Abstract

The Caucasus, at the border of Europe and Asia, is important for migration and over-wintering of wild waterbirds. Three flyways, the Central Asian, East Africa-West Asia, and Mediterranean/Black Sea flyways, converge in the Caucasus region. Thus, the Caucasus region might act as a migratory bridge for influenza virus transmission when birds aggregate in high concentrations in the post-breeding, migrating and overwintering periods. Since August 2009, we have established a surveillance network for influenza viruses in wild birds, using five sample areas geographically spread throughout suitable habitats in both eastern and western Georgia. We took paired tracheal and cloacal swabs and fresh feces samples. We collected 8343 swabs from 76 species belonging to 17 families in 11 orders of birds, of which 84 were real-time RT-PCR positive for avian influenza virus (AIV). No highly pathogenic AIV (HPAIV) H5 or H7 viruses were detected. The overall AIV prevalence was 1.6%. We observed peak prevalence in large gulls during the autumn migration (5.3–9.8%), but peak prevalence in Black-headed Gulls in spring (4.2–13%). In ducks, we observed increased AIV prevalence during the autumn post-moult aggregations and migration stop-over period (6.3%) but at lower levels to those observed in other more northerly post-moult areas in Eurasia. We observed another prevalence peak in the overwintering period (0.14–5.9%). Serological and virological monitoring of a breeding colony of Armenian Gulls showed that adult birds were seropositive on arrival at the breeding colony, but juveniles remained serologically and virologically negative for AIV throughout their time on the breeding grounds, in contrast to gull AIV data from other geographic regions. We show that close phylogenetic relatives of viruses isolated in Georgia are sourced from a wide geographic area throughout Western and Central Eurasia, and from areas that are represented by multiple different flyways, likely linking different host sub-populations.

Highlights

  • Aquatic birds are the natural reservoir for all avian influenza A viruses (AIVs), and are subtyped according to 16 haemagglutinin (HA) subtypes and 9 neuraminidase (NA) subtypes [1,2]

  • Virus detection by M real-time RT-PCR (RRT-PCR) from wild birds tended to coincide with migration or overwintering, on the Black Sea coast and eastern sample sites

  • The upland sample sites did not yield an M RRT-PCR-positive swab from Charadriiformes during the study period, despite intensive sampling of the breeding gull population, a high density of naive juvenile gulls, and detection of avian influenza virus (AIV) in ducks, which were using the sample site during migration and post-breeding moult. To account for these observations, one hypothesis is that three factors might be important in the ecology of gulls and AIVs in Georgia and the interplay among these factors affects the risk of AIV infection

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Summary

Introduction

Aquatic birds are the natural reservoir for all avian influenza A viruses (AIVs), and are subtyped according to 16 haemagglutinin (HA) subtypes and 9 neuraminidase (NA) subtypes [1,2]. Most AIVs are of low pathogenicity and cause mild or subclinical infections in aquatic birds. Low pathogenic avian influenza (LPAI) viruses have been isolated from over 136 species of wild birds and are most commonly isolated from Anseriformes and Charadriiformes [3]. There remain substantial unanswered questions about the spatial, temporal and ecological role of the host populations in defining the genetic structure of AIVs. Since the emergence and westward spread of HPAI H5N1 from SE-Asia, one of the outstanding questions is the role wild birds, long distance migrants, might play in the dissemination of AIV from SE-Asia to other geographic regions [4,5].

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