academic.oup.com Open in urlscan Pro
52.224.90.245 Public Scan

Back to summary

Submitted URL:
https://doi.org/10.1093/annweh/wxac056
Effective URL:
https://academic.oup.com/annweh/advance-article/doi/10.1093/annweh/wxac056/6693388
Submission: On December 05 via manual (December 5th 2022, 3:58:35 pm UTC) from US — Scanned from DE

Form analysis
1 forms found in the DOM

GET /Citation/Download

<form action="/Citation/Download" method="get" id="citationModal" citationmodal="set">
  <input type="hidden" name="resourceId" value="6693388">
  <input type="hidden" name="resourceType" value="3">
  <label for="selectFormat" class="hide js-citation-format-label">Select Format</label>
  <select required="" name="citationFormat" class="citation-download-format js-citation-format" id="selectFormat">
    <option selected="" disabled="">Select format</option>
    <option value="0">.ris (Mendeley, Papers, Zotero)</option>
    <option value="1">.enw (EndNote)</option>
    <option value="2">.bibtex (BibTex)</option>
    <option value="3">.txt (Medlars, RefWorks)</option>
  </select>
  <button class="btn citation-download-link disabled" type="submit">Download citation</button>
</form>

Text Content

We use cookies to enhance your experience on our website. By clicking 'continue'
or by continuing to use our website, you are agreeing to our use of cookies. You
can change your cookie settings at any time.
* Continue
* Find out more

We use cookies to enhance your experience on our website.By continuing to use
our website, you are agreeing to our use of cookies. You can change your cookie
settings at any time. Find out more Skip to Main Content
Advertisement
Journals
Books
* Search Menu
*
*
* Menu
*
*

Navbar Search Filter Annals of Work Exposures and Health Occupational
MedicineBooksJournalsOxford Academic Mobile Microsite Search Term Search
* Sign In
*

* Issues
* More Content
* Advance articles
* Editor's Choice
* Supplements
* Thematic Issues
* Submit
* Author Guidelines
* Online Submission Instructions
* Submission Site
* Open Access
* Purchase
* Alerts
* About
* About Annals of Work Exposures and Health
* About the British Occupational Hygiene Society
* Editorial Board
* Advertising and Corporate Services
* International Advisory Board
* Journals Career Network
* Self-Archiving Policy
* Contact the BOHS
* Journals on Oxford Academic
* Books on Oxford Academic

Close
Navbar Search Filter Annals of Work Exposures and Health Occupational
MedicineBooksJournalsOxford Academic Microsite Search Term Search
Advanced Search
Search Menu

Article Navigation
Close mobile search navigation
Article Navigation

ARTICLE CONTENTS

* Abstract
* Introduction
* Methods and materials
* Results
* Discussion
* Acknowledgements
* Funding
* Conflict of Interest
* Data Availability
* Creative commons
* References
* Supplementary data

Article Navigation
Article Navigation
Journal Article

DETECTION OF SARS-COV-2 IN AIR AND ON SURFACES IN ROOMS OF INFECTED NURSING HOME
RESIDENTS

Kimberly J Linde,
Kimberly J Linde
Institute for Risk Assessment Sciences, Utrecht University
,
Utrecht
,
The Netherlands
Author to whom correspondence should be addressed. Tel: +31302535358;
e-mail:K.j.linde@uu.nl
https://orcid.org/0000-0003-1190-9538
Search for other works by this author on:
Oxford Academic
PubMed
Google Scholar
Inge M Wouters,
Inge M Wouters
Institute for Risk Assessment Sciences, Utrecht University
,
Utrecht
,
The Netherlands
Search for other works by this author on:
Oxford Academic
PubMed
Google Scholar
Jan A J W Kluytmans,
Jan A J W Kluytmans
Julius Center for Health Sciences and Primary Care, University Medical Center
Utrecht, Utrecht University
,
Utrecht
,
The Netherlands
Search for other works by this author on:
Oxford Academic
PubMed
Google Scholar
Marjolein F Q Kluytmans-van den Bergh,
Marjolein F Q Kluytmans-van den Bergh
Julius Center for Health Sciences and Primary Care, University Medical Center
Utrecht, Utrecht University
,
Utrecht
,
The Netherlands
Department of Infection Control, Amphia Hospital
,
Breda
,
The Netherlands
Search for other works by this author on:
Oxford Academic
PubMed
Google Scholar
Suzan D Pas,
Suzan D Pas
Microvida Location Amphia/Bravis
,
Breda/Roosendaal
,
The Netherlands
Search for other works by this author on:
Oxford Academic
PubMed
Google Scholar
Corine H GeurtsvanKessel,
Corine H GeurtsvanKessel
Department of ViroScience, Erasmus MC
,
Rotterdam
,
The Netherlands
Search for other works by this author on:
Oxford Academic
PubMed
Google Scholar
Marion P G Koopmans,
Marion P G Koopmans
Department of ViroScience, Erasmus MC
,
Rotterdam
,
The Netherlands
https://orcid.org/0000-0002-5204-2312
Search for other works by this author on:
Oxford Academic
PubMed
Google Scholar
Melanie Meier,
Melanie Meier
Mijzo
,
Waalwijk
,
The Netherlands
Search for other works by this author on:
Oxford Academic
PubMed
Google Scholar
Patrick Meijer,
Patrick Meijer
Institute for Risk Assessment Sciences, Utrecht University
,
Utrecht
,
The Netherlands
Search for other works by this author on:
Oxford Academic
PubMed
Google Scholar
Ceder R Raben,
Ceder R Raben
Institute for Risk Assessment Sciences, Utrecht University
,
Utrecht
,
The Netherlands
Search for other works by this author on:
Oxford Academic
PubMed
Google Scholar
... Show more
Jack Spithoven,
Jack Spithoven
Institute for Risk Assessment Sciences, Utrecht University
,
Utrecht
,
The Netherlands
Search for other works by this author on:
Oxford Academic
PubMed
Google Scholar
Monique H G Tersteeg-Zijderveld,
Monique H G Tersteeg-Zijderveld
Institute for Risk Assessment Sciences, Utrecht University
,
Utrecht
,
The Netherlands
Search for other works by this author on:
Oxford Academic
PubMed
Google Scholar
Dick J J Heederik,
Dick J J Heederik
Institute for Risk Assessment Sciences, Utrecht University
,
Utrecht
,
The Netherlands
Search for other works by this author on:
Oxford Academic
PubMed
Google Scholar
Wietske Dohmen,
Wietske Dohmen
Institute for Risk Assessment Sciences, Utrecht University
,
Utrecht
,
The Netherlands
Search for other works by this author on:
Oxford Academic
PubMed
Google Scholar
COCON Consortium
COCON Consortium
Search for other works by this author on:
Oxford Academic
PubMed
Google Scholar
Annals of Work Exposures and Health, wxac056,
https://doi.org/10.1093/annweh/wxac056
Published:
07 September 2022
Article history
Received:
24 February 2022
Revision received:
12 July 2022
Editorial decision:
13 July 2022
Accepted:
29 July 2022
Published:
07 September 2022

* PDF
* Split View
* Views

* Article contents
* Figures & tables
* Supplementary Data
* Cite

CITE

Kimberly J Linde, Inge M Wouters, Jan A J W Kluytmans, Marjolein F Q
Kluytmans-van den Bergh, Suzan D Pas, Corine H GeurtsvanKessel, Marion P G
Koopmans, Melanie Meier, Patrick Meijer, Ceder R Raben, Jack Spithoven,
Monique H G Tersteeg-Zijderveld, Dick J J Heederik, Wietske Dohmen, COCON
Consortium, Detection of SARS-CoV-2 in Air and on Surfaces in Rooms of
Infected Nursing Home Residents, Annals of Work Exposures and Health, 2022;,
wxac056, https://doi.org/10.1093/annweh/wxac056

