Microbial monitoring of the hospital environment: why and how?

Journal of Hospital Infection

Volumn 82, Issue 3, 2012, Pages 143-151

  Galvin, S ^a   Dolan, A ^b   Cahill, O ^c   Daniels, S ^c   Humphreys, H ^a,d  

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^b Biotrin International   (Ireland)

^c DUBLIN CITY UNIVERSITY   (Ireland)

^d BEAUMONT HOSPITAL   (Ireland)

Author keywords

Contact plates; Environmental hygiene; Microbial monitoring; Nosocomial pathogens; Sampling; Swabs

Indexed keywords

EXTENDED SPECTRUM BETA LACTAMASE;

ACINETOBACTER BAUMANNII; ANAEROBIC BACTERIUM; BACTERIAL COUNT; BACTERIUM DETECTION; CLEANING; DISINFECTION; EPIDEMIC; HOSPITAL; HOSPITAL HYGIENE; HOSPITAL INFECTION; HUMAN; MEDLINE; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; NONHUMAN; POLYMERASE CHAIN REACTION; REVIEW; VANCOMYCIN RESISTANT ENTEROCOCCUS;

COLONY COUNT, MICROBIAL; CROSS INFECTION; ENVIRONMENTAL MICROBIOLOGY; EPIDEMIOLOGICAL MONITORING; HUMANS; INFECTION CONTROL; MICROBIAL SENSITIVITY TESTS; TIME FACTORS;

EID: 84867720669     PISSN: 01956701     EISSN: 15322939     Source Type: Journal    
DOI: 10.1016/j.jhin.2012.06.015     Document Type: Review

References (86)

