Journal of Food Composition and Analysis xxx (xxxx) xxxx

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Journal of Food Composition and Analysis

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Original Research Article

Determination of biogenic amines in processed and unprocessed mushrooms

from the Polish market
Ewa Jabłońska-Ryśa, Aneta Sławińskaa,*, Anna Stachniukb, Joanna Stadnikc
a
Department of Fruits, Vegetables and Mushrooms Technology, Faculty of Food Science and Biotechnology, University of Life Sciences in Lublin, Skromna 8, 20-704,
Lublin, Poland
b
Department of Pathophysiology, Medical University of Lublin, Jaczewskiego 8b, 20-090, Lublin, Poland
c
Department of Animal Raw Materials Technology, Faculty of Food Science and Biotechnology, University of Life Sciences in Lublin, Skromna 8, 20-704, Lublin, Poland

ARTICLE INFO ABSTRACT

Keywords: Mushrooms and mushroom products are very popular in many countries around the world. However, these food
Edible mushroom products can be a source of biogenic amines, due to the content of precursors of these compounds and the high
Processed mushroom susceptibility to microbiological spoilage. Biogenic amines have a significant impact on food quality and may
Biogenic amines pose a threat to human health. The presence of spermidine, putrescine, tyramine, cadaverine, histamine, sper-
Histamine
mine, and agmatine was determined for the first time in 53 processed and unprocessed mushroom products
Spermidine
Putrescine
available on the Polish market. The results showed a high variation in the content of biogenic amines in the
Tyramine individual products, depending on the producer. Spermidine and putrescine were the main biogenic amines, as
Cadaverine they were found in 47 and 39 types of mushroom products, respectively. Tyramine and cadaverine were found in
15 samples of processed mushrooms. Histamine was present in only eight samples of dried Polish forest
mushrooms; nevertheless, it was regarded a real threat to consumer health due to its very large quantities. It
should be noted that dried mushrooms are intermediate products used after hydration as ingredients of various
dishes, e.g. soups, sauces, stuffing; hence, the amount of histamine in the final product is substantially lower.

1. Introduction
Biogenic amines (BAs) are chemical compounds formed through
decarboxylation of amino acids or amination and transamination of
aldehydes and ketones. At the cellular level, these compounds serve
various important functions, e.g. they have an impact on protein
synthesis, DNA replication, and cell membrane permeability. They are
essential as factors for the growth, maintenance, and function of normal
cells. BAs are involved in male and female reproductive processes and
embryonic/foetal development (Cieślik and Migdał, 2011; Kalač,
2014). On the other hand, they may exert a negative effect on the or-
ganism. Large amounts of BAs supplied with food may produce several
physiological symptoms, such as nausea, respiratory distress, headache,
sweating, heart palpitations, and hyper- or hypotension (Feddern et al.,
2019; Kalač, 2014). These compounds can also react with nitrite to
form carcinogenic nitrosamines (EFSA, 2011; Wójciak et al., 2019). In
normal conditions, small amounts of dietary BAs are metabolised by
specific enzymes - monoamine oxydase (MAO) and diamine oxydase
(DAO) (Prester, 2011). However, when the detoxification ability is
disturbed, as in the case of patients administered with monoamino
oxidase inhibitor (MAOI) drugs, severe health problems may develop
(Doeun et al., 2017; EFSA, 2011). People with respiratory disorder,
heart problems, or vitamin B12 deficiency are at risk as well (Cardozo
et al., 2013).
In food, amines are produced with the involvement of bacterial
enzymes (decarboxylases), which transform amino acids into biogenic
amines. Therefore, amines are mainly detected in products undergoing
fermentation and maturation. Additionally, products with high contents
of protein and amino acids, i.e. BA precursors, are a source of these
compounds (Doeun et al., 2017; Feddern et al., 2019; Ruiz-Capillas and
Herrero, 2019). It has been found that the use of microbiologically
contaminated low-quality raw materials as well as improper food sto-
rage and processing conditions can contribute to an increase in the level
of BAs. The content of these compounds can serve as a marker of food
hygiene (EFSA, 2011; Simon-Sarkadi, 2019).
According to the EFSA (European Food Safety Authority), further
research on the toxicity and associated concentrations of biogenic
amines in different foods is needed (EFSA, 2011; Simon-Sarkadi, 2019).
During the past decade, the number of papers on BAs in food system-
atically increased (Papageorgiou et al., 2018; Simon-Sarkadi, 2019).

