Appendix 1: Health Search Strategy – example list of search strings
The search strategy presented below was used in Medline. It should be noted that the search strings
did differ slightly between each database, as the different databases require different inputs and
wildcard operators (please refer to the key). However the search strings presented below is generally
what was used in each search, and adapted thus.
#1. exp "bacterial infections and mycoses"/ or exp parasitic diseases/ or exp digestive system diseases/
or exp respiratory tract diseases/ or exp eye diseases/ or exp "female urogenital diseases and
pregnancy complications"/ or exp cardiovascular diseases/ or exp "congenital, hereditary, and
neonatal diseases and abnormalities"/ or exp endocrine system diseases/ or exp immune system
diseases/ or exp "disorders of environmental origin"/ or exp occupational diseases/
#2. ((health adj (impact or effect or complaint or response or outcome or ill)) or (exposure response or
dose response or disease or symptom or illness or infection or asthma or neutrophilia or immune or
aspergillosis or ABPA or mycosis or legionnaire or allerg$ or alveolitis or inflamm$ or lung or
bronch$ or airway or pneumon$ or respiratory or dysnpoea or rhinitis or hypoxemia or pulmon$ or
ODTS or syndrome or gastr$ or GI or nausea or vomit$ or diarrh?ea or skin or dermat$ or fatigue or
headache or irritat$ or MMI or mucosal or eye)).ti,ab.
#3. (((reproductive or birth or neonat$) adj2 (adverse or outcome$ or weight or congenital or
abdominal or cardiovascular or abnormal or defect or death or anomol$ or prematur$ or genitourinary
or renal or dysplasia or orofacial or cleft)) or (intrauterine adj2 growth adj2 (restrict$ or retard$)) or
iugr or sga or vlbw or lbw or elbw or hypospadia or epispadia or neural tube or gastroschisis or
exomphalos or omphalocele).ti,ab.
#4. 1 or 2 or 3
#5. (bio?solid or ((waste adj2 (organic or solid or domestic or municipal or manag$)) not (hazardous
or combustion or incinerat$)) or (recycl$ adj2 (organic or domestic or municipal))).ti,ab.
#6. (microb$ or biological or bacteri$ or micr?org$ or fung$ or spore or mo?ld or clostridium or
aspergillus or a fumigatus or penicillium or antigen or pathogen or endotoxin or peptidoglycan or
$glucan or mycotoxin or actinomycetes or actinobact$ or sacc?aropolyspora rectivirgula or
sacc?aromonospora viridis or thermoactinomyces sacc?ari or thermoactinomyces vulgaris or
sacc?aride or metabolite or MVOC or dust or particle or PM? or particulate).ti,ab.
#7. (endotoxin or mycotoxin or lipopolysaccharides or beta-glucans or peptidoglycan or
microorganism).ti,ab.
#8. (bio?aerosol or aerosol$ or airborne or emission or emit$ or dispers$ or expos$).ti,ab.
#9. exp Bacteria/ or exp Yeasts/ or exp Fungi/ or exp Endotoxins/ or Mycotoxins/ or
lipopolysaccharides/ or polysaccharides/ or beta-glucans/ or peptidoglycan/
#10. (compost$ or bio?waste).ti,ab.
#11. 6 or 7 or 8 or 9
#12. 5 and 11
#13. 10 or 12
#14. 4 and 13
Key:
# replaces one character, for example ioni#ation
? replaces zero or one character, for example col?r, mo?ld ($ was the equivalent wildcard in some
databases)
$ retrieves any number of characters after stem (or no characters) (* or ? was the equivalent wildcard
in some databases)
“ ” to search for exact phrases
‘exp’ includes sub-headings in the search
‘adj2’ is an adjacency operator (NEAR was the equivalent wildcard in some databases
Appendix 2: Exposure Search Strategy – example search strings
The search strategy presented below was used in Medline. It should be noted that the search strings
did differ slightly between each database, as the different databases require different inputs and
wildcard operators (please refer to the key). However the search strings presented below is generally
what was used in each search, and adapted thus.
((bio?aerosol and (compost: or bio?waste)) or ((microb: or biological or bacteri: or micr?org: or fung:
or spore or mo?ld or clostridium or aspergillus or a#fumigatus or penicillium or antigen or pathogen
or endotoxin or peptidoglycan or :glucan or mycotoxin or actinomycetes or actinobact: or
sacc?aropolyspora#rectivirgula or sacc?aromonospora#viridis or thermoactinomyces#sacc?ari or
thermoactinomyces#vulgaris or sacc?aride or metabolite or "MVOC" or dust or particle or PM# or
particulate or (Bacteria or Yeasts or Fungi or endotoxin or Endotoxins or mycotoxin or Mycotoxins or
lipopolysaccharides or lipopolysaccharides or polysaccharides or beta-glucans or beta-glucans or
peptidoglycan or peptidoglycan or microorganism)) and (compost: or bio?waste or bio?solid or
((waste adj2 (organic or solid or domestic or municipal or manag:)) not (hazardous or combustion or
incinerat:)) or (recycl: adj2 (organic or domestic or municipal))) and (aerosol: or airborne or emission
or emit: or dispers: or expos:))).ti,ab.
