journal article·2021-07-04Open access

Antimicrobial Properties of Strontium Functionalized Titanium Surfaces for Oral Applications, A Systematic Review

Hatem Alshammari, Fahad Bakitian, Jessica Neilands, Ole Zoffmann Andersen, Andreas Stavropoulos

Coatings· Volume 11· Issue 7

Abstract

The aim of this systematic review was to assess the current scientific evidence of the antimicrobial potential of strontium (Sr) when used to functionalize titanium (Ti) for oral applications. Out of an initial list of 1081 potentially relevant publications identified in three electronic databases (MEDLINE via PubMed, Scopus, and Cochrane) up to 1 February 2021, nine publications based on in vitro studies met the inclusion criteria. The antimicrobial potential of Sr was investigated on different types of functionalized Ti substrates, employing different application methods. Nine studies reported on the early, i.e., 6–24 h, and two studies on the late, i.e., 7–28 days, antimicrobial effect of Sr, primarily against Staphylococcus aureus (S. aureus) and/or Escherichia coli (E. coli). Sr-modified samples demonstrated relevant early antimicrobial potential against S. aureus in three studies; only one of which presented statistical significance values, while the other two presented only the percentage of antimicrobial rate and biofilm inhibition. A relevant late biofilm inhibition potential against S. aureus of 40% and 10%—after 7 and 14 days, respectively—was reported in one study. Combining Sr with other metal ions, i.e., silver (Ag), zinc (Zn), and fluorine (F), demonstrated a significant antimicrobial effect and biofilm inhibition against both S. aureus and E. coli. Sr ion release within the first 24 h was generally low, i.e., below 50 µg/L and 0.6 ppm; however, sustained Sr ion release for up to 30 days, while maintaining up to 90% of its original content, was also demonstrated. Thus, in most studies included herein, Sr-functionalized Ti showed a limited immediate (i.e., 24 h) antimicrobial effect, likely due to a low Sr ion release; however, with an adequate Sr ion release, a relevant antimicrobial effect, as well as a biofilm inhibition potential against S. aureus—but not E. coli—was observed at both early and late timepoints. Future studies should assess the antimicrobial potential of Ti functionalized with Sr against multispecies biofilms associated with peri-implantitis.
Source: crossref · Quality: baseline

Research context

OpenAlex topics: Orthopedic Infections and Treatments · Scientific and Engineering Research Topics · Dental Implant Techniques and Outcomes

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Department of Periodontology, Faculty of Odontology, Malmö University, 205 06 Malmö, Sweden

Department of Preventive Dentistry, College of Dentistry, University of Hail, Hail 50141, Saudi Arabia

Department of Restorative Dentistry, College of Dentistry, Umm Al-Qura University, Mecca 21961, Saudi Arabia

Department of Oral Biology, Faculty of Odontology, Malmö University, 205 06 Malmö, Sweden

Elos Medtech, 3330 Gørløse, Denmark

Division of Regenerative Dental Medicine and Periodontology, University Dental Clinics, CUMD, University of Geneva, 1211 Geneva, Switzerland

References (76)

