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. 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.

Poyang Lake is situated within the East Asian Flyway, a migratory corridor for waterfowl that also encompasses Guangdong Province, China, the epicenter of highly pathogenic avian influenza (HPAI) H5N1. The lake is the largest freshwater body in China and a significant congregation site for waterfowl; however, surrounding rice fields and poultry grazing have created an overlap with wild waterbirds, a situation conducive to avian influenza transmission. Reports of HPAI H5N1 in healthy wild ducks at Poyang Lake have raised concerns about the potential of resilient free-ranging birds to disseminate the virus. Yet the role wild ducks play in connecting regions of HPAI H5N1 outbreak in Asia is hindered by a lack of information about their migratory ecology. During 2007–08 we marked wild ducks at Poyang Lake with satellite transmitters to examine the location and timing of spring migration and identify any spatiotemporal relationship with HPAI H5N1 outbreaks. Species included the Eurasian wigeon (Anas penelope), northern pintail (Anas acuta), common teal (Anas crecca), falcated teal (Anas falcata), Baikal teal (Anas formosa), mallard (Anas platyrhynchos), garganey (Anas querquedula), and Chinese spotbill (Anas poecilohyncha). These wild ducks (excluding the resident mallard and Chinese spotbill ducks) followed the East Asian Flyway along the coast to breeding areas in northern China, eastern Mongolia, and eastern Russia. None migrated west toward Qinghai Lake (site of the largest wild bird epizootic), thus failing to demonstrate any migratory connection to the Central Asian Flyway. A newly developed Brownian bridge spatial analysis indicated that HPAI H5N1 outbreaks reported in the flyway were related to latitude and poultry density but not to the core migration corridor or to wetland habitats. Also, we found a temporal mismatch between timing of outbreaks and wild duck movements. These analyses depend on complete or representative reporting of outbreaks, but by documenting movements of wild waterfowl, we present ecological knowledge that better informs epidemiological investigations seeking to explain and predict the spread of avian influenza viruses.

Prior to the emergence of the A/goose/Guangdong/1/1996 (Gs/GD) H5N1 influenza A virus, the long‐held and well‐supported paradigm was that highly pathogenic avian influenza (HPAI) outbreaks were restricted to poultry, the result of cross‐species transmission of precursor viruses from wild aquatic birds that subsequently gained pathogenicity in domestic birds. Therefore, management agencies typically adopted a prevention, control, and eradication strategy that included strict biosecurity for domestic bird production, isolation of infected and exposed flocks, and prompt depopulation. In most cases, this strategy has proved sufficient for eradicating HPAI. Since 2002, this paradigm has been challenged with many detections of viral descendants of the Gs/GD lineage among wild birds, most of which have been associated with sporadic mortality events. Since the emergence and evolution of the genetically distinct clade 2.3.4.4 Gs/GD lineage HPAI viruses in approximately 2010, there have been further increases in the occurrence of HPAI in wild birds and geographic spread through migratory bird movement. A prominent example is the introduction of clade 2.3.4.4 Gs/GD HPAI viruses from East Asia to North America via migratory birds in autumn 2014 that ultimately led to the largest outbreak of HPAI in the history of the United States. Given the apparent maintenance of Gs/GD lineage HPAI viruses in a global avian reservoir; bidirectional virus exchange between wild and domestic birds facilitating the continued adaptation of Gs/GD HPAI viruses in wild bird hosts; the current frequency of HPAI outbreaks in wild birds globally, and particularly in Eurasia where Gs/GD HPAI viruses may now be enzootic; and ongoing dispersal of AI viruses from East Asia to North America via migratory birds, HPAI now represents an emerging disease threat to North American wildlife. This recent paradigm shift implies that management of HPAI in domestic birds alone may no longer be sufficient to eradicate HPAI viruses from a given country or region. Rather, agencies managing wild birds and their habitats may consider the development or adoption of mitigation strategies to minimize introductions to poultry, to reduce negative impacts on wild bird populations, and to diminish adverse effects to stakeholders using wildlife resources. The main objective of this review is, therefore, to provide information that will assist wildlife managers in developing mitigation strategies or approaches for dealing with outbreaks of Gs/GD HPAI in wild birds in the form of preparedness, surveillance, research, communications, and targeted management actions. Resultant outbreak response plans and actions may represent meaningful steps of wildlife managers toward the use of collaborative and multi‐jurisdictional One Health approaches when it comes to the detection, investigation, and mitigation of emerging viruses at the human‐domestic animal‐wildlife interface.

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. 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.