1337

Agnieszka Kalwasin
ska

Aleksandra Burkowska
Maria Swiontek Brzezinska
Faculty of Biology and Environmental
Protection, Department of
Environmental Microbiology and
Biotechnology, Nicolaus Copernicus
University, Torun, Poland
Research Article
Exposure of Workers of Municipal Landll Site to
Bacterial and Fungal Aerosol
The present research was aimed at assessing the quality of air in work environment of
the municipal landll site in Torun
. Air samples were collected in the outdoor space
(operating landll cell, technological square), and in indoor space (sorting station,
weighing station, social room) using the impaction method. The microbiological air
testing included determining the number of airborne mesophilic bacteria and molds.
Bacterial strains were identied with appropriate API tests; molds were identied
according to their macro and micro characteristics. In outdoor air, the highest average
concentration of mesophilic bacteria were recorded at the operating landll cell (1361
colony forming unit (CFU)/m3). The highest average concentrations of molds were
recorded at the technological square (1179 CFU/m3). In indoor air, the highest average
concentration of investigated microorganisms (bacteria: 10 707 CFU/m3, molds:
12 471 CFU/m3) were recorded in the sorting facility. The concentration of micro-
organisms in the outdoor air depended on the season (p < 0.05), but did not depend on
the sampling site, while in the indoor air depended on the sampling site (p < 0.05) but
did not depend on the season. Bioaerosol emitted in municipal facility was the source of
bacterial (Bacillus subtilis, Pseudomonas aeruginosa) and fungal species (Aspergillus fumigatus,
Madurella grisea, Penicillium manfferei, Scedosporium apiospermium, Cryptococcus neoformans),
posing a health risk for humans. However Gram-negative bacteria constituted only a
small fraction of the isolated microorganisms. The highest risk of exposure to biological
agents was determined in the sorting station. The majority of the outdoor air samples
were classied as uncontaminated. The results emphasize the need for regular
monitoring of microbiological tests in indoor and outdoor air of municipal landll sites
as well as for control strategies in order to protect workers at landll.
Keywords: Air quality; Bacteria; Bioaerosol; Molds; Occupational exposure
Received: May 15, 2013; revised: August 27, 2013; accepted: September 23, 2013
DOI: 10.1002/clen.201300385

1 Introduction
Exposure to biological agents at work (occupational exposure) is a major
problem of occupational medicine and public healthcare because it is
associated with detrimental health effects ranging from simple
irritation and discomfort to allergic reactions, infections, infectious
diseases, and toxic reactions [1, 2]. In the work environment, harmful
biological agents are most commonly components of bioaerosols.
Pathogens and allergens, transmitted in the air through dust or liquid
droplets, invade the body through the skin and mucous membranes or
are introduced by a bite of hematophagous insects. At landlls,
concentrations of airborne bacteria and molds can be hundreds to
Correspondence: Dr. A. Kalwasi

nska, Faculty of Biology and Environmental
Protection, Department of Environmental Microbiology and Biotechnology,
Nicolaus Copernicus University, Lwowska Street 1, 87100 Torun,
Poland
E-mail: kala@umk.pl
Abbreviations: CFU, colony forming unit; CHP, heat and power plant;
MSWMP, municipal solid waste management plant
thousands times higher than in homes and public buildings [35].
Employees of municipal landll sites with the collection and disposal of
municipal waste (i.e., waste dumping, sorting, and composting) are
classied as the high-risk group when exposure to biological agents at
work is considered [6]. There is data on the microbiological exposure of
workers who have direct contact with solid waste [79]. These studies
indicated that workers of this industry have an excess risk of work-
related health problems such as musculoskeletal problems, pulmonary
diseases, organic dust toxic syndrome symptoms (caught, chest-
tightness, dyspnoea, and inuenza-like symptoms), gastrointestinal
problems and irritation of the eyes, skin, and mucous membranes.
However, data on indoor bioaerosols and health risks to ofce workers
employed at municipal waste landlls is insufcient [5]. Therefore, the
goal of this study was to evaluate the inuence of a municipal waste
landll site on microbiological air quality both in indoor spaces located
at the landll area (weigh station, social room, sorting station) and
outside the buildings (at the operating landll cell and at the
technological square). The assessment was made on the basis of the
bacterial and fungal aerosol concentration levels and the isolated
bacterial and molds species.

