The effect of environmental parameters on the survival of airborne infectious agents

Journal of the Royal Society Interface

Volumn 6, Issue SUPPL. 6, 2009, Pages

  Tang, Julian W ^a  

^a NATIONAL UNIVERSITY HOSPITAL   (Singapore)

Author keywords

Airborne; Bacteria; Fung; Infection control; Transmission; Virus

Indexed keywords

ATMOSPHERIC HUMIDITY; BACTERIOLOGY; DISEASE CONTROL; PATHOGENS; VIRUSES;

AIRBORNE BACTERIA; AIRBORNE INFECTION; AIRBORNE PATHOGENS; ENVIRONMENTAL CONTROL; ENVIRONMENTAL FACTORS; ENVIRONMENTAL PARAMETER; FUNG; INFECTION CONTROL; INFECTIOUS AGENTS; INFECTIOUS DISEASE; TEMPERATURE AND RELATIVE HUMIDITY;

HUMIDITY CONTROL;

VIRUS RNA;

AIRBORNE INFECTION; AIRBORNE MICROORGANISM; BACTERIAL SURVIVAL; DISEASE TRANSMISSION; ENVIRONMENTAL PARAMETERS; HUMAN; HUMIDITY; INFECTION CONTROL; NONHUMAN; REVIEW; TEMPERATURE SENSITIVITY; VIRUS DETECTION; VIRUS SURVIVAL;

FUNGI;

EID: 73449139423     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2009.0227.focus     Document Type: Review

References (95)

