The identification and epidemiology of meticillin-resistant Staphylococcus aureus and Clostridium difficile in patient rooms and the ward environment

BMC Infectious Diseases

Volumn 13, Issue 1, 2013, Pages

  Faires, Meredith C ^a   Pearl, David L ^a   Berke, Olaf ^a   Reid Smith, Richard J ^a   Weese, J Scott ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

Clostridium difficile; Environment; Epidemiology; Hospital; Meticillin resistant Staphylococcus aureus; Patient rooms; Ribotype 078; Risk factors; Ward

Indexed keywords

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM CONTAMINATION; BACTERIUM CULTURE; BACTERIUM ISOLATE; CLOSTRIDIUM DIFFICILE; CLOTHING; COMMUNITY HOSPITAL; CONTROLLED STUDY; ENVIRONMENTAL FACTOR; GENOTYPE; HOSPITAL DEPARTMENT; HOSPITAL PATIENT; MEDICAL WARD; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; NONHUMAN; PREVALENCE; RIBOTYPING; RISK ASSESSMENT; RISK FACTOR; SAMPLING; SPA GENE; SURGICAL WARD; WARD;

EID: 84880938280     PISSN: None     EISSN: 14712334     Source Type: Journal    
DOI: 10.1186/1471-2334-13-342     Document Type: Article

References (62)

