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Volume 26, Number 9—September 2020
Detection of Severe Acute Respiratory Syndrome Coronavirus 2 RNA on Surfaces in Quarantine Rooms
We investigated severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) environmental contamination in 2 rooms of a quarantine hotel after 2 presymptomatic persons who stayed there were laboratory-confirmed as having coronavirus disease. We detected SARS-CoV-2 RNA on 8 (36%) of 22 surfaces, as well as on the pillow cover, sheet, and duvet cover.
Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has rapidly spread globally and. as of May 2, 2020, had caused >3 million confirmed coronavirus disease cases (1). Although SARS-CoV-2 transmission through respiratory droplets and direct contact is clear, the potential for transmission through contact with surfaces or objects contaminated with SARS-CoV-2 is poorly understood (2). The virus can be detected on various surfaces in the contaminated environment from symptomatic and paucisymptomatic patients (3,4). Moreover, we recently reported detection of SARS-CoV-2 RNA on environmental surfaces of a symptomatic patient’s household (5). Because SARS-CoV-2 remains viable and infectious from hours to days on surfaces (6,7), contact with a contaminated surface potentially could be a medium for virus transmission. In addition, high viral load in throat swab specimens at symptom onset (8,9) and peak infectiousness at 0–2 days for presymptomatic patients (8) suggest that presymptomatic patients may easily contaminate the environment. However, data are limited on environmental contamination of SARS-CoV-2 by patients who may be presymptomatic. Therefore, to test this hypothesis, we examined the presence of SARS-CoV-2 RNA in collected environmental surface swab specimens from 2 rooms of a centralized quarantine hotel where 2 presymptomatic patients had stayed.
Two Chinese students studying overseas returned to China on March 19 (patient A) and March 20 (patient B), 2020 (Table 1). On the day of their arrival in China, neither had fever or clinical symptoms, and they were transferred to a hotel for a 14-day quarantine. They had normal body temperatures (patient A, 36.3°C; patient B, 36.5°C) and no symptoms when they checked into the hotel. During the quarantine period, local medical staff were to monitor their body temperature and symptoms each morning and afternoon. On the morning of the second day of quarantine, they had no fever (patient A, 36.2°C for patient A; patient B, 36.7°C) or symptoms. At the same time their temperatures were taken, throat swab samples were collected; both tested positive for SARS-CoV-2 RNA by real-time reverse transcription PCR (rRT-PCR). The students were transferred to a local hospital for treatment. At admission, they remained presymptomatic, but nasopharyngeal swab, sputum, and fecal samples were positive for SARS-CoV-2 RNA with high viral loads (Table 1). In patient A, fever (37.5°C) and cough developed on day 2 of hospitalization, but his chest computed tomography images showed no significant abnormality during hospitalization. In patient B, fever (37.9°C) and cough developed on day 6 of hospitalization, and her computed tomography images showed ground-glass opacities.
Approximately 3 hours after the 2 patients were identified as positive for SARS-CoV-2 RNA, we sampled the environmental surfaces of the 2 rooms in the centralized quarantine hotel in which they had stayed. Because of the SARS-CoV-2 outbreak in China, the hotel had been closed during January 24–March 18, 2020. Therefore, only these 2 persons had stayed in the rooms. We used a sterile polyester-tipped applicator, premoistened in viral transport medium, to sample the surfaces of the door handle, light switch, faucet handle, thermometer, television remote, pillow cover, duvet cover, sheet, towel, bathroom door handle, and toilet seat and flushing button. We also collected control swab samples from 1 unoccupied room. We collected each sample by swabbing each individual surface. We tested the samples with an rRT-PCR test kit (DAAN GENE Ltd, http://www.daangene.com) targeting the open reading frame 1ab (ORF1ab) and N genes of SARS-CoV-2. We interpreted cycle threshold (Ct) <40 as positive for SARS-CoV-2 RNA and Ct >40 as negative.
We collected a total of 22 samples from the 2 rooms of the quarantine hotel (Table 2). Eight (36%) samples were positive for SARS-CoV-2 RNA. Ct values ranged from 28.75 to 37.59 (median 35.64). Six (55%) of 11 samples collected from the room of patient A were positive for SARS-CoV-2 RNA. Surface samples collected from the sheet, duvet cover, pillow cover, and towel tested positive for SARS-CoV-2 RNA, and surface samples collected from the pillow cover and sheet had a high viral load; Ct for ORF1ab gene from the pillow cover was 28.97 and from the sheet, 30.58. Moreover, the Ct values of these 2 samples correlated with those of patient A’s nasopharyngeal (24.73) and fecal (33.12) swab samples at hospital admission. One surface sample from the faucet in patient B’s room was positive for SARS-CoV-2 RNA; the Ct was 28.75 for the ORF1ab gene. Again, we detected SARS-CoV-2 RNA from the surface samples of the pillow cover; Ct was 34.57. All control swab samples were negative for SARS-CoV-2 RNA.
Our study demonstrates extensive environmental contamination of SARS-CoV-2 RNA in a relatively short time (<24 hours) in occupied rooms of 2 persons who were presymptomatic. We also detected SARS-CoV-2 RNA in the surface swab samples of the pillow cover, duvet cover, and sheet.
