Indoor air quality should be a matter of daily concern, because most people spend time indoors [1]. Building occupants are exposed to airborne particulate matter including bioaerosols [2]. Quality indoor air is imperative for hospitals or health care facilities, where the air is potentially contaminated with microorganisms because poor air quality can be a potential source of various nosocomial diseases. Exposure to indoor airborne bacteria and fungi may impact the health of people in affected areas [3]. Studies from Thailand [4, 5], Taiwan [6], Singapore [7], and Egypt [8] have shown that indoor airborne bacterial and fungal concentrations in hospitals exceeded the recommended levels of airborne microorganisms in the buildings (bacteria and fungi ≤500 colony-forming units (cfu)/m3) [9]. A study of air quality at a hospital found that wards accommodating patients at risk for tuberculosis (TB) had high bacterial and fungal counts [5]. Long-term surveillance of airborne bioaerosols in health care facilities is required to protect both patients and health care workers [10].
TB, a respiratory disease caused by
The aims of the present study were to determine the concentrations and sizes of airborne bioaerosols (bacteria and fungi) and their contributing factors in TB high-risk areas in 7 large health care facilities in central Thailand. Specifically, we sought to determine the indoor-to-outdoor (I/O) ratio of airborne bioaerosols and examine the relationship between the concentration of indoor airborne bioaerosols and environmental parameters of the areas such as air change rate, room temperature and relative humidity, type of ventilation, daily number of occupants, daily number of active TB patient(s), and daily number of coughs by TB patients not wearing a protective mask.
This cross-sectional study was conducted in 7 large health care facilities in Bangkok and nearby in central Thailand: 2 university hospitals, 1 super tertiary care hospital, 3 regional/general hospitals, and 1 National Infectious Disease Institute. The TB high-risk areas in each health care facility targeted for this study were TB outpatient clinics, TB inpatient wards, emergency departments, and bronchoscopy units. Data were collected from January to December 2015.
The present study was approved by an ethics committee at each site. For the 2 university hospitals, the institutional review board (IRB) approval numbers were 795/2014 (IRB No. 484/57 Chulalongkorn University, Faculty of Medicine) and MURA251/2015 (Faculty of Medicine Ramathibodi Hospital, Mahidol University). For the super tertiary care hospital, the IRB approval number was 001/2015 (Phra Nakhon Si Ayutthaya Hospital). For the 3 regional/general (tertiary care) hospitals, the IRB approval numbers were 035/2016 (Rajavithi Hospital), 046/2015 (Pranangklao Hospital), and 003/2015 (Saraburi Hospital). For the Thai National Infectious Disease Institute, the IRB approval number was RO18b/2015.
Air was sampled from 99 indoor and 28 outdoor areas including TB clinics (18 indoor and 7 outdoor areas), TB wards (47 indoor and 7 outdoor areas), emergency departments (27 indoor and 7 outdoor areas), and bronchoscopy units (7 indoor and 7 outdoor areas). We collected 6 air samples for each area. A total of 1,524 samples (1,188 indoor and 336 outdoor) were collected. Equal numbers of blank samples were also collected from the same areas. Air samples were collected using a six-stage Andersen cascade impactor for viable aerosols (Thermo Scientific) at a flow rate of 28.3 L/min [15] and a sampling time of 10 min to determine the bioaerosol concentrations and their size distribution. The aerodynamic diameter ranges for each stage in the Andersen cascade impactor were >7.0 μm (stage 1), 4.7–7.0 μm (stage 2), 3.3–4.7 μm (stage 3), 2.1–3.3 μm (stage 4), 1.1–2.1 μm (stage 5), and 0.65–1.1 μm (stage 6). Air samplers were disinfected with 70% ethanol before collecting the samples, and air-sampling devices were placed within 1 m of the patients and 1.5 m above the floor to represent a human breathing zone. The outdoor air samples were collected on the same day as the indoor samples. Tryptic soy agar (incubation at 37°C for 2 days) was used to culture airborne bacteria. Sabouraud dextrose agar (incubation at 25°C for 5 days) was used to culture airborne fungi [16]. The concentrations of microorganisms are expressed as cfu/m3 and calculated as follows: the concentrations of microorganisms of each Andersen impactor stage (cfu/m3) = (cfu at the stage × 103)/(sampling flow rate (L/min) × (sampling time (min)) [17].