1. Arundel, A. V., Sterling, E. M., Biggin, J. H. & Sterling, T. D. 1986 Indirect health effects of relative humidity in indoor environments. Environ. Health Perspect. 65, 351-361. (doi:10.2307/3430203)
2. Basilico Mde, L., Chiericatti, C., Aringoli, E. E., Althaus, R. L. & Basilico, J. C. 2007 Influence of environmental factors on airborne fungi in houses of Santa Fe City, Argentina. Sci. Total Environ. 376, 143-150. (doi:10.1016/j.scitotenv.2007.01.001)
3. Bernstein, J. A., Levin, L., Crandall, M. S., Perez, A. & Lanphear, B. 2005 A pilot study to investigate the effects of combined dehumidification and HEPA filtration on dew point and airborne mold spore counts in day care centers. Indoor Air 15, 402-407. (doi:10.1111/j.1600-0668.2005. 00379.x)
4. Blachere, F. M., Lindsley, W. G., Slaven, J. E., Green, B. J., Anderson, S. E., Chen, B. T. & Beezhold, D. H. 2007 Bioaerosol sampling for the detection of aerosolized influenza virus. Influenza Other Respir. Viruses 1, 113-120. (doi:10.1111/j.1750-2659.2007.00020.x)
5. Blachere, F. M. et al. 2009 Measurement of airborne influenza virus in a hospital emergency department. Clin. Infect. Dis. 48, 438-440. (doi:10.1086/596478)
6. Bolister, N. J., Johnson, H. E. &Wathes, C. M. 1992 The ability of airborne Klebsiella pneumoniae to colonize mouse lungs. Epidemiol. Infect. 109, 121-131.
7. Bridges, C. B., Kuehnert, M. J. & Hall, C. B. 2003 Transmission of influenza: implications for control in health care settings. Clin. Infect. Dis. 37, 1094-1101. (doi:10.1086/378292)
8. Burch, M. & Levetin, E. 2002 Effects of meteorological conditions on spore plumes. Int. J. Biometeorol. 46, 107-117. (doi:10.1007/s00484-002-0127-1)
9. Burge, H. A., Pierson, D. L., Groves, T. O., Strawn, K. F. & Mishra, S. K. 2000 Dynamics of airborne fungal populations in a large office building. Curr. Microbiol. 40, 10-16. (doi:10.1007/s002849910003)
10. Cox, C. S. 1970 Aerosol survival of Escherichia coli B disseminated from the dry state. Appl. Microbiol. 19, 604-607.
11. Cox, C. S. 1971 Aerosol survival of Pasteurella tularensis disseminated from the wet and dry states. Appl. Microbiol. 21, 482-486.
12. Cox, C. S. 1989 Airborne bacteria and viruses. Sci. Prog. 73, 469-499.
13. Cox, C. S. 1998 The microbiology of air. In Topley & Wilson's microbiology and microbial infections (eds L. Collier, A. Balows & M. Sussman), pp. 339-350, 9th edn. London, UK: Arnold, Oxford University Press.
14. Dennis, P. J. & Lee, J. V. 1988 Differences in aerosol survival between pathogenic and non-pathogenic strains of Legionella pneumophila serogroup 1. J. Appl. Bacteriol. 65, 135-141.
15. Dinter, P. S. & Muller, W. 1984 Tenacity of bacteria in the airborne state. III. Model studies on the epidemiology of Pasteurella multocida influenced by a tropical climate. Zentralbl. Bakteriol. Mikrobiol. Hyg. B 179, 139-150.
16. Dinter, P. S. & Muller, W. 1988 The tenacity of bacteria in the airborne state. VI. Tenacity of airborne S. senftenberg. Zentralbl. Bakteriol. Mikrobiol. Hyg. B 186, 278-288.
17. Dunklin, E. W. & Puck, T. T. 1948 The lethal effect of relative humidity on air-borne bacteria. J. Exp. Med. 87, 87-101. (doi:10.1084/jem.87.2.87)
18. Ehrlich, R. & Miller, S. 1973 Survival of airborne Pasteurella tularensis at different atmospheric temperatures. Appl. Microbiol. 25, 369-372.
19. Ehrlich, R., Miller, S. & Walker, R. L. 1970 Relationship between atmospheric temperature and survival of airborne bacteria. Appl. Microbiol. 19, 245-249.
20. Erkara, I. P., Asan, A., Yilmaz, V., Pehlivan, S. & Okten, S. S. 2008 Airborne Alternaria and Cladosporium species and relationship with meteorological conditions in Eskisehir City, Turkey. Environ. Monit. Assess. 144, 31-41.
