FUNGAL GROWTH ON BUILDING MATERIALS AND LEVELS OF AIRBORNE FUNGI IN HOMES

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1 FUNGAL GROWTH ON BUILDING MATERIALS AND LEVELS OF AIRBORNE FUNGI IN HOMES BF Gi, PC Wu, JC Tsai, HJ Su * 1 Department of Environmental and Occupational Health, Medical College, National Cheng Kung University, Tainan 70428, Chinese Taipei ABSTRACT Our study aimed to identify the fungal species on different types of contaminated building materials. Forty-five families with current fungal growth agreed to participate at the time of field sampling. Surface sample were collected by scrape, and duplicate air samples were by Burkard samplers. Ceiling tile and wall were the most common sites at homes where fungal growth was identified. The major type of building materials with fungal growth was concrete with paint. The moisture contents of building materials with fungal growth were generally higher than those without fungi; however, Paecilomyces and Yeast were found on materials with moisture content below 30 percent. Furthermore, presence of Penicillium and non-sporulating fungi on building materials was significantly related to levels of indoor airborne fungal concentrations. Surface analysis of fungi, a much easier and less-expensive measure, can be an effective index for predicting degree of health risk in a contaminated environment. INDEX TERMS fungi, indoor air, building materials, Penicillium, Paecilomyces INTRODUCTION Epidemiological studies have identified damp living conditions as a major risk for reporting respiratory symptoms in children (Spengler J et al. 1994; Li and Hsu 1996). It is also established that fungi and house dust mites prosper in damp conditions (Harving et al. 1993), and increasing frequency of respiratory allergy and asthma may be associated with fungal exposure (Peat et al. 1998; Tsuang et al. 2003). Study had further demonstrated that reporting fungi growth on building surface is associated with presenting respiratory and nonspecific symptoms, after adjusting for exposure to dust mite antigens and bacterial endotoxin, (Dales et al, 1999). Airborne fungi concentrations in tropical countries were higher than those in temperate zone (Wu et al., 2001), and such findings have highlighted the need to critically evaluate approaches to reduce indoor fungal exposure. Fungal contamination on buildings materials was identified as a pollution source contributing to poor indoor air quality (Ellringer et al, 2000). But for the most part, observation of mold growth in indoor environment was not significantly related to airborne levels of fungi inside residences (Ren et al, 2001). Although previous research had suggested the association between indoor microbial concentrations and selected home characteristics (Dharmage et al. 1999), data and pattern of associations found in this region, where overall high levels of indoor microbes have been observed, were not as conclusive. The aim of this study was therefore to examine whether microbial levels were associated with the fungi growth on building materials. METHODS Study subjects Forty-five families, selected from a group of 344 families reporting fungal growth in interiors based on a prior citywide random questionnaire survey on housing characteristics, agreed to participate in field measurement. Environmental measurements Surface samples were collected, by scrape and plated directly onto culture medium, from area suspect for fungal *Corresponding author amb.wu@msa.hinet.net 1500

