III.1. External exposome
Airborne fungal spores and subcellular components originate from
different sources, for example, soil, plants, animals, and water. Fungal
spores are distributed by physical mechanisms of gravity, wind, water
and animals. Airborne particles originating from biological sources
(viable and nonviable e.g. bacteria, fungal spores, pollen, mites, dead
tissues, and pieces of these materials or their metabolic products
including endotoxins and mycotoxins) are called bioaerosols (36).
Bioaerosols are ubiquitous; they originate mainly from soil and aquatic,
animal, vegetal, and anthropogenic sources, become airborne and may
travel long distances in the environment before sedimenting in so-called
sinks, or settle, e.g. on indoor surfaces or clothing (25,36,37). The
wind dispersal fungal spores, ranging from 1 to 30 µm in size, are major
components of bioaerosols, where their release, time of flight,
survival, and hence fitness for subsequent growth follow a variety of
pathways (37–39).
Culture-independent studies have demonstrated a very high diversity of
airborne fungal taxa. As an example, each dust sample taken from the
outer surface of hundreds of US homes contained more than 1,000 fungal
phylotypes, most of which belonging to taxa not been described at the
time of the study (25). However, only Cladosporium ,Toxicladosporium , and Alternaria were found in this study
in virtually all samples. These were also dominant taxa in terms of
abundance, with Cladosporium spp often amounting to 75% of the
whole fungal content of samples and Alternaria spp making up to
50% (25). The results of a questionnaire sent to national and regional
networks involved in the European Aeroallergen Network (EAN) and
counting fungal spore, have shown that most networks (44.7%) identified
five or fewer fungal spore types, and only two networks (12.5%)
identified more than 20 fungal spore types. On the other hand, all
networks examined Alternaria (16), most of themCladosporium (14) and the third more cited spore wasEpicoccum (10). Other fungal spores where cited (45) in the list,
but only by 1 to 6 networks (39). Partly overlapping findings were
reported from the European urban areas of Bratislava (Slovakia,
temperate continental climate), Thessaloniki (Greece, Mediterranean
climate), and Madrid (Spain, warm-temperate subtropical climate). The
five top abundant Slovakian fungal spores were Cladosporium,
Leptosphaeria, Coprinus, Alternaria, and Ganoderma (40), while
their Greek counterparts were Cladosporium, Alternaria, Ustilago,and Ascospores (Aspergillus/Penicillium ) (41).Cladosporium, Alternaria, Eurotium, Epicoccum, Penicillium , andSporobolomyces were detected in more than 90% of samples from
Madrid (42). In more arid climate types, such as Karachi (Pakistan) and
Kuwait, Cladosporium, Alternaria, Aspergillus, andPenicillium were also found among the top frequent airborne
fungal spores, together with Curvularia and Periconia in
Karachi (43) and Cryptococcus, Candida, Schizophyllum, Fusarium ,
and Gleotinia in Kuwait (44). Finally, under tropical climates,
airborne fungal spores were dominated by Cladosporium,
Leptosphaeria, Coprinus, Aspergillus, and Penicillium in Havana
(Cuba) using a culture-independent direct identification method (45) and
by Penicillium and Aspergillus in Nigeria using a
culture-dependent approach (46).
Under temperate climates, seasonal variations usually increase fungal
abundance with higher temperatures and rainfall, such as during summer
and fall (42). However, very high temperature values may negatively
affect the abundance of airborne fungal spores, as observed in Karachi
and Lagos (43,46). Significant interannual variations in rainfall are
common and associated with variations in airborne fungal abundance
(42,45).
Depending on the considered fungi, spore release may occur
preferentially during the daytime, as observed for Alternaria,Cladosporium , Epicoccum, and Exosporium or at
night, e.g. Coprinus and Leptosphaeria (40). Particulate
air pollution such as PM10 is positively correlated with the fungal
spore load (40).
To sum up, the nature and abundance of the dominant fungal spores in the
atmosphere exhibit marked variations related to climate (mean annual
precipitation and temperature, soil pH, plant diversity, distance to
coastal regions), season, time of the day, particulate air pollution,
and include Cladosporium and Alternaria as consistently
predominant genera, followed by Aspergillus and Penicillium,accompanied by locally important airborne fungi, such as Fusarium,
Curvularia, Cryptococcus, and Ustilago .
Indoor exposure is paramount, as most people now spend most of their
time indoors (47). Fungi can be transported by dust particles, people,
pets, and air ventilation systems into the indoor environment. The
relative humidity and moisture content of building materials may also
control to a certain level the fungal burden present on indoor
materials. Water damage, defined as “a moisture problem caused by
various leaks of water” (48), is an essential contributor to indoor
mold growth, often related to climatic events (e.g ., floods,
storms, rising ocean levels) or poor housing standards, including older
homes (23,47,49). Indoors, fungi can colonize virtually any material:
walls, windows frames, furniture, carpets, books, wallpapers, and even
spacecrafts. Biodeterioration due to fungal colonization poses
additional health threats, both direct such as skin contact with fungi
growing on documents from archives or libraries, and increased airborne
spore and mycotoxin load, and indirect due to the toxicity of biocide
treatments (50–52).
The abundance of indoor fungal spores shows geographic and seasonal
variations related to exchanges between the outdoor and indoor
environments, fungal growth, and meteorological conditions (23). The
degree of exposure to indoor molds was estimated at 5-10% under
cold-temperate climates, and up to 30% in warmer climates (27). An
Environmental Relative Moldiness Index (ERMI) may be used as a
quantitative marker of indoor mold exposure (49). The original ERMI,
developed in the United States of America, is computed using PCR
quantification of 36 common indoor molds, of which 26 are related to
water damage and 10 are not (53). In order to acknowledge local fungal
variability at the levels of species and abundance, the need for an
adapted ERMI was demonstrated (54).
Exposure to mold also occurs at various workplaces. A distinction has to
be made between the intentional use of molds and unintentional exposure
to moldy materials. The intentional use of molds in workplaces is found
in food production, pharmaceutical production and microbiological
laboratories. Representatives of the fungal genus Penicillium are
found in ripen cheese and salamis and produce antibiotics.Aspergillus niger produces citric acid from residues of the sugar
industry. In microbiology laboratories, workers come into contact with
molds when growing and multiplying microorganisms. Many more workers
come into contact with mold unintentionally: farmers working in fields
or keeping animals, waste processors sorting by hand in waste
management, wood processors handling moldy wood, metal workers inhaling
contaminated cooling lubricants, renovating houses, to name just a few
areas.
Despite the diversity of indoor molds, with more than 80 species
currently described, and the fact that indoor air may be 70–100 times
more contaminated than outdoor air (55,56), there are only four genera
of significant importance: Aspergillus, Penicillium, Alternaria ,
and Cladosporium (47).