ARTICLE IN PRESS

Int. J. Hyg. Environ. Health 211 (2008) 121–131

1438-4639/$ - se

doi:10.1016/j.ijh

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Guido.Fischer@

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Recommendations for study design and sampling strategies for

airborne microorganisms, MVOC and odours in the surrounding of

composting facilities

Andreas Albrechta,c,1, Guido Fischera,b,1, Gefion Brunnemann-Stubbea,Udo Jackela,d, Peter Kampfera,�

aInstitut fur Angewandte Mikrobiologie, Justus-Liebig-Universitat Giessen, Heinrich-Buff-Ring 26-32, 35392 Gießen, GermanybInstitut fur Hygiene und Umweltmedizin, Juniorprofessur ‘‘Umwelthygiene-Mykologie und biogene Umweltnoxen’’,

Universitatsklinikum Aachen, Pauwelsstr. 30, 52074 Aachen, GermanycBundesanstalt fur Arbeitsschutz und Arbeitsmedizin, jetzt: Berufsgenossenschaft fur Gesundheitsdienst und Wohlfahrtspflege,

Neureuter Straße 37 b, 76185 Karlsruhe, GermanydBundesanstalt fur Arbeitsschutz und Arbeitsmedizin, Noldnerstraße 40-42, D-10317 Berlin, Germany

Received 20 December 2006; received in revised form 22 May 2007; accepted 24 May 2007

Abstract

Microorganisms and odour emissions from composting plants often lead to complaints by residents, especially bypeople living close to such plants. Both parameters were studied in a systematic approach under specific localmeteorological conditions at nine different composting plants in Germany with emphasis on dispersal ofmicroorganisms. Measurements were done at emission points and at sampling sites in the downwind and upwinddirections of the facilities under ‘normal case’ (i.e. weather conditions typical for the location in combination withworking activities at the plants) and ‘real worst case’ conditions (dispersal of bioaerosols into the surroundingsexpected to occur with high probability). Airborne microorganisms were sampled using filtration and impingement.Subsequent cultivation on four different culture media allowed quantification and identification of the culturablemicroflora. It turned out that a general assessment of emissions and dispersal of bioaerosols from composting plants isnot possible because of the coherences of various factors influencing the dispersal. The site-specific meteorologicalsituations must be considered carefully, whenever sampling locations are selected and need to be recorded in anysampling protocol. Air inversions in particular can lead to high concentrations of microorganisms (4104–105 cfum�3

of thermophilic actinomycetes and thermotolerant fungi) in the surroundings of composting plants. Finally, it wasshown that both thermotolerant fungi and thermophilic actinomycetes can serve as indicator organisms.r 2007 Elsevier GmbH. All rights reserved.

Keywords: Bioaerosols; Airborne microorganisms; Odour; Composting; Measurement strategy; Emission

e front matter r 2007 Elsevier GmbH. All rights reserved.

eh.2007.05.004

ing author. Tel.: +49641 9937352;

37359.

esses: Andreas.Albrecht@bgw-online.de (A. Albrecht),

post.rwth-aachen.de (G. Fischer),

baua.bund.de (U. Jackel),

agrar.uni-giessen.de (P. Kampfer).

equally.

Introduction

The composting process, now an integral part ofmodern waste management strategies, is based on theprinciple of recycling with the objective of mass and

ARTICLE IN PRESSA. Albrecht et al. / Int. J. Hyg. Environ. Health 211 (2008) 121–131122

volume reduction of the biodegradable parts of solidwastes. The compost generated can be used for variouspurposes, but is mostly used as organic fertiliser inagriculture. In 2001, more than 600 full-scale compost-ing plants processed nearly 6–7 million tons of biologicalwastes in Germany (Kampfer and Weißenfels, 2001).Most of these existing composting facilities were builtwithin the last 10–15 years and, because of a relativelyhigh population density, it was often difficult to findsuitable locations for such plants. Often they were set upclose to residential areas without consideration ofspecific topographical or, more importantly, meteoro-logical facts. In recent years, the proximity of compost-ing plants to residential areas have raised the question,whether biological emissions originating from compost-ing plants might have a negative impact on the health ofresidents.

Compost as source of bioaerosols

Because self-heating to 55–60 1C is an inherent partof the composting process (Lacey and Crook, 1988)the number of thermophilic and thermotolerantmicroorganisms increases clearly during the thermo-philic composting phase. These include, for example,not only mucoraceous fungi, penicillia, and aspergilli,especially Aspergillus fumigatus (Fischer, 2000; Fischeret al., 2001, 2004a, b, 2005; Haas et al., 1999; Millneret al., 1994), but also Bacteria or methanogenic Archaea

(Jackel et al., 2005; Thummes et al., 2007), whichshowed that compost contains in total about 1010–1011

microbial cells per gram of dry material. Duringcomposting, the initially shredded organic materialsare moved repeatedly. Towards the end of the process,the compost is sieved to remove large fragments,including materials which are not readily biodegradable.Because a part of the mentioned microorganismsare able to produce airborne spores, these propagulescan be released into the surrounding during varioussteps of waste treatment (Kampfer et al., 2002;HMFUFL, 1999; Reiß, 1995). The spectrum of micro-organisms emitted can change throughout the differentphases of composting as was shown, e.g., for microfungi(Fischer, 2000).

