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Effects of onion or caraway on the formation of biogenic amines during sauerkraut fermentation and refrigerated storage
Food Chemistry 298 (2019) 125083
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Effects of onion or caraway on the formation of biogenic amines during sauerkraut fermentation and refrigerated storage
T
Jagoda Majcherczyk , Krzysztof Surówka ⁎
Department of Refrigeration and Food Concentrates, Faculty of Food Technology, University of Agriculture in Krakow, 122 Balicka Street, 30-149 Cracow, Poland
ARTICLE INFO
ABSTRACT
Chemical compounds: Putrescine (PubChem CID1045) Cadaverine (PubChem CID273) Spermidine (PubChem CID1102) Spermine (PubChem CID1103) Histamine (PubChem CID774) Tyramine (PubChem CID560) Phenethylamine (PubChem CID1001) Tryptamine (PubChem CID1150) Serotonin (PubChem CID5202)
The effects of onion or caraway on changes in the content of biogenic amines were examined in sauerkraut during a fermentation process at 18 °C or 31 °C for 14 days and subsequent storage at 4 °C for 12 weeks. The amines were analysed by high-performance liquid chromatography with pre-column benzoylation. Total biogenic-amine concentration at the end of the fermentation was lower at 31 °C than at 18 °C. However, at this lower temperature, the presence of caraway or onion more significantly (than at 31 °C) reduced the total biogenic-amine content as compared to the control sample without an additive. After 12 weeks of refrigerated storage, concentrations of phenethylamine, tryptamine, and tyramine in the sauerkraut fermented with caraway (and concentrations of putrescine and tryptamine in the sauerkraut fermented with onion) at 31 °C increased as compared to the samples on the last day of fermentation, but did not pose a risk for consumer health.
Keywords: Sauerkraut Fermentation Biogenic amine Caraway Onion
1. Introduction Sauerkraut is one of the most traditional fermented products in many European countries, especially popular in the diet of the inhabitants of Central and Eastern regions of this continent. Sauerkraut is prepared by spontaneous lactic acid fermentation of shredded and salted cabbage, but varieties of sauerkraut can be a result of addition of some spices or ingredients (linked to a specific geographic area) during the fermentation. Sauerkraut is a rich source of minerals and vitamins and contains autochthonous lactic acid bacteria, some of which possess probiotic properties. Moreover, during fermentation of white cabbage, some glucosinolates contained in cabbage are transformed into ascorbigen, which has substantial anticarcinogenic activity (Beganović et al., 2014; Martinez-Villaluenga et al., 2009; Šamec, Pavlović, & SalopekSondi, 2017; Tamang, Shin, Jung, & Chae, 2016). The fermentation process can be implemented in two ways. The first type is initiated spontaneously by the natural bacterial population of the raw material, and the second one is conducted with certain selected lactic acid bacteria as inoculants. The use of starter cultures ensures
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control of the fermentation process, whereas during the spontaneous process, there is limited control of the quality and safety of the final product. Moreover, certain additives such as spices can change the conditions of fermentation, thus possibly leading to an increase or decrease in the amounts of some endogenous compounds such as biogenic amines in the final product (Kuley et al., 2012; Zhou, Qiu, Zhao, Lu, & Ding, 2016). Biogenic amines are basic nitrogenous compounds that can be found in a variety of foods, such as meat, fish, cheese, vegetables, wines, and soy sauce (Dong & Xiao, 2017). They can be formed by the enzymes of a raw material or generated by microbial decarboxylation of amino acids (Biji, Ravishankar, Venkateswarlu, Mohan, & Gopal, 2016; Halász, Baráth, Simon-Sarkadi, & Holzapfel, 1994;). Factors that promote microbial activity are substrate and water availability, pH of the environment, salt concentration, and temperature (Jairath, Singh, Dabur, Rani, & Chaudhari, 2015). Several authors have reported the presence of putrescine, cadaverine, spermidine, spermine, histamine, tyramine, phenethylamine, and tryptamine in fermented food products (Alvarez & Moreno-Arribas, 2014; Dong & Xiao, 2017). The initial concentration of
Corresponding author. E-mail addresses: [email protected] (J. Majcherczyk), [email protected] (K. Surówka).
https://doi.org/10.1016/j.foodchem.2019.125083 Received 25 November 2018; Received in revised form 14 June 2019; Accepted 25 June 2019 Available online 26 June 2019 0308-8146/ © 2019 Elsevier Ltd. All rights reserved.
Food Chemistry 298 (2019) 125083
J. Majcherczyk and K. Surówka
biogenic amines in the fresh products is usually low. The formation of these compounds is related to the type of treatment a raw material is subjected to as well as storage conditions and duration. For example, Kosson and Elkner (2010) reported that fresh cabbage contains only putrescine and spermidine at very low levels (under 2 and 10 μg g−1, respectively). During its fermentation, four additional biogenic amines appear, and in most cases, their concentration increases with time. Even though fermented products have many beneficial effects on health, biogenic amines that are present in them can have a toxic effect on the human body. Biotransformation of these compounds is mainly performed by monoamine oxidase and diamine oxidase. People whose mechanism of detoxification is defective and those who take monoamine oxidase- or diamine oxidase-inhibiting drugs are particularly vulnerable to the presence of biogenic amines in food. Excessive intake of these compounds, especially histamine and tyramine, exerts many psychoactive and vasoactive effects (Naila, Flint, Fletcher, Bremer, & Meerdink, 2010; Stadnik & Dolatowski, 2010). Currently, there are no regulatory standards for toxic levels of biogenic amines. Histamine and tyramine are considered the most toxic. Based on the literature, the levels of 25 to 50 mg of histamine and 600 mg of tyramine per meal have no adverse effect on a healthy person (EFSA, 2011). Determination of the exact toxic limits of the rest of the biogenic amines is difficult because the toxic dose is dependent on the detoxifying mechanisms in different individuals (Önal, 2007). It has been found that the use of certain additives in food can inhibit the formation of biogenic amines (Kuley et al., 2012). Mah, Kim, and Hwang (2009) reported that addition of a garlic extract to fermented anchovy decreases levels of these compounds by as much as 18.4% in comparison to a control sample. An excellent review on the occurrence and reduction of biogenic amines in fermented Asian soybean foods was published recently (Park, Lee, & Mah, 2019). Nonetheless, there is no information in the freely available literature about the effects of various ingredients, such as spices, herbs, or other plant products, on biogenicamine formation during sauerkraut production. Conducting a process of sauerkraut fermentation in the presence of onion or caraway gives the final product new original sensory features. The objective of this study was to determine the impact of these additives on the chemical composition of the final products immediately after fermentation and during subsequent refrigerated storage. It was assumed that both additives, in the fermentation process conducted at one of two temperatures (18 °C ± 1 °C or 31 °C ± 1 °C), and during refrigerated storage (4 °C ± 1 °C), can influence the concentrations of the eight most frequently occurring biogenic amines (Doeun, Davaatseren, & Chung, 2017). Chemical compounds belonging to the alkylthiosulphonate class in onion and the terpenoid family in caraway can cause a decrease in the concentration of biogenic amines in the final product by affecting the activity of microorganisms (Ma et al., 2018; Sharma, Mahato, & Lee, 2018; Thippeswamy, Naidu, & Achur, 2013).
NaCl concentration was 2.5%, and the caraway seed and shredded onion supplementation of the selected samples amounted to 10 and 350 g/(kg of sauerkraut), respectively. The closed jars were incubated for fermentation at 18 °C ± 1 °C or 31 °C ± 1 °C via the following scheme: the control group (only 2.5% NaCl), group with caraway (2.5% NaCl + caraway), and the group with onion (2.5% NaCl + onion). Spontaneous fermentation was carried out for 14 days. Then, all jars were placed in a refrigerator at 4 °C ± 1 °C and stored for 12 weeks. pH, total acidity, and biogenic-amine concentrations as well as sensory quality were analysed at the following time points: a fresh sample; after the 3rd, 7th, and 14th day of fermentation; and after the 2nd and 12th week of storage. 2.3. Physicochemical measurements pH of the sauerkraut was measured by directly inserting the combined pH electrode (Elmetron, Poland) into a jar containing the product, whereas total acidity was measured by titration of a product homogenate with 0.1 mol L−1 NaOH according to AOAC procedures (AOAC, 2007) and was expressed in milligrams of lactic acid per 100 g of sauerkraut. 2.4. Determination of biogenic amines Biogenic-amine standards (putrescine dihydrochloride, cadaverine dihydrochloride, spermidine trihydrochloride, spermine tetrahydrochloride, histamine dihydrochloride, tyramine hydrochloride, phenethylamine, tryptamine hydrochloride, and serotonin hydrochloride) and a 99% benzoyl chloride solution were purchased from Sigma-Aldrich (Germany). The purity levels of all the standards were higher than 99%. Stock standard solutions of the amines were prepared by dissolving an accurately weighed amount in 10 mL of high-performance liquid chromatography (HPLC) grade water. All the solvents used were HPLC grade. Concentrations of eight biogenic amines (putrescine, cadaverine, spermidine, spermine, histamine, tyramine, phenethylamine, and tryptamine) in the raw cabbage and sauerkraut samples were measured by trichloroacetic acid (TCA) extraction, derivatisation with benzoyl chloride, and HPLC quantification according to Özogul, Taylor, Quantick, and Özogul (2002) with slight modifications. Each sample (5 g) was homogenised with 20 mL of 6% TCA, then centrifuged at 10000×g for 10 min and passed through filter paper. The collected supernatant was diluted to 50 mL with distilled water. After that, a 2 mL aliquot of a sample was spiked with 1 mg mL−1 serotonin (50 μL) as an internal standard and alkalinised with 1 mL of 1 mol L−1 NaOH. For derivatisation, 20 μL of benzoyl chloride was added, and the reaction mixture was incubated at 24 °C ± 1 °C for 30 min. From the individual amines, corresponding N-benzamides formed as a result of the Schotten–Baumann reaction. The reaction was stopped by adding 2 mL of a saturated sodium chloride solution, and each sample was extracted twice with 2 mL of diethyl ether. Next, combined organic layers were evaporated to dryness in a nitrogen stream. The residue was dissolved in 1 mL of acetonitrile (Merck, Germany), passed through a 0.45 μm syringe filter (Millipore, USA), and 10 μL of the resultant sample was loaded on an HPLC column. Three separate analyses of each sample were carried out. HPLC analysis was performed on a Merck Hitachi LaChrom HPLC System with a diode array detector. Separation of analytes was carried out on an ACE 3C-18 column (150 × 4.6 mm) at 30 °C via gradient elution with acetonitrile and HPLC grade water (Polwater, Poland). The elution started with 40% of acetonitrile and was ramped to 75% (13 min) and then to 100% (3 min) at a flow rate 1 to 1.5 mL min−1 within 16 min. Detection was conducted at 254 nm. Calibration curves for each amine standard were constructed in the range 2–100 µg mL−1. Quantitative analysis of biogenic amines was performed by an external calibration curve method with serotonin as the internal standard (50 µg mL−1). The essential validation parameters of the method for separation and quantification of biogenic amines
2. Materials and methods 2.1. Plant material Heads of white cabbage (Brassica oleracea L. var. capitata L.) were purchased at a local supermarket and stored in wooden containers for less than 2 days at 4 °C in the dark until analysis. Caraway seeds (Carum carvi L.) and onion (Allium cepa L.) were purchased from a retail shop. 2.2. Sauerkraut production From the heads of white cabbage, the outer leaf layer was removed, and the heads were sliced to a thickness of 3–5 mm. The sliced cabbage was evenly mixed with NaCl, then the whole mixture was divided into three parts: caraway seeds were added to the first, shredded onion to the second, and the third one, without additives, was treated as a control. These mixtures were packed tightly into glass jars. The final 2
Food Chemistry 298 (2019) 125083
J. Majcherczyk and K. Surówka
were as follows: linearity of the calibration curves was observed in the range of 2–100 μg mL−1 with a correlation coefficient of greater than 0.995. Limits of detection (LOD) and limits of quantification (LOQ) for all compounds were calculated and turned out to be in the ranges of 0.16–3.02 and 0.53–10.07 μg mL−1, respectively. Total biogenic-amine concentration was calculated as the sum content of the eight assayed amines.
