Evaluation of functional dynamics during osseointegration and regeneration associated with oral implants

Clinical Oral Implants Research

Volumn 21, Issue 1, 2010, Pages 1-12

  Chang, Po Chun ^a,b,c   Lang, Niklaus P ^d   Giannobile, William V ^a,b  

^a UNIVERSITY OF MICHIGAN SCHOOL OF DENTISTRY   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Bone implant interactions; Finite element analysis; Growth factor

Indexed keywords

SIGNAL PEPTIDE;

ANIMAL; ARTICLE; BIOMECHANICS; BONE REGENERATION; FINITE ELEMENT ANALYSIS; HUMAN; PHYSIOLOGY; SURFACE PROPERTY; TOOTH IMPLANTATION;

ANIMALS; BIOMECHANICS; DENTAL IMPLANTATION, ENDOSSEOUS; DENTAL IMPLANTS; FINITE ELEMENT ANALYSIS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; OSSEOINTEGRATION; SURFACE PROPERTIES;

EID: 72949099261     PISSN: 09057161     EISSN: 16000501     Source Type: Journal    
DOI: 10.1111/j.1600-0501.2009.01826.x     Document Type: Article

References (145)

1. Akça, K., Cehreli, M.C. Iplikcioglu, H. (2003) Evaluation of the mechanical characteristics of the implant-abutment complex of a reduced-diameter morse-taper implant. A nonlinear finite element stress analysis. Clinical Oral Implants Research 14 : 444 454.
2. Akça, K., Chang, T.L., Tekdemir, I. Fanuscu, M.I. (2006) Biomechanical aspects of initial intraosseous stability and implant design: a quantitative micro-morphometric analysis. Clinical Oral Implants Research 17 : 465 472.
3. Alsberg, E., Anderson, K.W., Albeiruti, A., Franceschi, R.T. Mooney, D.J. (2001) Cell-interactive alginate hydrogels for bone tissue engineering. Journal of Dental Research 80 : 2025 2029.
4. Andrades, J.A., Han, B., Becerra, J., Sorgente, N., Hall, F.L. Nimni, M.E. (1999) A recombinant human TGF-beta1 fusion protein with collagen-binding domain promotes migration, growth, and differentiation of bone marrow mesenchymal cells. Experimental Cell Research 250 : 485 498.
5. Andreykiv, A., van Keulen, F. Prendergast, P.J. (2008) Computational mechanobiology to study the effect of surface geometry on peri-implant tissue differentiation. J Biomechanical Engineering 130 : 051015.
6. Anselme, K. Bigerelle, M. (2005) Topography effects of pure titanium substrates on human osteoblast long-term adhesion. Acta Biomaterialia 1 : 211 222.
7. Aparicio, C., Lang, N.P. Rangert, B. (2006) Validity and clinical significance of biomechanical testing of implant/bone interface. Clinical Oral Implants Research 17 (Suppl. 2) : 2 7.
8. Atsumi, M., Park, S.H. Wang, H.L. (2007) Methods used to assess implant stability: current status. International Journal of Oral and Maxillofacial Implants 22 : 743 754.
9. Barboza, E.P., Caula, A.L., Caula Fde, O., de Souza, R.O., Geolas Neto, L., Sorensen, R.G., Li, X.J. Wikesjo, U.M. (2004) Effect of recombinant human bone morphogenetic protein-2 in an absorbable collagen sponge with space-providing biomaterials on the augmentation of chronic alveolar ridge defects. Journal of Periodontology 75 : 702 708.
10. Becker, W., Lynch, S.E., Lekholm, U., Becker, B.E., Caffesse, R., Donath, K. Sanchez, R. (1992) A comparison of ePTFE membranes alone or in combination with platelet-derived growth factors and insulin-like growth factor-I or demineralized freeze-dried bone in promoting bone formation around immediate extraction socket implants. Journal of Periodontology 63 : 929 940.
11. Beer, A., Gahleitner, A., Holm, A., Tschabitscher, M. Homolka, P. (2003) Correlation of insertion torques with bone mineral density from dental quantitative CT in the mandible. Clinical Oral Implants Research 14 : 616 620.
12. Berglundh, T., Abrahamsson, I., Lang, N.P. Lindhe, J. (2003) De novo alveolar bone formation adjacent to endosseous implants. Clinical Oral Implants Research 14 : 251 262.
13. Berzins, A., Shah, B., Weinans, H. Sumner, D.R. (1997) Nondestructive measurements of implant-bone interface shear modulus and effects of implant geometry in pull-out tests. J Biomedical Materials Research 34 : 337 340.
14. Bianchi, J., Fiorellini, J.P., Howell, T.H., Sekler, J., Curtin, H., Nevins, M.L. Friedland, B. (2004) Measuring the efficacy of rhBMP-2 to regenerate bone: a radiographic study using a commercially available software program. International Journal of Periodontics and Restorative Dentistry 24 : 579 587.
