Skip to main content

Advertisement

Log in

Inhibition of biofilm formation on iodine-supported titanium implants

  • Original Paper
  • Published:
International Orthopaedics Aims and scope Submit manuscript

Abstract

Purpose

We have developed iodine-supported titanium implants that suppress microbial activities and conducted in vivo and in vitro studies to determine their antimicrobial properties.

Methods

The implants were Ti-6Al-4 V titanium implants either untreated (Ti), treated with oxide film on the Ti surface by anodization (Ti-O), or treated with an iodine coating on oxidation film (Ti-I). The strain of bacteria used in this study was Gram-positive Staphylococcus aureus strain ATCC 25923. We analyzed the antibacterial attachment effects in vivo by using rats. The attachment bacteria on the implant surface were evaluated using a spread-plate method assay. A biofilm study was performed in vitro. The biofilm formed after bacterial attachment was qualitatively studied with fluorescence microscopy (FM) and scanning electron microscopy (SEM). Also, the formed biofilm was quantitatively studied with a spread-plate method assay.

Results

In vivo analysis of antimicrobial attachment effects showed that the mean viable bacterial number was significantly lower on Ti-I than Ti or Ti-O surfaces. In the in vitro biofilm study, FM and SEM images showed thick and mature biofilm formation on Ti and Ti-O and thin, small biofilm formation on Ti-I. A quantitative biofilm analysis found a significant difference in the number of viable bacteria between Ti-I and Ti or Ti-O.

Conclusions

This study showed that iodine-supported implants have a good antibacterial attachment effect and inhibit biofilm formation and growth. Iodine-supported implants may have great potential as innovative antibacterial implants that can prevent implant related infection in orthopaedic surgery.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Ridgeway S, Wilson J, Charlet A, Kafatos G, Pearson A, Coello R (2005) Infection of the surgical site after arthroplasty of the hip. J Bone Joint Surg Br 87:844–850

    Article  CAS  PubMed  Google Scholar 

  2. Olsen MA, Nepple JJ, Riew KD, Lenke LG, Bridwell KH, Mayfield J et al (2008) Risk factors for surgical site infection following orthopaedic spinal operations. J Bone Joint Surg Am 90:62–69

    Article  PubMed  Google Scholar 

  3. Mahan J, Selgison D, Henry SL, Hynes P, Dobbins J (1991) Factors in pin tract infections. Orthopedics 14:305–308

    CAS  PubMed  Google Scholar 

  4. Lee-Smith J, Santy J, Davis P, Jester R, Kneale J (2001) Pin site management. Towards a consensus: part I. J Orthop Nurs 5:37–42

    Article  Google Scholar 

  5. Nohr RS, Macdonald JG (1994) New biomaterials through surface segregation phenomenon: new quaternary ammonium compounds as antibacterial agents. J Biomater Sci Polym Ed 5:607–619

    Article  CAS  PubMed  Google Scholar 

  6. An YH, Stuart GW, McDowell SJ, McDaniel SE, Kang Q, Friedman RJ (1996) Prevention of bacterial adherence to implant surfaces with a cross-linked albumin coating in vivo. J Orthop Res 14:846–849

    Article  CAS  PubMed  Google Scholar 

  7. Tyagi M, Singh H (1997) Preparation and antibacterial evaluation of urinary balloon catheter. Biomed Sci Instrum 33:240–245

    CAS  PubMed  Google Scholar 

  8. Yorganci K, Krepel C, Weigelt JA, Edmiston CE (2002) In vitro evaluation of the antibacterial activity of three different central venous catheters against grampositive bacteria. Eur J Clin Microbiol Infect Dis 21:379–384

    Article  CAS  PubMed  Google Scholar 

  9. Kinnari TJ, Peltonen LI, Kuusela P, Kivilahti J, Kononen M, Jero J (2005) Bacterial adherence to titanium surface coated with human serum albumin. Otol Neurotol 26:380–384

    Article  PubMed  Google Scholar 

  10. Akiyama T, Miyamoto H, Yonekura Y, Tsukamoto M, Ando Y, Noda I et al (2013) Silver oxide-containing hydroxyapatite coating has in vivo antibacterial activity in the rat tibia. J Orthop Res 31(8):1195–1200

    Article  CAS  PubMed  Google Scholar 

  11. Nganga S, Travan A, Marsich E, Donati I, Söderling E, Moritz N et al. (2013) In vitro antimicrobial properties of silver-polysaccharide coatings on porous fiber-reinforced composites for bone implants. J Mater Sci Mater Med 24(12):2775–2785

  12. Kyomoto M, Shobuike T, Moro T, Yamane S, Takatori Y, Tanaka S et al (2015) Prevention of bacterial adhesion and biofilm formation on a vitamin E-blended, cross-linked polyethylene surface with a poly (2-methacryloyloxyethyl phosphorylcholine) layer. Acta Biomater 24:24–34

    Article  CAS  PubMed  Google Scholar 

  13. Jennings JA, Carpenter DP, Troxel KS, Beenken KE, Smeltzer MS, Courtney HS et al (2015) Novel antibiotic-loaded point-of-care implant coating inhibits biofilm. Clin Orthop Relat Res 473(7):2270–2282

    Article  PubMed  PubMed Central  Google Scholar 

  14. Kraft CN, Hansis M, Arens S, Menger MD, Vollmar B (2000) Striated muscle microvascular response to silver implants: a comparative in vivo study with titanium and stainless steel. J Biomed Mater Res 49:192–199

