Bioactive ceramics: from bone grafts to tissue engineering

Bioactive ceramics bond directly with living tissues when implanted. For this reason they have been profusely investigated as biomaterials. The first synthetic bioactive materials were specific compositions of glasses and glass ceramics as well as sintered hydroxyapatite. However, all these bioceramics are brittle, and for this reason their main application for years has been as a grafting material for the filling of small bone defects and periodontal anomalies. The efforts to expand the applications of bioactive bioceramics were mainly focused in two areas: (A) the synthesis of organic–inorganic hybrids to apply in tissue engineering and of ceramic coatings on metallic substrates for applications requiring good mechanical behavior, and (B) the synthesis of porous materials with very quick bioactive response that can be upgraded by adding biomolecules or therapeutic inorganic ions to be used in bone tissue engineering. For these developments, the in vitro studies in solutions mimicking blood plasma played a major role. At the present, it is universally considered that both bioactive and biodegradable materials are going to play a central role in the fabrication of porous scaffolds that after being decorated with cells and signals form constructs: basic elements of tissue engineering. This article reviews the pathway followed by the bioactive materials from their original applications in bone grafts to the present day where they are widely investigated as porous scaffolds for bone tissue engineering. After defining the concept of bioactivity, important bioactive materials will be listed in this article. Then, the specific characteristics of bioactive materials when used in bulk or coatings as well as the comparison with biodegradable materials will be presented. Finally, and after describing the in vitro studies for the evaluation of bioactive ceramics, the main characteristics of template glasses, compared with conventional sol–gel glasses, and the advantages of using porous bioactive ceramics to obtain scaffolds for bone tissue engineering will be explained.

[1]  C. Laurencin,et al.  Biodegradable polymers as biomaterials , 2007 .

[2]  M. Vallet‐Regí,et al.  Biomimetic Apatite Deposition on Calcium Silicate Gel Glasses , 2001 .

[3]  M. Vallet‐Regí,et al.  Interaction of an ordered mesoporous bioactive glass with osteoblasts, fibroblasts and lymphocytes, demonstrating its biocompatibility as a potential bone graft material. , 2010, Acta biomaterialia.

[4]  M. Vallet‐Regí,et al.  Bioactive Carbonate−Hydroxyapatite Coatings Deposited onto Ti6Al4V Substrate , 2004 .

[5]  T. Kokubo,et al.  REVIEW Bioactive metals: preparation and properties , 2004, Journal of materials science. Materials in medicine.

[6]  W. E. Brown,et al.  Octacalcium Phosphate as a Precursor in Biomineral Formation , 1987, Advances in dental research.

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

[8]  Huipin Yuan,et al.  Osteoinductive ceramics as a synthetic alternative to autologous bone grafting , 2010, Proceedings of the National Academy of Sciences.

[9]  K. de Groot,et al.  X-ray diffraction studies on plasma-sprayed calcium phosphate-coated implants. , 1990, Journal of biomedical materials research.

[10]  Guang-Ling Song,et al.  Control of biodegradation of biocompatable magnesium alloys , 2007 .

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

[12]  M. Vallet‐Regí,et al.  Nanostructured Hybrid Materials for Bone Tissue Regeneration , 2006 .

[13]  M. Vallet‐Regí,et al.  The in vivo behaviour of a sol-gel glass and a glass-ceramic during critical diaphyseal bone defects healing. , 2005, Biomaterials.

[14]  M. Vallet‐Regí,et al.  Fascinating properties of bioactive templated glasses: A new generation of nanostructured bioceramics , 2011 .

[15]  G. H. Nancollas,et al.  Growth of calcium phosphate on hydroxyapatite crystals. Effect of supersaturation and ionic medium , 1974 .

[16]  María Vallet-Regí,et al.  Ceramics for medical applications , 2001 .

[17]  K. Groot Bioceramics consisting of calcium phosphate salts. , 1980 .

[18]  Yasuhiro Sakamoto,et al.  Three-dimensional structure of large-pore mesoporous cubic Ia3d silica with complementary pores and its carbon replica by electron crystallography. , 2004, Angewandte Chemie.

[19]  Francesco Baino,et al.  Three-dimensional glass-derived scaffolds for bone tissue engineering: current trends and forecasts for the future. , 2011, Journal of biomedical materials research. Part A.

[20]  T Kitsugi,et al.  Solutions able to reproduce in vivo surface-structure changes in bioactive glass-ceramic A-W. , 1990, Journal of biomedical materials research.

[21]  Dehong Chen,et al.  Synthesis and phase behaviors of bicontinuous cubic mesoporous silica from triblock copolymer mixed anionic surfactant , 2007 .