Select Format Select format .ris (Mendeley, Papers, Zotero) .enw (EndNote)
.bibtex (BibTex) .txt (Medlars, RefWorks) Download citation
Close
* Permissions Icon Permissions
* Share

* Email
* Twitter
* Facebook
* More

Navbar Search Filter Annals of Work Exposures and Health Occupational
MedicineBooksJournalsOxford Academic Mobile Microsite Search Term Search
* Sign In
*

Close
Navbar Search Filter Annals of Work Exposures and Health Occupational
MedicineBooksJournalsOxford Academic Microsite Search Term Search
Advanced Search
Search Menu

ABSTRACT

There is an ongoing debate on airborne transmission of Severe Acute Respiratory
Syndrome Coronavirus 2 (SARS-CoV-2) as a risk factor for infection. In this
study, the level of SARS-CoV-2 in air and on surfaces of SARS-CoV-2 infected
nursing home residents was assessed to gain insight in potential transmission
routes. During outbreaks, air samples were collected using three different
active and one passive air sampling technique in rooms of infected patients.
Oropharyngeal swabs (OPS) of the residents and dry surface swabs were collected.
Additionally, longitudinal passive air samples were collected during a period of
4 months in common areas of the wards. Presence of SARS-CoV-2 RNA was determined
using RT-qPCR, targeting the RdRp- and E-genes. OPS, samples of two active air
samplers and surface swabs with Ct-value ≤35 were tested for the presence of
infectious virus by cell culture. In total, 360 air and 319 surface samples from
patient rooms and common areas were collected. In rooms of 10 residents with
detected SARS-CoV-2 RNA in OPS, SARS-CoV-2 RNA was detected in 93 of 184
collected environmental samples (50.5%) (lowest Ct 29.5), substantially more
than in the rooms of residents with negative OPS on the day of environmental
sampling (n = 2) (3.6%). SARS-CoV-2 RNA was most frequently present in the
larger particle size fractions [>4 μm 60% (6/10); 1–4 μm 50% (5/10); <1 μm 20%
(2/10)] (Fischer exact test P = 0.076). The highest proportion of RNA-positive
air samples on room level was found with a filtration-based sampler 80% (8/10)
and the cyclone-based sampler 70% (7/10), and impingement-based sampler 50%
(5/10). SARS-CoV-2 RNA was detected in 10 out of 12 (83%) passive air samples in
patient rooms. Both high-touch and low-touch surfaces contained SARS-CoV-2
genome in rooms of residents with positive OPS [high 38% (21/55); low 50%
(22/44)]. In one active air sample, infectious virus in vitro was detected. In
conclusion, SARS-CoV-2 is frequently detected in air and on surfaces in the
immediate surroundings of room-isolated COVID-19 patients, providing evidence of
environmental contamination. The environmental contamination of SARS-CoV-2 and
infectious aerosols confirm the potential for transmission via air up to several
meters.

air levels, nursing home, SARS-CoV-2, surface
Issue Section:
Original Article
What’s Important About This Paper?

This study, conducted in a nursing home, provides insights into the extent of
SARS-CoV-2 presence in air and on surfaces around patients, and the infectivity
of aerosols. These insights can contribute to the discussion on potential
airborne transmission of SARS-CoV-2 and facilitates effective design of
prevention strategies such as use of facemasks, respirators, and ventilation.

INTRODUCTION

The ongoing pandemic, caused by Severe Acute Respiratory Syndrome Coronavirus 2
(SARS-CoV-2), continues to constitute a public health emergency of international
concern. There is consensus on the role of direct contact transmission and
airborne transmission at short distances (up to 3 m) through large droplets
caused by e.g. couhing and sneezing. There is an ongoing debate on transmission
through fomites and airborne transmission through smaller droplets caused by
e.g. speaking and breathing at larger distances (up to several meters) as a risk
factor for subsequent infection (Lednicky et al., 2020; Sikkema et al., 2020).
The relative importance of this mode of transmission as driver of the pandemic
is unknown. Several modes of transmission through the environment as a possible
risk of infection of SARS-CoV-2 is considered important for groups at high risk
(Cherrie et al., 2021).

Previous studies investigating SARS-CoV-2 air concentrations in healthcare
facilities showed contradictory results. In a limited number of studies in
hospital settings, SARS-CoV-2 has been detected in air in proximity (2–5 m) of
COVID-19 patients (Chia et al., 2020; Guo et al., 2020; Lednicky et al., 2020;
Liu et al., 2020; Santarpia et al., 2020; Conway-Morris et al., 2021). Other
studies did not find evidence of SARS-CoV-2 in air (Faridi et al., 2020;
Masoumbeigi et al., 2020; Lane et al., 2021; Vosoughi et al., 2021). However,
the comparability of studies is limited due to differences in sampling methods,
sampling duration, and distance to infected persons. Oropharyngeal swabs were
not consistently collected from infected persons for confirmation of infection
and the actual level SARS-CoV-2 shedding in addition to the collection of air
samples. Infectiousness of SARS-CoV-2 detected in air was not investigated in
most studies (Chia et al., 2020; Guo et al., 2020; Liu et al., 2020;
Conway-Morris et al., 2021) or could not be shown (Döhla et al., 2022; Nannu
Shankar et al., 2022). Infectivity and amount of shed virus have been reported
to rapidly decline during the first week after illness onset (van Beek et al.,
2021; van Kampen et al., 2021). As viral RNA can persist and be shed for
prolonged periods of time without being infectious, it is important to
investigate the viability of virus in air to understand airborne transmission
routes of the virus. Therefore, to successfully investigate modes of
transmission of SARS-CoV-2, it seems crucial to investigate SARS-CoV-2 air
concentrations in the first days following infection.

After the first pandemic wave in The Netherlands, nursing homes had introduced
enhanced surveillance screening for SARS-CoV-2, which led to the identification
of new infections at an early stage (National Institute for Public Health and
the Environment, 2021). To investigate potential airborne transmission routes
from SARS-CoV-2 infected patients to their immediate surroundings, we measured
SARS-CoV-2 in air and on surfaces in Dutch nursing home residencies as well as
in rooms of SARS-CoV-2 isolated infected nursing home residents.

METHODS AND MATERIALS

The study consisted of two arms: a series of environmental investigations during
outbreaks and longitudinal air monitoring (Fig. 1). Weekly SARS-CoV-2 infections
were registered and notified in 28 nursing homes from Mijzo Care organisation in
Noord-Brabant in the Netherlands. In case of two or more confirmed SARS-CoV-2
infections in residents within the same ward, an outbreak investigation was
initiated, consisting of extensive environmental sample collection and
SARS-CoV-2 testing of persons. In a subsample of 3 of the 28 nursing homes,
longitudinal monitoring took place in the direct living environment. The study
protocol was evaluated by the Medical Research Ethics Committee of University
Medical Centre Utrecht. As the study did not fall within the scope of the Dutch
Act on Medical Research Involving Human Subjects no further medical ethical
approval was required (METC protocol no. 20-277/C). The study was conducted in
agreement with the European legislation on handling privacy-sensitive data.

Figure 1.
Open in new tabDownload slide

Design of the study. The study consisted of an outbreak investigation which was
complemented by longitudinal air monitoring

OUTBREAK INVESTIGATION

Residents of the nursing homes were tested for possible SARS-CoV-2 infection in
case they experienced COVID-19-related symptoms. When one or more residents in a
ward tested positive for SARS-CoV-2 infection, all other ward residents were
screened for SARS-CoV-2 infection during surveillance rounds. Residents who
tested positive for SARS-CoV-2 RNA were eligible for inclusion in the outbreak
investigation within 8 days since the onset of symptoms or within 8 days since
the first positive surveillance test result. Only patients in isolation from
somatic wards were included. Oral informed consent was obtained from patients
and/or from an authorized legal representative or family member.

