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.

Circulation of avian influenza viruses in wild birds in Inner Niger Delta, Mali

“…The number of waterbird in the IND increases considerably with the arrival of Eurasian migrants, in particular migratory wildfowl (Figure 1F). 1 Moreover, it is worth noting that a large majority of the migratory wildfowl wintering in West Africa are ducks of the Anas genus, a group of species that consistently show the highest AIV prevalence among wild birds 2 , 9 . This massive arrival of Eurasian migrants is followed during the second half of their wintering period by the concentration of waterbirds on remnant water bodies because of decreasing water levels and the reduction in the surface of wetland habitat (Figure 1B,E).…”

“…Finally, the presence of immunologically naïve bird in the host community is considered an important driver of the transmission dynamics of AIV 9 , 11 . Most of the Afro‐tropical waterbirds species of the IND breed during the rainy season or during the early dry season 12 .…”

Detection of Influenza A viruses at migratory bird stopover sites in Michigan, USA

“…Numerous factors including species, age, sex, and densities of birds at the site affect detection rates of influenza in water and feces [2,5,51,52]. The sites with the greatest number of positive samples were the Muskegon Wastewater Management System, the Shiawassee National Wildlife Refuge, and Tawas Point State Park.…”

“…If further characterization of influenza positive sites were of interest, the RT-PCR results could be confirmed by virus isolation. Further characterization of subtypes may be warranted, particularly for highly pathogenic subtypes seen in North American migratory birds [5]. If positive samples/subtypes are recovered, more localized and intensive cloacal and/or pharyngeal sampling of hunter-killed or live-captured birds could also be added to provide additional information on infection rates and species involved.…”

“…The LPAI, which generally produce asymptomatic infections in wild birds, are far more numerous. These LPAI infect more than 105 species of birds from 26 families, but the Anseriformes (ducks, geese, swans) and Charadriiformes (shorebirds) are the primary biotic reservoirs [3–5]. Within some hemagglutinin subtypes, such as H5 and H7, mutation can increase the pathogenic potential [6,7] resulting in disease outbreaks.…”