Aerosol transmission, an indispensable route of COVID-19 spread: case study of a department-store cluster

Abstract

Patients with COVID-19 have revealed a massive outbreak around the world, leading to widespread concerns in global scope. Figuring out the transmission route of COVID-19 is necessary to control further spread. We analyzed the data of 43 patients in Baodi Department Store (China) to supplement the transmission route and epidemiological characteristics of COVID-19 in a cluster outbreak. Incubation median was estimated to endure 5.95 days (2–13 days). Almost 76.3% of patients sought medical attention immediately uponillness onset. The median period ofillness onsetto hospitalization and confirmation were 3.96 days (0–14) and 5.58 days (1–21), respectively. Patients with different cluster case could demonstrate unique epidemiological characteristics due to the particularity of outbreak sites. SRAS-CoV-2 can be released into the surrounding air through patient’s respiratory tract activities, and can exist for a long time for long-distance transportation. SRAS-CoV-2 RNA can be detected in aerosol in different sites, including isolation ward, general ward, outdoor, toilet, hallway, and crowded public area. Environmental factors influencing were analyzed and indicated that the SARS-CoV-2 transportation in aerosol was dependent on temperature, air humidity, ventilation rate and inactivating chemicals (ozone) content. As for the infection route of case numbers 2 to 6, 10, 13, 16, 17, 18, 20 and 23, we believe that aerosol transmission played a significant role in analyzing their exposure history and environmental conditions in Baodi Department Store. Aerosol transmission could occur in some cluster cases when the environmental factors are suitable, and it is an indispensable route of COVID-19 spread.

References

  1. Bassetti M, Vena A, Giacobbe D R (2020). The novel Chinese coronavirus (2019-nCoV) infections: Challenges for fighting the storm. European Journal of Clinical Investigation, 50(3): e13209

    CAS  Article  Google Scholar 

  2. Bhagavathula A S, Rahmani J, Aldhaleei W A, Kumar P, Rovetta A (2020). Global, regional and national incidence and case-fatality rates of novel coronavirus (COVID-19) across 154 countries and territories: A systematic assessment of cases reported from January to March 16, 2020. New York: medRxiv preprint

  3. Bukhari Q, Jameel Y (2020). Will coronavirus pandemic diminish by summer? Rochester,: Social Science Research Network eLibrery preprint

  4. Buonanno G, Stabile L, Morawska L (2020). Estimation of airborne viral emission: Quanta emission rate of SARS-CoV-2 for infection risk assessment. Environment International, 141: 105794

    CAS  Article  Google Scholar 

  5. Chan J F W, Yuan S F, Kok K H, To K K W, Chu H, Yang J, Xing F F, Liu J L, Yip C C Y, Poon R W S, Tsoi H W, Lo S K F, Chan K H, Poon V K M, Chan W M, Ip J D, Cai J P, Cheng V C C, Chen H L, Hui C K M, Yuen K Y (2020). A familial cluster of pneumonia associated with the 2019 novel coronavirus indicating person-to-person transmission: A study of a family cluster. Lancet, 395(10223): 514–523

    CAS  Article  Google Scholar 

  6. Chen N S, Zhou M, Dong X, Qu J M, Gong F Y, Han Y, Qiu Y, Wang J L, Liu Y, Wei Y, Xia J A, Yu T, Zhang X X, Zhang L (2020). Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: A descriptive study. Lancet, 395(10223): 507–513

    CAS  Article  Google Scholar 

  7. Chia P Y, Coleman K K, Tan Y K, Ong S W X, Gum M, Lau S K, Lim X F, Lim A S, Sutjipto S, Lee P H, Son T T, Young B E, Milton D K, Gray G C, Schuster S, Barkham T, De P P, Vasoo S, Chan M, Ang B S P, Tan B H, Leo Y S, Ng O T, Wong M S Y, Marimuthu K (2020). Detection of air and surface contamination by SARS-CoV-2 in hospital rooms of infected patients. Nature Communications, 11(1): 2800

    CAS  Article  Google Scholar 

  8. Fabian P, McDevitt J J, DeHaan W H, Fung ROP, 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(7): e2691

    Article  Google Scholar 

  9. Gralton J, Tovey E, McLaws M L, Rawlinson W D (2011). The role of particle size in aerosolised pathogen transmission: A review. Journal of Infection, 62(1): 1–13

