COMPARISON OF ANTIOXIDATIVE AND SYNERGISTIC EFFECTS OF SKULLCAP (SCUTELLARIA BAICALENSIS GEORGI) IN SUNFLOWER OIL-IN-WATER EMULSION DURING STORAGE

Aneta Wojdyło, Jan Oszmiański, Anna Sokół-Łętowska
Department of Fruit, Vegetable and Cereal Technology, Wrocław University of Environmental and Life Sciences, Poland

ABSTRACT

The antioxidative activity and synergistic effects of skullcap extracts and other natural compounds (α-tocopherol, β-carotene, citric and ascorbic acid) were evaluated in sunflower oil-in-water emulsion during storage at 50°C in the light exposure (3600-3900 lx). The oxidation process was followed by measuring the formation of primary (peroxide value) and secondary (TBARS) oxidation products, which were monitored during periods of storage. Flavones of skullcap (S) actively protected the sunflower oil-in-water emulsion during storage. Synergistic mixtures: flavones of S and α-tocopherol, β-carotene, citric and ascorbic acid exhibited stronger antioxidative properties than single components of these mixtures or synergists alone but weaker than flavones alone.

Key words: skullcap, antioxidant, synergism, sunflower oil-in-water emulsion, storage in light.

INTRODUCTION

Autooxidation or oxidative rancidity, which occurs during food storage, is the major cause of quality losses in plant oils and other fats included in food [11]. To retard or prevent the oxidative deterioration, the antioxidants are added into food. The antioxidants (of synthetic or natural origin) maintain the quality and extend the shelf-life of many food products.

Nowadays, consumers generally prefer natural compounds or vitamin antioxidants (tocopherols, ascorbic and citric acid and their salts) rather than synthetic additives [19]. Polyphenols are one of the most important groups of natural antioxidants. They occur only in the material of plant origin.

Many herbs and spices are known to be better antioxidants than the food antioxidants (vitamin C, E or β-carotene) used in oil and food stability. Many studies have been made to examine the antioxidative activity of crude compounds or extracts. However, not all of consumers do accept those, because they give new odour, taste, and colour to the food, i.e. rosemary, sage, oregano and thyme.

Many herbs and spices, Scutellaria baicalensis Georgi among them, belonging to the Labiatae family exhibited the highest antioxidative activity. Skullcap is one of the most important medicinal herbs widely used for the treatment of various inflammatory diseases, cancer, allergy, hepatitis, tumours and used as sedative, antiviral, and antioxidant in East Asian countries such as China, Korea and Japan [5, 9, 17, 21, 22].

The root of this plant has been reported to contain a large number (over 40) of flavonoids (more than 20% in dry matter) such as the glucuronides, and other constituents, like phenyl alcohols, sterols, essential oils, and amino acids. Baicalin, a flavone glucuronide, is the most predominant flavonoid, varying from 12-19% in the dry root. Other common flavonoids in Scutellaria baicalensis are baicalein, wogonin, wogonoside, oroxylin A, skullcapflavone I and II, and many others [23]. This flavonoid has metoxyl and/or hydroxyl groups at various positions of the aromatic rings A (Fig. 1). In recent years very often was studies flavones of Skullcap in relation to the influence on the human organism. This is particularly important as there are reports that baicalein and wogonin have weak benzodiazepine-receptor binding activity[16], that glucuronide metabolites have been detected in human urine [4, 12] and that some human gut microflora and human tissue β-glucuronidase can hydrolyse such glucuronides [20].

Fig. 1. Structure of the four major flavonoids in the radix of Scutellaria baicalensis Georgii

Baicalin: R1=OH, R2= glucuronic acid, R3=H Baicalein: R1=OH, R2= H, R3=H Wogonoside: R1=H, R2= glucuronic acid, R3=OCH3 Wogonin: R1=H, R2=H, R3=OCH3

The use of synergistic mixtures of antioxidants allows for a reduction in the concentration of each compound and also increases the antioxidative effectiveness as compared with the activity of each separate components. However, little is reported about the interaction of plant phenolic and other antioxidants such as tocopherols, ascorbic and citric acid which are present in most of the food lipid systems [13].

The aim of this work is to evaluate the antioxidant and synergistic effect of skullcap, alone and in combination with α-tocopherol, β-carotene, citric and ascorbic acid during storage of sunflower oil-in-water emulsion at 50°C in light exposure (3600-3900 lx).

