1932

Abstract

Respiratory viruses, such as influenza viruses, cause significant morbidity and mortality worldwide through seasonal epidemics and sporadic pandemics. Influenza viruses transmit through multiple modes including contact (either direct or through a contaminated surface) and inhalation of expelled aerosols. Successful human to human transmission requires an infected donor who expels virus into the environment, a susceptible recipient, and persistence of the expelled virus within the environment. The relative efficiency of each mode can be altered by viral features, environmental parameters, donor and recipient host characteristics, and viral persistence. Interventions to mitigate transmission of influenza viruses can target any of these factors. In this review, we discuss many aspects of influenza virus transmission, including the systems to study it, as well as the impact of natural barriers and various nonpharmaceutical and pharmaceutical interventions.

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2023-09-29
2024-04-21
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Literature Cited

  1. 1.
    Molinari NA, Ortega-Sanchez IR, Messonnier ML, Thompson WW, Wortley PM et al. 2007. The annual impact of seasonal influenza in the US: measuring disease burden and costs. Vaccine 25:5086–96
    [Google Scholar]
  2. 2.
    Bart KJ, Orenstein WA, Preblud SR, Hinman AR. 1985. Universal immunization to interrupt rubella. Rev. Infect. Dis. 7:S177–84
    [Google Scholar]
  3. 3.
    Plotkin SA 2017. Rubella vaccines. Plotkin's Vaccines SA Plotkin, WA Orenstein, PA Offit 970–1000. Philadelphia: Elsevier. , 7th ed..
    [Google Scholar]
  4. 4.
    Wang CC, Prather KA, Sznitman J, Jimenez JL, Lakdawala SS et al. 2021. Airborne transmission of respiratory viruses. Science 373:6558eabd914
    [Google Scholar]
  5. 5.
    Marr LC, Tang JW, Van Mullekom J, Lakdawala SS. 2019. Mechanistic insights into the effect of humidity on airborne influenza virus survival, transmission and incidence. J. R. Soc. Interface 16:20180298
    [Google Scholar]
  6. 6.
    Bourouiba L. 2021. Fluid dynamics of respiratory infectious diseases. Annu. Rev. Biomed. Eng. 23:547–77
    [Google Scholar]
  7. 7.
    Lakdawala SS, Jayaraman A, Halpin RA, Lamirande EW, Shih AR et al. 2015. The soft palate is an important site of adaptation for transmissible influenza viruses. Nature 526:122–25
    [Google Scholar]
  8. 8.
    Richard M, van den Brand JMA, Bestebroer TM, Lexmond P, de Meulder D et al. 2020. Influenza A viruses are transmitted via the air from the nasal respiratory epithelium of ferrets. Nat. Commun. 11:766
    [Google Scholar]
  9. 9.
    Xie C, Su W, Sia SF, Choy KT, Morrell S et al. 2022. A(H1N1)pdm09 influenza viruses replicating in ferret upper or lower respiratory tract differed in onward transmission potential by air. J. Infect. Dis. 225:65–74
    [Google Scholar]
  10. 10.
    Gustin KM, Belser JA, Wadford DA, Pearce MB, Katz JM et al. 2011. Influenza virus aerosol exposure and analytical system for ferrets. PNAS 108:8432–37
    [Google Scholar]
  11. 11.
    Luo B, Schaub A, Glas I, Klein LK, David SC et al. 2023. Expiratory aerosol pH: the overlooked driver of airborne virus inactivation. Environ. Sci. Technol. 57:486–97
    [Google Scholar]
  12. 12.
    Moser MR, Bender TR, Margolis HS, Noble GR, Kendal AP, Ritter DG. 1979. An outbreak of influenza aboard a commercial airliner. Am. J. Epidemiol. 110:1–6
    [Google Scholar]
  13. 13.
    Wong BC, Lee N, Li Y, Chan PK, Qiu H et al. 2010. Possible role of aerosol transmission in a hospital outbreak of influenza. Clin. Infect. Dis. 51:1176–83
    [Google Scholar]
  14. 14.
    Cowling BJ, Ip DK, Fang VJ, Suntarattiwong P, Olsen SJ et al. 2013. Aerosol transmission is an important mode of influenza A virus spread. Nat. Commun. 4:1935
    [Google Scholar]
  15. 15.
    Belser JA, Eckert AM, Tumpey TM, Maines TR. 2016. Complexities in ferret influenza virus pathogenesis and transmission models. Microbiol. Mol. Biol. Rev. 80:733–44
    [Google Scholar]
  16. 16.
    Lowen AC, Bouvier NM, Steel J. 2014. Transmission in the guinea pig model. Curr. Top. Microbiol. Immunol. 385:157–83
    [Google Scholar]
  17. 17.
    Talaat M, Afifi S, Dueger E, El-Ashry N, Marfin A et al. 2011. Effects of hand hygiene campaigns on incidence of laboratory-confirmed influenza and absenteeism in schoolchildren, Cairo, Egypt. Emerg. Infect. Dis. 17:619–25
    [Google Scholar]
  18. 18.
    Gordon A, Tsang TK, Cowling BJ, Kuan G, Ojeda S et al. 2018. Influenza transmission dynamics in urban households, Managua, Nicaragua, 2012–2014. Emerg. Infect. Dis. 24:1882–88
    [Google Scholar]
  19. 19.
    Lowen AC, Mubareka S, Steel J, Palese P. 2007. Influenza virus transmission is dependent on relative humidity and temperature. PLOS Pathog. 3:1470–76
    [Google Scholar]
  20. 20.
