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1.  Predicting the risk of avian influenza A H7N9 infection in live poultry markets across Asia 
Nature communications  2014;5:4116.
Two epidemic waves of an avian influenza A (H7N9) virus have so far affected China. Most human cases have been attributable to poultry exposure at live-poultry markets, where most positive isolates were sampled. The potential geographic extent of potential re-emerging epidemics is unknown, as are the factors associated with it. Using newly assembled datasets of the locations of 8,943 live-poultry markets in China and maps of environmental correlates, we develop a statistical model that accurately predicts the risk of H7N9 market infection across Asia. Local density of live-poultry markets is the most important predictor of H7N9 infection risk in markets, underscoring their key role in the spatial epidemiology of H7N9, alongside other poultry, land cover and anthropogenic predictor variables. Identification of areas in Asia with high suitability for H7N9 infection enhances our capacity to target biosurveillance and control, helping to restrict the spread of this important disease.
doi:10.1038/ncomms5116
PMCID: PMC4061699  PMID: 24937647
2.  Modelling spatial patterns of urban growth in Africa 
The population of Africa is predicted to double over the next 40 years, driving exceptionally high urban expansion rates that will induce significant socio-economic, environmental and health changes. In order to prepare for these changes, it is important to better understand urban growth dynamics in Africa and better predict the spatial pattern of rural-urban conversions. Previous work on urban expansion has been carried out at the city level or at the global level with a relatively coarse 5–10 km resolution. The main objective of the present paper was to develop a modelling approach at an intermediate scale in order to identify factors that influence spatial patterns of urban expansion in Africa. Boosted Regression Tree models were developed to predict the spatial pattern of rural-urban conversions in every large African city. Urban change data between circa 1990 and circa 2000 available for 20 large cities across Africa were used as training data. Results showed that the urban land in a 1 km neighbourhood and the accessibility to the city centre were the most influential variables. Results obtained were generally more accurate than results obtained using a distance-based urban expansion model and showed that the spatial pattern of small, compact and fast growing cities were easier to simulate than cities with lower population densities and a lower growth rate. The simulation method developed here will allow the production of spatially detailed urban expansion forecasts for 2020 and 2025 for Africa, data that are increasingly required by global change modellers.
doi:10.1016/j.apgeog.2013.07.009
PMCID: PMC4139116  PMID: 25152552
Africa; urban growth; modelling; spatial pattern; boosted regression trees
3.  Spatial epidemiology of porcine reproductive and respiratory syndrome in Thailand 
BMC Veterinary Research  2014;10:174.
Background
Porcine reproductive and respiratory syndrome (PRRS) has become a worldwide endemic disease of pigs. In 2006, an atypical and more virulent PRRS (HP-PRRS) emerged in China and spread to many countries, including Thailand. This study aimed to provide a first description of the spatio-temporal pattern of PRRS in Thailand and to quantify the statistical relationship between the presence of PRRS at the sub-district level and a set of risk factors. This should provide a basis for improving disease surveillance and control of PRRS in Thailand.
Results
Spatial scan statistics were used to detect clusters of outbreaks and allowed the identification of six spatial clusters covering 15 provinces of Thailand. Two modeling approaches were used to relate the presence or absence of PRRS outbreaks at the sub-district level to demographic characteristics of pig farming and other epidemiological spatial variables: autologistic multiple regressions and boosted regression trees (BRT). The variables showing a statistically significant association with PRRS presence in the autologistic multiple regression model were the sub-district human population and number of farms with breeding sows. The predictive power of the model, as measured by the area under the curve (AUC) of the receiver operating characteristics (ROC) plots was moderate. BRT models had higher goodness of fit the metrics and identified the sub-district human population and density of farms with breeding sows as important predictor variables.
Conclusions
The results indicated that farms with breeding sows may be an important group for targeted surveillance and control. However, these findings obtained at the sub-district level should be complemented by farm-level epidemiological investigations in order to obtain a more comprehensive view of the factors affecting PRRS presence. In this study, the outbreaks of PRRS could not be differentiated from the potential novel HP-PPRS form, which was recently discovered in the country.
doi:10.1186/s12917-014-0174-y
PMCID: PMC4236821  PMID: 25091559
Spatial epidemiology; PRRS; Autologistic multiple regression; BRT; Breeding sows; Thailand
4.  Agro-Environmental Determinants of Avian Influenza Circulation: A Multisite Study in Thailand, Vietnam and Madagascar 
PLoS ONE  2014;9(7):e101958.
