key: cord-1046806-n8bh8rc8 authors: Almatawah, Qadreyah A.; Al-Rashidi, Mufaerh S.; Yassin, Mohamed F.; Varghese, Julie S. title: Microbiological contamination of indoor and outdoor environments in a desert climate date: 2022-04-11 journal: Environ Monit Assess DOI: 10.1007/s10661-022-10032-9 sha: 650db953007f3028657cfb31e60af09d4afa194c doc_id: 1046806 cord_uid: n8bh8rc8 Microbiological air contamination in the desert environment is becoming an essential subject for the health of office building occupants and public health. In this study, the concentrations and compositions of airborne microorganisms (bacteria and fungi) were assessed in indoor and outdoor environments using a multistory building complex in Kuwait as a case study. Airborne microorganism samples were collected from 12 sites within the building complex containing nineteen stories over four seasons. Culturable airborne bacteria and fungi were impacted on selected media to determine their concentrations and compositions with a Biolog Omnilog GEN III system and Biolog MicroStation. The indoor mean airborne bacterial count concentrations ranged from 35 to 18,463 CFU/m(3), concentrations that are higher than 2,000 CFU/m(3), demonstrating high–very high contamination levels in all seasons. Fungal contamination was high in winter and summer, with detected concentrations > 2,000 CFU/m(3). Indoor-to-outdoor (I/O) ratios showed that airborne microbial contamination inside building floors originated from indoor air contamination. All the building floors showed bacterial and fungal concentrations ranging from less than 2,000 to more than 2,000 CFU/m(3), indicative of a high to very high air contamination level. Statistical analysis showed no correlation between bacterial and fungal concentrations, demonstrating that they originated from unrelated sources. In the indoor building air, the most prevalent bacterial isolate was Bacillus pseudomycoides/cereus, whereas the most dominant fungal isolate was Aspergillus spp. The low count for indoor air bacterial species suggested no particular health risk for the occupants. In contrast, the high count of indoor air fungal species in the winter samples and the presence of potentially allergenic genera detected may suggest possible health risks for the occupants. The results obtained are the basis for the recommendation that the maintenance activities of the HVAC system and the periodical cleaning operation program be revised and preplanned as protective measures. Building office air quality has become of great significance for workers' healthiness and welfare. Previous epidemiological studies of office indoor environments Abstract Microbiological air contamination in the desert environment is becoming an essential subject for the health of office building occupants and public health. In this study, the concentrations and compositions of airborne microorganisms (bacteria and fungi) were assessed in indoor and outdoor environments using a multistory building complex in Kuwait as a case study. Airborne microorganism samples were collected from 12 sites within the building complex containing nineteen stories over four seasons. Culturable airborne bacteria and fungi were impacted on selected media to determine their concentrations and compositions with a Biolog Omnilog GEN III system and Biolog MicroStation. The indoor mean airborne bacterial count concentrations ranged from 35 to 18,463 CFU/m 3 , concentrations that are higher than 2,000 CFU/m 3 , demonstrating high-very high contamination levels in all seasons. Fungal contamination was high in winter and summer, with detected concentrations > 2,000 CFU/m 3 . Indoor-to-outdoor (I/O) ratios showed that airborne microbial contamination show that more than 30% of office employees complain about their health issues, related to indoor environmental contamination (Gołofit-Szymczak & Górny, 2018) . They are exposed to numerous harmful elements, biological and chemical contaminants, mechanical vibration, noise, lighting, electromagnetic fields, static energy, and several microclimates. The building's offices are at risk of regular exposure to microbial contamination. Once microbiological contaminants are found in low concentrations and no pathogens are discovered, they are widely treated as no threat to human health. The primary problem of microbiological contamination arises when the extent of contamination exceeds a particular limit, which is considered ordinary for a specific environment. Many studies on the enclosed environment's microbiological contaminants have