Food Engineering Reviews

, Volume 6, Issue 1–2, pp 29–42

Biofilm Formation in Food Processing Environments is Still Poorly Understood and Controlled

Review Article


The presence of undesirable biofilms on food processing contact surfaces may lead to: (1) transmission of diseases; (2) food spoilage; (3) shortened time between cleaning events; (4) contamination of product by nonstarter bacteria; (5) metal corrosion in pipelines and tanks; (6) reduced heat transfer efficacy or even obstruction of the heat equipment. Despite the significant problems caused by biofilms in the food industry, biofilm formation in these environments is still poorly understood and effective control of biofilms remains challenging. Although it is understood that cell attachment and biofilm formation are influenced by several factors, including type of strain, chemical–physical properties of the surface, temperature, growth media and the presence of other microorganisms, some conflicting statements can be retrieved from the literature and there are no general trends yet that allow us to easily predict biofilm development. It is likely that still unexplored interaction of factors may be more critical than the effect of a single parameter. New alternative biofilm control strategies, such as biocontrol, use of enzymes and phages and cell-to-cell communication interference, are now available that can reduce the use of chemical agents. In addition, as preventing biofilm formation is a more efficient strategy than controlling mature biofilm, the use of surface-modified materials have been suggested. These strategies may better reveal their beneficial potential when the ecological complexity of biofilms in food environments is addressed.


Biofilm Antibiofilm action Food safety Alternative control 


  1. 1.
    Abee T, Van Schaik W, Siezen RJ (2004) Impact of genomics on microbial food safety. Trends Biotechnol 22:653–660Google Scholar
  2. 2.
    Abramzon N, Joaquin JC, Bray J, Brelles-Mariño G (2006) Biofilm destruction by RF high-pressure cold plasma jet. IEEE Trans Plasma Sci 34:1304–1309Google Scholar
  3. 3.
    Alpkvista E, Klapper I (2007) A multidimensional multispecies continuum model for heterogeneous biofilm development. Bull Math Biol 69:765–789Google Scholar
  4. 4.
    Bai AJ, Rai VR (2011) Bacterial quorum sensing and food industry. Compr Rev Food Sci Food Saf 10:184–194Google Scholar
  5. 5.
    Barish JA, Goddard JM (2013) Anti-fouling surface modified stainless steel for food processing. Food Bioprod Process. doi:10.1016/j.fbp.2013.01.003
  6. 6.
    Beech IB, Sunner J (2004) Biocorrosion: towards understanding interactions between biofilms and metals. Curr Opin Biotechnol 15:181–186Google Scholar
  7. 7.
    Behnke S, Parker AE, Woodall D, Camper AK (2011) Comparing the chlorine disinfection of detached biofilm clusters with those of sessile biofilms and planktonic cells in single- and dual-species cultures. Appl Environ Microbiol 77:7176–7184Google Scholar
  8. 8.
    Beresford MR, Andrew PW, Shama G (2001) Listeria monocytogenes adheres to many materials found in food-processing environments. J Appl Microbiol 90:1000–1005Google Scholar
  9. 9.
    Boistier-Marquisa E, Oulahal-Lagsirb N, Larpentc J-P (2000) Methodology for a comparative evaluation of sensitivity to fouling and cleanability of floor materials used in the food industry. Biofouling 14:279–286Google Scholar
  10. 10.
    Bremer PJ, Monk I, Osborne CM (2001) Survival of Listeria monocytogenes attached to stainless steel surfaces in the presence or absence of Flavobacterium spp. J Food Prot 64:1369–1376Google Scholar
  11. 11.
    Brooks JD, Flint SH (2008) Biofilms in the food industry: problems and potential solutions. Int J Food Sci Technol 43:2163–2176Google Scholar
  12. 12.
    Buchovec I, Paskeviciute E, Luksiene Z (2010) Photosensitization-based inactivation of food pathogen Listeria monocytogenes in vitro and on the surface of packaging material. J Photochem Photobiol, B 99:9–14Google Scholar
  13. 13.
