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Applied and Environmental Microbiology, May 2000, p. 1899-1904, Vol. 66, No. 5
Finnish Institute of Occupational Health
(FIOH), Uusimaa Regional Institute, FIN-00370
Helsinki,1 City of Vantaa Environment
Center, FIN-01300 Vantaa,2 City of
Helsinki Environment Center, FIN-00530
Helsinki,3 and HUCH Diagnostics,
Mycological Laboratory,4 and Department
of Dermatology and Allergic Diseases,5
Helsinki University Central Hospital, FIN-00250 Helsinki, Finland
Received 7 September 1999/Accepted 1 March 2000
We analyzed 79 bulk samples of moldy interior finishes from Finnish
buildings with moisture problems for 17 mycotoxins, as well as for
fungi that could be isolated using one medium and one set of growth
conditions. We found the aflatoxin precursor, sterigmatocystin, in 24%
of the samples and trichothecenes in 19% of the samples.
Trichothecenes found included satratoxin G or H in five samples;
diacetoxyscirpenol in five samples; and 3-acetyl-deoxynivalenol,
deoxynivalenol, verrucarol, or T-2-tetraol in an additional five
samples. Citrinine was found in three samples. Aspergillus
versicolor was present in most sterigmatocystin-containing samples, and Stachybotrys spp. were present in the samples
where satratoxins were found. In many cases, however, the presence of fungi thought to produce the mycotoxins was not correlated with the
presence of the expected compounds. However, when mycotoxins were
found, some toxigenic fungi usually were present, even if the species
originally responsible for producing the mycotoxin was not isolated. We
conclude that the identification and enumeration of fungal species
present in bulk materials are important to verify the severity of mold
damage but that chemical analyses are necessary if the goal is to
establish the presence of mycotoxins in moldy materials.
Mycotoxins are "natural products
produced by fungi that evoke a toxic response when introduced in low
concentrations to higher vertebrates by a natural route" (J. W. Bennett, Editorial, Mycopathologia 100:3-5, 1987). These
compounds can cause a wide range of acute and chronic systemic effects
in humans and animals that cannot be attributed to fungal growth within
the host or allergic reactions to foreign proteins (22). The
over 400 known mycotoxins are all complex organic compounds, most with
molecular masses between 200 and 800 kDa (40), that are not
volatile at ambient temperatures. Inhalant exposure to mycotoxins can
occur by inhaling airborne particulates containing mycotoxins,
including dust and fungal components. In agricultural settings,
mycotoxicoses in both farm animals and humans can result from oral,
dermal, or inhalant exposure of mycotoxin-contaminated grain or dust
(for reviews, see references 4, 11, 12, 23, 36, 38,
and 41). In laboratory mammals, symptoms can be
induced by systemic, oral, dermal, subcutaneous, or inhalant exposure
(25, 44), with inhalant exposure in some cases being several
orders of magnitude more toxic than dermal or even systemic
administration (13, 32, 34).
Toxigenic fungi have been isolated from building materials and air
samples in buildings with moisture problems, where the residents have
suffered from nonspecific symptoms possibly related to mycotoxin
production, such as cough; irritation of eyes, skin, and respiratory
tract; joint ache; headache; and fatigue (3, 8-10, 24, 27, 29,
37, 39). In some cases involving Stachybotrys chartarum (Ehrenberg ex Link) Hughes, exposure has resulted in pulmonary hemorrhage (8-10), and S. chartarum
isolates from such sites have been shown to produce a number of
mycotoxins, including satratoxins (26). Very few studies
have, however, established a causal relationship between mycotoxin
exposure and building-related illnesses (reviewed in reference
19).
