Preparation of trivalent rare-earth element-substituted bioactive glass robocast scaffolds for osteosarcoma treatment: structural, morphological, mechanical, drug delivery, and biological properties
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Abstract
Abstract In this study, trivalent rare-earth ion (Eu3+, Gd3+, and Yb3+)-substituted silicate-based bioactive glass scaffolds were prepared by robocasting method using sol–gel-derived bioactive glass powders for tissue engineering applications and cancer therapy. The structural, morphological, and mechanical properties of the prepared scaffolds as well as their in vitro bioactivity in simulated body fluid (SBF) were investigated in detail. In addition, an anticancer drug (5-FU) adsorption and release behavior of the scaffolds was studied as a function of time. In vitro, cytotoxicity and alkaline phosphatase activity were investigated using human skin fibroblast BJ and osteosarcoma SaOS-2 cells. Results showed that using lanthanide ion-containing (0.5, 1, 3, and 5 wt%) sol–gel-derived bioactive glass powders it was possible to successfully fabricate periodic, mesh-like patterned robocast glass scaffolds. All of the scaffolds prepared in the study sintered at 675 °C showed an amorphous structure. The compressive strength of scaffolds was in the range of 8.8 MPa to 13.6 MPa and the highest strength values were obtained in the Yb3+-containing scaffolds. Hydroxyapatite formation was obtained for the scaffolds immersed in SBF for 28 days. The fluorouracil adsorption amount was calculated to be ~ 25% for all types of scaffolds and the cumulative drug release was in the range of 20–25% depending on the dopant concentration. Results of the in vitro cell culture experiments revealed that all of the scaffolds fabricated in the study were not cytotoxic to fibroblast and osteosarcoma cells for up to 7 days under in vitro conditions. An increase was obtained for the ALP activities for both types of cells as the incubation time was increased.
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Research context
OpenAlex topics: Bone Tissue Engineering Materials · Facial Trauma and Fracture Management · Dental Implant Techniques and Outcomes
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References (53)
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1. E. Sharifi, A. Bigham, S. Yousefiasl, M. Trovato, M. Ghomi, Y. Esmaeili, P. Samadi, A. Zarrabi, M. Ashrafizadeh, S. Sharifi, R. Sartorius, F. Dabbagh, A. Maleki, H. Song, T. Agarwal, T.K. Maiti, N. Nikfarjam, C. Burvill, V. Mattoli, M.G. Raucci, K. Zheng, A.R. Boccaccini, L. Ambrosio, P. Makvandi, Mesoporous bioactive glasses in cancer diagnosis and therapy: stimuli-responsive, toxicity, immunogenicity, and clinical translation. Adv. Sci. 9, 2102678 (2022). https://doi.org/10.1002/advs.20210267810.1002/advs.202102678 ↗
2. Y. Lin, J.C. Mauro, G. Kaur, Chapter 10—bioactive glasses for cancer therapy, in Woodhead publishing series in biomaterials, biomedical, therapeutic and clinical applications of bioactive Glasses. ed. by G. Kaur (Woodhead Publishing, 2019), pp.273–312. https://doi.org/10.1016/B978-0-08-102196-5.00010-010.1016/B978-0-08-102196-5.00010-0 ↗
3. L.L. Hench, R.J. Splinter, W.C. Allen, T.K. Greenlee, Bonding mechanism at the interface of ceramic prosthetic materials. J. Biomed. Mater. Res. 2, 117–141 (1971). https://doi.org/10.1002/jbm.82005061110.1002/jbm.820050611 ↗
