The Effect of Cooking on Total Polyphenolic Content and Antioxidant Activity of Selected Vegetables

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1 International Journal of Food Properties ISSN: (Print) (Online) Journal homepage: The Effect of Cooking on Total Polyphenolic Content and Antioxidant Activity of Selected Vegetables Memnune Şengül, Hilal Yildiz & Arzu Kavaz To cite this article: Memnune Şengül, Hilal Yildiz & Arzu Kavaz (2014) The Effect of Cooking on Total Polyphenolic Content and Antioxidant Activity of Selected Vegetables, International Journal of Food Properties, 17:3, , DOI: / To link to this article: Copyright Taylor and Francis Group, LLC Accepted author version posted online: 03 Apr Published online: 03 Apr Submit your article to this journal Article views: 1050 View Crossmark data Citing articles: 6 View citing articles Full Terms & Conditions of access and use can be found at

2 International Journal of Food Properties, 17: , 2014 Copyright Taylor & Francis Group, LLC ISSN: print / online DOI: / THE EFFECT OF COOKING ON TOTAL POLYPHENOLIC CONTENT AND ANTIOXIDANT ACTIVITY OF SELECTED VEGETABLES Memnune Şengül 1, Hilal Yildiz 2, and Arzu Kavaz 1 1 Department of Food Engineering, Faculty of Agriculture, Ataturk University, Erzurum, Turkey 2 Department of Food Engineering, Faculty of Engineering, Gumushane University, Gumushane, Turkey The aim of this study to investigate the effect of different cooking methods (boiling, steaming, stir-frying, and microwaving) on the total polyphenolic content and total antioxidant activity of selected vegetables (beet, red cabbage, broccoli, white cabbage, black radish, kale, turnip, and red radish) from Turkey. A wide variation on total phenolic content was observed in raw vegetables, ranging from ± 0.47 (beet, Beta vulgaris L. subsp. vulgaris) to ± 5.18 (red radish, Raphanus sativus L.) µg gallic acid equivalent/mg of sample. Considering uncooked vegetables, the order of total antioxidant activity determined by β-carotene bleaching assay was beet > red cabbage > broccoli > white cabbage > black radish > kale > turnip > red radish. In DPPH assay, kale had an exceptionally high antioxidant activity followed by red cabbage, broccoli, turnip, black radish, beet, white cabbage, and red radish. Keywords: Vegetable, Cooking, Antioxidant activity, DPPH, Total phenolic content. INTRODUCTION In recent years, increasing attention has been paid by humans to the role of diet in human health. Epidemiological studies have shown that a high intake of plant-originated foods is strongly associated with a reduced risk of a number of chronic diseases, such as cancer and atherosclerosis, [1] neurodegenerative diseases, including Parkinson s and Alzheimer s diseases as well as inflammation, problems caused by cell, cutaneous aging, [2] cataract, macular degeneration, [3] and diabetes. [4] These beneficial effects have been partly attributed to the compounds present in plants that possess antioxidant activity. Also, antioxidant compounds possess antimutagenic, antibacterial, or antiviral activities to a greater or lesser extent. [4] Antioxidant compounds, which are found in plants (fruits, vegetables, medicinal herbs, etc.), are free radical scavenging molecules, such as phenolic compounds (e.g., phenolic acids, flavonoids, quinones, stilbenes, lignans, coumarins, tannins), nitrogen compounds (alkaloids, amines, betalains), endogenous metabolites, [4] vitamins (C, E), and terpenoids (including carotenoids). [1,4] Received 16 June 2011; accepted 19 August Address correspondence to Memnune Şengül, Department of Food Engineering, Faculty of Agriculture, Ataturk University, Erzurum 25240, Turkey. memnune@atauni.edu.tr 481

