Journal of Infection
Volume 57, Issue 5 , Pages 361-373 , November 2008

Inactivation of influenza A viruses in the environment and modes of transmission: A critical review

  • Thomas P. Weber

      Affiliations

    • Joint Research Centre, European Commission, T.P. 267, Via Enrico Fermi 2749, I-21027 Ispra, Italy
    • Corresponding Author InformationCorresponding author. Tel.: +39 0332 785165; fax: +39 0332 785154.
  • ,
  • Nikolaos I. Stilianakis

      Affiliations

    • Joint Research Centre, European Commission, T.P. 267, Via Enrico Fermi 2749, I-21027 Ispra, Italy
    • Department of Biometry and Epidemiology, University Erlangen-Nürnberg, Waldstrasse 6, D-91054 Erlangen, Germany

,Accepted 27 August 2008.

References 

  1. Garner JS. Guideline for isolation precautions in hospitals. Am J Infect Control. 1996;24:24–52
  2. Nicas M, Nazaroff WW, Hubbard A. Towards understanding the risk of secondary airborne infection: emission of respirable pathogens. J Occ Env Hyg. 2005;2:143–154
  3. Tellier R. Review of aerosol transmission of influenza A virus. Emerg Infect Dis. 2006;12:1657–1662
  4. Brankston G, Gitterman L, Hirji Z, Lemieux C, Gardam M. Transmission of influenza A in human beings. Lancet Infect Dis. 2007;7:257–265
  5. Boone SA, Gerba CP. Significance of fomites in the spread of respiratory and enteric viral disease. Appl Environ Microbiol. 2007;73:1687–1696
  6. Drossinos Y, Housiadas C. Aerosol flows. In:  Crowe CT editors. Multiphase flow handbook. Boca Raton, FL: CRC Press; 2006;p. 6-1–6-58
  7. Morawska L. Droplet fate in indoor environments, or can we prevent the spread of infection. Indoor Air. 2006;16:335–347
  8. Tellier R. Transmission of influenza A in human beings. Lancet Infect Dis. 2007;7:759–760
  9. Lemieux C, Brankston G, Gitterman L, Hirji Z, Gardam M. Questioning aerosol transmission of influenza. Emerg Infect Dis. 2007;13:173–175
  10. Tang WJ, Li Y. Transmission of influenza A in human beings. Lancet Infect Dis. 2007;7:758
  11. Gardam M, Lemieux C. Transmission of influenza A in human beings, Authors' reply. Lancet Infect Dis. 2007;7:761–763
  12. Lee RV. Transmission of influenza A in human beings. Lancet Infect Dis. 2007;7:760–761
  13. Sagripanti JL, Lytle CD. Inactivation of influenza virus by solar radiation. Photochem Photobiol. 2007;83:1278–1282
  14. World Health Organisation Writing Group . Nonpharmaceutical interventions for pandemic influenza, international measures. Emerg Infect Dis. 2006;12:81–87
  15. Nicoll A. Personal (non-pharmaceutical) protective measures for reducing transmission of influenza: ECDC interim recommendations. Eurosurveill. 2006;11:pii=3061. Available from: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleID=3061
  16. Aledort JE, Lurie N, Wasserman J, Bozzette SA. Non-pharmaceutical public health interventions for pandemic influenza: an evaluation of the evidence base. BMC Public Health. 2007;7:208
  17. Cole EC, Cook CE. Characterization of infectious aerosols in health care facilities: an aid to effective engineering controls and preventive strategies. Am J Infect Control. 1998;26:453–464
  18. Salgado C, Farr BM, Hall KK, Hayden FG. Influenza in the acute hospital setting. Lancet Infect Dis. 2002;2:145–155
  19. Nicas M, Sun G. An integrated model of infection risk in a health-care environment. Risk Anal. 2006;26:1085–1095
  20. Tang JW, Li Y, Eames I, Chan PKS, Ridgway GL. Factors involved in the aerosol transmission of infection and control of ventilation in healthcare premises. J Hosp Infect. 2006;64:100–114
