Environmental cleaning resources and activities in Canadian acute care hospitals

Environmental cleaning resources and activities in Canadian acute care hospitals

American Journal of Infection Control 42 (2014) 490-4 Contents lists available at ScienceDirect American Journal of Infection Control American Jour...

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American Journal of Infection Control 42 (2014) 490-4

Contents lists available at ScienceDirect

American Journal of Infection Control

American Journal of Infection Control

journal homepage: www.ajicjournal.org

Major article

Environmental cleaning resources and activities in Canadian acute care hospitals Dick E. Zoutman MD, FRCPC a, b, *, B. Douglas Ford MA a, Keith Sopha CEM c, d a

Department of Pathology and Molecular Medicine, Queen’s University, Kingston, Ontario, Canada Quinte Health Care, Belleville, Canada c Canadian Association of Environmental Management, Guelph, Ontario, Canada d Homewood Health Centre, Guelph, Ontario, Canada b

Key Words: Environmental services Methicillin-resistant Staphylococcus aureus Vancomycin-resistant Enterococcus Clostridium difficile

Background: Environmental cleaning interventions have increased cleaning effectiveness and reduced antibiotic-resistant organisms in hospitals. This study examined cleaning in Canadian acute care hospitals with the goal of developing strategies to improve cleaning and reduce antibiotic-resistant organism rates. Methods: Managers most responsible for environmental services (EVS) completed an extensive online survey that assessed EVS resources and cleaning practices. Results: The response rate was 50.5%; 96 surveys were completed, representing 103 of 204 hospitals. Whereas 86.3% (82/95) of managers responsible for EVS reported their staff was adequately trained and 76.0% (73/96) that supplies and equipment budgets were sufficient, only 46.9% (45/96) reported that EVS had enough personnel to satisfactorily clean their hospital. A substantial minority (36.8%, 35/95) of EVS departments did not audit the cleaning of medical surgical patient rooms on at least a monthly basis. Cleaning audits of medical surgical patient rooms frequently included environmental marking methods in only one third (33.3%, 31/93) of hospitals and frequently included the measurement of residual bioburden in only 13.8% (13/94). Conclusion: There was a general need for increased and improved auditing of environmental cleaning in Canadian hospitals, and there were perceived EVS staffing deficits in the majority of hospitals. Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.

Antibiotic-resistant organisms (AROs) are endemic in Canadian acute care hospitals.1,2 There is considerable evidence that environmental contamination by pathogens in hospitals is associated with patients contracting infections.3-8 In studies that assessed environmental cleaning, significant cleaning deficits were found, and only half of designated surfaces in patient rooms were being effectively cleaned.9-11 Environmental cleaning interventions and enhancements have reduced ARO levels in acute care hospitals.3,12-15 The purpose of this study was to examine the state of environmental cleaning resources and practices in Canadian acute care hospitals. This study will provide a benchmark of environmental cleaning practices in Canadian acute care hospitals. The study should provide new strategies for improving the * Address correspondence to Dick E. Zoutman, MD, FRCPC, Quinte Health Care, 265 Dundas Street East, Belleville, Ontario, Canada K8N 5A9. E-mail address: [email protected] (D.E. Zoutman). This research was supported by the Canadian Association of Environmental Management through an unrestricted grant-in-aid from Wood Wyant. Conflicts of interest: None to report.

provision of environmental services and help reduce ARO rates resulting in reduced patient morbidity, mortality, and health care costs. METHODS The environmental cleaning resources and activities of environmental services (EVS) in Canadian medium to large acute care hospitals were quantitatively assessed as part of the Canadian Hospitals Environmental Services Studies (CHESS). In 2012 and the first half of 2013, the manager most responsible for EVS completed an online survey that assessed the cleaning resources and activities in their hospital in 2011. The CHESS project also included a separate online survey that assessed the working relationships of infection prevention and control programs and EVS in acute care hospitals.16 The CHESS project was reviewed and approved by the Queen’s University Research Ethics Board. The EVS survey was developed in conjunction with an expert steering committee composed of experts in infection prevention

0196-6553/$36.00 - Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajic.2014.01.013