1. Simor AE, Gilbert NL, Gravel D, Mulvey MR, Bryce E, Loeb M, Matlow A, McGeer A, Louie L, Campbell J. Canadian Nosocomial Infection Surveillance Program Methicillin-resistant Staphylococcus aureus colonization or infection in Canada: national surveillance and changing epidemiology, 1995-2007. Infect Control Hosp Epidemiol 2010, 31:348-356. 10.1086/651313, 20148693, Canadian Nosocomial Infection Surveillance Program.
2. Gravel D, Miller M, Simor A, Taylor G, Gardam M, McGeer A, Hutchinson J, Moore D, Kelly S, Boyd D, Mulvey M. Canadian Nosocomial Infection Surveillance Program Health care-associated Clostridium difficile infection in adults admitted to acute care hospitals in Canada: a Canadian nosocomial infection surveillance program study. Clin Infect Dis 2009, 48:568-576. 10.1086/596703, 19191641, Canadian Nosocomial Infection Surveillance Program.
3. Poutanen SM, Simor AE. Clostridium difficile-associated diarrhea in adults. CMAJ 2004, 171:51-58. 10.1503/cmaj.1031189, 437686, 15238498.
4. Dancer SJ, White LF, Lamb J, Girvan EK, Robertson C. Measuring the effect of enhanced cleaning in a UK hospital: a prospective cross-over study. BMC Med 2009, 7:28. 10.1186/1741-7015-7-28, 2700808, 19505316.
5. Boyce JM, Havill NL, Otter JA, McDonald LC, Adams NM, Cooper T, Thompson A, Wiggs L, Killgore G, Tauman A, Noble-Wang J. Impact of hydrogen peroxide vapour room decontamination on Clostridium difficile environmental contamination and transmission in a health care setting. Infect Control Hosp Epidemiol 2008, 29:723-729. 10.1086/589906, 18636950.
6. Boyce JM. Environmental contamination makes an important contribution to hospital infection. J Hosp Infect 2007, 65(Suppl 2):50-54.
7. Wagenvoort JH, Sluijsmans W, Penders RJ. Better environmental survival of outbreak vs. sporadic MRSA isolates. J Hosp Infect 2000, 45:231-234. 10.1053/jhin.2000.0757, 10896803.
8. 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, 7:43-48.
9. Dettenkofer M, Ammon A, Astagneau P, Dancer SJ, Gastmeier P, Harbarth S, Humphreys H, Kern WV, Lyytikäinen O, Sax H, Voss A, Widmer AF. Infection control-a European research perspective for the next decade. J Hosp Infect 2011, 77:7-10. 10.1016/j.jhin.2010.07.025, 21145620.
10. Samore MH. Epidemiology of nosocomial Clostridium difficile. J Hosp Infect 1999, 43(Suppl):183-190.
11. Annex A. Screening, testing and surveillance for antibiotic-resistant organisms (AROs). http://www.publichealthontario.ca/en/eRepository/PIDAC-IPC_Annex_A_Screening_Testing_Surveillance_AROs_2013.pdf.
12. Shopsin B, Gomez M, Montgomery SO, Smith DH, Waddington M, Dodge DE, Bost DA, Riehman M, Naidich S, Kreiswirth BN. Evaluation of protein A gene polymorphic region DNA sequencing for typing Staphylococcus aureus strains. J Clin Microbiol 1999, 37:3556-3563. 85690, 10523551.
13. eGenomics. http://tools.egenomics.com.
14. Ridom SpaServer. http://www.spaserver.ridom.de.
15. Golding GR, Campbell JL, Spreitzer DJ, Veyhl J, Surynicz K, Simor A, Mulvey MR. Canadian Nosocomial Infection Surveillance Program A preliminary guideline for the assignment of methicillin-resistant Staphylococcus aureus to a Canadian pulsed-field gel electrophoresis epidemic type using spa typing. Can J Infect Dis Med Microbiol 2008, 19:273-281. 2604773, 19436507, Canadian Nosocomial Infection Surveillance Program.
16. Rankin S, Roberts S, O'Shea K, Maloney D, Lorenzo M, Benson CE. Panton valentine leukocidin (PVL) toxin positive MRSA strains isolated from companion animals. Vet Microbiol 2005, 108:145-148. 10.1016/j.vetmic.2005.02.013, 15917142.
17. Kato H, Kato N, Watanabe K, Iwai N, Nakamura H, Yamamoto T, Suzuki K, Kim SM, Chong Y, Wasito EB. Identification of toxin A-negative, toxin B-positive Clostridium difficile by PCR. J Clin Microbiol 1998, 36:2178-2182. 105000, 9665986.
18. Lemee L, Dhalluin A, Testelin S, Mattrat MA, Maillard K, Lemeland JF, Pons JL. Multiplex PCR targeting tpi (triose phosphate isomerise), tcdA (toxin a), tcdB (toxin B), genes for toxigenic culture of Clostridium difficile. J Clin Microbiol 2004, 42:5710-5714. 10.1128/JCM.42.12.5710-5714.2004, 535266, 15583303.
19. Stubbs S, Rupnik M, Gibert M, Brazier J, Duerden B, Popoff M. Production of actin-specific ADP-ribosyltransferase (binary toxin) by strains of Clostridium difficile. FEMS Microbiol Lett 2000, 186:307-312. 10.1111/j.1574-6968.2000.tb09122.x, 10802189.
20. Bidet P, Barbut F, Lalande V, Burghoffer B, Petit JC. Development of a new PCR-ribotyping method for Clostridium difficile based on ribosomal RNA gene sequencing. FEMS Microbiol Lett 1999, 175:261-266. 10.1111/j.1574-6968.1999.tb13629.x, 10386377.
21. Rupnik M, Avesani V, Janc M, von Eichel-Streiber C, Delmée M. A novel toxinotyping scheme and correlation of toxinotypes with serogroups of Clostridium difficile isolates. J Clin Microbiol 1998, 36:2240-2247. 105025, 9665999.
22. Dohoo IR, Martin W, Stryhn H. Model-building strategies 2003, 317-334. Charlottetown, Prince Edward Island: AVC, Inc, Veterinary epidemiologic research.
