You are on page 1of 8

Food Chemistry 239 (2018) 377–384

Contents lists available at ScienceDirect

Food Chemistry
journal homepage: www.elsevier.com/locate/foodchem

A study of the tyramine/glucose Maillard reaction: Variables,


characterization, cytotoxicity and preliminary application
Wei Jiang a, Yaxin Chen b, Xiaoxia He c, Shiwei Hu a, Shijie Li a, Yu Liu a,⇑
a
Laboratory of Seafood Processing, Innovative and Application Institute, Zhejiang Ocean University, Zhoushan, Zhejiang 316022, China
b
College of Food Science and Pharmacy, Zhejiang Ocean University, Zhoushan, Zhejiang 316022, China
c
Qingdao Entry-Exit Inspection and Quarantine Bureau, Qingdao, Shandong 266002, China

a r t i c l e i n f o a b s t r a c t

Article history: The tyramine/glucose Maillard reaction was proposed as an emerging tool for tyramine reduction in a
Received 8 March 2017 model system and two commercial soy sauce samples. The model system was composed of tyramine
Received in revised form 14 May 2017 and glucose in buffer solutions with or without NaCl. The results showed that tyramine was reduced
Accepted 14 June 2017
in the model system, and the reduction rate was affected by temperature, heating time, initial pH value,
Available online 20 June 2017
NaCl concentration, initial glucose concentration and initial tyramine concentration. Changes in fluores-
cence intensity and ultraviolet–visible (UV–vis) absorption spectra showed three stages of the Maillard
Chemical compounds studied in this article:
reaction between tyramine and glucose. Cytotoxicity assay demonstrated that tyramine/glucose
Tyramine (PubChem CID: 5610)
Glucose (PubChem CID: 5793)
Maillard reaction products (MRPs) were significantly less toxic than that of tyramine (p < 0.05).
Dansyl chloride (PubChem CID: 11801) Moreover, tyramine concentration in soy sauce samples was significantly reduced when heated with
Dimethyl sulfoxide (PubChem CID: 679) the addition of glucose (p < 0.05). Experimental results showed that the tyramine/glucose Maillard reac-
Sodium chloride (PubChem CID: 5234) tion is a promising method for tyramine reduction in foods.
Methanol (PubChem CID: 887) Ó 2017 Elsevier Ltd. All rights reserved.
Streptomycin (PubChem CID: 19649)
Ampicillin (PubChem CID: 6249)

Keywords:
Tyramine
Biogenic amine
Glucose
Maillard reaction
Reduction
Cytotoxicity
Soy sauce

1. Introduction due to the presence of amine oxidases in the human intestine. Nev-
ertheless, consumption of foods containing high level of tyramine
Tyramine, (4-(2-aminoethyl) phenol), is a biogenic amine causes migraine, neurological disorders, headaches, respiratory
derived from the decarboxylation of amino acid tyrosine by bacte- disorders and hypertension, which are together known as the
ria. As shown in Fig. 1, tyramine is an aromatic monoamine com- ‘‘cheese effect” (Finberg & Gillman, 2011). These symptoms can
pound. Tyramine can accumulate in a wide range of foods, be much more severe in people taking antidepressant monoamine
especially fermented foods, such as cheese, fish sauce and soy oxidase inhibitor medication (Ladero, Calles-Enriquez, Fernandez,
sauce (Guidi & Gloria, 2012; Jiang, Xu, Li, Dong, & Wang, 2014; & Alvarez, 2010). Besides, tyramine can react with nitrite to form
Linares, Martín, Ladero, Alvarez, & Fernández, 2011). A low level C-nitroso compounds, which are known carcinogenic agents (Gon
of tyramine does not cause harmful effects in normal individuals zález-Jiménez, Arenas-Valgañón, García-Santos, Calle, & Casado,
2017). Recent studies suggest that tyramine exhibits a stronger
Abbreviations: UV–vis, ultraviolet–visible; MRPs, Maillard reaction products; and more rapid cytotoxic effect than histamine (Linares et al.,
RPMI, Roswell Park Memorial Institute; FBS, fetal bovine serum; DMSO, dimethyl
2016). Therefore, the prevention of tyramine formation in foods
sulfoxide; 5-HMF, 5-hydroxymethlofurfural; AGEs, advanced glycation end prod-
ucts; Has, heterocyclic amines; MTT, 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenylte or reduction of its level once it has formed should be studied.
trazolium bromide. In the past few decades, high hydrostatic pressure (Matějková,
⇑ Corresponding author. Křížek, Vácha, & Dadáková, 2013), irradiation (Zhang, Wang,
E-mail address: liuyu1987@zjou.edu.cn (Y. Liu).

http://dx.doi.org/10.1016/j.foodchem.2017.06.085
0308-8146/Ó 2017 Elsevier Ltd. All rights reserved.
378 W. Jiang et al. / Food Chemistry 239 (2018) 377–384

