Skip to main content

Advertisement

SpringerLink
Log in

Is coating of titanium implants effective at preventing Staphylococcus aureus infections? A meta-analysis of animal model studies

  • Review Article
  • Published:
International Orthopaedics Aims and scope Submit manuscript

Abstract

Aim of the study

To assess the effects of the available coating methods against methicillin-resistant Staphylococcus aureus (MRSA) and methicillin-susceptible S. aureus (MSSA) biofilm development on titanium implants.

Methods

We searched the MEDLINE, Embase, and CENTRAL databases until May 18, 2019, for studies that used animal models of infections to evaluate various titanium implant coating methods to prevent S. aureus infection. Twenty-seven studies were eligible for inclusion in qualitative synthesis. Of those, twenty-three were considered in pair-wise meta-analysis. In addition, subgroup analysis of implant protection strategies relative to uncoated controls was performed, and any adverse events stemming from the coating applications were reported. Quality assessment was performed using SYRCLE’s risk of bias tool for animal studies.

Results

Meta-analysis showed that active coating with antibiotics was favoured over uncoated controls (standardised mean differences [SMD] for MRSA and MSSA were – 2.71 [95% CI, − 4.24 to − 1.18], p = 0.0005, and − 2.5 [− 3.79 to − 1.22], p = 0.0001, respectively). Likewise, large effect sizes were demonstrated when a combination of active and conventional non-degradable passive coatings was compared with controls (SMDs for MRSA and MSSA were – 0.62 [95% CI, − 1.15 to − 0.08], p = 0.02, and − 1.93 [95% CI, − 2.87 to − 0.98], p < 0.001, respectively).

Discussion/conclusion

As a standalone prevention method, active titanium coating with antibiotics yielded promising results against both MSSA and MRSA. Combinations between active and non-degradable passive coatings, potentially allowing for sustained antimicrobial substance release, provided consistent hardware infection protection. Thus, we recommend that future research efforts focus on combined coating modalities against S. aureus biofilm infections in the presence of titanium implants.

Systematic Review Registration

CRD42019123462

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Kurtz SM, Lau E, Schmier J, Ong KL, Zhao K, Parvizi J (2008) Infection burden for hip and knee arthroplasty in the United States. J Arthroplast 23(7):984–991. https://doi.org/10.1016/j.arth.2007.10.017

    Article  Google Scholar 

  2. Cats-Baril W, Gehrke T, Huff K, Kendoff D, Maltenfort M, Parvizi J (2013) International consensus on periprosthetic joint infection: description of the consensus process. Clin Orthop Relat Res 471(12):4065–4075. https://doi.org/10.1007/s11999-013-3329-4

    Article  PubMed  PubMed Central  Google Scholar 

  3. Lenguerrand E, Whitehouse MR, Beswick AD, Toms AD, Porter ML, Blom AW (2017) Description of the rates, trends and surgical burden associated with revision for prosthetic joint infection following primary and revision knee replacements in England and Wales: an analysis of the National Joint Registry for England, Wales, Northern Ireland and the Isle of Man. BMJ Open 7(7):–e014056. https://doi.org/10.1136/bmjopen-2016-014056

  4. Bonnevialle P, Bonnomet F, Philippe R, Loubignac F, Rubens-Duval B, Talbi A, Le Gall C, Adam P (2012) Early surgical site infection in adult appendicular skeleton trauma surgery: a multicenter prospective series. Orthop Traumatol Surg Res 98(6):684–689. https://doi.org/10.1016/j.otsr.2012.08.002

    Article  CAS  PubMed  Google Scholar 

  5. Berbari EF, Osmon DR, Lahr B, Eckel-Passow JE, Tsaras G, Hanssen AD, Mabry T, Steckelberg J, Thompson R (2012) The Mayo prosthetic joint infection risk score: implication for surgical site infection reporting and risk stratification. Infect Control Hosp Epidemiol 33(8):774–781. https://doi.org/10.1086/666641

    Article  PubMed  Google Scholar 

  6. Oliveira PR, Carvalho VC, da Silva FC, de Paula AP, Santos-Silva J, Lima AL (2016) The incidence and microbiological profile of surgical site infections following internal fixation of closed and open fractures. Rev Bras Ortop 51(4):396–399. https://doi.org/10.1016/j.rboe.2015.09.012 eCollection 2016 Jul-Aug.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Dale H, Hallan G, Hallan G, Espehaug B, Havelin LI, Engesaeter LB (2009) Increasing risk of revision due to deep infection after hip arthroplasty. Acta Orthop 80(6):639–645. https://doi.org/10.3109/17453670903506658