Outbreaks of highly pathogenic avian influenza have occurred and have been studied in a variety of ecological systems. However, differences in the spatial resolution, geographical extent, units of analysis and risk factors examined in these studies prevent their quantitative comparison. This study aimed to develop a high-resolution, comparative study of a common set of agro-environmental determinants of avian influenza viruses (AIV) in domestic poultry in four different environments: (1) lower-Northern Thailand, where H5N1 circulated in 2004–2005, (2) the Red River Delta in Vietnam, where H5N1 is circulating widely, (3) the Vietnam highlands, where sporadic H5N1 outbreaks have occurred, and (4) the Lake Alaotra region in Madagascar, which features remarkable similarities with Asian agro-ecosystems and where low pathogenic avian influenza viruses have been found. We analyzed H5N1 outbreak data in Thailand in parallel with serological data collected on the H5 subtype in Vietnam and on low pathogenic AIV in Madagascar. Several agro-environmental covariates were examined: poultry densities, landscape dominated by rice cultivation, proximity to a water body or major road, and human population density. Relationships between covariates and AIV circulation were explored using spatial generalized linear models. We found that AIV prevalence was negatively associated with distance to the closest water body in the Red River Delta, Vietnam highlands and Madagascar. We also found a positive association between AIV and duck density in the Vietnam highlands and Thailand, and with rice landscapes in Thailand and Madagascar. Our findings confirm the important role of wetlands-rice-ducks ecosystems in the epidemiology of AI in diverse settings. Variables influencing circulation of the H5 subtype in Southeast Asia played a similar role for low pathogenic AIV in Madagascar, indicating that this area may be at risk if a highly virulent strain is introduced.
doi:10.1371/journal.pone.0101958
PMCID: PMC4100877  PMID: 25029441
5.  Mapping the Global Distribution of Livestock 
PLoS ONE  2014;9(5):e96084.
Livestock contributes directly to the livelihoods and food security of almost a billion people and affects the diet and health of many more. With estimated standing populations of 1.43 billion cattle, 1.87 billion sheep and goats, 0.98 billion pigs, and 19.60 billion chickens, reliable and accessible information on the distribution and abundance of livestock is needed for a many reasons. These include analyses of the social and economic aspects of the livestock sector; the environmental impacts of livestock such as the production and management of waste, greenhouse gas emissions and livestock-related land-use change; and large-scale public health and epidemiological investigations. The Gridded Livestock of the World (GLW) database, produced in 2007, provided modelled livestock densities of the world, adjusted to match official (FAOSTAT) national estimates for the reference year 2005, at a spatial resolution of 3 minutes of arc (about 5×5 km at the equator). Recent methodological improvements have significantly enhanced these distributions: more up-to date and detailed sub-national livestock statistics have been collected; a new, higher resolution set of predictor variables is used; and the analytical procedure has been revised and extended to include a more systematic assessment of model accuracy and the representation of uncertainties associated with the predictions. This paper describes the current approach in detail and presents new global distribution maps at 1 km resolution for cattle, pigs and chickens, and a partial distribution map for ducks. These digital layers are made publically available via the Livestock Geo-Wiki (http://www.livestock.geo-wiki.org), as will be the maps of other livestock types as they are produced.
doi:10.1371/journal.pone.0096084
PMCID: PMC4038494  PMID: 24875496
6.  Risk factor modelling of the spatio-temporal patterns of highly pathogenic avian influenza (HPAIV) H5N1: a review 
Highly pathogenic avian influenza virus (HPAIV) H5N1 continues to impact on smallholder livelihoods, to constrain development of the poultry production sector, and to cause occasional human fatalities. HPAI H5N1 outbreaks have occurred in a variety of ecological systems with economic, agricultural and environmental differences. This review aimed to identify common risk factors amongst spatial modelling studies conducted in these different agro-ecological systems, and to identify gaps in our understanding of the disease’s spatial epidemiology. Three types of variables with similar statistical association with HPAI H5N1 presence across studies and regions were identified: domestic waterfowl, several anthropogenic variables (human population density, distance to roads) and indicators of water presence. Variables on socio-economic conditions, poultry trade, wild bird distribution and movements were comparatively rarely considered. Few studies have analysed the HPAI H5N1 distribution in countries such as Egypt and Indonesia, where HPAIV H5N1 continues to circulate extensively.
doi:10.1016/j.sste.2012.01.002
PMCID: PMC3389348  PMID: 22749203
Spatial epidemiology; avian influenza; H5N1
7.  Millennium development health metrics: where do Africa’s children and women of childbearing age live? 
The Millennium Development Goals (MDGs) have prompted an expansion in approaches to deriving health metrics to measure progress toward their achievement. Accurate measurements should take into account the high degrees of spatial heterogeneity in health risks across countries, and this has prompted the development of sophisticated cartographic techniques for mapping and modeling risks. Conversion of these risks to relevant population-based metrics requires equally detailed information on the spatial distribution and attributes of the denominator populations. However, spatial information on age and sex composition over large areas is lacking, prompting many influential studies that have rigorously accounted for health risk heterogeneities to overlook the substantial demographic variations that exist subnationally and merely apply national-level adjustments.
Here we outline the development of high resolution age- and sex-structured spatial population datasets for Africa in 2000-2015 built from over a million measurements from more than 20,000 subnational units, increasing input data detail from previous studies by over 400-fold. We analyze the large spatial variations seen within countries and across the continent for key MDG indicator groups, focusing on children under 5 and women of childbearing age, and find that substantial differences in health and development indicators can result through using only national level statistics, compared to accounting for subnational variation.