COLLECTION OF AIR SAMPLES

Air samples were collected at three locations in the patient’s room: (i) near
the head of the patients within approximately 0.5 m of the patient, (ii) near
the feet of bedridden patients approximately 1.5 m from the head or
approximately 1.5 m from mobile patients sitting in a chair, and (iii) near the
location often used by healthcare workers more than 2 m away from the patient
such as the sink, all positioned at 1.5 m height. In every patient room, 6-hr
inhalable dust samples were taken using a filtration-based technique at all
three locations [Conical Inhalable dust Sampler (CIS), JS Holdings, UK]. In
addition, one 6-hr two-stage cyclone-based sample with filter back-up was
positioned near the feet of the patient when bedridden or at 1.5 m from the
chair of the patient (NIOSH BC 251, kindly provided by Dr William G Lindsley,
NIOSH CDC, Morgantown, USA), as well as a 1-hr impingement-based sampler
positioned in proximity of the head of the patient (5 ml BioSampler, SKC, UK)
[see Supplement Fig. S1 (available at Annals of Occupational Hygiene online)].
During the 6-hr sample collection, mobile patients were allowed to move in the
room. During the 1-hr impingement-based sample collection, they were asked to
stay seated in their chair. The filtration-based sampler was equipped with a 37
mm diameter 2.0 μm pore-size Teflon filter (Pall incorporated, Ann Arbor, USA).
The two-stage cyclone-based sampler allowed size-selective sampling and was
equipped with two conical tubes (of 15 ml and 1.5 ml) which sample respectively
particulates of 1–4 μm and >4 μm, and a back-up Teflon filter (37 mm diameter
2.0 μm pore-size Pall incorporated, Ann Arbor, USA) for particulates of <1 μm
when operated at a flow of 3.5 l min‐1. The 15 ml and 1.5 ml conical tubes were
filled with virus transport medium 1 (VTM-1; Erasmus Medical Center (EMC),
Rotterdam, The Netherlands) during sampling and Opti-MeM (Gibco, UK) was added
immediately after collection [see Supplementary methods (available at Annals of
Occupational Hygiene online) for more details and composition of media]. Adding
VTM-1 is a modification of the standard operating procedure for this sampler
with the aim to enhance the culturability of the virus. The impingement-based
sampler contained VTM-1 during sampling, and after completion of sampling,
Opti-MeM was added as well.

Airborne settling dust was sampled using Electrostatic Dust Collectors (EDCs)
(Noss et al., 2008), which were placed in each included patient room and the
corresponding hallway, common living room, and nurse office of the ward. EDCs
were placed in holders pinned to the ceiling in the middle of the space,
approximately 30 cm underneath the ceiling or on top of a cabinet. EDCs were
collected after 2–4 weeks of sampling, dependent on the timing of extensive
cleaning of the room.

COLLECTION OF SURFACE SAMPLES

High- and low-touch surface samples were collected using dry surface swabs
(Medical Wire Dry Swabs, MW730, Corsham, UK) as described previously (WHO and
World Health Organization, 2020; de Rooij et al., 2021). A total of 10 samples
were taken in each patient room, and in the corresponding hallway, common living
room, and nurse office of the ward. Disposable plastic grids of 10 cm2 were used
to standardize collection of surface swabs. Swabs were placed in viral transport
medium 2 (VTM-2; Erasmus Medical Center (EMC), Rotterdam, The Netherlands)
directly after collection [see Supplementary methods (available at Annals of
Occupational Hygiene online) for the composition of media].

Field blank samples were collected every other outbreak sampling day for each
air sampling technique and every outbreak sampling day for surface swab
sampling. See Supplementary methods (available at Annals of Occupational Hygiene
online) for details on sample collection and laboratory methods.

PATIENT CHARACTERISTICS

Patient characteristics were obtained: gender, year of birth, date of symptom
onset, symptoms, date of SARS-CoV-2 test, SARS-CoV-2 test results, COVID-19
treatment such as oxygen therapy and mobility. An affirmative oropharyngeal swab
(OPS) (Medical Wire Dry Swabs, 111598, Milan, Italy) was collected during the
outbreak investigation and stored in a tube containing VTM-2.

LONGITUDINAL AIR MONITORING

Three of the 28 nursing homes with at least three wards (somatic and/or
geriatric) were selected for longitudinal air monitoring. In each selected
nursing home, settling dust samples were collected repeatedly in three to four
wards from December 2020 until May 2021. Per ward, six EDCs were placed in
hallways, living rooms, and nurse offices and renewed every four weeks for a
period of four months. Incidence of SARS-CoV-2 infections in patients and staff
members at the included wards was obtained in weekly reports.

LABORATORY ANALYSIS

All samples, except settling dust samples, were stored and sent to the
laboratory refrigerated at 4°C directly after collection. At the laboratory,
samples were stored at 4°C until further processing within 24-hr under biosafety
laboratory (BSL)-2+ conditions (Duane, 2013). Filters were removed from the
filter holder and transferred to a tube containing VTM-1. These and all other
outbreak investigation samples were subsequently vortexed. Settling dust samples
were transferred to tubes containing VTM-2 and tamped down, vortexed, and soaked
repeatedly for several minutes. For RT-qPCR analysis, an aliquot of VTM was
mixed in a 1:1 dilution with MagNA Pure 96 External Lysis Buffer for each sample
(Roche Diagnostics, Almere the Netherlands). The remaining VTM from
cyclone-based samples, impingement-based samples, surface swabs, and OPS were
stored for culturing. All samples were stored frozen at ‐80°C until further
processing. More details are described in Supplementary methods (available at
Annals of Occupational Hygiene online).

REAL-TIME SEMI-QUANTITATIVE REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION

VTM-lysis buffer samples were tested for the presence of SARS-CoV-2 RNA using a
SARS-CoV-2 RNA RT-qPCR, targeting the E-gene and CoV-2 RdRp-gene of SARS-CoV-2
using the cobas 6800/8800 Systems (Roche Diagnostics) (Stohr et al., 2020). If
both E-gene and RdRp-gene were detected with Cobas RT-qPCR, samples were
classified as positive. In case of a discrepant result, i.e. only one of the two
genes was detected, an in-house RT-qPCR assay was conducted for confirmation
(Kluytmans-Van Den Bergh et al., 2020). In the case of detection of SARS-CoV-2
RNA, the sample was classified as positive and in the case of inconclusive or
nondetection with in-house RT-qPCR, the final result was classified as
inconclusive. Samples with nondetection of both genes were classified as
negative.

VIRUS CULTURE

OPS, cyclone-based samples, impingement-based samples, and surface swabs tested
positive by RT-qPCR with RdRp Ct ≤35 were tested for infectious SARS-CoV-2, as
described previously (van Kampen et al., 2021). Virus culture was performed in
24-wells plates seeded with Vero cells, clone 118. Samples were added to the
wells, centrifuged, and inoculum was discarded. Virus culture medium was added,
and samples were cultured at 37°C and 5% CO2 for seven days. If a virus-induced
cytopathic effect (CPE) was observed, immunofluorescent detection of SARS-CoV-2
nucleocapsid protein was performed to confirm the presence of SARS-CoV-2.

SARS-COV-2 WHOLE GENOMEN SEQUENCING (WGS)

In samples with RT-PCR RdRp Ct-values <31 whole genome sequencing was performed
on the primary clinical specimen by Microvida to determine the SARS-CoV-2
variant. Genomes with >90% genome coverage were included. For more details see
Supplementary Methods (available at Annals of Occupational Hygiene online).

