Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 7, Number 2—April 2001
4th Decennial International Conference on Nosocomial and Healthcare-Associated Infections
State of the Art

Increasing Resistance to Vancomycin and Other Glycopeptides in Staphylococcus aureus

Fred C. Tenover*, James W. Biddle*, and Michael V. Lancaster†
Author affiliations: *Centers for Disease Control and Prevention, Atlanta, Georgia, USA; †Bright Ideas, Monterey, California, USA

Main Article

Table 3

Resistance patterns of staphylococcal study isolates to commonly tested antimicrobial agentsa

Isolate (source) Resistant or intermediateb Susceptible
Staphylococcus aureus (Michigan) Cd, Cip, E, Gm, Ox, P C, L, Q-D, Rif, SXT, T
S. aureus (New Jersey) Cd, Cip, E, Ox, P, Rif C, Gm, L, Q-D, SXT, T
S. aureus (New York) Cip, E, Ox, P, Rif C, Cd, Gm, L, Q-D, SXT, T
S. aureus (Illinois) C(I), Cd, Cip, E, Ox, P, Rif L, Q-D, SXT, T
S. aureus (Germany) Ak, Cd, Cip, E, Gm, Ox, P, Te Fu, Ne
S. aureus (France, LIM-2) C, Cd, Cip, E, Ox, P, Rif, Te C, L, Q-D, SXT

aAs determined using the broth microdilution reference method. bAbbreviations: C: chloramphenicol; Cd: clindamycin; Cip: ciprofloxacin; E: erythromycin; Fu: fusidic acid; Gm: gentamicin; L: linezolid; Ne: netilmycin; Ox: oxacillin; P: penicillin; Q-D, quinupristin-dalfopristin; Rif: rifampin; SXT: trimethoprim/ sulfamethoxazole; T: tetracycline. (I): intermediate. Based on data presented in references 20, 26, 32, and unpublished observations from CDC.

