Indoor airborne bacterial communities are influenced by ventilation,occupancy, and outdoor air source

Architects and engineers are beginning to consider a new dimension of indoor air: the structure and composition of airborne microbial communities. A first step in this emerging field is to understand the forces that shape the diversity of bioaerosols across space and time within the built environment. In an effort to elucidate the relative influences of three likely drivers of indoor bioaerosol diversity – variation in outdoor bioaerosols, ventilation strategy, and occupancy load – we conducted an intensive temporal study of indoor airborne bacterial communities in a high‐traffic university building with a hybrid HVAC (mechanically and naturally ventilated) system. Indoor air communities closely tracked outdoor air communities, but human‐associated bacterial genera were more than twice as abundant in indoor air compared with outdoor air. Ventilation had a demonstrated effect on indoor airborne bacterial community composition; changes in outdoor air communities were detected inside following a time lag associated with differing ventilation strategies relevant to modern building design. Our results indicate that both occupancy patterns and ventilation strategies are important for understanding airborne microbial community dynamics in the built environment.     

High temporal variability in airborne bacterial diversity and abundance inside single‐family residences

Our homes are microbial habitats, and although the amounts and types of bacteria in indoor air have been shown to vary substantially across residences, temporal variability within homes has rarely been characterized. Here, we sought to quantify the temporal variability in the amounts and types of airborne bacteria in homes, and what factors drive this variability. We collected filter samples of indoor and outdoor air in 15 homes over 1 year (approximately eight time points per home, two per season), and we used culture‐independent DNA sequencing approaches to characterize bacterial community composition. Significant differences in indoor air community composition were observed both between homes and within each home over time. Indoor and outdoor air community compositions were not significantly correlated, suggesting that indoor and outdoor air communities are decoupled. Indoor air communities from the same home were often just as different at adjacent time points as they were across larger temporal distances, and temporal variation correlated with changes in environmental conditions, including temperature and relative humidity. Although all homes had highly variable indoor air communities, homes with the most temporally variable communities had more stable, lower average microbial loads than homes with less variable communities.     

Changing microbial concentrations are associated with ventilation performance in Taiwan's air-conditioned office buildings

Our study conducted serial environmental measurements in 12 large office buildings with two different ventilation designs to obtain airborne microbial concentrations in typical office buildings, and to examine the effects of occupant density, ventilation type and air exchange efficiency on indoor microbial concentrations. Duplicate samples of airborne fungi and bacteria, a total of 2477 measurements, were collected based on a scheme of conducting sampling three times a day for at least seven consecutive days at every study building. Air change rates (ACHs) were also estimated by tracer gas concentration decay method, and measured by continuous Multi-Gas monitor for each building. Most sampling sites were with total fungal and bacteria concentrations higher than 1000 CFU/m(3), an often-quoted guideline in earlier research. Significantly higher concentrations of fungi and bacteria, as well as higher indoor/outdoor (I/O) ratios across most groups of airborne microbes, were identified in buildings with fan coil unit (FCU) system than those with air-handling unit (AHU) system (Student's t test, P < 0.0001). Older buildings and higher air exchange rates were statistically associated with greater indoor bacteria levels in FCU ventilated buildings (R(2) = 0.452); a pattern not found in AHU buildings. Increasing ACH seemed to be the determinant factor for rising indoor fungal and Cladosporium concentrations in those FCU buildings (R(2) = 0.346; 0.518). Our data indicated that FCU ventilated buildings might have provided more outdoor matters into indoor environments through direct penetration of outdoor air. Results also demonstrated a quantitative association between rising numbers of occupants and increasing indoor levels of yeast in both FCU and AHU ventilated buildings. The regression model identified in this study may be considered a reference value for proposing an optimal ACH, while with adequate filtration of fresh air, as an effective strategy in lowering indoor microbial concentrations in air-conditioned buildings. PRACTICAL IMPLICATIONS: As control of indoor microbial contamination has become an increasing concern around the world, feasibility and effectiveness of adopting ventilation approach has attracted a significant interest. This field investigation demonstrated, quantitatively, critical variables to be taken into consideration while applying such a measure, including the kinds of microbes to be removed and the types of ventilation system already in place.     