Table 2 Changes in pH and total acidity (mg 100 g−1) of sauerkraut with a different additive after preparation at different temperatures (18 °C ± 1 °C or 31 °C ± 1 °C) during storage at 4 °C ± 1 °C. Composition
Control (NaCl only)
NaCl + caraway
NaCl + onion
Production temperature
18 °C
31 °C
18 °C
31 °C
18 °C
31 °C
3.58b 2425b
4.09a 950c
4.36c 1075d
4.20d 850e
3.78e 1875f
3.73b 2700b
4.42c 1175c
4.46c 1300d
4.46c 1425e
3.98d 2325f
3.06b 2775b
3.92c 1200c
3.74d 1625a
3.63d 1300d
3.34e 2625e
2.5. Sensory analysis pH Total acidity
This analysis of sauerkraut during the fermentation process and refrigerated storage was performed according to the Polish standard (Polish Standardization Committee, 1990) by a panel of six trained people. The panel members were asked about the colour, taste, odour, consistency, and appearance of the juice released. A scale from 1 to 5 was employed for each feature, where 5 was the best and 1 was the worst. For each quality feature, scores given by the six panellists were totalled, and the mean was calculated. The overall sensory quality was obtained as the sum of means of all features multiplied by an individual weighting factor (colour: 0.2, taste: 0.3, odour: 0.3, consistency: 0.1, and the appearance of juice released: 0.1).
pH Total acidity pH Total acidity
immediately after production 4.10a 1250a after 2 weeks of storage 4.15a 1625a after 12 weeks of storage 3.60a 1625a
Mean values marked with the same letter in a row do not differ significantly (p ≥ 0.05).
conditions; however, at the beginning of the process (3rd day), the presence of caraway or onion in the samples fermented at the same temperature generally did not influence the measured parameters, which means that the changes were caused mainly by the temperature. These results are consistent with the findings of Halász, Baráth, and Holzapfel (1999), who reported a greater pH drop at 30 °C than at 11 °C, after 96 h of sauerkraut fermentation. After 7 days of the process, an effect of supplementation with the additives on acidity and pH was observed. Statistically significant differences in pH were noted only at 31 °C, but acidity values were clearly different at both temperatures. At the end of the fermentation, the control sample showed the highest acidity and the lowest pH, suggesting that onion and caraway can (separately) exert inhibitory effects on the fermentation process.
2.6. Statistical methods To obtain the results, the mean ± standard deviation of triplicate determinations were computed. The significance of differences was determined by 2-way analysis of variance (ANOVA) with the least significant difference (LSD) post hoc test and contrast analysis. All statistical data were obtained in the Statistica software, ver. 12 package (StatSoft, Cracow, Poland). A p value less than 0.05 was assumed to indicate a significant difference. 3. Results and discussion 3.1. The influence of fermentation conditions on pH and acidity of sauerkraut
4. The impact of storage duration on the pH and acidity of sauerkraut
Table 1 shows the pH and total acidity values both in the raw cabbage and during the fermentation process at 18 °C or 31 °C in three groups: control (only NaCl) and with an additive (NaCl + caraway or NaCl + onion). Although the 3-day period of fermentation at 18 °C caused some slight increase in pH and a decrease in total acidity as compared to raw cabbage, a significant decrease in pH and an increase in acidity at 31 °C were observed. After 7 or 14 days at both applied fermentation temperatures, there was a further pronounced increase in acidity and a pH drop. This tendency was especially clearly visible in the control group (NaCl only), where at 31 °C, pH decreased by ∼40% and acidity increased more than six-fold on the 14th day of fermentation as compared to the raw cabbage. There were also many significant differences in pH and acidity of sauerkraut produced under various
Changes in the pH and total acidity of sauerkraut, seen under the six conditions (two temperatures and three recipes) mentioned above, after storage at 4 °C ± 1 °C for 2 and 12 weeks, are presented in Table 2. During the first 2 weeks of refrigerated storage, a slight increase in pH was observed, accompanied by an increase in acidity. The greatest growth of this parameter was detected in the sauerkraut with onion fermented at 31 °C; this parameter was 24% greater in relation to the sample immediately after fermentation. During the comparison of samples treated with caraway or onion and samples without either, a clear influence of each additive on pH and acidity after 12 weeks of storage was observed. The two measured parameters – pH and acidity –
Table 1 Changes in pH and total acidity (mg 100 g−1) in sauerkraut during fermentation processes at 18 °C ± 1 °C or 31 °C ± 1 °C. Composition
Raw cabbage
Fermentation temperature
Control (NaCl only)
NaCl + caraway
18 °C
pH Total acidity
5.89a 390a
pH Total acidity
5.89a 390a
pH Total acidity
5.89a 390a
after 3rd day of fermentation 6.32b 375a after 7th day of fermentation 4.25b 1175b after 14th day of fermentation 4.10b 1250b
Mean values marked with the same letter in a row do not differ significantly (p 0.05). 3
NaCl + onion
31 °C
18 °C
31 °C
18 °C
31 °C
4.48c 825b
6.25b 375a
4.45c 825b
6.17b 375a
4.71d 800b
4.39c 950c
4.33b,c 800d
4.23b 1075e
4.30b 1075e
3.69d 1975f
3.58c 2425c
4.09b 950d
4.36d 1075e
4.20e 850f
3.78f 1875g
Food Chemistry 298 (2019) 125083
J. Majcherczyk and K. Surówka
Fig. 1. Separation of biogenic amines extracted from sauerkraut fermented with caraway at 31 °C and stored for 12 weeks at 4 °C. ID numbers of amines: 1, putrescine; 2, cadaverine; 3, spermidine; 4, tyramine; 5, phenethylamine; 6, spermine; 7, histamine; 8, internal standard (serotonin); and 9, tryptamine.
were the lowest and highest, respectively, for the sauerkraut treated only with NaCl. This finding may indicate that the inhibitory effect of caraway and onion seen during fermentation also occurs during refrigerated storage of the products. The pH value obtained after 12 weeks of storage for control samples fermented at 18 °C was congruent with the results obtained by Kalač, Špička, Křížek, and Pelikánová (2000) and Rabie, Siliha, El-Saidy, El-Badawy, and Malcata (2011) during sauerkraut storage under similar fermentation conditions.
process regardless of temperature. Similarly, an inhibitory effect of green onion on tyramine production in fermented anchovy was reported by Mah et al. (2009). Moreover, it was noted here that the concentrations of cadaverine and tyramine generally were lower at a higher temperature of fermentation. The lower cadaverine concentration obtained at the higher temperature is in agreement with the results of Cvetković et al. (2015). There, this tendency was independent of the varieties of cabbage, salt concentration, and duration of fermentation. During fermentation, a decreasing tendency of spermine content in the samples fermented at 18 °C and a slight increase at 31 °C were observed. Spermidine levels decreased at both fermentation temperatures. There were no significant differences between samples with and without an additive. The content of histamine in sauerkraut was generally at a similar level with the exception where caraway was added and fermentation was conducted at 18 °C. The determined amount of histamine was higher than that reported by other authors (Peñas et al., 2010; Cvetković et al., 2015), but the concentration of this amine was still lower than the maximal level (100 mg kg−1) allowed in foods (Halász et al., 1999). Onion manifested the greatest inhibitory effect on the accumulation of four (cadaverine, spermine, phenethylamine, and tyramine) out of the eight biogenic amines in the sauerkraut fermentation process, especially at 18 °C. This impact may be related to the antimicrobial activity of onion because biogenic amines are formed by microbial enzymatic activity (Santas, Almajano, & Carbó, 2010; Sharma et al., 2018). Even though the compounds present in caraway also possess antimicrobial activities (Thippeswamy et al., 2013), an inhibitory effect on biogenic-amine levels was observed only for cadaverine and tyramine after 7 days of fermentation. Total biogenic-amine concentrations in control samples after 14 days of the process at 18 °C or 31 °C were 102.65 and 82.49 mg kg−1, respectively. The effect of caraway and onion at the lower temperature was a decrease in this index by 13.3% and 18.8%, respectively. Significantly smaller changes (by 3.8% and 3.9%) were recorded in the fermented products with each of these additives at 31 °C.