been conducted in office buildings, schools, universities, and hospitals (Bonetta et al., 2010; Graudenz et al., 2005; Hospodsky et al., 2012; Huang et al., 2008; Huttunen et al., 2008; Kalogerakis et al., 2005; Kim & Kim, 2007; Law et al., 2001; Łukaszuk et al., 2011; Meadow et al., 2014; Qian et al., 2012; Shoemaker & House, 2006; Stanley et al., 2008; Stetzenbach, 2007; Taubel et al., 2009; Wamedo et al., 2012; Yu et al., 2009) . Regarding the assessment of microbial contaminants in office buildings, Awad et al. (2018) studied the microbial indoor air quality in public buildings that included schools, faculties, libraries, hospitals, and child daycare centers and their association with microclimatic conditions, particulate matter (PM), and ventilation type. The results indicated that the fungal and bacterial concentrations varied based on occupancy intensity, ventilation, and human activity. Gołofit-Szymczak and Górny (2018) assessed employees' exposure to fungal and bacterial aerosols in office buildings with different ventilation structures by evaluating the microbial air quality within the studied premises. The results confirmed that the microbiological air quality in the building offices depended on the type and maintenance condition of the building's ventilation structure. analyzed the microbial air quality of naturally ventilated office rooms and air-conditioned rooms in the Upper Silesia region of Poland. They showed that the mean indoor bacterial aerosol concentrations were less than the Polish suggestions for threshold limit standards in office buildings. characterized the quality and quantity of culturable bacterial aerosols in an office building in southern Poland for the duration of the spring season. They found that Staphylococcus xylosus could form biofilms. In another review, Gilbert and Stephens (2018) outlined the history of a building's environmental microbiology and discussed the current understanding of this microbiome's ecology and evolution. Grisoli et al. (2019) developed the microbiological contamination global index, the amplification index, and the mesophilic bacterial contamination index to assess the contamination levels in offices, gyms, and libraries. Their outcome confirmed that microbial contamination varied depending on the analyzed environment and highlighted the easy applicability of the proposed indices. Regarding the assessment of microbial contaminants in schools, Enitan et al. (2017) determined the indoor air bacterial and fungal density in selected private primary schools in Ilishan-Remo of Ogun State at different sampling times of the day using the settle plate method. The results showed that the concentrations of aeroflora above the permissive standard recorded in this study underscore the importance of this microenvironment for children's high exposure to bioaerosols. Another study by Fsadni et al. (2017) analyzed the association of a school's indoor air quality contaminants, school characteristics, and respiratory health. They found that bacteria, fungi, dog, and cat allergens directly influence school indoor air quality in the Maltese Islands when compared to European statistics. Brągoszewska et al. (2020) studied students' exposure to bacterial aerosols in a high school gym in the urban region of southern Poland. The results showed that the bacterial aerosol concentration was 4.20 × 10 2 ± 49.19 CFU/m 3 before gym classes and was more than doubled (8.75 × 10 2 ± 121.39 CFU/ m 3 ) during gym classes. Chegini et al. (2020) investigated the nature of aerosols for culturable fungi and bacteria in indoor and outdoor air in different kindergartens at Rasht, Iran, by over various seasons. The results revealed that 33% and 8% of the indoor and outdoor bacterial and fungal concentrations, respectively, were higher than the recommended value, indicating medium risk. Another study in daycare centers by Harbizadeh et al. (2019) investigated seasonal variations in airborne bacteria in indoor and outdoor air quality in Ahvaz, Iran. The results revealed that the lowest and highest indoor and outdoor concentrations of airborne bacteria were in the daycare centers within the residential and high-traffic regions. Regarding the assessment of microbial contaminants in universities, Ekhaise and Erhunmwunsee (2013) evaluated the airborne microorganisms associated with the indoor environment and hygienic conditions of the University of Benin, Nigeria, using settle plate methods. Their outcome confirmed the existence of seven airborne bacterial and nine fungal isolates in the