4. J.R. Jones, Review of bioactive glass: from Hench to hybrids. Acta Biomater. 9(1), 4457–4486 (2013). https://doi.org/10.1016/j.actbio.2012.08.023. (Epub 2012 Aug 21 PMID: 22922331)10.1016/j.actbio.2012.08.023 ↗
5. M.N. Rahaman, D.E. Day, B.S. Bal, Q. Fu, S.B. Jung, L.F. Bonewald, A.P. Tomsia, Bioactive glass in tissue engineering. Acta Biomater. 7, 2355-2373 (2011). https://doi.org/10.1016/j.actbio.2011.03.01610.1016/j.actbio.2011.03.016 ↗
6. V. Mouriño, J.P. Cattalini, A.R. Boccaccini, Metallic ions as therapeutic agents in tissue engineering scaffolds: an overview of their biological applications and strategies for new developments. J. R. Soc. Interface. 9(68), 401–419 (2012). https://doi.org/10.1098/rsif.2011.0611. (Epub 2011 Dec 7. PMID: 22158843; PMCID: PMC3262432)10.1098/rsif.2011.0611 ↗
7. B.A.E. Ben-Arfa, I.E. Palamá, I.M. Miranda Salvado, J.M.F. Ferreira, R.C. Pullar, Cytotoxicity and bioactivity assessments for Cu2+ and La3+ doped high-silica sol-gel derived bioglasses: the complex interplay between additive ions revealed. J. Biomed. Mater. Res. 107A, 2680–2693 (2019). https://doi.org/10.1002/jbm.a.3677210.1002/jbm.a.36772 ↗
8. M. Wang, G. Pi, Bo. Lei, Europium doped monodispersed bioactive glass nanoparticles regulate the osteogenic differentiation of human marrow mesenchymal stem cells. J. Biomed. Nanotechnol. 14, 756–764 (2018). https://doi.org/10.1166/jbn.2018.250410.1166/jbn.2018.2504 ↗
9. A.M. Deliormanlı, B. Rahman, S. Oguzlar, M.Z. Ongun, Investigation of the structural, photoluminescence properties, bioactivity and 5-fluorouracil delivery behavior of Dy3+ and Dy:Eu3+-doped bioactive glasses. J. Alloys Compounds. 944, 169153 (2023). https://doi.org/10.1016/j.jallcom.2023.16915310.1016/j.jallcom.2023.169153 ↗
10. A.M. Deliormanli, S.A.M. Issa, M.S. Al-Buriahi, B. Rahman, H.M.H. Zakaly, H.O. Tekin, Erbium (III)- and Terbium (III)-containing silicate-based bioactive glass powders: physical, structural and nuclear radiation shielding characteristics. Appl. Phys. A 127, 463 (2021). https://doi.org/10.1007/s00339-021-04615-510.1007/s00339-021-04615-5 ↗
11. A.M. Deliormanlı, M. Türk, Flow behavior and drug release study of injectable pluronic F-127 hydrogels containing bioactive glass and carbon-based nanopowders. J. Inorg. Organomet. Polym. 30, 1184–1196 (2020). https://doi.org/10.1007/s10904-019-01346-210.1007/s10904-019-01346-2 ↗
12. M. Duchna, I. Cieślik, Rare earth elements in new advanced engineering applications. Rare earth elements—emerging advances technology utilization and resource procurement (IntechOpen, 2023). https://doi.org/10.5772/intechopen.10924810.5772/intechopen.109248 ↗
13. A. Baranowska, M. Kochanowicz, J. Żmojda, P. Miluski, A. Wajda, M. Leśniak, D. Dorosz, Biological properties of rare-earth doped bioactive glass (SPIE, 2020). https://doi.org/10.1117/12.256634710.1117/12.2566347 ↗
14. F. Fernández, R. Sáez-Puche, C. Cascales, C.M. Marcano, I. Rasines, X-ray diffraction data and magnetic properties of the oxides R3Sb5O12 (R = Pr, Nd, Sm, Eu, Gd, Yb). J. Phys. Chem. Solids 50(9), 871–875 (1989). https://doi.org/10.1016/0022-3697(89)90033-410.1016/0022-3697(89)90033-4 ↗
15. A.M. Deliormanlı, S.Z. Oguzlar, M. Ongun, Effects of Eu3+, Gd3+ and Yb3+ substitution on the structural, photoluminescence, and decay properties of silicate-based bioactive glass powders. J. Mater. Res. 37, 622–635 (2022). https://doi.org/10.1557/s43578-021-00461-610.1557/s43578-021-00461-6 ↗