    Lowen AC, Steel J, Mubareka S, Palese P. 2008. High temperature (30 degrees C) blocks aerosol but not contact transmission of influenza virus. J. Virol. 82:5650–52
    [Google Scholar]
  21. 21.
    Gustin KM, Belser JA, Veguilla V, Zeng H, Katz JM et al. 2015. Environmental conditions affect exhalation of H3N2 seasonal and variant influenza viruses and respiratory droplet transmission in ferrets. PLOS ONE 10:e0125874
    [Google Scholar]
  22. 22.
    Kormuth KA, Lin K, Qian Z, Myerburg MM, Marr LC, Lakdawala SS. 2019. Environmental persistence of influenza viruses is dependent upon virus type and host origin. mSphere 4:4e00552–19
    [Google Scholar]
  23. 23.
    Irwin CK, Yoon KJ, Wang C, Hoff SJ, Zimmerman JJ et al. 2011. Using the systematic review methodology to evaluate factors that influence the persistence of influenza virus in environmental matrices. Appl. Environ. Microbiol. 77:1049–60
    [Google Scholar]
  24. 24.
    Thai PQ, Mai LQ, Welkers MRA, Hang NLK, Thanh LT et al. 2014. Pandemic H1N1 virus transmission and shedding dynamics in index case households of a prospective Vietnamese cohort. J. Infect. 68:581–90
    [Google Scholar]
  25. 25.
    Loeb M, Singh PK, Fox J, Russell ML, Pabbaraju K et al. 2012. Longitudinal study of influenza molecular viral shedding in Hutterite communities. J. Infect. Dis. 206:1078–84
    [Google Scholar]
  26. 26.
    Memoli MJ, Czajkowski L, Reed S, Athota R, Bristol T et al. 2015. Validation of the wild-type influenza A human challenge model H1N1pdMIST: an A(H1N1)pdm09 dose-finding investigational new drug study. Clin. Infect. Dis. 60:693–702
    [Google Scholar]
  27. 27.
    Freitas FT, Cabral AP, Barros EN, Burigo MJ, Prochnow RD et al. 2013. Pre-symptomatic transmission of pandemic influenza H1N1 2009: investigation of a family cluster, Brazil. Epidemiol. Infect. 141:763–66
    [Google Scholar]
  28. 28.
    Carrat F, Vergu E, Ferguson NM, Lemaitre M, Cauchemez S et al. 2008. Time lines of infection and disease in human influenza: a review of volunteer challenge studies. Am. J. Epidemiol. 167:775–85
    [Google Scholar]
  29. 29.
    Fox JP, Hall CE, Cooney MK, Foy HM. 1982. Influenzavirus infections in Seattle families, 1975–1979. I. Study design, methods and the occurrence of infections by time and age. Am. J. Epidemiol. 116:212–27
    [Google Scholar]
  30. 30.
    Buck C. 1956. Acute upper respiratory infections in families. Am. J. Hyg. 63:1–12
    [Google Scholar]
  31. 31.
    Lidwell OM, Sommerville T. 1951. Observations on the incidence and distribution of the common cold in a rural community during 1948 and 1949. J. Hyg. 49:365–81
    [Google Scholar]
  32. 32.
    Dingle JH, Badger GF, Feller AE, Hodges RG, Jordan WS Jr., Rammelkamp CH Jr. 1953. A study of illness in a group of Cleveland families. I. Plan of study and certain general observations. Am. J. Hyg. 58:16–30
    [Google Scholar]
  33. 33.
    Viboud C, Boelle PY, Cauchemez S, Lavenu A, Valleron AJ et al. 2004. Risk factors of influenza transmission in households. Br. J. Gen. Pract. 54:684–89
    [Google Scholar]
  34. 34.
    Cauchemez S, Ferguson NM, Fox A, Mai LQ, Thanh LT et al. 2014. Determinants of influenza transmission in South East Asia: insights from a household cohort study in Vietnam. PLOS Pathog. 10:e1004310
    [Google Scholar]
  35. 35.
    Carcione D, Giele CM, Goggin LS, Kwan KS, Smith DW et al. 2011. Secondary attack rate of pandemic influenza A(H1N1) 2009 in Western Australian households, 29 May–7 August 2009. Eurosurveillance 16:19765
    [Google Scholar]
  36. 36.
    Cowling BJ, Chan KH, Fang VJ, Lau LLH, So HC et al. 2010. Comparative epidemiology of pandemic and seasonal influenza A in households. N. Engl. J. Med. 362:2175–84
    [Google Scholar]
  37. 37.
    Zhao X, Nie W, Zhou C, Cheng M, Wang C et al. 2019. Airborne transmission of influenza virus in a hospital of Qinhuangdao during 2017–2018 flu season. Food Environ. Virol. 11:427–39
    [Google Scholar]
  38. 38.
    Chamseddine A, Soudani N, Kanafani Z, Alameddine I, Dbaibo G et al. 2021. Detection of influenza virus in air samples of patient rooms. J. Hosp. Infect. 108:33–42
    [Google Scholar]
  39. 39.
    Blachere FM, Lindsley WG, Pearce TA, Anderson SE, Fisher M et al. 2009. Measurement of airborne influenza virus in a hospital emergency department. Clin. Infect. Dis. 48:438–40
    [Google Scholar]
  40. 40.
    Bischoff WE, Swett K, Leng I, Peters TR. 2013. Exposure to influenza virus aerosols during routine patient care. J. Infect. Dis. 207:1037–46
    [Google Scholar]
  41. 41.
