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Aerodynamic Characteristics and RNA Concentration of SARS-CoV-2 Aerosol in
Wuhan Hospitals during COVID-19 Outbreak
Yuan Liu, Ph.D.,1, †, Zhi Ning, Ph.D.,2, †, *, Yu Chen, Ph.D.,1, †, *, Ming Guo, Ph.D.,1, †, Yingle
Liu, Ph.D.,1, Nirmal Kumar Gali, Ph.D.,2, Li Sun, M.Sc.,2, Yusen Duan, M.Sc.,3, Jing Cai,
Ph.D.,4, Dane Westerdahl2, D.Env.,2, Xinjin Liu, M.Sc.,1, Kin-fai Ho, Ph.D.,5, *, Haidong Kan,
Ph.D.,4, *, Qingyan Fu, Ph.D.,3, *, Ke Lan, MD, PhD, 1, *
† These authors contributed equally to this work.
Affiliations:
1 State Key Laboratory of Virology, Modern Virology Research Center, College of Life
Sciences, Wuhan University, Wuhan, 430072, P. R. China;
2 Division of Environment and Sustainability, The Hong Kong University of Science and
Technology, Hong Kong SAR, P. R. China;
3 Shanghai Environmental Monitoring Center, Shanghai 200235, P. R. China;
4 School of Public Health, Key Lab of Public Health Safety of the Ministry of Education and
Key Lab of Health Technology Assessment of the Ministry of Health, Fudan University,
Shanghai 200032, P. R. China;
5 JC School of Public Health and Primary Care, The Chinese University of Hong Kong, Hong
Kong SAR, P. R. China
*Corresponding authors:
Ke Lan, State Key Laboratory of Virology, Modern Virology Research Center, College
of Life Sciences, Wuhan University, Wuhan, 430072, P. R. China. E-mail: klan@whu.edu.cn
Zhi Ning, Division of Environment and Sustainability, The Hong Kong University of
Science and Technology, Hong Kong SAR, P. R. China. E-mail:zhining@ust.hk
Yu Chen, State Key Laboratory of Virology, Modern Virology Research Center,
College of Life Sciences, Wuhan University, Wuhan, 430072, P. R. China. E-mail:
chenyu@whu.edu.cn
Qingyan Fu, Shanghai Environmental Monitoring Center, Shanghai 200235, P.
R.China. E-mail: qingyanf@sheemc.cn
Haidong Kan, P.O. Box 249, 130 Dong-An Road, Shanghai 200032, P. R. China.
Tel/fax: +86 (21) 5423 7908. E-mail: kanh@fudan.edu.cn
Kin-fai Ho, JC School of Public Health and Primary Care, The Chinese University of
Hong Kong, Hong Kong SAR, P. R. China. Email: kfho@cuhk.edu.hk
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Abstract
Background: The ongoing outbreak of COVID-19 has spread rapidly and sparked global
concern. While the transmission of SARS-CoV-2 through human respiratory droplets and
contact with infected persons is clear, the aerosol transmission of SARS-CoV-2 has been
little studied.
Methods: Thirty-five aerosol samples of three different types (total suspended particle, size
segregated and deposition aerosol) were collected in Patient Areas (PAA) and Medical Staff
Areas (MSA) of Renmin Hospital of Wuhan University (Renmin) and Wuchang Fangcang
Field Hospital (Fangcang), and Public Areas (PUA) in Wuhan, China during COVID-19
outbreak. A robust droplet digital polymerase chain reaction (ddPCR) method was employed
to quantitate the viral SARS-CoV-2 RNA genome and determine aerosol RNA concentration.
Results: The ICU, CCU and general patient rooms inside Renmin, patient hall inside
Fangcang had undetectable or low airborne SARS-CoV-2 concentration but deposition
samples inside ICU and air sample in Fangcang patient toilet tested positive. The airborne
SARS-CoV-2 in Fangcang MSA had bimodal distribution with higher concentration than
those in Renmin during the outbreak but turned negative after patients number reduced and
rigorous sanitization implemented. PUA had undetectable airborne SARS-CoV-2
concentration but obviously increased with accumulating crowd flow.
Conclusions: Room ventilation, open space, proper use and disinfection of toilet can
effectively limit aerosol transmission of SARS-CoV-2. Gathering of crowds with
asymptomatic carriers is a potential source of airborne SARS-CoV-2. The virus aerosol
deposition on protective apparel or floor surface and their subsequent resuspension is a
potential transmission pathway and effective sanitization is critical in minimizing aerosol
transmission of SARS-CoV-2.