    Article  PubMed  PubMed Central  Google Scholar 

  8. Kurtz SM, Lau E, Watson H, Schmier JK, Parvizi J (2012) Economic burden of periprosthetic joint infection in the United States. J Arthroplast 27(8 Suppl):61–5.e1. https://doi.org/10.1016/j.arth.2012.02.022

    Article  Google Scholar 

  9. Romanò CL, Scarponi S, Gallazzi E, Romanò D, Drago L (2015) Antibacterial coating of implants in orthopaedics and trauma: a classification proposal in an evolving panorama. J Orthop Surg Res 10:157. https://doi.org/10.1186/s13018-015-0294-5

    Article  PubMed  PubMed Central  Google Scholar 

  10. Saeidnia S, Manayi A, Abdollahi M (2015) From in vitro experiments to in vivo and clinical studies; pros and cons. Curr Drug Discov Technol 12(4):218–224

    Article  CAS  PubMed  Google Scholar 

  11. Romanò CL, Toscano M, Romanò D, Drago L (2013) Antibiofilm agents and implant-related infections in orthopaedics: where are we? J Chemother 25(2):67–80. https://doi.org/10.1179/1973947812Y.0000000045

    Article  CAS  PubMed  Google Scholar 

  12. Hooijmans CR, IntHout J, Ritskes-Hoitinga M, Rovers MM (2014) Meta-analyses of animal studies: an introduction of a valuable instrument to further improve healthcare. ILAR J 55(3):418–426. https://doi.org/10.1093/ilar/ilu042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Geetha M, Singh AK, Asokamani R, Gogia AK (2009) Ti based biomaterials, the ultimate choice for orthopaedic implants – a review. Prog Mater Sci 54(3):397–425

    Article  CAS  Google Scholar 

  14. Miller (2017) Miller’s Review of Orthopaedics. In: Miller’s Review of Orthopaedics, 7th edn, pp 94

  15. Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6(7):e1000097. https://doi.org/10.1371/journal.pmed.1000097

    Article  PubMed  PubMed Central  Google Scholar 

  16. Hooijmans CR, Rovers MM, de Vries RB, Leenaars M, Ritskes-Hoitinga M, Langendam MW (2014) SYRCLE’s risk of bias tool for animal studies. BMC Med Res Methodol 14:43. https://doi.org/10.1186/1471-2288-14-43

    Article  PubMed  PubMed Central  Google Scholar 

  17. Higgins JPT, Altman DG, Sterne JAC (editors). Chapter 8: assessing risk of bias in included studies. In: Higgins JPT, Green S (editors). Cochrane handbook for systematic reviews of interventions Version 5.1.0 (updated March 2011). The Cochrane Collaboration, 2011. Available from www.handbook.cochrane.org

  18. Sterne JAC, Egger M, Moher D (2008) Chapter 10: addressing reporting biases. In: Higgins JPT, Green S (eds) Cochrane handbook for systematic reviews of interventions. John Wiley & Sons, Chichester (UK)

    Google Scholar 

  19. Cheng H, Li Y, Huo K, Gao B, Xiong W (2014) Long-lasting in vivo and in vitro antibacterial ability of nanostructured titania coating incorporated with silver nanoparticles. J Biomed Mater Res A 102(10):3488–3499. https://doi.org/10.1002/jbm.a.35019

    Article  CAS  PubMed  Google Scholar 

  20. Zhang L, Yan J, Yin Z, Tang C, Guo Y, Li D, Wei B, Xu Y, Gu Q, Wang L (2014) Electrospun vancomycin-loaded coating on titanium implants for the prevention of implant-associated infections. Int J Nanomedicine 9:3027–3036. https://doi.org/10.2147/IJN.S63991eCollection 2014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Deeks JJ, Higgins JPT, Altman DG (2008) Chapter 9: analysing data and undertaking meta-analyses. In: Higgins JPT, Green S (eds) Cochrane handbook for systematic reviews of interventions. John Wiley & Sons, Chichester (UK)

    Google Scholar 

  22. Review Manager (RevMan) [Computer program]. Version 5.3. Copenhagen: The Nordic Cochrane Centre, The Cochrane Collaboration, 2014

