBR with 39.08 b/p/n, compared to H.K.B (11.40 b/p/n, CI: 7.91-14.88, P <0.0001). However, this rate is comparable to that obtained from Camp sea, which was 28.60 b/p/n (CI: 18.62-38.59) (P=0.20). In Camp sea (Man), the second vector (An, funestas s.I.) showed a low density which is 0.39 b/p/n (IC: 0.16-0.63). In rural settings, An, gambiae s.I. appeared to be the predominant anopheline species in Kaforo, with a peak biting rate, of 51.72 b/p/n (CI: 37.18-66.28). The HBR of this malaria vector in this village is comparable to that obtained in Kassiapleu which was 25.92 b/p/n (CI: 19-32.67) (P=0.0883) and is higher than that observed in Assekro, which was 19.67 b/p/n (CI: 11.08-28.88, P=0.0024). Regarding An, funestas s.l., an average biting rate of6.60 b/p/n (CI: 3.0710.06) was recorded in Kassiapleu, rural setting of Man. The evolution of vector populations also varied according to seasons, with the highest biting rate recorded at the beginning of the rainy season (March) and in October for An, gambiae s.l. and An, funestas s.l.
Table 2: Biting behaviour of malaria vectors in urban and rural settings of the three study site from July 2015 to March 2016

Click here to view
Table 3: Trends of human biting rates with confidential interval in urban and rural sittings of An. gambiae in the study sites from July 2015 to March 2016

Click here to view

Parity rate (PR) and Infection rate (IR)

The ovaries examination of anophelines females permitted to determine a parity rate of malaria vectors in each setting and overall this rate is high, suggesting that the malaria vectors are aged. In fact, in urban settings, the PR of An, gambiae s.l was significantly higher in Logokaha (100%, n=1001) than in Camp sea (99.16%, n=713, CI: 98.21-99.32) and HKB (89.91%, n=426, CI: 87.0392.78) (P=0.004). The PR of An, funestus s.l. was 100% in Camp sea. In rural settings, the PR in Kaforo was 96.16% (n=860, CI: 94.88-97.45) for An, gambiae s.I. This rate for An, gambiae s.l. was lower to that obtained in Kassiapleu which was 98.97% (n=678, CI: 98.20-99.73) (P < 0.001) and higher to that obtained in Assekro which was 82.65% (n=461, CI: 79.18-86.12) (P < 0.001). The females of the second vector (An, funestus s.l.) met in Kassiapleu were all aged and able to transmit malaria.

A total of 3668 Anopheles mosquitoes (3502 An. gambiae s.l. and 166 An, funestus s.l.) was tested for Plasmodium infection using ELISA CSP and the IR of malaria vectors ranged from 0 to 7.7% [Table 4]. The P. falciparum IR for An. gambiae s.l. did not significantly vary between urban areas and was 1.7% in Logokaha, 4.2% of Camp sea and 2% in H.K.B (P=0.72). No infected An. funestus s.l. has been recorded in Camp sea. In rural areas, the P. falciparum IR for An. gambiae s.l. in Kaforo was 0.5%. This rate for An. gambiae s.l. is lower than those obtained in Kassiapleu and Assekro which were respectively 5.1% and 6.4% (P=0.325). This IR of An. gambiae s.l. observed in Kassiapleu was 7.7%.
Table 4: Number of mosquitoes tested and infection rates of malaria vectors in the three study sites from July 2015 to March 2016

