Mechanistic transmission modeling of COVID-19 on the Diamond Princess cruise ship demonstrates the importance of aerosol transmission

Edited by Andrea Rinaldo, École Polytechnique Fédérale de Lausanne, Lausanne, Switzerland, and approved January 7, 2021 (received for review July 22, 2020)
February 3, 2021
118 (8) e2015482118

Significance

We find that airborne transmission likely accounted for >50% of disease transmission on the Diamond Princess cruise ship, which includes inhalation of aerosols during close contact as well as longer range. These findings underscore the importance of implementing public health measures that target the control of inhalation of aerosols in addition to ongoing measures targeting control of large-droplet and fomite transmission, not only aboard cruise ships but in other indoor environments as well. Guidance from health organizations should include a greater emphasis on controls for reducing spread by airborne transmission. Last, although our work is based on a cruise ship outbreak of COVID-19, the model approach can be applied to other indoor environments and other infectious diseases.

Abstract

Several lines of existing evidence support the possibility of airborne transmission of coronavirus disease 2019 (COVID-19). However, quantitative information on the relative importance of transmission pathways of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) remains limited. To evaluate the relative importance of multiple transmission routes for SARS-CoV-2, we developed a modeling framework and leveraged detailed information available from the Diamond Princess cruise ship outbreak that occurred in early 2020. We modeled 21,600 scenarios to generate a matrix of solutions across a full range of assumptions for eight unknown or uncertain epidemic and mechanistic transmission factors. A total of 132 model iterations met acceptability criteria (R2 > 0.95 for modeled vs. reported cumulative daily cases and R2 > 0 for daily cases). Analyzing only these successful model iterations quantifies the likely contributions of each defined mode of transmission. Mean estimates of the contributions of short-range, long-range, and fomite transmission modes to infected cases across the entire simulation period were 35%, 35%, and 30%, respectively. Mean estimates of the contributions of larger respiratory droplets and smaller respiratory aerosols were 41% and 59%, respectively. Our results demonstrate that aerosol inhalation was likely the dominant contributor to COVID-19 transmission among the passengers, even considering a conservative assumption of high ventilation rates and no air recirculation conditions for the cruise ship. Moreover, close-range and long-range transmission likely contributed similarly to disease progression aboard the ship, with fomite transmission playing a smaller role. The passenger quarantine also affected the importance of each mode, demonstrating the impacts of the interventions.

Continue Reading

Data Availability

Code have been deposited in Zenodo (https://zenodo.org/record/3955528#.XxfUqp5KjIU).

Supporting Information

Appendix (PDF)

