Food Control 102 (2019) 17–21

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Food Control
journal homepage: www.elsevier.com/locate/foodcont

Mercury in stir-fried and raw mushrooms from the Boletaceae family from T
the geochemically anomalous region in the Midu county, China
Jerzy Falandysza,b,c,∗,1, Ji Zhangc,d, Małgorzata Mędyka, Xue Zhange
a
University of Gdańsk, Environmental Chemistry & Ecotoxicology, 80-308, Gdańsk, Poland
b
Environmental and Computational Chemistry Group, School of Pharmaceutical Sciences, Zaragocilla Campus, University of Cartagena, 130015, Cartagena, Colombia
c
Institute of Medicinal Plants, Yunnan Academy of Agricultural Sciences, Kunming, 650200, China
d
Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Kunming, 650223, China
e
Faculty of Chemistry and Pharmacy, Yunnan Industry & Trade Vocational College, Anning, 650300, China

A R T I C LE I N FO A B S T R A C T

Keywords: Investigation has been made on contamination with mercury of a raw and stir-fried in moderate oil mushrooms
Cooking grew in geochemically anomalous soils in south-west Asia. The “bolete” mushrooms studied were Baorangia
Exposure bicolor, Boletus edulis, Boletus speciosus, Retiboletus griseus, Rugiboletus extremiorientalis and Sutorius magnificus. The
Food toxicology batches of fresh mushrooms were respectively dried and stir-fried in moderate oil using a wok pan. Data ob-
Mercury intake
tained confirmed on elevated Hg content in mushrooms from the southwestern China and showed on elevated
Organic food
content of the element in popular mushroom dishes. The meal (100 g) made of fried “boletes” could provide for
consumer Hg in dose from 0.27 to 1.4 (median 0.96) μg kg−1 body mass (RfD, reference dose is 0.3 μg kg−1 bm
per day). Fried mushrooms if taken daily over a week period (100 g × 7) could provide Hg in dose from 1.9 to
9.6 (median 6.8) μg kg−1 bm. In view of the reference values for safe intake of inorganic Hg (PTWI, provisionally
tolerable weekly intake is 4 μg kg−1 bm) and moderate consumption, the fried bolete mushrooms could provide
Hg in doses exceeding the safe limit.

1. Introduction
Toxic mercury (Hg) that usually occurs in a small concentration in
soils is well transferred into the flesh by some mushrooms, including
edible species (Falandysz, 2002 and, 2016; Falandysz et al., 2003). In
the world there are regions with soils naturally Hg-enriched due to
formation of the mercuriferous belts with polymetallic soils/geochem-
ical anomalies (Gustin et al., 1999). Mushrooms from soils both natu-
rally elevated in Hg or polluted because of the cinnabar mining and
processing or from other sources can accumulate Hg in elevated con-
centrations (Bargagli & Baldi, 1984; Falandysz, 2017; Vogel-Mikuš
et al., 2016). A diffusive pollution of the environment with airborne Hg
on a global scale also contribute to a forest topsoil pollution (Suchara &
Sucharova, 2002), and so contribute also to its higher soil background
regionally and locally.
China has regions with polymetallic soils, including the south-
western part of the country that is also rich in mountainous forests and
edible mushrooms. In previous studies of the forest topsoil and mush-
rooms from the southwestern China has been observed that Hg in
0–10 cm layer of soils was well above 0.1 mg kg−1 dry matter (dm), and
maximum was 3.4 mg kg−1 dm (Falandysz, Dryżałowska, Saba, Wang,
& Zhang, 2014; 2015a). Mushrooms grown on polymetallic Yunnan
soils showed elevated levels of Hg (up to 22 mg kg−1 dry biomass (db)
in pooled samples of caps and 8.4 mg kg−1 db in stems in Boletus spp.)
and high bioconcentration factors (BCF) reaching 6.5 for caps and 2.5
for stems (Falandysz et al., 2015b and, 2016, 2015a; Kojta et al., 2015).
In the regions of Asia are many places with a geochemical anomalies
and biodiversity of mushrooms that are widely collected and cooked
either fresh or preserved (Liu et al., 2018; Murugkar & Subbulakshmi,
2005; Wang et al., 2014). A popular composite of a dinner served in
south-west Asia are meals made of a stir-fried young “bolete” mush-
rooms and other species (Falandysz & Borovička, 2013; Liu et al., 2018;
Zhang, Li, Yang, Liu, & Wang, 2015). A term “bolete” mushrooms is
traditionally used in Yunnan for mushrooms from the genus Boletus and
others similar mushrooms from the family Boletaceae, regardless of the
latest achievements in the molecular biology and changes in the sys-
tematic classification.
China is also a major producer and exporter of the cultivated and

