Effect of ultrasound, heating and enzymatic pre-treatment on bioactive compounds in juice from Berberis amurensis Rupr.

Ultrasonics - Sonochemistry 63 (2020) 104971

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Effect of ultrasound, heating and enzymatic pre-treatment on bioactive compounds in juice from Berberis amurensis Rupr.

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Elżbieta Radziejewska-Kubzdelaa, , Artur Szwengiela, Henryk Ratajkiewiczb, Kinga Nowakc a

Institute of Technology of Food of Plant Origin, Poznań University of Life Sciences, Wojska Polskiego 31, 60-624 Poznań, Poland Department of Entomology and Environmental Protection, Poznan University of Life Sciences, Dąbrowskiego 159, 60-594 Poznan, Poland c Institute of Dendrology, Polish Academy of Sciences, ul. Parkowa 5, 62-035, Kórnik, Poland b

A R T I C LE I N FO

A B S T R A C T

Keywords: Barberry Juice Sonication Heating Enzymatic pre-treatment

The aim of the study was to assess the influence of ultrasound (frequency 20 kHz, amplitude 70%, power 140 W for 10 min), heating (80 °C, 5 min) and enzymatic pre-treatment of mash (50 °C, Rohapect 10L at a dose of 0.23 g/1000 g, maceration time 60 min) on the yield, the content of phenolic compounds (including anthocyanins), ascorbic acid, and the antioxidative capacity of Berberis amurensis juice. Additionally, the polyphenols profile of this raw material and juices was identified. 25 phenolic compounds were identified in the fruit and 24 in juices. The content of phenolics in the fruit was 636 mg/100 g. Chlorogenic acid, 4-hydroxybenzoate and quercetin-3-O-glicoside were predominant. The content of anthocyanins in the fruit was 217 mg/100 g f.w., where peonidin-3-O-glucoside (98%) was predominant. The content of ascorbic acid amounted to 16.60 mg/ 100 g. The yield of the barberry juice pressing process ranged from 56% to 60% – there were no differences between the mash treatment methods. The enzymatic and thermal treatment of the mash resulted in the highest content of phenolic compounds in the juice. The sonication resulted in the highest content of anthocyanins, including peonidin-3-O-glucoside, as the main anthocyanin. The thermal treatment of the mash resulted in a lower loss of ascorbic acid than the other methods. The juice from the mash subjected to pectinolysis or heat treatment exhibited the highest antioxidative capacity.

1. Introduction Berberis amurensis Rupr. belongs to the Berberidaceae family. Plants from this family grow mainly in China, the central and northern part of the Korean Peninsula, the far east of Russia, in Europe and South America. Fruits, leaves, bark and stems are used in folk medicine to treat disorders such as enteritis and diarrhoea [1] and as a haemostatic [2,3] and antihypertensive [4,5]. Berberis is very rich in bioactive compounds, including anthocyanins. Their content is often higher than in other widely consumed berries. For instance, Berberis microphylla contains 18 anthocyanins, whose concentration ranges from 14.2 to 26.1 µmol/g of fresh weight [6]. Some species are also good sources of hydroxycinnamic acids, quercetin derivatives, and epicatechin [6–8]. The total content of phenolics may range from 261 to 1074 mg/100 g [7,9,10]. The content of vitamin C in barberry ranges from 11.5 to 198 mg/100 g f.w. [7,9,11]. Barberry also exhibits high antioxidative and free radical scavenging activity [12]. So far the profile of phenolic compounds in B. amurensis has not been described in publications. Many studies on

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plants of the Berberidaceae family usually analyse isoquinoline alkaloids such as berbamine and palmatine. They have various biological effects, e.g. antidiabetic [13], hypotensive [4] and neuroprotective [14]. The highest concentration of berberine was found in the bark and roots, whereas the lowest was in the leaves and fruits [15]. B. amurensis produces small red berries with sour taste. In some countries fruits of the Berberis species are consumed fresh, dried, as jellies, wines, juices, concentrates, and carbonated beverages. Barberry anthocyanins are also considered a natural colouring agent [11,16]. One of the most commonly consumed products is juice. In juice technology, the pre-treatment of mash often causes an increase in the content of bioactive compounds. For instance, enzymatic maceration degrades the cell wall matrix, thus enhancing the juice yield and increasing the extractability of phenolic compounds, including anthocyanins [17–19]. An increase in the content of phenolic compounds may also result from the heat treatment of mash. The denaturation of cell membrane proteins facilitates the release of phenolic compounds from the skin into the juice [20]. Ultrasonication has also been increasingly often taken into consideration as a pre-treatment method in

Corresponding author. E-mail address: [email protected] (E. Radziejewska-Kubzdela).

https://doi.org/10.1016/j.ultsonch.2020.104971 Received 6 October 2019; Received in revised form 8 January 2020; Accepted 10 January 2020 Available online 13 January 2020 1350-4177/ © 2020 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/BY/4.0/).