Progress toward meeting the MDGs will be measured through national-level indicators that mask substantial inequalities and heterogeneities across nations. Cartographic approaches are providing opportunities for quantitative assessments of these inequalities and the targeting of interventions, but demographic spatial datasets to support such efforts remain reliant on coarse and outdated input data for accurately locating risk groups. We have shown here that sufficient data exist to map the distribution of key vulnerable groups, and that doing so has substantial impacts on derived metrics through accounting for spatial demographic heterogeneities that exist within nations across Africa.
doi:10.1186/1478-7954-11-11
PMCID: PMC3724578  PMID: 23875684
Population; Demography; Mapping; Millenium development goals
8.  Predicting Hotspots for Influenza Virus Reassortment 
Emerging Infectious Diseases  2013;19(4):581-588.
TOC summary: Reassortment is most likely to occur in eastern China, central China, or the Nile Delta in Egypt.
The 1957 and 1968 influenza pandemics, each of which killed ≈1 million persons, arose through reassortment events. Influenza virus in humans and domestic animals could reassort and cause another pandemic. To identify geographic areas where agricultural production systems are conducive to reassortment, we fitted multivariate regression models to surveillance data on influenza A virus subtype H5N1 among poultry in China and Egypt and subtype H3N2 among humans. We then applied the models across Asia and Egypt to predict where subtype H3N2 from humans and subtype H5N1 from birds overlap; this overlap serves as a proxy for co-infection and in vivo reassortment. For Asia, we refined the prioritization by identifying areas that also have high swine density. Potential geographic foci of reassortment include the northern plains of India, coastal and central provinces of China, the western Korean Peninsula and southwestern Japan in Asia, and the Nile Delta in Egypt.
doi:10.3201/eid1904.120903
PMCID: PMC3647410  PMID: 23628436
influenza in birds; influenza A virus H3N2 subtype; influenza A virus H5N1 subtype; reassortant viruses; viruses; zoonoses; avian influenza; influenza
9.  Predicting the distribution of intensive poultry farming in Thailand 
Intensification of animal production can be an important factor in the emergence of infectious diseases because changes in production structure influence disease transmission patterns. In 2004 and 2005, Thailand was subject to two highly pathogenic avian influenza epidemic waves and large surveys were conducted of the poultry sector, providing detailed spatial data on various poultry types. This study analysed these data with the aim of establishing the distributions of extensive and intensive poultry farms, based on the number of birds per holder. Once poultry data were disaggregated into these two production systems, they were analysed in relation to anthropogenic factors using simultaneous autoregressive models. Intensive chicken production was clustered around the capital city of Bangkok and close to the main consumption and export centres. Intensively-raised ducks, mainly free-grazing, showed a distinct pattern with the highest densities distributed in a large area located in the floodplain of the Chao Phraya River. Accessibility to Bangkok, the percentage of irrigated areas and human population density were the most important predictors explaining the geographical distribution of intensively-raised poultry. The distribution of extensive poultry showed a higher predictability. Extensive poultry farms were distributed more homogeneously across the country and their distribution was best predicted by human population density.
doi:10.1016/j.agee.2011.12.019
PMCID: PMC3272562  PMID: 22323841
Agricultural intensification; livestock mapping; disaggregation; livestock production systems; remote sensing; free-grazing ducks
10.  Predicting the spatio-temporal distribution of Culicoides imicola in Sardinia using a discrete-time population model 
Parasites & Vectors  2012;5:270.
Background
Culicoides imicola KIEFFER, 1913 (Diptera: Ceratopogonidae) is the principal vector of Bluetongue disease in the Mediterranean basin, Africa and Asia. Previous studies have identified a range of eco-climatic variables associated with the distribution of C. imicola, and these relationships have been used to predict the large-scale distribution of the vector. However, these studies are not temporally-explicit and can not be used to predict the seasonality in C. imicola abundances. Between 2001 and 2006, longitudinal entomological surveillance was carried out throughout Italy, and provided a comprehensive spatio-temporal dataset of C. imicola catches in Onderstepoort-type black-light traps, in particular in Sardinia where the species is considered endemic.
Methods
We built a dynamic model that allows describing the effect of eco-climatic indicators on the monthly abundances of C. imicola in Sardinia. Model precision and accuracy were evaluated according to the influence of process and observation errors.
Results
A first-order autoregressive cofactor, a digital elevation model and MODIS Land Surface Temperature (LST)/or temperatures acquired from weather stations explained ~77% of the variability encountered in the samplings carried out in 9 sites during 6 years. Incorporating Normalized Difference Vegetation Index (NDVI) or rainfall did not increase the model's predictive capacity. On average, dynamics simulations showed good accuracy (predicted vs. observed r corr = 0.9). Although the model did not always reproduce the absolute levels of monthly abundances peaks, it succeeded in reproducing the seasonality in population level and allowed identifying the periods of low abundances and with no apparent activity. On that basis, we mapped C. imicola monthly distribution over the entire Sardinian region.