    Article  Google Scholar 

  10. Gralton J, Tovey E R, Mclaws M L, Rawlinson W D (2013). Respiratory virus RNA is detectable in airborne and droplet particles. Journal of Medical Virology, 85(12): 2151–2159

    CAS  Article  Google Scholar 

  11. Guo Z D, Wang Z Y, Zhang S F, Li X, Li L, Li C, Cui Y, Fu R B, Dong Y Z, Chi X Y, Zhang M Y, Liu K, Cao C, Liu B, Zhang K, Gao Y W, Lu B, Chen W (2020). Aerosol and surface distribution of severe acute respiratory syndrome coronavirus 2 in hospital wards, Wuhan, China, 2020. Emerging Infectious Diseases, 26(7): 1583–1591

    Article  Google Scholar 

  12. Huang C L, Wang Y M, Li X W, Ren L L, Zhao J P, Hu Y, Zhang L, Fan G H, Xu J Y, Gu X Y, Cheng Z S, Yu T, Xia J A, Wei Y, Wu W J, Xie X L, Yin W, Li H, Liu M, Xiao Y, Gao H, Guo L, Xie J G, Wang G F, Jiang R M, Gao Z C, Jin Q, Wang J W, Cao B (2020). Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet, 395(10223): 497–506

    CAS  Article  Google Scholar 

  13. Jiang J K, Vincent Fu Y, Liu L, Kulmala M (2020a). Transmission via aerosols: Plausible differences among emerging coronaviruses. Aerosol Science and Technology, 54(8): 865–868

    CAS  Article  Google Scholar 

  14. Jiang Y F, Wang H F, Chen Y K, He J X, Chen L G, Liu Y, Hu X Y, Li A, Liu S W, Zhang P, Zou H Y, Hua S C (2020b). Clinical data on hospital environmental hygiene monitoring and medical staffs protection during the coronavirus disease 2019 outbreak. New York: medRxiv preprint

  15. Kampf G, Todt D, Pfaender S, Steinmann E (2020). Persistence of coronaviruses on inanimate surfaces and their inactivation with biocidal agents. Journal of Hospital Infection, 104(3): 246–251

    CAS  Article  Google Scholar 

  16. Lau H, Khosrawipour T, Kocbach P, Ichii H, Bania J, Khosrawipour V (2020). Evaluating the massive underreporting and undertesting of COVID-19 cases in multiple global epicenters. Pulmonology

  17. Leung N H L, Chu D K W, Shiu E Y C, Chan K H, McDevitt J J, Hau B J P, Yen H L, Li Y G, Ip D K M, Peiris J S M, Seto W H, Leung G M, Milton D K, Cowling B J (2020). Respiratory virus shedding in exhaled breath and efficacy of face masks. Nature Medicine, 26(5): 676–680

    CAS  Article  Google Scholar 

  18. Li Q, Guan X H, Wu P, Wang X Y, Zhou L, Tong Y Q, Ren R Q, Leung K S M, Lau E H Y, Wong J Y, Xing X S, Xiang N J, Wu Y, Li C, Chen Q, Li D, Liu T, Zhao J, Liu M, Tu W X, Chen C D, Jin L M, Yang R, Wang Q, Zhou S H, Wang R, Liu H, Luo Y B, Liu Y, Shao G, Li H, Tao Z F, Yang Y, Deng Z Q, Liu B X, Ma Z T, Zhang Y P, Shi G Q, Lam T T Y, Wu J T, Gao G F, Cowling B J, Yang B, Leung G M, Feng Z J (2020). Early transmission dynamics in Wuhan, China, of novel coronavirus-infected pneumonia. The New England Journal of Medicine, 382(13): 1199–1207

    CAS  Article  Google Scholar 

  19. Liu Q H, Liu Z C, Zhu J K, Zhu Y H, Li D Q, Gao Z F, Zhou L L, Tang Y B, Zhang X, Yang J Y, Wang Q (2020a). Assessing the Global Tendency of COVID-19 Outbreak. New York: medRxiv preprint