HO Park Memorial Institute (RPMI) 1640 medium, fetal bovine serum


(FBS), streptomycin sulphate, ampicillin, trypsin and 3-(4,5-dime
thylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) were
obtained from Gibco Invitrogen Co., (Burlington, ON, Canada). Glu-
cose was obtained from Solarbio Inc. (Beijing, China). Methanol
NH2 (HPLC grade) was supplied by Merck (Darmstadt, Germany). Ultra-
pure water was prepared by Milli-Q (Millipore, Billerica, MA, USA).
Fig. 1. Structure of tyramine. The other chemicals used were of analytical grade and obtained
from Sinopharm Chemical Regent Co. Ltd (Shanghai, China).
Zhang, Wang, & Ye, 2016), modified atmosphere packing
(Yassoralipour, Bakar, Rahman, & Abu Bakar, 2012) and low storage
2.2. Tyramine/glucose Maillard reaction model system
temperature (Fan et al., 2016) have been employed to prevent the
formation of tyramine by inhibiting the growth of microorganisms.
Tyramine was incubated with glucose in 16 mm  155 mm
Nevertheless, microbial inhibition by these methods is random, not
glass screw tubes capped with a tight screw-cap. Unless otherwise
only aiming at tyramine producing bacteria. Thus, they are not
stated, the incubations contained 50 mM potassium phosphate, pH
suitable for fermented foods where the growth of microorganisms
8.0, 2.5 mM tyramine and 40 mM glucose in a total volume of
is very important. Moreover, the above techniques cannot decrease
5.0 ml. The tubes were incubated at designed temperature in a Dig-
the level of tyramine that already exists. Tyramine degrading bac-
ital Dry Bath (Jinxin, JX100-4, Shanghai, China). To ensure the reac-
teria can be used as functional starter cultures to reduce already
tion was stopped at appropriate time points, the tubes were cooled
existing tyramine (Xu, Liu, Xu, Wang, & Jiang, 2016), but more
in a mixture of ice and water for 30 min.
effective tyramine degrading strains and professional equipment/
staff are required. Therefore, high efficiency, lower cost and more
2.3. Variables of the tyramine/glucose Maillard reaction model system
convenient methods are desired for tyramine reduction.
The Maillard reaction occurs between the amino group of amino
2.3.1. Temperature
acids, peptides, proteins or other nitrogen containing compounds
To evaluate the effect of temperature on the tyramine reduction
and carbonyl groups of reducing sugars, during the processing
rate, 2.5 mM tyramine and 40 mM glucose were incubated at pH
and storing of foods. This reaction is a series of successive and par-
8.0 and 60, 70, 80, 90, 100 or 110 °C for 12 h without the addition
allel reactions, which can be influenced by many factors such as
of NaCl. Samples were taken at 0, 0.5, 1, 1.5, 2, 2.5, 3, 4, 6, 8, 10 and
temperature, heating time, pH, substrate type, substrate concen-
12 h.
tration and water activity (Caballero, Finglas, & Toldrá, 2016). To
reduce the complexity of the Maillard reaction, the reaction pro-
2.3.2. Initial pH
cess is divided into three stages (namely initial stage, intermediate
To evaluate the effect of initial pH value on the tyramine reduc-
stage and final stage) according to the generation of different com-
tion rate, 2.5 mM tyramine and 40 mM glucose were incubated at
pounds, which can be characterized by fluorescence intensity and
100 °C and pH 5.0, 6.0, 7.0, 8.0, 9.0, 10.0, 11.0 or 12.0 for 5 h with-
ultraviolet–visible (UV–vis) absorption (Nursten, 2005). Although
out the addition of NaCl. Samples were taken at 0.5, 1, 3 and 5 h.
the Maillard reaction can result in the loss of essential amino acids,
production of undesired pigment and generation of toxicants
2.3.3. NaCl concentration
(Zhang, Tao, Wang, Chen, & Wang, 2015), it can also enhance the
To evaluate the effect of NaCl concentration on the tyramine
emulsifying property, solubility, antioxidant activity and metal
reduction rate, 2.5 mM tyramine and 40 mM glucose were incu-
chelating activity of food ingredients (Dong et al., 2012; Oliveira,
bated at 100 °C and pH 8.0 with 0, 1, 3, 5, 8, 11, 14, 19, 24 or
Coimbra, Oliveira, Zuñiga, & Rojas, 2016). The Maillard reaction
29% (w/v) of NaCl for 5 h. Samples were taken at 0.5, 1, 3 and 5 h.
has also been used to reduce fumonisin B1 in corn grits
(Bullerman et al., 2008), which expands the application area of
2.3.4. Initial glucose concentration
Maillard reaction to the reduction of toxic substances. As shown
To evaluate the effect of initial glucose concentration on the
in Fig. 1, tyramine has a free amino group, suggesting that it may
tyramine reduction rate, different initial glucose concentrations
be reduced by Maillard reaction. However, the Maillard reaction
of 5, 10, 20, 40, 60, 80, 160 or 320 mM glucose and 2.5 mM tyra-
between tyramine and sugars has not been studied previously.
mine were incubated at 100 °C and pH 8.0 for 5 h without the addi-
In this study, effects of temperature, heating time, initial pH
tion of NaCl. Samples were taken at 0.5, 1, 3 and 5 h.
value, NaCl concentration, initial glucose concentration and initial
tyramine concentration on tyramine reduction in the tyramine/
2.3.5. Initial tyramine concentration
glucose Maillard reaction model system were investigated. Three
To evaluate the effect of initial tyramine concentration on the
stages of the tyramine/glucose Maillard reaction were character-
tyramine reduction rate, different initial tyramine concentrations
ized by fluorescence intensity and UV–vis spectroscopy. Cytotoxi-
of 0.5, 1.0, 2.5, 5.0, 10.0 or 20.0 mM tyramine and 40 mM glucose
city of tyramine, glucose, tyramine-glucose mixture, and
were incubated at 100 °C and pH 8.0 for 5 h without the addition
tyramine/glucose Maillard reaction products (MRPs) was assayed.
of NaCl. Samples were taken at 0.5, 1, 3 and 5 h.
Furthermore, the reduction of tyramine by Maillard reaction in
commercial soy sauce samples was preliminarily evaluated. The
2.4. Tyramine concentration determination
aim was to reveal the possibility of using tyramine/glucose Mail-
lard reaction for tyramine reduction in foods.
Tyramine concentration was determined by HPLC using pre-
column derivatization with dansyl chloride (Jiang et al., 2014).
2. Materials and methods The HPLC system consisted of a Waters 2695 series (Milford,
USA) equipped with a degasser, quaternary pump, column oven,
2.1. Chemicals fluorescence detector and automatic sampler. A reversed-phase
chromatographic column (Capcell PAK 5 lm C18 MG,
Tyramine, dansyl chloride and dimethyl sulfoxide (DMSO) were 150  4.6 mm) was used. The derivatised tyramine was detected
obtained from Sigma-Aldrich, Inc. (St. Louis, MO, USA). Roswell at 350 nm (excitation) and 520 nm (emission). Calibration curves
W. Jiang et al. / Food Chemistry 239 (2018) 377–384 379

were constructed of peak area vs standard tyramine concentration 2.9. Incubation of soy sauce with glucose
(0.01–2.5 mM).
To evaluate the tyramine reduction ability of Maillard reaction
2.5. Fluorescence intensity in foods, two commercial soy sauce samples obtained from a mar-
ket in Zhoushan, Zhejiang, China, and were incubated with glucose
Fluorescence intensities were determined using a fluorescence under designed conditions. The salt concentrations of sample A and
spectrophotometer (Hitachi, F-4500, Kyoto, Japan) using the sample B were measured as 11.28 ± 0.79% (w/v) and 16.12 ± 1.04%
method described previously (Morales & Jiménez-Pérez, 2001). (w/v), respectively. The pH values of sample A and sample B were
Samples were diluted 10-fold with ultrapure water. The fluores- measured as 6.21 ± 0.14 and 5.98 ± 0.09, respectively. Sample A
cence intensities were measured at an excitation wavelength of was manufactured using water, white sugar, salt, soybean, wheat
350 nm and an emission wavelength of 420 nm. flour, yeast extract, lactic acid, caramel and potassium sorbate,
while sample B was produced using water, white sugar, salt, soy-
bean, wheat, yeast extract, sodium glutamate, sucralose and
2.6. UV–vis spectroscopy
sodium benzoate. The obtained soy sauce samples were opened
and their net volumes were measured. Then 2% (w/v) glucose (equal
UV–vis spectra were determined using an UV–vis spectropho-
to 125 mM glucose) was added and mixed gently. The mixture was
tometer (Shimadzu, UV-2600, Kyoto, Japan). Samples were diluted
transferred to a sealable glass container. After that, the container
to 50-fold with ultrapure water. UV–vis spectra were recorded
was incubated in a water bath at 95 °C. Samples were taken at
from 220 to 800 nm with an interval of 0.5 nm. Meanwhile, the
the heating time of 0, 1, 2 and 3 h. The same samples without the
absorbance at 294 and 420 nm was measured.
addition of glucose were incubated under the same conditions.

