ENVIRONMENTAL ENGINEERING SCIENCE ORIGINAL ARTICLES

Volume 32, Number 4, 2015

ª Mary Ann Liebert, Inc.
DOI: 10.1089/ees.2014.0050

Assessment of Airborne Bacteria and Fungi

in Various University Indoor Environments:
A Case Study in Chang’an University, China
Yanpeng Li,1,2,* Wei Wang,1 Xiao Guo,1 Tinglu Wang,1 Honglei Fu,1 Yue Zhao,1 and Wenke Wang1,2
1
Key Laboratory of Subsurface Hydrology and Ecology in Arid Areas of Ministry of Education, Chang’an University, Xi’an, P.R. China.
2
School of Environmental Science and Engineering, Chang’an University, Xi’an, P.R. China.

Received: January 25, 2014 Accepted in revised form: December 16, 2014

Abstract
To quantify characteristics of bioaerosols in university indoor environments, concentration and size distribution
of airborne culturable bacteria and fungi were examined in four types of buildings of Chang’an University in
Xi’an, China, from March, 2012 to February, 2013. Indoor temperature and relative humidity (RH) were also
measured to determine correlations between bioaerosols and environmental parameters. Results showed that
concentration and size distribution of airborne bacteria and fungi varied in various indoor environments due to
the appearance of different indoor sources and human occupancy. The highest mean concentrations of airborne
bacteria and fungi were found in the canteen (1,025 – 91 and 699 – 57 CFU/m3), followed by the clinic and
dormitories, and the lowest in classrooms (479 – 66 and 345 – 15 CFU/m3). Airborne bacteria and fungi here
showed higher concentrations than those of western universities. Similar seasonal variations of airborne fungal
concentrations were observed for all indoor environments, with higher levels in fall and winter and lower in
spring and summer. Indoor temperature showed more significant correlation with bioaerosols than RH in all
indoor environments. Another important finding was that more than 75% bacterial and fungal aerosols were in
respirable size range in each indoor environment.

Key words: bioaerosols; concentration; indoor environments; size distribution; university

Introduction direct contact with the contaminated materials or by inhala-

tion of bioaerosols. There is a growing evidence that expo-
W ith the acceleration of urbanization recently in
China, more and more contemporary people spend
nearly 80–90% of their daily time in indoor environments.
sure to bioaerosols in indoor environments can induce diverse
adverse health effects, such as infectious diseases, acute toxic
effects, allergies, and cancer (Ross et al., 2000; Douwes
Indoor air quality has been recognized to influence the health
et al., 2003; Bolashikov and Melikov, 2009; Goldman and
and safety of occupants directly. Among research on indoor
Huffnagle, 2009; Chatzidiakou et al., 2012).
air quality, the issue of indoor bioaerosol contamination has
Numerous studies have been conducted to assess personal
attracted more and more attention, especially since the out-
exposure to airborne bacteria and fungi in various indoor en-
break of severe acute respiratory syndrome (SARS) and the
vironments: apartments and houses ( Jones and Harrison, 2004;
emergence of Avian Influenza (H7N9). Bioaerosols, defined
Lee and Jo, 2006; Lee et al., 2006; LeBouf et al., 2008; Nasir
as airborne particles consisting of living organisms (e.g.,
and Colbeck, 2010, 2012; Frankel et al., 2012), public build-
bacteria, fungi, and viruses) or originating from nonliving
ings (Pastuszka et al., 2000; Kim and Kim, 2007; Dutil et al.,
organisms such as toxins, by-products of microbial metabo-
2009; Zuraimi et al., 2009; Karbowska-Berent et al., 2011; Lal
lism, or fragments of dead microorganism (ACGIH, 1999),
et al., 2013; Li et al., 2013), public transport vehicles (Lee and
can spread through air and cause a potential health risk for
Jo, 2005; Wang et al., 2010b), agricultural setting (Rosas et al.,
people staying in indoor environments as a consequence of
2001; Kim et al., 2009; Martin et al., 2010), and food pro-
cessing settings (Zorman and Jersek, 2008; Rajasekar and
Balasubramanian, 2011). These investigations have indi-
*Corresponding author: Key Laboratory of Subsurface Hydrology cated that there are wide variations in the concentration and
and Ecology in Arid Areas of Ministry of Education, Chang’an
University, 126 Yanta Road, Yanta District, Xi’an 710054, P.R. size distribution of bioaerosols in different microenviron-
China. Phone: + 86 029 82339991; Fax: + 86 029 85585485; ments, depending on such biotic and abiotic factors as the
E-mail: liyanp01@chd.edu.cn type of microorganism species, relative humidity (RH) and

