Bioceramic Bone Graft Substitutes: Influence of Porosity and Chemistry
Corresponding Author
Karin A. Hing
IRC in Biomedical Materials, Queen Mary University of London, London E1 4NS, U.K
*[email protected]Search for more papers by this authorCorresponding Author
Karin A. Hing
IRC in Biomedical Materials, Queen Mary University of London, London E1 4NS, U.K
*[email protected]Search for more papers by this authorAbstract
Bioceramics have been considered for use as synthetic bone graft substitutes (BGSs) for over 30 years, throughout which there have been two primary areas of research: (i) optimization of the physical pore structure and (ii) formulation of an appropriate bioceramic chemistry. While it is well recognized that both the rate of integration and the final volume of regenerated bone are primarily dependent on the macroporosity, there still seems to be some dispute regarding the optimum “type” of porosity. The rate and quality of bone integration have, in turn, been related to a dependence on pore size, porosity volume fraction, and interconnection size and interconnection density, both as a function of structural permeability and mechano-transduction. Moreover, the role of strut microstructure and pore geometry have been considered with respect to their influence on entrapment and recruitment of growth factors (GFs) in addition to its influence on scaffold mechanics. Deconvoluting the relative affects of these parameters is complicated by the use of both resorbable and nonresorbable bioactive bioceramics, which are believed to mediate bioactivity in the osseous environment through two principal mechanisms: (i) directly through dissolution and release of ionic products in vivo, elevating local concentrations of soluble species that interact directly with local cells or influence cell behavior by their effect on local pH, (ii) indirectly through the influence that surface chemistry will have on protein adsorption, GF entrapment, and subsequent cell attachment and function. This article aims to review some of the recent developments in bioceramic BGSs, with a view to understanding how the various physiochemical parameters may be optimized to promote bone healing.
References
- 1 P. J. Meeder and C. Eggers, “The History of Autogenous Bone Grafting,”Injury, 25 [Suppl. 1] A2–A3 (1994).
- 2 A. Czitrom and A. Gross, Allografts in Orthopaedic Practice. Williams & Wilkins, Baltimore, 1992.
- 3
J. Wolff, “Uber die innrer Architektur der knochen und ihre Bedeutung fur die Fragen vom Knochenwachsthum,”Virchows Arch. Path. Anat. Physiol., 50
389–450 (1870).
10.1007/BF01944490 Google Scholar
- 4 M. G. Mullender and R. Huiskes, “Osteocytes and Bone Lining Cells: Which are the Best Candidates for Mechano-Sensors in Cancellous Bone?,”Bone, 20 [6] 527–532 (1997).
- 5
D. A. Cameron, “ The Ultrastructure of Bone,” The Biochemistry and Physiology of Bone, 2nd Edition, ed., G. H. Bourne. Academic Press, New York, NY, 191–236, 1972.
10.1016/B978-0-12-119201-3.50013-5 Google Scholar
- 6 D. Togawa, T. W. Bauer, I. H. Lieberman, and H. Sakai, “Lumbar Intervertebral Body Fusion Cages: Histological Evaluation of Clinically Failed Cages Retrieved from Humans,”J. Bone Joint Surg. Am., 86-A [1] 70–79 (2004).
- 7 A. Barriga, P. Diaz-de-Rada, J. L. Barroso, M. Alfonso, M. Lamata, S. Hernaez, J. L. Beguiristain, M. San-Julian, and C. Villas, “Frozen Cancellous Bone Allografts: Positive Cultures of Implanted Grafts in Posterior Fusions of the Spine,”Eur. Spine J., 13 [2] 152–156 (2004).
- 8 S. McCann, J. L. Byrne, M. Rovira, P. Shaw, P. Ribaud, S. Sica, L. Volin, E. Olavarria, S. Mackinnon, P. Trabasso, M. T. VanLint, P. Ljungman, K. Ward, P. Browne, A. Gratwohl, A. F. Widmer, and C. Cordonnier, “Outbreaks of Infectious Diseases in Stem Cell Transplant Units: A Silent Cause of Death for Patients and Transplant Programmes,”Bone Marrow Transplant, 33 [5] 519–529 (2004).
- 9 “Orthopaedics: Key Markets & Emerging Technologies,” Clin. Rep., PJB Publications, Ltd., London (2002).
- 10 A. H. Reddi, “Morphogenesis and Tissue Engineering of Bone and Cartilage: Inductive Signals, Stem Cells, and Biomimetic Biomaterials,”Tissue Eng., 6 [4] 351–359 (2000).
- 11 S. F. Hulbert, F. A. Young, R. S. Mathews, J. J. Klawitter, C. D. Talbert, and F. H. Stelling, “Potential of Ceramic Materials as Permanently Implantable Skeletal Prostheses,”J. Biomed. Mater. Res., 4 [3] 433–456 (1970).
- 12 S. F. Hulbert, S. J. Morrison, and J. J. Klawitter, “Tissue Reaction to Three Ceramics of Porous and Non-Porous Structures,”J. Biomed. Mater. Res., 6 [5] 347–374 (1972).
- 13 J. J. Klawitter, J. G. Bagwell, A. M. Weinstein, and B. W. Sauer, “An Evaluation of Bone Growth Into Porous High Density Polyethylene,”J. Biomed. Mater. Res., 10 [2] 311–323 (1976).
