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
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
Role of Environment in Transmission
of Healthcare-Associated Pathogens
•
Numerous investigators have provided evidence
that contaminated environmental surfaces can
contribute to transmission of healthcareassociated 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
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
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
Check lists to Improve Cleaning Practices
http://www.cdc.gov/hai/toolkits/evaluating-environmental-cleaning.html
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
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. 2010 Decennial conference, Abstr 60
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
Guerrero DM et al. ICHE 2013;34:524
Percent of inoculated surfaces positive
for C. difficile after cleaning, with
different interventions
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
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
VRE on Bedside Rail
• Useful for sampling irregularly shaped objects,
medical equipment, hard to reach areas, HCP hands
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
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
RODAC Plates
Cultures of Overbed Table
Before Cleaning
Boyce JM et al. SHEA 2011, Abstr 4711
After Cleaning
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
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: 76 - 92%
•
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
Improving Cleaning Practices
by Using Fluorescent Marker System
•
Prospective study in 36 acutecare 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
Percent of Objects
Cleaned
•
80
70
60
50
40
30
20
10
0
Baseline
•
Intervention included providing
housekeepers with
performance feedback
Carling PC et al. ICHE 2008;29:1035
Post-Intervention
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
6 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
Evaluating Cleaning Measures in an ICU
Using Fluorescent Marker System
Goodman ER et al. Infect Control Hosp Epidemiol 2008;29:593
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
ATP Bioluminescence Method
Step 1
Step 2
Use special swab
to sample surface
Place swab in
reaction tube
Step 3
Place tube in luminometer
Results: Relative Light Units
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
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
Percent
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
100
90
80
70
60
50
40
30
20
10
0
75.6
76.8
45
Fluorescent
Marker
ACC
P < 0.0001
P = 0.65
ATP
Proportion of 382 High-Touch Surfaces Classified as
Having Been Cleaned by Fluorescent Marker, or
Clean by ATP After Terminal Cleaning
100
74.8
Percent
80
60
38.9
40
20
0
Fluorescent Marker
P < 0.0001
Rooms Classified as Clean BEFORE
terminal cleaning by ATP were excluded
ATP
Percent
382 High-Touch Surfaces Classified as Not Clean
Before Terminal Cleaning,
Results for Fluorescent Marker and ATP
100
90
80
70
60
50
40
30
20
10
0
ATP > 250
ATP < 250
(53.6%)
(34.7%)
(6.7%)
Wiped Off
N = 168
Partially
Wiped
N = 124
Boyce JM et al. ICHE 2011;32:1187
Not Wiped
N = 90
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
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)
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
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
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
Advantages and Disadvantages of Methods for
Monitoring Cleaning and Disinfection Practices
Housekeepers may “game” system
Havill NL Am J Infect Control 2013;41:S26
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
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
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
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
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
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
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)