Skip to main content

Characterization of Bacterial Adhesion and Biofilm Formation

  • Chapter
  • First Online:
Antimicrobial Coatings and Modifications on Medical Devices

Abstract

Antimicrobial materials require careful characterization and testing to evaluate their performance. Multiple methods exist for evaluating whether a material or coating prevents bacterial adhesion and/or biofilm formation. Given that the scenario and conditions in which the material or coating will be used must be taken into account to accurately assess anti-fouling efficacy, the selection of appropriate characterization techniques is critical. This chapter introduces the basic concepts associated with analyzing cell adhesion and describes several analytical methods that are used for testing. The testing procedure, benefits, and limitations of various techniques are also discussed.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. R.M. Donlan, Biofilms: microbial life on surfaces. Emerg. Infect. Dis. 8, 881–890 (2002)

    Article  Google Scholar 

  2. R. Rusconi, S. Lecuyer, L. Guglielmini, H.A. Stone, Laminar flow around corners triggers the formation of biofilm streamers. J. R. Soc. Interface 7, 1293–1299 (2010)

    Article  Google Scholar 

  3. R. Rusconi, S. Lecuyer, N. Autrusson, L. Guglielmini, A. Stone Howard, Secondary flow as a mechanism for the formation of Biofilm streamers. Biophys. J. 100, 1392–1399 (2011)

    Article  Google Scholar 

  4. P.G. Falkowski, T. Fenchel, E.F. DeLong, The microbial engines that drive Earth's biogeochemical cycles. Sci 320, 1034–1039 (2008)

    Article  Google Scholar 

  5. W.G. Zumft, Cell biology and molecular basis of denitrification. Microbiol. Mol. Biol. Rev. 61, 533–616 (1997)

    Google Scholar 

  6. J. Vymazal, Removal of nutrients in various types of constructed wetlands. Sci. Total Environ. 380, 48–65 (2007)

    Article  Google Scholar 

  7. C.J. Richardson, Mechanisms controlling phosphorus retention capacity in freshwater wetlands. Sci 228, 1424–1427 (1985)

    Article  Google Scholar 

  8. W.M. Dunne, Bacterial adhesion: seen any good Biofilms lately? Clin. Microbiol. Rev. 15, 155–166 (2002)

    Article  Google Scholar 

  9. L. Hall-Stoodley, J.W. Costerton, P. Stoodley, Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2, 95–108 (2004)

    Article  Google Scholar 

  10. P. Stoodley, K. Sauer, D.G. Davies, J.W. Costerton, Biofilms as complex differentiated communities. Annu. Rev. Microbiol. 56, 187–209 (2002)

    Article  Google Scholar 

  11. H.J. Busscher, H.C. Van der Mei, How do bacteria know they are on a surface and regulate their response to an adhering state. PLoS Pathog. 8, e1002440 (2012)

    Article  Google Scholar 

  12. H.H. Tuson, D.B. Weibel, Bacteria-surface interactions. Soft Matter 9, 4368–4380 (2013)

    Article  Google Scholar 

  13. R. Bos, H.C. Van der Mei, H.J. Busscher, Physico-chemistry of initial microbial adhesive interactions- its mechanisms and methods for study. FEMS Microbiol. Rev. 23, 179–230 (1999)

    Article  Google Scholar 

  14. H. Wang, M. Sodagari, Y. Chen, X. He, B.M. Newby, et al., Initial bacterial attachment in slow flowing systems: effects of cell and substrate surface properties. Colloids Surf. B Biointerfaces 87, 415–422 (2011)

    Article  Google Scholar 

  15. Y. Liu, J. Strauss, T.A. Camesano, Thermodynamic investigation of Staphylococcus epidermis interactions with protein-coated substrata. Langmuir 23, 7134–7142 (2007)

    Article  Google Scholar 

  16. M.E. Schrader, Young-dupre revisited. Langmuir 11, 3585–3589 (1995)

    Article  Google Scholar 

  17. N.P. Boks, W. Norde, H.C. van der Mei, H.J. Busscher, Forces involved in bacterial adhesion to hydrophilic and hydrophobic surfaces. Microbiology 154, 3122–3133 (2008)

    Article  Google Scholar 

  18. M.C.M. Van Loosdrecht, J. Lyklema, W. Norde, A.J.B. Zehnder, Influence of interfaces on microbial activity. Microbiol. Rev. 54, 75–87 (1990)