273
274
temperature, outdoor concentrations, air exchange rates, and
human activities.
Most of the above studies on bioaerosols in public build-
ings have been carried out in offices, hospitals, libraries, and
schools. Relatively limited studies have been conducted in
university indoor environments, especially in Chinese uni-
versities. Moreover, the existing studies on university indoor
environments mainly focused on a single type of university
building such as classrooms (Grisoli et al., 2012; Qian et al.,
2012), research laboratories (Giulio et al., 2010), and ar-
chives (Karbowska-Berent et al., 2011; Nunes et al., 2013),
there is very little information on bioaerosol concentrations
in different types of university indoor environments, how
they compare across these environments, and their dominant
sources (Stryjakowska-Sekulska et al., 2007; Chan et al.,
2008; Lal et al., 2013).
It is well known that the campus setting of Chinese uni-
versities is generally different from that of western univer-
sities. For example, Chinese universities have many public
canteens, student dormitories, and public clinics in which
there are no ventilation and air-conditioning (HVAC) sys-
tems. In addition, Chinese universities have a higher popu-
lation density than western universities regardless of whether
it is academic year or vacation. Generally, room conditions
and human occupancy have been reported to considerably
contribute to the varying concentrations of bioaerosols (Kim
and Kim, 2007; Nasir and Colbeck, 2010; Chatzidiakou et al.,
2012; Frankel et al., 2012; Qian et al., 2012). Therefore, the
potential to come into contact with bioaerosols and then be
infected in Chinese universities might be higher than western
universities.
To effectively control the adverse health effects in
indoor environments, the Ministry of Health (MOH),
Ministry of Environmental Protection (MEP), and General
Administration of Quality Supervision, Inspection and
Quarantine (AQSIQ) of China announced an Indoor Air
Quality Standard (2002). According to the standard, Chi-
nese residential buildings and office buildings are regu-
lated in regard of threshold limit value of 2,500 CFU/m3
for total airborne microorganism. The American Industrial
Hygiene Association (AIHA) published a proposition of
FIG. 1. Sampling sites in
university indoor environ-
ments of Xi’an, China.
LI ET AL.
guidelines for the amount of fungal spores in different
indoor environments (e.g., residential and commercial build-
ings) in 2001. Guidelines for residential buildings are less
than 500 CFU/m3 and for commercial buildings are less
than 250 CFU/m3 (Wonder Makers Environmental, Inc.,
2001). Other countries’ requirements are similar (Stryja-
kowska-Sekulska et al., 2007). Therefore, knowledge of the
concentration of bioaerosols in various indoor environments
including university indoor environments is significantly
critical to evaluate whether the current Chinese standard is
pertinent.
In addition, the effects of indoor bioaerosols on occupa-
tional and environmental health depend not only on their
concentrations and species, but also on their size distribu-
tions. Bioaerosols with different aerodynamic diameters are
recognized to be deposited in different positions of the
respiratory system. According to Chatigny et al. (1989),
particles with the diameter less than 4.7 lm, the so-called
respirable particles, can penetrate into the human alveoli and
lead to allergic alveolitis and other serious illnesses. In
contrast to intensive studies on size distribution of bioaer-
osols in other indoor environments, very few studies on size
distribution of airborne bacteria and fungi in the university
indoor environments have been reported in the literature
(Qian et al., 2012). To understand the human exposure to
airborne microorganisms, information on the size distribu-
tion of bioaerosols is also indispensable in various indoor
environments.
The present study aims to find out the typical concentration
levels and size distributions of culturable bacterial and fungal
aerosols in four types of typical university indoor environ-
ments in Xi’an, China. The seasonal distribution of bioaer-
osols is also discussed. The indoor temperature and RH were
measured to determine correlation degree between bioaer-
osols and environmental parameters.
Materials and Methods
Sampling sites
Field sampling of indoor bioaerosols was carried out in
a university campus, located at the southern part of Xi’an city
ASSESSMENT OF AIRBORNE BACTERIA AND FUNGI 275

(N 34260 and E 108940 ), China. As the largest city in north-

No.a
1

2
western China, Xi’an occupies an area of about 9,983 km2,
with a population of 8.468 million and a total number of ve-

11:00 am–1:00 pm

11:00 am–1:00 pm

11:00 am–1:00 pm

11:00 am–1:00 pm
hicles more than 1.60 million. As a typical semi-arid inland
city, Xi’an is located in the middle of the Yellow River valley

Time
and in the center of the Guanzhong Plain, surrounded by the

Measurement
Loess Plateau and Qinling Mountain. Moreover, Xi’an has
four distinct seasons with long summer and winter and short
spring and autumn. Summer is usually from May to the end
of August, and then autumn starts until the end of October.
November, December, January, and February are usually the

Characteristics of Four Types of University Indoor Environments in the Present Study

Hall (first floor)

Hall (first floor)

Rooms (second
winter season, and March and April are the spring season.

Rooms (third
Location
This university campus is *5 km away from the city
center, surrounded by residential dwellings, public buildings,

floor)

floor)
and several asphalt roads, as shown in Fig. 1. There are also
no industries surrounding this campus and there is little ve-
hicle traffic in the campus. In the university campus, four
different types of indoor environments were chosen as fol-

Ventilation

Natural

Natural

Natural

Natural
lowing: a canteen, a clinic, two dormitories, and two class-

type
rooms (also shown in Fig. 1). The details of these indoor
environments are presented in Table 1. All indoor rooms are
within 100 m of each other and thus, ambient conditions are
expected to be similar. To reduce the influence of human

no

no

no

no
Moldy condition
occupancy as much as possible, the population density of

No visible mold,

No visible mold,

No visible mold,

No visible mold,
smell of mold

smell of mold

smell of mold

smell of mold
each selected site was ensured to be relatively stable during
the sampling period. Moreover, the Cultural Square sur-
rounded by the above rooms was selected as an outdoor
sampling site during this research period to determine the
average ambient conditions.

