Stachybotrys chartarum (atra) contamination of the indoor environment: Health implications

Abstract

In 1998, widespread contamination of water-damaged school portables with the toxigenic mold Stachybotrys chartarum was detected in the province of Ontario. This mold may cause human disease through direct irritation, type 1 hypersensitivity or the production of toxins. A variety of respiratory, dermatological, eye and constitutional symptoms have been associated with heavy and prolonged exposure to S chartarum. S chartarum has also been potentially implicated as a rare cause of idiopathic pulmonary hemorrhage in infants. Ingestion of food heavily contaminated with toxin-producing molds, including S chartarum, can cause bone marrow suppression and immunotoxicity. However, the level of toxin exposure that occurs following inhalation of S chartarum is very low; consequently, serious adverse health effects from such an exposure are extremely unlikely. In a child with symptoms felt to be temporally related to the school environment, an assessment of the child’s school should be carried out by the public health authorities so that potential irritants and allergens can be identified. Avoidance of exposure is the most effective mode of therapy. Buildings found to be heavily contaminated with molds, particularly S chartarum, should undergo thorough cleaning and repair to remove the offending agent(s), and prevent further water damage and mold overgrowth.

Fungi are eukaryotic organisms that are ubiquitous in the environment. The single cell forms are known as yeasts, while those composed of multiple cells forming a filamentous mycelium are referred to as molds. Mold growth in the indoor environment is promoted by the presence of water damage and dampness (1–3). Poorly maintained heating, ventilation and air conditioning systems can also be a source of mold overgrowth (3,4). Among Canadian children, the prevalence of lower respiratory symptoms, including cough, wheeze, bronchitis and asthma, is increased by approximately 50% in the presence of dampness and mold in the home environment (2).

Fungal-induced human disease can arise from tissue invasion (mycosis); direct irritation by spores, mycelia and other fungal constituents; hypersensitivity reactions to fungal antigens; or exposure to fungal mycotoxins (4–5). Mycoses, with the exception of hair, skin and nail infections, occur predominantly in immunocompromised hosts. Direct irritation of skin and mucous membranes from mold exposure is usually restricted to those directly handling or cleaning heavily contaminated sites or objects without adequate protection. Of primary concern in the indoor environment is the potential for hypersensitivity reactions to fungal antigens and toxic injury resulting from mycotoxin exposure. Molds commonly encountered in the indoor environment include Aspergillus, Penicillium, Fusarium, Alternaria and Stachybotrys species (3).

In early 1998, widespread contamination of school portables with the toxigenic mold Stachybotrys chartarum (atra) was discovered in Ontario. The organism was typically isolated from building surfaces, such as drywall, that had become damp due to water penetration. The purpose of this article is to review briefly the issues surrounding mold contamination of the indoor environment, with particular attention given to the mycology, toxicology and clinical manifestations associated with exposure to S chartarum.

MYCOLOGY AND TOXICOLOGY OF S CHARTARUM

Mycology:

S chartarum is a cellulolytic saprophytic filamentous fungus with a worldwide distribution (4). As with most fungi, temperature, moisture, relative humidity and growth substrate are all important factors influencing its growth. Stachybotrys species can grow over a wide range of temperatures, and require a moisture content of at least 15% in the substrate, a relative humidity of 70% to 90% and a substrate with high cellulose content (3,5). Cellulose-based materials, including straw, hay, plant debris, cereal grains, and various building materials such as fibre board and gypsum liner paper that become moist and are subject to temperature fluctuations, provide ideal growth conditions for S chartarum.

Trichothecene mycotoxins:

Trichothecene mycotoxins are toxic organic compounds produced by a variety of fungi including S chartarum (3). These toxins are potent inhibitors of protein synthesis in eukaryotes (6,7). Rapidly dividing cells, such as those of the bone marrow and gastrointestinal tract, are most vulnerable to the action of these toxins (3,5,6). The lipid solubility of trichothecenes permits its rapid penetration of cell membranes and systemic absorption from skin and mucosal surfaces (8).