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were the accordance with the manufacturer's recommendation. The fourth variant was not pre-treated. After the pre-treatment the mashes were pressed in a Para-press laboratory press (Arauner Kitzingen, Kitzingein, Germany) at 0.28 MPa for 10 min. The juices were stored at −50 °C for further analysis.

juice production. Ultrasounds propagate in liquids and cause cavitation. Cavitation bubbles collapse as the pressure and temperature rise locally. Ultrasonication can disrupt cell membranes and walls and thus contribute to the extraction intracellular compounds [21]. The aim of the study was to determine the effect of ultrasound, heating and enzymatic pre-treatment of mash on the yield, the content of bioactive compounds, and the antioxidative capacity of B. amurensis juice. Additionally, the polyphenols profile of B. amurensis fruits and juices was identified.

2.4. Ascorbic acid determination 10 g of the raw material or juice was weighed and homogenised with 25 mL of 10 g/L metaphosphoric acid. Then, the samples were shaken for 15 min and centrifuged at 3800×g for 15 min at 4 °C. The extraction procedure was repeated twice. The supernatants were combined and 10 g/L of meta-phosphoric acid was added to a volume of 50 mL. 1 mL of 50 g/L dithiothreitol and 10 mL of the sample were mixed. The volume of the samples was made up to 25 mL by metaphosphoric acid. The samples were analysed with the LC Agilent Technologies 1200 Rapid Resolution system (Waldbronn, Germany), using a Poroshell 120, SB-C18 column (4.6 × 150 mm, 2.7 µm) (Agilent Technologies, Wilmington, USA) and a UV–Vis detector (DAD 1260, Waldbronn, Germany). Methanol (phase A) and 0.005 mol/L KH2PO4 solution (pH 2.6, phase B) were used as mobile phases. The gradient was used as follows: 5% to 22% phase A for 6 min and then return to the initial conditions within 9 min. The flow rate was 0.7 mL/min, detection at 245 nm. The results were expressed as mg ascorbic acid/ 100 g fresh weight (f.w.) [26].

2. Material and methods 2.1. Chemicals Meta-phosphoric acid (HPO3), HPLC grade acetonitrile (CH3CN) and methanol (MeOH) were purchased from Sigma Aldrich Chemie GmbH (Steinheim, Germany). L-ascorbic acid (C6H8O6), 2,2-azinobis(3-ethylbenzothiazoline-6-sulphonic acid) (ABTS), 6-hydroxy-2,5,7,8tetramethylchroman-2-carboxylic acid (Trolox), formic acid (CH2O2), catechin and gallic acid were supplied by Sigma Aldrich Chemie Co. (St. Louis, USA). L-dithiothreitol, potassium persulphate (K2O8S2) and chlorogenic acid were purchased from Sigma Aldrich Chemie Co. (Buchs, Switzerland). Monobasic potassium phosphate (KH2PO4) was provided by Sigma Aldrich Chemie Co. (Tokyo, Japan). Sodium acetate (C2H3NaO2) was purchased from Chempur (Piekary Śląskie, Poland). Cyanidin-3-O-glucoside chloride was purchased from ChromaDex (Boulder, USA). Ultrapure water was produced in a laboratory, using a Direct-Q UV3 Water Purification System (Millipore, Billerica, USA).

2.5. Anthocyanins analysis Barberries or barberry juices (10 g) were homogenised with an IKA T-25 homogeniser (Staufen, Germany) and extracted with a solvent mixture of methanol, water, and acetic acid (50:48:2 V/V/V). Next, the extracts were shaken in a Water Bath Shaker type 357 (Elpin, Lubawa, Poland) for 15 min and then centrifuged at 3000×g for 20 min in an MPW-351R centrifuge (Warsaw, Poland). Anthocyanins were extracted twice. The supernatants were combined and concentrated in vacuum (Büchi R-205 evaporator, Flawil, Switzerland) at 35 °C. The anthocyanins were diluted with distilled water and separated by means of the LC Agilent Technologies 1200 Rapid Resolution system (Waldbronn, Germany) with a UV–Vis detector (DAD 1260, Waldbronn, Germany). The pigments were separated with the Poroshell 120, SBC18 column (4.6 × 150 mm, 2.7 µm) (Agilent Technologies, Wilmington, USA). Solvent A with formic acid (10%), and solvent B consisting of formic acid (10%), acetonitrile (30%) and water (60%) were used for elution. The gradient increased as follows: 0–8 min, 20% B; 8–15 min, 40% B in A; 15–16 min, 50% B; 16–20 min 100% B. The flow rate was 1 mL/min. The absorbance was monitored at 520 nm and scanned from λ 250 to 600 nm. Anthocyanins were quantified as mg cyanidin-3-Oglucoside equivalent/100 g f.w. [27].

