Bacteria–Biomaterial Interactions

  • Antti Soininen
  • Emilia Kaivosoja
  • Jaime Esteban
  • Riina Rautemaa-Richardson
  • Alberto Ortiz-Pérez
  • Gonçalo Barretto
  • Yrjö T. KonttinenEmail author


The prevalence of orthopedic implant-related (deep) infections is approximately 0.5–1.5 %. They are divided to early (<1 months after the implantation) and delayed (1 months–2 years after the implantation) infections, which are somewhat overlapping with late infections (over 1–2 years after the implantation). Early and delayed infections are usually caused by direct contamination during the operation by more or less virulent microbes in patients with lowered local and/or systemic bacterial resistance, but late infections are usually hematogenous. Microbes in the body are usually fought back in healthy living tissues, but implantation-associated hemorrhage and the abiotic implants form an unprotected surface, locus minoris resistentiae. Here, planktonic bacteria easily adhere and soon form a protective extracellular polymeric substance (EPS, biofilm, “bacterial slime”) and transform to dormant but intercommunicating and even polymicrobial colonies. Embedded in the biofilm, antibiotics cannot by diffusion reach high enough (therapeutic concentrations), and suboptimal concentrations only select for resistant strains. Leukocytes, antibodies, and complement have poor access to biofilms. Further, using quorum sensing, biofilm bacteria behave very intelligently, adjusting the colonies to various threats to their existence, by adjusting the bacterial population to a size which realistically can survive, by developing antibiotic resistance and exchanging resistance between themselves, and by developing organized structures so that the microbes at every layer and depth have adjusted to their local micromilieu, e.g., oxygen tension, nutrients, EPS composition, antibiotics, and antifungals. If the in vivo “culture conditions” are favorable for the microbes, e.g., due to developing immunosuppression of the host, colonies can activate and start to send metastatic satellites to invade adjacent and remote new sites (foci). Removal of the infected implant is often the only effective therapy but happens at the cost of the implant, with antibiotics only playing an adjunct role. Diagnosis can be verified by detaching biofilm hidden bacteria by ultrasonication from the retrieved implant contained in fluid in a plastic bag and by combining routine microbial diagnosis, such as culture and staining, with more modern polymerase chain reaction analysis of the microbial DNA. The race between evolutionary antimicrobial resistance development and the drug companies developing new antibiotics seems to be tipping in favor of microbes. Therefore, intelligent use of systemic and local antibiotic prophylaxis, disinfection, aseptic techniques, testing of eventual carriers of resistant but asymptomatic strains, and separating carriers from clean but infection-prone patients are important principles. The development of implants and implant coatings able to resist bacterial adhesion and colonization is important, and new antimicrobial drugs working using new modes of action, e.g., based on the use of bacteriophages, should get more scientific attention.


Bacteria Cytokine Biomaterial Adhesion Coatings 


  1. 1.
    Lew DP, Waldvogel FA. Osteomyelitis. N Engl J Med. 1997;336(14):999–1007.PubMedCrossRefGoogle Scholar
  2. 2.
    Lowy FD. Medical progress – Staphylococcus aureus infections. N Engl J Med. 1998;339(8):520–32.PubMedCrossRefGoogle Scholar
  3. 3.
    Sanderson PJ. Infection in orthopedic implants. J Hosp Infect. 1991;18:367–75.PubMedCrossRefGoogle Scholar
  4. 4.
    Romero R, Schaudinn C, Kusanovic JP, Gorur A, Gotsch F, Webster P, Nhan-Chang CL, Erez O, Kim CJ, Espinoza J, Goncalves LF, Vaisbuch E, Mazaki-Tovi S, Hassan SS, Costerton JW. Detection of a microbial biofilm in intraamniotic infection. Am J Obstet Gynecol. 2008;198(1):135. doi: 10.1016/j.ajog.2007.11.026.PubMedGoogle Scholar
  5. 5.
