Journal of Materials Science

, Volume 52, Issue 15, pp 8793–8811 | Cite as

Effects of boron oxide substitution on the structure and bioactivity of SrO-containing bioactive glasses

  • Xiaonan Lu
  • Lu Deng
  • Po-Hsuen Kuo
  • Mengguo Ren
  • Ian Buterbaugh
  • Jincheng DuEmail author
In Honor of Larry Hench


B2O3/SiO2 substitution in 55S4.3 bioactive glasses with 5 mol% of SrO has been synthesized and characterized to understand their structure and bioactivity as a function of composition by combining experimental and computer simulation techniques. Raman spectrometry, X-ray diffraction (XRD) and Fourier transform infrared spectrometry (FTIR) were utilized to characterize the structural changes induced by boron content and to identify the formation of hydroxyapatite (HAp). In vitro bioactivity tests were performed in simulated body fluid with a fixed glass mass to solution volume ratio and a particle size range. Needle-like HAp was found to form on the surface of the 55S4.3 with SrO sample from scanning electron microscopy and confirmed from XRD and FTIR. In addition to the experimental efforts, these glasses were also simulated using classical molecular dynamics simulations with partial charge potentials and recently developed parameters for boron oxide to understand their short- and medium-range structures. The glasses from simulations were analyzed in terms of the local structure around the glass network formers, especially the boron coordination number, and found to agree well with theoretical models. The medium-range structural information such as Q n distribution and network connectivity was also obtained and used to understand the compositional dependence of property and bioactivity. The results show that additional boron oxide increased the network connectivity of the 55S4.3 glass and inhibited or delayed the formation of HAp in vitro.


Simulated Body Fluid Bioactive Glass Glass Powder Borate Glass Boron Oxide 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We gratefully acknowledge support by National Science Foundation (NSF) (project # 1508001). ESEM, XRD, Raman and FTIR experiments were conducted at the Center for Advanced Research and Technology (CART) at University of North Texas (UNT). Computer simulations were performed on UNT Talon 2 high-performance computer (HPC) cluster. We would also like to acknowledge Dr. Narendra Dahotre and Dr. Yee Hsien Ho for the helpful discussions. Lastly, we want to thank our anonymous reviewers for both insightful comments and suggestions.


  1. 1.
    Hench LL (2006) The story of Bioglass. J Mater Sci Mater Med 17:967–978CrossRefGoogle Scholar
  2. 2.
    Hench LL, Splinter RJ, Allen WC, Greenlee TK (1971) Bonding mechanisms at the interface of ceramic prosthetic materials. J Biomed Mater Res 5:117–141CrossRefGoogle Scholar
  3. 3.
    Ogino M, Ohuchi F, Hench LL (1980) Compositional dependence of the formation of calcium phosphate films on bioglass. J Biomed Mater Res 14:55–64CrossRefGoogle Scholar
  4. 4.
    Brink M (1997) The influence of alkali and alkaline earths on the working range for bioactive glasses. J Biomed Mater Res 36:109–117CrossRefGoogle Scholar
  5. 5.
    Raju KS, Alessandri G, Ziche M, Gullino PM (1982) Ceruloplasmin, copper ions, and angiogenesis. J Natl Cancer Inst 69:1183–1188Google Scholar
  6. 6.
    Rahaman MN, Day DE, Sonny Bal B, Fu Q, Jung SB, Bonewald LF, Tomsia AP (2011) Bioactive glass in tissue engineering. Acta Biomater 7:2355–2373CrossRefGoogle Scholar
  7. 7.
    Jones JR (2015) Reprint of: review of bioactive glass: from Hench to hybrids. Acta Biomater 23:S53–S82CrossRefGoogle Scholar
  8. 8.
    Bonnelye E, Chabadel A, Saltel F, Jurdic P (2008) Dual effect of strontium ranelate: stimulation of osteoblast differentiation and inhibition of osteoclast formation and resorption in vitro. Bone 42:129–138CrossRefGoogle Scholar
  9. 9.
    Marie PJ, Hott M, Modrowski D, De Pollak C, Guillemain J, Deloffre P, Tsouderos Y (1993) An uncoupling agent containing strontium prevents bone loss by depressing bone resorption and maintaining bone formation in estrogen-deficient rats. J Bone Miner Res 8:607–615CrossRefGoogle Scholar
  10. 10.
