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An optimal method for generating stable vancomycin heteroresistance and intermediate susceptibility in methicillin-resistant Staphylococcus aureus blood isolates under in-vitro vancomycin pressure

Year 2012, Volume: 2 Issue: 04, 129 - 134, 01.12.2012
https://doi.org/10.5799/jmid.123125

Abstract

Objectives: The relevance of vancomycin intermediately-susceptible (VISA) and hetero-resistant (hVISA) methicillin-resistant Staphylococcus aureus (MRSA) remains uncertain because of their low frequency. In vitro attempts to generate reduced susceptibility have been inconsistent. We describe a simple method for generating VISA/hVISA. Materials and methods: Twenty-four SCCmec type II and IV MRSA blood isolates plus USA100 and USA300 controls were cultured (107 CFU/ml) in BHI broth with 0, 2 and 3 mg/L vancomycin for 10 days followed by 10 days vancomycin-free-passage. We monitored vancomycin minimum inhibitory concentration (MIC; Etest) and population analysis profile-area under the curve (PAP-AUC) ratios of tested isolate/Mu3 during and after vancomycin pressure (VP). PAP-AUC ratios 1.3 were considered consistent with susceptible, hVISA and VISA, respectively. Results: VP at 2 mg/L (VP-2) increased MIC to 3 mg/L in 20 (83.3%) isolates and raised PAP-AUC ratio to hVISA (n=18; 75.0%) and VISA (six; 25.0%) ranges. VP-3 increased MIC to 3 and 4 mg/L in 19 (79.2%) and three (12.5%) isolates, respectively and raised PAP-AUC ratio to hVISA (n=3; 12.5%) and VISA (n=19; 79.2%) ranges. SCCmec IV isolates had lower pre-exposure PAP-AUC ratios (0.48&plusmn;0.14 vs. 0.69&plusmn;0.10; p<0.001) and lower MIC (1.6&plusmn;0.2 vs. 1.8&plusmn;0.2 mg/L; p=0.1) but MIC rise and hVISA/VISA emergence was comparable. MIC and PAP-AUC ratio rises were stable in 20/22 isolates during drug-free passages. Conclusions: VISA/hVISA readily emerges among MRSA SCCmec type II and IV isolates under VP. VP at the MIC level generates hVISA while pressure at slightly higher level results in the VISA phenotype.