    Leung NH, Zhou J, Chu DK, Yu H, Lindsley WG et al. 2016. Quantification of influenza virus RNA in aerosols in patient rooms. PLOS ONE 11:e0148669
    [Google Scholar]
  42. 42.
    Yip L, Finn M, Granados A, Prost K, McGeer A et al. 2019. Influenza virus RNA recovered from droplets and droplet nuclei emitted by adults in an acute care setting. J. Occup. Environ. Hyg. 16:341–48
    [Google Scholar]
  43. 43.
    Xie C, Lau EHY, Yoshida T, Yu H, Wang X et al. 2020. Detection of influenza and other respiratory viruses in air sampled from a university campus: a longitudinal study. Clin. Infect. Dis. 70:850–58
    [Google Scholar]
  44. 44.
    Coleman KK, Sigler WV. 2020. Airborne influenza A virus exposure in an elementary school. Sci. Rep. 10:1859
    [Google Scholar]
  45. 45.
    Shiu EYC, Huang W, Ye D, Xie Y, Mo J et al. 2020. Frequent recovery of influenza A but not influenza B virus RNA in aerosols in pediatric patient rooms. Indoor Air 30:805–15
    [Google Scholar]
  46. 46.
    Milton DK, Fabian MP, Cowling BJ, Grantham ML, McDevitt JJ. 2013. Influenza virus aerosols in human exhaled breath: particle size, culturability, and effect of surgical masks. PLOS Pathog. 9:e1003205
    [Google Scholar]
  47. 47.
    Yan J, Grantham M, Pantelic J, Bueno de Mesquita PJ, Albert B et al. 2018. Infectious virus in exhaled breath of symptomatic seasonal influenza cases from a college community. PNAS 115:1081–86
    [Google Scholar]
  48. 48.
    Lindsley WG, Blachere FM, Beezhold DH, Thewlis RE, Noorbakhsh B et al. 2016. Viable influenza A virus in airborne particles expelled during coughs versus exhalations. Influenza Other Respir. . Viruses 10:404–13
    [Google Scholar]
  49. 49.
    Lindsley WG, Noti JD, Blachere FM, Thewlis RE, Martin SB et al. 2015. Viable influenza A virus in airborne particles from human coughs. J. Occup. Environ. Hyg. 12:107–13
    [Google Scholar]
  50. 50.
    Hatagishi E, Okamoto M, Ohmiya S, Yano H, Hori T et al. 2014. Establishment and clinical applications of a portable system for capturing influenza viruses released through coughing. PLOS ONE 9:e103560
    [Google Scholar]
  51. 51.
    Pan M, Lednicky JA, Wu CY. 2019. Collection, particle sizing and detection of airborne viruses. J. Appl. Microbiol. 127:1596–611
    [Google Scholar]
  52. 52.
    Nguyen-Van-Tam JS, Killingley B, Enstone J, Hewitt M, Pantelic J et al. 2020. Minimal transmission in an influenza A (H3N2) human challenge-transmission model within a controlled exposure environment. PLOS Pathog. 16:e1008704
    [Google Scholar]
  53. 53.
    Killingley B, Enstone JE, Greatorex J, Gilbert AS, Lambkin-Williams R et al. 2012. Use of a human influenza challenge model to assess person-to-person transmission: proof-of-concept study. J. Infect. Dis. 205:35–43
    [Google Scholar]
  54. 54.
    Nguyen TQ, Rollon R, Choi YK. 2021. Animal models for influenza research: strengths and weaknesses. Viruses 13:1011
    [Google Scholar]
  55. 55.
    O'Donnell CD, Subbarao K. 2011. The contribution of animal models to the understanding of the host range and virulence of influenza A viruses. Microbes Infect. 13:502–15
    [Google Scholar]
  56. 56.
    Lowen AC, Mubareka S, Tumpey TM, Garcia-Sastre A, Palese P. 2006. The guinea pig as a transmission model for human influenza viruses. PNAS 103:9988–92
    [Google Scholar]
  57. 57.
    Schulman JL, Kilbourne ED. 1963. Experimental transmission of influenza virus infection in mice: II. Some factors affecting the incidence of transmitted infection. J. Exp. Med. 118:267–75
    [Google Scholar]
  58. 58.
    Steel J, Lowen AC, Mubareka S, Palese P. 2009. Transmission of influenza virus in a mammalian host is increased by PB2 amino acids 627K or 627E/701N. PLOS Pathog. 5:e1000252
    [Google Scholar]
  59. 59.
    Steel J, Staeheli P, Mubareka S, Garcia-Sastre A, Palese P, Lowen AC. 2010. Transmission of pandemic H1N1 influenza virus and impact of prior exposure to seasonal strains or interferon treatment. J. Virol. 84:21–26
    [Google Scholar]
  60. 60.
    Steel J, Palese P, Lowen AC 2011. Transmission of a 2009 pandemic influenza virus shows a sensitivity to temperature and humidity similar to that of an H3N2 seasonal strain. J. Virol. 85:1400–2
    [Google Scholar]
  61. 61.
    Pica N, Chou YY, Bouvier NM, Palese P. 2012. Transmission of influenza B viruses in the guinea pig. J. Virol. 86:4279–87
    [Google Scholar]
  62. 62.
    Mubareka S, Lowen AC, Steel J, Coates AL, Garcia-Sastre A, Palese P. 2009. Transmission of influenza virus via aerosols and fomites in the guinea pig model. J. Infect. Dis. 199:858–65
    [Google Scholar]
  63. 63.
