Effect of Superatmospheric Oxygen on Anthocyanins, Phenolics and Antioxidant Activity of Blueberries and Strawberries

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1 Effect of Superatmospheric Oxygen on Anthocyanins, Phenolics and Antioxidant Activity of Blueberries and Strawberries Y. Zheng C.Y. Wang Nanjing Agricultural University Produce Quality and Safety Laboratory Nanjing USDA-ARS, Beltsville, MD 275 China USA S.Y. Wang Fruit Laboratory USDA-ARS, Beltsville, MD 275 USA W. Zheng Zhejiang University Zhejiang China Keywords: high oxygen storage, blueberry, strawberry, antioxidant activity, anthocyanin, phenolic Abstract The effects of superatmospheric oxygen levels on anthocyanins, phenolics, antioxidant activity and fruit quality of blueberries (Vaccinium corymbosum L.) and strawberries (Fragaria ananassa Duch.) during storage at 5 C were investigated. High oxygen treatment increased the levels of total anthocyanins, total phenolics as well as several individual flavonoid compounds during the first 21 days of storage for blueberries and first 7 days of storage for strawberries. Antioxidant activity, measured as oxygen radical absorbance capacity or ORAC, also increased in these fruits during the same period after exposure of the fruit to superatmospheric oxygen concentrations. However, these effects diminished with prolonged storage duration. No significant differences in total anthocyanins, total phenolics, ORAC values or individual flavonoid compounds were observed between high oxygen and air-treated fruit during the later part of storage. Little differences were also found in titratable acidity, total soluble solids or surface color among the fruits treated with various concentrations of oxygen throughout the storage period. These results suggest that high oxygen treatments may improve the antioxidant activities of blueberry and strawberry fruits during the initial stage of storage. INTRODUCTION Antioxidants are compounds that are capable of performing a number of functions including acting as free radical scavengers, peroxide decomposers, singlet and triplet oxygen quenchers, enzyme inhibitors, and synergists (Larson, 1988). Antioxidants can also delay or inhibit the oxidation of lipids or other molecules by inhibiting the initiation or propagation of oxidizing chain reaction (Velioglu et al., 1998). Fruits contain a great variety of phytonutrients and are good sources of antioxidants (Block et al., 1992; Ness and Powles, 1977). The phytonutrients in fruits responsible for antioxidant activity can largely be attributed to phenolic compounds such as anthocyanins, carotenoids, and other flavonoid compounds. These compounds may act independently or in combination as anticancer or cardio-protective agents through various mechanisms. Berry fruits have high content of anthocyanins and phenolics. These compounds protect plants against damaging photodynamic reactions by quenching the excited state of active oxygen species (Larson, 1988; Lewis, 1993). Anthocyanins have received attention as important dietary constituents that provide health benefits and contribute antioxidant capacity beyond that provided by essential micronutrients such as ascorbate and tocopherols. The increased interest in healthy diet and the development of functional foods are stimulating the need for more information concerning the bioavailability and efficacy of phenolics and anthocyanins. Changes in the content of phenolics and anthocyanins and the antioxidant activity in fruits during postharvest period have received much attention during recent years. Proc. IX th Intl. Contr. Atmos. Res. Conf. Ed.: R.M. Beaudry Acta Hort. 857, ISHS

