Skip to main content
Log in

Characteristics of the community-genotype sequence type 72 methicillin-resistant Staphylococcus aureus isolates that underlie their persistence in hospitals

  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

Panton-Valentine leukocidin-negative methicillin-resistant Staphylococcus aureus (MRSA) clone ST72, known as a major community-associated MRSA in Korea, has emerged as an important pathogen in hospitals. To understand bacterial properties that underlie transformation of this clone into a nosocomial pathogen, we compared characteristics of the community-genotype ST72 MRSA isolates with those of ST5 and ST239 MRSA, which have been predominant nosocomial MRSA clones in Korea. Several genes associated with adhesion and virulence were absent or rarely found in ST72 isolates. Many ST72 isolates (70.1%) belonged to agr group I, but the agr group of other ST72 isolates could not be determined. As indicated by d-hemolysin production, ST72 isolates expressed fully functional agr, whereas agr dysfunction was observed in ST5 and ST239 isolates. In the biofilm formation assay, no upregulation of biofilm-forming activity of ST72 MRSA was detected. However, ST72 isolates demonstrated persistence under hypotonic and desiccating conditions (survival rates 72.3% and 33.9%, respectively), which was similar to characteristics of ST5 or ST239 isolates. ST72- MRSA isolates showed low virulence, but properties of their functional agr system could facilitate their spread in hospitals. In conclusion, tolerance to stressful environments, e.g., hypotonic and dry conditions, may also contribute to survival of the community-associated MRSA clones in healthcare facilities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ando, E., Monden, K., Mitsuhata, R., Kariyama, R., and Kumon, H. 2004. Biofilm formation among methicillin-resistant Staphylococcus aureus isolates from patients with urinary tract infection. Acta Med. Okayama 58, 207–214.

    CAS  PubMed  Google Scholar 

  • Cha, J.O., Park, Y.K., Lee, Y.S., and Chung, G.T. 2011. In vitro biofilm formation and bactericidal activities of methicillin-resistant Staphylococcus aureus clones prevalent in Korea. Diagn. Microbiol. Infect. Dis. 70, 112–118.

    Article  CAS  PubMed  Google Scholar 

  • Chen, Y., Chatterjee, S.S., Porcella, S.F., Yu, Y.S., and Otto, M. 2013. Complete genome sequence of a Panton-Valentine leukocidinnegative community-associated methicillin-resistant Staphylococcus aureus strain of sequence type 72 from Korea. PLoS One 8, e72803.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, Y., Yeh, A.J., Cheung, G.Y., Villaruz, A.E., Tan, V.Y., Joo, H.S., Chatterjee, S.S., Yu, Y., and Otto, M. 2015. Basis of virulence in a Panton-Valentine leukocidin-negative community-associated methicillin-resistant Staphylococcus aureus strain. J. Infect. Dis. 211, 472–480.

    Article  PubMed  PubMed Central  Google Scholar 

  • Davis, S.L., Rybak, M.J., Amjad, M., Kaatz, G.W., and McKinnon, P.S. 2006. Characteristics of patients with healthcare-associated infection due to SCCmec type IV methicillin-resistant Staphylococcus aureus. Infect. Control Hosp. Epidemiol. 27, 1025–1031.

    Article  PubMed  Google Scholar 

  • Espinal, P., Marti, S., and Vila, J. 2012. Effect of biofilm formation on the survival of Acinetobacter baumannii on dry surfaces. J. Hosp. Infect. 80, 56–60.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jawad, A., Heritage, J., Snelling, A.M., Gascoyne-Binzi, D.M., and Hawkey, P.M. 1996. Influence of relative humidity and suspending menstrua on survival of Acinetobacter spp. on dry surfaces. J. Clin. Microbiol. 34, 2881–2887.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Joo, E.J., Chung, D.R., Ha, Y.E., Park, S.Y., Kang, S.J., Kim, S.H., Kang, C.I., Peck, K.R., Lee, N.Y., Ko, K.S., et al. 2012. Community-associated Panton-Valentine leukocidin-negative meticillin-resistant Staphylococcus aureus clone (ST72-MRSA-IV) causing healthcare-associated pneumonia and surgical site infection in Korea. J. Hosp. Infect. 81, 149–155.

