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

OBJECTIVES The aim of this paper is to review current investigations on functional assessments of osseointegration and assess correlations to the peri-implant structure. MATERIAL AND METHODS The literature was electronically searched for studies of promoting dental implant osseointegration, functional assessments of implant stability, and finite element (FE) analyses in the field of implant dentistry, and any references regarding biological events during osseointegration were also cited as background information. RESULTS Osseointegration involves a cascade of protein and cell apposition, vascular invasion, de novo bone formation and maturation to achieve the primary and secondary dental implant stability. This process may be accelerated by alteration of the implant surface roughness, developing a biomimetric interface, or local delivery of growth-promoting factors. The current available pre-clinical and clinical biomechanical assessments demonstrated a variety of correlations to the peri-implant structural parameters, and functionally integrated peri-implant structure through FE optimization can offer strong correlation to the interfacial biomechanics. CONCLUSIONS The progression of osseointegration may be accelerated by alteration of the implant interface as well as growth factor applications, and functional integration of peri-implant structure may be feasible to predict the implant function during osseointegration. More research in this field is still needed.

[1]  William V Giannobile,et al.  Platelet-derived growth factor stimulates bone fill and rate of attachment level gain: results of a large multicenter randomized controlled trial. , 2005, Journal of periodontology.

[2]  S. Lynch,et al.  Recombinant human platelet-derived growth factor: biology and clinical applications. , 2008, The Journal of bone and joint surgery. American volume.

[3]  Kozo Nakamura,et al.  Erk pathways negatively regulate matrix mineralization. , 2007, Bone.

[4]  V. Ottani,et al.  Biological fixation of endosseous implants. , 2005, Micron.

[5]  J. Fiorellini,et al.  Randomized study evaluating recombinant human bone morphogenetic protein-2 for extraction socket augmentation. , 2005, Journal of periodontology.

[6]  G. Mazziotti,et al.  Growth hormone, insulin-like growth factors, and the skeleton. , 2008, Endocrine reviews.

[7]  M. Ueda,et al.  Relationship between insertion torque and removal torque analyzed in fresh temporal bone. , 1991, The International journal of oral & maxillofacial implants.

[8]  U. Joos,et al.  Mineralization at the interface of implants. , 2006, International journal of oral and maxillofacial surgery.

[9]  J. Wozney,et al.  The effect of rhBMP-2 around endosseous implants with and without membranes in the canine model. , 2006, Journal of periodontology.

[10]  Antonios G Mikos,et al.  Dual delivery of an angiogenic and an osteogenic growth factor for bone regeneration in a critical size defect model. , 2008, Bone.

[11]  B. B. Panigrahi,et al.  In vitro fibroblast response to ultra fine grained titanium produced by a severe plastic deformation process , 2008, Journal of materials science. Materials in medicine.

[12]  H Weinans,et al.  Trabecular bone's mechanical properties are affected by its non-uniform mineral distribution. , 2001, Journal of biomechanics.

[13]  H. Ozawa,et al.  Impact of recombinant human bone morphogenetic protein-2 on residual ridge resorption after tooth extraction: an experimental study in the rat. , 2001, The International journal of oral & maxillofacial implants.

[14]  C. A. Dunn,et al.  BMP gene delivery for alveolar bone engineering at dental implant defects. , 2005, Molecular therapy : the journal of the American Society of Gene Therapy.

[15]  S. Hansson,et al.  The relation between surface roughness and interfacial shear strength for bone-anchored implants. A mathematical model. , 1999, Journal of biomechanics.

[16]  C. Kirker-Head,et al.  Bone formation in the goat maxillary sinus induced by absorbable collagen sponge implants impregnated with recombinant human bone morphogenetic protein-2. , 1996, The International journal of periodontics & restorative dentistry.

[17]  Jörg Meyer,et al.  Effect of RGD peptide coating of titanium implants on periimplant bone formation in the alveolar crest. An experimental pilot study in dogs. , 2002, Clinical Oral Implants Research.

[18]  T. Turner,et al.  Additive enhancement of implant fixation following combined treatment with rhTGF-beta2 and rhBMP-2 in a canine model. , 2006, The Journal of bone and joint surgery. American volume.

