Archives of Microbiology

, Volume 196, Issue 7, pp 453–472 | Cite as

Biofilm formation and persistence on abiotic surfaces in the context of food and medical environments

  • Marwan Abdallah
  • Corinne Benoliel
  • Djamel Drider
  • Pascal Dhulster
  • Nour-Eddine Chihib


The biofilm formation on abiotic surfaces in food and medical sectors constitutes a great public health concerns. In fact, biofilms present a persistent source for pathogens, such as Pseudomonas aeruginosa and Staphylococcus aureus, which lead to severe infections such as foodborne and nosocomial infections. Such biofilms are also a source of material deterioration and failure. The environmental conditions, commonly met in food and medical area, seem also to enhance the biofilm formation and their resistance to disinfectant agents. In this regard, this review highlights the effect of environmental conditions on bacterial adhesion and biofilm formation on abiotic surfaces in the context of food and medical environment. It also describes the current and emergent strategies used to study the biofilm formation and its eradication. The mechanisms of biofilm resistance to commercialized disinfectants are also discussed, since this phenomenon remains unclear to date.


Abiotic surfaces Biofilm Environmental conditions Biofilm resistance Disinfectants 



The authors are grateful to French Agency for Research and Technology (ANRT) and SCIENTIS laboratory for the CIFRE grant supporting this work (CIFRE: 2010/0205).


  1. Abdallah M et al (2014) Effect of growth temperature, surface type and incubation time on the resistance of Staphylococcus aureus biofilms to disinfectants. Appl Microbiol Biotechnol 98:2597–2607. doi: 10.1007/s00253-013-5479-4 PubMedGoogle Scholar
  2. Abddallah M, Benoliel C, Charafeddine J, Drider D, Dhulster P, Chihib NE (2014) Thermodynamic prediction of growth temperature dependence in the adhesion of Pseudomonas aeruginosa and Staphylococcus aureus to stainless steel and polycarbonate. J Food Prot. doi: 10.4315/0362-028X.JFP-13-365 Google Scholar
  3. Anaissie EJ, Penzak SR, Dignani MC (2002) The hospital water supply as a source of nosocomial infections: a plea for action. Arch Intern Med 162:1483–1492. doi: 10.1001/archinte.162.13.1483 PubMedGoogle Scholar
  4. Arciola CR, Campoccia D, Speziale P, Montanaro L, Costerton JW (2012) Biofilm formation in Staphylococcus implant infections. A review of molecular mechanisms and implications for biofilm-resistant materials. Biomaterials 33:5967–5982. doi: 10.1016/j.biomaterials.2012.05.031 PubMedGoogle Scholar
  5. Arnold JW, Bailey GW (2000) Surface finishes on stainless steel reduce bacterial attachment and early biofilm formation: scanning electron and atomic force microscopy study. Poult Sci 79:1839–1845PubMedGoogle Scholar
  6. Banin E, Vasil ML, Greenberg EP (2005) Iron and Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci USA 102:11076–11081. doi: 10.1073/pnas.0504266102 PubMedCentralPubMedGoogle Scholar
  7. Bayoudh S, Othmane A, Mora L, Ben Ouada H (2009) Assessing bacterial adhesion using DLVO and XDLVO theories and the jet impingement technique. Colloids Surf B Biointerfaces 73:1–9. doi: 10.1016/j.colsurfb.2009.04.030 PubMedGoogle Scholar
  8. Belessi CE, Gounadaki AS, Psomas AN, Skandamis PN (2011) Efficiency of different sanitation methods on Listeria monocytogenes biofilms formed under various environmental conditions. Int J Food Microbiol 1:25. doi: 10.1016/j.ijfoodmicro.2010.10.020 Google Scholar
  9. Benamara H, Rihouey C, Jouenne T, Alexandre S (2011) Impact of the biofilm mode of growth on the inner membrane phospholipid composition and lipid domains in Pseudomonas aeruginosa. Biochim Biophys Acta 1:98–105. doi: 10.1016/j.bbamem.2010.09.004 Google Scholar
  10. Bisbiroulas P, Psylou M, Iliopoulou I, Diakogiannis I, Berberi A, Mastronicolis SK (2011) Adaptational changes in cellular phospholipids and fatty acid composition of the food pathogen Listeria monocytogenes as a stress response to disinfectant sanitizer benzalkonium chloride. Lett Appl Microbiol 52:275–280. doi: 10.1111/j.1472-765X.2010.02995.x PubMedGoogle Scholar
  11. Bixler GD, Bhushan B (2012) Biofouling: lessons from nature. Philos Trans A Math Phys Eng Sci 370:2381–2417. doi: 10.1098/rsta.2011.0502 PubMedGoogle Scholar
  12. Boles BR, Horswill AR (2008) Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog 4:1000052. doi: 10.1371/journal.ppat.1000052 Google Scholar
  13. Bonez PC et al (2013) Chlorhexidine activity against bacterial biofilms. Am J Infect Control 1:00854–00857. doi: 10.1016/j.ajic.2013.05.002 Google Scholar
  14. Bos R, van der Mei HC, Busscher HJ (1999) Physico-chemistry of initial microbial adhesive interactions—its mechanisms and methods for study. FEMS Microbiol Rev 23:179–230. doi: 10.1111/j.1574-6976.1999.tb00396.x PubMedGoogle Scholar
  15. Bridier A, Dubois-Brissonnet F, Greub G, Thomas V, Briandet R (2011) Dynamics of the action of biocides in Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 55:2648–2654. doi: 10.1128/AAC.01760-10 PubMedCentralPubMedGoogle Scholar
  16. Bruinsma GM, van der Mei HC, Busscher HJ (2001) Bacterial adhesion to surface hydrophilic and hydrophobic contact lenses. Biomaterials 22:3217–3224. doi: 10.1016/S0142-9612(01)00159-4 PubMedGoogle Scholar
  17. Brunkard JM et al (2011) Surveillance for waterborne disease outbreaks associated with drinking water—United States, 2007–2008. MMWR Surveill Summ 60:38–68PubMedGoogle Scholar
  18. Bryers JD (2008) Medical biofilms. Biotechnol Bioeng 100:1–18. doi: 10.1002/bit.21838 PubMedCentralPubMedGoogle Scholar
  19. Buckingham-Meyer K, Goeres DM, Hamilton MA (2007) Comparative evaluation of biofilm disinfectant efficacy tests. J Microbiol Methods 70:236–244. doi: 10.1016/j.mimet.2007.04.010 PubMedGoogle Scholar
  20. Byrd MS et al (2009) Genetic and biochemical analyses of the Pseudomonas aeruginosa Psl exopolysaccharide reveal overlapping roles for polysaccharide synthesis enzymes in Psl and LPS production. Mol Microbiol 73:622–638. doi: 10.1111/j.1365-2958.2009.06795.x PubMedGoogle Scholar
  21. Campanac C, Pineau L, Payard A, Baziard-Mouysset G, Roques C (2002) Interactions between biocide cationic agents and bacterial biofilms. Antimicrob Agents Chemother 46:1469–1474. doi: 10.1128/AAC.46.5.1469-1474.2002 PubMedCentralPubMedGoogle Scholar
  22. Carnazza S, Satriano C, Guglielmino S, Marletta G (2005) Fast exopolysaccharide secretion of Pseudomonas aeruginosa on polar polymer surfaces. J Colloid Interface Sci 289:386–393. doi: 10.1016/j.jcis.2005.03.089 PubMedGoogle Scholar
