Dielectric barrier atmospheric cold plasma applied on camu-camu juice processing: Effect of the excitation frequency

Food Research International 131 (2020) 109044

Contents lists available at ScienceDirect

Food Research International journal homepage: www.elsevier.com/locate/foodres

Dielectric barrier atmospheric cold plasma applied on camu-camu juice processing: Effect of the excitation frequency

T

Debora Raquel Gomes de Castroa,b, Josiana Moreira Marc, Laiane Santos da Silvac, Kalil Araújo da Silvac, Edgar Aparecido Sanchesc, Jaqueline de Araújo Bezerrad, Sueli Rodriguese, ⁎ Fabiano A.N. Fernandesf, Pedro Henrique Campeloa,b, a

Grupo de Inovação em Biotecnologia e Alimentos da Amazônia (gIBA), Federal University of Amazonas, Manaus, Amazonas, Brazil Faculty of Agrarian Science, Federal University of Amazonas, Brazil c Laboratory of Nanostructured Polymers (NANOPOL), Federal University of Amazonas, Manaus, Amazonas, Brazil d Federal Institute of Education, Science and Technology of Amazonas, Manaus, Amazonas, Brazil e Department of Food Engineering, Federal University of Ceará, Fortaleza, Ceará, Brazil f Department of Chemical Engineering, Federal University of Ceará, Fortaleza, Ceará, Brazil b

A R T I C LE I N FO

A B S T R A C T

Keywords: Myrciaria dubia Radiofrequency cold plasma Emerging technologies Ascorbic acid Anthocyanins Bioavailability

The aim of this paper was to evaluate the effect of cold plasma excitation frequency on camu-camu juice processing. Different levels of frequency (200, 420, 583, 698 and 960 Hz) were applied on camu-camu juice to measure the contents of ascorbic acid and anthocyanins, as well as to evaluate the antioxidant compounds (DPPH, ABTS, FRAP and phenolic compounds), peroxidase and polyphenol oxidase enzymatic activity and color. Furthermore, the juice bioaccessibility was evaluated after simulated digestion. The ascorbic acid concentration was increased when higher excitation frequencies were employed, increasing their bioavailability. Anthocyanins, peroxidase and polyphenol oxidase presented considerable degradation with increasing the plasma excitation frequency. For this reason, the juice processing proposed herein represents an alternative to enhance its nutritional quality. Moreover, the use of cold plasma reduced the activity concentration of endogenous enzymes, presenting considerable degradation for higher excitation frequency.

1. Introduction Camu-camu (Myrciaria dubia, Myrtaceae) is a popular fruit from Amazon region. Studies have reported its high concentration of ascorbic acid (2–4 g per 100 g of fruit), besides several bioactive compounds such as anthocyanins, carotenoids, tannins, and vitamins (CunhaSantos, Viganó, Neves, Martínez, & Godoy, 2019; Neri-Numa, Soriano Sancho, Pereira, & Pastore, 2018). Food industry has been interested in replacing some conventional food processing techniques due to the sensory and nutritional losses in foods as a result of heat exposure or addition of preservative substances. Emerging technologies-based food processing have been employed to improve productivity by increasing the durability of foods without affecting their nutritional contents, organoleptic properties or specifications (Li, Chen, Zhang, & Fu, 2017; Moreira, Alexandre, Pintado, & Saraiva, 2019; Oliveira et al., 2018). Plasma is known as the fourth state of the highly energized matter, which is constituted of excited atoms and molecules, ionized gases, free

⁎

radicals and electrons (Suhem, Matan, Nisoa, & Matan, 2013). Most reactive species generated by commonly used plasma sources include electronically excited oxygen and nitrogen, reactive nitrogen species (RNS), as well as reactive oxygen species (ROS) (Scholtz, Pazlarova, Souskova, Khun, & Julak, 2015). In liquid foods, plasma has contact with each volume element. Electron dissociation reactions as well as interaction with organic molecules are observed as a result of the plasma contact with water molecules (Locke & Shih, 2011). For this reason, microorganisms, enzymes as well as bioactive compounds can be inactivated, modifying the nutritional quality of fruit juices (Paixão, Fonteles, Oliveira, Fernandes, & Rodrigues, 2019; Rodríguez, Gomes, Rodrigues, & Fernandes, 2017). Therefore, understanding the effect of processing parameters on liquid foods has become important for improving their nutritional quality. The excitation frequency represents an important parameter in cold plasma technology because it is related to the excitation behavior of electrons and ions from plasma. The excitation frequency is directly related to the type and amount of the plasmas’s reactive species

Corresponding author at: Grupo de Inovação em Biotecnologia e Alimentos da Amazônia (gIBA), Federal University of Amazonas, Manaus, Amazonas, Brazil. E-mail address: [email protected] (P.H. Campelo).

https://doi.org/10.1016/j.foodres.2020.109044 Received 16 September 2019; Received in revised form 14 January 2020; Accepted 27 January 2020 Available online 29 January 2020 0963-9969/ © 2020 Elsevier Ltd. All rights reserved.

Food Research International 131 (2020) 109044

D.R.G. de Castro, et al.

power (FRAP) (Azevedo et al., 2018).

