Balancing osteoblast functions and bacterial adhesion on functionalized titanium surfaces

Biomaterials

Volumn 33, Issue 10, 2012, Pages 2813-2822

  Neoh, Koon Gee ^a   Hu, Xuefeng ^a   Zheng, Dong ^a   Kang, En Tang ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Bacterial adhesion; Infection; Osteoblast; Surface modification; Titanium implant

Indexed keywords

BACTERIAL ADHESION; BACTERIAL COLONIZATION; BONE TISSUE; CONCURRENT DEVELOPMENT; FUNCTIONALIZED; IMPLANT SURFACE; INFECTION; OSTEOBLAST FUNCTION; SURFACE MODIFICATION TECHNIQUES; TISSUE CELLS; TITANIUM IMPLANT; TITANIUM SURFACES;

BACTERIA; DENTAL ALLOYS; DENTAL PROSTHESES; OSTEOBLASTS; SURFACE TREATMENT; TISSUE; TITANIUM; TITANIUM ALLOYS;

ADHESION;

BACTERIAL PROTEIN; CELL PROTEIN; TITANIUM;

ARTICLE; BACTERIAL CELL; BACTERIAL COLONIZATION; BACTERIUM ADHERENCE; BONE REGENERATION; CELL FUNCTION; CELL INTERACTION; HUMAN; IMPLANT; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STRUCTURE; SURFACE PROPERTY; TOTAL HIP PROSTHESIS;

BACTERIAL ADHESION; CELL COMMUNICATION; OSTEOBLASTS; PROSTHESES AND IMPLANTS; SURFACE PROPERTIES; TITANIUM;

BACTERIA (MICROORGANISMS);

EID: 84862818876     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2012.01.018     Document Type: Article

References (101)

