Kouassi et al.

Malaria Journal 2023, 22(1):14 Malaria Journal

https://doi.org/10.1186/s12936-023-04439-z

RESEARCH Open Access

Entomological monitoring data

driving decision‑making for appropriate
and sustainable malaria vector control in Côte
d’Ivoire
Bernard Loukou Kouassi1, Constant Edi2, Allassane Foungoye Ouattara2, Armand Kouassi Ekra2,
Louise Golou Bellai2, Janice Gouaméné2, Yves Alain Kadio Kacou2, Jackson Koffi Ives Kouamé2,
Armel‑Hermann Obo Béké2, Firmain N’Dri Yokoli2, Constant Guy N’Guessan Gbalegba1,6, Emmanuel Tia3,
Roseline Monsan Yapo3, Lucien Yao Konan4, Roméo N’Tamon N’Tamon4, Maurice Adja Akré5,
Alphonsine Amanan Koffi5, Antoine Mea Tanoh6, Pascal Zinzindohoué7, Blaise Kouadio7,
Patricia L. Yepassis‑Zembrou8, Allison Belemvire9, Seth R. Irish10, Ndombour Gning Cissé1,
Cecilia Flatley11 and Joseph Chabi11*

Abstract
Background Entomological surveillance provides critical information on vectors for appropriate malaria vector con‑
trol and strategic decision-making. The widely documented insecticide resistance of malaria vectors in Côte d’Ivoire
requires that any vector control intervention deployment be driven by entomological data to optimize its effective‑
ness and appropriate resource allocations.
To achieve this goal, this study documents the results of monthly vector surveillance and insecticide susceptibility
tests conducted in 2019 and a review of all previous entomological monitoring data used to guide vector control
decision making. Furthermore, susceptibility to pirimiphos-methyl and clothianidin was assessed in addition to
chlorfenapyr and pyrethroids (intensity and piperonyl butoxide (PBO) synergism) tests previously reported. Vector
bionomic data were conducted monthly in four sites (Sakassou, Béoumi, Dabakala and Nassian) that were selected
based on their reported high malaria incidence. Adult mosquitoes were collected using human landing catches
(HLCs), pyrethrum spray catches (PSCs), and human-baited CDC light traps to assess vector density, behaviour, species
composition and sporozoite infectivity.
Results Pirimiphos-methyl and clothianidin susceptibility was observed in 8 and 10 sites, respectively, while previous
data reported chlorfenapyr (200 µg/bottle) susceptibility in 13 of the sites, high pyrethroid resistance intensity and
increased mortality with PBO pre-exposure at all 17 tested sites.
Anopheles gambiae sensu lato was the predominant malaria vector collected in all four bionomic sites. Vector den‑
sity was relatively higher in Sakassou throughout the year with mean biting rates of 278.2 bites per person per night
(b/p/n) compared to Béoumi, Dabakala and Nassian (mean of 48.5, 81.4 and 26.6 b/p/n, respectively). The mean

*Correspondence:
Joseph Chabi
Joseph_Chabi@pmivectorlink.com
Full list of author information is available at the end of the article

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Kouassi et al. Malaria Journal 2023, 22(1):14 Page 2 of 15

entomological inoculation rate (EIR) was 4.44 infective bites per person per night (ib/p/n) in Sakassou, 0.34 ib/p/n
in Beoumi, 1.17 ib/p/n in Dabakala and 1.02 ib/p/n in Nassian. The highest EIRs were recorded in October in Béoumi
(1.71 ib/p/n) and Nassian (3.22 ib/p/n), in July in Dabakala (4.46 ib/p/n) and in May in Sakassou (15.6 ib/p/n).
Conclusion Based on all results and data review, the National Malaria Control Programme developed and imple‑
mented a stratified insecticide-treated net (ITN) mass distribution in 2021 considering new generation ITNs. These
results also supported the selection of clothianidin-based products and an optimal spraying time for the first indoor
residual spraying (IRS) campaign in Sakassou and Nassian in 2020.
Keywords Malaria, Anopheles gambiae, Insecticide resistance monitoring, Vector bionomics, ITNs, IRS, Decision-
making, Côte d’Ivoire

