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The in vitro and in vivo performance of a strontium-containing coating on the low-modulus Ti35Nb2Ta3Zr alloy formed by micro-arc oxidation

  • Biocompatibility Studies
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Abstract

The β-titanium alloy is thought to be a promising alloy using as orthopedic or dental implants owing to its characteristics, which contains low elastic modulus, high corrosion resistance and well biocompatibility. Our previous study has reported that a new β-titanium alloy Ti35Nb2Ta3Zr showed low modulus close to human bone, equal tissue compatibility to a traditional implant alloy Ti6Al4V. In this study, micro-arc oxidation (MAO) was applied on the Ti35Nb2Ta3Zr alloy to enhance its surface characteristics and biocompatibility and osseointegration ability. Two different coatings were formed, TiO2 doped with calcium–phosphate coating (Ca–P) and calcium–phosphate–strontium coating (Ca–P–Sr). Then we evaluated the effects of the MAO coatings on the Ti35Nb2Ta3Zr alloy through in vitro and in vivo tests. As to the characteristics of the coatings, the morphology, chemical composition, surface roughness and contact angle of MAO coatings were tested by scanning electron microscopy, energy dispersive spectroscopy, atomic force microscopy, and video contact-angle measurement system respectively. Besides, we performed MTT assay, ALP test and cell morphology-adhesion test on materials to evaluate the MAOed coating materials’ biocompatibility in vitro. The in vivo experiment was performed through rabbit model. Alloys were implanted into rabbits’ femur shafts, then we performed micro-CT, histological and sequential fluorescent labeling analysis to evaluate implants’ osseointegration ability in vivo. Finally, the Ca–P specimens and Ca–P–Sr specimens exhibited a significant enhancement in surface roughness, hydrophilicity, cell proliferation, cell adhesion. More new bone was found around the Ca–P–Sr coated alloy than Ca–P coated alloy and Ti35Nb2Ta3Zr alloy. In conclusion, the MAO treatment improved in vitro and in vivo performance of Ti35Nb2Ta3Zr alloy. The Ca–P–Sr coating may be a promising modified surface formed by MAO for the novel β-titanium alloy Ti35Nb2Ta3Zr.

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References

  1. Hao YL, Li SJ, Sun BB, Sui ML, Yang R. Ductile titanium alloy with low Poisson’s ratio. Phys Rev Lett. 2007;98(21):216405.

    Article  Google Scholar 

  2. Wang K. The use of titanium for medical applications in the USA. Mater Sci Eng A. 1996;213(1):134–7.

    Article  Google Scholar 

  3. Snyder SM, Schneider E. Estimation of mechanical properties of cortical bone by computed tomography. J Orthop Res. 1991;9(3):422–31. doi:10.1002/jor.1100090315.

    Article  Google Scholar 

  4. Gefen A. Computational simulations of stress shielding and bone resorption around existing and computer-designed orthopaedic screws. Med Biol Eng Comput. 2002;40(3):311–22.

    Article  Google Scholar 

  5. Rehder D. Vanadium. its role for humans. Metal ions in life sciences. 2013;13:139–69. doi:10.1007/978-94-007-7500-8_5.

    Article  Google Scholar 

  6. Goyer RA, Clarkson TW. Toxic effects of metals. In: Klaassen CD, editors. Casarett & Doull’s toxicology the basic science of poisons, 5th ed. New York: McGraw-Hill Health Professions Division; 1996. ISBN 71054766.

  7. Long M, Rack HJ. Titanium alloys in total joint replacement—a materials science perspective. Biomaterials. 1998;19(18):1621–39.

    Article  Google Scholar 

  8. Guo Y, Chen D, Lu W, Jia Y, Wang L, Zhang X. Corrosion resistance and in vitro response of a novel Ti35Nb2Ta3Zr alloy with a low Young’s modulus. Biomed Mater. 2013;8(5):055004. doi:10.1088/1748-6041/8/5/055004.

    Article  Google Scholar 

  9. Guo Y, Chen D, Cheng M, Lu W, Wang L, Zhang X. The bone tissue compatibility of a new Ti35Nb2Ta3Zr alloy with a low Young’s modulus. Int J Mol Med. 2013;31(3):689–97. doi:10.3892/ijmm.2013.1249.

