Synthesis and characterization of manganese containing mesoporous bioactive glass nanoparticles for biomedical applications

Abstract

Mesoporous bioactive glass (BG) nanoparticles based in the system: SiO2–P2O5–CaO–MnO were synthesized via a modified Stöber process at various concentrations of Mn (0–7 mol %). The synthesized manganese-doped BG nanoparticles were characterized in terms of morphology, composition, in vitro bioactivity and antibacterial activity. Scanning electron microscopy (SEM), transmission electron microscopy (TEM) and Brunauer–Emmett–Teller (BET) analysis confirmed that the particles had spherical morphology (mean particle size: 110 nm) with disordered mesoporous structure. Energy dispersive X-ray spectroscopy (EDX) confirmed the presence of Mn, Ca, Si and P in the synthesized Mn-doped BG particles. Moreover, X-ray diffraction (XRD) analysis showed that Mn has been incorporated in the amorphous silica network (bioactive glass). Moreover, it was found that manganese-doped BG particles form apatite crystals upon immersion in simulated body fluid (SBF). Inductively coupled plasma atomic emission spectroscopy (ICP-OES) measurements confirmed that Mn is released in a sustained manner, which provided antibacterial effect against Bacillus subtilis, Pseudomonas aeruginosa and Staphylococcus aureus. The results indicate that the incorporation of Mn in the bioactive glass network is an effective strategy to develop novel multifunctional BG nanoparticles for bone tissue engineering.

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

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

References

  1. 1.

    Nicolini V, Malavasi G, Menabue L, Lusvardi G, Benedetti F, Valeri S, Luches P. Cerium-doped bioactive 45S5 glasses: spectroscopic, redox, bioactivity and biocatalytic properties. J Mater Sci. 2017;52:8845–57.

  2. 2.

    Eqtesadi S, Motealleh A, Miranda P, Pajares A, Lemos A, Ferreira JMF. Robocasting of 45S5 bioactive glass scaffolds for bone tissue engineering. J Eur Ceram Soc. 2014;34:107–18.

    CAS  Article  Google Scholar 

  3. 3.

    Gerhardt L-C, Boccaccini AR. Bioactive Glass and Glass-Ceramic Scaffolds for Bone Tissue Engineering. Materials. 2010;3:3867–910.

    CAS  Article  Google Scholar 

  4. 4.

    Salgado AJ, Coutinho OP, Reis RL. Bone tissue engineering: State of the art and future trends. Macromol Biosci. 2004;4:743–65.

    CAS  Article  Google Scholar 

  5. 5.

    Hench LL, hompson I. Twenty-first century challenges for biomaterials. J R Soc Interface. 2014;7:S379–91.

    Article  Google Scholar 

  6. 6.

    Hench LL. The story of Bioglass. J Mater Sci Mater Med. 2006;17:967–78.

    CAS  Article  Google Scholar 

  7. 7.

    Jones JR, Review of bioactive glass: From Hench to hybrids. Acta Biomater. 2015;23:S53–82.

    Article  Google Scholar 

  8. 8.

    Miguez-Pacheco V, Hench LL, Boccaccini AR. Bioactive glasses beyond bone and teeth: Emerging applications in contact with soft tissues. Acta Biomater. 2015;13:1–15.

    CAS  Article  Google Scholar 

  9. 9.

    Schröder HC, Wang XH, Wiens M, Diehl-Seifert B, Kropf K, Schloßmacher U, Müller WEG, Silicate modulates the cross-talk between osteoblasts (SaOS-2) and osteoclasts (RAW 264.7 cells): Inhibition of osteoclast gro wth and differentiation. J Cell Biochem. 2012;113:3197–206..

  10. 10.

    Shie MY, Ding SJ, Chang HC. The role of silicon in osteoblast-like cell proliferation and apoptosis. Acta Biomater. 2011;7:2604–14.

    CAS  Article  Google Scholar 

  11. 11.

