Energy Education Science and Technology
2004 Volume(issue) 13(1): 31-38
Contents of detrimental metals mercury,
cadmium and lead in wild growing edible
mushrooms: a review
Pavel Kalač*, Lubomír Svoboda, Božena Havlíčková
Univ. of South Bohemia, Faculty of Agriculture, Dept. of Chemistry, 370 05 České Budějovice, Czech Republic
Received 15 July 2003; accepted 13 September 2003
Abstract
Mushrooms have been a popular delicacy in many countries. Some species, mainly from genera
Agaricus, Macrolepiota, Lepista and Calocybe accumulate high contents of mercury and cadmium
even in unpolluted sites. The contents of both metals and also of lead increase significantly in the
heavily polluted sites, such as in the vicinity of metal smelters or inside cities. Current data on
mercury content in many less common species growing in Poland and on cadmium content in species
typical for Turkey are presented in tables. Present knowledge of metal speciation in mushrooms is
limited, as is knowledge of their bioavailability in man. Consumption of the accumulating species
should be thus restricted. The cultivated species contain only low levels of the metals. Very limited
information is available on metal shrinkage during preservation and culinary treatments of
mushrooms.
Keywords: Heavy metals; Mercury; Cadmium; Lead; Edible mushroom
1. Introduction
Wild growing mushrooms (higher fungi, macrofungi) have been a popular delicacy in
many countries and their consumption has been several kilos per year for some individuals.
However, research found out during last three decades that many mushroom species
accumulate several trace elements, mainly mercury, cadmium and lead, at levels greatly
exceeding contents in other foods. Moreover, a lot of mushroom species accumulate
radioactive isotopes of cesium [1].
The accomplished research has had two main objectives: screening of mushroom fruiting
bodies as bioindicators of environmental pollution and searching for edible species
accumulating high levels of some trace elements. The former aim was preferred in Western
Europe where consumption of wild growing mushrooms has been very limited, culminated in
1980´s and declined after finding that mushrooms cannot be used as a reliable indicator. The
latter approach has been exerted mainly in countries with popular consumption of wild
growing mushrooms, e.g. in countries of Central and East Europe, and in Turkey.
Several reviews of trace element contents were published [2-4]. The latest literature data
dealing with contents of harmful heavy metals mercury, cadmium and lead in edible
mushrooms are reviewed in this article.
________
*
Corresponding author. Tel: +420-387-772-657; fax: +420-385-310-405
E.mail address: kalac@zf.jcu.cz (P. Kalač)
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2. Factors affecting the heavy metals concentrations in fruiting bodies
Some mycological terms are used in the review. Fruiting body is visible part of a
mushroom, fructification is formation of fruiting body. Fruiting body consists of cap (pileus)
with spores-forming part (sporophore) and stipe (stem, stalk). Mushroom uptakes nutrients
from a substrate via spacious mycelium.
Knowledge on roles of mercury, cadmium and lead in physiology of higher fungi has been
very limited. Contents of the metals are primarily species-dependent, while role of a genus or
a family is of lower importance, as is nutritional strategy – mycorrhizal, parasitic or
saprophytic. Substrate composition is an important factor; however, great differences exist in
uptake of individual metals [2, 5, 6]. Mercury and cadmium are accumulated in fruiting
bodies, while lead contents are lower in the fruiting body than in the substrate. The reported
bioaccumulation factors are 30-500, 50-300 and 0.01-0.1 for mercury, cadmium and lead,
respectively.
Age and size of the fruiting body are of less importance. The proportion of the metal
contents originating from atmospheric depositions seems to be also of less importance due to
the short lifetime of a fruiting body, which is usually 10-14 days. In our opinion, metal
contents in fruiting bodies are considerably affected by the age of mycelium and by the
interval between the fructifications. Maximum metal contents are observed in the initial
harvest wave of cultivated white mushroom (Agaricus bisporus). The metal levels determined
in wild growing A. bisporus are considerably higher than contents in cultivated fruiting
bodies. Probable explanation is not only in different substrate composition and contamination,
but also in different age of mycelium, which may exist for several years in nature, while only
for several months in a cultivation plant.
Combination of all these factors causes very wide variability of the metal contents within a
species, usually to one order of magnitude. Thus, ranges of the metal levels are remarkably
wider than in plant materials. Contents have been usually expressed as mg kg-1 dry matter.
There exists a consensus for recalculation to fresh matter that dry matter content of
mushrooms is 10 %. For calculations, usually 300 g of fresh mushrooms per meal, is
assumed.
The metals are distributed unevenly within a fruiting body. The highest levels are observed
in the spore-forming part, but not in spores, lower contents in the rest of the cap and the
lowest in the stipe.
