Skip to main content

Advertisement

Log in

Detection and characterisation of SCCmec remnants in multiresistant methicillin-susceptible Staphylococcus aureus causing a clonal outbreak in a Swedish county

  • Article
  • Published:
European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

Abstract

The purpose of this study was to investigate if multiresistant methicillin-susceptible Staphylococcus aureus (MR-MSSA) causing a clonal outbreak in Östergötland County, Sweden, were derived from methicillin-resistant S. aureus (MRSA) by carrying remnants of SCCmec, and, if so, to characterise this element. A total of 54 MSSA isolates with concomitant resistance to erythromycin, clindamycin and tobramycin from 49 patients (91% clonally related, spa type t002) were investigated with the BD GeneOhm MRSA assay and real-time polymerase chain reaction (PCR) targeting the SCCmec integration site/SCCmec right extremity junction. DNA sequencing of one isolate representing the MR-MSSA outbreak clone was performed by massive parallel 454 pyrosequencing. All isolates that were part of the clonal outbreak carried SCCmec remnants. The DNA sequencing revealed the carriage of a pseudo-SCC element 12 kb in size, with a genomic organisation identical to an SCCmec type ΙΙ element, except for a 41-kb gap. This study demonstrates the presence of a pseudo-SCC element resembling SCCmec type II among MR-MSSA, suggesting possible derivation from MRSA. The presence of SCCmec remnants should always be considered when SCCmec typing is used for MRSA detection, and may not be suitable in locations with a high prevalence of MR-MSSA, since this might give a high number of false-positive results.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Hiramatsu K, Cui L, Kuroda M, Ito T (2001) The emergence and evolution of methicillin-resistant Staphylococcus aureus. Trends Microbiol 9:486–493

    Article  PubMed  CAS  Google Scholar 

  2. International Working Group on the Classification of Staphylococcal Cassette Chromosome Elements (IWG-SCC) (2009) Classification of staphylococcal cassette chromosome mec (SCCmec): guidelines for reporting novel SCCmec elements. Antimicrob Agents Chemother 53:4961–4967

    Article  Google Scholar 

  3. Katayama Y, Ito T, Hiramatsu K (2000) A new class of genetic element, staphylococcus cassette chromosome mec, encodes methicillin resistance in Staphylococcus aureus. Antimicrob Agents Chemother 44:1549–1555

    Article  PubMed  CAS  Google Scholar 

  4. Robinson DA, Enright MC (2003) Evolutionary models of the emergence of methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 47:3926–3934

    Article  PubMed  CAS  Google Scholar 

  5. Hiramatsu K, Katayama Y, Yuzawa H, Ito T (2002) Molecular genetics of methicillin-resistant Staphylococcus aureus. Int J Med Microbiol 292:67–74

    Article  PubMed  CAS  Google Scholar 

  6. Ito T, Okuma K, Ma XX, Yuzawa H, Hiramatsu K (2003) Insights on antibiotic resistance of Staphylococcus aureus from its whole genome: genomic island SCC. Drug Resist Updat 6:41–52

    Article  PubMed  CAS  Google Scholar 

  7. Kondo Y, Ito T, Ma XX, Watanabe S, Kreiswirth BN, Etienne J, Hiramatsu K (2007) Combination of multiplex PCRs for staphylococcal cassette chromosome mec type assignment: rapid identification system for mec, ccr, and major differences in junkyard regions. Antimicrob Agents Chemother 51:264–274

    Article  PubMed  CAS  Google Scholar 

  8. Kluytmans-Vandenbergh MF, Kluytmans JA (2006) Community-acquired methicillin-resistant Staphylococcus aureus: current perspectives. Clin Microbiol Infect 12(Suppl 1):9–15

    Article  PubMed  CAS  Google Scholar 

  9. Johnson AP, Pearson A, Duckworth G (2005) Surveillance and epidemiology of MRSA bacteraemia in the UK. J Antimicrob Chemother 56:455–462

    Article  PubMed  CAS  Google Scholar 

  10. Donnio PY, Louvet L, Preney L, Nicolas D, Avril JL, Desbordes L (2002) Nine-year surveillance of methicillin-resistant Staphylococcus aureus in a hospital suggests instability of mecA DNA region in an epidemic strain. J Clin Microbiol 40:1048–1052

