Proceedings: Indoor Air 2002

HIDDEN SOMETIMES ENTERS THE INDOOR AIR

P Morey1∗, M Andrew2, B Ligman2, and J Jarvis3

1Air Quality Sciences, Inc., Gettysburg, PA, USA 2Air Quality Sciences, Inc., Atlanta, GA, USA 3University of Nevada School of Medicine, Reno, NV, USA

ABSTRACT Air sampling for culturable fungi was carried out in two new school buildings each with hidden mold colonization on envelope construction materials. An objective of the study was to determine if from the moldy envelope were entering indoor air. Penicillium, Aspergillus and Stachybotrys were major colonizers of envelope construction materials in both buildings including stucco paper. Air sampling in one of the two buildings showed that Penicillium species from hidden mold reservoirs were entering the indoor air. However, Stachybotrys did not enter the indoor air in significant amounts in both buildings. A medical surveillance program concurrent with environmental monitoring was carried out to identify occupants with symptoms of new onset allergic disease.

INDEX TERMS Building envelope, Hidden mold, Medical surveillance, Penicillium, Stachybotrys.

INTRODUCTION It is well known that allergic respiratory disease can occur among persons occupying chronically damp or water damaged buildings where visible mold growth is evident (Jarvis and Morey, 2001; Dales and Miller, 2001). However, it is uncertain if allergic respiratory disease occurs among occupants of buildings where mold growth is hidden within building construction. The two schools described in this study were new buildings characterized by profuse water leaks in the envelope and hidden mold growth in envelope construction materials. Both buildings were the subject of construction defect litigation associated with water leakage and biodeterioration of envelope construction materials such as building (stucco) paper. The public agencies operating both school buildings were concerned about potential occupant exposure to fungi from hidden mold reservoirs in envelope construction. Consequently, air sampling evaluations and medical surveillance of occupants were performed during the several years when litigation occurred. An objective of air sampling was to determine if spores from fungal reservoirs in envelope construction were entering the indoor air.

METHODS Building A is a university residence hall with an envelope construction of stucco veneer on paper backed lath over steel studs. Biodegradable materials in the envelope included building paper, Kraft backed batt insulation between studs, and a single panel of paper faced gypsum board. The building is located in climactic region J as defined by the U.S. Environmental Protection Agency’s Building Assessment and Survey Evaluation (BASE; Womble, et al., 1996). Chronic water leakage occurred around windows in building A. The amount of

∗ Contact author email: [email protected]

455 Proceedings: Indoor Air 2002 visible mold colonizing building paper, insulation, and gypsum board varied from minimal to extensive in each room. , Chaetomium globosum, Penicillium chrysogenum, and P. corylophilum were major colonizers of biodegradable envelope construction materials. Because of water leakage and mold growth problems, university authorities excluded occupancy of building A by any student with a history of allergic respiratory disease. In addition, all student rooms were required to be cleaned with a HEPA vacuum twice each month to remove dust reservoirs that might contain fungal spores.

Building B is a high school campus consisting of several one and two story buildings located in BASE climactic region E. Building envelope construction consists of stucco veneer on paper backed lath over steel studs. Water enters the envelope around windows and around beams which penetrate the wall system. Minimal to extensive amounts of mold colonize envelope construction materials in each room. Stachybotrys chartarum, Chaetomium globosum, Penicillium chrysogenum, P. aurantiogriseum, and Aspergillus versicolor were predominant colonizers on envelope construction materials in building B. Air sampling was performed quiescently in occupied rooms of buildings A and B using a culture plate (cellulose or malt extract agars) impactor operating at a flow rate of approximately 0.18 m3/minute.

RESULTS AND DISCUSSION Table 1. Concentrations (cfu/m3) of fungal taxa indoors and outdoors at building A in August 2000. Taxa Outdoor air Indoor air x SD x SD C. cladosporioides 368 274 641 1186 Alt alternata 20 13 3 11 Epi nigrum 6 9 1 5 CAE TOTAL 394 647 Pen brevicompactum 31 25 17 102 Pen chrysogenum 2 5 182 643 Pen citrinum 1 3 47 438 Pen crustosum 1 2 145 660 Pen glabrum 6 10 6 18 Asp fumigatus 1 3 1 5 Asp niger 8 7 4 21 Asp versicolor 0.3 1.4 2 6 PA TOTAL 61 424 NS hyaline fungi 12 17 292 997 Aureo pullulans 8 11 0.3 2 Stachybotrys ND - ND - Chaetomium ND - ND - GRAND TOTAL 514 1382 Number of samples: Outdoors N = 18, Indoors N = 97; cellulose agar; CAE = Cladosporium + Alternaria + Epicoccum; PA = Penicillium + Aspergillus; NS = Nonsporulating; x = average; SD = standard deviation