[19]  Rickard Brånemark,et al.  Biomechanical characterization of osseointegration: An experimental in vivo investigation in the beagle dog , 1998, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[20]  K. Anseth,et al.  Cellular delivery of TGFβ1 promotes osteoinductive signalling for bone regeneration , 2007 .

[21]  C. Kiritsy,et al.  Comparative effects of platelet-derived growth factor-BB and insulin-like growth factor-I, individually and in combination, on periodontal regeneration in Macaca fascicularis. , 1996, Journal of periodontal research.

[22]  Shoichi Suzuki,et al.  Effects of local administration of insulin-like growth factor-I on mandibular condylar growth in rats. , 2003, Journal of medical and dental sciences.

[23]  Y. M. Lee,et al.  The bone regenerative effect of platelet-derived growth factor-BB delivered with a chitosan/tricalcium phosphate sponge carrier. , 2000, Journal of periodontology.

[24]  Maxence Bigerelle,et al.  Topography effects of pure titanium substrates on human osteoblast long-term adhesion. , 2005, Acta biomaterialia.

[25]  U. Joos,et al.  Ultrastructural characterization of the implant/bone interface of immediately loaded dental implants. , 2004, Biomaterials.

[26]  P. Layrolle,et al.  Surface treatments of titanium dental implants for rapid osseointegration. , 2007, Dental materials : official publication of the Academy of Dental Materials.

[27]  W Schulte,et al.  The Periotest method. , 1992, International dental journal.

[28]  R. Triplett,et al.  Effect of recombinant human bone morphogenetic protein-2 on the osseointegration of dental implants: a biomechanics study , 2004, Clinical Oral Investigations.

[29]  M. Longaker,et al.  Transforming Growth Factor-β1 Stimulates Chondrogenic Differentiation of Posterofrontal Suture–Derived Mesenchymal Cells In Vitro , 2008, Plastic and reconstructive surgery.

[30]  L Sennerby,et al.  A comparison between cutting torque and resonance frequency measurements of maxillary implants. A 20-month clinical study. , 1999, International journal of oral and maxillofacial surgery.

[31]  William V Giannobile,et al.  Engineering of tooth-supporting structures by delivery of PDGF gene therapy vectors. , 2004, Molecular therapy : the journal of the American Society of Gene Therapy.

[32]  I. Turkyilmaz,et al.  Assessment of correlation between computerized tomography values of the bone, and maximum torque and resonance frequency values at dental implant placement. , 2006, Journal of oral rehabilitation.

[33]  L. Bonewald,et al.  Implant Surface Characteristics Modulate Differentiation Behavior of Cells in the Osteoblastic Lineage , 1999, Advances in dental research.

[34]  J. A. Currey,et al.  Molecular Analysis of Healing at a Bone-Implant Interface , 2007, Journal of dental research.

[35]  Y. Izumi,et al.  Periodontal Tissue Regeneration Using Fibroblast Growth Factor -2: Randomized Controlled Phase II Clinical Trial , 2008, PloS one.

[36]  D. Graves,et al.  Pulse application of platelet‐derived growth factor enhances formation of a mineralizing matrix while continuous application is inhibitory , 1998, Journal of cellular biochemistry.

[37]  J. Fiorellini,et al.  A feasibility study evaluating rhBMP-2/absorbable collagen sponge device for local alveolar ridge preservation or augmentation. , 1997, The International journal of periodontics & restorative dentistry.

[38]  U C Belser,et al.  Stimulating effect of implant loading on surrounding bone. Comparison of three numerical models and validation by in vivo data. , 2004, Clinical oral implants research.

[39]  M. Sevimay,et al.  Three-dimensional finite element analysis of the effect of different bone quality on stress distribution in an implant-supported crown. , 2005, The Journal of prosthetic dentistry.

[40]  R. Colvin,et al.  Growth factors in wound healing. Single and synergistic effects on partial thickness porcine skin wounds. , 1989, The Journal of clinical investigation.

[41]  M. Ueda,et al.  A comparative study of removal torque of endosseous implants in the fibula, iliac crest and scapula of cadavers: preliminary report. , 1997, Clinical oral implants research.

[42]  B. Boyan,et al.  The role of implant surface characteristics in the healing of bone. , 1996, Critical reviews in oral biology and medicine : an official publication of the American Association of Oral Biologists.