2.2. Raw material Barberries (Berberis amurensis Rupr.) came from the Polish Academy of Sciences, Institute of Dendrology, Polish Academy of Sciences, in Kórnik (Poland) (52°14′41.5″N 17°05′56.5″E). The fruits (13 kg) were collected as fully mature, damaged or overripe fruits were discarded. The fruits were harvested in early November and frozen at −50 °C to protect against quality changes from harvest to use. 2.3. Technological process The fruits were thawed. Next, they were comminuted in a Thermomix laboratory mill (Wuppertal, Vorwerk, Germany). The resulting mash was pre-treated in four variants. Each batch contained 1000 g of the fruit mash. The first variant was subjected to ultrasonication with a Sonopuls HD 3200 ultrasonic homogeniser (Bandelin, Berlin, Germany) consisting of a GM 3200 ultrasonic generator and UW 3200 ultrasonic converter with a standard SH 213G horn and a TT13 titanium flat tip. Effective ultrasonic extraction of various compounds from plant material has been reported mainly for 20–100 kHz, time 10–60 min and power 100–650 W [22,23]. In our study, ultrasonication was conducted at a constant frequency of 20 kHz, amplitude of 70% and power of 140 W for 10 min. The mash was placed in a glass beaker and an ultrasonic probe was submerged in the mash to a depth of 2 cm above the bottom of the beaker. The second variant was heated. Zadernowski and Oszmiański [24] show that heat treatment of the mash at a temperature of 80 °C–90 °C facilitates extraction of pigments from the skin during pressing. Borowska et al. [25] used mash treatment at 85 °C for 5 min, they obtained a significant increase of the anthocyanins content in the chokeberry juice compared to the sample obtained from the mash without treatment. In our study, we used the mash heating during 16 min to 80 °C and then was kept at 80 °C for 5 min. The resulted mash was hot-pressed. The third was subjected to enzymatic maceration. 1000 g of the fruit mash was weighed and heated up to 50 °C for 8 min. Then Rohapect 10L enzyme (pectinase) (AB Enzymes, Darmstadt, Germany) was added at a dose of 0.23 g/1000 g mash. The maceration time was 60 min. Parameters of the enzymatic maceration

2.6. Polyphenols determination 10 g of the barberry fruits and juices was weighed and homogenised with 50 mL of 700 g/L methanol, using an IKA T-25 homogeniser (Staufen, Germany). Then, the homogenates were shaken in a Water Bath Shaker type 357 (Elpin, Lubawa, Poland) for 15 min and centrifuged in an MPW-351R centrifuge (Warsaw, Poland) at 3000×g for 20 min. The extraction was conducted twice. The phenolic extracts were combined and then evaporated in a vacuum Büchi R-205 evaporator (Flawil, Switzerland) at 40 °C. The condensed extracts were made up to 25 mL with ultrapure water [28]. Phenolic compounds were analysed by means of the LC Agilent Technologies 1200 Rapid Resolution system equipped with a Poroshell 120, SB-C18 column (4.6 × 150 mm, 2.7 μm). 60 g/L acetic acid in 0.002 mol/L sodium acetate (solvent A) and acetonitrile (solvent B) were used as a mobile phase [29]. The run time was 35 min and the flow rate was 1 mL/min. The separation was conducted with the 2

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following gradient programme: 0–15% B for 15 min, 1530% B for 25 min, 30–50% B for 5 min and 50–100% B for 5 min. The phenolics were quantified at 280 nm, 320 nm and 360 nm, using the external standard method. Gallic acid, chlorogenic acid, catechin, and quercetin were used as a standard. High-performance liquid chromatography – electrospray ionisation mass spectrometry coupled to a Bruker maXis impact ultrahigh resolution orthogonal quadrupole-time-of-flight accelerator (qTOF) equipped with an ESI source and operated in the positive-ion mode (Bruker Daltonik, Bremen, Germany) were used for the identification of polyphenols in barberry fruits and juice extracts. The ESI-MS settings were previously described by Mildner-Szkudlarz et al. [30]. The unretained sugars (0–3.5 min) were directed to the waste to protect the ion source capillary. Molecular ions: [M]+ and [M+H]+ were extracted from full scan chromatograms and peak areas were integrated with the Find Molecular Features (FMF) algorithm, which finally defines compounds, called a bucket (Bruker Daltonik, Bremen, Germany). The compounds in each sample were identified on the basis of their molecular mass and structural information from the MS detector during MS/MS experiments. The tandem mass spectrometric data were used to search the molecular structure with two computational methods. We used CSI:FingerID, which combines fragmentation tree computation and machine learning [31,32] and the in silico fragmenter MetFrag [33].

Table 1 Ascorbic acid content in barberry fruits (Berberis amurensis) and juices from mash after different pre-treatment. Sample raw material juice from mash juice from mash juice from mash juice from mash

without pre-treatment after enzymatic treatment after thermal processing after ultrasound treatment

16.60 ± 2.48d 8.50 ± 0.00b 5.27 ± 0.12a 12.03 ± 0.26c 7.47 ± 0.25ab

Means within columns marked by the same letter do not differ significantly.