    Ghannoum M, O’Toole GA. Microbial biofilms. Washington, DC: ASM Press; 2004.Google Scholar
  6. 6.
    Knobloch JKM, von Osten H, Horstkotte MA, Rohde H, Mack D. Minimal attachment killing (MAK): a versatile method for susceptibility testing of attached biofilm-positive and -negative Staphylococcus epidermidis. Med Microbiol Immunol. 2002;191(2):107–14. doi: 10.1007/s00430-002-0125-2.PubMedCrossRefGoogle Scholar
  7. 7.
    Otto M, Kong KF, Vuong C. Staphylococcus quorum sensing in biofilm formation and infection. Int J Med Microbiol. 2006;296(2–3):133–9. doi: 10.1016/j.ijmm.2006.01.042.PubMedGoogle Scholar
  8. 8.
    Otto M. Quorum-sensing control in Staphylococci – a target for antimicrobial drug therapy? FEMS Microbiol Lett. 2004;241(2):135–41. doi: 10.1016/j.femsle.2004.11.016.PubMedCrossRefGoogle Scholar
  9. 9.
    Hench LL, Thompson I. Twenty-first century challenges for biomaterials. J R Soc Interface. 2010;7:S379–91. doi: 10.1098/rsif.2010.0151.focus.PubMedCrossRefGoogle Scholar
  10. 10.
    Wenzel RP. Health care-associated infections: major issues in the early years of the 21st century. Clin Infect Dis. 2007;45:85–8. doi: 10.1086/518136.CrossRefGoogle Scholar
  11. 11.
    Klevens RM, Edwards JR, Richards CL, Horan TC, Gaynes RP, Pollock DA, Cardo DM. Estimating health care-associated infections and deaths in US hospitals, 2002. Public Health Rep. 2007;122(2):160–6.PubMedGoogle Scholar
  12. 12.
    van der Mei HC, Fernandez ICS, Metzger S, Grainger DW, Engelsman AF, Nejadnik MR, Busscher HJ. In vitro and in vivo comparisons of staphylococcal biofilm formation on a cross-linked poly(ethylene glycol)-based polymer coating. Acta Biomater. 2010;6(3):1119–24. doi: 10.1016/j.actbio.2009.08.040.PubMedCrossRefGoogle Scholar
  13. 13.
    Sousa C. Staphylococcus epidermidis: adhesion and biofilm formation onto biomaterials. Saarbrücken: LAP LAMBERT Academic Publishing; 2011.Google Scholar
  14. 14.
    An YH, Friedman RJ. Concise review of mechanisms of bacterial adhesion to biomaterial surfaces. J Biomed Mater Res. 1998;43(3):338–48.PubMedCrossRefGoogle Scholar
  15. 15.
    Miller LG, Perlroth J, Kuo M, Tan J, Bayer AS. Adjunctive use of rifampin for the treatment of Staphylococcus aureus infections. Arch Intern Med. 2008;168(8):805–19.PubMedCrossRefGoogle Scholar
  16. 16.
    Svensater G, Welin J, Wilkins JC, Beighton D, Hamilton IR. Protein expression by planktonic and biofilm cells of Streptococcus mutans. FEMS Microbiol Lett. 2001;205(1):139–46.PubMedCrossRefGoogle Scholar
  17. 17.
    Gal L, Rollet C, Guzzo J. Biofilm-detached cells, a transition from a sessile to a planktonic phenotype: a comparative study of adhesion and physiological characteristics in Pseudomonas aeruginosa. FEMS Microbiol Lett. 2009;290(2):135–42. doi: 10.1111/j.1574-6968.2008.01415.x.PubMedGoogle Scholar
  18. 18.
    Kinnari TJ, Soininen A, Esteban J, Zamora N, Alakoski E, Kouri VP, Lappalainen R, Konttinen YT, Gomez-Barrena E, Tiainen VM. Adhesion of staphylococcal and Caco-2 cells on diamond-like carbon polymer hybrid coating. J Biomed Mater Res A. 2008;86A(3):760–8. doi: 10.1002/jbm.a.31643.CrossRefGoogle Scholar
  19. 19.