[43]  Franchi Marco,et al.  Peri-implant osteogenesis in health and osteoporosis. , 2005, Micron.

[44]  Niklaus P Lang,et al.  De novo alveolar bone formation adjacent to endosseous implants. , 2003, Clinical oral implants research.

[45]  C. Choong,et al.  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. , 2008, Blood.

[46]  Jung-Suk Han,et al.  Biomechanical and histomorphometric study of dental implants with different surface characteristics. , 2008, Journal of biomedical materials research. Part B, Applied biomaterials.

[47]  L Sennerby,et al.  Measurements comparing the initial stability of five designs of dental implants: a human cadaver study. , 2000, Clinical implant dentistry and related research.

[48]  T. Goto,et al.  Bone bonding behavior of titanium and its alloys when coated with titanium oxide (TiO2) and titanium silicate (Ti5Si3). , 1996, Journal of biomedical materials research.

[49]  Jie Yang,et al.  A three-dimensional finite element study on the biomechanical behavior of an FGBM dental implant in surrounding bone. , 2007, Journal of biomechanics.

[50]  H. Maruo,et al.  Insertional torque and axial pull-out strength of mini-implants in mandibles of dogs. , 2008, American journal of orthodontics and dentofacial orthopedics : official publication of the American Association of Orthodontists, its constituent societies, and the American Board of Orthodontics.

[51]  J B Brunski,et al.  Biomechanical factors affecting the bone-dental implant interface. , 1992, Clinical materials.

[52]  Sharmila Majumdar,et al.  Contribution of inter-site variations in architecture to trabecular bone apparent yield strains. , 2004, Journal of biomechanics.

[53]  P J Prendergast,et al.  Computational mechanobiology to study the effect of surface geometry on peri-implant tissue differentiation. , 2008, Journal of biomechanical engineering.

[54]  Q. Jin,et al.  Gene therapeutics for periodontal regenerative medicine. , 2006, Dental clinics of North America.

[55]  J. Fiorellini,et al.  Measuring the efficacy of rhBMP-2 to regenerate bone: a radiographic study using a commercially available software program. , 2004, The International journal of periodontics & restorative dentistry.

[56]  Arturo N Natali,et al.  Analysis of bone-implant interaction phenomena by using a numerical approach. , 2006, Clinical oral implants research.

[57]  伊藤 嘉洋.  Relevance of resonance frequency analysis to evaluate dental implant stability : simulation and histomorphometrical animal experiments , 2006 .

[58]  J. Lan,et al.  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. , 2006, Journal of periodontology.

[59]  Po-Chun Chang,et al.  Bone tissue engineering with novel rhBMP2-PLLA composite scaffolds. , 2007, Journal of biomedical materials research. Part A.

[60]  P Nilsson,et al.  Biomechanical characterization of osseointegration during healing: an experimental in vivo study in the rat. , 1997, Biomaterials.

[61]  Y. Ishii,et al.  PDGF Receptor β Is a Potent Regulator of Mesenchymal Stromal Cell Function , 2008, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[62]  S A Goldstein,et al.  Heterogeneity of bone lamellar-level elastic moduli. , 2000, Bone.

[63]  R. Huiskes,et al.  A biomechanical regulatory model for periprosthetic fibrous-tissue differentiation , 1997, Journal of materials science. Materials in medicine.

[64]  Steven A. Goldstein,et al.  PDGF-B Gene Therapy Accelerates Bone Engineering and Oral Implant Osseointegration , 2009, Gene Therapy.

[65]  L. Molly.  Bone density and primary stability in implant therapy. , 2006, Clinical oral implants research.

[66]  M. Tonetti,et al.  Roughness response genes in osteoblasts. , 2004, Bone.

[67]  Niklaus P Lang,et al.  Implant surfaces and design (Working Group 4). , 2009, Clinical oral implants research.

[68]  U. Wikesjö,et al.  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. , 2004, Journal of periodontology.

[69]  Mihoko Atsumi,et al.  Methods used to assess implant stability: current status. , 2007, The International journal of oral & maxillofacial implants.

[70]  D Buser,et al.  Influence of surface characteristics on bone integration of titanium implants. A histomorphometric study in miniature pigs. , 1991, Journal of biomedical materials research.