15. Bischof, M., Nedir, R., Szmukler-Moncler, S., Bernard, J.P. Samson, J. (2004) Implant stability measurement of delayed and immediately loaded implants during healing. Clinical Oral Implants Research 15 : 529 539.
16. Bowers, K.T., Keller, J.C., Randolph, B.A., Wick, D.G. Michaels, C.M. (1992) Optimization of surface micromorphology for enhanced osteoblast responses in vitro. International Journal of Oral and Maxillofacial Implants 7 : 302 310.
17. Boyne, P.J., Lilly, L.C., Marx, R.E., Moy, P.K., Nevins, M., Spagnoli, D.B. Triplett, R.G. (2005) De novo bone induction by recombinant human bone morphogenetic protein-2 (rhBMP-2) in maxillary sinus floor augmentation. Journal of Oral and Maxillofacial Surgery 63 : 1693 1707.
18. Brånemark, R., Ohrnell, L.O., Nilsson, P. Thomsen, P. (1997) Biomechanical characterization of osseointegration during healing: an experimental in vivo study in the rat. Biomaterials 18 : 969 978. (Pubitemid 27296557)
19. Brånemark, R., Ohrnell, L.O., Skalak, R., Carlsson, L. Branemark, P.I. (1998) Biomechanical characterization of osseointegration: an experimental in vivo investigation in the beagle dog. Journal of Orthopaedic Research 16 : 61 69.
20. Brett, P.M., Harle, J., Salih, V., Mihoc, R., Olsen, I., Jones, F.H. Tonetti, M. (2004) Roughness response genes in osteoblasts. Bone 35 : 124 133.
21. Brunski, J.B. (1992) Biomechanical factors affecting the bone-dental implant interface. Clinical Materials 10 : 153 201.
22. Brunski, J.B., Puleo, D.A. Nanci, A. (2000) Biomaterials and biomechanics of oral and maxillofacial implants: current status and future developments. International Journal of Oral and Maxillofacial Implants 15 : 15 46.
23. Buser, D., Schenk, R.K., Steinemann, S., Fiorellini, J.P., Fox, C.H. Stich, H. (1991) Influence of surface characteristics on bone integration of titanium implants. A histomorphometric study in miniature pigs. Journal of Biomedical Materials Research 25 : 889 902.
24. Chang, P.C., Liu, B.Y., Liu, C.M., Chou, H.H., Ho, M.H., Liu, H.C., Wang, D.M. Hou, L.T. (2007) Bone tissue engineering with novel rhBMP2-PLLA composite scaffolds. Journal of Biomedical Materials Research A 81 : 771 780.
25. Chang, P.C., Seol, Y.J., Cirelli, J.A., Pellegrini, G., Jin, Q., Franco, L.M., Goldstein, S.A., Chandler, L.A., Sosnowski, B. Giannobile, W.V. (2009a) PDGF-B gene therapy accelerates bone engineering and oral implant osseointegration. Gene Therapy 16 : in press.
26. Chang, P.C., Seol, Y.J., Kikuchi, N., Goldstein, S.A. Giannobile, W.V. (2009b) Functional apparent moduli: Indicators to predict dyanmics of oral implant osseointegration. In review.
27. Chang, Y.L., Lew, D., Park, J.B. Keller, J.C. (1999) Biomechanical and morphometric analysis of hydroxyapatite-coated implants with varying crystallinity. Journal of Oral and Maxillofacial Surgery 57 : 1096 1108, discussion 1108-1099.
28. Chaudhary, L.R. Hruska, K.A. (2001) The cell survival signal Akt is differentially activated by PDGF-BB, EGF, and FGF-2 in osteoblastic cells. Journal of Cellular Biochemistry 81 : 304 311.
29. Chen, D., Zhao, M. Mundy, G.R. (2004) Bone morphogenetic proteins. Growth Factors 22 : 233 241.
30. Cho, T.J., Gerstenfeld, L.C. Einhorn, T.A. (2002) Differential temporal expression of members of the transforming growth factor beta superfamily during murine fracture healing. Journal of Bone and Mineral Research 17 : 513 520.
31. Cochran, D.L., Schenk, R., Buser, D., Wozney, J.M. Jones, A.A. (1999) Recombinant human bone morphogenetic protein-2 stimulation of bone formation around endosseous dental implants. Journal of Periodontology 70 : 139 150.
32. Colnot, C., Romero, D.M., Huang, S., Rahman, J., Currey, J.A., Nanci, A., Brunski, J.B. Helms, J.A. (2007) Molecular analysis of healing at a bone-implant interface. Journal of Dental Research 86 : 862 867.
33. Dunn, C.A., Jin, Q., Taba, M. Jr., Franceschi, R.T., Bruce Rutherford, R. Giannobile, W.V. (2005) BMP gene delivery for alveolar bone engineering at dental implant defects. Molecular Therapy 11 : 294 299.
