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Introduction to Biofilms

  • Steven L. PercivalEmail author
  • Sladjana Malic
  • Helena Cruz
  • David W. Williams
Chapter
Part of the Springer Series on Biofilms book series (BIOFILMS, volume 6)

Abstract

In the seventeenth century, a dry-goods merchant named Antonie van Leeuwenhoek first observed “animalcules” swarming on living and dead matter. Leeuwenhoek’s curiosity and inventiveness were remarkable; he discovered these “animalcules” in the tartar on his own teeth and even after meticulous cleansing, the remaining opaque deposits isolated between his teeth were still “as thick as if it were batter”. These deposits contained a mat of various forms of “animalcules” that we now know were the bacteria of dental plaque. It is reasonable to suggest that this early study of dental plaque was the first documented evidence of the existence of microbial biofilms. Today, we generally define such biofilms as microbial communities adhered to a substratum and encased within an extracellular polymeric substance (EPS) produced by the microbial cells themselves. Biofilms may form on a wide variety of surfaces, including natural aquatic systems living tissues, indwelling medical devices and industrial/potable water system piping. The vast majority of microbes grow as biofilms in aqueous environments. These biofilms can be benign or pathogenic, releasing harmful products and toxins, which become encased within the biofilm matrix. Biofilm formation is a phenomenon that occurs in both natural and man-made environments under diverse conditions, occurring on most moist surfaces, plant roots and nearly every living animal. Biofilms may exist as beneficial epithilic communities in rivers and streams, wastewater treatment plant trickling beds or in the alimentary canal of mammals. Given the prevalence of biofilms in natural environments, it is not surprising that these growth forms are responsible for infection in humans and animals. In humans, biofilms have been linked with numerous conditions and equally in animals equivalent infections may occur.

Keywords

Extracellular Polymeric Substance Quorum Sense Urinary Catheter Dental Plaque Extracellular Polymer 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Anderl JN, Zahller J, Roe F, Stewart PS (2003) Role of nutrient limitation and stationary-phase existence in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob Agents Chemother 47:1251–1256PubMedCrossRefGoogle Scholar
  2. Anwar H, Strap JL, Costerton JW (1992a) Establishment of aging biofilms: possible mechanism of bacterial resistance to antimicrobial therapy. Antimicrob Agents Chemother 36:1347–1351PubMedGoogle Scholar
  3. Anwar H, Strap JL, Chen K, Costerton JW (1992b) Dynamic interactions of biofilms of mucoid Pseudomonas aeruginosa with tobramycin and piperacillin. Antimicrob Agents Chemother 36:1208–1214PubMedGoogle Scholar
  4. Baier RE (1980) Substrate influence on adhesion of microorganisms and their resultant new surface properties. In: Bitton G, Marshall KC (eds) Adsorption of microorganisms to surfaces. Wiley, New York, pp 59–104Google Scholar
  5. Baier RE (1984) Initial events in microbial film formation. In: Costlow JD, Tipper RC (eds) Marine biodetermination: an interdisciplinary approach. E & FN Spon, London, pp 57–62Google Scholar
  6. Bashan Y, Levanony H (1988) Active attachment of Azospirillum brasilense Cd to quartz sand and to a light-textured soil by protein bridging. J Gen Microbiol 134:2269–2279Google Scholar
  7. Bayston R (1999) Medical problems due to biofilms: clinical impact, aetiology, molecular pathogenesis, treatment and prevention. In: Wilson M, Newman HN (eds) Dental plaque revisited: oral biofilms in health and disease. BioLine, Cardiff, pp 111–124Google Scholar
