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ADVANCES IN APPLIED MICROBIOLOGY, VOLUME 55 Copyright 2004, Elsevier Inc.

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truly amazing is that this course of action is not too different from what we do today, over 33 centuries later. The building material used at that time was "straw" bricks, that is, cellulose-based stones and plaster. What of course is different today is that we now know what microorganisms cause these problems and we know, or at least strongly suspect, what products these fungi produce that can cause health problems in human beings.

One of the early scientific papers published regarding the effects of mold spores on humans appeared in 1873 (Blackley). Charles Blackley, who was one of the early describers of pollen skin tests, wrote about his asthmatic responses to the inhalation of Penicillium species conidia (spores) (Licorish et al., 1985). It now appears that the literature is quite clear on the importance of the inhalation of fungal spores on respiratory disease in man. The Centers for Disease Control (CDC) recently published a statement for the record for the United States House of Representatives (Redd, 2002). In it they state, ''While there remain many unresolved scientific questions, we do know that exposure to high levels of mold causes some illnesses in susceptible people. Because molds can be harmful, it is important to maintain buildings, prevent water damage and mold growth, and clean up moldy materials.'' We have spent the last decade trying to understand the above concepts. It is our humble hope that some of the work we have done can help elucidate the role of fungi in the phenomenon known as sick building syndrome.

Reports in the literature about building structures with poor indoor air quality (IAQ) increasingly appeared soon after the mid-1970s (Hodgson, 1992; Spangler and Sexton, 1983). SBS, a term that is sometimes used for symptoms commonly associated with poor IAQ, was first described in 1982. The first study examining more than one building with SBS was published in 1984 (Finnigan et al.). Although SBS has been difficult to define, evidence is now coming to the fore that seems to indicate the importance of indoor fungal growth in this phenomenon (Straus, 2001). SBS literally means that there is something inside of said building that is actually making people sick. These symptoms most commonly are fatigue, runny nose, itchy eyes, sore throat, and headaches (Cooley et al., 1998). Although no single cause for the above symptoms is likely to be found, the presence of certain molds is becoming increasingly associated with this phenomenon (Burrell, 1991; Cooley et al., 1998; Dales et al., 1991; Jaakkola et al., 2002; Lehrer et al., 1983; Miller, 1992).

II. Inhalation of Fungal Spores Causes Respiratory Disease in Humans

Our first study examining the role of fungi in SBS was published in 1998 (Cooley et al.). In that paper we showed that there was a correlation between certain fungi (Pénicillium species [Figs. 1 and 2, see color insert] in the air and Stachybotrys species [Figs. 3 and 4, see color insert] on building surfaces) and the symptoms seen in SBS. The finding that the elevation of culturable (viable) Pénicillium species conidia in the indoor air over those levels in the outside air caused health problems in human beings should not have been a surprise. As mentioned previously, the inhalation of Pénicillium species conidia was associated with the initiation of an asthmatic attack as early as 1873 (Blackley). Alternaria species spores and Pénicillium species conidia were shown to provoke immediate and delayed-type asthma in individuals already sensitized to these organisms (Licorish et al., 1985). A 1998 study (Garret et al.) demonstrated that childhood asthma could be correlated with exposure to Penicillium species conidia levels in the air but not to visible mold. In many of our investigations, we observed that Penicillium

Penicillium Frequentans
Fig. 1. Penicillium chrysogenum colonies on PDA for 7 days.
Penicillium Roqueforti Pda
Fig. 2. Pénicillium chrysogenum at 400x magnification.

species tended to colonize the heating, ventilation, and air conditioning (HVAC) systems of buildings (Cooley and Wong, unpublished data from ARAL database, 2003). In 2002, Gent et al., showed that infants with high risk for development of asthma who were exposed to high levels of Pénicillium species conidia were at significant risk for persistent cough and wheeze. This study was particularly interesting, because this correlation between respiratory distress and mold exposure was valid for Pénicillium species conidia but not for Cladosporium species spores. Obviously there is something different about the genus Pénicillium that sets it apart from other fungal genera in this regard. In 1984, Fergussen et al. described for the first time Pénicillium species allergic alveolitis caused by the faulty installation of a central heating system unit that introduced a great deal of water into a residence. In this case the two fungal species found growing in the dwelling were

Acne Vulgaris Colony
Fig. 3. Stachybotrys chartarum colonies on PDA for 14 days.

