Surface modification of biomedical and dental implants and the processes of inflammation, wound healing and bone formation

International Journal of Molecular Sciences

Volumn 11, Issue 1, 2010, Pages 354-369

  Stanford, Clark M ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

Implant; Macrophage; Surfaces; Wound healing

Indexed keywords

BIOMEDICINE; BONE TURNOVER; CELL DIFFERENTIATION; IMPLANT; INFLAMMATION; MACROPHAGE ACTIVATION; NECROSIS; OSSIFICATION; OSTEOBLAST; REVIEW; TOOTH IMPLANTATION; TOPOGRAPHY; WOUND HEALING;

IMPLANT; MACROPHAGE; SURFACES; WOUND HEALING;

DENTAL IMPLANTS; HUMANS; INFLAMMATION; OSTEOGENESIS; PROSTHESES AND IMPLANTS; SURFACE PROPERTIES; TITANIUM; WOUND HEALING;

EID: 75349093042     PISSN: None     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms11010354     Document Type: Review

References (122)

1. Roos, J.; Sennerby, L.; Albrektsson, T. An update on the clinical documentation on currently used bone anchored endosseous oral implants. Dent. Update 1997, 24, 194-200.
2. Stanford, C.M.; Brand, R.A. Toward an understanding of implant occlusion and strain adaptive bone modeling and remodeling. J. Prosth. Dent. 1999, 81, 553-561.
3. Albrektsson, T.; Sennerby, L. State of the art in oral implants. J. Clin. Periodontol. 1991, 18, 474-481.
4. Smith, D.E.; Zarb, G.A. Criteria for success of osseointegrated endosseous implants. J. Prosth. Dent. 1989, 62, 567-572.
5. Widmark, G.; Andersson, B.; Carlsson, G.E.; Lindvall, A.M.; Ivanoff, C.J. Rehabilitation of patients with severely resorbed maxillae by means of implants with or without bone grafts: A 3-to 5-year follow-up clinical report. Int. J. Oral Maxillofac. Implants 2001, 16, 73-79.
6. Berglundh, T.; Abrahamsson, I.; Lindhe, J. Bone reactions to longstanding functional load at implants: An experimental study in dogs. J. Clin. Periodontol. 2005, 32, 925-932.
7. Fransson, C.; Lekholm, U.; Jemt, T.; Berglundh, T. Prevalence of subjects with progressive bone loss at implants. Clin. Oral Implant. Res. 2005, 16, 440-446.
8. Lang, N.P.; Berglundh, T.; Heitz-Mayfield, L.J.; Pjetursson, B.E.; Salvi, G.E.; Sanz, M. Consensus statements and recommended clinical procedures regarding implant survival and complications. Int. J. Oral Maxillofac. Implants 2004, 19 (Suppl. 1), 150-154.
9. Berglundh, T.; Persson, L.; Klinge, B. A systematic review of the incidence of biological and technical complications in implant dentistry reported in prospective longitudinal studies of at least 5 years. J. Clin. Periodontol. 2002, 29 (Suppl. 3), 197-212.
10. Renvert, S.; Roos-Jansaker, A.M.; Lindahl, C.; Renvert, H.; Rutger Persson, G. Infection at titanium implants with or without a clinical diagnosis of inflammation. Clin. Oral Implant. Res. 2007, 18, 509-516.
11. Roos-Jansaker, A.M.; Renvert, H.; Lindahl, C.; Renvert, S. Nine- to fourteen-year follow-up of implant treatment. Part III: Factors associated with peri-implant lesions. J. Clin. Periodontol. 2006, 33, 296-301.
12. Roos-Jansaker, A.M.; Lindahl, C.; Renvert, H.; Renvert, S. Nine- to fourteen-year follow-up of implant treatment. Part II: Presence of peri-implant lesions. J. Clin. Periodontol. 2006, 33, 290-295.
13. Roos-Jansaker, A.M.; Lindahl, C.; Renvert, H.; Renvert, S. Nine- to fourteen-year follow-up of implant treatment. Part I: Implant loss and associations to various factors. J. Clin. Periodontol. 2006, 33, 283-289.
14. Stanford, C.M. Biomechanical and functional behavior of implants. Adv. Dent. Res. 1999, 13, 88-92.
15. Hansson, S. The implant neck: Smooth or provided with retention elements-A biomechanical approach. Clin. Oral Implant. Res. 1999, 10, 394-405.
