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Systematic Review

SARS-CoV-2 and the role of airborne transmission: a systematic review

[version 1; peer review: 1 approved with reservations, 2 not approved]
Carl J. Heneghan
https://orcid.org/0000-0002-1009-1992
1, Elizabeth A. Spencer
https://orcid.org/0000-0002-9079-8006
1, Jon Brassey
https://orcid.org/0000-0002-7812-6311
2, [...] Annette Plüddemann1, Igho J. Onakpoya1, David H. Evans
https://orcid.org/0000-0001-5871-299X
3, John M. Conly4, Tom Jefferson1
Carl J. Heneghan
https://orcid.org/0000-0002-1009-1992
1, Elizabeth A. Spencer
https://orcid.org/0000-0002-9079-8006
1, [...] Jon Brassey
https://orcid.org/0000-0002-7812-6311
2, Annette Plüddemann1, Igho J. Onakpoya1, David H. Evans
https://orcid.org/0000-0001-5871-299X
3, John M. Conly4, Tom Jefferson1
PUBLISHED 24 Mar 2021
Author details Author details
OPEN PEER REVIEW
REVIEWER STATUS

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Abstract

Background: Airborne transmission is the spread of an infectious agent caused by the dissemination of droplet nuclei (aerosols) that remain infectious when suspended in the air. We carried out a systematic review to identify, appraise and summarise the evidence from studies of the role of airborne transmission of SARS-CoV-2.
Methods: We searched LitCovid, MedRxiv, Google Scholar and the WHO Covid-19 database from 1 February to 20 December 2020 and included studies on airborne transmission. Data were dual extracted and we assessed quality using a modified QUADAS 2 risk of bias tool.
Results: We included 67 primary studies and 22 reviews on airborne SARS-CoV-2. Of the 67 primary studies, 53 (79%) reported data on RT-PCR air samples, 12 report cycle threshold values and 18 copies per sample volume. All primary studies were observational and of low quality. The research often lacked standard methods, standard sampling sizes and reporting items. We found 36 descriptions of different air samplers deployed. Of the 42 studies conducted in-hospital that reported binary RT-PCR tests, 24 (57%) reported positive results for SARs-CoV-2 (142 positives out of 1,403 samples: average 10.1%, range 0% to 100%). There was no pattern between the type of hospital setting (ICU versus non-ICU) and RT-PCR positivity. Seventeen studies reported potential air transmission in the outdoors or in the community. Seven performed RT-PCR sampling, of which two studies report weak positive RNA samples for 2 or more genes (5 of 125 samples positive: average 4.0%). Ten studies attempted viral culture with no serial passage for viral culture.
Conclusion:  SARS-CoV-2 RNA is detected intermittently in the air in various settings. Standardized guidelines for conducting and reporting research on airborne transmission are needed. The lack of recoverable viral culture samples of SARS-CoV-2 prevents firm conclusions over airborne transmission.

Keywords

SARs-CoV-2, transmission, COVID, Airborne

Corresponding author: Carl J. Heneghan
Competing interests: CH holds grant funding from the NIHR School of Primary Care Research, the NIHR BRC Oxford and the World Health Organization for a series of Living rapid review on the modes of transmission of SARs-CoV-2 reference WHO registration No2020/1077093. He has received expenses and fees for his media work. He receives expenses for teaching EBM and is also paid for his GP work in NHS out of hours (contract Oxford Health NHS Foundation Trust) and for appraising treatment recommendations in non-NHS settings. He is the Director of CEBM and is an NIHR Senior Investigator. TJ was in receipt of a Cochrane Methods Innovations Fund grant to develop guidance on the use of regulatory data in Cochrane reviews (2015-018). In 2014–2016, he was a member of three advisory boards for Boehringer Ingelheim. TJ was a member of an independent data monitoring committee for a Sanofi Pasteur clinical trial on an influenza vaccine. TJ is occasionally interviewed by market research companies about phase I or II pharmaceutical products for which he receives fees (current). TJ was a member of three advisory boards for Boehringer Ingelheim (2014-16). TJ was a member of an independent data monitoring committee for a Sanofi Pasteur clinical trial on an influenza vaccine (2015-2017). TJ is a relator in a False Claims Act lawsuit on behalf of the United States that involves sales of Tamiflu for pandemic stockpiling. If resolved in the United States’ favour, he would be entitled to a percentage of the recovery. TJ is co-holder of a Laura and John Arnold Foundation grant for the development of a RIAT support centre (2017-2020) and Jean Monnet Network Grant, 2017-2020 for The Jean Monnet Health Law and Policy Network. TJ is an unpaid collaborator to the project Beyond Transparency in Pharmaceutical Research and Regulation led by Dalhousie University and funded by the Canadian Institutes of Health Research (2018-2022). TJ consulted for Illumina LLC on next-generation gene sequencing (2019-2020). TJ was the consultant scientific coordinator for the HTA Medical Technology programme of the Agenzia per i Serivizi Sanitari Nazionali (AGENAS) of the Italian MoH (2007-2019). TJ is Director of Medical Affairs for BC Solutions, a market access company for medical devices in Europe. TJ is funded by NIHR UK and the World Health Organization (WHO) to update Cochrane review A122, “Physical Interventions to interrupt the spread of respiratory viruses”. TJ is funded by Oxford University to carry out a living review on the transmission epidemiology of COVID-19. Since 2020, TJ receives fees for articles published by The Spectator and other media outlets. TJ is part of a review group carrying out “Living rapid literature review on the modes of transmission of SARS-CoV-2 (WHO Registration 2020/1077093-0)”. He is a member of the WHO COVID-19 Infection Prevention and Control Research Working Group. DE has been awarded U.S. patents as a co‐inventor of related oncolytic virus technologies and is a co‐owner of Prophysis Inc., which retains a partial interest in the licensing rights for these technologies. JMC holds grants from the Canadian Institutes for Health Research on acute and primary care preparedness for COVID-19 in Alberta, Canada and was the primary local Investigator for a Staphylococcus aureus vaccine study funded by Pfizer for which all funding was provided only to the University of Calgary. He also received support from the Centers for Disease Control and Prevention (CDC) to attend an Infection Control Think Tank Meeting. AP holds grant funding from the NIHR School of Primary Care Research. IJO, EAS, and JB have no interests to disclose.
Grant information: The review was funded by the World Health Organization: Living rapid review on the modes of transmission of SARs-CoV-2 reference WHO registration No 2020/1077093. CH, AP and ES also receive funding support from the National Institute of Health Research School of Primary Care Research Evidence Synthesis Working Group project 390 (https://www.spcr.nihr.ac.uk/eswg).
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Copyright:  © 2021 Heneghan CJ et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
How to cite: Heneghan CJ, Spencer EA, Brassey J et al. SARS-CoV-2 and the role of airborne transmission: a systematic review [version 1; peer review: 1 approved with reservations, 2 not approved]. F1000Research 2021, 10:232 (https://doi.org/10.12688/f1000research.52091.1) First published: 24 Mar 2021, 10:232 (https://doi.org/10.12688/f1000research.52091.1) Latest published: 19 Oct 2022, 10:232 (https://doi.org/10.12688/f1000research.52091.3)

Introduction

Airborne transmission is defined as the spread of an infectious agent caused by the dissemination of droplet nuclei (aerosols) that remain infectious when suspended in air over long distances and time1. A collection of particles (liquid or solid) ranging in size from 0.001 μm to over 100 mm suspended in a gas defines an aerosol2. Droplet nuclei are airborne residue (with or without embedded pathogens) of a respiratory droplet containing non-volatile solutes, from which water has evaporated to the point of equilibrium with the ambient relative humidity defines3.

Airborne transmission via droplets and aerosols enables some viruses to spread efficiently among humans, causing outbreaks that are difficult to control. Many studies, however, often report inconclusive findings as many outbreaks are studied retrospectively and evidence to inform transmission from controlled experiments is often not available4,5. Among case clusters for which airborne transmission is hypothesised, published detailed investigations cannot rule out that droplet and fomite transmission could also explain human-to-human transmission6. Therefore, we aimed to systematically review the airborne transmission evidence for SARS-CoV-2.

Methods

We are undertaking a series of living systematic reviews investigating factors and circumstances that impact the transmission of SARS-CoV-2, based on our published protocol last updated on 1 December 2020 (archived protocol: Extended data: Appendix 17) Briefly, this review aims to identify, appraise, and summarize the evidence (from studies peer-reviewed or awaiting peer review) relating to the role of airborne transmission of SARS-CoV-2 and the factors influencing transmissibility.

We searched four main databases: LitCovid, medRxiv, Google Scholar and the WHO Covid-19 database for COVID-19 using the terms Airborne: aerosol OR airborne OR airbourne OR inhalation OR air OR droplet) from 1 February 2020 up to 20 December 2020 (see Extended data: Appendix 2 for the search strategies7). Searches were updated every two weeks. We aimed to include sampling for the detection of SARs-CoV-2 in the population or the environment on airborne transmission. Studies can be observational including case series, ecological, or prospective; or interventional including randomised trials and clinical reports, outbreak reports, case-control studies, experimental studies, non-predictive modelling. Studies should include sampling for the detection of SARs-CoV-2. Studies on factors influencing transmission are included, such as location settings, meteorological or immunological factors. Studies incorporating models to describe observed data were eligible. Studies reporting solely predictive modelling were excluded. For relevant articles citation tracking was undertaken. We searched the included studies of all retrieved reviews and included them in the results section for reference.

We included field studies that included airborne sampling for SARs-CoV-2 in the population or the environment. JB performed the searches, TJ and ES performed the first screen and CH checked these initial screening of studies. One reviewer (ES) extracted data for each study, and a second reviewer (CH) checked and edited the extraction. We extracted information on the study characteristics, the study population, setting and methods, and the main results from included studies. We also extracted data on the type of study, setting, sample source and methods, RT-PCR positive samples for SARS-CoV-2 RNA including cycle threshold (Ct) and copies per m3, viral culture methods and results, size of air particles (when reported) and proportion in the sample. We tabulated the data and summarised the data narratively by type of sample. Because of substantial heterogeneity across the included studies, we did not perform a meta-analysis. We assessed quality using a modified QUADAS 2 risk of bias tool,8. We simplified the tool as the included studies were not designed as primary diagnostic accuracy studies and the quality of transmission studies is known to be low9. We gave particular importance to the description of methods for air sampling and the reporting of sufficient detail to replicate. We summarise data narratively and report the outcomes as stated in the paper, including quantitative estimates when reported and the detection of culture of SARS-CoV-2.

Results

We identified 89 studies (see Figure 1; 19 full-text studies were excluded because they were not reviews or there was no SARs-CoV-2 airborne transmission outcome studied and we excluded four laboratory studies: see Extended data: Appendix 3 for a list of excluded studies7). We included 67 primary studies and 22 systematic reviews (see Extended data: Appendix 3 for references to included studies and Table 1 and Table 2 for the characteristics of the included studies7).

c6ec3de6-4882-4d44-ae41-fa814d87b0d1_figure1.gif

Figure 1. Flow chart.

Table 1. Study characteristics: primary studies.