Show source-provided references
1. Peri-implant diseases10.1111/eos.12529 ↗
2. Peri-implant mucositis
3. Peri-implantitis10.1002/JPER.16-0350 ↗
4. Clinical characteristics of peri-implant mucositis and peri-implantitis10.1111/clr.13152 ↗
5. Long-term implant prognosis in patients with and without a history of chronic periodontitis: A 10-year prospective cohort study of the ITI dental implant system10.1034/j.1600-0501.000.00934.x ↗
6. Survival of dental implants at sites after implant failure: A systematic review10.1016/j.prosdent.2018.11.007 ↗
7. Peri-implant health and disease. A systematic review of current epidemiology10.1111/jcpe.12334 ↗
8. Epidemiology and risk factors of peri-implantitis: A systematic review10.1111/jre.12562 ↗
9. Surgical treatment of peri-implantitis—Consensus report of working group 410.1111/idj.12505 ↗
10. Antibiotics in the treatment of peri-implantitis
11. Risk for recurrence of disease following surgical therapy of peri-implantitis—A prospective longitudinal study10.1111/clr.13653 ↗
12. Surface modification techniques of titanium and its alloys to functionally optimize their biomedical properties: Thematic review10.3389/fbioe.2020.603072 ↗
13. Review of titanium surface modification techniques and coatings for antibacterial applications10.1016/j.actbio.2018.10.036 ↗
14. Carinci, F., Lauritano, D., Bignozzi, C.A., Pazzi, D., Candotto, V., Santos de Oliveira, P., and Scarano, A. (2019). A New strategy against peri-implantitis: Antibacterial internal coating. Int. J. Mol. Sci., 20.10.3390/ijms20163897 ↗
15. Antimicrobial dental implant functionalization strategies—A systematic review10.4012/dmj.2015-314 ↗
16. Targeting implant-associated infections: Titanium surface loaded with antimicrobial10.1016/j.isci.2020.102008 ↗
17. Biomaterial and antibiotic strategies for peri-implantitis: A review10.1002/jbm.b.31152 ↗
18. Emerging antibacterial biomaterial strategies for the prevention of peri-implant inflammatory diseases
19. Enhanced antibacterial activity of titanium by surface modification with polydopamine and silver for dental implant application
20. ZnO@ZnS nanorod-array coated titanium: Good to fibroblasts but bad to bacteria10.1016/j.jcis.2020.06.055 ↗
21. Antibacterial, angiogenic, and osteogenic activities of Ca, P, Co, F, and Sr compound doped titania coatings with different Sr content10.1038/s41598-019-50496-3 ↗
22. Synthesis and antimicrobial activity of silver complexes with histidine and tryptophan10.1007/BF02524634 ↗
23. Silver nanoparticles as a new generation of antimicrobials10.1016/j.biotechadv.2008.09.002 ↗
24. Mechanical, in vitro antimicrobial, and biological properties of plasma-sprayed silver-doped hydroxyapatite coating10.1021/am201610q ↗
25. Synergistic effects of dual Zn/Ag ion implantation in osteogenic activity and antibacterial ability of titanium10.1016/j.biomaterials.2014.05.074 ↗
26. Antibacterial ability and osteogenic activity of porous Sr/Ag-containing TiO2 coatings10.1088/1748-6041/11/4/045008 ↗
27. Evaluation of osteogenic and antibacterial properties of strontium/silver-containing porous TiO10.1002/jbm.b.34719 ↗
28. Alshammari, H., Neilands, J., Svensäter, G., and Stavropoulos, A. (2021). Antimicrobial potential of strontium hydroxide on bacteria associated with peri-implantitis. Antibiotics, 10.10.3390/antibiotics10020150 ↗
29. Study of the dual effect of gamma irradiation and strontium substitution on bioactivity, cytotoxicity, and antimicrobial properties of 45S5 bioglass10.1002/jbm.a.36035 ↗
30. Strontium-substituted bioactive glasses in vitro osteogenic and antibacterial effects10.1016/j.dental.2015.12.013 ↗
31. A strontium-incorporated nanoporous titanium implant surface for rapid osseointegration10.1039/C5NR08580B ↗
32. In vivo osseointegration of Ti implants with a strontium-containing nanotubular coating
33. Loading deproteinized bovine bone with strontium enhances bone regeneration in rat calvarial critical size defects10.1007/s00784-018-2588-6 ↗
34. Strontium ranelate for preventing and treating postmenopausal osteoporosis
35. Strontium ranelate in post-menopausal osteoporosis
36. Effects of long-term strontium ranelate treatment on the risk of nonvertebral and vertebral fractures in postmenopausal osteoporosis: Results of a five-year, randomized, placebo-controlled trial10.1002/art.23461 ↗
37. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement10.1136/bmj.b2535 ↗
38. [Antimicrobial prosthesis coatings]10.1007/s00132-015-3189-6 ↗
39. Multifunction Sr, Co and F co-doped microporous coating on titanium of antibacterial, angiogenic and osteogenic activities10.1038/srep29069 ↗
40. Surface functionalization of titanium with zinc/strontium-doped titanium dioxide microporous coating via microarc oxidation10.1016/j.nano.2018.12.006 ↗
41. Strontium incorporation to optimize the antibacterial and biological characteristics of silver-substituted hydroxyapatite coating10.1016/j.msec.2015.08.061 ↗