4.1. The influence of fermentation conditions on the formation of biogenic amines Fig. 1 depicts a typical chromatogram of separation of biogenic amines extracted from sauerkraut in the form of their benzoyl derivatives. Changes in the formation of these compounds during preparation of sauerkraut are given in Table 3 for fermentation at 18 °C or 31 °C, in the presence of caraway or onion as an additive to cabbage with NaCl. According to the experimental results, fresh cabbage contained all the analysed amines in the range from 2.52 mg kg−1 (tryptamine) to 16.39 mg kg−1 (spermine), and the total content of biogenic amines was ∼76 mg kg−1, which is similar to the data obtained by other authors (Peñas, Frias, Sidro, & Vidal-Valverde, 2010; Rabie et al., 2011). On the other hand, Kosson and Elkner (2010), who applied the same derivatisation technique as the one used here, detected only putrescine and spermidine in cabbage. Fermentation for 14 days at 18 °C with or without caraway or onion caused no significant changes in the putrescine level, but at 31 °C, an increase was observed. At 18 °C, cadaverine, tryptamine, and tyramine showed a slow but significant rise of concentrations with fermentation time, and these concentrations were two- or threefold higher than those registered in the raw cabbage. In some cases, a similar tendency was observed in the sauerkraut prepared at 31 °C. The inhibitory effect of the addition of caraway or onion on the formation of cadaverine and tyramine, especially at the lower temperature, can also be seen. The sauerkraut that was produced without any additives contained significantly higher concentrations of the discussed amines than did the sauerkraut with one of the additives. Besides, the level of cadaverine determined in samples fermented with onion did not change during the 4
Food Chemistry 298 (2019) 125083
J. Majcherczyk and K. Surówka
Table 3 Changes in biogenic-amine concentrations (mg kg−1) in sauerkraut during fermentation processes at 18 °C ± 1 °C or 31 °C ± 1 °C with a different additive. Composition
Control (NaCl only)
Duration of fermentation (days)
18 °C
Putrescine 0 3 7 14 Cadaverine 0 3 7 14 Spermidine 0 3 7 14 Histamine 0 3 7 14 Phenethylamine 0 3 7 14 Tryptamine 0 3 7 14 Spermine 0 3 7 14 Tyramine 0 3 7 14
6.72 7.16 7.03 6.79
± ± ± ±
0.40 0.13A 0.23A 0.16A,C
6.83 ± 0.57a 7.12 ± 0.40a 14.39 ± 0.51b,A 15.34 ± 0.44b,A 14.51 13.67 12.64 11.92
± ± ± ±
0.47a 0.19a,c,A 0.54b,c,A 0.28b,A
NaCl + caraway 31 °C
18 °C
6.72 ± 0.40a 9.74 ± 1.76b,B 10.79 ± 2.20b,B 9.98 ± 0.48b,B
6.72 7.26 6.33 7.62
6.83 6.87 8.70 7.11
± ± ± ±
14.51 13.10 12.47 12.22
0.57a 0.75a 1.53b,B 0.40a,B
± ± ± ±
0.47a 1.86a,b,A 1.48b,A 0.63b,A
± ± ± ±
0.40 0.18A 0.33A 0.43A
6.83 ± 0.57a 7.48 ± 0.46a,b 8.49 ± 1.57b,B,C 12.00 ± 1.25d,C 14.51 14.06 10.15 11.90
± ± ± ±
0.47a 2.10a,A 0.82b,B 0.40c,A
NaCl + onion 31 °C
18 °C
6.72 ± 0.40a 7.31 ± 0.83a,A 7.26 ± 0.42a,A 10.13 ± 0.94b,B
6.72 6.73 6.73 6.39
± ± ± ±
0.40 0.25A 0.10A 0.07C
6.72 ± 0.40a 7.44 ± 0.15a,A 10.04 ± 0.57b,B 8.37 ± 0.21b,D
0.57a 0.41a,b 0.70b,B,C 0.27a,b,B
6.83 6.61 6.94 6.99
± ± ± ±
0.57 0.11 0.28C 0.12B
6.83 7.00 6.83 7.20
6.83 6.95 7.89 7.23
± ± ± ±
14.51 10.91 11.10 14.45
± ± ± ±
0.47a 1.00b,B 0.19b,A,B 0.49a,B
31 °C
14.51 14.93 12.06 13.07
± ± ± ±
0.47a,c 0.18a,A 0.12b,c,A 0.49c,C
9.07 8.71 9.13 8.23
± ± ± ±
0.54 0.13A 0.52A 0.07A
9.07 8.36 8.87 9.36
± ± ± ±
0.54 0.11A 0.64A,B 0.19B
9.07 ± 0.54a 9.61 ± 1.01a,B 12.50 ± 0.4b,C 10.28 ± 0.97a,B
9.07 8.20 8.61 9.90
± ± ± ±
0.54 0.20A 0.32B 0.77B
9.07 ± 0.54 8.85 ± 0.39A,B 10.78 ± 0.76A 8.74 ± 0.28A
7.41 5.70 8.07 8.37
± ± ± ±
0.21a 0.10b,A 0.78a,A,B 0.43a,A
7.41 6.74 7.13 6.23
± ± ± ±
0.21 0.29B 0.91A 0.24B
7.41 5.75 7.09 8.70
± ± ± ±
0.21a,b,c 1.54a,A 0.03b,A 1.40c,A
7.41 5.56 7.63 6.33
± ± ± ±
0.21a,c 0.43b,A 0.92c,A 038a,b,B
7.41 5.50 9.29 6.47
± ± ± ±
2.52 2.52 2.75 6.50
± ± ± ±
0.39a 0.55a,A 0.46a,A 0.94b,A
2.52 1.11 3.67 9.16
± ± ± ±
0.39a,c 0.63a,A 1.65c,A,B 0.40b,B
2.52 1.54 2.23 6.73
± ± ± ±
0.39a 0.49a,A 1.37a,A 1.95b,A
2.52 4.33 4.09 3.70
± ± ± ±
0.39a 1.61b,B 1.42a,b,B 0.25a,b,C
2.52 2.26 2.65 8.62
± ± ± ±
± ± ± ±
14.51 12.81 11.49 13.11
0.57 0.16 0.20C 0.17B
± ± ± ±
0.47a 0.22b,A,B 0.52b,A 0.47a,b,C
9.07 8.59 9.29 9.01
± ± ± ±
0.54 0.26A 0.32A,B 0.59A,B
0.21a 0.35b,A 0.46c,B 0.88a,b,B
7.41 7.89 7.20 5.98
± ± ± ±
0.21a,b 0.26a,C 0.42a,A 0.14b,B
0.39a 0.58a,A 0.35a,A 0.38b,A
2.52 ± 0.39a 8.61 ± 1.74b,C 10.38 ± 0.53c,C 4.35 ± 0.77d,C
16.39 14.67 15.39 15.67
± ± ± ±
1.46a 0.19b,A 0.52a,b,A 0.44a,b,A
16.39 15.62 15.01 16.78
± ± ± ±
1.46a,b 0.09a,b,B 0.54a,A 0.65b,A
16.39 14.68 15.05 15.51
± ± ± ±
1.46a 0.04b,A 0.97a,b,A 0.92a,b,A
16.39 15.83 15.62 17.66
1.46a,b 0.43a,B 0.13a,A 2.32b,B
16.39 15.31 14.91 14.85
± ± ± ±
1.46a 1.12a,b,A,B 0.07b,A 0.32a,b,A
16.39 15.74 18.23 16.78
± ± ± ±
1.46a 0.16a,B 0.65b,B 0.82a,A,B
12.72 14.34 21.49 29.83
± ± ± ±
0.41a 0.30a,A 4.23b,A 0.57c,A
12.72 13.87 14.63 11.65
± ± ± ±
0.41a 1.52a,c,A 1.12b,c,B 0.86a,B
12.72 17.22 17.39 16.28
± ± ± ±
0.41a,b 1.67b,c,B 1.90b,B 1.60b,C
12.72 ± 0.41a 9.04 ± 0.02b,C 12.82 ± 0.40a,B 16.23 ± 3.96c,C
12.72 14.44 13.68 18.26
± ± ± ±
0.41a 2.69a,A 1.33a,A,B 0.88b,C
12.72 12.50 10.88 13.78
± ± ± ±
0.41 0.55A 1.24B 0.68B
± ± ± ±
Mean values for an amine marked with the same superscript or not marked at all in the column do not differ significantly (p ≥ 0.05). Mean values marked with the same capital letter or not marked at all in the row do not differ significantly (p ≥ 0.05).
4.2. The impact of storage duration on the biogenic amines in the sauerkraut
caraway or onion, levels of the amines (phenethylamine, tryptamine, and tyramine for caraway, and putrescine and tryptamine for onion) were significantly higher than those in the control. These results are consistent with the data of Kalač et al. (2000), who reported that during 4 months of sauerkraut storage, the change in tyramine concentration increased more than 3-fold. Nonetheless, our study revealed a similar tendency, but the change in the amount of the above-mentioned amine was much smaller in the samples with an additive. These data may mean that the inhibitory effect persisted even a few weeks after the fermentation. At the end of the storage (after 12 weeks), concentrations of putrescine, cadaverine, phenethylamine, and spermidine significantly increased in the samples fermented with caraway at 18 °C; however, they did not exceed the values of the control. During the storage, histamine was detected in every sample of sauerkraut. However, after 2 weeks, the concentration of this amine obtained at 31 °C in the samples without an additive was significantly lower as compared with the beginning of the storage. This tendency for the samples fermented at the higher temperature with caraway was observed after 12 weeks too. No significant differences (p greater than 0.05) in the amount of cadaverine from samples fermented at 31 °C were detected between sauerkraut with or without an additive and the control samples.
