Performance of the EUCAST disk diffusion method, the CLSI agar screen method, and the Vitek 2 automated antimicrobial susceptibility testing system for detection of clinical isolates of enterococci with low- and medium-level VanB-type vancomycin resistance: A multicenter study

Journal of Clinical Microbiology

Volumn 52, Issue 5, 2014, Pages 1582-1589

  Hegstad, Kristin ^a,b   Giske, Christian G ^c   Haldorsen, Bjørg ^a   Matuschek, Erika ^d   Schønning, Kristian ^e   Leegaard, Truls M ^f   Kahlmeter, Gunnar ^d   Sundsfjord, Arnfinn ^a,b  

^a UNIVERSITY HOSPITAL OF NORTH NORWAY   (Norway)

^b UNIVERSITY OF TROMSØ   (Norway)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^d EUCAST Laboratory for Antimicrobial Susceptibility Testing   (Sweden)

^e HVIDOVRE HOSPITAL   (Denmark)

^f AKERSHUS UNIVERSITY HOSPITAL   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

AGAR DIFFUSION; ARTICLE; BACTERIUM DETECTION; BACTERIUM ISOLATION; CONCENTRATION (PARAMETERS); DIAGNOSTIC ERROR; DISK DIFFUSION; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; GENOTYPE; INTERMETHOD COMPARISON; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SENSITIVITY AND SPECIFICITY; VANCOMYCIN RESISTANT ENTEROCOCCUS; ANTIBIOTIC RESISTANCE; CLINICAL TRIAL; CULTURE MEDIUM; DRUG EFFECTS; GENETICS; GRAM-POSITIVE BACTERIAL INFECTIONS; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; MULTICENTER STUDY; PROCEDURES;

AGAR; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; CULTURE MEDIUM; VANB PROTEIN, ENTEROCOCCUS; VANCOMYCIN;

AGAR; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CULTURE MEDIA; DISK DIFFUSION ANTIMICROBIAL TESTS; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; GENOTYPE; GRAM-POSITIVE BACTERIAL INFECTIONS; HUMANS; MICROBIAL SENSITIVITY TESTS; SENSITIVITY AND SPECIFICITY; VANCOMYCIN; VANCOMYCIN RESISTANCE;

EID: 84899550843     PISSN: 00951137     EISSN: 1098660X     Source Type: Journal    
DOI: 10.1128/JCM.03544-13     Document Type: Article

References (43)

