Aerosol Transmission of SARS-CoV-2

Aerosol and Surface Stability of SARS-CoV-2 as Compared with SARS-CoV-1
March 17, 2020
DOI: 10.1056/NEJMc2004973



A novel human coronavirus that is now named severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) (formerly called HCoV-19) emerged in Wuhan, China, in late 2019 and is now causing a pandemic.1 We analyzed the aerosol and surface stability of SARS-CoV-2 and compared it with SARS-CoV-1, the most closely related human coronavirus.2

We evaluated the stability of SARS-CoV-2 and SARS-CoV-1 in aerosols and on various surfaces and estimated their decay rates using a Bayesian regression model (see the Methods section in the Supplementary Appendix, available with the full text of this letter at NEJM.org). SARS-CoV-2 nCoV-WA1-2020 (MN985325.1) and SARS-CoV-1 Tor2 (AY274119.3) were the strains used. Aerosols (<5 μm) containing SARS-CoV-2 (105.25 50% tissue-culture infectious dose [TCID50] per milliliter) or SARS-CoV-1 (106.75-7.00 TCID50 per milliliter) were generated with the use of a three-jet Collison nebulizer and fed into a Goldberg drum to create an aerosolized environment. The inoculum resulted in cycle-threshold values between 20 and 22, similar to those observed in samples obtained from the upper and lower respiratory tract in humans.

Our data consisted of 10 experimental conditions involving two viruses (SARS-CoV-2 and SARS-CoV-1) in five environmental conditions (aerosols, plastic, stainless steel, copper, and cardboard). All experimental measurements are reported as means across three replicates.


Figure 1.

Viability of SARS-CoV-1 and SARS-CoV-2 in Aerosols and on Various Surfaces.
SARS-CoV-2 remained viable in aerosols throughout the duration of our experiment (3 hours), with a reduction in infectious titer from 103.5 to 102.7 TCID50 per liter of air. This reduction was similar to that observed with SARS-CoV-1, from 104.3 to 103.5 TCID50 per milliliter (Figure 1A).

SARS-CoV-2 was more stable on plastic and stainless steel than on copper and cardboard, and viable virus was detected up to 72 hours after application to these surfaces (Figure 1A), although the virus titer was greatly reduced (from 103.7 to 100.6 TCID50 per milliliter of medium after 72 hours on plastic and from 103.7 to 100.6 TCID50 per milliliter after 48 hours on stainless steel). The stability kinetics of SARS-CoV-1 were similar (from 103.4 to 100.7 TCID50 per milliliter after 72 hours on plastic and from 103.6 to 100.6 TCID50 per milliliter after 48 hours on stainless steel). On copper, no viable SARS-CoV-2 was measured after 4 hours and no viable SARS-CoV-1 was measured after 8 hours. On cardboard, no viable SARS-CoV-2 was measured after 24 hours and no viable SARS-CoV-1 was measured after 8 hours (Figure 1A).

Both viruses had an exponential decay in virus titer across all experimental conditions, as indicated by a linear decrease in the log10TCID50 per liter of air or milliliter of medium over time (Figure 1B). The half-lives of SARS-CoV-2 and SARS-CoV-1 were similar in aerosols, with median estimates of approximately 1.1 to 1.2 hours and 95% credible intervals of 0.64 to 2.64 for SARS-CoV-2 and 0.78 to 2.43 for SARS-CoV-1 (Figure 1C, and Table S1 in the Supplementary Appendix). The half-lives of the two viruses were also similar on copper. On cardboard, the half-life of SARS-CoV-2 was longer than that of SARS-CoV-1. The longest viability of both viruses was on stainless steel and plastic; the estimated median half-life of SARS-CoV-2 was approximately 5.6 hours on stainless steel and 6.8 hours on plastic (Figure 1C). Estimated differences in the half-lives of the two viruses were small except for those on cardboard (Figure 1C). Individual replicate data were noticeably “noisier” (i.e., there was more variation in the experiment, resulting in a larger standard error) for cardboard than for other surfaces (Fig. S1 through S5), so we advise caution in interpreting this result.

We found that the stability of SARS-CoV-2 was similar to that of SARS-CoV-1 under the experimental circumstances tested. This indicates that differences in the epidemiologic characteristics of these viruses probably arise from other factors, including high viral loads in the upper respiratory tract and the potential for persons infected with SARS-CoV-2 to shed and transmit the virus while asymptomatic.3,4 Our results indicate that aerosol and fomite transmission of SARS-CoV-2 is plausible, since the virus can remain viable and infectious in aerosols for hours and on surfaces up to days (depending on the inoculum shed). These findings echo those with SARS-CoV-1, in which these forms of transmission were associated with nosocomial spread and super-spreading events,5 and they provide information for pandemic mitigation efforts.

