Increased high-level gentamicin resistance in invasive Enterococcus faecium is associated with aac(6′)Ie-aph(2″)Ia-encoding transferable megaplasmids hosted by major hospital-adapted lineages

FEMS Immunology and Medical Microbiology

Volumn 66, Issue 2, 2012, Pages 166-176

  Rosvoll, Torill C S ^a   Lindstad, Belinda L ^a   Lunde, Tracy M ^b   Hegstad, Kristin ^a,b   Aasnæs, Bettina ^b   Hammerum, Anette M ^c   Lester, Camilla H ^c   Simonsen, Gunnar S ^a,b   Sundsfjord, Arnfinn ^a,b   Pedersen, Torunn ^b  

^a UNIVERSITY OF TROMSØ   (Norway)

^b UNIVERSITY HOSPITAL OF NORTH NORWAY   (Norway)

^c STATENS SERUM INSTITUT   (Denmark)

Author keywords

aac(6 )Ie aph(2 )Ia; High level gentamicin resistance; Hospital adapted lineages; Megaplasmids; PLG1 replicon type; Virulence genes

Indexed keywords

AMINOGLYCOSIDE; GENTAMICIN;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; BLOOD CULTURE; ENTEROCOCCUS FAECIUM; GENE LOCUS; GENETIC CODE; GENETIC LINKAGE; GENOTYPE; HOSPITAL; MULTILOCUS SEQUENCE TYPING; NONHUMAN; PLASMID; PREVALENCE; PRIORITY JOURNAL; PULSED FIELD GEL ELECTROPHORESIS; REPLICON; SEQUENCE ANALYSIS;

ACETYLTRANSFERASES; ANTI-BACTERIAL AGENTS; CROSS INFECTION; DRUG RESISTANCE, BACTERIAL; ENTEROCOCCUS FAECIUM; GENOTYPE; GENTAMICINS; GRAM-POSITIVE BACTERIAL INFECTIONS; HOSPITALS; HUMANS; MOLECULAR TYPING; NORWAY; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PLASMIDS;

EID: 84867703341     PISSN: 09288244     EISSN: 1574695X     Source Type: Journal    
DOI: 10.1111/j.1574-695X.2012.00997.x     Document Type: Article

References (56)

