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1. Introduction
In most tropical countries, malaria remains a major cause of morbidity and mortality (Chanda et al.
2012; Sokhna et al. 2017) where an estimated 3.2 billion people are at risk of contracting the disease.
The disease is transmitted to humans by infected female Anopheles mosquitoes (Hoshen and Morse
2004; Ogunbadewa 2012; Ruktanonchai et al. 2016). Malaria impedes human economic development
by reducing savings and worker productivity (Ogunbadewa 2012). In addition, countries with high
malaria burden incur high medical costs estimated into hundreds of millions of dollars in fighting
the disease (Sachs and Malaney 2002; Guinovart et al. 2006). In the last 15 years, malaria burden has
considerably declined; for example, global malaria incidence declined by about 41% and mortality
rates by 62% between 2000 and 2015 (Patouillard et al. 2017; Yakob et al. 2017). The decline resulted
mainly from sustained large-scale vector control and case management (Bhatt et al. 2015). The decline
in malaria mortality and malaria incidence can be sustained by adoption of spatial techniques that
provide important insights into malaria epidemiology of a country hence the need for malaria strat-
ification. Despite significant successes achieved in controlling malaria, the disease still ranks among
the top three most deadly tropical parasitic diseases (WHO 2016). This has mainly been due to the
close link of the disease to the environment, particularly its relationship to temperature and rainfall
variables. Thus, understanding the nature of the relationship between malaria occurrence and envi-
ronmental variables is critical for its control.
Malaria risk stratification is recommended by the World Health Organization as it helps in tailoring
malaria interventions to local contexts as part of the global technical strategy to eliminate malaria by
2030 (Bhatt et al. 2015; WHO 2016). Several malaria risk stratification schemes exist. They include
schemes which demarcate geographic regions into malaria risk zones using climate-based predic-
tive models that generate the probability of malaria infection in an average year (Craig et al. 1999;
Hoshen and Morse 2004). Other stratification schemes delineate malaria risk zones by incorporating
inter-annual variation in malaria incidence as well as environmental factors superimposed on the
underlying average risk of malaria (Ceccato et al. 2007). Such stratification schemes depend on the
proper definition of risk. Malaria risk results from an array of factors that relate to the presence and
density of vectors and parasites, all of which vary in space and time (Alimi et al. 2016). Thus, malaria
risk is defined as the environmental space characterized by the intersection of malaria vector suitability
and malaria prevalence. This operational definition of malaria risk paves way for using a stratifica-
tion approach in which malaria prevalence data are combined with vector suitability in a geographic
information system (GIS) to stratify a region into distinct malaria risk zones.
The environmental dependence of malaria, particularly on temperature and rainfall, has been
widely documented (Lindsay et al. 1998; Craig et al. 1999; Lindsay and Bayoh 2004; Drakeley et al.
2005; Mabaso et al. 2006; Patz and Olson 2006; Paaijmans et al. 2010). However, quantification of
the interaction of several determinants of malaria occurrence in space and over time (Bousema et al.
2012; Mosha et al. 2013) which is important for the determination of malaria risk zones still remains
rudimentary. It is thus, important to develop methods that delineate malaria risk zones and their
spatial dynamics as a first step towards targeted control of the disease. Recent advances in GIS-based
methods coupled with improved spatial data capture methods to exploit the environmental datasets
(Ngarakana-Gwasira et al. 2016) provide an opportunity to map malaria risk zones. GIS has been
successfully used to model malaria risk and is increasing useful to locate the foci of infection and
predict the potential distribution of diseases (Tanser and Le Sueur 2002).
In this study, ecological niche modelling using the maximum entropy (MaxEnt) algorithm was
applied to predict malaria vector habitat in terms of key bioclimatic and biophysical variables.
Predictive modelling of geographic distribution of malaria vectors based on ecological niche is an
important indirect indicator of malaria risk in an area. The output continuous vector suitability map
was then weighted and combined with malaria prevalence data to delimit malaria risk zones for
Zimbabwe using GIS. The malaria risk zones were validated by malaria case data which were not
used in the model training. The approach used is based on the premise that about 70–90% of malaria
risk is associated with environmental factors which in turn influence the abundance and survival of
the vectors (Baird et al. 2002; Smith and McKenzie 2004; de Castro et al. 2007; Ye′ et al. 2009). Thus,
a combination of vector suitability with prevalence data was hypothesized to result in an improved
malaria risk zone map for the country. The existing malaria risk map has four zones delimited in
correspondence with the less than 600, 600–900, 900–1, 200 m and greater than 1200 m altitudinal
classes (Taylor and Mutambu 1986). By using a combination of vector suitability and malaria preva-
lence data, we hypothesize that this will result in an improved malaria risk zone map. This is because
in Zimbabwe, malaria risk zones have previously been delimited using altitude and prevalence data
only (Taylor and Mutambu 1986). These risk zones do not take into consideration fine-scale spatial
variation in vector suitability throughout the country.
