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A review of microbial biofilms of produce: Future challenge to food safety

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Abstract

Outbreaks of produce-related food-borne pathogens have undergone a sharp increase in last three decades because of high produce consumption. A paradigm of food safety for produce is important due to its susceptibility to microbial attack and biofilms formation. Greater attention should be paid to decontaminating the pathogens in biofilms as they pose a risk to public health. This review will focus on produce-related outbreaks, attachments, quorum sensing, biofilms formation, resistance to sanitizers and disinfectants, and current and emerging control strategies for fresh and minimally processed produce, providing new insight into food safety. The consequences of biofilms formation on produce include the formation of a protective environment that is resistant to cleaning and disinfection. Alternative means of controlling or inhibiting biofilms formation on produce will be explained briefly and we will identify where additional research is needed.

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References

  1. World Health Organization. Resolution WHA53.15 on food safety. 53rd World Health Assembly, Geneva, Switzerland. Available from: http://www.who.int/wha-l998/EB_WHA/PDF/WHA53/l5.pdf. Accessed Aug. 02, 2001.

  2. Stein C, Kuchenmuller T, Hendrickx S, Pruss-Ustun A, Wolfson L, Engels D, Schlundt J. The global burden of disease assessments — Who is responsible? PLoS Neglect. Trop. D. 1: e161 (2007)

    Article  Google Scholar 

  3. World Health Organization. Fact Sheet Number 237: Food safety and foodborne illness. Geneva, Switzerland: World Health Organization. Available from: http://www.who.int/mediacentre/factsheets/fs237/en/. Accessed Dec. 8, 2009.

  4. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson M, Roy SL, Jones JL, Griffin PM. Foodborne illness acquired in the United States-major pathogens. Emerg. Infect. Dis. 17: 7–15 (2011)

    Article  Google Scholar 

  5. Potera C. Forging a link between biofilms and disease. Science 283: 1837–1839 (1999)

    Article  CAS  Google Scholar 

  6. De Roever C. Microbiological safety evaluations and recommendations on fresh produce. Food Control 9: 321–347 (1998)

    Article  Google Scholar 

  7. Lund BM. Ecosystems in vegetable foods. J. Appl. Bacteriol. 73: 115S–135S (1992)

    Google Scholar 

  8. Harapas D, Premier R, Tomkins B, Franz P, Ajlouni S. Persistence of Escherichia coli on injured vegetable plants. Int. J. Food Microbiol. 138: 232–237 (2010)

    Article  Google Scholar 

  9. Natvig EE, Ingham SC, Ingham BH, Cooperband LR, Roper TR. Salmonella enterica Serovar Typhimurium and Escherichia coli contamination of root and leaf vegetables grown in soils with incorporated bovine manure. Appl. Environ. Microb. 68: 2737–2744 (2002)

    Article  CAS  Google Scholar 

  10. Erickson MC, Webb CC, Diaz-Perez JC, Phatak SC, Silvoy JJ, Davey L, Payton AS, Liao J, Ma L, Doyle MP. Surface and internalized Escherichia coli O157:H7 on field-grown spinach and lettuce treated with spray-contaminated irrigation water. J. Food Protect. 73: 1023–1029 (2010)

    Google Scholar 

  11. Taormina PJ, Beuchat LR, Slutsker L. Infections associated with eating seed sprouts: An international concern. Emerg. Infect. Dis. 5: 626–634 (1999)

    Article  CAS  Google Scholar 

  12. Jacobsen CS, Bech TB. Soil survival of Salmonella and transfer to freshwater and fresh produce. Food Res. Int. 45: 557–566 (2012)

    Article  Google Scholar 

  13. Burnett SL, Beuchat LR. Human pathogens associated with raw produce and unpasteurized juices, and difficulties in decontamination. J. Ind. Microbiol. Biot. 27: 104–110 (2001)

    Article  CAS  Google Scholar 

  14. United States Food and Drug Administration (USFDA). Guidance for industry: Guide to minimize microbial food safety hazards of fresh-cut fruits and vegetables. Available from: http://www.fda.gov/Food/guidanceComplianceRegulatoryInformation/GuidanceDocuments/ProduceandPlanProducts/ucm064458.htm. Accessed Mar. 9, 2007.

  15. Sanja I, Odomeru J, Jeffrey TL. Coliforms and prevalence of Escherichia coli and foodborne pathogens on minimally processed spinach in two packing plants. J. Food Protect. 71: 2398–2403 (2008)

    Google Scholar 

  16. Erickson MC. Microbial risks associated with cabbage, carrots, celery, onions, and deli salads made with these produce items. Compr. Rev. Food Sci. F. 9: 602–619 (2010)

    Article  Google Scholar 

  17. Hao YY, Brackett RE. Pectinase activity of vegetable spoilage bacteria in modified atmosphere. J. Food Sci. 59: 175–178 (1994)

    Article  CAS  Google Scholar 

  18. Caponigro V, Ventura M, Chiancone I, Amato L, Parente E, Piro F. Variation of microbial load and visual quality of ready-to-eat salads by vegetable type, season, processor, and retailer. Food Microbiol. 27: 1071–1077 (2010)

    Article  Google Scholar 

  19. Kim MG, Oh MH, Lee GY, Hwang IG, Kwak HS, Kang YS, Koh YH, Jun HK, Kwon KS. Analysis of major foodborne pathogens in various foods in Korea. Food Sci. Biotecnol. 17: 483–488 (2008)

    CAS  Google Scholar 

  20. Oliveira M, Wijnands L, Abadias M, Aarts H, Franz E. Pathogenic potential of Salmonella Typhimurium DT104 following sequential passage through soil, packaged fresh-cut lettuce, and a model gastrointestinal tract. Int. J. Food Microbiol. 148: 149–155 (2011)

    Google Scholar 

  21. European Commission. Risk Profile on the Microbiological Contamination of Fruits and Vegetables Eaten Raw. http://ec.europa.eu/food/fs/sc/scf/out125_en.pdf. Accessed Apr. 29, 2002.

  22. Morbidity and Mortality Weekly Report (MMWR). Surveillance for Foodborne Disease Outbreaks-United States, 2008. Available from: http://www.cdc.gov/mmwr/preview/mmwrhtml/mm6035a3.htm. Accessed Sep. 9, 2011.

  23. World Health Organization. Surface decontamination of fruits and vegetables eaten raw: A review. Prepared by L.R. Beuchat. Doc. WHO/FSF/FOS/98.2. Available from: http://www.who.int/foodsafety/publications/fs_management/en/surface_decon.pdf. Accessed Oct. 27, 2008.

  24. Food and Agriculture Organization/World Health Organization. Microbiological hazards in fresh fruits and vegetables. Meeting Reports. Microbiological Risk Assessment Series, No.14. Available from: http://www.fao.org/ag/agn/agns/jerma_riskassessment_fresh_produce_en.asp. Accessed Dec. 23, 2008.

  25. National Institute of Infectious Diseases and Infectious Diseases Control Division, Ministry of Health and Welfare of Japan. Verocytotoxin-producing Escherichia coli (enterohemorrhagic E. coli) infection, Japan, 1996–June 1997. Infect. Agents Surveill. Rep. 18: 153–154 (1997)

    Google Scholar 

  26. Pires SM, Vieira AR, Perez E, Wong DLF, Hald T. Attributing human foodborne illness to food sources and water in Latin America and the Caribbean using data from outbreak investigations. Int. J. Food Microbiol. 152: 129–138 (2012)

    Article  Google Scholar 

  27. Gwack J, Lee K, Lee HJ, Kwak W, Lee DW, Choi YH, Kim JS, Kang YA. Trends in water- and foodborne disease outbreaks in Korea, 2007–2009. Public Health Res. Perspect. 1: 50–54 (2010)

    Article  Google Scholar 

  28. United States Food and Drug Administration. Guidance for industry: Guide to minimize microbial food safety hazards of leafy greens; draft guidance. Available from: http://www.fda.gov/Food/GuidanceComplianceRegulatoryInformation/GuidanceDocuments/ProduceandPlanProducts/ucm174200.htm. Accessed Nov. 4, 2009.

