Skip to main content
SpringerLink
Log in

Comparison of the efficacy of physical and chemical strategies for the inactivation of biofilm cells of foodborne pathogens

  • Review
  • Published:
Food Science and Biotechnology Aims and scope Submit manuscript

Abstract

Biofilm formation is a strategy in which microorganisms generate a matrix of extracellular polymeric substances to increase survival under harsh conditions. The efficacy of sanitization processes is lowered when biofilms form, in particular on industrial devices. While various traditional and emerging technologies have been explored for the eradication of biofilms, cell resistance under a range of environmental conditions renders evaluation of the efficacy of control challenging. This review aimed to: (1) classify biofilm control measures into chemical, physical, and combination methods, (2) discuss mechanisms underlying inactivation by each method, and (3) summarize the reduction of biofilm cells after each treatment. The review is expected to be useful for future experimental studies and help to guide the establishment of biofilm control strategies in the food industry.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Akbas MY, Cag S. Use of organic acids for prevention and removal of Bacillus subtilis biofilms on food contact surfaces. Food Science and Technology International. 22: 587-597 (2016)

    Article  CAS  PubMed  Google Scholar 

  • Anyasi TA, Jideani AIO, Mchau GRA. Effects of organic acid pretreatment on microstructure, functional and thermal properties of unripe banana flour. Journal of Food Measurement and Characterization. 11: 99-110 (2017)

    Article  Google Scholar 

  • Araújo PA, Machado I, Meireles A, Leiknes T, Mergulhão F, Melo LF, Simões M. Combination of selected enzymes with cetyltrimethylammonium bromide in biofilm inactivation, removal and regrowth. Food Research International. 95: 101-107 (2017)

    Article  PubMed  Google Scholar 

  • Arevalos-Sánchez M, Regalado C, Martin SE, Domínguez-Domínguez J, García-Almendárez BE. Effect of neutral electrolyzed water and nisin on Listeria monocytogenes biofilms, and on listeriolysin O activity. Food Control. 24: 116-122 (2012)

    Article  Google Scholar 

  • Argyraki A, Markvart M, Nielsen A, Bjarnsholt T, Bjørndal L, Petersen PM. Comparison of UVB and UVC irradiation disinfection efficacies on Pseudomonas aeruginosa (P. aeruginosa) biofilm. 303-309. Proceedings SPIE 9887, Biophotonics: Photonic Solutions for Better Health Care V, 988730 (2016)

  • Arnaouteli S, Bamford NC, Stanley-Wall NR, Kovács ÁT. Bacillus subtilis biofilm formation and social interactions. Nature Reviews Microbiology. 19: 600-614 (2021)

    Article  CAS  PubMed  Google Scholar 

  • Arroqui C, Rumsey T, Lopez A, Virseda P. Effect of different soluble solids in the water on the ascorbic acid losses during water blanching of potato tissue. Journal of Food Engineering. 47: 123-126 (2001)

    Article  Google Scholar 

  • Assadian O, Zatorska B, Presterl E, Diab-El Schahawi M. A novel micellar formulation based on natural plant extracts enhances the efficacy of hydrogen peroxide against biofilms of Staphylococcus spp. and Pseudomonas aeruginosa. Biofouling. 36: 576-586 (2020)

    Article  CAS  PubMed  Google Scholar 

  • Awad T, Moharram H, Shaltout O, Asker D, Youssef M. Applications of ultrasound in analysis, processing and quality control of food: A review. Food Research International. 48: 410-427 (2012)

    Article  CAS  Google Scholar 

  • Ayebah B, Hung YC, Frank JF. Enhancing the bactericidal effect of electrolyzed water on Listeria monocytogenes biofilms formed on stainless steel. Journal of Food Protection. 68: 1375-1380 (2005)

    Article  PubMed  Google Scholar 

  • Azam A, Ahmed AS, Oves M, Khan MS, Habib SS, Memic A. Antimicrobial activity of metal oxide nanoparticles against Gram-positive and Gram-negative bacteria: a comparative study. International Journal of Nanomedicine. 7: 6003-6009 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Azeredo J, Azevedo NF, Briandet R, Cerca N, Coenye T, Costa AR, Desvaux M, Di Bonaventura G, Hébraud M, Jaglic Z, Kačániová M, Knøchel S, Lourenço A, Mergulhão F, Meyer RL, Nychas G, Simões M, Tresse O, Sternberg C. Critical review on biofilm methods. Critical Reviews in Microbiology. 43: 313-351 (2017)

    Article  CAS  PubMed  Google Scholar 

  • Back KH, Ha JW, Kang DH. Effect of hydrogen peroxide vapor treatment for inactivating Salmonella Typhimurium, Escherichia coli O157:H7 and Listeria monocytogenes on organic fresh lettuce. Food Control. 44: 78-85 (2014)

    Article  CAS  Google Scholar 

  • Ban GH, Kang DH. Effect of sanitizer combined with steam heating on the inactivation of foodborne pathogens in a biofilm on stainless steel. Food Microbiology. 55: 47-54 (2016a)

    Article  CAS  PubMed  Google Scholar 

  • Ban GH, Kang DH. Effectiveness of superheated steam for inactivation of Escherichia coli O157:H7, Salmonella Typhimurium, Salmonella Enteritidis phage type 30, and Listeria monocytogenes on almonds and pistachios. International Journal of Food Microbiology. 220: 19-25 (2016b)

    Article  CAS  PubMed  Google Scholar 

  • Ban GH, Kang DH. Inactivation of Escherichia coli O157:H7, Salmonella Typhimurium, and Listeria monocytogenes on cherry tomatoes and oranges by superheated steam. Food Research International. 112: 38-47 (2018)

    Article  CAS  PubMed  Google Scholar 

  • Ban GH, Lee J, Choi CH, Li Y, Jun S. Nano-patterned aluminum surface with oil-impregnation for improved antibacterial performance. LWT. 84: 359-363 (2017)

    Article  CAS  Google Scholar 

  • Ban GH, Li Y, Wall MM, Jun S. A nanoengineered stainless steel surface to combat bacterial attachment and biofilm formation. Foods. 9: 1518 (2020)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ban GH, Park SH, Kim SO, Ryu S, Kang DH. Synergistic effect of steam and lactic acid against Escherichia coli O157:H7, Salmonella Typhimurium, and Listeria monocytogenes biofilms on polyvinyl chloride and stainless steel. International Journal of Food Microbiology. 157: 218-223 (2012)

    Article  CAS  PubMed  Google Scholar 

  • Ban GH, Yoon H, Kang DH. A comparison of saturated steam and superheated steam for inactivation of Escherichia coli O157:H7, Salmonella Typhimurium, and Listeria monocytogenes biofilms on polyvinyl chloride and stainless steel. Food Control. 40: 344-350 (2014)

    Article  CAS  Google Scholar 

  • Bang J, Hong A, Kim H, Beuchat LR, Rhee MS, Kim Y, Ryu JH. Inactivation of Escherichia coli O157:H7 in biofilm on food-contact surfaces by sequential treatments of aqueous chlorine dioxide and drying. International Journal of Food Microbiology. 191: 129-134 (2014)

    Article  CAS  PubMed  Google Scholar 

  • Bansal M, Nannapaneni R, Kode D, Chang S, Sharma CS, McDaniel C, Kiess A. Rugose morphotype in Salmonella Typhimurium and Salmonella Heidelberg induced by sequential exposure to subinhibitory sodium hypochlorite aids in biofilm tolerance to lethal sodium hypochlorite on polystyrene and stainless steel surfaces. Frontiers in Microbiology. 10: 2704 (2019)

    Article  PubMed  PubMed Central  Google Scholar 

  • Bari ML, Inatsu Y, Isobe S, Kawamoto S. Hot water treatments to inactivate Escherichia coli O157: H7 and Salmonella in mung bean seeds. Journal of Food Protection. 71: 830-834 (2008)

    Article  CAS  PubMed  Google Scholar 

  • Beier RC, Pillai SD, Phillips TD, Ziprin RL. Preharvest and postharvest food safety: contemporary issues and future directions. Wiley-Blackwell, Hoboken, NJ, USA. (2008)