Investigation of bacterial and fungal communities in indoor and outdoor air of elementary school classrooms by 16S rRNA gene and ITS region sequencing

The advent of high-throughput sequencing methods allowed researchers to fully characterize microbial community in environmental samples, which is crucial to better understand their health effects upon exposures. In our study, we investigated bacterial and fungal community in indoor and outdoor air of nine classrooms in three elementary schools in Seoul, Korea. The extracted bacterial 16S rRNA gene and fungal ITS regions were sequenced, and their taxa were identified. Quantitative polymerase chain reaction for total bacteria DNA was also performed. The bacterial community was richer in outdoor air than classroom air, whereas fungal diversity was similar indoors and outdoors. Bacteria such as Enhydrobacter, Micrococcus, and Staphylococcus that are generally found in human skin, mucous membrane, and intestine were found in great abundance. For fungi, Cladosporium, Clitocybe, and Daedaleopsis were the most abundant genera in classroom air and mostly related to outdoor plants. Bacterial community composition in classroom air was similar among all classrooms but differed from that in outdoor air. However, indoor and outdoor fungal community compositions were similar for the same school but different among schools. Our study indicated the main source of airborne bacteria in classrooms was likely human occupants; however, classroom airborne fungi most likely originated from outdoors.     

Co-occurrence of toxic bacterial and fungal secondary metabolites in moisture-damaged indoor environments

Toxic microbial secondary metabolites have been proposed to be related to adverse health effects observed in moisture-damaged buildings. Initial steps in assessing the actual risk include the characterization of the exposure. In our study, we applied a multi-analyte tandem mass spectrometry-based methodology on sample materials of severely moisture-damaged homes, aiming to qualitatively and quantitatively describe the variety of microbial metabolites occurring in building materials and different dust sample types. From 69 indoor samples, all were positive for at least one of the 186 analytes targeted and as many as 33 different microbial metabolites were found. For the first time, the presence of toxic bacterial metabolites and their co-occurrence with mycotoxins were shown for indoor samples. The bacterial compounds monactin, nonactin, staurosporin and valinomycin were exclusively detected in building materials from moist structures, while chloramphenicol was particularly prevalent in house dusts, including settled airborne dust. These bacterial metabolites are highly bioactive compounds produced by Streptomyces spp., a group of microbes that is considered a moisture damage indicator in indoor environments. We show that toxic bacterial metabolites need to be considered as being part of very complex and diverse microbial exposures in 'moldy' buildings. PRACTICAL IMPLICATIONS: Bacterial toxins co-occur with mycotoxins in moisture-damaged indoor environments. These compounds are measurable also in settled airborne dust, indicating that inhalation exposure takes place. In attempts to characterize exposures to microbial metabolites not only mycotoxins but also bacterial metabolites have to be targeted by the analytical methods applied. We recommend including analysis of samples of outdoor air in the course of future indoor assessments, in an effort to better understand the outdoor contribution to the indoor presence of microbial toxins. There is a need for a sound risk assessment concerning the exposure to indoor microbial toxins at concentrations detectable in moisture-damaged indoor environments.     

