J Med Microbiol Email Content Delivery
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
 QUICK SEARCH:   [advanced]


     


This Article
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via CrossRef
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Ma, S. H.
Right arrow Articles by Lee, J. C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Ma, S. H.
Right arrow Articles by Lee, J. C.
Agricola
Right arrow Articles by Ma, S. H.
Right arrow Articles by Lee, J. C.
J Med Microbiol 56 (2007), 866-868; DOI: 10.1099/jmm.0.46962-0
© 2007 Society for General Microbiology
ISSN 1473-5644


Correspondence

Meticillin-resistant Staphylococcus aureus clones with distinct clinical and microbiological features in a Korean community

Sang Hyuk Ma1, Yeong Seon Lee2, Seung Hoon Lee1, Han Kil Kim3, Jong Sook Jin4, Eun Kyung Shin2 and Je Chul Lee4

1 Department of Pediatrics, Changwon Fatima Hospital, Changwon, Korea

2 Division of Antimicrobial Resistance, Center for Infectious Diseases, National Institute of Health, Korea Center for Disease Control and Prevention, Seoul, Korea

3 Department of Clinical Pathology, Changwon Fatima Hospital, Changwon, Korea

4 Department of Microbiology, Kyungpook National University School of Medicine, Daegu 700-422, Korea

Correspondence
Je Chul Lee
leejc{at}knu.ac.kr


Meticillin-resistant Staphylococcus aureus (MRSA) is well established as a major pathogen in healthcare-associated infections, but in recent years it has also become increasingly common in community-acquired infections. Community-acquired MRSA (CA-MRSA) strains are characterized by the predominance of staphylococcal chromosomal cassette mec (SCCmec) type IV, the lack of multi-drug resistance, and the presence of specific toxins, including Panton-Valentine leukocidin (PVL) and occasionally exfoliative toxins. CA-MRSA has been shown to arise from diverse clones rather than from the worldwide spread of specific clones, and in Asian countries the most predominant PVL-positive CA-MRSA clone is sequence type (ST)30 (Takizawa et al., 2005; Hsu et al., 2006; Wijaya et al., 2006).

In Korea, healthcare-associated MRSA (HA-MRSA) has risen dramatically over the last decade and currently accounts for up to 70 % of S. aureus infections in most tertiary care hospitals (Kim et al., 2003; Cha et al., 2005), represented by two predominant clones, ST239 and ST5. To date, there has been no report of CA-MRSA infections in Korea, but since 2003, sporadic cases of staphylococcal scalded skin syndrome (SSSS), and skin and soft tissue infections not attributable to HA-MRSA have been recorded in Kyungnam Province, Korea. This finding prompted us to investigate the clinical and microbiological characteristics of the isolates from such infections.

From November 2004 to August 2005, 21 CA-MRSA isolates were collected from outpatients in Kyungnam Province, Korea (Table 1Go). Two isolates from patients with SSSS in 2003 were also included in the strain set. CA-MRSA was defined as an MRSA isolate recovered from a clinical culture from a patient who had no history of hospitalization or admission to a long-term care facility within one year before the MRSA-culture date. MRSA was confirmed by PCR amplification of the nuc and mecA genes (Pérez-Roth et al., 2001). Isolates were investigated for multilocus ST (Enright et al., 2000), spa gene type (Shopsin et al., 1999), SCCmec cassette group (Oliveira & de Lencastre, 2002; Chongtrakool et al., 2006) and by PFGE of SmaI digests. The presence of toxin genes eta, etb and pvl (Becker et al., 1998; Jarraud et al., 2002), and ermA and ermC (Sutcliffe et al., 1996), was investigated by PCR with specific primers. The antimicrobial susceptibility of the isolates was determined by agar dilution according to the National Committee for Clinical Laboratory Standards guidelines (NCCLS, 2003). Inducible clindamycin resistance was determined using the D-test (Schreckenberger et al., 2004).


View this table:
[in this window]
[in a new window]

 
Table 1. Clinical and microbiological characteristics of CA-MRSA infections in Kyungnam province, Korea

 
The 23 CA-MRSA isolates were classified into 3 STs, 4 spa types, 4 PFGE types and 2 SCCmec types with variants (Table 1Go); the pvl gene was not detected in any of the isolates. Ten ST89 MRSA isolates carried the SCCmec type II variant and were indistinguishable in PFGE pattern (type D). These isolates carried ccr2, class A mec, pUB110, dcs and mecI, but not kdp. SCCmec elements carrying type 2 ccr and class A mec are typical features of SCCmec type II. The etb gene was detected in 9 of the 10 ST89 isolates. A total of 11 ST72 MRSA isolates were SCCmec type IVA and PFGE type C but were subdivided into 2 spa types, t324 (3 isolates) and t664 (8 isolates). Two isolates were of ST5 but the structures of SCCmec were different from those of ST5 HA-MRSA isolates; one ST5 CA-MRSA isolate carried SCCmec type IV and the other was a SCCmec type II variant with an identical pattern to the ST89 strains.

