Influenza is one of the most contagious and rapidly spreading infectious diseases and an important global cause of hospital admissions and mortality. There are some amounts of the virus in the air constantly. These amounts is generally not enough to cause disease in people, due to infection prevention by healthy immune systems. However, at a higher concentration of the airborne virus, the risk of human infection increases dramatically. Early detection of the threshold virus concentration is essential for prevention of the spread of influenza infection. This review discusses different approaches for measuring the amount of influenza A virus particles in the air and assessing their infectiousness. Here we also discuss the data describing the relationship between the influenza virus subtypes and virus air transmission, and distribution of viral particles in aerosol drops of different sizes. 1. Introduction Influenza is one of the most contagious and rapidly spreading infectious diseases and an important global cause of hospital admissions and mortality [1]. Influenza virus concentration [2, 3], air circulation time, air temperature, and humidity [4] play an important role in overcoming the epidemic threshold. Influenza virus particles are constantly circulating in the air (airborne) in different forms (within dust particles or aerosol droplets) [5, 6]. There are some amounts of the virus in the air constantly. These amounts are insufficient to cause disease in people (the immune system of healthy humans prevents infection). However, at a higher concentration of the airborne virus, the risk of human infection increases dramatically. Early detection of the threshold virus concentration is essential for prevention of the spread of influenza infection. Furthermore, manufacturers are going to integrate detectors of virus particle numbers into hospital air control system equipment. This review discusses different approaches for measuring the amount of influenza A virus particles in the air and assessing their infectiousness. One of the fundamental works focused on the definition of the harmful concentration of the influenza A virus in the air is a paper by Alford, with coworkers [7]. It is cited in many recent reports [8–10]. A study was initiated to determine the minimum infectious aerosol dose and the resulting patterns of infection and illness. Observations made during experimental infections with human volunteers are particularly interesting and relevant. In studies conducted by Alford and colleagues [7], volunteers were exposed to carefully titrated
References
[1]
T. Vega, J. E. Lozano, T. Meerhoff et al., “Influenza surveillance in Europe: establishing epidemic thresholds by the Moving Epidemic Method,” Influenza and other Respiratory Viruses, vol. 7, no. 4, pp. 546–558, 2013.
[2]
G. Cao, F. M. Blachere, W. G. Lindsley, J. D. Noti, and D. H. Beezhold, “Development of a methodology to detect viable airborne virus using personal aerosol samplers,” EPA/600/R-10/127, Environmental Protection Agency, Washington, DC, USA, 2010.
[3]
I. Marois, A. Cloutier, é. Garneau, and M. V. Richter, “Initial infectious dose dictates the innate, adaptive, and memory responses to influenza in the respiratory tract,” Journal of Leukocyte Biology, vol. 92, no. 1, pp. 107–121, 2012.
[4]
J. McDevitt, S. Rudnick, M. First, and J. Spengler, “Role of absolute humidity in the inactivation of influenza viruses on stainless steel surfaces at elevated temperatures,” Applied and Environmental Microbiology, vol. 76, no. 12, pp. 3943–3947, 2010.
[5]
C. B. Hall, “The spread of influenza and other respiratory viruses: complexities and conjectures,” Clinical Infectious Diseases, vol. 45, no. 3, pp. 353–359, 2007.
[6]
R. Tellier, “Aerosol transmission of influenza A virus: a review of new studies,” Journal of the Royal Society Interface, vol. 6, supplement 6, pp. S783–S790, 2009.
[7]
R. H. Alford, J. A. Kasel, P. J. Gerone, and V. Knight, “Human influenza resulting from aerosol inhalation.,” Proceedings of the Society for Experimental Biology and Medicine, vol. 122, no. 3, pp. 800–804, 1966.
[8]
M. P. Atkinson and L. M. Wein, “Quantifying the routes of transmission for pandemic influenza,” Bulletin of Mathematical Biology, vol. 70, no. 3, pp. 820–867, 2008.
[9]
P. Fabian, J. J. McDevitt, W. H. DeHaan et al., “Influenza virus in human exhaled breath: an observational study,” PLoS ONE, vol. 3, no. 7, Article ID e2691, 2008.
[10]
W. Yang, S. Elankumaran, and L. C. Marr, “Concentrations and size distributions of airborne influenza A viruses measured indoors at a health centre, a day-care centre and on aeroplanes,” Journal of the Royal Society Interface, vol. 8, no. 61, pp. 1176–1184, 2011.
[11]
C. L. Ward, M. H. Dempsey, C. J. A. Ring et al., “Design and performance testing of quantitative real time PCR assays for influenza A and B viral load measurement,” Journal of Clinical Virology, vol. 29, no. 3, pp. 179–188, 2004.