    Bouvier NM, Rahmat S, Pica N. 2012. Enhanced mammalian transmissibility of seasonal influenza A/H1N1 viruses encoding an oseltamivir-resistant neuraminidase. J. Virol. 86:7268–79
    [Google Scholar]
  64. 64.
    Danzy S, Lowen AC, Steel J. 2021. A quantitative approach to assess influenza A virus fitness and transmission in guinea pigs. J. Virol. 95:11e02320–20
    [Google Scholar]
  65. 65.
    Van Hoeven N, Belser JA, Szretter KJ, Zeng H, Staeheli P et al. 2009. Pathogenesis of 1918 pandemic and H5N1 influenza virus infections in a guinea pig model: antiviral potential of exogenous alpha interferon to reduce virus shedding. J. Virol. 83:2851–61
    [Google Scholar]
  66. 66.
    Jayaraman A, Chandrasekaran A, Viswanathan K, Raman R, Fox JG, Sasisekharan R. 2012. Decoding the distribution of glycan receptors for human-adapted influenza A viruses in ferret respiratory tract. PLOS ONE 7:e27517
    [Google Scholar]
  67. 67.
    van Riel D, Munster VJ, de Wit E, Rimmelzwaan GF, Fouchier RA et al. 2007. Human and avian influenza viruses target different cells in the lower respiratory tract of humans and other mammals. Am. J. Pathol. 171:1215–23
    [Google Scholar]
  68. 68.
    Belser JA, Katz JM, Tumpey TM. 2011. The ferret as a model organism to study influenza A virus infection. Dis. Model Mech. 4:575–79
    [Google Scholar]
  69. 69.
    Le Sage V, Jones JE, Kormuth KA, Fitzsimmons WJ, Nturibi E et al. 2021. Pre-existing heterosubtypic immunity provides a barrier to airborne transmission of influenza viruses. PLOS Pathog. 17:e1009273
    [Google Scholar]
  70. 70.
    Roberts KL, Shelton H, Stilwell P, Barclay WS. 2012. Transmission of a 2009 H1N1 pandemic influenza virus occurs before fever is detected, in the ferret model. PLOS ONE 7:e43303
    [Google Scholar]
  71. 71.
    Koster F, Gouveia K, Zhou Y, Lowery K, Russell R et al. 2012. Exhaled aerosol transmission of pandemic and seasonal H1N1 influenza viruses in the ferret. PLOS ONE 7:e33118
    [Google Scholar]
  72. 72.
    Linster M, van Boheemen S, de Graaf M, Schrauwen EJ, Lexmond P et al. 2014. Identification, characterization, and natural selection of mutations driving airborne transmission of A/H5N1 virus. Cell 157:329–39
    [Google Scholar]
  73. 73.
    Sutton TC, Lamirande EW, Patel DR, Johnson KEE, Czako R et al. 2022. Sequential transmission of influenza viruses in ferrets does not enhance infectivity and does not predict transmissibility in humans. mBio 13:e0254022
    [Google Scholar]
  74. 74.
    Buhnerkempe MG, Gostic K, Park M, Ahsan P, Belser JA, Lloyd-Smith JO. 2015. Mapping influenza transmission in the ferret model to transmission in humans. eLife 4:e07969
    [Google Scholar]
  75. 75.
    Cox NJ, Trock SC, Burke SA. 2014. Pandemic preparedness and the Influenza Risk Assessment Tool (IRAT). Curr. Top. Microbiol. Immunol. 385:119–36
    [Google Scholar]
  76. 76.
    World Health Organ 2016. Tool for Influenza Pandemic Risk Assessment (TIPRA) Geneva: World Health Organ.
  77. 77.
    Frise R, Bradley K, van Doremalen N, Galiano M, Elderfield RA et al. 2016. Contact transmission of influenza virus between ferrets imposes a looser bottleneck than respiratory droplet transmission allowing propagation of antiviral resistance. Sci. Rep. 6:29793
    [Google Scholar]
  78. 78.
    Lakdawala SS, Subbarao K. 2012. The ongoing battle against influenza: the challenge of flu transmission. Nat. Med. 18:1468–70
    [Google Scholar]
  79. 79.
    Kutter JS, de Meulder D, Bestebroer TM, Lexmond P, Mulders A et al. 2021. SARS-CoV and SARS-CoV-2 are transmitted through the air between ferrets over more than one meter distance. Nat. Commun. 12:1653
    [Google Scholar]
  80. 80.
    Andrewes CH, Glover RE. 1941. Spread of infection from the respiratory tract of the ferret. I. Transmission of influenza A virus. Br. J. Exp. Pathol. 22:91–97
    [Google Scholar]
  81. 81.
    Schulman JL, Kilbourne ED. 1962. Airborne transmission of influenza virus infection in mice. Nature 195:1129–30
    [Google Scholar]
  82. 82.
    Belser JA, Pulit-Penaloza JA, Maines TR. 2020. Ferreting out influenza virus pathogenicity and transmissibility: past and future risk assessments in the ferret model. Cold Spring Harb. . Perspect. Med. 10:7a038323
    [Google Scholar]
  83. 83.
    Herfst S, Schrauwen EJ, Linster M, Chutinimitkul S, de Wit E et al. 2012. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336:1534–41
    [Google Scholar]
  84. 84.
    Imai M, Watanabe T, Hatta M, Das SC, Ozawa M et al. 2012. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 486:420–28
    [Google Scholar]
  85. 85.
    Lakdawala SS, Lamirande EW, Suguitan AL Jr., Wang W, Santos CP et al. 2011. Eurasian-origin gene segments contribute to the transmissibility, aerosol release, and morphology of the 2009 pandemic H1N1 influenza virus. PLOS Pathog. 7:e1002443
    [Google Scholar]
  86. 86.