    Google Scholar 

  • Bell KY, Cutter CN, Sumner SS. Reduction of foodborne micro-organisms on beef carcass tissue using acetic acid, sodium bicarbonate, and hydrogen peroxide spray washes. Food Microbiology. 14: 439-448 (1997)

    Article  CAS  Google Scholar 

  • Brackman G, Coenye T. Quorum sensing inhibitors as anti-biofilm agents. Current Pharmaceutical Design. 21: 5-11 (2015)

    Article  CAS  PubMed  Google Scholar 

  • Brandl MT, Pan Z, Huynh S, Zhu Y, McHugh TH. Reduction of Salmonella Enteritidis population sizes on almond kernels with infrared heat. Journal of Food Protection. 71: 897-902 (2008)

    Article  PubMed  Google Scholar 

  • Bridier A, Sanchez-Vizuete P, Guilbaud M, Piard J-C, Naïtali M, Briandet R. Biofilm-associated persistence of food-borne pathogens. Food Microbiology. 45: 167-178 (2015)

    Article  CAS  PubMed  Google Scholar 

  • Carrasco E, Morales-Rueda A, García-Gimeno RM. Cross-contamination and recontamination by Salmonella in foods: a review. Food Research International. 45: 545-556 (2012)

    Article  Google Scholar 

  • Cenkowski S, Pronyk C, Zmidzinska D, Muir W. Decontamination of food products with superheated steam. Journal of Food Engineering. 83: 68-75 (2007)

    Article  CAS  Google Scholar 

  • Cha MY, Ha JW. Low-energy X-ray irradiation effectively inactivates major foodborne pathogen biofilms on various food contact surfaces. Food Microbiology. 106: 104054 (2022)

    Article  CAS  PubMed  Google Scholar 

  • Chauhan R, Kumari S, Goel G, Azmi W. Synergistic combination of malic acid with sodium hypochlorite impairs biofilm of Cronobacter sakazakii. LWT. 155: 112902 (2022)

    Article  CAS  Google Scholar 

  • Chen C, Hu W, He Y, Jiang A, Zhang R. Effect of citric acid combined with UV-C on the quality of fresh-cut apples. Postharvest Biology and Technology. 111: 126-131 (2016)

    Article  CAS  Google Scholar 

  • Cui H, Bai M, Yuan L, Surendhiran D, Lin L. Sequential effect of phages and cold nitrogen plasma against Escherichia coli O157:H7 biofilms on different vegetables. International Journal of Food Microbiology. 268: 1-9 (2018)

    Article  CAS  PubMed  Google Scholar 

  • Cui H, Li W, Li C, Lin L. Synergistic effect between Helichrysum italicum essential oil and cold nitrogen plasma against Staphylococcus aureus biofilms on different food-contact surfaces. International Journal of Food Science & Technology. 51: 2493-2501 (2016)

    Article  CAS  Google Scholar 

  • Cui H, Zhang C, Li C, Lin L. Inhibition mechanism of cardamom essential oil on methicillin-resistant Staphylococcus aureus biofilm. LWT. 122: 109057 (2020)

    Article  CAS  Google Scholar 

  • DeFlorio W, Liu S, White AR, Taylor TM, Cisneros-Zevallos L, Min Y, Scholar EM. Recent developments in antimicrobial and antifouling coatings to reduce or prevent contamination and cross-contamination of food contact surfaces by bacteria. Comprehensive Reviews in Food Science and Food Safety. 20: 3093-3134 (2021)

    Article  PubMed  Google Scholar 

  • Delgado DA, de Souza Sant’Ana A, Granato D, de Massaguer PR. Inactivation of Neosartorya fischeri and Paecilomyces variotii on paperboard packaging material by hydrogen peroxide and heat. Food Control. 23: 165-170 (2012)

  • Delorme MM, Guimarães JT, Coutinho NM, Balthazar CF, Rocha RS, Silva R, Margalho LP, Pimentel TC, Silva MC, Freitas MQ. Ultraviolet radiation: An interesting technology to preserve quality and safety of milk and dairy foods. Trends in Food science & Technology. 102: 146-154 (2020)

    Article  CAS  Google Scholar 

  • Desai MA, Soni KA, Nannapaneni R, Schilling MW, Silva JL. Reduction of Listeria monocytogenes biofilms on stainless steel and polystyrene surfaces by essential oils. Journal of Food Protection. 75: 1332-1337 (2012)

    Article  CAS  PubMed  Google Scholar 

  • de São José JFB, de Andrade NJ, Ramos AM, Vanetti MCD, Stringheta PC, Chaves JBP. Decontamination by ultrasound application in fresh fruits and vegetables. Food Control. 45: 36-50 (2014)

    Article  Google Scholar 

  • Desbois AP, Smith VJ. Antibacterial free fatty acids: activities, mechanisms of action and biotechnological potential. Applied Microbiology and Biotechnology. 85: 1629-1642 (2010)

    Article  CAS  PubMed  Google Scholar 

  • Dhakad AK, Pandey VV, Beg S, Rawat JM, Singh A. Biological, medicinal and toxicological significance of Eucalyptus leaf essential oil: a review. Journal of the Science of Food and Agriculture. 98: 833-848 (2018)

    Article  CAS  PubMed  Google Scholar 

  • Dhakal J, Sharma CS, Nannapaneni R, McDaniel CD, Kim T, Kiess A. Effect of chlorine-induced sublethal oxidative stress on the biofilm-forming ability of Salmonella at different temperatures, nutrient conditions, and substrates. Journal of Food Protection. 82: 78-92 (2019)

    Article  CAS  PubMed  Google Scholar 

  • do Prado DB, dos Anjos Szczerepa MM, Capeloto OA, Astrath NGC, dos Santos NCA, Previdelli ITS, Nakamura CV, Mikcha JMG, de Abreu Filho BA. Effect of ultraviolet (UV-C) radiation on spores and biofilms of Alicyclobacillus spp. in industrialized orange juice. International Journal of Food Microbiology. 305: 108238 (2019)

  • Dosoky NS, Setzer WN. Chemical composition and biological activities of essential oils of Curcuma species. Nutrients. 10: 1196 (2018)

    Article  PubMed  PubMed Central  Google Scholar 

  • Duraisamy S, Balakrishnan S, Ranjith S, Husain F, Sathyan A, Peter AS, Prahalathan C, Kumarasamy A. Bacteriocin–a potential antimicrobial peptide towards disrupting and preventing biofilm formation in the clinical and environmental locales. Environmental Science and Pollution Research. 27: 44922-44936 (2020)

    Article  CAS  PubMed  Google Scholar 

  • Dychdala GR, Chlorine and chlorine compounds, in: Disinfection, Sterilization and Preservation, fourth ed., Lea & Febiger, Philadelphia, PA, USA. (1991)

  • Epstein AK, Wong TS, Belisle RA, Boggs EM, Aizenberg J. Liquid-infused structured surfaces with exceptional anti-biofouling performance. Proceedings of the National Academy of Sciences. 109: 13182-13187 (2012)

    Article  CAS  Google Scholar 

  • Erriu M, Blus C, Szmukler-Moncler S, Buogo S, Levi R, Barbato G, Madonnaripa D, Denotti G, Piras V, Orrù G. Microbial biofilm modulation by ultrasound: current concepts and controversies. Ultrasonics Sonochemistry. 21: 15-22 (2014)

    Article  CAS  PubMed  Google Scholar 

  • Espitia PJP, Soares NdFF, Coimbra JSdR, de Andrade NJ, Cruz RS, Medeiros EAA. Zinc oxide nanoparticles: synthesis, antimicrobial activity and food packaging applications. Food and Bioprocess Technology. 5: 1447-1464 (2012)

    Article  CAS  Google Scholar 

  • Fang J, Liu C, Law CL, Mujumdar AS, Xiao HW, Zhang C. Superheated steam processing: An emerging technology to improve food quality and safety. Critical Reviews in Food Science and Nutrition: 1-17 (2022)