Important properties of bioaerosols

It has been known for a long time that bioaerosolsoriginating from compost or composting facilitiescontain vegetative cells and spores of microorganisms,especially of actinomycetes and fungi (Millner et al.,1977, 1980, 1994). The cells, spores or hyphae are oftenattached to each other as aggregates or bound toorganic particles (Henningson and Ahlberg, 1994). Thevast majority of the airborne microorganisms (with

the exception of some Gram-positive bacteria andfungal spores) are rapidly inactivated as a result ofdesiccation, temperature increase or UV radiation(Mohr, 1997). Because of these environmental stressfactors, viable and culturable fractions represent only asmall part of the total microorganisms present inbioaerosols. The classic cultivation-based detectionmethods for microorganisms on solid media cansignificantly underestimate the total numbers ofmicroorganisms (Albrecht and Kampfer, 2000; Kampferand Neef, 2002). It has been estimated that platecounts record only 10% or less of the total popu-lation within environmental samples (Griffith andDeCosemo, 1994). Furthermore, the total number ofculturable microorganisms does not provide specificinformation about the ability of a microorganism tocolonise and/or infect a host (Griffith and DeCosemo,1994).

Hygienic relevance of bioaerosols

Bioaerosols can be hazardous to humans in a numberof ways. Infections can occur after inhalation oringestion of viable pathogenic or potentially pathogenicmicroorganisms, which are mainly relevant for immu-nocompromised people. Even among highly exposedworkers in composting plants, infections due to micoor-ganisms in organic dust are rarely reported. Butexposure to elevated concentrations of airborne micro-organisms can lead to sensitization and initiate allergicdiseases. For the initiation of an allergic response theviability of these microorganisms is not a prerequisite,because dead cells and cell debris may also containallergens. For this reason, the total number of airbornemicroorganisms is as important as the number ofcolony-forming units (CFU) (Griffith and DeCosemo,1994; Millner et al., 1994). Even fragments of microbialcells (e.g. cell walls, flagella and genetic material) andmetabolites of microbial origin (e.g. volatile organiccompounds, endotoxins, and mycotoxins) are ofconcern (Stetzenbach, 1997). Airborne thermophilicactinomycetes (e.g. Thermoactinomyces vulgaris andSaccharopolyspora rectivirgula) were implicated in sev-eral cases of hypersensitivity-induced pneumonitis andother allergic reactions. These microorganisms naturallyoccur in organic materials that self-heat to temperaturesof 65–70 1C, e.g. during composting (Lacey and Crook,1988; Stetzenbach, 1997). The only known mesophilicactinomycetes implicated in allergic alveolitis are Strep-

tomyces olivaceus and S. albus (Lacey and Crook, 1988).Airborne thermophilic and thermotolerant fungi arealso very important disease-initiating agents, combininginfectious, allergenic, and toxinogenic properties(Fischer et al., 2005).

ARTICLE IN PRESSA. Albrecht et al. / Int. J. Hyg. Environ. Health 211 (2008) 121–131 123

Dispersal of bioaerosols

Aspergillus and Penicillium species are some of themost abundant fungi in composting processes (Fischer,2000; Fischer et al., 2004a). When compost material ismixed, these microorganisms are dispersed into the airin large numbers (Lacey and Crook, 1988). On the otherhand, the dominance of Cladosporium and Alternaria innatural environments is well known (Millner et al., 1994;Lacey, 1996). The thermotolerant A. fumigatus, anallergenic, toxigenic, and opportunistic mould, has beenisolated worldwide and is common in the environment.However, its concentration in the natural environment isusually low in comparison with other fungi, such asCladosporium and Alternaria (Fischer et al., 2005;Millner et al., 1994). When there are sources of self-heating materials in the environment, e.g. windrows in acomposting plant, the concentration of A. fumigatus canincrease (Fischer et al., 2004b; Lacey and Crook, 1988).In conclusion, dominance of A. fumigatus in thedownwind vicinity of a composting plant, therefore, isan indication for the release of emissions from the plant(Fischer et al., 2004a; Millner et al., 1977, 1980, 1994;Recer et al., 2001).

Odour dispersal

In addition, composting processes often are sourcesof massive odour emissions, and the location ofcomposting plants in close proximity to residentialareas often leads to acceptance problems of thecomposting technology in general. Although biofiltersare used to reduce the load of odours, they are notalways effective. Despite these problems, data on (a)odour concentrations in the surrounding areas, and (b)transport of microorganisms and odours are relativelyscarce, and a detailed analysis of possible coincidencesin the surroundings of composting facilities is stillmissing.

Aims of the study

In the light of this complex situation, extensiveinvestigations were performed at several compostingplants in Germany to determine the dispersal ofmicroorganisms from composting material into thesurroundings (Kampfer et al., 2002). Site-specificsampling strategies were developed considering thetopographic and meteorological conditions, whichenabled aerial transport from the plant to the individu-ally selected sampling points. The objective of thispublication is to formulate recommendations for so-phisticated sampling strategies, when bioaerosol emis-sions from composting facilities and their dispersal mustbe assessed with respect to the specific situation at each

facility. It is demonstrated, that local topographical andmeteorological conditions are crucial factors, whichinfluence the aerial transport of microorganisms andodours. Widely standardised methods often used inGermany for measuring microbiological agents, odoursand weather parameters are described in detail. Basedon hypotheses formulated on the basis of the dataassessed (see Fischer et al., 2007), consequences andrecommendations are deduced for differentiated con-cepts of investigations in the future.