21. Fabian, P., McDevitt, J. J., DeHaan, W. H., Fung, R. O., Cowling, B. J., Chan, K. H., Leung, G. M. & Milton, D. K. 2008 Influenza virus in human exhaled breath: an observational study. PLoS ONE 3, e2691. (doi:10.1371/journal.pone.0002691)
22. Fang, Z., Ouyang, Z., Zheng, H., Wang, X. & Hu, L. 2007 Culturable airborne bacteria in outdoor environments in Beijing, China. Microb. Ecol. 54, 487-496. (doi:10.1007/s00248-007-9216-3)
23. Garrett, M. H., Rayment, P. R., Hooper, M. A., Abramson, M. J. & Hooper, B. M. 1998 Indoor airborne fungal spores, house dampness and associations with environmental factors and respiratory health in children. Clin. Exp. Allergy 28, 459-467. (doi:10.1046/j.1365-2222.1998. 00255.x)
24. Gorny, R. L. & Dutkiewicz, J. 2002 Bacterial and fungal aerosols in indoor environment in Central and Eastern European countries. Ann. Agric. Environ. Med. 9, 17-23.
25. Gorny, R. L., Dutkiewicz, J. & Krysinska-Traczyk, E. 1999 Size distribution of bacterial and fungal bioaerosols in indoor air. Ann. Agric. Environ. Med. 6, 105-113.
26. Hambleton, P., Broster, M. G., Dennis, P. J., Henstridge, R., Fitzgeorge, R. & Conlan, J. W. 1983 Survival of virulent Legionella pneumophila in aerosols. J. Hyg. (Lond.) 90, 451-460. (doi:10.1017/ S0022172400029090)
27. Handley, B. A. & Webster, A. J. 1993 Some factors affecting airborne survival of Pseudomonas fluorescens indoors. J. Appl. Bacteriol. 75, 35-42.
28. Handley, B. A. & Webster, A. J. 1995 Some factors affecting the airborne survival of bacteria outdoors. J. Appl. Bacteriol. 79, 368-378.
29. Hardin, B. D., Kelman, B. J. & Saxon, A. 2003 Adverse human health effects associated with molds in the indoor environment. J. Occup. Environ. Med. 45, 470-478. (doi:10.1097/00043764-200305000-00006)
30. Harper, G. J. 1961 Airborne micro-organisms: survival tests with four viruses. J. Hyg. (Lond.) 59, 479-486. (doi:10.1017/ S0022172400039176)
31. Hatch, M. T., Wright, D. N. & Bailey, G. D. 1970 Response of airborne Mycoplasma pneumoniae to abrupt changes in relative humidity. Appl. Microbiol. 19, 232-238.
32. Heidelberg, J. F., Shahamat, M., Levin, M., Rahman, I., Stelma, G., Grim, C. & Colwell, R. R. 1997 Effect of aerosolization on culturability and viability of Gram-negative bacteria. Appl. Environ. Microbiol. 63, 3585-3588.
33. Hemmes, J. H., Winkler, K. C. & Kool, S. M. 1960 Virus survival as a seasonal factor in influenza and polimyelitis. Nature 188, 430-431. (doi:10.1038/188430a0)
34. Hersoug, L. G. 2005 Viruses as the causative agent related to 'dampness' and the missing link between allergen exposure and onset of allergic disease. Indoor Air 15, 363-366. (doi:10.1111/j.1600-0668.2005.00382.x)
35. Hollins, P. D., Kettlewell, P. S., Atkinson, M. D., Stephenson, D. B., Corden, J. M., Millington, W. M. & Mullins, J. 2004 Relationships between airborne fungal spore concentration of Cladosporium and the summer climate at two sites in Britain. Int. J. Biometeorol. 48, 137-141. (doi:10.1007/s00484-003-0188-9)
36. Huynh, K. N., Oliver, B. G., Stelzer, S., Rawlinson, W. D. & Tovey, E. R. 2008 A new method for sampling and detection of exhaled respiratory virus aerosols. Clin. Infect. Dis. 46, 93-95. (doi:10.1086/523000)
37. Ijaz, M. K., Brunner, A. H., Sattar, S. A., Nair, R. C. & Johnson-Lussenburg, C. M. 1985 Survival characteristics of airborne human coronavirus 229E. J. Gen. Virol. 66, 2743-2748. (doi:10.1099/0022-1317-66-12-2743)
38. Ijaz, M. K., Karim, Y. G., Sattar, S. A. & Johnson-Lussenburg, C. M. 1987 Development of methods to study the survival of airborne viruses. J. Virol. Methods 18, 87-106. (doi:10.1016/0166-0934(87)90114-5)