1. Raikar G.N., Gregory J.C., Ong J.L., Lucas L.C., Lemons J.E., Kawahara D., et al. Surface characterization of titanium implants. JVac Sci Technol 1995, 13:2633-2637.
2. Sul Y., Johansson C.B., Petronis S., Krozer A., Jeong Y., Wennerberg A., et al. Characteristics of the surface oxides on turned and electrochemically oxidized pure titanium implants up to dielectric breakdown: the oxide thickness, micropore configurations, surface roughness, crystal structure and chemical composition. Biomaterials 2002, 23:491-501.
3. Schwartz-Arad D., Laviv A., Levin L. Failure causes, timing, and cluster behavior: an 8-year study of dental implants. Implant Dent 2008, 17:200-203.
4. Kobayashi N., Procop G.W., Krebs V., Kobayashi H., Bauer T.W. Molecular identification of bacteria from aseptically loose implants. Clin Orthop Relat Res 2008, 466:1716-1725.
5. Clohisy J.C., Calvert G., Tull F., McDonald D., Maloney W.J. Reasons for revision hip surgery: a retrospective review. Clin Orthop Relat Res 2004, 429:188-192.
6. Boos C., Fink K., Stomberg P., Koeller W., Igl B.W., Russlies M. The influence of bone quality and the fixation procedure on the primary stability of cementless implanted tibial plateaus. Biomed Tech 2008, 53:70-76.
7. Darouiche R.O. Treatment of infections associated with surgical implants. NEngl J Med 2004, 350:1422-1429.
8. Del Pozo J.L., Patel R. Infection associated with prosthetic joints. New Engl J Med 2009, 361:787-794.
9. Zimmerli W. Prosthetic-joint-associated infections. Best Pract Res Clin Rheu 2006, 20:1045-1063.
10. Whitehouse N.D.F., Kirkland K.B., Richardson W.J., Sexton D.J. The impact of surgical-site infections following orthopedic surgery at a community hospital and a university hospital: adverse quality of life, excess length of stay, and extra cost. Infect Control Hosp Epidemiol 2002, 23:183-189.
11. Lucke M., Wildemann B., Sadoni S., Surke C., Schiller R., Stemberger A., et al. Systemic versus local application of gentamicin in prophylaxis of implant-related osteomyelitis in a rat model. Bone 2005, 36:770-778.
12. Esposito S., Leone S. Prosthetic joint infections: microbiology, diagnosis, management and prevention. Int J Antimicrob Ag 2008, 32:287-293.
13. Schmidmaier G., Lucke M., Wildemann B., Haas N.P., Raschke M. Prophylaxis and treatment of implant-related infections by antibiotic-coated implants: a review. Inj Int J Care Injured 2006, 37(Suppl 2):S105-S112.
14. Langlais F., Belot N., Ropars M., Thomazeau H., Lambotte J.C., Cathelineau G. Antibiotic cements in articular prostheses: current orthopaedic concepts. Int J Antimicrob Ag 2006, 28:84-99.
15. Campoccia D., Montanaro L., Arciola C.R. The significance of infection related to orthopedic devices and issues of antibiotic resistance. Biomaterials 2006, 27:2331-2339.
16. Brånemark P.I. Osseointegration and its experimental studies. JProsthet Dent 1983, 50:399-410.
17. Albrektsson T., Albrektsson B. Osseointegration of bone implants. A review of an alternative mode of fixation. Acta Orthop Scand 1987, 58:567-577.
18. de Jonge L.T., Leeuwenburgh S.C.G., Wolke J.G.C., Jansen J.A. Organic-inorganic surface modifications for titanium implant surfaces. Pharm Res 2008, 25:2357-2369.
19. Kuzyk P.R.T., Schemitsch E.H. The basic science of peri-implant bone healing. Indian J Orthopaedics 2011, 45:108-115.
20. Montanaro L., Campoccia D., Arciola C.R. Nanostructured materials for inhibition of bacterial adhesion in orthopedic implants: a minireview. Int J Artif Organs 2008, 31:771-776.
21. Braceras I., Alava J.I., Goikoetxea L., de Maeztu M.A., Onate J.I. Interaction of engineered surfaces with the living world: ion implantation vs. osseointegration. Surf Coat Tech 2007, 201:8091-8098.
22. Mavrogenis A.F., Dimitriou R., Parvizi J., Babis G.C. Biology of implant osseointegration. JMusculoskelet Neuronal Interact 2009, 9:61-71.
