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Preservation of Reactive Species in Frozen Plasma-Activated Water and Enhancement of its Bactericidal Activity Through pH Adjustment

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Abstract

Maintaining the characteristics of plasma-activated water (PAW) over a long period is a challenging task as it could compromise its beneficial properties such as antibacterial activity and reactivity. In this study, we aimed to present a practical method to produce PAW for fresh produce treatment. As the use of PAW during the postharvest processing stages could be beneficial, we implemented a strategy to develop frozen PAW (FPAW) containing high concentrations of reactive species and effective in deactivating pathogenic bacteria. However, lowering the freezing temperature from − 20 to − 80 °C and shortening the freezing time failed to maintain the concentrations of hydrogen peroxide (H2O2) and nitrite (NO2−) in FPAW, ultimately reducing its bactericidal activity after a while. Furthermore, we successfully applied pH adjustment to preserve the reactive species and restore the bactericidal activity of FPAW. The reactive species were maintained for up to 10 days by increasing PAW pH from 3.5 to 5 or 7. At the end of the storage period, acidification restored the bactericidal activity of FPAW, significantly reducing the viable populations of Escherichia coli and Staphylococcus aureus. The highest log reduction of E. coli and S. aureus obtained were 4.46 and 3.55 log colony forming units/mL, respectively. These results supported that frozen PAW treated by pH adjustment is a potential strategy for developing effective treatment agents for fresh produce.

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References

  1. Brandt K, Christensen LP, Hansen-Møller J et al (2004) Health promoting compounds in vegetables and fruits: a systematic approach for identifying plant components with impact on human health. Trends Food Sci Technol 15:384–393. https://doi.org/10.1016/j.tifs.2003.12.003

    Article  CAS  Google Scholar 

  2. Mahajan PV, Caleb OJ, Singh Z et al (2014) Postharvest treatments of fresh produce. Philos Trans R Soc A Math Phys Eng Sci 372:20130309. https://doi.org/10.1098/rsta.2013.0309

    Article  CAS  Google Scholar 

  3. Ben-Yehoshua S, Rodov V (2002) Transpiration and water stress. In: Postharvest physiology and pathology of vegetables. CRC Press, pp 143–197

  4. Brosnan T, Sun DW (2001) Compensation for water loss in vacuum-precooled cut lily flowers. J Agric Eng Res 79:299–305. https://doi.org/10.1006/jaer.2001.0704

    Article  Google Scholar 

  5. Yoga Milani MD, Samarawickrama DS, Perera PSD et al (2020) Eco friendly packaging material from banana pseudo stem for transportation of fruits and vegetables. Acta Horticulturae. International Society for Horticultural Science (ISHS), Leuven, Belgium, pp 59–64

    Google Scholar 

  6. Rana S, Siddiqui S, Gandhi K (2018) Effect of individual vacuum and modified atmosphere packaging on shelf life of guava. Int J Chem Stud 6:966–972

    Google Scholar 

  7. Ali S, Sattar Khan A, Ullah Malik A et al (2021) Combined application of ascorbic and oxalic acids delays postharvest browning of litchi fruits under controlled atmosphere conditions. Food Chem 350:129277. https://doi.org/10.1016/j.foodchem.2021.129277

    Article  CAS  PubMed  Google Scholar 

  8. Dziedzic E, Błaszczyk J, Bieniasz M et al (2020) Effect of modified (MAP) and controlled atmosphere (CA) storage on the quality and bioactive compounds of blue honeysuckle fruits (Lonicera caerulea L.). Sci Hortic. https://doi.org/10.1016/j.scienta.2020.109226

    Article  Google Scholar 

  9. Koyuncu MA, Erbas D, Onursal CE et al (2019) Postharvest treatments of salicylic acid, oxalic acid and putrescine influences bioactive compounds and quality of pomegranate during controlled atmosphere storage. J Food Sci Technol 56:350–359. https://doi.org/10.1007/s13197-018-3495-1

    Article  CAS  PubMed  Google Scholar 

  10. Ji Y, Hu W, Liao J et al (2021) Ethanol vapor delays softening of postharvest blueberry by retarding cell wall degradation during cold storage and shelf life. Postharvest Biol Technol 177:111538. https://doi.org/10.1016/j.postharvbio.2021.111538

    Article  CAS  Google Scholar 

  11. Secretaria LB, Bayogan ERV, Photchanachai S (2021) Effect of ethanol vapor and perforations in polyethylene bags on the postharvest and antioxidant qualities of thai round green eggplant fruit. Mindanao J Sci Technol 19:65–83

