Journal of Environmental Health Science and Engineering (2021) 19:1635–1642

https://doi.org/10.1007/s40201-021-00719-5

RESEARCH ARTICLE

Bacteria bioaerosol in the indoor air of educational

microenvironments: Measuring exposures and assessing
health effects
Anoshirvan Sadigh 1 & Ebrahim Fataei 2 & Mohsen Arzanloo 3 & Ali Akbar Imani 4

Received: 17 July 2021 / Accepted: 4 August 2021 / Published online: 13 August 2021
# Springer Nature Switzerland AG 2021

Abstract
Exposure to bioaerosols has been identified to be linked the incidence of various health effects, i.e., infectious diseases, acute
toxic effects, allergies, and cancer. The aim of this study was to determine the bacterial bioaerosols in the indoor air of the
educational environments of Ardabil universities and to evaluate the exposure and to determine its health risk. In this
cross-sectional study, different sections of the educational environments of Ardabil universities were studied. For differential
diagnosis of bacteria, methods such as gram staining and biochemical detection methods including DNAse, catalase, oxidase,
coagulase, bile esculin hydrolysis test, urease, citrate test, antibiotic resistance to novobiocin and Bacitracin, optochin, glucose
uptake, and other differential tests were used. For sampling, a single-stage Anderson sampler was used at a flow rate of 28.3 l at a
duration of 10 min per minute. The results showed that, in medical school of Ardabil University of Medical Sciences, the average
concentration of bacteria in the outdoor air of school, halls, classes and rooms of professors and staff were 18, 88.4, 76.6, and
77.4 CFU/m3, respectively, and, in Ardabil Islamic Azad University, the average bacterial concentration was 103, 97, 124, and
132 CFU/m3 in the outdoor air of the schools, halls, classrooms, and rooms of professors and staff, respectively. The predominant
bacterial species in indoor air are S. aureus, S. epidermidis, Actinomycetes, and Bacillus, respectively. As results indicated, the
concentration of bacterial bioaerosols in indoor air is within the standard levels, but due to frequency of bacterial species,
occurrence of different in lung and intestinal diseases can be expected among faculty, staff and students in the long-term.

