Community Outbreak Investigation of SARS-CoV-2 Transmission Among Bus Riders in Eastern China | Global Health | JN Learning | AMA Ed Hub [Skip to Content]
Access to paid content on this site is currently suspended due to excessive activity being detected from your IP address 18.206.177.17. Please contact the publisher to request reinstatement.
[Skip to Content Landing]

Community Outbreak Investigation of SARS-CoV-2 Transmission Among Bus Riders in Eastern China

Educational Objective
To understand the transmission rate of COVID-19 among bus riders in Eastern China
1 Credit CME
Key Points

Question  Is airborne transmission of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) a potential means of spreading coronavirus disease 2019 (COVID-19)?

Findings  In this cohort study of 128 individuals who rode 1 of 2 buses and attended a worship event in Eastern China, those who rode a bus with air recirculation and with a patient with COVID-19 had an increased risk of SARS-CoV-2 infection compared with those who rode a different bus. Airborne transmission may partially explain the increased risk of SARS-CoV-2 infection among these bus riders.

Meaning  These results suggest that future efforts at prevention and control must consider the potential for airborne spread of SARS-CoV-2, which is a highly transmissible pathogen in closed environments with air recirculation.

Abstract

Importance  Evidence of whether severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the virus that causes coronavirus disease 2019 (COVID-19), can be transmitted as an aerosol (ie, airborne) has substantial public health implications.

Objective  To investigate potential transmission routes of SARS-CoV-2 infection with epidemiologic evidence from a COVID-19 outbreak.

Design, Setting, and Participants  This cohort study examined a community COVID-19 outbreak in Zhejiang province. On January 19, 2020, 128 individuals took 2 buses (60 [46.9%] from bus 1 and 68 [53.1%] from bus 2) on a 100-minute round trip to attend a 150-minute worship event. The source patient was a passenger on bus 2. We compared risks of SARS-CoV-2 infection among at-risk individuals taking bus 1 (n = 60) and bus 2 (n = 67 [source patient excluded]) and among all other individuals (n = 172) attending the worship event. We also divided seats on the exposed bus into high-risk and low-risk zones according to the distance from the source patient and compared COVID-19 risks in each zone. In both buses, central air conditioners were in indoor recirculation mode.

Main Outcomes and Measures  SARS-CoV-2 infection was confirmed by reverse transcription polymerase chain reaction or by viral genome sequencing results. Attack rates for SARS-CoV-2 infection were calculated for different groups, and the spatial distribution of individuals who developed infection on bus 2 was obtained.

Results  Of the 128 participants, 15 (11.7%) were men, 113 (88.3%) were women, and the mean age was 58.6 years. On bus 2, 24 of the 68 individuals (35.3% [including the index patient]) received a diagnosis of COVID-19 after the event. Meanwhile, none of the 60 individuals in bus 1 were infected. Among the other 172 individuals at the worship event, 7 (4.1%) subsequently received a COVID-19 diagnosis. Individuals in bus 2 had a 34.3% (95% CI, 24.1%-46.3%) higher risk of getting COVID-19 compared with those in bus 1 and were 11.4 (95% CI, 5.1-25.4) times more likely to have COVID-19 compared with all other individuals attending the worship event. Within bus 2, individuals in high-risk zones had moderately, but nonsignificantly, higher risk for COVID-19 compared with those in the low-risk zones. The absence of a significantly increased risk in the part of the bus closer to the index case suggested that airborne spread of the virus may at least partially explain the markedly high attack rate observed.

Conclusions and Relevance  In this cohort study and case investigation of a community outbreak of COVID-19 in Zhejiang province, individuals who rode a bus to a worship event with a patient with COVID-19 had a higher risk of SARS-CoV-2 infection than individuals who rode another bus to the same event. Airborne spread of SARS-CoV-2 seems likely to have contributed to the high attack rate in the exposed bus. Future efforts at prevention and control must consider the potential for airborne spread of the virus.

Sign in to take quiz and track your certificates

Buy This Activity

JN Learning™ is the home for CME and MOC from the JAMA Network. Search by specialty or US state and earn AMA PRA Category 1 CME Credit™ from articles, audio, Clinical Challenges and more. Learn more about CME/MOC

Article Information

Accepted for Publication: August 11, 2020.

Published Online: September 1, 2020. doi:10.1001/jamainternmed.2020.5225

Correction: This article was corrected on January 25, 2021, to update information about the index patient and to add an omitted acknowledgment to thank the index patient and her family members for granting permission to publish this information.