DATA ANALYSIS

Data entry was carried out in Microsoft Access Version 16 2012. Descriptive
statistics were obtained by R studio Version 1.4.1106 2021. Active air sample
techniques were compared on room level. If one or more of the filtration-based
samples in a room were positive, the outcome on room level was classified as
positive. The same applied for the CDC-NIOSH cyclone-based samples on room
level. Fisher’s exact test was used to compare the proportion of positive
samples in association with particle size fractions, distance, and location, and
to compare air sampling techniques. Agreement between outcomes of
filtration-based and cyclone-based samples collected at the same location was
investigated through Cohen’s Kappa test statistics. A threshold of 0.05 was used
for the P-value for statistical significance.

RESULTS

A total of 679 environmental samples were collected from five nursing home
wards, including 101 air samples and 122 surface samples from the patient rooms
and 259 air samples and 197 surface samples from common areas. In total, 13
patients were included for environmental sample collection during outbreak
investigations. One patient withdrew from the study during sampling. Of the
remaining 12 patients, 2 tested negative, and 10 tested positive in affirmative
OPS collected on the day of environmental sample collection (Table 1). From one
of the two patients with negative OPS only surface swabs were collected because
the patient retracted participation to the study after surface swab sampling.
For air samples, RdRp Ct-values ranged from 29.5 to 37.2 and from 30.2 to 37.8
in surface swab and from 19.8 to 34.7 in OPS. All field and laboratory blanks
tested negative for viral SARS-CoV-2 RNA.

Table 1.

SARS-CoV-2 PCR in environmental samples in the surrounding of isolated patients
and common areas in nursing homes

Outbreak . Location . Patient characteristics . Environmental samples . .
. Day of illness . Mobility . Oropharyngeal swab (RdRp CT) . Active air sampling
. Passive (air) sampling . . . . . . CIS-inhalable dust . CDC-NIOSH
bioaerosol sampler-cyclone-based . SKC Bio-sampler -Impinger . EDC-settling dust
. Surface swabs . . . . . . PTFE filter . PTFE filter
(<1 μm) . Microcentrifuge tube
1.5 ml
(1–4 μm) . Centrifuge tube
15 ml
(>4 μm) . . . . A Patient room 10 4 No 19.8C 3/0/0 1/0/0 1/0/0 1/0/0
C 1/0/0 NO 4/1/5 Patient room 11x 6 Yes Neg NO NO NO NO NO 0/1/0 1/0/9 Patient
room 12 7 NoOX 29.6 2/1/0 0/0/1 1/0/0 0/1/0 0/0/1 NO 3/0/6 Common
areas – – – – – – – – 2/1/3 0/0/20* B1 Patient room
13 1 NoOX 27.6C 3/0/0 0/0/1 1/0/0 1/0/0 1/0/0 1/0/0 9/0/1 Patient room
14 AS Yes Neg 0/0/3 0/0/1 0/0/1 0/0/1 0/0/1 0/1/1 0/0/10 Patient room
15 Unclear Yes 29.7 0/0/3 0/0/1 0/0/1 0/0/1 1/0/0 1/0/0 5/1/4 Common
areas – – – – – – – – 3/0/2 0/0/30 B2 Patient room
16 AS Yes 32.8 2/0/1 0/0/1 0/0/1 1/0/0 0/0/1 2/0/0 4/0/6 Patient room
17 AS Yes 19.9C 3/0/0 1/0/0 1/0/0 1/0/0 1/0/0 2/0/0 5/1/4 Patient room
18 1 Yes 33.6 2/0/1 0/0/1 0/0/1 1/0/0 0/0/1 1/0/1 4/0/6 Common
areas – – – – – – – – 3/0/2 4/0/26 C** Patient room
19x 5 Yes NO 0/0/3 0/0/1● 0/0/1● 0/0/1● NO 0/0/2 NO Common
areas – – – – – – – – NO 0/0/30 Patient room
20 5 Yes 34.7 3/0/0 0/0/1 1/0/0 1/0/0 1/0/0 2/0/0 12/0/1*** Common
areas – – – – – – – – NO 1/0/26 D
E Patient room
22 3 NoOX 30.8 1/0/2 0/0/1 0/0/1 0/0/1 0/0/1 0/0/1 0/0/10 Common
areas – – – – – – – – 0/0/5 0/0/30 Patient room
25V 6 Yes 33.5 0/1/2 0/0/1 0/1/0 0/1/0 0/1/0 1/0/0 0/1/9 Common
areas – – – – – – – – 0/0/6 0/0/30

SARS-CoV-2 results from environmental samples: Number of
positive/inconclusive/negative. All positive samples from PCR are cultured from
oropharyngeal swab, CDC-NIOSH bioaerosol sampler, SKC Bio-sampler, and surfaces
wabs. Day of illness is counted since onset of symptoms. In case planned samples
were not obtained the following reasons applied: retraction patient, no
availability, or accessibility of area during sample collection, sample got
lost, or discarded by staff.

*Living room was not available for sampling due to closure.

**Two patients on different wards.

***Cat supplies were sampled additionally.

● Duration of sampling 4 hr due to retraction patient/NO = 1 sample was not
obtained/C = positive culture/AS = asymptomatic/OX = optiflow/V = vaccinated. In
total 27 samples were not obtained because of retraction patient, no
availability of area during sample collection, or discarded by staff.

Open in new tab
Table 1.

SARS-CoV-2 PCR in environmental samples in the surrounding of isolated patients
and common areas in nursing homes

*Living room was not available for sampling due to closure.

**Two patients on different wards.

***Cat supplies were sampled additionally.

Open in new tab

SARS-COV-2 CONTAMINATION IN AIR

Of the 184 environmental samples, 82 air and 102 surface samples, collected in
rooms of patients with positive OPS on the day of sampling, 50.5% were positive
(93/184). From the two patients with negative OPS, only one of the samples
tested positive (1/29), which appeared a surface swab (Table 1).

All four air sampling techniques detected SARS-CoV-2 RNA and showed high rates
of positive samples in the rooms of patients with positive OPS (Table 3). The
highest proportion of positive active air samples was found with the
filtration-based sampler 80% (8/10) and CDC-NIOSH cyclone-based sampler [70%
(7/10)]. The impingement-based sampler [50% (5/10)] showed a slightly lower
proportion of positive samples, but the results were not statistically
significant (Fisher-exact test P-value = 0.69). The cyclone-based samples
sampled approximately 1.26 m3 of air, the filtration-based samples 1.26 m3, and
the impingement-based 0.75 m3. Ten of the collected 12 settling dust samples
from rooms were positive (83%). Filtration-based samples and cyclone-based
samples collected side-by-side at the same distance from the patient were
concordant in 8 out of 10 cases [moderate agreement (Cohen’s kappa coefficient
kappa = 0.5, P-value = 0.197)] (Supplement Table S4, available at Annals of
Occupational Hygiene online).

SARS-CoV-2 was detected at all distances from the patient (bedridden and mobile
patients). No clear trend was seen in numbers of positive samples with distance
from the patient in filtration-based air samples [>1.5 m 50% (6/12); ≤1.5 m 67%
(10/15)] (Fisher-exact test, P-value = 0.4175) (Supplement Table S3, available
at Annals of Occupational Hygiene online).

In all particle size-specific fractions [>4 μm 60% (6/10); 1–4 μm 50% (5/10); <1
μm 20% (2/10)] SARS-CoV-2 RNA was detected (Table 2). However, inconclusive and
positive results were more frequently present in the largest particle size
fraction, followed by the intermediate size fraction. These differences in
distribution of size categories was borderline statistically significant
(Fischer exact test P-value = 0.076).

Table 2.

