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GIS-based stratification of malaria risk zones for Zimbabwe

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Geocarto International

ISSN: 1010-6049 (Print) 1752-0762 (Online) Journal homepage: http://www.tandfonline.com/loi/tgei20

GIS-based stratification of malaria risk zones for


Zimbabwe

Isaiah Gwitira, Amon Murwira, Mhosisi Masocha, Fadzai M. Zengeya,


Munyaradzi Davis Shekede, Joconiah Chirenda, Willard Tinago, Joseph
Mberikunashe & Ron Masendu

To cite this article: Isaiah Gwitira, Amon Murwira, Mhosisi Masocha, Fadzai M. Zengeya,
Munyaradzi Davis Shekede, Joconiah Chirenda, Willard Tinago, Joseph Mberikunashe &
Ron Masendu (2018): GIS-based stratification of malaria risk zones for Zimbabwe, Geocarto
International, DOI: 10.1080/10106049.2018.1478889

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Geocarto International, 2018
https://doi.org/10.1080/10106049.2018.1478889

GIS-based stratification of malaria risk zones for Zimbabwe


Isaiah Gwitiraa, Amon Murwiraa, Mhosisi Masochaa, Fadzai M. Zengeyaa, Munyaradzi
Davis Shekedea, Joconiah Chirendab, Willard Tinagob, Joseph Mberikunashec and
Ron Masendud
a
Department of Geography and Environmental Science, University of Zimbabwe, Harare, Zimbabwe; bDepartment
of Community Medicine, College of Health Sciences, University of Zimbabwe, Harare, Zimbabwe; cMinistry of Health
and Child Care, Harare, Zimbabwe; dAbt Associates, Zimbabwe, Harare

ABSTRACT ARTICLE HISTORY


Malaria burden has considerably declined in the last 15 years mainly due Received 17 October 2017
to large-scale vector control. The continued decline can be sustained Accepted 14 May 2018
through malaria risk stratification. Malaria stratification is the classification
KEYWORDS
of geographical areas according to malaria risk. In this study, ecological niche Bioclimatic variables;
modelling using the maximum entropy algorithm was applied to predict ecological niche modelling;
malaria vector habitat suitability in terms of bioclimatic and topographic k-means clustering; malaria
variables. The output vector suitability map was integrated with malaria prevalence; MaxEnt; vector
prevalence data in a GIS to stratify Zimbabwe into different malaria risk zones. habitat suitability
Five improved and validated malaria risk zones were successfully delimited
for Zimbabwe based on the World Health Organization classification scheme.
These results suggest that the probability of occurrence of major vectors of
malaria is a key determinant of malaria prevalence. The delimited malaria risk
zones could be used by National Malaria Control programmes to plan and
implement targeted malaria interventions based on vector control.

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

CONTACT  Isaiah Gwitira  gwitirai@gis.uz.ac.zw


© 2018 Informa UK Limited, trading as Taylor & Francis Group
2   I. GWITIRA ET AL.

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.

1.1.  Conceptual framework


Figure 1 illustrates the conceptual framework that underpins the proposed stratification approach
used in this study. The risk of malaria is dependent on interactions between the host, agent (vector)
and environment (Baird et al. 2002; Fastring and Griffith 2009). In this conceptual model, varying
environmental conditions result in differential probability levels of vector habitat suitability. Habitat
GEOCARTO INTERNATIONAL   3

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.

2.  Materials and methods


2.1.  Study area
The study was conducted in Zimbabwe. The total human population was estimated at 13 million in
2012. About 67% of the population lives in the rural areas (ZIMSTAT 2012). The country is dominated
by communal land ownership interspaced with commercial farming land. The climate is subtropical
with distinct seasons moderated by altitude resulting in relatively humid conditions at high altitudes
(Torrance 1981; Marshall 2010). Altitude varies between 300  and 2 500  m above mean sea level
(a.s.l). Higher altitudes (>1000 m a.s.l) experience cooler temperatures and receive higher amounts
precipitation compared to the lower altitude areas. There is a distinct spatial gradient of rainfall char-
acterized by annual rainfall which decreases from over 1 000 mm in the eastern highlands which
are >2 000 m a.s.l to 350 mm in the western and south-eastern regions of the country located <1 to
000 m a.s.l. Zimbabwe experiences a subtropical climate with three recognizable seasons. These are:
the hot wet season or summer which stretches from mid-November to March; the cold dry season or
winter which stretches from April to July; and the hot dry season or spring stretching from August
to mid-November (Ndhlovu et al. 2017; Swiswa et al. 2017). Mean monthly maximum temperature
varies from 15 °C in July to 24 °C in November (Gwitira et al. 2018).