Corresponding Authors: Feng Ling, MD, Zhejiang Provincial Center for Disease Control and Prevention, 3399 Binsheng Rd, Hangzhou, China (fengl@cdc.zj.cn); Guozhang Xu, MD, Ningbo Municipal Center for Disease Control and Prevention, 237 Yongfeng Rd, Ningbo, China (xugz@nbcdc.org.cn).

Author Contributions: Dr Ling had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Drs Shen, C. Li, Dong, Z. Wang, and Y. Li are co–first authors. Drs Ling, J. Chen, and Xu are co–senior authors.

Conflict of Interest Disclosures: None reported.

Funding/Support: This study was funded by a Ningbo Science and Technology Major Project Grant (2020C50001) and Zhejiang Science and Technology Major Project Grant (2020C03124).

Role of the Funder/Sponsor: The funding organizations had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

Additional Contributions: We thank the index patient and her family members for granting permission to publish this information.

References
1.
Li  Q , Guan  X , Wu  P ,  et al.  Early transmission dynamics in Wuhan, China, of novel coronavirus-infected pneumonia.   N Engl J Med. 2020;382(13):1199-1207. doi:10.1056/NEJMoa2001316 PubMedGoogle ScholarCrossref
2.
Chen  N , Zhou  M , Dong  X ,  et al.  Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study.   Lancet. 2020;395(10223):507-513. doi:10.1016/S0140-6736(20)30211-7 PubMedGoogle ScholarCrossref
3.
World Health Organization. Coronavirus disease 2019 (COVID-19) situation report—197. Accessed August 5, 2020. https://www.who.int/docs/default-source/coronaviruse/situation-reports/20200804-covid-19-sitrep-197.pdf?sfvrsn=94f7a01d_2
4.
Chan  JF-W , Yuan  S , Kok  K-H ,  et al.  A familial cluster of infection associated with the 2019 novel coronavirus indicating possible person-to-person transmission during the incubation period.   Lancet. 2020;395(10223):514-523. doi:10.1016/S0140-6736(20)30154-9 PubMedGoogle ScholarCrossref
5.
Yu  P , Zhu  J , Zhang  Z , Han  Y , Huang  L .  A familial cluster of infection associated with the 2019 novel coronavirus indicating potential person-to-person transmission during the incubation period.   J Infect Dis. 2020;221(11):1757-1761. doi:10.1093/infdis/jiaa077 PubMedGoogle ScholarCrossref
6.
Phan  LT , Nguyen  TV , Luong  QC ,  et al.  Importation and human-to-human transmission of a novel coronavirus in Vietnam.   N Engl J Med. 2020;382(9):872-874. doi:10.1056/NEJMc2001272 PubMedGoogle ScholarCrossref
7.
Tellier  R , Li  Y , Cowling  BJ , Tang  JW .  Recognition of aerosol transmission of infectious agents: a commentary.   BMC Infect Dis. 2019;19(1):101. doi:10.1186/s12879-019-3707-y PubMedGoogle ScholarCrossref
8.
Jones  RM , Brosseau  LM .  Aerosol transmission of infectious disease.   J Occup Environ Med. 2015;57(5):501-508. doi:10.1097/JOM.0000000000000448 PubMedGoogle ScholarCrossref
9.
Wong  TW , Lee  CK , Tam  W ,  et al; Outbreak Study Group.  Cluster of SARS among medical students exposed to single patient, Hong Kong.   Emerg Infect Dis. 2004;10(2):269-276. doi:10.3201/eid1002.030452 PubMedGoogle ScholarCrossref
10.
Olsen  SJ , Chang  HL , Cheung  TY ,  et al.  Transmission of the severe acute respiratory syndrome on aircraft.   N Engl J Med. 2003;349(25):2416-2422. doi:10.1056/NEJMoa031349 PubMedGoogle ScholarCrossref
11.
Yu  IT , Li  Y , Wong  TW ,  et al.  Evidence of airborne transmission of the severe acute respiratory syndrome virus.   N Engl J Med. 2004;350(17):1731-1739. doi:10.1056/NEJMoa032867 PubMedGoogle ScholarCrossref
12.
Nishiura  H , Oshitani  H , Kobayashi  T ,  et al.  Closed environments facilitate secondary transmission of coronavirus disease 2019 (COVID-19).   medRxiv. Preprint posted online March 3, 2020. doi:10.1101/2020.02.28.20029272Google Scholar
13.
