Journal of Environmental and Public Health
Volume 2020 (2020), Article ID 7292198, 8 pages
https://doi.org/10.1155/2020/7292198

Research Article

Environmental Factors and Ventilation Affect Concentrations of Microorganisms in Hospital Wards of Southern Thailand

Nutthajit Onmek,¹ Jinda Kongcharoen,² Ailada Singtong,² Angkana Penjumrus,² and Siripich Junnoo²

¹Faculty of Science and Technology, Bansomdejchaopraya Rajabhat University, Bangkok 10600, Thailand
²Faculty of Science and Industrial Technology, Prince of Songkla University, Surat Thani Campus, Surat Thani 84000, Thailand

Correspondence should be addressed to Jinda Kongcharoen; jinda.suv@psu.ac.th

Received 26 December 2019; Revised 1 May 2020; Accepted 18 May 2020; Published 8 June 2020

Academic Editor: Stefano Capolongo

Copyright © 2020 Nutthajit Onmek et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract.

Hospitals tend to have high density of occupancy. Poor indoor environmental quality in hospital buildings can exacerbate the health problems of patients and also harm visitors and staff. This study investigated the environmental characteristics and ventilation affecting the concentration of microorganisms in multiple-bed hospital wards. The measurements were accomplished by using a biosampler and an open plate method at four wards, different positions of electric fans, and different times. Data were analyzed by t-test and MANOVA. The results revealed that the concentrations of airborne bacteria were higher than the concentrations of fungi. There were significant differences in the concentrations of bacteria and fungi between sampling times and between hospital wards (), while no difference was observed by positions of electric fans. Correlations between the concentrations and other environmental parameters indicate that temperature, number of occupants, and humidity were physical factors associated with the concentrations of microorganisms. In addition, mostly, Gram-positive bacteria were observed. This indicates the conditions in buildings in the tropical climate, and regular housekeeping of all room areas is needed to prevent the growth of airborne contaminants and the related risks to patients, visitors, and staff.

1. Introduction

Hospitals are dynamic environments exposed to various indoor and outdoor environmental sources and can support microbial survival and growth [1–3]. Characterizing the airborne microorganisms in hospital buildings is important. There is an opportunity to spread infections via air by coughing, conversation, laughing, or sneezing. Outbreaks of infectious diseases, such as tuberculosis, measles, and influenza, have been linked with poor microbiological quality of hospital indoor air [4–6]. The presence of nosocomial infectious microorganisms is a source of nosocomial infections in hospitals [7]. These conditions may negatively impact the health of those working in such buildings, and microbial contamination may cause diseases.

Several studies have shown that microbial contamination of indoor air in a hospital is mostly by bacteria and fungi. There is increasing evidence of high airborne concentrations of bacteria in hospitals of Singapore [8]. The wards are potentially risky places for human occupants in a hospital. Investigation of airborne concentrations in different wards of a hospital was carried out in Isfahan, and high levels of airborne bacteria were observed [9]. Previous studies have focused on airborne concentrations of bacteria, while the concentrations of fungi have received less attention. In Thailand, Srion and Nathapindhu [10] found bacteria on about half the sampled surfaces, in Nonsang and Nongbua Lamphu hospitals. Also, seven genera of bacteria and fungi were identified in the air of Khonkaen hospital [11]. The environmental characteristics affecting airborne concentrations have not yet been determined.

The presence of high concentrations of bacteria and fungi within hospital buildings is related to the number of occupants, their activities, and ventilation. Microorganisms that are major causes of illness had increased concentrations in the environment affecting visitors. The high concentration of bacteria or fungi in the air indicates poor ventilation [12, 13]. Proper air ventilation is one method that can reduce the air pollution and the airborne microorganisms in buildings [14,15]. The strategy in the design of the ventilation system of the building is to control the environmental parameters, including air movement, humidity, temperature, air velocity, and cleanliness [1,16]. Generally, the microbiological quality indoors was not higher than the air quality standards and not higher than the outdoors. It is important to reduce and control the concentrations of harmful microorganisms in the air, to ensure good air quality. Several studies [17–19] have indicated that an important aspect in the work environment is the efficiency of the ventilation system and suggested associations among sources, risk factors, and transmission of microorganisms in the hospital and that air cleaning could decrease the concentrations.

