Urban malaria in sub-Saharan Africa: dynamic of the vectorial system and the entomological inoculation rate

Sub-Saharan Africa still bears the highest burden of malaria morbidity and mortality worldwide despite improvements in the diagnostic of the pathogens and large-scale deployment of vector control measures, such as Long-Lasting Insecticidal Nets (LLINs) and Indoor Residual Spraying (IRS) [1]. In 2019 over 229 million cases and 409,000 deaths were recorded across the world [1]. Although the whole sub-Saharan Africa region is exposed to malaria transmission risk, high heterogeneity in malaria transmission patterns exists on the continent, particularly between urban and rural settings [2‐4]. It is considered that people living in rural settings are more exposed to malaria transmission risk compared to those living in urban settings [3, 5]. Studies conducted so far suggested higher densities and a greater diversity of malaria vector population sizes in rural compared to urban settings [6]. Many factors have been reported to affect malaria transmission intensity in urban settings including pollution, which can affect anopheline larval habitats and reduce their population size as well as impact mosquito life cycles and consequently their vectorial capacity. Urban dwellers may also have greater mosquito avoidance behaviour, including the use of repellents, screens on windows, insecticides spray and coils [2, 7‐9]. During the last decade, sub-Saharan Africa registered an unprecedented growth of it urban population.

The urban population which was estimated at 491 million in 2015 is projected to grow to nearly 1.5 billion by 2050 [10]. However the rapid unplanned urbanization observed in many sub-Saharan Africa cities characterized by the colonization of lowland areas for house construction, the absence of drainage system for water, the presence of standing water collection everywhere due to the bad state of roads and poor housing are all considered to affect the distribution of vector population and malaria transmission pattern [11]. Now, many cities are reporting increase practice of urban agriculture in both the city centre and periphery; all these activities create favourable breeding habitats for mosquitoes [12‐14]. The rapid unplanned urbanization appears as a potential risk factor promoting malaria and arboviral diseases transmission in urban settings [15, 16]. Studies conducted so far suggested higher densities and a greater diversity of malaria vectors in rural compared to urban settings [2, 6, 17]. Besides, it has been reported that the most efficient malaria vectors Anopheles gambiae sensu lato (s.l.) namely Anopheles gambiae, Anopheles coluzzii, Anopheles arabiensis, which had a strong preference for unpolluted water [13] now displays a great adaptation pattern to polluted waters in urban cities [18, 19] and breed in different human-made habitats including containers filled with water, swimming pools, tyre tracks, water tanks [20]. Housing construction sites or construction materials were also found to be productive habitats for malaria vectors [21, 22]. The situation of malaria in sub-Saharan African cities is further becoming complex with the recent invasion of the Asian malaria vectors Anopheles stephensi [23, 24]. Although the epidemiological consequences of such invasion is still not well understood, it is likely that the addition of new competent vectors in the urban environment may further negatively affect malaria control strategies in urban areas. Considering the potential public health impact that urban malaria could have and potential effects on the economic development of countries, there have been during the last decade a renewed interest with several studies assessing malaria transmission pattern and vector bionomic in urban settings across sub-Saharan Africa [11, 18, 21, 25‐29]. However there have been so far not enough studies summarising findings from previous works in order to capture the general trend of malaria transmission, vector distribution and larvae preferred breeding habitats in urban settings. For instance, there have been fewer studies providing an overview of the general distribution pattern of main species in urban settings across Africa. The present study’s objective is to carry out a review of the existing literature on malaria transmission across sub-Saharan Africa in order to provide a better understanding of the evolution of vector populations and malaria transmission pattern.

The present study is an update of previous reviews on urban malaria in sub-Saharan Africa [2‐4, 29, 32, 33], it provides new data on malaria transmission pattern and anopheline species distribution. Urbanization is increasingly blamed of influencing the epidemiology and evolution of vector-borne diseases in sub-Saharan Africa. More than half of the world’s population now lives in towns or cities and it is projected that this number could rise to 75% by 2050 [34]. From the review it appears that, the Entomological Inoculation Rate (EIR) is highly heterogeneous in cities across the continent [18, 35, 36]. In many cities centre, malaria transmission is low or absent while others register high EIR estimates [11, 37]. The difference between cities could derive from the scale of urban development, population size and the magnitude of unplanned urbanization. Unplanned urbanization characterized by the colonization of lowland areas for habitat construction, poor drainage system in urban settings, the development of slums and spontaneous habitats and the practice of agriculture in the city centre was reported to deeply influence malaria transmission intensity [15, 38]. Although EIR estimates were always higher in rural and peri-urban settings compared to urban centres [2], it also appeared that, because of increase poverty in urban settings there are an increasing number of people exposed to malaria transmission risk. In the city of Libreville for instance, a high transmission rate was recorded in the city centre characterized by poor housing, high population density, low socio-economic level and inadequate management of waste, compared to the periphery where the population had a high socio-economic level and good management infrastructure [39]. In the city of Yaoundé, where slum-like conditions are common across the city, malaria transmission was highly prevalent in both the city centre and the periphery [11]. The close association between malaria and the economic status of the household has been highlighted in different studies across the continent [4]. Additional factors including river overflowing, city landscape and seasonal variations were also found to influence the intensity and pattern of malaria transmission [14, 40]. Important differences were noted when comparing malaria transmission intensity in the city centre before and after 2003. The comparison of the two periods suggested an increase in malaria transmission intensity in urban settings across sub-Saharan Africa after 2003 [11, 13, 31, 39, 41]. Transmission estimates surpassing 50 infected bites/person/year were frequently reported in cities across Africa supporting the existence of high parasite reservoirs in urban settings including migrants coming from highly endemic rural settings or population moving from urban to rural settings which could be infecting mosquito populations [30, 37]. It is also possible that the introduction of new techniques for the detection of Plasmodium infections in mosquitoes, such as ELISA and PCR techniques which were not used before could have increased the EIR estimates [42‐44]. These highly sensitive techniques were reported to overestimate the true infection rate after salivary gland dissection by 1.1 to 1.9 folds [45‐48]. The use of new molecular techniques or genomic advances could be vital for malaria control and elimination in Africa and there is a need to promote the use of new techniques to improve malaria vector control and surveillance in Africa [49].

