Topography as a modifier of breeding habitats and concurrent vulnerability to malaria risk in the western Kenya highlands
© Atieli et al; licensee BioMed Central Ltd. 2011
Received: 8 November 2011
Accepted: 23 December 2011
Published: 23 December 2011
Topographic parameters such as elevation, slope, aspect, and ruggedness play an important role in malaria transmission in the highland areas. They affect biological systems, such as larval habitats presence and productivity for malaria mosquitoes. This study investigated whether the distribution of local spatial malaria vectors and risk of infection with malaria parasites in the highlands is related to topography.
Four villages each measuring 9 Km2 lying between 1400-1700 m above sea level in the western Kenya highlands were categorized into a pair of broad and narrow valley shaped terrain sites. Larval, indoor resting adult malaria vectors and infection surveys were collected originating from the valley bottom and ending at the hilltop on both sides of the valley during the rainy and dry seasons. Data collected at a distance of ≤500 m from the main river/stream were categorized as valley bottom and those above as uphill. Larval surveys were categorized by habitat location while vectors and infections by house location.
Overall, broad flat bottomed valleys had a significantly higher number of anopheles larvae/dip in their habitats than in narrow valleys during both the dry (1.89 versus 0.89 larvae/dip) and the rainy season (1.66 versus 0.89 larvae/dip). Similarly, vector adult densities/house in broad valley villages were higher than those within narrow valley houses during both the dry (0.64 versus 0.40) and the rainy season (0.96 versus 0.09). Asymptomatic malaria prevalence was significantly higher in participants residing within broad than those in narrow valley villages during the dry (14.55% vs. 7.48%) and rainy (17.15% vs. 1.20%) season. Malaria infections were wide spread in broad valley villages during both the dry and rainy season, whereas over 65% of infections were clustered at the valley bottom in narrow valley villages during both seasons.
Despite being in the highlands, local areas within low gradient topography characterized by broad valley bottoms have stable and significantly high malaria risk unlike those with steep gradient topography, which exhibit seasonal variations. Topographic parameters could therefore be considered in identification of high-risk malaria foci to help enhance surveillance or targeted control activities in regions where they are most needed.
One fifth of the African population lives in malaria epidemic prone areas (desert fringes and highlands)  where all age groups are at risk of clinical malaria due to the limited acquired immunity. The prevention of malaria in these vulnerable populations is one of the priorities for the governments, African leaders and international agencies . In Kenya, transmission of Plasmodium falciparum in the highlands has been a re-emerging problem in several regions in the last three decades . The malaria situation has been getting worse partly due to resistance to anti-malarial drugs and lack of sufficient vector control measures [4, 5]. Furthermore, it has been demonstrated that malaria epidemics in the Western Kenya highlands are partly driven by climate variability [6, 7]. The impact of malaria epidemics on human morbidity and mortality may become more severe because climate variability is predicted to become more frequent and intense . Understanding the epidemiology of malaria transmission and variations that occur within areas with close proximity in the highlands would support the improvement of an area specific national strategy plan for prevention and transmission control. It is therefore, necessary to explore possible factors fuelling these changes in transmission so as to identify vulnerable villages to allow interventions to be directed at these high-risk communities .
Topography has long been recognized to be one of the factors associated with malaria [9, 10] due to its association with cooler temperatures that slow the development of anopheline vectors and the Plasmodium parasites they transmit [5, 11]. The topography of the highlands comprises hills, valleys and plateaus. Rivers and streams run along the valley bottoms in the valley ecosystem and swamps are a common feature. Unlike in lowland plains, where drainage is poor and mosquito breeding habitats have an extensive distribution, the majority of breeding habitats in the hilly highlands are confined to the valley bottoms because the hillside gradients provide efficient drainage . Variation in the local shape of the land may also play an important role in determining regions of suitability for mosquito breeding at smaller spatial scales . Depending on the variation in local valley shape, malaria risk may diminish within a few hundred meters from known breeding sites [14, 15], although a number of vector and environmental factors have been found to influence this range [16, 17].
