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Food Control 82 (2017) 136e144

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

Histamine reduction by Maillard reaction with glucose


Wei Jiang a, Xiaoxia He b, Huicheng Yang c, Xingwei Xiang c, Shiwei Hu a, Shijie Li a,
Yu Liu a, *
a
Laboratory of Seafood Processing, Institute of Innovative and Application, Zhejiang Ocean University, Zhoushan, Zhejiang, 316022, China
b
Qingdao Entry-Exit Inspection and Quarantine Bureau, Qingdao, Shandong, 266002, China
c
Zhejiang Marine Development Research Institute, Zhoushan, Zhejiang, 316022, China

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

Article history: Histamine, well known as a toxic biogenic amine, is found in a variety of foods. Reducing its concen-
Received 15 April 2017 tration and toxicity is desirable. In this study, the glucose/histamine Maillard reaction was proposed as a
Received in revised form novel tool for histamine control. Effects of temperature, heating time, initial pH value, NaCl concentra-
19 June 2017
tion, initial histamine concentration and initial glucose concentration on percentage removal of hista-
Accepted 23 June 2017
Available online 24 June 2017
mine in the glucose/histamine Maillard reaction model were investigated. The results showed that
histamine reduction was affected by these variables, and could be almost eliminated under appropriate
conditions. Fluorescence intensity and ultravioletevisible spectroscopy analyses were used to charac-
Keywords:
Histamine
terize the glucose/histamine Maillard reaction. Cytotoxicity assay revealed that the glucose/histamine
Biogenic amine Maillard reaction significantly reduced the toxicity of histamine (P < 0.05). Furthermore, histamine
Glucose concentrations in canned tuna samples were significantly reduced by thermal treatment with glucose
Maillard reaction (P < 0.05). This study demonstrates that the glucose/histamine Maillard reaction is a promising method
Reduction for histamine control.
Cytotoxicity © 2017 Elsevier Ltd. All rights reserved.
Canned tuna

Chemical compounds studied in this article:


Histamine (PubChem CID: 774)
Glucose (PubChem CID: 5793)
Ampicillin (PubChem CID: 6249)
Methanol (PubChem CID: 887)
Dansyl chloride (PubChem CID: 11801)
Streptomycin (PubChem CID: 19649)
Sodium chloride (PubChem CID: 5234)
Dimethyl sulfoxide (PubChem CID: 679)

1. Introduction scombroid poisoning worldwide. It can not only cause a mild illness
with symptoms including dizziness, headache, hypotension, oral
Histamine, (2-(4-imidazolyl) ethylamine), is a biogenic amine burning and sweating, but also bring about life-threatening (Feng,
produced from the decarboxylation of amino acid histidine by Teuber, & Gershwin, 2016).
bacterial or tissue enzyme. As shown in Fig. 1, histamine is a het- The risk of histamine poisoning has attracted worldwide
erocyclic monoamine chemical. High content of histamine is widely attention. Reducing histamine concentration and toxicity in foods is
found in various foods, especially in fermented foods (Koral et al., desirable. Briefly, histamine reduction can be achieved by two
2013; Nei, Nakamura, Ishihara, Kimura, & Satomi, 2017; Pradenas, means, namely preventing the formation of histamine and
Galarce-Bustos, Henríquez-Aedo, Mundaca-Uribe, & Aranda, consuming the existed histamine. For instance, high hydrostatic
2016; Todoroki et al., 2014). Taking foods with high levels of his- pressure (Krí jkov
zek, Mate cha, & Dada
a, Va kova, 2014), irradiation
tamine can cause histamine poisoning, which is also known as (Aflaki, Ghoulipour, Saemian, Shiebani, & Tahergorabi, 2015) and
modified atmosphere packing (Rodrigues et al., 2016) are employed
to inhibit the growth of microorganisms and thus suppress the
formation of histamine. However, these techniques are not appli-
* Corresponding author. cable for fermented foods where the growth of microorganisms is
E-mail address: liuyu1987@zjou.edu.cn (Y. Liu).

http://dx.doi.org/10.1016/j.foodcont.2017.06.035
0956-7135/© 2017 Elsevier Ltd. All rights reserved.
W. Jiang et al. / Food Control 82 (2017) 136e144 137

