Fungi in the domestic environment and community settings – association with health problems
D. Stevens
March 2004
Summary
This report reviews the external literature on the infection potential in community and domestic settings with particular reference to fungi (commonly referred to as mould).
The report looks at what are fungi, evidence for fungal contamination in the indoor environment, and why fungi are a problem in community settings and the domestic environment. Infections, allergies and health effects that fungi cause are discussed.
The evidence of where fungal contamination in community and domestic settings has been linked to health effects and infection outbreaks is reviewed. The evidence showing that removal of mould plays a part in reducing or eliminating such infections and allergies is also highlighted.
Finally, the evidence that removal of mould from the home improves indoor air quality and the effectiveness of chemicals is discussed.
Contents
1. Background
2. What conditions favour fungal growth?
3. Evidence for occurrence of fungal contamination indoors
3.1 Surveys of fungi in community and domestic settings
3.2 Concentrations of fungi
4. Why are fungi a health problem?
4.1 Surface damage
4.2 Spores
4.3 Allergens
4.4 Cell wall components
4.5 Mycotoxins
4.6 Volatile organic compounds
5. Fungal infections
6. Health problems associated with fungi
6.1 Allergies
6.2 Respiratory/Non-respiratory symptoms
6.3 SBS/BRI
7. Evidence linking presence of fungi in the home to health problems
7.1 Respiratory Illnesses
7.2 Non-respiratory illnesses
7.3 Asthma
7.4 Allergies
7.5 Illness associated with Stachybotrys atra
7.6 Alveolitis
8. Evidence linking presence of fungi in community settings to health problems
8.1 Hospitals
8.2 Day care centres/schools
8.3 Other buildings
9. Removal of exposure to mould
10. Efficacy of chemicals against fungi
11. Conclusions
12. References
1. Background
Fungi are ubiquitous in all environments, indoors and outdoors. All fungi are eukaryotic organisms and exist in different growth forms such as rusts, mushrooms, mould and yeasts. Yeasts grow as oval or spherical single cells and multiply by budding and division. Filamentous fungi (more commonly known as moulds) consist of long, branching filaments called hyphae. Fungi reproduce via formation of spores from sexual or asexual processes. Some fungi can exhibit both growth forms and are known as dimorphic fungi. Many species of fungi live as commensal organisms in or on the surfaces of the body e.g. Candida, Rhodoturula. Candida albicans can be cultured from more than half of the population that has no evidence of active infection.
This report reviews the external literature on the potential health problems caused by fungi (more commonly referred to as mould or mildew) with regard to its presence in the domestic home and community settings. It does not address fungi associated with food spoilage/food poisoning or fungal exposure in agricultural settings.
2. What conditions favour fungal growth?
Airborne fungal spores are present in outdoor air all year round, usually in high numbers. These spores can enter indoor environments via natural ventilation (open windows and doors) and mechanical ventilation systems such as air conditioning. They are also brought indoors on people’s clothing and shoes and pets. Therefore, indoor fungi can be a mixture of fungi from outdoors and fungi from indoor sources. Fungi can be present in the soil of houseplants, in house dust or on pets, as well as on household surfaces.
Mould, or mildew as it may be referred to, likes warmth and moderate to high humidity, and so can be a problem in developing countries where humid weather conditions are frequent. In developed countries, the high humidity and temperatures often found in bathrooms and kitchens are conducive to mould growth. Activities such as drying laundry indoors, on clothes driers or in tumble driers not vented to the outside, can increase humidity levels in the home. Water damaged carpets, ceilings or walls are prime sites for new growth if they continue to remain damp. Buildings where mould growth problems are reported have usually have water damage, e.g. leaking roofs or plumbing. Penicillium spore counts are related to home dampness (Li and Hsu 1995). Provided there is sufficient moisture, fungi may grow on any building material (Pasanen et al. 1991). Damp housing is a common problem and is often associated with mould problems (see table 1). Moisture and mould are also common in buildings used as day-care centres (DCC).
