Food Control 31 (2013) 49e52

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Food Control
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Short communication

Biogenic amines occurrence in sh meat sampled from restaurants in region

of Czech Republic

ka a, *, Pavel Budinsk b, Blanka Zimkov c, Marek Merhaut c, Radka Flasarov a,
Franti
sek Bun

a, Leona Bun

kov d
Vendula Pachlov a, Vlastimil Kubn
a

Department of Food Technology, Faculty of Technology, Tomas Bata University in Zlin, nam. T. G. Masaryka 5555, 76001 Zlin, Czech Republic
Faculty Hospital in Motol, V valu 84, 15006 Prague, Czech Republic
Department of Hotel Management, The Institute of Hospitality Management, Svdnick 506, 18100 Prague, Czech Republic
d
Department of Environmental Protection Engineering, Faculty of Technology, Tomas Bata University in Zlin, nam. T. G. Masaryka 5555, 76001 Zlin, Czech Republic
b
c

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 27 May 2012
Received in revised form
16 September 2012
Accepted 25 September 2012

The aim of the work was to monitor the content of 8 biogenic amines (histamine, tyramine,
phenylethylamine, tryptamine, putrescine, cadaverine, spermidine and spermine) in 112 samples of raw
freshwater and see sh, and other animals living in the water which are offered in restaurants in the
Czech Republic. In approx. 15% of the sampled bodies, increased levels of biogenic amines (practically
more than 100 mg/kg) have been observed. In 6 samples of sh, the concentration of histamine was
higher than the limit specied in Commission Regulation (EC) No 2073/2005 (more than 200 mg/kg). The
results pointed out the necessity of keeping the storage conditions (cooling and/or freezing chain) during
the distribution of products to consumers.
2012 Elsevier Ltd. All rights reserved.

Keywords:
Fish
Biogenic amines
Histamine
Restaurants
Health risk

1. Introduction
Biogenic amines (BAs) are aliphatic (putrescine, cadaverine),
aromatic (tyramine, 2-phenylethylamine) or heterocyclic (histamine, tryptamine) alkaline compounds formed in foodstuff mainly
by microbial decarboxylation. BA precursors are free amino acids
provided by proteolytic changes of proteins and/or peptides.
Histamine is formed from histidine, tyramine from tyrosine, phenylethylamine from phenylalanine, tryptamine from tryptophane,
cadaverine from lysine, and putrescine from arginine or ornitine.
Apart from BAs mentioned above, the concentrations of polyamines,
such as agmatine, spermine, and spermidine should be also
observed. Agmatine is formed from arginine, spermine and spermidine from putrescine (Halsz, Barth, Simon-Sarkadi, & Holzapfel,
1994; Shalaby, 1996; Silla Santos, 1996).
Contaminating bacteria from family Enterobacteriaceae (e.g.
some strains from genera Salmonella, Shigella, Escherichia, Serratia,
Yersinia, Morganella) and genera Pseudomonas are usually included
in groups of microorganisms possessing decarboxylase enzymes.

* Corresponding author. Tel.: 420 576 033 011; fax: 420 577 210 172.

ka).
E-mail address: bunka@ft.utb.cz (F. Bun
0956-7135/$ e see front matter 2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.foodcont.2012.09.044

BAs are produced also by some lactic acid bacteria (e.g. strains from
genera Lactobacillus, Enterococcus etc.). Lactic acid bacteria also
occur in some food as contaminants failing the quality and safety of
the product (e.g. in case of some meat products, beer, and wine).
Presence of particular decarboxylases is not specic within the
species and occurs only among certain number of strains in the