Figure 1. Conceptual framework illustrating the interactions of malaria vector, the host and the environmental space that shape
malaria transmission intensity. The transmission intensity can then be classified into malaria risk zones and mapped to inform disease
management based on the disease triangle.
suitability in turn provides the basis for malaria occurrence as long as there is a host (human beings)
in contact with the vector (an infected mosquito that transmits plasmodium parasites). Thus, when the
environment is conducive for the development and survival of malaria vectors, it is hypothesized to
support high populations of the vector thereby increasing the rate of pathogen transmission resulting
in high disease prevalence (Wilson 2010). In contrast, an environment that provides conditions outside
the tolerance levels of the vector will support low or no populations of the vector. This scenario results
in limited transmission of the malaria pathogen leading to low disease prevalence or the absence of
the disease in an area. Between these two extremes, suboptimal environmental conditions will support
moderate populations of the vector. This results in intermediate transmission of the malaria pathogen
leading to moderate prevalence. In this regard, the disease triangular model can be used to represent
the reciprocal effect of agent, host and environment which aids understanding and prediction of
patterns of disease (Fastring and Griffith 2009). Hence, the disease triangle can be used to predict
epidemiological outcomes locally. Thus, the epidemiologic triangle permits objective stratification of
geographic regions into distinct malaria risk zones using the level of malaria prevalence and vector
habitat suitability as illustrated in Figure 1.
4 I. GWITIRA ET AL.
Figure 2. Average malaria prevalence mapped at district level in Zimbabwe based on incidence data for the period from 2005 to 2014.
wetness index (TWI) was included as the sixth predictor variable because previous research found
it more useful for predicting malaria risk compared to land use and landcover (Cohen et al. 2010;
McCann et al. 2014; Alimi et al. 2015, 2016). TWI was calculated as follows;
TWI = ln(𝛼∕tan(𝛽)) (1)
where ln is the natural logarithm, α = specific catchment area and β is the slope in radians. Altitude
and TWI raster maps were re-sampled to a 1 km spatial resolution to match the pixel size of the
bioclimatic variables.
3. Results
3.1. Predicted habitat suitability for common malaria vectors
Figure 3 shows the probability surfaces indicating habitat suitability for the three common malaria
vectors in Zimbabwe. Figure 3(a) illustrates that the probability of occurrence of A. arabiensis is high
in the south-east, north-east, northern and north-western parts of Zimbabwe. By contrast, the central
and southern parts of the country are characterized by low probability. It can be observed that A.
funestus has a restricted suitable habitat confined to the eastern region of Zimbabwe. The probability
of occurrence of A. merus has a similar pattern to A. arabiensis although the highest probability is in
8 I. GWITIRA ET AL.
Figure 3. Modelled habitat suitability for (a) A. arabiensis, (b) A. funestus, (c) A. Merus and (d) combined habitat suitability for all the
three malaria vectors in Zimbabwe.
the north and north-western parts of Zimbabwe. Comparatively, A. arabiensisis is the most widespread
malaria vector in Zimbabwe.
The results for the combined probabilities of occurrence of the three vectors are illustrated in Figure
3(d). The north-western, northern, eastern and south-eastern regions of the country are characterized
by high probability of occurrence while the central and south western parts of the country are char-
acterized by low probability of occurrence. Model validation results illustrate that habitat suitability
was predicted with high accuracy. The AUC values based on training data achieved were 0.80, 0.93
and 0.97 for A. arabiensis, A. funestus and A. merus, respectively.
Figure 4 presents the five stratified malaria risk zones for Zimbabwe. Zone 1, which is predicted
free from malaria but experiences sporadic malaria, extends from the south-western to the central
regions of the country where it narrows. Zone 2 has the same spatial pattern to zone 1 except that it
is more expansive and extends farther into the interior of the country. Zone 5, characterized by high
and perennial malaria risk occupies the southern, eastern, northern and north-western regions of
the country.
Zone 4 characterized by high and seasonal malaria has a crescent shape. It extends inwards into
the country from the south-western, eastern, north-eastern, northern and north-western regions of
the country. Zone 3 classified as experiencing moderate and seasonal malaria lies in between zones 2
and 4. Table 2 shows the area occupied by each malaria risk zone and the density of health facilities
per risk zone.
GEOCARTO INTERNATIONAL 9
Figure 4. Distribution of five new malaria risk zones for Zimbabwe derived from k-means classification of a malaria risk continuous map.
Table 2. Variation in the density of health facilities among the five malaria risk zones in Zimbabwe.
The results illustrate that Zone 4 is the largest by area while Zone 1 is the smallest. In terms of
density of health facilities we observe that there is a lower density of health facilities in zones with the
highest malaria risk and vice versa. Specifically, zone 1 which has the lowest risk has a higher density
of health facilities than Zone 4 which has a higher risk.