  20. Liu Y, Ning Z, Chen Y, Guo M, Liu Y L, Gali N K, Sun L, Duan Y S, Cai J, Westerdahl D, Liu X J, Xu K, Ho K F, Kan H D, Fu Q Y, Lan K (2020b). Aerodynamic analysis of SARS-CoV-2 in two Wuhan hospitals. Nature, 582: 557–560

    CAS  Article  Google Scholar 

  21. Ma Y L, Zhao Y D, Liu J T, He X T, Wang B, Fu S H, Yan J, Niu J P, Luo B (2020). Effects of temperature variation and humidity on the mortality of COVID-19 in Wuhan. New York: medRxiv preprint McMichael T M, Currie D W, Clark S, Pogosjans S, Kay M, Schwartz N G, Lewis J, Baer A, Kawakami V, Lukoff M D, Ferro J, Brostrom-Smith C, Rea T D, Sayre M R, Riedo F X, Russell D, Hiatt B, Montgomery P, Rao A K, Chow E J, Tobolowsky F, Hughes M J, Bardossy A C, Oakley L P, Jacobs J R, Stone N D, Reddy S C, Jernigan J A, Honein M A, Clark T A, Duchin J S (2020). Epidemiology of Covid-19 in a long-term care facility in King County, Washington. The New England Journal of Medicine, 382(21): 2005–2011

    Article  Google Scholar 

  22. Milton D K, Fabian M P, Cowling B J, Grantham M L, McDevitt J J (2013). Influenza virus aerosols in human exhaled breath: particle size, culturability, and effect of surgical masks. PLoS Pathogens, 9(3): e1003205

    CAS  Article  Google Scholar 

  23. Myatt T A, Johnston S L, Zuo Z F, Wand M, Kebadze T, Rudnick S, Milton D K (2004). Detection of airborne rhinovirus and its relation to outdoor air supply in office environments. American Journal of Respiratory and Critical Care Medicine, 169(11): 1187–1190

    Article  Google Scholar 

  24. Pan X F, Chen D X, Xia Y, Wu X W, Li T S, Ou X T, Zhou L Y, Liu J (2020). Asymptomatic cases in a family cluster with SARS-CoV-2 infection. Lancet. Infectious Diseases, 20(4): 410–411

    CAS  Google Scholar 

  25. Phan L T, Nguyen T V, Luong Q C, Nguyen T V, Nguyen H T, Le H Q, Nguyen T T, Cao T M, Pham Q D (2020). Importation and human-to-human transmission ofa novel coronavirus in Vietnam. New England Journal of Medicine, 382(9): 872–874

    Article  Google Scholar 

  26. Rockx B, Kuiken T, Herfst S, Bestebroer T, Lamers M M, Oude Munnink B B, de Meulder D, van Amerongen G, van den Brand J, Okba N M A, Schipper D, van Run P, Leijten L, Sikkema R, Verschoor E, Verstrepen B, Bogers W, Langermans J, Drosten C, Fentener van Vlissingen M, Fouchier R, de Swart R, Koopmans M, Haagmans B L (2020). Comparative pathogenesis of COVID-19, MERS, and SARS in a nonhuman primate model. Science, 368(6494): 1012–1015

    CAS  Article  Google Scholar 

  27. Rothe C, Schunk M, Sothmann P, Bretzel G, Froeschl G, Wallrauch C, Zimmer T, Thiel V, Janke C, Guggemos W, Seilmaier M, Drosten C, Vollmar P, Zwirglmaier K, Zange S, Wölfel R, Hoelscher M (2020). Transmission of 2019-nCoV infection from an asymptomatic contact in Germany. The New England Journal of Medicine, 382(10): 970–971

    Article  Google Scholar 

  28. Roy C J, Milton D K (2004). Airborne transmission of communicable infection: The elusive pathway. New England Journal of Medicine, 350(17): 1710–1712

    CAS  Article  Google Scholar 

  29. Santarpia J L, Rivera D N, Herrera V L, Morwitzer M J, Creager H M, Santarpia G W, Crown K K, Brett-Major D M, Schnaubelt E R, Broadhurst M J, Lawler J V, Reid S P, Lowe J J (2020). Aerosol and surface contamination of SARS-CoV-2 observed in quarantine and isolation care. Scientific Reports, 10(1): 12732