residence halls. The quality of indoor air in the Universiti Tun Hussein Onn Malaysia was assessed by Er et al. (2015) . The bacterial concentrations in the affected building areas were significantly higher than the maximum exposure limit of 500 CFU/m 3 . Onet et al. (2018) evaluated the indoor air microbial contamination level for the Polyvalent Sports Hall at the University of Oradea, Romania. The fungal concentration was lower than the bacterial concentration in indoor air and ranged between 0 and 10 3 CFU/m 3 . Dang et al. (2020) assessed indoor air microbial contamination in classrooms at the University of Science, Ho Chi Minh City, Vietnam. The results showed fungal and bacterial densities ranged from 106.1-928.9 CFU/m 3 and 359.6-2,427.3 CFU/ m 3 , respectively. Other studies in university buildings in Malaysia by Idris et al. (2020) and Mazlan et al. (2020) measured the biological contaminant concentration levels and indoor air pollutants in different laboratories and research facilities. They showed that the bacteria found in laboratories and research facilities were identified as gram-positive bacteria. In addition, they found the occurrence of Bacillus laterosporus, Bacillus cereus, Bacillus sphaericus, Staphylococcus epidermis, Staphylococcus aureus, Micrococcus luteus, Enterobacter cloacae, Pseudomonas stutzeri, Pseudomonas fluorescens and Aeromonas hydrophila bacteria. Regarding the assessment of microbial contaminants in hospitals, Fekadu and Getachewu (2015) evaluated the indoor air microorganisms of Jimma University Specialized Hospital wards and determined their health risks. The results indicated that the measured bacterial concentrations were significantly different. Verde et al. (2015) performed the assessment of the fungal load and aerobic mesophilic bacterial counts in the various sites in a Portuguese Hospital (e.g., the emergency service, the operating theater, and the surgical ward). Bacterial concentrations were under the limited criteria in the surgical ward and operating theater. In another study on airborne environmental mesophilic bacteria and fungi at governmental and private Egyptian hospitals, the admission departments, operating theatres, intensive care units, and outdoors were evaluated for comparison by Osman et al. (2017) . Bacillus licheniformis was found at the private hospital, and Alloiococcus otitis was found at the governmental hospital. Recently, Busso et al. (2020) applied a QuEChER method to monitor the levels of airborne microorganisms and evaluated possible variables that alter the load of air microorganisms. They showed a straightforward correlation between air exchange rates, airborne particles, and a number of people. Zenaide-Neto and do Nascimento (2020) analyzed airborne fungal density in a hospital in Paraíba, Brazil. The results indicated that 12 of the 23 rooms in the hospital found a fungal density above the acceptable standard limit, with higher occurrence in obstetrics rooms. Recently, another study by Bjelić et al. (2020) examined bacterial and fungal occurrence, relative humidity, and temperature in a clinical hospital in Doboj, the Republic of Srpska. They indicated a high microbiological contamination level in the hospital air. Jankowiak et al. (2020) measured microbiological contamination in dispensing areas in pharmacies in hospital buildings. The results showed that the highest heterotrophic bacteria and staphylococci concentrations recorded were in pharmacies. Finally, the microbiology indoor air quality of COVID-19 patients at the hospital before and during the pandemic was discussed by Rahardhiman et al. (2020) . Their results revealed that the number of microorganisms was increased before and during the pandemic, although it was still under the quality standard. Workers and employees spend more than 90% of their time in an enclosed environment over their lifetime. Although numerous researchers in many countries have carried out several studies assessing microbiological contaminants, airborne bacteria and fungi, investigations of the enclosed environment in desert climates are still lacking. Therefore, the primary goal of this study is to assess the indoor environment of a 19-floor office building equipped with a heating, ventilation, and air conditioning (HVAC) system for bacterial and fungal concentrations and composition. The work comprised measuring and identifying bacterial and fungal concentrations in the air of selected floors. It was executed in response to the complaints of the building occupants. 