Evidence for SARS-CoV-2 transmission by indirect contact was identified in a cluster of infections at a shopping mall in China (10). However, no clear evidence of infection caused by contact with the contaminated environment was found. SARS-CoV-2 RNA has been detected on environmental surfaces in isolation rooms where the symptomatic or paucisymptomatic patients stayed for several days (3–5). In our study, we demonstrate high viral load shedding in presymptomatic patients, which is consistent with previous studies (8,9), providing further evidence for the presymptomatic transmission of the virus (5,11–15). In addition, presymptomatic patients with high viral load shedding can easily contaminate the environment in a short period.
Our results also indicate a higher viral load detected after prolonged contact with sheets and pillow covers than with intermittent contact with the door handle and light switch. The detection of SARS-CoV-2 RNA in the surface samples of the sheet, duvet cover, and pillow cover highlights the importance of proper handling procedures when changing or laundering used linens of SARS-CoV-2 patients. Thus, to minimize the possibility of dispersing virus through the air, we recommend that used linens not be shaken upon removal and that laundered items be thoroughly cleaned and dried to prevent additional spread.
The absence of viral isolation in our investigation was an obstacle to demonstrating the infectivity of the virus, but SARS-CoV-2 has been reported to remain viable on surfaces of plastic and stainless steel for up to 4–7 days (6,7) and 1 day for treated cloth (7). In summary, our study demonstrates that presymptomatic patients have high viral load shedding and can easily contaminate environments. Our data also reaffirm the potential role of surface contamination in the transmission of SARS-CoV-2 and the importance of strict surface hygiene practices, including regarding linens of SARS-CoV-2 patients.
Dr. Jiang is an epidemiologist in Qingdao Center for Disease Control and Prevention, Qingdao, Shandong Province, China. His primary research interests included infectious disease control and prevention and emerging infectious diseases.
This work was supported by the National Major Project for Control and Prevention of Infectious Disease of China (2017ZX10303401-006), the National Natural Science Foundation of China (81773494 and 81621005), and the Special National Project on investigation of basic resources of China (2019FY101502).
- World Health Organization. Coronavirus disease (COVID-19). Situation report—102 [cited 2020 May 1]. https://www.who.int/docs/default-source/coronaviruse/situation-reports/20200501-covid-19-sitrep.pdf
- Centers for Disease Control and Prevention. Coronavirus disease 2019 (COVID-19). How COVID-19 spreads [cited 2020 May 2]. https://www.cdc.gov/coronavirus/2019-ncov/prevent-getting-sick/how-covid-spreads.html
- Ong SWX, Tan YK, Chia PY, Lee TH, Ng OT, Wong MSY, 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;323:1610.
- Yung CF, Kam KQ, Wong MSY, Maiwald M, Tan YK, Tan BH, et al. Environment and personal protective equipment tests for SARS-CoV-2 in the isolation room of an infant with infection. Ann Intern Med. 2020;
M20-0942; Epub ahead of print.
- Jiang XL, Zhang XL, Zhao XN, Li CB, Lei J, Kou ZQ, et al. Transmission potential of asymptomatic and paucisymptomatic SARS-CoV-2 infections: a three-family cluster study in China. J Infect Dis. 2020;
jiaa206; Epub ahead of print.
- van Doremalen N, Bushmaker T, Morris DH, Holbrook MG, Gamble A, Williamson BN, et al. Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1. N Engl J Med. 2020;382:1564–7.
- Chin AWH, Chu JTS, Perera MRA, Hui KPY, Yen H-L, Chan MCW, et al. Stability of SARS-CoV-2 in different environmental conditions. Lancet Microbe. 2020;1:
- He X, Lau EHY, Wu P, Deng X, Wang J, Hao X, et al. Temporal dynamics in viral shedding and transmissibility of COVID-19. Nat Med. 2020;26:672–5; Epub ahead of print.
- Wölfel R, Corman VM, Guggemos W, Seilmaier M, Zange S, Müller MA, et al. Virological assessment of hospitalized patients with COVID-2019. Nature. 2020; Epub ahead of print.
- Cai J, Sun W, Huang J, Gamber M, Wu J, He G. Indirect virus transmission in cluster of COVID-19 cases, Wenzhou, China, 2020. Emerg Infect Dis. 2020;26: Epub ahead of print.
- 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.
- Yu P, Zhu J, Zhang Z, Han Y. 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;221:1757–61.
- Tong ZD, Tang A, Li KF, Li P, Wang HL, Yi JP, et al. Potential presymptomatic transmission of SARS-CoV-2, Zhejiang province, China, 2020. Emerg Infect Dis. 2020;26:1052–4.
- Wei WE, Li Z, Chiew CJ, Yong SE, Toh MP, Lee VJ. Presymptomatic Transmission of SARS-CoV-2 - Singapore, January 23-March 16, 2020. MMWR Morb Mortal Wkly Rep. 2020;69:411–5.
- Kimball A, Hatfield KM, Arons M, James A, Taylor J, Spicer K, et al.; Public Health – Seattle & King County; CDC COVID-19 Investigation Team. Public Health–Seattle & King County; CDC COVID-19 Investigation Team. Asymptomatic and presymptomatic SARS-CoV-2 infections in residents of a long-term care skilled nursing facility—King County, Washington, March 2020. MMWR Morb Mortal Wkly Rep. 2020;69:377–81.
Suggested citation for this article: Jiang FC, Jiang XL, Wang ZG, Meng ZH, Shao SF, Anderson BD, et al. Detection of severe acute respiratory syndrome coronavirus 2 RNA on surfaces in quarantine rooms. Emerg Infect Dis. 2020 Sep [date cited]. https://doi.org/10.3201/eid2609.201435
Original Publication Date: May 18, 2020
1These authors contributed equally to this article.