1. Monitoring Cleaning and Disinfection Practices
John M. Boyce, MD
Director, Hospital Epidemiology & Infection Control
Yale-New Haven Hospital
and
Clinical Professor of Medicine
Yale University School of Medicine
New Haven, CT
Disclosures: Consultant to Clorox Corporation, 3M Corporation, BIOQUELL PLC.
Honoraria from Clorox, 3M. Research support from 3M, Clorox, Crothall

2. Advances in Environmental Cleaning/Disinfection
Approaches to monitoring cleaning practices
Coating surfaces with antimicrobial metals
Applying products with long-term antimicrobial activity to suppress contamination of surfaces

3. Role of Environment in Transmission of Healthcare-Associated Pathogens
Numerous investigators have provided evidence that contaminated environmental surfaces can contribute to transmission of healthcare-associated infections
Hota B Clin Infect Dis 2004;39:1182
Boyce JM J Hosp Infect 2007;65 (Suppl 2):50
Weber DJ et al. Am J Infect Control 2010;38 (5 Suppl 1):S25
Weber DJ and Rutala WA Infect Control Hosp Epidemiol 2011;32:207
Otter JA et al. Infect Control Hosp Epidemiol 2011;32:687
Weber DJ et al. Curr Opin Infect Dis 2013;26:338

4. Improving Cleaning/Disinfection Practices
Pay close attention to cleaning and disinfection of high-touch surfaces in patient-care areas
Ensure compliance by housekeeping staff with cleaning and disinfection procedures
Disinfect (or clean) environmental surfaces on a regular basis, and when surfaces are visibly soiled
Sehulster L et al. MMWR Recomm Rep 2003;52(RR-10):1
Rutala WA, Weber DJ et al. HICPAC Guideline for
Disinfection and Sterilization in Healthcare Facilities, 2008

5. Methods for Assessing Cleaning Practices
Visual inspection of surfaces
Check lists sometimes used
Observation of housekeeper technique
Fluorescent marker system
Aerobic colony counts
ATP bioluminescence assays
Griffith CJ et al. J Hosp Infect 2000;45:19
Cooper RA et al. Am J Infect Control 2007;35:338
Dancer SJ J Hosp Infect 2009;73:378
Luick L et al. Am J Infect Control 2013;41:751

6. Check lists to Improve Cleaning Practices

7. Visual Inspection of Surfaces
Simple, can be conducted in any facility
Usually performed by housekeeping managers
Assess surfaces to detect visible dirt/stains
Problem: Surfaces that appeared clean by visual inspection often failed to pass criteria for cleanliness when tested by objective measures: aerobic colony counts or ATP bioluminescence
Griffith CJ et al. J Hosp Infect 2000;45:19
Cooper RA et al. AJIC 2007;35:338
Luick L et al. AJIC 2013;41:751

8. Observation of Housekeeper Technique
Covert or overt observation of housekeepers during routine cleaning/disinfection activities
Establish variations in amount of time spent cleaning or disinfecting high-touch objects
Determine number of disinfectant wipes used/room
Detect which surfaces are not wiped adequately
Establish if housekeepers are allowing disinfectant to remain on surfaces for appropriate contact time
Hayden MK et al. Clin Infect Dis 2006;42:1552
Boyce JM et al. ICHE 2010;31:99
Guerrero D et al Decennial conference, Abstr 60

9. Observation and Supervision of Housekeeper Performance
Investigators applied C. difficile spores (non-toxigenic) to 3 high-touch surfaces in mulitple rooms before terminal cleaning
Phase 1: housekeepers were not observed and were unaware
Phase 2: Housekeeper education and direct monitoring of practice
Phase 3: Direct supervision by investigator, reinforcement of education and real-time feedback
Results: Education and passive observation sigificantly improved disinfection
Further significant reduction in contamination occurred with direct supervision and real-time feedback significantly improved disinfection
Percent of inoculated surfaces positive
for C. difficile after cleaning, with
different interventions
Guerrero DM et al. ICHE 2013;34:524

10. Aerobic Colony Counts Methods of culturing environmental surfaces
Moistened swab inoculated onto agar +/- broth enrichment
Most useful for irregularly shaped surfaces
Agar contact plates (Rodac)
Recommended for flat surfaces
Yield number of colonies per square inch or centimeter
Currently, no standard methods for how to obtain & to process specimens for aerobic colony counts
Provide data on contamination by important pathogens
No accepted criteria for defining a surface as “clean” by using aerobic colony counts
Sehulster L et al. MMWR Recomm Rep 2003;52(RR-10):1
Dancer SJ J Hosp Infect 2004;56:10