Main Article

  1. Lowy  FD. Staphylococcus aureus infections. N Engl J Med. 1998;339:52032. DOIPubMedGoogle Scholar
  2. Kauffman  CA, Bradley  SF. Epidemiology of community-acquired infection. In: Crossley KB, Archer GL, editors. The staphylococci in human disease. New York: Churchill Livingstone; 1997. p. 287-308.
  3. Cockerill  FR III, Hughes  JG, Vetter  EA, Mueller  RA, Weaver  AL, Ilstrup  DM, Analysis of 281,797 consecutive blood cultures performed over an eight-year period: trends in microorganisms isolated and the value of anaerobic culture of blood. Clin Infect Dis. 1997;24:40318. DOIPubMedGoogle Scholar
  4. Weinstein  MP, Towns  ML, Quartey  SM, Mirrett  S, Reimer  LG, Parmigiani  G, The clinical significance of positive blood cultures in the 1990s: a prospective comprehensive evaluation of the microbiology, epidemiology, and outcome of bacteremia and fungemia in adults. Clin Infect Dis. 1997;24:584602.PubMedGoogle Scholar
  5. Vallés  J, León  C, Alvarez-Lerma  F. Nosocomial bacteremia in critically ill patients: a multicenter study evaluating epidemiology and prognosis. Clin Infect Dis. 1997;24:38795. DOIPubMedGoogle Scholar
  6. Struelens  MJ, Mertens  R. the Groupement pour le Dépistage, l'Etude et la Prévention des Infections Hospitalières. National survey of methicillin-resistant Staphylococcus aureus. Eur J Clin Microbiol Infect Dis. 1994;13:5663. DOIPubMedGoogle Scholar
  7. Maranan  MC, Moreira  B, Boyle-Vavra  S, Daum  RS. Antimicrobial resistance in staphylococci: epidemiology, molecular mechanisms, and clinical relevance. Infect Dis Clin North Am. 1997;11:81349. DOIPubMedGoogle Scholar
  8. Ena  J, Dick  RW, Jones  RN, Wenzel  RP. The epidemiology of intravenous vancomycin usage in a university hospital: a 10 year study. JAMA. 1993;269:598602. DOIPubMedGoogle Scholar
  9. Cunha  BA. Vancomycin. Med Clin North Am. 1995;79:81731.PubMedGoogle Scholar
  10. Kernodle  DS, Kaiser  AB. Postoperative infections and antimicrobial prophylaxis. In: Mandell GL, Bennett JE, Dolin R, editors. Principles and practice of infectious diseases. 4th ed. New York: Churchill Livingstone; 1996. p. 2742-56.
  11. Kirst  HA, Thompson  DG, Nicas  TI. Historical yearly usage of vancomycin. Antimicrob Agents Chemother. 1998;42:13034.PubMedGoogle Scholar
  12. Fridkin  SK, Edwards  JR, Pichette  SC, Pryor  ER, McGowan  JE Jr, Tenover  FC, Determinants of vancomycin use in adult intensive care units in 41 United States Hospitals. Clin Infect Dis. 1999;28:111925. DOIPubMedGoogle Scholar
  13. Hiramatsu  K, Hanaki  H, Ino  T, Yabuta  K, Oguri  T, Tenover  FC. Methicillin-resistant Staphylococcus aureus clinical strain with reduced vancomycin susceptibility. J Antimicrob Chemother. 1997;40:1356. DOIPubMedGoogle Scholar
  14. Centers for Disease Control and Prevention. Staphylococcus aureus with reduced susceptibility to vancomycin-United States, 1997. MMWR Morb Mortal Wkly Rep. 1997;46:7656.PubMedGoogle Scholar
  15. Tenover  FC. VRSA, VISA, and GISA: the dilemma behind the name game. Clin Microbiol Newsl. 2000;22:4953. DOIGoogle Scholar
  16. Johnson  AP. Intermediate vancomycin resistance in Staphylococcus aureus: a major threat or a minor inconvenience? J Antimicrob Chemother. 1998;42:28991. DOIPubMedGoogle Scholar
  17. Waldvogel  FA. New resistance in Staphylococcus aureus. N Engl J Med. 1999;340:5567. DOIPubMedGoogle Scholar
  18. National Committee for Clinical Laboratory Standards. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. 5th ed. Approved standard M7-A5. Wayne (PA): The Committee; 2000.
  19. National Committee for Clinical Laboratory Standards. Performance standards for antimicrobial disk susceptibility tests. 7th ed. Approved standard M2-A7. Wayne (PA): The Committee; 2000.