mean values of multiple groups. Correlations were analysed with Pearson’s test. Statistical significance was set at P < 0.05. The STATISTICA version 13.1 software (Statsoft, Inc., Tulsa, OK, USA) was used for the analyses. 3. Results and discussion 3.1. Ascorbic acid content The content of ascorbic acid in the barberry fruits (B. amurensis) was 16.60 mg/100 g of f.w. According to references, the content of this acid in Berberis vulgaris fruit was similar – it ranged from 11.5 to 25.6 mg/ 100 g f.w. [7,8]. Some species have higher content of ascorbic acid. For example, it ranged from 97 to 198 mg/100 g f.w. in B. microphylla [11]. As far as juices are concerned, the highest content of ascorbic acid was found in samples obtained from the mash subjected to the heat treatment (72% content in fruit). The content was significantly lower in the juices made from the untreated mash, and from the mash subjected to sonication or pectinolysis (51%, 45% and 32% content in the raw material, respectively) (Table 1). The best retention of ascorbic acid in the juices made from the thermally processed mash may have been caused by rapid inactivation of ascorbic acid oxidase. The thermal pre-treatment enables the maintenance of higher content of ascorbic acid despite the degradation of this compound during heating. For example, only about 10% of vitamin C is lost during the pasteurisation (85 °C, 30 s) of blackcurrant juice [36]. The effect of ascorbic acid oxidase in the other samples was longer, it may have caused oxidation of ascorbic acid. Bender et al. [37], pointed to this effect in their study. They found that the content of ascorbic acid in the blackcurrant juices made from the mash that had been heated (85 °C, 5 min) before pectinolysis was higher than when only pectinolysis was applied. At the same time, the authors found that the effect was species-dependent (they did not observe this dependence in raspberries or blueberries) [37]. Ramadan et al. [38] did not also observe a decrease in the content of ascorbic acid in the goldenberries juice made from the mash subjected to enzymatic treatment. In our study, the long-term of holding barberry mash during pre-treatment caused a decrease in the content of ascorbic acid in the juice. Laaksonen et al. [18], observed a similar dependence. They found that the content of ascorbic acid in the juices made from the mash subjected to enzymatic treatment (4 h) was significantly lower than in the blackcurrant juices made from the untreated mash. Clegg and Morton [39] indicated that the protective effect on ascorbic acid during pre-treatment (without earlier inactivation of ascorbic acid oxidase) might depend on the specific profile of phenolic compounds present in raw material.

2.7. ABTS+ free radical scavenging assay [34] 2,2-Azino-bis-(3-ethylbenzothiazoline-6-sulphonic acid) radical (ABTṠ+) was produced by reacting 0.007 mol/L ABTS (Sigma Aldrich Chemie Co., St. Louis, USA) water solution with 0.002 mol/L potassium persulphate. The phenolic extract (50 μL) was added into 5 mL diluted ABTS + solution. Then the absorption was measured after 6 min incubation at 30 °C at 734 nm. The antioxidative activity was expressed as micromoles of 6-hydroxy-2,5,7,8-tetramethylchroman-2-carboxylic acid (Trolox) per 1 g f.w. 2.8. Yield The yields of barberry juices (Y) were calculated according to equation below:

Yield (%) =

Ascorbic acid content [mg/100 g]

Amount of juice recovered (g ) × 100 Amount of mash taken (g )

2.9. Sensory quality The sensory properties of barberry juices were assessed by 10 trained panellists, who rated the desirability of colour, aroma, taste and consistency with a structured linear scale of 100 mm in length. The following boundary descriptors were assumed: highly undesirable (0 mm) and highly desirable (100 mm). The panel members marked the score of the samples on the scale, taking the boundary descriptors into consideration. The results were converted into numerical values in a scale of 0–10 units (0–100 mm, respectively). The sections of the scale marked by the panel members were converted into numbers by measuring the distance of each score from the scale boundary (0 mm) [35]. The juices were served in randomly numbered cups. The technological process in each of the tested variant was repeated three time. The results were reported as means of scores from these replications.

3.2. Anthocyanins content The content of anthocyanins in the barberries (B. amurensis) was 217 mg/100 g f.w., where the share of peonidin-3-O-glucoside amounted to 98%, whereas the remainder was cyanidin-3-rutinoside. The content of anthocyanins was more than two times greater than in B. vulgaris fruits (45–93 mg/100 g), which are also a red-skinned species [9,40]. The content of anthocyanins in violet species (B. microphylla,

2.10. Statistical analysis The analyses were conducted in triplicate. The analysis of variance (ANOVA) was used to determine the significance of the main effects. Tukey’s post hoc test was used to determine differences between the 3

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Table 2 Anthocyanins content in barberry fruits (Berberis amurensis) and juices from mash after different pre-treatment. Sample raw material juice from mash juice from mash juice from mash juice from mash

without pre-treatment after enzymatic treatment after thermal processing after ultrasound treatment

Cyanidin-3-rutinoside [mg/100 g]

Peonidin-3-O-glucoside [mg/100 g]

Total anthocyanin content [mg/100 g]

5.1 ± 0.4a 8.2 ± 1.4a 6.8 ± 0.6a 13.4 ± 1.3b 8.1 ± 1.6a

212 148 218 218 253

217 156 224 231 261

± ± ± ± ±

8b 15a 13b 11b 5c

± ± ± ± ±

9b 16a 14b 13b 6c

Means within columns marked by the same letter do not differ significantly.