Changes of biogenic amines in sauerkraut fermented under different conditions (temperatures and additives) and stored at 4 °C for 12 weeks are given in Fig. 2. Samples of sauerkraut on the last day of fermentation were regarded as the control (storage time = 0 weeks). Even though all the samples were stored at the same temperature, different tendencies of changing levels of biogenic amines quantified in sauerkraut fermented at 18 °C and 31 °C were observed. This finding is probably due to the differences in acidity and pH among individual products, as a result of bacterial growth, and consequently affects the activity of decarboxylases. After the first 2 weeks of refrigerated storage, the sauerkraut obtained at lower temperature contained lower amounts of five compounds (cadaverine, spermidine, phenethylamine, spermine, and tyramine) as compared to the control. These reductions were approximately two- or three-fold for spermidine and spermine contents, detected in sauerkraut fermented with or without an additive, respectively. The rest of the mentioned amines showed a similar decreasing tendency, whereas for tyramine, this tendency was observed only in the sample without an additive. During the storage (4 °C ± 1 °C), a tendency for increasing amounts of putrescine, tryptamine, phenethylamine, and tyramine was observed in the sauerkraut obtained at 31 °C. Especially for the samples with 5
Food Chemistry 298 (2019) 125083
J. Majcherczyk and K. Surówka
Cadaverine
Putrescine 14
b
12
a
8
a
a
a,b
a,b b
b
a
10
18 16
a a
14
b b
12
b
10
a
8
6
6
4
4
2
2 0
0
2
0
2
01
12
Spermidine 16 14 12
a
b
b
Phenethylamine
a
12
a
a
a a
a
a
10
b
10
b b b
8
b
b
12
b
a
a a
b
8
b b b
b
b
a
Fig. 2. Effects of duration of storage (at 4 °C ± 1 °C) of the sauerkraut obtained with different additives at 18 °C ± 1 °C or 31 °C ± 1 °C on concentrations of eight biogenic amines. Production temperature and the additives were as follows: 18 °C; 2.5% NaCl 18 °C; 2.5% NaCl; caraway 18 °C; 2.5% NaCl; onion 31 °C; 2.5% NaCl 31 °C; 2.5% NaCl; caraway 31 °C; 2.5% NaCl; onion. Mean values for an amine marked with the same letter in a graph or not marked at all for the product obtained at the same temperature and additive do not differ significantly (p ≥ 0.05).
a
a
b b
a a
6
6
4
4 2
2 0
0 1
0
12
2
Histamine
Tryptamine
Concentration (mg kg-1)
12
2
01
10
14
b
b b
b
8
12
a
10 6
a
8
a a
4
a
b b
b
6 4
2
2
0
18 16
a a
a
a
14 12
c
10
b b b b b b
b
c b b
6 4 2 0
0 1
2
12
2
Tyramine
a
8
01
Spermine
a
20
0
12
2
0 1
12
b
32 30 28 26 24 22 20 18 16 14 12 10 8 6 4 2 0
a
a
01
a,b
b
2
b
b
12
Storage time (weeks) 18°C; 2.5% NaCl 31°C; 2.5% NaCl
18°C; 2.5% NaCl; caraway 31°C; 2.5% NaCl; caraway
18°C; 2.5% NaCl; onion 31°C; 2.5% NaCl; onion
4.3. Sensory quality
changed the least. This trend also persisted throughout the 12-week storage period at 4 °C. The overall sensory quality of the samples obtained at 18 °C with caraway was higher than that with onion and lower than that in the control. The results indicated that the addition of caraway affected the sensory features of sauerkraut to a lesser extent than onion did.
This quality of sauerkraut is usually determined during the fermentation process, and after its completion, the product should retain good features during refrigerated storage. In Table 4, overall sensory quality scores are presented for the products with NaCl only or with caraway or onion. According to the members of the evaluation panel, starting from the 7th day, the quality of sauerkraut fermented at 31 °C was generally worse than that of the respective products at 18 °C. Sauerkraut obtained at 31 °C with caraway or onion was characterised by a too intense odour and taste; this result was the main reason for the lower ratings, while the colour and appearance of the juice released
5. Conclusion To prevent or reduce formation and accumulation of biogenic amines in food, the decarboxylase activity should be limited by means of a microbial starter preventing their production or via application of 6
Food Chemistry 298 (2019) 125083
J. Majcherczyk and K. Surówka
Table 4 Overall sensory quality of the sauerkraut during preparation and refrigerated storage. Variant
Control (NaCl only)
Fermentation temperature
18 °C
Fermentation
after 3rd day of fermentation 4.1 ± 0.08a 4.4 ± 0.21a after 7th day of fermentation 4.4 ± 0.11b,d 3.7 ± 0.14b after 14th day of fermentation 4.8 ± 0.12c 4.4 ± 0.14a after 2 weeks of storage at 4 °C ± 1 °C 4.5 ± 0.05b 3.9 ± 0.10b after 12 weeks of storage 4 °C ± 1 °C 3.4 ± 0.10c 4.3 ± 0.16d
Storage
NaCl + caraway 31 °C
NaCl + onion
18 °C
31 °C
18 °C
31 °C
3.9 ± 0.06a
3.8 ± 0.11a
3.5 ± 0.10a
3.8 ± 0.14a
4.2 ± 0.20a,c
3.4 ± 0.06b
4.1 ± 0.08b
3.8 ± 0.07a
4.7 ± 0.20b
3.4 ± 0.10b
3.7 ± 0.12a
3.7 ± 0.20a
4.3 ± 0.14c
3.4 ± 0.09b
3.5 ± 0.05a
3.3 ± 0.08b
4.0 ± 0.02a
3.2 ± 0.14c
3.2 ± 0.15c
3.1 ± 0.10c
Mean values marked with the same letter in a column do not differ significantly (p ≥ 0.05).
inhibitors. Nevertheless, during sauerkraut production in practice, starter cultures are not employed. Therefore, the use of spices, herbs, or some vegetables that can limit the formation of biogenic amines is fully justified. The results of this study show that the addition of caraway or onion to sauerkraut during fermentation influences the level of biogenic amines. Analysis of sauerkraut fermented at 18 °C or 31 °C in the three groups (control, with caraway, or with onion) indicates that total concentrations of biogenic amines after 14 days of fermentation are lower in the samples fermented at the higher temperature, and in the samples treated with caraway or onion at 18 °C, these additives contribute to a reduction in cadaverine and tyramine contents, and at 31 °C, in tryptamine content. During refrigerated storage at 4 °C ± 1 °C, concentrations of biogenic amines were changing in different ways depending on the temperature of fermentation during preparation of the final product. The consequence of this phenomenon is the variation of pH and acidity among individual stored samples; these parameters affect the activity of enzymes including decarboxylases. After the first 2 weeks, levels of spermidine and spermine decreased significantly, whereas at the end of the storage, the amounts of putrescine, phenethylamine, tryptamine, and tyramine quantified in some samples fermented at 31 °C were higher than those at the beginning. To sum up, this study indicates that addition of caraway or onion inhibits the formation of some biogenic amines in sauerkraut. Moreover, it was confirmed that the derivatisation of amines with benzoyl chloride enables their separation by HPLC on an octadecylsilane column. Sauerkraut with caraway or onion changes the sensory qualities only slightly as compared to the sample without an additive but achieves acceptable ratings during the fermentation process and yields ‘encouraging’ results of preliminary sensory evaluation.
Biogenic amines in seafood: A review. Journal of Food Science and Technology, 53(5), 2210–2218. Cvetković, B. R., Pezo, L. L., Tasić, T., Šarić, L., Kevrešan, Ž., & Mastilović, J. (2015). The optimisation of traditional fermentation process of white cabbage (in relation to biogenic amines and polyamines content and microbiological profile). Food Chemistry, 168, 471–477. Doeun, D., Davaatseren, M., & Chung, M. (2017). Biogenic amines in foods. Food Science and Biotechnology, 26(6), 1463–1474. Dong, H., & Xiao, K. (2017). Modified QuEChERS combined with ultra high performance liquid chromatography tandem mass spectrometry to determine seven biogenic amines in Chinese traditional condiment soy sauce. Food Chemistry, 229, 502–508. EFSA (European Food Safety Authority), EFSA J. 9 (2011) 2393, Available from: http:// www.efsa.europa.eu/de/efsajournal/doc/2393.pdf. Halász, A., Baráth, Á., Simon-Sarkadi, L., & Holzapfel, W. (1994). Biogenic amines and their production by microorganisms in food. Trends in Food Science and Technology, 5(2), 42–49. Halász, A., Baráth, Á., & Holzapfel, W. H. (1999). The influence of starter culture selection on sauerkraut fermentation. European Food Research and Technology, 208(5–6), 434–438. Jairath, G., Singh, P. K., Dabur, R. S., Rani, M., & Chaudhari, M. (2015). Biogenic amines in meat and meat products and its public health significance: A review. Journal of Food Science and Technology, 52(11), 6835–6846. Kalač, P., Špička, J., Křížek, M., & Pelikánová, T. (2000). Changes in biogenic amine concentrations during sauerkraut storage. Food Chemistry, 69(3), 309–314. Kosson, R., & Elkner, K. (2010). Effect of storage period on biogenic amine content in sauerkraut. Vegetable Crops Research Bulletin, 73(1), 151–160. Kuley, E., Durmus, M., Ucar, Y., Riza Kosker, A., Tugçe Aksun Tumerkan, E., Regenstein, J., & Ozogul, F. (2012). Combined effects of plant and cell-free extracts of lactic acid bacteria on biogenic amines and bacterial load of fermented sardine stored at 3 ± 1 °C. Food Bioscience, 24, 127–136. Ma, Y. L., Zhu, D. Y., Thakur, K., Wang, C. H., Wang, H., Ren, Y. F., ... Wei, Z. J. (2018). Antioxidant and antibacterial evaluation of polysaccharides sequentially extracted from onion (Allium cepa L.). International Journal of Biological Macromolecules, 111, 92–101. Mah, J. H., Kim, Y. J., & Hwang, H. J. (2009). Inhibitory effects of garlic and other spices on biogenic amine production in myeolchi-jeot, Korean salted and fermented anchovy product. Food Control, 20(5), 449–454. Martinez-Villaluenga, C., Peñas, E., Frias, J., Ciska, E., Honke, J., Piskula, M. K., & VidalValverde, C. (2009). Influence of fermentation conditions on glucosinolates, ascorbigen, and ascorbic acid content in white cabbage (Brassica oleracea var. capitata cv. Taler) cultivated in different seasons. Journal of Food Science, 74(1), 62–67. Naila, A., Flint, S., Fletcher, G., Bremer, P., & Meerdink, G. (2010). Control of biogenic amines in food – existing and emerging approaches. Journal of Food Science, 75(7), 139–150. Önal, A. (2007). A review: Current analytical methods for the determination of biogenic amines in foods. Food Chemistry, 103(4), 1475–1486. Özogul, F., Taylor, K. D. A., Quantick, P., & Özogul, Y. (2002). Biogenic amines formation in Atlantic herring (Clupea harengus) stored under modified atmosphere packaging using a rapid HPLC method. International Journal of Food Science and Technology, 37(5), 515–522. Park, Y. K., Lee, J. H., & Mah, J. (2019). Occurrence and reduction of biogenic amines in traditional Asian fermented soybean foods: A review. Food Chemistry, 278, 1–9. Peñas, E., Frias, J., Sidro, B., & Vidal-Valverde, C. (2010). Impact of fermentation conditions and refrigerated storage on microbial quality and biogenic amine content of sauerkraut. Food Chemistry, 123(1), 143–151. Polish Standardization Committee. (1990). Fruit and vegetable products – Preparation of samples and testing methods – General principles and range of standard. PN-90/A75101/01.50. Rabie, M. A., Siliha, H., El-Saidy, S., El-Badawy, A. A., & Malcata, F. X. (2011). Reduced biogenic amine contents in sauerkraut via addition of selected lactic acid bacteria. Food Chemistry, 129(4), 1778–1782. Šamec, D., Pavlović, I., & Salopek-Sondi, B. (2017). White cabbage (Brassica oleracea var. capitata f. alba): Botanical, phytochemical and pharmacological overview. Phytochemistry Reviews, 16(1), 117–135.
