Proposal for a Global Classification and Nomenclature System for A/H9 Influenza Viruses

Abstract

Influenza A/H9 viruses circulate worldwide in wild and domestic avian species, continuing to evolve and posing a zoonotic risk. A substantial increase in human infections with A/H9N2 subtype avian influenza viruses (AIVs) and the emergence of novel reassortants carrying A/H9N2-origin internal genes has occurred in recent years. Different names have been used to describe the circulating and emerging A/H9 lineages. To address this issue, an international group of experts from animal and public health laboratories, endorsed by the WOAH/FAO Network of Expertise on Animal Influenza, has created a practical lineage classification and nomenclature system based on the analysis of 10,638 hemagglutinin sequences from A/H9 AIVs sampled worldwide. This system incorporates phylogenetic relationships and epidemiologic characteristics designed to trace emerging and circulating lineages and clades. To aid in lineage and clade assignment, an online tool has been created. This proposed classification enables rapid comprehension of the global spread and evolution of A/H9 AIVs.

Keywords: A/H9 influenza viruses; Lan Y; Lu L; Pu J; Suggested citation for this article: Fusaro A; Tassoni L; Zhou Y; classification; et al. Proposal for a global classification and nomenclature system for A/H9 influenza viruses. Emerg Infect Dis. 2024 August [date cited]. https://doi.org/10.3201/eid3008.231176; global; hemagglutinin; influenza; nomenclature; phylogeny; respiratory infections; viruses.

Figure 1

Phylogenetic trees and assigned clades of as part of a proposed global classification and nomenclature system for A/H9 influenza viruses. A) Maximum-likelihood (ML) phylogenetic tree obtained using the complete dataset. The branches are colored according to the 3 identified lineages. A/quail/Hong Kong/A28945/1988 and A/Quail/Hong Kong/AF157/1992 were used as an outgroup black). B) ML phylogenetic tree of the Y lineage dataset. Six sequences of the G lineage were used as the outgroup. Numbers next to the clade-defining nodes represent ultra-fast bootstrap supports. Clades are labeled and marked in colors. C) ML phylogenetic tree of the G lineage. Six sequences of the Y lineage were selected as the outgroup. Numbers next to the clade-defining nodes represent ultra-fast bootstrap supports. Clades are labeled and marked in colors. D) ML phylogenetic tree of the B lineage. Six sequences of the Y lineage were used as the outgroup. Numbers next to the clade-defining nodes represent ultra-fast bootstrap supports. Clades are labeled and marked in colors. Scale bars indicate substitutions per site.

Figure 2

Pilot maximum-likelihood phylogenetic tree of the A/H9 influenza virus gene sequences obtained by using the representative dataset (Appendix 3) for the Y lineage provided as part of a proposed global classification and nomenclature system for A/H9 influenza viruses. Each clade is represented by >3 sequences, each labeled and colored according to the clade of belonging. Ultrafast-bootstrap supports >80% are indicated next to nodes. Scale bar indicates substitutions per site.

Figure 3

Pilot maximum-likelihood phylogenetic tree of the A/H9 influenza virus gene sequences obtained by using the representative dataset (Appendix 3) for the G lineage provided as part of a proposed global classification and nomenclature system for A/H9 influenza viruses. Each clade is represented by >3 sequences, each labeled and colored according to the clade of belonging. Ultrafast-bootstrap supports >80% are indicated next to nodes. Scale bar indicates substitutions per site.

Figure 4

Pilot maximum-likelihood phylogenetic tree of the A/H9 influenza virus gene sequences obtained by using the representative dataset (Appendix 3) for the B lineage provided as part of a proposed global classification and nomenclature system for A/H9 influenza viruses. Each clade is represented by >3 sequences, each labeled and colored according to the clade of belonging. Ultrafast-bootstrap supports >80% are indicated next to nodes. Scale bar indicates substitutions per site.

Figure 5

Temporal distribution of each lineage and clade for A/H9 influenza viruses as part of a proposed global classification and nomenclature system for A/H9 influenza viruses. The heat map displays the number of sequences for each lineage and clade per year.

Figure 6

Geographic distribution of each lineage and clade for A/H9 influenza viruses as part of a proposed global classification and nomenclature system for A/H9 influenza viruses. The heat map displays the number of sequences for each lineage and clade per country. Countries were ordered by their macro-region (upper panels). Each country displaying >1 sequence was colored on the map in green (Y lineage), blue (G lineage), or red (B lineage) (bottom panels).

Figure 7

Host distribution of each lineage and clade for A/H9 influenza viruses as part of a proposed global classification and nomenclature system for A/H9 influenza viruses. The bar chart illustrates the percentage of host composition for each lineage and clade. Hosts are grouped into the following categories, represented as colors on each bar: avian wild, avian domestic, avian (birds that are not identified as wild or domestic), environment, human, and mammalian (other than human).