All known mycotoxins are fungal secondary metabolites, which means that
mycotoxin production need not be correlated with the growth and
proliferation of the producing species and that factors such as
induction, end product inhibition, catabolite repression, and phosphate
regulation will determine production (6, 7). Therefore, even
though some fungi can grow on almost any natural or synthetic
construction material, mycotoxin production occurs preferentially on
materials that both allow these fungi to grow and provide the
conditions for mycotoxin production. From the many studies of the
production of mycotoxins by fungal isolates derived from agricultural
environments, a great deal is known about the fungal species that are
capable of producing known mycotoxins and about the growth media and
conditions that induce production (5, 14, 25, 28). It is
known that some species include strains that produce mycotoxins and
others that lack this ability (6, 7). It also has been
established that many of the known mycotoxin producers are frequent
colonizers in indoor environments (30, 35, 37). Less is
known, however, about the presence of mycotoxins in indoor
environments, and it is only in recent years that the presence of some
mycotoxins has been verified in crude building materials (1,
14, 21, 27, 40, 41a). In fact, most mycotoxins have yet to be
extracted from either air samples or bulk material derived from indoor environments.
Satratoxins belong to the macrocyclic trichothecene class of
mycotoxins. Over 100 trichothecenes with irritatory and
immunosuppressive effects are known (43). Most
trichothecenes were originally isolated from species of
Fusarium, but they also may be produced by other fungi, such
as species of Stachybotrys, Trichothecium, Cylindrocarpon, Myrothecium,
Trichoderma, Vertinosporum, and
Acremonium (5, 14, 28, 43). Other mycotoxins
potentially present in indoor environments include the carcinogenic
aflatoxins and their precursor, sterigmatocystin, which has
immunosuppressive and carcinogenic properties. Fumonisins, ochratoxins
(nephrotoxic and carcinogenic), zearalenone (estrogenic), gliotoxin
(immunosuppressive), patulin (carcinogenic and neurotoxic), and
citrinine (nephrotoxic) also may be present (reviewed in reference
22). Penicillium and
Aspergillus species also may produce mycotoxins, commonly found in association with indoor air problems (18).
Aspergillus ochraceus Wilhelm (ochratoxin A),
Aspergillus fumigatus Fresenius (fumitremorgins, gliotoxin,
and verrucologen), Aspergillus versicolor (Vuillemin)
Tiraboschi (sterigmatocystin), Aspergillus flavus Link
(aflatoxins), Aspergillus parasiticus Speare (aflatoxins), and Penicillium citrinum Thom (citrinine) are among those of
particular concern (16-18, 22). Sterigmatocystin also may
be produced by A. flavus, Aspergillus nidulans,
Aspergillus rugulosus, Aspergillus unguis,
Bipolaris spp., and Chaetomium spp., while
Penicillium verrucosum and Penicillium
viridicatum may produce citrinine (5, 14, 25, 28).
In the present study, over a period of 4 months, we collected samples
for mycotoxin analysis from four major environmental laboratories in
southern Finland that are collectively responsible for over 90% of the
mycological analyses performed on moisture problem sites in this area.
Samples were selected based on mycological analyses down to genus
level. A group of 17 mycotoxins likely to be encountered in indoor
environments were analyzed, including 4 macrocyclic trichothecenes, 10 nonmacrocyclic trichothecenes, citrinine, sterigmatocystin, and
ochratoxin A. As only one set of growth conditions was used to isolate
fungi growing on one particular medium, we did not attempt to identify
the fungi responsible for producing the mycotoxins in each case.
Rather, our objectives were to establish (i) whether these mycotoxins
occur in moisture problem sites, (ii) in what materials individual
mycotoxins occur, and (iii) which fungal species are associated with
mycotoxin-containing samples.
Sample composition.