11. Moistened Swab with Direct Plating
Use moistened swab to sample surfaces
If defined area not sampled; results are at
best semi-quatitative
If a defined area is sampled using a template,
results are quantitative (CFUs/cm2); preferable
Moistening (wetting) agents include normal saline,
broth media (most common), or broth containing
disinfectant neutralizer(s)
Swab is used to directly inoculate non-selective or
selective media, followed by incubation x 48 hrs
Useful for sampling irregularly shaped objects,
medical equipment, hard to reach areas, HCP hands
VRE on Bedside Rail
Lemmen SW et al. Int J Hyg Environ Health 2001;203:245
Duckro AN et al. Arch Intern Med 2005;165:302
Donskey CJ et al. N Engl J Med 2009;360:e3
Hand imprint culture

12. Aerobic Colony Counts Using RODAC Plates
RODAC plates are small petri plates filled with agar in order to provide convex surface for sampling flat environmental surfaces
Agar surface is pressed against a flat surface, plate is incubated
Advantages:
Very easy to perform; more standardized approach than others
Results can be expressed as CFUs/cm2 (quantitative result)
May be preferable for detecting Gram-positive bacteria (e.g., MRSA)
Neutralizer – containing media (Dey-Engley) are available
Disadvantages:
Greater cost; limited media available; sample small area per plate
Obee P et al. J Hosp Infect 2007;65:35
Rutala WA et al. ICHE 2010;31:1025
Galvin S et al. J Hosp Infect 2012;82:143
Havill NL Am J Infect Control 2013;41:S26
Anderson DJ et al. ICHE 2013;34:466

13. RODAC Plates Before Cleaning After Cleaning
Cultures of Overbed Table
Before Cleaning After Cleaning
Boyce JM et al. SHEA 2011, Abstr 4711

14. Fluorescent Marker System for Monitoring Cleaning Practices
Prospective study conducted in 3 hospitals
12 high-touch objects in patient rooms were marked with invisible fluorescent solution after terminal cleaning
Marks moistened by disinfectant spray could be removed by wiping surface for 5 seconds with light pressure
After at least 2 patients had occupied the rooms and rooms were terminally cleaned, target surfaces were evaluated using a portable UV light to see if the marker had been wiped off
Intervention: education and feedback given to cleaning staff
Carling PC et al. J Hosp Infect 2008;68:3

15. Improving Cleaning Practices by Using Fluorescent Marker System
1404 objects were evaluated before the intervention
744 objects were evaluated after the intervention
Proportion of objects cleaned
Before intervention: 47%
After interventions: %
Technique improved in all 3 hospitals (p < 0.001)
This method has been used to improve cleaning practices in several larger studies
Carling PC et al. Clin Infect Dis 2006;42:385
Carling PC et al. Infect Control Hosp Epidemiol 2008;29:1
Carling PC et al. Crit Care Med 2010;38:1054

16. Improving Cleaning Practices by Using Fluorescent Marker System
Prospective study in 36 acute-care hospitals
Hospital size: 25 to 721 beds
Fluorescent markers applied to 14 types of objects before terminal room disinfection
20,646 surfaces checked after terminal cleaning
Intervention included providing housekeepers with performance feedback
Carling PC et al. ICHE 2008;29:1035

17. Evaluating Cleaning Measures in an ICU Using Fluorescent Marker System
Prospective study of the impact of cleaning interventions on environmental contamination by MRSA and VRE
Intervention consisted of
Change from use of pour bottles to bucket immersion of cleaning cloths
Educational campaign for housekeepers
Feedback regarding adequacy of terminal room cleaning
15 surfaces in rooms were marked with a fluorescent dye, and surfaces in patient rooms were cultured for MRSA and VRE
Results:
Removal of fluorescent dye occurred on
44% of surfaces during baseline period
71% of surfaces during intervention period
Cultures (+) for MRSA or VRE decreased from 45% at baseline to 27%
Goodman ER et al. Infect Control Hosp Epidemiol 2008;29:593

18. Evaluating Cleaning Measures in an ICU Using Fluorescent Marker System
Goodman ER et al. Infect Control Hosp Epidemiol 2008;29:593

