Efficient surface modification of biomaterial to prevent biofilm formation and the attachment of microorganisms


Biomaterials play a fundamental role in disease management and the improvement of health care. In recent years, there has been a significant growth in the diversity, function, and number of biomaterials used worldwide. Yet, attachment of pathogenic microorganisms onto biomaterial surfaces remains a significant challenge that substantially undermines their clinical applicability, limiting the advancement of these systems. The emergence and escalating pervasiveness of antibiotic-resistant bacterial strains makes the management of biomaterial-associated nosocomial infections increasingly difficult. The conventional post-operative treatment of implant-caused infections using systemic antibiotics is often marginally effective, further accelerating the extent of antimicrobial resistance. Methods by which the initial stages of bacterial attachment and biofilm formation can be restricted or prevented are therefore sought. The surface modification of biomaterials has the potential to alleviate pathogenic biofouling, therefore preventing the need for conventional antibiotics to be applied.

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

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 199

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2


  1. Agarwal A, Weis TL, Schurr MJ, Faith NG, Czuprynski CJ, McAnulty JF, Murphy CJ, Abbott NL (2010) Surfaces modified with nanometer-thick silver-impregnated polymeric films that kill bacteria but support growth of mammalian cells. Biomaterials 31:680–690

  2. Ahearn DG, May LL, Gabriel MM (1995) Adherence of organisms to silver-coated surfaces. J Ind Microbiol Biot 15:372–376

  3. An YH, Friedman RJ, Draughn RA, Smith EA, Nicholson JH, John JF (1995) Rapid quantification of staphylococci adhered to titanium surfaces using image analyzed epifluorescence microscopy. J Microbiol Methods 24:29–40

  4. Andersson DI, Hughes D (2011) Persistence of antibiotic resistance in bacterial populations. FEMS Microbiol Rev 35:901–911

  5. Andrews SS (2009) Accurate particle-based simulation of adsorption, desorption and partial transmission. Phys Biol 6:046015

  6. Ansari SA, Husain Q (2012) Potential applications of enzymes immobilized on/in nano materials: a review. Biotechnol Adv 30:512–523

  7. Anselme K, Davidson P, Popa AM, Giazzon M, Liley M, Ploux L (2010) The interaction of cells and bacteria with surfaces structured at the nanometre scale. Acta Biomater 6:3824–3846

  8. Ardehali R, Shi L, Janatova J, Mohammad SF, Burns Gregory L (2002) The effect of apo-transferrin on bacterial adhesion to biomaterials. Artif Organs 26:512–520

  9. Baum C, Meyer W, Stelzer R, Fleischer LG, Siebers D (2002) Average nanorough skin surface of the pilot whale (Globicephala melas, Delphinidae): considerations on the self-cleaning abilities based on nanoroughness. Mar Biol 140:653–657

  10. Bazaka K, Jacob MV, Truong VK, Wang F, Pushpamali WA, Wang J, Ellis A, Berndt CC, Crawford RJ, Ivanova EP (2010) Effect of plasma-enhanced chemical vapour deposition on the retention of antibacterial activity of terpinen-4-ol. Biomacromolecules 11:2016–2026

  11. Bazaka K, Crawford RJ, Ivanova EP (2011a) Do bacteria differentiate between degrees of nanoscale surface roughness? Biotechnol J 6:1103–1114

  12. Bazaka K, Crawford RJ, Nazarenko EL, Ivanova EP (2011b) Bacterial extracellular polysaccharides. In: Linke D, Goldman A (eds) Bacterial adhesion, vol. 715. Advances in experimental medicine and biology. Springer, Netherlands, pp 213–226

  13. Bazaka K, Jacob M, Truong VK, Crawford RJ, Ivanova EP (2011c) The effect of polyterpenol thin film surfaces on bacterial viability and adhesion. Polymers 3:388–404

  14. Bazaka K, Jacob MV, Crawford RJ, Ivanova EP (2011d) Plasma assisted surface modification of organic biopolymers. Acta Biomater 7:2015–2028

  15. Bendrea A-D, Cianga L, Cianga I (2011) Review paper: progress in the field of conducting polymers for tissue engineering applications. J Biomater Appl 26:3–84

  16. Bhushan B, Koch K, Jung YC (2008) Nanostructures for superhydrophobicity and low adhesion. Soft Matter 4:1799–1804

  17. Birla SS, Tiwari VV, Gade AK, Ingle AP, Yadav AP, Rai MK (2009) Fabrication of silver nanoparticles by Phoma glomerata and its combined effect against Escherichia coli, Pseudomonas aeruginosa and Staphylococcus aureus. Lett Appl Microbiol 48:173–179