3 482 ŞENGÜL, YILDIZ, AND KAVAZ Among horticultural crops, fruits are most commonly consumed raw; however, vegetables are generally cooked by different cooking processes, including boiling in water or microwaving, before being consumed. These processes alter the physical and chemical properties of vegetables. [3,5] Cooking processes may have an affect on the antioxidant content of food due to antioxidant release, destruction, or creation of redoxactive metabolites. [6] Antioxidant compounds, such as ascorbic acid and some carotenoids, are very sensitive to heat and storage. Conversely, polyphenols have shown a certain stability when exposed to high temperatures. [5] Previous studies conducted on different vegetables showed that, after cooking, total polyphenol content and antioxidant activity of samples can be higher or lower compared to fresh vegetables. For example, Faller and Fialho [5] showed that cooking decreased antioxidant capacity for most of the vegetables and small differences found between the cooking methods applied. Wachtel-Galor et al. [6] reported that antioxidant content was lowest in microwaved samples and was followed by boiled and steamed samples and decreased with longer cooking time, regardless of the method in all cooked vegetables. Antioxidant contents increased for all steamed vegetables over that of raw vegetables. Effects were variable for boiling and microwaving. Boiling caused lesser antioxidant loss in cooking than did microwaving. Turkmen et al. [3] reported that after cooking, total antioxidant activity increased or did not change depending on the type of vegetable but not type of cooking. Zhang and Hamauzu [7] pointed out that antioxidant components and antioxidant activity in broccoli samples were lost quickly during cooking. Vegetables used in this study were either eaten uncooked or more commonly were eaten after cooking by steaming, boiling, or microwaving. Cooking methods have major importance on nutritional values of vegetables. Therefore, in this study, we analyzed total polyphenol contents and antioxidant activity of some raw vegetables (beet, turnip, red radish, black radish, kale, white cabbage, red cabbage, and broccoli) and their changes during boiling, steaming, stir-frying, and microwave cooking. MATERIALS AND METHODS Materials Eight commonly grown and consumed vegetables in Eastern Anatolia, i.e., beet (Beta vulgaris L. subsp. vulgaris), turnip (Brassica rapa var. rapa), red radish (Raphanus sativus L.), black radish (Raphanus sativus L.), kale (Brassica oleracea var. acephala), white cabbage (Brassica oleracea var. capitata), red cabbage (Brassica oleracea var. capitata), and broccoli (Brassica oleracea var. italica) were purchased from local supermarkets in Erzurum, Turkey. The healthy vegetables, without damage and insects (approximately 1.5 kg of each), were randomly selected from the market shelves and immediately transported to the laboratory. Chemicals and Reagents β-carotene, Tween 40, BHA (2-tert-butyl-4-methoxyphenol), gallic acid, and Folin Ciocalteu were purchased from a branch of Sigma-Aldrich in Turkey. 2,2-Diphenyl-1- picrylhydrazyl (DPPH ) was obtained from Sigma-Aldrich. Linoleic acid was purchased from Fluka. Ethanol, chloroform, and sodium carbonate were obtained from Riedel-de Haën. All reagents were of analytical grade.

4 THE EFFECT OF COOKING ON SELECTED VEGETABLES 483 Preparation of Vegetable Samples The pre-treatment and cooking procedures were adapted from Turkmen et al. [3] with some modifications. The vegetables were first washed with tap water and followed by washing twice with deionized water. Extraneous matter were removed with a knife or by hand. Vegetables were dried on a paper towel and were cut into almost equal small pieces or slices then mixed well. Then, 1500 g of samples for each vegetable were taken and divided into five portions (300 g for each application): one for analysis as raw, and the others for cooking. Vegetables were cooked by four different methods in triplicate, as given below. Cooking of Vegetables For boiling in water, each vegetable sample (about 100 g weight) was added to 150 ml of boiled water in a stainless steel pan and cooked for 7 min. For steam cooking, the vegetables were placed on a tray in a steam cooker (Tefal) covered with a lid and steamed over boiling water for 7 min under atmospheric pressure. For stir-fry cooking, each vegetable sample (100 g) was placed in heated olive oil (5 g) and stirred for 7 min. Microwave cooking was performed as follows: each vegetable sample (100 g) was placed in a beher glass and 15 ml of distilled water was added. The beher glass was covered with a cooking bag having several holes and cooked. Vegetables were microwaved at 900 MHz in water (vegetable:water, 100:15) for 7 min using an Arçelik microwave oven. The cooked vegetables were then cooled rapidly in a water bath. Preparation of the Extracts Vegetable juices were obtained by using a juicer. The samples of raw and cooked vegetables were squeezed in a juicer (Arzum, Turkey). Ten milliliters of the vegetable juice was mixed with 10 ml of ethanol-water (90:10, v/v) and stirred for 2 h with a magnetic stirrer. The suspension was filtered through Whatman No. l filter paper. Final solutions were used as stock solution for the analysis of total antioxidant activity and total polyphenol compounds and kept at 20 C until analysis. Determination of Total Polyphenol Content Total polyphenol content in the ethanol-water (90:10, v/v) extracts of vegetables was determined by the Folin Ciocalteau colorimetric method [8] with analytical grade gallic acid as standard. Briefly, 1 ml of the solution (contains 1 mg sample) extract in water was pipetted into a flask. Then, 46 ml of distilled water and 1 ml of Folin Ciocalteu s reagent were added and mixed thoroughly. The mixture was left to stand for 3 min and 3.0 ml of 2% sodium carbonate were added. After 120 min of incubation at ambient temperature with shaking, the resulting absorbance was measured at 760 nm using a visible spectrophotometer (T60V, PG Instruments Ltd.). Measurements were carried out in triplicate, the calibration curve was performed with gallic acid, and the results were expressed as μg of gallic acid equivalents per milligram of sample (μg GAE/mg of sample). Total Antioxidant Activity Total antioxidant activity in the ethanol-water (90:10, v/v) extracts of vegetables was determined according to the β-carotene bleaching method described by Kaur and Kapoor [9]