D.E. Zoutman et al. / American Journal of Infection Control 42 (2014) 490-4

and control and environmental services. The survey was pilot tested by 6 managers who were responsible for EVS in Canadian acute care hospitals. There were French and English versions of the survey. The survey assessed EVS human, equipment, supply, and work space resources and cleaning and disinfection policies and practices. Respondents quantitatively rated the adequacy of staffing levels, the EVS staff training, and the supplies and equipment budget. Respondent addresses were obtained from the Canadian Hospital Association database, and respondents were contacted by mail. Second and third invitations to participate were mailed to nonresponders. Respondents were also contacted by e-mail when email addresses were available. Descriptive statistics were predominately used to present the data. Data were analyzed with StatView Version 5.0 (SAS Institute, Cary, NC). RESULTS The response rate was 50.5%; 96 surveys were completed, representing 103 of 204 facilities. Three surveys were received from larger health organizations each representing 2 hospitals, and 1 survey was completed on behalf of 5 hospitals. Respondents were managers responsible for EVS, also called Housekeeping or Support Services, at their hospital. Respondents’ mean environmental cleaning experience was 17.3 (standard deviation [SD], 10.3) years. 43.8% (42/96) Of respondents were certified in environmental cleaning, holding Canadian certificates such as Certificate in Environmental Management and Professional Healthcare Housekeeping certificate or had similar qualifications. Two thirds (65.6%, 63/96) of managers responsible for EVS held academic diplomas or degrees. Two thirds (67.4%, 64/95) were also responsible for departments other than EVS. Of respondents responsible for other departments, 65.7% (SD, 24.7) of their time was allocated to EVS.

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Table 1 Topics covered in environmental services introductory and ongoing training programs

Topics covered Infection control Basic cleaning techniques Hand hygiene Use of personal protective equipment Health and safety policies Waste disposal Cleaning and storage of equipment Areas of responsibility Customer service Personal hygiene Dealing with spillages

Introductory training programs (n ¼ 95), %

Ongoing training programs (n ¼ 80), %

100 100 97.9 97.9

93.8 90.0 91.3 87.5

94.7 94.7 92.6

87.5 73.8 70.0

90.4 80.9 79.8 71.3

65.0 73.8 60.0 72.5

responsibility and personal hygiene were covered the least (Table 1). Almost all (94/96) EVS departments kept records of staff participation in training and education activities. 57.3% (55/96) Of EVS departments reviewed their training programs often or always. 82.0% (78/94) Of managers responsible for EVS reported managers and supervisors who were hospital employees had received the training necessary to perform their duties satisfactorily and that 72.7% (16/22) of external contracted managers and supervisors had received the necessary training. 85.9% (79/92) Of respondents reported hospital employed cleaning staff had received the training necessary to perform their duties satisfactorily and that 73.3% (11/15) of external contracted cleaning staff had received the necessary training. 86.3% (82/95) Of respondents reported that, overall, personnel performing EVS functions in their hospital were adequately trained to satisfactorily clean the hospital to the required standards.

Human resources Equipment, supply, and work space resources Most (92.7%, 89/96) hospitals had EVS managers and supervisors employed directly by the hospital, and 24.0% (23/96) had external contracted EVS managers or supervisors. 39.3% (SD, 41.3) Of hospital-employed EVS managers and supervisors were certified, and 46.3% (SD, 42.0) of EVS external contracted managers and supervisors were certified. Most (93.8%, 90/96) hospitals had EVS cleaners employed directly by the hospital, and 15.6% (15/96) had external contracted EVS cleaners. A minority (46.9%, 45/96) of respondents reported that EVS had enough personnel to satisfactorily clean their hospital to the required standards, of which only 5.2% (5/96) strongly agreed there were sufficient EVS personnel. In hospitals in which the manager responsible for EVS agreed there were sufficient staff, there was a mean of 4.0 (SD, 1.4) beds per fulltime equivalent cleaner versus 5.0 (SD, 2.3) beds per full-time equivalent cleaner in hospitals that did not report sufficient staff, and this difference was significant (t ¼ 2.4, P ¼ .02). This calculation was based on full-time equivalent cleaners and total beds for the entire facility. All but 1 EVS department had introductory training programs for new personnel with a mean duration of 44.7 (SD, 32.3) hours with a median of 37.5 and a range of 4 to 186. Infection control, basic cleaning techniques, use of personal protective equipment, and hand hygiene were the most frequently covered topics in introductory training programs, and customer service, personal hygiene, and dealing with spillages were covered the least (Table 1). 16.7% (16/96) Of EVS departments did not have an ongoing training and professional development program. Infection control, hand hygiene, and basic cleaning techniques were the most frequently covered topics in ongoing training programs, and areas of

