Pone 0178007 PDF

RESEARCH ARTICLE
A scoping review on bio-aerosols in

healthcare and the dental environment
Charifa Zemouri*, Hans de Soet, Wim Crielaard, Alexa Laheij
Department of Preventive Dentistry, Academic Centre for Dentistry Amsterdam, University of Amsterdam &
Vrije Universiteit Amsterdam, Amsterdam, The Netherlands
* c.zemouri@acta.nl
Abstract
a1111111111 Background
a1111111111
a1111111111 Bio-aerosols originate from different sources and their potentially pathogenic nature may
a1111111111 form a hazard to healthcare workers and patients. So far no extensive review on existing evi-
a1111111111 dence regarding bio-aerosols is available.
Objectives
This study aimed to review evidence on bio-aerosols in healthcare and the dental setting.
OPEN ACCESS
The objectives were 1) What are the sources that generate bio-aerosols?; 2) What is the
Citation: Zemouri C, de Soet H, Crielaard W, Laheij
microbial load and composition of bio-aerosols and how were they measured?; and 3) What
A (2017) A scoping review on bio-aerosols in
healthcare and the dental environment. PLoS ONE is the hazard posed by pathogenic micro-organisms transported via the aerosol route of
12(5): e0178007. https://doi.org/10.1371/journal. transmission?
pone.0178007
Editor: Dongsheng Zhou, Beijing Institute of

Microbiology and Epidemiology, CHINA Methods
Received: December 5, 2016 Systematic scoping review design. Searched in PubMed and EMBASE from inception to
09-03-2016. References were screened and selected based on abstract and full text accord-
Accepted: May 6, 2017
ing to eligibility criteria. Full text articles were assessed for inclusion and summarized. The
Published: May 22, 2017
results are presented in three separate objectives and summarized for an overview of
Copyright: © 2017 Zemouri et al. This is an open evidence.
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and Results
reproduction in any medium, provided the original
author and source are credited. The search yielded 5,823 studies, of which 62 were included. Dental hand pieces were
found to generate aerosols in the dental settings. Another 30 sources from human activities,
Data Availability Statement: All relevant data are
within the paper and its Supporting Information interventions and daily cleaning performances in the hospital also generate aerosols. Fifty-
files. five bacterial species, 45 fungi genera and ten viruses were identified in a hospital setting
Funding: The author(s) received no specific and 16 bacterial and 23 fungal species in the dental environment. Patients with certain risk
funding for this work. factors had a higher chance to acquire Legionella in hospitals. Such infections can lead to
Competing interests: The authors have declared irreversible septic shock and death. Only a few studies found that bio-aerosol generating
that no competing interests exist. procedures resulted in transmission of infectious diseases or allergic reactions.
PLOS ONE | https://doi.org/10.1371/journal.pone.0178007 May 22, 2017 1 / 25

A scoping review on bio-aerosols in healthcare and the dental environment
Conclusion
Bio-aerosols are generated via multiple sources such as different interventions, instruments
and human activity. Bio-aerosols compositions reported are heterogeneous in their microbi-
ological composition dependent on the setting and methodology. Legionella species were
found to be a bio-aerosol dependent hazard to elderly and patients with respiratory com-
plaints. But all aerosols can be can be hazardous to both patients and healthcare workers.
Introduction
Aerosols are defined as liquid or solid particles suspended in the air by humans, animals,
instruments, or machines. Bio-aerosols are aerosols consisting of particles of any kind of
organism [1, 2]. The characteristics of bio-aerosols differ depending on environmental influ-
ences such as humidity, air flow, and temperature. Aerosols, which are responsible for the
transmission of airborne micro-organisms by air, consist of small particles named droplet
nuclei (1–5μm) or droplets (>5μm). Droplet nuclei can stay airborne for hours, transport over
long distances and contaminate surfaces by falling down [1]. It has been proven that droplets
can contaminate surfaces in a range of 1 meter (3ft) [2]. The droplets are capable of penetrat-
ing deep into the alveoli, offering a potential route of infection [3]. The susceptibility of acquir-
ing an infectious agent is determined by factors such as: virulence; dose; and pathogenicity of
the micro-organism; and the host’s immune response [3–5]. Humans generate bio-aerosols by
talking, breathing, sneezing or coughing [1]. Based on the infectious status of a person, the
bio-aerosols are proven to contain influenza or rhinoviruses [6, 7], Mycobacterium tuberculosis
[3], Staphylococcus aureus, Varicella Zoster Virus, Streptococcus spp. or Aspergillus spp. [8].
Moreover, bio-aerosols can be generated by devices such as ventilation systems, showers and
high energetic instruments running on tap water. Showers and instruments cooled with tap
water are able to spread environmental microbes such as Legionella spp. or other bacteria origi-
nating from water sources or water derived biofilms from tubing [4, 5, 9].
Due to the nature of their profession, healthcare workers (HCWs) are at higher risk to ac-
quire pathogenic micro-organisms. Their risk of exposure is in line with the infectious nature
of their patients, interventions or instruments that produce bio-aerosols. HCWs working in
wards with patients suffering from pneumonia, who produce high virulence bio-aerosols, or
HCWs exposed to bio-aerosol sources in dental practices, are at higher risk for developing dis-
ease or allergies [10, 11]. According to a risk assessment study, conducted in a hospital with
HCWs exposed to high risk procedures, a risk ratio (RR) of 2.5 was found for acquiring viral
or bacterial infection [12]. Multiple studies have found that HCWs were at higher risk to ac-
quire an infectious disease, observing a high serological status of Legionella spp. and high rates
of asymptomatic tuberculosis in dental practitioners and hospital staff [10, 13–15]. It is plausi-
ble that other diseases could also be acquired via bio-aerosols. Finally, evidence shows that
patients with cystic fibrosis, who are immunosuppressed, are highly susceptible to airborne
agents like Pseudomonas spp. [16]. Knowing this, we can assume that bio-aerosols with a high
load of micro-organisms are a threat to immunocompromised patients suffering from leuke-
mia, psoriasis, aplastic anemia and others [17]. Thus, the risk of acquiring pathogenic agents
by bio-aerosols may be a hazard to both healthy and immunosuppressed patients as well as to
HCWs.
To our knowledge, no detailed summary of the evidence regarding bio-aerosols in dental
and hospital settings is available. Therefore, we chose to perform a scoping review on the

present body of evidence regarding bio-aerosols. This results in an up-to-date summary of the
literature, allowing us to make recommendations for future research by identifying gaps in
current knowledge, and to underline the risks for HCW and immunocompromised. Since this
is a scoping review, our objectives are broad and cover three areas concerning bio-aerosols in
hospital and dental settings [18, 19]:
• What are the sources that generate bio-aerosols?
• What is the microbial load and composition of bio-aerosols and how were they measured?
• What is the hazard posed by pathogenic micro-organisms transported via the aerosol route
of transmission?
Methods
Design and search strategy
A scoping review was performed systematically according to the PRISMA statement for trans-
parent reporting of systematic reviews and meta-analysis [20] and JBI Briggs Reviewers Man-
ual [21] (see S1 PRISMA checklist). Three search strings were run in PubMed and EMBASE
from inception to 09-03-2016. In PubMed the following strings were combined: Hospitals
[Mesh] OR hospital OR hospitals OR "health care category" [Mesh] OR "health care" OR
"Cross infection" [Mesh] OR "cross infection" OR cross-infection OR nosocomial OR "health
facilities"[Mesh] OR "health facility" OR "health facilities" AND aerosols [Mesh] OR aerosol
OR aerosols OR bioaerosol OR bio-aerosol OR "bio aerosol" OR bio-aerosols OR "bio aerosols"
AND bacteria [Mesh] OR bacteria OR bacterial OR bacteremia OR bacteraemia OR sepsis OR
septicaemia OR septicemia OR virus OR viruses OR viral OR viridae OR viral OR viruses
[Mesh] OR Amoebozoa [Mesh] OR amoebozoa OR amoebe OR amoebas OR amoebic OR
fungi [Mesh] OR fungus OR fungal OR fungi OR fungating OR parasites [Mesh] OR parasitic
OR parasite OR parasites OR parasitemia OR parasitemias OR “micro organism” OR “micro
organisms” microorganism OR microorganisms OR micro-organism OR micro-organisms
OR “health care associated infections” OR infections OR infection OR infectious. For EMBASE
we used the following strings combined: ‘hospitals/exp OR hospitals OR (health AND care
AND category) OR healthcare OR ‘cross infection’OR ‘health facility’ OR ‘health facilities’ AND
Infection/exp OR microorganism/exp OR fungi/exp OR virus/exp OR sepsis/exp OR bacteria/
exp AND Aerosol OR aerosols/exp OR bioaerosol OR bio-aerosol OR bioaerosols OR aerosols.
Screening process and inclusion criteria