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ska et al.
A. Kalwasin

2.2 Sampling sites

The air samples were collected once a month from May 2010 to
April 2012 in the three following indoor spaces on the premises of the
landll sites (Fig. 1):

(1) Sorting station: a sampling site located near pre-sort cabin and
sorting line.
(2) Weighing station: an ofce near the scale.
(3) Social room: a room where workers can rest and eat their lunch.

Figure 1. Outlook of the research sites.
2 Materials and methods
2.1 Description of the study site
The research was conducted on the premises of municipal solid waste
management plant (MSWMP) in Toru
n, Poland (Fig. 1). The MSWMP
opened at the end of 2009. Located in the north of Toru
n,
approximately 12 km from the town center, it is surrounded by at
sandy wasteland. The landll cell has an area of 6.6 ha and the
capacity of 1080 000 m3 (Fig. 1). In addition to the landll cell,
MSWMP comprises two leachate ponds, a leachate treatment plant,
composting facilities, technological grounds for composting, and a
sorting station. It borders the ash dump of the heat and power plant
(CHP, Toru
n) in the south-east, the reclaimed landll cell, industrial
areas and a railway line in the south, and the forest it the west and
north. Annually, an average sorting station processes 27 000 Mg of
waste raw materials and 57 000 Mg of mixed waste. The basic
technological system of the sorting station consists of a pre-sort
cabin, a double-deck rotating sieve (20 and 80 mm mesh) with
conveyor belts, two sorting lines, a press for sorted materials, and
separators for ferromagnetic materials.
Air samples were also collected at the operating landll cell and at
the technological square, a site located near the sorting and
composting facilities. Samples were collected during the morning
time (9 am) at both indoor and outdoor environments for one day per
month. Details of measurements are presented in Tab. 1. The
following air parameters were measured during sample
collection: air temperature, relative humidity, and wind velocity
(Tab. 2). These measurements were carried out using a Nielsen-
Kellerman anemometer, Kestrel 3500 (Toronto, USA).
2.3 Air sampling
Air samples were obtained according to Polish Standard [10] 1.3 m
above the ground/oor level. The samples were collected using a
microbial impactor (MAS-100, Merck, Darmstadt, Germany),
which corresponds to the fth degree in the Andersen sampler.
The air-ow rate was 100 L/min. Sampling time was chosen so as not
to overload the plates (30 s to 2 min). According to the Polish
Standard, the microbiological air testing included determining the
number of:
a. mesophilic bacteria cultured on PCA medium with addition of
0.1 g/L of actidione to inhibit the growth of molds and incubated
24 h at the temperature 37C [11];
b. molds cultured on Czapek-Dox medium and on Wort agar and
incubated seven days at the temperature 25C [12].
All analyses were performed in three replicates. All media were
purchased from Biocorp (Warsaw, Poland). The collected samples

Table 1. Details of measurements

Environment Research site Sampling time Occupant number Ventilation type, rate
Outdoor air Operating landfill cell 2 min 2
Technological square 2 min 3
Indoor air Social room 2 min 4 Natural ventilation
Weighing station 2 min 2 Natural ventilation
Sorting station 30 s 22 Mechanical (149 000 m3/h) and natural ventilation

Table 2. Meteorological parameters of indoor and outdoor air of the municipal waste dumping sites in Torun

Environment Meteorological parameter Range Mean SD

Outdoor air Temperature 8.324.5 8.6 10.4
Humidity 53.193.3 70.7 11.5
Air velocity 1.226.5 4.5 4.9
Indoor air Temperature 1.226.6 21.9 6.3
Humidity 38.584.4 47.9 10.7

SD, standard deviation.