1. Dancer S.J. How do we assess hospital cleaning? A proposal for microbiological standards for surface hygiene in hospitals. J Hosp Infect 2004, 56:10-15.
2. Griffith C.J., Cooper R.A., Gilmore J., Davies C., Lewis M. An evaluation of hospital cleaning regimes and standards. J Hosp Infect 2000, 45:19-28.
3. Carling P.C., Briggs J., Hylander D., Perkins J. An evaluation of patient area cleaning in 3 hospitals using a novel targeting methodology. Am J Infect Control 2006, 34:513-519.
4. Carling P.C., Briggs J.L., Perkins J., Highlander D. Improved cleaning of patient rooms using a new targeting method. Clin Infect Dis 2006, 42:385-388.
5. Davies A., Pottage T., Bennett A., Walker J. Gaseous and air decontamination technologies for Clostridium difficile in the healthcare environment. J Hosp Infect 2011, 77:199-203.
6. Van der Mee-Marquet N., Savoyen P., Domelier-Valentin A.S., Mourens C., Quentin R. CTX-M-type fluoroquinolone-resistant Escherichia coli: analysis of the colonization of residents and inanimate surfaces 1 year after a first case of urinary tract infection at a nursing home in France. Infect Control Hosp Epidemiol 2010, 31:968-970.
7. Touati A., Brasme L., Benallaoua S., Madoux J., Gharout A., de Champs C. Enterobacter cloacae and Klebsiella pneumoniae isolates producing CTX-M-15 recovered from hospital environmental surfaces from Algeria. J Hosp Infect 2008, 68:183-185.
8. Kac G., Podglajen I., Vaupre S., Colardelle N., Buu-Hof A., Gutmann L. Molecular epidemiology of extended-spectrum beta-lactamase-producing Enterobacteriaceae isolated from environmental and clinical specimens in a cardiac surgery intensive care unit. Infect Control Hosp Epidemiol 2004, 25:852-855.
9. Agata E.M., Venkataraman L., DeGirolami P., Samore M. Molecular epidemiology of ceftazidime-resistant Gram-negative bacilli on inanimate surfaces and their role in cross-transmission during nonoutbreak periods. J Clin Microbiol 1999, 37:3065-3067.
10. O'Fallon E., Schreiber R., Kandel R., D'Agata E.M. Multidrug-resistant Gram-negative bacteria at a long-term care facility: assessment of residents, healthcare workers, and inanimate surfaces. Infect Control Hosp Epidemiol 2009, 30:1172-1179.
11. Huang S.S., Datta R., Platt R. Risk of acquiring antibiotic-resistant bacteria from prior room occupants. Arch Intern Med 2006, 166:1945-1951.
12. Nseir S., Blazejewski C., Lubret R., Wallet F., Courcol R., Durocher A. Risk of acquiring multidrug-resistant Gram-negative bacilli from prior room occupants in the intensive care unit. Clin Microbiol Infect 2011, 17:1201-1208.
13. Rohr U., Kaminski A., Wilhelm M., Jurzik L., Gatermann S., Muhr G. Colonization of patients and contamination of the patients' environment by MRSA under conditions of single-room isolation. Int J Hyg Environ Health 2009, 212:209-215.
14. Manian F.A., Griesenauer S., Senkel D., et al. Isolation of Acinetobacter baumannii complex and methicillin-resistant Staphylococcus aureus from hospital rooms following terminal cleaning and disinfection: can we do better?. Infect Control Hosp Epidemiol 2011, 32:667-672.
15. Creamer E., Humphreys H. The contribution of beds to healthcare-associated infection: the importance of adequate decontamination. J Hosp Infect 2008, 69:8-23.
16. Martirosian G. Recovery of Clostridium difficile from hospital environments. J Clin Microbiol 2006, 44:1202-1203.
17. Otter J.A., French G.L. Survival of nosocomial bacteria and spores on surfaces and inactivation by hydrogen peroxide vapor. J Clin Microbiol 2009, 47:205-207.
18. Touati A., Zenati K., Brasme L., Benallaoua S., de Champs C. Extended-spectrum beta-lactamase characterisation and heavy metal resistance of Enterobacteriaceae strains isolated from hospital environmental surfaces. J Hosp Infect 2010, 75:78-79.
19. Hobson R.P., MacKenzie F.M., Gould I.M. An outbreak of multiply-resistant Klebsiella pneumoniae in the Grampian region of Scotland. J Hosp Infect 1996, 33:249-262.
20. Shore A.C., Rossney A.S., Kinnevey P.M., et al. Enhanced discrimination of highly clonal ST22-methicillin-resistant Staphylococcus aureus IV isolates achieved by combining spa, dru, and pulsed-field gel electrophoresis typing data. J Clin Microbiol 2011, 48:1839-1852.
21. Hardy K.J., Oppenheim B.A., Gossain S., Gao F., Hawkey P.M. A study of the relationship between environmental contamination with methicillin-resistant Staphylococcus aureus (MRSA) and patients' acquisition of MRSA. Infect Control Hosp Epidemiol 2006, 27:127-132.
