Skip to main content
SpringerLink
Log in

Osteogenic potential of sol–gel bioactive glasses containing manganese

  • Biocompatibility Studies
  • Original Research
  • Published:
Journal of Materials Science: Materials in Medicine Aims and scope Submit manuscript

Abstract

Bioactive glasses (BGs) are widely used for bone regeneration, and allow the incorporation of different ions with therapeutic properties into the glass network. Amongst the different ions with therapeutic benefits, manganese (Mn) has been shown to influence bone metabolism and activate human osteoblasts integrins, improving cell adhesion, proliferation and spreading. Mn has also been incorporated into bioceramics as a therapeutic ion for improved osteogenesis. Here, up to 4.4 mol% MnO was substituted for CaO in the 58S composition (60 mol% SiO2, 36 mol% CaO, 4 mol% P2O5) and its effects on the glass properties and capability to influence the osteogenic differentiation were evaluated. Mn-containing BGs with amorphous structure, high specific surface area and nanoporosity were obtained. The presence of Mn2+ species was confirmed by X-ray photoelectron spectroscopy (XPS). Mn-containing BGs presented no cytotoxic effect on human mesenchymal stem cells (hMSCs) and enabled sustained ion release in culture medium. hMSCs osteogenic differentiation stimulation and influence on the mineralisation process was also confirmed through the alkaline phosphatase (ALP) activity, and expression of osteogenic differentiation markers, such as collagen type I, osteopontin and osteocalcin, which presented higher expression in the presence of Mn-containing samples compared to control. Results show that the release of manganese ions from bioactive glass provoked human mesenchymal stem cell (hMSC) differentiation down a bone pathway, whereas hMSCs exposed to the Mn-free glass did not differentiate. Mn incorporation offers great promise for obtaining glasses with superior properties for bone tissue regeneration.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  1. Hench LL, Splinter RJ, Allen WC, Greenlee TK. Bonding mechanisms at the interface of ceramic prosthetic materials. J Biomed Mater Res. 1971;5:117–41. https://doi.org/10.1002/jbm.820050611.

    Article  Google Scholar 

  2. Baino F. Bioactive glasses—when glass science and technology meet regenerative medicine. Ceram Int. 2018;44:14953–66. https://doi.org/10.1016/j.ceramint.2018.05.180.

    Article  CAS  Google Scholar 

  3. Jones JR, Brauer DS, Hupa L, Greenspan DC. Bioglass and bioactive glasses and their impact on healthcare. Int J Appl Glas Sci. 2016;7:423–34. https://doi.org/10.1111/ijag.12252.

    Article  CAS  Google Scholar 

  4. Xynos ID, Edgar AJ, Buttery LDK, Hench LL, Polak JM. Gene-expression profiling of human osteoblasts following treatment with the ionic products of Bioglass 45S5 dissolution. J Biomed Mater Res. 2001;55:151–7. https://doi.org/10.1002/1097-4636(200105)55:2<151::AID-JBM1001>3.0.CO;2-D.

    Article  CAS  Google Scholar 

  5. Bosetti M, Cannas M. The effect of bioactive glasses on bone marrow stromal cells differentiation. Biomaterials. 2005;26:3873–9. https://doi.org/10.1016/j.biomaterials.2004.09.059.

    Article  CAS  Google Scholar 

  6. Reilly GC, Radin S, Chen AT, Ducheyne P. Differential alkaline phosphatase responses of rat and human bone marrow derived mesenchymal stem cells to 45S5 bioactive glass. Biomaterials. 2007;28:4091–7. https://doi.org/10.1016/j.biomaterials.2007.05.038.

    Article  CAS  Google Scholar 

  7. Bielby RC, Phil D, Pryce RS, Phys M, Ph D, Hench LL et al. Enhanced derivation of osteogenic cells from murine embryonic stem cells after treatment with ionic dissolution products of 58S bioactive sol–gel glass. Tissue Eng. 2005;11:479–88.

    Article  CAS  Google Scholar 

  8. Houreh AB, Labbaf S, Ting H-K, Ejeian F, Jones JR, Esfahani M-HN. Influence of calcium and phosphorus release from bioactive glasses on viability and differentiation of dental pulp stem cells. J. Mater. Sci. 2017. https://doi.org/10.1007/s10853-017-0946-4.

