Botrytis cinerea

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Code: m7
Latin name: Botrytis cinerea
Source material: Spores and mycelium
Family: Sclerotiniaceae

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Botrytis cinerea is called ‘the grey mould’, as it covers the decayed tissues with conidiophores.

Mould

A mould, which may result in allergy symptoms in sensitised individuals.

Allergen Exposure

B. cinerea has a worldwide distribution but occurs mainly in humid, temperate and subtropical regions. B. cinerea is found regularly in soil, though its proportion of the total fungus population is not high. It is considered to be the most prevalent of the 25 species belonging to the genus Botrytis. B. cinerea is an ascomycete with high genetic diversity and a complex population structure. (1) A considerable genetic variability has been observed in different Botrytis magnoceps strains (polyploidy). Although there are fungicides for its control, many classes of fungicides have failed because of its genetic plasticity. (2)

The fungus grows either parasitically or saprophytically on the vast majority of plants, vegetables and soft fruits, and can cause substantial crop losses (especially in greenhouses), while other Botrytis species have narrower host ranges. (Cited in 3) Parasitically it causes blight or rot of leaves, flowers and fruits. It is called ‘the grey mould’ because it covers the decayed tissues with conidiophores, e.g. the grey mould of cabbage or lettuce, tomato. It is especially seen on soft fruits, e.g. strawberries and grapes. Botrytis exposure is relatively high in environments such as greenhouses and grain mills, and in wine cellars during grape pressing. (Cited in 3, 4)

B. cinerea is known to infect more than 200 plant species, including sunflower, (5) kiwi fruit, (6) tomato plants, (7) berries, (8) citrus and strawberry (9) and cherry, causing significant economic losses worldwide. Secreted proteins are released as an initial response of the fungus to its plant host. (10) It can affect most ornamental plants and may be responsible for serious pre-harvest diseases and postharvest losses in fruits, vegetables and flowers. (11) It is a very complex species in which different populations seem to be adapted to different hosts. (12)

B. cinerea is a necrotrophic fungus that affects many plant species, although its most notable hosts may be wine grapes. In viticulture, it is commonly known as botrytis bunch rot; in horticulture, it is usually called grey mould or gray mold. The fungus gives rise to two different kinds of infections on grapes: grey rot is the result of consistently wet or humid conditions, and typically results in the loss of the affected bunches; noble rot occurs when drier conditions follow wetter, and can result in distinctive sweet dessert wines, such as Sauternes or the Aszú of Tokaji.

The conidia of B. cinerea are mainly airborne, and their release is regulated by a hygroscopic mechanism after a drop in humidity and air movement – such as rain splashes, which can release large numbers. (Cited in 3) In a greenhouse of geranium cuttings, for example, any activity that results in air movement (such as planting, irrigation, cleaning, fertilisation and even spraying fungicides) may raise conidia levels substantially. (13)

Similarly, the airborne fungi present in water-damaged buildings before and after reconstruction showed viable B. cinerea spores were only found during demolition activity, (14) although other researchers have found them in dust from water-damaged buildings. (15)

Botrytis has an all-year presence in the temperate climate of Europe, with an approximate season starting in April and lasting until November, and peaking in August or September. However, this varies between countries: a 15-year study in Thessaloniki (Greece) showed a low, nearly even distribution over the year, with a slight decrease in December and January, whereas in Porto Alegre (Brazil), Botrytis was only found in autumn and winter; and in Porto (Portugal), a 1-year study found a seasonal distribution from April to December, where Botrytis peaked from July to December with a low in November. In Canada, low exposure to Botrytis was found at schools in winter (November-February) and spring (April-June), with a major increase in the autumn season (September-November). (Cited in 3)

B. cinerea is characterised by abundant hyaline conida (asexual spores) borne on grey, branching, tree-like conidiophores. The fungus also produces highly resistant sclerotia as survival structures in older cultures. It survives winters as sclerotia or intact mycelia, both of which germinate in spring to produce conidiophores. The conidia are dispersed by wind and rainwater and cause new infections. B. cinerea produces a range of cell-wall-degrading enzymes, toxins and other low-molecular-weight compounds such as oxalic acid. New evidence suggests that the pathogen triggers the host to induce programmed cell death as an attack strategy. (2) The dispersal of spores follows a diurnal pattern in which the spore level increases in the early morning hours, decreasing towards the late afternoon. Exposure to Botrytis may also increase during rainfall at night. Thus, Botrytis-allergic patients should ventilate their rooms in the late evening, at night, or in the very early morning hours, except during rainfall. (3)

Allergen Description

No allergens have been characterised.

