Urbanization and the global malaria recession

Abstract

Background
The past century has seen a significant contraction in the global extent of malaria transmission, resulting in over 50 countries being declared malaria free, and many regions of currently endemic countries eliminating the disease. Moreover, substantial reductions in transmission have been seen since 1900 in those areas that remain endemic today. Recent work showed that this malaria recession was unlikely to have been driven by climatic factors, and that control measures likely played a significant role. It has long been considered, however, that economic development, and particularly urbanization, has also been a causal factor. The urbanization process results in profound socio-economic and landscape changes that reduce malaria transmission, but the magnitude and extent of these effects on global endemicity reductions are poorly understood.

Methods
Global data at subnational spatial resolution on changes in malaria transmission intensity and urbanization trends over the past century were combined to examine the relationships seen over a range of spatial and temporal scales.

Results/Conclusions
A consistent pattern of increased urbanization coincident with decreasing malaria transmission and elimination over the past century was found. Whilst it remains challenging to untangle whether this increased urbanization resulted in decreased transmission, or that malaria reductions promoted development, the results point to a close relationship between the two, irrespective of national wealth. The continuing rapid urbanization in malaria-endemic regions suggests that such malaria declines are likely to continue, particularly catalyzed by increasing levels of direct malaria control.

Full text

Urbanization and the global malaria recession
Tatem et al.
Tatem et al. Malaria Journal 2013, 12:133
http://www.malariajournal.com/content/12/1/133

R E S E A R C H Open Access
Urbanization and the global malaria recession
Andrew J Tatem
1,2*
, Peter W Gething
3
, David L Smith
2,4,5
and Simon I Hay
2,3
Abstract
Background: The past century has seen a significant contraction in the global extent of malaria transmission,
resulting in over 50 countries being declared malaria free, and many regions of currently endemic countries
eliminating the disease. Moreover, substantial reductions in transmission have been seen since 1900 in those areas
that remain endemic today. Recent work showed that this malaria recession was unlikely to have been driven by
climatic factors, and that control measures likely played a significant role. It has long been considered, however,
that economic development, and particularly urbanization, has also been a causal factor. The urbanization process
results in profound socio-economic and landscape changes that reduce malaria transmission, but the magnitude
and extent of these effects on global endemicity reductions are poorly understood.
Methods: Global data at subnational spatial resolution on changes in malaria transmission intensity and
urbanization trends over the past century were combined to examine the relationships seen over a range of spatial
and temporal scales.
Results/Conclusions: A consistent pattern of increased urbanization coincident with decreasing malaria
transmission and elimination over the past century was found. Whilst it remains challenging to untangle whether
this increased urbanization resulted in decreased transmission, or that malaria reductions promoted development,
the results point to a close relationship between the two, irrespective of national wealth. The continuing rapid
urbanization in malaria-endemic regions suggests that such malaria declines are likely to continue, particularly
catalyzed by increasing levels of direct malaria control.
Keywords: Urbanization, Global malaria endemicity, Plasmodium falciparum,Plasmodium vivax, Malaria elimination
Background
The range of malaria has contracted through a century
of economic development and disease control [1-3].
During an era of renewed interest in elimination and
eradication there is a need to better understand and
quantify the forces behind this recession. A variety of
direct control efforts were likely a major factor behind
the global contraction in malaria transmission [2,3], al-
though these gains were often coincident with rapid eco-
nomic and social development and land use changes
[4-6]. One major aspect of this development that has
been shown to significantly impact malaria transmission
is urbanization [7-9].
The process of urbanization includes physical landscape
modification and transformation of environs through de-
mand for resources and improved communications. More-
over, urbanization involves significant socio-economic
change; generally improved health, housing and increased
wealth [10,11]. These factors, common to urban areas,
cause marked entomological, parasitological and behav-
ioural effects that result in reduced malaria transmission
both within the urban core and surrounding peri-urban
areas [7,9,12]. A century of rapid urbanization has
therefore likely had an impact on malaria transmission
globally, but the size and importance of this impact has
never been examined.