    Canalis E, Hott M, Deloffre P, Tsouderos Y, Marie PJ (1996) The divalent strontium salt S12911 enhances bone cell replication and bone formation in vitro. Bone 18:517–523CrossRefGoogle Scholar
  11. 11.
    Buehler J, Chappuis P, Saffar JL, Tsouderos Y, Vignery A (2001) Strontium ranelate inhibits bone resorption while maintaining bone formation in alveolar bone in monkeys (Macaca fascicularis). Bone 29:176–179CrossRefGoogle Scholar
  12. 12.
    Abdelghany AM, Ouis MA, Azooz MA, ElBatal HA, El-Bassyouni GT (2016) Role of SrO on the bioactivity behavior of some ternary borate glasses and their glass ceramic derivatives. Spectrochim Acta Part A Mol Biomol Spectrosc 152:126–133CrossRefGoogle Scholar
  13. 13.
    Fredholm YC, Karpukhina N, Brauer DS, Jones JR, Law RV, Hill RG (2011) Influence of strontium for calcium substitution in bioactive glasses on degradation, ion release and apatite formation. J R Soc Interface 9:880–889CrossRefGoogle Scholar
  14. 14.
    Massera J, Hupa L (2014) Influence of SrO substitution for CaO on the properties of bioactive glass S53P4. J Mater Sci Mater Med 25:657–668CrossRefGoogle Scholar
  15. 15.
    Massera J, Kokkari A, Närhi T, Hupa L (2015) The influence of SrO and CaO in silicate and phosphate bioactive glasses on human gingival fibroblasts. J Mater Sci Mater Med 26:196CrossRefGoogle Scholar
  16. 16.
    Lotfibakhshaiesh N, Brauer DS, Hill RG (2010) Bioactive glass engineered coatings for Ti6Al4V alloys: influence of strontium substitution for calcium on sintering behaviour. J Non Cryst Solids 356:2583–2590CrossRefGoogle Scholar
  17. 17.
    Morohashi T, Sano T, Yamada S (1994) Effects of strontium on calcium metabolism in rats I. A distinction between the pharmacological and toxic doses. Jpn J Pharmacol 64:155–162CrossRefGoogle Scholar
  18. 18.
    Grynpas MD, Marie PJ (1990) Effects of low doses of strontium on bone quality and quantity in rats. Bone 11:313–319CrossRefGoogle Scholar
  19. 19.
    Qiu K, Zhao XJ, Wan CX, Zhao CS, Chen YW (2006) Effect of strontium ions on the growth of ROS17/2.8 cells on porous calcium polyphosphate scaffolds. Biomaterials 27:1277–1286CrossRefGoogle Scholar
  20. 20.
    Tian M, Chen F, Song W, Song Y, Chen Y, Wan C, Yu X, Zhang X (2009) In vivo study of porous strontium-doped calcium polyphosphate scaffolds for bone substitute applications. J Mater Sci Mater Med 20:1505–1512CrossRefGoogle Scholar
  21. 21.
    Hesaraki S, Gholami M, Vazehrad S, Shahrabi S (2010) The effect of Sr concentration on bioactivity and biocompatibility of sol–gel derived glasses based on CaO–SrO–SiO2–P2O5 quaternary system. Mater Sci Eng, C 30:383–390CrossRefGoogle Scholar
  22. 22.
    Fu Q, Rahaman MN, Bal BS, Bonewald LF, Kuroki K, Brown RF (2010) Silicate, borosilicate, and borate bioactive glass scaffolds with controllable degradation rate for bone tissue engineering applications. II. In vitro and in vivo biological evaluation. J Biomed Mater Res Part A 95A:172–1799CrossRefGoogle Scholar
  23. 23.
    Peddi L, Brow RK, Brown RF (2008) Bioactive borate glass coatings for titanium alloys. J Mater Sci Mater Med 19:3145–3152CrossRefGoogle Scholar
  24. 24.
    RK Brow, SK Saha, JI Goldstein (1993) Interfacial reactions between titanium and borate glass. In: MRS online proceedings library archive, vol 314. p 77 (5 pages)Google Scholar
  25. 25.
    Xie K, Zhang L, Yang X, Wang X, Yang G, Zhang L, Shao H, He Y, Fu J, Gou Z (2015) Preparation and characterization of low temperature heat-treated 45S5 bioactive glass-ceramic analogues. Biomed Glasses 1:80–92CrossRefGoogle Scholar
  26. 26.
