The air we breathe contains microorganisms that can cause infectious respiratory diseases. After two occupants of an apartment were diagnosed with influenza in February of 2013, efforts were made to detect and isolate airborne influenza virus using two different types of active air samplers: a Sioutas Personal Cascade Impactor Sampler (PCIS) and an SKC BioSampler. The PCIS collects size-fractionated particles by impaction on polytetrafluoroethylene filters, whereas the SKC BioSampler collects airborne particles in liquid media. Influenza H3N2 virus was collected by both types of air samplers. The PCIS collected a range of particle sizes containing influenza virus near one of the sick individuals but only ultrafine particles when the samplers were positioned farther away. Viable virus was present in the liquid collection media of the SKC BioSampler and some PCIS filters. These findings suggest that influenza patients produce ultrafine aerosol particles that contain viable virus. 1. Introduction Airborne microorganisms are typically present in the air we breathe and are potential causes of infectious diseases. Influenza viruses are among the respiratory pathogens that can be transmitted by airborne routes [1–4]. Breathing, coughing, sneezing, and talking during the course of influenza generate a cloud of airborne particles containing influenza virus. The airborne particles have diameters that range from a few millimeters (large droplets formed during coughing and sneezing) to submicron (<1？μm) (formed during breathing). Small particles (≤5？μm) including droplet nuclei from evaporated larger particles can remain airborne for hours (these concepts and their relevance to influenza viruses are discussed in [1, 3–14]). Presently, the US Centers for Disease Control and Prevention (CDC) and the World Health Organization (WHO) state that influenza virus transmission occurs mostly by large-particle respiratory droplets that travel only a short distance from the source (1.829？m (6 feet) according to the CDC and 1？m (3.3 feet) according to the WHO) [15–17]. Noteworthy, deposition of influenza virus into the lungs (as small particles) versus the upper respiratory tract (as large droplets) may increase infection risk and illness severity [3, 9, 18–20]. Assessments of microbiological air quality are useful for studies of the airborne transmission of pathogens and of other biological particles in the air that may cause noninfectious diseases (such as allergy to pollen). The two principle methods of assessing microbiological air quality are passive monitoring and active
References
[1]
G. Brankston, L. Gitterman, Z. Hirji, C. Lemieux, and M. Gardam, “Transmission of influenza A in human beings,” Lancet Infectious Diseases, vol. 7, no. 4, pp. 257–265, 2007.
[2]
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.
[3]
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.
[4]
J. A. Belser, T. R. Maines, T. M. Tumpey, and J. M. Katz, “Influenza A virus transmission: contributing factors and clinical implications,” Expert Reviews in Molecular Medicine, vol. 12, article e39, 2010.
[5]
M. Nicas, W. W. Nazaroff, and A. Hubbard, “Toward understanding the risk of secondary airborne infection: emission of respirable pathogens,” Journal of Occupational and Environmental Hygiene, vol. 2, no. 3, pp. 143–154, 2005.
[6]
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.
[7]
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.
[8]
S. Stelzer-Braid, B. G. Oliver, A. J. Blazey et al., “Exhalation of respiratory viruses by breathing, coughing, and talking,” Journal of Medical Virology, vol. 81, no. 9, pp. 1674–1679, 2009.
[9]
J. A. Lednicky, S. B. Hamilton, R. S. Tuttle, W. A. Sosna, D. E. Daniels, and D. E. Swayne, “Ferrets develop fatal influenza after inhaling small particle aerosols of highly pathogenic avian influenza virus A/Vietnam/1203/2004 (H5N1),” Virology Journal, vol. 7, article 231, 2010.
[10]
P. Fabian, J. Brain, E. A. Houseman, J. Gern, and D. K. Milton, “Origin of exhaled breath particles from healthy and human rhinovirus-infected subjects,” Journal of Aerosol Medicine and Pulmonary Drug Delivery, vol. 24, no. 3, pp. 137–147, 2011.
[11]
J. Gralton, E. Tovey, M. L. McLaws, and W. D. Rawlinson, “The role of particle size in aerosolised pathogen transmission: a review,” Journal of Infection, vol. 62, no. 1, pp. 1–13, 2011.
[12]
W. G. Lindsley, T. A. Pearce, J. B. Hudnall et al., “Quantity and size distribution of cough-generated aerosol particles produced by influenza patients during and after illness,” Journal of Occupational and Environmenatl Hygiene, vol. 9, no. 7, pp. 443–449, 2012.
[13]
W. E. Bischoff, K. Swett, I. Leng, and T. R. Peters, “Exposure to influenza virus aerosols during routine patient care,” Journal of Infectious Diseases, vol. 207, no. 7, pp. 1037–1046, 2013.
