Bioactive glasses enriched with zinc and strontium: synthesis, characterization, cytocompatibility with osteoblasts and antibacterial properties

Ciołek, Lidia; Chraniuk, Milena; Bollin, Piotr; Biernat, Monika; Panasiuk, Mirosława; Nidzworski, Dawid; Gromadzka, Beata; Jaegermann, Zbigniew; Pamuła, Elżbieta

doi:10.37190/abb-02339-2023-02

Abstract

Purpose: The aim of the presented work was to characterize the new obtained bioglasses and assess their biological performance in vitro. Bioglasses were produced using the sol-gel method in the SiO₂-P₂O₅-CaO system, for the purpose as composite ingredients. Their chemical composition was enriched with ZnO to introduce antibacterial properties and SrO with osteoinductive effect. The properties of bioglasses were compared and the effect of chemical composition and particle size on their biological properties was assessed.

Methods: The bioglasses were evaluated via TG-DTA, FTIR, SEM-EDS analyses before and after incubation in SBF solution. LDH and WST-1 tests were used to determine the level of cytotoxicity of the tested bioglasses on hFOB1.19 osteoblasts.

Results: The results show that the developed bioglasses release Ca²⁺, are bioactive in SBF solution, not cytotoxic and show antibacterial activity in contact with Pseudomonas aeruginosa and Staphylococcus aureus strains. Bioglasses enriched with ZnO show the highest bactericidal activity. All tested bioglasses enhanced hFOB 1.19 cells proliferation. Particle size has a lower effect on biological performance of the bioglasses than their chemical composition.

Conclusions: The conducted research showed that bioglass modification with SrO and ZnO can be considered particularly for the development of biomaterials supporting bone regeneration and the treatment of infected bone defects.