Material and Methods

Study design and sampling strategy

Concentrations of microorganisms and odours werestudied in nine different composting facilities (for adetailed description, see Table 1) and at sampling sites inthe surrounding of the composting facilities. At eachplant, five sampling points were defined for emissionmeasurements and seven sampling sites in the surround-ings. Five or six points were established in increasingdistances downwind and one or two of the samplingpoints were located upwind from the plant. The latterwere used as reference points to measure backgroundlevels of aerosol concentrations.

Specific topographic situations and meteorologicalcircumstances were considered for the measurements ateach plant and were carefully registered during thesamplings. Measurements in the surroundings wereperformed only in case of stable meteorological condi-tions, when constant and almost undisturbed transportof microorganisms could be expected (forecast system ofthe German’s National Meteorological Service(Deutscher Wetterdienst DWD), Germany). All mea-surements were carried out under constant winddirections and predominantly low wind velocities of upto a maximum of 2m s�1. Odours and microorganismswere measured simultaneously.

One set of measurements was made under ‘standardconditions’ (most frequently occurring meteorologicalconditions). Usual working activities at the plant(compost material was moved or shredded) werecharacteristic for this ‘normal case’ (see Fig. 1 formoving and Fig. 2 for sieving). Another set ofmeasurements was carried out during drainage flowconditions in hilly grounds and stable atmosphericlayering (cold air flows very slowly in the downhilldirection in the early hours of cloudless nights). Like-wise, usual operational activities were maintained in theplants (‘real worst case’ scenario). During measurementsin the surrounding, relevant meteorological parameters(humidity, air temperature, wind direction and velocity)were registered.

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Table 1. Concept and type of process engineering for composting, input and capacity, topographical and meteorological situation

as well as distances to residential areas of the compost facilities investigated

Concept/process Input and capacity Topographical and

meteorological situation

Remarks

1 � Enclosed� Biofilter� Enclosed storage

� Domestic wastes 95%� Plant residues 5%� 40 000 t/a

� Next residences in

500m� Drainage flow situation

Landfill site next to the

compost facility

2 � Open pile� Open storage, covered

by a roof

� Domestic wastes 85%� Plant residues 15%� 6 500 t/a

� Next residences in

1100m� Main wind direction:

W/E� Drainage flow situation

Regular complaints of the

residents near the facility,

independent from daytime

3 � Open pile, covered with

a semi-permeable

membrane� Open storage, covered

by a roof

� Domestic wastes 70%� Plant residues 30%� 8000 t/a

� Next residences in

500m� Main wind direction:

SW� Drainage flow situation

No complaints of the

residents since covering

the piles with a membrane;

Measurements at wind

from N-NE

4 � Enclosed tunnels� Open storage, covered

by a roof

� Domestic wastes 85%� Plant residues 15%� 30 000 t/a

� Next to residences� Main wind direction:

SE� No drainage flow

Rare complaints of the

residents near the facility

5 � Open pile� Open storage, covered

by a roof

� Domestic wastes 75%� Plant residues 25%� 6 000 t/a

� Next residences in

500m� Main wind direction:

NW� Drainage flow situation

No dusty working

activities at certain

weather conditions

6 � Open pile , covered

with a semi-permeable

membrane

� Domestic wastes 90%� Plant residues 10%� 25 000 t/a

� Next residences in

500m� Main wind direction:

S–SW� Drainage flow situation

Measurements at wind

direction from E; 2 stables

of turkeys near the facility

7 � Enclosed� Biofilter and wet

precipitator� Storage open/covered

by a roof

� Domestic wastes 90%� Plant residues 10%� 60 000 t/a

� Next residences in

600m� Main wind direction:

W� Drainage flow situation

Regular complaints of the

residents near the facility

8 � Enclosed� Biofilter and wet

precipitator� Open storage

� Domestic wastes 70%� Plant residues 30%� 20 000 t/a

� Next residences in

300m

No complaints of the

residents

9 � Enclosed� Bofilter and wet

precipitator� Enclosed storage

� Domestic wastes 77%� Plant residues 23%� 40 000 t/a

� Next residences in

350m

Next to a motorway

junction

Numbering of facilities corresponds to Fischer et al. (2007).

A. Albrecht et al. / Int. J. Hyg. Environ. Health 211 (2008) 121–131124

Emission of bioaerosols was measured at active sourceswith a quantifiable exhaust air rate (biofilters) as well as atpassive diffuse sources without a measurable exhaust air

rate (shredding, sieving of fresh or ripened compost, pilesin idle or turnover situations). Biofilters samples weretaken both from raw as well as from clean air (Fig. 3).

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Fig. 1. Measuring with a MD8 filtration sampler during

moving of a compost pile. Fluid aerosols containing micro-

organisms are seen behind the moving machine.

Fig. 2. Sieving situation in an open storage covered by a roof.

In front of the excavator the top of a MD8 filtration sampler is

seen (left side).

Fig. 3. Hood for measurements of flow velocities according to

VDI 3475 (Anonymous, 2003) placed on a biofilter of a

composting plant. Inside the evacuated fibre glass box on the

hood, the polycarbonate foil sampling bag is located. A

sampling port for measurements of bioaerosols is placed at the

extension of the hood-nozzle.