kov et al., 2009; Halsz et al., 1994; Shalaby, 1996;
species (Bun
Silla Santos, 1996).
BAs and polyamines are endogenous compounds with the key
functions in the metabolism of living organisms. Generally,
low concentrations of BAs in food and drink (practically under
100 mg/kg) do not represent a signicant risk for a healthy human.
Human intestinal tract has detoxifying system consisting of monoaminooxidase (MAO), diaminooxidase (DAO), and histamine
methyl-transpherase (HMT). However, higher amounts of BAs
(generally above 100 mg/kg) may induce undesirable psychoactive
and vasoactive effects (hypotension or hypertension, headache,
nausea, breathing problems etc.). Histamine and tyramine may
cause the latter mentioned undesirable effects directly. On the
other hand, putrescine and cadaverine act as potentiators of effects
of histamine or tyramine because putrescine and cadaverine could
inhibit the detoxifying enzymatic system (Arnold & Brown, 1978;

kov et al., 2009; Halsz et al., 1994; Ten Brink, Damink, Joosten,
Bun


ka et al. / Food Control 31 (2013) 49e52

F. Bun

50

& Huis int Veld, 1990). In Commission Regulation (EC) No. 2073
(2005), the concentration limit for histamine (100, resp. 200 mg/
kg) in sh and shery products (especially in sh species of families
Scombridae, Clupeidae, Engraulidae, Coryfenidae, Pomatomidae,
Scombresosidae) is established. Thereby, the importance of BAs
observation in these commodities is emphasized.
Fish and sh products are consumed insufciently in the region
of Middle Europe. Fish meat could be considered to be functional
food due to its nutritious characteristics (the high content of n-3
polyunsaturated fatty acids; high content of iron, zinc, and selenium; and simultaneously low content of sodium) (Dadkov,
K
r

zek, & Peliknov, 2009; Zhang et al., 2011; Zhang, Xaio,
Samaraweera, Lee, & Ahn, 2010). Nowadays, many common and/or
special restaurants offer wide group of sh and shery products.
Salmon, tuna, mackerel, striped catsh, trout or carp are often
consumed species of sh in Middle Europe. On the other hand, sh
meat represents the system with very short shelf-life because
postmortal changes are very fast. Therefore, the key requirements
for food-safety maintenance of sh meat are quick chilling or even
freezing and subsequently, keeping sh meat under desired
temperature (in whole chilling or freezing chain). In sh meat, BAs
may occur very often which correspond with fast postmortal
changes (Arnold & Brown, 1978; Jaw et al., 2012; K
r

zek, Vacha, &
Peliknov, 2011; Rawles, Flick, & Martin, 1996). Data of BAs
occurrence in sh meat in restaurants in the region of Middle Europe
have not been published in available literature. Only a few papers

dealing especially with modeling kinetics of BA production in model

sh systems have been found (e.g. K
r

zek et al., 2011).
The aim of this work was to monitor the content of 8 BAs
(histamine e HIM, tyramine e TYM, phenylethylamine e PHE,
tryptamine e TRM, putrescine e PUT, cadaverine e CAD, spermidine e SPD, spermine e SPN) in the sh meat offered in restaurants
in the Czech Republic.
2. Materials and methods
2.1. Samples
One hundred and twelve raw samples were analyzed (details are
shown in Table 1). Ninety-nine sh raw samples (10 freshwater
species and 16 sea sh species) were obtained in the years 2010 and
2011 from restaurants and sushi bars in the Czech Republic. One
cartilaginous sh sample (angler) and 12 other seafood (especially
calamari, prawn and squid) were also sampled. Individual samples
were stored frozen by the provider (at the temperature of 18  C
and lower; totally 53 samples) or they were stored on ice (at
the temperature of melting ice; totally 59 samples). Samples were
taken from commonly consumed parts of animal bodies. During the
transport to the laboratory, samples were kept in isothermal
containers (approx. 2 h); and immediately, they were lyophilized
(Christ Alpha 1e4). Lyophilized material was stored in 70  C until
the analysis.