⁎
Corresponding author.
E-mail address: aneta.slawinska@up.lublin.pl (A. Sławińska).

https://doi.org/10.1016/j.jfca.2020.103492
Received 28 November 2019; Received in revised form 2 April 2020; Accepted 3 April 2020
0889-1575/ © 2020 Elsevier Inc. All rights reserved.

Please cite this article as: Ewa Jabłońska-Ryś, et al., Journal of Food Composition and Analysis, https://doi.org/10.1016/j.jfca.2020.103492
E. Jabłońska-Ryś, et al.
The greatest number of reports on BAs has been focused on fish and fish
products, dairy products, alcoholic beverages, and meat products (e.g.
Gustaw and Waśko, 2018; Jairath et al., 2015; Perin and Nero, 2020;
Prester, 2011). Only a few studies on BAs in mushrooms are available
(Cipolla et al., 2007; Dadáková et al., 2009; Hamana et al., 2005; Kalač
and Křížek, 1997; Lasota and Stefańczyk, 1980; Meng et al., 2019;
Nishibori et al., 2007; Nishimura et al., 2006; Okamoto et al., 1997;
Yamamoto et al., 1982), and they focused on unprocessed mushrooms.
The reported contents of amines differ significantly, e.g. the content of
spermidine, i.e. a fungal biogenic amine, in white button mushrooms
was estimated by Dadáková et al. (2009) at 604 mg kg–1 of dry matter,
which is equivalent to 43.45 mg kg–1 of fresh weight. In turn, Meng
et al. (2019) reported a value of approximately 30 mmol kg–1, i.e.
4357.5 mg kg–1of fresh weight. To date, to the best of our knowledge,
processed mushroom products have not been analysed for the content
of BAs.
Mushrooms are rich in protein, but perishable. They are prone to
microbiological spoilage, mainly because they have no cuticle to pro-
tect them from physical or microbial factors (Singh et al., 2010). Such
factors can potentially promote generation of BAs (EFSA, 2011). The
Polish market offers fresh cultivated mushrooms, primarily white and
brown button mushrooms as well as oyster and shiitake mushrooms and
various processed products from both cultivated and wild-growing
mushrooms. The high popularity of these products has prompted the
assessment of their quality and health safety related to the content of
biogenic amines.
In this context, the content of seven BAs (spermidine – SPD, pu-
trescine – PUT, tyramine – TYR, cadaverine – CAD, histamine – HIS,
spermine – SPM, and agmatine – AGM) in processed and unprocessed
mushrooms from the Polish market were analysed for the first time.
2. Materials and methods
2.1. Standards and chemicals
The BA standards (spermidine, putrescine, tyramine, cadaverine,
histamine, spermine, and agmatine), Na+/K + citric buffer and nin-
hydrin were supplied by Ingos, Prague, the Czech Republic.
Trichloroacetic acid (TCA) used for sample preparation was obtained
from Merck, Darmstadt, Germany.
2.2. Mushroom samples
Forty seven processed mushroom products and 6 unprocessed
mushrooms were purchased in Polish stores in June 2019. The pro-
cessed mushroom set consisted of pickled mushrooms (11 species, 13
producers), mushrooms in natural brine (1 species, 2 producers), dried
mushrooms (5 species, 6 producers), and other mushroom products (5
species, 3 producers). The raw material samples were composed of
three species of cultivated mushrooms that are most popular in Poland;
they were produced by three manufacturers. In total, 53 mushroom
samples of 13 different mushrooms species from 23 producers were
examined for the content of biogenic amines. Details are presented in
Table 1. Three packages of each product and three portions of un-
packaged mushrooms weighing approximately 1 kg each were pur-
chased. Canned and dried samples were kept in a dark place at 20 °C
and the frozen samples were stored at -20 °C until analysis (3–14 days).
Unprocessed mushroom samples were extracted immediately on the
day of purchase.
2.3. Sample preparation
BAs were extracted from the mushroom samples with the method
developed by Rabie et al. (2011) with some modifications. Three grams
of a sample was taken from each of the three unit packages of mush-
