Implant osseointegration and the role of microroughness and nanostructures: Lessons for spine implants

Acta Biomaterialia

Volumn 10, Issue 8, 2014, Pages 3363-3371

  Gittens, Rolando A ^a,b,c   Olivares Navarrete, Rene ^d   Schwartz, Zvi ^b,d   Boyan, Barbara D ^a,b,d,e  

^a Georgia Institute of Technology   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^c INSTITUTO DE INVESTIGACIONES CIENTÍFICAS Y SERVICIOS DE ALTA TECNOLOGÍA   (Panama)

^d Virginia Commonwealth University   (United States)

^e Emory University   (United States)

Author keywords

Bone; Nanostructures; Spine fusion; Titanium surface properties; Topography roughness

Indexed keywords

BONE; METAL IMPLANTS; SURFACE PROPERTIES; TITANIUM;

CHEMICAL COMPOSITIONS; DIFFERENT SHAPES; FUSION CAGES; MICRO-ROUGHNESS; OSSEOINTEGRATION; SPINAL IMPLANT; SPINE FUSION; TITANIA SURFACE PROPERTY; TITANIA SURFACES; TOPOGRAPHY ROUGHNESS;

NANOSTRUCTURES;

NANOMATERIAL; BIOMATERIAL;

BONE DEVELOPMENT; BONE REGENERATION; BONE REMODELING; BONE STRUCTURE; CELL FUNCTION; CHEMICAL COMPOSITION; DONOR SITE; FIBRIN CLOT; HUMAN; IN VITRO STUDY; IN VIVO STUDY; OSSIFICATION; OSTEOBLAST; PRIORITY JOURNAL; REVIEW; SPINE FUSION; SPINE IMPLANT; SURFACE PROPERTY; SURGICAL TECHNIQUE; WOUND HEALING; ANIMAL; CHEMISTRY; DEVICE FAILURE ANALYSIS; DEVICES; PHYSIOLOGY; PROSTHESES AND ORTHOSES; PROSTHESIS DESIGN; SPINE; SURGERY;

ANIMALS; BIOCOMPATIBLE MATERIALS; EQUIPMENT FAILURE ANALYSIS; HUMANS; NANOSTRUCTURES; OSSEOINTEGRATION; PROSTHESES AND IMPLANTS; PROSTHESIS DESIGN; SPINAL FUSION; SPINE; SURFACE PROPERTIES;

EID: 84903717549     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2014.03.037     Document Type: Review

References (118)