16. N.L. Ignjatović, L. Mančić, M. Vuković, Z. Stojanović, M.G. Nikolić, S. Škapin, S. Jovanović, L. Veselinović, V. Uskoković, S. Lazić, S. Marković, M.M. Lazarević, D.P. Uskoković, Rare-earth (Gd3+, Yb3+/Tm3+, Eu3+) co-doped hydroxyapatite as magnetic, up-conversion and down-conversion materials for multimodal imaging. Sci. Rep. 9(1), 16305 (2019). https://doi.org/10.1038/s41598-019-52885-010.1038/s41598-019-52885-0 ↗
17. F.S. Canisares, A.M. Mutti, D.G. Cavalcante, A.E. Job, A.M. Pires, S.A. Lima, Luminescence and cytotoxic study of red emissive europium(III) complex as a cell dye. J. Photochem. Photobiol. A Chem. 422, 113552 (2022). https://doi.org/10.1016/j.jphotochem.2021.11355210.1016/j.jphotochem.2021.113552 ↗
18. E. Andronescu, D. Predoi, I.A. Neacsu, A.V. Paduraru, A.M. Musuc, R. Trusca, O. Oprea, E. Tanasa, O.R. Vasile, A.I. Nicoara et al., Photoluminescent hydroxylapatite: Eu3+ doping effect on biological behaviour. Nanomaterials 9(9), 1187 (2019). https://doi.org/10.3390/nano909118710.3390/nano9091187 ↗
19. M. Rogosnitzky, S. Branch, Gadolinium-based contrast agent toxicity: a review of known and proposed mechanisms. Biometals 29(3), 365–376 (2016). https://doi.org/10.1007/s10534-016-9931-710.1007/s10534-016-9931-7 ↗
20. M.A. Sieber, H. Pietsch, J. Walter, W. Haider, T. Frenzel, H.J. Weinmann, A preclinical study to investigate the development of nephrogenic systemic fibrosis: a possible role for gadolinium-based contrast media. Investig Radiol. 43, 65–75 (2008). https://doi.org/10.1097/RLI.0b013e31815e627710.1097/RLI.0b013e31815e6277 ↗
21. M. Port, J.M. Idee, C. Medina, C. Robic, M. Sabatou, C. Corot, Efficiency, thermodynamic and kinetic stability of marketed gadolinium chelates and their possible clinical consequences: a critical review. Biometals 21, 469–490 (2008). https://doi.org/10.1007/s10534-008-9135-x10.1007/s10534-008-9135-x ↗
22. Y.C. Dong, A. Kumar, D.N. Rosario-Berríos, S. Si-Mohamed, J.C. Hsu, L.M. Nieves, P. Douek, P.B. Noël, D.P. Cormode, Ytterbium nanoparticle contrast agents for conventional and spectral photon-counting CT and their applications for hydrogel imaging. ACS Appl. Mater. Interfaces 14(34), 39274–39284 (2022). https://doi.org/10.1021/acsami.2c1235410.1021/acsami.2c12354 ↗
23. Z. Liu, Z. Li, J. Liu, Gu. Song, Q. Yuan, J. Ren, Qu. Xiaogang, Long-circulating Er3+-doped Yb2O3 up-conversion nanoparticle as an in vivo X-Ray CT imaging contrast agent. Biomaterials 33(28), 6748–6757 (2012). https://doi.org/10.1016/j.biomaterials.2012.06.03310.1016/j.biomaterials.2012.06.033 ↗
24. V. Selvaraj, S. Bodapati, E. Murray, K.M. Rice, N. Winston, T. Shokuhfar, Y. Zhao, E. Blough, Cytotoxicity and genotoxicity caused by yttrium oxide nanoparticles in HEK293 cells. Int. J. Nanomed. 12(9), 1379–1391 (2014). https://doi.org/10.2147/IJN.S5262510.2147/IJN.S52625 ↗
25. S. Oğuzlar, M.Z. Ongun, A.M. Deliormanlı, Modulation of optical oxygen sensitivity of H2(TPP) by using Eu3+, Gd3+ and Yb3+ ions doped silicate-based bioactive glass powders immersed in simulated body fluid. Optik, 294, 171458 (2023). https://doi.org/10.1016/j.ijleo.2023.17145810.1016/j.ijleo.2023.171458 ↗
26. A. Şakar-Deliormanlı, E. Celik, M. Polat, Adsorption of anionic polyelectrolyte and comb polymers onto lead magnesium niobate. Colloids Surfaces A 316(1–3), 202–209 (2008). https://doi.org/10.1016/j.colsurfa.2007.09.004. (ISSN 0927-7757)10.1016/j.colsurfa.2007.09.004 ↗
27. A.M. Deliormanlı, M. Türk, H. Atmaca, Response of mouse bone marrow mesenchymal stem cells to graphene-containing grid-like bioactive glass scaffolds produced by robocasting. J. Biomater. Appl. 33(4), 488–500 (2018). https://doi.org/10.1177/088532821879961010.1177/0885328218799610 ↗