Measurement and analysis

Concrete walls, glass windows,

Concrete walls, glass windows,

and doors, ceramic tile floor

and doors, ceramic tile floor

Concrete walls, glass windows

Concrete walls, glass windows

wooden doors, cement floor

wooden doors, cement floor

An Andersen six-stage cascade impactor (Westech) with
Construction material

six glass petri dishes of 93 mm in diameter was employed to

collect bioaerosol samples with different size ranges. The
range of aerodynamic diameter at each stage is as follows:
‡ 7.0 lm (stage 1), 7.0–4.7 lm (stage 2), 4.7–3.3 lm (stage
3), 3.3–2.1 lm (stage 4), 2.1–1.1 lm (stage 5), and 1.1–
0.65 lm (stage 6). According to Chatigny et al.’s (1989)
definition, the respirable fraction of particles corresponds to
the size range between stages 3–6. The number of each type of indoor environments investigated.
Bioaerosols sampling and monitoring of RH and temper-
ature (T) were conducted at four indoor sites in four different
Size (m2) of persons (year)

seasons from March 2012 to February 2013. The RH and

Age

10

20

20

10

T were recorded using a hygrothermograph (TES1364,

Taishi, Chinese Taiwan). At each site, sampling was per-
formed at the height of about 1.5 m above the floor surface
Number

50–100

(i.e., in the breathing zone of a normal person) in several

10–20

20–30

4–6
Table 1.

consecutive sunny days each season and during the same

period between 11:00 am and 1:00 pm throughout the year.
Samples were collected for about 10 min by sucking the air at
the rate of 28.3 L/min with three repetitions each time.
40–50

15–20
200

30

Therefore, a total of 24 samples (144 plates) were collected

including 12 samples (72 plates) for bacteria and 12 samples
(72 plates) for fungi at each site in this study. For comparison
Student dormitory

with the outdoor concentration, measurement was also taken

College canteen

simultaneously at the selected outdoor site.

College clinic

Before each sampling, the sampler was disinfected with

Classroom

75% ethanol. After the alcohol was volatilized sufficiently

(about 3–5 min), the agar plates were loaded to the sampler
according to collection stage inside of a Class II biosafety
Site

