Skip to main content
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Resource Announcements
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems
  • Log in
  • My alerts
  • My Cart

Main menu

  • Home
  • Articles
    • Current Issue
    • Accepted Manuscripts
    • COVID-19 Special Collection
    • Archive
    • Minireviews
  • For Authors
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Abbreviations and Conventions
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About AAC
    • Editor in Chief
    • Editorial Board
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • AAC Podcast
    • RSS
    • FAQ
  • Subscribe
    • Members
    • Institutions
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Resource Announcements
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems

User menu

  • Log in
  • My alerts
  • My Cart

Search

  • Advanced search
Antimicrobial Agents and Chemotherapy
publisher-logosite-logo

Advanced Search

  • Home
  • Articles
    • Current Issue
    • Accepted Manuscripts
    • COVID-19 Special Collection
    • Archive
    • Minireviews
  • For Authors
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Abbreviations and Conventions
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About AAC
    • Editor in Chief
    • Editorial Board
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • AAC Podcast
    • RSS
    • FAQ
  • Subscribe
    • Members
    • Institutions
Clinical Therapeutics

Systematic Review and Meta-Analysis of the Significance of Heterogeneous Vancomycin-Intermediate Staphylococcus aureus Isolates

Sebastiaan J. van Hal, David L. Paterson
Sebastiaan J. van Hal
1Department of Microbiology and Infectious Diseases, Liverpool Hospital, Liverpool BC, NSW 1087, Sydney, Australia
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: Sebastian.vanHal@sswahs.nsw.gov.au
David L. Paterson
2University of Queensland Centre for Clinical Research, Royal Brisbane and Women's Hospital Campus, Herston, QLD 4029, Australia
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
DOI: 10.1128/AAC.01133-10
  • Article
  • Figures & Data
  • Info & Metrics
  • PDF
Loading

ABSTRACT

The prevalence of heteroresistant vancomycin-intermediate Staphylococcus aureus (hVISA) is 1.3% in published studies. Clinical associations include high-inoculum infections and glycopeptide failure, with hVISA infections associated with a 2.37-times-greater failure rate (95% confidence interval [CI], 1.53 to 3.67) compared to vancomycin-sensitive Staphylococcus aureus (VSSA) infections. Despite this, 30-day mortality rates were similar to those for VSSA infections (odds ratio [OR], 1.18; 95% CI, 0.81 to 1.74). The optimal therapy for hVISA requires further study.

In the presence of selection pressure, vancomycin-susceptible Staphylococcus aureus (VSSA) isolates are able to transform their cell wall and become less susceptible to vancomycin (51). These vancomycin-intermediate S. aureus (VISA) isolates are defined by a vancomycin broth microdilution MIC of 4 to 8 μg/ml (57) and may progress through a precursor phenotype known as heteroresistant vancomycin-intermediate Staphylococcus aureus (hVISA) (11). Although the precise definition is disputed, heteroresistance refers to the presence of a resistant subpopulation (typically at a frequency of ≤10−5 to 10−6 CFU) in a fully susceptible isolate (a broth microdilution MIC of ≤2 μg/ml).

Detection.

hVISA detection is problematic, as commercial susceptibility platforms use inocula lower than the required threshold. As a consequence, multiple screening and detection methods using higher inocula and growth promotion of resistant subpopulations have been developed. Controversy remains, as some of these methods may select for resistant subpopulations in vitro rather than detect the in vivo presence of heteroresistance (60). The most accurate and reproducible method is the modified population analysis profile (PAP)-area under the curve (AUC), which utilizes the plot of the number of viable colonies against vancomycin concentration. An AUC ratio of the test strain to the reference strain (Mu3) of ≥0.9 confirms an hVISA isolate. However, PAP-AUC use is limited as it is expensive and labor- and time-intensive.

Epidemiology.

Following the first documented VISA (Mu50) and hVISA (Mu3) strains from Japan (22, 23), both phenotypes have been reported worldwide. The precise burden of hVISA is difficult to determine given the range of testing methodologies, definitions, and changes in vancomycin susceptibility breakpoints in 2006. This may explain the marked variation in hVISA prevalences detected across institutions, geographical regions, and patient populations, with surveillance studies generally confirming lower hVISA rates than those for selected clinical isolates. Nevertheless, the overall hVISA prevalence remains low at approximately 1.3% of all methicillin-resistant S. aureus (MRSA) isolates tested (Table 1) (1-6, 8, 9, 12-16, 18-20, 22, 24, 29-39, 41-47, 49, 50, 52, 55, 56, 58, 61).

View this table:
  • View inline
  • View popup
TABLE 1.

Prevalence of hVISA based on method of screening/detection, origin of study, and isolate selection

Clinical significance of hVISA.

