Contents lists available at ScienceDirect
International Journal of Hygiene andEnvironmental Health
journal homepage: www.elsevier.com/locate/ijheh
Bioaerosol exposure from composting facilities and health outcomes inworkers and in the community: A systematic review updateSarah Robertsona,b,1, Philippa Douglasb,c,1,∗, Deborah Jarvisc, Emma Marczyloa,b
a Centre for Radiation, Chemical and Environmental Hazards, Public Health England, Harwell Campus, Didcot, Oxfordshire, UKbNational Institute for Health Research Health Protection Research Unit (NIHR HPRU) in Health Impact of Environmental Hazards, UKcNational Heart and Lung Institute, MRC PHE Centre for Environment and Health, Imperial College London, London, UK
A R T I C L E I N F O
Keywords:BioaerosolsAllergensPrimary biological airborne particlesCompostingRespiratory health
A B S T R A C T
Background: Rapid population growth and urbanisation around the world has led to increasing waste generationrates. Composting of organic waste in large-scale facilities is part of a growing trend in the UK, and elsewhere, tobetter manage and re-use the organic waste. However, composting inevitably generates bioaerosols, which havebeen associated with human health effects. In 2015, we reported that there was some, albeit limited, qualitativeevidence linking bioaerosol emissions from composting facilities to poor respiratory health in nearby residents.However, the limited evidence precluded any quantitative assessment. Since then, the number of operationalindustrial-scale composting facilities in England has increased by 9% - nearly twice the growth from 2012 to2014. At the same time, rapid urbanisation has led to expansion of city borders with more people living nearlarge composting facilities and exposed to bioaerosol pollution. It is essential that regulatory authorities haveaccess to the most up to date and accurate information.Objective: In this update of a systematic review published in 2015, we review and summarise the evidence frommore recent studies that have assessed bioaerosol exposures within and near composting facilities and theirassociated health effects in both community and occupational health settings. Specifically, we wanted to find outif new evidence has emerged since the previous review to strengthen and confirm its conclusions.Material and methods: Two electronic databases (Medline and Embase) and bibliographies were searched forstudies reporting on health outcomes and/or exposure to bioaerosols from composting facilities published be-tween 1 January 2014 and 15 June 2018. Identification of relevant articles and data extraction was undertakenand studies were assessed for risk of bias.Results: 23 studies met the inclusion criteria (15 exposure studies, 4 health studies, 4 health and exposure studies(one of which used an exposure proxy)). The majority of studies were conducted in occupational settings, andover short time periods. Some progress has been made in the characterisation of bioaerosol emissions from thesecomposting facilities, with the application of molecular-based methods. Whilst the latest health studies do notrely solely on subjective self-reported measures of health status but include more objective health measures,these studies were almost exclusively carried out in compost workers and were characterised by profoundmethodological limitations. Only one community health study was identified and used a proxy measure ofbioaerosol exposure.Conclusions: Although this review identified an additional 23 studies since the earlier review, the conclusionsremain largely unchanged. Given the absence of any consistent evidence on the toxicity of bioaerosols fromcomposting facilities, there is insufficient evidence to provide a quantitative comment on the risk to nearbyresidents from exposure to compost bioaerosols. To improve risk assessment and to best advise on risk man-agement, it is important to ensure that the research recommendations outlined in this review are addressed.
https://doi.org/10.1016/j.ijheh.2019.02.006Received 14 December 2018; Received in revised form 17 January 2019; Accepted 12 February 2019
Abbreviations: ABAS, Ausschuss für Biologische Arbeitsstoffe (Committee on Biological Agents); ARG, Anti microbial Resistance Genes; DECOS, Dutch ExpertCommittee on Occupational Safety; EBC, Exhaled Breath Condensate; TBRA, Technischen Regeln für Biologische Arbeitsstoffe (Technical Rules for Biological Agents)
∗ Corresponding author. EHE, CRCE, Public Health England, Chilton, Harwell Campus, Didcot, OX11 0RQ, UK.E-mail addresses: [email protected] (S. Robertson), [email protected], [email protected] (P. Douglas),
[email protected] (D. Jarvis), [email protected] (E. Marczylo).1 Robertson and Philippa Douglas are joint first authors.
International Journal of Hygiene and Environmental Health 222 (2019) 364–386
1438-4639/ © 2019 Elsevier GmbH. This is an open access article under the CC BY license (http://creativecommons.org/licenses/BY/4.0/).
T
1. Introduction
Around the world, waste generation rates are rising with rapid po-pulation growth and urbanisation. Worldwide, the amount of municipalwaste generated is expected to triple by 2100 (Population matters,2018). As a result, waste management has drawn increasing attention.In recent years, the UK has moved away from reliance on landfills to-wards more environmentally sustainable methods of managing wasteand resources. A key driver in this has been the European UnionLandfill Directive, which requires the UK (and other Member States) toreduce the biodegradable waste sent to landfill to 35% of the 1995 levelby 2020 (Council of the European Union, 1999). Composting of organicwaste in large-scale facilities is part of a growing trend in the UK and in2017 there were 327 operational industrial-scale composting facilitiesin England, a 134% increase from the 2010 figure of 140 (EnvironmentAgency, 2018c) (Fig. 1).
Commercial scale composting is conducted either in open-air turnedwindrows (long heaps of composting material), or in-vessel systems(also referred to as reactor systems and where the composting materialis enclosed). Open windrow composting systems are employed by thevast majority (∼70%) of facilities in the UK (Environment Agency,2018c) The downside of composting is the biological air pollution(bioaerosols) released or produced, particularly as a consequence ofagitation activities (such as shredding, turning and screening) (Tahaet al., 2006). Bioaerosols, also known as primary biological airborneparticles (PBAPs) have been linked to various health effects, affectingprimarily the respiratory system, in a number of occupational settings,including composting (Pearson et al., 2015). The increased utilisation ofcomposting as a sustainable waste management option, has led to in-creased public concern regarding potential health impacts withincommunities surrounding the sites. The Centre for Radiation, Chemicaland Environmental Hazards (CRCE) within Public Health England(PHE) received 12 composting-related enquiries in August 2017 toAugust 2018, whereas there was only one composting-related enquiryin 2009–10 (PHE Environmental Hazards and Emergencies Department,personal communication, 6th September 2018).
We previously performed a systematic review of studies of bioaer-osol exposures from waste composting and related health effects in-dexed in bibliographic databases up to July 2014 (Pearson et al., 2015).There was some, albeit limited, qualitative evidence linking bioaerosolemissions from composting facilities to poor respiratory health innearby residents (Pearson et al., 2015). However, the limited evidenceprecluded any quantitative assessment. Rapid urbanisation has meantan expansion of city borders, and the boundaries of both rural andurban regions have becoming increasingly blurred (Eurostat, 2016)
with more people likely to be living in the vicinities of industrial-scalecomposting facilities. In view of the potential health effects of nearbycommunity exposure to composting bioaerosol and to ensure regulatoryauthorities have access to the most up-to-date information, this updatedreview looks at the evidence published since 2014.
1.1. Bioaerosol exposure at composting facilities
Composting results in elevated concentrations of bioaerosols, parti-cularly during agitation activities (Taha et al., 2006). Bioaerosol con-centrations and emissions are influenced by a number of biotic andabiotic factors (Brągoszewska et al., 2017). The continuation of an up-ward trend in the number of composting facilities is therefore likely toincrease bioaerosol concentrations and diversity. Bioaerosols can staysuspended in the air for prolonged periods and potentially travel longdistances from their source (Nygard et al., 2008) and as a result may posehealth hazards to nearby communities with elevated exposures.
1.2. Potential health effects of bioaerosols at composting facilities
In many occupational settings, including composting, exposure tobioaerosols has been associated with a range of acute and chronic ad-verse health effects and diseases (Douwes, 2003; Pearson et al., 2015).The most commonly reported are respiratory system problems (e.g.rhinitis, asthma, bronchitis and sinusitis), through both atopic and non-atopic allergic mechanisms as well as non-allergic pathways (Douwes,2003; Pearson et al., 2015). Other health problems reported includegastrointestinal (GI) disturbance, fatigue, weakness and headache(Douwes, 2003). Bioaerosol exposure occurs primarily through in-halation, although ingestion also contributes. Dependent on particlesize, bioaerosols may penetrate into the lungs and become embedded inalveoli (Douwes, 2003; Ivens et al., 1999). While there is no conclusiveevidence, several modes of action have been proposed to explain theassociation between occupational exposure to bioaerosols and health,such as airway inflammation and oxidative stress (Li et al., 2003; Quet al., 2017; Samake et al., 2017). A robust systematic review of theliterature (Pearson et al., 2015) found some, albeit limited, qualitativeevidence of linkage between living near large-scale composting facil-ities and respiratory ill health. The annual report of the UK ChiefMedical Officer, 2017 ‘Health Impacts of Air Pollution – what do weknow?’ also drew attention to the potential of public health risks frombioaerosol liberation at composting sites and highlighted the need forbetter understanding (Chief Medical Officer, 2017).
While there tends to be a bias towards the presumption of health risksfrom bioaerosols, the converse – beneficial health effects – may also
Fig. 1. Number of operational, industrial-scale composting facilities per year in England based on compost site permit data (Environment Agency, 2018c).
S. Robertson, et al. International Journal of Hygiene and Environmental Health 222 (2019) 364–386
365
occur (e.g. increased microbial exposure, particularly during early life,may improve the immune system and reduce incidences of infection andallergic disease) (Bloomfield et al., 2016; Mirabelli et al., 2006).
1.3. Bioaerosol and composting legislation
At present, there are no quantitative dose-response estimates toinform legislation on bioaerosol emissions from composting facilities.The UK and several other countries, including Germany and theNetherlands, have developed regulatory guidelines to assess risk andcontrol exposures to workers and nearby residents but these guidelinesdiffer between countries. In England, the Environment Agency (EA)adopt a precautionary stance, and updated their guidance in January2018 (Environment Agency, 2018a). In summary, composting facilitieswith ‘sensitive receptors’ (a place where people live or work for morethan 6 h at a time) within 250 m of the site boundary are required tocomplete a site specific risk assessment, and monitor bioaerosols usingthe EA's Technical Guidance Note (M9) for the environmental mon-itoring of bioaerosols at regulated facilities (Environment Agency,2018b). The M9 replaces the 2009 Association for Organics Recycling(AfOR) standardised protocol for the monitoring of bioaerosols at opencomposting facilities. Composting facilities should demonstrate thatbioaerosols are maintained at ‘acceptable levels’ above backgroundlevels (Environment Agency, 2010, 2018a). The ‘acceptable levels’ are(Environment Agency, 2018a):
• 1000 colony forming units per cubic metre (CFU m−3) for totalbacteria;
• 500 (CFU m−3) for Aspergillus fumigatus
Gram-negative bacteria levels are no longer required to be mon-itored (Environment Agency, 2018a). In the UK, there are no occupa-tional exposure limits for bioaerosols. The Health and Safety Executive(HSE) provide composting facility employers with guidance on how tocomply with the Control of Substances Hazardous to Health (COSHH)regulations to control exposure and protect workers' health (Health andsafety executive, 2016). Under these regulations, the duty holder isobliged to assess risk and control workers' exposure to as ‘low as rea-sonably possible’. In Germany, the committee for Biological for Biolo-gical Agents (ABAS) have proposed a Technical Control Value of50,000 CFU m−3 for mesophilic fungus (TBRA, 2019). A proposed oc-cupational exposure limit of 90 endotoxin units per cubic metre (EUm−3) has also been proposed in the Netherlands (8 h time weightedaverage) by the Dutch Expert Committee on Occupational Safety(DECOS) (DECOS, 2010). In Poland, the Polish Committee for theHighest Permissible Concentrations and Intensities of Noxious Agents inthe Workplace have set limits of 100,000 CFU m−3 for mesophilicbacteria, 50,000 CFU m−3 for fungi and 200 ng m−3 – 2000 EU m−3 forendotoxin (Gutarowska et al., 2015).
1.4. Aim
The aim of this study was to undertake a systematic review of stu-dies conducted in occupational and community settings measuringconcentrations, and/or assessing the health effects associated withbioaerosol emissions within and nearby composting facilities. This is anupdate of an earlier systematic review (Pearson et al., 2015), whichreported limited qualitative evidence of an association between livingand/or working near large-scale composting facilities and ill health.Specifically, we wanted to find out if the relevant evidence that hasaccumulated over the last three years continue to support this position.
2. Material and methods
As per Pearson et al. (2015) the systematic review method was in-formed by Meta-Analyses and Systematic Reviews of Observational
Studies (MOOSE) criteria (Stroup et al., 2000) and Preferred ReportingItems for Systematic Reviews and Meta-Analyses (PRISMA) guidelines(Moher et al., 2009). The PROSPERO registration number isCRD42018089422.
2.1. Search strategy
A literature search was conducted across two electronic databases(Medline and Embase). The two search strings (provided in AppendixA) used to identify both health-based and exposure-based studies wereidentical to those developed by Pearson et al. (2015). The search stringswere inputted within the title and abstract fields of the electronic da-tabase and adapted to each of the individual databases. The search wasrestricted to English-language papers published between 1 January2014 and 15 June 2018. References were downloaded into the refer-encing software programme Endnote (version X8).
2.2. Study selection
After excluding duplicates, the selection of studies from the elec-tronic databases was conducted in three stages; first by titles; next byabstract and then by full text (PD, EM, SR). A conservative approachwas taken during the screening process. Any study with uncertaineligibility was taken forward for further consideration. To be includedin the final analysis, studies had to fulfil all of the following inclusioncriteria (adapted from Pearson et al. (2015)):
• The study was published in English between January 2014 and June2018
• The study concerned exposure (studies that measured bioaerosol orused proxies) or health effects relating to bioaerosols emitted fromcomposting sites
• The study was either peer reviewed or was published by a re-cognised institution
Studies were excluded if (adapted from Pearson et al. (2015)):
• They did not concern waste composting• They did not concern bioaerosols• They did not include original data• They were review papers, although the reference list was still
searched to identify any other potential relevant studies• They were unavailable in English• Full texts were unavailable
Discrepancies were resolved by discussion between reviewers (PD,SR & EM) and, if necessary, referral to an independent reviewer (DJ).
2.3. Data extraction
The standardised checklist developed by Pearson et al. (2015) wasused to extract data from studies that met the inclusion criteria. In-formation collected from all the studies were: study aims, study setting,statistical analysis, main findings and limitations. In studies containinghealth data, study design, study population, health metrics and out-come assessment were also extracted. In studies containing exposureinformation, the bioaerosols measured, bioaerosol sampling details andlaboratory methods were also extracted, as well as any quantitativeconcentration data. The data extraction was conducted independentlyby two authors (exposure information by PD and EM, and health in-formation by PD and SR).
2.4. Bias assessment
We used the quality assessment scoring tool from Douglas et al.(2018) which was itself previously developed from Shah et al. (2011).
S. Robertson, et al. International Journal of Hygiene and Environmental Health 222 (2019) 364–386
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Fig. 2. Flow diagram summarising the study selection and exclusion process.
S. Robertson, et al. International Journal of Hygiene and Environmental Health 222 (2019) 364–386
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This scoring tool, which was originally designed to assess bias fromcross-sectional and cohort studies, was adapted to allow bias from ex-perimental and quasi-experimental studies (Appendix B). Two re-viewers (PD, SR) independently assessed each study with reportedhealth effects for eight potential sources of bias: study design, selection,responder, confounder, exposure assessment, outcome assessment,sample size and analysis. A third reviewer (EM, DJ) resolved any dis-putes. Scores were provided on a scale of 1–4; a score of 4 was givenwhere there was a low risk of bias.
3. Results
3.1. Study selection
The study selection process is represented in Fig. 2.After removing duplicates, the search strategies identified 817 ci-
tations, of which 606 were excluded on title screening. After screeningfor relevance on abstracts and full text, 23 papers remained. The mostfrequent reasons for exclusion were: did not concern bioaerosols, didnot publish original data or did not concern composting. This reviewconsidered studies that measured exposures of bioaerosols and/or as-sessed the health effects associated with bioaerosol emissions withinand nearby composting facilities; occupational and community studieswere considered separately for both categories. Fig. 2 details thenumber of studies within each category.
