The global limits and population at risk of soil-transmitted helminth infections in 2010

Background: Understanding the global limits of transmission of soil-transmitted helminth (STH) species is essential for quantifying the population at-risk and the burden of disease. This paper aims to define these limits on the basis of environmental and socioeconomic factors, and additionally seeks to investigate the effects of urbanisation and economic development on STH transmission, and estimate numbers at-risk of infection with Ascaris lumbricoides, Trichuris trichiura and hookworm in 2010. Methods: A total of 4,840 geo-referenced estimates of infection prevalence were abstracted from the Global Atlas of Helminth Infection and related to a range of environmental factors to delineate the biological limits of transmission. The relationship between STH transmission and urbanisation and economic development was investigated using high resolution population surfaces and country-level socioeconomic indicators, respectively. Based on the identified limits, the global population at risk of STH transmission in 2010 was estimated. Results: High and low land surface temperature and extremely arid environments were found to limit STH transmission, with differential limits identified for each species. There was evidence that the prevalence of A. lumbricoides and of T. trichiura infection was statistically greater in peri-urban areas compared to urban and rural areas, whilst the prevalence of hookworm was highest in rural areas. At national levels, no clear socioeconomic correlates of transmission were identified, with the exception that little or no infection was observed for countries with a per capita gross domestic product greater than US$ 20,000. Globally in 2010, an estimated 5.3 billion people, including 1.0 billion school-aged children, lived in areas stable for transmission of at least one STH species, with 69% of these individuals living in Asia. A further 143 million (31.1 million school-aged children) lived in areas of unstable transmission for at least one STH species. Conclusions: These limits provide the most contemporary, plausible representation of the extent of STH risk globally, and provide an essential basis for estimating the global disease burden due to STH infection. © 2012 Pullan and Brooker; licensee BioMed Central Ltd. This analysis utilizes data on the prevalence of STH species collated in the GAHI (http://www.thiswormyworld.org) [18]. This project aims to provide an open-access, global information resource on the distribution of STH and schistosomiasis, with the specific aims of 1) describing the global distribution and prevalence of infection of each species and 2) highlighting geographical areas for which further survey information is required. The developed maps, along with sources of identified surveys, are presented on an open access website (http://www.thiswormyworld.org). The GAHI database is regularly updated using structured searches of the formal and grey literature, and has strict inclusion criteria: only random or whole community samples are included, excluding data from hospital or clinic surveys or surveys among non-representative sub-populations, such as among refugees, prisoners or nomads. For data from clinical trials or cohort studies, only baseline, pre-intervention estimates of prevalence are included. Efforts are made to geo-position each survey to a single longitude and latitude using a combination of electronic gazetteers, national school and village databases digitised from topographical maps and contact with authors who used a global positioning system (GPS; see Brooker et al. [18]). Where this point geo-position was not possible, efforts were made to geo-position surveys to the second administrative level, using the 2009 version of the Administrative Level Boundaries project (SALB) [19]. The purpose of this first analysis was to determine biological and climatic suitability for STH transmission, based on post-1980 data that could be geo-located to a single survey location. To reduce the influence of control measures, we excluded data collected after the initiation of national STH control programmes, defined as >25% of the at-risk school-aged population receiving anthelmintic treatment for five years prior to the survey date, as reported to the World Health Organization (WHO) [20]. This resulted in the exclusion of 746 survey points from Burundi, Egypt, Honduras, Lao PDR, Mali, Nepal, Niger, Peru, Sierra Leone, Uganda and Venezuela. Data were also excluded if surveys were conducted in an irrigated area, which was classified as districts with >50% land surface equipped for irrigation [21], excluding a further 25 survey points in Afghanistan, Egypt, India, Madagascar, Mexico, Nepal, Pakistan, South Africa, Thailand, Venezuela and Viet Nam. On the basis of the above, 4,633 independent prevalence surveys were included. Experimental and field studies indicate that the survival and development of STH free living stages, and hence STH transmission, are crucially dependent on ambient and surface temperature and humidity [22-25]. Indirect estimates of these factors can be identified from high-resolution satellite and meteorological data. Synoptic mean, minimum and maximum monthly values of land surface temperature (LST) for the period 1950–2000 were derived from the WorldClim database of interpolated global weather station temperature data at 1 km spatial resolution [26,27]. Humidity was indirectly estimated on the basis of (i) annual precipitation