34. Eriksson, R.A., Albrektsson, T. Magnusson, B. (1984) Assessment of bone viability after heat trauma. A histological, histochemical and vital microscopic study in the rabbit. Scandinavian Journal of Plastic and Reconstructive Surgery 18 : 261 268.
35. Ferguson, S.J., Broggini, N., Wieland, M., de Wild, M., Rupp, F., Geis-Gerstorfer, J., Cochran, D.L. Buser, D. (2006) Biomechanical evaluation of the interfacial strength of a chemically modified sandblasted and acid-etched titanium surface. Journal of Biomedical Materials Research A 78 : 291 297.
36. Fiorellini, J.P., Howell, T.H., Cochran, D., Malmquist, J., Lilly, L.C., Spagnoli, D., Toljanic, J., Jones, A. Nevins, M. (2005) Randomized study evaluating recombinant human bone morphogenetic protein-2 for extraction socket augmentation. Journal of Periodontology 76 : 605 613.
37. Franchi, M., Fini, M., Martini, D., Orsini, E., Leonardi, L., Ruggeri, A., Giavaresi, G. Ottani, V. (2005) Biological fixation of endosseous implants. Micron 36 : 665 671.
38. Friberg, B., Sennerby, L., Meredith, N. Lekholm, U. (1999) A comparison between cutting torque and resonance frequency measurements of maxillary implants. A 20-month clinical study. International Journal of Oral and Maxillofacial Surgery 28 : 297 303.
39. Friberg, B., Sennerby, L., Roos, J., Johansson, P., Strid, C.G. Lekholm, U. (1995) Evaluation of bone density using cutting resistance measurements and microradiography: an in vitro study in pig ribs. Clinical Oral Implants Research 6 : 164 171.
40. Futami, T., Fujii, N., Ohnishi, H., Taguchi, N., Kusakari, H., Ohshima, H. Maeda, T. (2000) Tissue response to titanium implants in the rat maxilla: ultrastructural and histochemical observations of the bone-titanium interface. Journal of Periodontology 71 : 287 298.
41. Gabet, Y., Muller, R., Levy, J., Dimarchi, R., Chorev, M., Bab, I. Kohavi, D. (2006) Parathyroid hormone 1-34 enhances titanium implant anchorage in low-density trabecular bone: a correlative micro-computed tomographic and biomechanical analysis. Bone 39 : 276 282.
42. Garcia, A.J. Reyes, C.D. (2005) Bio-adhesive surfaces to promote osteoblast differentiation and bone formation. Journal of Dental Research 84 : 407 413.
43. Geng, J.P., Tan, K.B. Liu, G.R. (2001) Application of finite element analysis in implant dentistry: a review of the literature. Journal of Prosthetic Dentistry 85 : 585 598.
44. Geurs, N.C., Jeffcoat, R.L., McGlumphy, E.A., Reddy, M.S. Jeffcoat, M.K. (2002) Influence of implant geometry and surface characteristics on progressive osseointegration. International Journal of Oral and Maxillofacial Implants 17 : 811 815.
45. Giannobile, W.V., Hernandez, R.A., Finkelman, R.D., Ryan, S., Kiritsy, C.P., D'Andrea, M. Lynch, S.E. (1996) Comparative effects of platelet-derived growth factor-BB and insulin-like growth factor-I, individually and in combination, on periodontal regeneration in Macaca fascicularis. Journal of Periodontal Research 31 : 301 312.
46. Giustina, A., Mazziotti, G. Canalis, E. (2008) Growth hormone, insulin-like growth factors, and the skeleton. Endocrine Reviews 29 : 535 559.
47. Hak, D.J., Makino, T., Niikura, T., Hazelwood, S.J., Curtiss, S. Reddi, A.H. (2006) Recombinant human BMP-7 effectively prevents non-union in both young and old rats. Journal of Orthopaedic Research 24 : 11 20.
48. Hansson, S. Norton, M. (1999) The relation between surface roughness and interfacial shear strength for bone-anchored implants. A mathematical model. Journal of Biomechanics 32 : 829 836.
49. Himmlova, L., Dostalova, T., Kacovsky, A. Konvickova, S. (2004) Influence of implant length and diameter on stress distribution: a finite element analysis. Journal of Prosthetic Dentistry 91 : 20 25.
50. Hoffler, C.E., Moore, K.E., Kozloff, K., Zysset, P.K., Brown, M.B. Goldstein, S.A. (2000) Heterogeneity of bone lamellar-level elastic moduli. Bone 26 : 603 609. (Pubitemid 30301653)
51. Hollinger, J.O., Hart, C.E., Hirsch, S.N., Lynch, S. Friedlaender, G.E. (2008) Recombinant human platelet-derived growth factor: biology and clinical applications. Journal of Bone and Joint Surgery. American volume 90 (Suppl. 1) : 48 54.
52. Hollister, S.J., Brennan, J.M. Kikuchi, N. (1994) A homogenization sampling procedure for calculating trabecular bone effective stiffness and tissue level stress. Journal of Biomechanics 27 : 433 444.