Background control strategies [5]. Furthermore, the effectiveness of

Malaria is one of the most important diseases of pov- vector control interventions depends on accurate infor-
erty and its public health relevance, particularly in sub- mation regarding distribution and abundance of the main
Saharan Africa, is still a concern [1]. It remains a primary vector species and their resistance to insecticides [6–10],
cause of illness and deaths worldwide, with 84 countries and this data can only be produced through entomologi-
around the world reporting malaria cases and deaths in cal monitoring. In most endemic countries, the spread
2021 [2]. However, significant progress has been made of vectors resistant to the insecticides used in ITNs and
over the past 20 years resulting in a reduction of malaria IRS has been widely reported as the outcomes of long-
prevalence by 50%, with reports dropping to 232 million term use of the same class of insecticide in public health
cases in 2019, though the recent COVID-19 pandemic vector control [6–10] in addition to the unregulated use
has impacted the gain with increasing cases to 245 mil- of pesticides in agriculture [11, 12]. This requires timely
lion and 247 million observed in 2020 and 2021 respec- and close monitoring of the vectors following WHO rec-
tively. Nonetheless, there was a decreasing number of ommendations whilst new insecticides and products are
deaths worldwide due to malaria following reports of becoming available.
619,000 deaths in 2021 compared to 625,000 deaths in Furthermore, potential malaria transmission within a
2020 [2]. country is often heterogeneous and differs significantly
Preventive measures are the most effective and com- from one location to another due to the eco-geographi-
monly prioritized control methods recommended by cal position of sites. Important bionomics traits such as
the World Health Organization (WHO) for malaria vector species composition, biting time, biting behav-
control. Insecticide-based vector control still represents iour, host preference, and resting behaviours should be
the main control method, which has enabled the reduc- known for all the principal malaria vectors and assessed
tion of malaria burden over the last two decades [1, 3]. over time to detect any seasonal or other environmental
Insecticide-treated nets (ITNs) and indoor residual changes that could affect the effectiveness of interven-
spraying (IRS), represent the core vector control inter- tions [13].
ventions for malaria prevention and their widespread use In Côte d’Ivoire, malaria remains a major public health
has resulted in significant decreases in malaria morbidity problem with a general population incidence of 441
and mortality [1, 3]. Entomological surveillance is con- malaria cases per thousand inhabitants and morbidity of
ducted to ensure optimal deployment of these interven- about 173 deaths per thousand in 2020 among the chil-
tions, and to guide insecticide resistance management dren under 5 years old [14]. Anopheles gambiae sensu
strategies. Five “pillars” have been proposed by the WHO lato (s.l.), Anopheles funestus s.l. and Anopheles nili are
to support and orient malaria endemic countries on the three major malaria vectors in the country [15, 16],
insecticide resistance management [4]. According to the with An. gambiae s.l. being the main vector across the
WHO, all National Malaria Control Programme (NMCP) country. The annual entomological inoculation rate (EIR)
and stakeholder decisions must be strategically linked was also heterogeneous across the country and ranged
to entomological surveillance activities to inform vec- between 6 and 789 Plasmodium falciparum-infected
tor control planning and implementation and to ensure bites per person per year [15, 17, 18]. Plasmodium falci-
that appropriate interventions are being used where they parum was responsible for about 99% of the uncompli-
should be. cated and severe malaria cases, followed by Plasmodium
A greater emphasis was put on strengthening national malariae [14].
capacities to generate, analyse and use high quality ento- The country is known as one of the areas hosting highly
mological surveillance data to maximize impact of vector resistant malaria vector populations. This has been
Kouassi et al. Malaria Journal 2023, 22(1):14 Page 3 of 15

