Inactivation of foodborne viruses: Opportunities for cold atmospheric plasma

Aboubakr, 2016, Inactivation of virus in solution by cold atmospheric pressure plasma: Identification of chemical inactivation pathways, Journal of Physics D: Applied Physics, 49, 10.1088/0022-3727/49/20/204001 Aboubakr, 2018, Cold argon-oxygen plasma species oxidize and disintegrate capsid protein of feline calicivirus, PLoS One, 13, 10.1371/journal.pone.0194618 Ahlfeld, 2015, Inactivation of a foodborne norovirus outbreak strain with nonthermal atmospheric pressure plasma, mBio, 6, 10.1128/mBio.02300-14 Alshraiedeh, 2013, Atmospheric pressure, nonthermal plasma inactivation of MS 2 bacteriophage: Effect of oxygen concentration on virucidal activity, Journal of Applied Microbiology, 115, 1420, 10.1111/jam.12331 Aman Mohammadi, 2021, Inactivation of viruses using nonthermal plasma in viral suspensions and foodstuff: A short review of recent studies, Journal of Food Safety, 41, 10.1111/jfs.12919 Anderson-Coughlin, 2021, Enteric viruses and pepper mild mottle virus show significant correlation in select mid-atlantic agricultural waters, Applied and Environmental Microbiology, 87, 10.1128/AEM.00211-21 Bae, 2015, Inactivation of murine norovirus-1 and hepatitis A virus on fresh meats by atmospheric pressure plasma jets, Food Research International, 76, 342, 10.1016/j.foodres.2015.06.039 Baert, 2009, Reported foodborne outbreaks due to noroviruses in Belgium: The link between food and patient investigations in an international context, Epidemiology and Infection, 137, 316, 10.1017/S0950268808001830 Bae, 2008, Evaluation of murine norovirus, feline calicivirus, poliovirus, and MS2 as surrogates for human norovirus in a model of viral persistence in surface water and groundwater, Applied and Environmental Microbiology, 74, 477, 10.1128/AEM.02095-06 Bae, 2008, Evaluation of murine norovirus, feline calicivirus, poliovirus, and MS2 as surrogates for human norovirus in a model of viral persistence in surface water and groundwater, Applied and Environmental Microbiology, 74, 477, 10.1128/AEM.02095-06 Bárdos, 2010, Cold atmospheric plasma: Sources, processes, and applications, Thin Solid Films, 518, 6705, 10.1016/j.tsf.2010.07.044 Bauer, 2019, The synergistic effect between hydrogen peroxide and nitrite, two long-lived molecular species from cold atmospheric plasma, triggers tumor cells to induce their own cell death, Redox Biology, 26, 101291, 10.1016/j.redox.2019.101291 Bekeschus, 2020, Gas plasma technology—an asset to healthcare during viral pandemics such as the COVID-19 crisis?, IEEE Transactions on Radiation and Plasma Medical Sciences, 4, 391, 10.1109/TRPMS.2020.3002658 Berger, 2010, Fresh fruit and vegetables as vehicles for the transmission of human pathogens, Environmental Microbiology, 12, 2385, 10.1111/j.1462-2920.2010.02297.x Bosch, 2018, Foodborne viruses: Detection, risk assessment, and control options in food processing, International Journal of Food Microbiology, 285, 110, 10.1016/j.ijfoodmicro.2018.06.001 Bourke, 2018, The potential of cold plasma for safe and sustainable food production, Trends in Biotechnology, 36, 615, 10.1016/j.tibtech.2017.11.001 Bozkurt, 2021, Outbreaks, occurrence, and control of norovirus and hepatitis a virus contamination in berries: A review, Critical Reviews in Food Science and Nutrition, 61, 116, 10.1080/10408398.2020.1719383 CDC National Centre for Immunization Cook, 2016, Persistence and elimination of human norovirus in food and on food contact surfaces: A critical review, Journal of Food Protection, 79, 1273, 10.4315/0362-028X.JFP-15-570 Coulepis, 1982, Biophysical and biochemical characterization of hepatitis A virus, Intervirology, 18, 107, 10.1159/000149314 D'Souza, 2009, High-pressure homogenization for the inactivation of human enteric virus surrogates, Journal