  23. Schunemann HJ, Oxman AD, Vist GE, Higgins JPT, Deeks JJ, Glasziou P, Guyatt GH (2008) Chapter 12: interpreting results and drawing conclusions. In: Higgins JPT, Green S (eds) Cochrane handbook for systematic reviews of interventions. John Wiley & Sons, Chichester (UK)

    Google Scholar 

  24. Cohen J (1988) Statistical power analysis for the behavioral sciences. Lawrence Erlbaum Associates, Hillsdale, NJ, U.S.A

    Google Scholar 

  25. Alt V, Kirchhof K, Seim F, Hrubesch I, Lips KS, Mannel H, Domann E, Schnettler R (2014) Rifampicin-fosfomycin coating for cementless endoprostheses: antimicrobial effects against methicillin-sensitive Staphylococcus aureus (MSSA) and methicillin-resistant Staphylococcus aureus (MRSA). Acta Biomater 10(10):4518–4524. https://doi.org/10.1016/j.actbio.2014.06.013

    Article  CAS  PubMed  Google Scholar 

  26. Cao H, Qin H, Zhao Y, Jin G, Lu T, Meng F, Zhang X, Liu X (2016) Nano-thick calcium oxide armed titanium: boosts bone cells against methicillin-resistant Staphylococcus aureus. Sci Rep 6:21761. https://doi.org/10.1038/srep21761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Kose N, Çaylak R, Pekşen C, Kiremitçi A, Burukoglu D, Koparal S, Doğan A (2015) Silver ion doped ceramic nano-powder coated nails prevent infection in open fractures: in vivo study. Injury 47(2):320–324. https://doi.org/10.1016/j.injury.2015.10.006

  28. Metsemakers WJ, Emanuel N, Cohen O, Reichart M, Potapova I, Schmid T, Segal D, Riool M, Kwakman PH, de Boer L, de Breij A, Nibbering PH, Richards RG, Zaat SA, Moriarty TF (2015) A doxycycline-loaded polymer-lipid encapsulation matrix coating for the prevention of implant-related osteomyelitis due to doxycycline-resistant methicillin-resistant Staphylococcus aureus. J Control Release 209:47–56. https://doi.org/10.1016/j.jconrel.2015.04.022

    Article  CAS  PubMed  Google Scholar 

  29. Nie B, Ao H, Long T, Zhou J, Tang T, Yue B (2017) Immobilizing bacitracin on titanium for prophylaxis of infections and for improving osteoinductivity: an in vivo study. Colloids Surf B: Biointerfaces 150:183–191. https://doi.org/10.1016/j.colsurfb.2016.11.034

    Article  CAS  PubMed  Google Scholar 

  30. Sinclair KD, Pham TX, Williams DL, Farnsworth RW, Loc-Carrillo CM, Bloebaum RD (2013) Model development for determining the efficacy of a combination coating for the prevention of perioperative device related infections: a pilot study. J Biomed Mater Res B Appl Biomater 101(7):1143–1153. https://doi.org/10.1002/jbm.b.32924

    Article  CAS  PubMed  Google Scholar 

  31. Moojen DJ, Vogely HC, Fleer A, Nikkels PG, Higham PA, Verbout AJ, Castelein RM, Dhert WJ (2009) Prophylaxis of infection and effects on osseointegration using a tobramycin-periapatite coating on titanium implants--an experimental study in the rabbit. J Orthop Res 27(6):710–716. https://doi.org/10.1002/jor.20808

    Article  CAS  PubMed  Google Scholar 

  32. Bouloussa H, Humblot V, Court C (2017) Comparative description of in vitro and in vivo MRSA biofilms on titanium surfaces: why animal models still matter. Spine J 17(10):S167–S168

    Article  Google Scholar 

  33. Croes M, Bakhshandeh S, van Hengel IAJ, Lietaert K, van Kessel KPM, Pouran B, van der Wal BCH, Vogely HC, Van Hecke W, Fluit AC, Boel CHE, Alblas J, Zadpoor AA, Weinans H, Amin Yavari S (2018) Antibacterial and immunogenic behavior of silver coatings on additively manufactured porous titanium. Acta Biomater 81:315–327. https://doi.org/10.1016/j.actbio.2018.09.051

    Article  CAS  PubMed  Google Scholar 

  34. Darouiche RO, Mansouri MD, Zakarevicz D, Alsharif A, Landon GC (2007) In vivo efficacy of antimicrobial-coated devices. J Bone Joint Surg Am 89(4):792–797