Key:
# replaces one character, for example ioni#ation
? replaces zero or one character, for example col?r, mo?ld ($ was the equivalent wildcard in some
databases)
‘adj2’ is an adjacency operator (NEAR was the equivalent wildcard in some databases
Appendix 3: Risk of Bias Assessment Tool
Risk of bias assessment tool developed for the cross-sectional and cohort studies in the review. Developed from Shah and Balkhair (2011). The responder
criteria relates to response rate and whether this was adequately described in the article
Risk of bias
Very low (score of 4)
Low (score of 3)
Moderate (score of 2)
High (score of 1)
Study design
Prospective cohort
Retrospective cohort
Case-control
Case-series
Case-control
Cross-sectional
Case-studies
Ecological
Selection
Clear selection criteria Appropriate to
Selection criteria not fully explained
Unclear if selection criteria appropriate to
Selection criteria not explained
study aim and design
Appropriate to study aim and design, or
study aim Unclear if sample is representative
Sample potentially not representative of population
All available participants selected
of population under study
under study
Minimal details of selection criteria reported
Responder
>90% response and follow-up
>70% response and follow-up
>50% response and follow-up
Response or follow-up rate not reported
Reasons for loss to follow-up explained
Reasons for loss to follow-up explained and
Reasons for loss to follow-up explained and
OR
and investigated
investigated
investigated
50% or lower response or follow-up
OR
Reasons for loss to follow-up not fully investigated
or explained
Confounders
Confounders identified and important
Confounders identified and most important
Confounders identified but some important
confounders controlled
confounders adjusted for
confounders not adjusted for
Most important confounders not adjusted for
Risk of bias
Very low (score of 4)
Low (score of 3)
Moderate (score of 2)
High (score of 1)
Exposure
Direct personal sampling of subjects and
Direct ambient monitoring of studied
On-site ambient sampling over inadequate time
No exposure measures, or poor or non-standard
assessment
controls for studied bioaerosols over
bioaerosols over adequate time period on-site
period or
sampling methods
adequate time period
Standard methodology or non-standard
at limited number of representative sites
Exposures predicted from concentrations sampled at
Standard or recognised methodology or
methods explained
OR
other sites or times
non-standard methods explained
OR
Distance from source used as proxy, with
OR
Exposure modelling using sample,
appropriate exposure bands but no modelling
distance from source used as proxy with unsuitable
meteorological and source term input data to
exposure bands
create exposure bands
Outcome
Direct questioning with standardised
Direct questioning with standardised questions
Use of records of non-standardised clinical
Assessment from open-ended or leading questions
assessment
questions and blinding of interviewer
but without interviewer blinding to exposures
examinations
Non-standardised clinical examination
Standardised clinical examination with
Standardised clinical examination without
Direct questioning but questions not described
blinding of clinician to exposures
blinding of clinician to exposures
or not standardized
Use of records of standardised routine
examinations
Sample size
Analysis
Sample size calculations
No sample size calculation performed but all
No sample size calculations
Adequate sample size (>1000)
available participants studied (201-1000)
Small sample size, reasons not clear (50-200)
Appropriate statistics for study design
Adequate statistical methods but better
Appropriate analytical method but flaws in
Inappropriate analysis for the study design and type
Appropriate analysis for the type of
methods available
implementation
of sample
sample and sampling strategy
OR
Inadequate analysis performed
Very small sample size (<50)
Appendix 4: Summary Characteristics of Exposure and Health Studies
Location
UK
Europe
USA/Canada
Other
Year (range)
Exposure only studies (n=48)
Occupational Community Occupational
only (n=38)
only (n=4)
and
community
(n=6)
Health only studies (n=8)
Occupational only Community
(n=6) (3 cross- only (n=2) (1
sectional, 2 case cross-sectional,
reports,
1 1 case report)
experimental)
9
21
6
2
1983-2014
1
5
0
0
1984-2012
2
1
1
0
1998-2013
2
2
2
0
1995-2009
0
1
1
0
1989-2011
Exposure and Health studies (n=10)
Occupational only Community only
(n=6) (2 cross (n=4) (2 crosssectional, 1 cohort, sectional, 1 lab
1 lab based, 1 quasi based, 1 panel
experimental,
1 study )
quasi-experimental
and cross-sectional)
0
1
5
2
0
1
1
0
1980-2014
2001-2011
Bioaerosols, composting and health: Systematic review
Appendix 5: Occupational Exposure Articles – Study Characteristics
Author
Country
(year)
Number / Type of
Position and activity
Exposure assessment methods (manufacturer and flow
Bioaerosols measured
rate)
Sites
Albrecht
Germany; 1 site open
Compost area during turning
(2007)
Bünger
Total microorganisms
Impinger: AGI-30 - 12.7 l/min
Germany; 6 sites
(2007)
Byeon,
Filter: MD8 Sartorious - 100 l/min
Machinery platform, driver cabins with/without filtered
Personal air sampling
Actinomycetes, total fungi
Impaction: six-stage impactor (TE-10-800, Tisch Environmental)
Total microorganisms
air, manual sorting cabins with/without ventilation
Korea; 1 site enclosed
Plant screening area
(2008)
- 28.3 l/min
Clark
Sweden; 4 sites
(1983)
mixed domestic waste /
Screening area, control room, compost area
Impaction six-stage impactor (Andersen) for 30s to 4m at 1.5m
Dust, endotoxin
above ground
sludge; mostly open
Chang
Not specified, 1 site
(2014)
Composting hall, maintenance area, restaurant, indoor,
Impactor: single stage ambient viable microbe sampler (Tisch
Endotoxin, Aspergillus fumigatus,
outdoor
Environmental) operating at 28.3 l/min and 1.5m above ground
bacteria, mould
and a five-stage cascade sioutas impactor (SKC Inc.) operated at a
flow rate of 9 l/min at 1.5m above ground
Filter: SKC sampler with polycarbonate filter with a flow rate of 4
l/min
Coccia
Italy; 1 site
Sorting, compost area, office, background
(2010)
Impaction: dual head active impactor (DUO SAS 360, PB
Total bacteria (22 and 37oC),
International) - 180 L/min; 1.5m above ground
actinomycetes, total fungi, Endotoxin
Impinger: BioSampler 12.5 L/min; 1.5m above ground
Crook
UK; 4 sites (2 open, 2
(2008)
IVC)
Cyprowski
Poland; 3 sites
Compost workers
Personal air sampler: IOM personal inhalable sampler, 2 l/min;
Dust, Aspergillus fumigatus ,
Partisol: static samplers for PM10 measurement; 16.7 l/min;
actinomycetes, total fungi, endotoxin,
Impaction: Andersen samplers; 28 l/min
(2011)
Compost mixer, compost piles, compost sieve (active)
Filter: 25-mm-glass-fibre filters; button aerosol sampler (SKC)
Dust, total fungi, beta(1→3) glucans
with pump flow rate 4 l/min. 1.5m height.
