Effect of high voltage atmospheric cold plasma on

Research Article Received: 6 December 2016

Revised: 3 February 2017

Accepted article published: 13 February 2017

Published online in Wiley Online Library: 8 March 2017

(wileyonlinelibrary.com) DOI 10.1002/jsfa.8268

Effect of high voltage atmospheric cold plasma on white grape juice quality Shashi Kishor Pankaj, Zifan Wan, William Colonna and Kevin M Keener* Abstract BACKGROUND: This study focuses on the effects of novel, non-thermal high voltage atmospheric cold plasma (HVACP) processing on the quality of grape juice. A quality-based comparison of cold plasma treatment with thermal pasteurization treatment of white grape juice was done. RESULTS: HVACP treatment of grape juice at 80 kV for 4 min resulted in a 7.4 log10 CFU mL−1 reduction in Saccharomyces cerevisiae without any significant (P > 0.05) change in pH, acidity and electrical conductivity of the juice. An increase in non-enzymatic browning was observed, but total color difference was very low and within acceptable limits. Spectrophotometric measurements showed a decrease in total phenolics, total flavonoids, DPPH free radical scavenging and antioxidant capacity, but they were found to be comparable to those resulting from thermal pasteurization. An increase in total flavonols was observed after HVACP treatments. CONCLUSION: HVACP treatment of white grape juice at 80 kV for 2 min was found to be comparable to thermal pasteurization in all analyzed quality attributes. HVACP has shown the potential to be used as an alternative to thermal treatment of white grape juice. © 2017 Society of Chemical Industry Keywords: grape juice; HVACP; cold plasma; juice quality

INTRODUCTION

4016

Fruit juices have become an integral part of human diet owing to the health benefits offered by them and the growing consumer awareness about health issues. Citrus juices are the most popular fruit juices, accounting for more than 50% of international commerce in juices.1 Grape juice has demonstrated various positive health benefits such as improvement of endothelial function, increase of serum antioxidant capacity, protection of low-density lipoproteins against oxidation, decrease of native plasma protein oxidation and reduction of platelet aggregation.2 Glucose, fructose and the organic acids tartaric and malic are the main soluble solids in grape juice.3 The juice contains no sucrose and very small amounts of protein, with arginine, proline and glutamine as major free amino acids.4 Grape juice is usually preserved through thermal pasteurization and addition of chemical preservatives, which can result in undesirable effects on product quality.5 Traditionally, grape juices were thermally pasteurized, although several non-thermal technologies have shown potential for use as suitable alternatives. Non-thermal technologies have the potential to take over from conventional heat treatment, at least partially, depending on the nature of the food product.6 Non-thermal technologies such as high pressure processing,7,8 pulsed electric field,9 – 11 dense phase carbon dioxide processing5,12 and ultrasound13,14 have been explored with grape juices. High voltage atmospheric cold plasma (HVACP) is a novel, non-thermal technology which has recently caught a lot of attention for its application in the food industry. HVACP has shown considerable potential for microbial decontamination,15,16 enzyme J Sci Food Agric 2017; 97: 4016–4021

inactivation,17 pesticide degradation,15 enhanced seed vigor18,19 and surface modification.20 – 23 Cold plasma effects on orange,24 pomegranate,25,26 chokeberry27 and apple28 juices have been studied previously. However, no studies exist showing the effect of HVACP on the quality of white grape juice, which forms the focus of this work. The objective of the present study was to analyze the effect of HVACP treatment on grape juice quality in comparison with thermally pasteurized juice.

MATERIALS AND METHODS Chemicals Ascorbic acid, sodium hydroxide (NaOH), ethanol, methanol, aluminum chloride (AlCl3 ), sodium carbonate (Na2 CO3 ), sodium acetate, sodium nitrite (NaNO2 ), ammonium molybdate and sulfuric acid (H2 SO4 ) were purchased from Thermo Scientific (Waltham, MA, USA). Quercetin hydrate and gallic acid were obtained from Acros Organics (Fair Lawn, NJ, USA). Catechin hydrate was procured from TCI (Tokyo, Japan). 2,2-Diphenyl-1-picrylhydrazyl (DPPH) was obtained from Alfa Aesar (Ward Hill, MA, USA). Folin–Ciocalteu reagent was bought from Spectrum Chemical Mfg. Corp. (Gardena, CA, USA). All chemicals and reagents used in the study were of analytical reagent (AR) grade.

