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1.  Culturability and concentration of indoor and outdoor airborne fungi in six single-family homes 
In this study, the culturability of indoor and outdoor airborne fungi was determined through long-term sampling (24-h) using a Button Personal Inhalable Aerosol Sampler. The air samples were collected during three seasons in six Cincinnati area homes that were free from moisture damage or visible mold. Cultivation and total microscopic enumeration methods were employed for the sample analysis. The geometric means of indoor and outdoor culturable fungal concentrations were 88 and 102 colony-forming units (CFU) m-3, respectively, with a geometric mean of the I/O ratio equal to 0.66. Overall, 26 genera of culturable fungi were recovered from the indoor and outdoor samples. For total fungal spores, the indoor and outdoor geometric means were 211 and 605 spores m-3, respectively, with a geometric mean of I/O ratio equal to 0.32. The identification revealed 37 fungal genera from indoor and outdoor samples based on the total spore analysis. Indoor and outdoor concentrations of culturable and total fungal spores showed significant correlations (r = 0.655, p<0.0001 and r = 0.633, p<0.0001, respectively). The indoor and outdoor median viabilities of fungi were 55% and 25%, respectively, which indicates that indoor environment provides more favorable survival conditions for the aerosolized fungi. Among the seasons, the highest indoor and outdoor culturability of fungi was observed in the fall. Cladosporium had a highest median value of culturability (38% and 33% for indoor and outdoor, respectively) followed by Aspergillus/Penicillium (9% and 2%) among predominant genera of fungi. Increased culturability of fungi inside the homes may have important implications because of the potential increase in the release of allergens from viable spores and pathogenicity of viable fungi on immunocompromised individuals.
PMCID: PMC2367149  PMID: 18458748
Indoor air; Outdoor air; Total fungal spore; Culturable fungi; Culturability
2.  Air- and Dustborne Mycoflora in Houses Free of Water Damage and Fungal Growth 
Applied and Environmental Microbiology  2004;70(11):6394-6400.
Typically, studies on indoor fungal growth in buildings focus on structures with known or suspected water damage, moisture, and/or indoor fungal growth problems. Reference information on types of culturable fungi and total fungal levels are generally not available for buildings without these problems. This study assessed 50 detached single-family homes in metropolitan Atlanta, Ga., to establish a baseline of “normal and typical” types and concentrations of airborne and dustborne fungi in urban homes which were predetermined not to have noteworthy moisture problems or indoor fungal growth. Each home was visually examined, and samples of indoor and outdoor air and of indoor settled dust were taken in winter and summer. The results showed that rankings by prevalence and abundance of the types of airborne and dustborne fungi did not differ from winter to summer, nor did these rankings differ when air samples taken indoors were compared with those taken outdoors. Water indicator fungi were essentially absent from both air and dust samples. The air and dust data sets were also examined specifically for the proportions of colonies from ecological groupings such as leaf surface fungi and soil fungi. In the analysis of dust for culturable fungal colonies, leaf surface fungi constituted a considerable portion (>20%) of the total colonies in at least 85% of the samples. Thus, replicate dust samples with less than 20% of colonies from leaf surface fungi are unlikely to be from buildings free of moisture or mold growth problems.
PMCID: PMC525119  PMID: 15528497
3.  Relationship between indoor and outdoor bioaerosols collected with a button inhalable aerosol sampler in urban homes 
Indoor air  2006;16(1):37-47.
This field study investigated the relationship between indoor and outdoor concentrations of airborne actinomycetes, fungal spores, and pollen. Air samples were collected for 24 h with a button inhalable aerosol sampler inside and outside of six single-family homes located in the Cincinnati area (overall, 15 pairs of samples were taken in each home). The measurements were conducted during three seasons – spring and fall 2004, and winter 2005. The concentration of culturable actinomycetes was mostly below the detection limit. The median indoor/outdoor ratio (I/O) for actinomycetes was the highest: 2.857. The indoor of fungal and pollen concentrations followed the outdoor concentrations while indoor levels were mostly lower than the outdoor ones. The I/O ratio of total fungal spores (median = 0.345) in six homes was greater than that of pollen grains (median = 0.025). The low I/O ratios obtained for pollen during the peak ambient pollination season (spring) suggest that only a small fraction penetrated from outdoor to indoor environment. This is attributed to the larger size of pollen grains. Higher indoor concentration levels and variability in the I/O ratio observed for airborne fungi may be associated with indoor sources and/or higher outdoor-to-indoor penetration of fungal spores compared to pollen grains.
PMCID: PMC2233950  PMID: 16420496
Bioaerosol; Exposure; Indoor; Outdoor; Bacteria; Fungal spore; Pollen
4.  Profiles of Airborne Fungi in Buildings and Outdoor Environments in the United States 
We examined 12,026 fungal air samples (9,619 indoor samples and 2,407 outdoor samples) from 1,717 buildings located across the United States; these samples were collected during indoor air quality investigations performed from 1996 to 1998. For all buildings, both indoor and outdoor air samples were collected with an Andersen N6 sampler. The culturable airborne fungal concentrations in indoor air were lower than those in outdoor air. The fungal levels were highest in the fall and summer and lowest in the winter and spring. Geographically, the highest fungal levels were found in the Southwest, Far West, and Southeast. The most common culturable airborne fungi, both indoors and outdoors and in all seasons and regions, were Cladosporium, Penicillium, nonsporulating fungi, and Aspergillus. Stachybotrys chartarum was identified in the indoor air in 6% of the buildings studied and in the outdoor air of 1% of the buildings studied. This study provides industrial hygienists, allergists, and other public health practitioners with comparative information on common culturable airborne fungi in the United States. This is the largest study of airborne indoor and outdoor fungal species and concentrations conducted with a standardized protocol to date.