SARS-CoV-2 PCR results in size-specific fractions obtained by cyclone-based air
sampling in rooms of patients with positive oropharyngeal swab

. CDC-NIOSH cyclone-based bioaerosol sampler . . <1 μm . 1–4 μm . >4 μm .
. PTFE filter . Microcentrifuge tube 1.5 ml . Centrifuge tube 15 ml . . n (%)
. n (%) . n (%) . Negative (‐ ‐) 8 (80) 4 (40) 2 (20) Inconclusive (‐ +) 0 (0) 1
(10) 2 (20) Positive (+ +) 2 (20) 5 (50) 6 (60)

Open in new tab
Table 2.

SARS-CoV-2 PCR results in size-specific fractions obtained by cyclone-based air
sampling in rooms of patients with positive oropharyngeal swab

Open in new tab
Table 3.

SARS-CoV-2 results from three active and one passive air sampling technique used
during the outbreak investigation from patients with positive oropharyngeal swab

. CIS-
inhalable dust . SKC Bio-sampler -
Impinger . CDC-NIOS Hcyclone- based bioaerosol * . EDC -
settling dust . . n (%) . n (%) . n (%) . n (%) . Negative (‐ ‐) 9 (30) 4
(40) 2 (20) 2 (17) Inconclusive (‐ +) 2 (7) 1 (10) 1 (10) 0 (0) Positive (+
+) 19 (63) 5 (50) 7 (70) 10 (83)

*If one of the fractions of the cyclone-based sample detected SARS-CoV-2, the
overall parameter is classified positive.

Open in new tab
Table 3.

SARS-CoV-2 results from three active and one passive air sampling technique used
during the outbreak investigation from patients with positive oropharyngeal swab

*If one of the fractions of the cyclone-based sample detected SARS-CoV-2, the
overall parameter is classified positive.

Open in new tab

HIGH- AND LOW-TOUCH SURFACE SWABS

The proportion of positive surface samples was much higher in rooms from
patients with positive OPS compared to rooms with negative patients [43% (43/99)
versus 0.5% (1/20)] [see Supplement Table S5 (available at Annals of
Occupational Hygiene online)]. SARS-CoV-2 RNA was detected slightly more
frequently in surface swabs from low-touch surfaces than from high-touch
surfaces [low 50% (22/44); high 38% (21/55)] (Fisher’s exact test P-value =
0.18). Only 5 of the 197 surface samples collected in common areas were positive
for SARS-CoV-2; four low and one high-touch sample (Supplement Table S6,
available at Annals of Occupational Hygiene online).

VIRUS CULTURE

Among the 78 positive OPS, cyclone-based samples, impingement-based samples,
surface swab samples, 44 had a RdRp Ct-value ≤35 and were further investigated
by in vitro virus culture. This selection contained four impingement-based
samples, three cyclone-based samples fraction size >4 μm, three cyclone-based
samples fraction size 1–4 μm, 26 surface swabs, and eight OPS collected in nine
patient rooms. The impingement-based samples and cyclone-based samples were
collected in four patient rooms. Cytopathic effects were observed in three OPS
and one active air sample and were confirmed by immunofluorescent staining. The
active air sample from the CDC-NIOSH sampler (>4 µm size fraction) had the
lowest Ct-value of all environmental samples (29.5) and was derived from the
room of the patient with the lowest OPS Ct-value (19.82).

WHOLE GENOME SEQUENCING (WGS)

In total, nine samples with RdRp Ct-values ranging from 19.8 to 30.2 were
selected for SARS-CoV-2 whole genome sequencing, of which six OPS, one
cyclone-based sample, one filtration-based sample, and one surface swab. From
five OPS samples, >90% of the reference was covered and uploaded in GISAID. All
variants were B.1.221, a known variant, circulating in The Netherlands at the
time of the study. Samples collected at the same location were closely
genetically related. During the data collection from December 2020 until May
2021, B.1.1.7, also known as the Alpha variant, became the dominant SARS-CoV-2
circulating variant in The Netherlands (National Institute for Public Health and
the Environment, 2022). The sequences have been registered in GISAID
(www.gisaid.org; Accession ID EPI_ISL_2259112, EPI_ISL_2259136,
EPI_ISL_2259188). See Supplementary Methods (available at Annals of Occupational
Hygiene online) for more details see acknowledgement table.

LONGITUDINAL AIR MONITORING

Only seven of the 259 settling dust samples collected repeatedly in three wards
were positive (2.7%). All samples were collected in common areas in nursing
homes where SARS-CoV-2 infections had been reported among residents (Supplement
Table S7, available at Annals of Occupational Hygiene online). The low rate
corroborates with the incidence of infections in patients and healthcare
workers, which rapidly decreased during the study (Supplementary Table S7,
available at Annals of Occupational Hygiene online). No viral RNA was detected
in wards without registered SARS-CoV-2 infected patients and/or healthcare
workers shortly before or during sampling.

DISCUSSION

In this study, comprising 679 environmental samples, SARS-CoV-2 was frequently
detected in air and on surfaces in the immediate surroundings of COVID-19
patients, providing evidence of virus shedding to the environment through air by
infected persons. SARS-CoV-2 was detected more frequently in the particle size
fraction 1–4 μm (respirable fraction) and particulates >4 μm as compared to <1
μm. Airborne particulates might be infectious, as illustrated by the fact that
we were able to replicate virus from an active air sample. Our results support
the role of airborne transmission of SARS-CoV-2, which in turn is a risk factor
for subsequent infection.

SARS-CoV-2 RNA was detected in all types of air samples and on high- and
low-touch surfaces in the surrounding of patients with a positive OPS. No
SARS-CoV-2 RNA was detected in air or the immediate surroundings of patients who
tested negative. The number of positive environmental samples in this study was
high compared to other studies (Lednicky et al., 2020; Semelka et al., 2021).
Although the study size is small to modest, environmental sampling was performed
extensively, using a range of sampling techniques, around patients in the early
phase of infection, assuming active shedding of SARS-CoV-2. Previously, van Beek
et al. (2021), established a shedding curve using data from 223 persons testing
SARS-CoV-2 in a drive-through test station, showing that viral loads were
highest within eight days post-onset of symptoms. Moreover, Van Kampen et al.
(2021), reported that infectious virus shedding also occurred mainly within the
first eight days post-onset, based on data from 129 hospitalized patients with
repeated measurements. Therefore, our study’s timing of environmental
measurements has likely contributed to the high detection rate in environmental
samples. This is in agreement with a study from Chia et al. (2020) only
detecting SARS-CoV-2 in air or the immediate surroundings of two patients
infected less than eight days compared to no detection of SARS-CoV-2 in the air
of another patient nine days postinfection. Several other studies were not able
to detect SARS-CoV-2 in air in the surrounding of patients more than eight days
after post-onset of symptoms (Chia et al., 2020; Dumont-Leblond et al., 2021;
Semelka et al., 2021). Moreover, in other studies in human and animal settings,
SARS-CoV-2 was only detected in environmental samples if the human and animal
source organisms were actively shedding SARS-CoV-2 during sampling (de Rooij et
al., 2021; Jonker et al., 2022). These observations emphasize that timing of
sampling in the direct environment of patients and other populations is of
importance for detecting SARS-CoV-2 and that surroundings from SARS-CoV-2
patients in early stage are contaminated with SARS-CoV-2.

