MRSA and the environment: implications for comprehensive control measures

Review

Abstract

Environmental contamination with methicillin-resistant Staphylococcus aureus (MRSA) is established soon after colonized or infected patients become resident. There are many studies that detail the mechanisms of spread and environmental survival of methicillin-susceptible Staphylococcus aureus (MSSA); this knowledge translates directly into the same findings for MRSA. The potential ubiquity of MRSA in a health-care setting poses challenges for decontamination. Whereas patients and medical staff are important sources for MRSA spread, the environmental burden may contribute significantly in various contexts. Effective control measures must therefore include consideration for MRSA in the environment.

References

  1. 1.
    Colbeck JC (1960) Environmental aspects of staphylococcal infections acquired in hospitals. 1. The hospital environment–its place in the hospital staphylococcus infections problem. Am J Public Health 50:468–473CrossRefGoogle Scholar
  2. 2.
    Cimolai N (2002) Are all MRSA made equal? Can J Microbiol 48:560–566PubMedGoogle Scholar
  3. 3.
    Shooter RA, Smith MA, Griffiths JD, Brown MEA, Williams REO, Rippon JE, Jevons MP (1958) Spread of staphylococci in a surgical ward. BMJ 1:607–613PubMedGoogle Scholar
  4. 4.
    Williams REO, Blowers R, Garrod LP, Shooter RA (1960) Hospital infection: causes and prevention. Year Book Publishers, Inc., ChicagoGoogle Scholar
  5. 5.
    Williams REO (1966) Epidemiology of airborne staphylococcal infection. Bacteriol Rev 30:660–672PubMedGoogle Scholar
  6. 6.
    Williams REO (1967) Spread of airborne bacteria pathogenic for man. In: Gregory PH, Monteith JL (eds) Airborne microbes. Cambridge University Press, Cambridge, EnglandGoogle Scholar
  7. 7.
    Hare R, Ridley M (1958) Further studies on the transmission of Staphylococcus aureus. BMJ 1:69–73PubMedGoogle Scholar
  8. 8.
    White A (1961) Relation between quantitative nasal cultures and dissemination of staphylococci. J Lab Clin Med 58:273–277PubMedGoogle Scholar
  9. 9.
    Speers R Jr, Bernard H, O’Grady F, Shooter RA (1965) Increased dispersal of skin bacteria into the air after shower baths. Lancet i:478–480Google Scholar
  10. 10.
    Noble WC, Davies RR (1965) Studies on the dispersal of staphylococci. J Clin Pathol 18:16–19PubMedGoogle Scholar
  11. 11.
    Solberg CO (2000) Spread of Staphylococcus aureus in hospitals: causes and prevention. Scand J Infect Dis 32:587–595PubMedGoogle Scholar
  12. 12.
    Hare R, Thomas CGA (1956) The transmission of Staphylococcus aureus. BMJ 2:840–844PubMedGoogle Scholar
  13. 13.
    Mortimer EA, Wolinsky E, Gonzaga AJ, Rammelkamp CH (1966) Role airborne transmission in staphylococcal infections. BMJ 1:319–322PubMedCrossRefGoogle Scholar
  14. 14.
    Noble WC (1962) The dispersal of staphylococci in hospital wards. J Clin Pathol 15:552–558PubMedGoogle Scholar
  15. 15.
    Hambraeus A (1973) Transfer of Staphylococcus aureus via nurses’ uniforms. J Hyg 71:799–814Google Scholar
  16. 16.
    Lidwell OM, Brock B, Shooter RA, Cooke EM, Thomas GE (1975) Airborne infection in a fully air-conditioned hospital. IV. Airborne dispersal of Staphylococcus aureus and its nasal acquisition by patients. . J Hyg 75:445–474Google Scholar
  17. 17.
    Perry C, Marshall R, Jones E (2001) Bacterial contamination of uniforms. J Hosp Infect 48:238–241PubMedGoogle Scholar
  18. 18.
    Bethune DW, Blowers R, Parker M, Pask EA (1965) Dispersal of Staphylococcus aureus by patients and surgical staff. Lancet i:480–483Google Scholar
  19. 19.
    Solberg CO (1965) A study of carriers of Staphylococcus aureus with special regard to quantitative bacterial estimations. Acta Med Scand 178(Suppl. 436):1–96Google Scholar
  20. 20.
    Solberg CO, Bruun JN, Boe J (1972/73) Aerial dissemination of Staphylococcus aureus by hospital patients: causes and prevention. Prevent 1:43–50Google Scholar
  21. 21.
    Walter CW, Kundsin RB, Shilkret MA, Day MM (1958–1959) The spread of staphylococci to the environment. Antibiot Annu 6:952–957Google Scholar
  22. 22.
    Reiss-Levy E, McAllister E (1979) Pillows spread methicillin-resistant staphylococci. Med J Aust 39:92Google Scholar
  23. 23.
    Noble WC, Lidwell OM, Kingston D (1963) The size distribution of airborne particles carrying micro-organisms. J Hyg 61:385–391Google Scholar
  24. 24.
    Davies RR, Noble WC (1963) Dispersal of bacteria on desquamated skin. Lancet i:1111Google Scholar
  25. 25.
    Duguid JP, Wallace AT (1948) Air infection with dust liberated from clothing. Lancet ii:845–849Google Scholar
  26. 26.
    Lidwell OM, Lowbury EJ (1950) The survival of bacteria in dust. II. The effect of atmospheric humidity on the survival of bacteria in dust. J Hyg 48:21–27Google Scholar
  27. 27.
    Davies RR, Noble WC (1962) Dispersal of bacteria on desquamated skin. Lancet ii:1295–1297Google Scholar
  28. 28.
    Lidwell OM, Davies J, Payne RW, Newman P, Williams REO (1971) Nasal acquisition of Staphylococcus aureus in partly divided wards. J Hyg 69:113–121Google Scholar
  29. 29.