[22]  M. Vallet‐Regí,et al.  Mesoporous bioactive scaffolds prepared with cerium-, gallium- and zinc-containing glasses. , 2013, Acta biomaterialia.

[23]  A R Boccaccini,et al.  Biomedical coatings on magnesium alloys - a review. , 2012, Acta biomaterialia.

[24]  J. Lu,et al.  Role of interconnections in porous bioceramics on bone recolonization in vitro and in vivo , 1999, Journal of materials science. Materials in medicine.

[25]  M. Vallet‐Regí,et al.  The osteoinductive properties of mesoporous silicate coated with osteostatin in a rabbit femur cavity defect model. , 2010, Biomaterials.

[26]  M. Vallet‐Regí,et al.  Medical applications of organic-inorganic hybrid materials within the field of silica-based bioceramics. , 2011, Chemical Society reviews.

[27]  M. S. Yong,et al.  In vitro degradation behavior of M1A magnesium alloy in protein-containing simulated body fluid , 2011 .

[28]  M. Vallet‐Regí,et al.  Effect of the continuous solution exchange on the in vitro reactivity of a CaO-SiO(2) sol-gel glass. , 2000, Journal of biomedical materials research.

[29]  A. Boccaccini,et al.  Biodegradable and bioactive porous polymer/inorganic composite scaffolds for bone tissue engineering. , 2006, Biomaterials.

[30]  R. Reis,et al.  Novel hydroxyapatite/carboxymethylchitosan composite scaffolds prepared through an innovative "autocatalytic" electroless coprecipitation route. , 2009, Journal of biomedical materials research. Part A.

[31]  M. Vallet‐Regí,et al.  New Nanocomposite System with Nanocrystalline Apatite Embedded into Mesoporous Bioactive Glass , 2012 .

[32]  M. Vallet‐Regí,et al.  Essential Role of Calcium Phosphate Heterogeneities in 2D-Hexagonal and 3D-Cubic SiO2−CaO−P2O5 Mesoporous Bioactive Glasses , 2009 .

[33]  Julian R Jones,et al.  Review of bioactive glass: from Hench to hybrids. , 2013, Acta biomaterialia.

[34]  O. Terasaki,et al.  High-performance mesoporous bioceramics mimicking bone mineralization , 2008 .

[35]  Matthias Epple,et al.  Biological and medical significance of calcium phosphates. , 2002, Angewandte Chemie.

[36]  T. Peltola,et al.  Calcium phosphate formation on porous sol-gel-derived SiO2 and CaO-P2O5-SiO2 substrates in vitro. , 1999, Journal of biomedical materials research.

[37]  J M Polak,et al.  Scaffolds and biomaterials for tissue engineering: a review of clinical applications. , 2003, Clinical otolaryngology and allied sciences.

[38]  K. Leong,et al.  The design of scaffolds for use in tissue engineering. Part II. Rapid prototyping techniques. , 2002, Tissue engineering.

[39]  Rozalia Dimitriou,et al.  Bone regeneration: current concepts and future directions , 2011, BMC medicine.

[40]  Shan Zhao,et al.  Synthesis of CaO–SiO2–P2O5 mesoporous bioactive glasses with high P2O5 content by evaporation induced self assembly process , 2011, Journal of materials science. Materials in medicine.

[41]  Scott J Hollister,et al.  Mechanical and in vivo performance of hydroxyapatite implants with controlled architectures. , 2002, Biomaterials.

[42]  M. Vallet‐Regí,et al.  Substitutions of cerium, gallium and zinc in ordered mesoporous bioactive glasses. , 2011, Acta biomaterialia.

[43]  J. Mackenzie,et al.  Bioactivity of sol–gel derived organically modified silicates: Part I: In vitro examination , 1997, Journal of materials science. Materials in medicine.

[44]  María Vallet-Regí,et al.  From the bioactive glasses to the star gels , 2006, Journal of materials science. Materials in medicine.

[45]  M. Vallet‐Regí,et al.  Bioactivity of three CaO-P2O5-SiO2 sol-gel glasses. , 2002, Journal of biomedical materials research.

[46]  Y. Catonné,et al.  Clinical, radiological and histological evaluation of biphasic calcium phosphate bioceramic wedges filling medial high tibial valgisation osteotomies. , 2009, The Knee.

[47]  J. M. Merino,et al.  Microstructure and macroscopic properties of bioactive CaO-SiO2-PDMS hybrids. , 2007, Journal of biomedical materials research. Part B, Applied biomaterials.