of Food Protection, 72, 2418, 10.4315/0362-028X-72.11.2418 Davies, 2003, Singlet oxygen-mediated damage to proteins and its consequences, Biochemical and Biophysical Research Communications, 305, 761, 10.1016/S0006-291X(03)00817-9 Filipić, 2020, Cold plasma, a new hope in the field of virus inactivation, Trends in Biotechnology, 38, 1278, 10.1016/j.tibtech.2020.04.003 Filipić, 2019, Cold atmospheric plasma as a novel method for inactivation of potato virus Y in water samples, Food and Environmental Virology, 11, 220, 10.1007/s12560-019-09388-y Fraisse, 2011, Comparison of chlorine and peroxyacetic-based disinfectant to inactivate Feline calicivirus, Murine norovirus and Hepatitis A virus on lettuce, International Journal of Food Microbiology, 151, 98, 10.1016/j.ijfoodmicro.2011.08.011 Franck, 2015, Norovirus genotypes in hospital settings: Differences between nosocomial and community-acquired infections, The Journal of Infectious Diseases, 212, 881, 10.1093/infdis/jiv105 Fridman, 2005, Non-thermal atmospheric pressure discharges, Journal of Physics D: Applied Physics, 38, R1, 10.1088/0022-3727/38/2/R01 Gilmore, 2018, Cold plasmas for biofilm control: Opportunities and challenges, Trends in Biotechnology, 36, 627, 10.1016/j.tibtech.2018.03.007 Gracanin, 2009, Singlet-oxygen-mediated amino acid and protein oxidation: Formation of tryptophan peroxides and decomposition products, Free Radical Biology and Medicine, 47, 92, 10.1016/j.freeradbiomed.2009.04.015 Guo, 2015, Bactericidal effect of various non-thermal plasma agents and the influence of experimental conditions in microbial inactivation: A review, Food Control, 50, 482, 10.1016/j.foodcont.2014.09.037 Guo, 2018, Mechanism of virus inactivation by cold atmospheric-pressure plasma and plasma-activated water, Applied and Environmental Microbiology, 84, 10.1128/AEM.00726-18 Hall, 2012, Epidemiology of foodborne norovirus outbreaks, United States, 2001-2008, Emerging Infectious Diseases, 18, 1566, 10.3201/eid1810.120833 Hall, 2014, Vital signs: Foodborne norovirus outbreaks - United States, 2009-2012, MMWR Morb Mortal Wkly Rep, 63, 491 Hanbal, 2018, Atmospheric-pressure plasma irradiation can disrupt tobacco mosaic virus particles and RNAs to inactivate their infectivity, Archives of Virology, 163, 2835, 10.1007/s00705-018-3909-4 Han, 2016, Mechanisms of inactivation by High-Voltage atmospheric cold plasma differ for Escherichia coli and Staphylococcus aureus, Applied and Environmental Microbiology, 82, 450, 10.1128/AEM.02660-15 Han, 2020, Antimicrobial efficacy of cold plasma treatment against food-borne pathogens on various foods, Journal of Physics D: Applied Physics, 53, 10.1088/1361-6463/ab761f Hoffmann, 2012, Annual cost of illness and quality-adjusted life year losses in the United States due to 14 foodborne pathogens, Journal of Food Protection, 75, 1292, 10.4315/0362-028X.JFP-11-417 Hoffmann, 2013, Cold atmospheric plasma: Methods of production and application in dentistry and oncology, Medical Gas Research, 3, 1, 10.1186/2045-9912-3-21 Joshi, 2013, Novel disinfectants for fresh produce, Trends in Food Science & Technology, 34, 54, 10.1016/j.tifs.2013.08.008 Keeffe, 1995, Is hepatitis A more severe in patients with chronic hepatitis B and other chronic liver diseases?, American Journal of Gastroenterology, 90, 201 Kim, 1980, Mechanism of ozone inactivation of bacteriophage f2, Applied and Environmental Microbiology, 39, 210, 10.1128/aem.39.1.210-218.1980 Kniel, 2014, The makings of a good human norovirus surrogate, Current Opinion Virology, 4, 85, 10.1016/j.coviro.2014.01.002 Koff, 1992, Clinical manifestations and diagnosis OF hepatitis-a virus-infection, Vaccine, 10, S15, 10.1016/0264-410X(92)90533-P Lacombe, 2017, Nonthermal inactivation of norovirus surrogates on blueberries using atmospheric cold plasma, Food