2.7. Cell culture 2.10. Tyramine extraction

The normal human liver HL-7702 cell line (BNCC 100966) was Tyramine was extracted from soy sauce by a reported method
obtained from BeNa Culture Collection Co. Ltd. (Beijing, China). (Yongmei et al., 2009) with some modifications. Two milliliters of
Cells were maintained in RPMI 1640 medium containing 10% soy sauce were placed into a centrifuge tube containing 3 ml of
(v/v) FBS, 0.01% (w/v) ampicillin and 0.05% (w/v) streptomycin at 400 mM perchloric acid. The tubes were mixed for 70 s by a vortex
37 °C under a humidified atmosphere containing 5% CO2. mixer (IKA, MS3, Staufen, German) and centrifuged at 1  104 g at
0 °C for 3 min using a refrigerated centrifuge (Zhongke, HC-
2.8. Cytotoxicity assay 3018R, Anhui, China). The supernatant was filtered through qualita-
tive paper. The acid extraction steps were repeated twice again. The
Cytotoxicity of tyramine, glucose, tyramine-glucose mixture filtrates were all transferred into a calibrated volumetric flask and
and tyramine/glucose Maillard reaction products (MRPs) was eval- diluted with 0.4 M perchloric to 10 ml. The diluted solution was
uated by the MTT assay using HL-7702 cells. Briefly, cells were used for the determination of tyramine concentration in soy sauce.
seeded into a 96-well plate at density of 5  103 cells per well with
100 ll of RPMI 1640 medium containing 10% (v/v) FBS, 0.01% (w/v) 2.11. Statistical analyses
ampicillin and 0.05% (w/v) streptomycin. After incubation for 24 h
at 37 °C under a humidified atmosphere containing 5% CO2, 100 ll Statistical analyses were performed using the software IBM
of culture medium containing different test substances as shown in SPSS Statistics 22.0 (IBM, USA). Data were analyzed by one-way
Table 1 were added to the wells of experiment groups, and 100 ll analysis of variance (ANOVA) with the Tukey test. The experiments
of culture medium were added to the wells of the negative control were performed in triplicate and the data were expressed as aver-
group. The cells were subsequently cultured for 24 h at 37 °C under age ± standard deviation.
a humidified atmosphere containing 5% CO2. After that, 10 ll of
MTT solution (5 mg/ml) was added to each well and the plate 3. Results and discussion
was incubated for another 4 h. After careful removal of the super-
natant, 100 ll of DMSO was added to each well and the plate was 3.1. Variables influencing tyramine reduction rates in the tyramine/
shaken at room temperature for 20 min. The absorbance at 490 nm glucose Maillard reaction model system
was measured in a microplate reader (PULANG, DNM-9606, Bei-
jing, China). The cell growth inhibition rate was calculated using 3.1.1. Effect of temperature and heating time on tyramine reduction
the following formula: Cell growth inhibition rate (%) = (Absor- rates
bance value of control Absorbance value of sample)/Absorbance Fig. 2A shows the changes of tyramine reduction rates in the
value of control  100. tyramine/glucose Maillard reaction model system during heating

Table 1
Experimental design for cytotoxicity assay.

Levels Concentration (mM)


Tyramine Glucose MixtureA MRPs-1B MRPs-5B
1 2 32 34 34 34
2 4 64 68 68 68
3 6 96 102 102 102
4 8 128 136 136 136
5 10 160 170 170 170
A
The mixture was prepared by freeze-drying the mixture of 2.5 mM tyramine and 40 mM glucose in 50 mM PBS (pH 8.0).
B
The MRPs were prepared by freeze-drying the reaction products of 2.5 mM tyramine and 40 mM glucose after heating at 100 °C for 1 h (MRPs-1) or 5 h (MRPs-5) in
50 mM PBS (pH 8.0).
380 W. Jiang et al. / Food Chemistry 239 (2018) 377–384

160
A
Equation y = a + b*x (from 0 to 1.5 h)

C
b Equation
Temperature
Value Standard Error Residual Sum of Squares Pearson's r Adj. R-Square
140 60°C 5.33755 0.65174 2.79575 0.97836 0.94292
70°C 8.56659 0.37513 0.76365 0.99714 0.99237

Tyramine reduction rate (%)


80°C 11.24973 0.81391 28.99032 0.96314 0.90353
90°C 24.24657 4.0698 49.74058 0.96024 0.89609
120 100°C 34.00309 4.39051 52.26173 0.97589 0.93649
110°C 52.10133 4.80891 50.55998 0.98746 0.96677

100

80

60

40

20

0 1 2 3 4 5 6 7 8 9 10 11 12
Heating time (h)

100 B ef f C
Tyramine reduction rate (%)

f 100
e
Tyramine reduction rate (%)

ef
e
d de d
80 g 80
de g e ded cd
d f
c f de
60 e 60 c
c
e
c c c
de c bc
d
40 d 40 d c bc b ab
b bc b ab
b c cd b b
c b b a
c bc
a bc ab ab
20 b 20 b ab a a
a b a a a
ab a a
aa
0 0
5 6 7 8 9 10 11 12 0 1 3 5 8 11 14 19 24 29
Initial pH NaCl concentration (%)

100 D g
g
100 E f
f
e
Tyramine reduction rate (%)

Tyramine reduction rate (%)

f f
ef
f d
80 80 f
h c
e e d
d d e
60 d g 60
c e b
c
ef f e d d a
e b
b c de
40 40 c
b d c a
c cd
a c b
a b b a
20 b 20 ab
a ab
a a

0 0
5 10 20 40 60 80 160 320 0.5 1 2.5 5 10 20
Glucose concentration (mM) Tyramine concentration (mM)

