REVIEW Annals of Internal Medicine

Cleaning Hospital Room Surfaces to Prevent Health Care–

Associated Infections
A Technical Brief
Jennifer H. Han, MD, MSCE*; Nancy Sullivan, BA*; Brian F. Leas, MS, MA*; David A. Pegues, MD; Janice L. Kaczmarek, MS; and
Craig A. Umscheid, MD, MSCE

The cleaning of hard surfaces in hospital rooms is critical for re- most commonly assessed outcome. Comparative effectiveness
ducing health care–associated infections. This review describes studies of disinfecting methods and monitoring strategies were
the evidence examining current methods of cleaning, disinfect- uncommon. Future research should evaluate and compare
ing, and monitoring cleanliness of patient rooms, as well as con- newly emerging strategies, such as self-disinfecting coatings for
textual factors that may affect implementation and effectiveness. disinfecting and adenosine triphosphate and ultraviolet/fluores-
Key informants were interviewed, and a systematic search for cent surface markers for monitoring. Studies should also assess
publications since 1990 was done with the use of several biblio- patient-centered outcomes, such as infection, when possible.
graphic and gray literature resources. Studies examining surface Other challenges include identifying high-touch surfaces that
contamination, colonization, or infection with Clostridium diffi- confer the greatest risk for pathogen transmission; developing
cile, methicillin-resistant Staphylococcus aureus, or vancomycin- standard thresholds for defining cleanliness; and using methods
resistant enterococci were included. to adjust for confounders, such as hand hygiene, when examin-
Eighty studies were identified—76 primary studies and 4 sys- ing the effect of disinfecting methods.
tematic reviews. Forty-nine studies examined cleaning methods, Ann Intern Med. 2015;163:598-607. doi:10.7326/M15-1192 www.annals.org
14 evaluated monitoring strategies, and 17 addressed chal- For author affiliations, see end of text.
lenges or facilitators to implementation. Only 5 studies were ran- * Dr. Han, Ms. Sullivan, and Mr. Leas contributed equally to this work.
domized, controlled trials, and surface contamination was the This article was published online first at www.annals.org on 11 August 2015.

H ealth care–associated infections (HAIs) are a lead-

ing cause of illness and death in the United States
and worldwide. In 2011, an estimated 721 800 HAIs oc-
The goal of this review is to provide a systematic over-
view on environmental cleaning of hospital room sur-
faces to prevent HAIs. We focus on environmental
curred in the United States, leading to 75 000 deaths cleaning of the hard surfaces most frequently touched
(1). A multifaceted approach to preventing infection is by patients and health care workers, which are often
critical to reducing the risk for HAIs, including hand hy- called high-touch surfaces or objects. We also discuss
giene practices, antimicrobial stewardship, and envi- key health care–associated pathogens for which there
ronmental cleaning and disinfecting. is the most evidence for environmental transmission,
Several studies demonstrate that health care– specifically methicillin-resistant Staphylococcus aureus
associated pathogens frequently contaminate the pa- (MRSA), vancomycin-resistant enterococci (VRE), and
tient environment, including both porous surfaces Clostridium difficile (5– 8). Finally, we enumerate the ev-
(such as curtains) and hard, nonporous surfaces (such idence gaps in the literature and propose future re-
as bed rails and medical equipment) (2– 4). Contami- search directions.
nated surfaces are a reservoir for transmission of patho-
gens directly through patient contact with the environ-
ment or indirectly through contamination of health care
workers' hands and gloves. METHODS
Environmental cleaning is important for reducing This review is based on a protocol and technical
microbial contamination of surfaces and subsequent brief produced by the ECRI Institute–Penn Medicine
risk for HAIs. Environmental cleaning is a complex, mul- Evidence-based Practice Center for the Agency for
tifaceted process and involves the physical action of Healthcare Research and Quality (AHRQ) (9). The pro-
cleaning surfaces to remove organic and inorganic ma- tocol and final report are available at www.effective
terial, followed by application of a disinfectant, as well healthcare.ahrq.gov. Twelve key informants with
as monitoring strategies to ensure the appropriateness expertise in infectious diseases, infection control, envi-
of these practices. In addition, contextual factors, such ronmental disinfection, hospital epidemiology, micro-
as management tools and organizational structure, and biology, and management of environmental services
culture can affect the implementation and effectiveness staff in health care settings contributed to the protocol
of cleaning, disinfecting, and monitoring strategies. and report, including helping to refine the literature
search, review limitations in the current evidence, and
discuss potential directions for future research.