Relationship between outdoor and indoor air quality in eight French schools

In the frame of the French national research program PRIMEQUAL (inter-ministry program for better air quality in urban environments), measurements of outdoor and indoor pollution have been carried out in eight schools in La Rochelle (France) and its suburbs. The buildings were naturally ventilated by opening the windows, or mechanically ventilated, and showed various air permeabilities. Ozone, nitrogen oxides (NO and NO(2)), and airborne particle (particle counts within 15 size intervals ranging from 0.3 to 15 mum) concentrations were continuously monitored indoors and outdoors for two 2-week periods. The indoor humidity, temperature, CO(2) concentration (an indicator of occupancy), window openings and building permeability were also measured. The temporal profiles of indoor and outdoor concentrations show ozone and nitrogen oxides behave differently: NO and NO(2) indoor/outdoor concentration ratios (I/O) were found to vary in a range from 0.5 to 1, and from 0.88 to 1, respectively, but no correlation with building permeability was observed. On the contrary, I/O ratios of ozone vary in a range from 0 to 0.45 and seem to be strongly influenced by the building air-tightness: the more airtight the building envelope, the lower the ratio. Occupancy, through re-suspension of previously deposited particles and possible particle generation, strongly influences the indoor concentration level of airborne particles. However, this influence decreases with particle size, reflecting the way deposition velocities vary as a function of size. The influence of particle size on deposition and penetration across the building envelope is also discussed by analyzing the I/O ratios measured when the buildings were unoccupied, by comparing the indoor concentrations measured when the buildings were occupied and when they were not (O/U ratios), and by referring to previously published studies focussing on this topic. Except one case, I/O were found to vary in the range from 0.03 to 1.79. All O/U are greater than one and increase up to 100 with particle size. PRACTICAL IMPLICATIONS: Assessing children's total exposure requires the knowledge of outdoor and indoor air contaminant concentrations. The study presented here provides data on compared outdoor and indoor concentration levels in school buildings, as well as information on the parameters influencing the relationship between outdoor and indoor air quality. It may be used as a basis for estimating indoor concentrations from outdoor concentrations data, or as a first step in designing buildings sheltering children against atmospheric pollution.     

Characterizing the bacterial communities in retail stores in the United States

The microorganisms present in retail environments have not been studied in detail despite the fact that these environments represent a potentially important location for exposure. In this study, HVAC filter dust samples in 13 US retail stores were collected and analyzed via pyrosequencing to characterize the indoor bacterial communities and to explore potential relationships between these communities and building and environmental parameters. Although retail stores contained a diverse bacterial community of 788 unique genera, over half of the nearly 118K sequences were attributed to the Proteobacteria phylum. Streptophyta, Bacillus, Corynebacterium, Pseudomonas, and Acinetobacter were the most prevalent genera detected. The recovered indoor airborne microbial community was statistically associated with both human oral and skin microbiota, indicating occupants are important contributors, despite a relatively low occupant density per unit volume in retail stores. Bacteria generally associated with outdoor environments were present in the indoor communities with no obvious association with air exchange rate, even when considering relative abundance. No significant association was observed between the indoor bacterial community recovered and store location, store type, or season. However, predictive functional gene profiling showed significant associations between the indoor community and season. The microbiome recovered from multiple samples collected months apart from the same building varied significantly indicating that caution is warranted when trying to characterize the bacterial community with a single sampling event.     

Characterizing airborne fungal and bacterial concentrations and emission rates in six occupied children's classrooms

Baseline information on size‐resolved bacterial, fungal, and particulate matter (PM) indoor air concentrations and emission rates is presented for six school classrooms sampled in four countries. Human occupancy resulted in significantly elevated airborne bacterial (81 times on average), fungal (15 times), and PM mass (nine times) concentrations as compared to vacant conditions. Occupied indoor/outdoor (I/O) ratios consistently exceeded vacant I/O ratios. Regarding size distributions, average room‐occupied bacterial, fungal, and PM geometric mean particle sizes were similar to one another while geometric means estimated for bacteria, fungi, and PM mass during vacant sampling were consistently lower than when occupied. Occupancy also resulted in elevated indoor bacterial‐to‐PM mass‐based and number‐based ratios above corresponding outdoor levels. Mean emission rates due to human occupancy were 14 million cells/person/h for bacteria, 14 million spore equivalents/person/h for fungi, and 22 mg/person/h for PM mass. Across all locations, indoor emissions contributed 83 ± 27% (bacteria), 66 ± 19% (fungi), and 83 ± 24% (PM mass) of the average indoor air concentrations during occupied times.     