room products/portions of fresh mushrooms (n = 3). Next, the samples
2
Journal of Food Composition and Analysis xxx (xxxx) xxxx
were homogenized with 10 mL of 10% (w/v) trichloroacetic acid (TCA)
in a homogeniser (IKAT10 basic ULTRA-TURRAX, Staufen, Germany)
and shaken for 1 h in an orbital shaker (DragonLab, SK-330-Pro,
Beijing, China). The samples were centrifuged at 1957 g for 15 min at 4
°C (MPW-350R, Warsaw, Poland). Supernatants were kept at -20 °C for
1 h and centrifuged again in the same conditions. Purified extracts were
filtered through a 0.22 μm membrane filter (Alfachem, Poznań, Poland)
and stored at 4 °C until analysis.
2.4. Determination of the content of biogenic amines
The analysis of BAs was performed using an AAA500 amino acid
analyser (Ingos, Prague, Czech Republic) equipped with an Ostion LG
AAA8 ion-exchange column (3.6 × 100.8 μm). Separation was per-
formed by stepwise gradient elution using Na+/K + citric buffers.
Detection was carried out with spectrophotometry at 570 nm after post-
column derivatisation with ninhydrin. The operating parameters were
as follows: column temperature of 75 °C, eluent flow rate of 0.30 mL
min–1, reagent flow rate 0.20 mL min–1, reactor temperature of 120 °C,
and sample volume of 100 mL (Wójciak et al., 2019). Determination of
BAs was confirmed by comparing the retention times of the particular
biogenic amine standards with those of the components present in the
samples. BA concentrations were reported as mg kg–1 of mushroom
samples.
2.5. Statistical analysis
Statistical evaluation was carried out with Statistica v.13.1 (Statsoft,
Cracow, Poland). Three samples were used (one of each unit packet) for
each of the mushroom products or raw mushroom species and all the
measurements were done in triplicate. The results were expressed as the
mean ± SD (standard deviation). The data within each group of pro-
ducts (pickled mushrooms, mushrooms in natural marinade, dried
mushrooms) and for the raw mushrooms were assessed using one-way
analysis of variance with a level of significance set at P < 0.05. Tukey’s
test was carried out to compare the data.
3. Results
Spermidine was the most abundant BA determined in the mushroom
samples (Table 1). It was detected in 41 out of the 47 types of processed
products and in all raw material samples. The SPD content in the un-
processed samples of the white button mushrooms, which are the most
popular and most widely consumed mushrooms in Poland, ranged from
1686.58 to 2714.74 mg kg–1. Statistically significant differences in the
content of this compound were found, depending on the producer of the
white button mushrooms. The lowest SPD content in fresh mushrooms
was detected in the oyster mushroom samples (738.66 mg kg–1).
A large assortment of pickled mushrooms is available on the Polish
market. The presence of SPD was detected in most samples of these
products. This compound was found in all samples of the most popular
pickles, i.e. pickled white button mushrooms, chanterelles, and bay
boletes, in the range of 470.20–1129.35 mg kg–1, 21.67–268.77 mg
kg–1, and 28.19–735.40 mg kg–1, respectively. Statistically significant
differences were found in the content of this compound depending on
the marinade producer.
The largest amount of SPD was found in the dried mushroom
samples. The compound was detected in the dried products of all the
analysed mushroom species, and its content varied significantly de-
pending on the producer. The smallest amount of SPD was found in the
dried variegated boletes (389.48 mg kg–1), whereas the highest content
was detected in the dried bay boletes provided by producer I (30357.05
mg kg–1).
Putrescine was present in 39 samples (Table 1). In the unprocessed
material, small amounts of PUT were detected only in one of the three
tested samples of white button mushrooms. This amine was not present
E. Jabłońska-Ryś, et al. Journal of Food Composition and Analysis xxx (xxxx) xxxx