23. Vlacic-Zischke J., Hamlet S.M., Friis T., Tonetti M.S., Ivanovski S. The influence of surface microroughness and hydrophilicity of titanium on the up-regulation of TGFβ/BMP signalling in osteoblasts. Biomaterials 2011, 32:665-671.
24. Kim H.J., Kim S.H., Kim M.S., Lee E.J., Oh H.G., Oh W.M., et al. Varying Ti-6Al-4V surface roughness induces different early morphologic and molecular responses in MG63 osteoblast-like cells. JBiomed Mater Res 2005, 74A:366-373.
25. Junker R., Dimakis A., Thoneick M., Jansen J.A. Effects of implant surface coatings and composition on bone integration: a systematic review. Clin Oral Impl Res 2009, 20(Suppl. 4):185-206.
26. Moriarty T.F., Schlegel U., Perren S., Richards R.G. Infection in fracture fixation: can we influence infection rates through implant design?. JMater Sci Mater Med 2010, 21:1031-1035.
27. Levent T., Vandevelde D., Delobelle J.M., Labourdette P., Létendard J., Lesage P., et al. Infection risk prevention following total knee arthroplasty. Orthop Traumatol Surg Res 2010, 96:49-56.
28. Hetrick E.M., Schoenfisch M.H. Reducing implant-related infections: active release strategies. Chem Soc Rev 2006, 35:780-789.
29. An Y.H., Friedman R.J. Prevention of sepsis in total joint arthroplasty. JHosp Infect 1996, 33:93-108.
30. Harris L.G., Tosatti S., Wieland M., Textor M., Richards R.G. Staphylococcus aureus adhesion to titanium oxide surfaces coated with non-functionalized and peptide-functionalized poly(L-lysine)-grafted-poly(ethylene glycol) copolymers. Biomaterials 2004, 25:4135-4148.
31. Zimmerli W., Waldvogel F.A., Vaudaux P., Nydegger U.E. Pathogenesis of foreign body infection: description and characteristics of an animal model. JInfect Dis 1982, 146(4):487-497.
32. Gristina A.G. Biomaterial-centered infection: microbial adhesion versus tissue integration. Science 1987, 237:1588-1595.
33. Trampuz A., Osmon D., Hanssen A., Steckelberg J.M., Patel R. Molecular and antibiofilm approaches to prosthetic joint infection. Clin Orthop Relat Res 2003, 414:69-88.
34. Schachter B. Slimy business - the biotechnology of biofilms. Nat Biotech 2003, 21:361-365.
35. Davies D. Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Discov 2003, 2:114-122.
36. Poelstra K.A., Barekzi N.A., Rediske A.M., Felts A.G., Slunt J.B., Grainger D.W. Prophylactic treatment of gram-positive and gram-negative abdominal implant infections using locally delivered polyclonal antibodies. JBiomed Mater Res 2002, 60:206-215.
37. Anselme K., Davidson P., Popa A.M., Giazzon M., Liley M., Ploux L. The interaction of cells and bacteria with surfaces structured at the nanometre scale. Acta Biomater 2010, 6:3824-3846.
38. Ploux L., Ponche A., Anselme K. Bacteria/material interfaces: role of the material and cell wall properties. JAdhes Sci Technol 2010, 24:2165-2201.
39. Whitehead K.A., Colligon J., Verran J. Retention of microbial cells in substratum surface features of micrometer and sub-micrometer dimensions. Colloid Surf B 2005, 41:129-138.
40. Flint S.H., Brooks J.D., Bremer P.J. Properties of the stainless steel substrate influencing the adhesion of thermo-resistant streptococci. JFood Eng 2000, 43:235-242.
41. Hilbert L.R., Bagge-Ravn D., Kold J., Gram L. Influence of surface roughness of stainless steel on microbial adhesion and corrosion resistance. Int Biodeter Biodegr 2003, 52:175-185.
42. Puckett S.D., Taylor E., Raimondo T., Webster T.J. The relationship between the nanostructure of titanium surfaces and bacterial attachment. Biomaterials 2010, 31:706-713.
43. Del Curto B., Brunella M.F., Giordano C., Pedeferri M.P., Valtulina V., Visai L., et al. Decreased bacterial adhesion to surface-treated titanium. Int J Artif Organs 2005, 28:718-730.
44. Martin J.Y., Schwartz Z., Hummert T.W., Schraub D.M., Simpson J., Lankford J., et al. Effect of titanium surface roughness on proliferation, differentiation, and protein synthesis of human osteoblast-like cells (MG63). JBiomed Mater Res 1995, 29:389-401.
