Concentrations and size distributions of airborne influenza A viruses measured indoors at a health centre, a day-care centre and on aeroplanes
The relative importance of the aerosol transmission route for influenza remains contentious. To determine the potential for influenza to spread via the aerosol route, we measured the size distribution of airborne influenza A viruses. We collected size-segregated aerosol samples during the 2009–2010 flu season in a health centre, a day-care facility and onboard aeroplanes. Filter extracts were analysed using quantitative reverse transcriptase polymerase chain reaction. Half of the 16 samples were positive, and their total virus concentrations ranged from 5800 to 37 000 genome copies m. On average, 64 per cent of the viral genome copies were associated with fine particles smaller than 2.5 µm, which can remain suspended for hours. Modelling of virus concentrations indoors suggested a source strength of 1.6 ± 1.2 × 10 genome copies m air h and a deposition flux onto surfaces of 13 ± 7 genome copies m h by Brownian motion. Over 1 hour, the inhalation dose was estimated to be 30 ± 18 median tissue culture infectious dose (TCID50), adequate to induce infection. These results provide quantitative support for the idea that the aerosol route could be an important mode of influenza transmission.
Aligned with A/PR/8/34 (H1N1) segment 7 (M gene).
Recovery efficiency significantly less than 100%.
Not available owing to a logging error.
No detectable influenza A virus genome.
This material is based in part upon work supported by the National Science Foundation under Grant Number CBET-0547107. We thank A. Pruden for sharing laboratory space and equipment, J. Petruska for much assistance, K. Charoensiri of the university health centre and a day-care centre in Blacksburg for allowing sampling in their facilities.
- 1. Tellier R. 2009. Aerosol transmission of influenza A virus: a review of new studies. J. R. Soc. Interface6, S783–S79010.1098/rsif.2009.0302.focus () ] [[PubMed]
- 2. Brankston G., Gitterman L., Hirji Z., Lemieux C., Gardam M. 2007. Transmission of influenza A in human beings. Lancet Infect. Dis.7, 257–26510.1016/S1473-3099(07)70029-4 ()  [[PubMed]
- 3. Tellier R. 2006. Review of aerosol transmission of influenza A virus. Emerg. Infect. Dis.12, 1657–1662
- 4. Fabian P., Mcdevitt J. J., Lee W.-M., Houseman E. A., Milton D. K. 2009. An optimized method to detect influenza virus and human rhinovirus from exhaled breath and the airborne environment. J. Environ. Monit.11, 314–31710.1039/b813520g () ] [[PubMed]
- 5. Fabian P., Mcdevitt J. J., Houseman E. A., Milton D. K. 2009. Airborne influenza virus detection with four aerosol samplers using molecular and infectivity assays: considerations for a new infectious virus aerosol sampler. Indoor Air19, 433–44110.1111/j.1600-0668.2009.00609.x () ] [[PubMed]
- 6. Chen P.-S., et al. 2009. Quantification of airborne influenza and avian influenza virus in a wet poultry market using a filter/real-time qPCR method. Aerosol Sci. Technol.43, 290–29710.1080/02786820802621232 () [[PubMed]
- 7. Blachere F. M., et al. 2009. Measurement of airborne influenza virus in a hospital emergency department. Clin. Infect. Dis.48, 438–44010.1086/596478 ()  [[PubMed]
- 8. Lindsley W. G., et al. 2010. Distribution of airborne influenza virus and respiratory syncytial virus in an urgent care medical clinic. Clin. Infect. Dis.50, 693–69810.1086/650457 ()  [[PubMed]
- 9. Boone S. A., Gerba C. P. 2005. The occurrence of influenza A virus on household and day care center fomites. J. Infect.51, 103–10910.1016/j.jinf.2004.09.011 ()  [[PubMed]
- 10. Wagner B., Coburn B., Blower S. 2009. Calculating the potential for within-flight transmission of influenza A (H1N1). BMC Med.7, 81.10.1186/1741-7015-7-81 () ] [[PubMed]
- 11. Moser M. R., Bender T. R., Margolis H. S., Noble G. R., Kendal A. P., Ritter D. G. 1979. An outbreak of influenza aboard a commercial airliner. Am. J. Epidemiol.110, 1–6 [[PubMed]