confirmed in a section of this project by Kouassi et al. the centre considered as a transitional zone between the
[19], reporting the resistance status and intensity of An. South and the North, a sub-Sudanese savannah zone, and
gambiae s.l. in about 15 sites selected across the country. a Sudanese savannah zone both in the northern part of
Furthermore, previous studies had also highlighted the the country. The climate in the South is equatorial, with
same trends in different parts of the Côte d’Ivoire, with annual rainfall between 2100 mm and 2500 mm and
several resistance mechanisms involved in the resistance sub-equatorial in the western forest with average rainfall
of the vector populations [20–24]. between 1600 mm and 2300 mm per year. In the central
This level of resistance was certainly affecting efforts transitional zone, the climate is tropical, with an average
that the country was making to increase the access to of 1200 mm rainfall per year. The climate is also tropi-
insecticide-based vector control interventions. Cur- cal in the northern sub-Sudan and Sudan zones, with an
rent strategies for malaria vector control in Côte d’Ivoire annual average rainfall of 900 mm [Société d’Exploitation
are universal mass ITN distribution every three years, et de Développement Aéroportuaire, Aéronautique et
routine distribution of ITNs to pregnant women dur- Météorologique (SODEXAM)]. Insecticide resistance
ing their first antenatal care visit, to children under one data review was conducted in a total of 17 sites distrib-
year of age during immunization visits and to children uted across the country including the 15 sites reported
between one and five years of age during health consul- by Kouassi et al. in 2020 [16] and the sites of Bocanda
tations. It is important to note that only pyrethroid-only and Jacqueville where data was available. The longitudi-
ITNs had been distributed in Côte d’Ivoire prior to 2021, nal monitoring surveys were carried out in four of these
and no efforts were made to correlate ITN distributions sites including Nassian, Sakassou Beoumi and Dabakala
and malaria vector resistance in each of the recipient (Fig. 1). Four houses were selected in each district to
districts, while the effectiveness of vector control using serve as mosquito collection houses and used throughout
pyrethroid treated tools is now being threatened by the the collection period.
spread of insecticide resistance, coupled with vector
behaviour such as increase in outdoor biting or daytime WHO insecticide susceptibility tests
biting [6, 7, 25, 26]. Insecticide susceptibility tests were conducted between
Supported by the U.S. President’s Malaria Initia- June and September 2019 on 2–5-day old adult female
tive (PMI), and by the Global Fund, the NMCP of Côte An. gambiae s.l. reared from field collected larvae from
d’Ivoire through its 2016–2020 malaria national strategic each of the surveyed site. Various larval habitats were
plan (NSP) opted for new approaches to malaria control surveyed within each of the sites and, collected larvae
[27]. Therefore, the NMCP decided, based on entomo- were pooled and reared to adults at a field laboratory. The
logical evidence, to introduce new types of ITNs incor- resistance status of the local vectors against the diagnos-
porating either synergist or dual active ingredients for tic concentrations of permethrin (0.75%), deltamethrin
mass and routine distribution and implement targeted (0.05%), alpha-cypermethrin (0.05%) and pirimiphos-
IRS within the country. Due to the widely reported insec- methyl (0.25%) was determined using WHO tube tests
ticide resistance of the vectors and the heterogeneity of [28]. When resistance was confirmed, the intensity of
malaria endemicity in Côte d’Ivoire, it was important to resistance at 5 and 10 times the diagnostic concentra-
use entomological data for intervention decision making tion of each insecticide and synergism using 4% pipero-
to ensure appropriate allocation of resources and opti- nyl butoxide (PBO) with one hour pre-exposure and
mize the effectiveness of these interventions and ulti- pyrethroids, were conducted to assess the level of resist-
mately increase impact on malaria vectors. ance and implication of mono-oxygenase enzymes using
This study presents entomological baseline data collec- WHO tube tests [28].
tions including monthly vector surveillance and annual Additionally, clothianidin papers were treated locally at
insecticide susceptibility tests conducted in 2019 in addi- a dose of 2% using 264 mg of a formulated SumiShield
tion to literature review of all previous entomological product diluted in 20 ml of distilled water. Two millili-
monitoring data to guide ITN selection for mass distribu- tres of the solution were used to impregnate a 12 × 15 cm
tion and IRS implementation within the country in 2020. Whatman filter paper grade 1. The treated papers were
dried overnight and preserved in aluminum foil at 4˚C
Methods before testing is conducted. The susceptibility testing
Study sites was conducted as described above, and the mortality
Côte d’Ivoire is a coastal country divided into five dif- was recorded every 24 h, up to seven days post-exposure.
ferent geographical zones including an evergreen for- CDC bottle assays were used to evaluate the susceptibil-
est zone in the south and costal part of the country, a ity of the vectors to chlorfenapyr at two doses (100 µg a.i/
deciduous forest zone, a forest/savanna mosaic zone in bottle and 200 µg a.i/bottle when resistance was observed
Kouassi et al. Malaria Journal 2023, 22(1):14 Page 4 of 15

Fig. 1 Map of the entomological monitoring sites

to 100 µg a.i/bottle) with mortality recorded up to 72 h 6:00 p.m. to 6:00 a.m. The PSCs were conducted in 30
[29]. Testing conditions were recorded at the start and houses per site per month between 6:00 a.m. and 8:00
end of the test with an average temperature of 25ºC a.m. For houses with open eaves, collectors sprayed from
(± 2 ºC). the outside through the eaves before entering and spray-
ing indoors and all mosquitoes knocked down were col-
Adult mosquito collection lected from the white sheets and placed into Petri dishes.
Adult mosquitoes were collected monthly from January The same houses were maintained for HLC and CDC
to December 2019 in Sakassou (12 months) and from light trap collections throughout the longitudinal moni-
May to December 2019 (8 months) in Nassian, Dabakala toring period, while PSC collections were conducted in
and Beoumi, using human landing catches (HLC), pyre- randomly selected houses, depending on the availability
thrum spraying catches (PSC), and CDC light trap collec- of households. All Anopheles mosquitoes collected were
tion methods. The longitudinal monitoring started later morphologically identified using the key of Gillies and
in Nassian, Dabakala, and Beoumi compared to Sakassou Coetzee [30] and the potential vectors such as An. gam-
due to change of initially selected sites which included biae s.l., An. funestus s.l. and An. nili were individually
Gagnoa, Jacqueville, and Bocanda. preserved in Eppendorf tubes containing silica gel desic-
HLCs were conducted indoors and outdoors in four cant for further laboratory analyses.
houses per site during two consecutive nights per month
to collect adult mosquitoes landing on human baits. The Species identification and sporozoite infection detection
human-baited CDC light trap collections were performed of malaria vectors
in four different houses from HLCs during two consecu- In the four longitudinal monitoring sites, a subsample
tive nights per site per month. CDC light traps were sus- of about 80 samples of the preserved vectors was ran-
pended indoors where people slept under a treated ITN domly selected per month to determine subspecies of
(received from mass ITN distribution campaign) from An. gambiae s.l. and P. falciparum sporozoite infection.
Kouassi et al. Malaria Journal 2023, 22(1):14 Page 5 of 15