Quantification of Muramic Acid,a Marker for Bacterial Peptidoglycan,in Dust Collected from Hospital and Home Air-Conditioning Filters using Gas Chromatography — Mass Spectrometry

The development of standardized non-culture-based approaches capable of assessing microbial contarnination of airborne dust is sorely needed. Direct chemical analysis has previously been successfully used for measuring components unique to Gram-negative bacteria. In the present study, dust from primary filters of hospital air-conditioning intake systems (which filter incoming outdoor and recirculated air) and dust from secondary room filters (filtering primarily indoor air) were analyzed. Dust from home air-condition-ing filters (which also filter outdoor air, with recirculation) were also analyzed. Muramic acid is an aminosugar present in Gram-positive and Gram-negative bacterial cell walls and can serve as a measure of bacterial contamination in dust. Samples were analyzed by gas chromatography-mass spectrometry after hydrolysis and conversion of released sugars (including muramic acid) to alditol acetates. Primary hospital filters contained 26.3 ± 10.0 ng of muramic acid/mg dust while secondary filters contained 5.3 ± 5.4 ng/mg. The level of inuramic acid in home air-conditioner dust was 31.7 ± 13.4 ng/mg. This study of dust collected from air-conditioners demonstrates the feasibility of chemical assessment of the microbial contamination of indoor air.     

Assessment of airborne bacteria and fungi in food courts

A study was undertaken to determine the effect of variations in temperature, relative humidity, occupancy density and location (indoor/outdoor) on the concentrations of viable airborne bacterial and fungal spores at an air-conditioned and a non air-conditioned food stall in Singapore. Typically, bioaerosols consisted of 50.5% bacteria and 49.5% fungi in the indoor environment. In contrast, for the outdoor environment, bacteria on an average only accounted for 20.6% of culturable airborne microorganisms whereas fungal concentrations were 79.4%. Results on bioaerosol size distributions revealed that 67% of indoor bacteria and 68% of outdoor bacteria, 85% of indoor fungi and 68% of outdoor fungi were associated with fine mode particulates (<3.3 μm). Occupant density was the key factor that affected indoor airborne bacteria concentrations while concentrations of outdoor airborne bacteria depended strongly on ambient temperature. Indoor fungal concentration was positively correlated to relative humidity whereas outdoor fungal concentration was positively correlated to relative humidity and negatively correlated to temperature. The study also compared the biological air quality between a non air-conditioned food stall (Stall A) and an air-conditioned food stall (Stall B). The dining area of the former had lower bacterial concentrations as compared to the latter, while fungal spore’s concentrations showed a reverse trend. The dominant airborne bacteria genera were Staphylococcus, Pseudomonas, Alcaligens, and Corynebacterium whereas Penicillium, Aspergillus and Cladosporium were the most common fungal genera and groups in both food stalls.     

上海中心大厦生态宜居环境营建理论与实践

营造舒适的生态宜居环境是超高层建筑普遍面临的最大挑战之一。为解决此难题,作为中国第一高楼的上海中心大厦引入可持续绿色垂直城市理念,采用"建筑、区域、城市"协同气候环境设计,通过室外宜居环境营建、室内宜居环境营建和建筑整体舒适度提升手段,最终实现大厦室内外环境品质的全面提升。     

Size-resolved emission rates of airborne bacteria and fungi in an occupied classroom

The role of human occupancy as a source of indoor biological aerosols is poorly understood. Size-resolved concentrations of total and biological particles in indoor air were quantified in a classroom under occupied and vacant conditions. Per-occupant emission rates were estimated through a mass-balance modeling approach, and the microbial diversity of indoor and outdoor air during occupancy was determined via rDNA gene sequence analysis. Significant increases of total particle mass and bacterial genome concentrations were observed during the occupied period compared to the vacant case. These increases varied in magnitude with the particle size and ranged from 3 to 68 times for total mass, 12-2700 times for bacterial genomes, and 1.5-5.2 times for fungal genomes. Emission rates per person-hour because of occupancy were 31 mg, 37 × 10(6) genome copies, and 7.3 × 10(6) genome copies for total particle mass, bacteria, and fungi, respectively. Of the bacterial emissions, ～18% are from taxa that are closely associated with the human skin microbiome. This analysis provides size-resolved, per person-hour emission rates for these biological particles and illustrates the extent to which being in an occupied room results in exposure to bacteria that are associated with previous or current human occupants. PRACTICAL IMPLICATIONS: Presented here are the first size-resolved, per person emission rate estimates of bacterial and fungal genomes for a common occupied indoor space. The marked differences observed between total particle and bacterial size distributions suggest that size-dependent aerosol models that use total particles as a surrogate for microbial particles incorrectly assess the fate of and human exposure to airborne bacteria. The strong signal of human microbiota in airborne particulate matter in an occupied setting demonstrates that the aerosol route can be a source of exposure to microorganisms emitted from the skin, hair, nostrils, and mouths of other occupants.     

