Abstract
Compost is an ecological niche for Aspergillus fumigatus due to its role as a decomposer of organic matter and its ability to survive the high temperatures associated with the composting process. Subsequently, composting facilities are associated with high levels of A. fumigatus spores that are aerosolized from compost and cause respiratory illness in workers. In the UK, gardening is an activity enjoyed by individuals of all ages, and it is likely that they are being exposed to A. fumigatus spores when handling commercial compost or compost they have produced themselves. In the present study, 246 citizen scientists collected 509 soil samples from locations in their gardens in the UK, from which were cultured 5,174 A. fumigatus isolates. Of these isolates, 736 (14%) were resistant to tebuconazole: the third most-sprayed triazole fungicide in the UK, which confers cross-resistance to the medical triazoles used to treat A. fumigatus lung infections in humans. These isolates were found to contain the common resistance mechanisms in the A. fumigatus cyp51A gene TR34/L98H or TR46/Y121F/T289A, as well as the less common resistance mechanisms TR34, TR53, TR46/Y121F/T289A/S363P/I364V/G448S, and (TR46)2/Y121F/M172I/T289A/G448S. Regression analyses found that soil samples containing compost were significantly more likely to grow tebuconazole-susceptible and tebuconazole-resistant A. fumigatus strains than those that did not and that compost samples grew significantly higher numbers of A. fumigatus than other samples. IMPORTANCE The findings presented here highlight compost as a potential health hazard to individuals with predisposing factors to A. fumigatus lung infections and as a potential health hazard to immunocompetent individuals who could be exposed to sufficiently high numbers of spores to develop infection. Furthermore, we found that 14% of A. fumigatus isolates in garden soils were resistant to an agricultural triazole, which confers cross-resistance to medical triazoles used to treat A. fumigatus lung infections. This raises the question of whether compost bags should carry additional health warnings regarding inhalation of A. fumigatus spores, whether individuals should be advised to wear facemasks while handling compost, or whether commercial producers should be responsible for sterilizing compost before shipping. The findings support increasing public awareness of the hazard posed by compost and investigating measures that can be taken to reduce the exposure risk.
Highlights
The fungus Aspergillus fumigatus plays an important role in the environment as a decomposer, recycling nutrients from decaying plant matter into the soil
Fumigatus a globally ubiquitous fungus3. Exposure to this mould is medically important and it is estimated that humans inhale several hundred A. fumigatus spores per day4, which can trigger an immunoinflammatory response resulting in severe asthma with fungal sensitisation (SAFS) or allergic bronchopulmonary aspergillosis (ABPA)5
The concentration of spores and mycelial fragments averaged across the samples that grew A. fumigatus was 316 CFU/g, which ranged from 0 CFU/g in the sample collected from a border plus manure bag to 600 CFU/g in the sample collected from a manure bag
Summary
The fungus Aspergillus fumigatus plays an important role in the environment as a decomposer, recycling nutrients from decaying plant matter into the soil This highly sporulating mould is commonly found in woodchip piles, compost from household waste, sewage, sludge and mouldy hay, where its thermotolerance enables it to proliferate during the thermogenic phase of composting when temperatures reach 40-60oC2. The size of the spores allows them to bypass mucociliary clearance in the lung whereupon they must evade clearance by the host innate and adaptive immune responses. The size of the spores allows them to bypass mucociliary clearance in the lung whereupon they must evade clearance by the host innate and adaptive immune responses7 If they survive, germinated spores establish in lung cavities where they can eventually cause chronic pulmonary aspergillosis (CPA). The number of patients in the UK presenting with infections that are resistant to one or more of itraconazole (ICZ), voriconazole (VCZ)
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