Table 1
Content of BAs in processed and unprocessed mushroom samples.
No. Code* Mushroom species Spermidine Putrescine Tyramine Cadaverine Histamine Spermine Agmatine

−1 −1 −1 −1 1 −1
mg kg SD mg kg SD mg kg SD mg kg SD mg kg− SD mg kg SD mg kg−1 SD

Pickled mushroom pasteurized

1 A/PL White button mushroom 1129.35l 42.0 462.04i 3.5 nd nd nd nd nd

2 B/PL Agaricus bisporus 846.18j 45.3 716.70j 33.9 nd 259.28e 23.3 nd nd nd
3 C/PL 1090.87k,l 28.7 nd nd nd nd nd nd
4 D/PL 904.60j 56.8 nd nd nd nd nd nd
5 E/PL 1002.03k 46.8 nd nd nd nd nd nd
6 F/PL 517.17h 32.1 nd nd nd nd nd nd
7 G/PL 470.20h 61.7 nd nd nd nd nd nd

8 H/PL Chanterelle 21.67a 1.0 nd nd nd nd nd nd

9 I/PL Cantharellus cibarius 168.94e 13.1 nd nd nd nd nd nd
10 J/PL 268.77g 21.7 31.32a,b 2.5 nd nd nd 30.95a 6.0 nd
11 B/PL 28.31a,b 1.6 27.60a 4.1 nd nd nd nd nd

12 J/PL Bay bolete 535.67h 23.4 84.06d 1.8 259.62c 13.0 38.11c 1.5 nd nd nd
13 I/PL Imleria badia 735.40i 1.6 348.62h 7.9 236.80c 15.1 21.16a,b 1.7 nd nd nd
14 H/PL 28.19a,b 1.6 26.04a 0.6 nd nd nd nd nd
15 F/PL 33.35b 4.5 36.18b 2.7 nd nd nd nd nd
16 K/PL 260.23g 6.5 278.87g 11.2 138.59b 13.1 26.82b 1.7 nd nd nd
17 B/PL 100.97d 9.6 48.83b,c 1.8 nd 15.07a 2.2 nd nd nd

18 H/PL Slippery jack nd 46.97b,c 2.1 nd nd nd nd nd

19 B/PL Suillus luteus nd 41.93b,c 1.6 nd nd nd nd nd
20 L/PL 193.77e,f 6.8 117.92e 2.4 nd nd nd nd nd

21 K/PL Weeping bolete nd 277.60g 7.8 nd nd nd nd nd

Suillus granulatus

22 I/PL Honey mushroom 24.26a 2.9 68.63c,d 4.1 nd nd nd nd nd

23 L/PL Armillaria mellea 178.44e,f 11.4 47.71b,c 0.5 nd nd nd nd nd

24 I/PL Red pine mushroom nd 63.37c,d 3.8 nd nd nd nd 219.83 41.7

Lactarius deliciosus

25 I/PL King bolete 871.30j 38.4 191.80f 7.4 324.26d 68.9 nd nd nd nd

26 B/PL Boletus edulis nd 42.19b,c 2.8 nd nd nd nd nd

27 M/PL Oyster 514.60h 57.2 46.02b,c 4.1 nd 65.40d 4.8 nd 21.14a 3.1 nd
Pleurotus ostreatus
28 M/PL Shiitake 447.24h 16.2 nd nd nd nd nd nd
Lentinula edodes

29 F/PL Jelly ear 62.02c 5.2 44.04b,c 1.7 63.36a 7.2 85.77d 5.5 nd nd nd
Auricularia auricula

Mushrooms in a natural marinade, sterilized

a
30 N/PL White button mushroom 247.53 13.8 141.65b 12.2 nd nd nd nd nd
31 O/NL Agaricus bisporus 264.87a 25.3 38.03a 3.0 nd nd nd 34.19 3.7 nd

Dried mushrooms

32 I/PL King bolete 14921.08f 330.4 9087.95e 49.3 nd 5338.94e 54.7 12451.59e 224.3 nd nd
33 R/PL Boletus edulis 6522.85c 79.0 10761.06f 359.4 nd 4813.22d 171.0 21126.94f 292.3 nd nd
34 K/PL 12529.16e 173.6 3606.24c 30.2 1624.60b 250.3 4650.85d 55.3 4152.33d 168.4 nd nd
35 P/PL 22601.23h 540.2 7327.60d 61.3 2928.06e 133.6 3863.94c 173.5 4205.37d 241.5 nd nd

36 P/PL Variegated bolete 389.48a 79.9 3429.32c 57.1 nd nd 1239.73a 30.3 nd nd

Suillus variegatus

37 I/PL Bay bolete 30357.05i 628.2 9074.25e 141.7 2557.65c-e 295.2 3793.11c 324.3 3297.48b,c 226.8 nd nd
38 R/PL Imleria badia 17615.2g 103.0 8630.64e 179.5 2886.59d,e 274.0 2280.73b 143.4 3889.54c,d 302.5 nd nd
39 P/PL 14503.65f 123.3 7141.98d 242.2 2458.74c-e 142.4 1349.17a 82.0 2972.77b 139.9 nd nd

40 S/CN Shiitake 10198.96d 173.0 nd 162.20a 17.2 nd nd nd nd

Lentinula edodes

41 T/CN Jelly ear 523.13a 92.3 437.11a 18.2 2320.12c 113.9 nd nd nd nd

42 S/CN Auricularia auricula 985.44b 96.0 719.14b 48.4 2375.12c,d 102.1 nd nd nd nd

Frozen mushrooms
(continued on next page)

