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Journal of Advanced Biomedical & Pathobiology Research Vol.7 No.1, August 2017, 1-13
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Histamine content in various types of canned foods (fruits and
syrups) stored under different temperature conditions over
time - an in vitro study
1*Balavinayagamani Ganapathy, 1Ali Qusay Khalid, 2Mong Xin Ru, 3Paulraj
Ponnaiah
Department of Biomedical Sciences, Faculty of Medicine, MAHSA University, Bandar Saujana
Putra, Selangor Dahrul Ehsan, Malaysia
balavinayagamani@gmail.com
Abstract
Histamine (Biogenic amines) is one of the most important nitrogen containing compounds present
in many vegetables, fruits and poultry food products and has biological importance in creating
allergic reaction most of the times. Some toxicological descriptions of food poisoning are often
associated with histamine -the most prominent biogenic amines in the category. The secondary
amines involved in nitrosation and form nitrosamines which are toxic initiates illnesses to our
organs. Their concentration in high level is detected in processed foods especially. In considering
the food safety they have been related to food spoilage and fermentation processes. The aim of our
study is to correlate the histamine in canned foods safety and analyse the presence of biogenic
amines especially histamine in processed fruit syrups and pickles under different storing
temperatures over time. The 5 different chosen varieties of canned fruits (mango pickle, fermented
durian, canned pineapple syrup, canned rambutan syrup and canned lychee syrup) were brought into
the laboratory unopened and on the day of purchase, they were opened and analysed for histamine
for the first time. Further they have portioned into five, and each of the portion was stored in six
different temperatures (0°C, 10°C, 20°C, 30°C , 40°C and 50°C) for 14 days and 28 days period and
at the end of 14 days and 28 days they were analysed. The second part of the experiment was to fix
the room temperature as the storage temperature for these canned foods (25±2°C) and analysed on
7, 14, 21 and 28 days period. It was revealed that fermented food item (canned fermented durian)
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Journal of Advanced Biomedical & Pathobiology Research Vol.7 No.1, August 2017, 1-13
significantly has higher level of histamine over other preserved food items regardless of storage
temperature and period. In general, it was found that the storing time along with the increased
temperature increase the level of histamine in food items. In this study, we found that the stable
room temperature (25±2°C) under the dried conditions favours the most suitable for maintaining the
histamine level in food. Temperature variation revealed that has an impact over the increased
concentration of histamine in food items.
Key words: Biogenic amines, histamine, temperature, food toxicity, canned fruits, storage time
________________________________________________________________________________
1. Introduction
Histamine is one of the frequently occurring biogenic amines (BA) which are present naturally in
most of the food items. The nitrogen containing amines are formed majorly by decarboxylation of
amino acids or by amination and transamination of aldehydes and ketones (Maijala, RL. & Eerola,
1993). They are produced from histidine, tyrosine, ornithine, lysine, β-phenylalanine amino acids.
They are low molecular weight bases which are synthesized by microbial, vegetable and animal
metabolisms (Brink et al., 1990). These amines in food and beverages are formed by the enzymes of
raw material by naturally or are generated by microbial decarboxylation of amino acids when they
acted upon, but some of the aliphatic amines can also be formed by amination from equivalent
aldehydes (Maijala, RL. & Eerola, 1993). These BA’s are present in a wide range of food products,
including fish, meat, cheese, wine, beer, vegetables, fruits and nuts. In fermented foods their
presence is as a result of the fermentation process.
1.1 Importance of Histamine
Histamines are usually released by mast cells and basophils, and its biological effects are usually
seen in the course of allergic and other reactions. Histamine can cause pseudo-allergic reactions
meant to include the symptoms such as: urticaria, eczema, diarrorea, or spasm of bronchi etc.,
(Bardocz, 1993). There are 3 histamine receptors where they seen in epithelial cells of major organ
system. Histamine effect is applied only when they bind to the receptors on cellular membranes in
the major organ tissues. Skin rashes and itching is associated with the urticarial lesions due to
sensory and motor neuron stimulation (Karovicova J & Kohajdova Z, 2005). So the symptoms exert
according to the tissue type where they bind to the receptors.