16. Binon, P.P. Implants and components: Entering the new millennium. Int. J. Oral Maxillofac. Implants 2000, 15, 76-94.
17. Lindh, T.; Gunne, J.; Tillberg, A.; Molin, M. A meta-analysis of implants in partial edentulism. Clin. Oral Implant. Res. 1998, 9, 80-90.
18. Deporter, D.A.; Friedland, B.; Watson, P.A.; Pilliar, R.M.; Howley, T.P.; Abdulla, D.; Melcher, A.H.; Smith, D.C. A clinical and radiographic assessment of a porous-surfaced, titanium alloy dental implant system in dogs. J. Dent. Res. 1986, 65, 1071-1077.
19. Lowenberg, B.F.; Pilliar, R.M.; Aubin, J.E.; Fernie, G.R.; Melcher, A.H. Migration, attachment, and orientation of human gingival fibroblasts to root slices, naked and porous-surfaced titanium alloy discs, and Zircalloy 2 discs in vitro. J. Dent. Res. 1987, 66, 1000-1005.
20. Deporter, D.A.; Watson, P.A.; Pilliar, R.M.; Chipman, M.L.; Valiquette, N. A histological comparison in the dog of porous-coated vs. threaded dental implants. J. Dent. Res. 1990, 69, 1138-1145.
21. Pilliar, R.M. Dental implants: Materials and design. J. Can. Dent. Assoc. 1990, 56, 857-861.
22. Pilliar, R.M.; Deporter, D.A.; Watson, P.A.; Valiquette, N. Dental implant design-effect on bone remodeling. J. Biomed. Mater. Res. 1991, 25, 467-483.
23. Deporter, D.A.; Watson, P.A.; Booker, D. Simplifying the treatment of edentulism: A new type of implant. J. Am. Dent. Assoc. 1996, 127, 1343-1349.
24. Vaillancourt, H.; Pilliar, R.M.; McCammond, D. Factors affecting crestal bone loss with dental implants partially covered with a porous coating: A finite element analysis. Int. J. Oral Maxillofac. Implants 1996, 11, 351-359.
25. Pilliar, R.M. Overview of surface variability of metallic endosseous dental implants: Textured and porous surface-structured designs. Implant Dent. 1998, 7, 305-314.
26. Stanford, C.M. The role of opinion. J. Am. Dent. Assoc. 2007, 138, 574-576.
27. Slaets, E.; Naert, I.; Carmeliet, G.; Duyck, J. Early cortical bone healing around loaded titanium implants: A histological study in the rabbit. Clin. Oral Implant. Res. 2009, 20, 126-134.
28. Sims, N.A.; Gooi, J.H. Bone remodeling: Multiple cellular interactions required for coupling of bone formation and resorption. Semin. Cell Dev. Biol. 2008, 19, 444-451.
29. Wikesjo, U.M.; Qahash, M.; Polimeni, G.; Susin, C.; Shanaman, R.H.; Rohrer, M.D.; Wozney, J.M.; Hall, J. Alveolar ridge augmentation using implants coated with recombinant human bone morphogenetic protein-2: Histologic observations. J. Clin. Periodontol. 2008, 35, 1001-1010.
30. Leknes, K. N.; Yang, J.; Qahash, M.; Polimeni, G.; Susin, C.; Wikesjo, U.M. Alveolar ridge augmentation using implants coated with recombinant human bone morphogenetic protein-2: Radiographic observations. Clin. Oral Implant. Res. 2008, 19, 1027-1133.
31. Wennerberg, A.; Albrektsson, T. Suggested guidelines for the topographic evaluation of implant surfaces. Int. J. Oral Maxillofac. Implants 2000, 15, 331-344.
32. Wennerberg, A.; Ektessabi, A.; Albrektsson, T.; Johansson, C.; Andersson, B. A 1-year follow-up of implants of differing surface roughness placed in rabbit bone. Int. J. Oral Maxillofac. Implants 1997, 12, 486-494.
33. Hansson, S. The implant neck: Smooth or provided with retention elements. A biomechanical approach. Clin. Oral Implant. Res. 1999, 10, 394-405.
34. Hansson, S. Surface roughness parameters as predictors of anchorage strength in bone: A critical analysis. J. Biomech. 2000, 33, 1297-1303.
