In vitro bioactivity and antibacterial properties of bismuth oxide modified bioactive glasses

Abstract

Chronic osteomyelitis, a bone infection caused by bacteria, requires extensive parenteral treatments. With an aim to develop bioactive glass with antibacterial properties to resist such infections, bioactive glasses with bismuth oxide as the dopant in various amounts up to 8 wt% were prepared. X-ray diffraction patterns and Fourier-transform infrared spectra of glass samples after immersion in simulated body fluid showed the presence of hydroxyapatite (HAp) and hydroxyl carbonate apatite for all samples except with the one having Bi2O3 substitution of 8 wt%. In vitro cell proliferation by MTT assay studies using a mouse fibroblast cell line (NIH3T3) have also been carried out. Primary antimicrobial activity of the glass particles was analyzed against Escherichia coli (E. coli) using broth microdilution method which exhibited bacteriostatic effects and bactericidal properties in selected samples. The combination of bioactivity, cell proliferation, and antibacterial properties of selected Bismuth-containing bioactive glasses could be exploited in treating bone-related infections.

This is a preview of subscription content, access via your institution.

FIG. 1
FIG. 2
FIG. 3
FIG. 4
FIG. 5
FIG. 6
FIG. 7
FIG. 8

References

  1. 1.

    L.L. Hench and J.R. Jones: Bioactive glasses: Frontiers and challenges. Front. Bioeng. Biotechnol. 3, 1 (2015).

    Article  Google Scholar 

  2. 2.

    L.L. Hench: The story of Bioglass®. J. Mater. Sci.: Mater. Med. 17, 967 (2006).

    CAS  Google Scholar 

  3. 3.

    Ö.H. Andersson, G. Liu, K.H. Karlsson, L. Niemi, J. Miettinen, and J. Juhanoja: In vivo behaviour of glasses in the SiO2–Na2O–CaO–P2O5–Al2O3–B2O3 system. J. Mater. Sci.: Mater. Med. 1, 219 (1990).

    CAS  Google Scholar 

  4. 4.

    M. Brink, T. Turunen, R-P. Happonen, and A. Yli-Urpo: Compositional dependence of bioactivity of glasses in the system Na2O–K2O–MgO–CaO–B2O3–P2O5–SiO2. J. Biomed. Mater. Res., Part A 37, 114 (1997).

    CAS  Article  Google Scholar 

  5. 5.

    D.P. Lew and F.A. Waldvogel: Osteomyelitis. Lancet 364, 369 (2004).

    CAS  Article  Google Scholar 

  6. 6.

    G. Sakoulas and R.C. Moellering: Increasing antibiotic resistance among methicillin-resistant Staphylococcus aureus strains. Clin. Infect. Dis. 46, S360 (2008).

    CAS  Article  Google Scholar 

  7. 7.

    W-T. Jia, Q. Fu, W-H. Huang, C-Q. Zhang, and M.N. Rahaman: Comparison of borate bioactive glass and calcium sulfate as implants for the local delivery of teicoplanin in the treatment of methicillin-resistant Staphylococcus aureus-induced osteomyelitis in a rabbit model. Antimicrob. Agents Chemother. 59, 7571 (2015).

    CAS  Article  Google Scholar 

  8. 8.

    I. Allan, H. Newman, and M. Wilson: Antibacterial activity of particulate Bioglass® against supra-and subgingival bacteria. Biomaterials 22, 1683 (2001).

    CAS  Article  Google Scholar 

  9. 9.

    M. Bellantone, H.D. Williams, and L.L. Hench: Broad-spectrum bactericidal activity of Ag2O-doped bioactive glass. Antimicrob. Agents Chemother. 46, 1940 (2002).

    CAS  Article  Google Scholar 

  10. 10.

    H. Zhu, C. Hu, F. Zhang, X. Feng, J. Li, T. Liu, J. Chen, and J. Zhang: Preparation and antibacterial property of silver-containing mesoporous 58S bioactive glass. Mater. Sci. Eng., C 42, 22 (2014).

    CAS  Article  Google Scholar 

  11. 11.

    M. Ottomeyer, A. Mohammadkah, D. Day, and D. Westenberg: Broad-spectrum antibacterial characteristics of four novel borate-based bioactive glasses. Adv. Microbiol. 6, 776 (2016).

    CAS  Article  Google Scholar 

  12. 12.

    A.M. Mulligan, M. Wilson, and J.C. Knowles: Effect of increasing silver content in phosphate-based glasses on biofilms of Streptococcus sanguis. J. Biomed. Mater. Res., Part A 67, 401 (2003).

    CAS  Article  Google Scholar 

  13. 13.

    E.A.A. Neel, I. Ahmed, J. Pratten, S.N. Nazhat, and J.C. Knowles: Characterisation of antibacterial copper releasing degradable phosphate glass fibres. Biomaterials 26, 2247 (2005).

