1887

Abstract

Biofilm resistance mechanisms are multifactorial and vary from one organism to another. The purpose of this study was to investigate the efficacy of linezolid against indwelling device-related meticillin-resistant (MRSE) biofilm, and compare this with other antimicrobials. MICs, minimum biofilm inhibitory concentrations (MBICs) and minimum biofilm eradication concentrations (MBECs) were determined by the microtitre plate method. Fourteen and thirteen isolates from patients with indwelling device-related bacteraemia (IDB) and indwelling device colonization not associated with bacteraemia, respectively, were assessed. High MBIC was associated with a high intensity of biofilm formation (gentamicin  = 0.796; linezolid  = 0.477; rifampicin  = 0.634; tigecycline  = 0.410; and vancomycin  = 0.771), but this correlation was not observed with MBEC. Linezolid demonstrated better antimicrobial activity than other antimicrobials (MBIC – gentamicin <0.001, rifampicin  = 0.019, vancomycin  = 0.008; MBEC – gentamicin <0.001, rifampicin  = 0.002, vancomycin <0.001). Biofilm growth inhibition was strongly associated with biofilm formation intensity; however, biofilm eradication was not cell number dependent. MRSE biofilm eradication would represent a huge advance for IDB, although high concentrations of gentamicin, linezolid, rifampicin, tigecycline and vancomycin were required for that. In general, linezolid reached better concentrations and was demonstrated to be highly active against MRSE biofilms by inhibiting their growth during biofilm formation.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.048678-0
2013-03-01
2019-09-22
Loading full text...

Full text loading...

/deliver/fulltext/jmm/62/3/394.html?itemId=/content/journal/jmm/10.1099/jmm.0.048678-0&mimeType=html&fmt=ahah