∗

Correspondence to: KM Keener, Center for Crop Utilization Research, Iowa State University, Ames, IA 50011, USA. E-mail: [email protected] Center for Crop Utilization Research, Iowa State University, Ames, IA, USA

www.soci.org

© 2017 Society of Chemical Industry

Effect of HVACP on white grape juice quality

www.soci.org

Figure 1. Schematic diagram of grape juice HVACP treatments.

Yeast strain Ethanol Red yeast (Saccharomyces cerevisiae) (Le Saffre, Milwaukee, WI, USA) was used throughout this investigation. The organism was maintained at 4 ∘ C on Sabouraud (SAB) dextrose agar slants. In preparation for experiments, yeasts were cultivated in Bacto SAB broth with 20 g L−1 glucose. Cells were grown overnight in a (New Brunswick Scientific., Enfield, CT, USA) G76 gyrotory water bath at 30 ∘ C and 180 rpm in 250 mL Erlenmeyer flasks containing 50 mL of broth. Cells were aseptically transferred to sterile 50 mL centrifuge tubes and harvested by centrifugation at 12 000 × g for 8 min at 4 ∘ C in a Sorvall Legend XTR refrigerated centrifuge equipped with a FIBERLite® F15-8 × 50C (Thermo Fischer Scientific, Waltham, MA, USA). The supernatant was discarded. The yeast cells were washed by resuspension in sterile deionized water and then harvested again as above. The cells were then diluted with sterile grape juice to give an initial concentration of 7.3 log10 colony-forming units (CFU) mL−1 . Prior to use, the juice was thawed and filter sterilized under vacuum through a Stericup with a 0.22 μm PES membrane (EMD Millipore Corp., Billerica, MA, USA). Grape juice preparation Fresh seedless grapes (Vitis vinifera cv. Thompson seedless) were purchased from a local market (Hyvee, Ames, IA, USA) to produce fresh juice. The grapes were split from bunches, and homogeneous berries were screened manually for any visible defects before being crushed using a domestic juice extractor (Model 67608Z, Hamilton Beach, Ontario, Canada). The juice was centrifuged (7277 × g, 10 min) and filtered to remove coarse particles and impurities. The juice obtained was immediately frozen at −18 ∘ C. Frozen samples were processed within 2 weeks.

J Sci Food Agric 2017; 97: 4016–4021

Optical emission spectroscopy The spectra of HVACP treatments were recorded using a computer-controlled Ocean Optics spectrometer (Ocean Optics, Inc., Winter Park, FL, USA). The light from the plasma was delivered by an Ocean Optics optical fiber. The fiber had a core diameter of 1000 μm and was suitable for measuring UV–visible light within the wavelength range 200–1100 nm. Ocean Optics collimating lenses of 5 mm diameter optimized for light within the wavelength range 200–2000 nm were used to parallelize the light entering the optical fiber. The length from the collimating lenses to the edge of the sample was 15 cm. The emission spectrum of the HVACP treatment at 80 kV for 4 min was collected and saved. Yeast inactivation assay After the HVACP treatments, samples were stored for 24 h under refrigerated conditions. The bags were subsequently opened and the cells were transferred from the plates to sterile tubes. The cells were then serially diluted with sterile deionized water, plated on SAB agar with 40 g L−1 glucose and incubated at 30 ∘ C. After 40–48 h, the plates were counted and the resulting CFU data were used to determine yeast inactivation. Data represent the average values of CFU determine in triplicate. Determination of pH, acidity and electrical conductivity pH of grape juice was determined in triplicate using a digital pH meter (Orion Dual Star, Thermo Scientific). The pH meter was calibrated before use with commercial buffer solutions of pH 4.0 and 7.0. Titratable acidity (TA) of grape juice was analyzed in triplicate using end-point titration. A 10 mL juice sample was placed in a 250 mL beaker, and 90 mL of distilled water was added. This solution was then titrated against standardized 0.1 mol L−1 NaOH to the phenolphthalein end-point (pH 8.2 ± 0.1). The volume of NaOH was converted to g citric acid per 100 mL juice, and TA was calculated using the equation TA (%) = (V × 0.1 × 0.067 × 100) ∕m where V is the titer volume of NaOH (mL) and m is the volume of grape juice (mL).


wileyonlinelibrary.com/jsfa

4017

Plasma treatment Grape juice samples were placed in petri plates (15 cm diameter) and packed in Ziploc bags (S.C. Johnson & Son, Inc., Racine, WI, USA). The Ziploc bags were flushed with dry air for 3 min before being heat sealed. Samples were placed in the processing chamber, which consisted of two circular aluminum plate electrodes (outer diameter 158 mm) (Fig. 1). Plexiglass (10 mm) and polypropylene (2 mm) sheets were used as dielectric barriers to avoid any arc transition and ensure homogeneity of the plasma treatment. The voltage applied to the electrode was given by a step-up transformer (Phenix Technologies, Inc., Accident, MD, USA) with an input of 230 V, 60 Hz from the mains supply. The applied voltage was controlled using a variac. The atmospheric air condition at the time of treatment was 46% relative humidity and 24 ∘ C. The grape juice samples were treated at 80 kV (peak-to-peak) for 1, 2, 3 and 4 min. Control samples were also packed in the same manner but were not treated. All treatments were done in duplicate.

