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Inductive biomaterials for bone regeneration

Published online by Cambridge University Press:  28 February 2017

Rafid Kasir ,
Varadraj N. Vernekar Open the ORCID record for Varadraj N. Vernekar [Opens in a new window]  and
Cato T. Laurencin
Rafid Kasir
Affiliation:
Institute for Regenerative Engineering, Raymond and Beverly Sackler Center for Biomedical, Biological, Physical and Engineering Sciences, and Department of Orthopaedic Surgery, University of Connecticut Health Center, Farmington, CT 06030, USA
Varadraj N. Vernekar
Affiliation:
Institute for Regenerative Engineering, Raymond and Beverly Sackler Center for Biomedical, Biological, Physical and Engineering Sciences, and Department of Orthopaedic Surgery, University of Connecticut Health Center, Farmington, CT 06030, USA
Cato T. Laurencin*
Affiliation:
Institute for Regenerative Engineering, University of Connecticut Health Center, Raymond and Beverly Sackler Center for Biomedical, Biological, Physical and Engineering Sciences, and Department of Orthopaedic Surgery, Farmington, CT 06030, USA; Department of Materials Science and Engineering, Department of Chemical and Biomolecular Engineering, and Department of Biomedical Engineering, University of Connecticut, Storrs, CT 06269, USA
*
a)Address all correspondence to this author. e-mail: laurencin@uchc.edu
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Abstract

Inductive biomaterials are sought as alternatives to traditional materials used to treat bone defects. Traditional materials include autologous bone grafts that must be obtained surgically, and allografts that carry the risk of disease transmission and infection. Whereas the use of growth factors to stimulate bone growth has seen considerable advances, their efficacy is usually limited to supra-physiological doses with considerable side effects. On the other hand, certain biomaterials have an intrinsic ability to stimulate bone regeneration in lieu of growth factor use, and their use in repairing bone defects as well as improving the osteointegration of implants has been promising. These materials known as osteoinductive biomaterials include ceramics, metals, polymers, and composites of these materials. In this review, we examine the relevant properties of these different materials in their ability to induce bone formation.

Keywords

osteoinductionbone graftbone regeneration
Type
Invited Feature Paper
Information
Journal of Materials Research , Volume 32 , Issue 6 , 28 March 2017 , pp. 1047 - 1060
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Copyright
Copyright © Materials Research Society 2017 

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Footnotes

b)

These authors contributed equally to this work.

Contributing Editor: Adrian B. Mann

This paper has been selected as an Invited Feature Paper.

References

REFERENCES

Dimitriou, R., Mataliotakis, G.I., Angoules, A.G., Kanakaris, N.K., and Giannoudis, P.V.: Complications following autologous bone graft harvesting from the iliac crest and using the RIA: A systematic review. Injury 42, S3 (2011).Google Scholar
Nodzo, S.R., Kaplan, N.B., Hohman, D.W., and Ritter, C.A.: A radiographic and clinical comparison of reamer–irrigator–aspirator versus iliac crest bone graft in ankle arthrodesis. Int. Orthop. 38, 1199 (2014).Google Scholar
Centers for Disease Control (CDC): Transmission of HIV through bone transplantation: Case report and public health recommendations. MMWR Morb. Mortal. Wkly Rep. 37, 597 (1988).Google Scholar
Mankin, H.J., Hornicek, F.J., and Raskin, K.A.: Infection in massive bone allografts. Clin. Orthop. 432, 210 (2005).CrossRefGoogle Scholar
Daculsi, G., Fellah, B., Miramond, T., and Durand, M.: Osteoconduction, osteogenicity, osteoinduction, what are the fundamental properties for a smart bone substitutes. IRBM 34, 346 (2013).CrossRefGoogle Scholar
Barradas, A., Yuan, H., Blitterswijk, C.A., and Habibovic, P.: Osteoinductive biomaterials: Current knowledge of properties, experimental models and biological mechanisms. Eur. Cells Mater. 21, 407 (2011).Google Scholar
