Bioactive Glass and Glass-Ceramic Scaffolds for Bone Tissue Engineering

Materials - Tập 3 Số 7 - Trang 3867-3910
L.‐C. Gerhardt1, Aldo R. Boccaccını2,3
1Department of Materials, Imperial College London, Prince Consort Road, London SW7 2BP, UK
2Department of Materials, Imperial College London, Prince Consort Road, London SW7 2BP, UK. [email protected].
3Institute of Biomaterials, University of Erlangen-Nuremberg, 91058 Erlangen, Germany. [email protected].

Tóm tắt

Traditionally, bioactive glasses have been used to fill and restore bone defects. More recently, this category of biomaterials has become an emerging research field for bone tissue engineering applications. Here, we review and discuss current knowledge on porous bone tissue engineering scaffolds on the basis of melt-derived bioactive silicate glass compositions and relevant composite structures. Starting with an excerpt on the history of bioactive glasses, as well as on fundamental requirements for bone tissue engineering scaffolds, a detailed overview on recent developments of bioactive glass and glass-ceramic scaffolds will be given, including a summary of common fabrication methods and a discussion on the microstructural-mechanical properties of scaffolds in relation to human bone (structure-property and structure-function relationship). In addition, ion release effects of bioactive glasses concerning osteogenic and angiogenic responses are addressed. Finally, areas of future research are highlighted in this review.

Từ khóa


Tài liệu tham khảo

Hench, 2002, Third-generation biomedical materials, Science, 295, 1014, 10.1126/science.1067404

Williams, 2004, Benefit and risk in tissue engineering, Mater. Today, 7, 24, 10.1016/S1369-7021(04)00232-9

Guarino, 2007, Bioactive scaffolds for bone and ligament tissue, Expert Rev. Med. Devices, 4, 405, 10.1586/17434440.4.3.405

Hutmacher, 2007, State of the art and future directions of scaffold-based bone engineering from a biomaterials perspective, J. Tissue Eng. Regen. Med., 1, 245, 10.1002/term.24

Hench, 1998, Bioceramics, J. Am. Ceram. Soc., 81, 1705, 10.1111/j.1151-2916.1998.tb02540.x

Kokubo, 2003, Novel bioactive materials with different mechanical properties, Biomaterials, 24, 2161, 10.1016/S0142-9612(03)00044-9

Xynos, 2001, Gene-expression profiling of human osteoblasts following treatment with the ionic products of Bioglass® 45S5 dissolution, J. Biomed. Mater. Res., 55, 151, 10.1002/1097-4636(200105)55:2<151::AID-JBM1001>3.0.CO;2-D

Hench, 2006, The story of Bioglass®, J. Mater. Sci. Mater. Med., 17, 967, 10.1007/s10856-006-0432-z

Hench, 1971, Bonding mechanisms at the interface of ceramic prosthetic materials, J. Biomed. Mater. Res., 5, 117, 10.1002/jbm.820050611

Jones, 2009, New trends in bioactive scaffolds: The importance of nanostructure, J. Eur. Ceram. Soc., 29, 1275, 10.1016/j.jeurceramsoc.2008.08.003

Hench, 1991, Bioceramics: from concept to clinic, J. Am. Ceram. Soc., 74, 1487, 10.1111/j.1151-2916.1991.tb07132.x

Hench, 1993, Bioactive glasses, An Introduction to Bioceramics, Volume 1, 41, 10.1142/9789814317351_0003

Miola, 2008, 3D-glass-ceramic scaffolds with antibacterial properties for bone grafting, Chem. Eng. J., 137, 129, 10.1016/j.cej.2007.07.083

Verne, 2005, Microstructural and in vitro characterization of SiO2-Na2O-CaO-MgO glass-ceramic bioactive scaffolds for bone substitutes, J. Mater. Sci. Mater. Med., 16, 909, 10.1007/s10856-005-4425-0

Verne, 2007, Development of glass-ceramic scaffolds for bone tissue engineering: characterisation, proliferation of human osteoblasts and nodule formation, Acta Biomater., 3, 199, 10.1016/j.actbio.2006.07.012

Gentleman, 2010, The effects of strontium-substituted bioactive glasses on osteoblasts and osteoclasts in vitro, Biomaterials, 31, 3949, 10.1016/j.biomaterials.2010.01.121

Pan, H.B., Zhao, X.L., Zhang, X., Zhang, K. B., Li, L.C., Li, Z.Y., Lam, W.M., Lu, W.W., Wang, D.P., Huang, W.H., Lin, K.L., and Chang, J. Strontium borate glass: Potential biomaterial for bone regeneration. J. Roy. Soc. Interface, in press.

Hill, 2010, Influence of strontium and the importance of glass chemistry and structure when designing bioactive glasses for bone regeneration, Acta Biomater., 6, 2382, 10.1016/j.actbio.2010.01.006

Hsi, 2007, Crystallization kinetics and magnetic properties of iron oxide contained 25Li2O-8MnO2-20CaO-2P2O5-45SiO2 glasses, J. Eur. Ceram. Soc., 27, 3171, 10.1016/j.jeurceramsoc.2006.11.081

Balamurugan, 2008, An in vitro biological and anti-bacterial study on a sol-gel derived silver-incorporated bioglass system, Dental Mater., 24, 1343, 10.1016/j.dental.2008.02.015

Bellantone, 2002, Broad-spectrum bactericidal activity of Ag2O-doped bioactive glass, Antimicrob. Agents Chemother., 46, 1940, 10.1128/AAC.46.6.1940-1945.2002

Blaker, 2004, Development and characterisation of silver-doped bioactive glass-coated sutures for tissue engineering and wound healing applications, Biomaterials, 25, 1319, 10.1016/j.biomaterials.2003.08.007

Delben, 2009, Synthesis and thermal properties of nanoparticles of bioactive glasses containing silver, J. Therm. Anal. Calorim., 97, 433, 10.1007/s10973-009-0086-4