7
Bioaerosols, composting and health: Systematic review
Author
Country
(year)
Number / Type of
Position and activity
Exposure assessment methods (manufacturer and flow
Bioaerosols measured
rate)
Sites
Deacon
UK; 1 site
50m downwind
Filter: SKC pump; IOM head; 2.0 ± 0.1 l/min; height 1.7 m
Aspergillus fumigatus , endotoxin
UK, 1 site
Upwind, within the operational area, site boundary and
Filter: SKC pump; IOM head; 2.0 ± 0.1 l/min; height 1.7 m
Endotoxin
Personal air sampler: PAS6 2 l/min;
Dust, total bacteria, gram-negative
Filter: Andersen sampler 28.3 l/min
bacteria, total fungi, endotoxin
Dust, endotoxin, beta(1→3) glucans
(2009a)
Deacon
(2009b)
downwind (50, 80, 100, 150, 180 and 280 m).
Douwes
Netherlands
(1997)
1 site; type unknown
Site workers
Douwes
Netherlands
Production workers, technical personnel, supervisors,
Personal air sampler: PAS6 2 l/min;
(2000)
1 site; type unknown
bulldozer operator, process hall, workshop, offices and
Filter: Andersen sampler 28.3 l/min for 1 minute;
Drew
UK; 3 sites:
(2007)
A: Open; Bandand C: In-
canteen
Background, A B and C (Summer, Autumn, Winter)
Personal air filter; IOM head; 2 ± 0.2 l/min
Aspergillus fumigatus, actinomycetes,
All indoor areas
Filter: 3-piece closed-face cassettes (Millipore) connected to
Total microorganisms, total bacteria,
Background: 40m Upwind
portable constant flow pumps (Gilian) at 2l/min - height 1.7 m
total fungi, endotoxin
US; 3 sites (2 open, 1 IVC)
On-site, various locations
Filter: membrane filters; 2 l/min
Total bacteria, total fungi
USA
Personal, feedstock mixing (summer and winter), pile
Personal air sampler: Marple multiple cascade impactor
Dust, Aspergillus fumigatus, endotoxin
screening (summer and winter), pile activity (summer
Impactor: Andersen 2-stage impactor for Aspergillus fumigatus -
and winter)
28 l/min;
vessel
Duquenne
France; 1 site indoor
(2012)
Durand
(2002)
Epstein
(2001)
Dust sampling using National Institute of Occupational Safety and
Health 0500 method, collected through nylon cyclone
Fischer
Germany ; 1 site
Loading Area, compost hall, storage area
Filter: MD 8 air sampler (Sartorius) 1.5m above ground
Aspergillus fumigatus
Germany; 1 site
Loading area, compost hall
Filter: MD 8 air sampler (Sartorius) 1.5m above ground
Aspergillus fumigatus, total fungi
(1998)
Fischer
(2000)
8
Bioaerosols, composting and health: Systematic review
Author
Country
(year)
Number / Type of
Position and activity
Exposure assessment methods (manufacturer and flow
Bioaerosols measured
rate)
Sites
Fischer
Germany; 9 sites
(2007)
Folmsbee
On-site, turning, shredding, in 'drainage flow'
Filter: MD8 (Sartorious); 100 L/min
Total bacteria, actinomycetes, total
conditions
Impinger: glass liquid-30 (AGI-30); 12.7 L/min
fungi
USA
On-site: median of 3 sites 10 yards from windrow
Impactor: six-stage sampler (Andersen) 28.3 l/m;
Total bacteria, gram negative bacteria,
Italy; 3 sites mixed
Indoor windrow, sieving and grinding, final sieving,
Impactor: Surface Air System-Super 180; 180 l/min - 1.6m above
biofilter, compost discharge, downwind, upwind, cabin,
ground;
(1999)
Fracchia
actinomycetes, total fungi
(2006)
Total bacteria, actinomycetes
bag tearing, external windrows turning
Haas
Austria
On-site - open windrow and closed
Impactor: six-stage (Andersen) impactor. 28.3 l/min
Actinomycetes
Netherlands
Indoors on-site
Impactor: two-stage (Andersen). 28.3l/min. 1.5m above ground.
Total bacteria, gram negative bacteria,
(1999)
Heida
(1995)
Heldal
total fungi
Norway
On-site
(2003)
Hryhoczuk
USA
On-site 18 samples 1m and 10m from compost
Filter: Two PAS-6 cassettes collected on polycarbonate and
Organic dust; endotoxin; beta
glass fiber filters
(1→3) glucans
Collector: one-stage (Andersen). 0.5m above ground.
