Abstract
Bioactive scaffolds with interconnected porous structures are essential for guiding cell growth and new bone formation. In this work, we successfully fabricated three-dimensional (3D) porous \(\upbeta \)-tricalcium phosphate (\(\upbeta \)-TCP)/calcium silicate (CS) composite scaffolds with different ratios by 3D printing technique and further investigated the physiochemical properties, in vitro apatite mineralization properties and degradability of porous \(\upbeta \)-TCP/CS scaffolds. Moreover, a series of in vitro cell experiments including the attachment, proliferation and osteogenic differentiation of mouse bone marrow stromal cells were conducted to testify their biological performances. The results showed that 3D printed \(\upbeta \)-TCP/CS scaffolds possessed of controllable internal porous structures and external shape. Furthermore, the introduction of CS decreased the shrinkage of scaffolds and improved the in vitro apatite formation activity and degradation rate. Meanwhile, compared with pure \(\upbeta \)-TCP scaffold, the \(\upbeta \)-TCP/CS composite scaffolds were more conducive to promote cell adhesion, spread and osteogenesis differentiation. However, when the content of CS was increased to 45%, the ions dissolution rate of the composite scaffolds was so high that leaded to the increase in pH value, which inhibited the proliferation of cells. Our results suggested that the introduction of appropriate CS into \(\upbeta \)-TCP bioceramic is an effective strategy to prepare bioactive 3D printed bioceramic scaffolds for hard tissue regeneration.
References
Fei L, Wang C, Xue Y, Lin K, Chang J, Sun J (2012) Osteogenic differentiation of osteoblasts induced by calcium silicate and calcium silicate/beta-tricalcium phosphate composite bioceramics. J Biomed Mater Res B Appl Biomater 100(5):1237–44
Liu S, Jin F, Lin K, Lu J, Sun J, Chang J, Dai K, Fan C (2013) The effect of calcium silicate on in vitro physiochemical properties and in vivo osteogenesis, degradability and bioactivity of porous beta-tricalcium phosphate bioceramics. Biomed Mater 8(2):025008
Wang C, Xue Y, Lin K, Lu J, Chang J, Sun J (2012) The enhancement of bone regeneration by a combination of osteoconductivity and osteostimulation using beta-CaSiO\(_{3}\)/beta-Ca\(_{3}\)(PO\(_{4}\))\(_{2}\) composite bioceramics. Acta Biomater 8(1):350–60
Schroeder HC, Wang XH, Wiens M, Diehl-Seifert B, Kropf K, Schlossmacher U, Mueller WEG (2012) Silicate modulates the cross-talk between osteoblasts (SaOS-2) and osteoclasts (RAW 264.7 Cells): inhibition of osteoclast growth and differentiation. J Cell Biochem 113(10):3197–3206
Wiens M, Wang X, Schroder HC, Kolb U, Schlossmacher U, Ushijima H, Muller WE (2010) The role of biosilica in the osteoprotegerin/RANKL ratio in human osteoblast-like cells. Biomaterials 31(30):7716–25
Li H, Chang J (2013) Stimulation of proangiogenesis by calcium silicate bioactive ceramic. Acta Biomater 9(2):5379–89
Wu C, Fan W, Zhou Y, Luo Y, Gelinsky M, Chang J, Xiao Y (2012) 3D-printing of highly uniform CaSiO\(_{3}\) ceramic scaffolds: preparation, characterization and in vivo osteogenesis. J Mater Chem 22(24):12288
Huang MH, Kao CT, Chen YW, Hsu TT, Shieh DE, Huang TH, Shie MY (2015) The synergistic effects of Chinese herb and injectable calcium silicate/beta-tricalcium phosphate composite on an osteogenic accelerator in vitro. J Mater Sci Mater Med 26(4):161
Fei L, Chen W, Yang X, Lin K, Jiang C, Jiao S (2012) Osteogenic differentiation of osteoblasts induced by calcium silicate and calcium silicate/\(\beta \)-tricalcium phosphate composite bioceramics. J Biomed Mater Res B Appl Biomater 100B(5):1237–1244
Ni S, Lin K, Chang J, Chou L (2008) Beta-CaSiO\(_{3}\)/beta-Ca\(_{3}\)(PO\(_{4}\))\(_{2}\) composite materials for hard tissue repair: in vitro studies. J Biomed Mater Res Part A 85A(1):72–82
Mehdizadeh H, Sumo S, Bayrak ES, Brey EM, Cinar A (2013) Three-dimensional modeling of angiogenesis in porous biomaterial scaffolds. Biomaterials 34(12):2875–87
Park J, Lee SJ, Jo HH, Lee JH, Kim WD, Lee JY, Park SA (2017) Fabrication and characterization of 3D-printed bone-like \(\beta \)-tricalcium phosphate/polycaprolactone scaffolds for dental tissue engineering. J Ind Eng Chem 46:175–181
Baino F, Vitale-Brovarone C (2011) Three-dimensional glass-derived scaffolds for bone tissue engineering: current trends and forecasts for the future. J Biomed Mater Res A 97(4):514–35
Xu M, Li H, Zhai D, Chang J, Chen S, Wu C (2015) Hierarchically porous nagelschmidtite bioceramic–silk scaffolds for bone tissue engineering. J Mater Chem B 3(18):3799–3809
Wu C, Ramaswamy Y, Zreiqat H (2010) Porous diopside (CaMgSi(2)O(6)) scaffold: a promising bioactive material for bone tissue engineering. Acta Biomater 6(6):2237–45
Pei X, Ma L, Zhang B, Sun J, Sun Y, Fan Y, Gou Z, Zhou C, Zhang X (2017) Creating hierarchical porosity hydroxyapatite scaffold with osteoinduction by three-dimensional printing and microwave sintering. Biofabrication 9(4):045008
Barba A, Diezescudero A, Maazouz Y, Rappe K, Espanol M, Montufar EB, Bonany M, Sadowska JM, Guillemmarti J, Öhmanmägi C (2017) Osteoinduction by foamed and 3D-printed calcium phosphate scaffolds: effect of nanostructure and pore architecture. Acs Appl Mater Interfaces 9(48):41722–41736
Hwang KS, Choi JW, Kim JH, Chung HY, Jin S, Shim JH, Yun WS, Jeong CM, Huh JB (2017) Comparative efficacies of collagen-based 3D printed PCL/PLGA/\(\beta \)-TCP composite block bone grafts and biphasic calcium phosphate bone substitute for bone regeneration. Materials 10(4):421
Therriault D, Shepherd R, White S, Lewis J (2005) Fugitive inks for direct-write assembly of three-dimensional microvascular networks. Adv Mater 17(4):395–399
Hutmacher DW (2000) Scaffolds in tissue engineering bone and cartilage. Biomaterials 21(24):2529–2543
Tunchel S, Blay A, Kolerman R, Mijiritsky E, Shibli JA (2016) 3D printing/additive manufacturing single titanium dental implants: a prospective multicenter study with 3 years of follow-up. Int J Dent 2016(6):1–9
Jones JR, Ehrenfried LM, Hench LL (2006) Optimising bioactive glass scaffolds for bone tissue engineering. Biomaterials 27(7):964–73
Wu C, Chang J, Zhai W, Ni S (2007) A novel bioactive porous bredigite (Ca\(_{7}\)MgSi\(_{4}\)O\(_{16}\)) scaffold with biomimetic apatite layer for bone tissue engineering. J Mater Sci Mater Med 18(5):857–64
Gandolfi MG, Ciapetti G, Taddei P, Perut F, Tinti A, Cardoso MV, Van Meerbeek B, Prati C (2010) Apatite formation on bioactive calcium-silicate cements for dentistry affects surface topography and human marrow stromal cells proliferation. Dent Mater 26(10):974–92
Xu S, Lin K, Wang Z, Chang J, Wang L, Lu J, Ning C (2008) Reconstruction of calvarial defect of rabbits using porous calcium silicate bioactive ceramics. Biomaterials 29(17):2588–96
Hing KA, Wilson LF, Buckland T (2007) Comparative performance of three ceramic bone graft substitutes. Spine J 7(4):475–490
Wu C, Luo Y, Cuniberti G, Xiao Y, Gelinsky M (2011) Three-dimensional printing of hierarchical and tough mesoporous bioactive glass scaffolds with a controllable pore architecture, excellent mechanical strength and mineralization ability. Acta Biomater 7(6):2644–50
Butenko RG, Lipsky KA, Chernyak ND, Arya HC (1984) Changes in culture medium pH by cell suspension cultures of dioscorea. Plant Sci Lett 35(3):207–212
Song J, Gao H, Zhu G, Cao X, Shi X, Wang Y (2016) The construction of three-dimensional composite fibrous macrostructures with nanotextures for biomedical applications. Biofabrication 8(3):035009
Shie MY, Ding SJ, Chang HC (2011) The role of silicon in osteoblast-like cell proliferation and apoptosis. Acta Biomater 7(6):2604–14
Kao CT, Huang TH, Chen YJ, Hung CJ, Lin CC, Shie MY (2014) Using calcium silicate to regulate the physicochemical and biological properties when using beta-tricalcium phosphate as bone cement. Mater Sci Eng C Mater Biol Appl 43:126–34
Huang SC, Wu BC, Kao CT, Huang TH, Hung CJ, Shie MY (2015) Role of the p38 pathway in mineral trioxide aggregate-induced cell viability and angiogenesis-related proteins of dental pulp cell in vitro. Int Endod J 48(3):236–245
Ge CX, Xiao GZ, Jiang D, Franceschi RT (2007) Critical role of the extracellular signal-regulated kinase-MAPK pathway in osteoblast differentiation and skeletal development. J Cell Biol 176(5):709–718
Wang C, Lin K, Chang J, Sun J (2014) The stimulation of osteogenic differentiation of mesenchymal stem cells and vascular endothelial growth factor secretion of endothelial cells by beta-CaSiO\(_{3}\)/beta-Ca\(_{3}\)(PO\(_{4}\))\(_{2}\) scaffolds. J Biomed Mater Res A 102(7):2096–104
Ortiz J, Chou LL (2012) Calcium upregulated survivin expression and associated osteogenesis of normal human osteoblasts. J Biomed Mater Res A 100(7):1770–6
Nakamura S, Matsumoto T, Sasaki J, Egusa H, Lee KY, Nakano T, Sohmura T, Nakahira A (2010) Effect of calcium ion concentrations on osteogenic differentiation and hematopoietic stem cell niche-related protein expression in osteoblasts. Tissue Eng Part A 16(8):2467–73
Zeng H, Chittur KK, Lacefield WR (1999) Analysis of bovine serum albumin adsorption on calcium phosphate and titanium surface. Biomaterials 20(4):377–384
Zhu XD, Fan HS, Xiao YM, Li DX, Zhang HJ, Luxbacher T, Zhang XD (2009) Effect of surface structure on protein adsorption to biphasic calcium-phosphate ceramics in vitro and in vivo. Acta Biomater 5(4):1311–8
Acknowledgements
This work was financially supported by the National Key Research and Development Program of China (Grant No. 2016YFB0700803), the Science and Technology program of Guangzhou city (Grant No.201607010234), the Science and Technology program of Guangdong Province (Grant No.2017B090911008) and Guangdong Natural Science Funds for Distinguished Young Scholar (Grant No. 2016A030306018).
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Dong, Y., Duan, H., Zhao, N. et al. Three-dimensional printing of \(\varvec{\upbeta }\)-tricalcium phosphate/calcium silicate composite scaffolds for bone tissue engineering. Bio-des. Manuf. 1, 146–156 (2018). https://doi.org/10.1007/s42242-018-0010-5
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DOI: https://doi.org/10.1007/s42242-018-0010-5