In late 2014, a highly pathogenic avian influenza (hereafter HPAI) H5N1 outbreak infected whooper swans Cygnus cygnus wintering at the Sanmenxia Reservoir area, China, and raised concerns about migratory linkages between wintering and breeding grounds of whooper swans. In this study, 61 swans were satellite tracked from 2013 to 2016 to determine the spatial association of their migration routes and H5N1 outbreaks, and 3596 fecal samples were collected along the migration routes for virology testing. Swans departed the wintering grounds and migrated along the Yellow River, and flew over the Yin Mountains in China. The Brownian bridge movement model showed there was a high degree of spatiotemporal overlap between the core use area along the spring migration pathway and historical H5N1 events in China and Mongolia from 2005 to 2015. The H5N1 strain was isolated and phylogenetic analyses confirmed that the HA gene sequence generated is genetically similar to that of the epidemic strain at a previous wintering site (the Sanmenxia Reservoir area) along its flyway. Our results identified a previously unknown migratory link of whooper swans in central China with Mongolia and confirmed that the swans could carry the HPAI H5N1 virus during migration, resulting in long-distance transmission.

Highly pathogenic influenza A(H5N8) viruses have caused several worldwide outbreaks in birds and are able cross the species barrier to infect humans, posing a substantial threat to public health. After the first detection of H5N8 viruses in deceased swans in Inner Mongolia, we performed early warning and active monitoring along swan migration routes in central China. We isolated and sequenced 42 avian influenza viruses, including 40 H5N8 viruses, 1 H5N2 virus, and 1 H9N2 virus, in central China. Our H5N8 viruses isolated in swan stopover sites and wintering grounds showed high nucleotide homologies in the whole genome, revealing a common evolutionary source. Phylogenetic analysis revealed that the H5 viruses of clade 2.3.4.4b prevalent in 2020 have further diverged into two sub-clades: b1 and b2. The phylogeographic analysis also showed that the viruses of sub-clade b2 most likely originated from poultry in Russia. Notably, whooper swans were found to be responsible for the introduction of sub-clade b2 viruses in central China; whooper and tundra swans play a role in viral spread in the Yellow River Basin and the Yangtze River Basin, respectively. Our findings highlight swans as an indicator species for transborder spreading and monitoring of the H5N8 virus.

Influenza A(H5N8) Viruses in Wild Ducks, China

The H7 subtype avian influenza viruses, such as H7N2, H7N3, H7N4, H7N7, and H7N9, were documented as being capable of infecting humans, and the H7 subtype low pathogenicity avian influenza viruses are capable of mutating into highly pathogenic avian influenza; therefore, they pose a serious threat to public health. Here, we investigated the evolutionary history, molecular characteristics, and pathogenicity of shorebird-origin influenza A(H7N4) viruses, showing a similar evolutionary trajectory with Jiangsu human A(H7N4) viruses in HA and NA genes.