2.2.  Sources and processing of datasets


2.2.1.  Vector presence data
Geo-referenced data for the three main malaria vectors, Anopheles arabiensis, A. funestus and A.
merus, were obtained from nationwide surveys conducted by the Ministry of Health and Child Care
(MOHCC) between 1999 and 2015. Additional presence data were obtained from 16 sentinel surveil-
lance sites located in districts prone to malaria epidemics in the country. The vector presence data were
also supplemented by presence data accessed from the Global Biodiversity Information Facility-GBIF
(http://www.gbif.org/). A total of 154 presence records for A. arabiensis, 55 presence records for A.
funestus and 134 presence records for A. merus were used to create separate habitat suitability maps
for these three malaria vectors.

2.2.2.  Malaria prevalence data


The MOHCC provided malaria case data recorded at approximately 1300 geo-referenced health
facilities distributed throughout the country. The health facilities include public hospitals, local
clinics and rural health centres. In Zimbabwe, malaria is a notifiable disease. As such trained per-
sonnel manning health facilities are responsible for testing any person showing symptoms of the
disease. The testing is done using rapid diagnostic tests or microscopy (MOHCC 2014) and only
positive malaria cases established through standard clinical diagnostic procedures are included in the
MOHCC malaria database. For the purpose of delimiting malaria risk zones, the malaria case data
for the period 2005–2014 were aggregated by administrative district. The rationale for aggregating
the data at district level was that malaria interventions in Zimbabwe are planned and implemented
using the administrative district as the spatial epidemiological unit (Midzi et al. 2018). For each of
the country’s 71 administrative districts targeted, malaria prevalence was calculated by dividing the
total number of malaria cases recorded in a district by the total human population of that district. The
resultant ratio was multiplied by 1 000 to make prevalence easy to interpret. Figure 2 shows spatial
variation in malaria prevalence within and across the 71 administrative districts of Zimbabwe. High
prevalence of malaria can be observed in the south-eastern, north-eastern and western regions of
the country. By contrast, the central and southern regions of the country are characterized by low
prevalence of malaria.
GEOCARTO INTERNATIONAL   5

Figure 2. Average malaria prevalence mapped at district level in Zimbabwe based on incidence data for the period from 2005 to 2014.

2.2.3.  Environmental variables


Environmental variables used to characterize the ecological niche of the three common malaria vectors
in Zimbabwe included climatic variables related to temperature and precipitation as well as topographic
variables, specifically altitude and the topographic wetness index. Previous work has demonstrated
that temperature and rainfall variables are key in determining the suitable habitat of mosquito species
(Lindsay and Bayoh 2004). Based on the niche theory, mosquito species, which are the main malaria
vectors, occur in habitats where environmental conditions are most suitable for reproduction and
survival of the larvae (Hongoha et al. 2012). The temperature and rainfall dependence of reproduction
and survival of mosquitoes is well documented (Paaijmans et al. 2009, 2010). Therefore, it was deemed
necessary to use these climatic variables to build ecological niche models that best characterize the
suitable habitats of three malaria vectors mostly implicated in spreading malaria in Zimbabwe.
Two temperature-related bioclimatic variables, namely isothermality (Bio 3) and temperature
seasonality (Bio 4), were used to represent the influence of temperature of vector reproduction and
survival. Isothermality quantifies how the day-to-night temperatures oscillate relative to the sum-
mer-to-winter (annual) oscillations (O’Donnell and Ignizio 2012). Temperature seasonality is defined
as the coefficient of variation in temperature over a given period, for example, a season (O’Donnell
and Ignizio 2012).Two rainfall-related bioclimatic variables namely, annual precipitation (Bio 12)
and precipitation of the wettest month (Bio 13) were used to represent the influence of water on the
distribution of vector breeding sites. Bio 12 is calculated as the sum of all total monthly precipitation
values. Precipitation of the wettest month represents the month with the highest cumulative precip-
itation. Malaria transmission was expected to peak in such a month (O’Donnell and Ignizio 2012).
The four bioclimatic variables were downloaded from the Worldclim database (www. worldclim.
org) at a spatial resolution of 1 km. The advantage of using bioclimatic variables in modelling habitat
suitability of the mosquito vectors is that compared to raw monthly rainfall and temperature averages
(Aguirre-Gutierrez et al. 2013; Olivier and Aranda 2017), bioclimatic variables have been fine-tuned
to be more biologically meaningful. As a result, they have proved successful in representing physio-
logical tolerances of a species (Elith et al. 2006; Kumar et al. 2009; Molloy et al. 2014). The bioclimatic
variables used in this study were selected from a list of 19 bioclimatic variables following tests for
collinearity (Gwitira et al. 2015).
Altitude was the fifth environmental variable used to model habitat suitability of three malaria
vector species. This was done to build upon previous work (Taylor and Mutambu 1986) that delimited
malaria risk zones for Zimbabwe using altitudinal zones. Data on altitude were derived from the NASA’s
Shuttle Radar Topography Mission (SRTM) at a resolution of 90 m (www.usgs.gov). The topographic
6   I. GWITIRA ET AL.