  18. Bjellanda AM, Søruma H, Tegegneb DA, Winther-Larsena HC, Willassenb NP, Hansen H (2012) LitR of Vibrio salmonicida is a salinity-sensitive quorum-sensing regulator of phenotypes involved in host interactions and virulence. Infect Immun 80:1681–1689

  19. Bordi C, de Bentzmann S (2011) Hacking into bacterial biofilms: a new therapeutic challenge. Ann Intens Care 1:19

  20. 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 23:179–229

  21. Boulangé-Petermann L, Rault J, Bellon-Fontaine MN (1997) Adhesion of Streptococcus thermophilus to stainless steel with different surface topography and roughness. Biofouling 11:201–216

  22. Brunetti V, Maiorano G, Rizzello L, Sorce B, Sabella S, Cingolani R, Pompa PP (2010) Neurons sense nanoscale roughness with nanometer sensitivity. Proc Natl Acad Sci U S A 107:6264–6269

  23. Busscher HJ, Norde W, Sharma PK, van der Mei HC (2010) Interfacial re-arrangement in initial microbial adhesion to surfaces. Curr Opin Colloid Interface Sci 15:510–517

  24. Cappella B, Dietler G (1999) Force–distance curves by atomic force microscopy. Surf Sci Rep 34:5–104

  25. Cardoso MV, de Almeida NA, Mine A, Coutinho E, Van Landuyt K, De Munck J, Van Meerbeek B (2011) Current aspects on bonding effectiveness and stability in adhesive dentistry. Aust Dent J 56:31–44

  26. Chen W, Liu Y, Courtney HS, Bettenga M, Agrawal CM, Bumgardner JD, Ong JL (2006) In vitro anti-bacterial and biological properties of magnetron co-sputtered silver-containing hydroxyapatite coating. Biomaterials 27:5512–5517

  27. Cho M, Chung H, Choi W, Yoon J (2005) Different inactivation behaviours of MS-2 phage and Escherichia coli in TiO2 photocatalytic disinfection. Appl Environ Microbiol 71:270–275

  28. Chung KK, Schumacher JF, Sampson EM, Burne RA, Antonelli PJ, Brennan AB (2007) Impact of engineered surface microtopography on biofilm formation of Staphylococcus aureus. Biointerphases 2:89–94

  29. Colon G, Ward BC, Webster TJ (2006) Increased osteoblast and decreased Staphylococcus epidermidis functions on nanophase ZnO and TiO2. J Biomed Mater Res, Part A 78:595–604

  30. Colvin KM, Gordon VD, Murakami K, Borlee BR, Wozniak DJ, Wong GC, Parsek MR (2011) Thepel polysaccharide can serve a structural and protective role in the biofilm matrix of Pseudomonas aeruginosa. PLoS Pathog 7:e1001264

  31. Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322

  32. Davies DG, Geesey GG (1995) Regulation of the alginate biosynthesis gene algC in Pseudomonas aeruginosa during biofilm development in continuous culture. Appl Environ Microbiol 61:860–867

  33. Decho AW (2000) Microbial biofilms in intertidal systems: an overview. Cont Shelf Res 20:1257–1273

  34. Desmet T, Morent R, Geyter ND, Leys C, Schacht E, Dubruel P (2009) Nonthermal plasma technology as a versatile strategy for polymeric biomaterials surface modification: a review. Biomacromolecules 10:2351–2378

  35. Diaz C, Cortizo MC, Schilardi PL, de Saravia SGG, de Mele MAFL (2007) Influence of the nano-micro structure of the surface on bacterial adhesion. Mater Res 10:11–14

  36. Díaz C, Schilardi PL, Salvarezza RC, Lorenzo F, de Mele M (2007) Nano/microscale order affects the early stages of biofilm formation on metal surfaces. Langmuir 23:11206–11210

  37. Dibrov P, Dzioba J, Gosink KK, Häse CC (2002) Chemiosmotic mechanism of antimicrobial activity of Ag(+) in Vibrio cholerae. Antimicrob Agents Chemother 46:2668–2670

  38. Ditta IB, Steele A, Liptrot C, Tobin J, Tyler H, Yates HM, Sheel DW, Foster HA (2008) Photocatalytic antimicrobial activity of thin surface films of TiO2, CuO and TiO2/CuO dual layers on Escherichia coli and bacteriophage T4. Appl Microbiol Biotechnol 79:127–133

  39. Dobrzyński M, Bernatowicz P, Kloc M, Kubiak J (2011) Evolution of bet-hedging mechanisms in cell cycle and embryo development stimulated by weak linkage of stochastic processes. In: Kubiak JZ (ed) Cell cycle in development, vol 53. Results and problems in cell differentiation. Springer, Berlin, pp 11–30