Environmental parameters of interest in this study were air change rate (h–1), temperature (°C), and relative humidity (%). Air change rate was measured using a standard method to determine air change in a single zone by means of a tracer gas dilution [9], and temperature and relative humidity were measured using an AQ 200 Indoor Air Quality Meter (Kimo Instruments). Information about other potential contributing factors, such as daily number of patient(s) with active TB in each area, daily number of occupants in each area and department, and type of ventilation system, was obtained from the TB health care workers working in each area. The daily number of coughs by TB patient(s) not wearing a protective mask in each area was obtained from a TB patient interview and by direct observation by one of the authors during the 8 h of air sample collection per day. In addition, information about the presence of TB infection control measures was also collected using a set of structured questionnaires modified from those suggested by the WHO [18]; this questionnaire assessed infection control policy and management (11 items), administrative control (15 items), environmental control (2 items), and personal protection (2 items). The result was then summarized as the nosocomial TB prevention score with a total possible score of 30, and a score of 0–10 was considered as low, 11–20 moderate, and 21–30 high.
In describing continuous variables (airborne bioaerosol concentration, air change rate, temperature and relative humidity, TB infection control score, daily number of active TB patients in each area, daily number of coughs by TB patient(s) not wearing a protective mask in each area, and daily number of occupants in each area), the mean and standard deviation (SD) or median and 25th and 75th percentiles or interquartile range (IQR) are used for variables with normal or skewed distributions, respectively. Categorical variables (types of department and ventilation system) are presented as frequency and percentage. An unpaired
The association between indoor airborne bioaerosol concentration and potential contributing factors (potential environmental attributors and ventilation systems) was initially examined by linear regression. Subsequently, multiple linear regression was conducted. Backward stepwise selection was used in the statistical modeling by including variables with
In TB high-risk areas, the median air change rate was 6.2 h–1, temperature was 27.9°C, and relative humidity was 62.2%, while the daily number of occupants in each area was 10.0, daily number of patient(s) with active TB in each area was 1.0, and daily number of coughs by TB patient(s) not wearing a protective mask in each area was 0.0. The TB infection control scores for most areas were high (21–30 of the total score of 30). The ventilation systems used in the areas were mostly split-type (44%) and central-type air conditioners (48%;
Indoor bacterial and fungal concentrations in TB high-risk areas based on environmental parameters and other potential contributors
Data for TB high-risk areas Median (IQR), unless indicated otherwise | Emergency department (n = 27) | TB ward (n = 47) | Bronchoscopy unit (n = 7) | TB clinic (n = 18) | All areas (n = 99) |
---|---|---|---|---|---|
Air change rate (h–1) | 6.0 (5.9–6.2) | 6.7 (6.1–7.3) | 7.0 (5.2–7.1) | 6.3 (5.2–7.0) | 6.2 (6.0–7.1) |
Temperature (°C) | 25.6 (25.1–27.1) | 31.5 (29.1–32.0) | 24.6 (24.2–25.7) | 28.3 (26.3–30.7) | 27.9 (25.3–31.5) |
Relative humidity (%) | 61.7 (60.0–63.7) | 66.7 (57.8–70.1) | 57.2 (53.8–66.3) | 68.2 (58.2–70.6) | 62.2 (57.8–70.0) |
TB infection control score† | 24.0 (21.0–28.0) | 26.0 (22.0–28.0) | 21.0 (14.0–25.0) | 27.0 (23.8–28.0) | 26.0 (22.0–28.0) |
Good level, frequency (%) | 23.0 (85.2) | 37.0 (78.7) | 4.0 (57.1) | 16.0 (88.9) | 80.0 (80.8) |