Marcacci, M., Kon, E., Moukhachev, V., Lavroukov, A., Kutepov, S., Quarto, R., Mastrogiacomo, M., and Cancedda, R.: Stem cells associated with macroporous bioceramics for long bone repair: 6-to 7-year outcome of a pilot clinical study. Tissue Eng. 13, 947 (2007).Google Scholar
Blokhuis, T. and Arts, J.C.: Bioactive and osteoinductive bone graft substitutes: Definitions, facts and myths. Injury 42, S26 (2011).Google Scholar
Miron, R.J. and Zhang, Y.F.: Osteoinduction: A review of old concepts with new standards. J. Dent. Res. 91, 736 (2012).Google Scholar
Urist, M.R.: Bone: formation by autoinduction. Science 150, 893 (1965).CrossRefGoogle ScholarPubMed
Song, G., Habibovic, P., Bao, C., Hu, J., Van Blitterswijk, C.A., Yuan, H., Chen, W., and Xu, H.H.: The homing of bone marrow MSCs to non-osseous sites for ectopic bone formation induced by osteoinductive calcium phosphate. Biomaterials 34, 2167 (2013).Google Scholar
Urist, M.R. and Strates, B.S.: Bone morphogenetic protein. J. Dent. Res. 50, 1392 (1971).CrossRefGoogle ScholarPubMed
Sato, K. and Urist, M.R.: Induced regeneration of calvaria by bone morphogenetic protein (BMP) in dogs. Clin. Orthop. 197, 301 (1985).Google Scholar
Kukreja, S., Ahmed, O.I., Haydel, J., Nanda, A., and Sin, A.H.: Complications of anterior cervical fusion using a low-dose recombinant human bone morphogenetic protein-2. Korean J Spine 12, 68 (2015).CrossRefGoogle ScholarPubMed
Neovius, E., Lemberger, M., Skogh, A.D., Hilborn, J., and Engstrand, T.: Alveolar bone healing accompanied by severe swelling in cleft children treated with bone morphogenetic protein-2 delivered by hydrogel. J. Plast. Reconstr. Aesthetic Surg. 66, 37 (2013).Google Scholar
Winter, G.D.: Heterotopic bone formed in a synthetic sponge in the skin of young pigs. Nature 223, 88 (1969).Google Scholar
Chai, Y.C., Roberts, S.J., Schrooten, J., and Luyten, F.P.: Probing the osteoinductive effect of calcium phosphate by using an in vitro biomimetic model. Tissue Eng., Part A 17, 1083 (2010).Google Scholar
Dvorak, M.M., Siddiqua, A., Ward, D.T., Carter, D.H., Dallas, S.L., Nemeth, E.F., and Riccardi, D.: Physiological changes in extracellular calcium concentration directly control osteoblast function in the absence of calciotropic hormones. Proc. Natl. Acad. Sci. U. S. A. 101, 5140 (2004).Google Scholar
Barradas, A.M., Fernandes, H.A., Groen, N., Chai, Y.C., Schrooten, J., van de Peppel, J., van Leeuwen, J.P., van Blitterswijk, C.A., and de Boer, J.: A calcium-induced signaling cascade leading to osteogenic differentiation of human bone marrow-derived mesenchymal stromal cells. Biomaterials 33, 3205 (2012).Google Scholar
González-Vázquez, A., Planell, J.A., and Engel, E.: Extracellular calcium and CaSR drive osteoinduction in mesenchymal stromal cells. Acta Biomater. 10, 2824 (2014).CrossRefGoogle ScholarPubMed
Cushnie, E.K., Ulery, B.D., Nelson, S.J., Deng, M., Sethuraman, S., Doty, S.B., Lo, K.W., Khan, Y.M., and Laurencin, C.T.: Simple signaling molecules for inductive bone regenerative engineering. PLoS One 9, e101627 (2014).Google Scholar
Guth, K., Buckland, T., and Hing, K.A.: Silicon dissolution from microporous silicon substituted hydroxyapatite and its effect on osteoblast behaviour. Key Eng. Mater. 309, 117 (2006).Google Scholar
Carlisle, E.M.: Biochemical and morphological changes associated with long bone abnormalities in silicon deficiency. J. Nutr. 110, 1046 (1980).CrossRefGoogle ScholarPubMed
Coathup, M.J., Samizadeh, S., Fang, Y.S., Buckland, T., Hing, K.A., and Blunn, G.W.: The osteoinductivity of silicate-substituted calcium phosphate. J. Bone Jt. Surg., Am. Vol. 93, 2219 (2011).Google Scholar
Nagineni, V.V., James, A.R., Alimi, M., Hofstetter, C., Shin, B.J., Njoku, I. Jr, Tsiouris, A.J., and Hartl, R.: Silicate-substituted calcium phosphate ceramic bone graft replacement for spinal fusion procedures. Spine 37, E1264 (2012).Google Scholar
Khatiwala, C.B., Kim, P.D., Peyton, S.R., and Putnam, A.J.: ECM compliance regulates osteogenesis by influencing MAPK signaling downstream of RhoA and ROCK. J. Bone Miner. Res. 24, 886 (2009).Google Scholar
