Background
The commitment to eradicate malaria from the globe through increased malaria control and treatment has resulted in a remarkable decrease in the number of cases and mortality associated with this disease [
1‐
3]. It is estimated that the scale-up of the major interventions, long-lasting insecticidal nets (LLINs), indoor residual spraying (IRS) and treatment with artemisinin-based combination therapy reduced malaria cases and mortality by 37 % and 60 %, respectively, between 2000 and 2015 [
4]. However, malaria remains a serious disease affecting the well-being of people living in the tropical and subtropical countries of the world and progress against malaria has slowed down considerably in the past few years [
1].
In Ethiopia, malaria is still an important cause of morbidity and mortality as in other countries in tropical Africa. Despite a prevalence of less than 1 % in the country, malaria is important in certain foci that pose a risk for epidemics. The National Malaria Control Programme of the Federal Ministry of Health of Ethiopia has recently set an ambitious goal of eliminating malaria from all 565 malarious districts by the year 2030 [
5]. In order to achieve this goal, it is important to understand when and where malaria is being transmitted, both at large and small-scale levels. This is important for planning appropriate malaria control strategies and their efficient implementation.
One of the areas where malaria transmission is of concern is in lowland agricultural development areas. Ethiopia has been practicing an Agricultural Development Led Industrialization (ADLI) since 1991 [
6]. As a result, various agricultural development areas have been created in the country. Such agricultural investments grow high cash generating crops such as sesame, green grams, cow peas, and sorghum. Agricultural development in such areas has resulted in the migration of hundreds of thousands of seasonal workers into areas where vector-borne diseases, such as malaria and visceral leishmaniasis, are endemic [
7].
As these areas offer opportunities for employment, mobile and migrant populations travel to these sites, often during the rainy season for cultivating crops in the area. Those workers stay working in the agricultural development areas until harvesting time. These areas are productive for crops, but also for mosquitoes. This is mainly due to their warm climate and creation of many temporary breeding habitats during the rainy season that provide favourable environment for mosquitoes. Migrant workers may leave mosquito nets in their permanent homes, and stay in temporary, substandard shelters, thus increasing their risk of contracting malaria. Additionally, they may work or remain exposed to mosquitoes in ways and at times that are different from when they are in their hometowns. They may also carry malaria parasites back to their home areas of relatively low malaria risk, complicating the efforts towards malaria elimination in these districts [
8].
The biting behaviour of mosquitoes is an important risk factor for infection with malaria parasites [
9]. Hence, prevention and control measures for the disease should take the site and time of people’s exposure to mosquito bites into account. There is very little previous research on malaria vectors in Benishangul Gumuz, western Ethiopia, which is home to a large number of agricultural development areas. In order to establish an effective malaria control programme through targeted malaria prevention messages and control interventions, it is essential to understand the mosquito species present in the study area, the venue and times that mosquitoes bite humans and the risk of humans becoming infected with malaria. This study aimed to provide the entomological context of malaria transmission in agricultural settings in this area in tandem with a second study investigating the human behaviour in agricultural development areas. Accordingly, this work aimed to determine the host-seeking behaviour of
Anopheles mosquitoes in this area that is one of the agricultural development areas in Ethiopia with substantial migrant human populations from highland areas.
Discussion
The mosquito literature from Benishangul-Gumuz is extremely limited and no literature related to the malaria vectors in Dangur woreda was found. In this study, eight species of
Anopheles were collected and identified, with
An. arabiensis, the major malaria vector in Ethiopia, as the most prevalent. Additionally,
An. arabiensis was the only species found to have
Plasmodium circumsporozoite protein in the head and thorax, indicating that this is likely to be the most important vector in agricultural areas in Dangur woreda. However,
An. coustani and
An. pharoensis were also collected in small numbers and these species have been found to be capable of transmitting
Plasmodium parasites in laboratory and field studies [
21,
22].
The biting times of
An. arabiensis present a challenge for the protection of migrant workers from infectious bites.