    Google Scholar 

  10. Hu H, Qiao Y, Meng F, Liu X, Ding C. Enhanced apatite-forming ability and cytocompatibility of porous and nanostructured TiO2/CaSiO3 coating on titanium. Colloids Surf B. 2013;101:83–90. doi:10.1016/j.colsurfb.2012.06.021.

    Article  Google Scholar 

  11. Wang G, Lu Z, Liu X, Zhou X, Ding C, Zreiqat H. Nanostructured glass-ceramic coatings for orthopaedic applications. J R Soc Interface. 2011;8(61):1192–203. doi:10.1098/rsif.2010.0680.

    Article  Google Scholar 

  12. Chen XB, Li YC, Du Plessis J, Hodgson PD, Wen C. Influence of calcium ion deposition on apatite-inducing ability of porous titanium for biomedical applications. Acta Biomater. 2009;5(5):1808–20. doi:10.1016/j.actbio.2009.01.015.

    Article  Google Scholar 

  13. Treves C, Martinesi M, Stio M, Gutierrez A, Jimenez JA, Lopez MF. In vitro biocompatibility evaluation of surface-modified titanium alloys. J Biomed Mater Res A. 2010;92(4):1623–34. doi:10.1002/jbm.a.32507.

    Google Scholar 

  14. Heimann RB, Wirth R. Formation and transformation of amorphous calcium phosphates on titanium alloy surfaces during atmospheric plasma spraying and their subsequent in vitro performance. Biomaterials. 2006;27(6):823–31. doi:10.1016/j.biomaterials.2005.06.029.

    Article  Google Scholar 

  15. Xie Y, Liu X, Huang A, Ding C, Chu PK. Improvement of surface bioactivity on titanium by water and hydrogen plasma immersion ion implantation. Biomaterials. 2005;26(31):6129–35. doi:10.1016/j.biomaterials.2005.03.032.

    Article  Google Scholar 

  16. Wei D, Zhou Y, Jia D, Wang Y. Characteristic and in vitro bioactivity of a microarc-oxidized TiO(2)-based coating after chemical treatment. Acta Biomater. 2007;3(5):817–27. doi:10.1016/j.actbio.2007.03.001.

    Article  Google Scholar 

  17. Boanini E, Gazzano M, Bigi A. Ionic substitutions in calcium phosphates synthesized at low temperature. Acta Biomater. 2010;6(6):1882–94. doi:10.1016/j.actbio.2009.12.041.

    Article  Google Scholar 

  18. Bracci B, Torricelli P, Panzavolta S, Boanini E, Giardino R, Bigi A. Effect of Mg2+, Sr2+, and Mn2+ on the chemico-physical and in vitro biological properties of calcium phosphate biomimetic coatings. J Inorg Biochem. 2009;103(12):1666–74. doi:10.1016/j.jinorgbio.2009.09.009.

    Article  Google Scholar 

  19. Kuo MC, Yen SK. The process of electrochemical deposited hydroxyapatite coatings on biomedical titanium at room temperature. Mater Sci Eng C. 2002;20(1–2):153–60. doi:10.1016/S0928-4931(02)00026-7.

    Article  Google Scholar 

  20. Dahl SG, Allain P, Marie PJ, Mauras Y, Boivin G, Ammann P, Tsouderos Y, Delmas PD, Christiansen C. Incorporation and distribution of strontium in bone. Bone. 2001;28(4):446–53. doi:10.1016/S8756-3282(01)00419-7.

    Article  Google Scholar 

  21. Meunier PJ, Roux C, Ortolani S, Diaz-Curiel M, Compston J, Marquis P, Cormier C, Isaia G, Badurski J, Wark JD, Collette J, Reginster JY. Effects of long-term strontium ranelate treatment on vertebral fracture risk in postmenopausal women with osteoporosis. Osteoporos Int. 2009;20(10):1663–73. doi:10.1007/s00198-008-0825-6.

    Article  Google Scholar 

  22. Bonnelye E, Chabadel A, Saltel F, Jurdic P. Dual effect of strontium ranelate: stimulation of osteoblast differentiation and inhibition of osteoclast formation and resorption in vitro. Bone. 2008;42(1):129–38. doi:10.1016/j.bone.2007.08.043.