AuthorsSettingCountryMethodSamples sourceAir Samples PCR positive for SARs-CoV-2 RNA (unless otherwise stated)Viral cultureViral concentrations copies/m3 or copies/L or Cycle threshold (Ct)size of air particles and proportion in sampleNotes
Ahn JY 2020HospitalChinaAir (and surface) samples
collected. Virus culture
was attempted on PCR
positive samples.		Air sampling at 1.2 m above floor level, 1.0 m
from each patient, using an SKC BioSampler
and a Swab sampler. 		0/ (denominator unclear)
samples 		Not attempted.N/A (no air samples positive)N/AViral RNA was detected in the air
outlet fan on the ceiling suggesting
airborne contamination by
aerosols. Only the outside surface
of the endotracheal tubes in the
area connected to the ventilator
circuit tested positive for SARS-
CoV-2 Viable viruses detected
on the outside surface of the
endotracheal tube and and seven
sites in patient 3's room.
Bays D 2020Healthcare settingUSATwo detailed case studiesNo sampling performedNot attempted.N/AN/AN/AA total of 421 health care
workers were exposed in total,
and the results of the case
contact investigations identified
8 secondary infections in health
care workers. In all 8 cases, the
staff had close contact with the
index patients without sufficient
personal protective equipment.
Importantly, despite multiple
aerosol generating procedures,
there was no evidence of airborne
transmission.
Binder 2020HospitalUSACase series of 20
patients hospitalized with
coronavirus disease 		8 National Institute for Occupational
Safety and Health (NIOSH) BC 251 Aerosol
Samplers (Figure S3) were placed 1.5m from
the ground, at ~1 meter, ~1.4 meters, ~2.2
meters, and ~3.2 meters from the SARS-CoV-
2 patient’s head and subsequently run for
~4 hours. 195 air samples were collected 		3/195 samples from 3
patients 		0/3 viable virusSample at 1.4m, <4uM first
PCR Ct 36.6, second PCR
Ct 37.1
Sample at 2.2m, <4uM first
PCR 37.4, second PCR Ct 39.9
Sample at 2.2m, >4uM first
PCR 39.1, second PCR Ct 39.6		detected in aerosols
particle size <4 µm 		for captured droplet size, the
NIOSH sampler has roughly a 95%
collection efficiency for aerosols
with a diameter of 7 µm or less,
which decreases t\o approximately
40% efficiency for aerosols ~80 µm
in diameter. Dry cyclone aerosol
samplers, which are not as well-
suited for viable virus collection
when compared to liquid collection
medium-based bioaerosol
samplers
Charlotte N 2020Choir practiceFranceFollow-up of a choir
practice: 27 participants,
including 25 male
singers, a conductor and
an accompanist attended
a choir practice on 12
March 2020.		No sampling performedNot attempted.Not attempted.N/AN/A70% of the participants (19/27)
were diagnosed with COVID-19
from 1 to 12 days after the
rehearsal (median 5.1 days).
Cheng VCC 2020aHospitalChinaAir sampling: 6 patients’
air sampled, and 5
positive controls 		The air sampler was perpendicularly
positioned 10 cm away from the patient’s
chin, collecting at a rate of 50 L/minute. An
air tent was used to increase the proportion
of exhaled air collected. Participants
sneezed directly onto gelatin filter and spit
saliva droplets onto gelatin filter.		0/6 Not attempted.N/A (no air samples positive)N/AInfection isolation rooms had 12
air changes per hour. 5% surface
samples were found to be PCR-
positive.
Cheng VCC 2020bHospitalChina Air sampling using ISO
180 model 86834 air
sampler was performed
in the room of a patient.		Air samples were collected 10 cm from the
one patient’s chin. The patient performed 4
different manoeuvres (normal breathing, deep
breathing, speaking “1, 2, 3” continuously, and
coughing continuously) while putting on and
removing the surgical mask. 		0/8 Not attempted.N/A (no air samples positive)N/ASARS-CoV-2 was identified in 1 of
13 environmental surface samples
of the patient’s room.
Chia PY 2020HospitalSingaporeAir (and surface)
sampling surrounding 61
hospitalized COVID-19
patients in airborne
infection isolation rooms		Air sampling was performed in three of the
27 airborne infection isolation rooms (AIIRs).
Bioaerosol samplers used to collect air
samples, set at a flow-rate of 3.5 L/min and
run for four hours, collecting a total of 5,040
L of air from each patient’s room.		2/3Not attempted.Total SARS-CoV-2
concentrations in air ranged
from 1.84 × 103 to 3.38 × 103
RNA copies per m3 air
sampled. 		positive particles
of sizes >4 µm and
1–4 µm detected in
two rooms		Patient 1 intermittently faced the
samplers seated 1m from the 1st
tripod and 2.1m from the 2nd.
In the rooms of Patients 2 and
3, three NIOSH samplers were
attached to each of two tripod
stands at 1.2m, 0.9m, and 0.7m
height. Patients 2 & 3 remained
in bed within 1 m from all 6 air
samplers. Patient 3 was also
talking on the phone for much of
that time.
Chirizzi D 2020OutdoorItalyStudy of the outdoor
concentrations and
size distributions of
virus-laden aerosol
simultaneously collected,
in May 2020, in northern
(Veneto) and southern
(Apulia) regions of Italy. 		Genetic material of SARS-CoV-2 (RNA) was
determined, using both real time RT-PCR
and ddPCR, in air samples collected using
PM10 samplers and cascade impactors
able to separate 12 size ranges from
nanoparticles (diameter D & 0.056 µm) up to
coarse particles (D > 18 µm).		Outdoor atmospheric
concentrations of SARS-
CoV-2 were very small (<0.8
copies m−3) 		Not attempted.SARS-CoV-2 concentrations
were <0.8 copies m−3 for
each size range.		(D < 0.056 µm) up to
coarse particles (D >
18 µm) 		It is possible to conclude that
outdoor air in residential and
urban areas was generally not
infectious and safe for the public in
both northern and southern Italy,
with the possible exclusion of very
crowded sites (See Liu 2020)
Declementi M 2020HospitalItaly Air sampling to
assess environmental
contamination in a
COVID-19 non-Intensive
Care Unit. Two patients
admitted to the hospital
rooms were positive for
COVID-19 for more than
a week. 		8 air samples were collected before and
after the application of two different
sanitization devices. Pumps were placed
in 4 sites: patient 1 room, patient 2 room,
an empty room nearby patients’ rooms,
corridor outside the rooms. Pumps (47
mm filter cassettes and 0.45 μm filters in
polytetrafluoroethylene-PTFE) positioned
1 meter above the floor for 340 minutes
at 15 l/min. 		0/8 Not attempted.N/A (no air samples positive)N/A Surface samples collected before
and after sanitization (n=24)
were all negative. Patient 1
rhinopharyngeal swab was positive
while patient 2 rhinopharyngeal
swab was negative (Table 2).
De Man P 2020Care homeThe
Netherlands		Case series. Responding
to an outbreak in a care
home, the ventilation
system of the outbreak
ward was investigated
in addition to routine
source and contact
tracing		No air samples collected.Not attempted.N/AN/A N/A The ventilation system allowed
recirculation of air below a
certain CO2 limit. The outbreak
ward was additionally cooled by
2 air conditioning units, which
recirculated air through a 1-mm
mesh dust filter. The other 6 wards
(no outbreak) were ventilated with
outside air.
Di Carlo P 2020Inside a busItalyObservational
measurements were
carried out across
the last week of the
lockdown and the first
week when, gradually, all
travel restrictions were
removed. 12 to 22 May
2020 in Chieti, Italy. 		Samples of air inside the bus were taken
every day of the two observational weeks,
excluding weekends. Two microbiological
gelatine membrane sample filters of 80
mm diameter were installed on board: one
close to the ticket machine, the other on
the rear part of the bus. All the air samples
were gathered during the 6.5 hours daily
operation of the bus,		0/14 Not attempted.N/A (no air samples positive)N/A During the whole observation
period about 1100 passengers
travelled on the trolleybus. Hand
sanitizing was a strict requirement
to get on the bus, and rule of
wearing a facial mask during travel,
and the recommendation to keep
the windows open to allow high air
ventilation.
Ding Z 2020HospitalChinaSampling, including of
air, within and around 4
isolation rooms each with
3 patients. Other areas in
the hospital and its roof
air-exhausts were also
sampled. 		46 air samples, two exhaled condensate
samples, and two expired air samples (also
47 surface samples) were collected within
and beyond the 4 three-bed isolation rooms. 		1/46 air samples weakly
positive. Both exhaled
condensate samples
negative.
Both expired air samples
negative.		Not attempted.RNA copies for weakly
positive sample not
calculated.		NRThe toilet area was the area most
contaminated by SARS-CoV-2 RNA
as detected by PCR. Two exhaled
condensate samples and the two
expired air samples were negative .
Dohla M 2020Quarantined
households		GermanyStudy of 43 adults and
15 children living in 21
households; air (also
surface and wastewater)
samples taken.		Air samples obtained using Coriolis Micro-
Air sampler; air collectors were positioned
in the middle of the room used most
frequently by the residents (usually the living
room or kitchen) - no rooms had ventilation
equipment. Close contact to the air sampler
was avoided (e.g. speaking in a range below
2 m but not above 3 m). 		0/15 Infectious virus could
not be isolated in
Vero E6 cells from any
environmental sample.		N/A (no air samples positive)N/A 26 of all 43 tested adults were
positive by RT-PCR.
10 of 66 wastewater samples and
4/119 surface swab samples were
positive for SARS-CoV-2
Dumont-LeblondN 2020HospitalCanadaAir sampling in acute
care hospital rooms over
the course of nearly two
months		100 air samples in acute care hospital rooms
hosting 22 patients using three different air
sampling protocols. Two conductive plastic
Institute of Occupational Medicine (IOM)
samplers with 3 µm gelatine filters or one
IOM and a 37 mm cassette with 0.8 µm
polycarbonate filters.		11/100 from 6 patient
rooms		Viral cultures were
negative		Among 11 positives for N
gene target, Ct ranged from
36.46 to 39.8, mean 37.99.
Among 8 positives for ORF1b
target, Ct ranged from 32.07
to 35.15, mean 33.69
Among the 8 positive for
both N and Orf1b, viral
concentrations ranged from
9.86 to 514.17, mean 201.64
genomes /m3 		NREven when the IOM and cassette
were positive (patient D), SARS-
CoV-2 could not be recovered
in the air using the SASS®3100
according to the protocol. 7/11
positive air samples collected
using IOMs. When both IOMs and
cassettes were used, cassettes
lead to positive results more often
than IOMs (5/5 vs. 3/5) and higher
concentrations overall. "No live
virus was isolated from air samples,
either due to viral inactivation
through the sampling process
or the true absence of whole,
infectious virions."
Faridi S 2020HospitalIranAir sampling in wards
of Covid-19 patients
with severe and critical
symptoms.		10 air samples were collected into the sterile
standard midget impingers containing 20
mL DMEM with 100 μg/mL streptomycin,
100 U/mL penicillin and 1% antifoam
reagent for 1 h. Air samplers placed 1.5 to
1.8 m above the floor and approximately
2 to 5 m away from the patients' beds.
Some patients coughed during the sample
collection. 		0/10 Not attempted.N/A (no air samples positive)N/A. Air samples which were collected 2
to 5 m from the patients' beds
Feng B 2020HospitalChinaEnvironmental
contamination
investigated around 21
COVID-19 patients in the
later stage of infection		For sampling of isolation room air, a NIOSH
sampler was placed on a tripod 1.2 m in
height and 0.2 m away from the bed at the
side of the patient’s head. The sampling
duration was 30 min, and a total of 105-L
room air was sampled. (9 Exhaled Breath
(EB) samples, 8 Exhaled Breath Condensate
(EBC) samples, 12 bedside air samples)		0/14 EB
2/8 EBC
1/12 room air		Not attempted.RNA detected in air sample,
with virus concentrations
of 1111 copies/m3 and 744
copies/m3 in the <1 μm and
>4 μm fractions, respectively		RNA detected in air
sample in <1 μm and
>4 μm fractions, 		An exhaled aerosol collection
system was developed and the
patients were asked to breathe
normally through a mask for 30
min, and asked to perform 10
forced coughs during this time.
Ge XY 2020HospitalChina Environmenta; air
samples from 6 different
sites of 3 hospitals		Air samples were collected for 30 min using
the National Institute for Occupational
Safety and Health (NIOSH) bioaerosol
sampler (BC251) with air pumps (XR5000,
SKC). The stream of air has been set to 3.5
L / minute. 		ICU 3/3
Haemodyalysis clinic 0/12
fever clinic 0/12
respiratory ward 0/6		Not attempted.ICU: Ct 36.5 - 37.8NR
Günther T 2020Meat Processing
Plant 		GermanyStaff tested based on
self‐reported symptoms,
possible contacts to
other infected persons,
returning to work after
more than 96 h absence
from work		Eight air conditioning units placed near
the ceiling in the proximal half of the room
constantly cool the air. Fans project the air in
a lateral direction, either directly from frontal
openings in the unit or via perforated hoses
mounted underneath the ceiling		Not attempted Not attempted.N/A. N/A. Low temperature, low air
exchange rates, and constant
air recirculation, together with
relatively close distance between
workers and demanding physical
work, may have promoted efficient
aerosol transmission.
Guo ZD 2020HospitalChinaAir (and surface) samples
of ICU and Covid-19
wards.		Indoor air and the air outlets were sampled
to detect aerosol exposure. Air samples
were collected by using a SASS 2300 Wetted
Wall Cyclone Sampler at 300
L/min for 30 min. Samples were tested for the open
reading frame 1ab and nucleoprotein (N)
genes of SARS-CoV-2 by qRT- PCR		AIr samples:
14/40 ICU*
2/16 General Ward
Air outlet swab samples:
8/12 for ICUs
1/12 for GWs. 		Not attempted.Indoor air near the air outlet:
Ct 35.7, 3.8/L
Indoor air near the patients:
Ct 44.4. 1.4/L
Indoor air near the doctor's’
office area: Ct 12.5 0.52/L		NR*ICU high-risk area was the patient
care and treatment area, where
rate of positivity was 40.6% (13/32).
The low-risk area was the doctor's’
office area, where rate of positivity
was 12.5% (1/8).
Hamner L 2020 and
Miller SL 2020		Choir PracticeUSAFollow up of choir
practice attendees 		In total, 78 members attended the 3rd
March 2020 practice, and 61 attended
the 10th March 2020 practice. Overall, 51
(65.4%) of the 3rd March practice attendees
became ill; all but one of these persons also
attended the 10th March practice. Among
60 attendees at the 10th March practice
(excluding the patient who became ill 7th
March, who also attended), 52 (86.7%) choir
members subsequently became ill. 32 were
confirmed and 20 probable secondary
COVID-19 cases occurred.		Not attempted.Not attempted.N/AN/AAttendees had a 15-minute
break, during which cookies and
oranges were available at the
back of the large room. No one
reported physical contact between
attendees. The seating chart was
not reported because of concerns
about patient privacy. One hour of
the practice occurring outside of
the seating arrangement,
Hernández JL 2020HospitalMexicoAir samples of
Emergency areas and
Covid-19 patients rooms.		Air sampled in three areas: Emergency area
(Clinic A), Internal medicine (Clinic A), COVID
19 patient area (Clinic A), and COVID-19
patients care room (Clinic B). Sampling in
all areas was accomplished in 3 h. Filters of
25 mm diameter with 0.22 μm pores were
utilized (Millipore, AAWP02500), placed in a
sterilized filter holder (Millipore, SWINNX)
coupled to a vacuum system through a
previously disinfected plastic hose, filtering
the air with a flow of 9.6 L/min in each filter
holder.		3/15 Not attempted.Not reportedfiltration through 0.22
μm pores.		All three positive samples were in
COVID 19 patient area (Clinic A)
Horve PF 2020HospitalUSAAir handling units (AHUs)
sampled, including the
pre-filters, final filters,
and supply air dampers.		Samples were collected using Puritan
PurFlock Ultra swabs and swabs were
taken in triplicate at each AHU location
from the left, middle, and right side of each
area along the path of airflow. Swabs were
pre-moistened using viral transport media.
Swabbing occurred for 20 seconds on an
area approximately 20 X 30 cm at each
location and swabs were immediately placed
into 15 mL conical tubes (Cole-Parmer,
catalog #UX-06336-89) containing 1.5 mL
viral transport media and stored on ice
for transport to a BSL-2 laboratory with
enhanced precautions (BSL2+) lab for
processing, which typically occurred within
two hours after collection. 		14/56 s Not attempted.The highest abundance
sample (~245 gene copies)
was found on the pre-filters,
where outside air mixes with
recirculated building air.
[Other copy number data not
found in report.]		NRHighest abundance sample (~245
gene copies) was found on the pre-
filters, where outside air mixes with
recirculated building air. Of the
samples collected, 35% (7/20) of
samples at the pre-filters, 16.67%
(2/12) of samples at the final filter,
and 20.8% (5/24) of samples at
the supply air dampers contained
detectable SARS161 CoV-2 RNA
Hu J 2020HospitalChinaIndoor and outdoor air
samples in ICUs and CT
rooms 		Aerosol samples were collected over 30
min intervals with the use of a centrifugal
aerosol-to-hydrosol sampler (WA-400,
Beijing Dingblue Technology Co., Ltd.,
China). Twenty-three masks from patients
and 24 swabs from surfaces in ICUs were
also collected and analyzed. Ten 3MTM
VersafloTM TR-600 respirator filters and 40
masks from healthy workers in the P3 lab of
Wuhan Institute of Virology were collected
for viral RNA detection. The airflow rate of
the respiratory filters was 190 L/min and
the surface area was ~30 cm2. All viral RNA
positive aerosol samples were subjected
to cell culture. All viral RNA positive aerosol
samples were subjected to cell culture to
determine whether viable virus could be
recovered from them.		Aerosol samples
8/38 from ICUs
1/6 from CT rooms
samples from medical
staff rest areas and
corridors, were all negative
(denominator not clear)		All positive aerosol
samples were negative
after three passages of
Vero-E6 cells inoculated
in a blind test. 		The range of virus
concentrations in the positive
aerosol samples was 1.11
× 103 to 1.12 × 104 RNA
copies m3. In 10% of the
outdoor air samples collected
10 m from the doors of
inpatient and outpatient
buildings, respectively, viral
concentrations ranged
from 0.89 to 1.65 × 103 RNA
copies m3.		NR5 surface swabs (cabinet, patient’s
bed rail, door handle, and patient
monitor) out of 24 from the ICU
were positive for SARS-CoV-2,
with viral RNA. After rigorous
disinfection, no viral RNA was
detected in a second batch
samples from the same places.
Positive rates for the mask samples
were relatively high compared with
the aerosol or surface samples.
All positive masks were subjected
to cell culture and inoculated with
Vero-E6 cells after blind passage
for three generations. One mask
from a critically ill patient detected
positive.
Jiang Y 2020HospitalChinaIndoor air samples from
Covid-19 isolation ward		Air was collected by two methods: natural
sedimentation and a microbial air sampler
(MAS-100 ECO), for which the stream of air
was set to exactly 100 liters/minute (Merck,
Germany).		1/28 air samples Not attempted.Not reported NRThe isolation ward with an ICU
patient was positive. Based on
the original 24 hours of UV air
filtering and 1000-2000 mg/L
chlorine-containing disinfectant for
ambient air and floor disinfection,
the frequencies and duration times
of air disinfectants were extended.
Key surfaces such as computer
keyboards easily overlooked
were clearly noted and carefully
disinfected. The samples from the
positive area and indoor air were
collected 24 hours later, and the
test results were negative.
Jin T 2020HospitalChinaAir and surface samples
of ICU of one Covid-19
patient.		Two hours after routine cleaning, high-
volume air samples were taken 0.5m from
the patient bed and in the staff PPE dressing
room, using a WA 400 Portable viral aerosol
sampler at 400 L/min for 15 min at 1.5m
height, while the patient was present and
was not wearing a mask.		Air sample:
0/1 staff PPE dressing room
1/1 ICU patient isolation
room 		Not attempted.Not reportedNRAll surface samples tested
negative. The concentration of
airborne SARS-CoV-2 was not
quantified. The aerodynamic size
distribution of SARS-CoV-2 aerosols
was not evaluated.
Kang M 2020Block of flatsChinaAir (and surface)
sampling, and
experimental air flow
study. 		Air samples from 11 of the 83 flats in
the building, public areas, and building
drainage systems.Investigated gas flows and
dispersion as an indicator of the movement
of virus-laden droplets in the drainage
system, tracer gas (ethane) was released
into bathrooms. The hydraulic interactions
of toilet wastewater and the stack were
observed. 		0/11 air samplesNot attempted.N/A (no air samples positive)N/AVirus-containing fecal aerosols
may have been produced during
toilet flushing by index cases.
The infected families lived in 3
vertically aligned flats connected
by drainage pipes in the master
bathrooms. There were 9 infected
patients, 193 other residents of the
building, and 24 members of the
building's management staff.
Kenarkoohi A 2020HospitalIranAir sampling through
hospital wards indoor air
by confirmed COVID-19
patients on 7th May
2020.		A liquid impinger biosampler calibrated for
a flow rate of 12 L.min−1 at 1.5 m above
ground floor and at least 2 m away from
the patient beds was used to take fourteen
air samples in different wards of the indoor
air of the hospital: ICU, ICU entrance hall,
hospital entrance hall, laboratory ward, CT
scan, radiology, men internal ward, woman
internal ward and emergency ward.		2/14 air samples (both
in ICU) 		Not attempted.Cycle threshold (CT) values
were around 38 and 35 for
ORF1ab and nucleoprotein
gene, respectively.		The particulate
matter PM1,
PM2.5 and PM10
concentrations during
the air
sampling in the
hospital wards was
reported but no RNA
samples 		Two of 14 air samples contained
SARS-CoV-2 RNA. Droplet
vs airborne could not be
distinguished.
Kim UJ 2020HospitalKoreaSurface and air sampling.The rooms of 8 COVID-19 patients in
four hospitals. On days 0, 3, 5, and 7 of
hospitalization, the surfaces in the rooms
and anterooms were swabbed, and air
samples were collected 2 m from the patient
and from the anterooms. 		0/52 air samples positive
for SARS-CoV-2 RNA		Not attempted.N/A (no air samples positive)N/AAll 52 air samples from 8 Covid-19
patients’ rooms were negative
for SARS-CoV-2 RNA. Surface
contamination with SARS-CoV-2
RNA was widespread; negative
after disinfectant cleaning.
Kwon KS 2020CommunityKoreaInvestigation was
implemented based
on personal interviews
and data collection on
closed-circuit television
images, and cell phone
location data. 		A total of 39 environmental samples of
inlets and outlets of air conditioners, table
seat of case A, and nearby tables and chairs
in consideration of air flow direction were
collected on June 23 for testing of SARS-CoV
-2 in the environment and were analyzed
by rRT-PCR test. Air speed and direction at
several specified positions were precisely
measured using a portable anemometer 		0/39 positive Not attempted.N/A (no air samples positive)N/AMaximum air flow velocity of
1.2 m/s was measured between
the infector and infectee in
a restaurant equipped with
ceiling-type air conditioners.
Environmental samples were
collected at 11 days after the
inspector visit.
Lednicky JA 2020aHospitalUSAAir samples collected,
and virus culture
attempted		VIVAS air samples from the room of two
COVID-19 patients were set up 2m to 4.8m
away from the patients. Three serial 3-hr air
samples were collected. For each sampler,
the second of the three samplings was
performed with a high efficiency particulate
arrestance (HEP A) filter affixed to the inlet
tube, a process to reveal whether virus
detected in consecutive samplings reflect
true collection and not detection of residual
virus within the collector.		4/4 air samples without a
HEPA filter
0/2 samples using a HEPA
filter		Virus-induced CPE were
observed for 4/4 RNA-
positive air samples.		Four positive samples
estimated to contain:
2.82E+03, 9.12E+02,
1.15E+03, 4.68E+02 genome
equivalents/ 25 μL, with Cycle
quantification (Cq) values
36.02, 37.69, 37.42, 38.69,
respectively (mean Cq 37.46)		NRNo other respiratory virus was
identified in the samples using a
BioFire FilmArray Respiratory 2
Panel. The amount of airborne
virus detected per liter of air was
small. Plaque assays could not be
performed due to a nationwide
non availability of some critical
media components (due to COVID-
19 pandemic-related temporary
lockdown of production facilities),
so TCID50 assays were performed
in Vero E6 cells to estimate the
percentage of the collected
virus particles that were viable.
Estimates ranged from 2 to 74
TCID50 units/L of air
Lednicky JA 2020bStudent
Healthcare centre		USAAir samples collected,
and virus culture
attempted		The air sampling device was placed in a
hallway along which potential Covid-19
cases walked, wearing a mask, to reach
clinical evaluation rooms. The air inlet was
approximately 1.5m above floor level.		1/2General virus-induced
cytopathic effects were
observed within two
days post-inoculation		0.87 virus genome
equivalents L -1 of air; Ct
value 39.13		NRThe amount of virus present in
390 L of sampled air was low
(approximately 340 virus genome
equivalents). PCR tests for SARS-
CoV-2 vRNA from cell culture were
negative. Three respiratory viruses
were identified using the Biofire
RVP: Influenza A H1N1, Influenza
A H3N2, and Human coronavirus
OC43
Lei H 2020HospitalChinaAir and surface samples
from the intensive
care unit (ICU) and an
isolation ward for COVID-
19 patients. 		Air samples were collected with a two‐stage
cyclonic bioaerosol sampler (NIOSH) and an
aerosol particle liquid concentrator, between
8am and 12 noon. The NIOSH sampler was
placed on a tripod at the head of the bed
within 1m of the patient's head at a height
of 1.3 m. In the isolation ward, the sampler
was also used in the bathroom by mounting
it on an infusion support near the sink, < 1m
from the toilet. 		Surface and air:
1/218 ICU samples
2/182 isolation ward
samples		Not attempted.near the head of the patient
Ct 41.25.		NRThe number of air samples is
unclear. One air sample collected
using the DingBlue sampler placed
near the head of the patient in bed
14 showed amplification at cycle
threshold (Ct) 41.25.
The detection of viral RNA was also
in the air samples in the bathroom.
Li YH & Fan YZ 2020HospitalChinaAerosol samples &
surface samples collected
in a hospital for severe
COVID-19 patients		Aerosol samples collected by an
impingement air sampler BIO-Capturer-6.
135 135 aerosol samples from 45 locations
taken from the ICU ward, general isolation
wards, fever clinic, storage room for medical
waste, conference rooms and the public
area.		0/135 Not attempted.N/A (no air samples positive)N/A The ICU ward has 12 air inlets
with 16 discharges per hour;
isolation room 8 air inlets with 12
discharges per hour. COVID-19
patients in a ward were separated
by a minimum of 1.5 m. Air was
cleaned with 4-time-daily air
disinfection using a plasma air
steriliser. with the exception of two
samples from a COVID-19 patient's
mask, all 90 environmental
surfaces sampled were negative
for SARS-CoV-2.
Li Y & Qian H 2020RestaurantChina Observational and
experimental: Data
from a video record
and a patron seating-
arrangement from the
restaurant in Hong Kong
were collected. Secondly,
the dispersion of a warm
tracer gas was assessed,
as a surrogate for
exhaled droplets		No sampling performedNot attempted.N/AN/A N/A
Lin G 2020Block of flatsChina Case series: Nine
COVID-19 cases in
one community in
Guangzhou who lived in
three vertically aligned
units of one building
sharing the same piping
system.		Given that all the cases occurred in the
same unit and that these households
shared a common pipe system, we therefore
conducted a tracer-gas experiment
to simulate the process of potential
transmission through air		Not attempted.N/AN/A N/A Airflow detection and simulation
experiment revealed that flushing
the toilets could increase the
speed of airflow in the pipes
and transmitted the airflow from
Apartment 15-b to 25-b and 27-b.
Reduced exhaust flow rates in
the infected building might have
contributed to the outbreak.
Liu Y & Ning Z 2020Hospital and
public spaces 		ChinaMeasured SARS-CoV-2
RNA in air samples from
2 Covid-19 hospitals,
and quantified the copy
counts using a droplet
digital PCR-based
detection method 		Over a 2 week period: 30 aerosol samples
of total suspended particles collected
on 25-mm-diameter filters loaded into
styrene filter cassettes (SKC) by sampling
air at a fixed flow rate of 5.0 l min−1 using
a portable pump (APEX2, Casella). Three
size-segregated aerosol samples collected
using a miniature cascade impactor (Sioutas
Impactor, SKC) that separated aerosols into
five ranges (>2.5 μm, 1.0 to 2.5 μm, 0.50 to
1.0 μm and 0.25 to 0.50 μm on 25-mm filter
substrates, and 0 to 0.25 μm on 37-mm
filters) at a flow rate of 9.0 l min−1. Two
aerosol deposition samples collected using
80-mm-diameter filters packed into a holder
with an effective deposition area of 43.0
cm2; filters were placed intact on the floor in
two corners of an ICU for 7 days.		ICU, 2/3 positive
15/22 Isolation wards &
ventilated rooms
4/11 public areas 		Not attempted.ICU - 31 &113 copies m3
Isolation wards & ventilated
rooms (concentrations very
low: <43 m3.
public areas (very low
concentrations (<11 m3 ) 		NRNegatively pressurized isolation
and high air exchange rates were
inside the intensive care units,
coronary care units and ward
room. Reported values are virus
aerosol deposition rates in copies
m−2 h−1. Very low or undetectable
concentrations of airborne SARS-
CoV-2 were found in most of the
patient areas of Renmin Hospital.
The authors suggest that the
negatively pressurized isolation
and high air exchange rate inside
the intensive care units, coronary
care units and ward room of
Renmin Hospital are effective in
limiting the airborne transmission
of SARS-CoV-2.
Lu J 2020RestaurantChina Study of an outbreak
apparently centred
on a restaurant; air
flow studied & surface
samples taken		Air samples not taken. 6 smear samples
taken from the air conditioner (3 from the
air outlet and 3 from the air inlet)		Not attempted.N/AN/A N/A 0/6 smear samples tested positive
by PCR.
Luo K 2020Bus trip ChinaCase study of a SARS-
CoV-2 outbreak event
during bus trips of an
index patient in Hunan
Province, China.		No sampling performedNot attempted.N/AN/A. N/A. Could not verify transmission
via fomites as no environmental
samples were collected; (2) the
SAR was likely overestimated as it
is solely based on a single large
cluster; (3) there might be recall
bias because the information
(including the seat number) was
collected retrospectively; (4) no
viral genetic sequence data were
available from these cases to
prove linkage; and (5) some of the
secondary and tertiary cases could
have been exposed to unknown
infections
Ma J 2020Hospital and
quarantine hotel 		ChinaExhaled breath
condensate (EBC)
samples were collected
from 20 imported COVID-
19 cases, 29 local cases
and 15 healthy controls. 		EBC samples were collected using a
BioScreen device developed by Peking
University. 242 surface swabs from
quarantine hotels and hospitals or from
personal items of COVID-19 patients were
obtained using wet cotton swabs		14/52 EBC sample positive;
1/26 air samples positive		Not attempted.EBC samples, 14 positive:
Ct values 35.54 ± 3.14 were
obtained for each positive.
The breath emission rate
was estimated to be from
1.03 × 10 5 to 2.25 × 10 7
viruses per hour. The positive
air sample was estimated
to contain 6.07 × 10 3
viruses/m3. 		NRIn the ward of patient C, the virus
was present on the surface of an
air ventilation duct entrance that
was located below the patient’s
bed. Cycle threshold range (N or
ORF1a/b) for EBC samples 35.5 ±
3.1 and air samples CT = 38.4. 1
sample (air-1) from an unventilated
quarantine hotel toilet room was
positiv SARS-CoV-2 emission does
not continue at the same rate but
rather is a sporadic event. For
example, 2 EBC samples (EBC-1,
EBC-2) collected from patient E but
on different dates and using the
same method returned different
test results
Marchetti R 2020HospitalItalyAir sampling in three
different hospitals in
Milan, Italy.		For particles’ sampling the AEROTRAK™
Portable Airborne Particle Counter was used
for cleanroom particles classification. For
microbiological air sampling, the SAS Super
IAQ Surface Air System (model 90593),
which conveys a known volume of air during
a fixed period on Petri Plates filled with
Standard Plate Count Agar (PCA) was used.
Ten AIRcel units per hospital were placed
in three different hospitals in Milan, Italy. In
total 68 samples were processed in three
distinct test sessions between April and
June 2020, using the QIAGEN Rotor-Gene
thermal cycler.		E gene 19/68 samples,
ORF1ab + N detected in
7/68 samples.
.		Not attempted.Not reported NRThe result of the RT-PCR showed a
marked presence of the target β-
coronavirus E gene for 19 of the 68
samples, while the target ORF1ab
+ N was detected in 7 samples. In
particular, at Sacco Hospital, the
test results show the detection of
ORF1ab + N and/or E gene in 15
samples out of 40.
Masoumbeigi H2020Military hospitalIranRandom air sampling
with continuously
sterilised sample
equipment		All patients aged 55-65 were either
intubated or had severe symptoms.
Sampling of 100-1000 l for 20 mins in two
randomly chosen stations 0.5 metres from
the beds. RT-PCR performed at 42 cycles.
Air sampling was done (n = 31) on selected
wards including Emergency 1, Emergency
2, bedridden (4-B, 10-D), ICU 2, ICU 3, CT-
SCAN, and laundry.		0/31Not attempted.N/A (no air samples positive)N/A. Cycle threshold for detection
used = 42
McGain F 2020HospitalAustraliaCase report of a
tracheostomy procedure;
air samples were
collected throughout		Two spectrometers to measure aerosol
particles: the portable Mini Wide Range
Aerosol Sizer 1371 (MiniWRAS) and the
Aerodynamic Particle Sizer (APS). During the
procedure, the aerosol detector inlet was
positioned 30 cm directly above the patient’s
neck, representing the surgeon’s breathing
air space		Not attempted.Not attempted.N/A APS detected larger
aerosols (> 0.37
mm) and MiniWRAS
smaller particles
(0.01–0.35 mm).		Maximum aerosol particles were
generated during diathermy, but
overall low levels. It is unlikely
that viruses will survive the high
temperature of diathermy.
Moreno T 2020Buses and
Subway Trains		Spain75 samples from buses
and 24 from subway
trains, collected from
surfaces using swabs (78
samples), from ambient
air (12 samples), and
from air-conditioning
filters (9 samples)		Air sampling in the subway took place June
17–19, 2020 on three consecutive days.
Six samples of particulate matter with a
diameter of <2.5 µm (PM2.5) were collected
inside 6 trains using 47 mm Teflon filters
with PEM (Personal Environmental Monitor)
equipment. The sampling of the buses took
place between 20:00 and 03:00 on the night
of May 25–26, 2020 in one of the four main
bus depots in Barcelona. After sampling, the
bus was disinfected. 		1/6 air samples on buses
gave weak positive result
2/6 subway trains		Not attempted.Bus: Positive sample genome
count values ranged between
14 to 446/m2 for IP2, 9 to
490/m2 for IP4 and 5 to
378/m2 for E. Subway: first
positive sample estimated
viral load 23.4 GC/m3,
second positive sample the
amplified target gene regions
were IP2 (18.8 GC/m3) and
the envelope protein E (5.6
GC/m3).		NROnly fragments of 1 or 2 gene
targets were identified, not an
infectious virion, and furthermore,
even if they were infectious
viruses, it is estimated that only
one particle in 10 million would
be able to produce an infectious
cycle. Bus calculated viral load
(supposing that RNA represents
the unlikely worst situation of
being representative of infective
virus load) of 1.44 GC/m3. 6 PM2.5
samples collected in ambient air
2 gave a positive signal. In the
first case the target gene region
identified was IP2, with a figured
viral load of 23.4 GC/m3. In the
second case the amplified target
gene regions were IP2 (18.8
GC/m3) and the envelope protein E
(5.6 GC/m3)
Morioka S 2020HospitalJapan2 case reports Air was sampled using an MD8 airscan
sampling device and sterile gelatin filters.
Air was sampled twice at a speed of 50
L/minute for 20 minutes in the negative-
pressure rooms of two patients and its
associated bathrooms. 		0/2 patient 1
0/2 patient 2 		Not attempted.N/A. N/A. Intubation was performed for
patient 1 three days before
the sampling. Patient 2 was
asymptomatic when the sampling
was conducted.
Mponponsuo K 2020HospitalCanadaEpidemiological
study investigating
airborne versus droplet
transmission of SARS-
CoV-2 		Air samples not taken. From 5 HCWs with
positive SARS-CoV-2 tests and Covid-19
symptoms, no onward transmission was
observed from 72 exposures		Not attempted.Not attempted.N/A. N/A. No transmission from multiple
high-risk exposures from 5 COVID-19
HCWs to either patients or other
staff.
Nakamura K 2020HospitalJapanNasopharyngeal,
environmental and air
samples from patients 		11 air samples in three negative pressure
bays (Bay 1 to Bay 3), a single negative
pressure room in a general ward (Room
1) and a single negative pressure room
in an isolation ward (Room 2) using an
MD8 airscan sampling device (Sartorius,
Goettingen, Germany) and sterile gelatin
filters (80 mm diameter and 3 μm pores;
Sartorius). We placed the device on the floor
about 1.5 meters–2 meters away from the
patient's head. Air was sampled twice, at a
speed of 50 L/minute for 20 minutes, in the
negative pressure rooms and its associated
restrooms		0/11 Not attempted.N/A (no air samples positive)N/A (no air samples
positive)		 4/141 swab samples collected
from the three bays and two single
rooms were positive
Nissen K 2020HospitalSwedenObservational: surface
swabs and fluid
samples collected, and
experimental: virus
culture was attempted.		In a Covid-19 ward, surface samples were
taken at air vent openings in isolation rooms
and in filters. Fluid sample collections were
done in the ventilation system.separate
HEPA filter systems, distance measured
to between 49 and 56 meters. Admitted
patients in the ward were between day 5
and 23 after symptom onset 		7/19 room vents
11 days later, 4/19 for both
genes.
8/9 main exhaust filters +ve
for both genes. 		No significant CPE
was seen after three
passages on Vero E6
cells from samples
retrieved from ward
vent openings or central
ventilation ducts or
filters		Petri dishes Ct values 35.32
and 33.16 for N and E genes
respectively.