Microbiology, 63, 1, 10.1016/j.fm.2016.10.030 Laroussi, 1996, Sterilization of contaminated matter with an atmospheric pressure plasma, IEEE Transactions on Plasma Science, 24, 1188, 10.1109/27.533129 Lee, 2020, Evaluation of in-package atmospheric dielectric barrier discharge cold plasma treatment as an intervention technology for decontaminating bulk ready-to-eat chicken breast cubes in plastic containers, Applied Sciences, 10, 6301, 10.3390/app10186301 Liao, 2017, Inactivation mechanisms of non-thermal plasma on microbes: A review, Food Control, 75, 83, 10.1016/j.foodcont.2016.12.021 Lieberman, 2005 Li, 2022, Insights into amoxicillin degradation in water by non-thermal plasmas, Chemosphere, 291, 10.1016/j.chemosphere.2021.132757 Li, 2015, A novel microbial source tracking microarray for pathogen detection and fecal source identification in environmental systems, Environmental Science and Technology, 49, 7319, 10.1021/acs.est.5b00980 Lukes, 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 Science and Technology, 23, 10.1088/0963-0252/23/1/015019 Mai-Prochnow, 2014, Atmospheric pressure plasmas: Infection control and bacterial responses, International Journal of Antimicrobial Agents, 43, 508, 10.1016/j.ijantimicag.2014.01.025 Mai-Prochnow, 2021, Interactions of plasma-activated water with biofilms: Inactivation, dispersal effects and mechanisms of action, Npj Biofilms and Microbiomes, 7, 11, 10.1038/s41522-020-00180-6 Mangen, 2015, Cost-of-illness and disease burden of food-related pathogens in The Netherlands, 2011, International Journal of Food Microbiology, 196, 84, 10.1016/j.ijfoodmicro.2014.11.022 Mangen, 2013 Min, 2016, Dielectric barrier discharge atmospheric cold plasma inhibits Escherichia coli O157: H7, Salmonella, Listeria monocytogenes, and Tulane virus in romaine lettuce, International Journal of Food Microbiology, 237, 114, 10.1016/j.ijfoodmicro.2016.08.025 Miranda, 2018, Farm to fork quantitative microbial risk assessment for norovirus on frozen strawberries, Microbial Risk Analysis, 10, 44, 10.1016/j.mran.2018.06.002 Mir, 2020, Promising applications of cold plasma for microbial safety, chemical decontamination and quality enhancement in fruits, Journal of Applied Microbiology, 129, 474, 10.1111/jam.14541 Misra, 2015, The effects of nonthermal plasma on chemical quality of strawberries, Postharvest Biology and Technology, 110, 197, 10.1016/j.postharvbio.2015.08.023 Mohamed, 2021, Non-thermal plasma as a novel strategy for treating or preventing viral infection and associated disease, Frontiers in Physics, 9, 10.3389/fphy.2021.683118 Moldgy, 2020, Inactivation of virus and bacteria using cold atmospheric pressure air plasmas and the role of reactive nitrogen species, Journal of Physics D Applied Physics, 53, 12, 10.1088/1361-6463/aba066 Nayak, 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 Processes and Polymers, 15, 10.1002/ppap.201700119 Nguyen, 2017, A systematic review and meta-analysis of the prevalence of norovirus in cases of gastroenteritis in developing countries, Medicine (Baltimore), 96, 10.1097/MD.0000000000008139 Niemira, 2012, Cold plasma decontamination of foods, Annual Review of Food Science and Technology, 3, 125, 10.1146/annurev-food-022811-101132 Niemira, 2014, Cold plasma rapid decontamination of food contact surfaces contaminated with Salmonella biofilms, Journal of Food Science, 79, M917, 10.1111/1750-3841.12379 Niemira, 2011, Nonthermal plasma as a novel food processing technology, Nonthermal Processing Technologies for Food, 272 Organization, 2003 Pankaj, 2018, Effects of cold plasma on food quality: A review, Foods, 7, 10.3390/foods7010004 Parvulescu, 2012 Perucca, 2010, 1 Pignata, 2017, A review on microbiological decontamination of fresh produce with nonthermal plasma, Journal of Applied Microbiology, 122, 1438, 