  40. Dodiuk H, Rios PF, Dotan A, Kenig S (2007) Hydrophobic and self-cleaning coatings. Polym Adv Technol 18:746–750

  41. Donald LE (2011) Liquid–liquid two-phase systems for the production of porous hydrogels and hydrogel microspheres for biomedical applications: a tutorial review. Acta Biomater 7:31–56

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

  43. Döring G, Parameswaran IG, Murphy TF (2011) Differential adaptation of microbial pathogens to airways of patients with cystic fibrosis and chronic obstructive pulmonary disease. FEMS Microbiol Rev 35:124–146

  44. Dorobantu LS, Bhattacharjee S, Foght JM, Gray MR (2009) Analysis of force interactions between AFM tips and hydrophobic bacteria using DLVO theory. Langmuir 25:6968–6976

  45. Dorozhkin SV (2011) Biocomposites and hybrid biomaterials based on calcium orthophosphates. Biomatter 1:3–56

  46. Dowling DP, Donnelly K, McConnell ML, Eloy R, Arnaud MN (2001) Deposition of anti-bacterial silver coatings on polymeric substrates. Thin Solid Films 398–399:602–606

  47. Edwards KJ, Rutenberg AD (2001) Microbial response to surface microtopography: the role of metabolism in localized mineral dissolution. Chem Geol 180:19–32

  48. Estrin Y, Kasper C, Diederichs S, Lapovok R (2009) Accelerated growth of preosteoblastic cells on ultrafine grained titanium. J Biomed Mater Res, Part A 90A:1239–1242

  49. Ewald A, Gluckermann S, Thull R, Gbureck U (2006) Antimicrobial titanium/silver PVD coatings on titanium. Biomed Engineer Online 5:22

  50. Fadeeva E, Schlie S, Koch J, Ngezahayo A, Chichkov BN (2009) The hydrophobic properties of femtosecond laser fabricated spike structures and their effects on cell proliferation. Phys Status Solidi A 206:1348–1351

  51. Fadeeva E, Truong VK, Stiesch M, Chichkov BN, Crawford RJ, Wang J, Ivanova EP (2011) Bacterial retention on superhydrophobic titanium surfaces fabricated by femtosecond laser ablation. Langmuir 27:3012–3019

  52. Favia P, Vulpio M, Marino R, d'Agostino R, Mota RP, Catalano M (2000) Plasma-deposition of Ag-containing polyethyleneoxide-like coatings. Plasmas Polym 5:1–14

  53. Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633

  54. Flemming HC, Neu TR, Wozniak DJ (2007) The EPS matrix: The “House of biofilm cells”. J Bacteriol 189:7945–7947

  55. Freire-Moran L, Aronsson B, Manz C, Gyssens IC, So AD, Monnet DL, Cars O (2011) Critical shortage of new antibiotics in development against multidrug-resistant bacteria—time to react is now. Drug Resist Updates 14:118–124

  56. Fu J, Ji J, Yuan W, Shen J (2005) Construction of anti-adhesive and antibacterial multilayer films via layer-by-layer assembly of heparin and chitosan. Biomaterials 26:6684–6692

  57. Fu R-H, Wang Y-C, Liu S-P, Huang C-M, Kang Y-H, Tsai C-H, Shyu W-C, Lin S-Z (2011) Differentiation of stem cells: strategies for modifying surface biomaterials. Cell Transplant 20:37–47

  58. Gabriel GJ, Som A, Madkour AE, Eren T, Tew GN (2007) Infectious disease: connecting innate immunity to biocidal polymers. Mater Sci Eng, R 57:28–64

  59. Gioe T, Sharma A, Tatman P, Mehle S (2011) Do “premium” joint implants add value?: Analysis of high cost joint implants in a community registry. Clin Orthop Relat Res 469:48–54

  60. Gogniat G, Thyssen M, Denis M, Pulgarin C, Dukan S (2006) The bactericidal effect of TiO2 photocatalysis involves adsorption onto catalyst and the loss of membrane integrity. FEMS Microbiol Lett 258:18–24

  61. Gottenbos B, Grijpma DW, van der Mei HC, Feijen J, Busscher HJ (2001) Antimicrobial effects of positively charged surfaces on adhering Gram-positive and Gram-negative bacteria. J Antimicrob Chemother 48:7–13

