1887

Journal of Medical Microbiology logo

Volume 68, Issue 6

Reduced vancomycin susceptibility and increased macrophage survival in Staphylococcus aureus strains sequentially isolated from a bacteraemic patient during a short course of antibiotic therapy Free

Abstract

Purpose. The purpose of the present study was to determine the relatedness of Staphylococcus aureus strains successively isolated over a 7-day period from a single bacteraemic patient undergoing antibiotic treatment with vancomycin.

Methods. The S. aureus strains had been isolated and sequenced previously. Antibiotic susceptibility testing, population analysis profiling, and lysostaphin sensitivity and phagocytic killing assays were used to characterize these clonal isolates.

Results. The seven isolates (MEH1–MEH7) were determined to belong to a common multilocus sequence type (MLST) and spa type. Within the third and fifth day of vancomycin treatment, mutations were observed in the vraS and rpsU genes, respectively. Population analysis profiles revealed that the initial isolate (MEH1) was vancomycin-susceptible S. aureus (VSSA), while those isolated on day 7 were mostly heteroresistant vancomycin-intermediate S. aureus (hVISA). Supporting these findings, MEH7 was also observed to be slower in growth, to have an increase in cell wall width and to have reduced sensitivity to lysostaphin, all characteristics of VISA and hVISA strains. In addition, MEH7, although phagocytosed at numbers comparable to the initial isolate, MEH1, survived in higher numbers in RAW 264.7 macrophages. Macrophages infected with MEH7 also released more TNF-α and IFN-1β.

Conclusion. We report an increasing resistance to vancomycin coupled with daptomycin that occurred within approximately 3 days of receiving vancomycin and steadily increased until the infection was cleared with an alternative antibiotic therapy. This study reiterates the need for rapid, efficient and accurate detection of hVISA and VISA infections, especially in high-bacterial load, metastatic infections like bacteraemia.

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  • Accepted:
  • Published Online:
Keyword(s): hVISA , resilence to immunoclearance , Staphylococcus aureus and vancomycin resistance
© 2019
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2019-05-28
2024-04-24
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References

  1. Levine DP. Vancomycin: a history. Clin Infect Dis 2006; 42:S5–S12 [View Article]
     [Google Scholar]
  2. Garnier F, Chainier D, Walsh T, Karlsson A, Bolmström A et al. A 1 year surveillance study of glycopeptide-intermediate Staphylococcus aureus strains in a French hospital. J Antimicrob Chemother 2006; 57:146–149 [View Article]
     [Google Scholar]
  3. Jones RN. Microbiological features of vancomycin in the 21st century: minimum inhibitory concentration creep, bactericidal/static activity, and applied breakpoints to predict clinical outcomes or detect resistant strains. Clin Infect Dis 2006; 42:S13–S24 [View Article]
     [Google Scholar]
  4. Gould IM. Clinical relevance of increasing glycopeptide MICs against Staphylococcus aureus. Int J Antimicrob Agents 2008; 31:1–9 [View Article]
     [Google Scholar]
  5. Kirst HA, Thompson DG, Nicas TI. Historical yearly usage of vancomycin. Antimicrob Agents Chemother 1998; 42:1303–1304 [View Article]
     [Google Scholar]
  6. Small PM, Chambers HF. Vancomycin for Staphylococcus aureus endocarditis in intravenous drug users. Antimicrob Agents Chemother 1990; 34:1227–1231 [View Article]
     [Google Scholar]
  7. Stryjewski ME, Szczech LA, Benjamin DK, Inrig JK, Kanafani ZA et al. Use of vancomycin or first-generation cephalosporins for the treatment of hemodialysis-dependent patients with methicillin-susceptible Staphylococcus aureus bacteremia. Clin Infect Dis 2007; 44:190–196 [View Article]
     [Google Scholar]
  8. Moise PA, Schentag JJ. Vancomycin treatment failures in Staphylococcus aureus lower respiratory tract infections. Int J Antimicrob Agents 2000; 16:31–34 [View Article]