Fig. 2. (A) Effect of temperature on tyramine reduction rate in the tyramine/glucose Maillard reaction model for up to 12 h. Temperature: 60 °C ( ), 70 °C ( ), 80 °C ( ),
90 °C ( ), 100 °C ( ), 110 °C ( ). Tyramine heated alone at pH 8.0 and 110 °C was also studied ( ). The inserted table showed the parameters of the liner fitting equation
(y = a + b * x) from 0 to 1.5 h at different temperatures. The slope value represented the mean tyramine reduction rate per hour (%/h, mean ± SD) from 0 to 1.5 h. Effect of (B)
initial pH value, (C) NaCl concentration, (D) initial glucose concentration and (E) initial tyramine concentration on tyramine reduction rates in the tyramine/glucose Maillard
reaction model system after heating for 0.5 h ( ), 1 h ( ), 3 h ( ) and 5 h ( ). Bars of the same color (the same reaction time) with different letters are significantly
different (p < 0.05). Reaction conditions: (A) 2.5 mM tyramine and 40 mM glucose at pH 8.0 and different temperatures; (B) 2.5 mM tyramine and 40 mM glucose at 100 °C
and different initial pH values; (C) 2.5 mM tyramine and 40 mM glucose at 100 °C and pH 8.0 with the addition of different concentration of NaCl; (D) 2.5 mM tyramine and
different initial concentration of glucose at 100 °C and pH 8.0; (E) 40 mM glucose and different initial concentration of tyramine at 100 °C and pH 8.0.
W. Jiang et al. / Food Chemistry 239 (2018) 377–384 381

at different temperature (from 60 to 110 °C) and in tyramine solu- Matthey-Doret, & Robert, 2003) and lysine/fructose (Ajandouz &
tion during heating at 110 °C for 12 h. It was observed that the Tchiakpe, 2001) Maillard reaction systems. The inhibition of tyra-
tyramine concentration did not change significantly when heated mine reduction in acidic solution might be explained by the proto-
alone without glucose at 110 °C for 12 h, exhibiting its thermosta- nation of tyramine, which resulted in hindering the condensation
bility. However, the tyramine reduction rate was strongly affected of amino with carbonyl group and thus reducing the consumption
by temperature (from 60 to 110 °C) and heating time (from 0 to of tyramine (Liu, Yang, Chen, Chen, & Chen, 2011). Besides, reaction
12 h) when 2.5 mM tyramine and 40 mM glucose reacted at pH 8.0. rate could be slowed down by the fact that the pH value always
As shown in Fig. 2A, on the one hand, the tyramine reduction decreased in the process of Maillard reaction (Cai et al., 2016;
rate increased in the tyramine/glucose Maillard reaction model Liu, Yang, Jin, Hsu, & Chen, 2008), which was attributed to the con-
system as the reaction time was prolonged. It also can be seen that sumption of the basic amino group and the formation of acidic
the tyramine reaction rate increased sharply during the first few MRPs. Furthermore, it was reported that the activation energy
hours and rose slowly afterward. For example, when reacted at decreased as the system pH increased in glucose/bovine serum
80 °C, the tyramine reduction rate increased from 0 to albumin and glucose/casein Maillard reaction systems (El Hassan
29.33 ± 2.22% in the first four hours but further increased to only Ajandouz et al., 2008), indicating that the Maillard action occurred
46.88 ± 1.79% in the next eight hours. On the other hand, the tyra- more easily at a higher pH value.
mine reduction rate increased in the tyramine/glucose Maillard
reaction model system as temperature increased from 60 to 3.1.3. Effect of NaCl concentration on tyramine reduction rates
110 °C. The tyramine reduction rates were 20.55 ± 4.69, As tyramine has always existed in fermented foods with high
32.50 ± 1.11, 46.88 ± 1.79, 76.50 ± 2.03, 93.00 ± 1.89 and salt content (Yongmei et al., 2009), effect of NaCl concentrations
97.93 ± 1.89% when 2.5 mM tyramine and 40 mM glucose reacted on tyramine reduction rates in the tyramine/glucose Maillard reac-
for 12 h at 60, 70, 80, 90, 100 and 110 °C, respectively. The table tion model system during heating at 100 °C and pH 8.0 for 5 h was
inserted in Fig. 2A shows the parameters of the liner fitting equa- investigated. As shown in Fig. 2C, the tyramine/glucose Maillard
tion between tyramine reduction rate and time (0–1.5 h). The slope reaction was inhibited by the addition of NaCl. After heating at
value represented the initial tyramine reduction rate per hour, 100 °C and pH 8.0 for 5 h, the tyramine reduction rate was
which increased as temperature increased from 60 to 110 °C. The significantly decreased from 77.41 ± 3.22% without NaCl to
initial tyramine reduction rate per hour was only 5.34 ± 0.654%/h 22.54 ± 4.12% with 29.0% of NaCl (p < 0.05). Similar trends were
at 60 °C, but which increased by nearly 10 times (52.10 ± 4.81%/ also observed at 0.5, 1, and 3 h, indicating that the tyramine reduc-
h) if the temperature was 110 °C. These results indicated that tyra- tion rate was inhibited in foods with high content of salt.
mine was thermostable, but could be reduced with the addition of Effect of NaCl addition on the Maillard reaction was also studied
glucose during heating in model system. previously. Thongraung and Kangsanan (2010) found that the addi-
As the Maillard reaction is endothermic, the extent of reaction tion of 0.5–2.5% NaCl inhibited the Maillard reaction between fruc-
in a certain reaction system always increases as temperature goes tose and surimi wash water at 95 °C and pH 9.0 for up to 12 h. In
up. In a fumonisin/glucose Maillard action model system, it was contrast, Rizzi (2008) reported that the addition of 0.040 M NaCl
reported that the apparent reaction rate constants of fumonisin enhanced the Maillard reaction between ribose and glycine at
B1 loss increased as temperature increased (Lu et al., 2002). Tem- 100 °C and pH 7.2 for up to 80 min. In another study, Kwak and
perature is an important variable in the Maillard reaction. The Lim (2004) studied the effect of NaCl addition on the Maillard reac-
Maillard reaction occurs at both low temperature (storage of food tion between glucose and each of nine amino acids at 100 °C and
products) and high temperature (processing and sterilization pro- pH 6.5 for up to 6 h. The results showed that the addition of 1%
cesses) (Caballero et al., 2016). Sheng et al. (2016) investigated NaCl enhanced the glucose/alanine and glucose/phenylalanine
the Maillard reaction in intermediate moisture protein-sugar foods Maillard reactions but inhibited the reactions between glucose
with or without the addition of resveratrol during storage at 45 °C. and other amino acids, while the addition of 10% NaCl inhibited
El Hassan Ajandouz, Desseaux, Tazi, and Puigserver (2008) studied the reactions between glucose and each of the nine amino acids.
the Maillard reaction between bovine casein peptides and galac-
tose during heating at 70–120 °C. Heating time is another impor- 3.1.4. Effects of initial glucose concentration and initial tyramine
tant parameter which contributes to the extent of reaction in concentration on tyramine reduction rates
Maillard reaction. An equivalent degree of Maillard reaction is Effect of initial glucose concentrations on tyramine reduction
obtained during a high-intensity short time heating and during a rates in the tyramine/glucose Maillard reaction model system is
weak treatment for a long time (Caballero et al., 2016). shown in Fig. 2D, during heating at 100 °C and pH 8.0 for 5 h. It
was observed that the tyramine reduction rates significantly rose
3.1.2. Effect of initial pH value on tyramine reduction rates from 6.89 ± 0.41% with 5 mM glucose to 43.16 ± 3.10% with
Effect of initial pH value on tyramine reduction rates in the 320 mM glucose after heating for 0.5 h (p < 0.05). Similar trends
tyramine/glucose Maillard reaction model system is shown in were also observed at 1, 3, and 5 h, indicating that the tyramine
Fig. 2B, during heating at 100 °C for 5 h. Firstly, the tyramine reduc- reduction rate increased as glucose concentration increased. Effect
tion rate significantly increased from 12.17 ± 3.22% after 0.5 h to of initial tyramine concentrations on tyramine reduction rates in
58.37 ± 2.36% after 5 h during heating at 100 °C and pH 7.0 the tyramine/glucose Maillard reaction model system is shown in
(p < 0.05). The similar trends were also seen at initial pH values Fig. 2E, during heating at 100 °C and pH 8.0 for 5 h. After heating
of 5.0, 6.0, 8.0, 9.0, 10.0, 11.0 and 12.0, suggesting that the tyra- for 5 h, the tyramine reduction rates were 100.00 ± 0.00,
mine reduction rate increased as heating time prolongs at different 92.07 ± 2.54, 78.25 ± 5.02, 65.54 ± 7.41, 52.03 ± 0.39 and
initial pH values. Secondly, the tyramine reduction rate signifi- 39.80 ± 4.48% when 40 mM glucose reacted with 0.5, 1, 2.5, 5, 10
cantly increased from 18.06 ± 3.02% at pH 5.0 to 95.61 ± 2.40% at and 20 mM tyramine, respectively. The decreased trends were also
pH 12.0 after heat treatment at 100 °C for 5 h (p < 0.05). The similar observed at 0.5, 1 and 3 h, suggesting that tyramine reduction rate
trends were also observed at 0.5, 1, and 3 h, indicating that the decreased as tyramine concentration increased.
tyramine reduction rate increased as initial pH value increased. The results indicate that tyramine loss is enhanced by the
Previous studies have demonstrated that the losses of reactants decreasing tyramine concentration or the increasing glucose con-
were promoted at higher initial pH value in casein/glucose centration, exhibiting a positive correlation between tyramine
(El Hassan Ajandouz et al., 2008), proline/glucose (Blank, Devaud, reduction rate and the concentration ratio of glucose to tyramine.
382 W. Jiang et al. / Food Chemistry 239 (2018) 377–384