10.1111/jam.13412 Ponraj, 2017, Argon gas plasma to decontaminate and extend shelf life of milk, Plasma Processes and Polymers, 14, 10.1002/ppap.201600242 Qadri, 2015, Fresh-cut fruits and vegetables: Critical factors influencing microbiology and novel approaches to prevent microbial risks—a review, Cogent Food & Agriculture, 1, 10.1080/23311932.2015.1121606 Rachmadi, 2020, Required chlorination doses to fulfill the credit value for disinfection of enteric viruses in water: A critical review, Environmental Science and Technology, 54, 2068, 10.1021/acs.est.9b01685 Ragaert, 2004, Consumer perception and choice of minimally processed vegetables and packaged fruits, Food Quality and Preference, 15, 259, 10.1016/S0950-3293(03)00066-1 Rekhy, 2014, Promoting consumption of fruit and vegetables for better health. Have campaigns delivered on the goals?, Appetite, 79, 113, 10.1016/j.appet.2014.04.012 Roh, 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, 127, 10.1016/j.lwt.2020.109429 Roos, 2020, Water and pathogenic viruses inactivation—food engineering perspectives, Food Engineering Reviews, 12, 251, 10.1007/s12393-020-09234-z Roualdes, 2017, 1.10 plasma membranes, Comprehensive Membrane Science and Engineering, 236, 10.1016/B978-0-12-409547-2.12224-3 Sakudo, 2014, N2 gas plasma inactivates influenza virus mediated by oxidative stress, Frontiers in Bioscience, 6, 69, 10.2741/E692 Sakudo, 2016, Nitrogen gas plasma generated by a static induction thyristor as a pulsed power supply inactivates adenovirus, PLoS One, 11, 10.1371/journal.pone.0157922 Sakudo, 2019, Disinfection and sterilization using plasma technology: Fundamentals and future perspectives for biological applications, International Journal of Molecular Sciences, 20, 5216, 10.3390/ijms20205216 Sánchez, 2016, Survival of enteric viruses in the environment and food, Viruses in Foods, 367, 10.1007/978-3-319-30723-7_13 Sarangapani, 2018, Recent advances in the application of cold plasma technology in foods, Annual Review of Food Science and Technology, 9, 609, 10.1146/annurev-food-030117-012517 Scallan, 2011, Foodborne illness acquired in the United States--major pathogens, Emerging Infectious Diseases, 17, 7, 10.3201/eid1701.P11101 Scharff, 2015, State estimates for the annual cost of foodborne illness, Journal of Food Protection, 78, 1064, 10.4315/0362-028X.JFP-14-505 Shen, 2019, Preferential production of reactive species and bactericidal efficacy of gas-liquid plasma discharge, Chemical Engineering Journal, 362, 402, 10.1016/j.cej.2019.01.018 Su, X., Tian, Y., Zhou, H., Li, Y., Zhang, Z., Jiang, B., Yang, B., Zhang, J. & Fang, J. (2018). Inactivation efficacy of nonthermal plasma-activated solutions against Newcastle disease virus. Applied and Environmental Microbiology, 84(9), e02836-17. Tabares, 2021, Cold plasma systems and their application in surface treatments for medicine, Molecules, 26, 1903, 10.3390/molecules26071903 Tendero, 2006, Atmospheric pressure plasmas: A review, Spectrochimica Acta Part B: Atomic Spectroscopy, 61, 2, 10.1016/j.sab.2005.10.003 Teunis, 2015, Shedding of norovirus in symptomatic and asymptomatic infections, Epidemiology and Infection, 143, 1710, 10.1017/S095026881400274X Thirumdas, 2015, Cold plasma: A novel non-thermal technology for food processing, Food Biophysics, 10, 1, 10.1007/s11483-014-9382-z Todd, 2007, Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 2. Description of outbreaks by size, severity, and settings, Journal of Food Protection, 70, 1975, 10.4315/0362-028X-70.8.1975 Todd, 2007, Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 3. Factors contributing to outbreaks and description of outbreak categories, Journal of Food Protection, 70, 2199, 10.4315/0362-028X-70.9.2199 Torii, 2020, Inactivation kinetics of waterborne virus by ozone determined by a continuous quench flow