Advertisement

Clinical, Epidemiologic, and Laboratory Aspects of Methicillin-Resistant Staphylococcus aureus Infections

  • Elizabeth L. Palavecino
Part of the Methods in Molecular Biology book series (MIMB, volume 1085)

Abstract

Methicillin-resistant Staphylococcus aureus (MRSA) is a major pathogen responsible for both hospital and community onset disease. Resistance to methicillin in S. aureus is mediated by PBP2a, a penicillin-binding protein with low affinity to beta-lactams, encoded by the mecA gene. Accurate susceptibility testing of S. aureus isolates and screening of patients for colonization with MRSA are important tools to limit the spread of this organism. This review focuses on the clinical significance of MRSA infections and new approaches for the laboratory diagnosis and epidemiologic typing of MRSA strains.

Key words

Staphylococcus aureus MRSA HA-MRSA CA-MRSA Antimicrobial resistance Staphylococcal infections Susceptibility testing Molecular typing Virulence 

Notes

Acknowledgments

I thank my research collaborators, Faith Coldren and David Carroll for providing the AFM images, and Carlos A. Fasola for helpful suggestions to the manuscript.

References

  1. 1.
    Panlilio AL, Culver DH, Gaynes RP et al (1992) Methicillin-resistant Staphylococcus aureus in U.S. hospitals, 1975–1991. Infect Control Hosp Epidemiol 13:582–586PubMedCrossRefGoogle Scholar
  2. 2.
    Stefani S, Varaldo PE (2003) Epidemiology of methicillin-resistant staphylococci in Europe. Clin Microbiol Infect 9:1179–1186PubMedCrossRefGoogle Scholar
  3. 3.
    Kuehnert MJ, Hill HA, Kupronis BA et al (2005) Methicillin-resistant-Staphylococcus aureus hospitalizations, United States. Emerg Infect Dis 11:868–872PubMedCrossRefGoogle Scholar
  4. 4.
    Mera RM, Suaya JA, Amrine-Madsen H et al (2011) Increasing role of Staphylococcus aureus and community-acquired methicillin-resistant Staphylococcus aureus infections in the United States: a 10-year trend of replacement and expansion. Microb Drug Resist 17:321–328PubMedCrossRefGoogle Scholar
  5. 5.
    Rosenthal VD, Bijie H, Maki DG et al (2012) International Nosocomial Infection control consortium (INICC) report, data summary of 36 coutries, for 2004–2009. Emerg Infect Dis 18:700–702PubMedCrossRefGoogle Scholar
  6. 6.
    Cosgrove SE, Qi Y, Kaye KS et al (2005) The impact of methicillin resistance in Staphylococcus aureus bacteremia on patient outcomes: mortality, length of stay, and hospital charges. Infect Control Hosp Epidemiol 26:166–174PubMedCrossRefGoogle Scholar
  7. 7.
    Abramson MA, Sexton DJ (1999) Nosocomial methicillin-resistant and methicillin-susceptible Staphylococus aureus primary bacteremia: at what costs? Infect Control Hosp Epidemiol 20:408–411PubMedCrossRefGoogle Scholar
  8. 8.
    Hidron AI, Edwards JR, Patel J et al (2008) HHSN annual update: antimicrobial-resistant pathogens associated with Health-care-associated infections: annual summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006–2007. Infect Control Hosp Epidemiol 29:996–1011PubMedCrossRefGoogle Scholar
  9. 9.
    Wisplinghoff H, Bischoff T, Tallent SM, Seifert H, Wenzel RP, Edmond MB (2004) Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin Infect Dis 39:309–317PubMedCrossRefGoogle Scholar
  10. 10.
    Jones ME, Draghi DC, Thornsberry C, Karlowsky JA, Sahm DF, Wenzel RP (2004) Emerging resistance among bacterial pathogens in the intensive care unit—a European and North American Surveillance study (2000–2002). Ann Clin Microbiol Antimicrob 29(3):14CrossRefGoogle Scholar
  11. 11.