References yielded from the search strategy were imported in Covidence, an online web appli-
cation for screening systematic reviews, and duplicates were removed. C.Z. and A.L. screened
and scored the relevance of the hits independently, based on their title and abstract. The full
text manuscripts were retrieved via Endnote, Google, Research Gate or by addressing the cor-
responding and/or first author. Subsequently, the studies were assessed on their eligibility for
inclusion based on the full text. A study was included for final data extraction and summary
when it met one of the following criteria: bio-aerosol composition; pathogenicity; sources; con-
ducted in healthcare or the dental setting; published in English, German, French, Spanish or
Dutch. Discussion papers, letters to the editor, animal studies, protocols, prevention of bio-
aerosols, technical studies, reviews without pooled data, narrative reviews, development of
drug therapy, or studies conducted in other settings besides healthcare were excluded. Addi-
tionally, a reference check and search through grey literature was conducted and included in
the flowchart termed ‘snowballing’.

Data extraction and summary

Data on the origin of bio-aerosols was categorized based on sources. Studies on the microbial
composition of the bio-aerosols were summarized based on the colony forming units (CFU).
References that reported sampling time were recalculated for a sampling time of 10 minutes
and finally Log-transformed to make comparison possible between studies. These studies are
presented in figures. References not reporting sampling time were not summarized and are
presented in the study of characteristics table. The micro-organisms reported in individual
studies were summarized per type of organism and setting. Potential hazard for patients and
HCWs were summarized narratively.
Results
A total of 5823 studies were retrieved, of which 678 duplicates and 4797 irrelevant studies were
removed. After reading 311 abstracts, 201 full text studies were assessed for eligibility. This
eventually resulted in 62 studies including references from snowballing (see Fig 1. PRISMA
flowchart).
Generation of bio-aerosols
One study reported solely on the generation of bio-aerosols [22]. Therefore, we extracted data
on the generation of bio-aerosols from papers selected for the other objectives [23–44]. The
sources of bio-aerosols in dental clinics were: ultrasonic scalers, high speed hand pieces, air
turbines, three in one syringes, and air water syringes. Studies conducted in hospitals reported
Fig 1. PRISMA flowchart.

https://doi.org/10.1371/journal.pone.0178007.g001

30 different bio-aerosol generating sources. Humans produced aerosols by coughing, and

sneezing. Patients with cystic fibrosis positive for Burkoderia cepacia were also capable of pro-
ducing pathogenic aerosols. Interventions conducted by HCWs that produced aerosols were:
colonoscopy, tracheal intubation, suction before and after intubation, manipulation oxygen
mask, bronchoscopy, non-invasive ventilation, insertion of nasogastric tube, defibrillation,
chest physiotherapy, and washing the patient. Bed making, ward rounds, tea trolley round,
activity at bed, floor mopping, moving furniture, lunch time, drugs round, evening meal, vac-
uum cleaner, toilet use, cold-mist humidifier, shower, cleaning patients room and the neb-
ulizer were found to be other activities in a hospital to produce aerosols [22].
Hospital environment
Thirty-one studies analyzed the microbial composition of bio-aerosols in the hospital environ-
ment [11, 30, 35–37, 39, 41–65]. The studies combined identified a total of 111 organisms by
using culture techniques (see Table 1 for overview of micro-organisms identified and Table 2
study characteristics hospital setting). Fifty-six bacterial species (23 Gram-negative and 32
Gram-positive; 1 mycobacteria), 45 fungal genera and ten viral species were identified[11, 30,
35–37, 39, 41–52, 54, 56–66] Most bacteria originated from human skin or the human gut, the
environment or water. The identified viruses originated from the human respiratory tract. The
methods for collecting air samples from the bio-aerosols and the methods for culturing micro-
organisms were heterogeneous. The method most frequently used to actively collect micro-
organisms was the Andersen air sampler (N = 9). Four studies used passive collection of
micro-organisms by placing Petri dishes with agar. In all studies, 21 different culture methods
were used, wherefrom Tryptic soy agar (N = 7) was most frequently used.
Fourteen studies analyzed the bacterial load of the bio-aerosols [11, 39, 41, 42, 45–47, 50,
55, 58, 60, 61, 64, 65]. The mean Log-10 of CFU/m3 ranged from 0.8 to 3.8 (see Fig 2). Addi-
tionally, five studies analyzed the bio-aerosol contamination before and/or after treatment,
intervention or of a room when a patient with an infectious disease was present. The measured
bacterial or fungal load ranged from Log 0.6–4.2 at baseline to Log 1.2–4.3 after the second
measurement (see Fig 3) [30, 35, 43, 56, 57]. Seven studies reported on the fungal load in bio-
aerosols during the day when patients were present in a hospital room. Fungal loads ranged
from Log 0.8–3.5 CFU/m3 in various hospital wards [45, 47, 50, 56, 59, 61, 66]. Multiple studies
quantified the air in patient specific areas or via specific methods.
Two studies identified multiple viruses in bio-aerosols after patients with symptoms of a
cold coughed, however both studies did not report on the viral load [51, 62]. Viral loads in the
bio-aerosol ranged between Log 2.2 plaque forming units /m3 in the air of an infant nursery
positive for RSV and Log 5.5 PFU/m3 in the air contaminated by patients positive for Influenza
A virus [52, 54]. Another study reported the RNA copy/L and found Log 3.3–5.2 in aerosols
produced by patients positive for Influenza A virus [33].
Dental environment
Seventeen studies analyzed the microbial composition of dental clinics [23–29, 67–76]. The
studies cumulatively identified 38 types of micro-organisms by using culture techniques (see
Table 3 for complete overview of micro-organisms identified and Table 4 for study characteris-
tics in dental setting). Wherefrom nineteen bacteria (7 Gram-negative and 12 Gram-positive)
and 23 fungal genera were detected. The bacteria originated from water, human skin and the
oral cavity. None of the included studies looked for viruses or parasites. Similar to the hospital
setting, the active Andersen air sampler (N = 4) and the passive culturing method by placing
Petri dishes with agar (N = 6) were the most frequent used air sampling techniques. Thirteen

Table 1. Overview of micro-organisms identified in hospital setting.

Bacteria N = 56
Gram negative Gram positive
Achromobacter Moraxella Bacillus cereus Rodococcus spp Staphylococcus saprophyticus
xylosoxidans
Acinetobacter baumannii Neisseria spp Bacillus spp Staphylococcus aureus Staphylococcus schleiferi
Acinetobacter Ochrobactrum anthropic Bacillus sutilis Staphylococcus auriculans Staphylococcus sciuri
calcoaceticus
Branhamella catarrhalis Pantoea agglomerans Brevibacterium casei Staphylococcus capitis Staphylococcus werneri
Burkholderia cepacia Proteus Clostridium difficile Staphylococcus caprae Staphylococcus xylosus
Enterobacter spp Pseudomonas aeruginosa Corynebacterium Staphylococcus Sterptococcus pyogens
chromogenes
Escherichia coli Pseudomonas fluorescens Diphtheroid spp Staphylococcus cohnii Streptococcus spp.
Flavobacterium spp Pseudomonas putida Kocuria kristinae Staphylococcus epidermidis Viridans Streptococci
Klebsiella oxytoca Rahnella aquatilis Kocuria varians Staphylococcus Other strain:Mycobacterium
haemolyticus tuberculosis
Klebsiella pneumonia Shigella Micrococcus luteus Staphylococcus hominis
Legionella pneumophila Strenotrophomonas Micrococcus lylae Staphylococcus lentus
maltohilia
Neisseria flavescens Micrococcus spp Staphylococcus
saprophyticus
Viruses N = 10
Human metapneumovirus Human adenovirus Influenza A H1N1 Influenza B virus Influenza virus
Parainfluenza virus 1–3 Picornavirus Respiratory syncytial Rhinovirus Toque teno virus
virus
Parasites N = 0
None reported
Fungi N = 45
Absidia spp Candida spp Epicoccum spp Nigrospora spp Scopulariopsos spp
Acremonium spp Chaetomium spp Exserohilum spp Paecilomyces spp Sepedonium spp
Alternaria spp Chrysonilia spp Fusarium spp Penicillium spp Sporotrichum
Aspergillosis fumigatus Chrysoporium spp Geotrichum candidum Phoma spp Stemphylium spp
Aspergillus flavus Cladosporium spp Geotrichum spp Pithomyces spp Syncephalastrum spp
Aspergillus niger Conidiobulus spp Gliocladium spp Rhinocladiella spp Trichoderma album
Aspergillus spp Curvalaria spp Monilia spp Rhizopus nigricans Trichosporon
Aureobasidium spp Dactylaria spp Mucor spp Scedosporium spp Ulocladium spp
Bipolaris spp Emonsia spp Myclia sterilia Scopulariopsis brevicaulis Verticillium spp
https://doi.org/10.1371/journal.pone.0178007.t001
different culture methods were used to identify the collected micro-organisms, of which Tryp-
tic soy agar (N = 3) and blood agar (N = 3) were used most often.
The mean bacterial load in the bio-aerosols ranged from Log 1–3.9 CFU/m3 (see Fig 4).
Furthermore, six studies analyzed the bio-aerosol contamination before and after treatment.
The bacterial or fungal load ranging from Log -0.7–2.4 CFU/m3 at baseline and from Log
1–3.1 CFU/m3 after treatment (see Fig 5) [25, 68, 71, 72]. Only one study reported on the rela-
tion between the distance from the bio-aerosol generating source and the bacterial load. They
found a higher bacterial load in the bio-aerosols at 1.5 meter from the oral cavity of the patient
than in the bio-aerosols within 1 meter from the patient [26]. One study screened for B. cepacia
and one screened for M. tuberculosis, however both studies could not retrieve these organisms
after regular patient treatment [24, 28].

Table 2. Study characteristics hospital setting.

Study Set up Findings
Anderson 1996 Setting: Pediatric hematology and oncology ward Fungi:Aspergillosis fumigatus
Sampling method: Air dust sampler L100; 100L/min; 10 min Before: 24 CFU/m3 After: 62 CFU/m3
before and after vacuum cleaning; 0.5m above cleaner. Fungal
isolates by morphology. Sampling: Before and after vacuuming
Augustowska Setting: Pneumological ward, hospital Mean monthly CFU/m3 range of airborne bacteria:257.1–436.3Mean
2006 monthly CFU/m3 range of fungi:9.9–96.1
Sampling method Air sampled with a custom-designed particle- Bacteria:
sizing slit sampler; 20L/min; daily at 9:00 and 13:00h. Blood and Gram positive cocci: 34.4–46.4% à Staphylococcus epidermidis;
Sabouraud agar. Micrococcus; Streptococcus.
Gram negative: 11.8–27.5%à Flavobacterium spp; Acinetobacter
calcoaceticus; Pantoea agglomerans; Escherichia coli; Enterobacter
spp; Klebsiella oxytoca; Pseudomonas auruginosa; Branhamella
catarrhalis; Neisseria flavescens; Corynebacterium; Rodococcus
spp; Bacillus spp.Fungi: 7.6–42.5%Aspergillus fumigatus: 77%
Aspergillus niger; Aspergillus flavus; Aspergillus spp; Penicillium
spp; Geotrichum candidum; Trichoderma album; Mucor spp;
Rhizopus nigricans.
Best, 2012 Setting: Toilet, hospital Mean CFU:
Sampling method: Air sampled using AirTrace Environmental After flushing: 36Recovery of C. difficile mean CFU:
portable sampler placed at toilet seat height; 250-500L, 10cm Toilet lid closed vs open 0–30 min: 4 vs 1630–60 min: 4 vs 360–90
above seat and 25 cm at handle height; 28.3L/min. Selective min: 0 vs 1
agar plate placed around the toilet; placed before flushing and
Bacteria:C. difficile
remained for 90 min.
Cabo Verde, Setting: OT, SW, ES hospital CFU/m3 range bacteria:ES: 240-736SW: 99-495OT: 12–170
2015 Sampling method: Air sampler MAS-100 100L/min; 1m above CFU/m3 range fungiES: 27–933 SW: 1–32 OT: 0–1
floor when possible.Trypic soy agar; malt extract agar; gram Total % bacteriaStaphylococcus aureus, capitis, hominis, epidermis,
staining. werneri: 51%Micrococcus luteus, lylae: 37%Neisseria: 4%
Brevibacterium casei: 1%Shigella: 0.3%Proteus: 2%
Total % fungi
Penicillium spp: 41%Aspergillus spp: 24%Cladosporium spp: 14%
Chrysonilia spp: 5%Chrysoporium spp: 3%Scopulariopsis
brevicaulis: 3%
Chen, 2008 Setting: TB and non TB area; hospital Average concentration:
Sampling method: Air sampled using Nucleipore filter; 20L/min; TB area:3.8 x 103 ± 1.7 x 103 copy/m3
2x4h a day; 1.2–1.5m height. DNA isolation qPCR Non-TB area:3.9 x 10 ± 2.1 x 10 copy/ m3
Emergency department:4.0 x 103 ± 2.6 x 103 copy/m3Ward area
medical department:102 ± 5.5 x 101 copy/m3
Chen, 2007 Setting: TB and Non TB area; Hospital Range concentration:1.43 x 10 copy/m3 to 2.06 x 105 copy/m3
Sampling method: Air sampled using Nucleipore filter; 22L/min;
8h sampling; 1m from patients bed at 1.2–1.5m height. DNA
isolation qPCR
Fekadu, 2015 Setting: MW, SW hospital Mean CFU/m3 (range):
Sampling method: Air samples were taken by passive method. Bacteria: 5583 (3106–9733)
Petri dishes placed 1m above the floor in room’s center. Fungi: 3008 (2123–4168)
Samples collected in the morning and evening time of exposure:
30, 60, 90 min. Nutrient and Sabouraud agar plates.
Fennelly, 2012 Setting: TB and Non TB area; Hospital TB median CFU (range):16 (1–710)
Sampling method: Cough bio-aerosol sampling system method
used to collect bio-aerosols in TB positive patients. Andersen
six-stage sampler with 7H11 agar collection for 5 minutes.
(Continued)

Table 2. (Continued)

Humphreys, Setting: Hospital Bacteria:B. cepacia
1994 Sampling method: CF patients colonized with B. cepacia. Air During stay CFU/m3:Range: 1-158Mean: 32
sampled with Surface Air System air sampler, 900 l for 5 min; After stay CFU/m3:Range: 3-53Mean: NR
100 cm from patient. Samples taken 15 min intervals for one
hour after patient had left the room and 18 h after vacating.
Selective B. cepacia agar medium.
Huynh, 2008 Setting: Laboratory Virus:Influenza virus; para influenza virus; Rhinovirus; Influenza A
Sampling method: Reading aloud (20 min), quiet breathing (20 virus.
min), 20 voluntary coughs over a 3–5 min period in a separate
sampling mask. PCR
Heimbuch, 2016 Setting: Hospital Mean CFU/cm2Mask 1 external layer: 24.15Mask 2 external layer:
3.33
Sampling method: No direct bio-aerosol sampling. Viable Bacteria:Kocuria kristinae, varians; Micrococcus spp.;
bacteria found on mask was measured. Tryptic soy agar; Gram Staphylococcus aureus, S. auriculans, S. capitis, S. caprae, S.
staining. chromogenes, S. cohnii, S. epidermidis, S. haemolyticus, S.
hominis, S. lentus, S. saprophyticus, S. schleiferi, S. sciuri, S.
warneri, S. xylosus; Acinetobacter baumannii; Ochrobactrum
anthropic; Pesudomonas fluorescens /putida; Rahnella aquatilis;
Stenotrophomonas matophilia.
Knibbs, 2014 Setting: Children’s hospital Total mean CFU/m3 (range) per distance:1m: 52.6 (40.9–67.6)2m:
37.3 (28.9–48.0)4m: 24.8 (19.2–32.0)
Sampling method: CF patients colonized with B. cepacia. Cough Total mean CFU/m3 (range) per duration:5 min: 14.6 (11.0–19.2)15
bio-aerosols collected by Andersen Impactor (28.3L/min); min: 11.9 (8.9–15.7)45 min: 7.7 (5.4–11.0)
chocolate bacitracin agar for B. cepacia and isolates by % of subjects positive for bacteria:P. aeruginosa: 100Mucoid P.
RT-PCR. aeruginosa: 78.9Non-mucoid P. aeruginosa: 94.7S. aureus:
26.3Strenotrophomonas maltohilia: 10.5
Subjects positive for fungi (%):Trichosporon: 15.8Aspergillus spp:
15.8Scedosporium spp: 10.5Candida spp.: 5.7
Kulkarni, 2016 Setting: Infant nursing bay, hospital Mean PFU of RSV:315.189; range: 82.600–1.120.000
Sampling method: Air sampled with Westech six-stage Microbial 2h after discharge:6.175.
sampler; 28.3L/min for 30 min; 1m distance from infected infant.
PCR
Virus:RSV
Kumar, 2010 Setting: GW, PW, OT, ICU, hospital Bacteria %:S. aureus: 43.8Escherichia coli: 17.9Klebsiella
Sampling method: Air sampled by passive settling plate pneumonia: 16Sterptococcus pyogens: 13.2Pseudomonas
technique. Nutrient, blood, and MacConkey’s agar 5 min aeruginosa: 8.9
exposure.
Lindsley, 2015 Setting: Laboratory Range 5 to 538 PFU, mean (SD): 142 (125).
Sampling method: Bio-aerosols collected using SKC Virus: Influenza A
BioSampler with 5ml vessel containing viral transport media:
Hank Balanced Salt Solution. qPCR
Li, 2003 Setting: ICU, hospital Range of mean CFU/m3 Fungi: 0–3115
Sampling method: Air was sampled using Andersen six stage Bacteria: 0–423
sampler; 28.3L/min; 1m height. Sampling time 20–30 min.
Tryptic soya and malt extract agar.
Martins-Diniz, Setting: SW, ICU, hospital Mean total fungi CFU/m3
2005 Sampling method: Air samples taken by Andersen sampler. 80L SC morning: 13,362
of air sampled on Sabouraud agar and chloramphenicol culture SC afternoon: 20,939
medium. Samples taking during the morning and immediately
ICU morning: 16.925
after cleaning, late afternoon and end of regular shift, monthly
collections. ICU afternoon: 16,392
(Continued)


Total CFU/m3 SW & ICU morning/afternoon:
Cladosporium spp.: 6,338/16,587 11,587/11,192
Fusarium spp: 2,350/900 514/612
Pencillium spp: 912/813 1,425/950
Chrysosporium spp.: 401/562 637/950
Aspergillus spp.: 362/289 775/413
Aureobasidium spp.: 562/200 238/476
Myclia sterilia; 350/300 64/237
Monilia spp.: 325/100 62/250
Paecilomyces spp.: 89/275 162/175
Curvalaria spp.: 262/200 26/75
Chaetomium spp.: 275/12 75/212
Stemphylium spp.: 162/100 38/63
Rhinocladiella spp.: 75/38 137/0
Exserohilum spp.: 25/0 87/38
Epicoccum spp: 0/75 88/150
Phoma spp.: 100/25 201/125
Alternaria spp.: 26/26 137/88
Nigrospora spp.: 162/25 13/100
Syncephalastrum spp.: 51/87 137/25
Bipolaris spp.: 25/25 0
Dactylaria spp.: 12/0 37/37
Acremonium spp: 25/12 87/26
Conidiobulus spp.: 0 12/112
Verticillium spp.: 12/0 87/0
Gliocladium spp.: 62/37 87/0
Pithomyces spp.: 0/25 100/0
Sepedonium spp.: 0 0
Scopulariopsos spp.: 0/25 25/12
Sporotrichum: 0/12 50/0
Ulocladium spp.: 0/12 0/25
Scedosporium spp.: 25/0 0
Emonsia spp.: 0 0/12
Geotrichum spp.: 12/0 0
Menzies, 2003 Setting: Screening center for TB Average airborne viable CFU/m3 at induction:
Sampling method: Sputum induction by ultrasonic nebulizer for Before: 233
15 min. Samples taken with Andersen six stage sampler 15L/ During: 351
min, at the height of the therapists breathing zone (1.5m height).
After: 106
Sheep blood agar.
Mirhoseini, 2015 Setting: OT, ICU, SW, IM, hospital Total mean CFU/m3:
Sampling method: Air sampled with AGI 12.5L/min 180–240 OT: 396
min. Tryptic soy agar culture. ICU: 222
SW: 537
IM: 524
Total: 420
(Continued)


Mirzai, 2014 Setting: OR, ED, Hospital Total mean CFU/m3 ED & OR:
Sampling method: Air samples taken by eight step Andersen Total ER: 103.88 (33.84)
28.1L/min. Once a month for a year every morning before start Total OR: 63.32 (32.94)
of the shift. Plates at 1m height and 1m from obstacles exposed
for 10 min. Blood, BHI, and McConkey agar. Micrococcus: 14.85/16.09
Streptococcus A: 1.26/2.19
Viridans Streptococci: 2.92/1.72
Pneumococcus: 7.81/3.81
Escherichia coli: 6.91/2.0
Bacillus sutilis: 6.64/1.63
S. aereus: 14.17/10.92
S.epidermis: 10.95/5.72
S. saprophyticus: 11.35/5.45
Bacilluscereus: 7.14/1.73
Diphtheroid spp: 5.28/2.27
Pseudomonas spp: 4/3.47
Klebsiella: 4.19/1.09
Enterobacter: 1.17/0.27
Citrobacter: 0.77/1.62
Branhamla: 0.19/0.36
Bacterial, 20˚C CFU/m3 mean (range):
Conv. Flow morning: 141 (42–325)
Conv. Flow evening: 82 (49–141)
Lam. Flow morning: 25 (0–92)
Lam. Flow evening: 82 (7–233)Bacterial, 30˚C CFU/m3 mean
(range):
Conv. Flow evening:77 (35–170)Lam. Flow morning: 110 (14–572)
Lam. Flow evening: 11 (0–42)Gram negative CFU/m3 mean (range):
Conv. Flow morning:2 (0–14)
Conv. Flow evening: 0
Lam. Flow morning: 0
Lam. Flow evening: 0Fungi CFU/m3 mean (range):
Conv. Flow evening: 38 (0–99)
Lam. Flow morning: 5 (0–21)
Lam. Flow evening: 80 (0–455)
Ortiz, 2009 Setting: General hospital Average 2 years TAC:
Sampling method: Air sampler MAS-100 100L/min; petri dish. OT: 25.6 CFU/m3
Total aerobic count; rose-bengal agar, microscopy and staining.
Sampling: Before and after intervention. 2 years. Plate count MW: 67 CFU/m3
agar; Rose Bengal agar HR: 124.4 CFU/m3 Average 2 years FL:
OT: 0.05 CFU/m3
MW: 6.9 CFU/m3
HR: 10.6 CFU/m3 Fungi:
Aspergillosis fumigatus, flavus: 89%, 11%.
Bacteria:
not specified.
(Continued)


Sudharsanam, Setting: OW, Hospital Total range of bacteria:
2012 45–150 CFU/plate.
Sampling method: Passive air sampling and active by active Total range of fungi: 0–13 CFU/plate
using filter and impinger. Petri dishes at 60–70 cm height, Bacteria:
exposed for 30 min. 3.5L/min of air for 20 min. Samples taken in
multiple months. Blood, Sabouraud’s Dextroser, and Coagulase negative staphylococci; micrococci; Enterobacter;
MacConkey agar. Pseudomonas.
Fungi:
Aspergillus fumigatus; flavus; niger.; Absidia spp.
Stelzer-Braid, Setting: Hospital Virus:
2009 Sampling method: Bio-aerosols collected with face mask. Influenza A; Influenza B; parainfluenza 1, 2, 3, respiratory syncytial
RT-PCR virus, human metapneumovirus, picornavirus.
Thompson, 2013 Setting: Hospital Median RNA copy no/L (IQR): Airway suction: 1.852 (1.543–2.7521)
Sampling method: Air sampled with Glass May-3stage Baseline: 7.913 (2.436–11.613)
impingers at 55L/min at 1m height; 1m from patients head; 40 Bronchoscopy: 148.805 (12.735–284.875)
min collection. RT-PCR.
Intubation: 2.838 (2.838–2.838)Virus:
Influenza A H1N1
Vavricka, 2010 Setting: Endoscopy unit, hospital Mean CFU/m3 (range) with air suction:
Sampling method: Air sampled with MAS-100; 100L/min; before Before: 4 (1–7)
first colonoscopy and end of evening; 30 sec; 1.2m height; 0.3m End: 16 (9–22)
distance. Colombia agar.
Mean CFU/m3 (range) without air suction:
Before: 14 (0–142)
End: 7 (1–88)Bacteria:
Staphylococci spp.
Vélez-Pereira, Setting: ICU, hospital Range mean (SD) CFU/m3:
2014 Sampling method: Air sampled with cascade impactor; 28.3L/ Staphylococcus spp 67.3 (1.7)– 277 (59.2)
min; 1.5m height; mannitol salt; pseudomonas agar. Pseudomonas spp 6.4 (1.7)– 204 (9.2)
Bacteria %:
Staphylococcus spp.: 71.5
Pseudomonas aeruginosa: 64.6
Verani, 2014 Setting: Nephrology, hospital Mean concentration/cm2 (SD):
Sampling method: Air sampled with microflow impactor sampler; Human adenovirus
1,000L for virus and 180L for bacteria sampled; tryptone soy Before disinfection: 349 (51)
agar; samples before and after disinfection toilet. RT-PCR
After disinfection: 1,371 (49)
Total viruses %:
Human adenovirus: 77
Toque teno virus: 15
Norovirus: 0
Combination: 7
Total bacteria %: 41
Before disinfection: 1.57
After disinfection: 1,371 (49)
Wainwright, Setting: Children’s Hospital Voluntary cough range CFU: 0–13,485
2009 Sampling method: Air sampled with Cough bio-aerosol sampling Mean CFU settle plate: 6 (95%CI 3–14)
system and Anderson six stage impactors for 5 min in children Bacteria:
with CF positive for Pseudomonas aeruginosa. Chocolate agar.
Pseudomonas aeruginosa; Strenotrophomonas maltophilia;
Achromobacter xylosoxidans.
(Continued)


Wan, 2011 Setting: OR, hospital Median CFU/m3 (range):
Sampling method: Air sampled with Andersen one-stage viable Transplantation room: 76.0 (9–477)
impactor at 28.3L/min volume for 3 min; 1.2–1.5m height; 1.5m Trauma room: 121.5 (13–756)
from operation tables. Tryptic soy agar.
Cardiovascular surgery: 13 (0–163)
Colon surgery: 73.5 (0–567)
Orthopedic surgery: 89 (4–243)
Bacteria % in transplantation, trauma, cardiovascular surgery, rectal
and orthopedic surgery room:
Bacillus spp: 32; 24; 16; 16; 34
Micrococcus spp: 35; 25; 26; 39; 9
Staphylococcus spp: 16; 20; 33; 26; 23
Acinetobacter spp: 0; 8; 3; 0; 6
Moraxella spp: 1; 0; 6; 0; 0;
Pseudomonas spp: 1; 0; 0; 0; 0
Woo, 1986 Setting: Hospital Distance (cm) and colonies/plate:
Sampling method: Air sampled by passive technique placing Adaptor / adaptor + extension:
plates in different places within a hospital shower. Buffered 0: 3 / 3
charcoal yeast extract agar.
1: 10 / 5
4: 7 / 5
10: 4 / 2
20: 2 / 1
Bacteria:
Legionella pneumophila
Abbreviation: AMHB = aerobic mesophilic heterotrophic bacteria; BHI = blood heart infusion; CFU = Colony forming units; CF = cystic fibrosis;
cm = centimeters; ED = emergency department; ER = emergency room; ES = emergency service; FL = fungal load; GW = general ward; HR = hospital
room; IM = internal medicine; IQR = inter quartile range; L = liters; min = minutes; m = meters; MW = maternity ward; NR = not reported;
NTM = nontuberculous mycobacteria; OR = operation room; OT = operation theatre; OW = operation ward; PFU = plaque forming units; PW = pulmonary
ward; RSV = respiratory syntical virus; SC = surgical center; SD = standard deviation; SW = Surgical Ward; TAC = total aerobic count; TB = tuberculosis;
qPCR = quantitative polymerase chain reaction.
Hazard of a bio-aerosol
Seven studies reported on the hazard of micro-organisms to HCWs and/or patients, see
Table 5 study characteristics hazard in healthcare and the dental setting [12, 31, 34, 45, 77–79]
Three studies looked into the risks for patients when exposed to Legionella pneumophila con-
taining sources that may produce bio-aerosols [34, 38, 78]. They reported that cooling towers,
air conditioning or mechanical ventilation systems could be a source of L. pneumophila. Kool
et al. concluded that patients had an increased risk to acquire L. pneumophila in hospitals
when they used corticosteroids (OR = 13; 95CI% 1.6–102) and when intubated (OR = 10; 95%
CI 1.3–73) [34]. Another study identified smoking, drinking alcohol, having chronic lung dis-
ease and cancer as risk factors for getting an infection with L. pneumophila [78]. For the dental
clinic there is one case study reported that reported of irreversible septic shock and died after
two days in a patient that was infected with L. pneumophila [79].
One systematic review reported on the pooled odds ratio (OR) for the transmission and
exposure to Severe Acute Respiratory Syndrome (SARS) in HCWs during bio-aerosol generat-
ing procedures. Tracheal intubation (OR = 6.6; 95%CI 2.3–18.9) and noninvasive ventilation

Fig 2. Bacterial or fungal loads in mean Log-10 CFU/m3 in hospitals. * = passive sampling method; #
active sampling method.
Fig 3. Bacterial or fungal loads in mean Log-10 CFU/m3 in hospitals, measured twice. * = passive
sampling method; # active sampling method.

Table 3. Complete overview micro-organisms identified in the dental setting.