35. Buser, D.; Schenk, R.K.; Steinemann, S.; Fiorellini, J.P.; Fox, C.H.; Stich, H. Influence of surface characteristics on bone integration of titanium implants. A histomorphometric study in miniature pigs [see comments]. J. Biomed. Mater. Res. 1991, 25, 889-902.
36. Wennerberg, A.; Johansson, C.B.; Ellingson, J.E. In Enhanced Fixation to Bone with Flouride Modified Oral Implants; IADR: Washington DC, USA, 2000; p. 254.
37. Brunski, J.B. The new millennium in biomaterials and biomechanics. Int. J. Oral Maxillofac. Implants 2000, 15, 327-328.
38. Kasemo, B.; Lausmaa, J. Material-tissue interfaces: The role of surface properties and processes. Environ. Health Perspect. 1994, 102 (Suppl. 5), 41-45.
39. Larsson, C.; Thomsen, P.; Lausmaa, J.; Rodahl, M.; Kasemo, B.; Ericson, L.E. Bone response to surface modified titanium implants: Studies on electropolished implants with different oxide thicknesses and morphology. Biomaterials 1994, 15, 1062-1074.
40. Sanchez, A.R.; Sheridan, P.J.; Kupp, L.I. Is platelet-rich plasma the perfect enhancement factor? A current review. Int. J. Oral Maxillofac. Implants 2003, 18, 93-103.
41. Christenson, E.M.; Anseth, K.S.; van den Beucken, J.J.; Chan, C.K.; Ercan, B.; Jansen, J.A.; Laurencin, C.T.; Li, W.J.; Murugan, R.; Nair, L.S.; Ramakrishna, S.; Tuan, R.S.; Webster, T.J.; Mikos, A.G. Nanobiomaterial applications in orthopedics. J. Orthop. Res. 2007, 25, 11-22.
42. Thor, A.; Rasmusson, L.; Wennerberg, A.; Thomsen, P.; Hirsch, J.M.; Nilsson, B.; Hong, J. The role of whole blood in thrombin generation in contact with various titanium surfaces. Biomaterials 2007, 28, 966-974.
43. Stanford, C.; Schneider, G.; Masaki, C.; Zaharias, R.; Seabold, D.; Eckdhal, J.; Di Paola, J. Effects of Fluoride-modified titanium dioxide grit blasted implant surfaces on Platelet activation and Osteoblast differentiation. Appl. Osseointegr. Res. 2006, 5, 24-30.
44. Mosser, D.M.; Edwards, J.P. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 2008, 8, 958-969.
45. Tan, K.S.; Qian, L.; Rosado, R.; Flood, P.M.; Cooper, L.F. The role of titanium surface topography on J774A.1 macrophage inflammatory cytokines and nitric oxide production. Biomaterials 2006, 27, 5170-5177.
46. Chehroudi, B.; Ghrebi, S.; Murakami, H.; Waterfield, J.D.; Owen, G.; Brunette, D.M. Bone formation on rough, but not polished, subcutaneously implanted Ti surfaces is preceded by macrophage accumulation. J. Biomed. Mater. Res.: A 2009, doi:10.1002/jbm.a.32587.
47. Cao, S.; Zhang, X.; Edwards, J.P.; Mosser, D.M. NF-kappaB1 (p50) homodimers differentially regulate pro- and anti-inflammatory cytokines in macrophages. J. Biol. Chem. 2006, 281, 26041-26050.
48. Meirelles, L.; Melin, L.; Peltola, T.; Kjellin, P.; Kangasniemi, I.; Currie, F.; Andersson, M.; Albrektsson, T.; Wennerberg, A. Effect of hydroxyapatite and titania nanostructures on early in vivo bone response. Clin. Implant Dent. Relat. Res. 2008, 10, 245-254.
49. Meirelles, L.; Arvidsson, A.; Albrektsson, T.; Wennerberg, A. Increased bone formation to unstable nano rough titanium implants. Clin. Oral Implant. Res. 2007, 18, 326-332.
50. Veis, A.A.; Papadimitriou, S.; Trisi, P.; Tsirlis, A.T.; Parissis, N.A.; Kenealy, J.N. Osseointegration of Osseotite and machined-surfaced titanium implants in membrane-covered critical-sized defects: A histologic and histometric study in dogs. Clin. Oral Implant. Res. 2007, 18, 153-160.