NH2
water activity (Caballero, Finglas, & Toldr
a, 2016). It can be used as
an important tool for acquiring valuable Maillard reaction products
(MRPs) (Kanzler, Haase, Schestkowa, & Kroh, 2016; Lee et al., 2016).
Moreover, the Maillard reaction of glucose/fumonisin B1 was used
to the reduction of mycotoxin-fumonisin B1 (Lu et al., 2002),
implying that Maillard reaction might be applied to the reduction of
harmful chemicals with amino groups. Considering that histamine
has a free amino group (Fig. 1), it may be consumed by Maillard
reaction theoretically. Nevertheless, the Maillard reaction between
sugar and histamine has not been studied previously.
This study investigated the effects of temperature, initial pH
value, NaCl concentration, initial glucose concentration and initial
histamine concentration on histamine reduction in a glucose/his-
tamine Maillard reaction model. The intermediate and final stages
of this reaction were characterized by fluorescence intensity and
ultravioletevisible spectroscopy. Cytotoxicity of histamine, glucose,
glucose/histamine mixture, and glucose/histamine MRPs was
compared. Moreover, the reduction of histamine content in canned
tuna by the glucose/histamine Maillard reaction was assessed
preliminarily. The aim was to evaluate the possibility of applying

N
the glucose/histamine Maillard reaction to reduce histamine level
and detoxification of it.

2. Materials and methods

2.1. Chemicals

Histamine, dansyl chloride and dimethyl sulfoxide were pro-


vided by Sigma-Aldrich, Inc. (St. Louis, MO, USA). Glucose was
provided by Solarbio Inc. (Beijing, China). Methanol (HPLC grade)
was provided by Merck (Darmstadt, Germany). Ultrapure water
was prepared by Milli-Q (Millipore, Billerica, MA, USA). Roswell
Park Memorial Institute (RPMI) 1640 medium, fetal bovine serum,

N
streptomycin sulphate, ampicillin, trypsin, 3-(4,5-dimethylthiazol-
2-yl)-2,5-diphenyltetrazolium bromide (MTT) were provided by
Gibco (Invitrogen Co., Burlington, ON, Canada).

2.2. Glucose/histamine maillard reaction model

H Fig. 1. Structure of histamine.


Glucose/histamine Maillard reaction was conducted in
16 mm  155 mm glass screw tubes capped with tight screw-caps.
Unless otherwise stated, the incubations contained 50 mM potas-
sium phosphate, pH 8.0, 40 mM glucose, and 2.5 mM histamine in a
total volume of 5.0 mL without the addition of NaCl. The tubes were
incubated at designed temperatures in a Digital Dry Bath (Jinxin,
very important. Furthermore, the existing histamine cannot be
JX100-4, Shanghai, China). To ensure that the reaction was stopped
consumed by these methods. Thus, some other researchers isolated
at the appropriate time point, the tubes were cooled in a mixture of
histamine degrading strains as functional starter cultures (Xu, Liu,
ice and water for 30 min.
Xu, Wang, & Jiang, 2016) or applied amine oxidase (Naila et al.,
2012) for the degradation of histamine. However, the amine oxi-
2.3. Factors affecting percentage removal of histamine in the
dase is expensive at present, and professional equipment/staff are
glucose/histamine maillard reaction model
required for the application of histamine degrading strains. Hence,
a more feasible method is required for histamine control in foods.
Effect of temperatures (60, 70, 80, 90, 100 and 110  C) on per-
Maillard reaction, also known as non-enzymatic browning re-
centage removal of histamine was investigated by the reaction of
action, is a complex chemical reaction between carbonyl groups of
40 mM glucose and 2.5 mM histamine at pH 8.0 for 12 h without
reducing sugars and free amino groups of amino acids, peptides,
the addition of NaCl. Samples were taken at 0, 0.5, 1, 1.5, 2, 2.5, 3, 4,
proteins or some other nitrogen containing compounds. Maillard
6, 8, 10 and 12 h. Effects of initial pH values (5.0, 6.0, 7.0, 8.0, 9.0,
reaction plays an important role in food industry and occurs during
10.0, 11.0 and 12.0), NaCl concentrations (0, 0.5, 1.0, 1.5, 2.0, 2.5, 3.0,
thermal processing or food storage. According to the compounds
4.0, 6.0, 8.0, 10.0 and 12.0%, w/v), initial glucose concentrations (5,
generated during Maillard reaction, the reaction process is divided
10, 20, 40, 60, 80, 160 and 320 mM) and initial histamine concen-
into early, intermediate and final stages (Nursten, 2005). Among
trations (0.5, 1.0, 2.5, 5.0, 10.0 and 20.0 mM) on percentage removal
them, the intermediate and final stages can be characterized by
of histamine were investigated by changing one parameter at a
fluorescence intensity and ultravioletevisible absorption. Maillard
time in the reaction of 40 mM glucose and 2.5 mM histamine at
reaction is affected by a variety of variables, such as temperature,
100  C and pH 8.0 for 5 h without the addition of NaCl. Samples
reaction time, pH, substrate concentration, substrate type, and
were taken at 0.5, 1, 3 and 5 h.
138 W. Jiang et al. / Food Control 82 (2017) 136e144

