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1.  Movements of Wild Ruddy Shelducks in the Central Asian Flyway and Their Spatial Relationship to Outbreaks of Highly Pathogenic Avian Influenza H5N1 
Viruses  2013;5(9):2129-2152.
Highly pathogenic avian influenza H5N1 remains a serious concern for both poultry and human health. Wild waterfowl are considered to be the reservoir for low pathogenic avian influenza viruses; however, relatively little is known about their movement ecology in regions where HPAI H5N1 outbreaks regularly occur. We studied movements of the ruddy shelduck (Tadorna ferruginea), a wild migratory waterfowl species that was infected in the 2005 Qinghai Lake outbreak. We defined their migration with Brownian Bridge utilization distribution models and their breeding and wintering grounds with fixed kernel home ranges. We correlated their movements with HPAI H5N1 outbreaks, poultry density, land cover, and latitude in the Central Asian Flyway. Our Akaike Information Criterion analysis indicated that outbreaks were correlated with land cover, latitude, and poultry density. Although shelduck movements were included in the top two models, they were not a top parameter selected in AICc stepwise regression results. However, timing of outbreaks suggested that outbreaks in the flyway began during the winter in poultry with spillover to wild birds during the spring migration. Thus, studies of the movement ecology of wild birds in areas with persistent HPAI H5N1 outbreaks may contribute to understanding their role in transmission of this disease.
PMCID: PMC3798894  PMID: 24022072
Brahminy duck; movement ecology; Tadorna ferruginea; avian influenza
2.  Mapping Avian Influenza Transmission Risk at the Interface of Domestic Poultry and Wild Birds 
Emergence of avian influenza viruses with high lethality to humans, such as the currently circulating highly pathogenic A(H5N1) (emerged in 1996) and A(H7N9) cause serious concern for the global economic and public health sectors. Understanding the spatial and temporal interface between wild and domestic populations, from which these viruses emerge, is fundamental to taking action. This information, however, is rarely considered in influenza risk models, partly due to a lack of data. We aim to identify areas of high transmission risk between domestic poultry and wild waterfowl in China, the epicenter of both viruses. Two levels of models were developed: one that predicts hotspots of novel virus emergence between domestic and wild birds, and one that incorporates H5N1 risk factors, for which input data exists. Models were produced at 1 and 30 km spatial resolution, and two temporal seasons. Patterns of risk varied between seasons with higher risk in the northeast, central-east, and western regions of China during spring and summer, and in the central and southeastern regions during winter. Monte-Carlo uncertainty analyses indicated varying levels of model confidence, with lowest errors in the densely populated regions of eastern and southern China. Applications and limitations of the models are discussed within.
PMCID: PMC3854848  PMID: 24350197
H5N1; avian influenza; spatial modeling; uncertainty; China; waterfowl; poultry; Monte-Carlo
3.  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.
PMCID: PMC3134362  PMID: 21765567
poultry; China; distribution modelling; population estimates; GIS; epidemiology
4.  Eco-Virological Approach for Assessing the Role of Wild Birds in the Spread of Avian Influenza H5N1 along the Central Asian Flyway 
PLoS ONE  2012;7(2):e30636.
A unique pattern of highly pathogenic avian influenza (HPAI) H5N1 outbreaks has emerged along the Central Asia Flyway, where infection of wild birds has been reported with steady frequency since 2005. We assessed the potential for two hosts of HPAI H5N1, the bar-headed goose (Anser indicus) and ruddy shelduck (Tadorna tadorna), to act as agents for virus dispersal along this ‘thoroughfare’. We used an eco-virological approach to compare the migration of 141 birds marked with GPS satellite transmitters during 2005–2010 with: 1) the spatio-temporal patterns of poultry and wild bird outbreaks of HPAI H5N1, and 2) the trajectory of the virus in the outbreak region based on phylogeographic mapping. We found that biweekly utilization distributions (UDs) for 19.2% of bar-headed geese and 46.2% of ruddy shelduck were significantly associated with outbreaks. Ruddy shelduck showed highest correlation with poultry outbreaks owing to their wintering distribution in South Asia, where there is considerable opportunity for HPAI H5N1 spillover from poultry. Both species showed correlation with wild bird outbreaks during the spring migration, suggesting they may be involved in the northward movement of the virus. However, phylogeographic mapping of HPAI H5N1 clades 2.2 and 2.3 did not support dissemination of the virus in a northern direction along the migration corridor. In particular, two subclades (2.2.1 and 2.3.2) moved in a strictly southern direction in contrast to our spatio-temporal analysis of bird migration. Our attempt to reconcile the disciplines of wild bird ecology and HPAI H5N1 virology highlights prospects offered by both approaches as well as their limitations.