    Cappello S, Guglielmino SPP (2006) Effects of growth temperature on polystyrene adhesion of Pseudomonas aeruginosa ATCC 27853. Braz J Microbiol 37:205–207Google Scholar
  14. 14.
    Carpentier B, Cerf O (1993) Biofilms and their consequences, with particular reference to hygiene in food industry. J Appl Bacteriol 75:499–511Google Scholar
  15. 15.
    Carpentier B, Chassaing D (2004) Interactions in biofilms between Listeria monocytogenes and resident microorganisms from food industry premises. Int J Food Microbiol 97:111–122Google Scholar
  16. 16.
    Castelijn GA, van der Veen S, Zwietering MH, Moezelaar R, Abee T (2012) Diversity in biofilm formation and production of curli fimbriae and cellulose of Salmonella Typhimurium strains of different origin in high and low nutrient medium. Biofouling 28:51–63Google Scholar
  17. 17.
    Characklis WG (1981) Fouling biofilm development: a process analysis. Biotechnol Bioeng 23:1923–1960Google Scholar
  18. 18.
    Chia TWR, Goulter RM, McMeekin T, Dykes GA, Fegan N (2009) Attachment of different Salmonella serovars to materials commonly used in a poultry processing plant. Food Microbiol 26:853–859Google Scholar
  19. 19.
    Chmielewski RAN, Frank JF (2003) Biofilm formation and control in food processing facilities. Compr Rev Food Sci Food Saf 2:22–32Google Scholar
  20. 20.
    Costerton JW, Ellis B, Lam K, Johnson F, Khoury AE (1994) Mechanism of electrical enhancement of efficacy of antibiotics in killing biofilm bacteria. Antimicrob Agents Chemother 38:2803–2809Google Scholar
  21. 21.
    Costerton JW (2007) The biofilm primer. Springer series on biofilms, vol 1. Springer, BerlinGoogle Scholar
  22. 22.
    Critzer FJ, Kelly-Wintenberg K, South SL, Golden DA (2007) Atmospheric plasma inactivation of foodborne pathogens on fresh produce surfaces. J Food Prot 70:2290–2296Google Scholar
  23. 23.
    da Silva Meira QG, de Medeiros Barbosa I, Aguiar Athayde AJA, de Siqueira-Júnior JP, de Souza EL (2012) Influence of temperature and surface kind on biofilm formation by Staphylococcus aureus from food-contact surfaces and sensitivity to sanitizers. Food Control 25:469–475Google Scholar
  24. 24.
    Dat NM, Hamanaka D, Tanaka F, Uchino T (2012) Control of milk pH reduces biofilm formation of Bacillus licheniformis and Lactobacillus paracasei on stainless steel. Food Control 23:215–220Google Scholar
  25. 25.
    Davies DG, Marques CN (2009) A fatty acid messenger is responsible for inducing dispersion in microbial biofilms. J Bacteriol 191:1393–1403Google Scholar
  26. 26.
    Di Bonaventura G, Piccolomini R, Paludi D, D’Orio V, Vergara A, Conter M, Ianieri A (2008) Influence of temperature on biofilm formation by Listeria monocytogenes on various food-contact surfaces: relationship with motility and cell surface hydrophobicity. J Appl Microbiol 104:1552–1561Google Scholar
  27. 27.
    Djordjevic D, Wiedmann M, McLandsborough LA (2002) Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation. Appl Environ Microbiol 68:2950–2958Google Scholar
  28. 28.
    Donlan RM (2002) Biofilms: microbial life on surfaces. Emerg Infect Dis 8:881–890Google Scholar
  29. 29.
    Dunne MW Jr (2002) Bacterial adhesion: seen any good biofilms lately? Clin Microbiol Rev 15:155–166Google Scholar
  30. 30.
    Flemming H-C, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633Google Scholar
  31. 31.
    Flint SH, Bremer PJ, Brooks JD (1997) Biofilms in dairy manufacturing plant-description, current concerns and methods of control. Biofouling 11:81–97Google Scholar
  32. 32.