Of the SARS-CoV-2 containing aerosols, 54% was in the size range <4 µm and 46%
in the size range of ≥4 µm. When including samples with inconclusive qPCR test
results, these figures hardly changed (50–50%). Although the use of the NIOSH
sampler was modified by adding VTM to the vials prior to sampling, which may
theoretically have altered size-selective sampling characteristics, our results
are in line with other studies that performed size-selective sampling of
SARS-CoV-2 virus. For instance, Adenaiye et al. (2021), analysed SARS-CoV-2
virus in exhaled breath collected from 49 COVID-19 cases (mean days postonset
3.8 ± 2.1) in an experimental setting and found SARS-CoV-2 RNA in 36% of fine
(≤5 µm), and 26% of coarse (>5 µm) aerosols. Moreover, other studies using the
same CDC-NIOSH bio-sampler methodology as this study, exclusively detected
SARS-CoV-2 in the larger ≥4 µm and intermediate size fraction 1–4 µm in
environmental samples collected in rooms of COVID-19 patients in hospitals (Chia
et al., 2020; Conway-Morris et al., 2021). Similar observations in size
distribution have been reported previously for human influenza virus (Blachere
et al., 2009; Lindsley et al., 2010). These results for different viruses from
infected patients indicate that a substantial part of particulates is found in
the respirable fraction (Blachere et al., 2009). Viral RNA loads and infectious
viral RNA loads can differ between patients and are likely influenced by
infection status and disease progression. Moreover, the strain-specific viral
load and the location of infection in airways influence the particle size
distribution and transmission mode to the environment. A different variant, such
as Omikron, which is more contagious and is primarily present in the upper
respiratory tract, might therefore distribute differently in the environment
(Vihta et al., 2022).

Out of ten active air samples eligible for culture, we were able to replicate
virus from one sample. Only a few studies successfully showed signs of
SARS-CoV-2 replication in air samples (Lednicky et al., 2020; Santarpia et al.,
2020; Adenaiye et al., 2021). However, underestimation of infectiousness is a
likely consequence of virus inactivation during sample collection (Lindsley et
al., 2010). Current culture techniques may not be optimal for low viral
concentrations as in air samples (Zhang et al., 2020). Overall, results suggest
that virus particulates can cause infection in individuals who inhale these
particulates when the infectious dose is sufficiently high.

Literature on the infectious dose of SARS-CoV-2 is scarce. Dabisch et al. (2021)
reported an infectious dose of 52 TCID50 for a seroconversion response and 256
TCID50 for a fever response based on an inhalation exposure of 10 min in
nonhuman primates Macaques. Others have estimated an infectious dose for
infection ranging between single and 1000 virions based on a model combining
information on viral mutations obtained through deep sequencing and epidemiology
in known infector-infectee pairs (Popa et al., 2020; Martin and Koelle, 2021;
Nicholson et al., 2021). Based on the estimated relationship between E-gene
RT-PCR Cq values and cell-cultured SARS-CoV-2 virus loads by Schuijt et al.
(2021), the air sample which showed replication in our study contained
approximately 170 000 viral copies per cubic meter of air. Despite uncertainties
associated with this simple calculation (for instance, assuming similarity in
RT-qPCR responses between cell-cultured virus and air samples), the estimated
dose may indeed be capable of causing infection. Quantification of the other
environmental samples was not attempted, since uncertainty would even be greater
due to high Ct-values. Moreover, our measurements took place during relatively
long periods. Environmental levels likely varied considerably over the sampling
period. Variation in viral load could not be established over this time span.
However, it is unlikely that viral shedding is constant over time. Coughing, for
instance, results in higher viral RNA loads over a short time span.

There is an ongoing debate on the airborne transmission route of SARS-CoV-2 and
the effect of ventilation on airborne transmission. Greenhalg et al. (2021)
previously pointed out multiple reasons for airborne transmission as the main
route of SARS-CoV-2, to which our study provides additional strength. First, our
study detected SARS-CoV-2 in abundance in air and on surfaces, including
numerous low-touch surfaces such as on top of the wardrobe, which implicates
viral dissemination through the air by aerosols. Second, SARS-CoV-2 was
primarily found in particle size fractions of 1–4 μm and larger than 4 μm, which
are known to stay airborne for extended periods of time and thus disseminate
potentially over larger distances. Third, we successfully cultured SARS-CoV-2
from an active air sample from particle size >4 μm and aerosols have been
reported to stay infectious in the air for up to 3 hr (van Doremalen et al.,
2020).

Based on our study, smaller particles (<1 μm), which can travel further, do not
seem to be the key vehicle of SARS-CoV-2 transmission. Although virus
contamination was omnipresent in air in infected patient rooms, the vast
majority of settling dust and surface swab samples from common areas were
negative, suggesting SARS-CoV-2 transmission is more a local phenomenon than
widespread. To mitigate (occupational) transmission risks, it is important to
investigate the effect of ventilation and air filtration on airborne
transmission reduction. Till date, only Conway-Morris et al. (2021) investigated
and successfully demonstrated removal of SARS-CoV-2 from air by placing active
filtration and sterilization devices in wards. Further research on the effect of
ventilation and filtration devices is required to draw strong conclusions about
the role of ventilation conditions in reducing airborne transmission. Despite
the aforementioned limitations of this study, such as sample size and
semi-quantitative results, SARS-CoV-2 is detected regularly confirming the
potential airborne transmission route of SARS-CoV-2 for subsequent infection.
Replication of this study in a larger sample size is required to investigate
dispersal abilities, infectiousness, and particle sizes of aerosol containing
SARS-CoV-2.

In conclusion, in this study potential airborne transmission routes from
SARS-CoV-2 infected patients to their immediate surroundings were investigated.
SARS-CoV-2 was numerously detected in air and on surfaces in case of actively
shedding patients. Furthermore, the environmental contamination of SARS-CoV-2
and infectious aerosols confirm the potential for airborne transmission routes
via air up to several meters and therefore the possible risk of infection of
SARS-CoV-2. These insights can contribute to the discussion on airborne
transmission and facilitate effective design of prevention strategies such as
use of facemasks and optimising ventilation conditions.

ACKNOWLEDGEMENTS

We thank the patients and healthcare workers for their cooperation and in
particular Michelle van Wanrooij and Adrie de Laat from the overarching
healthcare organisation Mijzo Waalwijk for their commitment and contribution. We
further thank our colleagues Daan Cohen, Calvin Gue, Kees Meliefste, Duco
Ottevanger, Santiago Parga, Myrna de Rooij, Peter Scherpenisse and Wouter van
der Hoef from Institute Risk Assessment, Lennie Derde and Etienne Sluis from the
University Medical Center Utrecht for their contribution in optimalisation of
air sampling, laboratorial preparations and sample processing, and Microvida
location Amphia Roosendaal and Department of ViroScience of Erasmus MC Rotterdam
for further analysis of the samples. Moreover, we thank Dr. Lindsley from
National Institute for Occupational Safety and Health Morgentown for the
CDC-NIOSCH bio-samplers for their assistance in the pilot study. This study is
funded by ZonMw (projectnumber 10150062010004) and part of Control of COVID-19
iN Hospitals (COCON) consortium which also involves Rosa van Mansfeld,
Karin-Ellen Veldkamp, and Andreas Voss.

FUNDING

Funding for this project was provided by ZonMw and part of Control of COVID-19
iN Hospitals (COCON) consortium (project number 10150062010004).

CONFLICT OF INTEREST

The authors declare they have nothing to disclose. The authors declare no
conflict of interest relating to the material presented in this Article. Its
contents, including any opinions and/or conclusions expressed, are solely those
of the authors.

DATA AVAILABILITY

The data underlying this article will be shared on reasonable request to the
corresponding author.

CREATIVE COMMONS

This is an open access article distributed in accordance with the Creative
Commons Attribution Non Commercial (CC BY-NC 4.0) license.

REFERENCES

Adenaiye
OO
,
Jianyu
L
,
Jacob Bueno de Mesquita
P
et al. (
2021
)
Infectious severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in
exhaled aerosols and efficacy of masks during early mild infection
.
Clin Infect Dis
;
ciab797
. doi:10.1093/cid/ciab797.