In southern Thailand, high temperature and humidity favor airborne microorganisms, and poor indoor air quality in hospitals may cause diverse healthcare-associated infections of patients and staff. Our prior indoor air quality (IAQ) studies have reported on concentrations of Aspergillus spp., Cladosporium spp., and Penicillium spp. in three schools. They indicated that these fungi comprise a risk factor at the school, potentially inducing asthma symptoms in the students [20]. Previous studies [13,21,22] have indicated that air pollution sources (e.g., volatile organic compounds (VOCs), nitrogen dioxide (NO₂), radon, ventilation, formaldehyde, humidity, temperature, and biocontaminants) might have negative effects on indoor air quality in schools. These studies suggested that the importance of natural ventilation could be focused and increased for improving indoor air quality and children’s health. Schools, like hospitals, as communal premises, are critical environments due to the long stay and exposure of vulnerable groups of people. Thus, indoor air quality represents an important issue in both hospitals and schools due to the highest risk of exposure to contaminants, which can accumulate particularly when correct air ventilation is not implemented. Prasomwong et al. [23] sampled a hotel in Thailand, and the measurement results showed that humidity and temperature were both above recommended limits, and poor air quality was detected. Fatigue and general malaise, nasal symptoms, and eye irritation typical in sick building syndrome were found in hotel staff [24]. It can be seen that air quality and air quality management are related to diseases and their symptoms.

There are several factors involving indoor air quality. The environmental factors such as bioaerosol and human activity are also significant. Additionally, based on the risk assessment report of hospitals, the source of chemical emissions from wards is not considered. The study of relevant factors of indoor air quality management in hospitals is one approach to reduce hospital infections. Therefore, this current study aimed at determining the airborne contamination levels in multiple-bed wards of hospitals, where more stringent hygiene standards are pursued. The purposes of this study were to determine concentrations of airborne microorganisms within a large hospital center in southern Thailand. This study also compares the concentrations in different wards, relative to positions of electric fans, and by sampling time. Moreover, the physical environmental characteristics (temperature, humidity, and air velocity) and number of occupants expected to affect the concentrations of microorganisms were investigated.

2. Materials and Methods

2.1. Sample Location

The hospital assessed in this study has a large ward capacity with 800 beds in total, and controlled natural ventilation includes windows, doors, and electric fans. Gola et al. [25] informed that natural ventilation was identified as a strategy of healthier ventilation and natural force of wind-driven pressure through doors, apertures, and windows. The ventilation system of the ward was provided with wall fans for generating air motions. There were 18 electric fans in each ward, with ambient air at 25.4–30.3°C and 72% relative humidity. The four wards were selected for male surgery (A), female surgery (B), male medicine (C), and female medicine (D) with 40 beds. The service hours were from 12:00 am to 8:00 pm. Sampling was done in three daily periods: before (10:00–12:00 am), during (4:00–6:00 pm), and after (8:00–10:00 pm) the patient visits.

2.2. Sample Collection

This study was performed from June to October, which was rainy season, in a hospital. Airborne microorganisms were collected in 3 points relating wind turbulence from electric fans [26,27] to the positions of ceiling fans in the wards: under a ceiling fan, in the blow of a ceiling fan, and far away from the blow of ceiling fans (see Figure 1). The sampling methods were bioaerosol sampling and open plate method. Each position was measured as follows: bioaerosol sampler at 60 cm height from floor level was set up to collect 100 liters and an open plate with culture medium was put at 60 cm height from floor level for 20 minutes.

Figure 1: Sketch and the measurement in the multiple-bed ward.

Trypticase Soy Agar (TSA) was used to cultivate bacteria and Malt Extract Agar (MEA) was used to cultivate fungi. The measurement of temperature and ventilation used a thermoanemometer (Model DF618) and WBGT Heat Stress Monitor was used to measure heat and humidity during each sampling period. The occupant density at the hospital was determined by observing the number of people within a period. The plates were incubated at 37°C for 24–48 hours and 48–72 hours for bacteria and fungi, respectively. Colony-forming units (CFUs) were counted and stained to identify the bacteria as Gram-positive or Gram-negative and to assess the morphology of microorganisms.

2.3. Data Analysis

The airborne microorganism levels were analyzed from descriptive statistics and with t-tests. Multivariate analysis of variance (MANOVA) was carried out to explore group differences among the concentrations of bacteria and fungi by section wards, positions of electric fans, and time. When differences were detected, post hoc comparisons were performed using Tukey’s honestly significant difference (HSD) to test the difference between different pairs of the groups [28]. Differences were considered significant for . The associations among environmental characteristics with concentrations of bacteria and fungi were assessed from Pearson’s correlation coefficients.