cabinet (BSC-1500; Biobase) and then the sampler was

276
carried in a dust-free box to the sampling sites. According to
Fang et al. (2008), nutrient agar (3 g beef extract, 10 g pep-
tone, 5 g sodium chloride, 15 g agar, and 1,000 mL distilled
water, pH = 7.2) and Sabouraud dextrose agar (40 g glu-
cose, 10 g peptone, 20 g agar, and 1,000 mL distilled water,
pH = 7.2) were used as bacterial and fungal culture medium,
respectively in the present study. After sampling, the agar
plates were immediately transported to the laboratory for
incubation. Bacteria were incubated at 37C for 48 h and
fungi were incubated at 25C for 72 h (Taiwan EPA, 2009a,
2009b).
After incubation, the colonies were counted followed by
the positive-hole correction method to correct for colony
overlapping. Each concentration of bioaerosols, generally
expressed as total colony-forming units (CFU/m3) for re-
spective particle size, was then calculated by dividing the
number of colonies formed on the culture medium at each
stage by the sampling air volume.
Statistical analysis of the observed data was conducted
using regression analysis. The standard deviations associated
with the annual or seasonal mean values at each sampling site
are shown in the respective figures in the form of error bars. In
addition, number median diameter (NMD) and geometric
standard deviation (GSD) were used to describe the size
distribution for each indoor site. The differences between
bioaerosol concentrations at different sites were also tested
by a student’s t-test, in which p-value of < 0.05 was consid-
ered to be statistically significant. Pearson’s correlation
analysis was performed to evaluate the statistical signifi-
cances of correlation between various environmental fac-
tors and each concentration of airborne culturable bacteria
and fungi.
Results and Discussion
Concentrations of airborne culturable bacteria
and fungi
The annual mean concentrations of airborne culturable
bacteria and fungi in all four indoor environments examined
are shown in Table 2. It can be clearly seen that the airborne
bacterial concentrations vary in different indoor environ-
ments, ranging from 186 to 1,593 CFU/m3. The highest mean
concentration of bacteria occurs in canteen (1,025 – 91 CFU/
m3), followed by clinic (689 – 26 CFU/m3) and dormito-
ries (614 – 34 CFU/m3), and the lowest is found in class-
rooms (479 – 66 CFU/m3). Fungal concentration ranges from
130 to 940 CFU/m3. The maximum concentration is also
detected in canteen (699 – 57 CFU/m3) followed by clinic
Table 2. Annual Mean Concentrations of Airborne Bacteria and Fungi
in Various Indoor Environments of Chang’an University
Bacteria (CFU/m3)
Site Mean – SD Range
College canteen 1,025 – 91a 652–1,593
Classrooms 479 – 66b 186–777
College clinic 689 – 26c 469–878
Student dormitories 614 – 34d,c 414–1,031
a,b,c,d
Mean values within the column by the same letter are not significantly different ( p < 0.05).
*The differences between airborne fungi and bacteria are compared by t-test.
LI ET AL.
(584 – 43 CFU/m3) and dormitories (421 – 52 CFU/m3), while
the lowest is also found in classrooms (345 – 15 CFU/m3).
Statistically, airborne culturable bacterial and fungal
concentrations detected in canteens are significantly higher
than those at other three indoor sites ( p < 0.05). In the clinic,
the concentration of total culturable fungi is also significantly
higher than that in classrooms and dormitories ( p < 0.05)
and the concentration of total culturable bacteria is higher
significantly than that in classrooms ( p < 0.05). However, no
significant difference is found between dormitories and the
clinic ( p > 0.05).
According to Nasir and Colbeck (2012), bioaerosols in
indoor environments can be of both outdoor and indoor ori-
gin. Outdoor bioaerosols can migrate into indoor environ-
ments through a range of avenues such as doors, windows,
and human movement. As the indoor sites in this study are
within 100 m of each other, ambient conditions are expected
to be similar and thus, it is reasonable that outdoor origin is
approximately considered as the same for all indoor sites.
Therefore, the variations in the concentration in various in-
door environments may be attributed mainly to different
amounts of aerosolized bioaerosols from various indoor
sources. During the sampling, remains of meals, medical
wastes, and dirty socks and clothing may be found in the
canteen, clinic, and dormitories, respectively, which is
common in Chinese public places and is also a reflection of
daily lifestyles of Chinese people. This phenomenon is un-
deniably connected with an appearance of a new indoor
source of bioaerosols, leading to the accumulation of mi-
croorganisms and the increase of bioaerosol concentrations.
Another reason why the higher concentrations show in the
canteen and clinic may be owing to higher occupant density
and more human activities than in classrooms. As seen in
Table 1, there were more persons in the canteen (50–100
persons) and clinic (20–30 persons) than in classrooms (10–
20 persons) and dormitories (4–6 persons) when the sampling
was carried out. As suggested by Qian et al. (2012), both
resuspended dust deposited on the floor due to human
activities and direct shedding from human occupants are
important contributors to indoor bioaerosol populations.
Furthermore, patient oral and respiratory fluid emitted via
coughing, sneezing, talking, and breathing may be another
significant source of bioaerosols (Hospodsky et al., 2012).
This is why there are more elevated bioaerosols in clinic than
in classrooms despite similar number of persons in both sites.
The ratio of indoor-to-outdoor airborne bacteria and fungi
(I/O ratio) is generally used to check if indoor spaces are
contaminated with them. If this ratio is larger than 1, it might
Fungi (CFU/m3)
Mean – SD Range p-Value*
699 – 57a 435–940 0.0297
345 – 15b 130–523 0.0392
584 – 43c 372–790 0.0064
421 – 52b,d 263–727 0.0304
ASSESSMENT OF AIRBORNE BACTERIA AND FUNGI 277

Stryjakowska-Sekulska

Grisoli et al. (2012)

Nunes et al. (2013)

Karbowska-Berent

Lal et al. (2013)

Reference

et al. (2007)

et al. (2011)
Current study
Comparison of Bioaerosols Concentrations in Different University Indoor Environments Worldwide

215 in library, 455 in reading room,

20.50 for simple ventilation, 41.5

2,000 in monsoon seasons, 9,733

clinic, 421 – 52 in dormitories,

180 in canteen, 410 in toilets

699 – 57 in canteen, 584 – 43 in

in postmonsoon seasons
345 – 15 in classrooms

for air-conditioning
Fungi
Mean microbial concentration (CFU/m3)
FIG. 2. Indoor and outdoor ratio of levels of airborne
bacteria and fungi in the university indoor environments of
Chang’an University.

483 – 18.4
be suspected that the indoor air has been contaminated with

6–1
airborne microorganisms (Lee et al., 2006; Kim and Kim,
2007; Karbowska-Berent et al., 2011). The present results,
shown in Fig. 2, indicate that the I/O ratios for both bacteria

room, 1,080 in canteen, 2,350 in

75.50 for simple ventilation, 75.50

2,083 in monsoon seasons, 12,933

1,025 – 91 in canteen, 689 – 26 in
and fungi are higher than 1 in most investigated buildings

clinic, 614 – 34 in dormitories,

310 in library, 1,285 in reading

except for classrooms. As discussed earlier, this can be ex-
plained by the fact that there are commonly remains of meals,

in postmonsoon seasons
479 – 66 in classrooms
medical wastes, and dirty clothing carelessly discarded in
these places, which provide favorable conditions for bacterial
Bacteria

for air-conditioning
and fungal growth and proliferation, resulting in I/O ratios
larger than 1.
Similar results were also reported by Nasir and Colbeck