Among the final set of 23 papers, there were 18 exposure studies, ofwhich 17 examined occupational exposure (4 also looked at communityexposure data). Eight health studies were reviewed, the majority ofwhich were occupation-based (n = 7). Only three of the health studiesincluded corresponding bioaerosol exposure data and all were con-ducted in an occupational setting (Gutarowska et al., 2018; Heldalet al., 2015, 2016; a fourth community health-based study used dis-tance from site as a proxy of exposure (Douglas et al., 2016). The ma-jority of studies were located in Germany, Canada, France, and Eng-land; studies involving these countries were included in the earlierreview (Pearson et al., 2015). However, a number of papers wereidentified in previously unstudied regions of Europe, (Ireland, Hungary,Switzerland), as well as in non-European countries (India, China).
The full study characteristics of the exposure and health studies arelisted in Table 1 and Table 2, respectively.
3.2. Exposure studies
Eighteen exposure studies (with measured exposures of bioaerosols)were reviewed; 13 of these were conducted in an occupational setting(Bonifait et al., 2017; Conza et al., 2014; Duquenne et al., 2015; Feeneyet al., 2018; Gutarowska et al., 2015; Gutarowska et al., 2018; Heldalet al., 2016; Heldal et al., 2015; Mbareche et al., 2017; O'Connor et al.,2015; Rashidi et al., 2017; Sebok et al., 2016; Veillette et al., 2018), onein a community setting (Gales et al., 2015) and four in both an occu-pational and community setting (Gao et al., 2018; Pahari et al., 2016;Pasciak et al., 2014; Tamer Vestlund et al., 2014). Only two of the 18exposure studies also assessed health outcomes (Heldal et al., 2015,2016, with a further study investigating the in vitro cytotoxicity of settleddust collected from a composting facility (Gutarowska et al., 2018).
The methods used in the exposure studies varied, with differentbioaerosol types and species being measured, using different samplingmethods and analytical techniques. It was not possible to extract ex-posure data on airborne levels when values were not included in themanuscript, or qualitative analyses were used.
3.2.1. Sampling methods and analytical techniquesStudies were heterogenous in design, and the bioaerosols were sam-
pled, and analysed using different methods, as summarised in Table 1.The majority of studies used a combination of different samplers.
Coriolis liquid impinger samplers (n = 4), Andersen impaction
samplers (n = 5) or filter samplers (n = 4), sampling for short periodsof time (Coriolis: 4–10 min, Andersen: 2–15 min, Filter: 30–360 min).Two studies adopted longer-term (> 24 h) sampling methods (Feeneyet al., 2018; O'Connor et al., 2015). These studies used Wideband In-tegrated Bioaerosol Sensors (WIBS) to sample fluorescent particles or aspore watch spore counter (to count spores per hour) (Feeney et al.,2018). However, sampling times remained relatively short (7 days). Insome studies it was not clear what sampling time was used (e.g. sam-pling time was reported for one sampling method but not another); andthree studies did not report a sampling time (Pasciak et al., 2014;Rashidi et al., 2017; Sebok et al., 2016).
Many different analytical techniques were used to quantify/identifybioaerosols in the collected samples, with all 18 studies performingsome type of microbial characterisation. The majority of studies(n = 10) used culture based methods; seven of which complementedthe culture methods with further verification methods (such as micro-scopic imaging; biochemical, physiological, antibiotic susceptibility orchemotaxic testing; immunofluorescence assays; mass spectroscopy; ormicrobial DNA sequencing). The different analytical techniques used bythe studies are summarised in Appendix C.
Five studies extracted DNA directly from air samples or settled dust toanalyse the wider (culture independent) microbial characteristics ofbioaerosols; using polymerase chain reaction (PCR)-based methods and/or next generation sequencing (NGS) for downstream microbial identi-fication. Four studies used PCR to detect bacteria (Bonifait et al., 2017;Gales et al., 2015; Gao et al., 2018; Veillette et al., 2018). Two of thesestudies (Bonifait et al., 2017; Gales et al., 2015) also used PCR to detectfungal species. Four studies used NGS to amplify 16S rRNA and/or rDNAITS1/2 regions to identify bacteria and fungi, respectively (Gao et al.,2018; Gutarowska et al., 2018; Mbareche et al., 2017; Veillette et al.,2018). No studies used whole genome sequencing to analyse all of themicrobial DNA (metagenome) within collected samples. One study (Gaoet al., 2018) detected antimicrobial resistance genes (ARGs).
In addition, nine studies performed some type of other (non-mi-crobial) bioaerosol characterisation. Seven studies used spectroscopy,gravimetry or WIBS to measure inhalable dust/particulate matter (PM).Four studies, including two studies that also included health data(Heldal et al., 2015, 2016), used the Limulus amoebocyte lysate (LAL)assay (Duquenne et al., 2015; Heldal et al., 2015, 2016) or massspectroscopy (Gutarowska et al., 2015) to quantify endotoxin con-centrations. One study used the MTT (3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide) assay to measure the cytotoxicity ofsettled dust in human lung cells (Gutarowska et al., 2018). While cy-totoxicity is not a microbial characteristic per se, it may be related tomicrobial and/or non-microbial bioaerosol characteristics.
3.2.2. Bioaerosols/pollutants measuredMost studies reported bioaerosol concentrations, although it was not
always possible to extract this data from the study (e.g. data was onlypresented in graphs/figures). There was no one bioaerosol character-istic that was consistently measured across all of the studies. However,eleven studies enumerated total bacteria, eight total fungi, eightActinobacteria, four endotoxins, and eight measured inhalable dust/particulate matter/fluorescing particulate concentrations. Seven ofthese studies also measured the size distribution of microbial particlesand/or inhalable dust/particulate matter (see section 3.2.3).
Where possible, the concentrations of total bacterial and total fungi,the most commonly measured bioaerosols enumerated from the dif-ferent studies, are summarised in Figs. 3 and 4 respectively.
Overall total bacteria concentrations were higher than total fungi,and both were highly variable, with measurements of total bacteria andtotal fungi ranging across eight orders of magnitude(∼10–∼1,000,000,000 CFU m−3 for total bacteria and ∼1 to∼100,000,000 CFU m−3 for total fungi). There was evidence of con-siderable within site variability from replicates as denoted by the errorbars in the graph, which represent minimum and maximum reported
S. Robertson, et al. International Journal of Hygiene and Environmental Health 222 (2019) 364–386
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Table1
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ette
filte
rco
nnec
ted
toa
GilA
ir®
pum
p(2
Lm
in-1
,36
–210
min
(med
ian
90m
in),
heig
htof
1.7
m)
Num
bers
:
•tota
lsam
ples
=28
1(2
70an
alys
ed)
Tim
ing:
•9fa
cilit
ies
wer
evi
site
don
ce
•6fa
cilit
ies
wer
evi
site
dtw
ice
•Jun
2009
–Jan
2012
LAL
assa
y(3C)
:
•end
otox
in•O
mitt
ing
depo
sits
onth
ein
ner
surf
aces
ofth
eca
sset
tefil
ters
from
anal
ysis
unde
rest
imat
edth
eco
ncen
trat
ions
mea
sure
d
•35%
ofth
esa
mpl
esw
ere
abov
eth
eO
ELof
90EU
m−
3pr
opos
edby
the
Dut
chEx
pert
Com
mitt
eeon
Occ
upat
iona
lSta
ndar
dsin
2010
Feen
eyet
al.
(201
8)Ir
elan
d1
gree
nw
aste
open
win
drow
com
post
ing
faci
lity
1lo
catio
nat
the
Nor
thW
est
corn
erof
the
faci
lity
duri
nghi
gh,
low
orno
activ
ity
Sam
pler
s:
•WIB
S-4A
(7da
ys,0
.5–1
5μm
)
•spor
ew
atch
elec
tron
icsp
ore
&po
llen
sam
pler
(10
Lm
in−
1 ,tap
esu
rfac
em
oved
2m
mh−
1 ,7da
ys,h
eigh
tof
3m
)N
umbe
rs:
•con
tinuo
ussa
mpl
ing
over
7da
ysw
itha
reso
lutio
nof
1h
Tim
ing:
•1vi
sit
•29t
hFe
b-7t
hM
ar20
16
Spor
esa
mpl
er+
optic
alm
icro
scop
y(2A):
•fung
alsp
ores
WIB
S-4A
(2B/3B):
•bio
aero
sols
(fluo
resc
ent)
•non
-fluo
resc
ent
dust
•size
&sh
ape
data
•Tw
om
etho
dssh
owso
me
corr
elat
ions
&ov
erla
p
•Sam
pled
atth
esa
me
faci
lity
asO
'Con
nor
etal
.(20
15)
(continuedon
nextpage
)
S. Robertson, et al. International Journal of Hygiene and Environmental Health 222 (2019) 364–386
369
Table1
(continued)
Aut
hor
(yea
r)Co
untr
yN
umbe
r/ty
peof
site
sst
udie
dEx
posu
resa
mpl
ing
loca
tion/
activ
ityEx
posu
resa
mpl
ing
met
hods
aBi
oaer
osol
s/po
lluta
nts
mea
sure
d&
anal
ytic
alm
etho
dsb
Com
men
ts
Gut
arow
ska
etal
.(20
15)
Pola
nd4
com
post
ing
faci
litie
s:
•2gr
een
was
te(u
rban
area
s,fr
uit&
vege
tabl
em
arke
ts,
hort
icul
tura
lfac
ilitie
s)
•2pr
oduc
ing
subs
trat
esfo
rin
dust
rial
culti
vatio
nof
butt
onm
ushr
oom
s(w
heat
&ry
est
raw
,chi
cken
&ho
rse
man
ure)
3lo
catio
ns/a
ctiv
ities
perf
acili
ty:
•mus
hroo
msu
bstr
ates
1–
seed
ing/
sell
halls
•mus
hroo
msu
bstr
ates
2–
load
ing/
tran
sfer
/sel
lhal
ls
•gre
enw
aste
1–
open
aira
rea
•gre
enw
aste
2–
sort
ing
area
/lo
adin
gha
ll/m
achi
nero
om
•offi
ces(
inte
rnal
back
grou
nd)
•atm
osph
eric
air
(ext
erna
lba
ckgr
ound
,5–1
0km
from
faci
lity)
Plus
dust
sam
ples
from
gree
nw
aste
2w
aste
sort
ing
area
,&gr
een
was
te2
seed
ing/
sell
halls
Sam
pler
s:
•MA
S-10
0Ec
oai
rsam
pler
(acc
ordi
ngto
PN-
EN13
098:
2007
stan
dard
,50
&10
0L,
heig
htof
1.5
m)
•six-
stag
eA
nder
sen
impa
ctor
(28.
3L
min
−1 ,5
min
,hei
ght
of1.
5m
,in
prod
uctio
nha
llof
1m
ushr
oom
com
post
prod
ucin
gfa
cilit
ydu
ring
activ
ity&
follo
win
gcl
eani
ngpl
usin
tern
al&
exte
rnal
back
grou
nds)
Num
bers
:
•MA
S-10
0–
n=
16–1
8pe
rlo
catio
n/ac
tivity
,tot
alsa
mpl
es=
70
•And
erse
n–
n=
3pe
rlo
catio
n/ac
tivity
,to
tals
ampl
es=
24Ti
min
g:
•1vi
sit
per
faci
lity
•Feb
–Mar
2013
MA
S-10
0sa
mpl
er+
cultu
re(1A):
•tota
lbac
teri
a
•tota
lfun
giM
AS-
100
sam
pler
+cu
lture
+m
orph
olog
ical
&bi
oche
mic
alid
entifi
catio
n(1B)
:
•bac
teri
aldi
vers
ity
•fung
aldi
vers
ityM
AS-
100
sam
pler
+cu
lture
+N
GS(1F)
:
•bac
teri
alin
dica
tors
ofm
icro
biol
ogic
alco
ntam
inat
ion
(16S
rRN
A)
•fung
alin
dica
tors
ofm
icro
biol
ogic
alco
ntam
inat
ion
(ITS
1/2
rDN
A)
And
erse
nim
pact
or+
cultu
re(1A):
•size
dist
ribu
tion
ofba
cter
ia
•size
dist
ribu
tion
offu
ngi
GCM
S(3D):
•end
otox
in
•Bac
teri
aw
ere
the
pred
omin
ant
grou
pof
airb
orne
mic
roor
gani
sms
inco
mpo
stin
gfa
cilit
ies
prod
ucin
gbu
tton
mus
hroo
msu
bstr
ates
(78–
88%
)w
hile
fung
idom
inat
edin
gree
nw
aste
com
post
ing
faci
litie
s(5
3–56
%)
•Tot
alm
icro
orga
nism
sdi
dno
tex
ceed
quan
titat
ive.
Polis
hth
resh
olds
,alth
ough
the
high
est
mea
sure
dup
per
limit
exce
eded
BAU
Alim
its
•May
have
sam
pled
atso
me
ofth
esa
me
faci
litie
sas
Pasc
iak
etal
.(2
014)
Mba
rech
eet
al.
(201
7)Ca
nada
2co
mpo
stin
gfa
cilit
ies:
•dom
estic
(gre
enw
aste
)
•ani
mal
(pig
carc
asse
s&
plac
enta
)
5lo
catio
ns/a
ctiv
ities
perf
acili
ty:
•on-
site
,pri
orto
any
activ
ity
•on-
site
,beg
inni
ngof
wor
kac
tiviti
es
•on-
site
,mid
dle
ofw
ork
activ
ities
•on-
site
,end
ofw
ork
activ
ities
•off-
site
,upw
ind
Plus
com
post
sam
ples
(1L)
Sam
pler
:
•Cor
iolis
μ®liq
uid
impi
nger
(300
Lm
in−
1 ,10
min
)N
umbe
rs:
•n=
1pe
rlo
catio
n/ac
tivity
per
faci
lity
per
visi
t
•tota
lsam
ples
=30
Tim
ing:
•dom
estic
faci
lity
–4
visi
ts(2
insp
ring
&2
insu
mm
er)
•ani
mal
faci
lity
–2
visi
ts(1
insu
mm
er&
1in
autu
mn)
NG
S(I
TS1/
2ge
nes)(2D):
•fung
aldi
vers
ity•S
ome
fung
iwer
een
rich
edin
the
air
(com
pare
dto
com
post
)
•Rec
omm
end
taki
ngac
tion
tore
duce
wor
ker
expo
sure
O'C
onno
ret
al.
(201
5)Ir
elan
d1
gree
nw
aste
open
win
drow
com
post
ing
faci
lity
3lo
catio
ns/a
ctiv
ities
:
•∼20
mSo
uth-
East
ofou
tdoo
rpr
oduc
tco
mpo
star
ea&
∼20
mN
orth
-Eas
tof
deliv
er/l
oadi
ng/g
reen
was
tear
eadu
ring
heav
y,lig
ht&
noac
tiviti
es(W
IBS-
4on
ly)
•∼10
0m
upw
ind
(And
erse
non
ly)
•∼10
0m
dow
nwin
d(A
nder
sen
only
)
Sam
pler
:
•WIB
S-4
(7da
ys,h
eigh
tof
1.5–
2.0
m,
<13
μm)
•And
erse
ngr
absa
mpl
er(1
5m
in)
Num
bers
:
•WIB
S–
cont
inuo
ussa
mpl
ing
over
7da
ys
•And
erse
n–
n=
1pe
rlo
catio
n,to
tal
sam
ples
=2
Tim
ing:
•WIB
S–
30th
Sep-
1stO
ct20
14(1
day
heav
yac
tivity
),10
th-1
3th
Oct
2014
(3da
yno
activ
ity)
&15
th-1
7th
Oct
2014
(3da
ylig
htac
tivity
)
•And
erse
n–
13.0
0–14
.00
on16
thO
ct20
14
WIB
S-4(2B/3B):
•bio
aero
sols
(fluo
resc
ent)
•non
-fluo
resc
ent
dust
•size
&sh
ape
data
And
erse
nsa
mpl
er+
cultu
re(f
ollo
win
gM
9sa
mpl
ing
prot
ocol
)(1A):
•mes
ophi
licba
cter
ia
•A.fumigatus
Tota
lfun
gi&
bact
eria
coun
tsdu
ring
light
activ
ityw
ere
belo
wex
pect
edam
bien
tle
vels
Rash
idie
tal
.(2
017)
Iran
1m
unic
ipal
was
teco
mpo
stin
gfa
cilit
y(f
ood
was
te,p
aper
,woo
d,st
reet
was
tes,
ferr
ous
&no
n-fe
rrou
sm
etal
s,gl
ass,
plas
tic,e
tc)
4lo
catio
nsw
ithhi
ghw
orke
rtr
affic:
•scre
en
•con
veyo
rbe
lt
•aer
ated
pile
•stat
icpi
le
Sam
pler
:
•mul
ti-st
age
Qui
ckTa
ke30
impa
ctor
(acc
ordi
ngto
AST
ME8
84-8
2(2
001)
guid
elin
es,2
8.3
Lm
in−
1 ,hei
ght
of∼
1.5
m)
Num
bers
:
•n=
4pe
rlo
catio
n
•tota
lsam
ples
=20
Tim
ing:
•sum
mer
&w
inte
r20
15
Cultu
re(1A):
•tota
lbac
teri
a
•tota
lfun
gi
•S.aureus
•Klebsiella
•Con
cent
ratio
nsof
bact
eria
&fu
ngiw
ere
high
erth
anth
em
icro
bial
stan
dard
fori
nhal
edai
r
•Rec
omm
end
met
hods
tore
duce
wor
ker
expo
sure
(continuedon
nextpage
)
S. Robertson, et al. International Journal of Hygiene and Environmental Health 222 (2019) 364–386
370
Table1
(continued)
Aut
hor
(yea
r)Co
untr
yN
umbe
r/ty
peof
site
sst
udie
dEx
posu
resa
mpl
ing
loca
tion/
activ
ityEx
posu
resa
mpl
ing
met
hods
aBi
oaer
osol
s/po
lluta
nts
mea
sure
d&
anal
ytic
alm
etho
dsb
Com
men
ts
Sebo
ket
al.