    Haro Durand LA, Vargas GE, Romero NM, Vera-Mesones R, Porto-López JM, Boccaccini AR, Zago MP, Baldi A, Gorustovich A. Angiogenic effects of ionic dissolution products released from a boron-doped 45S5 bioactive glass. J Mater Chem B. 2015;3:1142–8.

    CAS  Article  Google Scholar 

  12. 12.

    Balasubramanian P, Hupa L, Jokic B, Detsch R, Grünewald A, Boccaccini AR, Angiogenic potential of boron-containing bioactive glasses: in vitro study. J Mater Sci. 2017;52:8785–92.

  13. 13.

    Hench LL, Chronology of Bioactive Glass Development and Clinical Applications. New J Glas Ceram. 2013;3:67–73.

    Article  Google Scholar 

  14. 14.

    Qazi TH, Hafeez S, Schmidt J, Duda GN, Boccaccini AR, Lippens E. Comparison of the effects of 45S5 and 1393 bioactive glass microparticles on hMSC behavior. J Biomed Mater Res-Part A. 2017;105:2772–82.

    CAS  Article  Google Scholar 

  15. 15.

    Hoppe A, Guldal NS, Boccaccini AR. A review of the biological response to ionic dissolution products from bioactive glasses and glass-ceramics. Biomaterials. 2011;32:2757–74.

  16. 16.

    Salinas AJ, Shruti S, Malavasi G, Menabue L, Vallet-Regí M. Substitutions of cerium, gallium and zinc in ordered mesoporous bioactive glasses. Acta Biomater. 2011;7:3452–8.

    CAS  Article  Google Scholar 

  17. 17.

    Wu C, Zhou Y, Fan W, Han P, Chang J, Yuen J, Zhang M, Xiao Y. Hypoxia-mimicking mesoporous bioactive glass scaffolds with controllable cobalt ion release for bone tissue engineering. Biomaterials. 2012;33:2076–85.

  18. 18.

    Zheng K, Dai X, Lu M, Huser N, Taccardi N, Boccaccini AR. Synthesis of copper-containing bioactive glass nanoparticles using a modified Stober method for biomedical applications. Colloids Surf B Biointerfaces. 2017;150:159–67.

    CAS  Article  Google Scholar 

  19. 19.

    Wu C, Zhou Y, Lin C, Chang J, Xiao Y. Strontium-containing mesoporous bioactive glass scaffolds with improved osteogenic/cementogenic differentiation of periodontal ligament cells for periodontal tissue engineering. Acta Biomater. 2012;8:3805–15.

  20. 20.

    Kavitha RJ, Subha B, Shanmugam S, Ravichandran K. Synthesis and Invitro Characterisation of Lithium Doped Bioactive Glass through Quick Alkali Sol - Gel Method. Int J Innov Res Sci Eng. 2014;2:2347–3207.

  21. 21.

    Miguez-Pacheco V, de Ligny D, Schmidt J, Detsch R, Boccaccini AR. Development and characterization of niobium-releasing silicate bioactive glasses for tissue engineering applications. J Eur Ceram Soc. 2017;38:871–76.

    Article  Google Scholar 

  22. 22.

    Wu C, Miron R, Sculean A, Kaskel S, Doert T, Schulze R, Zhang Y. Proliferation, differentiation and gene expression of osteoblasts in boron-containing associated with dexamethasone deliver from mesoporous bioactive glass scaffolds. Biomaterials. 2011;32:7068–78.

    CAS  Article  Google Scholar 

  23. 23.

    Balasubramanian P, Strobel LA, Kneser U, Boccaccini AR. Zinc-containing bioactive glasses for bone regeneration, dental and orthopedic applications. Biomed Glas. 2015;1:51–69.

    Google Scholar 

  24. 24.

    Sopyan I, Ramesh S, Nawawi NA, Tampieri A, Sprio S. Effects of manganese doping on properties of sol-gel derived biphasic calcium phosphate ceramics. Ceram Int. 2011;37:3703–15.

    CAS  Article  Google Scholar 

  25. 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.

  26. 26.

    Srivastava AK, Pyare R, Singh SP. In vitro bioactivity and physical–mechanical properties of MnO2 substituted 45S5 bioactive glasses and glass-ceramics. J Biomater Tissue Eng. 2012;2:249–58.