Liu, 2009, Bioactive borosilicate glass scaffolds: improvement on the strength of glass-based scaffolds for tissue engineering, J. Mater. Sci. Mater. Med., 20, 365, 10.1007/s10856-008-3582-3

Liu, 2009, Bioactive borosilicate glass scaffolds: in vitro degradation and bioactivity behaviors, J. Mater. Sci. Mater. Med., 20, 1237, 10.1007/s10856-009-3691-7

Munukka, 2008, Bactericidal effects of bioactive glasses on clinically important aerobic bacteria, J. Mater. Sci. Mater. Med., 19, 27, 10.1007/s10856-007-3143-1

Gorriti, 2009, In vitro study of the antibacterial activity of bioactive glass-ceramic scaffolds, Adv. Eng. Mater., 11, B67, 10.1002/adem.200900081

Cannillo, 2009, Potassium-based composition for a bioactive glass, Ceram. Int., 35, 3389, 10.1016/j.ceramint.2009.06.011

Aina, 2009, Zinc-containing bioactive glasses: Surface reactivity and behaviour towards endothelial cells, Acta Biomater., 5, 1211, 10.1016/j.actbio.2008.10.020

Haimi, 2009, Characterization of zinc-releasing three-dimensional bioactive glass scaffolds and their effect on human adipose stem cell proliferation and osteogenic differentiation, Acta Biomater., 5, 3122, 10.1016/j.actbio.2009.04.006

Misra, 2006, Polyhydroxyalkanoate (PHA)/inorganic phase composites for tissue engineering applications, Biomacromolecules, 7, 2249, 10.1021/bm060317c

Chen, 2008, Investigation on bio-mineralization of melt and sol-gel derived bioactive glasses, Appl. Surf. Sci., 255, 562, 10.1016/j.apsusc.2008.06.101

Boccaccini, 2007, Bioactive ceramics and glasses, Tissue Engineering Using Ceramics and Polymers, Volume 1, 52

Gupta, 2008, Bioactive materials for biomedical applications using sol-gel technology, Biomed. Mater., 3, 034005, 10.1088/1748-6041/3/3/034005

Wilson, 1981, Toxicology and biocompatibility of bioglasses, J. Biomed. Mater. Res., 15, 805, 10.1002/jbm.820150605

Hench, 2004, Bioactive glasses for in situ tissue regeneration, J. Biomater. Sci.-Polym. Ed., 15, 543, 10.1163/156856204323005352

Rezwan, 2006, Biodegradable and bioactive porous polymer/inorganic composite scaffolds for bone tissue engineering, Biomaterials, 27, 3413, 10.1016/j.biomaterials.2006.01.039

Yang, 2001, The design of scaffolds for use in tissue engineering. Part I. Traditional factors, Tissue Eng., 7, 679, 10.1089/107632701753337645

Garcia, 1998, Effect of surface reaction stage on fibronectin-mediated adhesion of osteoblast-like cells to bioactive glass, J. Biomed. Mater. Res., 40, 48, 10.1002/(SICI)1097-4636(199804)40:1<48::AID-JBM6>3.0.CO;2-R

Ylanen, 1999, Porous bioactive glass matrix in reconstruction of articular osteochondral defects, Ann. Chir. Gynaecol., 88, 237

Xynos, 2000, Bioglass® 45S5 stimulates osteoblast turnover and enhances bone formation in vitro: Implications and applications for bone tissue engineering, Calcif. Tissue Int., 67, 321, 10.1007/s002230001134

Boccaccini, 2003, Bioresorbable and bioactive polymer/Bioglass® composites with tailored pore structure for tissue engineering applications, Compos. Sci. Technol., 63, 2417, 10.1016/S0266-3538(03)00275-6

Chen, 2006, 45S5 Bioglass®-derived glass-ceramic scaffolds for bone tissue engineering, Biomaterials, 27, 2414, 10.1016/j.biomaterials.2005.11.025

Brunner, T.J., Grass, R.N., and Stark, W.J. (2006). Glass and bioglass nanopowders by flame synthesis. Chem. Commun., 1384–1386.

Vollenweider, 2007, Remineralization of human dentin using ultrafine bioactive glass particles, Acta Biomater., 3, 936, 10.1016/j.actbio.2007.04.003

Misra, 2010, Effect of nanoparticulate bioactive glass particles on bioactivity and cytocompatibility of poly(3-hydroxybutyrate) composites, J. Roy. Soc. Interface, 7, 453, 10.1098/rsif.2009.0255

Misra, 2010, Poly(3-hydroxybutyrate) multifunctional composite scaffolds for tissue engineering applications, Biomaterials, 31, 2806, 10.1016/j.biomaterials.2009.12.045

Misra, 2008, Comparison of nanoscale and microscale bioactive glass on the properties of P(3HB)/Bioglass composites, Biomaterials, 29, 1750, 10.1016/j.biomaterials.2007.12.040

Liu, 2008, Surface modification of bioactive glass nanoparticles and the mechanical and biological properties of poly(L-lactide) composites, Acta Biomater., 4, 1005, 10.1016/j.actbio.2008.02.013

Lu, 2003, Three-dimensional, bioactive, biodegradable, polymer-bioactive glass composite scaffolds with improved mechanical properties support collagen synthesis and mineralization of human osteoblast-like cells in vitro, J. Biomed. Mater. Res. Part A, 64, 465, 10.1002/jbm.a.10399

Hench, 2009, Genetic design of bioactive glass, J. Eur. Ceram. Soc., 29, 1257, 10.1016/j.jeurceramsoc.2008.08.002

Ghosh, 2008, In vivo response of porous hydroxyapatite and beta-tricalcium phosphate prepared by aqueous solution combustion method and comparison with bioglass scaffolds, J. Biomed. Mater. Res. B Appl. Biomater., 86, 217, 10.1002/jbm.b.31009