(201
6)H
unga
ry3
com
post
ing
faci
litie
s:
•mun
icip
alw
aste
(pap
er,f
ood
resi
dual
s,pl
astic
s,et
c)
•agr
icul
tura
lwas
te(p
lant
resi
dues
)
•hor
ticul
tura
lwas
te(p
lant
resi
dues
,pot
ting
soil,
gree
nw
aste
)
1lo
catio
npe
rfa
cilit
y:
•1m
from
com
post
ing
pile
s
•plu
s1
unsp
ecifi
edna
tura
l(p
astu
re)
off-s
iteen
viro
nmen
t(ba
ckgr
ound
for
allf
acili
ties)
Plus
com
post
sam
ples
(∼1
kg)
Sam
pler
:
•And
erse
nim
pact
or(2
8.3
Lm
in−
1 ,hei
ght
of1.
5m
)N
umbe
rs:
•n=
3(3
days
of3
cons
ecut
ive
wee
kspe
rm
onth
visi
ted)
per
faci
lity
per
visi
t
•tota
lsam
ples
=48
Tim
ing:
•4vi
sits
•Oct
2011
,&Ja
n,A
pr&
July
2012
Cultu
re(1A):
•ther
mop
hilic
fung
iCu
lture
+m
orph
olog
ical
iden
tifica
tion
+co
nfirm
atio
nw
ithN
GS
(ITS
regi
on)(1B/1F):
•fung
aldi
vers
ity
Veill
ette
etal
.(2
018)
Cana
da3
com
post
ing
faci
litie
s:
•dom
estic
was
te(g
reen
was
te)
•veg
etal
was
te(m
anur
e,co
wbe
ddin
g)
•ani
mal
was
te(p
igca
rcas
ses
&pl
acen
taw
ithsp
inet
)
2-4
loca
tions
/act
iviti
espe
rfa
cilit
y:
•dom
estic
was
te–
1–2
mfr
omso
rtin
gor
siev
ing
•veg
etal
was
te–
1–2
mfr
omfil
ling,
tran
sfer
,mat
urat
ion
orsp
read
ing
•ani
mal
was
te–
1–2
mfr
omfil
ling
orbr
ewin
gPl
usco
mpo
stsa
mpl
es(1
0L)
Sam
pler
:•C
orio
lisμ®
liqui
dim
ping
er(3
00L
min
-1,
10m
in)
Num
bers
:
•n=
3pe
rlo
catio
n/ac
tivity
per
faci
lity
per
visi
t
•tota
lsam
ples
=60
(onl
y38
anal
ysed
)Ti
min
g:
•dom
estic
faci
lity
–4
visi
ts(2
inA
pr&
2in
July
)
•veg
etal
faci
lity
–2
visi
ts(J
un–A
ug)
•ani
mal
faci
lity
–2
visi
ts(J
un–S
ep)
qPCR
(2E)
:
•tota
lbac
teri
a
•tota
lmyc
obac
teri
a
•S.rectivirgula
NG
S(1
6SV6
eV8
regi
on)(2D):
•bac
teri
aldi
vers
ity
•Som
esp
ecie
sse
emto
have
apr
efer
ence
for
aero
solis
atio
n
•Sou
rce
mat
eria
lcom
posi
tion
may
notb
ea
good
prox
yof
the
com
posi
tion
&na
ture
ofbi
oaer
osol
s
•May
have
sam
pled
atso
me
ofth
esa
me
faci
litie
sas
Mba
rech
eet
al.
(201
7)
Gut
arow
ska
etal
.(20
18)
Pola
nd1
com
post
ing
faci
lity
Plus
4ot
her
non-
com
post
ing
faci
litie
s(c
emen
tpl
ant,
poul
try
farm
,cul
tivat
edar
ea)
1lo
catio
n(h
omog
enis
atio
nha
ll)w
ith1–
5w
orke
rsPl
usse
ttle
ddu
st(1
.5m
,24
h)
Sam
pler
:
•Dus
tTra
k™D
RXae
roso
lmon
itor
8533
port
able
lase
rph
otom
eter
(3L
min
−1 ,1
ssa
mpl
ing
inte
rval
over
24h,
heig
htof
1.5
m,0
.1–1
5μm
,0.0
01–1
50m
gm
−3 )
Num
bers
:
•n=
3
•tota
lsam
ples
=3
(+n
=3
sett
led
dust
sam
ples
)Ti
min
g:
•1vi
sit
•9th
Sep
2017
Spec
trom
etry(3B)
:
•PM
1
•PM
2.5
•PM
4
•PM
10
•tota
lPM
Cultu
re(s
ettle
ddu
st)(1A):
•tota
lbac
teri
a
•tota
lfun
gi
•xer
ophi
licfu
ngi
•Act
inom
ycet
es
•hae
mol
yticStaphylococcus
•Staphylococcus
spp
•Pseudomonasfluorescens
•Enterobacteriaceae
NG
S(s
ettle
ddu
st)(2D):
•bac
teri
aldi
vers
ity(1
6SrR
NA
V3e
V4re
gion
)
•fung
aldi
vers
ity(I
TSre
gion
)M
TTas
say
(set
tled
dust
)(3E)
:
•cyt
otox
icity
•Fun
gal&
bact
eria
ldiv
ersi
tym
easu
red
inse
ttle
ddu
st
•Sam
pled
the
sam
eco
mpo
stin
gfa
cilit
yas
Gut
arow
ska
etal
.(20
15)
Occupationalexposurestudiesthatalsocontainhealthdata
Hel
dale
tal
.(2
015)
Nor
way
10co
mpo
stin
gfa
cilit
ies
(org
anic
hous
ehol
dw
aste
,sew
age
slud
ge,
orga
nic
food
indu
stry
was
te):
•5op
enw
indr
ow
•5cl
osed
reac
tors
2lo
catio
ns/a
ctiv
ities
:
•com
post
wor
kers
'per
sona
len
viro
nmen
t
•37
office
wor
kers
'per
sona
len
viro
nmen
tPl
us44
sew
age
wor
kers
Sam
pler
:
•per
sona
lPA
S-6
cass
ette
filte
rco
nnec
ted
toan
air
pum
p(2
Lm
in−
1 ,∼6
hsi
ngle
shift
)N
umbe
rs:
•n=
47co
mpo
stw
orke
rs
•n=
37offi
cew
orke
rs
•n=
2pe
rw
orke
r(f
ordi
ffere
ntm
easu
rem
ents
)
•tota
lsam
ples
=16
8
Gra
vim
etry(3A):
•inha
labl
edu
stFl
uore
scen
cem
icro
scop
y(2A):
•non
-bra
nchi
ngba
cter
iaSE
M(2A):
•Act
inom
ycet
essp
ores
•fung
alsp
ores
LAL
assa
y(3C)
:
•end
otox
in
All
sam
ples
exce
eded
BAU
Alim
its
(continuedon
nextpage
)
S. Robertson, et al. International Journal of Hygiene and Environmental Health 222 (2019) 364–386
371
Table1
(continued)
Aut
hor
(yea
r)Co
untr
yN
umbe
r/ty
peof
site
sst
udie
dEx
posu
resa
mpl
ing
loca
tion/
activ
ityEx
posu
resa
mpl
ing
met
hods
aBi
oaer
osol
s/po
lluta
nts
mea
sure
d&
anal
ytic
alm
etho
dsb
Com
men
ts
Tim
ing:
•1m
easu
rem
ent
betw
een
two
heal
thex
amin
atio
ns(1
prio
rto
,&1
follo
win
g,ex
posu
re)
Hel
dale
tal
.(2
016)
Nor
way
10co
mpo
stin
gfa
cilit
ies
•5op
enw
indr
ow
•5cl
osed
reac
tors
Plus
8sl
udge
trea
tmen
tfa
cilit
ies
(4w
ithdr
iers
&4
with
out)
2lo
catio
ns/a
ctiv
ities
:
•com
post
wor
kers
'per
sona
len
viro
nmen
t
•38
office
wor
kers
'per
sona
len
viro
nmen
t
Sam
pler
:
•per
sona
lPA
S-6
cass
ette
filte
rco
nnec
ted
toan
air
pum
p(2
Lm
in−
1 ,4–5
hsi
ngle
shift
)N
umbe
rs:
•n=
47co
mpo
stw
orke
rs
•n=
38offi
cew
orke
rs
•n=
2pe
rw
orke
r(f
ordi
ffere
ntm
easu
rem
ents
)
•tota
lsam
ples
=17
0(3
lost
due
todi
srup
ted
pum
pflo
w)
Tim
ing:
•1m
easu
rem
ent
betw
een
two
heal
thex
amin
atio
ns(1
prio
rto
,&1
follo
win
g,ex
posu
re)
Gra
vim
etry(3A):
•inha
labl
edu
stFl
uore
scen
cem
icro
scop
y(2A):
•tota
lbac
teri
aSE
M(2A):
•Act
inom
ycet
essp
ores
•fung
alsp
ores
LAL
assa
y(3C)
:
•end
otox
in
•Mea
sure
dup
per
leve
lsex
ceed
BAU
Alim
its
•Use
dth
esa
me
com
post
wor
kers
asde
scri
bed
inH
elda
let
al.(
2015
)
Occupationaland
communityexposurestudies
Gao
etal
.(2
018)
Chin
a4
com
post
ing
faci
litie
s(m
ixtu
reof
man
ures
from
catt
le,p
oultr
y&
swin
e,m
ushr
oom
resi
due
&co
rnst
raw
)
5lo
catio
ns/a
ctiv
ities
perf
acili
ty:
•com
post
ing
area
(n=
9)
•pac
kagi
ngar
ea(n
=7)
•offi
cear
ea(n
=8)
•∼25
0m
dow
nwin
d(n
=4)
•plu
s1
sam
ple
∼25
0m
upw
ind
(bac
kgro
und
for
all
faci
litie
s)
Sam
pler
:
•tota
lsus
pend
edpa
rtic
ulat
eim
pact
or(1
00L
min
−1 ,2
4h)
Num
bers
:
•n=
1–3
per
loca
tion/
activ
itype
rfa
cilit
y
•tota
lsam
ples
=29
Tim
ing:
•1vi
sit
per
faci
lity
•Oct
2014
–Oct
2015
NG
S(1
6SrR
NA
V3e
V4re
gion
)(2D):
•bac
teri
aldi
vers
itydd
PCR(2E)
:
•Escherichiacoli
•Sta
phyl
ococ
cus
spp
•cla
ss1
inte
gron
:int
l1
•4A
RGty
pes:
-β-
lact
am-
tetr
acyc
line
-su
lpho
nam
ides
-er
ythr
omyc
in
•22
ARG
subt
ypes
:-
β-la
ctam
:bla
CARB
-4,b
laO
XA-1
8,bl
aOXA
1,bl
aOXA
II,bl
aOXA
III,b
laPS
E,bl
aTEM
-te
trac
yclin
e:te
tQ,t
etM
,tet
S,te
tT,t
etW
,te
tA/P
,tet
G,t
etL,
tetZ
,tet
X-
sulp
hona
mid
es:s
ul1,
sul2
,sul
3,df
rA1
-er
ythr
omyc
in:e
rmB
Paha
riet
al.
(201
6)In
dia
1w
aste
trea
tmen
tfac
ility
with
anop
enw
indr
owco
mpo
stin
gar
ea(v
eget
able
mar
ket
was
te&
mun
icip
also
lidw
aste
[org
anic
mat
ter,
plas
tic,r
ubbe
r,cl
oth,
woo
d,pa
per,
glas
s,m
etal
,san
d/st
one]
)
7lo
catio
ns/a
ctiv
ities
:
•on-
site
,mor
ning
,hig
hac
tivity
inw
aste
rece
ivin
g&
pre-
sort
ing
sect
ion
•on-
site
,lun
chbr
eak,
no/l
owac
tivity
•on-
site
,afte
rnoo
n,hi
ghac
tivity
inth
eco
mpo
stw
indr
ow,&
com
post
refin
emen
t&ba
ggin
gse
ctio
ns
•off-
site
,afte
rnoo
n,∼
200
mEa
st
•off-
site
,afte
rnoo
n,∼
120
mN
orth
-Wes
t
Sam
pler
s:
•six-
stag
eA
nder
sen
impa
ctor
(28.
3L
min
−1 ,2
min
,hei
ght
of1.
