Science of the Total Environment 788 (2021) 147832

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Science of the Total Environment

journal homepage: www.elsevier.com/locate/scitotenv

Review

Occupational exposure to fungi on recyclable paper pots and growing

media and associated health effects – A review of the literature
Anne Mette Madsen a,⁎, Brian Crook b
a
The National Research Centre for the Working Environment, Lersø Parkallé 105, DK-2100 Copenhagen, Denmark
b
Health and Safety Executive, Science and Research Centre, Buxton SK17 9JN, UK

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• Peziza ostracoderma is found on many

different growing and casing media.
• Other fungal species are also found on/
in growing and casing media.
• Hypersensitivity pneumonitis is caused
by fungi from growing and casing
media.
• The air and hands are important routes
of exposure to consider.
• Limited knowledge on occupational
health associated with growing and
casing media.

a r t i c l e i n f o a b s t r a c t

Article history: Different types of pots and growing and casing media, including biodegradable materials, are used for plant and
Received 1 May 2021 mushroom production. The fungus Peziza ostracoderma has gained attention for its visible growth on growing
Received in revised form 11 May 2021 media for plants and casing media for mushrooms. Through a review of the literature we aim to evaluate whether
Accepted 12 May 2021
exposure to fungi from recyclable pots and different growing and casing media occurs and causes occupational
Available online 18 May 2021
health effects.
Editor: Frederic Coulon Based on the published papers, specific fungal species were not related to a specific medium. Thus P. ostracoderma
has been found on paper pots, peat, sterilized soil, vermiculite, and rockwool with plants, and on peat, pumice,
and paper casing for mushrooms. It has been found in high concentrations in the air in mushroom farms. Also
Keywords: Acremonium spp., Aspergillus niger, A. fumigatus, Athelia turficola, Aureobasidium pullulans, Chaetomium globosum,
Greenhouse Chrysonilia sitophila, Cladosporium spp., Cryptostroma corticale, Lecanicillium aphanocladii, Sporothrix schenckii,
Hypersensitivity pneumonitis Stachybotrys chartarum, and Trichoderma spp. have been found on different types of growing or casing media.
Mushroom Most of the fungi have also been found in the air in greenhouses, but the knowledge about airborne fungal species
Peat
in mushroom farms is very limited. Eight publications describe cases of health effects associated directly with ex-
Peziza
posure to fungi from pots or growing or casing media. These include cases of hypersensitivity pneumonitis
caused by exposure to: A. fumigatus, A. niger, Au. pullulans, Cr. corticale, P. ostracoderma, and a mixture of fungi
growing on different media. Different approaches have been used to avoid growth of saprophytes including:
chemical fungicides, the formulation of biodegradable pots and growing media and types of peat. To increase
the sustainability of growing media different types of media are tested for their use and with the present study
we highlight the importance of also considering the occupational health of the growers who may be exposed
to fungi from the media and pots.
© 2021 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license (http://
creativecommons.org/licenses/by/4.0/).

⁎ Corresponding author.
E-mail address: amm@nrcwe.dk (A.M. Madsen).

https://doi.org/10.1016/j.scitotenv.2021.147832
0048-9697/© 2021 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
A.M. Madsen and B. Crook Science of the Total Environment 788 (2021) 147832

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2. Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
3. Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3.1. Fungi on surfaces of pots and growing media and in the air in greenhouses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3.2. Fungi on casings and in the air in mushroom farms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3.3. Fungi in other environments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3.4. Health effects of exposure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
4. Discussion and perspectives. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
Funding . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
CRediT authorship contribution statement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
Declaration of competing interest. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12

1. Introduction
The global use of greenhouses for food production has increased six-
fold over the past 20 years (Kirkham et al., 2020), and in addition
ornamental plants are produced in greenhouses. Furthermore, the
worldwide production of edible mushrooms has increased more than
30-fold since 1978 till 2013 (Royse et al., 2017), and is expected to con-
tinue to increase with the reduction of consumption of meat in some
countries. In the European Union, the total volume of growing media
produced yearly is around 3.5 × 107 m3, and the consumption of mineral
wool, perlite, and peat in professional horticulture is about 0.5, 0.3, and
1.6 × 107 m3, respectively (Schmilewski, 2017).
Manufacturing of growing media and plant pots have an important
environmental impact in life cycle assessment of several greenhouse
production systems (Vandecasteele et al., 2020). The fate of pots and
spent growing media may further contribute to this. Plastic and
rockwool are not degradable by enzymes and therefore will remain in
nature. As an attempt to reduce the environmental impact, biodegrad-
able materials as recycled food-grade paperboard, waste newspaper,
waste from distillation lees (Yamauchi et al., 2006), and from waste
pulp with the addition of cereal bran or peat (Sandak et al., 2019) are
also used for pot production. The casing for mushroom production
(Table s1) traditionally is made of mainly composed of peat, however
peat as a resource is limited, peatland is protected nature, and damaged
peatland is a major contributor of CO2 emission. Therefore, peat and
rockwool may be reused and handled repeatedly by the grower even
though they may be colonized by microorganisms. Furthermore, alter-
natives to peat, such as waste paper, wood fibre, and different types of
biowaste are used or being tested for their usefulness (Gruda, 2019;
Pardo et al., 2004; Sassine et al., 2007; Ślusarski and Smolińska, 2010).
People advising greenhouse growers have observed that growing
media may be colonized by visible saprophytic fungi (Carlile, 1999).
Due to the biodegradability of the paper pots, growth of fungi on their
surfaces during use have also been reported (Alsanius and Wohanka,
2019). These fungi have been of concern as they may inhibit the growth
of especially slowly growing plants and may also be an aesthetical
concern (Alsanius and Wohanka, 2019; Meinken et al., 2015). Further-
more, it may also present a health concern for the exposed workers,
and according to personal communication with greenhouse workers
and advisors, this potential health effect seems to limit the use of biode-
gradable paper pots.
The fungus found repeatedly on peat has previously been called
‘peat mould’ and ‘cinnamon mould’, and has been assigned to different
genera, but now belongs to the genus Peziza (Hennebert and Korf,
1975). In the scientific papers these visible fungi are called either Peziza
atrovinosa, P. fulva, or P. ostracoderma, or the names of the anamorphic
states Chromelosporium ollare and Chr. fulvum. These names are
described as synonyms, and we will in this paper in general use the
same names as used in the cited papers. The phylogenetic relationship
between some Peziza species and related genera has been studied
(Hansen et al., 2001; Norman and Egger, 1999). In addition to Peziza
spp., we expect that other fungi, for example Trichoderma spp. (Gams
et al., 2004; Hermosa et al., 1999), are also able to grow and sporulate
in these environments.
Work in greenhouses is associated with elevated exposure to
airborne fungi (Hansen et al., 2010) and can be associated with develop-
ment of acute and chronic respiratory symptoms (Zuskin et al., 1993),
including occupational rhinitis (Gerth van Wijk et al., 2011), allergy
(Thilsing et al., 2012), and asthma (Farruggia and Bellia, 2001;
Lindström et al., 2018; Monso, 2004; Monsó et al., 2002). Furthermore,
systemic inflammation has been shown to be related with exposure to
fungi during work in greenhouses (Madsen et al., 2020). Work with
mushroom production can cause exposure to high concentrations of air-
borne spores (Lee and Liao, 2014), and work with production of edible
mushrooms has caused development of extrinsic allergic alveolitis
(Kamm et al., 1991).
Airborne fungi in general in greenhouses are expected to be derived
mainly from plants as the exposure is seen to increase with the sizes of
plants (Hansen et al., 2012; Madsen et al., 2014). However, based on the
presence of fungi on the surfaces of pots or on growing and casing
media, we hypothesize that airborne spores may also derive from the
pots and growing and casing media, made airborne during work activi-
ties, and may cause occupational exposure of the airways. Furthermore,
spores on these surfaces may also cause exposure of the growers' hands
and arms. In this study, we aim to evaluate whether exposure to fungi
from recyclable pots and growing and casing media causes occupational
health effects of exposed workers. This will be done through a review of
the literature. We will compile knowledge about which fungal species
are present on the surfaces of pots and growing and casing media, and
whether they will also be present in the air making exposure of both
skin and the airways possible. For these fungi we will compile knowl-
edge about reports on health risks associated with exposure to these
fungi in general and in particular concerning cases of health effects
caused by the fungi growing on surfaces of recyclable pots and growing
and casing media. For further context we will illuminate factors that
may inhibit fungal growth on these pots and media.
2. Methods
We searched Google Scholar and PubMed for literature without any
year limitation using a combination of the search terms as summarized
in Table 1. As it appeared that other fungi than Peziza are also present
on the pots and on growing and casing media, we also used these fungal
names combined with the search terms in Table 1. The fungal names can

