Antibacterial activity and biocompatibility of titanium nickelide augments with the addition of silver nanoparticles for bone grafting: an experimental study

Cover Page

Cite item

Full Text

Abstract

BACKGROUND: The relevance of this study was supported by the increasing number of infectious complications of bone augmentation in children and adults. Currently, porous titanium nickelide alloys are among the most preferred materials used in bone plasty. Despite the observable advantages of porous nickelide titanium alloys in terms of biochemical and biomechanical compatibility with the body, research on the antibacterial activity of alloys is ongoing to counter the development of infections at the implant–biological tissue border.

AIM: To perform an experimental study of the biocompatible antibacterial surface in porous titanium nickelide alloys with the addition of silver nanoparticles.

MATERIALS AND METHODS: Titanium nickelide alloys with 62% porosity were obtained using the self-propagating high-temperature synthesis method from nickel, titanium, and nanosilver powders at concentrations of 0.2 at.% Ag, 0.5 at.% Ag, and 1.0 at.% Ag, respectively. The experiment was conducted on nine sexually mature female white laboratory rats. They were divided into three groups, with three rats each. All animals were implanted with titanium nickelide along with porous granules of silver additives. The first group was the control, the second received 0.2 at.% silver, and the third received 0.5% silver. The standard method of incubating Staphylococcus epidermidis in liquid broth in the presence of the studied images was used to determine bactericidal activity, followed by seeding on solid media and counting colonies.

RESULTS: The antibacterial effect of the samples on S. epidermidis gradually increased with increasing silver concentration. The significance of the differences between the experiment and control was confirmed by Student’s criterion p < 0.005, whereas the sample without silver nanoparticles and the control do not differ significantly. Thus, these alloys may have bioactive properties because they contain silver nanoparticles. An alloy with a silver concentration of 0.5 at.% Ag showed the best antibacterial activity to S. epidermidis. In the clinical evaluation of the results of the experimental study, purulent inflammatory complications were not observed in all animals at all times. On day 75, the animals underwent computed tomography, which showed good occupancy of the bone defect and absence of a dystrophic effect on the area where the bone and soft tissue are in contact with the material.

CONCLUSIONS: If the concentration of silver nanoparticles is increased up to 0.5 at%, the antibacterial activity and cytocompatibility of the implant also increase. Clinical experimental evaluation in all groups of animals showed that osteointegration of alloys with 0.5 at.% Ag begins immediately after implantation and is completed 2 weeks earlier than that in the remaining groups.

About the authors

Semyon A. Borisov

Ural State Medical University

Email: drborissovsa@gmail.com
ORCID iD: 0000-0002-1783-3776
SPIN-code: 5782-1443
Russian Federation, Yekaterinburg

Ivan I. Gordienko

Ural State Medical University

Author for correspondence.
Email: ivan-gordienko@mail.ru
ORCID iD: 0000-0003-3157-4579
SPIN-code: 5368-0964

MD, Cand. Sci. (Medicine)

Russian Federation, Yekaterinburg

Natalya A. Tsap

Ural State Medical University

Email: tsapna-ekat@rambler.ru
ORCID iD: 0000-0001-9050-3629
SPIN-code: 7466-8731

MD, Dr. Sci. (Medicine), Professor

Russian Federation, Yekaterinburg

Gulsharat A. Baigonakova

National Research Tomsk State University

Email: gat27@mail.ru
ORCID iD: 0000-0001-9853-2766
SPIN-code: 1192-6016

MD, Cand. Sci. (Medicine)

Russian Federation, Tomsk

Ekaterina S. Marchenko

National Research Tomsk State University

Email: 89138641814@mail.ru
ORCID iD: 0000-0003-4615-5270
SPIN-code: 7116-2901

Dr. Sci. (Physics and Mathematics)

Russian Federation, Tomsk

Victor A. Larikov

National Research Tomsk State University

Email: calibra1995@gmail.com
ORCID iD: 0009-0002-3365-5997
Russian Federation, Tomsk