All English-language studies containing the term S. aureus and any of the terms reduced susceptibility, intermediate susceptibility, and heteroresistance or heteroresistant to vancomycin or glycopeptides were identified through Medline (2006 to 2010) and reviewed. All articles with clinical details are summarized in Table 2 (2, 4, 5, 8, 16, 24, 28, 31, 33, 37, 38, 41). Considerable heterogeneity exists between studies due to the differing patient populations studied, testing methodologies used, and MRSA isolates selected (i.e., initial blood culture compared to final isolate). Despite this, high-inoculum infections (such as infective endocarditis, osteomyelitis, deep abscesses, and prosthetic device infections) (8, 16, 37) and vancomycin treatment failure (defined as persistent infection or bacteremia duration and/or ongoing signs of infection) (2, 4, 8, 16, 42) were common associations with hVISA infection. After the available data were pooled, the odds of glycopeptide failure were 2.37 times greater for hVISA than for VSSA infections (odds ratio [OR], 2.37; 95% confidence interval [CI], 1.53 to 3.67) (Fig. 1). Since high-inoculum infections are independently associated with bacteremic persistence (therapeutic failure) (10, 17, 31) and de novo hVISA infections do not always result in treatment failure, hVISA may reflect the consequence rather than the cause of treatment failure.

FIG. 1.
  • Open in new tab
  • Download powerpoint
FIG. 1.

Forest plot (using Mantel-Haenszel analysis) of events denoting vancomycin (VAN) treatment failure (with all definitions regarded the same) in hVISA- compared to VSSA-infected patients. Squares indicate point estimates, and the size of the square indicates the weight of each study. *, data obtained by personal communication.

View this table:
  • View inline
  • View popup
TABLE 2.

Published studies containing clinical details of hVISA-infected patients

Intuitively, persistent bacteremia should result in greater morbidity. However, compared to VSSA infections, hVISA persistence does not lead to more metastatic complications (41). Other parameters of morbidity have not been extensively examined. A significant increase in the mean hospital stay in patients with hVISA infection has been documented in one study (16). Similarly, infection-related complications are generally not reported (secondary to the heterogeneity of the principal diagnosis) except for one study where hVISA infective endocarditis patients were more likely to develop congestive cardiac failure (4).

Significance of MIC in hVISA.

The proportion of hVISA detected is directly related to increases in vancomycin MIC with the majority (>80%) of hVISA isolates demonstrating an Etest MIC of ≥2 μg/ml (41). Although a detailed discussion of the clinical significance of higher MICs is beyond the scope of this review, several studies have documented greater mortality associated with higher-MIC-susceptible MRSA isolates (generally between 1.5 and 2 μg/ml) (21, 53). Only one study has examined both variables (vancomycin MIC and heteroresistance phenotype) in the same isolates, with neither variable predictive of overall mortality on multivariate analysis (41). Thus, the relative contribution of heteroresistance to MIC-related outcomes remains unclear and requires further study.

Mortality and hVISA.

Since hVISA is associated with parameters known to influence mortality (i.e., high-inoculum infections, persistent bacteremia, and high vancomycin MICs), one would expect an increased mortality compared to that of VSSA infections (Table 2). However, no study to date has had the power to detect such a difference. After all available data from comparative studies were pooled, hVISA was associated with a 30-day mortality rate similar to that of VSSA infections (OR, 1.18; 95% CI, 0.81 to 1.74) (Fig. 2). These findings can in part be explained by the reduced virulence and decreased host immune responses demonstrated in animal infection models and laboratory studies with hVISA infections (27, 40). A clinical study indirectly supports this link, with hVISA significantly more likely to be associated with colonization rather than infection (24).

FIG. 2.
  • Open in new tab
  • Download powerpoint
FIG. 2.

Forest plot (using Mantel-Haenszel analysis) of 30-day mortality in hVISA- compared to VSSA-infected patients with “events” denoting deaths in each group. Squares indicate point estimates, and the size of the square indicates the weight of each study.

Conclusion and therapeutic implications.

The role of vancomycin in the treatment of hVISA remains unclear, as heteroresistance may emerge during glycopeptide therapy, especially in infections associated with poor antibiotic penetration (infective endocarditis and osteomyelitis) (8). Despite these deficiencies, no new antibiotic has been documented to be superior to vancomycin (17). Alternative agents have been used successfully in numerous case reports (25). However, potential concerns remain when prescribing these agents. These include toxicity with prolonged linezolid use (7), possible cross-resistance with lipoglycopeptides (54), and the clinical relevance of emerging low-level daptomycin nonsusceptibility during treatment of hVISA infections (48). An important adjunct to antimicrobial therapy and a key component of success is surgical debridement for high-inoculum hVISA infections (26). Irrespective of treatment choice, MRSA bacteremia mortality remains high (59). Therefore, further research should be aimed at developing new agents and defining the optimal pharmacodynamic parameters of current antibiotics, including vancomycin, in targeting specific clinical contexts.

