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Journal of Material Science and Technology Research

Articles

Vol. 10 (2023)

3D Printing of β-TCP/S53P4 Scaffolds: Physicochemical, Mechanical, and Biological in vitro Evaluation

DOI
https://doi.org/10.31875/2410-4701.2023.10.06
Submitted
June 6, 2023
Published
2023-06-06

Abstract

Abstract: The focus of bone tissue engineering is on the new strategies for developing bioactive and resorbable scaffolds, which have become an alternative to the treatment of bone diseases and trauma. β-tricalcium phosphate (β-TCP) is considered resorbable and has excellent osteoconductivity. In an attempt to achieve good densification of the β-TCP scaffold and improve its biological properties, it arises the possibility of combining this material with S53P4 bioactive glass. Several techniques are used to produce bioceramic scaffolds, among them, direct ink writing (DIW) a type of additive manufacturing based on material extrusion, which allows the production of customized parts, with high complexity and good reproducibility. This work prepared β-TCP and β-TCP/S53P4 (β-TCP/10-S53P4 = 10% wt of S53P4 and β-TCP/20-S53P4 = 20% wt of S53P4) scaffolds by DIW. The ceramic inks showed pseudoplastic behavior and the 3D-printed scaffolds showed similar aspects to the digital model. Also, the β-TCP/S53P4 scaffolds (β-TCP/10-S53P4 = 1.6 ± 0.6 MPa and β-TCP/20-S53P4 = 2.1 ± 0.9 MPa) showed an increase in compressive strength when compared to β-TCP scaffolds (0.9 ± 0.1 MPa). All scaffolds showed apatite-mineralization ability in SBF after soaking for 7 and 14 days, being that the β-TCP/20-S53P4 scaffold showed a higher ability of apatite formation compared to the other scaffolds. Concerning the biological in vitro assays, all the scaffolds showed good cell viability. Thus, the β-TCP/S53P4 scaffolds showed adequate properties which become them, good candidates, to be used in bone tissue engineering.

References

  1. H.C. Pape, A. Evans, P. Kobbe, Autologous Bone Graft: Properties and Techniques, 24 (2010) 36-40. https://doi.org/10.1097/BOT.0b013e3181cec4a1
  2. A.H. Schmidt, Autologous bone graft: Is it still the gold standard?, Injury. (2021) 1-5. https://doi.org/10.1016/j.injury.2021.01.043
  3. W. Wang, K.W.K. Yeung, Bone grafts and biomaterials substitutes for bone defect repair: A review, Bioact. Mater. 2 (2017) 224-247. https://doi.org/10.1016/j.bioactmat.2017.05.007
  4. L. Vidal, C. Kampleitner, M. Brennan, A. Hoornaert, P. Layrolle, Reconstruction of Large Skeletal Defects: Current Clinical Therapeutic Strategies and Future Directions Using 3D Printing, Front. Bioeng. Biotechnol. 8 (2020). https://doi.org/10.3389/fbioe.2020.00061
  5. T. Winkler, F.A. Sass, G.N. Duda, K. Schmidt-Bleek, A review of biomaterials in bone defect healing, remaining shortcomings and future opportunities for bone tissue engineering: The unsolved challenge, Bone Jt. Res. 7 (2018) 232-243. https://doi.org/10.1302/2046-3758.73.BJR-2017-0270.R1
  6. G. Brunello, S. Panda, L. Schiavon, S. Sivolella, L. Biasetto, M. Del Fabbro, The impact of bioceramic scaffolds on bone regeneration in preclinical in vivo studies: A systematic review, Materials (Basel). 13 (2020) 1-26. https://doi.org/10.3390/ma13071500