355 Page 4 of 16 Vol:. (1234567890) The general characteristic of the weather in Kuwait is that of a typical arid, and hot desert clime (excess of evaporation over precipitation) with a maximum air temperature approaching as high as 50 °C between July and August. Such weather conditions lead the population of Kuwait to spend most of their time in an indoor environment. The multistory complex building used for assessing microbiological contaminants is located on the seaside approximately 2 km west of Kuwait City on the Al-Shuwaikh coast ( Fig. 1) , away from commercial and recreational activities. Airborne microorganisms were collected from 12 sites in the building. The study was carried out on a nineteenstory 10-year-old building with open-space offices and a central HVAC system. The HVAC system of the building was composed of outdoor air intakes located on the first floor and the rooftop, air removal through ceiling vent ducts, and outdoor air passing duct to the air treatment unit (ATU). As needed, fresh and recycled air streams were mixed and filtered, cooled or heated, and humidified or dehumidified in the ATU. Then, conditioned air was distributed throughout a network duct to the supply vents located in the false ceiling. Cooling and heating devices (fan coil units) to cool or heat recycled indoor air were distributed in open spaces. Airborne microorganism sampling Two sets of sites were designated to follow the duct air distribution from the fresh air intake to the end of the process. The first set of sites went from the basement to the 9th floor, and the second set went from the 10th floor to the rooftop (see Fig. 2 and Table 1 ). In the center of each office site, the air sample was collected at 1.5 m above the floor twice a day (at 9.00 a.m. and 1.30 p.m.). A total of 120 air samples were collected for bacterial and fungal assessment in each season. A calibrated impactor sampler (a six-stage Anderson air sampler, HRTECH Model: FSC-A6) was used to collect airborne bacteria and fungi at an airflow rate of 0.0283 m 3 /min for 10 min. At each sampling point, six plates were collected, including one field blank that accompanied the sampler during air monitoring for quality control. The field blanks were processed and analyzed similarly as the rest of the plates. Water samples from the cooling tower water tank were collected for Legionella sp. analysis. Level 3 Level 7 Level 6 Level 8 Level 10 Level 9 Level 11 Level 16 Level 18 Level 17 Level 13 Level 15 Level 14 Level 12 Level 19 Roof Water Tank S2 S1 O/S1 Intake point Water sample-cooling tower-inside 3 Air sample-outside-inlet to pump room 4 Air sample-pump room (basement) 5 Air sample-main lobby-1st floor 6 Air sample-meeting room-1st floor 7 Air sample-office-5th floor 8 Air sample-office-9th floor 9 Air sample-office-10th floor 10 Air sample-office-15th floor 11 Air sample-gathering room-19th floor 12 Air sample-roof top-near filter room Airborne microorganism's analyses Bacterial total counts were examined on trypticase soy agar supplemented with cycloheximide (100 μg/L), and total fungal counts were examined on Rose-Bengal agar supplemented with chloramphenicol (100 μg/L). Petri plates were incubated for 24 h at 37 °C for the bacterial counts and 4-8 days at 24 °C for the fungal counts. The mean colony counts for duplicate samples were estimated and expressed in colony-forming units per cubic meter (CFU/m 3 ). The most dominant bacterial and fungal colonies were selected from each sample and isolated based on their morphology from the indoor and outdoor samples. The water samples from the ATU air humidification tank were analyzed for Legionella spp. according to ISO standard method (ISO, 2004) . Metabolic fingerprint analysis was conducted for bacterial identification using the Biolog Omnilog GEN III system (Biolog, Hayward, CA, USA). The Biolog Omnilog GEN III system is primarily used for soil and water microorganism identification (Avidano et al., 2005) . It tests the ability of microorganisms to utilize or oxidize different carbon sources that can be detected by a redox dye (tetrazolium violet). In brief, the isolated bacteria were grown on Biolog Universal Growth agar at 37 °C for 24 h. The pure colonies were suspended in a 0.4% saline solution, and then their inoculum density was adjusted to the specified turbidity range required. Then, the cells were inoculated in a Biolog GP Microplate and incubated at 37 °C. After 24 h, the result was manually read, and the purple well pattern was analyzed by Biolog_Microlog 2 software. Fungal identification was performed by