Ward 1 +ve specimen had Ct
value 33.00, for E gene only.		NRCycle threshold (Ct) values varied
between 35.3 and 39.8 for the
N and E gene. Virus culture was
attempted: RNA detected in
sequential passages but CPE
not observed. Petri dishes of cell
medium, placed in inspection
hatches in the central ventilation
system prior to the exhaust filters,
were +ve for both N and E genes.
1/3 specimens from ward 1
contained only the E gene.
Ogawa Y 2020HospitalJapanObservational study of
15 HCP who had contact
exposures (15/15) and
aerosol exposures (7/15)
to a hospitalized Covid-
19 patient who re-tested
positive 18 days after
initial negative PCR. 		Air sampling not performed, All PCR tests
performed on exposed HCWs using a
nasopharyngeal swab obtained on the 10th
day after the exposure were negative, and
the results of the tests for IgG antibodies
to SARS-CoV-2 on the specimens collected
approximately 20 days after exposure were
also negative.		Not attempted.N/AN/A. N/ADue to sudden change in
symptoms, the patient underwent
nasopharyngeal and sputum PCR
testing for SARS-CoV-2 again;
the results were re-positive. Due
to this, several HCP who had
interacted with this patient had to
be marked for active isolation. The
core issue is determining whether
the patients whose PCR test results
are re-positive are infectious. A
low probability of infection from a
re-positive case.
Ong SWX 2020HospitalSingaporeAir, surface and PPE swab
samples collected for 3
hospitalized Covid-19
patients.		Air sampling was done on 2 days
using SKC Universal pumps (with
37-mm filter cassettes and 0.3-μm
polytetrafluoroethylene filters for 4 hours
at 5 L/min) in the room and anteroom and
a Sartorius MD8 microbiological sampler
(with gelatin membrane filter for 15 minutes
at 6 m3/h) outside the room. Supplemental
file Blue icons labelled A to E indicate the
position of the air samplers within the
room (A to C), anteroom (D), and common
corridor (E).		0/5 Not attempted.N/A (no air samples positive)N/ASurface contamination with SARS-
CoV-2 RNA was widespread but
undetectable after cleaning; swabs
taken at air outlets tested positive
suggesting droplet deposition; all
air samples were negative.
Orenes-Piñero E2020HospitalSpanish Study of COVID-19 traps
to measure the capacity
of SARS-CoV-2 aerosol
transmission.		“COVID-19 traps”were placed only in the
rooms of patients with a confirmed positive
diagnostic. Interestingly, the rooms where
COVID-19 patients were isolated had a
ventilation rate of 1800 m3/h. 6 different
surfaces trapped in boxes with plastic,
protective grids to avoid that samples
could be touched by the patient or by the
healthcare personnel. The different surfaces
were: polypropylene (PP), glass, polyvinyl
chloride (PVC), methacrylate, agar medium
and carbon steel. PP surfaces were obtained
from PP black panels and had a semi-gloss
finish with a thickness of 2 mm.		0/18 ICU "traps"
2/18 Covid wards "traps"		 Not attempted.Ct from positive surfaces
were more than 10 cycles
after than those obtained
from the patient, indicating
that the viral load was lower
in the room environment.		NRNo-one could touch the surfaces
of the 'traps" and patients were
isolated in their rooms. RNA was
found in two different surfaces at
72 h in the room of a patient with
a nasal cannula. No positives were
found at 24 or 48 h on the same
surfaces. The rest of surfaces,
placed in rooms with patients with no
respiratory support, were not
positive .
Razzini K 2020HospitalItalyObservational; 5 air (&
37 surface) samples
collected in the ICU for
Covid-19 patients.		Air samples done using an MD8 Airport
Portable Air Sampler with gelatine
membrane filters, 1 filter for each monitored
area.
Each aspiration cycle was 40 min with a flow
of 50 l/min. The detector was positioned
1.5 m above the floor. Air (n = 5) samples
were collected from three zones classified
as contaminated (corridor for patients and
ICU), semi-contaminated (undressing room)
and clean areas: (lockers and passage for
the medical staff and a dressing room). 		20/20 from the
contaminated area
0/8 semi-contaminated
0/9 clean areas.		Not attempted.Mean Ct for ICU air samples
22.6
Mean Ct for corridor air
samples 31.1 		NRSurface contamination with
SARS-CoV-2 RNA in Covid-19 wards
was widespread, but not found in
hospital “clean” areas. A total of
37 swab samples were collected
within the five areas and 24%
were positive for viral. Air samples
collected from ICU and corridor for
patients were positive for viral RNA
with mean concentrations of 22.6
and 31.1 Ct value, respectively. In
the present study the correlation
between the virus concentration
and the distance from patients
was also evaluated. The Spearman
coefficient suggests that there
may be a moderate correlation
and that the viral load of the
surfaces increases with the patient
proximity.
Santarpia JL 2020aHospitalUSASize-fractionated aerosol
samples collected; virus
culture was attempted.		Air samplers were placed in various places
in the vicinity of the patient, including over
2m distant. Personal air sampling devices
were worn by study personnel on two days
during sampling. Measurements were
made to characterize the size distribution
of aerosol particles, and size-fractionated,
aerosol samples were collected to assess
the presence of infectious virus in particles
sizes of >4.1 µm, 1-4 µm, and <1 µm in
the patient environment. An Aerodynamic
Particle Sizer Spectrometer was used to
measure aerosol concentrations and size
distributions from 0.542 µm up to 20 µm. A
NIOSH BC251 sampler was used to provide
size segregated aerosol samples for both
rRT-PCR and culture analysis.		6/6 patient rooms.In 3 aerosol samples of
size <1 μm, cell culture
resulted in increased
viral RNA.
Viral replication of
aerosol was also
observed in the 1
to 4 μm size but did
not reach statistical
significance.		Most RNA was identified in <1
microM particles (rather than
1-4 microM or >4.1 microM);
concentrations up to around
7.5 TCID 50 / m3 of air.		Two of 1-4
µm samples
demonstrated viral
growth, between 90%
and 95% confidence		Western blot assay was done using
the antibody against SARS-CoV
N protein, in cell supernatant
samples with statistically
significant evidence of replication.
The presence of SARS-CoV-2
was reported to be observed via
western blot for all but one of the
samples (<1 um, Room 7B) with
statistically significant evidence
of replication, by rRT-PCR (Figure 2).
Intact virus was reported to be
observed via TEM in the submicron
sample from Room 5 , and
reported as "indicating active viral
replication in that sample."
Santarpia JL 2020bHealthcare centreUSAHigh-volume (50 Lpm)
and low-volume (4 Lpm)
personal air samples
(& surface samples)
collected from 13 Covid-
19 patients; virus culture
was attempted.		We initiated an ongoing study of
environmental contamination obtaining
surface and air samples in 2 NBU hospital
and 9 NQU residential isolation rooms
housing individuals testing positive for
SARS-CoV-2. Samples were obtained in the
NQU on days 5–9 of occupancy and in the
NBU on day 10		63% of in-room air samples
positive (denominator
unclear)		Cultivation of virus was
not confirmed in these
experiments. Authors
suggest this was due to
the low concentrations
recovered in the
samples.		Concentration of gene copies
present in the recovered
liquid sample (copies/µL):
generally low and highly
variable from sample to
sample ranging from 0 to
1.75 copies/µL; with the
highest concentration
recovered from an air
handling grate in the NBU.		NRAerosol samples were analyzed
by RT-PCR targeting the E gene
of SARS-CoV-2. Partial evidence
of virus replication from one air
sample. In the NBU, for the first
two sampling events performed on
Day 10, the sampler was placed on
the window ledge away from the
patient, and was positive for RNA
(2.42 copies/L of air). On Day 18 in
NBU Room B occupied by Patient
3, one sampler was placed near the
patient and one was placed near
the door greater than 2 meters
from the patient’s bed while the
patient was receiving oxygen (1L)
via nasal cannula. Both samples
were positive by PCR, with the one
closest to the patient indicating
a higher airborne concentration
of RNA (4.07 as compared to 2.48
copies/L of air). Samples taken
outside the rooms in the hallways
were 58% positive . Between 5 and
16 samples were collected from
each room, with a mean of 7.35
samples per room and a mode
of 6 samples per room.*in two of
the samples, cell culture indicated
some evidence for the presence of
replication competent virus
Setti L 2020Outdoor samplingItalyObservational study
of particulate matter
collected in industrial
area of Bergamo over
a continuous 3-week
period		Particulate matter was collected using fiber
filters by using a low-volume gravimetric air
sampler (38.3 l/min for 24 h), compliant with
the reference method EN12341:2014 for
PM10 monitoring. This sampling procedure
allows collection of aerosol and bioaerosol,
by filtering 55 m3 per day, in a wide
dimensional range; an approach considered
suitable for sentinel and surveillance
purposes.		20/34 PM samples positive
for one gene
4/34 positive for 2 genes		Not attempted.Not reported.PM reported particulate matter in defined
conditions of atmospheric stability
and high concentrations of PM10,
Seyyed Mahdi SM2020Hospital Iran Cross-sectional study in
the Covid-19 ICU ward. 		Air and surface sampling; impinger method
was applied for air sampling: at a distance
of 1.5 to 1.8 meters from the ground, the
air of the ICU ward was passed through
a sampling pump with an flow rate of 1.5
l/min into the porous midget impeller-30
ml containing 15 ml of virus transmission
medium (PVTM) for 45 minutes.		6/10 air samplesNot attempted.Highest RNA concentrations
observed at the point
between beds 6 and 7 (3913
copies per ml)		NRHighest RNA concentrations
observed at the point between
beds 6 and 7 (3913 copies per ml).
Most of the reported negative air
samples were from the middle
of the ward, which was further
away from the patients beds.
ten samples taken from different
surfaces of the ward, 4 samples
were positive (40%) and the
highest concentration (8318 copies
per ml) was related to the table
next to bed number 3.
Shen Y 2020Community
including
transport on
buses		ChinaObservational
epidemiology: cohort of
128 individuals.		128 individuals travelled on 1 of 2 buses to
attend a worship event in Eastern China.
Those who rode a bus with air recirculation
and with a patient with COVID-19 had an
increased risk of SARS-CoV-2 infection
compared with those who rode a different
bus.		Not attempted.Not attempted.N/A. N/A. Fomites and droplet transmission
can not reasonably be excluded.
Song Z 2020Public Health
Clinical Center		China Observational
surveillance to evaluate
the risk of viral
transmission in AIIRs
with 115 rooms in three
buildings at the Shanghai
Public Health Clinical
Center, Shanghai, during
the treatment of 334
patients infected with
SARS-CoV-2. 		In patient rooms, an air sampler was placed
on the ground with a distance of about
1.0 m from patient’s bed. In changing
rooms, it was located between air supply
outlet and air exhaust to capture particles
from the unidirectional airflow. In addition,
HEPA filters of air exhaust outlet in AIIRs in
building 2 were collected.		0/7 ICU air samples
0/2 non ICU buildings.		Not attempted.N/A (no air samples positive)N/A. We collected air samples from
15 AIIRs, including 7 ICU-AIIRs
in building 3 and 8 non-ICU
AIIRs in buildings 1 and 2. Two
of the samples were collected
in the ICU-AIIR of building 3
when tracheotomy surgery was
performed. Directional airflow and
strong environmental hygiene
procedures were in place.
None of 290 HCWs was infected
when working in the AIIRs at this
hospital. Additionally, testing of all
surface samples from air exhaust
and HEPA filters failed to detect
any viral RNA
Tan L 2020HospitalChina Observational study of
air and surface samples
collected from isolation
wards and ICU for 15
COVID-19 patients.		Air samples were obtained by placing an air
sampler within 1 m of the patient’s head;
this continuously filtered air at a speed of 5
l/min and trapped small virus particles on
a membrane. After 1 h the membrane was
removed and cut into small pieces to be
stored in VTM prior to further testing. The
air sampler was placed at the same height
as (or slightly lower than) an electronic fan
installed on top of the windows to expel
the air from the wards to the outside. Air
samples were obtained from patient rooms,
the corridor outside the patient rooms, and
in the nearby nursing stations.		1/29
0/17 clean areas
1/12 patient rooms*		Not attempted.Not attempted.NR*Only one sample was positive for
SARS-CoV-2, which was collected
within 10 cm of a female patient
who was undergoing endotracheal
intubation for invasive mechanical
ventilation.
SARS-CoV-2 RNA was not detected
on any of the 36 surgical masks
from 18 patients (14 mild and four
severe/critical), although some of
the patients had worn the same
mask for 24 h.
Most patients were 20 days post
symptom onset, and 10/24 (42%)
tested positive for SARS-CoV-2
by throat swab on the day of
sampling.
Wei L 2020 (a)HospitalChina Sampled the
surroundings and air
of 6 negative-pressure
non-ICU rooms 		In a designated isolation ward occupied
by 13 Covid-19 patients, including 2
asymptomatic patients. Air was sampled
between 10:30 am and 13:00 pm during
the routine medical activities using an air
sampler (FSC-1V; Hongrui, Suzhou, China)
with 0.22-μm-pore-size filter membranes
for 15 min at 100 liters/min. The air sampler
was placed about 0.6 m away from each
patient and 1 m above the floor in each
room. The filter membranes were wiped
by the use of pre moistened sterile swabs
(Copan).		0/6 room air samples Not attempted.N/A (no air samples positive)NR 3/6 of samples from air exhaust
outlets in three rooms were
positive for SARS-CoV-2. It appears
that the patient surroundings
in rooms with a SARS-CoV-2-
positive air exhaust outlet are
usually extensive contaminated
(26.7% to 95.7%). It is possible
that small virus-laden particles
may be displaced by airflows and
deposited on patient surroundings
as suggested previously. 44/112
surface samples tested positive.
Wei L (2020 (b)HospitalChina Observational study in
patient surroundings
and on PPE in a non-ICU
isolation ward		The air from rooms for nine COVID-19
patients with illness or positive PCR > 30
days, before and after nasopharyngeal/
oropharyngeal swabbing and
before and after nebulization treatment. Air sampling
was performed using an air microbiological
sampler (FSC-1V; Hongrui, Suzhou, China)
with 0.22 μm filter membranes on a nutrient
agar plate for 15 min at 100 L/min, which
was placed about 2 m away from patient
and 1.1 m above the ground. Air was also
sampled before and after performing
nebulization treatment for all patients
required (n = 4 on March 4 and n = 2 on
March 12, 2020). After air sampling, the
filters and the surface of agar were wiped
using sterile swabs.		0/34 room air samples Not attempted.N/A (no air samples positive)N/AEnvironmental sampling was
not performed at the early stage
of COVID-19 when viral load in
upper respiratory tract is higher.
SARS-CoV-2 was not detected at
distances > 1 m away from patients
with a SARS-CoV-2-positive swab
(n = 5 for nasopharyngeal and n = 2
for oropharyngeal) when collecting
swabs nor after nebulization for
patients with positive respiratory
samples
Wong JCC 2020Home residenceSingapore Observational study
of environmental
contamination of
SARS-CoV-2 in non 24
healthcare settings and
assessed the efficacy of
cleaning and disinfection
in removing SARS-CoV-2
contamination.		Air samples were collected (n=4) in an
accommodation room (occupied by Case
1) that was thought to be poorly ventilated
and another 2 samples were collected right
outside the room entrance. All samples were
taken after the infected persons vacated the
sites and have been isolated in healthcare
facilities. 		0/6 home residence
samples 		Not attempted.N/A (no air samples positive)N/AHalf of the surface swab and air
samples were taken before the
cleaning and disinfection and the
other half was taken after the
disinfection procedure, performed
by third party commercial
companies
Wong SCY 2020HospitalChina Case report and contact
tracing and testing
outbreak investigation of
a patient in with COVID-
19 who was nursed
prior to Covid diagnosis
in an open cubicle of a
general hospital ward,
Hong Kong.		Samples not collected.Not attempted.Not attempted.N/A N/AFindings suggest that SARS-CoV-2
is not spread by an airborne route.
A total of 71 staff and 49 patients
were identified from contact
tracing, 7 staff and 10 patients
fulfilled the criteria of ‘close
contact’. After 28-day surveillance,
76 tests were performed on 52
contacts and all were negative,
including all patient close contacts
and 6/7 staff close contacts.
The remaining contacts were
asymptomatic throughout the
surveillance period. Evidence
against airborne transmission: no
positive test among close contacts
up to 28 days. The patient could
not wear a surgical mask as she
was on oxygen therapy through a
simple facemask.
Wu S 2020HospitalChina Observational study of
air and surface samples
in hospital including rest
rooms 		Air samples from medical areas were
collected through natural precipitation
according to the Hygienic Standard for
Disinfection in Hospitals.9 All samples were
collected under emergency conditions
around 8:00 AM before routine cleaning and
disinfection 		0/44
0/13 ICU
0/13 Wards
0/18 fever clinic		N/A N/A N/A The positive rates in 200
environmental surface samples in
medical areas (24.83%) was higher
than that in living quarters (3.64%),
with a significant difference (P
< .05).
Yuan XN 2020HospitalChina Observational study of
the contaminated area in
COVID-19 wards		Air samples from the clean area, the buffer
room and the contaminated area in the
COVID-19 wards using a portable bioaerosol
concentrator WA-15. 		0/90 Not attempted.N/A (no air samples positive)N/AThe 38 high-frequency contact
surfaces samples of the
contaminated area and 16
surface samples of medical staff's
protective equipment including
outermost gloves and isolation
clothing were all negative.
Zhang D 2020Outdoor
environment of 3
hospitals		China Air (and wastewater and
soil samples) collected
from the surroundings of
a Covid-19 hospital.		73 air and wastewater samples from the
environment of three hospitals in Wuhan
treating Covid-19 patients. 		3/16 Not attempted.SARS-CoV-2 RNA found in
aerosols ranged from 285 to
1,130 copies/m3.
Inside the adjusting tank of
Hospital 1 and Hospital 2,
respectively, SARS-CoV-2 in
aerosols was found at a level
of 285 copies/m3 and 603
copies/m3.

