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Original Articles

Comparison of the survival of different isolates of SARS-CoV-2 in evaporating aerosols

ORCID Icon, , , , , & show all
Pages 1146-1155 | Received 15 Aug 2022, Accepted 16 Sep 2022, Published online: 10 Oct 2022

References

  • Adenaiye, O. O., J. Lai, P. J. Bueno de Mesquita, F. Hong, S. Youssefi, J. German, S. Tai, B. Albert, M. Schanz, and S. Weston. 2022. Infectious severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in exhaled aerosols and efficacy of masks during early mild infection. Clin. Infect. Dis. 75 (1):e241–48.
  • Almstrand, A.-C., B. Bake, E. Ljungström, P. Larsson, A. Bredberg, E. Mirgorodskaya, and A.-C. Olin. 2010. Effect of airway opening on production of exhaled particles. J. Appl. Physiol. 108 (3):584–88. doi:10.1152/japplphysiol.00873.2009.
  • Benbough, J. 1967. Death mechanisms in airborne Escherichia coli. J. Gen. Microbiol. 47 (3):325–33. doi:10.1099/00221287-47-3-325.
  • Bicer, E. M. 2015. Compositional characterisation of human respiratory tract lining fluids for the design of disease specific simulants. Doctoral diss., King’s College London.
  • Bolze, A., S. Luo, S. White, E. T. Cirulli, D. Wyman, A. Dei Rossi, H. Machado, T. Cassens, S. Jacobs, and K. M. Schiabor Barrett. 2021. SARS-CoV-2 variant delta rapidly displaced variant alpha in the United States and led to higher viral loads. Cell Rep. Med. 3 (3):100564.
  • Bourouiba, L. 2020. Turbulent gas clouds and respiratory pathogen emissions: Potential implications for reducing transmission of covid-19. Jama 323 (18):1837–38. doi:10.1001/jama.2020.4756.
  • Bourouiba, L., E. Dehandschoewercker, and J. W. Bush. 2014. Violent expiratory events: On coughing and sneezing. J. Fluid Mech. 745:537–63. doi:10.1017/jfm.2014.88.
  • Boydston, J. A., J. J. Yeager, J. R. Taylor, and P. A. Dabisch. 2021. Influence of aerodynamic particle size on botulinum neurotoxin potency in mice. Inhal. Toxicol. 33 (1):1–7. doi:10.1080/08958378.2020.1851327.
  • Bredberg, A., J. Gobom, A.-C. Almstrand, P. Larsson, K. Blennow, A.-C. Olin, and E. Mirgorodskaya. 2012. Exhaled endogenous particles contain lung proteins. Clin. Chem. 58 (2):431–40. doi:10.1373/clinchem.2011.169235.
  • Chao, C. Y. H., M. P. Wan, L. Morawska, G. R. Johnson, Z. D. Ristovski, M. Hargreaves, K. Mengersen, S. Corbett, Y. Li, X. Xie, et al. 2009. Characterization of expiration air jets and droplet size distributions immediately at the mouth opening. J. Aerosol Sci. 40 (2):122–33. doi:10.1016/j.jaerosci.2008.10.003.
  • Dabisch, P., M. Schuit, A. Herzog, K. Beck, S. Wood, M. Krause, D. Miller, W. Weaver, D. Freeburger, I. Hooper, et al. 2021. The influence of temperature, humidity, and simulated sunlight on the infectivity of SARS-CoV-2 in aerosols. Aerosol Sci. Technol. 55 (2):142–53. doi:10.1080/02786826.2020.1829536.
  • Dabisch, P. A., J. Biryukov, K. Beck, J. A. Boydston, J. S. Sanjak, A. Herzog, B. Green, G. Williams, J. Yeager, J. K. Bohannon, et al. 2021. Seroconversion and fever are dose-dependent in a nonhuman primate model of inhalational covid-19. PLoS Pathog. 17 (8):e1009865. doi:10.1371/journal.ppat.1009865.
  • Day, W. C, and R. F. Berendt. 1972. Experimental tularemia in Macaca mulatta: Relationship of aerosol particle size to the infectivity of airborne pasteurella tularensis. Infect. Immun. 5 (1):77–82. doi:10.1128/iai.5.1.77-82.1972.
