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
Article

Abstract

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.

References

  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. http://www.sfm-microbiologie.org/pages/?page=746&id_page=182. January 2008
  12. 12.
    British Society for Antimicrobial Chemotherapy (BSAC) (2007) BSAC Methods for Antimicrobial Susceptibility Testing. Available online at: http://bsac.org.uk/wp-content/uploads/2012/02/version_6.1.pdf
  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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