1. Werner G, Coque TM, Franz CM, Grohmann E, Hegstad K, Jensen L, van Schaik W, Weaver K. 2013. Antibiotic resistant enterococci: tales of a drug resistance gene trafficker. Int. J. Med. Microbiol. 303:360-379. http://dx.doi.org/10. 1016/j.ijmm.2013.03.001.
2. Gilmore MS, Lebreton F, van Schaik W. 2013. Genomic transition of enterococci from gut commensals to leading causes of multidrug-resistant hospital infection in the antibiotic era. Curr. Opin. Microbiol. 16:10-16. http://dx.doi.org/10.1016/j.mib.2013.01.006.
3. de Kraker ME, Jarlier V, Monen JC, Heuer OE, van de Sande N, Grundmann H. 2013. The changing epidemiology of bacteraemias in Europe: trends from the European Antimicrobial Resistance Surveillance System. Clin. Microbiol. Infect. 19:860-868. http://dx.doi.org/10.1111/1469-0691.12028.
4. Gilmore MS, Ferretti JJ. 2003. Microbiology: the thin line between gut commensal and pathogen. Science 299:1999-2002. http://dx.doi.org/10.1126/ science.1083534.
5. Zhang X, Top J, de Been M, Bierschenk D, Rogers M, Leendertse M, Bonten MJ, van der Poll T, Willems RJ, van Schaik W. 2013. Identification of a genetic determinant in clinical Enterococcus faecium strains that contributes to intestinal colonization during antibiotic treatment. J. Infect. Dis. 207:1780-1786. http://dx.doi.org/10.1093/infdis/jit076.
6. Arias CA, Contreras GA, Murray BE. 2010. Management of multi-drug resistant enterococcal infections. Clin. Microbiol. Infect. 16:555-562. http://dx.doi.org/10.1111/j.1469-0691.2010.03214.x.
7. Hegstad K, Mikalsen T, Coque TM, Jensen LB, Werner G, Sundsfjord A. 2010. Mobile genetic elements and their contribution to the emergence of antimicrobial resistant Enterococcus faecalis and E. faecium. Clin. Microbiol. Infect. 16:541-554. http://dx.doi.org/10.1111/j.1469-0691.2010.03226.x.
8. Xu X, Lin D, Yan G, Ye X, Wu S, Guo Y, Zhu D, Hu F, Zhang Y, Wang F, Jacoby GA, Wang M. 2010. vanM, a new glycopeptide resistance gene cluster found in Enterococcus faecium. Antimicrob. Agents Chemother. 54:4643-4647. http://dx.doi.org/10.1128/AAC.01710-09.
9. Lebreton F, Depardieu F, Bourdon N, Fines-Guyon M, Berger P, Camiade S, Leclercq R, Courvalin P, Cattoir V. 2011. D-Ala-D-Ser VanN-type transferable vancomycin resistance in Enterococcus faecium. Antimicrob. Agents Chemother. 55:4606-4612. http://dx.doi.org/10.1128/AAC.00714-11.
10. Werner G, Coque TM, Hammerum AM, Hope R, Hryniewicz W, Johnson A, Klare I, Kristinsson KG, Leclercq R, Lester CH, Lillie M, Novais C, Olsson-Liljequist B, Peixe LV, Sadowy E, Simonsen GS, Top J, Vuopio-Varkila J, Willems RJ, Witte W, Woodford N. 2008. Emergence and spread of vancomycin resistance among enterococci in Europe. Euro Surveill. 13(47):pii-19046. http://www. eurosurveillance.org/View Article.aspx?ArticleId-19046.
11. Granlund M, Carlsson C, Edebro H, Emanuelsson K, Lundholm R. 2006. Nosocomial outbreak of vanB2 vancomycin-resistant Enterococcus faecium in Sweden. J. Hosp Infect. 62:254-256. http://dx.doi.org/10.1016/j.jhin. 2005.06.031.
12. Werner G, Klare I, Fleige C, Geringer U, Witte W, Just HM, Ziegler R. 2012. Vancomycin-resistant vanB-type Enterococcus faecium isolates expressing varying levels of vancomycin resistance and being highly prevalent among neonatal patients in a single ICU. Antimicrob. Resist. Infect. Control 1:21. http://dx.doi.org/10.1186/2047-2994-1-21.
13. Bourdon N, Fines-Guyon M, Thiolet JM, Maugat S, Coignard B, Leclercq R, Cattoir V. 2011. Changing trends in vancomycin-resistant enterococci in French hospitals, 2001-08. J. Antimicrob. Chemother. 66:713-721. http://dx.doi.org/10. 1093/jac/dkq524.
14. Söderblom T, Aspevall O, Erntell M, Hedin G, Heimer D, Hökeberg I, Kidd-Ljunggren K, Melhus Å, Olsson-Liljequist B, Sjögren I, Smedjegård J, Struwe J, Sylvan S, Tegmark-Wisell K, Thore M. 2010. Alarming spread of vancomycin resistant enterococci in Sweden since 2007. Euro Surveill. 15(29):pii-19620. http://www.eurosurveillance.org/View Article.aspx?ArticleId-19620.