Total bacteria, gram negative bacteria,
(2001)
actinomycetes, total fungi, endotoxin,
beta(1→3) glucans
Krajewski
Poland; 3 sites
(2002)
Composting site worker, machine operator, reloading
Personal air sampler: personal filters of workers
facility machine operator, reloading facility site worker,
Total microorganisms, dust, total
bacteria, total fungi, endotoxin
sorter, waste collection (loader), background (city
streets)
Lundholm
Sweden
70 on-site samples
Impactor: six stage sampler (Andersen)
Gram-negative bacteria
Canada; 1 site IVC
10 different sites
Impactor: six-stage sampler (Andersen) for bacteria and N-6
Total bacteria, gram negative bacteria,
sampler for fungi. 1.5m above ground; 28 L / min flow rate
total fungi
Spain; 1 site indoor
Sorting cabins, reception, anaerobic digestion,
Impactor: AES Sampl’AirMK2 doubleheader; bacteria 80 l/min,
Total bacteria, gram negative bacteria,
composting tunnels, outdoors (downwind and upwind)
fungi 100 l/min
Aspergillus fumigatus, total fungi
(1980)
Marchand
(1995)
Nadal
(2009)
9
Bioaerosols, composting and health: Systematic review
Author
Country
(year)
Number / Type of
Position and activity
Exposure assessment methods (manufacturer and flow
Bioaerosols measured
rate)
Sites
Nikaeen
Iran; 1 site open
(2009)
Composting piles, storage piles, screening, background,
Impactor: biosampler (Andersen N6 single stage viable cascade
Total bacteria, Aspergillus fumigatus,
50m, 100m, 200m and 250m downwind, 100m upwind
impactor)
total fungi
Persoons
France; 1 site partly
2 areas: green compost only and IVC domestic waste.
Impactor: single stage viable particle impactor (Andersen);28.3
Total bacteria, gram negative bacteria,
(2010)
enclosed
Site boundary, summer, winter, shredding,
l/min.
Aspergillus fumigatus, thermal
fermentation, maturation/storage, washing towers,
actinomycetes, total fungi
quiescent piles, turning piles.
Reinthaler
Austria; 3 sites (1 open, 2
Open Windrow (No major activity), Closed system
Impactor: six-stage viable impactor (Andersen) 28.3 l/min. 1.6m
(1997)
closed)
(postrot area/indoor), Enclosed system (dropoff area,
above ground level.
Total bacteria, total fungi
composting area - fresh material, composting area - 68wk old material, sieving area, sorting area)
Reinthaler
Austria; 2 sites - 1 large
2 locations: Large scale (biofilter, exit postrot area),
Impactor: six-stage viable impactor (Andersen) 28.3 l/min. 1.6m
Total bacteria, thermophilic bacteria,
(1999)
scale and 1 agricultural
agricultural (near windrows, near road). Control site
above ground level.
Aspergillus fumigatus, moulds
(meadow)
Reinthaler
Austria; 1 site open (year
Inside plants, between rots, 150m downwind,
Impactor: six-stage viable impactor (Andersen) 28.3 l/min. 1.8m
Mesophilic bacteria, thermophilic
(2004)
2000 and after safety
background levels
above ground level.
bacteria, Aspergillus fumigatus,
measures in 2002)
thermophilic actinomycetes,
mesophilic moulds
Sanchez-
Closed sites (2 x static pile with forced aeriation, 3 x
Impactor: six-stage viable impactor (Andersen) 28.3 l/min. 1.8m
Mesophilic bacteria, Aspergillus
Monedero
UK; 7 sites
forced aeriation and turning)
above ground level.
fumigatus
and
Open windrows (no activity, shredding, turning,
Stentiford
screening)
Background (40m and >200m downwind): turn, shred,
Impactor: six-stage viable impactor (Andersen) 28.3 l/min. 1.8m
Mesophilic bacteria, Aspergillus
Monedero
screen, no activity
above ground level.
fumigatus
(2005)
Downwind: turn, shred, screen, no activity
(2003)
Sanchez-
UK; 1 site
10
Bioaerosols, composting and health: Systematic review
Author
Country
(year)
Number / Type of
Position and activity
Exposure assessment methods (manufacturer and flow
Bioaerosols measured
rate)
Sites
Schlosser
France: 3 sites, UK; 2 sites,
Mixing, screening, maturation, shredding, background,
(2009)
Spain 1 site (2 green waste
summer, winter
Personal sampling: aerosol sampler (CIP 10 M). 10l/in.
negative bacteria, Aspergillus
sites - not clear which
fumigatus, actinomycetes, mesophilic
country.)
Sigsgaard
Denmark
(1994)
Dust, mesophilic bacteria, gram
moulds, endotoxins
Green waste composting plant and domestic
Personal air sampler: two-piece filter holders
Total microorganisms, dust, gram
waste/compost plant
Impinger: flow rate of 0.9 l/min
negative bacteria, total fungi,
endotoxin
Stagg
UK - 6 sites
(2010)
Site A - open air windrows: turning, no activity
Impactor: six-stage viable impactor (Andersen) 28.3 l/min.