The recent construction of 20th Century time series of
global urban extent data [13], and a contemporary mal-
aria transmission map [14] that is comparable to historic
data [15], enables a more detailed exploration of this re-
lationship. Here, these datasets were utilized to examine
for the first time the association at global, national and
* Correspondence: andy.tatem@gmail.com
1
Department of Geography and Environment, University of Southampton,
Highfield, Southampton, UK
2
Fogarty International Center, National Institutes of Health, Bethesda, MD
20892, USA
Full list of author information is available at the end of the article
© 2013 Tatem et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative
Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and
reproduction in any medium, provided the original work is properly cited.
Tatem et al. Malaria Journal 2013, 12:133
http://www.malariajournal.com/content/12/1/133

subnational scales between changes in malaria transmis-
sion and urban growth across the last century.
Methods
Data
Urbanization
HYDE 3.1 [13,16] is a dynamic modelling effort of long-
term historical population growth, providing a consistent
database of 20th-century population and urban distribu-
tion at 5-minute spatial resolution (equivalent to approxi-
mately 10 km at the Equator). Full details of dataset
construction are provided in Goldwijk et al. [13,16]. In
brief, urban-rural population numbers and fractions for
each country and for each decade were obtained from a
variety of sources, including the UN [17] and published
databases and reviews [18]. Urban areas were then
mapped by combining different spatial datasets [19-21]
and contemporary urban population datasets, which were
derived from existing databases [21,22]. Finally, urban
population densities over time were estimated based on
the fitting of asymmetric Gaussian probability density
function models to the population data [13]. The range of
input datasets, assumptions and modeling methods used
in construction of the HYDE 3.1 datasets mean that sig-
nificant uncertainties are inherent in the outputs, and
these are likely higher in the mapping covering both the
early 20th Century and lower income areas of the World,
where data scarcity meant that more assumptions had to
be made [13,16]. Nevertheless, at the broad spatial and
temporal scales of analysis undertaken here, the effects of
such assumptions and uncertainties on results are likely
small. Figure 1 shows changes in urban population sizes
across the malaria endemic world from 1900 to 2000.
Additional file 1 shows the mapped urban areas for 1900
and 2000, while Additional file 2 maps the change in
urban extent over the 100-year period, and Additional file
3 shows urban extents in 1900 and 2000 for Brazil.
Malaria endemicity
The only global map of pre-intervention malaria endem-
icity dates from a 1968 study [15,23] in which a major
synthesis of historical records, documents and maps of a
variety of malariometric indices for all four Plasmodium
species was used to map parasite rate (PR—the propor-
tion of individuals with malaria parasites detectable in
their peripheral blood) and stratified into four endemic
classes associated with Plasmodium falciparum endem-
icity [24] (hypo-endemic, PR < 10%; meso-endemic, PR >
10% and <50%; hyperendemic, PR > 50% and < 75%;
holo-endemic, PR > 75%). This map is the only recon-
struction of historical malaria at its assumed historical
peak around the start of the 20th Century and triangu-
lates well with the plethora of national level malaria
maps published throughout the last century [25]. The
historical malaria endemicity map was scanned from the
original publication, digitized on-screen and rasterized
to a 5 × 5 km grid. The map for an area of Brazil is
shown in Additional file 3(a) –the full map can be seen
in Gething et al. [3].