A. Albrecht et al. / Int. J. Hyg. Environ. Health 211 (2008) 121–131 125

Recommendation for standardised strategies and

methods

The comparability of results generated in the presentinvestigation depends on the standardisation of themethods and strategies used. A summary of the methodsused was given by Kampfer and Albrecht (2001).

These protocols can serve as standard approaches forthe investigation of bioaerosols and odours insidecompost facilities as well as in the surrounding areas,with the focus on comparability.

Documentation of weather and visualisation of

drainage flow conditions

Relevant weather conditions for ‘normal case’ as wellas ‘real worst case’ scenarios (see definition in sampling

strategies) were selected by experts of the German’sNational Meteorological Service (Deutscher Wetter-dienst DWD). Next to the measurements of aerosolsand odours, meteorological parameters such as humid-ity (capacitive humidity sensor (Rotronic, Ettlingen,Germany), mean values of 10min), air temperature(platinum-thermometer, measuring every second andcalculation of mean values of 10min), wind direction,and wind velocity (ultrasonic anemometer, Gill, Ger-many; measuring every 0.25 s and calculation of meanvalues of 10min) were documented at one location at10m height and at three to four other locations at 2mheight (Fig. 4: technical device for measurements ofclimate data at heights of 2 and 10m).

Air movements, especially drainage flow (‘real worstcase’), were visualised by release of coloured smokefrom cartridges (Ubax V grau-weiß, Blornax, Sweden orRauchstein weiß, Komet AG, Bremerhaven, Germany).Smoke was emitted for 4 or 10min without producingheat. The smoke was transported over distances of100m or more by horizontal air movements, becausethere was no buoyancy. These experiments were done byiMA (Richter & Rockle, Freiburg, Germany) in the firsthours of nights with very few clouds. Experimental

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Fig. 4. Mast for measurements of weather parameters (wind

direction, wind velocity, air temperature, humidity) at heights

of 2 and 10m. The mast is placed near a composting plant.

A. Albrecht et al. / Int. J. Hyg. Environ. Health 211 (2008) 121–131126

measurements and visualisations of drainage flow weredone on several sampling dates. During all measure-ments in ‘real worst case’ situations soap bubbles wereused to visualise local air movements as one part ofquality management.

Results

From the measurements carried out (3 years, 9facilities, 36 measurements) in composting facilities ofdifferent types of process engineering (Table 1) and intheir surrounding (see Fischer et al., 2007) hypothesesfor the emission and dispersal of microorganisms wereformulated (described below). Consequences and re-commendations were deduced from each hypothesis andshould be critically evaluated and tested in futurestudies. A checklist of parameters to be measured orassessed in future investigations (Table 2) was compiledon the basis of the data presented in Fischer et al.(2007).

Emission of airborne microorganisms

With respect to the dispersal of microorganisms twohypotheses can be formulated for further investigations

on the basis of the data of the present study (Fischeret al., 2007):

(1)

The thermophilic actinomycetes and thermotolerantmicrofungi can serve as indicator microorganismsfor the measurement of bioaerosols at biowaste-handling facilities.

(2)

Ratios of the two groups may be used to identifysources of emission (turning, sieving).

It was already discussed that thermophilic andthermotolerant microorganisms (actinomycetes andfungi) play an important role in transformationprocesses during the thermophilic phase of composting.These organisms are found in higher concentrations inair samples in the surroundings of composting plantsthan in background samples (DVGW, 1998; HMFUFL,1999; Kampfer et al., 2002; StMLU, 1999, Muller et al.,2004a; Fischer et al., 2004a, b).

Consequences and recommendations

(1)

The microbial parameters assessed in downwinddirection of composting facilities should be thermo-philic actinomycetes and thermotolerant fungi.Mesophilic fungi and bacteria are not suited asindicator microorganisms, because background con-centrations may be too high.

(2)

Nevertheless, bacteria can be the prevalent micro-organisms emitted by biofilters and, for this purpose,should be measured to quantify emissions frombiofilters.

(3)

There are some indications that actinomycetes occurin highest concentrations during sieving (ripenedcompost), whereas during turning (fresh compost)the thermotolerant fungi seem to predominate.Therefore, both parameters must be assessed tocharacterise the emissions from plants concerningthe estimation of health hazards.

Dispersal of airborne microorganisms in downwind

direction

Two hypotheses were deduced from the data (Fischeret al., 2007) for further investigations.

(1)

Under ‘real worst case’ and ‘normal case’ conditions,concentrations of thermotolerant fungi and thermo-philic actinomycetes in 600–1400m distance fromthe plant are 1–2 orders of magnitude highercompared with natural background levels.

(2)

Background concentrations of thermotolerant mi-croorganisms have to be assessed in distances4300m in upwind direction from the facilities toexclude any contamination from the plant.

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Table 2. Recommendations for target-orientated investigations in the surrounding of composting facilities under ‘normal case’

(‘NC’) or ‘real’ worst case (‘RWC’) conditions

Type of facility Total

CFU

Therm.

fungi

Therm.

actinom.