2 contamination; for example, moist spots, peeling paint, etc. We measured the airborne fungal concentrations (CFU/m 3 ), using Burkard portable air sampler with Malt Extract Agar, inside the home where surface fungi appeared to be present on building materials, and outside the entrance to the house. Sample plates were incubated at 25 for 5 days after collection. Fungi were identified morphologically to level of genus, except for Aspergillus whose characteristics were identified to species level by microscopic examination of the colony or spore structure. Tramex Moisture Encounter, a moisture meter, was used to document the moisture content by detecting moisture through paint, wallpaper, floor, and ceiling tiles. Questionnaire A self-administered questionnaire, inquiring about the age and type of the building, use of air conditioner, air filter, and dehumidifier, materials of flooring, wall, and ceiling tile, the number of occupants, years of occupation, presence of furry pets, cleaning routines, the habit of cooking, smoking and burn incense, was used to characterize the home environment and occupants behavior which might have an impact on the presence of fungal propagules in indoor air. RESULTS No statistical difference was found, using One-way ANOVA, when comparing frequency distribution of selected housing and resident characteristics between those families agreeing and those rejecting the filed measurements, from the original questionnaire cohort. Representativeness of the study population was supported. Environmental measurements were available for 56 rooms from 45 families. Table 1 presented the fungal genus identified from building materials, and ceiling tile and wall appeared to be common sources for surface fungal growth. The fungi genus that identified from concrete was included Aspergillus, Alternaria, Cladosporium, Drechslera, Fusarium, Microsporium, Paecilomyces, Penicillium, Non-sporulating, Yeast. The moisture indicative moulds in concrete were included A. fumigatus, A. versicolor, and Fusarium. Building materials Table 1. Fungal genus and the characteristics of contaminated building materials. Number Moisture Moisture Fungi genus of content of fungi content of samples growth area* Fungal growth area non-fungal growth area* A. fumigatus, A.niger, A.nidulans, A. versicolor, Alternaria, Cladosporium, Paint wall 48 78% 23% Drechslera, Fusarium, Microsporum, Non-sporulating, Paecilomyces, Penicillium, Yeast, Ceiling-tile 2 100% 30% A. fumigatus, A. niger Wood wall 2 75% 30% Paecilomyces, Alternaria Plastics Ceiling-tile 1 30% 10% Yeast Wall-paper wall 3 70% 23% A. fumigatus, A. niger, Cladosporium, Drechslera, Penicillium, Yeast *: Moisture Encounter, Tramex, IrelandFungal genera identified from wood included Alternaria, and Paecilomyces, and Aspergillus, Cladosporium, Drechslera, Penicillium, and Yeast were from wallpaper. Aspergillus was found to grow on most types of building materials. The averaged moisture contents of building materials with fungal growth were generally higher than those without. The frequency of fungal occurrence on building materials was shown on Table2. The predominant genera found on building materials were Cladosporium, Non-sporulating, Aletnaria, and Yeast. The moisture contents on the building materials with fungal growth were mostly higher than 70%. However, Alternaria, Cladosporium, and Penicillium was still present when the moisture contents was below 70%; Paecilomyces and Yeast could also grow on the materials with only 30% moisture content. 1501

3 Table 2. Frequency of fungi identified from the surface sample and the moisture content of the corresponding contaminated building materials. Fungi genus and species Frequency (n) Moisture content range Aspergillus 10.7%(6) 70%-100% A. niger 7%(4) 70%-100% A. nidulans 1.7%(1) 100% A. fumigatus 5.4%(3) 70%-100% A. versicolor 1.7%(1) 80% Alternaria 32%(18) 50%-100% Cladosporium 57%(32) 50%-100% Drechslera 3.5%(2) 70%-90% Microsporum 1.7%(1) 100% Paecilomyces 3.5%(2) 30%-80% Penicillium 12.5%(7) 60%-100% Yeast 32%(18) 30%-100% Non-sporulating 35.7%(20) 70%-100% n: number of times for identifying the genus or species from the surface sample Table 3. Comparison of fungal concentrations from areas with and without contaminated building materials. The fungi present on materials The fungi absent on materials Sample Concentration of indoor air Sample Concentration of indoor air size (n) Median (25%-75%) size (n) Median (25%-75%) P-value* Aspergillus (0-490) 50 0 (0-196) 0.37 A. niger (0-98) NA A. nidulans NA A. fumigatus NA A. versicolor NA Alternaria 18 0 (0-98) 38 0 (0-98) 0.47 Cladosporium ( ) (0-7296) 0.14 Drechslera 2 49(0-98) 54 0 NA Microsporum NA Paecilomyces ( ) 54 0 (0-98) NA Penicillium ( ) (0-196) <0.01 Yeast (0-196) 38 0 (0-98) 0.64 Non-sporulating (98-269) 36 0 (0-196) <0.01 NA: not analysis, *: Wilcoxon rank sum test Table 4. Comparison of indoor to outdoor ratio (I/O) of fungal concentrations from homes with and without contaminated building materials. The fungi present on materials The fungi absent on materials Sample The indoor to outdoor ratio Sample The indoor to outdoor ratio size (n) Median (25%-75%) size (n) Median (25%-75%) P-value* Aspergillus (0-196) 50 0 (0-1) 0.44 A. niger (0-1.6) NA A. nidulans NA A. fumigatus NA A. versicolor NA Alternaria 18 0 (0-98) 38 0 (0-1.63) 0.33 Cladosporium ( ) ( ) 0.24 Drechslera 2 49(0-98) 54 0 NA Microsporum 1 0 (0-98) 55 0 (0-98) NA Penicillium (1-588) (0-2.5) <0.01 Yeast (0-122) 38 0 (0-26) 0.48 Non-sporulating (0-3.2) 36 0 (0-1.38)