  27. 27.

    Fujitani W, Hamada Y, Kawaguchi N, Mori S, Daito K, Uchinaka A, Matsumoto T, Kojima Y, Daito M, Nakano T, Matsuura N. Synthesis of Hydroxyapatite Contining Manganese and Its Evaluation of Biocompatibility. Nano Biomed. 2010;2:37–46.

  28. 28.

    Miola M, Brovarone CV, Maina G, Rossi F, Bergandi L, Ghigo D, Saracino S, Maggiora M, Canuto RA, Muzio G, Vernè E. In vitro study of manganese-doped bioactive glasses for bone regeneration. Mater Sci Eng C. 2014;38:107–18.

  29. 29.

    Barrioni BR, Oliveira AC, de Fatima Leite M, de Magalhaes Pereira M. Sol-gel-derived manganese-releasing bioactive glass as a therapeutic approach for bone tissue engineering. J Mater Sci. 2017;52:8904–27.

  30. 30.

    Creaven BS, Egan DA, Karcz D, Kavanagh K, McCann M, Mahon M, Noble A, Thati B, Walsh M. Synthesis, characterisation and antimicrobial activity of copper(II) and manganese(II) complexes of coumarin-6,7-dioxyacetic acid (cdoaH2) and 4-methylcoumarin-6,7-dioxyacetic acid (4-MecdoaH2): X-ray crystal structures of [Cu(cdoa)(phen)2] · 8.8H2O and [Cu(4-Mecdoa)(phen)2] · 13H2O (phen = 1,10-phenanthroline). J Inorg Biochem. 2007;101:1108–19.

  31. 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.

    CAS  Article  Google Scholar 

  32. 32.

    Dorkov P, Pantcheva IN, Sheldrick WS, Mayer-Figge H, Petrova R. Mitewa M. Synthesis, structure and antimicrobial activity of manganese(II) and cobalt(II) complexes of the polyether ionophore antibiotic Sodium Monensin A. J Inorg Biochem. 2008;102:26–32.

    CAS  Article  Google Scholar 

  33. 33.

    Philippart A, Gómez-Cerezo N, Arcos D, Salinas AJ, Boccardi E, Vallet-Regi M, Boccaccini AR. Novel ion-doped mesoporous glasses for bone tissue engineering: Study of their structural characteristics influenced by the presence of phosphorous oxide. J Non Cryst Solids. 2017;455:90–7.

  34. 34.

    Erol-Taygun M, Zheng K, Boccaccini AR. Nanoscale Bioactive Glasses in Medical Applications. Int J Appl Glas Sci. 2013;4:136–48.

  35. 35.

    Zhao L, Yan X, Zhou X, Zhou L, Wang H, Tang J, Yu C. Mesoporous bioactive glasses for controlled drug release. Microporous Mesoporous Mater. 2008;109:210–5.

    CAS  Article  Google Scholar 

  36. 36.

    Yan X, Yu C, Zhou X, Tang J, Zhao D. Highly ordered mesoporous bioactive glasses with superior in vitro bone-forming bioactivities. Angew Chem-Int Ed. 2004;43:5980–4.

  37. 37.

    Tang F, Li L, Chen D. Mesoporous silica nanoparticles: Synthesis, biocompatibility and drug delivery. Adv Mater. 2012;24:1504–34.

  38. 38.

    Xia W, Chang J. Well-ordered mesoporous bioactive glasses (MBG): A promising bioactive drug delivery system. J Control Release. 2006;110:522–30.

  39. 39.

    Gargiulo N, Cusano AM, Causa F, Caputo D, Netti PA. Silver-containing mesoporous bioactive glass with improved antibacterial properties. J Mater Sci Mater Med. 2013;24:2129–35.

  40. 40.

    Wu C, Zhou Y, Xu M, Han P, Chen L, Chang J, Xiao Y. Copper-containing mesoporous bioactive glass scaffolds with multifunctional properties of angiogenesis capacity, osteostimulation and antibacterial activity. Biomaterials. 2013;34:422–33.