  23. CDC (2013) Estimating foodborne illness: an overview. CDC J.
  24. Cerca N, Jefferson KK (2008) Effect of growth conditions on poly-N-acetylglucosamine expression and biofilm formation in Escherichia coli. FEMS Microbiol Lett 283:36–41. doi: 10.1111/j.1574-6968.2008.01142.x PubMedGoogle Scholar
  25. Cerca N, Pier GB, Vilanova M, Oliveira R, Azeredo J (2005) Quantitative analysis of adhesion and biofilm formation on hydrophilic and hydrophobic surfaces of clinical isolates of Staphylococcus epidermidis. Res Microbiol 156:506–514. doi: 10.1016/j.resmic.2005.01.007 PubMedCentralPubMedGoogle Scholar
  26. Cerf O, Carpentier B, Sanders P (2010) Tests for determining in-use concentrations of antibiotics and disinfectants are based on entirely different concepts: “resistance” has different meanings. Int J Food Microbiol 136:247–254. doi: 10.1016/j.ijfoodmicro.2009 PubMedGoogle Scholar
  27. Ceri H, Olson ME, Stremick C, Read RR, Morck D, Buret A (1999) The Calgary Biofilm Device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J Clin Microbiol 37:1771–1776PubMedCentralPubMedGoogle Scholar
  28. Chaturongkasumrit Y, Takahashi H, Keeratipibul S, Kuda T, Kimura B (2011) The effect of polyesterurethane belt surface roughness on Listeria monocytogenes biofilm formation and its cleaning efficiency. Food Control 22:1893–1899. doi: 10.1016/j.foodcont.2011.04.032 Google Scholar
  29. Chavant P, Martinie B, Meylheuc T, Bellon-Fontaine MN, Hebraud M (2002) Listeria monocytogenes LO28: surface physicochemical properties and ability to form biofilms at different temperatures and growth phases. Appl Environ Microbiol 68:728–737. doi: 10.1128/AEM.68.2.728-737.2002 PubMedCentralPubMedGoogle Scholar
  30. Chavant P, Gaillard-Martinie B, Hebraud M (2004) Antimicrobial effects of sanitizers against planktonic and sessile Listeria monocytogenes cells according to the growth phase. FEMS Microbiol Lett 236:241–248PubMedGoogle Scholar
  31. Chavant P, Gaillard-Martinie B, Talon R, Hebraud M, Bernardi T (2007) A new device for rapid evaluation of biofilm formation potential by bacteria. J Microbiol Methods 68:605–612. doi: 10.1016/j.mimet.2006.11.010 PubMedGoogle Scholar
  32. Chaves Simoes L, Simoes M (2013) Biofilms in drinking water: problems and solutions. RSC Adv 3:2520–2533. doi: 10.1039/c2ra22243d Google Scholar
  33. Cheesbrough M (2006) District laboratory practice in tropical countries. Cambridge University Press, Cambridge, MAGoogle Scholar
  34. Cherchi C, Gu AZ (2011) Effect of bacterial growth stage on resistance to chlorine disinfection. Water Sci Technol 64:7–13. doi: 10.2175/193864710798193608 PubMedGoogle Scholar
  35. Chia TW, Nguyen VT, McMeekin T, Fegan N, Dykes GA (2011) Stochasticity of bacterial attachment and its predictability by the extended Derjaguin-Landau-Verwey-Overbeek theory. Appl Environ Microbiol 77:3757–3764. doi: 10.2175/193864710798193608 PubMedCentralPubMedGoogle Scholar
  36. Choi N-Y, Kim B-R, Bae Y-M, Lee S-Y (2013) Biofilm formation, attachment, and cell hydrophobicity of foodborne pathogens under varied environmental conditions. J Korean Soc Appl Biol Chem 56:207–220. doi: 10.1007/s13765-012-3253-4 Google Scholar
  37. Cochran WL, Suh SJ, McFeters GA, Stewart PS (2000) Role of RpoS and AlgT in Pseudomonas aeruginosa biofilm resistance to hydrogen peroxide and monochloramine. J Appl Microbiol 88:546–553. doi: 10.1046/j.1365-2672.2000.00995.x PubMedGoogle Scholar
  38. Coenye T, De Prijck K, De Wever B, Nelis HJ (2008) Use of the modified Robbins device to study the in vitro biofilm removal efficacy of NitrAdine, a novel disinfecting formula for the maintenance of oral medical devices. J Appl Microbiol 105:733–740. doi: 10.1111/j.1365-2672.2008.03784.x PubMedGoogle Scholar
  39. Condell O et al (2012) Efficacy of biocides used in the modern food industry to control Salmonella enterica, and links between biocide tolerance and resistance to clinically relevant antimicrobial compounds. Appl Environ Microbiol 78:3087–3097. doi: 10.1128/AEM.07534-11 PubMedCentralPubMedGoogle Scholar
  40. Corbin A, Pitts B, Parker A, Stewart PS (2011) Antimicrobial penetration and efficacy in an in vitro oral biofilm model. Antimicrob Agents Chemother 55:3338–3344. doi: 10.1128/AAC.00206-11 PubMedCentralPubMedGoogle Scholar
  41. Cotter PA, Stibitz S (2007) c-di-GMP-mediated regulation of virulence and biofilm formation. Curr Opin Microbiol 10:17–23. doi: 10.1016/j.mib.2006.12.006 PubMedGoogle Scholar
  42. Czaczyk K, Myszka K (2007) Biosynthesis of extracellular polymeric substances (EPS) and its role in microbial biofilm formation. Pol J Environ Stud 16:799Google Scholar
  43. da Silva Meira QG, de Medeiros Barbosa I, Alves Aguiar Athayde AJ, 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 25:469–475. doi: 10.1016/j.foodcont.2011.11.030 Google Scholar
  44. Davis AO et al (2005) Characterization of Staphylococcus aureus mutants expressing reduced susceptibility to common house-cleaners. J Appl Microbiol 98:364–372. doi: 10.1111/j.1365-2672.2004.02460.x PubMedCentralPubMedGoogle Scholar
  45. Davison WM, Pitts B, Stewart PS (2010) Spatial and temporal patterns of biocide action against Staphylococcus epidermidis biofilms. Antimicrob Agents Chemother 54:2920–2927. doi: 10.1128/AAC.01734-09 PubMedCentralPubMedGoogle Scholar
  46. de Kievit TR (2009) Quorum sensing in Pseudomonas aeruginosa biofilms. Environ Microbiol 11:279–288. doi: 10.1111/j.1462-2920.2008.01792.x PubMedGoogle Scholar
  47. Dehus O et al (2011) Growth temperature-dependent expression of structural variants of Listeria monocytogenes lipoteichoic acid. Immunobiology 216:24–31. doi: 10.1016/j.imbio.2010.03.008 PubMedGoogle Scholar
  48. Donlan RM (2001) Biofilms and device-associated infections. Emerg Infect Dis 7:277–281PubMedCentralPubMedGoogle Scholar