  29. United States Food and Drug Administration. Guidance for industry: Guide to minimize microbial food safety hazards of melons; Draft Guidance. Available from: http://www.fda.gov/Food/GuidanceComplianceRegulatoryInformation/GuidanceDocuments/ProduceandPlanProducts/ucm174171.htm. Accessed Aug. 03, 2009.

  30. United States Food and Drug Administration. Guidance for industry: Guide to minimize microbial food safety hazards of tomatoes; draft guidance. Available from: http://www.fda.gov/Food/GuidanceComplianceRegulatoryInformation/GuidanceDocuments/ProduceandPlanProducts/ucm173902.htm. Accessed Aug. 03, 2009.

  31. Palmer J, Flint S, Brooks J. Bacterial cell attachment, the beginning of a biofilm. J. Ind. Microbiol. Biot. 34: 577–588 (2007)

    Article  CAS  Google Scholar 

  32. Ukuku DO, Fett WF. Effects of cell surface charge and hydrophobicity on atatchemnts of 16 Salmonella serovars to cantaloupe rind and decontamination with sanitizers. J. Food Protect. 69: 1835–1843 (2006)

    Google Scholar 

  33. Pratt LA, Kolter R. Genetic analyses of bacterial biofilm formation. Curr. Opin. Microbiol. 2: 598–603 (1999)

    Article  CAS  Google Scholar 

  34. Ukuku DO, Fett WF. Relationship of cell surface charge and hydrophobicity to strength of attachment of bacteria to cantaloupe. J. Food Protect. 65: 1093–1099 (2002)

    Google Scholar 

  35. Mandrell RE, Gorski L, Brandl MT. Attachment of microorganisms to fresh produce. pp. 50–91. In: Microbiology of Fruits and Vegetables. Sapers GM, Gorny JR, Yousuf AE (eds). CRC Press, Inc., Boca Raton, FL, USA (2006)

    Google Scholar 

  36. Barak JD, Gorski L, Naraghi-Arani P, Charkowski AO. Salmonella enterica virulence genes are required for bacterial attachment to plant tissue. Appl. Environ. Microb. 71: 5685–5691 (2005)

    Article  CAS  Google Scholar 

  37. Barak JD, Jahn CE, Gibson DL, Charkowski AO. The role of cellulose and O-antigen capsule in the colonization of plants by Salmonella enterica. Mol. Plant Microbe In. 20: 1083–1091 (2007)

    Article  CAS  Google Scholar 

  38. Patel J, Sharma M, Ravishakar S. Effect of curli expression and hydrophobicity of Escherichia coli O157:H7 on attachment to fresh produce surfaces. J. Appl. Microbiol. 110: 737–745 (2011)

    Article  CAS  Google Scholar 

  39. Ryu JH, Beuchat LR. Biofilm formation by Escherichia coli O157:H7 on stainless steel: Effect of exopolysaccharide and Curli production on its resistance to chlorine. Appl. Environ. Microb. 71: 247–254 (2005)

    Article  CAS  Google Scholar 

  40. Han Y, Sherman DM, Linton RH, Nielsen SS, Nelson PE. The effects of washing and chlorine dioxide gas on survival and attachment of Escherichia coli O157: H7 to green pepper surfaces. Food Microbiol. 17: 521–533 (2000)

    Article  CAS  Google Scholar 

  41. Reina LD, Fleming HP, Breidt JRF. Bacterial contamination of cucumber fruit through adhesion. J. Food Protect. 65: 1881–1887 (2002)

    Google Scholar 

  42. Ells TC, Hansen LT. Strain and growth temperature influence Listeria spp. attachment to intact and cut cabbage. Int. J. Food Microbiol. 111: 34–42 (2006)

    Article  Google Scholar 

  43. Hassan AN, Frank JF. Attachment of Escherichia coli O157:H7 grown in tryptic soy broth and nutrient broth to apple and lettuce surfaces as related to cell hydrophobicity, surface charge, and capsule production. Int. J. Food Microbiol. 96: 103–109 (2004)

    Article  CAS  Google Scholar 

  44. Patel J, Sharma M. Differences in attachment of Salmonella enterica serovars to cabbage and lettuce leaves. Int. J. Food Microbiol. 139: 41–47 (2010)

    Article  Google Scholar 

  45. Sperandio V, Torres AG, Jarvis B, Nataro JP, Kaper JB. Bacteriahost communication: The language of hormones. P. Natl. Acad. Sci. USA 100: 8951–8956 (2003)

    Article  CAS  Google Scholar 

  46. Parsek MR, Greenberg EP. Sociomicrobiology: The connections between quorum sensing and biofilms. Trends Microbiol. 13: 27–33 (2005)

    Article  CAS  Google Scholar 

  47. Miller MB, Bassler BL. Quorum sensing in bacteria. Ann. Rev. Microbiol. 55: 165–199 (2001)

    Article  CAS  Google Scholar 

  48. Bai AJ, Rai VR. Bacterial quorum sensing and food industry. Compr. Rev. Food Sci. F. 10: 183–193 (2011)

    Article  CAS  Google Scholar 

  49. Smith JL, Fratamico PM, Novak JS. Quorum sensing: A primer for food microbiologists. J. Food Protect. 67: 1053–1070 (2004)

    CAS  Google Scholar 

  50. Rasch M, Andersen JB, Nielsen KF, Flodgaard LR, Christensen H, Givskov M, Gram L. Involvement of bacterial quorum-sensing signals in spoilage of bean sprouts. Appl. Environ. Microb. 71: 3321–3330 (2005)

    Article  CAS  Google Scholar 

  51. Silagyi K, Kim SH, Lo YM, Wei CI. Production of biofilm and quorum sensing by Escherichia coli O157:H7 and its transfer from contact surfaces to meat, poultry, ready-to-eat deli, and produce products. Food Microbiol. 26: 514–519 (2009)

    Article  CAS  Google Scholar 

  52. Moons P, Van Houdt R, Aertsen A, Vanoirbeek K, Engelborghs Y, Michiels CW. Role of quorum sensing and antimicrobial component production by Serratia plymuthica in formation of biofilms including mixed biofilms with Escherichia coli. Appl. Environ. Microb. 72: 7294–7300 (2006)

    Article  CAS  Google Scholar 

  53. Cataldi TRI, Bianco G, Palazzo L, Quaranta V. Occurrence of N-acyl-l-homoserine lactones in extracts of some Gram-negative bacteria evaluated by gas chromatography-mass spectrometry. Anal. Biochem. 361: 226–235 (2007)

    Article  CAS  Google Scholar 

  54. Schauder S, Shokat K, Surette MG, Bassler BL. The LuxS family of bacterial autoinducers: Biosynthesis of a novel quorum-sensing signal molecule. Mol. Microbiol. 41: 463–476 (2001)

    Article  CAS  Google Scholar 

  55. Lu L, Hume ME, Pillai SD. Autoinducer-2-like activity on vegetable produce and its potential involvement in bacterial biofilm formation on tomatoes. Foodborne Pathog. Dis. 2: 242–249 (2005)

    Article  Google Scholar 

  56. Gram L, Christensen AB, Ravn L, Molin S, Givskov M. Production of acylated homoserine lactones by psychrotrophic members of the Enterobacteriaceae isolated from foods. Appl. Environ. Microb. 65: 3458–3463 (1999)

