Journal List > Korean J Nosocomial Infect Control > v.18(2) > 1098337

Korean J Nosocomial Infect Control. 2013 Dec;18(2):51-56. Korean.
Published online December 26, 2013.
Copyright © 2013 Korean Society for Nosocomial Infection Control
Nasal Colonization and Molecular Characterization of Methicillin-Resistant Staphylococcus aureus among Hemodialysis Patients in 7 Korean Hospitals
Jae-Seok Kim,1 Sun-Hwa Lee,2 Joseph Jeong,3 Kyoung Ho Roh,4 Hae-Kyung Lee,5 Sook Jin Jang,6 Hye Soo Lee,7 Jeong-Uk Kim,8 Sung Hee Lee,9 Joon Sup Yeom,10 Sang Oh Lee,11 Jeong Sil Choi,12 So-Yeon Yoo,13 Jae Sim Jeong,14 and Mi-Na Kim15
1Department of Laboratory Medicine, Hallym University College of Medicine, Kangdong Sacred Heart Hospital, Seoul, Korea.
2Neodin Medical Institute, Seoul, Korea.
3Department of Laboratory Medicine, University of Ulsan and Ulsan University Hospital, Ulsan, Korea.
4Department of Laboratory Medicine, Korea University College of Medicine, Anam Hospital, Seoul, Korea.
5Department of Laboratory Medicine, The Catholic University of Korea College of Medicine, Uijeongbu St. Mary's Hospital, Uijeongbu, Korea.
6Department of Laboratory Medicine, Chosun University College of Medicine, Gwangju, Korea.
7Department of Laboratory Medicine, Chonbuk National University Medical School, Jeonju, Korea.
8Department of Laboratory Medicine, University of Ulsan College of Medicine and Gangnung Asan Hospital, Gangnung, Korea.
9Department of Laboratory Medicine, Hanmaeum General Hospital, Jeju, Korea.
10Department of Internal Medicine, Kangbuk Samsung Hospital, Sungkyunkwan University, School of Medicine, Seoul, Korea.
11Department of Internal Medicine, University of Ulsan College of Medicine and Asan Medical Center, Seoul, Korea.
12Nursing College, Gachon University, Incheon, Korea.
13Infection Control Office, The Catholic University of Korea College of Medicine, St. Vincent's Hospital, Suwon, Korea.
14Department of Clinical Nursing, University of Ulsan College of Medicine, Ulsan, Korea.
15Department of Laboratory Medicine, University of Ulsan College of Medicine and Asan Medical Center, Seoul, Korea.

Correspondence to: Mi-Na Kim, Department of Laboratory Medicine, University of Ulsan and Asan Medical Center, 88, Olympic-ro 43 gil, Songpa-gu, Seoul 138-736, Korea. Tel: 02-3010-4511, Fax: 02-478-0884, Email:
Received August 21, 2013; Revised October 10, 2013; Accepted October 18, 2013.



Staphylococcus aureus is a major bacteremia-causing pathogen in hemodialysis patients, frequently colonizing patient skin and mucosa. Active infection control is necessary to prevent methicillin-resistant S. aureus (MRSA) infection in hospitals; however, the spread of community-associated MRSA has recently become a concern for MRSA infection control. We evaluated the nasal colonization of MRSA among hemodialysis patients and the molecular characterization of the MRSA isolates.


Nasal swabs were obtained from 482 hemodialysis patients in 7 nationwide hospitals in November 2009, and cultured for MRSA colonization. Swabs were inoculated and cultured in 6.5% NaCl tryptic soy broth, then subcultured on MRSASelect medium (Bio-Rad, Hercules, CA) for 20-24 h. Multiplex PCR was performed to analyze staphylococcal cassette chromosome mec (SCCmec) types of MRSA isolates.


Of 482 hemodialysis patients, 57 (11.8%) carried MRSA, ranging from 6.7% to 19.0%. Among the 57 MRSA isolates, we identified 3 (5.3%) SCCmec II, 1 (1.8%) SCCmec IIA, 30 (52.6%) SCCmec IIB, 1 (1.8%) SCCmec III, 6 (10.5%) SCCmec IV, and 16 (28.1%) SCCmec IVA subtypes.


The MRSA carriage rate (11.8%) of hemodialysis patients in this study was high. The SCCmec IIB subtype, a healthcare-associated strain, was the predominant strain, although SCCmec IV isolates, typically found in community-associated MRSA infections, were also frequently observed. To prevent healthcare-associated MRSA infections in hemodialysis patients, standardized infection control measures should be performed, and efforts to reduce MRSA carriage rates should be considered.