    Konttinen YT, Levon J, Myllymaa K, Kouri VP, Rautemaa R, Kinnari T, Myllymaa S, Lappalainen R. Patterned macroarray plates in comparison of bacterial adhesion inhibition of tantalum, titanium, and chromium compared with diamond-like carbon. J Biomed Mater Res A. 2010;92A(4):1606–13. doi: 10.1002/jbm.a.32486.Google Scholar
  20. 20.
    Kinnari TJ, Peltonen LI, Kuusela T, Kivilahti J, Kononen M, Jero J. Bacterial adherence to titanium surface coated with human serum albumin. Otol Neurotol. 2005;26(3):380–4.PubMedCrossRefGoogle Scholar
  21. 21.
    Soininen A, Tiainen VM, Konttinen YT, van der Mei HC, Busscher HJ, Sharma PK. Bacterial adhesion to diamond-like carbon as compared to stainless steel. J Biomed Mater Res B Appl Biomater. 2009;90B(2):882–5. doi: 10.1002/jbm.b.31359.CrossRefGoogle Scholar
  22. 22.
    Soininen A, Levon J, Katsikogianni M, Myllymaa K, Lappalainen R, Konttinen YT, Kinnari TJ, Tiainen VM, Missirlis Y. In vitro adhesion of staphylococci to diamond-like carbon polymer hybrids under dynamic flow conditions. J Mater Sci Mater Med. 2011;22(3):629–36. doi: 10.1007/s10856-011-4231-9.PubMedCrossRefGoogle Scholar
  23. 23.
    Dailloux M, Albert M, Laurain C, Andolfatto S, Lozniewski A, Hartemann P, Mathieu L. Mycobacterium xenopi and drinking water biofilms. Appl Environ Microbiol. 2003;69(11):6946–8.PubMedCrossRefGoogle Scholar
  24. 24.
    September SM, Brozel VS, Venter SN. Diversity of nontuberculoid Mycobacterium species in biofilms of urban and semiurban drinking water distribution systems. Appl Environ Microbiol. 2004;70(12):7571–3. doi: 10.1128/AEM.70.12.7571-7573.2004. PII:70/12/7571.PubMedCrossRefGoogle Scholar
  25. 25.
    Falkinham 3rd JO, Norton CD, LeChevallier MW. Factors influencing numbers of Mycobacterium avium, Mycobacterium intracellulare, and other Mycobacteria in drinking water distribution systems. Appl Environ Microbiol. 2001;67(3):1225–31. doi: 10.1128/AEM.67.3.1225-1231.2001.PubMedCrossRefGoogle Scholar
  26. 26.
    Marshall HM, Carter R, Torbey MJ, Minion S, Tolson C, Sidjabat HE, Huygens F, Hargreaves M, Thomson RM. Mycobacterium lentiflavum in drinking water supplies, Australia. Emerg Infect Dis. 2011;17(3):395–402.PubMedCrossRefGoogle Scholar
  27. 27.
    Esteban J, Martin-de-Hijas NZ, Kinnari TJ, Ayala G, Fernandez-Roblas R, Gadea I. Biofilm development by potentially pathogenic non-pigmented rapidly growing mycobacteria. BMC Microbiol. 2008;8:184. doi: 10.1186/1471-2180-8-184. PII:1471-2180-8-184.PubMedCrossRefGoogle Scholar
  28. 28.
    Costerton JW. Biofilm theory can guide the treatment of device-related orthopaedic infections. Clin Orthop Relat Res. 2005;437:7–11. PII:00003086-200508000-00003.PubMedCrossRefGoogle Scholar
  29. 29.
    Donlan RM, Costerton JW. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev. 2002;15(2):167–93.PubMedCrossRefGoogle Scholar
  30. 30.
