Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1

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1
Aerosol and Surface Stability of SARS-CoV-2
as Compared with SARS-CoV-1
To the Editor: 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 stabilit y 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. Aero-
sols (<5 μm) containing SARS-CoV-2 (10
5.25
50%
tissue-culture infectious dose [TCID
50
] per milli-
liter) or SARS-CoV-1 (10
6. 75 -7. 0 0
TCID
50
per milliliter)
were generated with the use of a three-jet Colli-
son nebulizer and fed into a Goldberg drum to
create an aerosolized environment. The inocu-
lum 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 condi-
tions involving two viruses (SARS-CoV-2 and
SARS-CoV-1) in five environmental conditions
(aerosols, plastic, stainless steel, copper, and card-
board). All experimental measurements are re-
ported as means across three replicates.
SARS-CoV-2 remained viable in aerosols
throughout the duration of our experiment
(3 hours), with a reduction in infectious titer from
10
3.5
to 10
2.7
TCID
50
per liter of air. This reduction
was similar to that observed with SARS-CoV-1,
from 10
4.3
to 10
3.5
TCID
50
per milliliter (Fig. 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 ap-
plication to these surfaces (Fig. 1A), although
the virus titer was greatly reduced (from 10
3.7
to
10
0.6
TCID
50
per milliliter of medium after 72 hours
on plastic and from 10
3.7
to 10
0.6
TCID
50
per milli-
liter after 48 hours on stainless steel). The sta-
bility kinetics of SARS-CoV-1 were similar (from
10
3.4
to 10
0.7
TCID
50
per milliliter after 72 hours
on plastic and from 10
3.6
to 10
0.6
TCID
50
per milli-
liter 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 (Fig. 1A).
Both viruses had an exponential decay in vi-
rus titer across all experimental conditions, as
indicated by a linear decrease in the log
10
TCID
50
per liter of air or milliliter of medium over time
(Fig. 1B). The half-lives of SARS-CoV-2 and
SARS-CoV-1 were similar in aerosols, with me-
dian 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
(Fig. 1C, and Table S1 in the Supplementary Ap-
pendix). The half-lives of the t wo 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 me-
dian half-life of SARS-CoV-2 was approximately
5.6 hours on stainless steel and 6.8 hours on
plastic (Fig. 1C). Estimated differences in the half-
lives of the t wo viruses were small except for
those on cardboard (Fig. 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 ex-
perimental circumstances tested. This indicates
that differences in the epidemiologic character-
istics of these viruses probably arise from other
factors, including high viral loads in the upper
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of
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2
Titer
(TCID50/liter of air)
104
102
103
101
100
0 0.5 1.0 2.0 3.0
Hours
Titer
(TCID50/ml of medium)
104
102
103
101
100
0 1 84 4824 9672 0 1 84 4824 9672 0 1 84 4824 9672 0 1 84 4824 9672
104
102
103
101
100
104
102
103
101
100
104
102
103
101
100
Hours
Aerosols Copper Cardboard Stainless Steel Plastic
BPredicted Decay of Virus Titer
ATiters of Viable Virus
Titer
(TCID50/liter of air)
104
102
103
101
100
0 1.0 2.0 3.0
Hours
Titer
(TCID50/ml of medium)
104
102
103
101
100
0 20 40 60 80 0 20 40 60 80 0 20 40 60 80 0 20 40 60 80
104
102
103
101
100
104
102
103
101
100
104
102
103
101
100
Titer
(TCID50/liter of air)
104
102
103
101
100
0 1.0 2.0 3.0
Titer
(TCID50/ml of medium)
104
102
103
101
100
0 20 40 60 80 0 20 40 60 80 0 20 40 60 80 0 20 40 60 80
104
102
103
101
100
104
102
103
101
100
104
102
103
101
100
Hours
Aerosols Copper Cardboard Stainless Steel Plastic
CHalf-Life of Viable Virus
Half-Life (hr)
10
4
6
8
2
0
Half-Life (hr)
10
4
6
8
2
0
10
4
6
8
2
0
10
4
6
8
2
0
10
4
6
8
2
0
Aerosols Copper Cardboard Stainless Steel Plastic
SARS-CoV-2 SARS-CoV-1
SARS-CoV-2
SARS-CoV-1
SARS-CoV-2
SARS-CoV-1
SARS-CoV-2 SARS-CoV-1 SARS-CoV-2 SARS-CoV-1 SARS-CoV-2 SARS-CoV-1SARS-CoV-2 SARS-CoV-1
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Cor re spondence
n engl j med nejm.org
3
respiratory tract and the potential for persons
infected with SARS-CoV-2 to shed and transmit
the virus while asymptomatic.