  • Farjami A, Hatami M, Siahi‐Shadbad M, Lotfipour F. Peracetic acid activity on biofilm formed by Escherichia coli isolated from an industrial water system. Letters in Applied Microbiology. 74: 613-621 (2022)

    Article  CAS  PubMed  Google Scholar 

  • Food and Drug Administration. CFR - Code of Federal Regulations Title 21 (2017). Available at: https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfcfr/cfrsearch.cfm. Accessed Jan. 9, 2023

  • Food and Drug Administration. FDA Food Code 2009: Chapter 4: equipment, utensils and linens. Available at: https://www.fda.gov/food/fda-food-code/food-code-2009. Accessed Nov. 06, 2022

  • Fujishima A, Rao TN, Tryk DA. Titanium dioxide photocatalysis. Journal of Photochemistry and Photobiology C: Photochemistry Reviews. 1: 1-21 (2000)

    Article  CAS  Google Scholar 

  • Fukuzaki S. Mechanisms of actions of sodium hypochlorite in cleaning and disinfection processes. Biocontrol Science. 11: 147-157 (2006)

    Article  CAS  PubMed  Google Scholar 

  • Gayán E, Condón S, Álvarez I. Biological aspects in food preservation by ultraviolet light: A review. Food and Bioprocess Technology. 7: 1-20 (2014)

    Article  Google Scholar 

  • Giaouris E, Chorianopoulos N, Doulgeraki A, Nychas GJ. Co-culture with Listeria monocytogenes within a dual-species biofilm community strongly increases resistance of Pseudomonas putida to benzalkonium chloride. PLoS One. 8: e77276 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gil MI, López-Gálvez F, Andújar S, Moreno M, Allende A. Disinfection by-products generated by sodium hypochlorite and electrochemical disinfection in different process wash water and fresh-cut products and their reduction by activated carbon. Food Control. 100: 46-52 (2019)

    Article  CAS  Google Scholar 

  • Gilmore BF, Flynn PB, O’Brien S, Hickok N, Freeman T, Bourke P. Cold plasmas for biofilm control: opportunities and challenges. Trends in Biotechnology. 36: 627-638 (2018)

    Article  CAS  PubMed  Google Scholar 

  • Gkana EN, Doulgeraki AI, Chorianopoulos NG, Nychas GJE. Anti-adhesion and anti-biofilm potential of organosilane nanoparticles against foodborne pathogens. Frontiers in Microbiology. 8: 1295 (2017)

    Article  PubMed  PubMed Central  Google Scholar 

  • Gomes L, Deschamps J, Briandet R, Mergulhão FJ. Impact of modified diamond-like carbon coatings on the spatial organization and disinfection of mixed-biofilms composed of Escherichia coli and Pantoea agglomerans industrial isolates. International Journal of Food Microbiology. 277: 74-82 (2018)

    Article  CAS  PubMed  Google Scholar 

  • Góngora-Nieto M, Sepúlveda D, Pedrow P, Barbosa-Cánovas G, Swanson B. Food processing by pulsed electric fields: treatment delivery, inactivation level, and regulatory aspects. LWT. 35: 375-388 (2002)

    Article  Google Scholar 

  • Gordon G, Rosenblatt AA. Chlorine dioxide: the current state of the art. Ozone: Science & Engineering. 27: 203-207 (2005)

    Article  CAS  Google Scholar 

  • Govaert M, Smet C, Verheyen D, Walsh JL, Van Impe JF. Combined effect of cold atmospheric plasma and hydrogen peroxide treatment on mature Listeria monocytogenes and Salmonella Typhimurium biofilms. Frontiers in Microbiology. 10: 2674 (2019)

    Article  PubMed  PubMed Central  Google Scholar 

  • Graves DB. 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. 45: 263001 (2012)

    Article  Google Scholar 

  • Gu T, Meesrisom A, Luo Y, Dinh QN, Lin S, Yang M, Sharma A, Tang R, Zhang J, Jia Z, Millner PD, Pearlstein, AJ, Zhang B. Listeria monocytogenes biofilm formation as affected by stainless steel surface topography and coating composition. Food Control. 130: 108275 (2021)

    Article  CAS  Google Scholar 

  • Guerrero-Beltrán J, Barbosa-Cánovas G. Advantages and limitations on processing foods by UV light. Food Science and Technology International. 10: 137-147 (2004)

    Article  Google Scholar 

  • Gule NP, Begum NM, Klumperman B. Advances in biofouling mitigation: A review. Critical Reviews in Environmental Science and Technology. 46: 535-555 (2016)

    Article  CAS  Google Scholar 

  • Guo C, He Y, Wang Y, Yang H. NMR-based metabolomic investigation on antimicrobial mechanism of Salmonella on cucumber slices treated with organic acids. Food Control. 137: 108973 (2022)

    Article  CAS  Google Scholar 

  • Guo L, Sun Y, Zhu Y, Wang B, Xu L, Huang M, Li Y, Sun J. The antibacterial mechanism of ultrasound in combination with sodium hypochlorite in the control of Escherichia coli. Food Research International. 129: 108887 (2020)

    Article  CAS  PubMed  Google Scholar 

  • Han JY, Song WJ, Kang JH, Min SC, Eom S, Hong EJ, Ryu S, Kim SB, Cho S, Kang DH. Effect of cold atmospheric pressure plasma-activated water on the microbial safety of Korean rice cake. LWT. 120: 108918 (2020)

    Article  CAS  Google Scholar 

  • Han JY, Park SH, Kang DH. Effects of plasma bubble-activated water on the inactivation against foodborne pathogens on tomatoes and its wash water. Food Control. 144: 109381 (2023)

    Article  CAS  Google Scholar 

  • Handorf O, Pauker VI, Schnabel U, Weihe T, Freund E, Bekeschus S, Riedel K, Ehlbeck J. Characterization of antimicrobial effects of plasma-treated water (PTW) produced by microwave-induced plasma (MidiPLexc) on Pseudomonas fluorescens biofilms. Applied Sciences. 10: 3118 (2020)

    Article  CAS  Google Scholar 

  • Handorf O, Pauker VI, Weihe T, Schäfer J, Freund E, Schnabel U, Bekeschus S, Riedel K, Ehlbeck J. Plasma-treated water affects Listeria monocytogenes vitality and biofilm structure. Frontiers in Microbiology. 12: 652481 (2021)

    Article  PubMed  PubMed Central  Google Scholar 

  • Hao J, Zhang J, Zheng X, Zhao D. Bactericidal efficacy of slightly acidic electrolyzed water (SAEW) against Listeria monocytogenes planktonic cells and biofilm on food-contact surfaces. Food Quality and Safety. 6: fyab038 (2022)

    Article  Google Scholar 

  • Hernando-Amado S, Alcalde-Rico M, Gil-Gil T, Valverde JR, Martínez JL. Naringenin inhibition of the Pseudomonas aeruginosa quorum sensing response is based on its time-dependent competition with N-(3-oxo-dodecanoyl)-l-homoserine lactone for LasR binding. Frontiers in Molecular Biosciences. 7: 25 (2020)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu H, Cai L, Dong Y, Wang H, Xu X, Zhou G. Modeling the degradation of acidic electrolyzed water and its ability to disinfect a dual-species biofilm. LWT. 104: 159-164 (2019a)

    Article  CAS  Google Scholar 

  • Hu J, Lin J, Zhang Y, Lin Z, Qiao Z, Liu Z, Yang W, Liu X, Dong M, Guo Z. A new anti-biofilm strategy of enabling arbitrary surfaces of materials and devices with robust bacterial anti-adhesion via a spraying modified microsphere method. Journal of Materials Chemistry A. 7: 26039-26052 (2019b)

    Article  CAS  Google Scholar 

  • Huang L. Numerical analysis of heat transfer during surface pasteurization of hot dogs with vacuum‐steam‐vacuum technology. Journal of Food Science. 69: E455-E464 (2004)