  21. Hall CB. The spread of influenza and other respiratory viruses: complexities and conjectures. Clin Infect Dis. 2007;45:353–359
  22. Walther BA, Ewald PW. Pathogen survival in the external environment and the evolution of virulence. Biol Rev. 2004;79:849–869
  23. Mitsakou C, Helmis C, Housiadas C. Eulerian modeling of lung deposition with sectional representation of aerosol dynamics. J Aerosol Sci. 2005;36:75–94
  24. Chapin CV. The sources and modes of infection. New York: John Wiley; 1910;
  25. Wells WF, Brown HW. Recovery of influenza virus suspended in air and its destruction by ultraviolet radiation. Am J Hyg. 1936;24:407–413
  26. Wells WF, Brown HW. Recovery of influenza virus suspended in air. Science. 1936;84:68–69
  27. Wells WF, Henle W. Experimental airborne disease. Quantitative inoculation by inhalation of influenza virus. Proc Soc Exp Biol Med. 1941;48:298–301
  28. Edward DGF. Resistance of influenza virus to drying and its demonstration on dust. Lancet. 1941;238:664–666
  29. Loosli CG, Lemon HM, Robertson OH, Appel E. Experimental airborne influenza infection. I. Influence of humidity on survival of virus in air. Proc Soc Exp Biol. 1943;53:205–206
  30. Shechmeister IL. Studies on the experimental epidemiology of respiratory infections. III. Certain aspects of the behavior of type A influenza virus as an air-borne cloud. J Infect Dis. 1950;87:128–132
  31. Hemmes JH, Winkler KC, Kool SM. Virus survival as a seasonal factor in influenza and poliomyelitis. Nature. 1960;188:430–431
  32. Hood AM. Infectivity of influenza virus aerosols. J Hyg. 1963;61:331–335
  33. Harper GJ. Airborne micro-organisms: survival tests with four viruses. J Hyg. 1961;59:479–486
  34. Hemmes JH, Kool SM, Winkler KC. Virus survival as a seasonal factor in influenza and poliomyelitis. Anton van Lee J M S. 1962;28:221–233
  35. Harper GJ. The influence of environment on the survival of airborne virus particles in the laboratory. Arch Gesamte Virusforsch. 1963;13:64–71
  36. Schulman JL, Kilbourne ED. Experimental transmission of influenza virus in mice. II. Some factors affecting the incidence of transmitted infection. J Exp Med. 1963;118:267–275
  37. Alford RH, Kasel JA, Gerone PJ, Knight V. Human influenza resulting from aerosol inhalation. Proc Soc Exp Biol Med. 1966;122:800–804
  38. Songer JR. Influence of relative humidity on the survival of some airborne viruses. Appl Microbiol. 1967;15:35–42
  39. Mitchell CA, Guerin LF, Robillard J. Decay of influenza A viruses of human and avian origin. Can J Comp Med. 1968;32:544–546
  40. Benbough JE. Some factors affecting survival of airborne viruses. J Gen Virol. 1971;10:209–220
  41. Mitchell CA, Guerin LF. Influenza A of human, swine, equine and avian origin: comparison of survival in aerosol form. Can J Comp Med. 1972;36:9–11
  42. Trouwborst T, Kuyper S, de Jong JC, Plantinga AD. Inactivation of some bacterial and animal viruses by exposure to liquid–air interfaces. J Gen Virol. 1974;24:155–165
  43. Schaffer FL, Soergel ME, Straube DC. Survival of airborne influenza virus: effects of propagating host, relative humidity and composition of spray fluids. Arch Virol. 1976;51:263–273
  44. Knight V. Viruses as agents of airborne contagion. Ann Ny Acad Sci. 1980;353:147–156
  45. Moser MR, Bender T, Margolis HS, Noble GR, Kendal AP, Ritter DG. An outbreak of influenza aboard a commercial airliner. Am J Epidemiol. 1979;110:1–6
  46. Pirtle EC, Beran GW. Virus survival in the environment. Rev Sci Tech OIE. 1991;10:733–748
