Temporal and Spatial Distribution of SARS-CoV-2 Aerosols in a Large-Scale Fangcang Shelter Hospital in Shanghai, China

Jiafu Jiang, Zhe Yin, Jing Li, Leili Jia, Rulin He, Wenhui Yang, Jihu Yang, Hang Fan, Sen Zhang, Yunfei Wang, Zengming Zhao, Haoran Peng, Lizhong Li, Yi Yang, Shi-Yong Fan, Rong Xiang, Jianshu Guo, Jinjin Wang, Juanning Wei, Fengling Zhou, Ding Liu, Ping Zhao, Yujun Cui, Yunxi Liu, Dongsheng Zhou, Gang Dong

Engineering ›› 2023, Vol. 28 ›› Issue (9) : 222-233.

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Engineering ›› 2023, Vol. 28 ›› Issue (9) : 222-233. DOI: 10.1016/j.eng.2023.06.006
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Temporal and Spatial Distribution of SARS-CoV-2 Aerosols in a Large-Scale Fangcang Shelter Hospital in Shanghai, China

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Abstract

The coronavirus disease 2019 (COVID-19) pandemic caused by frequently mutating severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has had a worldwide impact. However, detailed data on the potential aerosol transmission of SARS-CoV-2 in real-world and controlled laboratory settings remain sparse. During the COVID-19 pandemic in Shanghai, China in 2022, samples were collected in a Fangcang shelter hospital, a large-scale temporary hospital rapidly built by converting the existing National Exhibition and Convention Center (Shanghai) into a health care facility. Aerosol samples at different sites and intervals around patients and in public areas, surface samples, and pharyngeal swab samples from corresponding patients were included. Samples were tested for SARS-CoV-2 using real-time quantitative polymerase chain reaction (RT-qPCR) assays, followed by sequencing if the cycle threshold (Ct) value was < 30. The positivity rate for SARS-CoV-2 in aerosol samples was high in contaminated zones (37.5%, 104/277), especially around the bed (41.2%, 68/165) and near ventilation inlets (45.2%, 14/31). The prevalence of SARS-CoV-2 around the bed, public areas, and air inlets of exhaust vents fluctuated and was closely related to the positivity rate among patients at corresponding sampling sites. Some surface samples of different personal protective equipment from medical staff had high positivity rates. Sixty sequences of joined ORF1ab and spike genes obtained from sixty samples represented two main clusters of Omicron SARS-CoV-2. There was consistency in virus sequences from the same patient and their environment, and the detected virus sequences matched those of virus strains in circulation during the collection periods, which indicated a high likelihood of cross-contamination in the Fangcang shelter hospital. In summary, the results provide a quantitative and real landscape of the aerosol transmission of SARS-CoV-2 and a patient-centered view of contamination in large and enclosed spaces and offer a useful guide for taking targeted measures to avoid nosocomial infections during the management of SARS-CoV-2 or other respiratory virus diseases in a Fangcang shelter hospital.

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Coronavirus disease 2019 / Severe acute respiratory syndrome coronavirus 2 / Aerosols / Fangcang shelter hospital / China

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Jiafu Jiang, Zhe Yin, Jing Li, Leili Jia, Rulin He, Wenhui Yang, Jihu Yang, Hang Fan, Sen Zhang, Yunfei Wang, Zengming Zhao, Haoran Peng, Lizhong Li, Yi Yang, Shi-Yong Fan, Rong Xiang, Jianshu Guo, Jinjin Wang, Juanning Wei, Fengling Zhou, Ding Liu, Ping Zhao, Yujun Cui, Yunxi Liu, Dongsheng Zhou, Gang Dong. Temporal and Spatial Distribution of SARS-CoV-2 Aerosols in a Large-Scale Fangcang Shelter Hospital in Shanghai, China. Engineering, 2023, 28(9): 222‒233 https://doi.org/10.1016/j.eng.2023.06.006

