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Osteogenic response and osteoprotective effects in vivo of a nanostructured titanium surface with antibacterial properties

  • Engineering and Nano-engineering Approaches for Medical Devices
  • Original Research
  • Published:
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Abstract

In implantology, as an alternative approach to the use of antibiotics, direct surface modifications of the implant addressed to inhibit bacterial adhesion and to limit bacterial proliferation are a promising tactic. The present study evaluates in an in vivo normal model the osteogenic response and the osteointegration of an anodic spark deposition nanostructured titanium surface doped with gallium (ASD + Ga) in comparison with two other surface treatments of titanium: an anodic spark deposition treatment without gallium (ASD) and an acid etching treatment (CTR). Moreover the study assesses the osteoprotective potential and the antibacterial effect of the previously mentioned surface treatments in an experimentally-induced peri-implantitis model. The obtained data points out a more rapid primary fixation in ASD and ASD + Ga implants, compared with CTR surface. Regarding the antibacterial properties, the ASD + Ga surface shows osteoprotective action on bone peri-implant tissue in vivo as well as an antibacterial effect within the first considered time point.

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References

  1. Mangram AJ, et al. Guideline for prevention of surgical site infection, 1999. Centers for Disease Control and Prevention (CDC) Hospital Infection Control Practices Advisory Committee. Am J Infect Control. 1999;27(2):97–132 quiz 133–134; discussion 96.

    Article  Google Scholar 

  2. Hayes G, Moens N, Gibson T. A review of local antibiotic implants and applications to veterinary orthopaedic surgery. Vet Comp Orthop Traumatol. 2013;26(4):251–9.

    Article  Google Scholar 

  3. Gristina A. Biomaterial-centered infection: microbial adhesion versus tissue integration. Clin Orthop Relat Res. 1987;2004(427):4–12.

    Google Scholar 

  4. Katsikogianni M, Missirlis YF. Concise review of mechanisms of bacterial adhesion to biomaterials and of techniques used in estimating bacteria-material interactions. Eur Cell Mater. 2004;8:37–57.

    Google Scholar 

  5. Campoccia D, Montanaro L, Arciola CR. The significance of infection related to orthopedic devices and issues of antibiotic resistance. Biomaterials. 2006;27(11):2331–9.

    Article  Google Scholar 

  6. Gristina AG. Implant failure and the immuno-incompetent fibro-inflammatory zone. Clin Orthop Relat Res. 1994;298:106–18.

    Google Scholar 

  7. Arciola CR, et al. Interactions of staphylococci with osteoblasts and phagocytes in the pathogenesis of implant-associated osteomyelitis. Int J Artif Organs. 2012;35(10):713–26.

    Google Scholar 

  8. Hudson MC, Ramp WK, Frankenburg KP. Staphylococcus aureus adhesion to bone matrix and bone-associated biomaterials. FEMS Microbiol Lett. 1999;173(2):279–84.

    Article  Google Scholar 

  9. Del Pozo JL, Patel R. Clinical practice. Infection associated with prosthetic joints. N Engl J Med. 2009;361(8):787–94.

    Article  Google Scholar 

  10. Wininger DA, Fass RJ. Antibiotic-impregnated cement and beads for orthopedic infections. Antimicrob Agents Chemother. 1996;40(12):2675–9.

    Google Scholar 

  11. Ethell MT, et al. In vitro elution of gentamicin, amikacin, and ceftiofur from polymethylmethacrylate and hydroxyapatite cement. Vet Surg. 2000;29(5):375–82.

    Article  Google Scholar 

  12. Andersson RE, et al. Local administration of antibiotics by gentamicin-collagen sponge does not improve wound healing or reduce recurrence rate after pilonidal excision with primary suture: a prospective randomized controlled trial. World J Surg. 2010;34(12):3042–8.

    Article  Google Scholar 

  13. Lapid O. Use of gentamicin collagen sponges for the treatment of periprosthetic breast implant infection. J Plast Reconstr Aesthet Surg. 2011;64(12):e313–6.

    Article  Google Scholar 

  14. Lewis CS, et al. Local antibiotic delivery with demineralized bone matrix. Cell Tissue Bank. 2012;13(1):119–27.

    Article  Google Scholar 

  15. Diefenbeck M, Mückley T, Hofmann GO. Prophylaxis and treatment of implant-related infections by local application of antibiotics. Injury. 2006;37(Suppl 2):S95–104.

    Article  Google Scholar 

  16. Cohn LA, Middleton JR. A veterinary perspective on methicillin-resistant staphylococci. J Vet Emerg Crit Care (San Antonio). 2010;20(1):31–45.

    Article  Google Scholar 

  17. Zhao L, et al. Antibacterial coatings on titanium implants. J Biomed Mater Res B Appl Biomater. 2009;91(1):470–80.

    Article  Google Scholar 

  18. Puckett SD, et al. The relationship between the nanostructure of titanium surfaces and bacterial attachment. Biomaterials. 2010;31(4):706–13.