    Article  CAS  Google Scholar 

  14. 14.

    A.M. Mulligan, M. Wilson, and J.C. Knowles: The effect of increasing copper content in phosphate-based glasses on biofilms of Streptococcus sanguis. Biomaterials 24, 1797 (2003).

    CAS  Article  Google Scholar 

  15. 15.

    Y-F. Goh, A.Z. Alshemary, M. Akram, M.R.A. Kadir, and R. Hussain: In vitro characterization of antibacterial bioactive glass containing ceria. Ceram. Int. 40, 729 (2014).

    CAS  Article  Google Scholar 

  16. 16.

    D.W. Bierer: Bismuth subsalicylate: History, chemistry, and safety. Rev. Infect. Dis. 12, S3 (1990).

    CAS  Article  Google Scholar 

  17. 17.

    J.R. Lambert and P. Midolo: The actions of bismuth in the treatment of Helicobacter pylori infection. Aliment. Pharmacol. Ther. 11, 27 (1997).

    Article  Google Scholar 

  18. 18.

    M. Parirokh and M. Torabinejad: Mineral trioxide aggregate: A comprehensive literature review—Part I: Chemical, physical, and antibacterial properties. J. Endod. 36, 16 (2010).

    Article  Google Scholar 

  19. 19.

    M. Torabinejad and M. Parirokh: Mineral trioxide aggregate: A comprehensive literature review—Part II: Leakage and biocompatibility investigations. J. Endod. 36, 190 (2010).

    Article  Google Scholar 

  20. 20.

    T.J. Webster, E.A. Massa-Schlueter, J.L. Smith, and E.B. Slamovich: Osteoblast response to hydroxyapatite doped with divalent and trivalent cations. Biomaterials 25, 2111 (2004).

    CAS  Article  Google Scholar 

  21. 21.

    G. Ciobanu, A.M. Bargan, and C. Luca: New bismuth-substituted hydroxyapatite nanoparticles for bone tissue engineering. JOM 67, 2534 (2015).

    CAS  Article  Google Scholar 

  22. 22.

    S. Heid, P.R. Stoessel, T.T. Tauböck, W.J. Stark, M. Zehnder, and D. Mohn: Incorporation of particulate bioactive glasses into a dental root canal sealer. Biomed. Glasses 2, 29 (2016).

    Article  Google Scholar 

  23. 23.

    D. Mohn, M. Zehnder, T. Imfeld, and W.J. Stark: Radio-opaque nanosized bioactive glass for potential root canal application: Evaluation of radiopacity, bioactivity and alkaline capacity. Int. Endontic. J. 43, 210 (2010).

    CAS  Article  Google Scholar 

  24. 24.

    T. Kokubo, H. Kushitani, S. Sakka, T. Kitsugi, and T. Yamamuro: Solutions able to reproduce in vivo surface-structure changes in bioactive glass-ceramic A–W3. J. Biomed. Mater. Res. 24, 721 (1990).

    CAS  Article  Google Scholar 

  25. 25.

    S.A. Bernard, V.K. Balla, N.M. Davies, S. Bose, and A. Bandyopadhyay: Bone cell–materials interactions and Ni ion release of anodized equiatomic NiTi alloy. Acta Biomater. 7, 1902 (2011).

    CAS  Article  Google Scholar 

  26. 26.

    S. Bodhak, V.K. Balla, S. Bose, A. Bandyopadhyay, U. Kashalikar, S.K. Jha, and S. Sastri: In vitro biological and tribological properties of transparent magnesium aluminate (Spinel) and aluminum oxynitride (ALON®). J. Mater. Sci.: Mater. Med. 22, 1511 (2011).

    CAS  Google Scholar 

  27. 27.

    J.M. Andrews: Determination of minimum inhibitory concentrations. J. Antimicrob. Chemother. 48, 5 (2001).

    CAS  Article  Google Scholar 

  28. 28.

    X. Ou, S. Xu, J.M. Warnett, S.M. Holmes, A. Zaheer, A.A. Garforth, M.A. Williams, Y. Jiao, and X. Fan: Creating hierarchies promptly: Microwave-accelerated synthesis of ZSM-5 zeolites on macrocellular silicon carbide (SiC) foams. Chem. Eng. J. 312, 1 (2017).

    CAS  Article  Google Scholar 

  29. 29.

    K.M. El Badry, F.A. Moustaffa, M.A. Azooz, and F.H. El Batal: Infrared absorption spectroscopy of some bio-glasses before and after immersion in various solutions. Indian J. Pure Appl. Phys. 38, 741 (2000).

    Google Scholar 

  30. 30.

    S. Koutsopoulos: Synthesis and characterization of hydroxyapatite crystals: A review study on the analytical methods. J. Biomed. Mater. Res. 62, 600 (2002).