Keywords: Colonization; Dialysis unit; Hemodialysis; Infection control; MRSA; Staphylococcus aureus


Table 1
Characteristics of methicillin-resistant Staphylococcus aureus isolates from nasal swabs of dialysis patients and nurses according to the hospitals and particular SCCmec subtypes
Click for larger image


This study was granted by Korean Centers for Disease Control and Prevention in 2009.

1. Ravani P, Palmer SC, Oliver MJ, Quinn RR, MacRae JM, Tai DJ, et al. Associations between hemodialysis access type and clinical outcomes: a systematic review. J Am Soc Nephrol 2013;24:465–473.
2. Parker MG, Doebbeling BN. The challenge of methicillin-resistant Staphylococcus aureus prevention in hemodialysis therapy. Semin Dial 2012;25:42–49.
3. Snyder GM, D'Agata EM. Novel antimicrobial-resistant bacteria among patients requiring chronic hemodialysis. Curr Opin Nephrol Hypertens 2012;21:211–215.
4. Kee SY, Park CW, Lee JE, Kwon YJ, Pyo HJ, et al. Western Dialysis Physical Association. Healthcare-associated risk factors of vancomycin-resistant Enterococci colonization among outpatients undergoing hemodialysis. Jpn J Infect Dis 2012;65:57–60.
5. van Rijen M, Bonten M, Wenzel R, Kluytmans J. Mupirocin ointment for preventing Staphylococcus aureus infections in nasal carriers. Cochrane Database Syst Rev 2008;(4):CD006216.
6. Kim HJ, Kim SH, Park WD. The difference of complications and overall survival according to the types of vascular access in hemodialysis. Korean J Med 2004;67:22–32.
7. Lee J, Kim S, Jeong J. A study of the bloodstream infections in one university hospital hemodialysis patients. Korean J Nosocomial Infect Control 2005;10:19–31.
8. Oliveira DC, de Lencastre H. Multiplex PCR strategy for rapid identification of structural types and variants of the mec element in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 2002;46:2155–2161.
9. Lina G, Piémont Y, Godail-Gamot F, Bes M, Peter MO, Gauduchon V, et al. Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis 1999;29:1128–1132.
10. Wertheim HF, Melles DC, Vos MC, van Leeuwen W, van Belkum A, Verbrugh HA, et al. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis 2005;5:751–762.
11. Lederer SR, Riedelsdorf G, Schiffl H. Nasal carriage of meticillin resistant Staphylococcus aureus: the prevalence, patients at risk and the effect of elimination on outcomes among outclinic haemodialysis patients. Eur J Med Res 2007;12:284–288.
12. Lai CF, Liao CH, Pai MF, Chu FY, Hsu SP, Chen HY, et al. Nasal carriage of methicillin-resistant Staphylococcus aureus is associated with higher all-cause mortality in hemodialysis patients. Clin J Am Soc Nephrol 2011;6:167–174.
13. Yeoh LY, Tan FL, Willis GC, Ooi ST. Methicillin-resistant Staphylococcus aureus carriage in hospitalized chronic hemodialysis patients and its predisposing factors. Hemodial Int. 2013
in press.
14. Kang YC, Tai WC, Yu CC, Kang JH, Huang YC. Methicillin-resistant Staphylococcus aureus nasal carriage among patients receiving hemodialysis in Taiwan: prevalence rate, molecular characterization and de-colonization. BMC Infect Dis 2012;12:284.
15. Uehara Y, Kuwahara-Arai K, Hori S, Kikuchi K, Yanai M, Hiramatsu K. Investigation of nasal meticillin-resistant Staphylococcus aureus carriage in a haemodialysis clinic in Japan. J Hosp Infect 2013;84:81–84.
16. Yi J, Kim EC. Microbiological Characteristics of Methicillin-resistant Staphylococcus aureus. Korean J Clin Microbiol 2010;13:1–6.
17. Johnson LB, Jose J, Yousif F, Pawlak J, Saravolatz LD. Prevalence of colonization with community-associated methicillin-resistant Staphylococcus aureus among end-stage renal disease patients and healthcare workers. Infect Control Hosp Epidemiol 2009;30:4–8.
18. Hong SK, Kim TS, Park KU, Kim JS, Kim EC. Active surveillance for multidrug-resistant organisms. Ann Clin Microbiol 2013;16:53–60.
19. Yoo JH. Could the active surveillance culture and decolonization reduce infections by nosocomial methicillin-resistant Staphylococcus aureus? Korean J Nosocomial Infect Control 2009;14:8–14.
20. Jeon JH, Kim HB. Active surveillance culture for methicillin resistant Staphylococcus aureus. Korean J Nosocomial Infect Control 2009;14:1–7.
21. Schmid H, Romanos A, Schiffl H, Lederer SR. Persistent nasal methicillin-resistant Staphylococcus aureus carriage in hemodialysis outpatients: a predictor of worse outcome. BMC Nephrol 2013;14:93.