39. Jericho, K. W., Langford, E. V. & Pantekoek, J. 1977 Recovery of Pasteurella hemolytica from aerosols at differing temperature and humidity. Can. J. Comp. Med. 41, 211-214.
40. Jo, W. K. & Seo, Y. J. 2005 Indoor and outdoor bioaerosol levels at recreation facilities, elementary schools, and homes. Chemosphere 61, 1570-1579. (doi:10.1016/j.chemosphere.2005.04.103)
41. Johnson, D. F., Druce, J. D., Birch, C. & Grayson, M. L. 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, 275-277. (doi:10.1086/600041)
42. Karim, Y. G., Ijaz, M. K., Sattar, S. A. & Johnson-Lussenburg, C. M. 1985 Effect of relative humidity on the airborne survival of rhinovirus-14. Can. J. Microbiol. 31, 1058-1061.
43. Karra, S. & Katsivela, E. 2007 Microorganisms in bioaerosol emissions from wastewater treatment plants during summer at a Mediterranean site. Water Res. 41, 1355-1365. (doi:10.1016/j.watres.2006.12.014)
44. Khan, N. N. & Wilson, B. L. 2003 An environmental assessment of mold concentrations and potential mycotoxin exposures in the greater Southeast Texas area. J. Environ. Sci. Health A Tox. Hazard. Subst. Environ. Eng. 38, 2759-2772.
45. Ko, G., First, M. W. & Burge, H. A. 2000 Influence of relative humidity on particle size and UV sensitivity of Serratia marcescens and Mycobacterium bovis BCG aerosols. Tuber. Lung Dis. 80, 217-228. (doi:10.1054/tuld.2000.0249)
46. Lee, J. H. & Jo, W. K. 2006 Characteristics of indoor and outdoor bioaerosols at Korean high-rise apartment buildings. Environ. Res. 101, 11-17. (doi:10.1016/j.envres.2005.08.009)
47. Li, C. S. & Kuo, Y. M. 1994 Characteristics of airborne microfungi in subtropical homes. Sci. Total Environ. 155, 267-271. (doi:10.1016/0048-9697(94)90505-3)
48. Lighthart, B. 1973 Survival of airborne bacteria in a high urban concentration of carbon monoxide. Appl. Microbiol. 25, 86-91.
49. Lowen, A. C., Mubareka, S., Tumpey, T. M., García-Sastre, A. & Palese, P. 2006 The guinea pig as a transmission model for human influenza viruses. Proc. Natl Acad. Sci. USA 103, 9988-9992. (doi:10.1073/pnas.0604157103)
50. Lowen, A. C., Mubareka, S., Steel, J. & Palese, P. 2007 Influenza virus transmission is dependent on relative humidity and temperature. PLoS Pathog. 3, 1470-1476. (doi:10.1371/journal.ppat.0030151)
51. Lowen, A. C., Steel, J., Mubareka, S. & Palese, P. 2008 High temperature (30°C) blocks aerosol but not contact transmission of influenza virus. J. Virol. 82, 5650-5652. (doi:10.1128/JVI.00325-08)
52. Lundholm, I. M. 1982 Comparison of methods for quantitative determinations of airborne bacteria and evaluation of total viable counts. Appl. Environ. Microbiol. 44, 179-183.
53. MacIntosh, D. L., Brightman, H. S., Baker, B. J., Myatt, T. A., Stewart, J. H. & McCarthy, J. F. 2006 Airborne fungal spores in a cross-sectional study of office buildings. J. Occup. Environ. Hyg. 3, 379-389. (doi:10.1080/10543400600760438)
54. Maher, J. A. & DeStefano, J. 2004 The ferret: an animal model to study influenza virus. Lab. Anim. (NY) 33, 50-53. (doi:10.1038/laban1004-50)
55. Maines, T. R. et al. 2006 Lack of transmission of H5N1 avian-human reassortant influenza viruses in a ferret model. Proc. Natl Acad. Sci. USA 103, 12 121-12 126. (doi:10.1073/pnas.0605134103)
56. Maines, T. R. et al. 2009 Transmission and pathogenesis of swine-origin 2009 A(H1N1) influenza viruses in ferrets and mice. Science 325, 484-487. (doi:10.1126/science.1177238)
57. Marthi, B., Fieland, V. P., Walter, M. & Seidler, R. J. 1990 Survival of bacteria during aerosolization. Appl. Environ. Microbiol. 56, 3463-3467.
58. McDermid, A. S. & Lever, M. S. 1996 Survival of Salmonella enteritidis Pt4 and Salm. typhimurium Swindon in aerosols. Lett. Appl. Microbiol. 23, 107-109. (doi:10.1111/j.1472-765X.1996.tb00042. x)