References

  1. Antunes A. L. , Secchi C. , Reiter K. C. , Perez L. R. , de Freitas A. L. , D’Azevedo P. A. . ( 2008; ). Feasible identification of Staphylococcus epidermidis using desferrioxamine and fosfomycin disks. . APMIS 116:, 16–20. [CrossRef] [PubMed]
    [Google Scholar]
  2. Antunes A. L. , Trentin D. S. , Bonfanti J. W. , Pinto C. C. F. , Perez L. R. R. , Macedo A. J. , Barth A. L. . ( 2010; ). Application of a feasible method for determination of biofilm antimicrobial susceptibility in staphylococci. . APMIS 118:, 873–877. [CrossRef] [PubMed]
    [Google Scholar]
  3. Antunes A. L. , Bonfanti J. W. , Perez L. R. , Pinto C. C. , Freitas A. L. , Macedo A. J. , Barth A. L. . ( 2011; ). High vancomycin resistance among biofilms produced by Staphylococcus species isolated from central venous catheters. . Mem Inst Oswaldo Cruz 106:, 51–55. [CrossRef] [PubMed]
    [Google Scholar]
  4. Anwar H. , Dasgupta M. K. , Costerton J. W. . ( 1990; ). Testing the susceptibility of bacteria in biofilms to antibacterial agents. . Antimicrob Agents Chemother 34:, 2043–2046. [CrossRef] [PubMed]
    [Google Scholar]
  5. Arciola C. R. , Campoccia D. , Speziale P. , Montanaro L. , Costerton J. W. . ( 2012; ). Biofilm formation in Staphylococcus implant infections. A review of molecular mechanisms and implications for biofilm-resistant materials. . Biomaterials 33:, 5967–5982. [CrossRef] [PubMed]
    [Google Scholar]
  6. Bannerman T. L. . ( 2011; ). Staphylococcus, Micrococcus, and other catalase-positive cocci that grow aerobically. . In Manual of Clinical Microbiology, pp. 384–404. Edited by Murray P. R. , Jorgensen E. J. , Jolken M. A. . . Washington, DC:: American Society for Microbiology;.
    [Google Scholar]
  7. Bayston R. , Ullas G. , Ashraf W. . ( 2012; ). Action of linezolid or vancomycin on biofilms in ventriculoperitoneal shunts in vitro . . Antimicrob Agents Chemother 56:, 2842–2845. [CrossRef] [PubMed]
    [Google Scholar]
  8. Cafiso V. , Bertuccio T. , Spina D. , Purrello S. , Stefani S. . ( 2010; ). Tigecycline inhibition of a mature biofilm in clinical isolates of Staphylococcus aureus: comparison with other drugs. . FEMS Immunol Med Microbiol 59:, 466–469.[PubMed]
    [Google Scholar]
  9. Ceri H. , Olson M. E. , Stremick C. , Read R. R. , Morck D. , Buret A. . ( 1999; ). The Calgary Biofilm Device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. . J Clin Microbiol 37:, 1771–1776.[PubMed]
    [Google Scholar]
  10. Cha J. O. , Park Y. K. , Lee Y. S. , Chung G. T. . ( 2011; ). In vitro biofilm formation and bactericidal activities of methicillin-resistant Staphylococcus aureus clones prevalent in Korea. . Diagn Microbiol Infect Dis 70:, 112–118. [CrossRef] [PubMed]
    [Google Scholar]
  11. CLSI ( 2011; ). Performance Standards for Antimicrobial Susceptibility Testing; M100–S21. . Wayne, PA:: Clinical and Laboratory Standards Institute;.
  12. CLSI ( 2012; ). Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically; approved standard, 9th edn, M07–A9. . Wayne, PA:: Clinical and Laboratory Standards Institute;.
  13. Conlon K. M. , Humphreys H. , O’Gara J. P. . ( 2004; ). Inactivations of rsbU and sarA by IS256 represent novel mechanisms of biofilm phenotypic variation in Staphylococcus epidermidis. . J Bacteriol 186:, 6208–6219. [CrossRef] [PubMed]
    [Google Scholar]
  14. Costerton J. W. , Stewart P. S. , Greenberg E. P. . ( 1999; ). Bacterial biofilms: a common cause of persistent infections. . Science 284:, 1318–1322. [CrossRef] [PubMed]
    [Google Scholar]
  15. Dagostino L. , Goodman A. E. , Marshall K. C. . ( 1991; ). Physiological responses induced in bacteria adhering to surfaces. . Biofouling 4:, 113–119. [CrossRef]
    [Google Scholar]
  16. Dandache P. , Moise P. A. , Orsini J. , Montecalvo M. , Sakoulas G. . ( 2009; ). Reduced biofilm production associated with increasing linezolid MICs among linezolid-resistant staphylococci. . J Antimicrob Chemother 64:, 1114–1115. [CrossRef] [PubMed]
    [Google Scholar]
  17. Donlan R. M. , Costerton J. W. . ( 2002; ). Biofilms: survival mechanisms of clinically relevant microorganisms. . Clin Microbiol Rev 15:, 167–193. [CrossRef] [PubMed]
    [Google Scholar]
  18. Duguid I. G. , Evans E. , Brown M. R. , Gilbert P. . ( 1992; ). Growth-rate-independent killing by ciprofloxacin of biofilm-derived Staphylococcus epidermidis; evidence for cell-cycle dependency. . J Antimicrob Chemother 30:, 791–802. [CrossRef] [PubMed]
    [Google Scholar]
  19. Fredheim E. G. , Klingenberg C. , Rohde H. , Frankenberger S. , Gaustad P. , Flaegstad T. , Sollid J. E. . ( 2009; ). Biofilm formation by Staphylococcus haemolyticus. . J Clin Microbiol 47:, 1172–1180. [CrossRef] [PubMed]
    [Google Scholar]
  20. Jain A. , Agarwal A. . ( 2009; ). Biofilm production, a marker of pathogenic potential of colonizing and commensal staphylococci. . J Microbiol Methods 76:, 88–92. [CrossRef] [PubMed]
    [Google Scholar]
  21. Jefferson K. K. , Goldmann D. A. , Pier G. B. . ( 2005; ). Use of confocal microscopy to analyze the rate of vancomycin penetration through Staphylococcus aureus biofilms. . Antimicrob Agents Chemother 49:, 2467–2473. [CrossRef] [PubMed]
    [Google Scholar]
  22. Mack D. , Rohde H. , Harris L. G. , Davies A. P. , Horstkotte M. A. , Knobloch J. K. . ( 2006; ). Biofilm formation in medical device-related infection. . Int J Artif Organs 29:, 343–359.[PubMed]
    [Google Scholar]
  23. Mah T. F. , O’Toole G. A. . ( 2001; ). Mechanisms of biofilm resistance to antimicrobial agents. . Trends Microbiol 9:, 34–39. [CrossRef] [PubMed]