  49. Donlan RM (2009) Preventing biofilms of clinically relevant organisms using bacteriophage. Trends Microbiol 17:66–72. doi: 10.1016/j.tim.2008.11.002 PubMedGoogle Scholar
  50. Donlan RM, Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15:167–193. doi: 10.1128/CMR.15.2.167-193.2002 PubMedCentralPubMedGoogle Scholar
  51. Dunne WM Jr (2002) Bacterial adhesion: seen any good biofilms lately? Clin Microbiol Rev 15:155–166. doi: 10.1128/CMR.15.2.155-166.2002 PubMedCentralPubMedGoogle Scholar
  52. EFSA (2009) The Community Summary Report on Food-Borne Outbreaks in The European Union in 2007. EFSA J. doi: 10.2903/j.efsa.2009.271r
  53. Epstein AK, Pokroy B, Seminara A, Aizenberg J (2011) Bacterial biofilm shows persistent resistance to liquid wetting and gas penetration. Proc Natl Acad Sci USA 108:995–1000. doi: 10.1073/pnas.1011033108 PubMedCentralPubMedGoogle Scholar
  54. Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633. doi: 10.1038/nrmicro2415 PubMedGoogle Scholar
  55. Flemming HC, Meier M, Schild T (2013) Mini-review: microbial problems in paper production. Biofouling 29:683–696. doi: 10.1080/08927014.2013.798865 PubMedGoogle Scholar
  56. Folsom JP et al (2010) Physiology of Pseudomonas aeruginosa in biofilms as revealed by transcriptome analysis. BMC Microbiol 10:1471–2180. doi: 10.1186/1471-2180-10-294 Google Scholar
  57. Friedman L, Kolter R (2004) Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol Microbiol 51:675–690. doi: 10.1046/j.1365-2958.2003.03877.x PubMedGoogle Scholar
  58. Ganeshnarayan K, Shah SM, Libera MR, Santostefano A, Kaplan JB (2009) Poly-N-acetylglucosamine matrix polysaccharide impedes fluid convection and transport of the cationic surfactant cetylpyridinium chloride through bacterial biofilms. Appl Environ Microbiol 75:1308–1314. doi: 10.1128/AEM.01900-08 PubMedCentralPubMedGoogle Scholar
  59. Ghafoor A, Hay ID, Rehm BH (2011) Role of exopolysaccharides in Pseudomonas aeruginosa biofilm formation and architecture. Appl Environ Microbiol 77:5238–5246. doi: 10.1128/AEM.00637-11 PubMedCentralPubMedGoogle Scholar
  60. Gianotti A, Serrazanetti D, Sado Kamdem S, Guerzoni ME (2008) Involvement of cell fatty acid composition and lipid metabolism in adhesion mechanism of Listeria monocytogenes. Int J Food Microbiol 123:9–17. doi: 10.1016/j.ijfoodmicro.2007.11.039 PubMedGoogle Scholar
  61. Giaouris E, Samoilis G, Chorianopoulos N, Ercolini D, Nychas GJ (2013) Differential protein expression patterns between planktonic and biofilm cells of Salmonella enterica serovar Enteritidis PT4 on stainless steel surface. Int J Food Microbiol 162:105–113. doi: 10.1016/j.ijfoodmicro.2012.12.023 PubMedGoogle Scholar
  62. Gilbert P, Moore LE (2005) Cationic antiseptics: diversity of action under a common epithet. J Appl Microbiol 99:703–715. doi: 10.1111/j.1365-2672.2005.02664.x PubMedGoogle Scholar
  63. Glinel K, Thebault P, Humblot V, Pradier CM, Jouenne T (2012) Antibacterial surfaces developed from bio-inspired approaches. Acta Biomater 8:1670–1684. doi: 10.1016/j.actbio.2012.01.011 PubMedGoogle Scholar
  64. Gomez-Suarez C et al (2002) Influence of extracellular polymeric substances on deposition and redeposition of Pseudomonas aeruginosa to surfaces. Microbiology 148:1161–1169PubMedGoogle Scholar
  65. Gordesli FP, Abu-Lail NI (2012) The role of growth temperature in the adhesion and mechanics of pathogenic L. monocytogenes: an AFM study. Langmuir 28:1360–1373. doi: 10.1021/la203639k PubMedGoogle Scholar
  66. Gounadaki AS, Skandamis PN, Drosinos EH, Nychas GJ (2008) Microbial ecology of food contact surfaces and products of small-scale facilities producing traditional sausages. Food Microbiol 25:313–323. doi: 10.1016/ PubMedGoogle Scholar
  67. Gousia P, Economou V, Sakkas H, Leveidiotou S, Papadopoulou C (2011) Antimicrobial resistance of major foodborne pathogens from major meat products. Foodborne Pathog Dis 8:27–38. doi: 10.1089/fpd.2010.0577 PubMedGoogle Scholar
  68. Grobe KJ, Zahller J, Stewart PS (2002) Role of dose concentration in biocide efficacy against Pseudomonas aeruginosa biofilms. J Ind Microbiol Biotechnol 29:10–15. doi: 10.1038/sj.jim.7000256 PubMedGoogle Scholar
  69. Guobjoernsdottir B, Einarsson H, Thorkelsson G (2005) Microbial adhesion to processing lines for fish fillets and cooked shrimp: influence of stainless steel surface finish and presence of gram-negative bacteria on the attachment of Listeria monocytogenes. Food Technol Biotechnol 43:55–61Google Scholar
  70. Gutierrez D et al (2012) Incidence of Staphylococcus aureus and analysis of associated bacterial communities on food industry surfaces. Appl Environ Microbiol 78:8547–8554. doi: 10.1128/AEM.02045-12 PubMedCentralPubMedGoogle Scholar
  71. Haagensen JA et al (2007) Differentiation and distribution of colistin- and sodium dodecyl sulfate-tolerant cells in Pseudomonas aeruginosa biofilms. J Bacteriol 189:28–37. doi: 10.1128/JB.00720-06 PubMedCentralPubMedGoogle Scholar
  72. Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108. doi: 10.1038/nrmicro821 PubMedGoogle Scholar
  73. Hamadi F et al (2005) Effect of pH on distribution and adhesion of Staphylococcus aureus to glass. J Adhes Sci Technol 19:73–85Google Scholar
  74. Hammond AA et al (2011) An in vitro biofilm model to examine the effect of antibiotic ointments on biofilms produced by burn wound bacterial isolates. Burns 37:312–321. doi: 10.1016/j.burns.2010.09.017 PubMedCentralPubMedGoogle Scholar
  75. Harmsen M, Yang L, Pamp SJ, Tolker-Nielsen T (2010) An update on Pseudomonas aeruginosa biofilm formation, tolerance, and dispersal. FEMS Immunol Med Microbiol 59:253–268. doi: 10.1111/j.1574-695X.2010.00690.x PubMedGoogle Scholar
  76. Harrison JJ et al (2008) Copper and quaternary ammonium cations exert synergistic bactericidal and antibiofilm activity against Pseudomonas aeruginosa. Antimicrob Agents Chemother 52:2870–2881. doi: 10.1128/AAC.00203-08 PubMedCentralPubMedGoogle Scholar