FOOTNOTES

    • Received 16 August 2010.
    • Returned for modification 21 October 2010.
    • Accepted 2 November 2010.
    • Accepted manuscript posted online 15 November 2010.
  • Copyright © 2011, American Society for Microbiology. All Rights Reserved.

REFERENCES

  1. 1.↵
    Adam, H. J., L. Louie, C. Watt, D. Gravel, E. Bryce, M. Loeb, A. Matlow, A. McGeer, M. R. Mulvey, and A. E. Simor. 2010. Detection and characterization of heterogeneous vancomycin-intermediate Staphylococcus aureus isolates in Canada: results from the Canadian Nosocomial Infection Surveillance Program, 1995-2006. Antimicrob. Agents Chemother. 54:945-949.
    OpenUrlAbstract/FREE Full Text
  2. 2.↵
    Ariza, J., M. Pujol, J. Cabo, C. Pena, N. Fernandez, J. Linares, J. Ayats, and F. Gudiol. 1999. Vancomycin in surgical infections due to methicillin-resistant Staphylococcus aureus with heterogeneous resistance to vancomycin. Lancet 353:1587-1588.
    OpenUrlCrossRefPubMedWeb of Science
  3. 3.
    Aucken, H. M., M. Warner, M. Ganner, A. P. Johnson, J. F. Richardson, B. D. Cookson, and D. M. Livermore. 2000. Twenty months of screening for glycopeptide-intermediate Staphylococcus aureus. J. Antimicrob. Chemother. 46:639-640.
    OpenUrlCrossRefPubMedWeb of Science
  4. 4.↵
    Bae, I. G., J. J. Federspiel, J. M. Miro, C. W. Woods, L. Park, M. J. Rybak, T. H. Rude, S. Bradley, S. Bukovski, C. G. de la Maria, S. S. Kanj, T. M. Korman, F. Marco, D. R. Murdoch, P. Plesiat, M. Rodriguez-Creixems, P. Reinbott, L. Steed, P. Tattevin, M. F. Tripodi, K. L. Newton, G. R. Corey, and V. G. Fowler, Jr. 2009. Heterogeneous vancomycin-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. 200:1355-1366.
    OpenUrlCrossRefPubMedWeb of Science
  5. 5.↵
    Bert, F., J. Clarissou, F. Durand, D. Delefosse, C. Chauvet, P. Lefebvre, N. Lambert, and C. Branger. 2003. Prevalence, molecular epidemiology, and clinical significance of heterogeneous glycopeptide-intermediate Staphylococcus aureus in liver transplant recipients. J. Clin. Microbiol. 41:5147-5152.
    OpenUrlAbstract/FREE Full Text
  6. 6.↵
    Bierbaum, G., K. Fuchs, W. Lenz, C. Szekat, and H. G. Sahl. 1999. Presence of Staphylococcus aureus with reduced susceptibility to vancomycin in Germany. Eur. J. Clin. Microbiol. Infect. Dis. 18:691-696.
    OpenUrlCrossRefPubMedWeb of Science
  7. 7.↵
    Bishop, E., S. Melvani, B. P. Howden, P. G. Charles, and M. L. Grayson. 2006. Good clinical outcomes but high rates of adverse reactions during linezolid therapy for serious infections: a proposed protocol for monitoring therapy in complex patients. Antimicrob. Agents Chemother. 50:1599-1602.
    OpenUrlAbstract/FREE Full Text
  8. 8.↵
    Charles, P. G., P. B. Ward, P. D. Johnson, B. P. Howden, and M. L. Grayson. 2004. Clinical features associated with bacteremia due to heterogeneous vancomycin-intermediate Staphylococcus aureus. Clin. Infect. Dis. 38:448-451.
    OpenUrlCrossRefPubMedWeb of Science
  9. 9.↵
    Chung, G., J. Cha, S. Han, H. Jang, K. Lee, J. Yoo, H. Kim, S. Eun, B. Kim, O. Park, and Y. Lee. 2010. Nationwide surveillance study of vancomycin intermediate Staphylococcus aureus strains in Korean hospitals from 2001 to 2006. J. Microbiol. Biotechnol. 20:637-642.
    OpenUrlPubMed
  10. 10.↵
    Cremieux, A. C., B. Maziere, J. M. Vallois, M. Ottaviani, A. Azancot, H. Raffoul, A. Bouvet, J. J. Pocidalo, and C. Carbon. 1989. Evaluation of antibiotic diffusion into cardiac vegetations by quantitative autoradiography. J. Infect. Dis. 159:938-944.
    OpenUrlCrossRefPubMedWeb of Science
  11. 11.↵
    Cui, L., X. Ma, K. Sato, K. Okuma, F. C. Tenover, E. M. Mamizuka, C. G. Gemmell, M. N. Kim, M. C. Ploy, N. El-Solh, V. Ferraz, and K. Hiramatsu. 2003. Cell wall thickening is a common feature of vancomycin resistance in Staphylococcus aureus. J. Clin. Microbiol. 41:5-14.
    OpenUrlAbstract/FREE Full Text
  12. 12.↵