References

  1. Bozic KJ, Ries MD. The impact of infection after total hip arthroplasty on hospital and surgeon resource utilization. J Bone Joint Surg Am. 2005;87(8):1746–1751. doi: 10.2106/JBJS.D.02937
  2. Khon VE, Zagorodniy NV, Komlev VS, et al. Nfluence of the degree of calcium substitution by argentum in tricalcium phosphate on its biological properties in vitro. N.N. Priorov journal of traumatology and orthopedics. 2013;20(4):23–28. EDN: RTKACB
  3. Czyzewski K, Galazka P, Zalas-Wiecek P, et al. Infectious complications in children with malignant bone tumors: a multicenter nationwide study. Infect Drug Resist. 2019;30(12):1471–1480. doi: 10.2147/IDR.S199657
  4. Lake J, Gordon O. Implant-associated spinal infections in children: how can we improvediagnosis and management? Infect Dis Clin North Am. 2022;36(1):101–123. doi: 10.1016/j.idc.2021.11.005
  5. Yasenchuk YuF, Gyunter SV, Marchenko ES, Iuzhakov MM. Biocompatibility of porous SHS-TiNi. Mater Sci Forum. 2019;970(12):320–327. doi: 10.4028/ href='www.scientific.net/MSF.970.320' target='_blank'>www.scientific.net/MSF.970.320
  6. Topolnitskiy E, Chekalkin T, Marchenko E, et al. Evaluation of clinical performance of TiNi-based implants used in chest wall repair after resection for malignant tumors. J Funct Biomater. 2021;12(4):60–71. doi: 10.3390/jfb12040060
  7. Sevilla P, Aparicio C, Planell JA, Gil FJ. Comparison of the mechanical properties between tantalum and nickel-titanium foams implant materials for bone ingrowth applications. J Alloys Compd. 2007;439(1-2):67–73. doi: 10.1016/j.jallcom.2006.08.069
  8. Hornbogen E. Microstructure and thermo-mechanical properties of NiTi shape memory alloys. Mater Sci Forum. 2004;455(2):335–341. doi: 10.4028/ href='www.scientific.net/MSF.455-456.335' target='_blank'>www.scientific.net/MSF.455-456.335
  9. Marchenko ES, Luchsheva V, Baigonakova GA, et al. Functionalization of the surface of porous nickel-titanium alloy with macrocyclic compounds. Materials. 2022;16(1):66–78. doi: 10.3390/ma16010066
  10. Marchenko ES, Baigonakova GA, Yasenchuk YF, et al. Structure, biocompatibility and corrosion resistance of the ceramic-metal surface of porous nitinol. Ceram Int. 2022;48(22):33514–33523. doi: 10.1016/j.ceramint.2022.07.296
  11. Oh K-T, Joo U-H, Park G-H, et al. Effect of silver addition on the properties of nickel-titanium alloys for dental application. J Biomed Mater. 2006;76B(12):306–314. doi: 10.1002/jbm.b.30369
  12. Zhao L, Chu PK, Zhang Y, Wu Z. Antibacterial coatings on titanium implants. J Biomed Mater Res. 2009;91(1):470–480. doi: 10.1002/jbm.b.31463
  13. Chouirfa H, Bouloussa H, Migonney V, Falentin-Daudré C. Review of titanium surface modification techniques and coatings for antibacterial applications. Acta biomaterialia. 2019;83(1):37–54. doi: 10.1016/j.actbio.2018.10.036
  14. Ferraris S, Spriano S. Antibacterial titanium surfaces for medical implants. Mater Sci Eng. 2016;61(2):965–978. doi: 10.1016/j.msec.2015.12.062
  15. Schmidt-Braekling T, Streitbuerger A, Gosheger G, et al. Silver-coated megaprostheses: review of the literature. Eur J Orthop Surg Traumatol. 2017;27(4):483–489. doi: 10.1007/s00590-017-1933-9
  16. Liu X, Gan K, Liu H, et al. Antibacterial properties of nano-silver coated PEEK prepared through magnetron sputtering. Dent Mater. 2017;33(9):348–360. doi: 10.1016/j.dental.2017.06.014
  17. Kim JS, Kuk E, Yu KN, et al. Antimicrobial effects of silver nanoparticles. Nanomedicine, nanotechnology, biology, and medicine. 2007;3(1):95–101. doi: 10.1016/j.nano.2006.12.001
  18. Aurore V, Caldana F, Blanchard M, et al. Silver-nanoparticles increase bactericidal activity and radical oxygen responses against bacterial pathogens in human osteoclasts. Nanomedicine. 2018;14(2):601–607. doi: 10.1016/j.nano.2017.11.006
  19. Praba VL, Kathirvel M, Vallayyachari K, et al Bactericidal effect of silver nanoparticles against mycobacterium tuberculosis. J Bionanosci. 2013;7(3):282–287. doi: 10.1166/jbns.2013.1138
  20. Van Dong P, Ha CH, Binh LT, et al. Chemical synthesis and antibacterial activity of novel-shaped silver nanoparticles. Int Nano Lett. 2012;2(2):9–18. doi: 10.1186/2228-5326-2-9
  21. Thangavel E, Dhandapani VS, Dharmalingam K, et al. RF magnetron sputtering mediated NiTi/Ag coating on Ti-alloy substrate with enhanced biocompatibility and durability. Mater Sci Eng. 2019;99(4):304–314. doi: 10.1016/j.msec.2019.01.099
  22. Martinez-Gutierrez F, Olive PL, Banuelos A, et al. Synthesis, characterization, and evaluation of antimicrobial and cytotoxic effect of silver and titanium nanoparticles. Nanomedicine: nanotechnology, biology, and medicine. 2010;6(5):681–688. doi: 10.1016/j.nano.2010.02.001
  23. Albers CE, Hofstetter W, Siebenrock KA, et al. In vitro cytotoxicity of silver nanoparticles on osteoblasts and osteoclasts at antibacterial concentrations. Nanotoxicology. 2013;7(1):30–36. doi: 10.3109/17435390.2011.626538
  24. Marchenko ES, Baigonakova GA, Kokorev OV, et al. Phase equilibrium, structure, mechanical and biocompatible properties of TiNi-based alloy with silver. Mater. Res. Express. 2019;6(6):1–11. doi: 10.1088/2053-1591/ab0edd
  25. Pauksch L, Rohnke M, Schnettler R, Lips KS. Silver nanoparticles do not alter human osteoclastogenesis but induce cellular uptake. Toxicol Rep. 2014;1(1):900–908. doi: 10.1016/j.toxrep.2014.10.012
  26. Goodman SB, Yao Z, Keeney M, Yang F. The future of biologic coatings for orthopaedic implants. Biomaterials. 2013;34(13):3174–3183. doi: 10.1016/j.biomaterials.2013.01.074
  27. Marchenko E, Baigonakova G, Larikov V, et al. Structure and mechanical properties of porous TiNi alloys with Ag nanoparticles. Coatings. 2023;13(1):24–37. doi: 10.3390/coatings13010024
  28. Boudreau MD, Imam MS, Paredes AM, et al. Differential effects of silver nanoparticles and silver ions on tissue accumulation, distribution, and toxicity in the sprague dawley rat following daily oral gavage administration for 13 weeks. Toxicol Sci. 2016;150(1):131–160. doi: 10.1093/toxsci/kfv318
  29. Guo H, Zhang J, Boudreau M, et al. Intravenous administration of silver nanoparticles causes organ toxicity through intracellular ROS-related loss of inter-endothelial junction. Part Fibre Toxicol. 2016;13(3):21–33. doi: 10.1186/s12989-016-0133-99