- 14
J. J. Klawitter and
S. F. Hulbert, “Application of Porous Ceramics for the Attachment of Load Bearing Internal Orthopaedic Applications,”J. Biomed. Mater. Res. Symp., 2
[1]
161–229 (1971).
10.1002/jbm.820050613 Google Scholar
- 15 R. S. Ling, A. J. Timperley, and L. Linder, “Histology of Cancellous Impaction Grafting in the Femur. A Case Report,”J. Bone Joint Surg. Br., 75 [5] 693–696 (1993).
- 16 K. Soballe, H. Brockstedt-Rasmussen, E. S. Hansen, and C. Bunger, “Hydroxyapatite Coating Modifies Implant Membrane Formation. Controlled Micromotion Studied in Dogs,”Acta Orthop. Scand., 63 [2] 128–140 (1992).
- 17 P. K. Stephenson, M. A. Freeman, P. A. Revell, J. Germain, M. Tuke, and C. J. Pirie, “The Effect of Hydroxyapatite Coating on Ingrowth of Bone Into Cavities in an Implant,”J. Arthroplasty, 6 [1] 51–58 (1991).
- 18 J. H. Kuhne, R. Bartl, B. Frisch, C. Hammer, V. Jansson, and M. Zimmer, “Bone Formation in Coralline Hydroxyapatite. Effects of Pore Size Studied in Rabbits,”Acta Orthop. Scand., 65 [3] 246–252 (1994).
- 19 R. E. Holmes, “Bone Regeneration Within a Coralline Hydroxyapatite Implant,”Plast. Reconstr. Surg., 63 [5] 626–633 (1979).
- 20 D. M. Liu, “Fabrication of Hydroxyapatite Ceramic with Controlled Porosity,”J. Mater. Sci. Mater. Med., 8 [4] 227–232 (1997).
- 21 F. C. M. Driessens, “ Formation and Stability of Calcium Phosphates in Relation to the Phase Composition of the Mineral in Calcified Tissue,” Bioceramics of Calcium Phosphates. ed., K. DeGroot. CRC Press, Florida, 2–32, 1983.
- 22 J. G. J. Peelen, B. V. Rejda, and K. DeGroot, “Preparation and Properties of Sintered Hydroxyapatite,”Ceramiurgica Int., 4 [2] 71–74 (1978).
- 23 A. Slosarczyk, “Highly Porous Hydroxyapatite Material,”Powder Metall. Int., 21 [4] 24–25 (1989).
- 24 D. M. Roy and S. K. Linnehan, “Hydroxyapatite Formed from Coral Skeletal Carbonate by Hydrothermal Exchange,”Nature, 247 [438] 220–222 (1974).
- 25 M. Dard, A. Bauer, A. Liebendorger, H. Wahlig, and E. Dingeldein, “Preparation Physiochemical and Biological Evaluation of a Hydroxyapatite Ceramic from Bovine Spongiosa,”Acta Odontol. Stomat., 185 61–66 (1994).
- 26 R. Holmes, V. Mooney, R. Bucholz, and A. Tencer, “A Coralline Hydroxyapatite Bone Graft Substitute. Preliminary Report,”Clin. Orthop., [188] 252–262 (1984).
- 27 K. A. Hing, S. M. Best, and W. Bonfield, “Characterization of Porous Hydroxyapatite,”J. Mater. Sci. Mater. Med., 10 [3] 135–145 (1999).
- 28 D. Tadic and M. Epple, “A Thorough Physicochemical Characterisation of 14 Calcium Phosphate-Based Bone Substitution Materials in Comparison to Natural Bone,”Biomaterials, 25 [6] 987–994 (2004).
- 29 A. Schmalholz, “External Skeletal Fixation Versus Cement Fixation in the Treatment of Redislocated Colles' Fracture,”Clin. Orthop. Relat. Res., [254] 236–241 (1990).
- 30 P. Kopylov, K. Runnqvist, K. Jonsson, and P. Aspenberg, “Norian SRS Versus External Fixation in Redisplaced Distal Radial Fractures. A Randomized Study in 40 Patients,”Acta Orthop. Scand., 70 [1] 1–5 (1999).
- 31 P. A. Glazer, U. M. Spencer, R. N. Alkalay, and J. Schwardt, “In Vivo Evaluation of Calcium Sulfate as a Bone Graft Substitute for Lumbar Spinal Fusion,”Spine J., 1 [6] 395–401 (2001).
- 32 A. Jamali, A. Hilpert, J. Debes, P. Afshar, S. Rahban, and R. Holmes, “Hydroxyapatite/Calcium Carbonate (HA/CC) vs. Plaster of Paris: A Histomorphometric and Radiographic Study in a Rabbit Tibial Defect Model,”Calcif. Tissue Int., 71 [2] 172–178 (2002).
- 33 E. Liljensten, E. Adolfsson, K. G. Strid, and P. Thomsen, “Resorbable and Nonresorbable Hydroxyapatite Granules as Bone Graft Substitutes in Rabbit Cortical Defects,”Clin. Implant Dent. Relat. Res., 5 [2] 95–101 (2003).