B. cinerea has aspartic proteinase (AP) activity, i.e. contains an alkaline thiol protease. (16, 17) In other fungi, aspartic proteases have been shown to have allergenic potential; however, the allergenic potential of this aspartic proteinase has not been investigated. The purified AP had an apparent molecular mass of 43 kDa. The enzyme retained 85% of its activity by treatment at 50°C over 120 min; it maintained 50% of activity after 60 min of heating at 60°C. Furthermore, the protease retained almost complete activity after 4 weeks storage at 25°C. (17)

A study aiming to characterise fungal virulence factors using proteomic research identified 22 protein spots, with some corresponding to forms of malate dehydrogenase and glyceraldehyde-3-phosphate dehydrogenase. Two more spots matched a cyclophilin and a protein with an unknown function. (12) Cyclophilin and malate dehydrogenase have been shown to have allergenic potential in other fungi, but were not evaluated in this study.

B. cinerea is generally not described or shown as a mycotoxin-producing fungus, although one study found that it had ciliostatic activity in a chicken trachea bio-assay. Like other fungi, B. cinerea contains (1?3)-ß-D-glucan and chitin in its cell wall. Studies have shown that fungal (1?3)-ß-D-glucan can elicit respiratory inflammation. (3, 18) Moreover, a recent study indicates that chitin may also be involved in allergic reactions upon frequent exposure. (3, 19, 20)

Potential Cross-Reactivity

No studies have evaluated the cross-reactivity of B. cinerea. If the aspartic proteinase, cyclophilin and other proteins detected have allergenic potential, then cross-reactivity with other fungi containing these proteins is possible.

Clinical Experience

IgE-mediated reactions

Individuals exposed to B. cinerea may be sensitised to this fungus without experiencing any clinical symptoms, or may experience exacerbation of symptoms of asthma, hayfever or sinusitis, or may develop hypersensitivity pneumonitis (also known as ‘winegrower's lung’). IgE- binding components from B. cinerea appear to have both early- and late-phase antigens. (21)

Allergy to B. cinerea has been estimated to range between 1.3% and 52%, with a calculated median of 18.8%. (3) In certain occupational settings, such as in the production of raspberries or in greenhouses, or in the production of wine and certain dessert wines where infestation with B. cinerea is necessary, exposure to B. cinerea can reach high levels. (Cited in 3)

In a panel of 1 250 Swedish patients with ‘allergy-related’ complaints, and skin-prick tested with B. cinerea, a strong positive reaction was demonstrated in 50% of mould-sensitised patients. (22) Of 150 of these patients tested, 50% were serum-specific IgE-positive for B. cinerea. (22)

Studies have found that allergy towards B. cinerea is the most prevalent allergy, or is just as prevalent as allergy towards the typically investigated Alternaria, Cladosporium and Aspergillus in young Finnish children newly diagnosed with asthma and schoolchildren suspected of asthma. (23, 24) Of 144 Finish school children with suspected asthma, 1.3% were skin-prick-test positive for B. cinerea. (23) Of 122 Finnish children with newly-diagnosed asthma, 2.6% were SPT positive for B. cinerea. (24) As authors have pointed out, this is surprising considering that no airborne B. cinerea was identified at the children’s school, (23) and that B. cinerea seems to have a low prevalence in ambient air in Finland. (3) In an earlier Finnish study of 121 suspected mould-allergic children with asthma, of which 40.5% were positive for a mould screen, 24% had raised serum-specific IgE for B. cinerea. (25)

Other European studies confirm sensitisation to B. cinerea to be significant: in 404 European patients with suspected allergies, 2.7% had raised serum-specific IgE for B. cinerea. (26, 27)

A study was undertaken to see whether the principal airborne fungi in the North-East Netherlands were also found to be the most reactive in skin testing. Concurrent atmospheric samples were taken at the same time as skin-prick tests of 833 patients were evaluated for recurrent bronchial obstructive complaints and a suspected allergy. Of these, 4.6% were shown to have skin-prick-test reactions consisting of a wheal of 10 mm diameter or more to one or more of the fungi being tested. The airborne fungal composition consisted of almost three-quarters of seven genera, namely (in order of occurrence): Cladosporium (42.6%), Botrytis (8.6%), Yeasts (7%), Penicillium (5.8%), Basidiomycetes (5.7%), Aspergillus (3.7%), and Alternaria (0.9%). In skin testing, however, a different order of prevalence was found: Beauveria (6.8%), Botrytis (6.1%), Aspergillus (4.7%), Mucor (3.8%), Epicoccum (3%), Cladosporium (2.3%), and Alternaria (1.1%). The authors concluded that the most prevailing airborne moulds were not necessarily the most potent allergens, at least in skin testing. Aspergillus and Botrytis showed a high sensitisation rate, while Cladosporium and Alternaria did not. Of 68 patients with suspected allergy or asthma, 7.3% were skin-prick-test positive for B. cinerea. (28)