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Journal of Advanced Biomedical & Pathobiology Research Vol.7 No.1, August 2017, 1-13
For example, it causes dilatation of blood vessels, capillaries and major arteries, thus resulting in
hypotension and headache. Histamine induces contraction of intestinal smooth muscles resulting in
abdominal cramps, diarrhoea, and vomiting. It also induces gastric acid secretion (Rice SL et al.,
1976).
The histamine toxicity can be well treated by using antihistamines drugs. Histamine is the most
toxic amine detected in food products (Brink et al., 1990; Huis in’t Veld et al., 1990). The
toxicological effect depends on histamine intake, presence of other different amines, amino oxidase
activity and the absorbing capacity of the individual intestine. If the concentration of amines is
above normal level which is usually determined by the various factors, harmful effects may occur
(Christine et al., 2007)
1.2 Histamine in Food
The concentration of histamine is used as a criterion of the quality of food. BA in food can be of
endogenous, which means that they were formed by metabolic conversion of the plant or animal
and thus they may be present in the raw material of the food or exogenous, which means that if
bacteria are the contaminant favor the histamine production and have even if they have been killed,
the enzyme activities still continue to produce it (Linares DM et al.,2012). Foods rich in proteins
such as fish, meat, and cheese as well as fruits and vegetables are regarded as histamine containing
products since fermentation of these increases the histamine production (Landete et al., 2005).
Endogenous origin of BAs are usually present in low concentrations in unfermented foods like
fruits and vegetables, meat, fish and milk (Önal A, 2007). Exogenous biogenic amines are the result
of microbial decarboxylation of free amino acids and are present in higher concentrations. Most of
the time the precursor amino acids were already present in the raw materials (Bodmer et al., 1999).
But there are many factors which contribute to increase the histamine concentration even if the
origin is of endogenous.
The storage time and temperature is considered as among the important factors in determining BAs
content. Increased temperatures and longer storage time yield higher amounts of biogenic amines. It
is also explained that Klebsiella pneumoniae produced more biogenic amines at 20°C than at 10°C
(Silla santos MH , 1996). Normally BA production is increased between 10°C and 37°C, and it can
be inhibited by storing less than 10°C. In general, the levels of BA will be lower in refrigerated
foods compared to the foods stored in increased temperature (Suzzi et al., 2003).
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Journal of Advanced Biomedical & Pathobiology Research Vol.7 No.1, August 2017, 1-13
At relatively high temperature, during fermentation favors the production of biogenic amines,
however perusal of report demonstrated that the effect of fermentation temperature is highly
dependent on the starter culture used (Maijala et al., 1995).
The detoxification mechanisms exist in our body is capable of metabolizing normal dietary
presence of biogenic amines in various foods which we consume daily. (Huis in’t Veld et al., 1990).
The dietary exogenous source of amines are absorbed from food are readily detoxified by the action
of group of enzymes called as amino oxidases or by conjugation reaction -one of the detoxification
reaction. There are certain circumstances where there is a presence of monoamine oxidase (MAO)
inhibitors, high level consumption and the issues in the detoxification process (defective enzymes
for detoxification or genetic causes) in an individual disturbs and as a result the biogenic amines
accumulate in the body. Amino oxidases are inducible enzymes in the presence of mono- or
diamines (Joanna Stadnik & Zbigniew J. Dolatowski, 2010). The enzymes MAO and di amino
oxidases play an important role in the detoxification process.
In this context, the study is focused to present an analysis on the histamine level in five categories
of preserved fruits and syrups in different brands which normally consumed by the people as
available in the major supermarkets in Malaysia (mango pickle, fermented durian, canned pineapple
syrup, canned rambutan syrup and canned lychee syrup). We also took two major factors (storage
temperature and storage period) which has an implications on our safety on consumption of food to
check their influence over the histamine content of the selected food items. The reason for our
analysis preferred on preserved fruits and syrups is that since they are the one which is commonly
consumed as such and regardless of age.
2. Materials and Methods
Enzymatic methods including radio immuno assays and enzyme-linked immunosorbent assay
system (ELISA) have been applied to detect histamine with the advantages of rapidity and not
requiring expensive instrumentation like HPLC (Stratton et al., 1991).
Enzyme-linked immunosorbent assay (ELISA) is a detection system based on the binding of an
antibody to an antigen and detection using an enzyme label. The enzyme acts on a colorless
substrate to give a colored product, which is readily detectable at specific wavelength. The
histamine detection kit was purchased from BioVision Company through the local supplier in Kuala
Lumpur, Malaysia.