28. A.M. Deliormanlı, B. Rahman, Fabrication and characterization of novel multifunctional superparamagnetic and fluorescent bioactive glasses for biomedical applications. J. Alloys Compounds 967, 171653 (2023). https://doi.org/10.1016/j.jallcom.2023.17165310.1016/j.jallcom.2023.171653 ↗
29. T. Kokubo, H. Takadama, How useful is SBF in predicting in vivo bone bioactivity? Biomaterials 27(15), 2907–2915 (2006). https://doi.org/10.1016/j.biomaterials.2006.01.01710.1016/j.biomaterials.2006.01.017 ↗
30. E. Murray, D. Provvedini, D. Curran, B. Catherwood, H. Sussman, S. Manolagas, Characterization of a human osteoblastic osteosarcoma cell line (SAOS-2) with high bone alkaline phosphatase activity. J. Bone Mineral Res. 2, 231–238 (2009). https://doi.org/10.1002/jbmr.565002031010.1002/jbmr.5650020310 ↗
31. H.-J. Hausser, R.E. Brenner, Phenotypic instability of Saos-2 cells in long-term culture. Biochem. Biophys. Res. Commun. 333(1), 216–222 (2005). https://doi.org/10.1016/j.bbrc.2005.05.09710.1016/j.bbrc.2005.05.097 ↗
32. S.P. Pereira, C.M. Deus, T.L. Serafim, T. Cunha-Oliveira, P.J. Oliveira, Metabolic and phenotypic characterization of human skin fibroblasts after forcing oxidative capacity. Toxicol. Sci. 164(1), 91–204 (2018). https://doi.org/10.1093/toxsci/kfy06810.1093/toxsci/kfy068 ↗
33. P.W. Sylvester, Optimization of the tetrazolium dye (MTT) colorimetric assay for cellular growth and viability. Methods Mol. Biol. 716, 157–168 (2011). https://doi.org/10.1007/978-1-61779-012-6_910.1007/978-1-61779-012-6_9 ↗
34. A.M. Efimov, V.G. Pogareva, IR absorption spectra of vitreous silica and silicate glasses: the nature of bands in the 1300 to 5000 cm-1 region. Chem. Geol. 229, 198–217 (2006). https://doi.org/10.1016/j.chemgeo.2006.01.02210.1016/j.chemgeo.2006.01.022 ↗
35. W. R. Taylor, Application of infrared spectroscopy to studies of silicate glass structure: Examples from the melilite glasses and the systems Na20-SiO2 and Na20-AI203-SiO2, Proc. Indian Acad. Sci. (Earth Planet. Sci.), 99(1), 99–117 (1990)10.1007/BF02871899 ↗
36. M. Trivedi, A. Branton, D. Trivedi, G. Nayak, K. Bairwa, S. Jana, Spectroscopic characterization of disodium hydrogen orthophosphate and sodium nitrate after biofield treatment. J. Chromatogr. Sep. Tech. 6(5),1000282 (2015). https://doi.org/10.4172/2157-7064.100028210.4172/2157-7064.1000282 ↗
37. A. Aronne, S. Esposito, P. Pernice, FTIR and DTA study of lanthanum aluminosilicate glasses. Mater. Chem. Phys. 51, 163–168 (1997). https://doi.org/10.1016/S0254-0584(97)80287-810.1016/S0254-0584(97)80287-8 ↗
38. G. Hou, C. Zhang, Fu. Wenbin, G. Li, J. Xia, Y. Ping, Improvement of mechanical strength in Y3+/La3+ co-doped silicate glasses for display screen. Ceram. Int. 45(9), 11850–11855 (2019). https://doi.org/10.1016/j.ceramint.2019.03.06610.1016/j.ceramint.2019.03.066 ↗
39. M.T. Wang, M. Li, J.S. Cheng, F. He, Z.G. Liu, Y.H. Hu, The role of Gd2O3 and Y2O3 in corrosion of soda lime silicate glass. J. Nucl. Mater. 433(1–3), 287–296 (2013). https://doi.org/10.1016/j.jnucmat.2012.09.03210.1016/j.jnucmat.2012.09.032 ↗
40. C.E. Misch, Z. Qu, M.W. Bidez, Mechanical properties of trabecular bone in the human mandible: implications for dental implant treatment planning and surgical placement. J. Oral Maxillofac. Surg. 57(6), 700–706 (1999). https://doi.org/10.1016/s0278-2391(99)90437-810.1016/s0278-2391(99)90437-8 ↗
41. O.H. Andersson, K.H. Karlsson, K. Kngasniemi, Calcium phosphate formation at the surface of bioactive glass in vivo. J. Non Cryst. Solids 119, 290–296 (1990). https://doi.org/10.1016/0022-3093(90)90301-210.1016/0022-3093(90)90301-2 ↗