2.4. Histamine concentration determination RPMI 1640 medium containing 10% (v/v) fetal bovine serum, 0.01%
(w/v) ampicillin and 0.05% (w/v) streptomycin. After incubated at
Histamine concentration was determined using HPLC method 37  C for 24 h under a humidified atmosphere containing 5% CO2,
by pre-column derivatization with dansyl chloride (Jiang, Xu, Li, 100 mL of culture medium containing different test substances (as
Dong, & Wang, 2014). Derivatization process was performed as shown in Table 1) were added to the wells of experiment groups.
previously reported (Dad akova, Krí nova
zek, & Pelika , 2009) with Meanwhile, 100 mL of culture medium without test substances were
some modifications. One milliliter of sample was mixed with 1.5 mL added to the wells of the negative control group. The cells were
of carbonate buffer (pH 11) in a 10 mL centrifuge tube. The car- subsequently cultured for 24 h at 37  C under a humidified atmo-
bonate buffer was prepared according to a previously reported sphere containing 5% CO2. Then 10 mL of MTT solution (5 mg/mL)
method (Dada kova et al., 2009). After mixed, 1.0 mL of dansyl was added to each well and the plate was incubated for another 4 h.
chloride solution (dansyl chloride in acetone, 10 mg/mL) was After carefully removal of the supernatant, 100 mL of dimethyl
added. The centrifuge tube was shaken at 40  C in a water bath for sulfoxide was added to each well and the plate was shaken at room
1 h in darkness. To consuming the remaining dansyl chloride, temperature for 20 min. The absorbance at 490 nm was measured
0.2 mL of proline solution (proline in ultrapure water, 100 mg/mL) in a microplate reader (PULANG, DNM-9606, Beijing, China). The
was added and the mixture was shaken for another 1 h in darkness. cell growth inhibition rate was calculated as follow: Cell growth
Then 3 mL of heptane was added and the mixture was shaken for inhibition rate (%) ¼ (Absorbance value of control - Absorbance
30 min. After stratification, 1.0 mL of the heptane part was dried at value of sample)/Absorbance value of control  100.
40  C using a gas blowing concentrator (Jinxin, JXDC-400, Shanghai,
China). The dried residue was dissolved in 1 mL of methanol.
2.9. Thermal treatment of canned tuna with glucose
Samples were filtered through a 0.22 mm filter (Millipore, Bedford,
MA, USA) prior to analysis. The HPLC system consist of a Waters
To evaluate the histamine reduction ability of Maillard reaction
2695 series (Milford, USA) equipped with a degasser, quaternary
in foods, two commercial canned tuna samples were obtained from
pump, column oven, ultraviolet detector and automatic sampler. A
a market in Zhoushan, Zhejiang, China. The salt concentrations of
reversed-phase chromatographic column (Capcell PAK 5 mm C18
sample A and sample B were measured as 2.03± 0.21% (w/v) and
MG, 150  4.6 mm) was provided by Shiseido Co. (Tokyo, Japan).
1.85± 0.37% (w/v), respectively. The pH values of sample A and
The chromatographic column was equilibrated at 30  C with the
sample B were measured as 6.68 ± 0.07 and 6.82 ± 0.16, respec-
mobile phase of 55% methanol and 45% ultrapure water. The
tively. The obtained canned tuna was opened and its net weight
derivatized histamine was detected at 254 nm. The injection vol-
was measured. Then 2% (w/w) of glucose (equal to 125 mM of
ume was 10 mL. Calibration curves were constructed of peak area
glucose) was added and mixed gently. The mixture was transferred
versus standard histamine concentration (0.01e2.5 mM).
to a sealable glass container. After that, the container was incubated
in a water bath at 95  C. Samples were taken at the heating time
2.5. Fluorescence intensity
points of 0, 1, 2 and 3 h.
Fluorescence intensities of samples were determined by a
fluorescence spectrophotometer (Hitachi, F-4500, Kyoto, Japan) as 2.10. Histamine extraction from canned tuna
nez-Pe
the method described previously (Morales & Jime rez, 2001).
Samples were diluted 10-fold with ultrapure water. The fluores- Histamine was extracted from canned tuna by a reported
cence intensities were measured at an excitation wavelength of method (Evangelista et al., 2016) with some modifications. The
350 nm and an emission wavelength of 420 nm. samples were chopped and ground using a glass tissue grinder.
After homogenization, 2.0 g of samples were placed into centrifuge
2.6. Ultravioletevisible spectroscopy tubes containing 3 mL of 5% (w/v) trichloroacetic acid. The tubes
were mixed for 70 s by a vortex mixer (IKA, MS3, Staufen, German)
Ultravioletevisible spectra of samples were determined by an and centrifuged at 11250 g and 4  C for 3 min by a refrigerated
ultravioletevisible spectrophotometer (Shimadzu, UV-2600, Kyoto, centrifuge (Zhongke, HC-3018R, Anhui, China). The supernatant
Japan) as the method described previously (Zhou et al., 2013) with was filtered through qualitative paper. The acid extraction step was
some modifications. Samples were diluted 50-fold with ultrapure repeated twice again. The filtrates were all transferred into a cali-
water. Ultravioletevisible spectra were recorded from 220 to brated volumetric flask and diluted with 5% trichloroacetic acid to
800 nm with an interval of 0.5 nm. Meanwhile, the absorbance at 10 mL. The diluted solution was used for the determination of
294 and 420 nm was measured. histamine concentration in canned tuna.