    Delgado, A., J. T. Riordan, R. Lamichhane-Khadka, D. C. Winnett, J. Jimenez, K. Robinson, F. G. O'Brien, S. A. Cantore, and J. E. Gustafson. 2007. Hetero-vancomycin-intermediate methicillin-resistant Staphylococcus aureus isolate from a medical center in Las Cruces, New Mexico. J. Clin. Microbiol. 45:1325-1329.
    OpenUrlAbstract/FREE Full Text
  13. 13.
    Denis, O., C. Nonhoff, B. Byl, C. Knoop, S. Bobin-Dubreux, and M. J. Struelens. 2002. Emergence of vancomycin-intermediate Staphylococcus aureus in a Belgian hospital: microbiological and clinical features. J. Antimicrob. Chemother. 50:383-391.
    OpenUrlCrossRefPubMedWeb of Science
  14. 14.
    Eguia, J. M., C. Liu, M. Moore, E. M. Wrone, J. Pont, J. L. Gerberding, and H. F. Chambers. 2005. Low colonization prevalence of Staphylococcus aureus with reduced vancomycin susceptibility among patients undergoing hemodialysis in the San Francisco Bay area. Clin. Infect. Dis. 40:1617-1624.
    OpenUrlCrossRefPubMedWeb of Science
  15. 15.
    Fitzgibbon, M. M., A. S. Rossney, and B. O'Connell. 2007. Investigation of reduced susceptibility to glycopeptides among methicillin-resistant Staphylococcus aureus isolates from patients in Ireland and evaluation of agar screening methods for detection of heterogeneously glycopeptide-intermediate S. aureus. J. Clin. Microbiol. 45:3263-3269.
    OpenUrlAbstract/FREE Full Text
  16. 16.↵
    Fong, R. K., J. Low, T. H. Koh, and A. Kurup. 2009. Clinical features and treatment 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. 28:983-987.
    OpenUrlCrossRefPubMedWeb of Science
  17. 17.↵
    Fowler, V. G., Jr., H. W. Boucher, G. R. Corey, E. Abrutyn, A. W. Karchmer, M. E. Rupp, D. P. Levine, H. F. Chambers, F. P. Tally, G. A. Vigliani, C. H. Cabell, A. S. Link, I. DeMeyer, S. G. Filler, M. Zervos, P. Cook, J. Parsonnet, J. M. Bernstein, C. S. Price, G. N. Forrest, G. Fatkenheuer, M. Gareca, S. J. Rehm, H. R. Brodt, A. Tice, and S. E. Cosgrove. 2006. Daptomycin versus standard therapy for bacteremia and endocarditis caused by Staphylococcus aureus. N. Engl. J. Med. 355:653-665.
    OpenUrlCrossRefPubMedWeb of Science
  18. 18.↵
    Franchi, D., M. W. Climo, A. H. Wong, M. B. Edmond, and R. P. Wenzel. 1999. Seeking vancomycin resistant Staphylococcus aureus among patients with vancomycin-resistant enterococci. Clin. Infect. Dis. 29:1566-1568.
    OpenUrlCrossRefPubMedWeb of Science
  19. 19.
    Garnier, F., D. Chainier, T. Walsh, A. Karlsson, A. Bolmstrom, C. Grelaud, M. Mounier, F. Denis, and M. C. Ploy. 2006. A 1 year surveillance study of glycopeptide-intermediate Staphylococcus aureus strains in a French hospital. J. Antimicrob. Chemother. 57:146-149.
    OpenUrlCrossRefPubMedWeb of Science
  20. 20.↵
    Geisel, R., F. J. Schmitz, L. Thomas, G. Berns, O. Zetsche, B. Ulrich, A. C. Fluit, H. Labischinsky, and W. Witte. 1999. Emergence of heterogeneous intermediate vancomycin resistance in Staphylococcus aureus isolates in the Dusseldorf area. J. Antimicrob. Chemother. 43:846-848.
    OpenUrlCrossRefPubMedWeb of Science
  21. 21.↵
    Hidayat, L. K., D. I. Hsu, R. Quist, K. A. Shriner, and A. Wong-Beringer. 2006. High-dose vancomycin therapy for methicillin-resistant Staphylococcus aureus infections: efficacy and toxicity. Arch. Intern. Med. 166:2138-2144.
    OpenUrlCrossRefPubMedWeb of Science
  22. 22.↵
    Hiramatsu, K., N. Aritaka, H. Hanaki, S. Kawasaki, Y. Hosoda, S. Hori, Y. Fukuchi, and I. Kobayashi. 1997. Dissemination in Japanese hospitals of strains of Staphylococcus aureus heterogeneously resistant to vancomycin. Lancet 350:1670-1673.
    OpenUrlCrossRefPubMedWeb of Science
  23. 23.↵
    Hiramatsu, K., H. Hanaki, T. Ino, K. Yabuta, T. Oguri, and F. C. Tenover. 1997. Methicillin-resistant Staphylococcus aureus clinical strain with reduced vancomycin susceptibility. J. Antimicrob. Chemother. 40:135-136.
    OpenUrlCrossRefPubMedWeb of Science
  24. 24.↵