The publication of an evidence-based map of contem-
porary malaria endemicity [14] and its conversion to
classes that match the c.1900 map [3] described above,
allows an audit of changes in the global epidemiology of
malaria since the start of the 20th Century. With just
two timepoints of malaria endemicity data, precise infor-
mation on the timing and progression of changes is
absent, placing a limitation on the conclusions that can
be drawn from analyses. However, the datasets do pro-
vide a unique and valuable quantitative picture of the
spatial changes in malaria epidemiology that have
occurred over the last 100 years. The map of contem-
porary malaria endemicity was generated from a recently
defined model of age-standardized P. falciparum parasite
rate, PfPR2-10 [26]. Using a model-based geostatistical
framework, the underlying value of PfPR2-10 at each
location was modelled for the year 2007 as a transform-
ation of a space-time Gaussian process (GP), with the
number of P. falciparum-positive individuals in each
survey modelled as a binomial variate given the unob-
served age-standardized prevalence surface [14]. The GP
was parameterized by a mean component and a space-
time covariance function which was spatially anisotropic,
used great-circle distance to incorporate the curvature of
Earth, and included a periodic temporal component to
capture seasonality. Bayesian inference was implemented
using Markov chain Monte Carlo and direct simulation
to generate posterior predictive samples of the 2007 an-
nual mean prevalence surface and to assign each pixel
to the endemicity class with the highest posterior prob-
ability of membership. This dataset for an area of Brazil
is shown in Additional file 3(b). The classes matched
those of the c.1900 endemicity map, enabling a class
change dataset to be produced, which is shown in
Figure 1 and Additional file 4.
In order to compare the observed changes in endem-
icity between these two time periods with levels of
urbanization, it was necessary to translate both the his-
torical and contemporary maps into approximate units
of PfR
C
, the P. falciparum basic reproductive number
under the levels of control that existed at the time. This
enabled comparisons of the effect sizes of changes in en-
demicity, following previous studies [3], and was under-
taken using a simple P. falciparum transmission model
[27] to estimate a value of PfR
C
corresponding to the
mid-value of each endemicity class. Using these conver-
sion values, maps of PfR
C
were made corresponding to
both historical and contemporary endemicity. These two
maps were overlaid in a geographical information system
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(GIS) (ArcGIS 9.2, ESRI Inc, Redlands CA, USA), and
the relative change in PfR
C
between the historic and
contemporary map was calculated for each 5 × 5 km
pixel. These relative changes were summarized as areas
of increase, areas of no change, and areas of decrease of
between zero and one, one and two and greater than
two orders of magnitude (see Additional file 5).
Finally, the recent construction of an evidence-based
map of the limits of Plasmodium vivax transmission
[28] meant that analyses could be repeated to examine
the similarity in results between the two parasite species.
Additional file 6 shows the P. vivax transmission limits
map, constructed using data on the presence of P. vivax
infection and spatial information on climatic conditions
that impede transmission (low ambient temperature and
extremely arid environments) in order to delineate areas
where transmission was unlikely to take place.
Analyses
The data analyses focused on statistical explorations of
the link between urbanization and changes in malaria
endemicity. They covered three areas, examining in each
case different spatial scales and factors:
(i) National scale analyses of differences in urbanization
between countries that eliminated malaria during
the past century and those that remain endemic
today. Here, urban area percentages between 1900
and 2000 for those countries that remain endemic
today, and urban area percentages between 1900 and
Figure 1 Maps showing global changes in urban population size 1900-2000 and change in malaria endemicity. The bar height is
proportional to the size of urban population change. Areas that saw no change or an increase in endemicity are coloured dark red, those that
saw a reduction by one endemicity class are in red, two classes in orange and three or more classes in yellow.
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the date of elimination (Additional file 7) for those
countries that achieved it were compared.
(ii)Within country analyses of subnational differences
in urbanization trends between regions that
underwent malaria elimination 1900-2007, and
regions within the same country that remain
endemic today. Here, countries for which >20% of
their land area became malaria-free over the past
century and for which >20% of their land area
remains endemic today were identified, and
differences in urban areas, populations and rates of
change between them were examined.
(iii)Within country analyses of changes in transmission
intensity over the past century and their relationship
to urbanization trends. Here, per-country mean
changes in transmission class in areas that are urban
today, versus those that have remained rural, for
malaria-endemic areas in 1900 were examined.