53. Homolka, P., Beer, A., Birkfellner, W., Nowotny, R., Gahleitner, A., Tschabitscher, M. Bergmann, H. (2002) Bone mineral density measurement with dental quantitative CT prior to dental implant placement in cadaver mandibles: pilot study. Radiology 224 : 247 252.
54. Howell, T.H., Fiorellini, J., Jones, A., Alder, M., Nummikoski, P., Lazaro, M., Lilly, L. Cochran, D. (1997) A feasibility study evaluating rhBMP-2/absorbable collagen sponge device for local alveolar ridge preservation or augmentation. International Journal of Periodontics and Restorative Dentistry 17 : 124 139.
55. Hsieh, S.C. Graves, D.T. (1998) Pulse application of platelet-derived growth factor enhances formation of a mineralizing matrix while continuous application is inhibitory. Journal of Cellular Biochemistry 69 : 169 180.
56. Huang, Y.C., Kaigler, D., Rice, K.G., Krebsbach, P.H. Mooney, D.J. (2005) Combined angiogenic and osteogenic factor delivery enhances bone marrow stromal cell-driven bone regeneration. Journal of Bone and Mineral Research 20 : 848 857.
57. Huiskes, R., Van Driel, W.D., Prendergast, P.J. Soballe, K. (1997) A biomechanical regulatory model for periprosthetic fibrous-tissue differentiation. Journal of Material Science. Materials in Medicine 8 : 785 788.
58. Ito, Y., Sato, D., Yoneda, S., Ito, D., Kondo, H. Kasugai, S. (2008) Relevance of resonance frequency analysis to evaluate dental implant stability: simulation and histomorphometrical animal experiments. Clinical Oral Implants Research 19 : 9 14.
59. Itoh, K., Suzuki, S. Kuroda, T. (2003) Effects of local administration of insulin-like growth factor-I on mandibular condylar growth in rats. Journal of Medical and Dental Sciences 50 : 79 85.
60. Jin, Q., Anusaksathien, O., Webb, S.A., Printz, M.A. Giannobile, W.V. (2004) Engineering of tooth-supporting structures by delivery of PDGF gene therapy vectors. Molecular Therapy 9 : 519 526.
61. Johansson, C.B., Han, C.H., Wennerberg, A. Albrektsson, T. (1998) A quantitative comparison of machined commercially pure titanium and titanium-aluminum-vanadium implants in rabbit bone. International Journal of Oral and Maxillofacial Implants 13 : 315 321.
62. Jones, A.A., Buser, D., Schenk, R., Wozney, J. Cochran, D.L. (2006) The effect of rhBMP-2 around endosseous implants with and without membranes in the canine model. Journal of Periodontology 77 : 1184 1193.
63. Joos, U., Wiesmann, H.P., Szuwart, T. Meyer, U. (2006) Mineralization at the interface of implants. International Journal of Oral and Maxillofacial Surgery 35 : 783 790.
64. Jovanovic, S.A., Hunt, D.R., Bernard, G.W., Spiekermann, H., Wozney, J.M. Wikesjo, U.M. (2007) Bone reconstruction following implantation of rhBMP-2 and guided bone regeneration in canine alveolar ridge defects. Clinical Oral Implants Research 18 : 224 230.
65. Jung, R.E., Glauser, R., Scharer, P., Hammerle, C.H., Sailer, H.F. Weber, F.E. (2003) Effect of rhBMP-2 on guided bone regeneration in humans. Clinical Oral Implants Research 14 : 556 568.
66. Junker, R., Dimakis, A., Thoneck, M. Jansen, J. (2009) Effects of implant surface coatings and composition on bone integration. Clinical Oral Implants Research 20 (Suppl. 4) : 187 208.
67. Kasemo, B. Gold, J. (1999) Implant surfaces and interface processes. Advances in Dental Research 13 : 8 20.
68. Kempen, D.H., Lu, L., Heijink, A., Hefferan, T.E., Creemers, L.B., Maran, A., Yaszemski, M.J. Dhert, W.J. (2009) Effect of local sequential VEGF and BMP-2 delivery on ectopic and orthotopic bone regeneration. Biomaterials 30 : 2816 2825.
69. Kieswetter, K., Schwartz, Z., Dean, D.D. Boyan, B.D. (1996) The role of implant surface characteristics in the healing of bone. Critical Reviews in Oral Biology and Medicine 7 : 329 345.
70. Kilpadi, D.V. Lemons, J.E. (1994) Surface energy characterization of unalloyed titanium implants. Journal of Biomedical Materials Research 28 : 1419 1425.
71. Kim, T.N., Balakrishnan, A., Lee, B.C., Kim, W.S., Dvorankova, B., Smetana, K., Park, J.K. Panigrahi, B.B. (2008) In vitro fibroblast response to ultra fine grained titanium produced by a severe plastic deformation process. Journal of Material Science. Materials in Medicine 19 : 553 557.