Almost all respondents (96.8%, 92/95) reported that their preferred hospital-grade licensed cleaning and disinfection products were used in their hospital. Hydrogen peroxide-based (71.9%, 69/96) and quaternary ammonium (63.5%, 61/96) compounds were the most frequently used disinfectants for daily cleaning, and phenolics (3.1%, 3/96) were least often used. Almost all respondents (96.8%, 92/95) reported their hospital used their preferred cleaning and disinfection equipment. Microfiber cleaning cloths were frequently used by 61.1% (58/95) of hospitals. For cleaning the average medical-surgical patient room, microfiber cleaning cloths were used in 58.3% (56/96) of hospitals followed by rags in 21.9% (21/96), manufactured cloths with edges in 16.7% (16/96), and disposable wipers in 3.1% (3/96). A minority (37.5%, 36/96) of hospitals frequently used cleaning cloths that were color coded for different applications. Vacuum cleaners with highefficiency particulate air filtration were frequently used in clinical areas in 71.3% (67/94) of hospitals. Toilet bowl brushes were used in more than 1 patient washroom in 45.8% (44/96) of hospitals, dedicated to 1 washroom in 34.4% (33/96), discarded after each use in 10.4% (10/96), and were not used in 9.4% (9/96). It was reported there were sufficient supplies of personal protective equipment for cleaning staff in almost all hospitals (97.9%, 94/96). There were clean supply rooms close to patient care areas in 89.6% (86/96) of hospitals, and there were sufficient housekeeping rooms and closets in a slim majority (55.2%, 53/96). Three quarters (76.0%, 73/96) of respondents reported their supplies and equipment budget was sufficient to clean and disinfect their hospital to standards.

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Table 2 Cleaning and disinfection practices in Canadian acute care hospitals Practices Cleaning took place according to a predetermined schedule (n ¼ 96) Cleaning schedules took into account activity taking place in an area and the risk of infection (n ¼ 96) Checklists used to ensure cleaning tasks were completed on schedule (n ¼ 96) Cleaning tasks reviewed on a regular basis to determine the ability of cleaning staff to meet demands (n ¼ 96) Worn, stained, cracked, or torn furnishings were replaced or repaired promptly (n ¼ 96) Furnishings and equipment were compatible with hospital-grade cleaning and disinfectant agents (n ¼ 95) Cleaning staff used bucket immersion for applying disinfectant to cleaning cloths (n ¼ 95) Separate cloths were used for cleaning patient washrooms (n ¼ 96) Equipment used to clean toilets in patient rooms was reused room to room (n ¼ 94) Cleaning equipment such as cloths and mop heads were cleaned and disinfected according to recommended standards (n ¼ 95) There was a clear separation of clean and dirty laundry (n ¼ 96) Waste within the hospital was transported along specified routes (n ¼ 95) Environmental Services cleaning staff adhered to Routine Practices* when cleaning patient rooms (n ¼ 95) Cleaning staff followed best practices for hand hygiene in the work environment (n ¼ 96) Environmental Services had input into the choices of surfaces and finishes in patient care areas with regard to cleanability (n ¼ 96) Environmental Services modified cleaning practices to incorporate the latest environmental cleaning evidence to prevent infections (n ¼ 96)

