Effect of Gold Nanoparticles and Silicon on the Bioactivity and Antibacterial Properties of Hydroxyapatite/Chitosan/Tricalcium Phosphate-Based Biomicroconcretes
Abstract
:1. Introduction
2. Materials
2.1. Hybrid Hydroxyapatite-Chitosan Granules (HA/CTS)
2.2. Hybrid HA/CTS Granules Modified with Gold Nanoparticles (AuNPs-HA/CTS)
2.3. α-Tricalcium Phosphate and Silicon Modified αTCP Powders
2.4. Hydroxyapatite/Chitosan/Tricalcium Phosphate-Based Biomicroconcretes
3. Methods
3.1. Chemical and Phase Composition
3.2. Setting Times
3.3. Compressive Strength
3.4. Microstructure
3.5. Chemical Stability and Bioactivity In Vitro
3.6. In Vitro Antibacterial Activity
3.6.1. Microorganisms and Culture Conditions
3.6.2. Antibacterial Activity Test
3.6.3. Statistics
4. Results and Discussion
4.1. Chemical and Phase Composition
4.2. Setting Times
4.3. Compressive Strength
4.4. Microstructure
4.5. Chemical Stability and In Vitro Bioactivity
4.6. In Vitro Antibacterial Activity
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Yousefi, A.M. A review of calcium phosphate cements and acrylic bone cements as injectable materials for bone repair and implant fixation. J. Appl. Biomater. Funct. Mater. 2019, 17, 2280800019872594. [Google Scholar] [CrossRef] [PubMed]
- Lee, H.J.; Kim, B.; Padalhin, A.R.; Lee, B.T. Incorporation of chitosan-alginate complex into injectable calcium phosphate cement system as a bone graft material. Mater. Sci. Eng. C 2019, 94, 385–392. [Google Scholar] [CrossRef]
- Meng, D.; Dong, L.; Yuan, Y.; Jiang, Q. In vitro and in vivo analysis of the biocompatibility of two novel and injectable calcium phosphate cements. Regen. Biomater. 2019, 6, 13–19. [Google Scholar] [CrossRef] [Green Version]
- Vorndran, E.; Geffers, M.; Ewald, A.; Lemm, M.; Nies, B.; Gbureck, U. Ready-to-use injectable calcium phosphate bone cement paste as drug carrier. Acta Biomater. 2013, 9, 9558–9567. [Google Scholar] [CrossRef]
- Wu, T.; Shi, H.; Liang, Y.; Lu, T.; Lin, Z.; Ye, J. Improving osteogenesis of calcium phosphate bone cement by incorporating with manganese doped β-tricalcium phosphate. Mater. Sci. Eng. C 2020, 109, 110481. [Google Scholar] [CrossRef]
- Hasan, M.L.; Kim, B.; Padalhin, A.R.; Faruq, O.; Sultana, T.; Lee, B.T. In vitro and in vivo evaluation of bioglass microspheres incorporated brushite cement for bone regeneration. Mater. Sci. Eng. C 2019, 103, 109775. [Google Scholar] [CrossRef] [PubMed]
- Dziadek, M.; Zima, A.; Cichoń, E.; Czechowska, J.; Ślósarczyk, A. Biomicroconcretes based on the hybrid HAp/CTS granules, α-TCP and pectins as a novel injectable bone substitutes. Mater. Lett. 2020, 265, 127457. [Google Scholar] [CrossRef]
- Zima, A.; Czechowska, J.; Szponder, T.; Ślósarczyk, A. In vivo behavior of biomicroconcretes based on α-tricalcium phosphate and hybrid hydroxyapatite/chitosan granules and sodium alginate. J. Biomed. Mater. Res. Part A 2020, 108, 1243–1255. [Google Scholar] [CrossRef] [PubMed]
- Czechowska, J.; Zima, A.; Ślósarczyk, A. Comparative study on physicochemical properties of alpha-TCP/calcium sulphate dihydrate biomicroconcretes containing chitosan, sodium alginate or methylcellulose. Acta Bioeng. Biomech. 2020, 22, 47–56. [Google Scholar] [CrossRef]
- Amirian, J.; Makkar, P.; Lee, G.H.; Paul, K.; Lee, B.T. Incorporation of alginate-hyaluronic acid microbeads in injectable calcium phosphate cement for improved bone regeneration. Mater. Lett. 2020, 272, 127830. [Google Scholar] [CrossRef]