Effect of the ratio of reactants on Maillard reactions has been 450


reported previously. For example, Li, Luo, and Feng (2011) investi-
400 A

Fluorescence intensity (A.U.)


gated the effect of the weight ratio of whey protein isolate to mal-
tose on the antigenicity of a-lactalbumin and b-lactoglobulin in 350
conjugates of whey protein isolate in whey protein isolate/maltose 300
Maillard reaction. Yang et al. (2015) studied the effect of the
250
weight ratio of soy protein isolate to soy soluble polysaccharide
on the emulsification capacity of the MRPs from soy protein isolate 200
and soy soluble polysaccharide. 150
100
3.2. Characterization of the tyramine/glucose Maillard reaction model
system 50
0
The Maillard reaction is a complex reaction between carbonyl
0 1 2 3 4 5 6 7 8 9 10 11 12
group of reducing sugars and free amino groups from amino acids,
peptides, proteins or other amino containing compounds. Gener- Time (h)
ally, the reaction process of Maillard reaction is divided into three 0.800
B
Time (h) 294 nm 420 nm
stages, namely initial stage, intermediate stage and final stage 0 0.003 0.000
(Nursten, 2005). 0.700 0.5 0.013 0.000
1 0.031 0.000
0.600 1.5 0.078 0.007
2 0.089 0.009
3.2.1. Changes in fluorescence intensity 2.5 0.122 0.015
Fluorescent compounds appeared prior to the formation of the 0.500 3 0.148 0.019

Absorbance
4 0.161 0.022
visible brown pigments. This is always used as the indicator of 0.400
12 h
6 0.204 0.033
10 h
the initial stage of the Maillard reaction (Baisier & Labuza, 1992). 8h
8
10
0.247
0.274
0.044
0.053
Fig. 3A shows the changes of fluorescence intensity of 2.5 mM tyra- 0.300 6h 12 0.298 0.057
heating time
mine, 40 mM glucose, the MRPs of 2.5 mM tyramine and 40 mM 4h
3h
0.200
glucose during heating at 100 °C and pH 8.0 for 12 h. It was
2.5 h
2h