[71]  L. P. Karjalainen,et al.  Cellular response of preosteoblasts to nanograined/ultrafine-grained structures. , 2009, Acta biomaterialia.

[72]  L Sennerby,et al.  Evaluation of bone density using cutting resistance measurements and microradiography: an in vitro study in pig ribs. , 1995, Clinical oral implants research.

[73]  L. Chaudhary,et al.  The cell survival signal Akt is differentially activated by PDGF‐BB, EGF, and FGF‐2 in osteoblastic cells , 2001, Journal of cellular biochemistry.

[74]  D. Cochran,et al.  Mitogenic effects of growth factors on human periodontal ligament cells in vitro. , 1993, Journal of periodontology.

[75]  T. Webster,et al.  Nano rough micron patterned titanium for directing osteoblast morphology and adhesion , 2008, International journal of nanomedicine.

[76]  M. Tschabitscher,et al.  Correlation of insertion torques with bone mineral density from dental quantitative CT in the mandible. , 2003, Clinical oral implants research.

[77]  L J van Ruijven,et al.  Biomechanical effect of mineral heterogeneity in trabecular bone. , 2008, Journal of biomechanics.

[78]  G. Liu,et al.  Application of finite element analysis in implant dentistry: a review of the literature. , 2001, The Journal of prosthetic dentistry.

[79]  S. Curtiss,et al.  Recombinant human BMP‐7 effectively prevents non‐union in both young and old rats , 2006, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[80]  P. Marie.  Fibroblast growth factor signaling controlling osteoblast differentiation. , 2003, Gene.

[81]  T Albrektsson,et al.  Assessment of bone viability after heat trauma. A histological, histochemical and vital microscopic study in the rabbit. , 1984, Scandinavian journal of plastic and reconstructive surgery.

[82]  J. B. Park,et al.  Biomechanical and morphometric analysis of hydroxyapatite-coated implants with varying crystallinity. , 1999, Journal of oral and maxillofacial surgery : official journal of the American Association of Oral and Maxillofacial Surgeons.

[83]  Carlos Aparicio,et al.  Validity and clinical significance of biomechanical testing of implant/bone interface. , 2006, Clinical oral implants research.

[84]  I. Tekdemir,et al.  Biomechanical aspects of initial intraosseous stability and implant design: a quantitative micro-morphometric analysis. , 2006, Clinical oral implants research.

[85]  C Aparicio,et al.  Periotest method as a measure of osseointegrated oral implant stability. , 1990, The International journal of oral & maxillofacial implants.

[86]  N. Kikuchi,et al.  A homogenization sampling procedure for calculating trabecular bone effective stiffness and tissue level stress. , 1994, Journal of biomechanics.

[87]  J C Keller,et al.  Optimization of surface micromorphology for enhanced osteoblast responses in vitro. , 1993, The International journal of oral & maxillofacial implants.

[88]  C. R. Howlett,et al.  The effect of different titanium and hydroxyapatite-coated dental implant surfaces on phenotypic expression of human bone-derived cells. , 2004, Journal of biomedical materials research. Part A.

[89]  S. vandeVondele,et al.  RGD-containing peptide GCRGYGRGDSPG reduces enhancement of osteoblast differentiation by poly(L-lysine)-graft-poly(ethylene glycol)-coated titanium surfaces. , 2004, Journal of biomedical materials research. Part A.

[90]  Murat Cavit Cehreli,et al.  Evaluation of the mechanical characteristics of the implant-abutment complex of a reduced-diameter morse-taper implant. A nonlinear finite element stress analysis. , 2003, Clinical oral implants research.

[91]  J. Kinney,et al.  Numerical errors and uncertainties in finite-element modeling of trabecular bone. , 1998, Journal of biomechanics.

[92]  Y C Loo,et al.  Application of finite element method in dental implant research , 2009 .

[93]  Thomas A Einhorn,et al.  Differential Temporal Expression of Members of the Transforming Growth Factor β Superfamily During Murine Fracture Healing , 2002, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[94]  I. Turkyilmaz,et al.  Biomechanical aspects of primary implant stability: a human cadaver study. , 2009, Clinical implant dentistry and related research.

