Properties of osteoconductive biomaterials: calcium phosphates.

Bone is formed by a series of complex events involving the mineralization of extracellular matrix proteins rigidly orchestrated by cells with specific functions of maintaining the integrity of the bone. Bone, similar to other calcified tissues, is an intimate composite of the organic (collagen and noncollagenous proteins) and inorganic or mineral phases. The bone mineral idealized as calcium hydroxyapatite, Ca10 (PO4)(6)(OH)2, is a carbonatehydroxyapatite, approximated by the formula: (Ca,X)(10)(PO4,HPO4,CO3)(6)(OH,Y)2, where X are cations (magnesium, sodium, strontium ions) that can substitute for the calcium ions, and Y are anions (chloride or fluoride ions) that can substitute for the hydroxyl group. The current author presents a brief review of CaP biomaterials that now are used as grafts for bone repair, augmentation, or substitution. Commercially-available CaP biomaterials differ in origin (natural or synthetic), composition (hydroxyapatite, beta-tricalcium phosphate, and biphasic CaP), or physical forms (particulates, blocks, cements, coatings on metal implants, composites with polymers), and in physicochemical properties. CaP biomaterials have outstanding properties: similarity in composition to bone mineral; bioactivity (ability to form bone apatitelike material or carbonate hydroxyapatite on their surfaces), ability to promote cellular function and expression leading to formation of a uniquely strong bone-CaP biomaterial interface; and osteoconductivity (ability to provide the appropriate scaffold or template for bone formation). In addition, CaP biomaterials with appropriate three-dimensional geometry are able to bind and concentrate endogenous bone morphogenetic proteins in circulation, and may become osteoinductive (capable of osteogenesis), and can be effective carriers of bone cell seeds. Therefore, CaP biomaterials potentially are useful in tissue engineering for regeneration of hard tissues.

[1]  H. Aoki,et al.  [Studies on the application of apatite to dental materials. (I) --Apatite ceramics-- (author's transl)]. , 1976, Shika rikogaku zasshi. Journal of the Japan Society for Dental Apparatus and Materials.

[2]  T. Vijayaraghavan,et al.  Electrodeposition of apatite coating on pure titanium and titanium alloys , 1994 .

[3]  R.Z. Legfros,et al.  Magnesium and Carbonate in Enamel and Synthetic Apatites , 1996, Advances in dental research.

[4]  A Leith,et al.  Mineral and organic matrix interaction in normally calcifying tendon visualized in three dimensions by high-voltage electron microscopic tomography and graphic image reconstruction. , 1993, Journal of structural biology.

[5]  K. Mueller,et al.  Bioceramic implants in surgically produced infrabony defects. , 1975, Journal of periodontology.

[6]  J. Osborn,et al.  The material science of calcium phosphate ceramics. , 1980, Biomaterials.

[7]  H. Ohgushi.  Coral Derived Porous Framework Having Different Chemical Compositions as a Scaffold for Osteoblastic Differentitation , 1997 .

[8]  P. Chakravarthy,et al.  alpha-BSM: a biomimetic bone substitute and drug delivery vehicle. , 1999, Clinical orthopaedics and related research.

[9]  A. Boyde,et al.  Osteoconduction in large macroporous hydroxyapatite ceramic implants: evidence for a complementary integration and disintegration mechanism. , 1999, Bone.

[10]  A. Reddi,et al.  Morphogenesis and tissue engineering of bone and cartilage: inductive signals, stem cells, and biomimetic biomaterials. , 2000, Tissue engineering.

[11]  D. Mcconnell.  The Crystal Chemistry of Carbonate Apatites and their Relationship to the Composition of Calcified Tissues , 1952, Journal of dental research.

[12]  RACQUEL ZAPANTA-LEGEROS,et al.  Effect of Carbonate on the Lattice Parameters of Apatite , 1965, Nature.

[13]  J. Bobick,et al.  Hydroxylapatite synthesis and characterization in dense polycrystalline form , 1976 .

[14]  D. S. Metsger,et al.  Tricalcium phosphate ceramic--a resorbable bone implant: review and current status. , 1982, Journal of the American Dental Association.