Declaration of Competing Interest None. Acknowledgements This research was financed by the Ministry of Science and Higher Education of the Republic of Poland. References AOAC (2007). Official method analysis of AOAC International (18th ed.). USA: Maryland. Alvarez, M. A., & Moreno-Arribas, M. V. (2014). The problem of biogenic amines in fermented foods and the use of potential biogenic amine-degrading microorganisms as a solution. Trends in Food Science and Technology, 39(2), 146–155. Beganović, J., Kos, B., Leboš Pavunc, A., Uroić, K., Jokić, M., & Šušković, J. (2014). Traditionally produced sauerkraut as source of autochthonous functional starter cultures. Microbiological Research, 169(7–8), 623–632. Biji, K. B., Ravishankar, C. N., Venkateswarlu, R., Mohan, C. O., & Gopal, T. K. S. (2016).
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J. Majcherczyk and K. Surówka Santas, J., Almajano, M. P., & Carbó, R. (2010). Antimicrobial and antioxidant activity of crude onion (Allium cepa, L.) extracts. International Journal of Food Science and Technology, 45(2), 403–409. Sharma, K., Mahato, N., & Lee, Y. R. (2018). Systematic study on active compounds as antibacterial and antibiofilm agent in aging onions. Journal of Food and Drug Analysis, 26(2), 518–528. Stadnik, J., & Dolatowski, Z. J. (2010). Biogenic amines in meat and fermented meat products. Acta Scientiarum Polonorum, Technologia Alimentaria, 9(3), 251–263.
Tamang, J. P., Shin, D.-H., Jung, S.-J., & Chae, S.-W. (2016). Functional properties of microorganisms in fermented foods. Frontiers in Microbiology, 578, 7–13. Thippeswamy, N. B., Naidu, K. A., & Achur, R. N. (2013). Antioxidant and antibacterial properties of phenolic extract from Carum carvi L. Journal and Pharmacy Research, 7(4), 352–357. Zhou, X., Qiu, M., Zhao, D., Lu, F., & Ding, Y. (2016). Inhibitory effects of spices on biogenic amine accumulation during fish sauce fermentation. J ournal of Food Science, 81(4), M913–M920.
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Effects of onion or caraway on the formation of biogenic amines during sauerkraut fermentation and refrigerated storage
T
Jagoda Majcherczyk , Krzysztof Surówka ⁎
Department of Refrigeration and Food Concentrates, Faculty of Food Technology, University of Agriculture in Krakow, 122 Balicka Street, 30-149 Cracow, Poland
ARTICLE INFO
ABSTRACT
Chemical compounds: Putrescine (PubChem CID1045) Cadaverine (PubChem CID273) Spermidine (PubChem CID1102) Spermine (PubChem CID1103) Histamine (PubChem CID774) Tyramine (PubChem CID560) Phenethylamine (PubChem CID1001) Tryptamine (PubChem CID1150) Serotonin (PubChem CID5202)
The effects of onion or caraway on changes in the content of biogenic amines were examined in sauerkraut during a fermentation process at 18 °C or 31 °C for 14 days and subsequent storage at 4 °C for 12 weeks. The amines were analysed by high-performance liquid chromatography with pre-column benzoylation. Total biogenic-amine concentration at the end of the fermentation was lower at 31 °C than at 18 °C. However, at this lower temperature, the presence of caraway or onion more significantly (than at 31 °C) reduced the total biogenic-amine content as compared to the control sample without an additive. After 12 weeks of refrigerated storage, concentrations of phenethylamine, tryptamine, and tyramine in the sauerkraut fermented with caraway (and concentrations of putrescine and tryptamine in the sauerkraut fermented with onion) at 31 °C increased as compared to the samples on the last day of fermentation, but did not pose a risk for consumer health.
Keywords: Sauerkraut Fermentation Biogenic amine Caraway Onion
1. Introduction Sauerkraut is one of the most traditional fermented products in many European countries, especially popular in the diet of the inhabitants of Central and Eastern regions of this continent. Sauerkraut is prepared by spontaneous lactic acid fermentation of shredded and salted cabbage, but varieties of sauerkraut can be a result of addition of some spices or ingredients (linked to a specific geographic area) during the fermentation. Sauerkraut is a rich source of minerals and vitamins and contains autochthonous lactic acid bacteria, some of which possess probiotic properties. Moreover, during fermentation of white cabbage, some glucosinolates contained in cabbage are transformed into ascorbigen, which has substantial anticarcinogenic activity (Beganović et al., 2014; Martinez-Villaluenga et al., 2009; Šamec, Pavlović, & SalopekSondi, 2017; Tamang, Shin, Jung, & Chae, 2016). The fermentation process can be implemented in two ways. The first type is initiated spontaneously by the natural bacterial population of the raw material, and the second one is conducted with certain selected lactic acid bacteria as inoculants. The use of starter cultures ensures
⁎
control of the fermentation process, whereas during the spontaneous process, there is limited control of the quality and safety of the final product. Moreover, certain additives such as spices can change the conditions of fermentation, thus possibly leading to an increase or decrease in the amounts of some endogenous compounds such as biogenic amines in the final product (Kuley et al., 2012; Zhou, Qiu, Zhao, Lu, & Ding, 2016). Biogenic amines are basic nitrogenous compounds that can be found in a variety of foods, such as meat, fish, cheese, vegetables, wines, and soy sauce (Dong & Xiao, 2017). They can be formed by the enzymes of a raw material or generated by microbial decarboxylation of amino acids (Biji, Ravishankar, Venkateswarlu, Mohan, & Gopal, 2016; Halász, Baráth, Simon-Sarkadi, & Holzapfel, 1994;). Factors that promote microbial activity are substrate and water availability, pH of the environment, salt concentration, and temperature (Jairath, Singh, Dabur, Rani, & Chaudhari, 2015). Several authors have reported the presence of putrescine, cadaverine, spermidine, spermine, histamine, tyramine, phenethylamine, and tryptamine in fermented food products (Alvarez & Moreno-Arribas, 2014; Dong & Xiao, 2017). The initial concentration of
Corresponding author. E-mail addresses: [email protected] (J. Majcherczyk), [email protected] (K. Surówka).
https://doi.org/10.1016/j.foodchem.2019.125083 Received 25 November 2018; Received in revised form 14 June 2019; Accepted 25 June 2019 Available online 26 June 2019 0308-8146/ © 2019 Elsevier Ltd. All rights reserved.
Food Chemistry 298 (2019) 125083
J. Majcherczyk and K. Surówka
biogenic amines in the fresh products is usually low. The formation of these compounds is related to the type of treatment a raw material is subjected to as well as storage conditions and duration. For example, Kosson and Elkner (2010) reported that fresh cabbage contains only putrescine and spermidine at very low levels (under 2 and 10 μg g−1, respectively). During its fermentation, four additional biogenic amines appear, and in most cases, their concentration increases with time. Even though fermented products have many beneficial effects on health, biogenic amines that are present in them can have a toxic effect on the human body. Biotransformation of these compounds is mainly performed by monoamine oxidase and diamine oxidase. People whose mechanism of detoxification is defective and those who take monoamine oxidase- or diamine oxidase-inhibiting drugs are particularly vulnerable to the presence of biogenic amines in food. Excessive intake of these compounds, especially histamine and tyramine, exerts many psychoactive and vasoactive effects (Naila, Flint, Fletcher, Bremer, & Meerdink, 2010; Stadnik & Dolatowski, 2010). Currently, there are no regulatory standards for toxic levels of biogenic amines. Histamine and tyramine are considered the most toxic. Based on the literature, the levels of 25 to 50 mg of histamine and 600 mg of tyramine per meal have no adverse effect on a healthy person (EFSA, 2011). Determination of the exact toxic limits of the rest of the biogenic amines is difficult because the toxic dose is dependent on the detoxifying mechanisms in different individuals (Önal, 2007). It has been found that the use of certain additives in food can inhibit the formation of biogenic amines (Kuley et al., 2012). Mah, Kim, and Hwang (2009) reported that addition of a garlic extract to fermented anchovy decreases levels of these compounds by as much as 18.4% in comparison to a control sample. An excellent review on the occurrence and reduction of biogenic amines in fermented Asian soybean foods was published recently (Park, Lee, & Mah, 2019). Nonetheless, there is no information in the freely available literature about the effects of various ingredients, such as spices, herbs, or other plant products, on biogenicamine formation during sauerkraut production. Conducting a process of sauerkraut fermentation in the presence of onion or caraway gives the final product new original sensory features. The objective of this study was to determine the impact of these additives on the chemical composition of the final products immediately after fermentation and during subsequent refrigerated storage. It was assumed that both additives, in the fermentation process conducted at one of two temperatures (18 °C ± 1 °C or 31 °C ± 1 °C), and during refrigerated storage (4 °C ± 1 °C), can influence the concentrations of the eight most frequently occurring biogenic amines (Doeun, Davaatseren, & Chung, 2017). Chemical compounds belonging to the alkylthiosulphonate class in onion and the terpenoid family in caraway can cause a decrease in the concentration of biogenic amines in the final product by affecting the activity of microorganisms (Ma et al., 2018; Sharma, Mahato, & Lee, 2018; Thippeswamy, Naidu, & Achur, 2013).