2
A.M. Madsen and B. Crook
be seen in the Table 2. We have not included data from papers where the
fungi have only been found in the rhizosphere or as an endophyte. A de-
scription of some of the growing and casing media can be found in
Table s1. The main results are presented in tables. In the tables we will
also mention the method used for identification of the fungi. Concerning
fungi on surfaces of pots and on growing and casing media the results for
greenhouses and mushroom production are presented separated.
3. Results
3.1. Fungi on surfaces of pots and growing media and in the air in
greenhouses
The following fungal species have been found on paper pot surfaces
in greenhouses: Acremonium spp., C. globosum, P. ostracoderma,
S. chartarum, and Trichoderma sp. (Table 2). Chromelosporium fulvum
has also been found to colonize paper which for experimental reasons
was placed in a chamber with a nutrient solution and plants (Le Marié
et al., 2014). In a greenhouse with plants in paper pots colonized by
S. chartarum around 30–100 S. chartarum conidia per m3 of air have
been found, and it increased to 7500 conidia per m3 during handling
of the pots (Dill et al., 1997) (Table 2).
The following species have been found on rockwool used as growing
medium: Ac. charticola, A. niger, Cladosporium sp., L. aphanocladii,
P. ostracoderma, S. chartarum, T. harzianum, and T. viride.
On peat based media A. fumigatus, A. niger, At. turficola, Sporothrix
schenckii, and P. ostracoderma have been found. On mixtures of the
peat and vermiculite or perlite P. ostracoderma has been found. In a sin-
gle study perlite has been used in combination with soil and here sev-
eral different fungi have been found. On coco fibre substrates A. niger
and T. harzianum were found and on sand with soybean chop
P. ostracoderma has been found. On bark media Cryptostroma corticale
and Peziza atrovinosa have been found (Table 2).
In an experimental study, different types of growing media
(pH adjusted to 5.5) were treated with the same fertilizer and inoculated
with P. ostracoderma. The fungus colonized the slightly decomposed peat,
coir pith, wood fibre, and a mixture of peat, coir pith, or wood fibre. In con-
trast, it did not grow well in moderately and strongly decomposed peat
nor in green waste and bark compost (Meinken et al., 2015). Most studies
have only investigated the air or the surfaces, but Acremonium spp.,
A. fumigatus, A. niger, Cladosporium sp., P. ostracoderma, L. aphanocladii,
and S. chartarum were all in at least one study found on both the surfaces
and in the air of the same environment (Tables 2 and 3). Fig. 1 gives an
overview of species found on the surfaces of paper pots and/or on grow-
ing media and whether they are also found in the air. In the cited papers
describing fungi on pots or growing media it was in general not
mentioned whether the pots were made of e.g. plastic or paper.
In studies in greenhouses in a botanical garden (Rodolfi et al., 2003)
and an orchid greenhouse (Magyar et al., 2011) Stachybotrys, but not
Peziza, were found in the phyllosphere or in the air; fungal species
Table 1
Summary of search terms.
Primary searcha Contextual search Exposure scenario search
Peziza Bark chips Airborne
Chromelosporium Coco fibre Exposure
Coir pith Indoor
Greenhouse Mushroom
Paper pots Occupational exposure
Rockwool Recycle
Peat pots
Perlite
Stonewool
Wood chips
a
Supplemented by all fungal names in Table 2.
Science of the Total Environment 788 (2021) 147832
found in these studies were cultivated and identified based on morphol-
ogy. Athelia turficola has not been found in the air in any of the studied
publications and none of the studies have looked particularly for this
species in the air in greenhouses.
3.2. Fungi on casings and in the air in mushroom farms
Peziza ostracoderma has been found on rockwool used for mushroom
production. On peat and/or paper casings with mushrooms the following
species have been found: Ac. murorum, A. fumigatus, A. niger, C. globosum,
Chrysonilia sitophila, P. ostracoderma, S. chartarum, Trichophaea abundans,
and T. viride (Table 3). Acremonium spp., A. fumigatus, A. niger, Chr. fulvum,
Cladosporium herbarum, T. harzianum, and T. viride have also been found in
black areas of spent mushroom compost (Fergus, 1978; Milenkovic et al.,
2000).
In a mushroom farm, concentrations of airborne fungi have been mea-
sured using stationary samplers during different work activities. During
mushroom picking, P. ostracoderma has been found in a concentration
of 103 CFU/m3 while A. fumigatus has been found in concentrations of
100 to 103 CFU/m3, and Trichoderma spp. in concentrations of 300 to
103 CFU/m3 (Crook and Lacey, 1991). Aspergillus fumigatus was found in
the air during spawning of mushrooms (2 × 104 CFU/m3) and disposal
of compost (105 CFU/m3) from mushrooms (Crook and Lacey, 1991).
Peziza has also been found in the air during preparation and use of com-
post for growing mushrooms (~500 CFU/m3) (Lacey et al., 1996)
(Table 5). In most studies the fungi have been identified by microscopy
by their morphology post cultivation on agar (Tables 2–5).
In a mushroom farm, 13 airborne fungal genera were found, but the
genera Acremorium, Peziza, and Trichoderma were not found; in the
study the fungi were identified to genus level based on their morphol-
ogy (Tarigan et al., 2017). An overview of fungal species on surfaces of
casing media and whether they have also been found in the air in mush-
room farms can be found in Fig. 1.
3.3. Fungi in other environments
The following species, in contrast to the other species in Tables 2–5,
are expected to be less commonly found in other occupational settings:
At. turficola, Cr. corticale, P. ostracoderma, Sp. schenckii and L. aphanocladii.
We reviewed the literature, to see whether people are potentially ex-
posed to these species in other environments. Of these fungi, only Peziza,
Sp. schenckii, and Cr. corticale were found in other settings (Table 6).
3.4. Health effects of exposure
Reported cases of health effects caused directly by species from pots
and growing and casing media are presented in Table 7. Peziza
ostracoderma has been identified as the causative agent of extrinsic hy-
persensitivity pneumonitis (also called extrinsic allergic alveolitis and in
the following called HP) among carnation cutting workers, and the
Health effects search Search term combinations
Asthma Greenhouse-occupational exposure-bioaerosols
Allergy Greenhouse-occupational exposure-fungi
Allergic alveolitis Greenhouse-plant-fungi-exposure-occupational
Occupational asthma Mushroom-occupational exposure- bioaerosols
Hypersensitivity pneumonitis Mushroom-occupational exposure- fungal exposure
ODTS (Organic Dust Toxic Syndrome)
Dermatitis
Onychomycosis
3
A.M. Madsen and B. Crook Science of the Total Environment 788 (2021) 147832

Table 2
Fungi found on surfaces of growing media and paper pots in greenhouses.

Fungus Environments Sampling identification Reference

Atheliaceae
Athelia turficola On peat growing medium, Germany Nm (Alsanius and Wohanka, 2019)
Athelia turficola On the surface of peat based growing media, Germany Nm, cultivation+morphology (Schlechte and Hoffmann, 2000)

Chaetomiaceae
Chaetomium globosum On surfaces of recyclable paper pots with ornamental plants, Nm, cultivation+morphology (Dill et al., 1997)
Germany
Chaetomium globosum On non-specified plant growing medium, Germany Nm (Alsanius and Wohanka, 2019)

Cordycipitaceae
Lecanicillium On rockwool blocks with cannabis cuttings, Canada Material samples, cultivation+morphology (Punja, 2020)
aphanocladiia

Davidiellaceae
Cladosporium On reused rockwool slabs for tomato plant growth, Poland Cork borer, cultivation, nm (Ślusarski and Smolińska, 2010)
sphaerospermum
Cladosporium sp.a On sandy loam soil covered with perlite, wheat plants in pots in Material, sequencing (Latz et al., 2020)
greenhouses, Denmark

Dothioraceae
Aureobasidium pullulansa On sandy loam soil covered with perlite, wheat plants in pots in Material, sequencing (Latz et al., 2020)
greenhouses, Denmark