Thermal pasteurization Grape juice was thermally pasteurized at 85 ∘ C for 43 s.29 The juice sample was placed in a water bath maintained at 95 ∘ C. After about 7 min, the sample reached 85 ± 1 ∘ C. It was held at this temperature for 43 s, then cooled rapidly in ice to room temperature (25 ± 1 ∘ C). After the thermal pasteurization procedure, samples were stored and analyzed in duplicate in the same way as for plasma-treated samples.

www.soci.org

SK Pankaj et al.

Figure 2. Optical emission spectrum of HVACP treatment of grape juice at 80 kV for 4 min.

Electrical conductivity of grape juice was measured using a conductivity meter (Eutech Instruments PCSTestr 35, Thermo Scientific). Determination of color and non-enzymatic browning The color of grape juice samples was assessed based on the L*, a*, b* color coordinate system using a Hunter MiniScan colorimeter (Hunter Associates Laboratory, Inc., Reston, VA, USA) at room temperature. Color values L* (whiteness/darkness), a* (redness/greenness) and b* (yellowness/blueness) were measured. Hue angle (h), chroma (C*) and total color difference (TCD) were also calculated using the equations

Figure 3. Saccharomyces cerevisiae inactivation by HVACP treatment at 80 kV.

h = tan−1 (b∗ ∕a∗ ) )1∕2 ( C ∗= a∗2 + b∗2 [ ]1∕2 TCD = (ΔL∗ )2 + (Δa∗ )2 + (Δb∗ )2 Non-enzymatic browning was assessed by first centrifuging the grape juice at 12 500 × g for 10 min. The supernatant was collected and filtered through a 0.45 μm filter. The browning index was determined by measuring the absorbance at 420 nm using a spectrophotometer at room temperature.

4018

Determination of total phenolic, flavonoid and flavonol contents Total phenolic content of grape juice was determined by the method proposed by Slinkard and Singleton30 with minor modifications. Briefly, 1 mL of Folin–Ciocalteu reagent was mixed well with 0.5 mL of juice sample and left for 6 min. Then 2 mL of 200 g L−1 Na2 CO3 solution was added and the mixture was left for 60 min at 30 ∘ C. The phenols were measured at 760 nm using a


UV–visible spectrophotometer (Genesys 10S, Thermo Scientific). A calibration curve was prepared using standard solutions of gallic acid, and the results for total phenols were expressed as μg gallic acid equivalent (GAE) mL−1 sample. Total flavonoid content of grape juice was determined using the method described by Kim et al.31 with slight modification. Briefly, 0.25 mL of juice sample was mixed with 1.25 mL of deionized water and then 75 𝜇L of 50 g L−1 NaNO2 solution was added. After 6 min, 150 𝜇L of 100 g L−1 AlCl3 solution was added, followed by, after a further 5 min, 0.5 mL of 1 mol L−1 NaOH. The final volume was made up to 2.5 mL with distilled water and mixed well. The absorbance at 415 nm was measured using a spectrophotometer. A calibration curve was prepared using standard solutions of catechin hydrate, and the results for total flavonoids were expressed as μg (+)-catechin equivalent (CE) mL−1 sample. Total flavonol content of grape juice was analyzed by the method of Kumaran and Karunakaran.32 Briefly, 2 mL of juice sample was mixed with 2 mL of 20 g L−1 AlCl3 solution, then 3 mL of 50 g L−1 sodium acetate solution was added. The mixture was kept at 20 ∘ C for 150 min. The absorbance at 440 nm was measured using a spectrophotometer. A calibration curve was prepared using standard