    CAS  Google Scholar 

  57. Van Houdt R, Moons P, Jansen A, Vanoirbeek K, Michiels CW. Genotypic and phenotypic characterization of a biofilm-forming Serratia plymuthica isolate from a raw vegetable processing line. FEMS. Microbiol. Lett. 246: 265–272 (2005)

    Article  CAS  Google Scholar 

  58. Abee T, Kova’cs AT, Kuipers OP, Veen S. Biofilm formation and dispersal in Gram-positive bacteria. Curr. Opin. Biotechnol. 22: 172–179 (2011)

    Article  CAS  Google Scholar 

  59. Morris CE, Monier JM, Jacques MA. Methods for observing microbial biofilms directly on leaf surfaces and recovering them for isolation of culturable microorganisms. Appl. Environ. Microb. 63: 1570–1576 (1997)

    CAS  Google Scholar 

  60. Stewart PS, McFeters GA, Huang CT. Biofilm control by antimicrobial agents. pp.373–405. In: Biofilms II: Process Analysis and Applications. Bryers JD (ed). Wiley-Liss, New York, NY, USA (2000)

    Google Scholar 

  61. Danese PN, Pratt LA, Kolter R. Exopolysaccharide production is required for development of Escherichia coli K-12 biofilm architecture. J. Bacteriol. 182: 3593–3596 (2000)

    Article  CAS  Google Scholar 

  62. Houdt RV, Michiels CW. Biofilm formation and the food industry, a focus on the bacterial outer surface. J. Appl. Microbiol. 109: 1117–1131 (2010)

    Article  Google Scholar 

  63. Rayner J, Veeh R, Flood J. Prevalence of microbial biofilms on selected fresh produce and household surfaces. Int. J. Food. Microbiol. 95: 29–39 (2004)

    Article  CAS  Google Scholar 

  64. Davey ME, O’Toole GA. Microbial biofilms: From ecology to molecular genetics. Microbiol. Mol. Biol. Rev. 64: 847–867 (2000)

    Article  CAS  Google Scholar 

  65. Stoodley P, DeBeer D, Lewandowski Z. Liquid flow in biofilm systems. Appl. Environ. Microb. 60: 2711–2716 (1994)

    CAS  Google Scholar 

  66. Stapper AP, Narasimhan G, Ohman DE, Barakat J, Hentzer M, Molin S, Kharazmi A, Høiby N, Mathee K. Alginate production affects Pseudomonas aeruginosa biofilm development and architecture, but is not essential for biofilm formation. J. Med. Microbiol. 53: 679–690 (2004)

    Article  CAS  Google Scholar 

  67. Kaplan B. Biofilm dispersal: Mechanisms, clinical implications, and potential therapeutic uses. J. Dent. Res. 89: 205–218 (2010)

    Article  CAS  Google Scholar 

  68. Mai-Prochnow A, Webb JS, Ferrari BC, Kjelleberg S. Ecological advantages of autolysis during the development and dispersal of Pseudoalteromonas tunicata biofilms. Appl. Environ. Microb. 72: 5414–5420 (2006)

    Article  CAS  Google Scholar 

  69. Hunt SM, Werner EM, Huang B, Hamilton MA, Stewart PS. Hypothesis for the role of nutrient starvation in biofilm detachment. Appl. Environ. Microb. 70: 7418–7425 (2004)

    Article  CAS  Google Scholar 

  70. Lindow SE, Brandl MT. Microbiology of the phyllosphere. Appl. Environ. Microb. 69: 1875–1883 (2003)

    Article  CAS  Google Scholar 

  71. Morris CE, Monier JM, Jacques MA. A technique to quantify the population size and composition of the biofilm component in communities of bacteria in the phyllosphere. Appl. Environ. Microb. 64: 4789–4795 (1998)

    CAS  Google Scholar 

  72. Fett WF. Naturally occurring biofilms on alfalfa and other types of sprouts. J. Food Protect. 63: 625–632 (2000)

    CAS  Google Scholar 

  73. Rudi K, Flateland SL, Hanssen JF, Bengtsson G, Nissen H. Development and evaluation of a 16S ribosomal DNA array-based approach for describing complex microbial communities in ready-to-eat vegetable salads packed in a modified atmosphere. Appl. Environ. Microb. 68: 1146–1156 (2002)

    Article  CAS  Google Scholar 

  74. Ölmez H, Temur SD. Effects of different sanitizing treatments on biofilms and attachment of Escherichia coli and Listeria monocytogenes on green leaf lettuce. LWT-Food. Sci. Technol. 43: 964–970 (2010)

    Article  CAS  Google Scholar 

  75. 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. Int. J. Food Microbiol. 132: 134–140 (2009)

    Article  CAS  Google Scholar 

  76. Burnett SL, Chen J, Beuchat LR. Attachment of Escherichia coli O157:H7 to the surfaces and internal structures of apples as detected by confocal scanning laser microscopy. Appl. Environ. Microb. 66: 4679–4687 (2000)

    Article  CAS  Google Scholar 

  77. Niemira BA, Cooke PH. Escherichia coli O157:H7 biofilm formation on Romaine lettuce and spinach leaf surfaces reduces efficacy of irradiation and sodium hypochlorite washes. J. Food Sci. 75: M270–M277 (2010)

    Article  CAS  Google Scholar 

  78. Niemira BA, Sommers CH, Ukuku D. Mechanisms of microbial spoilage of fruits and vegetables. pp. 463–482. In: Produce Degradation: Reaction Pathways and Their Prevention. Lamikanra O, Imam SH, Ukuku DO (eds). CRC Press, New York, NY, USA (2005)

    Google Scholar 

  79. Warner JC, Rothwell SD, Keevil CW. Use of episcopic differential interference contrast microscopy to identify bacterial biofilms on salad leaves and track colonization by Salmonella Thompson. Environ. Microbiol. 10: 918–925 (2008)

    Article  CAS  Google Scholar 

  80. Food and Drug Administration. Preliminary studies on the potential for infiltration, growth and survival of Salmonella enterica serovar Hartford and Escherichia coli O157:H7 within oranges. Available from: http://www.fda.gov/Food/FoodSafety/HazardAnalysisCriticalControlPointsHACCP/JuiceHACCP/ucm082650.htm. Accessed Jun. 18, 2009.

  81. Fransisca L, Zhou B, Park H, Feng H. The effect of calcinated calcium and chlorine treatments on Escherichia coli O157:H7 87-23 population reduction in radish sprouts. J. Food Sci. 76: M404–M412 (2011)

    Article  CAS  Google Scholar 

  82. Liao CH, Cooke PH. Response to trisodium phosphate treatment of Salmonella Chester attached to fresh-cut green pepper slices. Can. J. Microbiol. 47: 25–32 (2001)

    CAS  Google Scholar 

  83. Khalil RK, Frank JF. Behavior of Escherichia coli O157:H7 on damaged leaves of spinach, lettuce, cilantro, and parsley stored at abusive temperatures. J. Food Protect. 73: 212–220 (2010)

    Google Scholar 

  84. Seo KH, Frank JF. Attachment of Escherichia coli O157:H7 to lettuce leaf surface and bacterial viability in response to chlorine treatment as demonstrated by using confocal scanning laser microscopy. J. Food Protect. 62: 3–9 (1999)

    CAS  Google Scholar 

  85. Donlan RM. Biofilms: Microbial life on surfaces. Emerg. Infect. Dis. 8: 881–890 (2002)

    Article  Google Scholar 

  86. Fuster-Valls N, Herna’ndez-Herrero M, Marý’n-de-Mateo M, Rodrý’guez-Jerez JJ. Effect of different environmental conditions on the bacteria survival on stainless steel surfaces. Food Control 19: 308–314 (2008)