    Article  Google Scholar 

  23. Peng S, Liu XS, Huang S, Li Z, Pan H, Zhen W, Luk KD, Guo XE, Lu WW. The cross-talk between osteoclasts and osteoblasts in response to strontium treatment: involvement of osteoprotegerin. Bone. 2011;49(6):1290–8. doi:10.1016/j.bone.2011.08.031.

    Article  Google Scholar 

  24. Zhao L, Wang H, Huo K, Zhang X, Wang W, Zhang Y, Wu Z, Chu PK. The osteogenic activity of strontium loaded titania nanotube arrays on titanium substrates. Biomaterials. 2013;34(1):19–29. doi:10.1016/j.biomaterials.2012.09.041.

    Article  Google Scholar 

  25. Fu DL, Jiang QH, He FM, Yang GL, Liu L. Fluorescence microscopic analysis of bone osseointegration of strontium-substituted hydroxyapatite implants. J Zhejiang Univ Sci B. 2012;13(5):364–71. doi:10.1631/jzus.B1100381.

    Article  Google Scholar 

  26. Li Y, Li Q, Zhu S, Luo E, Li J, Feng G, Liao Y, Hu J. The effect of strontium-substituted hydroxyapatite coating on implant fixation in ovariectomized rats. Biomaterials. 2010;31(34):9006–14. doi:10.1016/j.biomaterials.2010.07.112.

    Article  Google Scholar 

  27. Matsunaga K, Murata H. Strontium substitution in bioactive calcium phosphates: a first-principles study. J Phys Chem B. 2009;113(11):3584–9. doi:10.1021/jp808713m.

    Article  Google Scholar 

  28. Zhang W, Wang G, Liu Y, Zhao X, Zou D, Zhu C, Jin Y, Huang Q, Sun J, Liu X, Jiang X, Zreiqat H. The synergistic effect of hierarchical micro/nano-topography and bioactive ions for enhanced osseointegration. Biomaterials. 2013;34(13):3184–95. doi:10.1016/j.biomaterials.2013.01.008.

    Article  Google Scholar 

  29. dos Santos A, Araujo JR, Landi SM, Kuznetsov A, Granjeiro JM, de Sena LA, Achete CA. A study of the physical, chemical and biological properties of TiO2 coatings produced by micro-arc oxidation in a Ca–P-based electrolyte. J Mater Sci Mater Med. 2014;25(7):1769–80. doi:10.1007/s10856-014-5207-3.

    Article  Google Scholar 

  30. Li LH, Kong YM, Kim HW, Kim YW, Kim HE, Heo SJ, Koak JY. Improved biological performance of Ti implants due to surface modification by micro-arc oxidation. Biomaterials. 2004;25(14):2867–75. doi:10.1016/j.biomaterials.2003.09.048.

    Article  Google Scholar 

  31. Ventre M, Causa F, Netti PA. Determinants of cell-material crosstalk at the interface: towards engineering of cell instructive materials. J R Soc Interface. 2012;9(74):2017–32. doi:10.1098/rsif.2012.0308.

    Article  Google Scholar 

  32. Parsons JT, Horwitz AR, Schwartz MA. Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat Rev Mol Cell Biol. 2010;11(9):633–43. doi:10.1038/nrm2957.

    Article  Google Scholar 

  33. Vogler EA. Water and the acute biological response to surfaces. J Biomater Sci Polym Ed. 1999;10(10):1015–45.

    Article  Google Scholar 

  34. Lincks J, Boyan BD, Blanchard CR, Lohmann CH, Liu Y, Cochran DL, Dean DD, Schwartz Z. Response of MG63 osteoblast-like cells to titanium and titanium alloy is dependent on surface roughness and composition. Biomaterials. 1998;19(23):2219–32.

    Article  Google Scholar 

  35. del Rio A, Perez-Jimenez R, Liu R, Roca-Cusachs P, Fernandez JM, Sheetz MP. Stretching single talin rod molecules activates vinculin binding. Science. 2009;323(5914):638–41. doi:10.1126/science.1162912.

