A Study on the Concentration and Characteristics of Methicillin-resistant Staphylococci in the Indoor Air of Childcare Facilities

일부 어린이집의 실내공기 중 메치실린내성 포도알균의 오염 실태 및 특성

  • Received : 2013.09.13
  • Accepted : 2013.10.30
  • Published : 2013.10.31


Objectives: This study aims to understand the concentration, diversity, and antibiotic characteristics of staphylococci present in the indoor air of child-care facilities. Methods: Air sampling was performed from October 2012 to January 2013 in 120 child-care facilities in Seoul, Korea. Methicillin-resistant bacteria were selected from the total obtained airborne bacteria and subjected to 16S rRNA analysis for methicillin-resistant staphylococcal species determination. Identified staphylococcal strains were tested for resistance to a range of antibiotics. Results: Average total airborne bacterial concentration was $508.9{\pm}246.3CFU/m^3$. Indoor concentration of total airborne bacteria had a significant positive correlation with the $CO_2$ concentration in the child-care facilities. Methicillin-resistant staphylococci were present in 13.3% of the child-care facilities studied. A total of four species (S. epidermidis, S. cohnii, S. saprophyticus, S. sp.) and 55 strains were identified from the indoor air of the child-care facilities. Staphylococcus cohnii was the most common species (54.5%), followed by S. epidermidis (38.2%). All of the isolated staphylococcal strains exhibited high resistance to oxacillin, erythromycin, mupirocin, and ceftizoxime. Especially, S. saprophyticus strains showed more multidrug resistance to oxacillin, vancomycin, clindamycin, erythromycin, lincomycin, ceftizoxime, mupirocin, and tetracycline than did other species. Conclusion: The results of this study showed that a monitoring system for multidrug-resistant bacteria is needed in facilities for children, as the community-associated infections of these bacteria are increasing.


Methicillin-resistant staphylococci;coagulase-negative staphylococci;total airborne bacteria;child-care facilities;indoor air