2 Increasing the carbon dioxide concentration in the storage atmosphere inhibits the postharvest increase of anthocyanin in strawberries (Gil et al., 1997; Holcroft and Kader, 1999). The total antioxidant activity increased overall by about 45% in cranberry fruits stored in air, but this increase was prevented by storage in 3% CO 2 plus 21% O 2 (Gunes et al., 22). Mareczek et al. (2) reported that the level of total phenolics in the peel of Golden Reinders and Gala Must apples were similar in fruit stored for 7 months at o C in air and in CA (3% O 2 +5% CO 2 ), but phenolics were reduced after an additional 8 days at 16 C in the peel of Gala Must fruit previously stored in air. On the other hand, Mazza and Miniati (1993) observed that anthocyanins in apples were relatively stable when stored at 2 C in air, but decreased in low O 2 and high CO 2. High O 2 treatment has recently been demonstrated as an alternative to traditional low O 2 and high CO 2 controlled atmosphere technique to maintain quality and safety of fresh produce (Day, 1996). The elevated O 2 atmospheres have been proven to be particularly effective in inhibiting microbial growth and enzymatic discoloration and preventing anaerobic fermentation reactions (Amanatidou et al., 23; Day, 1996; Jacxsens et al., 23; Wszelaki and Mitcham, 2). However, little information is available concerning the effect of superatmospheric oxygen on antioxidant system in fruits and vegetables during storage. This study was undertaken to determine the changes of phenolics, anthocyanins and antioxidant capacity in blueberries and strawberries in response to high oxygen exposures. MATERIALS AND METHODS Chemicals Kaempferol, (R)-phycoerythrin (R-PE) and quercetin were purchased from Sigma Chemical Co. (St. Louis, MO). 2, 2 -Azobis (2-amidinopropane) dihydrochloride (AAPH) was obtained from Wako Chemicals USA Inc. (Richmond VA). Trolox (6- hydroxy-2,5,7,8-tetramethylchroman-2-carboxylic acid) was purchased from Aldrich (Milwaukee, WI). Acetonitrile, methanol, acetone, and water were of HPLC grade and were purchased from Baxter (Muskegon, MI). All anthocyanins and their aglycons were obtained from Indofine Chemical Co., Inc. (Somerville, NJ). Other authentic standards were obtained from Sigma and Fisher Scientific (Pittsburgh, PA). Plant Materials and Treatments Blueberries (Vaccinium corymbosum L. cv. Duke) and strawberries (Fragaria ananassa Duch. cv. Allstar) were hand-harvested at commercially mature stage from Butler s orchard, MD and sorted to eliminate damaged and unripe fruit and selected for uniform size and color. Three kilograms of samples were placed in each 18 L jar and three jars were used for each treatment. The jars were placed at 5 C and connected to continuous flow (12 ml/min) of humidified air (control), 4, 6, 8 or 1% O 2 (balanced with N 2 in all high O 2 treatments). The gases were checked regularly with an O 2 /CO 2 analyzer (AMETEK, Pittsburgh, PA) and maintained at ±2% for the duration of the experiment. Samples were taken initially and during storage for decay evaluation and other analysis. Fruit Decay Fruit decay was visually evaluated during the course of the experiment. Any berries with visible mold growth were considered decayed. Fruit decay was expressed as percentage of fruit showing decay symptoms. Sample Preparation for Various Assays Ten berries from each replicate were cut into small slices and mixed. Batches of 5- g samples were stored at -8 C until analyzed. To prepare the fruit extracts, three 5-g samples of berries from each replicate were extracted twice with 15 ml of 8% acetone containing.2% formic acid using a Polytron (Brinkmann Instruments, Inc., Westbury, 476