See also: Data Sources and Search Strategy

We searched several databases and gray literature
Editorial comment . . . . . . . . . . . . . . . . . . . . . . . . . 642
sources from 1 January 1990 through 4 February 2015.
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 Environmental Cleaning and HAIs REVIEW
The complete set of databases searched and the
Key Summary Points
search strategy is available in Appendix Tables 1 and 2
(available at www.annals.org). Environmental cleaning is an important component of a
multifaceted infection control strategy to prevent health
Study Selection
care–associated infections.
Titles, abstracts, and full-text articles were screened
in duplicate using the database Distiller SR (Evidence Emerging technologies have led to increased interest in
Partners). We included studies of any design that ad- evaluating environmental cleaning, disinfecting, and
dressed our clinical questions; examined any inpatient monitoring in the acute care hospital setting.
wards (such as medicine, surgery, and critical care); ad-
dressed high-touch surfaces; evaluated environmental A major limitation of the evidence base is the lack of
contamination, colonization, or infection with C. diffi- comparative studies addressing the relative effective-
cile, MRSA, or VRE or included several unspecified ness of various cleaning, disinfecting, and monitoring
pathogens that were likely to include those infections; strategies.
and were published in English. Studies were excluded
if they took place exclusively in pediatric, ambulatory, Few studies assess clinical, patient-centered outcomes,
operating room, or long-term care settings; addressed including patient colonization and health care–
only soft, porous surfaces (such as linens or curtains) or associated infection rates.
transmission routes not inherent to the environmental
reservoir (such as caregiver hands, stethoscopes, or in- Future studies are needed that directly compare newer
vasive medical devices); examined products or pro- disinfecting and monitoring methods, assess the effect
cesses not available in the United States or not cur- of contextual factors on implementation, and evaluate
rently being investigated; or were in vitro studies that patient-centered outcomes.
did not collect samples from actual patient rooms.
Data Extraction and Synthesis
A standardized data extraction form was used by 1
reviewer to collect information on patient populations;
pathogens; high-touch surfaces; type of cleaning, dis- Of the 80 clinical studies, 49 (61%) (2 systematic
infecting, monitoring, and implementation strategy; reviews) focused on cleaning or disinfecting, 14 (18%)
study design; and study outcomes. A random sample (2 systematic reviews) focused on monitoring, and 17
of 25% of abstracted data was verified by another re- (21%) focused on implementation of cleaning or moni-
viewer. Descriptions of cleaning/disinfecting and mon- toring strategies. No conference abstracts presented
itoring methods currently used in hospital settings are within the past 2 years were identified for inclusion. Ap-
shown in Appendix Tables 3 and 4 (available at www pendix Tables 5 and 6 (available at www.annals.org)
.annals.org), respectively. We developed an evidence describe identified clinical practice guidelines and clin-
map to synthesize information on the type and depth of ical trials (ClinicalTrials.gov), respectively.
research available on cleaning, disinfecting, and moni- The primary setting for most studies was the inten-
toring processes. We also highlighted important knowl- sive care unit. The most commonly examined high-
edge gaps in the evidence base. touch objects included bed rails, call buttons, light
switches, side or tray tables, and toilets, but the
Role of the Funding Source selection of high-touch objects across studies varied
This project was funded by AHRQ. A representative substantially.
from AHRQ served as a contracting officer's technical Outcomes reported in the 76 primary studies were
representative and provided technical assistance and broadly categorized as surface contamination (such as
feedback during the conduct of the evidence report. bacterial burden, number of surfaces cleaned, and pos-
AHRQ did not directly participate in the literature itive microbiological cultures), patient colonization
search; determination of study eligibility criteria; data (such as new VRE colonization), or infection rate (such
analysis or interpretation; or preparation, review, or ap- as incidence rate expressed per 1000 patient days).
proval of the manuscript for publication. This work was Among the primary studies reporting pathogens of in-
also supported in part by the National Institutes of terest, the most commonly reported pathogen was C.
Health, which had no role in the design and conduct of difficile (n = 40), followed by MRSA (n = 30) and VRE
the study; collection, management, analysis, or inter- (n = 30). Some studies evaluated several pathogens.
pretation of the data; or preparation, review, or ap-
proval of the manuscript. Evidence Map
Figure 1 shows the number and research designs
of published studies that address major categories of
RESULTS cleaning or disinfection strategies and monitoring
The literature searches yielded 80 clinical studies methods, respectively. Figure 2 depicts evidence gaps
for inclusion in the review, 76 of which were primary that suggest high-impact areas for future research, as
studies and 4 of which were systematic reviews. The recommended by our key informants or indicated by
Appendix Figure (available at www.annals.org) shows our analysis of the current evidence base. The interven-
the study selection process. tions are organized in a framework adapted from
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 REVIEW Environmental Cleaning and HAIs

Figure 1. Evidence map showing the number and study designs of published studies that address major categories of
cleaning and disinfection strategies and monitoring methods.

Cleaning and Disinfection Strategies*

Electrolyzed water Historical controls

Nonrandomized concurrent controls

Microfiber RCTs

Systematic reviews
Coatings

HPV

UV light

Sporicidal/HP wipes

Chlorine-based

Quaternary

0 2 4 6 8 10
Studies, n

Monitoring Methods†

Visual inspection

Descriptive
Aerobic colony counts

Historical controls

Nonrandomized concurrent controls

UV light Systematic reviews

ATP

0 1 2 3 4 5 6
Studies, n

ATP = adenosine triphosphate; HP = hydrogen peroxide; HPV = hydrogen peroxide vapor; RCT = randomized, controlled trial; UV = ultraviolet.
* 2 systematic reviews and 47 primary studies. Some studies evaluated >1 method.
† 2 systematic reviews and 12 primary studies. Some studies evaluated >1 method.

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 Environmental Cleaning and HAIs REVIEW

Figure 2. Evidence needs for future research in environmental cleaning.

Cleaning/Disinfection Monitoring Implementation

Evidence Hierarchy Study Design Interventions Interventions Interventions

Aerobic
colony counts
Reduced QAC Audit and feedback
infections RCTs Bleach Adenosine
triphosphate assays Education and
Nonrandomized HPV devices training
concurrent controls UV light–emitting devices UV light–
visible markers Outsourcing

Copper or silver coatings PCR-based assays

Light-activated
antimicrobial coatings
Reduced
colonization

Nonrandomized
concurrent controls Peracetic acid wipes
Historical controls HP wipes

In vivo
reduction of
surface Microfiber
contamination
(clinical studies)

Identifying
Electrolyzed water Defining
Laboratory high-risk
cleanliness
testing surfaces
In vitro
reduction of
surface
contamination
(laboratory studies)

Adapted from reference 10. HP = hydrogen peroxide; HPV = hydrogen peroxide vapor; PCR = polymerase chain reaction; QAC = quaternary
ammonium compound; RCT = randomized, controlled trial; UV = ultraviolet.