    Shiomori T, Miyamoto H, Makishima K (2001) Significance of airborne transmission of methicillin-resistant Staphylococcus aureus in an otolaryngology-head and neck surgery unit. Arch Otolaryngol Head Neck Surg 127:644–648PubMedGoogle Scholar
  30. 30.
    Shiomori T, Miyamoto H, Makishima K, Yoshida M, Fujiyoshi T, Udaka T, Inaba T, Hiraki N (2002) Evaluation of bedmaking-related airborne and surface methicillin-resistant Staphylococcus aureus contamination. J Hosp Infect 50:30–35PubMedGoogle Scholar
  31. 31.
    Sherertz RJ, Reagan DR, Hampton KD et al (1996) A cloud adult: the Staphylococcus aureus-virus interaction revisited. Ann Intern Med 124:539–547Google Scholar
  32. 32.
    Voss A (2007) Preventing the spread of MRSA. BMJ 329:521Google Scholar
  33. 33.
    Cree RGA, Aleljung P, Paulsson M, Witte W, Noble WC, Ljung A, Wadstrom T (1994) Cell surface hydrophobicity and adherence to extra-cellular matrix proteins in two collections of methicillin-resistant Staphylococcus aureus. Epidemiol Infect 112:307–314PubMedGoogle Scholar
  34. 34.
    Beard-Pegler MA, Stubbs E, Vickery AM (1988) Observations on the resistance to drying to staphylococcal strains. J Med Microbiol 26:251–255PubMedGoogle Scholar
  35. 35.
    Conner-Kerr TA, Sullivan PK, Gaillard J, Franklin ME, Jones RM (1998) The effects of ultraviolet radiation on antibiotic-resistant bacteria in vitro. Ostomy/Wound Management 44:50–56PubMedGoogle Scholar
  36. 36.
    McDade JJ, Hall LB (1963) Survival of Staphylococcus aureus in the environment. I. Exposure on surfaces. Am J Hyg 78:330–337PubMedGoogle Scholar
  37. 37.
    Wagenvoort JHT, Penders RJR (1997) Long-term in-vitro survival of an epidemic MRSA phage-group III-29 strain. J Hosp Infect 35:322–325PubMedGoogle Scholar
  38. 38.
    Wagenvoort JHT, Sluijsmans W, Penders RJR (2000) Better environmental survival of outbreak vs. sporadic MRSA isolates. J Hosp Infect 45:231–234PubMedGoogle Scholar
  39. 39.
    Duckworth GJ, Jordens JZ (1990) Adherence and survival properties of an epidemic methicillin-resistant strain of Staphylococcus aureus compared with those of methicillin-sensitive strains. J Med Microbiol 32:195–200PubMedGoogle Scholar
  40. 40.
    Farrington M, Brenwald N, Haines D, Walpole E (1992) Resistance to desiccation and skin fatty acids in outbreak strains of methicillin-resistant Staphylococcus aureus. J Med Microbiol 36:56–60PubMedGoogle Scholar
  41. 41.
    Rountree PM (1963) The effect of dessication on the viability of Staphylococcus aureus. J Hyg 61:265–272Google Scholar
  42. 42.
    Lacey RW, Barr KW, Barr VE, Inglis TJ (1986) Properties of methicillin-resistant Staphylococcus aureus colonizing patients in a burns unit. J Hosp Infect 7:137–148PubMedGoogle Scholar
  43. 43.
    Hardy KJ, Oppenheim BA, Gossain S, Gao F, Hawkey PM (2006) A study of the relationship between environmental contamination with methicillin-resistant Staphylococcus aureus (MRSA) and patients’ acquisition of MRSA. Infect Control Hosp Epidemiol 27:127–132PubMedGoogle Scholar
  44. 44.
    Dietze B, Rath A, Wendt C, Martiny H (2001) Survival of MRSA on sterile goods packaging. J Hosp Infect 49:255–261PubMedGoogle Scholar
  45. 45.
    Hirai Y (1991) Survival of bacteria under dry conditions; from a viewpoint of nosocomial infections. J Hosp Infect 19:191–200PubMedGoogle Scholar
  46. 46.
    Huang R, Mehta S, Weed D, Price CS (2006) Methicillin-resistant Staphylococcus aureus survival on hospital fomites. Infect Control Hosp Epidemiol 27:1267–1269PubMedGoogle Scholar
  47. 47.
    Oie S, Kamiya A (1996) Survival of methicillin-resistant Staphylococcus aureus (MRSA) on naturally contaminated dry mops. J Hosp Infect 34:145–149PubMedGoogle Scholar
  48. 48.
    Tolba O, Loughrey A, Goldsmith CE, Millar BC, Rooney PJ, Moore JE (2007) Survival of epidemic strains of nosocomial- and community-acquired methicillin-resistant Staphylococcus aureus on coins. Am J Infect Control 35:342–346PubMedGoogle Scholar
  49. 49.
    Noyce JO, Michels H, Keevil CW (2006) Potential use of copper surfaces to reduce survival of epidemic meticillin-resistant Staphylococcus aureus in the healthcare environment. J Hosp Infect 63:289–297PubMedGoogle Scholar
  50. 50.
    Anderson JD, Cox CS (1967) Microbial survival. In: Gregory PH, Monteith JL (eds) Airborne Microbes. Cambridge University Press, Cambridge, EnglandGoogle Scholar
  51. 51.
    Hinton NA, Maltman, Orr JH (1960) The effect of desiccation on the ability of Staphylococcus pyogenes to produce disease in mice. Am J Hyg 72:343–350PubMedGoogle Scholar
  52. 52.
    Allen KD, Anson JJ, Parsons LA, Frost NG (1997) Staff carriage of methicillin-resistant Staphylococcus aureus (EMRSA 15) and the home environment: a case report. J Hosp Infect 35:307–311PubMedGoogle Scholar
  53. 53.