References

  • Bae IG, Federspiel JJ, Miró JM, et al. Heterogeneous vanco- mycin-intermediate susceptibility phenotype in bloodstream methicillin-resistant Staphylococcus aureus isolates from an international cohort of patients with infective endocarditis: prevalence, genotype and clinical significance. J Infect Dis 2009; 200:1355-1366.
  • Fridkin SK, Hageman J, McDougal KL, et al. Vancomycin-Inter- mediate Staphylococcus aureus Epidemiology Study Group. Epidemiological and microbiological characterization of infec- tion caused by Staphylococcus aureus with reduced suscep- tibility to vancomycin, United States, 1997-2001. Clin Infect Dis 2003; 36:429-439.
  • Khatib R, Jose J, Musta AC, et al. The relevance of vanco- mycin-intermediate susceptibility and heteroresistance in methicillin-resistant Staphylococcus aureus bacteremia. J Antimicrob Chem 2011; 66:1594-1599.
  • Kosowaska-shick K, Ednie LM, McGhee P, et al. Incidence and characteristics of vancomycin nonsusceptible strains of methicillin-resistant Staphylococcus aureus at Hershey medi- cal center. Antimicrob Agent Chemother 2008; 52:4510-4513.
  • Musta AC, Riederer K, Shemes S, et al. Vancomycin MIC plus heteroresistance and the outcome of methicillin-resistant Staphylococcus aureus bacteremia: trends over 11 years. J Clin Microbiol 2009; 47:1640-1644.
  • Riederer K, Shemes S, Chase P, Musta AC, Mar A, Khatib R. Detection of intermediately vancomycin-susceptible and het- erogeneous Staphylococcus aureus isolates: comparison of Etest and agar screening methods. J Clin Microbiol 2011; 49:2147-2150.
  • Rybak MJ, Leonard SN, Rossi KL, Cheung CM, Sadar HS, Jones RN. Characterization of vancomycin-heteroresistant Staphylococcus aureus from the Metropolitan Area of Detroit, Michigan, over a 22-year period (1986-2007). J Clin Microbiol 2008; 46:2950-2954.
  • Sieradzki K, Leski T, Dick J, Borio L, Tomasz A. 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.
  • Howden BP, Ward PB, Robson J, Morris AJ, Mayall BC, Gray- son ML. Treatment outcomes for serious infections caused by methicillin-resistant Staphylococcus aureus with reduced vancomycin susceptibility. Clin Infect Dis 2004; 38:521-528.
  • Fong RK, Low J, Koh TH, Kurup A. Clinical features and treat- ment outcomes of vancomycin-intermediate Staphylococcus aureus (VISA) and heteroresistant vancomycin-intermediate Staphylococcus aureus (hVISA) in a tertiary care institution in Singapore. Eur J Clin Microbiol Infect Dis 2009; 28:983-987.
  • Moise PA, Forrest A, Bayer AS, Xiong YQ, Yeaman MR, Sakoulas G. Factors influencing time to vancomycin-induced clearance of non-endocarditis methicillin-resistant Staphylo- coccus aureus bacteremia: role of platelet microbial protein killing and agr genotypes. J Infect Dis 2010; 201:233-240.
  • Sakoulas G, Gold HS, Cohen RA, Venkataraman L, Moel- lering RC, Eliopoulos GM. Effects of prolonged vancomycin administration on methicillin-resistant Staphylococcus aureus (MRSA) in a patient with recurrent bacteremia. J Antimicrob Chemother 2006; 57:699-704.
  • Song JH. Emergence of Staphylococcus aureus with reduced susceptibility to vancomycin in Asia. In: LU Yichen, eds. Emerging Infections in Asia. New York: Springer, 2008; 233- 242.
  • Moise PA, Smyth DS, El-Fawal N, et al. Microbiological effects of prior vancomycin use in patients with methicillin-resistant Staphylococcus aureus bacteraemia. J Antimicrob Chemoth- er 2008; 61:85-90.
  • Vaudaux P, Francois P, Berger-Bachi B, Lew DP. In vivo emer- gence of subpopulations expressing teicoplanin or vanco- mycin resistance phenotypes in a glycopeptide-susceptible, methicillin-resistant strain of Staphylococcus aureus. J Anti- microb Chemother 2001; 47:163-170.