    Google Scholar 

  12. Jafarzadeh S, Mohammadi Nafchi A, Salehabadi A et al (2021) Application of bio-nanocomposite films and edible coatings for extending the shelf life of fresh fruits and vegetables. Adv Colloid Interface Sci 291:102405. https://doi.org/10.1016/j.cis.2021.102405

    Article  CAS  PubMed  Google Scholar 

  13. Salehi F (2020) Edible coating of fruits and vegetables using natural gums: a review. Int J Fruit Sci 20:S570–S589. https://doi.org/10.1080/15538362.2020.1746730

    Article  Google Scholar 

  14. Sapper M, Chiralt A (2018) Starch-based coatings for preservation of fruits and vegetables. Coatings 8:1–19. https://doi.org/10.3390/coatings8050152

    Article  CAS  Google Scholar 

  15. Tahir HE, Xiaobo Z, Mahunu GK et al (2019) Recent developments in gum edible coating applications for fruits and vegetables preservation: a review. Carbohydr Polym 224:115141. https://doi.org/10.1016/j.carbpol.2019.115141

    Article  CAS  PubMed  Google Scholar 

  16. Baswal AK, Ramezanian A (2021) 1-methylcyclopropene potentials in maintaining the postharvest quality of fruits, vegetables, and ornamentals: a review. J Food Process Preserv 45:e15129. https://doi.org/10.1111/jfpp.15129

    Article  CAS  Google Scholar 

  17. Cheng S, Yu Y, Guo J et al (2020) Effect of 1-methylcyclopropene and chitosan treatment on the storage quality of jujube fruit and its related enzyme activities. Sci Hortic 265:109281. https://doi.org/10.1016/j.scienta.2020.109281

    Article  CAS  Google Scholar 

  18. Zhang J, Ma Y, Dong C et al (2020) Meta-analysis of the effects of 1-methylcyclopropene (1-MCP) treatment on climacteric fruit ripening. Hortic Res 7:208. https://doi.org/10.1038/s41438-020-00405-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Álvarez-Hernández MH, Martínez-Hernández GB, Avalos-Belmontes F et al (2020) Postharvest quality retention of apricots by using a novel sepiolite–loaded potassium permanganate ethylene scavenger. Postharvest Biol Technol 160:111061. https://doi.org/10.1016/j.postharvbio.2019.111061

    Article  CAS  Google Scholar 

  20. Mariah MAA, Vonnie JM, Erna KH et al (2022) The emergence and impact of ethylene scavengers techniques in delaying the ripening of fruits and vegetables. Membranes (Basel) 12:1–19. https://doi.org/10.3390/membranes12020117

    Article  CAS  Google Scholar 

  21. Terry LA, Ilkenhans T, Poulston S et al (2007) Development of new palladium-promoted ethylene scavenger. Postharvest Biol Technol 45:214–220. https://doi.org/10.1016/j.postharvbio.2006.11.020

    Article  CAS  Google Scholar 

  22. Wei H, Seidi F, Zhang T et al (2021) Ethylene scavengers for the preservation of fruits and vegetables: a review. Food Chem 337:127750. https://doi.org/10.1016/j.foodchem.2020.127750

    Article  CAS  PubMed  Google Scholar 

  23. Min T, Zhu Z, Sun X et al (2020) Highly efficient antifogging and antibacterial food packaging film fabricated by novel quaternary ammonium chitosan composite. Food Chem 308:125682. https://doi.org/10.1016/j.foodchem.2019.125682

    Article  CAS  PubMed  Google Scholar 

  24. Yang W, Owczarek JS, Fortunati E et al (2016) Antioxidant and antibacterial lignin nanoparticles in polyvinyl alcohol/chitosan films for active packaging. Ind Crop Prod 94:800–811. https://doi.org/10.1016/j.indcrop.2016.09.061

    Article  CAS  Google Scholar 

  25. Zhang B, Huang C, Zhang L et al (2019) Application of chlorine dioxide microcapsule sustained-release antibacterial films for preservation of mangos. J Food Sci Technol 56:1095–1103. https://doi.org/10.1007/s13197-019-03636-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Herianto S, Hou CY, Lin CM, Chen HL (2021) Nonthermal plasma-activated water: a comprehensive review of this new tool for enhanced food safety and quality. Compr Rev Food Sci Food Saf 20:583–626. https://doi.org/10.1111/1541-4337.12667

    Article  CAS  PubMed  Google Scholar 

  27. Patel AH, Sharma HP, Pal M (2021) Effect of plasma activated water (PAW) on fruits and vegetables. Am J Food Nutr 9:60–68. https://doi.org/10.12691/ajfn-9-2-1