Click here to view

Contribution of malaria vectors to transmission expressed in terms of the EIR

The annual EIR for each malaria species and locality is presented in [Table 5]. According to this study, the biting and sporozoite rates recorded indicate that An. gambiae s.l. and An. gambiae s.l. were all vectors of P. falciparum in the study settings, although their relative importance varied with the setting. In urban settings, the annual EIR for An. gambiae s.I. was 2-fold higher in Logokaha (242.49 infected bites per person per year) than in H.K.B (83.22 ib/p/y) and lower than that obtained in Camp sea (438.44 ib/p/y). In rural settings, the annual EIR for An. gambiae s.l. was 94.90 ib/p/y in Kaforo, 482.5 ib/p/y in Kassiapleu and 459.42 ib/p/y in Assekro. However, in Kassiapleu, the annual EIR for An, funestas s.l was 186.15 ib/p/y. Overall, inhabitants receive more infected bites per year in the settings except in urban H.K.B (urban Abengourou) and in rural Kaforo (rural Korhogo) where the inhabitants are lowly exposed to Plasmodium-infected Anopheles bites. Taken together, these data indicate that An, gambiae s.l. was responsible for most of the transmission of P falciparum parasites in the settings, even if An. funestas s.l. was also involved in malaria transmission in Kassiapleu (Man).
Table 5: Entomological inoculation rates in urban and rural settings in the three study sites from July 2015 to March 2016

Click here to view

  Discussion Top

The reduction of the malaria burden in endemic and epidemic regions mainly depends on the knowledge of malaria-transmitting mosquito species, populations and behavioural characteristics, as well as malaria exposure risks. The LLINs were scaled-up to prevent malaria transmission in Côte d’Ivoire. The present study carried out in urban and rural settings aimed to better understand the influence of mass distribution of LLINs on vector transmission of malaria in three regions of Côte d’Ivoire. In this study, we have highlighted the relative diversity and abundance of Anopheles mosquitoes in three regions of Côte d’Ivoire and assessed their implications in malaria transmission to local communities. Our results have shown that An. gambiae s.l. was most the abundant vector of malaria in the three regions[6],[14],[23],[24]. An. gambiae s.l. and An. funestus s.l. were captured all year round and constituted more than 77% of the anopheline fauna. Their occurrence confirms an earlier study by Doucet et al.,[25] and those of some other authors[14], [24], [26]. Moreover, An. gambiae s.l. was the predominant species in all study sites. 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 any species. Indeed, permanent water courses, puddles and small dams are probably abundant in these areas. In addition, we found that malaria vectors collected, exhibited high parity rates in all regions, thus suggesting that a significant proportion of the local vector population 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[14]. In this study, no An, nili species has been identified. This is explained by the rarity of the characteristic lodgings of this species. According to a recent study in Côte d’Ivoire, the preferential lodgings of this species are the rivers[4]. The larval biology of this species is already described in the basic book of Gillies et De Meillon[16].

Analysis by PCR of the members of An. gambiae s.l. complex has shown that An. coluzzii was the dominant species in forest area of Côte d’Ivoire, whilst An . gambiae s.s. was the dominant species in the savannah. The relative dominance of these two species may be associated with specific and characteristic breeding sites. The presence of An, gambiae s.s. and An, coluzzii has been previously reported in Côte d’Ivoire[5][6]. The abundance of An, coluzzii in our samples from forest areas could be related to the type of breeding sites and the climatic conditions in these study sites[31]–32. Several studies carried out in Côte d’Ivoire have shown a predominance of An. coluzzii in forest area[6], [14]. Therefore, An. gambiae s.s. was most abundant in the northern region. This result is similar to that obtained by several other authors[27][28] in the same region, suggesting that environmental conditions in savannah zones are unfavorable for the reproduction and the survival of An. coluzzii. This is in-line with observations made by other studies[29],[30] which report that these molecular forms are cohesive and constitute exclusive taxonomic groups across their shared range. An. coluzzii is more adapted to urbanized and polluted environments[31] and environments having high salinity rates[32], while An. gambiae s.s. seems predominant in semi-urban, rural and arid environments.