    Article  PubMed  Google Scholar 

  • Kang, C.K., Cho, J.E., Choi, Y.J., Jung, Y., Kim, N.H., Kim, C.J., Kim, T.S., Song, K.H., Choe, P.G., Park, W.B., et al. 2015. agr dysfunction affects staphylococcal cassette chromosome mec type-dependent clinical outcomes in methicillin-resistant Staphylococcus aureus bacteremia. Antimicrob. Agents Chemother. 59, 3125–3132.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, S.W., Choi, C.H., Moon, D.C., Jin, J.S., Lee, J.H., Shin, J.H., Kim, J.M., Lee, Y.C., Seol, S.Y., Cho, D.T., et al. 2009. Serum resistance of Acinetobacter baumannii through the binding of factor H to outer membrane proteins. FEMS Microbiol. Lett. 301, 224–231.

    Article  CAS  PubMed  Google Scholar 

  • 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., Ki, H.K., et al. 2005. Genotypic diversity of methicillin-resistant Staphylococcus aureus isolates in Korean hospitals. Antimicrob. Agents Chemother. 49, 3583–3585.

    Article  CAS  Google Scholar 

  • Ko, K.S., Lim, S.K., Jung, S.C., Yoon, J.M., Choi, J.Y., and Song, J.H. 2011. Sequence type 72 methicillin-resistant Staphylococcus aureus isolates from humans, raw meat and soil in South Korea. J. Med. Microbiol. 60, 442–445.

    Article  CAS  PubMed  Google Scholar 

  • Li, M., Cheung, G.Y.C., Hu, J., Wang, D., Joo, H.S., DeLeo, F.R., and Otto, M. 2010. Comparative analysis of virulence and toxin expression of global community-associated methicillin-resistant Staphylococcus aureus strains. J. Infect. Dis. 202, 1866–1876.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lim, S., Chung, D.R., Baek, J.Y., Kim, S.H., Peck, K.R., Lee, N.Y., and Song, J.H. 2013. A third case of USA300 community-associated methicillin-resistant Staphylococcus aureus infection in Korea. Korean J. Intern. Med. 28, 258–260.

    Article  PubMed  PubMed Central  Google Scholar 

  • Moore, P.C. and Lindsay, J.A. 2001. Genetic variation among hospital isolates of methicillin-sensitive Staphylococcus aureus: evidence for horizontal transfer of virulence genes. J. Clin. Microbiol. 39, 2760–2767.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park, K.H., Chong, Y.P., Kim, S.H., Lee, S.O., Choi, S.H., Lee, M.S., Jeong, J.Y., Woo, J.H., and Kim, Y.S. 2015. Community-associated MRSA strain ST72-SCCmecIV causing bloodstream infections: clinical outcomes and bacterial virulence factors. J. Antimicrob. Chemother. 70, 1185–1192.

    CAS  PubMed  Google Scholar 

  • Peacock, S.J., Moore, C.E., Justice, A., Kantzanou, M., Story, L., Mackie, K., O’ Neill, G., and Day, N.P. 2002. Virulent combinations of adhesin and toxin genes in natural populations of Staphylococcus aureus. Infect. Immun. 70, 4987–4996.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saiman, L., O’ Keefe, M., Graham, P.L.3rd., Wu, F., Said-Salim, B., Kreiswirth, B., LaSala, A., Schlievert, P.M., and Della-Latta, P. 2003. Hospital transmission of community-acquired methicillinresistant Staphylococcus aureus among postpartum women. Clin. Infect. Dis. 37, 1313–1319.