5 484 ŞENGÜL, YILDIZ, AND KAVAZ with some modifications. Briefly, 4 ml of β-carotene solution (0.1 mg in 1 ml chloroform), 40 mg of linoleic acid, and 400 mg of Tween 40 were transferred to a round-bottom flask. The mixture was evaporated at 50 C by means of a rotary evaporator to remove chloroform. Then, 100 ml of oxygenated distilled water were added slowly to the residue and vigorously agitated to give a stable emulsion. Next, 800 μl of the extract were added to 3 ml aliquots of β-carotene/linoleic acid emulsion. As soon as the emulsion was added to each tube, the zero time absorbance was measured at 470 nm using a visible spectrophotometer (T60V, PG Instruments Ltd). The mixtures were incubated at 50 C for 100 min. The measurement was carried out at 10-min intervals for 100 min. Ethanol was used as control. A blank, devoid of β-carotene, was prepared for background subtraction. Butylated hydroxyanisole (BHA) and butylated hydroxytoluene (BHT) were used as a standard. All samples were assayed in triplicate. Degradation rate (DR) was calculated according to first-order kinetics, using the following equation based on: ln(a/b) l/t = DR sample or Dr standart, where ln is natural log, a is the initial absorbance (470 nm) at time 0, b is the absorbance (470 nm) at 100 min, and t is the time. Antioxidant activity (AA) was expressed as percent of inhibition relative to the control, using the following formula: AA = (DR control DR sample or DR standart /DR control ) 100. DPPH Radical Scavenging Assay Effect of extract on DPPH free radical was measured based on Gulein. [10] Briefly, 0.1 mm solution of DPPH was prepared in ethanol and 0.5 ml of this solution was added to 1.5 ml of vegetable extract solution in ethanol at different concentrations ( μg/ml). These solutions were vortexed thoroughly and incubated in the dark for 30 min. The absorbance was measured at 517 nm against blank samples lacking scavenger. A standard curve was prepared using different concentrations of DPPH. The DPPH scavenging capacity was expressed as mm in the reaction medium and was calculated from the calibration curve determined by linear regression: DPPH scavenging effect (%) = [1 (A s /A c )] 100, where A c is the absorbance at 517 nm of the control reaction (containing DPPH solution without vegetable extract), and A s is the absorbance of the test sample. IC 50 value (μg/ml) is the concentration of sample required to scavenge 50% DPPH free radical and was calculated from a calibration curve by a linear regression. Statistical Analysis Analysis of variance was performed by ANOVA procedures (SPSS 13.0 for Windows). [11] Significant differences between means were determined by Duncan s multiple range tests.