2m
)
•Env
iroT
ech
high
volu
me
sam
pler
(1.2
Lm
in−
1 ,30–
95m
in,h
eigh
tof
1.2
m,
<10
μm)
•thre
e-st
age
Siot
uspe
rson
alca
scad
eim
pact
or(9
Lm
in−
1 ,30–
95m
in,h
eigh
tof
1.2
m,0
.5–2
.5μm
&>
2.5
μm)
•use
dsi
mul
tane
ousl
yN
umbe
rs:
•And
erse
n–
n=
2pe
rlo
catio
n/ac
tivity
,to
tals
ampl
es=
14
•Env
iroT
ech
–n
=1
per
loca
tion/
activ
ity,
tota
lsam
ples
=7
And
erse
nsa
mpl
er+
cultu
re(1A):
•non
-fast
idio
usba
cter
ia
•Act
inom
ycet
esA
nder
sen
sam
pler
+cu
lture
+bi
oche
mic
alte
sts
+N
GS
(16S
rDN
A)(1B/1F):
•bac
teri
aldi
vers
ityEn
viro
Tech
sam
pler(3A):
•>PM
10
Siot
usim
pact
or(3A):
•PM
0.5-
2
•>PM
2.5
•Obs
erve
dgo
odco
rrel
atio
nbe
twee
nto
talb
ioae
roso
ls&
aero
sols
(PM
10)
colle
cted
usin
gth
eA
nder
sen
impa
ctor
&En
viro
Tech
sam
pler
,res
pect
ivel
y
•Obs
erve
dbi
oaer
osol
sle
vels
near
the
slum
area
exce
eded
the
reco
mm
ende
dva
lues
•Fac
ility
poss
ibly
cont
ribu
ted
toel
evat
edco
ncen
trat
ions
ofbi
oaer
osol
sin
the
near
bysl
umar
ea
(continuedon
nextpage
)
S. Robertson, et al. International Journal of Hygiene and Environmental Health 222 (2019) 364–386
372
Table1
(continued)
Aut
hor
(yea
r)Co
untr
yN
umbe
r/ty
peof
site
sst
udie
dEx
posu
resa
mpl
ing
loca
tion/
activ
ityEx
posu
resa
mpl
ing
met
hods
aBi
oaer
osol
s/po
lluta
nts
mea
sure
d&
anal
ytic
alm
etho
dsb
Com
men
ts
•off-
site
,afte
rnoo
n,∼
190
mSo
uth-
East
•off-
site
,lun
chbr
eak
&af
tern
oon,
∼15
0–20
0m
Wes
tnea
rsl
umar
ea
•Sio
tus
–n
=1
per
loca
tion/
activ
ity,t
otal
sam
ples
=7
Tim
ing:
•1vi
sit
•Dec
2014
–Mar
2015
Pasc
iak
etal
.(2
014)
Pola
nd1
faci
lity
prod
ucin
gco
mpo
stfo
rm
ushr
oom
grow
ing
7lo
catio
ns/a
ctiv
ities
:
•pro
duct
ion
&sa
les
halls
(n=
9)
•offi
ces&
labo
rato
ries
(n=
7)
•ent
ranc
e(n
=2)
•faci
lity
owne
rs'h
ouse
(100
mfr
omth
efa
cilit
y)(n
=9)
•faci
lity
owne
rs'h
ouse
entr
ance
(n=
2)
•faci
lity
owne
rs'c
ar(n
=2)
•out
door
,∼2
kmfr
omfa
cilit
y(n
=5)
Plus
n=
3–5
surf
ace
sam
ples
(wal
ls&
equi
pmen
tof
the
prod
uctio
nha
ll)&
com
post
sam
ples
Sam
pler
:
•MA
S-10
0Ec
oA
irsa
mpl
er(5
0or
100
L)N
umbe
rs:
•n=
3–5
per
loca
tion/
activ
ity
•tota
lsam
ples
=36
Tim
ing:
•1vi
sit
•Nov
2008
–Feb
2009
Cultu
re(1A):
•tota
lbac
teri
aCu
lture
+bi
oche
mic
al,m
orph
olog
ical
iden
tifica
tion(1B)
:
•aer
ialm
ycel
ium
actin
obac
teri
a
•bac
teri
aldi
vers
ityCu
lture
+ph
ysio
logi
cal,
antib
iotic
susc
eptib
ility
,che
mot
axic
&16
SrR
NA
sequ
enci
ngba
sed
iden
tifica
tion(1B/F)
:
•pre
dom
inan
tac
tinob
acte
rial
stra
in
One
case
ofhy
pers
ensi
tivity
penu
mon
itis
inan
office
wor
ker
(&,
alth
ough
not
clin
ical
lyco
nfirm
ed,
chro
nic
head
ache
s&
wea
knes
sof
othe
rw
orke
rsan
dth
eow
ner's
fam
ilym
embe
rs)
repo
rted
Tam
erVe
stlu
ndet
al.(
2014
)En
glan
d1
open
win
drow
com
post
ing
site
10lo
catio
ns/a
ctiv
ities
:
•sour
ce(w
indr
ow)
usin
ga
win
dtu
nnel
(sta
ticso
urce
)
•sour
ce(w
indr
ow)
from
agita
tion
activ
ities
(agi
tatio
n)
•2by
the
scre
enin
gar
ea
•2at
sour
ce(w
indr
ows)
•10
mdo
wnw
ind
ofw
indr
ows
•50
mdo
wnw
ind
ofw
indr
ows
•100
mdo
wnw
ind
ofw
indr
ows
•50
mup
win
d
Sam
pler
:
•per
sona
lSKC
filte
rsa
mpl
er(2
Lm
in-1
,30
min
,hei
ght
of1.
8m
)N
umbe
rs:
•n=
3
•tota
lsam
ples
=30
Tim
ing:
•1vi
sit
SEM(2A):
•par
ticle
:-
num
ber
-si
ze(0
.5–1
0μm
)-
shap
e-
type
-ag
greg
atio
nst
atus
Communityexposurestudies
Gal
eset
al.
(201
5)Fr
ance
One
gree
nw
aste
open
win
drow
com
post
ing
faci
lity
2lo
catio
nsdu
ring
agita
tion
activ
ities
:
•50
mdo
wnw
ind
•100
mup
win
d
Sam
pler
s:
•11-
stag
eEL
PI™
elec
tric
allo
wpr
essu
reim
pact
or(1
0L
min
−1 ,9
0m
in,3
nm-
10μm
)
•GRI
MM
optic
alpa
rtic
leco
unte
r(1
.2L
min
−1 ,9
0m
in,0
.3–2
0μm
)N
umbe
rs:
•ELP
I™–
n=
1(5
0m
dow
nwin
dlo
catio
non
ly)
per
visi
t,to
tals
ampl
es=
3
•–G
RIM
Mn
=1
per
loca
tion
per
visi
t,to
tals
ampl
es=
8Ti
min
g:
•ELP
I™–
3vi
sits
,11t
h,12
th&
18th
Sep
2012
•GRI
MM
–8
visi
ts,1
0th-1
3th
&17
th-2
0th
Sep
2012
Real
-tim
esp
ectr
osco
py(3B)
:
•par
ticle
:-
num
ber
-si
ze(0
.3–2
0μm
)Cu
lture(1A):
•size
dist
ribu
tion
ofth
erm
ophi
licce
llsqP
CR(2E)
:
•size
dist
ribu
tion
of:
-to
talb
acte
ria
-S.
rect
ivir
gula
&re
lativ
es-
A.f
umig
atus
Flow
cyto
met
ry(2C)
:
•size
dist
ribu
tion
ofto
talm
icro
bial
cells
aW
here
valu
esar
eno
tpr
ovid
edfo
rsp
ecifi
csa
mpl
ing
para
met
ers
(suc
has
flow
rate
,sam
plin
gtim
e,sa
mpl
ing
heig
htet
c.),
they
wer
eno
tre
port
ed.
bN
umbe
rsco
rres
pond
toth
esa
mpl
ing
met
hod
asde
taile
din
App
endi
xC.
S. Robertson, et al. International Journal of Hygiene and Environmental Health 222 (2019) 364–386
373
Table2
Char
acte
rist
ics
ofth
ehe
alth
stud
ies
incl
uded
inth
ere
view
.
Aut
hor
(yea
r)St
udy
desi
gnSe
ttin
gPo
pula
tion/
subj
ects
stud
ied
Expo
sure
asse
ssm
enta
Out
com
eas
sess
men
tBi
oaer
osol
s/po
lluta
nts
stud
ied
Dou
glas
etal
.(2
016)
Cros
s-se
ctio
nals
mal
lar
eaec
olog
ical
stud
y(c
omm
unity
stud
y)
All
perm
itted
indu
stri
al-s
cale
com
post
ing
faci
litie
sop
erat
ing
2008
–201
0,w
ithan
outd
oor
com
post
ing
com
pone
nt,i
nEn
glan
d(n
=14
8;of
whi
ch11
7op
enw
indr
owan
d31
in-v
esse
l)
34,9
63re
spir
ator
yho
spita
lad
mis
sion
sin
4656
cens
usou
tput
area
sw
ithin
250–
2500
mof
aco
mpo
stsi
te
Dis
tanc
efr
omsi
tew
asus
edas
apr
oxy
for
bioa
eros
olex
posu
re(p
re-
defin
eddi
stan
ceba
nds
of0–
250,
250–
750,
750–
1500
and
1500
–250
0m
;dis
tanc
eas
aco
ntin
uous
mea
sure
was
also
exam
ined
)
Emer
genc
yan
dno
n-em
erge
ncy
hosp
itala
dmis
sion
sfo
rpo
stco
dear
eas
(fro
mH
ospi
talE
piso
deSt
atis
tics)
,with
are
spir
ator
y-re
late
dpr
imar
ydi
agno
sis
for
adm
issi
on(a
ccor
ding
toIn
tern
atio
nal
Clas
sific
atio
nof
Dis
ease
(ICD
10)
code
)(a
lso
stra
tified
into
resp
irat
ory
infe
ctio
ns,a
sthm
a,an
dch
roni
cob
stru
ctiv
epu
lmon
ary
dise
ase
(CO
PD))
Non
e(d
ista
nce
used
asa
prox
yfo
rbi
oaer
osol
expo
sure
)
Gut
arow
ska
etal
.(2
018)
Lab-
base
dto
xico
logi
cals
tudy
(occ
upat
iona
lstu
dy)
Aco
mpo
stin
gfa
cilit
y,tw
oce
men
tfa
cilit
ies,
apo
ultr
yfa
rman
da
culti
vate
dar
ealo
cate
din
Pola
nd
No
subj
ects
–th
eA
-549
cell
line
(hum
anad
enoc
arci
nom
alu
ngep
ithel
iala
dher
ent
cells
)w
asus
edto
anal
ysis
the
toxi
city
ofdu
stco
llect
edfr
om4
wor
king
envi
ronm
ents
Mea
sure
men
tte
chni
que:
Air
born
edu
stco
ncen
trat
ion
was
mea
sure
dby
usin
ga
Dus
tTra
k™D
RXA
eros
olM
onito
r85
33po
rtab
lela
ser
phot
omet
er(T
SI).
Mea
sure
men
tsob
tain
edat
ahe
ight
of1.
5m
from
grou
ndle
veli
ntr
iplic
ate
for
each
loca
tion,
with
asa
mpl
ing
rate
of3
Lm
inan
da
sam
plin
gin
terv
alof
1s.
Als
o,se
ttle
ddu
stsa
mpl
es(p
arto
fai
rbor
nepa
rtic
ulat
em
atte
r(PM
)tha
tfe
lldo
wn
onto
sam
plin
gsu
rfac
edu
ring
wor
kac
tiviti
es)
was
colle
cted
onto
5gl
ass
plat
es(p
ositi
oned
1.5
mfr
omgr
ound
leve
l)fo
r24
h.Id
entifi
catio
n/en
umer
atio
nof
mic
robi
alco
mm
unity
Iden
tifica
tion
ofba
cter
iaan
dfu
ngi
byce
llcu
lture
met
hods
and
byus
ing
poly
mer
ase
chai
nre
actio
n(P
CR)
ampl
ifica
tion
and
sequ
enci
ngof
ribo
som
alRN
A.
The
MTT
assa
yw
asus
edto
anal
yse
the
cyto
toxi
city
and
cell
viab
ility
ofhu
man
lung
aden
ocar
cino
ma
epith
elia
lcel
ls(A
-549
)ex
pose
dto
dust
sam
ples
.
Xero
phili
cfu
ngia
ndno
n-xe
roph
ilic
spec
ies,
tota
lnum
ber
ofba
cter
ia,
haem
olyt
icStaphylococcus
,A
ctin
omyc
etes
,man
nito
l-pos
itive
Staphylococcus
spp,Pseudomonas
fluorescens
,Enterobacteriaceae
;se
quen
cing
regi
ons
ofrR
NA
gene
sfro
mba
cter
ia(1
6S)
and
fung
i(IT
S);m
ass
conc
entr
atio
nsof
size
-seg
rega
ted
part
icle
s(P
Mto
tal,
PM10
,PM
4,PM
2.5
&PM
1)
Hel
dale
tal
.(2
015)
Occ
upat
iona
lqua
si-
expe
rim
enta
l(pr
e-po
stsh
ift)
5W
indr
ow(m
ainl
you
tdoo
r)co
mpo
stin
gsi
tes
and
5re
acto
r(c
ompo
stin
gm
ainl
yin
door
s)fa
cilit
ies
inN
orw
ay
47w
orke
rs(2
0w
indr
owco
mpo
stw
orke
rs;2
7re
acto
rfa
cilit
yw
orke
rs)
and
37un
expo
sed
cont
rols
(mai
nly
whi
teco
llar
wor
kers
from
the
adm
inis
trat
ion
atth
efa
cilit
ies)
Pers
onal
filte
rsa
mpl
ers
(PA
S-6
cass
ette
s)at
aflo
wra
teof
2L
min
−1
2di
ffere
ntfil
ters
wer
eus
ed:(
1)po
lyca
rbon
ate
filte
r(p
ore
size
0.8
μm)
for
mic
robi
olog
ical
anal
ysis
(tot
alba
cter
ia,f
unga
l&A
ctin
omyc
etes
spor
es);
(2)g
lass
fibre
filte
rsfo
ren
doto
xins
Self-
adm
inis
tere
dqu
estio
nnai
re,
spir
omet
ry,a
cous
ticrh
inom
etry
,bl
ood
sam
ples
colle
cted
(pos
t-shi
fton
ly)
for
mea
sure
men
tof
bloo
dpn
eum
opro
tein
s(C
C16;
SP-A
;SP-
D)
Endo
toxi
n,fu
ngal
spor
es,
Act
inom
ycet
essp
ores
,non
-bra
nchi
ngba
cter
ia,i
nhal
able
dust
Hel
dale
tal
.(2
016)
Occ
upat
iona
lqua
si-
expe
rim
enta
l(pr
e-po
stsh
ift)
10co
mpo
stfa
cilit
ies
(5w
indr
owfa
cilit
ies&
5re
acto
rfac
ilitie
s)an
d8
sew
age
slud
getr
eatm
ent
faci
litie
sin
Nor
way
47co
mpo
stw
orke
rs(a
sde
scri
bed
inH
elda
let
al.(
2015
)),4
4se
wag
efa
cilit
yw
orke
rs(1
9fr
om4
faci
litie
sus
ing
slud
gedr
ying
,25
from
4fa
cilit
ies
that
didn
'tus
esl
udge
dryi
ng),
38un
expo
sed
cont
rols
(all
adm
inis
trat
ive
staff
from
the
faci
litie
s;28
from
the
com
post
faci
litie
s&
9fr
omth
ese
wag
etr
eatm
ent
faci
litie
s)
Pers
onal
filte
rsa
mpl
ers
(PA
S-6
cass
ette
s)at
aflo
wra
teof
2L
min
−1
for
appr
ox.4
–5h
2di
ffere
ntfil
ters
wer
eus
ed:(
1)po
lyca
rbon
ate
filte
r(p
ore
size
0.8
μm)
for
mic
robi
olog
ical
anal
ysis
(tot
alba
cter
ia,f
unga
l&A
ctin
omyc
etes
spor
es);
(2)g
lass
fibre
filte
rsfo
ren
doto
xins
Pers
onal
filte
rsa
mpl
ers
(PA
S-6
cass
ette
s)at
aflo
wra
teof
2L
min
−1
for
appr
oxim
atel
y5–
6h
Post
-shi
fton
lySe
lf-ad
min
iste
red
ques
tionn
aire
spir
omet
ry,b
lood
sam
ples
colle
cted
for
mea
suri
ngle
vels
(con
cent
ratio
ns)
ofbi
omar
kers
ofin
flam
mat
ion
(CRP
;IC
AM
-1,V
CAM
),co
agul
atio
n(fi
brin
ogen
,D-d
imer
)an
dal
lerg
en-
spec
ific
IgE
antib
odie
s
Inha
labl
edu
st,t
otal
bact
eria
,fun
gal
spor
es,A
ctin
omyc
etes
spor
es,
endo
toxi
n
Expo
sure
asse
ssm
ent
not
cond
ucte
dEx
posu
reas
sess
men
tnot
cond
ucte
d
(continuedon
nextpage
)
S. Robertson, et al. International Journal of Hygiene and Environmental Health 222 (2019) 364–386
374
Table2
(continued)
Aut
hor
(yea
r)St
udy
desi
gnSe
ttin
gPo
pula
tion/
subj
ects
stud
ied
Expo
sure
asse
ssm
enta
Out
com
eas
sess
men
tBi
oaer
osol
s/po
lluta
nts
stud
ied
Hoff
mey
eret
al.
(201
4)O
ccup
atio
nalc
ross
-se
ctio
nals
tudy
31co
mpo
stin
gsi
tes
inno
rth-
wes
tern
Ger
man
y19
0cu
rren
tlyex
pose
dco
mpo
stw
orke
rs,5
9fo
rmer
com
post
wor
kers
,38
whi
te-c
olla
rw
orke
rsw
ithou
toc
cupa
tiona
lexp
osur
e
Self-
adm
inis
tere
dqu
estio
nnai
redi
agno
sis
ofch
roni
cbr
onch
itis,
rhin
itis
and
conj
unct
iviti
sw
asba
sed
onth
epr
opor
tion
ofse
lf-re
port
edsy
mpt
oms,
spir
omet
ryw
asus
edto
diag
nose
COPD
and
the
GO
LDcl
assi
ficat
ion
syst
emw
asus
edto
cate
gori
sedi
seas
ese
veri
ty(I
-IV),
scor
e-ba
sed
diag
nosi
sof
asth
ma
(inc
lude
da
ques
tionn
aire
&ex
amin
atio
nfo
rcl
inic
alm
easu
res
ofas
thm
a&
atop
y)H
offm
eyer
etal
.(2
015)
Occ
upat
iona
lcro
ss-
sect
iona
lstu
dy31
com
post
ing
site
sin
nort
h-w
este
rnG
erm
any
119
curr
ently
expo
sed
com
post
wor
kers
,str
atifi
edby
smok
ing
and
atop
y(f
rom
sam
eco
hort
asus
edin
Hoff
mey
eret
al.(
2014
))
Self-
adm
inis
tere
dqu
estio
nnai
res
(dai
lytim
epe
rta
sk,p
erso
nal
prot
ectiv
ede
vice
uses
)and
resu
ltsof
ambi
ent
mon
itori
ngat
wor
kpla
ces
was
used
toca
tego
rise
subj
ects
into
2ex
posu
regr
oups
:hig
han
dlo
wle
vel
expo
sure
Air
way
infla
mm
atio
n/ox
idat
ive
stre
ssus
ing:
(1)
exha
led
brea
thco
nden
sate
(EBC
)co
llect
ion
for
pH&
conc
entr
atio
nsof
eico
sano
ids
and
(2)
frac
tiona
lexh
aled
nitr
icox
ide
(FeN
O)
Bloo
dsa
mpl
esco
llect
edfo
rm
easu
ring
leve
ls(c
once
ntra
tions
)of
alle
rgen
-spe
cific
IgE
antib
odie
s
Non
e
Raul
fet
al.