  • Chui L, Ma X, Sato K, et al. Cell wall thickening is a common feature of vancomycin resistance in Staphylococcus aureus. J Clin Microbiol 2003; 41:5-14.
  • Sakoulas G, Eliopoulos GM, Moellering RC Jr, et al. Staphy- lococcus aureus accessory gene regulator (agr) group II: is there a relationship to the development of intermediate-level glycopeptide resistance? J Infect Dis 2003; 187:929-938.
  • Hanaki H, Kuwahara-Arai K, Boyle-Varva S, Daum RS, La- bischinski H, Hiramatsu K. Activated cell-wall synthesis is as- sociated with vancomycin resistant Staphylococcus aureus clinical strains Mu3 and Mu50. J Antimicrob Chemother 1998; 42:199-209.
  • Cameron DR, Ward DV, Kostoulias X et al. Serine/threonine phosphatase Stp1 contributes to reduced susceptibility to vancomycin and virulence in Staphylococcus aureus. J Infect Dis 2012; 205:1677-1687.
  • Howden BP, Davies JK, Johnsosn PDR, Stinear TP, Grayson ML. Reduced vancomycin susceptibility in Staphylococcus aureus, including vancomycin-intermediate and heteroge- neous vancomycin-intermediate strains: resistance mecha- nisms, laboratory detection, and clinical implications. Clin Microbiol Rev 2010; 23: 99-139.
  • Rose WE, Leonard SN, Rossi KL, Kaatz GW, Rybak MJ. Im- pact of inoculum size and heterogeneous vancomycin-inter- mediate Staphylococcus aureus (hVISA) on vancomycin ac- tivity and emergence of VISA in an in-vitro pharmacodynamic model. Antimicrob Agents Chemother 2009; 53:805-807.
  • Plipat N, Livni G, Bertram H, Thompson RB Jr. Unstable van- comycin heteroresistance is common among clinical isolates of methicillin-resistant Staphylococcus aureus. J Clin Micro- biol 2005; 43:2494-2496.
  • Wong SSY, Ho PL, Woo PCY, Yuen KY. Bacteremia caused by staphylococci with inducible vancomycin resistance. Clin Infect Dis 1999; 29:760-767.
  • Daum RS, Gupta S, Sabbagh R, Milewski WM. Characteriza- tion of Staphylococcus aureus isolates with decreased sus- ceptibility to vancomycin and teicoplanin: isolation and puri- fication of a constitutively produced protein associated with susceptibility. J Infect Dis 1992; 166:1066-1072.
  • Pfeltz RF, Singh VK, Schmidt JL, et al. Characterization of passage-selected vancomycin-resistant Staphylococcus aureus strains of diverse parental backgrounds. Antimicrob Agents Chemother 2000; 44:294-303.
  • Zafar U, Johnson LB, Hanna M, et al. Prevalence of nasal colonization among patients with community-associated methicillin-resistant Staphylococcus aureus infection and their household contacts. Infect Control Hosp Epidemiol 2007; 28:966-969.
  • Wootton M, Howe RA, Hillman R, Walsh TR, Bennett PM, MacGowan AP. A modified population analysis profile (PAP) method to detect hetero-resistance to vancomycin in Staphy- lococcus aureus in a UK hospital. J Antimicrob Chemother 2001; 47:399-403.
  • Howden BP, Davies JK, Johnson PDR, Stinear TP, Grayson ML. Reduced vancomycin susceptibility in Staphylococcus aureus, including vancomycin-intermediate and heteroge- neous vancomycin-intermediate strains: resistance mecha- nisms, laboratory detection and clinical implications. Clin Mi- crobiol Rev 2010; 23:99-139.
  • Moise PA, Smyth DS, Robinson DA, El-Fawal N, McCalla C, Sakoulas G. Genotypic and phenotypic relationships among methicillin-resistant Staphylococcus aureus from three mul- ticenter bacteremia studies. J Antimicrob Chemother 2009; 63:873-876.
  • Bozdogan B, Ednie L, Credito K, Kosowaska K, Appelbaum PC. Derivative of a vancomycin-resistant Staphylococcus aureus strain isolated at Hershey Medical Center. Antimicrob Agent Chemother 2004; 48:4762-4765.