1. J.J. Jacobs, G.B.J. Andersson, J.E. Bell, S.L. Weinstein, J.P. Dormans, and S.M. Gnatz et al. United States bone and joint decade: the burden of musculoskeletal diseases in the United States 2008 AAOS Rosemont, IL
2. E.N. Hanley The indications for lumbar spinal fusion with and without instrumentation Spine 20 1995 S143 S153
3. R.J. Hacker, J.C. Cauthen, T.J. Gilbert, and S.L. Griffith A prospective randomized multicenter clinical evaluation of an anterior cervical fusion cage Spine 25 2000 2646 2654
4. T.A. Zdeblick, and F.M. Phillips Interbody cage devices Spine 28 2003 S2 S7
5. C.M. Agrawal, M. Attawia, M.D. Borden, B.D. Boyan, S.P. Bruder, and R.W. Bucholz et al. Bone graft substitutes 2003 ASTM International/AAOS West Conshohocken, PA
6. C.D. Ray Threaded fusion cages for lumbar interbody fusions - an economic comparison with 360 degrees fusions Spine 22 1997 681 685
7. P.I. Branemark, B.O. Hansson, R. Adell, U. Breine, J. Lindstrom, and O. Hallen et al. Osseointegrated implants in the treatment of the edentulous jaw. Experience from a 10-year period Scand J Plast Reconstr Surg Suppl 16 1977 1 132
8. A. Bobbio The first endosseous alloplastic implant in the history of man Bull Hist Dent 20 1972 1 6
9. B.R. Lang, and A.A. Chiappa Mandibular implants - a new method of attachment J Prosthet Dent 22 1969 261 267
10. N. Sykaras, A.M. Iacopino, V.A. Marker, R.G. Triplett, and R.D. Woody Implant materials, designs, and surface topographies: their effect on osseointegration. A literature review Int J Oral Maxillofac Implants 15 2000 675 690
11. P.M. Beck Endosseous implants: a review of current advances and a case report Oral Health 60 1970 19 21
12. J.C. Southam, and P. Selwyn Structural changes around screws used in the treatment of fractured human mandibles Br J Oral Surg 8 1971 211 221
13. D.C. Picton, R.B. Johns, D.J. Wills, and W.I. Davies The relationship between the mechanisms of tooth and implant support Oral Sci Rev 5 1974 3 22
14. N.A. Athanasou, J. Quinn, and C.J. Bulstrode Resorption of bone by inflammatory cells derived from the joint capsule of hip arthroplasties J Bone Joint Surg Br 74 1992 57 62
15. J. Lassus, J. Salo, W.A. Jiranek, S. Santavirta, J. Nevalainen, and M. Matucci-Cerinic et al. Macrophage activation results in bone resorption Clin Orthop Relat Res 1998 7 15
16. S. Szmukler-Moncler, H. Salama, Y. Reingewirtz, and J.H. Dubruille Timing of loading and effect of micromotion on bone-dental implant interface: review of experimental literature J Biomed Mater Res 43 1998 192 203
17. H.P. Cook Immediate reconstruction of the mandible by metallic implant following resection for neoplasm Ann R Coll Surg Engl 42 1968 233 259
18. K.A. Thomas, J.F. Kay, S.D. Cook, and M. Jarcho The effect of surface macrotexture and hydroxylapatite coating on the mechanical strengths and histologic profiles of titanium implant materials J Biomed Mater Res 21 1987 1395 1414
19. N.J. Hallab, B.W. Cunningham, and J.J. Jacobs Spinal implant debris-induced osteolysis Spine (Phila Pa 1976) 28 2003 S125 S138
20. S.M. Kurtz, and J.N. Devine PEEK biomaterials in trauma, orthopedic, and spinal implants Biomaterials 28 2007 4845 4869
21. E.R. Santos, D.G. Goss, R.K. Morcom, and R.D. Fraser Radiologic assessment of interbody fusion using carbon fiber cages Spine (Phila Pa 1976) 28 2003 997 1001
22. N.K. Anjarwalla, R.K. Morcom, and R.D. Fraser Supplementary stabilization with anterior lumbar intervertebral fusion - a radiologic review Spine 31 2006 1281 1287
23. B.W. Cunningham, C.M. Orbegoso, A.E. Dmitriev, N.J. Hallab, J.C. Sefter, and P. Asdourian et al. The effect of spinal instrumentation particulate wear debris. An in vivo rabbit model and applied clinical study of retrieved instrumentation cases Spine J 3 2003 19 32