    Article  CAS  Google Scholar 

  87. Lim J, Lee KM, Kim SH, Nam SW, Oh YJ, Yun HS, Jo W, Oh S, Kim SH, Park S. Nanoscale characterization of Escherichia coli biofilm formed under laminar flow using atomic force microscopy (AFM) and scanning electron microscopy (SEM). Bull. Korean Chem. Soc. 29: 2114–2118 (2008)

    Article  CAS  Google Scholar 

  88. Fett WF, Cooke PH. A survey of native microbial aggregates on alfalfa, clover, and mung bean sprout cotyledons for thickness as determined by confocal scanning laser microscopy. Food Microbiol. 22: 253–259 (2005)

    Article  Google Scholar 

  89. Neu TR, Manz B, Volke F, Dynes JJ, Hitchcock AP, Lawrence JR. Advanced imaging techniques for assessment of structure, composition, and function in biofilm systems. FEMS Microbiol. Ecol. 72: 1–21 (2010)

    Article  CAS  Google Scholar 

  90. Gamble R, Muriana PM. Microplate fluorescence assay for measurement of the ability of strains of Listeria monocytogenes from meat and meat-processing plants to adhere to abiotic surfaces. Appl. Environ. Microb. 73: 5235–5244 (2007)

    Article  CAS  Google Scholar 

  91. Mariscal A, Lopez-Gigosos RM, Carnero-Varo M, Fernandez-Crehuet J. Fluorescent assay based on resazurin for detection of activity of disinfectants against bacterial biofilm. Appl. Microbiol. Biot. 82: 773–783 (2009)

    Article  CAS  Google Scholar 

  92. Rodrigues AC, Wuertz S, Brito AG, Melo LF. Three-dimensional distribution of GFP-labeled Pseudomonas putida during biofilm formation on solid PAHs assessed by confocal laser scanning microscopy. Water Sci. Technol. 47: 139–142 (2003)

    CAS  Google Scholar 

  93. Lapidot A, Romling U, Yaron S. Biofilm formation and the survival of Salmonella Typhimurium on parsley. Int. J. Food Microbiol. 109: 229–233 (2006)

    Article  CAS  Google Scholar 

  94. Peneau S, Chassaing D, Carpentier B. First evidence of division and accumulation of viable but nonculturable Pseudomonas fluorescens cells on surfaces subjected to conditions encountered at meat processing premises. Appl. Environ. Microb. 73: 2839–2846 (2007)

    Article  CAS  Google Scholar 

  95. Lee J, Kim IS, Yu HW. Flow cytometric detection of Bacillus spoOA gene in biofilm using quantum dot labeling. Anal. Chem. 82: 2836–2843 (2010)

    Article  CAS  Google Scholar 

  96. Ali L, Khambaty F, Diachenko G. Investigating the suitability of the Calgary Biofilm Device for assessing the antimicrobial efficacy of new agents. Bioresource Technol. 97: 1887–1893 (2006)

    Article  CAS  Google Scholar 

  97. Almeida C, Azevedo NF, Santos S, Keevil CW, Vieira MJ. Discriminating multi-species populations in biofilms with peptide nucleic acid fluorescence in situ hybridization (PNA FISH. PLoS. One 6: e14786 (2011)

    Article  CAS  Google Scholar 

  98. Yashiro E, Spear RN, McManus PS. Culture-dependent and culture-independent assessment of bacteria in the apple phyllosphere. J. Appl. Microbiol. 110: 1284–1296 (2011)

    Article  CAS  Google Scholar 

  99. Gibson H, Taylor JH, Hall KE, Holah JT. Effectiveness of cleaning techniques used in the food industry in terms of the removal of bacterial biofilms. J. Appl. Microbiol. 87: 41–49 (1999)

    Article  CAS  Google Scholar 

  100. Donlan RM, Costerton JW. Biofilms: Survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15: 167–193 (2002)

    Article  CAS  Google Scholar 

  101. Davies D. Understanding biofilm resistance to antibacterial agents. Nat. Rev. Drug Discov. 2: 114–122 (2003)

    Article  CAS  Google Scholar 

  102. ASTM E2197-11. Standard Quantitative Disk Carrier Test Method for Determining the Bactericidal, Virucidal, Fungicidal, Mycobactericidal, and Sporicidal Activities of Liquid Chemical Germicides. Avialable from: http://www.astm.org/Standards/E2197.htm. Accessed Jan. 01, 2011.

  103. European Committee for Standardization (CEN). Chemical disinfectants and antiseptics-quantitative suspension test for the evaluation of bactericidal activity of chemical disinfectants and antiseptics used in food, industrial, domestic, and institutional areas-test method and requirements (phase 2, step 1) (Standard No. EN 1276:2009). Accessed Dec. 22, 2009.

  104. ASTM E2799-11. Standard Test Method for Testing Disinfectant Efficacy against Pseudomonas aeruginosa Biofilm using the MBEC Assay. Available from: http://www.astm.org/Standards/E2799.htm. Accessed Jan. 4, 2011.

  105. Keskinen LA, Annous BA. Efficacy of adding detergents to sanitizer solutions for inactivation of Escherichia coli O157:H7 on Romaine lettuce. Int. J. Food Microbiol. 147: 157–161 (2011)

    Article  CAS  Google Scholar 

  106. Issa-Zacharia A, Kamitani Y, Tiisekwa A, Morita K, Iwasaki K. In vitro inactivation of Escherichia coli, Staphylococcus aureus, and Salmonella spp. using slightly acidic electrolyzed water. J. Biosci. Bioeng. 110: 308–313 (2010)

    Article  CAS  Google Scholar 

  107. Chang SS, Redondo-Solano M, Thippareddi H. Inactivation of Escherichia coli O157:H7 and Salmonella spp. on alfalfa seeds by caprylic acid and monocaprylin. Int. J. Food Microbiol. 144: 141–146 (2010)

    Article  CAS  Google Scholar 

  108. López-Gálvez F, Gil MI, Truchado P, Selma MV, Allende A. Cross-contamination of fresh-cut lettuce after a short-term exposure during pre-washing cannot be controlled after subsequent washing with chlorine dioxide or sodium hypochlorite. Food Microbiol. 27: 199–204 (2010)

    Article  CAS  Google Scholar 

  109. Nthenge AK, Weese JS, Carter M, Wei CI, Huang TS. Efficacy of γ radiation and aqueous chlorine on Escherichia coli O157:H7 in hydroponically grown lettuce plants. J. Food Protect. 70: 748–752 (2007)

    Google Scholar 

  110. Niemira BA. Relative efficacy of sodium hypochlorite wash vs. irradiation to inactivate Escherichia coli O157:H7 internalized in leaves of romaine lettuce and baby spinach. J. Food Protect. 70: 2526–2532 (2007)

    Google Scholar 

  111. Schmidt HM, Palekar MP, Maxim JE, Castillo A. Improving the microbiological quality and safety of fresh-cut tomatoes by lowdose electron beam irradiation. J. Food Protect. 69: 575–581 (2006)

    Google Scholar 

  112. Ukuku DO, Bari ML, Kawamoto S, Isshiki K. Use of hydrogen peroxide in combination with nisin, sodium lactate, and citric acid for reducing transfer of bacterial pathogens from whole melon surfaces to fresh-cut pieces. Int. J. Food Microbiol. 104: 225–233 (2005)

    Article  CAS  Google Scholar 

  113. Ukuku DO, Fett WF. Effect of nisin in combination with EDTA, sodium lactate, and potassium sorbate for reducing Salmonella on whole and fresh-cut cantaloupe. J. Food Protect. 67: 2143–2150 (2004)

    CAS  Google Scholar 

  114. Ukuku DO, Sapers GM. Effect of sanitizer treatments on Salmonella Stanley attached to the surface of cantaloupe and cell transfer to fresh-cut tissues during cutting practices. J. Food Protect. 64: 1286–1291 (2001)

    CAS  Google Scholar 

  115. Liao CH, Cooke PH. Response to trisodium phosphate treatment of Salmonella Chester attached to fresh-cut green pepper slices. Can. J. Microbiol. 47: 25–32 (2001)

    CAS  Google Scholar 

  116. Kenney SJ, Beuchat LR. Comparison of aqueous commercial cleaners for effectiveness in removing Escherichia coli O157:H7 and Salmonella muenchen from the surface of apples. Int. J. Food Microbiol. 74: 47–55 (2002)

    Article  CAS  Google Scholar 

  117. Rutala WA, Weber DJ. The Healthcare Infection Control Practices Advisory Committee. CDC guideline for disinfection and sterilization in healthcare facilities. Available from: http://www.cdc.gov/ncidod/dhqp/pdf/guidelines/Disinfection_Nov_2008.pdf. Accessed Oct. 14, 2009.

