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Emergence of Panton-Valentine leucocidin-positive ST8-methicillin-resistant Staphylococcus aureus (USA300 clone) in Korea causing healthcare-associated and hospital-acquired bacteraemia

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Abstract

Panton-Valentine leucocidin (PVL)-positive sequence type (ST)8-MRSA-SCCmec IVa (USA300) is the epidemic strain of community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA) in North America. USA300 is extremely rare in South Korea, and PVL-negative ST72 SCCmec type IVc is the predominant CA-MRSA clone. In a multicentre, prospective cohort study of S. aureus bacteraemia, we identified PVL-positive ST8-MRSA isolates by performing multilocus sequence typing and PCR for PVL. We analyzed the clinical characteristics of patients with PVL-positive ST8-MRSA bacteraemia, and performed SCCmec, spa, and agr typing, PCR for arginine catabolic mobile element (ACME), virulence gene profiling, and pulsed-field gel electrophoresis (PFGE). Among a total of 818 MRSA isolates, we identified ten isolates of PVL-positive ST8-MRSA (USA300) (3 from Hospital D, 4 from Hospital G, and 3 from Hospital A), all of which involved exclusively healthcare-associated (5 isolates) and hospital-acquired bacteraemia (5 isolates). This strain accounted for 8~10 % of the hospital-acquired MRSA bacteraemia in Hospitals D and G. Bacteraemia of unknown origin was the most common type of infection followed by pneumonia. All the isolates were SCCmec type IVa, spa type t008, and agr group I. Eight of the isolates harboured ACME. In a PFGE analysis, four isolates were identical to the USA300 control strain, five differed by a single band, and the remaining one differed by two bands. All the isolates were pulsed-field type USA300. This is the first report of healthcare-associated and hospital-acquired bacteraemia caused by USA300 in South Korea. USA300 seems to be an emerging hospital clone in this country.

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References

  1. Chambers HF, Deleo FR (2009) Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol 7(9):629–641. doi:10.1038/nrmicro2200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. DeLeo FR, Otto M, Kreiswirth BN, Chambers HF (2010) Community-associated meticillin-resistant Staphylococcus aureus. Lancet 375(9725):1557–1568. doi:10.1016/s0140-6736(09)61999-1

    Article  PubMed  PubMed Central  Google Scholar 

  3. David MZ, Daum RS (2010) Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic. Clin Microbiol Rev 23(3):616–687. doi:10.1128/cmr.00081-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Lindsay JA (2010) Genomic variation and evolution of Staphylococcus aureus. Int J Med Microbiol 300(2–3):98–103. doi:10.1016/j.ijmm.2009.08.013

    Article  CAS  PubMed  Google Scholar 

  5. Nimmo GR (2012) USA300 abroad: global spread of a virulent strain of community-associated methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect 18(8):725–734. doi:10.1111/j.1469-0691.2012.03822.x

    Article  CAS  PubMed  Google Scholar 

  6. Kim ES, Song JS, Lee HJ, Choe PG, Park KH, Cho JH, Park WB, Kim SH, Bang JH, Kim DM, Park KU, Shin S, Lee MS, Choi HJ, Kim NJ, Kim EC, Oh MD, Kim HB, Choe KW (2007) A survey of community-associated methicillin-resistant Staphylococcus aureus in Korea. J Antimicrob Chemother 60(5):1108–1114. doi:10.1093/jac/dkm309

    Article  CAS  PubMed  Google Scholar 

  7. Lee JY, Chong YP, Kim T, Hong HL, Park SJ, Lee ES, Kim MN, Kim SH, Lee SO, Choi SH, Woo JH, Kim YS (2014) Bone and joint infection as a predictor of community-acquired methicillin-resistant Staphylococcus aureus bacteraemia: a comparative cohort study. J Antimicrob Chemother 69(7):1966–1971. doi:10.1093/jac/dku076

    Article  CAS  PubMed  Google Scholar 

  8. Park KH, Chong YP, Kim SH, Lee SO, Choi SH, Lee MS, Jeong JY, Woo JH, Kim YS (2015) Community-associated MRSA strain ST72-SCCmecIV causing bloodstream infections: clinical outcomes and bacterial virulence factors. J Antimicrob Chemother 70(4):1185–1192. doi:10.1093/jac/dku475