    O’Hara FP, Amrine-Madsen H, Mera RM et al (2012) Molecular characterization of Staphylococcus aureus in the United States 2004–2008 reveals the rapid expansion of USA 300 among inpatients and outpatients. Microb Drug Resist 18:555PubMedCrossRefGoogle Scholar
  12. 12.
    Palavecino E (2004) Community-acquired methicillin-resistant Staphylococcus aureus infections. Clin Lab Med 24:403–418PubMedCrossRefGoogle Scholar
  13. 13.
    Herold BC, Immergluck LC, Maranan MC et al (1998) Community-acquired methicillin-resistant Staphylococcus aureus in children with no identified predisposing risk. JAMA 279:593–598PubMedCrossRefGoogle Scholar
  14. 14.
    Francis JS, Doherty MC, Lopatin U et al (2005) Severe community-onset pneumonia in healthy adults caused by methicillin-resistant Staphylococcus aureus carrying the Panton-Valentine leukocidin genes. Clin Infect Dis 40:100–107PubMedCrossRefGoogle Scholar
  15. 15.
    Miller LG, Perdreau-Remington F, Rieg G et al (2005) Necrotizing fasciitis caused by community-associated methicillin-resistant Staphylococcus aureus in Los Angeles. N Engl J Med 352:1445–1453PubMedCrossRefGoogle Scholar
  16. 16.
    Naimi TS, LeDell KH, Como-Sabetti K et al (2003) Comparison of community- and health care-associated methicillin-resistant Staphylococcus aureus infection. JAMA 290:2976–2984PubMedCrossRefGoogle Scholar
  17. 17.
    Fey PD, Said-Salim B, Rupp ME et al (2003) Comparative molecular analysis of community- or hospital-acquired methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 47:196–203PubMedCrossRefGoogle Scholar
  18. 18.
    Mulvey MR, MacDougall L, Cholin B et al (2005) Community-associated methicillin-resistant Staphylococcus aureus, Canada. Emerg Infect Dis 11:844–850PubMedCrossRefGoogle Scholar
  19. 19.
    Vandenesch F, Naimi T, Enright MC et al (2003) Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: worldwide emergence. Emerg Infect Dis 9:978–984PubMedCrossRefGoogle Scholar
  20. 20.
    Okuma K, Iwakawa K, Turnidge JD et al (2002) Dissemination of new methicillin-resistant Staphylococcus aureus clones in the community. J Clin Microbiol 40:4289–4294PubMedCrossRefGoogle Scholar
  21. 21.
    Deurenberg RH, Stobberingh EE (2008) The evolution of Staphylococcus aureus. Infect Genet Evol 8:747–763PubMedCrossRefGoogle Scholar
  22. 22.
    Moran GJ, Krishnadasan A, Gorwitz RJ et al (2006) Methicillin-resistant S aureus infections among patients in the emergency department. N Engl J Med 355:666–674PubMedCrossRefGoogle Scholar
  23. 23.
    Gonzalez BE, Rueda AM, Shelburne SA III et al (2006) Community-associated strains of methicillin-resistant Staphylococcus aureus as the cause of healthcare-associated infection. Infect Control Hosp Epidemiol 27:1051–1056PubMedCrossRefGoogle Scholar
  24. 24.
    Maree CL, Daum RS, Boyle-Vavra S et al (2007) Community-associated methicilin resistant Staphylococcus aureus isolates causing health-care associated infections. Emerg Infect Dis 13:236–242PubMedCrossRefGoogle Scholar
  25. 25.
    Valsesia G, Rossi M, Bertschy S et al (2010) Emergence of SCCmec type IV and SCCmec type V methicillin-resistant Staphylococcus aureus containing the Panton-Valentine leukocidin genes in a large academic teaching hospital in central Switzerland: external invaders or persisting circulators? J Clin Microbiol 48:720–727PubMedCrossRefGoogle Scholar
  26. 26.
    Otter JA, French GL (2011) Community-associated meticillin-resistant Staphylococcus aureus strains as a cause of healthcare-associated infection. J Hosp Infect 79:189–193PubMedCrossRefGoogle Scholar