Results of Kruskal–Wallis analysis indicate significant differences in the median number of malaria
cases among some of the five malaria-risk zones. There are statistically significant differences in malaria
cases among the five zones (Kruskal–Wallis X2 = 33.624, p = 0.00). Figure 5 illustrates a linear increase
in malaria prevalence from zone 1 to zone 5 with zones 1 and 5 having the least and highest malaria
prevalence, respectively. Although overall, there is a statistically significant difference in malaria cases
among the five malaria risk zones, results of post hoc analysis illustrate that the differences are not
significant between predominantly spatially adjacent zones, i.e. zone 1 and 3, zone 2 and 3, zone and
4 and 5 (p > 0.05). Malaria risk was significantly higher in zone 2 compared to zone 1 but the median
malaria cases for zone 3 did not differ from those of zone 2 suggesting existence of an overlap. Zone
4 had a higher median number of malaria cases compared to zones 1, 2 and 3, separately. Zone 5 also
had a significantly higher median number of malaria cases compared to the other zones except zone 4.
Overall, these results illustrate the existence of spatial overlaps among neighbouring malaria zones,
for example zone 2 and 3 as well as zone 4 and 5. This does not hold for zones 1 and 2 as well as zones
3 and 4, which were successfully discriminated from each other. Figure 6 shows the spatial overlaps
that exist among adjacent zones.
10 I. GWITIRA ET AL.
45
c
40
35
c
25 b
20
15
b
10
5 a
0
Free/SporadicLow and short Moderate and High and High and
seasonal seasonal seasonal perennial
Malaria Class
Figure 5. Variation in malaria prevalence among the five new delimited malaria risk zones based on the 2015 malaria prevalence data.
the vector distribution may be contributing to the occurrence of malaria in areas that used to be malaria
free. We thus, deduce that mosquito habitat suitability in combination with malaria prevalence data
can be successfully used to demarcate malaria risk zones for targeted malaria control interventions.
In general, the spatial distribution of malaria prevalence mirrors the probability of occurrence of
major malaria causing vectors in Zimbabwe. This suggests that the probability of occurrence of the
major vectors of malaria may be a key determinant of malaria prevalence (Cox et al. 2014). This explains
the observed pattern of malaria prevalence where regions to the south-east, east, north-east, north
and north-west are characterized by high prevalence and corresponding high vector habitat suitability.
Based on the ecology of malaria, areas with conducive conditions for the survival of malaria vectors
may explain the high malaria prevalence (Noor et al. 2012). Therefore, the use of a combination of
vector suitability and malaria prevalence which is dependent on presence of malaria causing vectors
may be useful in the stratifying different geographic units into different malaria risk zones.
Results of this study indicate that environmental suitability is primarily important in understand-
ing malaria risk (Graves et al. 2009). In this study, we found altitude, isothermality, temperature
seasonality, annual precipitation, topographic wetness index and precipitation of wettest month as
important factors in predicting the habitat suitability of the three key malaria vectors. These results
are consistent with Levine et al. (2004) who also found the same factors to be relevant for predicting
the vector habitat although at a continental scale. In fact, precipitation derived factors are known to
be key in determining the habitat suitability of mosquito species as they provide breeding sites for the
mosquitoes while temperature derived factors are key in the mosquito life cycle (Bødker et al. 2003;
Paaijmans et al. 2010). However, the utility of environmental variables in determining malaria risk is
augmented by prevalence data.
Given that bioclimatic variables are now readily available combined with the fact that most malar-
ious countries have well-established malaria surveillance systems through health management infor-
mation systems, the use of a combination of vector suitability and prevalence data offers more accurate
malaria stratification than use of prevalence data or vector suitability in isolation. We contend that
by including the ecology of the vectors we can improve the accuracy of malaria risk classification
as ecological determinants are a useful supplement to epidemiological data (Schapira and Boutsika
2012). In addition, by using both the vector suitability and malaria prevalence data, we can rely on the
environment-host-agent relationship as key concepts in understanding malaria risk.
This study differs from previous studies in that the stratification scheme that was used combines
vector ecology and malaria cases. Previous studies mainly relied on stratification schemes which used
either vector ecology or malaria prevalence separately (Taylor and Mutambu 1986). The results imply
that by taking the into consideration the key elements of malaria epidemiology (e.g. vector ecology and
malaria case prevalence) an appropriate mix of interventions can be implemented. While acknowl-
edging that as countries progress towards elimination, it is important to carry out micro-epidiological
stratification (Bannister-Tyrrell et al. 2017), the use of coarse-scale data (e.g. collected at district and
regional scale) adopted in this study may be used as a bench mark for future fine-scale stratification.
We however recommend that in future molecular epidemiological data should be included to further
characterize malaria occurrence. Furthermore, we suggest that results of this study be used by National
Malaria Control programmes (NMCP) to design malaria interventions by malaria risk zone rather
than using malaria prevalence data in isolation.
Acknowldgements
We acknowledge the contribution of the Ministry of Health and Child Care and the Health Research Institute for availing
vector species data and malaria case data used in this study.
Disclosure statement
No potential conflict of interest was reported by the authors.
12 I. GWITIRA ET AL.
Funding
This work was conducted under the auspicies of the Ministry of Health and Child Care in Zimbabwe as a part the Malaria
re-stratification project and funded by the Government of Zimbabwe under the National Malaria Control Programme.
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