Genesis and spread of multiple reassortants during the 2016/2017 H5 avian influenza epidemic in Eurasia

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Highly pathogenic avian influenza (HPAI) viruses of the H5 A/goose/ Guangdong/1/96 lineage can cause severe disease in poultry and wild birds, and occasionally in humans. In recent years, H5 HPAI viruses of this lineage infecting poultry in Asia have spilled over into wild birds and spread via bird migration to countries in Europe, Africa, and North America. In 2016/2017, this spillover resulted in the largest HPAI epidemic on record in Europe and was associated with an unusually high frequency of reassortments between H5 HPAI viruses and cocirculating low-pathogenic avian influenza viruses. Here, we show that the seven main H5 reassortant viruses had various combinations of gene segments 1, 2, 3, 5, and 6. Using detailed time-resolved phylogenetic analysis, most of these gene segments likely originated from wild birds and at dates and locations that corresponded to their hosts' migratory cycles. However, some gene segments in two reassortant viruses likely originated from domestic anseriforms, either in spring 2016 in east China or in autumn 2016 in central Europe. Our results demonstrate that, in addition to domestic anseriforms in Asia, both migratory wild birds and domestic anseriforms in Europe are relevant sources of gene segments for recent reassortant H5 HPAI viruses. The ease with which these H5 HPAI viruses reassort, in combination with repeated spillovers of H5 HPAI viruses into wild birds, increases the risk of emergence of a reassortant virus that persists in wild bird populations yet remains highly pathogenic for poultry.

OriginalsprogEngelsk
TidsskriftProceedings of the National Academy of Sciences of the United States of America
Vol/bind117
Udgave nummer34
Sider (fra-til)20814-20825
Antal sider12
ISSN0027-8424
DOI
StatusUdgivet - 2020

Bibliografisk note

Funding Information:
We thank Nicole Reimer and Patrick Wysocki for technical assistance in the preparation of the maps and Franz Conraths for critical review of the manuscript. This work was supported by European Union Horizon 2020 COllaborative Management Platform for detection and Analyses of (Re-) emerging and foodborne outbreaks in Europe (COMPARE) Grant 643476 and Dynamics of avian influenza in a changing world (DELTA-FLU) Grant 727922, by the Biotechnology and Biosciences Research Council (BBSRC) Institute Strategic Programme Grant: Control of Infectious Diseases BBS/E/D/20002173, and by the Scottish Government Rural and Environment Science and Analytical Services Division as part of the Centre of Expertise on Animal Disease Outbreaks (EPIC). S.J.L. is also supported by a University of Edinburgh Chancellor’s Fellowship. The map in Fig. 5 was created using ArcGISÒ software by Esri. ArcGISÒ and ArcMapTM are the intellectual property of Esri and are used herein under license. Copyright © Esri. All rights reserved. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Government.

Funding Information:
ACKNOWLEDGMENTS. We thank Nicole Reimer and Patrick Wysocki for technical assistance in the preparation of the maps and Franz Conraths for critical review of the manuscript. This work was supported by European Union Horizon 2020 COllaborative Management Platform for detection and Analyses of (Re-) emerging and foodborne outbreaks in Europe (COMPARE) Grant 643476 and Dynamics of avian influenza in a changing world (DELTA-FLU) Grant 727922, by the Biotechnology and Biosciences Research Council (BBSRC) Institute Strategic Programme Grant: Control of Infectious Diseases BBS/E/D/20002173, and by the Scottish Government Rural and Environment Science and Analytical Services Division as part of the Centre of Expertise on Animal Disease Outbreaks (EPIC). S.J.L. is also supported by a University of Edinburgh Chancellor’s Fellowship. The map in Fig. 5 was created using ArcGIS® software by Esri. ArcGIS® and ArcMapTM are the intellectual property of Esri and are used herein under license. Copyright © Esri. All rights reserved. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Government.

Publisher Copyright:
Copyright © Esri. All rights reserved. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Government.

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