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Clonal spreading of methicillin-resistant SCCmec Staphylococcus aureus with specific spa and dru types in central Taiwan

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Abstract

The goal of this study was to delineate the molecular characteristics of methicillin-resistant Staphylococcus aureus (MRSA) in Taiwan. Ninety-six MRSA isolates were collected from the blood cultures of different patients during the period July to December of 2008. The spa typing, staphylococcal chromosomal cassette (SCCmec) typing, mec-associated direct repeat unit (dru) copy numbers, and toxin genes (sea, seb, sec, tst, lukS/F) of each isolate were determined. Thirty-eight, 28, 18, and 12 MRSA isolates were SCCmec type II, SCCmec type III, SCCmec type IV, and SCCmec type V, respectively. Most (31/38, 81.6%) of the SCCmec type II isolates were of spa t002 with four dru repeats. Some of them also carried the sec or tst toxin gene (67.7 and 80.6%, respectively). Of the 28 SCCmec type III MRSA isolates, 15 (53.6%) were of t037 with 14 dru repeats, and all also carried the sea gene. Of the 18 SCCmec type IV MRSA isolates, 13 (72.2%) were of t437 with nine dru repeats, and ten of them also had the seb gene. Among the SCCmec type V MRSA isolates, nine were type VT. Five (55.6%) of them were of t437 with 11 dru repeats, and all contained the lukS/F gene. The clonal spreading of SCCmec MRSA strains with specific spa and dru types was found. Further longitudinal, multiple-site surveillance is required in order to define the MRSA evolution in Taiwan.

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References

  1. Lowy FD (1998) Staphylococcus aureus infections. N Engl J Med 339(8):520–532

    Article  PubMed  CAS  Google Scholar 

  2. Arvidson S, Tegmark K (2001) Regulation of virulence determinants in Staphylococcus aureus. Int J Med Microbiol 291(2):159–170

    Article  PubMed  CAS  Google Scholar 

  3. Chambers HF (2001) The changing epidemiology of Staphylococcus aureus? Emerg Infect Dis 7(2):178–182

    Article  PubMed  CAS  Google Scholar 

  4. 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  PubMed  CAS  Google Scholar 

  5. Deurenberg RH, Stobberingh EE (2008) The evolution of Staphylococcus aureus. Infect Genet Evol 8(6):747–763. doi:10.1016/j.meegid.2008.07.007

    Article  PubMed  CAS  Google Scholar 

  6. Clinical and Laboratory Standards Institute (CLSI) (2008) Performance standards for antimicrobial susceptibility testing. Eighteenth informational supplement. CLSI document M100-S18. CLSI, Wayne, PA

  7. Buck JM, Como-Sabetti K, Harriman KH, Danila RN, Boxrud DJ, Glennen A, Lynfield R (2005) Community-associated methicillin-resistant Staphylococcus aureus, Minnesota, 2000–2003. Emerg Infect Dis 11(10):1532–1538

    Article  PubMed  CAS  Google Scholar 

  8. 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(1):264–274. doi:10.1128/AAC.00165-06

    Article  PubMed  CAS  Google Scholar 

  9. Lina G, Boutite F, Tristan A, Bes M, Etienne J, Vandenesch F (2003) Bacterial competition for human nasal cavity colonization: role of Staphylococcal agr alleles. Appl Environ Microbiol 69(1):18–23. doi:10.1128/AEM.69.1.18-23.2003

    Article  PubMed  CAS  Google Scholar 

  10. Frénay HM, Bunschoten AE, Schouls LM, van Leeuwen WJ, Vandenbroucke-Grauls CM, Verhoef J, Mooi FR (1996) Molecular typing of methicillin-resistant Staphylococcus aureus on the basis of protein A gene polymorphism. Eur J Clin Microbiol Infect Dis 15(1):60–64

    Article  PubMed  Google Scholar 

  11. Harmsen D, Claus H, Witte W, Rothgänger J, Claus H, Turnwald D, Vogel U (2003) Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol 41(12):5442–5448. doi:10.1128/JCM.41.12.5442-5448.2003

    Article  PubMed  CAS  Google Scholar 

  12. 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

    PubMed  CAS  Google Scholar 

  13. Goering RV, Morrison D, Al-Doori Z, Edwards GF, Gemmell CG (2008) Usefulness of mec-associated direct repeat unit (dru) typing in the epidemiological analysis of highly clonal methicillin-resistant Staphylococcus aureus in Scotland. Clin Microbiol Infect 14(10):964–969. doi:10.1111/j.1469-0691.2008.02073.x

