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Food Control
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Short communication
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
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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
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,
Kr
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; Kr
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
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
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
51
52
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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