(201
5)O
ccup
atio
nalc
ross
-se
ctio
nals
tudy
31co
mpo
stin
gsi
tes
inno
rth-
wes
tern
Ger
man
y14
0cu
rren
tlyex
pose
dco
mpo
stw
orke
rs,4
9fo
rmer
com
post
wor
kers
and
29w
hite
-col
lar
wor
kers
from
sam
eco
hort
asus
edin
Hoff
mey
eret
al.(
2014
)
Expo
sure
asse
ssm
ent
not
cond
ucte
dSe
lf-ad
min
iste
red
ques
tionn
aire
,di
agno
sis
ofch
roni
cbr
onch
itis
was
base
don
aco
mbi
natio
nof
the
prop
ortio
nof
self-
repo
rted
sym
ptom
san
dsp
irom
etry
test
;blo
odsa
mpl
esco
llect
edfo
ral
lerg
en-s
peci
ficIg
Ete
st(a
llerg
yde
tect
ion)
,ind
uced
sput
umw
asan
alys
edfo
rtot
alan
ddi
ffere
ntia
lce
llula
rco
unts
and
for
conc
entr
atio
nsof
tota
lpro
tein
,sol
uble
CD14
,MM
P-9,
8-is
o-PG
F 2α
and
IL-8
Expo
sure
asse
ssm
entn
otco
nduc
ted
van
Kam
pen
etal
.(2
016)
Occ
upat
iona
lcoh
ort
stud
y13
-yea
rfo
llow
-up
(199
6/7–
2009
)
31co
mpo
stin
gsi
tes
inno
rth-
wes
tern
Ger
man
y74
curr
ently
expo
sed
com
post
wor
kers
,42
form
erco
mpo
stw
orke
rs(w
hoha
dle
ftdu
ring
the
13-y
ear
follo
w-u
p)an
d37
non-
expo
sed
cont
rols
(fro
msa
me
coho
rtas
used
inH
offm
eyer
etal
.(20
14))
Expo
sure
asse
ssm
ent
not
cond
ucte
dEx
posu
regr
oups
(cur
rent
,for
mer
,co
ntro
ls)
cate
gori
sed
into
coug
h,co
ugh
with
phle
gmor
chro
nic
bron
chiti
sbas
edon
prop
ortio
nof
self-
repo
rted
sym
ptom
s,bl
ood
sam
ples
colle
cted
for
alle
rgen
-spe
cific
IgE
test
(alle
rgy
dete
ctio
n),i
ndic
esde
rive
dfr
omsp
irom
etry
wer
eus
edto
diag
nose
COPD
Expo
sure
asse
ssm
entn
otco
nduc
ted
aSe
eTa
ble
1fo
rde
tails
.Whe
reva
lues
are
not
prov
ided
for
spec
ific
sam
plin
gpa
ram
eter
s(s
uch
asflo
wra
te,s
ampl
ing
time,
sam
plin
ghe
ight
etc.
),th
eyw
ere
not
repo
rted
.
S. Robertson, et al. International Journal of Hygiene and Environmental Health 222 (2019) 364–386
375
measured values. The highest concentrations of total bacteria weremeasured on personal samplers worn by workers and on site (Fig. 3). Asimilar pattern was observed for total fungi concentrations (Fig. 4). Notall studies measured or reported upwind/background concentrations,so it was not always possible to tell if on-site concentrations were di-rectly attributable to composting activities. Four studies (Bonifait et al.,2017; Gutarowska et al., 2015; Heldal et al., 2015, 2016 report thatsome levels exceeded Polish limits of 100,000 CFU m−3 for mesophilicbacteria. All samples reported by Heldal et al. (2015) exceeded thePolish limits, although one of these is a background measurement in-dicating that there are high levels of naturally occurring bacteria, andreported bacterial cells, not CFU, which may not be mesophilic orcompletely comparable. High background measurements were alsoobserved for Bonifait et al. (2017). One of the two (Heldal et al., 2016)
samples exceeded Polish limits, but background values were not pro-vided. The upper limits of one sample exceed the Polish limits inGutarowska et al. (2015), but as the mean concentration does not ex-ceed this limit, the authors concluded that total microorganisms did notexceed quantitative thresholds. Four studies (Bonifait et al., 2017;Gutarowska et al., 2015; Heldal et al., 2015, 2016 report some levelsthat exceeded German occupational technical control values of50,000 CFU m−3 for mesophilic fungi (TBRA, 2019) and Polish limitsfor fungi, which is also 50,000 CFU m−3 (Gutarowska et al., 2015). Allsamples reported by Heldal et al. (2015), and the upper limits of Heldalet al. (2016) exceeded German technical control values/Polish limits,although one of the Heldal et al. (2015) samples is a backgroundmeasurement indicating high levels of naturally occurring fungi, andfungal spores are presented in this study, which are not necessary
Fig. 3. Mean (or median if mean is not reported) airborne total bacteria concentrations at different location reported in studies with exposure data. Error barsrepresent minimum and maximum concentrations (or standard deviation if minima and maxima not reported), if reported in the study. Location A = Background/Upwind, B=Office, C=Compost Hall, D = Personal, E = Waste receiving area, F= On Site, G = Bagging area, H=Screening, I = Downwind (at an unspecifieddistance), J = Downwind 100 m, K = Downwind 200 m, L = Downwind 2000 m. Results from Gutarowska et al. (2018) are not included as they measured settled(not airborne) dust. The red line represents the Polish Committee for the Highest Permissible Concentrations and Intensities of Noxious Agents in the Workplace limitfor mesophilic bacteria, which is 100,000 CFU m−3 (Gutarowska et al., 2015). See Table 1 for exposure study characteristics. (1) Some measurements in Bonifait et al.(2017) were reported as genomes m−3. (2) Results in (Heldal et al., 2015) were reported as cells m−3. (3) Results in Heldal et al. (2016) were reported as bacteriam−3. (4) Pasciak et al. (2014) reported measurements taken at offsite locations and provided approximate distances from site, but did not explicitly state thesemeasurements were taken downwind. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
Fig. 4. Mean (or median if mean is not re-ported) airborne total fungi concentrations atdifferent location reported in studies withexposure data. Error bars represent minimumand maximum concentrations, if reported inthe study. Location A = Background/Upwind,B=Office, C=Compost Hall, D = Personal,E = On Site, F=Screening. Results fromGutarowska et al. (2018) are not included asthey measured settled (not airborne) dust. Thered line represents the German technicalcontrol value of 50,000 CFU m−3 for meso-philic fungi (TBRA, 2019) and the PolishCommittee for the Highest Permissible Con-centrations and Intensities of Noxious Agentsin the Workplace limit for fungi, which is also50,000 CFU m−3 (Gutarowska et al., 2015).See Table 1 for exposure study characteristics.(1) Presented results as spores m−3. (For in-terpretation of the references to colour in thisfigure legend, the reader is referred to theWeb version of this article.).
S. Robertson, et al. International Journal of Hygiene and Environmental Health 222 (2019) 364–386
376
mesophilic. One sampling point and the upper limits of two samplingpoints in Bonifait et al. (2017) who did present results for mesophilicmould exceed German technical control values/Polish limits, however,upwind values are not provided. The measured levels in Gutarowskaet al. (2015) exceed the German technical control value; airborne fungiwas measured in this study, which may or may not include mesophilicfungi.
It was only possible to extract endotoxin concentrations from twostudies (Heldal et al., 2015, 2016. Both studies measured personal en-dotoxin exposures from composting workers. Heldal et al. (2015) re-ported mean concentrations of 4–38 EU m−3 (range 0–730 EU m−3),and Heldal et al. (2016) reported a median concentration of 3 EU m−3
(range 1–310 EU m−3). The upper limits of endotoxin concentrationsreported in these studies exceed proposed Dutch limits of 90 EU m−3
(DECOS, 2010), however, both studies sampled for less than 8 h, andthe proposed Dutch limits are an 8 h time weighted average.
As there were only five studies that included community exposuremeasurements, it was not possible to determine how bioaerosol con-centration may deplete downwind from the composting facilities.Pasciak et al. (2014) reported measurements from several offsite loca-tions, and detected total bacteria and Actinobacteria 2 km from the site.However, it was not clear whether these were taken downwind or up-wind of composting activities, and therefore whether these werenaturally occurring bioaerosols, or emitted from the composting site.
The studied bioaerosol characteristics are summarised in Table 1,including (but not limited to) total bacteria, endotoxin, actinomycetes,Legionella, total fungi/mould, and Aspergillus fumigatus. The levels ofmicroorganisms detected by the exposure studies are summarised inAppendix D, and the microbial genera detected in two or more studies issummarised in Fig. 5. The key fungal genera detected were Aspergillus,Penicillium, and Cladosporium. The predominant bacterial general weremostly gram-positive (Staphylococcus, Bacillus and Kocuria) with somegram-negative genera such as Pseudomonas. The inhalable dust/parti-culate matter concentrations ranged from 2.29 × 10−1 –5.00 × 104 μg m−3.
3.2.3. Bioaerosol size distributionSix studies examined the size distribution of the microbial con-
stituent of bioaerosols. Two observed that the majority of fluorescingparticles were small, with a diameter of < 2 μm (Feeney et al., 2018) or0.5–3.0 μm (O'Connor et al., 2015); and generally elongated to ellip-soidal/spherical in shape (O'Connor et al., 2015). Likewise, four studiesreported that the predominant bacterial particles were small and thus insingle cell form, in the range of 0.95–2.40 μm (mean 1.3 μm) (Galeset al., 2015); < 1 μm (Tamer Vestlund et al., 2014); 0.65–1.1 and1.2–2.1 μm (Gutarowska et al., 2015); or 0.65–2.1 μm (Pahari et al.,2016); and spherical (Tamer Vestlund et al., 2014). Only one study alsomeasured the size distribution of fungal particles (Gutarowska et al.,2015). They demonstrated that, in contrast to bacterial particles, fungalparticles within the facility were heavily influenced by those present inthe atmospheric air, with particles of 1.1–2.1 and 2.1–3.3 μm pre-dominating in both indoor and outdoor air (Gutarowska et al., 2015).
Five studies collected data on the size distribution of inhalable dust/particulate matter. However, only two reported full analysis of thisdata, both of which observed an increase in small particulatematter < 1 μm (Gutarowska et al., 2018) or 0.6–1.8 μm (Gales et al.,2015). These particles could be of both non-microbial and microbialorigin, and in combination with the data above suggest that much of thesmall particulate matter may be single bacterial cells. Two studies usedthe data to demonstrate that there was increase in fluorescent bioaer-osols over non-fluorescent particles during compost facility activityreporting the ratio/difference only (Feeney et al., 2018); or that therewas a greater association of bacteria with PM > 2.5 μm (Pahari et al.,2016). The remaining study failed to report any (non-fluorescent) dustdata (O'Connor et al., 2015).
3.3. Health studies
Eight health studies relating to bioaerosols from composting facil-ities were published since (Pearson et al., 2015). All were conducted inEurope. The majority (6 out of 8) were in occupational groups (i.e.compost workers). Of the eight health studies, four were cross-sectionalin design (Douglas et al., 2016; Hoffmeyer et al., 2014, 2015; Raulfet al., 2015), two were pre-post exposure, quasi-experimental in design(Heldal et al., 2015, 2016), one was a prospective cohort (van Kampenet al., 2016), and one was a laboratory-based study (Gutarowska et al.,2018), examining the cytotoxicity of compost dust samples in humanepithelial A-549 cells. Only three of the health studies combinedbioaerosol exposure data with health information and all were oncompost workers (Gutarowska et al., 2018; Heldal et al., 2015, 2016). Afourth community health-based study used distance from site as a proxyof exposure (Douglas et al., 2016). The full characteristics for bothoccupational and community based studies are displayed in Table 2.
3.3.1. Occupational health studiesFor the six occupational-based health studies, sample sizes ranged
from 84 to 262 compost workers. Various outcome measures or end-points were used, but chiefly related to respiratory health. The studiestypically used a combination of both subjective (based on self-report,usually questionnaires) and objective measures (based on direct phy-siological measurement). For each study, only a small number of thetotal endpoints examined showed statistically significant association asreported in Table 3 and described further in the text below.
3.3.1.1. Baseline lung function. Three papers including one prospectivecohort study (van Kampen et al., 2016) and two quasi-experimentalstudies (Heldal et al., 2015, 2016), reported baseline spirometryindices. All three (Heldal et al., 2015, 2016; van Kampen et al., 2016)reported a lower FEV1/FVC ratio (ratio of the forced expiratory volumein the first 1 s to the forced vital capacity of the lungs) at baseline incompost workers compared to non-exposed controls; although only onefound significant (p < 0.05) differences (Heldal et al., 2015). The non-exposed control groups consisted of administrative staff from within(Heldal et al., 2015, 2016) or outside (van Kampen et al., 2016) thecomposting facilities. The study by van Kampen and colleaguesincluded current and former compost workers and observed nodifference in the FEV1/FVC ratio measured at baseline (van Kampenet al., 2016).
3.3.1.2. Post-shift decline in lung function. One study investigated acutecross-shift changes in lung function among compost workers (Heldalet al., 2015). Heldal and co-workers reported a lower FEV1/FVC ratio in47 Norwegian compost workers (20 employed at five windrow facilitiesand 27 employed at five reactor facilities) (Heldal et al., 2015).Personal samplers were used to measure full-shift exposuremeasurements at the same time as health examinations and thisindicated that the cross-shift decline in the FEV1/FVC ratio wasassociated with exposure to actinomycetes spores (p = 0.003).
3.3.1.3. Long-term decline in lung function. One study examined changesin lung function in workers (74 currently exposed compost workers, 42former workers and 37 controls) over a 13-year follow-up (van Kampenet al., 2016). There was no difference in the magnitude of changes inFVC or FEV1 during the follow-up period in active and former Germancompost workers compared with non-exposed control subjects(administrative employees from outside the composting operations),after taking into account smoking status.
3.3.1.4. Cough, chronic bronchitis and COPD. A quasi-experimental(Heldal et al., 2015) and cross-sectional (Hoffmeyer et al., 2014)study measured self-reported cough symptoms with prevalence'sranging from 14.6% to 45% and odd ratios (ORs) ranging from 4.1 to
S. Robertson, et al. International Journal of Hygiene and Environmental Health 222 (2019) 364–386
377
Fig. 5. The number of studies detecting bioaerosols/pollutants (left), and microorganisms (middle and right), measured in studies with exposure measurements.Some studies classified microbes at phylum/division level (middle), but some classified further to genus level (right). See Appendix D for a full list of the micro-organisms detected by the exposure studies. Only microorganisms that were measured in two or more studies are included. (1) Total bacteria (n = 10) and my-cobacteria (n = 2). (2) Endotoxin are molecules found in the outer membrane of gram-negative bacteria. (3) Dust/particulates (n = 6), fluorescing particles (n = 2).(4) All (n = 2) were Ustilaginomycetes class. (5) n = 2 measured to phylum/division level only. (6) All (n = 3) were of the Bacteroides genus. (7) All (n = 2) were ofthe Ktedonobacteria class. (8) n = 8 measured to phylum/division level only (9). n = 3 measured to phylum/division level only. NOTE: Heldal et al. (2015) andHeldal et al. (2016) may have reported results from the same samples, and counted twice in the figure, although this is not clear in the manuscripts.
S. Robertson, et al. International Journal of Hygiene and Environmental Health 222 (2019) 364–386
378
Table3
Sign
ifica
ntre
sults
from
the
heal
thst
udie
s.