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 Exposure of Workers of Municipal Landfill Site 1339

were transported to the laboratory and incubated at given temper-
atures. After the incubation, the grown colonies were counted and
the results were converted to the colony forming units in 1 m3 of air
(CFU/m3).
2.4 Identification of airborne bacteria and molds
In order to identify bacteria and molds, pure bacterial and fungal
cultures were isolated from the surfaces of nutrient agar/Czapek-Dox
plates, respectively. Each month, 100 randomly selected bacterial/
fungal colonies (selected from 30 plates) were inoculated into slants
containing the same nutrient. Bacterial morphology was determined
with Gram-staining procedure performed on the second and fth day
of bacterial cultures growing in nutrient broth. Bacterial strains were
identied with appropriate API tests (BioMrieux, Marcy-ltoile,
France). Gram-negative rods were identied with API 20 E test, cocci
with API Staph test and API 20 Strep test, and Gram-positive bacilli
with API 50 CH test. After the results had been recorded and numerical
prole obtained, the bacteria were identied with apiwebTM. Isolated
molds were identied according to their macro and micro character-
istics using selected taxonomic monographs [1316].
2.5 Statistical analysis
A statistical analysis of the results was performed using IBM SPSS
Statistics 21 software. Differences in the numbers of the investigated
bacterial groups in comparison to the different location of the
sampling sites and the month of the research were tested using
analysis of variance, followed by Tukeys HSD test. The differences
were considered statistically signicant when p < 0.05.
3 Results
The concentrations of mesophilic bacteria and molds in the outdoor
and indoor air at the municipal landll site in Toru

n are presented in
Tab. 3. Outside the highest average concentration of bacteria
(1361 CFU/m3) noted at the landll cell was more than twice the
average concentration of bacteria on the technological square. The
highest concentration of bacteria in the outdoor air exceeded
5000 CFU/m3. The highest concentration of mold fungi (6750 CFU/m3)
was recorded at the landll cell but the average concentration of
molds were higher at the sampling site located at the technological
square (1179 CFU/m3) than at the landll cell (897 CFU/m3). Two-way
analysis of variance shows that the concentration of microorganisms
(bacteria and molds) in the outdoor air depended on the season
(p < 0.05), but did not depend on the sampling site (Tab. 4).
Considerably higher values noted in summer than in autumn and
winter.
Indoors the highest concentration of bacteria in the air was
recorded in the sorting station (10 707 CFU/m3 on average;
20 000 CFU/m3 at most). The results of the Tukeys HSD test
indicate that this sampling site was distinguished from the
remaining by higher concentrations of mesophilic bacteria
(p < 0.001). The lowest concentrations of bacterial bioaerosol
were noted in the weigh station. Similarly, the highest concen-
trations of molds were noted in the sorting station (12 471 CFU/m3
on average; 21 200 CFU/m3 at most). The results of Tukeys HSD
test indicate that this sampling site was distinguished from
the weigh station and the social room by higher concentration of
molds (p < 0.01). The lowest concentration of molds was noted in
the social room. Two-way analysis of variance shows that the
concentrations of the investigated microbial groups in the indoor
air depended on the sampling site (p < 0.05) but did not depend
on the season (Tab. 4).
According to Polish Standard [11], a majority of the outdoor air
samples collected at the municipal landll site in Toru
n can be
classied as uncontaminated with mesophilic bacteria. 21.7% of all
air samples collected at the landll cell were classied as heavily
contaminated; no air samples collected on the technological square
were contaminated with mesophilic bacteria (Tab. 5). According

Table 3. Bacterial concentration in the indoor and outdoor air of the municipal landll sites

Bacteria (CFU/m3) Molds (CFU/m3)

Environment Mean Range SD Mean Range SD

Outdoor air Operating landfill cell 1361 105500 1864 897 406750 1410
Technological square 578 202420 716 1179 405620 1353
Indoor air Social room 742 1403680 836 534 403360 776
Weighing station 576 503590 733 569 303920 888
Sorting station 10 707 124020 000 9081 12 471 93021 200 8155

Table 4. Analysis of variance of bacterial and fungal concentrations of municipal landll sites according to the location of the research sites (1) and
season of the research (2)

Environment Microorganisms Factor F P-value

Outdoor air Bacteria Site (1) 4.001 0.052
Season (2) 2.936 0.044
Molds Site (1) 0.666 0.419
Season (2) 6.743 0.001
Indoor air Bacteria Site (1) 29.136 0.000
Season (2) 1.513 0.222
Molds Site (1) 5.656 0.006
Season (2) 0.604 0.615

F among: groups variance/within: groups variance, P signicance level.

