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Effect of Cold Atmospheric Plasma on Inactivation of Escherichia coli and Physicochemical Properties of Apple, Orange, Tomato Juices, and Sour Cherry Nectar

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Abstract

In this study, orange, tomato, apple juices, and sour cherry nectar were exposed to an atmospheric pressure plasma jet. Plasma treatments were carried out using air as a precursor under constant gas flow (3000 L/h) at 650 W for different treatment times (30, 60, 90, and 120 s). After plasma processing, reduction of Escherichia coli, Hunter’s color parameters (L*, a*, b*), total phenolic content, and pH values were evaluated. The inactivation effect of cold atmospheric plasma (CAP) was investigated on E. coli, and the highest significant reductions were achieved in apple juice (4.02 ± 0.03 log CFU/mL) followed by sour cherry (3.34 ± 0.09 log CFU/mL), while the values in orange (1.59 ± 0.17 log CFU/mL) and tomato juices (1.43 ± 0.22 log CFU/mL) were lower, which could be attributed to the food matrix. Color parameters, except for apple juice, did not show significant changes after processing. Compared to untreated juice, plasma treatment yielded higher phenolic content from 10 to 15%, while pH values did not change significantly and the temperature remained below 40 °C after all plasma treatments. This study showed that CAP treatment had positive influences on phenolic stability and color change in all samples regardless of food intrinsic factors, while it was more effective on bacterial inactivation in clear juices than turbid ones. Our results indicate that atmospheric plasma appears to be a promising technology for microbial inactivation without causing undesirable changes in food product.

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References

  • Almeida, F. D. L., Cavalcante, R. S., Cullen, P. J., Frias, J. M., Bourke, P., Fernandes, F. A. N., et al. (2015). Effects of atmospheric cold plasma and ozone on prebiotic orange juice. Innovative Food Science & Emerging Technologies, 32, 127–135.

    Article  CAS  Google Scholar 

  • Arjunan, K. P., Sharma, V. K., & Ptasinska, S. (2015). Effects of atmospheric pressure plasmas on isolated and cellular DNA—a review. International Journal of Molecular Sciences, 16(2), 2971–3016.

    Article  CAS  Google Scholar 

  • Baier, M., Gorgen, M., Ehlbeck, J., Knorr, D., Herppich, W. B., & Schluter, O. (2014). Non-thermal atmospheric pressure plasma: screening for gentle process conditions and antibacterial efficiency on perishable fresh produce. Innovative Food Science & Emerging Technologies, 22, 147–157.

    Article  CAS  Google Scholar 

  • Barba, F. J., Parniakov, O., Pereira, S. A., Wiktor, A., Grimi, N., Boussetta, N., et al. (2015a). Current applications and new opportunities for the use of pulsed electric fields in food science and industry. Food Research International, 77, 773–798.

    Article  Google Scholar 

  • Barba, F. J., Terefe, N. S., Buckow, R., Knorr, D., & Orlien, V. (2015b). New opportunities and perspectives of high pressure treatment to improve health and safety attributes of foods. A review. Food Research International, 77, 725–742.

    Article  Google Scholar 

  • Bermudez-Aguirre, D., Wemlinger, E., Pedrow, P., Barbosa-Canovas, G., & Garcia-Perez, M. (2013). Effect of atmospheric pressure cold plasma (APCP) on the inactivation of Escherichia coli in fresh produce. Food Control, 34(1), 149–157.

    Article  CAS  Google Scholar 

  • Biederman, H., Boyaci, I. H., Bilkova, P., Slavinska, D., Mutlu, S., Zemek, J., et al. (2001). Characterization of glow-discharge-treated cellulose acetate membrane surfaces for single-layer enzyme electrode studies. Journal of Applied Polymer Science, 81(6), 1341–1352.

    Article  CAS  Google Scholar 

  • Brandenburg, R., Ehlbeck, J., Stieber, M., von Woedtke, T., Zeymer, J., Schluter, O., et al. (2007). Antimicrobial treatment of heat sensitive materials by means of atmospheric pressure rf-driven plasma jet. Contributions to Plasma. Physics, 47(1–2), 72–79.

    CAS  Google Scholar 

  • Buchner, N., Krumbein, A., Rohn, S., & Kroh, L. W. (2006). Effect of thermal processing on the flavonols rutin and quercetin. Rapid Communications in Mass Spectrometry, 20(21), 3229–3235.

    Article  CAS  Google Scholar 

  • Butz, P., & Tauscher, B. (2002). Emerging technologies: chemical aspects. Food Research International, 35(2–3), 279–284.