51. Shalabi, M.M.; Gortemaker, A.; Van't Hof, M.A.; Jansen, J.A.; Creugers, N.H. Implant surface roughness and bone healing: A systematic review. J. Dent. Res. 2006, 85, 496-500.
52. + T cells to be sustained during chronic infection. J. Immunol. 2007, 179, 3926-3936.
53. Brandt, E.; Woerly, G.; Younes, A.B.; Loiseau, S.; Capron, M. IL-4 production by human polymorphonuclear neutrophils. J. Leukoc. Biol. 2000, 68, 125-130.
54. Linkhart, T.A.; Mohan, S.; Baylink, D.J. Growth factors for bone growth and repair: IGF, TGF beta and BMP. Bone 1996, 19 (Suppl. 1), 1S-12S.
55. Crowther, M.; Brown, N.J.; Bishop, E.T.; Lewis, C.E. Microenvironmental influence on macrophage regulation of angiogenesis in wounds and malignant tumors. J. Leukoc. Biol. 2001, 70, 478-490.
56. Lewis, J.S.; Lee, J.A.; Underwood, J.C.; Harris, A.L.; Lewis, C.E. Macrophage responses to hypoxia: Relevance to disease mechanisms. J. Leukoc. Biol. 1999, 66, 889-900.
57. Okazaki, T.; Ebihara, S.; Takahashi, H.; Asada, M.; Kanda, A.; Sasaki, H. Macrophage colonystimulating factor induces vascular endothelial growth factor production in skeletal muscle and promotes tumor angiogenesis. J. Immunol. 2005, 174, 7531-7538.
58. Lohmann, C.H.; Schwartz, Z.; Koster, G.; Jahn, U.; Buchhorn, G.H.; MacDougall, M.J.; Casasola, D.; Liu, Y.; Sylvia, V.L.; Dean, D.D.; Boyan, B.D. Phagocytosis of wear debris by osteoblasts affects differentiation and local factor production in a manner dependent on particle composition. Biomaterials 2000, 21, 551-561.
59. Moradian-Oldak, J.; Wen, H.B.; Schneider, G.B.; Stanford, C.M. Tissue engineering strategies for the future generation of dental implants. Periodontol. 2006, 41, 157-176.
60. Stanford, C.M.; Schneider, G.B. Functional behaviour of bone around dental implants. Gerodontology 2004, 21, 71-77.
61. Messer, R.L.; Tackas, G.; Mickalonis, J.; Brown, Y.; Lewis, J.B.; Wataha, J.C. Corrosion of machined titanium dental implants under inflammatory conditions. J. Biomed. Mater. Res.: B 2009, 88, 474-481.
62. Paul, N.E.; Skazik, C.; Harwardt, M.; Bartneck, M.; Denecke, B.; Klee, D.; Salber, J.; Zwadlo-Klarwasser, G. Topographical control of human macrophages by a regularly microstructured polyvinylidene fluoride surface. Biomaterials 2008, 29, 4056-4064.
63. Aubin, J.E.; Liu, F.; Malaval, L.; Gupta, A.K. Osteoblast and chondroblast differentiation. Bone 1995, 17 (Suppl. 2), 77S-83S.
64. Ducy, P.; Zhang, R.; Geoffroy, V.; Ridall, A.L.; Karsenty, G. Osf2/Cbfa1: A transcriptional activator of osteoblast differentiation. Cell 1997, 89, 747-754.
65. Xiao, G.; Wang, D.; Benson, M.D.; Karsenty, G.; Franceschi, R. T. Role of the alpha2-integrin in osteoblast-specific gene expression and activation of the Osf2 transcription factor. J. Biol. Chem. 1998, 273, 32988-32994.
66. Harada, H.; Tagashira, S.; Fujiwara, M.; Ogawa, S.; Katsumata, T.; Yamaguchi, A.; Komori, T.; Nakatsuka, M. Cbfa1 isoforms exert functional differences in osteoblast differentiation. J. Biol. Chem. 1999, 274, 6972-6978.
67. Ducy, P.; Starbuck, M.; Priemel, M.; Shen, J.; Pinero, G.; Geoffroy, V.; Amling, M.; Karsenty, G.A Cbfa1-dependent genetic pathway controls bone formation beyond embryonic development. Gene. Develop. 1999, 13, 1025-1036.
