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Int J Env Health Eng 2020,  9:21

A comparative evaluation of bioaerosol emission and particle matter concentration in Urban primary schools

1 Department of Environmental Health Engineering, School of Health, Arak University of Medical Sciences, Arak, Iran
2 Student Research Committee, School of Health, Arak University of Medical Sciences, Arak, Iran

Date of Submission29-Apr-2020
Date of Acceptance04-Jul-2020
Date of Web Publication31-Dec-2020

Correspondence Address:
Seyed Hamed Mirhoseini
Department of Environmental Health Engineering, School of Health, Ghods Street, Golestan quarter, Arak
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ijehe.ijehe_30_20

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Aim: In this study, the levels of indoor and outdoor (I/O) airborne particles and bioaerosols were assessed in two primary schools. Simultaneously, I/O microbial airborne and particle matter (PM) concentrations were analyzed during the autumn of 2018. Materials and Methods: A total of 96 I/O air samples were taken by using a single-stage Andersen sampler from two selected primary schools located in Arak, Iran. Simultaneous with sampling, PM10 and PM2.5 concentrations, temperature, and relative humidity were also measured. Results: The results indicated that the mean levels of indoor airborne bacteria and fungi were 448 and 94 CFU/m3, respectively. The I/O ratios of bacteria and fungi were 2.1 and 0.7, respectively. The airborne bacteria levels showed a weak-positive and moderate-positive association with PM2.5 (r = 0.28, P < 0.05) and PM10 (r = 0.32, P < 0.05), respectively. Further, a moderate-positive association was observed between indoor fungi and the PM2.5 (r = 0.46, P < 0.05) and PM10 (r = 0.30, P < 0.05). In our study, the most fungal species identified were Penicillium, Cladosporium, and Aspergillus, and Staphylococcus spp., Micrococcus spp., and Bacillus spp. were the most frequently founded indoor bacteria. Conclusion: Comparative analysis of classrooms in two schools showed that indoor sources and building conditions have a key role in indoor air quality.

Keywords: Bioaerosols, indoor air, particle mass concentration, primary school

How to cite this article:
Mirhoseini SH, Dehdashti FA, Mohammadi S. A comparative evaluation of bioaerosol emission and particle matter concentration in Urban primary schools. Int J Env Health Eng 2020;9:21

How to cite this URL:
Mirhoseini SH, Dehdashti FA, Mohammadi S. A comparative evaluation of bioaerosol emission and particle matter concentration in Urban primary schools. Int J Env Health Eng [serial online] 2020 [cited 2021 Dec 2];9:21. Available from:

  Introduction Top

Nowadays, indoor air quality (IAQ) in schools has become a major health concern. Children spend more of their time at school compared to anywhere else.[1] Because of their undeveloped immune and respiratory system, inferior body mass index and breathing pattern of children are more susceptible to the effects of air pollution than adults.[2] Studies have shown that exposure to environmental contaminants in schools may result in harmful health impacts, such as infectious diseases, increased risk of asthma and allergies, and acute toxic effects, and also decreased learning performance of children.[3],[4] Mentese and Tasdibi reported that respiratory illnesses from airborne contaminants are a common problem for humans, particularly for children.[5] Daisey et al. carried out a review of the existing published works on IAQ and building-related health symptoms in schools. The type of health problems observed in schools was very similar to those defined as the sick building syndrome. Species of Penicillium, Aspergillus, and Cladosporium have been most frequently associated with allergy and exist both in indoor and outdoor (I/O) environments.[6] The indoor environment of each school consists of exclusive features which may be affected by different factors. The high number of students in classrooms, deficient air ventilation, poor maintenance, old buildings, and equipment could deteriorate IAQ levels in classrooms.[7],[8] Airborne particle matter (PM), a complex and dynamic mixture of components with biological, physical, and chemical origins, is one of the pollutants that can cause a decrease of IAQ in school buildings.[9] It is known that bioaerosols consist of about 24% of whole airborne particles and 5%–10% of airborne-suspended particles.[1] In many indoor environments, microbial particles with aerodynamic <5 μ can penetrate deep into the respiratory tract.[10] In recent investigations, more attention has been paid to the biological fraction of PM (bioaerosols) and suggests that bioaerosols may be the main cause of the impact of PM on people's health.[11],[12] Because kids attending school spend a lot of time in the classroom, it is very important to ensure of their optimal health condition, especially the concentration of allergenic or toxigenic airborne bacteria and fungi along with their relationship with IAQ.[13] The major fraction of bioaerosols consists of bacterial and fungal spores.[14] Indoor air pollution consists of approximately 5%–34% bioaerosols.[15],[16] Considering the importance of bioaerosols, the World Health Organization has set a guideline for bioaerosols, such as indoor bacteria and fungi levels.[10] Therefore, the investigation of the biological quality of indoor air in primary schools is necessary for the determination of the levels of contaminants along with the implementation of corrective measures to further improve the quality of the air. The aims of this study are as follows: (1) to investigate the concentration levels of airborne bacteria and fungi in two primary schools; (2) to determine the PM mass concentration (PM10 and PM2.5) and meteorological parameters (temperature and relative humidity [RH]) and their association with the levels of bacteria and fungi; and (3) to identify the predominant bacterial and fungal genera in the indoor environment of selected schools.