3
E. Jabłońska-Ryś, et al. Journal of Food Composition and Analysis xxx (xxxx) xxxx

Table 1 (continued)

No. Code* Mushroom species Spermidine Putrescine Tyramine Cadaverine Histamine Spermine Agmatine

mg kg−1 SD mg kg−1 SD mg kg−1 SD mg kg−1 SD mg kg−1 SD mg kg−1 SD mg kg−1 SD

43 U/PL Chanterelle Cantharellus 197.00 21.1 61.29 4.8 nd nd nd nd nd

cibarius

Stewed mushrooms

44 I/PL Chanterelle Cantharellus 175.86 27.4 63.76 2.0 nd nd nd nd nd

cibarius

Mushrooms paste

45 I/PL Red pine mushroom nd 57.69 2.3 nd nd nd nd nd

Lactarius deliciosus

Fried forest mushrooms

46 K/PL Slippery jack Suillus 359.51 12.3 470.39 7.5 213.75 33.1 nd nd nd nd
luteus
Bay bolete Imleria badia

Forest mushrooms - concentrate

47 K/PL King bolete Boletus edulis 413.99 24.4 738.48 7.9 1794.00 17.8 212.73 10.5 nd nd nd
Slippery jack Suillus
luteus
Bay bolete Imleria badia

Raw mushrooms

48 X/PL White button mushroom 1686.58c 86.2 nd nd nd nd nd nd

49 Y/PL Agaricus bisporus 2714.74e 94.6 nd nd nd nd nd nd
50 Z/PL 2393.86d 168.3 53.37 1.3 nd nd nd nd nd

c
51 X/PL Brown button mushroom 1821.46 86.7 nd nd nd nd nd nd
Agaricus bisporus

52 X/PL Oyster 738.66a 27.9 nd nd nd nd nd nd

Pleurotus ostreatus

53 X/PL Shiitake 1238.59b 119.0 nd nd nd nd nd nd

Lentinula edodes

*Sample code, Factory/Country (PL-Poland, NL- Netherlands, CN-China); a–l Different superscripts indicate significant statistical differences (P < 0.05) according to
the Tukey’s test, within a specific product group (pickled mushrooms, mushrooms in a natural marinade, dried mushrooms, and raw mushrooms).

in brown button mushrooms and other species of unprocessed mush-
rooms.
PUT was detected in the dried products of all mushrooms with the
exception of shiitake. This compound was not detected in marinated
and unprocessed shiitake either. The dried Polish forest mushrooms
were characterised by substantially higher content of putrescine
(3429.32–10761.06 mg kg–1) than dried mushrooms from China
(437.11–719.14 mg kg–1). Statistically significant differences in the
content of this compound were found between the dried products, de-
pending on the producer.
No putrescine was found in eight of the 29 samples of pickled
mushrooms, i.e. pickled shiitake, white button mushrooms produced by
five different manufacturers, and pickled chanterelles supplied by two
producers. In this group of processed mushrooms, the highest amount
of PUT was detected in the marinated white button mushroom supplied
by producer B (716.70 mg kg–1). In the other marinated products, the
content of this compound was substantially lower with significant dif-
ferences, depending on the producer.
Among the other mushroom products, a high PUT level was de-
tected in the forest mushrooms concentrate (738.48 mg kg–1).
Tyramine and cadaverine were found in 15 processed mushroom
samples (Table 1). In the case of these compounds, the highest content
was determined in the dried mushroom samples. None of these com-
pounds was found in the dried variegated boletes, and CAD was not
found in the dried shiitake and jelly ear mushrooms. The content of TYR
and CAD in the dried samples of the same species of mushrooms was
significantly different, depending on the producer. The highest TIR
content was found in the dried king boletes from producer P (2928.06
mg kg–1), whereas this compound was not present in the dried product
of the same mushroom species from the other two other producers. The
highest CAD content in the dried mushrooms was observed in the king
bolete species (5338.94 mg kg–1). The content of both these compounds
in the other mushroom products was substantially lower. An exception
was the forest mushrooms concentrate, as this product contained
1794.00 mg kg–1 of TYR. The pickled mushrooms contained up to
324.26 and 259.28 mg kg–1 for TYR and CAD, respectively. TYR was
detected in the pickled bay boletes (in samples of 3 of the 6 producers),
king boletes (in a sample of 1 of the 2 producers), and jelly ear. In turn,
CAD was found in the pickled bay boletes (in samples of 4 of the 6
producers) as well as oyster, jelly ear, and white button mushrooms (in
sample of 1 of the 7 producers).
The sterilized mushrooms exhibited no content of TYR and CAD.
These BAs were not found in any of the raw mushroom samples, too.
Histamine was detected in only eight samples of processed