  20. Tenover  FC, Lancaster  MV, Hill  BC, Steward  C, Stocker  S, Hancock  G, Characterization of staphylococci with reduced susceptibilities to vancomycin and other glycopeptides. J Clin Microbiol. 1998;36:10207.PubMedGoogle Scholar
  21. Goldstein  F, Soussy  C-J, Thabaut  A. Report of the Comité de l'Antibiogramme de la Société Française de Microbiologie. Definition of the clinical antibacterial spectrum of activity. Clin Microbiol Infect. 1996;2:S409. DOIPubMedGoogle Scholar
  22. Working Party of the British Society for Antimicrobial Chemotherapy. Breakpoints in in-vitro antibiotic susceptibility testing. J Antimicrob Chemother. 1988;21:70110. DOIPubMedGoogle Scholar
  23. Hiramatsu  K, Aritaka  N, Hanaki  H, Kawasaki  S, Hosoda  Y, Hori  S, Dissemination in Japanese hospitals of strains of Staphylococcus aureus heterogeneously resistant to vancomycin. Lancet. 1997;350:16703. DOIPubMedGoogle Scholar
  24. Howe  RA, Bowker  KE, Walsh  TR, Feest  TG, MacGowan  AP. Vancomycin-resistant Staphylococcus aureus. Lancet. 1998;351:602. DOIPubMedGoogle Scholar
  25. Wong  SS, Ho  PL, Woo  PC, Yuen  KY. Bacteremia caused by staphylococci with inducible vancomycin heteroresistance. Clin Infect Dis. 1999;29:7607. DOIPubMedGoogle Scholar
  26. Bierbaum  G, Fuchs  K, Lenz  W, Szekat  C, Sahl  H-G. Presence of Staphylococcus aureus with reduced susceptibility to vancomycin in Germany. Eur J Clin Microbiol Infect Dis. 1999;18:6916. DOIPubMedGoogle Scholar
  27. Kantzanou  M, Tassios  PT, Tseleni-Kotsovili  A, Legakis  NJ, Vatopoulos  AC. Reduced susceptibility to vancomycin of nosocomial isolates of methicillin-resistant Staphylococcus aureus. J Antimicrob Chemother. 1999;43:72931. DOIPubMedGoogle Scholar
  28. Geisel  R, Schmitz  F-J, Thomas  L, Berns  G, Zetsche  O, Ulrich  B, Emergence of heterogeneous intermediate vancomycin resistance in Staphylococcus aureus isolates in the Düsseldorf area. J Antimicrob Chemother. 1999;43:8468. DOIPubMedGoogle Scholar
  29. Smith  T, Pearson  ML, Wilcox  KR, Cruz  C, Lancaster  ML, Robinson-Dunn  B, Emergence of vancomycin resistance in Staphylococcus aureus: epidemiology and clinical significance. N Engl J Med. 1999;340:493501. DOIPubMedGoogle Scholar
  30. Rotun  SS, McMath  V, Schoonmaker  DJ, Maupin  PS, Tenover  FC, Hill  BC, Staphylococcus aureus with reduced susceptibility to vancomycin isolated from a patient with fatal bacteremia. Emerg Infect Dis. 1999;5:1479. DOIPubMedGoogle Scholar
  31. Centers for Disease Control and Prevention. Staphylococcus aureus with reduced susceptibility to vancomycin-Illinois, 1999. MMWR Morb Mortal Wkly Rep. 2000;48:11657.PubMedGoogle Scholar
  32. Ploy  MC, Grélaud  C, Martin  C, de Lumley  L, Denis  F. First clinical isolate of vancomycin-intermediate Staphylococcus aureus in a French hospital. Lancet. 1998;351:1212. DOIPubMedGoogle Scholar
  33. Ariza  J, Pujol  M, Cabo  J, Pena  C, Fernandez  N, Linares  J, Vancomycin in surgical infections due to methicillin-resistant Staphylococcus aureus with heterogeneous resistance to vancomycin. Lancet. 1999;353:15878. DOIPubMedGoogle Scholar
  34. Hood  J, Cosgrove  B, Curran  E, Lockhart  M, Thakker  B, Gemmell  C, Vancomycin-intermediate resistant Staphylococcus aureus in Scotland. Abstracts of the 4th Decennial International Conference on Nosocomial and HealthCare-Associated Infections, Mar 2000, Atlanta, Georgia. Atlanta: Centers for Disease Control and Prevention; 2000.
  35. Climo  MW, Patron  RL, Archer  GL. Combinations of vancomycin and beta-lactams are synergistic against staphylococci with reduced susceptibility to vancomycin. Antimicrob Agents Chemother. 1999;43:174753.PubMedGoogle Scholar