  7. K. Lin, R. Sheikh, S. Romanazzo, I. Roohani, 3D printing of bioceramic scaffolds-barriers to the clinical translation: From promise to reality, and future perspectives, Materials (Basel). 12 (2019). https://doi.org/10.3390/ma12172660
  8. F. Baino, G. Novajra, C. Vitale-Brovarone, Bioceramics and scaffolds: A winning combination for tissue engineering, Front. Bioeng. Biotechnol. 3 (2015) 1-17. https://doi.org/10.3389/fbioe.2015.00202
  9. H. Jodati, B. Yılmaz, Z. Evis, A review of bioceramic porous scaffolds for hard tissue applications: Effects of structural features, Ceram. Int. 46 (2020) 15725-15739. https://doi.org/10.1016/j.ceramint.2020.03.192
  10. M.V. Varma, B. Kandasubramanian, S.M. Ibrahim, 3D printed scaffolds for biomedical applications, Mater. Chem. Phys. 255 (2020) 123642. https://doi.org/10.1016/j.matchemphys.2020.123642
  11. R. Galante, C.G. Figueiredo-Pina, A.P. Serro, Additive manufacturing of ceramics for dental applications: A review, Dent. Mater. 35 (2019) 825-846. https://doi.org/10.1016/j.dental.2019.02.026
  12. Y. Yang, G. Wang, H. Liang, C. Gao, S. Peng, L. Shen, C. Shuai, Additive manufacturing of bone scaffolds, Int. J. Bioprinting. 5 (2019) 1-25. https://doi.org/10.18063/ijb.v5i1.148
  13. X. Zhou, Y. Feng, J. Zhang, Y. Shi, L. Wang, Recent advances in additive manufacturing technology for bone tissue engineering scaffolds, Int. J. Adv. Manuf. Technol. 108 (2020) 3591-3606. https://doi.org/10.1007/s00170-020-05444-1
  14. Y. Chen, W. Li, C. Zhang, Z. Wu, J. Liu, Recent Developments of Biomaterials for Additive Manufacturing of Bone Scaffolds, Adv. Healthc. Mater. 9 (2020) 1-28. https://doi.org/10.11648/j.am.20200901.11
  15. C. Garot, G. Bettega, C. Picart, Additive Manufacturing of Material Scaffolds for Bone Regeneration: Toward Application in the Clinics, Adv. Funct. Mater. 31 (2021) 1-17. https://doi.org/10.1002/adfm.202006967
  16. E. Peng, D. Zhang, J. Ding, Ceramic Robocasting: Recent Achievements, Potential, and Future Developments, Adv. Mater. 30 (2018) 1-14.
  17. https://doi.org/10.1002/adma.201802404
  18. U. Golcha, A.S. Praveen, D.L. Belgin Paul, Direct ink writing of ceramics for bio medical applications - A Review, IOP Conf. Ser. Mater. Sci. Eng. 912 (2020). https://doi.org/10.1088/1757-899X/912/3/032041
  19. M. Ginebra, Rheological characterisation of ceramic inks for 3D direct ink writing: A review, J. Eur. Ceram. Soc. (2021). J.H. Shepherd, S.M. Best, Calcium phosphate scaffolds for bone repair, Jom. 63 (2011) 83-92. https://doi.org/10.1007/s11837-011-0063-9
  20. Q. Liu, W.F. Lu, W. Zhai, Toward stronger robocast calcium phosphate scaffolds for bone tissue engineering: A mini-review and meta-analysis, Mater. Sci. Eng. C. (2021) 112578. https://doi.org/10.1016/j.msec.2021.112578
  21. H. Ma, C. Feng, J. Chang, C. Wu, 3D-printed bioceramic scaffolds: From bone tissue engineering to tumor therapy, Acta Biomater. 79 (2018) 37-59. https://doi.org/10.1016/j.actbio.2018.08.026
  22. N. Eliaz, N. Metoki, Calcium phosphate bioceramics: A review of their history, structure, properties, coating technologies and biomedical applications, Materials (Basel). 10 (2017). https://doi.org/10.3390/ma10040334
