Skip to main content

Advertisement

SpringerLink
Log in

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

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

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 via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • 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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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

    Google Scholar 

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

    CAS  Google Scholar 

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

    Google Scholar 

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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

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

    CAS  Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

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

    Google Scholar 

  • 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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

  • 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

    CAS  Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

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

    CAS  Google Scholar 

Download references

Acknowledgements

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

Authors and Affiliations

  1. Electronic Materials Research Lab, School of Engineering, James Cook University, Townsville, Queensland, 4811, Australia

    Kateryna Bazaka

  2. Faculty of Life and Social Sciences, Swinburne University of Technology, PO Box 218, Hawthorn, Victoria, 3122, Australia

    Mohan V. Jacob, Russell J. Crawford & Elena P. Ivanova

Authors
  1. Kateryna Bazaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mohan V. Jacob
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Russell J. Crawford
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elena P. Ivanova
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

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). https://doi.org/10.1007/s00253-012-4144-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-012-4144-7

Keywords

Search

Navigation