Abstract
Global food production sustainability and the demand for fresh and nutritious food necessitate the development of novel technologies to provide food with a long shelf life. Hurdle technologies combing several interventions can ensure microbial safety without inducing notable changes to food quality. Cold plasma, as a promising nonthermal technology, has increasingly attracted attention in food industry. Recently, cold plasma–based hurdles have been proposed as novel intervention strategies for microbial decontamination. This review summarizes currently existing cold plasma–based hurdle strategies, including thermal treatment and nonthermal techniques (e.g., organic acids, essential oils, ultrasound) that have been reported in the literature. In addition, we highlight some critical issues, including the microbial stress response, the processing parameters, and the effects on food quality, that need to be taken into account during the optimization and implementation of cold plasma–based hurdles. Cold plasma–based hurdles overcome certain limitations of individual cold plasma treatment to improve the inactivation efficacy and retain the maximum food quality attributes.
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Augustin MA, Riley M, Stockmann R, Bennett L, Kahl A, Lockett T, Osmond M, Sanguansri P, Stonehouse W, Zajac I, Cobiac L (2016) Role of food processing in food and nutrition security. Trends Food Sci Technol 56:115–125
Arroyo C, Lyng JG (2017) Pulsed electric fields in hurdle approaches for microbial inactivation. Handbook of electroporation. Springer International, Berlin, Germany, pp 1–30
Berdejo D, Pagán E, García-Gonzalo D, Pagán R (2019) Exploiting the synergism among physical and chemical processes for improving food safety. Curr Opin Food Sci 30:14–20
Belletti N, Kamdem SS, Tabanelli G, Lanciotti R, Gardini F (2010) Modeling of combined effects of citral, linalool and β-pinene used against Saccharomyces cerevisiae in citrus-based beverages subjected to a mild heat treatment. Int J Food Microbiol 136(3):283–289
Butscher D, Zimmermann D, Schuppler M, von Rohr PR (2016) Plasma inactivation of bacterial endospores on wheat grains and polymeric model substrates in a dielectric barrier discharge. Food Control 60:636–645
Bourke P, Ziuzina D, Boehm D, Cullen PJ, Keener K (2018) The potential of cold plasma for safe and sustainable food production. Trends Biotechnol 36(6):615–626
Bigwood T, Hudson J, Billington C, Carey-Smith G, Heinemann J (2008) Phage inactivation of foodborne pathogens on cooked and raw meat. Food Microbiol 25(2):400–406
Bergholz TM, Tang SL, Wiedmann M, Boor KJ (2013) Nisin resistance of Listeria monocytogenes is increased by exposure to salt stress and is mediated via LiaR. Appl Environ Microbiol 79(18):5682–5688
Calvo T, Álvarez-Ordóñez A, Prieto M, González-Raurich M, López M (2016) Influence of processing parameters and stress adaptation on the inactivation of Listeria monocytogenes by non-thermal atmospheric plasma (NTAP). Food Res Int 89:631–637
Calvo T, Alvarezordóñez A, Prieto M, Bernardo A, López M (2017) Stress adaptation has a minor impact on the effectivity of non-thermal atmospheric plasma (NTAP) against Salmonella spp. Food Res Int 102:519–525
Calo JR, Crandall PG, O'Bryan CA, Ricke SC (2015) Essential oils as antimicrobials in food systems – a review. Food Control 54:111–119
Chaplot S, Yadav B, Jeon B, Roopesh M (2019) Atmospheric cold plasma and peracetic acid–based hurdle intervention to reduce Salmonella on raw poultry meat. J Food Prot 82(5):878–888
Cheon HL, Shin JY, Park KH, Chung MS, Kang DH (2015) Inactivation of foodborne pathogens in powdered red pepper (Capsicum annuum L) using combined UV-C irradiation and mild heat treatment. Food Control 50:441–445