(Noriega, Shama, Laca, Díaz, & Kong, 2011). The excitation frequencies are classified as low (< 13.56 MHz) and high frequency (> 300 MHz), in which the plasma is constituted of radiofrequency and microwave, respectively (Wertheimer & Moisan, 1985). Radiofrequency generated plasma has been widely used to improve seed germination (Wertheimer & Moisan, 1985). However, only one report has been found, to the best of our knowledge, on the influence of excitation frequency of cold plasma applied on the decontamination of Listeria innocua in meat and chicken (Noriega et al., 2011). Some other reports focused on different process parameters such as plasma voltage (Chen et al., 2019), atmosphere (Misra et al., 2014), processing time (Dong & Yang, 2019) or plasma flow rate (Fernandes, Santos, & Rodrigues, 2019; Paixão et al., 2019). The effect of cold plasma excitation frequency on fruit juice processing represents a research area of both potential scientific and technological interest. Therefore, the effect of cold plasma excitation frequency on the physicochemical properties of camu-camu juices was evaluated. Different levels of frequency (200, 420, 583, 698 and 960 Hz) were applied in order to measure the contents of ascorbic acid and anthocyanins, as well as to evaluate the antioxidant compounds (2,2-diphenyl-1-picrylhydrazyl/DPPH, 2,2′-azino-bis (3-ethylbenzothiazoline-6-sulfonicacid)/ABTS, Ferric ion reducing antioxidant power/FRAP and phenolic compounds), peroxidase and polyphenol oxidase enzymatic activity and color. Furthermore, the juice bioaccessibility was evaluated after simulated digestion.

2.5. Total phenolic content Total phenolic content analysis (TPC) was carried out based on the spectroscopic technique (Oliveira et al., 2018). Briefly, 100 μL of the appropriate diluted extract was mixed with 1 mL phenol reagent, 1 mL of sodium bicarbonate solution (10% m/w) and 4 mL distilled water. The mixture was allowed to stand for 2 h in the dark. The total phenolic concentration was calculated from a calibration curve by plotting known solutions of gallic acid against absorbance at 760 nm. All results were expressed as gallic acid equivalent per 100 mL−1 of camu-camu juice. 2.6. Monomeric anthocyanin content Monomeric anthocyanin content was measured by UV–vis spectroscopy using the pH-differential method (Mercali, Gurak, Schmitz, & Marczak, 2015). Juices were centrifuged at 5 °C (10 min, 3000 × g) and the supernatant was diluted in potassium chloride buffer (pH 1.0) or in sodium acetate buffer (pH 4.5) at room temperature for 20 min. The absorbance was calculated following the Eq. (1) and the concentration of monomeric anthocyanins was expressed as cyanidin-3glucoside (majority of camu-camu juice, Zanatta, Cuevas, Bobbio, Winterhalter, and Mercadante (2005)) according to Eq. (2).

Abs = (A520 − A700 )pH 1 − (A520 − A700 )pH 4.5

2. Material and methods

Abs × MW × DF × 100 ε×l

(1)

2.1. Materials

MAC =

Fruit pulp was purchased in Manaus, Brazil, which was obtained using a crashing pulp machine without water addition. Juices (pulp/ water, 1:1 w/w) were processed in an industrial blender for 5 min and maintained in polyethylene terephthalate flasks at −18 °C until further analysis.

where A520 and A700 are the absorbance at 520 and 700 nm, respectively; MW is the molar weight (g mol−1); DF is the dilution factor; ε is the molar absorptivity (26,900 L mol−1 cm−1) and l is path length of the cuvette (cm).

(2)

2.7. Enzymes (Peroxidase and polyphenol oxidase) 2.2. Cold plasma treatments Peroxidase (POD) and polyphenol oxidase (PPO) activities were measured using an UV–vis spectrophotometer at 470 nm and 395 nm, respectively (Paixão et al., 2019; Souza Comapa et al., 2019). The residual enzymatic activity (Eq. (3)) after juice processing was calculated as the percentual ratio of the processed samples to the activity of the untreated juice.

A volume of 40 mL of juice was added in a glass Petri dish and subjected for 15 min to the cold plasma in an equipment Inergiae, model Pulse, using 24 kV at different frequency levels (200, 420, 583, 698 or 960 Hz). The aluminum electrodes (8 cm diameter) were isolated from the samples by a distance of 15 mm using acrylic plates. After processing, the juices were placed in polypropylene tubes and stored at −18 °C until further analysis.

Residual activity (%) = 100 ×

At A0

(3)

where At and A0 are the enzyme activity of the treated and untreated juices, respectively.

2.3. Ascorbic acid Ascorbic acid content was quantified by high performance liquid chromatography (HPLC) (Souza Comapa, Carvalho, Lamarão, & Souza, 2019). Brevemente, 15 mL of the extractive solution (3% metaphosphoric acid, 8% acetic acid, 0.3 N sulfuric acid and 1 mM EDTA) and 5 mL of ultrapure water were mixed with the camu-camu juices samples. The solution was homogenized and centrifuged for 30 min (5,000 rpm/4 °C). The supernatant was filtered through porosity of 0.45 μm and injected into an Agilent 1260 Infinity system equipped with four high-pressure pumps model Agilent G1311B, UV–VIS detector ProStar model 345, and a column oven (Agilent G1316A). Separations were done using a Biorad HPX 87H (300 × 7.8 mm) column at 50 °C. The mobile phase was H2SO4 0.01 N at 0.6 mL/min.

