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Cytotoxicity and antibacterial efficacy of silver deposited onto titanium plates by low-energy ion implantation

  • Tatiana P. Soares (a1), Charlene S.C. Garcia (a2), Mariana Roesch-Ely (a2), Marcelo E.H. Maia da Costa (a3), Marcelo Giovanela (a1) and Cesar Aguzzoli (a1)...


Contamination by bacterial biofilms has a strong negative impact, especially on the surface of prostheses, implants, pins, and other medical-surgical devices. To prevent their formation, one of the alternatives is the modification of the metal surface incorporating silver by low-energy ion implantation, thus avoiding initial bacteria adhesion to the modified surface and further development of the biofilm. The bactericidal properties of silver atoms incorporated on commercially pure titanium surfaces by low-energy ion implantation (4 keV) were evaluated. The surface modifications were analyzed by Rutherford backscattering spectrometry, glow discharge-optical emission spectroscopy, contact angle measure, optical profilometry, and X-ray photoelectron spectroscopy. The microbiological assays were conducted by using Escherichia coli (E. coli). The results demonstrated a reduction on bacterial counting. No toxic effect of silver was detected on human MG-63 cells. The choice of parameters to obtain a bactericidal and nontoxic biomaterial for human cells should consider the ideal combination “energy + silver concentration”. Therefore, it can be considered for industrial application.