The DNA of each individual mosquito was extracted chlorfenapyr and 7 days for clothianidin. Mortality of
using the protocol designed by Collins et al. [31]. Anoph- less than 90% was considered as “confirmed resistance”,
eles gambiae complex species were identified follow- between 90 and 98% as “possible resistance”, and 98%
ing the Short-Interspersed Element protocol described and greater as “susceptible”. The mean human biting rate
by Santolamazza et al. [32]. The sporozoite infection of (HBR) and entomological inoculation rate (EIR) was cal-
a subsample of An. gambiae s.l. and An. funestus s.l. col- culated using the average of all collection-months per
lected by HLC from each site was determined using site. The Kruskal–Wallis equality of population rank test
the enzyme-linked immunosorbent assay protocol for was used to compare the mean HBR and EIR between the
identification of P. falciparum circumsporozoite infec- four different sites. All differences were considered sig-
tion [33] and all positive mosquitoes were retested for nificant at P < 0.05.
confirmation.
Results
Malaria epidemiological data of Sakassou and Nassian WHO susceptibility test, intensity, and synergist assays
To overlap the entomological monitoring data and the Kouassi et al. [19] had already reported high pyrethroid
epidemiological data over the year for a more robust resistance at 15 sites tested and a substantial increase
decision-making process, the number of rapid diagnos- in vector mortality after pre-exposure to PBO. In addi-
tics tested (RDT) malaria cases from the previous two tion to those sites, high resistance intensity was also
years (2017 and 2018) were collected through the country recorded against pyrethroid insecticides in Bocanda and
health information management system (HIMS) data as Jacqueville, and pre-exposure to PBO increased vector
monthly reported cases to provide estimates of the num- mortality when exposed to deltamethrin, alpha-cyperme-
ber of confirmed cases and periodicity throughout the thrin, and permethrin as observed in the other reported
year to estimate the peak of malaria incidences at each sites [19].
site. However, the 2019 HMIS data was not available dur-
ing the decision-making time. Susceptibility status of An. gambiae to clothianidin
and pirimiphos‑methyl
Statistical analysis For clothianidin, susceptibility was recorded in 9 out of
Insecticide resistance status was defined following the 17 sites including Nassian and Sakassou, both ini-
WHO criteria [28] measuring mortality after 24 h for tially targeted districts for IRS. Resistance to clothianidin
pyrethroids and pirimiphos-methyl, after 3 days for was observed in Abengourou, Aboisso, Bettié, Bouaké,

Fig. 2 Susceptibility of An. gambiae s.l. to clothianidin 2% by site in 2019

Kouassi et al. Malaria Journal 2023, 22(1):14 Page 6 of 15

Bouna, Daloa, Odienné, and Yamoussoukro (Fig. 2). collected in Béoumi, Dabakala, Nassian and Sakassou,
Susceptibility to pirimiphos-methyl was recorded at the respectively. Anopheles funestus s.l. was the other malaria
diagnostic dose in 11 sites, while low resistance inten- vector found in Beoumi (0.1%; n = 7) and Nassian (8.5%;
sity was observed in 5 of the remaining sites (Aboisso, n = 368), while both An. funestus s.l. and An. nili were
Adzopé, Bettié, Bocanda, and Daloa). Only Jacqueville found in Dabakala (6%; n = 998 and 3.4%; n = 560), and
recorded a moderate resistance to pirimiphos-methyl Sakassou (0.45%; n = 282 and 0.1%, n = 13), respectively
(Fig. 3). (Table 1).

Adult mosquito fauna across the four bionomic monitoring Molecular species identification of adults An. gambiae
sites collected for bionomic monitoring
A total of 105,225 mosquitoes, including 12,206 (11.6%) A subsample of 694 An. gambiae s.l. from Béoumi, 698
culicines and 93,019 Anopheles (88.4%) were collected from Dabakala, 608 from Nassian, and 731 from Sakas-
over the year (January through December 2019) using the sou were molecularly identified to the sub-species level.
three collection methods (HLC, PSC and CDC light trap). Anopheles coluzzii represented the predominant spe-
Anopheles gambiae s.l. was the predominant malaria vec- cies in Béoumi (mean of 86.5%) and Dabakala (mean of
tor species, representing 94.4% (87,765/93,019) of the 89.3%) (all collection methods included) and was the only
total Anopheles mosquitoes collected across all sites. species found in Sakassou. In Nassian, An. gambiae sensu
Using HLC, a total of 77,122 Anopheles mosquitoes stricto (s.s.) was the only vector species found using the
were collected. With PSC and CDC light trap methods, three methods. Few hybrids of the two species were
10,254 and 5,643 mosquitoes were collected, respectively. found in the HLC samples from Béoumi (0.2%) (Fig. 4).
Anopheles gambiae s.l. was the most collected vector
using all three methods (Table 1). Anopheles gambiae human biting rate
Out of the 93,019 Anopheles, 8,757 were collected in The human biting rates (HBRs) were higher in Sakas-
Béoumi, 16,732 in Dabakala, 4,343 in Nassian from May sou (p = 0.0001), with an overall rate ranging from
through December and 63,187 in Sakassou from Janu- 125.4 b/p/n in January to 423.0 b/p/n in Novem-
ary through December 2019. Anopheles gambiae s.l. was ber indoors and from 98.2 b/p/n in January to 511.6
the most collected malaria vector species in the four sites b/p/n in October outdoors compared to Dabakala (6.0
representing 90.6% (n = 7,930), 88.8% (n = 14,864), 91.4% b/p/n in December to 150.0 b/p/n in July indoors and
(n = 3,968) and 96.5% (n = 61,003) of the total Anopheles 13.8 b/p/n in December to 157.8 b/p/n in September