4 NA: not analysis, *: Wilcoxon rank sum test Airborne concentrations of genera at the homes with and without fungal grown on building materials were shown on Table 3, and significant difference was observed for Penicillium and non-sporulating fungi (p<0.05).. When sample size was smaller than 6, the p-value was not calculated. Where Penicillium and non-sporulating fungi identified on building materials, higher levels of airborne genera could also be found indoors. To examine the effects from outdoors or other potential fungal reservoir, ratios of indoor to outdoor fungal concentrations were calculated to document the likely presence of indoor- derived contamination. The significantly higher levels of the average I/O ratios for Penicillium and non-sporulating fungi were found at homes with these particular genera growth on the materials (Table 4). Further analysis was performed to identify relationships between housing characteristics and the levels of airborne Penicillium and non-sporulating indoors. Burning incense appeared to be associated with higher levels of Penicillium, and smoking activity was linked to higher levels of non-sporulating fungi. When Penicillium was present on building surface, higher levels of airborne Penicillium was also found indoors (P< 0.05, β=515), shown from multivariate analysis; on the other hand, concurrent presence of surface and airborne non-sporulating fungi disappeared after accounting for the effects of other house characteristics (P= 0.17, β=33). DISCUSSION To the best of our knowledge, this study is the first one to examine the association between the fungal growth on building materials, mostly attributable to excessive moisture (Haverinen et al., 1999), and corresponding airborne fungal levels in homes of tropical climate, such as Taiwan. Although moisture contents are statistically higher in the sampling areas with visible fungal growth than those without (P-value <0.001), the most common genera cultured on building materials, namely Cladosporium, Non-sporulating, Alternaria, and Yeast, were different from what have found in northern Europe, like Penicillium, Aspergillus, Chaetomium, Stachybotrys (Gravesen et al., 1999; Tuomi et al., 2000). Genera requiring high water activity to support growth for like Acremonium, Stachbotrys, Trichoderma, Ulocladium could not be identified on the building materials in our study (Gravesen et al., 1999; Tuomi et al., 2000), performed theoretically in the geographic regions of high relatively humidity year-round. Difference in building characteristics, materials used, and the mechanism resulting in water damage may all be considered plausible confounders to justify the above observations. In addition, the study region has regular rainy season with periodically attacked by typhoon and excessive rainfall in summer and early autumn and dry season in winter. We could easily collect rich fungal colonies from building materials with moisture contents lower than 70%. A more focused design is warranted should the underlying mechanism be understood. As Penicillium has been found most common in indoor air (Jacob et al., 2002; Su et al., 2001; Takahashi et al., 1997; Verhoeff et al., 1994; Rosas et al., 1993), it was also often seen on contaminated building surface in Denmark and Finland (Gravesen et al., 1999; Tuomi et al., 2000). Yet, other studies were not able to support a consistent and significant association between the fungal growth on building materials and the measured total fungal propagates in indoor air (Ren et al., 2001; Dales et al., 1997), with the exception for Penicillium and Non-sporulating fungi found in present study. Although Penicillium was not the common genus present on material samples in this study, its airborne concentrations were higher in those homes with the corresponding presence of this genus on building surface than those without. We consider this as a supportive evidence to rationalize how the observation between airborne and surface growth of Penicillium can be reasonable, meaningful, and of important value for practical implication. European study has shown that ceiling tiles and wall can be common sources for fungal growth in indoor environment (Karunasena et al., 2001); yet, we found no particular fungal growth on our samples of building materials. It may be attributable to the fact that in northern Europe, the ambient temperature is usually lower than indoors, and warm moist indoor air diffuses through walls and contacts cold vapor barriers, leading to condensation and growth of fungi (Pessi et al., 2002). However, the scenario can be very different at this subtropical climate where no significant temperature gradient is experienced between in/outdoors and therefore condensation will not be as common under most circumstances. CONCLUSION AND IMPLICATIONS Common fungi found on building materials in this region appear to be different from those often observed in cold climates. Moisture contents in building materials may be the determining factor, and airborne concentrations of Penicillium and Non-sporulating are highly associated with corresponding growth observed on building materials 1503

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