    Anderson RL, Mackel DC, Stoler BS, Mallison GF (1982) Carpeting in hospitals: an epidemiological evaluation. J Clin Microbiol 15:408–415PubMedGoogle Scholar
  54. 54.
    Banerjee D, Fraise D, Chana K (1999) Writing pens are an unlikely vector of cross-infection with methicillin-resistant Staphylococcus aureus (MRSA). J Hosp Infect 43:73–75PubMedGoogle Scholar
  55. 55.
    Beamer JER, Cox RA (1999) MRSA contamination of a laryngoscope blade: a potential vector for cross infection. Anaesthesia 54:1007–1024Google Scholar
  56. 56.
    Bitar CM, Mayhall CG, Lamb VA, Bradshaw TJ, Spadora AC, Dalton HP (1987) Outbreak due to methicillin- and rifampin-resistant Staphylococcus aureus: epidemiology and eradication of the resistant strain from the hospital. Infect Control 8:15–23PubMedGoogle Scholar
  57. 57.
    Blythe D, Keenlyside D, Dawson SJ, Galloway A (1998) Environmental contamination due to methicillin-resistant Staphylococcus aureus (MRSA). J Hosp Infect 38:67–70PubMedGoogle Scholar
  58. 58.
    Boyce JM, Landry A, Deetz TR, DuPont HL (1981) Epidemiologic studies of an outbreak of nosocomial methicillin-resistant Staphylococcus aureus infections. Infect Control 2:110–116PubMedGoogle Scholar
  59. 59.
    Boyce JM, Potter-Bynoe G, Chenevert C, King T (1997) Environmental contamination due to methicillin-resistant Staphylococcus aureus: possible infection control implications. Infect Control Hosp Epidemiol 18:622–627PubMedGoogle Scholar
  60. 60.
    Bures S, Fishbain JT, Uyehara CFT, Parker JM, Berg BW (2000) Computer keyboards and faucet handles as reservoirs of nosocomial pathogens in the intensive care unit. Am J Infect Control 28:465–470PubMedGoogle Scholar
  61. 61.
    Cohen HA, Amir J, Matalon A, Mayan R, Beni S, Barzilai A (1997) Stethoscopes and otoscopes–a potential vector of infection? Family Practice 14:446–449PubMedGoogle Scholar
  62. 62.
    Cookson B, Peters B, Webster M, Phillips I, Rahman M, Noble W (1989) Staff carriage of epidemic methicillin-resistant Staphylococcus aureus. J Clin Microbiol 27:1471–1476PubMedGoogle Scholar
  63. 63.
    Crossley K, Landesman B, Zaske D (1979) An outbreak of infections caused by strains of Staphylococcus aureus resistant to methicillin and aminoglycosides. II. Epidemiologic studies. J Infect Dis 139:280–287PubMedGoogle Scholar
  64. 64.
    Devine J, Cooke RPD, Wright EP (2001) Is methicillin-resistant Staphylococcus aureus (MRSA) contamination of ward-based computer terminals a surrogate marker for nosocomial MRSA transmission and handwashing compliance? J Hosp Infect 48:72–75PubMedGoogle Scholar
  65. 65.
    Everett ED, McNitt TR, Rahm AE, Stevens DL, Peterson HE (1978) Epidemiologic investigation of methicillin resistant Staphylococcus aureus in a burn unit. Mil Med 143:165–167PubMedGoogle Scholar
  66. 66.
    Farrell AM, Shanson DC, Ross JS, Roberts NM, Fry C, Cream JJ, Staughton RCD, Bunker CB (1998) An outbreak of methicillin-resistant Staphylococcus aureus (MRSA) in a dermatology day-care unit. Clin Exp Dermatol 23:249–253PubMedGoogle Scholar
  67. 67.
    Fitzpatrick F, Murphy OM, Brady A, Prout S, Fenelon LE (2000) A purpose built MRSA cohort unit. J Hosp Infect 46:271–279PubMedGoogle Scholar
  68. 68.
    French G, Otter JA, Shannon KP, Adams NMT, Watling D, Parks MJ (2004) Tackling contamination of the hospital environment by methicillin-resistant Staphylococcus aureus (MRSA): a comparison between conventional terminal cleaning an hydrogen peroxide vapour decontamination. J Hosp Infect 57:31–37PubMedGoogle Scholar
  69. 69.
    Kumari DNP, Haji TC, Keer V, Hawkey PM, Duncanson V, Flower E (1998) Ventilation grilles as a potential source of methicillin-resistant Staphylococcus aureus causing an outbreak in an orthopedic ward at a district general hospital. J Hosp Infect 39:127–133PubMedGoogle Scholar
  70. 70.
    Layton MC, Perez M, Heald P, Patterson JE (1993) An outbreak of mupirocin-resistant Staphylococcus aureus on a dermatology ward associated with an environmental reservoir. Infect Control Hosp Epidemiol 14:369–375PubMedGoogle Scholar
  71. 71.
    Lemmen SW, Hafner H, Zolldann D, Stanzel S, Lutticken R (2004) Distribution of multi-resistant Gram-negative versus Gram-positive bacteria in the hospital inanimate environment. J Hosp Infect 56:191–197PubMedGoogle Scholar
  72. 72.
    Lemmen SW, Hafner H, Zolldann D, Amedick G, Lutticken R (2001) Comparison of two sampling methods for the detection of Gram-positive and Gram-negative bacteria in the environment: moistened swabs versus Rodac plates. Int J Hyg Environ Health 203:245–248PubMedGoogle Scholar
  73. 73.
    Loeffler A, Boag AK, Sung J, Lindsay JA, Guardabassi L, Dalsgaard A, Smith H, Stevens KB, Lloyd DH (2005) Prevalence of methicillin-resistant Staphylococcus aureus among staff and pets in a small animal referral hospital in the UK. J Antimicrob Chemother 56:692–697PubMedGoogle Scholar
  74. 74.