  27. 27.
    Varga M, Kuntova L, Pantucek R et al (2012) Efficient transfer of antibiotic resistance plasmids by transduction within methicillin-resistant Staphylococcus aureus USA 300 clone. FEMS Microbiol Lett 332:146–152PubMedCrossRefGoogle Scholar
  28. 28.
    Molla B, Byrne M, Abley M et al (2012) Epidemiology and genotypic characteristics of methicillin-resistant Staphylococcus aureus strains of porcine origen. J Clin Microbiol 50:3687–3693PubMedCrossRefGoogle Scholar
  29. 29.
    Krziwanek K, Metz-Gercek S, Mittermayer H (2009) Methicillin-resistant Staphylococcus aureus ST398 from human patients, upper Austria. Emerg Infect Dis 15:766–769PubMedCrossRefGoogle Scholar
  30. 30.
    Mammina C, Cala C, Plano MR, Bonura C, Vella A, Monastero R, Palma DM (2010) Ventilator-associated pneumonia and MRSA ST398, Italy. Emerg Infect Dis 16:730–731Google Scholar
  31. 31.
    McCormick JK, Yarwood JM, Schlievert PM (2001) Toxic shock syndrome and bacterial superantigens: an update. Annu Rev Microbiol 55:77–104PubMedCrossRefGoogle Scholar
  32. 32.
    Lina G, Piemont Y, Godail-Gamot F et al (1999) Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis 29:1128–1132PubMedCrossRefGoogle Scholar
  33. 33.
    Said-Salim B, Mathena B, Braughton K et al (2005) Differential distribution and expression of Panton-Valentine leucocidin among community-acquired methicillin-resistant Staphylococcus aureus strains. J Clin Microbiol 43:3373–3379PubMedCrossRefGoogle Scholar
  34. 34.
    Labandeira-Rey M, Couzon F, Boisset S et al (2007) Staphylococcus aureus Panton-Valentine leukocidin causes necrotizing pneumonia. Science 315:1130–1133PubMedCrossRefGoogle Scholar
  35. 35.
    Voyich JM, Otto M, Mathema B et al (2006) Is Panton-Valentine leukocidin the major virulence determinant in community-associated methicillin-resistant Staphylococcus aureus disease? J Infect Dis 194:1761–1770PubMedCrossRefGoogle Scholar
  36. 36.
    Wang R, Braugton KR, Kretschmer D et al (2007) Identification of novel cytolytic peptides as key virulence determinants for community-associated MRSA. Nat Med 13:1510–1514PubMedCrossRefGoogle Scholar
  37. 37.
    Barber M (1961) Methicillin-resistant staphylococci. J Clin Pathol 14:385–393PubMedCrossRefGoogle Scholar
  38. 38.
    McDougal LK, Thornsberry C (1986) The role of beta-lactamase in staphylococcal resistance to penicillinase-resistant penicillins and cephalosporins. J Clin Microbiol 23:832–839PubMedGoogle Scholar
  39. 39.
    Tomasz A, Drugeon HB, de Lencastre HM et al (1989) New mechanism for methicillin resistance in Staphylococcus aureus: clinical isolates that lack the PBP 2a gene and contain normal penicillin-binding proteins with modified penicillin-binding capacity. Antimicrob Agents Chemother 33:1869–1874PubMedCrossRefGoogle Scholar
  40. 40.
    Ubukata K, Yamashita N, Konno M (1985) Occurrence of a beta-lactam-inducible penicillin-binding protein in methicillin-resistant staphylococci. Antimicrob Agents Chemother 27:851–857PubMedCrossRefGoogle Scholar
  41. 41.
    Chambers HF (1997) Methicillin resistance in staphylococci: molecular and biochemical basis and clinical implications. Clin Microbiol Rev 10:781–791PubMedGoogle Scholar
  42. 42.
    Fasola EL, Peterson LR (1992) Laboratory detection and evaluation of antibiotic-resistant Staphylococcus aureus nosocomial infections. Advances in pathology and laboratory medicine, vol 5. Mosby-Year Book, Inc., Chicago, IL, pp 285–306Google Scholar
  43. 43.