  23. A. Boskey, Bone mineral crystal size., Osteoporos. Int. 14 Suppl 5 (2003) 16-21.
  24. https://doi.org/10.1007/s00198-003-1468-2
  25. R.Z. Legeros, J.P. Legeros, Hydroxyapatite, Bioceram. Their Clin. Appl. (2008) 367-394. https://doi.org/10.1533/9781845694227.2.367
  26. C. Rey, C. Combes, C. Drouet, M.J. Glimcher, Bone mineral: Update on chemical composition and structure, Osteoporos. Int. 20 (2009) 1013-1021. https://doi.org/10.1007/s00198-009-0860-y
  27. J. Jeong, J.H. Kim, J.H. Shim, N.S. Hwang, C.Y. Heo, Bioactive calcium phosphate materials and applications in bone regeneration, Biomater. Res. 23 (2019) 1-11. https://doi.org/10.1186/s40824-018-0153-7
  28. J. Lu, H. Yu, C. Chen, Biological properties of calcium phosphate biomaterials for bone repair: a review, RSC Adv. (2018) 2015-2033. https://doi.org/10.1039/C7RA11278E
  29. Z.F. Chen, B.W. Darvell, V.W.H. Leung, Hydroxyapatite solubility in simple inorganic solutions, Arch. Oral Biol. 49 (2004) 359-367. https://doi.org/10.1016/j.archoralbio.2003.12.004
  30. S. Yamada, D. Heymann, J.M. Bouler, G. Daculsi, Osteoclastic resorption of calcium phosphate ceramics with different hydroxyapatite/β-tricalcium phosphate ratios, Biomaterials. 18 (1997) 1037-1041. https://doi.org/10.1016/S0142-9612(97)00036-7
  31. M. Bohner, B.L.G. Santoni, N. Döbelin, β-tricalcium phosphate for bone substitution: Synthesis and properties, Acta Biomater. 113 (2020) 23-41. https://doi.org/10.1016/j.actbio.2020.06.022
  32. R. Al Jasser, A. AlSubaie, F. AlShehri, Effectiveness of beta-tricalcium phosphate in comparison with other materials in treating periodontal infra-bony defects around natural teeth: a systematic review and meta-analysis, BMC Oral Health. 21 (2021) 1-14. https://doi.org/10.1186/s12903-021-01570-8
  33. E. Champion, Sintering of calcium phosphate bioceramics, Acta Biomater. 9 (2013) 5855-5875. https://doi.org/10.1016/j.actbio.2012.11.029
  34. H.S. Ryu, H.J. Youn, K. Sun Hong, B.S. Chang, C.K. Lee, S.S. Chung, An improvement in sintering property of β-tricalcium phosphate by addition of calcium pyrophosphate, Biomaterials. 23 (2002) 909-914. https://doi.org/10.1016/S0142-9612(01)00201-0
  35. J.H. Lopes, J.A. Magalhães, R.F. Gouveia, C.A. Bertran, M. Motisuke, S.E.A. Camargo, E. de S. Trichês, Hierarchical structures of β-TCP/45S5 bioglass hybrid scaffolds prepared by gelcasting, J. Mech. Behav. Biomed. Mater. 62 (2016) 10-23. https://doi.org/10.1016/j.jmbbm.2016.04.028
  36. Y. Ma, H. Dai, X. Huang, Y. Long, 3D printing of bioglass-reinforced β-TCP porous bioceramic scaffolds, J. Mater. Sci. 54 (2019) 10437-10446. https://doi.org/10.1007/s10853-019-03632-3
  37. S.B. Hua, J. Su, Z.L. Deng, J.M. Wu, L.J. Cheng, X. Yuan, F. Chen, H. Zhu, D.H. Qi, J. Xiao, Y.S. Shi, Microstructures and properties of 45S5 bioglass® & BCP bioceramic scaffolds fabricated by digital light processing.pdf, Addit. Manuf. 45 (2021) 102074. https://doi.org/10.1016/j.addma.2021.102074
  38. L.L. Hench, The story of Bioglass®, J. Mater. Sci. Mater. Med. 17 (2006) 967-978. https://doi.org/10.1007/s10856-006-0432-z
  39. D.C. Greenspan, Glass, and Medicine: The Larry Hench Story, Int. J. Appl. Glas. Sci. 7 (2016). https://doi.org/10.1111/ijag.12204
  40. J.R. Jones, Reprint of Review of bioactive glass: From Hench to hybrids, Acta Biomater. 23 (2015) S53-S82. https://doi.org/10.1016/j.actbio.2015.07.019
  41. F. Baino, S. Hamzehlou, S. Kargozar, Bioactive glasses: Where are we and where are we going?, J. Funct. Biomater. 9 (2018). https://doi.org/10.3390/jfb9010025
  42. L.L. Hench, Some comments on bioglass: Four eras of discovery and development, Biomed. Glas. 1 (2015). https://doi.org/10.1515/bglass-2015-0001
  43. J.R. Jones, D.S. Brauer, L. Hupa, D.C. Greenspan, Bioglass and Bioactive Glasses and Their Impact on Healthcare, Int. J. Appl. Glas. Sci. 7 (2016) 423-434. https://doi.org/10.1111/ijag.12252
  44. N.A.P. Van Gestel, J. Geurts, D.J.W. Hulsen, B. Van Rietbergen, S. Hofmann, J.J. Arts, Clinical Applications of S53P4 Bioactive Glass in Bone Healing and Osteomyelitis Treatment: A Literature Review, Biomed Res. Int. (2015). https://doi.org/10.1155/2015/684826
  45. A.P.N. Alves, M. Arango-Ospina, R.L.M.S. Oliveira, I.M. Ferreira, E.G. de Moraes, M. Hartmann, A.P.N. de Oliveira, A.R. Boccaccini, E. de Sousa Trichês, 3D-printed β-TCP/S53P4 bioactive glass scaffolds coated with tea tree oil: Coating optimization, in vitro bioactivity and antibacterial properties, J. Biomed. Mater. Res. - Part B Appl. Biomater. (2022) 1-14.