Moderate level, frequency (%) | 4.0 (14.8) | 10.0 (21.3) | 3.0 (42.9) | 2.0 (11.1) | 19.0 (19.2) |
Daily number of occupants in each area | 35.0 (15.0–60.0) | 7.0 (5.0–10.0) | 6.0 (5.0–15.0) | 20.0 (6.8–69.3) | 10.0 (5.0–30.0) |
Daily number of active TB patient(s) in each area | – | 1.0 (1.0–1.0) | 1.0 (0.0–1.0) | 2.0 (1.0–7.0) | 1.0 (0.0–1.0) |
Daily number of coughs by TB patient(s) not | 1.0 (0.0–1.0) | 3.0 (1.0–3.0) | – | 0.0 (0.0–1.0) | |
wearing a protective mask in each area | |||||
Ventilation system | |||||
Natural ventilation, frequency (%) | 2.0 (7.4) | 37.0 (78.7) | – | 8.0 (44.4) | 47.0 (47.5) |
Central-type air conditioner, frequency (%) | 12.0 (44.4) | – | – | 7.0 (38.9) | 19.0 (19.2) |
Split-type air conditioner, frequency (%) | 13.0 (48.2) | 10.0 (21.3) | 7.0 (100.0) | 3.0 (16.7) | 33.0 (33.3) |
Indoor airborne bacteria (cfu/m3)‡ | 691.0 ± 79.61 | 533.8 ± 132.50 | 567.9 ± 208.55 | 627.2 ± 124.60 | 596.1 ± 140.90 |
Indoor airborne fungi (cfu/m3)‡ | 618.4 ± 108.03 | 464.7 ± 130.11 | 478.1 ± 178.01 | 539.7 ± 129.59 | 521.2 ± 142.20 |
IQR, interquartile range; SD, standard deviation; TB, tuberculosis
†Good level = score 21–30 score; moderate level = score 11–20; poor level = score 0–10
‡cfu/m3: colony forming unit per cubic meter, mean ± SD
The mean indoor (all areas) airborne bacterial and fungal concentrations were 596.1 and 521.2 cfu/m3, respectively, and the mean outdoor airborne bacterial and fungal concentrations were 496.5 and 650.1 cfu/m3, respectively. The emergency department had the highest mean indoor and outdoor concentrations of airborne bacteria and fungi; the concentrations were higher than other areas studied (indoors 691.0 cfu/m3 and 618.4 cfu/m3 for bacteria and fungi, and outdoors 523.5 cfu/m3 and 721.4 cfu/m3, respectively). The TB wards had the lowest mean concentrations of airborne bacteria and fungi (indoors 533.8 cfu/m3 and 464.7 cfu/m3, and outdoors 461.5 cfu/m3 and 583.0 cfu/m3, respectively) as shown in
The indoor airborne bacterial concentrations were significantly higher than the outdoor airborne bacterial concentrations (I/O = 1.2,
The size distributions of airborne bacteria and fungi peaked at stage 3–4 (2.1–4.7 μm), and their median concentrations were at 245.6 and 219.1 cfu/m3, respectively. The median concentrations of airborne bacteria and fungi for all size distributions were highest in the emergency departments and lowest in bronchoscopy units as shown in
The linear regression found that the potential contributing factors for indoor airborne bioaerosol concentrations were environmental parameters and other potential contributors, including ventilation systems as summarized in
Comparison of factors and indoor airborne bioaerosol concentration using linear regression
Factor | Bacteria (cfu/m3)† | Fungi (cfu/m3)† | ||||
---|---|---|---|---|---|---|
B† | 95% CI (lower, upper) | Ba | 95% CI (lower, upper) | |||
Air change rate (h–1) | –71.30 | –87.54, –55.06 | <0.001*** | –71.64 | –88.09, –55.19 | <0.001*** |
Temperature (°C) | –5.54 | –14.77, 3.69 | 0.24 | –4.36 | –13.70, 4.99 | 0.36 |
Relative humidity (%) | 6.66 | 2.20, 11.12 | 0.004** | 6.07 | 1.53, 10.61 | 0.009** |
TB infection control score | –3.39 | –10.48, 3.07 | 0.35 | –4.77 | –11.89, 2.36 | 0.19 |
Daily number of patients with active TB (in each area) | –8.69 | –19.24, 1.85 | 0.11 | –9.03 | –19.66, 1.61 | 0.095 |
Daily number of occupants in each area | 1.81 | 0.75, 2.87 | 0.001** | 1.82 | 0.75, 2.89 | 0.001** |
Daily number of coughs by TB patients | 14.81 | 2.14, 27.47 | 0.022* | 10.40 | –2.56, 23.37 | 0.14 |
(not wearing a protective mask) Department‡ | ||||||
Emergency department | 130.49 | 72.77, 188.22 | <0.001*** | 133.59 | 75.50, 191.67 | <0.001*** |
TB clinic and bronchoscopy unit | 19.42 | –45.48, 84.33 | 0.55 | 1.68 | –63.95, 67.30 | 0.96 |