4
E. Jabłońska-Ryś, et al.
mushrooms (Table 1), i.e. in all samples of dried Polish forest mush-
rooms. This compound was found neither in the dried shiitake and jelly
ear mushrooms nor in the other types of processed and unprocessed
mushrooms. There was a significant difference in the levels of HIS
among the dried mushrooms, with the lowest level in the variegated
boletes (1239.73 mg kg–1) and the highest in the king boletes (21126.94
mg kg–1). There was also a significant variation in the dried mushroom
samples of the same species, depending on the producer.
Low levels of spermine were detected in three samples of processed
mushrooms, i.e. pickled oysters, pickled chanterelles, and sterilised
white button mushrooms in a natural marinade (21.14, 30.95, and
34.19 mg kg–1, respectively). Agmatine (219.83 mg kg–1) was found
only in pickled red pine mushrooms (Table 1).
4. Discussion
To our knowledge, we present the first study of the content of
biogenic amines in processed mushrooms. As shown in the Table 1, the
BA concentrations differ considerably between the mushroom products.
Spermidine and putrescine were the main biogenic amines. These
compounds are commonly present in mushrooms, as confirmed by in-
vestigations of unprocessed mushrooms. As mentioned in the In-
troduction, data from available sources on the content level of these
BAs vary widely, even within one species. In the case of white button
mushroom, the content of SPD ranges from 43.45 mg kg–1 of fresh
weight (Dadáková et al., 2009) to 4357.5 mg kg–1 of fresh weight
(Meng et al., 2019). In turn, the content of PUT is from 0.9 mg kg–1 of
fresh weight (Yamamoto et al., 1982) to approximately 1 mmol kg–1,
i.e. 88.15 mg kg–1 of fresh weight (Meng et al., 2019). Recent data have
been obtained in investigations of fresh mushrooms analysed im-
mediately after harvest. However, as demonstrated in the studies, sto-
rage of mushrooms at 4 °C for 7 days causes a tenfold increase in the
content of this compound. The content of SPD and SPM does not change
significantly during storage (Meng et al., 2019). As suggested by Kalač
and Křížek (1997), temperature has a significant impact on the increase
in the PUT and CAD content in stored white button mushroom. Fresh
samples and those stored for 48 h at 6 °C did not exhibit the presence of
these compounds. In samples stored at 20 °C, the levels of PUT and CAD
were 368 mg kg–1 of dry weight and 36.9 mg kg–1 of dry weight, re-
spectively. Yen (1992) also observed a significant increase in biogenic
amines, e.g. PUT, CAD, and HIS, in Volvariella volvacea mushrooms
stored at 4 and 25 °C for 5 days. As demonstrated by Doeun et al.
(2017), BAs can be produced by mesophilic bacteria especially at the
temperature ranging from 20 to 37 °C. For this reason, unprocessed and
thermally untreated mushrooms should be stored in refrigerated con-
ditions. All fresh mushrooms purchased for the analysis were stored at
room temperature in the shops. Nevertheless, the presence of PUT was
detected only in one of the three tested samples of white button
mushrooms, while CAD was not found in any fresh mushroom sample.
There are many factors affecting the content of BAs in mushrooms.
Dadáková et al. (2009) showed that the content of BAs in the fruiting
bodies of fungi depends on the morphological part of the fungus (stipe,
spore-forming parts, the rest of the cap). The considerably higher SPD
content in spore-forming parts as compared to stipes and the rest of the
caps is evident. The amine content also depends on different stages of
development of fruiting bodies. These authors claimed that the method
of handling mushroom fruit bodies is important, during both picking
and subsequent technological processing. Mechanical bruise on soft
mushroom tissues can accelerate the activity of decarboxylating bac-
teria.
The pickled white button mushrooms were found to contain sub-
stantially lower amounts of this compound than the unprocessed pro-
duct, i.e. in the range from 470.20 to 1129.35 mg kg–1, whereas the
sterilised product exhibited a level of SPD of 247.53–264.87 mg kg–1.
Thermal treatment such as cooking and pasteurisation can significantly
reduce the content of BAs in food (Doeun et al., 2017; Yen, 1992).
5
Journal of Food Composition and Analysis xxx (xxxx) xxxx
Nevertheless, some authors have reported no effects of the sterilisation
process on the level of these compounds (Cieślik and Migdał, 2011).
BAs are heat stable and will not be destroyed by cooking, baking, or