References

1
D. Lewis, Is the coronavirus airborne? Experts can’t agree. Nature 580, 175 (2020).
2
WHO, Modes of transmission of virus causing COVID-19: Implications for IPC precaution recommendations. Scientific Brief (2020). https://www.who.int/news-room/commentaries/detail/modes-of-transmission-of-virus-causing-covid-19-implications-for-ipc-precaution-recommendations. Accessed 22 July 2020.
4
CDC, Scientific brief: SARS-CoV-2 and potential airborne transmission. Coronavirus disease 2019 (COVID-19) (2020). https://www.cdc.gov/coronavirus/2019-ncov/more/scientific-brief-sars-cov-2.html. Accessed 25 November 2020.
5
L. Morawska, J. Cao, Airborne transmission of SARS-CoV-2: The world should face the reality. Environ. Int. 139, 105730 (2020).
6
P. Bahl et al., Airborne or droplet precautions for health workers treating COVID-19? J.Infect. Dis., (2020).
7
K. A. Prather, C. C. Wang, R. T. Schooley, Reducing transmission of SARS-CoV-2. Science 368, 1422–1424 (2020).
8
L. Morawska et al., How can airborne transmission of COVID-19 indoors be minimised? Environ. Int. 142, 105832 (2020).
9
S. J. Dancer et al., Putting a balance on the aerosolization debate around SARS-CoV-2. J. Hosp. Infect. 105, 569–570 (2020).
10
S. Asadi, N. Bouvier, A. S. Wexler, W. D. Ristenpart, The coronavirus pandemic and aerosols: Does COVID-19 transmit via expiratory particles? Aerosol Sci. Technol. 0, 1–4 (2020).
11
National Academies of Sciences, Engineering, and Medicine, Rapid Expert Consultation on SARS-CoV-2 Viral Shedding and Antibody Response for the COVID-19 Pandemic (April 8, 2020) (National Academies Press, 2020).
12
E. A. Nardell, R. R. Nathavitharana, Airborne spread of SARS-CoV-2 and a potential role for air disinfection. JAMA 324, 141–142 (2020).
13
J. Allen, L. Marr, Re-thinking the potential for airborne transmission of SARS-CoV-2. https://doi.org/10.20944/preprints202005.0126.v1 (15 June 2020).
14
L. Morawska, D. K. Milton, It is time to address airborne transmission of Coronavirus disease 2019 (COVID-19). Clinical Infect. Dis. 71, 2311–2313 (2020).
15
F. C. Fang et al., COVID-19—lessons learned and questions remaining. Clinical Infect. Dis., (2020).
16
ASHRAE, “ASHRAE issues statements on relationship between COVID-19 and HVAC in buildings” (2020). https://www.ashrae.org/about/news/2020/ashrae-issues-statements-on-relationship-between-covid-19-and-hvac-in-buildings. Accessed 22 July 2020.
17
L. Bourouiba, Turbulent gas clouds and respiratory pathogen emissions: Potential implications for reducing transmission of COVID-19. JAMA 323, 1837–1838 (2020).
18
V. Stadnytskyi, C. E. Bax, A. Bax, P. Anfinrud, The airborne lifetime of small speech droplets and their potential importance in SARS-CoV-2 transmission. Proc. Natl. Acad. Sci. U.S.A. 117, 11875–11877 (2020).
19
R. Tellier, Y. Li, B. J. Cowling, J. W. Tang, Recognition of aerosol transmission of infectious agents: A commentary. BMC Infect. Dis. 19, 101 (2019).
20
P. Y. Chia et al.; Singapore 2019 Novel Coronavirus Outbreak Research Team, Detection of air and surface contamination by SARS-CoV-2 in hospital rooms of infected patients. Nat. Commun. 11, 2800 (2020).
21
Y. Liu et al., Aerodynamic analysis of SARS-CoV-2 in two Wuhan hospitals. Nature 582, 557–560 (2020).
22
J. L. Santarpia et al., Aerosol and surface contamination of SARS-CoV-2 observed in quarantine and isolation care. Sci. Rep. 10, 12732 (2020).
23
J. A. Lednicky et al., Collection of SARS-CoV-2 virus from the air of a clinic within a university student health care center and analyses of the viral genomic sequence. Aerosol Air Qual. Res. 20, 1167–1171 (2020).
24
J. A. Lednicky et al., Viable SARS-CoV-2 in the air of a hospital room with COVID-19 patients. Int. J. Infect. Dis. 100, 476–482 (2020).
25
K. Nissen et al., Long-distance airborne dispersal of SARS-CoV-2 in COVID-19 wards. Sci. Rep. 10, 19589 (2020).
26
Y. Li et al., Evidence for probable aerosol transmission of SARS-CoV-2 in a poorly ventilated restaurant. Infectious Diseases (except HIV/AIDS). https://doi.org/10.1101/2020.04.16.20067728 (31 May 2020).
27
S. L. Miller et al., Transmission of SARS‐CoV‐2 by inhalation of respiratory aerosol in the Skagit Valley Chorale superspreading event. Indoor Air, (2020).
28
Y. Shen et al., Community outbreak investigation of SARS-CoV-2 transmission among bus riders in Eastern China. JAMA Intern Med, (2020).
29
E. C. Dick, L. C. Jennings, K. A. Mink, C. D. Wartgow, S. L. Inhorn, Aerosol transmission of rhinovirus colds. J. Infect. Dis. 156, 442–448 (1987).
30
H. Lei et al., Routes of transmission of influenza A H1N1, SARS CoV, and norovirus in air cabin: Comparative analyses. Indoor Air 28, 394–403 (2018).
31
A. N. M. Kraay et al., Fomite-mediated transmission as a sufficient pathway: A comparative analysis across three viral pathogens. BMC Infect. Dis. 18, 540 (2018).
32
S. Xiao, Y. Li, T. W. Wong, D. S. C. Hui, Role of fomites in SARS transmission during the largest hospital outbreak in Hong Kong. PLoS One 12, e0181558 (2017).
33
R. M. Jones, E. Adida, Influenza infection risk and predominate exposure route: Uncertainty analysis. Risk Anal. 31, 1622–1631 (2011).
34
B. Stephens et al., Microbial exchange via fomites and implications for human health. Curr. Pollution Rep. 5, 198–213 (2019).
35
L. F. Moriarty, Public health responses to COVID-19 outbreaks on cruise ships—worldwide, February–March. MMWR Morb. Mortal. Wkly. Rep. 69, 347–352 (2020).
36
Worldometer, February 2020 coronavirus news updates—Worldometer (2020). https://www.worldometers.info/coronavirus/feb-2020-news-updates-covid19/. Accessed 3 April 2020.
37
Princess Cruise Lines, Ltd., Diamond Princess updates—notices and advisories (2020). https://www.princess.com/news/notices_and_advisories/notices/diamond-princess-update.html. Accessed 2 April 2020.
38
G. N. Sze To, C. Y. H. Chao, Review and comparison between the Wells-Riley and dose-response approaches to risk assessment of infectious respiratory diseases. Indoor Air 20, 2–16 (2010).
39
M. Wang, C.-H. Lin, Q. Chen, Advanced turbulence models for predicting particle transport in enclosed environments. Build. Environ. 47, 40–49 (2012).
40
C. Chen, W. Liu, C.-H. Lin, Q. Chen, Comparing the Markov chain model with the Eulerian and Lagrangian models for indoor transient particle transport simulations. Aerosol Sci. Technol. 49, 857–871 (2015).
41
M. Nicas, R. M. Jones, Relative contributions of four exposure pathways to influenza infection risk. Risk Anal. 29, 1292–1303 (2009).
42
M. Nicas, G. Sun, An integrated model of infection risk in a health-care environment. Risk Anal. 26, 1085–1096 (2006).
43
R. M. Jones et al., Characterizing the risk of infection from Mycobacterium tuberculosis in commercial passenger aircraft using quantitative microbial risk assessment. Risk Anal. 29, 355–365 (2009).
44
R. M. Jones, M. Nicas, Benchmarking of a Markov multizone model of contaminant transport. Ann. Occup. Hyg. 58, 1018–1031 (2014).
45
R. M. Jones, M. Nicas, Experimental evaluation of a Markov multizone model of particulate contaminant transport. Ann. Occup. Hyg. 58, 1032–1045 (2014).
46
M. Nicas, D. Best, A study quantifying the hand-to-face contact rate and its potential application to predicting respiratory tract infection. J. Occup. Environ. Hyg. 5, 347–352 (2008).
47
US Department of Homeland Security Science and Technology, Master question list for COVID-19 (caused by SARS-CoV-2): Weekly report (Hazard Awareness and Characterization Technology Center, 2020). https://www.dhs.gov/publication/st-master-question-list-covid-19. Accessed 22 July 2020.
48
A. L. Hartman et al., SARS-CoV-2 infection of African green monkeys results in mild respiratory disease discernible by PET/CT imaging and shedding of infectious virus from both respiratory and gastrointestinal tracts. PLoS Pathog. 16, e1008903 (2020).
49
S. F. Sia et al., Pathogenesis and transmission of SARS-CoV-2 in golden hamsters. Nature 583, 834–838 (2020).
50
W. Chen, N. Zhang, J. Wei, H.-L. Yen, Y. Li, Short-range airborne route dominates exposure of respiratory infection during close contact. medRxiv:2020.03.16.20037291 (20 March 2020).
51
R. M. Jones, Relative contributions of transmission routes for COVID-19 among healthcare personnel providing patient care. J. Occup. Environ. Hyg. 17, 408–415 (2020).
52
E. T. Isakbaeva et al., Norovirus transmission on cruise ship. Emerg. Infect. Dis. 11, 154–158 (2005).
53
R. Vivancos et al., Norovirus outbreak in a cruise ship sailing around the British isles: Investigation and multi-agency management of an international outbreak. J. Infect. 60, 478–485 (2010).