Aut
hor
(yea
r)Su
bjec
tin
form
atio
nH
ealth
outc
ome
Conf
ound
ers
Sign
ifica
ntfin
ding
sCo
mm
ents
Odd
sra
tios
(ORs
)/re
lativ
eri
sks
(RR)
and
p-va
lues
and
95%
confi
denc
ein
terv
als
(CI)
whe
rere
port
ed
Occ
upat
iona
lstu
dies
Hel
dale
tal
.(2
015)
47w
orke
rs(2
0w
indr
owco
mpo
stw
orke
rs;2
7re
acto
rfa
cilit
yw
orke
rs)
and
37un
expo
sed
cont
rols
mai
nly
whi
teco
llar
wor
kers
from
the
adm
inis
trat
ion
atth
efa
cilit
ies
Sam
eda
yse
lf-re
port
edqu
estio
nnai
reto
asse
sspu
lmon
ary,
gast
ro-in
test
inal
(GI)
,an
dge
nera
lsym
ptom
s/ill
ness
esSp
irom
etry
(FEV
1,FV
C)m
easu
rem
ents
take
npr
e-an
dpo
st-s
hift.
Aco
ustic
rhin
omet
rym
easu
red
pre-
and
post
-shi
ft.
Adj
uste
dfo
rag
ean
dsm
okin
gA
djus
ted
fors
mok
ing,
age
and
atop
yA
djus
ted
for
smok
ing
and
age
Coug
hin
win
drow
site
wor
kers
(OR:
4.3
(CI:
1.0–
18.2
)).O
neor
mor
ew
ork-
rela
ted
sym
ptom
sin
win
drow
site
wor
kers
(OR:
4.0
(CI:
1.1–
14.7
,p
<0.
05))
.Sym
ptom
sw
ere
incr
ease
din
the
mid
dle
expo
sure
cate
gory
ofA
ctin
omyc
etes
spor
esfo
rco
ugh
(OR:
4.3
(CI:
1.1–
16.0
,p<
0.05
)),
uppe
rai
rway
irri
tatio
n(O
R:6.
2(C
I:1.
5–25
.0,
p<
0.05
)),n
ose
irri
tatio
n(O
R:6.
1(C
I:1.5
–25.
0,p
<0.
05))
,one
orm
ore
airw
aysy
mpt
oms
(OR:
3.8
(CI:
1.1–
13.0
,p<
0.05
)),a
ndon
eor
mor
ew
ork-
rela
ted
sym
ptom
s(O
R:4.
5(C
I:1.2
–17.
0,p
<0.
05))
,Cou
ghw
asal
soin
crea
sed
with
the
mid
dle
expo
sure
cate
gory
ofba
cter
ia(O
R:3.
9(C
I:1.1
–14.
0,p
<0.
05))
,end
otox
ins
(OR:
4.7
(CI:1
.2–1
9.0,
p<
0.05
)),a
nddu
st(O
R:4.
9(C
I:1.3
–19.
0,p
<00
.5))
Pred
icte
dFV
C%lo
wer
for
allc
ompo
stw
orke
rs(1
02.2
%)
and
reac
tor
faci
lity
wor
kers
(102
.3%
)co
mpa
red
toco
ntro
ls(1
09.5
%)(
p<
0.05
).Cr
oss-
shift
decr
ease
inFE
V 1/F
VCra
tioin
the
mid
dle
expo
sure
cate
gory
for
Act
inom
ycet
es(−
3.2%
,p
<0.
05)
Cros
s-sh
iftde
crea
sein
the
oute
rvo
lum
eof
the
nasa
lcav
ity(T
VOL1
)am
ong
allw
orke
rs(−
0.22
cm3
p<
0.05
)an
dre
acto
rfa
cilit
yw
orke
rs(−
0.28
cm3
p<
005)
.
Adm
inis
trat
ive
staff
atth
esi
tes
are
nott
rue
popu
latio
n-ba
sed
cont
rols
–i.e
.sub
ject
slik
ely
tobe
mor
eex
pose
dth
ange
nera
lpo
pula
tion.
Asl
ight
expo
sure
amon
gth
eco
ntro
lsw
ould
resu
ltin
anun
dere
stim
atio
nof
effec
ts.T
here
was
also
ahi
gher
prop
ortio
nof
fem
ales
inth
eco
ntro
lgro
up.
The
use
ofre
spir
ator
ypr
otec
tion
(whi
chw
asno
tcon
trol
led
for)
was
mos
tpre
vale
ntin
wor
kers
inth
ehi
ghes
texp
osur
eca
tego
ryan
dex
plai
nth
elo
wer
risk
for
self-
repo
rted
sym
ptom
sin
this
grou
pco
mpa
red
toth
em
iddl
eex
posu
reca
tego
rySu
bjec
tsw
ere
notb
linde
dto
the
expo
sure
cond
ition
and
the
dura
tion
ofem
ploy
men
tof
the
wor
kers
was
not
spec
ified
.The
stat
istic
alpo
wer
was
also
limite
dby
the
smal
lsiz
eof
the
resp
onde
ntpo
pula
tion.
Hel
dale
tal
.(2
016)
47co
mpo
stw
orke
rs(a
sde
scri
bed
inH
elda
let
al.(
2015
)),4
4se
wag
efa
cilit
yw
orke
rs(1
9fr
om4
faci
litie
sus
ing
slud
gedr
ying
,25
from
4fa
cilit
ies
that
didn
'tus
esl
udge
dryi
ng),
38un
expo
sed
cont
rols
(all
adm
inis
trat
ive
staff
from
the
faci
litie
s;28
from
the
com
post
faci
litie
s&
9fr
omth
ese
wag
etr
eatm
ent
faci
litie
s)
Spir
omet
ry(F
EV1,
FVC)
mea
sure
men
tsta
ken
pre-
and
post
-shi
ftPo
st-s
hift
bloo
dsa
mpl
efo
rth
ede
term
inat
ion
ofbi
omar
kers
ofin
flam
mat
ion
(IL-
6,IC
AM
-1,V
CAM
-1,
CRP)
and
coag
ulat
ion
(D-D
imer
,fib
rino
gen)
spec
ific
alle
rgen
s
Adj
uste
dfo
rag
e,sm
okin
g,ge
nder
and
atop
yA
ll(c
ompo
st&
sew
age
wor
kers
com
bine
d)ex
pose
dsu
bjec
tsha
dlo
wer
FVC
(100
.3%
)th
anco
ntro
ls(1
09.5
%)
CRP,
fibri
noge
nan
dIC
AM
-1si
gnifi
cant
ly(p
<0.
05)
high
erin
alle
xpos
edco
mpa
red
toco
ntro
ls.W
hen
stra
tifyi
ngin
tose
wag
eor
com
post
wor
kers
,fibr
inog
en(p
<0.
05)
and
ICA
M-1
(p=
0.01
)re
mai
ned
sign
ifica
ntly
high
erin
com
post
wor
kers
com
pare
dto
the
cont
rols
.N
onlin
ear
asso
ciat
ions
betw
een
seru
mCR
Pan
dFE
V 1an
dFV
Cw
ere
obse
rved
(dec
line
inFE
V 1st
artin
gat
aCR
Pco
ncen
trat
ion
ofap
prox
imat
ely
2m
gL−
1 ).Se
rum
conc
entr
atio
nsof
ICA
M-1
wer
eas
soci
ated
with
CRP
conc
entr
atio
nsw
hen
cons
ider
ing
allw
orke
rs(I
CAM
-1=
290
+62
.5Ig
CRP,
p<
0.01
)(a
ndfo
rth
ese
wag
ean
dco
mpo
stw
orke
rsse
para
tely
)IC
AM
-1co
ncen
trat
ions
wer
epo
sitiv
ely
asso
ciat
edw
ithdu
st(β
=38
.6,p
<0.
05)
and
bact
eria
(β=
23.0
,p<
0.05
)ex
posu
ream
ong
alle
xpos
edw
orke
rs.
Adm
inis
trat
ive
staff
atth
esi
tes
are
nott
rue
popu
latio
n-ba
sed
cont
rols
–i.e
.sub
ject
slik
ely
tobe
mor
eex
pose
dth
ange
nera
lpo
pula
tion.
Asl
ight
expo
sure
amon
gth
eco
ntro
lsw
ould
resu
ltin
anun
dere
stim
atio
nof
effec
ts.
Infla
mm
ator
ym
arke
rsm
aybe
conf
ound
edby
obes
ity(B
MIw
asno
tmea
sure
d)Su
bjec
tsw
ere
notb
linde
dto
the
expo
sure
cond
ition
and
the
dura
tion
ofem
ploy
men
tof
the
wor
kers
was
not
spec
ified
.The
stat
istic
alpo
wer
was
also
limite
dby
the
smal
lsiz
eof
the
resp
onde
ntpo
pula
tion.
(continuedon
nextpage
)
S. Robertson, et al. International Journal of Hygiene and Environmental Health 222 (2019) 364–386
379
Table3
(continued)
Aut
hor
(yea
r)Su
bjec
tin
form
atio
nH
ealth
outc
ome
Conf
ound
ers
Sign
ifica
ntfin
ding
sCo
mm
ents
Odd
sra
tios
(ORs
)/re
lativ
eri
sks
(RR)
and
p-va
lues
and
95%
confi
denc
ein
terv
als
(CI)
whe
rere
port
ed
Hoff
mey
eret
al.
(201
4)19
0cu
rren
tlyex
pose
dco
mpo
stw
orke
rs,
59fo
rmer
com
post
wor
kers
,38
whi
te-
colla
rw
orke
rsw
ithou
toc
cupa
tiona
lex
posu
re
Self-
adm
inis
tere
dqu
estio
nnai
redi
agno
sis
ofch
roni
cbr
onch
itis
Eye
and
nose
irri
tatio
nas
sess
edby
self-
adm
inis
tere
dqu
estio
nnai
reSp
irom
etry
was
used
todi
agno
seCO
PDan
dth
eG
OLD
clas
sific
atio
nsy
stem
was
used
toca
tego
rise
dise
ase
seve
rity
(I-IV
)
Befo
read
just
men
tA
fter
adju
stm
entf
orth
eeff
ect
ofag
e,sm
okin
gha
bits
,BM
Ian
dat
opy
Befo
read
just
men
tA
fter
adju
stm
entf
orth
eeff
ect
ofag
e,sm
okin
gha
bits
,BM
Ian
dat
opy
Befo
read
just
men
t
Chro
nic
bron
chiti
sw
ashi
ghes
tam
ongs
tfor
mer
wor
kers
(25.
5%)
com
pare
dto
curr
ent
wor
kers
(4.5
%)
and
cont
rols
(9.1
%).
Prev
alen
ceof
chro
nic
bron
chiti
sdi
ffere
dsi
gnifi
cant
lyfr
omco
ntro
lsu
bjec
tsfo
rfo
rmer
wor
kers
(p<
0.00
01),
butn
otcu
rren
tw
orke
rs.
Com
pare
dto
neve
rsm
oker
s,pr
eval
ence
ofch
roni
cbr
onch
itis
was
sign
ifica
ntly
high
erin
curr
ent
smok
ers.
Curr
ent
com
post
wor
kers
iden
tified
asat
opic
dem
onst
rate
da
sign
ifica
ntly
enha
nced
OR
for
chro
nic
bron
chiti
s(6
.25;
CI:1
.19–
32.9
0)Co
mpa
red
toco
ntro
ls,f
orm
erco
mpo
stw
orke
rsre
port
edm
ore
eye
irri
tatio
n(p
=0.
03)
Eye
irri
tatio
nw
asas
soci
ated
with
chro
nic
bron
chiti
sin
curr
ent
com
post
wor
kers
(OR
7.22
,CI
:1.1
2–46
.8)
and
form
erw
orke
rs(O
R38
.6,C
I:1.
33->
1000
.0)
Nos
eir
rita
tion
was
asso
ciat
edw
ithco
ugh
incu
rren
tcom
post
wor
kers
(OR
3.51
,CI:
1.07
–11.
6)an
dch
roni
cbr
onch
itisi
nfo
rmer
wor
kers
(OR
25.0
CI:1
.21–
513.
0)Co
-mor
bidi
tyof
chro
nic
bron
chiti
san
dCO
PDw
asm
ore
appa
rent
info
rmer
wor
kers
(13.
7%)
com
pare
dto
curr
ent
wor
kers
(0.6
%)
and
cont
rols
(3.0
%)
(p<
0.00
01)
25su
bjec
tspr
evio
usly
diag
nose
dw
ithal
lerg
icas
thm
aw
ere
excl
uded
from
furt
her
anal
ysis
(fur
ther
anal
yses
cond
ucte
don
178
curr
ent
wor
kers
,51
form
erw
orke
rsan
d33
cont
rols
)A
dmin
istr
ativ
est
affat
the
site
sar
eno
ttru
epo
pula
tion-
base
dco
ntro
ls–
i.e.s
ubje
cts
likel
yto
bem
ore
expo
sed
than
gene
ral
popu
latio
n.A
slig
htex
posu
ream
ong
the
cont
rols
wou
ldre
sult
inan
unde
rest
imat
ion
ofeff
ects
.The
cont
rolg
roup
wer
eal
sosi
gnifi
cant
lyol
der
(p<
0.00
01)
and
had
been
empl
oyed
for
long
er(p
<0.
0001
)In
crea
sed
prev
alen
ceof
chro
nic
bron
chiti
s,an
dse
vere
airfl
owlim
itatio
nsin
form
erw
orke
rsbu
tno
tcu
rren
tw
orke
rsm
aybe
due
tohe
alth
yw
orke
raff
ect.
Subj
ects
wer
eno
tblin
ded
toth
eex
posu
reco
nditi
on.T
hest
atis
tical
pow
erw
asal
solim
ited
byth
esm
alls
ize
ofth
ere
spon
dent
popu
latio
n
Hoff
mey
eret
al.
(201
5)11
9cu
rren
tlyex
pose
dco
mpo
stw
orke
rs,
stra
tified
bysm
okin
gan
dat
opy
(fro
msa
me
coho
rtas
used
inH
offm
eyer
etal
.(2
014)
)
pHan
dle
vels
ofei
cosa
noid
sin
EBC
Frac
tiona
lexh
aled
nitr
icox
ide
(FeN
O)
Bloo
dsa
mpl
esco
llect
edfo
rm
easu
ring
leve
ls(c
once
ntra
tions
)of
alle
rgen
-spe
cific
IgE
antib
odie
s
Befo
rest
ratifi
catio
nA
fter
stra
tifica
tion
onat
opy
and
smok
ing
habi
tsA
fter
stra
tifica
tion
onat
opy
and
smok
ing
habi
ts
Leve
lsof
8-is
o-PG
F 2α
(mar
ker
ofox
idat
ive
stre
ss)
inEB
Cw
ashi
gher
inw
orke
rscl
assi
fied
ashi
ghex
posu
reco
mpa
red
toth
elo
wex
posu
regr
oup
(p=
0.04
7).
pHof
EBC
was
low
erin
smok
ing
com
pare
dto
non-
smok
ing
subj
ects
inbo
thth
elo
wan
dhi
ghex
posu
regr
oups
(p=
0.04
9an
d0.
009
resp
ectiv
ely)
.Sm
okin
gde
mon
stra
ted
asi
gnifi
cant
nega
tive
impa
cton
FeN
Ole
vels
both
inlo
w(p
=0.
0001
)an
dhi
gh(p
<0.
0001
)ex
pose
dw
orke
rs.B
oth
curr
ent
and
cum
ulat
ive
ciga
rett
eex
posu
rew
asne
gativ
ely
corr
elat
edto
FeN
O(p
<0.
001,
each
).Th
ere
was
also
ast
atis
tical
lysi
gnifi
cant
corr
elat
ion
betw
een
FeN
Oan
dbo
thtim
ew
orke
dun
der
clea
nai
rsu
pply
(p=
0.00
71)
and
dura
tion
ofem
ploy
men
tin
atop
icsu
bjec
ts(p
=0.