- 34 C. Wang, Y. Duan, B. Markovic, J. Barbara, C. R. Howlett, X. Zhang, and H. Zreiqat, “Phenotypic Expression of Bone-Related Genes in Osteoblasts Grown on Calcium Phosphate Ceramics with Different Phase Compositions,”Biomaterials, 25 [13] 2507–2514 (2004).
- 35 Z. Artzi, M. Weinreb, N. Givol, M. D. Rohrer, C. E. Nemcovsky, H. S. Prasad, and H. Tal, “Biomaterial Resorption Rate and Healing Site Morphology of Inorganic Bovine Bone and Beta-Tricalcium Phosphate in the Canine: A 24-Month Longitudinal Histologic Study and Morphometric Analysis,”Int. J. Oral Maxillofac. Implants, 19 [3] 357–368 (2004).
- 36 A. Moreira-Gonzalez, I. T. Jackson, T. Miyawaki, K. Barakat, and V. DiNick, “Clinical Outcome in Cranioplasty: Critical Review in Long-Term Follow-Up,”J. Craniofac. Surg., 14 [2] 144–153 (2003).
- 37 F. W. Bloemers, T. J. Blokhuis, P. Patka, F. C. Bakker, B. W. Wippermann, and H. J. Haarman, “Autologous Bone Versus Calcium-Phosphate Ceramics in Treatment of Experimental Bone Defects,”J. Biomed. Mater. Res. B Appl. Biomater., 66 [2] 526–531 (2003).
- 38 M. Muschik, R. Ludwig, S. Halbhubner, K. Bursche, and T. Stoll, “Beta-Tricalcium Phosphate as a Bone Substitute for Dorsal Spinal Fusion in Adolescent Idiopathic Scoliosis: Preliminary Results of a Prospective Clinical Study,”Eur. Spine J., 10 [Suppl 2] S178–S184 (2001).
- 39 T. M. Chu, D. G. Orton, S. J. Hollister, S. E. Feinberg, and J. W. Halloran, “Mechanical and In Vivo Performance of Hydroxyapatite Implants with Controlled Architectures,”Biomaterials, 23 [5] 1283–1293 (2002).
- 40 J. C. Le Huec, T. Schaeverbeke, D. Clement, J. Faber, and A. Le Rebeller, “Influence of Porosity on the Mechanical Resistance of Hydroxyapatite Ceramics Under Compressive Stress,”Biomaterials, 16 [2] 113–118 (1995).
- 41 A. Bignon, J. Chouteau, J. Chevalier, G. Fantozzi, J. P. Carret, P. Chavassieux, G. Boivin, M. Melin, and D. Hartmann, “Effect of Micro- and Macroporosity of Bone Substitutes on their Mechanical Properties and Cellular Response,”J. Mater. Sci. Mater. Med., 14 [12] 1089–1097 (2003).
- 42 K. Anselme, “Osteoblast Adhesion on Biomaterials,”Biomaterials, 21 668–680 (2000).
- 43 M. R. Urist, “Bone: Formation by Autoinduction,”Science, 150 [698] 893–899 (1965).
- 44 D. W. Burt and A. S. Law, “Evolution of the Transforming Growth Factor-Beta Superfamily,”Prog. Growth Factor Res., 5 [1] 99–118 (1994).
- 45 H. Zhu, P. Kavsak, S. Abdollah, J. L. Wrana, and G. H. Thomsen, “A SMAD Ubiquitin Ligase Targets the BMP Pathway and Affects Embryonic Pattern Formation,”Nature, 400 [6745] 687–693 (1999).
- 46 J. M. Wozney and V. Rosen, “Bone Morphogenetic Protein and Bone Morphogenetic Protein Gene Family in Bone Formation and Repair,”Clin. Orthop., [346] 26–37 (1998).
- 47 J. A. Skinner, P. O. Kroon, S. Todo, and G. Scott, “A Femoral Component with Proximal HA Coating. An Analysis of Survival and Fixation at up to Ten Years,”J. Bone Joint Surg. Br., 85 [3] 366–370 (2003).
- 48 A. H. Reddi, S. Wientroub, and N. Muthukumaran, “Biologic Principles of Bone Induction,”Orthop. Clin. North Am., 18 [2] 207–212 (1987).
- 49 P. Chen, J. L. Carrington, R. G. Hammonds, and A. H. Reddi, “Stimulation of Chondrogenesis in Limb Bud Mesoderm Cells by Recombinant Human Bone Morphogenetic Protein 2B (BMP-2B) and Modulation by Transforming Growth Factor Beta 1 and Beta 2,”Exp. Cell Res., 195 [2] 509–515 (1991).
- 50 H. M. Frost, “Bone “Mass” and the “Mechanostat”: A Proposal,”Anat. Rec., 219 [1] 1–9 (1987).
- 51 A. Katsumi, A. W. Orr, E. Tzima, and M. A. Schwartz, “Integrins in Mechanotransduction,”J. Biol. Chem., 279 [13] 12001–12004 (2004).
- 52 C. Zhong, M. Chrzanowska-Wodnicka, J. Brown, A. Shaub, A. M. Belkin, and K. Burridge, “Rho-Mediated Contractility Exposes A Cryptic Site in Fibronectin and Induces Fibronectin Matrix Assembly,”J. Cell Biol., 141 [2] 539–551 (1998).