Choi EJ, Park HW, Kim SB, Ryu S, Lim J, Hong EJ, Byeon YS, Chun HH (2019) Sequential application of plasma-activated water and mild heating improves microbiological quality of ready-to-use shredded salted kimchi cabbage (Brassica pekinensis L). Food Control 98:501–509
Cui H, Ma C, Lin L (2016a) Synergetic antibacterial efficacy of cold nitrogen plasma and clove oil against Escherichia coli O157: H7 biofilms on lettuce. Food Control 66:8–16
Cui H, Li W, Li C, Lin L (2016b) Synergistic effect between Helichrysum italicum essential oil and cold nitrogen plasma against Staphylococcus aureus biofilms on different food-contact surfaces. Int J Food Sci Technol 51(11):2493–2501
Cui H, Wu J, Li C, Lin L (2017) Promoting anti-listeria activity of lemongrass oil on pork loin by cold nitrogen plasma assist. J Food Saf 37(2):e12316
Cui H, Bai M, Yuan L, Surendhiran D, Lin L (2018) Sequential effect of phages and cold nitrogen plasma against Escherichia coli O157: H7 biofilms on different vegetables. Int J Food Microbiol 268:1–9
Chen C, Lee H, Chen S, Chen H, Chang M (2009) Ultrasound-assisted plasma: a novel technique for inactivation of aquatic microorganisms. Environ Sci Technol 43(12):4493–4497
Ding T, Oh DH, Liu D (2019) Electrolyzed water in food: fundamentals and applications. Springer, Singapore
Durán N, Marcato PD (2013) Nanobiotechnology perspectives. Role of nanotechnology in the food industry: a review. Int J Food Sci Technol 48(6):1127–1134
Echegoyen Y, Nerín C (2015) Performance of an active paper based on cinnamon essential oil in mushrooms quality. Food Chem 170:30–36
Fernández A, Noriega E, Thompson A (2013) Inactivation of Salmonella enterica serovar Typhimurium on fresh produce by cold atmospheric gas plasma technology. Food Microbiol 33(1):24–29
Flores MJ, Lescano MR, Brandi RJ, Cassano AE, Labas MD (2013) A novel approach to explain the inactivation mechanism of Escherichia coli employing a commercially available peracetic acid. Water Sci Technol 69(2):358–363
Georgescu N, Apostol L, Gherendi F (2017) Inactivation of Salmonella enterica serovar Typhimurium on egg surface, by direct and indirect treatments with cold atmospheric plasma. Food Control 76:52–61
Govaert M, Smet C, Verheyen D, Walsh JL, Van Impe JFM (2019) Combined effect of cold atmospheric plasma and hydrogen peroxide treatment on mature Listeria monocytogenes and Salmonella Typhimurium biofilms. Front Microbiol 10:2674
Gurol C, Ekinci FY, Aslan N, Korachi M (2012) Low temperature plasma for decontamination of E. coli in milk. Int J Food Microbiol 157:1–5
He Z, Liu K, Manaloto E, Casey A, Cribaro GP, Byrne HJ, Tian F, Barcia C, Conway GE, Cullen PJ, Curtin JF (2018) Cold atmospheric plasma induces ATP-dependent endocytosis of nanoparticles and synergistic u373mg cancer cell death. Sci Rep-UK 8(1):5298
Helgadóttir S, Pandit S, Mokkapati VR, Westerlund F, Apell P, Mijakovic I (2017) Vitamin C pretreatment enhances the antibacterial effect of cold atmospheric plasma. Front Cell Infect Microbiol 7:43
Hertwig C, Reineke K, Ehlbeck J, Knorr D, Schlüter O (2015) Decontamination of whole black pepper using different cold atmospheric pressure plasma applications. Food Control 55:221–229
Huang C, Hung Y, Weng Y, Chen W, Lai Y (2019) Sustainable development of carbon nanodots technology: natural products as a carbon source and applications to food safety. Trends Food Sci Technol 86:144–152
Kim GC, Kim GJ, Park SR, Jeon SM, Seo HJ, Iza F, Lee JK (2008) Air plasma coupled with antibody-conjugated nanoparticles: a new weapon against cancer. J Phys D Appl Phys 42(3):032005
Kim HJ, Yong HI, Park S, Choe W, Jo C (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
Kohli G, Jain G, Bisht A, Upadhyay A, Kumar A, Dabir S (2019) Effect of non-thermal hurdles in shelf life enhancement of sugarcane juice. LWT Food Sci Technol 112:108233