     [Google Scholar]
  9. Hiramatsu K, Hanaki H, Ino T, Yabuta K, Oguri T et al. Methicillin-resistant Staphylococcus aureus clinical strain with reduced vancomycin susceptibility. J Antimicrob Chemother 1997; 40:135–136 [View Article]
     [Google Scholar]
  10. Rotun SS, McMath V, Schoonmaker DJ, Maupin PS, Tenover FC et al. Staphylococcus aureus with reduced susceptibility to vancomycin isolated from a patient with fatal bacteremia. Emerg Infect Dis 1999; 5:147–149 [View Article]
     [Google Scholar]
  11. Seifert H, von Eiff C, Fätkenheuer G. Fatal case due to methicillin-resistant Staphylococcus aureus small colony variants in an AIDS patient. Emerg Infect Dis 1999; 5:450–453 [View Article]
     [Google Scholar]
  12. Centers for Disease Control and Prevention (CDC) Staphylococcus aureus with reduced susceptibility to vancomycin—United States, 1997. MMWR Morb Mortal Wkly Rep 1997; 46:765–766
     [Google Scholar]
  13. Centers for Disease Control and Prevention (CDC) Fourth case of vancomycin-resistant Staphylococcus infection reported in US. MMWR Morb Mortal Wkly Rep 2000; 48:1165–1171
     [Google Scholar]
  14. CLSI Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically, Approved standard, 7th ed. CLSI document (M7–A8). Wayne, PA: CLSI; 2009
     [Google Scholar]
  15. Hiramatsu K, Aritaka N, Hanaki H, Kawasaki S, Hosoda Y et al. Dissemination in Japanese hospitals of strains of Staphylococcus aureus heterogeneously resistant to vancomycin. Lancet 1997; 350:1670–1673 [View Article]
     [Google Scholar]
  16. Marlowe EM, Cohen MD, Hindler JF, Ward KW, Bruckner DA et al. Practical strategies for detecting and confirming vancomycin-intermediate Staphylococcus aureus: a tertiary-care hospital laboratory's experience. J Clin Microbiol 2001; 39:2637–2639 [View Article]
     [Google Scholar]
  17. Charles PG, Ward PB, Johnson PDR, Howden BP, Grayson ML et al. Clinical features associated with bacteremia due to heterogeneous vancomycin-intermediate Staphylococcus aureus. Clin Infect Dis 2004; 38:448–451 [View Article]
     [Google Scholar]
  18. Howden BP, Johnson PDR, Ward PB, Stinear TP, Davies JK et al. Isolates with low-level vancomycin resistance associated with persistent methicillin-resistant Staphylococcus aureus bacteremia. Antimicrob Agents Chemother 2006; 50:3039–3047 [View Article]
     [Google Scholar]
  19. Howden BP, Ward PB, Charles PGP, Korman TM, Fuller A et al. Treatment outcomes for serious infections caused by methicillin-resistant Staphylococcus aureus with reduced vancomycin susceptibility. Clin Infect Dis 2004; 38:521–528 [View Article]
     [Google Scholar]
  20. Moore MR, Perdreau-Remington F, Chambers HF. Vancomycin treatment failure associated with heterogeneous vancomycin-intermediate Staphylococcus aureus in a patient with endocarditis and in the rabbit model of endocarditis. Antimicrob Agents Chemother 2003; 47:1262–1266 [View Article]
     [Google Scholar]
  21. Cosgrove SE, Carroll KC, Perl TM. Staphylococcus aureus with reduced susceptibility to vancomycin. Clin Infect Dis 2004; 39:539–545 [View Article]
     [Google Scholar]
  22. Tenover FC, McDonald LC. Vancomycin-resistant staphylococci and enterococci: epidemiology and control. Curr Opin Infect Dis 2005; 18:300–305 [View Article]
     [Google Scholar]
  23. Sieradzki K, Leski T, Dick J, Borio L, Tomasz A et al. Evolution of a vancomycin-intermediate Staphylococcus aureus strain in vivo: multiple changes in the antibiotic resistance phenotypes of a single lineage of methicillin-resistant S. aureus under the impact of antibiotics administered for chemotherapy. J Clin Microbiol 2003; 41:1687–1693 [View Article]
     [Google Scholar]
  24. Sieradzki K, Tomasz A. Alterations of cell wall structure and metabolism accompany reduced susceptibility to vancomycin in an isogenic series of clinical isolates of Staphylococcus aureus. J Bacteriol 2003; 185:7103–7110 [View Article]
     [Google Scholar]