22. Asoh N., Masaki H., Watanabe H., et al. 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 2005, 44:41-45.
23. Weber D.J., Rutala W.A., Miller M.B., Huslage K., Sickbert-Bennett E. Role of hospital surfaces in the transmission of emerging health care-associated pathogens: norovirus, Clostridium difficile, and Acinetobacter species. Am J Infect Control 2010, 38:S25-S33.
24. Hirai Y. Survival of bacteria under dry conditions; from a viewpoint of nosocomial infection. J Hosp Infect 1991, 19:191-200.
25. Jawad A., Heritage J., Snelling A.M., Gascoyne-Binzi D.M., Hawkey P.M. Influence of relative humidity and suspending menstrua on survival of Acinetobacter spp. on dry surfaces. J Clin Microbiol 1996, 34:2881-2887.
26. Musa E.K., Desai N., Casewell M.W. The survival of Acinetobacter calcoaceticus inoculated on fingertips and on formica. J Hosp Infect 1990, 15:219-227.
27. Creamer E., Dorrian S., Dolan A., et al. When are the hands of healthcare workers positive for methicillin-resistant Staphylococcus aureus?. J Hosp Infect 2010, 75:107-111.
28. Stiefel U., Cadnum J.L., Eckstein B.C., Guerrero D.M., Tima M.A., Donskey C.J. Contamination of hands with methicillin-resistant Staphylococcus aureus after contact with environmental surfaces and after contact with the skin of colonized patients. Infect Control Hosp Epidemiol 2011, 32:185-187.
29. Dancer S.J., White L., Robertson C. Monitoring environmental cleanliness on two surgical wards. Int J Environ Health Res 2008, 18:357-364.
30. Wagenvoort J.H., De Brauwer E.I., Penders R.J., Willems R.J., Top J., Bonten M.J. Environmental survival of vancomycin-resistant Enterococcus faecium. J Hosp Infect 2011, 77:282-283.
31. Kramer A., Schwebke I., Kampf G. How long do nosocomial pathogens persist on inanimate surfaces? A systematic review. BMC Infect Dis 2006, 6:130.
32. Coughenour C., Stevens V., Stetzenbach L.D. An evaluation of methicillin-resistant Staphylococcus aureus survival on five environmental surfaces. Microb Drug Resist 2011, 17:457-461.
33. Wagenvoort J.H., Sluijsmans W., Penders R.J. Better environmental survival of outbreak vs. sporadic MRSA isolates. J Hosp Infect 2000, 45:231-234.
34. Gad G.F., El-Domany R.A., Zaki S., Ashour H.M. Characterization of Pseudomonas aeruginosa isolated from clinical and environmental samples in Minia, Egypt: prevalence, antibiogram and resistance mechanisms. J Antimicrob Chemother 2007, 60:1010-1017.
35. Das I., Lambert P., Hill D., Noy M., Bion J., Elliott T. Carbapenem-resistant Acinetobacter and role of curtains in an outbreak in intensive care units. J Hosp Infect 2002, 50:110-114.
36. Enoch D.A., Summers C., Brown N.M., et al. Investigation and management of an outbreak of multidrug-carbapenem-resistant Acinetobacter baumannii in Cambridge, UK. J Hosp Infect 2008, 70:109-118.
37. Fawley W.N., Underwood S., Freeman J., et al. Efficacy of hospital cleaning agents and germicides against epidemic Clostridium difficile strains. Infect Control Hosp Epidemiol 2007, 28:920-925.
38. Wilcox M.H., Fawley W.N. Hospital disinfectants and spore formation by Clostridium difficile. Lancet 2000, 356:1324.
39. Dumford D.M., Nerandzic M.M., Eckstein B.C., Donskey C.J. What is on that keyboard? Detecting hidden environmental reservoirs of Clostridium difficile during an outbreak associated with North American pulsed-field gel electrophoresis type 1 strains. Am J Infect Control 2009, 37:15-19.
40. Dubberke E.R., Reske K.A., Noble-Wang J., et al. Prevalence of Clostridium difficile environmental contamination and strain variability in multiple health care facilities. Am J Infect Control 2007, 35:315-318.
41. Mutters R., Nonnenmacher C., Susin C., Albrecht U., Kropatsch R., Schumacher S. Quantitative detection of Clostridium difficile in hospital environmental samples by real-time polymerase chain reaction. J Hosp Infect 2009, 71:43-48.
42. Eckstein B.C., Adams D.A., Eckstein E.C., et al. Reduction of Clostridium difficile and vancomycin-resistant Enterococcus contamination of environmental surfaces after an intervention to improve cleaning methods. BMC Infect Dis 2007, 7:61.
43. Lemmen S.W., Hafner H., Zolldann D., Amedick G., Lutticken R. 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 2001, 203:245-248.