    Article  PubMed  Google Scholar 

  35. de Breij A, Riool M, Kwakman PH, de Boer L, Cordfunke RA, Drijfhout JW, Cohen O, Emanuel N, Zaat SA, Nibbering PH, Moriarty TF (2016) Prevention of Staphylococcus aureus biomaterial-associated infections using a polymer-lipid coating containing the antimicrobial peptide OP-145. J Control Release 222:1–8. https://doi.org/10.1016/j.jconrel.2015.12.003

    Article  CAS  PubMed  Google Scholar 

  36. Diefenbeck M, Schrader C, Gras F, Mückley T, Schmidt J, Zankovych S, Bossert J, Jandt KD, Völpel A, Sigusch BW, Schubert H, Bischoff S, Pfister W, Edel B, Faucon M, Finger U (2016) Gentamicin coating of plasma chemical oxidized titanium alloy prevents implant-related osteomyelitis in rats. Biomaterials 101:156–164. https://doi.org/10.1016/j.biomaterials.2016.05.039

    Article  CAS  PubMed  Google Scholar 

  37. Inoue D, Kabata T, Ohtani K, Kajino Y, Shirai T, Tsuchiya H (2017) Inhibition of biofilm formation on iodine-supported titanium implants. Int Orthop 41(6):1093–1099. https://doi.org/10.1007/s00264-017-3477-3Epub 2017 Apr 7

    Article  PubMed  Google Scholar 

  38. Liu D, He C, Liu Z, Xu W (2017) Gentamicin coating of nanotubular anodized titanium implant reduces implant-related osteomyelitis and enhances bone biocompatibility in rabbits. Int J Nanomedicine 12:5461–5471. https://doi.org/10.2147/IJN.S137137eCollection 2017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Lovati AB, Bottagisio M, Maraldi S, Violatto MB, Bortolin M, De Vecchi E, Bigini P, Drago L, Romanò CL (2018) Vitamin E phosphate coating stimulates bone deposition in implant-related infections in a rat model. Clin Orthop Relat Res 476(6):1324–1338. https://doi.org/10.1097/01.blo.0000534692.41467.02

    Article  PubMed  PubMed Central  Google Scholar 

  40. Riool M, Dirks AJ, Jaspers V, de Boer L, Loontjens TJ, van der Loos CM, Florquin S, Apachitei I, Rijk LN, Keul HA, Zaat SA (2017) A chlorhexidine-releasing epoxy-based coating on titanium implants prevents Staphylococcus aureus experimental biomaterial-associated infection. Eur Cell Mater 33:143–157. https://doi.org/10.22203/eCM.v033a11

    Article  CAS  PubMed  Google Scholar 

  41. Stewart S, Barr S, Engiles J, Hickok NJ, Shapiro IM, Richardson DW, Parvizi J, Schaer TP (2012) Vancomycin-modified implant surface inhibits biofilm formation and supports bone-healing in an infected osteotomy model in sheep: a proof-of-concept study. J Bone Joint Surg Am 94(15):1406–1415. https://doi.org/10.2106/JBJS.K.00886

    Article  PubMed  PubMed Central  Google Scholar 

  42. Antoci V Jr, Adams CS, Parvizi J, Ducheyne P, Shapiro IM, Hickok NJ (2007) Covalently attached vancomycin provides a nanoscale antibacterial surface. Clin Orthop Relat Res 461:81–87

    Article  PubMed  Google Scholar 

  43. Cashman JD, Jackson JK, Mugabe C, Gilchrist S, Ball K, Tredwell S, Burt HM (2013) The use of tissue sealants to deliver antibiotics to an orthopaedic surgical site with a titanium implant. J Orthop Sci 18(1):165–174. https://doi.org/10.1007/s00776-012-0325-6

    Article  CAS  PubMed  Google Scholar 

  44. Li D, Lv P, Fan L, Huang Y, Yang F, Mei X, Wu D (2017) The immobilization of antibiotic-loaded polymeric coatings on osteoarticular Ti implants for the prevention of bone infections. Biomater Sci 5(11):2337–2346. https://doi.org/10.1039/c7bm00693d