  25. Yamaguchi T, Suzuki S, Okamura S, Miura Y, Tsukimori A et al. Evolution and single-nucleotide polymorphisms in methicillin-resistant Staphylococcus aureus strains with reduced susceptibility to vancomycin and daptomycin, based on determination of the complete genome. Antimicrob Agents Chemother 2015; 59:3585–3587 [View Article]
     [Google Scholar]
  26. Steinkraus G, White R, Friedrich L. Vancomycin MIC creep in non-vancomycin-intermediate Staphylococcus aureus (VISA), vancomycin-susceptible clinical methicillin-resistant S. aureus (MRSA) blood isolates from 2001–05. J Antimicrob Chemother 2007; 60:788–794 [View Article]
     [Google Scholar]
  27. Walsh TR, Bolmström A, Qwärnström A, Ho P, Wootton M et al. Evaluation of current methods for detection of staphylococci with reduced susceptibility to glycopeptides. J Clin Microbiol 2001; 39:2439–2444 [View Article]
     [Google Scholar]
  28. Tóth A, Kispál G, Ungvári E, Violka M, Szeberin Z et al. First report of heterogeneously vancomycin-intermediate Staphylococcus aureus (hVISA) causing fatal infection in Hungary. J Chemother 2008; 20:655–656 [View Article]
     [Google Scholar]
  29. Méhes L, Taskó S, Székely A, Tóth A, Ungvári E et al. Phagocytosis and intracellular killing of heterogeneous vancomycin-intermediate Staphylococcus aureus strains. J Med Microbiol 2012; 61:198–203 [View Article]
     [Google Scholar]
  30. Basco MDS, Revollo JR, McKinzie PB, Agnihothram S, Kothari A et al. Draft Genome Sequences of Two Staphylococcus aureus Strains Isolated in Succession from a Case of Bacteremia. Genome Announc 2017; 5:e00259–17 [View Article]
     [Google Scholar]
  31. Koboldt DC, Zhang Q, Larson DE, Shen D, McLellan MD et al. VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res 2012; 22:568–576 [View Article]
     [Google Scholar]
  32. Larsen MV, Cosentino S, Rasmussen S, Friis C, Hasman H et al. Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol 2012; 50:1355–1361 [View Article]
     [Google Scholar]
  33. Harmsen D, Claus H, Witte W, Rothgänger J, Claus H et al. Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol 2003; 41:5442–5448 [View Article]
     [Google Scholar]
  34. Berscheid A, Francois P, Strittmatter A, Gottschalk G, Schrenzel J et al. Generation of a vancomycin-intermediate Staphylococcus aureus (VISA) strain by two amino acid exchanges in VraS. J Antimicrob Chemother 2014; 69:3190–3198 [View Article]
     [Google Scholar]
  35. Hiramatsu K. Vancomycin-resistant Staphylococcus aureus: a new model of antibiotic resistance. Lancet Infect Dis 2001; 1:147–155 [View Article]
     [Google Scholar]
  36. CLSI Performance Standard for Antimicrobial Susceptibility Testing, twentieth informational supplement. Document M100–S20. Wayne, PA: CLSI; 2010
     [Google Scholar]
  37. Neoh HM, Cui L, Yuzawa H, Takeuchi F, Matsuo M et al. Mutated response regulator graR is responsible for phenotypic conversion of Staphylococcus aureus from heterogeneous vancomycin-intermediate resistance to vancomycin-intermediate resistance. Antimicrob Agents Chemother 2008; 52:45–53 [View Article]
     [Google Scholar]
  38. Katayama Y, Murakami-Kuroda H, Cui L, Hiramatsu K. Selection of heterogeneous vancomycin-intermediate Staphylococcus aureus by imipenem. Antimicrob Agents Chemother 2009; 53:3190–3196 [View Article]
     [Google Scholar]
  39. Kato Y, Suzuki T, Ida T, Maebashi K. Genetic changes associated with glycopeptide resistance in Staphylococcus aureus: predominance of amino acid substitutions in YvqF/VraSR. J Antimicrob Chemother 2010; 65:37–45 [View Article]
     [Google Scholar]
  40. Cui L, Neoh HM, Shoji M, Hiramatsu K. Contribution of vraSR and graSR point mutations to vancomycin resistance in vancomycin-intermediate Staphylococcus aureus. Antimicrob Agents Chemother 2009; 53:1231–1234 [View Article]
     [Google Scholar]
  41. Hiramatsu K, Kayayama Y, Matsuo M, Aiba Y, Saito M et al. Vancomycin-intermediate resistance in Staphylococcus aureus. J Glob Antimicrob Resist 2014; 2:213–224 [View Article]
     [Google Scholar]