3. Results and Discussion

3.1. Concentrations of Bacteria and Fungi by Hospital Wards and Various Times

The average concentration of bacteria in bioaerosols sampler ranged from 335.5 to 928.89 CFU/m³ whereas the open plate had the range 209.69–592.06 CFU/m³. The highest average concentrations of bacteria were detected after the visiting hours in ward D, according to both measurement methods (see Figure 2). Regarding the fungal concentrations, the average concentration from bioaerosols sampler method ranged from 134.50 to 487.22 CFU/m³, and for open plate measurements, the range was 18.82–87.50 CFU/m³. Also, the highest average concentrations of fungi were found in ward D when using bioaerosols sampler, but in ward A when using open plate at nighttime. Airborne microorganisms reached their concentration peak after the patient visits and then gradually decreased until the next visits.

(a)

(b)

Figure 2: Bacterial and fungal concentrations in four hospital wards at three daily periods, measured using (a) biosampler and (b) open plate method.

Our study revealed that the concentrations of airborne bacteria were higher than those of fungi, according to both sampling methods, agreeing in this sense with a prior study [29]. Augustowska and Dutkiewicz [30] indicated as monthly averages, measured in a hospital ward in Poland, 257–436 CFU/m³ of bacteria and 10–96 CFU/m³ of fungi. Our measurement results showed higher airborne concentrations than this prior study of a hospital ward in Poland. However, the measurement results of concentrations of bacteria did not exceed the standard limit of NIOSH set in 2004 and ACGIH (1,000 CFU/m³), and the fungal concentration did not exceed the 500 CFU/m³ of fungi guideline set by WHO in 2000 [31,32]. Higher airborne concentrations during nighttime were observed after the visiting hours (i.e., after 8:00 pm). Most microorganisms tend to come from skin (exudate) infected lesions and dust from human respiration [33], so the concentration of microorganisms tends to be higher indoors than outside of the building. Previous studies have reported greater concentrations indoors than outdoors [31], and our study agrees with this pattern. Ekhaise et al. [7] and Jaffal et al. [34] concluded that the indoor air environment can potentially place patients at greater risk than the outside environment because enclosed spaces can confine aerosols and allow their accumulation to reach infectious levels. The hospital wards have no housekeeping in the room areas after the service hours. This may increase infection risks for the patients. The level of cleanliness in the wards was considered.

3.2. Comparisons of Bacterial and Fungal Concentrations by Hospital Ward and by Sampling Time

The compared differences of bacterial and fungal concentrations at four different wards were statistically significant (), and the results are presented in Table 1. The results from biosampler indicate that the A, B, and C wards did not significantly differ in the mean bacterial concentrations, while ward D had significantly higher mean bacterial concentration than these (Table 2). For fungi, wards A and D had significantly higher mean concentrations than wards B and C. The open plate sampling gave no significant differences in the mean concentrations of bacteria at B and D or between A and C. In the fungal concentrations, A and B did not differ, and neither did C and D. This is because of the same department on the same floor of the hospital, as well as proper ventilation systems.

Table 1: MANOVA of bacterial and fungal concentrations by hospital ward and by sampling time.

Method
Source
Concentration
SS
df
MS
F

Biosampler
Ward
Bacteria
4353266.40
3
1451088.80
13.761
≤0.001

Fungi
774011.64
3
258003.88
6.107
0.001

Time
Bacteria
2766032.18
2
1383016.09
13.116
≤0.001

Fungi
1359200.96
2
679600.48
16.086
≤0.001

Open plate
Ward
Bacteria
2348144.91
3
782714.97
30.900
≤0.001

Fungi
22250.63
3
7416.88
8.688
≤0.001

Time
Bacteria
593514.98
2
296757.49
11.716
≤0.001

Fungi
38179.84
2
19089.92
22.362
≤0.001

Note: ; SS: sum of squares; df: degrees of freedom; MS: mean square.

Table 2: Tukey’s HSD post hoc test results by hospital ward.

Method
Concentration
A
B
C
D

Biosampler
Bacteria
533.81a
550.15a
577.00a
880.19b

Fungi
351.19ab
261.36a
264.67a
318.70b

Open plate
Bacteria
271.56a
454.58b
325.69a
442.55b

Fungi
40.69a
46.67a
57.40b
58.65b

Within each row, different letters indicate statistically significant differences, based on Tukey’s HSD multiple comparison test.

There were significant differences in the mean fungal concentrations between the time periods (). The highest concentrations were measured during and after patient visits. Both bacterial and fungal concentrations were comparatively lower before the visiting time than at other observation periods (Table 3). This might be because of the low night temperatures and high humidity. The high concentrations during and after visits could alternatively be attributed to the visitors. The results showed that there was no significant difference between the bacterial and fungal concentrations and the positions of electric fans. This study also revealed that the occurrence of air fluctuations and turbulence from electric fans did not affect exposure levels. The results disagree with the findings of a previous study [26] claiming that microorganism contamination increased with the ambient air exchange rate when the fan blew air downwards. Air quality inside was very similar to air quality outside, indicating that there was good natural ventilation quality implemented for the building.