References

[1]
M. Riediker, L. Briceno-Ayala, G. Ichihara, D. Albani, D. Poffet, D.H. Tsai, et al. Higher viral load and infectivity increase risk of aerosol transmission for Delta and Omicron variants of SARS-CoV-2. Swiss Med Wkly, 152 (0102) (2022), Article w30133. DOI: 10.4414/smw.2022.w30133
[2]
M.C. Chiu, C. Li, X. Liu, Y. Yu, J. Huang, Z. Wan, et al. A bipotential organoid model of respiratory epithelium recapitulates high infectivity of SARS-CoV-2 Omicron variant. Cell Discov, 8 (1) (2022), p. 57
[3]
J. Li, Y.N. Wu, S. Zhang, X.P. Kang, T. Jiang. Deep learning based on biologically interpretable genome representation predicts two types of human adaptation of SARS-CoV-2 variants. Brief Bioinform, 23 (3) (2022), Article bbac036
[4]
C.C. Wang, K.A. Prather, J. Sznitman, J.L. Jimenez, S.S. Lakdawala, Z. Tufekci, et al. Airborne transmission of respiratory viruses. Science, 373 (6558) (2021), p. 6558. DOI: 10.3390/ma14216558
[5]
J.W. Tang. SARS-CoV-2 and aerosols—arguing over the evidence. J Virol Methods, 289 (2021), Article 114033
[6]
U. Ranga. SARS-CoV-2 aerosol and droplets: an overview. Virusdisease, 32 (2) (2021), pp. 190-197. DOI: 10.1007/s13337-021-00660-z
[7]
A.A. Rabaan, S.H. Al-Ahmed, M. Al-Malkey, R. Alsubki, S. Ezzikouri, F.H. Al-Hababi, et al. Airborne transmission of SARS-CoV-2 is the dominant route of transmission: droplets and aerosols. Infez Med, 29 (1) (2021), pp. 10-19
[8]
N. Van Doremalen, T. Bushmaker, D.H. Morris, M.G. Holbrook, A. Gamble, B.N. Williamson, et al. Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1. N Engl J Med, 382 (16) (2020), pp. 1564-1567. DOI: 10.1056/nejmc2004973
[9]
L. Morawska, D.K. Milton. It is time to address airborne transmission of coronavirus disease 2019 (COVID-19). Clin Infect Dis, 71 (9) (2020), pp. 2311-2313. DOI: 10.1093/cid/ciaa939
[10]
A. Dinoi, M. Feltracco, D. Chirizzi, S. Trabucco, M. Conte, E. Gregoris, et al. A review on measurements of SARS-CoV-2 genetic material in air in outdoor and indoor environments: implication for airborne transmission. Sci Total Environ, 809 (2022), Article 151137
[11]
M. Conte, M. Feltracco, D. Chirizzi, S. Trabucco, A. Dinoi, E. Gregoris, et al. Airborne concentrations of SARS-CoV-2 in indoor community environments in Italy. Environ Sci Pollut Res Int, 29 (10) (2022), pp. 13905-13916. DOI: 10.1007/s11356-021-16737-7
[12]
D. Lewis. Mounting evidence suggests coronavirus is airborne—but health advice has not caught up. Nature, 583 (7817) (2020), pp. 510-513. DOI: 10.1038/d41586-020-02058-1
[13]
D. Lewis. Why the WHO took two years to say COVID is airborne. Nature, 604 (7904) (2022), pp. 26-31. DOI: 10.1038/d41586-022-00925-7
[14]
A.X. Ang, I. Luhung, B.A. Ahidjo, D.I. Drautz-Moses, P.A. Tambyah, C.K. Mok, et al. Airborne SARS-CoV-2 surveillance in hospital environment using high-flowrate air samplers and its comparison to surface sampling. Indoor Air, 32 (1) (2022), Article e12930
[15]
Z. Baboli, N. Neisi, A.A. Babaei, M. Ahmadi, A. Sorooshian, Y.T. Birgani, et al. On the airborne transmission of SARS-CoV-2 and relationship with indoor conditions at a hospital. Atmos Environ, 261 (2021), Article 118563
[16]
Z.D. Guo, Z.Y. Wang, S.F. Zhang, X. Li, L. Li, C. Li, et al. Aerosol and surface distribution of severe acute respiratory syndrome coronavirus 2 in hospital wards, Wuhan, China, 2020. Emerg Infect Dis, 26 (7) (2020), pp. 1583-1591. DOI: 10.3201/eid2607.200885