Tsai, K., Kao, S., Wang, C., Wang, Y., Wang, J., and Hung, S.: Type I collagen promotes proliferation and osteogenesis of human mesenchymal stem cells via activation of ERK and Akt pathways. J. Biomed. Mater. Res., Part A 94, 673 (2010).Google Scholar
Wang, Y., Yu, X., Cohen, D.M., Wozniak, M.A., Yang, M.T., Gao, L., Eyckmans, J., and Chen, C.S.: Bone morphogenetic protein-2-induced signaling and osteogenesis is regulated by cell shape, RhoA/ROCK, and cytoskeletal tension. Stem Cells Dev. 21, 1176 (2011).Google Scholar
Coathup, M.J., Hing, K.A., Samizadeh, S., Chan, O., Fang, Y.S., Campion, C., Buckland, T., and Blunn, G.W.: Effect of increased strut porosity of calcium phosphate bone graft substitute biomaterials on osteoinduction. J. Biomed. Mater. Res., Part A 100, 1550 (2012).Google Scholar
Du, J., Chen, X., Liang, X., Zhang, G., Xu, J., He, L., Zhan, Q., Feng, X.Q., Chien, S., and Yang, C.: Integrin activation and internalization on soft ECM as a mechanism of induction of stem cell differentiation by ECM elasticity. Proc. Natl. Acad. Sci. U. S. A. 108, 9466 (2011).Google Scholar
Lee, J., Abdeen, A.A., Zhang, D., and Kilian, K.A.: Directing stem cell fate on hydrogel substrates by controlling cell geometry, matrix mechanics and adhesion ligand composition. Biomaterials 34, 8140 (2013).Google Scholar
Kilian, K.A., Bugarija, B., Lahn, B.T., and Mrksich, M.: Geometric cues for directing the differentiation of mesenchymal stem cells. Proc. Natl. Acad. Sci. U. S. A. 107, 4872 (2010).Google Scholar
Hing, K., Annaz, B., Saeed, S., Revell, P., and Buckland, T.: Microporosity enhances bioactivity of synthetic bone graft substitutes. J. Mater. Sci.: Mater. Med. 16, 467 (2005).Google Scholar
Dalby, M.J., Gadegaard, N., Tare, R., Andar, A., Riehle, M.O., Herzyk, P., Wilkinson, C.D., and Oreffo, R.O.: The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. Nat. Mater. 6, 997 (2007).Google Scholar
Zhang, J., Barbieri, D., ten Hoopen, H., de Bruijn, J.D., van Blitterswijk, C.A., and Yuan, H.: Microporous calcium phosphate ceramics driving osteogenesis through surface architecture. J. Biomed. Mater. Res., Part A 103, 1188 (2015).Google Scholar
Wang, L., Luo, X., Barbieri, D., Bao, C., and Yuan, H.: Controlling surface microstructure of calcium phosphate ceramic from random to custom-design. Ceram. Int. 40, 7889 (2014).Google Scholar
Discher, D.E., Janmey, P., and Wang, Y.L.: Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139 (2005).Google Scholar
Engler, A.J., Sen, S., Sweeney, H.L., and Discher, D.E.: Matrix elasticity directs stem cell lineage specification. Cell 126, 677 (2006).Google Scholar
Witkowska-Zimny, M., Walenko, K., Wrobel, E., Mrowka, P., Mikulska, A., and Przybylski, J.: Effect of substrate stiffness on the osteogenic differentiation of bone marrow stem cells and bone-derived cells. Cell Biol. Int. 37, 608 (2013).Google Scholar
Zouani, O.F., Kalisky, J., Ibarboure, E., and Durrieu, M.: Effect of BMP-2 from matrices of different stiffnesses for the modulation of stem cell fate. Biomaterials 34, 2157 (2013).Google Scholar
Tse, J.R. and Engler, A.J.: Stiffness gradients mimicking in vivo tissue variation regulate mesenchymal stem cell fate. PLoS One 6, e15978 (2011).CrossRefGoogle ScholarPubMed
Vincent, L.G., Choi, Y.S., Alonso-Latorre, B., del Álamo, J.C., and Engler, A.J.: Mesenchymal stem cell durotaxis depends on substrate stiffness gradient strength. Biotechnol. J. 8, 472 (2013).Google Scholar
Murphy, W.L., McDevitt, T.C., and Engler, A.J.: Materials as stem cell regulators. Nat. Mater. 13, 547 (2014).Google Scholar
Olivares-Navarrete, R., Raz, P., Zhao, G., Chen, J., Wieland, M., Cochran, D.L., Chaudhri, R.A., Ornoy, A., Boyan, B.D., and Schwartz, Z.: Integrin alpha2beta1 plays a critical role in osteoblast response to micron-scale surface structure and surface energy of titanium substrates. Proc. Natl. Acad. Sci. U. S. A. 105, 15767 (2008).Google Scholar
Dalby, M.J., Gadegaard, N., and Oreffo, R.O.: Harnessing nanotopography and integrin-matrix interactions to influence stem cell fate. Nat. Mater. 13, 558 (2014).Google Scholar