    Hall-Stoodley L, Lappin-Scott H. Biofilm formation by the rapidly growing mycobacterial species Mycobacterium fortuitum. FEMS Microbiol Lett. 1998;168(1):77–84. PII:S0378-1097(98)00422-4.PubMedCrossRefGoogle Scholar
  31. 31.
    Martinez A, Torello S, Kolter R. Sliding motility in mycobacteria. J Bacteriol. 1999;181(23):7331–8.PubMedGoogle Scholar
  32. 32.
    Carter G, Wu M, Drummond DC, Bermudez LE. Characterization of biofilm formation by clinical isolates of Mycobacterium avium. J Med Microbiol. 2003;52(Pt 9):747–52.PubMedCrossRefGoogle Scholar
  33. 33.
    Recht J, Martinez A, Torello S, Kolter R. Genetic analysis of sliding motility in Mycobacterium smegmatis. J Bacteriol. 2000;182(15):4348–51.PubMedCrossRefGoogle Scholar
  34. 34.
    Yamazaki Y, Danelishvili L, Wu M, Macnab M, Bermudez LE. Mycobacterium avium genes associated with the ability to form a biofilm. Appl Environ Microbiol. 2006;72(1):819–25. doi: 10.1128/AEM.72.1.819-825.2006. PII:72/1/819.PubMedCrossRefGoogle Scholar
  35. 35.
    Recht J, Kolter R. Glycopeptidolipid acetylation affects sliding motility and biofilm formation in Mycobacterium smegmatis. J Bacteriol. 2001;183(19):5718–24. doi: 10.1128/JB.183.19.5718-5724.2001.PubMedCrossRefGoogle Scholar
  36. 36.
    Arora K, Whiteford DC, Lau-Bonilla D, Davitt CM, Dahl JL. Inactivation of lsr2 results in a hypermotile phenotype in Mycobacterium smegmatis. J Bacteriol. 2008;190(12):4291–300. doi: 10.1128/JB.00023-08. PII:JB.00023-08.PubMedCrossRefGoogle Scholar
  37. 37.
    Ojha A, Anand M, Bhatt A, Kremer L, Jacobs Jr WR, Hatfull GF. GroEL1: a dedicated chaperone involved in mycolic acid biosynthesis during biofilm formation in mycobacteria. Cell. 2005;123(5):861–73. doi: 10.1016/j.cell.2005.09.012. PII:S0092-8674(05)00965-7.PubMedCrossRefGoogle Scholar
  38. 38.
    Nessar R, Reyrat JM, Davidson LB, Byrd TF. Deletion of the mmpL4b gene in the Mycobacterium abscessus glycopeptidolipid biosynthetic pathway results in loss of surface colonization capability, but enhanced ability to replicate in human macrophages and stimulate their innate immune response. Microbiology. 2011. doi: 10.1099/mic.0.046557-0. PII:mic.0.046557-0.
  39. 39.
    Deshayes C, Bach H, Euphrasie D, Attarian R, Coureuil M, Sougakoff W, Laval F, Av-Gay Y, Daffe M, Etienne G, Reyrat JM. MmpS4 promotes glycopeptidolipids biosynthesis and export in Mycobacterium smegmatis. Mol Microbiol. 2010;78(4):989–1003. doi: 10.1111/j.1365-2958.2010.07385.x.PubMedCrossRefGoogle Scholar
  40. 40.
    Deshayes C, Laval F, Montrozier H, Daffe M, Etienne G, Reyrat JM. A glycosyltransferase involved in biosynthesis of triglycosylated glycopeptidolipids in Mycobacterium smegmatis: impact on surface properties. J Bacteriol. 2005;187(21):7283–91. doi: 10.1128/JB.187.21.7283-7291.2005. PII:187/21/7283.PubMedCrossRefGoogle Scholar
  41. 41.