    Rodriguez O, Curran DJ, Papini M, Placek LM, Wren AW, Schemitsch EH, Zalzal P, Towler MR (2016) Characterization of silica-based and borate-based, titanium-containing bioactive glasses for coating metallic implants. J Non Cryst Solids 433:95–102CrossRefGoogle Scholar
  27. 27.
    Huang W, Day DE, Kittiratanapiboon K, Rahaman MN (2006) Kinetics and mechanisms of the conversion of silicate (45S5), borate, and borosilicate glasses to hydroxyapatite in dilute phosphate solutions. J Mater Sci Mater Med 17:583–596CrossRefGoogle Scholar
  28. 28.
    Fu Q, Rahaman MN, Fu H, Liu X (2010) Silicate, borosilicate, and borate bioactive glass scaffolds with controllable degradation rate for bone tissue engineering applications. I. Preparation and in vitro degradation. J Biomed Mater Res, Part A 95A:164–171CrossRefGoogle Scholar
  29. 29.
    Yao A, Wang D, Huang W, Fu Q, Rahaman MN, Day DE (2007) In vitro bioactive characteristics of borate-based glasses with controllable degradation behavior. J Am Ceram Soc 90:303–306CrossRefGoogle Scholar
  30. 30.
    Liang W, Rahaman MN, Day DE, Marion NW, Riley GC, Mao JJ (2008) Bioactive borate glass scaffold for bone tissue engineering. J Non Cryst Solids 354:1690–1696CrossRefGoogle Scholar
  31. 31.
    Ebisawa Y, Kokubo T, Ohura K, Yamamuro T (1990) Bioactivity of CaO·SiO2-based glasses:in vitro evaluation. J Mater Sci Mater Med 1:239–244CrossRefGoogle Scholar
  32. 32.
    Manupriya, Thind KS, Sharma G, Singh K, Rajendran V, Aravindan S (2007) Soluble borate glasses. In vitro analysis. J Am Ceram Soc 90:467–471CrossRefGoogle Scholar
  33. 33.
    Hill R (1996) An alternative view of the degradation of bioglass. J Mater Sci Lett 15:1122–1125CrossRefGoogle Scholar
  34. 34.
    Lopes PP, Ferreira BJML, Gomes PS, Correia RN, Fernandes MH, Fernandes MHV (2011) Silicate and borate glasses as composite fillers: a bioactivity and biocompatibility study. J Mater Sci Mater Med 22:1501–1510CrossRefGoogle Scholar
  35. 35.
    Marquardt LM, Day D, Sakiyama-Elbert SE, Harkins AB (2014) Effects of borate-based bioactive glass on neuron viability and neurite extension. J Biomed Mater Res Part A 102:2767–2775CrossRefGoogle Scholar
  36. 36.
    Modglin VC, Brown RF, Jung SB, Day DE (2013) Cytotoxicity assessment of modified bioactive glasses with MLO-A5 osteogenic cells in vitro. J Mater Sci Mater Med 24:1191–1199CrossRefGoogle Scholar
  37. 37.
    J Du (2015) Challenges in molecular dynamics simulations of multicomponent oxide glasses. In: Molecular dynamics simulations of disordered materials: from network glasses to phase-change memory alloys. Springer series in material science, vol 215. Springer, pp 157–177Google Scholar
  38. 38.
    Xiang Y, Du J (2011) Effect of strontium substitution on the structure of 45S5 bioglasses. Chem Mater 23:2703–2717CrossRefGoogle Scholar
  39. 39.
    Du J, Xiang Y (2016) Investigating the structure–diffusion–bioactivity relationship of strontium containing bioactive glasses using molecular dynamics based computer simulations. J Non-Cryst Solids 432:35–40CrossRefGoogle Scholar
  40. 40.
    Du J, Xiang Y (2012) Effect of strontium substitution on the structure, ionic diffusion and dynamic properties of 45S5 bioactive glasses. J Non Cryst Solids 358:1059–1071CrossRefGoogle Scholar
  41. 41.
    Xiang Y, Du J, Skinner LB, Benmore CJ, Wren AW, Boyd DJ, Towler MR (2013) Structure and diffusion of ZnO–SrO–CaO–Na2O–SiO2 bioactive glasses: a combined high energy X-ray diffraction and molecular dynamics simulations study. RSC Adv 3:5966–5978CrossRefGoogle Scholar
  42. 42.