MATERIALS AND METHODS

Materials
Traditional sunflower oil, free of synthetic antioxidants, was purchased from local shop. α-tocopherol, β-carotene, citric and ascorbic acid, malondialdehyde (MDA), Tween 20, were purchased from Sigma Chemical Co. (St. Louis, MO, USA). Thiobarbituric acid (TBA) was purchased from LOBA (Germany); active carbon and methanol were purchased from Polish Factory of Chemicals-POCH (Gliwice, Poland).

Powder flavones of skullcap were purchased from WIMEX BEIJNG.

HPLC analysis of flavones of Skullcap
Powder flavones of Skullcap were analyzing by HPLC analysis. A Polymer Laboratories PLRP-S 100 Å (5µm) column (Shropshire, United Kingdom) was used for the analysis. The solvents used were 80% acetonitrile in 4.5% formic acid (A) and 4.5% formic acid (B), at a flow rate of 1 mL · min^-1. The elution profile was: 0-7 min 0-85% B in A, 7-15 min 85-0% B in A, 15-21 min 0-100% B. Recording was carried out at 280 nm. The composition of purchased skullcap powder (S) was determined by HPLC contained 95% baicalin (Fig. 2).

Fig. 2. HPLC chromatograms of flavones of skullcap: 1 – baicalin, 2, 3, – flavones not identified, 4 – baicalein detected at 280 nm

Purification of oil from natural polyphenols
Purification of oil from natural polyphenols was described previously by Chimi et al. [60]. 50 g of oil was diluted in 100 ml hexane and mixed 4 times with 50 ml MeOH: water (60:40, v/v) for 3 min, in order to remove natural polyphenols. Next, oil contained in the hexane layer was mixed with 30 g of active carbon using a shaker (ELPAN type 358S, Poland) for 30 min. After shaking, the mixture was filtered on anhydrous sodium sulphate (Na₂SO₄) and hexane was evaporated on vacuum evaporator (UNIPAN type 350 P, Poland) at 40°C.

Preparation and storage of oil-in-water emulsion with antioxidant
Oil-in-water emulsion containing 3 g of sunflower oil, was mixed with 150 ml of 0.05 M TRIS:HCL buffer (pH 7.54) and then emulsified with 3% Tween-20. The antioxidant was dissolved in TRIS:HCL buffer, and underwent sonication (5 min) in ultrasonic sonicator model (UNITRA, Olsztyn, Poland) The emulsion with antioxidant (200 ml) was transfered in to a 500 ml Erlenmeyer flask and homogenized by Heidolph DIAX 900 (Merck) for 3 min.

The antioxidants or their mixtures were added to sunflower oil in the following quantities:

as individual components:

• 100, 300 and 500 ppm flavones of skullcap (S);

• 100 ppm: skullcap (S,) citric acid (CA,) ascorbic acid (AA,) α-tocopherol (TOK,) and β-carotene (CAR)

as two – components mixtures:

• mixtures of 100 ppm S and 100 ppm: CA, AA, TOK, CAR;

• mixtures of 100 ppm S and 50 ppm: CA, AA, TOK, CAR;

• mixtures of 50 ppm S and 50 ppm: CA, AA, TOK, CAR.

the sample without antioxidant was used for the control (CONTROL).

These oil-in-water emulsions were stored in a model conditions in the light exposure (3600-3900 lx, de Luxe ‘TLD’ 18W/965, Philips) at 50°C for 4 days. Every day before analysis oil-in-water emulsions, were mixed for 2 min by homogenizer (Heidolph DIAX 900, Merck) for the be paying on delivery of representative test. Oxidative stability was determined by measuring primary and secondary oxidation products every 24 h. All oil-in-water emulsions were performed in duplicate.

Ferric thiocyanate analysis for peroxides
Peroxide value was carried out by procedures described by Haraguchi et al. [10]. The 0.1 ml emulsion was diluted with 9.7 ml of 75% EtOH, to which 0.1 ml of 30% ammonium thiocyanate was added. Precisely 3 min after the addition of 0.1 ml of 20 nM ferrous chloride diluted in 3.5% hydrochloric acid to the reaction mixture, the absorbance at 500 nm was measured. The absorbance was measured using a PC 2401 UV-VIS spectrophotometer (Shimadzu, Tokyo, Japan). All determinations were performed in triplicate.

