Advertisement

Emergence of daptomycin resistance following vancomycin-unresponsive Staphylococcus aureus bacteraemia in a daptomycin-naïve patient—a review of the literature

  • S. J. van HalEmail author
  • D. L. Paterson
  • I. B. Gosbell
Review

Abstract

A patient developed a daptomycin-resistant methicillin-resistant Staphylococcus aureus (MRSA) infection, despite being daptomycin-naïve, in the setting of persistent bacteraemia secondary to vertebral osteomyelitis. Modified population analysis profiling of sequential MRSA blood culture isolates revealed transition from a vancomycin-susceptible phenotype to a vancomycin-intermediate S. aureus (VISA) phenotype through a vancomycin-heteroresistant S. aureus (hVISA) intermediary. Increased cell wall thickening, determined by transmission electron microscopy, correlated with the emergence of daptomycin resistance. This case supports the current hypothesis that MRSA with reduced glycopeptide susceptibility are less susceptible to daptomycin because of a thickened cell wall. This may have significance for the use of daptomycin in salvage therapy. Other predictors of daptomycin resistance include bacteraemic persistence and the presence of high inoculum infections. As resistance may appear de novo and be unstable in vivo, all isolates should have daptomycin susceptibility testing performed. The optimal antibiotic option for salvage therapy of these daptomycin-resistant infections is unknown. However, these findings emphasise the importance of optimising management, including the consideration of early surgical intervention to avoid the emergence of daptomycin resistance, especially in high inoculum infections.

