Urbanization and the global malaria recession
© Tatem et al.; licensee BioMed Central Ltd. 2013
Received: 9 January 2013
Accepted: 24 March 2013
Published: 17 April 2013
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© Tatem et al.; licensee BioMed Central Ltd. 2013
Received: 9 January 2013
Accepted: 24 March 2013
Published: 17 April 2013
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.
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.
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.
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], although these gains were often coincident with rapid economic 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 demand for resources and improved communications. Moreover, 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 behavioural 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 , and a contemporary malaria transmission map  that is comparable to historic data , enables a more detailed exploration of this relationship. Here, these datasets were utilized to examine for the first time the association at global, national and subnational scales between changes in malaria transmission and urban growth across the last century.
The only global map of pre-intervention malaria endemicity 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 proportion of individuals with malaria parasites detectable in their peripheral blood) and stratified into four endemic classes associated with Plasmodium falciparum endemicity  (hypo-endemic, PR < 10%; meso-endemic, PR > 10% and <50%; hyperendemic, PR > 50% and < 75%; holo-endemic, PR > 75%). This map is the only reconstruction of historical malaria at its assumed historical peak around the start of the 20th Century and triangulates well with the plethora of national level malaria maps published throughout the last century . 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..
The publication of an evidence-based map of contemporary malaria endemicity  and its conversion to classes that match the c.1900 map  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 information 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 provide a unique and valuable quantitative picture of the spatial changes in malaria epidemiology that have occurred over the last 100 years. The map of contemporary malaria endemicity was generated from a recently defined model of age-standardized P. falciparum parasite rate, PfPR2-10 . Using a model-based geostatistical framework, the underlying value of PfPR2-10 at each location was modelled for the year 2007 as a transformation 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 unobserved age-standardized prevalence surface . 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 annual mean prevalence surface and to assign each pixel to the endemicity class with the highest posterior probability 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 endemicity between these two time periods with levels of urbanization, it was necessary to translate both the historical and contemporary maps into approximate units of PfRC, 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 endemicity, following previous studies , and was undertaken using a simple P. falciparum transmission model  to estimate a value of PfRC corresponding to the mid-value of each endemicity class. Using these conversion values, maps of PfRC were made corresponding to both historical and contemporary endemicity. These two maps were overlaid in a geographical information system (GIS) (ArcGIS 9.2, ESRI Inc, Redlands CA, USA), and the relative change in PfRC 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  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.
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 the date of elimination (Additional file 7) for those countries that achieved it were compared.
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.
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 endemicity 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 .
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 declines, a consistent pattern of greater transmission reduction in those areas that have undergone urbanization should be seen. Comparing mean changes in transmission 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. This confirms that greater transmission reductions occurred in areas that are urban today, but does not indicate if the largest declines were coincident with greater rates of urbanization.
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 exhibit 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 correlated 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 towards the success of interventions, however, in several cases the decline began before specific interventions were deployed, suggesting the contribution of alternative factors . While malaria declines due to urbanization and its effects are likely to be more gradual than some of the sudden drops seen, it remains a possibility that the rapid urbanization ongoing in sub-Saharan Africa  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 attributing changes to a single cause. Recent analyses have indicated that vector-borne and parasitic diseases have systematically impacted economic growth , but more detailed studies of these types of relationships across disease 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 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 assumptions made to fill these gaps . 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 formal quantification of the global P. falciparum endemicity declines and their link to urbanization beyond the broad relationships presented here. Nevertheless, recent mapping of the limits of P. vivax transmission  and analyses of contemporary impacts of urbanization , 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 countries that eliminated malaria (Additional file 8). Significant efforts towards modelling future malaria scenarios have been completed or are underway, focused principally 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 . 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 . 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 transmission 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 cities 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 between 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 continue to catalyze malaria declines on the path to the goal of a malaria-free future.
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 ( http://www.afripop.org, http://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.
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