2.8. Color analysis Color parameters were obtained using a colorimeter Delta Vista, Delta Color, Brazil, using the scale CIELAB to obtain luminosity (L*), redish-greenish (a*) and yelloowish-blueish (b*). The color difference (ΔE*) was obtained according to Eq. (4). The color parameters variation (Δ) was calculated as the difference between the value of the treated and the untreated juices (Sarangapani, O’Toole, Cullen, & Bourke, 2017):

ΔE ∗ =

(ΔL∗)2 + (Δa∗)2 + (Δb∗)2

(4)

2.4. Antioxidant activity

2.9. Bioaccessibility of ascorbic acid

Different methods were employed to analyze the antioxidant activity of the untreated and the plasma treated juices: DPPH radical (Oliveira et al., 2018), ABTS radical and ferric reducing antioxidant

The INFOGEST digestibility protocol was employed (Brodkorb et al., 2019), excluding the oral phase. Two treatments, as well as the control for the in vitro digestibility tests were chosen. The bioaccessibility index 2

Food Research International 131 (2020) 109044

D.R.G. de Castro, et al.

(%) was calculated by Eq. (5), where the concentration of ascorbic acid in the accessible fraction was divided by the concentration of ascorbic acid of the untreated juice, expressed in %.

Bioaccessibility index (%) =

Ascorbic acid content after cold plasma Ascorbic acid content of control (5)

2.10. Statistical analysis The results were evaluated by ANOVA one-way (variable: excitation frequency). Statistical analysis was carried out using the R software package (version 3.6.0). The Duncan test at 95% of confidence level was applied. All measurements were performed in triplicate.

Fig. 2. Effect of cold plasma excitation frequencies of cold plasma on the total monomeric anthocyanins of camu-camu juices. a-cDifferent letters differ significantly (p-value < 0.05).

3. Results and discussion

excitation, the lower the anthocyanin content in the juice. Unlike observed for ascorbic acid, the anthocyanin contents were considerably lower at 960 Hz. Higher excitation frequencies increase the energy density of plasma ions and electrons, presenting more stability and reactivity (McKay, Iza, & Kong, 2010). The low chemical stability of anthocyanins has also been observed in studies on cold plasma application in blueberry juices (Hou et al., 2019; Lacombe et al., 2015). It is also well known that higher frequencies produce higher amounts of ozone or free radicals, which can react with anthocyanins. Free radicals may interact with the pyrillium rings of the anthocyanin molecular structure, resulting in glycosylated chalcones. These chalcones would then be cleaved, rapidly degrading to phenolic acids and aldehydes (Sadilova, Carle, & Stintzing, 2007).

3.1. Ascorbic acid content Vitamin C is a substance with high antioxidant activity that induces inactivation of free radicals and other reactive oxygen and nitrogen species that cause oxidative damage to molecules such as lipids and DNA (Silveira et al., 2019). The ascorbic acid contents of the untreated and the plasma treated juices are shown in Fig. 1. All juices treated with cold plasma showed increased vitamin C concentration. Different treatments were significant (p-value < 0.05), with higher value of ascorbic acid content for juices treated at 960 Hz. Cold plasma acts on surfaces, modifying the chemical and physical properties of foods (Pankaj, Wan, & Keener, 2018; Zhang et al., 2019), as well as the cellulose polymeric structure by the hydrolysis of the β-1,4-glycosidic bonds (Benoit et al., 2011; Vasilieva, 2012). From 200, 420, 582 and 698 Hz no significant difference of ascorbic acid content was observed in the camu-camu juices. Moreover, higher excitation frequencies resulted in better plasma stability and reactivity (Perni, Shama, & Kong, 2008; Shi & Kong, 2005), increasing the membrane degradation rate of food plant cells. It was observed for seriguela juice that cold plasma application increased the concentration of vitamins (B3, B6 and C) (Paixão et al., 2019). Significant increase in vitamin C content was also observed for cold plasma treated guava-flavored whey beverages (Silveira et al., 2019).

3.3. Antioxidant activity The antioxidant activity values obtained by the DPPH, ABTS and FRAP methods are shown in Fig. 3A. Only DPPH presented no significant difference between treatments (data not shown). Similar result was also observed in studies on prebiotic orange juice treated using cold plasma (Almeida et al., 2015). In general, the effect of cold plasma excitation frequency on compounds with antioxidant activity presented similar behavior. An increase of the concentration of antioxidant compounds at lower frequencies (200 Hz) was observed, as well as a reduction in the intermediate excitation frequencies (420–628 Hz) and a significant increase (p-value < 0.05) for the excitation frequencies 960 Hz. Radiofrequency plasma formation was accompanied by the formation of ultraviolet radiation (Bormashenko, Grynyov, Bormashenko, & Drori, 2012). As the excitation frequency of cold plasma increases, the dissipated power in food also increased, creating more radicals to cause oxidative damage to cells and organic molecules (Sousa et al., 2011).