  77. Hassan M, Tuckman HP, Patrick RH, Kountz DS, Kohn JL (2010) Cost of hospital-acquired infection. Hosp Top 88:82–89. doi: 10.1080/00185868.2010.507124 PubMedGoogle Scholar
  78. Hassett DJ et al (1999) Quorum sensing in Pseudomonas aeruginosa controls expression of catalase and superoxide dismutase genes and mediates biofilm susceptibility to hydrogen peroxide. Mol Microbiol 34:1082–1093. doi: 10.1046/j.1365-2958.1999.01672.x PubMedGoogle Scholar
  79. Hemery G, Chevalier S, Bellon-Fontaine MN, Haras D, Orange N (2007) Growth temperature and OprF porin affect cell surface physicochemical properties and adhesive capacities of Pseudomonas fluorescens MF37. J Ind Microbiol Biotechnol 34:49–54. doi: 10.1007/s10295-006-0160-x PubMedGoogle Scholar
  80. Herrera JJ, Cabo ML, Gonzalez A, Pazos I, Pastoriza L (2007) Adhesion and detachment kinetics of several strains of Staphylococcus aureus subsp. aureus under three different experimental conditions. Food Microbiol 24:585–591. doi: 10.1016/ PubMedGoogle Scholar
  81. Hostacka A, Ciznar I, Stefkovicova M (2010) Temperature and pH affect the production of bacterial biofilm. Folia Microbiol 55:75–78. doi: 10.1007/s12223-010-0012-y Google Scholar
  82. Hota B (2004) Contamination, disinfection, and cross-colonization: are hospital surfaces reservoirs for nosocomial infection? Clin Infect Dis 39:1182–1189. doi: 10.1086/424667 PubMedGoogle Scholar
  83. Houry A, Briandet R, Aymerich S, Gohar M (2010) Involvement of motility and flagella in Bacillus cereus biofilm formation. Microbiology 156:1009–1018. doi: 10.1099/mic.0.034827-0 PubMedGoogle Scholar
  84. Huang C-Y et al (2009) Impact of disinfectant and nutrient concentration on growth and biofilm formation for Pseudomonas strain and the mixed cultures from a fine paper machine system. Int Biodeterior Biodegradation 63:998–1007. doi: 10.1016/j.ibiod.2009.07.004 Google Scholar
  85. Hui YW, Dykes GA (2012) Modulation of cell surface hydrophobicity and attachment of bacteria to abiotic surfaces and shrimp by Malaysian herb extracts. J Food Prot 75:1507–1511. doi: 10.4315/0362-028X PubMedGoogle Scholar
  86. Hwang G, Lee CH, Ahn IS, Mhin BJ (2010) Analysis of the adhesion of Pseudomonas putida NCIB 9816-4 to a silica gel as a model soil using extended DLVO theory. J Hazard Mater 179:983–988. doi: 10.1016/j.jhazmat.2010.03.101 PubMedGoogle Scholar
  87. Hwang G, Liang J, Kang S, Tong M, Liu Y (2013) The role of conditioning film formation in Pseudomonas aeruginosa PAO1 adhesion to inert surfaces in aquatic environments. Biochem Eng J 76:90–98. doi: 10.1016/j.bej.2013.03.024 Google Scholar
  88. Ioannou CJ, Hanlon GW, Denyer SP (2007) Action of disinfectant quaternary ammonium compounds against Staphylococcus aureus. Antimicrob Agents Chemother 51:296–306. doi: 10.1128/AAC.00375-06 PubMedCentralPubMedGoogle Scholar
  89. Jang A, Szabo J, Hosni AA, Coughlin M, Bishop PL (2006) Measurement of chlorine dioxide penetration in dairy process pipe biofilms during disinfection. Appl Microbiol Biotechnol 72:368–376. doi: 10.1007/s00253-005-0274-5 PubMedGoogle Scholar
  90. Karam L, Jama C, Dhulster P, Chihib NE (2013) Study of surface interactions between peptides, materials and bacteria for setting up antimicrobial surfaces and active food packaging. J Mater Environ Sci 4:798–821Google Scholar
  91. Karatan E, Watnick P (2009) Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol Mol Biol Rev 73:310–347. doi: 10.1128/MMBR.00041-08 PubMedCentralPubMedGoogle Scholar
  92. Kelly D, McAuliffe O, Ross RP, Coffey A (2012) Prevention of Staphylococcus aureus biofilm formation and reduction in established biofilm density using a combination of phage K and modified derivatives. Lett Appl Microbiol 54:286–291. doi: 10.1111/j.1472-765X.2012.03205.x PubMedGoogle Scholar
  93. Kim SH, Wei CI (2007) Antibiotic resistance and Caco-2 cell invasion of Pseudomonas aeruginosa isolates from farm environments and retail products. Int J Food Microbiol 115:356–363. doi: 10.1016/j.ijfoodmicro.2006.12.033 PubMedGoogle Scholar
  94. Klausen M et al (2003) Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Mol Microbiol 48:1511–1524. doi: 10.1046/j.1365-2958.2003.03525.x PubMedGoogle Scholar
  95. Klevens RM et al (2007) Estimating health care-associated infections and deaths in U.S. hospitals, 2002. Public Health Rep 122:160–166PubMedCentralPubMedGoogle Scholar
  96. Knobloch JK, Bartscht K, Sabottke A, Rohde H, Feucht HH, Mack D (2001) Biofilm formation by Staphylococcus epidermidis depends on functional RsbU, an activator of the sigB operon: differential activation mechanisms due to ethanol and salt stress. J Bacteriol 183:2624–2633. doi: 10.1128/JB.183.8.2624-2633.2001 PubMedCentralPubMedGoogle Scholar
  97. Korstgens V, Flemming HC, Wingender J, Borchard W (2001) Influence of calcium ions on the mechanical properties of a model biofilm of mucoid Pseudomonas aeruginosa. Water Sci Technol 43:49–57PubMedGoogle Scholar
  98. Langsrud S, Sundheim G, Holck AL (2004) Cross-resistance to antibiotics of Escherichia coli adapted to benzalkonium chloride or exposed to stress-inducers. J Appl Microbiol 96:201–208. doi: 10.1046/j.1365-2672.2003.02140.x PubMedGoogle Scholar
  99. Latorre AA et al (2010) Biofilm in milking equipment on a dairy farm as a potential source of bulk tank milk contamination with Listeria monocytogenes. J Dairy Sci 93:2792–2802. doi: 10.3168/jds.2009-2717 PubMedGoogle Scholar
  100. Lazazzera BA (2005) Lessons from DNA microarray analysis: the gene expression profile of biofilms. Curr Opin Microbiol 8:222–227. doi: 10.1016/j.mib.2005.02.015 PubMedGoogle Scholar