The inhibition of oxidative process [%] of all tested antioxidants was calculated according to the following formula:

where S_d is the sample with the antioxidant from the given day (d,) S₀ is the sample with the antioxidant from the first day_, C_d is the control sample from the given day (d,) C₀ is the control sample from the first day.

Thiobarbituric acid method
Thiobarbituric acid reactive substances (TBARS) were quantified using a modified method of Mei et al. [24]. A TBA solution was prepared by mixing 15 g of trichloroacetic acid, 0.375 g of TBA, 2 ml of HCl, and 82,9 ml of distilled water. Two millilitres of TBA solution was mixed with 5 ml of emulsion and 3 ml of distilled water. The mixture was heated in boiling water bath for 20 min, cooled to room temperature using tap water, and centrifuged at 10 000 g for 5 min. Absorbance was measured at 532 nm. A calibration curve was prepared with pure malondialdehyde (MDA) standard, and results were expressed as nmol MDA equivalents per g of oil. All determinations were performed in triplicate.

Statistical analysis
Results were given as mean ± standard deviation of three independent determinations. All statistical analyses were performed with Statistica 7.0. One-way analysis of variance (ANOVA) by Duncan’s test was used to compare the means. Differences were considered to be significant at P<0.05.

RESULTS AND DISCUSSION

Effect of plant antioxidant on sunflower oil-in-water emulsion
Samples of oil emulsion with natural, plant antioxidant only were stored at 50°C in the light (3600-3900 lx) exposure for 8 days. The primary and secondary oxidation products were monitored during storage periods. The formation of this product increased significantly more in control sunflower emulsion than in emulsion with plant antioxidant (P<0.05). Antioxidant activity of the skullcap was first compared at a concentration of 100, 300, 500 ppm. The peroxide values of sunflower emulsion with added crude skullcap only, at 50°C with light, are presented in Figure 3.

Fig. 3. Effect of different skullcap flavones doses on the formation of lipid peroxide (A) and MDA (B) of oil-in-water emulsion during 8 days storage at 50°C and illumination (3600-3900 lx)

Hydroperoxides are the primary products formed during oxidation, but they are also labile intermediate compounds that decompose into several secondary oxidation products. The protective effect of flavones on oxidation of oil-in-water emulsions was dose-dependent. As the concentration of flavones increased from 100 to 500 ppm, the hydroperoxides and secondary products of emulsion decreased. The 100 ppm skullcap flavones dose was twice weaker in inhibiting oxidative reactions than the other doses examined; 500 and 300 ppm dose retarded the hydroperoxide and secondary product formation significantly (P<0.05). The increase of hydroperoxides was lowered due to addition of skullcap and lasted for 4 days, whereas in the control sample only for 1 day. To confirm the above relation, inhibition was calculated (shown in Fig. 4). The ability to inhibit formation of peroxides as well as secondary oxidation products in the stored emulsion samples, expressed in relation to the products formed when tested without an antioxidant, was high in the first days. Inhibition values calculated after the first day of emulsion oxidation ranged from 7% up, and then decreased. Samples with 100 ppm dose of S were the first to lose their activity. For samples stabilised with a 300 ppm or 500 ppm dose, the ability continued at a high level. As peroxides in the oxidation process are formed at the beginning of the oxidation period, it was also possible to calculate inhibition for the 8th day of sample storage. The peroxide inhibition measured in those days was at low level, i.e. 5% for the sample with addition of 100 ppm and 25% for the sample with 500 ppm of flavones. The secondary oxidation products inhibition measured in those days was at low level, i.e. 6% for the sample with addition of 100 ppm and 33% for the sample with 500 ppm of flavones. The antioxidant activity of flavonoid is governed by many factors including its structure and the number and location of polyphenolic hydroxyl groups on the A, B, and C rings [25]. Yang et al. [29] suggested, that baicalin was more potent than the coresponding flavonoids (such as rutin, luteolin) because of the presence of the o-dihydroxyl group on the A ring, not on B and C. Flavonoid of skullcap – baicalein indicates that number and position of hydroxyl groups on rings A, not on B and C, play important role in contributing to antioxidant activity (Fig. 1).