As characterized by Balls et al. in Tanzania, the risk of malaria in the highland region is a broad altitudinal trend modified at smaller spatial scales by local topography . Within the highlands, there are broader valleys with slow gradients while others are narrower with stiff gradients. The broader valleys with 'U' shaped bottoms tend to have fairly extensive distribution of breeding habitats compared to the narrow 'V' shaped valleys. Many vector control efforts assume the same strategy of malaria control. While this may be largely true in the lowlands, such an assumption is not true in the highlands. This assumption may lead to expensive and extensive control efforts. It would be advisable to categorize the villages for targeted interventions. Recognizing and understanding consistent foci of these ecological factors would therefore permit control efforts to be directed at specific geographic areas, reducing costs and increasing outcome. Using topography as a factor, this study assessed spatial patterns of mosquito larval breeding habitats, vectors and malaria incidence in four villages with variation in local valley shape in an epidemic-prone area of the Western Kenyan highlands.
Digital elevation model
The elevation differences between upstream and downstream drainage points were determined to indicate the efficiency of drainage thus the stability of the breeding habitats. The surface area with no slope at the bottom of the valleys was determined. Valley shape is one of the terrain characteristic which is a key driver to malaria in the highlands . The U-shaped valleys were defined as broad valleys with slow moving rivers or streams and have poor drainage. Their river flow slope change rate is 1% and with a flat surface from the river edge of > 10 meters. On the other hand, the V-shaped valleys have a narrow bottom with a fast flowing river or stream and have good drainage. Their river flow slope change rate is 10% and with a flat surface of < 10 meters from the river edge (Githeko et al. unpublished data). These parameters were compared in a pair of villages within narrow V-shaped and another pair within flat-bottomed U-shaped valleys to determine whether there is consistency in the characteristics as explained above. The difference in topographic parameters between broad and narrow valley and their association with occurrence and stability of malaria risk was determined.
Selection of study houses and participants
Using a handheld GPS unit, coordinates of all houses within the sites were numbered and mapped. A hundred and twenty houses were randomly selected from each of the four villages making a total of 480 houses. In each village, 60 houses were assigned from both sides of the river from the valley bottom to uphill. Owners of selected houses were requested to sign a freely administered informed consent form while guardians of minors signed assent forms for participation in the study, and for entomologic, parasitological and questionnaire surveys.
Adult indoor resting mosquitoes were collected using the Pyrethrum Spray Collection (PSC) method  during the dry (February-March 2010, low transmission season) and the rainy (November-December, 2010, high transmission season) seasons from all the study houses (120 houses from each village in each season). Likewise, larval distribution surveys were done during the same period concurrently. A field team comprised of a researcher, technician and field assistant who surveyed the entire village for all aquatic habitats. Twenty dips were made in each habitat using a standard dipper (350 ml) manufactured by Bid Quip Products, Inc. California, USA. Small habitats were dipped as many times as possible. Larval densities were then adjusted to larvae per dip. Aquatic habitats with or without anopheline presence were identified, recorded and characterized into habitat type. Similarly, using handheld GPS, these habitats were mapped. Samples were taken to the Kenya Medical Research Institute (KEMRI) laboratory in Kisumu, for counting and morphological identification to species, and adult mosquitoes were classified according to their gonotrophic stages.
Malaria infection survey
Occupants from study houses sprayed each season for vector collection, (who freely consented to participate in the study), were screened for malaria parasites during both the dry and the rainy season. Thin and thick blood smears were taken in the field and the slides were stained with 4% Giemsa for 30 minutes . Households with absentees were revisited the following day to recruit those missing at the first visit. Symptomatic participants with positive slide tests were offered free treatment with artemisinin-based combination therapy (ACT) at the nearby health facility according to Kenya national MOH guidelines . Participants with complicated malaria cases during our survey were advised to visit the nearest health facility and transportation was provided for those who needed help to get to the facility.
Data was collected and entered in Excel spread sheets (Microsoft Corporation) and statistical analysis was performed by the use of STATA SE 9 (StataCorp LP, 4905 Lake Way Drive, College Station, TX 77845 USA). Study results were categorized into two, those closest (≤ 500 m) to the main river line valley where the majority of breeding habitats occurred at the valley bottom (VB) while those above that distance of 500 m were considered to be uphill (UH). A distance of 500 m was chosen having been used successfully elsewhere , although published distance of risk gradients vary  and sharp declines in risk are generally reported at greater distances . For comparison, density/house of indoor collected vectors, positive larval occurrence and abundance and the rate of malaria within the valley bottom and uphill between broad and narrow shaped valley villages were calculated.