McDonald and Arduino's recently proposed “evidence months. Most studies (n = 31 [66%]) used a primary
hierarchy” for environmental infection control (10). This outcome of surface contamination. Only 16 studies
framework represents the progression of evidence for (34%) reported pathogen colonization or infection rate
the effectiveness of environmental interventions, from as a primary outcome, and C. difficile was mostly com-
laboratory studies that measure surface contamination; monly assessed.
to clinical studies that assess contamination in real- Cleaning and disinfecting methods were generally
world settings; to studies that address patient-centered categorized as surface cleaning or disinfecting, auto-
outcomes, such as pathogen colonization and mated processes, or effectiveness of enhanced coat-
infection. ings or surfaces for disinfecting. Studies examining
Strategies for Environmental Cleaning chemical disinfectants reported mixed findings, includ-
Forty-seven primary studies (11–57) and 2 system- ing reductions in VRE (51) and C. difficile rates (16, 20,
atic reviews (58, 59) focusing on cleaning and disinfect- 21, 54) with the use of bleach-based disinfectants; de-
ing were identified. Of the 47 primary studies, 27 (57%) creased C. difficile spore levels with the use of acceler-
were done in the United States and the remaining 19 ated hydrogen peroxide (48); and ineffectiveness of a
were done in the United Kingdom, Australia, Sweden, chlorine-based product in reducing C. difficile contam-
Canada, Norway, and Italy. Studies were published be- ination and infection rates (14). Six studies integrating
tween 1998 and September 2014; 28 (60%) were pub- various wipes (such as hydrogen peroxide) into preven-
lished since 2012, reflecting recently intensified interest tive strategies (15, 17, 25–28) reported positive out-
in this topic. comes, including sustained reductions in C. difficile in-
Only 5 primary studies (11%) were randomized, fection rates (15, 27). Seventeen studies implementing
controlled trials, and 1 (2%) was a randomized cross- no-touch methods (such as ultraviolet [UV] light and hy-
over study. Study durations ranged from 4 weeks to 43 drogen peroxide vapor) reported positive findings (11,
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 REVIEW Environmental Cleaning and HAIs