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.

2.3.  Modelling habitat suitability of malaria vectors


Ecological niche modelling using the maximum entropy (MaxEnt) version 3.3 algorithm was applied
to predict malaria vector habitats as a function of four bioclimatic and two topographic variables in
Zimbabwe (Phillips et al. 2006). Although there are several ecological niche algorithms available,
MaxEnt was selected as it has better predictive power than other modelling approaches such as Genetic
Algorithm for Rule Set Production (GARP) (Slater and Michael 2012; Almeida et al. 2016). In addition,
MaxEnt has the advantage of being able to select ecologically relevant variables for the presence-only
records and use them to quantity environmental suitability for the species under study (Phillips et al.
2006; Olivier and Aranda 2017).
The contribution of each variable to the model was evaluated using the Jacknife approach (Yost et
al. 2008). The Jacknife approach has been shown to be a more reliable measure of variable importance
than other approaches such as variable per cent contribution (Phillips et al. 2006; Muñoz et al. 2011).
Jacknife results of our MaxEnt models illustrated that isothermality, temperature seasonality, annual
precipitation, altitude, topographic wetness index and precipitation of the wettest month contributed
significantly to the distribution of the three malaria vectors.

2.3.1.  Model calibration and validation


Prior to calibrating the MaxEnt model, we randomly split the presence data for each malaria vector
into 75% training set and 25% testing set as in previous studies (Kulkarni et al. 2010; Slater and Michael
2012). The area under the curve (AUC) was used to evaluate the predictive power of the MaxEnt mod-
els (McPherson and Jetz 2007). AUC values close to 100% indicate excellent discrimination between
suitable and unsuitable areas for malaria vectors (Phillips et al. 2006). MaxEnt models that achieved
AUC values in the range 60–69% were regarded as of average performance while those with AUC in
the range 70–79% were classified as good. MaxEnt models with AUC values ranging between 80 and
89% were regarded as very good and those with AUC values >90% were regarded as excellent in terms
of performance when applied to predict the vector habitat (Elith et al. 2006; Pittman and Brown 2011).
In this study an AUC of >0.80 was selected as the cut-off point since models with AUC above this
threshold are generally regarded as good for predictive purposes (Baldwin 2009). It has to be noted
that the MaxEnt models that were run in this study all achieved a high AUC value greater than 80%,
which implies low error. The habitat suitability models are presented separately for each species to
show spatial variations. However, a combined habitat suitability surface was derived from these three
separate model predictions in a GIS and used for malaria risk stratification.