Table 3: Tukey’s HSD post hoc test results by time.

Method
Concentration
Before
During
After

Biosampler
Bacteria
479.59a
675.14b
749.05b

Fungi
214.19a
309.86b
413.92c

Open plate
Bacteria
326.06a
376.89b
418.79b

Fungi
38.79a
50.61b
62.50c

Within each row, different letters indicate statistically significant differences, based on Tukey’s HSD multiple comparison test.

3.3. Environmental Characteristics and Concentrations of Airborne Bacteria and Fungi

The average temperature, air velocity, and humidity given by biosampler were 27.068 ± 1.14°C, 0.84 ± 0.53 m/s, and 72.09 ± 0.287%, respectively, whereas the average temperature, air velocity, and humidity at the open plates were 27.21 ± 1.27°C, 0.67 ± 0.50 m/s, and 72.16 ± 0.66%, respectively. The high humidity, velocity, and air temperature exceed the indoor air quality standards by WHO and ASHRAE 55 [35, 36]. A summary of the concentrations and environmental characteristics is shown in Tables 4 and 5.

Table 4: Summary of the average bacterial and fungal concentrations and other key environmental characteristics by hospital ward.

Method

A
B
C
D
Recommended level

Biosampler
Bacteria (CFU/m³)
533.81
550.15
577.00
880.19
<1,000 FU/m³

Fungi (CFU/m³)
351.19
261.36
264.67
318.70
<500 FU/m³

Temperature (°C)
27.17†
27.09†
27.18†
26.83†
22–26.1°C

Air velocity (m/s)
0.719†
0.832†
0.942†
0.817†
<0.25 m/s

Humidity (%)
72.00†
72.33†
72.00†
72.00†
30–60% RH

Open plate
Bacteria (CFU/m³)
271.56
454.58
325.69
442.55
<1,000 FU/m³

Fungi (CFU/m³)
40.69
46.67
57.40
58.65
<500 FU/m³

Temperature (°C)
27.27†
27.36†
27.19†
27.05†
22–26.1°C

Air velocity (m/s)
0.556†
0.698†
0.668†
0.741†
<0.25 m/s

Humidity (%)
72.25†
72.05†
72.33†
72.00†
30–60% RH

Remark: NIOSH, 2004; WHO, 2000, ASHRAE 55, 2004; †not in compliance with standard.

Table 5: Summary of the average bacterial and fungal concentrations and other key environmental characteristics by hospital time.

Method

Before
During
After
Recommended level

Biosampler
Bacteria (CFU/m³)
479.59
675.14
749.05
<1,000 FU/m³

Fungi (CFU/m³)
214.19
309.86
413.92
<500 FU/m³

Temperature (°C)
27.662†
26.553†
26.99†
22–26.1°C

Air velocity (m/s)
0.814†
0.808†
0.888†
<0.25 m/s

Humidity (%)
72.00†
72.00†
72.27†
30–60% RH

Open plate
Bacteria (CFU/m³)
326.06
376.89
418.79
<1,000 FU/m³

Fungi (CFU/m³)
38.79
50.61
62.50
<500 FU/m³

Temperature (°C)
28.039†
26.580†
27.022†
22–26.1°C

Air velocity (m/s)
0.701†
0.622†
0.678†
<0.25 m/s

Humidity (%)
72.04†
72.18†
72.26†
30–60% RH

Remark: NIOSH, 2004; WHO, 2000, ASHRAE 55, 2004; †not in compliance with standard.

Concentrations of airborne bacteria and fungi were positively linked with the number of people in the ward (Table 6). Temperature and humidity affect fungal concentrations significantly. Using the open plate data, a significant negative correlation was observed between the fungal concentrations and temperature. In addition, fungal concentrations were positively correlated with humidity given by biosampler. Normally, fungi grow the best in warmth and high humidity [2]. In this study, patient rooms had a humid and warm climate, with a humidity of over 60% and a temperature of about 27°C. The high temperatures suggest that air conditioning was not much in use. It is probably too expensive, as it would be to dehumidify the air.

Table 6: Correlations between the concentrations and other environmental characteristics.

Factor
Biosampler
Open plate

Bacteria
Fungi
Bacteria
Fungi

Temperature
0.076
−0.012
0.045
−0.162

Number
0.405
0.461
0.121
0.123

Air velocity
0.006
0.068
0.029
0.049

Humidity
0.072
0.149
0.050
0.026

Note: ; .