[17]
N. Dumont-Leblond, M. Veillette, S. Mubareka, L. Yip, Y. Longtin, P. Jouvet, et al. Low incidence of airborne SARS-CoV-2 in acute care hospital rooms with optimized ventilation. Emerg Microbes Infect, 9 (1) (2020), pp. 2597-2605. DOI: 10.1080/22221751.2020.1850184
[18]
M.A. Lane, M. Walawender, A.S. Webster, E.A. Brownsword, J.M. Ingersoll, C. Miller, et al. Sampling for SARS-CoV-2 aerosols in hospital patient rooms. Viruses, 13 (12) (2021), p. 2347. DOI: 10.3390/v13122347
[19]
J. Hu, C. Lei, Z. Chen, W. Liu, X. Hu, R. Pei, et al. Distribution of airborne SARS-CoV-2 and possible aerosol transmission in Wuhan hospitals. China Natl Sci Rev, 7 (12) (2020), pp. 1865-1867. DOI: 10.1093/nsr/nwaa250
[20]
R.A. Stern, M.E. Charness, K. Gupta, P. Koutrakis, K. Linsenmeyer, R. Madjarov, et al. Concordance of SARS-CoV-2 RNA in aerosols from a nurse station and in nurses and patients during a hospital ward outbreak. JAMA Netw Open, 5 (6) (2022), Article e2216176. DOI: 10.1001/jamanetworkopen.2022.16176
[21]
M. Kang, J. Wei, J. Yuan, J. Guo, Y. Zhang, J. Hang, et al. Probable evidence of fecal aerosol transmission of SARS-CoV-2 in a high-rise building. Ann Intern Med, 173 (12) (2020), pp. 974-980. DOI: 10.7326/m20-0928
[22]
M. Hadei, S.R. Mohebbi, P.K. Hopke, A. Shahsavani, S. Bazzazpour, M. Alipour, et al. Presence of SARS-CoV-2 in the air of public places and transportation. Atmos Pollut Res, 12 (3) (2021), pp. 302-306
[23]
Y. Tao, X. Zhang, G. Qiu, M. Spillmann, Z. Ji, J. Wang. SARS-CoV-2 and other airborne respiratory viruses in outdoor aerosols in three Swiss cities before and during the first wave of the COVID-19 pandemic. Environ Int, 164 (2022), Article 107266
[24]
J.R. Port, C.K. Yinda, V.A. Avanzato, J.E. Schulz, M.G. Holbrook, N. van Doremalen, et al. Increased small particle aerosol transmission of B.1.1.7 compared with SARS-CoV-2 lineage A in vivo. Nat Microbiol, 7 (2) (2022), pp. 213-223. DOI: 10.1038/s41564-021-01047-y
[25]
J. Zheng, Z. Wang, J. Li, Y. Zhang, L. Jiang, Y. Fu, et al. High amounts of SARS-CoV-2 in aerosols exhaled by patients with Omicron variant infection. J Infect, 84 (6) (2022), pp. e126-e128
[26]
Z. Zhang, X. Li, Q. Wang, X. Zhao, J. Xu, Q. Jiang, et al. Simulation studies provide evidence of aerosol transmission of SARS-CoV-2 in a multi-story building via air supply, exhaust and sanitary pipelines. Int J Environ Res Public Health, 19 (3) (2022), p. 1532. DOI: 10.3390/ijerph19031532
[27]
Z. Zhang, X. Li, Q. Wang, J. Xu, Q. Jiang, S. Jiang, et al. Field simulation of aerosol transmission of SARS-CoV-2 in a special building layout—Guangdong Province, China, 2021. China CDC Wkly, 3 (34) (2021), pp. 711-715. DOI: 10.46234/ccdcw2021.176
[28]
M. Zhang, P. Shrestha, X. Liu, T. Turnaoglu, J. DeGraw, D. Schafer, et al. Computational fluid dynamics simulation of SARS-CoV-2 aerosol dispersion inside a grocery store. Build Environ, 209 (2022), Article 108652
[29]
D. Vernez, S. Schwarz, J.J. Sauvain, C. Petignat, G. Suarez. Probable aerosol transmission of SARS-CoV-2 in a poorly ventilated courtroom. Indoor Air, 31 (6) (2021), pp. 1776-1785. DOI: 10.1111/ina.12866
[30]
L. Moeller, F. Wallburg, F. Kaule, S. Schoenfelder. Numerical flow simulation on the virus spread of SARS-CoV-2 due to airborne transmission in a classroom. Int J Environ Res Public Health, 19 (10) (2022), p. 6279. DOI: 10.3390/ijerph19106279