PMCID: PMC3274535  PMID: 22347393
5.  Wild Bird Migration across the Qinghai-Tibetan Plateau: A Transmission Route for Highly Pathogenic H5N1 
PLoS ONE  2011;6(3):e17622.
Qinghai Lake in central China has been at the center of debate on whether wild birds play a role in circulation of highly pathogenic avian influenza virus H5N1. In 2005, an unprecedented epizootic at Qinghai Lake killed more than 6000 migratory birds including over 3000 bar-headed geese (Anser indicus). H5N1 subsequently spread to Europe and Africa, and in following years has re-emerged in wild birds along the Central Asia flyway several times.
Methodology/Principal Findings
To better understand the potential involvement of wild birds in the spread of H5N1, we studied the movements of bar-headed geese marked with GPS satellite transmitters at Qinghai Lake in relation to virus outbreaks and disease risk factors. We discovered a previously undocumented migratory pathway between Qinghai Lake and the Lhasa Valley of Tibet where 93% of the 29 marked geese overwintered. From 2003–2009, sixteen outbreaks in poultry or wild birds were confirmed on the Qinghai-Tibet Plateau, and the majority were located within the migratory pathway of the geese. Spatial and temporal concordance between goose movements and three potential H5N1 virus sources (poultry farms, a captive bar-headed goose facility, and H5N1 outbreak locations) indicated ample opportunities existed for virus spillover and infection of migratory geese on the wintering grounds. Their potential as a vector of H5N1 was supported by rapid migration movements of some geese and genetic relatedness of H5N1 virus isolated from geese in Tibet and Qinghai Lake.
This is the first study to compare phylogenetics of the virus with spatial ecology of its host, and the combined results suggest that wild birds play a role in the spread of H5N1 in this region. However, the strength of the evidence would be improved with additional sequences from both poultry and wild birds on the Qinghai-Tibet Plateau where H5N1 has a clear stronghold.
PMCID: PMC3052365  PMID: 21408010
6.  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.
PMCID: PMC3048366  PMID: 21408202
7.  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.
PMCID: PMC3166606  PMID: 21267626
avian influenza; epidemiology; disease ecology; migration
8.  Migration of Whooper Swans and Outbreaks of Highly Pathogenic Avian Influenza H5N1 Virus in Eastern Asia 
PLoS ONE  2009;4(5):e5729.
Evaluating the potential involvement of wild avifauna in the emergence of highly pathogenic avian influenza H5N1 (hereafter H5N1) requires detailed analyses of temporal and spatial relationships between wild bird movements and disease emergence. The death of wild swans (Cygnus spp.) has been the first indicator of the presence of H5N1 in various Asian and European countries; however their role in the geographic spread of the disease remains poorly understood. We marked 10 whooper swans (Cygnus cygnus) with GPS transmitters in northeastern Mongolia during autumn 2006 and tracked their migratory movements in relation to H5N1 outbreaks. The prevalence of H5N1 outbreaks among poultry in eastern Asia during 2003–2007 peaked during winter, concurrent with whooper swan movements into regions of high poultry density. However outbreaks involving poultry were detected year round, indicating disease perpetuation independent of migratory waterbird presence. In contrast, H5N1 outbreaks involving whooper swans, as well as other migratory waterbirds that succumbed to the disease in eastern Asia, tended to occur during seasons (late spring and summer) and in habitats (areas of natural vegetation) where their potential for contact with poultry is very low to nonexistent. Given what is known about the susceptibility of swans to H5N1, and on the basis of the chronology and rates of whooper swan migration movements, we conclude that although there is broad spatial overlap between whooper swan distributions and H5N1 outbreak locations in eastern Asia, the likelihood of direct transmission between these groups is extremely low. Thus, our data support the hypothesis that swans are best viewed as sentinel species, and moreover, that in eastern Asia, it is most likely that their infections occurred through contact with asymptomatic migratory hosts (e.g., wild ducks) at or near their breeding grounds.
PMCID: PMC2684635  PMID: 19479053

Results 1-8 (8)