6 THE EFFECT OF COOKING ON SELECTED VEGETABLES 485 RESULTS AND DISCUSSION Total Polyphenol Content Table 1 indicates the concentrations of total polyphenols of the raw and cooked vegetables. We found a significant difference (P < 0.001) in the total polyphenol content among the eight vegetables in their raw and cooked state. Total polyphenol content ranged from to μg GAE/mg in raw vegetables and are listed in descending order: red cabbage > beet > black radish > kale > broccoli > white cabbage > turnip > red radish. Sikora et al. [12] reported mg/100 g total polyphenols in fresh kale. Higher total polyphenol content was found in red cabbage and beet ranging from and μg GAE/mg of sample. Medium total polyphenol content level was found in broccoli, kale, and black radish, ranging from to μg GAE/mg of sample. Similarly, a previous study showed that total polyphenol content of kale was higher than broccoli. [12] We found lower total polyphenol content in μg GAE/mg of sample in red radish (44.94), turnip (63.60), and white cabbage (86.93) (Table 1). Phenolic compounds are natural antioxidants present in plant foods and they have an important effect on human health. [13] These compounds reduce diseases, such as cancer, arteriosclerosis, brain disorders, and heart diseases. [14] We also examined the effects of cooking by boiling, steaming, microwave cooking, and stir-fry cooking on the total polyphenol content of the vegetables. The concentrations of total polyphenol contents of the cooked vegetables are shown in Table 1 with comparison of raw vegetables. Cooking style affected total polyphenol content of samples. All cooking processes had significantly effected (P < 0.01) total polyphenol content on all tested vegetables. All vegetables except kale and white cabbage lost their polyphenols after boiling. Among them red radish lost the highest percentage of total polyphenolic content (53.39%), followed by beet (43.51%), black radish (40.72%), turnip (27.77%), red cabbage (5.90%), and broccoli (4.09%) after blanching in boiling water. The results indicated that polyphenolic compounds were very sensitive to heat treatment. Conversely, blanching in boiling water increased total polyphenolic contents of kale (64.65%) and white cabbage (8.44%) (Table 1). Wen et al. [15] reported that the blanching process showed different effects on different vegetables and some vegetables increased their polyphenolic content while others decreased. Sahlin et al. [16] showed that boiling and baking had a small effect on the ascorbic acid, total polyphenolic, lycopene, and antioxidant activity of the tomatoes, while frying significantly reduced the ascorbic, total phenolic, and lycopene contents of the tomatoes. Steaming increased total polyphenolic content in red radish (5.21%), kale (129.42%), broccoli (54.64%), and white cabbage (23.08%). On the contrary, steaming decreased total polyphenolic contents in beet (15.01%), turnip (35.64%), black radish (4.87%), and red cabbage (15.29%). Steaming is a popular cooking method, especially in Asian countries. [17] Total polyphenolic compound loss was as high as 43.51% in the boiled beet compared with 15.01% when it is steamed. The loss of total polyphenolic content from black radish was greater when the vegetable was boiling in water (40.72%) than in steaming (4.87%) (Table 1). Stir-frying increased total polyphenolic contents of vegetables, with the exception of red cabbage, which decreased (13.01%). Microwave cooking showed different effects on vegetables. Microwaving increased total polyphenolic content of beet (17.97%), red radish (8.17%), and kale (8.17%), while it decreased turnip (22.25%), black radish (26.48%), red cabbage (48.92%), broccoli (34.21%), and white cabbage (65.56%) (Table 1). As is well known, many vegetables are cooked by a simple boiling process or microwave process

7 Table 1 Total phenolic contents (μg GAE/mg of sample) of raw and cooked vegetables. Vegetables Cooking methods Beet Turnip Red radish Black radish Kale Red cabbage Broccoli White cabbage Raw ± 0.00b ± 2.36b ± 0.47b ± 2.35ab ± 2.83d ± 5.18a ± 3.30c ± 1.41c Boiled ± 5.66d ± 1.89c ± 0.47c ± 0.94b ± 36.77c ± 59.87a ± 6.60cd ± 8.01c Steamed ± 3.30c ± 7.07c ± 7.54b ± 16.03ab ± 5.18a ± 11.31a ± 2.36b ± 2.43b Stir-fried ± 0.94a ± 6.60a ± 2.83a ± 28.28a ± 1.41d ± 3.77a ± 3.77a ± 0.94a Microwaved ± 6.60a ± 1.20c ± 0.00ab ± 47.61bc ± 18.85b ± 1.89b ± 3.77e ± 0.94d Different lowercase letters within the same column indicate significant differences ( P < 0.01) among the different percentages of vegetables. Results are means (SD) of triplicate samples, each tested in triplicate. 486