PMCID: PMC123871  PMID: 11916692
5.  Coarse and Fine Culturable Fungal Air Concentrations in Urban and Rural Homes in Egypt 
The main objective of the present study was to assess culturable airborne fungal concentrations, and types in different seasons. Two-stage viable impactor samplers were used with malt extract agar medium as the collection media. Culturable airborne fungal concentrations were collected indoors and outdoors of 43 homes in urban and rural environments from November 2008 to October 2009 in Egypt. Fungal concentrations were significantly higher in the rural environment than the urban environment. The median indoor and outdoor total fungal concentrations were 608 and 675 CFU/m3 in the urban environment and 1,932 and 1,872 CFU/m3 in the rural environment, respectively. The greatest concentrations were found in the autumn and spring season. Indoor and outdoor concentrations were significantly correlated (P < 0.001). The highest concentrations were observed in the fungal size range of <8 µm (fine fraction). The indoor/outdoor (I/O) ratios were not statistically different between seasons. Alternaria, Aspergillus, Cladosporium, Penicillium and yeasts were the predominant genera indoors and outdoors, and the abundance of genera varied by season and region. This study is of a potential interest as little reported research on the indoor fungal air quality from Egypt.
PMCID: PMC3709295  PMID: 23466829
air; fungi; homes; rural; urban
6.  Investigation on distribution of airborne fungi in outdoor environment in Tehran, Iran 
Airborne fungi are responsible for the majority of fungal infections in humans and animals. Outdoor air markedly influences the prevalence of fungal spore levels in indoor air and thus, it is the major source of fungal infections in indoor environments especially in hospitalized individuals.
Using a settle plate method, air sampling (1092 air samples from 93 sampling sites in 22 geographic regions of Tehran) was performed by exposing 90 mm settle plates containing Malt extract agar and Potato dextrose agar to the air for 30 min. The plates were incubated at 28°C for 2–3 weeks and examined daily for visible fungal growth. Purified fungal colonies were identified at the genus level based on morphological criteria according to standard methods.
A total of 6455 colonies belonging to 24 different fungal genera were isolated. Area V situated in the city center was the most contaminated region with 2523 fungal colonies (39.1%), while area IV in the West showed the least contamination rate (636 colonies; 9.8%). Airborne fungi isolated were classified into 4 classes including hyaline Hyphomycetes (53.5%), dematiaceous Hyphomycetes (41.6%), Zygomycetes (2.8%) and Coelomycetes (0.2%). Aspergillus (31.3%) was the most prominent isolated fungus followed by Cladosporium (22.1%), Penicillium (13.8%) and Alternaria (12.2%).
Our results indicate that outdoor air is a potential threat to public health because of harboring a wide array of pathogenic and allergenic airborne fungal spores which can serve as the main source of contamination of indoor environments such as homes, offices and hospitals.
PMCID: PMC3974021  PMID: 24588901
Airborne fungi; Outdoor air; Hyphomycetes; Zygomycetes; Aspergillus; Cladosporium; Penicillium; Alternaria; Tehran
7.  Seasonal Changes in Endotoxin Exposure and Its Relationship to Exhaled Nitric Oxide and Exhaled Breath Condensate pH Levels in Atopic and Healthy Children 
PLoS ONE  2013;8(6):e66785.
Endotoxin, a component of the cell walls of gram-negative bacteria, is a contaminant in organic dusts (house dust) and aerosols. In humans, small amounts of endotoxin may cause a local inflammatory response. Exhaled nitric oxide (eNO) levels, an inflammation indicator, are associated with the pH values of exhaled breath condensate (EBC). This study evaluated seasonal changes on indoor endotoxin concentrations in homes and the relationships between endotoxin exposure and eNO/EBC pH levels for healthy children and children with allergy-related respiratory diseases. In total, 34 children with allergy-related respiratory diseases and 24 healthy children were enrolled. Indoor air quality measurements and dust sample analysis for endotoxin were conducted once each season inside 58 surveyed homes. The eNO, EBC pH levels, and pulmonary function of the children were also determined. The highest endotoxin concentrations were on kitchen floors of homes of children with allergy-related respiratory diseases and healthy children, and on bedroom floors of homes of asthmatic children and healthy children. Seasonal changes existed in endotoxin concentrations in dust samples from homes of children with allergic rhinitis, with or without asthma, and in EBC pH values among healthy children and those with allergy-related respiratory diseases. Strong relationships existed between endotoxin exposure and EBC pH values in children with allergic rhinitis.