Hypocreaceae
Acremonium charticola On reused rockwool slabs for tomato plant growth, Poland Cork borer, cultivation, nm (Ślusarski and Smolińska, 2010)
Acremonium curvulum On sandy loam soil covered with perlite, wheat plants in pots in Material, sequencing (Latz et al., 2020)
greenhouses, Denmark
Acremonium persicinum On sandy loam soil covered with perlite, wheat plants in pots in Material, sequencing (Latz et al., 2020)
greenhouses, Denmark
Acremonium rutilum On sandy loam soil covered with perlite, wheat plants in pots in Material, sequencing (Latz et al., 2020)
greenhouses, Denmark
a
Acremonium spp. On surfaces of recyclable paper pots, Germany Surface sample, cultivation+morphology (Dill et al., 1997)
Trichoderma harzianum On reused rockwool slabs for tomato plant growth, Poland Cork borer, cultivation, nm (Ślusarski and Smolińska, 2010)
Trichoderma harzianum On coco fibre substrates in hydroponic cultivation of cannabis Material, cultivation+morphology (Punja et al., 2019)
plants, Canada
Trichoderma viride On wood bark chips (Douglas fir and Red wood bark) in an Chips samples, cultivation, nm (Shepherd et al., 1989)
orchid greenhouse with 1200 plants, USA
Trichoderma viride On reused rockwool slabs for tomato plants, Poland Cork borer, cultivation, nm (Ślusarski and Smolińska, 2010)
Trichoderma sp. On surfaces of recyclable paper pots with plants, Germany Surface sample, cultivation+morphology (Dill et al., 1997)
Trichoderma sp. On sandy loam soil covered with perlite, wheat plants in pots in Material, sequencing (Latz et al., 2020)
greenhouses, Denmark

Ophiostomataceae
Sporothrix schenckii On sphagnum moss with tree seedlings and from sphagnum Cultivation of dilutions of sphagnum moss (D'alessio et al., 1965)
moss piles, USA
Sporothrix schenckiid On sphagnum moss for tree seedlings, USA From a particular batch of sphagnum moss, (Powell et al., 1978)
cultivation+ morphology
Sporothrix schenckii On sphagnum moss for tree seedlings, USA Nm (Control, 1988)
Sporothrix schenckii On sphagnum moss for topiaries and plants, USA From sphagnum moss samples, cultivation and (Hajjeh et al., 1997)
DNA typing

Pezizaceae
Peziza cerea On a wooden box and the soil in the box, with tulip bulbs, Czech Sample, morphology (Rod, 1981)
Republic
Peziza domiciliana On surfaces in greenhouses, USA Nm, morphology (Seaver, 1916)
Chromelosporium fulvum On and in peat cubes with cabbage seedlings, USA Nm (Kilpatrick, 1977)
(Peziza ostracoderma)b
Chromelosporium fulvum On peat and vermiculite with pepper seedlings, China Nm, cultivation+morphology (Jin et al., 2008)
(Peziza ostracoderma)b
Chromelosporium fulvum On sterilized soil and vermiculite in pots in greenhouses, Iran Nm, cultivation+morphology (Jamali and Banihashemi, 2011)
Chromelosporium fulvum On the surface peat with Saintpaulia and on leaf debris on the Microscopy of peat surface and sample of leaf (Stępniewska-Jarosz et al., 2020)
(Peziza ostracoderma)b peat, Poland debris, cultivation+morphology
Chromelosporium ollare On peat on steam-sterilized soil and on paper pots in Nm, cultivation+morphology (Hennebert and Korf, 1975)
(Peziza ostracoderma)b greenhouses; Europe
Chromelosporium ollare On peat surfaces, carnation, greenhouses, Poland Nm, morphology (Pudełko, 2014)
(Peziza ostracoderma)b
Peziza atrovinosa On bark growing media in greenhouses with cucumber, Czech Sample, morphology (Rod, 1981)
Republic
Peziza ostracoderma On sterilized soil with peat-perlite mixture in clay pots, USA Material, cultivation+ morphology (Fergus, 1960)
Peziza ostracoderma Washed sand with peat, bentgrass; USA Nm (Shepard, 1978)
Peziza ostracoderma Washed sand with soybean chop, bentgrass, USA Nm (Shepard, 1978)
Peziza ostracoderma On perlite peat mixture, carnation cuttings, France Material, cultivation+ morphology (Guillot et al., 1988)
Peziza ostracoderma On rockwool blocks with seedlings, Germany Nm (Alsanius and Wohanka, 2019)
Peziza ostracodermaa On rockwool blocks used to root cannabis cuttings, Canada Material, sequencing (Punja, 2020)
Peziza vesiculosa On a wooden box and on the soil in the box, with tulip bulbs, Sample, morphology (Rod, 1981)
Czech Republic
Peziza vesiculosa On the border between straw and soil in a bed with cucumber Sample, morphology (Rod, 1981)
and lettuce, greenhouses, Czech Republic

4
A.M. Madsen and B. Crook
Table 2 (continued)
Fungus Environments
Plicaria fulva (Now: On steamed sphagnum (75%) with soil (25%), in a tomato plant Nm
Peziza ostracoderma)c bed in a greenhouse, Norway
Stachybotryaceae
Stachybotrys chartaruma On surfaces of recyclable paper pots with plants, Germany
Stachybotrys chartarum On reused rockwool slabs for tomato plant growth, Poland
Trichocomaceae
Aspergillus fumigatusa,d Surface of the peat, ornamental plants, Germany
Aspergillus fumigatus Orchid growing medium, Japan
Aspergillus nigera,d Surface of the peat, ornamental plants, Germany
Aspergillus niger On surfaces of rockwool with roses, Japan
Aspergillus niger Surfaces of soil and leaves, roses, Japan
Aspergillus niger On coco fibre substrates in hydroponic cultivation of cannabis
plants, Canada
Xylariaceae
Cryptostroma corticale On wood bark chips (Douglas fir and Red wood bark) in an
orchid greenhouse with 1200 plants, USA
a
Also found in the air in the same study.
b
Both names used in the paper.
c
Now called: P. ostracoderma; Nm = not mentioned.
d
Classified in risk class 2.
workers had precipitins against P. ostracoderma. It has been mentioned
that Plicaria fulva (P. ostracoderma) may be dangerous for exposed
mushroom workers (Van Der Vliet, 1960), but what this suggestion is
based on, is not mentioned. Another species in another environment,
P. domiciliana, has been identified as the causative agent of HP, and
also here the patient had serum precipitins against this fungus. The per-
son was exposed in the home from growth of the fungus in the crevices
of the basement floor walls, and the fungus was found in the air in the
basement (2250 CFU/m3) and the kitchen (2750 CFU/m3) (Wright
et al., 1999). Peziza vesiculosa (identified by sequencing) has been
found in higher concentrations in the airways of people with asthma
than in reference subjects (van Woerden et al., 2013), but it was not
studied whether it was involved in the development of the asthma.
A case of painful inflammation of the fingertips and scaling off of the
skin among greenhouse workers exposed to S. chartarum has been
reported. Stachybotrys chartarum was growing on decomposable plant-
pots made of recycling paper. Several cases of skin infection with Sp.
schenckii from peat has been published – all from the USA (Table 7),
and time from first exposure to the fungus onset was between 10 and
54 days (D'alessio et al., 1965). Also several cases of skin infection with
Sp. schenckii are reported from Japan among horticulture workers, but
the source of exposure is not identified (Kusuhara et al., 1988).
Aspergillus fumigatus has in two studies been identified as the caus-
ative agent of occupational HP; in both studies it grew on a growing
or a casing medium but the type of medium was not described
(Table 7). Other greenhouse workers developed HP after exposure to
A. fumigatus from straw present on the floor (Yoshida et al., 1993).
Weak positive reactions have been obtained when A. fumigatus antigens
were tested against mushroom workers' antiserum (Kleyn et al., 1981).
Aspergillus fumigatus has also caused allergic bronchopulmonary asper-
gillosis in garden waste collectors (Poole and Wong, 2013) and other al-
lergic airways diseases (Chaudhary and Marr, 2011). Exposure to Cr.
corticale from a bark chips growing medium has caused HP of orchid
grower (Table 7), and a shiitake mushroom grower had precipitating
antibodies towards this fungus – the mushrooms were grown on oak
wood logs (Matsui et al., 1992).
Aspergillus niger has been identified as a causative agent of cases of
HP among greenhouse workers growing roses, where it was found on
leaves and on the soil or on rockwool (Table 7), and among onion
farmers, where it was found on the onion peels (Sakamoto et al., 2018).
Childhood HP has been reported to be caused by exposure to the
yeast-like fungus Au. pullulans in a home where it was present in indoor
hydroponics. The child had serum precipitating antibodies against Au.
5
Science of the Total Environment 788 (2021) 147832
Sampling identification Reference
(Roll-Hansen, 1961)
Cultivation+morphology (Dill et al., 1997)
Cork borer, cultivation, nm (Ślusarski and Smolińska, 2010)
Sterile spoon, cultivation+morphology (Staib et al., 1978)
Nm (Kawaji et al., 1996)
Sterile spoon, cultivation+morphology (Staib et al., 1978)
Nm (Miyazaki et al., 2004)
Nm (Hamaguchi et al., 2009)
Material, cultivation+morphology (Punja et al., 2019)
Chips samples, cultivation, nm (Shepherd et al., 1989)
pullulans. The fungus was cultivated and identified based on morphol-
ogy (Table 7).
Trichoderma viride, C. globosum, and Ac. strictum have caused HP, and
the authors suggest that this may have been caused by exposure from
house plants in the home (Table 7). For the other fungal species found
associated with paper pots and surfaces of growing and casing media
we have found no reports on health effects.
4. Discussion and perspectives
Peziza ostracoderma has gained attention because of its visible
growth on paper pots and growing media, and in cultivation guides
for production of plants (e.g. Klasmann-Deilmann, 2020; Toppe and
Herrero, 2005) and mushrooms (Sharma et al., 2007) it is described as
a problem which is of increasing concern (Lohr et al., 2017b). It is also
mentioned that Plicaria fulva (now P. ostracoderma) may be dangerous
for mushroom workers (Van Der Vliet, 1960), and spores of
Oedocephalum glomerulosum (now Pyronema omphalodes) and Chr.
fulvum on paper pulp is a possible health hazard to mushroom workers
(Eicker and van Greuning, 1989). In this review we investigated
whether there is documented evidence of occupational exposure to
fungi growing on recyclable paper pots and growing and casing media
such as rockwool, perlite, vermiculite, coco fibre, and peat, and also
any documented evidence exposure-associated health effects.
This review shows that P. ostracoderma has been found on paper
pots, peat and paper casing for mushrooms, and on peat, sterilized
soil, and vermiculite, and rockwool blocks for plants. Overall, published
research shows that workers' hands and airways can be exposed to this
fungus. However, the documentation of exposure via the air is very lim-
ited as we have only found one greenhouse study where Peziza was
found in the air and the concentration was not measured. In mushroom
farms, P. ostracoderma or Peziza sp. has been found in the air in two stud-
ies, and the concentrations were up to 1000 CFU/m3 (Table 5). This con-
centration can be considered as high for a single species and as
compared to the general outdoor concentration of fungi. It is therefore
relevant to further characterize the personal work task-related expo-
sure to P. ostracoderma. It is also relevant to obtain knowledge about
the potential deposition of these fungi in the airways during work in
greenhouses and mushroom farms. Few studies show that
P. ostracoderma is also found in other environments than greenhouses
and mushroom farms (Table 6).
As long ago as 1960, Plicaria fulva (now P. ostracoderma) had been
suspected to cause health problems for people working with cultivation
A.M. Madsen and B. Crook Science of the Total Environment 788 (2021) 147832