    Furukawa S, Akiyoshi Y, O’Toole GA, Ogihara H, Morinaga Y (2010) Sugar fatty acid esters inhibit biofilm formation by food-borne pathogenic bacteria. Int J Food Microbiol 138:176–180Google Scholar
  33. 33.
    Gerstel U, Römling U (2001) Oxygen tension and nutrient starvation are major signals that regulate agfD promoter activity and expression of the multicellular morphotype in Salmonella typhimurium. Environ Microbiol 3:638–648Google Scholar
  34. 34.
    Gibson HJ, Taylor H, Hall KE, Holah JT (1999) Effectiveness of cleaning techniques used in the food industry in terms of the removal of bacterial biofilms. J Appl Microbiol 87:41–48Google Scholar
  35. 35.
    Gram L, Ravn L, Rasch M, Bartholin Bruhn J, Christensen AB, Givskov M (2002) Food spoilage—interactions between food spoilage bacteria. Int J Food Microbiol 78:79–97Google Scholar
  36. 36.
    Greer GG (2005) Bacteriophage control of foodborne bacteria. J Food Prot 68:1102–1111Google Scholar
  37. 37.
    Gunduz GT, Tuncel G (2006) Biofilm formation in an ice cream plant. Antonie Van Leeuwenhoek 89:329–336Google Scholar
  38. 38.
    Habimana O, Heir E, Langsrud S, Wold Åsli A, Møretrø T (2010) Enhanced surface colonization by Escherichia coli O157:H7 in biofilms formed by an Acinetobacter calcoaceticus isolate from meat-processing environments. Appl Environ Microbiol 76:4557–4559Google Scholar
  39. 39.
    Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108Google Scholar
  40. 40.
    Hamanaka D, Onishi M, Genkawa T, Tanaka F, Uchino T (2012) Effects of temperature and nutrient concentration on the structural characteristics and removal of vegetable-associated Pseudomonas biofilm. Food Control 24:165–170Google Scholar
  41. 41.
    Han J, Seale RB, Silcock P, McQuillan AJ, Bremer PJ (2011) The physico-chemical characterization of casein-modified surfaces and their influence on the adhesion of spores from a Geobacillus species. Biofouling 5:459–466Google Scholar
  42. 42.
    Hingston PA, Stea EC, Knøchel S, Hansen T (2013) Role of initial contamination levels, biofilm maturity and presence of salt and fat on desiccation survival of Listeria monocytogenes on stainless steel surfaces. Food Microbiol 36:46–56Google Scholar
  43. 43.
    Hinton AR, Trinh KT, Brooks JD, Manderson GJ (2002) Thermophile survival in milk fouling and on stainless steel during cleaning. Food Bioprod Process 80:299–304Google Scholar
  44. 44.
    Hook AL, Chang C-Y, Yang J, Luckett J, Cockayne A, Atkinson S, Mei Y, Bayston R, Irvine DJ, Langer R, Anderson DG, Williams P, Davies MC, Alexander MR (2012) Combinatorial discovery of polymers resistant to bacterial attachment. Nat Biotechnol 30:868–875Google Scholar
  45. 45.
    Husmark U, Faille C, Rönner U, Bénézech T (1999) Bacillus spores and moulding with TTC agar: a useful method for the assessment of food processing equipment cleanability. Biofouling 14:15–24Google Scholar
  46. 46.
    Jahid IK, Ha S-D (2012) A review of microbial biofilms of produce: future challenge to food safety. Food Sci Biotechnol 21:299–316Google Scholar
  47. 47.
    Jun W, Kim MS, Cho B-K, Millner PD, Chao K, Chan DE (2010) Microbial biofilm detection on food contact surfaces by macro-scale fluorescence imaging. J Food Eng 99:314–322Google Scholar
  48. 48.
    Kalmokoff ML, Austin JW, Wan XD, Sanders G, Banerjee S, Farber JM (2001) Adsorption, attachment and biofilm formation among isolates of Listeria monocytogenes using model conditions. J Appl Microbiol 91:725–734Google Scholar
  49. 49.
    Kaplan JB (2010) Biofilm dispersal: mechanisms, clinical implications, and potential therapeutic uses. J Dent Res 89:205–218Google Scholar
  50. 50.