Circulating in 206 countries and areas, the COVID-19 outbreak has
resulted in 857,641 confirmed cases including with 42,006 deaths
globally as of April 2, 2020. Due to its increasing threat to global health,
WHO has declared the COVID-19 outbreak as a pandemic and global
public health emergency. The causative pathogen of the COVID-19 outbreak
has been identified as a highly infectious novel coronavirus which
is referred to as the Severe Acute Respiratory Syndrome Coronavirus
2 (SARS-CoV-2)4–6. Reported transmission pathways of SARS-CoV-2 in
humans are: 1) inhalation of virus laden liquid droplets 2) close contact
with infected persons and 3) contact with surfaces contaminated with
SARS-CoV-21. Moreover, aerosol transmission has been suggested as an
additional yet important pathway from clinic observations in confined
spaces2,3. There are many respiratory diseases spread by the airborne
route such as tuberculosis, measles and chickenpox7,8. A retrospective
cohort study conducted after the SARS epidemic in Hong Kong in 2003
suggested that airborne spread may have played an important role
in the transmission of that disease9. At present, little is known on the
aerodynamic characteristics and transmission pathways of SARS-CoV-2
in aerosols, partly due to the difficulties in sampling virus containing
aerosol in real-world and challenges in their quantification at low
concentration.

In this study, we sampled airborne SARS-CoV-2 and its aerosol deposition
at 30 sites in two designated hospitals and public areas in Wuhan
and then quantified the SARS-CoV-2 copy counts of aerosol samples
using a robust droplet digital PCR-based detection method (ddPCR)10.
The two hospitals are exclusively used for COVID-19 patient treatment
during the outbreak but each with unique characteristics serving different
purposes. The Renmin Hospital of Wuhan University (Renmin
Hospital hereafter) represents Grade-A tertiary hospitals designated
for treatment of severe symptom COVID-19 patients, while the Wuchang
Fangcang Field Hospital (Fangcang Hospital hereafter) is representative
of the make-shift field hospitals which was renovated from indoor
sports facilities or exhibition centres to quarantine and treat patients
with mild symptoms. The sampling locations were classified into three
categories according to their accessibility by different groups: 1) Patient
Areas (PAA), where the COVID-19 patients have physical presence. These
include the Intensive Care Units (ICU), Coronary Care Units (CCU) and
ward rooms inside Renmin Hospital, a toilet and staff workstations
inside Fangcang Hospital; 2) Medical Staff Areas (MSA), the workplaces
in the two hospitals exclusively accessed by the medical staff who had
direct contact with the patients, and 3) Public Areas (PUA), venues
open for the general public (Supplementary Table 1).Three types of
aerosol samples were collected: 1) Aerosol samples of total suspended
particles (TSP) with no upper size limit to quantify RNA concentrations
of SARS-CoV-2 in aerosol; 2) Aerodynamic size-segregated aerosol
samples to determine the size distribution of airborne SARS-CoV-2;
3) Aerosol deposition samples to determine the deposition rate of
airborne SARS-CoV-2.

The existence of SARS-CoV-2 in aerosol samples was determined
through the quantification of its genetic material (RNA). The airborne
SARS-CoV-2 concentrations in different categorized sites are shown
in Table 1. Generally very low or non-detectable concentrations of airborne
SARS-CoV-2 were found in most PAA of Renmin Hospital, suggesting
the negatively pressurized isolation and high air exchange
rate inside ICU, CCU and ward room of Renmin Hospital are very
effective in limiting the airborne transmission of SARS-CoV-2. The
highest concentration in PAA was observed inside the Fangcang Hospital
patient mobile toilet room (19 copies m-3), which is a temporary
single toilet room of approximate 1 m2 in area without ventilation.
Airborne SARS-CoV-2 may come from either the patient's breath or
the aerosolization of the virus-laden aerosol from patient’s faeces or
urine during use11,12. Although the infectivity of the virus is not known
in this study, the results also relate to the findings by Ong et al. that
showed positive test results of wipe samples from room surfaces of
toilets used by SARS-CoV-2 patients13. In MSAs, the two sampling sites in
Renmin Hospital had low concentration of 6 copies m-3, while the sites
in Fangcang Hospital in general had higher concentrations. Particularly,
the Protective Apparel Removal Rooms (PARRs) in three different
zones inside Fangcang Hospital are among the upper range of airborne
SARS-CoV-2 concentration from 16 to 42 copies m-3 in the first batch
of sampling. In PUA outside the hospitals, we found the majority of
the sites have undetectable or very low concentrations of SARS-CoV-2
aerosol (below 3 copies m-3), except for one crowd gathering site
about 1 m to the entrance of a department store with customers frequently
passing through, and the other site next to Renmin Hospital
where the public including outpatients passed by. While both sites
were outside the building, it is possible that infected carriers of
SARS-CoV-2 in the crowd may have contributed as the source of
virus-laden aerosol during the sampling period. The results suggest
overall low risks in the well ventilated or open public venues but
do reinforce the importance of avoiding crowded gatherings and
implementing early identification and diagnosis of infected carriers
for quarantine or treatment.