1,035 – 54.4
(2012), who pointed out that this phenomenon was undeni-
ably a reflection of new significant microbiological source. toilets

107 – 12
However, the present values for both bacteria and fungi are
inconsistent with some other studies (Lee et al., 2006; Kim
and Kim, 2007; Karbowska-Berent et al., 2011). Kim and
Kim (2007) reported that the I/O ratios for airborne bacteria
During summer season in

and fungi were 0.58 and 0.56 in hospitals, 0.71 and 0.72 in
Once a month during 1

childcare centers, 0.28 and 0.33 in elderly welfare facilities,

Mar. 2012–Feb. 2013
Sampling period

Sep. 2010–Jan. 2011

and 0.63 and 0.66 in maternity recuperation centers, respec-

tively. Lee et al. (2006) and Karbowska-Berent et al. (2011)
Sep.–Oct. 2003

also found that the I/O ratios for airborne fungi were lower
than 1 regardless of the type of investigated public buildings.
Jul. 2010

Differences in the environmental conditions and indoor

2010

year

sources should be a likely reason for these inconsistencies.

Average bioaerosol exposures in this study inside different
university indoor environments do not exceed the threshold
limit value, 2,500 CFU/m3 announced by the MOH, MEP, and
Nehru University, Delhi, India
Storage rooms in the University
Nicolaus Copernicus University

AQSIQ of China (2002). However, it is valuable to compare

Chang’an University, Xi’an,
Table 3.

Library canteen in Jawaharlal

the present data with some guideline values proposed by

University rooms in Poznań,

University classrooms, Italy

Library in Toruń, Poland

various organizations all over the world. The AIHA has

suggested that the guideline values for fungal spores should be
Indoor environments in

less than 500 CFU/m3 in residential buildings and less than

archive, Portugal

250 CFU/m3 in commercial buildings (Wonder Makers En-

vironmental, Inc., 2001), respectively. In Swedish, the num-
ber of 500 CFU/m3 of bacteria and 300 CFU/m3 of fungal
spores can be accepted in an indoor environment (Abel et al.,
Poland
Location