[31]
G.K. Rencken, E.K. Rutherford, N. Ghanta, J. Kongoletos, L. Glicksman. Patterns of SARS-CoV-2 aerosol spread in typical classrooms. Build Environ, 204 (2021), Article 108167
[32]
W. Schade, V. Reimer, M. Seipenbusch, U. Willer, E.G. Hübner. Viral aerosol transmission of SARS-CoV-2 from simulated human emission in a concert hall. Int J Infect Dis, 107 (2021), pp. 12-14
[33]
R.L. Winslow, J. Zhou, E.F. Windle, I. Nur, R. Lall, C. Ji, et al. SARS-CoV-2 environmental contamination from hospitalised patients with COVID-19 receiving aerosol-generating procedures. Thorax, 77 (3) (2022), pp. 259-267. DOI: 10.1136/thoraxjnl-2021-218035
[34]
A. Dance. Omicron’s lasting mysteries: four questions scientists are racing to answer. Nature, 603 (7899) (2022), pp. 22-24. DOI: 10.1038/d41586-022-00428-5
[35]
S. Chen, H. Sun, M. Heng, X. Tong, P. Geldsetzer, Z. Wang, et al. Factors predicting progression to severe COVID-19: a competing risk survival analysis of 1753 patients in community isolation in Wuhan, China. Engineering, 13 (2022), pp. 99-106
[36]
J.L. Santarpia, V.L. Herrera, D.N. Rivera, S. Ratnesar-Shumate, S.P. Reid, D.N. Ackerman, et al. The size and culturability of patient-generated SARS-CoV-2 aerosol. J Expo Sci Environ Epidemiol, 32 (5) (2022), pp. 706-711. DOI: 10.1038/s41370-021-00376-8
[37]
J.A. Lednicky, M. Lauzard, Z.H. Fan, A. Jutla, T.B. Tilly, M. Gangwar, et al. Viable SARS-CoV-2 in the air of a hospital room with COVID-19 patients. Int J Infect Dis, 100 (2020), pp. 476-482
[38]
H. Kitagawa, T. Nomura, Y. Kaiki, M. Kakimoto, T. Nazmul, K. Omori, et al. Viable SARS-CoV-2 detected in the air of hospital rooms of patients with COVID-19 with an early infection. Int J Infect Dis, 126 (2023), pp. 73-78
[39]
W.B. Vass, J.A. Lednicky, S.N. Shankar, Z.H. Fan, A. Eiguren-Fernandez, C.Y. Wu. Viable SARS-CoV-2 Delta variant detected in aerosols in a residential setting with a self-isolating college student with COVID-19. J Aerosol Sci, 165 (2022), Article 106038
[40]
M. Alsved, D. Nygren, S. Thuresson, P. Medstrand, C.J. Fraenkel, J. Löndahl. SARS-CoV-2 in exhaled aerosol particles from COVID-19 cases and its association to household transmission. Clin Infect Dis, 75 (1) (2022), pp. e50-e56. DOI: 10.1093/cid/ciac202
[41]
H. Xiong, X. Ye, Y. Li, J. Qi, X. Fang, J. Kong. Efficient microfluidic-based air sampling/monitoring platform for detection of aerosol SARS-CoV-2 on-site. Anal Chem, 93 (9) (2021), pp. 4270-4276. DOI: 10.1021/acs.analchem.0c05154
[42]
S. Paton, S. Clark, A. Spencer, I. Garratt, I. Dinesh, K.A. Thompson, et al. Characterisation of particle size and viability of SARS-CoV-2 aerosols from a range of nebuliser types using a novel sampling technique. Viruses, 14 (3) (2022), p. 639. DOI: 10.3390/v14030639
[43]
C. Xu, W. Liu, X. Luo, X. Huang, P.V. Nielsen. Prediction and control of aerosol transmission of SARS-CoV-2 in ventilated context: from source to receptor. Sustain Cities Soc, 76 (2022), Article 103416
[44]
M. Pan, J.A. Lednicky, C.Y. Wu. Collection, particle sizing and detection of airborne viruses. J Appl Microbiol, 127 (6) (2019), pp. 1596-1611. DOI: 10.1111/jam.14278
[45]
S. Chen, J. Yang, W. Yang, C. Wang, T. Bärnighausen. COVID-19 control in China during mass population movements at New Year. Lancet, 395 (10226) (2020), pp. 764-766