Table 1 | RNA concentration of airborne SARS-CoV-2 at different locations in Wuhan
Category Sites Sample Type Concentration (copies m-3)
Patient Areas (PAA)
Fangcang Hospital 1. Zone A Workstation# TSPa 1
TSPb 9
2. Zone B Workstation TSP 1
3. Zone C Workstation# TSPa 5
TSPb 0
4. Patient Mobile Toilet Room TSP 19
Renmin Hospital 5. Intensive Care Unit (ICU) TSP 0
6. Intensive Care Unit (ICU) Deposition 31*
7. Intensive Care Unit (ICU) Deposition 113*
8. Coronary Care Unit (CCU) TSP 0
9. Ward Zone 16 TSP 0
Medical Staff Areas (MSA)
Fangcang Hospital 10. Zone A Protective Apparel Removal Room (PARR) # TSPa 16
TSPb 0
11. Zone B Protective Apparel Removal Room (PARR) Size Segregated 42
12. Zone C Protective Apparel Removal Room (PARR) # Size Segregateda 20
TSPb 0
13. Male Staff Change Room TSP 20
14. Female Staff Change Room TSP 11
15. Medical Staff’s Office Size Segregated 20
16. Meeting Room TSP 18
17. Warehouse # TSPa 21
TSPb 0
Renmin Hospital 18. Passageway for Medical Staff TSP 6
19. Dining Room for Medical Staff TSP 6
Public Areas (PUA)
20. Fangcang Hospital Pharmacy TSP 3
21. Renmin Hospital Doctor Office TSP 0
22. Renmin Hospital Outpatient Hall TSP 0
23. Renmin Hospital Outdoor TSP 7
24. University Office Doorside TSP 0
25. University Hospital Outpatient Hall TSP 0
26. Community Check Point TSP 0
27. Residential Building TSP 0
28. Supermarket TSP 0
29. Department Store 1 TSP 11
30. Department Store 2 TSP 3
31. Blank Control # Field Blanka 0

* The reported values are virus aerosol deposition rate in copies m-2 hour-1.
# Two batches of sampling were conducted for the sites. Detailed information is shown in Supplementary Table 1.
a The samples taken during the first batch of sampling from Feb 17 to Feb 24, 2020.


Inside the Renmin Hospital ICU rooms, the two aerosol deposition
samples tested positive with an estimated deposition rate of 31 and 113
copies m-2 hr-1, although the TSP aerosol sample concentration inside
this ICU room was below detection limit (Table 1). The sample with
the higher deposition rate was placed in the hindrance-free corner of
the room, approximately 3 m from the patient’s bed. The other sample
recorded lower virus copies and it was placed in another corner,
approximately 2 m from the patient’s bed and below medical equipment
which may have blocked the path of virus aerosol sediments. Our findings,
though based on a small sample size, indicate virus-laden aerosol
deposition may play a role in surface contamination and subsequent
contact by susceptible people resulting in human infection.
MSAs in general had higher concentrations of SARS-CoV-2 aerosol
compared to PAAs in both hospitals in the first batch of sampling during
the peak of COVID-19 outbreak (Table 1). For Renmin Hospital sampling
sites, the air circulation in MSA by design is isolated from that of the
patient rooms. While for Fangcang Hospital, the non-ventilated temporary
PARR was isolated from the patient hall where the SARS-CoV-2 aerosol
concentration was generally low. The second batch of TSP sampling
in Fangcang Hospital MSAs was conducted after number of patients
reduced from over 200 to less than 100 per zone and implementation
of more rigorous and thorough sanitization measures including
more frequent spraying of chlorinated disinfectant on the floor of
patient areas, additional disinfection by 3% hydrogen peroxide in the
PARR at least once a week, spraying alcohol disinfectant all over the
protective apparel before taking off, and prolonged operation time
of indoor air purifiers. The samples from this second batch showed all
non-detectable results (Table 1), confirming the importance of sanitization
in reducing the airborne SARS-CoV-2 in high risk areas.