Gorustovich, 2010, Effect of bioactive glasses on angiogenesis: In-vitro and in-vivo evidence. A review, Tissue Eng. Part B Rev., 16, 199, 10.1089/ten.teb.2009.0416

Day, 2005, Bioactive glass stimulates the secretion of angiogenic growth factors and angiogenesis in vitro, Tissue Eng., 11, 768, 10.1089/ten.2005.11.768

Day, 2005, In vitro and in vivo analysis of macroporous biodegradable poly(D,L-lactide-co-glycolide) scaffolds containing bioactive glass, J. Biomed. Mater. Res. Part A, 75, 778, 10.1002/jbm.a.30433

Leu, 2008, Proangiogenic potential of a collagen/bioactive glass substrate, Pharm. Res., 25, 1222, 10.1007/s11095-007-9508-9

Mortera, 2008, Synthesis and characterization of MCM-41 spheres inside bioactive glass-ceramic scaffold, Chem. Eng. J., 137, 54, 10.1016/j.cej.2007.07.094

Cauda, 2008, SBA-15 ordered mesoporous silica inside a bioactive glass-ceramic scaffold for local drug delivery, J. Mater. Sci. Mater. Med., 19, 3303, 10.1007/s10856-008-3468-4

2004, Advanced bioceramic composite for bone tissue engineering: design principles and structure-bioactivity relationship, J. Biomed. Mater. Res. Part A, 69, 490

Francis, 2010, Multi-functional P(3HB) microsphere/45S5 Bioglass®-based composite scaffolds for bone tissue engineering, Acta Biomater., 6, 2773, 10.1016/j.actbio.2009.12.054

Habraken, 2007, Ceramic composites as matrices and scaffolds for drug delivery in tissue engineering, Adv. Drug Deliv. Rev., 59, 234, 10.1016/j.addr.2007.03.011

Juan, 2009, The incorporation of 70s bioactive glass to the osteogenic differentiation of murine embryonic stem cells in 3D bioreactors, J. Tissue Eng. Regen. Med., 3, 63, 10.1002/term.135

Lin, 2003, Biphasic calcium phosphate bioceramics: Preparation, properties and applications, J. Mater. Sci. Mater. Med., 14, 201, 10.1023/A:1021559700915

Zhu, 2009, Comparison of the in vitro bioactivity and drug release property of mesoporous bioactive glasses (MBGs) and bioactive glasses (BGs) scaffolds, Micropor. Mesopor. Mater., 118, 176, 10.1016/j.micromeso.2008.08.046

Ostomel, 2006, Spherical bioactive glass with enhanced rates of hydroxyapatite deposition and hemostatic activity, Small, 2, 1261, 10.1002/smll.200600177

Bretcanu, 2006, Synthesis and characterization of coprecipitation-derived ferrimagnetic glass-ceramic, J. Mater. Sci., 41, 1029, 10.1007/s10853-005-2636-x

Li, 2010, Synthesis and characterization of magnetic bioactive glass-ceramics containing Mg ferrite for hyperthermia, Mater. Sci. Eng. C, 30, 148, 10.1016/j.msec.2009.09.011

Kawashita, 2004, Preparation of class-ceramics containing ferrimagnetic zinc-iron ferrite for the hyperthermal treatment of cancer, J. Ceram. Soc. Jpn., 112, 373, 10.2109/jcersj.112.373

Shah, 2010, Magnetic and bioactivity evaluation of ferrimagnetic ZnFe2O4 containing glass ceramics for the hyperthermia treatment of cancer, J. Magn. Magn. Mater., 322, 375, 10.1016/j.jmmm.2009.09.063

Thompson, 1998, Mechanical properties of bioactive glasses, glass-ceramics and composites, Proc. Inst. Mech. Eng. Part H-J. Eng. Med., 212, 127, 10.1243/0954411981533908

Kokubo, 1985, Mechanical-properties of a new type of apatite-containing glass-ceramic for prosthetic application, J. Mater. Sci., 20, 2001, 10.1007/BF01112282

Nakamura, 1985, A new glass-ceramic for bone replacement-evaluation of its bonding to bone, J. Biomed. Mater. Res., 19, 685, 10.1002/jbm.820190608

Wu, 2009, Methods of improving mechanical and biomedical properties of Ca-Si-based ceramics and scaffolds, Expert Rev. Med. Devices, 6, 237, 10.1586/erd.09.3

Karageorgiou, 2005, Porosity of 3D biomaterial scaffolds and osteogenesis, Biomaterials, 26, 5474, 10.1016/j.biomaterials.2005.02.002

Yang, 2002, The design of scaffolds for use in tissue engineering. Part II. Rapid prototyping techniques, Tissue Eng., 8, 1, 10.1089/107632702753503009

Yun, H.S., Kim, S.E., and Hyeon, Y.T. (2007). Design and preparation of bioactive glasses with hierarchical pore networks. Chem. Commun., 2139–2141.

Yunos, 2008, Polymer-bioceramic composites for tissue engineering scaffolds, J. Mater. Sci., 43, 4433, 10.1007/s10853-008-2552-y

Coleman, 2000, Tensile properties of bioactive fibers for tissue engineering applications, J. Biomed. Mater. Res., 53, 199, 10.1002/(SICI)1097-4636(2000)53:3<199::AID-JBM2>3.0.CO;2-J

Taboas, 2003, Indirect solid free form fabrication of local and global porous, biomimetic and composite 3D polymer-ceramic scaffolds, Biomaterials, 24, 181, 10.1016/S0142-9612(02)00276-4

Oliveira, 2003, Nature-inspired calcium phosphate coatings: present status and novel advances in the science of mimicry, Curr. Opin. Solid State Mater. Sci., 7, 309, 10.1016/j.cossms.2003.10.009

Boccaccini, 2005, Bioactive composite materials for tissue engineering scaffolds, Expert Rev. Med. Devices, 2, 303, 10.1586/17434440.2.3.303