In our study settings, malaria vectors were frequently caught outdoors in Camp sea, H.K.B and Assekro, suggesting an important role of LLINs in this exophagic behavior. These observations were recently made by Assouho et al.,[6] in the major districts of Côte d’Ivoire. Indeed, several studies in rural eastern Sudan[34], Benin35 and Senegal[36] have reported an exophagic behavior of malaria vectors following the introduction of LLINs. In fact, a recent study in Benin also showed that one year after universal coverage, the exophagic rate increased from 45 to 68.1%[37]. The massive introduction of LLINs could, therefore, induce a modification of the biting behavior of malaria vectors. However,An. funestus s.l. species in rural Man (Kassiapleu), were exclusively endophagic with a high biting rate despite the presence of LLINs in houses. This could be due to their high resistance to pyrethroid insecticides used to treat LLINs but also raises questions about the current use of LLINs by the populations to avoid the bites of mosquito vectors and to prevent malaria. Nevertheless, in Logokaha, Kaforo and Assekro, malaria vectors feed both indoor and outdoor, thus reflecting the start of a change in vector behaviour.

Our improved understanding of 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. and An. funestas s.l. were tested using the ELISA CSP method for the presence of P. falciparum sporozoites. The finding showed that the two species were involved in malaria transmission in Man, while An. gambiae s.l. being the main malaria vector in all regions. Although infection rates were almost similar between study sites, the intensity of transmission was very heterogeneous and this study revealed relatively high parity rates of female Anopheles (≥ 82%) in the study areas[33]. These variations underline the great variability of parity rates observed sometimes between study sites, and within the same site depending on the species density dynamics. The heterogeneity of malaria transmission observed in the present study is consistent with a recent study[6]. This may also be the effect of differences in intervention strategies coordinated by the National Malaria Control Program (NMCP), especially free distribution of LLINs to vulnerable populations and the use of ACTs for the early treatment of malaria cases. An. gambiae s.l. and An. funestas s.l. are efficient vectors of P. falciparum both in urban and rural settings of Côte d’Ivoire. Although, the intensity of transmission was very heterogeneous. In urban settings malaria transmission was higher in Logokaha and in Camp sea than in H.K.B. It is clear that LLINs have a beneficial effect on the population in the H.K.B neighborhood by reducing the level of malaria transmission. However, this reduction was not sufficient to eliminate the risk of infection of the city dwellers. In rural areas, malaria transmission remains relatively high in both western and eastern regions, but it remains relatively low in northern region. This result is consistent with the findings of Fofana in two villages of the southern region of Côte d’Ivoire[38] and in Benin[39]. This high transmission of malaria could be due to the high infection rate of malaria vectors and could be the result of relatively high parity rates recorded during this study[33], therefore malaria control interventions should be strengthened to reduce transmission and for the future elimination of malaria. Moreover, high sporozoite infection and parity rates were recorded in all three regions and highlighted the high transmission of malaria within local populations. These findings suggest that either the distributed LLINs are not being used properly by the populations or the local vector populations are developing resistance to the insecticide use in the LLINs.

Between the two species recorded, An. gambiae s.l. was responsible for most malaria transmission with An. funestus playing a secondary vector role. A similar observation was reported in a savannah area in the central regions of the Côte d’Ivoire[14]. By contrast, in a village of northern region (Kaforo), the infection rate was low. This result is consistent with the findings of Fofana et al.,[38] in two villages of the southern region of Côte d’Ivoire and in Benin[39].

  Conclusion Top

The present study showed that malaria transmission remains high and heterogeneous across Côte d’Ivoire, despite repeated mass distribution of LLINs. It is also found that in Man (Western region), two vectors are involved while only one is involved in Korhogo (Northern region) and in Abengourou (Eastern region) in the transmission. Malaria transmission is very high in rural settings except Kaforo (Korhogo) where the EIR remained low. In urban settings, malaria transmission is high. In addition, malaria vectors variously observed biting behaviour, which could be a consequence of mass distribution of LLINs by the National Malaria Control Program. The results underscore that these behaviours should be considered in the development of complementary control strategies in both rural and urban settings to effectively control this disease. Indeed, taking into account these results, which show that malaria vector populations feed both indoors and outdoors in urban and rural areas, it would be interesting to combine indoor residual spraying with current control. In addition, outdoor control tools (automatic insecticide dispenser, fumigation) need to be tested as current tools only to target indoor vectors.

