Commentary—New Recommendations for Use of Cloth Face Masks
Until recently, the US CDC advised that the general public need not wear masks in public (1, 2). People were told just to maintain an appropriate 6-foot (2-meter) distance from one another.
However, with mounting evidence that asymptomatic and pre-symptomatic people can spread SARS-CoV-2 and that the recommended distance of 3 or 6 feet may underestimate the distance and timescale over which a cloud of respiratory excretions can travel (23 to 27 feet) (3), the CDC now advises the general public to wear a home-made cloth mask (because surgical and N95 masks are in short supply) if a safe distance cannot be maintained, especially in areas of significant community-based transmission (4). Although the role of respiratory excretions in transmission has not yet been definitively defined, one occurrence early in the US epidemic illustrates the importance in SARS-CoV-2 transmission of people who are infected but not symptomatic and the cloud of respiratory particles that is generated by routine respiratory actions such a talking, breathing, or even singing.
On March 10, 2020, 60 choir members rehearsed together for 2½ hours in a church in Skagit County, Washington State. Although COVID-19 was already present in the Seattle area, about an hour’s drive away, at the time prohibitions on large gatherings had not yet been announced and no local cases had been reported (5). Even though no one was coughing or sneezing or appeared ill, and everyone came with their own sheet music and avoided direct physical contact, within the next 3 weeks, 28 of the choristers were diagnosed with COVID-19 and another 17 were ill with characteristic symptoms but were not tested; 3 were hospitalized and 2 died.
This incident resembles several known outbreaks of tuberculosis (TB), in which singing by an infected person apparently infected many other choristers. For example, in one TB outbreak at a boarding school, the rate of TB was higher in those who were in a choir with the index case than in those who shared a dormitory room or meals with the index case but were not in the choir (6). TB is a classic example of an infection transmitted by minute airborne infectious particles 5 microns or less in size, called aerosols, generated during coughing, shouting, or singing by those who have pulmonary or laryngeal TB (7).
What are aerosols?
Aerosols are part of a large population of particles of respiratory excretions that range in size from less than 1 to 20 microns in diameter that may enclose viable infectious organisms. They are expelled into the air when someone talks, sings, coughs, or sneezes. Singing has been shown to produce the same quantity of aerosol-sized particles as does coughing (8). The larger particles settle out by gravity quickly within several feet onto nearby environmental surfaces, on which, as demonstrated by Wells (9), they begin to lose water by evaporation. The larger particles also may settle onto the mucosal surfaces of the eyes, mouth, or nose of a nearby person. Smaller particles settle more slowly, evaporate, and become “droplet nuclei,” which are so small (5 microns or less) and lightweight they may remain suspended in the air for several hours. In the absence of air currents, the droplet nuclei will disperse slowly. If wafted by air currents, these particles can become widely dispersed beyond the 6-foot range currently advised as a safe avoidance radius by the CDC. If inhaled, particles the size of droplet nuclei deposit in the lower respiratory tract (10).
The extent of environmental contamination by SARS-CoV-2 can be significant. RNA from the virus has been found around a COVID-19-infected patient’s bedside and toilet, presumably deposited by large respiratory droplets and fecal shedding (11). SARS-CoV-2 RNA also was found in the air exhaust outlet of the ventilation system in this patient’s hospital room, likely having traveled as droplet nuclei in air currents long distances from the patient’s bedside (11), although viral cultures were not done to demonstrate that the virus was alive at these sites and capable of causing infection.
The ability of organisms within large or small droplets to cause infection depends on the survival characteristics of individual pathogens on environmental surfaces or in aerosols, and the susceptibility to infection (related to host cell surface receptors) of the different tissues exposed to these organisms. A recent study demonstrated that SARS-CoV-2 can survive for as long as 24 hours on cardboard, 48 hours on stainless steel, 72 hours on plastic, and also at least 3 hours as an aerosol under the laboratory conditions of the experiment (12).