Berry, 2006, The interaction of human bone marrow cells with nanotopographical features in three dimensional constructs, J. Biomed. Mater. Res. Part A, 79A, 431, 10.1002/jbm.a.30960

Stevens, 2005, Exploring and engineering the cell surface interface, Science, 310, 1135, 10.1126/science.1106587

Webster, 2007, Nanostructured biomaterials for tissue engineering bone, Tissue Engineering II, Volume 103, 275

Hench, 2004, Bioglass®: A short history and bibliography, J. Aust. Ceram. Soc., 40, 1

Best, 2008, Bioceramics: Past, present and for the future, J. Eur. Ceram. Soc., 28, 1319, 10.1016/j.jeurceramsoc.2007.12.001

Chevalier, 2009, Ceramics for medical applications: A picture for the next 20 years, J. Eur. Ceram. Soc., 29, 1245, 10.1016/j.jeurceramsoc.2008.08.025

Arcos, 2009, Promising trends of bioceramics in the biomaterials field, J. Mater. Sci. Mater. Med., 20, 447, 10.1007/s10856-008-3616-x

Boccaccini, 2010, Carbon nanotube composite scaffolds and coatings for tissue engineering applications, Key Engineering Materials: Advanced Bioceramics in Nanomedicine and Tissue Engineering, Volume 441, 31, 10.4028/www.scientific.net/KEM.441.31

Ramakrishna, 2001, Biomedical applications of polymer-composite materials: A review, Compos. Sci. Technol., 61, 1189, 10.1016/S0266-3538(00)00241-4

Tabata, 2009, Biomaterial technology for tissue engineering applications, J. Roy. Soc. Interface, 6, S311, 10.1098/rsif.2008.0448.focus

Smith, 2006, Confocal laser scanning microscopy as a tool for imaging cancellous bone, J. Biomed. Mater. Res. B Appl. Biomater., 79, 185, 10.1002/jbm.b.30529

Woodard, 2007, The mechanical properties and osteoconductivity of hydroxyapatite bone scaffolds with multi-scale porosity, Biomaterials, 28, 45, 10.1016/j.biomaterials.2006.08.021

Baino, 2009, High strength bioactive glass-ceramic scaffolds for bone regeneration, J. Mater. Sci. Mater. Med., 20, 643, 10.1007/s10856-008-3605-0

Ochoa, 2009, Permeability evaluation of 45S5 Bioglass®-based scaffolds for bone tissue engineering, J. Biomech., 42, 257, 10.1016/j.jbiomech.2008.10.030

Hench, 2005, Ceramics, Biomaterials, artificial organs and tissue engineering, Volume 1, 26

Boccaccini, 2007, Sintering, crystallisation and biodegradation behaviour of Bioglass-derived glass-ceramics, Faraday Discuss., 136, 27, 10.1039/b616539g

Hench, 2005, Biocomposites, Biomaterials, Artificial Organs and Tissue Engineering, Volume 1, 48

Fu, 2010, Preparation and in vitro evaluation of bioactive glass (13-93) scaffolds with oriented microstructures for repair and regeneration of load-bearing bones, J. Biomed. Mater. Res. Part A, 93A, 1380, 10.1002/jbm.a.32637

Kanczler, 2008, Osteogenesis and angiogenesis: the potential for engineering bone, Eur. Cells Mater., 15, 100, 10.22203/eCM.v015a08

Deville, 2006, Freezing as a path to build complex composites, Science, 311, 515, 10.1126/science.1120937

Baino, 2009, 3-D high-strength glass-ceramic scaffolds containing fluoroapatite for load-bearing bone portions replacement, Mater. Sci. Eng. C, 29, 2055, 10.1016/j.msec.2009.04.002

Bretcanu, 2008, Simple methods to fabricate Bioglass®-derived glass-ceramic scaffolds exhibiting porosity gradient, J. Mater. Sci., 43, 4127, 10.1007/s10853-008-2536-y

Vitale-Brovarone, C., Baino, F., and Verne, E. (2009). Feasibility and tailoring of bioactive glass-ceramic scaffolds with gradient of porosity for bone grafting. J. Biomater. Appl.

Fu, 2008, Mechanical and in vitro performance of 13-93 bioactive glass scaffolds prepared by a polymer foam replication technique, Acta Biomater., 4, 1854, 10.1016/j.actbio.2008.04.019

Brovarone, 2006, Macroporous bioactive glass-ceramic scaffolds for tissue engineering, J. Mater. Sci. Mater. Med., 17, 1069, 10.1007/s10856-006-0533-8

Fu, 2007, Preparation and bioactive characteristics of a porous 13-93 glass, and fabrication into the articulating surface of a proximal tibia, J. Biomed. Mater. Res. Part A, 82, 222, 10.1002/jbm.a.31156

Renghini, 2009, Micro-CT studies on 3-D bioactive glass-ceramic scaffolds for bone regeneration, Acta Biomater., 5, 1328, 10.1016/j.actbio.2008.10.017

Chen, 2006, The surface functionalization of 45S5 Bioglass®-based glass-ceramic scaffolds and its impact on bioactivity, J. Mater. Sci. Mater. Med., 17, 979, 10.1007/s10856-006-0433-y

Chen, 2007, Surface functionalization of Bioglass®-derived porous scaffolds, Acta Biomater., 3, 551, 10.1016/j.actbio.2007.01.008

Klein, 2009, Pore characteristics of bone substitute materials assessed by microcomputed tomography, Clin. Oral. Implants Res., 20, 67, 10.1111/j.1600-0501.2008.01605.x

Kohlhauser, 2009, Ultrasonic characterisation of porous biomaterials across different frequencies, Strain, 45, 34, 10.1111/j.1475-1305.2008.00417.x

Moimas, 2006, Rabbit pilot study on the resorbability of three-dimensional bioactive glass fibre scaffolds, Acta Biomater., 2, 191, 10.1016/j.actbio.2005.09.006