    Mitsuda T, Arai K, Fujita S, Yokota S (1995) Epidemiological analysis of strains of methicillin-resistant Staphylococcus aureus (MRSA) infection in the nursery; prognosis of MRSA carrier infants. J Hosp Infect 31:123–134PubMedGoogle Scholar
  75. 75.
    Moore EP, Williams EW (1991) A maternity hospital outbreak of methicillin-resistant Staphylococcus aureus. J Hosp Infect 19:5–16PubMedGoogle Scholar
  76. 76.
    Ndawula EM, Brown L (1991) Mattresses as reservoirs of epidemic methicillin-resistant Staphylococcus aureus. Lancet i:488–489Google Scholar
  77. 77.
    Nishijima S, Sugimachi T, Higashida T, Asada Y, Okuda K, Murata K (1992) An epidemiological study of methicillin-resistant Staphylococcus aureus (MRSA) isolated from medical staff, inpatients, and hospital environment in one ward at our hospital. J Dermatol 19:356–361PubMedGoogle Scholar
  78. 78.
    Prevost G, Pottecher B, Dahlet M, Bientz M, Mantz JM, Piemont Y (1991) Pulsed field gel electrophoresis as a new epidemiological tool for monitoring methicillin-resistant Staphylococcus aureus in an intensive care unit. J Hosp Infect 17:255–269PubMedGoogle Scholar
  79. 79.
    Rampling A, Wiseman S, Davis L, Hyett AP, Walbridge AN, Payne GC, Cornaby AJ (2001) Evidence that hospital hygiene is important in the control of methicillin-resistant Staphylococcus aureus. J Hosp Infect 49:109–116PubMedGoogle Scholar
  80. 80.
    Rao N, Jacobs S, Joyce L (1988) Cost-effective eradication of an outbreak of methicillin-resistant Staphylococcus aureus in a community teaching hospital. Infect Control Hosp Epidemiol 9:255–260PubMedGoogle Scholar
  81. 81.
    Rimland D (1985) Nosocomial infections with methicillin and tobramycin resistant Staphylococcus aureus–implications of physiotherapy in hospital-wide dissemination. Am J Med Sci 290:91–97PubMedGoogle Scholar
  82. 82.
    Saiman L, O’Keefe M, Graham PL III, Wu F, Said-Salim B, Kreiswirth B, LaSala A, Schlievert PM, Della-Latta P (2003) Hospital transmission of community-acquired methicillin-resistant Staphylococcus aureus among postpartum women. Clin Infect Dis 37:1313–1319PubMedGoogle Scholar
  83. 83.
    Schultsz C, Meester HHM, Kranenburg AMH, Savelkoul PHM, Boeijen-Donkers LEA, Kaiser AM, de Bree R, Snow GB, Vandenbroucke-Grauls CJME (2003) Ultra-sonic nebulizers as a potential source of methicillin-resistant Staphylococcus aureus causing an outbreak in a university tertiary care hospital. J Hosp Infect 55:269–275PubMedGoogle Scholar
  84. 84.
    Smith MA, Mathewson JJ, Ulert IA, Scerpella EG, Ericsson CD (1996) Contaminated stethoscopes revisited. Arch Intern Med 156:82–84PubMedGoogle Scholar
  85. 85.
    Walsh TJ, Vlahov D, Hansen SL, Sonnenberg E, Khabbaz R, Gadacz T, Standiford HC (1987) Prospective microbiologic surveillance in control of nosocomial methicillin-resistant Staphylococcus aureus. Infect Control 8:7–14PubMedGoogle Scholar
  86. 86.
    Ward TT, Winn RE, Hartstein AI, Sewell DL (1981) Observations relating to an inter-hospital outbreak of methicillin-resistant Staphylococcus aureus: role of antimicrobial therapy in infection control. Infect Control 2:453–459PubMedGoogle Scholar
  87. 87.
    Webster J, Faoagali JL (1990) Endemic methicillin-resistant Staphylococcus aureus in a special care baby unit: a 2 year review. J Pediatr Child Health 26:160–163Google Scholar
  88. 88.
    Wright IMR, Orr H, Porter C (1995) Stethoscope contamination in the neonatal intensive care unit. J Hosp Infect 29:65–68PubMedGoogle Scholar
  89. 89.
    French G, Rayner D, Branson M, Walsh M (1998) Contamination of doctors’ and nurses’ pens with nosocomial pathogens. Lancet 351:213PubMedGoogle Scholar
  90. 90.
    Oie S, Hosokawa I, Kamiya (2002) Contamination of room door handles by methicillin-resistant Staphylococcus aureus. J Hosp Infect 51:140–143PubMedGoogle Scholar
  91. 91.
    Oie S, Kamiya A (1998) Contamination of environmental surfaces by methicillin-resistant Staphylococcus aureus (MRSA). Biomed Lett 57:115–119Google Scholar
  92. 92.
    Wagenvoort JHT, De Brauwer EIGB, Sijstermans MLH (2002) MRSA decontamination of paper-containing objects. J Hosp Infect 51:74PubMedGoogle Scholar
  93. 93.
    Bernard L, Kereveur A, Durand D, Gonot J, Goldstein F, Mainardi JL, Acar J, Carlet J (1999) Bacterial contamination of hospital physicians’ stethoscopes. Infect Control Hosp Epidemiol 20:626–628PubMedGoogle Scholar
  94. 94.
    Henderson RJ, Williams REO (1963) Nasal carriage of staphylococci and post-operative staphylococcal wound infection. J Clin Pathol 16:452–456PubMedGoogle Scholar
  95. 95.
    Ayliffe GAJ, Collins BJ, Lowbury EJL, Babb JR, Lilly HA (1967) Ward floors and other surfaces as reservoirs of hospital infection. J Hyg 65:515–536Google Scholar
  96. 96.
    Ayliffe GAJ, Collines BJ, Lowbury EJL (1966) Cleaning and disinfection of hospital floors. BMJ 2:442–445PubMedGoogle Scholar
  97. 97.