[12]
L. J. R. Van Elden, M. Nijhuis, P. Schipper, R. Schuurman, and A. M. van Loon, “Simultaneous detection of influenza viruses A and B using real-time quantitative PCR,” Journal of Clinical Microbiology, vol. 39, no. 1, pp. 196–200, 2001.
[13]
W. G. Lindsley, F. M. Blachere, K. A. Davis et al., “Distribution of airborne influenza virus and respiratory syncytial virus in an urgent care medical clinic,” Clinical Infectious Diseases, vol. 50, no. 5, pp. 693–698, 2010.
[14]
W. G. Lindsley, F. M. Blachere, R. E. Thewlis et al., “Measurements of airborne influenza virus in aerosol particles from human coughs,” PLoS ONE, vol. 5, no. 11, Article ID e15100, 2010.
[15]
K. W. Moon, E. H. Huh, and H. C. Jeong, “Seasonal evaluation of bioaerosols from indoor air of residential apartments within the metropolitan area in South Korea,” Environmental Monitoring and Assessment, vol. 186, no. 4, pp. 2111–2120, 2014.
[16]
B. Schweiger, I. Zadow, R. Heckler, H. Timm, and G. Pauli, “Application of a fluorogenic PCR assay for typing and subtyping of influenza viruses in respiratory samples,” Journal of Clinical Microbiology, vol. 38, no. 4, pp. 1552–1558, 2000.
[17]
R. A. M. Fouchier, T. M. Bestebroer, S. Herfst, L. Van der Kemp, G. F. Rimmelzwaan, and A. D. M. E. Osterhaus, “Detection of influenza a viruses from different species by PCR amplification of conserved sequences in the matrix gene,” Journal of Clinical Microbiology, vol. 38, no. 11, pp. 4096–4101, 2000.
[18]
S. K. Poddar, “Detection of type and subtypes of influenza virus by hybrid formation of FRET probe with amplified target DNA and melting temperature analysis,” Journal of Virological Methods, vol. 108, no. 2, pp. 157–163, 2003.
[19]
B. Stone, J. Burrows, S. Schepetiuk et al., “Rapid detection and simultaneous subtype differentiation of influenza A viruses by real time PCR,” Journal of Virological Methods, vol. 117, no. 2, pp. 103–112, 2004.
[20]
C. Tseng, L. Chang, and C. Li, “Detection of airborne viruses in a pediatrics department measured using real-time qPCR coupled to an air-sampling filter method,” Journal of Environmental Health, vol. 73, no. 4, pp. 22–28, 2010.
[21]
R. Tellier, “Review of aerosol transmission of influenza A virus,” Emerging Infectious Diseases, vol. 12, no. 11, pp. 1657–1662, 2006.
[22]
G. Brankston, L. Gitterman, Z. Hirji, C. Lemieux, and M. Gardam, “Transmission of influenza A in human beings,” The Lancet Infectious Diseases, vol. 7, no. 4, pp. 257–265, 2007.
[23]
P. Fabian, J. J. McDevitt, E. A. Houseman, and D. K. Milton, “Airborne influenza virus detection with four aerosol samplers using molecular and infectivity assays: considerations for a new infectious virus aerosol sampler,” Indoor Air, vol. 19, no. 5, pp. 433–441, 2009.
[24]
J. D. Noti, W. G. Lindsley, F. M. Blachere et al., “Detection of infectious influenza virus in cough aerosols generated in a simulated patient examination room,” Clinical Infectious Diseases, vol. 54, no. 11, pp. 1569–1577, 2012.
[25]
Z. Wei, M. Mcevoy, V. Razinkov et al., “Biophysical characterization of influenza virus subpopulations using field flow fractionation and multiangle light scattering: correlation of particle counts, size distribution and infectivity,” Journal of Virological Methods, vol. 144, no. 1-2, pp. 122–132, 2007.
[26]
F. M. Blachere, W. G. Lindsley, T. A. Pearce et al., “Measurement of airborne influenza virus in a hospital emergency department,” Clinical Infectious Diseases, vol. 48, no. 4, pp. 438–440, 2009.
[27]
R. G. Loudon and R. M. Roberts, “Droplet expulsion from the respiratory tract,” The American Review of Respiratory Disease, vol. 95, no. 3, pp. 435–442, 1967.
[28]
M. W. Jennison, “Atomizing of mouth and nose secretions into the air as revealed by high-speed photography,” in Aerobiology, F. R. Moulton, Ed., pp. 106–128, American Association for the Advancement of Science, Washington, DC, USA, 1942.
[29]
R. S. Papineni and F. S. Rosenthal, “The size distribution of droplets in the exhaled breath of healthy human subjects,” Journal of Aerosol Medicine: Deposition, Clearance, and Effects in the Lung, vol. 10, no. 2, pp. 105–116, 1997.
[30]
C. Y. H. Chao, M. P. Wan, L. Morawska et al., “Characterization of expiration air jets and droplet size distributions immediately at the mouth opening,” Journal of Aerosol Science, vol. 40, no. 2, pp. 122–133, 2009.