PMCID: PMC3686731  PMID: 23840530
8.  Fungal Levels in the Home and Allergic Rhinitis by 5 Years of Age 
Environmental Health Perspectives  2005;113(10):1405-1409.
Studies have repeatedly demonstrated that sensitization to fungi, such as Alternaria, is strongly associated with allergic rhinitis and asthma in children. However, the role of exposure to fungi in the development of childhood allergic rhinitis is poorly understood. In a prospective birth cohort of 405 children of asthmatic/allergic parents from metropolitan Boston, Massachusetts, we examined in-home high fungal concentrations (> 90th percentile) measured once within the first 3 months of life as predictors of doctor-diagnosed allergic rhinitis in the first 5 years of life. In multivariate Cox regression analyses, predictors of allergic rhinitis included high levels of dust-borne Aspergillus [hazard ratio (HR) = 3.27; 95% confidence interval (CI), 1.50–7.14], Aureobasidium (HR = 3.04; 95% CI, 1.33–6.93), and yeasts (HR = 2.67; 95% CI, 1.26–5.66). The factors controlled for in these analyses included water damage or mild or mildew in the building during the first year of the child’s life, any lower respiratory tract infection in the first year, male sex, African-American race, fall date of birth, and maternal IgE to Alternaria > 0.35 U/mL. Dust-borne Alternaria and non-sporulating and total fungi were also predictors of allergic rhinitis in models excluding other fungi but adjusting for all of the potential confounders listed above. High measured fungal concentrations and reports of water damage, mold, or mildew in homes may predispose children with a family history of asthma or allergy to the development of allergic rhinitis.
PMCID: PMC1281288  PMID: 16203255
allergic rhinitis; fungi; mold; respiratory health effects; water damage
9.  Correlation between the prevalence of certain fungi and sick building syndrome 
OBJECTIVE: To examine the role of fungi in the production of sick building syndrome. METHODS: A 22 month study in the United States of 48 schools (in which there had been concerns about health and indoor air quality (IAQ). Building indoor air and surface samples, as well as outdoor air samples were taken at all sites to look for the presence of fungi or their viable propagules. RESULTS: Five fungal genera were consistently found in the outdoor air and comprised over 95% of the outdoor fungi. These genera were Cladosporium (81.5%), Penicillium (5.2%), Chrysosporium (4.9%), Alternaria (2.8%), and Aspergillus (1.1%). At 20 schools, there were significantly more colony forming units per cubic metre (CFU/m3) (p < 0.0001) of propagules of Penicillium species in the air samples from complaint areas when compared with the outdoor air samples and the indoor air samples from noncomplaint areas. At five schools, there were more, although not significant (p = 0.10), Penicillium propagules in the air samples from complaint areas when compared with the outdoor air samples and the indoor air samples from noncomplaint areas. In 11 schools, the indoor air (complaint areas) fungal ratios were similar to that in the outdoor air. In these 11 schools Stachybotrys atra was isolated from swab samples of visible growth under wetted carpets, on wetted walls, or behind vinyl wall coverings. In the remaining 11 schools, the fungal ratios and CFU/m3 of air were not significantly different in different areas. Many of the schools took remedial action that resulted in an indoor air fungal profile that was similar to that outdoors. CONCLUSIONS: Propagules of Penicillium and Stachybotrys species may be associated with sick building syndrome.
PMCID: PMC1757636  PMID: 9861178
10.  Household airborne Penicillium associated with peak expiratory flow variability in asthmatic children 
Exposure to airborne fungi has been associated with increased airway hyperreactivity and asthma prevalence.
To investigate the association between common indoor fungi and airway hyperreactivity measured by peak expiratory flow variability in asthmatic children.
Children 6 to 12 years of age (n = 225) with a physician diagnosis of asthma were enrolled in the study to have their peak expiratory flow recorded twice daily during a 2-week period. Genus-specific, quantitative, in-home airborne mold concentrations were measured. Logistic regression models were used to examine the relationship between a mean peak expiratory flow variability greater than 18.5% (75th percentile) and any mold in the home (total mold, Cladosporium, Penicillium, Aspergillus, and Alternaria).
Mold was detected in 93% of the homes. The most common molds were Cladosporium in 72% and Penicillium in 42% of the samples. Controlling for sex, ethnicity, age, and winter season of sampling, Penicillium measured in the home was associated with a mean peak expiratory flow variability greater than 18.5% (odds ratio, 2.4; 95% confidence interval, 1.2–4.8). Greater peak expiratory flow variability was not associated with total mold or other mold measured in the home.
Exposure to airborne Penicillium is associated with increased peak expiratory flow variability in asthmatic children.
PMCID: PMC2746059  PMID: 19663123
11.  Outdoor allergens. 
Environmental Health Perspectives  2000;108(Suppl 4):653-659.