SSSS was the most common disease presentation, accounting for 9 of the 23 (37.5 %) cases, followed by skin and soft tissue infections (impetigo and abscesses) in a further 9 patients (Table 1Go). ST89 was restricted to SSSS isolates, whereas ST72 was associated with a wide range of clinical manifestations in children and adults.

The MIC of oxacillin for all isolates ranged from 8 to 256 µg ml–1, and resistance rates to erythromycin, clindamycin, gentamicin and tetracycline were 87.0, 47.8, 34.8 and 8.7 %, respectively. A total of 6 of the 11 isolates with SCCmec type II variant were resistant to gentamicin through the integrated pUB110, with the remainder showing intermediate susceptibility (MIC 8 µg ml–1). Among the 20 erythromycin-resistant isolates, 11 isolates with SCCmec type II variant constitutively expressed ermA and were also resistant to clindamycin phenotypically, and 9 carried ermC but were susceptible to clindamycin and were positive in the D-test.

To our knowledge, this is the first report of the emergence of CA-MRSA infections in Korea. Three distinct CA-MRSA clones were identified in Kyungnam Province: ST89 SCCmec type II variant is a newly recognized genotype, while ST72 and ST5 strains are genetically identical or closely similar to HA-MRSA strains in Korea (Cha et al., 2005; Ko et al., 2005). The presence of PVL toxin and carriage of SCCmec type IV are important features of CA-MRSA strains (Vandenesch et al., 2003). However, our isolates did not carry the PVL toxin. Until now, sporadic cases of SSSS caused by ST89 MRSA have been reported in Kyungnam Province and other communities in Korea, but this ST has not been detected in isolates from healthcare-associated infections, suggesting that this strain did not originate in hospitals and spill over into the community. Analysis of Japanese CA-MRSA isolates from patients with bullous impetigo showed the predominance of ST89 and ST91, a single locus variant of ST89 (Piao et al., 2005; Takizawa et al., 2005). The Japanese strains carried the etb gene and two unclassified SCCmec types, but not the pvl gene, suggesting that the ST89 CA-MRSA clone in Korea and Japan have very similar genetic backgrounds. One possible explanation for the similarities between the Japanese clones and our strains is clonal spread between the two countries.

ST72 strains were previously found in a minority of HA-MRSA strains in Korea (Cha et al., 2005; Ko et al., 2005). They showed identical genetic backgrounds in terms of spa type, SCCmec type and PFGE patterns to those examined here from the community, indicating that they emerged from hospital reservoirs and are now widely distributed in the community. A similar migration from hospitals to the community appears to have occurred with strains of ST5 (Cha et al., 2005; Ko et al., 2005). The PVL-positive ST30 CA-MRSA clone was not detected in this survey despite its high prevalence in Asia.

ACKNOWLEDGEMENTS

This study was supported by a grant from National Institute of Health (2005), Korea Center for Disease Control and Prevention, Republic of Korea.

REFERENCES

Becker, K., Roth, R. & Peters, G. (1998). Rapid and specific detection of toxigenic Staphylococcus aureus: use of two multiplex PCR enzyme immunoassays for amplification and hybridization of staphylococcal enterotoxin genes, exfoliative toxin genes, and toxic shock syndrome toxin 1 gene. J Clin Microbiol 36, 2548–2553.[Abstract/Free Full Text]

Cha, H. Y., Moon, D. C., Choi, C. H., Oh, J. Y., Jeong, Y. S., Lee, Y. C., Seol, S. Y., Cho, D. T., Chang, H. H. & other authors (2005). Prevalence of the ST239 clone of methicillin-resistant Staphylococcus aureus and differences in antimicrobial susceptibilities of ST239 and ST5 clones identified in a Korean hospital. J Clin Microbiol 43, 3610–3614.[Abstract/Free Full Text]

Chongtrakool, P., Ito, T., Ma, X. X., Kondo, Y., Trakulsomboon, S., Tiensasitorn, C., Jamklang, M., Chavalit, T., Song, J. H. & other authors (2006). Staphylococcal cassette chromosome mec (SCCmec) typing of methicillin-resistant Staphylococcus aureus strains isolated in 11 Asian countries: a proposal for a new nomenclature for SCCmec elements. Antimicrob Agents Chemother 50, 1001–1012.[Abstract/Free Full Text]