    Article  CAS  Google Scholar 

  • Cerf, O. (1977). A review. Tailing of survival curves of bacterial spores. Journal of Applied Microbiology, 42, 1–19.

    CAS  Google Scholar 

  • Charles-Rodriguez, A. V., Nevarez-Moorillon, G. V., Zhang, Q. H., & Ortega-Rivas, E. (2007). Comparison of thermal processing and pulsed electric fields treatment in pasteurization of apple juice. Food and Bioproducts Processing, 85(C2), 93–97.

    Article  Google Scholar 

  • Dasan, B. G., Boyaci, I. H., & Mutlu, M. (2016a). Inactivation of aflatoxigenic fungi (Aspergillus spp.) on granular food model, maize, in an atmospheric pressure fluidized bed plasma system. Food Control, 70, 1–8.

    Article  CAS  Google Scholar 

  • Dasan, B. G., Mutlu, M., & Boyaci, I. H. (2016b). Decontamination of Aspergillus flavus and Aspergillus parasiticus spores on hazelnuts via atmospheric pressure fluidized bed plasma reactor. International Journal of Food Microbiology, 216, 50–59.

    Article  CAS  Google Scholar 

  • Dasan, B. G., Boyaci, I. H., & Mutlu, M. (2017a). Nonthermal plasma treatment of Aspergillus spp. spores on hazelnuts in an atmospheric pressure fluidized bed plasma system: impact of process parameters and surveillance of the residual viability of spores. Journal of Food Engineering, 196, 139–149.

    Article  CAS  Google Scholar 

  • Dasan, B. G., Onal-Ulusoy, B., Pawlat, J., Diatczyk, J., Sen, Y., & Mutlu, M. (2017b). A new and simple approach for decontamination of food contact surfaces with gliding arc discharge atmospheric non-thermal plasma. Food and Bioprocess Technology, 10, 650–661.

  • Deng, X. T., Shi, J. J., & Kong, M. G. (2006). Physical mechanisms of inactivation of Bacillus subtilis spores using cold atmospheric plasmas. IEEE Transactions on Plasma Science, 34(4), 1310–1316.

    Article  Google Scholar 

  • Dhuique-Mayer, C., Caris-Veyrat, C., Ollitrault, P., Curk, F., & Amiot, M. J. (2005). Varietal and interspecific influence on micronutrient contents in citrus from the Mediterranean area. Journal of Agricultural and Food Chemistry, 53(6), 2140–2145.

    Article  CAS  Google Scholar 

  • Echeverría, G., & López, M. L. (2014). Assessing juice quality: analysis of organoleptic properties of fruit juices. In V. Falguera & A. Ibarz (Eds.), Juice processing: quality, safety, and value-added opportunities (pp. 137–150). Boca Raton: CRC Press Taylor & Francis Group.

    Chapter  Google Scholar 

  • Falguera, V., & Ibarz, A. (2014). Squeezing fruits in the second decade of the twenty-first century: the current situation of the juice industry. In V. Falguera & A. Ibarz (Eds.), Juice processing: quality, safety, and value-added opportunities (pp. 1–12). Boca Raton: Taylor & Francis Group, LLC.

    Chapter  Google Scholar 

  • Ferrari, G., Maresca, P., & Ciccarone, R. (2010). The application of high hydrostatic pressure for the stabilization of functional foods: pomegranate juice. Journal of Food Engineering, 100(2), 245–253.

    Article  CAS  Google Scholar 

  • Fridman, G., Brooks, A. D., Balasubramanian, M., Fridman, A., Gutsol, A., Vasilets, V. N., et al. (2007). Comparison of direct and indirect effects of non-thermal atmospheric-pressure plasma on bacteria. Plasma Processes and Polymers, 4(4), 370–375.

    Article  CAS  Google Scholar 

  • Garofulic, I. E., Jambrak, A. R., Milosevic, S., Dragovic-Uzelac, V., Zoric, Z., & Herceg, Z. (2015). The effect of gas phase plasma treatment on the anthocyanin and phenolic acid content of sour cherry Marasca (Prunus cerasus var. Marasca) juice. Lwt-Food Science and Technology, 62(1), 894–900.

    Article  Google Scholar 

  • Gasperi, F., Aprea, E., Biasioli, F., Carlin, S., Endrizzi, I., Pirretti, G., et al. (2009). Effects of supercritical CO2 and N2O pasteurisation on the quality of fresh apple juice. Food Chemistry, 115(1), 129–136.