J Sci Food Agric 2017; 97: 4016–4021


www.soci.org

solutions of quercetin hydrate, and the results for total flavonols were expressed as μg quercetin (QE) equivalent mL−1 sample. Determination of DPPH free radical scavenging activity DPPH free radical scavenging activity of grape juice was determined using the method of Yi et al.33 with minor modifications. A 2 mL juice sample was mixed with 2 mL of DPPH solution (0.2 mmol L−1 in ethanol) and incubated at room temperature in the dark for 30 min. The same procedure was conducted for a blank using ethanol instead of juice sample. The decrease in absorbance at 517 nm was measured using a spectrophotometer. DPPH radical scavenging activity was calculated using the equation [( ) ] DPPH radical scavenging activity (%) = A0 − A1 ∕A0 × 100 where A0 is the absorbance of the blank and A1 is the absorbance of the juice sample. Determination of antioxidant capacity Antioxidant capacity of grape juice was determined by the method described by Prieto et al.34 Briefly, 0.4 mL of juice sample was mixed with 4 mL of reagent solution containing 28 mmol L−1 sodium phosphate, 4 mmol L−1 ammonium molybdate and 0.6 mol L−1 H2 SO4 . The mixture was then incubated in a water bath at 95 ∘ C for 90 min. A blank solution was also prepared in which methanol was used instead of juice sample. After cooling to room temperature, the absorbance of the mixtures was measured at 695 nm using a spectrophotometer. A suitable calibration curve was prepared using standard solutions of ascorbic acid, and results for antioxidant activity were expressed as μg ascorbic acid equivalent (AAE) mL−1 sample. Statistical analysis Data obtained are presented as mean value ± standard deviation. Analysis of variance was done for all treatments, and the significance of differences between treatments was assessed using Tukey’s multiple sample comparison tests. Significance levels were tested at P ≤ 0.05. All analyses were carried out using SPSS (SPSS Inc., Chicago, IL, USA) and Minitab (Minitab Inc., State College, PA, USA) software.

Table 1. pH, acidity and electrical conductivity of grape juice after HVACP treatment Sample Control 80 kV/1 min 80 kV/2 min 80 kV/3 min 80 kV/4 min Thermal

pH 3.38 ± 0.01a 3.38 ± 0.01a 3.37 ± 0.05a 3.35 ± 0.04a 3.30 ± 0.12a 3.44 ± 0.23a

TA (%) 0.62 ± 0.01a 0.55 ± 0.01b 0.56 ± 0.01b 0.56 ± 0.01b 0.54 ± 0.01b 0.53 ± 0.01b

EC (mS cm−1 ) 3.46 ± 0.01a 3.44 ± 0.03a 3.45 ± −.09a 3.34 ± 0.11a 3.01 ± 0.04b 3.41 ± 0.01a

Yeast inactivation Kloeckera apiculata, Candida stellata, S. cerevisiae and Brettanomyces intermedius are among the most common spoilage yeasts in grape juice and wine.5 Saccharomyces cerevisiae was used as the target organism in this study to confirm the effectiveness of the HVACP treatments.9 The effect of HVACP treatment time on S. cerevisiae inactivation is shown in Fig. 3. The yeast inactivation was observed to be in a linear relationship with the treatment time, with 7.4 log10 CFU mL−1 inactivation of S. cerevisiae being achieved after HVACP treatment at 80 kV for 4 min. The yeast inactivation could be attributed to the damaging effects of reactive gas species generated by HVACP and identified earlier from the emission spectrum. These reactive gas species result in cell leakage by electroporation, lipid peroxidation, enzyme inactivation and DNA cleavage leading to cell death.41 Effect on pH, acidity and electrical conductivity The effects of HVACP on the pH, acidity (TA) and electrical conductivity (EC) of white grape juice are shown in Table 1. The pH of untreated grape juice was 3.38, and no significant difference (P > 0.05) was observed after either HVACP treatment or thermal pasteurization. A significant decrease (P < 0.05) in TA was observed after HVACP treatment of the grape juice. This decrease in acidity could be due to the solubilization of hydroxyl radicals generated during the plasma discharge. The solubilization of reactive gas species generated during the plasma discharge could also explain the increase in EC observed after HVACP treatment at 80 kV for 4 min.

