Co-circulation of genetically distinct highly pathogenic avian influenza A clade 2.3.4.4 (H5N6) viruses in wild waterfowl and poultry in Europe and East Asia, 2017-18

Abstract

Highly pathogenic avian influenza (HPAI) H5 clade 2.3.4.4 viruses were first introduced into Europe in late 2014 and re-introduced in late 2016, following detections in Asia and Russia. In contrast to the 2014-15 H5N8 wave, there was substantial local virus amplification in wild birds in Europe in 2016-17 and associated wild bird mortality, with evidence for occasional gene exchange with low pathogenic avian influenza (LPAI) viruses. Since December 2017, several European countries have again reported events or outbreaks with HPAI H5N6 reassortant viruses in both wild birds and poultry, respectively. Previous phylogenetic studies have shown that the two earliest incursions of HPAI H5N8 viruses originated in Southeast Asia and subsequently spread to Europe. In contrast, this study indicates that recent HPAI H5N6 viruses evolved from the H5N8 2016-17 viruses during 2017 by reassortment of a European HPAI H5N8 virus and wild host reservoir LPAI viruses. The genetic and phenotypic differences between these outbreaks and the continuing detections of HPAI viruses in Europe are a cause of concern for both animal and human health. The current co-circulation of potentially zoonotic HPAI and LPAI virus strains in Asia warrants the determination of drivers responsible for the global spread of Asian lineage viruses and the potential threat they pose to public health.

Keywords: H5N6; avian influenza; emerging diseases; highly pathogenic avian influenza; phylogeny; virology.

Figure 1.

Overview of the number of wild birds reported to be infected with HPAI H5N6 based on the OIE update on avian influenza in animals (types H5 and H7) list 2017/2018 (OIE 2017; OIE 2018) per week starting from the first detection on 7 December 2017. The colours represent the country of detection. The asterisks (*) indicate the detections of HPAI H5N6 viruses in commercial (green) and backyard (blue) poultry.

Figure 2.

BEAST trees from viral sequences of HA (H5) gene sequences isolated from avian hosts between January 2016 and April 2018 with the addition of four H5N6 HA genes isolated from humans and seven co-circulating HPAI H5N2/H5N8 viruses (purple). Tip symbols are coloured according to the HA origin displaying our European-SOI (blue), Asian-SOI (red), the Chinese HPAI H5N6 viruses (orange) with the Chinese human-derived viruses (black), the 2016–17 HPAI H5N8 viruses (green), and other HPAI H5Nx viruses (purple). Tip symbols depict the location: Central Asia/Russia (●), Eastern/Southern Asia (▲), Europe (■), and other (+). Presence of node symbol (♦) indicates posterior P > 0.85. The numbers above the nodes represent TMRCA, the grey bars display the accompanying 95 per cent confidence interval. Viruses marked with an asterisk (*) were obtained and sequenced within the surveillance activities described in this manuscript.

Figure 3.

BEAST trees from viral sequences of NA (N6) gene sequences isolated from avian hosts between January 2007 and April 2018. Tip symbols are coloured according to the HA origin with recent Asian (red) and European (blue) HPAI H5N6 viruses, the early 2017 Greek (GRC) HPAI H5N6 (green), and (non-H5) HxN6 (grey) viruses. Symbols depict the location: Central Asia/Russia (●), Eastern/Southern Asia (▲) and Europe (■). Presence of node symbol (♦) indicates posterior P > 0.85. The numbers above the nodes represent TMRCA, the grey bars display the accompanying 95 per cent confidence interval. Viruses marked with an asterisk (*) were obtained and sequenced within the surveillance activities described in this manuscript.

Figure 4.

Phylogenetic incongruence analysis. Maximum likelihood trees for the HA segment and all internal genes MP, NP, NS, PA, PB1, and PB2 from equivalent strains were connected across the trees. Tips and connecting lines are coloured according to HA clade.