  62. Hanssen AD (2002) Managing the infected knee: as good as it gets. J Arthroplasty 17:98–101

  63. Harris LG, Tosatti S, Wieland M, Textor M, Richards RG (2004) Staphylococcus aureus adhesion to titanium oxide surfaces coated with non-functionalized and peptide-functionalized poly(-lysine)-grafted-poly(ethylene glycol) copolymers. Biomaterials 25:4135–4148

  64. Hashimoto K, Irie H, Fujishima A (2005) TiO2 photocatalysis: a historical overview and future prospects. Jpn J Appl Phys 44:8269–8285

  65. Hochbaum AI, Aizenberg J (2010) Bacteria pattern spontaneously on periodic nanostructure arrays. Nano Lett 10:3717–3721

  66. Holt KB, Bard AJ (2005) Interaction of silver(I) ions with the respiratory chain of Escherichia coli: an electrochemical and scanning electrochemical microscopy study of the antimicrobial mechanism of micromolar Ag+. Biochemistry 44:13214–13223

  67. Hoppe A, Güldal NS, Boccaccini AR (2011) A review of the biological response to ionic dissolution products from bioactive glasses and glass-ceramics. Biomaterials 32:2757–2774

  68. Hu C, Guo J, Qu J, Hu X (2007) Efficient destruction of bacteria with Ti(IV) and antibacterial ions in co-substituted hydroxyapatite films. Appl Catal B Environ 73:345–353

  69. Hynek B (2011) Nanocomposites and nanostructures based on plasma polymers. Surf Coat Technol 205(Supplement 2):S10–S14

  70. Ivanova EP, Mitik-Dineva N, Wang J, Pham DK, Wright JP, Nicolau DV, Mocanasu RC, Crawford RJ (2008) Staleya guttiformis attachment on poly(tert-butylmethacrylate) polymeric surfaces. Micron 39:1197–1204

  71. Ivanova EP, Truong VK, Wang JY, Berndt CC, Jones RT, Yusuf II, Peake I, Schmidt HW, Fluke C, Barnes D, Crawford RJ (2010) Impact of nanoscale roughness of titanium thin film surfaces on bacterial retention. Langmuir 26:1973–1982

  72. Ivanova E, Hasan J, Truong V, Wang J, Raveggi M, Fluke C, Crawford R (2011) The influence of nanoscopically thin silver films on bacterial viability and attachment. Appl Microbiol Biotechnol 91:1149–1157

  73. Jiao Y, Cody GD, Harding AK, Wilmes P, Schrenk M, Wheeler KE, Banfield JF, Thelen MP (2010) Characterization of extracellular polymeric substances from acidophilic microbial biofilms. Appl Environ Microbiol 76:2916–2922

  74. Karatan E, Watnick P (2009) Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol Mol Biol Rev 73:310–347

  75. Katsikogianni M, Missirlis YF (2004) Concise review of mechanisms of bacterial adhesion to biomaterials and of techniques used in estimating bacteria–material interactions. Eur Cells Mater 8:37–57

  76. Kelly PJ, Li H, Whitehead KA, Verran J, Arnell RD, Iordanova I (2009) A study of the antimicrobial and tribological properties of TiN/Ag nanocomposite coatings. Surf Coat Technol 204:1137–1140

  77. Khan OF, Sefton MV (2011) Endothelialized biomaterials for tissue engineering applications in vivo. Trends Biotechnol 29:379–387

  78. Kitao T, Ando Y, Yoshikawa M, Kobayashi M, Kimura T, Ohsawa H, Machida S, Yokoyama N, Sakota D, Konno T, Ishihara K, Takatani S (2011) In vivo evaluation of the “tinypump” as a pediatric left ventricular assist device. Artif Organs 35:543–553

  79. Körner E, Aguirre MH, Fortunato G, Ritter A, Rühe J, Hegemann D (2010) Formation and distribution of silver nanoparticles in a functional plasma polymer matrix and related Ag+ release properties. Plasma Process Polymer 7:619–625

  80. Körner E, Rupper P, Lübben JF, Ritter A, Rühe J, Hegemann D (2011) Surface topography, morphology and functionality of silver containing plasma polymer nanocomposites. Surf Coat Technol 205:2978–2984

  81. Kumar R, Münstedt H (2005) Silver ion release from antimicrobial polyamide/silver composites. Biomaterials 26:2081–2088

  82. Laue H, Schenk A, Li H, Lambertsen L, Neu TR, Molin S, Ullrich MS (2006) Contribution of alginate and levan production to biofilm formation by Pseudomonas syringae. Microbiology 152:2909–2918

  83. Lee B, Schjerling CK, Kirkby N, Hoffmann N, Borup R, Molin S, HØIby N, Ciofu O (2011) Mucoid Pseudomonas aeruginosa isolates maintain the biofilm formation capacity and the gene expression profiles during the chronic lung infection of CF patients. APMIS 119:263–274