  Materials and Methods Top

Geographical location of the study area

This study was done in two selected primary schools located in the Arak metropolitan area, Iran. Arak is the capital of Markazi Province [Figure 1] and is one of the major industrial cities located at the center of Iran. This city has Mediterranean continental weather with an average precipitation of about 350 mm and with a mean RH of 46%. The recent population city of Arak is about 520,000 people around 49.69° east longitude and 34.09° north latitude, with an average height of 1750 m above sea levels.[17] The location of the primary schools is shown in Figure 1. Data relating to the characteristics of the school building, the ventilation system, and the number of students in the classrooms are summarized in [Table 1].
Figure 1: Location of two primary schools in Arak, Iran

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Table 1: The school building characteristics

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Air sampling and analytical methods

I/O air samples were collected between September and December 2018. The I/O airborne microorganisms were collected using a single-stage Andersen sampler (SKC Inc.) with 400 holes. The flow rate of the pump was set at 28.3 L/min using a rotameter before each sampling. The impactor was sterilized with a 70% ethanol solution before and between sampling. The indoor samples were collected from about 1.5 m above the ground level, from the level of breathing zone, and in the middle of the classroom every 10 min. The outdoor samples were taken from the playgrounds of the primary schools and at least 2 m away from the adjacent buildings. The tryptic soy agar media and malt extract agar were used for bacteria and fungi, respectively. After the sampling, the samples were transferred to the microbiology laboratory (Department of Environmental Health, Arak University of Medical Sciences) in a cool box. The bacteria and fungi plates were incubated at 35°C for 24–48 h at 25°C (laboratory temperature) for 3–6 days. Colony-forming units (CFUs) were counted and calculated as CFU per cubic meter of air (CFU/m3).[18] The Bergey's Manual and biochemical tests were applied for the identification of bacterial genera. The fungal genera were identified based on their micromorphological and macromorphological characteristics.[14]

Environmental parameters

Simultaneous with sampling, temperature and RH were also recorded using a portable tester (Kimo instrument, France) at the I/O study sites. The portable dust track TSI Model 8520 Aerosol Monitor (TSI Instruments, TX, USA) was used for the measurement concentrations of particle mass (PM10 and PM2.5).

Statistical analysis

Statistical analysis was done using SPSS 16.0 (SPSS Inc., Chicago, IL, USA). Kolmogorov–Smirnov test and normality were applied upon the usage of parametric and nonparametric tests. We obtained a minimum, maximum, mean, and standard deviation to describe the I/O concentrations of bioaerosols. The Kruskal–Wallis test was used to compare the density differences of indoor airborne bacteria and fungi in the primary schools studied. Mann–Whitney U-test was applied to compare the I/O concentrations of PM10 and PM2.5. Further, the relationships between particle mass concentration and airborne microorganism were surveyed using the nonparametric Spearman's rank correlation method. P < 0.05 was considered statistically significant.

  Results Top

The data show significant differences between bacterial and fungal levels at different sampling sites. As shown in [Table 2], the levels of indoor bacteria ranged from 94 to 1056 CFU/m3 (mean 448 CFU/m3). Further, the concentrations in outdoor air varied from 75 to 456 CFU/m3 (mean 210 CFU/m3). In case of fungi, the indoor concentrations ranged between 5 and 250 CFU/m3 (mean 94 CFU/m3) and outdoor concentrations ranged between 45 and 273 CFU/m3 (mean 127 CFU/m3). However, there was no statistically significant difference between the concentrations of airborne bacteria and fungi found outside of the two school buildings (P > 0.05).
Table 2: Concentrations of the airborne bacterial and fungal (colony-forming units/m3) in the primary schools

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The overall mean of I/O particle mass (PM10 and PM2.5) concentrations and environmental parameters (temperature and RH) from the sampling sites is presented in [Table 3]. In the indoor environment of schools, PM10 and PM2.5 concentrations ranged between 8 and 111 (mean 57 ± 32) and 5–96 μg/m3 (mean 32 ± 16), respectively. The correlation Spearman's rank (r2) between environmental parameters and bioaerosols is shown in Table 4. A weak-positive significant correlation was found between RH and the concentration of airborne bacteria (P < 0.05, R2 = 0.298) and fungi (P < 0.05, R2 = 0.363). The predominant bacteria and fungi in indoor environment of primary schools are shown in Table 5. As seen in Table 5, Staphylococcus spp. (41.6%), Micrococcus spp. (27.5%), and Bacillus spp. (20.8%) were the dominant bacteria genera.
Table 3: The mean±standard deviation indoor and outdoor PM2.5 and PM10 concentrations (μgr/m3) with temperature and relative humidity in classrooms