13, 19, 29 –31, 39, 40, 42, 44 – 46, 50, 52, 53, 56), and 3 to pathogen type, C. difficile and VRE were the primary
of these studies specifically found reduced infection focus of 3 (75, 80, 81) and 2 (85, 90) studies, respec-
rates (29 –31). Seven of 8 studies (88%) evaluating en- tively. The remaining studies focused on at least 2
hanced coatings, such as copper-coated surfaces, re- pathogens of interest.
ported positive findings (12, 32–37). Appendix Tables 7 Three studies (18%) (75, 76, 80) used multicompo-
and 8 (available at www.annals.org) describe the char- nent strategies to prevent C. difficile infections and re-
acteristics of cleaning and disinfecting studies. ported positive findings. Five studies (64, 76, 81, 84,
87) reporting on sustainability of preventive strategies
Strategies for Monitoring Cleanliness
described ongoing education, direct feedback, and
Two systematic reviews (60, 61) and 12 primary
commitment and flexibility of administrative leaders as
studies (62–73) evaluated strategies for monitoring en-
key components to successful implementation.
vironmental cleaning and disinfecting. The locations for
Appendix Table 10 (available at www.annals.org)
11 of the 12 primary studies were reported and in-
describes the characteristics of the implementation
cluded the United States (n = 7 [64%]), United Kingdom
studies.
(n = 3 [27%]), and Canada (n = 1 [9%]). Studies were
published from 2003 to 2013; 3 (25%) were published
since 2012.
The most common study design was nonrandom- Contextual Factors
ized using concurrent control groups (n = 5 [42%]). Contextual factors for implementation strategies
Study durations ranged from 4 weeks to 8 months; 4 examined in the 76 primary studies and identified by
studies did not report duration. Eight studies (67%) as- key informants included structural organizational char-
sessed percentage of targets cleaned (62, 65– 67) or acteristics, such as outsourcing of environmental ser-
cleaning rate (63, 64, 68, 69) as the primary outcome. vices (80, 91) and organization of environmental ser-
Less commonly reported outcomes included microbial vices within the administrative hierarchy of a hospital.
burden counts (71, 73), sensitivity to detect pathogens External factors that affect environmental cleaning ef-
(70), and number of positive cultures (72). Four studies forts included adherence to “evidence-based policies
focused on a single pathogen (63, 66, 68, 72). and procedures” from various organizations (such as
Fluorescent/UV surface markers and adenosine the Centers for Medicare & Medicaid Services and The
triphosphate bioluminescence were the most com- Joint Commission). A positive patient safety culture that
monly evaluated monitoring methods. Six of the 8 stud- fosters collaboration and respect among clinical and
ies (75%) mainly focusing on fluorescent/UV surface support services staff, as well as between supervisors
markers (64 – 69) concluded that these monitoring and front-line personnel, were examined in 5 studies
methods were useful and highly objective and helped (77, 80, 84, 87, 92). Implementation and management
achieve substantial improvements in cleaning and dis- tools were identified as key contextual factors and in-
infecting practices. Visual observation was found to be clude staff education and training, dedicated training
inferior to various other monitoring methods in 4 of 5 time, use of internal audit and feedback, and presence
primary studies (80%) (62, 63, 70 –73) and 1 review of internal or external persons responsible for imple-
(100%) (61). Appendix Tables 7 and 9 (available at mentation. Of the 24 studies (32%) that integrated im-
www.annals.org) describe the characteristics of moni- plementation tools, education was reported as a key
toring studies. component in most (n = 23 [96%]); 5 studies (21%) spe-
cifically reported on training staff (13–15, 77, 84) and 5
Implementing Cleaning and Monitoring
additional studies (21%), all published since 2012, de-
Strategies scribed use of audits (14, 17, 81, 82, 84).
Implementation Strategies
Seventeen primary studies focused specifically on
implementing infection control interventions and con-
textual factors (74 –90). These studies were published DISCUSSION
between 2006 and September 2014; 9 (53%) were Contamination of high-touch environmental sur-
published since 2012. Most studies (n = 14 [82%]) were faces plays an important role in transmission of patho-
done in the United States, with remaining studies done gens in the acute care hospital setting. Increasing at-
in Australia and Canada. tention has been directed toward the importance of
Thirteen studies (76%) used historical controls, in- environmental cleaning and disinfecting in the preven-
cluding before-and-after study designs (n = 9), and in- tion of HAIs. We reviewed 4 systematic reviews and 76
terrupted time series (n = 4). Three studies (18%) were primary studies of environmental cleaning. We found
nonrandomized using concurrent control groups, and 1 considerable diversity with regard to both study design
(6%) was an uncontrolled, descriptive study. Study and cleaning/disinfecting and monitoring methods ex-
length ranged from 8 weeks to 4 years. Most studies amined across studies, as well as many limitations in the
reported a primary outcome of surface contamination. evidence base. There was a lack of direct, rigorous
Only 2 studies (12%) reported pathogen acquisition as comparative studies of various methods, with only 5
a primary outcome (83, 90). Clinical infection was re- studies designed as randomized, controlled trials. Our
ported as a primary and secondary outcome in 3 (80, review of the literature also highlighted a limited focus
83, 90) and 2 (75, 76) studies, respectively. With regard on patient-centered outcomes, such as patient coloni-
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 Environmental Cleaning and HAIs REVIEW
zation or infection. Instead, surface contamination was studies on monitoring methods demonstrated consid-
the most commonly reported outcome. erable variation in high-touch objects selected for eval-
The results of these studies, as well as synthesis of uation, making it challenging to determine which sur-
key informant input, suggest that evaluating the clinical faces are at greatest risk for microbial contamination
effectiveness of cleaning and disinfecting methods is and pathogen transmission.
challenging. A major limitation is the gap between op- Our review has important limitations. First, it pro-
timized use of surface cleaning or disinfecting agents in vides only an inventory of available evidence and does
studies and practical implementation in real-world set- not appraise the risk of bias of individual studies or
tings (such as appropriate dwell time and type of sur- provide overall ratings of the strength of evidence for
face targeted). Manufacturers provide recommenda- each intervention and outcome examined. Second, the
tions for proper use of their products, but most studies review was restricted to studies of C. difficile, MRSA,
do not report thoroughness of cleaning or adherence and VRE; thus, our findings may not be fully generaliz-
to disinfectant dwell time; this information also remains able to interventions aimed at reducing infections due
largely unknown in daily practice. An important related to other organisms (such as gram-negative pathogens).
concern is uncertainty by end users about the applica- Future research should seek to review the evidence
bility of some manufacturer recommendations. Guid- base for other pathogens. Further, many of the studies
ance that accompanies products may be based on lab- included in this review were undertaken during out-
oratory testing under ideal conditions rather than breaks and may not be representative of the effect of
clinical settings. Recommendations may also be devel- cleaning/disinfecting and monitoring in nonoutbreak
oped based on certain types of pathogens, but users settings.
may choose to implement a product or technology for Future research on environmental cleaning and
broader effects. Few studies directly compared the ef- disinfecting to reduce HAIs should address the follow-
fectiveness of different methods; instead, many used ing key questions: What surfaces, including high-touch
before-and-after study designs to assess the effect of a objects, should be cleaned and disinfected? How
single disinfecting method. should surfaces be cleaned and disinfected, and what
Another challenge to interpreting the results of the is the comparative effectiveness of different methods?
current evidence base is determining the specific effect How should cleaning and disinfecting be monitored
of environmental cleaning and disinfecting interven- and measured, and what would be appropriate bench-
tions in the context of multicomponent infection pre- marks for cleanliness and reduced risk for pathogen
vention strategies (93). Infection prevention comprises transmission? How should interventions be imple-
many critical components in addition to hard surface mented, including in-depth study of facilitators and
cleaning, including sterilization of instruments, imple- barriers to real-world implementation?
mentation of appropriate isolation precautions, and In summary, our review of the literature indicates
proper hand hygiene. These and other elements may an increased interest in environmental cleaning and
sometimes be included as interventions within a larger disinfecting for the prevention of HAIs. However, there
infection prevention strategy, limiting the ability to dis- are many limitations in the current evidence base. Fu-
cern the specific effect of any single approach. These ture research on environmental cleaning that addresses
factors also have the potential to modify the effective- these limitations and evidence gaps will be critical for
ness of environmental cleaning interventions. Consid- informing real-world interventions for reducing the risk
erable uncertainty also remains about which surfaces, for HAIs in the hospital setting.
including high-touch objects, should be targeted for
cleaning and disinfecting. From Perelman School of Medicine, University of Pennsylva-
Limitations in the evidence base for monitoring nia, and Center for Evidence-based Practice, University of
methods were also identified, including the lack of di- Pennsylvania Health System, Philadelphia, and ECRI Institute–
rect, rigorous comparative studies of various technolo- Penn Medicine Evidence-based Practice Center, Plymouth
gies. Key informants noted that hospitals may be reluc- Meeting, Pennsylvania.
tant to adopt such methods as adenosine triphosphate
and UV/fluorescent surface markers given the relative Disclaimer: This article is based on research conducted by the
absence of data. Another important limitation in the lit- ECRI Institute–Penn Medicine Evidence-based Practice Center
erature is the lack of consensus for thresholds of clean- under contract to AHRQ, U.S. Department of Health and Hu-
liness. Specifically, although various cleanliness thresh- man Services. The findings and conclusions in this document
olds with the use of adenosine triphosphate and certain are those of the authors, who are responsible for its contents
microbiological methods were described across stud- and should not be construed as endorsement by AHRQ or the
ies, there is no established benchmark for defining a U.S. Department of Health and Human Services.
surface as “clean.” The real-world goal of environmen-
tal cleaning and disinfecting should be to reduce risk Acknowledgment: The authors thank the following persons at
for pathogen transmission rather than establishing a the ECRI Institute for their assistance with the preparation of
continuously sterile surface. Benchmarks for surface the technical brief: Michele Datko, MS; James Davis, MSN,
cleanliness that correlate with decreases in pathogen RN; David Snyder, PhD; Gina Giradi, MS; Luke A. Petosa, MSc;
acquisition should therefore be determined. As with Joann Fontanarosa, PhD; Michael Phillips; Jennifer Dell’Aquila
studies evaluating cleaning and disinfecting methods, Maslin; Helen Dunn; Lydia Dharia; and Evidence-based Prac-
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 REVIEW Environmental Cleaning and HAIs