  118. Food and Drug Administration. Guidance for industry: Reducing microbial food safety hazards for sprouted seeds. Available from: http://vm.cfsan.fda.gov/~dms/sproud1.html. Accssed Oct. 27, 1999.

  119. Brandl MT, Mandrell RE. Fitness of Salmonella enterica serovar Thompson in the cilantro phyllosphere. Appl. Environ. Microb. 68: 3614–3621 (2002)

    Article  CAS  Google Scholar 

  120. Stewart D, Reineke K, Ulaszek J, Fu T, Tortorello M. Growth of Escherichia coli O157:H7 during sprouting of alfalfa seeds. Lett. Appl. Microbiol. 33: 95–99 (2001)

    Article  CAS  Google Scholar 

  121. Warriner K, Spaniolas S, Dickinson M, Wright C, Waites WM. Internalization of bioluminescent Escherichia coli and Salmonella Montevideo in growing bean sprouts. J. Appl. Microbiol. 95: 719–727 (2003)

    Article  CAS  Google Scholar 

  122. Sapers GM, Sites JE. Efficacy of 1% hydrogen peroxide wash in decontaminating apples and cantaloupe melons. J. Food Sci. 68: 1793–1797 (2003)

    Article  CAS  Google Scholar 

  123. Joseph B, Otta SK, Karunasagar I, Karunasagar I. Biofilm formation by Salmonella spp. on food contact surfaces and their sensitivity to sanitizers. Int. J. Food Microbiol. 64: 367–372 (2001)

    Article  CAS  Google Scholar 

  124. Behnke S, Parker AE, Woodall D, Camper AK. Comparing the chlorine disinfection of detached biofilm clusters with sessile biofilms and planktonic cells in single and dual species cultures. Appl. Environ. Microb. 77: 7176–7784 (2011)

    Article  CAS  Google Scholar 

  125. Weiss A, Hammes WP. Efficiency of heat treatment in the reduction of Salmonellae and Escherichia coli O157:H7 on alfalfa, mung bean, and radish seeds used for sprout production. Eur. Food Res. Technol. 221: 187–191 (2005)

    Article  CAS  Google Scholar 

  126. Luppens SB, Reij MW, van der Heijden RW, Rombouts FM, Abee T. Development of a standard test to assess the resistance of Staphylococcus aureus biofilm cells to disinfectants. Appl. Environ. Microb. 68: 4194–4200 (2002)

    Article  CAS  Google Scholar 

  127. Robbins JB, Fisher CW, Moltz AG, Martin SE. Elimination of Listeria monocytogenes biofilms by ozone, chlorine, and hydrogen peroxide. J. Food Protect. 68: 494–498 (2005)

    CAS  Google Scholar 

  128. Wirtanen G, Mattila-Sandholm T. Effect of the growth phase of foodborne biofilms on their resistance to a chlorine sanitizer. II. Lebensm. -Wiss. Technol. 25: 50–54 (1992)

    CAS  Google Scholar 

  129. Sommer P, Martin-Rouas C, Mettler, E. Influence of the adherent population level on biofilm population, structure, and resistance to chlorination. Food Microbiol. 16: 503–515 (1999)

    Article  CAS  Google Scholar 

  130. Mangalappalli-Illathu AK, Vidoviæ S, Korber DR. Differential adaptive response and survival of Salmonella enterica serovar enteritidis planktonic and biofilm cells exposed to benzalkonium chloride. Antimicrob. Agents Ch. 52: 3669–3680 (2008)

    Article  CAS  Google Scholar 

  131. Hall-Stoodley L, Costerton JW, Stoodley P. Bacterial biofilms: From the natural environment to infectious diseases. Nat. Rev. Microbiol. 2: 95–108 (2004)

    Article  CAS  Google Scholar 

  132. Percival SL, Walker JT, Hunter PR. Microbiological Aspects on Biofilms and Drinking Water. CRC Press LLC, Boca Raton, FL, USA. pp. 15–17 (2000)

    Book  Google Scholar 

  133. Manuzon MY, Wang HH. Mixed culture biofilms. pp.105–125. In: Biofilms in Food Environment. Blaschek HP, Wang HH, Agle ME (eds). Blackwell Publishing Ltd., Ames, IA, USA (2007)

    Google Scholar 

  134. Mah TF, O’Toole GA. Mechanisms of biofilm resistance to antimicrobial agents. Trends. Microbiol. 9: 34–39 (2001)

    Article  CAS  Google Scholar 

  135. Gilbert P, Allison DG, McBain AJ. Biofilms in vitro and in vivo: Do singular mechanisms imply cross-resistance? J. Appl. Microbiol. 92: 98S–110S (2002)

    Article  Google Scholar 

  136. del Pozo JL, R Patel R. The challenge of treating biofilm-associated bacterial infections. Clin. Pharmacol. Ther. 82: 204–209 (2007)

    Article  CAS  Google Scholar 

  137. Stewart PS, Mukkerjee PK, Ghannoum MA. Biofilm antimicrobial resistance. pp. 250–268. In: Microbial Biofilms. Ghannoum MA, O’Toole GA (eds). ASM Press, Washington, DC, USA (2004)

    Google Scholar 

  138. Leriche V, Briandet R, Carpentier B. Ecology of mixed biofilms subjected daily to a chlorinated alkaline solution: Spatial distribution of bacterial species suggests a protective effect of one species to another. Environ. Microbiol. 5: 64–71 (2003)

    Article  CAS  Google Scholar 

  139. Burmølle M, Webb JS, Rao D, Hansen LH, Sørensen SJ, Kjelleberg S. Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms. Appl. Environ. Microb. 72: 3916–3923 (2006)

    Article  CAS  Google Scholar 

  140. Chorianopoulos NG, Giaouris ED, Skandamis PN, Haroutounian SA, Nychas GJ. Disinfectant test against monoculture and mixed-culture biofilms composed of technological, spoilage, and pathogenic bacteria: Bactericidal effect of essential oil and hydrosol of Satureja thymbra and comparison with standard acid-base sanitizers. J. Appl. Microbiol. 104: 1586–1596 (2008)

    Article  CAS  Google Scholar 

  141. Shu M, Browngardt CM, Chen YY, Burne RA. Role of urease enzymes in stability of a 10-species oral biofilm consortium cultivated in a constant-depth film fermenter. Infect. Immun. 71: 7188–7192 (2003)

    Article  CAS  Google Scholar 

  142. McDonnell G, Russell AD. Antiseptics and disinfectants: Activity, action, and resistance. Clin. Microbiol. Rev. 12: 147–179 (1999)

    CAS  Google Scholar 

  143. Chapman JS. Disinfectant resistance mechanisms, cross-resistance, and co-resistance. Int. Biodeter. Biodegr. 51: 271–276 (2003)

