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Abstract

Wild waterfowl form the main reservoir of influenza A viruses, from which transmission occurs directly or indirectly to various secondary hosts, including humans1. Direct avian-to-human transmission has been observed for viruses of subtypes A(H5N1), A(H7N2), A(H7N3), A(H7N7), A(H9N2) and A(H10N7) upon human exposure to poultry2,3,4,5,6,7, but a lack of sustained human-to-human transmission has prevented these viruses from causing new pandemics. Recently, avian A(H7N9) viruses were transmitted to humans, causing severe respiratory disease and deaths in China8. Because transmission via respiratory droplets and aerosols (hereafter referred to as airborne transmission) is the main route for efficient transmission between humans, it is important to gain an insight into airborne transmission of the A(H7N9) virus. Here we show that although the A/Anhui/1/2013 A(H7N9) virus harbours determinants associated with human adaptation and transmissibility between mammals, its airborne transmissibility in ferrets is limited, and it is intermediate between that of typical human and avian influenza viruses. Multiple A(H7N9) virus genetic variants were transmitted. Upon ferret passage, variants with higher avian receptor binding, higher pH of fusion, and lower thermostability were selected, potentially resulting in reduced transmissibility. This A(H7N9) virus outbreak highlights the need for increased understanding of the determinants of efficient airborne transmission of avian influenza viruses between mammals.

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Acknowledgements

We thank P. van Run, S. van der Vliet and A. Reiners for technical assistance. We thank the Chinese CDC for providing the A/Anhui/1/2013 isolate and R. Webby for the synthetic construct of HA. This work was financed through NIAID-NIH contract HHSN266200700010C and EU FP7 programs EMPERIE and ANTIGONE.

Author information

Author notes

    • Mathilde Richard
    •  & Eefje J. A. Schrauwen

    These authors contributed equally to this work.

Affiliations

  1. Department of Viroscience, Erasmus Medical Center, 3015GE Rotterdam, The Netherlands

    • Mathilde Richard
    • , Eefje J. A. Schrauwen
    • , Miranda de Graaf
    • , Theo M. Bestebroer
    • , Monique I. J. Spronken
    • , Sander van Boheemen
    • , Dennis de Meulder
    • , Pascal Lexmond
    • , Martin Linster
    • , Sander Herfst
    • , Judith M. van den Brand
    • , Thijs Kuiken
    • , Guus F. Rimmelzwaan
    • , Albert D. M. E. Osterhaus
    •  & Ron A. M. Fouchier
  2. Department of Zoology, University of Cambridge, CB2 3EJ Cambridge, UK

    • Derek J. Smith
    •  & David F. Burke

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Contributions

M.R., E.J.A.S. and R.A.M.F. designed the experiments. M.R., E.J.A.S., M.G., M.I.J.S., T.M.B., S.v.B., D.M., P.L., M.L. and S.H. performed the experiments, M.R., E.J.A.S., T.M.B., S.B., J.M.v.d.B. and D.F.B. analysed the data, and M.R., E.J.A.S., D.J.S., T.K., G.F.R., A.D.M.E.O. and R.A.M.F. wrote the manuscript. M.R. and E.J.A.S. contributed equally to the work.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Ron A. M. Fouchier.

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    Supplementary Information

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DOI

https://doi.org/10.1038/nature12476

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