    Kocincova D, Singh AK, Beretti JL, Ren H, Euphrasie D, Liu J, Daffe M, Etienne G, Reyrat JM. Spontaneous transposition of IS1096 or ISMsm3 leads to glycopeptidolipid overproduction and affects surface properties in Mycobacterium smegmatis. Tuberculosis (Edinb). 2008;88(5):390–8. doi: 10.1016/ PII:S1472-9792(08)00021-8.CrossRefGoogle Scholar
  42. 42.
    Kocincova D, Winter N, Euphrasie D, Daffe M, Reyrat JM, Etienne G. The cell surface-exposed glycopeptidolipids confer a selective advantage to the smooth variants of Mycobacterium smegmatis in vitro. FEMS Microbiol Lett. 2009;290(1):39–44. doi: 10.1111/j.1574-6968.2008.01396.x. PII:FML1396.PubMedCrossRefGoogle Scholar
  43. 43.
    Esteban J, Martin-de-Hijas NZ, Fernandez AI, Fernandez-Roblas R, Gadea I. Epidemiology of infections due to nonpigmented rapidly growing mycobacteria diagnosed in an urban area. Eur J Clin Microbiol Infect Dis. 2008;27(10):951–7. doi: 10.1007/s10096-008-0521-7.PubMedCrossRefGoogle Scholar
  44. 44.
    Martin-de-Hijas NZ, Garcia-Almeida D, Ayala G, Fernandez-Roblas R, Gadea I, Celdran A, Gomez-Barrena E, Esteban J. Biofilm development by clinical strains of non-pigmented rapidly growing mycobacteria. Clin Microbiol Infect. 2009;15(10):931–6. doi: 10.1111/j.1469-0691.2009.02882.x. PII:CLM2882.PubMedCrossRefGoogle Scholar
  45. 45.
    Byrd TF, Lyons CR. Preliminary characterization of a Mycobacterium abscessus mutant in human and murine models of infection. Infect Immun. 1999;67(9):4700–7.PubMedGoogle Scholar
  46. 46.
    Falkinham 3rd JO. Growth in catheter biofilms and antibiotic resistance of Mycobacterium avium. J Med Microbiol. 2007;56(Pt 2):250–4. doi: 10.1099/jmm.0.46935-0. PII:56/2/250.PubMedCrossRefGoogle Scholar
  47. 47.
    Greendyke R, Byrd TF. Differential antibiotic susceptibility of Mycobacterium abscessus variants in biofilms and macrophages compared to that of planktonic bacteria. Antimicrob Agents Chemother. 2008;52(6):2019–26. doi: 10.1128/AAC.00986-07. PII:AAC.00986-07.PubMedCrossRefGoogle Scholar
  48. 48.
    Ortiz-Perez A, Martin-de-Hijas N, Alonso-Rodriguez N, Molina-Manso D, Fernandez-Roblas R, Esteban J. Importance of antibiotic penetration in the antimicrobial resistance of biofilm formed by non-pigmented rapidly growing mycobacteria against amikacin, ciprofloxacin and clarithromycin. Enferm Infecc Microbiol Clin. 2011;29(2):79–84. doi: 10.1016/j.eimc.2010.08.016. PII:S0213-005X(10)00451-9.PubMedCrossRefGoogle Scholar
  49. 49.
    Ha KY, Chung YG, Ryoo SJ. Adherence and biofilm formation of Staphylococcus epidermidis and Mycobacterium tuberculosis on various spinal implants. Spine (Phila Pa 1976). 2005;30(1):38–43. PII:00007632-200501010-00008.Google Scholar
  50. 50.
    Ojha AK, Baughn AD, Sambandan D, Hsu T, Trivelli X, Guerardel Y, Alahari A, Kremer L, Jacobs Jr WR, Hatfull GF. Growth of Mycobacterium tuberculosis biofilms containing free mycolic acids and harbouring drug-tolerant bacteria. Mol Microbiol. 2008;69(1):164–74. doi: 10.1111/j.1365-2958.2008.06274.x. PII:MMI6274.PubMedCrossRefGoogle Scholar
  51. 51.