19. Monitoring Hospital Cleanliness Using ATP Bioluminescence Assays
ATP bioluminescence assays have been used to monitor cleanliness of surfaces in hospitals
Daily cleaning or terminal cleaning
Assess variations in housekeeper performance
Griffith CL et al. J Hosp Infect 2000;45:19
Malik RE et al. AJIC 2003;31:181
Cooper RA et al. AJIC 2007;35:338
Lewis T et al. J Hosp Infect 2008;69:156
Boyce JM et al. Infect Control Hosp Epidemiol 2009;30:678
Boyce JM et al. Infect Control Hosp Epidemiol 2010;31:99
Moore G et al. AJIC 2010;38:617
Havill NL et al. AJIC 2011;39:602
Anderson RE et al. J Hosp Infect 2011;78:178

20. ATP Bioluminescence Method
Step Step Step 3
Use special swab Place swab in Place tube in luminometer
to sample surface reaction tube Results: Relative Light Units

21. Assessing Terminal Cleaning Practices Using 3 Methods
Prospective study to compare how many surfaces would be considered clean, based on
Aerobic colony counts obtained by agar contact plates
Fluorescent marker method
ATP bioluminescence assay system
5 high-touch surfaces were sampled in a convenience sample of 100 hospital rooms
Adjacent surfaces on 5 high-touch surfaces were sampled before and after terminal cleaning
Boyce JM et al. ICHE 2011;32:1187

22. Assessing Terminal Cleaning Practices Using 3 Methods
Main outcome measures expressed as percent of surfaces sampled after cleaning with:
Aerobic colony count < 2.5 cfu/cm2
Most or all of fluorescent marker removed
ATP reading of < 250 Relative Light Units

23. Proportion of 500 High-Touch Surfaces Classified as Having Been Cleaned by Fluorescent Marker, or as “Clean” by ACC or ATP Criteria After Terminal Cleaning
P <
P = 0.65

24. Proportion of 382 High-Touch Surfaces Classified as Having Been Cleaned by Fluorescent Marker, or Clean by ATP After Terminal Cleaning
P <
Rooms Classified as Clean BEFORE
terminal cleaning by ATP were excluded

25. 382 High-Touch Surfaces Classified as Not Clean Before Terminal Cleaning, Results for Fluorescent Marker and ATP
(53.6%) (34.7%)
(6.7%)
N = N = N = 90
Boyce JM et al. ICHE 2011;32:1187

26. Cleaning by housekeepers, using Quat disinfectant
Re-Evaluating Cutoffs for Defining Cleanliness, ATP Bioluminescence and Aerobic Colony Counts
Cleaning by housekeepers, using Quat disinfectant
Note: Each graph represents 1000 data points
Boyce JM et al. APIC Annual meeting, 2013, Poster 1705

27. Re-Evaluating Cutoffs for Defining Cleanliness, ATP Bioluminescence and Aerobic Colony Counts
Cleaning by infection preventionist, using peroxide-based disinfectant
Note: Each graph includes 720 data points (data are for after cleaning only)

28. ATP Bioluminescence for Evaluating Disinfection of C
ATP Bioluminescence for Evaluating Disinfection of C. difficile Isolation Rooms
140 high-touch sites in 50 rooms were cultured for C. difficile and sampled using an ATP assay after terminal or daily cleaning using bleach-based disinfectant
Surfaces with ATP < 250 RLU were considered to be clean
3% of 71 sites with ATP readings of < 250 RLU had positive culture
19% of 69 sites with ATP readings > 250 RLU had positive culture
Measuring ATP on surfaces could be a useful & rapid method to assess cleaning of C. difficile rooms
Deshpande A et al. Infect Control Hosp Epidemiol 2013;34:865

29. Comparison of Visual Inspection, Fluorescent Marker, Aerobic Colony Counts and ATP Bioluminescence
250 environmental surfaces in 50 rooms were sampled after terminal cleaning using three monitoring methods
Aerobic colony counts [ACC] (before & after cleaning)
Fluorescent markers (checked for complete removal after cleaning)
ATP bioluminescence assay system (before & after cleaning)
Results:
93% of surfaces had no visible contamination after cleaning
76% were considered clean by ATP method after cleaning
87% were considered clean by ACC after cleaning
Sensitivity, specificity and NPV of methods, compared to ACC
Fluorescent marker: sensitivity = 75%, specificity = 40%, NPV = 28%
ATP: sensitivity = 76%, specificity = 35%, NPV = 26%
Conclusion: Fluorescent marker and ATP are better than visual assessment. Both may be useful for monitoring cleaning
Luick L et al. AJIC 2013;41:751

