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Fabrication, characterization, and in vitro bioactivity evaluation of freeze-cast highly porous hardystonite ceramic reinforced by graphene oxide as a novel bone scaffold

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Abstract

One of the major challenges in bone tissue engineering is the preparation of highly interconnected porous scaffolds with suitable mechanical properties. Synthetic scaffolds used in medicine are usually made of single-phase of ceramic or polymer. However, the combination of these materials with graphene-based nanofillers can produce scaffolds with improved mechanical and biological properties. In this research, we synthesize highly porous (up to 85%) and lamellar hardystonite-graphene oxide (0–1.5 wt% GO) composite scaffolds through the freeze-casting technique and then sintering it for 5 h at 1150 °C. The results of microstructural observations showed using higher amounts of GO leads to an increase in the porosity and a decrease in the shrinkage level. The optimum mechanical properties among the studied samples are related to HT-1 wt% GO (E = 71.77 ± 2.40 MPa, σ = 1.8 ± 016 MPa, and K = 47.87 MJ/m3). Therefore, biological tests were performed on the HT-1 wt% GO scaffold and HT scaffold as the optimal and control samples, respectively. In vitro bioactivity experiments confirm the formation of apatite on surfaces of HT and HT-1 wt% GO specimens after soaking them in SBF for 14 days in static circumstances. Based on the cell studies, the HT-1 wt% GO scaffold sample showed the best attachment and proliferation of osteoblastic cells. The methyl thiazole tetrazolium (MTT) assays were used to characterize the biocompatibility of the HT-1 wt% GO composites in vitro. Also, the alkaline phosphatase (ALP) activity and proliferation rate of cells on the HT-1 wt% GO composite was higher compared with the pure HT ceramics. Overall, it is concluded that the HT-1 wt% GO scaffold with enhanced biological and mechanical features is suitable for use as a novel bone scaffold.

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References

  1. Burg, K.J.L., Porter, S., Kellam, J.F.: Biomaterial developments for bone tissue engineering. Biomaterials. 21, 2347–2359 (2000). https://doi.org/10.1016/S0142-9612(00)00102-2

    Article  CAS  Google Scholar 

  2. Dinescu, S., Ionita, M., Ignat, S.R., Costache, M., Hermenean, A.: Graphene oxide enhances chitosan-based 3D scaffold properties for bone tissue engineering. Int. J. Mol. Sci. 20, 5077 (2019). https://doi.org/10.3390/ijms20205077

    Article  CAS  Google Scholar 

  3. Shirtliff, V.J., Hench, L.L.: Bioactive materials for tissue engineering regeneration and repair. Mater. Sci. 38, 4697–4707 (2003). https://doi.org/10.1023/A:1027414700111

    Article  CAS  Google Scholar 

  4. Shao, G., Hanaor, D.A.H., Shen, X., Gurlo, A.: Freeze casting: from low-dimensional building blocks to aligned porous structures—a review of novel materials, methods, and applications. Adv. Mater. 32, 1907–1176 (2020). https://doi.org/10.1002/adma.201907176

    Article  CAS  Google Scholar 

  5. Schardosim, M., Soulié, J., Poquillon, D., Cazalbouc, S., Duployer, B., Tenailleau, C., Rey, C., Hübler, R., Combes, C.: Freeze-casting for PLGA/carbonated apatite composite scaffolds: structure and properties. Mater. Sci. Eng. C. 77, 731–738 (2017). https://doi.org/10.1016/j.msec.2017.03.302

    Article  CAS  Google Scholar 

  6. Le Huec, J.C., Schaeverbeke, T., Clement, D., Faber, J., Le Rebeller, A.: Influence of porosity on the mechanical resistance of hydroxyapatite ceramics under compressive stress. Biomaterials. 16, 113–118 (1995). https://doi.org/10.1016/0142-9612(95)98272-G

    Article  Google Scholar 

  7. Wegst, U.G., Schecter, M., Donius, A.E., Hunger, P.M.: Biomaterials by freeze casting. Philos. Trans. R. Soc. London. Ser. A. 368, 2099–2121 (2010). https://doi.org/10.1098/rsta.2010.0014

    Article  CAS  Google Scholar 

  8. Huang, J., Rubink, W.S., Lide, H., Scharf, T.W., Banerjee, R., Jolandan, M.M.: Alumina-nickel composite processed via co-assembly using freeze-casting and Spark plasma Sintering. Adv. Eng. Mater. 1801103 (2018). https://doi.org/10.1002/adem.201801103