observed that fluorescence intensity of tyramine or glucose was 0.100 1.5 h


1h

weak and did not change significantly during heating alone for 0.5 h
0h
0.000
12 h. However, fluorescence intensity of the MRPs of 2.5 mM tyra-
mine and 40 mM glucose during heating at 100 °C and pH 8.0 220 250 300 350 400 450 500 550 600 650 700 750 800
increased significantly to the maximum value of 402.5 ± 12.7 at nm
3 h, and decreased dramatically with prolonged heating time to
Fig. 3. (A) Change in fluorescence intensity of 2.5 mM tyramine ( ), 40 mM glucose
12 h. The development of fluorescence intensity in various Maillard
( ) and the mixture of 2.5 mM tyramine and 40 mM glucose ( ), during heating at
reaction systems has been widely investigated. Jiang, Wang, Wu, 100 °C and pH 8.0 for up to 12 h. Samples were diluted 10-fold with ultrapure water
and Wang (2013) studied fluorescence intensity changes of Mail- prior to analysis. (B) UV–vis absorbance spectra of the mixture of 2.5 mM tyramine
lard reactions between different sugars and bovine casein peptides. and 40 mM glucose during heating at 100 °C and pH 8.0 for up to 12 h. Samples
The results showed that the fluorescence intensity of bovine casein were diluted 50-fold with ultrapure water prior to analysis. The inserted table
shows the absorbance change at 294 and 420 nm during heating.
peptides/lactose MRPs rose steadily during heating at 95 °C for up
to 5 h, but bovine casein peptides/ribose MRPs decreased dramati-
cally after a maximum was reached at 1 h. Jiang and Brodkorb of the Maillard reaction (Morales & Jiménez-Pérez, 2001). As
(2012) found that fluorescence intensity of b-lactoglobulin/ribose shown in the inserted table in Fig. 3B, absorbance at 294 nm
MRPs during heating at 95 °C reached the maximum at 2 h, fol- increased with the prolonging of heating time, implying that the
lowed by a quick decline. Jing and Kitts (2002) revealed that fluo- intermediate MRPs formed within 0.5 h. Nevertheless, absorbance
rescence intensity of ribose/casein MRPs during heating at 55 °C at 420 nm did not rise in the first 1 h, but increased dramatically
reached the maximum within 5 days and decreased to a plateau after that. This result indicates that browning pigments formed
phase with prolonged heating time. These findings suggest that after the tyramine/glucose Maillard reaction had progressed for
the fluorescence intensity of MRPs of different Maillard reaction 1 h. Besides, a characteristic absorbance peak was observed at
systems change in various patterns. The reasons may be due to 265 nm, which might suggest the generation of new products. This
the formation of different fluorescent substances, which is dictated phenomenon was also reported in the Maillard reaction between
by the types of reactants and the reaction conditions. e-polylysine and dextran, where a characteristic absorbance peak
at 325 nm was observed (Li et al., 2014).
3.2.2. UV–vis absorption spectra
Fig. 3B shows the UV–vis absorption spectra of tyramine/glu-
cose MRPs during heating at 100 °C and pH 8.0 for up to 12 h. 3.3. Cytotoxicity assay
Without heat treatment, no detectable absorbance was observed
from 220 to 800 nm in the mixture of 2.5 mM tyramine and Although tyramine concentration was reduced during heating
40 mM glucose. As the heating time increased, the absorbance of with glucose under the proper conditions, the toxicity of the MRPs
tyramine/glucose MRPs increased significantly, indicating that was still unknown. Some categories of toxic MRPs such as
new compounds were formed in this process. The development 5-hydroxymethlofurfural (5-HMF), dicarbonyls, advanced glyca-
of UV–vis spectra has been studied in different Maillard reaction tion end products (AGEs) and heterocyclic amines (HAs), have
systems, which is reported affected by temperature (Li et al., attracted considerable attention (Zhang et al., 2015). Therefore,
2014), pH (Kim & Lee, 2008) and so on. cytotoxicity of tyramine, glucose, tyramine-glucose mixture and
The UV absorbance at 294 nm is often used as the representa- tyramine/glucose MRPs was evaluated by the MTT method using
tive of the MRPs in the intermediate stage, whereas the absorbance normal human liver HL-7702 cells. As shown in Table 2, tyramine
at 420 nm is related to the browning development in the final stage exhibited obvious cytotoxicity to HL-7702 cells, and cell growth
W. Jiang et al. / Food Chemistry 239 (2018) 377–384 383

inhibition rates increased from 16.99 ± 2.47% at the concentration 3.0


of 2 mM to 57.44 ± 2.40% at 10 mM (p < 0.05), indicating dose- A a
a

Tyramine concentration (mM)


dependent cytotoxicity to HL-7702 cells, whereas glucose did not a
2.5 a a
show observable toxicity. The results also showed that tyramine-
glucose mixture without heat treatment showed similar cytotoxi-
city to tyramine alone (p > 0.05). However, after heating at 100 °C ab
2.0
and pH 8.0 for 1 h, the cytotoxicity of MRPs-1 was significantly
lower than that of tyramine (p < 0.01). Furthermore, after at the b
c
same conditions for 5 h, the cytotoxicity of MRPs-5 was even lower 1.5
than that of MRPs-1. The results show that not only the tyramine
concentration was reduced in the tyramine/glucose Maillard reac-
tion, but also its cytotoxicity was lowered. The results were consis- 1.0
tent with a previous study which showed that the cytotoxicity of
fumonisin B1 could be reduced by Maillard reaction with glucose
(Meca et al., 2010). 0.5
0 1 2 3
Heating time (h)
3.4. Preliminary study on tyramine reduction in soy sauce
2.0

As food matrix is much more complex than the model system, B a


a a
a a

Tyramine concentration (mM)


the tyramine reduction ability of the tyramine/glucose Maillard
reaction was further assayed in soy sauce which has been reported
to contain high content of tyramine (Guidi & Gloria, 2012; Yongmei ab b
1.5
et al., 2009). Soy sauce is a traditional seasoning commonly used in
b
Asian countries. It is manufactured by fermentation of a mixture of
defatted soybean, roasted wheat flour, water and salt in the pres-
ence of koji mould for months. Soy sauce was mainly produced
by two types of manufacturing techniques, namely low-salt 1.0
solid-state fermentation and high-salt dilute-state fermentation
(Zhang, Zhou, Cui, Huang, & Wu, 2016). The low-salt soy sauce
sample is produced by low-salt solid-state fermentation and con-
tains 11.28 ± 0.79% (w/v) of salt with a pH of 6.21 ± 0.14, while
0.5
the high-salt soy sauce sample is produced by high-salt dilute- 0 1 2 3
state fermentation and contains 16.12 ± 1.04% (w/v) of salt with a Heating time (h)
pH of 5.98 ± 0.09. Tyramine concentrations of the low-salt soy
sauce and the high-salt soy sauce were measured as 2.54 ± 0.11 Fig. 4. Changes in tyramine concentrations in (A) low-salt and (B) high-salt soy
and 1.75 ± 0.09 mM, respectively. sauce samples with ( ) or without ( ) the addition of 2% (125 mM)
glucose during heating at 95 °C at different incubation times (0, 1, 2 and 3 h). Data
As the results in Fig. 2B and C show, soy sauce samples with
of the same group with different letters are significantly different (p < 0.05).
high salt content and low pH value are not ideal matrixes for the
tyramine/glucose Maillard reaction to proceed. Fig. 4 shows the
changes of tyramine concentrations in two soy sauce samples dur- other substances (such as amino acids, peptides, proteins and so
ing heating at 95 °C with or without the addition of 2% glucose on), or the presence of metal ions (Rizzi, 2017). These results
(125 mM). Tyramine concentrations in both samples without the indicate that tyramine reduction in the glucose-treated soy sauce
addition of glucose did not changed significantly during heating samples is mainly attributed to the tyramine/glucose Maillard
(p > 0.05). Nevertheless, after 3 h of glucose treatment, tyramine reaction. The influence on physiochemical properties of soy sauce
concentrations of low-salt soy sauce and high-salt soy sauce by Maillard reaction should be investigated in further experiments.
decreased significantly by 41.98 and 27.75%, respectively
(p < 0.05). The higher tyramine reduction rate in low-salt soy sauce 4. Conclusion
than in high-salt soy sauce might be explained by their differences
in salt content and pH value. Moreover, the tyramine reduction in In the tyramine/glucose Maillard reaction, effects of tempera-
soy sauce might be inhibited by the reactions between glucose and ture, heating time, initial pH value, NaCl concentration, initial

Table 2
Cytotoxicity assay of tyramine, glucose, tyramine-glucose mixture and tyramine/glucose Maillard reaction products (MRPs).