Schwab, E.H., Halbig, M., Glenske, K., Wagner, A., Wenisch, S., and Cavalcanti-Adam, E.A.: Distinct effects of RGD-glycoproteins on integrin-mediated adhesion and osteogenic differentiation of human mesenchymal stem cells. Int. J. Med. Sci. 10, 1846 (2013).Google Scholar
Wei, X., He, K., Yu, S., Zhao, W., Xing, G., Liu, Y., and Sun, J.: RGD peptide-modified poly (lactide-co-glycolide)/β-Tricalcium phosphate scaffolds increase bone formation after transplantation in a rabbit model. J. Biomater. Tissue Eng. 5, 378 (2015).Google Scholar
Das, R.K., Zouani, O.F., Labrugere, C., Oda, R., and Durrieu, M.: Influence of nanohelical shape and periodicity on stem cell fate. ACS Nano 7, 3351 (2013).Google Scholar
Frith, J.E., Mills, R.J., and Cooper-White, J.J.: Lateral spacing of adhesion peptides influences human mesenchymal stem cell behaviour. J. Cell Sci. 125, 317 (2012).Google Scholar
Wang, X., Li, S., Yan, C., Liu, P., and Ding, J.: Fabrication of RGD micro/nanopattern and corresponding study of stem cell differentiation. Nano Lett. 15, 1457 (2015).Google Scholar
Kilian, K.A. and Mrksich, M.: Directing stem cell fate by controlling the affinity and density of ligand? Receptor interactions at the biomaterials interface. Angew. Chem., Int. Ed. 51, 4891 (2012).Google Scholar
Gentleman, M.M. and Gentleman, E.: The role of surface free energy in osteoblast–biomaterial interactions. Int. Mater. Rev. 59, 417 (2014).Google Scholar
Kilpadi, K.L., Chang, P., and Bellis, S.L.: Hydroxylapatite binds more serum proteins, purified integrins, and osteoblast precursor cells than titanium or steel. J. Biomed. Mater. Res. 57, 258 (2001).Google Scholar
Yuan, H., Yang, Z., Li, Y., Zhang, X., De Bruijn, J., and De Groot, K.: Osteoinduction by calcium phosphate biomaterials. J. Mater. Sci.: Mater. Med. 9, 723 (1998).Google Scholar
Tsukanaka, M., Fujibayashi, S., Otsuki, B., Takemoto, M., and Matsuda, S.: Osteoinductive potential of highly purified porous β-TCP in mice. J. Mater. Sci.: Mater. Med. 26, 1 (2015).Google Scholar
Davison, N., Luo, X., Schoenmaker, T., Everts, V., Yuan, H., Barrere-de Groot, F., and de Bruijn, J.: Submicron-scale surface architecture of tricalcium phosphate directs osteogenesis in vitro and in vivo . Eur. Cells Mater. 27, 281 (2014).Google Scholar
Zhang, J., Luo, X., Barbieri, D., Barradas, A.M., de Bruijn, J.D., Van Blitterswijk, C.A., and Yuan, H.: The size of surface microstructures as an osteogenic factor in calcium phosphate ceramics. Acta Biomater. 10, 3254 (2014).Google Scholar
Kondo, N., Ogose, A., Tokunaga, K., Umezu, H., Arai, K., Kudo, N., Hoshino, M., Inoue, H., Irie, H., and Kuroda, K.: Osteoinduction with highly purified β-tricalcium phosphate in dog dorsal muscles and the proliferation of osteoclasts before heterotopic bone formation. Biomaterials 27, 4419 (2006).Google Scholar
Meagher, M.J., Weiss-Bilka, H.E., Best, M.E., Boerckel, J.D., Wagner, D.R., and Roeder, R.K.: Acellular hydroxyapatite-collagen scaffolds support angiogenesis and osteogenic gene expression in an ectopic murine model: Effects of hydroxyapatite volume fraction. J. Biomed. Mater. Res., Part A 104, 2178 (2016).Google Scholar
Lee, H., Kim, H., Ko, J., Choi, Y., Ahn, M., Kim, S., and Do, S.H.: Comparative characteristics of porous bioceramics for an osteogenic response in vitro and in vivo . PLoS One 8, e84272 (2013).Google Scholar
Wang, H., Zhi, W., Lu, X., Li, X., Duan, K., Duan, R., Mu, Y., and Weng, J.: Comparative studies on ectopic bone formation in porous hydroxyapatite scaffolds with complementary pore structures. Acta Biomater. 9, 8413 (2013).Google Scholar
Akiyama, N., Takemoto, M., Fujibayashi, S., Neo, M., Hirano, M., and Nakamura, T.: Difference between dogs and rats with regard to osteoclast-like cells in calcium-deficient hydroxyapatite-induced osteoinduction. J. Biomed. Mater. Res., Part A 96, 402 (2011).Google Scholar
Yuan, H., Kurashina, K., de Bruijn, J.D., Li, Y., De Groot, K., and Zhang, X.: A preliminary study on osteoinduction of two kinds of calcium phosphate ceramics. Biomaterials 20, 1799 (1999).CrossRefGoogle Scholar