An optimal method for generating stable vancomycin heteroresistance and intermediate susceptibility in methicillin-resistant Staphylococcus aureus blood isolates under in-vitro vancomycin pressure

Year 2012, Volume: 2 Issue: 04, 129 - 134, 01.12.2012
https://doi.org/10.5799/jmid.123125

Abstract

References

  • Bae IG, Federspiel JJ, Miró JM, et al. Heterogeneous vanco- mycin-intermediate susceptibility phenotype in bloodstream methicillin-resistant Staphylococcus aureus isolates from an international cohort of patients with infective endocarditis: prevalence, genotype and clinical significance. J Infect Dis 2009; 200:1355-1366.
  • Fridkin SK, Hageman J, McDougal KL, et al. Vancomycin-Inter- mediate Staphylococcus aureus Epidemiology Study Group. Epidemiological and microbiological characterization of infec- tion caused by Staphylococcus aureus with reduced suscep- tibility to vancomycin, United States, 1997-2001. Clin Infect Dis 2003; 36:429-439.
  • Khatib R, Jose J, Musta AC, et al. The relevance of vanco- mycin-intermediate susceptibility and heteroresistance in methicillin-resistant Staphylococcus aureus bacteremia. J Antimicrob Chem 2011; 66:1594-1599.
  • Kosowaska-shick K, Ednie LM, McGhee P, et al. Incidence and characteristics of vancomycin nonsusceptible strains of methicillin-resistant Staphylococcus aureus at Hershey medi- cal center. Antimicrob Agent Chemother 2008; 52:4510-4513.
  • Musta AC, Riederer K, Shemes S, et al. Vancomycin MIC plus heteroresistance and the outcome of methicillin-resistant Staphylococcus aureus bacteremia: trends over 11 years. J Clin Microbiol 2009; 47:1640-1644.
  • Riederer K, Shemes S, Chase P, Musta AC, Mar A, Khatib R. Detection of intermediately vancomycin-susceptible and het- erogeneous Staphylococcus aureus isolates: comparison of Etest and agar screening methods. J Clin Microbiol 2011; 49:2147-2150.
  • Rybak MJ, Leonard SN, Rossi KL, Cheung CM, Sadar HS, Jones RN. Characterization of vancomycin-heteroresistant Staphylococcus aureus from the Metropolitan Area of Detroit, Michigan, over a 22-year period (1986-2007). J Clin Microbiol 2008; 46:2950-2954.
  • Sieradzki K, Leski T, Dick J, Borio L, Tomasz A. 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.
  • Howden BP, Ward PB, Robson J, Morris AJ, Mayall BC, Gray- son ML. Treatment outcomes for serious infections caused by methicillin-resistant Staphylococcus aureus with reduced vancomycin susceptibility. Clin Infect Dis 2004; 38:521-528.
  • Fong RK, Low J, Koh TH, Kurup A. Clinical features and treat- ment outcomes of vancomycin-intermediate Staphylococcus aureus (VISA) and heteroresistant vancomycin-intermediate Staphylococcus aureus (hVISA) in a tertiary care institution in Singapore. Eur J Clin Microbiol Infect Dis 2009; 28:983-987.
  • Moise PA, Forrest A, Bayer AS, Xiong YQ, Yeaman MR, Sakoulas G. Factors influencing time to vancomycin-induced clearance of non-endocarditis methicillin-resistant Staphylo- coccus aureus bacteremia: role of platelet microbial protein killing and agr genotypes. J Infect Dis 2010; 201:233-240.
  • Sakoulas G, Gold HS, Cohen RA, Venkataraman L, Moel- lering RC, Eliopoulos GM. Effects of prolonged vancomycin administration on methicillin-resistant Staphylococcus aureus (MRSA) in a patient with recurrent bacteremia. J Antimicrob Chemother 2006; 57:699-704.
  • Song JH. Emergence of Staphylococcus aureus with reduced susceptibility to vancomycin in Asia. In: LU Yichen, eds. Emerging Infections in Asia. New York: Springer, 2008; 233- 242.
  • Moise PA, Smyth DS, El-Fawal N, et al. Microbiological effects of prior vancomycin use in patients with methicillin-resistant Staphylococcus aureus bacteraemia. J Antimicrob Chemoth- er 2008; 61:85-90.