2.4.  Delimitation of malaria risk zones


In this study, vector suitability and malaria prevalence were integrated in a GIS to stratify the whole
country into five malaria risk zones. First, the individual habitat suitability maps for the three vectors
were summed and divided by three to yield an average vector suitability map. The average vector suita-
bility map was assigned a weight of 0.78 while the malaria prevalence map was assigned a weight of 0.22.
Prevalence data tend to be affected by a low reporting rate which introduces bias. This characteristic
of prevalence data justify the low weight assigned to it. Then, malaria risk was calculated as the sum of
the weighted vector suitability and malaria prevalence maps. Formally, malaria risk was computed as:
GEOCARTO INTERNATIONAL   7

Mr = 0.78VS + 0.22Mp (2)


where Mr is a continuous malaria risk map, VS is vector suitability map and Mp is the malaria prev-
alence map.
The k-means clustering algorithm was applied to the output malaria risk map to generate five classes.
The World Health Organization (WHO) classification scheme applicable to Southern Africa (Table 1)
was adopted to define the five malaria risk zones in relation to the k-means classes created. For example,
the fifth k-means class was characterized by clustering of highest values of suitability and prevalence
in space. This class was therefore assigned to the high and perennial malaria risk zone. By contrast,
the first k-means class was dominated by clustering of lowest values of suitability and prevalence in
space. Hence, it was assigned to the free/sporadic malaria zone. The other three k-means classes were
assigned to the low and short seasonal, moderate and seasonal as well as the high and seasonal malaria
risk zones in order of increasing malaria risk. K-means algorithm was selected ahead of several other
cluster analysis algorithms as it is one of the most widely used algorithms. In addition, the k-means
algorithm is easy to implement, and efficient (Jain 2010; Abbas et al. 2016).

Table 1. Classification scheme for malaria risk zones in Southern Africa.

Zone No. Malaria risk Zone Description


1 Free/Sporadic Transmission never occurs due to unfavourable climatic conditions. At times
transmission does not normally occur due to control efforts or the area is on the
fringe of climatic suitability. However, abnormal events (meteorological, failure of
control, demographic) may cause outbreaks
2 Low and short seasonal Malaria transmission is low and highly seasonal
3 Moderate and seasonal Malaria transmission is moderate and seasonal
4 High and seasonal Malaria transmission is high with seasonal fluctuations
5 High and perennial Malaria transmission is high with negligible seasonal fluctuations

2.5.  Validation of malaria risk zones


To validate malaria risk zones, the raster map of malaria risk zones was converted from raster to vec-
tor format using Quantum GIS version 2.14 (QGISDevelopmentTeam 2009). After this, malaria case
data for 2015 was extracted for each malaria risk zone using Quantum GIS’s zonal statistics function.
The 2015 malaria case data was an independent data-set which was not used in the development of
the malaria risk map. Malaria case data for each risk zone were tested for normality using Shapiro
Wilk’s test. It was found out that prevalence data deviated from normality. Therefore, Kruskal–Wallis
test was used to check for significant differences in malaria cases between the malaria risk zones.
Furthermore, post hoc multiple comparison analysis was performed to test for statistically significant
pairwise differences in malaria prevalence among the five malaria risk zones. Specifically, Tamhane’s
T2 post hoc analysis was applied in SPSS version 21 since we assumed that the malaria risk zones had
unequal variance and size.

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.

Malaria risk zone Area (km2) Density


1 38,720 0.0046
2 96,881 0.0044
3 72,183 0.0054
4 98,721 0.0031
5 84,252 0.0045

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

Malaria Prevalence 2015


30

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.

Figure 6. Stratified malaria risk zones based on K-means.

4.  Discussion and conclusions


Results of this study indicate that a combination of habitat suitability and malaria prevalence can be
used to successfully delimit malaria risk zones. In fact, validation of the malaria risk levels using inde-
pendently collected malaria case data showed that malaria risk exponentially increases with increasing
malaria cases. In addition, we found a statistically significant difference in malaria cases among the
different malaria risk zones. However, in a few cases, post hoc analysis showed no significant differences
in malaria cases between some adjacent malaria risk zones. This could be as a result of the transitional
nature of malaria risk zones i.e. crisp boundaries are not expected in nature. Therefore, we deduce
that malaria interventions should consider that nearby areas influence each other in terms of disease
occurrence. It is also important to note that within a given year the area covered by a particular zone
can change due to the dynamic nature of environmental factors. In addition, the effect of migration on
GEOCARTO INTERNATIONAL   11

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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