Building A. Air sampling was performed seven times between 1999 and 2001. The results of two air sampling evaluations are presented in Tables 1 and 2. In August 2000 Cladosporium cladosporioides was the dominant taxon found both indoors and outdoors (Table 1). In outdoor air, the combined concentration of Cladosporium + Alternaria +

456 Proceedings: Indoor Air 2002

Epicoccum (CAE; phylloplane fungi) was 394 cfu/m3 while the CAE level in indoor air was 647 cfu/m3 (Table 1). The various Penicillium and Aspergillus (PA) species found outdoors and indoors at the same time are listed in Table 1. Penicillium brevicompactum (31 cfu/m3), (8 cfu/m3) and P. glabrum (6 cfu/m3) were the most common PA species found outdoors at building A. At the same time, P. chrysogenum (182 cfu/m3), P. crustosum (145 cfu/m3), and P. citrinum (47 cfu/m3) were the most frequent indoor PA species. The differing rank order of PA species indoors and outdoors suggests that some spores from envelope growth sites were entering the indoor air. It should be noted that culturable Stachybotrys and Chaetomium species were not detected in any of the 97 indoor samples, even though these fungi were major colonizers of envelope constructions.

In building A in April 2001, Cladosporium cladosporioides still dominated the outdoor taxa (303 cfu/m3; total CAE = 352 cfu/m3; Table 2). However, Penicillium chrysogenum (cfu/m3) and other unidentified Penicillium species (221 cfu/m3; total PA = 465 cfu/m3) were the dominant indoor fungi. A trace (<1 cfu/m3) of culturable Stachybotrys was found in April 2001 both indoors and outdoors.

Table 2. Concentrations (cfu/m3) of fungal taxa indoors and outdoors at building A in April 2001. Taxa Outdoor air Indoor air x SD x SD C. cladosporioides 303 244 74 95 Alt alternata 7 6 3 9 Epi nigrum 2 5 0.2 1 CAE TOTAL 352 92 Pen brevicompactum 31 31 5 7 Pen chrysogenum 9 12 204 931 Pen citrinum ND - 2 9 Pen crustosum ND - 6 24 Pen glabrum 5 12 5 21 Pen species 5.4 9.2 221 972 Asp fumigatus 10 21 3 10 Asp niger 1 3 2 11 Asp versicolor ND - 0.2 1.1 PA TOTAL 68 465 NS hyaline fungi 6 7 22 114 Aureo pullulans 6 14 0.2 1 Stachybotrys 0.2 1.1 0.5 3 Chaetomium ND - 0.1 0.8 GRAND TOTAL 442 586 Number of samples: Outdoors N = 30, Indoors N = 106; Other abbreviations like Table 1.

Considerable variation occurred in air sampling results between adjacent rooms on the same floor and between samples collected in the same room on different days (note high standard deviation in Tables 1 and 2). Some rooms, especially those with the most leaks, were characterized by concentrations of culturable Penicillium taxa exceeding 1 x 103 cfu/m3 and by nonculturable ( trap) Penicillium-Aspergillus often exceeding 1x104/m3.

457 Proceedings: Indoor Air 2002

During the academic years 1999-2000 and 2000-2001, all occupants of building A were required to complete questionnaires before taking up residence in the fall and then twice during the academic year. Occupants with a history of respiratory symptoms compatible with new onset allergic chest disease were referred to an academic pulmonary function clinic for further evaluation. Rates of respiratory symptoms were lower before taking up residence than during the academic semester. Although 10 occupants were found to have symptoms suggestive of new onset chest disease, onset of disease could not be confirmed by objective measurements (restrictive findings of spirometry). Building A was vacated at the end of the academic 2000-2001 year coincident with settlement of construction defect litigation.

Table 3. Concentrations (cfu/m3) of fungal taxa indoors and outdoors at building B in November 2001. Taxa Outdoor air Indoor air x SD x SD Cladosporium species 676 897 171 232 Alt alternata 9 29 4 7 Epi nigrum 0.5 2 0.0 0.3 CAE TOTAL 686 175 Pen brevicompactum 16 29 13 21 Pen chrysogenum 1 5 0.5 2 Pen citrinum 0.4 2 0.6 4 Pen crustosum 0.2 1 0.1 0.5 Pen glabrum 2 3 0.6 2 Asp fumigatus 1 4 0.3 1 Asp niger 9 11 6 7 Asp versicolor ND - 0.5 1 PA TOTAL 31 27 NS hyaline 16 24 6 13 Aureo pullulans 6 14 0.2 1 Stachybotrys ND - ND - Chaetomium ND - ND - GRAND TOTAL 788 217 Number of samples: Outdoors N = 29, Indoors N = 64; malt extract agar; Other abbreviations like Table 1.