Background
Circulating in China and 94 other countries and territories, the COVID-19 epidemic
has resulted in 103,168 confirmed cases including 22,355 outside mainland China, with
3,507 deaths reported (March 7, 2020). Due to its increasing threat to global health, WHO
has declared that the COVID-19 epidemic was a 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).1-3
The transmission of SARS-CoV-2 in humans is thought to be via at least 3 sources: 1)
inhalation of liquid droplets produced by and/or 2) close contact with infected persons and 3)
contact with surfaces contaminated with SARS-CoV-2.4 Moreover, aerosol transmission of
pathogens has been shown in confined spaces.5,6 There are many respiratory diseases
spread by the airborne route such as tuberculosis, measles and chickenpox.7,8 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 disease.9 At present, there is little information on the characteristics of airborne SARS-
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CoV-2 containing aerosols, their concentration patterns and behaviour during airborne
transmission due to the difficulties in sampling virus-laden aerosols and challenges in their
quantification at low concentration. Such a lack of understanding limits effective risk
assessment, prevention and control of COVID-19 disease outbreaks. This study on airborne
SARS-CoV-2 was conducted in different areas inside two hospitals and public areas in
Wuhan, China, the epicenter city during the initial disease outbreak. We aimed to 1) quantify
the concentrations of airborne SARS-CoV-2 both inside the hospitals and in outdoor public
areas, 2) evaluate the aerodynamic size distributions of SARS-CoV-2 aerosols that may
mediate its airborne transmission, and 3) determine the dry deposition rate of the airborne
SARS-CoV-2 in a patient ward room.
Methods
1. Study design
This study is an experimental investigation on the concentration and aerodynamic
characteristics of airborne SARS-CoV-2 aerosol in different areas of two hospitals: the
Renmin Hospital of Wuhan University, designated for treatment of severe symptom COVID-
19 patient during the disease outbreak and the Wuchang Fangcang Field Hospital, one of
the first temporary hospitals which was renovated from an indoor sports stadium to
quarantine and treat mildly symptom patients, and outdoor public areas in Wuhan during the
coronavirus outbreak. We further classified the sampling locations 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), which were venues open for the general public. The
description and characteristics of sampling sites are shown in Table S1.
Three types of aerosol samples were collected: 1) Aerosol samples of total
suspended particles (TSP) with no upper size limit to quantify RNA concentration of SARS-
CoV-2 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.
2. Sample collection
The sampling was conducted between February 17 and March 2, 2020 in the
locations by two batches as shown in Table 1. All aerosol samples were collected on
presterilized gelatin filters (Sartorius, Germany). Total of 30 TSP aerosol samples were
collected on 25 mm diameter filters loaded into styrene filter cassettes (SKC Inc, US) and
sampled air at a fixed flow rate of 5.0 litre per minute (LPM) using a portable pump (APEX2,
Casella, US). Total of 3 size segregated aerosol samples were collected using a miniature
cascade impactor (Sioutas impactor, SKC Inc., US) that separate aerosol into five ranges (>
2.5 m, 1.0 to 2.5 m, 0.50 to 1.0 m and 0.25 to 0.50 m on 25 mm filter substrates, and 0
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to 0.25 m on 37 mm filters) at a flow rate of 9.0 LPM. Total of 2 aerosol deposition samples
were collected using 80 mm diameter filters packed into a holder with an effective deposition
area of 43.0 cm2 and the filters were placed on the floor in two corners of Renmin Hospital
ICU room intact for 7 days. Sampling durations and operation periods are detailed in Table
S1. Prior to the field sampling, the integrity and robustness of experiment protocol was
examined in the laboratory and described in Supplementary Appendix (Table S2).
3. Analytical method and data analysis
After aerosol sample collection, all samples were handled immediately in the BSL-2
laboratory of Wuhan University. The 25, 37mm and 80 mm filter samples were dissolved in
deionized water, then TRIzol LS Reagent (Invitrogen) was added to inactivate SARS-CoV-2
viruses and extract RNA according to the manufacturer’s instruction. First strand cDNA was
synthesized using PrimeScript RT kit (TakaRa). Optimized ddPCR was used to detect the
presence of SARS-CoV-2 viruses following our previous study.10 Analysis of the ddPCR data
was performed with QuantaSoft software (Bio-Rad). The concentration reported by the
procedure equals copies of template per microliter of the final 1x ddPCR reaction, which was
normalized to copies m-3 in all the results, and hence the virus or viral RNA concentration in
aerosol is expressed in copies m-3 hereafter. A detailed protocol is provided in
Supplementary Appendix.