  42. Daum RS, Gupta S, Sabbagh R, Milewski WM. Characterization of Staphylococcus aureus isolates with decreased susceptibility to vancomycin and teicoplanin: isolation and purification of a constitutively produced protein associated with decreased susceptibility. J Infect Dis 1992; 166:1066–1072 [View Article]
     [Google Scholar]
  43. Pfeltz RF, Singh VK, Schmidt JL, Batten MA, Baranyk CS et al. Characterization of passage-selected vancomycin-resistant Staphylococcus aureus strains of diverse parental backgrounds. Antimicrob Agents Chemother 2000; 44:294–303 [View Article]
     [Google Scholar]
  44. Boyle-Vavra S, Carey RB, Daum RS. Development of vancomycin and lysostaphin resistance in a methicillin-resistant Staphylococcus aureus isolate. J Antimicrob Chemother 2001; 48:617–625 [View Article]
     [Google Scholar]
  45. Cui L, Murakami H, Kuwahara-Arai K, Hanaki H, Hiramatsu K et al. Contribution of a thickened cell wall and its glutamine nonamidated component to the vancomycin resistance expressed by Staphylococcus aureus Mu50. Antimicrob Agents Chemother 2000; 44:2276–2285 [View Article]
     [Google Scholar]
  46. Boyle-Vavra S, Labischinski H, Ebert CC, Ehlert K, Daum RS et al. A spectrum of changes occurs in peptidoglycan composition of glycopeptide-intermediate clinical Staphylococcus aureus isolates. Antimicrob Agents Chemother 2001; 45:280–287 [View Article]
     [Google Scholar]
  47. Filice G, Lanzarini P, Orsolini P, Soldini L, Perversi L et al. Effect of teicoplanin and vancomycin on Staphylococcus aureus ultrastructure. Microbiologica 1990; 13:231–237
     [Google Scholar]
  48. Hanaki H, Kuwahara-Arai K, Boyle-Vavra S, Daum RS, Labischinski H et al. Activated cell-wall synthesis is associated with vancomycin resistance in methicillin-resistant Staphylococcus aureus clinical strains Mu3 and Mu50. J Antimicrob Chemother 1998; 42:199–209 [View Article]
     [Google Scholar]
  49. Reipert A, Ehlert K, Kast T, Bierbaum G. Morphological and genetic differences in two isogenic Staphylococcus aureus strains with decreased susceptibilities to vancomycin. Antimicrob Agents Chemother 2003; 47:568–576 [View Article]
     [Google Scholar]
  50. Cui L, Iwamoto A, Lian JQ, Neoh HM, Maruyama T et al. Novel mechanism of antibiotic resistance originating in vancomycin-intermediate Staphylococcus aureus. Antimicrob Agents Chemother 2006; 50:428–438 [View Article]
     [Google Scholar]
  51. Moreira B, Boyle-Vavra S, deJonge BL, Daum RS. Increased production of penicillin-binding protein 2, increased detection of other penicillin-binding proteins, and decreased coagulase activity associated with glycopeptide resistance in Staphylococcus aureus. Antimicrob Agents Chemother 1997; 41:1788–1793 [View Article]
     [Google Scholar]
  52. Kuroda M, Kuwahara-Arai K, Hiramatsu K. Identification of the up- and down-regulated genes in vancomycin-resistant Staphylococcus aureus strains Mu3 and Mu50 by cDNA differential hybridization method. Biochem Biophys Res Commun 2000; 269:485–490 [View Article]
     [Google Scholar]
  53. Gatlin CL, Pieper R, Huang ST, Mongodin E, Gebregeorgis E et al. Proteomic profiling of cell envelope-associated proteins from Staphylococcus aureus. Proteomics 2006; 6:1530–1549 [View Article]
     [Google Scholar]
  54. Gardete S, Wu SW, Gill S, Tomasz A. Role of VraSR in antibiotic resistance and antibiotic-induced stress response in Staphylococcus aureus. Antimicrob Agents Chemother 2006; 50:3424–3434 [View Article]
     [Google Scholar]
  55. Renzoni A, Andrey DO, Jousselin A, Barras C, Monod A et al. Whole genome sequencing and complete genetic analysis reveals novel pathways to glycopeptide resistance in Staphylococcus aureus. PLoS One 2011; 6:e21577 [View Article]
     [Google Scholar]
  56. McAleese F, Wu SW, Sieradzki K, Dunman P, Murphy E et al. Overexpression of genes of the cell wall stimulon in clinical isolates of Staphylococcus aureus exhibiting vancomycin-intermediate- S. aureus-type resistance to vancomycin. J Bacteriol 2006; 188:1120–1133 [View Article]