Total microorganisms, dust, total
Site B - invessel system:Shredding (10m, 50m and
Partisol samplers - static 16.7l/min
bacteria, bacteria at 25 and 37oC,
150m downwind), inside and outside cab
Personal samplers IOM 2l/min near breathing zone of workers
Aspergillus fumigatus, actinomycetes,
Site C - invessel system:Inside and outside cab, 10m
total fungi, endotoxin
and 50m downwind, vehicle cabs loading compost,
turning
Site D - open-air:On-site, turning, inside and outside
cab
Site E - open-air windrowsInside and outside cab, onsite, 50m downwind
Site F - open-air windrows: No activity (10m
downwind), inside and outside cab
Sykes
UK; 4 sites
(2011)
In-vessel, open-windrow and in-vessel, open windrow
Personal and static sampling: Casella Apex Pro constant flow
and enclosed bays
pumps with IOM inhalable sampling heads, 2.0 l /min with
Manual sorting, shredding, turning, screening
Whatman GF/A glass fibre filters.
Dust, endotoxin, beta(1→3) glucans
Indoor, outdoor
Syzdek
USA; 1 site open
In facility
UK; 1 site
Composting plant
(1995)
Taha
(2006)
Seven day recording volumetric spore traps (Burkard), 1.5m above
Aspergillus fumigatus
ground.
Passive and active processing: portable air tunnel. Height of 1.8m
Aspergillus fumigatus, actinomycetes
above ground. Downwind (5-10m) of compost windrows.
11
Bioaerosols, composting and health: Systematic review
Author
Country
(year)
Number / Type of
Position and activity
Exposure assessment methods (manufacturer and flow
Bioaerosols measured
rate)
Sites
Taha
UK; 1 site
Windrow turning (x4), shredding (x2), screening (x2)
(2007)
Portable wind tunnel: direct sampling of bioaerosols from static
Aspergillus fumigatus, actinomycetes
compost windrows 21l/min. 1.8m above ground.
Personal sampling: aerosol filter sampler (SKC universal dust and
vapour sampling pump) 2+/- 0.11 l/min
Tolvanen
Finland; 1 site open
Crushing, turning, sieving, emptying of drum
Impactor: six stage impactor (Andersen) - 28.3 l/min.
(1997)
Dust, mesophilic bacteria,
actinomycetes, thermophilic bacteria,
endotoxin
Tolvanen
Finland; 1 site
(2005)
Drum composting plant: receiving hall, composting
Impactor: six stage impactor (Andersen) - 28.3 l/min.
hall, control room
Dust, microbes, mesophilic bacteria,
mesophilic actinomycetes, mesophilic
fungi, endotoxin
Van
Netherlands, 1 compost-
Tongeren
screening plant
Near each composting screen, upwind
Impactor: Andersen sampler with N6 modification – 28.3 l/min
Fungi, bacteria, gram-negative bacteria
for 1-15 minutes at a height of 1.5m
(1997)
vanderWerf
Canada; 1 site
(1996)
Debagging, turning (active windrows), processing
Impactor: six-stage Andersen sampler.
(curing), shipping finished compost
Dust, airbourne bacteria and fungi,
gram negative bacteria, Aspergillus
fumigatus, thermophilic fungi,
endotoxin
Van
Germany, 31 sites
Kampen
Sorting cabins, wheel loader cabins, delivery place/hall,
Filter: 3 Gesamtstaubprobenahme (GSP) samplers in parallel at
Total cell count, inhalable dust,
piles, shredding, processing, reference
breathing height. Polycarbonate, polytetrafluoroethylene and glass
beta(1->3) glucans, endotoxin,
fibre filters at a flow rate of 3.5 or 10 l/min depending on the tests
mesophilic moulds, Aspergillus
being completed
fumigatus, mesophilic actinomycetes,
(2014)
thermophilic actinomycetes
Vilavert
(2012)
Spain; 1 site indoor
Winter, summer, N, SE, SW, W, 300m, 600m, 900m
Impactor: Sampl'Air Lite with air flow rate of 100L/min.
Total bacteria, gram negative bacteria,
Aspergillus fumigatus, total fungi (25
and 37oC)
12
Bioaerosols, composting and health: Systematic review
Author
Country
(year)
Number / Type of
Position and activity
Exposure assessment methods (manufacturer and flow
Bioaerosols measured
rate)
Sites
Weber
UK; 1 site outdoor
On site, during compost handling
(1993)
All glass Impinger (AGI) as 12.5 1pm; Five stage cascade
Mesophilic bacteria, thermophilic
impactor
bacteria, fung, organic dust;
endotoxin
Wheeler
(2001)
UK; 2 sites
Screening, turning, shredding
Impactor: six-stage Andersen sampler- 28 l/min
Dust, total bacteria, gram negative
Personal sampling: Personal aerosol monitors - inhalable dust
bacteria, actinomycetes, total fungi
Cyclone sampler (AEA) 1.2 and 1.5 m
13
Bioaerosols, composting and health: Systematic review
Appendix 6: Community Exposure Articles – Study Characteristics
Author
Country
(year)
Number / Type of
Position and activity
Exposure assessment details
Bioaerosols measured
USA; 1 site
Study and reference area
Burkard-Hirst 7-day volumetric spore trap 1.5m above ground;
Aspergillus fumigatus
Germany
Upwind 500m, 200m, 300m, 550m
Sampling: Sartorius MD-8 sampler
Total bacteria, actinomycetes, fungal
Germany
Upwind 500m, downwind 200, 250, 300,
Not stated
Sites
Browne
(2001)
Herr
(2003)
Herr
spores
(2003a)
320,550
Total bacteria, moulds, thermophilic
actinomycetes, thermotolerant
actinomyetes
Kock
Austria, 7 sites
(1998)
Not stated although 350 individual counts were
Andersen-Volumetric sampler at a flow rate of 28.3 l/min and
conducted over 26 days.
