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Quantitative assessment of degradation, cytocompatibility, and in vivo bone regeneration of silicon-incorporated magnesium phosphate bioceramics

Published online by Cambridge University Press:  30 December 2019

Vinod Kumar ,
Kaushik Sarkar ,
Karuppasamy Bavya Devi ,
Debaki Ghosh ,
Samit Kumar Nandi  and
Mangal Roy
Vinod Kumar
Affiliation:
Department of Veterinary Surgery & Radiology, West Bengal University of Animal & Fishery Sciences, Kolkata 700037, India
Kaushik Sarkar
Affiliation:
Department of Metallurgical and Materials Engineering, Indian Institute of Technology-Kharagpur, Kharagpur 721302, India
Karuppasamy Bavya Devi
Affiliation:
Department of Metallurgical and Materials Engineering, Indian Institute of Technology-Kharagpur, Kharagpur 721302, India
Debaki Ghosh
Affiliation:
Department of Veterinary Surgery & Radiology, West Bengal University of Animal & Fishery Sciences, Kolkata 700037, India
Samit Kumar Nandi*
Affiliation:
Department of Veterinary Surgery & Radiology, West Bengal University of Animal & Fishery Sciences, Kolkata 700037, India
Mangal Roy*
Affiliation:
Department of Metallurgical and Materials Engineering, Indian Institute of Technology-Kharagpur, Kharagpur 721302, India
*
a)Address all correspondence to these authors. e-mail: [email protected]
b)e-mail: [email protected]
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Abstract

The effects of silicon incorporation on the in vitro and in vivo properties of magnesium phosphate (MgP) bioceramics were studied. Samples were prepared by conventional solid state synthesis method. Scanning electron microscopy and micro-computed tomography (µ-CT) analysis showed that Si doping reduces degradability of MgP. In vitro studies have shown that MG63 cells can attach and proliferate on MgP samples. Live/dead imaging showed that MgP–0.5Si sample had highest cell proliferation, which was also quantitatively confirmed by alamar blue assay. In vivo biocompatibility of MgP ceramics was assessed after implantation in rabbit model. Detailed µ-CT analysis showed new bone tissue formation around the implant after 30 and 90 days. MgP–0.5Si ceramics had 84% bone regeneration compared with 56% for pure MgP ceramics, as confirmed by oxytetracycline labeling. Our finding suggests that Si doping can alter physicochemical properties of MgP ceramics and promotes osseointegration, which can be a useful choice for bone tissue engineering.

Keywords

magnesium phosphatebioceramicdegradationin vitroin vivomicro-CT
Type
Article
Information
Journal of Materials Research , Volume 34 , Issue 24 , 30 December 2019 , pp. 4024 - 4036
Copyright
Copyright © Materials Research Society 2019 

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Footnotes

c)

These authors contributed equally to this work.