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  Discussion Top

Concentrations and indoor/outdoor ratios of bioaerosols

Previous studies in primary schools have reported a wide range of the I/O airborne bacteria and fungi concentrations. The indoor levels of bacteria and fungi obtained in this study were in accordance with data reported by various studies.[5],[7],[19] A few studies reported higher indoor levels of bacteria in the classrooms of primary schools in comparison to our current work.[2] The difference in sampling season, environmental conditions, different climatic regions, specific indoor sources, different study designs (sample size, duration, and sampling frequency), and sampling methods could explain the variations in these studies.[20] As a result upon the comparison of the two school environments, the mean concentration of indoor airborne bacteria and fungi in School B was significantly higher than School A (P < 0.05). Further, the highest average concentration of airborne bacteria (559 CFU/m3) and fungi (132 CFU/m3) was found in indoor air of B2 and B1, respectively. The possible explanation for this result may be related to the small space and the higher density of students in School B [Table 1]. This claim is also confirmed by previous reports in which individual occupancy was discovered to affect bioaerosol concentrations.[19],[20] On the other hand, School B, built in 2004, is an older building compared to School A, built in 2017 [Table 1]. Some studies have demonstrated that the difference in the school building (age, variety of building style, and construction material) may also affect the indoor microbial concentrations.[21],[22] In addition, these results could be due to weak ventilation, taking into account that the classrooms of School B contain natural ventilation [Table 1].

Overall, the findings show that the mean levels of bacteria were higher than that of the fungi in all I/O environments, which is consistent with previous reports.[14],[23] The meteorological parameters such as low RH and temperature could explain the lower outdoor levels of fungi. In regard to the maximum limit suggested for indoor airborne bacteria and fungi, reports have indicated the threshold to be 500 and 150 CFU/m3, respectively.[24] The mean level of airborne bacteria in School B exceeded the suggested limit, while neither of the indoor fungi samples exceeded the recommended levels.

Comparing the I/O ratios of bioaerosol concentrations can be a valuable tool to detect the I/O source of airborne bacteria and fungi. In this study, the I/O ratio of bacteria and fungi ranged between 1.4 and 5.6 (mean ratio 2.1) and 0.4 and 1.2 (mean ratio 0.7), respectively [Table 2]. The highest average I/O ratios (2.4) for bacteria levels were obtained from School B. Since the mean I/O ratio for bacteria was higher than 1, it can be concluded that the main sources of airborne bacteria in all sampling sites are indoor sources. In a study in the urban primary schools of Portugal, the mean ratio I/O of bacteria in winter and summer was 16.3 and 7.7, respectively.[25] The I/O value of bacterial aerosols obtained in two nursery schools in Poland ranged between 5.96 in spring and 8.57 in winter.[13] Further, Mentese et al. (2012) reported that the I/O value for bacteria concentrations in indoor classrooms varies from 0.63 to 7.5.[23] The results of the study conducted in Korea schools revealed the lowest value of I/O to be 1.8 and 1.3 for bacterial and fungal samples, respectively.[26]

The results of the statistical analysis indicated that there was a significant difference between I/O concentrations of airborne bacteria (P < 0.05). In addition, the indoor bacteria concentrations did not show a significant correlation with the outdoor concentrations (R2 = 0.26). Therefore, besides the outdoor causes, indoor factors also played a substantial role in the levels of the bacteria in the indoor environments of schools. On the contrary, in case of fungi, the statistical analysis showed that there was no significant difference between airborne fungi concentrations obtained indoors and outdoors (P > 0.05). The correlation coefficients (R2) between the indoor fungi concentrations and the outdoor corresponding concentrations were 0.76, which shows a significant association (P < 0.05).

As compared with other studies which show significantly higher fungi concentrations in the I/O environments of primary schools,[8],[27] it can be concluded that the investigated school classrooms in this work did not contain high fungal contamination.