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Journal of Advanced Biomedical & Pathobiology Research Vol.7 No.1, August 2017, 1-13
2.1 Sample Preparation
The method for amine determination involves enzymatic quantitative analysis, by using Histamine
assay kit which can be used to identify the levels of histamine in various fruit and vegetable
products, as well as other fermented foods. The histamine sample buffer was prepared according to
the guidelines given in the kit procedure in 1:1 ratio with 100% Methanol. The rambutan, pineapple
and lychee syrups were assayed directly. About 300 mg of pickled mango and fermented durian
were homogenized by using 1000 µl of histamine sample buffer. The samples were boiled for 10
min at 90°C in sealed tubes in a water bath, and then cooled on ice. They were centrifuged further at
10,000 X g for 5 min. supernatant was collected and was used for the assay.
2.2 Experimental Design
The 5 different chosen varieties of canned fruits (mango pickle, fermented durian, canned pineapple
syrup, canned rambutan syrup and canned lychee syrup) were bought from the super market in
Kuala Lumpur; Malaysia with the expiry date mentioned on it and was served as the sample for the
analysis.
They brought to the laboratory as unopened and on the day of purchase, they were opened and
analysed for histamine for the first time. Further they have portioned into 5, and each of the portion
was stored in six different temperatures (0°C, 10°C, 20°C, 30°C , 40°C and 50°C) for 14 days and
28 days period. At the end of 14 days and 28 days period the samples were taken out and analysed.
The second part of the experiment was to fix the room temperature as the storage temperature for
these canned fruits (25±2°C) and analysed on 7, 14, 21 and 28 days period. The following formula
was used to calculate the amount of histamine present in the canned fruit samples.
Eq.1: Concentration of histamine = B/V X D
Where ‘B’ is the amount of histamine in the sample well from standard curve (in nmol) ‘V’ is the
sample volume added into the reaction well (in µl) and ‘D’ is the sample dilution factor if any.
2.3 Statistical Analysis
Triplicate of each samples were analysed and used for further statistical analysis. The values were
expressed as mean± SD. Statistical analysis was done by using student’s t test. The results were
presented for discussion.
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Journal of Advanced Biomedical & Pathobiology Research Vol.7 No.1, August 2017, 1-13
3. Results and Discussion:
The histamine level (in triplicates) in the five canned food items we have chosen was carefully
analyzed by using the kit method based on immuno assay principle. After the food sample
extraction was done, the level of histamine was analysed and calculated. The level of histamine was
given in table I. It was found that the level of histamine in the mango pickle and fermented durian
were comparatively high among the selected canned food items and believed that the storage
temperature conditions played a major role on this. While picking up the items from the super
market, mango pickle and fermented durian were kept in the goods rack and it was at the normal
room temperature. The canned pineapple, rambutan and lychee syrups were stored and picked up
from the refrigerator showed the storage temperature of 180C.
Table I: Histamine level in sample triplicates (in mg/kg or mg/l) while at the time purchased
from the market. All values were expressed in mean ± SD.
The important consideration is amino acid decarboxylation and it is the major route of formation of
histamine and other biogenic amines (Shalaby, 1994). This reaction occurs through either by the
action of decarboxylase which is present naturally in food or by the microorganisms present in the
food items (Silla, 1993; Granata, 2012). It was also proven that the biogenic amines can also
produce by the addition of preservatives and other chemicals which are used extend their shelf life.
These are referred as potentiators which can be classified as either food borne putrefactive amines
or pharmacological agents (Stratton et al., 1991). Certain drugs like antihistamines, antimalarial
agents and other medications can inhibit histamine-metabolizing enzymes may be the reason to get
accumulated in our body (Brink et al., 1990; Stratton et al., 1991).
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Sample
Level of Histamine
Mango pickle (mg/Kg)
92.8±2.62
Fermented durian (mg/kg)
102.5±2.18
Canned pineapple syrup (mg/L)
15.4±0.2
Canned rambutan syrup (mg/L)
10.6±0.48
Canned lychee syrup (mg/L)
13.5±0.77
Journal of Advanced Biomedical & Pathobiology Research Vol.7 No.1, August 2017, 1-13
Table II: Histamine level in sample triplicates (in mg/Kg or mg/L) stored in different
temperatures for 14 days period. All values were expressed in mean ± SD (ND: Not detected).