Keywords Bioaerosol . Indoor air pollution . Bacterial . Ardabil

Introduction offices, schools), which are exposed to certain indoor environ-

Air is the most essential human need that contains various
particles and microorganisms [1–5]. More than 90% of peo-
ple’s lives is spent indoor environments (including homes,
* Ebrahim Fataei
eafataei@gmail.com
1
PhD Student in Environmental Science and
Engineering-Environmental Pollution, Department of environment
science and engineering, Ardabil branch, Islamic Azad university,
Ardabil, Iran
2
Department of Environment Science and engineering, Ardabil
Branch, Islamic Azad University, Ardabil, Iran
3
Department of Microbiology, School of Medicine, Ardabil
University of Medical Sciences, Ardabil, Iran
4
Department of Agricultural Engineering, Ardabil Branch, Islamic
Azad University, Ardabil, Iran
mental factors and can have negative effects on health and
well-being [6–9]. Bioaerosols can remain suspended in the
air for a long time and can exist in the air, alive or
non-living [10]. Therefore, exposure to bioaerosols in closed
environments is increased so that 5–34% of indoor air pollu-
tion is related to these airborne particles [11, 12]. Indoor air
may contain various type of microorganisms, e.g., bacteria,
fungi, and viruses, some of which can affect human health
[13]. Indoor air pollution concentrations depend on many fac-
tors such as internal sources and emissions, air exchange rates,
the penetration of external pollutants into the indoor environ-
ment, and the rate of sedimentation or removal of pollutants
on interior surfaces [14–16].
Bioaerosols enter the human body in different ways and
cause different health effects [17–19]. Exposure to bacterial
bioaerosols can cause a wide range of complications such as
inflammation and irritation of the upper and lower respiratory
tract and allergic reactions in the lungs, especially in
1636
susceptible individuals [20–23]. Indoor air quality and its im-
pact on student health are of great importance in public health
studies. The average attendance time of students in schools is
6 h [24]. The student is exposed to airborne physical, chemi-
cal, and microbial agents inside the classroom. Airborne trans-
mission is one of the routes of transmission of infectious dis-
eases in students [25]. The type and number of airborne bio-
logical aerosols in the classroom are associated with the
spread of disease in students; therefore, it is necessary to con-
trol the concentration and viability of biological aerosols in the
indoor air of schools [26]. According to the World Health
Organization (WHO), 5,000,000 people die each year before
reaching puberty from exposure to airborne aerosols [27–29].
It has been publicized that microorganism, particularly fungi
and bacteria, are associated with health risks for students. The
number of fungal spores in normal conditions is 103–104 per
cubic meter of air. The Taiwan Environmental Organization
has set the standard number of bacteria and fungi in the indoor
air of schools in terms of CFU/m3 at 500 and 100, respectively
[30]. According to the studies on biological aerosols in indoor
air, some carpet weaving industries and health centers
(hospitals) in different areas of our country such as Isfahan,
Shiraz, and Hamedan also have biological aerosols with a
concentration higher than the standards [27, 30, 31]. Studies
by the United States environmental protection agency
(USEPA) also confirm the fact that indoor air pollution is
more dangerous than outdoor air pollution [32]. The problem
of indoor air quality became serious when residents of some
areas complained of discomfort such as hair loss, itchy skin,
eyes, allergies, fatigue, headaches, and dizziness.
Bioaerosols enter the human body through a variety of
pathways (inhalation, ingestion, or absorption through the
skin) and produce a variety of health effects, including infec-
tious diseases, acute toxic effects, allergies, and cancer.
Inhalation is the most important pathway of transmission of
these microorganisms to the body. Respiratory infection and
impaired lung function are among the health implications
caused by exposure to bioaerosols. Considering that children
receive more air than adults according to their body weight
and older people also have a weak defense system, the expo-
sure risk of these people bioaerosols is much higher.
Environmental factors such as temperature, humidity, and
ventilation can expressively affect the levels of bioaerosols
in the building [32]. Activities such as talking, sneezing,
coughing, walking, washing, etc. can cause the production
of bioaerosols. Foods, plants, and pets, wood and furniture
materials, textiles, and carpets sometimes release fungal
spores into the air [33].
Each person breathes an average of 12,000 to 14,000 l of
air per day. For this reason, more than 99% of airborne germs
can be isolated from the respiratory system. Infection of the
respiratory system depends on the type and number of micro-
organisms in the air [34]. Therefore, the aim of this study was
J Environ Health Sci Engineer (2021) 19:1635–1642
to investigate the concentration of bacterial bioaerosols and
evaluate the exposure and determine the health risk in the
indoor air of Ardabil universities in 2019.
Materials and methods
Sampling location
This descriptive study was performed in Ardabil Universities
(Islamic Azad and Ardabil Medical Sciences) in the autumn of
2019. In this study, after determining the ventilation status of
respiratory air from different parts of the Faculty of Basic
Sciences of Islamic Azad University and the Faculty of
Medicine of Ardabil Medical Sciences at different times of
sampling and samples for Bacterial bioaerosols, temperature
and relative humidity were examined. The sampling site in-
cluded floor halls, classrooms, laboratories, meeting rooms,
and staff and faculty rooms. In addition, air sampling was
performed in the outdoor environments of university faculties
to compare the bacteriological status of the air and to compare
with each other. During sampling, information of each sample
including the type of culture medium, time and place of sam-
pling, sampling time, type of ventilation, number of people in
each section, temperature, and relative humidity were collect-
ed by the researcher-made questionnaire.
Air sampling from indoor air of educational
environments
The air sampling method was performed according to the
standard of the USEPA. Sampling in this study was performed
using Anderson single stage sampler model ZTHV 02 made
by German company Zefon with a flow rate of 28.3 l per
minute and a sampling time of 10–15 min [35, 36]. Prior to
sampling, sampling pump flow was calibrated by a digital
calibrator (defender). For sampling, the sampling device was
placed at a height of 120–150 cm above the ground (in the
respiratory area) and at a distance of more than 1 m from the
walls and obstacles. The culture medium used in this study
included Tryptic Soy Agar along with Cycloheximide antibi-
otic (Sarva company) as an antifungal for bacterial samples,
which was made in the laboratory by maintaining complete
sterile conditions and kept in the refrigerator until use [21].
Sterile conditions were required for the samples at each sam-
pling. Therefore, before placing the culture medium inside the
sampler, the cassette was disinfected and dried using 70%
ethanol alcohol to remove any initial contamination. The
plates, after sampling, were sealed with paraffin for reducing
the error caused by secondary contamination. After sampling,
the plates were placed in a cool box and immediately trans-
ferred to a laboratory. In addition, at each sampling, WBGT
J Environ Health Sci Engineer (2021) 19:1635–1642 1637