1. Abbassi MS, Achour W & Hassen AB (2007) High-level gentamicin-resistant Enterococcus faecium strains isolated from bone marrow transplant patients: accumulation of antibiotic resistance genes, large plasmids and clonal strain dissemination. Int J Antimicrob Agents 29: 658-664.
2. Araoka H, Kimura M & Yoneyama A (2011) A surveillance of high-level gentamicin-resistant enterococcal bacteremia. J Infect Chemother 17: 433-434.
3. Arias CA, Panesso D, Singh KV, Rice LB & Murray BE (2009) Cotransfer of antibiotic resistance genes and a hylEfm-containing virulence plasmid in Enterococcus faecium. Antimicrob Agents Chemother 53: 4240-4246.
4. Arias CA, Contreras GA & Murray BE (2010) Management of multidrug-resistant enterococcal infections. Clin Microbiol Infect 16: 555-562.
5. Chow JW (2000) Aminoglycoside resistance in enterococci. Clin Infect Dis 31: 586-589.
6. Costa Y, Galimand M, Leclercq R, Duval J & Courvalin P (1993) Characterization of the chromosomal aac(6′)-Ii gene specific for Enterococcus faecium. Antimicrob Agents Chemother 37: 1896-1903.
7. Dorobat OM, Badicut I, Talapan D, Tenea C & Rafila A (2010) Antibiotic resistance of Gram-positive cocci isolated in 2008. Bacteriol Virusol Parazitol Epidemiol 55: 83-92.
8. 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.
9. Ferretti JJ, Gilmore KS & Courvalin P (1986) Nucleotide sequence analysis of the gene specifying the bifunctional 6′-aminoglycoside acetyltransferase 2″-aminoglycoside phosphotransferase enzyme in Streptococcus faecalis and identification and cloning of gene regions specifying the two activities. J Bacteriol 167: 631-638.
10. Freitas AR, Tedim AP, Novais C, Ruiz-Garbajosa P, Werner G, Laverde-Gomez JA, Canton R, Peixe L, Baquero F & Coque TM (2010) Global spread of the hyl(Efm) colonization-virulence gene in megaplasmids of the Enterococcus faecium CC17 polyclonal subcluster. Antimicrob Agents Chemother 54: 2660-2665.
11. Freitas AR, Coque TM, Novais C et al. (2011) Human and swine hosts share vancomycin-resistant Enterococcus faecium CC17 and CC5 and Enterococcus faecalis CC2 clonal clusters harboring Tn1546 on indistinguishable plasmids. J Clin Microbiol 49: 925-931.
12. Hammerum AM, Lester CH, Olsen SS, Holm A, Hansen DS & Schonheyder HC (2012) Molecular characterisation of high-level gentamicin-resistant enterococci from bloodstream infections in Denmark: first description of clonal spread of aph(2″)-Ib. Int J Antimicrob Agents 39: 266-268.
13. Hegstad K, Mikalsen T, Coque TM, Werner G & Sundsfjord A (2010) Mobile genetic elements and their contribution to the emergence of antimicrobial resistant Enterococcus faecalis and Enterococcus faecium. Clin Microbiol Infect 16: 541-554.
14. Heikens E, Bonten MJ & Willems RJ (2007) Enterococcal surface protein Esp is important for biofilm formation of Enterococcus faecium E1162. J Bacteriol 189: 8233-8240.
15. Heikens E, Singh KV, Jacques-Palaz KD, van Luit-Asbroek M, Oostdijk EA, Bonten MJ, Murray BE & Willems RJ (2011) Contribution of the enterococcal surface protein Esp to pathogenesis of Enterococcus faecium endocarditis. Microbes Infect 13: 1185-1190.
16. Hendrickx AP, van Wamel WJ, Posthuma G, Bonten MJ & Willems RJ (2007) Five genes encoding surface-exposed LPXTG proteins are enriched in hospital-adapted Enterococcus faecium clonal complex 17 isolates. J Bacteriol 189: 8321-8332.
17. Hendrickx AP, Bonten MJ, van Luit-Asbroek M, Schapendonk CM, Kragten AH & Willems RJ (2008) Expression of two distinct types of pili by a hospital-acquired Enterococcus faecium isolate. Microbiology 154: 3212-3223.
18. Hendrickx AP, Willems RJ, Bonten MJ & van Schaik W (2009a) LPxTG surface proteins of enterococci. Trends Microbiol 17: 423-430.
19. Hendrickx AP, van Luit-Asbroek M, Schapendonk CM et al. (2009b) SgrA, a nidogen-binding LPXTG surface adhesin implicated in biofilm formation, and EcbA, a collagen binding MSCRAMM, are two novel adhesins of hospital-acquired Enterococcus faecium. Infect Immun 77: 5097-5106.