Table II showed the results of histamine level in various temperatures which we commonly
preferred to store the food items (0oC – 50oC). We opened the canned food items for the first time
and aliquoted it , stored in the listed temperatures for 14 days period. Upon storing at different
temperature ranges, even at very low temperatures (0oC and 10oC mango pickle and fermented
durian, found that have significant level of histamines. The other three items we did not find any
histamine. It was found that the raising temperature ultimately increase the amount of histamine.
This may be constituted either by the action of microorganisms or by the chemical preservatives or
additives added to the food items oxidized and decarboxylated to produce the histamines and other
biogenic amines. The increase in temperature help the microorganisms to grow on it to produce the
biogenic amines thus the level of histamines was found to be increased. The level of histamine was
very high at 50oC for mango pickle and fermented durian and it was found 105.0±2.44 mg/Kg, and
147.3±2.98 respectively.
Sometime it is possible that these microorganisms either cause the microbiota of the product or may
be introduced before, during or after food processing (Rokka et al., 2004). Biogenic amines are
present in low concentrations are not detected in fresh food normally (Granata et al, 2012).
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Temperature
0°C
10°C
20°C
30°C
40°C
50°C
Sample
Mango pickle
(mg/Kg)
20.8±1.18
26.3±0.96
40.8±1.34
78.2±1.66
94.8±1.62
105.0±2.44
Fermented durian
(mg/Kg)
32.6±1.44
34.8±1.00
47.5±1.57
100.9±2.30
129.3±1.55
147.3±2.98
Canned pineapple syrup
(mg/L)
ND
ND
13.2±0.48
26.6±0.80
44.4±1.00
57.9±1.08
Canned rambutan syrup
(mg/L)
ND
ND
14.6±0.42
19.3±1.48
48.0±0.96
65.2±1.11
Canned lychee syrup
(mg/L)
ND
ND
12.2±0.7
23.9±1.27
37.39±1.06
57.2±0.92
Journal of Advanced Biomedical & Pathobiology Research Vol.7 No.1, August 2017, 1-13
Table III: Histamine level in sample triplicates (in mg/Kg or mg/L) stored in different
temperatures for 28 days period. All values were expressed in mean ± SD (ND: Not detected).
The selected canned food items stored in different temperatures for 28 days period revealed that at
0oC mango pickle and fermented durian have found 26.8±0.3 mg/Kg and 40.5±1.56 mg/Kg
respectively. In the other three items, histamine was not detectable. It was found that the raising
temperature along with the longer storage period influence the level of histamine even than stored
for 14 days period (Table III). The gradual increase in the histamine level was observed in canned
pineapple, rambutan and lychee syrup over the temperature with the longer duration of storage (28
days). This would be probably due to accumulation of biogenic amines; however the accumulation
of these amines in food depends primarily on the availability of free amino acids and the presence
of microorganisms. The micro organisms which have decarboxylases can easily generate the
biogenic amines. (Önal, 2007). The level of amines and different types are linked to the nature of
the food and type of microorganism present (Arena et al., 2001; Deng-Fwu Hwang et al., 1997). It
was observed from our study that fermented durian always maintained higher level of histamine
indicated that the presence of histamine producing micro organisms were high. Since the product
was fermented, they can possibly induce a chemical poisoning. This was also suggested from other
studies that food of animal origin such as seafood, meat and fermented foods, contains biogenic
amines in high concentration (Granata et al, 2012).
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Temperature
0°C
10°C
20°C
30°C
40°C
50°C
Sample
Mango pickle
(mg/Kg)
26.8±0.3
33.4±1.17
88±1.75
91.4±1.22
102.2±0.98
116.4±2.4
Fermented durian
(mg/Kg)
40.5±1.56
46.2±1.46
82.3±0.92
110.5±2.14
126.7±1.9
179.7±1.45
Canned pineapple syrup
(mg/L)
ND
8.2±0.64
18.6±1.4
22.2±0.8
50.4±1.55
66.3±1.77
Canned rambutan syrup
(mg/L)
ND
5.6±0.38
20.9±1.14
31.5±1.22
50.0±2.5
62.8±2.2
Canned lychee syrup
(mg/L)
ND
6.4±0.9
16.6±0.86
29.4±1.36
44.3±2.0
60.5±2.56
Journal of Advanced Biomedical & Pathobiology Research Vol.7 No.1, August 2017, 1-13
Table IV: Histamine level in sample triplicates stored in room temperature (25±2°C) for 7, 14,
21 and 28 days period. All values were expressed in mean±SD.
