Abstract

Highly pathogenic avian influenza (HPAI) outbreaks in wild birds and poultry are no longer a rare phenomenon in Europe. In the past 15 years, HPAI outbreaks—in particular those caused by H5 viruses derived from the A/Goose/Guangdong/1/1996 lineage that emerged in southeast Asia in 1996—have been occuring with increasing frequency in Europe. Between 2005 and 2020, at least ten HPAI H5 incursions were identified in Europe resulting in mass mortalities among poultry and wild birds. Until 2009, the HPAI H5 virus outbreaks in Europe were caused by HPAI H5N1 clade 2.2 viruses, while from 2014 onwards HPAI H5 clade 2.3.4.4 viruses dominated outbreaks, with abundant genetic reassortments yielding subtypes H5N1, H5N2, H5N3, H5N4, H5N5, H5N6 and H5N8. The majority of HPAI H5 virus detections in wild and domestic birds within Europe coincide with southwest/westward fall migration and large local waterbird aggregations during wintering. In this review we provide an overview of HPAI H5 virus epidemiology, ecology and evolution at the interface between poultry and wild birds based on 15 years of avian influenza virus surveillance in Europe, and assess future directions for HPAI virus research and surveillance, including the integration of whole genome sequencing, host identification and avian ecology into risk-based surveillance and analyses.

Highlights

  • Wild waterbirds belonging to the order Anseriformes and Charadriiformes are the natural reservoir of low pathogenic avian influenza (LPAI) viruses

  • Significant progress has been made in describing highly pathogenic avian influenza (HPAI) H5 virus evolution and epidemiology—in particular, with respect to the identification of host species, time periods, habitats and geographies associated with increased risks of HPAI H5 introduction—due to collaborative efforts of virologists, ornithologists, ecologists, pathologists, and mathematical modellers amongst others, and due to faster and specific diagnostics, in particular, gene sequencing technologies

  • Following the initial detection of H5N8 clade 2.3.4.4b viruses, abundant reassortment with LPAI viruses was observed in poultry and wild birds in 2016–2017, resulting in the emergence of HPAI H5N5 viruses in several European countries between November

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Summary

Introduction

Wild waterbirds belonging to the order Anseriformes (mainly ducks, geese, swans) and Charadriiformes (gulls, terns, shorebirds) are the natural reservoir of low pathogenic avian influenza (LPAI) viruses. In 2009, a new clade of HPAI H5 GsGd caused mortality among wild birds at Qinghai Lake (clade 2.3.2), followed by outbreaks among poultry and wild birds within Asia These viruses were ancestral to the HPAI H5 clade 2.3.2.1c viruses detected in eastern Europe in 2010 and 2015. In response to the emergence of HPAI H5 GsGd viruses, outbreaks in wild birds and the long-distance dispersal of the viruses, avian influenza virus surveillance programs in wild birds and poultry were initiated and intensified globally These programs aimed at the early detection of (novel) HPAI H5 viruses into new geographical regions, and to investigate the role of wild birds in the spread of these HPAI H5 viruses. We provide recommendations for future research and surveillance to achieve earlier detection of novel HPAI viruses and further understanding of HPAI H5 evolution and epidemiology, as major gaps in knowledge remain

Recurring Emergence of HPAI H5 Viruses in Europe 2005–2020
Underlying
11 European countries tral to the emergence of novel
Underlying Mechanisms of Emergence of Novel HPAI H5 Viruses at the
Environmental-Related Drivers for Emergence of Novel HPAI H5 Viruses in
HPAI H5 Virus Introductions into Europe by Wild Birds
HPAI H5 Virus Introductions into Poultry Farms by Wild Birds
Whole Genome Sequencing
Environmental Monitoring
Host Species Identification
Wild Bird Surveillance Site Selection
Active Surveillance and Mitigation
Conclusions
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