Copyright Blackwell Munksgaard 2003
Allergy 2003: 58: 13–20
Printed in UK. All rights reserved
ALLERGY
ISSN 0105-4538
Original article
Dustborne and airborne fungal propagules represent a different
spectrum of fungi with differing relations to home characteristics
Background: Exposure to fungi is often assessed by culturing floor dust or air
samples. Our objective was to evaluate the relationships between dustborne and
airborne fungi and to identify factors that modify these relationships.
Methods: From November 1994 to September 1996 sequential duplicate 45-l air
samples were collected in bedrooms of 496 homes in the Boston area, using a
Burkard culture plate sampler. After air sampling, bedroom floors were sampled
with a vacuum cleaner that was modified to collect dust in a cellulose extraction
thimble. Dust was sieved, and the fine dust was dilution-plated onto DG-18
media.
Results: Concentrations of total culturable fungi per gram of bedroom-floor dust
were correlated weakly, but significantly, with those of indoor air (r ¼ 0.13,
P < 0.05). Concentrations of some individual taxa in the dust and indoor air
were also weakly associated. Adjusting for the concentrations of fungi in outdoor air, dustborne fungal concentrations were positively associated with those
in indoor air for the taxa Cladosporium and Penicillium, but not for total fungi.
The indoor air fungal levels were often predicted by different covariates to those
predicting fungal levels in dust. The type of housing (house or apartment) and
the presence of carpeting were often predictive factors for dust fungi. In contrast,
outdoor fungal levels were often predictive of the indoor air fungal levels.
Conclusions: Because our data do not indicate a strong overall relationship
between culturable fungi in dust and indoor air, the results from these two
methods (dust and air sampling) likely represent different types of potential fungal
exposures to residents. It may be essential to collect both air and dust samples, as
well as information on housing characteristics, as indicators for fungal exposure.
A recent report by the US National Academy of Sciences
stated that there was inadequate or insufficient evidence
to determine whether or not an association exists between
fungal exposure and the development of asthma (1).
However, two recent reviews of the effects of home
dampness and fungi have shown several positive associations between fungal exposure and increased risk of
adverse respiratory symptoms in children (2, 3). In
addition, exposure to unidentified outdoor fungal aerosols has been associated with decrements in peak flow in
asthmatic children (4). Sensitization to Alternaria, primarily an outdoor fungus, has been associated with
asthma exacerbations and asthma development in young
people (5–7), but associations between exposure to
Alternaria and these outcomes are as yet unknown.
One reason that study outcomes have been relatively
weakly associated with exposure is the possibly unrepresentative nature of exposure measures. Some studies
reporting associations between health and fungal exposure used questionnaires or direct observation to indicate
the presence of dampness or visible fungi; other studies
G. L. Chew1, C. Rogers2, H. A. Burge2,
M. L. Muilenberg2, D. R. Gold2,3
1
Department of Environmental Health Sciences,
Mailman School of Public Health, Columbia
University, New York; 2Department of Environmental
Health, Harvard School of Public Health; 3The
Channing Laboratory, Department of Medicine,
Brigham and Women's Hospital and Harvard
Medical School, Boston
Key words: air sampling; dust sampling; fungi; home
characteristics; mold.
Dr Ginger L. Chew
Mailman School of Public Health
Columbia University
60 Haven Avenue B-1
New York NY 10032–4206
USA
Accepted for publication 13 September 2002
used a variety of measures, including culture of air and
dust samples (8). All of these methods have limitations
that are yet to be clearly documented. In addition,
different hypotheses being tested by measurement of
fungal exposure require different approaches (9). In a
study of daily symptoms, asthma medication use, and/or
peak flow variability, one might wish to estimate the daily
inhaled concentration of fungal spores (and possibly their
associated antigens, mycotoxins, volatile organic compounds, etc.). However, to study chronic effects such as
development of allergic sensitization, an estimate of timeaveraged and/or cumulative fungal exposure might be of
more interest. Ideally, fungal exposure assessment would
include information about the biologically relevant
inhaled dose of fungal spores and associated agents
during an individual’s lifetime.