24. C.H. Lohmann, Z. Schwartz, G. Koster, U. Jahn, G.H. Buchhorn, and M.J. MacDougall et al. Phagocytosis of wear debris by osteoblasts affects differentiation and local factor production in a manner dependent on particle composition Biomaterials 21 2000 551 561
25. D.P. Pioletti, H. Takei, S.Y. Kwon, D. Wood, and K.L.P. Sung The cytotoxic effect of titanium particles phagocytosed by osteoblasts J Biomed Mater Res 46 1999 399 407
26. C. Maniatopoulos, R.M. Pilliar, and D.C. Smith Threaded versus porous-surfaced designs for implant stabilization in bone-endodontic implant model J Biomed Mater Res 20 1986 1309 1333
27. A. Piattelli, A. Scarano, L. Favero, G. Iezzi, G. Petrone, and G.A. Favero Clinical and histologic aspects of dental implants removed due to mobility J Periodontol 74 2003 385 390
28. R. Olivares-Navarrete, R.A. Gittens, J.M. Schneider, S.L. Hyzy, D.A. Haithcock, and P.F. Ullrich et al. Osteoblasts exhibit a more differentiated phenotype and increased bone morphogenetic protein production on titanium alloy substrates than on poly ether-ether-ketone Spine J 12 2012 265 272
29. R. Olivares-Navarrete, S.L. Hyzy, R.A.s. Gittens, J.M. Schneider, D.A. Haithcock, and P.F. Ullrich et al. Rough titanium alloys regulate osteoblast production of angiogenic factors Spine J 13 2013 1563 1570
30. Y.T. Sul, C. Johansson, P. Wennerberg, L.R. Cho, B.S. Chang, and P. Albrektsson Optimum surface properties of oxidized implants for reinforcement of osseointegration: surface chemistry, oxide thickness, porosity, roughness, and crystal structure Int J Oral Maxillofac Implants 20 2005 349 359
31. F. Schwarz, M. Wieland, Z. Schwartz, G. Zhao, F. Rupp, and J. Geis-Gerstorfer et al. Potential of chemically modified hydrophilic surface characteristics to support tissue integration of titanium dental implants J Biomed Mater Res B Appl Biomater 88B 2009 544 557
32. D.A. Puleo, and A. Nanci Understanding and controlling the bone-implant interface Biomaterials 20 1999 2311 2321
33. T. Kokubo, H.M. Kim, M. Kawashita, and T. Nakamura Bioactive metals: preparation and properties J Mater Sci Mater Med 15 2004 99 107
34. J.E. Davies Bone bonding at natural and biomaterial surfaces Biomaterials 28 2007 5058 5067
35. T. Albrektsson, and A. Wennerberg Oral implant surfaces. Part 1. Review focusing on topographic and chemical properties of different surfaces and in vivo responses to them Int J Prosthodont 17 2004 536 543
36. A. Wennerberg, and T. Albrektsson Effects of titanium surface topography on bone integration: a systematic review Clin Oral Implants Res 20 2009 172 184
37. G. Mendonca, D.B.S. Mendonca, F.J.L. Aragao, and L.F. Cooper Advancing dental implant surface technology - from micron- to nanotopography Biomaterials 29 2008 3822 3835
38. J.J. Regan, H. Yuan, and P.C. McAfee Laparoscopic fusion of the lumbar spine: minimally invasive spine surgery. A prospective multicenter study evaluating open and laparoscopic lumbar fusion Spine (Phila Pa 1976) 24 1999 402 411
39. P.C. McAfee Interbody fusion cages in reconstructive operations on the spine J Bone Joint Surg Am 81 1999 859 880
40. V. Baelum, and B. Ellegaard Implant survival in periodontally compromised patients J Periodontol 75 2004 1404 1412
41. J.D. Andrade, and V. Hlady Protein adsorption and materials biocompatibility - a tutorial review and suggested hypotheses Adv Polym Sci 79 1986 1 63
42. C.J. Wilson, R.E. Clegg, D.I. Leavesley, and M.J. Pearcy Mediation of biomaterial-cell interactions by adsorbed proteins: a review Tissue Eng 11 2005 1 18