Ventilation system§ | ||||||
Central-type air conditioner | 166.08 | 102.63, 229.53 | <0.001*** | 164.41 | 100.03, 228.78 | <0.001*** |
Split-type air conditioner | –46.27 | –105.46, 12.93 | 0.12 | –53.67 | –113.17, 5.84 | 0.077 |
†The mean indoor airborne bacteria and fungi (cfu/m3 = colony forming unit per cubic meter)
‡Emergency department (TB clinic and bronchoscopy unit, and TB ward = 0, Emergency department = 1), TB clinic and bronchoscopy unit
(Emergency department and TB ward = 0, TB clinic and bronchoscopy unit = 1)
§Central type air conditioner (natural ventilation and split type air conditioner = 0, central type air conditioner = 1), Split type air conditioner (natural ventilation and central type air conditioner = 0, split type air conditioner = 1)
*
**
***
Comparison of factors and indoor airborne bioaerosol concentration using multiple linear regression
Factors | Bacteria (cfu/m3)† | Fungi (cfu/m3)† | ||||
---|---|---|---|---|---|---|
B† | 95% CI (lower, upper) | B† | 95% CI (lower, upper) | |||
Air change rate (h–1) | –50.48 | –64.99, –35.97 | <0.001*** | –51.57 | –66.66, –36.48 | <0.001*** |
Relative humidity (%) | 7.27 | 4.25, 10.29 | <0.001*** | 6.59 | 3.44, 9.73 | <0.001*** |
Emergency department‡ | 65.05 | 21.99, 108.12 | 0.003** | 68.37 | 23.58, 113.15 | 0.003** |
Central-type air conditioner§ | 113.90 | 63.60, 164.19 | 0.001** | 107.38 | 55.08, 159.68 | <0.001*** |
Constant | 429.84 | 191.73, 667.96 | 0.001 | 405.80 | 158.18, 653.42 | 0.002 |
†The mean indoor airborne bacteria and fungi (cfu/m3 = colony forming unit per cubic meter)
‡Emergency department (TB clinic and bronchoscopy unit, and TB ward = 0, Emergency department = 1), TB clinic and bronchoscopy unit
(Emergency department and TB ward = 0, TB clinic and bronchoscopy unit = 1)
§Central type air conditioner (natural ventilation and split type air conditioner = 0, central type air conditioner = 1), split type air conditioner (natural ventilation and central type air conditioner = 0, split type air conditioner = 1)
Model bacteria (cfu/m3) r2 = 0.636, model fungi (cfu/m3) r2 = 0.614
*
**
The present study found that the mean ± SD of the concentration of indoor airborne bacteria (596.1 ± 140.90 cfu/m3) and fungi (521.2 ± 142.20 cfu/m3) exceeded the levels recommended by the ACGIH (≤ 500 cfu/m3) [9] by more than half in the areas studied (bacteria 67.7% and fungi 50.5%). This finding is consistent with findings from a survey by Chaivisit et al. who assessed the concentrations of airborne bacteria and fungi in a medical intensive care unit in a tertiary care hospital in Thailand in 2016, in which the indoor airborne bacterial concentration was 515.1 ± 246.75 and the indoor airborne fungal concentration was 531.4 ± 337.65 cfu/m3 [4]. However, 2 other surveys conducted in other hospitals in Thailand found comparable levels of indoor airborne bacteria, but much lower levels for indoor airborne fungi. In 2014, Luksamijarulkul et al. studied the indoor airborne bacterial and fungal concentrations in the waiting areas of 4 government hospitals in Bangkok and found that the bacterial levels were from 355.7 ± 86.8 to 500.8 ± 64.2 cfu
The findings from the present study are consistent with a study conducted in Singapore, which found that the airborne bacterial levels were high in a hospital lobby (445–890 cfu/m3) and pharmacy (201–827 cfu/m3) [7], and a study conducted in a hospital in Taiwan found that the level of airborne fungi was 699.3 cfu/m3 in the morning and was 626.2 cfu/m3 in the afternoon [6]. A study conducted in Egypt found that bacterial levels were 728.3 ± 673.2 cfu/m3 in an operating theater and 1,622.2 ± 663.1 cfu/m3 in the admission department of a governmental hospital and 512 ± 425.3 cfu/m3 in the intensive care unit and 1,126.5 ± 763.1 cfu/m3 in the admission department of a private hospital [8].