    Article  CAS  Google Scholar 

  144. Davison WM, Pitts B, Stewart PS. Spatial and temporal patterns of biocide action against Staphylococcus epiderismidis biofilms. Antimicrob. Agents Ch. 54: 2920–2927 (2010)

    Article  CAS  Google Scholar 

  145. Toté K, Horemans T, Vanden Berghe D, Maes L, Cos P. Inhibitory effect of biocides on the viable masses and matrices of Staphylococcus aureus and Pseudomonas aeruginosa biofilms. Appl. Environ. Microb. 76: 3135–3142 (2010)

    Article  CAS  Google Scholar 

  146. Sutherland IW. Microbial biofilm exopolysaccharides-superglues or velcro? pp. 33–39. In: Biofilms Community Interactions and Control. Winpenny J, Handley P, Gilbert P, Lappin-Scott H, Jones M (eds). Bioline Publications, Chippenham, UK (1997)

    Google Scholar 

  147. Hoyle BD, Wong CK, Costerton JW. Disparate efficacy of tobramycin on Ca(2+)-, Mg(2+)-, and HEPES-treated Pseudomonas aeruginosa biofilms. Can. J. Microbiol. 38: 1214–1218 (1992)

    Article  CAS  Google Scholar 

  148. Larsen P, Nielsen JL, Dueholm MS, Wetzel R, Otzen D, Nielsen PH. Amyloid adhesins are abundant in natural biofilms. Environ. Microbiol. 9: 3077–3090 (2007)

    Article  CAS  Google Scholar 

  149. Ahimou F, Semmens MJ, Haugstad G, Novak PJ. Effect of protein, polysaccharide, and oxygen concentration profiles on biofilm cohesiveness. Appl. Environ. Microb. 73: 2905–2910 (2007)

    Article  CAS  Google Scholar 

  150. Boles BR, Singh PK. Endogenous oxidative stress produces diversity and adaptability in biofilm communities. P. Natl. Acad. Sci. USA 105: 12503–12508 (2008)

    Google Scholar 

  151. Stewart PS, Franklin MJ. Physiological heterogeneity in biofilms. Nat. Rev. Microbiol. 6: 199–210 (2008)

    Article  CAS  Google Scholar 

  152. Sauer K, Camper AK, Ehrlich GD, Costerton JW, Davies DG. Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J. Bacteriol. 184: 1140–1154 (2002)

    Article  CAS  Google Scholar 

  153. Walters MC III, Roe F, Bugnicourt A, Franklin MJ, Stewart PS. Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob. Agents Ch. 47: 317–323 (2003)

    Article  CAS  Google Scholar 

  154. Rani SA, Pitts B, Beyenal H, Veluchamy RA, Lewandowski Z, Davison WM, Buckingham-Meyer K, Stewart PS. Spatial patterns of DNA replication, protein synthesis, and oxygen concentration within bacterial biofilms reveal diverse physiological states. J. Bacteriol. 189: 4223–4233 (2007)

    Article  CAS  Google Scholar 

  155. van der Veen S, Abee T. Importance of SigB for Listeria monocytogenes static and continuous-flow biofilm formation and disinfectant resistance. Appl. Environ. Microb. 76: 7854–7860 (2010)

    Article  CAS  Google Scholar 

  156. Schwab U, Hu Y, Wiedmann M, Boor KJ. Alternative sigma factor sigmaB is not essential for Listeria monocytogenes surface attachment. J. Food Protect. 68: 311–317 (2005)

    Google Scholar 

  157. Pérez-Osorio AC, Williamson KS, Franklin MJ. Heterogeneous rpoS and rhlR mRNA levels and 16S rRNA/rDNA (rRNA gene) ratios within Pseudomonas aeruginosa biofilms, sampled by laser capture microdissection. J. Bacteriol. 192: 2991–3000 (2010)

    Article  CAS  Google Scholar 

  158. Ando T, Itakura S, Uchii K, Sobue R, Maeda S. Horizontal transfer of non-conjugative plasmid in colony biofilm of Escherichia coli on food-based media. World J. Microbiol. Biot. 25: 1865–1869 (2009)

    Article  Google Scholar 

  159. Reisner A, Höller BM, Molin S, Zechner EL. Synergistic effects in mixed Escherichia coli biofilms: Conjugative plasmid transfer drives biofilm expansion. J. Bacteriol. 188: 3582–3588 (2006)

    Article  CAS  Google Scholar 

  160. Mølbak L, Licht TR, Kvist T, Kroer N, Andersen SR. Plasmid transfer from Pseudomonas putida to the indigenous bacteria on alfalfa sprouts: Characterization, direct quantification, and in situ location of transconjugant cells. Appl. Environ. Microb. 69: 5536–5542 (2003)

    Article  CAS  Google Scholar 

  161. Musovic S, Oregaard G, Kroer N, Sørensen SJ. Cultivation-independent examination of horizontal transfer and host range of an IncP-1 plasmid among Gram-positive and Gram-negative bacteria indigenous to the barley rhizosphere. Appl. Environ. Microb. 72: 6687–6692 (2006)

    Article  CAS  Google Scholar 

  162. Rusell AD. Mechanisms of action, resistance, and stress adaptation. pp.633–657. In: Antimicrobials in Food. Davidson PM, John N, Sofos JN, Branen AL (eds). CRC Press, Inc., Boca Raton, FL, USA (2005)

    Chapter  Google Scholar 

  163. Langsrud S, Sidhu MS, Heir E, Holck AL. Bacterial disinfectant resistance-a challenge for the food industry. Int. Biodeter. Biodegr. 51: 283–290 (2003)

    Article  CAS  Google Scholar 

  164. Sidhu MS, Heir E, Sørum H, Holck A. Genetic linkage between resistance to quaternary ammonium compounds and β-lactam antibiotics in food-related Staphylococcus spp. Microb. Drug Resist. 7: 363–371 (2001)

    Article  CAS  Google Scholar 

  165. Brooun A, Liu S, Lewis K. A dose-response study of antibiotic resistance in Pseudomonas aeruginosa biofilms. Antimicrob. Agents Ch. 44: 640–646 (2000)

    Article  CAS  Google Scholar 

  166. Lewis K. Persister cells and the riddle of biofilm survival. Biochemistry-Moscow+ 70: 267–274 (2005)

    Article  CAS  Google Scholar 

  167. Keren I, Shah D, Spoering A, Kaldalu N, Lewis K. Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J. Bacteriol. 186: 8172–8180 (2004)

    Article  CAS  Google Scholar 

  168. Lewis K. Persister cells, dormancy, and infectious disease. Nat. Rev. Microbiol. 5: 48–56 (2007)

    Article  CAS  Google Scholar 

  169. Lewis K. Persister cells. Annu. Rev. Microbiol. 64: 357–372 (2010)

    Article  CAS  Google Scholar 

  170. Parisien A, Allain B, Zhang J, Mandeville R, Lan CQ. Novel alternatives to antibiotics: Bacteriophages, bacterial cell wall hydrolases, and antimicrobial peptides. J. Appl. Microbiol. 104: 1–13 (2008)

    CAS  Google Scholar 

  171. Abuladze T, Li M, Menetrez MY, Dean T, Senecal A, Sulakvelidze A. Bacteriophages reduce experimental contamination of hard surfaces, tomato, spinach, broccoli, and ground beef by Escherichia coli O157:H7. Appl. Environ. Microb. 74: 6230–6238 (2008)

    Article  CAS  Google Scholar 

  172. Guenther S, Huwyler D, Richard S, Loessner MJ. Virulent bacteriophage for efficient biocontrol of Listeria monocytogenes in ready-to-eat foods. Appl. Environ. Microb. 75: 93–100 (2009)