44. Obee P., Griffith C.J., Cooper R.A., Bennion N.E. An evaluation of different methods for the recovery of meticillin-resistant Staphylococcus aureus from environmental surfaces. J Hosp Infect 2007, 65:35-41.
45. Dalmaso G., Bini M., Paroni R., Ferrari M. Qualification of high-recovery, flocked swabs as compared to traditional rayon swabs for microbiological environmental monitoring of surfaces. PDA J Pharm Sci Technol 2008, 62:191-199.
46. Verhoeven P., Grattard F., Carricajo A., Pozzetto B., Berthelot P. Better detection of Staphylococcus aureus nasal carriage by use of nylon flocked swabs. J Clin Microbiol 2010, 48:4242-4244.
47. De Silva S., Wood G., Quek T., Parrott C., Bennett C.M. Comparison of flocked and rayon swabs for detection of nasal carriage of Staphylococcus aureus among pathology staff members. J Clin Microbiol 2010, 48:2963-2964.
48. Saegeman V., Flamaing J., Muller J., Peetermans W.E., Stuyck J., Verhaegen J. Clinical evaluation of the Copan ESwab for methicillin-resistant Staphylococcus aureus detection and culture of wounds. Eur J Clin Microbiol Infect Dis 2011, 30:943-949.
49. Dolan A., Bartlett M., McEntee B., Creamer E., Humphreys H. Evaluation of different methods to recover meticillin-resistant Staphylococcus aureus from hospital environmental surfaces. J Hosp Infect 2011, 79:227-230.
50. Hedin G., Rynback J., Lore B. New technique to take samples from environmental surfaces using flocked nylon swabs. J Hosp Infect 2010, 75:314-317.
51. Manheimer W.A., Ybanez T. Observations and experiments on dish-washing. Am J Public Health 1917, 7:614-618.
52. Favero M.S., McDade J.J., Robertsen J.A., Hoffman R.K., Edwards R.W. Microbiological sampling of surfaces. J Appl Bacteriol 1968, 31:336-343.
53. Rose L., Jensen B., Peterson A., Banerjee S.N., Srduino M.J. Swab materials and Bacillus anthracis spore recovery from nonporous surfaces. Emerg Infect Dis 2004, 10:1023-1029.
54. Hodges L.R., Rose L.J., Peterson A., Noble-Wang J., Arduino M.J. Evaluation of a macrofoam swab protocol for the recovery of Bacillus anthracis spores from a steel surface. Appl Environ Microbiol 2006, 72:4429-4430.
55. Landers T.F., Hoet A., Wittum T.E. Swab type, moistening, and pre-enrichment for Staphylococcus aureus on environmental surfaces. J Clin Microbiol 2010, 48:2235-2236.
56. Moore G., Griffith C. Problems associated with traditional hygiene swabbing: the need for in-house standardization. J Appl Microbiol 2007, 103:1090-1103.
57. Dey B.P., Engley F.B. Methodology for recovery of chemically treated Staphylococcus aureus with neutralizing medium. Appl Environ Microbiol 1983, 45:1533-1537.
58. Dey B.P., Engley F.B. Comparison of Dey and Engley (D/E) neutralizing medium to Letheen medium and standard methods medium for recovery of Staphylococcus aureus from sanitized surfaces. J Ind Microbiol 1995, 14:21-25.
59. Hacek D.M., Trick W.E., Collins S.M., Noskin G.A., Peterson L.R. Comparison of the Rodac imprint method to selective enrichment broth for recovery of vancomycin-resistant enterococci and drug-resistant Enterobacteriaceae from environmental surfaces. J Clin Microbiol 2000, 38:4646-4648.
60. Scott E., Bloomfield S.F., Barlow C.G. A comparison of contact plate and calcium alginate swab techniques for quantitative assessment of bacteriological contamination of environmental surfaces. J Appl Bacteriol 1984, 56:317-320.
61. Pinto F., Hiom S., Girdlestone S., Maillard J.Y. Evaluation of the effectiveness of commercially available contact plates for monitoring microbial environments. Lett Appl Microbiol 2009, 48:379-382.
62. Foschino R., Picozzia C., Civardia A., Bandinib M., Faroldic P. Comparison of surface sampling methods and cleanability assessment of stainless steel surfaces subjected or not to shot peening. J Food Eng 2003, 60:375-381.
63. Kusumaningrum H.D., Riboldi G., Hazeleger W.C., Beumer R.R. Survival of foodborne pathogens on stainless steel surfaces and cross-contamination to foods. Int J Food Microbiol 2003, 85:227-236.
64. Wesche A.M., Gurtler J.B., Marks B.P., Ryser E.T. Stress, sublethal injury, resuscitation, and virulence of bacterial foodborne pathogens. J Food Prot 2009, 72:1121-1138.
65. Brashears M.M., Amezquita A., Stratton J. Validation of methods used to recover Escherichia coli O157:H7 and Salmonella spp. subjected to stress conditions. J Food Prot 2001, 64:1466-1471.
66. Oliver J.D. The viable but nonculturable state in bacteria. J Microbiol 2005, 43:93-100.