- 53 J. R. Mauney, S. Sjostorm, J. Blumberg, R. Horan, J. P. O'Leary, G. Vunjak-Novakovic, V. Volloch, and D. L. Kaplan, “Mechanical Stimulation Promotes Osteogenic Differentiation of Human Bone Marrow Stromal Cells on 3-D Partially Demineralized Bone Scaffolds In Vitro,”Calcif. Tissue Int., 74 [5] 458–468 (2004).
- 54 C. H. Turner, M. R. Forwood, and M. W. Otter, “Mechanotransduction in Bone—Do Bone-Cells Act as Sensors of Fluid-Flow,”Faseb J., 8 [11] 875–878 (1994).
- 55 P. P. Cherian, B. Cheng, S. Gu, E. Sprague, L. F. Bonewald, and J. X. Jiang, “Effects of Mechanical Strain on the Function of Gap Junctions in Osteocytes are Mediated Through the Prostaglandin EP2 Receptor,”J. Biol. Chem., 278 [44] 43146–43156 (2003).
- 56 S. C. Rawlinson, A. A. Pitsillides, and L. E. Lanyon, “Involvement of Different Ion Channels in Osteoblasts' and Osteocytes' Early Responses to Mechanical Strain,”Bone, 19 [6] 609–614 (1996).
- 57 L. Smith, “Ceramic–Plastic Material as a Bone Substitute,”Arch Surg., 87 653–661 (1963).
- 58 R. B. Martin, M. W. Chapman, N. A. Sharkey, S. L. Zissimos, B. Bay, and E. C. Shors, “Bone Ingrowth and Mechanical Properties of Coralline Hydroxyapatite 1 Yr after Implantation,”Biomaterials, 14 [5] 341–348 (1993).
- 59 A. Uchida, S. M. Nade, E. R. McCartney, and W. Ching, “The Use of Ceramics for Bone Replacement. A Comparative Study of Three Different Porous Ceramics,”J. Bone Joint Surg. Br., 66 [2] 269–275 (1984).
- 60 G. Daculsi and N. Passuti, “Effect of the Macroporosity for Osseous Substitution of Calcium Phosphate Ceramics,”Biomaterials, 11 86–87 (1990).
- 61 O. Gauthier, J. M. Bouler, E. Aguado, P. Pilet, and G. Daculsi, “Macroporous Biphasic Calcium Phosphate Ceramics: Influence of Macropore Diameter and Macroporosity Percentage on Bone Ingrowth,”Biomaterials, 19 [1–3] 133–139 (1998).
- 62 P. S. Eggli, W. Muller, and R. K. Schenk, “Porous Hydroxyapatite and Tricalcium Phosphate Cylinders with Two Different Pore Size Ranges Implanted in the Cancellous Bone of Rabbits. A Comparative Histomorphometric and Histologic Study of Bony Ingrowth and Implant Substitution,”Clin. Orthop., [232] 127–138 (1988).
- 63 J. X. Lu, B. Flautre, K. Anselme, P. Hardouin, A. Gallur, M. Descamps, and B. Thierry, “Role of Interconnections in Porous Bioceramics on Bone Recolonization In Vitro and In Vivo,”J. Mater. Sci. Mater. Med., 10 [2] 111–120 (1999).
- 64 K. A. Hing, S. M. Best, K. E. Tanner, W. Bonfield, and P. A. Revell, “Quantification of Bone Ingrowth Within Bone-Derived Porous Hydroxyapatite Implants of Varying Density,”J. Mater. Sci. Mater. Med., [10/11] 663–670 (1999).
- 65 K. A. Hing, S. M. Best, K. E. Tanner, W. Bonfield, and P. A. Revell, “Mediation of Bone Ingrowth in Porous Hydroxyapatite Bone Graft Substitutes,”J. Biomed. Mater. Res. A, 68 [1] 187–200 (2004).
- 66 S. Li, J. R. De Wijn, J. Li, P. Layrolle, and K. De Groot, “Macroporous Biphasic Calcium Phosphate Scaffold with High Permeability/Porosity Ratio,”Tissue Eng., 9 [3] 535–548 (2003).
- 67 P. A. Rubin, J. K. Popham, J. R. Bilyk, and J. W. Shore, “Comparison of Fibrovascular Ingrowth Into Hydroxyapatite and Porous Polyethylene Orbital Implants,”Ophthal. Plast. Reconstr. Surg., 10 [2] 96–103 (1994).
- 68
L. J. Gibson and
M. F. Ashby, Cellular Solids. Structure and Properties, 2nd Edition. Cambridge University Press, Cambridge, 1997.
10.1017/CBO9781139878326 Google Scholar
- 69 M. Bohner and F. Baumgart, “Theoretical Model to Determine the Effects of Geometrical Factors on the Resorption of Calcium Phosphate Bone Substitutes,”Biomaterials, 25 [17] 3569–3582 (2004).
- 70 B. Annaz, K. A. Hing, M. Kayser, T. Buckland, and L. Di Silvio, “Porosity Variation in Hydroxyapatite and Osteoblast Morphology: A Scanning Electron Microscopy Study,”J. Microsc., 215 [Part 1] 100–110 (2004).