    Article  CAS  Google Scholar 

  9. Jones JR. Review of bioactive glass: from Hench to hybrids. Acta Biomater. 2013;9:4457–86. https://doi.org/10.1016/j.actbio.2012.08.023.

    Article  CAS  Google Scholar 

  10. Baino F, Fiume E, Miola M, Verné E. Bioactive sol–gel glasses: rocessing, properties, and applications. Int J Appl Ceram Technol. 2018;15:841–60. https://doi.org/10.1111/ijac.12873.

    Article  CAS  Google Scholar 

  11. Naruphontjirakul P, Greasley SL, Chen S, Porter AE, Jones JR. Monodispersed strontium containing bioactive glass nanoparticles and MC3T3-E1 cellular response. Biomed Glas. 2016;2:72–81. https://doi.org/10.1515/bglass-2016-0009.

    Article  Google Scholar 

  12. Naruphontjirakul P, Porter AE, Jones JR. In vitro osteogenesis by intracellular uptake of strontium containing bioactive glass nanoparticles. Acta Biomater. 2018;66:67–80. https://doi.org/10.1016/j.actbio.2017.11.008.

    Article  CAS  Google Scholar 

  13. Gentleman E, Fredholm YC, Jell G, Lotfibakhshaiesh N, O’Donnell MD, Hill RG et al. The effects of strontium-substituted bioactive glasses on osteoblasts and osteoclasts in vitro. Biomaterials. 2010;31:3949–56. https://doi.org/10.1016/j.biomaterials.2010.01.121.

    Article  CAS  Google Scholar 

  14. Santocildes-romero ME, Crawford A, Hatton PV, Goodchild RL, Reaney IM, Miller CA. The osteogenic response of mesenchymal stromal cells to strontium-substituted bioactive glasses. J Tissue Eng Regen Med. 2015;9:619–31. https://doi.org/10.1002/term.2003.

    Article  CAS  Google Scholar 

  15. Yang F, Yang D, Tu J, Zheng Q, Cai L, Wang L. Strontium enhances osteogenic differentiation of mesenchymal stem cells and in vivo bone formation by activating Wnt/catenin. Stem Cells. 2011;29:981–91. https://doi.org/10.1002/stem.646.

    Article  CAS  Google Scholar 

  16. Cabrini L, Lo MP, Gorustovich AA, Steimetz T, Bfdq MP. Osteoconductivity of strontium-doped bioactive glass particles: a histomorphometric study in rats. J Biomed Mater Res Part A. 2009;92A:232–7. https://doi.org/10.1002/jbm.a.32355.

    Article  CAS  Google Scholar 

  17. Autefage H, Gentleman E, Littmann E, Hedegaard MAB, Von Erlach T, O’Donnell M et al. Sparse feature selection methods identify unexpected global cellular response to strontium-containing materials. PNAS. 2015;112:4280–5. https://doi.org/10.1073/pnas.1419799112.

    Article  CAS  Google Scholar 

  18. Naruphontjirakul P, Tsigkou O, Li S, Porter AE, Jones JR Human mesenchymal stem cells differentiate into an osteogenic lineage in presence of strontium containing bioactive glass nanoparticles, Acta Biomater. 2019. https://doi.org/10.1016/j.actbio.2019.03.038.

    Article  CAS  Google Scholar 

  19. Pires EG, Bonan RF, Rocha ÍM, Gonçalves IMF, de Souza JR, Gonzales LHV et al. Silver-doped 58S bioactive glass as an anti-Leishmania agent. Int J Appl Glas Sci. 2017;1:52–61. https://doi.org/10.1111/ijag.12285.

    Article  CAS  Google Scholar 

  20. Rahimnejad Yazdi A, Torkan L, Stone W, Towler MR. The impact of gallium content on degradation, bioactivity, and antibacterial potency of zinc borate bioactive glass. J. Biomed. Mater. Res. Part B Appl. Biomater. 2017: 1–10. https://doi.org/10.1002/jbm.b.33856.

    Article  Google Scholar 

  21. Barrioni BR, de Laia AGS, Valverde TM, da TM, Martins M, Caliari MV et al. Evaluation of in vitro and in vivo biocompatibility and structure of cobalt-releasing sol–gel bioactive glass. Ceram Int. 2018;44:20337–47. https://doi.org/10.1016/j.ceramint.2018.08.022.