  36. Sieradzki  K, Roberts  RB, Haber  SW, Tomasz  A. The development of vancomycin resistance in a patient with methicillin-resistant Staphylococcus aureus infection. N Engl J Med. 1999;340:51723. DOIPubMedGoogle Scholar
  37. Pfeltz  RF, Singh  VK, Schmidt  JL, Batten  MA, Baranyk  CS, Nadakavukaren  MJ, Characterization of passage-selected vancomycin-resistant Staphylococcus aureus strains of diverse parental backgrounds. Antimicrob Agents Chemother. 2000;44:294303. DOIPubMedGoogle Scholar
  38. Boyle-Vavra  S, Berke  SK, Lee  JC, Daum  RS. Reversion of glycopeptide resistance phenotype in Staphylococcus aureus clinical isolates. Antimicrob Agents Chemother. 2000;44:2727. DOIPubMedGoogle Scholar
  39. Hanaki  H, Kuwahara-Arai  K, Boyle-Vavra  S, Daum  RS, Labischinski  H, Hiramatsu  K. Activated cell-wall synthesis is associated with vancomycin resistance in methicillin-resistant Staphylococcus aureus clinical strains Mu3 and Mu50. J Antimicrob Chemother. 1998;42:199209. DOIPubMedGoogle Scholar
  40. Hanaki  H, Labischinski  H, Inaba  Y, Kondo  N, Murakami  H, Hiramatsu  K. Increase in glutamine-non-amidated muropeptides in the peptidoglycan of vancomycin-resistant Staphylococcus aureus strain Mu50. J Antimicrob Chemother. 1998;42:31520. DOIPubMedGoogle Scholar
  41. Fitch  L, Johnson  AP. Reduced susceptibility to teicoplanin in a methicillin-resistant strain of Staphylococcus aureus. J Antimicrob Chemother. 1998;41:578. DOIPubMedGoogle Scholar
  42. Hubert  SK, Mohammed  JM, Fridkin  SK, Gaynes  RP, McGowan  JE Jr, Tenover  FC. Glycopeptide-intermediate Staphylococcus aureus: evaluation of a novel screening method and results of a survey of selected U.S. Hospitals. J Clin Microbiol. 1999;37:35903.PubMedGoogle Scholar
  43. Centers for Disease Control and Prevention. Laboratory capacity to detect antimicrobial resistance, 1998. MMWR Morb Mortal Wkly Rep. 2000;48:116771.PubMedGoogle Scholar
  44. Zimakoff  J, Pedersen  FB, Bergen  L, Baagø-Nielsen  J, Daldorph  B, Espersens  F, Staphylococcus aureus carriage and infections among patients in four haemo- and peritoneal-dialysis center in Denmark. J Hosp Infect. 1996;33:289300. DOIPubMedGoogle Scholar
  45. Centers for Disease Control and Prevention. Interim guideline for prevention and control of staphylococcal infection associated with reduced susceptibility to vancomycin. MMWR Morb Mortal Wkly Rep. 1997;46:6268, 635–6.PubMedGoogle Scholar
  46. Centers for Disease Control and Prevention. Recommendations for preventing the spread of vancomycin resistance: recommendations of the Hospital Infection Control Practices Advisory Committee (HICPAC). Morb Mortal Wkly Rep MMWR 1995;44 (no. RR-12).
  47. Edmonds  MB, Wenzel  RP, Pasculle  AW. Vancomycin-resistant Staphylococcus aureus: perspectives on measures needed for control. Ann Intern Med. 1996;124:32934.PubMedGoogle Scholar
  48. Franchi  D, Climo  MW, Wong  AHM, Edmond  MB, Wenzel  RP. Seeking vancomycin resistant Staphylococcus aureus among patients with vancomycin-resistant enterococci. Clin Infect Dis. 1999;29:15568. DOIPubMedGoogle Scholar
  49. Sieradzki  K, Roberts  R, Serur  D, Hargrave  J, Tomasz  A. Heterogeneously vancomycin-resistant Staphylococcus epidermidis strain causing recurrent peritonitis in a dialysis patient during vancomycin therapy. J Clin Microbiol. 1999;37:3944.PubMedGoogle Scholar
  50. Pagano  L, Tacconelli  E, Tumbarello  M, Laurenti  L, Mele  L, Spanu  T, Teicoplanin-resistant coagulase-negative staphylococcal bacteraemia in patients with haemotologic malignancies: a problem of increasing importance. J Antimicrob Chemother. 1997;40:73840. DOIPubMedGoogle Scholar

Main Article

Page created: April 17, 2012
Page updated: April 17, 2012
Page reviewed: April 17, 2012
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.