Since the latter is not yet possible several large
epidemiological studies have used dust or air cultures as
surrogates for exposure to fungi (10–16). Our objective
was to evaluate the relationships between dustborne and
airborne fungi in residential environments, to examine
13
Chew et al.
factors that might alter these relationships, and to
comment on the usefulness of collecting both types of
data as estimates for childhood fungal exposure.
Material and methods
Home selection
From November 1994 to September 1996 we analyzed dust samples
from 397 homes and air samples from 496 homes. These homes were
from part of a prospective cohort study of 505 newborn babies in
499 homes, which was designed to identify relationships between
exposure to indoor allergens and the development of allergic sensitization and asthma (17). Homes were selected on the basis of 1)
the presence of a newborn child with a familial predisposition for
development of asthma (based on parental history of physiciandiagnosed asthma or allergy (18), 2) proximity to the city of Boston,
and 3) the stated intention of the parents not to change residence
during the first year of follow-up. Informed consent was obtained
from participating mothers in accordance with the institutional
review board of Brigham and Women’s Hospital.
Home characteristics
At the same time of air and dust sampling, a second field technician
administered a home characteristics questionnaire to an adult
occupant of each home. This included questions about the building
structure, number of occupants, type of heating, home dampness,
the presence of fungi, type of floor covering, presence of pets, and
frequency of cleaning (Table 1).
Air sampling
Indoor and outdoor air samples were collected from each home
using a Burkard culture plate sampler (Burkard Manufacturing,
Herefordshire, England) operated at 45 l/min (calculated cutpoint (D50) ¼ 2 (lm), which collected particles onto Dichloran
glycerol agar in 90-mm Petri dishes. D50 ¼ 50% of the airborne
particles that have an aerodynamic equivalent diameter
(AED) ¼ 2 lm will be impacted on the culture plate and 50%
will not be collected. The collection efficiency of particles with an
AED greater than 2 lm will be higher than 50% (given that the
flow rate is constant).
Sequential duplicate 1-min outdoor air samples were collected
3 m from the main entrance of each home. The field technician then
collected sequential duplicate 1-min air samples in the bedroom 1–
1.5 m above the area of the floor demarcated for dust collection.
The sampler sieve-plate was cleaned between sample collections
with an isopropanol swab. After sampling, the four Petri plates were
returned to the laboratory on the same day for incubation.
Dust collection
Variable
Type of building*
Apartment
House
Surface from which dust sample was collected
Smooth
Any carpet
Dog present in home
No
Yes
Cat present in home
No
Yes
Mold/mildew anywhere in home during past year No
Yes
Mold/mildew in bathroom during past year No
Yes
Mold/mildew in living room during past year No
Yes
Water damage in building during past year No
Yes
Concrete floor in child's bedroom
No
Yes
Humidifier used in child's bedroom during past day
No
Yes
Air conditioner in child's room
No
Yes
Dehumidifier used in summer months
No
Yes
N (%)
118 (24%)
381 (76%)
135 (27%)
364 (73%)
420 (84%)
79 (16%)
396 (79%)
103 (21%)
304 (62%)
188 (38%)
350 (70%)
148 (30%)
480 (96%)
19 (4%)
324 (66%)
168 (34%)
418 (94%)
27 (6%)
416 (83%)
83 (17%)
457 (92%)
40 (8%)
411 (82%)
88 (18%)
* Apartment buildings contained three or more units. Houses and duplexes were
grouped into one category.
Resident report of mold/mildew or water damage.
Temperature and relative humidity measurements
In each house, a psychrometer was placed on the bedroom floor and
wet-bulb and dry-bulb temperatures were recorded after a 3-min
equilibration period. Relative humidity (% RH) was calculated
from these two temperatures using the American Society of Testing
and Materials Method E337 (19).
Fungal analysis
2
After air samples were collected, 2 m of the floor surrounding the
newborn’s bed was vacuumed for 5 min, using a Eureka MightyMite canister vacuum cleaner (The Eureka Co, Bloomington, IN)
modified to collect dust in a 19 · 90-mm cellulose extraction thimble
(Whatman International, Maidstone, UK). In rooms with both a
smooth floor and a rug, 2.5 min was spent sampling each. After
sampling, the thimble was sealed in a plastic bag and returned to the
laboratory the same day for sifting (425-lm mesh sieve) and
weighing.