- Liang, W.; Gao, M.; Lou, J.; Bai, Y.; Zhang, J.; Lu, T.; Sun, X.; Ye, J.; Li, B.; Sun, L.; et al. Integrating silicon/zinc dual elements with PLGA microspheres in calcium phosphate cement scaffolds synergistically enhances bone regeneration. J. Mater. Chem. B 2020, 8, 3038–3049. [Google Scholar] [CrossRef]
- Qian, G.; Lu, T.; Zhang, J.; Liu, R.; Wang, Z.; Yu, B.; Li, H.; Shi, H.; Ye, J. Promoting bone regeneration of calcium phosphate cement by addition of PLGA microspheres and zinc silicate via synergistic effect of in-situ pore generation, bioactive ion stimulation and macrophage immunomodulation. Appl. Mater. Today 2020, 19, 100615. [Google Scholar] [CrossRef]
- Wu, S.; Lei, L.; Bao, C.; Liu, J.; Weir, M.D.; Ren, K.; Schneider, A.; Oates, T.W.; Liu, J.; Xu, H.H. An injectable and antibacterial calcium phosphate scaffold inhibiting Staphylococcus aureus and supporting stem cells for bone regeneration. Mater. Sci. Eng. C 2020, 111688. [Google Scholar] [CrossRef] [PubMed]
- Liao, J.; Shi, K.; Jia, Y.; Wu, Y.; Qian, Z. Gold nanorods and nanohydroxyapatite hybrid hydrogel for preventing bone tumor recurrence via postoperative photothermal therapy and bone regeneration promotion. Bioact. Mater. 2021, 6, 2221–2230. [Google Scholar] [CrossRef] [PubMed]
- Rau, J.V.; Fosca, M.; Graziani, V.; Egorov, A.A.; Zobkov, Y.V.; Fedotov, A.Y.; Ortenzi, M.; Caminiti, R.; Baranchikov, A.E.; Komlev, V.S. Silver-doped calcium phosphate bone cements with antibacterial properties. J. Funct. Biomater. 2016, 7, 10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gomes, S.; Vichery, C.; Descamps, S.; Martinez, H.; Kaur, A.; Jacobs, A.; Nedelec, J.M.; Renaudin, G. Cu-doping of calcium phosphate bioceramics: From mechanism to the control of cytotoxicity. Acta Biomater. 2018, 65, 462–474. [Google Scholar] [CrossRef] [PubMed]
- Xia, Y.; Chen, H.; Zhang, F.; Bao, C.; Weir, M.D.; Reynolds, M.A.; Ma, J.; Gu, N.; Xu, H.H. Gold nanoparticles in injectable calcium phosphate cement enhance osteogenic differentiation of human dental pulp stem cells. Nanomed. Nanotechnol. Biol. Med. 2018, 14, 35–45. [Google Scholar] [CrossRef]
- Wekwejt, M.; Michno, A.; Truchan, K.; Pałubicka, A.; Świeczko-Żurek, B.; Osyczka, A.M.; Zieliński, A. Antibacterial activity and cytocompatibility of bone cement enriched with antibiotic, nanosilver, and nanocopper for bone regeneration. Nanomaterials 2019, 9, 1114. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kurtjak, M.; Vukomanović, M.; Suvorov, D. Antibacterial nanocomposite of functionalized nanogold and gallium-doped hydroxyapatite. Mater. Lett. 2017, 193, 126–129. [Google Scholar] [CrossRef]
- Zima, A. Hydroxyapatite-chitosan based bioactive hybrid biomaterials with improved mechanical strength. Spectrochim. Acta Part A Mol. Biomol. Spectrosc. 2018, 193, 175–184. [Google Scholar] [CrossRef]
- Sánchez-López, E.; Gomes, D.; Esteruelas, G.; Bonilla, L.; Lopez-Machado, A.L.; Galindo, R.; Cano, A.; Espina, M.; Ettcheto, M.; Camins, A.; et al. Metal-based nanoparticles as antimicrobial agents: An overview. Nanomaterials 2020, 10, 292. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, L.; Hu, C.; Shao, L. The antimicrobial activity of nanoparticles: Present situation and prospects for the future. Int. J. Nanomed. 2017, 12, 1227. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mróz, W.; Bombalska, A.; Burdyńska, S.; Jedyński, M.; Prokopiuk, A.; Budner, B.; Ślósarczyk, A.; Zima, A.; Menaszek, E.; Ścisłowska-Czarnecka, A.; et al. Structural studies of magnesium doped hydroxyapatite coatings after osteoblast culture. J. Mol. Struct. 2010, 977, 145–152. [Google Scholar] [CrossRef]