  41. 41.

    Zhu Y, Li X, Yang J, Wang S, Gao H, Hanagata N. Composition-structure-property relationships of the CaO-MxOy-SiO2-P2O5 (M = Zr, Mg, Sr) mesoporous bioactive glass (MBG) scaffolds. J Mater Chem. 2011;21:9208–18.

    CAS  Article  Google Scholar 

  42. 42.

    Wu C, Chang J. Multifunctional mesoporous bioactive glasses for effective delivery of therapeutic ions and drug/growth factors. J Control Release. 2014;193:282–95.

    CAS  Article  Google Scholar 

  43. 43.

    Zheng K, Taccardi N, Beltrán AM, Sui B, Zhou T, Marthala VRR, Hartmann M, Boccaccini AR. Timing of calcium nitrate addition affects morphology, dispersity and composition of bioactive glass nanoparticles. RSC Adv. 2016;6:95101–11.

  44. 44.

    Kozon D, Zheng K, Boccardi E, Liu Y, Liverani L, Boccaccini AR. Synthesis of monodispersed Ag-doped bioactive glass nanoparticles via surface modification. Materials. 2016;9:225–32.

  45. 45.

    Ye J, He J, Wang C, Yao K, Gou Z. Copper-containing mesoporous bioactive glass coatings on orbital implants for improving drug delivery capacity and antibacterial activity. Biotechnol Lett. 2014;36:961–8.

  46. 46.

    Kokubo T, Takadama H. How useful is SBF in predicting in vivo bone bioactivity? Biomaterials 2006;27:2907–15.

  47. 47.

    Wumes SE, Smith JA, Struhl K. Culinary Biol. 1990;61:17-18.

  48. 48.

    Ur Rehman MA, Ferraris S, Goldmann WH, Perero S, Bastan FE, Nawaz Q, Di Confiengo GG, Ferraris M, Boccaccini AR. Antibacterial and Bioactive Coatings Based on RF Co-sputtering of Silver Nanocluster-silica Coatings on PEEK/ bioactive Glass Layers Obtained by Electrophoretic Deposition. ACS Appl Mater Interfaces. 2017;9:32489–97.

  49. 49.

    Pishbin F, Mouriño V, Gilchrist JB, McComb DW, Kreppel S, Salih V, Ryan MP, Boccaccini AR. Single-step electrochemical deposition of antimicrobial orthopaedic coatings based on a bioactive glass/chitosan/nano-silver composite system. Acta Biomater. 2013;9:7469–79.

  50. 50.

    Stähli C, James-Bhasin M, Hoppe A, Boccaccini AR, Nazhat SN. Effect of ion release from Cu-doped 45S5 Bioglass on 3D endothelial cell morphogenesis. Acta Biomater. 2015;19:15–22.

  51. 51.

    Masalov VM, Sukhinina NS, Kudrenko EA, Emelchenko GA. Mechanism of formation and nanostructure of Stöber silica particles. Nanotechnology. 2011;22:275718–26.

  52. 52.

    Tsigkou O, Labbaf S, Stevens MM, Porter AE, Jones JR. Monodispersed bioactive glass submicron particles and their effect on bone marrow and adipose tissue-derived stem cells. Adv Healthc Mater. 2014;3:115–25.

  53. 53.

    Bari A, Bloise N, Fiorilli S, Novajra G, Vallet-Regí M, Bruni G, Torres-Pardo A, González-Calbet JM, Visai L, Vitale-Brovarone C. Copper-containing mesoporous bioactive glass nanoparticles as multifunctional agent for bone regeneration. Acta Biomater. 2017;55:493–504.

  54. 54.

    Stöber W, Fink A, Bohn E. Controlled growth of monodisperse silica spheres in the micron size range. J Colloid Interface Sci. 1968;26:62–9.

  55. 55.

    Bantz C, Koshkina O, Lang T, Galla HJ, Kirkpatrick CJ, Stauber RH, Maskos M. Beilstein. The surface properties of nanoparticles determine the agglomeration state and the size of the particles under physiological conditions. J Nanotechnol. 2014;5:1774–86.