Table 1: Studies on damp/mould problems
Country / Findings / ReferenceAustria / 8% of homes reported by their occupants to be damp or mouldy / Hutter et al. 2002
Finland / 70% of day-care centre buildings had moisture or water damage problems / Ruotsalainen et al. 1993
Finland / 52% of houses assessed had a moisture problem / Koskinen et al. 1999a
Finland / visible mould or damp was reported by 15% of 10,000 students surveyed / Kipelainen et al. 2001
Netherlands / 24% of homes had dampness / Brunekreef 1992
Sweden / Dampness was found in 27% of homes / Norback et al. 1999
UK / 2.5 million homes affected by mould or damp / Smith et al. 1992
UK / 25-33% of houses affected by dampness, condensation or mould / Williamson et al. 1997
Association of health problems of the occupants with damp or mouldy homes has been studied. In some studies information on home dampness and/or mould and problems with health was obtained through completion of questionnaires by occupants rather than observations by researchers, so the information is on self-reported health problems rather than clinically diagnosed health problems. It has been suggested that an awareness of an association of living in a damp home and respiratory health problems may lead to over-reporting of symptoms by occupants of damp homes or over-reporting of damp problems if occupants have respiratory health problems (Strachan 1988).
The results of studies can be difficult to compare because the methods of measuring exposure and health outcomes have not been standardised. Several studies have found an association between reported respiratory symptoms/infections in children and reported damp/mould in the home (Fischer et al. 1988, Strachan and Sanders 1989, Dales et al. 1991b, Jaakkola et al. 1993, Verheoff et al. 1995, Yang et al. 1997, Andriessen et al. 1998, Koskinen et al. 1999b). Studies of children’s health are the most reliable because the effects of smoking and occupational exposures are absent. Studies of adult health have also shown that damp housing is associated with increased prevalence of respiratory symptoms and/or asthma (Dales et al. 1991a, Pirhonen et al. 1996, Koskinen et al. 1999a, Kipelainen et al. 2001).
3. Evidence for occurrence of fungal contamination indoors
3.1 Surveys of fungi in community and domestic settings
There have been a number of studies investigating fungal species in the home. Table 2 shows the global extent of mould problems in homes. As many as 29 different genera of fungi have been detected in both indoor and outdoor air at a single residence (Gots et al. 2003). In one study, spores of Penicillium spp. and Cladosporium spp. were isolated on every occasion from at least one room in all homes (Strachan et al. 1990). Aspergillus spp. and other fungi as well as yeasts were also isolated. Total airborne mould counts varied from 0-41000 cfu/m3 but were usually in the range 50-1500 cfu/m3.
Table 2: Results from studies on mould problems in the home
Location / Findings / ReferenceAustralia / Visible mould growth was present in every house at some time during the study / Garrett et al. 1998
Berlin / 63% homes had large amounts of viable fungal propagules or visible fungal growth / Dill and Niggemann 1996
Finland / Visible mould was reported in 3.7% of homes, and 5.5% reported mould odour / Pirhonen et al. 1996
Lithuania / 86% of dwellings investigated had visible mould growth / Krikstaponis 2000
Poland / Penicillium and Aspergillus occurred in 97% and 63% respectively of homes / Gorny and Dutkiewicz 2002
UK / Visible mould was found in 46% of households / Platt et al. 1989
In a survey in Central Scotland the main fungus isolated from indoor air was Penicillium, with Cladosporium being the second most common (Hunter et al. 1998). They also isolated pink and cream yeasts (Rhodotorula and Sporobolomyces) from the air of over 90% of houses. Penicillium, Cladosporium and Aspergillus were also the predominate fungi isolated from homes surveyed in Netherlands (Beaumont et al. 1985), North America (Miller et al. 1988), Taiwan (Su et al. 2001, Canada (Li and Kendrick 1995), Germany (Dill and Niggerman 1996), Lithuania (Krikstaponis 2000) and Turkey (Unlu et al 2003).
Wickman et al. (1992) found that Aspergillus levels correlated with wall to wall carpets. Cole and co-workers have also comprehensively documented fungal contamination of soft furnishings in the home. Levels of fungal contamination in carpets and upholstery have been shown to be almost and above 100,000 cfu/g and contain fungi such as Cladosporium, Alternaria and Penicillium (Cole et al. 2000). Other fungi recovered include Aspergillus versicolor, Rhodotorula, Aspergillus fumigatus, Aspergillus flavus, Paecilomyces, Trichoderma, Phialophora, Rhizopus, Ulocladium, Fusarium and Stachtbotrys (Cole et al. 1999). Klanova (2000) also found that higher concentrations of fungi in dwellings in the Czech Republic corresponded with presence of soft furniture and carpeting.
Fungi such as Aspergillus niger may also form in the topsoil of houseplants. In hospitals and homes, the soil from a wide range of potted plants was found to be a major source of A. fumigatus, as well as A. niger and A. flavus (Staib 1984). Fungi may be also found in air conditioning equipment, humidifier reservoirs, dehumidifier drip pans and showerheads.