  • Ferry, R. M., W. F. Brown, and E. B. Damon. 1958. Studies of the loss of viability of bacterial aerosols*: III. Factors affecting death rates of certain non-pathogens. J. Hyg. 56 (3):389–403. doi:10.1017/s0022172400037888.
  • Fitzgeorge, R., A. Baskerville, M. Broster, P. Hambleton, and P. Dennis. 1983. Aerosol infection of animals with strains of legionella pneumophila of different virulence: Comparison with intraperitoneal and intranasal routes of infection. J. Hyg. 90 (1):81–89. doi:10.1017/s0022172400063877.
  • Green, L. H, and G. M. Green. 1968. Direct method for determining the viability of a freshly generated mixed bacterial aerosol. Appl. Microbiol. 16 (1):78–81. doi:10.1128/am.16.1.78-81.1968.
  • Hess, G. E. 1965. Effects of oxygen on aerosolized serratia marcescens. Appl. Microbiol. 13 (5):781–87. doi:10.1128/am.13.5.781-787.1965.
  • Holmgren, H., E. Ljungström, A.-C. Almstrand, B. Bake, and A.-C. Olin. 2010. Size distribution of exhaled particles in the range from 0.01 to 2.0 μm. J. Aerosol Sci. 41 (5):439–46. doi:10.1016/j.jaerosci.2010.02.011.
  • Johnson, G. R., L. Morawska, Z. D. Ristovski, M. Hargreaves, K. Mengersen, C. Y. H. Chao, M. P. Wan, Y. Li, X. Xie, D. Katoshevski, et al. 2011. Modality of human expired aerosol size distributions. J. Aerosol Sci. 42 (12):839–51. doi:10.1016/j.jaerosci.2011.07.009.
  • Kumar, A., W. Terakosolphan, M. Hassoun, K.-K. Vandera, A. Novicky, R. Harvey, P. G. Royall, E. M. Bicer, J. Eriksson, K. Edwards, et al. 2017. A biocompatible synthetic lung fluid based on human respiratory tract lining fluid composition. Pharm. Res. 34 (12):2454–65. doi:10.1007/s11095-017-2169-4.
  • Larsson, P., E. Mirgorodskaya, L. Samuelsson, B. Bake, A.-C. Almstrand, A. Bredberg, and A.-C. Olin. 2012. Surfactant protein A and albumin in particles in exhaled air. Respir. Med. 106 (2):197–204. doi:10.1016/j.rmed.2011.10.008.
  • Lednicky, J. A., M. Lauzardo, M. M. Alam, M. A. Elbadry, C. J. Stephenson, J. C. Gibson, and J. G. Morris, Jr. 2021. Isolation of SARS-CoV-2 from the air in a car driven by a covid patient with mild illness. Int. J. Infect. Dis. 108:212–16. doi:10.1016/j.ijid.2021.04.063.
  • Lednicky, J. A., M. Lauzardo, Z. Hugh Fan, A. Jutla, T. B. Tilly, M. Gangwar, M. Usmani, S. N. Shankar, K. Mohamed, A. Eiguren-Fernandez, Jr., et al. 2020. Viable SARS-CoV-2 in the air of a hospital room with covid-19 patients. Int. J. Infect. Dis. 100:476–82. doi:10.1016/j.ijid.2020.09.025.
  • Li, B., A. Deng, K. Li, Y. Hu, Z. Li, Y. Shi, Q. Xiong, Z. Liu, Q. Guo, L. Zou, et al. 2022. Viral infection and transmission in a large, well-traced outbreak caused by the SARS-CoV-2 delta variant. Nat. Commun. 13 (1):9. doi:10.1038/s41467-022-28089-y.
  • Li, Y., and X. X. Tang. 2021. Abnormal airway mucus secretion induced by virus infection. Front. Immunol. 12:701443. doi:10.3389/fimmu.2021.701443.
  • Liu, L., J. Wei, Y. Li, and A. Ooi. 2017. Evaporation and dispersion of respiratory droplets from coughing. Indoor Air. 27 (1):179–90. doi:10.1111/ina.12297.
  • Ma, J., X. Qi, H. Chen, X. Li, Z. Zhang, H. Wang, L. Sun, L. Zhang, J. Guo, L. Morawska, et al. 2021. Coronavirus disease 2019 patients in earlier stages exhaled millions of severe acute respiratory syndrome coronavirus 2 per hour. Clin. Infect. Dis. 72 (10):e652–54. doi:10.1093/cid/ciaa1283.