The number of occupants, humidity, and temperature are physical factors associated with bacterial and fungal concentrations; however, these were not significantly affected by air velocity. Previous studies have indicated that the density of occupants is the key factor influencing the airborne concentrations in hospital wards [7,33,37]. Our study agrees with these previous studies. Moreover, Zemouri et al. [38] demonstrated that the daily cleaning operations in the hospital were related to the presence of aerosols. Normally, this area was cleaned twice per day (in the morning and in the afternoon). This cleaning frequency may not be a sufficient standard for safety. The management of cleaning procedures and the awareness of cleanings should be considered. Furthermore, a correlation between the number of people and the air volume was reported [39]. Organizing patient visits in separate spaces, with distancing to prevent infections, and control of crowding seems reasonable. Further, for example, smartphones could be used for patient communications with family members during hospital visits. The results show that the fungal presence was very high, and aside from people, this may be attributed to air ventilation and air conditioning. Most of the bacteria related to patients can be released in a hospital environment and can be breathed in by visitors and staff [9,40]. This study contrasted with the findings on temperature by Park et al. [1] who reported that the temperature significantly influenced the concentration of bacteria. No relationships between bacterial or fungal concentrations and air velocity were found.

3.4. Concentrations of Gram-Positive and Gram-Negative Bacteria

Our results indicate that Gram-positive cocci and rod-shaped bacteria were present in significantly larger numbers than the Gram-negative bacteria throughout the experiment. It has been reported that Gram-positive bacteria are more tolerant to environmental stresses than Gram-negative bacteria. The cell walls of Gram-negative bacteria are thinner and less compact, whereas in Gram-positive cells peptidoglycan forms a thick compact cell wall, which is the outermost structure of Gram-positive cells [41]. Airborne Gram-positive cocci are most frequently detected indoors in hospitals [42]. The samples collected were analyzed by microscopy. The overall culturable fungi were Aspergillus spp., Penicillium spp., Cladosporium spp., Alternaria spp., and Curvularia spp. Aspergillus spp. was the most frequently identified species in this study, and these fungal pathogens are associated with airway diseases [43]. It has been reported that Aspergillus spp. are the most common fungi found in various environments, such as food, water, and plants. Warmth with high moisture and lack of sunlight is favorable for their growth [44,45]. A previous study reported that Aspergillus spp. caused aspergillosis and allergic aspergillosis syndrome [11,46–48]. A study on concentrations of airborne microorganisms indicated that most fungi were found in a food center (Penicillium spp., Aspergillus spp., and Cladosporium spp.) [49]. However, these did not cause illnesses or health problems, possibly due to our immune system. Moreover, Penicillium spp. and Aspergillus spp. are common fungi found in buildings and are not considered pathogens. Nevertheless, these fungi might cause allergy, asthma, or respiratory illnesses. Hameed et al. [29] also reported on the diversity of airborne bacteria and fungi in Helwan city of Egypt, where the fungi most found were Aspergillus, Cladosporium, and Penicillium, in this order. In addition, Aspergillus spp., Penicillium spp., Cladosporium spp., Curvularia spp., and Alternaria spp. were found indoors as microbiological contaminants in the air, at a university building [50]. Our results overall agree with these prior studies. Some particular fungi are linked with the sick hospital syndrome, causing allergenic diseases nonspecifically, and come from construction dust or dust accumulated within ventilation [50–53]. Most invasive infections are acquired from indoor air [54]. The prevention and control of microorganism growth can reduce the human health risks from airborne microorganisms. To reduce concentrations of airborne contaminants, it is necessary to implement some control measures in wards, such as using air purifiers and sterilization using ozone.

4. Conclusions

Based on our measurements in a large hospital, located in southern Thailand, the airborne bacterial concentrations were significantly higher than the fungal concentrations. The general air quality characteristics indicated that bacteria can grow and are more prevalent than mold. The airborne bacterial and fungal concentrations did not exceed the standard limits, respectively, set by the NIOSH and the WHO. This study also revealed that the occurrence of air fluctuations and turbulence from electric fans had no effects on the level of exposure. Air quality inside is very similar to air quality outside, indicating good natural ventilation quality in the building. The five types of fungi found were Aspergillus spp., Penicillium spp., Cladosporium spp., Alternaria spp., and Curvularia spp. In general, these fungi are mostly observed in high-risk areas such as schools, theatres, and hospitals. Exposure to these contaminants may affect the respiratory system. The results suggest that the number of occupants in a building is positively associated with the airborne bacterial concentrations. Additionally, high humidity and high temperature were observed in multiple-bed hospital wards. This might be because of the tropical climate in the area of this study. The quality of air in the wards was better early in the day than later after the morning has passed. Room cleaning should be performed after patient visits, to decrease airborne bacteria. Cleaning and housekeeping of all room areas need to be regular to decrease the airborne contamination in all areas for patients, visitors, and staff. Nosocomial infections with indoor air quality in the buildings will be investigated in related future studies. In further research on factors that affect indoor air quality, chemical factors should be considered.

