Prevalence of community-associated meticillin-resistant Staphylococcus aureus and Panton–Valentine leucocidin-positive S. aureus in general practice patients with skin and soft tissue infections in the northern and southern regions of The Netherlands

  • D. Mithoe
  • M. I. A. Rijnders
  • B. M. Roede
  • E. Stobberingh
  • A. V. M. Möller


The purpose of this investigation was to determine the prevalence of community-associated meticillin-resistant Staphylococcus aureus (CA-MRSA) and Panton–Valentine leucocidin (PVL)-positive S. aureus in general practice (GP) patients with skin and soft tissue infections (SSTI) in the northern (Groningen and Drenthe) and southern (Limburg) regions of The Netherlands. Secondary objectives were to assess the possible risk factors for patients with SSTI caused by S. aureus and PVL-positive S. aureus using a questionnaire-based survey. From 2007 to 2008, wound and nose cultures were obtained from patients with SSTI in general practice. These swabs were analysed for the presence of S. aureus and the antibiotic susceptibility was determined. The presence of the PVL toxin gene was determined by polymerase chain reaction (PCR) and the genetic background with the use of spa typing. A survey was performed to detect risk factors for S. aureus infection and for the presence of PVL toxin.S. aureus was isolated from 219 out of 314 (70%) patients with SSTI, of which two (0.9%) patients were MRSA-positive. In 25 (11%) patients, the PVL toxin gene was found. A higher prevalence of PVL-positive S. aureus of patients with SSTI was found in the northern region compared to the south (p < 0.05). Regional differences were found in the spa types of PVL-positive S. aureus isolates, and for PVL-negative S. aureus isolates, the genetic background was similar in both regions. The prevalence of CA-MRSA in GP patients with SSTI in The Netherlands is low. Regional differences were found in the prevalence of PVL-positive S. aureus isolates from GP patients with SSTI. Household contacts having similar symptoms were found to be a risk factor for SSTI with S. aureus.


