The epidemiological success of pandemic and epidemic influenza A viruses relies on the ability to transmit efficiently from person-to-person via respiratory droplets. Respiratory droplet (RD) transmission of influenza viruses requires efficient replication and release of infectious influenza particles into the air. The 2009 pandemic H1N1 (pH1N1) virus originated by reassortment of a North American triple reassortant swine (TRS) virus with a Eurasian swine virus that contributed the neuraminidase (NA) and M gene segments. Both the TRS and Eurasian swine viruses caused sporadic infections in humans, but failed to spread from person-to-person, unlike the pH1N1 virus. We evaluated the pH1N1 and its precursor viruses in a ferret model to determine the contribution of different viral gene segments on the release of influenza virus particles into the air and on the transmissibility of the pH1N1 virus. We found that the Eurasian-origin gene segments contributed to efficient RD transmission of the pH1N1 virus likely by modulating the release of influenza viral RNA-containing particles into the air. All viruses replicated well in the upper respiratory tract of infected ferrets, suggesting that factors other than viral replication are important for the release of influenza virus particles and transmission. Our studies demonstrate that the release of influenza viral RNA-containing particles into the air correlates with increased NA activity. Additionally, the pleomorphic phenotype of the pH1N1 virus is dependent upon the Eurasian-origin gene segments, suggesting a link between transmission and virus morphology. We have demonstrated that the viruses are released into exhaled air to varying degrees and a constellation of genes influences the transmissibility of the pH1N1 virus. Author Summary Influenza A viruses spread rapidly from person-to-person via respiratory droplets (RDs). In this study we used a ferret model to explore viral functions involved in RD transmission of influenza viruses. The 2009 pandemic H1N1 (pH1N1) virus originated by reassortment of a North American triple reassortant swine (TRS) virus with a Eurasian swine virus. Both TRS and Eurasian swine viruses had previously caused sporadic infections in humans, but failed to spread from person-to-person, unlike the pH1N1 virus. We evaluated the release of influenza virus-containing aerosols and the transmissibility of the pH1N1, TRS, and Eurasian viruses in ferrets and found that the Eurasian-origin gene segments contributed to efficient RD transmission of the pH1N1 virus by modulating the release of influenza viral RNA-containing particles into the air. The increased release of viral RNA-containing particles correlated with increased viral neuraminidase activity and production of filamentous viral particles. These observations enhance what we currently know about the viral requirements for influenza virus RD transmission and have implications for assessing the potential of novel influenza viruses to spread.
Eurasian-Origin Gene Segments Contribute to the Transmissibility, Aerosol Release, and Morphology of the 2009 Pandemic H1N1 Influenza Virus
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