Data Availability

The data used to support the findings of this study are available from the corresponding author upon request.

Conflicts of Interest

The authors declare that there are no conflicts of interest.

Acknowledgments

The authors of this article would like to thank Prince of Songkla University, Surat Thani Campus, for funding support. The authors would like to thank Associate Professor Dr. Seppo Karrila for his valuable suggestions to improve the manuscript.

References

D.-U. Park, J.-K. Yeom, W. J. Lee, and K.-M. Lee, “Assessment of the levels of airborne bacteria, gram-negative bacteria, and fungi in hospital lobbies,” International Journal of Environmental Research and Public Health, vol. 10, no. 2, pp. 541–555, 2013.

C. Ponce-Caballero, M. Gamboa-Marrufo, M. López-Pacheco et al., “Seasonal variation of airborne fungal propagules indoor and outdoor of domestic environments in Mérida, Mexico,” Atmósfera, vol. 26, no. 3, pp. 369–377, 2013.

J. Božić, P. Ilić, and S. Ilić, “Indoor air quality in the hospital: the influence of heating, ventilating and conditioning systems,” Brazilian Archives of Biology and Technology, vol. 62, 2019.

S. Bhattacharyya, A. Sarfraz, and N. Jaiswal, “Hospital indoor air microbial quality: importance and monitoring,” Annali di Igiene, vol. 6, no. 2, pp. 154–156, 2015.

N. Manorat and N. Sinthununsakul, “Indoor air quality and microbial indoor air quality in tertiary care hospital,” Journal of Preventive Medicine Association of Thailand, vol. 9, no. 2, pp. 232–241, 2019.

R. L. Górny and J. Dutkiewicz, “Bacterial and fungal aerosols in indoor environment in central and eastern European countries,” The Annals of Agricultural and Environmental Medicine, vol. 9, no. 1, pp. 17–23, 2002.

F. O. Ekhaise, E. E. Isitor, O. Idehen, and A. O. Emoghene, “Airborne microflora in the atmosphere of an hospital environment of University of Benin Teaching Hospital (UBTH), Benin City, Nigeria,” World Journal of Agricultural Sciences, vol. 6, no. 1, pp. 166–170, 2010.

J. P. Obbard and L. S. Fang, “Airborne concentrations of bacteria in a hospital environment in Singapore,” Water, Air, and Soil Pollution, vol. 144, no. 1–4, pp. 333–341, 2003.

S. H. Mirhosseini, M. Nikaeen, H. Khanahmad, and A. Hassanzadeh, “Occurrence of airborne vancomycin-and gentamicin-resistant bacteria in various hospital wards in Isfahan Iran,” Advanced Biomedical Research, vol. 5, no. 1, p. 143, 2016.

T. Srion and G. Nathapindhu, “Type and quantity of microorganism on the surface of the device with in Nonsang Hospital and Nongbua Lamphu Hospital, Nongbua Lamphu Province,” Mahasarakham Hospital Journal, vol. 12, no. 2, pp. 69–80, 2015.

K. Sungkajuntranon, N. Chaiear, P. Sribenjalux, and P. Chuaybamroong, “Airborne bacteria and fungi in the hospital and the sampling method comparison,” Thailand Journal of Health Promotion & Environment, vol. 29, no. 4, pp. 113–124, 2006.

A. Bennett and S. Parks, “Microbial aerosol generation during laboratory accidents subsequent risk assessment,” Journal of Applied Microbiology, vol. 100, no. 4, pp. 658–663, 2006.

P. N. Pegas, M. G. Evtyugina, C. A. Alves et al., “Outdoor/indoor air quality in primary schools in Lisbon: a preliminary study,” Quimica Nova, vol. 33, no. 5, pp. 1145–1149, 2010.

C. B. Beggs, K. G. Kerr, C. J. Noakes, E. A. Hathway, and P. A. Sleigh, “The ventilation of multiple-bed hospital wards: review and analysis,” American Journal of Infection Control, vol. 36, no. 4, pp. 250–259, 2008.

Q. Zhou, H. Qian, and L. Liu, “Numerical investigation of airborne infection in naturally ventilated hospital wards with central-corridor type,” Indoor and Built Environment, vol. 27, no. 1, pp. 59–69, 2018.

Z. Liu, S. Ma, G. Cao, C. Meng, and B.-J. He, “Distribution characteristics, growth, reproduction and transmission modes and control strategies for microbial contamination in HVAC systems: a literature review,” Energy and Buildings, vol. 177, pp. 77–95, 2018.