  84. Lele UN, Baig UI, Watve MG (2011) Phenotypic plasticity and effects of selection on cell division symmetry in Escherichia coli. PLoS One 6:e14516

  85. Lewis G (2011) Viscoelastic properties of injectable bone cements for orthopaedic applications: state-of-the-art review. J Biomed Mater Res, Part B 98B:171–191

  86. Li W-R, Xie X-B, Shi Q-S, Duan S-S, Ouyang Y-S, Chen Y-B (2011) Antibacterial effect of silver nanoparticles on Staphylococcus aureus. BioMetals 24:135–141

  87. Liu X, Chu PK, Ding C (2004) Surface modification of titanium, titanium alloys, and related materials for biomedical applications. Mater Sci Eng, R 47:49–121

  88. Liu Y, Wang J-C, Ren L, Tu Q, Liu W-M, Wang X-Q, Liu R, Zhang Y-R, Wang J-Y (2011) Microfluidics-based assay on the effects of microenvironmental geometry and aqueous flow on bacterial adhesion behaviors. J Pharm Anal 1:175–183

  89. Livermore DM (2005) Minimising antibiotic resistance. Lancet Infect Dis 5:450–459

  90. Lok CN, Ho CM, Chen R, He QY, Yu WY, Sun H, Tam PKH, Chiu JF, Che CM (2007) Silver nanoparticles: partial oxidation and antibacterial activities. J Biol Inorg Chem 12:527–534

  91. Low WL, Martin C, Hill DJ, Kenward MA (2011) Antimicrobial efficacy of silver ions in combination with tea tree oil against Pseudomonas aeruginosa, Staphylococcus aureus and Candida albicans. Int J Antimicrob Agents 37:162–165

  92. Ma L, Jackson KD, Landry RM, Parsek MR, Wozniak DJ (2006) Analysis of Pseudomonas aeruginosa conditional Psl variants reveals roles for the Psl polysaccharide in adhesion and maintaining biofilm structure postattachment. J Bacteriol 188:8213–8221

  93. Madkour AE, Tew GN (2008) Towards self-sterilizing medical devices: controlling infection. Polym Int 57:6–10

  94. Malkin AJ, Plomp M (2011) High-resolution architecture and structural dynamics of microbial and cellular systems: insights from in vitro Atomic Force Microscopy. In: Kalinin SV, Gruverman A (eds) Scanning probe microscopy of functional materials. Springer, New York, pp 39–68

  95. Marambio-Jones C, Hoek E (2010) A review of the antibacterial effects of silver nanomaterials and potential implications for human health and the environment. J Nanopart Res 12:1531–1551

  96. Marini M, De Niederhausern S, Iseppi R, Bondi M, Sabia C, Toselli M, Pilati F (2007) Antibacterial activity of plastics coated with silver-doped organic–inorganic hybrid coatings prepared by sol–gel processes. Biomacromolecules 8:1246–1254

  97. Medilanski E, Kaufmann K, Wick LY, Wanner O, Harms H (2002) Influence of the surface topography of stainless steel on bacterial adhesion. Biofouling 18:193–203

  98. Mitik-Dineva N, Wang J, Mocanasu RC, Stoddart PR, Crawford RJ, Ivanova EP (2008) Impact of nano-topography on bacterial attachment. Biotechnol J 3:536–544

  99. Mitik-Dineva N, Wang J, Truong VK, Stoddart P, Malherbe F, Crawford RJ, Ivanova EP (2009) Escherichia coli, Pseudomonas aeruginosa and Staphylococcus aureus attachment patterns on glass surfaces with nanoscale roughness. Curr Microbiol 58:268–273

  100. Mitik-Dineva N, Wang J, Truong VK, Stoddart PR, Alexander MR, Albutt DJ, Fluke C, Crawford RJ, Ivanova EP (2010) Bacterial attachment on optical fibre surfaces. Biofouling 26:461–470

  101. Montanaro L, Campoccia D, Arciola CR (2007) Advancements in molecular epidemiology of implant infections and future perspectives. Biomaterials 28:5155–5168

  102. Morent R, De Geyter N, Desmet T, Dubruel P, Leys C (2011) Plasma surface modification of biodegradable polymers: a review. Plasma Process Polymer 8:171–190

  103. Nablo BJ, Chen T-Y, Schoenfisch MH (2001) Sol–gel derived nitric-oxide releasing materials that reduce bacterial adhesion. J Am Chem Soc 123:9712–9713

  104. Naderi H, Matin MM, Bahrami AR (2011) Review paper: critical issues in tissue engineering: biomaterials, cell sources, angiogenesis, and drug delivery systems. J Biomater Appl 26:383–417

  105. Norowski PA, Bumgardner JD (2009) Biomaterial and antibiotic strategies for peri-implantitis: a review. J Biomed Mater Res, Part B 88B:530–543

  106. Parreira P, Magalhães A, Gonçalves IC, Gomes J, Vidal R, Reis CA, Leckband DE, Martins MCL (2011) Effect of surface chemistry on bacterial adhesion, viability, and morphology. J Biomed Mater Res, Part A 99A:344–353

  107. Pavithra D, Mukesh D (2008) Biofilm formation, bacterial adhesion and host response on polymeric implants' issues and prevention. Biomed Mater 3:034003

  108. Petrova OE, Sauer K (2011) SagS contributes to the motile-sessile switch and acts in concert with BfiSR to enable Pseudomonas aeruginosa biofilm formation. J Bacteriol 193:6614–6628

  109. Petrova OE, Sauer K (2012) Sticky situations: key components that control bacterial surface attachment. J Bacteriol 194:2413–2425

  110. Ploux L, Anselme K, Dirani A, Ponche A, Soppera O, Roucoules V (2009) Opposite responses of cells and bacteria to micro/nanopatterned surfaces prepared by pulsed plasma polymerization and UV-irradiation. Langmuir 25:8161–8169

  111. Ploux L, Ponche A, Anselme K (2010) Bacteria/material interfaces: role of the material and cell wall properties. J Adhes Sci Technol 24:2165–2201

  112. Poulter N, Munoz-Berbel X, Johnson AL, Dowling AJ, Waterfield N, Jenkins ATA (2009) An organo-silver compound that shows antimicrobial activity against Pseudomonas aeruginosa as a monomer and plasma deposited film. Chem Commun 7312–7314

  113. Price JS, Tencer AF, Arm DM, Bohach GA (1996) Controlled release of antibiotics from coated orthopedic implants. J Biomed Mater Res 30:281–286

  114. Rai M, Yadav A, Gade A (2009) Silver nanoparticles as a new generation of antimicrobials. Biotechnol Adv 27:76–83

  115. Raynor JE, Capadona JR, Collard DM, Petrie TA, Garcia AJ (2009) Polymer brushes and self-assembled monolayers: versatile platforms to control cell adhesion to biomaterials (Review). Biointerphases 4:FA3–FA16

  116. Rios PF, Dodiuk H, Kenig S, McCarthy S, Dotan A (2006) The effects of nanostructure and composition on the hydrophobic properties of solid surfaces. J Adhes Sci Technol 20:563–587

  117. Rios PF, Dodiuk H, Kenig S, McCarthy S, Dotan A (2007) Transparent ultra-hydrophobic surfaces. J Adhes Sci Technol 21:399–408

  118. Rojas IA, Slunt JB, Grainger DW (2000) Polyurethane coatings release bioactive antibodies to reduce bacterial adhesion. J Contr Release 63:175–189

  119. Rowan B, Wheeler MA, Crooks RM (2002) Patterning bacteria within hyperbranched polymer film templates. Langmuir 18:9914–9917

  120. Rozhok S, Fan Z, Nyamjav D, Liu C, Mirkin CA, Holz RC (2006) Attachment of motile bacterial cells to prealigned holed microarrays. Langmuir 22:11251–11254

  121. Saito N, Aoki K, Usui Y, Shimizu M, Hara K, Narita N, Ogihara N, Nakamura K, Ishigaki N, Kato H, Haniu H, Taruta S, Ahm Kim Y, Endo M (2011) Application of carbon fibers to biomaterials: a new era of nano-level control of carbon fibers after 30-years of development. Chem Soc Rev 40:3824–3834

  122. Saldarriaga Fernández IC, Busscher HJ, Metzger SW, Grainger DW, van der Mei HC (2011) Competitive time- and density-dependent adhesion of staphylococci and osteoblasts on crosslinked poly(ethylene glycol)-based polymer coatings in co-culture flow chambers. Biomaterials 32:979–984

  123. Sardella E, Favia P, Gristina R, Nardulli M, d'Agostino R (2006) Plasma-aided micro- and nanopatterning processes for biomedical applications. Plasma Process Polymer 3:456–469

  124. Scheuerman TR, Camper AK, Hamilton MA (1998) Effects of substratum topography on bacterial adhesion. J Colloid Interface Sci 208:23–33

  125. Shadanbaz S, Dias GJ (2012) Calcium phosphate coatings on magnesium alloys for biomedical applications: a review. Acta Biomater 8:20–30