    Article  CAS  Google Scholar 

  173. Jassim SAA, Abdulamir AS, Bakar FA. Novel phage-based bioprocessing of pathogenic Escherichia coli and its biofilms. World J. Microbiol. Biot. 28: 47–60 (2012)

    Article  Google Scholar 

  174. Carlton RM, Noordman WH, Biswas B, de Meester ED, Loessner MJ. Bacteriophage P100 for control of Listeria monocytogenes in foods: Genome sequence, bioinformatic analyses, oral toxicity study, and application. Regul. Toxicol. Pharm. 43: 301–312 (2005)

    Article  CAS  Google Scholar 

  175. Hanlon GW, Denyer SP, Olliff CJ, Ibrahim LJ. Reduction in exopolysaccharide viscosity as an aid to bacteriophage penetration through Pseudomonas aeruginosa biofilms. Appl. Environ. Microb. 67: 2746–2753 (2001)

    Article  CAS  Google Scholar 

  176. Leverentz B, Conway WS, Camp MJ, Janisiewicz WJ, Abuladze T, Yang M, Saftner R, Sulakvelidze A. Biocontrol of Listeria monocytogenes on fresh-cut produce by treatment with lytic bacteriophages and a bacteriocin. Appl. Environ. Microb. 69: 4519–4526 (2003)

    Article  CAS  Google Scholar 

  177. Tait K, Skillman LC, Sutherland IW. The efficacy of bacteriophage as a method of biofilm eradication. Biofouling 18: 305–311 (2002)

    Article  Google Scholar 

  178. Kocharunchitt C, Ross T, McNeil DL. Use of bacteriophages as biocontrol agents to control Salmonella associated with seed sprouts. Int. J. Food Microbiol. 128: 453–459 (2009)

    Article  CAS  Google Scholar 

  179. Walker TS, Bais HP, Déziel E, Schweizer HP, Rahme LG, Fall R, Vivanco JM. Pseudomonas aeruginosa-plant root interactions. pathogenicity, biofilm formation, and root exudation. Plant Physiol. 134: 320–331 (2004)

    Article  CAS  Google Scholar 

  180. Bais HP, Prithiviraj B, Jha AK, Ausubel FM, Vivanco JM. Mediation of pathogen resistance by exudation of antimicrobials from roots. Nature 434: 217–221 (2005)

    Article  CAS  Google Scholar 

  181. Dong YH, Wang LY, Zhang LH. Quorum-quenching microbial infections: Mechanisms and implications. Philos. T. R. Soc. Lon. B 362: 1201–1211 (2007)

    Article  CAS  Google Scholar 

  182. Czajkowski R, Jafra S. Quenching of acyl-homoserine lactone-dependent quorum sensing by enzymatic disruption of signal molecules. Acta Biochim. Pol. 56: 1–16 (2009)

    CAS  Google Scholar 

  183. Zhu C, Yu Z, Sun M. Restraining Erwinia virulence by expression of N-acyl homoserine lactonase gene pro3A-aiiA in Bacillus thuringiensis subsp leesis. Biotechnol. Bioeng. 95: 526–532 (2006)

    Article  CAS  Google Scholar 

  184. Vanjildorj E, Song SY, Yang ZH, Choi JE, Noh YS, Park S, Lim WJ, Cho KM, Yun HD, Lim YP. Enhancement of tolerance to soft rot disease in the transgenic Chinese cabbage (Brassica rapa L. ssp. pekinensis) inbred line, Kenshin. Plant. Cell. Rep. 28: 1581–1591 (2009)

    Article  CAS  Google Scholar 

  185. Ponnusamy K, Paul D, Kweon JH. Inhibition of quorum sensing mechanism and Aeromonas hydrophila biofilm formation by vanillin. Environ. Eng. Sci. 26: 1359–1363 (2009)

    Article  CAS  Google Scholar 

  186. de Nys R, Givskov M, Kumar N, Kjelleberg S, Steinberg PD. Furanones. Prog. Mol. Subcell. Biol. 42: 55–86 (2006)

    Google Scholar 

  187. Janssens JC, Steenackers H, Robijns S, Gellens E, Levin J, Zhao H, Hermans K, De Coster D, Verhoeven TL, Marchal K, Vanderleyden J, De Vos DE, De Keersmaecker SC. Brominated furanones inhibit biofilm formation by Salmonella enterica serovar Typhimurium. Appl. Environ. Microb. 74: 6639–6648 (2008)

    Article  CAS  Google Scholar 

  188. Banat IM, Makkar RS, Cameotra SS. Potential commercial applications of microbial surfactants. Appl. Microbiol. Biot. 53: 495–508 (2000)

    Article  CAS  Google Scholar 

  189. Xavier JB, Picioreanu C, Rani SA, van Loosdrecht MC, Stewart PS. Biofilm-control strategies based on enzymic disruption of the extracellular polymeric substance matrix—a modelling study. Microbiology 151: 3817–3832 (2005)

    Article  CAS  Google Scholar 

  190. Lu TK, Collins JJ. Dispersing biofilms with engineered enzymatic bacteriophages. P. Natl. Acad. Sci. USA 104: 11197–11202 (2007)

    Article  CAS  Google Scholar 

  191. Rendueles O, Travier L, Latour-Lambert P, Fontaine T, Magnus J, Denamur E, Ghigo JM. Screening of Escherichia coli species biodiversity reveals new biofilm-associated antiadhesion polysaccharides. MBio 2: e00043-11 (2011)

    Article  CAS  Google Scholar 

  192. Yanti, Rukayadi Y, Lee K, Han S, Hwang JK. Anti-biofilm activity of xanthorrhizol isolated from Curcuma xanthorrhiza Roxb. against bacterial biofilms formed by saliva and artificial multispecies oral strains. Food Sci. Biotechnol. 18: 556–560 (2009)

    CAS  Google Scholar 

  193. Furukawa S, Akiyoshi Y, O’Toole GA, Ogihara H, Morinaga Y. Sugar fatty acid esters inhibit biofilm formation by food-borne pathogenic bacteria. Int. J. Food Microbiol. 138: 176–180 (2010)

    Article  CAS  Google Scholar 

  194. Orgaz B, Lobete MM, Puga CH, Jose CS. Effectiveness of chitosan against mature biofilms formed by food related bacteria. Int. J. Mol. Sci. 12: 817–828 (2011)

    Article  CAS  Google Scholar 

  195. Sandasi M, Leonard CM, Viljoen AM. The in vitro antibiofilm activity of selected culinary herbs and medicinal plants against Listeria monocytogenes. Lett. Appl. Microbiol. 50: 30–35 (2010)

    Article  CAS  Google Scholar 

  196. Jiang P, Li J, Han F, Duan G, Lu X, Gu Y, Yu W. Antibiofilm activity of an exopolysaccharide from marine bacterium Vibrio sp. QY101. PLoS. One 6: e18514 (2011)

    Article  CAS  Google Scholar 

  197. Sayem SM, Manzo E, Ciavatta L, Tramice A, Cordone A, Zanfardino A, De Felice M, Varcamonti M. Anti-biofilm activity of an exopolysaccharide from a sponge-associated strain of Bacillus licheniformis. Microb. Cell Fact. 10: 74 (2011)

    Article  CAS  Google Scholar 

  198. Khan R, Zakir M, Khanam Z, Shakil S, Khan AU. Novel compound from Trachyspermum ammi (Ajowan caraway) seeds with antibiofilm and antiadherence activities against Streptococcus mutans: A potential chemotherapeutic agent against dental caries. J. Appl. Microbiol. 109: 2151–2159 (2010)