Table 1 Risk parameters applied for simulation of HQ, and LADD of (LADDs) can be calculated according to documented methods
bacteria bioaerosols
of the USEPA [37]. Exposure assessment was conducted for
Parameter Abbreviation Value Reference employees referred to educational environments in university.
The people could be exposed to bioaerosols via dermal con-
Inhalation rate (m3/day) IR 18.7 IRIS EPA tact (skin), inhalation, and digestive. In addition, exposure is
Bacteria bioaerosol C – This study defined as the lifetime average daily dose (LADD) that can be
concentration (CFU/m3)
Exposure Frequency (day/year) EF 313 This study
estimated individually for both routes (dermal contact and
inhalation) [38, 39]. Hence, the design of exposure scenario
Exposure time (h/day) ET 8 This study
was performed as follows:
Exposure duration (year) ED 35 This study
The measurement of exposure time (ET) and exposure
Averaging time (year) AT 30*313 IRIS EPA
frequency (EF) of employees was accomplished by a
Skin adherence factor SAF 0.07 (33)
(kg (m3.d)−1)) face-to-face interview method. It was supposed that the
Exposure skin area (m2) ESA 0.215 (30) age of these people working in university were in range
Dermal absorption factor DAF 0.001 (30) of 25 to 60. Thus, the 35 years was considered as their
Reference dose (CFU/m3) RfD 5000 IRIS EPA exposure duration (ED).
According to eq. 1 and 2, the LADD for inhalation (CFU
(kg.d)−1) and dermal contact (CFU (kg.d)−1) were calculated
for employing in the estimation of non-carcinogenic risk.
model MK427JY made in England was employed to measure LADD inhalation = (C × IR × ET × EF × ED)/ (AT × BW)
temperature and relative humidity. (1).
LADD dermal = (C × ESA× SAF × DAF× ET × EF × ED)/
Culture and identification of bacteria (AT × BW) (2).
Where, C is concentration at exposure (CFU/m3), BW
To identify bacterial species, the culture medium was incubat- is body weight (kg), ET is exposure time (yr), IR is inha-
ed at 35 °C for 24 to 48 h. For differential diagnosis of bacte- lation rate (m 3 /day ), EF is e xposu re fre quen cy
ria, methods such as gram staining and biochemical detection (days/year), ED is exposure duration (yr), AT is average
methods including DNAse, catalase, oxidase, coagulase, bile lifetime (yr), ESA is exposure skin area (m2), DAF is
esculin hydrolysis test, urease, citrate test, antibiotic resistance Dermal absorption factor and SAF represents skin adher-
to novobiocin and bacitracin, optochin, sugar intake and other ence factor (kg (m3.d)−1) [38].
differential tests were used and finally air samples were re- Through employing hazard quotient (HQ), risk assessment
ported based on CFU/m3. for the non-carcinogenic risk of bacteria bioaerosol was cal-
culated. HQ was calculated as the ratio of lifetime average
Health risk assessment daily dose (LADD dermal or LADD inhalation) (CFU (kg.
d)−1) to the reference dose for chronic exposure (RfD) (CFU
After measuring the concentration of bacterial bioaerosols in (kg.d)−1); the equation for calculation of HQ is represented as
different educational units, lifetime average daily dose follows [37]:

Fig. 1 Average density of

100
bacteria in the air of medical 88.5
Average density of bacteria in the air

school, Ardabil University of 90

Medical Sciences 76.6 77.4
80
70
60
50
40
30
18
20
10
0
Outdoor air Halls Classrooms Rooms of
professors and
staff
1638 J Environ Health Sci Engineer (2021) 19:1635–1642

Fig. 2 Average density of

140 132
bacteria in the air of the Faculty of

Average density of bacteria in the air

124
Science, Ardabil Islamic Azad
University 120
103
97
100

80

60

40

20

0
Outdoor air Halls Classrooms Rooms of professors
and staff

LADD dermal ðCFU ðkg:dÞ−1Þ or LADD inhalation ðCFU ðkg:dÞ−1Þ

Results and discussion
HQ ¼
RfD ðCFU ðkg:dÞ−1Þ
In this study, a total of 80 samples were prepared from
ð3Þ
Ardabil universities (Islamic Azad and Medical Sciences)
The mean concentration of bacteria bioaerosols in the dif- and the density of bioaerosols was reported based on
ferent educational units was used to calculate the LAAD. Risk CFU/m3. The average concentration of bacteria in the in-
parameters used for calculating HQ and LADD for bacteria door and outdoor air of the studied universities is shown
bioaerosols are given in Table 1. in Figs. 1 and 2. As can be seen, in the medical school of
For HQ value above 1, the significant potential risk has Ardabil University of Medical Sciences, the average con-
been defined. Inversely, HQ ≤ 1 is indicative of an acceptable centration of bacteria in outdoor air, halls, classrooms and
level of risk because the dose level is lower than the reference rooms of professors and staff is equal to 18, 88.4, 76.6,
dose (RfD) [40–45]. and 77.4 CFU/m3, and the average concentration of bac-
teria in Ardabil Islamic Azad University in the outdoor air
Statistical analysis of the faculty, halls, classes and rooms of professors and
staff are 103, 97, 124, 132 CFU/m3, respectively. In the
In the present study, descriptive statistics were used for anal- present study, the highest concentration of bacteria was
ysis to determine the mean, distribution and standard devia- observed in Class 7 of Ardabil University of Medical
tion, and analytical statistics were used to determine the dif- Sciences (230 CFU/m3) and the lowest concentration of
ferences in data, correlation of variables and obtaining depen- bacteria was related to Class 5 of Ardabil University of
dency relationships. The Kolmogorov-Smirnov test (K-S Medical Sciences (22 CFU/m3). It should be noted that
testor KS test) was applied to recognize the normal distribu- the average temperature and relative humidity for the
tion of quantitative variables. The investigation of the relation- University of Medical Sciences were 24.1 degrees
ship between temperature and humidity and bacterial density Celsius and 29.8%, respectively, and for the Islamic
was carried out using Pearson correlation coefficient test. Data Azad University were 22.2 degrees Celsius and 36.5%,
analysis was performed using SPSS-20 software. Finally, the respectively.
results of counting colonies were compared with the standard The results related to analysis of variance exhibited the
provided by WHO (500 CFU/m3) [46]. existence of a significant difference among the 4 studied

Table 2 Bacteria diversity in indoor air of Ardabil University faculties based on the percent

University name Actinomycetes Bacillus Enterobacteriaceae E. faecium E. faecalis S. saprophyticus S. epidermidis S. aureus
EC

Medical sciences 17.5 7.5 2.5 2.5 12.5 2.5 60 75

Islamic Azad 0 40 0 2.5 5 0 25 90
J Environ Health Sci Engineer (2021) 19:1635–1642 1639

Table 3 Statistical summary of LADD-inh (inhalation) and LADD-der (dermal) and HQ-inh (inhalation) and HQ-der (dermal) in different universities
of Ardabil