2.7. Cell culture


Table 1
Experiment design for cytotoxicity assay of histamine, glucose, glucose/histamine
The normal human liver HL-7702 cell line (BNCC 100966) was mixture and glucose/histamine Maillard reaction products (MRPs).
provided by BeNa Culture Collection Co. Ltd. (Beijing, China). Cells
Levels Concentration (mM)
were maintained in RPMI 1640 medium containing 10% (v/v) fetal
bovine serum, 0.01% (w/v) ampicillin and 0.05% (w/v) streptomycin Histamine Glucose Mixturea MRPs-1b MRPs-5b
at 37  C under a humidified atmosphere containing 5% CO2. 1 2 32 34 34 34
2 4 64 68 68 68
2.8. Cytotoxicity assay 3 6 96 102 102 102
4 8 128 136 136 136
5 10 160 170 170 170
Cytotoxicity of histamine, glucose, glucose/histamine mixture,
a
and glucose/histamine MRPs were evaluated by the MTT assay It was prepared by freeze-drying of the mixture of 2.5 mM histamine and 40 mM
glucose in 50 mM PBS (pH 8.0).
using HL-7702 cells as a previously reported method (Xia et al., b
They were prepared by freeze-drying of the MRPs of 2.5 mM histamine and
2014) with some modifications. Briefly, cells were seeded into a 40 mM glucose after heating at 100  C for 1 h (MRPs-1) or 5 h (MRPs-5) in 50 mM
96-well plate at density of 5  103 cells per well with 100 mL of PBS (pH 8.0).
W. Jiang et al. / Food Control 82 (2017) 136e144 139