  47. Sattar SA, Iljaz MK. Spread of viral infections by aerosols. Crit Rev Env Contr. 1987;17:89–131
  48. Lowen AC, Mubareka S, Steel J, Palese P. Influenza virus transmission is dependent on relative humidity and temperature. PLoS Pathogens. 2007;3:e151
  49. Lowen AC, Steel J, Mubareka S, Palese P. High temperature (30°) blocks aerosol but not contact transmission of influenza virus. J Virol. 2008;82:5650–5652
  50. Yu ITS, Li YG, Wong TW, Tam W, Chan AT, Lee JHW, et al. Evidence of airborne transmission of the severe acute respiratory syndrome virus. N Engl J Med. 2004;350:1731–1739
  51. Fennelly KP, Davidow AL, Miller SL, Connell N, Ellner JJ. Airborne infection with Bacillus anthracis – from mills to mail. Emerg Infect Dis. 2004;10:996–1001
  52. Thacker SB. The persistence of influenza A in human populations. Epidemiol Rev. 1986;8:129–142
  53. Nelson MI, Simonsen L, Viboud C, Miller MA, Holmes EC. Phylogenetic analysis reveals the global migration of seasonal influenza A viruses. PLoS Pathogens. 2007;3:e131
  54. Rambaut A, Pybus OG, Nelson MI, Viboud C, Taubenberger JK, Holmes EC. The genomic and epidemiological dynamics of human influenza Avirus. Nature. 2008;453:615–619
  55. Russell CA, Jones TC, Barr IG, Cox NJ, Garten RJ, Gregory V, et al. The global circulation of seasonal influenza A (H3N2) viruses. Science. 2008;320:340–346
  56. Webster RG, Yakhno M, Hinshaw VS, Bean WJ, Murti KG. Intestinal influenza: replication and characterization of influenza viruses in ducks. Virology. 1978;84:268–278
  57. De Benedictis P, Beato MS, Capua I. Inactivation of avian influenza viruses by chemical agents and physical conditions: a review. Zoonoses Public Health. 2007;54:51–68
  58. Jin H, Leser GP, Zhang J, Lamb RA. Influenza virus hemagglutinin and neuraminidase cytoplasmatic tails control particle shape. EMBO J. 1997;16:1236–1247
  59. Burleigh LM, Calder LJ, Skehel JJ, Steinhauer DA. Influenza A viruses with mutations in the M1 helix six domain display a wide variety of morphological phenotypes. J Virol. 2005;79:1262–1270
  60. Roberts PC, Compans RW. Host cell dependence of viral morphology. Proc Natl Acad Sci U S A. 1998;95:5746–5751
  61. Nicholls JM, Chan MCW, Chan WY, Wong HK, Cheung CY, Kwong DLW, et al. Tropism of avian influenza A (H5N1) in the upper and lower respiratory tract. Nat Med. 2007;13:147–149
  62. Van Riel D, Munster VJ, de Wit E, Rimmelzwaan GF, Fouchier RAM, Osterhaus ADME, et al. Human and avian influenza viruses target different cells in the lower respiratory tract of humans and other mammals. Am J Pathol. 2007;171:1215–1223
  63. Matrosovich MN, Matrosovich TY, Gray T, Roberts NA, Klenk HD. Human and avian influenza viruses target different cell types in cultures of human airway epithelium. Proc Natl Acad Sci U S A. 2004;101:4620–4624
  64. Duan SM, Zhao XS, Huang JJ, Pi GH, Zhang SX, Han J, et al. Stability of SARS coronavirus in human specimens and environment and its sensitivity to heating and UV irradiation. Biomed Environ Sci. 2003;16:246–255
  65. Wolff MH, Sattar SA, Adegbunrin O, Tetro J. Environmental survival and microbicide inactivation of coronaviruses. In:  Schmidt A,  Wolff MH,  Weber O editor. Coronaviruses with special emphasis on first insights concerning SARS. Basel: Birkhäuser; 2005;p. 201–212
  66. Lai MYY, Cheng PKC, Lim WWL. Survival of severe acute respiratory syndrome coronavirus. Clin Infect Dis. 2005;41:e67–e71