  8. Beech IB, Gaylarde CC (1989) Adhesion of Desulfovibrio desulfuricans and Pseudomonas fluorescens to mild steel surfaces. J Appl Bacteriol 67:2017Google Scholar
  9. Bendinger B, Rijnaarts HHM, Altendorf K, Zehnder AJB (1993) Physicochemical cell surface and adhesive properties of coryneform bacteria related to the presence and chain length of mycolic acids. Appl Environ Microbiol 59:3973–3977PubMedGoogle Scholar
  10. Blenkinsopp SA, Costerton JW (1991) Understanding bacterial biofilms. Trends Biotechnol 9:138–143CrossRefGoogle Scholar
  11. Braunwald E (1997) Valvular heart disease. In: Braunwald E (ed) Heart disease, vol 2. W.B. Saunders, PhiladelphiaGoogle Scholar
  12. Brooun A, Liu S, Lewis K (2000) A dose-response study of antibiotic resistance in Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 44:640–646PubMedCrossRefGoogle Scholar
  13. Brown MRW, Barker J (1999) Unexplored reservoirs of pathogenic bacteria: protozoa and biofilms. Trends Microbiol 7:46–50PubMedCrossRefGoogle Scholar
  14. Brown CM, Ellwood DC, Hunter JR (1977) Growth of bacteria at surfaces: influence of nutrient limitations. FEMS Microbiol Lett 1:163–165CrossRefGoogle Scholar
  15. Bryers JD (1984) Biofilm formation and chemostat dynamics: pure and mixed culture considerations. Biotechnol Bioeng 26:948–958PubMedCrossRefGoogle Scholar
  16. Bryers JD (1987) Biologically active surfaces; processes governing the formation and persistence of biofilms. Biotechnology 3:57–68Google Scholar
  17. Bullitt R, Makowski L (1995) Structural polymorphism of bacterial adhesion pili. Nature 373:164–167PubMedCrossRefGoogle Scholar
  18. Busscher HJ, Weerkamp A (1987) Specific and non-specific interactions: role in bacterial adhesion to solid substrata. FEMS Microbiol Rev 46:165–173CrossRefGoogle Scholar
  19. Buswell CM, Herlihy YM, Marsh PD, Keevil CW, Leach SA (1997) Coaggregation amongst aquatic biofilm bacteria. J Appl Microbiol 83:477–484CrossRefGoogle Scholar
  20. Caldwell DE, Korber DR, Lawrence JR (1992) Confocal laser microscopy and digital image analysis in microbial ecology. Adv Microb Ecol 12:1–67Google Scholar
  21. Carpentier B, Cerf O (1993) Biofilms and their consequences, with particular reference to hygiene in the food industry. J Appl Bacteriol 75:499–511PubMedGoogle Scholar
  22. Carrel T, Nguyen T, Kipfer B, Althaus U (1998) Definitive cure of recurrent prosthetic endocarditis using silver-coated St. Jude medical heart valves: a preliminary case report. J Heart Valve Dis 7(5):531–533PubMedGoogle Scholar
  23. Chamberlain AHL (1992) The role of adsorbed layers in bacterial adhesion. In: Melo LF, Bott TR, Fletcher M, Capdeville B (eds) Biofilms-science and technology. Kluwer Academic, Dordrecht, pp 59–67Google Scholar
  24. Characklis WG (1973) Attached microbial growths-II. Frictional resistance due to microbial slimes. Water Res 7:1249–1258CrossRefGoogle Scholar
  25. Characklis WG (1981) Fouling biofilm development: a process analysis. Biotechnol Bioeng 23:1923–1960CrossRefGoogle Scholar
  26. Characklis WG, Cooksey KE (1983) Biofilms and microbial fouling. Adv Appl Microbiol 29:93–138CrossRefGoogle Scholar
  27. Characklis WG, McFeters GA, Marshall KC (1990a) Physiological ecology of biofilm systems. In: Characklis WG, Marshall KC (eds) Biofilms. Wiley, New York, pp 341–393Google Scholar
  28. Characklis WG, Turakhia MH, Zelver N (1990b) Transfer and interfacial transport phenomena. In: Characklis WG, Marshall KC (eds) Biofilms. Wiley, New York, pp 265–340Google Scholar
  29. Connell JH, Slatyer RO (1977) Mechanisms of succession in natural communities and their role in community stability and organization. Am Nat 111:1119–1144CrossRefGoogle Scholar