NaCl concentration was 2.5%, and the caraway seed and shredded onion supplementation of the selected samples amounted to 10 and 350 g/(kg of sauerkraut), respectively. The closed jars were incubated for fermentation at 18 °C ± 1 °C or 31 °C ± 1 °C via the following scheme: the control group (only 2.5% NaCl), group with caraway (2.5% NaCl + caraway), and the group with onion (2.5% NaCl + onion). Spontaneous fermentation was carried out for 14 days. Then, all jars were placed in a refrigerator at 4 °C ± 1 °C and stored for 12 weeks. pH, total acidity, and biogenic-amine concentrations as well as sensory quality were analysed at the following time points: a fresh sample; after the 3rd, 7th, and 14th day of fermentation; and after the 2nd and 12th week of storage. 2.3. Physicochemical measurements pH of the sauerkraut was measured by directly inserting the combined pH electrode (Elmetron, Poland) into a jar containing the product, whereas total acidity was measured by titration of a product homogenate with 0.1 mol L−1 NaOH according to AOAC procedures (AOAC, 2007) and was expressed in milligrams of lactic acid per 100 g of sauerkraut. 2.4. Determination of biogenic amines Biogenic-amine standards (putrescine dihydrochloride, cadaverine dihydrochloride, spermidine trihydrochloride, spermine tetrahydrochloride, histamine dihydrochloride, tyramine hydrochloride, phenethylamine, tryptamine hydrochloride, and serotonin hydrochloride) and a 99% benzoyl chloride solution were purchased from Sigma-Aldrich (Germany). The purity levels of all the standards were higher than 99%. Stock standard solutions of the amines were prepared by dissolving an accurately weighed amount in 10 mL of high-performance liquid chromatography (HPLC) grade water. All the solvents used were HPLC grade. Concentrations of eight biogenic amines (putrescine, cadaverine, spermidine, spermine, histamine, tyramine, phenethylamine, and tryptamine) in the raw cabbage and sauerkraut samples were measured by trichloroacetic acid (TCA) extraction, derivatisation with benzoyl chloride, and HPLC quantification according to Özogul, Taylor, Quantick, and Özogul (2002) with slight modifications. Each sample (5 g) was homogenised with 20 mL of 6% TCA, then centrifuged at 10000×g for 10 min and passed through filter paper. The collected supernatant was diluted to 50 mL with distilled water. After that, a 2 mL aliquot of a sample was spiked with 1 mg mL−1 serotonin (50 μL) as an internal standard and alkalinised with 1 mL of 1 mol L−1 NaOH. For derivatisation, 20 μL of benzoyl chloride was added, and the reaction mixture was incubated at 24 °C ± 1 °C for 30 min. From the individual amines, corresponding N-benzamides formed as a result of the Schotten–Baumann reaction. The reaction was stopped by adding 2 mL of a saturated sodium chloride solution, and each sample was extracted twice with 2 mL of diethyl ether. Next, combined organic layers were evaporated to dryness in a nitrogen stream. The residue was dissolved in 1 mL of acetonitrile (Merck, Germany), passed through a 0.45 μm syringe filter (Millipore, USA), and 10 μL of the resultant sample was loaded on an HPLC column. Three separate analyses of each sample were carried out. HPLC analysis was performed on a Merck Hitachi LaChrom HPLC System with a diode array detector. Separation of analytes was carried out on an ACE 3C-18 column (150 × 4.6 mm) at 30 °C via gradient elution with acetonitrile and HPLC grade water (Polwater, Poland). The elution started with 40% of acetonitrile and was ramped to 75% (13 min) and then to 100% (3 min) at a flow rate 1 to 1.5 mL min−1 within 16 min. Detection was conducted at 254 nm. Calibration curves for each amine standard were constructed in the range 2–100 µg mL−1. Quantitative analysis of biogenic amines was performed by an external calibration curve method with serotonin as the internal standard (50 µg mL−1). The essential validation parameters of the method for separation and quantification of biogenic amines
2. Materials and methods 2.1. Plant material Heads of white cabbage (Brassica oleracea L. var. capitata L.) were purchased at a local supermarket and stored in wooden containers for less than 2 days at 4 °C in the dark until analysis. Caraway seeds (Carum carvi L.) and onion (Allium cepa L.) were purchased from a retail shop. 2.2. Sauerkraut production From the heads of white cabbage, the outer leaf layer was removed, and the heads were sliced to a thickness of 3–5 mm. The sliced cabbage was evenly mixed with NaCl, then the whole mixture was divided into three parts: caraway seeds were added to the first, shredded onion to the second, and the third one, without additives, was treated as a control. These mixtures were packed tightly into glass jars. The final 2
Food Chemistry 298 (2019) 125083
J. Majcherczyk and K. Surówka
were as follows: linearity of the calibration curves was observed in the range of 2–100 μg mL−1 with a correlation coefficient of greater than 0.995. Limits of detection (LOD) and limits of quantification (LOQ) for all compounds were calculated and turned out to be in the ranges of 0.16–3.02 and 0.53–10.07 μg mL−1, respectively. Total biogenic-amine concentration was calculated as the sum content of the eight assayed amines.
Table 2 Changes in pH and total acidity (mg 100 g−1) of sauerkraut with a different additive after preparation at different temperatures (18 °C ± 1 °C or 31 °C ± 1 °C) during storage at 4 °C ± 1 °C. Composition
Control (NaCl only)
NaCl + caraway
NaCl + onion
Production temperature
18 °C
31 °C
18 °C
31 °C
18 °C
31 °C
3.58b 2425b
4.09a 950c
4.36c 1075d
4.20d 850e
3.78e 1875f
3.73b 2700b
4.42c 1175c
4.46c 1300d
4.46c 1425e
3.98d 2325f
3.06b 2775b
3.92c 1200c
3.74d 1625a
3.63d 1300d
3.34e 2625e
2.5. Sensory analysis pH Total acidity
This analysis of sauerkraut during the fermentation process and refrigerated storage was performed according to the Polish standard (Polish Standardization Committee, 1990) by a panel of six trained people. The panel members were asked about the colour, taste, odour, consistency, and appearance of the juice released. A scale from 1 to 5 was employed for each feature, where 5 was the best and 1 was the worst. For each quality feature, scores given by the six panellists were totalled, and the mean was calculated. The overall sensory quality was obtained as the sum of means of all features multiplied by an individual weighting factor (colour: 0.2, taste: 0.3, odour: 0.3, consistency: 0.1, and the appearance of juice released: 0.1).
pH Total acidity pH Total acidity
immediately after production 4.10a 1250a after 2 weeks of storage 4.15a 1625a after 12 weeks of storage 3.60a 1625a
Mean values marked with the same letter in a row do not differ significantly (p ≥ 0.05).
conditions; however, at the beginning of the process (3rd day), the presence of caraway or onion in the samples fermented at the same temperature generally did not influence the measured parameters, which means that the changes were caused mainly by the temperature. These results are consistent with the findings of Halász, Baráth, and Holzapfel (1999), who reported a greater pH drop at 30 °C than at 11 °C, after 96 h of sauerkraut fermentation. After 7 days of the process, an effect of supplementation with the additives on acidity and pH was observed. Statistically significant differences in pH were noted only at 31 °C, but acidity values were clearly different at both temperatures. At the end of the fermentation, the control sample showed the highest acidity and the lowest pH, suggesting that onion and caraway can (separately) exert inhibitory effects on the fermentation process.
2.6. Statistical methods To obtain the results, the mean ± standard deviation of triplicate determinations were computed. The significance of differences was determined by 2-way analysis of variance (ANOVA) with the least significant difference (LSD) post hoc test and contrast analysis. All statistical data were obtained in the Statistica software, ver. 12 package (StatSoft, Cracow, Poland). A p value less than 0.05 was assumed to indicate a significant difference. 3. Results and discussion 3.1. The influence of fermentation conditions on pH and acidity of sauerkraut
4. The impact of storage duration on the pH and acidity of sauerkraut
Table 1 shows the pH and total acidity values both in the raw cabbage and during the fermentation process at 18 °C or 31 °C in three groups: control (only NaCl) and with an additive (NaCl + caraway or NaCl + onion). Although the 3-day period of fermentation at 18 °C caused some slight increase in pH and a decrease in total acidity as compared to raw cabbage, a significant decrease in pH and an increase in acidity at 31 °C were observed. After 7 or 14 days at both applied fermentation temperatures, there was a further pronounced increase in acidity and a pH drop. This tendency was especially clearly visible in the control group (NaCl only), where at 31 °C, pH decreased by ∼40% and acidity increased more than six-fold on the 14th day of fermentation as compared to the raw cabbage. There were also many significant differences in pH and acidity of sauerkraut produced under various
Changes in the pH and total acidity of sauerkraut, seen under the six conditions (two temperatures and three recipes) mentioned above, after storage at 4 °C ± 1 °C for 2 and 12 weeks, are presented in Table 2. During the first 2 weeks of refrigerated storage, a slight increase in pH was observed, accompanied by an increase in acidity. The greatest growth of this parameter was detected in the sauerkraut with onion fermented at 31 °C; this parameter was 24% greater in relation to the sample immediately after fermentation. During the comparison of samples treated with caraway or onion and samples without either, a clear influence of each additive on pH and acidity after 12 weeks of storage was observed. The two measured parameters – pH and acidity –
Table 1 Changes in pH and total acidity (mg 100 g−1) in sauerkraut during fermentation processes at 18 °C ± 1 °C or 31 °C ± 1 °C. Composition
Raw cabbage
Fermentation temperature
Control (NaCl only)
NaCl + caraway
18 °C
pH Total acidity
5.89a 390a
pH Total acidity
5.89a 390a
pH Total acidity
5.89a 390a
after 3rd day of fermentation 6.32b 375a after 7th day of fermentation 4.25b 1175b after 14th day of fermentation 4.10b 1250b
Mean values marked with the same letter in a row do not differ significantly (p 0.05). 3
NaCl + onion
31 °C
18 °C
31 °C
18 °C
31 °C
4.48c 825b
6.25b 375a
4.45c 825b
6.17b 375a
4.71d 800b
4.39c 950c
4.33b,c 800d
4.23b 1075e
4.30b 1075e
3.69d 1975f
3.58c 2425c
4.09b 950d
4.36d 1075e
4.20e 850f
3.78f 1875g
Food Chemistry 298 (2019) 125083
J. Majcherczyk and K. Surówka
Fig. 1. Separation of biogenic amines extracted from sauerkraut fermented with caraway at 31 °C and stored for 12 weeks at 4 °C. ID numbers of amines: 1, putrescine; 2, cadaverine; 3, spermidine; 4, tyramine; 5, phenethylamine; 6, spermine; 7, histamine; 8, internal standard (serotonin); and 9, tryptamine.