Meso.

fungi

Olfacto-

metry

Odour

measurements*Meteorological

datesa

Enclosed (inhouse

or tunnels)

Biofilter Surrounding

‘NC’

| | | | |

Surrounding

‘RWC’

| | | | |

Emission | | | | (|)b

Open pile Static or

coveredcSurrounding

‘NC’

| |

Surrounding

‘RWC’

| |

Emission | (|)b

Turning Surrounding

‘NC’

| | | | | |

Surrounding

‘RWC’d| | | | | |

Emission | | | | | (|)b

Activities outsided Shredding

sieving

Surrounding

‘NC’

| | | | | |

Surrounding

‘RWC’

| | | | | |

Emission | | | | | (|)b

(actinom. ¼ actinomycetes, therm. ¼ thermophilic species, meso. ¼ mesophilic species)*measurements of MVOC only for specific questions.aHumidity and temperature of air, direction and velocity of wind, sometimes visualisation of air movements by release of coloured smoke.bOnly temperature and humidity of air.cCovered by semi-permeable membranes (without turning).dUsually no activities at night, only for investigation targets.

A. Albrecht et al. / Int. J. Hyg. Environ. Health 211 (2008) 121–131 127

It is obvious, that airborne microorganisms may be

transported over distances of up to 1000m downwindunder special conditions. However, in most cases, theinfluence of the facilities could only be documented fordistances of up to 300 or 500m. Earlier investigations(HMFUFL, 1999; Kampfer et al., 2002; Muller et al.,2004a; StMLU, 1999;) have also shown the possibility ofairborne transport of microorganisms over distances of500m, especially during working activities. Airbornetransport is dependent on various factors, whichindicates that a general recommendable minimumdistance between compost plants and residential areascannot be defined. It is obvious that the regulation(determination) of appropriate buffer distances shoulddepend on the

(a)

specific location, (b) design of the plant, (c) type of process engineering, (d) local micrometeorological conditions, and (e) emission controls.

Investigations in North-Rhine Westphalia showedthat even at distances of 800m , levels of thermotolerantfungi can be increased one order of magnitude(MUNLV, 2002). Up to now, regulations in this state

prescribe a minimum distance of 300 or 500m depend-ing on the annual turnover of the plant. In thesurrounding of some composting facilities, odours wereperceptible under special conditions at night when noactivities with moving materials occurred (e.g. ‘realworst case’ scenario). It must be considered, that theforecast of ‘real worst case’ situations is very difficulteven for institutions with extensive experience and aspacious measuring net. Drainage flows are influencedby different factors which are being discussed elsewherein literature (Rockle and Richter, 1998; Rockle et al.,1998; Anonymous, 2000, 2002). Nevertheless, investiga-tions focussed on possible transport distances ofmicroorganisms have to consider ‘normal case’ as wellas ‘real worst case’ scenarios.

Consequences and recommendations for future

investigations

(1)

As concentrations of thermophilic and thermotoler-ant microorganisms can be significantly increased(one order of magnitude) for distances greater than500m (800–1400m), depending on weather andatmospheric conditions, sampling locations mustbe established for distances greater than 500m aswell.

ARTICLE IN PRESSA. Albrecht et al. / Int. J. Hyg. Environ. Health 211 (2008) 121–131128

(2)

Reference concentrations must be assessed at dis-tances of more than 300m to exclude any influencefrom the facilities by turbulent airflow.

Emission of microbes and odour compounds from

biofilters and diffuse sources

Two hypotheses were deduced from the data of thepresent study (Fischer et al., 2007) for further investiga-tions:

(1)

Biofilters emit higher concentrations of odourcompared with static piles and open windrows.

(2)

Odour emission during turning, sieving and shred-ding may exceed those from the biofilters.

Main sources of odour during the day were those siteswhere working activities (‘normal case’) are carried out.As a rule, such activities were restricted to the day andtherefore, the biofilters became the most importantsources for odours during the night. Emission of odourfrom static piles seems to be less important for drainageflow (‘real worst case’) situations.

Biofilters were developed to reduce biologicallydegradable odours in waste gases by the activity ofmicroorganisms settled on the filter material. Thereduction of odour concentrations with an efficiency of90–95% shows that in most cases biofilters come up totheir purpose. However, biofilters were not developedprimarily to reduce concentrations of microorganisms.In some cases, they may even be a source formicroorganisms, which is comprehensible, because thereduction of odour is a result of the activity of fungiand bacteria (Anonymous, 1991). On the other hand,biofilters can only insufficiently reduce the concentra-tion of microorganisms and it should be kept inmind that a concentration of 106 cfum�3 of thermo-tolerant fungi in raw air can only be reduced to104 cfum�3 in clean air (99% reduction supposed). If104 cfum�3 of thermotolerant fungi are constantlyemitted by biofilters, such concentrations may alter thefungal airspora in downwind direction significantly(Fischer et al., 2004a) compared with the naturalbackground level.

While high numbers of thermophilic microorganismswere to be expected during turning of piles and sievingor shredding of compost, emissions from static piles donot seem to be relevant for total emission concentrationswhen biofilters are part of the process engineering.

Consequences and recommendations

(1)

The biofilters need to be maintained accurately toavoid emissions of MVOC, other odour compoundsor thermotolerant microorganisms.

(2)

Different biofilter segments at one facility may emitcompletely different qualities and quantities ofmicroorganisms.

Incidence of odour perception in the surroundings of

the facilities

Two hypotheses were deduced from the data of thepresent study (Fischer et al., 2007) for further investiga-tions:

(1)

The incidence of odour perception in the surround-ings of the facilities under drainage flow conditions(‘real worst case’) is not generally higher comparedwith normal case conditions. Dispersal of odourseems to be favoured under (A) normal caseconditions in combination with flat topographyand (B) under drainage flow conditions, when thefacility is situated in a valley.