  46. R.L.M.S. Oliveira, A.P.N. Alves, L. Barbosa, A.P. Silva, G.L. de Cena, K. Conceição, D.B. Tada, E. de S. Trichês, 3D printing of bioactive glass S53P4/sodium alginate sintering-free scaffolds, Bioprinting. 27 (2022). https://doi.org/10.1016/j.bprint.2022.e00226
  47. E. Feilden, E.G.T. Blanca, F. Giuliani, E. Saiz, L. Vandeperre, Robocasting of structural ceramic parts with hydrogel inks, J. Eur. Ceram. Soc. 36 (2016) 2525-2533. https://doi.org/10.1016/j.jeurceramsoc.2016.03.001
  48. T. Kokubo, H. Kushitani, S. Sakka, T. Kitsugi, T. Yamamuro, Solutions able to reproduce in vivo surface‐structure changes in bioactive glass‐ceramic A‐W3, J. Biomed. Mater. Res. 24 (1990) 721-734. https://doi.org/10.1002/jbm.820240607
  49. T. Kokubo, H. Takadama, How useful is SBF in predicting in vivo bone bioactivity?, Biomaterials. 27 (2006) 2907-2915. https://doi.org/10.1016/j.biomaterials.2006.01.017
  50. D. de C.R. Mello, L.M. Rodrigues, F.Z.D. Mello, T.F. Gonçalves, B. Ferreira, S.G. Schneider, L.D. de Oliveira, L.M.R. de Vasconcellos, Biological and microbiological interactions of Ti-35Nb-7Zr alloy and its basic elements on bone marrow stromal cells: good prospects for bone tissue engineering, Int. J. Implant Dent. 6 (2020). https://doi.org/10.1186/s40729-020-00261-3
  51. ISO 10993-5:2009(en), Biological evaluation of medical devices - Part 5: Tests for in vitro cytotoxicity, (n.d.).
  52. O.H. Lowry, N.J. Rosebrough, A.L. Farr, R.J. Randall, Protein Measurement with the Folin Phenol Reagent*, (1951). https://doi.org/10.1016/S0021-9258(19)52451-6
  53. B.R. Spirandeli, T.M.B. Campos, R.G. Ribas, G.P. Thim, E. de S. Trichês, Evaluation of colloidal and polymeric routes in sol-gel synthesis of a bioactive glass-ceramic derived from 45S5 bioglass, Ceram. Int. 46 (2020) 20264-20271. https://doi.org/10.1016/j.ceramint.2020.05.108
  54. F. Baino, S. Caddeo, C. Vitale-brovarone, Sintering effects of bioactive glass incorporation in tricalcium phosphate scaffolds - Journal Pre-proofs, Mater. Lett. 274 (2020) 128010. https://doi.org/10.1016/j.matlet.2020.128010
  55. H. Zhu, M. Li, X. Huang, D. Qi, L.P. Nogueira, X. Yuan, W. Liu, Z. Lei, J. Jiang, H. Dai, J. Xiao, 3D printed tricalcium phosphate-bioglass scaffold with gyroid structure enhance bone ingrowth in challenging bone defect treatment, Appl. Mater. Today. 25 (2021). https://doi.org/10.1016/j.apmt.2021.101166
  56. X. Li, H. Zhang, Y. Shen, Y. Xiong, L. Dong, J. Zheng, S. Zhao, Fabrication of porous β-TCP/58S bioglass scaffolds via top-down DLP printing with high solid loading ceramic-resin slurry, Mater. Chem. Phys. 267 (2021). https://doi.org/10.1016/j.matchemphys.2021.124587
  57. P.A. Forero-Sossa, J.D. Salazar-Martinez, V.J. Barajas-Aguilar, I.U. Olvera-Alvarez, J. Henao, D.G. Espinosa-Arbelaez, G. Trápaga-Martínez, A.L. Giraldo-Betancur, Effect of S53P4 bioactive glass content on structural and in-vitro behavior of hydroxyapatite/bioactive glass mixtures prepared by mechanical milling, Ceram. Int. 49 (2022) 4322-4330. https://doi.org/10.1016/j.ceramint.2022.09.317
  58. A.M. Pietak, J.W. Reid, M.J. Stott, M. Sayer, Silicon substitution in the calcium phosphate bioceramics, Biomaterials. 28 (2007) 4023-4032. https://doi.org/10.1016/j.biomaterials.2007.05.003