- 71 A. Boyde, A. Corsi, R. Quarto, R. Cancedda, and P. Bianco, “Osteoconduction in Large Macroporous Hydroxyapatite Ceramic Implants: Evidence for a Complementary Integration and Disintegration Mechanism,”Bone, 24 [6] 579–589 (1999).
- 72 K. Hing, B. Annaz, S. Saeed, P. Revell, and B. T., “Microporosity Enhances Bioactivity of Synthetic Bone Graft Substitutes,”J. Mater. Sci. Mater. Med., 16 467–475 (2005).
- 73 H. Yuan, K. Kurashina, J. D. De Bruijn, Y. Li, K. De Groot, and X. Zhang, “A Preliminary Study on Osteoinduction of Two Kinds of Calcium Phosphate Ceramics,”Biomaterials, 20 [19] 1799–1806 (1999).
- 74 M. J. Dalby, L. Di Silvio, E. J. Harper, and W. Bonfield, “Increasing Hydroxyapatite Incorporation Into Poly(Methylmethacrylate) Cement Increases Osteoblast Adhesion and Response,”Biomaterials, 23 [2] 569–576 (2002).
- 75 M. Lampin, C. Warocquier, C. Legris, M. Degrange, and M. F. Sigot-Luizard, “Correlation Between Substratum Roughness and Wettability, Cell Adhesion, and Cell Migration,”J. Biomed. Mater. Res., 36 [1] 99–108 (1997).
- 76 U. Ripamonti, “Osteoinduction in Porous Hydroxyapatite Implanted in Heterotopic Sites of Different Animal Models,”Biomaterials, 17 [1] 31–35 (1996).
- 77 C. D. McFarland, C. H. Thomas, C. DeFilippis, J. G. Steele, and K. E. Healy, “Protein Adsorption and Cell Attachment to Patterned Surfaces,”J. Biomed. Mater. Res., 49 [2] 200–210 (2000).
- 78 T. J. Webster, C. Ergun, R. H. Doremus, R. W. Siegel, and R. Bizios, “Specific Proteins Mediate Enhanced Osteoblast Adhesion on Nanophase Ceramics,”J. Biomed. Mater. Res., 51 [3] 475–483 (2000).
- 79 K. L. Kilpadi, A. A. Sawyer, C. W. Prince, P. L. Chang, and S. L. Bellis, “Primary Human Marrow Stromal Cells and Saos-2 Osteosarcoma Cells Use Different Mechanisms to Adhere to Hydroxylapatite,”J. Biomed. Mater. Res., 68A [2] 273–285 (2004).
- 80 A. L. Rosa, M. M. Beloti, and R. Van Noort, “Osteoblastic Differentiation of Cultured Rat Bone Marrow Cells on Hydroxyapatite with Different Surface Topography,”Dent. Mater., 19 [8] 768–772 (2003).
- 81 K. L. Kilpadi, P. L. Chang, and S. L. Bellis, “Hydroxylapatite Binds More Serum Proteins, Purified Integrins, and Osteoblast Precursor Cells than Titanium or Steel,”J. Biomed. Mater. Res., 57 [2] 258–267 (2001).
- 82 S. Ohtsubo, M. Matsuda, and M. Takekawa, “Angiogenesis After Sintered Bone Implantation in Rat Parietal Bone,”Histol. Histopathol, 18 [1] 153–163 (2003).
- 83 U. Ripamonti, B. Van den Heever, and J. Van Wyk, “Expression of the Osteogenic Phenotype in Porous Hydroxyapatite Implanted Extraskeletally in Baboons,”Matrix, 13 [6] 491–502 (1993).
- 84 A. Magan and U. Ripamonti, “Geometry of Porous Hydroxyapatite Implants Influences Osteogenesis in Baboons (Papio Ursinus),”J. Craniofac. Surg., 7 [1] 71–78 (1996).
- 85 Y. Kuboki, H. Takita, D. Kobayashi, E. Tsuruga, M. Inoue, M. Murata, N. Nagai, Y. Dohi, and H. Ohgushi, “BMP-Induced Osteogenesis on the Surface of Hydroxyapatite with Geometrically Feasible and Nonfeasible Structures: Topology of Osteogenesis,”J. Biomed. Mater. Res., 39 [2] 190–199 (1998).
- 86 P. Ducheyne and Q. Qiu, “Bioactive Ceramics: The Effect of Surface Reactivity on Bone Formation and Bone Cell Function,”Biomaterials, 20 [23–24] 2287–2303 (1999).
- 87 C. E. Oxnard, “Bone and Bones, Architecture and Stress, Fossils and Osteoporosis,”J. Biomech., 26 [Suppl. 1] 63–79 (1993).
- 88 J. A. O'Connor, L. E. Lanyon, and H. MacFie, “The Influence of Strain Rate on Adaptive Bone Remodelling,”J. Biomech., 15 [10] 767–781 (1982).
- 89 L. E. Lanyon, A. E. Goodship, C. J. Pye, and J. H. MacFie, “Mechanically Adaptive Bone Remodelling,”J. Biomech., 15 [3] 141–154 (1982).
- 90 D. B. Burr, R. B. Martin, M. B. Schaffler, and E. L. Radin, “Bone Remodeling in Response to In Vivo Fatigue Microdamage,”J. Biomech., 18 [3] 189–200 (1985).