    Article  CAS  Google Scholar 

  • Huang X, Lao Y, Pan Y, Chen Y, Zhao H, Gong L, Xie N, Mo CH. Synergistic antimicrobial effectiveness of plant essential oil and its application in seafood preservation: a review. Molecules. 26: 307 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang YR, Hung YC, Hsu SY, Huang YW, Hwang DF. Application of electrolyzed water in the food industry. Food Control. 19: 329-345 (2008)

    Article  Google Scholar 

  • Huang Z, Ghasemi H. Hydrophilic polymer-based anti-biofouling coatings: preparation, mechanism, and durability. Advances in Colloid and Interface Science. 284: 102264 (2020)

    Article  CAS  PubMed  Google Scholar 

  • Hussain MS, Tango CN, Oh DH. Inactivation kinetics of slightly acidic electrolyzed water combined with benzalkonium chloride and mild heat treatment on vegetative cells, spores, and biofilms of Bacillus cereus. Food Research International. 116: 157-167 (2019)

    Article  CAS  PubMed  Google Scholar 

  • Iñiguez-Moreno M, Gutiérrez-Lomelí M, Guerrero-Medina PJ, Avila-Novoa MG. Biofilm formation by Staphylococcus aureus and Salmonella spp. under mono and dual-species conditions and their sensitivity to cetrimonium bromide, peracetic acid and sodium hypochlorite. Brazilian Journal of Microbiology. 49: 310-319 (2018)

    Article  PubMed  Google Scholar 

  • Ishibashi K, Shimada K, Kawato T, Kaji S, Maeno M, Sato S, Ito K. Inhibitory effects of low-energy pulsed ultrasonic stimulation on cell surface protein antigen C through heat shock proteins GroEL and DnaK in Streptococcus mutans. Applied and Environmental Microbiology. 76: 751-756 (2010)

    Article  CAS  PubMed  Google Scholar 

  • James C, James SJ. Meat decontamination-the state of the art. MAFF Advanced Fellowship in Food Process Engineering. University of Bristol (1997)

  • Jennings MC, Buttaro BA, Minbiole KPC, Wuest WM. Bioorganic investigation of multicationic antimicrobials to combat QAC-resistant Staphylococcus aureus. ACS Infectious Diseases. 1: 304-309 (2015a)

    Article  CAS  PubMed  Google Scholar 

  • Jennings MC, Minbiole KPC, Wuest WM. Quaternary ammonium compounds: an antimicrobial mainstay and platform for innovation to address bacterial resistance. ACS Infectious Diseases. 1: 288-303 (2015b)

    Article  CAS  PubMed  Google Scholar 

  • Jha N, Ryu JJ, Choi EH, Kaushik NK. Generation and role of reactive oxygen and nitrogen species induced by plasma, lasers, chemical agents, and other systems in dentistry. Oxidative Medicine and Cellular Longevity. 2017: 7542540 (2017)

    Article  PubMed  PubMed Central  Google Scholar 

  • Jiang Y, Sokorai K, Pyrgiotakis G, Demokritou P, Li X, Mukhopadhyay S, Jin T, Fan X. Cold plasma-activated hydrogen peroxide aerosol inactivates Escherichia coli O157:H7, Salmonella Typhimurium, and Listeria innocua and maintains quality of grape tomato, spinach and cantaloupe. International Journal of Food Microbiology. 249: 53-60 (2017)

    Article  CAS  PubMed  Google Scholar 

  • Jin H, Tian L, Bing W, Zhao J, Ren L. Bioinspired marine antifouling coatings: Status, prospects, and future. Progress in Materials Science. 124: 100889 (2022)

    Article  CAS  Google Scholar 

  • Jindal S, Anand S, Huang K, Goddard J, Metzger L, Amamcharla J. Evaluation of modified stainless steel surfaces targeted to reduce biofilm formation by common milk sporeformers. Journal of Dairy Science. 99: 9502-9513 (2016)

    Article  CAS  PubMed  Google Scholar 

  • Jindal S, Anand S, Metzger L, Amamcharla J. A comparison of biofilm development on stainless steel and modified-surface plate heat exchangers during a 17-h milk pasteurization run. Journal of Dairy Science. 101: 2921-2926 (2018)

    Article  CAS  PubMed  Google Scholar 

  • Ju J, Chen X, Xie Y, Yu H, Guo Y, Cheng Y, Qian H, Yao W. Application of essential oil as a sustained release preparation in food packaging. Trends in Food Science & Technology. 92: 22-32 (2019)

    Article  CAS  Google Scholar 

  • Jung SJ, Park SY, Ha SD. Synergistic effect of X-ray irradiation and sodium hypochlorite against Salmonella enterica serovar Typhimurium biofilms on quail eggshells. Food Research International. 107: 496-502 (2018)

    Article  CAS  PubMed  Google Scholar 

  • Kang JW, Lee HY, Kang DH. Synergistic bactericidal effect of hot water with citric acid against Escherichia coli O157:H7 biofilm formed on stainless steel. Food Microbiology. 95: 103676 (2021)

    Article  CAS  PubMed  Google Scholar 

  • Kang J, Jin W, Wang J, Sun Y, Wu X, Liu L. Antibacterial and anti-biofilm activities of peppermint essential oil against Staphylococcus aureus. LWT. 101: 639-645 (2019)

    Article  CAS  Google Scholar 

  • Kang J, Liu L, Wu X, Sun Y, Liu Z. Effect of thyme essential oil against Bacillus cereus planktonic growth and biofilm formation. Applied Microbiology and Biotechnology. 102: 10209-10218 (2018)

    Article  CAS  PubMed  Google Scholar 

  • Keskinen LA, Burke A, Annous BA. Efficacy of chlorine, acidic electrolyzed water and aqueous chlorine dioxide solutions to decontaminate Escherichia coli O157:H7 from lettuce leaves. International Journal of Food Microbiology. 132: 134-140 (2009)

    Article  CAS  PubMed  Google Scholar 

  • Khalid HF, Tehseen B, Sarwar Y, Hussain SZ, Khan WS, Raza ZA, Bajwa SZ, Kanaras AG, Hussain I, Rehman A. Biosurfactant coated silver and iron oxide nanoparticles with enhanced anti-biofilm and anti-adhesive properties. Journal of Hazardous Materials. 364: 441-448 (2019)

    Article  CAS  PubMed  Google Scholar 

  • Khan SI, Blumrosen G, Vecchio D, Golberg A, McCormack MC, Yarmush ML, Hamblin MR, Austen WG Jr. Eradication of multidrug-resistant Pseudomonas biofilm with pulsed electric fields. Biotechnology and Bioengineering. 113: 643-650 (2016)

    Article  CAS  PubMed  Google Scholar 

  • Ki SH, Noh H, Ahn GR, Kim SH, Kaushik NK, Choi EH, Lee GJ. Influence of nonthermal atmospheric plasma-activated water on the structural, optical, and biological properties of Aspergillus brasiliensis spores. Applied Sciences. 10: 6378 (2020)

    Article  CAS  Google Scholar 

  • Kim SH, Park SH, Kim SS, Kang DH. Inactivation of Staphylococcus aureus biofilms on food contact surfaces by superheated steam treatment. Journal of food protection. 82: 1496-1500 (2019)

  • Kim J, Pitts B, Stewart PS, Camper A, Yoon J. Comparison of the antimicrobial effects of chlorine, silver ion, and tobramycin on biofilm. Antimicrobial Agents and Chemotherapy. 52: 1446-1453 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim JS, Kuk E, Yu KN, Kim J-H, Park SJ, Lee HJ, Kim SH, Park YK, Park YH, Hwang CY, Kim, YK, Lee, YS, Jeong, DH, Cho, MH. Antimicrobial effects of silver nanoparticles. Nanomedicine: Nanotechnology, Biology and Medicine. 3: 95-101 (2007)

    Article  CAS  PubMed  Google Scholar 

  • Kim M, Park SY, Ha SD. Synergistic effect of a combination of ultraviolet-C irradiation and sodium hypochlorite to reduce Listeria monocytogenes biofilms on stainless steel and eggshell surfaces. Food Control. 70: 103-109 (2016)