    Sorrell EM, Wan H, Araya Y, Song H, Perez DR. 2009. Minimal molecular constraints for respiratory droplet transmission of an avian-human H9N2 influenza A virus. PNAS 106:7565–70
    [Google Scholar]
  87. 87.
    Houser KV, Pearce MB, Katz JM, Tumpey TM. 2013. Impact of prior seasonal H3N2 influenza vaccination or infection on protection and transmission of emerging variants of influenza A(H3N2)v virus in ferrets. J. Virol. 87:13480–89
    [Google Scholar]
  88. 88.
    Lowen AC, Steel J, Mubareka S, Carnero E, Garcia-Sastre A, Palese P. 2009. Blocking interhost transmission of influenza virus by vaccination in the guinea pig model. J. Virol. 83:2803–18
    [Google Scholar]
  89. 89.
    Oh DY, Lowther S, McCaw JM, Sullivan SG, Leang SK et al. 2014. Evaluation of oseltamivir prophylaxis regimens for reducing influenza virus infection, transmission and disease severity in a ferret model of household contact. J. Antimicrob. Chemother. 69:2458–69
    [Google Scholar]
  90. 90.
    Paules CI, Lakdawala S, McAuliffe JM, Paskel M, Vogel L et al. 2017. The hemagglutinin A stem antibody MEDI8852 prevents and controls disease and limits transmission of pandemic influenza viruses. J. Infect. Dis. 216:3356–65
    [Google Scholar]
  91. 91.
    Lee LYY, Zhou J, Frise R, Goldhill DH, Koszalka P et al. 2020. Baloxavir treatment of ferrets infected with influenza A(H1N1)pdm09 virus reduces onward transmission. PLOS Pathog. 16:e1008395
    [Google Scholar]
  92. 92.
    Richard M, Schrauwen EJ, de Graaf M, Bestebroer TM, Spronken MI et al. 2013. Limited airborne transmission of H7N9 influenza A virus between ferrets. Nature 501:560–63
    [Google Scholar]
  93. 93.
    Sun X, Pulit-Penaloza JA, Belser JA, Pappas C, Pearce MB et al. 2018. Pathogenesis and transmission of genetically diverse swine-origin H3N2 variant influenza A viruses from multiple lineages isolated in the United States, 2011–2016. J. Virol. 92:e00665–18
    [Google Scholar]
  94. 94.
    Belser JA, Barclay W, Barr I, Fouchier RAM, Matsuyama R et al. 2018. Ferrets as models for influenza virus transmission studies and pandemic risk assessments. Emerg. Infect. Dis. 24:965–71
    [Google Scholar]
  95. 95.
    Belser JA, Lau EHY, Barclay W, Barr IG, Chen H et al. 2022. Robustness of the ferret model for influenza risk assessment studies: a cross-laboratory exercise. mBio 13:e0117422
    [Google Scholar]
  96. 96.
    Mukherjee DV, Cohen B, Bovino ME, Desai S, Whittier S, Larson EL. 2012. Survival of influenza virus on hands and fomites in community and laboratory settings. Am. J. Infect. Control 40:590–94
    [Google Scholar]
  97. 97.
    Greatorex JS, Digard P, Curran MD, Moynihan R, Wensley H et al. 2011. Survival of influenza A(H1N1) on materials found in households: implications for infection control. PLOS ONE 6:e27932
    [Google Scholar]
  98. 98.
    Perry KA, Coulliette AD, Rose LJ, Shams AM, Edwards JR, Noble-Wang JA. 2016. Persistence of influenza A (H1N1) virus on stainless steel surfaces. Appl. Environ. Microbiol. 82:3239–45
    [Google Scholar]
  99. 99.
    Thompson KA, Bennett AM. 2017. Persistence of influenza on surfaces. J. Hosp. Infect. 95:194–99
    [Google Scholar]
  100. 100.
    Thomas Y, Vogel G, Wunderli W, Suter P, Witschi M et al. 2008. Survival of influenza virus on banknotes. Appl. Environ. Microbiol. 74:3002–7
    [Google Scholar]
  101. 101.
    Bean B, Moore BM, Sterner B, Peterson LR, Gerding DN, Balfour HH Jr. 1982. Survival of influenza viruses on environmental surfaces. J. Infect. Dis. 146:47–51
    [Google Scholar]
  102. 102.
    Yang W, Elankumaran S, Marr LC. 2012. Relationship between humidity and influenza A viability in droplets and implications for influenza's seasonality. PLOS ONE 7:e46789
    [Google Scholar]
  103. 103.
    Noyce JO, Michels H, Keevil CW. 2007. Inactivation of influenza A virus on copper versus stainless steel surfaces. Appl. Environ. Microbiol. 73:2748–50
    [Google Scholar]
  104. 104.
    O'Brien FEM. 1948. The control of humidity by saturated salt solutions. J. Sci. Instrum. 25:73
    [Google Scholar]
  105. 105.
    Harper GJ. 1961. Airborne micro-organisms: survival tests with four viruses. J. Hyg. 59:479–86
    [Google Scholar]
  106. 106.
    Hood AM. 1963. Infectivity of influenza virus aerosols. J. Hyg. 61:331–35
    [Google Scholar]
  107. 107.
    Shephard RJ, Shek PN. 1998. Cold exposure and immune function. Can. J. Physiol. Pharmacol. 76:828–36
    [Google Scholar]
  108. 108.