  1. Cai JC, Hu YY, Zhang R, Zhou HW, Chen GX. Linezolid-resistant clinical isolates of methicillinresistant coagulase-negative staphylococci and Enterococcus faecium from China. Journal of Medical Microbiology. 2012; 61(11): 1568-1573.
  2. Ralska M, Szewczyk EM. Staphylococcus cohnii Hoemolysins-Isolation, Purification and Properties. Folia Microbiology. 2008; 53(6): 521-526.
  3. Valentin T, Leitner E, Rohn A, Zollner-Schwetz I, Hoenigl M, Salzer HJF, et al. Rifaximin intake leads to emergence of rifampin-resistant staphylococci. Journal of Infection. 2011; 62(1): 34-38.
  4. Vena A, Falcone M, Comandini E, Meledandri M, Novelli A, Campanile F, et al. Daptomycin plus trimethoprim/ sulfamethoxalzole combination therapy in post-neurosurgical meningitis caused by linezolid- resistant Staphylococcus epidermidis. Diagnostic Microbiology and Infectious Disease. 2013(1); 76: 99-102.
  5. Swenson JM, Robert Skov R, Patel JB. The cefoxitin disk test-what a clinical microbiologist needs to know. Clinical Microbiology Newsletter. 2007; 29(5): 33-40.
  6. Mammeri H, Nordmann P. Extended-spectrum cephalosporinase in enterobacteriaceae. Anti-Infective Agents Medicinal Chemistry. 2007; 6(1): 71-82.
  7. Yoo JI, Kang KS. Characterization of vancomycin intermediate Staphylococcus aureus(VISA) isolated from hospitals. Public Health Weekly Report. 2012; 5(32): 601-605.
  8. Wikipedia. /Methicillin-resistant Staphylococcus_aureus. Available: Staphylococcus_aureus[accessed 10 June 2013]
  9. Kim HS, Kim Ji. Monitoring of antimicrobial resistance on non-tertiary hospitals in Korea, 2007-2010. Public Health Weekly Report. 2012; 5(45): 853-856.
  10. Hardy KJ, Oppenheim BA, Gossain S, Gao F, Peter M, Hawkey PM. A Study of the Relationship Between Environmental Contamination with MethicillinResistant Staphylococcus aureus (MRSA) and Patients' Acquisition of MRSA. Infection Control and Hospital Epidemiology. 2006; 27(2): 127-132.
  11. Abudu L, Blair I, Fraise A, cheng KK. Methicillinresistant Staphylococuus aureus(MRSA): a community- based prevalence survey. Epidermiology and Infection. 2001; 126(3): 351-356.
  12. Benoit SR, Estivariz C, Mogdasy C, Pedreira W, Galiana A, Galiana A, et al. Community Strains of Methicillin-Resistant Staphylococcus aureus as Potential Cause of Healthcare-associated Infections, Uruguay, 2002-2004. Emerging Infectious Disease. 2008; 14(8): 1216-1223.
  13. Lis DO, Pacha JZ, Idzik D. Methicillin resistance of airborne coagulase-negative staphylococci in homes of persons having contact with a hospital environment. American Journal of Infection Control. 2009; 37(3): 177-182.
  14. Yoo JI. Monitoring of antimicrobial resistance on general hospitals in Korea. Public Health Weekly Report. 2011; 4(27): 485-487.
  15. Interface. Airborne transmission of disease in hospitals. Available: http://rsif.royalsocietypublishing. org/content/6/Suppl_6/S697.full [accessed 12 June 2013]
  16. Elsayed S, Laupland KB. Emergence gram-positive bacterial infections. Clinics Laboratory Medecine. 2004; 24(3): 587-603.
  17. Piette A, Verschraegen G. Role of coagulase-negative staphylococci in human disease. Veterinary Microbiology. 2009; 134(2): 45-54.
  18. Yoon SH, Sung TJ, Shin SH, Kim SK, Lee KH, Yoon HS. A study about clinical characteristics of methicillin resistant-coagulase negative staphylococcus infections in neonatal intensive care unit. Korean Journal of Pediatric Infectious Diseases. 2004; 11(1): 112-120.
  19. Nian H, Chu Y, Tian S, Sun, G, Ding L, Guo L, et al. First report of clinical linezolid-resistant Staphylococcus cohnii mediated by the cfr gene. African Journal of Microbiology Research. 2012; 6(23): 5043-5047.
  20. Wikipedia. Staphylococuus. Availble: pedia. org/wiki/Staphylococcus[accessed 10 June 2013]
  21. Infectionnet. Staphylococci. Available: http://infectionnet. org/notes/microorganisms/staphylococci/ [accessed 10 June 2013]
  22. Ahn GR. Study on the Concentation and Diversity of Bacteria in Indoor Air of Daycare centers. [master's thesis]. [Seoul]: Dankook University; 2010.
  23. Kim KY, Jang GY, Park JB, Kim CN, Lee KJ. Field study of characteristics of airborne bacteria distributed in the regulated public facilities. Journal of Korean Society of Occupational and Environmental Hygiene. 2006; 16(1): 1-10.
  24. Szewczyk EM, Piotrowski A, Ralska M. Predominant staphylococci in the intensive care unit of a paediatric hospital. Journal of Hospital infection. 2000; 45(2): 145-154.
  25. Qiao Y, Dong F, Song W, Wang L, Yang Y, Shen X. Hospital- and community-associated methicillinresistant Staphylococcus aureus: a 6-year surveillance study of invasive infections in Chinese children. Acta Paediatrica. 1013; 102(11): 1081-1086.
  26. Clinical Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing; 23rd informational supplement. M100-S23. Wayne, PA: Clinical Laboratory Standards Institute; 2013.
  27. Lee HY, Seong NC, Hong YS, Yoon DW, Sohn JR. Measurement on the indoor air contamination levels in darecare facilities. Korean Institute of Architecture Sustainable Environment and Building Systems. 2010; Autumn Symposium: 77-82.
  28. Park KS, Choi SG, Hong JK. The Study on the Distribution of indoor concentration of microorganism in commercial building. Architecture & Urban Research Information Center. 2006; 18(8): 620-626.
  29. Ministry of Health and welfare. Child-care Statistics 2012. Avalable: jb/sjb030301vw.jsp?PAR_MENU_ID=03&MENU_ ID=031604&page=2&CONT_SEQ=283136 [accessed 11 October 2013]
  30. Pnk A, Nurmi T, Sakminen E, Nykyri E. Infections and other inllness of chidren in day-care centers in helsinki I: Incidences and effects home and daycare center variables. Infection. 1991; 19(4): 230-236.
  31. Holmes SJ, Morrow AL, Pickering LK. Chlid-care practices: Effects of social change on the epidemiology of infectious disease and antibiotic resistance. Epidemiologic Reviews. 1996; 18(1): 10-28.
  32. Huh EH, Won DH, Moon KW. Trend in study of biological pollutants in indoor air quality in korea. Journal of Environmental Health Sci.ences. 2012; 38(4): 300-310.
  33. Hornstein M, Sautjeau-Rostoker C, Pduzzi J, Vessires A, Hong LTH, Barthlmy M, et al. Oxacillinhydrolyzing $\beta$-lactamase involved in resistance to imipenem in Acinetobacter baumannii. FEMS Microbiology Letters. 1997; 153(2): 333-339.
  34. Johnson AP, M. Warner, George RC, Boswell TC, Fraise AP, Manek N. Oxacillin-resistant pneumococci sensitive to penicillin. THE LANCET. 1993; 341(8854): 1222-1227.
  35. Koksal F, Samasti M. Antibiotic resistance patterns of coagulase-negative staphylococcus strains isolated from blood culture of septicemic patients in Turkey. Microbiology Research. 2009; 164(4): 404-410.
  36. Bouchami O, Achour W, Hassen AB. Species distribution and antibiotic sensitivity pattern of coagulasenegative Staphylococci other than Staphylococcus epidermidis isolated from various clinical specimens. African Journal of Microbiology Research. 2011; 5(110): 1298-1305.
  37. Szewczyk EM, Nowak T, Cielikowski T, Ralska M. Potential role of staphylococcus cohnii in a hospital environment. Microbial Ecology and Health and Disease. 2003; 15(1): 51-56.