This review shows the geographical distribution of A Pf EIR estimates across sub-Saharan Africa, the region at greatest malaria risk in the world , and highlights the vast gaps in knowledge on the transmission of this devastating disease. The fact that only half the countries of sub-Saharan Africa have data available on transmission intensities is of great concern. This dearth of fundamental data raises questions about how current large scale vector control, malaria elimination and eradication programmes currently underway across the continent can develop realistic plans to achieve their goals [43–49]. It emphasizes the need for systematic sampling across a wider geographical area, to include a more diverse range of demographic and ecological settings.
The highest number of A Pf EIR estimates were taken in rural populations, in particular in locations with <100 person per km2(n = 130). Very few measures were taken in urban areas where the population density was high i.e. > 1,000 per km2. Hence, there is a pressing need to know more about urban population transmission dynamics, given the rapid urbanization currently taking place across the continent . It is predicted that more than 60% of the population in sub-Saharan Africa will be urban dwelling by 2020. The examination of modelled population density to define differing demographic trends, suggests that they may be preferable to the urban-rural categories defined by Hay et al , which are potentially subjective e.g. urban areas can vary greatly in population density as elucidated in the three case studies.
Importantly, there was also great variation in the number of estimates taken in areas of different elevations and months of climate suitability. Approximately 40% of the A Pf EIR estimates were taken at elevations of <100 m, and these were, on average, significantly lower than all those taken at higher elevations. This apparent lower risk at lower elevations may be associated with the measurements taken in coastal locations where mosquito species such as An. melas and Anopheles merus prevail, but are considered to be poor vectors of malaria [36–38, 51–53]. It may also be related to urban populations, which are usually located at lower elevations and have better access to anti-malarial drugs . More importantly, nearly 80% of A Pf EIR estimates were taken in areas where climate suitability  was six months or less. This results in estimates from short transmission periods being extrapolated to average annual rates, thereby introducing inaccuracies. This points to whether A Pf EIR estimates would be better presented as monthly measures over a year, highlighting the seasonality, as well as local demographic and ecological factors such as interventions, community wealth and land use e.g. irrigation, which could potentially shorten or prolong the transmission season(s).
Bivariate correlations indicated that population density, elevation and climate were all significantly related to A Pf EIRs and important factors influencing the risk of transmission. Whilst these data and analyses are crude, in the absence of ground-truth data they provide some useful insights into potentially important associations, which can be followed up in more detail and depth. This work also highlights the advantages of using state of the art GIS tools and remote sensing (RS) technologies , especially with changes in population and climate becoming increasingly important to monitor in under-resourced regions of the world such as sub-Saharan Africa [8, 9].
The work on the methods used to measure A Pf EIRs is the most comprehensive review available. It highlights the overall increasing trend over time with a total of 21 measurements recorded in 1980–84, compared with 71 in 1995–99. Of note, however, few transmission studies have been undertaken in recent years. The reason for this lack of work is unclear, but may be related to the limited infrastructure and overall lack of financial resources, trained staff, vector ecologists and medical entomologists on the ground . This may also explain why the methods have varied so much over time, with the more labour intensive and specialized method of HBC to catch blood-fed mosquitoes and the sporozoite dissection technique, being replaced with different combinations of PSC, light traps, ELISA and PCR, which are quicker and simpler. This shift in methodological approaches is probably due to both a lack of human and financial resources, and ethical reasons related to the increasing prevalence of drug resistance across the continent .
The use of so many different methods has reduced the ability to compare malaria transmission dynamics within and between populations over time. Although there have been attempts to calibrate and understand the relationship between the different HBC [58–64] and sporozoite detection [65–72] methods, the advantages and disadvantages of each method have not been thoroughly examined, and it is still not known how they compare over long periods of time in different settings. This highlights the need for a simpler and more standardized method for measuring A Pf EIRs, a point previously emphasized by Service  and Hay et al . Alternative approaches such as the use of immunological tools (in combination with entomology) also need to be considered, as they have the potential to evaluate the medium- and long-term trends of transmission, and determine the influence of Anopheles vectors species on the regulation of antibody responses to P. falciparum [73–75]. This is critical for future studies to better understand the complexities of transmission and the impact of the changes occurring across Africa in terms of urbanization, climate change and large-scale intervention and control programmes involving the mass distribution of ITNs and extensive IRS [43–49].
This current study shows that there are clear and significant differences between urban and rural populations, when A Pf EIRs are measured using all methods (in accordance with Hay et al ), or HBC and dissection. However, these trends were not evident when other method combinations were used, nor when other demographic and ecological factors were stratified by different methods. The reasons may be that there is great variability within each method, and transmission heterogeneity within each location [76–79], both important factors that potentially were not taken into account. Most studies provided little or no explanation regarding mosquito distribution patterns, the rationale behind the choice of locations, houses, or trap placements, nor information on the human collectors, time of day, or frequency of mosquito collections. Further, it was found that PSC-based studies [80–83] did not routinely adjust for the different feeding and resting patterns of the mosquito species, an omission, which may be important in locations where vectors often rest outdoors after feeding e.g. Anopheles arabiensis .
Although they are difficult to measure, phenotypic variables like exophily, and genotypic variation in vector competence are also important considerations. Our simple comparisons between An. gambiae s.l and An. funestus presence show how crucial it is to take the Anopheles species characteristics and ecological niches into account. Malaria transmission appears to vary greatly by mosquitoes species, depending upon the land use, population density, elevation and climatic parameters . Overall, A Pf EIRs were twice as high in locations where both An. gambiae s.l and An. funestus were present, compared with locations which only comprised An. gambiae s.l. The greatest differences and highest A Pf EIRs occurred in locations of low population densities i.e. rural, those at elevations of 500 to 1,000 m and where periods of suitable climate exceeded six months.
These preliminary findings indicate that An. funestus is an important, yet potentially underappreciated, vector contributing to high levels of malaria transmission across sub-Saharan Africa. This may help to explain why some populations in close proximity have vastly different A Pf EIRs, as exemplified in Senegal, in the village of Dielmo where An. funestus was abundant and transmission 10× higher than the village Ndiope (5 km away), where An. funestus was rare [17, 18]. Furthermore, An. funestus is seldom found in urban areas, and, where rainfall is confined to a single season each year, is typically most abundant at the end of that season and beginning of the dry season that follows [17, 75, 76, 85–89]. Hence, in line with the other factors considered here, one important role of An. funestus is in extending the transmission season in rural areas. More specific research on this vector species is critical – it is a notoriously difficult vector to find in the field, catch and colonise.
The three case studies presented in this paper provide further insight into the ecological factors influencing the diverse mosquito distributions and P. falciparum malaria epidemiology across sub-Saharan Africa. Of note, and perhaps of most concern is the great variation in risk that occurs within relatively small geographical areas, especially in and around urban areas. The implications for a growing urban Africa are unclear. Will urbanization decrease the risk of malaria? Will the mosquito vectors commonly found in peri-urban or adjacent rural areas adapt to urban environments and increase the risk of malaria? How will we measure this? An improved approach to measurement will have numerous ramifications, some perhaps not widely anticipated. For instance differences in transmission intensity, and corresponding immunity, might help to explain circumstances in which frequencies of drug failure differ, far more than frequencies of drug-resistance markers, between urban and surrounding rural areas . This review highlights the complexity and multiplicity of malaria transmission, and serves as a foundation from which to move forward, to develop sensible and realistic methods for measuring malaria transmission in Africa today and for the future.