30. Caveats on Using ATP Bioluminescence to Monitor Environmental Cleaning
No standard, evidence-based criteria for defining surfaces as clean by ATP bioluminescence is currently available
Cut-offs used to classify surfaces as clean by ATP assays depends on the brand of assay used
Some systems classify surfaces with < 250 RLU as clean
Other systems classify surfaces with < 100 RLU as clean
Sensitivity and specificity of different luminometers and assay systems differ
Consider manufacturer’s recommendations for cut-off
Further research is needed to refine criteria for cleanliness, both by ATP assays and by aerobic colony counts
Mulvey D et al. J Hosp Infect 2011;77:25
Aiken ZA et al. Infect Control Hosp Epidemiol 2011;32:507
Shama G et al. Int J Hyg Environmental Health 2013;216:115

31. Advantages and Disadvantages of Methods for
Monitoring Cleaning and Disinfection Practices
Housekeepers may “game” system
Havill NL Am J Infect Control 2013;41:S26

32. Sequential Interventions and Use of Two Monitoring Methods Improved Disinfection of C. difficile Isolation Rooms
21-month prospective intervention trial was conducted to evaluate methods for disinfection of C. difficile isolation rooms
Phase 1) Fluorescent markers + education and feedback to housekeepers
Phase 2) Addition of automated UV light units for adjunctive disinfection
Phase 3) Use of dedicated daily disinfection team, and requiring rooms to be “cleared” by housekeeper supervisor or infection preventionist using
visual assessment and
ATP bioluminescence assay of 3 sites in each room
Surfaces were cultured for presence of C. difficile
Results: Percent of rooms with positive C.difficile cultures:
Baseline: 67%
Phase 1: 57%
Phase 2: 35%
Phase 3: 7%
Sitzlar B et al. Infect Control Hosp Epidemiol 2013;34:459

33. Sequential Interventions and Use of Two Monitoring Methods to Improve Disinfection of C. difficile Isolation Rooms
Sitzlar B et al. Infect Control Hosp Epidemiol 2013;34:459

34. Conclusions
Contaminated environmental surfaces can contribute to transmission of healthcare-associated pathogens
Monitoring cleaning and disinfection of environmental surfaces is recommended in national guidelines
Visual inspection correlates poorly with objective methods
Fluorescent marker methods and ATP bioluminescence are being used increasingly to monitoring cleaning
Each method has advantages and limitations
Can be used in combination
Aerobic colony counts are more expensive and require more time, but provide unique information
Have been used during outbreaks and for research purposes

36. Coating Surfaces with Antimicrobial Metals
Coating medical equipment with metals which have antimicrobial activity is a new strategy for reducing environmental contamination
Examples include:
Copper alloys (studied most extensively)
Silver or nano-silver particles + titanium dioxide
Zinc
Dancer SJ Eur J Clin Microbiol Infect Dis 2011;30:1473
Weber DJ et al. ICHE 2012;33:10

37. Copper Alloys as Antimicrobial Surfaces
Environmental surfaces or medical equipment coated with copper alloys have been shown to
Have sustained antimicrobial activity
Reduce levels of bacterial contamination of surfaces in clinical settings when compared with usual equipment
Effective against a variety of pathogens
Less effective against MRSA and C. difficile
Noyce JO et al. J Hosp Infect 2006;63:289
Wheeldon et al. J Antimicrob Chemother 2008;62:522
Casey AL et al. J Hosp Infect 2010;74:72
Grass G et al. Appl Environ Microbiol 2011;77:1541
Karpanen TJ et al. ICHE 2012;33:3

38. Antimicrobial (Self-Disinfecting) Surfaces Are Promising, But Require Further Study
Many of the proposed products yielded only modest killing of pathogens
Not proven to be effective against some important pathogens (e.g. C. difficile)
Cost of installing metal-coated equipment and of products applied to usual equipment not clear
Durability of antimicrobial activity of such products has not been established
No data on impact of such strategies on HAIs
Weber DJ et al. ICHE 2012;33:10

39. Applying of Compounds with Long-Term Antimicrobial Activity to Surfaces
Silver iodide-based compound
Triclosan
Quaternary ammonium salt-based surfactant
Organosilane compounds
Quaternary ammonium + silicone-based compound
Effective in a few trials, but not in another
Light-activated antimicrobial coatings
Toluidine blue O + rose Bengal
Weber DJ et al. ICHE 2012;33:10
Havill NL & Boyce JM (unpublished)