  • Malik, M., A.-C. Kunze, T. Bahmer, S. Herget-Rosenthal, and T. Kunze. 2021. SARS-CoV-2: Viral loads of exhaled breath and oronasopharyngeal specimens in hospitalized patients with covid-19. Int. J. Infect. Dis. 110:105–10. doi:10.1016/j.ijid.2021.07.012.
  • Morawska, L., G. Johnson, Z. Ristovski, M. Hargreaves, K. Mengersen, S. Corbett, C. Y. H. Chao, Y. Li, and D. Katoshevski. 2009. Size distribution and sites of origin of droplets expelled from the human respiratory tract during expiratory activities. J. Aerosol Sci. 40 (3):256–69. doi:10.1016/j.jaerosci.2008.11.002.
  • Moreira, F. R. R., M. D'arc, D. Mariani, A. L. Herlinger, F. B. Schiffler, Á. D. Rossi, I. C. Leitão, T. D. S. Miranda, M. A. C. Cosentino, M. C. P. Tôrres, et al. 2021. Epidemiological dynamics of SARS-CoV-2 VOC Gamma in Rio de Janeiro, Brazil. Virus Evol. 7 (2):veab087. doi:10.1093/ve/veab087.
  • Nicas, M., W. W. Nazaroff, and A. Hubbard. 2005. Toward understanding the risk of secondary airborne infection: Emission of respirable pathogens. J. Occup. Environ. Hyg. 2 (3):143–54. doi:10.1080/15459620590918466.
  • Oswin, H. P., A. E. Haddrell, M. Otero-Fernandez, J. F. S. Mann, T. A. Cogan, T. G. Hilditch, J. Tian, D. A. Hardy, D. J. Hill, A. Finn, et al. 2022. The dynamics of SARS-CoV-2 infectivity with changes in aerosol microenvironment. Proc. Natl. Acad. Sci. USA 119 (27):e2200109119. doi:10.1073/pnas.2200109119.
  • Proctor, G., and A. Shaalan. 2021. Disease-induced changes in salivary gland function and the composition of saliva. J. Dent. Res. 100 (11):1201–09. doi:10.1177/00220345211004842.
  • Ratnesar-Shumate, S., K. Bohannon, G. Williams, B. Holland, M. Krause, B. Green, D. Freeburger, and P. Dabisch. 2021. Comparison of the performance of aerosol sampling devices for measuring infectious SARS-CoV-2 aerosols. Aerosol Sci. Technol. 55 (8):975–86. doi:10.1080/02786826.2021.1910137.
  • Schaffer, F., M. Soergel, and D. Straube. 1976. Survival of airborne influenza virus: Effects of propagating host, relative humidity, and composition of spray fluids. Arch. Virol. 51 (4):263–73. doi:10.1007/BF01317930.
  • Schuit, M., J. Biryukov, K. Beck, J. Yolitz, J. Bohannon, W. Weaver, D. Miller, B. Holland, M. Krause, D. Freeburger, et al. 2021. The stability of an isolate of the SARS-CoV-2 B. 1.1.7 lineage in aerosols is similar to 3 earlier isolates. J. Infect. Dis. 224:1641–48. doi:10.1093/infdis/jiab171.
  • Schuit, M., S. Ratnesar-Shumate, J. Yolitz, G. Williams, W. Weaver, B. Green, D. Miller, M. Krause, K. Beck, S. Wood, et al. 2020. Airborne SARS-CoV-2 is rapidly inactivated by simulated sunlight. J. Infect. Dis. 222 (4):564–71. doi:10.1093/infdis/jiaa334.
  • Smither, S. J., L. S. Eastaugh, J. S. Findlay, and M. S. Lever. 2020. Experimental aerosol survival of SARS-CoV-2 in artificial saliva and tissue culture media at medium and high humidity. Emerg. Microbes Infect. 9 (1):1415–17. doi:10.1080/22221751.2020.1777906.
  • Sonkin, L. S. 1949. Infections induced in mice by local application of streptococci and pneumococci to the nasal mucosa and by intrapulmonary instillation. J. Infect. Dis. 84 (3):290–305. doi:10.1093/infdis/84.3.290.
  • Sonkin, L. S. 1951. The role of particle size in experimental air-borne infection. Am. J. Hyg. 53 (3):337–54. doi:10.1093/oxfordjournals.aje.a119459.