∗
Corresponding author. University of Gdańsk, Environmental Chemistry & Ecotoxicology, 80-308, Gdańsk, Poland.
E-mail address: jerzy.falandysz@gmail.com (J. Falandysz).
1
Visiting professor.

https://doi.org/10.1016/j.foodcont.2019.03.007
Received 25 January 2019; Received in revised form 7 March 2019; Accepted 8 March 2019
Available online 13 March 2019
0956-7135/ © 2019 Elsevier Ltd. All rights reserved.
J. Falandysz, et al.
wild growing mushrooms both for the Chinese domestic market and to
other countries and also is a large consumer of the boletes (Li et al.,
2016; Marzano, Bracchi, & Pizzetti, 2001; Zhang, Gao, Ma, Luo, & Su,
2008). China in 2016 produced 48,347.20 tons of the boletes and
46,220.00 tons of the collection came from the Yunnan province (CEFA,
2016).
The stir-frying of mushrooms can be performed in deep oil or with a
moderate volume of oil and sometimes after an initial blanching (par-
boiling) in a wok pan (Qiu, 2003). During the growing season, mainly
fresh and relatively young individuals are sold and cooked. The Hg
transfer from the polymetallic soils into the human meals containing
contaminated mushrooms may pose health risks, thus, it is important to
understand not only the content in raw mushrooms but also effect of
cooking, speciation and availability.
Cooking (boiling and pickling or canning) usually reduce content of
metallic elements, including Hg but also essential nutrients in a
mushroom meal (Drewnowska et al., 2017; Falandysz & Drewnowska,
2015 and, 2017; Pankavec et al., 2019). This study investigated the
potential effect of stir-frying in moderate volume of oil on fate of Hg in
“bolete” mushrooms as well as possible Hg intake with the mushrooms
meals in view of safety limits. Data on the effects of stir-frying in
moderate volume of oil using a wok on the Hg and other metallic ele-
ments content and intake from the mushrooms meals are absent in the
literature.
2. Materials and methods
2.1. Raw mushrooms
The raw mushrooms examined were such species as Baorangia bi-
color (Kuntze) G. Wu, Halling & Zhu L. Yang [previous name Boletus
bicolor Peck], Boletus edulis Bull., Boletus speciosus Forst., Retiboletus
griseus (Frost) Manfr. Binder & Bresinsky [previous name Boletus griseus
Frost], Rugiboletus extremiorientalis (Lj.N. Vassiljeva) G. Wu & Zhu L.
Yang [previous name Leccinum extremiorientale (Lj.N. Vassiljeva)] and
Sutorius magnificus (W.F. Chiu) G. Wu & Zhu L. Yang [previous name
Boletus magnificus W.F. Chiu] (Table 1). Mushrooms were collected from
the region of the Midu County in the Dali Bai Autonomous Prefecture in
west-central Yunnan province of China at the beginning of August
2018.
Mushrooms (from 5 to 21 of relatively young individuals in a pool)
(Table 1) were cleaned-up from any adhered soil debris using a plastic
knife and brush, separated for caps and stipes and sliced. Moisture
content of each sample was determined gravimetrically by oven-drying
of a pooled sample for 24 h to a constant biomass at 65 °C (Ultra
FD1000, Ezidri, Australia). Dried mushrooms were grounded to a fine
powder using the porcelain mortar and pestle and kept in screw poly-
ethylene bags in dry and clean condition until instrumental analysis.
2.2. Cooked mushrooms
The mushroom dishes were made of the same species as were the
raw mushrooms examined (Table 1). Mushrooms were of a similar size
(from 5 to 23 young individuals per a sample, respectively) and were
collected from the same sites and in the same time as were the raw
mushrooms. After clean-up using a plastic knife and brush, the mush-
room samples were separated for caps and stems and sliced. Each
sample was separately stir-fried with respectively from 15 to 55 g of a
hot vegetable oil (depending on the sample size) in a wok for 10 min.
Fried mushrooms were drained from any oil residues, freeze-dried,
grounded and kept in tightly closed polyethylene jars until analyses.
2.3. Analysis
The subsamples of dehydrated fungal materials were analysed using