    Hiramatsu K, Cui L, Kuroda M et al (2001) The emergence and evolution of methicillin-resistant Staphylococcus aureus. Trends Microbiol 9:486–493PubMedCrossRefGoogle Scholar
  44. 44.
    Song MD, Wachi M, Doi M et al (1987) Evolution of an inducible penicillin-target protein in methicillin-resistant Staphylococcus aureus by gene fusion. FEBS Lett 221:167–171PubMedCrossRefGoogle Scholar
  45. 45.
    Katayama Y, Ito T, Hiramatsu K (2000) A new class of genetic element, staphylococcus cassette chromosome mec, encodes methicillin resistance in Staphylococcus aureus. Antimicrob Agents Chemother 44:1549–1555PubMedCrossRefGoogle Scholar
  46. 46.
    Ito T, Katayama Y, Asada K et al (2001) Structural comparison of three types of staphylococcal cassette chromosome mec integrated in the chromosome in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 45:1323–1336PubMedCrossRefGoogle Scholar
  47. 47.
    International Working Gropu on the Staphylococcal Cassette Chromosome elements. http://www.sccmec.org/Pages/SCC_TypesEN.html. Accessed 26 Oct 2012
  48. 48.
    Ito T, Ma XX, Takeuchi F et al (2004) Novel type V staphylococcal cassette chromosome mec driven by a novel cassette chromosome recombinase, ccrC. Antimicrob Agents Chemother 48:2637–2651PubMedCrossRefGoogle Scholar
  49. 49.
    Oliveira DC, Milheirico C, de Lencastre H (2006) Redefining a structural variant of staphylococcal cassette chromosome mec, SCC type VI. Antimicrob Agents Chemother 50:3457–3459PubMedCrossRefGoogle Scholar
  50. 50.
    Takano T, Higuchi W, Otsuka T et al (2008) Novel Characteristics of community-acquired methicillin-resistant Staphylococcus aureus belonging to multilocus sequence type 59 in Taiwan. Antimicrob Agents Chemother 52:837–845PubMedCrossRefGoogle Scholar
  51. 51.
    Hiramatsu K, Hanaki H, Ino T et al (1997) Methicillin-resistant Staphylococcus aureus clinical strain with reduced vancomycin susceptibility. J Antimicrob Chemother 40:135–136PubMedCrossRefGoogle Scholar
  52. 52.
    Center for Disease Control and Prevention. CDC reminds clinical laboratories and healthcare preventionists of their role in the search and containment of vancomycin-resistant Staphylococcus aureus. http://www.cdc.gov/HAI/settings/lab/vrsa_lab_search_contaiment.html. Accessed 23 July 2013
  53. 53.
    Appelbaum PC (2007) Reduced glycopeptides susceptibility in methicillin-resistant Staphylococcus aureus (MRSA). Int J Antimicrob Agents 30:398–408PubMedCrossRefGoogle Scholar
  54. 54.
    Sievert DM, Rudrik JT, Patel JB et al (2008) Vancomycin-resistant Staphylococcus aureus in the United States, 2002–2006. Clin Infect Dis 46:668–674PubMedCrossRefGoogle Scholar
  55. 55.
    Finks J, Wells E, Dyke TL et al (2009) Vancomycin-resistant Staphylococcus aureus, Michigan, USA, 2007. Emerg Infect Dis 15:943–945PubMedCrossRefGoogle Scholar
  56. 56.
    Tiwari HK, Sen MR (2006) Emergence of vancomycin resistant Staphylococcus aureus (VRSA) from a tertiary care hospital from northern part of India. BMC Infect Dis 26:6–156Google Scholar
  57. 57.
    Azimiam A, Havaei SA, Faseli H et al (2012) Genetic characterization of a vancomycin-resistant Staphylococcus aureus isolate from the respiratory tract of a patient in a University Hospital in Northeastern Iran. J Clin Microbiol 50:3581–3585CrossRefGoogle Scholar
  58. 58.
    Tenover FC, McDonald LC (2005) Vancomycin-resistant staphylococci and enterococci: epidemiology and control. Curr Opin Infect Dis 18:300–305PubMedCrossRefGoogle Scholar
  59. 59.