68. Hoshi, K.; Komori, T.; Ozawa, H. Morphological characterization of skeletal cells in Cbfa1-deficient mice. Bone 1999, 25, 639-651.
69. Nakashima, K.; Zhou, X.; Kunkel, G.; Zhang, Z.P.; Deng, J.M.; Behringer, R.R.; de Crombrugghe, B. The novel zinc finger-containing transcription factor Osterix is required for osteoblast differentiation and bone formation. Cell 2002, 108, 17-29.
70. Masaki, C.; Schneider, G.B.; Zaharias, R.; Seabold, D.; Stanford, C. Effects of implant surface microtopography on osteoblast gene expression. Clin. Oral Implant. Res. 2005, 16, 650-656.
71. Mendonca, G.; Mendonca, D.B.; Simoes, L.G.; Araujo, A.L.; Leite, E.R.; Duarte, W.R.; Cooper, L.F.; Aragao, F.J. Nanostructured alumina-coated implant surface: Effect on osteoblast-related gene expression and bone-to-implant contact in vivo. Int. J. Oral Maxillofac. Implants 2009, 24, 205-215.
72. Mendonca, G.; Mendonca, D.B.; Simoes, L.G.; Araujo, A.L.; Leite, E.R.; Duarte, W.R.; Aragao, F.J.; Cooper, L.F. The effects of implant surface nanoscale features on osteoblast-specific gene expression. Biomaterials 2009, 30, 4053-4062.
73. Valencia, S.; Gretzer, C.; Cooper, L F. Surface nanofeature effects on titanium-adherent human mesenchymal stem cells. Int. J. Oral Maxillofac. Implants 2009, 24, 38-46.
74. Schneider, G.; Burridge, K. Formation of focal adhesions by osteoblasts adhering to different substrata. Exp. Cell Res. 1994, 214, 264-269.
75. Stanford, C.M.; Keller, J.C.; Solursh, M. Bone cell expression on titanium surfaces is altered by sterilization treatments. J. Dent. Res. 1994, 73, 1061-1071.
76. Boyan, B.D.; Lohmann, C.H.; Dean, D.D.; Sylvia, V.L.; Cochran, D.L.; Schwartz, Z. Mechanisms involved in osteoblast response to implant surface morphology. Annu. Rev. Mater. Res. 2001, 31, 357-371.
77. Boyan, B.D.; Sylvia, V.L.; Liu, Y.; Sagun, R.; Cochran, D.L.; Lohmann, C.H.; Dean, D.D.; Schwartz, Z. Surface roughness mediates its effects on osteoblasts via protein kinase A and phospholipase A2. Biomaterials 1999, 20, 2305-2310.
78. Isa, Z.M.; Schneider, G.B.; Zaharias, R.; Seabold, D.; Stanford, C.M. Effects of fluoride-modified titanium surfaces on osteoblast proliferation and gene expression. Int. J. Oral. Maxillofac. Implants 2006, 21, 203-211.
79. Schneider, G.B.; Zaharias, R.; Seabold, D.; Keller, J.; Stanford, C. Differentiation of preosteoblasts is affected by implant surface microtopographies. J. Biomed. Mater. Res.: A 2004, 69, 462-468.
80. Boyan, B.D.; Batzer, R.; Kieswetter, K.; Liu, Y.; Cochran, D.L.; Szmuckler-Moncler, S.; Dean, D.D.; Schwartz, Z. Titanium surface roughness alters responsiveness of MG63 osteoblast-like cells to 1 alpha,25-(OH)2D3. J. Biomed. Mater. Res. 1998, 39, 77-85.
81. Kokubu, E.; Hamilton, D.W.; Inoue, T.; Brunette, D.M. Modulation of human gingival fibroblast adhesion, morphology, tyrosine phosphorylation, and ERK 1/2 localization on polished, grooved and SLA substratum topographies. J. Biomed. Mater. Res.: A 2009, 91, 663-670.
82. Vercaigne, S.; Wolke, J.G.; Naert, I.; Jansen, J.A. Bone healing capacity of titanium plasmasprayed and hydroxylapatite-coated oral implants. Clin. Oral Implant. Res. 1998, 9, 261-271.
83. Deporter, D.A.; Watson, P.A.; Pilliar, R.M.; Pharoah, M.; Smith, D.C.; Chipman, M.; Locker, D.; Rydall, A. A prospective clinical study in humans of an endosseous dental implant partially covered with a powder-sintered porous coating: 3- to 4-year results. Int. J. Oral Maxillofac. Implants 1996, 11, 87-95.
