Inactivation of foodborne viruses by the cold plasma technology

PDF
Published: Apr 29, 2022
DOI: https://doi.org/10.12681/jhvms.25327
Keywords:
Cold plasma foodborne viruses novel food processing technologies
Andreana Pexara
DVM, PhD, Assistant Professor, Laboratory of Hygiene of Food of Animal Origin, Faculty of Veterinary Science, University of Thessaly, Greece
Abstract

Cold plasma (CP) is an innovative non-thermal food processing method. CP refers to a partially or completely ionized gas containing reactive chemical species, which are active against microorganisms, including viruses or enzymes of foods. CP has a minimal effect on the quality attributes of foods and can also elongate the shelf life of foods. Foodborne outbreaks caused by viruses have been increased in various countries in recent years. The research works on the inactivation effect of CP against viruses including foodborne viruses have been also increased in recent years. The most important foodborne viruses are human norovirus (HuNoV) and hepatitis A virus (HAV), involved in several outbreaks worldwide. Human astrovirus (HAstV), human adenovirus (HuAdV), Aichi virus (AiV), sapovirus (SaV) and enterovirus (EV) are also notable foodborne viruses and were associated in sporadic cases. The CP treatment proved efficient for the inactivation of foodborne viruses such as HuNoV and HAV. The present work reviews the CP as a non-thermal food processing technology and present the published data on the effect of CP process on foodborne viruses in foods.

Article Details
  • Section
  • Review Articles
Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

Authors who publish with this journal agree to the following terms:

· Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution Non-Commercial License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.

· Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g. post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.

· Authors are permitted and encouraged to post their work online (preferably in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.