References

LeGeros, R.Z.: Calcium phosphate-based osteoinductive materials. Chem. Rev. 108, 4742 (2008).10.1021/cr800427gCrossRefGoogle ScholarPubMed
Hwang, J-W., Park, J-S., Lee, J-S., Jung, U-W., Kim, C-S., Cho, K-S., Lee, Y-K., and Choi, S-H.: Comparative evaluation of three calcium phosphate synthetic block bone graft materials for bone regeneration in rabbit calvaria. J. Biomed. Mater. Res., Part B 100, 2044 (2012).CrossRefGoogle ScholarPubMed
Samavedi, S., Whittington, A.R., and Goldstein, A.S.: Calcium phosphate ceramics in bone tissue engineering: A review of properties and their influence on cell behavior. Acta Biomater. 9, 8037 (2013).CrossRefGoogle ScholarPubMed
LeGeros, R.Z.: Properties of osteoconductive biomaterials: Calcium phosphates. Clin. Orthop. Relat. Res. 395, 81 (2002).CrossRefGoogle Scholar
Detsch, R., Mayr, H., and Ziegler, G.: Formation of osteoclast-like cells on HA and TCP ceramics. Acta Biomater. 4, 139 (2008).CrossRefGoogle ScholarPubMed
Jalota, S., Bhaduri, S.B., and Tas, A.C.: In vitro testing of calcium phosphate (HA, TCP, and biphasic HA-TCP) whiskers. J. Biomed. Mater. Res., Part A 78, 481 (2006).CrossRefGoogle ScholarPubMed
Yuan, H., van Blitterswijk, C.A., de Groot, K., and de Bruijn, J.D.: A comparison of bone formation in biphasic calcium phosphate (BCP) and hydroxyapatite (HA) implanted in muscle and bone of dogs at different time periods. J. Biomed. Mater. Res., Part A 78, 139 (2006).10.1002/jbm.a.30707CrossRefGoogle ScholarPubMed
Ogose, A., Hotta, T., Hatano, H., Kawashima, H., Tokunaga, K., Endo, N., and Umezu, H.: Histological examination of beta-tricalcium phosphate graft in human femur. J. Biomed. Mater. Res. 63, 601 (2002).CrossRefGoogle ScholarPubMed
Chazono, M., Tanaka, T., Komaki, H., and Fujii, K.: Bone formation and bioresorption after implantation of injectable β-tricalcium phosphate granules–hyaluronate complex in rabbit bone defects. J. Biomed. Mater. Res., Part A 70, 542 (2004).CrossRefGoogle ScholarPubMed
Penel, G., Leroy, N., Van Landuyt, P., Flautre, B., Hardouin, P., Lemaître, J., and Leroy, G.: Raman microspectrometry studies of brushite cement: In vivo evolution in a sheep model. Bone 25, 81S (1999).10.1016/S8756-3282(99)00139-8CrossRefGoogle Scholar
Bohner, M., Theiss, F., Apelt, D., Hirsiger, W., Houriet, R., Rizzoli, G., Gnos, E., Frei, C., Auer, J.A., and von Rechenberg, B.: Compositional changes of a dicalcium phosphate dihydrate cement after implantation in sheep. Biomaterials 24, 3463 (2003).10.1016/S0142-9612(03)00234-5CrossRefGoogle Scholar
Kanter, B., Geffers, M., Ignatius, A., and Gbureck, U.: Control of in vivo mineral bone cement degradation. Acta Biomater. 10, 3279 (2014).CrossRefGoogle ScholarPubMed
Klammert, U., Ignatius, A., Wolfram, U., Reuther, T., and Gbureck, U.: In vivo degradation of low temperature calcium and magnesium phosphate ceramics in a heterotopic model. Acta Biomater. 7, 3469 (2011).CrossRefGoogle Scholar
Tamimi, F., Nihouannen, D.L., Bassett, D.C., Ibasco, S., Gbureck, U., Knowles, J., Wright, A., Flynn, A., Komarova, S.V., and Barralet, J.E.: Biocompatibility of magnesium phosphate minerals and their stability under physiological conditions. Acta Biomater. 7, 2678 (2011).CrossRefGoogle ScholarPubMed
Salimi, M.H., Heughebaert, J.C., and Nancollas, G.H.: Crystal growth of calcium phosphates in the presence of magnesium ions. Langmuir 1, 119 (1985).CrossRefGoogle Scholar
Castiglioni, S., Cazzaniga, A., Albisetti, W., and Maier, J.A.M.: Magnesium and osteoporosis: Current state of knowledge and future research directions. Nutrients 5, 3022 (2013).10.3390/nu5083022CrossRefGoogle ScholarPubMed