For (ii) and (iii), by undertaking analyses at the
subnational scale and treating each country independently,
the differences in wealth, governance and latitude between
countries that are often confounding factors in assessing
the drivers of long-term global changes in malaria endem-
icity are controlled for. For each set of analyses and each
time period, the total urban areas and urban population
counts were extracted using ArcGIS 9.3 (ArcGIS 9.2, ESRI
Inc, Redlands CA, USA) and analysed using R2.10 [29].
Results
A consistent pattern of greater rates of urbanization in
areas that either eliminated malaria or displayed the
greatest transmission reductions was found. At the time
of elimination certification of those countries that
achieved malaria elimination, those areas that were ori-
ginally malarious had significantly higher proportions
(Mann-Whitney test: area, z = -3.207, p < 0.01; populations,
z = -5.432, p < 0.01) of their populations living in urban
areas and higher percentages of urban land area (Figure 2)
than the contemporary situation in those areas of the
world that remain endemic today. Moreover, the rate of
urbanization from 1900 onwards was significantly larger
in those countries that achieved elimination than those
that remain endemic today (see Additional file 8). Those
countries that achieved elimination exhibited significantly
greater increases in the proportions of their populations
(Mann-Whitney test: z = -1.985, p < 0.05) and land area
(Mann-Whitney test: z = -3.232, p < 0.01) that became
urban during the 20 years prior to elimination, compared
to the recent rates of urbanization in currently endemic
countries over the last 20 years. Such findings confirm the
presence of a correlation between urbanization and the
achievement of malaria elimination at national scales, but
this relationship is likely to be intimately tied to wealth.
Countries with greater wealth have greater malaria control
resources at their disposal, and it is those wealthier coun-
tries that have succeeded in eliminating malaria, as con-
firmed by undertaking similar analyses based on average
income (average income data from [30], Mann-Whitney
test: z = -6.491, p < 0.01). Moreover, those higher income
countries that succeeded in elimination are located in
latitudinal regions of lower climatic and environmental
receptivity to malaria transmission, making elimination
likely an easier task with a fixed set of intervention tools.
Therefore, untangling the effects of urbanization upon
changes in malaria transmission required analysis inde-
pendent of these economic or latitudinal biases, and these
are described below.
Twenty-nine countries were identified for which at least
a fifth of their land area became malaria-free over the past
century and for which at least a fifth of their land area re-
mains endemic today. Over 75% of these countries had
greater proportions of land area urbanized in the malaria-
free areas, and showed a greater percentage increase in
urban extent (Figure 3) than the areas that remain en-
demic today. Both of these differences are significant
(Wilcoxen test: urban area: z = -2.505 p < 0.05, urban ex-
tent change: z= -2.001, p < 0.05). However, these relation-
ships show regional variations, (Figure 3). Almost all
countries analysed in the Americas (Figure 3a) and Asia
(Figure 3c) showed greater urbanization in their malaria-
free versus still-endemic areas. In the Africa and Arabian
Peninsula region (Figure 3b), where both levels of
urbanization and transmission reductions were smaller,
the results were more mixed. Many of those falling
below the one-to-one line (Figure 3a-3c) are countries
where extremely arid or mountainous conditions have
influenced human settlement to occur principally in
areas most suitable for malaria transmission (e.g., Saudi
Arabia, Botswana, Swaziland). A full set of national level
results can be found in the Additional file 9. In addition,
the results of a repeat analysis for P. vivax yielding very
similar results are shown in Additional file 10.