LevelsA Cell growth inhibition rate (%)


Tyramine Glucose MixtureB MRPs-1B MRPs-5C
1 16.99 ± 2.47a 1.87 ± 0.56**a 20.37 ± 5.59a 10.05 ± 1.53**a 5.22 ± 1.06**a
2 25.96 ± 2.93b 1.34 ± 0.76**b 25.28 ± 1.68ab 13.68 ± 1.84**a 8.51 ± 2.54**ab
3 30.05 ± 1.87bc 1.35 ± 0.12**b 31.01 ± 1.70b 22.50 ± 2.54*b 13.63 ± 4.93**bc
4 35.93 ± 3.18c 1.14 ± 0.94**b 33.21 ± 1.00b 25.04 ± 1.89**b 15.69 ± 1.44**bc
5 57.44 ± 2.40d 1.29 ± 0.81**b 53.49 ± 4.86c 32.85 ± 2.42**c 19.70 ± 2.57**c

Data in the same row with ** are significantly different vs Tyramine group (p < 0.01), * are significantly different vs Tyramine group (p < 0.05).
Data in the same column with different letters are significantly different (p < 0.05).
A
The details of levels were shown in Table 1.
B
The mixture was prepared by freeze-drying the mixture of 2.5 mM tyramine and 40 mM glucose in 50 mM PBS (pH 8.0).
C
The MRPs were prepared by freeze-drying the reaction products of 2.5 mM tyramine and 40 mM glucose after heating at 100 °C for 1 h (MRPs-1) or 5 h (MRPs-5) in
50 mM PBS (pH 8.0).
384 W. Jiang et al. / Food Chemistry 239 (2018) 377–384