the Reuter-Centrifugal-Sampler (RCS) and RCSplus both at a
Bacteria, yeasts and molds
flow rate of 40l/min. All samples were taken over a period of 4
minutes, 1.6m above the ground
Liu
UK; 2 sites open
(2011)
Upwind up to 400m, on-site (no activity, activity
Bioaerosols were captured on 0.8-mm pore size polycarbonate
and site boundary), downwind up to 600m
filters by the SKC sampling pump. Sampling heads were
Endotoxin
elevated to 1.7 m, and samples were collected using a flow rate
at 2.2 0.1 L/min for 30 or 120 minutes
Pankhurst
(2011a)
UK; 2 sites open
Site A: Upwind 100m, On-site (no activity and
Filter: 0.8 m pore size polycarbonate filter for 30 minutes at
Bacteria, Aspergillus Fumigatus,
activity), site boundary, 50m, 80m, 100m, 150m,
2.2 L/min, at 1.7 m height; >800 samples for actinomycetes
actinomycetes, endotoxin
180m, 250m, 280m, 300m
and Aspergillus fumigatus; >700 samples for Gram negative
Site B: Upwind 100m, on-site (no activity and
bacteria; >250 samples for endotoxin; Limulus Amebocyte
activity), site boundary, 50m, 100m, 150m,
Lysate (LAL) extraction for endotoxin;
200m, 300m, 400m, 500m, 600m
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Bioaerosols, composting and health: Systematic review
Author
Country
(year)
Number / Type of
Position and activity
Exposure assessment details
Bioaerosols measured
Sites
Williams
UK, 4 sites (1 in-vessel,
100m upwind, on-site, site-boundary, downwind
Andersen impactor sampler at 28.3 l/min for 2-10 minutes.
Aspergillus fumigatus, total bacteria,
(2013)
3 open windrow))
150m, 250m, and 500-1000m depending on wind
IOM filter samplers at 2 l/min for 30-45 minutes, CEN filter
gram negative bacteria, endotoxin, (1-
direction and site accessibility
sampler at 50 l/min for 20 minutes, Bertin coriolis liquid
3)- β-D- glucan, particulates
impinger sampler at 630 l/min for 10 minutes, and a topaz
particulate matter monitor at 0.6 l/min for 30-45 minutes were
all used at breathing height. Culture methods; malt extract agar
for Aspergillus fumigatus, nutrient agar for total bacteria,
MacConky agar for gram negative bacteria. The qPCR method
for Aspergillus fumigatus spore detection and quantification
was also used. Endotoxin quantification was performed using
a kinetic chromogenic LAL assay and (1-3)- β-D- glucan using
a kinetic chromogenic Glucatell kit.
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Bioaerosols, composting and health: Systematic review
Appendix 7: Occupational exposure studies – total bacteria measurements at
additional sampling locations
Measured total bacteria concentration - log scale
(CFU/m3)
1,000,000
100,000
10,000
1,000
100
10
1
Site boundary
Office
No activity*
Sorting area
Coccia et al., 2010
Sample Location
Durand et al., 2002
Fischer et al., 2007
Heida et al., 1995
Hryhoczuk et al., 2001
Nadal et al., 2009
Nikaeen et al., 2009**
Persoons et al., 2010
Reinthaler et al., 1997
Reinthaler et al., 1999
Stagg et al., 2010
Acceptable level set by
the Environment Agency
Mean/median airborne total bacteria concentrations at selected sampling locations in occupational
exposure studies. If provided in the study, the range of values included is denoted by the error bars.
Please refer to Appendix 5 for study characteristics. Measured concentrations of total bacteria at
additional sampling locations are provided in Figure 3.
*Areas of no activity also include storage and maturation areas
**The study by Nikaeen et al. (2009) presented only maximum values, and no mean/median or minimum values.
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Bioaerosols, composting and health: Systematic review
Appendix 8: Occupational exposure studies – Aspergillus fumigatus measurements
at additional sampling locations
Measured Aspergillus fumigatus concentration - log scale
(CFU/m3)
100,000,000
10,000,000
1,000,000
100,000
10,000
1,000
100
10
1
Site Boundary
No Activity*
Sorting areas
Activity
Clark et al. 1983
Sample Location
Deacon et al. 2009
Fischer et al. 1998
Fischer et al. 2000
Nadal et al. 2009**
Nikaeen et al. 2009
Persoons et al. 2010
Sanchez-Monedero
and Stentiford 2003
van Kampen et al. 2014
Schlosser et al. 2009
Stagg et al. 2010
Acceptable level set by
the Environment Agency
Mean/median airborne Aspergillus fumigatus concentrations at selected sampling locations in
occupational exposure studies. If provided in the study, the range of values included is denoted by the
error bars. Please refer to Appendix 6 for study characteristics. Measured concentrations of
Aspergillus fumigatus at additional sampling locations are provided in Figure 4.
*Areas of no activity also include storage and maturation areas
**The measured concentration at the downwind and background locations in Nadal et al. (2009) were quoted as ‘< 2’.
17
Bioaerosols, composting and health: Systematic review
Appendix 9: Significant and non-significant health effects grouped by type of study (occupational, community) and for
community further grouped by exposure assessment.