Conclusions
This study demonstrated prospects for modelling data arising from Culicoides longitudinal entomological surveillance. The framework explicitly incorporates the influence of eco-climatic factors on population growth rates and accounts for observation and process errors. Upon validation, such a model could be used to predict monthly population abundances on the basis of environmental conditions, and hence can potentially reduce the amount of entomological surveillance.
doi:10.1186/1756-3305-5-270
PMCID: PMC3561275  PMID: 23174043
Spatial ecology; Infectious disease; Remote-sensing; Dynamic model; Longitudinal entomological surveillance network; Mediterranean basin
11.  Improving Risk Models for Avian Influenza: The Role of Intensive Poultry Farming and Flooded Land during the 2004 Thailand Epidemic 
PLoS ONE  2012;7(11):e49528.
Since 1996 when Highly Pathogenic Avian Influenza type H5N1 first emerged in southern China, numerous studies sought risk factors and produced risk maps based on environmental and anthropogenic predictors. However little attention has been paid to the link between the level of intensification of poultry production and the risk of outbreak. This study revised H5N1 risk mapping in Central and Western Thailand during the second wave of the 2004 epidemic. Production structure was quantified using a disaggregation methodology based on the number of poultry per holding. Population densities of extensively- and intensively-raised ducks and chickens were derived both at the sub-district and at the village levels. LandSat images were used to derive another previously neglected potential predictor of HPAI H5N1 risk: the proportion of water in the landscape resulting from floods. We used Monte Carlo simulation of Boosted Regression Trees models of predictor variables to characterize the risk of HPAI H5N1. Maps of mean risk and uncertainty were derived both at the sub-district and the village levels. The overall accuracy of Boosted Regression Trees models was comparable to that of logistic regression approaches. The proportion of area flooded made the highest contribution to predicting the risk of outbreak, followed by the densities of intensively-raised ducks, extensively-raised ducks and human population. Our results showed that as little as 15% of flooded land in villages is sufficient to reach the maximum level of risk associated with this variable. The spatial pattern of predicted risk is similar to previous work: areas at risk are mainly located along the flood plain of the Chao Phraya river and to the south-east of Bangkok. Using high-resolution village-level poultry census data, rather than sub-district data, the spatial accuracy of predictions was enhanced to highlight local variations in risk. Such maps provide useful information to guide intervention.
doi:10.1371/journal.pone.0049528
PMCID: PMC3501506  PMID: 23185352
12.  Modelling the distribution of chickens, ducks, and geese in China 
Agriculture, ecosystems & environment  2011;141(3-4):381-389.
Global concerns over the emergence of zoonotic pandemics emphasize the need for high-resolution population distribution mapping and spatial modelling. Ongoing efforts to model disease risk in China have been hindered by a lack of available species level distribution maps for poultry. The goal of this study was to develop 1 km resolution population density models for China’s chickens, ducks, and geese. We used an information theoretic approach to predict poultry densities based on statistical relationships between poultry census data and high-resolution agro-ecological predictor variables. Model predictions were validated by comparing goodness of fit measures (root mean square error and correlation coefficient) for observed and predicted values for ¼ of the sample data which was not used for model training. Final output included mean and coefficient of variation maps for each species. We tested the quality of models produced using three predictor datasets and 4 regional stratification methods. For predictor variables, a combination of traditional predictors for livestock mapping and land use predictors produced the best goodness of fit scores. Comparison of regional stratifications indicated that for chickens and ducks, a stratification based on livestock production systems produced the best results; for geese, an agro-ecological stratification produced best results. However, for all species, each method of regional stratification produced significantly better goodness of fit scores than the global model. Here we provide descriptive methods, analytical comparisons, and model output for China’s first high resolution, species level poultry distribution maps. Output will be made available to the scientific and public community for use in a wide range of applications from epidemiological studies to livestock policy and management initiatives.
doi:10.1016/j.agee.2011.04.002
PMCID: PMC3134362  PMID: 21765567
poultry; China; distribution modelling; population estimates; GIS; epidemiology
13.  Modelling the distribution of domestic ducks in Monsoon Asia 
Agriculture, ecosystems & environment  2011;141(3-4):373-380.
Domestic ducks are considered to be an important reservoir of highly pathogenic avian influenza (HPAI), as shown by a number of geospatial studies in which they have been identified as a significant risk factor associated with disease presence. Despite their importance in HPAI epidemiology, their large-scale distribution in monsoon Asia is poorly understood. In this study, we created a spatial database of domestic duck census data in Asia and used it to train statistical distribution models for domestic duck distributions at a spatial resolution of 1 km. The method was based on a modelling framework used by the Food and Agriculture Organisation to produce the Gridded Livestock of the World (GLW) database, and relies on stratified regression models between domestic duck densities and a set of agro-ecological explanatory variables. We evaluated different ways of stratifying the analysis and of combining the prediction to optimize the goodness of fit of the predictions. We found that domestic duck density could be predicted with reasonable accuracy (mean RMSE and correlation coefficient between log-transformed observed and predicted densities being 0.58 and 0.80, respectively), using a stratification based on livestock production systems. We tested the use of artificially degraded data on duck distributions in Thailand and Vietnam as training data, and compared the modelled outputs with the original high-resolution data. This showed, for these two countries at least, that these approaches could be used to accurately disaggregate provincial level (administrative level 1) statistical data to provide high resolution model distributions.
doi:10.1016/j.agee.2011.04.013
PMCID: PMC3148691  PMID: 21822341
Livestock Mapping; Domestic ducks; Monsoon Asia; Regression models; Highly pathogenic avian influenza
14.  Population Distribution, Settlement Patterns and Accessibility across Africa in 2010 
PLoS ONE  2012;7(2):e31743.