2.11. Statistical analyses histamine Maillard reaction model with different initial pH values
are shown in Fig. 3A. Percentage removal of histamine significantly
Statistical analyses were performed using the software IBM SPSS increased as the initial pH value increased from 5.0 to 12.0
Statistics 22.0 (IBM, USA). Data were analyzed by one-way analysis (P < 0.05). Specifically, if the initial pH value was no less than 7.0,
of variance (ANOVA) with the Tukey test. The experiments were histamine was almost eliminated within 5 h. The promotion of
performed in triplicate and the data were expressed as reactants consumption at high initial pH value was reported in
average ± standard deviation. various Maillard reactions, such as glucose/casein (Ajandouz,
Desseaux, Tazi, & Puigserver, 2008), glucose/proline (Blank,
3. Results and discussion Devaud, Matthey-Doret, & Robert, 2003), and fructose/lysine
(Ajandouz & Tchiakpe, 2001). The inhibition of glucose/histamine
3.1. Effects of temperature and heating time on percentage removal Maillard reaction in acidic solution might be attributed to the
of histamine protonation of histamine (Liu, Yang, Chen, Chen, & Chen, 2011).
Under the condition of low pH value, the nitrogen atom in the
Changes of percentage removal of histamine during thermal amino group of histamine would be protonated and transformed
treatment with or without glucose are shown in Fig. 2. It was into an ammonium ion. This phenomenon resulted in suppressing
observed that histamine concentration remained essentially un- the condensation of amino group with carbonyl group and thus
changed when heated alone at 110  C for up to 12 h, indicating that reducing the consumption of histamine. Moreover, reaction rate
histamine was thermally stable at this temperature. Nevertheless, could be slowed down by the fact that the pH value always de-
histamine was consumed in the glucose/histamine Maillard reac- creases in the process of Maillard reaction, which was attributed to
tion model, and the percentage removal was influenced by tem- the consumption of the basic amino group and the formation of
perature and heating time. acidic MRPs (Cai et al., 2016). Furthermore, it was reported that the
It can be seen in Fig. 2 that percentage removal of histamine activation energy value decreased as the system pH increased in
increased as the reaction temperature increased from 60 to 110  C. Maillard reactions, indicating that Maillard action occurred easier
Temperature plays an important role in Maillard reaction, and this at higher pH value (Ajandouz et al., 2008).
reaction can occur during the storage, processing and sterilization
of foods. Recently, different research groups reported the sugar/ 3.3. Effect of NaCl concentration on percentage removal of
whey protein Maillard reactions at 37  C and 123  C (Leiva, Naranjo, histamine
& Malec, 2017; Ruiz et al., 2016). As Maillard reaction is an endo-
thermic reaction, the degree of this reaction is always enhanced at Since histamine was always found in fermented foods with high
higher temperature (Lu et al., 2002). salt content (Jiang et al., 2014), we investigated the effect of salt
Heating time is another important factor in Maillard reaction. As concentration on percentage removal of histamine in the glucose/
shown in Fig. 2, percentage removal of histamine increased with histamine Maillard reaction model. As shown in Fig. 3B, the addi-
the prolonging of heating time. Histamine was almost eliminated tion of NaCl decreased percentage removal of histamine in the
within 1.5, 2.5, and 6 h when heated at 110, 100, and 90  C, glucose/histamine Maillard reaction model. It was worth noting
respectively. The equal degree of Maillard reaction can be achieved that histamine was almost eliminated within 5 h if no more than
by a high-temperature short-time treatment or a low-temperature 8.0% of NaCl was added. The results were consistent with a previous
long-time treatment (Caballero et al., 2016). study in which the addition of 0.5e2.5% NaCl inhibited the fructose/
surimi wash water Maillard reaction at 95  C and pH 9.0 for 12 h
(Thongraung & Kangsanan, 2010).
3.2. Effect of initial pH value on percentage removal of histamine
3.4. Effects of initial glucose concentration and initial histamine
Results of percentage removal of histamine in the glucose/ concentration on percentage removal of histamine

Results of percentage removal of histamine in the glucose/his-


100 tamine Maillard reaction model at 100  C and pH 8.0 with 2.5 mM
histamine and different concentrations of glucose (5e320 mM) are
showed in Fig. 3C. Percentage removal of histamine increased with
Percentage removal (%)

80 increasing glucose concentration. Histamine was almost eliminated


after 1, 3, and 5 h with 2.5 mM histamine and no less than 320, 20,
60 and 10 mM of glucose, respectively. Results of percentage removal
of histamine in the glucose/histamine Maillard reaction model at
100  C and pH 8.0 with 40 mM glucose and different concentrations
40 of histamine (0.5e20 mM) are showed in Fig. 3D. Percentage
removal of histamine decreased as histamine concentration
20 increased. Histamine was almost eliminated after 3 and 5 h with
40 mM glucose and no more than 5 and 10 mM of histamine,
respectively.
0 As indicated in Fig. 3C and D, percentage removal of histamine in
0 1 2 3 4 5 6 7 8 9 10 11 12 the glucose/histamine Maillard reaction model positively corre-
Heating time (h) lated with initial glucose concentration and negatively correlated
with initial histamine concentration, suggesting that it might be
Fig. 2. Changes of percentage removal of histamine in the glucose/histamine Maillard determined by the concentration ratio between glucose and his-
reaction model during heating at different temperatures (60  C, ; 70  C, ; 80  C,
; 90  C, ; 100  C, ; 110  C, ) for up to 12 h. The reaction was performed with
tamine. When the reaction was proceeded with the concentration
2.5 mM histamine and 40 mM glucose at pH 8.0. Histamine heated alone at 100  C and ratio of glucose to histamine as four to one, percentage removal of
pH 8.0 was also studied ( ). histamine in Fig. 3C by 10 mM glucose and 2.5 mM histamine
140 W. Jiang et al. / Food Control 82 (2017) 136e144

(a) g
(b) f
c dc dc f dc f dc g f dc f f f f ff f f
100 e 100
b
e
Percentage removal (%)