    Goldberg LJ, Watkins HM, Boerke EE, Chatigny MA. 1958. The use of a rotating drum for the study of aerosols over extended periods of time. Am. J. Hyg. 68:85–93
    [Google Scholar]
  109. 109.
    Kormuth KA, Lin K, Prussin AJ 2nd, Vejerano EP, Tiwari AJ et al. 2018. Influenza virus infectivity is retained in aerosols and droplets independent of relative humidity. J. Infect. Dis. 218:739–47
    [Google Scholar]
  110. 110.
    French AJ, Longest AK, Pan J, Vikesland PJ, Duggal NK et al. 2022. Environmental stability of enveloped viruses is impacted by the initial volume and evaporation kinetics of droplets. bioRxiv 2022.07.26.501658. https://doi.org/10.1101/2022.07.26.501658
  111. 111.
    Lester W Jr. 1948. The influence of relative humidity on the infectivity of air-borne influenza A virus, PR8 strain. J. Exp. Med. 88:361–68
    [Google Scholar]
  112. 112.
    Shaman J, Goldstein E, Lipsitch M. 2011. Absolute humidity and pandemic versus epidemic influenza. Am. J. Epidemiol. 173:127–35
    [Google Scholar]
  113. 113.
    Shaman J, Pitzer VE, Viboud C, Grenfell BT, Lipsitch M. 2010. Absolute humidity and the seasonal onset of influenza in the continental United States. PLOS Biol. 8:e1000316
    [Google Scholar]
  114. 114.
    Tamerius J, Perzanowski M, Acosta L, Jacobson J, Goldstein I et al. 2013. Socioeconomic and outdoor meteorological determinants of indoor temperature and humidity in New York City dwellings. Weather Clim. Soc. 5:168–79
    [Google Scholar]
  115. 115.
    Morris DH, Yinda KC, Gamble A, Rossine FW, Huang Q et al. 2021. Mechanistic theory predicts the effects of temperature and humidity on inactivation of SARS-CoV-2 and other enveloped viruses. eLife 10:e65902
    [Google Scholar]
  116. 116.
    Kudo E, Song E, Yockey LJ, Rakib T, Wong PW et al. 2019. Low ambient humidity impairs barrier function and innate resistance against influenza infection. PNAS 116:10905–10
    [Google Scholar]
  117. 117.
    Ben-Aryeh H, Shalev A, Szargel R, Laor A, Laufer D, Gutman D. 1986. The salivary flow rate and composition of whole and parotid resting and stimulated saliva in young and old healthy subjects. Biochem. Med. Metab. Biol. 36:260–65
    [Google Scholar]
  118. 118.
    Ben-Aryeh H, Fisher M, Szargel R, Laufer D. 1990. Composition of whole unstimulated saliva of healthy children: changes with age. Arch. Oral Biol. 35:929–31
    [Google Scholar]
  119. 119.
    Bredberg A, Gobom J, Almstrand AC, Larsson P, Blennow K et al. 2012. Exhaled endogenous particles contain lung proteins. Clin. Chem. 58:431–40
    [Google Scholar]
  120. 120.
    Reynolds HY, Chrétien J. 1984. Respiratory tract fluids: analysis of content and contemporary use in understanding lung diseases. Dis. Mon. 30:51–103
    [Google Scholar]
  121. 121.
    Gralton J, Tovey E, McLaws ML, Rawlinson WD. 2011. The role of particle size in aerosolised pathogen transmission: a review. J. Infect. 62:1–13
    [Google Scholar]
  122. 122.
    Tada A, Senpuku H. 2021. The impact of oral health on respiratory viral infection. Dent. J. 9:443
    [Google Scholar]
  123. 123.
    Zanin M, Baviskar P, Webster R, Webby R. 2016. The interaction between respiratory pathogens and mucus. Cell Host Microbe 19:159–68
    [Google Scholar]
  124. 124.
    Rowe HM, Livingston B, Margolis E, Davis A, Meliopoulos VA et al. 2020. Respiratory bacteria stabilize and promote airborne transmission of influenza A virus. mSystems 5:5e00762–20
    [Google Scholar]
  125. 125.
    Mueller Brown K, Le Sage V, French AJ, Jones JE, Padovani GH et al. 2022. Secondary infection with Streptococcus pneumoniae decreases influenza virus replication and is linked to severe disease. FEMS Microbes 3:xtac007
    [Google Scholar]
  126. 126.
    Klein LK, Luo B, Bluvshtein N, Krieger UK, Schaub A et al. 2022. Expiratory aerosol pH is determined by indoor room trace gases and particle size. PNAS 119:e2212140119
    [Google Scholar]
  127. 127.
    Maeda T, Ohnishi S. 1980. Activation of influenza virus by acidic media causes hemolysis and fusion of erythrocytes. FEBS Lett. 122:283–87
    [Google Scholar]
  128. 128.
    Wei H, Vejerano EP, Leng W, Huang Q, Willner MR et al. 2018. Aerosol microdroplets exhibit a stable pH gradient. PNAS 115:287272–77
    [Google Scholar]
  129. 129.
    Gostic KM, Ambrose M, Worobey M, Lloyd-Smith JO. 2016. Potent protection against H5N1 and H7N9 influenza via childhood hemagglutinin imprinting. Science 354:722–26
    [Google Scholar]
  130. 130.
    Francis ME, McNeil M, Dawe NJ, Foley MK, King ML et al. 2019. Historical H1N1 influenza virus imprinting increases vaccine protection by influencing the activity and sustained production of antibodies elicited at vaccination in ferrets. Vaccines 7:4133
    [Google Scholar]
  131. 131.