Downloads
Download data is not yet available.
References
Aadil RH, Roobab U, Mann AA (2019) Effect of Heat on Food Properties. In: Encyclopedia of Food Chemistry, Melton L, Shahidi F, Varelis P (Eds.), Elsevier, Amsterdam, Netherlands: pp 70-75.
Aboubakr HA, Mor SK, Higgins L, Armien A, Youssef MM, Bruggeman PJ, Goyal SM (2018) Cold argon-oxygen plasma species oxidize and disintegrate capsid protein of feline calicivirus. PLoS One 13:e0194618.
Aboubakr HA, Williams P, Gangal U, Youssef MM, El-Sohaimy SAA, Bruggeman PJ, Goyal SM (2015) Virucidal effect of cold atmospheric gaseous plasma on feline calicivirus, a surrogate for human norovirus. Appl Environ Microbiol 81:3612–3622.
Aboubakr, HA, Gangal U, Youssef MM, Goyal SM, Bruggeman PJ (2016) Inactivation of virus in solution by cold atmospheric pressure plasma: identification of chemical inactivation pathways. J Phys D Appl Phys 49:1–17.
Adefisoye MA, Nwodo UU, Green E, Okoh AI (2016) Quantitative PCR detection and characterisation of human adenovirus, rotavirus and hepatitis A virus in discharged effluents of two wastewater treatment facilities in the Eastern Cape, South Africa. Food Environ Virol 8:262-274.
Ahlfeld B, Li Y, Boulaaba A, Binder A, Schotte U, Zimmermann JL, Morfill G, Klein G (2015) Inactivation of a foodborne norovirus outbreak strain with nonthermal atmospheric pressure plasma. MBio 6(1):e02300–e02314.
Almeida FDL, Cavalcante RS, Cullen PJ, Frias J, Bourke P, Fernandes FAN, Rodrigues S (2015) Effectsof atmospheric cold plasma and ozone on prebiotic orange juice. Innov Food Sci Emerg Technol 32:127–135.
Almeida FDL, Cavalcante RS, Cullen PJ, Frias JM, Bourke P, Fernandes FA, Rodrigues S (2015) Effects of atmospheric cold plasma and ozone on prebiotic orange juice. Innov Food Sci Emerg Technol 32:127–135.
Alshraiedeh NH, Alkawareek MY, Gorman SP, Graham WG, Gilmore BF (2013) Atmospheric pressure, nonthermal plasma inactivation of MS2 bacteriophage: effect of oxygen concentration on virucidal activity. J Appl Microbiol 115:1420–1426.
Apostol L, Georgescu N, Vatuiu I, Gaceu G (2015) Egg surface decontamination by using high voltage pulsed, cold atmospheric plasma jets. Journal of Eco Agri Tourism11:45–47.
Bae S-C, Park SY, Choe W, Ha S-D (2015) Inactivation of murine norovirus-1 and hepatitis A virus on fresh meats by atmospheric pressure plasma jets. Food Res Int 76: 342–347.
Bourke P, Ziuzina D, Han L, Cullen PJ, Gilmore BF (2017) Microbiological interactions with cold plasma. J Appl Microbiol 123(2):308–324.
Chizoba Ekezie F-G, Sun DW, Cheng JH (2017) A review on recent advances in cold plasma technology for the food industry: current applications and future trends. Trends Food Sci Technol 69:46–58.
EC (European Commission) (2014) Plasma gas technique as electronic preservation practice of organic food and feed, EGTOP/2014, Directorate-General for Agriculture and Rural Development, Directorate, B. Multilateral relations, quality policy, B.4. Organics, Expert Group for Technical Advice on Organic Production EGTOP, Final Report on Food (III). Available online: https://ec.europa.eu/agriculture/organic/sites/orgfarming/files/docs/body/egtop-final-report-food-iii_en.pdf/ [accessed 15 May 2020].
Filipić A, Gutierrez-Aguirre I, Primc G, Mozetič M, Dobnik D (2020) Cold plasma, a new hope in the field of virus inactivation. Trends Biotechnol 38:1278-1291.
Fröhling A, Durek J, Schnabel U, Ehlbeck J, Bolling J, Schlüter O (2012) Indirect plasma treatment of fresh pork: Decontamination efficiency and effects on quality attributes. Innov Food Sci Emerg Technol 16:381–390.
Gavahian M, Cullen PJ (2020) Cold Plasma as an Emerging Technique for Mycotoxin-Free Food: Efficacy, Mechanisms, and Trends. Food Rev Int 36(2):193-214.
Gavahian M, Khaneghah AM (2020) Cold plasma as a tool for the elimination of food contaminants: Recent advances and future trends. Crit Rev Food Sci Nutr 60(9):1581-1592.
Guo J, Huang K, Wang J (2015) Bactericidal effect of various non‐thermal plasma agents and the influence of experimental conditions in microbial inactivation: a review. Food Control 50:482–490.
Guo L, Xu R, Gou L, Liu Z, Zhao Y, Liu D, Zhang L, Chen H, Kong M (2018) Mechanism of virus inactivation by cold atmospheric pressure plasma and plasma-activated water. Appl Environ Microbiol 84:1–10.
Han Y, Cheng J-H, Sun D-W (2019) Activities and conformation changes of food enzymes induced by cold plasma: A review. Crit Rev Food Sci Nutr 59(5):794-811.
Kim H-J, Yong HI, ParkS, ChoeW, JoC (2013) Effects of dielectric barrier discharge plasma on pathogen inactivation and the physicochemical and sensory characteristics of pork loin. Curr Appl Phys 13:1420–1425.
King NJ, Hewitt J, Perchec‐Merien A‐M (2018) Hiding in plain sight? It's time to investigate other possible transmission routes for hepatitis E virus (HEV) in developed countries. Food Environ Virol 10:225–252.
Lacombe A, Niemira BA, Gurtler JB, Sites J, Boyd G, Kingsley DH, Li X, Chen H. (2017) Nonthermal inactivation of norovirus surrogates on blueberries using atmospheric cold plasma. Food Microbiol 63:1–5.
Lee J, Lee CW, Yong HI, Lee HJ, Jo C, JungS (2017) Use of Atmospheric Pressure Cold Plasma for Meat Industry. Korean J Food Sci Anim Resour 37:477-485.
Lee KH, Kim H-J, Woo KS JC, Kim J-K, KimSH, Park HY, Oh S-K, KimWH (2016) Evaluation of cold plasma treatments for improved microbial and physicochemical qualities of brown rice. LWT-Food Sci Technol 73:442–447.