Table 3
Fungi in the air of greenhouses.

Fungus Concentration Environments Sampling identification Reference

Chaetomiaceae
Chaetomium Nm In vegetable greenhouses, Italy Open Petri dish, cultivation+morphology (Cosentino and Palmas, 1991)
globosum

Cordycipitaceae
Lecanicillium Nm In a propagation room with cannabis in rockwool Open Petri dishes, cultivation+morphology (Punja, 2020)
aphanocladiia blocks, Canada

Davidiellaceae
Cladosporium 0.17–0.66 CFU In greenhouses in a botanical garden, Italy Open Petri dish, cultivation+morphology (Rodolfi et al., 2003)
sphaerospermum settledd
Cladosporium sp.a In 10 of 24 samples In greenhouses with wheat plants in soil with GSPb, sequencing (Latz et al., 2020)
perlite in pots, Denmark

Dothioraceae
Aureobasidium 0.25–3.3 CFU settled In greenhouses in a botanical garden, Italy Open Petri dish, cultivation+morphology (Rodolfi et al., 2003)
pullulans
Aureobasidium In 8 of 24 samples In greenhouses with wheat plants in soil with GSP, sequencing (Latz et al., 2020)
pullulansa perlite in pots, Denmark

Hypocreaceae
Acremonium In 1 of 24 samples In greenhouses with wheat plants in soil with GSP, sequencing (Latz et al., 2020)
persicinuma perlite in pots, Denmark
Acremonium sp.a Nm Greenhouse workers handling plants in pots made Spore-fall collector, microscopy (Dill et al., 1997)
of recycling paper, Germany
Acremonium spp. 0.3–6.6 CFU settled Greenhouses in a botanical garden, Italy Open Petri dish, cultivation+morphology (Rodolfi et al., 2003)
Acremonium sp. Nm A greenhouse with Gnetum, Russia Open Petri dishes, cultivation+morphology (Bogdanova et al., 2019)
Acremonium sp. 1240–4290 CFU/m3 Cucumber greenhouses, Denmark GSP personal air sampler, cultivation (Madsen et al., 2020)
NGS top 10 +MALDI-TOF MSc and sequencing
Acremonium sp. In 11 of 24 samples In greenhouses with wheat plants in soil with Perlite GSP, sequencing (Latz et al., 2020)
in pots, Denmark
Trichoderma viride 0.33–2.0 CFU settled In greenhouses in a botanical garden, Italy Open Petri dish, cultivation+morphology (Rodolfi et al., 2003)

Pezizaceae
Peziza Nm In a cannabis propagation room, Canada Open Petri dishes, cultivation, sequencing (Punja, 2020)
ostracodermaa

Stachybotryaceae
Stachybotrys 100–7500 spores/m3 Greenhouse workers handling plants in pots made Spore fall collector, microscopy (Dill et al., 1997)
chartaruma of recycling paper, Germany
Stachybotrys Nm In a greenhouse with Gnetum, Russia Open Petri dishes, cultivation+morphology (Bogdanova et al., 2019)
chartarum

Trichocomaceae
Aspergillus Nm Above dry peat in pots with cactus plants exposed to Open Petri dish, cultivation+morphology (Staib et al., 1978)
fumigatusa an air stream, Germany
Aspergillus 0.3–6.6 CFU settled In a greenhouses in a botanical garden, Italy Open Petri dish, cultivation+morphology (Rodolfi et al., 2003)
fumigatus
3
Aspergillus Max 88 CFU/m In tomato greenhouses, Denmark GSP personal air sampler, cultivation (Hansen et al., 2010)
fumigatus +morphology
Aspergillus Max 80 CFU/m3 Poinsettia greenhouses, Denmark GSP personal air sampler, cultivation (Hansen et al., 2012)
fumigatus +morphology
Aspergillus 70 CFU/m3 Cucumber greenhouses, Denmark GSP personal air sampler, cultivation (Madsen et al., 2020)
fumigatus +MALDI-TOF MS
Aspergillus nigera Nm Above dry peat in pots with Clivia plants, exposed to Open Petri dish, cultivation+morphology (Staib et al., 1978)
an air stream, Germany
Aspergillus niger 1.2 CFU/m3 In vegetable greenhouses, Italy Surface Air System, cultivation+morphology (Cosentino and Palmas, 1991)
Aspergillus niger Nm In a greenhouse with Gnetum, Russia Open Petri Dish cultivation+morphology (Bogdanova et al., 2019)
Aspergillus niger 0.3–27 CFU In greenhouses in a botanical garden, Italy Open Petri dish, cultivation+morphology (Rodolfi et al., 2003)
sedimented
Aspergillus niger 100 CFU sedimented In rose greenhouses, Japan Open Petri dish, cultivation+morphology (Miyazaki et al., 2004)
a
Also found in the same study on surfaces of pots or growing media.
b
Samples inhalable particles, and are used as personal or stationary samplers.
c
Matrix-assisted laser desorption ionization time-of-flight mass spectrometry.
d
Sampled by passive sedimentation. CFU = Colony Forming Units, NGS = Next-generation sequencing, Nm = Not mentioned.

of mushrooms (Van Der Vliet, 1960). Cases of HP among mushroom
workers have been reported repeatedly, but it has not been studied
whether these workers were exposed to Peziza nor how they react
upon exposure to this fungus. Antibody testing has been performed to
determine whether exposed workers reacted to the mushrooms being
cultivated (Cox et al., 1988; Kamm et al., 1991), or to typical mushroom
compost microbial components including A. glaucus (Yoshida et al.,
1990), and thermophilic actinobacteria (Van den Bogart et al., 1993).
When it comes to working in greenhouses, 3 cases of HP have been
documented among people working with carnation cuttings caused by
P. ostracoderma (Table 7). Lohr et al. mention that Peziza can cause aller-
gies but do not document this (Lohr et al., 2017a). Another Peziza spe-
cies in another environment, P. domiciliana, has been identified as the
causative agent of HP of an occupant (Wright et al., 1999). Based on
these cases, the general respiratory problems reported among green-
house (Zuskin et al., 1993) and mushroom (Hayes and Rooney, 2014)
workers, the frequent presence of Peziza spp. on different types of grow-
ing and casing media, the weaker documented presence of Peziza spp.