    Article  CAS  PubMed  Google Scholar 

  15. Walder B, Pittet D, Tramèr MR (2002) Prevention of bloodstream infections with central venous catheters treated with antiinfective agents depends on catheter type and insertion time: evidence from a meta-analysis. Infect Control Hosp Epidemiol 23:748–756

    Article  PubMed  Google Scholar 

  16. Crabtree JH, Burchette RJ, Siddiqi RA, Huen IT, Hadnott LL, Fishman A (2003) The efficacy of silver-ion implanted catheters in reducing peritoneal dialysis-related infections. Perit Dial Int 23:368–374

    CAS  PubMed  Google Scholar 

  17. Shirai T, Shimizu T, Ohtani K, Zen Y, Takaya M, Tsuchiya H (2011) Antibacterial iodine-supported titanium implants. Acta Biomater 7(4):1928–1933

    Article  CAS  PubMed  Google Scholar 

  18. Hashimoto K, Takaya M, Maejima A, Saruwatari K, Hirata M, Toda Y et al (1999) Antimicrobial characteristics of anodic oxidation coating of aluminum impregnated with iodine compound. Inorg Mater 6:457–462

    Google Scholar 

  19. Lucke M, Schmidmaier G, Sadoni S, Wildemann B, Schiller R, Stemberger A et al (2003) A new model of implant-related osteomyelitis in rats. J Biomed Mater Res B Appl Biomater 67(1):593–602

    Article  CAS  PubMed  Google Scholar 

  20. Braem A, Van Mellaert L, Mattheys T, Hofmans D, De Waelheyns E, Geris L et al (2014) Staphylococcal biofilm growth on smooth and porous titanium coatings for biomedical applications. J Biomed Mater Res A 102(1):215–224

    Article  PubMed  Google Scholar 

  21. Nishimura S, Tsurumoto T, Yonekura A, Adachi K, Shindo H (2006) Antimicrobial susceptibility of Staphylococcus aureus and Staphylococcus epidermidis biofilms isolated from infected total hip arthroplasty cases. J Orthop Sci 2006(11):46–50

    Article  Google Scholar 

  22. Life Technologies Corporation. Invitrogen—Protocol for film tracer TM FM_ 1–43 green biofilm cell stain. 2009. http://tools.invitrogen.com/content/sfs/manuals/mp10317.pdf. Accessed 23 April 2013

  23. Adachi K, Tsurumoto T, Yonekura A, Nishimura S, Kajiyama S, Hirakata Y, Shindo H (2007) New quantitative image analysis of staphylococcal biofilms on the surfaces of nontranslucent metallic biomaterials. J Orthop Sci 12(2):178–184

    Article  PubMed  Google Scholar 

  24. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675

    Article  CAS  PubMed  Google Scholar 

  25. Jorgensen J, Pfaller M, Carroll K, Funke G, Landry M, Richter S et al. (2015) Manual of Clinical Microbiology 11:184–186

  26. Houang ET, Gilmore OJ, Reid C, Shaw EJ (1976) Absence of bacterial resistance to povidone iodine. J Clin Pathol 29(8):752–755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Tanner J, Vallittu PK, Söderling E (2000) Adherence of Streptococcus mutans to an E-glass fiber-reinforced composite and conventional restorative materials used in prosthetic dentistry. J Biomed Mater Res 49(2):250–256

    Article  CAS  PubMed  Google Scholar 

  28. Koseki H, Yonekura A, Shida T, Yoda I, Horiuchi H, Morinaga Y et al (2014) Early staphylococcal biofilm formation on solid orthopaedic implant materials: in vitro study. PLoS One 9(10):e107588

    Article  PubMed  PubMed Central  Google Scholar 

  29. Necula BS, Fratila-Apachitei LE, Zaat SA, Apachitei I, Duszczyk J (2009) In vitro antibacterial activity of porous TiO2-ag composite layers against methicillin-resistant Staphylococcus aureus. Acta Biomater 5(9):3573–3580

    Article  CAS  PubMed  Google Scholar 

  30. Arciola CR, Campoccia D, Speziale P, Montanaro L, Costerton JW (2012) Biofilm formation in Staphylococcus implant infections. A review of molecular mechanisms and implications for biofilm-resistant materials. Biomaterials 33(26):5967–5982

    Article  CAS  PubMed  Google Scholar 

  31. Gbejuade HO, Lovering AM, Webb JC (2015) The role of microbial biofilms in prosthetic joint infections. Acta Orthop 86(2):147–158

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors wish to thank Mr. Tohru Shimizu, who was a Professor of Bacteriology at Kanazawa University, for considerable advice on experimental design and his skillful microbiological techniques. He suddenly died of illness during this research period and we express heartfelt condolences for his family.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hiroyuki Tsuchiya.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Funding

There is no funding source.

Ethical approval

This study was performed with the approval of the animal ethics committee at our institution (Approval date: 3 September 2013; Approval number: 132,928).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Inoue, D., Kabata, T., Ohtani, K. et al. Inhibition of biofilm formation on iodine-supported titanium implants. International Orthopaedics (SICOT) 41, 1093–1099 (2017). https://doi.org/10.1007/s00264-017-3477-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00264-017-3477-3

Keywords

Navigation