We found that the size distributions of indoor airborne bioaerosols (bacteria and fungi) peaked at stage 3–4 (2.1–4.7 μm) as consistent with previous findings. In a university hospital in Thailand, the bacterial aerosol sizes in a medical intensive care unit and fungal aerosol sizes in a surgical intensive care unit peaked at 2.1–3.3 μm [4], whereas a study in Taiwan reported that the indoor fungal aerosol sizes peaked at 0.65–2.5 μm [6].
Contamination with airborne bacteria and fungi can be monitored using the I/O ratio [21]. We found that I/O ratios were consistent with those found by other studies. The I/O ratios for airborne bacteria and fungi exceeded 1 (I/O>1) in the admission departments of government hospitals in Egypt [8]. A study of airborne bacteria and fungi conducted in Korea found that I/O > 1 in public buildings, whereas in a number of hospitals the ratios were <1.0 [21]. A study conducted in a tertiary care hospital in Thailand found that the I/O ratio of airborne bacteria was highest (>1) in a medical intensive care unit [4]. We found that indoor (
Our finding that low air change rates (h–1) were associated with high levels of airborne bioaerosols supports findings by previous studies that ventilation and air-conditioning systems are a source of airborne microorganisms [2] and the detection and microbial spread of pathogenic microorganisms such as airborne TB in a hospital may be related to air change rates or ventilation [12]. We found that more than half (55.5%) of the study areas had inadequate ventilation (data not shown). In these areas, air conditioners were used 24 h per day, 7 days per week, and most of had >10 years lifetime, which may reduce their efficiency resulting in inadequate ventilation. Inadequate ventilation, poor temperature control, and high relative humidity can promote bacterial and fungal growth and spread [7, 23].
In emergency departments, the daily occupancy in each area and air change rates were positively associated (
The ventilation in some emergency departments was extremely inadequate [25]. Such inadequacy can affect the health of patients and medical staff, because emergency departments support a variety of activities and high volumes of patients and medical staff. Indoor bioaerosols are associated with human-related bacteria. Many types of bacteria humans carry in their respiratory tract and saliva are released into the environment when people cough, sneeze, and speak. Therefore, if a patient does not use a mask and coughs, indoor airborne bacterial levels will increase [2, 7]. However, this factor is not associated with indoor airborne fungal levels, because the main source of fungi is from outdoors [2, 4, 21].
Our finding that temperature was unrelated to indoor bioaerosol concentration is consistent with previous findings from Thailand [4] and Singapore [7]. An association may be lacking, because each microorganism has a different optimal temperature range for growth, which affects its airborne bioaerosol level. Nor did the number of patient(s) with active TB in each area per day correlate with indoor bioaerosol levels, possibly because this number was negligible compared with the number of all occupants of the areas. Therefore, any additive effect on the airborne levels of bioaerosols may be miniscule. The TB infection control score was not associated with the indoor bioaerosol level, because the study areas have mostly implemented TB infection controls. As a result of these controls, the statistical power of areas without strong controls was limited and we therefore cannot determine the impact of TB patients on the total indoor bioaerosol levels.
In TB high-risk areas of health care facilities, the largest proportion of indoor airborne bioaerosol sizes were in the respirable fraction; the source of airborne bacteria was from indoors while that of fungi was from outdoors. More than half of the areas had indoor airborne bacterial and fungal levels that exceeded the recommendations of the ACGIH [9]. Therefore, control measures for indoor airborne bacterial and fungal levels in the hospitals are warranted. Potential contributors to the indoor airborne levels are low air change rates, central-type air-conditioning systems, and high relative humidity.