To determine possible modes of virus transmission, we investigated a cluster of coronavirus disease cases associated with a shopping mall in Wenzhou, China. Data indicated that indirect transmission of the causative virus occurred, perhaps resulting from virus contamination of common objects, virus aerosolization in a confined space, or spread from asymptomatic infected persons

Cai, Jing

Gamber, Michelle

He, Guiging

Huang, Jianping

Sun, Wenjie

Wu, Jing

English

DigitalCommons@Florida International University

Florida International University FIU Digital Commons Coronavirus Research at FIU 6-2020 Indirect Virus Transmission in Cluster of COVID-19 Cases, Wenzhou, China, 2020 Jing Cai Wenjie Sun Jianping Huang Michelle Gamber Jing Wu See next page for additional authors Follow this and additional works at: https://digitalcommons.fiu.edu/covid-19_research  Part of the Medicine and Health Sciences Commons This work is brought to you for free and open access by FIU Digital Commons. It has been accepted for inclusion in Coronavirus Research at FIU by an authorized administrator of FIU Digital Commons. For more information, please contact dcc@fiu.edu. Authors Jing Cai, Wenjie Sun, Jianping Huang, Michelle Gamber, Jing Wu, and Guiging He respiratory syndrome. Science. 2003;300:1966–70.  https://doi.org/10.1126/science.1086616  6. Park SH, Kim Y-S, Jung Y, Choi SY, Cho N-H, Jeong HW, et al. Outbreaks of Middle East respiratory syndrome in two hospitals initiated by a single patient in Daejeon, South Korea. Infect Chemother. 2016;48:99–107. https://doi.org/ 10.3947/ic.2016.48.2.99  7. Li Q, Guan X, Wu P, Wang X, Zhou L, Tong Y, et al. Early transmission dynamics in Wuhan, China, of novel coronavirus-infected pneumonia. N Engl J Med. 2020 Jan 29 [Epub ahead of print]. https://doi.org/10.1056/NEJMoa2001316  8. Wu JT, Leung K, Leung GM. Nowcasting and forecasting  the potential domestic and international spread of the  2019-nCoV outbreak originating in Wuhan, China: a modelling study. Lancet. 2020;395:689–97. https://doi.org/ 10.1016/S0140-6736(20)30260-9  9. Kenah E, Lipsitch M, Robins JM. Generation interval  contraction and epidemic data analysis. Math Biosci. 2008;213:71–9. https://doi.org/10.1016/j.mbs.2008.02.007Address for correspondence: Lauren Ancel Meyers, J.T. Patterson Labs Bldg, University of Texas at Austin, 2415 Speedway, Austin, TX 78712, USA; email: laurenmeyers@austin.utexas.eduIndirect Virus Transmission in Cluster of COVID-19  Cases, Wenzhou, China, 2020Jing Cai,1 Wenjie Sun,1 Jianping Huang,1  Michelle Gamber, Jing Wu, Guiqing HeAuthor affiliations: Wenzhou Sixth People’s Hospital,  Wenzhou Central Hospital Medical Group, Wenzhou, China  (J. Cai, J. Huang, G. He); The Second Affiliated Hospital of Fujian Traditional Chinese Medical University, Fuzhou, China (W. Sun); Robert Stempel College of Public Health and Social Work, Florida International University, Miami, Florida, USA (W. Sun);  Shenandoah University, Winchester, Virginia, USA (M. Gamber); Huashan Hospital, Fudan University, Shanghai, China (J. Wu)DOI: https://doi.org/10.3201/eid2606.200412Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the causative agent of coronavirus disease (COVID-19), is presumed to spread primarily via respiratory droplets and close contact. However, these transmission modes do not explain all cases. To determine how the virus may have spread among a cluster of COVID-19 cases associated with a shop-ping mall in Wenzhou (a city with 8 million residents), China, we monitored and traced close contacts and hypothesized possible transmission modes. We ana-lyzed clinical and laboratory data for cases by using real-time reverse transcription PCR (1). The study was approved with written consent from the Ethics Com-mittee of Wenzhou Central Hospital and written in-formed consent from all case-patients.On January 20, 2020, a 23-year-old man (patient E) sought care at a hospital after 11 days of fever and headache. On January 21, COVID-19 was confirmed for patient E and his co-worker, patient G. The Wen-zhou Center for Disease Control and Prevention traced and tested their contacts, and by January 28, COVID-19 was confirmed for 7 persons (patients A–G) from the same office (on floor 7).Patient A, a 30-year-old woman, the only case-pa-tient who indicated that she had been in Wuhan, China, returned from Wuhan on December 18, 2019. On Janu-ary 15–16, 2020, she had a fever, but symptoms resolved without treatment. Despite symptom resolution, on Jan-uary 30 she was confirmed to have SARS-CoV-2 infec-tion. If patient A is the index patient, infected in Wuhan, her incubation period would have been 28 days, which would be extremely long, according to updated infor-mation (W.J. Guan et al., unpub. data, https://www.medrxiv.org/content/10.1101/2020.02.06.20020974v1). Asymptomatic carrier transmission has been reported for SARS-CoV-2 (2); hence, patient A could have been screened as a close contact during her incubation pe-riod and then hospitalized on the basis of a positive test (PCR) result only. However, her clinical symptoms did not appear until after hospitalization. Because persons with asymptomatic COVID-19 can spread the virus, pa-tient A also could have been an asymptomatic carrier with a persistent infection (3).On January 22, the mall was shut down. During January 19–February 9, COVID-19 was diagnosed for 7 mall staff from floors B1–3 and for 10 mall cus-tomers. Close contacts associated with the mall were traced, and COVID-19 was confirmed for 11 persons. Sixteen patients had had direct contact with other pa-tients or had gone shopping in the mall. The average incubation period was 7.3 (range 1–17) days.The mall has 8 floors above ground and sev-eral basement levels; floors B1 to 6 are commercial  Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 26, No. 