Given the high level of transmission in the sampled localities, continued and intensified sensitisation is necessary to increase the use of LLINs. Other means such as indoor residual spraying should also be combined with the currently used LLINs.

Conflict of interest: None

  Acknowledgements Top

The authors would like to thank the Coordination of the National Malaria Control Program of Côte d’Ivoire, global fund to fight AIDS, tuberculosis and malaria, study site populations and health authorities for assistance in field surveys.

  References Top

OMS. Rapport sur le paludisme dans le monde 2015. 2016: 32  Back to cited text no. 1
PNLP. Rapport de la campagne nationale de distribution de moustiquaires imprégnées d’insecticide à longue durée d’action en 2011, Programme National de Lutte contre le Paludisme, Ministère de la Santé et de l’Hygiène Publique. République de Cote d’Ivoire 2011; 47.  Back to cited text no. 2
Dossou-Yovo J. Etude éthologique des moustiques vecteurs du paludisme en rapport avec les aspects parasitologiques de la transmission du Plasmodium dans la région de Bouaké. These de Doctorat d’Etat en Entomologie Medicale, Université de Cocody, Abidjan 2000.  Back to cited text no. 3
Adja A, N’goran K, Kengne P, Koudou G, Toure M, Koffi A, et al. Transmission vectorielle du paludisme en savane arboree a Ganse, en Cote d’Ivoire. Médecine Tropicale 2006; 66(5): 44955.  Back to cited text no. 4
Tia E, Chouaibou M, Gbalégba C, Boby A, Koné M, Kadjo A. Distribution des espèces et de la fréquence du gène Kdr chez les populations d’Anopheles gambiae ss et d’Anopheles coluzzii dans cinq sites agricoles de la Côte d’Ivoire. Bulletin de la Société de Pathologie Exotique 2017; 110(2): 130-4.  Back to cited text no. 5
Assouho KF, Adja AM, Guindo-Coulibaly N, Tia E, Kouadio A, Zoh DD, et al. Vectorial Transmission of Malaria in Major Districts of Côte d’Ivoire. Journal of Medical Entomology 2020; 57(3): 908–914.  Back to cited text no. 6
Altizer S, Dobson A, Hosseini P, Hudson P, Pascual M, Rohani P. Seasonality and the dynamics of infectious diseases. Ecology Letters 2006; 9(4): 467–84.  Back to cited text no. 7
Nmor JC, Sunahara T, Goto K, Futami K, Sonye G, Akweywa P, et al. Topographic models for predicting malaria vector breeding habitats: potential tools for vector control managers. Parasites & Vectors 2013; 6(1): 14.  Back to cited text no. 8
Minakawa N, Munga S, Atieli F, Mushinzimana E, Zhou G, Githeko AK, et al. Spatial distribution of anopheline larval habitats in Western Kenyan highlands: effects of land cover types and topography. The American Journal of Tropical Medicine and Hygiene 2005; 73(1): 157–65.  Back to cited text no. 9
Minakawa N, Omukunda E, Zhou G, Githeko A, Yan G. Malaria vector productivity in relation to the highland environment in Kenya. The American Journal of Tropical Medicine and Hygiene 2006; 75(3): 448–53.  Back to cited text no. 10
Garrett-Jones C. The human blood index of malaria vectors in relation to epidemiological assessment. Bulletin of the World Health Organization 1964; 30(2): 241.  Back to cited text no. 11
Henry MC, Rogier C, Nzeyimana I, Assi S, Dossou-Yovo J, Audibert M, et al. Inland valley rice production systems and malaria infection and disease in the savannah of Cote d’Ivoire. Tropical Medicine & International Health 2003; 8(5): 449-58.  Back to cited text no. 12
