Community Outbreak Investigation of SARS-Cov-2 Transmission Among Bus Riders in Eastern China
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Research JAMA Internal Medicine | Original Investigation Community Outbreak Investigation of SARS-CoV-2 Transmission Among Bus Riders in Eastern China Ye Shen, PhD; Changwei Li, PhD; Hongjun Dong, MD; Zhen Wang, MD; Leonardo Martinez, PhD; Zhou Sun, MD; Andreas Handel, PhD; Zhiping Chen, MD; Enfu Chen, MD; Mark H. Ebell, MD, MS; Fan Wang, MA; Bo Yi, MD; Haibin Wang, MD; Xiaoxiao Wang, MD; Aihong Wang, MD; Bingbing Chen, MD; Yanling Qi, PhD; Lirong Liang, MD, PhD; Yang Li, PhD; Feng Ling, MD; Junfang Chen, MD; Guozhang Xu, MD Supplemental content 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. Author Affiliations: Author affiliations are listed at the end of this article. Corresponding Authors: Feng Ling, MD, Zhejiang Provincial Center for Disease Control and Prevention, 3399 Binsheng Rd, Hangzhou, China ([email protected]); Guozhang Xu, MD, Ningbo Municipal Center for Disease Control and Prevention, JAMA Intern Med. 2020;180(12):1665-1671. doi:10.1001/jamainternmed.2020.5225 237 Yongfeng Rd, Ningbo, China Published online September 1, 2020. ([email protected]). (Reprinted) 1665 © 2020 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ by Ramiro Heredia on 12/08/2020 Research Original Investigation Community Outbreak Investigation of SARS-CoV-2 Transmission Among Bus Riders in Eastern China uman infection by the severe acute respiratory syn- drome coronavirus 2 (SARS-CoV-2) was first reported Key Points in late 2019 in Wuhan city of Hubei province in H Question Is airborne transmission of severe acute respiratory 1,2 China. The World Health Organization declared the corona- syndrome coronavirus 2 (SARS-CoV-2) a potential means of virus disease 2019 (COVID-19) outbreak a public health emer- spreading coronavirus disease 2019 (COVID-19)? gency of international concern on January 30, 2020. The Findings In this cohort study of 128 individuals who rode 1 of 2 ongoing epidemic has since affected more than 150 countries buses and attended a worship event in Eastern China, those who and territories. As of August 5, 2020, more than 18 million cases rode a bus with air recirculation and with a patient with COVID-19 have been confirmed and more than 650 000 people have had an increased risk of SARS-CoV-2 infection compared with died.3 those who rode a different bus. Airborne transmission may Greater efforts are needed to contain and combat the vi- partially explain the increased risk of SARS-CoV-2 infection rus; however, much remains unknown about SARS-CoV-2 among these bus riders. transmission, limiting our ability to implement effective in- Meaning These results suggest that future efforts at prevention terventions. Several studies have demonstrated transmis- and control must consider the potential for airborne spread of sion through close contact and respiratory droplets produced SARS-CoV-2, which is a highly transmissible pathogen in closed when an infected person coughs or sneezes.4-6 Whether environments with air recirculation. SARS-CoV-2 can be transmitted as an aerosol (ie, airborne) through inhalation of virus suspended in the air is unknown. Previous studies have suggested possible airborne transmis- firmed cases of COVID-19. Criteria for COVID-19 case defini- sion of other virulent coronaviruses, such as the severe acute tions and disease severity are provided in the eAppendix in respiratory syndrome coronavirus and the Middle East respi- the Supplement. ratory syndrome coronavirus.7-11 Recent reports suggest that closed environments may facilitate secondary transmission of Statistical Analyses SARS-CoV-2.12,13 An experimental study demonstrated that Attack rates were estimated as the number of diagnosed SARS-CoV-2 can remain viable in aerosols for 3 hours or COVID-19 cases divided by the total number of people at risk, longer,14 and experimental evidence of transmission of SARS- excluding the source patient of the outbreak. We compared the CoV-2 between ferrets via the air was also established.15,16 risk of COVID-19 between individuals taking the exposed bus Therefore, evidence supporting the potential for an airborne (bus 2) and individuals taking the unexposed bus (bus 1) as transmission route of SARS-CoV-2 is emerging. However, epi- well as the COVID-19 risk between individuals in bus 2 and all demiologic evidence from actual community transmission other individuals attending the worship event, excluding bus in human cohorts is lacking. To investigate the potential air- 2. In addition, we divided seats in bus 2 into high-risk and borne transmission route, we present the investigation of low-risk zones according to the definition of close contact with an outbreak of COVID-19 among lay Buddhists worshiping in COVID-19 in travel-associated settings, an area within 2 a temple in Zhejiang province. meters17 (classification 1) or 2 rows18 (classification 2) of the source patient. On bus 2, the distance between 2 rows was measured at 0.75 m, which converts 2 meters to 3 rows. There- Methods fore, the high-risk zone includes seats in the same row and within 2 or 3 rows (rows 6-10 or rows 5-11) of the index patient Data Collection (seated in row 8); low-risk zones include seats in other rows Data on demographics, travel history, and social and family ac- (Figure17,18). The COVID-19 risks in the 2 types of zones were tivities were collected by a standard questionnaire and addi- compared. All comparisons used χ2 or Fisher exact tests. Both tional phone or in-person interviews through epidemiologic risk ratios (RRs) and risk differences and corresponding investigation carried out by local Centers for Disease Control 95% confidence intervals were calculated. For an exposure- and Prevention staff between January 27 and February 23, disease category with no observations, we added a value of 0.5 2020. The standard case report form and details regarding to all cells.19 A Spearman rank correlation test was performed the initiation of the outbreak investigation are provided in the to test the correlation between the disease severity of those eAppendix in the Supplement. The research protocol was who developed infection and the distance to the index pa- approved by the institutional review board at the Zhejiang tient on bus 2 (eAppendix in the Supplement). Analyses were Provincial Centers for Disease Control and Prevention and conducted using SAS, version 9.4 (SAS Institute), and statis- all human participants gave written informed consent. tical significance was set at P< .05. Sample Collection and Diagnosis of COVID-19 Throat swabs (oropharynx and nasopharynx) were collected Results for all individuals involved in the outbreak and their close con- tacts identified through follow-up contact tracing.