Laboratory based studies have been excluded. ‘GI’ refers to gastrointestinal
Ratio of the number of significant to non-significant results
Study
author and
year
Significant results
Non-significant results
Lundholm
1980
Sigsgaard 1994
Not relevant - no analysis undertaken
N/A
All participants - not just
compost workers - decrement
in lung function
Bünger 2000
Tracheobronchitis; Diseases of
the airways (combined);
Diseases of the skin
(combined); total diseases;
Rhinitis allergia; atopic
diseases in the family
Lung
function
Respiratory
Eye/nose/
throat
GI
Skin
Other
Total
N/A
N/A
N/A
N/A
N/A
N/A
0/5
0/6
0/4
0/4
N/A
0/4
0/23
N/A
3/5
0/1
0/4
1 /4
2/4
6/18
Occupational
Lung function: Forced Expiratory Volume (FEV) 1%
predicted; %Forced Vital Capacity (FVC) of predicted;
FEV1/FVC; Peak Flow Rate (PFR)>20% in 24 hrs and
2 weeks
Respiratory: Asthma; chronic bronchitis; chronic dry
cough; dyspnoea with light work; asthma; chronic
bronchitis;
Eye/nose/throat: Itching of eyes at work; itching in
nose more than once a week; rhinorrhea more than
once a week; sore or itching throat more than once a
month
Gastrointestinal Symptoms: Lack of appetite more than
once a month; nausea more than once a month; change
in stool quality in previous 12 month; ever experienced
vomiting or diarrhoea related to work
Other: experienced chest tightness at work; flu-like
symptoms or fever related to work; occasional chest
tightness at work; ever experienced ODTS at work
Mucous membrane irritation; sinusitis; organic dust
toxic syndrome; eczema; dermatomycosis; pyoderma;
otitis externa; nausea; vomiting; diarrhoea; gastrointestinal symptoms (combined); extrinsic asthma
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Bioaerosols, composting and health: Systematic review
Ratio of the number of significant to non-significant results
Study
author and
year
Significant results
Non-significant results
Douwes 2000
Inflammatory markers - not
summarised in table
Symptoms only described, no analysis between
workers and controls
Heldal 2003
Inflammatory markers - not
summarised in table
Müller 2006
Inflammatory markers - not
summarised in table
Bünger 2007
van
2012
Lung
function
Respiratory
Eye/nose/
throat
GI
Skin
Other
Total
Occupational
Kampen
Hambach 2012
N/A
N/A
N/A
N/A
N/A
N/A
N/A
N/A
N/A
N/A
N/A
N/A
N/A
N/A
No change in any lung function parameter
0/2
N/A
N/A
N/A
N/A
N/A
0/2
Watering eyes; itching eyes;
conjunctivitis; chronic
bronchitis; FVC% in nonsmokers
Burning eyes; chest tightness; cough; asthma; allergic
alveolitis; Organic Duct Toxicity Syndrome (ODTS);
pharyngitis; skin lesions; FVC% in smoking workers
1 /2
1/5
3/4
N/A
0/1
0/2
5/14
Watering eyes; foreign body
sensation in eyes; FVC%
predicted
FEV1% predicted; FEV1/FVC % predicted; Cough;
dyspnea; absence of appetite; nausea; vomiting;
diarrhoea; eczema; redness; itching; sweating; fever;
ague; itching eyes; congested nose; runny nose;
dysfunction of olfactory sense; dysgeusia; croakiness
1/3
0/2
2/8
0/3
0/4
0/3
3/23
Respiratory symptoms (work
related and work related or
not); Gastrointestinal
symptoms (work related or
not); skin (work related or not)
Irritation (work related)
Association between exposure to Organic dust and
Irritation (work related or not); dry cough; phlegm;
wheezing; dyspnoea; chest tightness; runny eyes;
blocking of nose; runny nose; sore throat; tickling nose
or sneezing; nausea; pyrosis; lack of appetite
N/A
2/6
1/7
1/1
1 /4
0/1
5/19
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Bioaerosols, composting and health: Systematic review
Ratio of the number of significant to non-significant results
Study
author and
year
Significant results
Non-significant results
Lung
function
Respiratory
Eye/nose/
throat
GI
Skin
Other
Total
Community
Browne 2001
Asthma symptoms (including wheezing and coughing,
and allergy symptoms (including eye, nose and throat
irritations)
N/A
0/2
0/1
N/A
N/A
N/A
0/3
Frequency of colds; hay fever; sinusitis; shortness of
breath at rest; shortness of breath following exertion;
pneumonia; waking up with chest tightness; waking up
due to shortness of breath,; wheezing; itching eyes;
smarting eyes; loss of appetite; nausea/vomiting;
diarrhoea; shivering; fever; joint trouble; muscular
complaints
N/A
N/A
3/7
0/5
N/A
0/3
2/8
Frequency of colds; hay fever; sinusitis;
pneumonia; waking up with chest tightness; waking up
due to shortness of breath; wheezing; cough on
rising/during the day; shortness of breath following
exertion; itching eyes; loss of appetite; nausea or
vomiting; diarrhoea; Fever; joint trouble; muscular
complaints; current intake of medicine
N/A
N/A
3/7
1/5
N/A
0/3
2/8
Hay fever; sinusitis; pneumonia; shortness of breath at
rest; shortness of breath following exertion; waking up
with best tightness; waking up due to shortness of
breath; cough on rising/during the day; loss of appetite;
diarrhoea; excessive tiredness; fever; joint trouble;
muscular complaints; current intake of medicine
N/A
N/A
3/7
3/5
N/A
1/3
1/8
Maxillary sinusitis; respiratory infection; wheezing;
Cough/phlegm; wheezing; pain/pressing
feeling/tightness of the chest; non-allergic rhinitis; nose