  30. Corpe WA (1970) An acid polysaccharide produced by a primary film forming marine bacterium. Dev Ind Microbiol 11:402–412Google Scholar
  31. Corpe WA (1980) Microbial surface components involved in adsorption of microorganisms onto surfaces. In: Bitton G, Marshall KC (eds) Adsorption of microorganisms to surfaces. Wiley, New York, pp 105–144Google Scholar
  32. Costerton JW, Geesey GG (1979) In: Costerton JW, Colwell RR (eds) Native aquatic bacteria: enumeration, activity, and ecology. ASTM Press, Philadelphia, pp 7–18CrossRefGoogle Scholar
  33. Costerton JW, Lappin-Scott HM (1989) Behaviour of bacterial biofilms. Am Soc Microbiol News 55:650–654Google Scholar
  34. Costerton JW, Lashen ES (1984) The influence of biofilm efficacy of biocides on corrosion-causing bacteria. Mater Performance 23:34–37Google Scholar
  35. Costerton JW, Geesey GG, Cheng K-J (1978) How bacteria stick. Sci Am 238:86–95PubMedCrossRefGoogle Scholar
  36. Costerton JW, Irvin RT, Cheng KJ (1981) The bacterial glycocalyx in nature and disease. Annu Rev Microbiol 35:299–324PubMedCrossRefGoogle Scholar
  37. Costerton JW, Cheng KJ, Geesey GG, Ladd TIM, Nickel JC, Dasgupta M, Marie TJ (1987) Bacterial biofilms in nature and disease. Annu Rev Microbiol 41:435–464PubMedCrossRefGoogle Scholar
  38. Costerton JW, Lewandowski Z, de Beer D, Calwell D, Korber D, James G (1994) Biofilms, the customised microniches. J Bacteriol 176:2137–2142PubMedGoogle Scholar
  39. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM (1995) Microbial biofilms. Annu Rev Microbiol 49:711–745PubMedCrossRefGoogle Scholar
  40. Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322PubMedCrossRefGoogle Scholar
  41. Crampton SE, Gerke C, Schnell NF, Nichols WW, Gotz F (1999) The intacellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect Immun 67:5427–5433Google Scholar
  42. Danielsson A, Norkrans B, Bjornsson A (1977) On bacterial adhesion – the effect of certain enzymes on adhered cells in a marine Pseudomonas sp. Bot Mar 20:13–17CrossRefGoogle Scholar
  43. Davey ME, O’Toole A (2000) Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64:847–867PubMedCrossRefGoogle Scholar
  44. Davies D (2003) Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Discov 2:114–122PubMedCrossRefGoogle Scholar
  45. de Beer D, Stoodley P, Roe F, Lewandowski Z (1994) Effects of biofilm structures on oxygen distribution and mass transfer. Biotechnol Bioeng 43:1131–1138PubMedCrossRefGoogle Scholar
  46. De Kievit TR, Parkins MD, Gillis RJ, Srikumar R, Ceri H, Poole K, Iglewski BH, Storey DG (2001) Multidrug efflux pumps: expression patterns and contribution to antibiotic resistance in Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 45:1761–1770PubMedCrossRefGoogle Scholar
  47. Donlan R (2001) Biofilms and device-associated infections. Emerg Infect Dis 7:277–281PubMedCrossRefGoogle Scholar
  48. Donlan R, Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15:167–193PubMedCrossRefGoogle Scholar
  49. Douglas LJ (2003) Candida biofilms and their role in infection. Trends Microbiol 11:30–36PubMedCrossRefGoogle Scholar
  50. Dunne WM Jr (2002) Bacterial adhesion: seen any good biofilms lately? Clin Microbiol Rev 15:155–166PubMedCrossRefGoogle Scholar
  51. Flemming H-C, Wingender J, Griegbe T, Mayer C (2000) Physico-chemical properties of biofilms. In: Evans LV (ed) Biofilms: recent advances in their study and control. Harwood Academic, Amsterdam, pp 19–34Google Scholar
  52. Fletcher M (1977) The effects of culture concentration and age, time, and temperature on bacterial attachment to polystyrene. Can J Microbiol 23:1–6CrossRefGoogle Scholar