    Severin A, Wu SW, Tabei K et al (2004) Penicillin-binding protein 2 is essential for expression of high-level vancomycin resistance and cell wall synthesis in vancomycin-resistant Staphylococcus aureus carrying the enterococcal vanA gene complex. Antimicrob Agents Chemother 48:4566–4573PubMedCrossRefGoogle Scholar
  60. 60.
    Coldren FM, Palavecino E, Carroll DL (2005) Atomic force microscopy as a potential diagnostic technique in staphylococcal infections. Microsc Microanal 11(Suppl 2):980–981PubMedGoogle Scholar
  61. 61.
    Coldren FM, Palavecino EL, Levi-Polyachenko NH et al (2009) Encapsulated Staphylococcus aureus strains vary in adhesiveness assessed by atomic force microscopy. J Biomed Mater Res A 89:402–410PubMedGoogle Scholar
  62. 62.
    Tollersrud T, Berge T, Andersen SR et al (2001) Imaging the surface of Staphylococcus aureus by atomic force microscopy. APMIS 109:541–545PubMedCrossRefGoogle Scholar
  63. 63.
    Boyle-Vavra S, Hahm J, Sibener SJ et al (2000) Structural and topological differences between a glycopeptide-intermediate clinical strain and glycopeptide-susceptible strains of Staphylococcus aureus revealed by atomic force microscopy. Antimicrob Agents Chemother 44:3456–3460PubMedCrossRefGoogle Scholar
  64. 64.
    Crisostomo MI, Westh H, Tomasz A et al (2001) The evolution of methicillin resistance in Staphylococcus aureus: similarity of genetic backgrounds in historically early methicillin-susceptible and -resistant isolates and contemporary epidemic clones. Proc Natl Acad Sci USA 98:9865–9870PubMedCrossRefGoogle Scholar
  65. 65.
    Enright MC, Robinson DA, Randle G et al (2002) The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). Proc Natl Acad Sci USA 99:7687–7692PubMedCrossRefGoogle Scholar
  66. 66.
    Robinson DA, Enright MC (2003) Evolutionary models of the emergence of methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 47:3926–3934PubMedCrossRefGoogle Scholar
  67. 67.
    Feil EJ, Cooper JE, Grundmann H et al (2003) How clonal is Staphylococcus aureus? J Bacteriol 11:3307–3316CrossRefGoogle Scholar
  68. 68.
    Oliveira DC, Tomasz A, de Lencastre H (2002) Secrets of success of a human pathogen: molecular evolution of pandemic clones of methicillin-resistant Staphylococcus aureus. Lancet Infect Dis 2:180–189PubMedCrossRefGoogle Scholar
  69. 69.
    Bartel MD, Boye K, Rhod LA (2007) Rapid increase of genetically diverse methicillin-resistant Staphylococcus aureus, Copenhagen, Denmark. Emerg Infect Dis 13:1533–1540CrossRefGoogle Scholar
  70. 70.
    Peterson LR, Petzel RA, Clabots CR et al (1993) Medical technologists using molecular epidemiology as part of the infection control team. Diagn Microbiol Infect Dis 16:303–311PubMedCrossRefGoogle Scholar
  71. 71.
    Tenover F, Arbeit R, Goering RV et al (1995) Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 33:2233–2239PubMedGoogle Scholar
  72. 72.
    McDougal LK, Steward CD, Killgore GE et al (2003) Pulsed-field gel electrophoresis typing of oxacillin-resistant Staphylococcus aureus isolates from the United States: establishing a national database. J Clin Microbiol 41:5113–5120PubMedCrossRefGoogle Scholar
  73. 73.
    Stefani S, Chung DR, Lindsay JA (2012) Meticillin-resistant Staphylococcus aureus (MRSA): global epidemiology and harmonisation of typing methods. Int J Antimicrob Agents 39:273–282PubMedCrossRefGoogle Scholar
  74. 74.
    Enright MC, Day NP, Davies CE et al (2000) Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol 38:1008–1015PubMedGoogle Scholar
  75. 75.
    van Belkum A, Kluytmans J, van Leeuwen W et al (1995) Multicenter evaluation of arbitrarily primed PCR for typing of Staphylococcus aureus strains. J Clin Microbiol 33:1537–1547PubMedGoogle Scholar