  • Vaudaux P, Francois P, Berger-Bachi B, Lew DP. In vivo emer- gence of subpopulations expressing teicoplanin or vanco- mycin resistance phenotypes in a glycopeptide-susceptible, methicillin-resistant strain of Staphylococcus aureus. J Anti- microb Chemother 2001; 47:163-170.
  • Chui L, Ma X, Sato K, et al. Cell wall thickening is a common feature of vancomycin resistance in Staphylococcus aureus. J Clin Microbiol 2003; 41:5-14.
  • Sakoulas G, Eliopoulos GM, Moellering RC Jr, et al. Staphy- lococcus aureus accessory gene regulator (agr) group II: is there a relationship to the development of intermediate-level glycopeptide resistance? J Infect Dis 2003; 187:929-938.
  • Hanaki H, Kuwahara-Arai K, Boyle-Varva S, Daum RS, La- bischinski H, Hiramatsu K. Activated cell-wall synthesis is as- sociated with vancomycin resistant Staphylococcus aureus clinical strains Mu3 and Mu50. J Antimicrob Chemother 1998; 42:199-209.
  • Cameron DR, Ward DV, Kostoulias X et al. Serine/threonine phosphatase Stp1 contributes to reduced susceptibility to vancomycin and virulence in Staphylococcus aureus. J Infect Dis 2012; 205:1677-1687.
  • Howden BP, Davies JK, Johnsosn PDR, Stinear TP, Grayson ML. Reduced vancomycin susceptibility in Staphylococcus aureus, including vancomycin-intermediate and heteroge- neous vancomycin-intermediate strains: resistance mecha- nisms, laboratory detection, and clinical implications. Clin Microbiol Rev 2010; 23: 99-139.
  • Rose WE, Leonard SN, Rossi KL, Kaatz GW, Rybak MJ. Im- pact of inoculum size and heterogeneous vancomycin-inter- mediate Staphylococcus aureus (hVISA) on vancomycin ac- tivity and emergence of VISA in an in-vitro pharmacodynamic model. Antimicrob Agents Chemother 2009; 53:805-807.
  • Plipat N, Livni G, Bertram H, Thompson RB Jr. Unstable van- comycin heteroresistance is common among clinical isolates of methicillin-resistant Staphylococcus aureus. J Clin Micro- biol 2005; 43:2494-2496.
  • Wong SSY, Ho PL, Woo PCY, Yuen KY. Bacteremia caused by staphylococci with inducible vancomycin resistance. Clin Infect Dis 1999; 29:760-767.
  • Daum RS, Gupta S, Sabbagh R, Milewski WM. Characteriza- tion of Staphylococcus aureus isolates with decreased sus- ceptibility to vancomycin and teicoplanin: isolation and puri- fication of a constitutively produced protein associated with susceptibility. J Infect Dis 1992; 166:1066-1072.
  • Pfeltz RF, Singh VK, Schmidt JL, et al. Characterization of passage-selected vancomycin-resistant Staphylococcus aureus strains of diverse parental backgrounds. Antimicrob Agents Chemother 2000; 44:294-303.
  • Zafar U, Johnson LB, Hanna M, et al. Prevalence of nasal colonization among patients with community-associated methicillin-resistant Staphylococcus aureus infection and their household contacts. Infect Control Hosp Epidemiol 2007; 28:966-969.
  • Wootton M, Howe RA, Hillman R, Walsh TR, Bennett PM, MacGowan AP. A modified population analysis profile (PAP) method to detect hetero-resistance to vancomycin in Staphy- lococcus aureus in a UK hospital. J Antimicrob Chemother 2001; 47:399-403.
  • Howden BP, Davies JK, Johnson PDR, Stinear TP, Grayson ML. Reduced vancomycin susceptibility in Staphylococcus aureus, including vancomycin-intermediate and heteroge- neous vancomycin-intermediate strains: resistance mecha- nisms, laboratory detection and clinical implications. Clin Mi- crobiol Rev 2010; 23:99-139.
  • Moise PA, Smyth DS, Robinson DA, El-Fawal N, McCalla C, Sakoulas G. Genotypic and phenotypic relationships among methicillin-resistant Staphylococcus aureus from three mul- ticenter bacteremia studies. J Antimicrob Chemother 2009; 63:873-876.
  • Bozdogan B, Ednie L, Credito K, Kosowaska K, Appelbaum PC. Derivative of a vancomycin-resistant Staphylococcus aureus strain isolated at Hershey Medical Center. Antimicrob Agent Chemother 2004; 48:4762-4765.
There are 30 citations in total.