Fig. 3 Susceptibility of An. gambiae s.l. to pirimiphos-methyl by site in 2019

Kouassi et al. Malaria Journal 2023, 22(1):14 Page 7 of 15

Table 1 Number and percentages of mosquitoes collected in all sites using the three collection methods in 2019
Collection method Species Béoumi# (%) Dabakala# (%) Nassian# (%) Sakassou# (%) Total# (%)

All collection methods An. gambiae s.l 7,930 (90.6) 14,864 (88.8) 3,968 (91.4) 61,003 (96.5) 87,765 (94.4)
An. funestus s.l 7 (0.1) 998 (6.0) 368 (8.5) 282 (0.45) 1,655 (1.8)
An. nili 1 (0.2) 560 (3.4) 0 (0) 13 (0.1) 574 (0.6)
a
Other Anopheles 819 (27.1) 310 (10.2) 7 (0.2) 1,889 (62.4) 3,025 (3.3)
Total 8757 16732 4343 63,187 93,019
HLC An. gambiae s.l 6,102 (88.5) 10,643 (92.7) 3,408 (92.5) 53,179 (96.5) 73,332 (95.1)
An. funestus s.l 7 (0.1) 281 (2.4) 270 (7.3) 159 (0.3) 717 (0.9)
An. nili 1 (0.0) 426 (3.7) 0 (0) 13 (0.0) 440 (0.6)
*
Other Anopheles 783 (11.4) 135 (1.2) 7 (0.2) 1708 (3.1) 2633 (3.4)
Total 6893 11,485 3685 55,059 77,122
PSC An. gambiae s.l 1,183 (97.0) 2,381 (69.9) 501 (83.6) 4,725 (94.0) 8,790 (85.7)
An. funestus s.l 0 (0) 717 (21.0) 98 (16.4) 123 (2.4) 938 (9.1)
An. nili 0 (0) 134 (3.9) 0 (0) 0 (0) 134 (1.3)
*
Other Anopheles 36 (3) 175 (5.1) 0 (0) 181 (3.6) 392 (3.8)
Total 1219 3407 599 5,029 10,254
CDC light trap An. gambiae s.l 645 (100) 1840 (100) 59 (100) 3099 (100) 5643 (100)
Total 645 1840 59 3099 5643
*
Other Anopheles included Anopheles pharoensis, Anopheles ziemanni and Anopheles coustani; rows in bold represent the total Anopheles collected per site

Fig. 4 Proportion of An. gambiae species per collection methods in the bionomic monitoring sites in 2019

outdoors) and Béoumi (9.2 b/p/n in December to 161.8 biting rates were lowest in Nassian (from 0.8 b/p/n in
b/p/n in September indoors and 11.6 b/p/n in June to May to 118.2 b/p/n in October indoors and 2.2 b/p/n in
128.8 b/p/n in September outdoors b/p/n). The mean August to 83.4 b/p/n in October outdoors) regardless
Kouassi et al. Malaria Journal 2023, 22(1):14 Page 8 of 15

Fig. 5 Anopheles gambiae s.l. biting rate using HLC at all sites in 2019

of the months and the collection place (indoor or out- in Sakassou than indoors, and indoors than outdoors in
door) (Fig. 5). Overall, An. gambiae s.l. showed similar Béoumi (53.2% indoors) and Nassian (56.9% indoors),
biting behaviour across the four districts with peak bit- while equal percentages were recorded both outdoors
ing time observed between 10:00 p.m-3:00 a.m. (Addi- and indoors (50%) in Dabakala.
tional file 1). However, An. gambiae s.l. bite slightly
higher, but not significantly different outdoors (51.2%)

Table 2 Sporozoite infection rate and EIR of malaria vectors collected using HLC in the four vector bionomics sites
District An. gambiae s.l An. funestus s.l
TC TA P Mean SR Mean Mean EIR(ib/p/n) TC TA P Mean SR Mean Mean
HBR(b/ HBR(b/ EIR(ib/
p/n) p/n) p/n)