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Fig. 1. Antibacterial activity against S. epidermidis: a, vertical value expressed in CFU; b, examples of inoculations on solid agar

Download (94KB)
Indexing metadata
3. Fig. 2. Raster image of the surface after cultivation of samples of porous alloys: a — TiNi; b — TiNi + 0.2 at.% Ag; c —TiNi + 0.5 at.% Ag

Download (245KB)
Indexing metadata
4. Fig. 3. Quantitative analysis of cell viability on the surface of samples of porous TiNi alloys

Download (74KB)
Indexing metadata
5. Fig. 4. Computed tomography. Sagittal scan of a laboratory rat. Selected material installed in the medullary canal of the femur 75 days from implantation

Download (80KB)
Indexing metadata
6. Fig. 5. Computed tomography. Three-dimensional image of a laboratory rat. The implantation site in the bone and surrounding soft tissues is highlighted; image was taken 75 days after implantation

Download (177KB)
Indexing metadata
7. Fig. 6. Distribution of silver in a TiNi + 0.5 at.% Ag sample: a — TEM image and electron microdiffraction pattern of Ag; b–e — STEM-EDS elemental mapping*. *STEM — Scanning transmission electron microscopy; EDS — Energy dispersive spectroscopy

Download (258KB)
Indexing metadata

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies