Influenza virus infectivity is retained in aerosols and droplets independent of relative humidity

Journal of Infectious Diseases

Volumn 218, Issue 5, 2018, Pages 739-747

  Kormuth, Karen A ^a   Lin, Kaisen ^b   Prussin, Aaron J ^b   Vejerano, Eric P ^c   Tiwari, Andrea J ^b   Cox, Steve S ^b   Myerburg, Michael M ^a   Lakdawala, Seema S ^a   Marr, Linsey C ^b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b Virginia Polytechnic Institute and State University   (United States)

^c UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Aerosol; Influenza virus; Mucus; Relative humidity; Respiratory airway cells; Rotating drum; Transmission

Indexed keywords

AEROSOL; AIRBORNE VIRUS; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENVIRONMENTAL FACTOR; ENVIRONMENTAL IMPACT; EXTRACELLULAR MATRIX; GRAVITY; HBEC CELL LINE (BRONCHIAL EPITHELIUM); HUMAN; HUMAN CELL; HUMIDITY; INFLUENZA A VIRUS (H1N1); MDCK CELL LINE; NONHUMAN; PRIORITY JOURNAL; STATIONARY DROPLET; SURVIVAL ANALYSIS; VIRUS ENVELOPE; VIRUS INFECTIVITY; VIRUS LOAD; VIRUS TRANSMISSION; VIRUS VIABILITY; CELL CULTURE; ENVIRONMENTAL EXPOSURE; EPITHELIUM CELL; MICROBIAL VIABILITY; PHYSIOLOGY; TIME FACTOR; VIROLOGY;

AEROSOLS; CELLS, CULTURED; ENVIRONMENTAL EXPOSURE; EPITHELIAL CELLS; HUMANS; HUMIDITY; INFLUENZA A VIRUS, H1N1 SUBTYPE; MICROBIAL VIABILITY; TIME FACTORS;

EID: 85055003486     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jiy221     Document Type: Article

References (50)