    Article  CAS  PubMed  Google Scholar 

  45. Lucke M, Schmidmaier G, Sadoni S, Wildemann B, Schiller R, Haas NP, Raschke M (2003) Gentamicin coating of metallic implants reduces implant-related osteomyelitis in rats. Bone 32(5):521–531

    Article  CAS  PubMed  Google Scholar 

  46. Prinz C, Elhensheri M, Rychly J, Neumann HG (2017) Antimicrobial and bone-forming activity of a copper coated implant in a rabbit model. J Biomater Appl 32(2):139–149. https://doi.org/10.1177/0885328217713356

    Article  CAS  PubMed  Google Scholar 

  47. Windolf CD, Lögters T, Scholz M, Windolf J, Flohé S (2014) Lysostaphin-coated titan-implants preventing localized osteitis by Staphylococcus aureus in a mouse model. PLoS One 9(12):e115940. https://doi.org/10.1371/journal.pone.0115940eCollection 2014

  48. Xie K, Zhou Z, Guo Y, Wang L, Li G, Zhao S, Liu X, Li J, Jiang W, Wu S, Hao Y (2019) Long-term prevention of bacterial infection and enhanced osteoinductivity of a hybrid coating with selective silver toxicity. Adv Healthc Mater 8(5):e1801465. https://doi.org/10.1002/adhm.201801465

    Article  CAS  PubMed  Google Scholar 

  49. Yang Y, Ao HY, Yang SB, Wang YG, Lin WT, Yu ZF, Tang TT (2016) In vivo evaluation of the anti-infection potential of gentamicin-loaded nanotubes on titania implants. Int J Nanomedicine 11:2223–2234. https://doi.org/10.2147/IJN.S102752eCollection 2016

  50. Terrin N, Schmid CH, Lau J (2005) In an empirical evaluation of the funnel plot, researchers could not visually identify publication bias. J Clin Epidemiol 58(9):894–901

    Article  PubMed  Google Scholar 

  51. Higgins JP, Thompson SG (2004) Controlling the risk of spurious findings from meta-regression. Stat Med 23(11):1663–1682

    Article  PubMed  Google Scholar 

  52. Sterne JA, Sutton AJ, Ioannidis JP, Terrin N, Jones DR, Lau J, Carpenter J, Rücker G, Harbord RM, Schmid CH, Tetzlaff J, Deeks JJ, Peters J, Macaskill P, Schwarzer G, Duval S, Altman DG, Moher D, Higgins JP (2011) Recommendations for examining and interpreting funnel plot asymmetry in meta-analyses of randomised controlled trials. BMJ 343:d4002. https://doi.org/10.1136/bmj.d4002

    Article  PubMed  Google Scholar 

  53. Corvec S, Portillo ME, Pasticci BM, Borens O, Trampuz A (2012) Epidemiology and new developments in the diagnosis of prosthetic joint infection. Int J Artif Organs 35(10):923–934. https://doi.org/10.5301/ijao.5000168

    Article  PubMed  Google Scholar 

  54. Tande AJ, Patel R (2014) Prosthetic joint infection. Clin Microbiol Rev 27(2):302–345. https://doi.org/10.1128/CMR.00111-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Romanò CL, Malizos K, Capuano N, Mezzoprete R, D’Arienzo M, Van Der Straeten C, Scarponi S, Drago L (2016) Does an antibiotic-loaded hydrogel coating reduce early post-surgical infection after joint arthroplasty? J Bone Jt Infect 1:34–41. https://doi.org/10.7150/jbji.15986eCollection 2016

    Article  PubMed  PubMed Central  Google Scholar 

  56. Malizos K, Blauth M, Danita A, Capuano N, Mezzoprete R, Logoluso N, Drago L, Romanò CL (2017) Fast-resorbable antibiotic-loaded hydrogel coating to reduce post-surgical infection after internal osteosynthesis: a multicenter randomized controlled trial. J Orthop Traumatol 18(2):159–169. https://doi.org/10.1007/s10195-017-0442-2

    Article  PubMed  PubMed Central  Google Scholar 

  57. Schmidmaier G, Kerstan M, Schwabe P, Südkamp N, Raschke M (2017) Clinical experiences in the use of a gentamicin-coated titanium nail in tibia fractures. Injury 48(10):2235–2241. https://doi.org/10.1016/j.injury.2017.07.008