Habibovic, P., Kruyt, M.C., Juhl, M.V., Clyens, S., Martinetti, R., Dolcini, L., Theilgaard, N., and van Blitterswijk, C.A.: Comparative in vivo study of six hydroxyapatite-based bone graft substitutes. J. Orthop. Res. 26, 1363 (2008).Google Scholar
Ripamonti, U.: Osteoinduction in porous hydroxyapatite implanted in heterotopic sites of different animal models. Biomaterials 17, 31 (1996).Google Scholar
Habibovic, P., Gbureck, U., Doillon, C.J., Bassett, D.C., van Blitterswijk, C.A., and Barralet, J.E.: Osteoconduction and osteoinduction of low-temperature 3D printed bioceramic implants. Biomaterials 29, 944 (2008).Google Scholar
Duan, Y., Wu, Y., Wang, C., Chen, J., and Zhang, X.: A study of bone-like apatite formation on calcium phosphate ceramics in different kinds of animals in vivo . Shengwu Yixue Gongchengxue Zazhi 20, 22 (2003).Google Scholar
Fellah, B.H., Gauthier, O., Weiss, P., Chappard, D., and Layrolle, P.: Osteogenicity of biphasic calcium phosphate ceramics and bone autograft in a goat model. Biomaterials 29, 1177 (2008).Google Scholar
Cheng, L., Ye, F., Yang, R., Lu, X., Shi, Y., Li, L., Fan, H., and Bu, H.: Osteoinduction of hydroxyapatite/β-tricalcium phosphate bioceramics in mice with a fractured fibula. Acta Biomater. 6, 1569 (2010).Google Scholar
Yang, R., Ye, F., Cheng, L., Wang, J., Lu, X., Shi, Y., Fan, H., Zhang, X., and Bu, H.: Osteoinduction by Ca–P biomaterials implanted into the muscles of mice. J. Zhejiang Univ., Sci., B 12, 582 (2011).Google Scholar
Cheng, L., Shi, Y., Ye, F., and Bu, H.: Osteoinduction of calcium phosphate biomaterials in small animals. Mater. Sci. Eng., C 33, 1254 (2013).Google Scholar
Wang, J., Chen, Y., Zhu, X., Yuan, T., Tan, Y., Fan, Y., and Zhang, X.: Effect of phase composition on protein adsorption and osteoinduction of porous calcium phosphate ceramics in mice. J. Biomed. Mater. Res., Part A 102, 4234 (2014).Google Scholar
Wang, L., Barbieri, D., Zhou, H., de Bruijn, J.D., Bao, C., and Yuan, H.: Effect of particle size on osteoinductive potential of microstructured biphasic calcium phosphate ceramic. J. Biomed. Mater. Res., Part A 103, 1919 (2015).Google Scholar
Davison, N., Su, J., Yuan, H., van den Beucken, J., de Bruijn, J., and Barrère-de Groot, F.: Influence of surface microstructure and chemistry on osteoinduction and osteoclastogenesis by biphasic calcium phosphate discs. Eur. Cells Mater. 29, 314 (2015).Google Scholar
Miron, R.J., Sculean, A., Shuang, Y., Bosshardt, D.D., Gruber, R., Buser, D., Chandad, F., and Zhang, Y.: Osteoinductive potential of a novel biphasic calcium phosphate bone graft in comparison with autographs, xenografts, and DFDBA. Clin. Oral Implants Res. 7, 668–675 (2015).Google Scholar
Miron, R.J., Zhang, Q., Sculean, A., Buser, D., Pippenger, B.E., Dard, M., Shirakata, Y., Chandad, F., and Zhang, Y.: Osteoinductive potential of 4 commonly employed bone grafts. Clin. Oral. Investig. 1, 2259 (2016).Google Scholar
LeGeros, R., Lin, S., Rohanizadeh, R., Mijares, D., and LeGeros, J.: Biphasic calcium phosphate bioceramics: Preparation, properties and applications. J. Mater. Sci. Mater. Med. 14, 201 (2003).CrossRefGoogle ScholarPubMed
Jarcho, M.: Calcium phosphate ceramics as hard tissue prosthetics. Clin. Orthop. 157, 259 (1981).Google Scholar
Draenert, M., Draenert, A., and Draenert, K.: Osseointegration of hydroxyapatite and remodeling-resorption of tricalcium phosphate ceramics. Microsc. Res. Tech. 76, 370 (2013).Google Scholar
Martin, R. and Brown, P.: Mechanical properties of hydroxyapatite formed at physiological temperature. J. Mater. Sci.: Mater. Med. 6, 138 (1995).Google Scholar
van Eeden, S.P. and Ripamonti, U.: Bone differentiation in porous hydroxyapatite in baboons is regulated by the geometry of the substratum: Implications for reconstructive craniofacial surgery. Plast. Reconstr. Surg. 93, 959 (1994).Google Scholar
Yang, Z., Yuan, H., Tong, W., Zou, P., Chen, W., and Zhang, X.: Osteogenesis in extraskeletally implanted porous calcium phosphate ceramics: Variability among different kinds of animals. Biomaterials 17, 2131 (1996).Google Scholar