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1.Liu, X., Chu, P.K., and Ding, C.: Surface modification of titanium, titanium alloys, and related materials for biomedical application. Mater. Sci. Eng., R 47, 49 (2004).
2.Topolski, K., Bochniak, W., Lagoda, M., Ostachowski, P., and Garbacz, H.: Structure and properties of titanium produced by a new method of chip recycling. J. Mater. Process Technol. 248, 80 (2017).
3.Oldani, C. and Dominguez, A.: Titanium as a biomaterial for implants. In Recent Advances in Arthroplasty, Fokter, S.K., ed. (InTech, London, U.K., 2012); pp. 149162. Available at:
4.Zhu, C., Bao, N-R., Chen, S., and Zhao, J-N.: Antimicrobial design of titanium surface that kill sessile bacteria but support stem cells adhesion. Appl. Surf. Sci. 389, 7 (2016).
5.Feng, H., Wu, J., Chen, G.Q., Cuiz, F.Z., Kim, T.N., and Kim, J.O.: A mechanistic study of the antibacterial effect of silver ions on Escherichia coli and Staphylococcus aureus. J. Biomed. Mater. Res. 52, 662 (2000).
6.Wan, Y.Z., Raman, S., Hea, F., and Huang, Y.: Surface modification of medical metals by ion implantation of silver and copper. Vacuum 81, 1114 (2007).
7.Kurtz, S.M., Lau, E., Watsom, H., Schmier, J.K., and Parvizi, J.: Economic burden of periprosthetic joint infection in the United States. J. Arthroplasty 27, 61 (2012).
8.Inman, R.D., Gallegos, K.V., Brause, B.D., Redecha, P.B., and Christian, C.L.: Clinical and microbial features of prosthetic joint infection. Am. J. Med. 77, 47 (1984).
9.Zmistowski, B., Karam, J.A., Durinka, J.B., Casper, D.S., and Parvizi, J.: Periprosthetic joint infection increases the risk of one-year mortality. J. Bone Jt. Surg. 95, 2177 (2013).
10.Lentino, J.R.: Prosthetic joint infections: Bane of orthopedists, challenge for infectious disease specialists. Clin. Infect. Dis. 36, 1157 (2003).
11.Brady, M.J., Lisay, C.M., Yurkovetskiy, A.V., and Sawan, S.P.: Persistent silver disinfectant for the environmental control of pathogenic bacteria. Am. J. Infect. Control. 31, 208 (2003).
12.Ferrara, M.S., Courson, R., and Paulson, D.S.: Evaluation of persistent antimicrobial effects of an antimicrobial formulation. J. Athl. Train. 46, 629 (2011).
13.Liu, J., Sonshine, D.A., Shervani, S., and Hurt, R.H.: Controlled release of biologically active silver from nanosilver surfaces. ACS Nano 4, 6903 (2010).
14.Dunn, K. and Edwards-Jones, V.: The role of Acticoat™ with nanocrystalline silver in the management of burns. Burns 30, S1 (2004).
15.Zarpelon, F., Galiotto, D., Aguzzoli, C., Carli, L.N., Figueroa, C.A., Baumvol, I.J.R., Machado, G., Crespo, J.S., and Giovanela, M.: Removal of coliform bacteria from industrial wastewaters using polyelectrolytes/silver nanoparticles self-assembled thin films. J. Environ. Chem. Eng. 4, 137 (2016).
16.Wang, G., Jin, W., Qasim, A.M., Gao, A., Peng, X., Li, W., Feng, H., and Chu, P.K.: Antibacterial effects of titanium embedded with silver nanoparticles based on electron-transfer-induced reactive oxygen species. Biomaterials 124, 25 (2017).
17.Ballottin, D., Fulaz, S., Cabrini, F., Tsukamoto, J., Durán, N., Alves, O.L., and Tasic, L.: Antimicrobial textiles: Biogenic silver nanoparticles against Candida and Xanthomonas. Mater. Sci. Eng., C 75, 582 (2017).
18.Boateng, J. and Matthews, K.: Wound healing dressings and drug delivery systems: A review. J. Pharm. Sci. 97, 2892 (2008).
19.Innes, M.E., Umraw, N., Fish, J.S., Gomez, M., and Cartotto, R.C.: The use of silver coated dressings on donor site wounds: A prospective, controlled matched pair study. Burns 27, 621 (2001).
20.Saint, S., Elmore, J.G., Sullivan, S.D., Emerson, S.S., and Koepsell, T.D.: The efficacy of silver alloy-coated urinary catheters in preventing urinary tract infection: A meta-analysis. Am. J. Med. 105, 236 (1998).
21.Perelshtein, I., Applerot, G., Perkas, N., Wehrschuetz-Sigl, E., Hasmann, A., Guebitz, G., and Gedanken, A.: CuO–cotton nanocomposite: Formation, morphology, and antibacterial activity. Surf. Coat. Technol. 204, 54 (2009).
22.Knetsch, M.L.W. and Koole, L.H.: New strategies in the sevelopment of sntimicrobial coatings: The example of increasing usage of silver and silver nanoparticles. Polymers 3, 340 (2011).