system, Water Research, 186, 116291, 10.1016/j.watres.2020.116291 Uyttendaele, 2015, Microbial hazards in irrigation water: Standards, norms, and testing to manage use of water in fresh produce primary production, Comprehensive Reviews in Food Science and Food Safety, 14, 336, 10.1111/1541-4337.12133 Van de Velde, 2016, Optimization of strawberry disinfection by fogging of a mixture of peracetic acid and hydrogen peroxide based on microbial reduction, color and phytochemicals retention, Food Science and Technology International, 22, 485, 10.1177/1082013215625696 Velebit, 2015, Transmission of common foodborne viruses by meat products, 58th International Meat Industry Conference (Meatcon2015), 5, 304 Wang, 2016, Non-thermal plasma for inactivated-vaccine preparation, Vaccine, 34, 1126, 10.1016/j.vaccine.2015.10.099 Wende, 2015, Identification of the biologically active liquid chemistry induced by a nonthermal atmospheric pressure plasma jet, Biointerphases, 10, 10.1116/1.4919710 Who, 2015 2008 Wu, 2015, MS2 virus inactivation by atmospheric-pressure cold plasma using different gas carriers and power levels, Applied and Environmental Microbiology, 81, 996, 10.1128/AEM.03322-14 Yadav, 2020, In-package atmospheric cold plasma inactivation of Salmonella in freeze-dried pet foods: Effect of inoculum population, water activity, and storage, Innovative Food Science & Emerging Technologies, 66, 10.1016/j.ifset.2020.102543 Yamashiro, 2018, Key role of singlet oxygen and peroxynitrite in viral RNA damage during virucidal effect of plasma torch on feline calicivirus, Scientific Reports, 8, 1, 10.1038/s41598-018-36779-1 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 and Polymers, 7(3‐4), 301-308. Yeargin, 2019, Key characteristics of foods with an elevated risk for viral enteropathogen contamination, Journal of Applied Microbiology, 126, 996, 10.1111/jam.14113 Yong, 2018, Mechanism underlying green discolouration of myoglobin induced by atmospheric pressure plasma, Scientific Reports, 8, 10.1038/s41598-018-28096-4 Zhang, 2021, Degradation of cefixime antibiotic in water by atmospheric plasma bubbles: Performance, degradation pathways and toxicity evaluation, Chemical Engineering Journal, 421 Zhang, 2018, Quantification of plasma produced OH radical density for water sterilization, Plasma Processes and Polymers, 15, 10.1002/ppap.201700241 Zhou, 2019, Atmospheric-pressure plasma treated water for seed germination and seedling growth of mung bean and its sterilization effect on mung bean sprouts, Innovative Food Science & Emerging Technologies, 53, 36, 10.1016/j.ifset.2018.08.006 Zhou, 2022, In-package plasma: From reactive chemistry to innovative food preservation technologies, Trends in Food Science & Technology, 120, 59, 10.1016/j.tifs.2021.12.032 Zhou, 2021, Sustainable plasma-catalytic bubbles for hydrogen peroxide synthesis, Green Chemistry, 23, 2977, 10.1039/D1GC00198A Zhou, 2020, Surface plasma discharges for the preservation of fresh-cut apples: Microbial inactivation and quality attributes, Journal of Physics D: Applied Physics, 53, 10.1088/1361-6463/ab6f8f Zhou, 2018, Cold atmospheric plasma activated water as a prospective disinfectant: the crucial role of peroxynitrite, Green Chemistry, 20, 5276, 10.1039/C8GC02800A Zhou, 2019, Microplasma bubbles: Reactive vehicles for biofilm dispersal, ACS Applied Materials & Interfaces, 11, 20660, 10.1021/acsami.9b03961 Zhou, 2020, Plasma-activated water: Generation, origin of reactive species and biological applications, Journal of Physics D: Applied Physics, 53, 10.1088/1361-6463/ab81cf Ziuzina, 2015, Cold plasma inactivation of internalised bacteria and biofilms for Salmonella enterica serovar Typhimurium, Listeria monocytogenes and Escherichia coli, International Journal of Food Microbiology, 210, 53, 10.1016/j.ijfoodmicro.2015.05.019