of chlorogenic acid was also reported by Gundogdu [43] and Sokół–Łętowska [7] in their studies on B. vulgaris fruit. They also identified derivatives of synapic, ferulic, caffeic and p-coumaric acids, which were not found in the B. amurensis fruits in our study. As far as flavonoids are concerned, they found derivatives of quercetin, kaempferol, isorhamnetin and rutin, which were also identified in the samples analysed in our study (Tables 3, 4). The content of phenolic compounds in the juices made from the mash subjected to pectinolysis or heat treatment was 15% lower than in the fruits. The content in the samples pressed from the untreated mash or the mash subjected to sonication was about 30% lower. There was a significant (P < 0.05) decrease in the content of hydroxybenzoic acid derivatives in all the samples. In comparison with the raw fruits, the lowest (36%) decrease was noted in the samples made from the mash subjected to pectinolysis. The decrease in the other samples amounted to 50% (heat treatment), 69% (sonication) and 75% (no treatment). Among the hydroxybenzoic acids, two compounds were identified: 4hydroxybenzoate and formylsalicylic acid. Only the content of 4-hydroxybenzoate decreased significantly. The 4-hydroxybenzoate belongs to the cell wall-bound phenolics in plants [44]. Hence, this may result in the highest content of this compound in phenolic extracts obtained from whole fruits. The use of enzymatic, thermal pretreatment of the mash may improve the extractability of 4-hydroxybenzoate to the juice in relation to the juice obtained from the mash after sonification or untreatment. However, the biosynthetic pathway and degradation of 4hydroxybenzoate is not fully understood in plants [45,46] The following compounds were identified among hydroxycinnamic acid derivatives: chlorogenic acid (253–273 mg/100 g) and coumarin (2.2–4.2 mg/100 g). There were no significant differences between the fruits and juices obtained from untreated mash and subjected to pectinolysis or sonication in the content of chlorogenic acid. The highest content of this compound was in juice from mash subjected to heat treatment. Chlorogenic acid is one of the best substrate for polyphenol oxidase (PPO) [47]. PPO is largely responsible for enzymatic browning in fruits and vegetables. Hence, better retention of chlorogenic acid in juices obtained from mash subjected heat treatment may result from inactivation of PPO. The content of coumarins was significantly lower in the juices made from the untreated mash as well as the mash subjected to the heat treatment and sonication (2.2–2.8 mg/100 g). The following flavonoids were identified in the fruits and juices: flavonols (dihydrokaempferol, rutin, 6-hydroxykaempferol, quercetin 3-O-glucoside, quercetin 3-O-(6-O-malonyl-beta-D-glucoside), narcissin, kaempferol, quercetin 3-L-rhamnoside, kaempferol 3-(6⁗-malonylglucoside), isorhamnetin 3-(6⁗-malonylglucoside), afzelin, isorhamentin, quercetine) (58.2–66.6%); proanthocyanidins (kandelin A1, cinchonain 1a (27–35.7%)); flavanones (neocarthamin, carthamidin) (3.8–5.3%) and isoflavone (genistin (1.7–3%)), flavone (robinetin) (0.3–1.1%). The following flavonoids were dominant both in the fruits and juices: quercetin-3-O-glucoside, (47–65 mg/100 g), kandelin A-1 (21–39 mg/100 g) and cinchonain 1a (12.20–22 mg/100 g). In comparison with the raw material, the highest decrease in total flavonoid content was noted in the juices made from untreated mash (28%) and from the mash subjected to sonication (22%). The decrease in the content of above mentioned compounds in the samples subjected to pectinolysis or the heat treatment amounted to 9% and 2%, respectively

Berberis ilicifolia), which mainly grow in South America, is much higher and ranges from 638 to 1675 mg/100 g [11]. There are significant differences in the anthocyanins profile between individual species. Pelargonidin-3-O-glucoside was the dominant anthocyanin (77%) in B. vulgaris. Apart from that, cyanidin-3-glucoside was identified [7]. Glycosylated derivatives of delphinidin and petunidin were dominant in purple species. The main sugar moieties were glucoside and rutinoside. The profile of these compounds was broader, as there were also malvidin, peonidin and cyanidin derivatives [11]. The ultrasonic treatment of the barberry mash increased the content of peonidin-3-O-glucoside in the juice by about 20%, as compared with its content in the fruits. The content of peonidin-3-O-glucoside in the juices made from the mash subjected to pectinolysis or heat treatment was comparable to the content in the fruit. However, it was about 30% lower in the samples made from the untreated mash. As far as cyanidin3-rutinoside is concerned, only the heat treatment of the mash caused a significant (P < 0.05) increase in its content in the juice (2.5 time more), as compared with the content in the fruits. The content of cyanidin-3-rutinoside in the fruits and other juices did not differ significantly (Table 2). As the results showed, the increase in the content of individual anthocyanins in the juice after the pre-treatment of the mash may have been related to their profile. This dependence can be observed when different methods are used to extract anthocyanins from berry fruits. Chen et al. [41] researched the extraction of anthocyanins from red raspberries with the conventional method at 71 °C and with ultrasonication (at a temperature below 40 °C). The ultrasound-assisted extraction caused an increase in the total content of anthocyanins. However, conventional extraction resulted in a higher content of cyanidin-3-rutinoside. The content of peonidin-3-O-glucoside in the juices made from the mash exposed to ultrasounds as well as the mash treated thermally or enzymatically was greater than in the juices made from the untreated mash. The increase may have been caused by better extractability of this compound during the pre-treatment. This effect was observed by Buchert et al. [42] in their research on the yield of anthocyanins in bilberry and blackcurrant juices after the enzymatic treatment of the mash, as well as by Borowska et al. [25], who researched the thermal (85 °C for 5 min) or enzymatic treatment of chokeberry mash. 3.3. Polyphenols content The content of phenolic compounds in the barberry fruits was 636 mg/100 g. Reference publications provide no data on the content of phenols in the B. amurensis species. However, studies on the B. vulgaris and Berberis integerrima genotypes showed that content of phenolic compounds ranged widely from 261 to 1074 mg/100 g [7,9,10]. In our study, 25 phenolic compounds were identified in the B. amurensis fruits, whereas 24 were found in the juices (including two anthocyanins). 41% of them were derivatives of hydroxycinnamic acids, 32% were derivatives of hydroxybenzoic acids and 27% were flavonoids (Tables 3, 4). According to references, the share of flavonoids in the phenolic compound profile of B. vulgaris and B. integerrima ranges from 36% to 88% [10]. The following compounds were dominant in the B. amurensis fruits: chlorogenic acid (257 mg/100 g), 4-hydroxybenzoate (188 mg/ 100 g) and quercetin 3-O-glicoside (65 mg/100 g). The dominant share 4