    Hancock K, Veguilla V, Lu X, Zhong W, Butler EN et al. 2009. Cross-reactive antibody responses to the 2009 pandemic H1N1 influenza virus. N. Engl. J. Med. 361:1945–52
    [Google Scholar]
  132. 132.
    Itoh Y, Shinya K, Kiso M, Watanabe T, Sakoda Y et al. 2009. In vitro and in vivo characterization of new swine-origin H1N1 influenza viruses. Nature 460:1021–25
    [Google Scholar]
  133. 133.
    Skountzou I, Koutsonanos DG, Kim JH, Powers R, Satyabhama L et al. 2010. Immunity to pre-1950 H1N1 influenza viruses confers cross-protection against the pandemic swine-origin 2009 A (H1N1) influenza virus. J. Immunol. 185:1642–49
    [Google Scholar]
  134. 134.
    Ellebedy AH, Ducatez MF, Duan S, Stigger-Rosser E, Rubrum AM et al. 2011. Impact of prior seasonal influenza vaccination and infection on pandemic A (H1N1) influenza virus replication in ferrets. Vaccine 29:3335–39
    [Google Scholar]
  135. 135.
    Alford RH, Kasel JA, Gerone PJ, Knight V. 1966. Human influenza resulting from aerosol inhalation. Proc. Soc. Exp. Biol. Med. 122:800–4
    [Google Scholar]
  136. 136.
    Han A, Czajkowski LM, Donaldson A, Baus HA, Reed SM et al. 2019. A dose-finding study of a wild-type influenza A(H3N2) virus in a healthy volunteer human challenge model. Clin. Infect. Dis. 69:2082–90
    [Google Scholar]
  137. 137.
    Cowling BJ, Zhou Y, Ip DK, Leung GM, Aiello AE. 2010. Face masks to prevent transmission of influenza virus: a systematic review. Epidemiol. Infect. 138:449–56
    [Google Scholar]
  138. 138.
    Johnson DF, Druce JD, Birch C, Grayson ML. 2009. A quantitative assessment of the efficacy of surgical and N95 masks to filter influenza virus in patients with acute influenza infection. Clin. Infect. Dis. 49:275–77
    [Google Scholar]
  139. 139.
    Asadi S, Cappa CD, Barreda S, Wexler AS, Bouvier NM, Ristenpart WD. 2020. Efficacy of masks and face coverings in controlling outward aerosol particle emission from expiratory activities. Sci. Rep. 10:15665
    [Google Scholar]
  140. 140.
    Zhou J, Wei J, Choy KT, Sia SF, Rowlands DK et al. 2018. Defining the sizes of airborne particles that mediate influenza transmission in ferrets. PNAS 115:E2386–92
    [Google Scholar]
  141. 141.
    Atkinson J, Chartier Y, Pessoa-Silva CL, Jensen P, Li Y, Seto WH, eds. 2009. Natural Ventilation for Infection Control in Health-Care Settings Geneva: World Health Org.
  142. 142.
    Li Y, Leung GM, Tang JW, Yang X, Chao CY et al. 2007. Role of ventilation in airborne transmission of infectious agents in the built environment—a multidisciplinary systematic review. Indoor Air 17:2–18
    [Google Scholar]
  143. 143.
    McDevitt JJ, Rudnick SN, Radonovich LJ. 2012. Aerosol susceptibility of influenza virus to UV-C light. Appl. Environ. Microbiol. 78:1666–69
    [Google Scholar]
  144. 144.
    McLean RL. 1961. General discussion: the mechanism of spread of Asian influenza. Am. Rev. Respir. Dis. 83:36–38
    [Google Scholar]
  145. 145.
    Fischer RJ, Port JR, Holbrook MG, Yinda KC, Creusen M et al. 2022. UV-C light completely blocks aerosol transmission of highly contagious SARS-CoV-2 variants WA1 and Delta in hamsters. Environ. Sci. Technol. 56:12424–30
    [Google Scholar]
  146. 146.
    Chan L, Alizadeh K, Alizadeh K, Fazel F, Kakish JE et al. 2021. Review of influenza virus vaccines: the qualitative nature of immune responses to infection and vaccination is a critical consideration. Vaccines 9:979
    [Google Scholar]
  147. 147.
    Walter K. 2020. Influenza vaccine. JAMA 324:1476
    [Google Scholar]
  148. 148.
    Reichert TA, Sugaya N, Fedson DS, Glezen WP, Simonsen L, Tashiro M. 2001. The Japanese experience with vaccinating schoolchildren against influenza. N. Engl. J. Med. 344:889–96
    [Google Scholar]
  149. 149.
    Tsang TK, Wang C, Fang VJ, Perera R, So HC et al. 2022. Indirect protection from vaccinating children against influenza A virus infection in households. Viruses 14:2097
    [Google Scholar]
  150. 150.
    Baz M, Boonnak K, Paskel M, Santos C, Powell T et al. 2015. Nonreplicating influenza A virus vaccines confer broad protection against lethal challenge. mBio 6:e01487–15
    [Google Scholar]
  151. 151.
    Arevalo CP, Bolton MJ, Le Sage V, Ye N, Furey C et al. 2022. A multivalent nucleoside-modified mRNA vaccine against all known influenza virus subtypes. Science 378:899–904
    [Google Scholar]
  152. 152.
    Dolin R, Reichman RC, Madore HP, Maynard R, Linton PN, Webber-Jones J. 1982. A controlled trial of amantadine and rimantadine in the prophylaxis of influenza A infection. N. Engl. J. Med. 307:580–84
    [Google Scholar]
  153. 153.