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ska et al.
A. Kalwasin

Table 5. Outdoor air bacterial concentrations (in percent by sampling site)

Percent of samples by sampling site

Microorganisms Range of values (CFU/m3) Pollution degree Technological square Operating landfill cell
Bacteria <1000 Not polluted 78.3 69.6
10003000 Medium 21.7 8.7
>3000 Heavy 0.0 21.7
Molds 30005000 I 95.6 95.6
500010000 II 4.3 4.3
>10000 III 0.0 0.0

Pollution degree according to Polish standards [11, 12].

Table 6. Indoor air bacterial concentrations (in percent by sampling site)

Percent of samples by sampling site

3
Microorganism Permissible maximum concentration (CFU/m ) Social room Weighing station Sorting station
Bacteria <1  10 3
87.5 87.5 8.3
Molds <5  104 100 100 100

Pollution degree according to the standards in the air of working premises contaminated with organic dust according to Dutkiewicz and
Moocznik [17] and Grny and Dutkiewicz [18].

to Polish Standard [12], 95.6% of all outdoor air samples can be
classied as averagely contaminated (1st degree) with molds. No
contamination dangerous for the environment was detected at either
of the outdoor sampling sites throughout the entire research period
(Tab. 5).
According to the sanitary standards of the air of working premises
contaminated with organic dust proposed by Dutkiewicz and
Moocznik [17] and Grny and Dutkiewicz [18], the social room
and the weighing room met these criteria in 87.5% (Tab. 6). The
sorting station met these criteria only for fungal bioaresol, while
the concentrations of mesophilic bacteria usually exceeded the
permissible level.
Saprophytic bacilli of the Bacillus and streptococci of the
Staphylococcus constituted the most abundant group of bacteria in
the collected air samples (Tab. 7) Propagules of Penicillium spp.,
Cladosporium herbarum, Alternaria alternata, Aspergillus spp., and
Rhisopus sp. prevailed in the molds (Tab. 8). In the examined air,
we found bacterial (B. subtilis, P. aeruginosa) and molds species
(A. fumigatus, M. grisea, P. manfferei, S. apiospermium, C. neoformans)
qualied to the second group of risk according to the Regulation of
the Minister of Health from 22 April 2005 on biological factors in the
workplace and health care workers occupationally exposed to these
agents [6].
4 Discussion
Due to the origin of municipal waste, landll sites inuence all
components of the environment including the air. Availability of the
large amounts of organic matter in the waste is the source of
nutrition for microorganisms. Long-term holding of the unstable
waste biomass, inhabited by the microorganisms and the necessity of
pushing them, creates the bioaerosols with high microorganisms
concentration in air.
The concentrations of bacterial and fungal aerosol determined in
the present study (between 103 and 104 CFU/m3) fall within the range
normally observed in landll sites and correspond with results
obtained by other researchers [1922]. These levels were higher than

Table 7. Identication of airborne mesophilic bacteria isolated from all sampling sites at landll

Morphological forms of
total bacterial strains Genus Percentage (%) Dominant species
Gram-positive bacilli (60.5%) Bacillus 45.5 B. licheniformis, B. pumilus, B. cereus, B. lentus, B. subtilisa),
B. megaterium, B. firmus
Brevibacillus 7.8 B. laterosporus
Geobacillus 1.6 Geobacillus stearothermophilus
Others 5.6
Gram-positive cocci (37.7%) Staphylococcus 30.6 S. sciuri, S. cohnie, S. lentus, S. xylosus, S. lugdunensis,
S. hominis, S. capitis
Kocuria 2.9 K. varians, K. rosea
Micrococcus 1.3
Others 2.9
Gram-negative bacilli (rods) (1.8%) Pseudomonas 1.5 P. aeruginosaa)
Others 0.3
a)
Bacteria qualied to the second group of biological agents [6].