Table 1
Biogenic amines content in sampled bodies of sh, cartilaginous and other seafood animals (mg/kg).
English name

Latin name

Na

Db

Alaska pollock
Angler (sea devil)
Atlantic bluen tuna
Atlantic cod
Atlantic mackerel
Atlantic pomfret
Atlantic salmon
Brown trout
Bullet tuna
Calamari
Common carp
Escolar (buttersh)
European craysh
European hake
European seabass
European spiny lobster
European squid
Fleshy prawn
Giant tiger prawn
Gilthead seabream
Grass carp
Greenland halibut
Hoki
Nile tilapia
Northern prawn
Pike perch
Pollock
Rainbow trout
Scallop
Striped catsh
Swordsh
Tench
Turbot
Wels catsh
Yellown tuna

Theragra chalcogramma
Lophius piscatorius
Thunnus thynnus
Gadus morhua
Scomber scombrus
Brama brama
Salmo salar
Salmo trutta
Auxis rochei
Sepioteuthis sp.
Cyprinus carpio
Lepidocybium avobrunneum
Astacus astacus
Merluccius merluccius
Dicentrarchus labrax
Palinurus vulgaris
Loligo vulgaris
Penaeus chinensis
Penaeus monodon
Sparus aurata
Ctenopharyngodon idella
Reinhardtius hippoglossoides
Macruronus sp.
Oreochromis niloticus
Pandalus borealis
Sander lucioperca
Pollachius virens
Oncorhynchus mykiss
Pecten jacobaeus
Pangasius hypophthalmus
Xiphias gladius
Tinca tinca
Psetta maxima
Silurus glanis
Thunnus albacares

5
1
1
13
1
1
20
5
1
2
7
3
1
7
3
1
1
1
2
1
1
3
1
1
2
2
1
1
2
16
1
1
1
1
1

S
O
S
S
S
S
F
F
S
O
F
S
O
S
S
O
O
O
O
S
F
S
S
F
O
F
S
F
O
F
S
F
S
F
S

Biogenic amines and polyamines content (ND/////)c

HIM

PUT

CAD

SPD

SPN

5/0/0/0/0/0
0/1/0/0/0/0
0/1/0/0/0/0
0/11/1/0/0/1
0/0/0/0/0/1
0/0/0/0/0/1
12/3/3/2/0/0
5/0/0/0/0/0
1/0/0/0/0/0
1/1/0/0/0/0
6/0/1/0/0/0
3/0/0/0/0/0
0/1/0/0/0/0
7/0/0/0/0/0
2/0/1/0/0/0
1/0/0/0/0/0
1/0/0/0/0/0
1/0/0/0/0/0
2/0/0/0/0/0
1/0/0/0/0/0
1/0/0/0/0/0
1/0/0/0/0/2
1/0/0/0/0/0
1/0/0/0/0/0
2/0/0/0/0/0
1/1/0/0/0/0
1/0/0/0/0/0
1/0/0/0/0/0
2/0/0/0/0/0
14/0/1/0/0/1
1/0/0/0/0/0
1/0/0/0/0/0
1/0/0/0/0/0
1/0/0/0/0/0
1/0/0/0/0/0

0/0/5/0/0/0
0/0/0/1/0/0
0/0/1/0/0/0
0/0/11/2/0/0
0/1/0/0/0/0
1/0/0/0/0/0
1/11/3/4/0/1
0/0/4/1/0/0
1/0/0/0/0/0
0/1/1/0/0/0
0/2/4/1/0/0
2/1/0/0/0/0
0/0/1/0/0/0
0/0/5/2/0/0
0/1/2/0/0/0
0/0/0/1/0/0
0/1/0/0/0/0
0/0/1/0/0/0
0/0/2/0/0/0
1/0/0/0/0/0
0/0/1/0/0/0
1/2/0/0/0/0
0/0/1/0/0/0
0/0/1/0/0/0
0/0/1/1/0/0
0/2/0/0/0/0
0/0/1/0/0/0
0/1/0/0/0/0
1/0/0/0/0/1
4/2/10/0/0/0
0/1/0/0/0/0
0/0/1/0/0/0
1/0/0/0/0/0
0/0/0/0/1/0
1/0/0/0/0/0