cold-vapour atomic absorption spectroscopy (CV-AAS) by a direct
18
Food Control 102 (2019) 17–21
sample thermal decomposition coupled with amalgamation of Hg va-
pour with a gold wool trap and its further desorption and quantitative
measurement at wavelength of 253.7 nm. The spectroscope was a
mercury analyzer (MA-2000, Nippon Instruments Corporation,
Takatsuki, Japan) equipped with an auto-sampler, and the operational
details have been described previously (Falandysz et al., 2015a). One
blank sample and one certified reference material sample were ex-
amined with each two determinations of the fungal material studied.
Recovery of Hg for certified reference material (CS-M-3; dried
mushroom powder B. edulis; n = 11) produced by the Institute of
Nuclear Chemistry and Technology, Warsaw, Poland, examined con-
currently with experimental mushrooms was 99.9% (certified value of
Hg was 2.849 mg kg−1 and determined value was
2.87 ± 0.05 mg kg−1).
3. Results and discussion
3.1. Hg in raw mushrooms
The mushrooms B. bicolor, B. edulis, R. griseus, S. magnificus, B.
speciosus and R. extremiorientalis contained Hg in pooled samples of the
whole fruiting bodies in the range from 0.92 to 3.32 mg kg−1 dry bio-
mass (db). The caps were the morphological part that was from 1.6 to
2.9 fold higher in Hg than the stems (Table 2). The species R. ex-
tremiorientalis, R. griseus and B. edulis showed 2–3 fold higher con-
tamination with Hg than B. bicolor, S. magnificus or B. speciosus.
Data on high levels of Hg in “bolete” mushrooms obtained in this
study (Table 1) confirm that mushrooms foraged from a certain regions
of the Dali prefecture in Yunnan can be substantially contaminated with
this element. They agree with the previously available data for the
southwestern Asia (Falandysz et al., 2015b, 2016, 2015a; Kojta et al.,
2015). Nevertheless, because of the size of this montane region
(29,459 km2) and many sites where mushrooms can be foraged, a sys-
tematic study including soil substrata would be necessary to get a more
clear picture on a spatial distribution of Hg in soils and mushrooms
there.
3.2. Hg in stir-fried mushrooms
The stir-fried B. bicolor, B. edulis, R. griseus, S. magnificus, B. speciosus
and R. extremiorientalis contained Hg in pooled samples of the whole
fruiting bodies in the range from 0.29 to 1.92 mg kg−1 dry biomass
(db). Fried caps had Hg in concentration from 1.1 to 3.4 fold greater
than the stems (Table 2).
The studied batches of a corresponding species of mushrooms – on
the one hand, raw and on the other fried - were not equivalent re-
garding to the homogeneity of the composition. Thus, it is impossible
from the present study to conclude about the exact effect of cooking on
lowering or not of the Hg content during frying. The aim of the research
was, among others, the desire to learn what is the real content of Hg in
stir-fried mushrooms meals made in typical conditions in the roadside
restaurants in south-west Asia, and what is the Hg intake in view of the
safety limits.
It can be assumed that in the course of frying and regardless of a
volume of oil or fat/butter used some constituents will leak from
mushrooms into the oily residue (juice) and/or will co-evaporate with
water. Mushrooms’ flesh is made up of 90% water (Table 1). In the
frying process temperature is high (in deep oil frying oil reaches 175 °C
in average) (Bordin, Kunitake, Aracava, & Trindade, 2013), and a
portion of moisture evaporates (dehydration of foods) while a portion
of frying oil is absorbed by food.
In present study mushrooms in the course of frying lost from 36 to
55% of moisture and absorbed almost a whole volume of oil added
(Table 1). Oil absorption rate was from 24 to 32 g per 100 g of fried
mushrooms (left oily residue was from 0.82 to 5.7 g per a sample) and
varied for differed morphological parts of the fruiting bodies and
J. Falandysz, et al. Food Control 102 (2019) 17–21