Details

Primary Language English
Subjects Health Care Administration
Journal Section ART
Authors

Riad Khatib This is me

Jinson Jose This is me

Leonard B Johnson This is me

Kathleen Riederer This is me

Stephen Shemes This is me

Publication Date December 1, 2012
Published in Issue Year 2012 Volume: 2 Issue: 04

Cite

APA Khatib, R., Jose, J., Johnson, L. B., Riederer, K., et al. (2012). An optimal method for generating stable vancomycin heteroresistance and intermediate susceptibility in methicillin-resistant Staphylococcus aureus blood isolates under in-vitro vancomycin pressure. Journal of Microbiology and Infectious Diseases, 2(04), 129-134. https://doi.org/10.5799/jmid.123125
AMA Khatib R, Jose J, Johnson LB, Riederer K, Shemes S. An optimal method for generating stable vancomycin heteroresistance and intermediate susceptibility in methicillin-resistant Staphylococcus aureus blood isolates under in-vitro vancomycin pressure. J Microbil Infect Dis. December 2012;2(04):129-134. doi:10.5799/jmid.123125
Chicago Khatib, Riad, Jinson Jose, Leonard B Johnson, Kathleen Riederer, and Stephen Shemes. “An Optimal Method for Generating Stable Vancomycin Heteroresistance and Intermediate Susceptibility in Methicillin-Resistant Staphylococcus Aureus Blood Isolates under in-Vitro Vancomycin Pressure”. Journal of Microbiology and Infectious Diseases 2, no. 04 (December 2012): 129-34. https://doi.org/10.5799/jmid.123125.
EndNote Khatib R, Jose J, Johnson LB, Riederer K, Shemes S (December 1, 2012) An optimal method for generating stable vancomycin heteroresistance and intermediate susceptibility in methicillin-resistant Staphylococcus aureus blood isolates under in-vitro vancomycin pressure. Journal of Microbiology and Infectious Diseases 2 04 129–134.
IEEE R. Khatib, J. Jose, L. B. Johnson, K. Riederer, and S. Shemes, “An optimal method for generating stable vancomycin heteroresistance and intermediate susceptibility in methicillin-resistant Staphylococcus aureus blood isolates under in-vitro vancomycin pressure”, J Microbil Infect Dis, vol. 2, no. 04, pp. 129–134, 2012, doi: 10.5799/jmid.123125.
ISNAD Khatib, Riad et al. “An Optimal Method for Generating Stable Vancomycin Heteroresistance and Intermediate Susceptibility in Methicillin-Resistant Staphylococcus Aureus Blood Isolates under in-Vitro Vancomycin Pressure”. Journal of Microbiology and Infectious Diseases 2/04 (December 2012), 129-134. https://doi.org/10.5799/jmid.123125.
JAMA Khatib R, Jose J, Johnson LB, Riederer K, Shemes S. An optimal method for generating stable vancomycin heteroresistance and intermediate susceptibility in methicillin-resistant Staphylococcus aureus blood isolates under in-vitro vancomycin pressure. J Microbil Infect Dis. 2012;2:129–134.
MLA Khatib, Riad et al. “An Optimal Method for Generating Stable Vancomycin Heteroresistance and Intermediate Susceptibility in Methicillin-Resistant Staphylococcus Aureus Blood Isolates under in-Vitro Vancomycin Pressure”. Journal of Microbiology and Infectious Diseases, vol. 2, no. 04, 2012, pp. 129-34, doi:10.5799/jmid.123125.
Vancouver Khatib R, Jose J, Johnson LB, Riederer K, Shemes S. An optimal method for generating stable vancomycin heteroresistance and intermediate susceptibility in methicillin-resistant Staphylococcus aureus blood isolates under in-vitro vancomycin pressure. J Microbil Infect Dis. 2012;2(04):129-34.