    Article  Google Scholar 

  19. Schaer TP, et al. Hydrophobic polycationic coatings that inhibit biofilms and support bone healing during infection. Biomaterials. 2012;33(5):1245–54.

    Article  Google Scholar 

  20. Visai L, et al. Electrochemical surface modification of titanium for implant abutments can affect oral bacteria contamination. J Appl Biomater Biomech. 2008;6(3):170–7.

    Google Scholar 

  21. Shi Z, et al. Antibacterial and mechanical properties of bone cement impregnated with chitosan nanoparticles. Biomaterials. 2006;27(11):2440–9.

    Article  Google Scholar 

  22. Zhang F, et al. Silk-functionalized titanium surfaces for enhancing osteoblast functions and reducing bacterial adhesion. Biomaterials. 2008;29(36):4751–9.

    Article  Google Scholar 

  23. Harris LG, et al. Staphylococcus aureus adhesion to titanium oxide surfaces coated with non-functionalized and peptide-functionalized poly(l-lysine)-grafted-poly(ethylene glycol) copolymers. Biomaterials. 2004;25(18):4135–48.

    Article  Google Scholar 

  24. Visai L, et al. Titanium oxide antibacterial surfaces in biomedical devices. Int J Artif Organs. 2011;34(9):929–46.

    Article  Google Scholar 

  25. Song WH, Ryu HS, Hong SH. Antibacterial properties of Ag (or Pt)-containing calcium phosphate coatings formed by micro-arc oxidation. J Biomed Mater Res A. 2009;88(1):246–54.

    Article  Google Scholar 

  26. Lara HH, et al. Silver nanoparticles are broad-spectrum bactericidal and virucidal compounds. J Nanobiotechnology. 2011;9:30.

    Article  Google Scholar 

  27. Chen Y, et al. Anti-bacterial and cytotoxic properties of plasma sprayed silver-containing HA coatings. J Mater Sci Mater Med. 2008;19(12):3603–9.

    Article  Google Scholar 

  28. Fiedler J, et al. Copper and silver ion implantation of aluminium oxide-blasted titanium surfaces: proliferative response of osteoblasts and antibacterial effects. Int J Artif Organs. 2011;34(9):882–8.

    Article  Google Scholar 

  29. Zheng Y, et al. Antimicrobial and osteogenic effect of Ag-implanted titanium with a nanostructured surface. Int J Nanomedicine. 2012;7:875–84.

    Google Scholar 

  30. Lansdown AB. Silver in health care: antimicrobial effects and safety in use. Curr Probl Dermatol. 2006;33:17–34.

    Article  Google Scholar 

  31. Bernstein LR. Mechanisms of therapeutic activity for gallium. Pharmacol Rev. 1998;50(4):665–82.

    Google Scholar 

  32. Olakanmi O, et al. Polyvalent cationic metals induce the rate of transferrin-independent iron acquisition by HL-60 cells. J Biol Chem. 1997;272(5):2599–606.

    Article  Google Scholar 

  33. Nerren JR, et al. Evaluation of the effect of gallium maltolate on fecal Salmonella shedding in cattle. J Food Prot. 2011;74(4):524–30.

    Article  Google Scholar 

  34. Cochis A, et al. Biofilm formation on titanium implants counteracted by grafting gallium and silver ions. J Biomed Mater Res A. 2015;103(3):1176–87.

    Article  Google Scholar 

  35. Kaneko Y, et al. The transition metal gallium disrupts Pseudomonas aeruginosa iron metabolism and has antimicrobial and antibiofilm activity. J Clin Invest. 2007;117(4):877–88.

    Article  Google Scholar 

  36. Niesvizky R. Gallium nitrate in multiple myeloma: prolonged survival in a cohort of patients with advanced-stage disease. Semin Oncol. 2003;30(2 Suppl 5):20–4.

    Article  Google Scholar 

  37. Verron E, et al. Gallium modulates osteoclastic bone resorption in vitro without affecting osteoblasts. Br J Pharmacol. 2010;159(8):1681–92.

    Article  Google Scholar 

  38. Chai H, et al. Antibacterial effect of 317L stainless steel contained copper in prevention of implant-related infection in vitro and in vivo. J Mater Sci Mater Med. 2011;22(11):2525–35.

    Article  Google Scholar 

  39. Della Valle C, et al. A novel silicon-based electrochemical treatment to improve osteointegration of titanium implants. J Appl Biomater Funct Mater. 2013;11(2): e106–16.

  40. van Gaalen SM, et al. Use of fluorochrome labels in in vivo bone tissue engineering research. Tissue Eng Part B Rev. 2010;16(2):209–17.

    Article  Google Scholar 

  41. Dempster DW, et al. Standardized nomenclature, symbols, and units for bone histomorphometry: a 2012 update of the report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res. 2013;28(1):1–16.

    Article  Google Scholar 

  42. Ravanetti F, et al. In vitro cellular response and in vivo primary osteointegration of electrochemically modified titanium, in Acta Biomater. 2010, 2009 Acta Materialia Inc. Published by Elsevier Ltd: England. p. 1014-24.