    Kives J, Guadarrama D, Orgaz B, Rivera-Sen A, Vazquez J, SanJose C (2005) Interactions in biofilms of Lactococcus lactis ssp. cremoris and Pseudomonas fluorescens cultured in cold UHT milk. J Dairy Sci 88:4165–4171Google Scholar
  51. 51.
    Klapper I, Rupp CJ, Cargo R, Purvedorj B, Stoodley P (2002) Viscoelastic fluid description of bacterial biofilm material properties. Biotechnol Bioeng 80:289–296Google Scholar
  52. 52.
    Konopka A (2009) Microbial community ecology. ISME J 3:1223–1230Google Scholar
  53. 53.
    Kostaki M, Chorianopoulos N, Braxou E, Nychas G-J, Giaouris E (2012) Differential biofilm formation and chemical disinfection resistance of sessile cells of Listeria monocytogenes strains under monospecies and dual-species (with Salmonella enterica) conditions. Appl Environ Microbiol 78:2586–2595Google Scholar
  54. 54.
    Kregiel D (2013) Adhesion of Aeromonas hydrophila to glass surfaces modified with organosilanes. Food Technol Biotechnol 51:345–351Google Scholar
  55. 55.
    Kregiel D, Niedzielska K (2014) Effect of plasma processing and organosilane modifications of polyethylene on Aeromonas hydrophila biofilm formation. BioMed Res Int. doi:10.1155/2014/232514
  56. 56.
    Lee Y-D, Kim J-Y, Park J-H (2013) Characteristics of coliphage ECP4 and potential use as a sanitizing agent for biocontrol of Escherichia coli O157:H7. Food Control 34:255–260Google Scholar
  57. 57.
    Lee S-Y (2004) Microbial safety of pickled fruits and vegetables and hurdle technology. Internet J Food Saf 4:21–32Google Scholar
  58. 58.
    Lee KWK, Periasamy S, Mukherjee M, Xie C, Kjelleberg S, Rice SA (2014) Biofilm development and enhanced stress resistance of a model, mixed-species community biofilm. ISME J 8:894–907Google Scholar
  59. 59.
    Lemon KP, Higgins DE, Kolter R (2007) Flagellar motility is critical for Listeria monocytogenes biofilm formation. J Bacteriol 189:4418–4424Google Scholar
  60. 60.
    Lequette Y, Boels G, Clarisse M, Faille C (2010) Using enzymes to remove biofilms of bacterial isolates sampled in the food-industry. Biofouling 26:421–431Google Scholar
  61. 61.
    Lewis K (2010) Persister cells. Annu Rev Microbiol 64:357–372Google Scholar
  62. 62.
    Lindbäck T, Secic I, Rørvik LM (2011) A contingency locus in prfA in a Listeria monocytogenes subgroup allows reactivation of the PrfA virulence regulator during infection in mice. Appl Environ Microbiol 77:3478–3483Google Scholar
  63. 63.
    Lindsay D, Brözel VS, von Holy A (2006) Biofilm-spore response in Bacillus cereus and Bacillus subtilis during nutrient limitation. J Food Prot 69:1168–1172Google Scholar
  64. 64.
    Luksiene Z, Buchovec I, Paskeviciute E (2010) Inactivation of several strains of Listeria monocytogenes attached to the surface of packaging material by Na-Chlorophyllin-based photosensitization. J Photochem Photobiol, B 101:326–331Google Scholar
  65. 65.
    Luksiene Z, Brovko L (2013) Antibacterial photosensitization-based treatment for food safety. Food Eng Rev 5:185–199Google Scholar
  66. 66.
    Mah T-FC, O’Toole GA (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9:34–39Google Scholar
  67. 67.
    Malek F, Moussa-Boudjemaa B, Khaouani-Yousfi F, Kalai A, Kihal M (2012) Microflora of biofilm on Algerian dairy processing lines: an approach to improve microbial quality of pasteurized milk. Afr J Microbiol Res 6:3836–3844Google Scholar
  68. 68.