Information & Authors

Information

Published in

The cover image for PNAS Vol.118; No.8
Proceedings of the National Academy of Sciences
Vol. 118 | No. 8
February 23, 2021
PubMed: 33536312

Classifications

Data Availability

Code have been deposited in Zenodo (https://zenodo.org/record/3955528#.XxfUqp5KjIU).

Submission history

Published online: February 3, 2021
Published in issue: February 23, 2021

Keywords

  1. COVID-19
  2. transmission risk model
  3. aerosol transmission
  4. Diamond Princess Cruise Ship
  5. built environment

Notes

This article is a PNAS Direct Submission.

Authors

Affiliations

Environmental Health Department, Harvard T.H. Chan School of Public Health, Boston, MA 02115;
Environmental Health Department, Harvard T.H. Chan School of Public Health, Boston, MA 02115;
Jose Guillermo Cedeno Laurent https://orcid.org/0000-0001-7098-0954
Environmental Health Department, Harvard T.H. Chan School of Public Health, Boston, MA 02115;
Department of Civil, Architectural, and Environmental Engineering, Illinois Institute of Technology, Chicago, IL 60616
Joseph G. Allen1 [email protected]
Environmental Health Department, Harvard T.H. Chan School of Public Health, Boston, MA 02115;

Notes

1
To whom correspondence may be addressed. Email: [email protected] or [email protected].
Author contributions: P.A., B.S., and J.G.A. designed research; P.A., Z.K., and B.S. performed research; P.A., Z.K., J.G.C.L., B.S., and J.G.A. analyzed data; P.A., B.S., and J.G.A. wrote the paper; and P.A., Z.K., J.G.C.L., B.S., and J.G.A. reviewed the paper.

Competing Interests

The authors declare no competing interest.

Metrics & Citations

Metrics

Note: The article usage is presented with a three- to four-day delay and will update daily once available. Due to ths delay, usage data will not appear immediately following publication. Citation information is sourced from Crossref Cited-by service.


Citation statements

Altmetrics

Citations

Export the article citation data by selecting a format from the list below and clicking Export.

Cited by

    Loading...

    View Options

    View options

    PDF format

    Download this article as a PDF file

    DOWNLOAD PDF

    Login options

    Check if you have access through your login credentials or your institution to get full access on this article.

    Personal login Institutional Login

    Recommend to a librarian

    Recommend PNAS to a Librarian

    Purchase options

    Purchase this article to access the full text.

    Single Article Purchase

    Mechanistic transmission modeling of COVID-19 on the Diamond Princess cruise ship demonstrates the importance of aerosol transmission
    Proceedings of the National Academy of Sciences
    • Vol. 118
    • No. 8

    Media

    Figures

    Tables

    Other

    Share

    Share

    Share article link

    Share on social media