Google Scholar

OpenURL Placeholder Text

WorldCat

van Beek
J
,
Igloi
Z
,
Boelsums
T
et al. (
2021
)
From more testing to smart testing: data-guided SARS-CoV-2 testing choices, the
Netherlands, May to September 2020
.
Euro Surveillance
;
27
.

Google Scholar

OpenURL Placeholder Text

WorldCat

Blachere
FM
,
William
GL
,
Terri
AP
et al. (
2009
)
Measurement of airborne influenza virus in a hospital emergency department
.
Clin Infect Dis
;
48
:
438
–
40
.

Google Scholar

Crossref
Search ADS

PubMed

WorldCat

Cherrie
JW
,
Cherrie
MPC
,
Smith
A
et al. (
2021
)
Contamination of air and surfaces in workplaces with SARS-CoV-2 virus: a
systematic review
.
Ann Work Expo Health
;
65
:
879
–
92
.

Google Scholar

Crossref
Search ADS

PubMed

WorldCat

Chia
PY
,
Coleman
KK
,
Tan
YK
et al. (
2020
)
Detection of air and surface contamination by SARS-CoV-2 in hospital rooms of
infected patients
.
Nat Commun
;
11
:
2800
. doi:10.1038/s41467-020-16670-2.

Google Scholar

Crossref
Search ADS

PubMed

WorldCat

Conway-Morris
A
,
Sharrocks
K
,
Bousfield
R
et al. (
2021
)
The removal of airborne SARS-CoV-2 and other microbial bioaerosols by air
filtration on COVID-19 surge units
.
Clin Infect Dis
;
ciab933
. doi:10.1093/cid/ciab933.

Google Scholar

OpenURL Placeholder Text

WorldCat

Dabisch
PA
,
Jennifer
B
,
Katie
B
et al. (
2021
)
Seroconversion and fever are dose-dependent in a nonhuman primate model of
inhalational COVID-19
.
PLoS Pathog
;
17
:
e1009865
. doi:10.1371/journal.ppat.1009865.

Google Scholar

OpenURL Placeholder Text

WorldCat

Döhla
M
,
Wilbring
G
,
Schulte
B
et al. (
2022
)
SARS-CoV-2 in environmental samples of quarantined households
.
Viruses
;
14
:
1075
. doi: 10.3390/v14051075.

Google Scholar

Crossref
Search ADS

PubMed

WorldCat

van Doremalen
N
,
Bushmaker
T
,
Morris
D
. (
2020
)
Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1
.
N Engl J Med
;
382
:
1564
–
7
. doi:10.1056/NEJMc2004973.

Google Scholar

Crossref
Search ADS

PubMed

WorldCat

Duane
EG
. (
2013
)
A practical guide to implementing a BSL-2+ biosafety program in a research
laboratory
.
Appl Biosaf
;
18
:
30
–
6
.

Google Scholar

Crossref
Search ADS

WorldCat

Dumont-Leblond
N
,
Veillette
M
,
Bhérer
L
et al. (
2021
)
Positive no-touch surfaces and undetectable SARS-CoV-2 aerosols in long-term
care facilities: an attempt to understand the contributing factors and the
importance of timing in air sampling campaigns
.
Am J Infect Control
;
49
:
701
–
6
.

Google Scholar

Crossref
Search ADS

PubMed

WorldCat

Faridi
S
,
Niazi
S
,
Sadeghi
K
et al. (
2020
)
A field indoor air measurement of SARS-CoV-2 in the patient rooms of the largest
hospital in Iran
.
Sci Total Environ
;
725
:
138401
. doi:10.1016/j.scitotenv.2020.138401.

Google Scholar

Crossref
Search ADS

PubMed

WorldCat

Greenhalgh
T
,
Jimenez
JL
,
Prather
KA
et al. (
2021
)
Ten scientific reasons in support of airborne transmission of SARS-CoV-2
.
Lancet
;
397
:
1603
–
5
.

Google Scholar

Crossref
Search ADS

PubMed

WorldCat

Guo
ZD
,
Wang
ZY
,
Zhang
SF
, et al. (
2020
)
Aerosol and surface distribution of severe acute respiratory syndrome
coronavirus 2 in hospital wards, Wuhan, China, 2020
.
Emerg Infect Dis
;
26
:
1586
–
91
.

Google Scholar

Crossref
Search ADS

WorldCat

Jonker
L
,
Linde
KJ
,
De Hoog
MLA
et al. (
2022
)
SARS-CoV-2 outbreaks in secondary school settings in The Netherlands during fall
2020; silent circulation
.
MedRxiv
2022.05.02.22273861. doi: 10.1101/2022.05.02.22273861.

Google Scholar

OpenURL Placeholder Text

WorldCat

van Kampen
JJA
,
van de Vijver
DAMC
,
Fraaij
PLA
et al. (
2021
)
Duration and key determinants of infectious virus shedding in hospitalized
patients with coronavirus disease-2019 (COVID-19)
.
Nat Commun
;
12
:
267
. doi:10.1038/s41467-020-20568-4.

Google Scholar

Crossref
Search ADS

PubMed

WorldCat

Kluytmans-Van Den Bergh
MFQ
,
Buiting
AGM
,
Pas
SD
et al. (
2020
)
Prevalence and clinical presentation of health care workers with symptoms of
coronavirus disease 2019 in 2 Dutch hospitals during an early phase of the
pandemic
.
JAMA Netw Open
;
3
:
e209673
. doi: 10.1001/jamanetworkopen.2020.9673.

Google Scholar

Crossref
Search ADS

PubMed

WorldCat

Lane
MA
,
Brownsword
EA
,
Babiker
A
et al. (
2021
)
Bioaerosol sampling for severe acute respiratory syndrome coronavirus 2
(SARS-CoV-2) in a referral center with critically ill coronavirus disease 2019
(COVID-19) patients March-May 2020
.
Clin Infect Dis
;
73
:
e1790
–
94
.

Google Scholar

Crossref
Search ADS

PubMed

WorldCat

Lednicky
JA
,
Lauzard
M
,
Fan
ZH
et al. (
2020
)
Viable SARS-CoV-2 in the air of a hospital room with COVID-19 patients
.
Int J Infect Dis
;
100
:
476
–
82
.

Google Scholar

Crossref
Search ADS

PubMed

WorldCat

Lindsley
WG
,
Blachere
FM
,
Thewlis
RE
et al. (
2010
)
Measurements of airborne influenza virus in aerosol particles from human coughs
.
PLoS One
;
5
:
e15100
. doi:10.1371/journal.pone.0015100.

Google Scholar

Crossref
Search ADS

PubMed

WorldCat

Liu
Y
,
Ning
Z
,
Chen
Y
, et al. (
2020
)
Aerodynamic analysis of SARS-CoV-2 in two Wuhan hospitals
.
Nature
;
582
:
557
–
60
.

Google Scholar

Crossref
Search ADS

PubMed

WorldCat

Martin
MA
,
Koelle
K
. (
2021
)
Comment on ‘genomic epidemiology of superspreading events in Austria reveals
mutational dynamics and transmission properties of SARS-CoV-2’
.
Sci Transl Med
;
13
:
eabh1803
. doi:10.1126/scitranslmed.abh1803.

Google Scholar

Crossref
Search ADS

PubMed

WorldCat

Masoumbeigi
H
,
Ghanizadeh
G
,
Arfaei
RY
et al. (
2020
)
Investigation of hospital indoor air quality for the presence of SARS-Cov-2
.
J Environ Health Sci Eng
;
18
:
1259
–
63
. doi: 10.1007/s40201-020-00543-3.