Brown, 2008, Growth and differentiation of osteoblastic cells on 13-93 bioactive glass fibers and scaffolds, Acta Biomater., 4, 387, 10.1016/j.actbio.2007.07.006

Bretcanu, 2004, Macroporous glass-ceramic materials with bioactive properties, J. Mater. Sci. Mater. Med., 15, 209, 10.1023/B:JMSM.0000015480.49061.e1

Verne, 2008, Biocompatible glass-ceramic materials for bone substitution, J. Mater. Sci. Mater. Med., 19, 471, 10.1007/s10856-006-0111-0

Baino, 2009, Foam-like scaffolds for bone tissue engineering based on a novel couple of silicate-phosphate specular glasses: synthesis and properties, J. Mater. Sci. Mater. Med., 20, 2197, 10.1007/s10856-009-3788-z

Chen, 2008, Bioglass-derived glass-ceramic scaffolds: study of cell proliferation and scaffold degradation in vitro, J. Biomed. Mater. Res. Part A, 84, 1049, 10.1002/jbm.a.31512

Deb, 2010, A porous scaffold for bone tissue engineering/45S5 Bioglass® derived porous scaffolds for co-culturing osteoblasts and endothelial cells, J. Mater. Sci. Mater. Med., 21, 893, 10.1007/s10856-009-3936-5

Vargas, 2009, Biocompatibility and bone mineralization potential of 45S5 Bioglass®-derived glass-ceramic scaffolds in chick embryos, Acta Biomater., 5, 374, 10.1016/j.actbio.2008.07.016

Nandi, 2009, The repair of segmental bone defects with porous bioglass: An experimental study in goat, Res. Vet. Sci., 86, 162, 10.1016/j.rvsc.2008.04.008

Mahmood, 2001, Geometric effect of matrix upon cell differentiation: BMP-induced osteogenesis using a new bioglass with a feasible structure, J. Biochem., 129, 163, 10.1093/oxfordjournals.jbchem.a002828

Mantsos, 2009, Non-crystalline composite tissue engineering scaffolds using boron-containing bioactive glass and poly(D,L-lactic acid) coatings, Biomed. Mater., 4, 55002, 10.1088/1748-6041/4/5/055002

San Miguel, B., Kriauciunas, R., Tosatti, S., Ehrbar, M., Ghayor, C., Textor, M., and Weber, F.E. Enhanced osteoblastic activity and bone regeneration using surface-modified porous bioactive glass scaffolds. J. Biomed. Mater. Res. Part A, in press.

Hernandez, 2001, The influence of bone volume fraction and ash fraction on bone strength and modulus, Bone, 29, 74, 10.1016/S8756-3282(01)00467-7

Keaveny, 2001, Biomechanics of trabecular bone, Annu. Rev. Biomed. Eng., 3, 307, 10.1146/annurev.bioeng.3.1.307

Sun, 2008, Difference in femoral head and neck material properties between osteoarthritis and osteoporosis, Clin. Biomech., 23, S39, 10.1016/j.clinbiomech.2007.11.018

Nazarian, 2008, Bone volume fraction explains the variation in strength and stiffness of cancellous bone affected by metastatic cancer and osteoporosis, Calcif. Tissue Int., 83, 368, 10.1007/s00223-008-9174-x

Hench, 1993, Introduction, An introduction to bioceramics, Volume 1, 1

Clupper, 2004, Bioactive evaluation of 45S5 bioactive glass fibres and preliminary study of human osteoblast attachment, J. Mater. Sci. Mater. Med., 15, 803, 10.1023/B:JMSM.0000032821.32577.fc

Clupper, 2004, Strength and toughness of tape cast bioactive glass 45S5 following heat treatment, J. Eur. Ceram. Soc., 24, 2929, 10.1016/S0955-2219(03)00363-7

Frost, 1998, Could some biomechanical effects of growth hormone help to explain its effects on bone formation and resorption?, Bone, 23, 395, 10.1016/S8756-3282(98)00122-7

Meyers, 2008, Biological materials: Structure and mechanical properties, Prog. Mater. Sci., 53, 1, 10.1016/j.pmatsci.2007.05.002

Zhang, 2009, Nanotechnology and nanomaterials: Promises for improved tissue regeneration, Nano Today, 4, 66, 10.1016/j.nantod.2008.10.014

1991, Physiologically based models for bone-seeking elements: I. Rat skeletal and bone growth, Toxicol. Appl. Pharmacol., 111, 299, 10.1016/0041-008X(91)90032-A

1991, Physiologically based models for bone-seeking elements: III. Human skeletal and bone growth, Toxicol. Appl. Pharmacol., 111, 332, 10.1016/0041-008X(91)90034-C

Boccaccini, 2007, Bone regeneration and repair using tissue engineering, Tissue Engineering Using Ceramics and Polymers, Volume 1, 294

Gibson, 2005, Biomechanics of cellular solids, J. Biomech., 38, 377, 10.1016/j.jbiomech.2004.09.027

Jacobs, C.R. (1994). Numerical simulation of bone adaptation to mechanical loading. [Ph.D. Dissertation, Stanford University].

Diego, 2007, Polymer scaffolds with interconnected spherical pores and controlled architecture for tissue engineering: fabrication, mechanical properties, and finite element modeling, J. Biomed. Mater. Res. B Appl. Biomater., 81, 448, 10.1002/jbm.b.30683

Doblare, 2008, A mathematical model for bone tissue regeneration inside a specific type of scaffold, Biomech. Model. Mechanobiol., 7, 355, 10.1007/s10237-007-0089-7

Zaoui, 1987, Elements of homogenization for inelastic solid mechanics, Homogenization Techniques for Composite Media, Volume 272, 193

Sanz-Herrera, J.A., Doblaré, M., and García-Aznar, J.M. Scaffold microarchitecture determines internal bone directional growth structure: A numerical study. J. Biomech., in press.