microscopically examining colony characteristics and their microand macromorphological characteristics using standard taxonomic keys (Von Arx, 1981) and by using a Biolog MicroStation (Biolog, Hayward, CA, USA). Statistical analysis was performed using SPSS software for Windows, version 19.0. ANOVA variance analysis was performed on bacteria and fungi indoor air concentrations using the season, floor, and morning or afternoon as critical parameters. Pearson's correlation coefficient was used to analyze the relationship among the selected parameters. Microbiological indoor air quality Tables 2 and 3 summarize the seasonal sampling's bacterial and fungal indoor contamination levels. The resulting counts were compared with contamination category values designated by the Commission of European Communities (Table 4 , CEC, 1993). The range for bacterial concentrations determined at 37 °C was between 35 and 18,463 CFU/m 3 , with some values higher than the recommended CEC value for indoor contamination (i.e., 2,000 CFU/m 3 , high-very high contamination levels) in every season (Tables 2 and 5) . During the winter, the fungal contamination level was increase in all selected floors with measured concentrations > 2,000 CFU/m 3 . However, during the summer, only three floors (9, 10, 19) show high contamination with measured concentrations > 2,000 CFU/ m 3 (Tables 3 and 6 ). However, during the spring and autumn, the fungal concentrations decreased with the measured concentrations lower than 100 CFU/m 3 (very low-low contamination levels). The analysis of raw data with ANOVA showed significant differences in indoor bacterial and fungal contaminations are associated with the season ( Table 7) . The increasing trend for bacterial concentration was from spring to summer, to winter and fall, whereas the increase in fungal concentration was only in winter. Moreover, both the detected daily bacteria concentration measured at 37 °C and indoor fungal contamination showed significant differences. Each showed a tendency of higher contamination levels in the morning than in the afternoon (Table 7) . No significant correlation was detected between bacterial concentration at 37 °C and fungal concentration using Pearson's correlation coefficient. The effect of the ATU system on IAQ was evaluated by comparing the outdoor air and the indoor air sample microbial concentrations that were collected near air supply diffusers (Tables 8 and 9 ). The evaluation Table 8 Bacterial and fungal concentration (CFU/m 3 ) in outdoor air and at the ventilation shafts during seasonal samplings (AM) SD standard deviation, O outdoor air collected at the intake point of the ATU system, S1 indoor air at the level of the first ventilation shaft after the ATU system, S2 indoor air at the level of the last ventilation shaft after the ATU system, a mean value of the two measurements Table 9 Bacterial and fungal concentration (CFU/m 3 ) in outdoor air and at the ventilation shafts during seasonal samplings (PM) SD standard deviation, O outdoor air collected at the intake point of the ATU system, S1 indoor air at the level of the first ventilation shaft after the ATU system, S2 indoor air at the level of the last ventilation shaft after the ATU system, a mean value of the two measurements showed that fungal and bacterial counts from outdoor air increased from summer to winter/autumn. The fungal and bacterial counts were > 2,000 CFU/ m 3 in both the outdoor air and the indoor air diffusers in the winter samples, indicating that the ATU could not efficiently eliminate the fungal and bacterial material in outdoor air with high contamination. The ratio for indoor/outdoor air samples (I/O; Table 10 ) was estimated from the microbial counts for indoor and outdoor air samples determined throughout the four seasons. The I/O ratios revealed that the fungal concentrations in autumn, summer, and spring and the bacterial concentrations in autumn were higher outdoors than they were indoors, which is in agreement with other published studies in the area of office building air quality (Bonetta et al., 2010; Tsai et al., 2007) . Alternatively, I/O ratios close to 1 or higher were found for fungi in winter, and bacteria in the winter, spring, and summer at 37 °C indicated higher fungal and bacterial air contamination inside than outside the building. Contamination of the indoor environment by Legionella spp. is among the most common causes of severe pneumonia in society and is the cause of approximately 1-40% of hospital-acquired pneumonia cases (Diederen, 2008) . Legionella