43. E. Jansson, and P. Tengvall In vitro preparation and ellipsometric characterization of thin blood plasma clot films on silicon Biomaterials 22 2001 1803 1808
44. B.G. Keselowsky, D.M. Collard, and A.J. Garcia Surface chemistry modulates fibronectin conformation and directs integrin binding and specificity to control cell adhesion J Biomed Mater Res A 66A 2003 247 259
45. R.E. Marx Platelet-rich plasma: evidence to support its use J Oral Maxillofac Surg 62 2004 489 496
46. D. Di Iorio, T. Traini, M. Degidi, S. Caputi, J. Neugebauer, and A. Piattelli Quantitative evaluation of the fibrin clot extension on different implant surfaces: an in vitro study J Biomed Mater Res B Appl Biomater 74B 2005 636 642
47. J.E. Davies Understanding peri-implant endosseous healing J Dent Educ 67 2003 932 949
48. J.E. Davies Mechanisms of endosseous integration Int J Prosthodont 11 1998 391 401
49. J.E. Babensee, J.M. Anderson, L.V. McIntire, and A.G. Mikos Host response to tissue engineered devices Adv Drug Deliv Rev 33 1998 111 139
50. A. Schindeler, M.M. McDonald, P. Bokko, and D.G. Little Bone remodeling during fracture repair: the cellular picture Semin Cell Dev Biol 19 2008 459 466
51. A.I. Caplan, and J.E. Dennis Mesenchymal stem cells as trophic mediators J Cell Biochem 98 2006 1076 1084
52. S. Neuss, R.K. Schneider, L. Tietze, R. Knuchel, and W. Jahnen-Dechent Secretion of fibrinolytic enzymes facilitates human mesenchymal stem cell invasion into fibrin clots Cells Tissues Organs 191 2010 36 46
53. S.P. Bruder, D.J. Fink, and A.I. Caplan Mesenchymal stem cells in bone development, bone repair, and skeletal regeneration therapy J Cell Biochem 56 1994 283 294
54. R. Olivares-Navarrete, S.L. Hyzy, D.L. Hutton, C.P. Erdman, M. Wieland, and B.D. Boyan et al. Direct and indirect effects of microstructured titanium substrates on the induction of mesenchymal stem cell differentiation towards the osteoblast lineage Biomaterials 31 2010 2728 2735
55. L. Saruwatari, H. Aita, F. Butz, H.K. Nakamura, J. Ouyang, and Y. Yang et al. Osteoblasts generate harder, stiffer, and more delamination-resistant mineralized tissue on titanium than on polystyrene, associated with distinct tissue micro- and ultrastructure J Bone Miner Res 20 2005 2002 2016
56. T.A. Owen, M. Aronow, V. Shalhoub, L.M. Barone, L. Wilming, and M.S. Tassinari et al. Progressive development of the rat osteoblast phenotype invitro-reciprocal relationships in expression of genes associated with osteoblast proliferation and differentiation during formation of the bone extracellular-matrix J Cell Physiol 143 1990 420 430
57. J.E. Davies, and N. Baldan Scanning electron microscopy of the bone bioactive implant interface J Biomed Mater Res 36 1997 429 440
58. M.D. McKee, and A. Nanci Osteopontin at mineralized tissue interfaces in bone, teeth, and osseointegrated implants: ultrastructural distribution and implications for mineralized tissue formation, turnover, and repair Microsc Res Tech 33 1996 141 164
59. P.J. Thurner, S. Lam, J.C. Weaver, D.E. Morse, and P.K. Hansma Localization of phosphorylated serine, osteopontin, and bone sialoprotein on bone fracture surfaces J Adhes 85 2009 526 545
60. M.T.K. Mulari, Q. Qu, P.L. Harkonen, and H.K. Vaananen Osteoblast-like cells complete osteoclastic bone resorption and form new mineralized bone matrix in vitro Calcif Tissue Int 75 2004 253 261
61. S.L. Teitelbaum, and F.P. Ross Genetic regulation of osteoclast development and function Nat Rev Genet 4 2003 638 649
62. S.L. Teitelbaum Bone resorption by osteoclasts Science 289 2000 1504 1508
63. T.J. Chambers, P.A. Revell, K. Fuller, and N.A. Athanasou Resorption of bone by isolated rabbit osteoclasts J Cell Sci 66 1984 383 399