RESULTS AND DISCUSSION

J Sci Food Agric 2017; 97: 4016–4021

Effect on color and non-enzymatic browning The effects of HVACP on the color and non-enzymatic browning of grape juice are shown in Table 2. No significant differences in L* value but increases in a* and b* values were observed after plasma treatment. This suggests that the juice color was shifted toward red and yellow by plasma treatment. The chroma (C*) value signifies vividness or color saturation. An increase in C* means that the color gets closer to the pure hue, becoming more vivid. The increased C* values in plasma-treated samples mean that the treatment resulted in a more vivid instrumental color. Similar increases in C* after cold plasma treatments were also observed by Almeida et al.24 The hue angle (h) corresponds to the characteristic color of the sample. The maximum decrease in h after HVACP treatments was less than 2∘ , which is very low and insignificant (P > 0.05). The color changes were found to be in good agreement with the non-enzymatic browning data, which also showed similar increases after HVACP treatments. In citrus fruit juices mostly, the degradation of ascorbic acid may cause non-enzymatic browning.13 These results suggest that HVACP treatments increase



4019

Optical emission spectroscopy The plasma discharge was characterized by optical emission spectroscopy for identification of reactive species. The optical emission spectrum of the plasma discharge during HVACP treatment of grape juice at 80 kV for 4 min is shown in Fig. 2. High intensity peaks were observed in the wavelength range 310–430 nm which represent mostly excited nitrogen species, including nitrogen second positive system N2 (C-B) and first negative system N2 + (B-X). This air plasma emission spectrum was similar and comparable to emission spectra of other studies at atmospheric pressure.15,21,35 The OH (hydroxyl) peak was also observed around 300 nm along with the reactive nitrogen species. Furthermore, at 725 and 777 nm, two excited atomic oxygen species O(5s3 S → 3p3 P) and O(2s2 2p3 3p5 P → 2s2 2p3 3s5 S) respectively were found. The low intensity of the excited atomic oxygen species is most likely due to the quenching effect of excited atomic oxygen in air plasma.36 This spectrum shows that HVACP can be a source to generate both reactive nitrogen species and reactive oxygen species, which have been proven to have antimicrobial properties.37 – 40

www.soci.org

SK Pankaj et al.

Table 2. Color values and non-enzymatic browning of HVACP-treated grape juice

Sample Control 80 kV/1 min 80 kV/2 min 80 kV/3 min 80 kV/4 min Thermal

L* 19.04 ± 0.79a 19.53 ± 0.98a 19.62 ± 0.22a 19.24 ± 0.05a 19.04 ± 0.06a 20.65 ± 0.01a

a* 0.57 ± 0.23a 0.92 ± 0.06ab 1.03 ± 0.11ab 1.13 ± 0.00b 1.31 ± 0.06b 0.90 ± 0.11a,b

b* 4.84 ± 0.02a 7.05 ± 0.28b 7.98 ± 0.11c 9.01 ± 0.01d 8.64 ± 0.26c,d 5.22 ± 0.38a

Table 3. Total phenolic, flavonoid and flavonol contents of HVACP-treated grape juice

Sample

Total phenolics (μg GAE mL−1 )

Total flavonoids (μg CE mL−1 )

Total flavonols (μg QE mL−1 )

265.21 ± 0.29a 250.63 ± 1.47b 236.25 ± 1.18c 222.08 ± 1.18d 211.46 ± 1.47e 231.04 ± 2.65c

20.71 ± 1.52a 25.00 ± 0.51b 27.86 ± 1.01b 31.79 ± 0.51c 33.21 ± 0.51c 21.25 ± 0.25a

Chroma 4.87 ± 0.05a 7.10 ± 0.27b 8.05 ± 0.13c 9.08 ± 0.01d 8.73 ± 0.25 cd 5.29 ± 0.35a

83.35 ± 2.70a 82.59 ± 0.80a 82.69 ± 0.65a 82.85 ± 0.01a 81.40 ± 0.67a 80.15 ± 1.90a

720.62 ± 0.34a 568.72 ± 1.34b 555.21 ± 7.71b 444.08 ± 14.75c 445.02 ± 10.72c 483.41 ± 4.69d

juice browning depending on the treatment time. Although it is worth mentioning at this time that HVACP treatment induced some color changes in the juice samples, they were not perceptible with the naked eye, as expected from the low TCD values. Effect on total phenolic, flavonoid and flavonol contents Phenolic compounds, flavonoids and flavonols are very beneficial for human health owing to their antioxidant properties and their role in reducing the risk of cardiovascular diseases and cancer.42 The effects of HVACP and thermal pasteurization on grape juice are summarized in Table 3. Increasing the time of HVACP treatment resulted in a significant (P < 0.05) reduction in the total phenolic and flavonoid contents of grape juice. HVACP treatments with air generate many reactive oxygen species and ozone in the discharge. Phenolic compounds are particularly known to be susceptible to ozone attack through the degradation of aromatic rings in their structure.43,44 Similar degradation of phenolic compounds after cold plasma treatments was also reported in lettuce45 and orange juice.24 However, it was interesting to note that HVACP treatment significantly increased the total flavonols in grape juice in a time-dependent manner. This might suggest some incorporation of hydroxyl groups in the aromatic rings of phenolic compounds.13 However, more detailed studies are required for further explanation and understanding of the interaction mechanism between plasma reactive species and phenolic compounds. Thermal pasteurization also resulted in a decrease in total phenolics and flavonoids, with no change in flavonol content. HVACP treatment at 80 kV for 3 min was in close agreement with thermal pasteurization in terms of phenolic and flavonoid contents.