Outdoor allergens are an important part of the exposures that lead to allergic disease. Understanding the role of outdoor allergens requires a knowledge of the nature of outdoor allergen-bearing particles, the distributions of their source, and the nature of the aerosols (particle types, sizes, dynamics of concentrations). Primary sources for outdoor allergens include vascular plants (pollen, fern spores, soy dust), and fungi (spores, hyphae). Nonvascular plants, algae, and arthropods contribute small numbers of allergen-bearing particles. Particles are released from sources into the air by wind, rain, mechanical disturbance, or active discharge mechanisms. Once airborne, they follow the physical laws that apply to all airborne particles. Although some outdoor allergens penetrate indoor spaces, exposure occurs mostly outdoors. Even short-term peak outdoor exposures can be important in eliciting acute symptoms. Monitoring of airborne biological particles is usually by particle impaction and microscopic examination. Centrally located monitoring stations give regional-scale measurements for aeroallergen levels. Evidence for the role of outdoor allergens in allergic rhinitis is strong and is rapidly increasing for a role in asthma. Pollen and fungal spore exposures have both been implicated in acute exacerbations of asthma, and sensitivity to some fungal spores predicts the existence of asthma. Synergism and/or antagonism probably occurs with other outdoor air particles and gases. Control involves avoidance of exposure (staying indoors, preventing entry of outdoor aerosols) as well as immunotherapy, which is effective for pollen but of limited effect for spores. Outdoor allergens have been the subject of only limited studies with respect to the epidemiology of asthma. Much remains to be studied with respect to prevalence patterns, exposure and disease relationships, and control.
PMCID: PMC1637672  PMID: 10931783
12.  Residential Culturable Fungi, (1–3, 1–6)-β-D-glucan, and Ergosterol Concentrations in Dust Are Not Associated with Asthma, Rhinitis or Eczema Diagnoses in Children 
Indoor air  2013;24(2):158-170.
Qualitative reporting of home indoor moisture problems predicts respiratory diseases. However, causal agents underlying such qualitative markers remain unknown.
In the homes of 198 multiple allergic case children and 202 controls in Sweden, we cultivated culturable fungi by directly plating dust, and quantified(1–3, 1–6)-β-D-glucan, and ergosterol in dust samples from the child’s bedroom. We examined the relationship between these fungal agents and degree of parent or inspector reported home indoor dampness, and microbiological laboratory’s mold index. We also compared the concentrations of these agents between multiple allergic cases and healthy controls, as well as IgE-sensitization among cases.
The concentrations of culturable fungal agents were comparable between houses with parent and inspector reported mold issues and those without. There were no differences in concentrations of the individual or the total summed culturable fungi, (1–3, 1–6)-β-D-glucan, and ergosterol between the controls and the multiple allergic case children, or individual diagnosis of asthma, rhinitis or eczema.
Culturable fungi, (1–3, 1–6)-β-D-glucan, and ergosterol in dust were not associated with qualitative markers of indoor dampness or mold or indoor humidity. Furthermore, these agents in dust samples were not associated with any health outcomes in the children.
PMCID: PMC3992620  PMID: 24016225
indoor; asthma; allergies; children; dampness; mold
13.  Airborne Mold and Endotoxin Concentrations in New Orleans, Louisiana, after Flooding, October through November 2005 
Environmental Health Perspectives  2006;114(9):1381-1386.
The hurricanes and flooding in New Orleans, Louisiana, in October and November 2005 resulted in damp conditions favorable to the dispersion of bioaerosols such as mold spores and endotoxin.
Our objective in this study was to assess potential human exposure to bioaerosols in New Orleans after the flooding of the city.
A team of investigators performed continuous airborne sampling for mold spores and endotoxin outdoors in flooded and nonflooded areas, and inside homes that had undergone various levels of remediation, for periods of 5–24 hr during the 2 months after the flooding.
The estimated 24-hr mold concentrations ranged from 21,000 to 102,000 spores/m3 in outdoor air and from 11,000 to 645,000 spores/m3 in indoor air. The mean outdoor spore concentration in flooded areas was roughly double the concentration in nonflooded areas (66,167 vs. 33,179 spores/m3; p < 0.05). The highest concentrations were inside homes. The most common mold species were from the genera of Cladosporium and Aspergillus/Penicillium; Stachybotrys was detected in some indoor samples. The airborne endotoxin concentrations ranged from 0.6 to 8.3 EU (endo-toxin units)/m3 but did not vary with flooded status or between indoor and outdoor environments.
The high concentration of mold measured indoors and outdoors in the New Orleans area is likely to be a significant respiratory hazard that should be monitored over time. Workers and returning residents should use appropriate personal protective equipment and exposure mitigation techniques to prevent respiratory morbidity and long-term health effects.
PMCID: PMC1570051  PMID: 16966092
air quality; bioaerosols; endotoxin; flood; Katrina; mold; New Orleans
14.  Mold Occurring on the Air Cleaner High-Efficiency Particulate Air Filters Used in the Houses of Child Patients with Atopic Dermatitis 
Mycobiology  2014;42(3):286-290.