    Article  CAS  Google Scholar 

  • Kim S, Park S. Chlorine dioxide gas mediated inactivation of the biofilm cells of. Journal of Food Science and Technology. 59: 4863-4869 (2022)

    Article  CAS  PubMed  Google Scholar 

  • Kocot AM, Olszewska MA. Interaction of Pseudomonas aeruginosa and Staphylococcus aureus with Listeria innocua in dual species biofilms and inactivation following disinfectant treatments. LWT. 118: 108736 (2020)

    Article  CAS  Google Scholar 

  • Korany AM, Hua Z, Green T, Hanrahan I, El-Shinawy SH, El-Kholy A, Hassan G, Zhu MJ. Efficacy of ozonated water, chlorine, chlorine dioxide, quaternary ammonium compounds and peroxyacetic acid against Listeria monocytogenes biofilm on polystyrene surfaces. Frontiers in Microbiology. 9: 2296 (2018)

    Article  PubMed  PubMed Central  Google Scholar 

  • Kouassi KHS, Bajji M, Jijakli H. The control of postharvest blue and green molds of citrus in relation with essential oil-wax formulations, adherence and viscosity. Postharvest Biology and Technology. 73: 122-128 (2012)

    Article  CAS  Google Scholar 

  • Krzyżek P. Challenges and limitations of anti-quorum sensing therapies. Frontiers in Microbiology. 10: 2473 (2019)

    Article  PubMed  PubMed Central  Google Scholar 

  • Lamin A, Kaksonen AH, Cole IS, Chen XB. Quorum sensing inhibitors applications: A new prospect for mitigation of microbiologically influenced corrosion. Bioelectrochemistry: 108050 (2022)

  • Lebert I, Leroy S, Talon R. Effect of industrial and natural biocides on spoilage, pathogenic and technological strains grown in biofilm. Food Microbiology. 24: 281-287 (2007)

    Article  CAS  PubMed  Google Scholar 

  • Lee J, Jiang Y, Hizal F, Ban GH, Jun S, Choi CH. Durable omniphobicity of oil-impregnated anodic aluminum oxide nanostructured surfaces. Journal of Colloid and Interface Science. 553: 734-745 (2019a)

    Article  CAS  PubMed  Google Scholar 

  • Lee WN, Huang CH, Zhu G. Analytical methods for conventional and emerging disinfection by-products in fresh-cut produce. Food Chemistry. 291: 30-37 (2019b)

    Article  CAS  PubMed  Google Scholar 

  • Li X, Kim MJ, Bang WS, Yuk HG. Anti-biofilm effect of 405-nm LEDs against Listeria monocytogenes in simulated ready-to-eat fresh salmon storage conditions. Food Control. 84: 513-521 (2018)

    Article  CAS  Google Scholar 

  • Liao X, Liu D, Xiang Q, Ahn J, Chen S, Ye X, Ding T. Inactivation mechanisms of non-thermal plasma on microbes: A review. Food Control. 75: 83-91 (2017)

    Article  CAS  Google Scholar 

  • Liu D, Huang Q, Gu W, Zeng XA. A review of bacterial biofilm control by physical strategies. Critical Reviews in Food Science and Nutrition. 62: 3453-3470 (2022)

    Article  CAS  PubMed  Google Scholar 

  • Liu F, Du L, Zhao T, Zhao P, Doyle MP. Effects of phenyllactic acid as sanitizing agent for inactivation of Listeria monocytogenes biofilms. Food Control. 78: 72-78 (2017)

    Article  CAS  Google Scholar 

  • Liu F, Tang C, Wang D, Sun Z, Du L, Wang D. The synergistic effects of phenyllactic acid and slightly acid electrolyzed water to effectively inactivate Klebsiella oxytoca planktonic and biofilm cells. Food Control. 125: 107804 (2021a)

    Article  CAS  Google Scholar 

  • Liu T, Kang J, Liu L. Thymol as a critical component of Thymus vulgaris L. essential oil combats Pseudomonas aeruginosa by intercalating DNA and inactivating biofilm. LWT. 136: 110354 (2021b)

    Article  CAS  Google Scholar 

  • Liu K, Ren W, Ran C, Zhou R, Tang W, Zhou R, Yang Z, Ostrikov KK. Long-lived species in plasma-activated water generated by an AC multi-needle-to-water discharge: effects of gas flow on chemical reactions. Journal of Physics D: Applied Physics. 54: 065201 (2020)

    Article  Google Scholar 

  • Lories B, Roberfroid S, Dieltjens L, De Coster D, Foster KR, Steenackers HP. Biofilm bacteria use stress responses to detect and respond to competitors. Current Biology. 30: 1231-1244 (2020)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Los A, Ziuzina D, Boehm D, Cullen PJ, Bourke P. Inactivation efficacies and mechanisms of gas plasma and plasma-activated water against Aspergillus flavus spores and biofilms: a comparative study. Applied and Environmental Microbiology. 86: e02619-19 (2020)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma R, Wang G, Tian Y, Wang K, Zhang J, Fang J. Non-thermal plasma-activated water inactivation of food-borne pathogen on fresh produce. Journal of Hazardous Materials. 300: 643-651 (2015)

    Article  CAS  PubMed  Google Scholar 

  • Mai-Prochnow A, Zhou R, Zhang T, Ostrikov K, Mugunthan S, Rice SA, Cullen PJ. Interactions of plasma-activated water with biofilms: inactivation, dispersal effects and mechanisms of action. npj Biofilms and Microbiomes. 7: 11 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maverakis E, Miyamura Y, Bowen MP, Correa G, Ono Y, Goodarzi H. Light, including ultraviolet. Journal of Autoimmunity. 34: J247-J257 (2010)

    Article  CAS  PubMed  Google Scholar 

  • McDonnell G, Russell AD. Antiseptics and disinfectants: activity, action, and resistance. Clinical Microbiology Reviews. 12: 147-179 (1999)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Misra NN, Tiwari BK, Raghavarao KSMS, Cullen PJ. Nonthermal plasma inactivation of food-borne pathogens. Food Engineering Reviews. 3: 159-170 (2011)

    Article  Google Scholar 

  • Mohanty S, Mishra S, Jena P, Jacob B, Sarkar B, Sonawane A. An investigation on the antibacterial, cytotoxic, and antibiofilm efficacy of starch-stabilized silver nanoparticles. Nanomedicine. 8: 916-924 (2012)

    Article  CAS  PubMed  Google Scholar 

  • Morgan AI, Goldberg N, Radewonuk ER, Scullen OJ. Surface pasteurization of raw poultry meat by steam. LWT. 29: 447-451 (1996)

    Article  CAS  Google Scholar 

  • Mori M, Hamamoto A, Takahashi A, Nakano M, Wakikawa N, Tachibana S, Ikehara T, Nakaya Y, Akutagawa M, Kinouchi Y. Development of a new water sterilization device with a 365 nm UV-LED. Medical & Biological Engineering & Computing. 45: 1237-1241 (2007)

    Article  Google Scholar 

  • Múgica-Vidal R, Sainz-García E, Álvarez-Ordóñez A, Prieto M, González-Raurich M, López M, López M, Rojo-Bezares B, Sáenz Y, Alba-Elías F. Production of antibacterial coatings through atmospheric pressure plasma: a promising alternative for combatting biofilms in the food industry. Food and Bioprocess Technology. 12: 1251-1263 (2019)

    Article  Google Scholar 

  • Muñoz-Mahamud E, Gonzalez-Cuevas A, Sierra JM, Diaz-Brito V, Bermudes A, Soriano A, Castellanos J, Font-Vizcarra L. Pulsed electric fields reduce bacterial attachment to stainless steel plates. Acta Orthopaedica Belgica. 84: 11-16 (2018)

    PubMed  Google Scholar 

  • Ofori I, Maddila S, Lin J, Jonnalagadda SB. Chlorine dioxide oxidation of Escherichia coli in water – a study of the disinfection kinetics and mechanism. Journal of Environmental Science and Health, Part A. 52: 598-606 (2017)