University name parameter LADD-inh HQ-inh LADD-der HQ-der

Ardabil university of medical sciences Mean 494.9 0.1 1×10−5 2×10−9

Standard Deviation 368.7 0.07 9×10−6 1×10−9
minimum 8.27 0.001 2×10−7 4×10−11
maximum 3798.4 0.76 9×10−5 1×10−8
Islamic azad university Mean 610.2 0.12 1×10−5 3×10−9
Standard Deviation 330.9 0.07 8×10−6 1×10−9
minimum 18.8 0.003 8×10−7 1×10−10
maximum 3017.9 0.6 7×10−5 1×10−8

places only in terms of temperature and number of people,
while no significant difference was observed between the
studied places in terms of other characteristics.
Examination of the results of the respiratory air samples of
the faculties showed that 75% of the respiratory air of the
medical school and 90% of the respiratory air of the school
of science was infected with S. aureus and 60% of the respi-
ratory air of the medical school and 25% of the respiratory air
of the school of science was infected with S. epidermidis, and
S. saprophyticus, E. faecalis, E. faecium, Enterobacteriaceae,
Bacillus, and Actinomycetes were in low percentages
(Table 2).
Findings showed that the highest and lowest mean bacterial
concentrations among the studied faculties were related to the
respiratory air of the rooms of the faculty and staff of Ardabil
Islamic Azad University (132 CFU/m3) and the outdoor air of
the medical school of Ardabil University of Medical Sciences
(18 CFU/m3), respectively. The reason for this is the closed air
and the presence of people higher than standard levels in the
educational space and lack of proper ventilation. According to
the results, the highest percentage of bacteria in the respiratory
air of the medical school and the school of science was related
to S. aureus and S. epidermidis. Sadeghi et al. conducted a
study to inspect the type and density of bioaerosols in the air
of different wards of Valiasr Hospital in Khorramshahr. The
findings disclosed that the highest mean concentration of con-
tamination in spring with a concentration of 51.2 and in au-
tumn with a concentration of 167.0 CFU/ml was related to the
infectious ward and the lowest amount of contamination was
observed in the CCU ward. Also, in his study, the most

Fig. 3 Simulated HQ values for 450 450

bacteria bioaerosol originated 400 400
Ardabil university of medical

from exposure of inhalation and 350 350

dermal in Ardabil universities 300 300
Frequency
Frequency

250 250
200 200
150 150
i

100 100
50 50
0 0
0.00 0.08 0.15 0.23 0.30 0.00 0.00 0.00 0.00 0.00
HQ HQ
400 450
350 400
300 350
Islamic azad university