6, June 2020 1343RESEARCH LETTERSTo determine possible modes of virus transmission, we investigated a cluster of coronavirus disease cases as-sociated with a shopping mall in Wenzhou, China. Data indicated that indirect transmission of the causative vi-rus occurred, perhaps resulting from virus contamination of common objects, virus aerosolization in a confined space, or spread from asymptomatic infected persons.1These authors contributed equally to this article.1344 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 26, No. 6, June 2020RESEARCH LETTERSFigure. Cluster of COVID-19 cases associated with a shopping mall in Wenzhou, China. A) Distribution of COVID-19 case-patients by mall floor, time, and internal relationship. B) Dates of symptom onset, confirmed test results, and hospitalization information. Numbers within yellow bars indicate length of incubation period. Black vertical arrow indicates date when patient A returned from Wuhan, China. B1–7, mall floors; C, customer; COVID-19 coronavirus disease; Ct, cycle threshold; T, date of symptom onset; M, month; RT-PCR, reverse transcription PCR.shopping space, and floor 7 contains shopping and office space. We created an illustration showing the floors where the eventual COVID-19 case-patients worked or shopped, along with dates of symptom onset, potential incubation periods, symptom du-rations, confirmed times of positive diagnosis, and times of discharge (Figure 1, panel A).Except for those who had been on floor 7, all other case-patients denied direct close contact with other case-patients. The possibility of customers being infected from other sources cannot be excluded. However, most customers reported early symptom onset in a concen-trated time frame (Figure 1, panel B). We found no con-vincing evidence of definitive transmission pathways in this building. Patients A–G (Figure 1, panel A) worked in the same room on floor 7. Other case-patients who had been on other floors denied any direct contact with confirmed patients from floor 7, but they shared com-mon building facilities (e.g., restrooms, elevators). Also, staff from floor 7 visited shops on other floors daily.Until now, no evidence has shown that SARS-CoV-2 can survive outside the body for long. How-ever, Middle East respiratory syndrome coronavirus demonstrates high robustness and a strong capability to survive outside the body and can remain infectious for up to 60 minutes after aerosolization (4). Hence, the rapid spread of SARS-CoV-2 in our study could have resulted from spread via fomites (e.g., elevator buttons or restroom taps) or virus aerosolization in a confined public space (e.g., restrooms or elevators). All case-patients other than those on floor 7 were female, including a restroom cleaner, so common restroom use could have been the infection source. For case-patients who were customers in the shop-ping mall but did not report using the restroom, the source of infection could have been the elevators. The Guangzhou Center for Disease Control and Preven-tion detected the nucleic acid of SARS-CoV-2 on a doorknob at a patient’s house (5), but Wenzhou Cen-ter for Disease Control and Prevention test results for an environmental sample from the surface of a mall elevator wall and button were negative. We cannot exclude the possibility of unknown in-fected persons (e.g., asymptomatic carriers) spreading the virus. However, according to screening protocols implemented by the Wenzhou Center for Disease Control and Prevention, we traced all close contacts and included all patients with positive PCR results, including the asymptomatic carrier (patient A), in this study. Our findings appear to indicate that low intensity transmission occurred without prolonged close contact in this mall; that is, the virus spread by indirect transmission.The work was supported by Major Project of Wenzhou Municipal Science and Technology Bureau (ZY202004).About the AuthorDr. Cai is deputy chief physician and deputy director of the comprehensive internal medicine department. Her major research interest focuses on infectious diseases and gastrointestinal diseases.References  1. National Microbiology Data Center. Novel Coronavirus National Science and Technology Resource Service System [cited 2020 Jan 30]. http://nmdc.cn/nCoV  2. Bai Y, Yao L, Wei T, Tian F, Jin DY, Chen L, et al. Presumed asymptomatic carrier transmission of COVID-19. JAMA. 2020 Feb 21 [Epub ahead of print]. https://doi.org/10.1001/jama.2020.2565  3. Rothe C, Schunk M, Sothmann P, Bretzel G, Froeschl G, Wallrauch C, et al. Transmission of 2019-nCoV Infection from an asymptomatic contact in Germany. N Engl J Med. 2020;382:970–1. https://doi.org/10.1056/NEJMc2001468  4. Pyankov OV, Bodnev SA, Pyankova OG, Agranovski IE.  Survival of aerosolized coronavirus in the ambient air.  Journal of Aerosol Science. 2018;115:158–63.5. Meiping G. Coronavirus detected on doorknob in S.  China’s Guangzhou. 2020 [cited 2020 Feb 3].  https://news.cgtn.com/news/2020-02-03/Coronavirus-detected-on-doorknob-in-S-China-s-Guangzhou- NMua1LcOWY/index.htmlAddress for correspondence: Guiqing He, Department of Infectious Diseases, Infectious Diseases Laboratory, Wenzhou Sixth People’s Hospital, Wenzhou Central Hospital Medical Group, Wenzhou, 325000 China; email: hegq123@126.com; Jing Wu, Department of Infectious Diseases, #5-504, Huashan Hospital, Fudan Universit, 12 Wulumuqizhong Rd, Jing’an District Shanghai 200040, China; email: jingee@fudan.edu.cn Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 26, No. 6, June 2020 1345RESEARCH LETTERS

Indirect Virus Transmission in Cluster of COVID-19 Cases, Wenzhou, China, 2020

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Indirect Virus Transmission in Cluster of COVID-19 Cases, Wenzhou, China, 2020

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