    McLandsborough L, Rodriguez A, Perez-Conesa D, Weiss J (2006) Biofilms: at the interface between biophysics and microbiology. Food Biophys 1:94–114Google Scholar
  69. 69.
    Misra NN, Tiwari BK, Raghavarao KSMS, Cullen PJ (2011) Nonthermal plasma inactivation of food-borne pathogens. Food Eng Rev 3:159–170Google Scholar
  70. 70.
    Mireles JR II, Toguchi A, Harshey RM (2001) Salmonella enterica serovar Typhimurium swarming mutants with altered biofilm-forming abilities: surfactin inhibits biofilm formation. J Bacteriol 183:5848–5854Google Scholar
  71. 71.
    Møretrø T, Midtgaard ES, Nesse LL, Langsrud S (2003) Susceptibility of Salmonella isolated from fish feed factories to disinfectants and air-drying at surfaces. Vet Microbiol 94:207–217Google Scholar
  72. 72.
    Møretrø T, Vestby LK, Nesse LL, Storheim SE, Kotlarz K, Langsrud S (2009) Evaluation of efficacy of disinfectants against Salmonella from the feed industry. J Appl Microbiol 106:1005–1012Google Scholar
  73. 73.
    Møretrø T, Heir E, Nesse LL, Vestby LK, Langsrud S (2012) Control of Salmonella in food related environments by chemical disinfection. Food Res Int 45:532–544Google Scholar
  74. 74.
    Morimatsu K, Hamanaka D, Tanaka F, Toshitaka U (2013) Effect of temperature fluctuation on biofilm formation with bacterial interaction between Salmonella enterica and Pseudomonas putida. J Fac Agric Kyushu Univ 58:125–129Google Scholar
  75. 75.
    Nadell CD, Xavier JB, Foster KR (2009) The sociobiologyof biofilms. FEMS Microbiol Rev 33:206–224Google Scholar
  76. 76.
    Niemira BA (2012) Cold plasma decontamination of foods. Annu Rev Food Sci Technol 3:125–142Google Scholar
  77. 77.
    Nitschkea M, Costab SGVAO (2007) Biosurfactants in food industry. Trends Food Sci Techol 18:252–259Google Scholar
  78. 78.
    Norwood DE, Gilmour A (2000) The growth and resistance to sodium hypochlorite of Listeria monocytogenes in a steady-state multispecies biofilm. J Appl Microbiol 88:512–520Google Scholar
  79. 79.
    Orgaz B, Puga CH, Martínez-Suárez JV, SanJose C (2013) Biofilm recovery from chitosan action: a possible clue to understand Listeria monocytogenes persistence in food plants. Food Control 32:484–489Google Scholar
  80. 80.
    Ortega ME, Fernández-Fuentes MA, Grande Burgos MJ, Abriouel H, Pérez Pulido R, Gálvez A (2013) Biocide tolerance in bacteria. Int J Food Microbiol 162:13–25Google Scholar
  81. 81.
    Olsson I-M, Johansson E, Berntsson M, Eriksson L, Gottfries J, Wold S (2006) Rational DOE protocols for 96-well plates. Chemometr Intell Lab Syst 83:66–74Google Scholar
  82. 82.
    Oulahal-Lagsir N, Martial-Gros A, Boistier E, Blum LJ, Bonneau M (2000) The development of an ultrasonic apparatus for the non-invasive and repeatable removal of fouling in food processing equipment. Lett Appl Microbiol 30:47–52Google Scholar
  83. 83.
    Oulahal-Lagsir N, Martial-Gros A, Bonneau M, Blum LJ (2003) “Escherichia coli-milk” biofilm removal from stainless steel surfaces: synergism between ultrasonic waves and enzymes. Biofouling 19:159–168Google Scholar
  84. 84.
    Oulahal N, Martial-Gros A, Bonneau M, Blum LJ (2004) Combined effect of chelating agents and ultrasound on biofilm removal from stainless steel surfaces. Application to “Escherichia coli milk” and “Staphylococcus aureus milk” biofilms. Biofilms 1:65–73Google Scholar
  85. 85.