Building B. The campus of building B is occupied by about 3,000 students and 200 faculty. Cladosporium species dominated the fungi in the indoor and outdoor air both in November 2000 (Table 3) and in May 2001 (Table 4).

In November 2000 the total PA concentration outdoors was 31 cfu/m3 while the indoor PA level was 27 cfu/m3 (Table 3). Penicillium brevicompactum (concentration < 20 cfu/m3) and Aspergillus niger (concentration < 10 cfu/m3) were dominant taxa both indoors and outdoors (Table 3). In May 2001 the total PA concentration outdoors was 54 cfu/m3 while the indoor PA level was 47 cfu/m3 (Table 4). Several Penicillium species (P. funiculosum and P. minioluteum were found indoors but not outdoors in May 2001, at low (5 to 10 cfu/m3) levels (Table 4). With the exception noted above, it was concluded that exposure to PA species indoors in building B was normal or not substantially different from that which occurred outdoors. In addition, although Stachybotrys was a major colonizer of stucco paper in

458 Proceedings: Indoor Air 2002 building B, culturable Stachybotrys was not detected in any of the 298 air samples collected indoors (Tables 3 and 4).

Table 4. Concentrations (cfu/m3) of fungal taxa indoors and outdoors at building B in May 2001. Taxa Outdoor air Indoor air x SD x SD Cladosporium species 1616 1459 349 724 Alt alternata 47 51 11 16 Epi nigrum 2 5 1.1 4 CAE TOTAL 1665 363 Pen brevicompactum 2 9 0.6 3 Pen chrysogenum ND - 0.1 1 Pen citrinum ND - 0.1 1 Pen crustosum 3 14 0.2 1 Pen funiculosum ND - 10 147 Pen glabrum 0.4 2 0.6 4 Pen minioluteum 0.2 1 5 43 Pen species 14 32 16 67 Asp fumigatus 0.3 2 0.2 1 Asp niger 29 100 2 8 Asp versicolor ND - 0.1 1 PA TOTAL 54 47 NS hyaline fungi 5 7 4 6 Aureo pullulans 9 21 0.6 3 Stachybotrys ND - ND - Chaetomium ND - 0.7 10 GRAND TOTAL 1761 429 Number of samples: Outdoors N = 48, Indoors N = 234; Malt extract agar; Other abbreviations like Table 1.

Questionnaires were distributed to the faculty of building B and to the faculty of a control school (without known mold or water damage) in February 2001. Participation rates were high (about 90% for both schools), and the distribution of responses to questions about gender, age, professional status, medication use, and smoking status were similar in the two schools, with the exception that 7% of building B faculty reported current smoking while only 4% of the control school faculty reported current tobacco use. There were no statistically significant differences between building B and the control school in rates of reported respiratory symptoms, though building B faculty tended to report more coughing, mucous production, wheezing, and shortness of breath (e.g., 18.5% unusual cough in building B; 15.8% in control school). Since building B faculty had a higher rate of current smoking, a slightly higher rate of respiratory symptoms would be expected due to the smoking difference alone. It was concluded that though water damage and hidden mold growth had occurred in building B, there was no evidence as of February 2001 that respiratory disease was occurring more often than expected in building B.

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CONCLUSIONS Air sampling in building A but not in building B suggested that PA spores from hidden mold in the building envelope were entering the indoor air. Twice monthly HEPA vacuum cleaning of dormitory rooms in building A was inadequate to prevent domination of the indoor microflora by PA species. However, culturable Stachybotrys, which was a major colonizer of stucco paper, did not enter the indoor air in significant amounts in either building A or B.

The medical surveillance program in building A appeared adequate to identify students with respiratory symptoms prior to the development of new onset allergic disease. Medical surveillance suggested that no excess respiratory disease was occurring in building B.

This study showed that in one of two buildings, spores from hidden mold were entering the indoor air in substantial amounts despite extraordinary housekeeping efforts. The management of occupant health concerns in buildings with hidden mold is a difficult public health issue requiring both environmental monitoring as well as medical surveillance.

REFERENCES Dales R and Miller J. 2001. Building-related illness: epidemiological and case-related experience. In Microorganisms in Home and Indoor Work Environments. Flannigan B, Samson R, and Miller J, eds. London: Taylor & Francis, pp 217-227. Jarvis J and Morey P. 2001. Allergic respiratory disease and fungal remediation in a building in a subtropical climate. Applied Occupational and Environmental Hygiene. Vol. 16, pp 380-388. Womble S, Ronca E, and Girman J. 1996. Developing baseline information on buildings and (BASE ’95). In IAQ 96 Paths to Better Building Environments. Atlanta: American Society of Heating, Refrigerating and Air-Conditioning Engineers, Inc., pp 109-117.

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