  59. C. Shuai, W. Yang, P. Feng, S. Peng, H. Pan, Accelerated degradation of HAP/PLLA bone scaffold by PGA blending facilitates bioactivity and osteoconductivity, Bioact Mater. 6 (2021) 490-502. https://doi.org/10.1016/j.bioactmat.2020.09.001
  60. P. Feng, P. Wu, C. Gao, Y. Yang, W. Guo, W. Yang, C. Shuai, A Multimaterial Scaffold With Tunable Properties: Toward Bone Tissue Repair, Advanced Science. 5 (2018). https://doi.org/10.1002/advs.201700817
  61. P. Feng, K. Wang, Y. Shuai, S. Peng, Y. Hu, C. Shuai, Hydroxyapatite nanoparticles in situ grown on carbon nanotube as a reinforcement for poly (ε-caprolactone) bone scaffold, Mater Today Adv. 15 (2022). https://doi.org/10.1016/j.mtadv.2022.100272
  62. C. Shuai, B. Peng, P. Feng, L. Yu, R. Lai, A. Min, In situ synthesis of hydroxyapatite nanorods on graphene oxide nanosheets and their reinforcement in biopolymer scaffold, J Adv Res. 35 (2022) 13-24. https://doi.org/10.1016/j.jare.2021.03.009
  63. J. Sarin, M. Vuorenmaa, P.K. Vallittu, R. Grénman, P. Boström, P. Riihilä, L. Nissinen, V.M. Kähäri, J. Pulkkinen, The Viability and Growth of HaCaT Cells After Exposure to Bioactive Glass S53P4-Containing Cell Culture Media, Otol. Neurotol. 42 (2021) e559-e567. https://doi.org/10.1097/MAO.0000000000003057
  64. M. Waselau, M. Patrikoski, B. Mannerström, M. Raki, K.A. Bergstroem, B. von Rechenberg, S. Miettinen, In vivo Effects of Bioactive Glass S53P4 or Beta Tricalcium Phosphate on Osteogenic Differentiation of Human Adipose Stem Cells after Incubation with BMP-2, J. Stem Cell Res. Ther. 2 (2012) art. 1000125. https://doi.org/10.4172/2157-7633.1000125
  65. M.M. Beloti, A.L. Rosa, M. Márcio, A. Beloti, R. Luiz, Osteoblast differentiation of human bone marrow cells under continuous and discontinuous treatment with dexamethasone, Braz. Dent. J. 16 (2005) 156-161. https://doi.org/10.1590/S0103-64402005000200013
  66. Y.P. Chen, Y.L. Chu, Y.H. Tsuang, Y. Wu, C.Y. Kuo, Y.J. Kuo, Anti-Inflammatory Effects of Adenine Enhance Osteogenesis in the Osteoblast-Like MG-63 Cells, Life 2020, Vol. 10, Page 116. 10 (2020) 116. https://doi.org/10.3390/life10070116
  67. A. Suzuki, J. Guicheux, G. Palmer, Y. Miura, Y. Oiso, J.P.P. Bonjour, J. Caverzasio, Evidence for a role of p38 MAP kinase in expression of alkaline phosphatase during osteoblastic cell differentiation, Bone. 30 (2002) 91-98. https://doi.org/10.1016/S8756-3282(01)00660-3
  68. S. Prabakaran, M. Rajan, C. Lv, G. Meng, Lanthanides-substituted Hydroxyapatite/Aloe vera composite coated titanium plate for bone tissue regeneration, Int. J. Nanomedicine. 15 (2020) 8261-8279. https://doi.org/10.2147/IJN.S267632
  69. M. Ojansivu, A. Mishra, S. Vanhatupa, M. Juntunen, A. Larionova, J. Massera, S. Miettinen, The effect of S53P4-based borosilicate glasses and glass dissolution products on the osteogenic commitment of human adipose stem cells, PLoS One. 13 (2018) e0202740. https://doi.org/10.1371/journal.pone.0202740
  70. P.K. Vallittu, T.O. Närhi, L. Hupa, Fiber glass-bioactive glass composite for bone replacing and bone anchoring implants, Dent. Mater. 31 (2015) 371-381. https://doi.org/10.1016/j.dental.2015.01.003