  56. 56.

    Wu C, Fan W, Chang J. Functional mesoporous bioactive glass nanospheres: synthesis, high loading efficiency, controllable delivery of doxorubicin and inhibitory effect on bone cancer cells. J Mater Chem B. 2013;1:2710.

  57. 57.

    Courrol LC, de Oliveira Silva FR, Gomes L. A simple method to synthesize silver nanoparticles by photo-reduction. Colloids Surf A Physicochem Eng Asp. 2007;305:54–7.

  58. 58.

    Schumacher M, Reither L, Thomas J, Kampschulte M, Gbureck U, Lode A, Gelinsky M. Calcium phosphate bone cement/mesoporous bioactive glass composites for controlled growth factor delivery. Biomater Sci. 2017;5:578–88.

  59. 59.

    Balamurugan A, Sockalingum G, Michel J, Fauré J, Banchet V, Wortham L, Bouthors S, Laurent-Maquin D, Balossier G. Synthesis and characterisation of sol gel derived bioactive glass for biomedical applications. Mater Lett. 2006;60:3752–7.

  60. 60.

    Hoppe A, Meszaros R, Stähli C, Romeis S, Schmidt J, Peukert W, Marelli B, Nazhat SN, Wondraczek L, Lao J, Jallot E, Boccaccini AR. In vitro reactivity of Cu doped 45S5 Bioglass® derived scaffolds for bone tissue engineering. J Mater Chem B. 2013;1:5659–74.

  61. 61.

    Bejarano J, Caviedes P, Palza H. Sol–gel synthesis and in vitro bioactivity of copper and zinc-doped silicate bioactive glasses and glass-ceramics. Biomed Mater. 2015;10:25001–13.

  62. 62.

    de Oliveira AAR, de Carvalho BB, Mansur HS, de Magalhães M. Pereira. Synthesis and characterization of bioactive glass particles using an ultrasound-assisted sol–gel process: Engineering the morphology and size of sonogels via a poly (ethylene glycol) dispersing agent. Mater Lett. 2014;133:44–8.

  63. 63.

    Pishbin F, Mourino V, Flor S, Kreppel S, Salih V, Ryan MP, Boccaccini AR. Electrophoretic deposition of gentamicin-loaded bioactive glass/chitosan composite coatings for orthopaedic implants. ACS Appl Mater Interfaces. 2014;6:8796–806.

  64. 64.

    Atiq M, Rehman U, Bastan FE, Nawaz Q, Boccaccini AR. Electrophoretic deposition of lawsone loaded nanoscale silicate glass / chitosan composite on PEEK / BG layers. Electrochem Soc Tras. 2018;82:45–50.

  65. 65.

    Zheng K, Boccaccini AR, Sol-gel processing of bioactive glass nanoparticles. Adv Colloid Interface Sci. 2017;249:363–73.https://doi.org/10.1016/j.cis.2017.03.008.

    CAS  Article  Google Scholar 

  66. 66.

    Kaya S, Cresswell M, Boccaccini AR. Mesoporous silica-based bioactive glasses for antibiotic-free antibacterial applications. Mater Sci Eng C. 2018;83:99–107.

  67. 67.

    Ciapetti G, Savarino L, Miola M, Verné E, Vitale-Brovaron C,Baldini N. In vitro testing of manganese-doped bioglasses to stimulate osteoblast behaviour. Dental Materials. 2014;30:e166

    Article  Google Scholar 

Download references

Acknowledgements

QN would like to thank Higher Education Commission (HEC) of Pakistan for granting a scholarship. Authors would like to thank the TEM facilities of CITIUS-US. TEM analyses have been funded by Grant P2017/837 from the University of Seville (Spain).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Aldo R. Boccaccini.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Nawaz, Q., Rehman, M.A.U., Burkovski, A. et al. Synthesis and characterization of manganese containing mesoporous bioactive glass nanoparticles for biomedical applications. J Mater Sci: Mater Med 29, 64 (2018). https://doi.org/10.1007/s10856-018-6070-4

Download citation