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 Infectious Diseases

J Scott Weese²  Richard J Reid-Smith²  Olaf Berke⁶  Giovanna Zinken¹  Karen Straus⁵  William A Ciccotelli⁴  David L Pearl³  Meredith C Faires³ 

[1] Infection Prevention and Control, St. Mary’s General Hospital, Kitchener, ON, Canada;Department of Pathobiology, University of Guelph, Guelph, ON, Canada;Department of Population Medicine, University of Guelph, Guelph, ON, Canada;Department of Pathology and Molecular Medicine, McMaster University, Hamilton, ON, Canada;Infection Prevention and Control, Grand River Hospital, Kitchener, ON, Canada;Department of Mathematics and Statistics, University of Guelph, Guelph, ON, Canada

关键词: Ribotyping;    Spa typing;    Livestock-associated MRSA strain;    Risk factors;    General environment;    Hospital;    Clostridium difficile;    Methicillin-resistant Staphylococcus aureus;   

Others  :  1159600
DOI  :  10.1186/1471-2334-12-290

 received in 2012-06-28, accepted in 2012-11-01,  发布年份 2012

【 摘 要 】

Background

The hospital environment has been suggested as playing an important role in the transmission of hospital-associated (HA) pathogens. However, studies investigating the contamination of the hospital environment with methicillin-resistant Staphylococcus aureus (MRSA) or Clostridium difficile have generally focused on point prevalence studies of only a single pathogen. Research evaluating the roles of these two pathogens, concurrently, in the general hospital environment has not been conducted. The objectives of this study were to determine the prevalence and identify risk factors associated with MRSA and C. difficile contamination in the general environment of three community hospitals, prospectively.

Methods

Sampling of environmental surfaces distributed over the medicine and surgical wards at each hospital was conducted once a week for four consecutive weeks. Sterile electrostatic cloths were used for environmental sampling and information regarding the surface sampled was recorded. For MRSA, air sampling was also conducted. Enrichment culture was performed and spa typing was performed for all MRSA isolates. For C. difficile, isolates were characterized by ribotyping and investigated for the presence of toxin genes by PCR. Using logistic regression, the following risk factors were examined for MRSA or C. difficile contamination: type of surface sampled, surface material, surface location, and the presence/absence of the other HA pathogen under investigation.

Results

Overall, 11.8% (n=612) and 2.4% (n=552) of surfaces were positive for MRSA and C. difficile, respectively. Based on molecular typing, five different MRSA strains and eight different C. difficile ribotypes, including ribotypes 027 (15.4%) and 078 (7.7%), were identified in the hospital environment. Results from the logistic regression model indicate that compared to computer keyboards, the following surfaces had increased odds of being contaminated with MRSA: chair backs, hand rails, isolation carts, and sofas.

Conclusions

MRSA and C. difficile were identified from a variety of surfaces in the general hospital environment.

Several surfaces had an increased risk of being contaminated with MRSA but further studies regarding contact rates, type of surface material, and the populations using these surfaces are warranted.

【 授权许可】

   
2012 Faires et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

【 参考文献 】

• [1]Klevens RM, Morrison MA, Nadle J, Petit S, Gershman K, Ray S, Harrison LH, Lynfield R, Dumyati G, Townes JM, Craig AS, Zell ER, Fosheim GE, McDougal LK, Carey RB, Fridkin SK, Active Bacterial Core surveillance (ABCs) MRSA Investigators: Invasive methicillin-resistant Staphylococcus aureus infections in the United States. J Am Med Assoc 2007, 298:1763-1771.
• [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.
• [3]Embil JM, McLeod JA, Al-Barrak AM, Thompson GM, Aoki FY, Witwicki EJ, Stranc MF, Kabani AM, Nicoll DR, Nicolle LE: An outbreak of methicillin resistant Staphylococcus aureus on a burn unit: potential role of contaminated hydrotherapy equipment. Burns 2001, 27:681-688.
• [4]Eggertson L: C. difficile outbreaks in Gatineau, Sault Ste. Marie. Can Med Assoc J 2007, 177:334-335.
• [5]Goetghebeur M, Landry PA, Han D, Vicente C: Methicillin-resistant Staphylococcus aureus: A public health issue with economic consequences. Can J Infect Dis Med Microbiol 2007, 18:27-34.
• [6]Miller MA, Hyland M, Ofner-Agostini M, Gourdeau M, Ishak M, Canadian Hospital Epidemiology Committee, Canadian Nosocomial Infection Surveillance Program: Morbidity, mortality, and healthcare burden of nosocomial Clostridium difficile – associated diarrhea in Canadian hospitals. Infect Control Hosp Epidemiol 2002, 23:137-140.
• [7]Shaughnessy MK, Micielli RL, DePestel DD, Arndt J, Strachan CL, Welch KB, Chenoweth CE: Evaluation of hospital room assignment and acquisition of Clostridium difficile infection. Infect Control Hosp Epidemiol 2011, 32:201-206.
• [8]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. BioMed Central Full Text
• [9]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 healthcare setting. Infect Control Hosp Epidemiol 2008, 29:723-729.
• [10]Dancer SJ: Mopping up hospital infection. J Hosp Infect 1999, 43:85-100.
• [11]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 Enviro 2009, 212:209-215.
• [12]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.
• [13]Dumford DM 3rd, 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.
• [14]Martirosian G: Recovery of Clostridium difficile from hospital environments. J Clin Micro 2006, 44:1202-1203.
• [15]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.
• [16]Malamou-Ladas H, O’Farrell S, Nash JQ, Tabaqchali S: Isolation of Clostridium difficile from patients and the environment of hospital wards. J Clin Pathol 1983, 36:88-92.
• [17]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.
• [18]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.
• [19]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.
• [20]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.
• [21]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. BioMed Central Full Text
• [22]Samore MH, Venkataraman L, DeGirolami PC, Arbeit RD, Karchmer AW: Clinical and molecular epidemiology of sporadic and clustered cases of nosocomial Clostridium difficile diarrhea. Am J Med 1996, 100:32-40.
• [23]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.
• [24]eGenomics. http://tools.egenomics.com webcite
• [25]Ridom SpaServer. http://www.spaserver.ridom.de webcite
• [26]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.
• [27]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.
• [28]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.
• [29]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.
• [30]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.
• [31]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.
• [32]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.
• [33]Dohoo IR, Martin W, Stryhn H: Model-building strategies. Prince Edward Island: AVC, Inc, Charlottetown; 2003:317-334. [Veterinary Epidemiologic Research]
• [34]Dohoo IR, Martin W, Stryhn H: Confounder bias: analytic control and matching. Prince Edward Island: AVC, Inc, Charlottetown; 2003:235-271. [Veterinary Epidemiologic Research]
• [35]Shelly MJ, Scanlon TG, Ruddy R, Hannan MM, Murray JG: Meticillin-resistant Staphylococcus aureus (MRSA) environmental contamination in a radiology department. Clin Rad 2011, 66:861-864.
• [36]Dancer SJ: Importance of the environment in meticillin-resistant Staphylococcus aureus acquisition: the case for hospital cleaning. Lancet Infect Dis 2008, 8:101-113.
• [37]Dancer SJ, Coyne M, Speekenbrink A, Samavedam S, Kennedy J, Wallace PG: MRSA acquisition in an intensive care unit. Am J Infect Control 2006, 34:10-17.
• [38]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 Epi 2002, 23:641-647.
• [39]Kaatz GW, Gitlin SD, Schaberg DR, Wilson KH, Kauffman CA, Seo SM, Fekety R: Acquisition of Clostridium difficile from the hospital environment. Am J Epidemiol 1988, 127:1289-1294.
• [40]Gehanno JF, Louvel A, Nouvellon M, Caillard JF, Pestel-Caron M: Aerial dispersal of methicillin-resistant Staphylococcus aureus in hospital rooms by infected or colonised patients. J Hosp Infect 2009, 71:256-262.
• [41]Neely AN, Maley MP: Survival of enterococci and staphylococci on hospital fabrics and plastic. J Clin Microbiol 2000, 38:724-726.
• [42]Simor AE, Ofner-Agostini M, Bryce E, McGeer A, Paton S, Mulvey MR, Canadian Hospital Epidemiology Committee and Canadian Nosocomial Infection Surveillance Program, Health Canada: Laboratory characterization of methicillin-resistant Staphylococcus aureus in Canadian hospitals: Results of 5 years of National Surveillance, 1995-1999. J Infect Dis 2002, 186:652-660.
• [43]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.
• [44]Anderson MEC, Lefebvre SL, Weese JS: Evaluation of prevalence and risk factors for methicillin-resistant Staphylococcus aureus colonization in veterinary personnel attending an international equine veterinary conference. Vet Microbiol 2008, 129:410-417.
• [45]Price LB, Stegger M, Hasman H, Aziz M, Larsen J, Andersen PS, Pearson T, Waters AE, Foster JT, Schupp J, Gillece J, Driebe E, Liu CM, Springer B, Zdovc I, Battisti A, Franco A, Zmudzki J, Schwarz S, Butaye P, Jouy E, Pomba C, Porrero MC, Ruimy R, Smith TC, Robinson DA, Weese JS, Arriola CS, Yu F, Laurent F, Keim P, Skov R, Aarestrup FM: Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. MBio 2012, 3:e00305-e00311.
• [46]van der Mee-Marquet N, François P, Domelier-Valentin AS, Coulomb F, Decreux C, Hombrock-Allet C, Lehiani O, Neveu C, Ratovohery D, Schrenzel J, Quentin R, Bloodstream Infection Study Group of Réseau des Hygiénistes du Centre (RHC): Emergence of unusual bloodstream infections associated with pig-borne-like Staphylococcus aureus ST398 in France. Clin Infect Dis 2011, 52:152-153.
• [47]van Belkum A, Melles DC, Peeters JK, van Leeuwen WB, van Duijkeren E, Huijsdens XW, Spalburg E, de Neeling AJ, Verbrugh HA, Dutch Working Party on Surveillance and Research of MRSA-SOM: Methicillin-resistant and –susceptible Staphylococcus aureus sequence type 398 in pigs and humans. Emerg Infect Dis 2008, 14:479-483.
• [48]Bhat M, Dumortier C, Taylor BS, Miller M, Vasquez G, Yunen J, Brudney K, Sánchez-E J, Rodriguez-Taveras C, Rojas R, Leon P, Lowy FD: Staphylococcus aureus ST398, New York City and Dominican Republic. Emerg Infect Dis 2009, 15:285-287.
• [49]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. BioMed Central Full Text
• [50]Khanna T, Friendship R, Dewey C, Weese JS: Methicillin-resistant Staphylococcus aureus colonization in pigs and pig farmers. Vet Microbiol 2008, 128:298-303.
• [51]Tokateloff N, Manning ST, Weese JS, Campbell J, Rothenburger J, Stephen C, Bastura V, Gow SP, Reid-Smith R: Prevalence of methicillin-resistant Staphylococcus aureus colonization in horses in Saskatchewan, Alberta, and British Columbia. Can Vet J 2009, 50:1177-1180.
• [52]Floras A, Lawn K, Slavic D, Golding GR, Mulvey MR, Weese JS: Sequence type 398 meticillin-resistant Staphylococcus aureus infection and colonisation in dogs. Vet Rec 2010, 166:826-827.
• [53]Golding GR, Bryden L, Levett PN, McDonald RR, Wong A, Wylie J, Graham MR, Tyler S, Van Domselaar G, Simor AE, Gravel D, Mulvey MR: Livestock-associated methicillin-resistant Staphylococcus aureus sequence type 398 in humans, Canada. Emerg Infect Dis 2010, 16:587-594.
• [54]Wassenberg MW, Bootsma MC, Troelstra A, Kluytmans JA, Bonten MJ: Transmissibility of livestock-associated methicillin-resistant Staphylococcus aureus (ST398) in Dutch hospitals. Clin Microbiol Infect 2011, 17:316-319.
• [55]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.
• [56]Dolan A, Bartlett M, McEntee B, Creamer E, Humphreys H: Evaluation of different methods to recover methicillin-resistant Staphylococcus aureus from hospital environmental surfaces. J Hosp Infect 2011, 79:227-230.
• [57]Murphy CP, Reid-Smith RJ, Boerlin P, Weese JS, Prescott JF, Janecko N, Hassard L, McEwen SA: Escherichia coli and other selected veterinary and zoonotic pathogens isolated from environmental sites in companion animal veterinary hospitals in southern Ontario. Can Vet J 2010, 51:963-972.
• [58]Obee P, Griffith CJ, Cooper RA, Bennion NE: An evaluation of different methods for the recovery of methicillin-resistant Staphylococcus aureus from environmental surfaces. J Hosp Infect 2007, 65:35-41.
• [59]Buggy BP, Wilson KH, Fekety R: Comparison of methods for recovery of Clostridium difficile from an environmental surface. J Clin Microbiol 1983, 18:348-352.
• [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.