Rude, R.K., Gruber, H.E., Wei, L.Y., Frausto, A., and Mills, B.G.: Magnesium deficiency: Effect on bone and mineral metabolism in the mouse. Calcif. Tissue Int. 72, 32 (2003).10.1007/s00223-001-1091-1CrossRefGoogle Scholar
Zreiqat, H., Howlett, C.R., Zannettino, A., Evans, P., Schulze-Tanzil, G., Knabe, C., and Shakibaei, M.: Mechanisms of magnesium-stimulated adhesion of osteoblastic cells to commonly used orthopaedic implants. J. Biomed. Mater. Res. 62, 175 (2002).CrossRefGoogle ScholarPubMed
Cabrejos-Azama, J., Alkhraisat, M.H., Rueda, C., Torres, J., Blanco, L., and López-Cabarcos, E.: Magnesium substitution in brushite cements for enhanced bone tissue regeneration. Mater. Sci. Eng., C 43, 403 (2014).10.1016/j.msec.2014.06.036CrossRefGoogle ScholarPubMed
Cheng, M., Wahafu, T., Jiang, G., Liu, W., Qiao, Y., Peng, X., Cheng, T., Zhang, X., He, G., and Liu, X.: A novel open-porous magnesium scaffold with controllable microstructures and properties for bone regeneration. Sci. Rep. 6, 24134 (2016).CrossRefGoogle ScholarPubMed
Díaz-Tocados, J.M., Herencia, C., Martínez-Moreno, J.M., de Oca, A.M., Rodríguez-Ortiz, M.E., Vergara, N., Blanco, A., Steppan, S., Almadén, Y., Rodríguez, M., and Muñoz-Castañeda, J.R.: Magnesium chloride promotes osteogenesis through notch signaling activation and expansion of mesenchymal stem cells. Sci. Rep. 7, 7839 (2017).10.1038/s41598-017-08379-yCrossRefGoogle ScholarPubMed
Xue, W., Dahlquist, K., Banerjee, A., Bandyopadhyay, A., and Bose, S.: Synthesis and characterization of tricalcium phosphate with Zn and Mg based dopants. J. Mater. Sci.: Mater. Med. 19, 2669 (2008).Google ScholarPubMed
Wu, L., Luthringer, B.J.C., Feyerabend, F., Schilling, A.F., and Willumeit, R.: Effects of extracellular magnesium on the differentiation and function of human osteoclasts. Acta Biomater. 10, 2843 (2014).CrossRefGoogle ScholarPubMed
Carlisle, E.M.: Silicon as a trace nutrient. Sci. Total Environ. 73, 95 (1988).CrossRefGoogle ScholarPubMed
Carlisle, E.M.: Silicon: A possible factor in bone calcification. Science 167, 279 (1970).CrossRefGoogle ScholarPubMed
Carlisle, E.M.: Silicon: An essential element for the chick. Science 178, 619 (1972).CrossRefGoogle ScholarPubMed
Seaborn, C.D. and Nielsen, F.H.: Silicon deprivation decreases collagen formation in wounds and bone, and ornithine transaminase enzyme activity in liver. Biol. Trace Elem. Res. 89, 251 (2002).10.1385/BTER:89:3:251CrossRefGoogle ScholarPubMed
Reffitt, D.M., Ogston, N., Jugdaohsingh, R., Cheung, H.F.J., Evans, B.A.J., Thompson, R.P.H., Powell, J.J., and Hampson, G.N.: Orthosilicic acid stimulates collagen type 1 synthesis and osteoblastic differentiation in human osteoblast-like cells in vitro. Bone 32, 127 (2003).CrossRefGoogle ScholarPubMed
Kim, E-J., Bu, S-Y., Sung, M-K., and Choi, M-K.: Effects of silicon on osteoblast activity and bone mineralization of MC3T3-E1 cells. Biol. Trace Elem. Res. 152, 105 (2013).CrossRefGoogle ScholarPubMed
Arumugam, M.Q., Ireland, D.C., Brooks, R.A., Rushton, N., and Bonfield, W.: Orthosilicic acid increases collagen type I mRNA expression in human bone-derived osteoblasts in vitro. Key Eng. Mater. 254, 869 (2003).CrossRefGoogle Scholar
Schröder, H.C., Wang, X.H., Wiens, M., Diehl-Seifert, B., Kropf, K., Schloßmacher, U., and Müller, W.E.G.: 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, 3197 (2012).CrossRefGoogle ScholarPubMed
Hing, K.A., Revell, P.A., Smith, N., and Buckland, T.: Effect of silicon level on rate, quality and progression of bone healing within silicate-substituted porous hydroxyapatite scaffolds. Biomaterials 27, 5014 (2006).CrossRefGoogle ScholarPubMed