Fungi are the known sources of irritation associated with atopic diseases (e.g., asthma, allergic rhinoconjunctivitis, and atopic eczema). To quantitatively estimate their presence in the indoor environment of atopic dermatitis-inflicted child patient's houses (ADCPHs), the high-efficiency particulate air (HEPA) filters installed inside the air cleaners of three different ADCPHs were investigated for the presence of mold. The air cleaner HEPA filters obtained from the three different ADCPHs were coded as HEPA-A, -B, and -C, respectively, and tested for the presence of mold. The colony forming units (CFUs) corresponding to the HEPA-A, -B, and -C filters were estimated to be 6.51 × 102 ± 1.50 × 102 CFU/cm2, 8.72 × 102 ± 1.69 × 102 CFU/cm2, and 9.71 × 102 ± 1.35 × 102 CFU/cm2, respectively. Aspergillus, Penicillium, Alternaria, Cladosporium, Trichoderma, and other fungal groups were detected in the 2,494 isolates. The distribution of these fungal groups differed among the three filters. Cladosporium was the major fungal group in filters HEPA-A and -C, whereas Penicillium was the major fungal group in the filter HEPA-B. Nine fungal species, including some of the known allergenic species, were identified in these isolates. Cladosporium cladosporioides was the most common mold among all the three filters. This is the first report on the presence of fungi in the air cleaner HEPA filters from ADCPHs in Korea.
PMCID: PMC4206797  PMID: 25346608
Atopic dermatitis; Fungi; High-efficiency particulate air filters; Indoor air
15.  Dispersal in microbes: fungi in indoor air are dominated by outdoor air and show dispersal limitation at short distances 
The ISME Journal  2013;7(7):1262-1273.
The indoor microbiome is a complex system that is thought to depend on dispersal from the outdoor biome and the occupants' microbiome combined with selective pressures imposed by the occupants' behaviors and the building itself. We set out to determine the pattern of fungal diversity and composition in indoor air on a local scale and to identify processes behind that pattern. We surveyed airborne fungal assemblages within 1-month time periods at two seasons, with high replication, indoors and outdoors, within and across standardized residences at a university housing facility. Fungal assemblages indoors were diverse and strongly determined by dispersal from outdoors, and no fungal taxa were found as indicators of indoor air. There was a seasonal effect on the fungi found in both indoor and outdoor air, and quantitatively more fungal biomass was detected outdoors than indoors. A strong signal of isolation by distance existed in both outdoor and indoor airborne fungal assemblages, despite the small geographic scale in which this study was undertaken (<500 m). Moreover, room and occupant behavior had no detectable effect on the fungi found in indoor air. These results show that at the local level, outdoor air fungi dominate the patterning of indoor air. More broadly, they provide additional support for the growing evidence that dispersal limitation, even on small geographic scales, is a key process in structuring the often-observed distance–decay biogeographic pattern in microbial communities.
PMCID: PMC3695294  PMID: 23426013
bioaerosol; built environment microbiome; community assembly; isolation by distance; ITS; 454 pyrosequencing
16.  The effect of outdoor fungal spore concentrations on daily asthma severity. 
Environmental Health Perspectives  1997;105(6):622-635.
The relationship between day-to-day changes in asthma severity and combined exposures to community air pollutants and aeroallergens remains to be clearly defined. We examined the effects of outdoor air pollutants, fungi, and pollen on asthma. Twenty-two asthmatics ages 9-46 years were followed for 8 weeks (9 May-3 July 1994) in a semirural Southern California community around the air inversion base elevation (1,200 ft). Daily diary responses included asthma symptom severity (6 levels), morning and evening peak expiratory flow rates (PEFR), and as-needed beta-agonist inhaler use. Exposures included 24-hr outdoor concentrations of fungi, pollen, and particulate matter with a diameter < 10 microns (PM10; maximum = 51 micrograms/m3) and 12-hour day-time personal ozone (O3) measurements (90th percentile = 38 ppb). Random effects longitudinal regression models controlled for autocorrelation and weather. Higher temperatures were strongly protective, probably due to air conditioning use and diminished indoor allergens during hot, dry periods. Controlling for weather, total fungal spore concentrations were associated with all outcomes: per minimum to 90th percentile increase of nearly 4,000 spores/m3, asthma symptom scores increased 0.36 (95% CI, 0.16-0.56), inhaler use increased 0.33 puffs (95% CI, -0.02-0.69), and evening PEFR decreased 12.1 l/min (95% CI, -1.8-22.3). These associations were greatly enhanced by examining certain fungal types (e.g., Alternaria, basidiospores, and hyphal fragments) and stratifying on 16 asthmatics allergic to tested deuteromycete fungi. There were no significant associations to low levels of pollen or O3, but inhaler use was associated with PM10 (0.15 inhaler puffs/10 micrograms/m3; p < 0.02). These findings suggest that exposure to fungal spores can adversely effect the daily respiratory status of some asthmatics.
PMCID: PMC1470068  PMID: 9288497
17.  Seasonal Variations of Indoor Microbial Exposures and Their Relation to Temperature, Relative Humidity, and Air Exchange Rate 
Applied and Environmental Microbiology  2012;78(23):8289-8297.