  1. 1.
    Moran GJ, Krishnadasan A, Gorwitz RJ et al (2006) Methicillin-resistant S. aureus infections among patients in the emergency department. New Engl J Med 355:666–674PubMedCrossRefGoogle Scholar
  2. 2.
    Gillet Y, Issartel B, Vanhems P et al (2002) Association between Staphylococcus aureus strains carrying gene for Panton–Valentine leukocidin and highly lethal necrotising pneumonia in young immunocompetent patients. Lancet 359:753–759PubMedCrossRefGoogle Scholar
  3. 3.
    Lina G, Piémont Y, Godail-Gamot F et al (1999) Involvement of Panton–Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis 29:1128–1132PubMedCrossRefGoogle Scholar
  4. 4.
    Woodin AM (1960) Purification of the two components of leucocidin from Staphylococcus aureus. Biochem J 75:158–165Google Scholar
  5. 5.
    Kuehnert MJ, Kruszon-Moran D, Hill HA et al (2006) Prevalence of Staphylococcus aureus nasal colonization in the United States, 2001–2002. J Infect Dis 193:172–179PubMedCrossRefGoogle Scholar
  6. 6.
    Dufour P, Gillet Y, Bes M et al (2002) Community-acquired methicillin-resistant Staphylococcus aureus infections in France: emergence of a single clone that produces Panton–Valentine leukocidin. Clin Infect Dis 35(7):819–824PubMedCrossRefGoogle Scholar
  7. 7.
    SWAB. NethMap 2010. Consumption of antimicrobial agents and antimicrobial resistance among medically important bacteria in the Netherlands.$FILE/Nethmap_2010_def.pdf. Accessed 16 Dec 2010
  8. 8.
    EARSS Annual Report 2008. On-going surveillance of S. pneumoniae, S. aureus, E. coli, E. faecium, E. faecalis, K. pneumoniae, P. aeruginosa. The EARSS Management Team, members of the Advisory Board, and national representatives of EARSS, Bilthoven, The Netherlands, October 2009Google Scholar
  9. 9.
    Grundmann H, Aanensen DM, van den Wijngaard CC, European Staphylococcal Reference Laboratory Working Group et al (2010) Geographic distribution of Staphylococcus aureus causing invasive infections in Europe: a molecular-epidemiological analysis. PLoS Med 7(1):e1000215PubMedCrossRefGoogle Scholar
  10. 10.
    Otter JA, French GL (2010) Molecular epidemiology of community-associated meticillin-resistant Staphylococcus aureus in Europe. Lancet Infect Dis 10(4):227–239PubMedCrossRefGoogle Scholar
  11. 11.
    Stam-Bolink EM, Mithoe D, Baas WH et al (2007) Spread of a methicillin-resistant Staphylococcus aureus ST80 strain in the community of the northern Netherlands. Eur J Clin Microbiol Infect Dis 26:723–727PubMedCrossRefGoogle Scholar
  12. 12.
    Wannet WJ, Heck ME, Pluister GN et al (2004) Panton–Valentine leukocidin positive MRSA in 2003: the Dutch situation. Euro Surveill 9(11):28–29PubMedGoogle Scholar
  13. 13.
    Wannet WJ, Spalburg E, Heck ME et al (2005) Emergence of virulent methicillin-resistant Staphylococcus aureus strains carrying Panton–Valentine leucocidin genes in The Netherlands. J Clin Microbiol 43(7):3341–3345PubMedCrossRefGoogle Scholar
  14. 14.
    Deurenberg RH, Stobberingh EE (2008) The evolution of Staphylococcus aureus. Infect Genet Evol 8(6):747–763, Epub 2008 Jul 29PubMedCrossRefGoogle Scholar
  15. 15.
    The International Classification of Primary Care ICPC-2-R, Revised second edition, WONCA International Classification Committee, Oxford University Press 2005Google Scholar
  16. 16.
    Fridkin SK, Hageman JC, Morrison M, Active Bacterial Core Surveillance Program of the Emerging Infections Program Network et al (2005) Methicillin-resistant Staphylococcus aureus disease in three communities. N Engl J Med 352(14):1436–1444PubMedCrossRefGoogle Scholar
  17. 17.
    Isenberg HD (1998) Essential procedures for clinical microbiology. ASM Press, Washington, DCGoogle Scholar
  18. 18.
    Clinical and Laboratory Standards Institute (CLSI) (2007) Performance Standards for Antimicrobial Susceptibility Testing. CLSI, Wayne, PAGoogle Scholar
  19. 19.
    BSAC, Susceptibility Testing. BSAC Standardized Disc Susceptibility Testing Method. Version 6 Jan 2007. Accessed 16 June 2010
  20. 20.
    Fuchs PC, Jones RN, Barry AL (1990) Interpretive criteria for disk diffusion susceptibility testing of mupirocin, a topical antibiotic. J Clin Microbiol 28:608–609PubMedGoogle Scholar
  21. 21.
    Toma E, Barriault D (1995) Antimicrobial activity of fusidic acid and disk diffusion susceptibility testing criteria for gram-positive cocci. J Clin Microbiol 33:1712–1715PubMedGoogle Scholar
  22. 22.
    Donker GA, Deurenberg RH, Driessen C et al (2009) The population structure of Staphylococcus aureus among general practice patients from The Netherlands. Clin Microbiol Infect 15:137–143PubMedCrossRefGoogle Scholar
  23. 23.
    Nulens E, Stobberingh EE, van Dessel H et al (2008) Molecular characterization of Staphylococcus aureus bloodstream isolates collected in a Dutch University Hospital between 1999 and 2006. J Clin Microbiol 46:2438–2441PubMedCrossRefGoogle Scholar
  24. 24.
    Deurenberg RH, Vink C, Driessen C et al (2004) Rapid detection of Panton–Valentine leukocidin from clinical isolates of Staphylococcus aureus strains by real-time PCR. FEMS Microbiol Lett 240:225–228PubMedCrossRefGoogle Scholar
  25. 25.
    Wertheim HF, Vos MC, Boelens HA et al (2004) Low prevalence of methicillin-resistant Staphylococcus aureus (MRSA) at hospital admission in the Netherlands: the value of search and destroy and restrictive antibiotic use. J Hosp Infec 56:321–325CrossRefGoogle Scholar
  26. 26.
    RJ Kenens, L Hingstman. Netherlands Institute for Health Services Research (NIVEL). Cijfers uit de registratie van huisartsen: peiling 2005. Accessed 16 June 2010
  27. 27.
    Bartelds AIM. Netherlands Institute for Health Services Research (NIVEL). Continuous morbidity registration sentinel at Dutch sentinel stations, 2003. Accessed 16 June 2010
  28. 28.
    SWAB. NethMap 2005. Consumption of antimicrobial agents and antimicrobial resistance among medically important bacteria in the Netherlands.$FILE/Nethmap%202005.pdf. Accessed 16 June 2010
  29. 29.
    Holmes A, Ganner M, McGuane S et al (2005) Staphylococcus aureus isolates carrying Panton–Valentine leucocidin genes in England and Wales: frequency, characterization, and association with clinical disease. J Clin Microbiol 43:2384–2390PubMedCrossRefGoogle Scholar
  30. 30.
    Tristan A, Bes M, Meugnier H et al (2007) Global distribution of Panton–Valentine leukocidin-positive methicillin-resistant Staphylococcus aureus, 2006. Emerg Infect Dis 13(4):594–600PubMedCrossRefGoogle Scholar
  31. 31.
    Deurenberg RH, Nulens E, Valvatne H (2009) Cross-border dissemination of methicillin-resistant Staphylococcus aureus, Euregio Meuse-Rhin region. Emerg Infect Dis 15(5):727–734PubMedCrossRefGoogle Scholar
  32. 32.
    Calfee DP, Durbin LJ, Germanson TP et al (2003) Spread of methicillin-resistant Staphylococcus aureus (MRSA) among household contacts of individuals with nosocomially acquired MRSA. Infect Control Hosp Epidemiol 24(6):422–426PubMedCrossRefGoogle Scholar
  33. 33.
    Johansson PJ, Gustafsson EB, Ringberg H (2007) High prevalence of MRSA in household contacts. Scand J Infect Dis 39(9):764–768PubMedCrossRefGoogle Scholar
  34. 34.
    Enright MC, Robinson DA, Randle G et al (2002) The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). Proc Natl Acad Sci USA 99(11):7687–7692PubMedCrossRefGoogle Scholar
  35. 35.
    Mollema FP, Richardus JH, Behrendt M et al (2010) Transmission of methicillin-resistant Staphylococcus aureus to household contacts. J Clin Microbiol 48(1):202–207, Epub 2009 Nov 18PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • D. Mithoe
    • 1
    • 2
  • M. I. A. Rijnders
    • 3
  • B. M. Roede
    • 4
  • E. Stobberingh
    • 3
  • A. V. M. Möller
    • 1
    • 2
  1. 1.Laboratory for Infectious DiseasesGroningenThe Netherlands
  2. 2.Martini HospitalGroningenThe Netherlands
  3. 3.Department of Medical MicrobiologyMaastricht University Medical Centre, School for Public Health and Primary Care (CAPHRI)MaastrichtThe Netherlands
  4. 4.The National Institute for Public Health and the EnvironmentBilthovenThe Netherlands

Personalised recommendations