    Bradley SF, Terpenning MS, Ramsey MA, Zarins LT, Jorgensen KA, Sottile WS, Schaberg DR, Kauffman CA (1991) Methicillin-resistant Staphylococcus aureus: colonization and infection in a long-term care facility. Ann Intern Med 115:417–422PubMedGoogle Scholar
  98. 98.
    Cotterill S, Evans R, Fraise AP (1996) An unusual source for an outbreak of methicillin-resistant Staphylococcus aureus on an intensive care unit. J Hosp Infect 32:207–216PubMedGoogle Scholar
  99. 99.
    Danforth D, Nicolle LE, Hume K, Alfieri N, Sims H (1987) Nosocomial infections on nursing units with floors cleaned with a disinfectant compared with detergent. J Hosp Infect 10:229–235PubMedGoogle Scholar
  100. 100.
    Farrington M, Ling J, Ling T, French GL (1990) Outbreaks of infection with methicillin-resistant Staphylococcus aureus on neonatal and burn units of a new hospital. Epidemiol Infect 105:215–228PubMedCrossRefGoogle Scholar
  101. 101.
    Klimek JJ, Marsik FJ, Bartlett RC, Weir B, Shea P, Quintiliani R (1976) Clinical, epidemiologic and bacteriologic observations of an outbreak of methicillin-resistant Staphylococcus aureus at a large community hospital. Am J Med 61:340–345PubMedGoogle Scholar
  102. 102.
    Palmer R (1999) Bacterial contamination of curtains in clinical areas. Nurs Stand 14:33–35PubMedGoogle Scholar
  103. 103.
    Rutala WA, Katz E, Sherertz RJ, Sarubbi FA Jr (1983) Environmental study of a methicillin-resistant Staphylococcus aureus epidemic in a burn unit. J Clin Microbiol 18:683–688PubMedGoogle Scholar
  104. 104.
    Singh D, Kaur H, Gardner WG, Treen LB (2002) Bacterial contamination of hospital pagers. Infect Control Hosp Epidemiol 23:274–276PubMedGoogle Scholar
  105. 105.
    Trallero EP, Arenzana JG, Casteneda AA, Grisolia LP (1981) Unusual multiresistant Staphylococcus aureus in a newborn nursery. Am J Dis Child 135:689–692PubMedGoogle Scholar
  106. 106.
    De Boer HEL, van Elzelingen-Dekker CM, van Rheenen-Verberg CMF, Spanjaard L (2006) Use of gaseous ozone for eradication of methicillin-resistant Staphylococcus aureus from the home environment of a colonized hospital employee. Infect Control Hosp Epidemiol 27:1120–1122PubMedGoogle Scholar
  107. 107.
    Sexton T, Clarke P, O’Neill E, Dillane T, Humphreys H (2006) Environmental reservoirs of methicillin-resistant Staphylococcus aureus in isolation rooms: correlation with patient isolates and implications for hospital hygiene. J Hosp Infect 62:187–194PubMedGoogle Scholar
  108. 108.
    Meier PA, Carter CD, Wallace SE, Hollis RJ, Pfaller MA, Herwaldt LA (1996) A prolonged outbreak of methicillin-resistant Staphylococcus aureus in the burn unit of a tertiary medical centre. Infect Control Hosp Epidemiol 17:798–802PubMedGoogle Scholar
  109. 109.
    Lidwell OM, Polakoff S, Jevons MP, Parker MT, Shooter RA, French VI, Dunkerley DR (1966) Staphylococcal infection in thoracic surgery: experience in a subdivided ward. J Hyg 64:321–337Google Scholar
  110. 110.
    Omori A, Takahashi A, Watanabe K, Matsumoto K, Amano H, Yamaguchi K, Kobayashi M, Yoshida T, Mochinaga S (1992) Isolation of MRSA from inpatients, staff and environment in the hospital. Kansenshogaku Zasshi 66:1396–1403PubMedGoogle Scholar
  111. 111.
    Peacock JE, Marsik FJ, Wenzel RP (1980) Methicillin-resistant Staphylococcus aureus: introduction and spread within a hospital. Ann Intern Med 93:526–532PubMedGoogle Scholar
  112. 112.
    Otter JA, Havill NL, Boyce JM (2007) Evaluation of real-time polymerase chain reaction for the detection of methicillin-resistant Staphylococcus aureus on environmental surfaces. Infect Control Hosp Epidemiol 28:1003–1005PubMedGoogle Scholar
  113. 113.
    Obee P, Griffith CJ, Cooper RA, Bennion NE (2007) An evaluation of different methods for the recovery of meticillin-resistant Staphylococcus aureus from environmental surfaces. J Hosp Infect 65:35–41PubMedGoogle Scholar
  114. 114.
    Dancer SJ (2004) How do we assess hospital cleaning? A proposal for microbiological standards for surface hygiene in hospitals. J Hosp Infect 56:10–15PubMedGoogle Scholar
  115. 115.
    Griffith CJ, Cooper RA, Gilmore J, Davies C, Lewis M (2000) An evaluation of hospital cleaning regimes and standards. J Hosp Infect 45:19–28PubMedGoogle Scholar
  116. 116.
    Lally RT, Ederer MN, Woolfrey BF (1985) Evaluation of mannitol salt agar with oxacillin as a screening medium for methicillin-resistant Staphylococcus aureus. J Clin Microbiol 22:501–504PubMedGoogle Scholar
  117. 117.
    Cimolai N, Espersen F (2001) Staphylococcal infections. In: Cimolai N (ed) Laboratory Diagnosis of Bacterial Infections. Marcel Dekker, Inc., New York, NYGoogle Scholar
  118. 118.
    Baird RM, Lee WH (1995) Media used in the detection and enumeration of Staphylococcus aureus. Int J Food Microbiol 26:15–24PubMedGoogle Scholar
  119. 119.