  126. Shanks RMQ, Donegan NP, Graber ML, Buckingham SE, Zegans ME, Cheung AL, O'Toole GA (2005) Heparin stimulates Staphylococcus aureus biofilm formation. Infect Immun 73:4596–4606

  127. Shao W, Zhao Q (2010a) Effect of corrosion rate and surface energy of silver coatings on bacterial adhesion. Colloids Surf, B 76:98–103

  128. Shao W, Zhao Q (2010b) Influence of reducers on nanostructure and surface energy of silver coatings and bacterial adhesion. Surf Coat Technol 204:1288–1294

  129. Shenga GP, Yua HQ, Lib XY (2010) Extracellular polymeric substances (EPS) of microbial aggregates in biological wastewater treatment systems: a review. Biotechnol Adv 28:882–894

  130. Shukla A, Fleming KE, Chuang HF, Chau TM, Loose CR, Stephanopoulos GN, Hammond PT (2010) Controlling the release of peptide antimicrobial agents from surfaces. Biomaterials 31:2348–2357

  131. Silver S (2003) Bacterial silver resistance: molecular biology and uses and misuses of silver compounds. FEMS Microbiol Rev 27:341–353

  132. Solouk A, Cousins BG, Mirzadeh H, Seifalian AM (2011) Application of plasma surface modification techniques to improve hemocompatibility of vascular grafts: a review. Biotechnol Appl Biochem 58:311–327

  133. Stigter M, Bezemer J, de Groot K, Layrolle P (2004) Incorporation of different antibiotics into carbonated hydroxyapatite coatings on titanium implants, release and antibiotic efficacy. J Controlled Rel 99:127–137

  134. Stobie N, Duffy B, McCormack DE, Colreavy J, Hidalgo M, McHale P, Hinder SJ (2008) Prevention of Staphylococcus epidermidis biofilm formation using a low-temperature processed silver-doped phenyltriethoxysilane sol–gel coating. Biomaterials 29:963–969

  135. Subbiahdoss G, Kuijer R, Grijpma DW, van der Mei HC, Busscher HJ (2009) Microbial biofilm growth vs. tissue integration: "The race for the surface" experimentally studied. Acta Biomater 5:1399–1404

  136. Sun H, Meng F, Dias AA, Hendriks M, Feijen J, Zhong Z (2011) α-Amino acid containing degradable polymers as functional biomaterials: rational design, synthetic pathway, and biomedical applications. Biomacromolecules 12:1937–1955

  137. Tan A, Yildirimer L, Rajadas J, De La Peña H, Pastorin G, Seifalian A (2011) Quantum dots and carbon nanotubes in oncology: a review on emerging theranostic applications in nanomedicine. Nanomedicine 6:1101–1114

  138. Tarquinio KM, Kothurkar NK, Goswami DY, Sanders RC Jr, Zaritsky AL (2010) Levine AM (2010) Bactericidal effects of silver plus titanium dioxide-coated endotracheal tubes on Pseudomonas aeruginosa and Staphylococcus aureus. Int J Nanomed 5:177–183

  139. Truong VK, Rundell S, Lapovok R, Estrin Y, Wang JY, Berndt CC, Barnes DG, Fluke CJ, Crawford RJ, Ivanova EP (2009) Effect of ultrafine-grained titanium surfaces on adhesion of bacteria. Appl Microbiol Biotechnol 83:925–937

  140. Truong VK, Lapovok R, Estrin YS, Rundell S, Wang JY, Fluke CJ, Crawford RJ, Ivanova EP (2010a) The influence of nano-scale surface roughness on bacterial adhesion to ultrafine-grained titanium. Biomaterials 31:3674–3683

  141. Truong VK, Wang J, Lapovok R, Estrin Y, Malherbe F, Berndt C, Crawford R, Ivanova E (2010b) Bacterial attachment response on titanium surfaces with nanometric topographic features. In: Bucak S (ed) Trends in colloid and interface science XXIII, vol 137. Progress in colloid and polymer science. Springer, Berlin, pp 41–45

  142. Truong VK, Wang JY, Shurui W, Malherbe F, Berndt CC, Crawford RJ, Ivanova EP (2010c) Bacterial attachment response to nanostructured titanium surfaces. International Conference on Nanoscience and Nanotechnology, pp 253–256

  143. Valiev RZ, Semenova IP, Latysh VV, Rack H, Lowe TC, Petruzelka J, Dluhos L, Hrusak D, Sochova J (2008) Nanostructured titanium for biomedical applications. Adv Eng Mater 10:B15–B17