Indoor microbial exposure has been related to adverse pulmonary health effects. Exposure assessment is not standardized, and various factors may affect the measured exposure. The aim of this study was to investigate the seasonal variation of selected microbial exposures and their associations with temperature, relative humidity, and air exchange rates in Danish homes. Airborne inhalable dust was sampled in five Danish homes throughout the four seasons of 1 year (indoors, n = 127; outdoors, n = 37). Measurements included culturable fungi and bacteria, endotoxin, N-acetyl-beta-d-glucosaminidase, total inflammatory potential, particles (0.75 to 15 μm), temperature, relative humidity, and air exchange rates. Significant seasonal variation was found for all indoor microbial exposures, excluding endotoxin. Indoor fungi peaked in summer (median, 235 CFU/m3) and were lowest in winter (median, 26 CFU/m3). Indoor bacteria peaked in spring (median, 2,165 CFU/m3) and were lowest in summer (median, 240 CFU/m3). Concentrations of fungi were predominately higher outdoors than indoors, whereas bacteria, endotoxin, and inhalable dust concentrations were highest indoors. Bacteria and endotoxin correlated with the mass of inhalable dust and number of particles. Temperature and air exchange rates were positively associated with fungi and N-acetyl-beta-d-glucosaminidase and negatively with bacteria and the total inflammatory potential. Although temperature, relative humidity, and air exchange rates were significantly associated with several indoor microbial exposures, they could not fully explain the observed seasonal variations when tested in a mixed statistical model. In conclusion, the season significantly affects indoor microbial exposures, which are influenced by temperature, relative humidity, and air exchange rates.
PMCID: PMC3497365  PMID: 23001651
18.  Comparison of mold concentrations quantified by MSQPCR in indoor and outdoor air sampled simultaneously 
Mold specific quantitative PCR (MSQPCR) was used to measure the concentrations of the 36 mold species in indoor and outdoor air samples that were taken simultaneously for 48 h in and around 17 homes in Cincinnati, Ohio. The total spore concentrations of 353 per m3 of indoor air and 827 per m3 of outdoor air samples were significantly different (p≤0.05). However, only the concentrations of Aspergillus penicillioides, Cladosporium cladosporioides types 1 and 2 and Cladosporium herbarum were correlated in indoor and outdoor air samples (p-value≤0.05 and sufficient data for estimate and absolute value rho estimate ≥0.5). These results suggest that interpretation of the meaning of short-term (<48 h) mold measurements in indoor and outdoor air samples must be made with caution.
PMCID: PMC2233941  PMID: 17467772
Mold; Indoor air; Outdoor air; Mold specific quantitative PCR
19.  Airborne Bacterial Communities in Residences: Similarities and Differences with Fungi 
PLoS ONE  2014;9(3):e91283.
Genetic analysis of indoor air has uncovered a rich microbial presence, but rarely have both the bacterial and fungal components been examined in the same samples. Here we present a study that examined the bacterial component of passively settled microbes from both indoor and outdoor air over a discrete time period and for which the fungal component has already been reported. Dust was allowed to passively settle in five common locations around a home − living room, bedroom, bathroom, kitchen, and balcony − at different dwellings within a university-housing complex for a one-month period at two time points, once in summer and again in winter. We amplified the bacterial 16S rRNA gene in these samples and analyzed them with high-throughput sequencing. Like fungal OTU-richness, bacterial OTU-richness was higher outdoors then indoors and was invariant across different indoor room types. While fungal composition was structured largely by season and residential unit, bacterial composition varied by residential unit and room type. Bacteria from putative outdoor sources, such as Sphingomonas and Deinococcus, comprised a large percentage of the balcony samples, while human-associated taxa comprised a large percentage of the indoor samples. Abundant outdoor bacterial taxa were also observed indoors, but the reverse was not true; this is unlike fungi, in which the taxa abundant indoors were also well-represented outdoors. Moreover, there was a partial association of bacterial composition and geographic distance, such that samples separated by even a few hundred meters tended have greater compositional differences than samples closer together in space, a pattern also observed for fungi. These data show that while the outdoor source for indoor bacteria and fungi varies in both space and time, humans provide a strong and homogenizing effect on indoor bacterial bioaerosols, a pattern not observed in fungi.
PMCID: PMC3946336  PMID: 24603548
20.  Asthmatic Symptoms among Pupils in Relation to Winter Indoor and Outdoor Air Pollution in Schools in Taiyuan, China 
There are few studies on associations between children’s respiratory heath and air pollution in schools in China. The industrial development and increased traffic may affect the indoor exposure to air pollutants in school environment. Moreover, there is a need to study respiratory effects of environmental tobacco smoke (ETS) and emissions from new building materials in homes in China.
We studied the associations between pupils’ asthmatic symptoms and indoor and outdoor air pollution in schools, as well as selected home exposures, in a coal-burning city in north China.
A questionnaire survey was administered to pupils (11–15 years of age) in 10 schools in urban Taiyuan, collecting data on respiratory health and selected home environmental factors. Indoor and outdoor school air pollutants and climate factors were measured in winter.
A total of 1,993 pupils (90.2%) participated; 1.8% had cumulative asthma, 8.4% wheezing, 29.8% had daytime attacks of breathlessness. The indoor average concentrations of sulfur dioxide, nitrogen dioxide, ozone, and formaldehyde by class were 264.8, 39.4, 10.1, and 2.3 μg/m3, respectively. Outdoor levels were two to three times higher. Controlling for possible confounders, either wheeze or daytime or nocturnal attacks of breathlessness were positively associated with SO2, NO2, or formaldehyde. In addition, ETS and new furniture at home were risk factors for wheeze, daytime breathlessness, and respiratory infections.