    Horne, K. C., B. P. Howden, E. A. Grabsch, M. Graham, P. B. Ward, S. Xie, B. C. Mayall, P. D. Johnson, and M. L. Grayson. 2009. Prospective comparison of the clinical impacts of heterogeneous vancomycin-intermediate methicillin-resistant Staphylococcus aureus (MRSA) and vancomycin-susceptible MRSA. Antimicrob. Agents Chemother. 53:3447-3452.
    OpenUrlAbstract/FREE Full Text
  25. 25.↵
    Howden, B. P., J. K. Davies, P. D. Johnson, T. P. Stinear, and M. L. Grayson. 2010. Reduced vancomycin susceptibility in Staphylococcus aureus, including vancomycin-intermediate and heterogeneous vancomycin-intermediate strains: resistance mechanisms, laboratory detection, and clinical implications. Clin. Microbiol. Rev. 23:99-139.
    OpenUrlAbstract/FREE Full Text
  26. 26.↵
    Howden, B. P., P. D. Johnson, P. G. Charles, and M. L. Grayson. 2004. Failure of vancomycin for treatment of methicillin-resistant Staphylococcus aureus infections. Clin. Infect. Dis. 39:1544.
    OpenUrlCrossRefPubMedWeb of Science
  27. 27.↵
    Howden, B. P., D. J. Smith, A. Mansell, P. D. Johnson, P. B. Ward, T. P. Stinear, and J. K. Davies. 2008. 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. 8:39.
    OpenUrlCrossRefPubMed
  28. 28.↵
    Howden, B. P., P. B. Ward, P. G. Charles, T. M. Korman, A. Fuller, P. du Cros, E. A. Grabsch, S. A. Roberts, J. Robson, K. Read, N. Bak, J. Hurley, P. D. Johnson, A. J. Morris, B. C. Mayall, and M. L. Grayson. 2004. Treatment outcomes for serious infections caused by methicillin-resistant Staphylococcus aureus with reduced vancomycin susceptibility. Clin. Infect. Dis. 38:521-528.
    OpenUrlCrossRefPubMedWeb of Science
  29. 29.↵
    Ike, Y., Y. Arakawa, X. Ma, K. Tatewaki, M. Nagasawa, H. Tomita, K. Tanimoto, and S. Fujimoto. 2001. Nationwide survey shows that methicillin-resistant Staphylococcus aureus strains heterogeneously and intermediately resistant to vancomycin are not disseminated throughout Japanese hospitals. J. Clin. Microbiol. 39:4445-4451.
    OpenUrlAbstract/FREE Full Text
  30. 30.
    Kantzanou, M., P. T. Tassios, A. Tseleni-Kotsovili, N. J. Legakis, and A. C. Vatopoulos. 1999. Reduced susceptibility to vancomycin of nosocomial isolates of methicillin-resistant Staphylococcus aureus. J. Antimicrob. Chemother. 43:729-731.
    OpenUrlCrossRefPubMedWeb of Science
  31. 31.↵
    Khosrovaneh, A., K. Riederer, S. Saeed, M. S. Tabriz, A. R. Shah, M. M. Hanna, M. Sharma, L. B. Johnson, M. G. Fakih, and R. Khatib. 2004. Frequency of reduced vancomycin susceptibility and heterogeneous subpopulation in persistent or recurrent methicillin-resistant Staphylococcus aureus bacteremia. Clin. Infect. Dis. 38:1328-1330.
    OpenUrlCrossRefPubMedWeb of Science
  32. 32.
    Kim, H. B., W. B. Park, K. D. Lee, Y. J. Choi, S. W. Park, M. D. Oh, E. C. Kim, and K. W. Choe. 2003. Nationwide surveillance for Staphylococcus aureus with reduced susceptibility to vancomycin in Korea. J. Clin. Microbiol. 41:2279-2281.
    OpenUrlAbstract/FREE Full Text
  33. 33.↵
    Kim, M. N., S. H. Hwang, Y. J. Pyo, H. M. Mun, and C. H. Pai. 2002. Clonal spread of Staphylococcus aureus heterogeneously resistant to vancomycin in a university hospital in Korea. J. Clin. Microbiol. 40:1376-1380.
    OpenUrlAbstract/FREE Full Text
  34. 34.
    Kirby, A., R. Graham, N. J. Williams, M. Wootton, C. M. Broughton, M. Alanazi, J. Anson, T. J. Neal, and C. M. Parry. 2010. Staphylococcus aureus with reduced glycopeptide susceptibility in Liverpool, UK. J. Antimicrob. Chemother. 65:721-724.
    OpenUrlCrossRefPubMedWeb of Science
  35. 35.
    Kosowska-Shick, K., L. M. Ednie, P. McGhee, K. Smith, C. D. Todd, A. Wehler, and P. C. Appelbaum. 2008. Incidence and characteristics of vancomycin nonsusceptible strains of methicillin-resistant Staphylococcus aureus at Hershey Medical Center. Antimicrob. Agents Chemother. 52:4510-4513.
    OpenUrlAbstract/FREE Full Text
  36. 36.
    Lulitanond, A., C. Engchanil, P. Chaimanee, M. Vorachit, T. Ito, and K. Hiramatsu. 2009. The first vancomycin-intermediate Staphylococcus aureus strains isolated from patients in Thailand. J. Clin. Microbiol. 47:2311-2316.