    Brown A, Grubbs P, Mongey AB. Infection of total hip prosthesis by Mycobacterium tuberculosis and Mycobacterium chelonae in a patient with rheumatoid arthritis. Clin Rheumatol. 2008;27(4):543–5. doi: 10.1007/s10067-007-0788-6.PubMedCrossRefGoogle Scholar
  52. 52.
    Fernandez-Valencia JA, Garcia S, Riba J. Presumptive infection of a total hip prosthesis by Mycobacterium tuberculosis: a case report. Acta Orthop Belg. 2003;69(2):193–6.PubMedGoogle Scholar
  53. 53.
    Wright RA, Yang F, Moore WS. Tuberculous infection in a vascular prosthesis: a case of aortic graft infection resulting from disseminated tuberculosis. Arch Surg. 1977;112(1):79–81.PubMedCrossRefGoogle Scholar
  54. 54.
    Eskola A, Santavirta S, Konttinen YT, Tallroth K, Hoikka V, Lindholm ST. Cementless total replacement for old tuberculosis of the hip. J Bone Joint Surg Br. 1988;70(4):603–6.PubMedGoogle Scholar
  55. 55.
    Santavirta S, Eskola A, Konttinen YT, Tallroth K, Lindholm ST. Total hip-replacement in old tuberculosis - a report of 14 cases. Acta Orthop Scand. 1988;59(4):391–5.PubMedCrossRefGoogle Scholar
  56. 56.
    Eskola A, Santavirta S, Konttinen YT, Tallroth K, Lindholm ST. Arthroplasty for old tuberculosis of the knee. J Bone Joint Surg Br. 1988;70(5):767–9.PubMedGoogle Scholar
  57. 57.
    Rautemaa R, Ramage G. Oral candidiasis – clinical challenges of a biofilm disease. Crit Rev Microbiol. 2011;37(4):328–36.PubMedCrossRefGoogle Scholar
  58. 58.
    Younkin S, Evarts CM, Steigbigel RT. Candida-parapsilosis infection of a total hip-joint replacement – successful reimplantation after treatment with amphotericin-B and 5-fluorocytosine – a case-report. J Bone Joint Surg Am. 1984;66A(1):142–3.Google Scholar
  59. 59.
    Koch AE. Candida-albicans infection of a prosthetic knee replacement – a report and review of the literature. J Rheumatol. 1988;15(2):362–5.PubMedGoogle Scholar
  60. 60.
    Russell AD, Tattawasart U, Maillard JY, Furr JR. Possible link between bacterial resistance and use of antibiotics and biocides. Antimicrob Agents Chemother. 1998;42(8):2151–1.PubMedGoogle Scholar
  61. 61.
    Fischer D, Li YX, Ahlemeyer B, Krieglstein J, Kissel T. In vitro cytotoxicity testing of polycations: influence of polymer structure on cell viability and hemolysis. Biomaterials. 2003;24(7):1121–31.PubMedCrossRefGoogle Scholar
  62. 62.
    Youngblood JP, Stratton TR, Rickus JL. In vitro biocompatibility studies of antibacterial quaternary polymers. Biomacromolecules. 2009;10(9):2550–5. doi: 10.1021/bm9005003.PubMedCrossRefGoogle Scholar
  63. 63.
    Domb AJ, Beyth N, Houri-Haddad Y, Baraness-Hadar L, Yudovin-Farber I, Weiss EI. Surface antimicrobial activity and biocompatibility of incorporated polyethylenimine nanoparticles. Biomaterials. 2008;29(31):4157–63. doi: 10.1016/j.biomaterials.2008.07.003.PubMedCrossRefGoogle Scholar
  64. 64.
    Alexander JW. History of the medical use of silver. Surg Infect. 2009;10(3):289–92. doi: 10.1089/sur.2008.9941.CrossRefGoogle Scholar
  65. 65.