3,4
Our results in-
dicate that aerosol and fomite transmission of
SARS-CoV-2 is plausible, since the virus can re-
main viable and infectious in aerosols for hours
and on surfaces up to days (depending on the
inoculum shed). These f indings echo those with
SARS-CoV-1, in which these forms of transmission
were associated with nosocomial spread and su-
per-spreading events,
5
and they provide informa-
tion for pandemic mitigation efforts.
Neeltje van Doremalen, Ph.D.
Trenton Bushmaker, B.Sc.
National Institute of Allergy and Infectious Diseases
Hamilton, MT
Dylan H. Morris, M.Phil.
Princeton University
Princeton, NJ
Myndi G. Holbrook, B.Sc.
National Institute of Allergy and Infectious Diseases
Hamilton, MT
Amandine Gamble, Ph.D.
University of California, Los Angeles
Los Angeles, CA
Brandi N. Williamson, M.P.H.
National Institute of Allergy and Infectious Diseases
Hamilton, MT
Azaibi Tamin, Ph.D.
Jennifer L. Harcourt, Ph.D.
Natalie J. Thornburg, Ph.D.
Susan I. Gerber, M.D.
Centers for Disease Control and Prevention
Atlanta, GA
James O. Lloyd-Smith, Ph.D.
University of California, Los Angeles
Los Angeles, CA
Bethesda, MD
Emmie de Wit, Ph.D.
Vincent J. Munster, Ph.D.
National Institute of Allergy and Infectious Diseases
Hamilton, MT
vincent.munster@nih.gov
Dr. van Dorem alen, Mr. Bushmaker, and Mr. Morris contrib-
uted equally t o this letter.
The fi ndings and conclusions in t his let ter are those of the
authors and do not necessarily represent the of ficial posit ion of
the Centers for Disease Cont rol and Prevent ion (CDC). Names
of specif ic vendors, manufacturers, or products are i ncluded for
public healt h and informational purposes; inclusion does not
imply endorsement of the vendors, manufact urers, or products
by the CDC or t he Depa rtment of Healt h and Human Ser vice s.
Supported by the Intramural Research Program of t he Na-
tiona l Inst itute of Allergy and Infectious Diseases, Nation al In-
stitutes of Hea lth, a nd by contracts f rom the Defense Advanced
Research Proje cts Agency (DARPA PREEMPT No. D18AC00031,
to Drs. Lloyd-Smith a nd Gamble), from t he National Science
Foundat ion (DEB-1557022, to Dr. Lloyd-Smit h), and from the
Strategic Environmental Research and De velopment Program of
the Depart ment of Defense (SERDP, RC-2635, to Dr. Lloyd-Smith).
Disclosure forms provided by the authors are avail able wit h
the fu ll text of th is letter at NEJM.org.
This letter was published on March 17, 2020, at NEJM.org.
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Correspondence Copyright © 2020 Massachusetts Medical Society.
Figure 1 (facing page). Viability of SARS-CoV-1 and
SARS-CoV-2 in Aerosols and on Various Surfaces.
As shown in Panel A, the titer of aerosolized viable
virus is expressed in 50% tissue-culture infectious
dose (TCID
50
) per liter of air. Viruses were applied to
copper, cardboard, stainless steel, and plastic main-
tained at 21 to 23°C and 40% relative humidity over
7 days. The titer of viable virus is expressed as TCID
50
per milliliter of collection medium. All samples were
quantified by end-point titration on Vero E6 cells.
Plots show the means and standard errors (I bars)
across three replicates. As shown in Panel B, regres-
sion plots indicate the predicted decay of virus titer
over time; the titer is plotted on a logarithmic scale.
Points show measured titers and are slightly jittered
(i.e., they show small rapid variations in the ampli-
tude or timing of a waveform arising from f luctua-
tions) along the time axis to avoid overplotting. Lines
are random draws from the joint posterior distribu-
tion of the exponential decay rate (negative of the
slope) and intercept (initial virus titer) to show the
range of possible decay patterns for each experimen-
tal condition. There were 150 lines per panel, includ-
ing 50 lines from each plotted replicate. As shown in
Panel C, violin plots indicate posterior distribution for
the half-life of viable virus based on the estimated ex-
ponential decay rates of the virus titer. The dots indi-
cate the posterior median estimates, and the black
lines indicate a 95% credible inter val. Experimental
conditions are ordered according to the posterior me-
dian half-life of SARS-CoV-2. The dashed lines indicate
the limit of detection, which was 3.33×10
0.5
TCID
50
per liter of air for aerosols, 10
0.5
TCID
50
per milliliter
of medium for plastic, steel, and cardboard, and 10
1.5
TCID
50
per milliliter of medium for copper.
The New England Journal of Medicine
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Copyright © 2020 Massachusetts Medical Society. All rights reserved.