     [Google Scholar]
  57. Price CT, Bukka A, Cynamon M, Graham JE. Glycine betaine uptake by the ProXVWZ ABC transporter contributes to the ability of Mycobacterium tuberculosis to initiate growth in human macrophages. J Bacteriol 2008; 190:3955–3961 [View Article]
     [Google Scholar]
  58. Das D, Saha SS, Bishayi B. Intracellular survival of Staphylococcus aureus: correlating production of catalase and superoxide dismutase with levels of inflammatory cytokines. Inflamm Res 2008; 57:340–349 [View Article]
     [Google Scholar]
  59. Schulte W, Bernhagen J, Bucala R. Cytokines in sepsis: potent immunoregulators and potential therapeutic targets—an updated view. Mediators Inflamm 2013; 2013:1–16 [View Article]
     [Google Scholar]
  60. McCallum N, Karauzum H, Getzmann R, Bischoff M, Majcherczyk P et al. In vivo survival of teicoplanin-resistant Staphylococcus aureus and fitness cost of teicoplanin resistance. Antimicrob Agents Chemother 2006; 50:2352–2360 [View Article]
     [Google Scholar]
  61. Scherl A, François P, Charbonnier Y, Deshusses JM, Koessler T et al. Exploring glycopeptide-resistance in Staphylococcus aureus: a combined proteomics and transcriptomics approach for the identification of resistance-related markers. BMC Genomics 2006; 7:296 [View Article]
     [Google Scholar]
  62. Rose WE, Leonard SN, Sakoulas G, Kaatz GW, Zervos MJ et al. Daptomycin activity against Staphylococcus aureus following vancomycin exposure in an in vitro pharmacodynamic model with simulated endocardial vegetations. Antimicrob Agents Chemother 2008; 52:831–836 [View Article]
     [Google Scholar]
  63. Matsuo M, Cui L, Kim J, Hiramatsu K. Comprehensive identification of mutations responsible for heterogeneous vancomycin-intermediate Staphylococcus aureus (hVISA)-to-VISA conversion in laboratory-generated VISA strains derived from hVISA clinical strain Mu3. Antimicrob Agents Chemother 2013; 57:5843–5853 [View Article]
     [Google Scholar]
  64. Friedman L, Alder JD, Silverman JA. Genetic changes that correlate with reduced susceptibility to daptomycin in Staphylococcus aureus. Antimicrob Agents Chemother 2006; 50:2137–2145 [View Article]
     [Google Scholar]
  65. Cameron DR, Ward DV, Kostoulias X, Howden BP, Moellering RC et al. Serine/threonine phosphatase Stp1 contributes to reduced susceptibility to vancomycin and virulence in Staphylococcus aureus. J Infect Dis 2012; 205:1677–1687 [View Article]
     [Google Scholar]
  66. Kuroda M, Kuroda H, Oshima T, Takeuchi F, Mori H et al. Two-component system VraSR positively modulates the regulation of cell-wall biosynthesis pathway in Staphylococcus aureus. Mol Microbiol 2003; 49:807–821 [View Article]
     [Google Scholar]
  67. Howden BP, Smith DJ, Mansell A, Johnson PDR, Ward PB et al. Different bacterial gene expression patterns and attenuated host immune responses are associated with the evolution of low-level vancomycin resistance during persistent methicillin-resistant Staphylococcus aureus bacteraemia. BMC Microbiol 2008; 8:39 [View Article]
     [Google Scholar]
  68. Jarraud S, Mougel C, Thioulouse J, Lina G, Meugnier H et al. Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect Immun 2002; 70:631–641 [View Article]
     [Google Scholar]
  69. Bronner S, Monteil H, Prévost G. Regulation of virulence determinants in Staphylococcus aureus : complexity and applications. FEMS Microbiol Rev 2004; 28:183–200
     [Google Scholar]
  70. van Hal SJ, Paterson DL. Systematic review and meta-analysis of the significance of heterogeneous vancomycin-intermediate Staphylococcus aureus isolates. Antimicrob Agents Chemother 2011; 55:405–410 [View Article]
     [Google Scholar]
  71. Sakoulas G, Eliopoulos GM, Moellering RC, Wennersten C, Venkataraman L et al. Accessory gene regulator (agr) locus in geographically diverse Staphylococcusaureus isolates with reduced susceptibility to vancomycin. Antimicrob Agents Chemother 2002; 46:1492–1502 [View Article]
     [Google Scholar]
