Community-acquired methicillin-resistant Staphylococcus aureus clones circulating in Belgium from 2005 to 2009: changing epidemiology

  • J. Brauner
  • M. Hallin
  • A. Deplano
  • R. De Mendonça
  • C. Nonhoff
  • R. De Ryck
  • S. Roisin
  • M. J. Struelens
  • O. Denis


The present study reports the evolution of the demographic characteristics and the molecular epidemiology of community-acquired methicillin-resistant Staphylococcus aureus (CA-MRSA) in Belgium from 2005 to 2009. Four hundred and ten CA-MRSA isolates were prospectively collected and screened for the presence of Panton–Valentin leucocidin (PVL) and toxic shock syndrome toxin 1 (TSST-1) encoding genes, while clinical information were recorded. PVL- and TSST-1-positive isolates were genotyped by pulsed-field gel electrophoresis (PFGE). Staphylococcal cassette chromosome mec (SCCmec) type, spa type and multilocus sequence type (MLST) were determined on representative isolates. One hundred and fifty-nine (39 %) isolates were PVL-positive. PVL-positive isolates were significantly more frequently isolated from skin or soft tissue than PVL-negative isolates, causing mainly subcutaneous abscesses and furuncles. Patients with PVL-positive CA-MRSA were significantly younger than patients with PVL-negative CA-MRSA. Eighty-seven percent of the PVL-positive isolates belonged to a limited number (n = 7) of PFGE types belonging to sequence types (ST) ST80, ST8, ST30, ST5, ST152, ST338 and a new ST, a single-locus variant of ST1. A temporal evolution of the distribution of these PFGE types was observed, characterised by (1) the dissemination of the ST8-SCCmecIV arcA-positive (USA300) genotype and (2) a genetic diversification. Forty-seven (11 %) strains were TSST-1-positive, of which 65 % clustered into four PFGE types, all belonging to ST5. The epidemiology of CA-MRSA in Belgium is changing, as the rapid diffusion of the USA300 clone seems to occur, together with a clonal diversification.