tice Center Director, Karen Schoelles, MD, SM. They also 7. Drees M, Snydman DR, Schmid CH, Barefoot L, Hansjosten K, Vue
thank the following persons, who served as key informants on PM, et al. Prior environmental contamination increases the risk of
the associated technical brief: Michelle Alfa, PhD; Philip acquisition of vancomycin-resistant enterococci. Clin Infect Dis.
Carling, MD; Patti Costello; Mia Gonzales Dean, MBA, MS; 2008;46:678-85. [PMID: 18230044] doi:10.1086/527394
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Curtis Donskey, MD; Rich Feczko; Elaine Larson, PhD, RN; Luis
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Ostrosky-Zeichner, MD; William A. Rutala, PhD, MS, MPH;
2013;26:338-44. [PMID: 23743816] doi:10.1097/QCO.0b013
Daniel Schwartz, MD, MBA; and James P. Steinberg, MD. The e3283630f04
authors also thank the following persons, who served as peer 9. Leas BF, Sullivan N, Han JH, Pegues DA, Kaczmarek J, Umscheid
reviewers on the associated technical brief: Dottie Borton, RN, CA. Environmental Cleaning for the Prevention of Healthcare-
BSN, CIC; Mary K. Hayden, MD; L. Clifford McDonald, MD; Associated Infections (HAI). (Prepared by the ECRI Institute–Penn
Gina Pugliese, RN, MS; Gary A. Roselle, MD; and Robert A. Medicine Evidence-based Practice Center under contract HHSA290-
Weinstein, MD. They also acknowledge Kim Marie Witten- 2012-00011-I). Rockville, MD: Agency for Healthcare Research and
berg, MA, who served as the AHRQ Task Order Officer, and Quality; 2015.
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HHSA 290-2012-00011-I). This topic was nominated by a
Staphylococcus aureus. BMC Infect Dis. 2014;14:187. [PMID:
member of the 3M Hospital Hygiene Global Advisory Board 24708734] doi:10.1186/1471-2334-14-187
on behalf of the Board. This work was also supported in part 12. Schmidt MG, Attaway HH, Sharpe PA, John J Jr, Sepkowitz KA,
by the National Institutes of Health (K01-AI103028; Dr. Han). Morgan A, et al. Sustained reduction of microbial burden on com-
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Disclosures: Dr. Han, Ms. Sullivan, Mr. Leas, Dr. Pegues, Ms. .01032-12
Kaczmarek, and Dr. Umscheid report grants from AHRQ dur- 13. Mitchell BG, Digney W, Locket P, Dancer SJ. Controlling
ing the conduct of the study. Forms can be viewed at www methicillin-resistant Staphylococcus aureus (MRSA) in a hospital and
.acponline.org/authors/icmje/ConflictOfInterestForms.do?ms the role of hydrogen peroxide decontamination: an interrupted time
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Crothall Healthcare's Strategic Initiatives for Reducing Healthcare- .06.010

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 Annals of Internal Medicine
Current Author Addresses: Dr. Han: Division of Infectious Dis- Author Contributions: Conception and design: J.H. Han, B.F.
eases, Department of Medicine, Hospital of the University of Leas, D.A. Pegues, C.A. Umscheid.
Pennsylvania, 811 Blockley Hall, 423 Guardian Drive, Philadel- Analysis and interpretation of the data: J.H. Han, N. Sullivan,
phia, PA 19104. B.F. Leas, D.A. Pegues, C.A. Umscheid.
Ms. Sullivan and Ms. Kaczmarek: ECRI Institute Evidence- Drafting of the article: J.H. Han, N. Sullivan, D.A. Pegues.
based Practice Center and Health Technology Assessment Critical revision of the article for important intellectual con-
Group, ECRI Institute Headquarters, 5200 Butler Pike, Plym- tent: J.H. Han, B.F. Leas, D.A. Pegues, C.A. Umscheid.
outh Meeting, PA 19462-1298. Final approval of the article: J.H. Han, N. Sullivan, B.F. Leas,
Mr. Leas and Dr. Umscheid: Center for Evidence-based Prac- D.A. Pegues, J.L. Kaczmarek, C.A. Umscheid.
Provision of study materials or patients: B.F. Leas, C.A.
tice, University of Pennsylvania Health System, 3535 Market
Umscheid.
Street, Suite 50, Philadelphia, PA 19104.
Obtaining of funding: B.F. Leas, C.A. Umscheid.
Dr. Pegues: Department of Healthcare Epidemiology, Infec-
Administrative, technical, or logistic support: N. Sullivan, B.F.
tion Prevention, and Control, Hospital of the University of
Leas, J.L. Kaczmarek, C.A. Umscheid.
Pennsylvania, 3400 Spruce Street, Ground Founders, Philadel- Collection and assembly of data: J.H. Han, N. Sullivan, B.F.
phia, PA 19104. Leas, D.A. Pegues.

Appendix Table 1. Electronic Database Searches

Database Date Limits Platform or Provider
ClinicalTrials.gov Through February 3, 2015 U.S. National Institutes of Health
CENTRAL 1990 through 2015, Issue 2 Wiley
The Cochrane Database of Methodology Reviews (Methodology Reviews) 1990 through 2015, Issue 2 Wiley
The Cochrane Database of Systematic Reviews (Cochrane Reviews) 1990 through 2015, Issue 2 Wiley
CINAHL 1990 through 2015, Issue 2 EBSCOhost
DARE 1990 through 2015, Issue 2 Wiley
EMBASE 1990 through February 2, 2015 Elsevier
HTA Database 1990 through 2015, Issue 2 Wiley
Healthcare Standards Directory (ECRI Institute) Through February 3, 2015 ECRI Institute
MEDLINE (via EMBASE) 1990 through February 2, 2015 Elsevier
PubMed (In-process, Publisher, and PubMedNotMedline records) 1990 through February 2, 2015 U.S. National Library of Medicine
Scopus* Through February 4, 2015 Elsevier
U.K. NHS EED 1990 through 2015, Issue 2 Wiley
U.S. NGC Through February 3, 2015 AHRQ
AHRQ = Agency for Healthcare Research and Quality; CENTRAL = Cochrane Central Register of Controlled Trials; DARE = Database of Abstracts
of Reviews of Effects; EED = Economic Evaluation Database; HTA = Health Technology Assessment; NGC = National Guideline Clearinghouse;
NHS = National Health Service.
* Used for citation tracking and searching trade publications.