The spatial distribution of populations and settlements across a country and their interconnectivity and accessibility from urban areas are important for delivering healthcare, distributing resources and economic development. However, existing spatially explicit population data across Africa are generally based on outdated, low resolution input demographic data, and provide insufficient detail to quantify rural settlement patterns and, thus, accurately measure population concentration and accessibility. Here we outline approaches to developing a new high resolution population distribution dataset for Africa and analyse rural accessibility to population centers. Contemporary population count data were combined with detailed satellite-derived settlement extents to map population distributions across Africa at a finer spatial resolution than ever before. Substantial heterogeneity in settlement patterns, population concentration and spatial accessibility to major population centres is exhibited across the continent. In Africa, 90% of the population is concentrated in less than 21% of the land surface and the average per-person travel time to settlements of more than 50,000 inhabitants is around 3.5 hours, with Central and East Africa displaying the longest average travel times. The analyses highlight large inequities in access, the isolation of many rural populations and the challenges that exist between countries and regions in providing access to services. The datasets presented are freely available as part of the AfriPop project, providing an evidence base for guiding strategic decisions.
doi:10.1371/journal.pone.0031743
PMCID: PMC3283664  PMID: 22363717
15.  Characterizing the interface between wild ducks and poultry to evaluate the potential of transmission of avian pathogens 
Background
Characterizing the interface between wild and domestic animal populations is increasingly recognized as essential in the context of emerging infectious diseases (EIDs) that are transmitted by wildlife. More specifically, the spatial and temporal distribution of contact rates between wild and domestic hosts is a key parameter for modeling EIDs transmission dynamics. We integrated satellite telemetry, remote sensing and ground-based surveys to evaluate the spatio-temporal dynamics of indirect contacts between wild and domestic birds to estimate the risk that avian pathogens such as avian influenza and Newcastle viruses will be transmitted between wildlife to poultry. We monitored comb ducks (Sarkidiornis melanotos melanotos) with satellite transmitters for seven months in an extensive Afro-tropical wetland (the Inner Niger Delta) in Mali and characterise the spatial distribution of backyard poultry in villages. We modelled the spatial distribution of wild ducks using 250-meter spatial resolution and 8-days temporal resolution remotely-sensed environmental indicators based on a Maxent niche modelling method.
Results
Our results show a strong seasonal variation in potential contact rate between wild ducks and poultry. We found that the exposure of poultry to wild birds was greatest at the end of the dry season and the beginning of the rainy season, when comb ducks disperse from natural water bodies to irrigated areas near villages.
Conclusions
Our study provides at a local scale a quantitative evidence of the seasonal variability of contact rate between wild and domestic bird populations. It illustrates a GIS-based methodology for estimating epidemiological contact rates at the wildlife and livestock interface integrating high-resolution satellite telemetry and remote sensing data.
doi:10.1186/1476-072X-10-60
PMCID: PMC3280937  PMID: 22085837
Distribution modelling; Satellite Telemetry; Contact rate; Remote sensing; MODIS; GPS; Maxent
16.  Trees Wanted—Dead or Alive! Host Selection and Population Dynamics in Tree-Killing Bark Beetles 
PLoS ONE  2011;6(5):e18274.
Bark beetles (Coleoptera: Curculionidae, Scolytinae) feed and breed in dead or severely weakened host trees. When their population densities are high, some species aggregate on healthy host trees so that their defences may be exhausted and the inner bark successfully colonized, killing the tree in the process. Here we investigate under what conditions participating with unrelated conspecifics in risky mass attacks on living trees is an adaptive strategy, and what this can tell us about bark beetle outbreak dynamics. We find that the outcome of individual host selection may deviate from the ideal free distribution in a way that facilitates the emergence of tree-killing (aggressive) behavior, and that any heritability on traits governing aggressiveness seems likely to exist in a state of flux or cycles consistent with variability observed in natural populations. This may have implications for how economically and ecologically important species respond to environmental changes in climate and landscape (forest) structure. The population dynamics emerging from individual behavior are complex, capable of switching between “endemic” and “epidemic” regimes spontaneously or following changes in host availability or resistance. Model predictions are compared to empirical observations, and we identify some factors determining the occurrence and self-limitation of epidemics.
doi:10.1371/journal.pone.0018274
PMCID: PMC3102062  PMID: 21647433
17.  Spatial Distribution and Risk Factors of Highly Pathogenic Avian Influenza (HPAI) H5N1 in China 
PLoS Pathogens  2011;7(3):e1001308.