Yamasaki, H.: Heterotopic bone formation around porous hydroxyapatite ceramics in the subcutis of dogs. Jpn. J. Oral Biol. 32, 190 (1990).Google Scholar
Liu, B. and Lun, D.: Current application of β-tricalcium phosphate composites in orthopaedics. Orthop. Surg. 4, 139 (2012).Google Scholar
Merten, H., Wiltfang, J., Hönig, J., Funke, M., and Luhr, H.: Intra-individual comparison of alpha-and beta-TCP ceramics in an animal experiment. Mund Kiefer Gesichtschir. 4, S509 (2000).Google Scholar
Hollinger, J.O. and Battistone, G.C.: Biodegradable bone repair materials synthetic polymers and ceramics. Clin. Orthop. 207, 290 (1986).Google Scholar
Song, H.J., Liang, X., Luo, X.Q., Chen, M., and Sun, H.Q.: Experimental study on the reconstruction of bone defects in vivo and the osteoinduction with degradation products of alpha-tricalcium phosphate cements in vitro . Sichuan Daxue Xuebao, Yixueban 36, 847 (2005).Google Scholar
Ke, D., Dernell, W., Bandyopadhyay, A., and Bose, S.: Doped tricalcium phosphate scaffolds by thermal decomposition of naphthalene: Mechanical properties and in vivo osteogenesis in a rabbit femur model. J. Biomed. Mater. Res., Part B 103, 1549 (2015).CrossRefGoogle Scholar
Fielding, G. and Bose, S.: SiO2 and ZnO dopants in three-dimensionally printed tricalcium phosphate bone tissue engineering scaffolds enhance osteogenesis and angiogenesis in vivo . Acta Biomater. 9, 9137 (2013).Google Scholar
Bohner, M., Lemaître, J., and Ring, T.A.: Kinetics of dissolution of β-tricalcium phosphate. J. Colloid Interface Sci. 190, 37 (1997).Google Scholar
LeGeros, R.Z.: Calcium phosphates in oral biology and medicine. Monogr. Oral Sci. 15, 1 (1991).Google Scholar
de Ruiter, A., Dik, E., van Es, R., van der Bilt, A., Janssen, N., Meijer, G., Koole, R., and Rosenberg, A.: Micro-structured calcium phosphate ceramic for donor site repair after harvesting chin bone for grafting alveolar clefts in children. J. Craniomaxillofac. Surg. 42, 460 (2014).Google Scholar
de Ruiter, A., Meijer, G., Dormaar, T., Janssen, N., van der Bilt, A., Slootweg, P., de Bruijn, J., van Rijn, L., and Koole, R.: β-TCP versus autologous bone for repair of alveolar clefts in a goat model. Cleft Palate Craniofac. J. 48, 654 (2011).Google Scholar
Elliott, J.C.: Structure and Chemistry of the Apatites and Other Calcium Orthophosphates (Elsevier, Amsterdam, 2013).Google Scholar
Paul, W. and Sharma, C.P.: Effect of calcium, zinc and magnesium on the attachment and spreading of osteoblast like cells onto ceramic matrices. J. Mater. Sci.: Mater. Med. 18, 699 (2007).Google Scholar
Wei, J., Jia, J., Wu, F., Wei, S., Zhou, H., Zhang, H., Shin, J., and Liu, C.: Hierarchically microporous/macroporous scaffold of magnesium–calcium phosphate for bone tissue regeneration. Biomaterials 31, 1260 (2010).Google Scholar
Li, X., Niu, Y., Guo, H., Chen, H., Li, F., Zhang, J., Chen, W., Wu, Z., Deng, Y., and Wei, J.: Preparation and osteogenic properties of magnesium calcium phosphate biocement scaffolds for bone regeneration. J. Instrum. 8, C07010 (2013).Google Scholar
Haugen, H.J., Monjo, M., Rubert, M., Verket, A., Lyngstadaas, S.P., Ellingsen, J.E., Rønold, H.J., and Wohlfahrt, J.C.: Porous ceramic titanium dioxide scaffolds promote bone formation in rabbit peri-implant cortical defect model. Acta Biomater. 9, 5390 (2013).Google Scholar
Luo, X., Barbieri, D., Passanisi, G., Yuan, H., and de Bruijn, J.: Influence of fluoride in poly(d,l-lactide)/apatite composites on bone formation. J. Biomed. Mater. Res., Part B 103, 841 (2015).Google Scholar
Hench, L.L.: The story of bioglass® . J. Mater. Sci.: Mater. Med. 17, 967 (2006).Google Scholar
Kokubo, T.: Bioceramics and their clinical applications. (Elsevier, 2008).Google Scholar
Yuan, H., de Bruijn, J.D., Zhang, X., van Blitterswijk, C.A., and de Groot, K.: Bone induction by porous glass ceramic made from Bioglass®(45S5). J. Biomed. Mater. Res. 58, 270 (2001).Google Scholar
Ducheyne, P. and Qiu, Q.: Bioactive ceramics: The effect of surface reactivity on bone formation and bone cell function. Biomaterials 20, 2287 (1999).Google Scholar