45. Kieswetter K., Schwartz Z., Hummert T.W., Cochran D.L., Simpson J., Dean D.D., et al. Surface roughness modulates the local production of growth factors and cytokines by osteoblast-like MG-63 cells. JBiomed Mater Res 1996, 32A:55-63.
46. Rosales-Leal J.I., Rodríguez-Valverde M.A., Mazzagliaa G., Ramón-Torregrosa P.J., Díaz-Rodríguez L., García-Martínez O., et al. Effect of roughness, wettability and morphology of engineered titanium surfaces on osteoblast-like cell adhesion. Colloid Surf A 2010, 365:222-229.
47. Lovmand J., Justesen E., Foss M., Lauridsen R.H., Lovmand M., Modin C., et al. The use of combinatorial topographical libraries for the screening of enhanced osteogenic expression and mineralization. Biomaterials 2009, 30:2015-2022.
48. Yang J.Y., Ting Y.C., Lai J.Y., Liu H.L., Fang H.W., Tsai W.B. Quantitative analysis of osteoblast-like cells (MG63) morphology on nanogrooved substrata with various groove and ridge dimensions. JBiomed Mater Res 2009, 90A:629-640.
49. Wennerberg A., Albrektsson T. Effects of titanium surface topography on bone integration: a systematic review. Clin Oral Implants Res 2009, 20:172-184.
50. Wu Y., Zitelli J.P., TenHuisen K.S., Yu X., Libera M.R. Differential response of Staphylococci and osteoblasts to varying titanium surface roughness. Biomaterials 2011, 32:951-960.
51. 2. JBiomed Mater Res 2006, 78A:595-604.
52. Lim J.Y., Hansen J.C., Siedlecki C.A., Runt J., Donahue H.J. Human foetal osteoblastic cell response to polymer-demixed nanotopographic interfaces. JR Soc Interface 2005, 2:97-108.
53. Lord M.S., Foss M., Besenbacher F. Influence of nanoscale surface topography on protein adsorption and cellular response. Nano Today 2010, 5:66-78.
54. Hanawa T., Kamiura Y., Yamamoto S., Kohgo T., Amemiya A., Ukai H., et al. Early bone formation around calcium-ion implanted titanium inserted into rat tibia. JBiomed Mater Res 1997, 36:131-136.
55. Yoshinari M., Oda Y., Kato T., Okuda K., Hirayama A. Influence of surface modifications to titanium on oral bacterial adhesion invitro. JBiomed Mater Res 2000, 52:388-394.
56. Anagnostou F., Debet A., Pavon-Djavid G., Goudaby Z., Helary G., Migonney V. Osteoblast functions on functionalized PMMA based polymers exhibiting Staphylococcus aureus adhesion inhibition. Biomaterials 2006, 27:3912-3919.
57. Kerner S., Migonney V., Pavon-Djavid G., Helary G., Sedel L., Anagnostou F. Bone tissue response to titanium implant surfaces modified with carboxylate and sulfonate groups. JMater Sci Mater Med 2010, 21:707-715.
58. Nejadnik M.R., van der Mei H.C., Norde W., Busscher H.J. Bacterial adhesion and growth on a polymer brush-coating. Biomaterials 2008, 29:4117-4121.
59. Nejadnik M.R., Engelsman A.F., Saldarriaga Fernandez I.C., Busscher H.J., Norde W., van der Mei H.C. Bacterial colonization of polymer brush-coated and pristine silicone rubber implanted in infected pockets in mice. JAntimicrob Chemother 2008, 62:1323-1325.
60. Saldarriaga Fernández I.C., van der Mei H.C., Metzger S., Grainger D.W., Engelsman A.F., Nejadnik M.R., et al. Invitro and invivo comparisons of staphylococcal biofilm formation on a cross-linked poly(ethylene glycol)-based polymer coating. Acta Biomater 2010, 6:1119-1124.
61. Roosjen A., Norde W., van der Mei H.C., Busscher H.J. The use of positively charged or low surface free energy coatings versus polymer brushes in controlling biofilm formation. Prog Colloid Polym Sci 2006, 132:138-144.
62. Pitt W.G., Morris R.N., Mason M.L., Hall M.W., Luo Y., Prestwich G.D. Attachment of hyaluronan to metallic surfaces. JBiomed Mater Res 2004, 68A:95-106.
63. Cassinelli C., Morra M., Pavesio A., Renier D. Evaluation of interfacial properties of hyaluronan coated poly(methylmethacrylate) intraocular lenses. JBiomat Sci-Polym E 2000, 11:961-977.