We analyzed 79 bulk samples of moldy
interior finishes, including samples of wallpaper, cardboard, wood,
plywood, plasterboard, paper-covered gypsum board, mineral wool,
plaster, sand, soil, linoleum, polyurethane insulation, pipe
insulation, and paint. The samples were collected from buildings where
a moisture problem had been detected either by a municipal inspector or
by an occupational hygienist. Additionally, in all these buildings, the
examining inspector, hygienist, or physician had recorded the presence
of symptomatic individuals, or possibly a mold-induced disease. The 79-sample subset was selected from a larger group based on two criteria: (i) selected samples were usually covered with visible fungal
growth, and (ii) one or more of the following species dominated in CFU
measurements: Fusarium spp., Stachybotrys spp.,
Trichothecium spp., Cylindrocarpon spp.,
Myrothecium spp., Trichoderma spp., Verticinosporum spp., Acremonium spp.,
Bipolaris spp., Chaetomium spp., A. fumigatus, A. ochraceus, A. nidulans,
A. flavus, A. unguis, A. versicolor,
A. rugulosus, P. verrucosum, P. citrinum, and P. viridicatum. Samples were collected
over a period of 4 months by health inspectors, occupational
hygienists, or environmental inspectors and made available to us by the
City of Helsinki Environment Center, Helsinki, Finland; the City of
Vantaa Environment Center, Vantaa, Finland; the Finnish Institute of
Occupational Health (FIOH), Uusimaa Regional Institute, Helsinki,
Finland; HUCH Diagnostics, Mycological Laboratory, Helsinki University
Central Hospital, Helsinki, Finland; and the Department of Dermatology
and Allergic Diseases, Helsinki University Central Hospital.
Isolation and identification of fungal species.
Fungal
propagules were isolated from a suspension of 10 g of material in
90 ml of buffer solution (0.3 mM KH2PO4, 2.1 mM
MgSO4, 2 mM NaOH, 0.02% Tween 80). Dilutions from
10 Preparation and analysis of mycotoxin samples.
Mycotoxins
were extracted with aqueous 95% methanol, purified by a hexane wash
and solid-phase extraction, separated by reverse-phase high-pressure
liquid chromatography (HPLC), identified by tandem mass spectrometry,
and quantified using electrospray ionization (ESI) on a quadrupole ion
trap mass analyzer, as described previously (42).
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Mycotoxins in Crude Building Materials from
Water-Damaged Buildings
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
INTRODUCTION
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
MATERIALS AND METHODS
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
2 to 105 were spread on 2% malt extract
agar (Difco, Detroit, Mich.). Plates were incubated, in the dark, at
25°C for 7 days prior to enumeration and identification. Fungi were
identified morphologically to species or genus level.
3.24 V, and the second was 6.5 V, with the
interoctapole lens voltage set at 16 V and the octapole RF amplitude
at 400. The electron multiplier voltage was set to 800 V. For
collision-induced dissociation experiments, the relative collision
intensity in the ion trap varied from 12.6 (verrucarol) to 25.0 (satratoxin H [SATH] and RDRA). Maximum injection time was 200 ms,
and total microscans were set to 3. Samples were not analyzed in
replicates. To each sample, 2 µg of the alkaloid reserpine was added
as an internal standard prior to the extraction procedure. Each sample series of six samples contained one or more blank samples to exclude the possibility of false positives. Blank samples were analyzed prior
to injecting the actual samples and once more after the last sample had
been analyzed. The ion trap, particularly when used as a tandem mass
spectrometric device as in the present study, is qualitatively
reliable. However, the accuracy of the quantitative analysis was
limited by the characteristics of the ion trap, which is a
semiquantitative rather than a precise quantitative instrument (42).
Yields of the extraction and purification procedure ranged from 7 to
92%, and detection limits ranged from 0.02 to 200 ng (Table
1). Irrespective of the compound, the
intensity of at least two major fragments was used for quantitation
purposes (Table 1).
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RESULTS |
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Thirty-four of the 79 samples analyzed (43%) contained one or
more of the mycotoxins (Table 2).
Mycotoxins were found in most of the material categories tested, with
most (82%) of the mycotoxin-positive samples containing cellulosic
matter, such as paper, board, wood, or paper-covered gypsum board
(Table 3).
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Fifteen samples (19%) contained trichothecenes (Table 2), 5 containing the macrocyclic trichothecene satratoxin G or SATH, and 10 containing one of the nonmacrocyclic trichothecenes, diacetoxyscirpenol (DAS), deoxynivalenol (DON), 3-acetyl-DON (3-Ace-DON), T2-tetraol, or verrucarol. The most prevalent toxin was sterigmatocystin, which was detected in 19 samples (24%), while three samples (4%) contained citrinine (Table 2).