72. Kitamura, M., Nakashima, K., Kowashi, Y., Fujii, T., Shimauchi, H., Sasano, T., Furuuchi, T., Fukuda, M., Noguchi, T., Shibutani, T., Iwayama, Y., Takashiba, S., Kurihara, H., Ninomiya, M., Kido, J., Nagata, T., Hamachi, T., Maeda, K., Hara, Y., Izumi, Y., Hirofuji, T., Imai, E., Omae, M., Watanuki, M. Murakami, S. (2008) Periodontal tissue regeneration using fibroblast growth factor-2: randomized controlled phase II clinical trial. PLoS ONE 3 : e2611.
73. Kitsugi, T., Nakamura, T., Oka, M., Yan, W.Q., Goto, T., Shibuya, T., Kokubo, T. Miyaji, S. (1996) Bone bonding behavior of titanium and its alloys when coated with titanium oxide (TiO2) and titanium silicate (Ti5Si3). Journal of Biomedical Materials Research 32 : 149 156.
74. Knabe, C., Howlett, C.R., Klar, F. Zreiqat, H. (2004) The effect of different titanium and hydroxyapatite-coated dental implant surfaces on phenotypic expression of human bone-derived cells. Journal of Biomedical Materials Research A 71 : 98 107.
75. Kono, S.J., Oshima, Y., Hoshi, K., Bonewald, L.F., Oda, H., Nakamura, K., Kawaguchi, H. Tanaka, S. (2007) Erk pathways negatively regulate matrix mineralization. Bone 40 : 68 74.
76. Ladd, A.J. Kinney, J.H. (1998) Numerical errors and uncertainties in finite-element modeling of trabecular bone. Journal of Biomechanics 31 : 941 945.
77. Lan, J., Wang, Z., Wang, Y., Wang, J. Cheng, X. (2006) The effect of combination of recombinant human bone morphogenetic protein-2 and basic fibroblast growth factor or insulin-like growth factor-I on dental implant osseointegration by confocal laser scanning microscopy. Journal of Periodontology 77 : 357 363.
78. Lang, N.P. Jepsen, S. (2009) Implant surfaces and design. Consensus report of working group 4. Clinical Oral Implants Research 20 (Suppl. 4) : 230 233.
79. Lee, J.J., Rouhfar, L. Beirne, O.R. (2000a) Survival of hydroxyapatite-coated implants: a meta-analytic review. Journal of Oral and Maxillofacial Surgery 58 : 1372 1379, discussion 1379-1380.
80. Lee, Y.M., Park, Y.J., Lee, S.J., Ku, Y., Han, S.B., Klokkevold, P.R. Chung, C.P. (2000b) The bone regenerative effect of platelet-derived growth factor-BB delivered with a chitosan/tricalcium phosphate sponge carrier. Journal of Periodontology 71 : 418 424.
81. Le Guehennec, L., Soueidan, A., Layrolle, P. Amouriq, Y. (2007) Surface treatments of titanium dental implants for rapid osseointegration. Dental Materials 23 : 844 854.
82. Lioubavina-Hack, N., Lang, N.P. Karring, T. (2006) Significance of primary stability for osseointegration of dental implants. Clinical Oral Implants Research 17 : 244 250.
83. Lütolf, M.P., Weber, F.E., Schmoekel, H.G., Schense, J.C., Kohler, T., Muller, R. Hubbell, J.A. (2003) Repair of bone defects using synthetic mimetics of collagenous extracellular matrices. Nature Biotechnology 21 : 513 518.
84. Lynch, S.E., Buser, D., Hernandez, R.A., Weber, H.P., Stich, H., Fox, C.H. Williams, R.C. (1991) Effects of the platelet-derived growth factor/insulin-like growth factor-I combination on bone regeneration around titanium dental implants. Results of a pilot study in beagle dogs. Journal of Periodontology 62 : 710 716.
85. Lynch, S.E., Colvin, R.B. Antoniades, H.N. (1989a) Growth factors in wound healing. Single and synergistic effects on partial thickness porcine skin wounds. Journal of Clinical Investigations 84 : 640 646.
86. Lynch, S.E., Williams, R.C., Polson, A.M., Howell, T.H., Reddy, M.S., Zappa, U.E. Antoniades, H.N. (1989b) A combination of platelet-derived and insulin-like growth factors enhances periodontal regeneration. Journal of Clinical Periodontology 16 : 545 548.
87. Macdonald, K.K., Cheung, C.Y. Anseth, K.S. (2007) Cellular delivery of TGFbeta1 promotes osteoinductive signalling for bone regeneration. Journal of Tissue Engineering and Regenerative Medicine 1 : 314 317.
88. Marco, F., Milena, F., Gianluca, G. Vittoria, O. (2005) Peri-implant osteogenesis in health and osteoporosis. Micron 36 : 630 644.