  67. Hardestam J, Simon M, Hedlund KO, Vaheri A, Klingström J, Lundkvist Å. Ex vivo stability of the rodent-borne Hantaan virus in comparison to that of arthropod-borne members of the Bunyaviridae family. Appl Environ Microbiol. 2007;73:2547–2551
  68. Duguid JP. The size and duration of air-carriage of respiratory droplets and droplet-nuclei. J Hyg. 1946;44:471–479
  69. Loudon RG, Roberts RM. Relation between the airborne diameters of respiratory droplets and the diameter of stains left after recovery. Nature. 1967;213:95–96
  70. Papineni RS, Rosenthal FS. The size distribution of droplets in the exhaled breath of healthy human subjects. J Aerosol Med. 1996;10:105–116
  71. Kennedy NJ, Hinds WC. Inhalability of large solid particles. J Aerosol Sci. 2002;33:237–255
  72. Dai YT, Juang YJ, Wu YY, Breysse PN, Hsu DJ. In vivo measurement of ultralarge aerosol particles in calm air by humans. J Aerosol Sci. 2006;37:967–973
  73. Yu CP, Diu CK. Total and regional deposition of inhaled aerosols in humans. J Aerosol Sci. 1983;14:599–609
  74. Schulz H, Brand P, Heyder J. Particle deposition in the respiratory tract. In:  Gehr P,  Heyder J editor. Particle–lung interactions. New York, Basel: Marcel Dekker; 2000;p. 229–290
  75. De Jong JC, Trouwborst T, Winkler KC. The mechanisms of virus decay in aerosols. In:  Hers JFPh,  Winkler KC editor. Airborne transmission and airborne infection. New York: John Wiley & Sons; 1973;p. 124–130
  76. Rao BL, Banerjee K. Influenza surveillance in Pune, India 1978–90. Bull World Health Organ. 1993;71:177–181
  77. Dosseh A, Ndiaye K, Spiegel A, Sagna M, Mathiot C. Epidemiological and virological influenza survey in Dakar, Senegal: 1996–1998. Am J Trop Med Hyg. 2000;62:639–643
  78. De Arruda E, Hayden FG, McAuliffe JF, Desousa MA, Mota SB, McAuliffe MI, et al. Acute respiratory viral infections in ambulatory children in urban northeast Brazil. J Infect Dis. 1991;164:252–258
  79. Alonso WJ, Viboud C, Simonsen L, Hirano EW, Daufenbach LZ, Miller MA. Seasonality of influenza in Brazil: a traveling wave from the Amazon to the subtropics. Am J Epidemiol. 2007;165:1434–1442
  80. Chew FT, Doraisingham S, Ling AE, Kumarasinghe G, Lee BW. Seasonal trends of viral respiratory tract infections in the tropics. Epidemiol Infect. 1998;121:121–128
  81. Nguyen HL, Saito R, Ngiem HK, Nishikawa M, Shobugawa Y, Nguyen DC, et al. Epidemiology of influenza in Hanoi, Vietnam, from 2001 to 2003. J Infect. 2007;55:58–63
  82. Park AW, Glass K. Dynamic patterns of avian and human influenza in east and southeast Asia. Lancet Infect Dis. 2007;7:543–548
  83. Buckland FE, Tyrrell DAJ. Loss of infectivity on drying various viruses. Nature. 1962;195:1063–1064
  84. Tamm I, Fluke DJ. The effect of monochromatic ultraviolet radiation on the infectivity and hemagglutinating ability of the influenza type A strain PR-8. J Bacteriol. 1950;59:449–461
  85. Powell WF, Setlow RB. The effect of monochromatic ultraviolet radiation on the interfering property of influenza virus. Virology. 1956;2:337–343
  86. Jensen MM. Inactivation of airborne viruses by ultraviolet irradiation. Appl Microbiol. 1964;12:418–420
  87. Lytle CD, Sagripanti JL. Predicted inactivation of viruses of relevance to biodefense by solar radiation. J Virol. 2005;79:14244–14252
  88. Walker CM, Ko G. Effect of ultraviolet germicidal irradiation on viral aerosols. Environ Sci Technol. 2007;41:5460–5465
  89. Weber TP, Stilianakis NI. A note on the inactivation of influenza A viruses through solar radiation, relative humidity and temperature. Photochem Photobiol. doi:10.1111/j.1751-1097.2008.00416.x.
  90. Druett HA, May KR. Unstable germicidal pollutant in rural air. Nature. 1968;220:395–396
  91. De Mik G, de Groot I. Mechanisms of inactivation of bacteriophage psi-X174 and its DNA in aerosols by ozone and ozonized cyclohexene. J Hyg. 1977;78:199–211
  92. Kekez MM, Sattar SA. A new ozone-based method for virus inactivation: preliminary study. Phys Med Biol. 1997;42:2027–2039
  93. Bailey R, Fielding L, Young A, Griffith C. Effect of ozone and open air factor against aerosolized Micrococcus luteus. J Food Prot. 2007;70:2769–2773
  94. Polozov IV, Bezrukov L, Gawrisch K, Zimmerberg J. Progressive ordering with decreasing temperature of the phospholipids of influenza virus. Nature Chem Biol. 2008;4:248–255
  95. Adams MH. Surface inactivation of bacterial viruses and of proteins. J Gen Physiol. 1948;31:417–432
  96. Atkinson MP, Wein LM. Quantifying the routes of transmission for pandemic influenza. Bull Math Biol. 2008;70:820–867
  97. Couch RB, Douglas RG, Fedson DS, Kasel JR. Correlated studies of a recombinant influenza-virus vaccine. III. Protection against experimental infection in man. J Infect Dis. 1971;124:473–480
  98. Hayden FG, Treanor JJ, Betts RF, Lobo M, Esinhart JD, Hussey EK. Safety and efficacy of the neuraminidase inhibitor GG167 in experimental human influenza. JAMA. 1996;275:295–299
  99. Olofsson S, Kumlin U, Dimock K, Arnberg N. Avian influenza and sialic acid receptors: more than meets the eye?. Lancet Infect Dis. 2005;5:184–188
  100. Brady MT, Evans J, Cuartas J. Survival and disinfection of parainfluenza viruses on environmental surfaces. Am J Infect Control. 1990;18:18–23
  101. Ansari SA, Springthorpe VS, Sattar SA, Rivard S, Rahman M. Potential role of hands in the spread of respiratory viral infections – studies with human parainfluenza virus 3 and rhinovirus 14. J Clin Microbiol. 1991;29:2115–2119
  102. Woolwine JD, Gerberding JL. Effect of testing method on apparent activities of antiviral disinfectants and antiseptics. Antimicrobial Agents Chemother. 1995;39:921–923
  103. Sattar SA, Springthorpe VS, Tetro J, Vashon R, Keswick B. Hygienic hand antiseptics: should they not have activity and label claims against viruses?. Am J Infect Control. 2002;30:355–372
  104. Parker ER, MacNeal WJ. Persistence of influenza virus on the human hand. J Lab Clin Med. 1944;29:121–126
  105. Bean B, Moore BM, Sterner B, Peterson R, Gerding DN, Balfour HH. Survival of influenza viruses on environmental surfaces. J Infect Dis. 1982;146:47–51
  106. Schürmann W, Eggers HJ. Antiviral activity of an alcoholic hand disinfectant. Comparison of the in vitro suspension test with in vivo experiments on hands, and on individual fingertips. Antiviral Res. 1983;3:25–41
  107. Thomas Y, Vogel G, Wunderli W, Suter P, Witschi M, Koch D, et al. Survival of influenza virus on banknotes. Appl Environ Microbiol. 2008;74:3002–3007
  108. Boone SA, Gerba CP. The occurrence of influenza A virus on household and day care center fomites. J Infect. 2005;51:103–109
  109. Noyce JO, Michels H, Keevil CW. Inactivation of influenza A virus on copper versus stainless steel surfaces. Appl Environ Microbiol. 2007;73:2748–2750
  110. Tiwari A, Patnayak DP, Chander Y, Parsad M, Goyal SM. Survival of two avian respiratory viruses on porous and nonporous surfaces. Avian Dis. 2006;50:284–287
  111. Hendley JO, Wenzel RP, Gwaltney JR. Transmission of rhinovirus colds by self-inoculation. N Engl J Med. 1973;288:1361–1364
  112. Winther B, McCue K, Ashe K, Rubino JR, Hendley JO. Environmental contamination with rhinovirus and transfer to fingers of healthy individuals by daily life activity. J Med Virol. 2007;79:1606–1610
  113. Woolhouse ME, Gowtage-Sequeria S. Host range and emerging and reemerging pathogens. Emerg Infect Dis. 2005;11:1842–1847
  114. Webby RJ, Webster RG, Richt JA. Influenza viruses in animal wildlife populations. Curr Top Microbiol. 2007;31:67–83
  115. Olsen B, Wallensten A, Waldenström J, Osterhaus ADME, Fouchier RAM. Global patterns of influenza A virus in wild birds. Science. 2006;312:384–388
  116. Van Gils JA, Munster VJ, Radersma R, Liefhebber D, Fouchier RAM, Klaassen M. Hampered foraging and migratory performance in swans infected with low-pathogenic influenza A virus. PLoS One. 2007;1:e184
  117. Weber TP, Stilianakis NI. Ecologic immunology of avian influenza (H5N1) in migratory birds. Emerg Infect Dis. 2007;13:1139–1143
  118. Hinshaw VS, Webster RG, Turner B. Water-borne transmission of influenza A viruses. Intervirology. 1979;11:66–68
  119. Webster RG, Peiris M, Chen H, Guan Y. H5N1 outbreaks and enzootic influenza. Emerg Infect Dis. 2006;12:3–8
  120. Rimmelzwaan GF, van Riel D, Baars M, Bestebroer TM, van Amerongen G, Fouchier RAM, et al. Influenza A virus (H5N1) infection cats causes systemic disease with potential novel routes of virus spread within and between hosts. Am J Pathol. 2006;168:176–183
  121. Liu M, Guan Y, Peiris M, He S, Webby RJ, Perez D, et al. The quest of influenza A viruses for new hosts. Avian Dis. 2003;47:S849–S856
  122. World Health Organization . Review of latest available evidence on risks to human health through potential transmission of avian influenza (H5N1) through water and sewage. Geneva: The Organization; 2006;WHO/SDE/WSH/06.1
  123. Zhang G, Shoham D, Gilichinsky D, Davydov S, Castello JD, Rogers SO. Evidence of influenza A virus RNA in Siberian lake ice. J Virol. 2006;80:12229–12235
  124. Brown JD, Swayne DE, Cooper RJ, Burns RE, Stallknecht DE. Persistence of H5 and H7 avian influenza viruses in water. Avian Dis. 2007;51:285–289
  125. Haydon DT, Cleaveland S, Taylor LH, Laurenson MK. Identifying reservoirs of infection: a conceptual and practical challenge. Emerg Infect Dis. 2002;8:1468–1473
  126. England LS, Holmes SB, Trevors JT. Persistence of viruses and DNA in soil. World J Microbiol Biotechnol. 1998;14:163–169
  127. Lang AS, Kelly A, Runstadler JA. Prevalence and diversity of avian influenza viruses in environmental reservoirs. J Gen Virol. 2008;89:509–519
  128. Smith AW, Skilling DE, Castello JD, Rogers SO. Ice as a reservoir for pathogenic human viruses: specifically, caliciviruses, influenza viruses, and enteroviruses. Med Hypotheses. 2004;63:560–566
  129. Atmar RL. Influenza viruses. ch. 85 In:  Murray PR,  Baron EJ,  Jorgensen JH,  Pfaller MA,  Landry ML editor. Manual of clinicalmicrobiology. 9th ed.. Washington: ASM Press; 2007;
  130. Wororbey M. Phylogenetic evidence against evolutionary stasis and natural abiotic reservoirs of influenza A virus. J Virol. 2008;82:3769–3774
  131. Balasubramanian V, Wiegeshaus EH, Taylor BT, Smith DW. Pathogenesis of tuberculosis: pathway to apical localization. Tubercle Lung Dis. 1994;75:168–178
  132. Wei Z, Mcevoy M, Razinkov V, Polozova A, Li E, Casas-Finet J, et al. Biophysical characterization of influenza virus subpopulations using field flow fractionation and multi angle light scattering: correlation of particle counts, size distribution and infectivity. J Virol Methods. 2007;144:122–132
  133. Lamb RA, Krug RM. Orthomyxoviridae: the viruses and their replication. In:  Fields BN,  Knipe DM,  Howley PM,  Griffin DE,  Lamb RA,  Martin MA,  Roizman B,  Straus SE editor. Fields virology. 4th ed.. Philadelphia, PA: Lippincott Williams and Wilkins Publishers; 2001;p. 1487–1531
  134. Van Elden LJR, Nijhuis M, Schipper P, Schuurman R, van Loon AM. Simultaneous detection of influenza viruses A and B using real-time quantitative PCR. J Clin Microbiol. 2001;39:196–200
  135. Falsey AR, Criddle MM, Kolassa JE, McCann RM, Brower CA, Hall WJ. Evaluation of a handwashing intervention to reduce respiratory illness rates in senior day-care centers. Infect Control Hosp Epidemiol. 1999;20:200–202
  136. Rabie T, Curtis V. Handwashing and risk of respiratory infections: a quantitative systematic review. Trop Med Int Health. 2006;11:258–267
  137. Bloomfield SF, Aiello AE, Cookson B, O'Boyle C, Larson EL. The effectiveness of hand hygiene procedures in reducing the risks of infections in home and community settings including handwashing and alcohol-based hand sanitizers. Am J Infect Control. 2007;35(S1):S27–S64
  138. Lau JT, Tsui H, Lau M, Yang X. SARS transmission, risk factors, and prevention in Hong Kong. Emerg Infect Dis. 2004;10:587–592
  139. Nishiura H, Kurasutji T, Quy T, Phi NC, Van Ban V, Ha LE, et al. Rapid awareness and transmission of severe acute respiratory syndrome in Hanoi French Hospital, Vietnam. Am J Trop Med Hyg. 2005;73:17–25
  140. Seto WH, Tsang D, Yung RW, Ching TY, Ng TK, Ho M, et al. Effectiveness of precautions against droplets and contact in prevention of nosocomial transmission of severe acute respiratory syndrome. Lancet. 2003;361:1519–1520
  141. Lo JY, Tsang TH, Leung YH, Yeung EY, Wu T, Lim WW. Respiratory infections during SARS outbreak, Hong Kong, 2003. Emerg Infect Dis. 2005;11:1738–1741
  142. Nayak DP, Hui KHW, Barman S. Assembly and budding of influenza virus. Virus Res. 2004;106:147–165
  143. Aloia RC, Tian H, Jensen FC. Lipid composition and fluidity of the human immunodeficiency virus envelope and host cell plasma membrane. Proc Natl Acad Sci U S A. 1993;90:5181–5185
  144. Blough HA. Fatty acid composition of individual phospholipids of influenza virus. J Gen Virol. 1971;12:317–320
  145. Cummings KJ, Cox-Ganser J, Riggs MA, Edwards N, Kreiss K. Respirator donning in post-hurricane New Orleans. Emerg Infect Dis. 2007;13:700–707
  146. Reynolds DL, Garay JR, Deamond SL, Moran MK, Gold W, Styra R. Understanding, compliance and psychological impact of the SARS quarantine experience. Epidemiol Infect. 2008;136:997–1007

PII: S0163-4453(08)00292-2

doi: 10.1016/j.jinf.2008.08.013

Journal of Infection
Volume 57, Issue 5 , Pages 361-373 , November 2008