4020

Effect on DPPH free radical scavenging activity and antioxidant capacity Phenolic compounds and ascorbic acid are the major components of fruit juices responsible for DPPH free radical scavenging and


– 2.38 ± 0.45ab 3.23 ± 0.16 ac 4.22 ± 0.02d 3.87 ± 0.24 cd 1.71 ± 0.07b

Non-enzymatic browning 0.09 ± 0.00a 0.13 ± 0.00b 0.17 ± 0.01c 0.21 ± 0.01d 0.23 ± 0.01d 0.10 ± 0.00a

Table 4. DPPH free radical scavenging activity and total antioxidant capacity of HVACP-treated grape juice

Sample Control 80 kV/1 min 80 kV/2 min 80 kV/3 min 80 kV/4 min Thermal

Total color difference

Hue

Control 80 kV/1 min 80 kV/2 min 80 kV/3 min 80 kV/4 min Thermal

DPPH free radical scavenging activity (%) 88.16 ± 0.93a 87.63 ± 1.68a 82.74 ± 0.52b 79.21 ± 1.05bc 77.50 ± 0.22c 82.24 ± 0.92b

Total antioxidant capacity (μg AAE mL−1 ) 679.35 ± 3.38a 665.22 ± 2.46b 643.91 ± 0.61c 618.48 ± 1.54d 602.83 ± 2.15e 637.61 ± 2.15c

antioxidant capacity. These compounds have the potential to scavenge free radicals that cause damage to the body and also reduce the risk of many diseases originating from oxidative stress.13 The DPPH free radical scavenging activity and total antioxidant capacity of plasma-treated grape juice are shown in Table 4. A decrease in both DPPH free radical scavenging and antioxidant capacity was observed with increasing time of HVACP treatment. This could be attributed to the decrease in total phenols observed earlier after HVACP treatments. Thermal pasteurization also resulted in a decrease in DPPH free radical scavenging and total antioxidant capacity. Thermal treatment values were found to be comparable to those of HVACP treatment at 80 kV for 2 min (or longer).

CONCLUSION The effects of HVACP on the quality of grape juice were investigated in this work. HVACP treatment at 80 kV for 4 min resulted in a 7.4 log10 CFU mL−1 reduction in S. cerevisiae. No significant (P > 0.05) change in pH was observed after plasma treatment. A decrease in acidity and electrical conductivity was observed. Slight browning of the juice was noticed, but total color difference was very low. A decrease in total phenolics, total flavonoids, DPPH free radical scavenging and antioxidant capacity was also observed, but they were found to be comparable to those resulting from thermal pasteurization. HVACP treatment at 80 kV for 2 min (or longer) was found to be comparable to thermal pasteurization in terms of quality parameters. This study demonstrates the potential of HVACP to be used as an alternative to the traditional thermal pasteurization processing of white grape juice.

ACKNOWLEDGEMENTS The authors would like to thank the undergraduate students Wenrui Wu, Evan McCoy and Minyi Xu for their help during the experiments.