Nannu Shankar
S
,
Witanachchi
CT
,
Morea
AF
et al. (
2022
)
SARS-CoV-2 in residential rooms of two self-isolating persons with COVID-19
.
J Aerosol Sci
;
159
:
105870
. doi: 10.1016/j.jaerosci.2021.105870.

Google Scholar

Crossref
Search ADS

PubMed

WorldCat

National Institute for Public Health and the Environment, The Netherlands
(
2021
)
Coronadashboard.
Available at
https://coronadashboard.rijksoverheid.nl/landelijk/verpleeghuiszorg. Accessed
24 January 2022
.

National Institute for Public Health and the Environment, The Netherlands
(
2022
)
Varianten van Het Coronavirus SARS-CoV-2.
Available at https://www.rivm.nl/coronavirus-covid-19/virus/varianten. Accessed
24 January 2022
.

Nicholson
MD
,
Endler
L
,
Popa
A
et al. (
2021
)
Response to comment on ‘Genomic Epidemiology of Superspreading Events in Austria
Reveals Mutational Dynamics and Transmission Properties of SARS-CoV-2.’
Sci Transl Med
;
13
:
eabj3222
. doi:10.1126/scitranslmed.abj3222.

Google Scholar

Crossref
Search ADS

PubMed

WorldCat

Noss
I
,
Wouters
IM
,
Visser
M
et al. (
2008
)
Evaluation of a low-cost electrostatic dust fall collector for indoor air
endotoxin exposure assessment
.
Appl Environ Microbiol
;
74
:
5621
–
27
.

Google Scholar

Crossref
Search ADS

PubMed

WorldCat

Popa
A
,
Genger
JW
,
Nicholson
MD
et al. (
2020
)
Genomic epidemiology of superspreading events in Austria reveals mutational
dynamics and transmission properties of SARS-CoV-2
.
12
:
eabe2555
. doi:10.1126/scitranslmed.abe2555.

de Rooij
MMT
,
Hakze-Van der Honing
RW
,
Hulst
MM
et al. (
2021
)
Occupational and environmental exposure to SARS-CoV-2 in and around infected
mink farms
.
Occup Environ Med
;
78
:
893
–
9
. doi:10.1136/oemed-2021-107443.

Google Scholar

Crossref
Search ADS

PubMed

WorldCat

Santarpia
JL
,
Rivera
DN
,
Herrera
VL
et al. (
2020
)
Aerosol and surface contamination of SARS-CoV-2 observed in quarantine and
isolation care
.
Sci Rep
;
10
:
12732
. doi:10.1038/s41598-020-69286-3.

Google Scholar

Crossref
Search ADS

PubMed

WorldCat

Schuit
E
,
Veldhuijzen
IK
,
Venekamp
RP
et al. (
2021
)
Supplementary appendix of Diagnostic accuracy of rapid antigen tests in
asymptomatic and presymptomatic close contacts of individuals with confirmed
SARS-CoV-2 infection: cross sectional study
.
BMJ
;
374
:
n1676
. doi:10.1136/bmj.n1676.

Google Scholar

PubMed
OpenURL Placeholder Text

WorldCat

Semelka
CT
,
Ornelles
DA
,
O’Connell
NS
et al. (
2021
)
Detection of environmental spread of SARS-CoV-2 and associated patient
characteristics
.
Open Forum Infect Dis
;
8
:
ofab107
. doi:10.1093/ofid/ofab107.

Google Scholar

Crossref
Search ADS

PubMed

WorldCat

Sikkema
RS
,
Pas
SD
,
Nieuwenhuijse
DF
et al. (
2020
)
COVID-19 in health-care workers in three hospitals in the south of the
Netherlands: a cross-sectional study
.
Lancet Infect Dis
;
20
:
1273
–
80
.

Google Scholar

Crossref
Search ADS

PubMed

WorldCat

Stohr
JJJM
,
Wennekes
M
,
van der Ent
M
et al. (
2020
)
Clinical performance and sample freeze-thaw stability of the Cobas®6800
SARS-CoV-2 assay for the detection of SARS-CoV-2 in oro-/nasopharyngeal swabs
and lower respiratory specimens
.
J Clin Virol
;
133
:
104686
. doi:10.1016/j.jcv.2020.104686.

Google Scholar

OpenURL Placeholder Text

WorldCat

Vihta
KD
,
Pouwels
KB
,
Peto
TEA
(
2022
)
Omicron-associated changes in SARS-CoV-2 symptoms in the United Kingdom
.
Clin Infect Dis
;
ciac613
. doi:10.1093/cid/ciac613.

Google Scholar

OpenURL Placeholder Text

WorldCat

Vosoughi
M
,
Karami
C
,
Dargahi
A
et al. (
2021
)
Investigation of SARS-CoV-2 in hospital indoor air of COVID-19 Patients’ ward
with Impinger method
.
Environ Sci Pollut Res
;
28
:
50480
–
88
.

Google Scholar

Crossref
Search ADS

WorldCat

WHO, and World Health Organization
(
2020
)
Surface Sampling of Coronavirus Disease (COVID-19): a Practical “How to”
Protocol for Health Care and Public Health Professionals
. Available at https://apps.who.int/iris/handle/10665/331058. Accessed 24
January 2022.

Google Scholar

Google Preview

OpenURL Placeholder Text

WorldCat

COPAC

Zhang
XS
,
Duchaine
C
,
Bruchési
C
et al. (
2020
)
SARS-CoV-2 and health care worker protection in low-risk settings: a review of
modes of transmission and a novel airborne model involving inhalable particles
.
Clin Microbiol Rev
;
34
:
e00184
–
20
. doi: 10.1128/CMR.00184-20.

© The Author(s) 2022. Published by Oxford University Press on behalf of the
British Occupational Hygiene Society.
This is an Open Access article distributed under the terms of the Creative
Commons Attribution License (https://creativecommons.org/licenses/by/4.0/),
which permits unrestricted reuse, distribution, and reproduction in any medium,
provided the original work is properly cited.
© The Author(s) 2022. Published by Oxford University Press on behalf of the
British Occupational Hygiene Society.

Download all slides

SUPPLEMENTARY DATA

wxac056_suppl_Supplementary_Material - docx file

CITATIONS

2
CITATIONS

VIEWS

661

ALTMETRIC

More metrics information
×

EMAIL ALERTS

Article activity alert
Advance article alerts
New issue alert
Receive exclusive offers and updates from Oxford Academic

RECOMMENDED

1. Contamination of Air and Surfaces in Workplaces with SARS-CoV-2 Virus: A
Systematic Review
John W Cherrie et al., Annals of Work Exposures and Health
2. Distribution of airborne SARS-CoV-2 and possible aerosol transmission in
Wuhan hospitals, China
Jia Hu et al., National Science Review, 2020
3. Feasibility of a High-Volume Filter Sampler for Detecting SARS-CoV-2 RNA in
COVID-19 Patient Rooms
Amanda M Wilson et al., Annals of Work Exposures and Health

1. Presence of SARS-CoV-2 RNA in human corneal tissues donated in Italy during
the COVID-19 pandemic
Stefano Ferrari et al., Open Ophthalmology, 2022
2. Characterization of Specific Humoral Immunity in Asymptomatic SARS-CoV-2
Infection
Yingying Deng et al., Infectious Diseases & Immunity, 2021
3. Age-Related Susceptibility of Ferrets to SARS-CoV-2 Infection
J Virol, 2021

I consent to the use of Google Analytics and related cookies across the TrendMD
network (widget, website, blog). Learn more
Yes No

academic.oup.com Open in urlscan Pro 52.224.90.245 Public Scan

Form analysis 1 forms found in the DOM

GET /Citation/Download

Text Content

academic.oup.com Open in urlscan Pro
52.224.90.245 Public Scan

Form analysis
1 forms found in the DOM