    Article  CAS  Google Scholar 

  • Ortiz S, López V, Martínez-Suárez JV. The influence of subminimal inhibitory concentrations of benzalkonium chloride on biofilm formation by Listeria monocytogenes. International Journal of Food Microbiology. 189: 106-112 (2014)

    Article  CAS  PubMed  Google Scholar 

  • Pang X, Chen L, Yuk HG. Stress response and survival of Salmonella Enteritidis in single and dual species biofilms with Pseudomonas fluorescens following repeated exposure to quaternary ammonium compounds. International Journal of Food Microbiology. 325: 108643 (2020)

    Article  CAS  PubMed  Google Scholar 

  • Pang X, Zhang H, Seck HL, Zhou W. Inactivation effect of low-energy X-ray irradiation against planktonic and biofilm Pseudomonas fluorescens and its antibacterial mechanism. International Journal of Food Microbiology: 109716 (2022)

  • Park SH, Cheon HL, Park KH, Chung MS, Choi SH, Ryu S, Kang DH. Inactivation of biofilm cells of foodborne pathogen by aerosolized sanitizers. International Journal of Food Microbiology. 154: 130-134 (2012)

    Article  CAS  PubMed  Google Scholar 

  • Park SH, Kang DH. Inactivation of biofilm cells of foodborne pathogens by steam pasteurization. European Food Research and Technology. 238: 471-476 (2014)

    Article  CAS  Google Scholar 

  • Park SY, Jung SJ, Ha SD. Synergistic effects of combined X-ray and aqueous chlorine dioxide treatments against Salmonella Typhimurium biofilm on quail egg shells. LWT. 92: 54-60 (2018)

    Article  CAS  Google Scholar 

  • Patra R, Soma Raju KRC, Bhaskar B, Sarkar D, Chaudhuri S, Garg P, Subasri R. Biofilm inhibiting nanocomposite coatings—a promising alternative to combat surgical site infections. Journal of Coatings Technology and Research. 19: 1697-1711 (2022)

    Article  CAS  Google Scholar 

  • Perez-Roa RE, Tompkins DT, Paulose M, Grimes CA, Anderson MA, Noguera DR. Effects of localised, low-voltage pulsed electric fields on the development and inhibition of Pseudomonas aeruginosa biofilms. Biofouling. 22: 383-390 (2006)

    Article  PubMed  Google Scholar 

  • Poimenidou SV, Chrysadakou M, Tzakoniati A, Bikouli VC, Nychas GJ, Skandamis PN. Variability of Listeria monocytogenes strains in biofilm formation on stainless steel and polystyrene materials and resistance to peracetic acid and quaternary ammonium compounds. International Journal of Food Microbiology. 237: 164-171 (2016)

    Article  CAS  PubMed  Google Scholar 

  • Premkumar A, Nishtala SN, Nguyen JT, Bostrom MP, Carli AV. The AAHKS best podium presentation research award: Comparing the efficacy of irrigation solutions on staphylococcal biofilm formed on arthroplasty surfaces. The Journal of Arthroplasty. 36: S26-S32 (2021)

    Article  PubMed  Google Scholar 

  • Pronyk C, Cenkowski S, Muir W. Drying foodstuffs with superheated steam. Drying Technology. 22: 899-916 (2004)

    Article  Google Scholar 

  • Purkait S, Bhattacharya A, Bag A, Chattopadhyay R. Evaluation of antibiofilm efficacy of essential oil components β‐caryophyllene, cinnamaldehyde and eugenol alone and in combination against biofilm formation and preformed biofilms of Listeria monocytogenes and Salmonella typhimurium. Letters in Applied Microbiology. 71: 195-202 (2020)

    Article  CAS  PubMed  Google Scholar 

  • Rai M, Pandit R, Gaikwad S, Kövics G. Antimicrobial peptides as natural bio-preservative to enhance the shelf-life of food. Journal of Food Science and Technology. 53: 3381-3394 (2016)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robbins JB, Fisher CW, Moltz AG, Martin SE. Elimination of Listeria monocytogenes biofilms by ozone, chlorine, and hydrogen peroxide. Journal of Food Protection. 68: 494-498 (2005)

    Article  CAS  PubMed  Google Scholar 

  • Romeu MJ, Rodrigues D, Azeredo J. Effect of sub-lethal chemical disinfection on the biofilm forming ability, resistance to antibiotics and expression of virulence genes of Salmonella Enteritidis biofilm-surviving cells. Biofouling. 36: 101-112 (2020)

    Article  CAS  PubMed  Google Scholar 

  • Roy PK, Mizan MFR, Hossain MI, Han N, Nahar S, Ashrafudoulla M, Toushik SH, Shim WB, Kim YM, Ha SD. Elimination of Vibrio parahaemolyticus biofilms on crab and shrimp surfaces using ultraviolet C irradiation coupled with sodium hypochlorite and slightly acidic electrolyzed water. Food Control. 128: 108179 (2021)

    Article  CAS  Google Scholar 

  • Rumbaugh KP, Sauer K. Biofilm dispersion. Nature Reviews Microbiology. 18: 571-586 (2020)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rzhepishevska O, Hakobyan S, Ruhal R, Gautrot J, Barbero D, Ramstedt M. The surface charge of anti-bacterial coatings alters motility and biofilm architecture. Biomaterials Science. 1: 589-602 (2013)

    Article  CAS  PubMed  Google Scholar 

  • Sadekuzzaman M, Mizan MFR, Kim HS, Yang S, Ha SD. Activity of thyme and tea tree essential oils against selected foodborne pathogens in biofilms on abiotic surfaces. LWT. 89: 134-139 (2018)

    Article  CAS  Google Scholar 

  • Sadekuzzaman M, Yang S, Mizan MFR, Ha SD. Current and recent advanced strategies for combating biofilms. Comprehensive Reviews in Food Science and Food Safety. 14: 491-509 (2015)

    Article  Google Scholar 

  • Sandt C, Barbeau J, Gagnon MA, Lafleur M. Role of the ammonium group in the diffusion of quaternary ammonium compounds in Streptococcus mutans biofilms. Journal of Antimicrobial Chemotherapy. 60: 1281-1287 (2007)

    Article  CAS  PubMed  Google Scholar 

  • Shao L, Dong Y, Chen X, Xu X, Wang H. Modeling the elimination of mature biofilms formed by Staphylococcus aureus and Salmonella spp. Using combined ultrasound and disinfectants. Ultrasonics Sonochemistry. 69: 105269 (2020)

    Article  CAS  PubMed  Google Scholar 

  • Sharma N, Bhardwaj NK, Singh RBP. Environmental issues of pulp bleaching and prospects of peracetic acid pulp bleaching: a review. Journal of Cleaner Production. 256: 120338 (2020)

    Article  CAS  Google Scholar 

  • Sikdar R, Elias M. Quorum quenching enzymes and their effects on virulence, biofilm, and microbiomes: a review of recent advances. Expert Review of Anti-infective Therapy. 18: 1221-1233 (2020)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simões M, Simões LC, Vieira MJ. A review of current and emergent biofilm control strategies. LWT. 43: 573-583 (2010)

    Article  Google Scholar 

  • Smet C, Govaert M, Kyrylenko A, Easdani M, Walsh JL, Van Impe JF. Inactivation of single strains of Listeria monocytogenes and Salmonella typhimurium planktonic cells biofilms with plasma activated liquids. Frontiers in Microbiology. 10: 1539 (2019)

    Article  PubMed  PubMed Central  Google Scholar 

  • Song X, Wang L, Liu T, Liu Y, Wu X, Liu L. Mandarin (Citrus reticulata L.) essential oil incorporated into chitosan nanoparticles: characterization, anti-biofilm properties and application in pork preservation. International Journal of Biological Macromolecules. 185: 620-628 (2021)

    Article  CAS  PubMed  Google Scholar 

  • Stankic S, Suman S, Haque F, Vidic J. Pure and multi metal oxide nanoparticles: synthesis, antibacterial and cytotoxic properties. Journal of Nanobiotechnology. 14: 73 (2016)