Peters, 1997, Synthetic extracellular matrices for cell transplantation, Porous Materials for Tissue Engineering, Volume 250, 43

Li, 2003, Macroporous biphasic calcium phosphate scaffold with high permeability/porosity ratio, Tissue Eng., 9, 535, 10.1089/107632703322066714

Botchwey, 2003, Tissue engineered bone: Measurement of nutrient transport in three-dimensional matrices, J. Biomed. Mater. Res. Part A, 67, 357, 10.1002/jbm.a.10111

Kasper, 2008, Mechanical and flow characterization of Sponceram carriers: Evaluation by homogenization theory and experimental validation, J. Biomed. Mater. Res. B Appl. Biomater., 87, 42

Haddock, 1999, Structure-function relationships for coralline hydroxyapatite bone substitute, J. Biomed. Mater. Res., 47, 71, 10.1002/(SICI)1097-4636(199910)47:1<71::AID-JBM10>3.0.CO;2-U

Haugen, 2004, Ceramic TiO2-foams: Characterisation of a potential scaffold, J. Eur. Ceram. Soc., 24, 661, 10.1016/S0955-2219(03)00255-3

Kohles, 2001, Direct perfusion measurements of cancellous bone anisotropic permeability, J. Biomech., 34, 1197, 10.1016/S0021-9290(01)00082-3

Nauman, 1999, Dependence of intertrabecular permeability on flow direction and anatomic site, Ann. Biomed. Eng., 27, 517, 10.1114/1.195

Discher, 2005, Tissue cells feel and respond to the stiffness of their substrate, Science, 310, 1139, 10.1126/science.1116995

2003, Bone microarchitecture assessment: current and future trends, Osteoporos. Int., 14, S89, 10.1007/s00198-003-1479-z

Bonse, 2002, Micro-mechanical evaluation of bone microstructures under load, Developments in X-Ray Tomography III, Volume 4503, 189

Beaupied, 2007, Evaluation of macrostructural bone biomechanics, Joint Bone Spine, 74, 233, 10.1016/j.jbspin.2007.01.019

Weinans, 2007, Effects of microarchitecture on bone strength, Curr. Osteoporos. Rep., 5, 56, 10.1007/s11914-007-0003-3

Navarro, 2006, Development of a biodegradable composite scaffold for bone tissue engineering: Physicochemical, topographical, mechanical, degradation, and biological properties, Ordered Polymeric Nanostructures at Surfaces, Volume 200, 209, 10.1007/12_068

Rea, 2004, Bioactivity of ceramic-polymer composites with varied composition and surface topography, J. Mater. Sci. Mater. Med., 15, 997, 10.1023/B:JMSM.0000042685.63383.86

Blaker, 2010, Premature degradation of poly(α-hydroxyesters) during thermal processing of Bioglass®-containing composites, Acta Biomater., 6, 756, 10.1016/j.actbio.2009.08.020

Blaker, 2005, Mechanical properties of highly porous PDLLA/Bioglass® composite foams as scaffolds for bone tissue engineering, Acta Biomater., 1, 643, 10.1016/j.actbio.2005.07.003

Meretoja, 2006, Crosslinked poly(ε-caprolactone/D,L-lactide)/bioactive glass composite scaffolds for bone tissue engineering, J. Biomed. Mater. Res. Part A, 77, 261, 10.1002/jbm.a.30630

Meretoja, 2009, Osteoblast response to continuous phase macroporous scaffolds under static and dynamic culture conditions, J. Biomed. Mater. Res. Part A, 89, 317, 10.1002/jbm.a.31980

Yao, 2005, The effect of bioactive glass content on synthesis and bioactivity of composite poly (lactic-co-glycolic acid)/bioactive glass substrate for tissue engineering, Biomaterials, 26, 1935, 10.1016/j.biomaterials.2004.06.027

Keshaw, 2009, Assessment of polymer/bioactive glass-composite microporous spheres for tissue regeneration applications, Tissue Eng. Part A, 15, 1451, 10.1089/ten.tea.2008.0203

Saad, 2010, Synthesis of silicate glass/poly(L-lactide) composite scaffolds by freeze-extraction technique: characterization and in vitro bioactivity evaluation, Ceram. Int., 36, 995, 10.1016/j.ceramint.2009.11.012

Tsigkou, 2007, Enhanced differentiation and mineralization of human fetal osteoblasts on PDLLA containing Bioglass® composite films in the absence of osteogenic supplements, J. Biomed. Mater. Res. Part A, 80A, 837, 10.1002/jbm.a.30910

Maquet, 2004, Porous poly(α-hydroxyacid)/Bioglass composite scaffolds for bone tissue engineering. I: Preparation and in vitro characterisation, Biomaterials, 25, 4185, 10.1016/j.biomaterials.2003.10.082

Maquet, 2003, Preparation, characterization, and in vitro degradation of bioresorbable and bioactive composites based on Bioglass-filled polylactide foams, J. Biomed. Mater. Res. Part A, 66, 335, 10.1002/jbm.a.10587

Verrier, 2004, PDLLA/Bioglass® composites for soft-tissue and hard-tissue engineering: an in vitro cell biology assessment, Biomaterials, 25, 3013, 10.1016/j.biomaterials.2003.09.081

Misra, 2010, Characterization of carbon nanotube (MWCNT) containing P(3HB)/bioactive glass composites for tissue engineering applications, Acta Biomater., 6, 735, 10.1016/j.actbio.2009.09.023

Misra, 2009, Incorporation of vitamin E in poly(3-hydroxybutyrate)/Bioglass composite films: effect on surface properties and cell attachment, J. Roy. Soc. Interface, 6, 401, 10.1098/rsif.2008.0278

Helen, 2008, Cell viability, proliferation and extracellular matrix production of human annulus fibrosus cells cultured within PDLLA/Bioglass® composite foam scaffolds in vitro, Acta Biomater., 4, 230, 10.1016/j.actbio.2007.09.010

Helen, 2007, Three-dimensional culture of annulus fibrosus cells within PDLLA/Bioglass® composite foam scaffolds: Assessment of cell attachment, proliferation and extracellular matrix production, Biomaterials, 28, 2010, 10.1016/j.biomaterials.2007.01.011

Yang, 2006, Evaluation of human bone marrow stromal cell growth on biodegradable polymer/Bioglass® composites, Biochem. Biophys. Res. Commun., 342, 1098, 10.1016/j.bbrc.2006.02.021

Barroca, N., Daniel-da-Silva, A.L., Vilarinho, P.M., and Fernandes, M.H.V. Tailoring the morphology of high molecular weight PLLA scaffolds through bioglass additions. Acta Biomater., in press.