Mate-Sanchez De Val, J.E., Calvo-Guirado, J.L., Delgado-Ruiz, R.A., Ramirez-Fernandez, M.P., Martinez, I.M., Granero-Marin, J.M., Negri, B., Chiva-Garcia, F., Martinez-Gonzalez, J.M., and De Aza, P.N.: New block graft of α-TCP with silicon in critical size defects in rabbits: Chemical characterization, histological, histomorphometric and micro-CT study. Ceram. Int. 38, 1563 (2012).10.1016/j.ceramint.2011.09.042CrossRefGoogle Scholar
De Val Maté-Sánchez, J.E., Calvo-Guirado, J.L., Delgado-Ruiz, R.A., Ramírez-Fernández, M.P., Negri, B., Abboud, M., Martínez, I.M., and De Aza, P.N.: Physical properties, mechanical behavior, and electron microscopy study of a new α-TCP block graft with silicon in an animal model. J. Biomed. Mater. Res., Part A 100, 3446 (2012).10.1002/jbm.a.34259CrossRefGoogle Scholar
Velasquez, P., Luklinska, Z.B., Meseguer-Olmo, L., Mate-Sanchez De Val, J.E., Delgado-Ruiz, R.A., Calvo-Guirado, J.L., Ramirez-Fernandez, M.P., and De Aza, P.N.: αtCP ceramic doped with dicalcium silicate for bone regeneration applications prepared by powder metallurgy method: In vitro and in vivo studies. J. Biomed. Mater. Res., Part A 101, 1943 (2013).10.1002/jbm.a.34495CrossRefGoogle ScholarPubMed
Shie, M-Y., Ding, S-J., and Chang, H-C.: The role of silicon in osteoblast-like cell proliferation and apoptosis. Acta Biomater. 7, 2604 (2011).CrossRefGoogle ScholarPubMed
Zou, S., Ireland, D., Brooks, R.A., Rushton, N., and Best, S.: The effects of silicate ions on human osteoblast adhesion, proliferation, and differentiation. J. Biomed. Mater. Res., Part B 90, 123 (2009).Google ScholarPubMed
Han, P., Wu, C., and Xiao, Y.: The effect of silicate ions on proliferation, osteogenic differentiation and cell signalling pathways (WNT and SHH) of bone marrow stromal cells. Biomater. Sci. 1, 379 (2013).CrossRefGoogle Scholar
Gough, J.E., Jones, J.R., and Hench, L.L.: Nodule formation and mineralisation of human primary osteoblasts cultured on a porous bioactive glass scaffold. Biomaterials 25, 2039 (2004).CrossRefGoogle ScholarPubMed
Wu, L., Feyerabend, F., Schilling, A.F., Willumeit-Römer, R., and Luthringer, B.J.C.: Effects of extracellular magnesium extract on the proliferation and differentiation of human osteoblasts and osteoclasts in coculture. Acta Biomater. 27, 294 (2015).CrossRefGoogle ScholarPubMed
Maguire, M.E. and Cowan, J.A.: Magnesium chemistry and biochemistry. BioMetals 15, 203 (2002).CrossRefGoogle ScholarPubMed
Mao, L., Xia, L., Chang, J., Liu, J., Jiang, L., Wu, C., and Fang, B.: The synergistic effects of Sr and Si bioactive ions on osteogenesis, osteoclastogenesis and angiogenesis for osteoporotic bone regeneration. Acta Biomater. 61, 217 (2017).CrossRefGoogle ScholarPubMed
Sarkar, K., Kumar, V., Devi, K.B., Ghosh, D., Nandi, S.K., and Roy, M.: Effects of Sr doping on biodegradation and bone regeneration of magnesium phosphate bioceramics. Materialia 5, 100211 (2019).10.1016/j.mtla.2019.100211CrossRefGoogle Scholar
Kokubo, T. and Takadama, H.: How useful is SBF in predicting in vivo bone bioactivity? Biomaterials 27, 2907 (2006).CrossRefGoogle ScholarPubMed
Devi, K.B., Tripathy, B., Kumta, P.N., Nandi, S.K., and Roy, M.: In vivo biocompatibility of zinc-doped magnesium silicate bio-ceramics. ACS Biomater. Sci. Eng. 4, 2126 (2018).CrossRefGoogle Scholar
Devi, K.B., Tripathy, B., Roy, A., Lee, B., Kumta, P.N., Nandi, S.K., and Roy, M.: In vitro biodegradation and in vivo biocompatibility of forsterite bio-ceramics: Effects of strontium substitution. ACS Biomater. Sci. Eng. 5, 530 (2019).CrossRefGoogle Scholar
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