Prior infection with IBDV prolonged the shedding of a mallard H3N8 influenza A virus (IAV) challenge from the oropharyngeal cavity of some chickens and increased the number of amino acid substitutions in the IAV samples

Abstract

Infectious bursal disease virus (IBDV) is endemic worldwide and causes immunosuppression in chickens. We hypothesized that a previous history of IBDV in chickens would render them more susceptible to infection by influenza A viruses (IAVs) from aquatic waterfowl reservoirs. To model this, we inoculated 14 day old specific pathogen free (SPF) chickens with a low pathogenicity avian influenza (LPAI) virus strain from a mallard (A/Mallard/Alberta/156/01 (H3N8)) and compared replication and shedding between immunocompetent chickens and chickens that had immune dysregulation due to a prior IBDV infection with strain F52/70 (genogroup A1B1) at 2 days of age. The mallard IAV strain replicated in the upper respiratory tract of the chickens, and virus was shed from the oropharyngeal cavity, but there was no shedding from the cloaca, and no transmission to sentinel chickens. Replication of the mallard IAV in the chicken host was associated with amino acid substitutions in the polymerase complex and HA. IBDV infection increased the average fold change of IAV replication in the trachea of chickens, prolonged the shedding of infectious IAV from 5 to 6 days in some chickens, increased the number of amino acid substitutions detected in the IAV population from 13 to 30, and significantly increased the number of mutations per IAV sample from 2.50 (SD +/- 1.83) in the Mock/IAV group to 4.75 (SD +/- 1.81) in the IBDV/IAV group (p < 0.01). Taken together, IBDV infection prolonged the shedding of the mallard IAV in some chickens and changed IAV intra-host evolution. Author summarySpillover of IAVs from wild aquatic waterfowl into poultry populations occur frequently, which increases the risk of human infection as people have more contact with poultry than wild birds. Poultry flocks may have other co-morbidities that may influence the spread of IAV. Our data demonstrate that prior IBDV infection increased the average fold change of a mallard H3N8 LPAI virus in the trachea of inoculated chickens, prolonged the shedding of infectious IAV from the oropharyngeal cavity, and significantly increased the average number of amino acid substitutions per IAV sample. We hypothesize that IBDV infection could increase the amount of IAV shed into the environment and broaden the diversity of the IAV population shed. We conclude that controlling the spread of wild aquatic waterfowl strains of IAV in chickens should involve a holistic approach, including the control of co-morbidities and immunosuppressive diseases that could exacerbate their spread.