even canning (Feddern et al., 2019). Certainly, high-temperature pro-
cesses contribute to the reduction of the microflora involved in the
production of BAs (Doeun et al., 2017).
The largest amount of SPD was found in the dried mushroom
samples, which is associated primarily with the high concentration of
dry matter. Such a high level of BAs may also be caused by other fac-
tors, e.g. the quality and freshness of the unprocessed material and the
conditions of the drying process. Mushrooms are dried in a standard
temperature range from 40 to 70 °C and the initial temperature of
40–50 °C (Siwulski et al., 2007; Sławińska et al., 2017). In such con-
ditions, there may be increased synthesis of BAs in the initial drying
phase due to the high microbiological activity (Shalaby, 1996).
No TYR and CAD were found in any sample of the fresh mushrooms.
Mushrooms have not been tested for the content of tyramine so far. In
turn, the content of cadaverine in fresh mushrooms was analysed in
several studies. The content of this compound was 0.52 mg kg–1 of fresh
weight in white button mushroom (Cipolla et al., 2007), 0.6–2.5 mg
kg–1 of fresh weight in oyster mushrooms (Yamamoto et al., 1982),
1.5–7.77 mg kg–1 of fresh weight in shiitake mushrooms (Nishimura
et al., 2006; Yamamoto et al., 1982), and 4–9.4 mg kg–1 of fresh weight
in Boletus badius (Kalač and Křížek, 1997).
Tyramine was present in 5 samples of pickled mushrooms, 8 sam-
ples of dried mushrooms, fried forest mushrooms, and forest mushroom
concentrate. Cadaverine was detected in 7 samples of pickled mush-
rooms, 7 samples of dried mushrooms, and forest mushroom con-
centrate. As in the case of SPD and PUT, its highest levels were found in
the samples of dried mushrooms. In dried shiitake, which is a cultivated
mushroom, there was no CAD and the content of TYR was relatively
low, compared to the dried wild-growing mushrooms. It seems that the
content of biogenic amines may also depend on the source of mush-
rooms. Cultivated mushrooms grow on a sterile substrate, whereas
wild-growing mushrooms are naturally exposed to microflora.
Additionally, cultivated mushrooms are usually harvested at a strictly
defined stage of maturity and optimum quality, while the quality and
degree of maturity of mushrooms obtained from their natural habitat
are often highly diverse.
Histamine has not been detected in mushrooms so far, with the
exception of the study conducted by Lasota and Stefańczyk (1980), who
confirmed the presence of this compound in dried samples of edible
mushrooms Pleurotus ostreatus and Stropharia rugoso-annulata.
In the present study, HIS was detected in only eight samples of dried
Polish forest mushrooms. Such high levels of histamine may have arisen
in the initial stage of the drying process at the temperature of ap-
proximately 40 °C. The optimum temperature for histamine formation
is 37.8 °C (Cieślik and Migdał, 2011; Shalaby, 1996). This may be
confirmed by the fact that one of the producers of dried king boletes
and bay boletes (coded as I) produced pickles from the same species, in
which no histamine was detected. It can therefore be concluded that the
presence of this amine in processed mushrooms does not depend en-
tirely on the species but on the method of raw material processing. On
the other hand, better-quality raw material may have been used for the
production of the pickles, and worse quality material was sliced and
used for manufacture of the dried product.
As specified by the maximum allowable histamine content estab-
lished for fish and fish products, the level of this compound above 1000
mg kg–1 is regarded as toxic and dangerous for consumption (EFSA,
2011). It should be noted that dried mushrooms are intermediate pro-
ducts used after hydration as ingredients of various dishes, e.g. soups,
sauces, stuffing; hence, the amount of histamine in the final product is
substantially lower. However, these products may pose a potential
threat to the health of consumers.
In several studies, spermine and agmatine were analysed together
with SPD and PUT, as BAs characteristic for fungi. The SPM content in
E. Jabłońska-Ryś, et al.
the white button mushroom was below 3 mg kg–1 of fresh weight
(Cipolla et al., 2007; Dadáková et al., 2009; Yamamoto et al., 1982).
Only Meng et al. (2019) reported a substantially higher value of the
compound, i.e. below 1 mmol kg–1 of fresh weight, i.e. 202.34 mg kg–1
of fresh weight. In the case of oyster mushrooms, the SPM content