    Article  CAS  Google Scholar 

  • Geeraerd, A. H., Valdramidis, V. P., & Van Impe, J. F. (2005). GInaFiT, a freeware tool to assess non-log-linear microbial survivor curves. International Journal of Food Microbiology, 102, 95–105.

    Article  CAS  Google Scholar 

  • Gialleli, A. I., Bekatorou, A., Kanellaki, M., Nigam, P., & Koutinas, A. A. (2016). Apple juice preservation through microbial adsorption by nano/micro-tubular cellulose. Innovative Food Science & Emerging Technologies, 33, 416–421.

    Article  CAS  Google Scholar 

  • Graves, D. B. (2012). The emerging role of reactive oxygen and nitrogen species in redox biology and some implications for plasma applications to medicine and biology. Journal of Physics D-Applied Physics, IOP Publishing Ltd., 45(26).

  • Grzegorzewski, F., Ehlbeck, J., Schluter, O., Kroh, L. W., & Rohn, S. (2011). 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 Science and Technology, 44(10), 2285–2289.

    Article  CAS  Google Scholar 

  • Gunaydin, B., Sir, N., Kavlak, S., Guner, A., & Mutlu, M. (2010). A new approach for the electrochemical detection of phenolic compounds. Part I: modification of graphite surface by plasma polymerization technique and characterization by Raman spectroscopy. Food and Bioprocess Technology, 3(3), 473–479.

    Article  Google Scholar 

  • Gurol, C., Ekinci, F. Y., Aslan, N., & Korachi, M. (2012). Low temperature plasma for decontamination of E. coli in milk. International Journal of Food Microbiology, 157(1), 1–5.

    Article  CAS  Google Scholar 

  • Herceg, Z., Kovacevic, D. B., Kljusuric, J. G., Jambrak, A. R., Zoric, Z., & Dragovic-Uzelac, V. (2016). Gas phase plasma impact on phenolic compounds in pomegranate juice. Food Chemistry, 190, 665–672.

    Article  CAS  Google Scholar 

  • Hertwig, C., Reineke, K., Ehlbeck, J., Knorr, D., & Schluter, O. (2015). Decontamination of whole black pepper using different cold atmospheric pressure plasma applications. Food Control, 55, 221–229.

    Article  CAS  Google Scholar 

  • Ikawa, S., Kitano, K., & Hamaguchi, S. (2010). Effects of pH on bacterial inactivation in aqueous solutions due to low-temperature atmospheric pressure plasma application. Plasma Processes and Polymers, 7(1), 33–42.

    Article  CAS  Google Scholar 

  • Khoddami, A., Wilkes, M. A., & Roberts, T. H. (2013). Techniques for analysis of plant phenolic compounds. Molecules, 18(2), 2328–2375.

    Article  CAS  Google Scholar 

  • Kovacevic, D. B., Kljusuric, J. G., Putnik, P., Vukusic, T., Herceg, Z., & Dragovic-Uzelac, V. (2016a). Stability of polyphenols in chokeberry juice treated with gas phase plasma. Food Chemistry, 212, 323–331.

    Article  Google Scholar 

  • Kovacevic, D. B., Putnik, P., Dragovic-Uzelac, V., Pedisic, S., Jambrak, A. R., & Herceg, Z. (2016b). Effects of cold atmospheric gas phase plasma on anthocyanins and color in pomegranate juice. Food Chemistry, 190, 317–323.

    Article  Google Scholar 

  • Ma, T. J., & Lan, W. S. (2015). Effects of non-thermal plasma sterilization on volatile components of tomato juice. International journal of Environmental Science and Technology, 12(12), 3767–3772.

    Article  CAS  Google Scholar 

  • Ma, Y., Zhang, G. J., Shi, X. M., Xu, G. M., & Yang, Y. (2008). Chemical mechanisms of bacterial inactivation using dielectric barrier discharge plasma in atmospheric air. IEEE Transactions on Plasma Science, 36(4), 1615–1620.

    Article  CAS  Google Scholar 

  • Mai-Prochnow, A., Murphy, A. B., McLean, K. M., Kong, M. G., & Ostrikov, K. (2014). Atmospheric pressure plasmas: infection control and bacterial responses. International Journal of Antimicrobial Agents, 43(6), 508–517.

    Article  CAS  Google Scholar 

  • Moisan, M., Barbeau, J., Moreau, S., Pelletier, J., Tabrizian, M., & Yahia, L. H. (2001). Low-temperature sterilization using gas plasmas: a review of the experiments and an analysis of the inactivation mechanisms. International Journal of Pharmaceutics, 226(1–2), 1–21.

    Article  CAS  Google Scholar 

  • Mutlu, M., Mutlu, S., Boyaci, I. H., Alp, B., & Piskin, E. (1998). High-linearity glucose enzyme electrodes for food industries: preparation by a plasma polymerization technique. Polymers in Sensors, 690, 57–65.

    Article  CAS  Google Scholar 

  • Noci, F., Riener, J., Walkling-Ribeiro, M., Cronin, D. A., Morgan, D. J., & Lyng, J. G. (2008). Ultraviolet irradiation and pulsed electric fields (PEF) in a hurdle strategy for the preservation of fresh apple juice. Journal of Food Engineering, 85(1), 141–146.

    Article  Google Scholar 

  • Schluter, O., Ehlbeck, J., Hertel, C., Habermeyer, M., Roth, A., Engel, K. H., et al. (2013). Opinion on the use of plasma processes for treatment of foods. Molecular Nutrition & Food Research, 57(5), 920–927.

    Article  Google Scholar 

  • Shi, X. M., Zhang, G. J., Wu, X. L., Li, Y. X., Ma, Y., & Shao, X. J. (2011). Effect of low-temperature plasma on microorganism inactivation and quality of freshly squeezed orange juice. IEEE Transactions on Plasma Science, 39(7), 1591–1597.

    Article  CAS  Google Scholar 

  • Simunek, M., Jambrak, A. R., Dobrovic, S., Herceg, Z., & Vukusic, T. (2014). Rheological properties of ultrasound treated apple, cranberry and blueberry juice and nectar. Journal of Food Science and Technology-Mysore, 51(12), 3577–3593.

    Article  CAS  Google Scholar 

  • Singleton, V. L., Orthofer, R., & Lamuela-Raventos, R. M. (1999). Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Oxidants and Antioxidants, Pt A, 299, 152–178.

    Article  CAS  Google Scholar 

  • Smet, C., Noriega, E., Rosier, F., Walsh, J. L., Valdramidis, V. P., & Van Impe, J. F. (2016). Influence of food intrinsic factors on the inactivation efficacy of cold atmospheric plasma: impact of osmotic stress, suboptimal pH and food structure. Innovative Food Science & Emerging Technologies, 38, 393–406.

    Article  CAS  Google Scholar 

  • Smet, C., Noriega, E., Rosier, F., Walsh, J. L., Valdramidis, V. P., & Van Impe, J. F. (2017). Impact of food model (micro)structure on the microbial inactivation efficacy of cold atmospheric plasma. International Journal of Food Microbiology, 240, 47–56.

    Article  CAS  Google Scholar 

  • Surowsky, B., Frohling, A., Gottschalk, N., Schluter, O., & Knorr, D. (2014). Impact of cold plasma on Citrobacter freundii in apple juice: inactivation kinetics and mechanisms. International Journal of Food Microbiology, 174, 63–71.

    Article  CAS  Google Scholar 

  • Surowsky, B., Schluter, O., & Knorr, D. (2015). Interactions of non-thermal atmospheric pressure plasma with solid and liquid food systems: a review. Food Engineering Reviews, 7(2), 82–108.

    Article  CAS  Google Scholar 

  • Valdramidis, V. P., Graham, W. D., Beattie, A., Linton, M., Mckay, A., Fearon, A. M., et al. (2009). Defining the stability interfaces of apple juice: implications on the optimisation and design of high hydrostatic pressure treatment. Innovative Food Science & Emerging Technologies, 10(4), 396–404.

    Article  CAS  Google Scholar 

  • von Woedtke, T., Reuter, S., Masur, K., & Weltmann, K. D. (2013). Plasmas for medicine. Physics Reports-Review Section of Physics Letters, 530(4), 291–320.

    Google Scholar 

  • Zinoviadou, K. G., Galanakis, C. M., Brncic, M., Grimi, N., Boussetta, N., Mota, M. J., et al. (2015). Fruit juice sonication: implications on food safety and physicochemical and nutritional properties. Food Research International, 77, 743–752.

    Article  CAS  Google Scholar 

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Correspondence to Beyhan Gunaydin Dasan.

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Dasan, B.G., Boyaci, I.H. Effect of Cold Atmospheric Plasma on Inactivation of Escherichia coli and Physicochemical Properties of Apple, Orange, Tomato Juices, and Sour Cherry Nectar. Food Bioprocess Technol 11, 334–343 (2018). https://doi.org/10.1007/s11947-017-2014-0

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