rates available in the WorldClim database [26]; (ii) Potential Evapo-Transpiration (PET, a measure of the ability of the atmosphere to remove the water through evapo-transpiration); and (iii) Aridity Index (AI, calculated as mean annual precipitation divided by mean annual PET) [28,29]. In addition, extremely arid areas, such as deserts and their fringes, were identified using the GlobCover Land Cover product [30,31] for which the “bare areas” class denotes deserts. The environmental and climatic data were imported into ArcMap 9.2 (ESRI, Redlands, CA) and linked by geographical location to the parasitological survey data. Analysis was stratified by region (Asia, Latin America and Africa plus the Middle East) and by climatic zone (tropics, sub-tropics/temperate) [32]. Upper and lower thermal and humidity constraints for each species were investigated using scatter plots and box plots. Two sets of biological limits were identified: areas that were biologically unsuitable (where median and mean observed infection prevalence was <0.1%); and areas with low/unstable transmission (where median and mean infection prevalence was <2%). The appropriateness of selected limits were subsequently assessed using box plots of point and district-level district estimates according to the limits and compared using a Kruskal-Wallis non-parametric test. Based on observed relationships, region and species-specific contour maps were developed on a 1 × 1 km grid to mask areas as biologically unsuitable for STH transmission, and areas where transmission is likely to be low/unstable. Districts were masked if >50% of their surface area was covered by at least one of the climatic masks. The identified limits were, however, not applied to irrigated areas. The extent by which population density and urbanisation impacts upon STH transmission is uncertain [33]. The purpose of this analysis therefore was to determine whether STH transmission risk varies according to population density or settlement patterns and whether risk should be modified according to urbanisation, as has been done previously for malaria [34]. Population density was estimated using a global population database (Global Rural Urban Mapping Project (GRUMP)) [35,36]. To ensure prevalences were contemporaneous with the population data, analysis was restricted to surveys conducted between 2005 and 2011. Survey locations were classified as urban using an updated 2010 urban extents (UE) mask derived from GRUMP. The remaining surveys were classified as peri-urban (<15 km from the UE edge and population density >250/km2), rural (>15 km from the UE edge and/or population density <250/km2), and extreme rural (population density <1/km2) using the Gridded Population of the World version 3 (GPW3) population database, projected to 2010 by applying national, median variant, urban and rural-specific growth rates per country [35,36]. The effect of urbanisation on infection prevalence was assessed by identifying spatially and temporally matched urban–rural pairs. Here each urban survey prevalence value was matched to surveys in peri-urban and rural areas that were conducted within a 100 km and five year window. When more than one survey originated from the same UE, the mean prevalence was calculated. Averages of the peri-urban and rural sets of surveys were calculated and assigned to their urban counterpart, generating a series of map-defined urban/peri-urban/rural matched pairs. As prevalence distributions were highly skewed, the prevalence values for matched pairs were compared using the Wilcoxon signed-rank test, and overall prevalence distributions by settlement type compared using the Kruskal-Wallis non-parametric test. For subgroup analysis, data were stratified by country-level developmental indicators: the proportion of the urban population with access to improved sanitation (<25%, 25–50%, >50%), and the GINI coefficient (<35%, 35–50%, >50%). The third aim of this work is to determine whether territories can be identified as having no or very low STH transmission, or whether transmission risk should be modified, based on socioeconomic and development factors. Comparable, representative socioeconomic data are usually only available aggregated by country, and as such analysis of these limiting factors was restricted to the country level. National socioeconomic indicators were obtained from the World Bank databank [37], including GDP per capita; percentage of rural and urban populations with access to improved sanitation facilities; literacy rate in females ages 15–24 (proxy for maternal education), and GINI index (an indicator of the distribution of income within society, with 0% representing perfect equality and 100% perfect inequality) for the most recent year available. Parasite prevalence data were only included for the period 2005–2011, and incorporated all surveys conducted in this period that could be assigned to a country level. Scatter and box plots were used to explore ecological relationships between socioeconomic indicators and mean prevalence for each species. The identified biological and social limits were overlaid with the 2010 GRUMP population surface to estimate total population at risk (PAR) figures for each species individually, and at risk of infection with one or more species. To standardise to a single, representative age group of relevance to control, the proportion of the population of school-going age (5–14 years) was estimated for each country, based on the World Population Prospects: 2010 Revision Population Database [38].