6
A.M. Madsen and B. Crook Science of the Total Environment 788 (2021) 147832

Fungus Peat Peat or soil, Rockwool Paper Coco, Fibre Non Air Health Health in
with perlite wood, with specified other
or or bark peat, or other environ-
vermiculite bark or media ments
pumice
Acremonium charcola
Acremonium curvulum
Acremonium murorum
Acremonium persicinum
Acremonium rulum
Acremonium spp.
Aspergillus fumigatus
Aspergillus niger
Athelia turficola
Aureobasidium pullulans
Chaetomium globosum 2)

Chrysonilia sitophiIa
Cladosporium
sphaerospermum
Cladosporium sp.
Cryptostroma corcale
Lecanicillium
aphanocladii
Peziza cerea
Peziza domiciliana
Peziza ostracoderma 1)
Peziza vesiculosa
Pyronema omphalodes
Sporothrix schenckii
Stachybotrys chartarum
Trichoderma harzianum
Trichoderma viride 2)

Trichoderma sp.
Trichophaea abundans

Fig. 1. Overview of fungal species found on surfaces of paper pots and different growing media for plants or casing media for mushrooms and in the air, and whether hypersensitivity
pneumonitis or skin irritation or skin or nail infection are reported from fungal growth on these pots or media or in other occupational settings. 1) In the papers we cite, this species is
also called Chr. fulvum, Chr. ollare, P. atrovinosa, and P. ostracoderma. 2) A mixture of the two fungi and Ac. strictum.

on paper pots combined with the wish of substituting plastic pots with
paper pots, we suggest that the potential health effects of the Peziza spe-
cies present in these environments should be studied further.
Chaetomium globosum has been found on paper pots and peat and
compost casing for mushrooms. Laboratory experiments with biodegra-
dation of pots show that C. globosum grows very well on pots made of
recycled paper and wheat bran (Sandak et al., 2019). Only a single
study has found this fungus in the air in greenhouses and its concentra-
tion was not measured (Table 3), but it is common in the indoor home
environment (Ayanbimpe et al., 2010), where it has also gained atten-
tion because some isolates produce the cytotoxic mycotoxins
chaetoglobosins A and C (Fogle et al., 2007), and fungal particles can
be released from colonized materials when exposed to an airflow
(Madsen et al., 2015a). In addition, it has been found on wheat leaves
in a greenhouse (Latz et al., 2020) as well as on other leaves
(Cosentino and Palmas, 1991). In the normal population, allergy to-
wards C. globosum has been reported (Beezhold et al., 2008) and it has
caused onychomycosis (Aspiroz et al., 2007), but we have found no re-
ports on occupational health problems related to this fungus. In con-
trast, it is tested for its use as a biopesticide in greenhouses.
Trichoderma viride was found in greenhouses on peat, paper, coco
fibre, and rockwool, and in relatively high concentrations in the air
(Tables 2–5), and it has also been found in hydroponics in the indoor
home environment (Engelhart et al., 2009). Trichoderma viride and
T. harzianum are more or less common in the indoor home environment
(Beezhold et al., 2008) and in occupational settings and are used as bio-
pesticides in greenhouses (Madsen, 2011). In the normal population, al-
lergy towards T. viride has been reported (Beezhold et al., 2008).
Trichoderma viride from ultrasonic humidifiers has caused HP in an ex-
posed person (Enríquez-Matas et al., 2007) and, as shown in Table 7,
it is also described as a causative agent of HP in the home environment,
with ornamental plants presumed to be the source of fungal exposure.
In a study involving 389 patients with suspected respiratory allergy,
positive skin reactions to T. viride was observed in 27% of the patients
(Das and Gupta-Bhattacharya, 2010). It would therefore be relevant to
obtain more knowledge about occupational exposure related health ef-
fects of the two Trichoderma species.
Stachybotrys chartarum was found on peat and paper casing, paper
pots, and rockwool for plants and, in a single study, also in high concen-
trations in the air during work. This fungus grows well on cellulose-
containing compounds and can be present on walls and in air in damp
buildings (Johanning et al., 1996). Since S. chartarum on decomposable
plant-pots has caused painful inflammation of the fingertips among
greenhouse workers (Table 7), and has caused several human diseases
in other environments including dermatitis and HP (Kuhn and
Ghannoum, 2003), and allergy (Beezhold et al., 2008), it is relevant to

7
A.M. Madsen and B. Crook Science of the Total Environment 788 (2021) 147832

Table 4
Fungi found on surfaces of beds and casing media in mushroom farms.

Fungus Environments Sampling identification Reference

Chaetomiaceae
Oedochephalum globosum (now Chaetomium On peat and paper casing, South Africa Nm, cultivation+morphology (Eicker and van Greuning, 1989)
globosum)

Hypocreaceae
Acremonium murorum On paper casinga, South Africa Nm, cultivation+morphology (Eicker and van Greuning, 1989)
Trichoderma viride On casing soil, Netherland Nm (Van Der Vliet, 1960)
Trichoderma viride On peat and paper casing, South Africa Cultivation+morphology (Eicker and van Greuning, 1989)

Pezizaceae
Chromelosporium fulvum On paper casing, South Africa Nm, cultivation+morphology (Eicker and van Greuning, 1989)
Chromelosporium ollare (Peziza ostracoderma)a Mushroom beds in farms, South Africa Nm, cultivation+morphology (Coetzee, 1983)
Chromelosporium On peat casing, South Africa Sample, CFU + sequencing (Siyoum et al., 2016)
Peziza domiciliana Mushroom graves on surfaces, USA Nm, morphology (Seaver, 1916)
Plicaria fulva (now Peziza ostracoderma) On casing soil, Netherland Nm (Van Der Vliet, 1960)
Peziza ostracoderma On fibre-mixb with peat, bark, or pumice soil casing, Visually (Rainey, 1985)
New Zeeland
Peziza ostracoderma On peat casing with chalk, UK Visually (Richardson, 1991)

Pyronemataceae
Oedocephalum glomerulosum (now Pyronema On peat and paper casing, South Africa Nm, cultivation+morphology (Eicker and van Greuning, 1989)
omphalodes)
Trichophaea abundans On pasteurized peat, South Africa Nm, cultivation+morphology (Coetzee and Eicker, 1994)

Sordariaceae
Chrysonilia sitophiIa On peat and paper casing, South Africa Nm, cultivation+morphology (Eicker and van Greuning, 1989)

Stachybotryaceae
Stachybotrys atra (now Stachybotrys chartarum) On paper casing, South Africa Cultivation+morphology (Eicker and van Greuning, 1989)

Trichocomaceae
Aspergillus fumigatusc On unspecified casing, USA Casing sample, cultivation (Kleyn et al., 1981)
+morphology
Aspergillus fumigatus On peat and paper casing, South Africa Nm, cultivation+morphology (Eicker and van Greuning, 1989)
Aspergillus nigerc On peat and paper casing, South Africa Nm, cultivation+morphology (Eicker and van Greuning, 1989)
a
Both names are used in the same study.
b
A by-product of a process involving the extraction of poly-phenolic resins from the bark of Pinus radiate.
c
Classified in risk class 2. CFU=Colony Forming Units, Nm = not mentioned.

obtain knowledge about how universally this fungus grows and sporu-
lates on growing media and paper pots and whether it produces myco-
toxins on these media.
Two Aspergillus species, A. niger and A. fumigatus, have been found on
peat, rockwool, coco fibre, orchid growing medium, and hydroponics for
plants, and on peat and paper casing with mushrooms. The two species
have also been found in the air. Aspergillus niger has previously been
found on leaves in greenhouses (Cosentino and Palmas, 1991) and
both species have also been found as airborne fungi in other working
environments where organic material is handled as e.g. biofuel plants
(Madsen, 2006), sawmills (Land et al., 1987), and seed treating plants
(Madsen et al., 2015b). Of all the fungal species found, only
A. fumigatus is classified as a potential human pathogen according to
the directive on the protection of workers from risks related to exposure
to biological agents at work (89/391/EEC, 2000). However, this directive
does not consider the cytotoxic and inflammatory potential of microor-
ganisms. Two reports on HP caused by A. fumigatus related to growing
and casing media have been reported (Table 7), and it has also caused
HP in many other environments (Lacey and Crook, 1988). In addition,
A. fumigatus has been identified as the causative agent of allergic
bronchopulmonary aspergillosis among greenhouse workers exposed
to the fungus from straw present on the floor (Yoshida et al., 1993).
This fungus has also been identified as the causative agent of allergic
bronchopulmonary aspergillosis among garden waste collectors
(Poole and Wong, 2013), a vegetable compost plant worker (Vincken
and Roels, 1984), and occupants of a home where it grew on decayed
wood (Bryant and Rogers, 1991). It has also caused pneumonia of
workers in a mushroom factory where it was present in dust on the
floor (Shimaoka et al., 2006). Since it can be infectious it is important
to be aware of that fungicide resistance isolates of this species are

Table 5
Fungal speciesa found in the air of mushroom farms.

