Controversy around airborne versus droplet transmission of respiratory viruses: Implication for infection prevention

Current Opinion in Infectious Diseases

Volumn 32, Issue 4, 2019, Pages 372-379

  Shiu, Eunice Y C ^a   Leung, Nancy H L ^a   Cowling, Benjamin J ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

aerosol; droplet; healthcare settings; infection control; respiratory viruses

Indexed keywords

AEROSOL; AIRBORNE VIRUS; AVIAN INFLUENZA; AVIAN INFLUENZA VIRUS; HUMAN RESPIRATORY SYNCYTIAL VIRUS; INFECTION CONTROL; INFECTION PREVENTION; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; NONHUMAN; RESPIRATORY VIRUS; REVIEW; SEASONAL INFLUENZA; VIRUS TRANSMISSION; ADVERSE EVENT; ANIMAL; CROSS INFECTION; HUMAN; MICROBIOLOGY; PARTICULATE MATTER; RESPIRATORY TRACT INFECTION; VIROLOGY;

AIR MICROBIOLOGY; ANIMALS; CROSS INFECTION; HUMANS; PARTICULATE MATTER; RESPIRATORY TRACT INFECTIONS;

EID: 85068963897     PISSN: 09517375     EISSN: 14736527     Source Type: Journal    
DOI: 10.1097/QCO.0000000000000563     Document Type: Review

References (68)