[15]  A. Reddi,et al.  The critical role of geometry of porous hydroxyapatite delivery system in induction of bone by osteogenin, a bone morphogenetic protein. , 1992, Matrix.

[16]  J. Mulliken,et al.  Donor-site morbidity after harvesting rib and iliac bone. , 1984, Plastic and reconstructive surgery.

[17]  M Gineste,et al.  Physicochemical characterization of deposits associated with HA ceramics implanted in nonosseous sites. , 1988, Journal of biomedical materials research.

[18]  M. Glimcher,et al.  Identification of brushite in newly deposited bone mineral from embryonic chicks. , 1979, Journal of ultrastructure research.

[19]  D Abensur,et al.  Sinus grafting with porous bone mineral (Bio-Oss) for implant placement: a 5-year study on 15 patients. , 2000, The International journal of periodontics & restorative dentistry.

[20]  W. Kalk,et al.  Eleven-year study of hydroxyapatite implants. , 1989, The Journal of prosthetic dentistry.

[21]  S. Weiner,et al.  Crystal size and organization in bone. , 1989, Connective tissue research.

[22]  E. Dawson,et al.  Beta-tricalcium phosphate delivery system for bone morphogenetic protein. , 1984, Clinical orthopaedics and related research.

[23]  Larry L. Hench,et al.  Bonding mechanisms at the interface of ceramic prosthetic materials , 1971 .

[24]  J P LeGeros,et al.  Synergistic effects of magnesium and carbonate on properties of biological and synthetic apatites. , 1995, Connective tissue research.

[25]  J. Davies,et al.  In vitro modeling of the bone/implant interface , 1996, The Anatomical record.

[26]  W. E. Brown,et al.  Octacalcium Phosphate and Hydroxyapatite: Crystal Structure of Octacalcium Phosphate , 1962, Nature.

[27]  E.A. Monroe,et al.  New Calcium Phosphate Ceramic Material for Bone and Tooth Implants , 1971, Journal of dental research.

[28]  Michael Jarcho,et al.  Calcium phosphate ceramics as hard tissue prosthetics. , 1981, Clinical orthopaedics and related research.

[29]  M. Okazaki,et al.  Crystallographic and chemical properties of Mg-containing apatites before and after suspension in solutions. , 1992, Magnesium research.

[30]  T. Tateishi,et al.  Stimulatory effect of zinc-releasing calcium phosphate implant on bone formation in rabbit femora. , 2000, Journal of biomedical materials research.

[31]  C. Beevers.  The Atomic Structure of Fluor-Apatite and its Relation to that of Tooth and Bone Material , 1946 .

[32]  R. Pool.  Coral chemistry leads to human bone repair. , 1995, Science.

[33]  M. Urist,et al.  Bone: Formation by Autoinduction , 1965, Science.

[34]  R. Legeros,et al.  Spectral Properties of Carbonate in Carbonate-Containing Apatites , 1970 .

[35]  D. Roy,et al.  Hydroxyapatite formed from Coral Skeletal Carbonate by Hydrothermal Exchange , 1974, Nature.

[36]  G. Daculsi,et al.  A new injectable calcium phosphate biomaterial for immediate bone filling of extraction sockets: a preliminary study in dogs. , 1999, Journal of periodontology.

[37]  P. H. Crayton,et al.  Forming method for apatite prostheses. , 1969, Journal of biomedical materials research.

[38]  D. Liu.  Influence of Porous Microarchitecture on the In-Vitro Dissolution and Biological Behaviour of Porous Calcium Phosphate Ceramics , 1997 .

[39]  Y. Açil,et al.  Three-dimensional cultivation of human osteoblast-like cells on highly porous natural bone mineral. , 2000, Journal of biomedical materials research.

[40]  Linkow Li.  Bone transplants using the symphysis, the iliac crest and synthetic bone materials. , 1983 .

[41]  C. Bleiwas,et al.  Zinc effect on the in vitro formation of calcium phosphates: relevance to clinical inhibition of calculus formation. , 1999, American journal of dentistry.