  76. 76.
    Babouee B, Frei R, Schultheiss E et al (2011) Comparison of the DiversiLab repetitive element PCR system with spa typing and pulsed-field gel electrophoresis for clonal characterization of methicillin-resistant Staphylococcus aureus. J Clin Microbiol 49:1549–1955PubMedCrossRefGoogle Scholar
  77. 77.
    Shopsin B, Gomez M, Montgomery SO et al (1999) Evaluation of protein A gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains. J Clin Microbiol 37:3556–3563PubMedGoogle Scholar
  78. 78.
    Milheirico C, Oliveira DC, de Lencastre H (2007) Update to the multiplex PCR strategy for assignment of mec element types in Staphylococcus aureus. Antimicrob Agents Chemother 51:3374–3377PubMedCrossRefGoogle Scholar
  79. 79.
    Oliveira DC, Milheirico C, Vinga S et al (2006) Assessment of allelic variation in the ccrAB locus in methicillin-resistant Staphylococcus aureus clones. J Antimicrob Chemother 58:23–30PubMedCrossRefGoogle Scholar
  80. 80.
    Dunman PM, Mounts W, McAleese F et al (2004) Uses of Staphylococcus aureus GeneChips in genotyping and genetic composition analysis. J Clin Microbiol 42:4275–4283PubMedCrossRefGoogle Scholar
  81. 81.
    CLSI (2012) Performance standards for antimicrobial susceptibility testing; Twentieth informational supplement. CLSI document M100-S22. Clinical Laboratory Standard Institute, Wayne, PAGoogle Scholar
  82. 82.
    European Committee on Antimicrobial Susceptibility Testing (EUCAST). Clinical Breakpoints. http://www.eucast.org/clinical_breakpoints/. Accessed 23 Sept 2012
  83. 83.
    Chambers HF, Hackbarth CJ (1987) Effect of NaCl and nafcillin on penicillin-binding protein 2a and heterogeneous expression of methicillin resistance in Staphylococcus aureus. Antimicrob Agents Chemother 31:1982–1988PubMedCrossRefGoogle Scholar
  84. 84.
    Swenson JM, Tenover FC, Cefoxitin Disk Study Group (2005) Results of disk diffusion testing with cefoxitin correlate with presence of mecA in Staphylococcus spp. J Clin Microbiol 43:3818–3823PubMedCrossRefGoogle Scholar
  85. 85.
    Swenson JM, Williams PP, Killgore G et al (2001) Performance of eight methods, including two new rapid methods, for detection of oxacillin resistance in a challenge set of Staphylococcus aureus organisms. J Clin Microbiol 39:3785–3788PubMedCrossRefGoogle Scholar
  86. 86.
    Tenover FC, Moellering RC (2007) The rationale for revising the Clinical and Laboratory Standards Institute vancomycin minimal inhibitory concentration interpretative criteria for Staphylococcus aureus. Clin Infect Dis 44:1208–1215PubMedCrossRefGoogle Scholar
  87. 87.
    Swenson JM, Anderson KF, Lonsway DR et al (2009) Accuracy of Commercial and reference susceptibility testing methods for detecting vancomycin-intermediate Staphylococcus aureus. J Clin Microbiol 47:2013–2017PubMedCrossRefGoogle Scholar
  88. 88.
    Steinkraus G, White R, Friedrich L (2007) Vancomycin MIC creep in non-vancomycin-intermediate Staphylococcus aureus (VISA), vancomycin-susceptible clinical methicillin-resistant S aureus (MRSA) blood isolates from 2001-2005. J Antimicrob Chemother 60:788–794PubMedCrossRefGoogle Scholar
  89. 89.
    Holmes RL, Jorgensen JH (2008) Inhibitory activities of 11 antimicrobial agents and bactericidal activities of vancomycin and daptomycin against invasive methicillin-resistant Staphylococcus aureus isolates obtained from 1999 through 2006. Antimicrob Agents Chemother 52:757–760PubMedCrossRefGoogle Scholar
  90. 90.