    Cherkaoui A, Renzi G, Francois P, Schrenzel J (2007) Comparison of four chromogenic media for culture-based screening of meticillin-resistant Staphylococcus aureus. J Med Microbiol 56:500–503PubMedGoogle Scholar
  120. 120.
    Struelens M (2001) Molecular epidemiology. In: Cimolai N (ed) Laboratory Diagnosis of Bacterial Infections. Marcel Dekker, Inc., New York, NYGoogle Scholar
  121. 121.
    Wilson AP, Hayman S, Whitehouse T et al (2007) Importance of the environment for patient acquisition of methicillin-resistant Staphylococcus aureus in the intensive care unit: a baseline study. Crit Care Med 35:2275–2279PubMedCrossRefGoogle Scholar
  122. 122.
    Bartzokas CA, Paton JH, Gibson MF, Graham R, McLoughlin GA, Croton RS (1984) Control and eradication of methicillin-resistant Staphylococcus aureus on a surgical unit. N Engl J Med 311:1422–1425PubMedCrossRefGoogle Scholar
  123. 123.
    Shanson DC, Kensit JG, Duke R (1976) Outbreak of hospital infection with a strain of Staphylococcus aureus resistant to gentamicin and methicillin. Lancet ii:1347–1348Google Scholar
  124. 124.
    Trzcinski K, Hryniewicz W, Kluytmans J, van Leeuwen W, Sijmons M, Dulny G, Verbrugh H, van Belkum A (1997) Simultaneous persistence of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus in a neonatal ward of a Warsaw hospital. J Hosp Infect 36:291–303PubMedGoogle Scholar
  125. 125.
    Wilson APR, Hayman S, Folan P, et al (2005) Computer keyboards and the spread of MRSA. 62:390–392Google Scholar
  126. 126.
    Maley MP (1985) Methicillin-resistant Staphylococcus aureus. Lancet ii:605Google Scholar
  127. 127.
    Fujimura S, Kato S, Hashimoto M, Takeda H, Maki F, Watanabe A (2004) Survey of methicillin-resistant Staphylococcus aureus from neonates and the environment in the NICU. J Infect Chemother 10:131–132PubMedGoogle Scholar
  128. 128.
    Hardy KJ, Gossain S, Henderson N et al (2007) Rapid recontamination with MRSA of the environment of an intensive care unit after decontamination with hydrogen peroxide vapour. J Hosp Infect 66:360–368PubMedGoogle Scholar
  129. 129.
    Aihara M, Sakai M, Iwasaki M et al (1993) Prevention and control of methicillin-resistant Staphylococcus aureus in a premature infant ward–preventive effect of a povidone-iodine wipe of neonatal skin. Postgrad Med J 69(Suppl 3):117–121Google Scholar
  130. 130.
    Ohara T, Itoh Y, Itoh K (1998) Ultrasound instruments as possible vectors of staphylococcal infection. J Hosp Infect 40:73–77PubMedGoogle Scholar
  131. 131.
    Embil JM, McLoed JA, Al-Barrak AM et al (2001) An outbreak of methicillin resistant Staphylococcus aureus on a burn unit: potential role of contaminated hydrotherapy equipment. Burns 27:681–688PubMedGoogle Scholar
  132. 132.
    Deurenberg RH, Vink C, Kalenic S, Friedrich AW, Bruggeman CA, Stobberingh EE (2007) The molecular evolution of methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect 13:222–235PubMedGoogle Scholar
  133. 133.
    Fraise AP, Mitchell K, O’Brien SJ, Oldfield K, Wise R (1997) Methicillin-resistant Staphylococcus aureus (MRSA) in nursing homes in a major UK city: an anonymized point prevalence survey. Epidemiol Infect 118:1–5PubMedGoogle Scholar
  134. 134.
    Masterton RG, Coia JE, Notman AW, Kempton-Smith L, Cookson BD (1995) Refractory methicillin-resistant Staphylococcus aureus carriage associated with contamination of the home environment. J Hosp Infect 29:318–319PubMedGoogle Scholar
  135. 135.
    Weese JS, DaCosta T, Button L, Goth K, Ethier M, Boehnke K (2004) Isolation of methicillin-resistant Staphylococcus aureus from the environment in a veterinary teaching hospital. J Vet Intern Med 18:468–470PubMedGoogle Scholar
  136. 136.
    Thomas RJ, Goodbourne C, Goldie B (2004) The transmission of MRSA via orthopaedic marking pens–fact or fiction. Ann R Coll Surg Engl 86:51–52PubMedGoogle Scholar
  137. 137.
    Craven DE, Reed C, Kollisch N, DeMaria A, Lichtenberg D, Shen K, McCabe WR (1981) A large outbreak of infections caused by a strain of Staphylococcus aureus resistant to oxacillin and aminoglycosides. Am J Med 71:53–58PubMedGoogle Scholar
  138. 138.
    Lemoine L (1987) Possible transmission of methicillin-resistant Staphylococcus aureus by expressed human breast milk. J Hosp Infect 9:93–94PubMedGoogle Scholar
  139. 139.
    Rahman M (1993) Epidemic methicillin-resistant Staphylococcus aureus (EMRSA): experience from a health district of central England over five years. Postgrad Med J 69(Suppl. 3):126–129Google Scholar
  140. 140.
    Jeanes A, Rao G, Osman M, Merrick P (2005) Eradication of persistent environmental MRSA. J Hosp Infect 61:85–86PubMedGoogle Scholar
  141. 141.
    Boswell TC, Fox PC (2006) Reduction in MRSA environmental contamination with a portable HEPA-filtration unit. J Hosp Infect 63:47–54PubMedGoogle Scholar
  142. 142.
    Kluytmans J, van Leeuwen W, Goessens W, Hollis R, Messer S, Herwaldt L, Bruining H, Heck M, Rost J, van Leeuwen N, van Belkum A, Verbrugh H (1995) Food-initiated outbreak of methicillin-resistant Staphylococcus aureus analyzed by phenol- and genotyping. J Clin Microbiol 33:1121–1128PubMedGoogle Scholar
  143. 143.