Koide S, Shitanda D, Note M, Cao W (2011) Effects of mildly heated, slightly acidic electrolyzed water on the disinfection and physicochemical properties of sliced carrot. Food Control 22(3–4):452–456
Leistner L (1994) Further developments in the utilization of hurdle technology for food preservation. J Food Eng 22:421–432
Li J, Cheng H, Liao X, Liu D, Xiang Q, Wang J, Chen S, Ye X, Ding T (2019a) Inactivation of Bacillus subtilis and quality assurance in Chinese bayberry (Myrica rubra) juice with ultrasound and mild heat. LWT Food Sci Technol 108:113–119
Li J, Wang J, Zhao X, Wang W, Liu D, Chen S, Ye X, Ding T (2019b) Inactivation of Staphylococcus aureus and Escherichia coli in milk by different processing sequences of ultrasound and heat. J Food Saf 39(2):e12614
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
Liao X, Li J, Muhammad AI, Suo Y, Chen S, Ye X, Liu D, Ding T (2018a) Application of a dielectric barrier discharge atmospheric cold plasma (DBD-ACP) for Eshcerichia coli inactivation in apple juice. J Food Sci 83(2):401–408
Liao X, Su Y, Liu D, Chen S, Hu Y, Ye X, Wang J, Ding T (2018b) Application of atmospheric cold plasma-activated water (PAW) ice for preservation of shrimps (Metapenaeus ensis). Food Control 94:307–314
Liao X, Li J, Muhammad AI, Suo Y, Ahn J, Liu D, Chen S, Hu Y, Ye X, Ding T (2018c) Preceding treatment of non-thermal plasma (NTP) assisted the bactericidal effect of ultrasound on Staphylococcus aureus. Food Control 90:241–248
Liao X, Li J, Suo Y, Ahn J, Liu D, Chen S, Hu Y, Ye X, Ding T (2018d) Effect of preliminary stresses on the resistance of Escherichia coli and Staphylococcus aureus toward non-thermal plasma (NTP) challenge. Food Res Int 105:178–183
Liao X, Muhammad AI, Chen S, Hu Y, Ye X, Liu D, Ding T (2019) Bacterial spore inactivation induced by cold plasma. Cri Rev Food Sci 59(16):2562–2572
Liao X, Xiang Q, Cullen PJ, Su Y, Chen S, Ye X, Liu D, Ding T (2020a) Plasma-activated water (PAW) and slightly acidic electrolyzed water (SAEW) as beef thawing media for enhancing microbiological safety. LWT Food Sci Technol 117:108649
Liao X, Bai Y, Muhammad AI, Liu D, Hu Y, Ding T (2020b) The application of plasma-activated water combined with mild heat for the decontamination of Bacillus cereus spores in rice (Oryza sativa L ssp japonica). J Phys D Appl Phys 53(6):064003
Liao X, Liu D, Tian D (2020c) Nonthermal plasma (NTP) induces viable but nonculturable (VBNC) state in Staphylococcus aureus via metabolic suppression and oxidative stress response. Appl Environ Microbiol 86:e02216–e02219
Liu Z, Liu D, Chen C, Li D, Yang A, Rong M, Chen H, Kong M (2015) Physicochemical processes in the indirect interaction between surface air plasma and deionized water. J Phys D Appl Phys 48(49):495201
Mahnot NK, Mahanta CL, Farkas BE, Keener KM, Misra N (2019)Atmospheric cold plasma inactivation of Escherichia coli and Listeria monocytogenes in tender coconut water: Inoculation and accelerated shelf-life studies.Food Control 106:106678
Mandal R, Singh A, Singh AP (2018) Recent developments in cold plasma decontamination technology in the food industry. Trends Food Sci Technol 80:93–103
Matan N, Nisoa M, Matan N (2014) Antibacterial activity of essential oils and their main components enhanced by atmospheric RF plasma. Food Control 39:97–99
Matan N, Puangjinda K, Phothisuwan S, Nisoa M (2015) Combined antibacterial activity of green tea extract with atmospheric radio-frequency plasma against pathogens on fresh-cut dragon fruit. Food Control 50:291–296
Mir SA, Shah MA, Mir MM (2016) Understanding the role of plasma technology in food industry. Food Bioprocess Technol 9(5):734–750
Misra N, Schlüter O, Cullen PJ (2016) Cold plasma in food and agriculture: fundamentals and applications. Academic Press, MA.
