Influenza A viruses are transmitted via the air from the nasal respiratory epithelium of ferrets.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
07 02 2020
07 02 2020
Historique:
received:
18
09
2019
accepted:
23
01
2020
entrez:
9
2
2020
pubmed:
9
2
2020
medline:
19
5
2020
Statut:
epublish
Résumé
Human influenza A viruses are known to be transmitted via the air from person to person. It is unknown from which anatomical site of the respiratory tract influenza A virus transmission occurs. Here, pairs of genetically tagged and untagged influenza A/H1N1, A/H3N2 and A/H5N1 viruses that are transmissible via the air are used to co-infect donor ferrets via the intranasal and intratracheal routes to cause an upper and lower respiratory tract infection, respectively. In all transmission cases, we observe that the viruses in the recipient ferrets are of the same genotype as the viruses inoculated intranasally, demonstrating that they are expelled from the upper respiratory tract of ferrets rather than from trachea or the lower airways. Moreover, influenza A viruses that are transmissible via the air preferentially infect ferret and human nasal respiratory epithelium. These results indicate that virus replication in the upper respiratory tract, the nasal respiratory epithelium in particular, of donors is a driver for transmission of influenza A viruses via the air.
Identifiants
pubmed: 32034144
doi: 10.1038/s41467-020-14626-0
pii: 10.1038/s41467-020-14626-0
pmc: PMC7005743
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
766Subventions
Organisme : NIAID NIH HHS
ID : HHSN272201400008C
Pays : United States
Organisme : NIAID NIH HHS
ID : HHSN272201400004C
Pays : United States
Références
Weber, T. P. & Stilianakis, N. I. Inactivation of influenza A viruses in the environment and modes of transmission: a critical review. J. Infect. 57, 361–373 (2008).
pubmed: 18848358
doi: 10.1016/j.jinf.2008.08.013
Tellier, R. Aerosol transmission of influenza A virus: a review of new studies. J. R. Soc. Interface 6, S783–S790 (2009).
pubmed: 19773292
pmcid: 2843947
doi: 10.1098/rsif.2009.0302.focus
Brankston, G., Gitterman, L., Hirji, Z., Lemieux, C. & Gardam, M. Transmission of influenza A in human beings. Lancet Infect. Dis. 7, 257–265 (2007).
pubmed: 17376383
doi: 10.1016/S1473-3099(07)70029-4
Yan, J. et al. Infectious virus in exhaled breath of symptomatic seasonal influenza cases from a college community. Proc. Natl Acad. Sci. USA 115, 1081–1086 (2018).
pubmed: 29348203
doi: 10.1073/pnas.1716561115
Fabian, P. et al. Influenza virus in human exhaled breath: an observational study. PLoS ONE 3, e2691 (2008).
pubmed: 18628983
pmcid: 2442192
doi: 10.1371/journal.pone.0002691
Lindsley, W. G. et al. Viable influenza A virus in airborne particles expelled during coughs versus exhalations. Influenza Other Respir. Viruses 10, 404–413 (2016).
pubmed: 26991074
pmcid: 4947941
doi: 10.1111/irv.12390
Milton, D. K., Fabian, M. P., Cowling, B. J., Grantham, M. L. & McDevitt, J. J. Influenza virus aerosols in human exhaled breath: particle size, culturability, and effect of surgical masks. PLoS Pathog. 9, e1003205 (2013).
pubmed: 23505369
pmcid: 3591312
doi: 10.1371/journal.ppat.1003205
Lindsley, W. G. et al. Measurements of airborne influenza virus in aerosol particles from human coughs. PLoS ONE 5, e15100 (2010).
pubmed: 21152051
pmcid: 2994911
doi: 10.1371/journal.pone.0015100
Lindsley, W. G. et al. Quantity and size distribution of cough-generated aerosol particles produced by influenza patients during and after illness. J. Occup. Environ. Hyg. 9, 443–449 (2012).
pubmed: 22651099
pmcid: 4676262
doi: 10.1080/15459624.2012.684582
Hatagishi, E. et al. Establishment and clinical applications of a portable system for capturing influenza viruses released through coughing. PLoS ONE 9, e103560 (2014).
pubmed: 25083787
pmcid: 4118893
doi: 10.1371/journal.pone.0103560
Lindsley, W. G. et al. Viable influenza A virus in airborne particles from human coughs. J. Occup. Environ. Hyg. 12, 107–113 (2015).
pubmed: 25523206
pmcid: 4734406
doi: 10.1080/15459624.2014.973113
Bischoff, W. E., Swett, K., Leng, I. & Peters, T. R. Exposure to influenza virus aerosols during routine patient care. J. Infect. Dis. 207, 1037–1046 (2013).
pubmed: 23372182
doi: 10.1093/infdis/jis773
pmcid: 23372182
Lindsley, W. G. et al. Distribution of airborne influenza virus and respiratory syncytial virus in an urgent care medical clinic. Clin. Infect. Dis. 50, 693–698 (2010).