14
Table 1. Housing characteristics of study cohort
Fine dust was suspended (approximately 25 mg/ml) and serially
diluted (e.g. full strength, 1 : 10, 1 : 100) in a 0.02% Tween 20 solution. Duplicates of undiluted and diluted suspensions (100 ll
each) were spread-plated on DG-18 culture media. After at least
10 days of incubation (room temperature and standard fluorescent
lighting), fungal colonies on both air- and dust-sample plates were
identified to genus (subgenus in the case of Aspergillus isolates)
using standard mycological criteria (20, 21). The dilution of dust
samples with a yield closest to 10–30 colonies was used for colony
Dustborne and airborne fungi
identification and counting. The number of colonies recovered on
the air-sample plates was adjusted for multiple impactions through
a sieve-plate hole using a positive-hole correction equation (22). The
calculated concentrations of dustborne fungi were colony forming
units(cfu)/g of dust, and those of airborne fungi were cfu/m3 of air.
The number of fungal taxa recovered from dust samples was reported as number of taxa/total area sampled (i.e. 2 m2). For air
samples, the number of taxa/total volume sampled (i.e. 90 l) was
reported.
Statistical analysis
Air–dust comparisons of fungi. Inter- and intrahome variation of
number of taxa recovered and concentration of total fungi was
calculated for indoor and outdoor air samples as well as for dust
samples. As a surrogate for reproducibility of replicate samples,
reproducibility between duplicate culture plates was assessed by
Spearman rank correlation. Colony counts from duplicate plates of
dustborne fungi were averaged, as were the duplicate air sample
counts. For categorical analyzes, concentrations of fungi were
dichotomized using the 50th percentile of each taxon as the
cutpoint. For fungal taxa with a 50th percentile equal to zero
(i.e. rare fungal taxa) regression analyzes could not be performed.
Stepwise logistic regression was used to identify seasonal factors
and home characteristics that explained the variation in airborne
and dustborne fungi. There were four season categories: winter
(November–February), spring (March–May), summer (June–August),
and fall (September–October). Home characteristics were treated as
dichotomous categories. All data were analyzed using the sas
statistical software package (SAS Institute, Cary, NC).
Results
Quantitative results are presented in Tables 2–5, and
Fig. 1.
All outcome variables were positively skewed. Table 2
reveals the wide variability observed about the mean
concentrations of culturable fungi for indoor and outdoor air samples and dust samples. Variation in reproducibility was also observed between the duplicates of
culture plates from the dust, and especially the air
samples (Table 3). However, high correlations between
duplicate plates of air samples were evident for the more
common fungal taxa.
Figure 1 shows the frequencies of the most commonly
recovered taxa from air and dust samples. Yeasts were
recovered with greater frequency from dust than from air.
Nonsporulating fungi, Penicillium and Cladosporium were
the most frequently recovered taxa from indoor and
outdoor air samples, and they were frequently recovered
from dust (Fig. 1).
Fungi in indoor and outdoor air
Fewer colonies were recovered from indoor air samples
compared to outdoors (Wilcoxon signed rank test,
P ¼ 0.0001). Levels of total culturable fungi in indoor
and outdoor air were correlated (r ¼ 0.58, P ¼ 0.0001).
The number of fungal taxa per plate was not significantly
Table 2. Concentrations of fungi and numbers of taxa from different locations
Number of taxa
recovered
Concentration
Variable
Mean (SD)
Median Mean (SD) Median
Air samples
300
Indoor air (n ¼ 496) 580 (1 278) cfu/m3
Outdoor air (n ¼ 392) 986 (1 815) cfu/m3
511
Dust samples (n ¼ 397) 200 473 (782 038) cfu/g 71 667
4.7 (1.9)*
4.6 (1.8)*
8.4 (2.2) 5
5
9
SD, standard deviation.
* Number of taxa per 90-l air sample.