Indoor chemical air pollutants of mainly outdoor origin could be risk factors for pupils’ respiratory symptoms at school, and home exposure to ETS and chemical emissions from new furniture could affect pupils’ respiratory health.
PMCID: PMC2199281  PMID: 18197305
air pollution; asthma; China; formaldehyde; indoor; nitrogen dioxide; ozone; outdoor; school; sulfur dioxide
21.  Particle-size distributions and seasonal diversity of allergenic and pathogenic fungi in outdoor air 
The ISME Journal  2012;6(10):1801-1811.
Fungi are ubiquitous in outdoor air, and their concentration, aerodynamic diameters and taxonomic composition have potentially important implications for human health. Although exposure to fungal allergens is considered a strong risk factor for asthma prevalence and severity, limitations in tracking fungal diversity in air have thus far prevented a clear understanding of their human pathogenic properties. This study used a cascade impactor for sampling, and quantitative real-time PCR plus 454 pyrosequencing for analysis to investigate seasonal, size-resolved fungal communities in outdoor air in an urban setting in the northeastern United States. From the 20 libraries produced with an average of ∼800 internal transcribed spacer (ITS) sequences (total 15 326 reads), 12 864 and 11 280 sequences were determined to the genus and species levels, respectively, and 558 different genera and 1172 different species were identified, including allergens and infectious pathogens. These analyses revealed strong relationships between fungal aerodynamic diameters and features of taxonomic compositions. The relative abundance of airborne allergenic fungi ranged from 2.8% to 10.7% of total airborne fungal taxa, peaked in the fall, and increased with increasing aerodynamic diameter. Fungi that can cause invasive fungal infections peaked in the spring, comprised 0.1–1.6% of fungal taxa and typically increased in relative abundance with decreasing aerodynamic diameter. Atmospheric fungal ecology is a strong function of aerodynamic diameter, whereby through physical processes, the size influences the diversity of airborne fungi that deposit in human airways and the efficiencies with which specific groups of fungi partition from outdoor air to indoor environments.
PMCID: PMC3446800  PMID: 22476354
aerodynamic diameter; fungi; 454 pyrosequencing; allergen; bioaerosol
22.  The Diversity and Distribution of Fungi on Residential Surfaces 
PLoS ONE  2013;8(11):e78866.
The predominant hypothesis regarding the composition of microbial assemblages in indoor environments is that fungal assemblages are structured by outdoor air with a moderate contribution by surface growth, whereas indoor bacterial assemblages represent a mixture of bacteria entered from outdoor air, shed by building inhabitants, and grown on surfaces. To test the fungal aspect of this hypothesis, we sampled fungi from three surface types likely to support growth and therefore possible contributors of fungi to indoor air: drains in kitchens and bathrooms, sills beneath condensation-prone windows, and skin of human inhabitants. Sampling was done in replicated units of a university-housing complex without reported mold problems, and sequences were analyzed using both QIIME and the new UPARSE approach to OTU-binning, to the same result. Surfaces demonstrated a mycological profile similar to that of outdoor air from the same locality, and assemblages clustered by surface type. “Weedy” genera typical of indoor air, such as Cladosporium and Cryptococcus, were abundant on sills, as were a diverse set of fungi of likely outdoor origin. Drains supported more depauperate assemblages than the other surfaces and contained thermotolerant genera such as Exophiala, Candida, and Fusarium. Most surprising was the composition detected on residents’ foreheads. In addition to harboring Malassezia, a known human commensal, skin also possessed a surprising richness of non-resident fungi, including plant pathogens such as ergot (Claviceps purperea). Overall, fungal richness across indoor surfaces was high, but based on known autecologies, most of these fungi were unlikely to be growing on surfaces. We conclude that while some endogenous fungal growth on typical household surfaces does occur, particularly on drains and skin, all residential surfaces appear – to varying degrees – to be passive collectors of airborne fungi of putative outdoor origin, a view of the origins of the indoor microbiome quite different from bacteria.
PMCID: PMC3815347  PMID: 24223861
23.  Use of a robotic sampling platform to assess young children's exposure to indoor bioaerosols 
Indoor Air  2011;22(2):159-169.
Indoor exposures to allergens, mold spores and endotoxin have been suggested as etiological agents of asthma; therefore, accurate determination of those exposures, especially in young children (6–36 months), is important for understanding the development of asthma. Since use of personal sampling equipment in this population is difficult, and in children < 1 year of age impossible, we developed a personal sampling surrogate: the Pretoddler Inhalable Particulate Environmental Robotic sampler (PIPER) to better estimate their exposures. During sampling, PIPER simulates the activity patterns, speed of motion and the height of the breathing zones of young children, and mechanically resuspends the deposited dust just as a young child does during running and crawling. The concentrations of allergens, mold spores and endotoxin measured by PIPER were compared to those measured using traditional stationary air sampling in 75 homes in central New Jersey, US.