Highly pathogenic avian influenza (HPAI) H5N1 was first encountered in 1996 in Guangdong province (China) and started spreading throughout Asia and the western Palearctic in 2004–2006. Compared to several other countries where the HPAI H5N1 distribution has been studied in some detail, little is known about the environmental correlates of the HPAI H5N1 distribution in China. HPAI H5N1 clinical disease outbreaks, and HPAI virus (HPAIV) H5N1 isolated from active risk-based surveillance sampling of domestic poultry (referred to as HPAIV H5N1 surveillance positives in this manuscript) were modeled separately using seven risk variables: chicken, domestic waterfowl population density, proportion of land covered by rice or surface water, cropping intensity, elevation, and human population density. We used bootstrapped logistic regression and boosted regression trees (BRT) with cross-validation to identify the weight of each variable, to assess the predictive power of the models, and to map the distribution of HPAI H5N1 risk. HPAI H5N1 clinical disease outbreak occurrence in domestic poultry was mainly associated with chicken density, human population density, and elevation. In contrast, HPAIV H5N1 infection identified by risk-based surveillance was associated with domestic waterfowl density, human population density, and the proportion of land covered by surface water. Both models had a high explanatory power (mean AUC ranging from 0.864 to 0.967). The map of HPAIV H5N1 risk distribution based on active surveillance data emphasized areas south of the Yangtze River, while the distribution of reported outbreak risk extended further North, where the density of poultry and humans is higher. We quantified the statistical association between HPAI H5N1 outbreak, HPAIV distribution and post-vaccination levels of seropositivity (percentage of effective post-vaccination seroconversion in vaccinated birds) and found that provinces with either outbreaks or HPAIV H5N1 surveillance positives in 2007–2009 appeared to have had lower antibody response to vaccination. The distribution of HPAI H5N1 risk in China appears more limited geographically than previously assessed, offering prospects for better targeted surveillance and control interventions.
Author Summary
The geographical distribution of highly pathogenic avian influenza (HPAI) H5N1 and agro-ecological risk factors have been studied in a number of countries in Southeast Asia. However, little is know of its distribution in China where HPAI H5N1 first emerged in 1996, evolved, and spread throughout Asia and the western Palearctic in 2004–2006. This study analyzes separately the distribution, in domestic poultry, of HPAI virus (HPAIV) H5N1 isolated from active risk-based surveillance sampling and HPAI H5N1 clinical disease outbreaks. These data are analyzed in relation to the distribution of chicken and domestic waterfowl population density, proportion of land covered by rice or surface water, cropping intensity, elevation, and human population density. HPAI H5N1 viruses identified by risk-based surveillance are found to be associated with domestic waterfowl density, human population density, and the proportion of land covered by surface water. In contrast, HPAI H5N1 clinical disease outbreak occurrences were mainly associated with chicken density, human population density, and low elevation. These results show that the distribution of HPAI H5N1 risk in China appears more limited geographically than previously assessed, offering prospects for better targeted surveillance and control interventions.
doi:10.1371/journal.ppat.1001308
PMCID: PMC3048366  PMID: 21408202
18.  Flying Over an Infected Landscape: Distribution of Highly Pathogenic Avian Influenza H5N1 Risk in South Asia and Satellite Tracking of Wild Waterfowl 
Ecohealth  2011;7(4):448-458.
Highly pathogenic avian influenza (HPAI) H5N1 virus persists in Asia, posing a threat to poultry, wild birds, and humans. Previous work in Southeast Asia demonstrated that HPAI H5N1 risk is related to domestic ducks and people. Other studies discussed the role of migratory birds in the long distance spread of HPAI H5N1. However, the interplay between local persistence and long-distance dispersal has never been studied. We expand previous geospatial risk analysis to include South and Southeast Asia, and integrate the analysis with migration data of satellite-tracked wild waterfowl along the Central Asia flyway. We find that the population of domestic duck is the main factor delineating areas at risk of HPAI H5N1 spread in domestic poultry in South Asia, and that other risk factors, such as human population and chicken density, are associated with HPAI H5N1 risk within those areas. We also find that satellite tracked birds (Ruddy Shelduck and two Bar-headed Geese) reveal a direct spatio-temporal link between the HPAI H5N1 hot-spots identified in India and Bangladesh through our risk model, and the wild bird outbreaks in May–June–July 2009 in China (Qinghai Lake), Mongolia, and Russia. This suggests that the continental-scale dynamics of HPAI H5N1 are structured as a number of persistence areas delineated by domestic ducks, connected by rare transmission through migratory waterfowl.
Electronic supplementary material
The online version of this article (doi:10.1007/s10393-010-0672-8) contains supplementary material, which is available to authorized users.
doi:10.1007/s10393-010-0672-8
PMCID: PMC3166606  PMID: 21267626
avian influenza; epidemiology; disease ecology; migration
19.  Persistence of Highly Pathogenic Avian Influenza H5N1 Virus Defined by Agro-Ecological Niche 
Ecohealth  2010;7(2):213-225.
