[Skip to Content]
Access to paid content on this site is currently suspended due to excessive activity being detected from your IP address Please contact the publisher to request reinstatement.
[Skip to Content Landing]
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
 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
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
Pagano  M, Gauvreau  K.  Principles of Biostatistics. CRC Press; 2018.
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
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
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
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
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
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
Limit 200 characters
Limit 25 characters
Conflicts of Interest Disclosure

Identify all potential conflicts of interest that might be relevant to your comment.

Conflicts of interest comprise financial interests, activities, and relationships within the past 3 years including but not limited to employment, affiliation, grants or funding, consultancies, honoraria or payment, speaker's bureaus, stock ownership or options, expert testimony, royalties, donation of medical equipment, or patents planned, pending, or issued.

Err on the side of full disclosure.

If you have no conflicts of interest, check "No potential conflicts of interest" in the box below. The information will be posted with your response.

Not all submitted comments are published. Please see our commenting policy for details.

Limit 140 characters
Limit 3600 characters or approximately 600 words
    4 Comments for this article
    Were any of the riders wearing masks?
    David Eldredge |
    A question asked by one of my Twitter followers, were any of the bus riders or even the index individual wearing masks?

    Fascinating Study!
    Gary Ordog, MD, DABEM, DABMT | County of Los Angeles, Department of Health Services, (retired)
    First to answer the previous question, I believe it is stated in the article that no one was wearing masks, as a COVID-19 outbreak had not been identified at that time. My point here is that you have a fascinating article, that was extremely well done. Thank you and congratulations. I would like to see the next phase of a similar study using PPE. We already know that health care workers have a higher risk of infection despite using PPE. But it obviously helps. You study confirms the proverbial "sardine can" analogy, avoid buses, trains, planes and indoor restaurants in this time of COVID-19. Again, excellent study!
    NYT article says none of the worshipers wore masks.
    Peter Liepmann, MD MBA | NA
    Presumably the writers had access to the full article.

    "None of the worshipers wore masks."
    "But a version of the study published in China says the individual was a 64-year-old woman and that she developed symptoms on Jan. 18, a day after dining with guests from Hubei and a day before going to the temple. She took medicine but did not see a doctor."
    Persuasive study
    Julio Ozores, MD | Student Health and Counseling, UCSF
    Methodical, persuasive report or a study that capitalized beautifully on a fortuitous, natural experiment. Thank you, authors.
    Views 85,210
    Citations 0
    Original Investigation
    September 1, 2020

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

    Author Affiliations
    • 1Department of Epidemiology and Biostatistics, University of Georgia College of Public Health, Athens
    • 2Department of Epidemiology, Tulane University School of Public Health and Tropical Medicine, New Orleans, Louisiana
    • 3Ningbo Municipal Center for Disease Control and Prevention, Ningbo, China
    • 4Zhejiang Provincial Center for Disease Control and Prevention, Hangzhou, China
    • 5Division of Infectious Diseases and Geographic Medicine, Stanford University School of Medicine, Stanford, California
    • 6Hangzhou Municipal Center for Disease Control and Prevention, Hangzhou, China
    • 7Health Informatics Institute, University of Georgia College of Public Health, Athens
    • 8Center for the Ecology of Infectious Diseases, University of Georgia, Athens
    • 9Renmin University of China School of Statistics, Beijing, China
    • 10Statistical Consulting Center, Renmin University of China, Beijing, China
    • 11Haishu Center for Disease Control and Prevention, Ningbo, China
    • 12Department of Health Care Administration, California State University Long Beach, College of Health and Human Services, Long Beach
    • 13Department of Clinical Epidemiology and Tobacco Dependence Treatment Research, Beijing Chaoyang Hospital, Beijing, China
    • 14Center for Applied Statistics, Renmin University of China, Beijing, China
    JAMA Intern Med. Published online September 1, 2020. doi:10.1001/jamainternmed.2020.5225
    Key Points

    Question  Is airborne transmission of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) a potential mean 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.


    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.