5/0/0/0/0/0
0/1/0/0/0/0
0/1/0/0/0/0
1/7/5/0/0/0
1/0/0/0/0/0
1/0/0/0/0/0
10/5/5/0/0/0
1/3/1/0/0/0
1/0/0/0/0/0
1/1/0/0/0/0
3/2/2/0/0/0
3/0/0/0/0/0
0/1/0/0/0/0
4/3/0/0/0/0
1/1/1/0/0/0
0/0/1/0/0/0
0/1/0/0/0/0
0/0/1/0/0/0
0/1/1/0/0/0
1/0/0/0/0/0
0/1/0/0/0/0
3/0/0/0/0/0
1/0/0/0/0/0
0/0/1/0/0/0
0/2/0/0/0/0
0/1/1/0/0/0
1/0/0/0/0/0
1/0/0/0/0/0
1/0/0/1/0/0
9/7/0/0/0/0
0/1/0/0/0/0
1/0/0/0/0/0
1/0/0/0/0/0
1/0/0/0/0/0
1/0/0/0/0/0

0/5/0/0/0/0
0/1/0/0/0/0
0/0/1/0/0/0
0/12/1/0/0/0
0/1/0/0/0/0
0/1/0/0/0/0
1/15/3/1/0/0
0/4/1/0/0/0
1/0/0/0/0/0
0/1/1/0/0/0
0/0/7/0/0/0
0/1/2/0/0/0
0/1/0/0/0/0
0/7/0/0/0/0
1/1/1/0/0/0
0/1/0/0/0/0
0/1/0/0/0/0
0/1/0/0/0/0
0/2/0/0/0/0
1/0/0/0/0/0
0/0/1/0/0/0
1/2/0/0/0/0
0/1/0/0/0/0
0/0/1/0/0/0
0/2/0/0/0/0
1/1/0/0/0/0
0/1/0/0/0/0
0/0/1/0/0/0
2/0/0/0/0/0
1/13/2/0/0/0
0/1/0/0/0/0
0/0/1/0/0/0
0/1/0/0/0/0
0/0/1/0/0/0
0/1/0/0/0/0

0/5/0/0/0/0
0/1/0/0/0/0
0/1/0/0/0/0
0/12/1/0/0/0
0/0/1/0/0/0
0/0/1/0/0/0
1/16/3/0/0/0
0/5/0/0/0/0
1/0/0/0/0/0
0/1/1/0/0/0
0/7/0/0/0/0
0/0/2/1/0/0
0/1/0/0/0/0
0/7/0/0/0/0
1/1/1/0/0/0
0/1/0/0/0/0
0/0/1/0/0/0
0/0/1/0/0/0
0/1/1/0/0/0
1/0/0/0/0/0
0/1/0/0/0/0
1/1/1/0/0/0
0/1/0/0/0/0
0/0/1/0/0/0
0/2/0/0/0/0
1/1/0/0/0/0
0/1/0/0/0/0
0/0/1/0/0/0
1/0/1/0/0/0
1/13/1/1/0/0
0/1/0/0/0/0
0/1/0/0/0/0
0/1/0/0/0/0
0/1/0/0/0/0
0/1/0/0/0/0