23. StataCorp Exlogistic - exact logistic regression 2007, 423-439. College Station, Texas: Stata Press, Stata statistical software: release 10, StataCorp.
24. 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. 10.1016/j.ijheh.2008.05.003, 18667356.
25. French GL, Otter JA, Shannon KP, Adams NM, Watling D, Parks MJ. Tackling contamination of the hospital environment by methicillin-resistant Staphylococcus aureus (MRSA): a comparison between conventional terminal cleaning and hydrogen peroxide vapour decontamination. J Hosp Infect 2004, 57:31-37. 10.1016/j.jhin.2004.03.006, 15142713.
26. Eckstein BC, Adams DA, Eckstein EC, Rao A, Sethi AK, Yadavalli GK, Donskey CJ. 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. 10.1186/1471-2334-7-61, 1906786, 17584935.
27. Dubberke ER, Reske KA, Noble-Wang J, Thompson A, Killgore G, Mayfield J, Camins B, Woeltje K, McDonald JR, McDonald LC, Fraser VJ. Prevalence of Clostridium difficile environmental contamination and strain variability in multiple health care facilities. Am J Infect Control 2007, 35:315-318. 10.1016/j.ajic.2006.12.006, 17577478.
28. Dumford DM, Nerandzic MM, Eckstein BC, Donskey CJ. 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. 10.1016/j.ajic.2008.07.009, 19171247.
29. Carling PC, Parry MF, Bruno-Murtha LA, Dick B. Improving environmental hygiene in 27 intensive care units to decrease multidrug-resistant bacterial transmission. Crit Care Med 2010, 38:1054-1059. 10.1097/CCM.0b013e3181cdf705, 20081531.
30. Chang S, Sethi AK, Eckstein BC, Stiefel U, Cadnum JL, Donskey CJ. Skin and environmental contamination with methicillin-resistant Staphylococcus aureus among carriers identified clinically versus through active surveillance. Clin Infect Dis 2009, 15:1423-1428.
31. 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. 10.1016/j.jhin.2005.07.017, 16290319.
32. Rampling A, Wiseman S, Davis L, Hyett AP, Walbridge AN, Payne GC, Cornaby AJ. Evidence that hospital hygiene is important in the control of methicillin-resistant Staphylococcus aureus. J Hosp Infect 2001, 49:109-116. 10.1053/jhin.2001.1013, 11567555.
33. Verity P, Wilcox MH, Fawley W, Parnell P. Prospective evaluation of environmental contamination by Clostridium difficile in isolation side rooms. J Hosp Infect 2001, 49:204-209. 10.1053/jhin.2001.1078, 11716638.
34. Boyce JM, 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. 10.1086/647686, 9309433.
35. Trillis F, Eckstein EC, Budavich R, Pultz MJ, Donskey CJ. Contamination of hospital curtains with health care-associated pathogens. Infect Control Hosp Epidemiol 2008, 29:1074-1076. 10.1086/591863, 18823274.
36. Stacey A, Burden P, Croton C, Jones E. Contamination of television sets by methicillin-resistant Staphylococcus aureus (MRSA). J Hosp Infect 1998, 39:243-244. 10.1016/S0195-6701(98)90266-3, 9699147.
37. Dumford DM, Nerandzic M, Chang S, Richmond MA, Donskey C. Epidemiology of Clostridium difficile and vancomycin-resistant Enterococcus colonization in patients on a spinal cord unit. J Spinal Cord Med 2011, 34:22-27. 10.1179/107902610x12883422813822, 3066494, 21528623.
38. Sethi AK, Al-Nassir WN, Nerandzic MM, Bobulsky GS, Donskey CJ. Persistence of skin contamination and environmental shedding of Clostridium difficile during and after treatment of C. difficile infection. Infect Control Hosp Epidemiol 2010, 31:21-27. 10.1086/649016, 19929371.
39. Leitch A, McCormick I, Gunn I, Gillespie T. Reducing the potential for phlebotomy tourniquets to act as a reservoir for methicillin-resistant Staphylococcus aureus. J Hosp Infect 2006, 63:428-431. 10.1016/j.jhin.2006.03.006, 16759742.
40. Faires MC, Pearl DL, Ciccotelli WA, Straus K, Zinken G, Berke O, Reid-Smith RJ, Weese JS. A prospective study to examine the epidemiology of methicillin-resistant Staphylococcus aureus and Clostridium difficile contamination in the general environment of three community hospitals in southern Ontario, Canada. BMC Infect Dis 2012, 12:290. 10.1186/1471-2334-12-290, 3532087, 23136936.
41. Shelly MJ, Scanlon TG, Ruddy R, Hannan MM, Murray JG. Meticillin-resistant Staphylococcus aureus (MRSA) environmental contamination in a radiology department. Clin Radiol 2011, 66:861-864. 10.1016/j.crad.2011.05.002, 21676384.
42. Martirosian G. Recovery of Clostridium difficile from hospital environments. J Clin Microbiol 2006, 44:1202-1203. 10.1128/JCM.44.3.1202-1203.2006, 1393149, 16517932.
43. Pulvirenti JJ, Gerding DN, Nathan C, Hafiz I, Mehra T, Marsh D, Kocka F, Rice T, Fischer SA, Segreti J, Weinstein RA. Difference in the incidence of Clostridium difficile among patients infected with human immunodeficiency virus admitted to a public and a private hospital. Infect Control Hosp Epidemiol 2002, 23:641-647. 10.1086/501987, 12452290.