    Article  CAS  Google Scholar 

  22. Azevedo M, Jell G, O’Donnell M, Law R, Hill R, Stevens M. Synthesis and characterization of hypoxia-mimicking bioactive glasses for skeletal regeneration. J Mater Chem. 2010;20:8854–64. https://doi.org/10.1039/c0jm01111h.

    Article  CAS  Google Scholar 

  23. Romero-Sánchez LB, Marí-Beffa M, Carrillo P, Medina MÁ, Díaz-Cuenca A, Copper-containing mesoporous bioactive glass promotes angiogenesis in an in vivo zebrafish model, Acta Biomater. 2018. https://doi.org/10.1016/j.actbio.2017.12.032.

    Article  Google Scholar 

  24. Kargozar S, Lotfibakhshaiesh N, Ai J, Mozafari M, Brouki Milan P, Hamzehlou S et al. Strontium- and cobalt-substituted bioactive glasses seeded with human umbilical cord perivascular cells to promote bone regeneration via enhanced osteogenic and angiogenic activities. Acta Biomater. 2017;58:502–14. https://doi.org/10.1016/j.actbio.2017.06.021.

    Article  CAS  Google Scholar 

  25. Lüthen F, Bulnheim U, Müller PD, Rychly J, Jesswein H, Nebe JGB. Influence of manganese ions on cellular behavior of human osteoblasts in vitro. Biomol Eng. 2007;24:531–6. https://doi.org/10.1016/j.bioeng.2007.08.003.

    Article  CAS  Google Scholar 

  26. Miola M, Brovarone CV, Maina G, Rossi F, Bergandi L, Ghigo D et al. In vitro study of manganese-doped bioactive glasses for bone regeneration. Mater Sci Eng C. 2014;38:107–18. https://doi.org/10.1016/j.msec.2014.01.045.

    Article  CAS  Google Scholar 

  27. Bae YJ, Kim MH. Manganese supplementation improves mineral density of the spine and femur and serum osteocalcin in rats. Biol Trace Elem Res. 2008;124:28–34. https://doi.org/10.1007/s12011-008-8119-6.

    Article  CAS  Google Scholar 

  28. Fujitani W, Hamada Y, Kawaguchi N, Mori S, Daito K, Uchinaka A et al. Synthesis of hydroxyapatite containing manganese and its evaluation of biocompatibility. Nano Biomed 2010;2:37–46. https://doi.org/10.11344/nano.2.37.

    Article  Google Scholar 

  29. Torres PMC, Vieira SI, Cerqueira aR, Pina S, Da Cruz Silva OaB, Abrantes JCC et al. Effects of Mn-doping on the structure and biological properties of β-tricalcium phosphate. J Inorg Biochem 2014;136:57–66. https://doi.org/10.1016/j.jinorgbio.2014.03.013.

    Article  CAS  Google Scholar 

  30. Yu L, Tian Y, Qiao Y, Liu X. Mn-containing titanium surface with favorable osteogenic and antimicrobial functions synthesized by PIII&D. Colloids Surf B Biointerfaces. 2017;152:376–84. https://doi.org/10.1016/j.colsurfb.2017.01.047.

    Article  CAS  Google Scholar 

  31. Sharma N, Jandaik S, Kumar S, Chitkara M, Sandhu IS. Synthesis, characterisation and antimicrobial activity of manganese- and iron-doped zinc oxide nanoparticles. J Exp Nanosci. 2016;11:54–71. https://doi.org/10.1080/17458080.2015.1025302.

    Article  CAS  Google Scholar 

  32. Nawaz Q, Atiq M, Rehman U, Burkovski A, Schmidt J, Beltrán AM. et al., Synthesis and characterization of manganese containing mesoporous bioactive glass nanoparticles for biomedical applications. J. Mater. Sci. Mater. Med. 2018;5: https://doi.org/10.1007/s10856-018-6070-4.

  33. Barrioni BR, Oliveira AC, de Fátima Leite M, de Magalhães Pereira M. Sol–gel-derived manganese-releasing bioactive glass as a therapeutic approach for bone tissue engineering. J Mater Sci. 2017;52:8904–27. https://doi.org/10.1007/s10853-017-0944-6.

    Article  CAS  Google Scholar 

  34. Li R, Clark AE, Hench LL. An investigation of bioactive glass powders by sol–gel processing. J Appl Biomater. 1991;2:231–9. https://doi.org/10.1002/jab.770020403.