  9. Yang, Y., He, F., Ye, J.: Preparation, mechanical property and cytocompatibility of freeze-cast porous calcium phosphate ceramics reinforced by phosphate-based glass. Mater. Sci. Eng. C. 69, 1004–1009 (2016). https://doi.org/10.1016/j.msec.2016.08.008

    Article  CAS  Google Scholar 

  10. Deville, S., Maire, E., Lasalle, A., Bogner, A., Gauthier, C., Leloup, J., et al.: Influence of particle size on ice nucleation and growth during the ice-templating process. J. Am. Ceram. Soc. 93, 2507–2510 (2010). https://doi.org/10.1111/j.1551-2916.2010.03840.x

    Article  CAS  Google Scholar 

  11. Lasalle, A., Guizard, C., Leloup, J., Deville, S., Maire, E., Bogner, A., et al.: Ice-templating of alumina suspensions: effect of supercooling and crystal growth during the initial freezing regime. J. Am. Ceram. Soc. 95, 799–804 (2012). https://doi.org/10.1111/j.1551-2916.2011.04993.x

    Article  CAS  Google Scholar 

  12. Zamanian, A., Farhangdoust, S., Yasaei, M., Khorami, M., Hafezi, M.: The effect of particle size on the mechanical and microstructural properties of freeze-casted macroporous hydroxyapatite scaffolds. Int. J. Appl. Ceram. Technol. 11, 12–21 (2013). https://doi.org/10.1111/ijac.12031

    Article  CAS  Google Scholar 

  13. Ye, F., Zhang, J., Liu, L., Zhan, H.: Effect of solid content on pore structure and mechanical properties of porous silicon nitride ceramics produced by freeze casting. Mater. Sci. Eng. A. 528, 1421–1424 (2011). https://doi.org). https://doi.org/10.1016/J.MSEA.2010.10.066

    Article  Google Scholar 

  14. Deville, S.: Freeze-casting of porous ceramics: a review of current achievements and issues. Adv. Eng. Mater. 10, 155–169 (2008). https://doi.org/10.1002/adem.200700270

    Article  CAS  Google Scholar 

  15. Huang, T.H., Huang, T.H., Lin, Y.S., Chang, C.H., Chen, P.Y., Chang, S.W., Chen, C.S.: Phase-field modeling of microstructural evolution by freeze-casting. Adv. Eng. Mater. 00, 1700343 (2017). https://doi.org/10.1002/adem.201700343

    Article  CAS  Google Scholar 

  16. Farhangdoust, S., Zamanian, A., Yasaei, M., Khorami, M.: The effect of processing parameters and solid concentration on the mechanical and microstructural properties of freeze-casted macroporous hydroxyapatite scaffolds. Mater. Sci. Eng. C. 33, 453–460 (2013). https://doi.org/10.1016/j.msec.2012.09.013

    Article  CAS  Google Scholar 

  17. Deville, S., Saiz, E., Tomsia, A.P.: Ice-templated porous alumina structures. Acta Mater. 55, 1965–1974 (2007). https://doi.org/10.1016/j.actamat.2006.11.003

    Article  CAS  Google Scholar 

  18. Deville, S., Saiz, E., Tomsia, A.P.: Freeze casting of hydroxyapatite scaffolds for bone tissue engineering. Biomaterials. 27, 5480–5490 (2006). https://doi.org/10.1016/j.biomaterials.2006.06.028

    Article  CAS  Google Scholar 

  19. Sadeghzade, S., Emadi, R., Ghomi, H.: Mechanical alloying synthesis of forsteritediopside nanocomposite powder for using in tissue engineering. Ceramics-Silikáty. 59, 1–5 (2015)

    CAS  Google Scholar 

  20. Hafezi, M., Nezafati, N., Nadernezhad, A., Ghazanfari, S.M.H., Sepantamehr, M.: Bioinorganics in bioactive calcium silicate ceramics for bone tissue repair: bioactivity and biological properties. Ceram. Sci. Technol. 5, 1–12 (2014). https://doi.org/10.4416/JCST2013-00027