  144. Van Vlierberghe S, Dubruel P, Schacht E (2011) Biopolymer-based hydrogels as scaffolds for tissue engineering applications: a review. Biomacromolecules 12:1387–1408

  145. Vasilev K, Sah V, Anselme K, Ndi C, Mateescu M, Br D, Martinek P, Ys H, Ploux L, Griesser HJ (2009) Tunable antibacterial coatings that support mammalian cell growth. Nano Lett 10:202–207

  146. Vasilev K, Sah VR, Goreham RV, Ndi C, Short RD, Griesser HJ (2010) Antibacterial surfaces by adsorptive binding of polyvinyl-sulphonate-stabilized silver nanoparticles. Nanotechnology 21:215102

  147. Vasilev K, Griesser SS, Griesser HJ (2011) Antibacterial surfaces and coatings produced by plasma techniques. Plasma Process Polymer 8:1010–1023

  148. Vilain S, Pretorius JM, Theron J, Brözel VS (2009) DNA as an adhesin: Bacillus cereus requires extracellular DNA to form biofilms. Appl Environ Microbiol 75:2861–2868

  149. Wagoner Johnson AJ, Herschler BA (2011) A review of the mechanical behavior of CaP and CaP/polymer composites for applications in bone replacement and repair. Acta Biomater 7:16–30

  150. Webb HK, Hasan J, Truong VK, Crawford RJ, Ivanova EP (2011) Nature inspired structured surfaces for biomedical applications. Curr Med Chem 18:3367–3375

  151. Wenzel RN (1949) Surface roughness and contact angle. J Phys Colloid Chem 53:1466–1467

  152. Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS (2002) Extracellular DNA required for bacterial biofilm formation. Science 295:1487

  153. Whitehead KA, Colligon J, Verran J (2005) Retention of microbial cells in substratum surface features of micrometer and sub-micrometer dimensions. Colloids Surf B 41:129–138

  154. Whitehead KA, Rogers D, Colligon J, Wright C, Verran J (2006) Use of the atomic force microscope to determine the effect of substratum surface topography on the ease of bacterial removal. Colloids Surf B 51:44–53

  155. Whitehead K, Kelly P, Li H, Verran J (2010) Surface topography and physicochemistry of silver containing titanium nitride nanocomposite coatings. J Vac Sci Technol B Microelectron Nanometer Struct Process Meas Phenom 28:180–187

  156. Wu S, Liu X, Yeung A, Yeung KWK, Kao RYT, Wu G, Hu T, Xu Z, Chu PK (2011a) Plasma-modified biomaterials for self-antimicrobial applications. ACS Appl Mater Interfaces 3:2851–2860

  157. Wu Y, Zitelli JP, TenHuisen KS, Yu X, Libera MR (2011b) Differential response of Staphylococci and osteoblasts to varying titanium surface roughness. Biomaterials 32:951–960

  158. Yang L, Barken KB, Skindersoe ME, Christensen AB, Givskov M, Tolker-Nielsen T (2007) Effects of iron on DNA release and biofilm development by Pseudomonas aeruginosa. Microbiology 153:1318–1328

  159. Yates HM, Brook LA, Ditta IB, Evans P, Foster HA, Sheel DW, Steele A (2008) Photo-induced self-cleaning and biocidal behaviour of titania and copper oxide multilayers. J Photochem Photobiol A Chem 197:197–205

  160. Zaporojtchenko V, Podschun R, Schürmann U, Kulkarni A, Faupel F (2006) Physico-chemical and antimicrobial properties of co-sputtered Ag–Au/PTFE nanocomposite coatings. Nanotechnology 17:4904

  161. Zhao H, Yang Y, Yu G, Zhou J (2011) A systematic review of outcome and failure rate of uncemented Scandinavian total ankle replacement. Int Orthop 35:1751–1758

  162. Zilberman M, Elsner JJ (2008) Antibiotic-eluting medical devices for various applications. J Contr Release 130:202–215

Download references


This study was supported in part by Australian Research Council (ARC) and Advanced Manufacturing CRC.K. B. is a recipient of an Australian Postgraduate Award (APA) and an Australian Institute of Nuclear Science and Engineering Postgraduate Research Award (AINSE PGRA).

Author information

Correspondence to Russell J. Crawford or Elena P. Ivanova.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Bazaka, K., Jacob, M.V., Crawford, R.J. et al. Efficient surface modification of biomaterial to prevent biofilm formation and the attachment of microorganisms. Appl Microbiol Biotechnol 95, 299–311 (2012).

Download citation


  • Biomaterials
  • Surface treatment
  • Biofilm
  • Bacterial attachment