Matthews, F.L., and Rawlings, R.D. (1994). Composite Materials: Engineering and Science, Woodhead Publishing Limited CRC Press. [1st ed.].

Ishai, 1967, Elastic properties of filled and porous epoxy composites, Int. J. Mech. Sci., 9, 539, 10.1016/0020-7403(67)90053-7

Gibson, L.J., and Ashby, M.F. (1997). Cellular Solids: Structure and Properties, Cambridge University Press. [2nd ed.].

Lu, 2005, Compositional effects on the formation of a calcium phosphate layer and the response of osteoblast-like cells on polymer-bioactive glass composites, Biomaterials, 26, 6323, 10.1016/j.biomaterials.2005.04.005

Gao, 2009, Surface modification of bioactive glasses and preparation of PDLLA/bioactive glass composite films, J. Biomater. Appl., 24, 119, 10.1177/0885328208094265

Gubler, 2008, Do bioactive glasses convey a disinfecting mechanism beyond a mere increase in pH?, Int. Endod. J., 41, 670, 10.1111/j.1365-2591.2008.01413.x

Waltimo, 2007, Antimicrobial effect of nanometric bioactive glass 45S5, J. Dent. Res., 86, 754, 10.1177/154405910708600813

Waltimo, 2009, Fine-tuning of bioactive glass for root canal disinfection, J. Dent. Res., 88, 235, 10.1177/0022034508330315

Ravarian, 2010, Synthesis, characterization and bioactivity investigation of bioglass/hydroxyapatite composite, Ceram. Int., 36, 291, 10.1016/j.ceramint.2009.09.016

Mansur, 2008, Nanostructured poly(vinyl alcohol)/bioactive glass and poly(vinyl alcohol)/chitosan/bioactive glass hybrid scaffolds for biomedical applications, Chem. Eng. J., 137, 72, 10.1016/j.cej.2007.09.036

Mishra, 2009, Physical and cytocompatibility properties of bioactive glass-polyvinyl alcohol-sodium alginate biocomposite foams prepared via sol-gel processing for trabecular bone regeneration, J. Mater. Sci. Mater. Med., 20, 2493, 10.1007/s10856-009-3814-1

Hong, 2008, Preparation and in vitro characterization of scaffolds of poly(l-lactic acid) containing bioactive glass ceramic nanoparticles, Acta Biomater., 4, 1297, 10.1016/j.actbio.2008.03.007

Peter, 2009, Development of novel α-chitin/nanobioactive glass ceramic composite scaffolds for tissue engineering applications, Carbohyd. Polym., 78, 926, 10.1016/j.carbpol.2009.07.016

Ali, 2010, Development, characterization, and in vitro bioactivity studies of sol-gel bioactive glass/poly(l-lactide) nanocomposite scaffolds, Mater. Sci. Eng. C, 30, 120, 10.1016/j.msec.2009.09.008

Xie, 2008, In vivo bone regeneration using a novel porous bioactive composite, Appl. Surf. Sci., 255, 545, 10.1016/j.apsusc.2008.06.183

Hench, 2002, Gene activating glasses, J. Inorg. Mater., 17, 897

Bielby, 2004, Time- and concentration-dependent effects of dissolution products of 58S sol-gel bioactive glass on proliferation and differentiation of murine and human osteoblasts, Tissue Eng. Part A, 10, 1018, 10.1089/ten.2004.10.1018

Xynos, 2000, Ionic products of bioactive glass dissolution increase proliferation of human osteoblasts and induce insulin-like growth factor II mRNA expression and protein synthesis, Biochem. Biophys. Res. Commun., 276, 461, 10.1006/bbrc.2000.3503

Bielby, 2004, In vitro differentiation and in vivo mineralization of osteogenic cells derived from human embryonic stem cells, Tissue Eng. Part A, 10, 1518, 10.1089/ten.2004.10.1518

Bielby, 2005, Enhanced derivation of osteogenic cells from murine embryonic stem cells after treatment with ionic dissolution products of 58S bioactive sol-gel glass, Tissue Eng. Part A, 11, 479, 10.1089/ten.2005.11.479

Sun, 2007, The effect of the ionic products of Bioglass® dissolution on human osteoblasts growth cycle in vitro, J. Tissue Eng. Regen. Med., 1, 281, 10.1002/term.34

Jell, 2008, Bioactive glass-induced osteoblast differentiation: a noninvasive spectroscopic study, J. Biomed. Mater. Res. Part A, 86, 31, 10.1002/jbm.a.31542

Jell, 2006, Gene activation by bioactive glasses, J. Mater. Sci. Mater. Med., 17, 997, 10.1007/s10856-006-0435-9

Bohner, 2009, Silicon-substituted calcium phosphates - a critical view, Biomaterials, 30, 6403, 10.1016/j.biomaterials.2009.08.007

Santos, 2010, Vascularization in Bone Tissue Engineering: Physiology, Current Strategies, Major Hurdles and Future Challenges, Macromol. Biosci., 10, 12, 10.1002/mabi.200900107