  • Teyssou, E., H. Delagrèverie, B. Visseaux, S. Lambert-Niclot, S. Brichler, V. Ferre, S. Marot, A. Jary, E. Todesco, A. Schnuriger, et al. 2021. The delta SARS-CoV-2 variant has a higher viral load than the beta and the historical variants in nasopharyngeal samples from newly diagnosed covid-19 patients. J. Infect. 83 (4):e1–e3. doi:10.1016/j.jinf.2021.08.027.
  • Teyssou, E., C. Soulie, B. Visseaux, S. Lambert-Niclot, V. Ferre, S. Marot, A. Jary, S. Sayon, K. Zafilaza, V. Leducq, et al. 2021. The 501y. V2 SARS-CoV-2 variant has an intermediate viral load between the 501y. V1 and the historical variants in nasopharyngeal samples from newly diagnosed covid-19 patients. J. Infect. 83 (1):119–45. doi:10.1016/j.jinf.2021.04.023.
  • Theunissen, H., N. A. Lemmens-den Toom, A. Burggraaf, E. Stolz, and M. Michel. 1993. Influence of temperature and relative humidity on the survival of chlamydia pneumoniae in aerosols. Appl. Environ. Microbiol. 59 (8):2589–93. doi:10.1128/aem.59.8.2589-2593.1993.
  • Tinglev, Å. D., S. Ullah, G. Ljungkvist, E. Viklund, A.-C. Olin, and O. Beck. 2016. Characterization of exhaled breath particles collected by an electret filter technique. J. Breath Res. 10 (2):026001. doi:10.1088/1752-7155/10/2/026001.
  • van Doremalen, N., T. Bushmaker, D. H. Morris, M. G. Holbrook, A. Gamble, B. N. Williamson, A. Tamin, J. L. Harcourt, N. J. Thornburg, S. I. Gerber, et al. 2020. Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1. N. Engl. J. Med. 382 (16):1564–67. doi:10.1056/NEJMc2004973.
  • van Kampen, J. J. A., D. A. M. C. van de Vijver, P. L. A. Fraaij, B. L. Haagmans, M. M. Lamers, N. Okba, J. P. C. van den Akker, H. Endeman, D. A. M. P. J. Gommers, J. J. Cornelissen, et al. 2021. Duration and key determinants of infectious virus shedding in hospitalized patients with coronavirus disease-2019 (Covid-19). Nat. Commun. 12 (1):6. doi:10.1038/s41467-020-20568-4.
  • Wathes, C., K. Howard, and A. Webster. 1986. The survival of Escherichia coli in an aerosol at air temperatures of 15 and 30 °C and a range of humidities. J. Hyg. 97 (3):489–96. doi:10.1017/s0022172400063671.
  • Webb, S. 1959. Factors affecting the viability of air-borne bacteria: I. Bacteria aerosolized from distilled water. Can. J. Microbiol. 5 (6):649–69. doi:10.1139/m59-079.
  • Wells, W. F. 1955. Airborne contagion and air hygiene. An ecological study of droplet infections. In Airborne contagion and air hygiene. An ecological study of droplet infections, ed. G. Cumberlege, 117–122 and 352–371. London: Oxford University Press.
  • Wölfel, R., V. M. Corman, W. Guggemos, M. Seilmaier, S. Zange, M. A. Müller, D. Niemeyer, T. C. Jones, P. Vollmar, C. Rothe, et al. 2020. Virological assessment of hospitalized patients with Covid-2019. Nature 581 (7809):465–69. doi:10.1038/s41586-020-2196-x.
  • Xie, X., Y. Li, T. Zhang, and H. H. Fang. 2006. Bacterial survival in evaporating deposited droplets on a teflon-coated surface. Appl. Microbiol. Biotechnol. 73 (3):703–12. doi:10.1007/s00253-006-0492-5.
  • Yang, Q., T. K. Saldi, P. K. Gonzales, E. Lasda, C. J. Decker, K. L. Tat, M. R. Fink, C. R. Hager, J. C. Davis, C. D. Ozeroff, et al. 2021. Just 2% of SARS-CoV-2− positive individuals carry 90% of the virus circulating in communities. Proc. Natl. Acad. Sci. USA. 118 (21):e2104547118. doi:10.1073/pnas.2104547118.