[42]  J. Ganeles,et al.  Ultrastructure of durapatite-periodontal tissue interface in human intrabony defects. , 1986, Journal of periodontology.

[43]  S D Cook,et al.  Hydroxylapatite coating of porous implants improves bone ingrowth and interface attachment strength. , 1992, Journal of biomedical materials research.

[44]  Larry L. Hench,et al.  Bioceramics: From Concept to Clinic , 1991 .

[45]  H. Ohgushi,et al.  BMP-induced osteogenesis on the surface of hydroxyapatite with geometrically feasible and nonfeasible structures: topology of osteogenesis. , 1998, Journal of biomedical materials research.

[46]  T. Bauer.  Hydroxyapatite: coating controversies. , 1995, Orthopedics.

[47]  I. Losito,et al.  Detection of collagen synthesis by human osteoblasts on a tricalcium phosphate hydroxyapatite: an X-ray photoelectron spectroscopy investigation. , 2000, Journal of biomedical materials research.

[48]  R. Legeros,et al.  Apatite Crystallites: Effects of Carbonate on Morphology , 1967, Science.

[49]  F. H. Albee.  STUDIES IN BONE GROWTH: TRIPLE CALCIUM PHOSPHATE AS A STIMULUS TO OSTEOGENESIS. , 1920, Annals of surgery.

[50]  O. Suzuki,et al.  Implantation of octacalcium phosphate (OCP) in rat skull defects enhances bone repair. , 1999, Journal of dental research.

[51]  R. Holmes,et al.  Bone Regeneration Within a Coralline Hydroxyapatite Implant , 1979, Plastic and reconstructive surgery.

[52]  R. Baron,et al.  Cell-mediated extracellular acidification and bone resorption: evidence for a low pH in resorbing lacunae and localization of a 100-kD lysosomal membrane protein at the osteoclast ruffled border , 1985, The Journal of cell biology.

[53]  B Kerebel,et al.  Transformation of biphasic calcium phosphate ceramics in vivo: ultrastructural and physicochemical characterization. , 1989, Journal of biomedical materials research.

[54]  G. Daculsi,et al.  Biphasic calcium phosphates: influence of three synthesis parameters on the HA/beta-TCP ratio. , 2000, Journal of biomedical materials research.

[55]  G. Daculsi,et al.  Macroporous calcium phosphate ceramic for long bone surgery in humans and dogs. Clinical and histological study. , 1990, Journal of biomedical materials research.

[56]  M. Grégoire,et al.  Effects of hydroxyapatite particles on periodontal ligament fibroblast-like cell behavior. , 1997, Journal of periodontology.

[57]  L. Linkow.  Bone transplants using the symphysis, the iliac crest and synthetic bone materials. , 1983, The Journal of oral implantology.

[58]  R Z LeGeros,et al.  Chemical stability of carbonate- and fluoride-containing apatites. , 1983, Caries research.

[59]  T. Kokubo,et al.  Formation of biologically active bone-like apatite on metals and polymers by a biomimetic process , 1996 .

[60]  J. Wagner.  Clinical and histological case study using resorbable hydroxylapatite for the repair of osseous defects prior to endosseous implant surgery. , 1989, The Journal of oral implantology.

[61]  Racquel Z. LeGeros,et al.  7. Substrate Surface Dissolution and Interfacial Biological Mineralization , 1991 .

[62]  L. Dorr,et al.  Complications with hydroxyapatite particulate separation in total hip arthroplasty. , 1994, Clinical orthopaedics and related research.

[63]  K. Lynch,et al.  Tissue response to biphasic calcium phosphate ceramic with different ratios of HA/beta TCP in periodontal osseous defects. , 1992, Journal of periodontology.

[64]  H. Cheung,et al.  Cellular Responses to Whitlockite , 1999, Calcified Tissue International.

[65]  Racquel Z. LeGeros,et al.  Conversion of Monetite, CaHPO4, To Apatites: Effect of Carbonate on the Crystallinity and the Morphology of the Apatite Crystallites , 1970 .