The specific cellular receptor that binds the spike surface protein of SARS-CoV-2 and mediates viral entry into its target host cell is angiotensin-converting enzyme-2 (ACE2). This receptor is expressed on the surface of nasal epithelium, lung alveolar epithelial cells and enterocytes of the small intestine (13, 14), consistent with finding higher SARS-CoV-2 viral load in nasal than in throat specimens (15).
SARS-CoV, the human coronavirus that caused a global epidemic in 2002–2003 with 8,096 confirmed cases in more than 25 countries, is genetically related to SARS-CoV-2, but the virological dynamics differ. SARS-CoV viral titers increased with time after onset of symptoms, peaking approximately 10 days after symptom onset, suggesting transmissibility increased with time after onset of symptoms (16). In contrast, SARS-CoV-2 viral titers are detected soon after symptom onset. In some patients, SARS-CoV-2 can be detected before symptom onset and viral titers in an asymptomatic patient are similar to those in symptomatic patients, which suggests that asymptomatic and pre-symptomatic patients can transmit SARS-CoV-2 (17).
These virological findings are in accord with reports of transmission of SARS-CoV-2 by asymptomatic and pre-symptomatic patients and early in the course of symptomatic infection. There are multiple epidemiologic studies from China that report transmission of SARS-CoV-2 from asymptomatic carriers or transmission during the pre-symptomatic incubation period (18–23). In Germany, a cluster of 16 cases occurred at a car parts supplier in late January 2020, when a pre- or mildly symptomatic Chinese employee from Shanghai attended several business meetings near Munich, Germany, without clearly realizing she was sick (24). She felt unusual chest and back aches and was tired for her whole stay, which she attributed to jet lag. The woman’s parents from Wuhan had recently visited her in Shanghai and they later tested positive for COVID-19. She first realized she was sick once back in China.
In the US, a similar incident occurred when 3 employees of a Massachusetts biotechnology company, who were not as yet symptomatic during a company meeting in Boston, later tested positive for the virus. Subsequently, 15 employees who attended the meeting were diagnosed with COVID-19, several of whom then carried the infection back to their home states. Massachusetts says that more than half of its 179 confirmed cases of COVID-19 at the time had been linked to the biotech firm's Boston meeting (25).
In a study from Singapore of clusters in which pre-symptomatic transmission likely occurred, exposure occurred 1 to 3 days before symptom onset in the four clusters for which the date of exposure could be determined (26). Similarly, pre-symptomatic transmission was found to be occurring on average 2.55 and 2.89 days before onset of symptoms in a study of outbreaks in Singapore and Tianjin, China; in this study, the estimated serial intervals (that is, the time between successive cases in a chain of transmission) were shorter than incubation periods in both Singapore and Tianjin, suggesting that pre-symptomatic transmission was occurring (27).
Asymptomatic SARS-CoV-2 positivity is relatively common. During the outbreak of COVID-19 on board the Diamond Princess cruise ship that was quarantined in Yokohama, of a total of 3,063 passengers and crew members tested, an estimated 18% of the 634 people who tested positive for SARS-CoV-2 were asymptomatic and an estimated 33% of Japanese citizens evacuated from Wuhan tested positive were asymptomatic (28). The Chinese National Health Commission is now reporting that of 885 recent infections, 601 (68%) were asymptomatic (29). And the US CDC is now reporting that as many as 25 % of people infected with SARS-CoV-2 do not show symptoms (30).