pubmed: 20100093
pmcid: 20100093
Lednicky, J. A. & Loeb, J. C. Detection and isolation of airborne Influenza A H3N2 virus using a sioutas personal cascade impactor sampler. Influenza Res. Treat. 2013, 656825 (2013).
pubmed: 24224087
pmcid: 3810434
Blachere, F. M. et al. Measurement of airborne influenza virus in a hospital emergency department. Clin. Infect. Dis. 48, 438–440 (2009).
pubmed: 19133798
doi: 10.1086/596478
pmcid: 19133798
Andrewes, C. H. & Glover, R. E. Spread of Infection from the Respiratory Tract of the Ferret. I. Transmission of Influenza A Virus. Br. J. Exp. Pathol. 22, 91–97 (1941).
pmcid: 2065394
Van Hoeven, N. et al. Human HA and polymerase subunit PB2 proteins confer transmission of an avian influenza virus through the air. Proc. Natl Acad. Sci. USA 106, 3366–3371 (2009).
pubmed: 19211790
doi: 10.1073/pnas.0813172106
pmcid: 19211790
Munster, V. J. et al. Pathogenesis and transmission of swine-origin 2009 A(H1N1) influenza virus in ferrets. Science 325, 481–483 (2009).
pubmed: 19574348
pmcid: 4814155
doi: 10.1126/science.1177127
Lowen, A. C., Mubareka, S., Steel, J. & Palese, P. Influenza virus transmission is dependent on relative humidity and temperature. PLoS Pathog. 3, 1470–1476 (2007).
pubmed: 17953482
doi: 10.1371/journal.ppat.0030151
pmcid: 17953482
Lowen, A. C., Steel, J., Mubareka, S. & Palese, P. High temperature (30 degrees C) blocks aerosol but not contact transmission of influenza virus. J. Virol. 82, 5650–5652 (2008).
pubmed: 18367530
pmcid: 2395183
doi: 10.1128/JVI.00325-08
Linster, M. et al. Identification, characterization, and natural selection of mutations driving airborne transmission of A/H5N1 virus. Cell 157, 329–339 (2014).
pubmed: 24725402
pmcid: 4003409
doi: 10.1016/j.cell.2014.02.040
Imai, M. et al. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 486, 420–428 (2012).
pubmed: 22722205
pmcid: 3388103
doi: 10.1038/nature10831
Tumpey, T. M. et al. A two-amino acid change in the hemagglutinin of the 1918 influenza virus abolishes transmission. Science 315, 655–659 (2007).
pubmed: 17272724
doi: 10.1126/science.1136212
pmcid: 17272724
Pappas, C. et al. Receptor specificity and transmission of H2N2 subtype viruses isolated from the pandemic of 1957. PLoS ONE 5, e11158 (2010).
pubmed: 20574518
pmcid: 2888575
doi: 10.1371/journal.pone.0011158
Roberts, K. L., Shelton, H., Scull, M., Pickles, R. & Barclay, W. S. Lack of transmission of a human influenza virus with avian receptor specificity between ferrets is not due to decreased virus shedding but rather a lower infectivity in vivo. J. Gen. Virol. 92, 1822–1831 (2011).
pubmed: 21508186
doi: 10.1099/vir.0.031203-0
pmcid: 21508186
Stevens, J. et al. Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities. J. Mol. Biol. 355, 1143–1155 (2006).
pubmed: 16343533
doi: 10.1016/j.jmb.2005.11.002
pmcid: 16343533
van Riel, D. et al. Seasonal and pandemic human influenza viruses attach better to human upper respiratory tract epithelium than avian influenza viruses. Am. J. Pathol. 176, 1614–1618 (2010).
pubmed: 20167867
pmcid: 2843453
doi: 10.2353/ajpath.2010.090949
van Riel, D. et al. H5N1 virus attachment to lower respiratory tract. Science 312, 399 (2006).
pubmed: 16556800
doi: 10.1126/science.1125548
pmcid: 16556800
Shinya, K. et al. Avian flu: influenza virus receptors in the human airway. Nature 440, 435–436 (2006).
pubmed: 16554799
doi: 10.1038/440435a
pmcid: 16554799
Richard, M., Herfst, S., Tao, H., Jacobs, N. T. & Lowen, A. C. Influenza A virus reassortment is limited by anatomical compartmentalization following co-infection via distinct routes. J. Virol. 92, e02063-17 (2018).