Percentage removal (%)


e d
c
80 de
80 d cd c
e g

f
60 b 60 b
e
de d
c d f cd
a ef abb
40 40 de c
a
c d d b a
a b ab
cd
c
a
20 a 20 b
b ab
a a

0 0
5 6 7 8 9 10 11 12 0 1 3 5 8 11 14 19 24 29
Initial pH NaCl concentration (%)

(c) (d) c b
b cb cb cb c b cb hcb e c b c b c b b
100 g 100
e

Percentage removal (%)


h
Percentage removal (%)

b
80 f 80 f
g d b
d e
a e a

60 c ef f 60 c
a
a
d d
b b
40 40
c
c
a
a
20 b 20 b
a a

0 0
5 10 20 40 60 80 160 320 0.5 1 2.5 5 10 20
Glucose concentration (mM) Histamine concentration (mM)
Fig. 3. Effects of (a) initial pH value, (b) NaCl concentration, (c) initial glucose concentration and (d) initial histamine concentration on percentage removal of histamine in the
glucose/histamine Maillard reaction model system at different reaction time (0.5 h, ; 1 h, ; 3 h, ; 5 h, ). Reaction Conditions: (a) 2.5 mM histamine and 40 mM
glucose at 100  C and different initial pH values; (b) 2.5 mM histamine and 40 mM glucose at 100  C and pH 8.0 with different concentration of NaCl; (c) 2.5 mM histamine and
different concentration of glucose at 100  C and pH 8.0; (d) different concentration of histamine and 40 mM glucose at 100  C and pH 8.0. Bars of the same color (at the same
reaction time) with different letters are significantly different (P < 0.05).

(16.52% at 0.5 h, 36.74% at 1 h, 74.91% at 3 h, and 100% at 5 h) were Fluorescence intensity of ribose/a-lactoglobulin MRPs reached the
similar to those in Fig. 3D by 40 mM glucose and 10 mM histamine maximum within 2 h, followed by a rapid decline (Jiang &
(15.69% at 0.5 h, 35.61% at 1 h, 70.91% at 3 h and 100% at 5 h). Effect Brodkorb, 2012). Nevertheless, fluorescence intensity of xylan/
of the reactant ratio on Maillard reactions has been also reported in chitosan MRPs increased to a plateau phase in 2 h (Wu et al., 2014).
previous studies (Li, Luo, & Feng, 2011; Yang et al., 2015). In a binary Fluorescence intensity of MRPs is related to the generation and
Maillard reaction system, increasing of the concentration of one consumption of fluorescent substances, which is determined by
reactant always results in inhibiting its own reduction rate, but both the types of reactants and the extent of reaction. The results
enhancing the consumption of the other reactant. demonstrate that some fluorescent MRPs form during the glucose/
histamine Maillard reaction, and are converted into non-
fluorescent substances as the reaction proceeds.
3.5. Characterization on the glucose/histamine maillard reaction Ultravioletevisible spectrum, a useful tool for characterizing the
process of Maillard reaction, has been studied in a variety of models
Fluorescence substances can be detected in the intermediate (Hrynets, Ndagijimana, & Betti, 2015; Shrestha & De Meulenaer,
stage as the precursors of the brown products in the final stage 2014). Besides, the ultraviolet absorbance at 294 nm always rep-
(Jiang, Wang, Wu, & Wang, 2013). As shown in Fig. 4, during ther- resents the MRPs of the intermediate stage, and the visible absor-
mal treatment at 100  C and pH 8.0 for 4 h, fluorescence intensity of bance at 420 nm is associated with the browning development in
40 mM glucose alone or 2.5 mM histamine alone did not changed the final stage (Morales & Jime nez-Perez, 2001). Fig. 5 shows the
significantly. However, when the mixture of 40 mM glucose and ultravioletevisible spectra of the glucose/histamine MRPs, during
2.5 mM histamine were heated under the same conditions, the heating at 100  C and pH 8.0 with 40 mM glucose and 2.5 mM
fluorescence intensity of the glucose/histamine MRPs increased histamine for up to 4 h. The mixture of glucose and histamine
and reached the maximum value at 1.5 h. Thereafter, it decreased without thermal treatment (heating time ¼ 0 h) did not show
slightly as the heating time prolonged to 4 h. Previous studies detectable absorbance between 220 nm and 800 nm. Nevertheless,
suggested that fluorescence intensity of different MRPs changed in ultravioletevisible absorbance of the glucose/histamine MRPs
different modes. Fluorescence intensity of galactose/bovine casein increased obviously with the prolonging of heating time (0e4 h),
peptide MRPs was also found to quickly reach a maximum at 1 h implying that new substances generated in this process. As shown
and decreased dramatically thereafter (Jiang et al., 2013).
W. Jiang et al. / Food Control 82 (2017) 136e144 141