[46]
S. Chen, Z. Zhang, J. Yang, J. Wang, X. Zhai, T. Bärnighausen, et al. Fangcang shelter hospitals: a novel concept for responding to public health emergencies. Lancet, 395 (10232) (2020), pp. 1305-1314
[47]
Y. Han, Q. Zuo, S. Zhang, W. Xue, C. Qin, R. Li, et al. Retrospective analysis of COVID-19 patients’ clinical information and medicine/nursing management in Shanghai National Exhibition and Convention Center cabin hospital. Chi J Clin Thorac Cardiovasc Surg, 29 (9) (2022), pp. 1093-1099 [Chinese]. DOI: 10.1109/imcec55388.2022.10019831
[48]
C.C. Tseng, C.S. Li. Collection efficiencies of aerosol samplers for virus-containing aerosols. J Aerosol Sci, 36 (5) (2005), pp. 593-607
[49]
A. Stamatakis. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30 (9) (2014), pp. 1312-1313. DOI: 10.1093/bioinformatics/btu033
[50]
A. Robotto, A. Civra, P. Quaglino, D. Polato, E. Brizio, D. Lembo. SARS-CoV-2 airborne transmission: a validated sampling and analytical method. Environ Res, 200 (2021), Article 111783
[51]
P. Capparè, R. D’Ambrosio, R. De Cunto, A. Darvizeh, M. Nagni, E. Gherlone. The usage of an air purifier device with HEPA 14 filter during dental procedures in COVID-19 pandemic: a randomized clinical trial. Int J Environ Res Public Health, 19 (9) (2022), p. 5139. DOI: 10.3390/ijerph19095139
[52]
J.S. Kutter, D. de Meulder, T.M. Bestebroer, P. Lexmond, A. Mulders, M. Richard, et al. SARS-CoV and SARS-CoV-2 are transmitted through the air between ferrets over more than one meter distance. Nat Commun, 12 (1) (2021), Article 1653
[53]
S. Yuan, Z.W. Ye, R. Liang, K. Tang, A.J. Zhang, G. Lu, et al. Pathogenicity, transmissibility, and fitness of SARS-CoV-2 Omicron in Syrian hamsters. Science, 377 (6604) (2022), pp. 428-433. DOI: 10.1126/science.abn8939
[54]
T. Greenhalgh, J.L. Jimenez, K.A. Prather, Z. Tufekci, D. Fisman, R. Schooley. Ten scientific reasons in support of airborne transmission of SARS-CoV-2. Lancet, 397 (10285) (2021), pp. 1603-1605
[55]
P.V. Nielsen, Y. Li, M. Buus, F.V. Winther. Risk of cross-infection in a hospital ward with downward ventilation. Build Environ, 45 (9) (2010), pp. 2008-2014
[56]
CDC. Guidelines for preventing the transmission of Mycobacterium tuberculosis in health-care facilities, 1994. MMWR Recomm Rep, 43 (RR-13) (1994), pp. 1-132
[57]
L.F. Pease, N. Wang, T.I. Salsbury, R.M. Underhill, J.E. Flaherty, A. Vlachokostas, et al. Investigation of potential aerosol transmission and infectivity of SARS-CoV-2 through central ventilation systems. Build Environ, 197 (2021), Article 107633
[58]
V. Arumuru, J. Pasa, S.S. Samantaray. Experimental visualization of sneezing and efficacy of face masks and shields. Phys Fluids, 32 (11) (2020), Article 115129
[59]
T. Merhi, O. Atasi, C. Coetsier, B. Lalanne, K. Roger. Assessing suspension and infectivity times of virus-loaded aerosols involved in airborne transmission. Proc Natl Acad Sci USA, 119 (32) (2022), Article e2204593119
[60]
L.K. Orvihoho, J. Yin, Z.F. Zhou, J. Han, B. Chen, L.H. Fan, et al. Mechanisms controlling the transport and evaporation of human exhaled respiratory droplets containing the severe acute respiratory syndrome coronavirus: a review. Environ Chem Lett, 22 (2023), pp. 1-2
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