    Article  Google Scholar 

  21. Sadeghzade, S., Emadi, R., Tavangarian, F.: Combustion assisted synthesis of hardystonite nanopowder. Ceram. Inter. 42, 14656–14660 (2016). https://doi.org/10.1016/j.ceramint.2016.06.088

    Article  CAS  Google Scholar 

  22. Wu, C., Ramaswamy, Y., Zreiqat, H.: Porous Diopside (CaMgSi2O6) Scaffold: a promising bioactive material for bone tissue engineering. Acta Biomater. 6, 2237–2245 (2010). https://doi.org/10.1016/j.actbio.2009.12.022

    Article  CAS  Google Scholar 

  23. Geim, A.K., Novoselov, K.S.: The rise of graphene. Nat. Mater. 6, 183–191 (2007). https://doi.org/10.1038/nmat1849

    Article  CAS  Google Scholar 

  24. Kakran, M., Li, L.: Carbon nanomaterials for drug delivery. Key. Eng. Mater. 508, 76–80 (2012). https://doi.org/10.4028/www.scientific.net/KEM.508.76

    Article  CAS  Google Scholar 

  25. Shen, H., Zhang, L., Liu, M., Zhang, Z.: Biomedical applications of graphene. Theranostics. 2, 283–294 (2012). https://doi.org/10.7150/thno.3642

    Article  CAS  Google Scholar 

  26. Feng, L.Z., Liu, Z.A.: Graphene in biomedicine: opportunities and challenges. Nanomedicine. 6, 317–324 (2011). https://doi.org/10.2217/nnm.10.158

    Article  CAS  Google Scholar 

  27. Pan, Y., Sahoo, N.G., Li, L.: The application of graphene oxide in drug delivery. Exp. Opin. Drug. Deliv. 9, 13265–13276 (2012). https://doi.org/10.1517/17425247.2012.729575

    Article  CAS  Google Scholar 

  28. Liu, Z., Robinson, J.T., Tabakman, S.M., Yang, K., Dai, H.J.: Carbon materials for drug delivery & cancer therapy. Mater. Today. 14, 316–323 (2011). https://doi.org/10.1016/S1369-7021(11)70161-4

    Article  CAS  Google Scholar 

  29. Ghosh, D., Chandra, S., Chakraborty, A., Ghosh, S.K., Pramanik, P.: A novel graphene oxide-para amino benzoic acid nanosheet as effective drug delivery system to treat drug resistant bacteria. Int. J. Pharm. Sci. Drug. Res. 2, 127–133 (2010) https://ijpsdr.com/index.php/ijpsdr/article/view/103

    CAS  Google Scholar 

  30. Walker, L.S., Marotto, V.R., Rafiee, M.A., Koratkar, N., Corral, E.L.: Toughening in graphene ceramic composites. Acs. Nano. 5, 3182–3190 (2011). https://doi.org/10.1021/nn200319d

    Article  CAS  Google Scholar 

  31. Bódis, E., Tapasztó, O., Károly, Z., Fazekas, P., Klébert, S., Mária Keszler, A., et al.: Spark plasma sintering of Si3N4/multilayer graphene composites. Open. Chem. 13, 484–489 (2015). https://doi.org/10.1515/chem-2015-0064

    Article  Google Scholar 

  32. Kuşoğlu, I.M., Çavdar, U., Altintaş, A.: The effects of graphene nanoplatelet addition to in situ compacted alumina nanocomposites using ultra-high frequency induction sintering system. J. Aust. Ceram. Soc. 56, 233–241 (2020). https://doi.org/10.1007/s41779-019-00356-0

    Article  CAS  Google Scholar 

  33. Liu, Y., Huang, J., Li, H.: Synthesis of hydroxyapatite-reduced graphite oxide nanocomposites for biomedical applications: oriented nucleation and epitaxial growth of hydroxyapatite. Mater. Chem. B. 1, 1826–1834 (2013). https://doi.org/10.1039/C3TB00531C

    Article  CAS  Google Scholar 

  34. Liu, Y., Huang, J., Li, H.: Nanostructural characteristics of vacuum cold-sprayed hydroxyapatite/graphene-nanosheet coatings for biomedical applications. Therm. Spray. Technol. 23, 1149–1156 (2014). https://doi.org/10.1007/s11666-014-0069-2

