Wild Bird Migration across the Qinghai-Tibetan Plateau: A Transmission Route for Highly Pathogenic H5N1

Diann J Prosser,Yongdong Li,Zhi Xing,David C Douglas,Fumin Lei,Scott H Newman,Shan Guo,Nichola J Hill,William M Perry,John Y Takekawa,Yubang He,Yuansheng Hou,Tianxian Li,Yuanchun Zhou,Baoping Yan,Mingjie Tang,Peng Cui,Bridget M Collins,Yan Ropert-Coudert

doi:10.1371/journal.pone.0017622

Abstract

BackgroundQinghai 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 FindingsTo 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.Conclusions/SignificanceThis 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.

Highlights

Pathogenic avian influenza (HPAI) subtype H5N1 first emerged in domestic geese of south-eastern China in 1996 [1,2] and has since become endemic in poultry across much of Eurasia [3,4]
We hypothesized that if bar-headed geese were a significant contributor in the spread of H5N1 to Qinghai Lake (QHL), certain conditions would have had to occur: (1) exposure of geese to virus sources prior to arriving at QHL, (2) onset of migration and viral shedding before individuals became physiologically compromised, and (3) evidence of genetic relatedness between isolates from virus source regions frequented by geese and QHL
Our findings indicate that these conditions were met; we discuss caveats in our findings based on the most current H5N1 disease ecology

Summary

Introduction

Pathogenic avian influenza (HPAI) subtype H5N1 (hereafter H5N1) first emerged in domestic geese of south-eastern China in 1996 [1,2] and has since become endemic in poultry across much of Eurasia [3,4]. The first reports of spillover to wild birds occurred in low numbers of captive waterbirds at a Hong Kong waterfowl park in 2002 [7]. It was not until April 2005 that the first large epizootic (more than 6000 birds) occurred in wild species on the remote breeding grounds of Qinghai Lake (QHL), northwestern China [8,9]. 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. H5N1 subsequently spread to Europe and Africa, and in following years has re-emerged in wild birds along the Central Asia flyway several times

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Results

Conclusion