    OpenUrlAbstract/FREE Full Text
  37. 37.↵
    Maor, Y., M. Hagin, N. Belausov, N. Keller, D. Ben-David, and G. Rahav. 2009. Clinical features of heteroresistant vancomycin-intermediate Staphylococcus aureus bacteremia versus those of methicillin-resistant S. aureus bacteremia. J. Infect. Dis. 199:619-624.
    OpenUrlCrossRefPubMedWeb of Science
  38. 38.↵
    Maor, Y., G. Rahav, N. Belausov, D. Ben-David, G. Smollan, and N. Keller. 2007. Prevalence and characteristics of heteroresistant vancomycin-intermediate Staphylococcus aureus bacteremia in a tertiary care center. J. Clin. Microbiol. 45:1511-1514.
    OpenUrlAbstract/FREE Full Text
  39. 39.↵
    Marchese, A., G. Balistreri, E. Tonoli, E. A. Debbia, and G. C. Schito. 2000. Heterogeneous vancomycin resistance in methicillin-resistant Staphylococcus aureus strains isolated in a large Italian hospital. J. Clin. Microbiol. 38:866-869.
    OpenUrlAbstract/FREE Full Text
  40. 40.↵
    McCallum, N., H. Karauzum, R. Getzmann, M. Bischoff, P. Majcherczyk, B. Berger-Bachi, and R. Landmann. 2006. In vivo survival of teicoplanin-resistant Staphylococcus aureus and fitness cost of teicoplanin resistance. Antimicrob. Agents Chemother. 50:2352-2360.
    OpenUrlAbstract/FREE Full Text
  41. 41.↵
    Musta, A. C., K. Riederer, S. Shemes, P. Chase, J. Jose, L. B. Johnson, and R. Khatib. 2009. Vancomycin MIC plus heteroresistance and outcome of methicillin-resistant Staphylococcus aureus bacteremia: trends over 11 years. J. Clin. Microbiol. 47:1640-1644.
    OpenUrlAbstract/FREE Full Text
  42. 42.↵
    Neoh, H. M., S. Hori, M. Komatsu, T. Oguri, F. Takeuchi, L. Cui, and K. Hiramatsu. 2007. Impact of reduced vancomycin susceptibility on the therapeutic outcome of MRSA bloodstream infections. Ann. Clin. Microbiol. Antimicrob. 6:13.
    OpenUrlCrossRefPubMed
  43. 43.
    Nonhoff, C., O. Denis, and M. J. Struelens. 2005. Low prevalence of methicillin-resistant Staphylococcus aureus with reduced susceptibility to glycopeptides in Belgian hospitals. Clin. Microbiol. Infect. 11:214-220.
    OpenUrlCrossRefPubMedWeb of Science
  44. 44.
    Reverdy, M. E., S. Jarraud, S. Bobin-Dubreux, E. Burel, P. Girardo, G. Lina, F. Vandenesch, and J. Etienne. 2001. Incidence of Staphylococcus aureus with reduced susceptibility to glycopeptides in two French hospitals. Clin. Microbiol. Infect. 7:267-272.
    OpenUrlCrossRefPubMedWeb of Science
  45. 45.
    Rybak, M. J., R. Cha, C. M. Cheung, V. G. Meka, and G. W. Kaatz. 2005. Clinical isolates of Staphylococcus aureus from 1987 and 1989 demonstrating heterogeneous resistance to vancomycin and teicoplanin. Diagn. Microbiol. Infect. Dis. 51:119-125.
    OpenUrlCrossRefPubMedWeb of Science
  46. 46.
    Rybak, M. J., S. N. Leonard, K. L. Rossi, C. M. Cheung, H. S. Sader, and R. N. Jones. 2008. Characterization of vancomycin-heteroresistant Staphylococcus aureus from the metropolitan area of Detroit, Michigan, over a 22-year period (1986 to 2007). J. Clin. Microbiol. 46:2950-2954.
    OpenUrlAbstract/FREE Full Text
  47. 47.↵
    Sader, H. S., R. N. Jones, K. L. Rossi, and M. J. Rybak. 2009. Occurrence of vancomycin-tolerant and heterogeneous vancomycin-intermediate strains (hVISA) among Staphylococcus aureus causing bloodstream infections in nine USA hospitals. J. Antimicrob. Chemother. 64:1024-1028.
    OpenUrlCrossRefPubMed
  48. 48.↵
    Sakoulas, G., J. Alder, C. Thauvin-Eliopoulos, R. C. Moellering, Jr., and G. M. Eliopoulos. 2006. Induction of daptomycin heterogeneous susceptibility in Staphylococcus aureus by exposure to vancomycin. Antimicrob. Agents Chemother. 50:1581-1585.
    OpenUrlAbstract/FREE Full Text
  49. 49.↵
    Sancak, B., S. Ercis, D. Menemenlioglu, S. Colakoglu, and G. Hascelik. 2005. Methicillin-resistant Staphylococcus aureus heterogeneously resistant to vancomycin in a Turkish university hospital. J. Antimicrob. Chemother. 56:519-523.