The study also indicated high diversity of the vectorial system in different cities [12, 50‐53]. Yet members of An. gambiae complex were largely predominant in most urban settings [11, 14, 54, 55]. This is in conformity with these species capacities to adapt to anthropogenic and/or environmental changes and to feed exclusively on humans [56]. The preferential breeding habitats of species of the An. gambiae complex are temporary water collections exposed to sunlight. However, these species were reported to also breed in different types of habitats, including drains, septic tanks, artificial containers, standing water collection full of organic matters in urban settings [2, 15]. Moreover, it appears from the study that species composition could vary significantly between cities [51]. The following observation, highlights the influence of different factors genetic and tolerance level shaping the adaptation capacity of species in different environments [57, 58]. In the city of Yaoundé, the predominance of An. coluzzii over An. gambiae was attributed to the high tolerance of the species to organic pollutants, such as ammonia [59]. In coastal cities along the Atlantic Ocean, such as Libreville and Malabo, An. gambiae was found to be highly predominant whereas it was less abundant in Douala where An. coluzzii was the predominant species [60]. Explaining species distribution relying only on species specific data could be more complex as highlighted in a recent meta-analysis [61] and deserve further investigation. Urban agriculture coupled with uncontrolled disposal of containers to collect rainwater is creating an increasing number of favourable aquatic breeding habitats for Anopheles in urban cities. It has been reported that some Anopheles species are now adapting to this new environment, as described for An. stephensi, which breeds in man-made water containers, such as household water storage containers and garden reservoirs [24, 62]. The invasion of Africa by new species, such as An. stephensi, which is now found in many countries across East Africa such as Djibouti, Somalia, Sudan, and Ethiopia, could pose a great challenge for malaria elimination in Africa particularly in urban settings [1, 23, 63‐65]. The invasion of Djibouti by Anopheles stephensi in 2012 was associated with a 30-fold increase in malaria cases, from 1684 in 2012 to 49,402 in 2019 [1]. Anopheles stephensi was also reported to display high resistance to pyrethroids, carbamates and organophosphates [64]. The species bites outdoors and displays a highly opportunistic behaviour feeding on both human and animals, a behaviour which could affect the efficiency of current control measures [64].

Some cities exhibited a high species diversity with three to six species commonly reported whereas low species diversity was recorded in others. This heterogeneity between cities could derive from difference in vegetation, altitude, urbanization level and seasons [66‐70]. The presence of forest fringes as observed in the close neighbourhood of some cities [51] could increase the number of potential breeding sites exploited by mosquitoes and explain the diversity. Mosquitoes found in the urban environment are also exposed to a high selection pressure induce by the use of insecticide-treated nets, pollution, deforestation, anthropogenic changes and environmental changes which could reduce the diversity and distribution of species [15]. Indeed high intensity insecticide resistance affecting almost all insecticide families was reported in An. gambiae s.l. populations from most urban settings [12, 19, 71‐73]. The rapid expansion of multiresistance pattern was reported to reduce bed nets efficacy in different epidemiological settings [74‐76]. In urban settings where vector populations display resistance to insecticide, and outdoor feeding behaviour [11], the addition of targeted interventions such as larval control in hotspot areas could be keys for effective reduction of malaria transmission.

Plasmodium falciparum was the predominant malaria parasites recorded in almost all urban settings. This parasite is also the dominant species in rural settings [77]. Other species commonly found included Plasmodium malariae and Plasmodium ovale [53]. It is likely that the diversity of Plasmodium species in urban settings could be on the rise due to the intensification of travels between different regions of the globe. The exploration of factors favouring mosquito nuisance and malaria transmission in urban settings clearly shows the influence of urban expansion resulting from rapid population growth outpacing infrastructure development and highlight the need for further action by municipalities and public works services in the construction of drains or sewage systems to reduce breeding opportunities for mosquitoes [13].

The current review provides an update of the situation of malaria in urban settings in sub-Saharan Africa during the last decades. Although the risk of malaria transmission remains low in urban compared to rural settings, urban malaria is likely to increase as unplanned urbanization continues. Unplanned urbanization led to a proliferation of suitable breeding habitats for malaria vectors and thus increases the risk of exposition to mosquito bites and malaria transmission. To stop this trend in the disease burden, concerted actions need to be taken quickly at different levels to improve the management of malaria cases and control of vector populations. The development of integrated control approaches could be paramount for the effective control of vector-borne diseases in urban settings.