Dossou-Yovo J, Doannio J, Riviere F, Chauvancy G. Malaria in Côte d’Ivoire wet savannah region: the entomological input. Tropical medicine and parasitology: official organ of Deutsche Tropenmedizinische Gesellschaft and of Deutsche Gesellschaft fur Technische Zusammenarbeit (GTZ) 1995; 46(4): 263–9.  Back to cited text no. 13
Koudou B, Adja A, Matthys B, Doumbia M, Cissé G, Koné M, et al. Pratiques agricoles et transmission du paludisme dans deux zones éco-épidémiologiques au centre de la Côte d’Ivoire. Bull Soc Pathol Exot 2007; 100(2): 124–6.  Back to cited text no. 14
Fofana D, Konan KL, Djohan V, Konan YL, Koné AB, Doannio JMC, et al. Diversité spécifique et nuisance culicidienne dans les villages de N’gatty et d’Allaba en milieu côtier lagunaire de Côte-d’Ivoire. Bulletin de la Société de pathologie exotique 2010; 103(5): 333–9.  Back to cited text no. 15
Gillies MT, De Meillon B. The Anophelinae of Africa south of the Sahara (Ethiopian zoogeographical region). 1968; pp. 343.  Back to cited text no. 16
Gillies M, Coetzee M. A supplement to the Anophelinae of Africa south of the Sahara (Afrotropical region) 1987.  Back to cited text no. 17
Dotinova. Méthode à appliquer pour classer par groupe d’âge les diptères présentant une importance médicale 1960; 220p.  Back to cited text no. 18
Burkot T, Williams J, Schneider I. Identification of Plasmodium falciparum-infected mosquitoes by a double antibody enzyme-linked immunosorbent assay. The American Journal of Tropical Medicine and Hygiene 1984; 33(5): 783–8.  Back to cited text no. 19
Wirtz R, Burkot T, Graves P, Andre R. Field evaluation of enzyme-linked immunosorbent assays for Plasmodium falciparum and Plasmodium vivax sporozoites in mosquitoes (Diptera: Culicidae) from Papua New Guinea. Journal of Medical Entomology 1987; 24(4): 433–7.  Back to cited text no. 20
Collins FH, Mendez MA, Rasmussen MO, Mehaffey PC, Besansky NJ, Finnerty V. A ribosomal RNA gene probe differentiates member species of the Anopheles gambiae complex. The American Journal of Tropical Medicine and Hygiene 1987; 37(1): 37–41.  Back to cited text no. 21
Favia G, Lanfrancotti A, Spanos L, Sidén-Kiamos I, Louis C. Molecular characterization of ribosomal DNA polymorphisms discriminating among chromosomal forms of Anopheles gambiae ss. Insect Molecular Biology 2001; 10(1): 19–23.  Back to cited text no. 22
Doannio J, Dossou-Yovo J, Diarrassouba S, Rakotondraibe M, Chauvancy G, Rivière F. Comparaison de la composition spécifique et de la dynamique des populations de moustiques dans deux villages du centre de la Côte-d’Ivoire, avec et sans périmetre de riziculture irriguée. Bull Soc Pathol Exot 2006; 99(3): 204–6.  Back to cited text no. 23
Adja AM, Assare KR, Assi SB, N’Dri L, Yapi A, Ngoran KE. Etude du comportement au repos et des preferences trophiques de Anopheles gambiae dans la ville d’adzope, cote d’ivoire. European Scientific Journal 2015; 11 (3).  Back to cited text no. 24
Doucet J, Adam JP, Binson G. Mosquitoes of the Ivory Coast. Annales de Parasitologie Humaine et Comparee 1960; 35(3): 391–408.  Back to cited text no. 25
Adja A, N’goran E, Koudou B, Dia I, Kengne P, Fontenille D, et al. Contribution of Anopheles funestus, An. gambiae and An. nili (Diptera: Culicidae) to the perennial malaria transmission in the southern and western forest areas of Cote d’Ivoire. Annals of Tropical Medicine & Parasitology 2011; 105(1): 13–24.  Back to cited text no. 26