  101. Lequette Y, Boels G, Clarisse M, Faille C (2010) Using enzymes to remove biofilms of bacterial isolates sampled in the food-industry. Biofouling 26:421–431. doi: 10.1080/08927011003699535 PubMedGoogle Scholar
  102. Leung CY, Chan YC, Samaranayake LP, Seneviratne CJ (2012) Biocide resistance of Candida and Escherichia coli biofilms is associated with higher antioxidative capacities. J Hosp Infect 81:79–86. doi: 10.1016/j.jhin.2011.09.014 PubMedGoogle Scholar
  103. Lewis K (2010) Persister cells. Annu Rev Microbiol 64:357–372. doi: 10.1146/annurev.micro.112408.134306 PubMedGoogle Scholar
  104. Li B, Logan BE (2004) Bacterial adhesion to glass and metal-oxide surfaces. Colloids Surf B Biointerfaces 36:81–90. doi: 10.1016/j.colsurfb.2004.05.006 PubMedGoogle Scholar
  105. Lin C et al. (2011) Effect of superhydrophobic surface of titanium on Staphylococcus aureus adhesion. J Nanomater. doi:  10.1155/2011/178921
  106. Lin MH, Shu JC, Huang HY, Cheng YC (2012) Involvement of iron in biofilm formation by Staphylococcus aureus. PLoS One 7:27. doi: 10.1371/journal.pone.0034388 Google Scholar
  107. Litzler PY et al (2007) Biofilm formation on pyrolytic carbon heart valves: influence of surface free energy, roughness, and bacterial species. J Thorac Cardiovasc Surg 134:1025–1032. doi: 10.1016/j.jtcvs.2007.06.013 PubMedGoogle Scholar
  108. Loo CY, Young PM, Lee WH, Cavaliere R, Whitchurch CB, Rohanizadeh R (2012) Superhydrophobic, nanotextured polyvinyl chloride films for delaying Pseudomonas aeruginosa attachment to intubation tubes and medical plastics. Acta Biomater 8:1881–1890. doi: 10.1016/j.actbio.2012.01.015 PubMedGoogle Scholar
  109. Loughlin MF, Jones MV, Lambert PA (2002) Pseudomonas aeruginosa cells adapted to benzalkonium chloride show resistance to other membrane-active agents but not to clinically relevant antibiotics. J Antimicrob Chemother 49:631–639. doi: 10.1093/jac/49.4.631 PubMedGoogle Scholar
  110. Lu TK, Collins JJ (2007) Dispersing biofilms with engineered enzymatic bacteriophage. Proc Natl Acad Sci USA 104:11197–11202. doi: 10.1073/pnas.0704624104 PubMedCentralPubMedGoogle Scholar
  111. Luppens SB, Rombouts FM, Abee T (2002) The effect of the growth phase of Staphylococcus aureus on resistance to disinfectants in a suspension test. J Food Prot 65:124–129PubMedGoogle Scholar
  112. Ma L, Lu H, Sprinkle A, Parsek MR, Wozniak DJ (2007) Pseudomonas aeruginosa Psl is a galactose- and mannose-rich exopolysaccharide. J Bacteriol 189:8353–8356. doi: 10.1128/JB.00620-07 PubMedCentralPubMedGoogle Scholar
  113. Ma L, Conover M, Lu H, Parsek MR, Bayles K, Wozniak DJ (2009) Assembly and development of the Pseudomonas aeruginosa biofilm matrix. PLoS Pathog 5:27. doi: 10.1371/journal.ppat.1000354 Google Scholar
  114. Mafu AA, Roy D, Goulet J, Savoie L, Roy R (1990) Efficiency of sanitizing agents for destroying Listeria monocytogenes on contaminated surfaces. J Dairy Sci 73:3428–3432. doi: 10.3168/jds.S0022-0302(90)79040-6 PubMedGoogle Scholar
  115. Mafu AA, Plumety C, Deschenes L, Goulet J (2011) Adhesion of pathogenic bacteria to food contact surfaces: influence of pH of culture. Int J Microbiol 972494:11. doi: 10.1155/2011/972494 Google Scholar
  116. Maillard JY (2005) Antimicrobial biocides in the healthcare environment: efficacy, usage, policies, and perceived problems. Ther Clin Risk Manag 1:307–320PubMedCentralPubMedGoogle Scholar
  117. Manguiat LS, Fang TJ (2013) Microbiological quality of chicken- and pork-based street-vended foods from Taichung, Taiwan, and Laguna, Philippines. Food Microbiol 36:57–62. doi: 10.1016/ PubMedGoogle Scholar
  118. Mann EE, Wozniak DJ (2012) Pseudomonas biofilm matrix composition and niche biology. FEMS Microbiol Rev 36:893–916. doi: 10.1111/j.1574-6976.2011.00322.x PubMedGoogle Scholar
  119. Mann EE et al (2009) Modulation of eDNA release and degradation affects Staphylococcus aureus biofilm maturation. PLoS One 4:0005822. doi: 10.1371/journal.pone.0005822 Google Scholar
  120. Marino M, Frigo F, Bartolomeoli I, Maifreni M (2011) Safety-related properties of staphylococci isolated from food and food environments. J Appl Microbiol 110:550–561. doi: 10.1111/j.1365-2672.2010.04909.x PubMedGoogle Scholar
  121. Mc Cay PH, Ocampo-Sosa AA, Fleming GT (2010) Effect of subinhibitory concentrations of benzalkonium chloride on the competitiveness of Pseudomonas aeruginosa grown in continuous culture. Microbiology 156:30–38. doi: 10.1099/mic.0.029751-0 PubMedGoogle Scholar
  122. McDonnell G, Russell AD (1999) Antiseptics and disinfectants: activity, action, and resistance. Clin Microbiol Rev 12:147–179PubMedCentralPubMedGoogle Scholar
  123. McDougald D, Rice SA, Barraud N, Steinberg PD, Kjelleberg S (2011) Should we stay or should we go: mechanisms and ecological consequences for biofilm dispersal. Nat Rev Microbiol 10:39–50. doi: 10.1038/nrmicro2695 PubMedGoogle Scholar
  124. Mesaros N et al (2007) Pseudomonas aeruginosa: resistance and therapeutic options at the turn of the new millennium. Clin Microbiol Infect 13:560–578. doi: 10.1111/j.1469-0691.2007.01681.x PubMedGoogle Scholar
  125. Mitik-Dineva N et al (2009) Escherichia coli, Pseudomonas aeruginosa, and Staphylococcus aureus attachment patterns on glass surfaces with nanoscale roughness. Curr Microbiol 58:268–273. doi: 10.1007/s00284-008-9320-8 PubMedGoogle Scholar
  126. Morita Y et al (2003) Induction of mexCD-oprJ operon for a multidrug efflux pump by disinfectants in wild-type Pseudomonas aeruginosa PAO1. J Antimicrob Chemother 51:991–994. doi: 10.1093/jac/dkg173 PubMedGoogle Scholar
  127. Mulcahy H, Charron-Mazenod L, Lewenza S (2008) Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog 4:21. doi: 10.1371/journal.ppat.1000213 Google Scholar
  128. Newell DG et al (2010) Food-borne diseases—the challenges of 20 years ago still persist while new ones continue to emerge. Int J Food Microbiol 30:22. doi: 10.1016/j.ijfoodmicro.2010.01.021 Google Scholar
  129. Nguyen HDN, Yuk H-G (2013) Changes in resistance of Salmonella Typhimurium biofilms formed under various conditions to industrial sanitizers. Food Control 29:236–240. doi: 10.1016/j.foodcont.2012.06.006 Google Scholar
  130. Nguyen VT, Chia TW, Turner MS, Fegan N, Dykes GA (2011) Quantification of acid-base interactions based on contact angle measurement allows XDLVO predictions to attachment of Campylobacter jejuni but not Salmonella. J Microbiol Methods 86:89–96. doi: 10.1016/j.mimet.2011.04.005 PubMedGoogle Scholar
  131. Nilsson RE, Ross T, Bowman JP (2011) Variability in biofilm production by Listeria monocytogenes correlated to strain origin and growth conditions. Int J Food Microbiol 150:14–24. doi: 10.1016/j.ijfoodmicro.2011.07.012 PubMedGoogle Scholar
  132. Oulahal N, Martial-Gros A, Bonneau M, Blum LJ (2007) Removal of meat biofilms from surfaces by ultrasounds combined with enzymes and/or a chelating agent. Innov Food Sci Emerg Technol 8:192–196. doi: 10.1016/j.ifset.2006.10.001 Google Scholar
  133. Oulahal N, Brice W, Martial A, Degraeve P (2008) Quantitative analysis of survival of Staphylococcus aureus or Listeria innocua on two types of surfaces: polypropylene and stainless steel in contact with three different dairy products. Food Control 19:178–185. doi: 10.1016/j.foodcont.2007.03.006 Google Scholar
  134. Pagedar A, Singh J, Batish VK (2010) Surface hydrophobicity, nutritional contents affect Staphylococcus aureus biofilms and temperature influences its survival in preformed biofilms. J Basic Microbiol 50:201000034. doi: 10.1002/jobm.201000034 Google Scholar
  135. Palermo EF, Lee DK, Ramamoorthy A, Kuroda K (2011) Role of cationic group structure in membrane binding and disruption by amphiphilic copolymers. J Phys Chem B 115:366–375. doi: 10.1021/jp1083357 PubMedCentralPubMedGoogle Scholar
  136. Perrot F, Hebraud M, Charlionet R, Junter GA, Jouenne T (2000) Protein patterns of gel-entrapped Escherichia coli cells differ from those of free-floating organisms. Electrophoresis 21:645–653. doi: 10.1002/(SICI)1522-2683(20000201)21:3<645:AID-ELPS645>3.0.CO;2-1 PubMedGoogle Scholar
  137. Prokopovich P, Perni S (2009) An investigation of microbial adhesion to natural and synthetic polysaccharide-based films and its relationship with the surface energy components. J Mater Sci Mater Med 20:195–202. doi: 10.1007/s10856-008-3555-6 PubMedGoogle Scholar
  138. Rachid S, Ohlsen K, Wallner U, Hacker J, Hecker M, Ziebuhr W (2000) Alternative transcription factor sigma(B) is involved in regulation of biofilm expression in a Staphylococcus aureus mucosal isolate. J Bacteriol 182:6824–6826. doi: 10.1128/JB.182.23.6824-6826.2000 PubMedCentralPubMedGoogle Scholar
  139. Raisin (2013) Point prevalence survey of healthcare-associated infections and antimicrobial use in French hospitals, May–June 2012. Saint-Maurice: Institut de veille sanitaire; 2013.
  140. Renner LD, Weibel DB (2011) Physicochemical regulation of biofilm formation. MRS Bull 36:347–355PubMedCentralPubMedGoogle Scholar
  141. Resch A et al (2006) Comparative proteome analysis of Staphylococcus aureus biofilm and planktonic cells and correlation with transcriptome profiling. Proteomics 6:1867–1877. doi: 10.1002/pmic.200500531 PubMedGoogle Scholar
  142. Rice KC et al (2007) The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc Natl Acad Sci USA 104:8113–8118. doi: 10.1073/pnas.0610226104 PubMedCentralPubMedGoogle Scholar
  143. Rode TM, Langsrud S, Holck A, Moretro T (2007) Different patterns of biofilm formation in Staphylococcus aureus under food-related stress conditions. Int J Food Microbiol 116:372–383. doi: 10.1016/j.ijfoodmicro.2007.02.017 PubMedGoogle Scholar
  144. Rodriguez A, Autio WR, McLandsborough LA (2008) Effect of surface roughness and stainless steel finish on Listeria monocytogenes attachment and biofilm formation. J Food Prot 71:170–175PubMedGoogle Scholar
  145. Romao CM, Faria YN, Pereira LR, Asensi MD (2005) Susceptibility of clinical isolates of multiresistant Pseudomonas aeruginosa to a hospital disinfectant and molecular typing. Mem Inst Oswaldo Cruz 100:541–548. doi: 10.1590/S0074-02762005000500015 PubMedGoogle Scholar
  146. Rosenthal VD et al (2012) International Nosocomial Infection Control Consortium (INICC) report, data summary of 36 countries, for 2004–2009. Am J Infect Control 40:396–407. doi: 10.1016/j.ajic.2011.05.020 PubMedGoogle Scholar
  147. Sandt C, Barbeau J, Gagnon MA, Lafleur M (2007) Role of the ammonium group in the diffusion of quaternary ammonium compounds in Streptococcus mutans biofilms. J Antimicrob Chemother 60:1281–1287. doi: 10.1093/jac/dkm382 PubMedGoogle Scholar
  148. Sasidharan S, Prema B, Yoga LL (2011) Antimicrobial drug resistance of Staphylococcus aureus in dairy products. Asian Pac J Trop Biomed 1:130–132. doi: 10.1016/S2221-1691(11)60010-5 PubMedCentralPubMedGoogle Scholar
  149. Sauer K, Camper AK, Ehrlich GD, Costerton JW, Davies DG (2002) Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J Bacteriol 184:1140–1154. doi: 10.1128/jb.184.4.1140-1154.2002 PubMedCentralPubMedGoogle Scholar
  150. Sauer K, Cullen MC, Rickard AH, Zeef LA, Davies DG, Gilbert P (2004) Characterization of nutrient-induced dispersion in Pseudomonas aeruginosa PAO1 biofilm. J Bacteriol 186:7312–7326. doi: 10.1128/JB.186.21.7312-7326.2004 PubMedCentralPubMedGoogle Scholar
  151. Scharff RL (2012) Economic burden from health losses due to foodborne illness in the United States. J Food Prot 75:123–131. doi: 10.4315/0362-028X.JFP-11-058 PubMedGoogle Scholar
  152. Schlisselberg DB, Yaron S (2013) The effects of stainless steel finish on Salmonella Typhimurium attachment, biofilm formation and sensitivity to chlorine. Food Microbiol 35:65–72. doi: 10.1016/ PubMedGoogle Scholar
  153. Schulte S, Wingender J, Flemming H-C (2005) Efficacy of biocides against biofilms. In: Paulus W (ed) Directory of microbicides for the protection of materials. Springer, Berlin, pp 93–120Google Scholar
  154. Sharma M, Anand SK (2002) Characterization of constitutive microflora of biofilms in dairy processing lines. Food Microbiol 19:627–636. doi: 10.1006/fmic.2002.0472 Google Scholar
  155. Sharma PK, Rao KH (2002) Analysis of different approaches for evaluation of surface energy of microbial cells by contact angle goniometry. Adv Colloid Interface Sci 98:341–463. doi: 10.1016/S0001-8686(02)00004-0 PubMedGoogle Scholar
  156. Sharma S, Sachdeva P, Virdi JS (2003) Emerging water-borne pathogens. Appl Microbiol Biotechnol 61:424–428PubMedGoogle Scholar
  157. Shen Y, Stojicic S, Qian W, Olsen I, Haapasalo M (2010) The synergistic antimicrobial effect by mechanical agitation and two chlorhexidine preparations on biofilm bacteria. J Endod 36:100–104. doi: 10.1016/j.joen.2009.09.018 PubMedGoogle Scholar
  158. Shukla SK, Rao TS (2013) Effect of calcium on Staphylococcus aureus biofilm architecture: a confocal laser scanning microscopic study. Colloids Surf B Biointerfaces 103:448–454. doi: 10.1016/j.colsurfb.2012.11.003 PubMedGoogle Scholar
  159. Sievert DM et al (2013) Antimicrobial-resistant pathogens associated with healthcare-associated infections: summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2009–2010. Infect Control Hosp Epidemiol 34:1–14. doi: 10.1086/668770 PubMedGoogle Scholar
  160. Simoes LC, Lemos M, Pereira AM, Abreu AC, Saavedra MJ, Simoes M (2011) Persister cells in a biofilm treated with a biocide. Biofouling 27:403–411. doi: 10.1080/08927014.2011.579599 PubMedGoogle Scholar
  161. Simões M, Simões LC, Vieira MJ (2010) A review of current and emergent biofilm control strategies. LWT-Food Sci Technol 43:573–583. doi: 10.1016/j.lwt.2009.12.008 Google Scholar
  162. Singh AV et al (2011) Quantitative characterization of the influence of the nanoscale morphology of nanostructured surfaces on bacterial adhesion and biofilm formation. PLoS One 6:26. doi: 10.1371/journal.pone.0025029 Google Scholar
  163. Stewart PS, Franklin MJ (2008) Physiological heterogeneity in biofilms. Nat Rev Microbiol 6:199–210. doi: 10.1038/nrmicro1838 PubMedGoogle Scholar
  164. Stewart PS, Raquepas JB (1995) Implications of reaction-diffusion theory for the disinfection of microbial biofilms by reactive antimicrobial agents. Chem Eng Sci 50:3099–3104. doi: 10.1016/0009-2509(95)00143-S Google Scholar
  165. Stewart PS et al (2000) Effect of catalase on hydrogen peroxide penetration into Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 66:836–838. doi: 10.1128/AEM.66.2.836-838.2000 PubMedCentralPubMedGoogle Scholar
  166. Stewart PS, Rayner J, Roe F, Rees WM (2001) Biofilm penetration and disinfection efficacy of alkaline hypochlorite and chlorosulfamates. J Appl Microbiol 91:525–532. doi: 10.1046/j.1365-2672.2001.01413.x PubMedGoogle Scholar
  167. Stopforth JD, Samelis J, Sofos JN, Kendall PA, Smith GC (2002) Biofilm formation by acid-adapted and nonadapted Listeria monocytogenes in fresh beef decontamination washings and its subsequent inactivation with sanitizers. J Food Prot 65:1717–1727PubMedGoogle Scholar
  168. Suetens C, Hopkins S, Kolman J, Diaz Högberg L (2012) Point prevalence survey of healthcare-associated infections and antimicrobial use in European acute care hospitals 2011–2012. ECDCGoogle Scholar
  169. Surdeau N, Laurent-Maquin D, Bouthors S, Gelle MP (2006) Sensitivity of bacterial biofilms and planktonic cells to a new antimicrobial agent, Oxsil 320N. J Hosp Infect 62:487–493. doi: 10.1016/j.jhin.2005.09.003 PubMedGoogle Scholar
  170. Tabata A, Nagamune H, Maeda T, Murakami K, Miyake Y, Kourai H (2003) Correlation between resistance of Pseudomonas aeruginosa to quaternary ammonium compounds and expression of outer membrane protein OprR. Antimicrob Agents Chemother 47:2093–2099PubMedCentralPubMedGoogle Scholar
  171. Tang L, Pillai S, Revsbech NP, Schramm A, Bischoff C, Meyer RL (2011) Biofilm retention on surfaces with variable roughness and hydrophobicity. Biofouling 27:111–121 doi:  10.1128/AAC.47.7.2093-2099.2003. doi:  10.1080/08927014.2010.544848 Google Scholar
  172. Theraud M, Bedouin Y, Guiguen C, Gangneux JP (2004) Efficacy of antiseptics and disinfectants on clinical and environmental yeast isolates in planktonic and biofilm conditions. J Med Microbiol 53:1013–1018. doi: 10.1099/jmm.0.05474-0 PubMedGoogle Scholar
  173. Todd EC, Greig JD, Bartleson CA, Michaels BS (2009) Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 6. Transmission and survival of pathogens in the food processing and preparation environment. J Food Prot 72:202–219PubMedGoogle Scholar
  174. Toledo-Arana A, Merino N, Vergara-Irigaray M, Debarbouille M, Penades JR, Lasa I (2005) Staphylococcus aureus develops an alternative, ica-independent biofilm in the absence of the arlRS two-component system. J Bacteriol 187:5318–5329. doi: 10.1128/JB.187.15.5318-5329.2005 PubMedCentralPubMedGoogle Scholar
  175. Tote K, Horemans T, Vanden Berghe D, Maes L, Cos P (2010) Inhibitory effect of biocides on the viable masses and matrices of Staphylococcus aureus and Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 76:3135–3142. doi: 10.1128/AEM.02095-09 PubMedCentralPubMedGoogle Scholar
  176. Triandafillu K et al (2003) Adhesion of Pseudomonas aeruginosa strains to untreated and oxygen-plasma treated poly(vinyl chloride) (PVC) from endotracheal intubation devices. Biomaterials 24:1507–1518. doi: 10.1016/S0142-9612(02)00515-X PubMedGoogle Scholar
  177. Trotonda MP, Manna AC, Cheung AL, Lasa I, Penades JR (2005) SarA positively controls bap-dependent biofilm formation in Staphylococcus aureus. J Bacteriol 187:5790–5798. doi: 10.1128/JB.187.16.5790-5798.2005 PubMedCentralPubMedGoogle Scholar
  178. Tseng BS et al (2013) The extracellular matrix protects Pseudomonas aeruginosa biofilms by limiting the penetration of tobramycin. Environ Microbiol 13:1462–2920. doi: 10.1111/1462-2920.12155 Google Scholar
  179. van der Veen S, Abee T (2010) Importance of SigB for Listeria monocytogenes static and continuous-flow biofilm formation and disinfectant resistance. Appl Environ Microbiol 76:7854–7860. doi: 10.1128/AEM.01519-10 PubMedCentralPubMedGoogle Scholar
  180. Vazquez-Sanchez D, Habimana O, Holck A (2013) Impact of food-related environmental factors on the adherence and biofilm formation of natural Staphylococcus aureus isolates. Curr Microbiol 66:110–121. doi: 10.1007/s00284-012-0247-8 PubMedGoogle Scholar
  181. Verraes C et al (2013) Antimicrobial resistance in the food chain: a review. Int J Environ Res Public Health 10:2643–2669. doi: 10.3390/ijerph10072643 PubMedCentralPubMedGoogle Scholar
  182. Verran J, Whitehead K (2005) Factors affecting microbial adhesion to stainless steel and other materials used in medical devices. Int J Artif Organs 28:1138–1145PubMedGoogle Scholar
  183. Vickery K, Ngo QD, Zou J, Cossart YE (2009) The effect of multiple cycles of contamination, detergent washing, and disinfection on the development of biofilm in endoscope tubing. Am J Infect Control 37:470–475. doi: 10.1016/j.ajic.2008.09.016 PubMedGoogle Scholar
  184. Vickery K, Deva A, Jacombs A, Allan J, Valente P, Gosbell IB (2012) Presence of biofilm containing viable multiresistant organisms despite terminal cleaning on clinical surfaces in an intensive care unit. J Hosp Infect 80:52–55. doi: 10.1016/j.jhin.2011.07.007 PubMedGoogle Scholar
  185. Waite RD, Papakonstantinopoulou A, Littler E, Curtis MA (2005) Transcriptome analysis of Pseudomonas aeruginosa growth: comparison of gene expression in planktonic cultures and developing and mature biofilms. J Bacteriol 187:6571–6576. doi: 10.1128/JB.187.18.6571-6576.2005 PubMedCentralPubMedGoogle Scholar
  186. Wang X, Lunsdorf H, Ehren I, Brauner A, Romling U (2010) Characteristics of biofilms from urinary tract catheters and presence of biofilm-related components in Escherichia coli. Curr Microbiol 60:446–453. doi: 10.1007/s00284-009-9563-z PubMedGoogle Scholar
  187. Wang H, Sodagari M, Chen Y, He X, Newby BM, Ju LK (2011) Initial bacterial attachment in slow flowing systems: effects of cell and substrate surface properties. Colloids Surf B Biointerfaces 87:415–422. doi: 10.1016/j.colsurfb.2011.05.053 PubMedGoogle Scholar
  188. Wang X et al (2013) Staphylococcus aureus and methicillin-resistant Staphylococcus aureus in retail raw chicken in China. Food Control 29:103–106. doi: 10.1016/j.foodcont.2012.06.002 Google Scholar
  189. Weber H, Polen T, Heuveling J, Wendisch VF, Hengge R (2005) Genome-wide analysis of the general stress response network in Escherichia coli: sigmaS-dependent genes, promoters, and sigma factor selectivity. J Bacteriol 187:1591–1603. doi: 10.1128/JB.187.5.1591-1603.2005 PubMedCentralPubMedGoogle Scholar
  190. Weber DJ, Anderson D, Rutala WA (2013) The role of the surface environment in healthcare-associated infections. Curr Opin Infect Dis 26:338–344. doi: 10.1097/QCO.0b013e3283630f04 PubMedGoogle Scholar
  191. Weidenmaier C, Peschel A (2008) Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions. Nat Rev Microbiol 6:276–287. doi: 10.1038/nrmicro1861 PubMedGoogle Scholar
  192. Xavier JB, Picioreanu C, Rani SA, van Loosdrecht MC, Stewart PS (2005) Biofilm-control strategies based on enzymic disruption of the extracellular polymeric substance matrix—a modelling study. Microbiology 151:3817–3832. doi: 10.1099/mic.0.28165-0 PubMedGoogle Scholar
  193. Yang L, Hu Y, Liu Y, Zhang J, Ulstrup J, Molin S (2011) Distinct roles of extracellular polymeric substances in Pseudomonas aeruginosa biofilm development. Environ Microbiol 13:1705–1717. doi: 10.1111/j.1462-2920.2011 PubMedGoogle Scholar
  194. Zarei M, Maktabi S, Ghorbanpour M (2012) Prevalence of Listeria monocytogenes, Vibrio parahaemolyticus, Staphylococcus aureus, and Salmonella spp. in seafood products using multiplex polymerase chain reaction. Foodborne Pathog Dis 9:108–112. doi: 10.1089/fpd.2011.0989 PubMedGoogle Scholar
  195. Zhang Y, Hu Z (2013) Combined treatment of Pseudomonas aeruginosa biofilms with bacteriophages and chlorine. Biotechnol Bioeng 110:286–295. doi: 10.1002/bit.24630 PubMedGoogle Scholar
  196. Zhang Z, Nadezhina E, Wilkinson KJ (2011) Quantifying diffusion in a biofilm of Streptococcus mutans. Antimicrob Agents Chemother 55:1075–1081. doi: 10.1128/AAC.01329-10 PubMedCentralPubMedGoogle Scholar
  197. Zhao K et al (2013) Psl trails guide exploration and microcolony formation in Pseudomonas aeruginosa biofilms. Nature 497:388–391. doi: 10.1038/nature12155 PubMedGoogle Scholar
  198. Zita A, Hermansson M (1994) Effects of ionic strength on bacterial adhesion and stability of flocs in a wastewater activated sludge system. Appl Environ Microbiol 60:3041–3048PubMedCentralPubMedGoogle Scholar
  199. Zmantar T et al (2011) Atomic force microscopy and hydrodynamic characterization of the adhesion of Staphylococcus aureus to hydrophilic and hydrophobic substrata at different pH values. World J Microbiol Biotechnol 27:887–896. doi: 10.1007/s11274-010-0531-3 Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Marwan Abdallah
    • 1
    • 2
  • Corinne Benoliel
    • 2
  • Djamel Drider
    • 1
  • Pascal Dhulster
    • 1
  • Nour-Eddine Chihib
    • 1
  1. 1.Laboratoire de Procédés Biologiques, Génie Enzymatique et Microbien (ProBioGEM), IUT A/Polytech’LilleUniversité de Lille1-Science et TechnologiesVilleneuve d’Ascq CedexFrance
  2. 2.Laboratoire SCIENTISParc BiocitechRomainvilleFrance

Personalised recommendations