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 Appendix Table 2. Search Strategies*

Concept Set Search Statement

Number
Infections (broad terms, health 1 (“healthcare associated infection” OR “hospital infection”)/de
care–associated) 2 ((“health care acquired” next/1 (infection* OR pathogen*)) OR (“healthcare acquired” next/1 (infection*
OR pathogen*)) OR (“hospital acquired” next/1 (infection* OR pathogen*)) OR (“health care
associated” next/1 (infection* OR pathogen*)) OR (“healthcare associated” next/1 (infection* OR
pathogen*)) OR (“hospital associated” next/1 (infection* OR pathogen*))):ti,ab
3 (HAI OR HAIs):ti
Infections (specific 4 (“clostridium difficile” OR “clostridium difficile infection” OR “methicillin resistant staphylococcus aureus”
terms—bacterial) OR “methicillin resistant staphylococcus aureus infection” OR enterococcus OR “vancomycin resistant
enterococcus” OR “enterococcal infection”)/de
5 ((antibiotic OR “multi-drug” OR multidrug OR methicillin OR vancomycin) next/1 resistan*):ti,ab OR
difficile:ti,ab OR (“methicillin resistant” next/2 aureus):ti,ab OR (“vancomycin resistant” next/1
enterococc*):ti,ab
6 (CDI OR MRSA OR VRE):ti
Limit to patients 7 (#4 OR #5 OR #6) AND (patient/exp OR (inpatient* OR patient*):ti,ab)
Combine infection sets 8 #1 OR #2 OR #3 OR #7
Setting (hospitals, inpatient 9 (“health care facility” OR “hospital discharge”)/de OR hospital/exp
facilities, patient rooms) 10 (“acute care” OR “burn unit” OR “burn units” OR “common area” OR “common areas” OR “critical care”
OR “healthcare facility” OR “healthcare facilities” OR “health care facility” OR “health care facilities” OR
“healthcare setting” OR “healthcare settings” OR “health care setting” OR “health care settings” OR
hospital OR hospitalis* OR hospitaliz* OR ICU OR institution OR institutions OR “intensive care” OR
“patient care area” OR “medical facility” OR “medical facilities” OR “patient care areas” OR “patient
room” OR “patient rooms” OR “patients rooms” OR ward OR wards):ti,ab
Setting (high-touch surfaces) 11 (fomite OR “hospital bed” OR “hospital equipment”)/de
12 (fomes OR fomite* OR “environmental reservoir” OR “environmental reservoirs” OR “surface
contamination” OR “surface microbes”):ti,ab
13 (bathroom* OR “bed rail” OR “bed rails” OR bedrail* OR cart OR carts OR chair OR chairs OR “clinical
surfaces” OR commode* OR “environmental surfaces” OR “high contact” OR “high-touch” OR “hospital
bed” OR “hospital beds” OR “hospital surfaces” OR “mobile equipment” OR “portable medical
equipment” OR railing OR railings OR toilet* OR “shared medical equipment” OR wheelchair*):ti,ab
Combine setting sets 14 #9 OR #10 OR #11 OR #12 OR #13
Combine sets (any infection or 15 #8 OR #14
setting)
General cleaning 16 (cleaning OR disinfection OR “environmental sanitation”)/de OR “infection control”/mj
17 (“cleaning method” OR “cleaning methods” OR “cleaning practice” OR “cleaning practices” OR “cleaning
protocol” OR “cleaning protocols” OR “cleaning regimen” OR “cleaning regimens” OR “cleaning
routines” OR “cleaning technique” OR “cleaning techniques” OR “discharge cleaning” OR “discharge
room cleaning” OR “enhanced cleaning” OR “environmental cleaning” OR “environmental
decontamination” OR “environmental disinfection” OR “environmental sanitation” OR “hospital
cleaning” OR “pre cleaning” OR precleaning OR “room cleaning” OR “room decontamination” OR
“routine cleaning” OR “surface cleaning” OR “surface disinfection” OR “surface decontamination” OR
“terminal cleaning” OR “terminal disinfection” OR “terminal room”):ti,ab
18 (cleaning OR decontamination OR disinfect* OR “infection control”):ti
Disinfectants 19 “disinfectant agent”/exp OR (“bleaching agent” OR “quaternary ammonium derivative”/de)
20 (biocidal OR biocide* OR “chemical agent” OR “chemical agents” OR “chemical disinfection” OR
“cleaning agent” OR “cleaning agents” OR disinfectant* OR “disinfecting agent” OR “disinfecting
agents” OR “disinfection agent” OR “disinfection agents” OR germicidal OR germicide* OR sporicidal
OR sporicide*):ti,ab
21 (“accelerated hydrogen peroxide” OR aldehyde* OR alcohol OR alcohols OR bleach OR bleaching OR
“benzalkonium chloride” OR “calcium hypochlorite” OR “chlorhexidine digluconate” OR
glutaraldehyde OR “guanidine hydrochloride” OR hypochlorite* OR “ortho-phthalaldehyde” OR
orthophthalaldehyde OR “peracetic acid” OR phenolic* OR phenol OR phenols OR “quaternary
ammonium” OR QACs OR “sodium dichloroisocyanurate” OR “sodium hypochlorite” OR vinegar):ti,ab
Limit to disinfectant studies to 22 (#19 OR #20 OR #21) AND (clean* OR decontaminat* OR disinfect* OR housekeep*):ti,ab
cleaning
Automated devices 23 (“disinfection system” OR “ultraviolet irradiation” OR “ultraviolet radiation”)/de OR (“hydrogen peroxide”
AND (vapor OR “water vapor”))/de
24 (automated next/2 (cleaning OR device* OR decontamination OR disinfection)):ti,ab OR ((“no touch” OR
“non touch”) next/1 disinfect*):ti,ab OR (“room sterilisation” OR “room sterilization” OR “self
disinfecting”):ti,ab
25 ((405nm OR “405 nm” OR “pulsed ultrasound” OR “pulsed xenon” OR ((ultraviolet OR UV) next/1
(disinfection OR light OR irradiation OR radiation))):ti,ab) AND (clean* OR decontaminat* OR disinfect*
OR room OR rooms):ti,ab
26 “superoxidised water”:ti,ab OR “superoxidized water”:ti,ab OR ((“hydrogen peroxide” OR H2O2) AND
(aerosol* OR fogging OR mist OR steam OR system OR systems OR vapor* OR vapour*)):ti,ab
Enhanced coatings and surfaces 27 (copper AND “material coating”)/de
28 “self disinfecting”:ti,ab OR ((antimicrobial OR copper OR silver) NEAR/2 (coated OR coating* OR
impregnated OR surface*)):ti,ab
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 Appendix Table 2—Continued