42. G.A. Stanciu, I. Sandulescu, B. Savu, S.G. Stanciu, K.M. Paraskevopoulos, X. Chatzistavrou, E. Kontonasaki, P. Koidis, Investigation of the hydroxyapatite growth on bioactive glass surface. J. Biomed. Pharm. Eng. 1(1), 34–39 (2007)
43. L. Berzina-Cimdina, N. Borodajenko, Research of calcium phosphates using fourier transform infrared spectroscopy, in Infrared spectroscopy—materials science, engineering and technology. ed. by T. Theophile (InTech, 2012)
44. S. Gallinetti, C. Canal, M.-P. Ginebra, Development and Characterization of Biphasic Hydroxyapatite/β-TCP Cements. J. Am. Ceram. Soc. 97, 1065–1073 (2014). https://doi.org/10.1111/jace.1286110.1111/jace.12861 ↗
45. R.R. Earle, K.K. Bandaru, L. Usha, Formulation and characterization of sustained release coated matrix granules of metformin hydrochloride. Asian J. Pharm. Clin. Res. 11, 387 (2018). https://doi.org/10.22159/ajpcr.2018.v11i7.2499610.22159/ajpcr.2018.v11i7.24996 ↗
46. G. Zhou, Y. Li, Y. Ma, Z.Liu, L.Cao, D.Wang, S.Liu, W. Xu, W. Wang, Size-dependent cytotoxicity of yttrium oxide nanoparticles on primary osteoblasts in vitro. J. Nanopart. Res. 18, 135 (2016). https://doi.org/10.1007/s11051-016-3447-510.1007/s11051-016-3447-5 ↗
47. M. Ehlert, A. Radtke, T. Jędrzejewski, K. Roszek, M. Bartmanski, P. Piszczek, In vitro studies on nanoporous, nanotubular and nanosponge-like titania coatings, with the use of adipose-derived stem cells. Materials. 13, 1574 (2020). https://doi.org/10.3390/ma1307157410.3390/ma13071574 ↗
48. E. Murray, D. Provvedini, D. Curran, B. Catherwood, H. Sussman, S. Manolagas, Characterization of a human osteoblastic osteosarcoma cell line (SAOS-2) with high bone alkaline phosphatase activity. J. Bone Miner. Res. 2(3), 231–238 (1987). https://doi.org/10.1002/jbmr.5650020310. (PMID: 2843003)10.1002/jbmr.5650020310 ↗
49. X. Wang, E. Tolba, H.C. Schröder, M. Neufurth, Q. Feng, B. Diehl-Seifert, W. Müller, Effect of bioglass on growth and biomineralization of SaOS-2 cells in hydrogel after 3D cell bioprinting. PLoS ONE 9, e112497 (2014). https://doi.org/10.1371/journal.pone.011249710.1371/journal.pone.0112497 ↗
50. E. Boccardi, A. Philippart, V. Melli, L. Altomare, L. De Nardo, G. Novajra, A.R. Boccaccini, Bioactivity and mechanical stability of 45S5 bioactive glass scaffolds based on natural marine sponges. Ann. Biomed. Eng. 44(6), 1881–1893 (2016). https://doi.org/10.1007/s10439-016-1595-510.1007/s10439-016-1595-5 ↗
51. M. Alcaide, P. Portoles, A. Lopez-Noriega, D. Arcos, M. Vallet-Regi, M.T. Portoles, Interaction of an ordered mesoporous bioactive glass with osteoblasts, fibroblasts and lymphocytes, demonstrating its biocompatibility as a potential bone graft material. Acta Biomater. 6(3), 892–899 (2010). https://doi.org/10.1016/j.actbio.2009.09.00810.1016/j.actbio.2009.09.008 ↗
52. F. Baino, S. Fiorilli, R. Mortera, B. Onida, E. Saino, L. Visai, E. Verne, C. Vitale-Brovarone, Mesoporous bioactive glass as a multifunctional system for bone regeneration and controlled drug release. J. Appl. Biomater. Funct. Mater. 10(1), 12–21 (2012). https://doi.org/10.5301/JABFM.2012.927010.5301/JABFM.2012.9270 ↗
53. S. Wilkesmann, J. Fellenberg, Q. Nawaz, B.Reible, A. Moghaddam, A.R. Boccaccini, F. Westhauser, Primary osteoblasts, osteoblast precursor cells or osteoblast-like cell lines: which human cell types are (most) suitable for characterizing 45S5-bioactive glass? J. Biomed. Mater. Res. 108A, 663–674 (2020). https://doi.org/10.1002/jbm.a.3684610.1002/jbm.a.36846 ↗