[14]
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.
[15]
Healthcare Infection Control Practices Advisory Committee, “2007 guideline for isolation precautions: preventing transmission of infectious agents in healthcare settings,” 2013, http://www.cdc.gov/hicpac/2007IP/2007ip_part4.html#4.
[16]
Centers for Disease Control and Prevention, “Prevention strategies for seasonal influenza in healthcare settings,” 2010, http://www.cdc.gov/flu/professionals/infectioncontrol/healthcaresettings.htm.
[17]
World Health Organization, “Epidemic- and pandemic-prone acute respiratory diseases infection prevention and control for acute respiratory diseases in health-care facilities,” 2008, http://www.who.int/csr/resources/publications/EPR_AM3_E3.pdf.
[18]
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.
[19]
R. Tellier, “Review of aerosol transmission of influenza A virus,” Emerging Infectious Diseases, vol. 12, no. 11, pp. 1657–1662, 2006.
[20]
P. F. M. Teunis, N. Brienen, and M. E. E. Kretzschmar, “High infectivity and pathogenicity of influenza A virus via aerosol and droplet transmission,” Epidemics, vol. 2, no. 4, pp. 215–222, 2010.
[21]
W. Kowalski, Hospital Airborne Infection Control, CRC Press, 2011.
[22]
D. Verreault, S. Moineau, and C. Duchaine, “Methods for sampling of airborne viruses,” Microbiology and Molecular Biology Reviews, vol. 72, no. 3, pp. 413–444, 2008.
[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]
P. Fabian, J. J. McDevitt, W. M. Lee, E. A. Houseman, and D. K. Milton, “An optimized method to detect influenza virus and human rhinovirus from exhaled breath and the airborne environment,” Journal of Environmental Monitoring, vol. 11, no. 2, pp. 314–317, 2009.
[25]
S. A. Sattar and M. K. Ijaz, “Airborne virusesin,” in Manual of Environmental Microbiology, C. J. Hurst, G. R. Knudsen, M. J. Mcinerney, L. D. Stetzenbach, and M. V. Walter, Eds., pp. 682–692, ASM Press, Washington, DC, USA, 2002.
[26]
C. Misra, M. Singh, S. Shen, C. Sioutas, and P. M. Hall, “Development and evaluation of a personal cascade impactor sampler (PCIS),” Journal of Aerosol Science, vol. 33, no. 7, pp. 1027–1047, 2002.
[27]
K. Willeke, X. Lin, and S. A. Grinshpun, “Improved aerosol collection by combined impaction and centrifugal motion,” Aerosol Science and Technology, vol. 28, no. 5, pp. 439–456, 1998.
[28]
C. J. Hogan Jr., E. M. Kettleson, M. H. Lee, B. Ramaswami, L. T. Angenent, and P. Biswas, “Sampling methodologies and dosage assessment techniques for submicrometre and ultrafine virus aerosol particles,” Journal of Applied Microbiology, vol. 99, no. 6, pp. 1422–1434, 2005.
[29]
J. E. Farnsworth, S. M. Goyal, S. Won Kim et al., “Development of a method for bacteria and virus recovery from heating, ventilation, and air conditioning (HVAC) filters,” Journal of Environmental Monitoring, vol. 8, no. 10, pp. 1006–1013, 2006.
[30]
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.
[31]
G. Cao, J. D. Noti, F. M. Blachere, W. G. Lindsley, and D. H. Beezhold, “Development of an improved methodology to detect infectious airborne influenza virus using the NIOSH bioaerosol sampler,” Journal of Environmental Monitoring, vol. 13, no. 12, pp. 3321–3328, 2011.
[32]
J. A. Lednicky and D. E. Wyatt, “The art of animal cell culture for virus isolation,” in Biomedical Tissue Culture, L. Ceccherini-Nell and B. Matteoli, Eds., pp. 151–178, InTech, Zagreb, Croatia, 2012.
[33]
S. B. Hamilton, D. E. Wyatt, B. T. Wahlgren et al., “Higher titers of some H5N1 and recent human H1N1 and H3N2 influenza viruses in Mv1 Lu vs. MDCK cells,” Virology Journal, vol. 8, article 66, 2011.
[34]
World Health Organization, “WHO information for molecular diagnosis of influenza virus in humans,” update, 2012, http://www.who.int/influenza/gisrs_laboratory/molecular_diagnosis_influenza_virus_humans_update_201211.pdf.
[35]
J. D. Noti, F. M. Blachere, C. M. McMillen et al., “High humidity leads to loss of infectious influenza virus from simulated coughs,” PLoS ONE, vol. 8, no. 2, Article ID e57485, 2013.