The highly pathogenic avian influenza (HPAI) H5N1 virus has spread across Eurasia and into Africa. Its persistence in a number of countries continues to disrupt poultry production, impairs smallholder livelihoods, and raises the risk a genotype adapted to human-to-human transmission may emerge. While previous studies identified domestic duck reservoirs as a primary risk factor associated with HPAI H5N1 persistence in poultry in Southeast Asia, little is known of such factors in countries with different agro-ecological conditions, and no study has investigated the impact of such conditions on HPAI H5N1 epidemiology at the global scale. This study explores the patterns of HPAI H5N1 persistence worldwide, and for China, Indonesia, and India includes individual provinces that have reported HPAI H5N1 presence during the 2004–2008 period. Multivariate analysis of a set of 14 agricultural, environmental, climatic, and socio-economic factors demonstrates in quantitative terms that a combination of six variables discriminates the areas with human cases and persistence: agricultural population density, duck density, duck by chicken density, chicken density, the product of agricultural population density and chicken output/input ratio, and purchasing power per capita. The analysis identifies five agro-ecological clusters, or niches, representing varying degrees of disease persistence. The agro-ecological distances of all study areas to the medoid of the niche with the greatest number of human cases are used to map HPAI H5N1 risk globally. The results indicate that few countries remain where HPAI H5N1 would likely persist should it be introduced.
Electronic supplementary material
The online version of this article (doi:10.1007/s10393-010-0324-z) contains supplementary material, which is available to authorized users.
doi:10.1007/s10393-010-0324-z
PMCID: PMC3005111  PMID: 20585972
global ecology; highly pathogenic avian influenza; agro-ecology; epidemiology
20.  Assessing the use of global land cover data for guiding large area population distribution modelling 
Geojournal  2010;76(5):525-538.
Gridded population distribution data are finding increasing use in a wide range of fields, including resource allocation, disease burden estimation and climate change impact assessment. Land cover information can be used in combination with detailed settlement extents to redistribute aggregated census counts to improve the accuracy of national-scale gridded population data. In East Africa, such analyses have been done using regional land cover data, thus restricting application of the approach to this region. If gridded population data are to be improved across Africa, an alternative, consistent and comparable source of land cover data is required. Here these analyses were repeated for Kenya using four continent-wide land cover datasets combined with detailed settlement extents and accuracies were assessed against detailed census data. The aim was to identify the large area land cover dataset that, combined with detailed settlement extents, produce the most accurate population distribution data. The effectiveness of the population distribution modelling procedures in the absence of high resolution census data was evaluated, as was the extrapolation ability of population densities between different regions. Results showed that the use of the GlobCover dataset refined with detailed settlement extents provided significantly more accurate gridded population data compared to the use of refined AVHRR-derived, MODIS-derived and GLC2000 land cover datasets. This study supports the hypothesis that land cover information is important for improving population distribution model accuracies, particularly in countries where only coarse resolution census data are available. Obtaining high resolution census data must however remain the priority. With its higher spatial resolution and its more recent data acquisition, the GlobCover dataset was found as the most valuable resource to use in combination with detailed settlement extents for the production of gridded population datasets across large areas.
Electronic supplementary material
The online version of this article (doi:10.1007/s10708-010-9364-8) contains supplementary material, which is available to authorized users.
doi:10.1007/s10708-010-9364-8
PMCID: PMC3617592  PMID: 23576839
Population mapping; Global land cover data; Census data; Dasymetric modelling; GlobCover
21.  Anthropogenic factors and the risk of highly pathogenic avian influenza H5N1: prospects from a spatial-based model 
Veterinary Research  2009;41(3):28.
Beginning in 2003, highly pathogenic avian influenza (HPAI) H5N1 virus spread across Southeast Asia, causing unprecedented epidemics. Thailand was massively infected in 2004 and 2005 and continues today to experience sporadic outbreaks. While research findings suggest that the spread of HPAI H5N1 is influenced primarily by trade patterns, identifying the anthropogenic risk factors involved remains a challenge. In this study, we investigated which anthropogenic factors played a role in the risk of HPAI in Thailand using outbreak data from the “second wave” of the epidemic (3 July 2004 to 5 May 2005) in the country. We first performed a spatial analysis of the relative risk of HPAI H5N1 at the subdistrict level based on a hierarchical Bayesian model. We observed a strong spatial heterogeneity of the relative risk. We then tested a set of potential risk factors in a multivariable linear model. The results confirmed the role of free-grazing ducks and rice-cropping intensity but showed a weak association with fighting cock density. The results also revealed a set of anthropogenic factors significantly linked with the risk of HPAI. High risk was associated strongly with densely populated areas, short distances to a highway junction, and short distances to large cities. These findings highlight a new explanatory pattern for the risk of HPAI and indicate that, in addition to agro-environmental factors, anthropogenic factors play an important role in the spread of H5N1. To limit the spread of future outbreaks, efforts to control the movement of poultry products must be sustained.
doi:10.1051/vetres/2009076
PMCID: PMC2821766  PMID: 20003910
avian influenza; epidemiology; poultry farming; spatial analysis; Thailand
22.  REMOTE SENSING, ECOLOGICAL VARIABLES, AND WILD BIRD MIGRATION RELATED TO OUTBREAKS OF HIGHLY PATHOGENIC H5N1 AVIAN INFLUENZA1 
Journal of wildlife diseases  2007;43(1):40-47.