89. Marie, P.J. (2003) Fibroblast growth factor signaling controlling osteoblast differentiation. Gene 316 : 23 32.
90. Matin, K., Nakamura, H., Irie, K., Ozawa, H. Ejiri, S. (2001) Impact of recombinant human bone morphogenetic protein-2 on residual ridge resorption after tooth extraction: an experimental study in the rat. International Journal of Oral and Maxillofacial Implants 16 : 400 411.
91. Mellal, A., Wiskott, H.W., Botsis, J., Scherrer, S.S. Belser, U.C. (2004) Stimulating effect of implant loading on surrounding bone. Comparison of three numerical models and validation by in vivo data. Clinical Oral Implants Research 15 : 239 248.
92. Meredith, N., Shagaldi, F., Alleyne, D., Sennerby, L. Cawley, P. (1997) The application of resonance frequency measurements to study the stability of titanium implants during healing in the rabbit tibia. Clinical Oral Implants Research 8 : 234 243.
93. Meyer, U., Joos, U., Mythili, J., Stamm, T., Hohoff, A., Fillies, T., Stratmann, U. Wiesmann, H.P. (2004) Ultrastructural characterization of the implant/bone interface of immediately loaded dental implants. Biomaterials 25 : 1959 1967.
94. Misra, R.D., Thein-Han, W.W., Pesacreta, T.C., Hasenstein, K.H., Somani, M.C. Karjalainen, L.P. (2009) Cellular response of preosteoblasts to nanograined/ultrafine-grained structures. Acta Biomaterialia 5 : 1455 1467.
95. Molly, L. (2006) Bone density and primary stability in implant therapy. Clinical Oral Implants Research 17 (Suppl. 2) : 124 135.
96. Morgan, E.F., Bayraktar, H.H., Yeh, O.C., Majumdar, S., Burghardt, A. Keaveny, T.M. (2004) Contribution of inter-site variations in architecture to trabecular bone apparent yield strains. Journal of Biomechanics 37 : 1413 1420.
97. Motoyoshi, M., Yoshida, T., Ono, A. Shimizu, N. (2007) Effect of cortical bone thickness and implant placement torque on stability of orthodontic mini-implants. International Journal of Oral and Maxillofacial Implants 22 : 779 784.
98. Mukherjee, A. Rotwein, P. (2009) Akt promotes BMP2-mediated osteoblast differentiation and bone development. Journal of Cell Science 122 : 716 726.
99. Nakashima, M. Reddi, A.H. (2003) The application of bone morphogenetic proteins to dental tissue engineering. Nature Biotechnology 21 : 1025 1032.
100. Nash, T.J., Howlett, C.R., Martin, C., Steele, J., Johnson, K.A. Hicklin, D.J. (1994) Effect of platelet-derived growth factor on tibial osteotomies in rabbits. Bone 15 : 203 208.
101. Natali, A.N., Pavan, P.G. Ruggero, A.L. (2006) Analysis of bone-implant interaction phenomena by using a numerical approach. Clinical Oral Implants Research 17 : 67 74.
102. Nevins, M., Giannobile, W.V., McGuire, M.K., Kao, R.T., Mellonig, J.T., Hinrichs, J.E., McAllister, B.S., Murphy, K.S., McClain, P.K., Nevins, M.L., Paquette, D.W., Han, T.J., Reddy, M.S., Lavin, P.T., Genco, R.J. Lynch, S.E. (2005) Platelet-derived growth factor stimulates bone fill and rate of attachment level gain: results of a large multicenter randomized controlled trial. Journal of Periodontology 76 : 2205 2215.
103. Nevins, M., Kirker-Head, C., Nevins, M., Wozney, J.A., Palmer, R. Graham, D. (1996) Bone formation in the goat maxillary sinus induced by absorbable collagen sponge implants impregnated with recombinant human bone morphogenetic protein-2. International Journal of Periodontics and Restorative Dentistry 16 : 8 19.
104. Ng, F., Boucher, S., Koh, S., Sastry, K.S., Chase, L., Lakshmipathy, U., Choong, C., Yang, Z., Vemuri, M.C., Rao, M.S. Tanavde, V. (2008) PDGF, TGF-beta, and FGF signaling is important for differentiation and growth of mesenchymal stem cells (MSCs): transcriptional profiling can identify markers and signaling pathways important in differentiation of MSCs into adipogenic, chondrogenic, and osteogenic lineages. Blood 112 : 295 307.
105. Niimi, A., Ozeki, K., Ueda, M. Nakayama, B. (1997) A comparative study of removal torque of endosseous implants in the fibula, iliac crest and scapula of cadavers: preliminary report. Clinical Oral Implants Research 8 : 286 289.
106. Oates, T.W., Rouse, C.A., Cochran, D.L. (1993) Mitogenic effects of growth factors on human periodontal ligament cells in vitro. Journal of Periodontology 64 : 142 148.
107. Oates, T.W., Dowell, S., Robinson, M. McMahan, C.A. (2009) Glycemic control and implant stabilization in type 2 diabetes mellitus. Journal of Dental Research 88 : 367 371.