    CAS  PubMed  Google Scholar 

  9. Park C, Lee DG, Kim SW, Choi SM, Park SH, Chun HS, Choi JH, Yoo JH, Shin WS, Kang JH, Kim JH, Lee SY, Kim SM, Pyun BY (2007) Predominance of community-associated methicillin-resistant Staphylococcus aureus strains carrying staphylococcal chromosome cassette mec type IVA in South Korea. J Clin Microbiol 45(12):4021–4026. doi:10.1128/jcm.01147-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Park C, Lee D-G, Choi S-M, Park SH, Choi J-H, Yoo J-H, Hur JA, Shin W-S (2008) A case of perianal abscess due to Panton-Valentine leukocidin positive community-associated methicillin-resistant Staphylococcus aureus: report in Korea and literature review from the Far East. Infect Chemother 40(2):121–126

    Article  Google Scholar 

  11. Lim S, Chung DR, Baek JY, Kim SH, Peck KR, Lee NY, Song JH (2013) A third case of USA300 community-associated methicillin-resistant Staphylococcus aureus infection in Korea. Korean J Intern Med 28(2):258–260. doi:10.3904/kjim.2013.28.2.258

    Article  PubMed  PubMed Central  Google Scholar 

  12. Sohn KM, Chung DR, Baek JY, Kim SH, Joo EJ, Ha YE, Ko KS, Kang CI, Peck KR, Song JH (2012) Post-influenza pneumonia caused by the USA300 community-associated methicillin-resistant Staphylococcus aureus in Korea. J Korean Med Sci 27(3):313–316. doi:10.3346/jkms.2012.27.3.313

    Article  PubMed  PubMed Central  Google Scholar 

  13. Lee H, Kim ES, Choi C, Seo H, Shin M, Bok JH, Cho JE, Kim CJ, Shin JW, Kim TS, Song KH, Park KU, Kim BI, Kim HB (2014) Outbreak among healthy newborns due to a new variant of USA300-related meticillin-resistant Staphylococcus aureus. J Hosp Infect 87(3):145–151. doi:10.1016/j.jhin.2014.04.003

    Article  CAS  PubMed  Google Scholar 

  14. Friedman ND, Kaye KS, Stout JE, McGarry SA, Trivette SL, Briggs JP, Lamm W, Clark C, MacFarquhar J, Walton AL, Reller LB, Sexton DJ (2002) Health care—associated bloodstream infections in adults: a reason to change the accepted definition of community-acquired infections. Ann Intern Med 137(10):791–797

    Article  PubMed  Google Scholar 

  15. 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):1008–1015

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Shopsin B, Gomez M, Montgomery SO, Smith DH, Waddington M, Dodge DE, Bost DA, Riehman M, Naidich S, Kreiswirth BN (1999) Evaluation of protein A gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains. J Clin Microbiol 37(11):3556–3563

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Oliveira DC, de Lencastre H (2002) Multiplex PCR strategy for rapid identification of structural types and variants of the mec element in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 46(7):2155–2161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Shopsin B, Mathema B, Alcabes P, Said-Salim B, Lina G, Matsuka A, Martinez J, Kreiswirth BN (2003) Prevalence of agr specificity groups among Staphylococcus aureus strains colonizing children and their guardians. J Clin Microbiol 41(1):456–459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Traber KE, Lee E, Benson S, Corrigan R, Cantera M, Shopsin B, Novick RP (2008) agr function in clinical Staphylococcus aureus isolates. Microbiology 154(Pt 8):2265–2274. doi:10.1099/mic.0.2007/011874-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Lina G, Piemont Y, Godail-Gamot F, Bes M, Peter MO, Gauduchon V, Vandenesch F, Etienne J (1999) Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis 29(5):1128–1132. doi:10.1086/313461

    Article  CAS  PubMed  Google Scholar 

  21. Jarraud S, Mougel C, Thioulouse J, Lina G, Meugnier H, Forey F, Nesme X, Etienne J, Vandenesch F (2002) Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect Immun 70(2):631–641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Diep BA, Carleton HA, Chang RF, Sensabaugh GF, Perdreau-Remington F (2006) Roles of 34 virulence genes in the evolution of hospital- and community-associated strains of methicillin-resistant Staphylococcus aureus. J Infect Dis 193(11):1495–1503. doi:10.1086/503777