were the lowest and highest, respectively, for the sauerkraut treated only with NaCl. This finding may indicate that the inhibitory effect of caraway and onion seen during fermentation also occurs during refrigerated storage of the products. The pH value obtained after 12 weeks of storage for control samples fermented at 18 °C was congruent with the results obtained by Kalač, Špička, Křížek, and Pelikánová (2000) and Rabie, Siliha, El-Saidy, El-Badawy, and Malcata (2011) during sauerkraut storage under similar fermentation conditions.
process regardless of temperature. Similarly, an inhibitory effect of green onion on tyramine production in fermented anchovy was reported by Mah et al. (2009). Moreover, it was noted here that the concentrations of cadaverine and tyramine generally were lower at a higher temperature of fermentation. The lower cadaverine concentration obtained at the higher temperature is in agreement with the results of Cvetković et al. (2015). There, this tendency was independent of the varieties of cabbage, salt concentration, and duration of fermentation. During fermentation, a decreasing tendency of spermine content in the samples fermented at 18 °C and a slight increase at 31 °C were observed. Spermidine levels decreased at both fermentation temperatures. There were no significant differences between samples with and without an additive. The content of histamine in sauerkraut was generally at a similar level with the exception where caraway was added and fermentation was conducted at 18 °C. The determined amount of histamine was higher than that reported by other authors (Peñas et al., 2010; Cvetković et al., 2015), but the concentration of this amine was still lower than the maximal level (100 mg kg−1) allowed in foods (Halász et al., 1999). Onion manifested the greatest inhibitory effect on the accumulation of four (cadaverine, spermine, phenethylamine, and tyramine) out of the eight biogenic amines in the sauerkraut fermentation process, especially at 18 °C. This impact may be related to the antimicrobial activity of onion because biogenic amines are formed by microbial enzymatic activity (Santas, Almajano, & Carbó, 2010; Sharma et al., 2018). Even though the compounds present in caraway also possess antimicrobial activities (Thippeswamy et al., 2013), an inhibitory effect on biogenic-amine levels was observed only for cadaverine and tyramine after 7 days of fermentation. Total biogenic-amine concentrations in control samples after 14 days of the process at 18 °C or 31 °C were 102.65 and 82.49 mg kg−1, respectively. The effect of caraway and onion at the lower temperature was a decrease in this index by 13.3% and 18.8%, respectively. Significantly smaller changes (by 3.8% and 3.9%) were recorded in the fermented products with each of these additives at 31 °C.
4.1. The influence of fermentation conditions on the formation of biogenic amines Fig. 1 depicts a typical chromatogram of separation of biogenic amines extracted from sauerkraut in the form of their benzoyl derivatives. Changes in the formation of these compounds during preparation of sauerkraut are given in Table 3 for fermentation at 18 °C or 31 °C, in the presence of caraway or onion as an additive to cabbage with NaCl. According to the experimental results, fresh cabbage contained all the analysed amines in the range from 2.52 mg kg−1 (tryptamine) to 16.39 mg kg−1 (spermine), and the total content of biogenic amines was ∼76 mg kg−1, which is similar to the data obtained by other authors (Peñas, Frias, Sidro, & Vidal-Valverde, 2010; Rabie et al., 2011). On the other hand, Kosson and Elkner (2010), who applied the same derivatisation technique as the one used here, detected only putrescine and spermidine in cabbage. Fermentation for 14 days at 18 °C with or without caraway or onion caused no significant changes in the putrescine level, but at 31 °C, an increase was observed. At 18 °C, cadaverine, tryptamine, and tyramine showed a slow but significant rise of concentrations with fermentation time, and these concentrations were two- or threefold higher than those registered in the raw cabbage. In some cases, a similar tendency was observed in the sauerkraut prepared at 31 °C. The inhibitory effect of the addition of caraway or onion on the formation of cadaverine and tyramine, especially at the lower temperature, can also be seen. The sauerkraut that was produced without any additives contained significantly higher concentrations of the discussed amines than did the sauerkraut with one of the additives. Besides, the level of cadaverine determined in samples fermented with onion did not change during the 4
Food Chemistry 298 (2019) 125083
J. Majcherczyk and K. Surówka
Table 3 Changes in biogenic-amine concentrations (mg kg−1) in sauerkraut during fermentation processes at 18 °C ± 1 °C or 31 °C ± 1 °C with a different additive. Composition
Control (NaCl only)
Duration of fermentation (days)
18 °C
Putrescine 0 3 7 14 Cadaverine 0 3 7 14 Spermidine 0 3 7 14 Histamine 0 3 7 14 Phenethylamine 0 3 7 14 Tryptamine 0 3 7 14 Spermine 0 3 7 14 Tyramine 0 3 7 14
6.72 7.16 7.03 6.79
± ± ± ±
0.40 0.13A 0.23A 0.16A,C
6.83 ± 0.57a 7.12 ± 0.40a 14.39 ± 0.51b,A 15.34 ± 0.44b,A 14.51 13.67 12.64 11.92
± ± ± ±
0.47a 0.19a,c,A 0.54b,c,A 0.28b,A
NaCl + caraway 31 °C
18 °C
6.72 ± 0.40a 9.74 ± 1.76b,B 10.79 ± 2.20b,B 9.98 ± 0.48b,B
6.72 7.26 6.33 7.62
6.83 6.87 8.70 7.11
± ± ± ±
14.51 13.10 12.47 12.22
0.57a 0.75a 1.53b,B 0.40a,B
± ± ± ±
0.47a 1.86a,b,A 1.48b,A 0.63b,A
± ± ± ±
0.40 0.18A 0.33A 0.43A
6.83 ± 0.57a 7.48 ± 0.46a,b 8.49 ± 1.57b,B,C 12.00 ± 1.25d,C 14.51 14.06 10.15 11.90
± ± ± ±
0.47a 2.10a,A 0.82b,B 0.40c,A
NaCl + onion 31 °C
18 °C
6.72 ± 0.40a 7.31 ± 0.83a,A 7.26 ± 0.42a,A 10.13 ± 0.94b,B
6.72 6.73 6.73 6.39
± ± ± ±
0.40 0.25A 0.10A 0.07C
6.72 ± 0.40a 7.44 ± 0.15a,A 10.04 ± 0.57b,B 8.37 ± 0.21b,D
0.57a 0.41a,b 0.70b,B,C 0.27a,b,B
6.83 6.61 6.94 6.99
± ± ± ±
0.57 0.11 0.28C 0.12B
6.83 7.00 6.83 7.20
6.83 6.95 7.89 7.23
± ± ± ±
14.51 10.91 11.10 14.45
± ± ± ±
0.47a 1.00b,B 0.19b,A,B 0.49a,B
31 °C
14.51 14.93 12.06 13.07
± ± ± ±
0.47a,c 0.18a,A 0.12b,c,A 0.49c,C
9.07 8.71 9.13 8.23
± ± ± ±
0.54 0.13A 0.52A 0.07A
9.07 8.36 8.87 9.36
± ± ± ±
0.54 0.11A 0.64A,B 0.19B
9.07 ± 0.54a 9.61 ± 1.01a,B 12.50 ± 0.4b,C 10.28 ± 0.97a,B
9.07 8.20 8.61 9.90
± ± ± ±
0.54 0.20A 0.32B 0.77B
9.07 ± 0.54 8.85 ± 0.39A,B 10.78 ± 0.76A 8.74 ± 0.28A
7.41 5.70 8.07 8.37
± ± ± ±
0.21a 0.10b,A 0.78a,A,B 0.43a,A
7.41 6.74 7.13 6.23
± ± ± ±
0.21 0.29B 0.91A 0.24B
7.41 5.75 7.09 8.70
± ± ± ±
0.21a,b,c 1.54a,A 0.03b,A 1.40c,A
7.41 5.56 7.63 6.33
± ± ± ±
0.21a,c 0.43b,A 0.92c,A 038a,b,B
7.41 5.50 9.29 6.47
± ± ± ±
2.52 2.52 2.75 6.50
± ± ± ±
0.39a 0.55a,A 0.46a,A 0.94b,A
2.52 1.11 3.67 9.16
± ± ± ±
0.39a,c 0.63a,A 1.65c,A,B 0.40b,B
2.52 1.54 2.23 6.73
± ± ± ±
0.39a 0.49a,A 1.37a,A 1.95b,A
2.52 4.33 4.09 3.70
± ± ± ±
0.39a 1.61b,B 1.42a,b,B 0.25a,b,C
2.52 2.26 2.65 8.62
± ± ± ±
± ± ± ±
14.51 12.81 11.49 13.11
0.57 0.16 0.20C 0.17B
± ± ± ±
0.47a 0.22b,A,B 0.52b,A 0.47a,b,C
9.07 8.59 9.29 9.01
± ± ± ±
0.54 0.26A 0.32A,B 0.59A,B
0.21a 0.35b,A 0.46c,B 0.88a,b,B
7.41 7.89 7.20 5.98
± ± ± ±
0.21a,b 0.26a,C 0.42a,A 0.14b,B
0.39a 0.58a,A 0.35a,A 0.38b,A
2.52 ± 0.39a 8.61 ± 1.74b,C 10.38 ± 0.53c,C 4.35 ± 0.77d,C
16.39 14.67 15.39 15.67
± ± ± ±
1.46a 0.19b,A 0.52a,b,A 0.44a,b,A
16.39 15.62 15.01 16.78
± ± ± ±
1.46a,b 0.09a,b,B 0.54a,A 0.65b,A
16.39 14.68 15.05 15.51
± ± ± ±
1.46a 0.04b,A 0.97a,b,A 0.92a,b,A
16.39 15.83 15.62 17.66
1.46a,b 0.43a,B 0.13a,A 2.32b,B
16.39 15.31 14.91 14.85
± ± ± ±
1.46a 1.12a,b,A,B 0.07b,A 0.32a,b,A
16.39 15.74 18.23 16.78
± ± ± ±
1.46a 0.16a,B 0.65b,B 0.82a,A,B
12.72 14.34 21.49 29.83
± ± ± ±
0.41a 0.30a,A 4.23b,A 0.57c,A
12.72 13.87 14.63 11.65
± ± ± ±
0.41a 1.52a,c,A 1.12b,c,B 0.86a,B
12.72 17.22 17.39 16.28
± ± ± ±
0.41a,b 1.67b,c,B 1.90b,B 1.60b,C
12.72 ± 0.41a 9.04 ± 0.02b,C 12.82 ± 0.40a,B 16.23 ± 3.96c,C
12.72 14.44 13.68 18.26
± ± ± ±
0.41a 2.69a,A 1.33a,A,B 0.88b,C
12.72 12.50 10.88 13.78
± ± ± ±
0.41 0.55A 1.24B 0.68B
± ± ± ±
Mean values for an amine marked with the same superscript or not marked at all in the column do not differ significantly (p ≥ 0.05). Mean values marked with the same capital letter or not marked at all in the row do not differ significantly (p ≥ 0.05).