  43. Chiesa R, et al. In vitro and in vivo performance of a novel surface treatment to enhance osseointegration of endosseous implants. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2007;103(6):745–56.

    Article  Google Scholar 

  44. Giavaresi G, et al. Mechanical and histomorphometric evaluations of titanium implants with different surface treatments inserted in sheep cortical bone. Biomaterials. 2003;24(9):1583–94.

    Article  Google Scholar 

  45. Giavaresi G, et al. A novel multiphase anodic spark deposition coating for the improvement of orthopedic implant osseointegration: an experimental study in cortical bone of sheep. J Biomed Mater Res A. 2008;85(4):1022–31.

    Article  Google Scholar 

  46. Giavaresi G, et al. Histomorphometric and microhardness assessments of sheep cortical bone surrounding titanium implants with different surface treatments. J Biomed Mater Res A. 2003;67(1):112–20.

    Article  Google Scholar 

  47. Giavaresi G, et al. Effect of a multiphasic anodic spark deposition coating on the improvement of implant osseointegration in the osteopenic trabecular bone of sheep. Int J Oral Maxillofac Implants. 2008;23(4):659–68.

    Google Scholar 

  48. Verron E, Bouler JM, Scimeca JC. Gallium as a potential candidate for treatment of osteoporosis. Drug Discov Today. 2012;17(19–20):1127–32.

    Article  Google Scholar 

  49. Bockman R. The effects of gallium nitrate on bone resorption. Semin Oncol. 2003;30(2 Suppl 5):5–12.

    Article  Google Scholar 

  50. Hall TJ, Chambers TJ. Gallium inhibits bone resorption by a direct effect on osteoclasts. Bone Miner. 1990;8(3):211–6.

    Article  Google Scholar 

  51. Liewehr FR, et al. Effect of bisphosphonates and gallium on dentin resorption in vitro. Endod Dent Traumatol. 1995;11(1):20–6.

    Article  Google Scholar 

  52. Lakatos P, Mong S, Stern PH. Gallium nitrate inhibits bone resorption and collagen synthesis in neonatal mouse calvariae. J Bone Miner Res. 1991;6(10):1121–6.

    Article  Google Scholar 

  53. Blair HC, et al. Reversible inhibition of osteoclastic activity by bone-bound gallium (III). J Cell Biochem. 1992;48(4):401–10.

    Article  Google Scholar 

  54. Shaini FJ, et al. In vitro evaluation of the effect of freshly mixed amalgam and gallium-based alloy on the viability of primary periosteal and osteoblast cell cultures. Biomaterials. 2000;21(2):113–9.

    Article  Google Scholar 

  55. Jenis LG, et al. Effect of gallium nitrate in vitro and in normal rats. J Cell Biochem. 1993;52(3):330–6.

    Article  Google Scholar 

  56. Verron E, et al. Molecular effects of gallium on osteoclastic differentiation of mouse and human monocytes. Biochem Pharmacol. 2012;83(5):671–9.

    Article  Google Scholar 

  57. DeLeon K, et al. Gallium maltolate treatment eradicates Pseudomonas aeruginosa infection in thermally injured mice. Antimicrob Agents Chemother. 2009;53(4):1331–7.

    Article  Google Scholar 

  58. Arnold CE, et al. Antimicrobial activity of gallium maltolate against Staphylococcus aureus and methicillin-resistant S. aureus and Staphylococcus pseudintermedius: an in vitro study. Vet Microbiol. 2012;155(2–4):389–94.

    Article  Google Scholar 

  59. Valappil SP, et al. Effect of novel antibacterial gallium-carboxymethyl cellulose on Pseudomonas aeruginosa. Dalton Trans. 2013;42(5):1778–86.

    Article  Google Scholar 

  60. Valappil SP, et al. Role of gallium and silver from phosphate-based glasses on in vitro dual species oral biofilm models of Porphyromonas gingivalis and Streptococcus gordonii. Acta Biomater. 2012;8(5):1957–65.

    Article  Google Scholar 

  61. Patel M, et al. Animal models for the study of osteomyelitis. Semin Plast Surg. 2009;23(2):148–54.

    Article  Google Scholar 

  62. Cèsar LC. Long-term stability assessment of antibacterial tratment of titanium., in Department of Chemistry, Materials and Materials Engineering “G. Natta”. 2014, Politecnico di Milano: Master Thesis.

  63. Cochis A, et al. The effect of silver or gallium doped titanium against the multidrug resistant Acinetobacter baumannii. Biomaterials. 2016. doi: 10.1016/j.biomaterials.2015.11.042

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Acknowledgments

The authors would like to thank Eurocoating S.p.A. for their liberal donation that contributed the funding of this study. Furthermore, they declare no conflict of interest.

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Correspondence to F. Ravanetti.

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Ravanetti, F., Chiesa, R., Ossiprandi, M.C. et al. Osteogenic response and osteoprotective effects in vivo of a nanostructured titanium surface with antibacterial properties. J Mater Sci: Mater Med 27, 52 (2016). https://doi.org/10.1007/s10856-015-5661-6

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  • DOI: https://doi.org/10.1007/s10856-015-5661-6

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