15. Bjørkeng EK, Rasmussen G, Sundsfjord A, Sjöberg L, Hegstad K, Söderquist B. 2011. Clustering of polyclonal VanB-type vancomycinresistant Enterococcus faecium in a low-endemic area was associated with CC17-genogroup strains harbouring transferable vanB2-Tn5382 and pRUM-like repA containing plasmids with axe-txe plasmid addiction systems. APMIS 119:247-258. http://dx.doi.org/10.1111/j.1600-0463.2011.02724.x.
16. Johnson PD, Ballard SA, Grabsch EA, Stinear TP, Seemann T, Young HL, Grayson ML, Howden BP. 2010. A sustained hospital outbreak of vancomycin-resistant Enterococcus faecium bacteremia due to emergence of vanB E. faecium sequence type 203. J. Infect. Dis. 202:1278-1286. http://dx.doi.org/10. 1086/656319.
17. Dahl KH, Simonsen GS, Olsvik Ø, Sundsfjord A. 1999. Heterogeneity in the vanB gene cluster of genomically diverse clinical strains of vancomycinresistant enterococci. Antimicrob. Agents Chemother. 43:1105-1110.
18. Gold HS, Unal S, Cercenado E, Thauvin Eliopoulos C, Eliopoulos GM, Wennersten CB, Moellering RC, Jr. 1993. A gene conferring resistance to vancomycin but not teicoplanin in isolates of Enterococcus faecalis and Enterococcus faecium demonstrates homology with vanB, vanA, and vanC genes of enterococci. Antimicrob. Agents Chemother. 37:1604-1609. http://dx.doi.org/10. 1128/AAC.37.8.1604.
19. Patel R, Uhl JR, Kohner P, Hopkins MK, Steckelberg JM, Kline B, Cockerill FR III. 1998. DNA sequence variation within vanA, vanB, vanC-1, and vanC-2/3 genes of clinical Enterococcus isolates. Antimicrob. Agents Chemother. 42:202-205.
20. Courvalin P. 2006. Vancomycin resistance in Gram-positive cocci. Clin. Infect. Dis. 42(Suppl 1):S25-S34. http://dx.doi.org/10.1086/491711.
21. Boyce JM, Opal SM, Chow JW, Zervos MJ, Potter-Bynoe G, Sherman CB, Romulo RL, Fortna S, Medeiros AA. 1994. Outbreak of multidrugresistant Enterococcus faecium with transferable vanB class vancomycin resistance. J. Clin. Microbiol. 32:1148-1153.
22. European Committee on Antimicrobial Susceptibility Testing. 2013. Breakpoint tables for interpretation of MICs and zone diameters, version 3.1, 2013. http://www.eucast.org/fileadmin/src/media/PDFs/EUCAST-files/Breakpoint- tables/Breakpoint-table-v-3.1.pdf.
23. Hayden MK, Trenholme GM, Schultz JE, Sahm DF. 1993. In vivo development of teicoplanin resistance in a VanB Enterococcus faecium isolate. J. Infect. Dis. 167:1224-1227. http://dx.doi.org/10.1093/infdis/167.5.1224.
24. Kawalec M, Gniadkowski M, Kedzierska J, Skotnicki A, Fiett J, Hryniewicz W. 2001. Selection of a teicoplanin-resistant Enterococcus faecium mutant during an outbreak caused by vancomycin-resistant enterococci with the vanB phenotype. J. Clin. Microbiol. 39:4274-4282. http://dx.doi.org/10.1128/JCM.39.12.4274- 4282.2001.
25. San Millan A, Depardieu F, Godreuil S, Courvalin P. 2009. VanB-type Enterococcus faecium clinical isolate successively inducibly resistant to, dependent on, and constitutively resistant to vancomycin. Antimicrob. Agents Chemother. 53:1974-1982. http://dx.doi.org/10.1128/AAC.00034-09.
26. Holmes NE, Ballard SA, Lam MM, Johnson PD, Grayson ML, Stinear TP, Howden BP. 2013. Genomic analysis of teicoplanin resistance emerging during treatment of vanB vancomycin-resistant Enterococcus faecium infections in solid organ transplant recipients including donor-derived cases. J. Antimicrob. Chemother. 68:2134-2139. http://dx.doi.org/10.1093/jac/dkt130.
27. Dutka-Malen S, Evers S, Courvalin P. 1995. Detection of glycopeptide resistance genotypes and identification to the species level of clinically relevant enterococci by PCR. J. Clin. Microbiol. 33:24-27.
28. Fines M, Perichon B, Reynolds P, Sahm DF, Courvalin P. 1999. VanE, a new type of acquired glycopeptide resistance in Enterococcus faecalis BM4405. Antimicrob. Agents Chemother. 43:2161-2164.
29. Depardieu F, Perichon B, Courvalin P. 2004. Detection of the van alphabet and identification of enterococci and staphylococci at the species level by multiplex PCR. J. Clin. Microbiol. 42:5857-5860. http://dx.doi.org/10.1128/JCM. 42.12.5857-5860.2004.
30. Dahl KH, Lundblad EW, Røkenes TP, Olsvik Ø, Sundsfjord A. 2000. Genetic linkage of the vanB2 gene cluster to Tn5382 in vancomycinresistant enterococci and characterization of two novel insertion sequences. Microbiology 146:1469-1479.