Aerosols collected 5 m away
from Hospital 1 outpatient
building were 1130 copies/
m3, whereas undetected in
aerosols collected 5 m away
from the inpatient building. 		N/ASARS-CoV-2 RNA found in a
range of samples adjacent to
hospitals. Inside the adjusting
tank of Jinyintan Hospital and
Huoshenshan Hospital, SARS-CoV-
2 in aerosols was found at a level of
285 copies/m3 and 603 copies/m3.
Outside patient departments of
Jinyintan Hospital, SARS-CoV-2
in the aerosols collected 5 m
away from outpatient building
were 1130 copies/m3, whereas
undetected in aerosols collected 5
m away inpatient building.
Zhou J 2020HospitalUKObservational: (air
& surface) samples
collected from a hospital
with a high number of
Covid-19 inpatients.		In the Emergency Department dedicated for
patients with confirmed or suspected COVID-
19, two of the cubicles were occupied and one
patient was in the ambulatory wait area at the
time of sampling. These areas were disinfected
daily using a combined chlorine-based
detergent/disinfectant (Actichlor Plus, Ecolab),
with an additional twice daily disinfection
of high touch surfaces using the same
detergent/disinfectant. In each of these clinical
areas, four air samples were collected (five
air samples were collected in the Emergency
Department, and three in public areas of the
hospital). Air sampling was performed using
a Coriolis μ air sampler (referred to as Coriolis
hereafter) (Bertin Technologies), which collects
air at 100–300 litres per minute (LPM). After
10 min sampling at 100 LPM, a total of 1.0
m3 147 air was sampled into a conical vial
containing 5 mL Dulbecco’s minimal essential
medium (DMEM).		2/31 air samples positive
12/31 suspected 		0/14101 to 103 copies of SARS-
CoV-2 RNA was detected in
all air samples; no significant
difference between sample
areas.		NRWe defined samples where both
of the PCRs performed from an
air or surface sample detected
SARS-CoV-2 RNA as positive, and
samples where one of the two
PCRs performed from an air or
surface sample detected SARS-
CoV-2 RNA as suspected
Zhou L 2020HospitalChina Study of collected
samples of exhaled
breath of patients ready
for discharge and air
samples. 		The 13 patients in 4 hospitals were aged
70+ years. 10 were recovered Covid-19
patients ready for discharge; 3 were patients
recovered from influenza who tested
negative for SARS-CoV-2). Air (& surface)
samples were collected. Exhaled breath
condensate of 300-500 L was collected from
each patient: a long straw was used to allow
the patient to breathe into a tube that was
electrically cooled.
44 air samples were taken, from corridors,
hospital waste storage rooms, ICU rooms (5
samples), toilets, medical preparation rooms,
clinical observation rooms, and general
wards. Two impinger samplers were used:
WA-15 sampled at a flow rate of 15 L/min,
while the WA-400 sampled at 400 L/min.		0/44 Not attempted.N/A (no air samples positive)Not attempted.1.3% of surface swab samples
tested positive.20% of Covid-19
patients, who were ready for
a hospital discharge based on
current guidelines, had SARS-CoV-2
in their exhaled breath (~105 RNA
copies/m3); They were estimated
to emit about 1400 RNA copies
into the air per minute.