[31]
W. E. Bischoff, K. Swett, I. Leng, and T. R. Peters, “Exposure to influenza virus aerosols during routine patient care,” The Journal of Infectious Diseases, vol. 207, no. 7, pp. 1037–1046, 2013.
[32]
D. K. Milton, M. P. Fabian, B. J. Cowling, M. L. Grantham, and J. J. McDevitt, “Influenza virus aerosols in human exhaled breath: particle size, culturability, and effect of surgical masks,” PLoS Pathogens, vol. 9, no. 3, Article ID e1003205, 2013.
[33]
B. J. Cowling, D. K. Ip, V. J. Fang et al., “Aerosol transmission is an important mode of influenza A virus spread,” Nature Communications, vol. 4, article 1935, 2013.
[34]
T. P. Weber and N. I. Stilianakis, “Inactivation of influenza A viruses in the environment and modes of transmission: a critical review,” Journal of Infection, vol. 57, no. 5, pp. 361–373, 2008.
[35]
S. A. Sattar and M. K. Ijaz, “Airborne viruses,” in Manual of Environmental Microbiology, C. J. Hurst, R. L. Crawford, M. J. McInerney, G. R. Knudsen, and L. D. Stetzenbach, Eds., pp. 871–883, ASM Press, Washington, DC, USA, 2002.
[36]
L. Guertler, “Virology of human influenza,” in Influenza Report, B. S. Kamps, C. Hoffmann, and W. Preiser, Eds., pp. 87–91, Flying, Paris, France, 2006.
[37]
A. C. Lowen, S. Mubareka, T. M. Tumpey, A. García-Sastre, and P. Palese, “The guinea pig as a transmission model for human influenza viruses,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 26, pp. 9988–9992, 2006.
[38]
A. C. Lowen, S. Mubareka, J. Steel, and P. Palese, “Influenza virus transmission is dependent on relative humidity and temperature,” PLoS Pathogens, vol. 3, no. 10, pp. 1470–1476, 2007.
[39]
J. Steel, P. Palese, and A. C. Lowen, “Transmission of a 2009 pandemic influenza virus shows a sensitivity to temperature and humidity similar to that of an H3N2 seasonal strain,” Journal of Virology, vol. 85, no. 3, pp. 1400–1402, 2011.
[40]
W. Yang, S. Elankumaran, and L. C. Marr, “Relationship between humidity and influenza’ s seasonality,” PLoS ONE, vol. 7, no. 10, Article ID e46789, 2012.
[41]
N. Pica, Y. Chou, N. M. Bouvier, and P. Palese, “Transmission of influenza B viruses in the Guinea pig,” Journal of Virology, vol. 86, no. 8, pp. 4279–4287, 2012.
[42]
N. van Hoeven, C. Pappas, J. A. Belser et al., “Human HA and polymerase subunit PB2 proteins confer transmission of an avian influenza virus through the air,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 9, pp. 3366–3371, 2009.
[43]
Y. Chou, R. A. Albrecht, N. Pica et al., “The m segment of the 2009 new pandemic H1N1 influenza virus is critical for its high transmission efficiency in the Guinea pig model,” Journal of Virology, vol. 85, no. 21, pp. 11235–11241, 2011.
[44]
T. T. Lam, H. Zhu, J. Wang et al., “Reassortment events among swine influenza a viruses in China: implications for the origin of the 2009 influenza pandemic,” Journal of Virology, vol. 85, no. 19, pp. 10279–10285, 2011.
[45]
M. B. Pearce, A. Jayaraman, C. Pappas et al., “Pathogenesis and transmission of swine origin A(H3N2)v influenza viruses in ferrets,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 10, pp. 3944–3949, 2012.
[46]
K. H. Chan, S. T. Lai, L. L. M. Poon, Y. Guan, K. Y. Yuen, and J. S. M. Peiris, “Analytical sensitivity of rapid influenza antigen detection tests for swine-origin influenza virus (H1N1),” Journal of Clinical Virology, vol. 45, no. 3, pp. 205–207, 2009.
[47]
C. A. Corzo, A. Romagosa, S. A. Dee, M. R. Gramer, R. B. Morrison, and M. Torremorell, “Relationship between airborne detection of influenza A virus and the number of infected pigs,” Veterinary Journal, vol. 196, no. 2, pp. 171–175, 2013.
[48]
C. I. Fairchild and J. F. Stampfer, “Particle concentration in exhaled breath,” The American Industrial Hygiene Association Journal, vol. 48, no. 11, pp. 948–949, 1987.
[49]
D. A. Edwards, J. C. Man, P. Brand et al., “Inhaling to mitigate exhaled bioaerosols,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 50, pp. 17383–17388, 2004.