In Denmark, Gravesen et al. (1999) investigated materials from 72 mould-infected public buildings. The most frequent isolated fungi were Penicillium, Aspergillus, Chaetomium, Ulocladium, Stachybotrys and Cladosporium.
3.2 Concentrations of fungi
Indoor ambient concentrations are influenced by several factors including climate, temperature, humidity, presence of houseplants, type of ventilation, type of furniture and carpeting present or presence of pets. Activities such as dusting, vacuuming and dusting will also affect fungi levels detected in the air (Pieckova and Jesenska 1999).
Sampling and survey approaches report their findings in various ways. Fungal concentrations are reported as either viable colony-forming units per cubic metre (cfu/m3) or total spore counts per cubic metre. Spore concentrations are usually much lower in homes or community settings than in agricultural settings, but concentrations as high as 450,000 cfu/m3 have been reported (Hunter et al. 1988, Platt et al.1990).
It is suggested that the fungal levels indoors should be related or compared to levels measured outdoors because indoor levels of fungal spores are strongly dependent on the outdoor level of spores. However, Fischer and Dott (2003) state that in buildings with mould problems, the incidence of Penicillium and Aspergillus is often higher than in outdoor air. For example, on investigating fungal contamination of indoor air in homes of patients with asthma bronchiale, Senkpiel et al. (1996) found spore counts to be 4 to 40 times higher than that measured outdoors. Bardana (2003) suggests that the levels should also be measured in homes where occupants have not complained of health problems as this gives a normal baseline for the geographical area and season of the year. Hutter et al. (2002) found that classification of visible mould growth by medical doctors in flats in Austria correlated significantly with the ratio of indoor/outdoor concentrations of fungal spores. Gots et al. (2003) reviewed 31 studies that looked at indoor and outdoor air ambient concentrations of fungi in domestic homes and commercial buildings in which the occupants did not have health complaints. For domestic homes, the indoor average viable fungal concentration was 1252 cfu/m3 and ranged from 17-9100 cfu/m3, The outdoor concentrationranged from 20-11,883 cfu/m3, with an average of 1524cfu/m3. The total spore count indoors ranged from 68-2307 spores/m3, whilst the outdoor ranged from 400-80,000 spores/m3
In reviewing the many guidelines for acceptable quantitative levels of fungi in indoor environments, Rao et al. (1996) found there is no uniform agreement among them. However, data reviewed by Gots and colleagues (2003) suggest that current recommendations do not reflect the concentrations found in buildings in which the occupants have no health complaints, and they do not reflect the levels that could be associated with health problems.
As fungal concentrations are reported as either cfu/m3 or spores/m3, Klanova (2000) recommends that indoor fungal concentrations >2000cfu/m3 should be considered a serious risk factor for health of occupants, whereas Santilli and Rockwell (2003) state a concentration of >1000spores/m3 should be considered an unhealthy indoor environment. In Czech Republic, Klanova (2000) found occupants of mouldy rooms where the average concentration of fungi was 2476 cfu/m3 had health complaints such as cough, headache, rhinitis and sore throat.
4. Why are fungi a health problem?
Fungi in indoor environments are a problem for a number of reasons:
- They deteriorate/damage surfaces
- They cause unpleasant odours
- They can cause an allergic response
- They can be responsible for infections
- They can cause other health problems
4.1 Surface damage
Fungi cause discolouration and deterioration of household surfaces e.g. the characteristic blackening of walls or ceilings, wallpaper, grouting between tiles, plaster and around window frames in areas such as the bathroom. Fungi are usually referred to as mould or mildew in this context.
Some fungi may also cause wood decay. Dry rot is a localised fungal infection of damp timber and will die when the moisture is removed. Dry rot, which is more aggressive than wet rot, starts in wet timbers but can continue to grow with a restricted moisture supply. The fungus can travel through brickwork and plaster in search of further moisture spreading extensively through masonry to attack any timbers it meets.
4.2 Spores
The growth habitat of spore-forming fungi facilitates aerosol dispersal. Moulds produce millions of spores, which are loosely attached such that even slight air currents will disturb the spores making them airborne. Due to their small size (large spores are 10-20m, average 1-5m) spores easily stay airborne and may be respirable and breathed deep into the airways. Spores are very tolerant to dryness, changes in temperature, UV light and some chemicals. The spores may carry allergens and toxins, which are stable and may stay active even after the spore has lost its viability.