Number of taxa per 2 m2 of floor area dust.
Table 3. Spearman rank correlation coefficients (r) for duplicate sampling plates
Air samples r
Fungal taxa
Indoor
Outdoor
Dust samples r
Alternaria
Aspergillus niger
Aspergillus ochraceous
Aspergillus versicolor
Aureobasidium
Botrytis
Cladosporium
Coelomyces
Eurotium
Nonsporulating fungi
Penicillium
Pithomyces
Wallemia
Yeasts
Zygomycetes
Total
0.29 0.38 0.08
0.41 0.26 0.40 0.85 0.22 0.41 0.70 0.62 0.11 0.50 0.38 )0.01
0.92 0.33 0.15 )0.01
0.11*
0.39 0.33 0.89 0.07
0.12*
0.79 0.57 0.11*
)0.02
0.39 1.00 0.92 0.80 0.86 1.00 0.87 0.86 0.89 0.52 0.92 0.90 0.86 0.86 0.50*
0.95 0.83 0.93 0.96 * P < 0.05.
P < 0.01.
Table 4. Regression models for indoor airborne fungi (concentrations of fungi were
dichotomized using the 50th percentile of each taxon as the cutpoint)
Explanatory variable*
Odds ratio
(95% confidence interval)
Total indoor airborne fungi
Relative humidity (% RH)
Total outdoor fungi
Apartment
1.08 (1.05–1.11)
4.70 (2.57–8.57)
0.37 (0.19–0.71)
Cladosporium
Winter
Spring
Outdoor Cladosporium
Dustborne Cladosporium
0.02
0.03
2.57
2.93
Penicillium
Dustborne Penicillium
Outdoor Penicillium
1.97 (1.22–3.16)
3.28 (2.01–5.34)
Outcome variable
(0.01–0.05)
(0.01–0.08)
(1.20–5.50)
(1.44–5.96)
* The reference category for season is fall, and for apartment is a house or building
with two or fewer units.
different for indoor and outdoor air samples (Table 2),
and similar taxa were dominant in the two kinds of
samples (Fig. 1).
15
Chew et al.
Table 5. Regression models for dustborne fungi (concentrations of fungi were
dichotomized using the 50th percentile of each taxon as the cutpoint)
Outcome variable
Explanatory variable*
Odds ratio (95% CI)
Total dustborne fungi (cfu/g)
Outdoor total fungi
Carpeted surface
Dehumidifier use in summer
1.63 (1.01–2.63)
3.38 (1.76–6.50)
2.12 (1.12–4.00)
Alternaria
Carpeted surface
Dog
Winter
Spring
4.05
2.03
0.59
0.39
Aspergillus versicolor
Relative humidity
Summer
Apartment
0.98 (0.96–0.99)
0.56 (0.33–0.95)
0.38 (0.23–0.65)
Aureobasidium
Carpeted surface
Winter
Apartment
3.42 (1.94–6.02)
1.82 (1.16–2.85)
0.49 (0.29–0.82)
Cladosporium
Carpeted surface
Dehumidifier use in summer
Apartment
2.83 (1.50–5.34)
2.51 (1.28–4.94)
0.44 (0.25–0.78)
Eurotium
Carpeted surface
Winter
Apartment
3.30 (1.91-5.68)
1.73 (1.10–2.74)
0.42 (0.25–0.69)
Penicillium
Carpeted surface
Winter
Apartment
2.40 (1.28–4.53)
1.91 (1.11–3.31)
0.47 (0.27–0.83)
Yeasts
Carpeted surface
3.37 (1.92–5.89)
(2.26–7.24)
(1.10–3.75)
(0.36–0.97)
(0.23–0.67)
* The reference category for season is fall, for dog is no report of dog in the home,
for carpeted surface is a smooth surface, for apartment is a house or building with
two or fewer units, and for dehumidifier use in summer is no dehumidifier used
during summer.
CI, confidence interval.