Fig. 4. Influence of flavones of skullcap (S) on the inhibition of oxidative process [%] in oil emulsion stored at 50°C in light (3600-3900 lx)

Furthermore, the antioxidative activity obtained in samples with the addition of flavones of skullcap during their storage in light (3600-3900 lx) indicates their high photoprotective potential. Among 47 methanolic plant extracts investigated by Jung et al. [18] for the active inhibitors of oil photooxidation process, only few of them exhibited such properties. Among them there were flavones isolated from the roots of Scutellariae baicalensis Radix. This is the most significant as, according to the authors, synthetic compounds, such as BHA and BHT, fail to show any activity in the event of photooxidation processes.

Synergistic effect of antioxidant vitamins in sunflower oil-in-water emulsion
In order to determine the antioxidative activity level of skullcap flavones, some natural antioxidants have been tested at 100 ppm dose under the same conditions allowing comparable results.

The rate of hydroperoxide formation increased sharply after one day of oxidation (Fig. 5). During the first 3 days of incubation, the rate of hydroperoxide formation increased significantly more in the presence of 100 ppm of CAR than in the control emulsion and the emulsion with skullcap flavones added. The sample with β-carotene exhibited a prooxidative effect. TOK, AA and CA inhibited hydroperoxide formation and showed high antioxidative activity during the first two days, similar to this of 100 ppm skullcap flavones.

The formation of MDA was increased gradually in the similar way in all samples throughout the storage period, as was previously done with peroxide value (Fig. 6). Formation of MDA began rapidly after two days. The present results demonstrate clearly that the S was more effective than CAR, TOK, AA, and CA in these conditions.

Fig. 5. Antioxidant effect of different compounds (carotene, tocopherol, ascorbic and citric acid) (100 ppm) compared to dose of skullcap (100 ppm) on the formation of hydroperoxide of oil-in-water emulsion during 4 days of storage at 50°C and illumination (3600-3900 lx)

Fig. 6. Secondary oxidation products of sunflower emulsion without antioxidant and with added antioxidant mixtures of flavones with β-carotene, α-tocopherol, ascorbic and citric acid in different dose during storage at 50°C in light (3600-3900 lx)

Effect of antioxidant mixtures of skullcap flavones with CA, AC, CAR, and TOK
During the storage of oil-in-water emulsion, mixtures restricted to a different degree the formation of peroxides and secondary oxidation products. In the case of the activity of skullcap flavones, it was found that in the emulsion environment their antioxidative activity increased along with an increase of dose. When investigating the synergistic activity of mixtures in that respect, such explicit relationship was not found. The activities of doses tested, irrespectively of synergistic compound types used, could not be explicitly arranged in the following order: 100/100 > 100/50 [polyphenol/synergent]. In the case of mixtures of S with CAR, irrespectively of dose level, only after the first day an intensive increase of secondary oxidation products occurred, which continued until the end of the storage period (180 – 250 nM MDA/g oil). Also, the largest quantities of MDA were formed when emulsion was stabilized with mixture of S with TOK, AA and CA at the lowest doses tested (100/50 and 50/50 ppm). Moreover, in those mixtures the unfavourable so-called prooxidative effect was measured. The inhibition calculated for those samples varied and after the first day of storage ranged from 87% to 1%. The mixtures in which the total dose of both components amounted to 200 ppm (100+100 ppm) featured the highest activity. In the case of those mixtures, a considerable increase of MDA was measured for combinations of S+AA antioxidants after the second day and for S+TOK and S+CA combinations after the third day of emulsion storage at 50°C and exposure to light. Furthermore, the activity of AA and CA mixtures with S at that dose level was comparable to the activity of 100 ppm skullcap flavones.

The utilisation of CA synergistic properties is possible since, according to Szukalska [28] this compound is effective in the presence of tocopherol or other phenolic antioxidants. Ziemlański and Wartanowicz [30] have reported that flavonoids retard the decomposition of ascorbate into dehydroascorbate. On the other hand, ascorbic acid inhibits oxidative degradation of flavonoids. Compounds such as ascorbic and citric acid are typical secondary antioxidants able to exhibit their activity only when another antioxidant, the so-called primary antioxidant, is present. Furthermore, these are typical hydrophilic compounds, which are more active antioxidants in o/w than w/o environment [26]. Beddows et al. [3] in their studies have demonstrated positive synergistic effects of ascorbic acid combined with oregano, marjoram and rosemary, emphasizing at the same time that the ascorbic acid used alone as a sunflower oil stabiliser fails to show the desired antioxidative effect. It has been confirmed by the results obtained in these studies. However, β-carotene in oil emulsions as well as in oils alone is more effective as an antioxidant when used together with α-tocopherol than combined with either of these compounds alone [11, 27].

Despite the opportunity to utilise synergistic properties of antioxidative vitamins when used with natural plant preparations, conflicting opinions are still found in publications.

Hras et al. [14] in their studies have demonstrated that mixtures of polyphenols with synergists tested in sunflower oil stored at 60°C for 11 days exhibited stronger antioxidative effects than the antioxidative compounds alone. They have proved that TOK in combination with the rosemary extract does not exhibit such a strong antioxidative effect as in the mixture with citric acid or ester derivatives of this vitamin. However, Banias et al. [2] also reported that α-tocopherol showed a strong negative effect with different plant extracts. Frankel and Huang [7]; Frankel et al. [8], Huang et al. [15] and Hopia et al. [13] have come to a different conclusion after showing in their studies the higher antioxidative activity of α-tocopherol in emulsions than in oils when used in combination with plant extracts. Furthermore, they have proved that the antioxidative activity in multiphase environments results from the phenomenon of their interactions in parts where these compounds are concentrated.

Frankel et al. [8] and Huang et al. [15] showed that the relative effectiveness of lipophilic and hydrophilic antioxidants was dependent on the lipid substrate, physical state (bulk oil, emulsion,) antioxidant concentration, oxidation time and temperature, and the analytical method used to determine the extent and end point of oxidation. Frankel et al. [8] observed that in the oil-in-water emulsion system, lipophilic antioxidant (skullcap, α-tocopherol) are sufficiently surfaceactive to be oriented in the water-oil interface in order to protect oil against oxidation better. In contrast, hydrophilic antioxidants are oriented in the air-oil interface and become more protective against oxidation than the lipophilic antioxidants, which remain dissolved in the oil.

Moreover, plant oils contain natural antioxidants in their composition. The sunflower oil used for preparation of the emulsion did not contain natural polyphenols because they had been removed from it, however; it did contain trace amounts of tocopherols (data not shown). The tocopherol level, even if very small, could have additional influence on the activity of that mixture. That fact can further explain the different behaviour of β-carotene as compared to α-tocopherol, in spite of lipophilic nature of those compounds.

CONCLUSIONS

Flavones of Scutellaria baicalesis Georgi show the highest antioxidative activity in relation to primary and secondary oxidation products during storage of oil-in-water emulsion in the light at 50°C. Ascorbic and citric acid, α-tocopherol, β-carotene used alone, failed to achieve the desired, high antioxidative activity. Synergistic activity between flavones of skullcap and the compounds tested, mainly depended on the dose of particular mixture components. The performed tests have proved that it is possible to use the tested compounds in combinations but in order to achieve the high antioxidative activity (similar to the activity exhibited by the tested dose of 500 ppm S) particular component doses would have to be increased. The possibility to use these compounds is even more interesting since these compounds come from natural sources and, therefore, they are considered acceptable by food consumers.

The positive and high synergism between these preparations makes it possible to increase the stabilising activity of mixture without increasing the addition of individual components above permissible levels. By using polyphenol-synergist mixture, the cost of fat stabilization is also reduced as well as undesirable sensations associated with the taste and odour of natural antioxidants such as oregano, rosemary, and sage. When analysing the antioxidative activity values of mixtures, it was found that in the presented polyphenol-synergist system, not all combinations of compounds have exhibited high synergism in this environment.

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Accepted for print: 19.03.2007

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Aneta Wojdyło
Department of Fruit, Vegetable and Cereal Technology,
Wrocław University of Environmental and Life Sciences, Poland
C.K. Norwida 25, 50-375 Wrocław, Poland
Phone: (+48 71) 320 54 74
Fax: (+48 71) 320 54 77
email: aneta@ozi.ar.wroc.pl

Jan Oszmiański
Department of Fruit, Vegetable and Cereal Technology,
Wrocław University of Environmental and Life Sciences, Poland
C.K. Norwida 25, 50-375 Wrocław, Poland
Phone: (+48 71) 320 54 74
email: oszm@ozi.ar.wroc.pl

Anna Sokół-Łętowska
Department of Fruit, Vegetable and Cereal Technology,
Wrocław University of Environmental and Life Sciences, Poland
C.K. Norwida 25, 50-375 Wrocław, Poland
Phone: (+48 71) 320 54 74
Fax: (+48 71) 320 54 77

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