Keywords

Vancomycin Infective Endocarditis Linezolid Invasive Aspergillosis Daptomycin 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 1.
    Arbeit RD, Maki D, Tally FP, Campanaro E, Eisenstein BI (2004) The safety and efficacy of daptomycin for the treatment of complicated skin and skin-structure infections. Clin Infect Dis 38(12):1673–1681PubMedCrossRefGoogle Scholar
  2. 2.
    Fowler VG Jr, Boucher HW, Corey GR, Abrutyn E, Karchmer AW, Rupp ME, Levine DP, Chambers HF, Tally FP, Vigliani GA, Cabell CH, Link AS, DeMeyer I, Filler SG, Zervos M, Cook P, Parsonnet J, Bernstein JM, Price CS, Forrest GN, Fätkenheuer G, Gareca M, Rehm SJ, Brodt HR, Tice A, Cosgrove SE (2006) Daptomycin versus standard therapy for bacteremia and endocarditis caused by Staphylococcus aureus. N Engl J Med 355(7):653–665PubMedCrossRefGoogle Scholar
  3. 3.
    Silverman JA, Perlmutter NG, Shapiro HM (2003) Correlation of daptomycin bactericidal activity and membrane depolarization in Staphylococcus aureus. Antimicrob Agents Chemother 47(8):2538–2544PubMedCrossRefGoogle Scholar
  4. 4.
    Clinical and Laboratory Standards Institute (CLSI) (2010) Performance standards for antimicrobial susceptibility testing; twentieth informational supplement. M100-S20, vol. 30, no. 1. CLSI, Wayne, Pennsylvania 19087-1898 USAGoogle Scholar
  5. 5.
    European Committee on Antimicrobial Susceptibility Testing (EUCAST) (2010) Clinical breakpoints - bacteria (version 1.1). Available online at: http://www.eucast.org/clinical_breakpoints. Accessed November 2010
  6. 6.
    Mishra NN, Yang SJ, Sawa A, Rubio A, Nast CC, Yeaman MR, Bayer AS (2009) Analysis of cell membrane characteristics of in vitro-selected daptomycin-resistant strains of methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 53(6):2312–2318PubMedCrossRefGoogle Scholar
  7. 7.
    Friedman L, Alder JD, Silverman JA (2006) Genetic changes that correlate with reduced susceptibility to daptomycin in Staphylococcus aureus. Antimicrob Agents Chemother 50(6):2137–2145PubMedCrossRefGoogle Scholar
  8. 8.
    Patel JB, Jevitt LA, Hageman J, McDonald LC, Tenover FC (2006) An association between reduced susceptibility to daptomycin and reduced susceptibility to vancomycin in Staphylococcus aureus. Clin Infect Dis 42(11):1652–1653PubMedCrossRefGoogle Scholar
  9. 9.
    Cui L, Tominaga E, Neoh HM, Hiramatsu K (2006) Correlation between reduced daptomycin susceptibility and vancomycin resistance in vancomycin-intermediate Staphylococcus aureus. Antimicrob Agents Chemother 50(3):1079–1082PubMedCrossRefGoogle Scholar
  10. 10.
    Kirby A, Mohandas K, Broughton C, Neal TJ, Smith GW, Pai P, Nistal de Paz C (2009) In vivo development of heterogeneous glycopeptide-intermediate Staphylococcus aureus (hGISA), GISA and daptomycin resistance in a patient with meticillin-resistant S. aureus endocarditis. J Med Microbiol 58(Pt 3):376–380PubMedCrossRefGoogle Scholar
  11. 11.
    Lee CH, Wang MC, Huang IW, Chen FJ, Lauderdale TL (2010) Development of daptomycin nonsusceptibility with heterogeneous vancomycin-intermediate resistance and oxacillin susceptibility in methicillin-resistant Staphylococcus aureus during high-dose daptomycin treatment. Antimicrob Agents Chemother 54(9):4038–4040PubMedCrossRefGoogle Scholar
  12. 12.
    Mariani PG, Sader HS, Jones RN (2006) Development of decreased susceptibility to daptomycin and vancomycin in a Staphylococcus aureus strain during prolonged therapy. J Antimicrob Chemother 58(2):481–483PubMedCrossRefGoogle Scholar
  13. 13.
    Tenover FC, Sinner SW, Segal RE, Huang V, Alexandre SS, McGowan JE Jr, Weinstein MP (2009) Characterisation of a Staphylococcus aureus strain with progressive loss of susceptibility to vancomycin and daptomycin during therapy. Int J Antimicrob Agents 33(6):564–568PubMedCrossRefGoogle Scholar
  14. 14.
    Yang SJ, Nast CC, Mishra NN, Yeaman MR, Fey PD, Bayer AS (2010) Cell wall thickening is not a universal accompaniment of the daptomycin nonsusceptibility phenotype in Staphylococcus aureus: evidence for multiple resistance mechanisms. Antimicrob Agents Chemother 54(8):3079–3085PubMedCrossRefGoogle Scholar
  15. 15.
    Hayden MK, Rezai K, Hayes RA, Lolans K, Quinn JP, Weinstein RA (2005) Development of daptomycin resistance in vivo in methicillin-resistant Staphylococcus aureus. J Clin Microbiol 43(10):5285–5287PubMedCrossRefGoogle Scholar
  16. 16.