Results
1. Airborne SARS-CoV-2 concentrations
The airborne SARS-CoV-2 concentrations in different categorized sites are shown in
Table 1. The ICU, CCU and ward room in PAA of Renmin Hospital had negative test results.
Fangcang Hospital workstations in different zones had low concentrations (1-9 copies m-3) of
SARS-CoV-2 aerosol. The highest concentration in PAA of two hospitals was observed
inside the patient mobile toilet room (19 copies m-3). 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 18 to 42 copies m-3 in the first batch of sampling.
During the second batch of sampling, the two TSP samples in the PARRs had negative test
results with reduced number of medical staff and more rigorous sanitization processes in
Fangcang. In PUA, SARS-CoV-2 aerosol concentrations were below 3 copies m-3, except for
two occasions: one crowd gathering site near the entrance of a department store with
frequent customer flow and one outdoor site next to Renmin Hospital with outpatients and
passengers passing by.
2. Size distribution of SARS-CoV-2 aerosol
Figure 1 shows the SARS-CoV-2 aerosol concentrations in different aerodynamic
size bins collected from PARRs in Zone B and C, and Medical Staff’s Office in Fangcang
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Hospital. The peak concentration of SARS-CoV-2 aerosols appears in two distinct size
ranges, one in the submicron region with aerodynamic diameter dominant between 0.25 to
1.0 µm, and the other peak in supermicron region with diameter larger than 2.5 µm. The
submicron region was dominantly noted in PARRs in Zone B and C of Fangcang Hospital
(Figure 1a and 1b) with peak concentration of 40 and 9 copies m-3 in 0.25 to 0.5 µm and 0.5
to 1.0 µm, respectively. Whereas the supermicron region was observed in Fangcang
Hospital Zone C PARR and Medical Staff’s Office (Figure 1b and 1c) with 7 and 9 copies m-3.
The two concentration peaks in sub- and supermicron ranges have independent existence in
SARS-CoV-2 aerosols and they do not necessarily co-exist indicating possible different
formation mechanisms.
Figure 1 Concentration of airborne SARS-CoV-2 RNA in different aerosol size bins
3. Deposition rate of SARS-CoV-2 aerosol
The aerosol deposition sample collected from the Renmin Hospital ICU room had raw counts
of SARS-CoV-2 RNA significantly above the detection limit as shown in Table S1, although
the TSP aerosol sample concentration inside this ICU room was below detection limit during
the 3 hour sampling period. The much longer integration time of 7 days for the deposition
sample has contributed to the accumulation of virus sediment. The area normalized
deposition rate inside the ICU room is calculated to be 31 and 113 copies m-2 hour-1. The
sample with the higher deposition rate was placed in the hindrance-free corner of the room,
approximately 3 meters from the patient’s bed. The other sample recorded lower virus
copies and it was placed in another corner with medical equipment above, and
approximately 2 meters from the patient’s bed. This may have blocked the path of virus
aerosol sediment.
Discussion
Generally undetectable or very low concentrations of airborne SARS-CoV-2 were
found in most PAA inside the two hospitals in Wuhan. The negative pressure ventilation and
high air exchange rate inside ICU, CCU and ward room of Renmin Hospital are effective in
minimizing airborne SARS-CoV-2. Fangcang Hospital hosted over 200 mild symptom
patients in each zone during the peak of the COVID-19 outbreak. However, the SARS-CoV-
2 aerosol concentrations inside the patient hall were very low during the two batches of
sampling periods, showing the protective and preventive measures taken in Fangcang
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Hospital are effective in hindering the aerosol transmission and reducing the potential
infection risks of the medical staff. 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. The deposited virus may come from respiratory droplet or virus-laden aerosol
transmission. Our findings add support to a hypothesis that virus-laden aerosol deposition
may play a role in surface contamination and subsequent contact by susceptible people
resulting in human infection.
This study also recorded an elevated airborne SARS-CoV-2 concentration inside the
patient mobile toilet of Fangcang Hospital. This may come from either the patient's breath or
the aerosolization of the virus-laden aerosol from patient’s faeces or urine during use. Ong et
al. has found the wipe samples from room surfaces of toilets used by SARS-CoV-2 patients
tested positive.11 Our finding has confirmed the aerosol transmission as an important
pathway for surface contamination. We call for extra care and attention on the proper design,
use and disinfection of the toilets in hospitals and in communities to minimize the potential
source of the virus-laden aerosol.