E. Brągoszewska, “Exposure to bacterial and fungal aerosols: microorganism indices in a waste-sorting plant in Poland,” International Journal of Environmental Research and Public Health, vol. 16, no. 18, p. 3308, 2019.

U. Moscato, A. Borghini, and A. A. Teleman, “HVAC Management in Health Facilities,” in Indoor Air Quality in Healthcare Facilities, pp. 95–106, SpringerBriefs in Public Health, Berlin, Germany, 2017.

M. S. Mousavi, M. Hadei, M. Majlesi et al., “Investigating the effect of several factors on concentrations of bioaerosols in a well-ventilated hospital environment,” Environmental Monitoring and Assessment, vol. 191, no. 7, 2019.

N. Thongngern, S. Nakkruen, N. Onmek, and J. Kongcharoen, “Spore concentration of Aspergillus, Cladosporium and Penicillium potentially inducing asthma disease in student age 10–15 years,” Thammasat Journal of Science and Technology, vol. 24, no. 1, pp. 126–138, 2016.

A. Azara, M. Dettori, P. Castiglia et al., “Indoor radon exposure in Italian schools,” International Journal of Environmental Research and Public Health, vol. 15, no. 4, p. 749, 2018.

I. Vassura, E. Venturini, E. Bernardi, F. Passarini, and G. Settimo, “Assessment of indoor pollution in a school environment through both passive and continuous samplings,” Environmental Engineering and Management Journal, vol. 14, no. 7, pp. 1761–1770, 2015.

M. Prasomwong, W. Ho, T. Boonchua, J. Kongcharoen, and N. Onmek, “Indoor air quality in hotel buildings & sick building syndrome of hotel staff, Surat Thani Province,” Journal of Science & Technology, Ubon Ratchathani University, vol. 20, no. 3, pp. 64–73, 2018.

J. Kongcharoen, N. Onmek, and S. Karrila, “Factors affecting sick building syndrome among hotel staff,” Suranaree Journal of Science and Technology, vol. 26, no. 1, pp. 93–100, 2019.

M. Gola, G. Settimo, and S. Capolongo, “Indoor air quality in inpatient environments: a systematic review on factors that influence chemical pollution in inpatient wards,” Journal of Healthcare Engineering, vol. 2019, Article ID 8358306, 20 pages, 2019.

S. Zhu, J. Srebric, S. N. Rudnick, R. L. Vincent, and E. A. Nardell, “Numerical modeling of indoor environment with a ceiling fan and an upper-room ultraviolet germicidal irradiation system,” Building and Environment, vol. 72, pp. 116–124, 2014.

E. Canepa, A. Cattanei, F. M. Zecchin, and D. Parodi, “Instantaneous PIV data related to the leakage flow of a low-speed axial-flow fan with rotating shroud,” Data in Brief, vol. 24, Article ID 103895, 2019.

M. E. Hall, E. H. Blair, S. M. Smith, and J. D. Gorski, “Development of a theory-based safety climate instrument,” Journal of Safety, Health & Environmental Research, vol. 9, no. 1, pp. 58–69, 2013.

A. A. A. Hameed, M. I. Khoder, S. Yuosra, A. M. Osman, and S. Ghanem, “Diurnal distribution of airborne bacteria and fungi in the atmosphere of Helwan area, Egypt,” Science of the Total Environment, vol. 407, no. 24, pp. 6217–6222, 2009.

M. Augustowska and J. Dutkiewicz, “Variability of airborne microflora in a hospital ward within a period of one year,” Annals of Agricultural and Environmental Medicine, vol. 13, no. 1, pp. 99–106, 2006.

M. F. Yassin and S. Almouqatea, “Assessment of airborne bacteria and fungi in an indoor and outdoor environment,” International Journal of Environmental Science & Technology, vol. 7, no. 3, pp. 535–544, 2010.

P. A. Jensen and M. P. Schafer, Sampling and Characterization of Bioaerosols, National Institute for Occupational Safety and Health (NIOSH), Cincinnati, OH, USA, 1998.

C. Thunyasirinon, P. Sribenjalux, and P. Chuaybamroong, “Comparison of a six-stage and a single stage viable andersen impactor (N6) for airborne microbe sampling,” Khon Kaen University Journal (Graduate Studies), vol. 7, no. 3, pp. 107–117, 2007.

A. A. Jaffal, I. M. Banat, A. A. E. Mogheth, N. Nsanze, A. Bener, and A. S. Ameen, “Residential indoor airborne microbial populations in the United Arab Emirates,” Environment International, vol. 23, no. 4, pp. 529–533, 1997.