Knowledge of transport mechanisms of the metals from mycelium to the fruiting body has
been very limited. Mercury transport is likely to be affected by sulphydryl group content in a
protein carrier, while cadmium transport has another mechanism [7, 8].
3. The effects of environmental pollution on the metal contents in fruiting bodies
Surprising accumulation ability in several mushroom species promoted their screening as
bioindicators. Wondratschek and Röder in their review [9] concluded that no mushroom
species could be considered as a believable indicator of environmental pollution with heavy
metals. However, fruiting bodies can be useful to distinguish between polluted and unpolluted
areas. Coprinus comatus seems to have a higher informative value for contamination with
lead [10].
High contents of the metals have been observed in mushrooms growing in heavily polluted
areas, such as in close proximity to highways with heavy traffic [11], landfills of sewage
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33
sludge [12] and emission areas [13] including cities [14, 15, 16]. Extremely high metal levels
were determined in the vicinity of metal smelters [17-20]. High metal contents are reported
also from areas contaminated historically by ores mining and processing.
Ability of some mushrooms and filamentous fungi to accumulate heavy metals has been
tested for bioremediation of contaminated soils [21].
4. Health aspects
Extensive information is currently available on the metal contents in many mushroom
species. However, their assessment has been difficult due to limited knowledge on their
chemical forms and bioavailability in man.
Some countries have established statutory limits for the metals in edible mushrooms. For
instance, the limits 5.0, 2.0 and 10.0 mg kg-1 dry matter have been valid in the Czech
Republic since 1999 for mercury, cadmium and lead, respectively, in wild growing
mushrooms. According to FAO/WHO recommendations, acceptable weekly intakes are
0.005, 0.007 and 0.025 mg per kg body weight for mercury, cadmium and lead, respectively.
Usual mercury, cadmium and lead contents in 25 mushroom species widely consumed within
Europe, collected from unpolluted (background) areas, were tabulated in our previous review
[4]. Thus, only the latest data will be reviewed in the following text.
4.1 Mercury
Heavily accumulated species, up to 20 mg kg-1 dry matter, are Calocybe gambosa, Lepista
nuda and Agaricus arvensis. High contents up to 10 mg kg-1 dry matter are typical for genera
Agaricus and Macrolepiota and levels up to 5 mg kg-1 for species of genus Boletus. Extremely
high contents, one order of magnitude higher than the background levels, were observed in
areas polluted from both historical and present mercury smelters [19, 20, 22].
Current data on total mercury content in less frequently analysed mushroom species from
Poland [23-31] are given in Table 1. Moreover, interesting comprehensive information on
values of bioaccumulation factor between mercury content in cap or stipe and underlying
substrate from depth 0-10 cm was reported. However, both mercury contents and
bioaccumulation factor values varied widely within the individual species. Calvatia
excipuliformis seems to be the only species with increased mercury content.
Low mercury contents, rarely exceeding 1.5 mg kg-1 dry matter, were determined in over
200 mushroom species from different rural unpolluted parts of Turkey in a series of current
papers [32-41].
Limited information is available on the proportion of highly toxic methylmercury. This
was reported to be usually only a few per cent of total mercury content. About 1 % was found
in widely-consumed species Xerocomus badius and Leccinum scabrum. Mushrooms
accumulate methylmercury from substrate with a bioaccumulation factor of about 20 and/or
methylate mercuric salts [22].
4.2 Cadmium
Cadmium contents in the most of edible mushroom species growing in unpolluted areas
are below 2 mg kg-1 dry matter. However, levels in Boletus aestivalis, Leccinum scabrum,
Calocybe gambosa, Armillaria mellea and Russula cyanoxantha can be up to 5 mg kg-1 dry
matter and in the genus Agaricus up to 50 mg kg-1 dry matter, mainly in Agaricus species
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yellowing after mechanical damage of tissue [4]. Extremely high contents up to 300 mg kg-1
dry matter were noticed [2]. Considerably increased cadmium levels were reported in
mushrooms growing in the vicinity of metal smelters [18-20] and within a town [16].