    Bonhomme C, Gervais C, Folliet N, Pourpoint F, Coelho Diogo C, Lao J, Jallot E, Lacroix J, Nedelec J, Iuga D, Hanna JV, Smith ME, Xiang Y, Du J, Laurencin D (2012) 87Sr solid-state NMR as a structurally sensitive tool for the investigation of materials: antiosteoporotic pharmaceuticals and bioactive glasses. J Am Chem Soc 134:12611–12628CrossRefGoogle Scholar
  43. 43.
    Tilocca A, Cormack AN (2009) Modeling the water–bioglass interface by ab initio molecular dynamics simulations. ACS Appl Mater Interfaces 1:1324–1333CrossRefGoogle Scholar
  44. 44.
    Deng L, Du J (2016) Development of effective empirical potentials for molecular dynamics simulations of the structures and properties and boroaluminosilicate glasses. J Non Cryst Solids 453:177–194CrossRefGoogle Scholar
  45. 45.
    Macon AL, Kim TB, Valliant EM, Goetschius K, Brow RK, Day DE, Hoppe A, Boccaccini AR, Kim IY, Ohtsuki C, Kokubo T, Osaka A, Vallet-Regi M, Arcos D, Fraile L, Salinas AJ, Teixeira AV, Vueva Y, Almeida RM, Miola M, Vitale-Brovarone C, Verne E, Holand W, Jones JR (2015) A unified in vitro evaluation for apatite-forming ability of bioactive glasses and their variants. J Mater Sci Mater Med 26:115CrossRefGoogle Scholar
  46. 46.
    Kokubo T, Takadama H (2006) How useful is SBF in predicting in vivo bone bioactivity? Biomaterials 27:2907–2915CrossRefGoogle Scholar
  47. 47.
    Todorov IT, Smith W, Trachenko K, Dove MT (2006) DL_POLY_3: new dimensions in molecular dynamics simulations via massive parallelism. J Mater Chem 16:1911–1918CrossRefGoogle Scholar
  48. 48.
    L Deng, J Du, unpublished dataGoogle Scholar
  49. 49.
    Dell WJ, Bray PJ, Xiao SZ (1983) 11B NMR studies and structural modeling of Na2O–B2O3–SiO2 glasses of high soda content. J Non Cryst Solids 58:1–16CrossRefGoogle Scholar
  50. 50.
    Yun YH, Bray PJ (1978) Nuclear magnetic resonance studies of the glasses in the system Na2O–B2O3–SiO2. J Non Cryst Solids 27:363–380CrossRefGoogle Scholar
  51. 51.
    Du L, Stebbins JF (2005) Network connectivity in aluminoborosilicate glasses: a high-resolution 11B, 27Al and 17O NMR study. J Non Cryst Solids 351:3508–3520CrossRefGoogle Scholar
  52. 52.
    Fredholm YC, Karpukhina N, Law RV, Hill RG (2010) Strontium containing bioactive glasses: glass structure and physical properties. J Non Cryst Solids 356:2546–2551CrossRefGoogle Scholar
  53. 53.
    Tilocca A (2008) Short-and medium-range structure of multicomponent bioactive glasses and melts: an assessment of the performances of shell-model and rigid-ion potentials. J Chem Phys 129:084504CrossRefGoogle Scholar
  54. 54.
    Aguiar H, Solla EL, Serra J, González P, León B, Malz F, Jäger C (2008) Raman and NMR study of bioactive Na2O–MgO–CaO–P2O5–SiO2 glasses. J Non Cryst Solids 354:5004–5008CrossRefGoogle Scholar
  55. 55.
    Lin C, Chen S, Leung KS, Shen P (2012) Effects of CaO/P2O5 ratio on the structure and elastic properties of SiO2–CaO–Na2O–P2O5 bioglasses. J Mater Sci Mater Med 23:245–258CrossRefGoogle Scholar
  56. 56.
    Agathopoulos S, Tulyaganov DU, Ventura JMG, Kannan S, Karakassides MA, Ferreira JMF (2006) Formation of hydroxyapatite onto glasses of the CaO–MgO–SiO2 system with B2O3, Na2O, CaF2 and P2O5 additives. Biomaterials 27:1832–1840CrossRefGoogle Scholar
  57. 57.
    Zhang XH, Yue YL, Wu HT (2013) Effects of cation field strength on structure and properties of boroaluminosilicate glasses. Mater Res Innovations 17:212–217CrossRefGoogle Scholar
  58. 58.