    [Google Scholar]
  24. Maki D. G. , Weise C. E. , Sarafin H. W. . ( 1977; ). A semiquantitative culture method for identifying intravenous-catheter-related infection. . N Engl J Med 296:, 1305–1309. [CrossRef] [PubMed]
    [Google Scholar]
  25. Mermel L. A. , Farr B. M. , Sherertz R. J. , Raad I. I. , O’Grady N. , Harris J. S. , Craven D. E. . Infectious Diseases Society of America, American College of Critical Care Medicine, Society for Healthcare Epidemiology of America ( 2001; ). Guidelines for the management of intravascular catheter-related infections. . J Intraven Nurs 24:, 180–205.[PubMed]
    [Google Scholar]
  26. Patel R. . ( 2005; ). Biofilms and antimicrobial resistance. . Clin Orthop Relat Res 463:, 41–47. [CrossRef] [PubMed]
    [Google Scholar]
  27. Potoski B. A. , Adams J. , Clarke L. , Shutt K. , Linden P. K. , Baxter C. , Pasculle A. W. , Capitano B. , Peleg A. Y. . & other authors ( 2006; ). Epidemiological profile of linezolid-resistant coagulase-negative staphylococci. . Clin Infect Dis 43:, 165–171. [CrossRef] [PubMed]
    [Google Scholar]
  28. Presterl E. , Hajdu S. , Lassnigg A. M. , Hirschl A. M. , Holinka J. , Graninger W. . ( 2009; ). Effects of azithromycin in combination with vancomycin, daptomycin, fosfomycin, tigecycline, and ceftriaxone on Staphylococcus epidermidis biofilms. . Antimicrob Agents Chemother 53:, 3205–3210. [CrossRef] [PubMed]
    [Google Scholar]
  29. Qu Y. , Istivan T. S. , Daley A. J. , Rouch D. A. , Deighton M. A. . ( 2009; ). Comparison of various antimicrobial agents as catheter lock solutions: preference for ethanol in eradication of coagulase-negative staphylococcal biofilms. . J Med Microbiol 58:, 442–450. [CrossRef] [PubMed]
    [Google Scholar]
  30. Qu Y. , Daley A. J. , Istivan T. S. , Garland S. M. , Deighton M. A. . ( 2010; ). Antibiotic susceptibility of coagulase-negative staphylococci isolated from very low birth weight babies: comprehensive comparisons of bacteria at different stages of biofilm formation. . Ann Clin Microbiol Antimicrob 9:, 16. [CrossRef] [PubMed]
    [Google Scholar]
  31. Raad I. , Hanna H. , Jiang Y. , Dvorak T. , Reitzel R. , Chaiban G. , Sherertz R. , Hachem R. . ( 2007; ). Comparative activities of daptomycin, linezolid, and tigecycline against catheter-related methicillin-resistant Staphylococcus bacteremic isolates embedded in biofilm. . Antimicrob Agents Chemother 51:, 1656–1660. [CrossRef] [PubMed]
    [Google Scholar]
  32. Reiter K. C. , Da Silva Paim T. G. , De Oliveira C. F. , D’Azevedo P. A. . ( 2011; ). High biofilm production by invasive multiresistant staphylococci. . APMIS 119:, 776–781. [CrossRef] [PubMed]
    [Google Scholar]
  33. Rodríguez-Martínez J. M. , Ballesta S. , García I. , Conejo M. C. , Pascual A. . ( 2007; ). [Activity and penetration of linezolid and vancomycin against Staphylococcus epidermidis biofilms]. . Enferm Infecc Microbiol Clin 25:, 425–428 (in Spanish).[PubMed] [CrossRef]
    [Google Scholar]
  34. Rose W. E. , Poppens P. T. . ( 2009; ). Impact of biofilm on the in vitro activity of vancomycin alone and in combination with tigecycline and rifampicin against Staphylococcus aureus. . J Antimicrob Chemother 63:, 485–488. [CrossRef] [PubMed]
    [Google Scholar]
  35. Sandoe J. A. T. , Witherden I. R. , Au-Yeung H.-K. , Kite P. , Kerr K. G. , Wilcox M. H. . ( 2002; ). Enterococcal intravascular catheter-related bloodstream infection: management and outcome of 61 consecutive cases. . J Antimicrob Chemother 50:, 577–582. [CrossRef] [PubMed]
    [Google Scholar]
  36. Singh R. , Ray P. , Das A. , Sharma M. . ( 2010; ). Penetration of antibiotics through Staphylococcus aureus and Staphylococcus epidermidis biofilms. . J Antimicrob Chemother 65:, 1955–1958. [CrossRef] [PubMed]
    [Google Scholar]
  37. Stepanović S. , Vuković D. , Hola V. , Di Bonaventura G. , Djukić S. , Cirković I. , Ruzicka F. . ( 2007; ). Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. . APMIS 115:, 891–899. [CrossRef] [PubMed]
    [Google Scholar]
  38. Stewart P. S. , Costerton J. W. . ( 2001; ). Antibiotic resistance of bacteria in biofilms. . Lancet 358:, 135–138. [CrossRef] [PubMed]
    [Google Scholar]
  39. Suci P. A. , Mittelman M. W. , Yu F. P. , Geesey G. G. . ( 1994; ). Investigation of ciprofloxacin penetration into Pseudomonas aeruginosa biofilms. . Antimicrob Agents Chemother 38:, 2125–2133. [CrossRef] [PubMed]
    [Google Scholar]
  40. Suci P. A. , Vrany J. D. , Mittelman M. W. . ( 1998; ). Investigation of interactions between antimicrobial agents and bacterial biofilms using attenuated total reflection Fourier transform infrared spectroscopy. . Biomaterials 19:, 327–339. [CrossRef] [PubMed]
    [Google Scholar]
  41. Tormo M. A. , Úbeda C. , Martí M. , Maiques E. , Cucarella C. , Valle J. , Foster T. J. , Lasa I. , Penadés J. R. . ( 2007; ). Phase-variable expression of the biofilm-associated protein (Bap) in Staphylococcus aureus. . Microbiology 153:, 1702–1710. [CrossRef] [PubMed]
    [Google Scholar]
  42. Zhang K. , McClure J. A. , Elsayed S. , Louie T. , Conly J. M. . ( 2005; ). Novel multiplex PCR assay for characterization and concomitant subtyping of staphylococcal cassette chromosome mec types I to V in methicillin-resistant Staphylococcus aureus. . J Clin Microbiol 43:, 5026–5033. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.048678-0
Loading
/content/journal/jmm/10.1099/jmm.0.048678-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error