23.Liao, K-H., Ou, K-L., Cheng, H-C., Lin, C-T., and Peng, P-W.: Effect of silver on antibacterial properties of stainless steel. Appl. Surf. Sci. 256, 3642 (2010).
24.Lemire, J.A., Harrison, J.J., and Turner, R.J.: Antimicrobial activity of metals: Mechanisms, molecular targets and applications. Nat. Rev. Microbiol. 11, 371 (2013).
25.Politano, A.D., Campbell, K.T., Rosenberger, L.H., and Sawyer, R.G.: Use of silver in the prevention and treatment of infections: Silver review. Surg. Infect. 14, 8 (2013).
26.Sioshansi, P. and Tobin, E.J.: Surface treatment of biomaterials by ion beam processes. Surf. Coat. Technol. 83, 175 (1996).
27.Hirvonen, J.K.: Ion beam processing for industrial applications. Mater. Sci. Eng., A 116, 167 (1989).
28.Pezzagna, S. and Meijer, J.: High-resolution ion implantation from keV to MeV. In Ion Implantation, Goorsky, M., ed. (Rubion, Ruhr-Universität Bochum, London, U.K., 2012); pp. 324.
29.Poon, V.K. and Burd, A.: In vitro cytotoxicity of silver: Implication for clinical wound care. Burns 30, 140 (2004).
30.Wataha, J.C., Lockwood, P.E., and Schedle, A.: Effect of silver, copper, mercury, and nickel ions on cellular proliferation during extended, low-dose exposures. J. Biomed. Mater. Res. 52, 360 (2000).
31.Zhang, T., Wang, L., Chen, Q., and Chen, C.: Cytotoxic potential of silver nanoparticles. Yonsei Med. J. 55, 283 (2014).
32.Echeverrigaray, F.G., Echeverrigaray, S., Delamare, A.P.L., Wanke, C.H., Figueroa, C.A., Baumvol, I.J.R., and Aguzzoli, C.: Antibacterial properties obtained by low-energy silver implantation in stainless steel surfaces. Surf. Coat. Technol. 307, 345 (2016).
33.ASTM F 67: Standard Specification for Unalloyed Titanium for Surgical Implant Applications (ASTM International, West Conshohocken, Pennsylvania, 2006).
34.Duraccio, D., Mussano, F., and Faga, M.G.: Biomaterials for dental implants: Current and future trends. J. Mater. Sci. 50, 4779 (2015).
35.Ziegler, J.P., Ziegler, M.D., and Biersack, J.P.: The Program Stopping and Range of Ion in Matter (SRIM) 2013 Pro, 2018. Available at:
36.Strnad, G., Petrovan, C., and Russu, O.: Contact angle measurement on medical implant titanium based biomaterials. Proc. Technol. 22, 946 (2016).
37.Zeraik, A.N. and Nitschke, M.: Biosurfactants as agents to reduce adhesion of pathogenic bacteria to polystyrene surfaces: Effect of temperature and hydrophobicity. Curr. Microbiol. 61, 554 (2010).
38.Zareidoost, A., Yousefpour, M., Ghaseme, B., and Amanzadeh, A.: The relationship of surface roughness and cell response of chemical surface modification of titanium. J. Mater. Sci.: Mater. Med. 23, 1479 (2012).
39.Gadelmawla, E.S., Koura, M.M., Maksoud, T.M.A., Elewa, I.M., and Soliman, H.H.: Roughness parameters. J. Mater. Process. Technol. 123, 133 (2002).
40.Calderon, V.S., Cavaleiro, A., and Carvalho, S.: Chemical and structural characterization of ZrCNAg coatings: XPS, XRD, and Raman spectroscopy. Appl. Surf. Sci. 346, 240 (2015).
41.Ni, H-W., Zhang, H-S., Chen, R-S., Zhan, W-T., Huo, K-F., and Zuo, Z-Y.: Antibacterial properties and corrosion resistance of AISI 420 stainless steels implanted by silver and copper ions. Int. J. Miner., Metall. Mater. 19, 322 (2012).
42.Benzo, P., Cattaneo, L., Farcau, C., Andreozzi, A., Perego, M., Benassayag, G., Pécassou, B., Carles, R., and Bonafos, C.: Stability of Ag nanocrystals synthesized by ultra-low energy ion implantation in SiO2 matrices. J. Appl. Phys. 109, 103524 (2011).
43.Rai, M., Yadav, A., and Gade, A.: Silver nanoparticles as a new generation of antimicrobials. Biotechnol. Adv. 27, 76 (2009).
44.Fontenoy, C. and Kamel, S.O.: Silver in the medical devices/equipaments: Marketing or real clinical interest? Pharm. Hosp. 46, e1 (2011).
45.Chang, H-I. and Wang, Y.: Cell responses to surface and architecture of tissue engineering scaffolds. In Regenerative Medicine and Tissue Engineering—Cells and Biomaterials, Daniel, E., ed. (InTech, London, U.K., 2011); p. 571. Retrieve from:


Cytotoxicity and antibacterial efficacy of silver deposited onto titanium plates by low-energy ion implantation

  • Tatiana P. Soares (a1), Charlene S.C. Garcia (a2), Mariana Roesch-Ely (a2), Marcelo E.H. Maia da Costa (a3), Marcelo Giovanela (a1) and Cesar Aguzzoli (a1)...


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