64. L.M. Svanborg, M. Andersson, and A. Wennerberg Surface characterization of commercial oral implants on the nanometer level J Biomed Mater Res B Appl Biomater 92 2010 462 469
65. A. Wennerberg, R. Ohlsson, B.G. Rosen, and B. Andersson Characterizing three-dimensional topography of engineering and biomaterial surfaces by confocal laser scanning and stylus techniques Med Eng Phys 18 1996 548 556
66. M. Wieland, M. Textor, N.D. Spencer, and D.M. Brunette Wavelength-dependent roughness: a quantitative approach to characterizing the topography of rough titanium surfaces Int J Oral Maxillofac Implants 16 2001 163 181
67. H. Wang, M. Xu, W. Zhang, D.T. Kwok, J. Jiang, and Z. Wu et al. Mechanical and biological characteristics of diamond-like carbon coated poly aryl-ether-ether-ketone Biomaterials 31 2010 8181 8187
68. K.B. Sagomonyants, M.L. Jarman-Smith, J.N. Devine, M.S. Aronow, and G.A. Gronowicz The in vitro response of human osteoblasts to polyetheretherketone (PEEK) substrates compared to commercially pure titanium Biomaterials 29 2008 1563 1572
69. T.J. Dennes, and J. Schwartz A nanoscale adhesion layer to promote cell attachment on PEEK JACS 131 2009 3456 3457
70. Z. Schwartz, P. Raz, G. Zhao, Y. Barak, M. Tauber, and H. Yao et al. Effect of micrometer-scale roughness of the surface of Ti6Al4V pedicle screws in vitro and in vivo J Bone Joint Surg (Am) 90A 2008 2485 2498
71. C. Hallgren, H. Reimers, D. Chakarov, J. Gold, and A. Wennerberg An in vivo study of bone response to implants topographically modified by laser micromachining Biomaterials 24 2003 701 710
72. G. Giavaresi, M. Fini, R. Chiesa, C. Giordano, E. Sandrini, and A.E. Bianchi et al. A novel multiphase anodic spark deposition coating for the improvement of orthopedic implant osseointegration: an experimental study in cortical bone of sheep J Biomed Mater Res A 85 2008 1022 1031
73. C.A. Simmons, N. Valiquette, and R.M. Pilliar Osseointegration of sintered porous-surfaced and plasma spray-coated implants: an animal model study of early postimplantation healing response and mechanical stability J Biomed Mater Res 47 1999 127 138
74. D. Buser, T. Nydegger, H.P. Hirt, D.L. Cochran, and L.P. Nolte Removal torque values of titanium implants in the maxilla of miniature pigs Int J Oral Maxillofac Implants 13 1998 611 619
75. D. Buser, N. Broggini, M. Wieland, R.K. Schenk, A.J. Denzer, and D.L. Cochran et al. Enhanced bone apposition to a chemically modified SLA titanium surface J Dent Res 83 2004 529 533
76. 2/HCl treated titanium implants: an experimental study in the rabbit Int J Oral Maxillofac Surg 38 2009 677 681
77. S. Szmukler-Moncler, D. Perrin, V. Ahossi, G. Magnin, and J.P. Bernard Biological properties of acid etched titanium implants: effect of sandblasting on bone anchorage J Biomed Mater Res B Appl Biomater 68B 2004 149 159
78. O. Zinger, G. Zhao, Z. Schwartz, J. Simpson, M. Wieland, and D. Landolt et al. Differential regulation of osteoblasts by substrate microstructural features Biomaterials 26 2005 1837 1847
79. G. Zhao, O. Zinger, Z. Schwartz, M. Wieland, D. Landolt, and B.D. Boyan Osteoblast-like cells are sensitive to submicron-scale surface structure Clin Oral Implants Res 17 2006 258 264
80. G.S. Stein, and J.B. Lian Molecular mechanisms mediating proliferation/differentiation interrelationships during progressive development of the osteoblast phenotype Endocr Rev 14 1993 424 442
81. M.J. Kim, C.W. Kim, Y.J. Lim, and S.J. Heo Microrough titanium surface affects biologic response in MG63 osteoblast-like cells J Biomed Mater Res A 79 2006 1023 1032
82. B.D. Boyan, Z. Schwartz, L.F. Bonewald, and L.D. Swain Localization of 1,25-(Oh)2d3-responsive alkaline-phosphatase in osteoblast-like cells (Ros 17/2.8, Mg-63, and Mc-3t3) and growth cartilage cells in culture J Biol Chem 264 1989 11879 11886