China

2002). According to current Singaporean requirements, total

amount of airborne bacteria in indoor environments should
not exceed 500 CFU/m3 (Obbard and Fang, 2003). It is
278
evident that most of the bioaerosol concentrations detected in
this study are above these reference values. Such comparison
partly reflects the differences in geographic region of different
countries and localized characteristics of bioaerosols. On the
other hand, it is also a reflection of substantially strong air
pollution in China due to recent rapid economic growth in the
past decades, and the regulation of indoor air quality in China
still need further optimization.
Furthermore, it is worthwhile to carry out comparisons of
bioaerosol concentrations in different university indoor en-
vironments worldwide. Table 3 presents the comparison in
different university indoor environments worldwide. It can
be seen that the airborne bacteria and fungi detected in this
study show higher concentrations in comparison to previous
indoor studies in western universities (Karbowska-Berent
et al., 2011; Grisoli et al., 2012; Nunes et al., 2013). These
discrepancies should be due to differences in the occupant
density and lifestyle, ventilation behavior, and room condi-
tions between Chinese and western universities. The quantity
of indoor furnishings, general household cleaning practices,
and ventilation behavior will greatly affect the amount of
aerosolized bioaerosols from already deposited particles on
indoor surfaces and ingress of outdoor bioaerosols ( Jones and
Harrison, 2004). Another important reason may be attributed
to dissimilar meteorological and environmental conditions in
different cities. It should be noted that the referred investi-
gations were performed in the geographic regions different
from the present semi-arid region. Moreover, compared to
other cities examined in the world, the microbial concentra-
tion in the atmosphere was higher in Xi’an (Li et al., 2012).
Seasonal variation of airborne culturable bacterial
and fungal concentrations
Figure 3 shows the seasonal variation of airborne cultur-
able bacterial and fungal concentrations at all sampling sites.
In all four indoor sites, there are similar distinct seasonal
variations in the fungal concentrations. The highest fungal
concentrations occur in autumn, and relatively higher con-
centrations are detected in winter than in spring and summer,
although the seasonal difference between autumn and winter
FIG. 3. Seasonal variation of airborne (a) bacterial and (b) fungal concentrations in different sampling sites of Chang’an
University.
LI ET AL.
is not statistically significant ( p > 0.05). Similar seasonal
variations for fungal concentrations have also been reported
by Huang et al. (2002) and Lee et al. (2006). Huang et al.
(2002) investigated a seasonal distribution of airborne fungi
in municipal landfill sites, in which the total culturable mi-
crobial concentrations peaked in winter in closed or under-
going-closure landfill areas. Lee et al. (2006) studied the
culturability of airborne fungi collected in indoor and outdoor
environments in six Cincinnati area single-family homes.
Their results indicated that the highest indoor concentration
of fungi was observed in the fall. However, this kind of
seasonal variation was contrary to other studies where the
highest concentrations of bioaerosols occurred in summer
(Pastuszka et al., 2000; Tsai and Macher, 2005; Lee and
Jo, 2006; Wang et al., 2010a). This is more likely due to the
weather condition and various indoor microenvironments,
such as activities and life style of occupants, ventilation be-
havior, and ingress of particles from outdoor, furnishings.
The effect of weather conditions (temperature and RH) will
be discussed below. In addition, these factors fluctuate to a
great degree between various housing types, their condition
and geographic location.
A different seasonal variability of airborne fungi from
indoor sites can be also observed in the present outdoor site.
The concentration of airborne fungi reaches its highest level
in spring, and its lowest level in summer. This difference
in seasonal trend of airborne fungal concentration between
indoor and outdoor environments reflects the role of the
different sources and different influence factors for airborne
fungi indoor and outdoor. Normally, plants and vegetables
are regarded as the main sources of fungal air contamination
in outdoor environments (Awad, 2005; Fang et al., 2008). In
Xi’an, warm temperatures throughout the spring promote
plants growth quickly and vigorously, which can provide
favorable conditions for fungal proliferation, thereby greatly
contributing to the concentration of fungal spores. During
the present sampling period of summer, higher temperature
and stronger UV radiation in outdoor environment generally
result in decreased airborne fungal spore concentration.
The seasonal variation trend of airborne bacteria appar-
ently varies in four different indoor sites. For example, the
ASSESSMENT OF AIRBORNE BACTERIA AND FUNGI
FIG. 4. Temperature and relative humidity at the four indoor sites and one outdoor site during four seasons.
averaged bacterial concentrations are significantly higher in
summer and winter than in spring and autumn in canteen
( p < 0.05), while the lower average levels of airborne bacteria
are notably found in summer than any other seasons in
classrooms ( p < 0.05). Such seasonal variation for bacterial
concentrations seems to mainly depend on the various sam-
pling sites. Further research need to be performed in this area.
Correlations between airborne culturable bacteria
and fungi and environmental parameters
The temperature and RH at the four indoor sites and one
outdoor site during four seasons are shown in Fig. 4. It can be
seen that the difference of the temperature between any two of
different indoor sites is not significant ( p > 0.05) except for
that between clinic and each of other sites, especially during
summer, autumn, and winter. For example, during autumn in
the canteen, classrooms, and dormitories, the mean tempera-
tures are 15.5C, 14.4C, and 15.7C with a range of 12.7–
18.6C, 12.6–16.2C, and 13.5–19.8C, respectively, while in
the clinic the mean temperature is 8.5C with a range of 6.6–
11.7C. In addition, the difference of the RH between any two
different indoor sites is not significant ( p > 0.05) except for
that between clinic and each of other sites. For example,
during winter in the canteen, classrooms, and dormitories, the
mean temperatures are 32.8%, 32.1%, and 34.7% with a range
of 30.5–35.3%, 29.8–35.7%, and 31.8–36.3%, respectively,
while in the clinic the mean temperature is 39.5% with a range
of 38.3–43.0%. The humidity and temperature in four indoor