During analysis, data from the two broad valley villages were grouped together, likewise those from the two narrow valley villages were grouped together after preliminary results confirmed that in addition to their topographic aspects similarity, there were no intra-specific differences in both adult vectors and larval abundance and distribution characteristics. To determine whether there were differences in the abundance of adult vectors between the valley bottom and uphill in each particular village, i.e. broad and narrow shaped valley villages, density of vectors/house in houses located at the valley bottom were compared by t-test to those located uphill during both the rainy and the dry season. Similar comparisons using chi-square test were done to determine the difference in occurrence of positive larval habitats between areas located at the valley bottom and uphill during the dry and the rainy seasons in the broad and narrow shaped valley villages. Chi-square test was carried out to examine whether patterns of malaria surrounding households closer to the valley bottom locations might appear analogous to those uphill in broad and narrow shaped valley villages during both the rainy and dry seasons. Inter valley shape comparison between broad and narrow shaped villages were done comparing adults, larval and malaria occurrences. As for the abundance and distribution of adult vectors, a t-test was used, whilst a chi-square test was used for both positive larval habitats and malaria cases. Multivariate analysis- Tukey HSD test was done to determine the most predictive independent variable among valley shape, altitude and season for the occurrence of larvae, adult vectors and malaria cases as dependent variables.
Ethical clearance was obtained from the Ethical Review Committee of Kenya Medical Research Institute, "Ecology of African highland malaria (II), SSC No. 1382 (N)" dated May 15th 2008 and the Institutional Review Board of the University of California at Irvine. A freely administered informed consent with interpreters was given to residents for participation in the study.
Larval habitats survey
Summary of vector densities and parasite prevalence by valley shape and season
An. gambiae s.l
Adults vectors density/house
An. gambiae s.l
Parasite prevalence (%)
Percentage of habitats with malaria vector larvae within valley bottom and uphill locations in different valley shapes and different seasons
Rainy season (2009)
Dry season (2010)
Adult malaria vector survey
Percentage of houses with malaria vectors within valley bottom and uphill in different valley shapes and seasons
Dry season (2010)
Malaria infection rates
Malaria parasite positive rates in participants within valley bottom and uphill in different valley shapes and different seasons
Dry season (2010)
Malaria risk mapping requires inclusion of factors related to vector distribution, human-vector contact, human practices, and the environmental context in which they occur . Highland topographic features restrict the spatial distribution of vector breeding habitats confining them to the valley bottom [12, 27]. Furthermore, it restricts high intensity of exposure to malaria at the valley bottom resulting in a heterogeneous incidence of morbidity when compared to hilltop. Identification of area specific topographic features has important implications in classification of malaria epidemiology for specific micro-regions. Moreover, accurate prediction of malaria vector occurrence and plasmodium transmission risk is essential in heterogeneous environments to permit focal cost effective intervention strategies and heightened surveillance in the regions that require them the most . Results of this investigation concur with previous studies demonstrating associations between the occurrence of malaria vectors and malaria risk and topographic characteristics, specifically the shape of the valley in the highlands where malaria epidemics occurs. Importantly, however, it demonstrates that factors associated with malaria are not necessarily predictive of it, most likely because strong correlations between environmental factors can lead to confounded relationships.
In highland regions of East Africa, where unstable malaria transmission may result in part from the very low numbers of anopheline mosquito vectors , the proximity of houses to locations with suitable topography for mosquito breeding may be an important determinant of malaria risk . During this study, spatial surveys of the availability of larval habitats and presence of larvae in these habitats showed that, the actual numbers of positive larval habitats in broad valley regions were greater and stable in both the rainy and the dry seasons. In contrast, percentages of positive larval habitats were season dependent in narrow V-shaped valleys with significantly high occurrence during the rainy rather than during the dry season. This can be explained by the fact that unlike the broad U-shaped valleys that are characterized by meandering slow moving rivers, poor drainage and with large surfaces to hold water at the valley bottom suitable for larval breeding, the narrow V-shaped valley systems are characterized by fast running rivers at the valley bottoms. They too have steep slopes that provide good drainage in the area and so there are few vector breeding habitats in these ecosystems. Similarly, during the adult vector survey, households within the broad U-shaped valley had higher densities of vectors per house during both the dry and rainy seasons compared with those within the narrow V-shaped valley. This result concurs with earlier studies in the highlands which indicated that anopheline larval habitats and malaria transmission were generally clustered near the streams and rivers with poor drainage [12, 26]. Broad U-shaped valley regions were therefore suitable for larval breeding and productivity of adult vectors than the steep narrow V-shaped valley regions.