20. Hodel-Christian SL & Murray BE (1991) Characterization of the gentamicin resistance transposon Tn5281 from Enterococcus faecalis and comparison to staphylococcal transposons Tn4001 and Tn4031. Antimicrob Agents Chemother 35: 1147-1152.
21. Homan WL, Tribe D, Poznanski S, Li M, Hogg G, Spalburg E, Van Embden JD & Willems RJ (2002) Multilocus sequence typing scheme for Enterococcus faecium. J Clin Microbiol 40: 1963-1971.
22. Jensen LB, Garcia-Migura L, Valenzuela AJ, Lohr M, Hasman H & Aarestrup FM (2010) A classification system for plasmids from enterococci and other Gram-positive bacteria. J Microbiol Methods 80: 25-43.
23. 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.
24. Kao SJ, You I, Clewell DB, Donabedian SM, Zervos MJ, Petrin J, Shaw KJ & Chow JW (2000) Detection of the high-level aminoglycoside resistance gene aph(2″)-Ib in Enterococcus faecium. Antimicrob Agents Chemother 44: 2876-2879.
25. Kim DS, Singh KV, Nallapareddy SR, Qin X, Panesso D, Arias CA & Murray BE (2010) The fms21(pilA)-fms20 locus encoding one of four distinct pili of Enterococcus faecium is harboured on a large transferable plasmid associated with gut colonization and virulence. J Med Microbiol 59: 505-507.
26. Laverde Gomez JA, van Schaik W, Freitas AR, Coque TM, Weaver KE, Francia MV, Witte W & Werner G (2011) A multiresistance megaplasmid pLG1 bearing a hylEfm genomic island in hospital Enterococcus faecium isolates. Int J Med Microbiol 301: 165-175.
27. Leavis HL, Bonten MJ & Willems RJ (2006) Identification of high-risk enterococcal clonal complexes: global dispersion and antibiotic resistance. Curr Opin Microbiol 9: 454-460.
28. Leendertse M, Heikens E, Wijnands LM et al. (2009) Enterococcal surface protein transiently aggravates Enterococcus faecium-induced urinary tract infection in mice. J Infect Dis 200: 1162-1165.
29. Lester CH, Sandvang D, Olsen SS, Schonheyder HC, Jarlov JO, Bangsborg J, Hansen DS, Jensen TG, Frimodt-Moller N & Hammerum AM (2008) Emergence of ampicillin-resistant Enterococcus faecium in Danish hospitals. J Antimicrob Chemother 62: 1203-1206.
30. Moellering RC Jr (1991) The Garrod Lecture. The enterococcus: a classic example of the impact of antimicrobial resistance on therapeutic options. J Antimicrob Chemother 28: 1-12.
31. Morrison D, Woodford N, Barrett SP, Sisson P & Cookson BD (1999) DNA banding pattern polymorphism in vancomycin-resistant Enterococcus faecium and criteria for defining strains. J Clin Microbiol 37: 1084-1091.
32. Nallapareddy SR, Weinstock GM & Murray BE (2003) Clinical isolates of Enterococcus faecium exhibit strain-specific collagen binding mediated by Acm, a new member of the MSCRAMM family. Mol Microbiol 47: 1733-1747.
33. Nallapareddy SR, Singh KV, Okhuysen PC & Murray BE (2008) A functional collagen adhesin gene, acm, in clinical isolates of Enterococcus faecium correlates with the recent success of this emerging nosocomial pathogen. Infect Immun 76: 4110-4119.
34. NORM/NORM-VET (2008) NORM/NORM-VET 2008. Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. Tromsø/Oslo 2009. NORM/NORM-VET, Tromsø/Oslo.
35. Panesso D, Reyes J, Rincon S et al. (2010) Molecular epidemiology of vancomycin-resistant Enterococcus faecium: a prospective, multicenter study in South American hospitals. J Clin Microbiol 48: 1562-1569.
36. Panesso D, Montealegre MC, Rincon S, Mojica MF, Rice LB, Singh KV, Murray BE & Arias CA (2011) The hylEfm gene in pHylEfm of Enterococcus faecium is not required in pathogenesis of murine peritonitis. BMC Microbiol 11: 20.
37. Rice LB, Lakticova V, Carias LL, Rudin S, Hutton R & Marshall SH (2009) Transferable capacity for gastrointestinal colonization in Enterococcus faecium in a mouse model. J Infect Dis 199: 342-349.