    Palmer J, Flint S, Brooks J (2007) Bacterial cell attachment, the beginning of a biofilm. J Ind Microbiol Biotechnol 34:577–588Google Scholar
  86. 86.
    Pan Y, Breidt F Jr, Kathariou S (2006) Resistance of Listeria monocytogenes biofilms to sanitizing agents in a simulated food processing environment. Appl Environ Microbiol 72:7711–7717Google Scholar
  87. 87.
    Percival SL, Malic S, Cruz H, Williams DW (2011) In: Percival SL, Knottenbelt DC, Cochrane CA (eds) Biofilms and veterinary medicine. Springer series on biofilms, vol 6. Springer, BerlinGoogle Scholar
  88. 88.
    Pérez IM, Castellano P, Vignolo G (2014) Evaluation of anti-Listeria meat borne Lactobacillus for biofilm formation on selected abiotic surfaces. Meat Sci 96:295–303Google Scholar
  89. 89.
    Preston GM, Haubold B, Rainey PB (1998) Bacterial genomics and adaptation to life on plants: implications for the evolution of pathogenicity and symbiosis. Curr Opin Microbiol 1:589–597Google Scholar
  90. 90.
    Pilchová T, Hernould M, Prévost H, Demnerová K, Pazlarová J, Tresse O (2014) Influence of food processing environments on structure initiation of static biofilm of Listeria monocytogenes. Food Control 35:366–372Google Scholar
  91. 91.
    Potenski CJ, Gandhi M, Matthews KR (2003) Exposure of Salmonella Enteritidis to chlorine or food preservatives increases susceptibility to antibiotics. FEMS Microbiol Lett 220:181–186Google Scholar
  92. 92.
    Reuter M, Mallett A, Pearson BM, van Vliet AHM (2010) Biofilm Formation by Campylobacter jejuni is increased under aerobic conditions. Appl Environ Microbiol 76:2122–2128Google Scholar
  93. 93.
    Rijnaarts HHM, Norde W, Bouwer EJ, Lyklema J, Zehnder AJB (1993) Bacterial adhesion under static and dynamic conditions. Appl Environ Microbiol 59:3255–3265Google Scholar
  94. 94.
    Romanova NA, Gawande PV, Brovko LY, Griffiths MW (2007) Rapid methods to assess sanitizing efficacy of benzalkonium chloride to Listeria monocytogenes biofilms. J Microbiol Methods 71:231–237Google Scholar
  95. 95.
    Rørvik LM (2000) Listeria monocytogenes in the smoked salmon industry. Int J Food Microbiol 62:183–190Google Scholar
  96. 96.
    Rudi K, Flateland SL, Hanssen JF, Bengtsson G, Nissen H (2002) 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 Microbiol 68:1146–1156Google Scholar
  97. 97.
    Salustiano VC, Andrade NJ, Soares NFF, Lima JC, Bernardes PC, Luiz LMP, Fernandes PE (2009) Contamination of milk with Bacillus cereus by post-pasteurization surface exposure as evaluated by automated ribotyping. Food Control 20:439–442Google Scholar
  98. 98.
    SCENIHR (Scientific Committee on Emerging and Newly Identified Health Risks, European Commission) (2009) The scientific committee on emerging and newly identified health risks report. Accessed 19 Nov 2013
  99. 99.
    Schlisselberg DB, Yaron S (2013) The effects of stainless steel finish on Salmonella Typhimurium attachment, biofilm formation and sensitivity to chlorine. Food Microbiol 35:65–72Google Scholar
  100. 100.
    Schirmer BCT, Langsrud S, Møretrø T, Hagtvedt T, Heir E (2012) Performance of two commercial rapid methods for sampling and detection of Listeria in small-scale cheese producing and salmon processing environments. J Microbiol Methods 91:295–300Google Scholar
  101. 101.
    Shi X, Zhu X (2009) Biofilm formation and food safety in food industries. Trends Food Sci Techol 20:407–413Google Scholar
  102. 102.
    Sillankorva SM, Oliveira H, Azeredo J (2012) Bacteriophages and their role in food safety. Int J Microbiol. doi:10.1155/2012/863945 Google Scholar
  103. 103.