  72. Sakoulas G, Eliopoulos GM, Fowler VG, Moellering RC, Novick RP et al. Reduced susceptibility of Staphylococcus aureus to vancomycin and platelet microbicidal protein correlates with defective autolysis and loss of accessory gene regulator (agr) function. Antimicrob Agents Chemother 2005; 49:2687–2692 [View Article]
     [Google Scholar]
  73. Renzoni A, Francois P, Li D, Kelley WL, Lew DP et al. Modulation of fibronectin adhesins and other virulence factors in a teicoplanin-resistant derivative of methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 2004; 48:2958–2965 [View Article]
     [Google Scholar]
  74. Laganas V, Alder J, Silverman JA. In vitro bactericidal activities of daptomycin against Staphylococcus aureus and Enterococcus faecalis are not mediated by inhibition of lipoteichoic acid biosynthesis. Antimicrob Agents Chemother 2003; 47:2682–2684 [View Article]
     [Google Scholar]
  75. Hiramatsu K, Cui L, Kuroda M, Ito T. The emergence and evolution of methicillin-resistant Staphylococcus aureus. Trends Microbiol 2001; 9:486–493 [View Article]
     [Google Scholar]
  76. Schriever CA, Fernández C, Rodvold KA, Danziger LH. Daptomycin: a novel cyclic lipopeptide antimicrobial. Am J Health Syst Pharm 2005; 62:1145–1158 [View Article]
     [Google Scholar]
  77. Camargo ILBdaC, Neoh HM, Cui L, Hiramatsu K. Serial daptomycin selection generates daptomycin-nonsusceptible Staphylococcus aureus strains with a heterogeneous vancomycin-intermediate phenotype. Antimicrob Agents Chemother 2008; 52:4289–4299 [View Article]
     [Google Scholar]
  78. Cui L, Tominaga E, Neoh HM, Hiramatsu K. Correlation between reduced daptomycin susceptibility and vancomycin resistance in vancomycin-intermediate Staphylococcus aureus. Antimicrob Agents Chemother 2006; 50:1079–1082 [View Article]
     [Google Scholar]
  79. Drummelsmith J, Winstall E, Bergeron MG, Poirier GG, Ouellette M et al. Comparative proteomics analyses reveal a potential biomarker for the detection of vancomycin-intermediate Staphylococcus aureus strains. J Proteome Res 2007; 6:4690–4702 [View Article]
     [Google Scholar]
  80. Kuroda M, Kuwahara-Arai K, Hiramatsu K. Identification of the up- and down-regulated genes in vancomycin-resistant Staphylococcus aureus strains Mu3 and Mu50 by cDNA differential hybridization method. Biochem Biophys Res Commun 2000; 269:485–490 [View Article]
     [Google Scholar]
  81. Peterson PK, Verhoef J, Sabath LD, Quie PG. Effect of protein A on staphylococcal opsonization. Infect Immun 1977; 15:760–764
     [Google Scholar]
  82. Gemmell C, Tree R, Patel A, O'reilly M, Foster TJ. Susceptibility to opsonophagocytosis of protein A, alpha-haemolysin and beta-toxin deficient mutants of S. aureus isolated by allele-replacement. Zentralblatt fuer Bakteriologie 1991273–277
     [Google Scholar]
  83. Utaida S, Dunman PM, Macapagal D, Murphy E, Projan SJ et al. Genome-wide transcriptional profiling of the response of Staphylococcus aureus to cell-wall-active antibiotics reveals a cell-wall-stress stimulon. Microbiology 2003; 149:2719–2732 [View Article]
     [Google Scholar]
  84. Yan J, Han D, Liu C, Gao Y, Li D et al. Staphylococcus aureus VraX specifically inhibits the classical pathway of complement by binding to C1q. Mol Immunol 2017; 88:38–44 [View Article]
     [Google Scholar]
  85. Holmes NE, Johnson PD, Howden BP. Relationship between vancomycin-resistant Staphylococcus aureus, vancomycin-intermediate S. aureus, high vancomycin MIC, and outcome in serious S. aureus infections. J Clin Microbiol 2012; 50:2548–2552 [View Article]
     [Google Scholar]
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Reduced vancomycin susceptibility and increased macrophage survival in Staphylococcus aureus strains sequentially isolated from a bacteraemic patient during a short course of antibiotic therapy
J. Med. Microbiol. 68, 848 (2019); https://doi.org/10.1099/jmm.0.000988
/content/journal/jmm/10.1099/jmm.0.000988
/content/journal/jmm/10.1099/jmm.0.000988
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