References

Baheiraei N., Eyni H., Bakhshi B., Najafloo R., Rabiee N., Effects of strontium ions with potential antibacterial activity on in vivo bone regeneration, Sci. Rep., 2021, 11, 1–9, DOI: 10.1038/s41598-021-88058-1.
Search in Google Scholar Back to article
Balasubramanian P., Strobel L.A., Kneser U., Boccaccini A.R., Zinc-containing bioactive glasses for bone regeneration, dental and orthopedic applications, Biomed. Glas., 2015, 1, 51–69, DOI: 10.1515/bglass-2015-0006.
Search in Google Scholar Back to article
Beyersmann D., Homeostasis and Cellular Functions of Zinc, Materwiss. Werksttech., 2002, 33, 764–769, DOI: 10.1002/mawe.200290008.
Search in Google Scholar Back to article
Cacciotti I., Bivalent cationic ions doped bioactive glasses: the influence of magnesium, zinc, strontium and copper on the physical and biological properties, J. Mater. Sci., 2017, 52, 8812–8831, DOI: 10.1007/s10853-017-1010-0.
Search in Google Scholar Back to article
Ciołek L., Biernat M., Jaegermann Z., Zaczyńska E., Czarny A., Jastrzębska A., The studies of cytotoxicity and antibacterial activity of composites with ZnO-doped bioglass, Int. J. Appl. Ceram. Technol., 2019, 16, 541–551, DOI: 10.1111/ijac.13144.
Search in Google Scholar Back to article
Deshmukh K., Kovářík T., Křenek T., Docheva D., Stich T., Pola J., Recent advances and future perspectives of sol-gel derived porous bioactive glasses: a review, RSC Adv., 2020, 10, 33782–33835, DOI: 10.1039/d0ra04287k.
Search in Google Scholar Back to article
El-Kady A.M., Kamel N.A., Elnashar M.M., Farag M.M., Production of bioactive glass/chitosan scaffolds by freezegelation for optimized vancomycin delivery: Effectiveness of glass presence on controlling the drug release kinetics, J. Drug. Deliv. Sci. Technol., 2021, 66, 102779, DOI: 10.1016/j.jddst.2021.102779.
Search in Google Scholar Back to article
Fredholm Y.C., Karpukhina N., Brauer D.S., Jones J.R., Law R.V., Hill R.G., Influence of strontium for calcium substitution in bioactive glasses on degradation, ion release and apatite formation, J. R. Soc. Interface, 2012, 9, 880–889, DOI: 10.1098/rsif.2011.0387.
Search in Google Scholar Back to article
Gentleman E., Fredholm Y.C., Jell G., Lotfibakhshaiesh N., O’Donnell M.D., Hill R.G. et al., The effects of strontiumsubstituted bioactive glasses on osteoblasts and osteoclasts in vitro, Biomaterials, 2010, 31, 3949–3956, DOI: 10.1016/j.biomaterials.2010.01.121.
Search in Google Scholar Back to article
Gerhardt L.C., Boccaccini A.R., Bioactive glass and glass-ceramic scaffolds for bone tissue engineering, Materials (Basel), 2010, 3, 3867–3910, DOI: 10.3390/ma3073867.
Search in Google Scholar Back to article
Gorustovich A.A., Steimetz T., Cabrini R.L., Porto López J.M., Osteoconductivity of strontium-doped bioactive glass particles: A histomorphometric study in rats, J. Biomed. Mater. Res. – Part A, 2010, 92, 232–237, DOI: 10.1002/jbm.a.32355.
Search in Google Scholar Back to article
Hajduga M.B., Bobiński R., Dutka M., Ulman-Włodarz I., Bujok J., Pająk C. et al., Analysis of the antibacterial properties of polycaprolactone modified with graphene, bioglass and zinc doped bioglass, Acta Bioeng. Biomech., 2021, 23, https://doi.org/10.37190/ABB-01766-2020-03
Search in Google Scholar Back to article
Hench L.L., Wheeler D.L., Greenspan D.C., Molecular Control of Bioactivity in Sol-Gel Glasses, J. Sol-Gel Sci. Technol., 1998, 13, 245–250, DOI: 10.1023/a:1008643303888.
Search in Google Scholar Back to article
Hesaraki S., Gholami M., Vazehrad S., Shahrabi S., 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, 2010, 30, 383–390, DOI: 10.1016/j.msec.2009.12.001.
Search in Google Scholar Back to article
Hu S., Chang J., Liu M., Ning C., Study on antibacterial effect of 45S5 Bioglass®, J. Mater. Sci. Mater. Med., 2009, 20, 281–286, DOI: 10.1007/s10856-008-3564-5.
Search in Google Scholar Back to article
Isaac J., Nohra J., Lao J., Jallot E., Nedelec J.M., Berdal A., Effects of strontium-doped bioactive glass on the differentiation of cultured osteogenic cells, Eur. Cells Mater., 2011, 21, 130–143, DOI: 10.22203/eCM.v021a11.
Search in Google Scholar Back to article
Ito A., Kawamura H., Otsuka M., Ikeuchi M., Ohgushi H., Ishikawa K. et al., Zinc-releasing calcium phosphate for stimulating bone formation, Mater. Sci. Eng. C, 2002, 22, 21–25, DOI: 10.1016/S0928-4931(02)00108-X.
Search in Google Scholar Back to article
Kargozar S., Lotfibakhshaiesh N., Ai J., Mozafari M., Brouki M.P., Hamzehlou S. et al., Strontium- and cobaltsubstituted bioactive glasses seeded with human umbilical cord perivascular cells to promote bone regeneration via enhanced osteogenic and angiogenic activities, Acta Biomater., 2017, 58,502–514, DOI: 10.1016/j.actbio.2017.06.021.
Search in Google Scholar Back to article
Kargozar S., Montazerian M., Hamzehlou S., Kim H.W., Baino F., Mesoporous bioactive glasses: Promising platforms for antibacterial strategies, Acta Biomater., 2018, 81, 1–19, DOI: 10.1016/j.actbio.2018.09.052.
Search in Google Scholar Back to article
Liu X., Ding C., Chu P.K., Mechanism of apatite formation on wollastonite coatings in simulated body fluids, Biomaterials, 2004, 25, 1755–1761, DOI: 10.1016/j.biomaterials.2003.08.024.
Search in Google Scholar Back to article
Lukito D., Xue J.M., Wang J., In vitro bioactivity assessment of 70 (wt.)%SiO2–30 (wt.)%CaO bioactive glasses in simulated body fluid, Mater. Lett., 2005, 59, 3267–3271, DOI: 10.1016/j.matlet.2005.05.055.