    Article  PubMed  PubMed Central  Google Scholar 

  • Stepanović S, Ćirković I, Ranin L, Svabić-Vlahović M. Biofilm formation by Salmonella spp. and Listeria monocytogenes on plastic surface. Letters in Applied Microbiology. 38: 428-432 (2004)

    Article  PubMed  Google Scholar 

  • Stöckel S, Schumacher W, Meisel S, Elschner M, Rösch P, Popp J. Raman spectroscopy-compatible inactivation method for pathogenic endospores. Applied and Environmental Microbiology. 76: 2895-2907 (2010)

    Article  PubMed  PubMed Central  Google Scholar 

  • Sun J, Wang D, Sun Z, Liu F, Du L, Wang D. The combination of ultrasound and chlorogenic acid to inactivate Staphylococcus aureus under planktonic, biofilm, and food systems. Ultrasonics Sonochemistry. 80: 105801 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Surya T, Jeyasekaran G, Shakila RJ, Alsalhi MS, Devanesan S, Sivaraman B, Arisekar U, Pham TH. Effect of antibiotics and sanitizers on Salmonella biofilms associated with seafood contact surfaces. Microbiological Research. 266: 127213 (2023)

    Article  CAS  PubMed  Google Scholar 

  • Syed QA, Ishaq A, Rahman UU, Aslam S, Shukat R. Pulsed electric field technology in food preservation: a review. Journal of Nutritional Health & Food Engineering. 6: 168-172 (2017)

    Google Scholar 

  • Sysolyatina EV, Lavrikova AY, Loleyt RA, Vasilieva EV, Abdulkadieva MA, Ermolaeva SA, Sofronov AV. Bidirectional mass transfer-based generation of plasma-activated water mist with antibacterial properties. Plasma Processes and Polymers. 17: 2000058 (2020)

    Article  CAS  Google Scholar 

  • Tan J, Karwe MV. Inactivation and removal of Enterobacter aerogenes biofilm in a model piping system using plasma-activated water (PAW). Innovative Food Science & Emerging Technologies. 69: 102664 (2021)

    Article  CAS  Google Scholar 

  • Tao H, Liao Q, Xu YI, Wang HL. Efficacy of slightly acidic electrolyzed water for inactivation of Cronobacter sakazakii and biofilm cells. Journal of Food Protection. 85: 511-517 (2022)

    Article  CAS  PubMed  Google Scholar 

  • Tariq S, Wani S, Rasool W, Shafi K, Bhat MA, Prabhakar A, Shalla AH, Rather MA. A comprehensive review of the antibacterial, antifungal and antiviral potential of essential oils and their chemical constituents against drug-resistant microbial pathogens. Microbial Pathogenesis. 134: 103580 (2019)

    Article  CAS  PubMed  Google Scholar 

  • Thomas AR, Mani R, Reddy TV, Ravichandran A, Sivakumar M, Krishnakumar S. Evaluation of the antibacterial efficiency of a combination of 1% alexidine and sodium hypochlorite on Enterococcus faecalis biofilm models: an in vitro study. The Journal of Contemporary Dental Practice. 20: 1090-1094 (2019)

    Article  PubMed  Google Scholar 

  • Torlak E, Sert D. Combined effect of benzalkonium chloride and ultrasound against Listeria monocytogenes biofilm on plastic surface. Letters in Applied Microbiology. 57: 220-226 (2013)

    Article  CAS  PubMed  Google Scholar 

  • Tran VN, Dasagrandhi C, Truong VG, Kim YM, Kang HW. Antibacterial activity of Staphylococcus aureus biofilm under combined exposure of glutaraldehyde, near-infrared light, and 405-nm laser. PLoS One. 13: e0202821 (2018)

    Article  PubMed  PubMed Central  Google Scholar 

  • Trinetta V, Vaidya N, Linton R, Morgan M. Evaluation of chlorine dioxide gas residues on selected food produce. Journal of Food Science. 76: T11-T15 (2011)

    Article  CAS  PubMed  Google Scholar 

  • Tsukatani T, Sakata F. Combined effects of fumaric, lactic, and ferulic acid against food-borne pathogenic biofilms. Food Control. 138: 109024 (2022)

    Article  CAS  Google Scholar 

  • Tursi SA, Puligedda RD, Szabo P, Nicastro LK, Miller AL, Qiu C, Gallucci S, Relkin NR, Buttaro BA, Dessain SK, Tükel, C. Salmonella Typhimurium biofilm disruption by a human antibody that binds a pan-amyloid epitope on curli. Nature Communications. 11: 1007 (2020)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vaidya SV, Yuan M, Narváez AR, Daghfal D, Mattzela J, Smith D. Protein-resistant properties of a chemical vapor deposited alkyl-functional carboxysilane coating characterized using quartz crystal microbalance. Applied Surface Science. 364: 896-908 (2016)

    Article  CAS  Google Scholar 

  • Vazquez-Armenta FJ, Hernandez-Oñate MA, Martinez-Tellez MA, Lopez-Zavala AA, Gonzalez-Aguilar GA, Gutierrez-Pacheco MM, Ayala-Zavala JF. Quercetin repressed the stress response factor (sigB) and virulence genes (prfA, actA, inlA, and inlC), lower the adhesion, and biofilm development of L. monocytogenes. Food Microbiology. 87: 103377 (2020)

    Article  CAS  PubMed  Google Scholar 

  • Verran J. Biofouling in food processing: biofilm or biotransfer potential? Food and Bioproducts Processing. 80: 292-298 (2002)

    Article  Google Scholar 

  • Vetas D, Dimitropoulou E, Mitropoulou G, Kourkoutas Y, Giaouris E. Disinfection efficiencies of sage and spearmint essential oils against planktonic and biofilm Staphylococcus aureus cells in comparison with sodium hypochlorite. International Journal of Food Microbiology. 257: 19-25 (2017)

    Article  CAS  PubMed  Google Scholar 

  • Vladkova TG, Staneva AD, Gospodinova DN. Surface engineered biomaterials and ureteral stents inhibiting biofilm formation and encrustation. Surface and Coatings Technology. 404: 126424 (2020)

    Article  CAS  Google Scholar 

  • Wahlen L, Parker A, Walker D, Pasmore M, Sturman P. Predictive modeling for hot water inactivation of planktonic and biofilm-associated Sphingomonas parapaucimobilis to support hot water sanitization programs. Biofouling. 32: 751-761 (2016)

    Article  CAS  Google Scholar 

  • Wang F, Wei F, Song C, Jiang B, Tian S, Yi J, Yu C, Song Z, Sun L, Bao Y, Wu, Y, Huang, Y, Li, Y. Dodartia orientalis L. essential oil exerts antibacterial activity by mechanisms of disrupting cell structure and resisting biofilm. Industrial Crops and Products. 109: 358-366 (2017)

    Article  CAS  Google Scholar 

  • Wang H, Cai L, Li Y, Xu X, Zhou G. Biofilm formation by meat-borne Pseudomonas fluorescens on stainless steel and its resistance to disinfectants. Food Control. 91: 397-403 (2018a)

    Article  CAS  Google Scholar 

  • Wang Q, Li Y, Sun D-W, Zhu Z. Enhancing food processing by pulsed and high voltage electric fields: principles and applications. Critical reviews in Food Science and Nutrition. 58: 2285-2298 (2018b)

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Sun L, Hu L, Wang Z, Wang X, Dong Q. Adhesion and kinetics of biofilm formation and related gene expression of Listeria monocytogenes in response to nutritional stress. Food Research International. 156: 111143 (2022)

    Article  CAS  PubMed  Google Scholar 

  • Watson F, Keevil CW, Wilks SA, Chewins J. Modelling vaporised hydrogen peroxide efficacy against mono-species biofilms. Scientific Reports. 8: 12257 (2018)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei W, Wang X, Xie Z, Wang W, Xu J, Liu Y, Gao H, Zhou Y. Evaluation of sanitizing methods for reducing microbial contamination on fresh strawberry, cherry tomato, and red bayberry. Frontiers in Microbiology. 8: 2397 (2017)