    Article  CAS  Google Scholar 

  35. Gao, C., Liu, T., Shuai, C., Peng, S.: Enhancement mechanisms of graphene in nano-58S bioactive glass scaffold: mechanical and biological performance. Sci. Rep. 16, 4712–4722 (2012). https://doi.org/10.1038/srep04712

    Article  CAS  Google Scholar 

  36. Fan, Z., Wang, J., Liu, F., Nie, Y., Ren, L., Liu, B.: A new composite scaffold of bioactive glass nanoparticles/graphene: synchronous improvements of cytocompatibility and mechanical property. Colloids. Surf. B. 145, 438–446 (2016). https://doi.org/10.1038/srep0471210.1016/j.colsurfb.2016.05.026

    Article  CAS  Google Scholar 

  37. Mehrali, M., Moghaddam, E., Shirazi, S.F.S., Baradaran, S., Mehrali, M., Latibari, S.T., et al.: Synthesis, mechanical properties, and in vitro biocompatibility with osteoblasts of calcium silicate–reduced graphene oxide composites. Acs. Appl. Mater. Inter. 6, 3947–3962 (2014). https://doi.org/10.1021/am500845x

    Article  CAS  Google Scholar 

  38. Stankovich, S., Dikin, D.A., Dommett, G.H.B., et al.: Graphene-based composite materials. Nature. 442, 282–286 (2006). https://doi.org/10.1038/nature04969

    Article  CAS  Google Scholar 

  39. Williamson, G.K., Hall, W.H.: X-ray line broadening from filed aluminium and wolframL’elargissement des raies de rayons x obtenues des limailles d’aluminium et de tungsteneDie verbreiterung der roentgeninterferenzlinien von aluminium- und wolframspaenen. Acta Metall. 1, 22–31 (1953)

    Article  CAS  Google Scholar 

  40. Mallick, K.K.: Freeze casting of porous bioactive glass and bioceramics. Am. Ceram. Soc. 92, 85–94 (2009). https://doi.org/10.1111/j.1551-2916.2008.02784.x

    Article  CAS  Google Scholar 

  41. Heunisch, A., Dellert, A., Roosen, A.: Effect of powder, binder and process parameters on anisotropic shrinkage in tape cast ceramic products. Eur. Ceram. Soc. 30, 3397–3406 (2010). https://doi.org/10.1016/j.jeurceramsoc.2010.08.012

    Article  CAS  Google Scholar 

  42. Kokubo, T., Kushitani, H., Sakka, S., Kitsugi, T., Yamamuro, T.: Solutions able to reproduce in vivo surface-structure changes in bioactive glass-ceramic A-W3. Biomed. Mater. Res. 24, 721–734 (1990). https://doi.org/10.1002/jbm.820240607

    Article  CAS  Google Scholar 

  43. Depan, D., Misra, R.: The interplay between nanostructured carbon-grafted chitosan scaffolds and protein adsorption on the cellular response of osteoblasts: structure–function property relationship. Acta Biomater. 9, 6084–6094 (2013). https://doi.org/10.1016/j.actbio.2012.12.019

    Article  CAS  Google Scholar 

  44. Bazargan, A.M.: Sharif1, F., Mazinani, S., Naderi, N.: Highly conductive reduced graphene oxide transparent ultrathin film through joule-heat induced direct reduction. J Mater Sci: Mater Electron. 28, 1–9 (2017). https://doi.org/10.1007/s10854-016-5676-x

    Article  CAS  Google Scholar 

  45. Farzin, A., Emadi, R., Fathi, M.H.: Novel Sol-gel-derived Hardystonite-based biomagnetic nanoparticles for hyperthermia applications. J. Sol-Gel Sci. Technol. 80, 402–501 (2016). https://doi.org/10.1007/s10971-016-4100-6

    Article  CAS  Google Scholar 

  46. Bagherpour, I., Naghib, S.M., Yaghtin, A.H.: Synthesis and characterisation of nanostructured hardystonite coating on stainless steel for biomedical application. IET Nanobiotechnol. 12, 895–902 (2018). https://doi.org/10.1049/iet-nbt.2017.0275

    Article  Google Scholar 

  47. Cacciotti, I., Lombardi, M., Bianco, A., Ravaglioli, A., Montanaro, L.: Sol–gel derived 45S5 bioglass: synthesis, microstructural evolution and thermal behavior. Mater. Sci. Mater. Med. 23, 1849–1866 (2012). https://doi.org/10.1007/s10856-012-4667-6