3 NY) for 1 min and then centrifuged at 2,g for 2 min. The supernatants were combined and transferred to vials, stored at -8 C, and then used for analysis of total phenolics, total anthocyanins, and ORAC. Total Phenolics and Anthocyanins Analysis Total phenolic contents in strawberry extracts were determined according to the Folin-Ciocalteu procedure (Slinkard and Singleton, 1977). Results are expressed as milligrams of gallic acid equivalent (GAE) per 1 g of fresh weight. Total anthocyanin contents of strawberry extracts were measured using the ph differential method (Cheng and Breen, 1991). Results are expressed as milligrams of pelargonidin 3-glucoside (P 3- G) equivalents per 1 g of fresh weight. ORAC (Oxygen Radical Absorbance Capacity) Assay The procedures for the ORAC assay on strawberries were modified from the previously described method of Cao et al. (1993). This assay measures the effect of antioxidant components in strawberry extracts to inhibit the decline of R-PE fluorescence induced by a peroxyl radical generator, AAPH. The reaction mixture contained 1.7 ml of 75 mm phosphate buffer (ph 7.), 1 µl of R-PE (3.4 mg/l), 1 µl of 32 mm AAPH, and 1 µl of sample. Phosphate buffer was used as a blank and 1 µm Trolox (a watersoluble α-tocopherol analogue) was used as a standard during each run. The final volume was 2 ml and this reaction mixture was placed in a 1-mm-wide fluorometer cuvette. R- PE, phosphate buffer, and samples were preincubated at 37 C for 15 min. The reaction was started by the addition of AAPH. Fluorescence was measured and recorded every 5 min at the emission of 57 nm and excitation of 54 mm using a Shimadzu RF-Mini 15 recording fluorometer (Columbia, MD) until the fluorescence of the last reading declined to <5% of the first reading (~7 min). One blank, one standard, and a maximum of 1 samples were analyzed at the same time. Each sample was repeated three times. The ORAC value refers to the net protection area under the quenching curve of R-PE in the presence of an antioxidant. The final results (ORAC values) were calculated and expressed using Trolox equivalents (TE) per gram on a fresh weight basis. HPLC Analysis of Individual Anthocyanin and Phenolic Compounds The extraction and purification procedures and the high performance liquid chromatography (HPLC) conditions for the analysis of individual anthocyanin and phenolic compounds in berry fruits were described previously (Wang and Zheng, 21). RESULTS AND DISCUSSION Blueberries stored under air started to show decay on day 14 during storage at 5 o C. Treatment with 4% O 2 had little effect on blueberry decay. However, atmospheres enriched with 6% O 2 or higher were effective in inhibiting decay during storage, and improved decay control was obtained with increased O 2 concentration (Fig. 1). It is possible that atmospheres containing high oxygen are toxic to decay microorganisms. The inhibition of decay could be due to the unfavorable effects of high oxygen on the oxidation-reduction potential in the microbial system. The accumulation of injurious reactive oxygen species and the oxidation of certain enzymes especially those having sulfhydryl groups may be detrimental to the survival of microorganisms (Fridovitch, 1975). Total phenolic content and ORAC values in fruit treated with 6% O 2 were higher than those in air-stored fruit (Fig. 1). Chlorogenic acid was the major phenolic compound in blueberries. Its level fluctuated during storage and was not consistently affected by high O 2 treatments. No significant differences in chlorogenic acid were observed among all the treatments (Fig. 2). Quercetin-3-galactoside in blueberry fruit was enhanced by high oxygen treatments, particularly by 8% O 2 (Fig. 2). The effect of high O 2 treatments on main individual anthocyanins in blueberries is shown in Figure 3. In general, O 2 levels higher than 6% increased these anthocyanins. Oxygen concentrations higher than 6% also reduced decay and promoted the increases of total phenolics, total 477

4 anthocyanins, ORAC, pelargonidin-3-glucoside, and pelagonidin-3-glucoside-succinate in strawberry fruit during the first 7 days of storage at 5 C (Fig. 4). In conclusion, the results of these experiments indicate that blueberry and strawberry fruits treated with high O 2 levels generally had less decay and higher ORAC, total phenolic, and total anthocyanin contents as well as individual phenolic compounds than air-stored fruits during the initial stage of storage. ACKNOWLEDGEMENTS The authors would like to thank Hilarine Repace, David Spaulding, and Sue Kim for their technical assistance. The financial support of National Natural Science Foundation of China (NSFC, No ) to Dr. Y. Zheng is gratefully acknowledged. Literature Cited Amanatidou, A., Slump, R.A. and Smid, E.J. 23. Microbial interactions on minimally processed carrots under elevated oxygen and carbon dioxide concentrations. Acta Hort. 6: Block, G., Patterson, B. and Suber, A Fruits, vegetables and cancer prevention: A review of the epidemiological evidence. Nutr. Cancer. 18:1 9. Cao, G., Alessio, H.M. and Culter, R.G Oxygen-radical absorbance capacity assay for antioxidants. Free Radical Biol. Med. 14: Cheng, G.W. and Breen, P.J Activity of phenylalanine ammonia-lyase (PAL) and concentrations of anthocyanins and phenolics in developing strawberry fruit. J. Am. Soc. Hortic. Sci. 116: Day, B High oxygen modified atmosphere packaging for fresh prepared produce. Postharvest News and Info. 7: Fridovitch, I Superoxide dismutase. Ann. Rev. Biochem. 44: Gil, M.I., Holcroft, D.M. and Kader, A.A Changes in strawberry anthocyanins and other polyphenols in response to carbon dioxide treatments. J. Agri. Food Chem. 45: Gunes, G., Liu, R.H. and Watkins, C.B. 22. Controlled-atmosphere effects on postharvest quality and antioxidant activity of cranberry fruits. J. Agri. Food Chem. 5: Holcroft, D.M. and Kader, A.A Carbon dioxide-induced changes in color and anthocyanin synthesis of stored strawberry fruit. HortScience, 24: Jacxsens, L., Devlieghere, F., Van der Steen, C., Siro, I. and Debevere, J. 23. Application of ethylene absorbers in combination with high oxygen atmospheres for the storage of strawberries and raspberries. Acta Hort. 6: Larson, R.A The antioxidants of higher plants, Phytochemistry 27:969. Lewis, N.G Plant phenolics. p In: R.G. Alscher and J.L. Hess (eds.), Antioxidants in Higher Plants. CRC Press, Boca Raton, FL. Mareczek, A., Leja, M. and Ben, J. 2. Total phenolics, anthocyanins and antioxidant activity in the peel of the stored apples. J. Fruit Ornamental Plant Res. 8(2): Mazza, G. and Miniati, E Anthocyanins in Fruits, Vegetables and Grains. CRC Press, Boca Raton, FL. Ness, A.R. and Powles, J.W Fruits and vegetables, and cardiovascular disease: A review. Int. J. Epidemiol. 26:1 13. Slinkard, K. and Singleton, V.L Total phenol analysis: Automation and comparison with manual methods. Am. J. Enol. Vitic. 28: Velioglu, Y.S., Mazza, G., Gao, L. and Oomah, B.D Antioxidant activity and total phenolics in selected fruits, vegetables, and grain products. J. Agri. Food Chem. 46: Wang, S. and Zheng, W. 21. Effect of plant growth temperature on antioxidant capacity in strawberry. J. Agri. Food Chem. 49: Wszelaki, A.L. and Mitcham, E.J. 2. Effects of superatmospheric oxygen on strawberry fruit quality and decay. Postharvest Biol. Technol. 2:

5 Figures 1 A 25 B Decay (%) ORAC (μmol of TE g -1 ) Initial Air 4% 6% 8% 1% Initial Air 4% 6% 8% 1% Total Phenolics (mg 1g -1 ) C Initial Air 4% 6% 8% 1% Total Anthocyanin (mg 1g -1 ) D Initial Air 4% 6% 8% 1% Fig. 1. Blueberry fruit decay (A), total phenolics (C), total anthocyanin (D), and oxygen radical absorbance capacity (ORAC) (B) before and after storage at 5 o C in air or high-o 2 atmospheres for 21 days. Chlorogenic Acid (μg g -1 ) A Initial Air 4% 6% 8% 1% Quercetin 3-Galactoside ( μg g -1 ) B Initial Air 4% 6% 8% 1% Fig. 2. Chlorogenic acid (A) and quercetin 3-galactoside (B) in blueberry fruit before and after storage at 5 o C in air or high-o 2 atmospheres for 21 days. 479

6 Delphinidi-3-galactoside ( μg g -1 ) A Initial Air 4% 6% 8% 1% Cyanidin-3-glucoside (μg g -1 ) B Initial Air 4% 6% 8% 1% Petunidin-3-galactoside ( μg g -1 ) C Initial Air 4% 6% 8% 1% Petunidin-3-arabinoside ( μg g -1 ) D Initial Air 4% 6% 8% 1% Malvidin-3-galactoside ( μg g -1 ) E Initial Air 4% 6% 8% 1% Malvidin-3-arabinoside ( μg g -1 ) F Initial Air 4% 6% 8% 1% Fig. 3. Main individual anthocyanins in blueberry fruit before and after storage at 5 C in air or high-o 2 atmospheres for 21 days. 48

7 25 A 14 B Decay (%) Total Phenolics (mg 1g -1 ) Initial Air 6% 1% Initial Air 6% 1% Total Anthocyanin (mg 1g -1 ) C ORAC (μmol of TE g -1 ) D Initial Air 6% 1% Initial Air 6% 1% Pelargonidin-3-glucoside ( μg g -1 ) E Initial Air 6% 1% Pelargonidin-3-glucosidesuccinate (μg g -1 ) F Initial Air 6% 1% Fig. 4. Strawberry fruit decay (A), total phenolics (B), total anthocyanin (C), oxygen radical absorbance capacity (ORAC) (D), pelargonidin-3-glucoside (E), and pelargonidin-3-glucoside-succinate (F) before and after storage at 5 C in air or high-o 2 atmospheres for 7 days. 481

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