N e the number of samples in the certain species of freshwater or see sh or other water animals.
D e the group of samples: F e freshwater sh, S e see sh, O e other water animals.
The contents of biogenic amines were expressed using the magnitude: ND e not detected; <10 mg/kg; 10e50 mg/kg; 50e100 mg/kg;
100e200 mg/kg; >200 mg/kg.
b
c


ka et al. / Food Control 31 (2013) 49e52

F. Bun

51

2.2. Determination of biogenic amines content

Biogenic amines were extracted from the lyophilized matter
threefold with the use of 0.6 mol l1 perchloric acid. Content of 8
biogenic amines (HIM, TYM, PHE, TRM, PUT, CAD, SPD, SPN) was
determined by the method of high performance liquid chromatography (LabAlliance, State College, USA; Agilent Technologies, Agilent,
Paolo Alto, USA) after the preceding derivatization by dansylchloride. Derivatization, chromatographic separation (Cogent
column HPS C18, 150  4.6 mm, 5 mm, Cogent, Eatontown, USA) and
detection (spectrophotometrically l 254 nm) were performed

l, Pechov, Komprda,
according to Dadkov et al. (2009) and Sme

(2004). An example of chromatogram of a stanKlejdus, and Kubn
dard mixture of biogenic amines and chromatogram of extract from
a body of Atlantic salmon is shown in Fig. 1. Every sample was
extracted three times, every extract was derivatized twice and every
derivatized mixture was spread on the column (n 18) three times.
Results were expressed for the fresh matter before lyophilization.
Differences between biogenic amines concentrations in tested
bodies were statistically evaluated by KruskaleWallis and Wilcoxon tests. KruskaleWallis test was applied also for the analysis of
variance (the evaluation of effect of storage methods and samples
groups on BA occurrence). Statistical programme Unistat 5.5
(Unistat Ltd., London, UK) and the signicance level of 0.05 were
used for the tests.
3. Results and discussion
TRM was detected only in two sh samples (carp and pike
perch) in the amounts between 0.9 and 2.5 mg/kg (data not
shown). PHE was recorded in 13 sh samples (5 Atlantic cods, 4
Atlantic salmons, 2 Alaska pollocks and a sample of European hake
and striped catsh). In above mentioned cases, the concentrations
of PHE between 0.5 and 4.9 mg/kg were recorded (data not shown).
Silla Santos (1996) and Ten Brink et al. (1990) suggest (from point of
view of health risk) the limit for PHE income at the level of 30 mg/
kg. The latter mentioned limit was not exceeded in tested bodies.
Relatively low content of PHE (<4 mg/kg) in sh is presented also
by Hwang et al. (2012) and Zhai et al. (2012).
In 107 samples, TYM was not detected or the concentrations
ranged below 10 mg/kg (data not shown). Only in 5 bodies (4
Atlantic salmons and 1 carp), TYM concentrations between 10 and
50 mg/kg were recorded, which could be evaluated as safe for
healthy consumers (Halsz et al., 1994; Silla Santos, 1996; Ten Brink
et al., 1990). Low TYM content (practically < 50 mg/kg) in most of
the sh samples have been published by other authors (e.g. Hwang
et al., 2012; K
r

zek et al., 2011; Zhai et al., 2012).
HIM, PUT, CAD, SPD and SPN content determined in the samples
of bodies of freshwater and sea sh and other seafood are shown in
Table 1. The only controlled biogenic amine (by the national food
inspection authority) is HIM. HIM was not detected in 78 samples.
In 19 tested bodies, HIM concentrations below 10 mg/kg were
recorded. In other 9 cases, HIM concentrations of were below
100 mg/kg (P < 0.05) which is still considered as the safe limit for
a healthy human (Halsz et al., 1994; Silla Santos, 1996; Ten Brink
et al. 1990). On the other hand, in 6 bodies (two Greenland halibuts, and a sample of Atlantic mackerel, Atlantic cod, striped catsh
and Atlantic pomfret) the limit of 100 mg/kg was signicantly
exceeded (P < 0.05). Although the all latter mentioned sh samples
were stored at freezing temperatures (the sh bodies were obtained from six different restaurants), the concentrations reached
even the level above 1000 mg/kg (P < 0.05), which should be
considered as dangerous (Halsz et al., 1994; Silla Santos, 1996; Ten
Brink et al. 1990). These results emphasize the necessity of BAs
monitoring and evaluation of health risks.