Table 4. Pearson Correlation Analysis
for Airborne Fungal Concentration (CFU/m3)
and Temperature (C) and Humidity (%)
in the University Indoor Environments
Correlation College College Student
coefficient (R) canteen Classrooms clinic dormitories
Temperature - 0.579a - 0.744b - 0.842b - 0.891b
Humidity 0.621a 0.234 0.396 0.666a
a a
Correlation is significant at the 0.05 level (two-tailed).
b b
Correlation is significant at the 0.01 level (two-tailed).
279
environments are found to show relatively smaller change
compared with those in outdoor environment in this study. It
is worth noting that the sampling sessions were performed
during consecutive sunny days of each season and during the
same time between 11:00 am and 1:00 pm. Therefore, it is not
surprising that the variations of outdoor temperature and hu-
midity in each season are not huge.
Table 4 shows the correlation between concentrations of
airborne fungi and temperature and RH in four indoor sites. It
can be seen that the RH is statistically and positively corre-
lated with airborne fungal concentration only in canteen and
dormitories ( p < 0.05). Similar results are also reported by
Kim et al. (2009) and Nasir and Colbeck (2010). According
to them, the RH of the air has a major role in growth and
survival of airborne fungi. Therefore, higher RH could pro-
mote the higher airborne fungal number.
In contrast, there is a negative correlation between airborne
fungal concentrations and temperature in all the housing
types. All of these correlation values are statistically signif-
icant ( p < 0.05). This observation does not agree with the
general results reported in the literature, in which the con-
centrations of airborne fungi are high in a relatively warm
condition and low in a cool condition. However, the present
result is consistent with that obtained by Nasir and Colbeck
(2010). The possible reason still appears to attribute to the
specific microenvironments as discussed above.
Table 5 indicates the correlation between concentrations
of airborne bacteria and temperature and humidity in four
Table 5. Pearson Correlation Analysis
for Airborne Bacterial Concentration (CFU/m3)
and Temperature (C) and Humidity (%)
in the University Indoor Environments
Correlation College College Student
coefficient (R) canteen Classrooms clinic dormitories
Temperature 0.679a - 0.719b 0.310 0.660a
Humidity - 0.244 0.419 0.297 - 0.517
Correlation is significant at the 0.05 level (two-tailed).
Correlation is significant at the 0.01 level (two-tailed).
280
university indoor environments. Since all correlation coeffi-
cients of the bacterial concentrations with temperature at four
sites are larger than those with RH, indoor temperature is more
statistically correlated with bacterial concentration than indoor
humidity. This might be because the variations of the RH are
smaller than those of temperature in this study (as shown in
Fig. 4). To some extent, this is a reflection of meteorological
conditions of Xi’an city located in Chinese semi-arid region.
In addition, it is evident from Table 5 that there are obvious
differences in the degree of correlation between airborne
bacteria levels and temperature in different indoor sites. The
strongest correlation of bacterial counts with temperature is
found in classrooms, followed by canteen and dormitories. In
the clinic, a weak correlation with bacterial numbers can be
observed. Conversely, indoor humidity does not appear to
have a significant influence on bacterial concentrations in all
indoor sites investigated here. This suggests that the influence
of temperature and RH on airborne bacterial and fungal
concentrations is dynamic and the fluctuation of airborne
bacterial and fungal concentrations indoors affects by various
variables (LeBouf et al., 2008; Raisi et al., 2013).
Size distributions of airborne culturable bacteria
and fungi
Figure 5 illustrates the size distributions of airborne cul-
turable bacteria and fungi in all four indoor sites. For airborne
bacteria collected, there is a similar single-peak concentra-
tion, 4,591 and 4,934 CFU/m3/dlogDp (76 and 104 CFU/m3),
respectively in classrooms and dormitories, in a size range of
3.3–4.7 lm (stage 3). In contrast, there exists a double-peak
pattern of bacterial concentration in the canteen and clinic,
respectively. In the canteen, the major and second peak
concentrations are 7,617 and 7,351 CFU/m3/dlogDp (85 and
170 CFU/m3), in the > 7 lm (stage 1) and 3.3–4.7 lm (stage
FIG. 5. Size distributions
of airborne bacteria and
fungi in university indoor
environments.
LI ET AL.
3) size range, respectively. In the clinic, the major and second
peak concentrations are 4,826 and 4,399 CFU/m3/dlogDp
(135 and 67 CFU/m3) in the 3.3–4.7 lm (stage 3) and > 7 lm
(stage 1) size range, respectively.
For the airborne fungi, the double-peak pattern can be also
observed in the canteen and clinic, respectively: the major
peak concentration in the 3.3–4.7 lm (stage 3) and > 7 lm
(stage 1) size range, and another peak concentration in the
size range of > 7 lm (stage 1) and 3.3–4.7 lm (stage 3), re-
spectively. A single-peak concentration appears in a size
range of 3.3–4.7 lm (stage 3) in classrooms, whereas stage 3
(3.3–4.7 lm) and stage 2 (4.7–7 lm) dominate in dormitories.
The size distribution peaking toward the coarse size frac-
tion shows that bioaerosols may appear as agglomerates or
attached to other nonbiological matrixes rather than single
cells. The recent study by Qian et al. (2012) also found the
largest increase in concentration on the largest impactor stage
( > 9 lm) due to human occupancy. Moreover, the species
composition can also play a role in the size distribution. As
stated by Yamamoto et al. (2012), the size of bioaerosols is
different according to each genus and is dependent upon the
age and nutrient source of the spore. Therefore, some dif-
ferences in size distribution patterns of airborne bacteria or
fungi can be found in this study. For example, the size dis-
tributions of bacteria and fungi are different in dormitories in
this study, while in other three indoor environments show
similarity. It is still comparable with other results obtained by
Nasir and Colbeck (2010, 2012), in which the bacteria and
fungi show similar size distributions in Type I house (single
bedroom) and KIT (kitchen), while in other indoor environ-
ments differences exist. However, in this study we cannot
give further detailed explanation on this phenomenon due to
the lack of information on the age and nutrient source of
bioaerosols, but we will focus on this phenomenon in our
future studies.
ASSESSMENT OF AIRBORNE BACTERIA AND FUNGI
Figure 6 shows the cumulative size distributions of air-