P. chrysogenum and P. cyclopium. Finally, there is one other important respiratory disease caused by the inhalation of Penicillium species conidia. This disease is called cheese worker's lung or cheese washer's disease (Straus, 2002). This is an occupational disease that can occur in individuals who work in the cheese industry. Occupational lung diseases become more common as the world becomes more industrialized. Some of the other more common occupational lung diseases include maltster's lung, farmer's lung, bagassosis, suberosis, and wood pulp worker's lung. The organisms that cause the above diseases are Asper-gillus clavatus, thermophilic actinomycetes, Penicillium frequentans, and Alternaria species, respectively (Straus, 2002). These diseases are all phenomena related to hypersensitivity pneumonitis (HP). HP is an allergic reaction to a wide variety of different inhaled antigens. In the case of cheese washer's disease, the inhaled antigen is a fungus (either Penicillium casei or Penicillium roqueforti, which are used to flavor the cheese). The first report of cheese washer's disease was in Germany in 1969 (DeWeck et al.). In this study, two individuals reported difficulty

Stachybotrys Chartarum Pictures
Fig. 4. Stachybotrys chartarum at 400 x magnification.

in breathing, fever, fatigue, and productive cough. These individuals were cheese washers, and their symptoms appeared to be job related. Because Penicillium species are grown on the surface of cheese as it is being produced, it is necessary to have employees remove the fungi. These individuals are, of course, called cheese washers. Cheese washing is performed by rubbing a course salt on the formed product and then scrubbing it with a damp cloth (Marcer et al., 1996). The cheese product itself supplies all the food and water that the fungi need to multiply. Naturally, during this scrubbing process large numbers of fungal conidia are emitted into the air surrounding the cheese product. The organism most commonly found growing on the cheese in those situations is P. casei (Schleuter, 1993). As expected, antibodies to P. casei were detected in the sera of the two individuals described in the above 1969 study (DeWeck et al.). Fortunately, the disease appears to be reversible when the individual is no longer inhaling P. casei conidia (DeWeck et al., 1969). However, if one is continually inhaling the same type of fungal spores, ''progressive pulmonary fibrosis'' can occur with resultant granulomatous tissue formation and subsequent shortness of breath (Sell, 1996). Cheese washer's disease was originally described in Europe by DeWeck et al. (1969), but it has also been reported in the United States. Campbell et al. (1983) examined a worker who developed extrinsic allergic alveolitis (another term for hypersensitivity pneumo-nitis) caused by her inhalation of a fungus that was used in the production of the cheese and not one that grew on the cheese wheel as was described by DeWeck et al. (1969). In this case, the cheese worker was involved in the processing of blue cheese, which employs P. roqueforti. Her job involved the breaking up of the blue cheese so it could be more easily put in salad dressing bottles. This activity, of course, dispersed high concentrations of P. roqueforti conidia into the air in her immediate vicinity. Antibodies to P. roqueforti were found in her serum and lung washes (Campbell et al., 1983). There have been other reports in the literature describing similar cases of cheese washer's disease (Guglielminetti et al., 2001; Marcer et al., 1996).

III. Correlation Between the Presence of Certain Fungi and SBS

In the 1998 study (Cooley et al.), we showed that there is a correlation between the presence of certain fungi in a building and the symptoms associated with SBS. The symptoms associated with SBS and described in this study can be seen in Table I. In Table I, allergic-like symptoms were the main complaint at all of the schools, and with the moderate to high counts of culturable Penicillium species conidia found in the complaint areas, this is not surprising. However, with the exception of nausea, numerous symptoms other than allergic-like were reported at each school. This implies that there may be other mechanisms that may be inducing adverse health effects. In fact, we always observed a variety of different visible fungal growth on surfaces in the schools. This 22-month study of 48 schools in the southern United States examined buildings in which there were concerns about poor IAQ and health. Surface samples and indoor air and outdoor culturable air samples were taken at all 48 buildings to look for visible fungal growth as well as culturable airborne fungal spores. Five fungal genera were usually found in the outdoor air. They were Cladosporium (81.5%), Penicillium (5.2%), Chrysosporium (4.9%), Alternaria (2.8%), and Aspergillus (1.1%). Cladosporium species are commonly the dominant fungal species in the outdoor air (Shelton et al., 2002).

Incidences per 100 Employees (95% Cl) of Reported Complaints and Symptoms Regarding Indoor Air Quality (IAQ) at 48

United States Schools Between 1994 and 1996

Type of symptom

Incidence

95% Cl

Phenomenon

Incidence

95% Cl

phenomenon

Incidence

95% Cl

Nasal drainage and

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Responses

  • eva
    How to identify penicillium roqueforti?
    8 years ago
  • ross
    What causes penicillium to have different color?
    8 years ago
  • nicoletta
    What subfield of microbiology is penicillium chrysogenum involved in?
    6 months ago

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