108. Olive, J. Aparicio, C. (1990) Periotest method as a measure of osseointegrated oral implant stability. International Journal of Oral and Maxillofacial Implants 5 : 390 400.
109. O'Sullivan, D., Sennerby, L. Meredith, N. (2000) Measurements comparing the initial stability of five designs of dental implants: a human cadaver study. Clinical Implant Dentistry and Related Research 2 : 85 92.
110. Park, J.B., Matsuura, M., Han, K.Y., Norderyd, O., Lin, W.L., Genco, R.J. Cho, M.I. (1995) Periodontal regeneration in class III furcation defects of beagle dogs using guided tissue regenerative therapy with platelet-derived growth factor. Journal of Periodontology 66 : 462 477.
111. Park, J.Y. Davies, J.E. (2000) Red blood cell and platelet interactions with titanium implant surfaces. Clinical Oral Implants Research 11 : 530 539.
112. Patel, Z.S., Young, S., Tabata, Y., Jansen, J.A., Wong, M.E. Mikos, A.G. (2008) Dual delivery of an angiogenic and an osteogenic growth factor for bone regeneration in a critical size defect model. Bone 43 : 931 940.
113. Petrie, C.S. Williams, J.L. (2007) Probabilistic analysis of peri-implant strain predictions as influenced by uncertainties in bone properties and occlusal forces. Clinical Oral Implants Research 18 : 611 619.
114. Puckett, S., Pareta, R. Webster, T.J. (2008) Nano rough micron patterned titanium for directing osteoblast morphology and adhesion. International Journal of Nanomedicine 3 : 229 241.
115. Ramp, L.C. Jeffcoat, R.L. (2001) Dynamic behavior of implants as a measure of osseointegration. International Journal of Oral and Maxillofacial Implants 16 : 637 645.
116. Ramseier, C.A., Abramson, Z.R., Jin, Q. Giannobile, W.V. (2006) Gene therapeutics for periodontal regenerative medicine. Dental Clinics of North America 50 : 245 263, ix.
117. Renders, G.A., Mulder, L., Langenbach, G.E., van Ruijven, L.J. van Eijden, T.M. (2008) Biomechanical effect of mineral heterogeneity in trabecular bone. Journal of Biomechanics 41 : 2793 2798.
118. Salmoria, K.K., Tanaka, O.M., Guariza-Filho, O., Camargo, E.S., de Souza, L.T. Maruo, H. (2008) Insertional torque and axial pull-out strength of mini-implants in mandibles of dogs. American Journal of Orthodontics and Dentofacial Orthopedics 133 : 790 e715 790.e722.
119. Scarano, A., Degidi, M., Iezzi, G., Petrone, G. Piattelli, A. (2006) Correlation between implant stability quotient and bone-implant contact: a retrospective histological and histomorphometrical study of seven titanium implants retrieved from humans. Clinical Implant Dentistry and Related Research 8 : 218 222.
120. Schliephake, H., Scharnweber, D., Dard, M., Rossler, S., Sewing, A., Meyer, J. Hoogestraat, D. (2002) Effect of RGD peptide coating of titanium implants on periimplant bone formation in the alveolar crest. An experimental pilot study in dogs. Clinical Oral Implants Research 13 : 312 319.
121. Schulte, W. Lukas, D. (1992) The Periotest method. International Dental Journal 42 : 433 440.
122. Schulte, W. Lukas, D. (1993) Periotest to monitor osseointegration and to check the occlusion in oral implantology. Journal of Oral Implantology 19 : 23 32.
123. Schwartz, Z., Lohmann, C.H., Oefinger, J., Bonewald, L.F., Dean, D.D. Boyan, B.D. (1999) Implant surface characteristics modulate differentiation behavior of cells in the osteoblastic lineage. Advanced Dental Research 13 : 38 48.
124. Seifert, R.A., Hart, C.E., Phillips, P.E., Forstrom, J.W., Ross, R., Murray, M.J. Bowen-Pope, D.F. (1989) Two different subunits associate to create isoform-specific platelet-derived growth factor receptors. Journal of Biological Chemistry 264 : 8771 8778.
125. Sevimay, M., Turhan, F., Kilicarslan, M.A. Eskitascioglu, G. (2005) Three-dimensional finite element analysis of the effect of different bone quality on stress distribution in an implant-supported crown. Journal of Prosthetic Dentistry 93 : 227 234.
126. Shakesheff, K., Cannizzaro, S. Langer, R. (1998) Creating biomimetic micro-environments with synthetic polymer-peptide hybrid molecules. Journal of Biomaterials Science. Polymer Edition 9 : 507 518.
127. Singhatanadgit, W., Salih, V. Olsen, I. (2006) Up-regulation of bone morphogenetic protein receptor IB by growth factors enhances BMP-2-induced human bone cell functions. Journal of Cellular Physiology 209 : 912 922.