    Asoh N, Masaki H, Watanabe H, Watanabe K, Mitsusima H, Matsumoto K, Oishi K, Nagatake T (2005) Molecular characterization of the transmission between the colonization of methicillin-resistant Staphylococcus aureus to human and environmental contamination in geriatric long-term care wards. Intern Med 44:41–45PubMedGoogle Scholar
  144. 144.
    Berman DS, Schaefler S, Simberkoff MS, Rahal JJ (1986) Tourniquets and nosocomial methicillin-resistant Staphylococcus aureus. N Engl J Med 315:514–515PubMedCrossRefGoogle Scholar
  145. 145.
    Fellowes C, Kerstein R, Clark J, Azadian BS (2006) MRSA on tourniquets and keyboards. J Hosp Infect 64:86–88PubMedGoogle Scholar
  146. 146.
    Oie S, Suenaga S, Sawa A, Kamiya A (2007) Association between isolation sites of methicillin-resistant Staphylococcus aureus (MRSA) in patients with MRSA-positive body sites and MRSA contamination in their surrounding environmental surfaces. Jpn J Infect Dis 60:367–369PubMedGoogle Scholar
  147. 147.
    Stacey A, Burden P, Croton C, Jones E (1998) Contamination of television sets by methicillin-resistant Staphylococcus aureus (MRSA). J Hosp Infect 39:243–244PubMedGoogle Scholar
  148. 148.
    Wagenvoort JHT, Davies BI, Westermann EJA, Werink TJ, Toenbreker HMJ (1993) MRSA from air-exhaust channels. Lancet 341:840–841PubMedGoogle Scholar
  149. 149.
    Patel SN, Murray-Leonard J, Wilson APR (2006) Laundering of hospital staff uniforms at home. J Hosp Infect 62:89–93PubMedGoogle Scholar
  150. 150.
    Oie S, Huang Y, Kamiya A, Konishi H, Nakazawa T (1996) Efficacy of disinfectants against biofilm cells of methicillin-resistant Staphylococcus aureus. Microbios 85:223–230PubMedGoogle Scholar
  151. 151.
    Suller MTE, Russell AD (1999) Antibiotic and biocide resistance in methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococcus. J Hosp Infect 43:281–291PubMedGoogle Scholar
  152. 152.
    Lambert RJW (2004) Comparative analysis of antibiotic and antimicrobial biocide susceptibility data in clinical isolates of methicillin-sensitive Staphylococcus aureus, methicillin-resistant Staphylococcus aureus and Pseudomonas aeruginosa between 1989 and 2000. J Appl Microbiol 97:699–711PubMedGoogle Scholar
  153. 153.
    Al-Masaudi SB, Day MJ, Russell AD (1988) Sensitivity of methicillin-resistant Staphylococcus aureus strains to some antibiotics, antiseptics and disinfectants. J Appl Bacteriol 65:329–337PubMedGoogle Scholar
  154. 154.
    Brumfitt W, Dixson S, Hamilton-Miller JMT (1985) Resistance to antiseptics in methicillin and gentamicin resistant Staphylococcus aureus. Lancet i:1442–1443Google Scholar
  155. 155.
    Irizarry L, Merlin T, Rupp J, Griffith J (1996) Reduced susceptibility of methicillin-resistant Staphylococcus aureus to cetylpyridinium chloride and chlorhexidine. Microbiology 42:248–252Google Scholar
  156. 156.
    Haley CE, Marling-Cason M, Smith JW, Luby JP, Mackowiak PA (1985) Bactericidal activity of antiseptics against methicillin-resistant Staphylococcus aureus. J Clin Microbiol 21:991–992PubMedGoogle Scholar
  157. 157.
    Rutala WA, Stiegel MM, Sarubbi FA, Weber DJ (1997) Susceptibility of antibiotic-susceptible and antibiotic-resistant hospital bacteria to disinfectants. Infect Control Hosp Epidemiol 18:417–421PubMedCrossRefGoogle Scholar
  158. 158.
    Noguchi N, Hase M, Kitta M, Sasatsu M, Deguchi K, Kono M (1999) Antiseptic susceptibility and distribution of antiseptic-resistance genes in methicillin-resistant Staphylococcus aureus. FEMS Microbiol Lett 172:247–253PubMedGoogle Scholar
  159. 159.
    Noguchi N, Suwa J, Narui K, Sasatsu M, Ito T, Hiramatsu K, Song JH (2005) Susceptibilities to antiseptic agents and distribution of antiseptic-resistance genes qacA/B and smr of methicillin-resistant Staphylococcus aureus isolated in Asia during 1998 and 1999. J Med Microbiol 54:557–565PubMedGoogle Scholar
  160. 160.
    Emslie KR, Townsend DE, Grubb WB (1986) Isolation and characterization of a family of small plasmids encoding resistance to nucleic acid-binding compounds in Staphylococcus aureus. J Med Microbiol 22:9–15PubMedCrossRefGoogle Scholar
  161. 161.
    Gillespie MT, May JW, Skurray RA (1986) Plasmid-encoded resistance to acriflavine and quaternary ammonium compounds in methicillin-resistant Staphylococcus aureus. FEMS Microbiol Lett 34:47–51Google Scholar
  162. 162.
    Littlejohn TG, DiBerardino D, Messerotti LJ, Spiers SJ, Skurray RA (1990) Structure and evolution of a family of genes encoding antiseptic and disinfectant resistance in Staphylococcus aureus. Gene 101:59–66Google Scholar
  163. 163.
    Townsend DE, Greed L, Ashdown N, Grubb WB (1983) Plasmid-mediated resistance to quaternary ammonium compounds in methicillin-resistant Staphylococcus aureus. Med J Aust ii:310Google Scholar
  164. 164.