    Article  PubMed  Google Scholar 

  11. Donnio PY, Oliveira DC, Faria NA, Wilhelm N, Le Coustumier A, de Lencastre H (2005) Partial excision of the chromosomal cassette containing the methicillin resistance determinant results in methicillin-susceptible Staphylococcus aureus. J Clin Microbiol 43:4191–4193

    Article  PubMed  CAS  Google Scholar 

  12. Donnio PY, Février F, Bifani P, Dehem M, Kervégant C, Wilhelm N, Gautier-Lerestif AL, Lafforgue N, Cormier M; MR-MSSA Study Group of the Collège de Bactériologie-Virologie-Hygiène des Hôpitaux de France, Le Coustumier A (2007) Molecular and epidemiological evidence for spread of multiresistant methicillin-susceptible Staphylococcus aureus strains in hospitals. Antimicrob Agents Chemother 51:4342–4350

    Article  PubMed  CAS  Google Scholar 

  13. Shore AC, Rossney AS, O’Connell B, Herra CM, Sullivan DJ, Humphreys H, Coleman DC (2008) Detection of staphylococcal cassette chromosome mec-associated DNA segments in multiresistant methicillin-susceptible Staphylococcus aureus (MSSA) and identification of Staphylococcus epidermidis ccrAB4 in both methicillin-resistant S. aureus and MSSA. Antimicrob Agents Chemother 52:4407–4419

    Article  PubMed  CAS  Google Scholar 

  14. Lindqvist M, Isaksson B, Samuelsson A, Nilsson LE, Hallgren A (2009) A clonal outbreak of methicillin-susceptible Staphylococcus aureus with concomitant resistance to erythromycin, clindamycin and tobramycin in a Swedish county. Scand J Infect Dis 41:324–333

    Article  PubMed  CAS  Google Scholar 

  15. Huletsky A, Giroux R, Rossbach V, Gagnon M, Vaillancourt M, Bernier M, Gagnon F, Truchon K, Bastien M, Picard FJ, van Belkum A, Ouellette M, Roy PH, Bergeron MG (2004) New real-time PCR assay for rapid detection of methicillin-resistant Staphylococcus aureus directly from specimens containing a mixture of staphylococci. J Clin Microbiol 42:1875–1884

    Article  PubMed  CAS  Google Scholar 

  16. Baba T, Takeuchi F, Kuroda M, Yuzawa H, Aoki K, Oguchi A, Nagai Y, Iwama N, Asano K, Naimi T, Kuroda H, Cui L, Yamamoto K, Hiramatsu K (2002) Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 359:1819–1827

    Article  PubMed  CAS  Google Scholar 

  17. Ito T, Katayama Y, Asada K, Mori N, Tsutsumimoto K, Tiensasitorn C, Hiramatsu K (2001) Structural comparison of three types of staphylococcal cassette chromosome mec integrated in the chromosome in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 45:1323–1336

    Article  PubMed  CAS  Google Scholar 

  18. Kuroda M, Ohta T, Uchiyama I, Baba T, Yuzawa H, Kobayashi I, Cui L, Oguchi A, Aoki K, Nagai Y, Lian J, Ito T, Kanamori M, Matsumaru H, Maruyama A, Murakami H, Hosoyama A, Mizutani-Ui Y, Takahashi NK, Sawano T, Inoue R, Kaito C, Sekimizu K, Hirakawa H, Kuhara S, Goto S, Yabuzaki J, Kanehisa M, Yamashita A, Oshima K, Furuya K, Yoshino C, Shiba T, Hattori M, Ogasawara N, Hayashi H, Hiramatsu K (2001) Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet 357:1225–1240

    Article  PubMed  CAS  Google Scholar 

  19. Hallin M, Denis O, Deplano A, De Mendonça R, De Ryck R, Rottiers S, Struelens MJ (2007) Genetic relatedness between methicillin-susceptible and methicillin-resistant Staphylococcus aureus: results of a national survey. J Antimicrob Chemother 59:465–472