128. Stefani, C.M., Machado, M.A., Sallum, E.A., Sallum, A.W., Toledo, S. Nociti, F.H. Jr. (2000) Platelet-derived growth factor/insulin-like growth factor-1 combination and bone regeneration around implants placed into extraction sockets: a histometric study in dogs. Implant Dentistry 9 : 126 131.
129. Sumner, D.R., Turner, T.M., Urban, R.M., Virdi, A.S. Inoue, N. (2006) Additive enhancement of implant fixation following combined treatment with rhTGF-beta2 and rhBMP-2 in a canine model. Journal of Bone and Joint Surgery. American volume 88 : 806 817.
130. Sykaras, N., Iacopino, A.M., Triplett, R.G. Marker, V.A. (2004) Effect of recombinant human bone morphogenetic protein-2 on the osseointegration of dental implants: a biomechanics study. Clinical Oral Investigestions 8 : 196 205.
131. Taba, M. Jr., Jin, Q., Sugai, J.V. Giannobile, W.V. (2005) Current concepts in periodontal bioengineering. Orthodontics and Craniofacial Research 8 : 292 302.
132. Tokunaga, A., Oya, T., Ishii, Y., Motomura, H., Nakamura, C., Ishizawa, S., Fujimori, T., Nabeshima, Y., Umezawa, A., Kanamori, M., Kimura, T. Sasahara, M. (2008) PDGF receptor beta is a potent regulator of mesenchymal stromal cell function. Journal of Bone and Mineral Research 23 : 1519 1528.
133. Tosatti, S., Schwartz, Z., Campbell, C., Cochran, D.L., VandeVondele, S., Hubbell, J.A., Denzer, A., Simpson, J., Wieland, M., Lohmann, C.H., Textor, M. Boyan, B.D. (2004) RGD-containing peptide GCRGYGRGDSPG reduces enhancement of osteoblast differentiation by poly(L-lysine)-graft-poly(ethylene glycol)-coated titanium surfaces. Journal of Biomedical Materials Research A 68 : 458 472.
134. Turkyilmaz, I., Sennerby, L., McGlumphy, E.A. Tozum, T.F. (2009) Biomechanical aspects of primary implant stability: a human cadaver study. Clinical Implant Dentistry and Related Research 11 : 113 119.
135. Turkyilmaz, I., Tozum, T.F., Tumer, C. Ozbek, E.N. (2006) Assessment of correlation between computerized tomography values of the bone, and maximum torque and resonance frequency values at dental implant placement. Journal of Oral Rehabilitation 33 : 881 888.
136. Turkyilmaz, I., Tumer, C., Ozbek, E.N. Tozum, T.F. (2007) Relations between the bone density values from computerized tomography, and implant stability parameters: a clinical study of 230 regular platform implants. Journal of Clinical Periodontology 34 : 716 722.
137. Ueda, M., Matsuki, M., Jacobsson, M. Tjellstrom, A. (1991) Relationship between insertion torque and removal torque analyzed in fresh temporal bone. International Journal of Oral and Maxillofacial Implants 6 : 442 447.
138. van der Linden, J.C., Birkenhager-Frenkel, D.H., Verhaar, J.A. Weinans, H. (2001) Trabecular bone's mechanical properties are affected by its non-uniform mineral distribution. Journal of Biomechanics 34 : 1573 1580.
139. Van Staden, R.C., Guan, H. Loo, Y.C. (2006) Application of the finite element method in dental implant research. Computer Methods in Biomechanics Biomedical Engineering 9 : 257 270.
140. Wang, H.L., Pappert, T.D., Castelli, W.A., Chiego, D.J. Jr., Shyr, Y. Smith, B.A. (1994) The effect of platelet-derived growth factor on the cellular response of the periodontium: an autoradiographic study on dogs. Journal of Periodontology 65 : 429 436.
141. Wennerberg, A. Albrektsson, T. (2009) Effects of titanium surface topography on bone integration. Clinical Oral Implants Research 20 (Suppl. 4) : 174 186.
142. Wennerberg, A., Albrektsson, T. Lausmaa, J. (1996) Torque and histomorphometric evaluation of c.p. titanium screws blasted with 25- and 75-microns-sized particles of Al2O3. Journal of Biomedical Materials Research 30 : 251 260.
143. Xu, Y., James, A.W. Longaker, M.T. (2008) Transforming growth factor-beta1 stimulates chondrogenic differentiation of posterofrontal suture-derived mesenchymal cells in vitro. Plastic and Reconstructive Surgery 122 : 1649 1659.
144. Yang, J. Xiang, H.J. (2007) A three-dimensional finite element study on the biomechanical behavior of an FGBM dental implant in surrounding bone. Journal of Biomechanics 40 : 2377 2385.
145. Yeo, I.S., Han, J.S. Yang, J.H. (2008) Biomechanical and histomorphometric study of dental implants with different surface characteristics. Journal of Biomedical Materials Research B. Applied Biomaterials 87 : 303 311.