    Article  CAS  Google Scholar 

  199. Dheilly A, Soum-Soutéra E, Klein GL, Bazire A, Compère C, Haras D, Dufour A. Antibiofilm activity of the marine bacterium Pseudoalteromonas sp. strain 3J6. Appl. Environ. Microb. 76: 3452–3461 (2010)

    Article  CAS  Google Scholar 

  200. Novak JS, Fratamico PM. Evaluation of ascorbic acid as a quorum-sensing analogue to control growth, sporulation, and enterotoxin production in Clostridium perfringens. J. Food Sci. 69: FMS72–FMS78 (2004)

    Article  CAS  Google Scholar 

  201. Lee JH, Regmi SC, Kim JA, Cho MH, Yun H, Lee CS, Lee J. Apple flavonoid phloretin inhibits Escherichia coli O157:H7 biofilm formation and ameliorates colon inflammation in rats. Infect. Immun. 79: 4819–4827 (2011)

    Article  CAS  Google Scholar 

  202. Luksiene Z. New approach to inactivation of harmful and pathogenic microorganisms by photosensitization. Food Technol. Biotech. 43: 411–418 (2005)

    CAS  Google Scholar 

  203. Luksiene Z, Zukauskas A. Prospects of photosensitization in control of pathogenic and harmful micro-organisms. J. Appl. Microbiol. 107: 1415–1424 (2009)

    Article  CAS  Google Scholar 

  204. Luksiene Z, Buchovec I, Paskeviciute E. Inactivation of several strains of Listeria monocytogenes attached to the surface of packaging material by Na-chlorophyllin-based photosensitization. J. Photoch. Photobio. B 101: 326–331 (2010)

    Article  CAS  Google Scholar 

  205. Luksiene Z, Paskeviciute E. Novel approach to the microbial decontamination of strawberries: Chlorophyllin-based photosensitization. J. Appl. Microbiol. 110: 1274–1283 (2011)

    Article  CAS  Google Scholar 

  206. Leistner L. Basic aspects of food preservation by hurdle technology. Int. J. Food Microbiol. 55: 181–186 (2000)

    Article  CAS  Google Scholar 

  207. Ha JH, Lee DU, Auh JH, Ha SD. Synergistic effects of combined disinfecting treatments using sanitizers and UV to reduce levels of Bacillus cereus in oyster mushroom. J. Korean Soc. Appl. Biol. Chem. 54: 269–274 (2011)

    Google Scholar 

  208. United States Food and Drug Administration (USFDA). Guidance for industry: Guide to minimize microbial food safety hazards for fresh fruits and vegetables. Available from: http://www.fda.gov/Food/guidanceComplianceregulatoryInformation/GuidanceDocuments/ProduceandPlanProducts/ucm064574.htm. Accessed Oct. 29, 1998.

  209. Waje C, Kwon JH. Improving the food safety of seed sprouts through irradiation treatment. Food Sci. Biotechnol. 16: 171–176 (2007)

    Google Scholar 

  210. Allende A, Artés F. Combined ultraviolet-C and modified atmosphere packaging treatments for reducing microbial growth of fresh processed lettuce. Lebensm. -Wiss. Technol. 36: 779–786 (2003)

    CAS  Google Scholar 

  211. Yaun BR, Sumner SS, Eifert JD, Marcy JE. Inhibition of pathogens on fresh produce by ultraviolet energy. Int. J. Food Microbiol. 90: 1–8 (2004)

    Article  Google Scholar 

  212. Mattson TE, Johny AK, Amalaradjou MA, More K, Schreiber DT, Patel J, Venkitanarayanan K. Inactivation of Salmonella spp. on tomatoes by plant molecules. Int. J. Food Microbiol. 144: 464–468 (2011)

    Article  CAS  Google Scholar 

  213. Viazis S, Akhtar M, Feirtag J, Diez-Gonzalez F. Reduction of Escherichia coli O157:H7 viability on leafy green vegetables by treatment with a bacteriophage mixture and trans-cinnamaldehyde. Food Microbiol. 28: 149–157 (2011)

    Article  Google Scholar 

  214. Kim SY, Sagong HG, Ryu S, Mah JH, Kang DH. Development of oscillation method for reducing foodborne pathogens on lettuce and spinach. Int. J. Food Microbiol. 145: 273–278 (2011)

    Article  Google Scholar 

  215. Gopal A, Coventry J, Wan J, Roginski H, Ajlouni S. Alternative disinfection techniques to extend the shelf life of minimally processed iceberg lettuce. Food Microbiol. 27: 210–219 (2010)

    Article  CAS  Google Scholar 

  216. Seymour IJ, Burfoot D, Smith RL, Cox LA, Lockwook A. Ultrasound decontamination of minimally processed fruits and vegetables. Int. J. Food Sci. Tech. 37: 547–557 (2002)

    Article  CAS  Google Scholar 

  217. Bari ML, Ukuku DO, Kawasaki T, Inatsu Y, Isshiki K, Kawamoto S. Combined efficacy of nisin and pediocin with sodium lactate, citric acid, phytic acid, and potassium sorbate and EDTA in reducing the Listeria monocytogenes population of inoculated fresh-cut produce. J. Food Protect. 68: 1381–1387 (2005)

    CAS  Google Scholar 

  218. Allende A, Marín A, Buendía B, Tomás-Barberán F, Gil MI. Impact of combined postharvest treatments (UV-C light, gaseous O3, superatmospheric O2, and high CO2) on health promoting compounds and shelf-life of strawberries. Postharvest Biol. Tec. 46: 201–211 (2007)

    Article  CAS  Google Scholar 

  219. Marquenie D, Michiels CW, Geeraerd AH, Schenk A, Soontjen C, Van Impe JF, Nicolaï BM. Using survival analysis to investigate the effect of UV-C and heat treatment on storage rot of strawberry and sweet cherry. Int. J. Food Microbiol. 73: 187–196 (2002)

    Article  CAS  Google Scholar 

  220. Ha JH, Ha SD. Synergistic effects of ethanol and UV radiation to reduce levels of selected foodborne pathogenic bacteria. J. Food Protect. 73: 556–561 (2010)

    Google Scholar 

  221. Leverentz B, Conway WS, Janisiewicz W, Abadias M, Kurtzman CP, Camp MJ. Biocontrol of the food-borne pathogens Listeria monocytogenes and Salmonella enterica serovar Poona on freshcut apples with naturally occurring bacterial and yeast antagonists. Appl. Environ. Microb. 72: 1135–1140 (2006)

    Article  CAS  Google Scholar 

  222. Simões LC, Lemos M, Pereira AM, Abreu AC, Saavedra MJ, Simões M. Persister cells in a biofilm treated with a biocide. Biofouling 27: 403–411 (2011)

    Article  CAS  Google Scholar 

  223. Sapers GM. Efficacy of washing and sanitizing methods for disinfection of fresh fruit and vegetable products. Food Technol. Biotech. 39: 305–311 (2001)

    Google Scholar 

  224. Artés F, Gómez P, Aguayo E, Escalona V, Artés-Hernández F. Sustainable sanitation techniques for keeping quality and safety of fresh-cut plant commodities. Postharvest Biol. Tec. 51: 287–296 (2009)

    Article  CAS  Google Scholar 

  225. Parish ME, Beuchat LR, Suslow TV, Harris LJ, Garrett EH, Farber JN, Bust FF. Methods to reduce/eliminate pathogens from fresh and fresh-cut produce. Compr. Rev. Food Sci. F. 2: 161–173 (2003)

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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    Iqbal Kabir Jahid & Sang-Do Ha

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Jahid, I.K., Ha, SD. A review of microbial biofilms of produce: Future challenge to food safety. Food Sci Biotechnol 21, 299–316 (2012). https://doi.org/10.1007/s10068-012-0041-1

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