    Article  PubMed  Google Scholar 

  • Sakoulas, G., Eliopoulos, G.M., Moellering, R.C.Jr., Wennersten, C., Venkataraman, L., Novick, R.P., and Gold, H.S. 2002. Accessory gene regulator (agr) locus in geographically diverse Staphylococcus aureus isolates with reduced susceptibility to vancomycin. Antimicrob. Agents Chemother. 46, 1492–1502.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schweizer, M.L., Furuno, J.P., Sakoulas, G., Johnson, J.K., Harris, A.D., Shardell, M.D., McGregor, J.C., Thom, K.A., and Perencevich, E.N. 2011. Increased mortality with accessory gene regulator (agr) dysfunction in Staphylococcus aureus among bacteremic patients. Antimicrob. Agents Chemother. 55, 1082–1087.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seybold, U., Kourbatova, E.V., Johnson, J.G., Halvosa, S.J., Wang, Y.F., King, M.D., Ray, S.M., and Blumberg, H.M. 2006. Emergence of community-associated methicillin-resistant Staphylococcus aureus USA300 genotype as a major cause of health careassociated blood stream infections. Clin. Infect. Dis. 42, 647–656.

    Article  CAS  PubMed  Google Scholar 

  • Shopsin, B., Eaton, C., Wasserman, G.A., Mathema, B., Adhikari, R.P., Agolory, S., Altman, D.R., Holzman, R.S., Kreiswirth, B.N., and Novick, R.P. 2010. Mutations in agr do not persist in natural populations of methicillin-resistant Staphylococcus aureus. J. Infect. Dis. 202, 1593–1599.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song, J.H., Hsueh, P.R., Chung, D.R., Ko, K.S., Kang, C.I., Peck, K.R., Yeom, J.S., Kim, S.W., Chang, H.H., Kim, Y.S., et al. 2011. Spread of methicillin-resistant Staphylococcus aureus between the community and the hospitals in Asian countries: an ANSORP study. J. Antimicrob. Chemother. 66, 1061–1069.

    Article  CAS  PubMed  Google Scholar 

  • Stranden, A.M., Frei, R., Adler, H., Fluckiger, U., and Widmer, A.F. 2009. Emergence of SCCmec type IVas the most common type of methicillin-resistant Staphylococcus aureus in a university hospital. Infection 37, 44–48.

    Article  CAS  PubMed  Google Scholar 

  • Sung, J.Y., Lee, J., Choi, E.H., and Lee, H.J. 2012. Changes in molecular epidemiology of community-associated and healthcareassociated methicillin-resistant Staphylococcus aureus in Korean children. Diagn. Microbiol. Infect. Dis. 74, 28–33.

    Article  CAS  PubMed  Google Scholar 

  • Valsesia, G., Rossi, M., Bertschy, S., and Pfyffer, G.E. 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, 720–727.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vidal, P.M., Trindade, P.A., Garcia, T.O., Pacheco, R.L., Costa, S.F., Reinert, C., Hiramatsu, K., Mamizuka, E.M., Garcia, C.P., and Levin, A.S. 2009. Differences between “classical” risk factors for infections caused by methicillin-resistant Staphylococcus aureus (MRSA) and risk factors for nosocomial bloodstream infections caused by multiple clones of the staphylococcal cassette chromosome mec type IVMRSA strain. Infect. Control Hosp. Epidemiol. 30, 139–145.

    Article  PubMed  Google Scholar 

  • Vuong, C., Saenz, H.L., Götz, F., and Otto, M. 2000. Impact of the agr quorum-sensing system on adherence to polystyrene in Staphylococcus aureus. J. Infect. Dis. 182, 1688–1693.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kwan Soo Ko.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Joo, EJ., Choi, JY., Chung, D.R. et al. Characteristics of the community-genotype sequence type 72 methicillin-resistant Staphylococcus aureus isolates that underlie their persistence in hospitals. J Microbiol. 54, 445–450 (2016). https://doi.org/10.1007/s12275-016-6157-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-016-6157-x

Keywords

Navigation