Trichothecene mycotoxicosis:

Ingestion of food heavily contaminated with trichothecene-producing fungi has been associated with profound bone marrow suppression and immunotoxicity in both humans and animals (3,7). Alimentary toxic aleukia, a disease caused by the ingestion of grains contaminated with trichothecene-producing Fusarium species, afflicted hundreds of thousands of Russians during the Second World War (3,7). Gastrointestinal irritation characterized by mucosal ulceration, nausea, vomiting, abdominal pain and diarrhea are followed by an asymptomatic period during which progressive anemia, thrombocytopenia and leukopenia develop. Opportunistic infections and coagulopathy typically occur three to four weeks after the onset of illness. The Russian experience suggested a mortality rate of 10% to 60%, although with modern supportive medical therapy the prognosis is undoubtedly much better. Stachybotritoxicosis, a disease characterized by agranulocytosis, thrombocytopenia and death from opportunistic infections, has been well documented in horses and other farm animals following the ingestion of straw or hay contaminated with toxigenic strains of S chartarum (3,5,7). In Canada, the risk of trichothecene-induced bone marrow suppression in humans is extremely remote because the ingestion of heavily contaminated food is very unlikely.

CLINICAL MANIFESTATIONS

The health implications associated with inhalation exposure to S chartarum is of particular concern because of recent epidemiological reports implicating this organism as a potential cause of human disease in the indoor environment (9–13). Tissue invasion by Stachybotrys species does not occur. Type 1 hypersensitivity (immunoglobulin E-mediated) reactions to Stachybotrys species antigens may lead to development of allergic symptoms, although supporting data are limited. Direct inhalation of ‘free’ trichothecenes is unlikely because of the low volatility of these compounds (8). Spores and mycelia from Stachybotrys species have been shown to contain trichothecene mycotoxins (14), and it is reasonable to assume that heavy and prolonged inhalation exposure to trichothecene-containing dust particles, spores and mycelial fragments may lead to the development of human disease related to toxin exposure.

Pulmonary hemorrhage and S chartarum:

A recent epidemiological investigation of a cluster of 10 infants younger than six months of age with idiopathic pulmonary hemorrhage implicated S chartarum as a potential cause (9,10). All infants resided in water-damaged homes that were heavily contaminated by Aspergillus, Penicillium, Cladosporium and Stachybotrys species. The mean concentration of S chartarum in the air was 10-fold higher than in control homes. Of particular interest, five of the 10 infants suffered a second episode of pulmonary hemorrhage soon after returning home from hospital. It was suggested that young infants may be particularly susceptible to the toxic effects of inhaled trichothecene mycotoxins because their lungs are growing rapidly. The potential role of trichothecene mycotoxins in producing pulmonary hemorrhage is supported by animal studies (15,16). Intranasal inoculation of mice with toxigenic S chartarum spores resulted in development of severe intra-alveolar, bronchiolar and interstitial inflammation with hemorrhagic exudate in the alveolar lumina. Only mild inflammatory changes were detected when nontoxin-containing spores were used. Taken together, these data suggest that infants may rarely develop pulmonary hemorrhage following heavy inhalation of toxigenic S chartarum. There are no reports of pulmonary hemorrhage in older children and adults following exposure to this fungus.

‘Sick building syndrome’ and S chartarum:

Several epidemiological surveys of ‘sick buildings’ have implicated S chartarum as a potential cause of respiratory, dermatological, eye and a variety of other nonspecific symptoms (11–13). One of the best documented reports describes a water-damaged home with five inhabitants who had complained of sore throat, diarrhea, headache, malaise, dermatitis, intermittent focal alopecia and other constitutional symptoms over a five-year period (11). Toxigenic S chartarum was isolated from air samples, and heavy contamination of air ducts and water-damaged building materials was demonstrated. Workers involved in the cleaning of the contaminated air ducts and removal of debris developed significant cutaneous and respiratory irritation. After repairs were completed, the occupants returned and had no further symptoms. Another investigation of a water-damaged office building in New York, New York whose employees complained of similar symptoms, detected widespread contamination of building materials such as sheetrock (drywall) and insulation material, carpets, stored paper products and the air ventilation system with toxigenic strains of S chartarum (12). The significant water damage and heavy mold contamination found are typical of these and other reports of ‘sick buildings’. Commonly reported respiratory tract symptoms include nasal irritation, burning and congestion, cough, wheezing, chest tightness and dyspnea. Central nervous system manifestations include headache, irritability, lightheadedness, sleeping difficulty, concentration problems and mental fatigue. Alopecia, rashes, eye irritation and various constitutional symptoms are also frequently reported. The nonspecific nature of these symptoms makes it extremely difficult to assess causality. Type 1 hypersensitivity to fungal allergens is the most likely mold-related cause of respiratory and eye symptoms in children with a compatible exposure history, particularly in those known to suffer from asthma and allergic rhinitis. Mycotoxin-induced symptoms, although less common, must also be considered, particularly when exposure to a toxin-producing fungus such as Stachybotrys species is demonstrated.

Hematological and immunological toxicity following inhalation of S chartarum:

Mild immunological abnormalities have been described in employees in an office building heavily contaminated with toxigenic strains of S chartarum (12). A mild but statistically significant reduction in mature CD3 cells of these office workers compared with those of controls was reported. Reduced lymphocyte responses to mitogens (concanavalin A and phytohemaglutinin) were also detected, although the differences did not reach statistical significance. No evidence of bone marrow suppression was demonstrated. Based on this report, it appears that prolonged and intense respiratory exposure to toxigenic strains of S chartarum may result in some degree of immunological dysfunction. However, the level of toxin exposure by the inhalation route is much lower than that following ingestion of heavily contaminated food; consequently, bone marrow suppression and immunotoxicity, if they occur at all, are likely to be mild.

The adverse health effects associated with exposure to S chartarum are a function of the level and duration of exposure. Significant adverse health effects are unlikely in the absence of heavy and prolonged exposure. Unfortunately, what constitutes ‘heavy’ exposure has not yet been defined. In the school portable setting, exposure to spores and/or mycotoxins may occur, although such exposures are likely to be low level and transient; consequently, any adverse health effects, if they occur at all, are likely to be mild and short lived.

MANAGEMENT

Awareness of the potential adverse health effects associated with inhalation of S chartarum and other fungi in the indoor environment is the first step to the appropriate management of the health effects. Children who suffer from frequent upper and lower respiratory tract, eye, skin and constitutional symptoms, who also report prolonged and intense exposure to damp and mold contaminated buildings, be it at home or school, should be evaluated for possible fungal allergy and mycotoxin exposure. Similarly, the possibility of exposure to toxigenic S chartarum should be considered in infants with idiopathic pulmonary hemorrhage who have resided in buildings heavily contaminated with S chartarum.

Type 1 hypersensitivity to fungal antigens can be evaluated by skin testing (not currently available for Stachybotrys species) and measurement of allergen-specific immunoglobulin E (radioallergosorbant test). Such investigations should be reserved for those with significant allergic symptoms and a clear history of heavy exposure to a mold-contaminated environment. No specific laboratory tests are available for mycotoxin exposure; hematological and immunological investigations are unnecessary in the absence of opportunistic infections or coagulopathy suggestive of bone marrow failure. Type 1 hypersensitivity reactions to fungal allergens are best managed by reducing the level of exposure. The role of desensitization remains controversial. No specific therapy is available for trichothecene exposure, and the most important aspect of management is the avoidance of exposure.

In a child with symptoms felt to be temporally related to the school environment, an assessment of the child’s school should be carried out so that potential irritants and allergens can be identified. The local school board or health department should be contacted. Because of the nonspecific nature of the symptoms and the lack of reliable laboratory tests, the environmental assessment is of paramount importance. In addition to fungal contamination, poor indoor air quality resulting from inadequate air circulation, and high levels of allergens in settled dust or toxins such as formaldehyde released from indoor carpets must be considered as potential causes of symptoms (1). Buildings, including homes and schools, found to be heavily contaminated with molds, particularly S chartarum, should undergo thorough cleaning and repair to remove the offending agent(s) and prevent further water damage and mold overgrowth.