    Article  CAS  PubMed  Google Scholar 

  23. Campbell SJ, Deshmukh HS, Nelson CL, Bae IG, Stryjewski ME, Federspiel JJ, Tonthat GT, Rude TH, Barriere SL, Corey R, Fowler VG Jr (2008) Genotypic characteristics of Staphylococcus aureus isolates from a multinational trial of complicated skin and skin structure infections. J Clin Microbiol 46(2):678–684. doi:10.1128/jcm.01822-07

    Article  CAS  PubMed  Google Scholar 

  24. Diep BA, Gill SR, Chang RF, Phan TH, Chen JH, Davidson MG, Lin F, Lin J, Carleton HA, Mongodin EF, Sensabaugh GF, Perdreau-Remington F (2006) Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 367(9512):731–739. doi:10.1016/S0140-6736(06)68231-7

    Article  CAS  PubMed  Google Scholar 

  25. Planet PJ, LaRussa SJ, Dana A, Smith H, Xu A, Ryan C, Uhlemann AC, Boundy S, Goldberg J, Narechania A, Kulkarni R, Ratner AJ, Geoghegan JA, Kolokotronis SO, Prince A (2013) Emergence of the epidemic methicillin-resistant Staphylococcus aureus strain USA300 coincides with horizontal transfer of the arginine catabolic mobile element and speG-mediated adaptations for survival on skin. MBio 4(6):e00889–e00813. doi:10.1128/mBio.00889-13

    Article  PubMed  PubMed Central  Google Scholar 

  26. 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(11):5113–5120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Tenover FC, McDougal LK, Goering RV, Killgore G, Projan SJ, Patel JB, Dunman PM (2006) Characterization of a strain of community-associated methicillin-resistant Staphylococcus aureus widely disseminated in the United States. J Clin Microbiol 44(1):108–118. doi:10.1128/JCM.44.1.108-118.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Chuang YY, Huang YC (2013) Molecular epidemiology of community-associated meticillin-resistant Staphylococcus aureus in Asia. Lancet Infect Dis 13(8):698–708. doi:10.1016/s1473-3099(13)70136-1

    Article  PubMed  Google Scholar 

  29. Thurlow LR, Joshi GS, Clark JR, Spontak JS, Neely CJ, Maile R, Richardson AR (2013) Functional modularity of the arginine catabolic mobile element contributes to the success of USA300 methicillin-resistant Staphylococcus aureus. Cell Host Microbe 13(1):100–107. doi:10.1016/j.chom.2012.11.012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Tong SY, Davis JS, Eichenberger E, Holland TL, Fowler VG Jr (2015) Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin Microbiol Rev 28(3):603–661. doi:10.1128/cmr.00134-14

    Article  PubMed  PubMed Central  Google Scholar 

  31. Popovich KJ, Weinstein RA, Hota B (2008) Are community-associated methicillin-resistant Staphylococcus aureus (MRSA) strains replacing traditional nosocomial MRSA strains? Clin Infect Dis 46(6):787–794. doi:10.1086/528716

    Article  PubMed  Google Scholar 

  32. Seybold U, Kourbatova EV, Johnson JG, Halvosa SJ, Wang YF, King MD, Ray SM, Blumberg HM (2006) Emergence of community-associated methicillin-resistant Staphylococcus aureus USA300 genotype as a major cause of health care-associated blood stream infections. Clin Infect Dis 42(5):647–656. doi:10.1086/499815

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Y. P. Chong.

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Funding

This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (grant number: NRF-2014R1A1A2059093).

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All authors have no conflicting interests to declare.

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The Medical Review Ethics Committee of each participating hospital approved the study.

Additional information

J. Jung and E. H. Song contributed equally to this work.

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Jung, J., Song, E.H., Park, S.Y. et al. Emergence of Panton-Valentine leucocidin-positive ST8-methicillin-resistant Staphylococcus aureus (USA300 clone) in Korea causing healthcare-associated and hospital-acquired bacteraemia. Eur J Clin Microbiol Infect Dis 35, 1323–1329 (2016). https://doi.org/10.1007/s10096-016-2668-y

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  • DOI: https://doi.org/10.1007/s10096-016-2668-y

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