    Article  CAS  Google Scholar 

  28. Pignata C, D’Angelo D, Fea E, Gilli G (2017) A review on microbiological decontamination of fresh produce with nonthermal plasma. J Appl Microbiol 122:1438–1455. https://doi.org/10.1111/jam.13412

    Article  CAS  PubMed  Google Scholar 

  29. Puač N, Gherardi M, Shiratani M (2018) Plasma agriculture: a rapidly emerging field. Plasma Process Polym 15:1–5. https://doi.org/10.1002/ppap.201700174

    Article  CAS  Google Scholar 

  30. Zhao YM, Patange A, Sun DW, Tiwari B (2020) Plasma-activated water: physicochemical properties, microbial inactivation mechanisms, factors influencing antimicrobial effectiveness, and applications in the food industry. Compr Rev Food Sci Food Saf 19:3951–3979. https://doi.org/10.1111/1541-4337.12644

    Article  PubMed  Google Scholar 

  31. Kutasi K, Krstulović N, Jurov A et al (2021) Controlling: the composition of plasma-activated water by Cu ions. Plasma Sources Sci Technol 30:45015. https://doi.org/10.1088/1361-6595/abf078

    Article  CAS  Google Scholar 

  32. Tsoukou E, Bourke P, Boehm D (2020) Temperature stability and effectiveness of plasma-activated liquids over an 18 months period. Water (Basel) 12:1–18. https://doi.org/10.3390/w12113021

    Article  CAS  Google Scholar 

  33. Shen J, Tian Y, Li Y et al (2016) Bactericidal effects against S. aureus and physicochemical properties of plasma activated water stored at different temperatures. Sci Rep 6:28505. https://doi.org/10.1038/srep28505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Oehmigen K, Hähnel M, Brandenburg R et al (2010) The role of acidification for antimicrobial activity of atmospheric pressure plasma in liquids. Plasma Process Polym 7:250–257. https://doi.org/10.1002/ppap.200900077

    Article  CAS  Google Scholar 

  35. Joshi I, Salvi D, Schaffner DW, Karwe MV (2018) Characterization of microbial inactivation using plasma-activated water and plasma-activated acidified buffer. J Food Prot 81:1472–1480. https://doi.org/10.4315/0362-028X.JFP-17-487

    Article  CAS  PubMed  Google Scholar 

  36. Zheng Y, Wu S, Dang J et al (2019) Reduction of phoxim pesticide residues from grapes by atmospheric pressure non-thermal air plasma activated water. J Hazard Mater 377:98–105. https://doi.org/10.1016/j.jhazmat.2019.05.058

    Article  CAS  PubMed  Google Scholar 

  37. Baga AN, Johnson GRA, Nazhat NB, Saadalla-Nazhat RA (1988) A simple spectrophotometric determination of hydrogen peroxide at low concentrations in aqueous solution. Anal Chim Acta 204:349–353. https://doi.org/10.1016/S0003-2670(00)86374-6

    Article  CAS  Google Scholar 

  38. Rathore V, Patel D, Butani S, Nema SK (2021) Investigation of physicochemical properties of plasma activated water and its bactericidal efficacy. Plasma Chem Plasma Process 41:871–902. https://doi.org/10.1007/s11090-021-10161-y

    Article  CAS  Google Scholar 

  39. Ma R, Wang G, Tian Y et al (2015) Non-thermal plasma-activated water inactivation of food-borne pathogen on fresh produce. J Hazard Mater 300:643–651. https://doi.org/10.1016/j.jhazmat.2015.07.061

    Article  CAS  PubMed  Google Scholar 

  40. Shen J, Zhang H, Xu Z et al (2019) Preferential production of reactive species and bactericidal efficacy of gas-liquid plasma discharge. Chem Eng J 362:402–412. https://doi.org/10.1016/j.cej.2019.01.018

    Article  CAS  Google Scholar 

  41. Zhou R, Zhou R, Prasad K et al (2018) Cold atmospheric plasma activated water as a prospective disinfectant: the crucial role of peroxynitrite. Green Chem 20:5276–5284. https://doi.org/10.1039/c8gc02800a

    Article  CAS  Google Scholar 

  42. Dai S, Wen T, Cai Z, Zhang J (2020) Dynamics of nitrite in acidic soil during extraction with potassium chloride studied using 15N tracing. Rapid Commun Mass Spectrom 34:e8746. https://doi.org/10.1002/rcm.8746