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Table 3 Identification of phenolic compounds in barberry fruits (Berberis amurensis) and juices. UHPLC-Peak No.

Identified compound*

Ion formula

Time (min)

[M]+, [M+H]+ (m/ z)

Match (%)**

Compound identified in juice (j) and/or raw material (rm)

1 2 3 4 5 6 7 8 9 10 11 12 13 14

Coumarin Chlorogenic acid Genistin Neocarthamin Dihydrokaempferol Peonidin 3-O-glucoside Carthamidin Kandelin A-1 4-Hydroxybenzoate Formylsalicylic acid Rutin 6-Hydroxykaempferol Quercetin 3-O-glucoside Quercetin 3-O-(6-O-malonyl-beta-Dglucoside) Cyanidin-3-rutinoside Cinchonain 1a Narcissin Kaempferol Quercetin 3-L-rhamnoside (Quercitrin) Robinetin Kaempferol 3-(6′'''-malonylglucoside) Isorhamnetin 3-(6′'-malonylglucoside) Afzelin Isorhamentin Quercetine

C9H7O2 C16H19O9 C21H21O10 C21H21O11 C15H13O6 C22H23O11 + C15H13O6 C39H33O15 C7H6O3 C8H7O4 C27H31O16 C15H11O7 C21H21O12 C24H23O15

8.47 8.78 10.58 11.90 13.42 14.20 15.65 17.22 18.71 20.27 20.32 20.86 21.20 21.85

147.044 355.102 433.113 451.124 289.071 463.124 289.071 741.181 139.040 167.035 611.160 303.051 465.103 551.103

85 100 94 80 73 89 88 71 82 60 100 78 97 91

j/rm j/rm j/rm j/rm j/rm j/rm j/rm j/rm j/rm j/rm j/rm j/rm j/rm j/rm

C27H31O15 + C24H21O9 C28H33O16 C15H11O6 C21H21O11 C15H11O7 C24H23O14 C25H25O15 C21H21O10 C16H13O7 C15H11O7

22.00 22.04 22.71 23.28 23.62 23.97 24.91 26.37 26.65 27.68 29.18

595.165 453.118 625.176 287.056 449.108 303.050 535.108 565.119 433.168 317.066 303.051

81 68 94 100 79 85 90 58 94 86 96

j/rm j/rm j/rm j/rm j/rm j/rm j/rm j/rm rm j/rm j/rm

15 16 17 18 19 20 21 22 23 24 25

* The compounds were identified according to CSI:FingerID and MetFrag. ** The percentage of match was computed with CSI: FingerID.

Table 4 Phenolic compounds content and antioxidant capacity in barberry fruits (Berberis amurensis) and juices from mash after different pre-treatment. Compounds

Juice from mash without pre-treatment

Juice from mash enzymatic treatment

Juice from mash thermal processing

Juice from mash ultrasound treatment

Hydroxybenzoic acids derivatives [mg/100 g] 4-Hydroxybenzoate 188 ± 8d Formylsalicylic acid 18 ± 2a Total 206 ± 11d

36 ± 2a 16 ± 2a 52 ± 5a

115 ± 5c 17 ± 1a 132 ± 8c

82 ± 4b 20 ± 1a 102 ± 6b

48 ± 2a 16 ± 1a 64 ± 4a

Hydroxycinnamic acids derivatives [mg/100 g] Coumarin 4.2 ± 0.5c Chlorogenic acid 257 ± 4ba Total 261 ± 5a

2.2 ± 0.3a 268 ± 4bc 270 ± 5ab

3.6 ± 0.1bc 253 ± 1a 257 ± 2a

2.5 ± 0.2a 273 ± 6c 276 ± 8c

2.8 ± 0.1a 267 ± 3bc 270 ± 4ab

4.4 ± 0.4bc 15 ± 1b 1.23 ± 0.15b 65 ± 2c 1.48 ± 0.12a

2.7 ± 0.4a 10 ± 1a 0.83 ± 0.12a 47 ± 5a 1.55 ± 0.04a

3.5 ± 0.1a 8 ± 1a 0.63 ± 0.02a 53 ± 1ab 1.97 ± 0.13b

4.7 ± 0.4c 10 ± 1a 0.87 ± 0.06a 61 ± 3bc 1.62 ± 0.13ab

3.1 ± 0.2a 10 ± 1a 0.78 ± 0.02a 50 ± 2a 1.48 ± 0.12a

3.9 ± 0.2a 0.58 ± 0.08a 18.3 ± 1.4b

4.3 ± 0.4a 0.85 ± 0.12b 11.5 ± 0.9a

4.1 ± 0.1a 0.87 ± 0.02b 13.0 ± 0.3a

4.5 ± 0.2a 0.85 ± 0.08b 13.1 ± 0.7a

4.1 ± 0.2a 0.75 ± 0.04ab 12.1 ± 0.4a

0.12 ± 0.02ab 0.03 ± 0.00a 0.17 ± 0.02 0.17 ± 0.02a 0.17 ± 0.02ab 34 ± 3b 14.58 ± 0.08a 2.9 ± 0.3bc 3.5 ± 0.3a 2.8 ± 0.3a 0.50 ± 0.00a 169 ± 8c 636 ± 20c 71 ± 1b

0.07 ± 0.02a 0.03 ± 0.01a nd 0.15 ± 0.04a 0.08 ± 0.02a 21 ± 3a 12.20 ± 0.07a 2.0 ± 0.2a 4.5 ± 0.7a 3.1 ± 0.4a 1.25 ± 0.19b 123 ± 14a 445 ± 26a 34 ± 3a

0.18 ± 0.05b 0.07 ± 0.01b nd 0.35 ± 0.07b 0.22 ± 0.02b 33 ± 1b 22 ± 3b 2.9 ± 0.1bc 4.0 ± 0.1a 4.5 ± 0.1b 1.72 ± 0.02c 154 ± 7bc 543 ± 13b 65 ± 4b

0.08 ± 0.02a 0.02 ± 0.00a nd 0.08 ± 0.02a 0.33 ± 0.05c 39 ± 2b 14 ± 2a 3.6 ± 0.3c 4.1 ± 0.2a 5.0 ± 0.2b 1.65 ± 0.16c 165 ± 11c 542 ± 20b 63 ± 5b

0.05 ± 0.00a 0.01 ± 0.00a nd 0.07 ± 0.02a 0.22 ± 0.02b 25 ± 2a 13 ± 2a 2.5 ± 0.1ab 4.0 ± 0.1a 3.4 ± 0.2a 1.02 ± 0.06b 132 ± 9ab 466 ± 14a 30 ± 2a

Flavonoids [mg/100 g] Dihydrokaempferol Rutin 6-hydroxykaempferol Quercetin 3-O-glucoside Quercetin 3-O-(6-O-malonyl-beta-Dglucoside) Narcissin Kaempferol Quercetin 3-L-rhamnoside (Quercitrin) Kaempferol 3-(6⁗-malonylglucoside) Isorhamnetin 3-(6″-malonylglucoside) Afzelin Isorhamentin Quercetine Kandelin A-1 Cinchonain 1a Carthamidin Neocarthamin Genistin Robinetin Total Total phenol content ABTS [µmol Trolox/g]

Raw material

Means within raw marked by the same letter do not differ significantly. nd – not detected. 5

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Table 5 Effect of mash pre-treatment on barberry (Berberis amurensis) juice yield and sensory quality. Sample juice juice juice juice

from from from from

mash mash mash mash

without pre-treatment after enzymatic treatment after thermal processing after ultrasound treatment

Yield [%]

Colour

59 60 56 58

6.2 8.0 8.3 8.7

± ± ± ±

1a 3a 7a 4a

± ± ± ±

Aroma 0.4a 0.7b 0.5b 0.5c

7.7 7.3 6.8 7.8

± ± ± ±

Taste 1.6a 1.8a 2.2a 1.5a

5.3 4.8 4.7 5.7

± ± ± ±

Consistency 2.1a 1.7a 1.8a 1.8a

8.2 6.7 4.7 7.7

± ± ± ±

1.5b 1.5ab 2.2a 1.3b

Means within columns marked by the same letter do not differ significantly.

that the colour of juices made after the sonication of grape mash was better than the colour of the samples subjected to pectinolysis. In the case of aroma or taste, no significant differences were found between the tested samples. The taste was rated lower (4.7–5.7) than the aroma (6.8–7.8) due to the very sour taste of the raw material. The thermal treatment of the mash significantly (P < 0.05) deteriorated the consistency (4.7). The decrease in these scores was caused by the lack of stability of suspended particles in cloudy juice. The ratings of the consistency of the other samples ranged from 6.7 to 8.2 (Table 5).

(Tables 4). Thus, the enzymatic and thermal treatment of the mash resulted in the best of the phenolic compounds retention in the juice, as compared with the raw material. The authors of various studies on berry fruits indicated this effect [18,42]. There is little data on mash sonication in the juice production technology. Lieu and Le [48] compared the enzymatic treatment with the sonication of grape mash. They found that the content of phenolic compounds in the juice made from the mash subjected to sonication was 11% greater than in the product made from the mash subjected to pectinolysis. There was no such relationship found in our study. The effectiveness of sonication in releasing phenolic compounds from the mash into the juice may be related to their profile and their binding with the tissue structure. For example, in the study by Guandalini et al. [49], sonication did not increase the efficiency of extraction of phenolic compounds from mango peel, although this influence was described in studies on other raw materials (mandarin peel, grape skin) [50,51]. Some authors indicate that ultrasounds may cause greater degradation of phenolic compounds in the plant tissue as they damage cell membranes by cavitation [52].

4. Conclusion Berberis amurensis Rupr. fruits collected as fully mature from plants grown in central Poland, were a rich source of phenolic compounds and anthocyanins and an average source of ascorbic acid. The sonication of the mash increased the content of peonidin-3-O-glucoside (the main anthocyanin of B. amurensis) in the juice by about 20%, as compared with its content in the fruits. This positively affected the perception of the juice colour. The enzymatic and thermal treatment of the mash resulted in the best retention of phenolic compounds in the juice, as compared with the raw material. Nevertheless, the content of 4-hydroxybenzoate decreased significantly, whereas the content of chlorogenic acid remained at the same level or was higer and quercetin-3-Oglycoside was lower or at the same level, respectively. The thermal treatment of the mash resulted in the smallest loss of ascorbic acid in the juice. The antioxidative capacity of the juices was correlated with the content of phenolic compounds. Berberis amurensis fruits are a valuable raw material for the production of juices. The heat treatment and sonication of the mash may improve their quality. Therefore, it seems reasonable to further optimise the technological process to improve the sensory quality of juices and increase their content of bioactive compounds.

3.4. Antioxidant activity The antioxidative activity of the raw material was 71 µmol Trolox/g f.w. Ruiz et al. [6] observed similar antioxidative activity in their study on B. microphylla fruits (on average 74.5 µmol Trolox/g f.w.). There was no significant difference in the antioxidative capacity between the juices made from the mash subjected to pectinolysis or heat treatment and the raw material. However, the antioxidative activity of the juices made from the untreated mash or from the mash subjected to sonication decreased by about 55% (Table 4). There was a statistically significant correlation between the content of phenolic compounds and the antioxidative activity (R2 = 0.78). Zovko Končić et al. [53] also found a correlation between the content of phenolic compounds and the antioxidative activity of B. vulgaris and B. croatica roots, twigs and leaves. Ruiz et al. [6] observed such a relation for B. microphylla fruit extract.

Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

3.5. Yield The sonication, enzymatic and thermal treatment did not have significant influence on the juice pressing efficiency, which ranged from 56% to 60% (Table 5). There have been few studies on the use of sonication for mash processing. Bora et al. [21] also did not observe any influence of the treatment on the process efficiency in banana juice. In the case of enzymatic and thermal treatment of berry mash, both the increase and no effect of the process on yield were described [18,25].

Acknowledgement This study was supported with the grant for the project ‘Bioactive food’ POIG 01.01.02-00061/09. References [1] Z. Ye, K. Van Dyke, B. Yang, Interaction of berbamine and chloroquine or artemisinin against chloroquine-sensitive and -resistant plasmodium falciparum in vitro, Drug Dev. Res. 30 (1993) 229–237, https://doi.org/10.1002/ddr.430300405. [2] H.-Y. Lee, C.-W. Kim, Studies on the constituents of Berberis amurensis Ruprecht, Korean J. Pharmacogn. (Korea Republic) 28 (1997) 257–263. [3] M.M. Yusupov, A. Karimov, R. Shakirov, P.G. Gorovoi, M.F. Faskhutdinov, M.G. Levkovich, N.D. Abdullaev, Berberis alkaloids. XXVI. An investigation of the alkaloids of Berberis amurensis, Chem. Nat. Compd. (1993) 338–340, https://doi. org/10.1007/BF00630534 29. [4] Z. Fatehi-Hassanabad, M. Jafarzadeh, A. Tarhini, M. Fatehi, The antihypertensive and vasodilator effects of aqueous extract from Berberis vulgaris fruit on hypertensive rats, Phyther. Res. 19 (2005) 222–225, https://doi.org/10.1002/ptr.

3.6. Sensory quality The juice made from the mash subjected to sonication was rated the highest (8.7) for its colour. There were no significant differences in the colour of the juice made from the mash subjected to the heat treatment and pectinolysis. The colour of the juices made from the untreated mash were rated the lowest (6.2). There was a statistically significant correlation (R2 = 0.73) between the sensory evaluation of colour and the content of anthocyanins in the samples. Lieu and Le [48] also observed 6

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