500

Fluorescence intensity (A.U.) 400

300

200

100

0
0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0
Heating time (h)
Fig. 4. Change of fluorescence intensity of 40 mM glucose ( ), 2.5 mM histamine ( ) and the MRPs of 40 mM glucose and 2.5 mM histamine ( ), during heating at 100  C and pH
8.0 for up to 4 h. Samples were diluted 10-fold with ultrapure water prior to analysis.

0.250
0.10
Absorbance at 294 nm
0.09 Absorbance at 420 nm

0.08
0.200 0.07

0.06
Absorbance

0.05

0.04
0.150
Absorbance

0.03

0.02

0.01
4h
0.00
0.100 3.5 h 0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0
Heating time (h)
3h heating time
2.5 h

2h
0.050
1.5 h
1h
0.5 h
0.25 h
0.000 0h

220 250 300 350 400 450 500 550 600 650 700 750 800
nm
Fig. 5. Ultravioletevisible absorbance spectra of the MRPs of 40 mM glucose and 2.5 mM histamine during heating at 100  C and pH 8.0 for up to 4 h. Samples were diluted 50-fold
with ultrapure water prior to analysis. The inserted figure showed the absorbance changes at 294 nm and 420 nm.

in the figure inserted in Fig. 5, the absorbance at 294 nm increased 0.25 h. However, most of these MRPs generate from 1.5 to 3 h. The
dramatically as the heating time went on. It was also observed that inserted figure in Fig. 5 also shows that the absorbance at 420 nm
the absorbance increasing speed at 294 nm was lower in the first does not increase in the first 0.5 h, but increases dramatically
1.5 h (increase from 0.003 to 0.024) than that between 1.5 h and 3 h thereafter (from 0.001 at 0.5 h to 0.017 at 4 h) with the extended
(increase from 0.024 to 0.074). The results indicate that the glucose/ heating time. The results indicate that browning pigments, gener-
histamine MRPs of the intermediate stage form immediately within ating in the final stage of Maillard reaction, do not form
142 W. Jiang et al. / Food Control 82 (2017) 136e144

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

Levelsa Cell growth inhibition rate (%)

Histamine Glucose Mixtureb MRPs-1c MRPs-5c

1 14.29 ± 2.09a 1.87 ± 0.56**a 13.21 ± 1.97a 7.86 ± 0.61**a 1.82 ± 0.43**a
2 18.49 ± 0.68ab 1.34 ± 0.76**b 19.64 ± 0.81b 13.14 ± 0.88**b 2.59 ± 0.54**a
3 23.70 ± 1.33bc 1.35 ± 0.12**b 22.21 ± 1.12b 19.57 ± 1.35**c 2.22 ± 0.33**a
4 28.32 ± 2.12c 1.14 ± 0.94**b 28.58 ± 0.99c 20.51 ± 1.42**c 4.61 ± 2.90**ab
5 47.25 ± 2.82d 1.29 ± 0.81**b 50.21 ± 2.00d 26.72 ± 2.80**d 5.79 ± 1.65**b

Data in the same row with ** are significantly different vs Histamine group (P < 0.01).
Data in the same column with different letters are significantly different (P < 0.05).
a
The levels of different groups were shown in Table 1.
b
It was prepared by freeze-drying of the mixture of 2.5 mM histamine and 40 mM glucose in 50 mM PBS (pH 8.0).
c
They were prepared by freeze-drying of the MRPs of 2.5 mM histamine 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).