84. Buser, D.; Weber, H.P.; Bragger, U.; Balsiger, C. Tissue integration of one-stage ITI implants: 3-year results of a longitudinal study with Hollow-Cylinder and Hollow-Screw implants. Int. J. Oral Maxillofac. Implants 1991, 6, 405-412.
85. Buser, D.; Weber, H.P.; Bragger, U.; Balsiger, C. Tissue integration of one-stage implants: Three-year results of a prospective longitudinal study with hollow cylinder and hollow screw implants. Quintessence Int. 1994, 25, 679-686.
86. Buser, D.; Dula, K.; Lang, N.P.; Nyman, S. Long-term stability of osseointegrated implants in bone regenerated with the membrane technique. 5-year results of a prospective study with 12 implants. Clin. Oral Implant. Res. 1996, 7, 175-183.
87. Buser, D.; Belser, U.C.; Lang, N.P. The original one-stage dental implant system and its clinical application. Periodontology 2000, 17, 106-118.
88. Cochran, D.L. A comparison of endosseous dental implant surfaces. J. Periodontol. 1999, 70, 1523-1539.
89. Buser, D.; Broggini, N.; Wieland, M.; Schenk, R.K.; Denzer, A.J.; Cochran, D.L.; Hoffmann, B.; Lussi, A.; Steinemann, S.G. Enhanced bone apposition to a chemically modified SLA titanium surface. J. Dent. Res. 2004, 83, 529-533.
90. Blomqvist, J.E.; Alberius, P.; Isaksson, S.; Linde, A.; Hansson, B.G. Factors in implant integration failure after bone grafting: An osteometric and endocrinologic matched analysis. Int. J. Oral Maxillofac. Surg. 1996, 25, 63-68.
91. Hansson, S.; Norton, M. The relation between surface roughness and interfacial shear strength for bone-anchored implants. A mathematical model. J. Biomech. 1999, 32, 829-836.
92. 2 grit-blasted c.p. titanium endosseous implants. Biomaterials 2006, 27, 926-936.
93. Park, J.Y.; Gemmelll, C.H.; Davies, J.E. Platelet interactions with titanium: Modulation of platelet activity by surface topography. Biomaterials 2001, 22, 2671-2682.
94. Park, J.Y.; Davies, J.E. Red blood cell and platelet interactions with titanium implant surfaces. Clin. Oral Implant. Res. 2000, 11, 530-539.
95. Davies, J.E. Mechanisms of endosseous integration. Int. J. Prosthodont. 1998, 11, 391-401.
96. Brunski, J.B.; Slack, J.M. Orthodontic loading of implants: Biomechanical considerations. In Orthodontic Applications Of Osseointegrated Implants; Quintessence Publishing: Chicago, IL, USA, 2000.
97. Puleo, D.A.; Nanci, A. Understanding and controlling the bone-implant interface. Biomaterials 1999, 20, 2311-2321.
98. Puleo, D.A. Release and retention of biomolecules in collagen deposited on orthopedic biomaterials. Artif. Cells Blood Substit. Immobil. Biotechnol. 1999, 27, 65-75.
99. Rezania, A.; Healy, K.E. The effect of peptide surface density on mineralization of a matrix deposited by osteogenic cells. J. Biomed. Mater. Res. 2000, 52, 595-600.
100. Healy, K.E. Molecular engineering of materials for bioreactivity [Review]. Curr. Opin. Solid State Mat. Sci. 1999, 4, 381-387.
101. McFarland, C.D.; Thomas, C.H.; DeFilippis, C.; Steele, J.G.; Healy, K.E. Protein adsorption and cell attachment to patterned surfaces. J. Biomed. Mater. Res. 2000, 49, 200-210.
102. Rezania, A.; Johnson, R.; Lefkow, A.R.; Healy, K.E. Bioactivation of metal oxide surfaces. 1. Surface characterization and cell response. Langmuir 1999, 15, 6931-6939.
103. Rezania, A.; Healy, K.E. Integrin subunits responsible for adhesion of human osteoblast-like cells to biomimetic peptide surfaces. J. Orthopaed. Res. 1999, 17, 615-623.