ranged from 0.7 to 10.12 mg kg–1 of fresh weight (Hamana et al., 2005;
Yamamoto et al., 1982), and the level of AGM was 74.21 mg kg–1 of
fresh weight (Hamana et al., 2005). Four studies conducted on shiitake
demonstrated no presence of SPM or AGM (Nishibori et al., 2007;
Nishimura et al., 2006; Okamoto et al., 1997; Yamamoto et al., 1982).
In the present study, SPM was found only in three and AGM in one
sample of processed mushrooms.
As demonstrated in the present study, mushrooms and their pro-
ducts, especially dried mushrooms, may contain very high amounts of
BAs. To date, fish and fish products have been regarded to pose the
highest risk related to the presence of BAs. Shalaby (1996) demon-
strated the highest amounts of BAs recorded in available literature for
selected foods. The largest amount of histamine was present in anchovy
paste (34 400 mg kg–1), putrescine in dry sausage (15 060 mg kg–1), and
cadaverine and tyramine in soy products (6340 mg kg–1 and 35 680 mg
kg–1, respectively).
Histamine and tyramine are regarded as the most toxic BAs. The
upper limit of histamine established for fish and fish products by the
Good Manufacturing Practice (GMP) is 100–200 mg kg–1 (Buňka et al.,
2013; COMMISSION REGULATION, 2005, 2013). Consumption of 50
mg histamine and 600 mg tyramine in food by a healthy person does
not induce any negative health effects, whereas such doses consumed
by patients with impaired metabolism or administered drugs from the
group of monoamine oxidase inhibitors (MAO) can result in serious
poisoning or even death (EFSA, 2011). Additional presence of pu-
trescine and cadaverine, which are not directly toxic, may contribute to
an increase in the toxicity of other amines, including histamine
(Madejska et al., 2017). The no-observed-adverse-effect level (NOAEL)
established for putrescine, spermidine and spermine is 180, 83, and 19
mg kg–1 body weight, respectively (Kalač, 2014). In this respect, fresh
and processed mushrooms available on the Polish market are safe for
the consumer, except for dried Polish forest mushrooms.
Mushrooms are a protein-rich raw material. They are perishable
food, which can determine the content of biogenic amines in raw ma-
terial and processed mushrooms. According to EFSA (2011), the current
control of the BA increase in food is based primarily on the assurance
and maintenance of hygienic quality of raw materials and production
process. Importantly, fresh high-quality mushrooms should be used for
processing immediately after harvest. In the mushroom drying process,
the use of high temperatures is recommended, as it reduces the mi-
croflora and the risk of BA formation. For the same reason, unprocessed
and thermally untreated mushrooms should be stored in refrigerated
conditions.
5. Conclusions
Unprocessed and processed mushrooms are a popular food product
available on the Polish market as a variety of products. These products
should be included in the category of foods that are potentially rich in
biogenic amines. Significant differences in the content of BAs in the
mushroom products have been demonstrated. Most of the products
have not been shown to contain these compounds in a quantity that
could threaten consumer's health and life. Only the dried forest mush-
rooms available on the Polish market contain considerable amounts of
histamine, which may pose a threat to consumer health. It should be
noted that patients with metabolic disorders or taking drugs from the
group of monoamine oxidase inhibitors (MAO) should limit the con-
sumption of mushroom products. It is advisable to monitor the content
of biogenic amines in fungi and mushroom products to ensure food
quality and safety.
6
Journal of Food Composition and Analysis xxx (xxxx) xxxx
Author contributions
Ewa Jabłońska-Ryś designed the research; Ewa Jabłońska-Ryś,
Aneta Sławińska and Joanna Stadnik performed the experiments and
interpreted data; Anna Stachniuk analysed the results statistically; Ewa
Jabłońska-Ryś wrote the paper. All authors discussed, edited and ap-
proved the final version.
All authors have approved the manuscript and concurred with
submission thereof to Journal of Food Composition and Analysis.
Funding
This work was supported by the subsidy of the Ministry of Science
and Higher Education in Poland for the maintenance and development
of research potential.
Declaration of Competing Interest
The authors declare that they have no financial or commercial
conflict of interest.
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