    Bayston R, Furno F, Morley KS, Wong B, Sharp BL, Arnold PL, Howdle SM, Brown PD, Winship PD, Reid HJ. Silver nanoparticles and polymeric medical devices: a new approach to prevention of infection? J Antimicrob Chemother. 2004;54(6):1019–24. doi: 10.1093/jac/dkh478.PubMedCrossRefGoogle Scholar
  66. 66.
    Raabe A, Fichtner J, Guresir E, Seifert V. Efficacy of silver-bearing external ventricular drainage catheters: a retrospective analysis clinical article. J Neurosurg. 2010;112(4):840–6. doi: 10.3171/2009.8.JNS091297.PubMedCrossRefGoogle Scholar
  67. 67.
    Lackner P, Beer R, Broessner G, Helbok R, Galiano K, Pleifer C, Pfausler B, Brenneis C, Huck C, Engelhardt K, Obwegeser AA, Schmutzhard E. Efficacy of silver nanoparticles-impregnated external ventricular drain catheters in patients with acute occlusive hydrocephalus. Neurocrit Care. 2008;8(3):360–5. doi: 10.1007/s12028-008-9071-1.PubMedCrossRefGoogle Scholar
  68. 68.
    Johnson JR, Kuskowski MA, Wilt TJ. Systematic review: Antimicrobial urinary catheters to prevent catheter-associated urinary tract infection in hospitalized patients. Ann Intern Med. 2006;144(2):116–26.PubMedGoogle Scholar
  69. 69.
    Trautner BW. Management of catheter-associated urinary tract infection. Curr Opin Infect Dis. 2010;23(1):76–82. doi: 10.1097/QCO.0b013e328334dda8.PubMedCrossRefGoogle Scholar
  70. 70.
    Gray M, Willson M, Wilde M, Webb ML, Thompson D, Parker D, Harwood J, Callan L. Nursing interventions to reduce the risk of catheter-associated urinary tract infection part 2: staff education, monitoring, and care techniques. J Wound Ostomy Continence Nurs. 2009;36(2):137–54.PubMedCrossRefGoogle Scholar
  71. 71.
    Gilbert RE, Harden M. Effectiveness of impregnated central venous catheters for catheter related blood stream infection: a systematic review. Curr Opin Infect Dis. 2008;21(3):235–45.PubMedCrossRefGoogle Scholar
  72. 72.
    Karthaus M, Jaeger K, Zenz S, Juttner B, Ruschulte H, Kuse E, Heine J, Piepenbrock S, Ganser A. Reduction of catheter-related infections in neutropenic patients: a prospective controlled randomized trial using a chlorhexidine and silver sulfadiazine-impregnated central venous catheter. Ann Hematol. 2005;84(4):258–62. doi: 10.1007/s00277-004-0972-6.PubMedCrossRefGoogle Scholar
  73. 73.
    Rupp ME, Lisco SJ, Lipsett PA, Ped TM, Keating K, Civetta JM, Mermel LA, Lee D, Dellinger EP, Donahoe M, Giles D, Pfaller MA, Maki DG, Sherertz R. Effect of a second-generation venous catheter impregnated with chlorhexidine and silver sulfadiazine on central catheter – related infections – a randomized, controlled trial. Ann Intern Med. 2005;143(8):570–80.PubMedGoogle Scholar
  74. 74.
    Bukhari SS, Khare MD, Swann A, Spiers P, McLaren L, Myers J. Reduction of catheter-related colonisation by the use of a silver zeolite-impregnated central vascular catheter in adult critical care. J Infect. 2007;54(2):146–50. doi: 10.1016/j.jinf.2006.03.002.PubMedCrossRefGoogle Scholar
  75. 75.
    Kalfon P, De Vaumas C, Samba D, Boulet E, Lefrant JY, Eyraud D, Lherm T, Santoli F, Naija W, Riou B. Comparison of silver-impregnated with standard multi-lumen central venous catheters in critically ill patients. Crit Care Med. 2007;35(4):1032–9. doi: 10.1097/01.Ccm.0000259378.53166.1b.PubMedCrossRefGoogle Scholar
  76. 76.