    CAS  Article  Google Scholar 

  30. Setti L, Passarini F, De Gennaro G, Barbieri P, Perrone M G, Borelli M, Palmisani J, Di Gilio A, Torboli V, Fontana F, Clemente L, Pallavicini A, Ruscio M, Piscitelli P, Miani A (2020). SARS-Cov-2RNA found on particulate matter of Bergamo in Northern Italy: First evidence. Environmental Research, 188: 109754

    CAS  Article  Google Scholar 

  31. Siegel J D, Rhinehart E, Jackson M, Chiarello L (2007). Guideline for isolation precautions: preventing transmission of infectious agents in healthcare settings. American Journal of Infection Control, 35(10): S65–S164

    Article  Google Scholar 

  32. Sooryanarain H, Elankumaran S (2015). Environmental role in influenza virus outbreaks. Annual Review of Animal Biosciences, 3(1): 347–373

    Article  Google Scholar 

  33. Tellier R, Li Y G, Cowling B J, Tang J W (2019). Recognition of aerosol transmission of infectious agents: A commentary. BMC Infectious Diseases, 19: 101

    Article  Google Scholar 

  34. Wang W E, Tang J M, Wei F Q (2020). Updated understanding of the outbreak of 2019 novel coronavirus (2019-nCoV) in Wuhan, China. Journal of Medical Virology, 92(4): 441–447

    CAS  Article  Google Scholar 

  35. World Health Organization (2014). Infection prevention and control of epidemic- and pandemic-prone acute respiratory infections in health care. Geneva: World Health Organization https://apps.who.int/iris/handle/10665/112656

    Google Scholar 

  36. Xu B, Gutierrez B, Mekaru S, Sewalk K, Goodwin L, Loskill A, Cohn E L, Hswen Y, Hill S C, Cobo M M, Zarebski A E, Li S, Wu C, Hulland E, Morgan J D, Wang L, O’Brien K, Scarpino S V, Brownstein J S, Pybus O G, Pigott D M, Kraemer M U G (2020a). Epidemiological data from the COVID-19 outbreak, real-time case information. Scientific Data, 7(1): 106

    CAS  Article  Google Scholar 

  37. Xu R, Rahmandad H, Gupta M, DiGennaro C, Ghaffarzadegan N, Amini H, Jalali M S (2020b). The modest impact of weather and air pollution on COVID-19 transmission. New York: medRxiv preprint

  38. Yao M S, Zhang L, Ma J X, Zhou L (2020). On airborne transmission and control of SARS-Cov-2. Science of the Total Environment, 731: 139178

    CAS  Article  Google Scholar 

  39. Zhang X L, Ji Z, Yue Y, Liu H, Wang J (2020). Infection risk assessment of COVID-19 through aerosol transmission: a case study of South China Seafood Market. Environmental Science & Technology

  40. Zhu N, Zhang D Y, Wang W L, Li X W, Yang B Y, Song J D, Zhao X, Huang B Y, Shi W F, Lu R J, Niu P H, Zhan F X, Ma X J, Wang D Y, Xu W B, Wu G Z, Gao G F, Tan W J (2020). A novel coronavirus from patients with pneumonia in China, 2019. The New England Journal of Medicine, 382(8): 727–733

    CAS  Article  Google Scholar 

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Acknowledgements

This research was supported by the Key Technologies R&D Program of Tianjin (No. 20ZXGBSY00100)

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Correspondence to Can Wang.

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Highlights

• Aerosol transmission is an indispensable route of COVID-19 spread.

• Different outbreak sites have different epidemiologic feature.

• SRAS-CoV-2 can exist for a long time in aerosol.

• SRAS-CoV-2 RNA can be detected in aerosol in diverse places.

• Some environmental factors can impact SARS-CoV-2 transportation in aerosol.

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Jiang, G., Wang, C., Song, L. et al. Aerosol transmission, an indispensable route of COVID-19 spread: case study of a department-store cluster. Front. Environ. Sci. Eng. 15, 46 (2021). https://doi.org/10.1007/s11783-021-1386-6

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Keywords

  • SARS-CoV-2
  • COVID-19
  • Environmental factor
  • Aerosol transmission
  • Epidemiologic characteristic