In the USA, studies have demonstrated B. cinerea to be a significant allergen. In a Chicago study of a subgroup of 39 allergic rhinitis patients with suspected mould allergy, of which 44% were positive to a test panel of mould, 28.2% had raised B. cinerea serum-specific IgE. Of 32 randomly-selected patients of this group with suspected allergic rhinitis, 18.8% had raised serum-specific IgE for B. cinerea. (29) In a study of 10 American patients with allergic fungal sinusitis, 50% were skin-prick-test positive for B. cinerea. (30)

A study evaluating specific IgE in a standard and extended mould panel (which included B. cinerea) in order to evaluate sensitisation to mould in Europe and the USA found that in Sweden and Denmark, 18% additional mould-allergic patients could be identified, and 75% additional in the USA. (31) B. cinerea allergy was the second-most prevalent mould allergy in Sweden and Denmark, and the most prevalent in the USA. (30) A second research group found an additional 3.3% of mould-allergic patients with the extended panel, and B. cinerea was the fourth-most prevalent fungal allergy in the test groups. (25) In 21 American patients with suspected mould allergy, 52% had raised specific IgE to a mould-panel mix, whereas 52% had raised serum-specific IgE for B. cinerea; (30) whereas for Danish and Swedish patients, these figures were 77% and 47% respectively. (30)

Importantly, Botrytis may be found in any flat or dwelling that may be contaminated by mould, and not only in occupational settings. (32, 33, 34) In a Polish study of buildings in Lodz, mould contamination in the air of flats was high, and exceeded accepted limits in 75% of the cases. The most frequent species isolated from examined rooms were: Penicillium, Cladosporium, Aspergillus, Acremoniu and Alternaria. Evaluation of the occupants found that 16% were sensitised to moulds (includ B. cinerea). (35)

The general agreement with many of the studies is that although exposure to this mould in ambient air in most of the regions studied seems to be low, a substantial proportion of subjects tested do have an allergy to B. cinerea, i.e. there is no correlation between the ability to induce allergy and a fungus’ proportional share of the total fungal spore level. (3) However, for non-specific symptoms such as coughing and irritation of nose and eyes, a correlation between these symptoms and exposure to total fungal spore levels above 2×104 spores/m3 was reported in Norwegian farmers, but there was no correlation with wheezing and chest tightness. (Cited in 3)

An important context for exposure to B. cinerea occurs in occupational settings, and a number of studies have contributed to the understanding of the allergen in this area.

In a South African cross-sectional study of 207 workers on table grape farms, skin-prick tests using extracts of 8 common aeroallergens (including grape mould (B. cinerea) and Tetranychus urticae) found that the prevalence of sensitisation was highest to T. urticae (22%) followed by house dust mite (16%). Only 1% had allergy towards B. cinerea, though a relatively high exposure could have been expected. In the same group, 1.6% suffered from allergy to at least one fungus in a mould mix containing Alternaria alternata, C. herbarum and Fusarium. Hence, even though the level of allergy towards Botrytis was low it made up a large proportion of the fungal allergies. (36)

Occupational asthma and sensitisation to mould and flower allergens has been found in greenhouse workers. The prevalence of B. cinerea is high in greenhouses. (37, 38) In a study of the prevalence of allergy towards B. cinerea in greenhouse workers in the Netherlands, 4% of 104 chrysanthemum workers (39) and 13.8% of 109 bell pepper workers were shown to be sensitised to this mould. (40) Interestingly, the data were obtained by the same research group and using the same test extract. (3) The greenhouse workers’ respective prevalences of allergy to Botrytis are comparable to the values found in atopic and suspected atopic test subjects in the Netherlands.

However, patients suspected of mould allergy in the Netherlands had a higher prevalence of allergy to Botrytis. In a study in the Netherlands of 692 suspected allergic patients, 4.9% were skin-prick-test positive to Botrytis extract (from cultivated mould mycelium); and of 180 suspected mould-allergic patients, 24% were skin-prick-test positive. (41)

In an Austrian report, two farm workers working with noble rot grapes were described who developed hypersensitivity pneumonitis/allergic alveolitis caused by B. cinerea. (42)

A conclusion reached by many authors is that sensitisation to B. cinerea may well be underestimated (Cited in 3, 43 )and may occur more frequently than previously anticipated, and that this mould is not included in standard allergy panels but should be. (3) A survey of standard skin-prick tests from 29 allergy centres in Europe showed that routine testing is mainly carried out for one or two fungi, these being Alternaria and Cladosporium. Some of the centres in southern Europe test for more species, including Fusarium and Penicillium; but B. cinerea was tested routinely only at centres in Kraków and Montpellier. (26) The authors suggested that routine screening for B. cinerea should be implemented.

Other reactions

Nil known.

Compiled by Dr Harris Steinman.

References

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As in all diagnostic testing, the diagnosis is made by the physican based on both test results and the patient history.