Enright, M. C., Day, N. P., Davies, C. E., Peacock, S. J. & Spratt, B. G. (2000). Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol 38, 1008–1015.[Abstract/Free Full Text]

Hsu, L. Y., Koh, Y. L., Chlebicka, N. L., Tan, T. Y., Krishnan, P., Lin, R. T., Tee, N., Barkham, T. & Koh, T. H. (2006). Establishment of ST30 as the predominant clonal type among community-associated methicillin-resistant Staphylococcus aureus isolates in Singapore. J Clin Microbiol 44, 1090–1093.[Abstract/Free Full Text]

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, 631–641.[Abstract/Free Full Text]

Kim, H. B., Park, W. B., Lee, K. D., Choi, Y. J., Park, S. W., Oh, M., Kim, E. & Choe, K. W. (2003). Nationwide surveillance for Staphylococcus aureus with reduced susceptibility to vancomycin in Korea. J Clin Microbiol 41, 2279–2281.[Abstract/Free Full Text]

Ko, K. S., Kim, Y.-S., Song, J. H., Yeom, J. S., Lee, H., Jung, S. I., Jeong, D. R., Kim, S. W., Chang, H. H. & other authors (2005). Genotypic diversity of methicillin-resistant Staphylococcus aureus isolates in Korean hospitals. Antimicrob Agents Chemother 49, 3583–3585.[Abstract/Free Full Text]

NCCLS (2003). Methods For Dilution Antimicrobial Susceptibility Tests For Bacteria That Grow Aerobically, approved standard M7–A6. Wayne, PA: National Committee for Clinical Laboratory Standards.

Oliveira, D. C. & 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, 2155–2161.[Abstract/Free Full Text]

Pérez-Roth, E., Claverie-Martín, F., Villa, J. & Méndez-Álvarez, S. (2001). Multiplex PCR for simultaneous identification of Staphylococcus aureus and detection of methicillin and mupirocin resistance. J Clin Microbiol 39, 4037–4041.[Abstract/Free Full Text]

Piao, C., Karasawa, T., Totsuka, K., Uchiyama, T. & Kikuchi, K. (2005). Prospective surveillance of community-onset and healthcare-associated methicillin-resistant Staphylococcus aureus isolated from a university-affiliated hospital in Japan. Microbiol Immunol 49, 959–970.[Medline]

Schreckenberger, P. C., Ilendo, E. & Ristow, K. L. (2004). Incidence of constitutive and inducible clindamycin resistance in Staphylococcus aureus and coagulase-negative staphylococci in a community and a tertiary care hospital. J Clin Microbiol 42, 2777–2779.[Abstract/Free Full Text]

Shopsin, B., Gomez, M., Montgomery, S. O., Smith, D. H., Waddington, M., Dodge, D. E., Bost, D. A., Riehman, M., Naidich, S. & Kreiswirth, B. N. (1999). Evaluation of protein A gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains. J Clin Microbiol 37, 3556–3563.[Abstract/Free Full Text]

Sutcliffe, J., Grebe, T., Tait-Kamradt, A. & Wondrack, L. (1996). Detection of erythromycin-resistant determinants by PCR. Antimicrob Agents Chemother 40, 2562–2566.[Abstract]

Takizawa, Y., Taneike, I., Nakagawa, S., Oishi, T., Nitahara, Y., Iwakura, N., Ozaki, K., Takano, M., Nakayama, T. & Yamamoto, T. (2005). A Panton-Valentine leucocidin (PVL)-positive community-acquired methicillin-resistant Staphylococcus aureus (MRSA) strain, another such strain carrying a multiple-drug resistance plasmid, and other more-typical PVL-negative MRSA strains found in Japan. J Clin Microbiol 43, 3356–3363.[Abstract/Free Full Text]

Vandenesch, F., Naimi, T., Enright, M. C., Lina, G., Nimmo, G. R., Heffernan, H., Liassine, N., Bes, M., Greenland, T. & other authors (2003). Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: worldwide emergence. Emerg Infect Dis 9, 978–984.[Medline]

Wijaya, L., Hsu, L. Y. & Kurup, A. (2006). Community-associated methicillin-resistant Staphylococcus aureus: overview and local situation. Ann Acad Med Singapore 35, 479–486.[Medline]





This Article
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via CrossRef
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Ma, S. H.
Right arrow Articles by Lee, J. C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Ma, S. H.
Right arrow Articles by Lee, J. C.
Agricola
Right arrow Articles by Ma, S. H.
Right arrow Articles by Lee, J. C.


HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
INT J SYST EVOL MICROBIOL J MED MICROBIOL MICROBIOLOGY J GEN VIROL ALL SGM JOURNALS