Touré M, Carnevale P, Chandre F. Impact retardé des moustiquaires imprégnées de lambdacyhalothrine sur la fréquence de la mutation kdr chez Anopheles gambiae ss (Diptera: Culicidae) au nord de la Côte-d’Ivoire. Bulletin de La Société de Pathologie Exotique 2012; 1–6.  Back to cited text no. 27
Zogo B, Soma DD, Tchiekoi BNC, Somé A, Alou LPA, Koffi AA, et al. Anopheles bionomics, insecticide resistance mechanisms, and malaria transmission in the Korhogo area, northern Côte d’Ivoire: a pre-intervention study. Parasite 2019; 26: 40  Back to cited text no. 28
Fanello C, Santolamazza F, Della Torre A. Simultaneous identification of species and molecular forms of the Anopheles gambiae complex by PCR-RFLP. Medical and Veterinary Entomology 2002; 16(4): 461–4.  Back to cited text no. 29
De Queiroz K. Species concepts and species delimitation. Systematic Biology 2007; 56(6): 879–86.  Back to cited text no. 30
Kudom AA. Larval ecology of Anopheles coluzzii in Cape Coast, Ghana: water quality, nature of habitat and implication for larval control. Malaria Journal 2015; 14(1): 447.  Back to cited text no. 31
Tene Fossog B, Ayala D, Acevedo P, Kengne P, Ngomo Abeso Mebuy I, Makanga B, et al. Habitat segregation and ecological character displacement in cryptic African malaria mosquitoes. Evolutionary Applications 2015; 8(4): 326–45.  Back to cited text no. 32
Amvongo-Adjia N, Wirsiy EL, Riveron JM, Ndongmo WPC, Enyong PA, Njiokou F, et al. Bionomics and vectorial role of anophelines in wetlands along the volcanic chain of Cameroon. Parasites & Vectors 2018; 11(1): 471.  Back to cited text no. 33
Hamad AA, Abd El Hamid DN, Arnot DE, Giha HA, Abdel-Muhsin A-MA, Satti GM, et al. A marked seasonality of malaria transmsission in two rural sites in eastern Sudan. Acta Tropica 2002; 83(1): 71–82.  Back to cited text no. 34
Corbel V, N’Guessan R. Distribution, mechanisms, impact and management of insecticide resistance in malaria vectors: a pragmatic review. Anopheles mosquitoes-New insights into malaria vectors 2013.  Back to cited text no. 35
Ndiath MO, Mazenot C, Sokhna C, Trape JF. How the malaria vector Anopheles gambiae adapts to the use of insecticide-treated nets by African populations. PLoS One 2014; 9(6): e97700.  Back to cited text no. 36
Moiroux N, Bio Bangana A, Djènontin A, Chandre F, Corbel V, Guis H. Modeling the spatio-temporal distribution of M and S molecular forms of Anopheles gambiae and Anopheles funestus in south Benin. European Society for Vector Ecology 2012.  Back to cited text no. 37
Fofana D, Konan K, Djohan V, Konan Y, Koné A, Doannio J, et al. Diversité spécifique et nuisance culicidienne dans les villages de N’gatty et d’Allaba en milieu côtier lagunaire de Côte-d’Ivoire. Bulletin de la Société de Pathologie Exotique 2010; 103(5): 333–9.  Back to cited text no. 38
Akogbeto M, Chippaux J-P, Coluzzi M. Le paludisme urbain côtier à Cotonou (République du Bénin): Étude Entomologique. Revue d’Epidémiologie et Santé Publique 1992; 40: 233–9.  Back to cited text no. 39


  [Figure 1], [Figure 2]

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]


    Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
    Access Statistics
    Email Alert *
    Add to My List *
* Registration required (free)  

  In this article
Material & Methods
Material & Methods
Article Figures
Article Tables

 Article Access Statistics
    PDF Downloaded79    
    Comments [Add]    

Recommend this journal