Particle mass concentrations and environmental parameters

The particle mass concentrations obtained in this study were higher than previous reports obtained from primary school classrooms.[25],[28],[29] According to the results of a study in six Iranian primary schools,[4] the mean PM10 and PM2.5 concentrations (397.2 and 46.9 μg/m3, respectively) were reported to be higher compared to those measured in this study. Further, the indoor median of PM10 and PM2.5 concentrations in 73 classrooms of primary schools in Porto, Portugal, has reported being 127 and 82 μg/m3, respectively, during a 24-h sampling period.[20] The mean outdoor PM10 and PM2.5 concentrations were higher (Mann-Whitney U-test, P < 0.05) than the corresponding indoor concentrations in School A classrooms. However, there were no statistically significant differences between I/O PM concentrations in School B classrooms (P > 0.05). The obtained results are consistent with previous reports.[29],[30] In the present study, the schools were located near heavy traffic roads; thus, outside air contributed to the indoor PM concentration in the classrooms. The Spearman's correlation analysis between PM mass levels and bioaerosol concentrations is presented in [Table 4]. The airborne bacteria showed a weak- and moderate-positive correlation with PM2.5 (r = 0.28, P < 0.05) and PM10 (r = 0.32, P < 0.05), respectively. In addition, a moderate-positive correlation was observed between indoor fungi and PM2.5 (r = 0.46, P < 0.05) and PM10 (r = 0.30, P < 0.05). In contrast, Hospodsky et al. reported that there was no significant correlation between bacteria and fungi with particulate mass concentrations in indoor air, in a study consisting of six classrooms.[31] Meteorological conditions, including temperature and RH during the sampling period, were recorded to study the influence of these parameters on airborne bacteria and fungi concentrations [Table 3]. The mean indoor temperature and RH were 21.8°C and 37.3%. However, no correlation was discovered between temperature and airborne bacteria and fungi concentrations. In this regard, this study was conducted only during one season, which may contribute to the minor difference in the indoor values of temperature and RH, furthermore, preventing the detection of any correlation with airborne bacteria and fungi.
Table 4: Spearman's rank correlation coefficient

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Distribution of indoor bacteria and fungi

These findings, in agreement with other studies, indicate that Gram-positive cocci were observed to be the predominant bacteria in all indoor isolates from primary schools.[11],[13],[32] The Staphylococcus bacteria have a human origin and can cause a wide variety of diseases through either toxin production or penetration, particularly affecting the health of children in classrooms.[11] Moreover, Micrococcus have been isolated from the human skin and the environment (soil, plants, and water). The Corynebacterium spp. are often part of the normal human and animal skin flora. Some species of Corynebacterium also occur in the context of nosocomial infections and childhood asthma.[13]

As shown in [Table 5], Penicillium spp. (39.8%), Cladosporium spp. (18.6%), and Aspergillus spp. (16.2%) were the most prevalent fungi within the study. These dominant fungi accounted for about 75% of the total airborne fungi in the classrooms. The prevalent fungal genera in this study have also been identified in other studies.[19],[20],[31],[33] These three fungal species are usually the most dominant in indoor environments of schools, although the climate condition and location are the main effective factors.[34] On the other hand, they have also been considered the most important allergenic molds, having harmful effects on human health, particularly in schoolchildren.[35]
Table 5: The percentage of culturable bacterial and fungal genera in indoor environment of two primary schools (n=96)

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  Conclusion Top

The findings showed that the airborne bacteria were higher than the airborne fungi in the total samples, whether obtained from the I/O environment. The mean I/O ratio of bacteria was higher than 1; therefore, it seems that the main source of airborne bacteria in the two schools are from indoor sources. However, there was no significant difference found between I/O fungi levels in the two primary schools (P > 0.05). The comparisons of indoor airborne microorganism in the two schools studied supported the fact that the density of students, age of the building, and the type of ventilation are the main factors contributing to the bioaerosol concentration. The results demonstrated that airborne bacteria have a weak- and moderate-positive correlation with PM2.5 and PM10, respectively. In addition, there was a positive correlation between indoor fungi and PM mass concentrations. Penicillium, Cladosporium, and Aspergillus were the most identified genera of fungi within indoor air. The other founded species included Yeast, Alternaria, Stemphylium, Rhizopus, and Trichoderma. The identification of these species in the indoor environment of primary schools, due to its toxigenic, allergenic, and infectious effect on student health, should be the main concern for future epidemiological studies. Further, Staphylococcus spp., Micrococcus spp., and Bacillus spp. were the most frequently founded indoor bacteria. Comparative analysis of classrooms in the two schools showed that indoor sources and building conditions have a key role in IAQ.


The research was conducted with funds from the Vice-Chancellor of Research of Arak University of Medical Sciences (Research Project # 3079). The authors wish to extend their thanks to the school officials for their assistance during the study.

Ethics code

This article was obtained from a research proposal approved by the Research Ethics Committee of Arak University of Medical Sciences (code IR.ARAKMU.REC.1397.76).

Financial support and sponsorship

Arak University of Medical Sciences, Arak, Iran.

Conflicts of interest

There are no conflicts of interest.

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  [Figure 1]

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]


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