    Sears SD, Clements ML. 1987. Protective efficacy of low-dose amantadine in adults challenged with wild-type influenza A virus. Antimicrob. Agents Chemother. 31:1470–73
    [Google Scholar]
  154. 154.
    Dong G, Peng C, Luo J, Wang C, Han L et al. 2015. Adamantane-resistant influenza A viruses in the world (1902–2013): frequency and distribution of M2 gene mutations. PLOS ONE 10:e0119115
    [Google Scholar]
  155. 155.
    Wutzler P, Kossow KD, Lode H, Ruf BR, Scholz H et al. 2004. Antiviral treatment and prophylaxis of influenza in primary care: German recommendations. J. Clin. Virol. 31:84–91
    [Google Scholar]
  156. 156.
    Welliver R, Monto AS, Carewicz O, Schatteman E, Hassman M et al. 2001. Effectiveness of oseltamivir in preventing influenza in household contacts: a randomized controlled trial. JAMA 285:748–54
    [Google Scholar]
  157. 157.
    Lee VJ, Yap J, Cook AR, Chen MI, Tay JK et al. 2010. Oseltamivir ring prophylaxis for containment of 2009 H1N1 influenza outbreaks. N. Engl. J. Med. 362:2166–74
    [Google Scholar]
  158. 158.
    Hayden FG, Asher J, Cowling BJ, Hurt AC, Ikematsu H et al. 2022. Reducing influenza virus transmission: the potential value of antiviral treatment. Clin. Infect. Dis. 74:532–40
    [Google Scholar]
  159. 159.
    Komeda T, Takazono T, Hosogaya N, Ogura E, Fujiwara M et al. 2021. Comparison of household transmission of influenza virus from index patients treated with baloxavir marboxil or neuraminidase inhibitors: a health insurance claims database study. Clin. Infect. Dis. 72:e859–67
    [Google Scholar]
  160. 160.
    Schrauwen EJ, Fouchier RA. 2014. Host adaptation and transmission of influenza A viruses in mammals. Emerg. Microbes Infect. 3:e9
    [Google Scholar]
  161. 161.
    Belser JA, Maines TR, Tumpey TM, Katz JM. 2010. Influenza A virus transmission: contributing factors and clinical implications. Expert Rev. Mol. Med. 12:e39
    [Google Scholar]
  162. 162.
    Tumpey TM, Maines TR, Van Hoeven N, Glaser L, Solorzano A et al. 2007. A two-amino acid change in the hemagglutinin of the 1918 influenza virus abolishes transmission. Science 315:655–59
    [Google Scholar]
  163. 163.
    Russier M, Yang G, Rehg JE, Wong SS, Mostafa HH et al. 2016. Molecular requirements for a pandemic influenza virus: an acid-stable hemagglutinin protein. PNAS 113:1636–41
    [Google Scholar]
  164. 164.
    Zhou B, Pearce MB, Li Y, Wang J, Mason RJ et al. 2013. Asparagine substitution at PB2 residue 701 enhances the replication, pathogenicity, and transmission of the 2009 pandemic H1N1 influenza A virus. PLOS ONE 8:e67616
    [Google Scholar]
  165. 165.
    Van Hoeven N, Pappas C, Belser JA, Maines TR, Zeng H et al. 2009. Human HA and polymerase subunit PB2 proteins confer transmission of an avian influenza virus through the air. PNAS 106:3366–71
    [Google Scholar]
  166. 166.
    Chou YY, Albrecht RA, Pica N, Lowen AC, Richt JA et al. 2011. The M segment of the 2009 new pandemic H1N1 influenza virus is critical for its high transmission efficiency in the guinea pig model. J. Virol. 85:2111235–41
    [Google Scholar]
  167. 167.
    Jia N, Barclay WS, Roberts K, Yen HL, Chan RW et al. 2014. Glycomic characterisation of respiratory tract tissues of ferrets: implications for its use in influenza virus infection studies. J. Biol. Chem. 289:4128489–504
    [Google Scholar]
  168. 168.
    Walther T, Karamanska R, Chan RW, Chan MC, Jia N et al. 2013. Glycomic analysis of human respiratory tract tissues and correlation with influenza virus infection. PLOS Pathog. 9:e1003223
    [Google Scholar]
  169. 169.
    Tran TH, Nguyen TL, Nguyen TD, Luong TS, Pham PM et al. 2004. Avian influenza A (H5N1) in 10 patients in Vietnam. N. Engl. J. Med. 350:1179–88
    [Google Scholar]
  170. 170.
    Zitzow LA, Rowe T, Morken T, Shieh WJ, Zaki S, Katz JM. 2002. Pathogenesis of avian influenza A (H5N1) viruses in ferrets. J. Virol. 76:4420–29
    [Google Scholar]
  171. 171.
    Bolton MJ, Ort JT, McBride R, Swanson NJ, Wilson J et al. 2022. Antigenic and virological properties of an H3N2 variant that continues to dominate the 2021–22 Northern Hemisphere influenza season. Cell Rep. 39:110897
    [Google Scholar]
  172. 172.
    Adam DC, Wu P, Wong JY, Lau EHY, Tsang TK et al. 2020. Clustering and superspreading potential of SARS-CoV-2 infections in Hong Kong. Nat. Med. 26:1714–19
    [Google Scholar]
  173. 173.
    Lakdawala SS, Menachery VD. 2021. Catch me if you can: superspreading of COVID-19. Trends Microbiol. 29:919–29
    [Google Scholar]
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