- 91
L. L. Hench and
J. Wilson, An Introduction to Bioceramics. World Scientific, Singapore, 1993.
10.1142/2028 Google Scholar
- 92 J. Black, “Systemic Effects of Biomaterials,”Biomaterials, 5 [1] 11–18 (1984).
- 93 L. Hench and H. Paschall, “Direct Chemical Bond of Bioactive Glass–Ceramic Materials to Bone and Muscle,”J. Biomed. Mater. Res., 7 [3] 25–42 (1973).
- 94 J. D. De Bruijn, C. P. Klein, K. De Groot, and C. A. Van Blitterswijk, “The Ultrastructure of the Bone–Hydroxyapatite Interface In Vitro,”J. Biomed. Mater. Res., 26 [10] 1365–1382 (1992).
- 95 I. Ahmed, M. Lewis, I. Olsen, and J. C. Knowles, “Phosphate Glasses for Tissue Engineering: Part 1. Processing and Characterisation of a Ternary-Based P2O5–CaO–Na2O Glass System,”Biomaterials, 25 [3] 491–499 (2004).
- 96 J. E. Gough, J. R. Jones, and L. L. Hench, “Osteoblast Nodule Formation and Mineralisation on Foamed 58S Bioactive Glass,”Key Eng. Mater., 254–256 (2004).
- 97 P. N. De Aza, Z. B. Luklinska, A. Martinez, M. R. Anseau, F. Guitian, and S. De Aza, “Morphological and Structural Study of Pseudowollastonite Implants in Bone,”J. Microsc., 197 [Part 1] 60–67 (2000).
- 98 T. Nakamura, T. Yamamuro, S. Higashi, T. Kokubo, and S. Itoo, “A New Glass–Ceramic for Bone Replacement: Evaluation of its Bonding to Bone Tissue,”J. Biomed. Mater. Res., 19 [6] 685–698 (1985).
- 99 K. A. Hing, I. R. Gibson, P. A. Revell, S. M. Best, and W. Bonfield, “Influence of Phase Purity on the In Vivo Response to Hydroxyapatite,”Key Eng. Mater., 192–195 373–376 (2001).
- 100 L. Di Silvio, M. J. Dalby, and W. Bonfield, “Osteoblast Behaviour on HA/PE Composite Surfaces with Different HA Volumes,”Biomaterials, 23 [1] 101–107 (2002).
- 101 S. A. Redey, M. Nardin, D. Bernache-Assolant, C. Rey, P. Delannoy, L. Sedel, and P. J. Marie, “Behavior of Human Osteoblastic Cells on Stoichiometric Hydroxyapatite and Type A Carbonate Apatite: Role of Surface Energy,”J. Biomed. Mater. Res., 50 [3] 353–364 (2000).
- 102 S. A. Redey, S. Razzouk, C. Rey, D. Bernache-Assollant, G. Leroy, M. Nardin, and G. Cournot, “Osteoclast Adhesion and Activity on Synthetic Hydroxyapatite, Carbonated Hydroxyapatite, and Natural Calcium Carbonate: Relationship to Surface Energies,”J. Biomed. Mater. Res., 45 [2] 140–147 (1999).
- 103 E. A. Kaufmann, P. Ducheyne, S. Radin, D. A. Bonnell, and R. Composto, “Initial Events at the Bioactive Glass Surface in Contact with Protein-Containing Solutions,”J. Biomed. Mater. Res., 52 [4] 825–830 (2000).
- 104 T. Kobayashi, S. Nakamura, and K. J. Yamashita, “Enhanced Osteobonding by Negative Surface Charges of Electrically Polarized Hydroxyapatite,”J. Biomed. Res., 57 477–484 (2001).
- 105
K. Webb,
V. Hlady, and P. Tresco, “Relative Importance of Surface Wettability and Charged Functional Groups on NIH 3T3 Fibroblast Attachment, Spreading, and Cytoskeletal Organization,”J. Biomed. Mater. Res., 41
[3]
422–430 (1998).
10.1002/(SICI)1097-4636(19980905)41:3<422::AID-JBM12>3.0.CO;2-K CASPubMedWeb of Science®Google Scholar
- 106 G. Toworfe, R. Composto, C. Adams, I. Shapiro, and P. Ducheyne, “Fibronectin Adsorption on Surface-Activated Poly(Dimethylsiloxane) and its Effect on Cellular Function,”J. Biomed. Mater. Res., 71A 449–461 (2004).
- 107 S. Takemoto, Y. Kusudo, K. Tsuru, S. Hayakawa, A. Osaka, and S. Takashima, “Selective Protein Adsorption and Blood Compatibility of Hydroxy-Carbonate Apatites,”J. Biomed. Mater. Res., 69A [3] 544–551 (2004).
- 108 D. A. Pampena, K. A. Robertson, O. Litvinova, G. Lajoie, H. A. Goldberg, and G. K. Hunter, “Inhibition of Hydroxyapatite Formation by Osteopontin Phosphopeptides,”Biochem. J., 378 [Part 3] 1083–1087 (2004).
- 109
I. R. Gibson,
S. M. Best, and W. Bonfield, “Chemical Characterization of Silicon-Substituted Hydroxyapatite,”J. Biomed. Mater. Res., 44
[4]
422–428 (1999).