    Silva S, Teixeira P, Oliveira R, Azeredo J (2008) Adhesion to and viability of Listeria monocytogenes on food contact surfaces. J Food Prot 71:1379–1385Google Scholar
  104. 104.
    Simões M, Simões LC, Vieira MJ (2010) A review of current and emergent biofilm control strategies. LWT Food Sci Technol 43:573–583Google Scholar
  105. 105.
    Skandamis PN, Nychas GJ (2012) Quorum sensing in the context of food microbiology. Appl Environ Microbiol 78:5473–5482Google Scholar
  106. 106.
    Splendiani A, Livingston AG, Nicolella C (2006) Control membrane-attached biofilms using surfactants. Biotechnol Bioeng 94:15–23Google Scholar
  107. 107.
    Srey S, Jahid IK, Ha S-D (2013) Biofilm formation in food industries: a food safety concern. Food Control 31:572–585Google Scholar
  108. 108.
    Stepanović S, Ćirković I, Mijać V, Švabić-Vlahović M (2003) Influence of the incubation temperature, atmosphere and dynamic conditions on biofilm formation by Salmonella spp. Food Microbiol 20:339–343Google Scholar
  109. 109.
    Stewart PS (2003) Diffusion in biofilms. J Bacteriol 185:1485–1491Google Scholar
  110. 110.
    Strathmann M, Mittenzwey KH, Sinn G, Papadakis W, Flemming HC (2013) Simultaneous monitoring of biofilm growth, microbial activity, and inorganic deposits on surfaces with an in situ, online, real-time, non-destructive, optical sensor. Biofouling 29:573–583Google Scholar
  111. 111.
    Tang L, Pillai S, Revsbech NP, Schramm A, Bischoff C, Meyer RL (2011) Biofilm retention on surfaces with variable roughness and hydrophobicity. Biofouling 27:111–121Google Scholar
  112. 112.
    Taormina PJ, Beuchat LR (2002) Survival of Listeria monocytogenes in commercial food-processing equipment cleaning solutions and subsequent sensitivity to sanitizers and heat. J Appl Microbiol 92:71–80Google Scholar
  113. 113.
    Tarifa MC, Brugnoni LI, Lozano JE (2013) Role of hydrophobicity in adhesion of wild yeast isolated from the ultrafiltration membranes of an apple juice processing plant. Biofouling 29:841–853Google Scholar
  114. 114.
    Torlak E, Sert D (2013) Combined effect of benzalkonium chloride and ultrasound against Listeria monocytogenes biofilm on plastic surface. Lett Appl Microbiol 57:220–226Google Scholar
  115. 115.
    Toussaint A, Ghigo J-M, Salmond GPC (2003) A new evaluation of our life-support system. EMBO Rep 4:820–824Google Scholar
  116. 116.
    Trachoo N, Brooks JD (2005) Attachment and heat resistance of Campylobacter jejuni on Enterococcus faecium biofilm. Pak J Biol Sci 8:599–605Google Scholar
  117. 117.
    Valderrama WB, Cutter CN (2013) An ecological perspective of Listeria monocytogenes biofilms in food processing facilities. Crit Rev Food Sci Nutr 53:1–17Google Scholar
  118. 118.
    Valeriano C, Coutinho de Oliveira TL, Malfitano de Carvalho S, das Graças Cardoso M, Alves E, Hilsdorf Piccoli R (2012) The sanitizing action of essential oil-based solutions against Salmonella enterica serotype Enteritidis S64 biofilm formation on AISI 304 stainless steel. Food Control 25:673–677Google Scholar
  119. 119.
    van der Veen S, Abee T (2011) Mixed species biofilms of Listeria monocytogenes and Lactobacillus plantarum show enhanced resistance to benzalkonium chloride and peracetic acid. Int J Food Microbiol 144:421–431Google Scholar
  120. 120.
    Van Houdt R, Michiels CW (2010) Biofilm formation and the food industry, a focus on the bacterial outer surface. J Appl Microbiol 109:1117–1131Google Scholar
  121. 121.