Urban areas have been shown to exhibit lower levels
of transmission than surrounding rural ones [8,9]. If the
process of urbanization is a causal factor in malaria de-
clines, a consistent pattern of greater transmission re-
duction in those areas that have undergone urbanization
should be seen. Comparing mean changes in transmis-
sion class in areas that are urban today, versus those that
have remained rural, for malaria-endemic areas in 1900,
was possible in 158 countries. It shows that 82.3%
underwent a greater transmission reduction in their
urban areas than rural ones (Wilcoxen test: p < 0.001,
see Additional file 10). Of the 28 countries that displayed
a greater malaria reduction in rural areas, half of these
were in sub-Saharan Africa, where the smallest levels of
urbanization and reductions in transmission occurred.
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This confirms that greater transmission reductions oc-
curred in areas that are urban today, but does not indi-
cate if the largest declines were coincident with greater
rates of urbanization.
Finally, examination was undertaken of whether the
rate of urbanization was higher in regions of countries
that saw the greatest reductions in PfR
C
. Sixty-three
countries were identified that had two or more PfR
C
reduction classes, each covering at least 20% of their
land area, and the rates of urbanization 1900-2000 in
the areas exhibiting the smallest reduction in transmission
were compared to those in the areas displaying the
greatest reduction in transmission. Some 84.1% of
countries displayed a greater urban increase in the
areas that showed the greater PfR
C
reduction than
those that showed the smallest transmission reductions
(Wilcoxen test: p < 0.001, Figure 4). Further supporting
analyses and more detail on these analyses are presented
in Additional file 11.
Discussion
The process of urbanization results in a variety of changes
that reduce receptivity to malaria transmission [9-11].
Here, a clear picture of increased urbanization associated
with greater malaria transmission reductions across
countries and continents is documented for the first
time. Whilst it remains challenging to untangle whether
this urbanization resulted in decreased transmission, or
that malaria reductions promoted development, a close
relationship is evident, irrespective of national wealth
and latitude.
Other local evidence [7,12,31,32] hints that changes
commensurate with urbanization play a substantive role in
driving malaria transmission declines. Whether measured
by proportion of land area or population urbanized, the
majority of nations that remain malaria endemic today ex-
hibit substantially lower levels of urbanization compared to
that at the time of elimination for those countries that have
achieved it (Figure 2 and Additional file 8). Moreover, the
magnitude of change in urban extent from 1900 is also cor-
related with malaria declines, with continental differences,
notably sub-Saharan Africa showing lower levels of
urbanization today, and smaller changes in urban extent
and endemicity over the past century (Figure 3).
Recent malaria declines in sub-Saharan Africa point to-
wards the success of interventions, however, in several
cases the decline began before specific interventions were
deployed, suggesting the contribution of alternative factors
[33]. While malaria declines due to urbanization and its
effects are likely to be more gradual than some of the sud-
den drops seen, it remains a possibility that the rapid
urbanization ongoing in sub-Saharan Africa [34] is at least
a contributory driver to these changes.
While over three-quarters of countries show decreasing
transmission in areas that have undergone urbanization
over the past century, a handful of countries go against
this trend. A possible reason for this is the likely multi-
factorial complexity behind both changes in transmission
and human settlement dynamics, and the difficulty of at-
tributing changes to a single cause. Recent analyses have
indicated that vector-borne and parasitic diseases have
systematically impacted economic growth [35], but more
detailed studies of these types of relationships across dis-
ease types and ecozones are required to gain a fuller
understanding. Almost all of the countries that show
greater transmission reductions in rural areas are those
where human settlement was constrained to the more
malarious areas of the country, due to uninhabitable arid
Figure 2 Box plots of the percentage urban area in 1900 and in 2000 for countries that are still endemic and in the decade that
elimination was achieved for those countries that achieved elimination.
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Figure 3 (See legend on next page.)
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or mountainous areas elsewhere. Equally however, the
reverse is true for some countries –i.e. uninhabitable
areas with intense transmission forced human settlement
in the lower transmission regions.