- Cruz, R.; Calasans-Maia, J.; Sartoretto, S.; Moraschini, V.; Rossi, A.M.; Louro, R.S.; Granjeiro, J.M.; Calasans-Maia, M.D. Does the incorporation of zinc into calcium phosphate improve bone repair? A systematic review. Ceram. Int. 2018, 44, 1240–1249. [Google Scholar] [CrossRef]
- Shi, H.; Zeng, S.; Liu, X.; Yu, T.; Zhou, C. Effects of strontium doping on the degradation and Sr ion release behaviors of α-tricalcium phosphate bone cement. J. Am. Ceram. Soc. 2018, 101, 502–508. [Google Scholar] [CrossRef]
- Knabe, C.; Lopez Heredia, M.; Barnemitz, D.; Genzel, A.; Peters, F.; Hübner, W.D. Effect of Silicon-Doped Calcium Phosphate Bone Substitutes On Bone Formation And Osteoblastic Phenotype Expression In Vivo. In Key Engineering Materials; Trans Tech Publications Ltd.: Freienbach, Switzerland, 2014; Volume 614, pp. 31–34. [Google Scholar]
- Kermani, F.; Gharavian, A.; Mollazadeh, S.; Kargozar, S.; Youssefi, A.; Khaki, J.V. Silicon-doped calcium phosphates; the critical effect of synthesis routes on the biological performance. Mater. Sci. Eng. C 2020, 111, 110828. [Google Scholar] [CrossRef]
- Marcacci, M.; Kon, E.; Zaffagnini, S.; Giardino, R.; Rocca, M.; Corsi, A.; Benvenuti, A.; Bianco, P.; Quarto, R.; Martin, I.; et al. Reconstruction of extensive long bone defects in sheep using resorbable bioceramics based on silicon stabilized tricalcium phosphate. Tissue Eng. 2006, 12, 1261–1273. [Google Scholar]
- Langstaff, S.; Sayer, M.; Smith, T.J.N.; Pugh, S.M. Resorbable bioceramics based on stabilized calcium phosphates. Part II: Evaluation of biological response. Biomaterials 2001, 22, 135–150. [Google Scholar] [CrossRef]
- ASTM C266-20, Standard test method for time setting of hydraulic-cement paste by gillmore needles. In ASTM Annual Book of Standards; American Society for Testing and Mate Rials: West Conshohocken, PA, USA, 2020.
- Kokubo, T.; Takadama, H. How useful is SBF in predicting in vivo bone bioactivity? Biomaterials 2006, 27, 2907–2915. [Google Scholar] [CrossRef]
- Reid, J.W.; Pietak, A.; Sayer, M.; Dunfield, D.; Smith, T.J.N. Phase formation and evolution in the silicon substituted tricalcium phosphate/apatite system. Biomaterials 2005, 26, 2887–2897. [Google Scholar] [CrossRef]
- Szurkowska, K.; Szeleszczuk, Ł.; Kolmas, J. Effects of Synthesis Conditions on the Formation of Si-Substituted Alpha Tricalcium Phosphates. Int. J. Mol. Sci. 2020, 21, 9164. [Google Scholar] [CrossRef]
- Martínez, I.M.; Velásquez, P.; De Aza, P.N. The Sub-System α-TCP ss-Silicocarnotite Within the Binary System Ca3 (PO4) 2–Ca2SiO4. J. Am. Ceram. Soc. 2012, 95, 1112–1117. [Google Scholar]
- ISO/DIS 18531(en) Implants for surgery—Calcium phosphate bioceramics—Characterization of hardening bone paste materials.
- Wei, X.; Ugurlu, O.; Ankit, A.; Acar, H.Y.; Akinc, M. Dissolution behavior of Si, Zn-codoped tricalcium phosphates. Mater. Sci. Eng. C 2009, 29, 126–135. [Google Scholar] [CrossRef]
- Mestres, G.; Le Van, C.; Ginebra, M.P. Silicon-stabilized α-tricalcium phosphate and its use in a calcium phosphate cement: Characterization and cell response. Acta Biomater. 2012, 8, 1169–1179. [Google Scholar] [CrossRef]
- Czechowska, J.; Zima, A.; Siek, D.; Ślósarczyk, A. Influence of sodium alginate and methylcellulose on hydrolysis and physicochemical properties of α-TCP based materials. Ceram. Int. 2018, 44, 6533–6540. [Google Scholar] [CrossRef]
- Tsai, G.J.; Su, W.H. Antibacterial activity of shrimp chitosan against Escherichia coli. J. Food Prot. 1999, 62, 239–243. [Google Scholar] [CrossRef]
