Evidence for perennial malaria in rural and urban areas under the Sudanian climate of Kandi, Northeastern Benin

Malaria is a major cause of global morbidity and mortality, with most of the burden in sub-Saharan Africa [1, 2]. More than 90% of recorded malarial deaths occurring in Africa are among the most vulnerable population, such as children under five years old and pregnant women [3, 4]. In spite of many efforts of the National Malaria Control Programs (NMCP) and international donors to combat the disease through various vector control interventions, malaria continues to be a real public health problem.

In Benin, malaria was the leading reason for consultation and hospitalization in healthcare centers. In 2012, incidence of malaria in Kandi, northeastern Benin, was 28.55%, two times higher than the national average of 14.6 per 100 Benineses [5]. Despite a dry season period of about six months, in the Kandi municipality, several cases of malaria were still diagnosed. Healthcare registers in the health center of Sonsoro (rural Kandi) indicated that during the drought period between 2008 and 2012, clinical malaria cases were estimated at 15 to 30%. Of these, approximately nearly 60% were children under 10 years old (R. Govoetchan, personal communication). Although these unexpected cases could be linked to relapse or cases of imported malaria, the possibility of recent infection could not be ruled out in the light of the magnitude of the prevalence and the sedentary status of local people and especially children.

Several studies have shown that malaria infection is influenced by environmental factors such as temperature, rainfall, humidity and elevation. In tropical settings, temperature and rainfall conditions are nearly always favorable for the development of Anopheles mosquitoes, the intermediate hosts in the transmission of malaria parasites [6, 7]. According to Martin and Lefebvre [8], rain is generally synonymous with new mosquito breeding sites. However, rain can also destroy the existing ones: heavy rains can transform basins to streams, hinder the development of eggs and larvae, or simply eject them from water [8]. Conversely, extreme drought conditions lead to the evaporation of most of the conventional mosquito breeding sites and in turn lower the mosquito population [8–12]. For this reason, the dry season in tropical Africa is often regarded as a period of very low malaria transmission, a period during which no method of malaria prevention and control is deployed. This is due to the fact that, like most mosquitoes, Anopheles gambiae, depends on the availability of suitable surface water for oviposition. However, during the dry season and dry spells during the wet season, larval sites may not be available for days, weeks, or even months in different environments [13–16]. Under such conditions, mosquitoes that develop eggs (gravid specimens) cannot lay them [17] thereby seriously affecting the population size. Thus, the Culicidae nuisance and the anopheline density are significantly lowered compared to the wet periods of high transmission.

An important reason for the heavy malaria burden in Africa is that the malaria-transmission machinery consists of an exceptionally robust vectorial system including An. gambiae s.s (representing two incipient species known as the M and S molecular forms), a sibling species An. arabiensis, and An. funestus[18]. These vectors are not only able to exploit diverse environments including expansive dry savannas and semi-desert areas, but also able to ensure the maintenance of malaria transmission during periods of severe drought. Moreover, many studies reported changes in people’s behavior in relation to the individual methods of protection during the dry season. Given that the mosquito bites are less noticeable at this time of the year and that the night is sometimes excessively hot, people do not feel the need to sleep under bed nets and trivialize any other method of protection against possible scarce mosquito bites.

Very few scientific publications focusing on malaria during the dry season exist. In order to assess the sources of the several recent Plasmodium falciparum infections often reported during drought periods in Sonsoro, rural Kandi, we decided to conduct a year round study on the entomological profile of the location compared to a site in urban Kandi (Gansosso). We particularly and meticulously focused on what happens in the dry season. Moreover, we investigated malaria prevalence in the two locations (Sonsoro and Gansosso) during a period of aridity, a time supposed to be of very low or zero malaria transmission, and compared them with drought entomological data.

We observed that the entomological profile was not the same in rural and urban Kandi. An. gambiae, the main malaria vector in Africa is very abundant in rural settings of Kandi as compared to that in rural areas. This result suggested that there is an ecological dichotomy between the two study sites, the rural (Sonsoro) and the urban (Gansosso). Moreover, it is well known that urbanization greatly influenced the Culicidae diversity and is antagonistic to the anopheline abundance. The situation in drought was characterized by a significant decrease in vector density. In view of larval sampling data, we think that the few anopheles caught during the dry season, especially in urban Kandi, come from household water sources (canisters, jars) which become potential breeding sites in this period of the year. The situation was similar in rural Kandi although the proximity to a permanent water site appeared to be a risk factor. The poor conservation of water stocks in households in a period of scarcity of classical breeding sites indirectly causes the domestication of mosquito larval habitats. This could be avoided if the receptacles containing water supplies are well covered regularly.

Our results showed a lower aggressive density of An. gambiae during drought periods in both rural and urban settings as compared to the values in the wet season, nevertheless the HBR for the semester drought was 3.4 times higher in rural Kandi than in urban Kandi (p < 0.001). It is thought that the low density and the low aggressiveness often noted for An. gambiae in the dry season is particularly due to the fact that Anopheles adults are scattered in shelters for a summer diapause (aestivation), to ensure its survival [15]. Thus, sampling them is very difficult because, on one hand, they are resting in hiding, and on the other hand, they reduce the frequency of blood meals [26] as having significantly slowed the rate of ovarian development [27].