Data on 17 edible species with cadmium content exceeding 2 mg kg-1 dry matter are given in
Table 2. The species represent only below a tenth from mushrooms collected from different
Table l. Mean contents of total mercury in caps and stipes of several edible mushroom
species collected in Poland and mean values of bioaccumulation factor (fruiting
body/substrate ratio). Data from references [23-31]
Species
Boletus pinophilus
Calvatia excipuliformis
Clitocybe odora
Leccinum griseum
Leccinum rufum
(syn. L. aurantiacum)
Leccinum versipellis
Marasmius oreades
Rozites caperata
Russula vesca
Russula xerampelina
Sarcodon imbricatus
Suillus bovinus
Suillus flavus
Tricholoma flavovirens
Tricholoma portentosum
Tricholoma terreum
Mercury content (mg kg-1
dry matter)
Cap
Stipe
2.0
0.85
4.4
1.9
0.94
0.86
0.82
0.6 – 1.8
0.45 – 0.93
0.46 – 0.72
0.73 – 0.93
1.2
0.05
0.06
2.3
0.32
0.60
0.12 – 0.24
0.10 – 0.18
0.03 – 0.25
0.25 – 0.42
0.48
0.47
0.03
0.04
1.1
0.16
0.15
0.07 – 0.17
0.03 – 0.09
0.02 – 0.12
Bioaccumulation factor
Cap
110
960
54
22 - 73
Stipe
44
310
52
14 – 46
10 - 24
19
36
18
2.7
73
53
17
7.5 - 37
3.5 – 9.6
0.6 – 3.8
5.4 – 14
13
14
12
1.8
30
26
4.1
5–7
1.1 – 4.4
0.4
rural areas of Turkey [32-41]. Unfortunately, usually only one sample was analysed and wide
variation of contents must be supposed. The contents determined in Armillaria mellea and
Russula cyanoxantha are well comparable with data observed in Central Europe [4].
The information on chemical forms of cadmium in mushrooms has been very scarce.
Several works reported comparable and higher absorption from mushrooms than from
inorganic cadmium salts in both experimental animals and volunteers [42-44]. Cadmium level
in blood serum increased considerably following mushroom consumption [42]. Thus,
cadmium seems to be the most deleterious among heavy metals in mushrooms.
4.3 Lead
Common lead content in a lot of edible mushroom species from unpolluted sites is below 2
mg kg-1 dry matter, but levels up to 5 mg kg-1 dry matter have been reported for numerous
species. Contents up to 10 mg kg-1 dry matter are usual in the genera Agaricus and
Macrolepiota and in Lepista nuda, and even higher in Lycoperdon perlatum [4]. Increased
levels are common in mushrooms growing around highways. Extremely high lead levels over
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35
100 mg kg-1 dry matter were observed in the close vicinity of lead smelters [17, 18].
Lead contents above 3 mg kg-1 dry matter were reported only rarely in the surveys of over
200 mushroom species from several unpolluted Turkish sites [32-41].
5. The metals in cultivated mushrooms
Contents of mercury, cadmium and lead are considerably lower in the cultivated
mushrooms than those in the same or taxonomically-related wild growing species [45].
Agaricus bisporus has been very susceptible to increasing content of mercury and to a lesser
extent of cadmium in substrate and bioaccumulates the both metals and lead in its fruiting
bodies [46, 47].
Table 2. Edible mushroom species with cadmium content above 2 mg kg-1 dry matter
collected from unpolluted sites of Turkey [32-41]
Species
Cadmium content (mg kg-1 dry matter)
Agaricus bisporus
3.5
Agaricus bitorquis
3.1
Agaricus silvicolla
4.2 – 4.9
Armillaria mellea
2.5 – 5.5
Boletus luridus
2.2
Cantharellus subalbidus
2.3
Cantharellus tubaeformis
2.1
Cystoderma amianthinum
2.2
Hydnum repandum
3.1 – 3.6
Hypholoma capnoides
3.2
Kuehneromyces mutabilis
2.1
Laccaria amethystina
2.7
Laccaria laccata
2.1
Lactarius deliciosus
2.8
Lactarius sanguifluus
3.2
Russula cyanoxantha
3.2
Russula delica
2.3 – 4.3
6. Shrinkage of the metals during mushroom preservation and culinary processing
Data on possibility to decrease contents of the metals during mushroom preservation and
different culinary treatments are almost absent. Washing and peeling of A. bisporus decreased
contents of cadmium and lead by 30-40 % [48]. There was investigated leaching of mercury,
cadmium and lead from fresh, freeze-dried, air-dried and frozen slices of Xerocomus badius
during either soaking in 0.3% table salt solution at ambient temperature for 5, 10 or 15
minutes or repeatedly for 3x5 minutes or boiling in the same solution for 15, 30 or 60
minutes. Short-time boiling was found out to be a more efficient operation than soaking. The
metals were leached to the greatest extent from the most destroyed tissues of frozen
mushroom slices, but less so from fresh or freeze-dried tissues. The most extensive leaching
was observed for cadmium and the lowest for mercury [49].
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Acknowledgement
The authors thank the Grant Agency of the Czech Republic for the financial support by the
grant 525/03/D067.
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