[95]  I. Turkyilmaz,et al.  Relations between the bone density values from computerized tomography, and implant stability parameters: a clinical study of 230 regular platform implants. , 2007, Journal of clinical periodontology.

[96]  L Sennerby,et al.  The application of resonance frequency measurements to study the stability of titanium implants during healing in the rabbit tibia. , 1997, Clinical oral implants research.

[97]  B. Kasemo,et al.  Implant Surfaces and Interface Processes , 1999, Advances in dental research.

[98]  T. Albrektsson,et al.  Torque and histomorphometric evaluation of c.p. titanium screws blasted with 25- and 75-microns-sized particles of Al2O3. , 1996, Journal of biomedical materials research.

[99]  S. Ferguson,et al.  Biomechanical evaluation of the interfacial strength of a chemically modified sandblasted and acid-etched titanium surface. , 2006, Journal of biomedical materials research. Part A.

[100]  J. Wozney,et al.  Bone reconstruction following implantation of rhBMP-2 and guided bone regeneration in canine alveolar ridge defects. , 2007, Clinical oral implants research.

[101]  P. Rotwein,et al.  Akt promotes BMP2-mediated osteoblast differentiation and bone development , 2009, Journal of Cell Science.

[102]  T. Albrektsson,et al.  Effects of titanium surface topography on bone integration: a systematic review. , 2009, Clinical oral implants research.

[103]  R. Müller,et al.  Parathyroid hormone 1-34 enhances titanium implant anchorage in low-density trabecular bone: a correlative micro-computed tomographic and biomechanical analysis. , 2006, Bone.

[104]  D. Mooney,et al.  Combined Angiogenic and Osteogenic Factor Delivery Enhances Bone Marrow Stromal Cell‐Driven Bone Regeneration , 2004, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[105]  R. Genco,et al.  Periodontal regeneration in class III furcation defects of beagle dogs using guided tissue regenerative therapy with platelet-derived growth factor. , 1995, Journal of periodontology.

[106]  Michael J Yaszemski,et al.  Effect of local sequential VEGF and BMP-2 delivery on ectopic and orthotopic bone regeneration. , 2009, Biomaterials.

[107]  Myron Nevins,et al.  De novo bone induction by recombinant human bone morphogenetic protein-2 (rhBMP-2) in maxillary sinus floor augmentation. , 2005, Journal of oral and maxillofacial surgery : official journal of the American Association of Oral and Maxillofacial Surgeons.

[108]  Edwin A McGlumphy,et al.  Influence of implant geometry and surface characteristics on progressive osseointegration. , 2002, The International journal of oral & maxillofacial implants.

[109]  C. D. Reyes,et al.  Bio-adhesive Surfaces to Promote Osteoblast Differentiation and Bone Formation , 2005, Journal of dental research.

[110]  V. Salih,et al.  Up‐regulation of bone morphogenetic protein receptor IB by growth factors enhances BMP‐2‐induced human bone cell functions , 2006, Journal of cellular physiology.

[111]  Jean-Pierre Bernard,et al.  Implant stability measurement of delayed and immediately loaded implants during healing. , 2004, Clinical oral implants research.

[112]  H. Antoniades,et al.  A combination of platelet-derived and insulin-like growth factors enhances periodontal regeneration. , 1989, Journal of clinical periodontology.

[113]  F. Nociti,et al.  Platelet-derived growth factor/insulin-like growth factor-1 combination and bone regeneration around implants placed into extraction sockets: a histometric study in dogs. , 2000, Implant dentistry.

[114]  K. Shakesheff,et al.  Creating biomimetic micro-environments with synthetic polymer-peptide hybrid molecules. , 1998, Journal of biomaterials science. Polymer edition.

[115]  T. Oates,et al.  Glycemic Control and Implant Stabilization in Type 2 Diabetes Mellitus , 2009, Journal of dental research.

[116]  Noboru Kikuchi,et al.  Functional apparent moduli as predictors of oral implant osseointegration dynamics. , 2010, Journal of biomedical materials research. Part B, Applied biomaterials.

[117]  A. Piattelli,et al.  Correlation between implant stability quotient and bone-implant contact: a retrospective histological and histomorphometrical study of seven titanium implants retrieved from humans. , 2006, Clinical implant dentistry and related research.