It is clear that various sources of uncertainty exist in the
inputs and methodologies used in this study. Uncertainties
are inherent in the urbanization datasets through the lack
of data for many regions and time periods, and the as-
sumptions made to fill these gaps [13]. The proposed
levels of historical endemicity [15,23] are plausible when
triangulated against other values reported from the pre-
intervention era (for example, [26,36]), but the relatively
crude categorization of all-cause malaria endemicity strata
and the cartographic approach used preclude a more for-
mal quantification of the global P. falciparum endemicity
declines and their link to urbanization beyond the broad
relationships presented here. Nevertheless, recent map-
ping of the limits of P. vivax transmission [28] and
analyses of contemporary impacts of urbanization [8],
indicate very similar effects and contractions as that seen
for P. falciparum, with results repeated, where possible,
for P. vivax showing almost identical results (Additional
file 10), and transmission rarely more intense than meso-
endemic [37,38].
Much of the low-income world, where malaria burden
is highest and levels of urbanization are lowest, is set to
undergo an urban and demographic transition in the
coming decades [17,34], ultimately likely arriving at
levels of urbanization similar to those exhibited by coun-
tries that eliminated malaria (Additional file 8). Signifi-
cant efforts towards modelling future malaria scenarios
have been completed or are underway, focused princi-
pally on the effects of a variety of interventions [39-41]
or on climate change scenarios [42-45], but the impacts
of urbanization are rarely considered [46]. Yet, if the
past century of malaria declines are indicative, the study
of its impacts should receive more attention as nations
start to monitor their progress toward elimination [47].
(See figure on previous page.)
Figure 3 Plots showing urban area changes 1900-2000 between areas of countries that remain malaria endemic today, and those that
have undergone elimination for (a) the Americas, (b) Africa plus Arabian peninsula and (c) Asia. In each case, scatterplots of urban area
increases in endemic versus eliminated areas with one-to-one lines overlaid are shown at the top, and example plots of trends in urban area
percentages between areas that eliminated malaria (blue) and that remain endemic (red) are shown at the bottom (the full set of these plots is
provided in Additional file 9). The ISO country abbreviation for country name is used on the scatterplots (http://www.iso.org/iso/
english_country_names_and_code_elements).
Figure 4 Plasmodium falciparum basic reproductive number (PfR
C
) changes and urbanization. Countries in red show a greater percentage
increase in urban area over the past century in areas of the country with the greatest magnitude of PfR
C
decreases than areas that showed the
smallest changes. Countries in yellow show the reverse. Countries in light grey had either insufficient variation in PfR
C
changes, or no
transmission. Countries in dark grey have either always been malaria free, or only exhibited unstable transmission.
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There exist multiple data gaps and uncertainties in
obtaining suitable data to build urbanization into scenario
models, however. Firstly, simple consistent definitions of
what constitutes an urban area in general are difficult to
outline. Beyond this, multiple approaches to mapping
urban extents in a consistent fashion have been attempted
(e.g., [48-50]), but the spatial modelling of their future
growth is lacking. Secondly, definitions and measures of
urbanization that are relevant to understanding transmis-
sion patterns are poorly quantified, with only occasional
attempts at empirical definitions made [8,9], and little
consideration of the urban preferences of the dominant
Anopheles species [51-53], or adaptation of them to urban
environments [54,55]. Finally, the treatment of urban areas
as single homogenous entities ignores the great variations
in demographic, socio-economic and land uses within cit-
ies with, for example, urban agricultural practices often
maintaining transmission within urban areas [56-58].
The quantification of a global recession in the range
and intensity of malaria over the 20th century has
allowed us to review the impact that urbanization has
had on these declines, and gauge its importance as a
driver of future changes in malaria epidemiology. Results
highlight for the first time the consistent relationship be-
tween urbanization and malaria declines over the past
century globally, and point towards continuing declines
as urbanization permanently alters the receptivity of
many areas to malaria transmission. The findings
presented here suggest that these trends will likely con-
tinue to catalyze malaria declines on the path to the goal
of a malaria-free future.