Béoumi 7,930 900 9 0.011 48.47 0.34c 7 0 – – – –

Dabakala 14,864 868 16 0.018 81.36 1.17b 998 0 – – – –
Nassian 3,968 675 37 0.045 26.62 1.02b 368 215 16 0.074 16.4 1.21
#
Sakassou 52,484 1541 25 0.018 278.2 4.44a 282 0 – – – –
TC total collected; TA total analysed; P positive; SR sporozoite rate; HBR Human Biting Rate; EIR Entomological Inoculation Rate; (–) not analysed. EIR with different
symbols are significantly different
#
12 collection months were conducted in Sakassou and 8 months in the other 3 sites; the mean EIR of sites that have the same letter (a, b or c) are not significantly
different
Kouassi et al. Malaria Journal 2023, 22(1):14 Page 9 of 15

Plasmodium falciparum sporozoite infection For Sakassou, a peak of number of positive malaria
and entomological inoculation rate cases was observed in August 2017 and in April 2018.
Table 2 shows the overall infection rate and EIRs for An. Malaria incidence was averagely stable in the health dis-
gambiae s.l. and An. funestus s.l. collected by HLC in the trict between May and December 2017 (around 4000–
four districts. Nassian recorded the highest P. falcipa- 5000 cases) except the peak of 6,613 cases in August,
rum sporozoite infection rate (SR) among An. gambiae while all months had cases above 3000 from January to
s.l. (0.055), followed by Sakassou (0.021) and Dabakala December 2018 with the peak of more than 7000 malaria
(0.018). The lowest rate (0.010) was recorded in Beoumi. cases in April 2018. The lowest number of malaria cases
Additionally, 16 An. funestus s.l. mosquitoes were found was recorded between January and March 2017 in Sakas-
with sporozoite infections among the samples collected sou (Fig. 7).
in November and December 2019, representing a SR of In Nassian, even though the number of cases was
7.4% of the 215 analysed mosquitoes in Nassian. slightly lower than Sakassou, an incidence peak was
Sakassou recorded the highest EIR (4.44 ib/p/n) of An. observed in August 2017 (3,041 malaria cases) while two
gambiae s.l. (p = 0.0272), while Nassian and Dabakala similar peaks were recorded in April 2018 (2,544 cases)
had similar EIRs of 1.02 and 1.17 ib/p/n, respectively. and in June 2018 (2,432 cases). However, the number
Béoumi recorded the lowest EIR among the four sites, of malaria cases were slightly higher in 2018 than 2017
with 0.34 ib/p/n. May and November were the months except for a drop in cases that occurred in July 2018
with the highest number of An. gambiae s.l. infected bites (Fig. 8).
in Sakassou, while Dabakala recorded a single peak in
July, Béoumi, and Nassian in October (Fig. 6). An average Discussion
EIR value of 1.21 ib/p/n was recorded for An. funestus s.l. The study was set to collect and analyse entomological
analysed in Nassian. surveillance data to support and guide appropriate vec-
tor control decision-making in Côte d’Ivoire. To make
Epidemiological data of targeted sites good use of all the insecticide resistance monitoring data
HMIS data from 2017 and 2018 were averaged to pro- collected across the country and to support the NMCP’s
vide monthly estimates of the number of confirmed cases decision making to achieve its national strategic plan
within the population that were recorded from all health (NSP) goals targeting the reduction of malaria cases by
facilities of each district. at least 75% in 2025 and pre-elimination by 2030, the

Fig. 6 EIR of Malaria Vectors Collected Using HLC in the Four Vector Bionomics sites in 2019
Kouassi et al. Malaria Journal 2023, 22(1):14 Page 10 of 15

Fig. 7 Malaria confirmed cases over time in Sakassou in 2017–2018

Fig. 8 Malaria confirmed cases over time in Nassian in 2017–2018

NMCP, malaria stakeholders and partners prioritized the partners, epidemiologists, and NMCP, conducted a sys-
selection of ITNs for the 2021 mass distribution and, IRS tematic review and analysis of insecticide resistance
district and insecticide selections to be based on data. monitoring data available to design a stratified ITN mass
For consensus, the vector control committee composed distribution which would allocate ITNs by district fol-
of the country’s entomologists, financial and technical lowing the resistance status of local vectors. Similarity of
Kouassi et al. Malaria Journal 2023, 22(1):14 Page 11 of 15