    Article  CAS  PubMed  Google Scholar 

  43. Shen QR, Ran W, Cao ZH (2003) Mechanisms of nitrite accumulation occurring in soilnitrification. Chemosphere 50:747–753. https://doi.org/10.1016/S0045-6535(02)00215-1

    Article  CAS  PubMed  Google Scholar 

  44. Anbar M, Taube H (1954) Interaction of nitrous acid with hydrogen peroxide and with water. J Am Chem Soc 76:6243–6247. https://doi.org/10.1021/ja01653a007

    Article  CAS  Google Scholar 

  45. Mahaseth T, Kuzminov A (2017) Potentiation of hydrogen peroxide toxicity: from catalase inhibition to stable DNA-iron complexes. Mutat Res Rev Mutat Res 773:274–281. https://doi.org/10.1016/j.mrrev.2016.08.006

    Article  CAS  PubMed  Google Scholar 

  46. Schumb WC (1949) Stability of concentrated hydrogen peroxide solutions. Ind Eng Chem 41:992–1003. https://doi.org/10.1021/ie50473a026

    Article  CAS  Google Scholar 

  47. Korachi M, Gurol C, Aslan N (2010) Atmospheric plasma discharge sterilization effects on whole cell fatty acid profiles of Escherichia coli and Staphylococcus aureus. J Electrostat 68:508–512. https://doi.org/10.1016/j.elstat.2010.06.014

    Article  CAS  Google Scholar 

  48. Alvarez B, Denicola A, Radi R (1995) Reaction between peroxynitrite and hydrogen peroxide: formation of oxygen and slowing of peroxynitrite decomposition. Chem Res Toxicol 8:859–864. https://doi.org/10.1021/tx00048a006

    Article  CAS  PubMed  Google Scholar 

  49. Ma M, Zhang Y, Lv Y, Sun F (2020) The key reactive species in the bactericidal process of plasma activated water. J Phys D Appl Phys. https://doi.org/10.1088/1361-6463/ab703a

    Article  Google Scholar 

  50. 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 Process Polym 7:33–42. https://doi.org/10.1002/ppap.200900090

    Article  CAS  Google Scholar 

  51. Brunelli L, Crow JP, Beckham JS (1995) The comparative toxicity of nitric oxide and peroxinitrite to Escherichia coli. Arch Biochem Biophys 316:327–334

    Article  CAS  PubMed  Google Scholar 

  52. Oehmigen K, Winter J, Hähnel M et al (2011) Estimation of possible mechanisms of Escherichia coli inactivation by plasma treated sodium chloride solution. Plasma Process Polym 8:904–913. https://doi.org/10.1002/ppap.201000099

    Article  CAS  Google Scholar 

  53. Traylor MJ, Pavlovich MJ, Karim S et al (2011) Long-term antibacterial efficacy of air plasma-activated water. J Phys D Appl Phys 44:472001. https://doi.org/10.1088/0022-3727/44/47/472001

    Article  CAS  Google Scholar 

  54. Lukes P, Dolezalova E, Sisrova I, Clupek M (2014) Aqueous-phase chemistry and bactericidal effects from an air discharge plasma in contact with water: evidence for the formation of peroxynitrite through a pseudo-second-order post-discharge reaction of H2O2 and HNO2. Plasma Sources Sci Technol 23:15019. https://doi.org/10.1088/0963-0252/23/1/015019

    Article  CAS  Google Scholar 

  55. Szabó C (2003) Multiple pathways of peroxynitrite cytotoxicity. Toxicol Lett 140–141:105–112. https://doi.org/10.1016/S0378-4274(02)00507-6

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank Chen Li-Hsien for advice on experimental design.

Funding

This project is financially supported by the Ministry of Science and Technology, Taiwan, under Project No. MOST 110-2221-E-029-007.

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Authors and Affiliations

  1. Department of Food Science, Tunghai University, Taichung, Taiwan R.O.C.

    Gede Arda & Chuan-liang Hsu

  2. Agricultural Engineering and Biosystem Department, Faculty of Agricultural Technology, Udayana University, Denpasar, Bali, Indonesia

    Gede Arda

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  1. Gede Arda
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GA: Writing—original draft, Investigation, Data analysis. C-LH: Conceptualization, Writing-review, Supervision.

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Correspondence to Chuan-liang Hsu.

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Arda, G., Hsu, Cl. Preservation of Reactive Species in Frozen Plasma-Activated Water and Enhancement of its Bactericidal Activity Through pH Adjustment. Plasma Chem Plasma Process 43, 599–618 (2023). https://doi.org/10.1007/s11090-023-10327-w

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