Table 1
Description and size of the mushroom samples, percentage of moisture content of the fresh and cooked mushrooms, fresh and dry biomass share between caps and
stems of the fruiting bodies, percentage of hidden oil sorbed by fried mushrooms, percentage of moisture loss by cooked mushrooms due to dehydration and
proportion between fresh mushrooms biomass and oil sorbed in the course of frying.
Species Raw mushrooms Fried mushrooms

Moisture (%) Fresh biomass (g) share Dry biomass (g) share Moisture content Oil sorbed (%) Moisture lost (%) Fresh mushrooms: absorbed oil (g/
(%) (%) (%) g)a

Baorangia bicolor
Caps 89.4 59.9 65.1 46.0 20 27 5.3 : 1
Stems 88.3 40.1 34.9 41.0 40 60 3.1 : 1
Whole 88.9 100 100 44.9 24 36 4.2 : 1
Boletus edulis
Caps 91.9 42.7 40.3 60.5 28 61 6.3 : 1
Stems 90.3 57.3 59.7 59.1 26 47 4.7 : 1
Whole 90.6 100 100 59.7 27 53 5.5 : 1
Boletus speciosus
Caps 90.0 47.2 51.1 58.6 20 44 6.9 : 1
Stems 88.9 52.8 48.9 56.3 27 54 5.1 : 1
Whole 89.4 100 100 57.3 24 50 6.0 : 1
Retiboletus griseus
Caps 91.5 54.7 60.5 59.2 29 49 4.5 : 1
Stems 91.9 45.3 39.5 52.1 37 63 4.0 : 1
Whole 91.7 100 100 57.2 32 55 4.2 : 1
Rugiboletus extremiorientalis
Caps 87.7 32.5 35.4 54.3 29 48 4.3 : 1
Stems 88.5 67.4 64.6 52.3 29 52 4.9 : 1
Whole 88.2 100 100 53.0 29 51 4.6 : 1
Sutorius magnificus
Caps 90.0 55.4 53.2 59.1 28 46 4.4 : 1
Stems 88.2 42.7 46.8 55.3 21 52 7.6 : 1
Whole 89.2 100 100 57.4 25 49 6.0 : 1

Notes:
a
Oil used - whole weight: whole weight (g/g).