1. Centers for Disease Control and Prevention. National Hospital Ambulatory Medical Care Survey: 2016 Emergency Department Summary Tables. National Center for Health Statistics, 2016. Available at: https://www. cdc. gov/ nchs/data/nhamcs/web-tables/2016-ed-web-tables. pdf. (Accessed 25 March 2019)
2. World Health Organization. Infection prevention and control of epidemic-and pandemic prone acute respiratory infections in healthcare-WHOguidelines. 2014. Available at: http://www. who. int/csr/bioriskreduction/infection-control/ publication/en/. (Accessed 29 August 2017)
3. Siegel JD, Rhinehart E, Jackson M, et al. 2007 Guideline for isolation precautions:preventing transmission of infectious agents in healthcare settings. Centers for Disease Control and Prevention. 2007. Available at: https:// www. cdc. gov/infectioncontrol/guidelines/isolation/index. html. (Accessed 9 April 2019)
4. Roy CJ, Milton DK. Airborne transmission of communicable infection: the elusive pathway. N Engl J Med 2004; 350:1710-1712.
5. Seto WH. Airborne transmission and precautions: facts and myths. J Hosp Infect 2015; 89:225-228.
6. Tellier R, Li Y, Cowling BJ, et al. Recognition of aerosol transmission of infectious agents: a commentary. BMC Infect Dis 2019; 19:101.
7. Centers for Disease Control and Prevention. Facts about spread of respiratory diseases. How to prevent the spread of respiratory illnesses in disaster evacuation centers. 2019. Available at: https://www. cdc. gov/disasters/disease/ respiratoryic. html. (Accessed 25 March 2019)
8. Brankston G, Gitterman L, Hirji Z, et al. Transmission of influenza A in human beings. Lancet Infect Dis 2007; 7:257-265.
9. Killingley B, Nguyen-Van-Tam J. Routes of influenza transmission. Influenza Other Respir Viruses 2013; 7(Suppl 2):42-51.
10. Hinds. William C. Aerosol technology: properties, behavior, and measurement of airborne particles. Hoboken, New Jersey, USA: John Wiley & Sons; 2012.
11. Liu L, Wei J, Li Y, et al. Evaporation and dispersion of respiratory droplets from coughing. Indoor Air 2017; 27:179-190.
12. Grayson SA, Griffiths PS, Perez MK, et al. Detection of airborne respiratory syncytial virus in a pediatric acute care clinic. Pediatr Pulmonol 2017; 52:684-688.
13. Thomas RJ. Particle size and pathogenicity in the respiratory tract. Virulence 2013; 4:847-858.
14. Alford RH, Kasel JA, Gerone PJ, et al. Human influenza resulting from aerosol inhalation. Proc Soc Exp Biol Med 1966; 122:800-804.
15. Wonderlich ER, Swan ZD, Bissel SJ, et al. Widespread virus replication in alveoli drives acute respiratory distress syndrome in aerosolized H5N1 influenza infection of macaques. J Immunol 2017; 198:1616-1626.
16. Gralton J, Tovey E, McLaws ML, et al. The role of particle size in aerosolised pathogen transmission: a review. J Infect 2011; 62:1-13.
17. Nicas M, Nazaroff WW, Hubbard A. Toward understanding the risk of secondary airborne infection: emission of respirable pathogens. J Occup Environ Hyg 2005; 2:143-154.
18. Tellier R. Aerosol transmission of influenza A virus: a review of new studies. J R Soc Interface 2009; 6(Suppl 6):S783-S790.
19. Moss WJ. Measles. Lancet 2017; 390:2490-2502.
20. Remington PL, Hall WN, Davis IH, et al. Airborne transmission of measles in a physician's office. JAMA 1985; 253:1574-1577.
21. Bloch AB, Orenstein WA, Ewing WM, et al. Measles outbreak in a pediatric practice: airborne transmission in an office setting. Pediatrics 1985; 75:676-683.
22. Fiebelkorn AP, Redd SB, Kuhar DT. Measles in healthcare facilities in the United States during the postelimination era, 2001-2014. Clin Infect Dis 2015; 61:615-618.
23. Lake JG, Luvsansharav UO, Hagan JE, et al. Healthcare-associated measles after a nationwide outbreak in Mongolia. Clin Infect Dis 2018; 67:288-290.
24. George F, Valente J, Augusto GF, et al. Measles outbreak after 12 years without endemic transmission, Portugal, February to May 2017. Euro Surveill 2017; 22:pii: 30548.
25. Hahne SJ, Nic Lochlainn LM, van Burgel ND, et al. Measles outbreak among previously immunized healthcare workers, the Netherlands, 2014. J Infect Dis 2016; 214:1980-1986.
26. Lee CT, Hagan JE, Jantsansengee B, et al. Increase in infant measles deaths during a nationwide measles outbreak-Mongolia, 2015-2016. J Infect Dis 2019.
27. Turgeon N, Hamelin ME, Verreault D, et al. Design and validation with influenza A virus of an aerosol transmission chamber for ferrets. Int J Environ Res Public Health 2019; 16:.
28. Zhou J, Wei J, Choy KT, et al. Defining the sizes of airborne particles that mediate influenza transmission in ferrets. Proc Natl Acad Sci U S A 2018; 115:E2386-E2392.
29. Leung NH, Zhou J, Chu DK, et al. Quantification of Influenza Virus RNA in Aerosols in Patient Rooms. PLoS One 2016; 11:e0148669.
30. Bischoff WE, Swett K, Leng I, et al. Exposure to influenza virus aerosols during routine patient care. J Infect Dis 2013; 207:1037-1046.
31. Lindsley WG, Blachere FM, Davis KA, et al. Distribution of airborne influenza virus and respiratory syncytial virus in an urgent care medical clinic. Clin Infect Dis 2010; 50:693-698.
32. Pan M, Bonny TS, Loeb J, et al. Collection of viable aerosolized influenza virus and other respiratory viruses in a student healthcare center through waterbased condensation growth. mSphere 2017; 2:.
33. Rule AM, Apau O, Ahrenholz SH, et al. Healthcare personnel exposure in an emergency department during influenza season. PLoS One 2018; 13:e0203223.
34. Yan J, Grantham M, Pantelic J, et al. Infectious virus in exhaled breath of symptomatic seasonal influenza cases from a college community. Proc Natl Acad Sci U S A 2018; 115:1081-1086.
35. Lindsley WG, Blachere FM, Thewlis RE, et al. Measurements of airborne influenza virus in aerosol particles from human coughs. PLoS One 2010; 5:e15100.
36. Centers for Disease Control and Prevention. Interim Guidance for Infection Control Within Healthcare Settings When Caring for Confirmed Cases, Probable Cases, and Cases Under Investigation for Infection with Novel Influenza A Viruses Associated with Severe Disease. 2014. Available at: https://www. cdc. gov/flu/avianflu/novel-flu-infection-control. htm. (Accessed 9 April 2019)
37. Wu Y, Shi W, Lin J, et al. Aerosolized avian influenza A (H5N6) virus isolated from a live poultry market, China. J Infect 2017; 74:89-91.