COVID-19 spreads early in the course of symptomatic infection by respiratory droplets to others who are in close contact or by contact with contaminated objects and surfaces. It sometimes also spreads from asymptomatic carriers and for several days prior to onset of symptoms. Because asymptomatic individuals can transmit the virus, asking only sick people to stay home or wear masks is unlikely to be sufficient. Everyone must be urged to stay home and wear masks in public to prevent those who are unaware they have the virus from spreading it; and perhaps, considering the distance a cloud of respiratory excretions can travel (23 to 27 feet) (3), masks should be worn in public all the time, not just when a 6-foot distance cannot be maintained. Aerosol transmission of SARS-CoV-2 is well-recognized by the WHO and CDC when COVID-19 patients undergo aerosol-generating procedures such as intubation, but aerosol transmission is also likely in other circumstances, especially in outbreaks with large numbers of secondary cases, as illustrated by the choir outbreak in Skagit, Washington State. Significant environmental contamination by large respiratory droplets from patients with SARS-CoV-2 requires strict adherence to environmental and hand hygiene.
1. World Health Organization (WHO): Coronavirus disease (COVID-19) advice to the public: When and how to use masks. https://www.who.int/emergencies/diseases/novel-coronavirus-2019/advice-for-public/when-and-how-to-use-masks. Accessed April 16, 2020.
2. World Health Organization (WHO): Modes of transmission of virus causing COVID-19: Implications for IPC precaution recommendations [published online March 29, 2020]. Accessed April 16, 2020. https://www.who.int/news-room/commentaries/detail/modes-of-transmission-of-virus-causing-covid-19-implications-for-ipc-precaution-recommendations
3. Bourouiba L: Turbulent gas clouds and respiratory pathogen emissions: Potential implications for reducing transmission of COVID-19 [published online March 26, 2020]. JAMA doi:10.1001/jama.2020.4756. Available at: https://jamanetwork.com/journals/jama/fullarticle/2763852
4. Centers for Disease Control and Prevention (CDC): Use of cloth face coverings to help slow the spread of COVID-19. Accessed April 16, 2020. Available at: https://www.cdc.gov/coronavirus/2019-ncov/prevent-getting-sick/diy-cloth-face-coverings.html
5. Read, R: A choir decided to go ahead with rehearsal. Now dozens of members have COVID-19 and two are dead. Los Angeles Times March 29, 2020. Accessed April 16, 2020. Available at: https://www.latimes.com/world-nation/story/2020-03-29/coronavirus-choir-outbreak
7. Riley RL: Airborne infection. Am J Med 57: 466–475, 1974.
10. Knight V: Viral and Mycoplasma Infections of the Respiratory Tract. Philadelphia, PA, Lea & Febiger. 1973, pp 1-9.
11. 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 [published online March 04, 2020]. JAMA doi:10.1001/jama.2020.3227.
12. van Doremalen N, Bushmaker T, Morris DH, et al: Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1. New Engl J Med 383:1564-1567, 2020. Published online March 17, 2020. https://www.nejm.org/doi/full/10.1056/NEJMc2004973
13. Hamming I, Timens W, Bulthuis ML, et al: Tissue distribution of ACE2 protein, the functional receptor of SARS coronavirus. A first step in understanding SARS pathogenesis. J Pathol 203:631-637, 2004.
14. Sungnak W, Huang N, Becavin C, et al: SARS-CoV-2 entry genes are most highly expressed in nasal goblet and ciliated cells within human airways. arXiv Submitted March 13, 2020. Accessed April 16, 2020. Available at: https://arxiv.org/pdf/2003.06122.pdf
15. Wu C, Zheng M: Single-cell RNA expression profiling shows that ACE2, the putative receptor of COVID-19, has significant expression in nasal and mouth tissue, and is co-expressed with TMPRSS2 and not co-expressed with SLC6A19 in the tissues. 12 March 2020, PREPRINT (Version 1) available at Research Square https://www.researchsquare.com/article/rs-16992/v1
16. Peiris JSM, Chu CM, Cheng VCC, et al: Clinical progression and viral load in a community outbreak of coronavirus-associated SARS pneumonia: a prospective study. Lancet 361:1767-1772, 2003. https://www.ncbi.nlm.nih.gov/pubmed/12781535
17. Zou L, Ruan F, Huang M, et al: SARS-CoV-2 viral load in upper respiratory specimens of infected patients. N Engl J Med 382:1177-1179, 2020. DOI: 10.1056/NEJMc2001737
18. Hu Z, Song C, Xu C, et al: Clinical characteristics of 24 asymptomatic infections with COVID-19 screened among close contacts in Nanjing, China. Sci China Life Sci Mar 4, 2020. doi: 10.1007/s11427-020-1661-4. [Epub ahead of print]
19. Wei WE, Li Z, Chiew CJ, et al: Presymptomatic transmission of SARS-CoV-2 — Singapore, January 23–March 16, 2020. MMWR Morbidity and mortality weekly report. 2020;ePub: 1 April 2020. https://www.cdc.gov/mmwr/volumes/69/wr/mm6914e1.htm
20. Tong ZD, Tang A, Li KF, et al: Potential presymptomatic transmission of SARS-CoV-2, Zhejiang Province, China, 2020. Emerg Infect Dis 2020; May 26(5). DOI: 10.3201/eid2605.200198 epub ahead of print March 9, 2020.