44. Bures S, Fishbain JT, Uyehara CF, Parker JM, Berg BW. Computer keyboards and faucet handles as reservoirs of nosocomial pathogens in the intensive care unit. Am J Infect Control 2000, 28:465-471. 10.1067/mic.2000.107267, 11114617.
45. Conly JM, Johnston BL. The emergence of methicillin-resistant Staphylococcus aureus as a community-acquired pathogen in Canada. Can J Infect Dis 2003, 14:249-251. 2094949, 18159464.
46. Neely AN, Maley MP. Survival of enterococci and staphylococci on hospital fabrics and plastic. J Clin Microbiol 2000, 38:724-726. 86187, 10655374.
47. Fawley WN, Wilcox MH. Molecular epidemiology of endemic Clostridium difficile infection. Epidemiol Infect 2001, 126:343-350. 2869701, 11467790.
48. Kim KH, Fekety R, Batts DH, Brown D, Cudmore M, Silva J, Waters D. Isolation of Clostridium difficile from the environment and contacts of patients with antibiotic-associated colitis. J Infect Dis 1981, 143:42-50. 10.1093/infdis/143.1.42, 7217711.
49. Gilca R, Fortin E, Frenette C, Longtin Y, Gourdeau M. Seasonal variations in Clostridium difficile infections are associated with influenza and respiratory syncytial virus activity independently of antibiotic prescriptions: a time-series analysis in Quebec, Canada. Antimicrob Agents Chemother 2012, 56:639-646. 10.1128/AAC.05411-11, 3264229, 22106208.
50. Polgreen PM, Yang M, Bohnett LC, Cavanaugh JE. A time-series analysis of Clostridium difficile and its seasonal association with influenza. Infect Control Hosp Epidemiol 2010, 31:382-387. 10.1086/651095, 3024857, 20175682.
51. Christianson S, Golding GR, Campbell J, Mulvey MR. Canadian Nosocomial Infection Surveillance Program Comparative genomics of Canadian epidemic lineages of methicillin-resistant Staphylococcus aureus. J Clin Microbiol 2007, 45:1904-1911. 10.1128/JCM.02500-06, 1933033, 17428941, Canadian Nosocomial Infection Surveillance Program.
52. Loo VG, Poirier L, Miller MA, Oughton M, Libman MD, Michaud S, Bourgault AM, Nguyen T, Frenette C, Kelly M, Vibien A, Brassard P, Fenn S, Dewar K, Hudson TJ, Horn R, René P, Monczak Y, Dascal A. A predominantly clonal multi-institutional outbreak of Clostridium difficile-associated diarrhea with high morbidity and mortality. N Engl J Med 2005, 353:2442-2449. 10.1056/NEJMoa051639, 16322602.
53. Pépin J, Valiquette L, Cossette B. Mortality attributable to nosocomial Clostridium difficile -associated disease during an epidemic caused by a hypervirulent strain in Quebec. CMAJ 2005, 173:1037-1042. 10.1503/cmaj.050978, 1266326, 16179431.
54. Martin H, Willey B, Low DE, Staempfli HR, McGeer A, Boerlin P, Mulvey M, Weese JS. Characterization of Clostridium difficile strains isolated from patients in Ontario, Canada, from 2004 to 2006. J Clin Microbiol 2008, 46:2999-3004. 10.1128/JCM.02437-07, 2546775, 18650360.
55. Goorhuis A, Bakker D, Corver J, Debast SB, Harmanus C, Notermans DW, Bergwerff AA, Dekker FW, Kuijper EJ. Emergence of Clostridium difficile infection due to a new hypervirulent strain, polymerase chain reaction ribotype 078. Clin Infect Dis 2008, 47:1162-1170. 10.1086/592257, 18808358.
56. Mulvey MR, Boyd DA, Gravel D, Hutchinson J, Kelly S, McGeer A, Moore D, Simor A, Suh KN, Taylor G, Weese JS, Miller M. Canadian Nosocomial Infection Surveillance Program Hypervirulent Clostridium difficile strains in hospitalized patients, Canada. Emerg Infect Dis 2010, 16:678-681. 10.3201/eid1604.091152, 3321949, 20350386, Canadian Nosocomial Infection Surveillance Program.
57. Costa MC, Reid-Smith R, Gow S, Hannon SJ, Booker C, Rousseau J, Benedict KM, Morley PS, Weese JS. Prevalence and molecular characterization of Clostridium difficile isolated from feedlot beef cattle upon arrival and mid-feeding period. BMC Vet Res 2012, 8:38. 10.1186/1746-6148-8-38, 3353841, 22455611.
58. Weese JS, Rousseau J, Deckert A, Gow S, Reid-Smith RJ. Clostridium difficile and methicillin-resistant Staphylococcus aureus shedding by slaughter-age pigs. BMC Vet Res 2011, 7:41. 10.1186/1746-6148-7-41, 3162498, 21791057.
59. Rodriguez-Palacios A, Stämpfli HR, Duffield T, Peregrine AS, Trotz-Williams LA, Arroyo LG, Brazier JS, Weese JS. Clostridium difficile PCR ribotypes in calves, Canada. Emerg Infect Dis 2006, 12:1730-1736. 10.3201/eid1211.051581, 3372327, 17283624.
60. Weese JS, Finley R, Reid-Smith RR, Janecko N, Rousseau J. Evaluation of Clostridium difficile in dogs and the household environment. Epidemiol Infect 2010, 138:1100-1104. 10.1017/S0950268809991312, 19951453.
61. Blossom DB, McDonald LC. The challenges posed by reemerging Clostridium difficile infection. Clin Infect Dis 2007, 45:222-227. 10.1086/518874, 17578783.
62. Snell H, Ramos M, Longo S, John M, Hussain Z. Performance of the TechLab C. DIFF CHEK-60 enzyme immunoassay (EIA) in combination with the C. difficile Tox a/B/II EIA kit, the triage C. difficile panel immunoassay, and a cytotoxin assay for diagnosis of Clostridium difficile-associated diarrhea. J Clin Microbiol 2004, 42:4863-4865. 10.1128/JCM.42.10.4863-4865.2004, 522321, 15472364.