Fungus Concentration Environments Sampling identification Reference

Hypocreaceae
Trichoderma viride 100–1000 CFU/m3 In mushroom farms during work, UK Andersen sampler, cultivation, nm (Crook and Lacey, 1991)
Trichoderma sp. ~200–300 CFU/m3 During preparation of compost, UK Andersen sampler, cultivation, nm (Lacey et al., 1996)

Pezizaceae
Peziza ostracoderma 1000 CFU/m3 In mushroom farms during work, UK Andersen sampler, cultivation, nm (Crook and Lacey, 1991)
Peziza sp. 100–1000 CFU/m3 During preparation of compost, UK Andersen sampler, cultivation, nm (Lacey et al., 1996)

Trichocomaceae
Aspergillus fumigatus Nm Mushroom production, UK Air sampling, nm (Lacey, 1974)
Aspergillus fumigatus 100–105 CFU/m3 In mushroom farms during work, UK Andersen sampler, cultivation, nm (Crook and Lacey, 1991)
Aspergillus fumigatus 1000–106 CFU/m3 During preparation of compost, UK Andersen sampler, cultivation, nm (Lacey et al., 1996)
a
Only species which are also found on casing media. NM = not mentioned, CFU = colony forming units.

8
A.M. Madsen and B. Crook Science of the Total Environment 788 (2021) 147832

Table 6
Other environments where Sporothrix schenckii, Peziza (Chromelosporium), and Cryptostroma corticale are found.

Fungus Environments Sampling identification method Reference

Ophiostomataceae
Sporothrix schenckii Soil adhering to fragments of wood, Israel Soil samples, cultivation, morphology (Feuerman et al., 1976)
Sporothrix schenckii On surfaces of edible mushrooms from China, Taiwan, Extracted from the surfaces of the mushroom, cultivation, (Kazanas and Jackson, 1983)
and Thailand morphology and antisera test
Sporothrix schenckii On hay, Australia Hay sample, cultivation, morphology, DNA (Feeney et al., 2007)
Sporothrix schenckii Air in chicken farm Andersen sampler, cultivation, morphology (Wang et al., 2007)
Sporothrix schenckii Hospital and home surfaces, Brazil Adhesive tape, surfaces, cultivation, morphology (Mattei et al., 2011)
Sporothrix schenckii Indoor air, hospital, Iran Open Petri dish, morphology (Sepahvand et al., 2013)
Sporothrix schenckii Indoor air, university, Nigeria Open Petri dish, morphology (Shittu et al., 2019)

Pezizaceae
Chromelosporium Ancient laid-paper; Portugal Scratching, cultivation+ sequencing (Mesquita et al., 2009)
carneum
Chromelosporium Air in turkey confinement brooder house; USA Filter sampling, cultivation, (Pinello et al., 1977)
fulva Nm
Chromelosporium In air in homes; Belgium Reuter centrifugal air sampler, cultivation, nm (Beguin and Nolard, 1994)
fulvum
Chromelosporium In household waste; Sweden Waste sample, cultivation+morphology (Schnürer and Schnürer, 2006)
fulvum
Chromelosporium Outdoor air in the city; Greece Air sampler, cultivation, nm (Pyrri and Kapsanaki-Gotsi, 2015)
Chromelosporium On building partitions; Poland Surfaces sampling, (Piontek et al., 2017)
sp. cultivation+ morphology
Peziza Surfaces of ancient maps in museums; Italy Swabs, cultivation+morphology (Corte et al., 2003)
ostracoderma
Peziza Outdoor air in areas with greenhouses; Portugal Tape sampling of spores, microscopy (Oliveira et al., 2009)
Peziza Outdoor air; Nigeria Pollen sampler, microscopy (Njokuocha et al., 2019)
Peziza Wastewater; South Africa Water sample, sequencing (Assress et al., 2019)
Peziza Bed dust; Denmark Vacuum cleaning, NGS (Sørensen et al., 2020)

Xylariaceae
Cryptostroma In the air in a sawmill, USA Air samples and samples of face masks, microscopy (Wenzel et al., 1967)
corticale
Cryptostroma On trees in forests, in many countries e.g. Czech Cores of wood, PCR (Cochard and Lefort, 2016;
corticale Republic and Switzerland Kelnarová et al., 2017)

NGS=Next-generation sequencing.

found in soil (Fraaije et al., 2020) as well as in clinical settings (Garcia-
Rubio et al., 2020). Furthermore, A. fumigatus can produce the myco-
toxin gliotoxin on wood materials (Nieminen et al., 2002), and it
seems to enable it to persist in the respiratory tract and in lung infec-
tions (Bruns et al., 2010). Aspergillus niger has been identified twice as
a causative agent of HP in greenhouse workers growing roses
(Table 7) and also in onion farmers (Sakamoto et al., 2018). As green-
house workers are handling plants with their hands, it is also worth not-
ing that A. niger has caused occupational nail infections in e.g. workers at
a vegetable market reviewed in (Bongomin et al., 2018), and fungicide
resistance has been found in environmental isolates (Poulsen et al.,
2021). Furthermore, A. niger can produce the mycotoxin fumonisin B2
(Nielsen et al., 2009), but whether it is produced on the growing and
casing media is not known. Due to the potential health effects, it is rel-
evant to pay attention to growers' exposure levels to A. fumigatus and
A. niger.
Chrysonilia sitophila, which was found on paper and peat casing, has
been found in the air in sawmills (Klaric et al., 2012) and indoor air
(Salonen et al., 2007). We have found no cases of health effects of this
fungus related to work with mushrooms, but it has caused occupational
asthma in a person working as a coffee dispenser operator (Francuz
et al., 2010) and a person working in the logging industry (Tarlo et al.,
1996), and HP among several cork workers (Winck et al., 2004). This
species seems not to produce mycotoxins (Barreto et al., 2011).
Cladosporium sphaerospermum and Cladosporium sp. were found in
one study each and have caused HP from growth on wallpaper in a bed-
room (Marin et al., 2009) and in a greenhouse worker (the source of
exposure was not mentioned) (Abreu et al., 2020).
Athelia turficola was described in year 2000 as a new species growing
on horticultural growing substrates (Schlechte and Hoffmann, 2000),
and since then only a few papers have been published about this
species. Athelia turficola is the teleomorph of Burgoa turficola
(Diederich and Lawrey, 2007), and also with Burgoa turficola as the
search term we find no papers about this fungus which are relevant
for the present study.
Acremonium was found on paper pots and on different growing and
casing media. But, as in some studies it was only identified to genus
level, it is not possible to relate this to other studies about exposure
and potential health effects. Acremonium was also found as an airborne
fungus, and for cucumber greenhouse workers an exposure up to
4290 CFU Acremonium/m3 has been measured, and according to NGS
data it was among the top 10 most abundant fungi (Table 3). Therefore
it is relevant to illuminate whether this relatively high level will affect
workers' health. In the normal population, allergy towards Ac. strictum
has been reported (Beezhold et al., 2008), and Acremonium sp. has
caused onychomycosis (Tosti et al., 2000) and keratitis (Sahay et al.,
2020). In addition, Ac. strictum, T. viride, and C. globosum are reported
to have caused HP with peat in ornamental plants in a home as the
source of exposure (Table 7).
Aureobasidium pullulans was found on a growing medium with per-
lite and in the air in the same study. It has also been found on plastic
roofing of greenhouses (Durrell and Goldsberry, 1970). The species is
used as a post-harvest biopesticide and thus is expected to have been
through a safety evaluation. However, it has caused occupational HP
(Woodard et al., 1988) and childhood HP (Temprano et al., 2007) -
also related to exposure from hydroponics (Table 7), and a study of
105 asthmatic patients showed that sensitization to Au. pullulans was
a risk factor for severe asthma (Niedoszytko et al., 2007).
Cryptostroma corticale was found on a growing medium made of
bark chips, and it has caused HP of an orchid grower. The species is
known to cause HP among wood workers in paper mills (Emanuel
et al., 1962; Wenzel et al., 1967) where it was found in high