  53. Fletcher M (1980) The question of passive versus active attachment mechanisms in non-specific bacterial adhesion. In: Berkeley RCW (ed) Microbial adhesion to surfaces. Horwood, Chichester, pp 67–78Google Scholar
  54. Fletcher M, Loeb GI (1979) The influence of substratum characteristics on the attachment of a marine Pseudomonas to solid surfaces. Appl Environ Microbiol 37:67–72PubMedGoogle Scholar
  55. Fletcher M, Marshall KC (1982) Are solid surfaces of ecological significance to aquatic bacteria? Adv Microb Ecol 12:199–236Google Scholar
  56. Fredrickson AG (1977) Behaviour of mixed cultures of microorganisms. Annu Rev Microbiol 33:63–87CrossRefGoogle Scholar
  57. Fux CA, Costerton JW, Stewart PS, Stoodley P (2005) Survival strategies of infectious biofilms. Trends Microbiol 13:34–40PubMedCrossRefGoogle Scholar
  58. Gilbert P, Das J, Foley I (1997) Biofilm susceptibility to antimicrobials. Adv Dent Res 11:160–167PubMedCrossRefGoogle Scholar
  59. Habash M, Reid G (1999) Microbial biofilms: their development and significance for medical device-related infections. J Clin Pharmacol 39:887–898PubMedCrossRefGoogle Scholar
  60. Hamilton WA (1987) Biofilm: microbial interaction and metabolic activities. In: Fletcher M, Gray TRG, Jones JG (eds) Ecology of microbial communities. Society for general microbiology symposium 41. Cambridge University Press, Cambridge, pp 361–387Google Scholar
  61. Hamilton WA, Characklis WG (1989) Relative activities of cells in suspension and in biofilms. In: Characklis WG, Wilderer PA (eds) Structure and function of biofilms. Wiley, New York, pp 199–219Google Scholar
  62. Harrison JJ, Turner RJ, Ceri H (2005) Persister cells, the biofilm matrix and tolerance to metal cations in biofilm and planktonic Pseudomonas aeruginosa. Environ Microbiol 7:981–994PubMedCrossRefGoogle Scholar
  63. Heilmann C, Schweitzer O, Gerke C, Vanittanakom N, Mack D, Goetz F (1996) Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol Microbiol 20:1083–1091PubMedCrossRefGoogle Scholar
  64. Heukelekian H, Heller A (1940) Relation between food concentration and surface for bacterial growth. J Bacteriol 40:547–558PubMedGoogle Scholar
  65. Heurlier K, Denervaud V, Haas D (2006) Impact of quorum sensing on fitness of Pseudomonas aeruginosa. Int J Med Microbiol 296:93–102PubMedCrossRefGoogle Scholar
  66. Hill KE, Davies CE, Wilson MJ, Stephens P, Harding KG, Thomas DW (2003) Molecular analysis of the microflora in chronic venous leg ulceration. J Med Microbiol 52:365–369PubMedCrossRefGoogle Scholar
  67. Hofstad T (1992) Virulence factors in anaerobic bacteria. Eur J Clin Microbiol Infect Dis 11:1044–1048PubMedCrossRefGoogle Scholar
  68. Hoyle BD, Costerton JW (1991) Bacterial resistance to antibiotics: the role of biofilms. Prog Drug Res 37:91–105PubMedGoogle Scholar
  69. Humphrey BA, Dickson MR, Marshall KC (1979) Physiochemical and in situ observations on the adhesion of gliding bacteria to surfaces. Arch Microbiol 120:231–238CrossRefGoogle Scholar
  70. Illingworth B, Tweden K, Schroeder R, Cameron J (1999) In vivo efficacy of silver-coated (Silzone) infection-resistant polyester fabric against a biofilm-producing bacteria. Staphylococcus epidermidis. J Heart Valve Dis 7:524–530Google Scholar
  71. James GA, Beaudette L, Costerton JW (1995) Interspecies bacterial interactions in biofilms. J Ind Microbiol 15:257–262CrossRefGoogle Scholar
  72. Jones F (2005) Quorum sensing. Microbiol Today:34–35Google Scholar
  73. Jones HC, Roth IL, Saunders WM III (1969) Electron microscopic study of a slime layer. J Bacteriol 99:316–325PubMedGoogle Scholar
  74. Karchmer A, Gibbons G (1994) Infections of prosthetic heart valves and vascular grafts. In: Bisno AL, Waldovogel FA (eds) Infections associated with indwelling medical devices, 2nd edn. American Society for Microbiology, Washington, pp 213–249Google Scholar