Table 2 species (Table 1). Mushroom cutting and high temperature dehydration
Mercury contents in raw and cooked mushroom materials and Hg index Qc/s. can promote leakage of juice and compounds from plasma through
Species Raw mushrooms Fried mushrooms
damaged cell walls to oily phase during frying. Some water soluble
constituents can be lost from fried mushrooms to oily residue and co-
n∗ Hg (mg kg−1 db) Qc/s n∗ Hg (mg kg−1 db) Qc/s evaporate with water.
#
The boletes mmushrooms, e.g., Boletus edulis Bull., are high in sul-
Baorangia bicolor
Caps 21 1.63 ± 0.05 22 0.32 ± 0.01
phur and elevated both in Hg and Se (Falandysz, Zhang, Wiejak,
Stems 21 1.02 ± 0.05 22 0.19 ± 0.00 Baralkiewicz, & Hanc, 2017 and 2013; Falandysz, Frankowska, &
Whole fruiting 21 1.41 1.6 22 0.29 1.7 Mazur, 2007; Nasr & Arp, 2011; Nasr, Malloch, & Arp, 2012; Vogel-
bodies Mikuš et al., 2016). Mercury in mushrooms is largely in a form of the
Boletus edulis
compounds hardly soluble in water (largely Hg in bonds with eSH
Caps 5 3.54 ± 0.08 6 2.23 ± 0.10
Stems 5 1.21 ± 0.05 6 0.67 ± 0.04 groups in peptides and proteins and in minor part as HgSe, HgS and
Whole fruiting 5 2.14 2.9 6 1.23 3.4 CH3Hg+) (Stijve & Roschnik, 1974; Vogel-Mikuš et al., 2016). Thus, Hg
bodies may be less wasted and it remains largely with fried mushrooms.
Boletus speciosus When expressed on a wet biomass (whole weight or product weight)
Caps 5 1.40 ± 0.08 5 2.67 ± 0.05
Stems 5 0.56 ± 0.02 5 1.30 ± 0.08
basis, the stir-frying in moderate oil significantly increased content of
Whole fruiting 5 0.99 2.5 5 1.92 2.0 Hg in fried meals if relate to results for fresh mushrooms (Table 3).
bodies Dehydration causes concentration of Hg in fried mushrooms while ab-
Rugiboletus extremiorientalis sorbed oil (it was free from Hg) slightly dilutes this effect.
Caps 12 5.28 ± 0.28 12 2.85 ± 0.11
The reported data on the effect of frying (a flat pan) on the elements
Stems 12 2.28 ± 0.12 12 1.14 ± 0.01
Whole fruiting 12 3.32 2.3 12 1.70 2.5 content of cooked mushrooms relate so far only to the radioactive
bodies caesium (137Cs) (Kenigsberg et al. 1996; Steinhauser & Steinhauser,
Sutorius magnificus 2016). In a study by Kenisberg et al. 1996, the 137Cs activity con-
Caps 6 1.16 ± 0.01 7 0.88 ± 0.02 centration in mushrooms decreased by 70% in the course of frying
Stems 6 0.64 ± 0.01 7 0.79 ± 0.01
Whole fruiting 6 0.92 1.8 7 0.84 1.1
(without details on effect on possible 137Cs intake), while content in-
bodies creased by 105% when mushrooms were dried. The mushrooms Can-
Retiboletus griseus tharellus cibarius and Boletus edulis when wet or dry cleaned from soil
Caps 8 3.52 ± 0.04 8 1.94 ± 0.01 debris and fried with a small volume of vegetable oil leaked 137Cs into
Stems 8 1.79 ± 0.05 8 0.91 ± 0.03
the oily residue (juice) in higher rate by washed (19–29%) and dry-
Whole fruiting 8 2.80 2.0 8 1.60 2.1
bodies cleaned (2–16%) chanterelles than by washed (6%) and dry-cleaned
(0%) boletus (Steinhauser & Steinhauser, 2016).
Notes: n∗ (the number of specimens in a pool). A handful of data is available on loss of Hg (decrease respectively by
15–22%, 15–35%, 34–39%, 10% and 56 ± 2%) for a few species in the
course of a real household treatment such as blanching and pickling of