High larval and adult vector abundance within broad rather than narrow valleys further explains why spatial variation in malaria transmission in the highlands is a function of the terrain characteristics . This phenomenon also sheds more light on the reason why there is heterogeneity in malaria transmission in the highlands  and with variations in close proximity areas within the same region. Steep V-shaped valleys experience fast surface water and river flows during the rains. These events do not allow formation of habitats that would stay long enough to sustain survival of the mosquito aquatic life cycle. These ecosystems therefore experience wash effect on potential larval habitats. Habitats with either eggs or newly hatched larvae are often washed down-stream with running water. This fact was evident where vector densities in a narrow valley shape exhibited significant seasonality in distribution while those in broad valleys had similar distribution across the seasons (Figure 6). Probably because of the wash effect, the narrow valley exhibited unusual vector densities during the rainy season. Unlike in the broad valley where there were fairly higher densities of vectors/house during the rainy season, the narrow valley had significantly fewer vectors during the rainy than the dry season. Vector abundance and distribution were associated with valley shape, location and season. Similar studies on vector distribution in this region have shown that low-lying flat areas and reclaimed swamps are highly productive than steep terrains habitats [20, 27, 29, 30]. These findings using topographic parameters to identify area specific larvae and adult vectors spatial distribution can be utilized to characterize risk regions with close proximity for the purpose of targeted larval or adult vector control. Unlike blanket control, a targeted approach would use limited resources with expected greater outcomes.
The magnitude of the differences in vector abundance (2-10-fold difference) and 2-14-fold difference in malaria incidences between the narrow and broad valley regions during the dry and the rainy season respectively was striking, suggesting that even within this small area, risk of malaria ranges from very low to quite high depending on the shape of the valley. The ecological factors independently associated with increased malaria risk in this study - a broad U- shape valley, lower altitude and rainy season - are all physical contributors to increased malaria risk in the highlands [10, 20]. Moreover, the associations of these risk factors with vector abundance and malaria incidence were strong, consistent, similar over the seasons, and highly significant. The results of this study indicate that as a topographic factor, the shape of the valley either broad U-shaped or narrow V-shaped and distance from the valley bottom predicted the presence of both anopheline positive aquatic habitats and indoor malaria vectors and thus are highly predictive of malaria patterns in this small region. People living in areas within the broad valley shape appeared to be at significantly greater risk of fairly stable malaria infections than those living in areas of narrow valley shape. The non-homogeneous distribution of larval breeding habitats and adult vector spatial distribution between these two valley shape ecosystems may, consequently, lead to focal malaria transmission and heterogeneous human exposure to malaria. It can thus be expected that the malaria transmission profile in the highlands is influenced not only by hydrological factors, but also by topographic factors and distance from the foci of transmission. This heterogeneity in transmission can lead to variable stability of malaria transmission in space with some areas having stable and others unstable transmission. This would lead to different sensitivities to epidemics within relatively short distances in the highlands. Future studies should assess the utility of valley shape as a topographic factor for malaria risk prediction across larger and more geographically diverse areas, especially at scales useful for National division of malaria control to target interventions. Such replication of this work will be required before conclusions can be drawn about the utility of these methods elsewhere.
Given the cost of malaria intervention, accuracy of predicting and classifying high-risk foci in unstable malaria transmission regions is crucial. These findings indicate that malaria control programs operating in similar rugged terrain and highland regions might use topographic and local geographic variance to efficiently identify and derive risk maps of locations that are highly suitable for transmission and which may benefit from targeted interventions and enhanced vigilance.
We thank all the participants in the study and the technical assistance of A. Ouko, T. Otieno, C. Otieno, and J. Maritim. This article is published with permission of the Director of Kenya Medical Research Institute. The work was supported by NIH grant R01 A1050243.
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