An. arabiensis were found biting indoors and outdoors at nearly all time points, indicating an equal risk for workers staying indoors and outdoors, similar to elsewhere in Ethiopia [
23‐
26]. Pooling the overall
Anopheles species collection, Kenea et al. [
26] reported that the outdoor density was 3.3 times higher than the indoor density which also indicates the importance of outdoor biting activities for malaria transmission. Furthermore, biting started as early as the 18:00 h-19:00 h time period and reached a first peak between 19:00 and 22:00. Early biting of
An. arabiensis has been found in other studies in Ethiopia, but not always with a second peak [
27]. Tadesse et al. [
16] found that at least half of workers went to bed by 21:30, but this would leave them exposed to the first peak for 2.5 hours before sleep. Additionally, LLIN use by migrant workers was almost none, as they often left their nets with their families when they came to the farms for work and the farm owners do not provide any [
16]. One limitation of this study is that the HLCs were completed by 6:00 h, whereas mosquito host-seeking may have continued on beyond this time point, posing further risk for workers in the early morning. Higher mosquito densities in the large farms suggest that more farming activities and hence higher workers’ population might enhance the population of the vectors in those farms. Janko et al. [
22] reported a positive correlation of agriculture coverage and the density of biting
An. gambiae s.l. For example, they indicated that a 15 % increase in agricultural cover was associated with increased probabilities of
An. gambiae s.l. biting indoors.
The lower mosquito vector density in the fields compared to outdoors near shelters might be due to higher attraction to places where the host population was higher [
28,
29].
Seasonal variations were observed in the numbers of mosquitoes collected that were generally similar to those in other areas in Ethiopia, with an increase in mosquito populations during the main rainy season, and a decrease in population size as the rains end towards the end of the year [
23,
24]. It is important to notice that the peak of the agricultural activities and hence demand for workers occurs during the time of the year with the largest populations of
An. arabiensis.
Finally, the detection of sporozoites in
An. arabiensis allowed us to calculate their entomological inoculation rate. This was found to be 1.41 infectious bites per month in the study area during the 6 months that monitoring was conducted. This figure is similar to EIR found in other parts of Ethiopia. Massebo et al. [
24] found a yearly EIR of 17.1 in Chano, in the Southern Nations, Nationalities, and People’s Region. In both locations annual EIR is well above 0.003 inoculations per night, the threshold below which Smith et al. [
25] estimated EIRs needed to drop below for substantial reductions of malaria prevalence. However, EIRs in highly malarious areas where vector control has had an impact can often reach much higher levels [
30], indicating that improved vector control and treatment for malaria could have an important impact on transmission in these farms. Therefore, it might be very useful for the national malaria control strategy to focus on universal coverage of bed net distribution, including for the mobile and migrant populations and improvement of other vector control measures such as better IRS and environmental management (destruction of potential aquatic habitats) in such areas of the country.
Insecticide resistance was not assessed as a part of this study. Further work should be done to evaluate the insecticide susceptibility of An. arabiensis in this area. As IRS is not currently well implemented for protection of many of the workers due to the poor quality of structures or incomplete walls, the susceptibility testing should focus on the evaluation of Actellic 300CS, pyrethroids, Chlorfenapyr, and the synergism of pyrethroid susceptibility with piperonyl butoxide.
There were some limitations to the current study. Collections were only made over a six-month period, and not over the whole year. While the six months chosen were the primary season for malaria transmission, there may be risks of malaria transmission outside these months. Also, collections in the fields were conducted from September until December, whereas collections in the worker’s shelter areas were conducted from July to December. An additional limitation of this study was that the mosquito collections ended at 06:00, and there may be some mosquito biting after this time. The ELISA reactions were considered positive at twice the value of the mean optical density of negative controls and were not re-boiled when positive. Finally, the current recommendations for analysis of human exposure [
20] do not take into account mosquito response to human behaviour. Outdoor biting mosquitoes that do not find humans outdoor may to move indoors to feed on humans, and thus we may have underestimated the risk, for both net users, and, to a greater extent, non-users.
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