J Sci Food Agric 2017; 97: 4016–4021


www.soci.org

REFERENCES

J Sci Food Agric 2017; 97: 4016–4021

24 Almeida FDL, Cavalcante RS, Cullen PJ, Frias JM, Bourke P, Fernandes FAN et al., Effects of atmospheric cold plasma and ozone on prebiotic orange juice. Innovat Food Sci Emerg Technol 32:127–135 (2015). 25 Kovaˇcević DB, Putnik P, Dragović-Uzelac V, Pedisić S, Jambrak AR and Herceg Z, Effects of cold atmospheric gas phase plasma on anthocyanins and color in pomegranate juice. Food Chem 190:317–323 (2016). 26 Herceg Z, Kovaˇcević DB, Kljusurić JG, Jambrak AR, Zorić Z and Dragović-Uzelac V, Gas phase plasma impact on phenolic compounds in pomegranate juice. Food Chem 190:665–672 (2016). 27 Kovaˇcević DB, Kljusurić JG, Putnik P, Vukušić T, Herceg Z and Dragović-Uzelac V, Stability of polyphenols in chokeberry juice treated with gas phase plasma. Food Chem 212:323–331 (2016). 28 Surowsky B, Fröhling A, Gottschalk N, Schlüter O and Knorr D, Impact of cold plasma on Citrobacter freundii in apple juice: inactivation kinetics and mechanisms. Int J Food Microbiol 174:63–71 (2014). 29 Sandhu KS and Minhas KS, Oranges and citrus juices, in Handbook of Fruits and Fruit Processing, ed. by Hui YH. Blackwell, Oxford, pp. 309–357 (2006). 30 Slinkard K and Singleton VL, Total phenol analysis: automation and comparison with manual methods. Am J Enol Vitic 28:49–55 (1977). 31 Kim D-O, Jeong SW and Lee CY, Antioxidant capacity of phenolic phytochemicals from various cultivars of plums. Food Chem 81:321–326 (2003). 32 Kumaran A and Karunakaran RJ, In vitro antioxidant activities of methanol extracts of five Phyllanthus species from India. LWT – Food Sci Technol 40:344–352 (2007). 33 Yi Z, Yu Y, Liang Y and Zeng B, In vitro antioxidant and antimicrobial activities of the extract of Pericarpium Citri Reticulatae of a new Citrus cultivar and its main flavonoids. LWT – Food Sci Technol 41:597–603 (2008). 34 Prieto P, Pineda M and Aguilar M, Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: specific application to the determination of vitamin E. Anal Biochem 269:337–341 (1999). 35 Sarangapani C, Misra NN, Milosavljević V, Bourke P, O’Regan F and Cullen PJ, Pesticide degradation in water using atmospheric air cold plasma. J Water Process Eng 9:225–232 (2016). 36 Walsh JL, Liu DX, Iza F, Rong MZ and Kong MG, Contrasting characteristics of sub-microsecond pulsed atmospheric air and atmospheric pressure helium–oxygen glow discharges. J Phys D Appl Phys 43:032001 (2010). 37 Duday D, Clément F, Lecoq E, Penny C, Audinot J-N, Belmonte T et al., Study of reactive oxygen or/and nitrogen species binding processes on E. coli bacteria with mass spectrometry isotopic nanoimaging. Plasma Processes Polym 10:864–879 (2013). 38 Komine C and Tsujimoto Y, A small amount of singlet oxygen generated via excited methylene blue by photodynamic therapy induces the sterilization of Enterococcus faecalis. J Endodontics 39:411–414 (2013). 39 Pellieux C, Dewilde A, Pierlot C and Aubry J-M, Bactericidal and virucidal activities of singlet oxygen generated by thermolysis of naphthalene endoperoxides. Meth Enzymol 319:197–207 (2000). 40 Tatsuzawa H, Maruyama T, Misawa N, Fujimori K, Hori K, Sano Y et al., Inactivation of bacterial respiratory chain enzymes by singlet oxygen. FEBS Lett 439:329–333 (1998). 41 Han L, Patil S, Boehm D, Milosavljević V, Cullen PJ and Bourke P, Mechanisms of inactivation by high-voltage atmospheric cold plasma differ for Escherichia coli and Staphylococcus aureus. Appl Environ Microbiol 82:450–458 (2016). 42 Hertog MGL, Hollman PCH and Katan MB, Content of potentially anticarcinogenic flavonoids of 28 vegetables and 9 fruits commonly consumed in the Netherlands. J Agric Food Chem 40:2379–2383 (1992). 43 Stalter D, Magdeburg A, Wagner M and Oehlmann J, Ozonation and activated carbon treatment of sewage effluents: removal of endocrine activity and cytotoxicity. Water Res 45:1015–1024 (2011). 44 Pérez M, Torrades F, Domènech X and Peral J, Treatment of bleaching Kraft mill effluents and polychlorinated phenolic compounds with ozonation. J Chem Technol Biotechnol 77:891–897 (2002). 45 Grzegorzewski F, Ehlbeck J, Schlüter O, Kroh LW and Rohn S, Treating lamb’s lettuce with a cold plasma – influence of atmospheric pressure Ar plasma immanent species on the phenolic profile of Valerianella locusta. LWT – Food Sci Technol 44:2285–2289 (2011).