Fungal relationships between air and dust
Logistic regression analyzes revealed that some indoor-air
fungi were significantly associated with outdoor-air fungi
in addition to the fungi vacuumed from the floors
(Table 4). For example, the odds of recovering a high
level of Cladosporium (greater than the 50th percentile of
Cladosporium) in indoor air were 2.57 times higher if the
outdoor concentration was also high. In contrast, only
total fungi in the dust (not individual taxa) were
significantly associated with their outdoor air concentrations (Table 5).
Sampling season
Some of the strongest relationships observed in this study
were between season and airborne concentrations of fungi
(Table 4). For example, the concentration of Cladosporium in indoor air was lower in winter and spring compared
to the referent season (fall). Conversely, an opposite trend was observed for many of the dustborne fungi (e.g. Aspergillus versicolor, Aureobasidium,
16
Eurotium (the teliomorph of Aspergillus glaucus group,
and Penicillium) (Table 5), with the exception of
Alternaria.
Housing characteristics
The type of housing was significantly associated with
indoor air and dust concentrations of total fungi and
several individual fungal taxa; apartments had lower
levels of many fungal taxa. The effect of type of housing
was significant for Cladosporium and Penicillium in dust
samples, but was not evident for these taxa in indoor air.
Percent relative humidity (% RH) inside the homes
ranged from 14% to 77%. Regression analysis showed
that indoor % RH is a significant independent predictor
of total indoor air fungi (Table 4). In addition, the
reported use of a dehumidifier in the summer was
positively associated with dust concentrations of total
fungi and Cladosporium (Table 5). Other measures of
home dampness, such as report of water damage or mold/
mildew in the building during the past year, were not
associated with concentrations of fungi in air or dust.
Concentrations of fungi were higher in dust from
carpeted floors compared to smooth floors (Table 5).
However, no fungi in indoor air were associated with
carpeted floors (Table 4). Overall, adjusting for type of
floor covering did not significantly change the association
between dustborne and airborne fungi.
Another characteristic associated with fungi in the dust
was the presence of a dog in the home. Positive
associations were found between dog in the home and
high levels of Alternaria in dust (Table 5).
Discussion
Air–dust relationships
Dust sampling is often a surrogate measure for respiratory exposure to fungi. This practice assumes that fungi in
dust are representative of past and continuing airborne
exposure. It is likely that cumulative or average fungal
exposure is more relevant to health outcomes than a
single day’s exposure. Our data do not show the extent to
which our measures are representative of long-term
exposure. Overall, however, we saw very little association
between culturable fungi in indoor air and dust. This
leads to two hypotheses: firstly, dust populations are
unique and may not generally be representative of
airborne exposure; secondly, our short-term air samples
were not representative of long-term air concentrations
that might be associated with dust levels, and dust does
represent (primarily) spores that have settled from air
over longer periods of time.
The first hypothesis is supported by the fact that some
common dust fungi were rarely recovered from air and
that several fungi were unique to dust. It may be that dust
Dustborne and airborne fungi
Figure 1. Predominant fungi cultured from house-dust samples collected from dust and indoor and outdoor air. Each bar represents
the percentage of homes where at least one colony of a given fungal taxon was recovered.
represents only a selection of the hardy kinds of spores
entering from outdoor air along with those that can grow
and produce new spores in dust.
The second hypothesis is supported by the logic that
exposure occurs over much longer periods than our very
limited sampling times, and that populations of airborne
spores are known to vary dramatically over time. Thus,
it is true that on any on sampling occasion a short-term
air sample is unlikely to represent exposure over time.
This hypothesis is supported in our data by the strong
relationships between outdoor and indoor air fungi, but
not for outdoor air and dust, indicating that on a
day-to-day basis outdoor air is more representative of
indoor air than is dust, and a combination of outdoor
air and dust sampling may be appropriate for assessing
exposure. Furthermore, like the studies by Beaumont
et al. (23) and Su et al. (24), we found that levels of
airborne fungi were lowest in the winter and highest in
the summer and fall. Our study was limited by the
absence of information about the day of sampling,
whether the bedroom window had been open or closed,
and about the weather. These factors may have influenced air fungal levels, or taxa, and therefore the air–
dust relationship. Extensive literature supports the
hypothesis that airborne levels of fungi are influenced
by weather (25–27).