ASHRAE Standard 55, Thermal Environmental Conditions for Human Occupancy, ASHRAE, Atlanta, GA, USA, 2004, https://en.wikipe-dia.org/wiki/Thermal_comfort.

ASHRAE Standard 62.1, Ventilation for Acceptable Indoor Air Quality, ASHRAE, Atlanta, GA, USA, 2007, http://www.mintie.com-/assets/pdf/education/ASHRAE%2062.1-2007.pdf.

O. E. Agbagwa and S. A. Onyemaechi, “Microbiological quality of indoor air of a general hospital and a health center in rivers state Nigeria,” International Journal of Current Microbiology and Applied Sciences, vol. 3, no. 12, pp. 424–431, 2014.

C. Zemouri, H. D. Soet, W. Crielaard, and A. Laheij, “A scoping review on bio-aerosols in healthcare & the dental environment,” PLoS One, vol. 12, no. 5, Article ID e0178007, 2017.

A. D’Amico, M. T. Montagna, G. Caggiano et al., “Observational study on hospital building heritage and microbiological air quality in the orthopedic operating theater: the IM.PA.C.T. Project,” Annali di Igiene, vol. 31, no. 5, pp. 482–495, 2019.

J. Fiegel, R. Clarke, and D. A. Edwards, “Airborne infectious disease and the suppression of pulmonary bioaerosols,” Drug Discovery Today, vol. 11, no. 1-2, pp. 51–57, 2006.

S. Wongvijitsuk, “Hazard and control of airborne microorganisms in industrial plant,” Huachiew Chalermprakilet University, vol. 13, no. 26, pp. 65–80, 2010.

S. C. Verde, S. M. Almeida, J. Matos et al., “Microbiological assessment of indoor air quality at different hospital sites,” Research in Microbiology, vol. 166, no. 7, pp. 557–563, 2015.

D. A. Enoch, H. A. Ludlam, and N. M. Brown, “Invasive fungal infections: a review of epidemiology and management options,” Journal of Medical Microbiology, vol. 55, no. 7, pp. 809–818, 2006.

P. Choomsri, Relationship between Ventilation Performance and Airborne Microbes in a Hospital, Master of Public Health Program, Khon Kaen University, Khon Kaen, Thailand, 2006.

C. A. Ramos, C. Viegas, S. C. Verde, H. T. Wolterbeek, and S. M. Almeida, “Characterizing the fungal and bacterial microflora and concentrations in fitness centres,” Indoor and Built Environment, vol. 25, no. 6, pp. 872–882, 2016.

P. Choomsri, B. Suphim, and O. Parnpeth, “Types and quantities of airborne fungi in Loei rajabhat university library,” KKU Journal for Public Health Research, vol. 8, no. 2, pp. 1–9, 2015.

Y. Fukutomi and M. Taniguchi, “Sensitization to fungal allergens: resolved and unresolved issues,” Allergology International, vol. 64, no. 4, pp. 321–331, 2015.

E. Brągoszewska, “The dose of fungal aerosol inhaled by workers in a waste-sorting plant in Poland: a case study,” International Journal of Environmental Research and Public Health, vol. 17, no. 1, p. 177, 2020.

A. Rajasekar and R. Balasubramanian, “Assessment of airborne bacteria and fungi in food courts,” Building & Environment, vol. 46, no. 10, pp. 2081–2087, 2011.

M. Stryjakowska-Sekulska, A. Piotraszewska-Pajak, A. Szyszka, M. Nowicki, and M. Filipiak, “Microbiological quality of indoor air in university rooms,” Polish Journal of Environmental Studies, vol. 16, no. 4, pp. 623–632, 2007.

A. N. S. Wahab, M. F. Khamidi, and M. R. Ismail, “An investigation of mould growth in tropical climate buildings,” in Proceedings of the 2013 IEEE Business Engineering & Industrial Applications Colloquium, pp. 316–321, Langkawi, Malaysia, April 2013.

P. Luksamijarulkul, N. Somjai, N. Nankongnap, A. Pataitiemthong, P. Kongtip, and S. Woskie, “Indoor air quality at different sites of a governmental hospital, Thailand,” Nursing and Palliative Care, vol. 4, 2019.

D. D’Alessandro and G. M. Fara, “Hospital environments and epidemiology of healthcare-associated infections,” in Indoor Air Quality in Healthcare Facilities, pp. 41–52, SpringerBriefs in Public Health, Berlin, Germany, 2017.

S. A. Sajjadi, D. Ketabi, and F. Joulaei, “Fungal assessment of indoor air quality in wards and operating theatres in an organ transplantation hospital,” Health Scope, vol. 7, no. 4, 2018.