    Article  Google Scholar 

  36. Sethuraman A, Han M, Kane RS, Belfort G. Effect of surface wettability on the adhesion of proteins. Langmuir. 2004;20(18):7779–88. doi:10.1021/la049454q.

    Article  Google Scholar 

  37. Xu LC, Siedlecki CA. Effects of surface wettability and contact time on protein adhesion to biomaterial surfaces. Biomaterials. 2007;28(22):3273–83. doi:10.1016/j.biomaterials.2007.03.032.

    Article  Google Scholar 

  38. Rausch-fan X, Qu Z, Wieland M, Matejka M, Schedle A. Differentiation and cytokine synthesis of human alveolar osteoblasts compared to osteoblast-like cells (MG63) in response to titanium surfaces. Dent Mater. 2008;24(1):102–10. doi:10.1016/j.dental.2007.03.001.

    Article  Google Scholar 

  39. Qu Z, Rausch-Fan X, Wieland M, Matejka M, Schedle A. The initial attachment and subsequent behavior regulation of osteoblasts by dental implant surface modification. J Biomed Mater Res A. 2007;82(3):658–68. doi:10.1002/jbm.a.31023.

    Article  Google Scholar 

  40. Wennerberg A, Albrektsson T. On implant surfaces: a review of current knowledge and opinions. Int J Oral Maxillofac Implant. 2010;25(1):63–74.

    Google Scholar 

  41. Oliveira AL, Reis RL, Li P. Strontium-substituted apatite coating grown on Ti6Al4V substrate through biomimetic synthesis. J Biomed Mater Res B Appl Biomater. 2007;83(1):258–65. doi:10.1002/jbm.b.30791.

    Article  Google Scholar 

  42. Li Y, Li X, Song G, Chen K, Yin G, Hu J. Effects of strontium ranelate on osseointegration of titanium implant in osteoporotic rats. Clin Oral Implant Res. 2012;23(9):1038–44. doi:10.1111/j.1600-0501.2011.02252.x.

    Article  Google Scholar 

  43. Maimoun L, Brennan TC, Badoud I, Dubois-Ferriere V, Rizzoli R, Ammann P. Strontium ranelate improves implant osseointegration. Bone. 2010;46(5):1436–41. doi:10.1016/j.bone.2010.01.379.

    Article  Google Scholar 

  44. Chattopadhyay N, Quinn SJ, Kifor O, Ye C, Brown EM. The calcium-sensing receptor (CaR) is involved in strontium ranelate-induced osteoblast proliferation. Biochem Pharmacol. 2007;74(3):438–47. doi:10.1016/j.bcp.2007.04.020.

    Article  Google Scholar 

  45. Yamaguchi T. The calcium-sensing receptor in bone. J Bone Miner Metab. 2008;26(4):301–11. doi:10.1007/s00774-008-0843-7.

    Article  Google Scholar 

  46. Dvorak MM, Siddiqua A, Ward DT, Carter DH, Dallas SL, Nemeth EF, Riccardi D. Physiological changes in extracellular calcium concentration directly control osteoblast function in the absence of calciotropic hormones. Proc Natl Acad Sci USA. 2004;101(14):5140–5. doi:10.1073/pnas.0306141101.

    Article  Google Scholar 

  47. Coulombe J, Faure H, Robin B, Ruat M. In vitro effects of strontium ranelate on the extracellular calcium-sensing receptor. Biochem Biophys Res Commun. 2004;323(4):1184–90. doi:10.1016/j.bbrc.2004.08.209.

    Article  Google Scholar 

  48. Brennan TC, Rybchyn MS, Green W, Atwa S, Conigrave AD, Mason RS. Osteoblasts play key roles in the mechanisms of action of strontium ranelate. Br J Pharmacol. 2009;157(7):1291–300. doi:10.1111/j.1476-5381.2009.00305.x.

    Article  Google Scholar 

  49. Walsh MC, Kim N, Kadono Y, Rho J, Lee SY, Lorenzo J, Choi Y. Osteoimmunology: interplay between the immune system and bone metabolism. Annu Rev Immunol. 2006;24(1):33–63. doi:10.1146/annurev.immunol.24.021605.090646.

