Biodiversity and concentrations of airborne fungi in large US office buildings from the BASE study

Abstract

The Building Assessment Survey and Evaluation (BASE) study measured baseline concentrations of airborne fungi in 100 representative US office buildings in 1994–1998. Multiple samples for different sampling durations, sites, and times of the day were aggregated into building-wide indoor and outdoor average concentrations. Fungal concentrations were compared between locations (indoor vs. outdoor), sampling and analytical methods (culture vs. microscopy), and season (summer vs. winter). The arithmetic means (standard deviations) of the indoor/outdoor concentrations of culturable fungi and fungal spores were 100/680 (230/840) $\mathrm{CFU}{\mathrm{m}}^{-3}$ and 270/6540 (1190/6780) $\mathrm{spore}{\mathrm{m}}^{-3}$, respectively. Although fewer groups were observed indoors than outdoors, at lower average concentrations (except in two buildings), site-specific and building-wide indoor measurements had higher coefficients of variation. More groups were seen in summer, and aggregated concentrations tended to be higher than in winter except for culturable Aureobasidium spp. and Botrytis spp. outdoors and non-sporulating fungi in both locations. Rankings of the predominant fungi identified by both methods were similar, but overall indoor and outdoor spore concentrations were approximately 3 and 10 times higher, respectively, than concentrations of culturable fungi. In the 44 buildings with both measurements, the indoor and outdoor total culturable fungi to fungal spore ratios (total $C/S$ ratios) were 1.27 and 0.25, with opposite seasonal patterns. The indoor $C/S$ ratio was higher in summer than in winter (1.47 vs. 0.86; $N=29$ and 15, respectively), but the outdoor ratio was lower in summer (0.19 vs. 0.36, respectively). Comparison of the number of different fungal groups and individual occurrence in buildings and samples indicated that the outdoor environment and summer season were more diverse, but the proportional contributions of the groups were very similar suggesting that the indoor and outdoor environments were related as were summer and winter seasons for each location. The extreme (e.g., 90th percentile) indoor concentrations ($200\mathrm{CFU}{\mathrm{m}}^{-3}$ and $210\mathrm{spore}{\mathrm{m}}^{-3}$) may provide reference values for non-complaint US office environments.

Introduction

An Institute of Medicine report (IOM, 2004) concluded that there is strong scientific evidence linking indoor dampness, fungal growth, and health effects (e.g., upper respiratory tract symptoms, asthma symptoms in already sensitized asthmatic persons, and hypersensitivity pneumonitis) and that there is limited evidence for other outcomes (i.e., lower respiratory illness in otherwise healthy children). This panel agreed with others that have determined that dampness in buildings is a risk factor for health effects, although the literature is not conclusive as to which agents are causative (Bornehag et al., 2001, Bornehag et al., 2004). These adverse effects can result from bioaerosol exposure through a variety of mechanisms, including IgE-mediated hypersensitivity, irritant or inflammatory reactions to spores or fungal metabolites, fungal infection, and reactions to mycotoxins (Portnoy et al., 2005). The concern about adverse health effects from bioaerosol inhalation has led to consideration of permissible exposure limits for fungi; however, currently there are no specific US Occupational Safety and Health Administration Standards or Directives or other exposure limits for fungi (USDOL, 2006, CDC, 2006, USEPA, 2001).

The US Environmental Protection Agency (USEPA) conducted a cross-sectional study of indoor environmental quality (IEQ) in 100 large office buildings in 37 cities in 25 continental states. The primary goal of the Building Assessment Survey and Evaluation (BASE) study was to define the status of the existing building stock with respect to determinants of IEQ and occupant satisfaction by collecting normative data on environmental parameters, building characteristics, and occupant perceptions of comfort and IEQ. Public and commercial buildings in cities with $>100000$ population were selected randomly, excluding only facilities with highly publicized IEQ problems. These large office buildings primarily were urban (73%) or suburban (23%) with only a few in rural settings (4%) (Burton et al., 2000). Each building was studied during a 1-week period either in summer (June–September) or winter (December–April) following a standardized protocol (USEPA, 2003). Samples for biological agents included air samples for culturable fungi and fungal spores (Macher et al., 2001) and culturable bacteria (Tsai and Macher, 2005), settled dust samples and wet and dry bulk samples from areas of visible contamination for culturable fungi and bacteria, and dust samples for cat and dust mite allergens (Macher et al., 2005). Our prevalence analysis (Macher et al., 2001) showed that fungi were found more often in samples of outdoor than indoor air and in more samples collected in summer than winter in both locations. Mendell et al. (2006) found increases in building-related lower respiratory or mucous membrane symptoms with infrequent cleaning of ventilation equipment or past water damage in the BASE buildings. This paper presents concentration summaries of airborne culturable fungi and fungal spores by location (indoor vs. outdoor), collection and analytical method (multiple-hole agar vs. slit slide impaction; culture vs. microscopy), and season (summer vs. winter). Widely used biodiversity (entropy) indices were calculated to evaluate fungal community structure and the relatedness of sampling locations and seasons at the individual sample and aggregated building levels.