pyrethroid resistance, resistance intensity and PBO syn- significant increase in mortality using PBO was observed.
ergism was found among all previously reported data by Standard nets treated with alpha-cypermethrin and del-
Kouassi et al. [19], and Bocanda and Jacqueville were two tamethrin were further considered as secondary options
additional sites investigated [19]. per resource constraints but using the vector profile of
Regarding the IRS to be implemented in the coun- each site to be targeted with either of each insecticide
try, the vector surveillance data in all four study sites (Fig. 9). Eleven districts were, therefore, covered with
showed that, the proportion of vectors caught outdoors PBO-ITNs, eighteen districts with Interceptor G2 and
and indoors using HLC was similar, demonstrating that the remaining districts receiving either deltamethrin (75
the vectors could be feeding either indoors or outdoors. districts) or alpha-cypermethrin (9 districts)-based ITNs
This trend and the considerable indoor resting density of considering the resistance profile against both insecti-
the vectors could support a deployment of IRS which tar- cides at each district. Even though the pyrethroid-only
gets endophagic and endophilic vector populations. Most ITNs still show minimum protection against malaria vec-
vectors of all sites were recorded actively biting between tors [41] and no concrete ITN failure threshold has been
10:00 p.m. and 3:00 a.m., and this biting period repre- set to date, several studies have reported the added value
sents the ideal reported biting time for effective vector of new types of ITNs and particularly in area of high
control using both recommended strategies such as ITNs insecticide resistance of the mosquitoes [42–44]. Further
and IRS [34]. The period of biting activity mostly coincid- consideration will need to be taken for all upcoming mass
ing with human sleeping time appears to be an important distribution campaigns to enable coverage of the whole
determinant of vector population vulnerability to inter- country’s households with new generations of ITNs to
ventions [13]. Additionally, the monthly biting behav- help mitigate insecticide resistance.
iour of the vector has yielded different biting peaks and Finally, for the 113 health districts that composed the
infectivity according to sites. Sakassou recorded two high country with varying resistance patterns described, the
peaks compared to the others including two peaks of NMCP was able to purchase about 20 million of ITNs
EIRs, which could be related to the particularly irrigated to ensure the entire 32,172,759 people of Côte d’Ivoire
rice field activities undertaken in the area, while the other received the most appropriate ITNs for the upcoming
sites biting, and infection peaks coincided with the rainy campaign, including Interceptor G2 and PBO ITNs.
season during the year. If rain has a specific factor on
increasing larval habitats and mosquito density, it is also IRS district selection and implementation decision making
known that rice paddies contribute largely to mosquito As IRS is still not widely achievable in endemic coun-
proliferation, infection, and transmission [35–37]. The tries due to budgetary factors, several factors need to
trends have always been a particular focus for vector con- be considered before conducting IRS, including (i) the
trol interventions including social and human behaviour choice of the appropriate and targeted districts in-coun-
change, and communication to protect the population. In try, dependent on malaria incidence and the country’s
such periods, some of the countries intensify their vector elimination goals, (ii) the targeted district vector popula-
control approaches and strategies by adding complemen- tion density and behaviour, (iii) the insecticide resistance
tary measures such as seasonal malaria chemotherapy, status of the vectors to IRS insecticide, (iv) the peri-
larval source management, or intensified sensitization odic malaria incidence data, and (v) financial resources,
campaigns [38–40]. accessibility, and security. In Côte d’Ivoire, the selection
Furthermore, insecticide susceptibility test using piri- of districts to be targeted for IRS was first supported by
miphos-methyl and clothianidin that indicated suscepti- the epidemiological data provided by each district. Fur-
bility to pirimiphos-methyl and clothianidin in 11 and 9 thermore, the NMCP prioritized districts presenting the
of the 17 tested sites respectively, including Sakassou and highest malaria incidence across the country for imple-
Nassian, provided options for IRS sprayable insecticides menting IRS considering its goal to decrease transmis-
in the country. sion in highly endemic districts. In addition, following
the available resources and the constraints of IRS opera-
Stratified mass ITN distribution decision making tion, other parameters like the size of the district in terms
The first plan was thus made for the different sites where of population, number of structures and the geographi-
the resistance status of the vector populations was avail- cal accessibility have been considered in IRS site selec-
able and then extrapolated to the other districts in order tion. But susceptibility of local vectors to the available
to cover all 113 health districts within the country. Con- IRS insecticides and vector biting and resting behaviours
sequently, the availability of updated data supported the remained the determinant parameters for appropriate
inclusion of Interceptor G2 and PBO ITNs in targeted IRS site selection. With the level of resistance occurring
districts where the susceptibility to chlorfenapyr or in the country, limited insecticide classes were available
Kouassi et al. Malaria Journal 2023, 22(1):14 Page 12 of 15

Fig. 9 Map of stratified ITN mass distribution and IRS sites in Côte d’Ivoire

for spraying. As encountered in several countries, pyre- in the country [52], Sakassou represented the first tar-
throid and carbamate IRS insecticides report short term geted IRS district in Côte d’Ivoire. Furthermore, Nas-

cides (pirimiphos-methyl/Actellic®) [45–49]. Further-

residual efficacy compared to organophosphate insecti- sian recorded the highest infection rate and reported
the second highest malaria incidence of the country
more, it becomes crucial to have alternative insecticide in 2018–2019, though the district recorded the low-
molecules for IRS to enable rotation of insecticides for est density over the collection period. Nassian showed
resistance management as pirimiphos-methyl resistance a seasonal vector density and transmission with specific
is already being reported in several countries including peak density and incidence recorded between September
Côte d’Ivoire [50]. Thus, the use of the new WHO Pre- and October, coinciding with the single rainy season in
Qualified clothianidin based insecticides which were the area. Beoumi and Dabakala recorded slightly similar
reported to have slightly longer residual efficacy turned transmission parameters to Nassian with specific biting
out to be the applicable alternative to the country [51]. and infection peaks around the rainy season. The trends
Hence susceptibility to clothianidin, recorded against observed, the geographical position and similarity have
the local vector populations in Sakassou and Nassian allowed the selection of Beoumi and Dabakala as con-
compared to Bettié, has guided the selection of clothia- trol sites for an evaluation of IRS in Sakassou and Nas-
nidin-based insecticides to be sprayed in both targeted sian, respectively. Moreover, the WHO recommends
districts. scheduling IRS application to coincide with the build-up
With its extremely high mean biting rates (170.1 b/p/n) of vector populations just before the onset of the peak
coupled with the highest reported malaria incidence transmission season [5]. Even though the epidemiological
Kouassi et al. Malaria Journal 2023, 22(1):14 Page 13 of 15