    Article  CAS  Google Scholar 

  35. Brunauer S, Emmett PH, Teller E. Gases in multimolecular layers. J Am Chem Soc. 1938;60:309–19. https://doi.org/10.1021/ja01269a023.

    Article  CAS  Google Scholar 

  36. Barrett EP, Joyner LG, Halenda PP. The determination of pore volume and area distributions in porous substances. I. Computations from nitrogen isotherms. J Am Chem Soc. 1951;73:373–80. https://doi.org/10.1021/ja01145a126.

    Article  CAS  Google Scholar 

  37. Maçon ALB, Kim TB, Valliant EM, Goetschius K, Brow RK, Day DE et al. A unified in vitro evaluation for apatite-forming ability of bioactive glasses and their variants. J Mater Sci Mater Med. 2015;26:115 https://doi.org/10.1007/s10856-015-5403-9.

    Article  CAS  Google Scholar 

  38. de Oliveira AAR, de Souza DA, Dias LLS, de Carvalho SM, Mansur HS, de Magalhães M. Pereira, Synthesis, characterization and cytocompatibility of spherical bioactive glass nanoparticles for potential hard tissue engineering applications. Biomed Mater. 2013;8:025011 https://doi.org/10.1088/1748-6041/8/2/025011.

    Article  CAS  Google Scholar 

  39. Perez-Pariente J, Balas F, Vallet-Regi M. Surface and chemical study of SiO2·P2O5·CaO·(MgO) bioactive glasses. Chem Mater. 2000;12:750–5. https://doi.org/10.1021/cm9911114.

    Article  CAS  Google Scholar 

  40. Lin S, Ionescu C, Pike KJ, Smith ME, Jones JR. Nanostructure evolution and calcium distribution in sol–gel derived bioactive glass. J Mater Chem. 2009;19:1276–82. https://doi.org/10.1039/b814292k.

    Article  CAS  Google Scholar 

  41. Atkinson I, Anghel EM, Predoana L, Mocioiu OC, Jecu L, Raut I et al. Influence of ZnO addition on the structural, in vitro behavior and antimicrobial activity of sol–gel derived CaO–P2O5–SiO2 bioactive glasses. Ceram Int. 2016;42:3033–45. https://doi.org/10.1016/j.ceramint.2015.10.090.

    Article  CAS  Google Scholar 

  42. Gunawidjaja PN, Mathew R, Lo aYH, Izquierdo-Barba I, Garcia a, Arcos D et al. Local structures of mesoporous bioactive glasses and their surface alterations in vitro: inferences from solid-state nuclear magnetic resonance. Philos Trans R Soc A Math Phys Eng Sci. 2012;370:1376–99. https://doi.org/10.1098/rsta.2011.0257.

    Article  CAS  Google Scholar 

  43. El-Kady AM, Ali AF. Fabrication and characterization of ZnO modified bioactive glass nanoparticles. Ceram Int. 2012;38:1195–204. https://doi.org/10.1016/j.ceramint.2011.07.069.

    Article  CAS  Google Scholar 

  44. Moreira CDF, Carvalho SM, Mansur HS, Pereira MM. Thermogelling chitosan–collagen–bioactive glass nanoparticle hybrids as potential injectable systems for tissue engineering. Mater Sci Eng C. 2016;58:1207–16. https://doi.org/10.1016/j.msec.2015.09.075.

    Article  CAS  Google Scholar 

  45. Lusvardi G, Malavasi G, Menabue L, Shruti S. Gallium-containing phosphosilicate glasses: functionalization and in-vitro bioactivity. Mater Sci Eng C. 2013;33:3190–6. https://doi.org/10.1016/j.msec.2013.03.046.

    Article  CAS  Google Scholar 

  46. Paluszkiewicz C, Ślósarczyk A, Pijocha D, Sitarz M, Bućko M, Zima A et al. Synthesis, structural properties and thermal stability of Mn-doped hydroxyapatite. J Mol Struct. 2010;976:301–9. https://doi.org/10.1016/j.molstruc.2010.04.001.

    Article  CAS  Google Scholar 

  47. Ting H-K, Page S, Poologasundarampillai G, Chen S, Hanna JV, Jones JR. Phosphate content affects structure and bioactivity of sol–gel silicate bioactive glasses. Int. J. Appl. Glas. Sci. 2017. https://doi.org/10.1111/ijag.12322.