immediately at the beginning of the glucose/histamine Maillard thermal treatment showed similar cytotoxicity to that of the his-
reaction. tamine group. However, after 40 mM glucose and 2.5 mM hista-
mine reacted at 100  C and pH 8.0 for 1 h, the histamine
concentration was reduced by 60.66% (Fig. 2), and the cytotoxicity
3.6. Cytotoxicity comparison of MRPs-1 was significantly lower than that of histamine or the
mixture of glucose and histamine (P < 0.01). Furthermore, when
Various toxic MRPs, such as 5-hydroxymethlofurfural, dicar- the reaction time was 5 h, the cell growth inhibition rates of MRPs-
bonyls, advanced glycation end products and heterocyclic amines, 5 were all lower than 10%, exhibiting even lower cytotoxicity than
have caused wide concern over the recent years (Zhang, Tao, Wang, MRPs-1. The results show that the glucose/histamine Maillard re-
Chen, & Wang, 2015). Hence, although histamine concentration action does not only reduce the histamine content, but also lowered
decreased in the glucose/histamine Maillard reaction, the unknown its cytotoxicity.
toxicity of the MRPs was still a problem. Hence, we assayed cyto-
toxicity of histamine, glucose, glucose/histamine mixture and
glucose/histamine MRPs using normal human liver HL-7702 cells 3.7. Preliminary application of glucose/histamine maillard reaction
by MTT method. As shown in Table 2, histamine showed significant in canned tuna
cytotoxicity to HL-7702 cells in a dose-dependent manner
(P < 0.05). The cell growth inhibition rate of the histamine group In order to evaluate the potential application of the glucose/
increased significantly from 14.29% with 2 mM histamine to 47.25% histamine Maillard reaction, we tested its performance in com-
with 10 mM histamine (P < 0.05). However, the cell growth inhi- mercial canned tuna samples which always contained high levels of
bition rates of the glucose group were all less than 2%, indicating no histamine (Akbari-Adergani, Hosseini, Shekarchi, & Pirali-
observable toxicity. The mixture of histamine and glucose without Hamedani, 2012). The salt concentration, pH value, and histamine

0.9
c
Histamine concentration (mM)

0.8

0.7
b
0.6
b
0.5
ab a
0.4 a
0.3 a a
0.2

0.1

0.0
0 1 2 3
Heating time (h)
Fig. 6. Histamine reduction in two canned tuna samples (sample A, ; sample B, ) by the glucose/histamine Maillard reaction at different incubation time (0, 1, 2, 3 h). The
incubation was performed with 125 mM glucose at 95  C. Bars of the same sample with different letters are significantly different (P < 0.05).
W. Jiang et al. / Food Control 82 (2017) 136e144 143

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Leiva, G. E., Naranjo, G. B., & Malec, L. S. (2017). A study of different indicators of
reaction were characterized by fluorescence intensity and ultra- Maillard reaction with whey proteins and different carbohydrates under
violetevisible spectroscopy. The results showed that MRPs of the adverse storage conditions. Food Chemistry, 215, 410e416.
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analyzed in this study. Cytotoxicity assay indicated that the toxicity Liu, S.-C., Yang, D.-J., Chen, H.-Y., Chen, S.-L., & Chen, M.-L. (2011). Kinetics of fruc-
of glucose/histamine MRPs was significantly lower than that of tose on the Maillard brown colour development, pH change and antioxidative
histamine (P < 0.01). Furthermore, the glucose/histamine Maillard activity development in model fructose/glycine systems. International Journal of
Food Science & Technology, 46(8), 1768e1774.
reaction significantly reduced histamine concentration in two Lu, Y., Clifford, L., Hauck, C. C., Hendrich, S., Osweiler, G., & Murphy, P. A. (2002).
commercial canned tuna samples (P < 0.05). Taken together, this Characterization of fumonisin B1Glucose reaction kinetics and products.
study demonstrates that the glucose/histamine Maillard reaction Journal of Agricultural and Food Chemistry, 50(16), 4726e4733.
Morales, F. J., & Jime nez-Pe rez, S. (2001). Free radical scavenging capacity of Mail-
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Acknowledgments Naila, A., Flint, S., Fletcher, G. C., Bremer, P. J., Meerdink, G., & Morton, R. H. (2012).
Prediction of the amount and rate of histamine degradation by diamine oxidase
(DAO). Food Chemistry, 135(4), 2650e2660.
The work was supported by the Zhejiang Provincial Natural Nei, D., Nakamura, N., Ishihara, K., Kimura, M., & Satomi, M. (2017). A rapid
Science Foundation of China [grant number LQ15C200008], the screening of histamine concentration in fish fillet by direct analysis in real time
mass spectrometry (DART-MS). Food Control, 75, 181e186.
Natural Science Foundation of China [grant number 31501573], and Nursten, H. E. (2005). The maillard reaction: Chemistry, biochemistry, and implica-
the Research Start-up Funding of Zhejiang Ocean University [grant tions. Royal Society of Chemistry.
numbers Q1442, Q1443]. Pradenas, J., Galarce-Bustos, O., Henríquez-Aedo, K., Mundaca-Uribe, R., &
Aranda, M. (2016). Occurrence of biogenic amines in beers from Chilean market.
Food Control, 70, 138e144.
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