[48]  M. Bohner,et al.  Technological issues for the development of more efficient calcium phosphate bone cements: a critical assessment. , 2005, Biomaterials.

[49]  Galen D. Stucky,et al.  Rapid‐Setting, Mesoporous, Bioactive Glass Cements that Induce Accelerated In Vitro Apatite Formation , 2006 .

[50]  W. Vogel,et al.  Development of machineable bioactive glass ceramics for medical uses , 1986 .

[51]  M. Vallet‐Regí,et al.  A tissue engineering approach based on the use of bioceramics for bone repair. , 2013, Biomaterials science.

[52]  Larry L. Hench,et al.  Bioglass ®45S5 Stimulates Osteoblast Turnover and Enhances Bone Formation In Vitro: Implications and Applications for Bone Tissue Engineering , 2000, Calcified Tissue International.

[53]  D. Castner,et al.  Biomedical surface science: Foundations to frontiers , 2002 .

[54]  D. Heymann,et al.  Ultrastructural evidence in vitro of osteoclast-induced degradation of calcium phosphate ceramic by simultaneous resorption and phagocytosis mechanisms. , 2001, Histology and histopathology.

[55]  P. Ducheyne Stimulation of Biological Function With Bioactive Glass , 1998 .

[56]  Larry L Hench,et al.  Third-Generation Biomedical Materials , 2002, Science.

[57]  W. den Hollander,et al.  Macroporous calcium phosphate bioceramics in dog femora: a histological study of interface and biodegradation. , 1989, Biomaterials.

[58]  Chikara Ohtsuki,et al.  Mechanism of apatite formation on CaOSiO2P2O5 glasses in a simulated body fluid , 1992 .

[59]  Min Wang,et al.  Developing bioactive composite materials for tissue replacement. , 2003, Biomaterials.

[60]  L L Hench,et al.  An investigation of bioactive glass powders by sol-gel processing. , 1991, Journal of applied biomaterials : an official journal of the Society for Biomaterials.

[61]  M. Vallet‐Regí,et al.  Osteostatin-loaded onto mesoporous ceramics improves the early phase of bone regeneration in a rabbit osteopenia model. , 2012, Acta biomaterialia.

[62]  S. McNally,et al.  The results at nine to twelve years of the use of a hydroxyapatite-coated femoral stem. , 2000, The Journal of bone and joint surgery. British volume.

[63]  Tadashi Kokubo,et al.  How useful is SBF in predicting in vivo bone bioactivity? , 2006, Biomaterials.

[64]  M. Vallet‐Regí,et al.  Bioactive CaO−SiO2−PDMS Coatings on Ti6Al4V Substrates , 2005 .

[65]  R. Legeros,et al.  Calcium phosphate-based osteoinductive materials. , 2008, Chemical reviews.

[66]  A. Boccaccini,et al.  Therapeutic inorganic ions in bioactive glasses to enhance bone formation and beyond. , 2013, Biomaterials science.

[67]  G. Daculsi,et al.  Biphasic calcium phosphate concept applied to artificial bone, implant coating and injectable bone substitute. , 1998, Biomaterials.

[68]  T. Kokubo,et al.  Apatite formation on PDMS-modified CaO-SiO2-TiO2 hybrids prepared by sol-gel process. , 1999, Biomaterials.

[69]  J. Vacanti,et al.  Tissue engineering : Frontiers in biotechnology , 1993 .

[70]  M. Vallet‐Regí,et al.  Osteostatin-loaded bioceramics stimulate osteoblastic growth and differentiation. , 2010, Acta biomaterialia.

[71]  Delbert E Day,et al.  Bioactive glass in tissue engineering. , 2011, Acta biomaterialia.

[72]  Aldo R Boccaccini,et al.  A review of the biological response to ionic dissolution products from bioactive glasses and glass-ceramics. , 2011, Biomaterials.

[73]  M. Vallet‐Regí,et al.  Promising trends of bioceramics in the biomaterials field , 2009, Journal of materials science. Materials in medicine.

[74]  Eui Kyun Park,et al.  Bioactive glass–poly (ε-caprolactone) composite scaffolds with 3 dimensionally hierarchical pore networks , 2011 .

[75]  Takashi Nakamura,et al.  Apatite formation on zirconium metal treated with aqueous NaOH. , 2002, Biomaterials.

[76]  María Vallet-Regí,et al.  Preparation of 3-D scaffolds in the SiO2-P2O5 system with tailored hierarchical meso-macroporosity. , 2011, Acta biomaterialia.

[77]  M. Vallet‐Regí,et al.  Glasses with Medical Applications , 2003 .