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 Exposure of Workers of Municipal Landfill Site 1341

Table 8. Identication of molds species isolated from all sampling sites such as low temperature, ground freezing, and snow cover. The
at landll relationships between microbial agents and the meteorological
parameters as temperature, humidity, wind direction were not tested
Percentage Predominant because the changeable trafc, disturbances and re-disturbances of
Fungal species (%) species
dust and human activity cause that the relationships are unclear
Penicillium spp. 38.9 P. verrucosum, P. notatum, (direct). According to Bowers et al. [28] and Mansour et al. [22] the last
P. marneffeia), P. lanosum, parameters are most important than meteorological factors.
P. chrysogenum,
P. melagrinum The results further indicate that the exposure of the workers
Cladosporium spp. 15.1 employed in conned spaces of the municipal landll site to bacterial
Alternaria spp. 12.8 and fungal bioaerosol poses a serious problem. It is worth
Aspergillus spp. 11.2 A. fumigatusa), A. flavus, emphasizing, that the contamination with bioaerosol in the indoor
A. niger, A. clavatus
environment was signicantly different and depended primarily on
Rhisopus spp. 5.6
Phoma spp. 2.3 how the room was used. Due to the more stable environmental
Madurella griseaa) 2.3 conditions, the level of bioaerosol contamination of indoor air did
Paecilomyces spp. 2.3 not vary signicantly between seasons.
Geotrichum candidum 2.3 Average concentration of mesophilic bacteria in the sorting station
Acremonium spp. 1.6
was seven times higher than at the landll cell. The results obtained
Aureobasidium spp 1.6
Arthrographis sp. 1.6 by Kiviranta et al. [29] conrm that people working in sorting stations
Scedosporium apiospermuma) 1.6 are more exposed to harmful bioareosol than people working at
Cryptococcus neoformansa) 0.8 landll sites or people collecting waste. The researchers further
a) accentuate that the exposure to volatile organic compounds of
Molds qualied to the second group of biological agents [6].
workers who sort waste was three times higher than the exposure of
employees who work at the landll site, and reached the highest level
in the vicinity of that object. Donderski et al. [23] reported that during considered the limit of discomfort. As stated by Huttunen et al. [30],
similar studies conducted in Rubinkowo, the residential district of the concentration of microorganisms in the air is strongly related to
Toru
n, situated 2.5 km from municipal landll site, the concen- the immunotoxicity of aerosols. To reduce the health risks associated
trations of bacterial and fungal aerosols were frequently lower and with bioaerosol present in the sorting station, workers are obliged to
ranged between 79 and 102 CFU/m3, and between 49 and 140 CFU/m3, use engineering controls (ventilating rooms, enclosing the process),
respectively. At the same time, the concentrations of bacterial and administrative controls (changing clothes, washing hands, and
fungal aerosols in the Old Town in Toru
n (12 km from the municipal rotating tasks), and personal protective equipment [29, 31].
landll site) were 111189 and 53120 CFU/m3. Relatively low level of The concentration of bacterial bioaerosol in ofces is usually lower
bacterial contamination of air was also determined in spa town of than in homes [32, 33]. However, as mentioned by Lis et al. [5] people
Ciechocinek (10 555 inhabitants, located 20 km south-east of the city working in ofces located within a landll site are also exposed to
of Torun
) by Burkowska et al. [24]. The concentrations of mesophilic health hazards, especially when the ofces are located in vicinity of
bacteria in Ciechocinek air ranged from 23 CFU/m3 in February, in the weighing stations or the routes of waste collection vehicles. The
graduation tower area, to 566 CFU/m3 in June, in urbanized areas. concentration of bioaerosol in the social room and in the ofce on the
According to Maecka-Adamowicz [25], the concentration of hetero- premises of MSWMP in Toru
n never exceeded the maximum
trophic bacteria in the forest recreation park in My
slcinek located permissible level of bacterial and fungal aerosol for homes and
ca. 40 km from Toru
n was on average 341.0 CFU/m3 and the ofces, which is 5.0  103 CFU/m3 [18, 34].
concentration of molds was 2134 CFU/m3. Requirements concerning indoor air quality are not fully dened
According to Polish Standards [11, 12], the concentrations of in the legislation of Poland and the European Union. The assessments
bacterial and fungal aerosol determined in the present study do not of indoor air quality of non-industrial workplaces, private houses,
generally pose threat for humans or the environment. Occasionally, and public buildings (excluding hospitals) are based on the
the air at the landll cell was classied as heavily contaminated with classication of indoor spaces contained in the report of the
mesophilic bacteria as a consequence of earthworks including Commission of European Communities [35]. Dutkiewicz and
spreading and compacting the waste or building embankments Moocznik [17] followed by Grny and Dutkiewicz [18] established
around the landll. Subsequently, large amounts of dust introduced permissible maximum concentration of mesophilic bacteria
into the air at the time of sampling affected the results. According to (1.0  103 CFU/m3) and molds (5.0  104 CFU/m3) in the air of working
Barabasz et al. [26], and Nielsen et al. [27], all factors increasing the premises contaminated with organic dust. The social room and the
dust pollution in the municipal waste landll sites, as: transport and weighing room in most cases met these criteria. The sorting station
unloading the waste, leveling with the mechanical equipment, met these criteria only for fungal bioaresol, while the concentrations
compacting the waste layers and their covering favor the increase of of mesophilic bacteria usually exceed the permissible level. The
the microorganisms concentration in the air. ndings of epidemiological research indicate that exposure to high
The results of the present study indicate that the concentrations of concentrations of microbes in the air frequently leads to allergies,
bacteria and molds in the air on the premises of MSWMP differed asthma, hay fever [36], pneumonia [37], and many other health side-
signicantly depending on the season, with considerably higher effects, including infections [38]. Biological factors such as fungal
values noted in summer than in autumn and winter; the pattern is spores and mites are involved in sick building syndrome, a complex
also described by other authors [5, 7]. This seasonal decrease may situation in which occupants experience a variety of symptoms and
result from conditions considered highly unfavorable for cell become generally unwell, recovering only when they cease to
division, the formation of dust, and the spread of microorganisms frequent the building [39, 40].