Lindfors, N., Hyvönen, P., Nyyssönen, M., Kirjavainen, M., Kankare, J., Gullichsen, E., and Salo, J.: Bioactive glass S53P4 as bone graft substitute in treatment of osteomyelitis. Bone 47, 212 (2010).Google Scholar
Lindfors, N.C., Koski, I., Heikkilä, J.T., Mattila, K., and Aho, A.J.: A prospective randomized 14-year follow-up study of bioactive glass and autogenous bone as bone graft substitutes in benign bone tumors. J. Biomed. Mater. Res., Part B 94, 157 (2010).Google Scholar
Mcnamara, B.P., Toni, A., and Taylor, D.: Effects of implant material properties and implant-bone bonding on stress shielding in cementless total hip arthroplasty. Key Eng. Mater. 99, 309 (1995).Google Scholar
Fujibayashi, S., Neo, M., Kim, H., Kokubo, T., and Nakamura, T.: Osteoinduction of porous bioactive titanium metal. Biomaterials 25, 443 (2004).CrossRefGoogle ScholarPubMed
Zhao, C., Zhu, X., Liang, K., Ding, J., Xiang, Z., Fan, H., and Zhang, X.: Osteoinduction of porous titanium: A comparative study between acid-alkali and chemical-thermal treatments. J. Biomed. Mater. Res., Part B 95, 387 (2010).Google Scholar
Fukuda, A., Takemoto, M., Saito, T., Fujibayashi, S., Neo, M., Pattanayak, D.K., Matsushita, T., Sasaki, K., Nishida, N., and Kokubo, T.: Osteoinduction of porous Ti implants with a channel structure fabricated by selective laser melting. Acta Biomater. 7, 2327 (2011).Google Scholar
Kawai, T., Takemoto, M., Fujibayashi, S., Akiyama, H., Tanaka, M., Yamaguchi, S., Pattanayak, D.K., Doi, K., Matsushita, T., and Nakamura, T.: Osteoinduction on acid and heat treated porous Ti metal samples in canine muscle. PLoS One 9, e88366 (2014).Google Scholar
Boe, B.G., Stoen, R.O., Solberg, L.B., Reinholt, F.P., Ellingsen, J.E., and Nordsletten, L.: Coating of titanium with hydroxyapatite leads to decreased bone formation: A study in rabbits. Bone Joint Res. 1, 125 (2012).Google Scholar
Hudalla, G.A., Kouris, N.A., Koepsel, J.T., Ogle, B.M., and Murphy, W.L.: Harnessing endogenous growth factor activity modulates stem cell behavior. Integr. Biol. 3, 832 (2011).Google Scholar
Kisiel, M., Klar, A.S., Ventura, M., Buijs, J., Mafina, M., Cool, S.M., and Hilborn, J.: Complexation and sequestration of BMP-2 from an ECM mimetic hyaluronan gel for improved bone formation. PloS One 8, e78551 (2013).Google Scholar
Kanzaki, S., Takahashi, T., Kanno, T., Ariyoshi, W., Shinmyouzu, K., Tujisawa, T., and Nishihara, T.: Heparin inhibits BMP-2 osteogenic bioactivity by binding to both BMP-2 and BMP receptor. J. Cell. Physiol. 216, 844 (2008).Google Scholar
Jiang, T., Khan, Y., Nair, L.S., Abdel-Fattah, W.I., and Laurencin, C.T.: Functionalization of chitosan/poly(lactic acid–glycolic acid) sintered microsphere scaffolds via surface heparinization for bone tissue engineering. J. Biomed. Mater. Res., Part A 93, 1193 (2010).Google Scholar
Jiang, T., Nukavarapu, S.P., Deng, M., Jabbarzadeh, E., Kofron, M.D., Doty, S.B., Abdel-Fattah, W.I., and Laurencin, C.T.: Chitosan–poly (lactide-co-glycolide) microsphere-based scaffolds for bone tissue engineering: In vitro degradation and in vivo bone regeneration studies. Acta Biomater. 6, 3457 (2010).Google Scholar
Martino, M.M., Tortelli, F., Mochizuki, M., Traub, S., Ben-David, D., Kuhn, G.A., Muller, R., Livne, E., Eming, S.A., and Hubbell, J.A.: Engineering the growth factor microenvironment with fibronectin domains to promote wound and bone tissue healing. Sci. Transl. Med. 3, 100ra89 (2011).CrossRefGoogle ScholarPubMed
He, B., Ou, Y., Zhou, A., Chen, S., Zhao, W., Zhao, J., Li, H., Zhu, Y., Zhao, Z., and Jiang, D.: Functionalized d-form self-assembling peptide hydrogels for bone regeneration. Drug Des., Dev. Ther. 10, 1379 (2016).Google Scholar
Bhattacharyya, S., Kumbar, S.G., Khan, Y.M., Nair, L.S., Singh, A., Krogman, N.R., Brown, P.W., Allcock, H.R., and Laurencin, C.T.: Biodegradable polyphosphazene–nanohydroxyapatite composite nanofibers: Scaffolds for bone tissue engineering. J. Biomed. Nanotechnol. 5, 69 (2009).Google Scholar
Devin, J.E., Attawia, M.A., and Laurencin, C.T.: Three-dimensional degradable porous polymer-ceramic matrices for use in bone repair. J. Biomater. Sci., Polym. Ed. 7, 661 (1996).Google Scholar