Home characteristics contributing to air–dust
fungal differences
Apartments may not have such high concentrations of
fungi as houses, because the dirt tracked in through the
main entrance (possibly a source of air- and dustborne
fungi) might be diminished by the longer walk to an
17
Chew et al.
apartment. Apartments in Boston are also warmer and
drier during the winter than houses (28). This warm dry
environment may lead to loss of viability of airborne and
dustborne fungi.
Carpeted floors contained higher dustborne fungal
concentrations than smooth floors. Carpeting may provide a microenvironment that maintains the culturability
of fungi, or may even encourage fungal growth under
some circumstances. On the other hand, carpeting did not
predict higher levels of airborne fungi.
There are differences between studies in the relations
between home characteristics and indoor-dust fungal
concentrations. These differences might arise from the
varied methods of sampling and analysis, but also from
cultural differences in home furnishings and housing
stock, and atmospheric conditions (29–31). As in another
study in northeast USA, we found that concentrations of
some fungal taxa were higher in homes with dogs (31).
Positive associations between dogs and dustborne Alternaria may result from dogs tracking in these saprophytic
fungi from outside.
We compared the air–dust relationships of fungi only
in bedrooms. Other locations may have produced different results. For example, dust collected outside the main
entrance may have been more influenced by the outdoor
fungal aerosol, which may have affected indoor airborne
levels (14,29).
Resident reports of mold or mildew and water damage
were not significantly associated with higher levels of
fungi in the air or in the dust. Several studies have found
an association (11,12,30,32), but the subjectivity of
reports of dampness may have affected our statistical
analyzes. If we had sampled more homes with severe
water damage or fungal contamination, statistically
significant associations between home dampness and
fungal measurements might have been observed.
Air–dust differences in taxon frequencies
Overall, many of the fungal taxa that we recovered (e.g.
Penicillium, Cladosporium, Alternaria, Aspergillus) were
similar to those found commonly in other studies of
residential environments (11,12,23,31,33,34). The abundance of yeast in dust as compared to air may reflect their
better survival in dust than in air, and their lack of
dispersion.
Comparing dust and air sampling cultural data is
difficult because of the way the fungal units reach the
18
culture plates. Air samples are impacted directly onto an
agar surface, and a clump of fungi could lead to only one
colony forming unit. However, when dust is suspended in
solution, clumps of fungi could be broken, and each unit
could produce an individual colony. Fungi that tend to
travel as clumps of spores (e.g. Cladosporium species) are
more likely to be affected by this phenomenon than those
that tend to occur as single spores (e.g. Alternaria
species).
The use of culture analysis to detect fungi in either dust
or air samples means exclusion of some types of fungi.
Spores may be unable to grow in culture because they are
nonviable, or they are viable but injured, or because the
nutrients or temperature conditions are not appropriate,
or they are exposed to inhibitors (including those from
other fungi). Thus, the level of fungal growth in the
culture plate may be only loosely related to the level in the
environment.
Fungi need not be alive to elicit respiratory symptoms (35). While air-sampling methods are available
that produce total spore counts (regardless of viability),
comparable methods are not available for dust analysis.
Immunoassays for specific fungal antigens (e.g. Asp f1,
fungal extracellular polysaccharides (EPS)), or assays
for total fungal biomass (e.g. ergosterol, possibly b1)3glucans) offer some options. However, there are few of
these assays (36–40) and they have limitations
as estimates of biologically relevant exposure to fungi
(41).
With all the caveats discussed above, several epidemiological studies have shown associations between
culturable fungi and increased risk of adverse respiratory symptoms (24,32,42). Measures of culturable airborne fungi, dustborne fungi, and home characteristics,
likely provide different and complementary information
regarding the presence of fungi that may be inhalable
on a short-term or chronic basis. It is essential to
understand the ecologic and methodological reasons for
differences in the taxa and fungal levels obtained from
culture of air and dust fungi, so enable interpretation of
epidemiological studies of the health effects of airborne
fungi.
Acknowledgments
This work was supported by grants HL-07427 and AI-35786 from
the National Institutes of Health.
Dustborne and airborne fungi
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