42. Incorporation of silver and strontium in hydroxyapatite coating on titanium surface for enhanced antibacterial and biological properties10.1016/j.msec.2016.10.079 ↗
43. Antibacterial and biological characteristics of silver containing and strontium doped plasma sprayed hydroxyapatite coatings10.1016/j.actbio.2012.04.004 ↗
44. Deposition of substituted apatites with anticolonizing properties onto titanium surfaces using a novel blasting process
45. Bioactivity and antibacterial activity of strontium and silver ion releasing titanium10.1002/jbm.b.34695 ↗
46. Study of antibacterial and osteogenic activity of titanium metal releasing strontium and silver ions10.1177/0885328220959584 ↗
47. Bacterial adherence and biofilm formation on medical implants: A review10.1177/0954411914556137 ↗
48. Cluster of bacteria associated with peri-implantitis10.1111/cid.12052 ↗
49. Bacterial adhesion mechanisms on dental implant surfaces and the influencing factors10.1016/j.ijadhadh.2016.03.022 ↗
50. Titanium particles and ions favor dysbiosis in oral biofilms10.1111/jre.12711 ↗
51. The microbiologic profile associated with peri-implantitis in humans: A systematic review10.11607/jomi.4150 ↗
52. Bacterial colonization of the peri-implant sulcus in dentate patients: A prospective observational study10.1007/s00784-016-1941-x ↗
53. Peri-implantitis: A comprehensive overview of systematic reviews10.1563/aaid-joi-D-16-00122 ↗
54. Correction to: Induced surface proteins of Staphylococcus epidermidis adhering to titanium implant substrata10.1007/s00784-019-02879-z ↗
55. Microbiome and microbial biofilm profiles of peri-implantitis: A systematic review10.1902/jop.2017.170123 ↗
56. Five-year clinical, microbiological, and radiological outcome following treatment of peri-implantitis in man10.1902/jop.2003.74.10.1415 ↗
57. Stewart, E.J., Payne, D.E., Ma, T.M., VanEpps, J.S., Boles, B.R., Younger, J.G., and Solomon, M.J. (2017). Effect of antimicrobial and physical treatments on growth of multispecies staphylococcal biofilms. Appl. Environ. Microbiol., 83.10.1128/AEM.03483-16 ↗
58. The role of calcium ion release on biocompatibility and antimicrobial properties of hydraulic cements10.1038/s41598-019-55288-3 ↗
59. The release properties of silver ions from Ag-nHA/TiO2/PA66 antimicrobial composite scaffolds10.1088/1748-6041/5/4/044105 ↗
60. Metal ion-assisted self-assembly of complexes for controlled and sustained release of minocycline for biomedical applications10.1088/1758-5090/7/1/015006 ↗
61. Elemental ion release and cytotoxicity of antimicrobial acrylic resins incorporated with nanomaterial10.1111/ger.12267 ↗
62. Effect of silver nanoparticles on human primary keratinocytes10.1515/hsz-2012-0202 ↗
63. Effect of silver nanoparticles on human mesenchymal stem cell differentiation10.3762/bjnano.5.214 ↗
64. In vivo evaluation of plasma sprayed hydroxyapatite coatings having different crystallinity10.1016/S0142-9612(03)00545-3 ↗
65. The in vitro and in vivo performance of a strontium-containing coating on the low-modulus Ti35Nb2Ta3Zr alloy formed by micro-arc oxidation10.1007/s10856-015-5533-0 ↗
66. Sobolev, A., Wolicki, I., Kossenko, A., Zinigrad, M., and Borodianskiy, K. (2018). Coating formation on Ti-6Al-4V alloy by micro arc oxidation in molten salt. Materials, 11.10.3390/ma11091611 ↗
67. Biological responses to hydroxyapatite surfaces deposited via a co-incident microblasting technique10.1016/j.biomaterials.2009.09.067 ↗
68. Antibacterial and cytocompatibility study of modified Ti6Al4V surfaces through thermal annealing10.1016/j.msec.2019.02.058 ↗
69. Microstructure and cytotoxicity evaluation of duplex-treated silver-containing antibacterial TiO₂ coatings10.1016/j.msec.2014.07.002 ↗
70. Toxicity of silver ions, metallic silver, and silver nanoparticle materials after in vivo dermal and mucosal surface exposure: A review10.1016/j.yrtph.2018.08.007 ↗
71. Impact of treatments for postmenopausal osteoporosis (bisphosphonates, parathyroid hormone, strontium ranelate, and denosumab) on bone quality: A systematic review10.1007/s00223-010-9420-x ↗
72. The clinical effectiveness and cost-effectiveness of strontium ranelate for the prevention of osteoporotic fragility fractures in postmenopausal women10.3310/hta11040 ↗
73. The role of strontium ranelate and guided bone regeneration in osteoporotic and healthy conditions10.1111/jre.12825 ↗
74. Systemic administration of strontium ranelate to enhance the osseointegration of implants: Systematic review of animal studies10.1186/s40729-018-0132-8 ↗
75. Lu, W., Zhou, Y., Yang, H., Cheng, Z., and He, F. (2021). Efficacy of strontium supplementation on implant osseointegration under osteoporotic conditions: A systematic review. J. Prosthet. Dent., in press.10.1016/j.prosdent.2020.12.031 ↗
76. Effect of strontium-coated titanium implants on osseointegration in animal models: A literature systematic review10.11607/jomi.7827 ↗