Bacteria N = 19
Gram negative Gram positive
Acinetobacter wolffii Staphylococcus capitis Staphylococcus Micrococcus Diphteroids
chromogenes luteus
Legionella spp. Staphylococcus lentus Staphylococcus Micrococcus spp. Corynebacteria
haemolyticus
Pseudomonas aureus Staphylococcus xylosus Staphylococcus Micrococcus lylae Bacillus spp.
epidermidis
Staphylococcus aureus Staphylococcus fominis Bacillus pumilus Actinomycetes
Viruses N = 0
None reported
Parasites N = 0
None reported
Fungi N = 23
Alternaria alternata Aspergillus flavus Cladosporium cucumerinum Geotrichum spp Stemphylium spp
Alternaria brassicicola Aspergillus fumigatus Cladosporium ramotenellum Monocillim indicum Stemphylium spp
Alternaria citri Aspergillus niger Cladosporium Monodictys glauca Ulocladium alternariae
sphaerospermum
Arthrinium Botrytis spp Cladosporium spp Pencillium spp
phaesospermum
Aspergillus Cladosporium Cladosporium spongiosum Penicillium chrysogenum
cladosporiodias
(OR = 3.1; 95%CI 1.4–6.8) were risk factors for acquiring SARS. Other bio-aerosol generating
interventions such as manipulation of an oxygen mask were not significant risk factors [31].
Another study calculated that the risk ratio for acquiring clinical respiratory infections was 2.5
(95%CI 1.3–6.5) for HCWs performing a high risk procedure [12]. Augustowska et al. studied
the effect of bacteria and fungi on asthmatic patients. They reported a decrease in maximum
breathing capacity due to the increase of bacterial or fungal load in the air [45].
A case-study in a dental clinic described the risk of acquiring Herpes Simplex Virus (HSV)-
1 for the dentist and the dental hygienists when they treated a patient with active HSV-1. One
member of the treatment team became infected with HSV-1, probably by the bio-aerosol con-
taining HSV-1, induced by ultrasonic scaling or by rubbing her eyes while working. The
infected HCWs manifested recurrent HSV-1 infections [77].
Discussion
By conducting a scoping review we were able to summarize existing evidence on the genera-
tion, composition, load and hazards of bio-aerosols in hospital and dental environment. We
found that bio-aerosols are generated via multiple sources such as machines, different types of
interventions; instruments; and human activity. The composition of bio-aerosols depended on
the method of sampling (active versus passive), microbiological techniques (culture based
versus DNA-based, different culture plates used) and the setting of the study (specific clinics
versus general dental clinics). Bio-aerosols can be hazardous to both patients and HCWs. Mul-
tiple studies described the threat of Legionella species to elderly and patients with respiratory
complaints.
The composition of bio-aerosols was extensively studied in hospital environments (N = 31)
compared to dental environments (N = 16). Regarding the micro-organism composition of
bio-aerosols, we conclude that bio-aerosols contain a high variety of bacterial and fungal

Table 4. Study characteristics in the dental setting.

Almaghlouth, Setting: Dental clinic Before: Diphteroids spp; Micrococcus spp
2007 Sampling method: Passive air sample: Blood agar and Brain Heart During: Diphteroids spp; Micrococcus spp; Staphylococcus epidermidis.
agar culture plates. 15–20 min exposure during; 30 min in advance After: Diphteroids spp; Micrococcus spp; Staphylococcus epidermis,
and 2h after treatment. aureus.
Bennett, 2000 Setting: Dental clinic Range max peak CFU/m3
Sampling method: Air sampled with The Casella slit sampler; 30L/ Winter: 6.3 x 103–8.7 x 103
min; 2 min during treatment; 1m from patients mouth at bench height. Summer: 3.0 x 103–6.2 x 103
Andersen sampler 28L/min 5 min; during treatment; 2m from patient;
at foot of dental chair. Tryptone yeast extract Cystine agar; Columbia Bacteria:
blood agar. EPS producing streptococci: 50%
Barlean, 2010 Setting: Dental clinic Mean (range) CFU/m3 mesophilic bacteria:
Sampling method: Passive air sample: Tryptone soy agar, sheep Before: 129 (42–273)
blood; Sabouraud agar; exposed 15 min; 30cm and 2.5m distance After: 429.6 (105–1018)
from dental unit.
Range CFU/m3 fungi:
Before: 21–29
After: 52–808
Bacteria:
Mesophilic bacteria: Staphylococcus aureus: 6.6.%
Fungi: NR
Cellini, 2000 Setting: Dental clinic CFU/m3 range:
Sampling method: Air sampled with Air Microbial index, plate method; 4–18
placed prior to exposure; 1h exposure at 1m height and 1m from wall;
before and after
Dutil, 2007 Setting: Dental clinic Mean endotoxin in air CFU/m3:
Sampling method: Andersen six-stage air sampler; 28.3L.min during Before: 0.34
20 min; 2h before; during and 2h after dental treatment. 30cm from During: 0.54
patients mouth. R2A and blood agar.
After: 0.33
Duell, 1970 Setting: Dental clinic TB (not found)
Sampling method: Andersen six stage air sampler; petri dishes; 30
cm from patient; air sampling 15min.
Grenier, 1995 Setting: Dental clinic, closed and multichair Mean CFU/m3 (SD) 1:
Sampling method: Air sampled with Slit-to-agar biological air sampler, Before: 12 (4)
20L/min; 30 min before, during, after treatment duration of 30 min;
122cm from patient at 91 cm height
Three settings: During: 216 (75)
1. Closed dental operatory using ultrasonic scaler. After: 44 (14)
2. Operative treatments in closed dental operatory. 2h after: 10 (1)
3. Multichair 4h after: 6 (2)
Mean CFU/m3 (SD) 2:
Before: 14 (4)
During: 75 (22)
After: 51 (22)
2h after: 12 (4)
4h after: 9 (4)
Mean CFU/m3 (SD NR!)3:
Before: 13.5
After: 97.75
3h after initiation: 82.75
7h after: 9
(Continued)


Guida, 2012 Setting: Dental clinic within a hospital Active sampling CFU/m3 (SD)
Sampling method: Air sampled using Surface Air System; 180L/min Before: 86.6 (50.6)
500L volume; 1m height; 1m from unit. Passive sampling with petri During: 82.3 (48.3)
dish exposed for 1h. Before; during and after treatment. Tryptone
soya agar. After: 86.5 (64.8)\
Passive sampling CFU/m3 (SD):
Before: 38.3 (21)
During: 39.6 (28.2)
After: 20 (11.5)
Kadaifciler, Setting: Dental clinic AMHB range mean CFU/m3 (SD):
2013 Sampling method: Air sampled with HiAirflow, 100L/min, 1.4 height, Before treatment: 10 (0)– 453 (21)
near to dental unit, before; during and after treatment. Trypton soya After treatment: 10 (0)– 2.477 (57)
agar for AMHB; Sabouraud and RB-agar for fungi.
Fungi range mean CFU/m3 (SD):
Before treatment: 0–42 (23)
After treatment: 0–94 (95)
Yeast range mean CFU/m3 (SD):
Overall: 3–25
Bacteria:
Micrococcus spp.; Staphylococcus xylosus; Staphylococcus lentus;
Staphylococcus chromogenes.
Fungi %:
NSF: 27.30 P. chrysogenum: 21.27; Pencillium: 11.11; C. Cucumerinum:
5.55; Alternaria brassicicola: 4.96; Cladosporium spp: 4.49; Aspergillus
flavus: 3.86; Alternaria alternata: 2.83; Alternaria citri: 2.60; C.
Cladosporiodias: 2.48; C. spongiosum: 2.48; Aspergillus: 1.93
Aspergillus niger: 1.30; Ulocladium alternariae: 0.82; Arthrinium
phaesospermum: 0.82; Stemphylium spp.: 0.82; Acremonium zonatum:
0.82; Botrytis spp.: 0.82; Cladosporium sphaerospermum: 0.82;
Monocillim indicum: 0.82; Cladosporium ramotenellum: 0.82; Monodictys
glauca: 0.82.
Yeast %:
Geotrichum spp: 12.62
Kimmerle, 2012 Setting: Dental clinic, multi chair Bacteria average CFU/m3:
Sampling method: Air sampled with Andersen biological air sampler Micrococcus luteus: 188.8; Staphylococcus epidermidis & haemolyticus:
total of 100L at different time points. Colombia blood agar plates and 114.5; Micrococcus lylae: 16.6; Pseudomonas: 10.6; Chrysemona luteda:
enterococci-selective bile esculin agar; 16S RNA gene sequencing; 0.5; Staphylococcus hominis: 9.0; Acinetobacter wolffii: 5.1;
Gram staining. Pseudomonas stutzeri: 0; Staphylococcus capitis: 3.7; Bacillus pumilus:
6.8Fungi %:
Aspergillus fumigatus: 4.8; Aspergillus niger: 0.9; Aspergillus flavus: 0.2
Kedjarune, Setting: Multi chair dental clinic Total bacteria
2000 Sampling method: Air sampled with Slit-to-agar air sampler 75cm Total mean (SD) CFU/m3:
height and 30-35cm from dentists. Before: 177.41 (211.14); During: 232.49 (163.35)
After: 44.58 (46.82)
Total mean (SD) before/ during CFU/m3:
Endodontic: 264.16 (143.53) / 270.29 (158.33)
Operative: 188.28 (114.74) / 186.23 (69.26)
Scaling: 245.10 (134.55) / 182.57 (63.99)
Bacillus:
Total mean (SD) CFU/m3:
Before work: 10.89 (9.9); during work: 9.84 (20.14); after work: 3.34
(7.41)
Total mean before and during (SD) CFU/m3:
Endodontic: 11.15 (9.39) / 6.32 (4.98)
Operative: 16.20 (32.39) / 6.17 (7.58)
Scaling: 17.05 (11.74) / 8.69 (4.78)
(Continued)