    OpenUrlCrossRefPubMedWeb of Science
  50. 50.↵
    Schmitz, F. J., A. Krey, R. Geisel, J. Verhoef, H. P. Heinz, and A. C. Fluit. 1999. Susceptibility of 302 methicillin-resistant Staphylococcus aureus isolates from 20 European university hospitals to vancomycin and alternative antistaphylococcal compounds. SENTRY Participants Group. Eur. J. Clin. Microbiol. Infect. Dis. 18:528-530.
    OpenUrlCrossRefPubMedWeb of Science
  51. 51.↵
    Sieradzki, K., and A. Tomasz. 2003. Alterations of cell wall structure and metabolism accompany reduced susceptibility to vancomycin in an isogenic series of clinical isolates of Staphylococcus aureus. J. Bacteriol. 185:7103-7110.
    OpenUrlAbstract/FREE Full Text
  52. 52.↵
    Song, J. H., K. Hiramatsu, J. Y. Suh, K. S. Ko, T. Ito, M. Kapi, S. Kiem, Y. S. Kim, W. S. Oh, K. R. Peck, and N. Y. Lee. 2004. Emergence in Asian countries of Staphylococcus aureus with reduced susceptibility to vancomycin. Antimicrob. Agents Chemother. 48:4926-4928.
    OpenUrlAbstract/FREE Full Text
  53. 53.↵
    Soriano, A., F. Marco, J. A. Martinez, E. Pisos, M. Almela, V. P. Dimova, D. Alamo, M. Ortega, J. Lopez, and J. Mensa. 2008. Influence of vancomycin minimum inhibitory concentration on the treatment of methicillin-resistant Staphylococcus aureus bacteremia. Clin. Infect. Dis. 46:193-200.
    OpenUrlCrossRefPubMedWeb of Science
  54. 54.↵
    Streit, J. M., H. S. Sader, T. R. Fritsche, and R. N. Jones. 2005. Dalbavancin activity against selected populations of antimicrobial-resistant Gram-positive pathogens. Diagn. Microbiol. Infect. Dis. 53:307-310.
    OpenUrlCrossRefPubMedWeb of Science
  55. 55.↵
    Sun, W., H. Chen, Y. Liu, C. Zhao, W. W. Nichols, M. Chen, J. Zhang, Y. Ma, and H. Wang. 2009. Prevalence and characterization of heterogeneous vancomycin-intermediate Staphylococcus aureus isolates from 14 cities in China. Antimicrob. Agents Chemother. 53:3642-3649.
    OpenUrlAbstract/FREE Full Text
  56. 56.↵
    Tallent, S. M., T. Bischoff, M. Climo, B. Ostrowsky, R. P. Wenzel, and M. B. Edmond. 2002. Vancomycin susceptibility of oxacillin-resistant Staphylococcus aureus isolates causing nosocomial bloodstream infections. J. Clin. Microbiol. 40:2249-2250.
    OpenUrlAbstract/FREE Full Text
  57. 57.↵
    Tenover, F. C., and R. C. Moellering, Jr. 2007. The rationale for revising the Clinical and Laboratory Standards Institute vancomycin minimal inhibitory concentration interpretive criteria for Staphylococcus aureus. Clin. Infect. Dis. 44:1208-1215.
    OpenUrlCrossRefPubMedWeb of Science
  58. 58.↵
    Trakulsomboon, S., S. Danchaivijitr, Y. Rongrungruang, C. Dhiraputra, W. Susaemgrat, T. Ito, and K. Hiramatsu. 2001. First report of methicillin-resistant Staphylococcus aureus with reduced susceptibility to vancomycin in Thailand. J. Clin. Microbiol. 39:591-595.
    OpenUrlAbstract/FREE Full Text
  59. 59.↵
    Turnidge, J. D., D. Kotsanas, W. Munckhof, S. Roberts, C. M. Bennett, G. R. Nimmo, G. W. Coombs, R. J. Murray, B. Howden, P. D. Johnson, and K. Dowling. 2009. Staphylococcus aureus bacteraemia: a major cause of mortality in Australia and New Zealand. Med. J. Aust. 191:368-373.
    OpenUrlPubMedWeb of Science
  60. 60.↵
    Walsh, T. R., R. A. Howe, M. Wootton, P. M. Bennett, and A. P. MacGowan. 2001. Detection of glycopeptide resistance in Staphylococcus aureus. J. Antimicrob. Chemother. 47:357-358.
    OpenUrlCrossRefPubMedWeb of Science
  61. 61.↵
    Wong, S. S., P. L. Ho, P. C. Woo, and K. Y. Yuen. 1999. Bacteremia caused by staphylococci with inducible vancomycin heteroresistance. Clin. Infect. Dis. 29:760-767.
    OpenUrlCrossRefPubMedWeb of Science
PreviousNext
Back to top
Download PDF
Citation Tools
Systematic Review and Meta-Analysis of the Significance of Heterogeneous Vancomycin-Intermediate Staphylococcus aureus Isolates
Sebastiaan J. van Hal, David L. Paterson
Antimicrobial Agents and Chemotherapy Dec 2010, 55 (1) 405-410; DOI: 10.1128/AAC.01133-10