Concept Set Search Statement

Number
Cleaning personnel and training 29 (“hospital service” OR housekeeping OR “staff training”)/de
30 (“cleaning personnel” OR “cleaning service” OR “cleaning services” OR “cleaning staff” OR “cleaning
workers” OR “environmental services” OR “environmental technician” OR “environmental technicians”
OR housekeeper* OR housekeeping OR “service worker” OR “service workers”):ti,ab
Measuring and monitoring 31 (“adenosine triphosphate” AND bioluminescence)/de OR (“hospital hygiene”)/de
cleanliness 32 (((“adenosine triphosphate” OR ATP) next/1 bioluminescen*) OR cleanliness OR “fluorescent marker” OR
“fluorescent markers” OR “glo germ” OR glogerm OR “hospital hygiene” OR “surface hygiene”):ti,ab
Combine sets (any cleaning 33 #16 OR #17 OR #18 OR #22 OR #23 OR #24 OR #25 OR #26 OR #27 OR #28 OR #29 OR #30 OR #31 OR
concept) #32
Combine sets (any infection or 34 #15 AND #33
setting and any cleaning
concept)
Limit to English-language 35 #34 AND [english]/lim
publications
Remove undesired publication 36 #35 NOT (‘conference paper’/exp OR (‘case report’ OR book OR erratum OR letter OR note OR ‘short
types survey’)/de OR (book OR conference OR erratum OR letter OR note OR ‘short survey’):it OR (book OR
‘conference proceeding’):pt)
Limit to publications with abstracts 37 #36 AND [abstracts]/lim
Remove animal and in vitro 38 #37 NOT ([animal cell]/lim OR [animal experiment]/lim OR [animal model]/lim OR [animal tissue]/lim OR
studies “in vitro study”/de)
Remove pediatric studies 39 #38 NOT (adolescen* OR babies OR child* OR fetal OR infant OR infants OR neonat* OR newborn* OR
NICU OR paediatric* OR pediatric* OR school OR schools OR teen* OR youth*):ti
Remove undesired geographic 40 #39 NOT (africa/exp OR asia/exp OR mexico/de OR “oceanic regions”/exp OR “south and central
locations america”/exp)
Limit by publication date 41 #40 AND [1990-2015]/py
Limit to meta-analyses and 42 #41 AND (“meta analysis”/de OR “systematic review”/de OR (“evidence base” OR “evidence based” OR
systematic reviews published “meta analysis” OR methodologic* OR pooled OR “quantitative analysis” OR “quantitative review” OR
“research synthesis” OR search* OR “systematic review”):ti,ab)
Limit to clinical studies 43 #41 AND ((“comparative study” OR “controlled study” OR “experimental study” OR “field study” OR “in
vivo study” OR methodology OR model OR “observational study” OR “pilot study” OR “prevention
study” OR “quasi experimental study” OR “trend study” OR “validation study”)/exp OR (analysis OR
“case control” OR clinical OR cohort OR comparison OR “matched controls” OR random* OR study OR
trial):ti,ab OR article/de OR article:it OR “article in press”:it OR “priority journal”/de)
Limit to narrative reviews 44 #41 AND (review/de OR review:it OR (overview OR review):ti) AND [2009-2015]/py
published from 2009 onward
Limit to clinical practice guidelines 45 #41 AND (practice guideline/exp OR (“best practice” OR “best practices” OR consensus OR guidance OR
guideline* OR recommendation* OR standard* OR statement):ti)
Combine sets 46 #42 OR #43 OR #44 OR #45
* Strategy in EMBASE syntax; the search was simultaneously done across EMBASE and MEDLINE. A similar strategy was used to search the
databases comprising CINAHL, the Cochrane Library, and PubMed.

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 Appendix Table 3. Cleaning and Disinfecting Methods Used in Acute Care Settings

Product Description Application and Considerations for Use

Chemical disinfectants or touch modalities
Quaternary ammonium compounds: Frequently used for routine cleaning and disinfection of Application
noncritical environmental surfaces (e.g., floors, bed rails, tray tables). They are bactericidal, virucidal Spray; moistened paper towel, textile, or
against enveloped viruses, and fungicidal but not sporicidal and generally not mycobactericidal or microfiber cloth; premoistened wipe; paper
virucidal against nonenveloped viruses. High water hardness and materials such as cotton towels can towel or cloth soaked in disinfectant-filled
diminish microbicidal activity (94–96). Case reports of occupational asthma have been documented bucket
due to use of benzalkonium chloride (97, 98). Considerations for use
Hypochlorites: Most commonly used of the chlorine disinfectants, often for disinfecting bathroom Microorganisms being targeted
and food preparation surfaces and blood spills. They are bactericidal, fungicidal, virucidal, Type of surface
mycobactericidal, and sporicidal and are generally included in recommendations for disinfecting Characteristics of a specific disinfectant
surfaces or objects contaminated with hepatitis viruses, HIV, and Clostridium difficile. They may (e.g., compatibility on various surfaces)
cause skin and eye irritation, as well as oropharyngeal, esophageal, and gastric burns (99–101). They Cost
are also corrosive to metals in high concentrations (>500 ppm) and can discolor fabrics. Given that Ease of use
their activity is reduced by organic matter (e.g., blood, feces), surfaces must be precleaned before Safety of environmental services personnel
disinfection (102, 103). Use in spraying or fogging technologies not
Accelerated hydrogen peroxide: Recently introduced surface disinfectants with generally short recommended
required dwell times; they are bactericidal, virucidal, fungicidal, sporicidal, and mycobactericidal.
Lower-level concentrations are used for disinfecting hard surfaces, while higher-level concentrations
(2%) are used for high-level disinfection of medical instruments. They are considered safe for EVS
staff (i.e., lowest EPA toxicity category IV), benign for the environment, surface-compatible,
noncorrosive, and unaffected by organic material (104). However, they are more expensive than
other disinfectants, such as quaternary ammonium.
Phenolics: These are bactericidal, mycobactericidal, fungicidal, and virucidal but not sporicidal and are
used for surface disinfection (e.g., bedrails, tables) and for disinfecting noncritical medical devices.
These are less commonly used because of several disadvantages, including absorption by porous
materials, ability for residual product to irritate tissue, and depigmentation of skin.
Peracetic acid: Disinfectants that are bactericidal, fungicidal, virucidal, mycobactericidal, and sporicidal
and generally remain active in the presence of organic material. Most commonly used in automated
machines designed to sterilize medical instruments (e.g., endoscopes, dental instruments) and in a
formulation with hydrogen peroxide to disinfect hemodialyzers, although they have potential to
corrode metals, such as copper and brass.