3.2. Total monomeric anthocyanins Anthocyanins are bioactive compounds presenting health-enhancing effects (Misra, Pankaj, Frias, Keener, & Cullen, 2015). Fig. 2 shows the effect of cold plasma excitation frequency on the anthocyanin content of juice. A significant effect (p-value < 0.05) of the excitation frequency was observed. That is, the higher the processing frequency of

3.4. Total phenolic content Phenolic compounds and ascorbic acid are the substances responsible for the antioxidant activity in fruit juices (Pankaj, Wan, Colonna, & Keener, 2017). The effect of cold plasma excitation frequency was significant for phenolic compound contents (Fig. 3B), with lower concentrations of phenolic compounds at 698 Hz. Phenolic compounds are affected by the reactions that occur at the plasma-liquid interface (oxidation, reduction and photochemical reactions), contributing to their degradation via chemical reaction with nitrogen species (Fernandes et al., 2019). A considerable increase of the phenolic compounds content was observed at 960 Hz (see Fig. 3B).

Fig. 1. Effect of cold plasma excitation frequencies on the ascorbic acid content in camu-camu juices. a-cDifferent letters differ significantly (p-value < 0.05). 3

Food Research International 131 (2020) 109044

D.R.G. de Castro, et al.

the secondary structure, as well as modifications of protein amino acid side chains (Tinello & Lante, 2018), caused by hydroxyl radicals (OH%), superoxide anion radicals (O−2%) hydroperoxy radicals (HOO%) and nitric oxide (NO%) (Pankaj, Misra, & Cullen, 2013). In PPO, the change in the secondary structure causes a decrease in the α-helix content, and an increase in the β-sheet region (Tinello & Lante, 2018). For POD, structural changes may result in decreasing of the distance between tryptophan and the heme group, which leads to increased intramolecular energy transfer from tryptophan-heme and, therefore, an increase in tryptophan fluorescence tempering (Surowsky, Fischer, Schlueter, & Knorr, 2013). Endogenous enzyme degradation is influenced by the cold plasma process parameters (Marques Silva & Sulaiman, 2018). Considerable reduction of the residual peroxidase activity was observed with increased plasma application time in tomato samples (Khani, Shokri, & Khajeh, 2017). Higher cold plasma voltage also reduced the concentration of peroxidase and polyphenol oxidase in tomatoes (Pankaj et al., 2013). Another interesting observation herein was the increase of the enzymatic activity at 960 Hz. Although contradictory with the tendency of the other studied frequencies, the increase of enzymatic activity in this treatment may be associated with the release of intracellular enzymes when the excitation frequency was increased. As cellulose presents depolymerization in high energy plasma (Benoit et al., 2011), the membranes of plant cells are damaged and release their intracellular content. This fact results in high enzymes concentration in the juice serum. Moreover, plasma is more reactive and stable at higher frequencies (Perni et al., 2008), enhancing the depolymerization of cellulose.

Fig. 3. Effect of cold plasma excitation frequencies on the antioxidant activity of camu-camu juices: FRAP (FeII µM mL−1 and ABTS (µM of TE mL−1) (A) and total phenolics compounds (gallic acid equivalent mg mL−1) (B). a-e Equal letters do not differ significantly (p-value > 0.05). The lines are for better understanding of the results. To observe the colors of this figure, consult the web version of this paper.

3.6. Color analysis Color plays an important role in food choice, representing the most important parameter for consumer acceptance (Sarangapani et al., 2017). For this reason, it is desirable that emerging technologies do not considerably effect food color (Pankaj et al., 2018). Table 1 shows the color parameters for the untreated and cold plasma treated juices. In general, the different treatments presented significant difference (pvalue < 0.05) in relation to the color parameters. The luminosity (L*) decreased significantly for cold plasma application, but the different excitation frequencies did not differ from each other. The same behavior was observed for cold plasma application in apple and sour cherry juices (Dasan & Boyaci, 2018) in which brightness was affected with increased processing time. The L* reduction for juices may be related to the degradation of bioactive compounds, resulting in darker compounds. Higher excitation frequencies reduced the values of the parameter a* (reddish coloration) (Table 1). This result may be related to the anthocyanin degradation responsible for the bright red color of the camu-camu juice. The treatments with higher excitation frequencies resulted in higher energy density and dissipated power. Due to the fact

3.5. Peroxidase and polyphenol oxidase The endogenous enzyme inactivation has been searched by food industry, as well as the use of techniques that are able to inactivate these enzymes without modifying the nutritional and sensory quality of foods (Tappi et al., 2014). Fig. 4 shows the effect of the cold plasma excitation frequency on the stability of endogenous enzymes (peroxidase and polyphenol oxidase). For both enzymes, the different treatments were significant (p-value < 0.05) and presented lower enzymatic activity in relation to the untreated juice. We can also observe that there was a tendency to reduce the enzymatic activity for higher excitation frequencies. Free radicals generated in cold plasma act mainly on the protein bonds CeH, CeN and NeH (Tappi et al., 2014). Another possibility for inactivation of endogenous enzymes is changing

Table 1 Effect of excitation frequency of cold plasma on color parameters of camu-camu juice.

Fig. 4. Effect of cold plasma excitation frequencies on the endogenous enzymes (peroxidase and polyphenol oxidase) of camu-camu juice. For better visualization of colors, consult the web version of this paper.

Assays

L*

Control 200 Hz 420 Hz 583 Hz 698 Hz 960 Hz

21.1 20.4 20.5 20.6 20.3 20.7

a* ± ± ± ± ± ±

1a 1b 2b 1ab 1b 2ab

5.9 5.6 5.9 5.3 5.8 5.5

ΔE*

b* ± ± ± ± ± ±

0.1a 0.1a 0.2a 0.2a 0.1a 0.1b

1.4 1.5 1.5 1.6 1.8 2.3

± ± ± ± ± ±

0.1b 0.1b 0.1b 0.2b 0.1b 0.1a

– 0.8 ± 0.1b 0.7 ± 0.1b 0.8 ± 0.1b 1 ± 0.1a 1.1 ± 0.2a

Results are expressed in mean ± standard deviation (n = 3). Means with the same letter in the same column are not significantly different by the Duncańs test (p > 0.05). 4

Food Research International 131 (2020) 109044

D.R.G. de Castro, et al.

Emerging technologies have shown improvement in bioaccessibility of bioactive compounds. This fact is related to the low processing temperature, as well the damage caused in the plant cell membranes, releasing bioactive compounds and increasing their availability for absorption by humans (Barba et al., 2017). There are few studies reporting the effect of cold plasma on improving the bioavailability of bioactive compounds such as ascorbic acid. However, several other emerging technologies have already proven this behavior, such as the use of high pressure in orange juices (Sánchez-Moreno et al., 2005), pulse electric field in orange juices (Sánchez-Moreno et al., 2004) and ultrasound for cashew juices (Fonteles et al., 2016). 4. Conclusions This study revealed that the excitation frequency of cold plasma is a parameter that should be considered for food application studies. The results showed that higher excitation frequencies increased the availability of ascorbic acid in the juice serum. This result may be related to the plant cell membrane degradation, resulting in the release of intracellular bioactive compounds. Anthocyanins showed greater degradation with increasing excitation frequency. The same behavior was observed for endogenous enzymes (peroxidase and polyphenol oxidase). For this reason, the cold plasma represents an efficient alternative for inactivation of these enzymes. Moreover, our results have proven the increased bioavailability of ascorbic acid with cold plasma application, representing an interesting form for improving the nutritional quality of foods, as well as improving consumer health. Therefore, cold plasma processing can be successfully used as a technology for food industry, improving the nutritional quality of foods and reducing the activity of endogenous enzymes.

Fig. 5. In vitro digestibility of ascorbic acid in relation to the different digestion phases (A) and ascorbic acid bioaccessibility (B) of camu-camu juices. ac Different letters differ significantly (p-value < 0.05).

Author contribution

that anthocyanins are very degradable pigments, the increasing of the excitation frequency resulted in loss of reddish color. For juices (Hou et al., 2019), blueberries fruits (Sarangapani et al., 2017) and pomegranate juices (Bursać Kovačević et al., 2016), the authors also observed a reduction in the parameter a* with the increase of the processing time. The reduction of anthocyanin content was also observed with increased processing time, confirming the sensibility of anthocyanin molecules in relation to plasma increased exposure. The parameter b* (yellowish-green coloration) presented significant change only for excitation at 960 Hz, with a tendency to change coloration to yellowish region (+b*). These results may be related to the degradation of anthocyanins and ascorbic acid at high excitation frequency, resulting in a orange-brown color (+b* and +a*). Juices treated with higher excitation frequencies (698 and 960 Hz) presented considerable color variation. This result may be related to the greater degradation of anthocyanins. Despite significant variation in color parameters, the color variation may not interfere in product acceptance by consumers as previous studies reports that only values of ΔE* > 3 are noticeable (Dasan & Boyaci, 2018).

P.H. Campelo, F.A.N. Fernandes and S. Rodrigues devised the project, the main conceptual ideas and proof outline. D.R.G. Castro, F.A.N. Fernandes and S. Rodrigues carried out the cold plasma treatments. D.R.G. Castro, E.A. Sanches and J.A. Bezerra carried out ascorbic acid, anthocyanins, colors and enzymes experiments. D.R.G. Castro, J.M. Mar and L.S. da Silva carried out the antioxidant activity experiments. L.S. da Silva and K.A. da Silva carried out the digestibility experiments. P.H. Campelo supervised the project and wrote the paper. All authors discussed the results and contributed to the final manuscript. Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgment The authors are grateful to the Fundação de Amparo à Pesquisa do Estado do Amazonas (FAPEAM; 062.00917/2015 - FIXAM), the Coordenação de Aperfeiçoamento de Pessoal do Ensino Superior (CAPES) and to the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for their financial support.

3.7. Bioaccessibility of ascorbic acid Fig. 5A and B show the ascorbic acid concentration of juice during the simulated digestion process and final bioaccessibility, respectively. Only the treatments resulting in the highest concentration of ascorbic acid at the end of the cold plasma processing (683 and 960 Hz) were evaluated. The different treatments increased the availability of ascorbic acid at the end of the simulated digestion. This behavior is desirable in food industry as cold-processed foods may offer higher concentrations of bioactive compounds, helping to improve consumer health. Considering different excitation frequencies, the results corroborated to those observed in Fig. 1, in which the highest excitation frequency resulted in higher concentration of ascorbic acid among all analyzed treatments, including the untreated juice.

References Almeida, F. D. L., Cavalcante, R. S., Cullen, P. J., Frias, J. M., Bourke, P., Fernandes, F. A. N., & Rodrigues, S. (2015). Effects of atmospheric cold plasma and ozone on prebiotic orange juice. Innovative Food Science and Emerging Technologies, 32, 127–135. https:// doi.org/10.1016/j.ifset.2015.09.001. Azevedo, S. G., Mar, J. M., da Silva, L. S., França, L. P., Machado, M. B., Tadei, W. P., ... Sanches, E. A. (2018). Bioactivity of Licaria puchury-major essential oil against Aedes aegypti, Tetranychus urticae and Cerataphis lataniae. Records of Natural Products, 12(3), 229–238. https://doi.org/10.25135/rnp.25.17.05.036. Barba, F. J., Mariutti, L. R. B., Bragagnolo, N., Mercadante, A. Z., Barbosa-Cánovas, G. V.,

5

Food Research International 131 (2020) 109044

D.R.G. de Castro, et al.

05.007. Oliveira, A. F. A., Mar, J. M., Santos, S. F., da Silva Júnior, J. L., Kluczkovski, A. M., Bakry, A. M., ... Campelo, P. H. (2018). Non-thermal combined treatments in the processing of açai (Euterpe oleracea) juice. Food Chemistry, 265(May), 57–63. https://doi.org/ 10.1016/j.foodchem.2018.05.081. Paixão, L. M. N., Fonteles, T. V., Oliveira, V. S., Fernandes, F. A. N., & Rodrigues, S. (2019). Cold plasma effects on functional compounds of siriguela juice. Food and Bioprocess Technology, 12(1), 110–121. https://doi.org/10.1007/s11947-018-2197-z. Pankaj, S. K., Misra, N. N., & Cullen, P. J. (2013). Kinetics of tomato peroxidase inactivation by atmospheric pressure cold plasma based on dielectric barrier discharge. Innovative Food Science & Emerging Technologies, 19, 153–157. https://doi.org/10. 1016/j.ifset.2013.03.001. Pankaj, S. K., Wan, Z., & Keener, K. M. (2018). Effects of cold plasma on food quality: A review. Foods, 7, 4. https://doi.org/10.3390/foods7010004. Pankaj, S. K., Wan, Z., Colonna, W., & Keener, K. M. (2017). Effect of high voltage atmospheric cold plasma on white grape juice quality. Journal of the Science of Food and Agriculture, 97(12), 4016–4021. https://doi.org/10.1002/jsfa.8268. Perni, S., Shama, G., & Kong, M. G. (2008). Cold atmospheric plasma disinfection of cut fruit surfaces contaminated with migrating microorganisms. Journal of Food Protection, 71(8), 1619–1625. https://doi.org/10.4315/0362-028X-71.8.1619. Rodríguez, Ó., Gomes, W. F., Rodrigues, S., & Fernandes, F. A. N. (2017). Effect of indirect cold plasma treatment on cashew apple juice (Anacardium occidentale L.). LWT Food Science and Technology, 84, 457–463. https://doi.org/10.1016/j.lwt.2017.06. 010. Sadilova, E., Carle, R., & Stintzing, F. C. (2007). Thermal degradation of anthocyanins and its impact on color and in vitro antioxidant capacity. Molecular Nutrition & Food Research, 51(12), 1461–1471. https://doi.org/10.1002/mnfr.200700179. Sánchez-Moreno, C., Cano, M. P., De Ancos, B., Plaza, L., Olmedilla, B., Granado, F., ... Martín, A. (2004). Pulsed electric fields-processed orange juice consumption increases plasma vitamin C and decreases F2-isoprostanes in healthy humans. Journal of Nutritional Biochemistry, 15(10), 601–607. https://doi.org/10.1016/j.jnutbio.2004. 