041)
Stud
ydi
dno
tin
clud
ea
refe
renc
egr
oup
(i.e
.non
-exp
osed
cont
rolg
roup
).Th
est
atis
tical
pow
erw
asal
solim
ited
byth
esm
alls
ize
ofth
ere
spon
dent
popu
latio
nSu
bgro
ups
unde
rst
udy
had
diffe
rent
dist
ribu
tions
for
age
and
dura
tion
ofem
ploy
men
tin
the
com
post
ing
faci
lity
–ne
ither
ofth
ese
wer
ead
just
edfo
rin
the
mai
nan
alys
is
(continuedon
nextpage
)
S. Robertson, et al. International Journal of Hygiene and Environmental Health 222 (2019) 364–386
380
Table3
(continued)
Aut
hor
(yea
r)Su
bjec
tin
form
atio
nH
ealth
outc
ome
Conf
ound
ers
Sign
ifica
ntfin
ding
sCo
mm
ents
Odd
sra
tios
(ORs
)/re
lativ
eri
sks
(RR)
and
p-va
lues
and
95%
confi
denc
ein
terv
als
(CI)
whe
rere
port
ed
Raul
fet
al.
(201
5)14
0cu
rren
tlyex
pose
dco
mpo
stw
orke
rs,
49fo
rmer
com
post
wor
kers
and
29w
hite
-co
llar
wor
kers
(fro
msa
me
coho
rtas
used
inH
offm
eyer
etal
.(20
14))
Cellu
lar
and
solu
ble
mar
kers
inin
duce
dsp
utum
Befo
rest
ratifi
catio
nA
fter
stra
tifica
tion
ofth
e3
subj
ect
grou
psby
smok
ing
Afte
rst
ratifi
catio
nby
clin
ical
sym
ptom
san
dsm
okin
gha
bits
Com
pare
dw
ithw
hite
-col
lar
wor
kers
,co
ncen
trat
ions
ofsC
D14
and
8-is
opro
stan
eco
ncen
trat
ions
inin
duce
dsp
utum
sam
ples
wer
elo
wer
incu
rren
t(s
CD14
:p<
0.05
;8-is
opro
tane
:p
<0.
001)
and
form
ersC
D14
:p<
0.00
1;8-
isop
rota
ne:p
<0.
001c
ompo
stw
orke
rsTo
talc
ellc
ount
was
low
erin
form
erco
mpo
stw
orke
rsth
anin
curr
ent
com
post
wor
kers
(p=
0.00
1)an
din
whi
te-c
olla
rw
orke
rs(p
<0.
01).
Perc
enta
geof
neut
roph
ilsw
ashi
gher
incu
rren
twor
kers
com
pare
dw
ithth
ew
hite
-col
lar
wor
kers
(p<
0.01
).Th
ere
was
also
high
corr
elat
ion
betw
een
the
IL-8
conc
entr
atio
nan
dth
enu
mbe
rof
neut
roph
ils(p
<0.
0001
)N
on/e
x-sm
oker
sin
the
grou
pof
form
erw
orke
rssh
owed
low
erbi
omar
ker
conc
entr
atio
ns(M
MP-
9:p
<0.
001;
sCD
14:p
<0.
05)
com
pare
dw
ithth
eno
n/ex
-sm
oker
grou
pof
curr
ent
wor
kers
.Si
gnifi
cant
diffe
renc
esin
prev
alen
ceof
chro
nic
bron
chiti
s(p
=0.
018)
betw
een
form
erco
mpo
stw
orke
rs(2
4.5%
),cu
rren
tw
orke
rs(5
%),
and
whi
te-c
olla
rw
orke
rs(1
0.3%
).A
sign
ifica
ntly
high
er(p
<0.
05)
perc
enta
geof
neut
roph
ilsw
asm
easu
red
inin
duce
dsp
utum
ofsm
okin
gsu
bjec
tssu
fferi
ngfr
omch
roni
cbr
onch
itis.
Ther
ew
ashi
gher
IL-8
conc
entr
atio
nsin
the
smok
ers
inea
chgr
oup
(cur
rent
/for
mer
/whi
te-c
olla
r)an
din
crea
sing
ofIL
-8co
ncen
trat
ion
with
anau
gmen
tatio
nof
resp
irat
ory
sym
ptom
s.M
MP-
9al
sosi
gnifi
cant
lyin
crea
sed
inea
chgr
oup
with
augm
enta
tion
ofre
spir
ator
ysy
mpt
omsb
utw
asno
tin
fluen
ced
bysm
okin
gha
bits
.
Adm
inis
trat
ive
staff
atth
esi
tes
are
nott
rue
popu
latio
n-ba
sed
cont
rols
–i.e
.sub
ject
slik
ely
tobe
mor
eex
pose
dth
ange
nera
lpo
pula
tion.
Asl
ight
expo
sure
amon
gth
eco
ntro
lsw
ould
resu
ltin
anun
dere
stim
atio
nof
effec
ts.
Subj
ects
wer
eno
tblin
ded
toth
eex
posu
reco
nditi
on.T
hest
atis
tical
pow
erw
asal
solim
ited
byth
esm
alls
ize
ofth
ere
spon
dent
popu
latio
n
van
Kam
pen
etal
.(20
16)
74cu
rren
tlyex
pose
dco
mpo
stw
orke
rs,
42fo
rmer
com
post
wor
kers
(who
had
left
duri
ngth
e13
-yea
rfo
llow
-up)
and
37no
n-ex
pose
dco
ntro
ls(f
rom
sam
eco
hort
asus
edin
Hoff
mey
eret
al.(
2014
))
Prev
alen
ceof
self-
repo
rted
sym
ptom
s(q
uest
ionn
aire
data
)Lu
ngfu
nctio
n(v
iasp
irom
etry
)
Befo
read
just
men
tA
fter
adju
stm
ent
for
smok
ing
habi
ts,e
xpos
ure
grou
p,se
veri
tyof
resp
irat
ory
sym
ptom
san
ddu
ratio
nof
empl
oym
ent
Befo
read
just
men
t
Com
pare
dto
1996
/97,
the
num
ber
ofcu
rren
tand
form
erco
mpo
stw
orke
rsre
port
ing
coug
hin
crea
sed
in20
09(p
=0.
013
&p
=0.
003
resp
ectiv
ely)
.Fo
rmer
com
post
wor
kers
show
eda
high
erri
skof
coug
han
dco
ugh
with
phle
gm(p
=0.
024
&p
=0.
012,
resp
ectiv
ely)
duri
ngth
efo
llow
-up
peri
od.W
orki
ngas
aco
mpo
stw
orke
rfo
r>
5ye
ars
sign
ifica
ntly
incr
ease
dth
eri
skof
coug
han
dco
ugh
with
phle
gm(p
<0.
001
for
both
).Si
mila
rly,
smok
ing
incr
ease
dth
eri
skof
coug
han
dco
ugh
with
phle
gm(p
=0.
002
&p
=0.
004,
resp
ectiv
ely)
.Lu
ngfu
nctio
nm
easu
res
dece
ased
sign
ifica
ntly
duri
ngth
etim
eof
follo
w-u
pin
the
3gr
oups
(p<
0.00
1)
Did
nota
djus
tfor
grow
ing
use
ofpr
otec
tive
mea
sure
s(e
.g.r
espi
rato
rym
asks
)du
ring
the
13-y
ear
follo
w-u
ppe
riod
(thi
sis
likel
yto
conf
ound
expo
sure
resp
onse
asso
ciat
ions
)Su
bjec
tsw
ere
notb
linde
dto
the
expo
sure
cond
ition
.The
stat
istic
alpo
wer
was
also
limite
dby
the
smal
lsiz
eof
the
resp
onde
ntpo
pula
tion
(continuedon
nextpage
)
S. Robertson, et al. International Journal of Hygiene and Environmental Health 222 (2019) 364–386
381
4.3, when comparing compost workers, especially windrow compostingworkers, to non-exposed controls (administrative staff from within(Heldal et al., 2015) or outside (Hoffmeyer et al., 2014) the compostingfacilities). However, only one study found differences (Heldal et al.,2015) greater than would be expected by chance (p < 0.05). Heldalet al. (2015) also found increased prevalence of self-reported coughwith increasing exposure of compost workers to endotoxin, bacteria oractinomycetes spores as measured by personal samplers. Of note, themiddle tertile but not the highest tertile, of exposure to endotoxin,bacteria or actinomycetes spores had significantly increased adjusted(for age and smoke) OR's for cough prevalence. However, the analysesdid not include a trend test. In the 13-year follow-up study by vanKampen et al. (2016) the occurrence of symptoms was examined usingmodified Poisson regression. Former – but not current – compostworkers had a significantly increased risk of cough and cough withphlegm (relative risk (RR) and 95% confidence intervals (CI), 2.46;1.13–5.38, p = 0.024; and RR, 2.93; Cl, 1.27–6.76, p = 0.0.012,respectively) compared with non-exposed controls (administrativestaff from outside the composting facilites).
Three papers, including one prospective cohort study (van Kampenet al., 2016) and two cross-sectional studies (Hoffmeyer et al., 2014,2015, showed increased prevalence and incidence of chronic bronchitisin compost workers, with the highest levels among former compostworkers. Findings reached conventional levels of significance in two ofthe studies (Hoffmeyer et al., 2014, 2015).
Two studies reported on COPD (Hoffmeyer et al., 2014; van Kampenet al., 2016). Spirometry was used to classify subjects into COPD and itsGOLD (Global Initiative of Chronic Obstructive Lung Disease) severitystages (stages I-IV). A cross-sectional study by Hoffmeyer et al. (2014)in 190 current compost workers, 59 former workers and 28 controlsubjects reported no statistical significant differences in the prevalenceof COPD between groups. Likewise in the 13-year follow-up study byvan Kampen et al. (2016) there was no statistical differences in theprevalence of COPD among current compost workers, former workersand control subjects.
3.3.1.5. Asthma and asthma symptoms. One cross-sectional studyreported on asthma (Hoffmeyer et al., 2014). A score-based diagnosisof allergic asthma was less common in the current (12/190; 6.3%)compared to former workers (8/59; 13.6%), and to the control subjects(5/38. 13.2%) (Hoffmeyer et al., 2014). However, a quasi-experimentalanalysis (Heldal et al., 2015) of data on 47 Norwegian workersemployed at five windrow (n = 20) and five reactor facilities(n = 27) found increased odds of symptoms of asthma in the compostworkers compared with control subjects. This difference, however, didnot reach statistical significance.
3.3.1.6. Antigen-specific immunoglobulin (IgE) levels. Two cross-sectionalstudies on German compost workers detected no differences in theprevalence of atopic sensitisation in workers formerly and currentlyexposed (Hoffmeyer et al., 2014, 2015. Furthermore, median totalserum IgE concentrations at baseline and 13-year follow-up for currentand former compost workers were similar to the control group (vanKampen et al., 2016). Also, the percentage of participants with elevatedspecific IgG levels against Aspergillus fumigatus, Penicillium spp.,Saccharopolyspora rectivirgula and Thermoactinomyces vulgaris wassimilar at baseline and 13-year follow-up in all groups (van Kampenet al., 2016). Serum IgE and IgG concentrations in compost workerswere unrelated to duration of employment at the compost facility (vanKampen et al., 2016).
3.3.1.7. Eye and nose irritation. One cross-sectional study comparingcompost workers and controls reported increased occurrence of eyeirritation, especially among former workers (p = 0.03) (Hoffmeyeret al., 2014). In the same study, prevalence of nose irritation waslower in current compost workers, whereas it was higher in formerTa
ble3
(continued)
Aut
hor
(yea
r)Su
bjec
tin
form
atio
nH
ealth
outc
ome
Conf
ound
ers
Sign
ifica
ntfin
ding
sCo
mm
ents
Odd
sra
tios
(ORs
)/re
lativ
eri
sks
(RR)
and
p-va
lues
and
95%
confi
denc
ein
terv
als
(CI)
whe
rere
port
ed
Communitystudies
Dou
glas
etal
.(2
016)
34,9
63re
spir
ator
yho
spita
ladm
issi
ons
in46
56ce
nsus
outp
utar
eas
with
in25
0–25
00m
ofa
com
post
site
Emer
genc
yan
dno
n-em
erge
ncy
hosp
ital
adm
issi
ons
for
post
code
area
s(f
rom
Hos
pita
lEpi
sode
Stat
istic
s),w
ithre
spir
ator
y-re
late
dpr
imar
ydi
agno
sis
for
adm
issi
on(a
ccor
ding
toIn
tern
atio
nal
Clas
sific
atio
nof
Dis
ease
(ICD
10)
code
;all
resp
irat
ory
dise
ase,
resp
irat
ory
infe
ctio
ns,
asth
ma
&CO
PD)
Afte
rad
just
men
tfo
rag
ean
dse
xA
fter
adju
stm
ent
for
age,
sex,
soci
o-ec
onom
icde
priv
atio
nan
dto
bacc
osa
les
Smal
linc
reas
edri
skfo
rof
adm
issi
ons
for
all
resp
irat
ory
dise
ase
and
COPD
for
thos
eliv
ing
near
era
com
post
ing
site
sw
hen
asse
ssed
bydi
stan
ceba
nd(p
for
tren
d=
0.01
&0.
04,
resp
ectiv
ely)
Usi
nglo
g-tr
ansf
orm
eddi
stan
cefr
omsi
teth
ere
was
asm
alls
igni
fican
tde
crea
sing
risk
for
resp
irat
ory
adm
issi
ons
with
incr
easi
ngdi
stan
cefr
omsi
te(p
=0.
054)
Stud
ydi
dno
tac
coun
tfor
chan
ges
inse
ason
ality
and
did
not
have
info
rmat
ion
onin
divi
dual
-leve
lsm
okin
gor
co-
mor
bidi
ties.
The
stud
ydi
dno
tals
oco
nsid
erot
her
pote
ntia
lsou
rces
ofbi
oaer
osol
expo
sure
s(e
.g.i
nten
sive
farm
s)H
ospi
tala
dmis
sion
sre
pres
enta
seve
reen
dof
the
spec
trum
ofpo
tent
ialh
ealth
effec
tsof
bioa
eros
olex
posu
res.
Itis
unlik
ely
that
seve
reim
pact
sw
ould
have
been
relia
bly
dem
onst
rate
dif
infr
eque
nt
*W
here
valu
esar
eno
tpr
ovid
edfo
rsp
ecifi
csa
mpl
ing
para
met
ers
(suc
has
flow
rate
,sam
plin
gtim
e,sa
mpl
ing
heig
htet
c.),
they
wer
eno
tre
port
ed.
S. Robertson, et al. International Journal of Hygiene and Environmental Health 222 (2019) 364–386
382
workers (Hoffmeyer et al., 2014). A quasi-experimental analysiscomparing compost workers and controls reported no increasedprevalence's of nose irritation or eye irritation (Heldal et al., 2015).However, there was a positive and statistical significant relationshipbetween measured exposure to Acinomycetes (0.02–0.3 × 106 spores/m3) and reported nose irritation (p < 0.05) and increased swelling inthe outer part of the nose measured using acoustic rhinometry amongcompost workers when measured across shift (Heldal et al., 2015).There were no changes in the narrowest area of the nasal cavity,deemed the most accurate measure of inflammatory response (Heldalet al., 2015).
3.3.1.8. Lung and systemic inflammation. Induced sputum evaluationrevealed lower values of soluble biomarkers (sCD14 and 8-isoprostane)in current and former German compost workers compared to controls(administrative staff from outside the composting facility) (Raulf et al.,2015). Former workers had a significantly lower total cell countcompared to current compost workers (p = 0.001) or to the controlworkers (p < 0.01) (Raulf et al., 2015). The percentage of neutrophilswere significantly higher in the current compost workers, as compared tothe control group (p < 0.01) (Raulf et al., 2015). Furthermore,neutrophil levels correlated positively with IL-8 (r = 0.669, p <0.0001) (Raulf et al., 2015). Subgroup analysis showed that thesechanges in induced sputum were most pronounced in current than ex/non-smokers and in those with chronic bronchitis. (Raulf et al., 2015).This was true for all groups of subjects: current compost workers, formercompost workers and control workers (Raulf et al., 2015).
Heldal and co-workers (Heldal et al., 2016) showed that serum in-tracellular adhesion molecule-1 (ICAM-1) and fibrinogen levels (afteradjustment for age and smoking habits) were significantly higher amongNorwegian compost workers compared with the control group (admin-istrative staff from the composting facilities). Elevated CRP levels werefound to be associated with lower values of FEV1/FVC when data fromboth compost workers and sewage workers were analysed in a mixedmodel (Heldal et al., 2016). Similarly, a statistically significant positiveassociation between both dust and bacteria with ICAM-1 was also ob-served (Heldal et al., 2016). High levels of fractional exhaled nitric oxide(FeNO; considered a surrogate marker of airway inflammation) in com-post workers were reported to correlate with the intensity of exposure,but only in atopic compost workers (Hoffmeyer et al., 2015).