irritation/stuffy nose; sore throat; headache; toothache;
dizziness; nausea/vomiting; diarrhoea; asthma; allergic
rhinitis; itching eczema;
N/A
N/A
1/5
2/7
N/A
0/2
5/9
Highest vs Unexposed
Herr 2003
Bronchitis; waking up due to
coughing; coughing on rising
or during the day; excessive
tiredness; current medication
intake
Highest vs near background exposure levels
Herr, 2003
Bronchitis; waking up due to
coughing; shortness of breath
(at rest); smarting eyes (>10x
year) excessive tiredness (>5x
year); shivering
Duration of residency (>5 years)
Herr, 2003
Frequency of colds; bronchitis;
waking up due to coughing;
wheezing; itching eyes;
smarting eyes(>10x year);
nausea or vomiting (>5x year);
shivering
By odour annoyance
Aatamila 2011
Unusual shortness of breath;
eye irritation; hoarseness/dry
throat; toothache; unusual
tiredness; fever/shivering; joint
pain; muscular pain
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Bioaerosols, composting and health: Systematic review
Ratio of the number of significant to non-significant results
Study
author and
year
Significant results
Non-significant results
Lung
function
Respiratory
Eye/nose/
throat
GI
Skin
Other
Total
Community
Odour annoyance in the residential area
Herr, 2003
Itching eyes; smarting eyes;
joint trouble. muscular
complaints
Herr 2003a
TCI [Total Complaint Index]
difference between those living
150m away and controls
Frequency of colds; hay fever; sinusitis; bronchitis;
pneumonia; shortness of breath at rest; shortness of
breath following exertion; waking up with chest
tightness; waking up due to shortness of breath; waking
up due to coughing; wheezing; cough on rising/during
the day; loss of appetite; nausea/vomiting; diarrhoea;
excessive tiredness; shivering; fever; current intake of
medicine
TCI difference between another site 1500m away and
controls
N/A
N/A
0/7
2/5
N/A
0/3
2/8
N/A
N/A
N/A
N/A
N/A
N/A
N/A
Maxillary sinusitis; respiratory infection; unusual
shortness of breath; wheezing; pain/pressing
feeling/tightness of the chest; eye irritation' non-allergic
rhinitis; sore throat; headache; toothache; unusual
tiredness; dizziness; nausea/vomiting; diarrhoea; joint
pain; muscular pain; asthma; allergic rhinitis; itching
eczema
N/A
N/A
1/5
2/7
N/A
0/2
1/9
Maxillary sinusitis; respiratory infection; unusual
shortness of breath; wheezing; Cough/phlegm; nose
irritation/stuffy nose; hoarseness/dry throat;
fever/shivering; pain/pressing feeling/tightness of the
chest; eye irritation' non-allergic rhinitis; sore throat;
headache; toothache; unusual tiredness; dizziness;
nausea/vomiting; diarrhoea; muscular pain; asthma;
allergic rhinitis; itching eczema;
N/A
N/A
0/5
0/7
N/A
0/2
1/9
By distance band: <1.5km
Aatamila 2011
Cough/phlegm; nose
irritation/stuffy nose;
hoarseness/dry throat;
fever/shivering
By distance band: 1.5-3.0 km
Aatamila 2011
Joint pain
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Bioaerosols, composting and health: Systematic review
Appendix 10: Diseases and Toxigenicity of Bioaerosols
Microbes and microbial species identified in bioaerosols generated from composts (Crook, Stagg, and
Uwagboe 2008, Fischer et al. 2000, Douwes et al. 2003, Allermann and Poulsen 2000, Vincken and
Roels 1984) with microbe size and associated diseases.
Airborne microorganism
Group
Disease or Toxigenicity
Size microns
Gram-negative bacteria/ endotoxin
Bacteria
opportunistic infection
0.5-2.0
Actinobacter sp.
Bacteria
opportunistic infection
1.25
Mesophilic fungi
Fungi
respiratory allergic response
3.0-4.0
Aspergillus fumigatus
Fungi
Aspergillosis
3.5
A. flavus
Fungi
Carcinogenic
3.0
A. giganteus
Fungi
hepatoxic nephrotoxic
3.25
A. niger
Fungi
Antibiotic
3.25
A. versicolor
Fungi
Carcinogenic
3.25
Penicillium spp.
Fungi
allergic alveolitis
3.3
P. roqueforti
Fungi
neurotoxic
3.25
P. crustosum
Fungi
tremorgenic*
3.0
P. clavigerum
Fungi
hepatoxic/nephrotoxic/tremorgenic
3.0
Emericella nidulans
Fungi
allergic alveolitis
3.25
E. nidulans
Fungi
Carcinogenic
3.25
Absidia corymbifera
Fungi
zygomycosis/mucormycosis**
3.75
Paecilomyces sp.
Fungi
allergic alveolitis
3.0
*Tremorgenic mycotoxins are fungal secondary metabolites with a specific effect on the central nervous system (causing tremors), most of
which are synthesized by common saprophytic moulds of the genera Penicillium and Aspergillus.
**Absidia corymbifera is a genus of fungi in the family Mucoraceae, of the Zygomcota phylum, which causes zygomycosis, especially in
the form of mycotic spontaneous abortion in cows. It can also cause mucormycosis in humans. It is an allergenic that could cause mucorosis
in individuals with low immunity. It usually infects the lungs, nose, brain, eyesight and skin. While oral or cerebral mucormycosis are the
most common types of the disease, this infection can also manifest in the gastrointestinal tract, skin, and in other organ systems.
Absidia spp. are ubiquitous in most environments. They are often associated with warm decaying plant matter, such as in compost heaps
(Roden
et
al.
2005)
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Bioaerosols, composting and health: Systematic review
23