1. Lakdawala SS, Subbarao K. The ongoing battle against influenza: The challenge of flu transmission. Nat Med 2012; 18:1468-70.
2. Lindsley WG, Blachere FM, Beezhold DH, et al. Viable influenza A virus in airborne particles expelled during coughs versus exhalations. Influenza Other Respir Viruses 2016; 10:404-13.
3. Lindsley WG, Noti JD, Blachere FM, et al. Viable influenza A virus in airborne particles from human coughs. J Occup Environ Hyg 2015; 12:107-13.
4. Milton DK, Fabian MP, Cowling BJ, Grantham ML, McDevitt JJ. Influenza virus aerosols in human exhaled breath: particle size, culturability, and effect of surgical masks. PLoS Pathog 2013; 9:e1003205.
5. Yang W, Marr LC. Dynamics of airborne influenza A viruses indoors and dependence on humidity. PLoS One 2011; 6:e21481.
6. Fabian P, McDevitt JJ, DeHaan WH, et al. Influenza virus in human exhaled breath: an observational study. PLoS One 2008; 3:e2691.
7. Yan J, Grantham M, Pantelic J, et al.; EMIT Consortium. Infectious virus in exhaled breath of symptomatic seasonal influenza cases from a college community. Proc Natl Acad Sci U S A 2018; 115:1081-6.
8. Tang JW. The effect of environmental parameters on the survival of airborne infectious agents. J R Soc Interface 2009; 6(Suppl 6):S737-46.
9. Lowen AC, Mubareka S, Steel J, Palese P. Influenza virus transmission is dependent on relative humidity and temperature. PLoS Pathog 2007; 3:1470-6.
10. Tang JW, Li Y, Eames I, Chan PK, Ridgway GL. Factors involved in the aerosol transmission of infection and control of ventilation in healthcare premises. J Hosp Infect 2006; 64:100-14.
11. Tamerius J, Nelson MI, Zhou SZ, Viboud C, Miller MA, Alonso WJ. Global influenza seasonality: reconciling patterns across temperate and tropical regions. Environ Health Perspect 2011; 119:439-45.
12. Tang JW, Loh TP. Influenza seasonality. Curr Treat Options Infect Dis 2016; 8:343-67.
13. Deyle ER, Maher MC, Hernandez RD, Basu S, Sugihara G. Global environmental drivers of influenza. Proc Natl Acad Sci U S A 2016; 113:13081-6.
14. Shaman J, Goldstein E, Lipsitch M. Absolute humidity and pandemic versus epidemic influenza. Am J Epidemiol 2011; 173:127-35.
15. Shaman J, Kohn M. Absolute humidity modulates influenza survival, transmission, and seasonality. Proc Natl Acad Sci U S A 2009; 106:3243-8.
16. Shaman J, Pitzer VE, Viboud C, Grenfell BT, Lipsitch M. Absolute humidity and the seasonal onset of influenza in the continental United States. PLoS Biol 2010; 8:e1000316.
17. Harper GJ. Airborne micro-organisms: survival tests with four viruses. J Hyg (Lond) 1961; 59:479-86.
18. Hemmes JH, Winkler KC, Kool SM. Virus survival as a seasonal factor in influenza and poliomylitis. Antonie Van Leeuwenhoek 1962; 28:221-33.
19. Hood AM. Infectivity of influenza virus aerosols. J Hyg (Lond) 1963; 61:331-5.
20. Noti JD, Blachere FM, McMillen CM, et al. High humidity leads to loss of infectious influenza virus from simulated coughs. PLoS One 2013; 8:e57485.
21. 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; 51:263-73.
22. 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; 87:128-32.
23. Yang W, Elankumaran S, Marr LC. Relationship between humidity and influenza a viability in droplets and implications for influenza's seasonality. PLoS One 2012; 7:e46789.
24. Parker ER, Wolcott AB, Dunham MD, Mac Neal WJ. Resistance of the Melbourne strain of influenza virus to desiccation. J Lab Clin Med 1943:37-42.
25. Thomas Y, Vogel G, Wunderli W, et al. Survival of influenza virus on banknotes. Appl Environ Microbiol 2008; 74:3002-7.
26. Casado B, Pannell LK, Iadarola P, Baraniuk JN. Identification of human nasal mucous proteins using proteomics. Proteomics 2005; 5:2949-59.
27. Joo NS, Evans IA, Cho HJ, Park IH, Engelhardt JF, Wine JJ. Proteomic analysis of pure human airway gland mucus reveals a large component of protective proteins. PLoS One 2015; 10:e0116756.
28. Goldberg LJ, Watkins HM, Boerke EE, Chatigny MA. The use of a rotating drum for the study of aerosols over extended periods of time. Am J Hyg 1958; 68:85-93.
29. Mitchell CA, Guerin LF, Robillard J. Decay of influenza A viruses of human and avian origin. Can J Comp Med 1968; 32:544-6.
30. Lin K, Marr LC. Aerosolization of Ebola virus surrogates in wastewater systems. Environ Sci Technol 2017; 51:2669-75.
31. Turgeon N, Toulouse MJ, Martel B, Moineau S, Duchaine C. Comparison of five bacteriophages as models for viral aerosol studies. Appl Environ Microbiol 2014; 80:4242-50.
32. Myerburg MM, Harvey PR, Heidrich EM, Pilewski JM, Butterworth MB. Acute regulation of the epithelial sodium channel in airway epithelia by proteases and trafficking. Am J Respir Cell Mol Biol 2010; 43:712-9.
33. Nturibi E, Bhagwat AR, Coburn S, Myerburg MM, Lakdawala SS. Intracellular colocalization of influenza viral RNA and Rab11A is dependent upon microtubule filaments. J Virol 2017; 91.
34. Reed LJ, Muench H. A simple method of estimating fifty per cent endpoints. Am J Hyg 1938; 27:493-7.
35. Breen MS, Breen M, Williams RW, Schultz BD. Predicting residential air exchange rates from questionnaires and meteorology: model evaluation in central North Carolina. Environ Sci Technol 2010; 44:9349-56.
36. Daisey JM, Angell WJ, Apte MG. Indoor air quality, ventilation and health symptoms in schools: an analysis of existing information. Indoor Air 2003; 13:53-64.
37. Murray DM, Burmaster DE. Residential air exchange-rates in the United-States-empirical and estimated parametric distributions by season and climatic region. Risk Anal 1995; 15:459-65.
38. Nazaroff WW. Indoor particle dynamics. Indoor Air 2004; 14(Suppl 7):175-83.
39. Yamamoto N, Shendell DG, Winer AM, Zhang J. Residential air exchange rates in three major US metropolitan areas: results from the Relationship Among Indoor, Outdoor, and Personal Air Study 1999-2001. Indoor Air 2010; 20:85-90.
40. Quadros ME, Marr LC. Silver nanoparticles and total aerosols emitted by nanotechnology-related consumer spray products. Environ Sci Technol 2011; 45:10713-9.
41. Lee N, Chan PK, Hui DS, et al. Viral loads and duration of viral shedding in adult patients hospitalized with influenza. J Infect Dis 2009; 200:492-500.
42. Suess T, Buchholz U, Dupke S, et al. Shedding and transmission of novel influenza virus A/H1N1 infection in households-Germany, 2009. Am J Epidemiol 2010; 171:1157-64.
43. Lakdawala SS, Lamirande EW, Suguitan AL Jr, et al. Eurasianorigin gene segments contribute to the transmissibility, aerosol release, and morphology of the 2009 pandemic H1N1 influenza virus. PLoS Pathog 2011; 7:e1002443.
44. Mubareka S, Lowen AC, Steel J, Coates AL, Garcia-Sastre A, Palese P. Transmission of influenza virus via aerosols and fomites in the guinea pig model. J Infect Dis 2009; 199:858-65.
45. Tellier R. Review of aerosol transmission of influenza A virus. Emerg Infect Dis 2006; 12:1657-62.
46. Cowling BJ, Ip DK, Fang VJ, et al. Aerosol transmission is an important mode of influenza A virus spread. Nat Commun 2013; 4:1935.
47. Vejerano EP, Marr LC. Physico-chemical characteristics of evaporating respiratory fluid droplets. J R Soc Interface 2018; 15.
48. Lakdawala SS, Jayaraman A, Halpin RA, et al. The soft palate is an important site of adaptation for transmissible influenza viruses. Nature 2015; 526:122-5.
49. Halloran SK, Wexler AS, Ristenpart WD. A comprehensive breath plume model for disease transmission via expiratory aerosols. PLoS One 2012; 7:e37088.
50. Lai SK, Wang YY, Wirtz D, Hanes J. Micro-and macrorheology of mucus. Adv Drug Deliv Rev 2009; 61:86-100.