    Landmann R, Gordon O, Slenters TV, Brunetto PS, Villaruz AE, Sturdevant DE, Otto M, Fromm KM. Silver coordination polymers for prevention of implant infection: thiol interaction, impact on respiratory chain enzymes, and hydroxyl radical induction. Antimicrob Agents Chemother. 2010;54(10):4208–18. doi: 10.1128/Aac.01830-09.PubMedCrossRefGoogle Scholar
  77. 77.
    Drake PL, Hazelwood KJ. Exposure-related health effects of silver and silver compounds: a review. Ann Occup Hyg. 2005;49(7):575–85.PubMedCrossRefGoogle Scholar
  78. 78.
    Aberer W, Tomi NS, Kranke B. A silver man. Lancet. 2004;363(9408):532–2.PubMedCrossRefGoogle Scholar
  79. 79.
    Johnston HJ, Hutchison G, Christensen FM, Peters S, Hankin S, Stone V. A review of the in vivo and in vitro toxicity of silver and gold particulates: particle attributes and biological mechanisms responsible for the observed toxicity. Crit Rev Toxicol. 2010;40(4):328–46. doi: 10.3109/10408440903453074.PubMedCrossRefGoogle Scholar
  80. 80.
    Sondi I, Salopek-Sondi B. Silver nanoparticles as antimicrobial agent: a case study on E-coli as a model for Gram-negative bacteria. J Colloid Interface Sci. 2004;275(1):177–82. doi: 10.1016/j.jcis.2004.02.012.PubMedCrossRefGoogle Scholar
  81. 81.
    Mayr M, Kim MJ, Wanner D, Helmut H, Schroeder J, Mihatsch MJ. Argyria and decreased kidney function: are silver compounds toxic to the kidney? Am J Kidney Dis. 2009;53(5):890–4. doi: 10.1053/j.ajkd.2008.08.028.PubMedCrossRefGoogle Scholar
  82. 82.
    Valiyaveettil S, AshaRani PV, Mun GLK, Hande MP. Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano. 2009;3(2):279–90. doi: 10.1021/nn800596w.PubMedCrossRefGoogle Scholar
  83. 83.
    Song JM, Pal S, Tak YK. Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the gram-negative bacterium Escherichia coli. Appl Environ Microbiol. 2007;73(6):1712–20. doi: 10.1128/Aem.02218-06.PubMedCrossRefGoogle Scholar
  84. 84.
    Sharma VK, Panacek A, Kvitek L, Prucek R, Kolar M, Vecerova R, Pizurova N, Nevecna T, Zboril R. Silver colloid nanoparticles: synthesis, characterization, and their antibacterial activity. J Phys Chem B. 2006;110(33):16248–53. doi: 10.1021/jp063826h.PubMedCrossRefGoogle Scholar
  85. 85.
    Pratsinis SE, Sotiriou GA. Antibacterial activity of nanosilver ions and particles. Environ Sci Technol. 2010;44(14):5649–54. doi: 10.1021/es101072s.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag London 2012

Authors and Affiliations

  • Antti Soininen
    • 1
  • Emilia Kaivosoja
    • 2
  • Jaime Esteban
    • 3
  • Riina Rautemaa-Richardson
    • 4
  • Alberto Ortiz-Pérez
    • 3
  • Gonçalo Barretto
    • 2
  • Yrjö T. Konttinen
    • 5
    • 1
    • 2
    Email author
  1. 1.ORTON Research InstituteORTON Orthopaedic HospitalHelsinkiFinland
  2. 2.Department of MedicineInstitute of Clinical Medicine, Biomedicum 1 HusHelsinkiFinland
  3. 3.Bone and Joint Infectious Unit, Department of Clinical MicrobiologyIIS-Fundación Jiménez DíazMadridSpain
  4. 4.School of Translational MedicineManchester Academic Health Science Centre, University Hospital of South ManchesterManchesterUK
  5. 5.Department of MedicineCOXA Hospital for Joint ReplacementTampereFinland

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