    Google Scholar 

  19. S.F. Simoni, H. Harms, T.N.P. Bosma, A.J.B. Zehnder, Population heterogeneity affects transport of bacteria through sand columns at low flow rates. Environ. Sci. Technol. 32, 2100–2105 (1998)

    Article  Google Scholar 

  20. M.C.M. Van Loosdrecht, J. Lyklema, W. Norde, A.J.B. Zehnder, Bacterial adhesion: a physicochemical approach. Microb. Ecol. 17, 1–15 (1989)

    Article  Google Scholar 

  21. J.T. Gannon, V.B. Manilal, M. Alexander, Relationship between cell surface properties and transport of bacteria through soil. Appl. Environ. Microbiol. 57, 190–193 (1991)

    Google Scholar 

  22. T.J. Silhavy, D. Kahne, S. Walker, The bacterial cell envelope. Cold Spring Harb. Perspect. Biol. 2, a000414 (2010)

    Article  Google Scholar 

  23. M. Hermansson, The DLVO theory in microbial adhesion. Colloids Surf. B: Biointerfaces 14, 105–119 (1999)

    Article  Google Scholar 

  24. K. Hori, S. Matsumoto, Bacterial adhesion: from mechanism to control. Biochem. Eng. J. 48, 424–434 (2010)

    Article  Google Scholar 

  25. J.A. Redman, S.L. Walker, M. Elimelech, Bacterial adhesion and transport in porous media: role of the secondary energy minimum. Environ. Sci. Technol. 38, 1777–1785 (2004)

    Article  Google Scholar 

  26. H.H.M. Rijnaarts, W. Norde, E.J. Bouwer, J. Lyklema, A.J.B. Zehnder, Reversibility and mechanism of bacterial adhesion. Colloids Surf. B: Biointerfaces 4, 5–22 (1995)

    Article  Google Scholar 

  27. A. Zita, M. Hermansson, Effects of bacterial cell surface structures and Hydrophobicity on attachment to activated sludge Flocs. Appl. Environ. Microbiol. 63, 1168–1170 (1997)

    Google Scholar 

  28. A. Zita, M. Hermansson, Determination of bacterial cell surface hydrophobicity of single cells in cultures and in wastewater in situ. FEMS Microbiol. Lett. 152, 299–306 (1997)

    Article  Google Scholar 

  29. M.C.M. van Loosdrecht, J. Lyklema, W. Norde, G. Schraa, A.J.B. Zehnder, Electrophoretic mobility and hydrophobicity as a measured to predict the initial steps of bacterial adhesion. Appl. Environ. Microbiol. 53, 1898–1901 (1987)

    Google Scholar 

  30. M. Morra, C. Cassinelli, Bacterial adhesion to polymer surfaces: a critical review of surface thermodynamic approaches. J. Biomater. Sci. Polym. Ed. 9, 55–74 (1998)

    Article  Google Scholar 

  31. W. Qu, H.J. Busscher, J.M. Hooymans, H.C. van der Mei, Surface thermodynamics and adhesion forces governing bacterial transmission in contact lens related microbial keratitis. J. Colloid Interface Sci. 358, 430–436 (2011)

    Article  Google Scholar 

  32. S. McEldowney, M. Fletcher, Variablity of the influence of Physicochemical factors affecting bacterial adhesion to polystyrene Subsrata. Appl. Environ. Microbiol. 52, 460–465 (1986)

    Google Scholar 

  33. P.K. Sharma, K. Hanumantha Rao, Adhesion of Paenibacillus polymyxa on chalcopyrite and pyrite: surface thermodynamics and extended DLVO theory. Colloids Surf. B: Biointerfaces 29, 21–38 (2003)

    Article  Google Scholar 

  34. L.S. Dorobantu, S. Bhattacharjee, J.M. Foght, M.R. Gray, Analysis of force interactions between AFM tips and hydrophobic bacteria using DLVO theory. Langmuir 25, 6968–6976 (2009)

    Article  Google Scholar 

  35. G. Hwang, I.S. Ahn, B.J. Mhin, J.Y. Kim, Adhesion of nano-sized particles to the surface of bacteria: mechanistic study with the extended DLVO theory. Colloids Surf. B: Biointerfaces 97, 138–144 (2012)

    Article  Google Scholar 

  36. C. Van Oss, Energetics of cell-cell and cell-biopolymer interactions. Cell Biophys. 14, 1–16 (1989)

    Article  Google Scholar 

  37. Y.-L. Ong, A. Razatos, G. Georgiou, M.M. Sharma, Adhesion forces between E. coli bacteria and biomaterial surfaces. Langmuir 15, 2719–2725 (1999)