- Young, D.H.; Kauss, H. Release of calcium from suspension-cultured Glycine max cells by chitosan, other polycations, and polyamines in relation to effects on membrane permeability. Plant Physiol. 1983, 73, 698–702. [Google Scholar] [CrossRef] [Green Version]
- Santos, R.L.O.D.; Gamarra, J.G.A.; Lincopan, N.; Petri, D.F.S.; Paula, C.R.; Coto, N.P.; Dias, R.B. Production of Medical Grade Silicone for Facial Prosthesis with Bactericidal Properties from the Inclusion of Poly (Diallyldimethylammonium Chloride): An in Vitro Study. Pesqui. Bras. Em Odontopediatria E Clínica Integr. 2019, 19. [Google Scholar] [CrossRef]
- Tajima, M. The effect of silicon on the growth of Staphylococcus aureus. Nippon Jibiinkoka Gakkai Kaiho 1990, 93, 630–639. [Google Scholar] [CrossRef] [Green Version]
- Cui, Y.; Zhao, Y.; Tian, Y.; Zhang, W.; Lü, X.; Jiang, X. The molecular mechanism of action of bactericidal gold nanoparticles on Escherichia coli. Biomaterials 2012, 33, 2327–2333. [Google Scholar] [CrossRef]
- Zhang, Y.; Shareena Dasari, T.P.; Deng, H.; Yu, H. Antimicrobial activity of gold nanoparticles and ionic gold. J. Environ. Sci. Health 2015 Part C 2015, 33, 286–327. [Google Scholar] [CrossRef] [PubMed]
- Kavanagh, N.; Ryan, E.J.; Widaa, A.; Sexton, G.; Fennell, J.; O’rourke, S.; Cahill, K.C.; Kearney, C.J.; O’brien, F.J.; Kerrigan, S.W. Staphylococcal osteomyelitis: Disease progression, treatment challenges, and future directions. Clin. Microbiol. Rev. 2018, 31, e00084-17. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Crémet, L.; Broquet, A.; Brulin, B.; Jacqueline, C.; Dauvergne, S.; Brion, R.; Asehnoune, K.; Corvec, S.; Heymann, D.; Caroff, N. Pathogenic potential of Escherichia coli clinical strains from orthopedic implant infections towards human osteoblastic cells. Pathog. Dis. 2015, 73. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Material | Solid Phase | Liquid Phase | L/P (g/g) | |
---|---|---|---|---|
Granules (40 wt.%) | Powder (60 wt.%) | |||
HT | HA/CTS | αTCP | 0.75 wt.% methylcellulose in 2.0 wt.% Na2HPO4 | 0.6 |
Au-HT | Au-HA/CST | αTCP | ||
Au, Si-HT | Au-HA/CST | Si-αTCP |
Material | αTCP (wt.%) | HA (wt.%) | |
---|---|---|---|
Powders | αTCP initial | 98 ± 2 | 2 ± 2 |
Si-αTCP initial | 97 ± 1 | 3 ± 1 | |
Granules | HAp/CTS | - | 100 ± 0 |
Au-HAp/CTS | - | 100 ± 0 | |
Biomicroconcretes | HT | 54 ± 4 | 46 ± 4 |
Au-HT | 62 ± 2 | 38 ± 2 | |
Au, Si-HT | 62 ± 2 | 38 ± 2 |
Material | Setting Time (min) | |
---|---|---|
Initial | Final | |
HT | 7 ± 1 | 20 ± 1 |
Au-HT | 6 ± 1 | 16 ± 1 |
Au, Si-HT | 5 ± 1 | 10 ± 1 |
Strain | Material | ||
---|---|---|---|
HT | Au-HT | Au, Si-HT | |
S. aureus | 98.2 | 100 | 94.5 |
S. epidermidis | 85.6 | 99.4 | 100 |
E. coli | 100 | 100 | 100 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Czechowska, J.; Cichoń, E.; Belcarz, A.; Ślósarczyk, A.; Zima, A. Effect of Gold Nanoparticles and Silicon on the Bioactivity and Antibacterial Properties of Hydroxyapatite/Chitosan/Tricalcium Phosphate-Based Biomicroconcretes. Materials 2021, 14, 3854. https://doi.org/10.3390/ma14143854
Czechowska J, Cichoń E, Belcarz A, Ślósarczyk A, Zima A. Effect of Gold Nanoparticles and Silicon on the Bioactivity and Antibacterial Properties of Hydroxyapatite/Chitosan/Tricalcium Phosphate-Based Biomicroconcretes. Materials. 2021; 14(14):3854. https://doi.org/10.3390/ma14143854
Chicago/Turabian StyleCzechowska, Joanna, Ewelina Cichoń, Anna Belcarz, Anna Ślósarczyk, and Aneta Zima. 2021. "Effect of Gold Nanoparticles and Silicon on the Bioactivity and Antibacterial Properties of Hydroxyapatite/Chitosan/Tricalcium Phosphate-Based Biomicroconcretes" Materials 14, no. 14: 3854. https://doi.org/10.3390/ma14143854