Spatial, Temporal, and Species Variation in Prevalence of Influenza A Viruses in Wild Migratory Birds

Abstract

Although extensive data exist on avian influenza in wild birds in North America, limited information is available from elsewhere, including Europe. Here, molecular diagnostic tools were employed for high-throughput surveillance of migratory birds, as an alternative to classical labor-intensive methods of virus isolation in eggs. This study included 36,809 samples from 323 bird species belonging to 18 orders, of which only 25 species of three orders were positive for influenza A virus. Information on species, locations, and timing is provided for all samples tested. Seven previously unknown host species for avian influenza virus were identified: barnacle goose, bean goose, brent goose, pink-footed goose, bewick's swan, common gull, and guillemot. Dabbling ducks were more frequently infected than other ducks and Anseriformes; this distinction was probably related to bird behavior rather than population sizes. Waders did not appear to play a role in the epidemiology of avian influenza in Europe, in contrast to the Americas. The high virus prevalence in ducks in Europe in spring as compared with North America could explain the differences in virus–host ecology between these continents. Most influenza A virus subtypes were detected in ducks, but H13 and H16 subtypes were detected primarily in gulls. Viruses of subtype H6 were more promiscuous in host range than other subtypes. Temporal and spatial variation in influenza virus prevalence in wild birds was observed, with influenza A virus prevalence varying by sampling location; this is probably related to migration patterns from northeast to southwest and a higher prevalence farther north along the flyways. We discuss the ecology and epidemiology of avian influenza A virus in wild birds in relation to host ecology and compare our results with published studies. These data are useful for designing new surveillance programs and are particularly relevant due to increased interest in avian influenza in wild birds.

Author Summary

Significant gaps in our knowledge of the ecology of avian influenza in wild migratory birds have become apparent during recent outbreaks of H5N1 highly pathogenic avian influenza, in particular in relation to the risk of virus spread by wild birds. An eight-year surveillance study, which included more than 36,000 wild birds tested for low pathogenic avian influenza, provides new information on host species, prevalence, and temporal and geographical variation of avian influenza in wild migratory birds in Europe. Dabbling ducks harbored nearly all known influenza virus subtypes, with the exception of H13 and H16, which were found primarily in gulls. In contrast to American studies, waders did not play a role in the epidemiology of avian influenza in Europe. This study provides important information on the ecology and epidemiology of avian influenza A virus and could assist in the design of new surveillance studies for high and low pathogenic avian influenza in wild birds.