    Article  Google Scholar 

  50. Offermanns V, Andersen OZ, Falkensammer G, Andersen IH, Almtoft KP, Sorensen S, Sillassen M, Jeppesen CS, Rasse M, Foss M, Kloss F. Enhanced osseointegration of endosseous implants by predictable sustained release properties of strontium. J Biomed Mater Res B Appl Biomater. 2014;. doi:10.1002/jbm.b.33279.

    Google Scholar 

  51. Yamaguchi S, Nath S, Matsushita T, Kokubo T. Controlled release of strontium ions from a bioactive Ti metal with a Ca-enriched surface layer. Acta Biomater. 2014;10(5):2282–9. doi:10.1016/j.actbio.2014.01.026.

    Article  Google Scholar 

  52. Saidak Z, Hay E, Marty C, Barbara A, Marie PJ. Strontium ranelate rebalances bone marrow adipogenesis and osteoblastogenesis in senescent osteopenic mice through NFATc/Maf and Wnt signaling. Aging Cell. 2012;11(3):467–74. doi:10.1111/j.1474-9726.2012.00804.x.

    Article  Google Scholar 

  53. Minear S, Leucht P, Jiang J, Liu B, Zeng A, Fuerer C, Nusse R, Helms JA. Wnt proteins promote bone regeneration. Sci Transl Med. 2010;2(29):29ra30. doi:10.1126/scitranslmed.3000231.

    Article  Google Scholar 

  54. Fromigue O, Hay E, Barbara A, Marie PJ. Essential role of nuclear factor of activated T cells (NFAT)-mediated Wnt signaling in osteoblast differentiation induced by strontium ranelate. J Biol Chem. 2010;285(33):25251–8. doi:10.1074/jbc.M110.110502.

    Article  Google Scholar 

  55. Almeida M, Han L, Martin-Millan M, O’Brien CA, Manolagas SC. Oxidative stress antagonizes Wnt signaling in osteoblast precursors by diverting beta-catenin from T cell factor- to forkhead box O-mediated transcription. J Biol Chem. 2007;282(37):27298–305. doi:10.1074/jbc.M702811200.

    Article  Google Scholar 

  56. Yan J, Sun JF, Chu PK, Han Y, Zhang YM. Bone integration capability of a series of strontium-containing hydroxyapatite coatings formed by micro-arc oxidation. J Biomed Mater Res A. 2013;101(9):2465–80. doi:10.1002/jbm.a.34548.

    Article  Google Scholar 

  57. Schrooten I, Behets GJ, Cabrera WE, Vercauteren SR, Lamberts LV, Verberckmoes SC, Bervoets AJ, Dams G, Goodman WG, De Broe ME, D’Haese PC. Dose-dependent effects of strontium on bone of chronic renal failure rats. Kidney Int. 2003;63(3):927–35. doi:10.1046/j.1523-1755.2003.00809.x.

    Article  Google Scholar 

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Acknowledgments

The present study was supported by the National Natural Science Foundation of China (Grant Nos. 81271962 and 81171688), The Science and Technology Commission of Shanghai Municipality, China (Grant No. 12jc1407302).

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    Authors and Affiliations

    1. Department of Orthopedic, Shanghai Jiao Tong University Affiliated Sixth People’s Hospital, 600 Yishan Road, Shanghai, 200233, People’s Republic of China

      Wei Liu, Mengqi Cheng, Tuerhongjiang Wahafu, Yaochao Zhao, Hui Qin, Jiaxing Wang & Xianlong Zhang

    2. State Key Laboratory of Metal Matrix Composites, Shanghai Jiao Tong University, 800 Dongchuan Road, Shanghai, 200244, People’s Republic of China

      Liqiang Wang

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    1. Wei Liu
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    Wei Liu and Mengqi Cheng have contributed equally to this work.

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    Liu, W., Cheng, M., Wahafu, T. et al. The in vitro and in vivo performance of a strontium-containing coating on the low-modulus Ti35Nb2Ta3Zr alloy formed by micro-arc oxidation. J Mater Sci: Mater Med 26, 203 (2015). https://doi.org/10.1007/s10856-015-5533-0

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