    Verran J, Boyd RD, Hall KE, West R (2002) The detection of microorganisms and organic material on stainless steel food contact surfaces. Biofouling 18:167–176Google Scholar
  122. 122.
    Verstraeten N, Braeken K, Debkumari B, Fauvart M, Fransaer J, Vermant J, Michiels J (2008) Living on a surface: swarming and biofilm formation. Trends Microbiol 16:496–506Google Scholar
  123. 123.
    Villa F, Giacomucci L, Polo A, Principi P, Toniolo L, Levi M, Turri S, Cappitelli F (2009) N-vanillylnonanamide tested as a non-toxic antifoulant, applied to surfaces in a polyurethane coating. Biotechnol Lett 31:1407–1413Google Scholar
  124. 124.
    Villa F, Cappitelli F (2013) Plant-derived bioactive compounds at sub-lethal concentrations: towards smart biocide-free antibiofilm strategies. Phytochem Rev 12:245–254Google Scholar
  125. 125.
    Vinten AJA, Artz RRE, Thomas N, Potts JM, Avery L, Langan SJ, Watson H, Cook Y, Taylor C, Abel C, Reid E, Singh BK (2011) Comparison of microbial community assays for the assessment of stream biofilm ecology. J Microbiol Methods 85:190–198Google Scholar
  126. 126.
    Wang H, Ye K, Wei X, Cao J, Xu X, Zhou G (2013) Occurrence, antimicrobial resistance and biofilm formation of Salmonella isolates from a chicken slaughter plant in China. Food Control 33:378–384Google Scholar
  127. 127.
    Wang H–H, Ye K-P, Zhang Q–Q, Dong Y, Xu X-L, Zhou G-H (2013) Biofilm formation of meat-borne Salmonella enterica and inhibition by the cell-free supernatant from Pseudomonas aeruginosa. Food Control 32:650–658Google Scholar
  128. 128.
    Wanner O, Gujer W (1986) A multispecies biofilm model. Biotechnol Bioeng 28:314–328Google Scholar
  129. 129.
    Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346Google Scholar
  130. 130.
    Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS (2002) Extracellular DNA required for bacterial biofilm formation. Science 295:1487Google Scholar
  131. 131.
    Willis C, Baalham T, Greenwood M, Presland F (2006) Evaluation of a new chromogenic agar for the detection of Listeria in food. J Appl Microbiol 101:711–717Google Scholar
  132. 132.
    Wijman JGE, de Leeuw PPLA, Moezelaar R, Zwietering MH, Abee T (2007) Air-liquid interface biofilms of Bacillus cereus: formation, sporulation, and dispersion. Appl Environ Microbiol 73:1481–1488Google Scholar
  133. 133.
    Wong ACL (1998) Biofilms in food processing environments. J Dairy Sci 81:2765–2770Google Scholar
  134. 134.
    Wong HS, Townsend KM, Fenwick SG, Maker G, Trengove RD, O’Handley RM (2010) Comparative susceptibility of Salmonella Typhimurium biofilms of different ages to disinfectants. Biofouling 26:859–864Google Scholar
  135. 135.
    Wu H, Feng G-L, Li X-F, Liu H-W (2013) Application of proteomics in safety assessment and monitoring of food microorganisms. Mod Food Sci Technol 29:2793–2799Google Scholar
  136. 136.
    Xu H, Zou Y, Lee H-Y, Ahn J (2010) Effect of NaCl on the biofilm formation by foodborne pathogens. J Food Sci 75:M580–M585Google Scholar
  137. 137.
    Xu H, Lee H-Y, Ahn J (2011) Characteristics of biofilm formation by selected foodborne pathogens. J Food Saf 31:91–97Google Scholar
  138. 138.
    Yang H, Feirtag J, Diez-Gonzalez F (2013) Sanitizing effectiveness of commercial “active water” technologies on Escherichia coli O157:H7, Salmonella enterica and Listeria monocytogenes. Food Control 33:232–238Google Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Dipartimento di Scienze per gli Alimenti, la Nutrizione e l’AmbienteUniversità degli Studi di MilanoMilanItaly

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