38. Bui VN, Nguyen TT, Nguyen-Viet H, et al. Bioaerosol sampling to detect avian influenza virus in Hanoi's largest live poultry market. Clin Infect Dis 2019; 68:972-975.
39. Torremorell M, Alonso C, Davies PR, et al. Investigation into the airborne dissemination of H5N2 highly pathogenic avian influenza virus during the 2015 spring outbreaks in the Midwestern United States. Avian Dis 2016; 60:637-643.
40. Zeng X, Liu M, Zhang H, et al. Avian influenza H9N2 virus isolated from air samples in LPMs in Jiangxi, China. Virol J 2017; 14:136.
41. Bertran K, Balzli C, Kwon YK, et al. Airborne transmission of highly pathogenic influenza virus during processing of infected poultry. Emerg Infect Dis 2017; 23:1806-1814.
42. Cho SY, Kang JM, Ha YE, et al. MERS-CoV outbreak following a single patient exposure in an emergency room in South Korea: an epidemiological outbreak study. Lancet 2016; 388:994-1001.
43. Fehr AR, Channappanavar R, Perlman S. Middle East respiratory syndrome: emergence of a pathogenic human coronavirus. Annu Rev Med 2017; 68:387-399.
44. Kim KH, Tandi TE, Choi JW, et al. Middle East respiratory syndrome coronavirus (MERS-CoV) outbreak in South Korea, 2015: epidemiology, characteristics and public health implications. J Hosp Infect 2017; 95:207-213.
45. Mackay IM, Arden KE. Middle East respiratory syndrome: an emerging coronavirus infection tracked by the crowd. Virus Res 2015; 202:60-88.
46. Kim SH, Chang SY, Sung M, et al. Extensive Viable Middle East Respiratory Syndrome (MERS) coronavirus contamination in air and surrounding environment in MERS isolation wards. Clin Infect Dis 2016; 63:363-369.
47. World HealthOrganization. Infection prevention and control during healthcare for probable or confirmed cases of Middle East respiratory syndrome coronavirus (MERS-CoV) infection: Interim guidance. 2015. Available at: https:// www. who. int/csr/disease/coronavirus-infections/ipc-mers-cov/en/. (Accessed 8 April 2019)
48. World Health Organization. WHO MERS global summary and assessment of risk. Middle East respiratory syndrome coronavirus (MERS-CoV), 2018. Available at: https://www. who. int/csr/disease/coronavirus-infections/risk-assessment-august-2018. pdf?ua=1. (Accessed 14 April 2019)
49. Centers for Disease Control and Prevention. Interim infection prevention and control recommendations for hospitalized patients with Middle East respiratory syndrome coronavirus (MERS-CoV). 2017. https://www. cdc. gov/coronavirus/ mers/infection-prevention-control. html Accessed 9 April 2019.
50. French CE, McKenzie BC, Coope C, et al. Risk of nosocomial respiratory syncytial virus infection and effectiveness of control measures to prevent transmission events: a systematic review. Influenza Other Respir Viruses 2016; 10:268-290.
51. Centers for Disease Control and Prevention. RSV Transmission. Respiratory Syncytial Virus Infection (RSV), 2018. https://www. cdc. gov/rsv/about/transmission. html Accessed 25 March 2019.
52. Kulkarni H, Smith CM, Lee Ddo H, et al. Evidence of respiratory syncytial virus spread by aerosol. Time to revisit infection control strategies? Am J Respir Crit Care Med 2016; 194:308-316.
53. Ofner M, Lem M, Sarwal S, et al. Cluster of severe acute respiratory syndrome cases among protected health-care workers-Toronto, Canada, April 2003. JAMA 2003; 289:2788-2789
54. MMWR, vol 52, pg 433-436, 2003.
55. O'Neil CA, Li J, Leavey A, et al. Characterization of aerosols generated during patient care activities. Clin Infect Dis 2017; 65:1335-1341.
56. Tran K, Cimon K, Severn M, et al. Aerosol generating procedures and risk of transmission of acute respiratory infections to healthcare workers: a systematic review. PLoS One 2012; 7:e35797.
57. Thompson KA, Pappachan JV, Bennett AM, et al. Influenza aerosols in UK hospitals during the H1N1 (2009) pandemic-the risk of aerosol generation during medical procedures. PLoS One 2013; 8:e56278.
58. Tseng CC, Chang LY, Li CS. Detection of airborne viruses in a pediatrics department measured using real-time qPCR coupled to an air-sampling filter method. J Environ Health 2010; 73:22-28.
59. Mitchell AB, Tang B, Shojaei M, et al. A novel sampling method to detect airborne influenza and other respiratory viruses in mechanically ventilated patients: a feasibility study. Ann Intensive Care 2018; 8:45.
60. Li Y, Wong T, Chung J, et al. In vivo protective performance of N95 respirator and surgical facemask. Am J Ind Med 2006; 49:1056-1065.
61. Qian Y, Willeke K, Grinshpun SA, et al. Performance of N95 respirators: filtration efficiency for airborne microbial and inert particles. Am Ind Hyg Assoc J 1998; 59:128-132.
62. Lee SA, Grinshpun SA, Reponen T. Respiratory performance offered by N95 respirators and surgical masks: human subject evaluation with NaCl aerosol representing bacterial and viral particle size range. Ann Occup Hyg 2008; 52:177-185.
63. Balazy A, Toivola M, Adhikari A, et al. Do N95 respirators provide 95% protection level against airborne viruses, and how adequate are surgical masks? Am J Infect Control 2006; 34:51-57.
64. Smith JD, MacDougall CC, Johnstone J, et al. Effectiveness of N95 respirators versus surgical masks in protecting healthcare workers from acute respiratory infection: a systematic review and meta-analysis. CMAJ 2016; 188:567-574.
65. Atkinson J, Chartier Y, Pessoa-Silva CL, et al. Natural ventilation for infection control in health-care settings: WHO guidelines 2009. 2009. Available at: https://www. who. int/water-sanitation-health/publications/natural-ventilation/ en/. (Accessed 9 April 2019)
66. Gao X, Wei J, Cowling BJ, et al. Potential impact of a ventilation intervention for influenza in the context of a dense indoor contact network in Hong Kong. Sci Total Environ 2016; 569-570:373-381.
67. Centers for Disease Control and Prevention. Prevention Strategies for Seasonal Influenza in Healthcare Settings. Influenza (Flu), 2018. Available at: https://www. cdc. gov/flu/professionals/infectioncontrol/healthcaresettings. htm. (Accessed 14 April 2019)
68. World Health Organization. Frequently asked questions on Middle East respiratory syndrome coronavirus (MERS-CoV). Emergencies preparedness, response, 2019. Available at: https://www. who. int/csr/disease/coronavirus- infections/faq/en/. (Accessed 14 April 2019)