Table 2. Study characteristics: reviews.

Study (n=22)Fulfils
systematic
review
methods		Research question (search date up
to)		No. included studies (No.
participants)		Main resultsKey conclusions
Airborne transmission and its prevention (n=14)
Anderson EL 2020noWhat are the scientific uncertainties
and potential importance of aerosol
transmission of SARS‐CoV‐2. (search
methods and date not clear)		unclear Limited evidence reports that SARS-CoV-2 can remain active in
aerosol for at least 3 hours, although its concentration decreases
over time.		Further data collection required assessment under
differing conditions of temperature and humidity.
Such research should be relatively low cost and results
available in a short time.
Agarwal 2020yesTo summarize the evidence for the
efficacy, safety, and risk of aerosol
generation and infection transmission
during high-flow nasal cannula (HFNC)
use among patients with acute
hypoxemic respiratory failure due to
COVID-19 (search conducted to 14
May)		Four studies evaluating
droplet dispersion and
three evaluating aerosol
generation and dispersion. 		Two simulation studies and a crossover study showed mixed findings
regarding the effect of HFNC on droplet dispersion. Two simulation
studies reported no associated increase in aerosol dispersion, and
one reported higher flow rates were associated with increased
regions of aerosol density (evidence rated as very low certainty).		High-flow nasal cannula may reduce the need for
invasive ventilation and escalation of therapy
Bahl P 2020noWe aimed to review the evidence
supporting the rule of 1-meter (≈3
feet) spatial separation for droplet
precautions in the context of guidelines
issued by the WHO, CDC, and European
Centre for Disease Prevention and
Control (ECDC) for HCWs on respiratory
protection for COVID-19. (open search
to March 2020)		Ten papers were included in
the review 		We found that the evidence base for current guidelines is sparse, and
the available data do not support the 1- to 2-meter (≈3–6 feet) rule
of spatial separation. Of 10 studies on horizontal droplet distance, 8
showed droplets travel more than 2 meters (≈6 feet), in some cases
up to 8 meters (≈26 feet). Several studies of severe acute respiratory
syndrome coronavirus 2 (SARS-CoV-2) support aerosol transmission,
and 1 study documented virus at a distance of 4 meters (≈13 feet)
from the patient. 		The weight of combined evidence supports airborne
precautions for the occupational health and safety of
health workers treating patients with COVID-19.
Birgand G 2020 and
Birgand G 2020JAMA		noEvidence for airborne contamination
of SARS-CoV-2 in hospitals (search
conducted to 21 July repeated on
October 27, 2020 for JAMA publication)		17 articles
JAMA Dec: 24 cross-
sectional observational
studies		68/247 (28%) of air sampled from close patients environment were
positive for SARS-CoV-2: no difference according to the setting (ICU:
27/97, 27.8%; non-ICU: 41/150, 27.3%; p=0.93), or the distance from
patients (<1 metre: 1/64, 1.5%; 1 to 5 metres: 4/67, 6%; p=0.4). 3/78
(4%) viral cultures performed in three studies were positive (all were
samples from close to patients). JAMA: A total of 81 viral cultures were
performed across 5 studies, and 7 (8.6%) from 2 studies were positive,
all from close patient environments. 		In hospital, the air near and away from COVID-19
patients is frequently contaminated with SARS CoV-2
RNA, with however, rare proofs of their viability.
JAMA in this systematic review, the air close to
and distant from patients with coronavirus disease
2019 was frequently contaminated with SARS-CoV-
2 RNA; however, few of these samples contained
viable viruses. High viral loads found in toilets and
bathrooms, staff areas, and public hallways suggest
that these areas should be carefully considered.
Carducci A 2020 noTo describe the state of the art of
coronavirus airborne transmission
(search conducted 5 June)		64 papers classified into
three groups: laboratory
experiments (12 papers),
air monitoring (22) and
epidemiological and airflow
model studies (30		Airborne transmission of SARS-CoV-2 was suggested by studies
across the three groups, but methods were not standardised.		No studies had sufficient confirmatory evidence,
and there is only a hypothesis to support airborne
transmission
Chen PZ 2020 yesTo develop a comprehensive dataset
of respiratory viral loads (rVLs) of
SARS-CoV-2, SARS-CoV-1 and influenza
A(H1N1)pdm09 (search conducted to
7 Aug)		64 studies (n = 9,631 total
specimens)		Modelling of the likelihood of respiratory particles containing viable
SARS-CoV-2.
When expelled by the mean COVID-19 case during the infectious
period, respiratory particles showed low likelihoods of carrying viable
SARS-CoV-2. Aerosols (equilibrium aerodynamic diameter [da] ≤
100 µm) were ≤0.69% (95% CI: 0.43-0.95%) likely to contain a virion.
Droplets also had low likelihoods: at a equilibrium aerodynamic
diameter = 330 µm, 		Aerosols (≤100 μm) can be inhaled nasally, whereas
droplets (>100 μm) tend to be excluded. For
direct transmission, droplets must be sprayed
ballistically onto susceptible tissue. Hence, droplets
predominantly deposit on nearby surfaces,
potentiating indirect transmission. Aerosols can
be further categorized based on typical travel
characteristics: short-range aerosols (50–100 μm)
tend to settle within 2 m; long range ones (10–50 μm)
often travel beyond 2 m based on emission force; and
buoyant aerosols (≤10 μm) remain suspended and
travel based on airflow profiles for minutes to many
hours
Comber L 2020 yesTo synthesise the evidence for the
potential airborne transmission of
SARS‐CoV‐2 via aerosols. (Searches 1
Jan up to 27 July 2020).		28 studies (8
epidemiological case series
of SARS‐CoV‐2 clusters or
outbreaks;16 air sampling
studies, and 4 virological
studies).		10/16 air sampling studies detected SARS‐CoV‐2 ribonucleic acid;
however, only three of these studies attempted to culture the virus
with one being successful in a limited number of samples. Two of four
virological studies using artificially generated aerosols indicated that
SARS‐CoV‐2 is viable in aerosols.		The results of this review indicate there is inconclusive
evidence regarding the viability and infectivity of
SARS‐CoV‐2 in aerosols. Epidemiological studies
suggest possible transmission, with contextual factors
noted. However, there is uncertainty as to the nature
and impact of aerosol transmission of SARS‐CoV‐2,
and its relative contribution to the Covid‐19 pandemic
compared with other modes of transmission.
Ekram W 2020no To summarize the ways in which SARS-
CoV-2 is transmitted (Searches Dec 28,
2019 up to July 31 2020)		unclear Evidence-based hypotheses support the possibility of SARS-CoV-2
airborne transmission due to its persistence in aerosol droplets in a
viable and infectious forms.		Aerosolized transmission is likely the dominant
route for the spread of SARS-CoV-2, particularly in
healthcare facilities. Although SARS-CoV-2 has been
detected in non-respiratory specimens, including
stool, blood and breast milk, their role in transmission
remains uncertain.
Ji B 2020 no To reviews the information from
published papers, newsletters and large
number of scientific websites to profile
the transmission characteristics of the
coronaviruses in water, sludge, and air
environment, (search methods and
date not clear)		unclear It appears that the wastewater, sludge, aerosol are
potentially environmental transmission of coronavirus.
Mehraeen E 2020noTo review the current evidence of COVID-
19 transmission modes. (Searches Dec
2019 to April 2020)		36 studies including 31
articles (11 reports, eight
reviews, seven letters to
the editor, two modeling,
one perspective, and two
experimental studies) and
five clinical trials.		Identified five potential transmission modes of COVID-19 including
airborne, droplet, contact with contaminated surfaces, oral and fecal
secretions.		Droplet and contact with contaminated surfaces were
the most frequent transmission modes of COVID-19.
Fecal excretion, environmental contamination, and
fluid pollution might contribute to a viral transmission
Niazi S 2020 noTo evaluate the mechanisms of
generation of human pathogenic
coronaviruses, evaluating these viruses
in the air/field studies and available
evidence about their seasonality
patterns. (searches no restriction on
year up to July 31 2020)		total unclear (8 Studies of
air sampling: 6 Sars-CoV-2)		Evidence exists for respirable-sized airborne droplet nuclei containing
viral RNA, although this does not necessarily imply that the virus
is transmittable, capable of replicating in a recipient host, or that
inoculum is sufficient to initiate infection. However, evidence suggests
that coronaviruses can survive in simulated droplet nuclei for a
significant time (>24 h). Nevertheless, laboratory nebulized virus-
laden aerosols might not accurately model the complexity of human
carrier aerosols in studying airborne viral transport		Human respiratory activities generate respirable
sized aerosols that are of adequate size to support
an infectious virus. Knowledge of the properties of
respiratory aerosols and their effects on the viability
of viruses remains incomplete. Environmental factors
could directly affect the viability of virus on the
embedded viruses in aerosols. There is disagreement
on whether wild coronaviruses can be transmitted
via an airborne path. Further studies are required to
provide supporting evidence for the role of airborne
transmission.
Noorimotlagh Z 2020 noto review studies on airborne
transmission of SARS-CoV-2 in indoor air
environments.(search methods and
date not clear)		14 studies 11 studies were experimental and reported different findings on
positive or negative detection of SARS-CoV-2 airborne transmission
in indoor air. Among them, three studies indicated that all indoor air
samples in the hospital were negative, thus concluding that there
is no evidence that SARS-CoV-2 is transmitted by air (Faridi et al.,
2020; Kim et al., 2020; Masoumbeigi et al., 2020). the other included
experimental studies reported positive results that confirmed
transmission of the virus through the air. 		There is a possibility of airborne transmission of SARS-
CoV-2 in indoor air environments.
Rahmani 2020 noA review of methods used for sampling
and detection of SARS like viruses
in the air. (search methods and date
not clear)		not clear Factors that limit the interpretation included variable patient distance
from the sampler, use of protective or oxygen masks by patients,
patient activities, coughing and sneezing during sampling time, air
movement, air conditioning, sampler type, sampling conditions,
storage and transferring conditions.		Most studies are not able to discriminate between
airborne or respiratory droplet transmission.
Ren SY 2020 NoThis review aims to summarize
data on the persistence of different
coronaviruses on inanimate surfaces.
(search date unclear)		unclear Viruses in respiratory or fecal specimens can maintain infectivity for
quite a long time at room temperature. Absorbent materials like
cotton are safer than unabsorbent materials for protection from virus
infection. The risk of transmission via touching contaminated paper is
low. Preventive strategies such as washing hands and wearing masks
are critical to the control of coronavirus disease 2019.		Viruses in respiratory or fecal specimens can
maintain infectivity for quite a long time at room
temperature. Absorbent materials like cotton are
safer than unabsorbent materials for protection from
virus infection. The risk of transmission via touching
contaminated paper is low.
Singhal S 2020 noTo focus on different modes of
transmission of this virus, comparison of
this virus with previous similar analogy
viral diseases like SARS and MERS
(Searches Jan 1 to 29 April 2020)		unclear
Wilson NM 2020 noTo assess the airborne transmission
of severe acute respiratory syndrome
coronavirus‐2 to healthcare workers
(search methods and date not clear)		unclear Evidence largely from low-quality case and cohort studies where the
exact mode of transmission is unknown as aerosol production was
never quantified. The mechanisms and risk factors for transmission
were also largely unconfirmed. 		Limited evidence suggests aerosol generating
procedures cause an increase in airborne healthcare
worker transmission. Further research is required.
Airborne transmission and procedures (n=3)
Hussain A 2020 noExtent of infectious SARS-CoV-
2 aerosolisation as a result of
oesophagogastroduodenoscopy or
colonoscopy (search conducted up
to 5 June)		26 studies The aerosolisation and infectious extent of SARS-CoV-2 cannot be
accurately measured, and no clinical studies have confirmed aerosol
infection of SARS-CoV-2,
Kay JK 2020 yesWhat is the evidence for minimizing the
use of flexible laryngoscopy during the
coronavirus disease 2019 pandemic? (search conducted upto April 2020)		No studies provided
data for SARS-CoV-2
transmission during flexible
laryngoscopy. 		A paucity of data regarding the risks of SARs-CoV-2 aerosolization and
transmission during endoscopic procedures of the aerodigestive tract		More research is needed.
Schünemann HJyesTo review multiple streams of evidence
regarding the benefits and harms of
ventilation techniques for coronavirus
infections, including that causing COVID-
19 (search conducted up to 1 May).		123 (45 on COVID-19)Evidence suggests an increased risk for transmission of coronaviruses
with invasive procedures. An additional 34 studies in COVID-19
patients were found, by their methods and reporting were too poor
to synthesize data appropriately. 		Direct studies in COVID-19 are limited and poorly
reported.
Ventilation, air conditioning filtration and recirculation (n=3)
Mousavi EH 2020 noWhat is the safety of air filtration and
air recirculation in healthcare premises.
(search methods and date not clear)		109 documents categorized
into five levels		Evidence to support current practice is very scarce. No randomized
trials were retrieved and most experiments were designed to try to
prove airborne transmission as opposed to test the null hypothesis.
Observational evidence and animal studies showed contaminated air
can result in disease spread, and the combination of air filtration and
recirculation can reduce this risk.		There is a need for a rigorous and feasible line of
research in the area of air filtration and recirculation in
healthcare facilities.
Chirico F 2020noWhat is the impact of heating, ventilation and
air conditioning systems (HVAC) on
transmission of coronaviruses (search
conducted 11 July)		Six studies on SARS-CoV-2In three of six studies of SARS-CoV-2, the heating and ventilation
system was suspected to aid transmission; in two studies the data
did not support such an effect, and in one study only modelling
suggested an impact		The differences in HVAC systems prevent
generalization of the results. The few investigations
available do not provide sufficient evidence that SARS-
CoV-2 can be transmitted by HVAC systems.
Correia G 2020noWhat is the impact of HVAC in hospitals
or healthcare facilities on the spread of
the virus. (search methods and date
not clear)		unclearThe authors speculate that incorrect use of HVACs
might contribute to the transmission of the virus.