[118]  C. R. Howlett,et al.  Effect of platelet-derived growth factor on tibial osteotomies in rabbits. , 1994, Bone.

[119]  R. Jung,et al.  Effect of rhBMP-2 on guided bone regeneration in humans. , 2003, Clinical oral implants research.

[120]  Tohru Yoshida,et al.  Effect of cortical bone thickness and implant placement torque on stability of orthodontic mini-implants. , 2007, The International journal of oral & maxillofacial implants.

[121]  J. Davies,et al.  Red blood cell and platelet interactions with titanium implant surfaces. , 2000, Clinical oral implants research.

[122]  S. Lynch,et al.  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. , 1992, Journal of periodontology.

[123]  N. Lang,et al.  Significance of primary stability for osseointegration of dental implants. , 2006, Clinical oral implants research.

[124]  Svatava Konvicková,et al.  Influence of implant length and diameter on stress distribution: a finite element analysis. , 2004, The Journal of prosthetic dentistry.

[125]  S. Lynch,et al.  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. , 1991, Journal of periodontology.

[126]  H. Weinans,et al.  Nondestructive measurements of implant-bone interface shear modulus and effects of implant geometry in pull-out tests. , 1997, Journal of biomedical materials research.

[127]  J. Jansen,et al.  Effects of implant surface coatings and composition on bone integration: a systematic review. , 2009, Clinical oral implants research.

[128]  W. Birkfellner,et al.  Bone mineral density measurement with dental quantitative CT prior to dental implant placement in cadaver mandibles: pilot study. , 2002, Radiology.

[129]  Ralph Müller,et al.  Repair of bone defects using synthetic mimetics of collagenous extracellular matrices , 2003, Nature Biotechnology.

[130]  J. Andrades,et al.  A recombinant human TGF-beta1 fusion protein with collagen-binding domain promotes migration, growth, and differentiation of bone marrow mesenchymal cells. , 1999, Experimental cell research.

[131]  James Laney Williams,et al.  Probabilistic analysis of peri-implant strain predictions as influenced by uncertainties in bone properties and occlusal forces. , 2007, Clinical oral implants research.

[132]  K W Anderson,et al.  Cell-interactive Alginate Hydrogels for Bone Tissue Engineering , 2001, Journal of dental research.

[133]  J. Lemons,et al.  Surface energy characterization of unalloyed titanium implants. , 1994, Journal of biomedical materials research.

[134]  J B Brunski,et al.  Biomaterials and biomechanics of oral and maxillofacial implants: current status and future developments. , 2000, The International journal of oral & maxillofacial implants.

[135]  P. Phillips,et al.  Two different subunits associate to create isoform-specific platelet-derived growth factor receptors. , 1989, The Journal of biological chemistry.

[136]  J. Wozney,et al.  Recombinant human bone morphogenetic protein-2 stimulation of bone formation around endosseous dental implants. , 1999, Journal of periodontology.

[137]  W. Schulte,et al.  Periotest to monitor osseointegration and to check the occlusion in oral implantology. , 1993, The Journal of oral implantology.

[138]  Q. Jin,et al.  Current concepts in periodontal bioengineering. , 2005, Orthodontics & craniofacial research.

[139]  A. Reddi,et al.  The application of bone morphogenetic proteins to dental tissue engineering , 2003, Nature Biotechnology.

[140]  O R Beirne,et al.  Survival of hydroxyapatite-coated implants: a meta-analytic review. , 2000, Journal of oral and maxillofacial surgery : official journal of the American Association of Oral and Maxillofacial Surgeons.

[141]  Y. Shyr,et al.  The effect of platelet-derived growth factor on the cellular response of the periodontium: an autoradiographic study on dogs. , 1994, Journal of periodontology.

[142]  T Albrektsson,et al.  A quantitative comparison of machined commercially pure titanium and titanium-aluminum-vanadium implants in rabbit bone. , 1998, The International journal of oral & maxillofacial implants.

[143]  L. Ramp,et al.  Dynamic behavior of implants as a measure of osseointegration. , 2001, The International Journal of Oral and Maxillofacial Implants.

[144]  N. Fujii,et al.  Tissue response to titanium implants in the rat maxilla: ultrastructural and histochemical observations of the bone-titanium interface. , 2000, Journal of periodontology.