4021

1 Igual M, Contreras C, Camacho MM and Martínez-Navarrete N, Effect of thermal treatment and storage conditions on the physical and sensory properties of grapefruit juice. Food Bioprocess Technol 7:191–203 (2014). 2 Dávalos A, Bartolomé B and Gómez-Cordovés C, Antioxidant properties of commercial grape juices and vinegars. Food Chem 93:325–330 (2005). 3 Buglione M and Lozano J, Nonenzymatic browning and chemical changes during grape juice storage. J Food Sci 67:1538–1543 (2002). ˘ s F and Eren S, Nonenzymic browning reactions 4 Bozkurt H, Gögü¸ in boiled grape juice and its models during storage. Food Chem 64:89–93 (1999). 5 Gunes G, Blum LK and Hotchkiss JH, Inactivation of yeasts in grape juice using a continuous dense phase carbon dioxide processing system. J Sci Food Agric 85:2362–2368 (2005). 6 Misra NN, Kadam SU and Pankaj SK, An overview of nonthermal technologies in food processing. Indian Food Ind 30(5/6):45–52 (2011). 7 Del Pozo-Insfran D, Del Follo-Martinez A, Talcott ST and Brenes CH, Stability of copigmented anthocyanins and ascorbic acid in muscadine grape juice processed by high hydrostatic pressure. J Food Sci 72:S247–S253 (2007). 8 Daoudi L, Quevedo JM, Trujillo AJ, Capdevila F, Bartra E, Mínguez S et al., Effects of high-pressure treatment on the sensory quality of white grape juice. High Press Res 22:705–709 (2002). 9 Garde-Cerdán T, Arias-Gil M, Marsellés-Fontanet AR, Ancín-Azpilicueta C and Martín-Belloso O, Effects of thermal and non-thermal processing treatments on fatty acids and free amino acids of grape juice. Food Control 18:473–479 (2007). 10 Marsellés-Fontanet ÁR and Martín-Belloso O, Optimization and validation of PEF processing conditions to inactivate oxidative enzymes of grape juice. J Food Eng 83:452–462 (2007). 11 Marsellés-Fontanet ÀR, Puig A, Olmos P, Mínguez-Sanz S and Martín-Belloso O, Optimising the inactivation of grape juice spoilage organisms by pulse electric fields. Int J Food Microbiol 130:159–165 (2009). 12 Del Pozo-Insfran D, Balaban MO and Talcott ST, Microbial stability, phytochemical retention, and organoleptic attributes of dense phase CO2 processed muscadine grape juice. J Agric Food Chem 54:5468–5473 (2006). 13 Aadil RM, Zeng X-A, Han Z and Sun D-W, Effects of ultrasound treatments on quality of grapefruit juice. Food Chem 141:3201–3206 (2013). 14 Tiwari BK, Patras A, Brunton N, Cullen PJ and O’Donnell CP, Effect of ultrasound processing on anthocyanins and color of red grape juice. Ultrason Sonochem 17:598–604 (2010). 15 Misra NN, Pankaj SK, Walsh T, O’Regan F, Bourke P and Cullen PJ, In-package nonthermal plasma degradation of pesticides on fresh produce. J Hazard Mater 271:33–40 (2014). 16 Niemira BA, Cold plasma decontamination of foods. Annu Rev Food Sci Technol 3:125–142 (2012). 17 Misra NN, Pankaj SK, Segat A and Ishikawa K, Cold plasma interactions with enzymes in foods and model systems. Trends Food Sci Technol 55:39–47 (2016). 18 Li L, Jiang J, Li J, Shen M, He X, Shao H et al., Effects of cold plasma treatment on seed germination and seedling growth of soybean. Sci Rep 4:5859 (2014). 19 Mitra A, Li Y-F, Klämpfl TG, Shimizu T, Jeon J, Morfill GE et al., Inactivation of surface-borne microorganisms and increased germination of seed specimen by cold atmospheric plasma. Food Bioprocess Technol 7:645–653 (2014). 20 Pankaj SK, Bueno-Ferrer C, Misra NN, Milosavljević V, O’Donnell CP, Bourke P et al., Applications of cold plasma technology in food packaging. Trends Food Sci Technol 35:5–17 (2014). 21 Pankaj SK, Bueno-Ferrer C, Misra NN, O’Neill L, Jiménez A, Bourke P et al., Surface, thermal and antimicrobial release properties of plasma-treated zein films. J Renew Mater 2:77–84 (2014). 22 Pankaj SK, Bueno-Ferrer C, Misra NN, O’Neill L, Tiwari BK, Bourke P et al., Physicochemical characterization of plasma-treated sodium caseinate film. Food Res Int 66:438–444 (2014). 23 Pankaj SK, Bueno-Ferrer C, Misra NN, Bourke P and Cullen PJ, Zein film: effects of dielectric barrier discharge atmospheric cold plasma. J Appl Polym Sci 131:40803 (2014).