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1342
ska et al.
A. Kalwasin
The results of the present study indicate that the indoor and
outdoor air on the premises of the municipal landll site in Toru
n Handling of Source Separated Household Waste, Ann. Agric. Environ.
contained bacterial species (B. subtilis, P. aeruginosa) and molds species
(A. fumigatus, M. grisea, P. manfferei, S. apiospermium, C. neoformans)
classied into the second group of risk according to the Regulation of
the Minister of Health from April 22, 2005 on biological factors in the
workplace and healthcare workers occupationally exposed to these
agents [6]. The group includes biological agents, which can cause
diseases in humans and therefore may be dangerous for workers, but
which do not show a tendency to spread in human population and
which can be effectively prevented or treated.
The results of microbiological tests indicate that the air in
municipal facilities contains natural saprophytic microora (ubiqui-
tous organisms) as well as pathogenic species that threaten human
health including P. aeruginosa, S. aureus, Rhisopus microsporus, A. niger,
A. avus, and many others [41, 42]. All the above species produce
harmful secondary metabolites and cause allergic and fungal
diseases [4244]. However, qualitative studies of bacteria present in
the air at the municipal landll site in Toru
n indicate that Gram-
negative bacteria, the source of endotoxins (lipopolysaccharides) as a
component of their cell walls constituted only a small percentage
(1.8%) of all isolated bacterial strains. The effects of bacterial
endotoxins on the human body have been discussed in numerous
publications [4547]. Endotoxins inhaled with polluted air may lead
to toxic pneumonitis and nally to adult respiratory distress
syndrome [45].
Examining the results of the morphological research on bacteria in
the air of municipal landll sites in Toru
n, the predominance of the
Gram-positive forms should be emphasized as they constituted over
95% of the studied microorganisms. Considering the fact, it should
be remembered that only mesophilic bacteria were studied, as
recommended by Polish Norm [11]. Taking into account psychrophil-
ic forms, which include the majority of autochthonic bacteria living
in natural environment, could have an effect on percentage of
individual morphological forms in the studied samples. Rahkonen [7]
and Lis et al. [5] obtained different results much higher numbers of
Gram-negative bacteria ranging from 17 to 33%.
5 Concluding remarks
Our study conrmed that municipal waste is a serious source of
airborne bacteria and molds that could deteriorate the microbiolog-
ical air quality in work environment of the municipal landll site.
The present results show that the exposure of workers to micro-
organisms may be very high in sorting station. These data are
necessary for occupational health care personnel who organize
health surveillance and instruct workers on the potential health
effects of their work.
The authors have declared no conict of interest.
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