Muhammad AI, Liao X, Cullen PJ, Liu D, Xiang Q, Wang J, Chen S, Ye X, Ding T (2018a) Effects of nonthermal plasma technology on functional food components. Compr Rev Food Sci F 17(5):1379–1394
Muhammad AI, Xiang Q, Liao X, Liu D, Ding T (2018b) Understanding the impact of nonthermal plasma on food constituents and microstructure—a review. Food Bioprocess Technol 11(3):463–486
Muhammad AI, Chen W, Liao X, Xiang Q, Liu D, Ye X, Ding T (2019a) Effects of plasma-activated water and blanching on microbial and physicochemical properties of tiger nuts. Food Bioprocess Technol 12(10):1721–1732
Muhammad AI, Li Y, Liao X, Liu D, Ye X, Chen S, Hu Y, Wang J, Ding T (2019b) Effect of dielectric barrier discharge plasma on background microflora and physicochemical properties of tiger nut milk. Food Control 96:119–127
Modi R, Hirvi Y, Hill A, Griffiths M (2001) Effect of phage on survival of Salmonella enteritidis during manufacture and storage of cheddar cheese made from raw and pasteurized milk. J Food Prot 64(7):927–933
Nazzaro F, Fratianni F, De Martino L, Coppola R, De Feo V (2013) Effect of essential oils on pathogenic bacteria. Pharmaceuticals 6(12):1451–1474
Patange A, Lu P, Boeh D, Cullen P, Bourke P (2019) Efficacy of cold plasma functionalised water for improving microbiological safety of fresh produce and wash water recycling. Food Microbiol 84:103226
Pandit S, Mokkapati VR, Helgadóttir SH, Westerlund F, Mijakovic I (2017) Combination of cold atmospheric plasma and vitamin C effectively disrupts bacterial biofilms. Clin Microbiol 6:3
Ramazzina I, Berardinelli A, Rizzi F, Tappi S, Ragni L, Sacchetti G, Rocculi P (2015) Effect of cold plasma treatment on physico-chemical parameters and antioxidant activity of minimally processed kiwifruit. Postharvest Biol Technol 107:55–65
Scholtz V, Pazlarova J, Souskova H, Khun J, Julak J (2015) Nonthermal plasma—a tool for decontamination and disinfection. Biotechnol Adv 33(6):1108–1119
Shen J, Tian Y, Li Y, Ma R, Zhang Q, Zhang J, Fang J (2016) Bactericidal effects against S. aureus and physicochemical properties of plasma activated water stored at different temperatures. Sci Rep-UK 6:28505
Thirumdas R, Kothakota A, Annapure U, Siliveru K, Blundell R, Gatt R, Valdramidis VP (2018) Plasma activated water (PAW): chemistry, physico-chemical properties, applications in food and agriculture. Trends Food Sci Technol 77:21–31
Tian W, Kushner MJ (2014) Atmospheric pressure dielectric barrier discharges interacting with liquid covered tissue. J Appl Phys 47(16):165201
Trevisani M, Berardinelli A, Cevoli C, Cecchini M, Ragni L, Pasquali F (2017) Effects of sanitizing treatments with atmospheric cold plasma, SDS and lactic acid on verotoxin-producing Escherichia coli and Listeria monocytogenes in red chicory (radicchio). Food Control 78:138–143
United Nations (UN) (2019) World population prospects 2019 http://ww.esaunorg/unpd/wpp/download/standard/population/. Accessed 21 Sept 2019
Vilchèze C, Hartman T, Weinrick B, Jacobs JWR (2013) Mycobacterium tuberculosis is extraordinarily sensitive to killing by a vitamin C-induced Fenton reaction. Nat Commun 4:1881
Winter J, Tresp H, Hammer MU, Iseni S, Kupsch S, Schmidt-Bleker A, Wende K, Dünnbier M, Masur K, Reuter S (2014) Tracking plasma generated H2O2 from gas into liquid phase and revealing its dominant impact on human skin cells. J Appl Phys 47(28):285401
Wu D, Forghani F, Daliri EBM, Li J, Liao X, Liu D, Ye X, Chen S, Ding T (2020) Microbial response to some nonthermal physical technologies. Trends Food Sci Technol 95:107–117
Xiang Q, Kang C, Niu L, Zhao D, Li K, Bai Y (2018a) Antibacterial activity and a membrane damage mechanism of plasma activated water against Pseudomonas deceptionensis CM2. LWT Food Sci Technol 96:395–401
Xiang Q, Liu X, Li J, Liu S, Zhang H, Bai Y (2018b) Effects of dielectric barrier discharge plasma on the inactivation of Zygosaccharomyces rouxii and quality of apple juice. Food Chem 254:201–207
Xiang Q, Liu X, Liu S,Ma Y, Xu C, Bai Y (2019) Effect of plasma-activated water on microbial quality and physicochemical characteristics of mung bean sprouts. Innov Food Sci Emerg 52:49–56.
Xiang Q, Wang W, Zhao D, Niu L, Li K, Bai Y (2019) Synergistic inactivation of Escherichia coli O157:H7 by plasma-activated water and mild heat. Food Control 106:106741
Zhao YM, Alba MD, Sun DW, Tiwari B (2018) Principles and recent applications of novel non-thermal processing technologies for the fish industry—a review. Crit Rev Food Sci 59(5):728–742
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This research is supported by the National Natural Science Foundation of China (grants 31772079) and the National Key Research and Development Program of China (2017YFD0400403).
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Author PJ Cullen is CEO of PlasmaLeap Technologies, a cold plasma technology company.
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Liao, X., Cullen, P.J., Muhammad, A.I. et al. Cold Plasma–Based Hurdle Interventions: New Strategies for Improving Food Safety. Food Eng Rev 12, 321–332 (2020). https://doi.org/10.1007/s12393-020-09222-3
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DOI: https://doi.org/10.1007/s12393-020-09222-3