38. 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 pHTbeta-related replicons associated with glycopeptide resistance and stabilizing toxin-antitoxin systems. FEMS Immunol Med Microbiol 58: 254-268.
39. Sangsuk L, Dejsirilert S, Sawanpanyalert P, Aswapokee N & Jariyasethpong T (2009) Antimicrobial susceptibility of enterococci in Thailand from 2000 to 2005. J Med Assoc Thai 92(suppl 4): S1-S7.
40. Sava IG, Heikens E & Huebner J (2010a) Pathogenesis and immunity in enterococcal infections. Clin Microbiol Infect 16: 533-540.
41. Sava IG, Heikens E, Kropec A, Theilacker C, Willems R & Huebner J (2010b) Enterococcal surface protein contributes to persistence in the host but is not a target of opsonic and protective antibodies in Enterococcus faecium infection. J Med Microbiol 59: 1001-1004.
42. Sillanpaa J, Nallapareddy SR, Prakash VP, Qin X, Hook M, Weinstock GM & Murray BE (2008) Identification and phenotypic characterization of a second collagen adhesin, Scm, and genome-based identification and analysis of 13 other predicted MSCRAMMs, including four distinct pilus loci, in Enterococcus faecium. Microbiology 154: 3199-3211.
43. Sillanpaa J, Prakash VP, Nallapareddy SR & Murray BE (2009) Distribution of genes encoding MSCRAMMs and Pili in clinical and natural populations of Enterococcus faecium. J Clin Microbiol 47: 896-901.
44. Sillanpaa J, Nallapareddy SR, Singh KV, Prakash VP, Fothergill T, Ton-That H & Murray BE (2010) Characterization of the ebp(fm) pilus-encoding operon of Enterococcus faecium and its role in biofilm formation and virulence in a murine model of urinary tract infection. Virulence 1: 236-246.
45. Simjee S, Fraise AP & Gill MJ (1999) Plasmid heterogeneity and identification of a Tn5281-like element in clinical isolates of high-level gentamicin-resistant Enterococcus faecium isolated in the UK. J Antimicrob Chemother 43: 625-635.
46. Simjee S, Manzoor SE, Fraise AP & Gill MJ (2000) Nature of transposon-mediated high-level gentamicin resistance in Enterococcus faecalis isolated in the United Kingdom. J Antimicrob Chemother 45: 565-575.
47. Top J, Willems R, Blok H et al. (2007) Ecological replacement of Enterococcus faecalis by multiresistant clonal complex 17 Enterococcus faecium. Clin Microbiol Infect 13: 316-319.
48. Turabelidze D, Kotetishvili M, Kreger A, Morris JG Jr & Sulakvelidze A (2000) Improved pulsed-field gel electrophoresis for typing vancomycin-resistant enterococci. J Clin Microbiol 38: 4242-4245.
49. van Schaik W, Top J, Riley DR et al. (2010) Pyrosequencing-based comparative genome analysis of the nosocomial pathogen Enterococcus faecium and identification of a large transferable pathogenicity island. BMC Genomics 11: 239.
50. Watanabe S, Kobayashi N, Quinones D, Nagashima S, Uehara N & Watanabe N (2009) Genetic diversity of enterococci harboring the high-level gentamicin resistance gene aac(6′)-Ie-aph(2″)-Ia or aph(2″)-Ie in a Japanese hospital. Microb Drug Resist 15: 185-194.
51. Weaver KE, Kwong SM, Firth N & Francia MV (2009) The RepA_N replicons of Gram-positive bacteria: a family of broadly distributed but narrow host range plasmids. Plasmid 61: 94-109.
52. Weisburg WG, Barns SM, Pelletier DA & Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173: 697-703.
53. Werner G, Freitas AR, Coque TM et al. (2011) Host range of enterococcal vanA plasmids among Gram-positive intestinal bacteria. J Antimicrob Chemother 66: 273-282.
54. Willems RJ & van Schaik W (2009) Transition of Enterococcus faecium from commensal organism to nosocomial pathogen. Future Microbiol 4: 1125-1135.
55. Willems RJ, Top J, van Santen M et al. (2005) Global spread of vancomycin-resistant Enterococcus faecium from distinct nosocomial genetic complex. Emerg Infect Dis 11: 821-828.
56. Willems RJ, Hanage WP, Bessen DE & Feil EJ (2011) Population biology of Gram-positive pathogens: high-risk clones for dissemination of antibiotic resistance. FEMS Microbiol Rev 35: 872-900.