8 THE EFFECT OF COOKING ON SELECTED VEGETABLES 487 before use. These cooking processes caused a number of changes in physical characteristics and chemical composition of vegetables. [7] Faller and Fialho [5] showed that cooking led to negative results for most vegetables analyzed; however, some differences were observed among vegetables. Studies performed on different vegetables after cooking showed that the total polyphenol content and antioxidant capacity could be either higher or lower in comparison to fresh food. [5] Ismailetal. [18] showed that thermal treatment decreased the total polyphenolic content of vegetables, such as spinach, kale, swamp cabbage, and cabbage. The degree of polyphenols degradation depends very much on the processing time and the size of the vegetables. [12] Total Antioxidant Activity Oxidative stress is now recognized as a major factor associated with the development of chronic diseases, including cancer and cardiovascular disease. This has led to the hypothesis that the beneficial effects of fruits and vegetables could be largely explained by their high content of antioxidants. Antioxidant activity is involved in cancer prevention at the initiation stage, while antiproliferative activity is targeting cancer cells at the promotion and progression stages. [16] The total antioxidant activity, which reflected the ability of the vegetable extracts to inhibit the bleaching of β-carotene, was measured and compared with that of the control, which contained no antioxidant component. The comparison of mean total antioxidant activity of eight raw and cooked vegetables is presented in Table 2. The high absorbance values indicated that vegetable extracts possessed antioxidant activity. Among uncooked vegetables, the antioxidant capacity ranking in descending order is beet > red cabbage > broccoli > white cabbage > black radish > kale > turnip > red radish, with β-carotene bleaching assay values of 97.70, 95.40, 93.70, 91.62, 86.80, 82.80, 81.00, and 30.00%, respectively. Data in this study showed that fresh vegetables were good sources of antioxidant compounds. The β-carotene bleaching rates of the raw and cooked vegetable extracts are shown in Table 2. There was a decrease in absorbance values of β-carotene in the absence of vegetable extracts due to the oxidation of β-carotene and linoleic acid. In our study, boiling led to an increase in antioxidant activity of red radish, black radish, and kale. This effect is perhaps due to production of redox-active secondary plant metabolites or breakdown products, but is highly likely to be related to release of antioxidants from intracellular proteins, changes in plant cell wall structure, matrix modifications, and more efficient release of antioxidants during homogenization. [6] Conversely, boiling reduced the antioxidant activity of beet, turnip, red cabbage, white cabbage, and broccoli. Microwave cooking of beet, black radish, red cabbage, broccoli, and white cabbage resulted in a significant reduction (P < 0.01) of antioxidant activity when compared to the respective raw state. Stir-frying increased antioxidant activity of red radish, broccoli, and white cabbage. Wachtel-Galor et al. [6] showed that the effects of cooking on antioxidant capacity of different vegetables may be different. Cooking procedures reduced significantly (P < 0.05) antioxidant activity of beet and red cabbage, and reductions were nearly the same in all cooking methods. Conversely, considerable increase in antioxidant activity of red radish was also observed in cooking by all methods. Antioxidant activity of turnip, black radish, kale, broccoli, and white cabbage was significantly (P < 0.05) varied to various extents, depending on the type of cooking method. Ismail et al. [18] found that antioxidant activity of kale, spinach, and swamp cabbage