[66]  Y. Sato,et al.  Bone formation by cells from femurs cultured among three-dimensionally arranged hydroxyapatite granules. , 1997, Journal of biomedical materials research.

[67]  Donald L. Wise,et al.  Encyclopedic Handbook of Biomaterials and Bioengineering , 1995 .

[68]  E C Moreno,et al.  Physicochemical aspects of fluoride-apatite systems relevant to the study of dental caries. , 1977, Caries research.

[69]  R. Doremus,et al.  Direct electron microscopy studies of the bone-hydroxylapatite interface. , 1984, Journal of biomedical materials research.

[70]  A I Caplan,et al.  Stem cell technology and bioceramics: from cell to gene engineering. , 1999, Journal of biomedical materials research.

[71]  H K Koerten,et al.  Degradation of calcium phosphate ceramics. , 1999, Journal of biomedical materials research.

[72]  J. Elliott.  The problems of the composition and structure of the mineral components of the hard tissues. , 1973, Clinical orthopaedics and related research.

[73]  N Passuti,et al.  Osteogenic potential in vitro of human bone marrow cells cultured on macroporous biphasic calcium phosphate ceramic. , 1999, Journal of biomedical materials research.

[74]  C. V. van Blitterswijk,et al.  Osteoclastic resorption of calcium phosphates is potentiated in postosteogenic culture conditions. , 1994, Journal of biomedical materials research.

[75]  Raquel Zapanta LeGeros,et al.  Apatites in biological systems , 1981 .

[76]  G. Daculsi,et al.  Osteoclastic resorption of biphasic calcium phosphate ceramic in vitro. , 1997, Journal of biomedical materials research.

[77]  H. Oonishi,et al.  Comparative bone growth behavior in granules of bioceramic materials of various sizes. , 1999, Journal of biomedical materials research.

[78]  R. Geesink,et al.  Six-year results of hydroxyapatite-coated total hip replacement. , 1995, The Journal of bone and joint surgery. British volume.

[79]  W. E. Brown,et al.  Chemical Properties of Bone Mineral , 1976 .

[80]  C. Stanford,et al.  Calcium and phosphate supplementation promotes bone cell mineralization: implications for hydroxyapatite (HA)-enhanced bone formation. , 2000, Journal of biomedical materials research.

[81]  U. Joos,et al.  Interaction of osteogenic cells with hydroxylapatite implant materials in vitro and in vivo. , 1990, The International journal of oral & maxillofacial implants.

[82]  R. Craig,et al.  Early events associated with periodontal connective tissue attachment formation on titanium and hydroxyapatite surfaces. , 1999, Journal of biomedical materials research.

[83]  F A Pflughoeft,et al.  Functional loading of bioceramic augmented alveolar ridge--a pilot study. , 1980, The Journal of prosthetic dentistry.

[84]  H. Schroeder,et al.  Formation and inhibition of dental calculus. , 1969, Journal of periodontology.

[85]  R. Legeros,et al.  In Vitro Interactions of Bone Marrow Cells with Carbonate and Fluoride Containing Apatites , 2000 .

[86]  Racquel Z. LeGeros,et al.  Materials for Bone Repair, Augmentation, and Implant Coatings , 1992 .

[87]  Eugene P. Lazzari,et al.  CRC handbook of experimental aspects of oral biochemistry , 1983 .

[88]  A. S. Posner,et al.  Infrared Analysis of Rat Bone: Age Dependency of Amorphous and Crystalline Mineral Fractions , 1966, Science.

[89]  M. Shirkhanzadeh.  Bioactive calcium phosphate coatings prepared by electrodeposition , 1991 .

[90]  S A Goldstein,et al.  Skeletal repair by in situ formation of the mineral phase of bone. , 1995, Science.

[91]  R Z LeGeros,et al.  Biodegradation and bioresorption of calcium phosphate ceramics. , 1993, Clinical materials.

[92]  C J Damien,et al.  Bone graft and bone graft substitutes: a review of current technology and applications. , 1991, Journal of applied biomaterials : an official journal of the Society for Biomaterials.