300
250
Frequency
Frequency

250
200
200
150
150
100 100
50 50
0 0
0.01 0.08 0.16 0.23 0.30 0.00 0.00 0.00 0.00 0.00
HQ HQ
1640
bacteria recognized in the air sample were related to
Staphylococcus epidermis with 25.9% [1]. Also, in a study
conducted by Sudarsanam et al. for investigating bacteria
and fungi in selected hospitals in India, the results showed
that Staphylococcus and Micrococcus bacteria were the most
common bacterial species in air samples [47]. Asan et al. also
examined the predominant indoor and outdoor bacterial gen-
era in child day-care centers in Turkey [48]; their study con-
firmed the results of the present study. Also, different results
were also reported by Hsu et al.
(2012) [49] in at 39 public sites in Tainan (Taiwan) and
Naddafi et al. (2019) [21] at indoor air of 50 waterpipe cafes in
Ardabil (Iran) with the mean bacterial concentrations from
196 to 4875 CFU/m3 and from 6.0 to 6.5 × 101 CFU/m3,
respectively.
The independent sample t-test disclosed the existence a
significant difference between the two universities in terms
of all evaluated characteristics except the number of people
at the significance level of 1% probability; so that, comparison
of mean values showed that in terms of the average number of
bacterial colonies and relative humidity, Azad University was
more than the University of Medical Sciences, but in terms of
temperature, the medical sciences were higher than the Islamic
Azad University.
Based on the results, the most abundant bacteria detected in
university air were coagulase-negative staphylococci and en-
terococci. Among these microorganisms, coagulase-negative
staphylococci and enterococci were observed in both univer-
sities, both of which are gram-positive cocci. The high con-
centration of gram-positive cocci in the air may be due to the
lower sensitivity of these bacteria to ambient pressure or tem-
perature, which is consistent with the research conducted by
Norouzi et al. at Gorgan University [50]. Despite the fact that
coagulase-negative staphylococcus is not highly toxic, it is an
important cause of infection in high-risk groups.
Staphylococci are highly resistant to drought and harsh con-
ditions, and this feature facilitates their life in the environment,
food multiplication, and contagion [51]. Enterococci are resis-
tant bacteria in harsh conditions so they can survive in the air
[13].
Health risk assessment
The mean values of LADD and HQ calculated from inhalation
and dermal route for people in indoor air of Ardabil University
of medical sciences and Islamic Azad University are displayed
in Table 3 and Fig. 3. As observed, in the Ardabil University
of medical sciences, the lifetime average daily dose (LADD)
ranged from 8.2 to 3798.4 CFU (kg.d)−1 for the inhalation
route and from 2 × 10−7 to 9 × 10−5 CFU (kg.d)−1 for the der-
mal route. Also, In the Islamic azad university, the LADD
ranged from 18.8 to 3017.9 CFU (kg. d)−1 for the inhalation
route and from 8 × 10−7 to 7 × 10−5 CFU (kg. d)−1 for the
J Environ Health Sci Engineer (2021) 19:1635–1642
dermal route. The mean ± SD values of HQ in indoor air of
Ardabil University of medical sciences and Islamic Azad
University were 0.1 ± 0.07 and 0.12 ± 0.07, respectively. HQ
values>1 is indicative of unacceptable exposure conditions
with high chronic non-cancer risks for the target organs in
human body [43, 52].
The values were lower than the USEPA and WHO limit in
both groups. As can be seen in the table, the estimated HQ for
the Islamic Azad University was higher than the Ardabil
University of Medical Sciences mainly due to more density
in the Islamic Azad University. The risk of exposure of skin
was trivial. So, the risk of exposure to bioaerosols in the in-
door air was predominantly linked to the respiratory inhalation
pathway. Comparable findings have been acquired in a waste
paper and cardboard recycling factory of Tehran by Baghani
et al. (2020); based on their findings, the average HQ values
for the inhalation and dermal route in processing units were
7.2 × 10−3 and 6.9 × 10−9, respectively, which approves our
results [53]. Also, Yan et al. [54] implemented a study on
culturable airborne bacteria and fungi during winter in
Xinxiang and observed that the ranges of HQinh for adult
males, adult females, and children were 1.2 × 10−2 to 1.04 ×
10−1, 1.0 × 10−2 to 8.4 × 10−2, and 5.1 × 10−3 to 4.2 × 10−2,
respectively; this also is in agreement with the results of the
present study.
Conclusion
In general, the results obtained is indicative of this fact that the
density of bioaerosols in indoor air was higher than in the
outdoor air. In addition, the highest percentage of bacteria in
the respiratory air samples was related to S. aureus and
S. epidermidis. The results of this work demonstrated that
the mean of HQ in indoor air of Ardabil University of medical
sciences and Islamic Azad University were 0.1 and 0.12, re-
spectively which were lower than the USEPA and WHO limit
in both groups. The findings of the present study are useful for
governments to enact policies for teachers, young people and
students that are exposed to these educational places around
the world. In addition, these results can help researchers for
further studies on the respiratory diseases. The future research
may focus on species and concentration of fungi bioaerosols
and the influence factors on the bioaerosols.
Acknowledgments This research is extracted from the dissertation of the
Ph.D student in Environmental Engineering with a focus on environmen-
tal pollution at the Islamic Azad University of Ardabil with the disserta-
tion code of 1194814626441811398157599. Therefore, the authors ap-
preciate the esteemed president, educational and research deputies of
Ardabil Islamic Azad University for their cooperation in facilitating the
implementation of this project. Also, Dr. Mehdi Fazlzadeh, Dr. Abdollah
J Environ Health Sci Engineer (2021) 19:1635–1642
Dargahi and Dr. Peyman Azghani are sincerely appreciated and thanked
for their help in the process of this research.
Declarations
Conflict of interest The authors declare that there is no conflict of inter-
est regarding the publication of this manuscript.
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