    Article  CAS  Google Scholar 

  48. Aghajani, B., Karamian, E., Hosseini, B.: Hydroxyapatite-hardystonite nanocomposite scaffolds prepared by the replacing the polyurethane polymeric sponge technique for tissue engineering applications. Nanomed. 4, 254–262 (2017). https://doi.org/10.22038/nmj.2017.04.008

    Article  CAS  Google Scholar 

  49. Mohammadi, H., Hafezi, M., Hesaraki, S., Sepantafar, M.M.: Preparation and characterization of Sr-Ti-hardystonite (Sr-Ti-HT) nanocomposite for bone repair application. Nanomed. 2, 203–210 (2015). https://doi.org/10.7508/nmj

    Article  Google Scholar 

  50. Marcano, D.C., Kosynkin, D.V., Berlin, J.M., Sinitskii, A., Sun, Z., Slesarev, A., et al.: Improved synthesis of graphene oxide. ACS Nano. 4, 4806–4814 (2010). https://doi.org/10.1021/nn1006368

    Article  CAS  Google Scholar 

  51. Xu, Y., Bai, H., Lu, G., Li, C., Shi, G.: Flexible graphene films via the filtration of water-soluble noncovalent functionalized graphene sheets. Am. Chem. Soc. 130, 5856–5857 (2008). https://doi.org/10.1021/ja800745y

    Article  CAS  Google Scholar 

  52. Verma, S., Mungse, H.P., Kuma, N., Choudhary, S., Jain, S.L., Sain, B., et al.: Graphene oxide: an efficient and reusable carbocatalyst for aza-Michael addition of amines to activated alkenes. Chem. Commun. 47, 12673–12675 (2011). https://doi.org/10.1039/c1cc15230k

    Article  CAS  Google Scholar 

  53. Asgarian, R., Doost-Mohammadi, A.: Evaluation of corrosion behavior, bioactivity and cytotoxicity of nanostructured hardystonite coating on Ti-6Al-4V substrate. Surf. J. 28, 99–110 (2016)

    Google Scholar 

  54. Wu, C., Chang, J., Zhai, W.: A novel hardystonite bioceramic: preparation and characteristics. Ceram. Int. 31, 27–31 (2005). https://doi.org/10.1016/j.ceramint.2004.02.008

    Article  CAS  Google Scholar 

  55. Carter, C.B., Norton, M.G.: Ceramic Materials: Science and Engineering. Springer Science & Business Media, New York (2007)

    Google Scholar 

  56. Yang, H., Xu, S., Jiang, L., Dan, Y.: Thermal decomposition behavior of poly (vinyl alcohol) with different hydroxyl content. J. Macromol. Sci. Part B: Phys. 51, 464–480 (2012). https://doi.org/10.1080/00222348.2011.597687

    Article  CAS  Google Scholar 

  57. Hong, W., Meng, M., Xie, J., Gao, D., Xian, M., Wen, S., Huang, S., Kang, C.: Properties and thermal analysis study of modified polyvinyl acetate (PVA) adhesive. J. Adh. Sci. Technol. 32, 2180–2194 (2018). https://doi.org/10.1080/01694243.2018.1465687

    Article  CAS  Google Scholar 

  58. Bai, R.G., Muthoosamy, K., Manickam, S., Alnaqbi, A.H.: Graphene-based 3D scaffolds in tissue engineering: fabrication, application, and future scope in liver tissue engineering. Int. J. Nanomed. 14, 5753–5783 (2019). https://doi.org/10.2147/IJN.S192779

    Article  CAS  Google Scholar 

  59. Ege, D., Kamali, A.R., Boccaccini, A.R.: Graphene oxide/polymer-based biomaterials. Adv. Eng. Mater. 19, 1700627 (2017). https://doi.org/10.1002/adem.201700627

    Article  CAS  Google Scholar 

  60. Maca, K., Pouchly, V., Zalud, P.: Two-step sintering of oxide ceramics with various crystal structures. Eur. Ceram. Soc. 30, 583–589 (2010). https://doi.org/10.1016/j.jeurceramsoc.2009.06.008

    Article  CAS  Google Scholar 

  61. Barr, S.A., Luijten, E.: Structural properties of materials created through freeze casting. Acta Mater. 58, 709–715 (2010). https://doi.org/10.1016/j.actamat.2009.09.050