Reviews

We found 22 reviews on SARS-CoV-2: 16 reviews [Anderson EL 2020, Agarwal 2020, Bahl P 2020, Birgand G 2020, Carducci A 2020, Chen PZ 2020, Comber L 2020, Ekram W 2020, Ji B 2020, Mehraeen E 2020, Niazi S 2020, Noorimotlagh Z 2020, Rahmani 2020, Ren Y 2020, Singhal S 2020, and Wilson NM 2020] were about airborne transmission and prevention; three reviews on airborne transmission and procedures [Hussain A 2020, Kay JK 2020, and Schünemann HJ] and three on ventilation, air conditioning filtration and recirculation [Mousavi EH 2020, Chirico F 2020, and Correia G 2020] (see Table 2). The final search date of these reviews varied from April up to 27 October 2020. Only five reviews met systematic review methods criteria that include systematically searching for all available evidence, appraising the quality of the included studies, and synthesising the evidence into a usable form10.

Quality of included primary studies (n=67)

All included primary studies were observational (some with experimental components) and low quality (see Table 3). We could not identify a published protocol for any of the studies. Most studies were based on convenience sampling. While the description of methods provided sufficient detail to replicate 91% of studies (see Figure 2), the research often lacked standard methods, standard sampling sizes and reporting. In 69% of the studies, the sample sources were clear, however, outcomes that aimed to demonstrate the detection of viable, replicable viruses were lacking. Limitations of the sampling methods and the poor-quality reporting make it difficult to discriminate between airborne or droplet nuclei transmission. Interpretation is further limited by the variability in reporting of patient distance from the sampler, use of protective or oxygen masks by patients, patient activities (coughing and sneezing during sampling time), air movement, air conditioning sampler type, sampling, storage and transfer conditions.

Table 3. Quality of included studies.

StudyIs the source
popn adequately
described 		Description of
methods and
sufficient detail
to replicate		Samples
sources clear
and quantified		Analysis &
reporting
outcomes
appropriate		Was follow up
sufficient
Ahn JY 2020 YesYesNoUnclearNot Applicable
Bays D 2020YesYesNot ApplicableYesYes
Binder 2020YesYesYesYesYes
Charlotte N 2020YesUnclearNot ApplicableUnclearYes
Cheng VCC 2020aYesYesYesYesNot Applicable
Cheng VCC 2020bUnclearYesYesUnclearNot Applicable
Chia PY 2020YesYesYesYesNot Applicable
Chirizzi D 2020Not ApplicableYesYesYesNot Applicable
Declementi M 2020YesYesYesYesNot Applicable
De Man P 2020UnclearYesNot ApplicableUnclearNot Applicable
Di Carlo P 2020Not ApplicableYesYesYesNot Applicable
Ding Z 2020YesYesYesUnclearNot Applicable
Döhla M 2020UnclearYesYesUnclearNot Applicable
Dumont-Leblond 2020YesYesYesYesNot Applicable
Faridi S 2020YesYesYesYesNot Applicable
Feng B 2021YesYesYesYesNot Applicable
Ge XY 2020YesUnclearYesUnclearNot Applicable
Günther T 2020YesYesYesUnclearYes
Guo ZD 2020YesYesYesYesNot Applicable
Hamner 2020 and Miller SL 2020YesYesNot ApplicableUnclearYes
Hernández JL 2020UnclearYesYesYesNot Applicable
Horve PF 2020YesYesYesYesNot Applicable
Hu J 2020YesYesYesUnclearNot Applicable
Jiang Y 2020YesYesUnclearUnclearNot Applicable
Jin T 2020YesYesYesYesNot Applicable
Kang M 2020YesYesUnclearUnclearNot Applicable
Kenarkoohi A 2020YesYesYesUnclearNot Applicable
Kim UJ 2020YesYesYesYesNot Applicable
Kwon KS 2020YesYesNot ApplicableYesYes
Lednicky JA 2020aYesYesYesUnclearNot Applicable
Lednicky JA 2020bYesYesYesUnclearNot Applicable
Lei H 2020YesYesYesYesNot Applicable
Li Y & Qian H 2020YesYesNot ApplicableYesYes
Li YH & Fan YZ 2020YesYesYesYesNot Applicable
Lin G 2020YesYesNot ApplicableYesNot Applicable
Liu Y, Ning Z 2020YesYesYesYesNot Applicable
Lu J 2020YesUnclearNot ApplicableUnclearNot Applicable
Luo K 2020YesYesNot ApplicableYesYes
Ma J 2020YesYesYesYesNot Applicable
Marchetti 2020YesYesUnclearUnclearNot Applicable
Masoumbeigi 2020YesYesYesYesNot Applicable
McGain FYesYesUnclearUnclearNot Applicable
Moreno 2020Not ApplicableYesYesYesNot Applicable
Morioka S 2020YesYesNot ApplicableUnclearNot Applicable
Mponponsuo K 2020YesYesNot ApplicableYesYes
Nakamura K 2020YesYesYesYesNot Applicable
Nissen K 2020YesUnclearYesUnclearNot Applicable
Ogawa Y 2020YesYesYesYesYes
Ong SWX 2020YesYesYesYesNot Applicable
Orenes-Piñero E 2020YesYesNot ApplicableYesNot Applicable
Razzini K 2020YesYesYesYesNot Applicable
Santarpia JL 2020aYesYesYesUnclearNot Applicable
Santarpia JL 2020bYesYesYesNoNot Applicable
Setti L 2020Not ApplicableYesYesYesNot Applicable
Seyyed Mahdi SM
2020		YesYesYesUnclearNot Applicable
Shen Y 2020UnclearYesNot ApplicableNoUnclear
Song Z 2020UnclearYesYesYesNot Applicable
Tan L 2020YesYesYesUnclearNot Applicable
Wei L 2020aYesYesYesYesNot Applicable
Wei L 2020bYesYesYesYesNot Applicable
Wong JCC 2020YesYesUnclearYesNot Applicable
Wong SCY 2020YesYesNot ApplicableYesYes
Wu S 2020YesUnclearYesUnclearNot Applicable
Yuan XN 2020UnclearUnclearUnclearUnclearNot Applicable
Zhang D 2020YesUnclearYesUnclearNot Applicable
Zhou J 2020YesYesYesYesNot Applicable
Zhou L 2020YesYesYesYesNot Applicable
Total5660463911
6767676767
83.6%89.6%68.7%58.2%16.4%
c6ec3de6-4882-4d44-ae41-fa814d87b0d1_figure2.gif

Figure 2. Risk of bias (n=67).

Primary studies

We included 67 primary studies, of which 53 (79%) reported binary data on RT-PCR air samples (see Table 1). All were descriptive observational and none were comparative. Twelve studies reported Ct values and 18 report copies per sample volume (see Table 4). Two studies reported a Ct value < 25: Razzini K 2020 et al. reports in the intensive care unit the mean Ct was 22.6, and Guo ZD 2020 et al. report a Ct of 12.5 near the doctor's office area. Ten studies report Ct values > 35; two [Guo ZD 2020, Lei H 2020] report Ct > 40, and three studies [Dumont-Leblond 2020, Kenarkoohi 2020, Nissen 2020] report the detection of single genes.

Table 4. Concentrations of PCR samples recovered (n=25).

Study (n=64)Cycle Threshold (Ct)Copies per m³ (or L)
Binder 2020Sample at 1.4m, <4uM: 1st 36.6; 2nd 37.1
Sample at 2.2m, <4uM: 1st 37.4, 2nd 39.9
Sample at 2.2m, >4uM: 1st 39.1, 2nd 39.6
Chia PY 2020range 1.84 × 10³ to 3.38 × 10³ RNA copies per m³
Chirizzi D 2020<0.8 copies m ³ for each size range.
Ding Z 2020RNA copies for weakly positive sample not
calculated.
Dumont-Leblond N 2020N gene (range 36.5 to 39.8) mean 38.0
ORF1b gene (32.1 to 35.2) mean 33.7		8 positives for both N and Orf1b (range 9.9 to 514.2)
mean 201.6 genomes /m³
Feng B 2020<1 μm: 1,111 copies/m³
>4 μm: 744 copies/m³
Ge XY 2020ICU: Ct 36.5 - 37.8
Guo ZD 2020Indoor air near air outlet: Ct 35.7,
Near patients: Ct 44.4.
Near the doctor’s office area: Ct 12.5		Indoor air near the air outlet: 3.8/L
near the patients: 1.4/L
near the doctor’s office area: 0.52
Horve PF 2020The highest abundance sample (~245 gene copies)
found on the pre-filters,
Hu J 2020range 1.11 × 10³ to 1.12 × 104 copies m³
In 10% of outdoor air samples, 10 m from the doors
of inpatient & outpatient buildings range 0.89 to
1.65×10³ copies m³
Kenarkoohi A 2020Ct around 38 for ORF1ab
Ct around 35 for n gene
Lednicky JA 2020aCt 36.0, 37.7, 37.4, 38.7, respectively (mean
Cq 37.5)		Four positives contain: 2.82E+03, 9.12E+02,
1.15E+03, 4.68E+02 genome equivalents/25 μL,
Lednicky JA 2020bCt 39.10.87 virus genome equivalents L -1
Lei H 2020Near the head of the patient Ct 41.25.
Liu Y & Ning Z 2020ICU: rang- 0 -113 copies m³
Patient areas 0 -19 copies m³
Medical Staff Areas 0 - 42m³
Public areas: 0 -11copies m³
Ma J 2020Exhaled Breath Samples, 14 positives: Ct
35.5 ± 3.2		Breath emission rate estimate: 1.03 × 10 ⁵ to
2.25 × 10 ⁷ viruses per hour. Air sample estimate
6.1 × 10 3 viruses/m³
Moreno T 2020genome count range 14 to 446/m2 for IP2, 9 to
490/m2 for IP4 and 5 to 378/m2 for E.
Subway: 1st sample estimate 23.4 GC/m³, 2nd
amplified target gene IP2 (18.8 GC/m³) & protein E
(5.6 GC/m³).
Nissen K 2020Ct N gene: 35.3
Ct E gene 33.2
Ward 1 specimen Ct 33.0 for E gene only.
Orenes-Piñero E 2020Ct from surfaces > 10 cycles of those
obtained from the patient, indicating viral
load was lower in the room environment.
Razzini K 2020ICU: Mean Ct 22.6
Corridor: Mean Ct 31.1
Santarpia JL 2020aconcentrations up to around 7.5 TCID 50 / m3 of air.
Santarpia JL 2020bgene copies generally low and highly variable from
sample to sample ranging from 0 to 1.75 copies/µL
Seyyed Mahdi SM 2020Highest RNA concentrations observed between
beds 6 and 7 (3,913 copies per ml)
Zhang D 2020Range 285 to 1,130 copies/m3.
Inside adjusting tank 285 copies/m3 and 603
copies/m3.
5 m from Hospital outpatient building 1,130 copies/
m3,
5 m from the inpatient building undetected
Zhou J 2020101 to 103 copies of SARS-CoV-2 RNA in all air
samples; no significant difference between sample
areas.

