Highly Pathogenic Avian Influenza Viruses at the Wild-Domestic Bird Interface in Europe: Future Directions for Research and Surveillance

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.

Keywords: aquatic birds; avian influenza; ecology; epidemiology; evolution; highly pathogenic avian influenza; influenza subtypes; influenza surveillance; migratory birds; migratory flyways.

Figure 1

Highly pathogenic avian influenza H5 GsGd virus detections in wild birds and poultry in Europe, 2005–2020. Each panel shows the European countries in which the subclade had been detected, including the time period. Green, viruses detected in wild birds; orange, viruses detected in poultry; green-orange striped pattern, subclade detected in both wild birds and poultry at country level; light green, clade 2.2 viruses detected in wild birds and subclade unknown; light orange, clade 2.2 viruses detected in poultry and subclade unknown. References used [24,34,35,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57].

Figure 2

Highly pathogenic avian influenza H5 GsGd virus incursions into Europe (2005–2020) were associated with abundant reassortment with Asian and European low pathogenic avian influenza viruses. Multiple different clade 2.3.4.4b assortments circulated with some variants containing genomic segments derived from low pathogenic avian influenza viruses circulating in wild birds in Europe, suggesting reassortment upon introduction into Europe. Please note that inference of reassortment location is heavily biased by the intensity of influenza surveillance and the availability of virus genome sequences. References used [35,55,76].