    Article  CAS  Google Scholar 

  62. Dinescu, S., Ionita, M., Pandele, A.M., Galateanu, B., Iovu, H., Ardelean, A., Costache, M., Hermenean, A.: In vitro cytocompatibility evaluation of chitosan/graphene oxide 3D scaffold composites designed for bone tissue engineering. Bio-Med. Mater. Eng. 24, 2249 (2014). https://doi.org/10.3233/BME-141037

    Article  CAS  Google Scholar 

  63. Nair, M., Nancy, D., Krishnan, A.G., Anjusree, G.S., Vadukumpully, S., Nair, S.V.: Graphene oxide nanoflakes incorporated gelatin-hydroxyapatite scaffolds enhance osteogenic differentiation of human mesenchymal stem cell. Nanotechnol. 26, 161001–161011 (2015). https://doi.org/10.1088/0957-4484/26/16/161001

    Article  CAS  Google Scholar 

  64. Munch, E., Launey, M.E., Alsem, D.H., Saiz, E., Tomsia, A.P., Ritchie, R.O.: Tough, bio-inspired hybrid materials. Science. 322, 1516–1520 (2008). https://doi.org/10.1126/science.1164865

    Article  CAS  Google Scholar 

  65. Raucci, M.G., Giugliano, D., Longo, A., Zeppetelli, S., Carotenuto, G., Ambrosio, L.: Comparative facile methods for preparing graphene oxide–hydroxyapatite for bone tissue engineering. Tissue. Eng. Reg. Med. 11, 2204–2216 (2016). https://doi.org/10.1002/term.2119

    Article  CAS  Google Scholar 

  66. Gao, C., Liu, T., Shuai, C., Peng, S.: Enhancement mechanisms of graphene in nano-58S bioactive glass scaffold: mechanical and biological performance. Sci. Rep. 4, 4712–4722 (2014). https://doi.org/10.1038/srep04712

    Article  CAS  Google Scholar 

  67. Liu, J., Yang, Y., Hasssinin, H., Jumbu, N., Deng, S., Zuo, Q., Jiang, K.: Graphene-alumina nanocomposites with improved mechanical properties for biomedical applications. ACS Appl. Mater. Interfaces. 8, 2607–2616 (2016). https://doi.org/10.1021/acsami.5b10424

    Article  CAS  Google Scholar 

  68. Liu, X., Fan, Y.C., Li, J.L., Wang, L.J., Jiang, W.: Preparation and mechanical properties of graphene nanosheet reinforced alumina composites. Adv. Eng. Mater. 17, 28–35 (2015). https://doi.org/10.1002/adem.201400231

    Article  CAS  Google Scholar 

  69. Ghzanfari, S.M.H., Zamanian, A.: Phase transformation, microstructural and mechanical properties of hydroxyapatite/alumina nanocomposite scaffolds produced by freeze casting. Ceram. Inter. 39, 9835–9844 (2013). https://doi.org/10.1016/j.ceramint.2013.05.096

    Article  CAS  Google Scholar 

  70. Sadeghpour, S., Amirjani, A.M., Hafezi, M., Zamanian, A.: Fabrication of a novel nanostructured calcium zirconium silicate scaffolds prepared by a freeze-casting method for bone tissue engineering. Ceram. Inter. 40, 16107–16114 (2014). https://doi.org/10.1016/j.ceramint.2014.07.039

    Article  CAS  Google Scholar 

  71. Hafezi, M., Nezafati, N., Ali Nadernezhad, A., Yasaei, M., Zamanian, A., Mobini, S.: Effect of sintering temperature and cooling rate on the morphology, mechanical behavior and apatite-forming ability of a novel nanostructured magnesium calcium silicate scaffold prepared by a freeze casting method. J. Mater. Sci. 49, 1297–1305 (2014). https://doi.org/10.1007/s10853-013-7813-8

    Article  CAS  Google Scholar 

  72. Shahbazi, M.A., Ghalkhani, M., Maleki, H.: Directional freeze-casting: a bioinspired method to assemble multifunctional aligned porous structures for advanced applications. Adv. Eng. Mater. 2000033–2000059 (2020). https://doi.org/10.1002/adem.202000033

  73. Baradaran, S.: Mechanical and biological evaluations of hydroxyapatite composite for orthopedic applications. Ph.D. degree, University of Malaya, Kuala lumpur, (2015).