    Article  PubMed  PubMed Central  Google Scholar 

  • Xie X, Zhang Y, Zhang Y, Fu H, Gong M, Tian L, Fu Q. Study on the application of biocides in the seawater cooling system and their killing effect in the laboratory. Advances in Engineering. 100: 254-260 (2017)

    Google Scholar 

  • Xu H, Ma R, Zhu Y, Du M, Zhang H, Jiao Z. A systematic study of the antimicrobial mechanisms of cold atmospheric-pressure plasma for water disinfection. Science of the Total Environment. 703: 134965 (2020a)

    Article  CAS  PubMed  Google Scholar 

  • Xu Z, Zhou X, Yang W, Zhang Y, Ye Z, Hu S, Ye C, Li Y, Lan Y, Shen J, Ye, X, Yang, F, Cheng C. In vitro antimicrobial effects and mechanism of air plasma‐activated water on Staphylococcus aureus biofilm. Plasma Processes and Polymers. 17: 1900270 (2020b)

    Article  CAS  Google Scholar 

  • Xuan X, Ling J. Generation of electrolyzed water. In Electrolyzed Water in Food: Fundamentals and Applications. Edited by Ding T, Oh DH, Liu D. Springer Nature Singapore Pte Ltd. and Zhejiang University Press. 1-16 (2019)

  • Yan P, Chelliah R, Jo KH, Selvakumar V, Chen X, Jo HY, Oh DH. Stability and antibiofilm efficiency of slightly acidic electrolyzed water against mixed-species of Listeria monocytogenes and Staphylococcus aureus. Frontiers in Microbiology. 13: 865918 (2022)

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Hoe YW, Zheng Q, Chung HJ, Yuk HG. Biofilm formation by Salmonella Enteritidis in a simulated liquid egg processing environment and its sensitivity to chlorine and hot water treatment. Food Control. 73: 595-600 (2017)

    Article  CAS  Google Scholar 

  • Ye Z, Wang S, Chen T, Gao W, Zhu S, He J, Han Z. Inactivation mechanism of Escherichia coli induced by slightly acidic electrolyzed water. Scientific Reports. 7: 6279 (2017)

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu H, Liu Y, Li L, Guo Y, Xie Y, Cheng Y, Yao W. Ultrasound-involved emerging strategies for controlling foodborne microbial biofilms. Trends in Food Science & Technology. 96: 91-101 (2020)

    Article  CAS  Google Scholar 

  • Yu H, Liu Y, Yang F, Xie Y, Guo Y, Cheng Y, Yao W. Synergistic efficacy of high-intensity ultrasound and chlorine dioxide combination for Staphylococcus aureus biofilm control. Food Control. 122: 107822 (2021)

    Article  CAS  Google Scholar 

  • Yuan L, Hansen MF, Røder HL, Wang N, Burmølle M, He G. Mixed-species biofilms in the food industry: current knowledge and novel control strategies. Critical Reviews in Food Science and Nutrition. 60: 2277-2293 (2020)

    Article  PubMed  Google Scholar 

  • Zhang C, Brown PJB, Miles RJ, White TA, Grant DG, Stalla D, Hu Z. Inhibition of regrowth of planktonic and biofilm bacteria after peracetic acid disinfection. Water Research. 149: 640-649 (2019)

    Article  CAS  PubMed  Google Scholar 

  • Zhang C, Cui F, Zeng G, Jiang M, Yang Z, Yu Z, Zhu M, Shen L. Quaternary ammonium compounds (QACs): a review on occurrence, fate and toxicity in the environment. Science of the Total Environment. 518: 352-362 (2015)

    Article  PubMed  Google Scholar 

  • Zhang C, Brown PJB, Hu Z. Thermodynamic properties of an emerging chemical disinfectant, peracetic acid. The Science of the Total Environment. 621: 948-959 (2018)

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Chen SP, Seck HL, Zhou W. Low-energy X-ray inactivation of Salmonella Enteritidis on shell eggs in mono-/co-culture biofilms with Pseudomonas fluorescens. Food Control. 123: 107742 (2021a)

    Article  CAS  Google Scholar 

  • Zhang S, Wang Y, Lu J, Yu Z, Song H, Bond PL, Guo J. Chlorine disinfection facilitates natural transformation through ROS-mediated oxidative stress. The ISME Journal. 15: 2969-2985 (2021b)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Zhou W. Low-energy X-ray irradiation: A novel non-thermal microbial inactivation technology. Advances in Food and Nutrition Research. 100: 287-328 (2022)

    Article  PubMed  Google Scholar 

  • Zhang S, He Y, Sen B, Wang G. Reactive oxygen species and their applications toward enhanced lipid accumulation in oleaginous microorganisms. Bioresource Technology. 307: 123234 (2020)

    Article  CAS  PubMed  Google Scholar 

  • Zhang XS, García-Contreras R, Wood TK. YcfR (BhsA) influences Escherichia coli biofilm formation through stress response and surface hydrophobicity. Journal of Bacteriology. 189: 3051-3062 (2007)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao L, Li S, Yang H. Recent advances on research of electrolyzed water and its applications. Current Opinion in Food Science. 41: 180-188 (2021)

    Article  CAS  Google Scholar 

  • Zhao L, Poh CN, Wu J, Zhao X, He Y, Yang H. Effects of electrolysed water combined with ultrasound on inactivation kinetics and metabolite profiles of Escherichia coli biofilms on food contact surface. Innovative Food Science & Emerging Technologies. 76: 102917 (2022)

    Article  CAS  Google Scholar 

  • Zhao L, Zhang Y, Yang H. Efficacy of low concentration neutralised electrolysed water and ultrasound combination for inactivating Escherichia coli ATCC 25922, Pichia pastoris GS115 and Aureobasidium pullulans 2012 on stainless steel coupons. Food Control. 73: 889-899 (2017)

    Article  Google Scholar 

  • Zhou J, Velliou E, Hong SH. Investigating the effects of nisin and free fatty acid combined treatment on Listeria monocytogenes inactivation. LWT. 133: 110115 (2020)

    Article  CAS  Google Scholar 

  • Zhu Y, Li C, Cui H, Lin L. Feasibility of cold plasma for the control of biofilms in food industry. Trends in Food Science & Technology. 99: 142-151 (2020)

    Article  CAS  Google Scholar 

  • Ziuzina D, Han L, Cullen PJ, Bourke P. Cold plasma inactivation of internalised bacteria and biofilms for Salmonella enterica serovar Typhimurium, Listeria monocytogenes and Escherichia coli. International Journal of Food Microbiology. 210: 53-61 (2015)

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This study was carried out with support from the R&D Program for Forest Science Technology (Project No. 2021332C10-2123A01) provided by the Korea Forest Service (Korea Forestry Promotion Institute).

Author information

Author notes

  1. Ga-Hee Ban and Soo-Hwan Kim have contributed equally to this work.

Authors and Affiliations

  1. Department of Food Science and Biotechnology, Ewha Womans University, Seoul, 03760, Republic of Korea

    Ga-Hee Ban

  2. Department of Food and Animal Biotechnology, Department of Agricultural Biotechnology, Center for Food and Bioconvergence, Research Institute of Agricultural and Life Sciences, Seoul National University, Seoul, 08826, Republic of Korea

    Soo-Hwan Kim & Dong-Hyun Kang

  3. Department of Food Science and Technology, Kongju National University, Yesan, Chungnam, 32439, Republic of Korea

    Sang-Hyun Park

Authors
  1. Ga-Hee Ban
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Soo-Hwan Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dong-Hyun Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sang-Hyun Park
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sang-Hyun Park.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ban, GH., Kim, SH., Kang, DH. et al. Comparison of the efficacy of physical and chemical strategies for the inactivation of biofilm cells of foodborne pathogens. Food Sci Biotechnol 32, 1679–1702 (2023). https://doi.org/10.1007/s10068-023-01312-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10068-023-01312-2

Keywords

Search

Navigation