Homo- and Heterosubtypic Low Pathogenic Avian Influenza Exposure on H5N1 Highly Pathogenic Avian Influenza Virus Infection in Wood Ducks (Aix sponsa)

David E. Stallknecht,David E. Swayne,Todd Davis,Elizabeth W. Howerth,Justin D. Brown,Taiana P. Costa

doi:10.1371/journal.pone.0015987

Abstract

Wild birds in the Orders Anseriformes and Charadriiformes are the natural reservoirs for avian influenza (AI) viruses. Although they are often infected with multiple AI viruses, the significance and extent of acquired immunity in these populations is not understood. Pre-existing immunity to AI virus has been shown to modulate the outcome of a highly pathogenic avian influenza (HPAI) virus infection in multiple domestic avian species, but few studies have addressed this effect in wild birds. In this study, the effect of pre-exposure to homosubtypic (homologous hemagglutinin) and heterosubtypic (heterologous hemagglutinin) low pathogenic avian influenza (LPAI) viruses on the outcome of a H5N1 HPAI virus infection in wood ducks (Aix sponsa) was evaluated. Pre-exposure of wood ducks to different LPAI viruses did not prevent infection with H5N1 HPAI virus, but did increase survival associated with H5N1 HPAI virus infection. The magnitude of this effect on the outcome of the H5N1 HPAI virus infection varied between different LPAI viruses, and was associated both with efficiency of LPAI viral replication in wood ducks and the development of a detectable humoral immune response. These observations suggest that in naturally occurring outbreaks of H5N1 HPAI, birds with pre-existing immunity to homologous hemagglutinin or neuraminidase subtypes of AI virus may either survive H5N1 HPAI virus infection or live longer than naïve birds and, consequently, could pose a greater risk for contributing to viral transmission and dissemination. The mechanisms responsible for this protection and/or the duration of this immunity remain unknown. The results of this study are important for surveillance efforts and help clarify epidemiological data from outbreaks of H5N1 HPAI virus in wild bird populations.

Highlights

Wild birds, especially those in the Orders Anseriformes and Charadriiformes, are the natural reservoirs for all known hemagglutinin (HA) (H1–H16) and neuraminidase (NA) (N1–N9) subtypes of avian influenza (AI) viruses [1,2,3,4,5]
To better understand the epidemiology of H5N1 highly pathogenic avian influenza (HPAI) virus infections in wild bird populations, we experimentally investigated the effects that pre-exposure with homosubtypic (H5N1 or H5N2) or heterosubtypic (H1N1) low pathogenic avian influenza (LPAI) viruses had on the outcome of a Eurasian H5N1 HPAI virus challenge in wood ducks (Aix sponsa)
Both of these ducks were seronegative at 21 LPAIV-dpe on the H5 hemagglutination inhibition (HI) test (Table 2), antibodies were detected in one duck with the blocking enzymelinked immunosorbent assay (bELISA)

Summary

Introduction

Especially those in the Orders Anseriformes and Charadriiformes, are the natural reservoirs for all known hemagglutinin (HA) (H1–H16) and neuraminidase (NA) (N1–N9) subtypes of avian influenza (AI) viruses [1,2,3,4,5]. Pre-exposure to LPAI viruses has been shown to induce partial protection against H5N1 HPAI virus infection in Canada geese (Branta canadensis) [14,15], mute swans (Cygnus olor) [16], mallards (Anas platyrhynchos) [17], and chickens [18,19,20] as evidenced by reduced morbidity, mortality, susceptibility, and/or viral shedding Such protective immunity may be one possible explanation for unexpected field observations during natural outbreaks of H5N1 HPAI virus, including lower than anticipated morbidity in poultry in Hong Kong [21] and wild birds in Germany despite the presence of several hundred thousand susceptible birds in the affected area [22]. The mechanisms of this protective effect, are still poorly defined

Methods

Results

Conclusion