64. Saldarriaga Fernández I.C., Busscher H.J., Metzger S.W., Grainger D.W., van der Mei H.C. Competitive time- and density-dependent adhesion of staphylococci and osteoblasts on crosslinked poly(ethylene glycol)-based polymer coatings in co-culture flow chambers. Biomaterials 2011, 32:979-984.
65. Subbiahdoss G., Pidhatika B., Coullerez G., Charnley M., Kuijer R., van der Mei H.C., et al. Bacterial biofilm formation versus mammalian cell growth on titanium-based mono- and bi-functional coatings. Eur Cells Mater 2010, 19:205-213.
66. 2 depends on the competitive preadsorption of albumin and fibronectin. JBiomed Mater Res 2008, 84A:281-290.
67. Herrmann M., Vaudaux P.E., Pittet D., Auckenthaler R., Lew P.D., Schumacher-Perdreau F., et al. Fibronectin, fibrinogen, and laminin act as mediators of adherence of clinical staphylococcal isolates to foreign material. JInfect Dis 1988, 158:693-701.
68. Arciola C.R., Bustanji Y., Conti M., Campoccia D., Baldassarri L., Samorì B., et al. Staphylococcus epidermidis-fibronectin binding and its inhibition by heparin. Biomaterials 2003, 24:3013-3019.
69. Peacock S.J., Foster T.J., Cameron B.J., Berendt A.R. Bacterial fibronectin-binding proteins and endothelial cell surface fibronectin mediate adherence of Staphylococcus aureus to resting human endothelial cells. Microbiology 1999, 145:3477-3486.
70. Fowler T., Wann E.R., Joh D., Johansson S., Foster T.J., Hook M. Cellular invasion by Staphylococcus aureus involves a fibronectin bridge between the bacterial fibronectin-binding MSCRAMMs and host cell beta1 integrins. Eur J Cell Biol 2000, 79:672-679.
71. Sinha B., Francois P., Que Y.A., Hussain M., Heilmann C., Moreillon P., et al. Heterologously expressed Staphylococcus aureus fibronectin-binding proteins are sufficient for invasion of host cells. Infect Immun 2000, 68:6871-6878.
72. Maddikeri R.R., Tosatti S., Schuler M., Chessari S., Textor M., Richards R.G., et al. Reduced medical infection related bacterial strains adhesion on bioactive RGD modified titanium surfaces: a first step toward cell selective surfaces. JBiomed Mater Res 2008, 84A:425-435.
73. Zhang F., Zhang Z.B., Zhu X.L., Kang E.T., Neoh K.G. Silk-functionalized titanium surfaces for enhancing osteoblast functions and reducing bacterial adhesion. Biomaterials 2008, 29:4751-4759.
74. Vester H., Wildemann B., Schmidmaier G., Stöckle U., Lucke M. Gentamycin delivered from a PDLLA coating of metallic implants Invivo and invitro characterisation for local prophylaxis of implant-related osteomyelitis. Injury Int J Care Injured 2010, 41:1053-1059.
75. Raafat D., von Bargen K., Haas A., Sahl H.G. Insights into the mode of action of chitosan as an antibacterial compound. Appl Environ Microb 2008, 74:3764-3773.
76. Rabea E.I., Badawy M.E.T., Stevens C.V., Smagghe G., Steurbaut W. Chitosan as antimicrobial agent: applications and mode of action. Biomacromolecules 2003, 4:1457-1465.
77. Hamilton V., Yuan Y.L., Rigney D.A., Chesnutt B.M., Puckett A.D., Ong J.L., et al. Bone cell attachment and growth on well-characterized chitosan films. Polym Int 2007, 56:641-647.
78. Arpornmaeklong P., Suwatwirote N., Pripatnanot P., Oungbho K. Growth and differentiation of mouse osteoblasts on chitosan-collagen sponges. Int J Oral Maxillofac Surg 2007, 36:328-337.
79. Chua P.H., Neoh K.G., Kang E.T., Wang W. Surface functionalization of titanium with hyaluronic acid/chitosan polyelectrolyte multilayers and RGD for promoting osteoblast functions and inhibiting bacterial adhesion. Biomaterials 2008, 29:1412-1421.
80. Shi Z.L., Neoh K.G., Kang E.T., Poh C.K., Wang W. Bacterial adhesion and osteoblast function on titanium with surface-grafted chitosan and immobilized RGD peptide. JBiomed Mater Res 2008, 86A:865-872.
81. Morra M. Biochemical modification of titanium surfaces: peptides and ECM proteins. Eur Cell Mater 2006, 12:1-15.
82. Harwood P.J., Giannoudis P.V. Application of bone morphogenetic proteins in orthopedic practice: their efficacy and side effects. Expert Opin Drug Saf 2005, 4:75-89.