    Serra J, González P, Liste S, Serra C, Chiussi S, León B, Pérez-Amor M, Ylänen HO, Hupa M (2003) FTIR and XPS studies of bioactive silica based glasses. J Non Cryst Solids 332:20–27CrossRefGoogle Scholar
  59. 59.
    Aguiar H, Serra J, González P, León B (2009) Structural study of sol–gel silicate glasses by IR and Raman spectroscopies. J Non Cryst Solids 355:475–480CrossRefGoogle Scholar
  60. 60.
    Peitl Filho O, Latorre GP, Hench L (1996) Effect of crystallization on apatite-layer formation of bioactive glass 45%. J Biomed Mater Res 30:509–514CrossRefGoogle Scholar
  61. 61.
    Hench LL, Wilson J (1993) An introduction to bioceramics. World Scientific Publishing Co., Singapore, p 386CrossRefGoogle Scholar
  62. 62.
    Zadpoor AA (2014) Relationship between in vitro apatite-forming ability measured using simulated body fluid and in vivo bioactivity of biomaterials. Mater Sci Eng C 35:134–143CrossRefGoogle Scholar
  63. 63.
    Varila L, Fagerlund S, Lehtonen T, Tuominen J, Hupa L (2012) Surface reactions of bioactive glasses in buffered solutions. J Eur Ceram Soc 32:2757–2763CrossRefGoogle Scholar
  64. 64.
    Jones JR, Sepulveda P, Hench LL (2001) Dose-dependent behavior of bioactive glass dissolution. J Biomed Mater Res 58:720–726CrossRefGoogle Scholar
  65. 65.
    McGrail BP, Ebert WL, Bakel AJ, Peeler DK (1997) Measurement of kinetic rate law parameters on a Na–Ca–Al borosilicate glass for low-activity waste. J Nucl Mater 249:175–189CrossRefGoogle Scholar
  66. 66.
    Lebecq I, Désanglois F, Leriche A, Follet-Houttemane C (2007) Compositional dependence on the in vitro bioactivity of invert or conventional bioglasses in the Si–Ca–Na–P system. J Biomed Mater Res, Part A 83A:156–168CrossRefGoogle Scholar
  67. 67.
    Brink M, Turunen T, Happonen R, Yli-Urpo A (1997) Compositional dependence of bioactivity of glasses in the system Na2O–K2O–MgO–CaO–B2O3–P2O5–SiO2. J Biomed Mater Res 37:114–121CrossRefGoogle Scholar
  68. 68.
    Manupriya, Thind KS, Singh K, Kumar V, Sharma G, Singh DP, Singh D (2009) Compositional dependence of in vitro bioactivity in sodium calcium borate glasses. J Phys Chem Solids 70:1137–1141CrossRefGoogle Scholar
  69. 69.
    Saranti A, Koutselas I, Karakassides MA (2006) Bioactive glasses in the system CaO–B2O3–P2O5: preparation, structural study and in vitro evaluation. J Non Cryst Solids 352:390–398CrossRefGoogle Scholar
  70. 70.
    Brauer DS, Karpukhina N, O’Donnell MD, Law RV, Hill RG (2010) Fluoride-containing bioactive glasses: effect of glass design and structure on degradation, pH and apatite formation in simulated body fluid. Acta Biomater 6:3275–3282CrossRefGoogle Scholar
  71. 71.
    Cai S, Xu GH, Yu XZ, Zhang WJ, Xiao ZY, Yao KD (2009) Fabrication and biological characteristics of beta-tricalcium phosphate porous ceramic scaffolds reinforced with calcium phosphate glass. J Mater Sci Mater Med 20:351–358CrossRefGoogle Scholar
  72. 72.
    Brauer DS (2015) Bioactive glasses—structure and properties. Angew Chem Int Ed 54:4160–4181CrossRefGoogle Scholar
  73. 73.
    Edén M (2011) The split network analysis for exploring composition–structure correlations in multi-component glasses: I. Rationalizing bioactivity-composition trends of bioglasses. J Non Cryst Solids 357:1595–1602CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Xiaonan Lu
    • 1
  • Lu Deng
    • 1
  • Po-Hsuen Kuo
    • 1
  • Mengguo Ren
    • 1
  • Ian Buterbaugh
    • 1
  • Jincheng Du
    • 1
    Email author
  1. 1.Department of Materials Science and EngineeringUniversity of North TexasDentonUSA

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