3.3.2. Community health studiesOne cross-sectional community-based study (Douglas et al., 2016)
examined health effects in residents of communities at various distancesto composting facilities (see Table 2 for details).
Analysing 34,963 respiratory hospital admissions in 4656 censusoutput areas (COAs) within 250–2500 m of a large open-air compostingfacility in England, there were no significant trends using pre-defineddistance bands of > 250–750 m, > 750–1500 m and > 1500–2500 m.Using a continuous measure of distance, there was a small non-
statistically significant (p = 0.054) association with total respiratoryadmissions corresponding to a 1.5% (95% Cl: 0.0–2.9%) decrease inrisk if moving from 251 m to 501 m. There were no significant asso-ciations for subgroups of respiratory infections, asthma or COPD. Insummary, this national study does not provide evidence for increasedrisks of respiratory hospital admissions in those living beyond 250 m ofan outdoor composting area perimeter.
3.3.3. Bias assessmentTable 4 presents results of the bias assessment. Explanations for the
scores agreed for each study are presented in Appendix E. A high scoredenotes a low risk of bias and a low score denotes a high risk of bias.The highest possible score is 32, and the lowest possible score is 8.Overall studies included in this systematic review scored 17–26 a scoreof 25–26 for the two occupational studies measuring exposure, 17–20for the four occupational studies that did not assess occupational ex-posures, and a score of 26 for the 1 community study (using an ex-posure proxy).
The majority of studies used statistical tests appropriate for the type ofquestion and study design and in general, an adequate description of themethodology was provided. The occupational epidemiological studies wereprone to selection bias, related to studying only current workers (i.e.healthy worker survival bias). Three of the studies (Hoffmeyer et al., 2014;Raulf et al., 2015; van Kampen et al., 2016) attempted to correct partiallyfor this by including workers formerly and currently exposed. The twostudies from Heldal et al., 2015, 2016 scored higher on study design (quasi-experimental designs as opposed to cross-sectional design) and exposureassessment (as measured). In all six occupational studies, sample size wassmall and none of the studies presented sample size calculations. The onecommunity study (Douglas et al., 2016) had a higher sample size and wasless vulnerable to the effects of selection bias (included all compostingfacilities with an outdoor composting component in England) and responsebias (outcome data were objectively collected and independently codedhospital admissions to NHS hospitals rather than self-reported healthquestionnaires), with control for relevant confounders (age, sex, area-leveldeprivation and tobacco sales). While both community and occupationalstudies adjusted for a number of confounders such as age, sex and smokingstatus, the community study (Douglas et al., 2016) was the only study toinclude socio-economic status as a potential confounder. However, it wascross-sectional in design and did not measure exposure directly.
4. Discussion
This timely review serves as a comprehensive update of what newevidence has emerged on exposures and health outcomes in relation tobioaerosol emissions from composting facilities. Composting facilitiesare a major source of bioaerosols and in 2015 we reported that therewas some, albeit limited, evidence linking bioaerosol emissions fromcomposting facilities to poor respiratory health in nearby residents(Pearson et al., 2015). However, the limited evidence precluded any
Table 4Risk of bias in the health studies (excluding Gutarowska et al. (2018), a lab-based study), using the risk of bias assessment tool presented in Appendix B. Scores areprovided on a scale of 1–4, a maximum possible score of 32 represented the best quality study with minimal bias. Explanations for the scores are provided inAppendix E.
Author (year) Study design Selection Responder Confounders Exposure assessment Outcome assessment Sample size Analysis Total
Occupational health studiesHeldal et al. (2015) 3 3 4 2 4 3 2 4 25Heldal et al. (2016) 3 3 4 3 4 3 2 4 26Hoffmeyer et al. (2014) 2 3 1 3 1 3 3 4 20Hoffmeyer et al. (2015) 2 3 1 2 1 3 2 3 17Raulf et al. (2015) 2 3 1 3 1 3 2 3 18van Kampen et al. (2016) 4 3 2 3 1 3 2 4 22Community health studiesDouglas et al. (2016) 2 4 4 3 2 3 4 4 26
S. Robertson, et al. International Journal of Hygiene and Environmental Health 222 (2019) 364–386
383
quantitative assessment. Since then, the number of operational in-dustrial-scale composting facilities in England has increased by 9% -nearly twice the growth from 2012 to 2014. At the same time, rapidurbanisation has led to expansion of city borders. It is therefore likelythat more and more people are living near large composting facilitiesand being exposed to bioaerosol pollution.
Although this review identified a number of new studies, the con-clusions remain largely unchanged to those of our earlier review(Pearson et al., 2015). Bioaerosol concentrations in recent studies con-ducted in occupational settings remain similar to those reported in theprevious review. Furthermore, many of our research recommendationshave not yet been fully implemented. While some progress has beenmade characterising bioaerosol emissions from composting facilities,relatively little headway has been made regarding the potential publichealth risks associated with these bioaerosol emissions.
Studies included in the previous review (Pearson et al., 2015) mostlyrelied on traditional methods, such as culture and/or morphologicalidentification by microscopy, for analysing the microbial characteristicsof bioaerosols (Appendix F). Advances in molecular technologies haveenabled a more comprehensive characterisation of the bacterial andfungal components, providing greater microbial resolution and diversity.Since only a small percentage of bacteria (around 2%) and fungi (around5–17%) can be readily grown in the laboratory, culture-based methodsgreatly underestimate diversity (Stefani et al., 2015; Wade, 2002). Mi-croscopy is less prone to bias; however, classification remains challen-ging as many microorganisms share similar morphological character-istics. Methods analysing the microbial DNA (metagenome) directlyextracted from samples without any prior culture are culture-in-dependent, thereby enabling the identification of all microbes (un-culturable, culturable, viable and non-viable). This further maximisesclinical relevance, as microorganisms do not need to be viable nor cul-turable to elicit a response. Although over half (55%) of the exposurestudies analysing the metagenome were culture-independent, these re-present only 30% of the total exposure studies. Thus, the microbialcharacterisation of bioaerosols currently remains culture-dependent.
Metagenome analyses were based on the NGS and/or PCR of am-plified regions (amplicons) containing sections unique to a specificmicrobial genera or species, providing improved microbial resolutionand diversity data. Such molecular methods are not without their owncaveats. Results of amplicon-based analyses are often presented as re-lative abundance of microorganisms within a sample, suggesting thatthe number of amplicons (or sequences) designated to a particularmicroorganism relates to its abundance. This is not necessarily true –different species (and even strains) of bacteria and fungi can containdifferent numbers of the same genes, so called copy number variation.Thus, a specific microorganism may appear to have greater abundance,simply because it has a greater number of copies of the analysed DNAregion. Likewise, some microbial spores contain greater/lesser amountsof DNA and/or be easy/more difficult to break open, thus leading toresults that could be incorrectly interpreted as actual abundance. Whilethis is a problem when attempting to quantitatively compare theabundance of different microorganisms within a particular sample, it isnot necessarily an issue when monitoring temporal or spatial changes inthe same microorganism. Fortunately, the latter is probably of moreimmediate interest with respect to composting facilities; particularlysince the exposure studies to-date largely rely on short duration“snapshot” sampling. Subsequent targeted validation of microorgan-isms of interest, for example by qPCR, may be useful in future studies.Furthermore, sequencing generates vast amounts of data, but requiresrobust bioinformatics for accurate microorganism identification.Identification is only as good as the reference database used. Sequencesthat cannot be assigned to a reference, because the database lacks se-quences from particular genera or species, will remain unclassified orworse still, be misclassified. As the use of microbial metagenomicscontinues to increase, the molecular analysis methods, associated da-tabases and thus microbial identification will also improve. Indeed, it is
worth noting that the results of a two four-year Natural EnvironmentResearch Council (NERC; the UK's leading public funder of environ-mental science) funded program, which has involved developing,testing and comparing traditional and molecular methods, are due to bepublished soon. This will help to inform on the use of such methods anddrive improved and standardised bioaerosol characterisation protocols.
To evaluate the exposure and the dispersal of bioaerosols beyond thecomposting site, it is necessary to know their background concentrationsin air from unaffected areas. One of the shortcomings of the earlier studieswas the lack of background measurements. This problem remains. Onlyeight of the 18 bioaerosol exposure studies (44%) measured bioaerosolconcentrations at a background location, although this is an improvementcompared to our previous review (32%) (Pearson et al., 2015). As withother pollutants, untangling the contribution of an individual source (inthis case a composting site) from background bioaerosol concentrations isa challenge. For example, the composting site might be located in an areawhere there are many sources of bioaerosols. It is therefore very difficultto assess the potential risk to health arising from bioaerosols emitted fromcomposting sites on nearby communities.
This review underscores once again that far too little is known aboutwhether exposure to bioaerosol emissions from composting facilities cancontribute to poor health outcomes. Bioaerosol exposures and healthoutcomes among communities living within the vicinity of the compostingsite has not been sufficiently investigated. The few epidemiological studiesthat were identified were almost exclusively carried out in compostworkers and were characterised by significant methodological limitations(for example, small sample size and short time frames). Furthermore, theresults of such studies have been mixed, with some reporting adverse ef-fects, and others reporting no effect or even a protective effect. It is im-possible to determine whether a potential effect is a true causal effect ofexposure or a reflection of the selection bias in occupational epidemiolo-gical studies (also known as the healthy worker effect). In almost all cases,effect-sizes were small, and there was no discernible pattern of whethereffects may subside over time in the studies comparing current and formercompost workers. Studies focussed mainly on respiratory health with evenless information available on other outcomes such as cardiovascular andgastrointestinal outcomes. While health data on occupationally exposedworkers can provide some insight into the allergenicity, toxicity, infectiousand inflammatory processes, or lack thereof, resulting from bioaerosolexposure in the general population, caution should be exercised in makingany inferences. There tends to be a bias towards the presumption of healthrisks from bioaerosols. However, the converse – beneficial health effects –may also occur. The hygiene hypothesis (Stiemsma et al., 2015; Strachan,1989), a somewhat misleading term (Bloomfield et al., 2016), proposesthat exposure to microbial agents during early life may lead to lower levelof allergy and asthma.
The available evidence reveals some progress has been made re-garding health outcome assessment. Rather than relying solely on self-reported measures of health status, most studies included clinical out-come measurements, such as spirometry. However, given the (1) lim-ited number of studies; (2) small associations observed; (3) methodo-logical issues; and (4) potential for selection bias, a conclusiveinterpretation of these studies remains challenging. There was onecommunity study and this study relied on distance as a proxy forbioaerosol exposure (Douglas et al., 2016). One key advantage of thisstudy is that it used objective data, analysing respiratory-related hos-pital admission rates for small geographical areas in England from 2008to 2010. However, this was an ecological study, may not reflect in-dividual-level effects, is likely to have been hampered by exposuremisclassification (due to the use of distance as an exposure proxy), anddid not account for bioaerosol levels or meteorological effects. Thestudy also looked at respiratory-related hospital admissions as thehealth outcome, which may represent the more severe effects of po-tential bioaerosol-related health effects. Collection of health data in thecommunity, or use of primary care data (not currently available atnational level in the UK) would be more suitable.
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4.1. Impact
It is hoped that this review will provide support to help guide en-vironmental health decision-makers. This review not only examinespast research, but also identifies research gaps and argues for the needfor further research to better characterise composting-associatedbioaerosol exposures and health. This review is particularly topical inthe UK as bioaerosol emissions and their potential impacts on healthwas identified as an ongoing concern in the latest annual report fromthe Chief Medical Officer (Chief Medical Officer, 2017). The informa-tion provided at the time of this review does not provide evidence tosupport a change from the Environment Agency's current permit gui-dance of at least 250 m (Environment Agency, 2010, 2018a). However,this should be re-reviewed pending acquisition of further data.
4.2. Recommendations for future work
To address the gaps in knowledge highlighted above, studies thatincorporate the following are required:
1. Larger sample sizes
More studies with sufficient power are needed to draw meaningfulconclusions from the data. No studies included details of power calculations,making it difficult to identify which studies were sufficiently powered todetect a meaningful difference. Sample size and power considerationsshould therefore be an essential component of planning future studies.
2. More varied populations
The majority of studies have been conducted in occupational settings,which can be male-dominated and liable to healthy worker bias. There is aneed for detailed studies to be conducted in community settings. Futurestudies should include a more representative sample of individuals of, forexample; men and women, a wide age range (children, adults and theelderly), and different health status (asthmatics, immunocompromisedindividuals). This would also help to identify any susceptible populations.
3. Longer time scales
The majority of studies take a snapshot of a population and measurethe exposure and health outcomes over a very short time period. Longer-term studies are essential to capture the longer-term effects of acute andchronic bioaerosol exposure. This would be important for understandingwhether there are synergetic or interactive effects of temperature andbioaerosol exposure on human health. Since the previous review, therehas been modest improvements in the characterisation of bioaerosolsassociated with the advent of new sampling and analysis technologies.However, due to the lack of long-term sampling the spatial and temporalvariability of bioaerosol composition and concentration remains largelyunknown. Longer-term bioaerosol measurement methods are not wellestablished, but as highlighted in this review, there are developmentswith the use of WIBS technology (although studies included in this re-view only monitored bioaerosols over seven days). Homogeneity in thesampling methods used to quantify and characterise bioaerosols wouldalso be advantageous to allow easier comparison between studies, par-ticularly in studies conducted in different countries.
4. Quantification of background concentrations
To evaluate the exposure and the dispersal of bioaerosols beyond thecomposting site, it is necessary to know their background concentrationsin air from unaffected areas. Less than half of the exposure studiesmeasured a bioaerosol concentration at a background location. Thesemeasurements are needed to help determine which bioaerosol compo-nents and concentrations are released as a direct result of compositing.
5. Clearer health outcome definition
While health studies are starting to use objective health measure-ments, supplemented by questionnaire data, clearer definition of thehealth outcomes under study is required. This is difficult given thenature of bioaerosols, as different components may give rise differenthealth effects, and biochemical measurements alongside objectivehealth measurements should be considered.
6. Consideration of confounders
It is essential in all epidemiology studies studying environmental effectsof health outcomes to account for potential confounding factors. Healthstudies included in this review typically adjusted for age and sex but manyimportant potential confounding factors were overlooked (for example,socioeconomic status, quality of housing and other lifestyle factors).
7. Use of experimental studies to assess mechanisms
To identify the health effects of bioaerosols without confoundingeffects, and to determine the specific bioaerosol components that leadto specific health outcomes, more experimental work in model systemsis required. Mechanistic studies will improve our understanding of thebiological links between exposure and effect, enabling causal associa-tions to be established.
While all of these recommendations would greatly benefit this areaof research, it is unlikely that all will be applied in a single study.Therefore, we suggest, in the first instance, that future studies focus onwell-powered, long-term studies, using standardised methods to mea-sure both bioaerosol exposure and associated health outcomes incommunity settings.
5. Conclusions
Although this review identified an additional 23 studies since July 2014,our conclusions remain largely unchanged (Pearson et al., 2015). Un-fortunately, studies have not yet had the chance to implement many of ourresearch recommendations from Pearson et al. (2015). While some progresshas been made characterising the bioaerosol emissions from compostingfacilities, with the increasing use of molecular methods, relatively littleheadway has been made regarding the potential public health risks asso-ciated with these bioaerosol emissions. Only one community health studywas identified and used an imprecise measure of bioaerosol exposure. Giventhe absence of any consistent evidence on the toxicity of bioaerosols fromcomposting facilities, there is insufficient evidence to provide a quantitativecomment on the risk to nearby residents from exposure to compostingbioaerosols. To improve risk assessment and to best advise on risk man-agement a holistic approach is required to provide a more comprehensiveunderstanding of both bioaerosol characteristics and their associated healtheffects in nearby residents, within the same study.
Conflicts of interest
The authors report no conflicts of interest.
Acknowledgements
Philippa Douglas is an early career research fellow funded by theMRC-PHE Centre for Environment and Health. The research was partfunded by the National Institute for Health Research Health ProtectionResearch Unit (NIHR HPRU) in Health Impact of EnvironmentalHazards at King's College London in partnership with Public HealthEngland (PHE) and Imperial College London. We thank the librarians atthe Public Health England for their help with the literature search. Theviews expressed are those of the author(s) and not necessarily those ofthe NHS, the NIHR, the Department of Health & Social Care or PHE.
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Apendices
Apendices to this article can be found online at https://doi.org/10.1016/j.ijheh.2019.02.006.
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