Outbreaks of highly pathogenic avian influenza (HPAI) H5N1 subtype have occurred in many countries across Asia, Europe, and Africa since 2003. Better understanding of the ecology and risk factors of HPAI is critical for surveillance, risk assessment, and public health policy. We introduce satellite remote sensing as one important tool, and highlight the potential of using satellite images to monitor dynamics of climate and landscapes that are related to wild bird migration and agriculture in the context of avian influenza transmission.
PMCID: PMC2735754  PMID: 17347392
Avian influenza; land surface temperature; MODIS images; paddy rice
23.  Avian influenza, domestic ducks and rice agriculture in Thailand 
Highly pathogenic avian influenza (HPAI) caused by H5N1 viruses has become a global scale problem which first emerged in southern China and from there spread to other countries in Southeast and East Asia, where it was first confirmed in end 2003. In previous work, geospatial analyses demonstrated that free grazing ducks played critical role in the epidemiology of the disease in Thailand in the winter 2004/2005, both in terms of HPAI emergence and spread. This study explored the geographic association between free grazing duck census counts and current statistics on the spatial distribution of rice crops in Thailand, in particular the crop calendar of rice production. The analysis was carried out using both district level rice statistics and rice distribution data predicted with the aid of remote sensing, using a rice-detection algorithm. The results indicated a strong association between the number of free grazing ducks and the number of months during which second-crop rice harvest takes place, as well as with the rice crop intensity as predicted by remote sensing. These results confirmed that free grazing duck husbandry was strongly driven by agricultural land use and rice crop intensity, and that this later variable can be readily predicted using remote sensing. Analysis of rice cropping patterns may provide an indication of the location of populations of free grazing ducks in other countries with similar mixed duck and rice production systems and less detailed duck census data. Apart from free ranging ducks and rice cropping, the role of hydrology and seasonality of wetlands and water bodies in the HPAI risk analysis is also discussed in relation to the presumed dry season aggregation of wild waterfowl and aquatic poultry offering much scope for virus transmission.
doi:10.1016/j.agee.2006.09.001
PMCID: PMC2311503  PMID: 18418464
Highly pathogenic avian influenza; Domestic ducks; Remote sensing; Agriculture intensification; Rice paddy production
24.  Anatidae Migration in the Western Palearctic and Spread of Highly Pathogenic Avian Influenza H5N1 Virus 
Emerging Infectious Diseases  2006;12(11):1650-1656.
Anatids may have spread the virus along their autumn migration routes.
During the second half of 2005, highly pathogenic avian influenza (HPAI) H5N1 virus spread rapidly from central Asia to eastern Europe. The relative roles of wild migratory birds and the poultry trade are still unclear, given that little is yet known about the range of virus hosts, precise movements of migratory birds, or routes of illegal poultry trade. We document and discuss the spread of the HPAI H5N1 virus in relation to species-specific flyways of Anatidae species (ducks, geese, and swans) and climate. We conclude that the spread of HPAI H5N1 virus from Russia and Kazakhstan to the Black Sea basin is consistent in space and time with the hypothesis that birds in the Anatidae family have seeded the virus along their autumn migration routes.
doi:10.3201/eid1211.060223
PMCID: PMC3372333  PMID: 17283613
Avian influenza; Epidemiology; Disease Ecology; Migration; perspective
25.  Free-grazing Ducks and Highly Pathogenic Avian Influenza, Thailand 
Emerging Infectious Diseases  2006;12(2):227-234.
Free-grazing ducks in rice paddies are a critical factor in the spread and persistence of avian influenza.
Thailand has recently had 3 epidemic waves of highly pathogenic avian influenza (HPAI); virus was again detected in July 2005. Risk factors need to be identified to better understand disease ecology and assist HPAI surveillance and detection. This study analyzed the spatial distribution of HPAI outbreaks in relation to poultry, land use, and other anthropogenic variables from the start of the second epidemic wave (July 2004–May 2005). Results demonstrate a strong association between H5N1 virus in Thailand and abundance of free-grazing ducks and, to a lesser extent, native chickens, cocks, wetlands, and humans. Wetlands used for double-crop rice production, where free-grazing duck feed year round in rice paddies, appear to be a critical factor in HPAI persistence and spread. This finding could be important for other duck-producing regions in eastern and southeastern Asian countries affected by HPAI.
doi:10.3201/eid1202.050640
PMCID: PMC3373083  PMID: 16494747
Avian influenza; epidemiology; spatial analysis; Thailand; animal husbandry; research

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