Pankhurst, Setting: Dental clinic Bacteria:
1995 Sampling method: CF patients colonized with B. cepacia. Air sampled B. cepacia (not found)
before, during and after treatment by Surface Air System sampler,
540L per patient, 0.25m from patient. Selective culture for B. cepacia.
Pasquarella, Setting: Dental clinic Total mean bacteria CFU/m3before and after treatment:
2012 Sampling method: Passive air sample placing Tryptone Soya Agar for Passive sampling: 78/110Active sampling: 12/14
1 hour, 1 m above the floor. Active air sampling using SAS sampler,
180L/min volume 500 L.
Rautemaa, Setting: Dental clinic High speed:
2006 Sampling method: Passive air sample: Horse blood chocolate agar; 6 <1m: mean CFU 823/m2
locations; 0.5m – 2m from patient. Gram staining. Sampling 1.5 and 3 >1.5m: mean CFU 1120/m2Periodontal: mean CFU 598/m2
hours exposure at start of treatment
Bacteria:
Gram positive cocci; Gram negative cocci; Gram positive rods; Gram
negative rods.
Szymanska, Setting: Dental clinic Total bacteria % before disinfection:
2008 Sampling method: Air samples collected with portable Air Sampler Gram negative: 1.31; Staphylococci and other catalase positive cocci:
RCS plus, placed 25 cm distance from patient, 100L air per sample. 15.70; Streptococci and other catalase negative cocci: 79.23; Endospore
Tryptic soy agar and GP2 microplate. Sampling before and after forming bacilli: 1.45%; Corynebacteria and related organisms: 2.30;
disinfection (H2O2) of DUWL. Actinomycetes: 0.01%
Total bacteria % after disinfection:
Gram negative: 1.08; Staphylococci and other catalase positive cocci:
61.19; Streptococci and other catalase negative cocci: 24.28; Endospore
forming bacilli: 7.92; Corynebacteria and related organisms: 4.18;
Actinomycetes: 1.35
Mean CFU/m3 before disinfection:
Gram negative: 52; Staphylococci and other catalase positive cocci: 624;
Streptococci and other catalase negative cocci: 480; Endospore forming
bacilli: 50; Corynebacteria and related organisms: 30; Actinomycetes: 0
Mean CFU/m3 after disinfection:
Gram negative: 0; Staphylococci and other catalase positive cocci: 640;
Streptococci and other catalase negative cocci: 90; Endospore forming
bacilli: 50; Corynebacteria and related organisms: 30; Actinomycetes: 0
Timmerman Setting: Dental clinic Total CFU during high volume evacuation:
2003 Sampling method: Passive air sampling by placing Petri dishes during Before: 0.2 (0.4)
ultrasonic scaling. Baseline measure for 10min exposed dishes in 0–5 min 40cm: 0.4 (0.7)
middle of operatory. 2 plates on tray table over patient’s chest 40cm
away from mouth. 2 plates on cart 150cm from patient’s mouth next to 20–25 min 40cm: 1.6 (1.3)
wall, behind patient and dentist at 100cm height exposed for 20min. 0–20 min 150cm: 5.4 (8.3)
BHI agar. 20–40 min 150cm: 2.7 (3.2)
0–40 min 150cm: 8.1 (11.3)
Total CFU during conventional dental suction:
Before: 0.6 (0.7)
0–5 min 40cm: 2.5 (2.9)
20–25 min 40cm: 1.8 (1.6)
0–20 min 150cm: 4.3 (3.5)
20–40 min 150cm: 6.3 (5.9)
0–40 min 150cm: 4.0 (4.1)
Abbreviations: BHI = brain heart infusion; TB = tuberculosis; CFU = colony forming units; cm = centimeters; DUWL = dental unit waterline; h = hours;
m = meters; min = minutes; SD = standard deviation.

Fig 4. Bacterial or fungal loads in mean Log-10 CFU/m3 in dental. * = passive sampling method; # active
sampling method.
strains from different sources such as the human skin and intestine; and the environment such
as soil and water. Based on the sampling and culturing techniques, fungi and Gram-positive
bacteria were found most often. Pathogens such as Legionella and Pseudomonas species were
found in bio-aerosols that were distributed by instruments using tap water. Few studies looked
Fig 5. Bacterial or fungal loads in mean Log-10 CFU/m3 in dental, measured twice. * = passive sampling method; # active
sampling method.

Table 5. Study characteristics hazard in healthcare and the dental setting.

Augustowska Study the variability of airborne microflora of a hospital ward in Decrease of lung function:
2006 pneumonological department.Organism:
Mesophilic bacteria; fungi - Decrease spirographic indices in asthmatic patients at increase of
bacteria/fungi in air: 37.5%
Study design: - Decrease of vital capacity.
Cross-sectional study with microbiological examination of the air - Decrease of forced expiratory volume in 1 second.
and the lung function in asthmatic patients.
Browning 2012 Awareness of the risks involved in treating active herpes labialis Case 4:Dental hygienist got both eyes infected with HSV-1. Three
in a dental clinic possibilities: 1) high exposure to active herpes patients; 2)
Organism: HSV-1 ultrasonic scaling producing HSV-1 bio-aerosol; 3) rubbing eyes
while working.
Study design: Case series, N = 4
Kool 1998 Investigate a clustered of cases of legionnaires disease among Exposure factors OR univariate:
patients at a hospital.
Organism: L. pneumophila - Corticosteroids: 5.1 (1–50) SIG—Intubation: 4.6 (1.1–27) SIG
Study design: Case-control study N = 74 - Showering: 0.1 (0–1.3) NS—Medication nebulizer: 1.5 (0.3–6.8)
NS
- Drinking tap water: 1.3 (0.3–5.4) NS
Exposure factors OR multivariate:
- Walking in hallway 1–3 days: 0.07 (0.01–0.6) NS- Corticosteroids:
13 (1.6–102) SIG.
- Walking in hallway >3 days: 0.3 (0.03–2.6) NS—Intubation: 10
(1.3–73) SIG.
MacIntyre 2014 Description of the range of exposure to HRP in HCWs. RR infection high risk procedure performed vs not performed:
Organism: Adenovirus; human metapneumovirus; corona virus; Clinical respiratory infection: 2.5 (1.3–6.5) P<0.01
parainfluenza virus; influenza virus A, B; rhinovirus A,B; Confirmed virus: 2.8 (0.9–8.7) P = 0.07
streptococcus pneumonia; mycoplasma pneumonia; B.
pertussis; Legionella spp.; chlamydophilia; Haemophilus
influenza type B.
Study design: Virus or bacteria: 2.6 (1.4–5) P<0.01
Prospective study, participants recording following procedures Influenza: 1.5 (0.2–13) NS
on a daily basis: Provision of nebulizer medications; suction; RR bacteria of virus in HCWs:
intubation; bio-aerosol-generating procedures; chest
physiotherapy. N = 481 Influenza vaccine: 1.3 (0.56–2.8) NS
Hand washing: 0.7 (0.3–1.63) NS
HRP performed: 2.9 (1.37–6.22) P = 0.01
Palusinska- Description of the pathogenicity of legionella Symptoms:
Szysz 2009 Organism: L. pneumophila Early: mild cold; low fever; malaise; anorexia; muscles aches; puss
forming sputum; blood streaked sputum; cough blood.
Later: high fever; bronchiolitis; alveolitis; lung damage with
infiltrated regions.
Study design: Review Risk factors instruments:
Air conditioning; cooling towers; whirlpool spas; water delivery
systems; contaminated birth bathtub; intubation; mechanical
ventilation; aspiration; respiratory equipment.
Risk factors in human:
neonates; elderly; diabetes; chronic lung disease; chronic severe
renal failure; hematologic malignancies; lung cancer; male gender;
alcohol; gluco-corticosteroids; immunosuppression; high iron;
smokers.
(Continued)