21. Qian G, Yang N, Ma AHY, et al: A COVID-19 transmission within a family cluster by presymptomatic infectors in China. Clin Infect Dis 2020. 2020 Mar 23. pii: ciaa316. doi: 10.1093/cid/ciaa316. [Epub ahead of print]
22. Pan X, Chen D, Xia Y, et al: Asymptomatic cases in a family cluster with SARS-CoV-2 infection. Lancet Infect Dis 20(4):410-411, 2020. doi: 10.1016/S1473-3099(20)30114-6. Epub 2020 Feb 19.
23. Bai Y, Yao L, Wei T, et al: Presumed asymptomatic carrier transmission of COVID-19. JAMA 323(14):1406-1407, 2020. doi:10.1001/jama.2020.2565
24. Poltz J, Carrel P: Pass the salt: The minute details that helped Germany build virus defences. Reuters April 9, 2020. Accessed April 16, 2020. Available at: https://www.reuters.com/article/us-health-coronavirus-germany-defences-i/pass-the-salt-the-minute-details-that-helped-germany-build-virus-defences-idUSKCN21R1DB
25. Keown A: Approximately 100 COVID-19 cases stem from Biogen meeting. Biospace March 17,2020. Accessed April 16, 2020. Available at: https://www.biospace.com/article/approximately-100-covid-19-cases-stem-from-biogen-meeting/
26. Wei WE, Li Z, Chiew CJ, et al: Presymptomatic transmission of SARS-CoV-2 — Singapore, January 23–March 16, 2020. MMWR Morbidity and mortality weekly report. 2020; ePub: 1 April 2020. https://www.cdc.gov/mmwr/volumes/69/wr/mm6914e1.htm
27. Tindale L, Coombe M, Stockdale JE, et al: Transmission interval estimates suggest pre-symptomatic spread of COVID-19. March 6, 2020. PREPRINT medRxiv. Available at: .https://www.medrxiv.org/content/10.1101/2020.03.03.20029983v1
28. Mizumoto K, Kagaya K, Zarebski A, Chowell G: Estimating the asymptomatic proportion of coronavirus disease 2019 (COVID-19) cases on board the Diamond Princess cruise ship, Yokohama, Japan, 2020. Euro Surveill Mar 12; 25(10): 2000180 doi: 10.2807/1560-7917.ES.2020.25.10.2000180 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7078829/
29. Lo K: Coronavirus: 68 percent of cases confirmed in China in past eight days had no symptoms. South China Morning Post April 8, 2020. Accessed April 16, 2020. Available at: https://www.scmp.com/news/china/society/article/3079012/coronavirus-68-cent-cases-confirmed-china-past-eight-days-had-no30. Mandavilli A: Infected but feeling fine. The unwitting coronavirus spreaders. New York Times Published March 31, 2020; Updated April 1, 2020. Accessed April 16, 2020. Available at: https://www.nytimes.com/2020/03/31/health/coronavirus-asymptomatic-transmission.html