Fungi associated with mycotoxin-containing samples. Eighteen of 63 samples contaminated with Aspergillus spp. contained sterigmatocystin (Table 3), with A. versicolor occurring most frequently (13 samples). Three sterigmatocystin-containing samples did not yield any Aspergillus isolates. Species of Penicillium were isolated in two of the three cases where sterigmatocystin was found in the absence of Aspergillus spp. In addition to 14 samples containing sterigmatocystin, toxin-containing samples contaminated with Penicillium spp. included two of the three citrinine-containing samples. The majority of the 56 samples that contained Penicillium spp., however, were negative for both citrinine and sterigmatocystin (Tables 2 and 3). Species of Fusarium were detected in 12 samples, only two of which were associated with the production of nonmacrocyclic trichothecenes characteristic of Fusarium spp. (Tables 2 and 3). Satratoxins, with one exception, were found only in association with Stachybotrys species (Table 2).
Some species were more frequently associated with mycotoxin-containing materials, even when the toxins found were not characteristic of these species (Table 2). For example, A. ochraceus was found on eight occasions, all of which were associated with the production of mycotoxin. Yet, ochratoxin A, which is characteristic of this species, was not detected in any of the analyzed samples. On the other hand, all six samples containing Aspergillus niger were free from mycotoxin.| |
DISCUSSION |
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
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The present samples are a subset selected from a large pool of buildings with moisture problems and were biased in their microbiology as examined on one particular universal growth medium. Therefore, we cannot draw any conclusions regarding the fungal frequency on moisture-damaged building materials in general. One in five samples of material from which species of Aspergillus were recovered contained detectable levels of sterigmatocystin, making it the single most prevalent toxin in this study and, perhaps, indicating that sterigmatocystin is more ubiquitous than previously thought. As in previous studies (17, 21, 33), most sterigmatocystin-producing strains appeared to be A. versicolor, but it also is possible that this toxin may have been produced by Penicillium spp.
Spread plating on malt extract agar favors the growth of rapidly growing species of Aspergillus, Penicillium, and Alternaria at the expense of the generally slower-growing species of Stachybotrys, Acremonium, and Fusarium (20). The isolation of Fusarium spp. might require direct plating on medium specific for this purpose (2). In the present study, 15% of materials were contaminated with Fusarium species, but 10 of 12 samples containing nonmacrocyclic trichothecenes characteristic of Fusarium spp. yielded no Fusarium cultures. Verrucarol has been reported in Stachybotrys spp. (14), but judging from extensive reviews of the mycotoxins characteristic of different species of Fusarium and other fungi, it is highly unlikely that the other nonmacrocyclic trichothecenes present (DAS, DON, 3-Ace-DON, and T2-tetraol) originated from fungi other than Fusarium spp. (5, 28, 43). It seems that the procedure used to isolate the fungi left most of the Fusarium spp. undetected.
The mycology of the building materials did not correlate well with the toxin contents, although when a mycotoxin was found in a sample, representatives of a fungal genus known to contain toxigenic species were present. It is possible for toxigenic species with different growth requirements to be present in the same sample, as they may have proliferated during different stages of the water damage. For example, a surface may be overgrown by S. chartarum, which prefers cellulosic matter with a high water content, with nitrogen deficiency promoting satratoxin production, but at an earlier stage of the water damage, at a lower relative humidity, A. versicolor could have dominated.
Our findings agree with those of Gravesen et al. (21), in which sterigmatocystin was detected in 19 of 23 samples of building materials artificially contaminated with strains of Aspergillus sp. recovered from Danish buildings with moisture problems. They also found trichothecenes in six of eight natural samples tested. Previously, in Finnish water-damaged buildings, trichothecenes were detected in dust and construction material samples, as well as from samples of artificially enriched microbial media (41a). We hypothesize that sterigmatocystin and trichothecenes occur frequently in cellulosic construction materials of problem houses, where some of the fungi used to select the samples analyzed in the present study (A. ochraceus, Stachybotrys, Fusarium, Trichoderma, and Acremonium) have proliferated as a result of prolonged exposure to high water activities.
