Bioaerosol exposure from composting facilities and health ... · such as airway inflammation and oxidative stress (Li et al., 2003;Qu et al., 2017; Samake et al., 2017). A robust

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/).

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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).


366

Fig. 2. Flow diagram summarising the study selection and exclusion process.


367

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


368

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the

mai

nco

mpo

stin

gac

tiviti

espe

rfa

cilit

ySa

mpl

er:

•clo

sed-

face

thre

e-pi

ece

cass

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

)


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

)


370

http://www.astm.org/Standards/E884

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

)


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

)


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.


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

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(continuedon

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374

Table2

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spec

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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.).


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


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.


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

)


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

)


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

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(continuedon

nextpage

)


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

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wer

eno

tre

port

ed.


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


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.


385

Apendices

Apendices to this article can be found online at https://doi.org/10.1016/j.ijheh.2019.02.006.

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Bioaerosol exposure from composting facilities and health ... · such as airway inflammation and oxidative stress (Li et al., 2003;Qu et al., 2017; Samake et al., 2017). A robust