Search in Google Scholar Back to article
Łączka M., Cholewa-Kowalska K., Osyczka A.M., Bioactivity and osteoinductivity of glasses and glassceramics and their material determinants, Ceram. Int., 2016, 42, 14313–14325, DOI: 10.1016/j.ceramint.2016.06.077.
Search in Google Scholar Back to article
Mao L., Xia L., Chang J., Liu J., Jiang L., Wu C. et al., The synergistic effects of Sr and Si bioactive ions on osteogenesis, osteoclastogenesis and angiogenesis for osteoporotic bone regeneration, Acta Biomater., 2017, 61, 217–232, DOI: 10.1016/j.actbio.2017.08.015.
Search in Google Scholar Back to article
Moghanian A., Firoozi S., Tahriri M., Characterization, in vitro bioactivity and biological studies of sol-gel synthesized SrO substituted 58S bioactive glass, Ceram. Int., 2017, 43, 14880–14890, DOI: 10.1016/j.ceramint.2017.08.004.
Search in Google Scholar Back to article
Mulani M.S., Kamble E.E., Kumkar S.N., Tawre M.S., Pardesi K.R., Emerging Strategies to Combat ESKAPE Pathogens in the Era of Antimicrobial Resistance: A Review, Front. Microbiol., 2019, 10, DOI: 10.3389/fmicb.2019.00539.
Search in Google Scholar Back to article
Murphy S., Wren A.W., Towler M.R., Boyd D., The effect of ionic dissolution products of Ca–Sr–Na–Zn–Si bioactive glass on in vitro cytocompatibility, J. Mater. Sci. Mater. Med., 2010, 21, 2827–2834, DOI: 10.1007/s10856-010-4139-9.
Search in Google Scholar Back to article
O’Donnell M.D., Candarlioglu P.L., Miller C.A., Gentleman E., Stevens M.M., Materials characterisation and cytotoxic assessment of strontium-substituted bioactive glasses for bone regeneration, J. Mater. Chem., 2010, 20, 8934, DOI: 10.1039/c0jm01139h.
Search in Google Scholar Back to article
Pasquet J., Chevalier Y., Pelletier J., Couval E., Bouvier D., Bolzinger M.A., The contribution of zinc ions to the antimicrobial activity of zinc oxide, Colloids Surfaces A Physicochem Eng. Asp., 2014, 457, 263–274, DOI: 10.1016/j.colsurfa.2014.05.057.
Search in Google Scholar Back to article
Saino E., Grandi S., Quartarone E., Maliardi V., Galli D., Bloise N., In vitro calcified matrix deposition by human osteoblasts onto a zinc-containing bioactive glass, Eur. Cells Mater., 2011, 21, 59–72, DOI: 10.22203/eCM.v021a05.
Search in Google Scholar Back to article
Saravanapavan P., Hench L.L., Mesoporous calcium silicate glasses. I. Synthesis, J. Non. Cryst. Solids, 2003, 318, 1–13, DOI: 10.1016/S0022-3093(02)01864-1.
Search in Google Scholar Back to article
Sergi R., Bellucci D., Cannillo V., A review of bioactive glass/natural polymer composites: State of the art., Materials (Basel), 2020, 13, 1–38, DOI: 10.3390/ma13235560.
Search in Google Scholar Back to article
da Silva B.L., Abuçafy M.P., Manaia E.B., Junior J.A.O., Chiari-Andréo B.G., Pietro R.C.L.R. et al., Relationship between structure and antimicrobial activity of zinc oxide nanoparticles: An overview, Int. J. Nanomedicine, 2019, 14, 9395–9410, DOI: 10.2147/IJN.S216204.
Search in Google Scholar Back to article
Strobel L.A., Hild N., Mohn D., Stark W.J., Hoppe A., Gbureck U., Novel strontium-doped bioactive glass nanoparticles enhance proliferation and osteogenic differentiation of human bone marrow stromal cells, J. Nanoparticle Res., 2013, 15, DOI: 10.1007/s11051-013-1780-5.
Search in Google Scholar Back to article
Vaid C., Murugavel S., Das C., Asokan S., Mesoporous bioactive glass and glass-ceramics: Influence of the local structure on in vitro bioactivity, Microporous Mesoporous Mater., 2014, 186, 46–56, DOI: 10.1016/j.micromeso.2013.11.027.
Search in Google Scholar Back to article
Vukomanovic M., Gazvoda L., Anicic N., Rubert M., Suvorov D., Müller R., Multi-doped apatite: Strontium, magnesium, gallium and zinc ions synergistically affect osteogenic stimulation in human mesenchymal cells important for bone tissue engineering, Biomater. Adv., 2022, 140, 213051, DOI: 10.1016/j.bioadv.2022.213051.
Search in Google Scholar Back to article
Wu C., Ramaswamy Y., Chang J., Woods J., Chen Y., Zreiqat H., The effect of Zn contents on phase composition, chemical stability and cellular bioactivity in Zn-Ca-Si system ceramics, J. Biomed. Mater. Res. – Part B Appl. Biomater., 2008, 87, 346–53, DOI: 10.1002/jbm.b.31109.
Search in Google Scholar Back to article
Yan M., Song Y., Wong C.P., Hardin K., Ho E., Zinc deficiency alters DNA damage response genes in normal human prostate epithelial cells, J. Nutr., 2008, 138, 667–673, DOI: 10.1093/jn/138.4.667.
Search in Google Scholar Back to article
Zhang D., Hupa M., Hupa L., In situ pH within particle beds of bioactive glasses, Acta Biomater., 2008, 4, 1498–1505, DOI: 10.1016/j.actbio.2008.04.007.
Search in Google Scholar Back to article
Zheng K., Boccaccini A.R., Sol-gel processing of bioactive glass nanoparticles: A review. Adv. Colloid Interface Sci., 2017, 249, 363–373, DOI: 10.1016/j.cis.2017.03.008.
Search in Google Scholar Back to article
Zheng K., Lu M., Rutkowski B., Dai X., Yang Y., Taccardi N., ZnO quantum dots modified bioactive glass nanoparticles with pH-sensitive release of Zn ions, fluorescence, antibacterial and osteogenic properties, J. Mater. Chem. B, 2016, 4, 7936–7949, DOI: 10.1039/C6TB02053D.
Search in Google Scholar Back to article

Bioactive glasses enriched with zinc and strontium: synthesis, characterization, cytocompatibility with osteoblasts and antibacterial properties

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