Table 5 shows eight studies reporting the size of detectable particles containing RNA [Binder 2020, Chia PY 2020, Chirizzi D 2020, Feng B 2020, Hernández JL 2020, Liu Y & Ning Z 2020, McGain F 2020, and Santarpia 2020a]. Overall the reporting was heterogeneous. SARS-CoV-2 RNA was detectable in a range of air sample sizes from <1 μm through to >18 µm. Seven studies detected particles below <4 μm, and Chirizzi D 2020 et al. reported on coarse particles up to diameter > 18 µm. In one study, different samplers detected different size particles: McGain F 2020 et al. reported that the APS detected larger aerosols (> 0.37 µm) and MiniWRAS smaller particles (0.01–0.35 µm) (see Figure 3).

Table 5. The size of air particles in the sample (n=8).

Study (n=64)Samples SourceSize of air particles
Binder 20208 National Institute for Occupational Safety and
Health (NIOSH) BC 251 Aerosol Samplers (Figure S3)
were placed 1.5m from the ground, at ~1 meter, ~1.4
meters, ~2.2 meters, and ~3.2 meters from the SARS-CoV-2 patient’s head and subsequently run for
~4 hours. 195 air samples were collected		detected in aerosols particle size <4 µm
Chia PY 2020Air sampling was performed in three of the 27
airborne infection isolation rooms (AIIRs). Bioaerosol
samplers used to collect air samples, set at a flow-rate
of 3.5 L/min and run for four hours, collecting a total
of 5,040 L of air from each patient’s room.		positive particles of sizes >4 µm and 1–4 µm
detected in two rooms
Chirizzi D 2020The genetic material of SARS-CoV-2 (RNA) was
determined, using both real-time RT-PCR and ddPCR,
in air samples collected using PM10 samplers and
cascade impactors able to separate 12 size ranges
from nanoparticles (diameter D < 0.056 µm) up to
coarse particles (D > 18 µm).		(D < 0.056 µm) up to coarse particles (D > 18 µm)
Feng B 2020For a sampling of isolation room air, a NIOSH sampler
was placed on a tripod 1.2 m in height and 0.2 m away
from the bed at the side of the patient’s head. The
sampling duration was 30 min, and a total of 105-L
room air was sampled. (9 Exhaled Breath (EB) samples,
8 Exhaled Breath Condensate (EBC) samples, 12
bedside air samples)		RNA detected in the air sample in <1 μm and >4 μm
fractions,
Hernández JL 2020Air sampled in three areas: Emergency area (Clinic
A), Internal medicine (Clinic A), COVID 19 patient area
(Clinic A), and COVID-19 patients care room (Clinic
B). Sampling in all areas was accomplished in 3 h.
Filters of 25 mm diameter with 0.22 μm pores were
utilized (Millipore, AAWP02500), placed in a sterilized
filter holder (Millipore, SWINNX) coupled to a vacuum
system through a previously disinfected plastic hose,
filtering the air with a flow of 9.6 L/min in each filter
holder.		filtration through 0.22 μm pores.
Liu Y & Ning Z 2020Over a 2 week period: 30 aerosol samples of total
suspended particles collected on 25-mm-diameter
filters loaded into styrene filter cassettes (SKC) by
sampling air at a fixed flow rate of 5.0 l min−1 using a
portable pump (APEX2, Casella). Three size-segregated
aerosol samples collected using a miniature cascade
impactor (Sioutas Impactor, SKC) that separated
aerosols into five ranges (>2.5 μm, 1.0 to 2.5 μm,
0.50 to 1.0 μm and 0.25 to 0.50 μm on 25-mm filter
substrates, and 0 to 0.25 μm on 37-mm filters) at
a flow rate of 9.0 l min−1. Two aerosol deposition
samples collected using 80-mm-diameter filters
packed into a holder with an effective deposition area
of 43.0 cm2; filters were placed intact on the floor in
two corners of an ICU for 7 days.		SARS-CoV-2 aerosols one in the submicrometre
region (dp between 0.25 and 1.0 μm) and the other
in supermicrometre region (dp > 2.5 μm). Aerosols
in the submicrometre region were found with peak
concentrations of 40 and 9 copies m3 in the 0.25–0.5
μm and 0.5–1.0 μm range, respectively.
McGain F 2020Two spectrometers to measure aerosol particles:
the portable Mini Wide Range Aerosol Sizer 1371
(MiniWRAS) and the Aerodynamic Particle Sizer (APS).
During the procedure, the aerosol detector inlet was
positioned 30 cm directly above the patient’s neck,
representing the surgeon’s breathing air space		APS detected larger aerosols (> 0.37 mm) and
MiniWRAS smaller particles (0.01–0.35 mm).
Santarpia JL 2020aAir samplers were placed in various places in the
vicinity of the patient, including over 2m distant.
Personal air sampling devices were worn by
study personnel on two days during sampling.
Measurements were made to characterize the size
distribution of aerosol particles, and size-fractionated,
aerosol samples were collected to assess the
presence of infectious virus in particles sizes of >4.1
µm, 1-4 µm, and <1 µm in the patient environment.
An Aerodynamic Particle Sizer Spectrometer was
used to measure aerosol concentrations and size
distributions from 0.542 µm up to 20 µm. A NIOSH
BC251 sampler18 was used to provide size segregated
aerosol samples for both rRT-PCR and culture analysis.		Two of the 1-4 µm samples demonstrated viral
growth, between 90% and 95% confidence
c6ec3de6-4882-4d44-ae41-fa814d87b0d1_figure3.gif

Figure 3. The relative size of particles.

We found 36 different descriptions of air samplers deployed: the two most used samplers were the MD8 sampler, Sartorius, Goettingen, Germany (n=7 studies) and the National Institute for Occupational Safety and Health (NIOSH) BC 251 Aerosol sampler (n=6 studies) (see Extended data: Appendix 47). One study used four different methods [Ding Z 2020], and in seven studies the sampler used was unclear [Hernández JL 2020, Horve PF 2020, Kang M 2020, Kwon KS 2020, Seyyed Mahdi SM 2020, Tan L 2020 and Zhang D 2020].

Hospital. There were 50 studies conducted in healthcare settings: 45 studies included binary RT-PCR air samples (42 hospitals, 2 outdoors and 1 student healthcare centre).

Of the 42 studies that reported air sampling RT-PCR data within a hospital environment, 24 (57%) reported positive samples (142 positives out of 1,403 samples: average 10.1%). Samples taken per study varied from 2 to 135. In two studies [Ahn 2020 and Santarpia JL 2020b] the denominator was unclear. There was no pattern observed in terms of the type of hospital setting (ICU versus non-ICU) and RT-PCR positivity. Three studies involving ICUs reported 0% of samples were positive [Ma J, Song Z, Wu S] (see Figure 4).

c6ec3de6-4882-4d44-ae41-fa814d87b0d1_figure4.gif

Figure 4. Percentage hospital air samples positive for SARs-CoV-2 RNA (n=42).

Red bars indicate studies sampling ICUs.

Two studies conducted in hospitals also sampled other spaces. Liu Y & Ning Z et al. reported 4/13 public areas were RT-PCR positive; Ma J et al. reported 1 positive sample from an unventilated quarantine hotel toilet room out of 26 samples taken. Zhang D et al. sampled the outdoor environment of three hospitals and reported 3/16 samples were RT-PCR positive. Lednicky JA 2020b sampled in a respiratory infection evaluation area of a student health care center and reported one positive sample with a CT of 39 (virus genome equivalent of 0.87 virus genomes L–1 air).

Two studies reported on Exhaled Breath Condensate (EBC). Ma J et al. reported 14/52 EBC samples as RT-PCR positive and Feng B et al. reported 2/8 positive EBC samples. Five studies conducted in hospitals did not attempt RT-PCR air sampling [Bays D 2020; McGain F 2020; Mponponsuo K 2020 Ogawa Y 2020 and Wong SCY 2020] In Lei H et al., it was not possible to separate air from surface sample results.

Outdoors and community. Seventeen studies reported on the outdoors and in the community (see Figure 1). These settings were buses (four studies: two in china [Luo K 2020 and Shen Y 2020]; one in Italy [Di Carlo P 2020] and one from Spain that included subway trains [Moreno T 2020]); two studies each for the outdoors; restaurant; choir practice & block of flats, and one study each for a meat processing plant; home residence; quarantine hotel; quarantined household and a care home.

Seven of these studies undertook RT-PCR sampling [Di Carlo P 2020: inside a bus; Dohla M 2020: quarantined households; Kang M 2020: a block of flats; Kwon KS 2020: the community; Moreno T 2020; buses and subway trains; Setti L 2020: outdoor sampling; and Wong JCC 2020: in the home residence], and one Chirizzi D 2020 sampled atmospheric concentrations.

Of the eight studies, two reported positive RT-PCR samples (5 of 125 samples positive for 2 or more genes, average 4.0%), and one Chirizzi 2020 et al. found outdoor atmospheric concentrations of SARS-CoV-2 RNA at low levels <0.8 copies m3. Moreno 2020 et al. sampled on buses and subway trains in Barcelona, and reported samples were mainly positivity for only 1 of the 3 RNA targets, and Setti et al., in a study of outdoor sampling, reported 20/34 (59%) Particulate Matter (PM) samples were RNA positive for one gene, and 4/34 (11.8%) were positive for two genes (see Table 1). Five studies found no positive samples [Di Carlo P 2020: Dohla M 2020; Kang M 2020, Kwon KS 2020 and Wong JCC 2020].

Three studies reported on two choir practices and potential air transmission. Charlotte N et al. followed-up a choir practice in France with 27 participants who attended a choir practice on 12 March 2020. Two separate publications [Hamner L 2020 and Miller SL 2020] published on the same Choir Practice Skagit County, Washington, USA. In total, 78 members attended two practices: 87% of choir members subsequently became ill (32 confirmed cases and 20 probable secondary cases).

Viral culture. Ten studies attempted viral culture [Binder 2020, Dohla M 2020, Dumont-Leblond N 2020, Hu J 2020, Lednicky JA 2020a, Lednicky JA 2020b, Nissen K 2020, Santarpia JL 2020a, Santarpia JL 2020b, Zhou J 2020]. In seven of the ten studies, the infectious virus could not be isolated and cytopathic effects could not be observed [Binder 2020, Dohla M 2020, Dumont-Leblond N 2020, Hu J 2020, Nissen K 2020, Santarpia JL 2020b and Zhou J 2020] (see Table 6).

Table 6. Viral culture methodological issues.

StudyMethodological
Binder 2020 This study separated particles by three sizes: >4 µm, 1–4 µm, and <1 µm and used multiple sampling sites
which is a robust sampling methodology. The median day’s post symptom was reported as 10 with a range
of 1 to 34 days, and only one patient had a cycle threshold for the N gene < 20. This limits the finding of any
cultivatable virus and the conclusions.
Hu J All positive masks were subject to cell culture and inoculated with Vero-E6 cells after blind passage for three
generations which is a robust approach. One mask from a critically ill patient was positive for the virus but
no details on which passage and at what quantitative burden. The masks could have been contaminated by
saliva or nasal secretions and the conclusion stated that masks blocked the release of viable virus in the air
exhaled from the patient cannot be confirmed.
Lednicky 2020ait is not clear why plaque assays could not be performed due to a nationwide non-availability of some critical
media components in the US. Three serial 3-hr air samplings were performed. Over the 9 hours, it is likely
patients would have moved about and may have been in close proximity to the samplers. The method does
not mention particle sizing for the sampler (ie < or > 5 microns) and the sampled particles could be any size
and hence it is difficult to state they were true aerosols. No data are provided about health workers who
may have been in the room and might have handled the air samplers. Samples were not done at 0.5 m to 1
metre to see if there was a gradient effect. It was noted it took 6 to 11 days post-inoculation before rounding
of the cells with material collected by air sampler and there is no report of a serial subculture of the positive
air samples to demonstrate propagation of a healthy and propagating virus. Nothings is presented about
testing the air sampling isolates in susceptible animal models.
Santarpia JL 2020a
and b		For Santapria 2020 (a) we could only find a preprint publication. A large number of samples were collected.
Serial PCR of cell culture supernatant was unclear and incongruent with the statement that some
increase in viral RNA may have occurred. Increased viral RNA presence is a surrogate and subject to many
interpretations and should not be considered equal to the cultivation of replication and infection competent
virus on cell culture which was not identified. Western blot assay was not done in cell supernatant samples
with non-statistically significant evidence of replication, which would have acted as a control to ensure the
findings were not spurious. Western blots are very weak, with no positive control or size markers and the
signal doesn't necessarily come from a replicating virus, there's no "before culture" analysis.
The presence of virus-like particles on TEM is not proof that these are replicating viruses or necessarily even
SAR-CoV-2. No comparisons to control TEM photomicrographs of the live virus from fresh Vero cells are
presented to discuss.
No size-fractionation techniques were used to determine the size range of SARS-CoV-2 droplets and
particles, raising major issues with the statement the data suggests that viral aerosol particles are produced
by individuals that have the COVID-19.
No information is provided about activity by either patients or the doffing by health workers which may have
contributed to hallway air samples being PCR positive. The contamination identified may have accumulated
over the extended periods of occupancy and may represent the high frequency of reported PCR positive
sites, Floor samples were most heavily reported which supports this finding. The numbers don't match up, Ct
values were converted to pseudo TCID50 values based on an equation that obscures what Cts were actually
recorded. Reporting 100% or 200% increases in RNA levels is actually only 2–3 fold, and not the way viruses
replicate (i.e. exponentially).
No plaques were reported to have been detected and no serial passage on subculture was reported.
Statistical inferences are very difficult to interpret in Figure 1 based on the error bars. The broad sweeping
conclusions that SARS-CoV-2 RNA exists in respired aerosols less than 5 µm in diameter; that aerosols
containing SARS-CoV-2 RNA exist in particle modes that are produced during respiration is difficult to justify
based on the findings presented.
In Santarpia 2020 (b)There are “six patients in five rooms in two wards on three separate days in April of
2020” reported in the text. Table S1 reports are 6 rooms (2 are 7A and 7B and 4 are 5A-D). The abstract
reports SARS-CoV-2 RNA was detected in all six rooms – It is therefore not clear whether there are 6 rooms
or 5 – One room had 2 patients so the total could be 7 not 6 patients
There is no information in the patients and sampling is done 2–24 days post 1st covid test and looks like
4 were sampled less than 3 days post first covid test but there is no information of symptom onset. No ct
values were provided on the testing of the pts when first done. A Ct of 45 for E gene is not considered a
usual standard and much higher than what most labs use and accept and a lot of background “noise” as a
result
It is likely an equation as used to calculate the concentration of the virus, however, it is more robust to
measure the virus directly than use an equation. EM also does not confirm live virus and does not indicate
active viral replication as the authors suggest – where are the comparisons control EM photomicrographs.
Zhou J 2020No indication any particle size-fractionation techniques were used to determine the size range of droplets
and particle differentiation in air sampling. No information on patients is provided and it is possible they
were in the later stages of illness when no virus could be reliably cultivated. All surface and air samples from
the hospital environment had a Ct value >30, in a range where it is extremely difficult to cultivate the virus.
No attempt was made to ensure the sampler was placed at a specific distance from the individuals.
(Wang W, Xu Y 2020
and (Xiao F, Sun J
2020)		Electron microscopy alone does not proof of an infectious virus. Inactivated particles would look the same,
and images weren’t provided in these studies.