19
J. Falandysz, et al. Food Control 102 (2019) 17–21

Table 3
Mercury content in fresh mushrooms and in fried mushrooms meals (μg kg−1 wet product) from the Midu region of Yunnan, China and estimated daily and weekly
Hg intake with the mushroom meals.
Species Hg (μg kg−1 wet product) Hg (μg kg−1 wet product) Hg intake (μg) Hg intake (μg) Estimated daily Hg Estimated weekly Hg
in fresh mushrooms in fried mushrooms 100 g meal 100 g × 7 meals intake (μg kg−1 bm)a intake (μg kg−1 bm)b

Baorangia bicolor 160 160 16 110 0.27 1.9

Boletus edulis 200 500 50 350 0.83 5.8
Boletus speciosus 100 820 82 570 1.4 9.6
Retiboletus griseus 230 680 68 480 1.1 7.9
Rugiboletus extremiorientalis 390 800 80 560 1.3 9.3
Sutorius. Magnificus 100 360 36 250 0.60 4.2

Notes:
a
(adult of body mass 60 kg; one mushroom meal of 100 g per day; RfD for Hg is 0.3 μg kg−1 body mass).
b
(adult body mass 60 kg; seven mushroom meals - each 100 g - per week; PTWI for inorganic Hg is 4 μg kg−1 body mass).

fresh or deep frozen mushrooms (Falandysz & Drewnowska, 2015 and,
2017; Svoboda, Kalač, Špička, & Janoušková, 2002).
3.3. Mercury intake with stir-fried mushrooms meals
There is no previous data available on intake of Hg from real meals
made of stir-fried mushrooms with high level of Hg background. The
statistical figures about consumption of wild growing mushrooms per
capita and frequency are rare for the countries and not mention about
the species (Zhang et al., 2010). In the groups of a high consumers, the
annual intake per capita can be 20–24 kg of fresh wild growing mush-
rooms in the Yi nationality region of the Sichuan province of China
(Zhang et al., 2008 and 2010) and up to 26 kg (median 0.75 kg and
mean = 1.76 kg) for the questionnaire respondents in the Great Britain
(Barnett et al., 1999).
A portion of 300 g of fresh whole mushrooms or caps is considered
as typical mushrooms meal (Falandysz et al., 2013), and what roughly
corresponds to around 150 g of stir-fried mushrooms. It seems reason-
able to assume that in the season of mushrooms foraging in south-west
Asia, the 100 g portion of tasty stir-fried mushrooms is a daily rate per
capita for certain people in a period of several weeks.
As can be noted from Table 3, the 100 g mushrooms meal eaten once
will provide from 16 to 82 μg of Hg, and in a course of a week from 110
to 570 μg of Hg. Those values expressed per kilogram of the body mass
(60 kg adult) are in the range respectively from 0.27 to 1.4 and from 1.9
to 9.6 μg. Thus, they contribute substantially to daily intake of Hg from
foods in the region.
The actual reference values for safe intake of inorganic Hg such as
the RfD (reference dose that has been set by the U.S. Environmental
Protection Agency) and the PTWI (provisionally tolerable weekly intake
that has been set by the World Health Organization) are respectively
0.3 μg kg−1 body mass (RfD) and 4.0 μg kg−1 body mass (PTWI) (US
EPA, 1987; WHO, 2018).
4. Conclusions
The stir-frying of foodstuffs with vegetable oil (high, moderate or
low) and with or without a short an initial blanching (parboiling) using
a wok is popular mode of cooking in south-west Asia, while there is no
data on its impact on status of minerals in cooked mushrooms that
naturally are rich in some metallic elements and metalloids. The stir-
fried mushrooms due to a substantial loss of water (partial dehydration)
in the course of cooking become enriched in Hg on produce (wet)
weight base. Results from this study confirmed that wild-growing
mushrooms (“boletes”) from the regions of south-west Asia can be
elevated in Hg and that stir-fried mushrooms meals can contribute
substantially to a daily intake of this element from foods there.
Acknowledgements
A study granted in part by National Natural Science Foundation of
China - project no. 21667031.
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