10.1002/(SICI)1097-4636(19990315)44:4<422::AID-JBM8>3.0.CO;2-# CASPubMedWeb of Science®Google Scholar
- 110 I. R. Gibson and W. Bonfield, “Preparation and Characterization of Magnesium/Carbonate Co-Substituted Hydroxyapatites,”J. Mater. Sci. Mater. Med., 13 [7] 685–693 (2002).
- 111 M. Ikeuchi, A. Ito, Y. Dohi, H. Ohgushi, H. Shimaoka, K. Yonemasu, and T. Tateishi, “Osteogenic Differentiation of Cultured Rat and Human Bone Marrow Cells on the Surface of Zinc-Releasing Calcium Phosphate Ceramics,”J. Biomed. Mater. Res. A, 67 [4] 1115–1122 (2003).
- 112
J. D. Layani,
F. J. Cuisinier,
P. Steuer,
H. Cohen,
J. C. Voegel, and I. Mayer, “High-Resolution Electron Microscopy Study of Synthetic Carbonate and Aluminum Containing Apatites,”J. Biomed. Mater. Res., 50
[2]
199–207 (2000).
10.1002/(SICI)1097-4636(200005)50:2<199::AID-JBM15>3.0.CO;2-Q CASPubMedWeb of Science®Google Scholar
- 113 J. C. Merry, I. R. Gibson, S. M. Best, and W. Bonfield, “Synthesis and Characterization of Carbonate Hydroxyapatite,”J. Mater. Sci. Mater. Med., 9 [12] 779–783 (1998).
- 114
C. M. Botelho,
R. A. Brooks,
S. M. Best,
M. A. Lopes,
J. D. Santos,
N. Rushton, and W. Bonfield, “Biological and Physical–Chemical Characterisation of Phase-Pure HA and SI-Substituted Hydroxyapetite by Different Microscopic Techniques,”Key Eng. Mater. Bioceram., 16
845–848 (2004).
10.4028/www.scientific.net/KEM.254-256.845 Google Scholar
- 115 C. M. Botelho, M. A. Lopes, I. R. Gibson, S. M. Best, and J. D. Santos, “Structural Analysis of Si-Substituted Hydroxyapatite: Zeta Potential and X-Ray Photoelectron Spectroscopy,”J. Mater. Sci.: Mater. Med., 13 1123–1127 (2002).
- 116 N. Rashid, I. Harding, and K. A. Hing, “ Effect of Silicate Substitution of the Surface Charge of Hydroxyapatite,” 7th World Biomaterials Congress, Sydney, 2004.
- 117 K. A. Hing, S. Saeed, B. Annaz, T. Buckland, and P. A. Revell, “ Silicate Substitution Alters the Progression of Bone Apposition Within Porous Hydroxyapatite Bone Graft Substitutes,” 50th Annual Meeting of the Orthopaedic Research Society, San Francisco, 2004.
- 118 N. Patel, S. M. Best, W. Bonfield, I. R. Gibson, K. A. Hing, E. Damien, and P. A. Revell, “A Comparative Study on the In Vivo Behaviour of Hydroxyapatite and Silicon Substituted Hydroxyapatite Granules,”J. Mater. Sci.: Mater. Med., 13 1199–1206 (2002).
- 119 A. E. Porter, N. Patel, J. N. Skepper, S. M. Best, and W. Bonfield, “Comparison of In Vivo Dissolution Processes in Hydroxyapatite and Silicon-Substituted Hydroxyapatite Bioceramics,”Biomaterials, 24 [25] 4609–4620 (2003).
- 120 F. C. Driessens, “Probable Phase Composition of the Mineral in Bone,”Z. Naturforsch. [C], 35 [5–6] 357–362 (1980).
- 121 M. Hasegawa, Y. Doi, and A. Uchida, “Cell-Mediated Bioresorption of Sintered Carbonate Apatite in Rabbits,”J. Bone Joint Surg. Br., 85 [1] 142–147 (2003).
- 122 J. Barralet, M. Akao, and H. Aoki, “Dissolution of Dense Carbonate Apatite Subcutaneously Implanted in Wistar Rats,”J. Biomed. Mater. Res., 49 [2] 176–182 (2000).
- 123 T. R. Arnett and M. Spowage, “Modulation of the Resorptive Activity of Rat Osteoclasts by Small Changes in Extracellular pH Near the Physiological Range,”Bone, 18 [3] 277–279 (1996).
- 124 P. J. Marie, R. Travers, and E. E. Delvin, “Influence of Magnesium Supplementation on Bone Turnover in the Normal Young Mouse,”Calcif. Tissue Int., 35 [6] 755–761 (1983).
- 125 Y. Toba, Y. Kajita, R. Masuyama, Y. Takada, K. Suzuki, and S. Aoe, “Dietary Magnesium Supplementation Affects Bone Metabolism and Dynamic Strength of Bone in Ovariectomized Rats,”J. Nutr., 130 [2] 216–220 (2000).
- 126 H. Zeiqat, C. R. Howlett, A. Zannettino, P. Evans, G. Schulze-Tanzil, C. Knabe, and M. Shakibaei, “Mechanisms of Magnesium-Stimulated Adhesion of Osteoblastic Cells to Commonly Used Orthopaedic Implants,”J. Biomed. Mater. Res., 62 [2] 175–184 (2002).