    Article  Google Scholar 

  38. I. Banerjee, R.C. Pangule, R.S. Kane, Antifouling coatings: recent developments in the design of surfaces that prevent fouling by proteins, bacteria, and marine organisms. Adv. Mater. 23, 690–718 (2011)

    Article  Google Scholar 

  39. D.R. Monteiro, L.F. Gorup, A.S. Takamiya, A.C. Ruvollo-Filho, E.R. de Camargo, et al., The growing importance of materials that prevent microbial adhesion: antimicrobial effect of medical devices containing silver. Int. J. Antimicrob. Agents 34, 103–110 (2009)

    Article  Google Scholar 

  40. R.P. Allaker, The use of nanoparticles to control oral biofilm formation. J. Dent. Res. 89, 1175–1186 (2010)

    Article  Google Scholar 

  41. M.L.W. Knetsch, L.H. Koole, New strategies in the development of antimicrobial coatings: the example of increasing usage of silver and silver Nanoparticles. Polymer 3, 340–366 (2011)

    Article  Google Scholar 

  42. L.K. Ista, H. Fan, O. Baca, G.P. Lopez, Attachment of bacteria to model solid surfaces: oligo (ethylene glycol) surfaces inhibit bacterial attachment. FEMS Microbiol. Lett. 142, 59–63 (1996)

    Article  Google Scholar 

  43. E. Ostuni, R.G. Chapman, M.N. Liang, G. Meluleni, G. Pier, D.E. Ingber, G.M. Whitesides, Self-assembled Monolayers that resist the adsorption of proteins and the adhesion of bacterial and mammalian cells. Langmuir 17, 6336–6343 (2001)

    Article  Google Scholar 

  44. H.C. Flemming, J. Wingender, The biofilm matrix. Nat. Rev. Microbiol. 8, 623–633 (2010)

    Google Scholar 

  45. G. O'Toole, H.B. Kaplan, R. Kolter, Biofilm formation as microbial development. Annu. Rev. Microbiol. 54, 49–79 (2000)

    Article  Google Scholar 

  46. J. Kim, H.D. Park, S. Chung, Microfluidic approaches to bacterial biofilm formation. Molecules 17, 9818–9834 (2012)

    Article  Google Scholar 

  47. J.L. Connell, A.K. Wessel, M.R. Parsek, A.D. Ellington, M. Whiteley, J.B. Shear, Probing prokaryotic social behaviors with bacterial “lobster traps”. MBio 1(4), e00202–e00210 (2010)

    Article  Google Scholar 

  48. D.G. Davies, M.R. Parsek, J.P. Pearson, B.H. Iglewski, J.W. Costerton, E.P. Greenberg, The involvement of cell-to-cell signals in the development of a bacterial Biofilm. Science 280, 295–298 (1998)

    Article  Google Scholar 

  49. D.G. Davies, A.M. Chakrabarty, G.G. Geesey, Exopolysaccharide production in biofilms: Substratum activation of alginate gene expression by Pseudomonas aeruginosa. Appl. Environ. Microbiol. 59, 1181–1186 (1993)

    Google Scholar 

  50. D.G. Davies, G.G. Geesey, Regulation of the alginate biosynthesis Gene algC in Pseudomonas aeruginosa during Biofilm development in continuous culture. Appl. Environ. Microbiol. 61, 860–867 (1995)

    Google Scholar 

  51. O. Bahar, L. De La Fuente, S. Burdman, Assessing adhesion, biofilm formation and motility of Acidovorax citrulli using microfluidic flow chambers. FEMS Microbiol. Lett. 312, 33–39 (2010)

    Article  Google Scholar 

  52. A. Perry, I. Ofek, F.J. Silverblatt, Enhancement of mannose-mediated stimulation of human granulocytes by type 1 Fimbriae aggregated with antibodies on Escherichia coli surfaces. Infect. Immun. 39, 1334–1345 (1983)

    Google Scholar 

  53. S.N. Abraham, D. Sun, J.B. Dale, E.H. Beachey, Conservation of the D-mannose-adhesion protein among type 1 fimbriated members of the family Enterobacteriaceae. Nature 336, 682–684 (1988)

    Article  Google Scholar 

  54. M.N. Liang, S.P. Smith, S.J. Metallo, I.S. Choi, M. Prentiss, G.M. Whitesides, Measuring the forces involved in polyvalent adhesion of uropathogenic Escherichia coli to mannose-presenting surfaces. Proc. Natl. Acad. Sci. U. S. A. 97, 13092–13096 (2000)

    Article  Google Scholar 

  55. K.A. Krogfelt, H. Bergmans, P. Klemm, Direct evidence that the FimH protein is the mannose-specific Adhesin of Escherichia coli type 1 Fimbriae. Infect. Immun. 58, 1995–1998 (1990)

    Google Scholar 

  56. S.H. Hong, M. Hegde, J. Kim, X. Wang, A. Jayaraman, T.K. Wood, Synthetic quorum-sensing circuit to control consortial biofilm formation and dispersal in a microfluidic device. Nat. Commun. 3, 613 (2012)

    Article  Google Scholar 

  57. K. Lewis, Persister cells and the riddle of Biofilm survival. Biochem. Mosc. 70, 267–274 (2005)

    Article  Google Scholar 

  58. K. Sauer, A.K. Camper, G.D. Ehrlich, J.W. Costerton, D.G. Davies, Pseudomonas Aeruginosa displays multiple phenotypes during development as a Biofilm. J. Bacteriol. 184, 1140–1154 (2002)

    Article  Google Scholar 

  59. I. Kolodkin-Gal, S. Cao, L. Chai, T. Bottccher, R. Kolter, J. Clardy, R. Losick, A self-produced trigger for biofilm disassembly that targets exopolysaccharide. Cell 149(3), 684–692 (2012)

    Article  Google Scholar 

  60. CBE milestones: An abbreviated timeline. Retrieved 20 Apr 2015., from https://www.biofilm.montana.edu/cbe-milestones-abbreviated-timeline.html

  61. N. Zelver, M. Hamilton, B. Pitts, D. Goeres, D. Walker, P. Sturman, J. Heersink, Measuring antimicrobial effects on Biofilm bacteria: from laboratory to field. Methods Enzymol. 310, 608–628 (1999)

    Article  Google Scholar 

  62. ASTM E2562–12 Standard test method for quantification of Pseudomonas aeruginosa Biofilm grown with high shear and continuous flow using CDC Biofilm reactor, (2012), Retrieved 20 Apr 2015, from http://www.astm.org/Standards/E2562.htm

  63. D.L. Williams, K.L. Woodbury, B.S. Haymond, A.E. Parker, R.D. Bloebaum, A modified CDC Biofilm reactor to produce mature Biofilms on the surface of PEEK membranes for an in vivo animal model application. Curr. Microbiol. 62(6), 1657–1663 (2011)

    Article  Google Scholar 

  64. ASTM E2647–13 Standard test method for quantification of Pseudomonas aeruginosa Biofilm grown using Drip Flow Biofilm reactor with low shear and continuous flow, (2013), Retrieved 20 Apr 2015, from http://www.astm.org/Standards/E2647.htm

  65. Y. Liu, J.H. Tay, Metabolic response of biofilm to shear stress in fixed-film culture. J. Appl. Microbiol. 90(3), 337–342 (2001)

    Article  Google Scholar 

  66. A.P. Foncesa, J.C. Sousa, Effect of shear stress on growth, adhesion and biofilm formation of Pseudomonas Aeruginosa with antibiotic-induced morphological changes. Int. J. Antimicrob. Agents 30(3), 236–241 (2007)

    Article  Google Scholar 

  67. H. Ceri, M.E. Olson, C. Stremick, R.R. Read, D. Morck, A. Buret, The Calgary Biofilm device: new technology for rapid determination of antibiotic susceptibilities of bacterial Biofilms. J. Clin. Microbiol. 37(6), 1771–1776 (1999)

    Google Scholar 

  68. L. Santopolo, E. Marchi, L. Frediani, F. Decorosi, C. Viti, L. Giovannetti, A novel approach combining the Calgary Biofilm device and phenotype MicroArray for the characterization of the chemical sensitivity of bacterial biofilms. Biofouling 28(9), 1023–1032 (2012)

    Article  Google Scholar 

  69. Y.C. Choi, E. Morgenroth, Monitoring biofilm detachment under dynamic changes in shear stress using laser-based particle size analysis and mass fractionation. Water Sci. Technol. 47(5), 69–76 (2013)

    Google Scholar 

  70. E.L. Decker, B. Frank, Y. Suo, S. Garoff, Physics of contact angle measurement. Colloids Surf. A Physicochem. Eng. Asp. 156, 177–189 (1999)

    Article  Google Scholar 

  71. D. Daffonchio, J. Thaveesri, W. Verstraete, Contact angle measurement and cell Hydrophobicity of granular sludge from upflow anaerobic sludge bed reactors. Appl. Environ. Microbiol. 61, 3676–3680 (1995)

    Google Scholar 

  72. Y.C. Jung, B. Bhushan, Technique to measure contact angle of micro/nanodroplets using atomic force microscopy. J. Vac. Sci. Technol. A 26, 777 (2008)

    Article  Google Scholar 

  73. A.M. Gallardo-Moreno, M.L. Navarro-Perez, V. Vadillo-Rodriguez, J.M. Bruque, M.L. Gonzalez-Martin, Insights into bacterial contact angles: difficulties in defining hydrophobicity and surface Gibbs energy. Colloids Surf. B: Biointerfaces 88(1), 373–380 (2011)

    Article  Google Scholar 

  74. R.J. Palmer Jr., C. Sternberg, Modern microscopy in Biofilm research: confocal microscopy and other approaches. Curr. Opin. Biotechnol. 10, 263–268 (1999)

    Article  Google Scholar 

  75. M. Fletcher, Bacterial biofilms and biofouling. Curr. Opin. Biotechnol. 5, 302–306 (1994)

    Article  Google Scholar 

  76. M. Ferrando, W.E.L. Spiess, Review: confocal scanning laser microscopy. A powerful tool in food science. Food Sci. Technol. Int. 6, 267–284 (2000)

    Article  Google Scholar 

  77. Y. Yawata, K. Toda, E. Setoyama, J. Fukuda, H. Suzuki, H. Uchiyama, N. Nomura, Monitoring biofilm development in a microfluidic device using modified confocal reflection microscopy. J. Biosci. Bioeng. 110, 377–380 (2010)

    Article  Google Scholar 

  78. J.R. Lawrence, D.R. Korber, B.D. Hoyle, J.W. Costerton, D.E. Caldwell, Optical sectioning of microbial Biofilms. J. Bacteriol. 173, 6558–6567 (1991)

    Article  Google Scholar 

  79. D.E. Caldwell, D.R. Korber, J.R. Lawrence, Imaging of bacterial cells by fluorescence exclusion using scanning confocal laser microscopy. J. Microbiol. Methods 15, 249–261 (1992)

    Article  Google Scholar 

  80. D.E. Caldwell, D.R. Korber, J.R. Lawrence, Analysis of biofilm formation using 2D vs 3D digital imaging. J. Appl. Bacteriol. 74, 52S–66S (1993)

    Article  Google Scholar 

  81. S.R. Wood, J. Kirkham, P.D. Marsh, R.C. Shore, B. Nattress, et al., Architecture of intact natural human plaque Biofilms studied by Confocal laser scanning microscopy. J. Dent. Res. 79, 21–27 (2000)

    Article  Google Scholar 

  82. J. Kim, B. Pitts, P.S. Stewart, A. Camper, J. Yoon, Comparison of the antimicrobial effects of chlorine, silver ion, and Tobramycin on Biofilm. Antimicrob. Agents Chemother. 52, 1446–1453 (2008)

    Article  Google Scholar 

  83. C. Staudt, H. Horn, D.C. Hempel, T.R. Neu, Volumetric measurements of bacterial cells and extracellular polymeric substance glycoconjugates in biofilms. Biotechnol. Bioeng. 88, 585–592 (2004)

    Article  Google Scholar 

  84. T. Bjarnsholt, P.O. Jensen, M.J. Fiandaca, J. Pedersen, C.R. Hansen, C.B. Andersen, T. Pressler, M. Givskov, N. Hoiby, Pseudomonas aeruginosa biofilms in the respiratory tract of cystic fibrosis patients. Pediatr. Pulmonol. 44, 547–558 (2009)

    Article  Google Scholar 

  85. A. Touhami, M.H. Jericho, T.J. Beveridge, Atomic force microscopy of cell growth and division in Staphylococcus aureus. J. Bacteriol. 186, 3286–3295 (2004)

    Article  Google Scholar 

  86. H.H.P. Fang, K.-Y. Chan, L.-C. Xu, Quantification of bacterial adhesion forces using atomic force microscopy (AFM). J. Microbiol. Methods 40, 89–97 (2000)

    Article  Google Scholar 

  87. T.A. Camesano, M.J. Natan, B.E. Logan, Observation of changes in bacterial cell morphology using tapping mode atomic force microscopy. Langmuir 16, 4563–4572 (2000)

    Article  Google Scholar 

  88. C.J. Wright, M.K. Shah, L.C. Powell, I. Armstrong, Application of AFM from microbial cell to biofilm. Scanning 32, 134–149 (2010)

    Article  Google Scholar 

  89. Y.F. Dufrene, Atomic force microscopy, a powerful tool in microbiology. J. Bacteriol. 184, 5205–5213 (2002)

    Article  Google Scholar 

  90. D. Fotiadis, S. Scheuring, S.A. Müller, A. Engel, D.J. Müller, Imaging and manipulation of biological structures with the AFM. Micron 33, 385–397 (2002)

    Article  Google Scholar 

  91. M. Quirynen, C.M.L. Bollen, The influence of surface roughness and surface-free energy on supra- and subgingival plaque formation in man. J. Clin. Periodontol. 22, 1–14 (1995)

    Article  Google Scholar 

  92. H.J. Busscher, M. Rinastiti, W. Siswomihardjo, H.C. van der Mei, Biofilm formation on dental restorative and implant materials. J. Dent. Res. 89, 657–665 (2010)

    Article  Google Scholar 

  93. R. Burgers, W. Schneider-Brachert, M. Rosentritt, G. Handel, S. Hahnel, Candida albicans Adhesion to composite resin materials. Clin. Oral Investig. 13, 293–299 (2009)

    Article  Google Scholar 

  94. M. Quirynen, M. Marechal, D. Van Steenberghe, H.J. Busscher, H.C. Van Der Mei, The bacterial colonization of intra-oral hard surfaces in vivo: influence of surface free energy and surface roughness. Biofouling 4, 187–198 (1991)

    Article  Google Scholar 

  95. L. Mei, H.J. Busscher, H.C. van der Mei, Y. Ren, Influence of surface roughness on streptococcal adhesion forces to composite resins. Dent. Mater. 27, 770–778 (2011)

    Article  Google Scholar 

  96. E.S. Ovchinnikova, B.P. Krom, H.C. van der Mei, H.J. Busscher, Force microscopic and thermodynamic analysis of the adhesion between Pseudomonas Aeruginosa and Candida albicans. Soft Matter 8, 6454–6461 (2012)

    Article  Google Scholar 

  97. S.B. Velegol, S. Pardi, X. Li, D. Velegol, B.E. Logan, AFM imaging artifacts due to bacterial cell height and AFM tip geometry. Langmuir 19, 851–857 (2003)

    Article  Google Scholar 

  98. P. Chavant, B. Gaillard-Martinie, R. Talon, M. Hebraud, T. Bernardi, A new device for rapid evaluation of biofilm formation potential by bacteria. J. Microbiol. Methods 68, 605–612 (2007)

    Article  Google Scholar 

  99. Y. Wang, M. Libera, Length-Scale Effects on the Differential Adhesion of Bacteria and Mammalian Cells (ProQuest LLC, 2013)

    Google Scholar 

  100. T. Schwartz, C. Jungfer, S. Heissler, F. Friedrich, W. Faubel, et al., Combined use of molecular biology taxonomy, Raman spectrometry, and ESEM imaging to study natural biofilms grown on filter materials at waterworks. Chemosphere 77, 249–257 (2009)

    Article  Google Scholar 

  101. L. Bergmans, P. Moisiadis, B. Van Meerbeek, M. Quirynen, P. Lambrechts, Microscopic observation of bacteria: review highlighting the use of environmental SEM. Int. Endod. J. 38, 775–778 (2005)

    Article  Google Scholar 

  102. J.H. Priester, A.M. Horst, L.C. Van De Werfhorst, J.L. Saleta, L.A.K. Mertes, et al., Enhanced visualization of microbial Biofilms by staining and environmental scanning electron microscopy. J. Microbiol. Methods 68, 577–587 (2007)

    Article  Google Scholar 

  103. M. Ericsson, D. Hanstorp, P. Hagberg, J. Enger, T. Nystrom, Sorting out bacterial viability with optical tweezers. J. Bacteriol. 182, 5551–5555 (2000)

    Article  Google Scholar 

  104. A. Ashkin, J.M. Dziedzic, Optical trapping and manipulation of viruses and bacteria. Science 235(4795), 1517–1520 (1987)

    Article  Google Scholar 

  105. H. Zhang, K.K. Liu, Optical tweezers for single cells. J. R. Soc. Interface 5(24), 671–690 (2008)

    Article  Google Scholar 

  106. F.J.H. Hol, C. Dekker, Zooming in to see the bigger picture: microfluidic and nanofabrication tools to study bacteria Felix. Science 346(6208), 402–403 (2014)

    Article  Google Scholar 

  107. S. Lecuyer, R. Rusconi, Y. Shen, A. Forsyth, H. Vlamakis, R. Kolter, H.A. Stone, Shear stress increases the residence time of adhesion of Pseudomonas aeruginosa. Biophys. J. 100, 341–350 (2011)

    Article  Google Scholar 

  108. W.E. Thomas, E. Trintchina, M. Forero, V. Vogel, E.V. Sokurenko, Bacterial adhesion to target cells enhanced by shear force. Cell 109, 913–923 (2002)

    Article  Google Scholar 

  109. R. Rusconi, J.S. Guasto, R. Stocker, Bacterial transport suppressed by fluid shear. Nat. Phys. 10, 212–217 (2014)

    Article  Google Scholar 

  110. A. Park, H.H. Jeong, J. Lee, K.P. Kim, C.S. Lee, Effect of shear stress on the formation of bacterial biofilm in a microfluidic channel. Biochip J. 5(3), 236–241 (2011)

    Article  Google Scholar 

  111. N.P. Ivleva, M. Wagner, H. Horn, R. Niessner, C. Haisch, Towards a nondestructive chemical characterization of biofilm matrix by Raman microscopy. Anal. Bioanal. Chem. 393(1), 197–206 (2009)

    Article  Google Scholar 

  112. Y. Chao, T. Zhang, Surface-enhanced Raman scattering (SERS) revealing chemical variation during biofilm formation: from initial attachment to mature biofilm. Anal. Bioanal. Chem. 404(5), 1465–1475 (2012)

    Article  Google Scholar 

  113. P.A. Suci, G.G. Geesey, B.J. Tyler, Integration of Raman microscopy, differential interference contrast microscopy, and attenuated total reflection fourier transform infrared spectroscopy to investigate chlorhexidine spatial and temporal distribution in Candida albicans biofilms. J. Microbiol. Methods 46, 193–208 (2001)

    Article  Google Scholar 

  114. F. Humbert, F. Quiles, A. Delille, in Proceedings of the II International Conference on Environmental, Industrial and Applied Microbiology (BioMicroWorld2007) Current Research Topics in Applied Microbiology and Microbial Biotechnology, ed. by A Mendez-Vilas. In situ assessment of drinking water biostability using nascent reference biofilm ATR-FTIR fingerprint, (World Scientic Publishing Co. Pte. Ltd., Singapore, 2009), p. 268–272

    Google Scholar 

  115. K. Aslan, C.D. Geddes, Directional surface Plasmon coupled luminescence for analytical sensing applications: which metal, what wavelength, what observation angle? Anal. Chem. 81, 6913–6922 (2009)

    Article  Google Scholar 

  116. A.G. Koutsioubas, N. Spiliopoulos, D. Anastassopoulos, A.A. Vradis, G.D. Priftis, Nanoporous alumina enhanced surface plasmon resonance sensors. J. Appl. Phys. 103, 094521–094526 (2008)

    Article  Google Scholar 

  117. A.T.A. Jenkins, R. ffrench-constant, A. Buckling, D.J. Clarke, K. Jarvis, Study of the attachment of Pseudomonas Aeruginosa on gold and modified gold surfaces using surface Plasmon resonance. Biotechnol. Prog. 20, 1233–1236 (2004)

    Article  Google Scholar 

  118. J. Landrygan-Bakri, M.J. Wilson, D.W. Williams, M.A. Lewis, R.J. Waddington, Real-time monitoring of the adherence of Streptococcus anginosus group bacteria to extracellular matrix decorin and biglycan proteoglycans in biofilm formation. Res. Microbiol. 163, 436–447 (2012)

    Article  Google Scholar 

  119. A. Pranzetti, S. Salaün, S. Mieszkin, M.E. Callow, J.A. Callow, J.A. Preece, P.M. Mendes, Model organic surfaces to probe marine bacterial adhesion kinetics by surface Plasmon resonance. Adv. Funct. Mater. 22, 3672–3681 (2012)

    Article  Google Scholar 

  120. P. Janknecht, L. Melo, Online Biofilm monitoring. Rev. Environ. Sci. Biotechnol. 2, 269–283 (2003)

    Article  Google Scholar 

  121. P.N. Abadian, N. Tandogan, T.A. Webster, E.D. Goluch, Real-time detection of bacterial biofilm growth using surface plasmon resonance. 16th International Conference on Miniaturized Systems for Chemistry and Life Sciences (microTAS 2012), (Okinawa, JP, 2012), pp. 413–415