    Article  PubMed  CAS  Google Scholar 

  14. Zhang K, McClure JA, Elsayed S, Louie T, Conly JM (2005) Novel multiplex PCR assay for characterization and concomitant subtyping of staphylococcal cassette chromosome mec types I to V in methicillin-resistant Staphylococcus aureus. J Clin Microbiol 43(10):5026–5033. doi:10.1128/JCM.43.10.5026-5033.2005

    Article  PubMed  CAS  Google Scholar 

  15. 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. doi:10.1128/IAI.70.2.631-641.2002

    Article  PubMed  CAS  Google Scholar 

  16. Koreen L, Ramaswamy SV, Graviss EA, Naidich S, Musser JM, Kreiswirth BN (2004) spa typing method for discriminating among Staphylococcus aureus isolates: implications for use of a single marker to detect genetic micro- and macrovariation. J Clin Microbiol 42(2):792–799. doi:10.1128/JCM.42.2.792-799.2004

    Article  PubMed  CAS  Google Scholar 

  17. Strommenger B, Kettlitz C, Weniger T, Harmsen D, Friedrich AW, Witte W (2006) Assignment of Staphylococcus isolates to groups by spa typing, SmaI macrorestriction analysis, and multilocus sequence typing. J Clin Microbiol 44(7):2533–2540. doi:10.1128/JCM.00420-06

    Article  PubMed  CAS  Google Scholar 

  18. Wang JL, Wang JT, Chen SY, Chen YC, Chang SC (2010) Distribution of staphylococcal cassette chromosome mec types and correlation with comorbidity and infection type in patients with MRSA bacteremia. PLoS One 5(3):e9489. doi:10.1371/journal.pone.0009489

    Article  PubMed  Google Scholar 

  19. Chmelnitsky I, Navon-Venezia S, Leavit A, Somekh E, Regev-Yochai G, Chowers M, Shitrit P, Carmeli Y (2008) SCCmec and spa types of methicillin-resistant Staphylococcus aureus strains in Israel. Detection of SCCmec type V. Eur J Clin Microbiol Infect Dis 27(5):385–390. doi:10.1007/s10096-007-0426-x

    Article  PubMed  CAS  Google Scholar 

  20. Bartels MD, Boye K, Rhod Larsen A, Skov R, Westh H (2007) Rapid increase of genetically diverse methicillin-resistant Staphylococcus aureus, Copenhagen, Denmark. Emerg Infect Dis 13(10):1533–1540

    PubMed  CAS  Google Scholar 

  21. Enright MC, Robinson DA, Randle G, Feil EJ, Grundmann H, Spratt BG (2002) The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). Proc Natl Acad Sci U S A 99(11):7687–7692. doi:10.1073/pnas.122108599

    Article  PubMed  CAS  Google Scholar 

  22. Tristan A, Bes M, Meugnier H, Lina G, Bozdogan B, Courvalin P, Reverdy ME, Enright MC, Vandenesch F, Etienne J (2007) Global distribution of Panton–Valentine leukocidin-positive methicillin-resistant Staphylococcus aureus, 2006. Emerg Infect Dis 13(4):594–600

    Article  PubMed  CAS  Google Scholar 

  23. Vandenesch F, Naimi T, Enright MC, Lina G, Nimmo GR, Heffernan H, Liassine N, Bes M, Greenland T, Reverdy ME, Etienne J (2003) Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton–Valentine leukocidin genes: worldwide emergence. Emerg Infect Dis 9(8):978–984

    PubMed  Google Scholar 

  24. Wang JL, Wang JT, Chen SY, Hsueh PR, Kung HC, Chen YC, Chang SC (2007) Adult methicillin-resistant Staphylococcus aureus bacteremia in Taiwan: clinical significance of non-multi-resistant antibiogram and Panton–Valentine leukocidin gene. Diagn Microbiol Infect Dis 59(4):365–371. doi:10.1016/j.diagmicrobio.2007.06.021

    Article  PubMed  CAS  Google Scholar 

  25. Huang YH, Tseng SP, Hu JM, Tsai JC, Hsueh PR, Teng LJ (2007) Clonal spread of SCCmec type IV methicillin-resistant Staphylococcus aureus between community and hospital. Clin Microbiol Infect 13(7):717–724. doi:10.1111/j.1469-0691.2007.01718.x

    Article  PubMed  CAS  Google Scholar 

  26. Takano T, Higuchi W, Otsuka T, Baranovich T, Enany S, Saito K, Isobe H, Dohmae S, Ozaki K, Takano M, Iwao Y, Shibuya M, Okubo T, Yabe S, Shi D, Reva I, Teng LJ, Yamamoto T (2008) Novel characteristics of community-acquired methicillin-resistant Staphylococcus aureus strains belonging to multilocus sequence type 59 in Taiwan. Antimicrob Agents Chemother 52(3):837–845. doi:10.1128/AAC.01001-07