    Article  PubMed  CAS  Google Scholar 

  20. McDougal LK, Steward CD, Killgore GE, Chaitram JM, McAllister SK, Tenover FC (2003) Pulsed-field gel electrophoresis typing of oxacillin-resistant Staphylococcus aureus isolates from the United States: establishing a national database. J Clin Microbiol 41:5113–5120

    Article  PubMed  CAS  Google Scholar 

  21. Oliveira DC, Tomasz A, de Lencastre H (2002) Secrets of success of a human pathogen: molecular evolution of pandemic clones of meticillin-resistant Staphylococcus aureus. Lancet Infect Dis 2:180–189

    Article  PubMed  CAS  Google Scholar 

  22. Petersson AC, Olsson-Liljequist B, Miörner H, Haeggman S (2010) Evaluating the usefulness of spa typing, in comparison with pulsed-field gel electrophoresis, for epidemiological typing of methicillin-resistant Staphylococcus aureus in a low-prevalence region in Sweden 2000–2004. Clin Microbiol Infect 16:456–462

    Article  PubMed  CAS  Google Scholar 

  23. Wong H, Louie L, Lo RY, Simor AE (2010) Characterization of Staphylococcus aureus isolates with a partial or complete absence of staphylococcal cassette chromosome elements. J Clin Microbiol 48:3525–3531

    Article  PubMed  CAS  Google Scholar 

  24. Desjardins M, Guibord C, Lalonde B, Toye B, Ramotar K (2006) Evaluation of the IDI-MRSA assay for detection of methicillin-resistant Staphylococcus aureus from nasal and rectal specimens pooled in a selective broth. J Clin Microbiol 44:1219–1223

    Article  PubMed  CAS  Google Scholar 

  25. Deplano A, Tassios PT, Glupczynski Y, Godfroid E, Struelens MJ (2000) In vivo deletion of the methicillin resistance mec region from the chromosome of Staphylococcus aureus strains. J Antimicrob Chemother 46:617–620

    Article  PubMed  CAS  Google Scholar 

  26. Grubb WB, Annear DI (1972) Spontaneous loss of methicillin resistance in Staphylococcus aureus at room-temperature. Lancet 2:1257

    Article  PubMed  CAS  Google Scholar 

  27. Noto MJ, Fox PM, Archer GL (2008) Spontaneous deletion of the methicillin resistance determinant, mecA, partially compensates for the fitness cost associated with high-level vancomycin resistance in Staphylococcus aureus. Antimicrob Agents Chemother 52:1221–1229

    Article  PubMed  CAS  Google Scholar 

  28. Inglis B, Matthews PR, Stewart PR (1990) Induced deletions within a cluster of resistance genes in the mec region of the chromosome of Staphylococcus aureus. J Gen Microbiol 136:2231–2239

    PubMed  CAS  Google Scholar 

  29. Poston SM, Li Saw Hee FL (1991) Genetic characterisation of resistance to metal ions in methicillin-resistant Staphylococcus aureus: elimination of resistance to cadmium, mercury and tetracycline with loss of methicillin resistance. J Med Microbiol 34:193–201

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

S. aureus control strains were kindly provided by Teruyo Ito, Juntendo University, Tokyo, Japan, and Anna Shore, Trinity College, Dublin, Ireland. We thank Andreas Matussek, Ryhov Hospital, Jönköping, Sweden, for providing us with the modified MREJ protocol. We also thank the 454 node at the Norwegian Sequencing Centre, Oslo University, Norway, for performing the 454 pyrosequencing. A final thank you goes to the Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, MD USA (the IGS Annotation Engine), for the help with the annotation of the ECT-R 2 complete genome sequence.

Funding

This work was supported by the Östergötland County Council and the Scandinavian Society for Antimicrobial Chemotherapy (SSAC) (grant number 2009-22495).

Ethical standards

This study was approved by the Regional Ethical Review Board in Linköping, Sweden.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. Lindqvist.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lindqvist, M., Isaksson, B., Grub, C. et al. Detection and characterisation of SCCmec remnants in multiresistant methicillin-susceptible Staphylococcus aureus causing a clonal outbreak in a Swedish county. Eur J Clin Microbiol Infect Dis 31, 141–147 (2012). https://doi.org/10.1007/s10096-011-1286-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-011-1286-y

Keywords

Navigation