Ricci, 2012 Description infection source of legionella An 82-year-old woman admitted to intensive care unit with fever and
respiratory distress. The woman was positive for L. pneumophila.
The woman has acquired the infection from the contaminated
DUWL biofilm and died 2 days after diagnosis.
Organism: L. pneumophila OR per procedure:
- Tracheal intubation: 6.6 (2.3–18.9)–SIG
Study design: Case control - Non-invasive ventilation: 3.1 (1.4–6.8) SIG
- Suction before intubation: 3.5 (0.5–24.6) NS
Tran 2012 Risk of transmission of acute respiratory infections to HCWs - Suction after intubation: 1.3 (0.5–3.4) NS
exposed to bio-aerosol generating procedures
Organism: SARS - Nebulizer: 0.9 (0.1–13.6) NS
Study design: Systematic review and meta-analysis - Manipulation oxygen mask: 4.6 (0.6–32.5) NS
- Bronchoscopy: 1.9 (0.2–14.2) NS
- Insertion of nasogastric tube: 1.2 (0.4–4.0) NS
- Chest compression: 1.4 (0.2–11.2) NS
- Defibrillation: 2.5 (0.1–43.9) NS
- Chest physiotherapy: 0.8 (0.2–3.2) NS
Abbreviation: HCWs = healthcare workers; HSV-1: herpes simplex virus-1; HRP = high risk procedures; NS = not significant; OR = odds ratio; RR = risk
ratio; SARS = severe acute respiratory syndrome; SIG = significant; N = number of subjects.
for viruses, and in total only ten different viruses were identified, because no open ended
detection or identification methods are available for viruses. Therefore only specific targeted
techniques were used. Moreover, none of the studies conducted in dental practice have used
methods to identify the presence of viruses in the generated aerosols. Therefore, we must keep
in mind that the yielded results were dependent on the methodology of the individual study.
The results of the individual studies, and the heterogeneity we found in this review, are depen-
dent on the methods leading to an over- or under estimation of the complete bio-aerosol
profile. The same inconsistency is discussed in previous studies in which the researchers com-
pared two main sampling methods [80]. The methodological variety between studies, e.g. dif-
ferences in method of sampling and culturing or sequencing, differences in sampling time and
sampling area; and differences in distance to the bio-aerosol generating source caused difficul-
ties in comparing results. When a study used selective medium or agar it results in an overview
of selected micro-organisms. This leaves out other micro-organisms that were present at that
moment. The same accounts for duration of sampling or passive versus active sampling. In
passive sampling, the researcher waits for a certain amount of time for micro-organisms to
fall on a Petri dish, while other micro-organisms were still floating in the air and take more
time to fall on surfaces. The spread in a bio-aerosol is heterogeneous, so whatever is ‘catched’
on that moment may vary from the second, third or even fourth sampling attempt. So, the
method chosen (active or passive) should be dependent on the aim of the air quantification
[80]. Furthermore, in many studies variables in the experimental setup were not described,
like sampling time, distance and sampling location. Also, no standard deviations of the micro-
biological loads were reported consistently. Besides, the data might be an underestimation of
reality since studies looked for specific micro-organisms, in specific settings by selective sam-
pling and culture dependent techniques, thereby missing other micro-organisms present in
the bio-aerosols. Also, there was very little data available on the persistence of micro-organ-
isms in the air over time and the spatial distribution. None of the included studies looked for

parasites, although it has been reported that these are present in many tap water dependent
bio-aerosol producing systems with plastic tubing [81, 82].
We found little evidence to state the presence or absence of direct threats or health risks for
patients or HCWs with regards to bio-aerosols. In the hospital setting, two studies reported on
the hazard for the staff [12, 31], and four on the hazard for patients [34, 45, 78, 79]. The search
yielded one study for this objective assessing the hazard of an infectious disease to dental staff
[77]. However, it is known that on average, dental practitioners carry elevated levels of Legio-
nella antibodies [83], but the hazard to non-healthy HCWs and patients remains, based on our
findings, unknown. An estimation of the hazard of bio-aerosols is usually made based on the
microbial content and load of the bio-aerosols. We conclude that bio-aerosols can be hazard-
ous to certain populations that are extensively exposed to bio-aerosol generating procedures or
immunocompromised people.
Limitations
The search yielded 40 references that were to be screen based on full text. However, we could
not recover these 40 full text manuscripts to assess the their eligibility for inclusion, even
though we tried to contact the first and/or corresponding author, by retrieving his/her email
via the abstract or Google. We assume that the body of evidence for each objective would have
been larger if all 40 studies, or at least a part, would have been available and included. Another
limitation was that the outcomes and methods were inconsistent throughout all included stud-
ies. Also, there was little data on the hazard of bio-aerosols, thus no strong conclusions could
be drawn.
Recommendation for future research

We recommend that future research on bio-aerosols should create an extensive and complete
methodology for the quantification of air contamination. Time and frequency of air sampling,
distance from sources, location of sampling in both passive and active air sampling techniques
should be described thoroughly. Furthermore, the identification of micro-organisms should
be done by both selective and non-selective methods and cover organisms that find their origin
in water, human, and environment. Also, we believe that infections due to a bio-aerosol should
be structurally reported so that the risk for HCWs and patient can be analyzed. Finally, the
risks for HCWs, especially dentists, working in an environment in which they are continuously
exposed to bio-aerosols, and to their patients remain unclear and therefore need further re-
search. This is needed in order to comprehend the risks of bio-aerosols generated in clinical
settings to attention to staff and patients to improve awareness, hygienic standards, risks, and
prevention methods.
Conclusion
Bio-aerosols are generated via multiple sources such as different interventions, instruments
and human activity. Bio-aerosols have different microbiological profiles depending on the set-
ting and the used methodology. Bio-aerosols can be hazardous to both patients and healthcare
workers. Legionella species were found to be a bio-aerosol dependent hazard to elderly and
patients with respiratory complaints.
Supporting information
S1 PRISMA checklist.
(DOC)

Acknowledgments
The authors would like to thank Prof. dr. Geert van der Heijden for his consulting role during
the methodology process.
Author Contributions
Conceptualization: CZ HdS WC AL.
Data curation: CZ.
Formal analysis: CZ.
Investigation: CZ HdS AL.
Methodology: CZ.
Project administration: CZ.
Resources: CZ.
Software: CZ.
Supervision: HdS AL WC.
Validation: HdS AL.
Visualization: CZ.
Writing – original draft: CZ.
Writing – review & editing: HdS AL WC.
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RESEARCH ARTICLE

A scoping review on bio-aerosols in

Editor: Dongsheng Zhou, Beijing Institute of

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Screening process and inclusion criteria

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Data extraction and summary

Fig 1. PRISMA flowchart.

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30 different bio-aerosol generating sources. Humans produced aerosols by coughing, and

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Table 1. Overview of micro-organisms identified in hospital setting.

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Table 2. Study characteristics hospital setting.

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Study Set up Findings

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Study Set up Findings

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Study Set up Findings

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Study Set up Findings

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Study Set up Findings

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Table 3. Complete overview micro-organisms identified in the dental setting.

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Table 4. Study characteristics in the dental setting.

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Study Set up Findings

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Study Set up Findings

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Table 5. Study characteristics hazard in healthcare and the dental setting.

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Study Set up Findings

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Recommendation for future research

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