    Sader HS, Fey PD, Fish DN et al (2009) Evaluation of Vancomycin and Daptomycin Potency Trends (MIC Creep) against Methicillin-Resistant Staphylococcus aureus Isolates Collected in Nine U.S. Medical Centers from 2002 to 2006. Antimicrob Agents Chemother 53:4127–4132PubMedCrossRefGoogle Scholar
  91. 91.
    Howden BP, Davies JK, Johnson PDR et al (2010) Reduced vancomycin susceptibility in Staphylococcus aureus, including vancomyicn-intermediate strains: resistance mechanisms, laboratory detection, and clinical implications. Clin Microbiol Rev 23:99–139PubMedCrossRefGoogle Scholar
  92. 92.
    Hsu DI, Hidayat LK, Quist R et al (2008) Comparison of method-specific vancomycin minimum inhibitory concentration values and their predictability for treatment outcome of methicillin-resistant Staphylococcus aureus (MRSA) infections. Int J Antimicrob Agents 32:378–385PubMedCrossRefGoogle Scholar
  93. 93.
    Charles PG, Ward PB, Johnson PD et al (2004) Clinical features associated with bacteremia due to heterogeneous vancomycin-intermediate Staphylococcus aureus. Clin Infect Dis 38:448–451PubMedCrossRefGoogle Scholar
  94. 94.
    Howden BP, Ward PB, Charles PG et al (2004) Treatment outcomes for serious infections caused by methicillin-resistant Staphylococcus aureus with reduced vancomycin susceptibility. Clin Infect Dis 38:521–528PubMedCrossRefGoogle Scholar
  95. 95.
    Gu B, Kelesidis T, Tsiodras S et al (2013) The emerging problem of linezolid-resistant Staphylococcus. J Antimicrob Chemother 68:4. doi: 10.1093/jac/dks354 PubMedCrossRefGoogle Scholar
  96. 96.
    Tenover FC, Williams PP, Stocker S et al (2007) Accuracy of six antimicrobial susceptibility methods for testing linezolid against staphylococci and enterococci. J Clin Microbiol 45:2917–2922PubMedCrossRefGoogle Scholar
  97. 97.
    Palavecino EL, Burnell JM (2013) False daptomycin non-susceptible MIC results by Microscan panel PC29 compared to Etest in Staphylococcus aureus and enterococci. J Clin Microbiol 51:281. doi: 10.1128/JCM.01721-12 PubMedCrossRefGoogle Scholar
  98. 98.
    Friedrich L, Thorne G, Steenbergen JN et al (2009) Evidence for daptomycin Etest lot-related MIC elevations for Staphylococcus aureus. Diagn Microbiol Infect Dis 65:306–311PubMedCrossRefGoogle Scholar
  99. 99.
    Steed ME, Rybak MJ (2010) Ceftaroline: a new cephalosporin with activity against resistant gram-positive pathogens. Pharmacotherapy 30:375–389PubMedCrossRefGoogle Scholar
  100. 100.
    Jones ME (2007) In vitro profile of a new beta-lactam, ceftobiprole, with activity against methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect 13(Suppl 2):17–24PubMedCrossRefGoogle Scholar
  101. 101.
    Farrell DJ, Castanheira M, Mendes RE et al (2012) In vitro activity of ceftaroline against multidrug-resistant Staphylococcus aureus and Streptococcus pneumoniae: a review of published studies and the AWARE Surveillance Program (2008–2010). Clin Infect Dis 55(Suppl 3):S206–S214PubMedCrossRefGoogle Scholar
  102. 102.
    Castanheira M, Sader HS, Farrel DJ et al (2012) Activity of ceftaroline-avibactam tested against Gram-negative organism populations, including strains expressing one or more β-lactamases and methicillin-resistant Staphylococcus aureus carrying various staphylococcal cassette chromosome mec types. Antimicrob Agents Chemother 56:4779–4785PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2014

Authors and Affiliations

  • Elizabeth L. Palavecino
    • 1
  1. 1.Department of PathologyWake Forest School of MedicineWinston-SalemUSA

Personalised recommendations