83. Li R.H., Wozney J.M. Delivering on the promise of bone morphogenetic proteins. Trends Biotechnol 2001, 19:255-265.
84. Hall J., Sorensen R.G., Wozney J.M., Wikesjö U.M.E. Bone formation at rhBMP-2-coated titanium implants in the rat ectopic model. JClin Periodontol 2007, 34:444-451.
85. Puleo D.A., Kissling R.A., Sheu M.S. Atechnique to immobilize bioactive proteins, including bone morphogenetic protein-4 (BMP-4), on titanium alloy. Biomaterials 2002, 23:2079-2087.
86. Shi Z.L., Neoh K.G., Kang E.T., Poh C.K., Wang W. Titanium with surface-grafted dextran and immobilized bone morphogenetic protein-2 for inhibition of bacterial adhesion and enhancement of osteoblast functions. Tissue Eng Part A 2009, 15:417-426.
87. Shi Z.L., Neoh K.G., Kang E.T., Poh C.K., Wang W. Surface functionalization of titanium with carboxymethyl chitosan and immobilized bone morphogenetic protein-2 for enhanced osseointegration. Biomacromolecules 2009, 10:1603-1611.
88. Hu X.F., Neoh K.G., Shi Z.L., Kang E.T., Poh C.K., Wang W. An invitro assessment of titanium functionalized with polysaccharides conjugated with vascular endothelial growth factor for enhanced osseointegration and inhibition of bacterial adhesion. Biomaterials 2010, 31:8854-8863.
89. Lee J.H., Wang H., Kaplan J.B., Lee W.Y. Effects of Staphylococcus epidermidis on osteoblast cell adhesion and viability on a Ti alloy surface in a microfluidic co-culture environment. Acta Biomater 2010, 6:4422-4429.
90. Subbiahdoss G., Kuijer R., Grijpma D.W., van der Mei H.C., Busscher H.J. Microbial biofilm growth vs. tissue integration: ''The race for the surface" experimentally studied. Acta Biomater 2009, 5:1399-1404.
91. Somayaji S.N., Huet Y.M., Gruber H.E., Hudson M.C. UV-killed Staphylococcus aureus enhances adhesion and differentiation of osteoblasts on bone-associated biomaterials. JBiomed Mater Res 2010, 95A:574-579.
92. Rechendorff K., Hovgaard M.B., Foss M., Zhdanov V.P., Besenbacher F. Enhancement of protein adsorption induced by surface roughness. Langmuir 2006, 22:10885-10888.
93. Scopelliti P.E., Borgonovo A., Indrieri M., Giorgetti L., Bongiorno G., Carbone R., et al. The effect of surface nanometre-scale morphology on protein adsorption. PLoS One 2010, 5:e11862.
94. Galli C., Collaud Coen M., Hauert R., Katanaev V.L., Gröning P., Schlapbach L. Creation of nanostructures to study the topographical dependency of protein adsorption. Colloid Surf B 2002, 26:255-267.
95. Han M., Sethuraman A., Kane S.R., Belfort G. Nanometer-scale roughness having little effect on the amount or structure of adsorbed protein. Langmuir 2003, 19:9868-9872.
96. Cai K., Bossert J., Jandt K. Does the nanometre scale topography of titanium influence protein adsorption and cell proliferation?. Colloid Surf B 2006, 49:136-144.
97. Malmsten M., Emoto K., Van Alstine J.M. Effect of chain density on inhibition of protein adsorption by poly(ethylene glycol) based coatings. JColloid Interf Sci 1998, 202:507-517.
98. Dalsin J.L., Lin L., Tosatti S., Vörös J., Textor M., Messersmith P.B. Protein resistance of titanium oxide surfaces modified by biologically inspired mPEG-DOPA. Langmuir 2005, 21:640-646.
99. Yano K., Hoshino M., Ohta Y., Manaka T., Naka Y., Imai Y., et al. Osteoinductive capacity and heat stability of recombinant human bone morphogenetic protein 2 produced by Escherichia coli and dimerized by biochemical processing. JBone Miner Metab 2009, 27:355-363.
100. Winkler L., Bingmann D., Wiemann M. Heat treatment of BMP-2 depots on implant materials generates an immobilized layer of BMP-2 with pronounced bioactivity. JBiomed Mater Res 2006, 79A:895-901.
101. Wiemann M., Jennissen H., Rumpf H., Winkler L., Chatzinikolaidou M., Schmitz I., et al. Areporter-cell assay for the detection of BMP-2 immobilized on porous and nonporous materials. JBiomed Mater Res 2002, 62:119-127.