Hodcroft  EB .  Preliminary case report on the SARS-CoV-2 cluster in the UK, France, and Spain.   Swiss Med Wkly. 2020;150(9-10). doi:10.4414/smw.2020.20212 PubMedGoogle Scholar
14.
van Doremalen  N , Bushmaker  T , Morris  DH ,  et al.  Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1.   N Engl J Med. 2020;382(16):1564-1567. doi:10.1056/NEJMc2004973 PubMedGoogle ScholarCrossref
15.
Kim  YI , Kim  SG , Kim  SM ,  et al.  Infection and rapid transmission of SARS-CoV-2 in ferrets.   Cell Host Microbe. 2020;27(5):704-709.e2. doi:10.1016/j.chom.2020.03.023PubMedGoogle ScholarCrossref
16.
Richard  M , Kok  A , de Meulder  D ,  et al.  SARS-CoV-2 is transmitted via contact and via the air between ferrets.   Nat Commun. 2020;11(1):3496. doi:10.1038/s41467-020-17367-2 PubMedGoogle ScholarCrossref
17.
 WHO recommended measures for persons undertaking international travel from areas affected by severe acute respiratory syndrome (SARS).   Wkly Epidemiol Rec. 2003;78(14):97-99.PubMedGoogle Scholar
18.
Hertzberg  VS , Weiss  H .  On the 2-row rule for infectious disease transmission on aircraft.   Ann Glob Health. 2016;82(5):819-823. doi:10.1016/j.aogh.2016.06.003 PubMedGoogle ScholarCrossref
19.
Pagano  M , Gauvreau  K.   Principles of Biostatistics. CRC Press; 2018.
20.
Arons  MM , Hatfield  KM , Reddy  SC ,  et al; Public Health–Seattle and King County and CDC COVID-19 Investigation Team.  Presymptomatic SARS-CoV-2 infections and transmission in a skilled nursing facility.   N Engl J Med. 2020;382(22):2081-2090. doi:10.1056/NEJMoa2008457 PubMedGoogle ScholarCrossref
21.
He  X , Lau  EHY , Wu  P ,  et al.  Temporal dynamics in viral shedding and transmissibility of COVID-19.   Nat Med. 2020;26(5):672-675. doi:10.1038/s41591-020-0869-5 PubMedGoogle ScholarCrossref
22.
Lu  J , Gu  J , Li  K ,  et al.  COVID-19 outbreak associated with air conditioning in restaurant, Guangzhou, China, 2020.   Emerg Infect Dis. 2020;26(7):1628-1631. doi:10.3201/eid2607.200764 PubMedGoogle ScholarCrossref
23.
Moser  MR , Bender  TR , Margolis  HS , Noble  GR , Kendal  AP , Ritter  DG .  An outbreak of influenza aboard a commercial airliner.   Am J Epidemiol. 1979;110(1):1-6. doi:10.1093/oxfordjournals.aje.a112781 PubMedGoogle ScholarCrossref
24.
Liu  Y , Ning  Z , Chen  Y ,  et al.  Aerodynamic analysis of SARS-CoV-2 in two Wuhan hospitals.   Nature. 2020;582(7813):557-560. doi:10.1038/s41586-020-2271-3 PubMedGoogle ScholarCrossref
25.
Ong  SWX , Tan  YK , Chia  PY ,  et al.  Air, surface environmental, and personal protective equipment contamination by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) from a symptomatic patient.   JAMA. 2020;232(16):1610-1612. doi:10.1001/jama.2020.3227 PubMedGoogle ScholarCrossref
If you are not a JN Learning subscriber, you can either:
Subscribe to JN Learning for one year
Buy this activity
jn-learning_Modal_Multimedia_LoginSubscribe_Purchase
Close
If you are not a JN Learning subscriber, you can either:
Subscribe to JN Learning for one year
Buy this activity
jn-learning_Modal_Multimedia_LoginSubscribe_Purchase
Close
With a personal account, you can:
  • Access free activities and track your credits
  • Personalize content alerts
  • Customize your interests
  • Fully personalize your learning experience
Education Center Collection Sign In Modal Right
Close

Name Your Search

Save Search
Close
With a personal account, you can:
  • Track your credits
  • Personalize content alerts
  • Customize your interests
  • Fully personalize your learning experience
jn-learning_Modal_SaveSearch_NoAccess_Purchase
Close

Lookup An Activity

or

Close

My Saved Searches

You currently have no searches saved.

Close
With a personal account, you can:
  • Access free activities and track your credits
  • Personalize content alerts
  • Customize your interests
  • Fully personalize your learning experience
Education Center Collection Sign In Modal Right
Close