04.007. Sánchez-Moreno, C., Plaza, L., Elez-Martínez, P., De Ancos, B., Martín-Belloso, O., & Cano, M. P. (2005). Impact of high pressure and pulsed electric fields on bioactive compounds and antioxidant activity of orange juice in comparison with traditional thermal processing. Journal of Agricultural and Food Chemistry, 53(11), 4403–4409. https://doi.org/10.1021/jf048839b. Sarangapani, C., O’Toole, G., Cullen, P. J., & Bourke, P. (2017). Atmospheric cold plasma dissipation efficiency of agrochemicals on blueberries. Innovative Food Science and Emerging Technologies, 44, 235–241. https://doi.org/10.1016/j.ifset.2017.02.012. Scholtz, V., Pazlarova, J., Souskova, H., Khun, J., & Julak, J. (2015). Nonthermal plasma A tool for decontamination and disinfection. Biotechnology Advances, 33(6), 1108–1119. https://doi.org/10.1016/j.biotechadv.2015.01.002. Shi, J. J., & Kong, M. G. (2005). Expansion of the plasma stability range in radio-frequency atmospheric-pressure glow discharges. Applied Physics Letters, 87(20), 1–3. https://doi.org/10.1063/1.2128691. Silveira, M. R., Coutinho, N. M., Esmerino, E. A., Moraes, J., Fernandes, L. M., Pimentel, T. C., ... Cruz, A. G. (2019). Guava-flavored whey beverage processed by cold plasma technology: Bioactive compounds, fatty acid profile and volatile compounds. Food Chemistry, 279(October 2018), 120–127. https://doi.org/10.1016/j.foodchem.2018. 11.128. Sousa, J. S., Niemi, K., Cox, L. J., Algwari, Q. T., Gans, T., & O’Connell, D. (2011). Cold atmospheric pressure plasma jets as sources of singlet delta oxygen for biomedical applications. Journal of Applied Physics, 109(12), 1–8. https://doi.org/10.1063/1. 3601347. Souza Comapa, S., Carvalho, L. M. S., Lamarão, C. V., Souza, F. das C. do A., Aguiar, J. P. L., Silva, L. S., … Campelo, P. H. (2019). Microwave processing of camu‐camu juices: Physicochemical and microbiological parameters. Journal of Food Processing and Preservation, 43(7), 1–11. https://doi.org/10.1111/jfpp.13989. Suhem, K., Matan, N., Nisoa, M., & Matan, N. (2013). Inhibition of Aspergillus flavus on agar media and brown rice cereal bars using cold atmospheric plasma treatment. International Journal of Food Microbiology, 161(2), 107–111. https://doi.org/10.1016/ j.ijfoodmicro.2012.12.002. Surowsky, B., Fischer, A., Schlueter, O., & Knorr, D. (2013). Cold plasma effects on enzyme activity in a model food system. Innovative Food Science and Emerging Technologies, 19, 146–152. https://doi.org/10.1016/j.ifset.2013.04.002. Tappi, S., Berardinelli, A., Ragni, L., Dalla Rosa, M., Guarnieri, A., & Rocculi, P. (2014). Atmospheric gas plasma treatment of fresh-cut apples. Innovative Food Science and Emerging Technologies, 21, 114–122. https://doi.org/10.1016/j.ifset.2013.09.012. Tinello, F., & Lante, A. (2018). Recent advances in controlling polyphenol oxidase activity of fruit and vegetable products. Innovative Food Science and Emerging Technologies, 50(May), 73–83. https://doi.org/10.1016/j.ifset.2018.10.008. Vasilieva, T. M. (2012). Application of electron beam plasma for biopolymers modification. Journal of Physics: Conference Series, 370(1), 1–7. https://doi.org/10.1088/ 1742-6596/370/1/012012. Wertheimer, M. R., & Moisan, M. (1985). Comparison of microwave and lower frequency plasmas for thin film deposition and etching. Journal of Vacuum Science & Technology A: Vacuum, Surfaces, and Films, 3(6), 2643–2649. https://doi.org/10.1116/1.572805. Zanatta, C. F., Cuevas, E., Bobbio, F. O., Winterhalter, P., & Mercadante, A. Z. (2005). Determination of Anthocyanins from Camu-camu (Myrciaria dubia) by HPLC–PDA, HPLC–MS, and NMR. Journal of Agricultural and Food Chemistry, 53(24), 9531–9535. https://doi.org/10.1021/jf051357v. Zhang, X.-L., Deng, L.-Z., Wang, J., Xiao, H.-W., Zhong, C.-S., Mujumdar, A. S., & Yang, X.-H. (2019). Cold plasma pretreatment enhances drying kinetics and quality attributes of chili pepper (Capsicum annuum L.). Journal of Food Engineering, 241(August 2018), 51–57. https://doi.org/10.1016/j.jfoodeng.2018.08.002.