    Article  CAS  Google Scholar 

  48. Saboori A, Rabiee M, Moztarzadeh F, Sheikhi M, Tahriri M, Karimi M. Synthesis, characterization and in vitro bioactivity of sol–gel-derived SiO2-CaO-P2O5-MgO bioglass. Mater Sci Eng C. 2009;29:335–40. https://doi.org/10.1016/j.msec.2008.07.004.

    Article  CAS  Google Scholar 

  49. Toufiq AM, Wang F, Javed Q, Li Y. Influence of SiO2 on the structure-controlled synthesis and magnetic properties of prismatic MnO2 nanorods. Nanotechnology. 2013;24:415703 https://doi.org/10.1088/0957-4484/24/41/415703.

    Article  CAS  Google Scholar 

  50. Fayon F, Duée C, Poumeyrol T, Allix M, Massiot D. Evidence of nanometric-sized phosphate clusters in bioactive glasses as revealed by solid-state 31P NMR. J Phys Chem C. 2013;117:2283–8. https://doi.org/10.1021/jp312263j.

    Article  CAS  Google Scholar 

  51. Gostynski R, Conradie J, Erasmus E. Significance of the electron-density of molecular fragments on the properties of manganese(iii) β-diketonato complexes: an XPS and DFT study. RSC Adv. 2017;7:27718–28. https://doi.org/10.1039/C7RA04921H.

    Article  CAS  Google Scholar 

  52. Biesinger MC, Payne BP, Grosvenor AP, Lau LWM, Gerson AR, Smart RSC. Resolving surface chemical states in XPS analysis of first row transition metals, oxides and hydroxides: Cr, Mn, Fe, Co and Ni. Appl Surf Sci. 2011;257:2717–30. https://doi.org/10.1016/j.apsusc.2010.10.051.

    Article  CAS  Google Scholar 

  53. Cerrato JM, Hochella MF, Knocke WR, Dietrich AM, Cromer TF. Use of XPS to identify the oxidation state of Mn in solid surfaces of filtration media oxide samples from drinking water treatment plants. Environ Sci Technol. 2010;44:5881–6. https://doi.org/10.1021/es100547q.

    Article  CAS  Google Scholar 

  54. Nesbitt HW, Banerjee D. Interpretation of XPS Mn(2p) spectra of Mn oxyhydroxides and constraints on the mechanism of MnO2 precipitation. Am Miner. 1998;83:305–15. https://doi.org/10.2138/am-1998-3-414.

    Article  CAS  Google Scholar 

  55. Poinsignon C, Berthome G, Prélot B, Thomas F, Villiéras F. Manganese dioxides surface properties studied by XPS and gas adsorption. J Electrochem Soc. 2004;151:A1611–6. https://doi.org/10.1149/1.1789411.

    Article  CAS  Google Scholar 

  56. Bulavchenko OA, Vinokurov ZS, Afonasenko TN, Tsyrul’nikov PG, Tsybulya SV, Saraev AA et al. Reduction of mixed Mn–Zr oxides: in situ XPS and XRD. Stud, Dalt Trans. 2015;44:15499–507. https://doi.org/10.1039/C5DT01440A.

    Article  CAS  Google Scholar 

  57. Pascuta P, Borodi G, Jumate N, Vida-Simiti I, Viorel D, Culea E. The structural role of manganese ions in some zinc phosphate glasses and glass ceramics. J Alloy Compd. 2010;504:479–83. https://doi.org/10.1016/j.jallcom.2010.05.147.

    Article  CAS  Google Scholar 

  58. Gaddam A, Fernandes HR, Tulyaganov DU, Pascual MJ, Ferreira JMF. Role of manganese on the structure, crystallization and sintering of non-stoichiometric lithium disilicate glasses. RSC Adv. 2014;4:13581 https://doi.org/10.1039/c3ra46393a.

    Article  CAS  Google Scholar 

  59. Regan E, Groutso T, Metson JB, Steiner R, Ammundsen B, Hassell D et al. Surface and bulk composition of lithium manganese oxides. Surf Interface Anal. 1999;27:1064–8. https://doi.org/10.1002/(SICI)1096-9918(199912)27:12<1064::AID-SIA676>3.0.CO;2-S.