spp. was isolated from the water inside the cooling tower tank in the spring and summer with a trend of increasing concentration throughout the warmer seasons (spring to summer) ( Table 11 ). The Legionella concentration was > 1000 CFU/L, which means that the water tank needs to be disinfected and cleaned within 7 days, and the cleaning and disinfecting program should be reviewed (AWT, 2003) . The most prevalent bacterial species identified in the indoor air of the building were Bacillus pseudomycoides/ cereus (75.7%), Acinetobacter nosocomialis (11.7%), Bacillus thuringiensis/cereus (3.9%), Staphylococcus hemolyticus (3.6%), Acinetobacter lwoffii (2.7%), and Stenotrophomonas maltophilia (1.9%) (Fig. 3) . Figure 4 shows the seasonal distribution of bacterial species in the indoor air. Figure 6 shows the seasonal distribution of fungal species in the indoor air. Aspergillus foetidus (66.7%) was identified in all autumn indoor air samples, Penicillium aurantiovirens (25.3%) and Rhodotorula mucilaginosa (23%) were found in winter, Alternaria alternata (26.3%) and Ulocladium chartarum (26.3%) were found in spring, and Aspergillus niger (15.4%) and Cladosporium macrocarpum (15.4%) were found in summer. Other studies identified Aspergillus spp., Penicillium spp., and C. sphaerospermum as the most prevalent fungal genera in the environment of building indoor air (Nevalainen & Seuri, 2005; Rejc et al., 2020) . Penicillium spp., Rhodotorula mucilaginosa, and Cladosporium spp. were predominant in winter indoor air (33.3%), (23%), and (17.2%), respectively. In contrast, in autumn, Aspergillus spp. was the most widespread genus (66.7%). The identified fungal genera (Aspergillus, Penicillium, and Cladosporium) in the indoor air were previously documented as potential causes of respiratory allergies (Schwab & Straus, 2004; Tasic & Tasic, 2007) , which also associated Penicillium species with sick building syndrome. This study assessed the airborne microbial concentrations and compositions in the indoor and outdoor environments of a multistory building complex equipped with an HVAC system. It was executed in response to the complaints of the building occupants. Our data showed that airborne bacterial and fungal concentrations in all floors ranged from less than 2,000 to more than 2,000 CFU/m 3 , demonstrating a high-very high contamination level according to the Commission of European Communities (CEC, 1993) . In indoor air, higher concentrations of airborne bacteria compared to that detected outdoors may be associated with several internal sources, including human activity. During the winter, airborne fungal concentrations on all floors ranged from less than 2,000 to more than 2,000 CFU/m 3 , demonstrating a high-very high contamination level according to the Commission of European Communities. Statistical analysis showed no correlation between the bacterial and fungal concentrations, demonstrating that they originated from unrelated sources. Opportunistic pathogen bacterial species were isolated from indoor air (Acinetobacter lwoffii, Acinetobacter nosocomialis, Bacillus thuringiensis/cereus, Pseudomonas aeruginosa, Staphylococcus hemolyticus, Staphylococcus hominis, Stenotrophomonas maltophilia, and Streptococcus downei); however, the low counts recorded and the heterogeneity of the bacterial species do not indicate any potential risk for the health of building occupants. 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Neurotoxicology and Teratology Background culturable bacteria aerosol in two large public buildings using HVAC filters as long-term, passive, high-volume air samplers Introduction to Aerobiology Cladosporium spp.-cause of opportunistic mycoses The occupant as a source of house dust bacteria Biodiversity and concentrations of airborne fungi in large US office buildings from the BASE study Microbiological assessment of indoor air quality at different hospital sites The genera of fungi sporulating in pure culture Interaction between building design and indoor airborne microbial load in Nigeria Review of research on air-conditioning systems and indoor air quality control for human health Air quality and microbiological control in a hospital in Paraíba, Brazil The authors gratefully acknowledge the financial support of this research study of the indoor/outdoor air quality at the Oil Sector Complex Building (EM073C) from Kuwait Petroleum Corporation (KPC). The continuous support and cooperation of Mr. Abdulraheem Al-Rashidi, Environment Manager, are also gratefully acknowledged and highly appreciated.