Endotoxin was detected in all homes with median concentrations of 1.0 and 0.55 EU/m3 for PIPER and stationary sampler, respectively. The difference in median concentrations obtained using the two methods was statistically significant for homes with carpeted floors (p= 0.0001) in the heating season. For such homes, the average ratio of endotoxin concentration measured by PIPER and the stationary sampler was 2.96 (95% CI 2.29–3.63).
Fungal spores were detected in all homes, with median fungal concentrations of 316 and 380 spores/m3 for PIPER and stationary sampler, respectively. For fungi, the difference between the two sampling methods was not statistically significant. For both sampling methods, the total airborne mold levels were statistically significantly higher in the non-heating season than in the heating season. Allergens were detected in ~15% of investigated homes.
The data indicate that the traditional stationary air sampling methods may substantially underestimate personal exposures to endotoxin, especially due to resuspension of dust from carpeted floor surfaces. A personal sampling surrogate, such as PIPER, is a feasible approach to estimate personal exposures in young children. PIPER should be seriously considered as the sampling platform for future exposure studies in young children.
PMCID: PMC3260414  PMID: 21954880
Children's exposures; Robotic sampling platform; PIPER; Bioaerosol; Resuspension; Floor type
24.  Microbiological Quality of Indoor Air in University Libraries 
To evaluate the concentration of bacteria and fungi in the indoor environment of Jimma University libraries, so as to estimate the health hazard and to create standards for indoor air quality control.
The microbial quality of indoor air of eight libraries of Jimma University was determined. The settle plate method using open Petri-dishes containing different culture media was employed to collect sample twice daily. Isolates were identified according to standard methods.
The concentrations of bacteria and fungi aerosols in the indoor environment of the university libraries ranged between 367-2595 CFU/m3. According to the sanitary standards classification of European Commission, almost all the libraries indoor air of Jimma University was heavily contaminated with bacteria and fungi. In spite of their major source difference, the average fungi density found in the indoor air of libraries did appear to follow the same trend with bacterial density (P=0.001). The bacteria isolates included Micrococcus sp., Staphylococcus aureus, Streptococcus pyogenes, Bacillus sp. and Neisseria sp. while Cladosporium sp., Alternaria sp., Penicillium sp. and Aspergillus sp. were the most isolated fungi.
The indoor air of all libraries were in the range above highly contaminated according to European Commission classification and the most isolates are considered as potential candidates involved in the establishment of sick building syndromes and often associated with clinical manifestations like allergy, rhinitis, asthma and conjunctivitis. Thus, attention must be given to control those environmental factors which favor the growth and multiplication of microbes in indoor environment of libraries to safeguard the health of users and workers.
PMCID: PMC4025286  PMID: 25183103
Indoor air; Open-plate technique; Microbiological assessment; Bacteria; Fungi; Sedimentation technique
25.  Sensitization to Indigenous Pollen and Molds and Other Outdoor and Indoor Allergens in Allergic Patients From Saudi Arabia, United Arab Emirates, and Sudan 
Airborne allergens vary from one climatic region to another. Therefore, it is important to analyze the environment of the region to select the most prevalent allergens for the diagnosis and treatment of allergic patients.
To evaluate the prevalence of positive skin tests to pollen and fungal allergens collected from local indigenous plants or isolated molds, as well as other outdoor and indoor allergens in allergic patients in 6 different geographical areas in the Kingdom of Saudi Arabia (KSA), the United Arab Emirates, and Sudan.
Materials and methods
Four hundred ninety-two consecutive patients evaluated at different Allergy Clinics (276 women and 256 men; mean age, 30 years) participated in this study. The selection of indigenous allergens was based on research findings in different areas from Riyadh and adjoining areas. Indigenous raw material for pollen grains was collected from the desert near the capital city of Riyadh, KSA. The following plants were included: Chenopodium murale, Salsola imbricata, Rumex vesicarius, Ricinus communis, Artiplex nummularia, Amaranthus viridis, Artemisia monosperma, Plantago boissieri, and Prosopis juliflora. Indigenous molds were isolated from air sampling in Riyadh and grown to obtain the raw material. These included the following: Ulocladium spp., Penicillium spp., Aspergillus fumigatus, Cladosporium spp., and Alternaria spp. The raw material was processed under Good Manufacturing Practices for skin testing. Other commercially available outdoor (grass and tree pollens) and indoor (mites, cockroach, and cat dander) allergens were also tested.
The highest sensitization to indigenous pollens was detected to C. murale (32%) in Khartoum (Sudan) and S. imbricata (30%) and P. juliflora (24%) in the Riyadh region. The highest sensitization to molds was detected in Khartoum, especially to Cladosporium spp. (42%), Aspergillus (40%), and Alternaria spp. (38%). Sensitization to mites was also very prevalent in Khartoum (72%), as well as in Abu Dhabi (United Arab Emirates) (46%) and Jeddah (KSA) (30%).
The allergenicity of several indigenous pollens and molds derived from autochthonous sources was demonstrated. Prevalence studies in different regions of KSA and neighbor countries indicate different sensitization rates to these and other outdoor and indoor allergens.
PMCID: PMC3651151  PMID: 23283107
allergens; diagnostics; bronchial asthma; allergic rhinitis; Saudi Arabia; Salsola; Prosopis; mites

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