Similarly, we also observed significant seasonal variation in the infectivity of An. gambiae to P. falciparum in both study sites. The EIR was nil in urban Kandi due to the fact that no anopheline vector was found to be positive for the CSP of P. falciparum. The very low number of only 5 An. gambiae captured in urban Kandi during the whole drought period could explain it. For the whole study duration, we noted a higher transmission of malaria in rural Kandi (130.75 ib/h/year) than in urban Kandi (6.45 ib/h/year). The level of malaria transmission in rural and urban Kandi is more of a concern than in some locations under a wet climate in southern Benin. There are for instance Ossomou in the southeastern part (0 ib per semester) [28] and Ouidah-Kpomassè-Tori health district in the southwest (0.7 ib per 100 night) [29].In addition, the epidemiological situation of malaria is more complicated in Kandi than in many locations in Sub-Saharan Africa such as Bobo-Dioulassou in Burkina Faso [30], Edea in Cameroon [31], Dassilami in Gambia [32], Dakar (around Grande Niaye marsh) in Senegal [33] where the annual EIRs were lower.

The entomological data in Kandiwas perfectly reflected in the results of the parasitological survey conducted in both locations. Our results showed that Sonsoro in rural Kandi is a location of very high malaria risk during periods of drought. The prevalence of P. falciparum (RDTs) results showed that malaria is much more acute in the rural area especially in the dry season. The absence of urbanization has been identified as an important collateral risk factor. Our findings corroborate those of Gardiner et al.[34] in southeastern Ghana, Watts et al.[35] in Zambia, Trape [36] in Brazzaville, and Hay et al.[37] in most parts of tropical Africa who have all noticed that the lower density of Anopheles accompanying urbanization leads to significant parasitological and clinical implications [34–37].

Moreover, the low frequency of both positive RDTs and clinical malaria cases observed in Gansosso could also be due to self-treatment in urban populations and home care management of malaria once the onset of symptoms such as fever occurs. According to Gardiner et al.[34], the low incidence of malaria in an urban community, especially children under 10 years old is associated with widespread use of anti-malarial drugs such as a prophylactic treatment. This is probably one of the reasons why we note a gap in urban and rural Kandi results [34].

The existence of malaria cases in the dry season in urban areas where mosquito larval habitats and Anopheles vectors were scarce illustrated perfectly the perennity and the endemicity of malaria transmission in the municipality of Kandi, as in Bénin. The drought malaria prevalence recorded in urban Kandi (7.5%) is still relatively high for areas outside Africa, such as Asian countries. According to Trape [38], there is a threshold level of transmission beyond which malaria cases become common to the point that the malaria infection truly becomes a problem. Thus, above 2 ib per individual per year in a location, malaria transmission should be of major concern [38]. The annual value of EIR in urban Kandi (6.45 ib/h) exceeded the “threshold of Trape” and easily explained the malaria prevalence recorded there.

To this end, the indoor residual spraying of insecticide will be ideal, especially when we consider the fact that in and around Kandi, there is a single period of malaria transmission (May to October). However, given the very high night temperatures during the dry season, which compels individuals to sleep outside, malaria transmission prevention during this season of the year could be strengthened outdoors. Thus, populations may be encouraged to sleep outdoors with their bednets. Meanwhile, it is clear that due to the excessive heat, the use of bed nets during the dry season will be very difficult. In such conditions, it is important to provide them with new tools adapted to their practices and habits. The hypothesis of repellent perfumes or deodorants holds a great potential in this regard.

Our study is not without some limitations. The prevalence of malaria can be more accurately estimated by the use of PCR based diagnostics or microscopy instead of RTD [39, 40]. However, since the primary outcome of interest in this study was recent infection and a global view of malaria prevalence as opposed to parasitaemia, we believe this limitation will neither significantly affect interpretation of the results nor affect the scientific quality of the study. Another potential limitation of this study is the fact of not to present the larval density in the drought-refugia of mosquitoes. Our larval sampling data were qualitative in order to just identify the atypical habitats which maintain mosquito breeding and ipso facto malaria transmission when classical larval habitats have dried up.

Our results showed a high level of malaria transmission in the municipality of Kandi. Household water source plays an important role in maintaining the breeding of Anopheles larvae and the malaria transmission in Kandi. In rural settings, the proximity to a permanent water site could probably be the aggravating factor. These were the causes of the several malaria cases often recorded in Sonsoro during periods of drought. However, both entomological and parasitological data suggested that the epidemiological issue of malaria is not uniform in Kandi, especially in drought periods. At Sonsoro in the peripheral zone, the prevalence of malaria during the dry season was eight times higher than at Gansosso in downtown Kandi. Among the likely factors involved, the level of urbanization has been identified as potentially having a significant influence on the incidence of malaria in the municipality of Kandi.