Ecology and evolution of influenza viruses in poultry in Taiwan

Abstract

Taiwan is an important stopover site on a migratory flyway and an island containing high density of poultry populations, particularly of chickens and ducks. It has recently suffered from repeated avian influenza outbreaks caused by viruses of the Mexico/94-like H5N2 (Mex-like H5N2) and clade 2.3.4.4 of the Asian H5Nx highly pathogenic avian influenza lineages (2.3.4.4 H5Nx HP AIVs), resulting in considerable losses to the economy and livelihoods of farmers. Taiwan also reported the world’s first known H6N1 AIV infections in a human and a canine, from a lineage that is enzootic in chickens in this region (TW H6N1).

The increased influenza activity in Taiwan might be attributable to the development of contemporary agricultural systems which possibly promotes encroachment into wild bird habitats, increases contacts between wild and domestic birds and results in the emergence of novel AIVs.

To examine this, a collaborative surveillance of AIVs at a live poultry market in Taipei was implemented from December 2012 to May 2014. Totals of 141 and 586 AIVs were isolated from 14,602 chicken and 6,585 duck swabs. Genomic sequences of these viruses and the archived viruses isolated during 2005-11 from the same market, and 34 goose samples collected in 2015 at farms, were obtained for evolutionary analysis.

All chicken isolates in this study belonged to either TW H6N1 or Mex-like H5N2 lineages except for four H4 Eurasian gene pool-like (EA-GP) viruses. Different subtypes of AIVs (H2-H7 and H10-H11) were detected in domestic ducks. A novel H5N2 low pathogenic AIV lineage (TW H5N2) with exceptionally high prevalence, accounting for 47.8% of all duck isolates, was recognised. In recent years the TW H6N1 and Mex-like H5N2 viruses were also frequently detected from ducks, reflecting an increasing genetic diversity of AIVs in this host species.

In contrast to the viruses from wild waterfowl, TW H5N2 viruses were found to become persistent in domestic ducks with elevated evolutionary rates in genes, a partially fixed gene constellation and enhanced binding to both avian- and human-type receptors. Molecular analysis revealed the signatures in multiple proteins that may favour the mammalian infections in TW H6N1, Mex-like H5N2, 2.3.4.4 H5Nx and TW H5N2 virus lineages, suggesting the zoonotic potential of these viruses.

Here, my study has demonstrated that the evolution of poultry AIVs in the contemporary farming systems in Taiwan may increase viral flow between domestic ducks and other host species, such as wild waterfowl, chickens and mammals, which provides renewal evidence that domestic ducks played a bridging role between natural reservoirs and aberrant hosts in influenza ecosystem. Continuous and strengthened surveillance of AIVs in poultry, particularly in domestic ducks, is necessary to prevent the future emergence of novel AIVs in Taiwan.