31. International Organization for Standardization. 2006. Clinical laboratory testing and in vitro diagnostic test systems: susceptibility testing of infectious agents and evaluation of performance of antimicrobial susceptibility test devices. Part 1: reference method for testing the in vitro activity of antimicrobial agents against rapidly growing aerobic bacteria involved in infectious diseases. Publication ISO 20776-1. International Organization for Standardization, Geneva, Switzerland.
32. Dahl KH, Røkenes TP, Lundblad EW, Sundsfjord A. 2003. Nonconjugative transposition of the vanB-containing Tn5382-like element in Enterococcus faecium. Antimicrob. Agents Chemother. 47:786-789. http://dx.doi.org/10.1128/AAC.47.2.786-789.2003.
33. Harthug S, Digranes A, Hope O, Kristiansen BE, Allum AG, Langeland N. 2000. Vancomycin resistance emerging in a clonal outbreak caused by ampicillin-resistant Enterococcus faecium. Clin. Microbiol. Infect. 6:19-28. http://dx.doi.org/10.1046/j.1469-0691.2000.00008.x.
34. European Committee on Antimicrobial Susceptibility Testing. 2013. Antimicrobial susceptibility testing: EUCAST disk diffusion method, version 3.0, 2013. http://www.eucast.org/fileadmin/src/media/PDFs/EUCAST-files/Disk-test- documents/Manual-v-3.0-EUCAST-Disk-Test.pdf.
35. Swenson JM, Clark NC, Ferraro MJ, Sahm DF, Doern G, Pfaller MA, Reller LB, Weinstein MP, Zabransky RJ, Tenover FC. 1994. Development of a standardized screening method for detection of vancomycinresistant enterococci. J. Clin. Microbiol. 32:1700-1704.
36. Klare I, Fleige C, Geringer U, Witte W, Werner G. 2012. Performance of three chromogenic VRE screening agars, two EtestR vancomycin protocols, and different microdilution methods in detecting vanB genotype Enterococcus faecium with varying vancomycin MICs. Diagn. Microbiol. Infect. Dis. 74:171-176. http://dx.doi.org/10.1016/j.diagmicrobio.2012.06.020.
37. Grabsch EA, Chua K, Xie S, Byrne J, Ballard SA, Ward PB, Grayson ML. 2008. Improved detection of vanB2-containing Enterococcus faecium with vancomycin susceptibility by Etest using oxgall supplementation. J. Clin. Microbiol. 46:1961-1964. http://dx.doi.org/10.1128/JCM.01778-07.
38. Swenson JM, Clark NC, Sahm DF, Ferraro MJ, Doern G, Hindler J, Jorgensen JH, Pfaller MA, Reller LB, Weinstein MP. 1995. Molecular characterization and multilaboratory evaluation of Enterococcus faecalis ATCC 51299 for quality control of screening tests for vancomycin and high-level aminoglycoside resistance in enterococci. J. Clin. Microbiol. 33:3019-3021.
39. Kim EB, Kopit LM, Harris LJ, Marco ML. 2012. Draft genome sequence of the quality control strain Enterococcus faecalis ATCC 29212. J. Bacteriol. 194:6006-6007. http://dx.doi.org/10.1128/JB.01423-12.
40. Depardieu F, Bonora MG, Reynolds PE, Courvalin P. 2003. The vanG glycopeptide resistance operon from Enterococcus faecalis revisited. Mol. Microbiol. 50:931-948. http://dx.doi.org/10.1046/j.1365-2958.2003.03737.x.
41. Carias LL, Rudin SD, Donskey CJ, Rice LB. 1998. Genetic linkage and cotransfer of a novel, vanB-containing transposon (Tn5382) and a lowaffinity penicillin-binding protein 5 gene in a clinical vancomycinresistant Enterococcus faecium isolate. J. Bacteriol. 180:4426-4434.
42. Rosvoll TC, Pedersen T, Sletvold H, Johnsen PJ, Sollid JE, Simonsen GS, Jensen LB, Nielsen KM, Sundsfjord A. 2010. PCR-based plasmid typing in Enterococcus faecium strains reveals widely distributed pRE25-, pRUM-, pIP501- and pHTβ-related replicons associated with glycopeptide resistance and stabilizing toxin-antitoxin systems. FEMS Immunol. Med. Microbiol. 58:254-268. http://dx.doi.org/10.1111/j.1574-695X.2009.00633.x.
43. Nallapareddy SR, Wenxiang H, Weinstock GM, Murray BE. 2005. Molecular characterization of a widespread, pathogenic, and antibiotic resistance-receptive Enterococcus faecalis lineage and dissemination of its putative pathogenicity island. J. Bacteriol. 187:5709-5718. http://dx.doi.org/ 10.1128/JB.187.16.5709-5718.2005.