  75. Keevil CW, Dowsett AB, Rogers J (1993) Legionella biofilms and their control. Society for Applied Bacteriology technical series: microbiofilms. Society for Applied Bacteriology, Bedford, pp 203–215Google Scholar
  76. Khardori N, Yassien M (1995) Biofilms in device-related infections. J Ind Microbiol Biotechnol 15:141–147Google Scholar
  77. Kolenbrander PE, Palmer RJ, Rickard AH, Jakubovics NS, Chalmers NI, Diaz PI (2006) Bacterial interactions and successions during plaque development. Periodontology 2000(42):47–79CrossRefGoogle Scholar
  78. König C, Schwank S, Blaser J (2001) Factors compromising antibiotic activity against biofilms of Staphylococcus epidermidis. Eur J Clin Microbiol Infect Dis 20:20–26PubMedCrossRefGoogle Scholar
  79. Korber DR, Lawrence JR, Sutton B, Caldwell DE (1989) Effect of laminar flow velocity on the kinetics of surface recolonization by Mot+ and Mot- Pseudomonas fluorescens. Microb Ecol 18:1–19CrossRefGoogle Scholar
  80. Kumamoto CA, Marcelo DV (2005) Alternative Candida albicans lifestyles: growth on surfaces. Annu Rev Microbiol 59:113–133PubMedCrossRefGoogle Scholar
  81. Lappin-Scott HM, Jass J, Costerton JW (1993) Microbial biofilm formation and characterisation. Society for Applied Bacteriology technical series No. 30. Society for Applied Bacteriology, BedfordGoogle Scholar
  82. Lawrence JR, Neu TR (1999) Confocal laser scanning microscopy for analysis of microbial biofilms. Meth Enzymol 310:131–144PubMedCrossRefGoogle Scholar
  83. Lewandowski Z, Stoodley P, Roe F (1995) Internal mass transport in heterogeneous biofilms. Recent advances in corrosion/95, paper no. 222. NACE International, HoustonGoogle Scholar
  84. Loeb GI, Neihof RA (1975) Marine conditioning films. Adv Chem Ser 145:319–335CrossRefGoogle Scholar
  85. Mack D, Nedelmann M, Krokotsch A, Schwarzkopf A, Heesemann J, Laufs R (1994) Characterization of transposon mutants of biofilm-producing Staphylococcus epidermidis impaired in the accumulative phase of biofilm production: genetic identification of a hexosamine-containing polysaccharide intercellular adhesin. Infect Immun 62:3244–3253PubMedGoogle Scholar
  86. Mack D, Fischer W, Krokotsch A, Leopold K, Hartmann R, Egge H, Laufs R (1996) The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear beta-1,6-linked glucosaminoglycan: purification and structural analysis. J Bacteriol 178:175–183PubMedGoogle Scholar
  87. Mah T, O’Toole GA (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9:34–39PubMedCrossRefGoogle Scholar
  88. Mah T, Pitts B, Pellock B, Walker GC, Stewart PS, O’Toole GA (2003) A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 426:306–310PubMedCrossRefGoogle Scholar
  89. Maira-Litran T, Allison DG, Gilbert P (2000) An evaluation of the potential of the multiple antibiotic resistance operon (mar) and the multidrug efflux pump acrAB to moderate resistance towards ciprofloxacin in Escherichia coli biofilms. J Antimicrob Chemother 45:789–795PubMedCrossRefGoogle Scholar
  90. Marmur A, Ruckenstein E (1986) Gravity and cell adhesion. J Colloid Interface Sci 114:261–266CrossRefGoogle Scholar
  91. Marsh PD (1995) Dental plaque. In: Lappin-Scott HM, Costerton JW (eds) Microbial biofilms. Cambridge University Press, Cambridge, pp 282–300CrossRefGoogle Scholar
  92. Marshall KC (1992) Biofilms: a overview of bacterial adhesion, activity and control at surfaces. Am Soc Microbiol News 58:202–207Google Scholar
  93. Marshall KC, Stout R, Mitchell R (1971) Mechanism of the initial events in the sorption of marine bacteria to surfaces. J Gen Microbiol 68:337–348Google Scholar