    Article  CAS  PubMed  Google Scholar 

  58. Raschke M, Vordemvenne T, Fuchs T (2010) Limb salvage or amputation? The use of a gentamicin coated nail in a severe, grade IIIc tibia fracture. Eur J Trauma Emerg Surg 36(6):605–608. https://doi.org/10.1007/s00068-010-0017-x

    Article  CAS  PubMed  Google Scholar 

  59. Fuchs T, Stange R, Schmidmaier G, Raschke MJ (2011) The use of gentamicin-coated nails in the tibia: preliminary results of a prospective study. Arch Orthop Trauma Surg 131(10):1419–1425. https://doi.org/10.1007/s00402-011-1321-6

    Article  PubMed  PubMed Central  Google Scholar 

  60. Metsemakers WJ, Reul M, Nijs S (2015) The use of gentamicin-coated nails in complex open tibia fracture and revision cases: a retrospective analysis of a single centre case series and review of the literature. Injury 46(12):2433–2437. https://doi.org/10.1016/j.injury.2015.09.028

    Article  CAS  PubMed  Google Scholar 

  61. Tsuchiya H, Shirai T, Nishida H, Murakami H, Kabata T, Yamamoto N, Watanabe K, Nakase J (2012) Innovative antimicrobial coating of titanium implants with iodine. J Orthop Sci 17(5):595–604. https://doi.org/10.1007/s00776-012-0247-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Shirai T, Tsuchiya H, Nishida H, Yamamoto N, Watanabe K, Nakase J, Terauchi R, Arai Y, Fujiwara H, Kubo T (2014) Antimicrobial megaprostheses supported with iodine. J Biomater Appl 29(4):617–623. https://doi.org/10.1177/0885328214539365

    Article  CAS  PubMed  Google Scholar 

  63. Chen M, Yu Q, Sun H (2013) Novel strategies for the prevention and treatment of biofilm related infections. Int J Mol Sci 14(9):18488–18501. https://doi.org/10.3390/ijms140918488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Leopold SS (2014) Editorial: when “safe and effective” becomes dangerous. Clin Orthop Relat Res 472(7):1999–2001. https://doi.org/10.1007/s11999-014-3675-x

    Article  PubMed  PubMed Central  Google Scholar 

  65. Fernández-Sampedro M, Fariñas-Alvarez C, Garces-Zarzalejo C, Alonso-Aguirre MA, Salas-Venero C, Martínez-Martínez L, Fariñas MC (2017) Accuracy of different diagnostic tests for early, delayed and late prosthetic joint infection. BMC Infect Dis 17(1):592. https://doi.org/10.1186/s12879-017-2693-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We are grateful to Dimitris Mavridis, PhD, from University of Ioannina Greece for providing us with statistical support throughout the study.

Author information

Authors and Affiliations

  1. Orthopaedic Department, Royal Surrey Hospital, Guildford, UK

    Konstantinos Tsikopoulos

  2. Orthopaedic Department, General Hospital of Serres, Drama, Greece

    Konstantinos Sidiropoulos

  3. 1st Orthopaedic Department of Aristotle University, G. Papanikolaou General Hospital, Exohi, Thessaloniki, Greece

    Dimitrios Kitridis

  4. Orthopaedic Department, Lister Hospital, Stevenage, East and North Hertfordshire, UK

    Anas Hassan

  5. Laboratory of Clinical Microbiology, Department of Biochemical Sciences for Health, University of Milan, Milan, Italy

    Lorenzo Drago

  6. Orthopaedic Department, National and Kapodistrian University of Athens, Athens, Greece

    Andreas Mavrogenis

  7. Orthopaedic Department, University Hospitals of North Midlands, Stoke-on-Trent, UK

    Donald McBride

Authors
  1. Konstantinos Tsikopoulos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Konstantinos Sidiropoulos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dimitrios Kitridis
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anas Hassan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lorenzo Drago
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Andreas Mavrogenis
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Donald McBride
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Konstantinos Tsikopoulos.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(PDF 152 kb)

ESM 2

(PDF 115 kb)

ESM 3

(PDF 125 kb)

ESM 4

(DOCX 13 kb)

ESM 5

(DOCX 23 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tsikopoulos, K., Sidiropoulos, K., Kitridis, D. et al. Is coating of titanium implants effective at preventing Staphylococcus aureus infections? A meta-analysis of animal model studies. International Orthopaedics (SICOT) 45, 821–835 (2021). https://doi.org/10.1007/s00264-020-04660-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00264-020-04660-4

Keywords

Search

Navigation