9 Table 2 Total antioxidant activity (%) of raw and cooked vegetables. Vegetables Cooking methods Beet Turnip Red radish Black radish Kale Red cabbage Broccoli White cabbage Raw ± 0.42a ± 1.41bc ± 2.83c ± 1.41ab ± 3.96b ± 0.57a ± 0.14a ± 2.58b Boiled ± 0.35c ± 0.88c ± 1.77a ± 0.18a ± 3.36ab ± 0.00b ± 2.83bc ± 1.41c Steamed ± 1.24c ± 1.94ab ± 7.07a ± 5.30a ± 1.77c ± 0.14c ± 0.28b ± 2.83d Stir-fried ± 0.35b ± 3.68abc ± 7.07b ± 1.91b ± 0.18b ± 0.58b ± 0.23a ± 0.57a Microwaved ± 2.12b ± 7.57a ± 3.54a ± 3.36ab ± 1.94a ± 0.00d ± 4.24c ± 1.41d Different lowercase letters within the same column indicate significant differences ( P < 0.01) among the different percentages of vegetables. Results are means (SD) of triplicate samples, each tested in triplicate. Table 3 IC50 values (μg/ml) of raw and cooked vegetables. Vegetables Cooking methods Beet Turnip Red radish Black radish Kale Red cabbage Broccoli White cabbage Raw ± 1.47b ± 0.11e ± 1.38e ± 1.12d ± 0.76e ± 0.16a ± 1.47a ± 1.23a Boiled ± 1.51c ± 0.98a ± 1.73a ± 0.82a ± 1.85a ± 0.88c ± 1.04e ± 0.71c Steamed ± 1.48e ± 0.47d ± 1.46d ± 2.91b ± 0.77d ± 0.43d ± 0.18d ± 1.03e Stir-fried ± 1.32a ± 0.33c ± 2.17c ± 0.76c ± 1.68b ± 1.00b ± 0.71b ± 0.71d Microwaved ± 1.05d ± 1.23b ± 1.03b 0.00 ± 0.00e ± 1.47c ± 1.53d ± 1.56c ± 1.11b Different lowercase letters within the same column indicate significant differences ( P < 0.01) among the different percentages of vegetables. Results are means (SD) of triplicate samples, each tested in triplicate. 488

10 THE EFFECT OF COOKING ON SELECTED VEGETABLES 489 was reduced significantly (P < 0.05), but cabbage and shallots in this study did not show any significant difference in antioxidant activity after 1 min of thermal treatment. Free Radical-Scavenging Activity Free radical scavenging activity for DPPH radical was expressed as IC 50 in samples. There is an inverse relationship between IC 50 and antioxidant activity in all samples. Results of the IC 50 values of the eight vegetables for the uncooked and four cooking methods after 7 min of cooking are presented in Table 3. All the samples showed antioxidant activity in the order of kale > red cabbage > broccoli > turnip > black radish > beet > white cabbage > red radish. After cooking procedures, IC 50 values of turnip, red radish, black radish, and kale significantly (P < 0.05) increased, namely, antioxidant capacity reduced. Conversely, total antioxidant activity of broccoli, white cabbage, and red cabbage significantly (P < 0.05) increased during cooking procedures compared to the values for the raw ones. The earlier study showed that total antioxidant capacity of pepper, green beans, broccoli, and spinach increased during cooking procedures compared to the values for fresh vegetables. [3] Previous studies have shown that the radical scavenging capacity of vegetables decreased after cooking independently of the procedure. In the literature, cooked broccoli and potatoes, however, resulted in a higher scavenging capacity than the raw samples. [5] CONCLUSION Higher intakes of fruits and vegetables have been associated with a reduced risk of cardiovascular disease, cancer, and ischemic stroke. In this study, various cooking procedures affected the total polyphenolic content and the antioxidant activities in vegetables. It shows that all cooking processes had more variable effects on total polyphenol content and antioxidant properties. Generally, the total polyphenolic content and the antioxidant activities in cooked vegetables were lower than those of raw samples. REFERENCES 1. Podsędek, A. Natural antioxidants and antioxidant capacity of Brassica vegetables: A review. LWT Food Science and Technology 2007, 40, Dasgupta, N.; De, B. Antioxidant activity of some leafy vegetables of India: Comparative study. Food Chemistry 2007, 101, Turkmen, N.; Sari, F.; Velioglu, Y.S. The effect of cooking methods on total phenolics and antioxidant activity of selected green vegetables. Food Chemistry 2005, 93, Cai, Y.; Luo, Q.; Sun, M.; Corke, H. Antioxidant activity and phenolic compounds of 112 traditional Chinese medicinal plants associated with anticancer. Life Sciences 2004, 74, Faller, A.L.K.; Fialho, E. The antioxidant capacity and polyphenol content of organic and conventional retail vegetables after domestic cooking. Food Research International 2009, 42, Wachtel-Galor, S.; Wong, K.W.; Benzie I.F.F. The effect of cooking on Brassica vegetables. Food Chemistry 2008, 110, Zhang, D.; Hamauzu, Y. Phenolics, ascorbic acid, carotenoids and antioxidant activity of broccoli and their changes during conventional and microwave cooking. Food Chemistry 2004, 88,

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