data reported before the implementation of IRS did not Author contributions
BLK, CVAE and JC participated in the activity planning, supervision and drafted
ultimately overlap with the EIRs in Sakassou and Nassian, the manuscript, CGNG, ET, LYK, AAK, MAA and AFO supported and supervised
the timing of IRS and residual efficacy of the WHO rec- the data collection, AKE, LGB, JG, YAKK, JKIK, AHOB, RMY and RNN participated
ommended IRS insecticides reported in different coun- in data collection and laboratory analysis. ATM, PZ, PLY, AB, SRI, NGC, and CF
reviewed the manuscript for improvement. All authors read and approved the
tries could justify the impact of the intervention during final manuscript.
both epidemiological and entomological parameter’s
peak periods, As April through August represents the Funding
This study was supported by the United States President’s Malaria Initiative
long rainy season in Sakassou while June through Sep- through the United States Agency for International Development (USAID) Abt
tember represents the single rainy season in Nassian, the Associates / VectorLink Project.
IRS timing was selected, considering all above factors and
Availability of data and materials
results. Therefore, the highest vector densities recorded, The datasets used and/or analysed during the current study are available in
and the infectivity trends guided IRS campaign planning the Additional file 1 and could also be provided by the corresponding author
between April and May in Sakassou, right before the peak on reasonable request.
of transmission in May, and in June through July in Nas-
sian, right before the peak of infectivity. Declarations
In addition, both clothianidin-based products were Ethical approval and consent to participate
considered suitable, with Fludora Fusion and Sum- The study protocol was approved by the United States Agency for Inter‑
iShield selected to be sprayed in Sakassou and Nassian national Development/PMI Cor team. The study received ethics approval
from the Ethical Committee of the Ministry of Health of Côte d’Ivoire (N/Ref:
respectively. 168–18/MSHP/CNESVS-km). Written informed consent was obtained from
community leaders and heads of households before starting the study. Poten‑
tial mosquito collectors were required to sign a consent form before working
Conclusion as collectors.
Selection of appropriate public health interventions
Competing interests
should be based on evidence through entomological The authors declare that they have no competing interests.
monitoring to achieve expected goals. The data collec-
tion and analysis conducted prior to the deployment of Declarations
The findings and conclusions expressed herein are those of the author(s) and
vector control tools in Côte d’Ivoire guided the selection do not necessarily represent the official position of neither USAID nor PMI, nor
and implementation of appropriate vector control tools those of Centers for Disease Control and Prevention (CDC).
and strategies, with the introduction of new genera-
Author details
tion of ITNs and IRS. Use of data to drive vector control 1
PMI VectorLink project, Abidjan, Côte d’Ivoire. 2 Swiss Centre of Scientific
decision-making is essential for appropriate and targeted Research in Côte d’Ivoire, Abidjan, Côte d’Ivoire. 3 Centre of Veterinary
interventions. Furthermore, continuous monitoring of and Medical Entomology, Abidjan, Côte d’Ivoire. 4 National Institute of Public
Hygiene, Abidjan, Côte d’Ivoire. 5 National Institute of Public Health/Pierre
intervention effects where possible and consideration for Richet Institute, Bouake, Côte d’Ivoire. 6 National Malaria Control Programme,
other vector borne diseases, when possible, are required. Abidjan, Côte d’Ivoire. 7 U.S. President’s Malaria Initiative, USAID, Abidjan, Côte
For both IRS selected districts, the presence of different d’Ivoire. 8 U.S. President’s Malaria Initiative, Centers for Disease Control and Pre‑
vention (CDC), Abidjan, Côte d’Ivoire. 9 U.S. President’s Malaria Initiative, USAID,
species in Nassian (An. gambiae s.s.) and Sakassou (An. Washington, DC, USA. 10 U.S. President’s Malaria Initiative, Entomology Branch,
coluzzii) will be important to monitor in order to esti- U.S. Centers for Disease Control and Prevention (CDC), Atlanta, GA, USA. 11 PMI
mate any change in the species population and/or vec- VectorLink Project, Washington, DC, USA.

tor behaviour that could affect the introduction of IRS, Received: 28 September 2022 Accepted: 3 January 2023
inform future interventions, and impact assessment. Published: 12 January 2023

Supplementary Information
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