    CAS  Article  Google Scholar 

  31. 31.

    F.Z. Ren and Y. Leng: Carbonated apatite, type-A or type-B? Key Eng. Mater. 493, 293 (2012).

    Google Scholar 

  32. 32.

    D.M. Ibrahim, A.A. Mostafa, and S.I. Korowash: Chemical characterization of some substituted hydroxyapatites. Chem. Cent. J. 5, 74 (2011).

    CAS  Article  Google Scholar 

  33. 33.

    I. Ardelean, S. Cora, and V. Ioncu: Structural investigation of CuO–Bi2O3–B2O3 glasses by FT-IR, Raman and UV-VIS spectroscopies. J. Optoelectron. Adv. Mater. 8, 1843 (2006).

    CAS  Google Scholar 

  34. 34.

    F. He, Z. He, J. Xie, and Y. Li: IR and Raman spectra properties of Bi2O3–ZnO–B2O3–BaO quaternary glass system. Am. J. Anal. Chem. 5, 1142 (2014).

    CAS  Article  Google Scholar 

  35. 35.

    J. Massera, S. Fagerlund, L. Hupa, and M. Hupa: Crystallization mechanism of the bioactive glasses, 45S5 and S53P4. J. Am. Ceram. Soc. 95, 607 (2012).

    CAS  Article  Google Scholar 

  36. 36.

    K. Fujikura, N. Karpukhina, T. Kasuga, D.S. Brauer, R.G. Hill, and R.V. Law: Influence of strontium substitution on structure and crystallisation of Bioglass® 45S5. J. Mater. Chem. 22, 7395 (2012).

    CAS  Article  Google Scholar 

  37. 37.

    X. Wang, S. Fagerlund, J. Massera, B. Södergård, and L. Hupa: Do properties of bioactive glasses exhibit mixed alkali behavior? J. Mater. Sci. 52, 8986 (2017).

    CAS  Article  Google Scholar 

  38. 38.

    K.C. da Silva Gasque, L.P. Al-Ahj, R.C. Oliveira, and A.C. Magalhães: Cell density and solvent are critical parameters affecting formazan evaluation in MTT assay. Braz. Arch. Biol. Technol. 57, 381 (2014).

    Article  Google Scholar 

  39. 39.

    C.R. Kruse, M. Singh, S. Targosinski, I. Sinha, J.A. Sørensen, E. Eriksson, and K. Nuutila: The effect of pH on cell viability, cell migration, cell proliferation, wound closure, and wound reepithelialization: In vitro and in vivo study. Wound Repair Regen. 25, 260 (2017).

    Article  Google Scholar 

  40. 40.

    A-M. Galow, A. Rebl, D. Koczan, S.M. Bonk, W. Baumann, and J. Gimsa: Increased osteoblast viability at alkaline pH in vitro provides a new perspective on bone regeneration. Biochem. Biophys. Rep. 10, 17 (2017).

    Google Scholar 

  41. 41.

    F. Thomas, B. Bialek, and R. Hensel: Medical use of bismuth: The two sides of the coin. J. Clin. Toxicol. S3, 495 (2011).

    Google Scholar 

  42. 42.

    P.T. Reynolds, K.C. Abalos, J. Hopp, and M.E. Williams: Bismuth toxicity: A rare cause of neurologic dysfunction. Int. J. Clin. Med. 3, 46 (2012).

    CAS  Article  Google Scholar 

  43. 43.

    Q.L. Feng, J. Wu, G.Q. Chen, F.Z. Cui, T.N. Kim, J.O. Kim, T.N. Kim, and J.O. Kim: A mechanistic study of the antibacterial effect of silver ions on Escherichia coli and Staphylococcus aureus. J. Biomed. Mater. Res. 52, 662 (2000).

    CAS  Article  Google Scholar 

Download references

ACKNOWLEDGMENTS

Authors would like to express their grateful thanks to Dr. K. Muraleedharan, Director, CSIR-CGCRI and Dr. Ranjan Sen, Head, Glass division for their encouragement and support toward this work. The financial help from P 81-113 of the CSIR Extramural Research Fund for Young Scientists and CSIR-HRDG (Extramural Research Group) for providing GATE-JRF fellowship to SPS for pursuing Integrated M.Tech Ph.D. program is gratefully acknowledged. The authors gratefully acknowledge the suggestions and experimental help offered by Dr. Biswanath Kundu, Senior Scientist and Dr. Vamsi K. Balla, Senior Principal Scientist, Bioceramics and Coating Division, CSIR-CGCRI.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Kaushik Biswas.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Prasad S, S., Ratha, I., Adarsh, T. et al. In vitro bioactivity and antibacterial properties of bismuth oxide modified bioactive glasses. Journal of Materials Research 33, 178–190 (2018). https://doi.org/10.1557/jmr.2017.442

Download citation