67. Otter J.A., Havill N.L., Adams N.M., Cooper T., Tauman A., Boyce J.M. Environmental sampling for Clostridium difficile: swabs or sponges?. Am J Infect Control 2009, 37:517-518.
68. Jawad A., Seifert H., Snelling A.M., Heritage J., Hawkey P.M. Survival of Acinetobacter baumannii on dry surfaces: comparison of outbreak and sporadic isolates. J Clin Microbiol 1998, 36:1938-1941.
69. Best E.L., Fawley W.N., Parnell P., Wilcox M.H. The potential for airborne dispersal of Clostridium difficile from symptomatic patients. Clin Infect Dis 2010, 50:1450-1457.
70. Boyce J.M., Potter-Bynoe G., Chenevert C., King T. Environmental contamination due to methicillin-resistant Staphylococcus aureus: possible infection control implications. Infect Control Hosp Epidemiol 1997, 18:622-627.
71. Boyce J.M. Environmental contamination makes an important contribution to hospital infection. J Hosp Infect 2007, 65:50-544.
72. Sexton T., Clarke P., O'Neill E., Dillane T., Humphreys H. Environmental reservoirs of methicillin-resistant Staphylococcus aureus in isolation rooms: correlation with patient isolates and implications for hospital hygiene. J Hosp Infect 2006, 62:187-194.
73. Creamer E., Dolan A., Sherlock O., et al. The effect of rapid screening for methicillin-resistant Staphylococcus aureus (MRSA) on the identification and earlier isolation of MRSA-positive patients. Infect Control Hosp Epidemiol 2010, 31:374-381.
74. Otter J.A., Havill N.L., Boyce J.M. Evaluation of real-time polymerase chain reaction for the detection of methicillin-resistant Staphylococcus aureus on environmental surfaces. Infect Control Hosp Epidemiol 2007, 28:1003-1005.
75. Desjardins M., Guibord C., Lalonde B., Toye B., Ramotar K. Evaluation of the IDI-MRSA assay for detection of methicillin-resistant Staphylococcus aureus from nasal and rectal specimens pooled in a selective broth. J Clin Microbiol 2006, 44:1219-1223.
76. Sherlock O., Dolan A., Humphreys H. MRSA screening: can one swab be used for both culture and rapid testing? An evaluation of chromogenic culture and subsequent Hain GenoQuick PCR amplification/detection. Clin Microbiol Infect 2009, 16:955-959.
77. Shiomori T., Miyamoto H., Makishima K., et al. Evaluation of bed making related airborne and surface methicillin-resistant Staphylococcus aureus contamination. J Hosp Infect 2002, 50:30-35.
78. Overton E. The Journal of Infection Control Nursing. Bed-making and bacteria. Nurs Times 1988, 84:69-71.
79. Best E.L., Sandoe J.A., Wilcox M.H. Potential for aerosolization of Clostridium difficile after flushing toilets: the role of toilet lids in reducing environmental contamination risk. J Hosp Infect 2012, 80:1-5.
80. Reisner B.S., Shaw S., Huber M.E., et al. Comparison of three methods to recover vancomycin-resistant enterococci (VRE) from perianal and environmental samples collected during a hospital outbreak of VRE. Infect Control Hosp Epidemiol 2000, 21(12):775-779.
81. Rampling A., Wiseman S., Davis L., et al. Evidence that hospital hygiene is important in the control of methicillin-resistant Staphylococcus aureus. J Hosp Infect 2001, 49(2):109-116.
82. Otter J.A., French G.L. Utility of antimicrobial susceptibility-based algorithms for the presumptive identification of genotypically-defined community-associated methicillin-resistant Staphylococcus aureus at a London teaching hospital. Eur J Clin Microbiol Infect Dis 2011, 30(3):459-463.
83. Hardy K.J., Gossain S., Henderson N., et al. Rapid recontamination with MRSA of the environment of an intensive care unit after decontamination with hydrogen peroxide vapour. J Hosp Infect 2007, 66(4):360-368.
84. Ndip R.N., Dilonga H.M., Ndip L.M., Akoachere J.F., Nkuo Akenji T. Pseudomanas aeruginosa isolates recovered from clinical and environmental samples in Buea, Cameroon: current status on biotyping and antibiogram. Trop Med Int Health 2005, 10(1):74-81.
85. Simor A.E., Lee M., Vearncombe M., et al. An outbreak due to multiresistant Acinetobacter baumannii in a burn unit: risk factors for acquisition and management. Infect Control Hosp Epidemiol 2002, 23(5):261-267.
86. Wilcox M.H., Fawley W.N., Wigglesworth N., Parnell P., Verity P., Freeman J. Comparison of the effect of detergent versus hypochloride cleaning on environmental contamination and incidence of Clostridium difficile infection. J Hosp Infect 2003, 54(2):109-114.