& Orlien, V. (2017). Bioaccessibility of bioactive compounds from fruits and vegetables after thermal and nonthermal processing. Trends in Food Science and Technology, 67, 195–206. https://doi.org/10.1016/j.tifs.2017.07.006. Benoit, M., Rodrigues, A., Zhang, Q., Fourré, E., De Oliveira Vigier, K., Tatibouët, J.-M., & Jérôme, F. (2011). Depolymerization of Cellulose Assisted by a Nonthermal Atmospheric Plasma. Angewandte Chemie International Edition, 50(38), 8964–8967. https://doi.org/10.1002/anie.201104123. Bormashenko, E., Grynyov, R., Bormashenko, Y., & Drori, E. (2012). Cold radiofrequency plasma treatment modifies wettability and germination speed of plant seeds. Scientific Reports, 2, 3–10. https://doi.org/10.1038/srep00741. Brodkorb, A., Egger, L., Alminger, M., Alvito, P., Assunção, R., Ballance, S., ... Recio, I. (2019). INFOGEST static in vitro simulation of gastrointestinal food digestion. Nature Protocols, 14(4), 991–1014. https://doi.org/10.1038/s41596-018-0119-1. Bursać Kovačević, D., Putnik, P., Dragović-Uzelac, V., Pedisić, S., Režek Jambrak, A., & Herceg, Z. (2016). Effects of cold atmospheric gas phase plasma on anthocyanins and color in pomegranate juice. Food Chemistry, 190, 317–323. https://doi.org/10.1016/ j.foodchem.2015.05.099. Chen, C., Liu, C., Jiang, A., Guan, Q., Sun, X., Liu, S., ... Hu, W. (2019). The effects of cold plasma-activated water treatment on the microbial growth and antioxidant properties of fresh-cut pears. Food and Bioprocess Technology. https://doi.org/10.1007/s11947019-02331-w. Cunha-Santos, E. C. E., Viganó, J., Neves, D. A., Martínez, J., & Godoy, H. T. (2019). Vitamin C in camu-camu [Myrciaria dubia (H.B.K.) McVaugh]: Evaluation of extraction and analytical methods. Food Research International, 115(August 2018), 160–166. https://doi.org/10.1016/j.foodres.2018.08.031. Dasan, B. G., & Boyaci, I. H. (2018). Effect of cold atmospheric plasma on inactivation of escherichia coli and physicochemical properties of apple, orange, tomato juices, and sour cherry nectar. Food and Bioprocess Technology, 11(2), 334–343. https://doi.org/ 10.1007/s11947-017-2014-0. Dong, X. Y., & Yang, Y. L. (2019). A novel approach to enhance blueberry quality during storage using cold plasma at atmospheric air pressure. Food and Bioprocess Technology, 12(8), 1409–1421. https://doi.org/10.1007/s11947-019-02305-y. Fernandes, F. A. N., Santos, V. O., & Rodrigues, S. (2019). Effects of glow plasma technology on some bioactive compounds of acerola juice. Food Research International, 115(February 2018), 16–22. https://doi.org/10.1016/j.foodres.2018.07.042. Fonteles, T. V., Leite, A. K. F., Silva, A. R. A., Carneiro, A. P. G., Miguel, E. D. C., Cavada, B. S., ... Rodrigues, S. (2016). Ultrasound processing to enhance drying of cashew apple bagasse puree: Influence on antioxidant properties and in vitro bioaccessibility of bioactive compounds. Ultrasonics Sonochemistry, 31, 237–249. https://doi.org/10. 1016/j.ultsonch.2016.01.003. Hou, Y., Wang, R., Gan, Z., Shao, T., Zhang, X., He, M., & Sun, A. (2019). Effect of cold plasma on blueberry juice quality. Food Chemistry, 290(October 2018), 79–86. https://doi.org/10.1016/j.foodchem.2019.03.123. Khani, M. R., Shokri, B., & Khajeh, K. (2017). Studying the performance of dielectric barrier discharge and gliding arc plasma reactors in tomato peroxidase inactivation. Journal of Food Engineering, 197, 107–112. https://doi.org/10.1016/j.jfoodeng.2016. 11.012. Lacombe, A., Niemira, B. A., Gurtler, J. B., Fan, X., Sites, J., Boyd, G., & Chen, H. (2015). Atmospheric cold plasma inactivation of aerobic microorganisms on blueberries and effects on quality attributes. Food Microbiology, 46, 479–484. https://doi.org/10. 1016/j.fm.2014.09.010. Li, F., Chen, G., Zhang, B., & Fu, X. (2017). Current applications and new opportunities for the thermal and non-thermal processing technologies to generate berry product or extracts with high nutraceutical contents. Food Research International, 100(June), 19–30. https://doi.org/10.1016/j.foodres.2017.08.035. Locke, B. R., & Shih, K. Y. (2011). Review of the methods to form hydrogen peroxide in electrical discharge plasma with liquid water. Plasma Sources Science and Technology, 20(3), https://doi.org/10.1088/0963-0252/20/3/034006. Marques Silva, F. V., & Sulaiman, A. (2018). Polyphenoloxidase in fruit and vegetables: inactivation by thermal and non-thermal processes. Encyclopedia of Food Chemistry, 2, 287–301. https://doi.org/10.1016/b978-0-08-100596-5.21636-3. McKay, K., Iza, F., & Kong, M. G. (2010). Excitation frequency effects on atmosphericpressure helium RF microplasmas: Plasma density, electron energy and plasma impedance. European Physical Journal D, 60(3), 497–503. https://doi.org/10.1140/ epjd/e2010-00191-7. Mercali, G. D., Gurak, P. D., Schmitz, F., & Marczak, L. D. F. (2015). Evaluation of nonthermal effects of electricity on anthocyanin degradation during ohmic heating of jaboticaba (Myrciaria cauliflora) juice. Food Chemistry, 171, 200–205. https://doi. org/10.1016/j.foodchem.2014.09.006. Misra, N. N., Moiseev, T., Patil, S., Pankaj, S. K., Bourke, P., Mosnier, J. P., ... Cullen, P. J. (2014). Cold plasma in modified atmospheres for post-harvest treatment of strawberries. Food and Bioprocess Technology, 7(10), 3045–3054. https://doi.org/10.1007/ s11947-014-1356-0. Misra, N. N., Pankaj, S. K., Frias, J. M., Keener, K. M., & Cullen, P. J. (2015). The effects of nonthermal plasma on chemical quality of strawberries. Postharvest Biology and Technology, 110, 197–202. https://doi.org/10.1016/j.postharvbio.2015.08.023. Moreira, S. A., Alexandre, E. M. C., Pintado, M., & Saraiva, J. A. (2019). Effect of emergent non-thermal extraction technologies on bioactive individual compounds profile from different plant materials. Food Research International, 115(May 2018), 177–190. https://doi.org/10.1016/j.foodres.2018.08.046. Neri-Numa, I. A., Soriano Sancho, R. A., Pereira, A. P. A., & Pastore, G. M. (2018). Small Brazilian wild fruits: Nutrients, bioactive compounds, health-promotion properties and commercial interest. Food Research International, 103(October 2017), 345–360. https://doi.org/10.1016/j.foodres.2017.10.053. Noriega, E., Shama, G., Laca, A., Díaz, M., & Kong, M. G. (2011). Cold atmospheric gas plasma disinfection of chicken meat and chicken skin contaminated with Listeria innocua. Food Microbiology, 28(7), 1293–1300. https://doi.org/10.1016/j.fm.2011.

6