104. Rezania, A.; Healy, K.E. Biomimetic peptide surfaces that regulate adhesion, spreading, cytoskeletal organization, and mineralization of the matrix deposited by osteoblast-like cells. Biotechnol. Prog. 1999, 15, 19-32.
105. Rezania, A.; Thomas, C.H.; Healy, K.E. A probabilistic approach to measure the strength of bone cell adhesion to chemically modified surfaces. Ann. Biomed. Eng. 1997, 25, 190-203.
106. Thomas, C.H.; McFarland, C.D.; Jenkins, M.L.; Rezania, A.; Steele, J.G.; Healy, K.E. The role of vitronectin in the attachment and spatial distribution of bone-derived cells on materials with patterned surface chemistry. J. Biomed. Mater. Res. 1997, 37, 81-93.
107. Healy, K.E.; Thomas, C.H.; Rezania, A.; Kim, J.E.; McKeown, P.J.; Lom, B.; Hockberger, P.E. Kinetics of bone cell organization and mineralization on materials with patterned surface chemistry. Biomaterials 1996, 17, 195-208.
108. Walboomers, X.F.; Ginsel, L.A.; Jansen, J.A. Early spreading events of fibroblasts on microgrooved substrates. J. Biomed. Mater. Res. 2000, 51, 529-534.
109. Walboomers, X.F.; Croes, H.J.; Ginsel, L.A.; Jansen, J.A. Contact guidance of rat fibroblasts on various implant materials. J. Biomed. Mater. Res. 1999, 47, 204-212.
110. Walboomers, X.F.; Croes, H.J.; Ginsel, L.A.; Jansen, J.A. Growth behavior of fibroblasts on microgrooved polystyrene. Biomaterials 1998, 19, 1861-1868.
111. Walboomers, X.F.; Croes, H.J.; Ginsel, L.A.; Jansen, J.A. Microgrooved subcutaneous implants in the goat. J. Biomed. Mater. Res. 1998, 42, 634-641.
112. Brunette, D.M.; Chehroudi, B. The effects of the surface topography of micromachined titanium substrata on cell behavior in vitro and in vivo. J. Biomech. Eng. 1999, 121, 49-57.
113. 2. J. Biomed. Mater. Res. 1999, 44, 227-242.
114. Meirelles, L.; Albrektsson, T.; Kjellin, P.; Arvidsson, A.; Franke-Stenport, V.; Andersson, M.; Currie, F.; Wennerberg, A. Bone reaction to nano hydroxyapatite modified titanium implants placed in a gap-healing model. J. Biomed. Mater. Res.: A 2008, 87A, 624-631.
115. Meirelles, L.; Arvidsson, A.; Andersson, M.; Kjellin, P.; Albrektsson, T.; Wennerberg, A. Nano hydroxyapatite structures influence early bone formation. J. Biomed. Mater. Res.: A 2008, 87A, 399-307.
116. Webster, T.J.; Ahn, E.S. Nanostructured biomaterials for tissue engineering bone. Adv. Biochem. Eng. Biotechnol. 2007, 103, 275-308.
117. Mendonca, G.; Mendonca, D.B.; Aragao, F.J.; Cooper, L.F. Advancing dental implant surface technology: From micron-to nanotopography. Biomaterials 2008, 29, 3822-3835.
118. Webster, T.J.; Siegel, R.W.; Bizios, R. Design and evaluation of nanophase alumina for orthopaedic/dental applications. Nanostruct. Mater. 1999, SI, 983-986.
119. Webster, T.J.; Ergun, C.; Doremus, R.H.; Siegel, R.W.; Bizios, R. Specific proteins mediate enhanced osteoblast adhesion on nanophase ceramics. J. Biomed. Mater. Res.: A. 2000, 51, 475-483.
120. 2 nanotubes functionalized with regions of bone morphogenetic protein-2 increases osteoblast adhesion. J. Biomed. Mater. Res.: A 2007, 84A, 447-453.
121. Sato, M.; Aslani, A.; Sambito, M.A.; Kalkhoran, N.M.; Slamovich, E.B.; Webster, T.J. Nanocrystalline hydroxyapatite/titania coatings on titanium improves osteoblast adhesion. J. Biomed. Mater. Res.: A 2007, 84A, 265-272.
122. Balasundaram, G.; Webster, T.J. An overview of nano-polymers for orthopedic applications. Macromol.Biosci. 2007, 7, 635-662.