[78]  T. Kokubo,et al.  Bioactive Ti Metal and its Alloys Prepared by Chemical Treatments: State‐of‐the‐Art and Future Trends , 2010 .

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

[80]  María Vallet-Regí,et al.  Structure and functionalization of mesoporous bioceramics for bone tissue regeneration and local drug delivery , 2012, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[81]  María Vallet-Regí,et al.  Ordered Mesoporous Bioactive Glasses for Bone Tissue Regeneration , 2006 .

[82]  T. Kokubo Surface chemistry of bioactive glass-ceramics , 1990 .

[83]  M. Hupa,et al.  Dissolution patterns of biocompatible glasses in 2-amino-2-hydroxymethyl-propane-1,3-diol (Tris) buffer. , 2013, Acta biomaterialia.

[84]  M. Vallet‐Regí Nanostructured mesoporous silica matrices in nanomedicine , 2010, Journal of internal medicine.

[85]  M. Vallet‐Regí,et al.  Nanostructure of Bioactive Sol−Gel Glasses and Organic−Inorganic Hybrids , 2005 .

[86]  María Vallet-Regí,et al.  Bioceramics: From Bone Regeneration to Cancer Nanomedicine , 2011, Advanced materials.

[87]  P. Ducheyne,et al.  Bioactive glass particles of narrow size range for the treatment of oral bone defects: a 1-24 month experiment with several materials and particle sizes and size ranges. , 1997, Journal of oral rehabilitation.

[88]  J. Jansen,et al.  Subperiosteal implantation of various RF magnetron sputtered Ca-P coatings in goats. , 1998, Journal of biomedical materials research.

[89]  T. Albrektsson,et al.  Osteoinduction, osteoconduction and osseointegration , 2001, European Spine Journal.

[90]  J. Pou,et al.  Micro- and nano-testing of calcium phosphate coatings produced by pulsed laser deposition. , 2003, Biomaterials.

[91]  A. Boccaccini,et al.  Sol–gel based fabrication and characterization of new bioactive glass–ceramic composites for dental applications , 2012 .

[92]  Larry L. Hench,et al.  The story of Bioglass® , 2006, Journal of materials science. Materials in medicine.

[93]  K A Gross,et al.  Material fundamentals and clinical performance of plasma-sprayed hydroxyapatite coatings: a review. , 2001, Journal of biomedical materials research.

[94]  M. Vallet‐Regí,et al.  Revisiting silica based ordered mesoporous materials: medical applications , 2006 .

[95]  Aldo R Boccaccini,et al.  45S5 Bioglass-derived glass-ceramic scaffolds for bone tissue engineering. , 2006, Biomaterials.

[96]  Rui L Reis,et al.  Bone tissue engineering: state of the art and future trends. , 2004, Macromolecular bioscience.

[97]  D. Kaplan,et al.  Porosity of 3D biomaterial scaffolds and osteogenesis. , 2005, Biomaterials.

[98]  María Vallet-Regí,et al.  Bioactive Star Gels , 2006 .

[99]  S. Radin,et al.  In Vitro Behavior of Silica-Based Xerogels Intended as Controlled Release Carriers , 1999 .

[100]  M. Vallet‐Regí,et al.  Evolution of Ceramics with Medical Applications , 2007 .

[101]  Xufeng Zhou,et al.  Highly ordered mesoporous bioactive glasses with superior in vitro bone-forming bioactivities. , 2004, Angewandte Chemie.

[102]  S. Heo,et al.  Hierarchically mesoporous-macroporous bioactive glasses scaffolds for bone tissue regeneration. , 2008, Journal of biomedical materials research. Part B, Applied biomaterials.

[103]  Anna Carlsson,et al.  Structural study of mesoporous MCM-48 and carbon networks synthesized in the spaces of MCM-48 by electron crystallography , 2002 .

[104]  V. Parikka,et al.  Intact surface of bioactive glass S53P4 is resistant to osteoclastic activity. , 2006, Journal of biomedical materials research. Part A.

[105]  J. Planell,et al.  Effect of the particle size on the micro and nanostructural features of a calcium phosphate cement: a kinetic analysis. , 2004, Biomaterials.

[106]  Sumio Sakka,et al.  Mechanical properties of a new type of apatite-containing glass-ceramic for prosthetic application , 1985 .

[107]  D. Greenspan,et al.  Processing and properties of sol-gel bioactive glasses. , 2000, Journal of biomedical materials research.

[108]  S. Bhaduri,et al.  Effect of carbonate content and buffer type on calcium phosphate formation in SBF solutions , 2006, Journal of materials science. Materials in medicine.