(2)

The incidence of odour perception was increased athigher distances (4 800m) at those facilities, wherethe ratio of green waste to domestic biowaste did notexceed 15%.

Consequences and recommendations for practical

application

(1)

The topography and the atmospheric conditionshave to be considered in future investigations, as acertain combination of these factors is likely to leadto increased incidences of odour for distances of upto 800–1400m from the plant. In areas with flattopography, bioaerosol measurements should becarried out under most frequently occurring meteor-ological conditions. In hilly landscapes, drainageflow conditions with stable atmospheric layeringshould be preferred for bioaerosol assessment.

(2)

The ratio of green waste and domestic (bio)wastesupposedly determines an increased incidence ofodour perception in the surroundings of the facil-ities. A ratio of less than 15% green waste todomestic (bio)waste is proposed as a critical valuewith respect to odour emissions.

Coincidence of odours and concentrations of

airborne microorganisms

The following observation was deduced from the dataof the present study (Fischer et al., 2007):

Odours and microorganisms seem to coincide

qualitatively, but not quantitatively

To our knowledge, this is the first investigationthat systemically compares odour measurements with

ARTICLE IN PRESSA. Albrecht et al. / Int. J. Hyg. Environ. Health 211 (2008) 121–131 129

concentrations of compost specific microorganisms on alarge scale. Only few systematic scientific studies havebeen done on the correlation between concentrations ofairborne microorganisms and odours at all. Partlycomparable investigations of combined measurementof microorganisms and air by field inspections corre-sponding to VDI 3940 were published by other authors(DVGW, 1998). In the surrounding of three compostingplants in Germany, in only three out of 17 cases, acoincidence was found in the transmission of micro-organisms and odours. The causal relation betweenodour perception and the occurrence of specific MVOCis under debate. The conclusion drawn here is based onmeasurements at only three out of nine plants and theanalysis of selected MVOC. On the other hand, recentlypublished results (Fischer et al., 2004a; Muller et al.,2004a, b) show coincidences between odours andMVOC. These investigators measured a partly differentspectrum of 27 MVOC-compounds. For only some ofthese a coincidence with odours was shown. Unfortu-nately, the relevant compounds of these new publica-tions were not measured in the project presented here.

Occurrence of MVOC in the surrounding

Three hypotheses were deduced from the data of thepresent study (Fischer et al., 2007) for further investiga-tions.

(1)

Concentrations of MVOC above the backgroundlevel seem to coincide generally with increasedpercentages of odour perception at greater distancesfrom the facility. A strict quantitative coincidence ofboth parameters was not observed.

(2)

Higher concentrations of MVOC can be found atgreater distances (4800 or 41200m) in normal casesituations, and concentrations were not consistentlyincreased under drainage flow conditions.

(3)

The MVOC measured here are not solely respon-sible, but may at least contribute to the typicalcompost odour.

Consequences, recommendations for practical application

A wider spectrum of MVOC (see Muller et al.,2004a, b; Fischer et al., 2004b) should be measured incase of odour problems in the surrounding of compost-ing facilities or when irritation of mucous membraneswere observed in residents. MVOC seem to be a sensitivemarker for emissions from the facilities (see Table 2).

Conclusions for future investigations

More detailed analytical data of the present investiga-tion of nine different composting plants and of their

surroundings were published by Fischer et al. (2007) inthe same issue. General recommendations deduced fromthese data are given in the following paragraphs. Ingeneral, the plant-specific situation must be consideredin any sampling strategy. The topography and site-specific meteorological situations are of major impor-tance for the spreading of odours and microorganisms.Thermotolerant fungi and thermophilic actinomycetescan be used as indicator organisms for air emissionsfrom composting plants. The following recommenda-tions can be given:

1.

The type of the composting plant and the sources ofemission must be considered carefully. Open systemsare totally different from housed composting tech-nologies mainly with respect to emission character-istics. Even biofilters mostly used in closed systemscan contribute to emissions of both odour andmicroorganisms.

2.

The topography in relation to the local meteorologi-cal conditions is of significant importance. Airinversions, which occur mostly in the evening or atnight, can lead to a more or less undiluted dispersionof odours in ‘real worst case’ situations. Thespreading of microorganisms in relevant amountscan only be measured during working procedures,such as shredding, sieving, or turning of piles.Therefore, such activities should not be done at nightwhen ‘real worst case’ situations are most likely tooccur.

3.

Generally, samplings should be performed under‘normal case’ conditions (most common meteorolo-gical conditions with working activities). ‘Real worstcase’ conditions can be relevant for odour measure-ments and, additionally, for analysis of microorgan-isms if working activities are performed at night.

4.

No obvious coincidence between levels of airbornemicroorganisms and odours could be detected,neither during emission-investigations nor duringmeasurements in the surrounding.

5.

It is essential to assess meteorological data (windspeed, wind direction, humidity, etc.) during sampling.

6.

Quantification and identification of specific groups ofmicroorganisms (in particular: thermotolerant fungiand thermophilic actinomycetes) is highly recom-mended. Therefore, species-differentiated microbio-logical approaches must be applied and, moreover,research on new methods, which are independent ofcultivation, is necessary.