4.3 Allergens
Some fungi do not produce infections but can cause allergic reactions. Fungal spores are generally recognised as important causes of respiratory allergies, in both the lower and upper respiratory tracts (WHO 1998). Allergic reactions usually occur at the site of allergen deposition. When larger fungal spores are inhaled, they are deposited in the nasopharynx and are associated with nasal and/or ocular symptoms usually referred to as hayfever (also known as rhinitis). Spores of <5m can penetrate the lower airways (Burrell 1991), where allergic reactions will usually manifest as asthma.
4.4 Cell wall components
ß(1-3)-glucans are major cell wall components of mould. In a pilot study, Douwes et al. (1998) measured ß(1-3)-glucan levels in house dust from floors and mattresses in 25 German homes, and was found to range from 182-3507µg/dust. ß(1-3)-glucan levels per square metre were found to be positively associated with total culturable fungi and Alternaria in house dust. In a larger follow-up study of 395 homes, a strong positive correlation was found between concentrations of ß(1-3)-glucan per square metre and culturable mould spores. Additionally, there was a correlation of ß(1-3)-glucan with culturable mould spore counts of Cladosporium and Alternaria per gram of dust (Gehring et al. 2001). A study from Beijer et al. (2002) suggests that an inhalation challenge to ß (1-3)-D-glucan has an effect on inflammatory cells and this effect may be related to a chronic exposure to moulds at home.
4.5 Mycotoxins
Some fungi produce secondary metabolites that are of valuable clinical use such as antibiotics. Other secondary fungal products called mycotoxins are toxic to vertebrates and other animals. There are more than 300 known mycotoxins. Aspergillus,Stachybotrys, Fusarium and Trichoderma produce mycotoxins. Mycotoxins are non-volatile but exposure may take place through inhalation or skin contact with toxin-carrying spores or mycelium. Mycotoxins associated with inhaled spores may be absorbed via the respiratory epithelium and translocated to other sites, possibly producing systemic effects (Flannigan et al. 1991).
Stachybotrys atra (also referred to as Stachybortrys chartarum) produces very potent mycotoxins referred to as satratoxins (Sorenson et al. 1987). It can grow on material with a high cellulose and low nitrogen content, such as fibreboard, paper, dust and lint, particularly when moisture is present. Under field conditions, several trichothecences have been detected in building materials heavily and naturally contaminated with S. chartarum (Gravesen et al. 1999).
The chemical make-up and structure of mycotoxins is available in a recently published extensive review (Bennett and Klich 2003).
4.6 Volatile organic compounds
Mould can also cause unpleasant odours (due to 2-octen-1-ol and geosmin) which are difficult to disguise. Numerous fungi e.g. Aspergillus, Penicillium and Fusarium have been found to produce volatile organic compounds (VOC) (Lewis et al. 1993). In buildings with visible mould growth, VOC at concentrations of 10-100ng/m3 of air have been found (Keller et al. 1998). The total concentrations of microbial VOC correlated to the odour perception in homes when cases have been classified in 3 groups: (1) fungus-like odour not recognisable (<35 ng/m3), (2) slight fungus-like odour (50-1720 ng/m3) or (3) strong fungus-like odour (160-12,300 ng/m3). Keller et al. concluded that concentrations above 50ng/m3 of airmay indicate indoor mould contamination, while outdoor concentrations are usually <10 ng/m3 air.
5. Fungal infections
Some fungi are pathogenic to healthy humans. Fungi cause superficial infections (or mycoses), where the fungus grows at the body surface such as the feet, skin, hair and nails, as well as the oral or vaginal mucosa. The important causative agents are the dermatophyte fungi of the genera Epidermophyton, Microsporum and Trichophyton. They are spread by direct contact and are highly contagious and easily spread to other individuals. Candida albicans can also cause superficial infections such as thrush and nappy rash. Candida infections are usually the result of antibiotic therapy that suppresses the normal resident bacterial microflora allowing Candida to flourish.
Infections within the body (deep mycoses) involve internal organs and are usually life- threatening. They are rare in healthy humans. However, people with impaired immune functions (e.g. cancer patients receiving chemotherapy or people with AIDS) are at significant risk of opportunistic fungal infections. They are acquired by inhalation of spores or by entry through wounds, whilst some exist as part of the normal body flora (e.g. Candida) and are innocuous unless the body’s defences are compromised in some way. Other opportunist fungi include Aspergillus, Penicillium, Cryptococcus neoformans and Histoplasmacapsulatum.