  1. 1.
    David MZ, Daum RS (2010) Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic. Clin Microbiol Rev 23(3):616–687CrossRefPubMedGoogle Scholar
  2. 2.
    Rasigade JP, Laurent F, Lina G, Meugnier H, Bes M, Vandenesch F et al (2010) Global distribution and evolution of Panton–Valentine leukocidin-positive methicillin-susceptible Staphylococcus aureus, 1981–2007. J Infect Dis 201(10):1589–1597CrossRefPubMedGoogle Scholar
  3. 3.
    Otter JA, French GL (2010) Molecular epidemiology of community-associated meticillin-resistant Staphylococcus aureus in Europe. Lancet Infect Dis 10(4):227–239CrossRefPubMedGoogle Scholar
  4. 4.
    Moran GJ, Krishnadasan A, Gorwitz RJ, Fosheim GE, McDougal LK, Carey RB et al (2006) Methicillin-resistant S. aureus infections among patients in the emergency department. N Engl J Med 355(7):666–674CrossRefPubMedGoogle Scholar
  5. 5.
    Witte W (2009) Community-acquired methicillin-resistant Staphylococcus aureus: what do we need to know? Clin Microbiol Infect 15(Suppl 7):17–25CrossRefPubMedGoogle Scholar
  6. 6.
    Blanco R, Tristan A, Ezpeleta G, Larsen AR, Bes M, Etienne J et al (2011) Molecular epidemiology of Panton–Valentine leukocidin-positive Staphylococcus aureus in Spain: emergence of the USA300 clone in an autochthonous population. J Clin Microbiol 49(1):433–436CrossRefPubMedGoogle Scholar
  7. 7.
    Denis O, Deplano A, De Beenhouwer H, Hallin M, Huysmans G, Garrino MG et al (2005) Polyclonal emergence and importation of community-acquired methicillin-resistant Staphylococcus aureus strains harbouring Panton–Valentine leucocidin genes in Belgium. J Antimicrob Chemother 56(6):1103–1106CrossRefPubMedGoogle Scholar
  8. 8.
    Roisin S, Nonhoff C, Denis O, Struelens MJ (2008) Evaluation of new Vitek 2 card and disk diffusion method for determining susceptibility of Staphylococcus aureus to oxacillin. J Clin Microbiol 46(8):2525–2528CrossRefPubMedGoogle Scholar
  9. 9.
    Hallin M, Maes N, Byl B, Jacobs F, De Gheldre Y, Struelens MJ (2003) Clinical impact of a PCR assay for identification of Staphylococcus aureus and determination of methicillin resistance directly from blood cultures. J Clin Microbiol 41(8):3942–3944CrossRefPubMedGoogle Scholar
  10. 10.
    Clinical and Laboratory Standard Institute (CLSI) (2006) Performance standards for antimicrobial disk susceptibility tests; Approved standard—ninth edition. CLSI document M2-A9. CLSI, WayneGoogle Scholar
  11. 11.
    Comité de l’Antibiogramme de la Société française de Microbiologie (2008) Recommandations. January 2008
  12. 12.
    British Society for Antimicrobial Chemotherapy (BSAC) (2007) BSAC Methods for Antimicrobial Susceptibility Testing. Available online at:
  13. 13.
    Jarraud S, Mougel C, Thioulouse J, Lina G, Meugnier H, Forey F et al (2002) Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect Immun 70(2):631–641CrossRefPubMedGoogle Scholar
  14. 14.
    Deplano A, Witte W, van Leeuwen WJ, Brun Y, Struelens MJ (2000) Clonal dissemination of epidemic methicillin-resistant Staphylococcus aureus in Belgium and neighboring countries. Clin Microbiol Infect 6(5):239–245CrossRefPubMedGoogle Scholar
  15. 15.
    Kondo Y, Ito T, Ma XX, Watanabe S, Kreiswirth BN, Etienne J et al (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(1):264–274CrossRefPubMedGoogle Scholar
  16. 16.
    Hallin M, Deplano A, Denis O, de Mendonça R, De Ryck R, Struelens MJ (2007) Validation of pulsed-field gel electrophoresis and spa typing for long-term, nationwide epidemiological surveillance studies of Staphylococcus aureus infections. J Clin Microbiol 45(1):127–133CrossRefPubMedGoogle Scholar
  17. 17.
    Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG (2000) Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol 38(3):1008–1015PubMedGoogle Scholar
  18. 18.
    Strommenger B, Braulke C, Pasemann B, Schmidt C, Witte W (2008) Multiplex PCR for rapid detection of Staphylococcus aureus isolates suspected to represent community-acquired strains. J Clin Microbiol 46(2):582–587CrossRefPubMedGoogle Scholar
  19. 19.
    Omoe K, Hu DL, Takahashi-Omoe H, Nakane A, Shinagawa K (2005) Comprehensive analysis of classical and newly described staphylococcal superantigenic toxin genes in Staphylococcus aureus isolates. FEMS Microbiol Lett 246(2):191–198CrossRefPubMedGoogle Scholar
  20. 20.
    Lina G, Quaglia A, Reverdy ME, Leclercq R, Vandenesch F, Etienne J (1999) Distribution of genes encoding resistance to macrolides, lincosamides, and streptogramins among staphylococci. Antimicrob Agents Chemother 43(5):1062–1066PubMedGoogle Scholar
  21. 21.
    Ng LK, Martin I, Alfa M, Mulvey M (2001) Multiplex PCR for the detection of tetracycline resistant genes. Mol Cell Probes 15(4):209–215CrossRefPubMedGoogle Scholar
  22. 22.
    Vanhoof R, Godard C, Content J, Nyssen HJ, Hannecart-Pokorni E (1994) Detection by polymerase chain reaction of genes encoding aminoglycoside-modifying enzymes in methicillin-resistant Staphylococcus aureus isolates of epidemic phage types. Belgian Study Group of Hospital Infections (GDEPIH/GOSPIZ). J Med Microbiol 41(4):282–290CrossRefPubMedGoogle Scholar
  23. 23.
    Vandendriessche S, Hallin M, Catry B, Jans B, Deplano A, Nonhoff C et al (2012) Previous healthcare exposure is the main antecedent for methicillin-resistant Staphylococcus aureus carriage on hospital admission in Belgium. Eur J Clin Microbiol Infect Dis 31(9):2283–2292CrossRefPubMedGoogle Scholar
  24. 24.
    Denis O, Jans B, Deplano A, Nonhoff C, De Ryck R, Suetens C et al (2009) Epidemiology of methicillin-resistant Staphylococcus aureus (MRSA) among residents of nursing homes in Belgium. J Antimicrob Chemother 64(6):1299–1306CrossRefPubMedGoogle Scholar
  25. 25.
    Denis O, Deplano A, Nonhoff C, Hallin M, De Ryck R, Vanhoof R et al (2006) In vitro activities of ceftobiprole, tigecycline, daptomycin, and 19 other antimicrobials against methicillin-resistant Staphylococcus aureus strains from a national survey of Belgian hospitals. Antimicrob Agents Chemother 50(8):2680–2685CrossRefPubMedGoogle Scholar
  26. 26.
    Hallin M, de Mendonça R, Denis O, Lefort A, El Garch F, Butaye P et al (2011) Diversity of accessory genome of human and livestock-associated ST398 methicillin resistant Staphylococcus aureus strains. Infect Genet Evol 11(2):290–299CrossRefPubMedGoogle Scholar
  27. 27.
    Robert J, Tristan A, Cavalié L, Decousser JW, Bes M, Etienne J et al (2011) Panton–Valentine leukocidin-positive and toxic shock syndrome toxin 1-positive methicillin-resistant Staphylococcus aureus: a French multicenter prospective study in 2008. Antimicrob Agents Chemother 55(4):1734–1739CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • J. Brauner
    • 1
  • M. Hallin
    • 1
    • 2
  • A. Deplano
    • 1
  • R. De Mendonça
    • 1
  • C. Nonhoff
    • 1
  • R. De Ryck
    • 1
  • S. Roisin
    • 1
  • M. J. Struelens
    • 1
    • 3
  • O. Denis
    • 1
  1. 1.Laboratoire de Référence MRSA-Staphylocoques, Service de MicrobiologieUniversité Libre de Bruxelles (ULB)—Hôpital ErasmeBrusselsBelgium
  2. 2.Service de MicrobiologieHôpital ErasmeBrusselsBelgium
  3. 3.Microbiology Coordination Section, Resource Management and Coordination UnitEuropean Centre for Disease Prevention and Control (ECDC)StockholmSweden

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