Deduction of recommendations for target-orientatedinvestigations in the future must be based on theconclusions discussed above based on the resultsof the present project (see Fischer et al., 2007).Recommendations on the parameters which have to beassessed in future investigations, with respect to

ARTICLE IN PRESSA. Albrecht et al. / Int. J. Hyg. Environ. Health 211 (2008) 121–131130

different constructional, topographic and local meteor-ological conditions, are summarised in Table 2.

Acknowledgements

This project was financially supported by the Ministryfor Education and Research (Bonn, Germany). Theauthors are grateful to the operating authorities of thecomposting plants involved for co-operation. Thesampling strategy, the methods used and the involvedcomposting plants were chosen in agreement with acommittee of experts and scientists from differentinstitutions and authorities. The authors would like tothank Mrs. Kraus (lawyer, University of Giessen) forher help in selecting the measurement teams by a publicinvitation of tenders (Bundesanzeiger and Die Zeit of09th of Dezember 1999) and award of contractsaccording to VOL (Verdingungsordnung fur Leistun-gen, Germany). Measurements of airborne microorgan-isms and analyses of odours were performed by the‘TUV Suddeutschland’ (Technischer Uberwachungsver-ein, Freiburg, Germany). Meteorological conditionswere measured by the ‘Deutscher Wetterdienst’ (Offen-bach, Germany). Visualisation of drainage flows bysmoke was done by iMA Richter & Rockle (Freiburg,Germany).

References

Albrecht, A., Kampfer, P., 2000. Wachstum und koloniemor-

phologisches Erscheinungsbild thermotoleranter und ther-

mophiler Actinomyceten. Gefahrstoffe-Reinhaltung der

Luft 60, 139–145.

Anonymous, 1991. Verein Deutscher Ingenieure (VDI):

Richtlinie 3477: Biological Waste Gas/Waste Air Purifica-

tion: Biofilters.

Anonymous, 2000. Verein Deutscher Ingenieure (VDI).

Richtlinie 3788, Part 1: environmental meteorology—

dispersion of odorants in the atmosphere—fundamentals.

Anonymous, 2002. Verein Deutscher Ingenieure (VDI).

Richtlinie 3787, Part 5: umweltmeteorologie; lokale kal-

tluft.

Anonymous, 2003. Verein Deutscher Ingenieure (VDI).

Richtlinie 3475, Part 1: emission control biological waste

treatment facilities-Composting and anaerobic digestion

plant capacities more than approx. 6000Mg/a.

DVGW-(Deutscher Verein des Gas- und Wasserfaches e.V.)

Forschungsstelle am Engler-Bunte-Institut der Universitat

Karlsruhe, 1998. Untersuchungsvorhaben zur Ausbreitung

von Keimen und Geruchen durch den Betrieb biologischer

Abfallbehandlungsanlagen, pp. 1–139.

Fischer, G., 2000. Comparison of microbiological and

chemical methods for assessing the exposure to air-borne

fungi in composting plants. Dissertation. In: Akademische

Edition Umweltforschung Band 10-Publikationsreihe des

interdisziplinaren Umwelt-Forums der RWTH Aachen.

Fischer, J.L., Albrecht, A., Kampfer, P., 2001. Mikrobiologie

der Kompostierung. In: Kampfer, P., Weißenfels, D.W.

(Eds.), Biologische Behandlung organischer Abfalle.

Springer, Berlin, Heidelberg, New York, pp. 3–43.

Fischer, G., Muller, T., Thißen, R., Braun, S., Dott, W.,

2004a. Process-dependent emission of airborne fungi and

MVOC from composting facilities. Air Quality Control 64,

160–167.

Fischer, G., Thißen, R., Muller, T., Braun, S., Dott, W.,

2004b. Microbial secondary metabolites as parameters for

exposure assessment in composting plants. Air Quality

Control 64, 229–238.

Fischer, G., Thißen, R., Hinz, R.-K., Hollbach, N., Schmitz,

C., Dott, W., 2005. Airborne moulds in human environ-

ment—health relevance and risk assessment. Air Qual.

Cont. 65, 335–340.

Fischer, G., Albrecht, A., Jackel, U., Kampfer, P., 2007.

Analysis of airborne microorganisms, MVOC and odour in

the surrounding of composting facilities and implications

for future investigations. Int. J. Hyg. Environ. Health., this

issue, doi:10.1016/j.ijheh.2007.05.003.

Griffith, W.D., DeCosemo, G.A.L., 1994. The assessment

of bioaerosols: critical review. J. Aerosol Sci. 25,

1425–1458.

Haas, D.U., Reinthaler, F.F., Wust, G., Skofitsch, G.,

Groth, I., Degenkolb, T., Schumann, P., Marth, E., 1999.

Emission of thermophilic actinomycetes in composting

facilities, their immediate surroundings and in an urban

area. Centr. Eur. J. Publ. Health 7, 94–99.

Henningson, E.W., Ahlberg, M.S., 1994. Evaluation of

microbiological aerosol samplers: review. J Aerosol Sci.

25, 1459–1492.

Hessisches Ministerium fur Umwelt, Landwirtschaft und

Forsten (HMFUFL) (Ed.), 1999. Umweltmedizinische

Relevanz von Emissionen aus Kompostierungsanlagen fur

die Anwohner. Immissionsmessungen und epidemiolo-

gische Daten und Befunde im Umfeld von drei Kompos-

tierungsanlagen, pp. 1–235.