MSAs in general have higher concentration of SARS-CoV-2 aerosol with biomodal
size distributions compared to PAA in both hospitals during the first batch of sampling in the
peak of COVID-19 outbreak. 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 has limited air penetration from the patient hall where the SARS-
CoV-2 aerosol concentration was generally low. We believe one direct source of the high
SARS-CoV-2 aerosol concentration may be the resuspension of virus-laden aerosol from the
surface of medical staff protective apparel while they are being removed. These
resuspended virus-laden aerosol originally may come from the direct deposition of
respiratory droplets or virus-laden aerosol onto the protective apparel while medical staff
having long working hours inside PAA, as shown from the SARS-CoV-2 deposition results in
ICU room. Another possible source is the resuspension of floor dust aerosol containing virus
that were transferred from PAA to MSA. The two virus-laden aerosol sources also appear to
correspond to the sub- and supermicron peaks found in size-segregated samples. We
hypothesize the submicron aerosol may come from the resuspension of virus-laden aerosol
from staff apparel due to its higher mobility while the supermicron virus-laden aerosol may
come from the resuspension of dust particles from the floors or other hard surfaces. The
findings suggest virus-laden aerosols could first deposit on the surface of medical staff
protective apparel and the floors in patient areas and are then resuspended by the
movements of medical staff. The second batch of TSP samples taken in Fangcang MSAs all
tested negative with reduced number of patients from > 200 to 100 per zone and
implementation of more rigorous and thorough sanitization measures in Fangcang. The
comparison of the two batches of samples showed the effectiveness and importance of
sanitization in reducing the airborne SARS-CoV-2 in high risk areas.
In PUA outside the hospitals, we found the majority of the sites have undetectable or
very low concentrations of SARS-CoV-2 aerosol, except for one crowd gathering site about 1
meter to the entrance of a department store with customers frequently passing through, and
the other site next to Renmin Hospital where the outpatients and passengers passed by. It is
possible that asymptomatic carriers of COVID-19 in the crowd may have contributed as the
source of virus-laden aerosol during the sampling period.12,13 The results showed overall low
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risks in the public venues but do reinforce the importance of avoiding crowded gatherings
and implementing early identification and diagnosis of asymptomatic carriers for early
quarantine or treatment. Personal protection equipment such as wearing masks in public
places or while in transit may reduce aerosol exposure and transmission.
The results from this study provide the first field report on the characteristics of
airborne SARS-CoV-2 in Wuhan with important implications for the public health prevention
and medical staff protection. We call for particular attentions on 1) the proper use and
cleaning of toilets (e.g. ventilation and sterilization), as a potential spread source of
coronavirus with relatively high risk caused by aerosolization of virus and contamination of
surfaces after use; 2) for the general public, the proper use of personal protection measures,
such as wearing masks and avoiding busy crowds; 3) the effective sanitization of the high
risk area and the use of high level protection masks for medical staff with direct contact with
the COVID-19 patients or with long stay in high risk area; 4) the renovation of large stadiums
as field hospitals with nature ventilation and protective measures is an effective approach to
quarantine and treat mild symptom patients so as to reduce the COVID-19 transmission
among the public; 5) the virus may be resuspended from the contaminated protective
apparel surface to the air while taking off and from the floor surface with the movement of
medical staff. Thus, surface sanitization of the apparel before they are taken off may also
help reduce the infection risk for medical staff.
Acknowledgement
This study was supported by Special Fund for COVID-19 Research of Wuhan University. We
are grateful to Taikang Insurance Group Co., Ltd, Beijing Taikang Yicai Foundation, Renmin
Hospital and Wuchang Fangcang Hospital for their great support to this work. We would like
to thank Prof. Hongmei Xu from Xi’an Jiaotong University, Qingdao Laoying Environmental
Technology Co., Ltd, Beijing Top Science Co.,Ltd, Shanghai Leon Scientific Instrument
Co.,Ltd, Shanghai Eureka Environmental Protection Hi-tech. Ltd, Sapiens Environmental
Technology Co., Ltd for their support in providing the sampling devices and technical support
in this study. The authors also thank Cuiping Wang, Qingli Zhang, Guoping Liang, Zhao
Song for their assistance in filter sample preparation and logistics support.
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1
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Table 1. 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#
TSP
a
1
TSP
b
9
2. Zone B Workstation
TSP
1
3. Zone C Workstation#
TSP
a
5
TSP
b
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) #
TSP
a
16
TSP
b
0
11. Zone B Protective Apparel Removal
Room (PARR) Size Segregated 42
12. Zone C Protective Apparel Removal
Room (PARR) #
Size Segregated
a
20
TSP
b
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 #
TSP
21
TSP
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 Blank
a
0
Field Blank
b
0
Note:
* 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 Table S1.
a The samples taken during the first batch of sampling from Feb 17 to Feb 24, 2020.
b The samples taken during the second batch of sampling on Mar 2, 2020.
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