9
A.M. Madsen and B. Crook
Table 7
Occupational health effects caused by exposure to fungi on recyclable paper pots or growing or casing media.
Causative agent
Dothioraceae
Aureobasidium pullulans
Ophiostomataceae
Sporothrix schenckii
Sporothrix schenckii
Sporothrix schenckii
Sporothrix schenckii
Sporothrix schenckii
Sporothrix schenckii
Pezizaceae
Peziza ostracoderma
(Chromelosporium
fulvum)c
Stachybotryaceae
Stachybotrys chartarum
Trichocomaceae
Aspergillus fumigatus
Aspergillus fumigatus
Aspergillus niger
Aspergillus niger
Xylariaceae
Cryptostroma corticale
Mixture
Trichoderma viride,
Cephalosporium
acremonium (now
Acremonium strictum),
Aspergillus fumigatus
a
Isolated from the environment.
b
Hypersensitivity pneumonitis (HP) is also called extrinsic allergic alveolitis and is a group of lung diseases in which the lungs become inflamed as an allergic reaction resulting from
repeated exposure to bioaerosols. Mushroom workers' lung is a type of HP.
c
Both names are used in the same study. Nm = not mentioned. DLCO = diffusion lung capacity of carbon monoxide test.
Science of the Total Environment 788 (2021) 147832
Disease Population Patient tests Duration Isolationa Reference
Hypersensitivity Occupant, 14 years Precipitins against Medication for 13 weeks, Hydroponics with (Engelhart et al., 2009)
pneumonitisb old, Germany Au. pullulans, healthy after 6 months clay pebbles, Yucca
DLCO = 38% elephantipes
cultivation+
morphology
Sporotrichosis 14 pine seedling Physician diagnosed, Nm, but needs long Sphagnum moss, (D'alessio et al., 1965)
workers, USA and fungus isolated treatment cultivation
from skin lesions
Sporotrichosis 17 pine seedling Physician diagnosed, Nm Sphagnum moss, (Powell et al., 1978)
workers, USA and fungus isolated cultivation
from skin lesions morphology
Sporotrichosis Seedling and peat Physician diagnosed, Nm Sphagnum moss, nm (Control, 1988)
handlers, 84 cases, and fungus isolated
USA from skin lesions
Sporotrichosis 3 nursery workers, Physician diagnosed, Nm Sphagnum moss, (Hajjeh et al., 1997)
topiary production, and fungus isolated cultivation and
USA from skin lesions molecular typing
Sporotrichosis 9 of 65 nursery Physician diagnosed, Treated for 22 to 71 days Sphagnum moss, (Hajjeh et al., 1997)
workers, topiary and fungus isolated cultivation and
production, USA from skin lesions molecular typing
Sporotrichosis 154 cases of which Physician diagnosed, nm No (Vismer and Hull, 1997)
some were caused by and fungus isolated
exposure from soil, from skin lesions or
South Africa histopathology
Hypersensitivity Carnation cuttings, 3 Serum precipitins Attempted to resume work Sample of growth (Guillot et al., 1988)
pneumonitis greenhouse workers, against P. after 10 month another medium, cultivation
France ostracoderma, other patient after 5 years – but + morphology
tests symptoms reappeared,
1 resumed work after
1 year
Painful Greenhouse workers Fungi on fingers Symptoms disappeared Paper pot surfaces (Dill et al., 1997)
inflammation of handling plants in were not studied after workers used gloves cultivation+
the fingertips, pots made of morphology
followed by scaling recycling paper,
off of the skin Germany
Mushroom Mushroom farmers, Weak positive Nm From casing (Kleyn et al., 1981)
workers' lungb USA immunological
reactions towards A.
fumigatus antigens
Hypersensitivity 2 orchid greenhouse Precipitins against Stopped at the job From orchid culture (Kawaji et al., 1996)
pneumonitis workers, worked A. fumigatus, medium
with changing media, DLCO = 36%
Japan
Hypersensitivity Rose greenhouse Precipitins against On return to work, the From rockwool and (Miyazaki et al., 2004)
pneumonitis worker, Japan A. niger, inhalation symptoms reappeared in the air
provocation test,
hypoxemia, DLCO
14%
Hypersensitivity Rose greenhouse Serum precipitins, – From leaves, soil, (Hamaguchi et al., 2009)
pneumonitis worker, Japan DLCO = 62%, other and pillar
tests
Hypersensitivity Orchid greenhouse, Serum precipitins, 1 week hospitalized, after From a bark growing (Shepherd et al., 1989)
pneumonitis with plants in pots other tests 2 months returned to medium
with bark mix, peat greenhouse with face mask
and vermiculite, USA
Hypersensitivity Exposed to the three Precipitating Ill at least 4 months No (Velcovsky and
pneumonitis fungi from the peat antibodies in serum Graubner, 1981)
from houseplants, against the three
Germany fungi.
10
A.M. Madsen and B. Crook
concentrations in the air (Wenzel et al., 1967). The species seems only
to have been found on wood or wood bark.
Sporothrix schenckii has been found in sphagnum moss, on different
surfaces including edible mushrooms, and has caused skin infections in
many workers handling sphagnum (Table 7) and also for people han-
dling straw during farm or gardening work (Feeney et al., 2007) and
wood fragments with soil in a garden (Feuerman et al., 1976). None of
the skin infections related to handling of seedlings in moss sphagnum
or other horticulture work are from Europe. In fact most cases are
from the USA, and as highlighted in a review it is not possible to con-
clude whether it is because occupational infections have only occurred
in the USA (de Lima Barros et al., 2011), or lack of awareness on the
link between infections and occupation. Another issue is whether Sp.
schenckii can be found with the typically used methods and whether it
can airborne and spread by air. It is a thermally dimorphic fungus and
has been isolated using different commonly used media as corn meal
agar (Feuerman et al., 1976), yeast extract (D'alessio et al., 1965),
sabouraud dextrose agar (SDA) and mycobiotic agar (Kazanas and
Jackson, 1983). Few studies have found Sp. schenckii in air samples
(Table 6).
The fungal species, Ac. charticola, A. fumigatus, Au. pullulans,
C. globosum, and S. chartarum, found in the greenhouse and mushroom
farm environments, have all been found on ancient paper and artworks
(Melo et al., 2019; Mesquita et al., 2009; Sequeira et al., 2019; Zotti et al.,
2008), on humid wallpaper (Boutin-Forzano et al., 2004; Wang et al.,
2016), and in paper archives and libraries (Andres et al., 2015; Foladi
et al., 2013) which shows that there is an overlap in the species to
which workers are exposed in these very different occupational
settings.
We did not include Penicillium in this study even though it is found
in some studies. This is based on the evaluation that Penicillium was ab-
sent on surfaces in many studies (Dill et al., 1997; Staib et al., 1978), has
been found in spent compost but not on paper casing for mushrooms
(Eicker and van Greuning, 1989). Furthermore, if found it is not always
clear whether it in fact grew on the studied surfaces or just was present,
as this genus is always present in the air in greenhouses and grows on
e.g. senescent leaves (Cosentino and Palmas, 1991; Madsen et al.,
2020: Punja, 2020). We limited this study only to include fungi, but
we are aware that actinobacteria have caused health problems in mush-
rooms farms (Lacey and Crook, 1988; Van den Bogart et al., 1993). We
have also limited the study not to include the health problems associ-
ated directly with the exposure to peat (Sandstrom et al., 1991), vermic-
ulite (Sullivan, 2007), perlite (Maxim et al., 2014), and rockwool
(Hansen et al., 1999) as the published reports are from the production
rather than from the use of the media.
For isolation and identification of P. ostracoderma on growing and
casing media and Chr. carneum on paper, the agar medium PDA (potato
dextrose agar) has been used successfully (Coetzee, 1983; Jamali and
Banihashemi, 2011; Jin et al., 2008; Mesquita et al., 2009; Punja, 2020;
Stępniewska-Jarosz et al., 2020). For studies of exposure via the air,
other agar media such as DG18 (Madsen et al., 2020; Rodolfi et al.,
2003), Czapek Dox Agar (Bogdanova et al., 2019) and SDA (Rodolfi
et al., 2003) are typically used. Cladosporium, A. fumigatus, and A. niger
grow well on these media. For future air studies of exposure it
would be relevant in advance to determine whether Peziza can also
grow on a preferentially used agar medium. In most of the cited pa-
pers in this study, Peziza spp. was identified based on morphology.
Another possibility might be to use DNA sequencing. Using DNA
sequencing other Peziza species have been found: Peziza arvernensis
on leaves (Latz et al., 2020) and P. quelepidotia on the surface of
whiteflies in tomato greenhouses (Hong et al., 2017). However
using DNA sequencing, Peziza was often only identified to genus
level as e.g. in the rhizosphere of strawberry plants (Yang et al.,
2020), in bed dust (Sørensen et al., 2020), in forest soil (Bastida
et al., 2019; De Witte et al., 2017), and in wastewater (Assress
et al., 2019).
11
Science of the Total Environment 788 (2021) 147832
In greenhouse cultivation, reuse of growing media and plant pots is
strongly encouraged because the disposal of growing media at the end
of the growing season is a waste of resources and potential source of
contamination of the environment. Fungal growth during the reuse of
growing media, whether saprophytes as described above or plant path-
ogens, may reduce the quality of plant growth (Vandecasteele et al.,
2020), but whether it affects the working environment has not been
studied. Different attempts have been made to avoid or inhibit growth