Fig. 1. Separation of mixtures of biogenic amines as dansylamides. Part A: a standard

mixture (tryptamine, phenylethylamine, putrescine, cadaverine, histamine, ISTD e internal
standard e 1,7eheptandiamine, tyramine, spermidine and spermine) in concentration of
50 mg/l in acetonitrile. Part B: a derivatized sample extracted from the body of Atlantic
salmon.

PUT was the most abundant biogenic amine observed in our

samples (Table 1). Only in 14 cases, PUT was not detected. PUT
concentrations up to 10 mg/kg and between 10 and 100 mg/kg were
recorded in 26 and 69 samples, respectively. Three bodies (Atlantic
salmon, Wels catsh and scallop) possessed PUT concentration
>100 mg/kg (P < 0.05), which should be pointed out as serious.
In 92 bodies, CAD was not detected or the concentrations were
up to 10 mg/kg. More signicant CAD concentrations were
observed in 20 cases, where only once the amount exceeded the
level 50 mg/kg (P < 0.05). PUT and CAD could act as potentiators of
toxicological effects of HIM and TYM (Arnold & Brown, 1978; Halsz

52

ka et al. / Food Control 31 (2013) 49e52

F. Bun

et al., 1994; Prester, 2011; Silla Santos, 1996; Ten Brink et al. 1990).
The occurrence of PUT and CAD is usually related to the hygiene
conditions in the process of meat treatment and could point out to
the presence of contaminating microora, especially gramnegative
strains of family Enterobacteriaceae and genus Pseudomonas (Halsz
et al., 1994; Hwang et al., 2012; Rawles et al., 1996; Zhai et al., 2012).
In nearly 80% of samples, SPD and SPN concentrations were very
low (up to 10 mg/kg) or these polyamines were not detected. SPD
concentration ranging between 50 and 100 mg/kg was determined in
the only case of Atlantic salmon. In two sh samples (striped catsh
and escolar) SPN concentration above 50 mg/kg were observed.
Apart from the concentrations of individual BAs, the sum of
determined BAs amounts was also evaluated. In almost 85% of
tested samples, the sum of BAs was below 100 mg/kg. On the other
hand, in 7% of observed bodies, the BAs concentrations between
100 and 200 mg/kg were recorded. Surprisingly, in 8% of samples,
the BAs concentrations above 200 mg/kg and in 5% of bodies even
the amounts exceeded 1000 mg/kg. The latter mentioned concentrations represent amounts which could cause serious health
problems even for healthy consumers. Unfortunately, potentially
dangerous concentrations of BAs were also observed in sh bodies
which are widely served in restaurants in the Middle Europe (e.g.
Atlantic mackerel, Atlantic salmon and striped catsh).
Analysis of variance showed no signicant difference between
the samples stored frozen and on ice (P  0.05). Similarly, the BAs
concentration in freshwater and sea sh did not differ signicantly
(P  0.05). The BAs concentrations of the other seafood samples
were not signicantly higher in comparison with the bodies of
freshwater and sea sh (P  0.05).
4. Conclusion
Monitoring of the occurrence of 8 biogenic amines in the bodies
of 112 sh and other seafood obtained from restaurants in the Czech
Republic has been performed. In more than three quarters of
samples, the sum of concentrations of biogenic amines was under
100 mg/kg, which could be considered to be a safe limit for healthy
consumers. On the other hand, in 8% of tested samples, dangerous
amounts of BAs were found out and in 6 cases even legislatively set
limits were exceeded. Although sh and sh products should be
a part of human diet, it is important to deal with their short shelf-life
which could be determined also by biogenic amines concentrations.

Acknowledgment
The nancial support from the Grant Agency of the Czech

503/11/1417) and Internal Grant of TBU in
Republic (Grant No. GACR
Zlin (No. IGA/FT/2012/027) is greatly acknowledged.
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