Geiger, 2005, Vascular endothelial growth factor gene-activated matrix (VEGF165-GAM) enhances osteogenesis and angiogenesis in large segmental bone defects, J. Bone Miner. Res., 20, 2028, 10.1359/JBMR.050701

Peng, 2005, VEGF improves, whereas sFlt1 inhibits, BMP2-induced bone formation and bone healing through modulation of angiogenesis, J. Bone Miner. Res., 20, 2017, 10.1359/JBMR.050708

Day, 2004, Assessment of polyglycolic acid mesh and bioactive glass for soft-tissue engineering scaffolds, Biomaterials, 25, 5857, 10.1016/j.biomaterials.2004.01.043

Keshaw, 2005, Release of angiogenic growth factors from cells encapsulated in alginate beads with bioactive glass, Biomaterials, 26, 4171, 10.1016/j.biomaterials.2004.10.021

Moosvi, 2009, Bioactive glass modulation of intestinal epithelial cell restitution, Acta Biomater., 5, 76, 10.1016/j.actbio.2008.08.003

Leach, 2006, Coating of VEGF-releasing scaffolds with bioactive glass for angiogenesis and bone regeneration, Biomaterials, 27, 3249, 10.1016/j.biomaterials.2006.01.033

Jarrahy, 2005, Osteogenic differentiation is inhibited and angiogenic expression is enhanced in MC3T3-E1 cells cultured on three-dimensional scaffolds, Am. J. Physiol. Cell Physiol., 289, C408, 10.1152/ajpcell.00196.2004

Andrade, 2006, In vivo performance of a sol-gel glass-coated collagen, J. Biomed. Mater. Res. B Appl. Biomater., 79B, 122, 10.1002/jbm.b.30521

Ross, 2003, Tissue adhesion to bioactive glass-coated silicone tubing in a rat model of peritoneal dialysis catheters and catheter tunnels, Kidney Int., 63, 702, 10.1046/j.1523-1755.2003.00764.x

Choi, 2006, Effect of synthetic bone glass particulate on the fibrovascularization of porous polyethylene orbital implants, Ophthalmic Plast. Reconstr. Surg., 22, 121, 10.1097/01.iop.0000197022.19166.dd

Leu, 2009, Angiogenic response to bioactive glass promotes bone healing in an irradiated calvarial defect, Tissue Eng. Part A, 15, 877, 10.1089/ten.tea.2008.0018

Chapanian, 2010, Combined and sequential delivery of bioactive VEGF165 and HGF from poly(trimethylene carbonate) based photo-cross-linked elastomers, J. Contr. Rel., 143, 53, 10.1016/j.jconrel.2009.11.025

Chiu, 2010, Scaffolds with covalently immobilized VEGF and Angiopoietin-1 for vascularization of engineered tissues, Biomaterials, 31, 226, 10.1016/j.biomaterials.2009.09.039

Patel, 2008, Dual delivery of an angiogenic and an osteogenic growth factor for bone regeneration in a critical size defect model, Bone, 43, 931, 10.1016/j.bone.2008.06.019

Briganti, 2010, A composite fibrin-based scaffold for controlled delivery of bioactive pro-angiogenetic growth factors, J. Contr. Rel., 142, 14, 10.1016/j.jconrel.2009.09.029

Kaigler, 2006, VEGF scaffolds enhance angiogenesis and bone regeneration in irradiated osseous defects, J. Bone Miner. Res., 21, 735, 10.1359/jbmr.060120

Rosengren, 2003, Protein adsorption onto two bioactive glass-ceramics, Biomaterials, 24, 147, 10.1016/S0142-9612(02)00272-7

Goller, 2004, The effect of bond coat on mechanical properties of plasma sprayed bioglass-titanium coatings, Ceram. Int., 30, 351, 10.1016/S0272-8842(03)00107-X

Guo, 2004, Characterization of hydroxyapatite- and bioglass-316L fibre composites prepared by spark plasma sintering, Mater. Lett., 58, 304, 10.1016/S0167-577X(03)00474-9

Ferraris, 2010, Alkaline phosphatase grafting on bioactive glasses and glass ceramics, Acta Biomater., 6, 229, 10.1016/j.actbio.2009.06.025

Wuisman, P.I.J.M., and Smit, T.H. (2009). Degradable Polymers for Skeletal Implants, Nova Science Publishers. [1st ed.].

Cordewener, 2000, Cytotoxicity of poly(96L/4D-lactide): The influence of degradation and sterilization, Biomaterials, 21, 2433, 10.1016/S0142-9612(00)00111-3

Janorkar, 2007, Degradation of Poly(L-Lactide) films under ultraviolet-induced photografting and sterilization conditions, J. Appl. Polym. Sci., 106, 1042, 10.1002/app.24692

Jukes, 2010, Skeletal tissue engineering using embryonic stem cells, J. Tissue Eng. Regen. Med., 4, 165, 10.1002/term.234

Oh, C.H., Hong, S.J., Jeong, I., Yu, H.S., Jegal, S.H., and Kim, H.W. (2009). Development of robotic dispensed bioactive scaffolds and human adipose-derived stem cell culturing for bone tissue engineering. Tissue Eng. Part C Methods, September 1.

Zhang, 2009, Preparation and biocompatibility evaluation of apatite/wollastonite-derived porous bioactive glass ceramic scaffolds, Biomed. Mater., 4, 45007, 10.1088/1748-6041/4/4/045007

Harrison, 2007, Carbon nanotube applications for tissue engineering, Biomaterials, 28, 344, 10.1016/j.biomaterials.2006.07.044

Boccaccini, 2007, Carbon nanotube coatings on bioglass-based tissue engnineering scaffolds, Adv. Funct. Mater., 17, 2815, 10.1002/adfm.200600887

Boccaccini, 2007, Biodegradable and bioactive polymer/ceramic composite scaffolds, Tissue Engineering Using Ceramics and Polymers, Volume 1, 72