83. P.V. Hauschka, J.B. Lian, D.E.C. Cole, and C.M. Gundberg Osteocalcin and matrix gla protein - vitamin K-dependent proteins in bone Physiol Rev 69 1989 990 1047
84. T.A. Petrie, C.D. Reyes, K.L. Burns, and A.J. Garcia Simple application of fibronectin-mimetic coating enhances osseointegration of titanium implants J Cell Mol Med 13 2009 2602 2612
85. A. van der Flier, and A. Sonnenberg Function and interactions of integrins Cell Tissue Res 305 2001 285 298
86. R. Olivares-Navarrete, P. Raz, G. Zhao, J. Chen, M. Wieland, and D.L. Cochran et al. Integrin alpha 2 beta 1 plays a critical role in osteoblast response to micron-scale surface structure and surface energy of titanium substrates Proc Natl Acad Sci U S A 105 2008 15767 15772
87. J.E. Villanueva, and M.E. Nimni Promotion of calvarial cell osteogenesis by endothelial-cells J Bone Miner Res 5 1990 733 739
88. C. Maes, T. Kobayashi, M.K. Selig, S. Torrekens, S.I. Roth, and S. Mackem et al. Osteoblast precursors, but not mature osteoblasts, move into developing and fractured bones along with invading blood vessels Dev Cell 19 2010 329 344
89. A.L. Raines, R. Olivares-Navarrete, M. Wieland, D.L. Cochran, Z. Schwartz, and B.D. Boyan Regulation of angiogenesis during osseointegration by titanium surface microstructure and energy Biomaterials 31 2010 4909 4917
90. S. Balloni, E.M. Calvi, F. Damiani, G. Bistoni, M. Calvitti, and P. Locci et al. Effects of titanium surface roughness on mesenchymal stem cell commitment and differentiation signaling Int J Oral Maxillofac Implants 24 2009 627 635
91. N. Donos, M. Retzepi, I. Wall, S. Hamlet, and S. Ivanovski In vivo gene expression profile of guided bone regeneration associated with a microrough titanium surface Clin Oral Implants Res 22 2011 390 398
92. R. Olivares-Navarrete, S. Hyzy, M. Wieland, B.D. Boyan, and Z. Schwartz The roles of Wnt signaling modulators Dickkopf-1 (Dkk1) and Dickkopf-2 (Dkk2) and cell maturation state in osteogenesis on microstructured titanium surfaces Biomaterials 31 2010 2015 2024
93. G. Karsenty, and E.F. Wagner Reaching a genetic and molecular understanding of skeletal development Dev Cell 2 2002 389 406
94. M. Kato, M.S. Patel, R. Levasseur, I. Lobov, B.H. Chang, and D.A. Glass 2nd et al. Cbfa1-independent decrease in osteoblast proliferation, osteopenia, and persistent embryonic eye vascularization in mice deficient in Lrp5, a Wnt coreceptor J Cell Biol 157 2002 303 314
95. M. Centrella, M.C. Horowitz, J.M. Wozney, and T.L. McCarthy Transforming growth factor-beta gene family members and bone Endocr Rev 15 1994 27 39
96. S. Lossdorfer, Z. Schwartz, L. Wang, C.H. Lohmann, J.D. Turner, and M. Wieland et al. Microrough implant surface topographies increase osteogenesis by reducing osteoclast formation and activity J Biomed Mater Res A 70 2004 361 369
97. S.L. Hyzy, R. Olivares-Navarrete, D.L. Hutton, C. Tan, B.D. Boyan, and Z. Schwartz Microstructured titanium regulates interleukin production by osteoblasts, an effect modulated by exogenous BMP-2 Acta Biomater 9 2013 5821 5829
98. R. Olivares-Navarrete, A.L. Raines, S.L. Hyzy, J.H. Park, D.L. Hutton, and D.L. Cochran et al. Osteoblast maturation and new bone formation in response to titanium implant surface features are reduced with age J Bone Miner Res 27 2012 1773 1783
99. C.N. Elias, and L. Meirelles Improving osseointegration of dental implants Expert Rev Med Devices 7 2010 241 256
100. L.M. Bjursten, L. Rasmusson, S. Oh, G.C. Smith, K.S. Brammer, and S. Jin Titanium dioxide nanotubes enhance bone bonding in vivo J Biomed Mater Res A 92 2010 1218 1224