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Print

Alerts
Sign In to Email Alerts with your Email Address
Email

Thank you for sharing this Antimicrobial Agents and Chemotherapy article.

NOTE: We request your email address only to inform the recipient that it was you who recommended this article, and that it is not junk mail. We do not retain these email addresses.

Enter multiple addresses on separate lines or separate them with commas.
Systematic Review and Meta-Analysis of the Significance of Heterogeneous Vancomycin-Intermediate Staphylococcus aureus Isolates
(Your Name) has forwarded a page to you from Antimicrobial Agents and Chemotherapy
(Your Name) thought you would be interested in this article in Antimicrobial Agents and Chemotherapy.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
Systematic Review and Meta-Analysis of the Significance of Heterogeneous Vancomycin-Intermediate Staphylococcus aureus Isolates
Sebastiaan J. van Hal, David L. Paterson
Antimicrobial Agents and Chemotherapy Dec 2010, 55 (1) 405-410; DOI: 10.1128/AAC.01133-10
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Top
  • Article
    • ABSTRACT
    • Detection.
    • Epidemiology.
    • Clinical significance of hVISA.
    • Significance of MIC in hVISA.
    • Mortality and hVISA.
    • Conclusion and therapeutic implications.
    • FOOTNOTES
    • REFERENCES
  • Figures & Data
  • Info & Metrics
  • PDF

Related Articles

Cited By...

About

  • About AAC
  • Editor in Chief
  • Editorial Board
  • Policies
  • For Reviewers
  • For the Media
  • For Librarians
  • For Advertisers
  • Alerts
  • AAC Podcast
  • RSS
  • FAQ
  • Permissions
  • Journal Announcements

Authors

  • ASM Author Center
  • Submit a Manuscript
  • Article Types
  • Ethics
  • Contact Us

Follow #AACJournal

@ASMicrobiology

       

ASM Journals

ASM journals are the most prominent publications in the field, delivering up-to-date and authoritative coverage of both basic and clinical microbiology.

About ASM | Contact Us | Press Room

 

ASM is a member of

Scientific Society Publisher Alliance

 

American Society for Microbiology
1752 N St. NW
Washington, DC 20036
Phone: (202) 737-3600

Copyright © 2021 American Society for Microbiology | Privacy Policy | Website feedback

Print ISSN: 0066-4804; Online ISSN: 1098-6596