borne bacteria and fungi detected in this study. About 83.1%,
82.0%, 79.9%, and 79.5% of airborne bacteria, and 84.7%,
85.8%, 81.3%, and 83.6% of airborne fungi, are found in the
size range of less than 4.7 lm, respectively, in canteen,
classrooms, clinic, and dormitories. This indicates that close
to 80% of bacterial aerosols and more than 80% fungal
aerosols are in respirable size range in all of the present in-
door environments. The respirable particles have potential to
deposit in the lower respiratory system. Therefore, there is a
potential risk of bioaerosols to students and staff in university
indoor environments. Furthermore, the present finding also
suggests that the respirable fraction of bioaerosols does not
significantly vary among housing type. To our knowledge,
the available results related to the respirable fractions of
bioaerosols in university indoor environments are very few.
However, the proportion of respirable bioaerosols in the
present environments are comparable to the results obtained
in other indoor environments (Pastuszka et al., 2000; Wang
et al., 2010a; Nasir and Colbeck, 2012), suggesting that the
respirable fraction of bacteria and fungi might be not de-
pendent on building type and material, geographical and
meteorological factors.
Based on the cumulative size distributions, both NMD and
GSD can be also obtained. The NMD and GSD of bacte-
rial concentrations are 2.99 – 0.12, 2.67 – 0.19, 2.83 – 0.09,
and 2.77 – 0.12 lm in the canteen, classrooms, clinic, and
dormitories, respectively, while both values of fungal con-
centrations are 2.83 – 0.10, 2.51 – 0.18, 2.76 – 0.97, and
2.59 – 0.26 lm, respectively. It is obvious that the NMD of
bacteria is larger than that of fungi at each indoor site, which
may be attributed to the fact that airborne bacteria primarily
exist in clusters or attached to particles. It can be also found
that the largest NMD of bacterial and fungal aerosols appear
in the canteen, while the smallest value happened in the
classrooms. This may due to different spore agglomeration
281
FIG. 6. Cumulative size
distributions of airborne bac-
teria and fungi in university
indoor environments.
rates affected by indoor activities and various species com-
position from different sources, which still needs further
study in our future work.
The NMD of airborne bacteria and fungi in four indoor
environments are all in the size range of 2.1–3.3 lm (stage 4),
which is consistent with other reported studies. Reponen
(1995), Zuraimi et al. (2009), and Wang et al. (2010a) found
that the NMD of airborne fungal spores was in the range 2.1–
3.3 lm in moisture-damaged buildings. Conversely, Nasir
and Colbeck (2010) reported larger NMD of total bacteria
and fungi concentrations (3.3–4.7 lm) in nonmouldy resi-
dences. Differences in use and management of room space,
mould infestation, and dampness are the most likely expla-
nations for the observed discrepancies.
Conclusions
In this study, it was found that the concentration of airborne
bacteria and fungi varied in different indoor environments
of Chang’an University in Xi’an, China. The highest mean
concentration of both airborne bacteria and fungi was ob-
served in the canteen, followed by the clinic and dormitories,
and the lowest found in classrooms. Moreover, the ratio of
indoor to outdoor concentration of airborne bacteria and fungi
was greater than 1 in most indoor environments except for
classrooms, implying that the indoor air might be contami-
nated with bioaerosols. It was also found that although mean
concentrations of airborne bacteria and fungi in investigated
university rooms did not exceed the threshold limit value of
China, they were higher than those detected in indoor envi-
ronments of western universities and most guideline values
proposed by some organizations all over the world.
Within the same room, the concentrations of both cultur-
able bacteria and fungi also varied with seasons. In all four
indoor sites, there were higher fungal concentrations in au-
tumn and winter than in spring and summer. In contrast, there
282
were not similar seasonal variations of airborne bacteria in
various indoor environments. The environmental parameters
investigated here are found to have different effects on
bioaerosols in various indoor environments. Indoor temper-
ature showed more significant correlation with bioaerosols
than RH in all indoor environments.
In addition, it was found that the size distribution of air-
borne bacteria and fungi varied in different indoor environ-
ments investigated in this study. The highest number of
culturable bacteria were observed in a size range of 3.3–
4.7 lm in classrooms and dormitories, while the size ranges
3.3–4.7 and 7 lm and above dominated in the canteen and
clinic. For culturable fungi, stage 1 (7 lm and above) and
stage 3 (3.3–4.7 lm) dominated in the clinic and canteen,
respectively, while stage 2 (4.7–7 lm) and stage 3 (3.3–
4.7 lm) dominated in dormitories, and stage 3 had a major
share in classrooms. Another finding was that about more
than 75% bacterial and fungal aerosols in university indoor
environments were in the respirable size range (less than
4.7 lm). The observed differences in concentration and size
distribution of bacterial and fungal aerosols in various uni-
versity rooms reflect not only the differences in sources of
bioaerosols but also the differences in influence factors such
as occupant density and lifestyle, room conditions, and en-
vironmental parameters.
It is worth noting that the number of microorganisms in
bioaerosols reported in this study is only for culturable ones
on selective media, probably accounting for < 0.1% of the
total microorganisms in each site. Although this could lead to
an underestimation of the total concentration, it can be ex-
pected from the present results of large I/O ratio and high
respirable fraction of bioaerosols that the indoor environ-
ments in Chinese universities could not be safe. Moreover,
the results derived from this study are useful for providing
valuable information on exposure assessment in university
indoor environments and future determination of Chinese
official standard in indoor air quality although this field study
is only carried out in one university in Xi’an and does not
consider the specific characteristics of hazardous factors of
airborne microorganism as well as characteristics of different
species.
Acknowledgments
The authors would like to thank the National Natural
Science Foundation of China (41230314, 51208059) and the
Special Fund for Basic Scientific Research of Central Col-
leges, Chang’an University (2013G2291013).
Author Disclosure Statement
No competing financial interests exist.
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