Stability of airborne microbes in the Louvre Museum over time

The microbial content of air has as yet been little described, despite its public health implications, and there remains a lack of environmental microbial data on airborne microflora in enclosed spaces. In this context, the aim of this study was to characterize the diversity and dynamics of airborne microorganisms in the Louvre Museum using high‐throughput molecular tools and to underline the microbial signature of indoor air in this human‐occupied environment. This microbial community was monitored for 6 month during occupied time. The quantitative results revealed variations in the concentrations of less than one logarithm, with average values of 10³ and 10⁴ Escherichia coli/Aspergillus fumigatus genome equivalent per m³ for bacteria and fungi, respectively. Our observations highlight the stability of the indoor airborne bacterial diversity over time, while the corresponding eukaryote community was less stable. Bacterial diversity characterized by pyrosequencing 454 showed high diversity dominated by the Proteobacteria which represented 51.1%, 46.9%, and 38.4% of sequences, for each of the three air samples sequenced. A common bacterial diversity was underlined, corresponding to 58.4% of the sequences. The core species were belonging mostly to the Proteobacteria and Actinobacteria, and to the genus Paracoccus spp., Acinetobacter sp., Pseudomonas sp., Enhydrobacter sp., Sphingomonas sp., Staphylococcus sp., and Streptococcus sp.     

通风与空气过滤对控制室内生物污染的影响研究

在分析室内空气微生物的来源、存活及传播等规律的基础上,介绍了通风与空气过滤两种建筑室内生物污染工程控制方法,采用微积分方法建立了通风过滤模型,分析了通风对降低室内生物污染浓度的影响,给出了通风空调系统各空气过滤器滤菌效率的设计计算公式。理论计算结果表明当以控制室内生物污染为主要目的时,自然通风效果不佳,应考虑机械通风;提高集中空调系统的各级过滤器滤菌效率,有助于改善室内生物污染状况。     

打造“绿色”室内环境抵御雾霾

从我国雾霾严重的室外环境现状入手,进一步阐述了绿色建筑中保障健康室内环境的重要性。通过对室内功能设计、建筑施工、室内装饰材料选择及能源浪费问题进行分析,并结合建筑使用者的心理需求,提出了我国绿色建筑中影响室内环境因素。最后,结合绿色科研技术提出了我国新型绿色建筑中优化室内环境的具体解决方法。     

Microbial analyses of airborne dust collected from dormitory rooms predict the sex of occupants

We have long known that human occupants are a major source of microbes in the built environment, thus raising the question: How much can we learn about the occupants of a building by analyzing the microbial communities found in indoor air? We investigated bacterial and fungal diversity found in airborne dust collected onto heating, ventilation, and air‐conditioning (HVAC) air filters and settling plates from 91 rooms within a university dormitory. The sex of the room occupants had the most significant effect on the bacterial communities, while the room occupants had no significant effect on fungal communities. By examining the abundances of bacterial genera, we could predict the sex of room occupants with 79% accuracy, a finding that demonstrates the potential forensic applications of studying indoor air microbiology. We also identified which bacterial taxa were indicators of female and male rooms, and found that those taxa often identified as members of the vaginal microbiome were more common in female‐occupied rooms while taxa associated with human skin or the male urogenital microbiota were more common in male‐occupied rooms.     