59. Mubareka, S., Lowen, A. C., Steel, J., Coates, A. L., García-Sastre, A. & Palese, P. 2009 Transmission of influenza virus via aerosols and fomites in the guinea pig model. J. Infect. Dis. 199, 858-865. (doi:10.1086/597073)
60. Muller, W. & Dinter, P. S. 1986 The tenacity of bacteria in the airborne state. IV: experimental studies on the viability of airborne E. coli 0:78 under the influence of different temperature and humidity. Zentralbl. Bakteriol. Mikrobiol. Hyg. A 262, 304-312.
61. Munster, V. J. et al. 2009 Pathogenesis and transmission of swine-origin 2009 A(H1N1) influenza virus in ferrets. Science 325, 481-483. (doi:10.1126/science.1177127)
62. Myatt, T. A., Johnston, S. L., Rudnick, S. & Milton, D. K. 2003 Airborne rhinovirus detection and effect of ultraviolet irradiation on detection by a semi-nested RT-PCR assay. BMC Public Health 3, 5. (doi:10.1186/1471-2458-3-5)
63. Oliveira, M., Ribeiro, H. & Abreu, I. 2005 Annual variation of fungal spores in atmosphere of Porto: 2003. Ann. Agric. Environ. Med. 12, 309-315.
64. Pei-Chih, W., Huey-Jen, S. & Chia-Yin, L. 2000 Characteristics of indoor and outdoor airborne fungi at suburban and urban homes in two seasons. Sci. Total Environ. 253, 111-118. (doi:10.1016/S0048-9697(00) 00423-X)
65. Peternel, R., Culig, J. & Hrga, I. 2004 Atmospheric concentrations of Cladosporium spp. and Alternaria spp. spores in Zagreb (Croatia) and effects of some meteorological factors. Ann. Agric. Environ. Med. 11, 303-307.
66. 2, temperature, and relative humidity. J. Occup. Environ. Hyg. 2, 553-566. (doi:10.1080/15459620500324453)
67. Riley, R. L. & Kaufman, J. E. 1972 Effect of relative humidity on the inactivation of airborne Serratia marcescens by ultraviolet radiation. Appl. Microbiol. 23, 1113-1120.
68. Rodriguez-Rajo, F. J., Iglesias, I. & Jato, V. 2005 Variation assessment of airborne Alternaria and Cladosporium spores at different bioclimatical conditions. Mycol. Res. 109, 497-507. (doi:10.1017/S0953756204001777)
69. Sabariego, S., Diaz de la Guardia, C. & Alba, F. 2000 The effect of meteorological factors on the daily variation of airborne fungal spores in Granada (southern Spain). Int. J. Biometeorol. 44, 1-5. (doi:10.1007/s004840050131)
70. Sakai, K., Tsubouchi, H. & Mitani, K. 2003 Airborne concentrations of fungal and indoor air pollutants in dwellings in Nagoya, Japan. Nippon Koshu Eisei Zasshi 50, 1017-1029.
71. Schaffer, F. L., Soergel, M. E. & Straube, D. C. 1976 Survival of airborne influenza virus: effects of propagating host, relative humidity, and composition of spray fluids. Arch. Virol. 51, 263-273. (doi:10.1007/BF01317930)
72. Shaman, J. & Kohn, M. 2009 Absolute humidity modulates influenza survival, transmission, and seasonality. Proc. Natl Acad. Sci. USA 106, 3243-3248. (doi:10.1073/pnas.0806852106)
73. Shelton, B. G., Kirkland, K. H., Flanders, W. D.& Morris, G. K. 2002 Profiles of airborne fungi in buildings and outdoor environments in the United States. Appl. Environ. Microbiol. 68, 1743-1753. (doi:10.1128/AEM.68.4.1743-1753.2002)
74. Stehmann, R., Rottmayer, J., Zschaubitz, K. & Mehlhorn, G. 1992 The tenacity of Bordetella bronchiseptica in the air. Zentralbl. Veterinarmed. B 39, 546-552.
75. Stelzer-Braid, S., Oliver, B. G., Blazey, A. J., Argent, E., Newsome, T. P., Rawlinson, W. D. & Tovey, E. R. 2009 Exhalation of respiratory viruses by breathing, coughing, and talking. J. Med. Virol. 81, 1674-1679. (doi:10.1002/jmv.21556)
76. Stennett, P. J. & Beggs, P. J. 2004 Alternaria spores in the atmosphere of Sydney, Australia, and relationships with meteorological factors. Int. J. Biometeorol. 49, 98-105. (doi:10.1007/s00484-004-0217-3)