glucose concentration and initial tyramine concentration on tyra- Jing, H., & Kitts, D. D. (2002). Chemical and biochemical properties of casein–sugar
Maillard reaction products. Food and Chemical Toxicology, 40(7), 1007–1015.
mine reduction rate were investigated. The increase of tempera-
Kim, J.-S., & Lee, Y.-S. (2008). Effect of reaction pH on enolization and racemization
ture, heating time, initial pH value or initial glucose concentration reactions of glucose and fructose on heating with amino acid enantiomers and
enhanced tyramine reduction, whereas the increase of NaCl con- formation of melanoidins as result of the Maillard reaction. Food Chemistry, 108
centration or tyramine concentration inhibited tyramine reduction. (2), 582–592.
Kwak, E.-J., & Lim, S.-I. (2004). The effect of sugar, amino acid, metal ion, and NaCl
Fluorescence intensity and UV–vis spectroscopy were used to on model Maillard reaction under pH control. Amino Acids, 27(1), 85–90.
characterize three stages (initial, intermediate and final stages) of Ladero, V., Calles-Enriquez, M., Fernandez, M., & Alvarez, M. A. (2010). Toxicological
the tyramine/glucose Maillard reaction. Cytotoxicity of tyramine, effects of dietary biogenic amines. Current Nutrition & Food Science, 6(2),
145–156.
glucose, tyramine-glucose mixture and tyramine/glucose MRPs to Li, C., Liu, F., Gong, Y., Wang, Y., Xu, H., Yuan, F., et al. (2014). Investigation into the
HL-7702 cells was assayed, revealing that tyramine/glucose MRPs Maillard reaction between e-polylysine and dextran in subcritical water and
were less toxic than tyramine. Furthermore, tyramine concentra- evaluation of the functional properties of the conjugates. LWT – Food Science and
Technology, 57(2), 612–617.
tions in two commercial soy sauce samples were significantly Li, Z., Luo, Y., & Feng, L. (2011). Effects of Maillard reaction conditions on the
reduced by heating with the addition of glucose. From a practical antigenicity of a-lactalbumin and b-lactoglobulin in whey protein conjugated
standpoint, this study provides a scientific basis for the application with maltose. European Food Research and Technology, 233(3), 387–394.
Linares, D. M., del Rio, B., Redruello, B., Ladero, V., Cruz Martin, M., Fernandez, M.,
of the Maillard reaction in foods for tyramine reduction. et al. (2016). Comparative analysis of the in vitro cytotoxicity of the dietary
biogenic amines tyramine and histamine. Food Chemistry, 197, 658–663.
Conflict of interest Linares, D. M., Martín, M., Ladero, V., Alvarez, M. A., & Fernández, M. (2011).
Biogenic amines in dairy products. Critical Reviews in Food Science and Nutrition,
51(7), 691–703.
The authors declare that they have no conflicts of interest. Liu, S.-C., Yang, D.-J., Chen, H.-Y., Chen, S.-L., & Chen, M.-L. (2011). Kinetics of
fructose on the Maillard brown colour development, pH change and
antioxidative activity development in model fructose/glycine systems.
Acknowledgements International Journal of Food Science & Technology, 46(8), 1768–1774.
Liu, S.-C., Yang, D.-J., Jin, S.-Y., Hsu, C.-H., & Chen, S.-L. (2008). Kinetics of color
This work was supported by the Zhejiang Provincial Natural development, pH decreasing, and anti-oxidative activity reduction of
Maillard reaction in galactose/glycine model systems. Food Chemistry, 108(2),
Science Foundation of China [grant number LQ15C200008], the 533–541.
Natural Science Foundation of China [grant number 31501573], Lu, Y., Clifford, L., Hauck, C. C., Hendrich, S., Osweiler, G., & Murphy, P. A. (2002).
and the Research Start-up Funding of Zhejiang Ocean University Characterization of Fumonisin B1–glucose reaction kinetics and products.
Journal of Agricultural and Food Chemistry, 50(16), 4726–4733.
[grant numbers Q1442 and Q1443].
Matějková, K., Křížek, M., Vácha, F., & Dadáková, E. (2013). Effect of high-pressure
treatment on biogenic amines formation in vacuum-packed trout flesh
References (Oncorhynchus mykiss). Food Chemistry, 137(1–4), 31–36.
Meca, G., Fernández-Franzón, M., Ritieni, A., Font, G., Ruiz, M. J., & Mañes, J. (2010).
Ajandouz, E. H., Desseaux, V., Tazi, S., & Puigserver, A. (2008). Effects of temperature Formation of fumonisin B1-glucose reaction product, in vitro cytotoxicity, and
and pH on the kinetics of caramelisation, protein cross-linking and Maillard lipid peroxidation on kidney cells. Journal of Agricultural and Food Chemistry, 58
reactions in aqueous model systems. Food Chemistry, 107(3), 1244–1252. (2), 1359–1365.
Ajandouz, E. H., & Tchiakpe, L. S. (2001). Effects of pH on caramelization and Morales, F. J., & Jiménez-Pérez, S. (2001). Free radical scavenging capacity of
Maillard reaction kinetics in fructose-lysine model systems. Journal of Food Maillard reaction products as related to colour and fluorescence. Food
Science, 66(7), 926–931. Chemistry, 72(1), 119–125.
Baisier, W. M., & Labuza, T. P. (1992). Maillard browning kinetics in a liquid model Nursten, H. E. (2005). The Maillard reaction: Chemistry, biochemistry, and implications.
system. Journal of Agricultural and Food Chemistry, 40(5), 707–713. Royal Society of Chemistry.
Blank, I., Devaud, S., Matthey-Doret, W., & Robert, F. (2003). Formation of odorants Rizzi, G. P. (2008). Effects of cationic species on visual color formation in model
in Maillard model systems based on L-proline as affected by pH. Journal of Maillard reactions of pentose sugars and amino acids. Journal of Agricultural and
Agricultural and Food Chemistry, 51(12), 3643–3650. Food Chemistry, 56(16), 7160–7164.
Bullerman, L. B., Bianchini, A., Hanna, M. A., Jackson, L. S., Jablonski, J., & Ryu, D. Rizzi, G. P. (2017). Use of sacrificial anode technology to mitigate non-enzymic
(2008). Reduction of fumonisin B1 in corn grits by single-screw extrusion. Maillard browning. Food Chemistry, 217, 205–208.
Journal of Agricultural and Food Chemistry, 56(7), 2400–2405. Sheng, Z., Gu, M., Hao, W., Shen, Y., Zhang, W., Zheng, L., et al. (2016).
Caballero, B., Finglas, P. M., & Toldrá, F. (2016). Encyclopedia of food and health. Physicochemical changes and glycation reaction in intermediate-moisture
Boulevard, Langford Lane, Kidlington, Oxford: Academic Press. protein–sugar foods with and without addition of resveratrol during storage.
Cai, L., Li, D., Dong, Z., Cao, A., Lin, H., & Li, J. (2016). Change regularity of the Journal of Agricultural and Food Chemistry, 64(24), 5093–5100.
characteristics of Maillard reaction products derived from xylose and Chinese Thongraung, C., & Kangsanan, S. (2010). Influence of pH, NaCl and pre-incubation on
shrimp waste hydrolysates. LWT – Food Science and Technology, 65, 908–916. utilisation of surimi wash water in generation of antioxidative material by using
Oliveira, F. C. de, Coimbra, J. S. dos R., Oliveira, E. B. de, Zuñiga, A. D. G., & Rojas, E. the Maillard reaction: Antioxidative activity of MRPs. International Journal of
E. G. (2016). Food protein-polysaccharide conjugates obtained via the Maillard Food Science & Technology, 45(8), 1696–1702.
reaction: A review. Critical Reviews in Food Science and Nutrition, 56(7), Xu, Y., Liu, Y., Xu, B., Wang, D., & Jiang, W. (2016). Characterisation and application
1108–1125. of Halomonas shantousis SWA25, a halotolerant bacterium with multiple
Dong, S., Panya, A., Zeng, M., Chen, B., Mcclements, D. J., & Decker, E. A. (2012). biogenic amine degradation activity. Food Additives and Contaminants Part A-
Characteristics and antioxidant activity of hydrolyzed b-lactoglobulin–glucose Chemistry Analysis Control Exposure & Risk Assessment, 33(4), 674–682.
Maillard reaction products. Food Research International, 46(1), 55–61. Yang, Y., Cui, S. W., Gong, J., Guo, Q., Wang, Q., & Hua, Y. (2015). A soy protein-
Fan, H., Liu, X., Hong, H., Shen, S., Xu, Q., Feng, L., et al. (2016). Quality changes and polysaccharides Maillard reaction product enhanced the physical stability of
biogenic amines accumulation of black carp (Mylopharyngodon piceus) fillets oil-in-water emulsions containing citral. Food Hydrocolloids, 48, 155–164.
stored at different temperatures. Journal of Food Protection, 79(4), 635–645. Yassoralipour, A., Bakar, J., Rahman, R. A., & Abu Bakar, F. (2012). Biogenic amines
Finberg, J. P. M., & Gillman, K. (2011). Selective inhibitors of monoamine oxidase formation in barramundi (Lates calcarifer) fillets at 8 °C kept in modified
type B and the ‘‘cheese effect”. In M. B. H. Y. P. Douce (Ed.), International Review atmosphere packaging with varied CO2 concentration. LWT – Food Science and
of Neurobiology (Vol. 100, pp. 169–190). Academic Press. Technology, 48(1), 142–146.
González-Jiménez, M., Arenas-Valgañón, J., García-Santos, M. del P., Calle, E., & Yongmei, L., Xiaohong, C., Mei, J., Xin, L., Rahman, N., Mingsheng, D., et al. (2009).
Casado, J. (2017). Mutagenic products are promoted in the nitrosation of Biogenic amines in Chinese soy sauce. Food Control, 20(6), 593–597.
tyramine. Food Chemistry, 216, 60–65. Zhang, X., Tao, N., Wang, X., Chen, F., & Wang, M. (2015). The colorants,
Guidi, L. R., & Gloria, M. B. A. (2012). Bioactive amines in soy sauce: Validation of antioxidants, and toxicants from nonenzymatic browning reactions and the
method, occurrence and potential health effects. Food Chemistry, 133(2), impacts of dietary polyphenols on their thermal formation. Food & Function, 6
323–328. (2), 345–355.
Jiang, Z., & Brodkorb, A. (2012). Structure and antioxidant activity of Maillard Zhang, H., Wang, W., Zhang, S., Wang, H., & Ye, Q. (2016a). Influence of 10-MeV E-
reaction products from a-lactalbumin and b-lactoglobulin with ribose in an beam irradiation and vacuum packaging on the shelf-life of grass carp surimi.
aqueous model system. Food Chemistry, 133(3), 960–968. Food and Bioprocess Technology, 9(5), 830–838.
Jiang, Z., Wang, L., Wu, W., & Wang, Y. (2013). Biological activities and Zhang, L., Zhou, R., Cui, R., Huang, J., & Wu, C. (2016b). Characterizing soy sauce
physicochemical properties of Maillard reaction products in sugar–bovine moromi manufactured by high-salt dilute-state and low-salt solid-state
casein peptide model systems. Food Chemistry, 141(4), 3837–3845. fermentation using multiphase analyzing methods. Journal of Food Science, 81
Jiang, W., Xu, Y., Li, C., Dong, X., & Wang, D. (2014). Biogenic amines in commercially (11), C2639–C2646.
produced Yulu, a Chinese fermented fish sauce. Food Additives & Contaminants
Part B-Surveillance, 7(1), 25–29.