    Article  CAS  Google Scholar 

  60. Goel A, Rajagopal RR, Ferreira JMF. Influence of strontium on structure, sintering and biodegradation behaviour of CaO–MgO–SrO–SiO2–P2O5–CaF2 glasses. Acta Biomater. 2011;7:4071–80. https://doi.org/10.1016/j.actbio.2011.06.047.

    Article  CAS  Google Scholar 

  61. Azevedo MM, Tsigkou O, Nair R, Jones JR, Jell G, Stevens MM. Hypoxia inducible factor-stabilizing bioactive glasses for directing mesenchymal stem cell behavior. Tissue Eng Part A 2014;00:1–8. https://doi.org/10.1089/ten.TEA.2014.0083.

    Article  Google Scholar 

  62. Caplan AI. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol 2007;213:341–7. https://doi.org/10.1002/jcp.21200.

    Article  CAS  Google Scholar 

  63. Safadi FF, Barbe MF, Abdelmagid SM, Rico MC, Aswad RA Bone structure, development and bone biology: bone pathology. In: Bone Pathology; 2009. https://doi.org/10.1007/978-1-59745-347-9_1.

    Google Scholar 

  64. Khorami M, Hesaraki S, Behnamghader A, Nazarian H, Shahrabi S. In vitro bioactivity and biocompatibility of lithium substituted 45S5 bioglass. Mater Sci Eng C. 2011;31:1584–92. https://doi.org/10.1016/j.msec.2011.07.011.

    Article  CAS  Google Scholar 

  65. Wu C, Xia L, Han P, Mao L, Wang J, Zhai D et al. Europium-containing mesoporous bioactive glass scaffolds for stimulating in vitro and in vivo osteogenesis. ACS Appl Mater Interfaces. 2016;8:11342–54. https://doi.org/10.1021/acsami.6b03100.

    Article  CAS  Google Scholar 

  66. Effah Kaufmann EA, Ducheyne P, Shapiro IM. Evaluation of osteoblast response to porous bioactive glass (45S5) substrates by RT-PCR analysis. Tissue Eng. 2000;6:19–28. https://doi.org/10.1089/107632700320856.

    Article  CAS  Google Scholar 

  67. Thurner PJ, Chen CG, Ionova-martin S, Sun L, Harman A, Porter A et al. Osteopontin deficiency increases bone fragility but preserves bone mass. Bone. 2010;46:1564–73. https://doi.org/10.1016/j.bone.2010.02.014.

    Article  CAS  Google Scholar 

  68. Isaac J, Nohra J, Lao J, Jallot E, Nedelec JM, Berdal A et al. Effects of strontium-doped bioactive glass on the differentiation of cultured osteogenic cells. Eur Cells Mater. 2011;21:130–43.

    Article  CAS  Google Scholar 

  69. LA Strobel, N Hild, D Mohn, WJ Stark, A Hoppe, U Gbureck, RE Horch, U Kneser, AR Boccaccini, Novel strontium-doped bioactive glass nanoparticles enhance proliferation and osteogenic differentiation of human bone marrow stromal cells. J Nanopart Res. 2013;15. https://doi.org/10.1007/s11051-013-1780-5.

Download references

Acknowledgements

The authors acknowledge financial support from CNPq, CAPES and FAPEMIG/Brazil and to the Advanced Photoelectron Spectroscopy Laboratory (APSL—Department of Materials—Imperial College London) for XPS analysis.

Author information

Authors and Affiliations

  1. Department of Metallurgical Engineering and Materials, Federal University of Minas Gerais, School of Engineering, Belo Horizonte, MG, Brazil

    Breno Rocha Barrioni & Marivalda de Magalhães Pereira

  2. Department of Materials, Imperial College London, South Kensington, London, SW7 2AZ, UK

    Elizabeth Norris, Siwei Li, Parichart Naruphontjirakul & Julian R. Jones

  3. Biological Engineering Program, King Mongkut’s University of Technology Thonburi, Thon Buri, Thailand

    Parichart Naruphontjirakul

Authors
  1. Breno Rocha Barrioni
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elizabeth Norris
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Siwei Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Parichart Naruphontjirakul
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Julian R. Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Marivalda de Magalhães Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Breno Rocha Barrioni.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Barrioni, B.R., Norris, E., Li, S. et al. Osteogenic potential of sol–gel bioactive glasses containing manganese. J Mater Sci: Mater Med 30, 86 (2019). https://doi.org/10.1007/s10856-019-6288-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10856-019-6288-9

Search

Navigation