of fungi on paper pots. Under experimental conditions, the fungicide
captan inhibited the growth of Chr. fulvum on paper in a nutrient solu-
tion with plant roots (Le Marié et al., 2014). In another study, cultivable
Sp. schenckii was isolated from topiaries, but not if the topiaries were
treated with fungicide (Hajjeh et al., 1997). In a study with cabbage
seedlings planted in peat cubes, P. ostracoderma colonized the surface
of the peat; and if treated with the fungicides captan and/or thiram
the growth was temporarily inhibited, but only on the surface of the
peat cubes (Kilpatrick, 1977). In a guideline for mushroom farmers,
the advice is to use chemical pesticides to control P. ostracoderma, C.
globosum, T. harzianum, and T. viride (Sharma et al., 2007). However,
the use of chemical fungicides on paper pots has a negative impact for
the environment and the working environment, and captan has been
found in biological waste of ornamental plants (Taube et al., 2002).
Also, when seen in the light of development of fungicide resistance,
the use of fungicide should not be the preferred approach.
It has been suggested that the colonization of paper pots and
growing and casing media with saprophytes is more likely to occur
due to lack of competition from other microorganisms (e.g. (Roll-
Hansen, 1961; Toppe and Herrero, 2005). This is in line with the fact
that P. ostracoderma has been found to colonize steam sterilized peat
cubes with seedlings (Kilpatrick, 1977) and that it has also been found
on paper pots, vermiculite, and rockwool which are made of heat
treated materials (Table s1). Therefore another attempt to avoid or min-
imize these fungi might be to apply competitive microorganisms to out-
compete the ‘problematic’ fungi. It is important that these
microorganisms do not sporulate on the surfaces of pots or growing
media to avoid aerosolisation of spores. We have found no studies
about this, but biopesticides to control plant pathogens are widely
used in greenhouses. It is, however, remarkable that some of the species
in focus in this paper are used as biopesticides.
Another approach could be to investigate the influence of different
ingredients of pots or growing media on the colonization by sapro-
phytes. The biodegradation rate of recycled paper has been studied
with C. globosum, and with a mixture of A. niger, T. viride, and Penicillium
funiculosum. The paper contained four concentrations of cereal bran.
The fungi colonized the paper and sporulated on the surface, and it
was found that the addition of wheat bran increased susceptibility to
fungal colonization and the degradation of the paper (Sandak et al.,
2011). Whether addition of wheat bran to paper pots also causes an in-
creased colonization by these fungi at greenhouse level has to our
knowledge not been studied. In nature, peat is formed when plant ma-
terial does not fully decay in acidic and anaerobic conditions, and it is
classified in terms of how much it is decomposed. As mentioned previ-
ously, under experimental conditions P. ostracoderma was shown to col-
onize different growing media such as slightly decomposed peat but not
moderately and strongly decomposed peat nor green waste and bark
compost (Meinken et al., 2015). In another study different media for
growing grass have been compared, and the author noted that
P. ostracoderma was found on the surfaces of sphagnum peat and soy-
bean chop media, but was absent on other media: corn chop, cotton
chop, pine bark, oak sawdust, and sewage sludge (Shepard, 1978).
Thus, it may be possible to avoid or reduce the colonization by
P. ostracoderma by using the right growing medium. According to data
from 2013 from 16 European countries, composted green waste and
composted or aged bark were mainly used for hobby plant production
while sphagnum peat was used in larger amounts for professional
plant production (Schmilewski, 2017). For mushroom production, a
A.M. Madsen and B. Crook
study with P. ostracoderma on casing material shows that the fungus
grows well on a fibre-mix with peat, bark, or pumice casing, but not
on pure bark (Rainey, 1985). Consequently, it seems to be possible to re-
duce growth of some fungi using the right composition of growing or
casing media or ingredients in paper pots. However, the ability of the
plants or mushrooms to grow in these media is of course essential. In
addition to considering the ingredients in pots, growing and casing
media, an approach could also be to study how plant cultivation condi-
tions such as light, fertilizer, and pH affect the colonization by sapro-
phytes. Under laboratory conditions, P. ostracoderma conidia are able
to germinate in a wide range of pH and temperatures, thus it can germi-
nate in a buffer with pH from 3 up to 8 and in temperatures from 20 °C
to 42 °C (Fergus, 1971). In studies in forest soils, drying out of the soil
(Bastida et al., 2019) and increased pH (De Witte et al., 2017) caused a
higher abundance of the genus Peziza and lower abundance of many
saprophytes.
Sporothrix schenckii mainly infects via trauma to the skin due to
punctures from thorns, splinters, or cut or abraded skin. To avoid infec-
tions with the skin pathogen Sp. schenckii workers handling sphagnum
moss are suggested to use long sleeves and puncture-resistant gloves;
for building topiary alternatives to sphagnum moss is suggested as e.g.
plastic foam (Control, 1988; Hajjeh et al., 1997).
To increase the sustainability of growing media different types of
biowastes are also tested for their use for growing media (Gruda,
2019), however in other occupational settings work with biowaste is as-
sociated with bioaerosol exposure related health effects (Breum et al.,
1996; Heldal et al., 2003). With the present study we have highlighted
the importance of also considering the occupational health of the
growers who may be exposed to fungi from biodegradable pots and
growing and casing media in use as well as media for reuse. The study
also shows that the cases of HP cause long periods of disease, and for
some workers it is not possible to go back to the same work. Financial
feasibility analysis of converting from e.g. plastic pots to degradable
paper pots for greenhouse companies have been performed (Hall
et al., 2010). We suggest to further investigate the extent and severity
of the occupational exposure related health effects of the transition to
biodegradable materials, and that occupational health is also part of
the financial feasibility analysis.
Continuing trends in intensive agriculture, requirements to ensure the
food supply chain security, and attempts to overcome unpredictable and
changing climate means that the production of vegetables in greenhouses
increases, and at the same time the production of edible mushrooms is in-
creasing. Therefore, a focus on occupational exposure and related health
in these environments is important. In summary, P. ostracoderma is a
coloniser of economic important paper pots and growing and casing
media, but exposure of workers to their growth on such materials may
also present the hazard of allergic respiratory disease. Further work is
therefore recommended to establish the likely levels of exposure and
the level of risk associated with this hazard, and as a consequence the mit-
igations required to reduce the risk. An attempt to reduce the fungal col-
onization could be to consider the formulation of paper pots and growing
or casing media. On the other hand this review shows that P. ostracoderma
grows on many different media. Furthermore, other fungi known to cause
occupational HP as A. fumigatus, A. niger, and T. viride were also found on
different media including paper and peat, and Cr. corticale on bark chips
has caused HP. Cases of skin irritation caused by S. chartarum on paper
pots have been reported, and serious skin infections by Sp. schenckii
from peat are reported. Overall this study shows that several fungal spe-
cies on pots and growing and casing media have caused HP, but for each
species the evidence is weak. On the other hand, the species have also
caused HP in other environments. In the measurement of risks associated
with work in greenhouses and mushroom farms and in the introduction
of new pots and growing and casing media the occupational fungal expo-
sure should be considered.
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.scitotenv.2021.147832.
12
Science of the Total Environment 788 (2021) 147832
Funding
This research did not receive any specific grant from funding agen-
cies in the public, commercial, or not-for-profit sectors.
CRediT authorship contribution statement
Anne Mette Madsen: Conceptualization, Data curation, Formal anal-
ysis, Investigation, Methodology, Project administration, Supervision,
Visualization, Writing – original draft, Writing – review & editing.
Brian Crook: Validation, Writing – review & editing.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influ-
ence the work reported in this paper.
Acknowledgements
Alicja Mortensen at NRCWE is greatly acknowledged for helping
with extracting information from papers in Polish. Petra Jackson is
greatly acknowledged for helping with extracting information from pa-
pers in Czech. Karen Bo Frydendall at NRCWE is highly acknowledged
for commenting on the manuscript.
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