Table IV showed that the results of histamine level in canned food items stored at room temperature
in dry conditions were considerably better even though there was an increase in histamine level.
However this increment was within the legal limits of histamine for food consumption. The dry
conditions with the constant room temperature (25±2°C) had not giving any room to micro
organisms to grow on it even though they have stored for longer duration. On a trial we also
observed that if the temperature was not constant and variate typically the level of histamine was
high. (Data was not shown here). This indicated that the temperature was one of the most important
deciding factors to influence the histamine level. Microorganisms such as Lactobacillus, Aspergillus
niger and Trichosporon spp., carry the oxidase enzymes possible induce the decarboxylation which
lead to the synthesis of amines (Halhsz A. et al., 1994). Some types of yeasts were found in cheese
varieties are capable of assimilating cadaverine, putrescine and histamine (Taylor SL et al., 1978).
The toxic level of amines was very difficult to establish because it depends on various factors which
include principally individual characteristics and the presence of other biogenic amines like
putrescine and cadaverine. Earlier studies based on food borne histamine intoxication revealed that
the level of 1000 mg/Kg (amine/food) was considered as dangerous for health (Sumner S et al ,
1985). Literatures reported that the values of 100-800 mg/Kg for tyramine and 30 mg/Kg for phenyl
ethylamine have been considered as toxic doses in foods (Brink et al., 1990; Halhsz A et al., 1994).
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Days
7 days
14 days
21 days
28 days
Sample
Mango pickle
(mg/Kg)
22.3±0.3
55.1±1.37
70.3±2.62
88.2±1.08
Fermented durian
(mg/Kg)
35.5±1.0
69.3±1.5
72.7±1.7
89.5±2.0
Canned pineapple syrup
(mg/L)
11.4±0.74
18.6±1.8
19±0.86
19.7±1.66
Canned rambutan syrup
(mg/L)
11.6±1.85
16.8±1.42
18.9±1.47
25.1±0.92
Canned lychee syrup
(mg/L)
14.5±0.58
19.5±1.25
20.3±1.88
21.9±2.34
Journal of Advanced Biomedical & Pathobiology Research Vol.7 No.1, August 2017, 1-13
The European Community has recently proposed that the average content of histamine should not
exceed 10-20 mg/100 g of fish (Joosten, HMLJ & Northolt, MD 1987). Addition of nitrite to raw
meat possibly enhances the reactions with amines and amino acids present in meat (Shahidi et al.,
1993). Range between 100 to 200 mg/ kg is considered as the safest level for histamine in meat
products approved by the Netherlands Institute of Dairy Research and also by the Czech Republic
(Bunkova et al., 2013). A maximum limit of 100 mg histamine/Kg food and 2 mg/l in alcoholic
beverages have been suggested as safest level for histamine.
4. Conclusion
Histamine based food poisoning is the major concern over the consumption of canned foods
specially. There are many factors which contributed to the histamine food poisoning. Most of the
time it is contributed by the availability of precursor amino acids, food storage time, temperature,
pH, various cooking methods, oxygen tension, availability of carbon sources, presence of vitamins,
co-enzymes, concentration of free amino acids , potentiators and other fermentable carbohydrates .
If the amines and the factors responsible for increasing amines are optimal and the individual is not
allergic to histamine, the consumed food would not cause any problems to the health. In this study,
we found that the stable room temperature under the dried conditions favours the most suitable for
maintaining the histamine level in food. Temperature variation revealed that has an impact over the
increased concentration of histamine in food items. It was also revealed that fermented food item
(canned fermented durian) significantly has higher level of histamine over other preserved food
items. Storing time along with the increase temperature overall increase the level of histamine in
food items. Thus, the main factors that influence the biosynthesis of amine compounds are storage
time and conditions, temperature as well as good manufacturing practices which principally make
them to keep within the safety level. A better knowledge of these factors controlling amines
formation is necessary in order to improve the quality and safety of canned food items.
Conflict of interest:
Nil
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Journal of Advanced Biomedical & Pathobiology Research Vol.7 No.1, August 2017, 1-13
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