    Google Scholar 

  122. S. Paul, P. Vadgama, A.K. Ray, Surface plasmon resonance imaging for biosensing. Nanobiotechnol. IET 3, 71–80 (2009)

    Article  Google Scholar 

  123. Y. Yanase, T. Hiragun, S. Kaneko, H.J. Gould, M.W. Greaves, M. Hide, Detection of refractive index changes in individual living cells by means of surface plasmon resonance imaging. Biosens. Bioelectron. 26, 674–681 (2010)

    Article  Google Scholar 

  124. K. Marion-Ferey, M. Pasmore, P. Stoodley, S. Wilson, G.P. Husson, J.W. Costerton, Biofilm removal from silicone tubing: an assessment of the efficacy of dialysis machine decontamination procedures using an in vitro model. J. Hosp. Infect. 53, 64–71 (2003)

    Article  Google Scholar 

  125. J.D. Chambless, S.M. Hunt, P.S. Stewart, A three-dimensional computer model of four hypothetical mechanisms protecting Biofilms from antimicrobials. Appl. Environ. Microbiol. 72, 2005–2013 (2006)

    Article  Google Scholar 

  126. R.D. Harris, J.S. Wilkinson, Waveguide surface plasmon resonance sensors. Sensors Actuators B Chem. 29, 261–267 (1995)

    Article  Google Scholar 

  127. A. Karabchevsky, L. Tsapovsky, R.S. Marks, I. Abdulhalim, Optical immunosensor for endocrine disruptor nanolayer detection by surface plasmon resonance imaging. Proc. SPIE 8099, Biosensing and Nanomedicine IV: 809918 (2011)

    Google Scholar 

  128. P.N. Abadian, C.P. Kelley, E.D. Goluch, Cellular analysis and detection using surface Plasmon resonance techniques. Anal. Chem. 86, 2799–2812 (2014)

    Article  Google Scholar 

  129. P.N. Abadian, N. Tandogan, J.J. Jamieson, E.D. Goluch, Using surface plasmon resonance imaging to study bacterial biofilms. Biomicrofluidics 8, 021804 (2014)

    Article  Google Scholar 

  130. N.A. Saad, S.K. Zaaba, A. Zakaria, L.M. Kamarudin, K. Wan, A.B. Shariman, Quartz crystal microbalance for bacteria application review. 2nd International Conference on Electronic Design (ICED), (Penang, 2014), pp. 455–460

    Google Scholar 

  131. D.E. Nivens, J.Q. Chambers, T.R. Anderson, D.C. White, Long-term, on-line monitoring of microbial biofilms using a quartz crystal microbalance. Anal. Chem. 61(1), 65–69 (1993)

    Article  Google Scholar 

  132. P. Castro, P. Resa, C. Durán, J.R. Maestre, M. Mateo, L. Elvira, Continuous monitoring of bacterial biofilm growth using uncoated thickness-shear mode resonators. IOP Conf. Ser. Mater. Sci. Eng 42, 012054 (2012)

    Article  Google Scholar 

  133. V. Reipa, J. Almeida, K.D. Cole, Long-term monitoring of biofilm growth and disinfection using a quartz crystal microbalance and reflectance measurements. J. Microbiol. Methods 66, 449–459 (2006)

    Article  Google Scholar 

  134. A.L.J. Olsson, H.C. van der Mei, H.J. Busscher, P.K. Sharma, Influence of cell surface appendages on the bacterium substratum Interface measured real-time using QCM-D. Langmuir 25, 1627–1632 (2009)

    Article  Google Scholar 

  135. N. Vanoyan, S.L. Walker, O. Gillor, M. Herzberg, Reduced bacterial deposition and attachment by quorum sensing inhibitor 4-nitro-pyridine-N-oxide: the role of Physicochemical effects. Langmuir 26, 12089–12094 (2010)

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Edgar D. Goluch .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Tandogan, N., Abadian, P.N., Huo, B., Goluch, E.D. (2017). Characterization of Bacterial Adhesion and Biofilm Formation. In: Zhang, Z., Wagner, V. (eds) Antimicrobial Coatings and Modifications on Medical Devices. Springer, Cham. https://doi.org/10.1007/978-3-319-57494-3_3

Download citation

Publish with us

Policies and ethics