Always, %

Often, %

Sometimes, %

Rarely, %

Never, %

58.3 77.1

35.4 15.6

5.2 7.3

1.0 0

0 0

27.1 19.8

32.3 45.8

26.0 26.0

8.3 8.3

6.3 0

13.5 14.7

38.5 48.4

32.3 29.5

13.5 6.3

2.1 1.0

65.3 71.9 8.5 90.5

12.6 1.0 18.1 5.3

1.0 1.0 9.6 4.2

7.4 1.0 7.4 0

13.7 25.0 56.4 0

84.4 55.8 80.0

12.5 26.3 20.0

2.1 5.3 0

0 6.3 0

1.0 6.3 0

47.9 10.4

43.8 33.3

6.3 39.6

2.1 9.4

0 7.3

45.8

42.7

9.4

2.1

0

*Routine Practices is the system of infection prevention and control practices recommended by the Public Health Agency of Canada to be used to prevent and control transmission of microorganisms in health care settings.

100

% Hospitals

75

82

66 53

50 12 22

25

22 25

8 10

0 IV Poles Always/Often

Wheelchairs

Sometimes/Rarely/Never

Glucose Meters Not EVS Responsibility

Fig 1. Cleaning of medical and transport equipment.

Cleaning and disinfection policies and practices Almost all respondents reported their hospital had written procedures for cleaning patient rooms for patients positive for methicillin-resistant Staphylococcus aureus (99.0%, 95/96), vancomycin-resistant Enterococcus (97.9%, 93/95), and Clostridium difficile (CDI) (98.9%, 94/95). The vast majority of hospitals had written policies and procedures for cleaning spills of bodily fluids (93.7%, 89/95), for dealing with biomedical waste (92.6%, 88/95), for cleaning specialized areas such as operating rooms (91.7%, 88/96), and for attendance management that make it clear cleaning staff do not come into work when acutely ill with a possible infection (88.5%, 85/96). A substantial minority (38.9%, 37/95) of hospitals did not have written policies for ongoing review of cleaning and disinfection procedures. In 93.8% (90/96) of hospitals, cleaning frequently took place according to a predetermined schedule (Table 2). 59.4% (57/96) Of hospitals used cleaning task checklists frequently to ensure cleaning tasks were completed on schedule. Two thirds (65.6%, 63/96) of hospitals reviewed cleaning tasks on a regular basis to determine the ability of cleaning staff to meet cleaning demands. In 88.5% (85/ 96) of hospitals, EVS frequently modified cleaning practices to incorporate the latest environmental cleaning evidence to prevent infections.

In 43.8% (42/96) of hospitals, EVS had frequent input into the choices of surfaces and finishes in patient care areas with regard to cleanability (Table 2). In 63.2% (60/95) of hospitals, the furnishings and equipment were compatible with hospital-grade cleaning and disinfectant agents. 79.2% (76/96) Of hospitals did not have carpets in patient care areas. Of the hospitals that did have carpets in patient care areas, 60.0% (12/20) frequently used hospital-grade sanitizing agents to clean the carpets. Cleaning staff frequently used bucket immersion, soaking cloths in a bucket with disinfectant, for applying disinfectant to cleaning cloths in 77.9% (74/95) of hospitals (Table 2). Separate cloths were used for cleaning patient washrooms in 72.9% (70/96) of hospitals. In one fourth (26.6%, 25/94) of hospitals, the equipment used to clean toilets in patient rooms was often or always reused room to room. In two-thirds (66.3%, 63/95) of hospitals, intravenous poles were frequently cleaned by EVS cleaning staff, and, in 22.1% (21/95) of hospitals, it was reported that cleaning intravenous poles was not the responsibility of EVS (Fig 1). In 53.1% (51/96) and 82.1% (78/95), respectively, of hospitals, the cleaning of transport equipment such as wheelchairs and the cleaning of glucose meters were reported not to be EVS responsibilities.

Environmental cleaning practices and patient ARO status Cleaning and related activities were more intensive for patients positive for AROs and were most intensive for patients positive for CDI (Table 3). High-touch objects in patient rooms for patients positive for CDI were cleaned twice a day in 69.8% (67/96) of hospitals, and, for patients without AROs, high-touch objects were cleaned twice a day in 8.4% (8/95) hospitals. The cleaning of an isolation room for CDI-positive patients frequently included the use of a checklist in 65.2% (60/92) of hospitals and included the use of a checklist 46.1% (41/89) of the time for patients without AROs. After CDI-positive patients were discharged from isolation rooms, almost all hospitals (99.0%, 95/96) always subjected isolation rooms to terminal cleaning, whereas, for patients without AROs, 73.7% (70/95) of hospitals always subjected isolation rooms to terminal cleaning.

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493

Table 3 Environmental cleaning practices and patient antibiotic resistant organism status

Practices The frequency with which high-touch objects in patient rooms were cleaned for patients with different antibiotic resistant-organism (ARO) status No ARO (n ¼ 95) Vancomycin-resistant Enterococcus (VRE) positive (n ¼ 95) Methicillin-resistant Staphylococcus aureus (MRSA) positive (n ¼ 93) Clostridium difficile positive (n ¼ 96) Practices

Twice a day, %

Daily, %

Every second day, %

Weekly, %

Less than weekly, %

8.4 37.9 25.8 69.8

90.5 62.1 74.2 30.2

1.0 0 0 0

0 0 0 0

0 0 0 0

Always, %

Often, %

Sometimes, %

Rarely, %

Never, %

23.6 34.8 32.6 40.2

22.5 26.1 25.0 25.0

6.7 3.3 4.3 4.3

11.2 8.7 10.9 5.4

36.0 27.2 27.2 25.0

17.8 28.0 25.3 33.3

23.3 29.0 28.6 29.0

26.7 17.2 19.8 17.2

13.3 9.7 9.9 6.5

18.9 16.1 16.5 14.0

73.7 97.9 94.8 99.0

11.6 0 2.1 0

9.5 1.0 2.1 0

3.2 1.0 1.0 1.0

2.1 0 0 0

Weekly, %

Monthly, %

Quarterly, %

Twice a year, %

Yearly, %

32.6

30.5

21.1

10.5

5.3

Always, %

Often, %

Sometimes, %

Rarely, %

Never, %

19.4

14.0

23.7

9.7

33.3

4.3

9.6

13.8

12.8

59.6

39.4 12.5

28.7 45.8

17.0 28.1

11.7 8.3

3.2 5.2

12.6 57.3

25.3 25.0

33.7 12.5

15.8 3.1

12.6 2.1

The cleaning of an isolation room for patients with different ARO status included the use of a checklist No ARO (n ¼ 89) VRE positive (n ¼ 92) MRSA positive (n ¼ 92) C difficile positive (n ¼ 92) Cleaning records of isolation rooms for patients with different ARO status reviewed for completeness and compliance No ARO (n ¼ 90) VRE positive (n ¼ 93) MRSA positive (n ¼ 91) C difficile positive (n ¼ 93) After patients were discharged from isolation rooms, the isolation rooms were subjected to terminal cleaning No ARO (n ¼ 95) VRE positive (n ¼ 96) MRSA positive (n ¼ 96) C difficile positive (n ¼ 96)

Table 4 Environmental cleaning audit practices in Canadian acute care hospitals

Practices Frequency with which cleaning in medical surgical patient rooms was audited (n ¼ 95)

Environmental marking methods were used in the auditing of cleaning of medical surgical patient rooms (n ¼ 93)* Auditing of cleaning of medical surgical patient rooms included measurement of residual bioburden (n ¼ 94)y Dispensing systems audited on a routine basis (n ¼ 94) Cleanliness of housekeeping closets and equipment was audited (n ¼ 96) Environmental Services audited hand hygiene of cleaning staff (n ¼ 95) Results of cleaning audits were fed back to cleaning staff with an action plan to correct deficits (n ¼ 96) *Fluorescent marking. Environmental culture, adenosine triphosphate bioluminescence.

y

Cleaning audit practices The environmental cleaning of an average medical surgical patient room was audited weekly in 32.6% (31/95) of hospitals and monthly in 30.5% (29/95) (Table 4). The auditing of cleaning of medical surgical patient rooms frequently included environmental marking methods such as fluorescent marking in one third (33.3%, 31/93) of hospitals and frequently included the measurement of residual bioburden (environmental culture, adenosine triphosphate bioluminescence) in 13.8% (13/94). The results of cleaning audits were frequently fed back to cleaning staff with an action plan to correct deficits in 82.3% (79/96) of hospitals. EVS working relationship with infection prevention and control All but 1 manager most responsible for EVS (95/96) agreed that EVS and Infection Prevention and Control cooperated well with one

another at their hospital. The vast majority of EVS respondents (95.8%, 92/96) reported that cleaning and disinfection products were frequently chosen in consultation with Infection Prevention and Control and that Infection Prevention and Control was frequently consulted before making changes to cleaning procedures and technologies (94.8%, 91/96).

DISCUSSION This is the first Canada-wide examination of environmental cleaning in acute care hospitals and provides a benchmark of the cleaning and disinfection resources and practices in Canadian acute care hospitals. The good response rate to the lengthy and comprehensive survey permits generalizations to the state of environmental cleaning in medium and large acute care hospitals across Canada.

494

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In Canadian hospitals, there was a general lack of cleaning practice reviews and audits. One third of hospitals did not review cleaning tasks on a regular basis to determine the ability of cleaning staff to meet cleaning demands. A substantial minority of EVS departments did not have written policies for ongoing review of cleaning and disinfection procedures and did not audit the environmental cleaning of patient rooms on at least a monthly basis. The auditing of the cleaning of patient rooms infrequently included environmental marking methods and more infrequently the measurement of residual bioburden. Environmental marking and residual bioburden are recommended components of cleaning audits.6 A substantial majority of managers responsible for EVS reported their staff was well trained and supply and equipment budgets were adequate; however, less than half reported they had sufficient staff to clean their hospitals to the desired standards. Staffing deficits translate into less frequent cleaning and corners being cut. Environmental cleaning effectiveness in a study of 36 US hospitals was positively associated with EVS staffing budgets.10 In the present study, managers most responsible for EVS were more likely to report they had sufficient staff to clean their hospitals when they had fewer beds per cleaner. In a study in which an additional cleaner was added to wards, there were improved cleaning levels and decreased methicillin-resistant Staphylococcus aureus rates that rebounded when the additional cleaner was removed.15 There are no recommended staffing levels for cleaners in hospitals in environmental cleaning guidelines.5,6 There is a need for further research to determine optimal EVS staffing levels. There were cleaning practices of particular concern. In a substantial minority of hospitals, toilet bowl brushes used in the washrooms in medical surgical patient rooms were used in more than one washroom. It is recommended that toilet bowl brushes not be used in more than one washroom.6 Another area of concern was the cleaning frequency of rooms with patients who are CDI positive. It is recommended their rooms be cleaned twice a day, yet this was not the practice in almost one-third of hospitals.6 The majority of respondents reported that cleaning blood glucose meters and wheelchairs were not EVS responsibilities. Although we did not assess this, one would probably find there were gray areas for EVS, nursing, and other health care staff about whose responsibility it was to clean the various pieces of medical equipment in patient care areas. In a study in which medical equipment in patient care areas was examined for biologic contaminants, the majority of items were found to be contaminated, including blood glucose meters.17 There is a need to designate who is responsible to clean what with regard to equipment in patient care areas. A limit of the present study was that the examination of EVS resources and activities relied on managers most responsible for EVS. Although these managers know best the state of EVS in their hospital, their responses may have a positive bias. It appears though that respondents were willing to acknowledge problem areas and deviations from recommended cleaning practices in their hospitals. There was an underrepresentation of hospitals that used contracted EVS services. The response from the provinces of British Columbia and Alberta, where environmental cleaning is more frequently contracted out, was less than in other provinces. The authors have 2 major recommendations. There is a clear need for increased and improved auditing of environmental cleaning in hospitals. Without comprehensive auditing programs in place,