  94. McEldowney S, Fletcher M (1988) Effect of pH, temperature, and growth conditions on the adhesion of a gliding bacterium and three nongliding bacteria to polystyrene. Microb Ecol 16:183–195CrossRefGoogle Scholar
  95. Mittelman MW (1996) Adhesion to biomaterials. In: Fletcher M (ed) Bacterial adhesion: molecular and ecological diversity. Wiley-Liss, New York, pp 89–127Google Scholar
  96. Moore PCL, Lindsay JA (2001) Genetic variation among hospital isolates of methicillin-sensitive Staphylococcus aureus: evidence for horizontal transfer of virulence genes. J Clin Microbiol 39:2760–2767PubMedCrossRefGoogle Scholar
  97. Mulhall AB, Chapman RG, Crow RA (1988) Bacteriuria during indwelling urethral catheterization. J Hosp Infect 11:253–262PubMedCrossRefGoogle Scholar
  98. Nemoto K, Hirota K, Ono T, Murakami K, Nagao D, Miyake Y (2000) Effect of Varidase (streptokinase) on biofilm formed by Staphylococcus aureus. Chemotherapy 46:111–115PubMedCrossRefGoogle Scholar
  99. Palmer RJ, Sternberg C (1999) Modern microscopy in biofilm research: confocal microscopy and other approaches. Curr Opin Biotechnol 10:263–268PubMedCrossRefGoogle Scholar
  100. Palmer R Jr, White DC (1997) Developmental biology of biofilms: implications for treatment and control. Trends Microbiol 5:435–440PubMedCrossRefGoogle Scholar
  101. Parsek MR, Greenberg EP (2000) Acyl-homoserine lactone quorum sensing in Gram-negative bacteria: a signaling mechanism involved in associations with higher organisms. Proc Natl Acad Sci USA 97:8789–8793PubMedCrossRefGoogle Scholar
  102. Percival SL, Bowler PG (2004) Biofilms and their potential role in wound healing. Wounds 16:234–240Google Scholar
  103. Percival SL, Kite P (2007) Catheters and infection control. J Vasc Access 2:69–80Google Scholar
  104. Percival SL, Thomas JG (2009) Helicobacter pylori prevalence and transmission and role of biofilms. Water Health 7(3):469–477CrossRefGoogle Scholar
  105. Percival SL, Walker JT (1999) Biofilms and public health significance. Biofouling 14:99–115CrossRefGoogle Scholar
  106. Percival SL, Knapp JS, Wales DS, Edyvean RGJ (1999) The effect of flow and surface roughness on biofilm formation. J Microbiol Biotechnol 22:152–159Google Scholar
  107. Percival SL, Walker J, Hunter P (2000) Microbiological aspects of biofilms and drinking water. CRC Press, New YorkCrossRefGoogle Scholar
  108. Percival SL, Hegarty JH, McKay G, Reid D (2001) Helicobacter pylori in biofilms. In: Gilbert PG, Allison D, Walker JT, Brading M (eds) Biofilm community interactions: chance or necessity. Species consortia. Wiley, New York, pp 59–63Google Scholar
  109. Percival SL, Sabbuba NA, Kite P, Stickler DJ (2009) The effect of EDTA instillations on the rate of development of encrustation and biofilms in Foley catheters. Urol Res 37(4):205–209PubMedCrossRefGoogle Scholar
  110. Percival SL, Thomas J, Williams D (2010) Biofilms and bacterial imbalances in chronic wounds: anti-Koch. Int Wound J 7(3):169–175PubMedCrossRefGoogle Scholar
  111. Percival SL, Thomas J, Thomas D, Williams D (2011) Antimicrobial tolerance and role of biofilms and persister cells in wounds. Wound Repair Regen 19(1):1–9PubMedCrossRefGoogle Scholar
  112. Powell MS, Slater NKH (1982) Removal rate of bacterial cells from glass surfaces by fluid shear. Biotechnol Bioeng 24:2527–2537PubMedCrossRefGoogle Scholar
  113. Pringle JH, Fletcher M (1983) Influence of substratum wettability on attachment of freshwater bacteria to solid surfaces. Appl Environ Microbiol 45:811–817PubMedGoogle Scholar
  114. Raad II, Sabbagh MF, Rand KH, Sherertz RJ (1992) Quantitative tip culture methods and the diagnosis of central venous catheter-related infections. Diagn Microbiol Infect Dis 15:13–20PubMedCrossRefGoogle Scholar