    Bayston R, Ashraf W, Smith T (2007) Triclosan resistance in methicillin-resistant Staphylococcus aureus expressed as small colony variants: a novel mode of evasion of susceptibility to antiseptics. J Antimicrob Chemother 59:848–853PubMedGoogle Scholar
  165. 165.
    Seaman PF, Ochs D, Day MJ. Comments on: Triclosan resistance in methicillin-resistant Staphylococcus aureus expressed as small colony variants: a novel mode of evasion of susceptibility to antibiotics. J Antimicrob Chemother DOI 10.1093/jac/dkm118
  166. 166.
    Narui K, Takano M, Noguchi N, Sasatsu M (2007) Susceptibilities of methicillin-resistant Staphylococcus aureus isolates to seven biocides. Biol Pharm Bull 30:585–587PubMedGoogle Scholar
  167. 167.
    Kobayashi H, Tsuzuki M, Hosobuchi K (1989) Bactericidal effects of antiseptics and disinfectants against methicillin-resistant Staphylococcus aureus. Infect Control Hosp Epidemiol 10:562–564PubMedCrossRefGoogle Scholar
  168. 168.
    Ayliffe GAJ, Coates D, Hoffman PN (1984) Chemical Disinfection in Hospitals. Public Health Laboratory Service, London, EnglandGoogle Scholar
  169. 169.
    Cimolai N (2006) Ocular methicillin-resistant Staphylococcus aureus infections among a newborn intensive care cohort. Amer J Ophthalmol 142:183–184Google Scholar
  170. 170.
    Gant VA, Wren MWD, Rollins MSM, Jeanes A, Hickok SS, Hall TJ (2007) Three novel highly charged copper-based biocides: safety and efficacy against healthcare-associated organisms. J Antimicrob Chemother 60:294–299PubMedGoogle Scholar
  171. 171.
    Mulligan ME, Murray-Leisure KA, Ribner BS, Standiford HC, Korvick JA, Kauffman CA, Yu VL (1993) Methicillin-resistant Staphylococcus aureus: a consensus review of the microbiology, pathogenesis, and epidemiology with implications for prevention and management. Am J Med 94:313–328PubMedGoogle Scholar
  172. 172.
    Muto CA, Jernigan JA, Ostrowsky BE, Richet HM, Jarvis WR, Boyce JM, Farr BM (2003) SHEA guideline for preventing nosocomial transmission of multidrug-resistant strains of Staphylococcus aureus and Enterococcus. Infect Control Hosp Epidemiol 24:362–386PubMedGoogle Scholar
  173. 173.
    Loveday HP, Pellowe CM, Jones SRLJ, Pratt RJ (2006) A systematic review of the evidence for interventions for the prevention and control of meticillin-resistant Staphylococcus aureus (1996–2004): report to the Joint MRSA Working Party (Subgroup A). J Hosp Infect 63S:S45–S70Google Scholar
  174. 174.
    Coia JE, Duckworth GJ, Edwards DI et al (2006) Guidelines for the control and prevention of methicillin-resistant Staphylococcus aureus (MRSA) in healthcare facilities. J Hop Infect 63S:S1–S144Google Scholar
  175. 175.
    Duckworth G et al (1990) Revised guidelines for the control of epidemic methicillin-resistant Staphylococcus aureus. J Hosp Infect 16:351–377Google Scholar
  176. 176.
    Green D, Wigglesworth N, Keegan T, Wilcox MH (2006) Does hospital cleanliness correlate with meticillin-resistant Staphylococcus aureus bacteraemia rates? J Hosp Infect 64:184–186PubMedGoogle Scholar
  177. 177.
    Griffith C (2006) Hospital cleanliness and MRSA rates. J Hosp Infect 65:275–276Google Scholar
  178. 178.
    Green D, Wigglesworth N, Keegan T, Wilcox MH (2006) Hospital cleanliness and MRSA rates. J Hosp Infect 65:276–277Google Scholar
  179. 179.
    Gould IM (2006) Costs of hospital-acquired methicillin-resistant Staphylococcus aureus (MRSA) and its control. Int J Antimicrob Agents 28:379–384PubMedGoogle Scholar
  180. 180.
    Casewell MW (1995) New threats to the control of methicillin-resistant Staphylococcus aureus. J Hosp Infect 30(Suppl.):465–471PubMedGoogle Scholar
  181. 181.
    Dancer SJ (2001) (No) control of MRSA? J Hosp Infect 47:72–73PubMedGoogle Scholar
  182. 182.
    Barrett FF, McGehee RF, Finland M (1968) Methicillin-resistant Staphylococcus aureus at Boston City Hospital. N Engl J Med 279:441–448PubMedCrossRefGoogle Scholar
  183. 183.
    Haley RW, Hightower AW, Khabbaz RF, Thornsberry C, Martone WJ, Allen JR, Hughes JM (1982) The emergence of methicillin-resistant Staphylococcus aureus infections in United States hospitals. Ann Intern Med 97:297–308PubMedGoogle Scholar
  184. 184.
    Maki DG (1978) Control of colonization and transmission of pathogenic bacteria in the hospital. Ann Intern Med 89:777–780PubMedGoogle Scholar
  185. 185.
    Muto CA, Blank MK, Marsh JW et al (2007) Control of an outbreak of infection with the hypervirulent Clostridium difficile BI strain in a university hospital using a comprehensive “bundle” approach. Clin Infect Dis 45:1266–73PubMedGoogle Scholar
  186. 186.
    Cimolai N (2007) MRSA control and the counter-culture. J Hosp Infect 66:189–190PubMedGoogle Scholar
  187. 187.
    Cimolai N (2007) MRSA, public concern, and legislative mandates. Infect Control Hosp Epidemiol 28:896PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.Department of Pathology and Laboratory Medicine, Faculty of MedicineThe University of British ColumbiaVancouverCanada
  2. 2.Department of Pathology and Laboratory MedicineChildren’s and Women’s Centre of British ColumbiaVancouverCanada

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