Numerical study of the effects of trees on outdoor particle concentration distributions

Outdoor particles are a major contributor to indoor particles which influence the indoor air quality. The outdoor particle concentration also affects the outdoor air quality but the real outdoor particle concentration around buildings may differ from monitored concentrations at monitoring sites. One main factor is the effect of vegetation, especially trees. Numerical simulations were used to investigate the effects of trees on particle concentration distributions around target buildings. The drift flux model was combined with the Reynolds-Averaged Navier-Stokes (RANS) model to model the particle distribution and the airflow. Thirteen cases were analyzed to compare the effects of tree type, tree-building distance and tree canopy-canopy distance on the outdoor particle concentration distribution. The results show that cypress trees reduce the outdoor particle concentration more than pine trees, that shorter tree-building distances (TBD) reduce the particle concentration more than longer tree-building distances, and that a zero tree canopy-canopy distance (CCD) reduces the particle concentration more than CCD=2 m. These results provide guidelines for determining the most effective configuration for trees to reduce outdoor particle concentrations near buildings.     

Estimates of pollutant temporal and spatial variability in commercial buildings from the joint urban 2003 field experiments

In this paper, we report on the indoor concentrations from a suite of full-scale outdoor tracer-gas point releases conducted in the downtown area of Oklahoma City in 2003. A point release experiment consisted of releases of sulfur hexafluoride (SF₆) in multiple buildings and from different outdoor locations. From the measurements, we are able to estimate the concentration variations indoors for a building operating under “typical” operating conditions. The mean indoor spatial coefficients of variation are 30% to 45% from a daytime outdoor release are around 80% during an outdoor evening release. Having estimates of the spatial coefficient of variation provides stakeholders, including first responders, with the likely range of concentrations in the building when little is known about the building characteristics and operating behavior, such as developing urban-scale hazard and consequence analyses. We show differences in indoor measurements at different distances to the release points, floors of the building, and heating, ventilation, and air conditioning system (HVAC) operation. We also show estimates at different time resolutions. The statistics show that in the studied medium to large commercial buildings, spatial differences would result in peak indoor concentrations in certain parts of the buildings that may be substantially higher than the building average. To our knowledge, very few tracer gas measurements have been conducted in buildings of this scope, particularly with measurements on multiple floors and within a floor. The resulting estimates of spatial variability provide a unique opportunity for hazard assessment, and comparison to multi-zone models.     

Outdoor Air Contaminants and Indoor Air Quality under Transient Conditions

The indoor concentrations of contaminants originating from outdoor sources have been measured and calculated under transient conditions. The results show that contaminants that are supplied to an office building via the ventilation system can reach considerably high concentration levels. The indoor/outdoor concentration ratio and time lag are dependent on the air change rate. In buildings with low air change rates the indoor concentration variations are smoothed out compared to buildings with high air change rates. The results from the theoretical model are compared to the results from both laboratory and field measurements and the model is verified for well mixed conditions in a 20 m³ test chamber. The model can be used to simulate different control strategies for reduction of indoor contaminant concentrations related to outdoor sources. One such control strategy is based on reduction of the outdoor air change rate during periods with peak outdoor contaminant concentrations.     

Ecological succession of the microbial communities of an air‐conditioning cooling coil in the tropics

Air‐conditioning systems harbor microorganisms, potentially spreading them to indoor environments. While air and surfaces in air‐conditioning systems are periodically sampled as potential sources of indoor microbes, little is known about the dynamics of cooling coil‐associated communities and their effect on the downstream airflow. Here, we conducted a 4‐week time series sampling to characterize the succession of an air‐conditioning duct and cooling coil after cleaning. Using an universal primer pair targeting hypervariable regions of the 16S/18S ribosomal RNA, we observed a community succession for the condensed water, with the most abundant airborne taxon Agaricomycetes fungi dominating the initial phase and Sphingomonas bacteria becoming the most prevalent taxa toward the end of the experiment. Duplicate air samples collected upstream and downstream of the coil suggest that the system does not act as ecological filter or source/sink for specific microbial taxa during the duration of the experiment.