77. Sze To, G. N., Wan, M. P., Chao, C. Y., Wei, F., Yu, S. C. & Kwan, J. K. 2008 A methodology for estimating airborne virus exposures in indoor environments using the spatial distribution of expiratory aerosols and virus viability characteristics. Indoor Air 18, 425-438. (doi:10.1111/j.1600-0668.2008.00544.x)
78. Takahashi, T. 1997 Airborne fungal colony-forming units in outdoor and indoor environments in Yokohama, Japan. Mycopathologia 139, 23-33. (doi:10.1023/A:1006831111595)
79. Tang, J. W., Lai, F. Y., Wong, F. & Hon, K. L. In press. Incidence of common respiratory viral infections related to climate factors in hospitalized children in Hong Kong. Epidemiol. Infect. 27.
80. Terzieva, S., Donnelly, J., Ulevicius, V., Grinshpun, S. A., Willeke, K., Stelma, G. N. & Brenner, K. P. 1996 Comparison of methods for detection and enumeration of airborne microorganisms collected by liquid impingement. Appl. Environ. Microbiol. 62, 2264-2272.
81. Theunissen, H. J., Lemmens-den Toom, N. A., Burggraaf, A., Stolz, E. & Michel, M. F. 1993 Influence of temperature and relative humidity on the survival of Chlamydia pneumoniae in aerosols. Appl. Environ. Microbiol. 59, 2589-2593.
82. Thomson, C. M., Chanter, N. & Wathes, C. M. 1992 Survival of toxigenic Pasteurella multocida in aerosols and aqueous liquids. Appl. Environ. Microbiol. 58, 932-936.
83. Troutt, C. & Levetin, E. 2001 Correlation of spring spore concentrations and meteorological conditions in Tulsa, Oklahoma. Int. J. Biometeorol. 45, 64-74. (doi:10.1007/s004840100087)
84. Tsai, F. C. & Macher, J. M. 2005 Concentrations of airborne culturable bacteria in 100 large US office buildings from the BASE study. Indoor Air 15(Suppl. 9), 71-81. (doi:10.1111/j.1600-0668.2005. 00346.x)
85. Vonberg, R. P. & Gastmeier, P. 2006 Nosocomial aspergillosis in outbreak settings. J. Hosp. Infect. 63, 246-254. (doi:10.1016/j.jhin.2006.02.014)
86. Walker, C. M. & Ko, G. 2007 Effect of ultraviolet germicidal irradiation on viral aerosols. Environ. Sci. Technol. 41, 5460-5465. (doi:10.1021/es070056u)
87. Walter, M. V., Marthi, B., Fieland, V. P. & Ganio, L. M. 1990 Effect of aerosolization on subsequent bacterial survival. Appl. Environ. Microbiol. 56, 3468-3472.
88. Wathes, C. M., Howard, K. & Webster, A. J. 1986 The survival of Escherichia coli in an aerosol at air temperatures of 15 and 30 degrees C and a range of humidities. J. Hyg. (Lond.) 97, 489-496.
89. Webb, S. J. 1959 Factors affecting the viability of air-borne bacteria. I. Bacteria aerosolized from distilled water. Can. J. Microbiol. 5, 649-669.
90. Won, W. D. & Ross, H. 1966 Effect of diluent and relative humidity on apparent viability of airborne Pasteurella pestis. Appl. Microbiol. 14, 742-745.
91. Wright, D. N., Bailey, G. D. & Hatch, M. T. 1968a Role of relative humidity in the survival of airborne Mycoplasma pneumoniae. J. Bacteriol. 96, 970-974.
92. Wright, D. N., Bailey, G. D. & Hatch, M. T. 1968b Survival of airborne Mycoplasma as affected by relative humidity. J. Bacteriol. 95, 251-252.
93. Wright, D. N., Bailey, G. D. & Goldberg, L. J. 1969 Effect of temperature on survival of airborne Mycoplasma pneumoniae. J. Bacteriol. 99, 491-495.
94. Wu, P. C., Li, Y. Y., Chiang, C. M., Huang, C. Y., Lee, C. C., Li, F. C. & Su, H. J. 2005 Changing microbial concentrations are associated with ventilation performance in Taiwan's air-conditioned office buildings. Indoor Air 15, 19-26. (doi:10.1111/j.1600-0668.2004.00313.x)
95. Xiao, W. J., Wang, M. L., Wei, W., Wang, J., Zhao, J. J., Yi, B. & Li, J. S. 2004 Detection of SARS-CoV and RNA on aerosol samples from SARS-patients admitted to hospital. Zhonghua Liu Xing Bing Xue Za Zhi 25, 882-885.