4.2. The impact of storage duration on the biogenic amines in the sauerkraut
caraway or onion, levels of the amines (phenethylamine, tryptamine, and tyramine for caraway, and putrescine and tryptamine for onion) were significantly higher than those in the control. These results are consistent with the data of Kalač et al. (2000), who reported that during 4 months of sauerkraut storage, the change in tyramine concentration increased more than 3-fold. Nonetheless, our study revealed a similar tendency, but the change in the amount of the above-mentioned amine was much smaller in the samples with an additive. These data may mean that the inhibitory effect persisted even a few weeks after the fermentation. At the end of the storage (after 12 weeks), concentrations of putrescine, cadaverine, phenethylamine, and spermidine significantly increased in the samples fermented with caraway at 18 °C; however, they did not exceed the values of the control. During the storage, histamine was detected in every sample of sauerkraut. However, after 2 weeks, the concentration of this amine obtained at 31 °C in the samples without an additive was significantly lower as compared with the beginning of the storage. This tendency for the samples fermented at the higher temperature with caraway was observed after 12 weeks too. No significant differences (p greater than 0.05) in the amount of cadaverine from samples fermented at 31 °C were detected between sauerkraut with or without an additive and the control samples.
Changes of biogenic amines in sauerkraut fermented under different conditions (temperatures and additives) and stored at 4 °C for 12 weeks are given in Fig. 2. Samples of sauerkraut on the last day of fermentation were regarded as the control (storage time = 0 weeks). Even though all the samples were stored at the same temperature, different tendencies of changing levels of biogenic amines quantified in sauerkraut fermented at 18 °C and 31 °C were observed. This finding is probably due to the differences in acidity and pH among individual products, as a result of bacterial growth, and consequently affects the activity of decarboxylases. After the first 2 weeks of refrigerated storage, the sauerkraut obtained at lower temperature contained lower amounts of five compounds (cadaverine, spermidine, phenethylamine, spermine, and tyramine) as compared to the control. These reductions were approximately two- or three-fold for spermidine and spermine contents, detected in sauerkraut fermented with or without an additive, respectively. The rest of the mentioned amines showed a similar decreasing tendency, whereas for tyramine, this tendency was observed only in the sample without an additive. During the storage (4 °C ± 1 °C), a tendency for increasing amounts of putrescine, tryptamine, phenethylamine, and tyramine was observed in the sauerkraut obtained at 31 °C. Especially for the samples with 5
Food Chemistry 298 (2019) 125083
J. Majcherczyk and K. Surówka
Cadaverine
Putrescine 14
b
12
a
8
a
a
a,b
a,b b
b
a
10
18 16
a a
14
b b
12
b
10
a
8
6
6
4
4
2
2 0
0
2
0
2
01
12
Spermidine 16 14 12
a
b
b
Phenethylamine
a
12
a
a
a a
a
a
10
b
10
b b b
8
b
b
12
b
a
a a
b
8
b b b
b
b
a
Fig. 2. Effects of duration of storage (at 4 °C ± 1 °C) of the sauerkraut obtained with different additives at 18 °C ± 1 °C or 31 °C ± 1 °C on concentrations of eight biogenic amines. Production temperature and the additives were as follows: 18 °C; 2.5% NaCl 18 °C; 2.5% NaCl; caraway 18 °C; 2.5% NaCl; onion 31 °C; 2.5% NaCl 31 °C; 2.5% NaCl; caraway 31 °C; 2.5% NaCl; onion. Mean values for an amine marked with the same letter in a graph or not marked at all for the product obtained at the same temperature and additive do not differ significantly (p ≥ 0.05).
a
a
b b
a a
6
6
4
4 2
2 0
0 1
0
12
2
Histamine
Tryptamine
Concentration (mg kg-1)
12
2
01
10
14
b
b b
b
8
12
a
10 6
a
8
a a
4
a
b b
b
6 4
2
2
0
18 16
a a
a
a
14 12
c
10
b b b b b b
b
c b b
6 4 2 0
0 1
2
12
2
Tyramine
a
8
01
Spermine
a
20
0
12
2
0 1
12
b
32 30 28 26 24 22 20 18 16 14 12 10 8 6 4 2 0
a
a
01
a,b
b
2
b
b
12
Storage time (weeks) 18°C; 2.5% NaCl 31°C; 2.5% NaCl
18°C; 2.5% NaCl; caraway 31°C; 2.5% NaCl; caraway
18°C; 2.5% NaCl; onion 31°C; 2.5% NaCl; onion
4.3. Sensory quality
changed the least. This trend also persisted throughout the 12-week storage period at 4 °C. The overall sensory quality of the samples obtained at 18 °C with caraway was higher than that with onion and lower than that in the control. The results indicated that the addition of caraway affected the sensory features of sauerkraut to a lesser extent than onion did.
This quality of sauerkraut is usually determined during the fermentation process, and after its completion, the product should retain good features during refrigerated storage. In Table 4, overall sensory quality scores are presented for the products with NaCl only or with caraway or onion. According to the members of the evaluation panel, starting from the 7th day, the quality of sauerkraut fermented at 31 °C was generally worse than that of the respective products at 18 °C. Sauerkraut obtained at 31 °C with caraway or onion was characterised by a too intense odour and taste; this result was the main reason for the lower ratings, while the colour and appearance of the juice released
5. Conclusion To prevent or reduce formation and accumulation of biogenic amines in food, the decarboxylase activity should be limited by means of a microbial starter preventing their production or via application of 6
Food Chemistry 298 (2019) 125083
J. Majcherczyk and K. Surówka
Table 4 Overall sensory quality of the sauerkraut during preparation and refrigerated storage. Variant
Control (NaCl only)
Fermentation temperature
18 °C
Fermentation
after 3rd day of fermentation 4.1 ± 0.08a 4.4 ± 0.21a after 7th day of fermentation 4.4 ± 0.11b,d 3.7 ± 0.14b after 14th day of fermentation 4.8 ± 0.12c 4.4 ± 0.14a after 2 weeks of storage at 4 °C ± 1 °C 4.5 ± 0.05b 3.9 ± 0.10b after 12 weeks of storage 4 °C ± 1 °C 3.4 ± 0.10c 4.3 ± 0.16d
Storage
NaCl + caraway 31 °C
NaCl + onion
18 °C
31 °C
18 °C
31 °C
3.9 ± 0.06a
3.8 ± 0.11a
3.5 ± 0.10a
3.8 ± 0.14a
4.2 ± 0.20a,c
3.4 ± 0.06b
4.1 ± 0.08b
3.8 ± 0.07a
4.7 ± 0.20b
3.4 ± 0.10b
3.7 ± 0.12a
3.7 ± 0.20a
4.3 ± 0.14c
3.4 ± 0.09b
3.5 ± 0.05a
3.3 ± 0.08b
4.0 ± 0.02a
3.2 ± 0.14c
3.2 ± 0.15c
3.1 ± 0.10c
Mean values marked with the same letter in a column do not differ significantly (p ≥ 0.05).
inhibitors. Nevertheless, during sauerkraut production in practice, starter cultures are not employed. Therefore, the use of spices, herbs, or some vegetables that can limit the formation of biogenic amines is fully justified. The results of this study show that the addition of caraway or onion to sauerkraut during fermentation influences the level of biogenic amines. Analysis of sauerkraut fermented at 18 °C or 31 °C in the three groups (control, with caraway, or with onion) indicates that total concentrations of biogenic amines after 14 days of fermentation are lower in the samples fermented at the higher temperature, and in the samples treated with caraway or onion at 18 °C, these additives contribute to a reduction in cadaverine and tyramine contents, and at 31 °C, in tryptamine content. During refrigerated storage at 4 °C ± 1 °C, concentrations of biogenic amines were changing in different ways depending on the temperature of fermentation during preparation of the final product. The consequence of this phenomenon is the variation of pH and acidity among individual stored samples; these parameters affect the activity of enzymes including decarboxylases. After the first 2 weeks, levels of spermidine and spermine decreased significantly, whereas at the end of the storage, the amounts of putrescine, phenethylamine, tryptamine, and tyramine quantified in some samples fermented at 31 °C were higher than those at the beginning. To sum up, this study indicates that addition of caraway or onion inhibits the formation of some biogenic amines in sauerkraut. Moreover, it was confirmed that the derivatisation of amines with benzoyl chloride enables their separation by HPLC on an octadecylsilane column. Sauerkraut with caraway or onion changes the sensory qualities only slightly as compared to the sample without an additive but achieves acceptable ratings during the fermentation process and yields ‘encouraging’ results of preliminary sensory evaluation.
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