Jackel, U., Thummes, K., Kampfer, P., 2005. Thermophilic

methane production and oxidation in compost. FEMS

Microbiol. Ecol. 52, 175–184.

Kampfer, P., Albrecht, A., 2001. Strategie zur Systematisierten

Untersuchung von Mikroorganismen-Freisetzungen aus

Kompostierungsanlagen und Erfassung der Immissionen

in deren Umfeld. In: Stegmann, R., Doedens, H., Hensel,

A. (Eds.), Hamburger Berichte Bd. 17-Abluft 2001. Verlag

Abfall aktuell, pp. 263–274.

Kampfer, P., Neef, A., 2002. Molecular identification of

airborne microorganisms from composting facilities. In:

Insam, H., Riddech, N., Klammer, S. (Eds.), Microbiology

of Composting. Springer, Berlin, Heidelberg, New York,

pp. 585–594.

Kampfer, P., Weißenfels, D.W., 2001. Biologische Behandlung

organischer Abfalle. Springer, Berlin, Heidelberg,

New York.

Kampfer, P., Jureit, C., Albrecht, A., Neef, A., 2002. Emission

of Microorganisms from Composting Facilities. In:

Insam, H., Riddech, N., Klammer, S. (Eds.), Microbiology

of Composting. Springer, Berlin, Heidelberg, New York,

pp. 571–584.

ARTICLE IN PRESSA. Albrecht et al. / Int. J. Hyg. Environ. Health 211 (2008) 121–131 131

Lacey, J., Crook, B., 1988. Fungal and actinomycete as

pollutants of the workplace and occupational allergens.

Ann. Occup. Hyg. 32, 515–533.

Lacey, J., 1996. Spore dispersal—its role in ecology and

disease: the British contribution to fungal aerobiology.

Mycol. Res. 100, 641–660.

Millner, P.D., Marsh, P.B., Snowden, R.B., Parr, J.F., 1977.

Occurence of Aspergillus fumigatus during composting of

sewage sludge. Appl. Environ. Microbiol. 34, 765–772.

Millner, P.D., Bassett, D., Marsh, P.B., 1980. Dispersal of

Aspergillus fumigatus from sewage sludge compost piles

subjected to mechanical agitation in open air. Appl.

Environ. Microbiol. 39, 1000–1009.

Millner, P.D., Olenchock, S.A., Epstein, E., Rylander, R.,

Haines, J., 1994. Bioaerosols associated with composting

facilities. Compost Sci. Util. 5, 6–57.

Ministerium fur Umwelt und Naturschutz, Landwirtschaft

und Verbraucherschutz NRW (MUNLV), 2002. For-

schungsprojekt Untersuchungen zur Emission und Immis-

sion von mikrobiellen Geruchsstoffen und luftgetragenen

Schimmelpilzen aus Kompostierungsanlagen,’’ gefordert

durch das MUNLV NRW, Verfasser: Dr. G. Fischer,

Institut fur Hygiene und Umweltmedizin der RWTH

Aachen, Universitatsklinikum Aachen.

Mohr, A.J., 1997. Fate and Transport of Microorganisms in

Air, Manual of Environmental Microbiology, Washington,

pp. 641–650.

Muller, T., Thißen, R., Braun, S., Dott, W., Fischer, G.,

2004a. (M)VOC and composting facilities part 1: (M)VOC

emissions from municipal biowaste and plant refuse.

Environ. Sci. Pollut. Res. 11, 91–97 (online first, 2003).

Muller, T., Thißen, R., Braun, S., Dott, W., Fischer, G.,

2004b. (M)VOC and composting facilities part 2: (M)VOC

dispersal in the environment. Environ. Sci. and Pollut. Res.

11, 152–157 (online first 2003).

Recer, G.M., Browne, M.L., Horn, E.G., Hill, K.M., Boehler,

W.F., 2001. Ambient air levels of Aspergillus fumigatus and

thermophilic actinomycetes in a residential neighbourhood

near a yard-waste composting facility. Aerobiologia 17 (2),

99–108.

Reiß, J., 1995. Moulds in containers with biological wastes.

Microbiol. Res. 150, 93–98.

Rockle, R., Richter, C.-J., 1998. Ausbreitung von Geruchs-

stoffen in Kaltluftabflussen—messungen und modellrech-

nungen. VDI-Berichte 1373 ‘‘Geruche in der Umwelt,’’

249–259.

Rockle, R., Richter, C.-J., Enderle, K.-H., 1998. Geruchsaus-

breitung innerhalb von Kaltluftabflussen. Entsorgungs

Praxis 7–8, 36–40.

Stetzenbach, L., 1997. Introduction to aerobiology. In:

Manual of Environmental Microbiology. American Society

for Microbiology, Washington, DC, pp. 617–628.

StMLU (Bayerisches Staatsministerium fur Landesentwick-

lung und Umweltfragen). 1999. Keimemissionen aus

biologischen Abfallbehandlungsanlagen—Ausbreitung luft-

getragener Keime aus Kompostierungs- und Vergarung-

sanlagen, Munchen, pp. 1–37.

Thummes, K., Kampfer, P., Jackel, U., 2007. Temporal

change of composition and potential activity of the

thermophilic archaeal community during the compo-

sting of organic material. Syst. Appl. Microbiol. 30,

418–429.