101. G. Mendonca, D.B.S. Mendonca, L.G.P. Simoes, A.L. Araujo, E.R. Leite, and A.L. Golin et al. Nanostructured implant surface effect on osteoblast gene expression and bone-to-implant contact in vivo Mater Sci Eng C Mater Biol Appl 31 2011 1809 1818
102. N. Tsukimura, T. Ueno, F. Iwasa, H. Minamikawa, Y. Sugita, and K. Ishizaki et al. Bone integration capability of alkali- and heat-treated nanobimorphic Ti-15Mo-5Zr-3Al Acta Biomater 7 2011 4267 4277
103. R. Jimbo, Y. Xue, M. Hayashi, H.O. Schwartz, M. Andersson, and K. Mustafa et al. Genetic responses to nanostructured calcium-phosphate-coated implants J Dent Res 90 2011 1422 1427
104. G. Mendonca, D.B.S. Mendonca, L.G.P. Simoes, A.L. Araujo, E.R. Leite, and W.R. Duarte et al. Nanostructured alumina-coated implant surface: effect on osteoblast-related gene expression and bone-to-implant contact in vivo Int J Oral Maxillofac Implants 24 2009 205 215
105. K.Y. Cai, J. Bossert, and K.D. Jandt Does the nanometre scale topography of titanium influence protein adsorption and cell proliferation? Colloids Surf B Biointerfaces 49 2006 136 144
106. T.J. Webster, and J.U. Ejiofor Increased osteoblast adhesion on nanophase metals: Ti, Ti6Al4V, and CoCrMo Biomaterials 25 2004 4731 4739
107. M.J.P. Biggs, R.G. Richards, N. Gadegaard, C.D.W. Wilkinson, and M.J. Dalby The effects of nanoscale pits on primary human osteoblast adhesion formation and cellular spreading J Mater Sci Mater Med 18 2007 399 404
108. D. Khang, J. Lu, C. Yao, K.M. Haberstroh, and T.J. Webster The role of nanometer and sub-micron surface features on vascular and bone cell adhesion on titanium Biomaterials 29 2008 970 983
109. M. Arnold, E.A. Cavalcanti-Adam, R. Glass, J. Blummel, W. Eck, and M. Kantlehner et al. Activation of integrin function by nanopatterned adhesive interfaces ChemPhysChem 5 2004 383 388
110. G. Mendonca, D.B.S. Mendonca, L.G.P. Simoes, A.L. Araujo, E.R. Leite, and W.R. Duarte et al. The effects of implant surface nanoscale features on osteoblast-specific gene expression Biomaterials 30 2009 4053 4062
111. P.T. de Oliveira, and A. Nanci Nanotexturing of titanium-based surfaces upregulates expression of bone sialoprotein and osteopontin by cultured osteogenic cells Biomaterials 25 2004 403 413
112. 2 nanonodular structures in a micro-to-nanoscale hierarchy model Biomaterials 30 2009 5319 5329
113. 2 treatment and its effects on osteoblast-specific gene expression of hMSCs J Biomed Mater Res A 94A 2010 169 179
114. A. Wilkinson, R.N. Hewitt, L.E. McNamara, D. McCloy, R.M. Dominic Meek, and M.J. Dalby Biomimetic microtopography to enhance osteogenesis in vitro Acta Biomater 7 2011 2919 2925
115. R.A. Gittens, T. McLachlan, R. Olivares-Navarrete, Y. Cai, S. Berner, and R. Tannenbaum et al. The effects of combined micron-/submicron-scale surface roughness and nanoscale features on cell proliferation and differentiation Biomaterials 32 2011 3395 3403
116. R.J. McMurray, N. Gadegaard, P.M. Tsimbouri, K.V. Burgess, L.E. McNamara, and R. Tare et al. Nanoscale surfaces for the long-term maintenance of mesenchymal stem cell phenotype and multipotency Nat Mater 10 2011 637 644
117. R.A. Gittens, R. Olivares-Navarrete, T. McLachlan, Y. Cai, S.L. Hyzy, and J.M. Schneider et al. Differential responses of osteoblast lineage cells to nanotopographically-modified, microroughened titanium-aluminum-vanadium alloy surfaces Biomaterials 33 2012 8986 8994
118. R.A. Gittens, R. Olivares-Navarrete, A. Cheng, D.M. Anderson, T. McLachlan, and I. Stephan et al. The roles of titanium surface micro/nanotopography and wettability on the differential response of human osteoblast lineage cells Acta Biomater 9 2013 6268 6277