Of the remaining three studies, Lednicky JA 2020b reported that general virus-induced cytopathic effects were observed within two days post-inoculation. The amount of virus present in 390 L of sampled air was low (approximately 340 virus genome equivalents). RT-PCR for SARS-CoV-2 RNA from the cell culture were negative, and three other respiratory viruses were identified: Influenza A H1N1, Influenza A H3N2, and human coronavirus OC43.

Lednicky JA 2020a observed presumed virus-induced CPE for 4/4 RNA-positive hospital air samples. The authors report that plaque assays could not be performed due to a nationwide non-availability of some critical media components in the USA. They also report that it took 6 to 11 days post-inoculation before rounding of the cells was observed with material collected by the air sampler and there is no report of a serial subculture of the positive air samples to demonstrate propagation of a complete replicating virus.

Santarpia JL 2020a reported 3/39 aerosol samples (particle size <1 μm) that cell culture resulted in increased viral RNA at very low levels. An intact virus was observed via transmission electron microscopy in the submicron sample from one room. This study was published as a preprint (checked 5 March 2021) and is subject to methodological criticisms. Serial RT-PCR of cell culture supernatant was unclear and incongruent with the statement that some increase in viral RNA may have occurred. No size-fractionation techniques were used to determine the size range of SARS-CoV-2 droplets and particles. (Table 7 sets out several methodological issues relating to viral culture).

Table 7. Live culture results (n=10).

Study
(n=64)		SettingMethodAir Samples
positive n/d for
SARs-CoV-2 RNA		Live cultureNotes
Binder 2020HospitalAn observational case
series of 20 patients
hospitalized with
coronavirus disease		3/195 samples
from 3 patients		0/3 viable virus
Dohla M 2020Quarantined
households		An observational
study of 43 adults
and 15 children living
in 21 households;
air (also surface and
wastewater) samples
taken.		0/15The infectious virus
could not be isolated
in Vero E6 cells from
any environmental
sample.		26 of all 43 tested adults
were positive by RT-PCR.
10 of 66 wastewater
samples and 4/119 surface
swab samples were
positive for SARS-CoV-2
Dumont-Leblond N 2020HospitalAn observational
study in acute care
hospital rooms over
the course of nearly
two months		11/100 from 6
patient rooms		Viral cultures were
negative
Hu J 2020HospitalAn observational
study: indoor and
outdoor air samples
in ICUs and CT rooms		aerosol samples
8/38 from ICUs
1/6 from CT rooms
samples from
medical staff
rest areas and
corridors were
all negative
(denominator not
clear)		All positive aerosol
samples were
negative after three
passages of Vero-E6
cells inoculated in a
blind test.		All positive masks were
subjected to cell culture
and inoculated with Vero-
E6 cells after blind passage
for three generations. One
mask from a critically ill
patient detected positive.
Lednicky JA 2020aHospitalObservational: air
samples collected,
and virus culture
attempted		4/4 air samples
without a HEPA
filter
0/2 samples using
a HEPA filter		Virus-induced
CPEwas observed for
4/4 RNA-positive air
samples.		No other respiratory
virus was identified in the
samples using a BioFire
FilmArray Respiratory
2 Panel. The amount of
airborne virus detected
per litre of air was small.
Plaque assays could not
be performed due to a
nationwide nonavailability
of some critical media
components (due to
COVID-19 pandemic-
related temporary
lockdown of production
facilities), so TCID50
assays were performed in
Vero E6 cells to estimate
the percentage of the
collected virus particles
that were viable. Estimates
ranged from 2 to 74
TCID50 units/L of air
Lednicky JA 2020bStudent
Healthcare
centre		Observational, air
samples collected,
and virus culture
attempted		1/2 air samplesGeneral virus-
induced cytopathic
effects were
observed within two
days post-inoculation		Estimated concentration
of 0.87 virus genomes
L–1 air. The amount of
virus present in 390 L
of sampled air was low
(approximately 340 virus
genome equivalents).
PCR tests for SARS-CoV-2
vRNA from cell culture
were negative. Three
respiratory viruses were
identified using the Biofire
RVP: Influenza A H1N1,
Influenza A H3N2, and
Human coronavirus OC43
Nissen K 2020HospitalObservational: surface
swabs and fluid
samples collected,
and experimental:
virus culture was
attempted.		7/19 filter were
positive
11 days later, 4/19
were positive for
both genes.		No significant CPE
was seen after three
passages on Vero E6
cells from samples
retrieved from ward
vent openings or
central ventilation
ducts or filters		Cycle threshold (Ct) values
varied between 35.3
and 39.8 for the N and E
gene. Virus culture was
attempted: RNA detected
in sequential passages but
CPE not observed.
Santarpia JL 2020aHospitalObservational: size-
fractionated aerosol
samples collected;
experimental:
virus culture was
attempted.		6/6 patient
rooms.		In 3 aerosol samples
size <1 μm, cell
culture resulted in
increased viral RNA.
Viral replication
of aerosol was
observed in the 1
to 4 μm size but did
not reach statistical
significance.		The presence of SARS-
CoV-2 was observed via
western blot for all but one
of the samples (<1 um,
with statistically significant
evidence of replication, by
rRT-PCR. The intact virus
was observed via TEM in
the submicron sample
from Room.
Santarpia JL 2020bHealthcare
centre		Observational: high-
volume (50 Lpm) and
low-volume (4 Lpm)
personal air samples
(& surface samples)
collected from 13
Covid-19 patients;
experimental:
virus culture was
attempted.		63% of in-room
air samples
positive
(denominator
unclear)		Due to the low
concentrations
recovered in the
samples cultivation
of the virus was not
confirmed in these
experiments. *		. Partial evidence of virus
replication from one air
sample. In the NBU, for
the first two sampling
events performed on
Day 10, the sampler was
placed on the window
ledge away from the
patients and was positive
for RNA (2.42 copies/L of
air). On Day 18 in NBU
Room B occupied by
Patient 3, one sampler was
placed near the patient
and one was placed near
the door greater than 2
meters from the patient’s
bed while the patient
was receiving oxygen (1L)
via nasal cannula. Both
samples were positive by
PCR, with the one closest
to the patient indicating
a higher airborne
concentration of RNA
(4.07 as compared to 2.48
copies/L of air).
Zhou J 2020HospitalObservational: (air
& surface) samples
collected from a
hospital with a high
number of Covid-19
inpatients.		2/31 air samples
positive
12/31 suspected		0/14We defined samples,
where both of the PCRs
performed from an air or
surface sample, detected
SARS-CoV-2 RNA as
positive, and samples
where one of the two PCRs
performed from an air or
surface sample detected
SARS-CoV-2 RNA as
suspected

Discussion

We identified 67 primary studies, all were observational and low quality. The results show that RT-PCR RNA can be detected sporadically in airborne samples in a variety of settings. About half the studies did not detect RNA positivity. Some of the reasons for this may be methodological weaknesses in the study design, the lack of validated methods and the location and variable distance of the sampling. There was no clear relationship between the type of setting and positivity of sampling or detectable viral RNA concentrations. The reporting of viral RNA concentrations was heterogeneous as were the sampling methods.

Past attempts to detect infectious particles have proved difficult: aerosols are dilute and culturing fine particles is problematic. In a NEJM editorial, Roy et al., report ‘the only clear proof that any communicable disease is transmitted by aerosol came from the famous experiment by Wells, Riley, and Mills in the 1950s, which required years of continual exposure of a large colony of guinea pigs to a clinical ward filled with patients who had active tuberculosis11.’ A 2019 review reported that viral RNA or DNA, depending on the virus, could be found in the air near patients with influenza, respiratory syncytial virus, adenovirus, rhinovirus, and other coronaviruses but rarely reported viable viruses12. For coronaviruses, previous evidence supporting the airborne route of transmission is weak13.

Several studies included in our systematic review and reported in the tables, do not support the airborne transmission hypothesis. An included US study performed active case finding from two index patients and 421 exposed HCWs [Bays D 2020]. Eight secondary infections in HCWs were reported, but despite multiple aerosol-generating procedures, there was no evidence of airborne transmission. No transmission events were found in multiple high-risk exposures from five symptomatic COVID-19 health care workers [Mponponsuo K 2020]; Wong SCY et al. reported none of 120 contacts of a patient with initially undetected Covid-19 subsequently became infectious, and Kim UJ et al. reported that all 52 air samples were negative for SARS-CoV-2 RNA.

Strengths and limitations

There is a current lack of well-conducted studies addressing airborne transmission: only nine studies identified during the search period reported air sampling outdoors and, in the environment, outside of hospitals. The findings of our review are limited by the low-quality included studies that lack standardised methods, reporting and outcomes. The small sample sizes, the absence of study protocols and the lack of replication further undermine the findings. Sporadic isolation of viral RNA may be due to problems with sampling techniques. Lack of quality is noted across several of the airborne reviews. Furthermore, while our search was comprehensive, it is likely there are studies that we have missed. Our continual updating and scoping of the literature mean we intend to update this review as more studies and evidence become available.

Evidence from the referenced systematic reviews noted the need to improve the quality of evidence. Anderson et al. reported the need for further data collection under differing conditions of temperature and humidity14. Carducci et al. considered no studies had sufficient confirmatory evidence, and only a hypothesis supports airborne transmission15, Schünemann et al. noted direct studies in COVID-19 are limited and poorly reported16, and Mousavi et al. noted the need for rigorous and feasible lines of research in the area of air filtration and recirculation in healthcare facilities17.

Future studies are warranted to verify findings (particularly including viral culture) before conclusions can be reached about a mode of transmission and important knowledge such as infectious dose. Because of the heterogeneity of the settings, the case-mix limitations, the sampling techniques used clear descriptions and variable study protocols, it is difficult to make meaningful comparisons of air sampling positivity or viral concentrations between settings. Many factors including relative humidity, temperature, aerosolization medium, exposure period, the chemical composition of the air, seasonality, sampling methods, and ultraviolet light exposure can affect the potential infectivity of airborne viruses. While sampling techniques have improved greatly over time, the lack of standardization requires addressing as it limits the development of general recommendations for the sampling of airborne viruses18.

One essential question is whether observed epidemiologic associations are causal19,20. Establishing transmission modes requires integrated epidemiological and mechanistic approaches to narrow uncertainty21. Transmission evidence should be context-specific to particular settings (i.e., indoor or outdoor), environment-specific (i.e., the presence of UV light. ventilation etc.) and ensure that exposure an infectious agent has taken place. Identifying those circumstances that promote transmission using all types of relevant evidence that are more likely to promote viral transmission, and therefore, more amenable to intervention.

Methodological issues of the culture methods used, as well as knowledge of the infectiousness of the patient hinder interpretation and suggest that the results should be interpreted with caution. The detection of SARS-CoV-2 RNA in the air cannot presume transmission, since only viable virions can cause disease. No airborne study to date definitively demonstrates SARS-CoV-2 is of an infectious nature, which offers the most robust evidence of transmissibility22. CPE alone cannot be relied upon to establish SARS-CoV-2 replication and additional methods are required, including demonstration of viral growth on permissive cell lines, immunofluorescence staining, and confirmed the exclusion of other pathogens or contaminants with sequence confirmation. General virus-induced cytopathic effects were observed in one study, however, RT-PCR tests for SARS-CoV-2 were negative while three other respiratory viruses were identified23.

Conclusion

SARS-COV-2 RNA can be detected intermittently by RT-PCR in the air in a variety of settings. A number of studies that looked for viral RNA in air samples found none, even in settings where surfaces were found to be contaminated with SARS-CoV-2 RNA. The lack of recoverable viral culture samples of SARS-CoV-2 prevents firm conclusions to be drawn about airborne transmission. The current evidence is low quality, and there is an urgent need to standardise methods and improve reporting.

Data availability

Underlying data

All data underlying the results are available as part of the article and no additional source data are required.

Extended data

Figshare: SARS-CoV-2 and the Role of Airborne Transmission: Systematic review, https://doi.org/10.6084/m9.figshare.14248055.v27.

This project contains the following extended data:

  • - Appendix 1: Updated protocol

  • - Appendix 2: Search strategy

  • - Appendix 3: References of included studies

  • - Appendix 4: Sampling methods

Reporting guidelines

Figshare: PRISMA checklist for ‘SARS-CoV-2 and the role of airborne transmission: a systematic review’, https://doi.org/10.6084/m9.figshare.14248055.v27.

Data are available under the terms of the Creative Commons Attribution 4.0 International license (CC-BY 4.0).

Acknowledgements

This work was commissioned and paid for by the World Health Organization (WHO). Copyright on the original work on which this article is based belongs to WHO. The authors have been given permission to publish this article. The author(s) alone is/are responsible for the views expressed in the publication. They do not necessarily represent views, decisions, or policies of the World Health Organization.

References

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    Raymond Tellier, McGill University, Montreal, Canada
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    Regarding the review in Heneghan et al. of Lednicky 2020a [1], which reported successful isolation in cell culture of SARS-CoV-2 from aerosol samples: Heneghan et al. take issues with the ... Continue reading
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    Jose-Luis Jimenez, University of Colorado-Boulder, USA
    14 May 2021
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Heneghan CJ, Spencer EA, Brassey J et al. SARS-CoV-2 and the role of airborne transmission: a systematic review [version 1; peer review: 1 approved with reservations, 2 not approved] F1000Research 2021, 10:232 (https://doi.org/10.12688/f1000research.52091.1)
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Maosheng Yao, College of Environmental Sciences and Engineering, Peking University, Beijing, China 
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Discussion is closed on this version, please comment on the latest version above.
  • Reader Comment 19 May 2021
    Raymond Tellier, McGill University, Montreal, Canada
    19 May 2021
    Reader Comment
    Regarding the review in Heneghan et al. of Lednicky 2020a [1], which reported successful isolation in cell culture of SARS-CoV-2 from aerosol samples: Heneghan et al. take issues with the ... Continue reading
    Report a concern
  • Reader Comment 14 May 2021
    Jose-Luis Jimenez, University of Colorado-Boulder, USA
    14 May 2021
    Reader Comment
    Heneghan et al’s paper is not, as it claims, a systematic review on the role of airborne transmission for SARS-CoV-2 (Heneghan et al. 2021). The mismatch between the paper’s title, ... Continue reading
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  1. David R. Tomlinson, University Hospitals Plymouth NHS Trust, Plymouth, UK
  2. Nancy H. L. Leung, The University of Hong Kong, Hong Kong, Hong Kong
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