Highly Pathogenic Avian Influenza Virus Infection of Mallards with Homo- and Heterosubtypic Immunity Induced by Low Pathogenic Avian Influenza Viruses

Abstract

The potential role of wild birds as carriers of highly pathogenic avian influenza virus (HPAIV) subtype H5N1 is still a matter of debate. Consecutive or simultaneous infections with different subtypes of influenza viruses of low pathogenicity (LPAIV) are very common in wild duck populations. To better understand the epidemiology and pathogenesis of HPAIV H5N1 infections in natural ecosystems, we investigated the influence of prior infection of mallards with homo- (H5N2) and heterosubtypic (H4N6) LPAIV on exposure to HPAIV H5N1. In mallards with homosubtypic immunity induced by LPAIV infection, clinical disease was absent and shedding of HPAIV from respiratory and intestinal tracts was grossly reduced compared to the heterosubtypic and control groups (mean GEC/100 µl at 3 dpi: 3.0×102 vs. 2.3×104 vs. 8.7×104; p<0.05). Heterosubtypic immunity induced by an H4N6 infection mediated a similar but less pronounced effect. We conclude that the epidemiology of HPAIV H5N1 in mallards and probably other aquatic wild bird species is massively influenced by interfering immunity induced by prior homo- and heterosubtypic LPAIV infections.

Identifying crucial gaps in our knowledge of the life-history of avian influenza viruses—an Australian perspective

“…Ots et al 1998;Forsman et al 2008). In particular, prior exposure to an HA-homologous virus of LPAI phenotype has been shown to be sufficient to reduce clinical symptoms and viral shedding (Fereidouni et al 2009). Even prior infection with an HA-heterologous virus may result in partially reduced symptoms and viral shedding (Fereidouni et al 2009;Jourdain et al 2010).…”

“…from Asia to Australia), the phenomenon of partial crossprotective immunity increases the potential for migrants to disperse HPAI over large distances. To date, most infection experiments have been conducted with seronegative birds; the studies by Fereidouni et al (2009) andJourdain et al (2010) highlight the importance of including infection history in the design of experiments.…”

“…HPAI viruses, however, are able to replicate throughout the bird in clinical cases of the disease, causing systemic organ and tissue damage (Alexander 2000). Under laboratory conditions, birds infected with LPAI will shed virus for between 1 and 2 weeks (Homme and Easterday 1970;Kida et al 1980), though the period of viral shedding appears to be significantly shorter when the individual has previously experienced an AIV (Kida et al 1980;Fereidouni et al 2009;Latorre-Margalef et al 2009;Jourdain et al 2010). The transmission of viruses between avian hosts is not well understood but there are various potential routes.…”

“…Unlike the surface proteins, these internal proteins have a highly conserved genetic sequence, which allows the detection of antibodies from birds infected with any influenza A virus (Suarez and Schultz-Cherry 2000). Antibody titre has been seen to increase rapidly as a result of re-infections, and is thought to be responsible for the decreased shedding period seen in re-infected individuals (Kida et al 1980;Fereidouni et al 2009Fereidouni et al , 2010Jourdain et al 2010). However, there is very little knowledge on how long these antibodies persist, with current estimates somewhere between a few months to a year (Nishiura et al 2009;Fereidouni et al 2010;Hoye et al 2010a).…”

Getting a free ride on poultry farms: how highly pathogenic avian influenza may persist in spite of its virulence

“…Similarly, Kalthoff et al (2008) showed that naïve mute swans died shortly after infection with HPAI H5N1 but those with previous exposure to LPAI viruses were able to survive without apparent symptoms. Fereidouni et al (2009) also showed that prior infection with low pathogenic H5N2 provided homosubtype immunity against HPAI H5N1 in waterfowl. These studies imply that previous infection with LPAI virus effectively reduces susceptibility of the host to infection and decreases transmission of HPAI virus, affecting the course of HPAI not only clinically, but also epidemiologically.…”