Additional files
Additional file 1: Urban extents and malaria transmission mapped
for 1900 and 2000. Description: Maps of urban extents in 1900 and
2000 overlaid onto mapped areas of where malaria was eliminated over
the past century and where it remains endemic today.
Additional file 2: Change in urban extent between 1900 and 2000.
Description: Map of estimated changes in urban extent globally between
1900 and 2000.
Additional file 3: Malaria endemicity classes and urban areas in
Brazil. Description: Maps of malaria endemicity classes and urban areas
in Brazil for 1900 and 2000.
Additional file 4: Change in malaria endemicity class between 1900
and 2007. Description: Map of changes in malaria endemicity class
between 1900 and 2007.
Additional file 5: The magnitude of decrease in P. falciparum basic
reproductive number 1900-2007. Description: Map of the magnitude
of decrease in P. falciparum basic reproductive number for 1900-2007.
Additional file 6: The global spatial limits of Plasmodium vivax
malaria transmission in 2009. Description: Map of the global spatial
limits of Plasmodium vivax malaria transmission in 2009.
Additional file 7: Dates of malaria elimination for those countries
that achieved it. Description: Table showing the estimated and official
dates of malaria elimination for those countries that achieved it.
Additional file 8: Urbanization and countries that have eliminated
malaria. Description: Description and results of statistical analyses of
urbanization levels between countries that achieved elimination and
those that remain endemic today.
Additional file 9: Urbanization and sub-national malaria
elimination. Description: Description and results of per-country statistical
analyses of urbanization levels between regions that became malaria free
and those that remain endemic today.
Additional file 10: Results using the contemporary limits of
Plasmodium vivax transmission. Description: Description and results of
analyses repeated using Plasmodium vivax transmission limits data.
Additional file 11: Urbanization and changes in malaria
transmission. Description: Description and results of per-country
statistical analyses of changes in malaria transmission intensity and
urbanization levels.
Competing interests
The authors declare that they have no competing interests.
Authors’contributions
AJT conceived the analyses, developed the study design and conducted the
analyses. PWG, DLS and SIH provided the malaria endemicity data and
mathematical models for dataset conversions. All authors contributed to the
writing of the manuscript. All authors read and approved the final
manuscript.
Acknowledgements
AJT and DLS are supported by grants from the Bill and Melinda Gates
Foundation (#49446, #1032350) and NIH/NIAID (#U19AI089674). All authors
acknowledge funding support from the RAPIDD program of the Science &
Technology Directorate, Department of Homeland Security, and the Fogarty
International Center, National Institutes of Health, USA. SIH is a Wellcome
Trust Senior Research Fellow (#095066). PWG is a Medical Research Council
(UK) Career Development Fellow (#K00669X) and acknowledges support
from the Bill and Melinda Gates Foundation (#OPP1068048). This work forms
part of the output of the AfriPop and AsiaPop projects (www.afripop.org,
www.asiapop.org), and part of the output of the Malaria Atlas Project (MAP,
http://www.map.ox.ac.uk), principally funded by the Wellcome Trust, UK.
Author details
1
Department of Geography and Environment, University of Southampton,
Highfield, Southampton, UK.
2
Fogarty International Center, National Institutes
of Health, Bethesda, MD 20892, USA.
3
Spatial Ecology and Epidemiology
Group, Tinbergen Building, Department of Zoology, University of Oxford,
South Parks Road, Oxford OX1 3PS, UK.
4
Department of Epidemiology, Johns
Hopkins Bloomberg School of Public Health, Baltimore, MD, USA.
5
Malaria
Research Institute, Johns Hopkins Bloomberg School of Public Health,
Baltimore, MD, USA.
Received: 9 January 2013 Accepted: 24 March 2013
Published: 17 April 2013
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doi:10.1186/1475-2875-12-133
Cite this article as: Tatem et al.:Urbanization and the global malaria
recession. Malaria Journal 2013 12:133.
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