hospital administrators cannot be certain that their hospital is sufficiently clean for infection prevention and control purposes. Second, there appears to be the need for more cleaning staff in the majority of Canadian hospitals. EVS staffing deficits mean that the cleaning necessary to prevent and control nosocomial infections will not be accomplished with the requisite frequency and thoroughness. Acknowledgment The authors thank the following members of the CHESS Steering Committee for their contributions to the project: Réjean Losier, Jean Francois Champagne, Christine Moore, Mike Nosko, Louis Anastasakos, Rob Scott, A. Brad Moser, Geoff Taylor, and Joanne Embree. References 1. Zoutman DE, Ford BD. A comparison of infection control program resources, activities, and antibiotic resistant organism rates in Canadian acute care hospitals in 1999and 2005: pre- and post-severe acute respiratory syndrome. Am J Infect Control 2008;36:711-7. 2. Simor AE, Williams V, McGeer A, Raboud J, Larios O, Weiss K, et al, Community and Hospital Infection Control Association-Canada. Prevalence of colonization and infection with methicillin-resistant Staphylococcus aureus and vancomycin-resistant Enterococcus and of Clostridium difficile infection in canadian hospitals. Infect Control Hosp Epidemiol 2013;34:687-93. 3. Rodríguez-Baño J, García L, Ramírez E, Martínez-Martínez L, Muniain MA, Fernández-Cuenca F, et al. Long-term control of hospital wide, endemic multidrug-resistant Acinetobacter baumannii through a comprehensive “bundle” approach. Am J Infect Control 2009;37:715-22. 4. Dancer SJ. The role of environmental cleaning in the control of hospitalacquired infection. J Hosp Infect 2009;73:378-85. 5. Centers for Disease Control and Prevention, Healthcare Infection Control Practices Advisory Committee. Guidelines for environmental infection control in health-care facilities. MMWR 2003;(RR-107):52:1-48. 6. Provincial Infectious Disease Advisory Committee (PIDAC). Best practices for cleaning, disinfection, and sterilization in all health care settings. Toronto: Ministry of Health and Long-term Care; 2006. 7. Otter JA, Yezli S, Salkeld JAG, French GL. Evidence that contaminated surfaces contribute to the transmission of hospital pathogens and an overview of strategies to address contaminated surfaces in hospital settings. Am J Infect Control 2013;41:S6-11. 8. Weber DJ, Anderson DJ, Sexton DJ, Rutala WA. Role of the environment in the transmission of Clostridium difficile in health care facilities. Am J Infect Control 2013;41:S105-10. 9. Carling PC, Parry MF, Von Beheren SM, Healthcare Environmental Hygiene Study Group. Identifying opportunities to enhance environmental cleaning in 23 acute care hospitals. Infect Control Hosp Epidemiol 2008;29:1-7. 10. Carling PC, Parry MM, Rupp ME, Po JL, Dick B, Von Beheren S, Healthcare Environmental Hygiene Study Group. Improving cleaning of the environment surrounding patients in 36 acute care hospitals. Infect Control Hosp Epidemiol 2008;29:1035-41. 11. 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;38:1054-9. 12. Goodman ER, Platt R, Bass R, Onderdonk AB, Yokoe DS, Huang SS. Impact of an environmental cleaning intervention on the presence of methicillin-resistant Staphylococcus aureus and vancomycin-resistant Enterococci on surfaces in intensive care unit rooms. Infect Control Hosp Epidemiol 2008;29:593-9. 13. Donskey CJ. Does improving surface cleaning and disinfection reduce health care-associated infections? Am J Infect Control 2013;41:S12-9. 14. Guerrero DM, Carling PC, Jury LA, Ponnada S, Nerandzic MM, Donskey CJ. Beyond the Hawthorne effect: reduction of Clostridium difficile environmental contamination through active intervention to improve cleaning practices. Infect Control Hosp Epidemiol 2013;34:524-6. 15. 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. 16. Zoutman DE, Ford BD, Sopha K. The working relationships of infection prevention and control programs and environmental services and associations with antibiotic-resistant organisms in Canadian acute care hospitals. Am J Infect Control 2014;42:349-52. 17. Anderson RE, Young V, Stewart M, Robertson C, Dancer SJ. Cleanliness audit of clinical surfaces and equipment: who cleans what? J Hosp Infect 2011;78:178-81.