Lee KH, Kim H-J, Yun S-W, Jo C, Kim J-K, Kim SH, Park HY, Oh S-K, Kim WH, (2016) Evaluation of cold plasma treatments for improved microbial and physicochemical qualities of brown rice. LWT 73:442–447.
Liao X, Liu D, Xiang Q, Ahn J, Chen S, Ye X, Ding T (2017) Inactivation mechanisms of non-thermal plasma on microbes: A review. Food Control 75:83–91.
López M, Calvo T, Prieto M, Múgica-Vidal R, Muro-Fraguas I, Alba-Elías F, Alvarez-Ordóñez A (2019) A Review on Non-thermal Atmospheric Plasma for Food Preservation: Mode of Action, Determinants of Effectiveness, and Applications. Front Microbiol 10:622.
Misra N, Jo C (2017) Applications of cold plasma technology for microbiological safety in meat industry. Trends Food Sci Technol 64:74–86.
Misra NN, Pankaj SK, Segat A, Ishikawa K (2016) Cold plasma interactions with enzymes in foods and model systems. Trends Food Sci Tech 55:39–47.
Misra NN, Pankaj SK,Segat A, Ishikawa K (2016) Cold plasma interactions with enzymes in foods and model systems. Trends Food Sci Tech 55:39–47.
Moisan M, Barbeau J, Crevier M-C, Pelletier J, Philip N, Saoudi B (2002) Plasma sterilization. Methods andmechanisms. Pure Appl Chem 74:349–358.
Nayak G, Aboubakr HA, Goyal SM, Bruggeman PJ (2018) Reactive species responsible for the inactivation of feline calicivirus by a two-dimensional array of integrated coaxial microhollow dielectric barrier discharges in air. Plasma Process Polym 15:1–12.
Niedźwiedź I, Waśko A, Pawłat J, Polak-Berecka M (2019) The State of Research on Antimicrobial Activity of Cold Plasma. Pol J Microbiol 68(2):153–164.
Pankaj SK, Wan Z, Keener KM (2018) Effects of Cold Plasma on Food Quality: A Review. Foods 7(1):4.
Petrescu DC, Vermeir I, Petrescu-Mag RM (2020) Consumer Understanding of Food Quality, Healthiness, and Environmental Impact: A Cross-National Perspective. Int J EnvironRes Public Health 17:169.
Pexara A and Govaris A (2020) Foodborne viruses and Innovative Non-Thermal Food-Processing Technologies. Foods 9:1520.
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.
Pires SM, Fischer‐Walker CL, Lanata CF, Devleesschauwer B, Hall AJ, Kirk MD, Duarte AS, Black RE, Angulo FJ (2015) Aetiology‐specific estimates of the global and regional incidence and mortality of diarrhoeal diseases commonly transmitted through food. PLoS ONE 10:e0142927.
Pradeep P and Chulkyoon M (2016) Review Paper: Non-thermal plasmas (NTPs) for inactivation of viruses in abiotic environment. Res J Biotechnol 11(6):91-86.
Rajvanshi AK (2008) Irving Langmuir – A Pioneering Industrial Physical Chemist. Resonance 13(7):619–626.
Roh SH, Oh YJ, Lee SY, Kang JH, Min SC (2020) Inactivation of Escherichia coli O157:H7, Salmonella, Listeria monocytogenes, and Tulane virus in processed chicken breast via atmospheric in-package cold plasma treatment. LWT - Food Sci Techn 127:109429.
Sakudo A, Toyokawa Y, Imanishi Y (2016) Nitrogen gas plasma generated by a static induction thyristor as a pulsed power supply inactivates adenovirus. PLoS One 11:e0157922.
Sánchez G, Bosch A (2016) Survival of Enteric Viruses in the Environment and Food. Viruses in Foods 26:367–392.
Scholtz V, Pazlarova J, Souskova H, Khun J, Julak J (2015) Nonthermal plasma – a tool for decontamination and disinfection. Biotechnol Adv 33:1108–1119.
Surowsky B, Schluter O, Knorr D (2015) Interactions of non-thermal atmospheric pressure plasma with solid and liquid food systems: a review. Food Eng Rev 7:82–108.
Takamatsu T, Uehara K, Sasaki Y, Hidekazu M, Matsumura Y, Iwasawa A, Norihiko Ito N, Kohno M, Azuma T, Okino A (2015) Microbial inactivation in the liquid phase induced by multigas plasma jet. PLoS One 10:e0132381.
Thirumdas R, Saragapani C, Ajinkya M, Deshmukh R, Annapure U (2016) Influence of low-pressure cold plasma on cooking and textural properties of brown rice. Innov Food Sci Emerg Technol 37:53–60.
Varilla C, Marcone M, Anno GA (2020) Potential of Cold Plasma Technology in Ensuring theSafety of Foods and Agricultural Produce: A Review. Foods 9:1435.
WuY, Liang Y, Wei K, Li W, Yao M, Zhang J, Grinshpun SA (2015) MS2 virus inactivation by atmospheric-pressure cold plasma using different gas carriers and power levels. Appl Environ Microbiol 81:996–1002.
Xia T, Kleinheksel A, Lee EM, Qiao Z, Wigginton KR, Clack HL (2019) Inactivation of airborne viruses using a packed bed nonthermal plasma reactor. J Phys D Appl Phys 52:255201.
Yamashiro R, Misawa T, Sakudo A (2018) Key role of singlet oxygen and peroxynitrite in viral RNA damage during virucidal effect of plasma torch on feline calicivirus. Sci Rep 8:17947.
Yasuda H, Miura T, Kurita H, Takashima K, Mizuno A (2010) Biological evaluation of DNA damage in bacteriophages inactivated by atmospheric pressure cold plasma. Plasma Processes Polym 7:301–308.
Yeargin T, Gibson KE (2019) Key characteristics of foods with an elevated risk for viral enteropathogen contamination. J Appl Microbiol 126(4):995-1301.
Yong HI, Lee SH, Kim SY, Park S, Park J, ChoeW, Jo C (2017) Color development, physiochemical properties, and microbiological safety of pork jerky processed with atmospheric pressure plasma. Innov Food Sci Emerg Technol 53:78-84.
Zhang Y, Qu S, Xu L (2019) Progress in the study of virus detection methods: the possibility of alternative methods to validate virus inactivation. Biotechnol Bioeng 116:2095–2102.
Zimmermann JL, Dumler K, Shimizu T, Morfill GE, Wolf A, Boxhammer V, J Schlegel J, Gansbacher B, Anton M (2011) Effects of cold atmospheric plasmas on adenoviruses in solution. J Phys D Appl Phys 44:505201.