- 12. Fabian P., Mcdevitt J. J., Dehaan W. H., Fung R. O. P., Cowling B. J., Chan K. H., Leung G. M., Milton D. K. 2008. Influenza virus in human exhaled breath: an observational study. PLoS ONE3, e2691.10.1371/journal.pone.0002691 () ] [[PubMed]
- 13. Lee W.-M., Grindle K., Pappas T., Marshall D. J., Moser M. J., Beaty E. L., Shult P. A., Prudent J. R., Gern J. E. 2007. High-throughput, sensitive, and accurate multiplex PCR-microsphere flow cytometry system for large-scale comprehensive detection of respiratory viruses. J. Clin. Microbiol.45, 2626–263410.1128/jcm.02501-06 () ] [[PubMed]
- 14. Ward C. L., Dempsey M. H., Ring C. J. A., Kempson R. E., Zhang L., Gor D., Snowden B. W., Tisdale M. 2004. Design and performance testing of quantitative real time PCR assays for influenza A and B viral load measurement. J. Clin. Virol.29, 179–18810.1016/S1386-6532(03)00122-7 ()  [[PubMed]
- 15. van Elden L. J. R., Nijhuis M., Schipper P., Schuurman R., van Loon A. M. 2001. Simultaneous detection of influenza viruses A and B using real-time quantitative PCR. J. Clin. Microbiol.39, 196–20010.1128/jcm.39.1.196-200.2001 () ] [[PubMed]
- 16. Munster V. J., et al. 2009. Practical considerations for high-throughput influenza A virus surveillance studies of wild birds by use of molecular diagnostic tests. J. Clin. Microbiol.47, 666–67310.1128/jcm.01625-08 () ] [[PubMed]
- 17. van der Vries E., et al. 2010. Evaluation of a rapid molecular algorithm for detection of pandemic influenza A (H1N1) 2009 virus and screening for a key oseltamivir resistance (H275Y) substitution in neuraminidase. J. Clin. Virol.47, 34–3710.1016/j.jcv.2009.09.030 ()  [[PubMed]
- 18. Yang J.-R., Lo J., Ho Y.-L., Wu H.-S., Liu T. 2011. Pandemic H1N1 and seasonal H3N2 influenza infection in the human population show different distributions of viral loads, which substantially affect the performance of rapid influenza tests. Virus Res.155, 163–16710.1016/j.virusres.2010.09.015 ()  [[PubMed]
- 19. Tompkins J. A., White J. A., Bozer Y. A., Tanchoco J. M. A. 2010. Facilities planning. New York, NY: John Wiley & Sons, Inc [PubMed]
- 20. Mangili A., Gendreau M. A. 2005. Transmission of infectious diseases during commercial air travel. Lancet365, 989–99610.1016/S0140-6736(05)71089-8 ()  [[PubMed]
- 21. Hinds W. C. 1999. Aerosol technology, p. 49 New York, NY: Wiley [PubMed]
- 22. Poon L. L., Chan K. H., Smith G. J., Leung C. S., Guan Y., Yuen K. Y., Peiris J. S. 2009. Molecular detection of a novel human influenza (H1N1) of pandemic potential by conventional and real-time quantitative RT–PCR assays. Clin. Chem.55, 1555–155810.1373/clinchem.2009.130229 ()  [[PubMed]
- 23. ATCC 2009 8/20/2009 Converting TCID to plaque forming units (PFU). See (retrieved 1 July 2010)[PubMed]
- 24. Yang S., Lee G. W. M., Chen C.-M., Wu C.-C., Yu K.-P. 2007. The size and concentration of droplets generated in human subjects. J. Aerosol. Med.20, 484–49410.1089/jam.2007.0610 ()  [[PubMed]
- 25. US EPA 1994 Methods for derivation of inhalation reference concentrations and application of inhalation dosimetry. EPA/600/8-90/066F, US Environmental Protection Agency, Office of Research and Development, Office of Health and Environmental Assessment, Washington, DC [PubMed]
- 26. Alford R. H., Kasel J. A., Gerone P. J., Knight V. 1966. Human influenza resulting from aerosol inhalation. Proc. Soc. Exp. Biol. Med.122, 800–804 [[PubMed]
- 27. Oberdorster G. 1993. Lung dosimetry—pulmonary clearance of inhaled particles. Aerosol Sci. Technol.18, 279–28910.1080/02786829308959605 () [[PubMed]
- 28. US CDC 2010 Seasonal influenza (flu). Past weekly surveillance reports See (retrieved 23 November 2010) [PubMed]
- 29. Bean B., Moore B. M., Sterner B., Peterson L. R., Gerding D. N., Balfour H. H., Jr 1982. Survival of influenza viruses on environmental surfaces. J. Infect. Dis.146, 47–51 [[PubMed]