    Sakoulas G, Rose W, Rybak MJ, Pillai S, Alder J, Moellering RC Jr, Eliopoulos GM (2008) Evaluation of endocarditis caused by methicillin-susceptible Staphylococcus aureus developing nonsusceptibility to daptomycin. J Clin Microbiol 46(1):220–224PubMedCrossRefGoogle Scholar
  17. 17.
    Cui L, Isii T, Fukuda M, Ochiai T, Neoh HM, Camargo IL, Watanabe Y, Shoji M, Hishinuma T, Hiramatsu K (2010) An RpoB mutation confers dual heteroresistance to daptomycin and vancomycin in Staphylococcus aureus. Antimicrob Agents Chemother 54(12):5222–5233PubMedCrossRefGoogle Scholar
  18. 18.
    LaPlante KL, Rybak MJ (2004) Impact of high-inoculum Staphylococcus aureus on the activities of nafcillin, vancomycin, linezolid, and daptomycin, alone and in combination with gentamicin, in an in vitro pharmacodynamic model. Antimicrob Agents Chemother 48(12):4665–4672PubMedCrossRefGoogle Scholar
  19. 19.
    Silverman JA, Oliver N, Andrew T, Li T (2001) Resistance studies with daptomycin. Antimicrob Agents Chemother 45(6):1799–1802PubMedCrossRefGoogle Scholar
  20. 20.
    Sharma M, Riederer K, Chase P, Khatib R (2008) High rate of decreasing daptomycin susceptibility during the treatment of persistent Staphylococcus aureus bacteremia. Eur J Clin Microbiol Infect Dis 27(6):433–437PubMedCrossRefGoogle Scholar
  21. 21.
    Moise PA, North D, Steenbergen JN, Sakoulas G (2009) Susceptibility relationship between vancomycin and daptomycin in Staphylococcus aureus: facts and assumptions. Lancet Infect Dis 9(10):617–624PubMedCrossRefGoogle Scholar
  22. 22.
    Darley ES, MacGowan AP (2004) Antibiotic treatment of gram-positive bone and joint infections. J Antimicrob Chemother 53(6):928–935PubMedCrossRefGoogle Scholar
  23. 23.
    Landersdorfer CB, Bulitta JB, Kinzig M, Holzgrabe U, Sörgel F (2009) Penetration of antibacterials into bone: pharmacokinetic, pharmacodynamic and bioanalytical considerations. Clin Pharmacokinet 48(2):89–124PubMedCrossRefGoogle Scholar
  24. 24.
    Udekwu KI, Parrish N, Ankomah P, Baquero F, Levin BR (2009) Functional relationship between bacterial cell density and the efficacy of antibiotics. J Antimicrob Chemother 63(4):745–757PubMedCrossRefGoogle Scholar
  25. 25.
    Vikram HR, Buenconsejo J, Hasbun R, Quagliarello VJ (2003) Impact of valve surgery on 6-month mortality in adults with complicated, left-sided native valve endocarditis: a propensity analysis. JAMA 290(24):3207–3214PubMedCrossRefGoogle Scholar
  26. 26.
    Walsh TR, Howe RA, Wootton M, Bennett PM, MacGowan AP (2001) Detection of glycopeptide resistance in Staphylococcus aureus. J Antimicrob Chemother 47(3):357–358PubMedCrossRefGoogle Scholar
  27. 27.
    Mangili A, Bica I, Snydman DR, Hamer DH (2005) Daptomycin-resistant, methicillin-resistant Staphylococcus aureus bacteremia. Clin Infect Dis 40(7):1058–1060PubMedCrossRefGoogle Scholar
  28. 28.
    Vikram HR, Havill NL, Koeth LM, Boyce JM (2005) Clinical progression of methicillin-resistant Staphylococcus aureus vertebral osteomyelitis associated with reduced susceptibility to daptomycin. J Clin Microbiol 43(10):5384–5387PubMedCrossRefGoogle Scholar
  29. 29.
    Skiest DJ (2006) Treatment failure resulting from resistance of Staphylococcus aureus to daptomycin. J Clin Microbiol 44(2):655–656PubMedCrossRefGoogle Scholar
  30. 30.
    Hirschwerk D, Ginocchio CC, Bythrow M, Condon S (2006) Diminished susceptibility to daptomycin accompanied by clinical failure in a patient with methicillin-resistant Staphylococcus aureus bacteremia. Infect Control Hosp Epidemiol 27(3):315–317PubMedCrossRefGoogle Scholar
  31. 31.
    Marty FM, Yeh WW, Wennersten CB, Venkataraman L, Albano E, Alyea EP, Gold HS, Baden LR, Pillai SK (2006) Emergence of a clinical daptomycin-resistant Staphylococcus aureus isolate during treatment of methicillin-resistant Staphylococcus aureus bacteremia and osteomyelitis. J Clin Microbiol 44(2):595–597PubMedCrossRefGoogle Scholar
  32. 32.
    Murthy MH, Olson ME, Wickert RW, Fey PD, Jalali Z (2008) Daptomycin non-susceptible meticillin-resistant Staphylococcus aureus USA 300 isolate. J Med Microbiol 57(Pt 8):1036–1038PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • S. J. van Hal
    • 1
    Email author
  • D. L. Paterson
    • 2
  • I. B. Gosbell
    • 1
    • 3
  1. 1.Department of Microbiology and Infectious DiseasesSydney South West Pathology Service—LiverpoolSydneyAustralia
  2. 2.University of Queensland Centre for Clinical Research (UQCCR)BrisbaneAustralia
  3. 3.Microbiology and Infectious Diseases Unit, School of MedicineUniversity of Western SydneyPenrith SouthAustralia

Personalised recommendations