Nukavarapu, S.P., Kumbar, S.G., Brown, J.L., Krogman, N.R., Weikel, A.L., Hindenlang, M.D., Nair, L.S., Allcock, H.R., and Laurencin, C.T.: Polyphosphazene/nano-hydroxyapatite composite microsphere scaffolds for bone tissue engineering. Biomacromolecules 9, 1818 (2008).Google Scholar
Polini, A., Pisignano, D., Parodi, M., Quarto, R., and Scaglione, S.: Osteoinduction of human mesenchymal stem cells by bioactive composite scaffolds without supplemental osteogenic growth factors. PLoS One 6, e26211 (2011).Google Scholar
Barbieri, D., Renard, A., Bruijn, D.J., and Yuan, H.: Heterotopic bone formation by nano-apatite conraining poly(D,L-lactide) composites. Eur. Cells Mater. 19, 252 (2010).Google Scholar
Danoux, C.B., Barbieri, D., Yuan, H., de Bruijn, J.D., van Blitterswijk, C.A., and Habibovic, P.: In vitro and in vivo bioactivity assessment of a polylactic acid/hydroxyapatite composite for bone regeneration. Biomatter 4, e27664 (2014).Google Scholar
Barrere, F., van der Valk, C.M., Dalmeijer, R.A., Meijer, G., van Blitterswijk, C.A., de Groot, K., and Layrolle, P.: Osteogenecity of octacalcium phosphate coatings applied on porous metal implants. J. Biomed. Mater. Res., Part A 66, 779 (2003).Google Scholar
Li, J., Habibovic, P., Yuan, H., van den Doel, M., Wilson, C.E., de Wijn, J.R., van Blitterswijk, C.A., and de Groot, K.: Biological performance in goats of a porous titanium alloy–biphasic calcium phosphate composite. Biomaterials 28, 4209 (2007).Google Scholar
Barbieri, D., Yuan, H., De Groot, F., Walsh, W.R., and De Bruijn, J.D.: Influence of different polymeric gels on the ectopic bone forming ability of an osteoinductive biphasic calcium phosphate ceramic. Acta Biomater. 7, 2007 (2011).Google Scholar
GĂśtz, W., Lenz, S., Reichert, C., Henkel, K., BienengrĂ, V., Pernicka, L., Gundlach, K.K., Gredes, T., Gerber, T., and Gedrange, T.: A preliminary study in osteoinduction by a nano-crystalline hydroxyapatite in the mini pig. Folia Histochem. Cytobiol. 48, 589 (2010).Google Scholar
Barbieri, D., Yuan, H., Luo, X., Farè, S., Grijpma, D.W., and de Bruijn, J.D.: Influence of polymer molecular weight in osteoinductive composites for bone tissue regeneration. Acta Biomater. 9, 9401 (2013).Google Scholar
Hongmin, L., Wei, Z., Xingrong, Y., Jing, W., Wenxin, G., Jihong, C., Xin, X., and Fulin, C.: Osteoinductive nanohydroxyapatite bone substitute prepared via in situ hydrothermal transformation of cuttlefish bone. J. Biomed. Mater. Res., Part B 103, 816 (2015).Google Scholar
Pati, F., Song, T., Rijal, G., Jang, J., Kim, S.W., and Cho, D.: Ornamenting 3D printed scaffolds with cell-laid extracellular matrix for bone tissue regeneration. Biomaterials 37, 230 (2015).Google Scholar
Mishra, R., Raina, D.B., Pelkonen, M., Lidgren, L., Tägil, M., and Kumar, A.: Study of in vitro and in vivo bone formation in composite cryogels and the influence of electrical stimulation. Int. J. Biol. Sci. 11, 1325 (2015).Google Scholar
Scott, M.A., Levi, B., Askarinam, A., Nguyen, A., Rackohn, T., Ting, K., Soo, C., and James, A.W.: Brief review of models of ectopic bone formation. Stem Cells Dev. 21, 655 (2011).Google Scholar
Kasuga, T., Maeda, H., Kato, K., Nogami, M., Hata, K., and Ueda, M.: Preparation of poly(lactic acid) composites containing calcium carbonate (vaterite). Biomaterials 24, 3247 (2003).Google Scholar
Bodde, E.W., Cammaert, C.T., Wolke, J.G., Spauwen, P.H., and Jansen, J.A.: Investigation as to the osteoinductivity of macroporous calcium phosphate cement in goats. J. Biomed. Mater. Res., Part B 83, 161 (2007).Google Scholar
Chan, O., Coathup, M., Nesbitt, A., Ho, C., Hing, K., Buckland, T., Campion, C., and Blunn, G.: The effects of microporosity on osteoinduction of calcium phosphate bone graft substitute biomaterials. Acta Biomater. 8, 2788 (2012).Google Scholar
Quan, R., Yang, D., Wu, X., Wang, H., Miao, X., and Li, W.: In vitro and in vivo biocompatibility of graded hydroxyapatite–zirconia composite bioceramic. J. Mater. Sci.: Mater. Med. 19, 183 (2008).Google Scholar