Marshall, N., Priyamvada, L., Ende, Z., Steel, J. & Lowen, A. C. Influenza virus reassortment occurs with high frequency in the absence of segment mismatch. PLoS Pathog. 9, e1003421 (2013).
pubmed: 23785286
pmcid: 3681746
doi: 10.1371/journal.ppat.1003421
Herfst, S. et al. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336, 1534–1541 (2012).
pubmed: 22723413
pmcid: 4810786
doi: 10.1126/science.1213362
Tao, H., Li, L., White, M. C., Steel, J. & Lowen, A. C. Influenza A virus coinfection through transmission can support high levels of reassortment. J. Virol. 89, 8453–8461 (2015).
pubmed: 26041285
pmcid: 4524221
doi: 10.1128/JVI.01162-15
van den Brand, J. M. et al. Comparison of temporal and spatial dynamics of seasonal H3N2, pandemic H1N1 and highly pathogenic avian influenza H5N1 virus infections in ferrets. PLoS ONE 7, e42343 (2012).
pubmed: 22905124
pmcid: 22905124
doi: 10.1371/journal.pone.0042343
Burke, D. F. & Smith, D. J. A recommended numbering scheme for influenza A HA subtypes. PLoS ONE 9, e112302 (2014).
pubmed: 25391151
pmcid: 4229193
doi: 10.1371/journal.pone.0112302
Wells, W. F. On airborne infection: study II. Droplets and droplet nuclei. Am. J. Hyg. 20, 611–618 (1934).
WHO. Infection prevention and control of epidemic - and pandemic - prone acute respiratory infections in health care. 2018 (2014).
Kutter, J. S., Spronken, M. I., Fraaij, P. L., Fouchier, R. A. & Herfst, S. Transmission routes of respiratory viruses among humans. Curr. Opin. Virol. 28, 142–151 (2018).
pubmed: 29452994
doi: 10.1016/j.coviro.2018.01.001
Zhou, J. et al. Defining the sizes of airborne particles that mediate influenza transmission in ferrets. Proc. Natl Acad. Sci. USA 115, E2386–E2392 (2018).
pubmed: 29463703
doi: 10.1073/pnas.1716771115
pmcid: 29463703
Gustin, K. M. et al. Influenza virus aerosol exposure and analytical system for ferrets. Proc. Natl Acad. Sci. USA 108, 8432–8437 (2011).
pubmed: 21536880
doi: 10.1073/pnas.1100768108
pmcid: 21536880
Fabian, P., Brain, J., Houseman, E. A., Gern, J. & Milton, D. K. Origin of exhaled breath particles from healthy and human rhinovirus-infected subjects. J. Aerosol Med Pulm. Drug Deliv. 24, 137–147 (2011).
pubmed: 21361786
pmcid: 3123971
doi: 10.1089/jamp.2010.0815
Edwards, D. A. et al. Inhaling to mitigate exhaled bioaerosols. Proc. Natl Acad. Sci. USA 101, 17383–17388 (2004).
pubmed: 15583121
doi: 10.1073/pnas.0408159101
pmcid: 15583121
Johnson, G. R. et al. Modality of human expired aerosol size distributions. J. Aerosol Sci. 42, 839–851 (2011).
doi: 10.1016/j.jaerosci.2011.07.009
Johnson, G. R. & Morawska, L. The mechanism of breath aerosol formation. J. Aerosol Med Pulm. Drug Deliv. 22, 229–237 (2009).
pubmed: 19415984
doi: 10.1089/jamp.2008.0720
pmcid: 19415984
Almstrand, A. C. et al. Effect of airway opening on production of exhaled particles. J. Appl Physiol. 108, 584–588 (2010).
pubmed: 20056850
doi: 10.1152/japplphysiol.00873.2009
pmcid: 20056850
Herfst, S. et al. Drivers of airborne human-to-human pathogen transmission. Curr. Opin. Virol. 22, 22–29 (2017).
pubmed: 27918958
doi: 10.1016/j.coviro.2016.11.006
pmcid: 27918958
Knight, V. Viruses as agents of airborne contagion. Ann. N. Y. Acad. Sci. 353, 147–156 (1980).
pubmed: 6261640
doi: 10.1111/j.1749-6632.1980.tb18917.x
Richard, M. et al. Limited airborne transmission of H7N9 influenza A virus between ferrets. Nature 501, 560–563 (2013).
pubmed: 23925116
pmcid: 3819191
doi: 10.1038/nature12476
Lakdawala, S. S. et al. The soft palate is an important site of adaptation for transmissible influenza viruses. Nature 526, 122–125 (2015).
pubmed: 26416728
pmcid: 4592815
doi: 10.1038/nature15379
Zeng, H. et al. Tropism and Infectivity of a Seasonal A(H1N1) and a Highly Pathogenic Avian A(H5N1) Influenza Virus in Primary Differentiated Ferret Nasal Epithelial Cell Cultures. J. Virol. 93, e00080-19 (2019).
de Wit, E. et al. Efficient generation and growth of influenza virus A/PR/8/34 from eight cDNA fragments. Virus Res 103, 155–161 (2004).
pubmed: 15163504
doi: 10.1016/j.virusres.2004.02.028
pmcid: 15163504
House, W. U.S. Government Gain-of-Function Deliberative Process and Research Funding Pause on Selected Gain-of-Function Research Involving Influenza, MERS, and SARS Viruses (2014).
Reed, L. J. & Muench, H. A simple method of estimating fifty percent endpoints. Am. J. Hyg. 27, 493–497 (1938).
van Riel, D. et al. H5N1 Virus Attachment to Lower Respiratory Tract. Science. 312, 399–399 (2006).
pubmed: 16556800
doi: 10.1126/science.1125548
pmcid: 16556800