Risk assessment of the inhalation of mycotoxins cannot be made from the
analysis of bulk samples of construction materials, even if dose
responses of humans to airborne mycotoxins were known. However, as many
of the fungi that we isolated can elicit allergenic reactions in
addition to being toxic (15), it seems that care should be
exercised when moisture-damaged sites are torn down or renovated.
Sterigmatocystin is an International Agency for Research on Cancer
class 2B carcinogen (25) and also has immunotoxic properties
(5), while satratoxin G and SATH are probably the chemical
agents responsible for stachybotryotoxicosis in mammals (41). In a recent study (24), S. chartarum and A. versicolor were implicated as causes
of building-associated pulmonary disease in workers in three adjacent
office buildings. A. versicolor predominated in the indoor
air, and S. chartarum was isolated from bulk samples containing parts-per-million levels of satratoxins. Unfortunately, sterigmatocystin could not be isolated in that study, due to peak interference in UV-HPLC. In addition to the work of Hodgson et al.
(24) (2 to 5 µg/g), satratoxins have previously been found in building materials by Johanning et al. (27) (16 µg/g),
Croft et al. (14) (not quantified), and Anderson et al.
(1) (17 µg/g). To our knowledge, sterigmatocystin has not
previously been extracted from building materials naturally
contaminated by fungi. The levels of satratoxins in our present study
(
0.77 µg/g of extracted material) were lower than those previously
found in building materials naturally contaminated by S. chartarum (1, 24, 27) but as high as those found in
building materials artificially inoculated with S. chartarum
and incubated to enrich toxins (31) and almost as high as
those encountered with Stachybotrys-contaminated rice or
fodder (31).
Mycological analyses of air and crude building materials are routinely performed in environmental laboratories to evaluate the extent and spread of damage in buildings with moisture problems and to assess the risk to residents. The isolation of toxigenic species does not substantiate the presence of mycotoxins. However, the present study demonstrates that when mycotoxins are found in bulk materials, some genus known to include toxigenic species usually is present, even if strains from the fungal species probably responsible for producing the mycotoxin are not recovered. In this context, we suggest that the sources of mycotoxic fungal contamination should be removed and necessary precautions should be taken to prevent exposure to potentially harmful aerosolized particles during renovation of buildings with moisture problems.
As the techniques to collect and analyze airborne propagules develop, mycotoxins can be analyzed from indoor air, enabling an assessment of the possible health consequences of mycotoxins for residents of water-damaged buildings. In future studies, the ubiquitousness of mycotoxins in indoor environments can be evaluated when more mycotoxins are added to the analysis protocol and when more moldy materials are sampled. There are techniques available to analyze most fungi present in environmental samples. Identifying the fungi responsible for producing mycotoxins in building materials will require using such techniques in combination with the enrichment of pure fungal isolates on building materials and extraction of mycotoxins from these isolates. The present study underlines the need for such research. In the largest screen from indoor environments with respect to the number of mycotoxins and samples analyzed, we found mycotoxins in more than 40% of samples.
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ACKNOWLEDGMENTS |
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This work was supported in part by the Academy of Finland.
We thank Paula Vanninen at VERIFIN (Finnish Institute for Verification of the Chemical Weapons Convention) for furnishing of mycotoxin standards; Tapio Suorti (Vantaa), Kari Vähämäki (FIOH), and Marjatta Malmberg (HUCHS) for collecting samples; Taru Järvimaa (Vantaa) and Tuula Laakso (Helsinki Environment Center) for identifying fungal species; Sirkku Kokko (HUCHS), Tuovi Karpeeki (FIOH), and Marita Airaksinen and Maria Sulasalmi (Vantaa) for preparing mycological samples; and Hilkka Martinkauppi at FIOH for performing the mycotoxin sample pretreatments.
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FOOTNOTES |
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* Corresponding author. Mailing address: Finnish Institute of Occupational Health (FIOH), Uusimaa Regional Institute, Arinatie 3 A, FIN-00370 Helsinki, Finland. Phone: 358-9-4747926. Fax: 358-9-5061087. E-mail: tapani.tuomi{at}occuphealth.fi.
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Discussion
References
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