  115. Ramage G, Martinez JP, Lopez-Ribot JL (2006) Candida biofilms on implanted biomaterials: a clinically significant problem. FEMS Yeast Res 6:979–986PubMedCrossRefGoogle Scholar
  116. Reid G, McGroarty J, Angotti R, Cook R (1988) Lactobacillus inhibitor production against Escherichia coli and coaggregation ability with uropathogens. Can J Microbiol 34:344–351PubMedCrossRefGoogle Scholar
  117. Rhoads DD, Wolcott RW, Cutting KF, Percival SL (2007) Evidence of biofilms in wounds and potential ramifications. In: Gilbert P, Allison D, Brading M, Pratten J, Spratt D, Upton M (eds) Biofilms: coming of age, vol 8. The Biofilm Club, pp. 131–143Google Scholar
  118. Rickard AH, Leach SA, Buswell CM, High NJ, Handley PS (2000) Coaggregation between aquatic bacteria is mediated by specific-growth-phase-dependent lectin-saccharide interactions. Appl Environ Microbiol 66:431–434PubMedCrossRefGoogle Scholar
  119. Rickard AH, Leach SA, Hall LS, Buswell CM, High NJ, Handley PS (2002) Phylogenetic relationships and coaggregation ability of freshwater biofilm bacteria. Appl Environ Microbiol 68:3644–3650PubMedCrossRefGoogle Scholar
  120. Rickard AH, Gilbert P, High NJ, Kolenbrander PE, Handley PS (2003a) Bacterial coaggregation: an integral process in the development of multi-species biofilms. Trends Microbiol 11:94–100PubMedCrossRefGoogle Scholar
  121. Rickard AH, McBain AJ, Ledder RG, Handley PS, Gilbert P (2003b) Coaggregation between freshwater bacteria within biofilm and planktonic communities. FEMS Microbiol Lett 220:133–140PubMedCrossRefGoogle Scholar
  122. Rittle KH, Helmstetter CE, Meyer AE, Baier RE (1990) Escherichia coli retention on solid surfaces as functions of substratum surface energy and cell growth phase. Biofouling 2:121–130CrossRefGoogle Scholar
  123. Rittman BE (1989) The effect of shear stress on biofilm loss rate. Biotechnol Bioeng 24:501–506CrossRefGoogle Scholar
  124. Roberts ME, Stewart PS (2005) Modelling protection from antimicrobial agents in biofilms through the formation of persister cells. Microbiology 151:75–80PubMedCrossRefGoogle Scholar
  125. Rosenberg M, Kjelleberg S (1986) Hydrophobic interactions in bacterial adhesion. Adv Microb Ecol 9:353–393Google Scholar
  126. Saye DE (2007) Recurring and antimicrobial-resistant infections: considering the potential role of biofilms in clinical practice. Ostomy Wound Care Manage 53:46–48Google Scholar
  127. Spoering AL, Lewis K (2001) Biofilms and planktonic cells of Pseudomonas aeruginosa have similar resistance to killing by antimicrobials. J Bacteriol 183:6746–6751PubMedCrossRefGoogle Scholar
  128. Stewart PS, Costerton JW (2001) Antibiotic resistance of bacteria in biofilms. Lancet 358:135–138PubMedCrossRefGoogle Scholar
  129. Stewart PS, Camper AK, Handran SD, Huang CT, Warnecke M (1997) Spatial distribution and coexistence of Klebsiella pneumoniae and Pseudomonas aeruginosa in biofilms. Microb Ecol 33:2–10PubMedCrossRefGoogle Scholar
  130. Stickler DJ (2002) Susceptibility of antibiotic-resistant Gram-negative bacteria to biocides: a perspective from the study of catheter biofilms. J Appl Microbiol 92:163S–170SPubMedCrossRefGoogle Scholar
  131. Stickler D (2005) Urinary catheters: ideal sites for the development of biofilm communities. Microbiol Today:22–25.Google Scholar
  132. Stickler DJ, Morris NS, Winters C (1999) Simple physical model to study formation and physiology of biofilms on urethral catheters. Meth Enzymol 310:494–501PubMedCrossRefGoogle Scholar
  133. Stoodley P, Boyle JD, Dodds I, Lappin-Scott HM (1997) Consensus model of biofilm structure. In: Biofilms: community interactions and control. Third meeting of the British Biofilm Club, Gregynog Hall, Powys, 26–28 September 1997, pp 1–9Google Scholar