- 127
H. Zreiqat,
P. Evans, and C. R. Howlett, “Effect of Surface Chemical Modificaton of Bioceramic on Phenotype of Human Bone-Derived Cells,”J. Biomed. Mater. Res., 44
[4]
389–396 (1999).
10.1002/(SICI)1097-4636(19990315)44:4<389::AID-JBM4>3.0.CO;2-O CASPubMedWeb of Science®Google Scholar
- 128 E. M. Carlisle, “Silicon: A Possible Factor in Bone Calcification,”Science, 167 [916] 279–280 (1970).
- 129 D. M. Reffitt, R. Jugdaohsingh, R. P. Thompson, and J. J. Powell, “Silicic Acid: Its Gastrointestinal Uptake and Urinary Excretion in Man and Effects on Aluminium Excretion,”J. Inorg. Biochem., 76 [2] 141–147 (1999).
- 130 I. D. Xynos, M. V. Hukkanen, J. J. Batten, L. D. Buttery, L. L. Hench, and J. M. Polak, “Bioglass 45S5 Stimulates Osteoblast Turnover and Enhances Bone Formation In Vitro: Implications and Applications for Bone Tissue Engineering,”Calcif. Tissue Int., 67 [4] 321–329 (2000).
- 131 T. Gao, H. T. Aro, H. Ylanen, and E. Vuorio, “Silica-Based Bioactive Glasses Modulate Expression of Bone Morphogenetic Protein-2 mRNA in Saos-2 Osteoblasts In Vitro,”Biomaterials, 22 [12] 1475–1483 (2001).
- 132 I. D. Xynos, A. J. Edgar, L. D. Buttery, L. L. Hench, and J. M. Polak, “Gene-Expression Profiling of Human Osteoblasts Following Treatment with the Ionic Products of Bioglass 45S5 Dissolution,”J. Biomed. Mater. Res., 55 [2] 151–157 (2001).
- 133 J. E. Gough, J. R. Jones, and L. L. Hench, “Nodule Formation and Mineralisation of Human Primary Osteoblasts Cultured on a Porous Bioactive Glass Scaffold,”Biomaterials, 25 [11] 2039–2046 (2004).
- 134 J. E. Gough, D. C. Clupper, and L. L. Hench, “Osteoblast Responses to Tape-Cast and Sintered Bioactive Glass Ceramics,”J. Biomed. Mater. Res., 69A [4] 621–628 (2004).
- 135 D. M. Reffitt, N. Ogston, R. Jugdaohsingh, H. F. Cheung, B. A. Evans, R. P. Thompson, J. J. Powell, and G. N. Hampson, “Orthosilicic Acid Stimulates Collagen Type 1 Synthesis and Osteoblastic Differentiation in Human Osteoblast-Like Cells In Vitro,”Bone, 32 [2] 127–135 (2003).
- 136 L. Brown, Z. Luklinska, P. N. De Aza, S. De Aza, M. Anseau, F. J. Hughes, and I. J. McKay, “ Mechanism of Osteoinduction by Pseudowollastonite (psW) Ceramic,” 7th World Biomaterials Congress, Sydney, 2004.
- 137 Y. L. Chang, C. M. Stanford, and J. C. Keller, “Calcium and Phosphate Supplementation Promotes Bone Cell Mineralization: Implications for Hydroxyapatite (HA)-Enhanced Bone Formation,”J. Biomed. Mater. Res., 52 [2] 270–278 (2000).
- 138 K. A. Hing, S. Saeed, B. Annaz, T. Buckland, and P. A. Revell, “ Variation in the Rate of Bone Apposition Within Porous Hydroxy Apatite and Tricalcium Bone Graft Substitutes,” 50th Annual Meeting of the Orthopaedic Research Society, San Francisco, 2004.
- 139 S. Saeed, K. Hing, and R. PA, “ Hydoxyapatite Activates T Lymphocytes and Causes Inflammation in the Liver and Spleen Retrieved from Rabbits Following Intraosseous Implantation,” 7th World Biomaterials Congress, Sydney, 2004.
- 140 J. Handschel, H. P. Wiesmann, U. Stratmann, J. Kleinheinz, U. Meyer, and U. Joos, “TCP is Hardly Resorbed and Not Osteoconductive in a Non-Loading Calvarial Model,”Biomaterials, 23 [7] 1689–1695 (2002).
- 141 C. P. Klein, A. A. Driessen, K. De Groot, and A. Van Den Hooff, “Biodegradation Behavior of Various Calcium Phosphate Materials in Bone Tissue,”J. Biomed. Mater. Res., 17 [5] 769–784 (1983).
- 142 A. E. Porter, C. M. Botelho, M. A. Lopes, J. D. Santos, S. M. Best, and W. Bonfield, “Ultrastructural Comparison of Dissolution and Apatite Precipitation on Hydroxyapatite and Silicon-Substituted Hydroxyapatite In Vitro and In Vivo,”J. Biomed. Mater. Res., 69A [4] 670–679 (2004).
- 143 E. Damien and P. Revell, “Changes in Distant Organs in Response to Local Osteogenic Growth Factors Delivered by Intraosseous Implants: A Histological Evaluation,”Key Eng. Mater., 254–256 797–800 (2004).