  74. Depan, D., Pesacreta, T., Misra, R.: The synergistic effect of a hybrid graphene oxide-chitosan system and biomimetic mineralization on osteoblast function. Biomater. Sci. 2, 264–274 (2014). https://doi.org/10.1039/C3BM60192G

    Article  CAS  Google Scholar 

  75. Wan, C., Chen, B.: Poly (e-Caprolactone)/graphene oxide biocomposites: mechanical properties and bioactivity. Biomed. Mater. 6, 055010 (2011). https://doi.org/10.1088/1748-6041/6/5/055010

    Article  CAS  Google Scholar 

  76. Chengtie, W.U., Chang, J., Zhai, W., Ni, S.: A novel bioactive porous bredigite (Ca7MgSi4O16) scaffold with biomimetic apatite layer for bone tissue engineering. Mater. Sci: Mater. Med. 18, 857–864 (2007). https://doi.org/10.1007/s10856-006-0083-0

    Article  CAS  Google Scholar 

  77. Olada, A., Bakht Khosh Hagha, H., Mirmohsenia, A., Farshi Azharb, F.: Graphene oxide and montmorillonite enriched natural polymeric scaffold for bone tissue engineering. Ceram. Inter. 45, 15609–15619 (2019). https://doi.org/10.1016/j.ceramint.2019.05.071

    Article  CAS  Google Scholar 

  78. Qiang, F.U.: Freeze casting of bioactive glass and ceramic scaffolds for bone tissue engineering. Ph.D. degree. Faculty of the Graduate School of the Missuri university of science and technology. (2009)

  79. Nasrollahi, N., Dehkordi, A.N., Jamshidizad, A., Chehelgerdi, M.: Preparation of brushite cements with improved properties by adding graphene oxide. Int. J. Nanomed. 14, 3785–3797 (2019). https://doi.org/10.2147/IJN.S196666

    Article  CAS  Google Scholar 

  80. Jeong, J.T., Choi, M.K., Sim, Y., Lim, J.T., Kim, G.S., Seong, M.J., Hyung, J.H., Kim, K.S., Umar, A., Lee, S.K.: Effect of graphene oxide ratio on the cell adhesion and growth behavior on a graphene oxide-coated silicon substrate. Sci. Rep. 6, 33835–33845 (2016). https://doi.org/10.1038/srep33835

    Article  CAS  Google Scholar 

  81. Eberli, D.: Regenerative medicine and tissue engineering-cells and biomaterials, pp. 569–588. In Tech (2011)

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Funding

The authors would like to extend their gratitude for the financial supports provided by Iran National Science Foundation (INSF: Iran-Tehran, 98/ص/6220, Date: 20 April 2019) and Materials and Energy Research Center (MERC) with research grant (No.: 781397001).

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Authors and Affiliations

  1. Materials Engineering Group, Department of Mining and Metallurgical Engineering, Yazd University, Yazd, 89195-741, Iran

    Mojdeh Azizi & Mahdi Kalantar

  2. Biomaterials Research Group, Department of Nanotechnology and Advanced Materials, Materials and Energy Research Center, Karaj, 3177983634, Iran

    Nader Nezafati & Ali Zamanian

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  1. Mojdeh Azizi
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  3. Nader Nezafati
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  4. Ali Zamanian
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Correspondence to Mahdi Kalantar.

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Highlights

• Hardystonite (HT) scaffolds with different contents of (0, 0.5, 1, and 1.5 wt%) graphene oxide (GO) were successfully fabricated by freeze-casting method.

• Investigation of microstructure, physical, and mechanical properties of scaffold samples with different weight ratios of GO.

• Investigation of biological properties on the HT-1 wt% GO scaffold as the optimal sample and HT scaffold as the control sample.

• The HT-1 wt% GO scaffold with improved mechanical and biological properties could have a potential to be used as a novel bone scaffold.

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Azizi, M., Kalantar, M., Nezafati, N. et al. Fabrication, characterization, and in vitro bioactivity evaluation of freeze-cast highly porous hardystonite ceramic reinforced by graphene oxide as a novel bone scaffold. J Aust Ceram Soc 57, 947–960 (2021). https://doi.org/10.1007/s41779-021-00601-5

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  • DOI: https://doi.org/10.1007/s41779-021-00601-5

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