  134. Sutherland IW (2001) The biofilm matrix: an immobilized but dynamic microbial environment. Trends Microbiol 9:222–227PubMedCrossRefGoogle Scholar
  135. Tenke P, Riedl CR, Jones GL, Williams GJ, Stickler D, Nagy E (2004) Bacterial biofilm formation on urologic devices and heparin coating as preventive strategy. Int J Antimicrob Agents 23:67–74CrossRefGoogle Scholar
  136. Trautner BW, Darouiche RO (2004) Role of biofilm in catheter-associated urinary tract infection. Am J Infect Control 32:177–183PubMedCrossRefGoogle Scholar
  137. Tunney MM, Jones DS, Gorman SP (1999) Biofilm and biofilm-related encrustations of urinary tract devices. In: Doyle RJ (ed) Methods in enzymology. Biofilms, vol 310. Academic, San Diego, pp 558–666Google Scholar
  138. Uhlinger DJ, White DC (1983) Relationship between physiological status and formation of extracellular polysaccharide glycocalyx in Pseudomonas atlantica. Appl Environ Microbiol 45:64–70PubMedGoogle Scholar
  139. Van der Mei HC, Free RH, Elving GJ, Van Weissenbruch R, Albers FW, Busscher HJ (2000) Effect of probiotic bacteria on prevalence of yeasts in oropharyngeal biofilms on silicone rubber voice prostheses in vitro. J Med Microbiol 49:713–718PubMedGoogle Scholar
  140. Vandevoorde L, Christiaens H, Verstraete W (1992) Prevalence of coaggregation reactions among chicken lactobacilli. J Appl Bacteriol 72:214–219PubMedGoogle Scholar
  141. Vieira MJ, Oliveira R, Melo L, Pinheiro M, van der Mei H (1992) Adhesion of Pseudomonas fluorescens to metallic surfaces. J Dispers Sci Technol 13(4):437–445CrossRefGoogle Scholar
  142. Wahl M (1989) Marine epibiosis. 1. Fouling and antifouling: some basic aspects. Mar Ecol Prog Ser 58:175–189CrossRefGoogle Scholar
  143. Walt DR, Smulow JB, Turesky SS, Hill RG (1985) The effect of gravity on initial microbial adhesion. J Colloid Interface Sci 107:334–336CrossRefGoogle Scholar
  144. Walters MC III, Roe F, Bugnicourt A, Franklin MJ, Stewart PS (2003) Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob Agents Chemother 47:317–323PubMedCrossRefGoogle Scholar
  145. Whittaker CJ, Klier CM, Kolenbrander PE (1996) Mechanisms of adhesion by oral bacteria. Annu Rev Microbiol 50:513–552PubMedCrossRefGoogle Scholar
  146. Wilson M (2001) Bacterial biofilms and human disease. Sci Prog 84:235–254PubMedCrossRefGoogle Scholar
  147. Wimpenny JWT, Colasanti R (1997) A unifying hypothesis for the structure of microbial biofilms based on cellular automaton models. FEMS Microbiol Ecol 22:1–6CrossRefGoogle Scholar
  148. Xie H, Cook GS, Costerton JW, Bruce G, Rose TM, Lamont RJ (2000) Intergeneric communication in dental plaque biofilms. J Bacteriol 182:7067–7069PubMedCrossRefGoogle Scholar
  149. Yarwood JM, Schlievert PM (2003) Quorum sensing in Staphylococcus infections. J Clin Investig 112:1620–1625PubMedGoogle Scholar
  150. Yasuda H, Ajiki Y, Koga T, Kawada H, Yokota T (1993) Interaction between biofilms formed by Pseudomonas aeruginosa and clarithromycin. Antimicrob Agents Chemother 37:1749–1755PubMedGoogle Scholar
  151. Zobell CE (1943) The effect of solid surfaces upon bacterial activity. J Bacteriol 46(1):39–56PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  • Steven L. Percival
    • 1
    Email author
  • Sladjana Malic
    • 2
  • Helena Cruz
    • 3
  • David W. Williams
    • 2
  1. 1.Department of Pathology, Medical SchoolWest Virginia UniversityMorgantownUSA
  2. 2.Oral Microbiology Group, Tissue Engineering and Reparative Dentistry, School of DentistryCardiff UniversityCardiffUK
  3. 3.Division of Microbiology and Risk Assessment, National Food InstituteTechnical University of DenmarkSøborgDenmark

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