    Article  PubMed  CAS  Google Scholar 

  27. Boyle-Vavra S, Ereshefsky B, Wang CC, Daum RS (2005) Successful multiresistant community-associated methicillin-resistant Staphylococcus aureus lineage from Taipei, Taiwan, that carries either the novel Staphylococcal chromosome cassette mec (SCCmec) type VT or SCCmec type IV. J Clin Microbiol 43(9):4719–4730. doi:10.1128/JCM.43.9.4719-4730.2005

    Article  PubMed  CAS  Google Scholar 

  28. Wang WY, Lee SY, Chiueh TS, Lu JJ (2009) Molecular and phenotypic characteristics of methicillin-resistant and vancomycin-intermediate Staphylococcus aureus isolates from patients with septic arthritis. J Clin Microbiol 47(11):3617–3623. doi:10.1128/JCM.00539-09

    Article  PubMed  CAS  Google Scholar 

  29. Hsueh PR, Lee SY, Perng CL, Chang TY, Lu JJ (2010) Clonal dissemination of meticillin-resistant and vancomycin-intermediate Staphylococcus aureus in a Taiwanese hospital. Int J Antimicrob Agents 36(4):307–312. doi:10.1016/j.ijantimicag.2010.06.035

    Article  PubMed  CAS  Google Scholar 

  30. Valsesia G, Rossi M, Bertschy S, Pfyffer GE (2010) Emergence of SCCmec type IV and SCCmec type V methicillin-resistant Staphylococcus aureus containing the Panton–Valentine leukocidin genes in a large academic teaching hospital in central Switzerland: external invaders or persisting circulators? J Clin Microbiol 48(3):720–727. doi:10.1128/JCM.01890-09

    Article  PubMed  CAS  Google Scholar 

  31. Daum RS (2007) Clinical practice. Skin and soft-tissue infections caused by methicillin-resistant Staphylococcus aureus. N Engl J Med 357(4):380–390. doi:10.1056/NEJMcp070747

    Article  PubMed  CAS  Google Scholar 

  32. 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  PubMed  CAS  Google Scholar 

  33. Ho CM, Hsueh PR, Liu CY, Lee SY, Chiueh TS, Shyr JM, Tsao SM, Chuang YC, Yan JJ, Wang LS, Wang JH, Ho MW, Tien N, Lu JJ (2010) Prevalence and accessory gene regulator (agr) analysis of vancomycin-intermediate Staphylococcus aureus among methicillin-resistant isolates in Taiwan—SMART program, 2003. Eur J Clin Microbiol Infect Dis 29(4):383–389. doi:10.1007/s10096-009-0868-4

    Article  PubMed  CAS  Google Scholar 

  34. Swenson JM, Anderson KF, Lonsway DR, Thompson A, McAllister SK, Limbago BM, Carey RB, Tenover FC, Patel JB (2009) Accuracy of commercial and reference susceptibility testing methods for detecting vancomycin-intermediate Staphylococcus aureus. J Clin Microbiol 47(7):2013–2017. doi:10.1128/JCM.00221-09

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by grants from the National Science Council (NSC 98-2320-B-039-032-MY3), China Medical University Hospital (DMR-100-122), and China Medical University (CMU98-NTU-04), Taiwan. We thank Dr. Chao-Hung Lee for the assistance with the manuscript.

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Authors and Affiliations

  1. Department of Laboratory Medicine, China Medical University Hospital, No. 2, Yuh-Der Road, Taichung, 40447, Taiwan

    C.-M. Ho, C.-Y. Lee, N. Tien & J.-J. Lu

  2. Division of Infectious Diseases, Department of Internal Medicine, China Medical University Hospital, Taichung, Taiwan

    C.-M. Ho & M.-W. Ho

  3. Graduate Institute of Clinical Medical Science, China Medical University, Taichung, Taiwan

    C.-M. Ho & J.-J. Lu

  4. Department of Laboratory Medicine, Linkou Chang-Gung Memorial Hospital, Taoyuan, Taiwan

    J.-J. Lu

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  1. C.-M. Ho
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Correspondence to J.-J. Lu.

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Ho, CM., Ho, MW., Lee, CY. et al. Clonal spreading of methicillin-resistant SCCmec Staphylococcus aureus with specific spa and dru types in central Taiwan. Eur J Clin Microbiol Infect Dis 31, 499–504 (2012). https://doi.org/10.1007/s10096-011-1338-3

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