Automated or no-touch modalities

UV-C devices: Uses UV-C wavelength light, which is germicidal and involves breaking of molecular Application
bonds in DNA, resulting in microorganism death. UV-C has microbicidal activity against a wide range Automated dispersal system
of health care–associated pathogens, including C. difficile. More rapid room decontamination Considerations for use
compared with hydrogen peroxide–producing systems but requires the user to move Requires the room to be vacated before
equipment/furniture away from walls to prevent shadowing. decontamination
Hydrogen peroxide systems: Several systems that produce hydrogen peroxide using differing Adjunctive disinfection measure and limited
methods are available (e.g., dry mist, vapor). These systems demonstrate reliable microbicidal to terminal disinfection (versus daily routine
activity against various health care–associated pathogens, including C. difficile. Can uniformly disinfection)
distribute hydrogen peroxide without requiring user to move equipment/furniture. Significant cost
Significant time to effectively disinfect a room

Self-disinfecting surfaces
Heavy metals, such as copper and silver: Copper generally toxic to most microorganisms due to Application
generation of reactive oxygen species, resulting in damage of nucleic acids, proteins, and lipids, and Coating of high-touch surfaces, such as bed
ultimately cell death. Has been examined as a mechanism to kill clinically important pathogens, rails, trays, and intravenous poles
including MRSA, Escherichia coli, Enterococcus spp., and Mycobacterium tuberculosis. Silver has Considerations for use
greatest antimicrobial activity of heavy metals, but mechanism of action not completely elucidated Used as an adjunct to routine room
and clinical impact has not been evaluated. disinfection
Altered topography: Materials with altered surface topography to inhibit bacterial biofilm formation Not currently considered standard of care
are currently under investigation. No data exist on use in the real-world hospital environment, and
disadvantages include potential difficulty in retrofitting surfaces with these materials, as well as lack
of microbicidal properties.
Light-activated antimicrobial surface coatings: Irradiation of certain compounds (e.g., titanium dioxide,
photosensitizers) with visible or UV light results in the production of reactive radicals that
nonselectively target microorganisms, although it is unclear whether these surfaces are sporicidal.
Although these surfaces may provide a less toxic approach than the use of chemical disinfectants, a
constant source of photoactivation is required.
EPA = U.S. Environmental Protection Agency; EVS = environmental services; MRSA = methicillin-resistant Staphylococcus aureus; UV = ultraviolet;
UV-C = ultraviolet C.

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 Appendix Table 4. Monitoring Methods Used in Acute Care Settings

Product Description Considerations for Use

Visual inspection
Covert visual monitoring of EVS staff during actual cleaning or visual Advantages
inspection postcleaning is used to provide an objective assessment of an Straightforward
individual staff member's adherence to routine cleaning protocols, often Easy to implement
in conjunction with direct feedback and educational interventions. Often performed by EVS managers
May be related to patients' perceptions of cleanliness and
satisfaction
Disadvantages
Direct visual inspection can assess only visible cleanliness (e.g.,
removal of organic debris, dust, moisture) from surfaces and not
microbial contamination
Interobserver variability
Biases secondary to the Hawthorne effect (when the presence of
observation affects observed behavior)

Aerobic colony counts

A microbiologic method used to quantify microbial contamination of Advantages
environmental surfaces. Swab cultures are typically used to sample Aerobic culture (with or without enumerating colony counts) is the
irregular surfaces and inoculated onto agar, often with broth enrichment. only method that can provide information about the viability of
Sampling of flat environmental surfaces can also be performed using pathogens of interest (e.g., MRSA, VRE)
Rodac contact plates, which are small petri plates filled with agar. A less Disadvantages
commonly used method is the agar slide culture, in which an agar-coated Lack of accepted criteria for defining a surface as “clean”
slide with finger holds is used for sampling of flat, hard surfaces. Cost of processing (e.g., identifying isolates in the microbiology
laboratory)
Delay in results
Small sample area per swab or slide
Need to determine precleaning levels of microbial
decontamination for each object/surface evaluated

UV light—visible surface markers

Used to determine adequate removal of fluorescent markers (powder or Advantages of fluorescent marker gel formulation
gel formulations) on high-touch surfaces. Dries to a transparent finish on surfaces; is abrasion-resistant; and,
unlike powder, is not easily disturbed
Most well-studied method to assess surface cleaning and to
quantify the impact of educational interventions
Disadvantages of fluorescent markers
Surfaces that are effectively disinfected (i.e., decreased microbial
contamination) but less effectively cleaned may be noted as a
failure to meet quality standards of cleaning
Cannot be used to detect the presence of a specific organism;
therefore, its utility during a pathogen-specific outbreak may be
limited

ATP bioluminescence assays

Detect the presence of organic debris on surfaces. Cutoffs used to classify Advantages
surfaces as “clean” by ATP bioluminescence assays depend on the assay Easy to use
system used. Can provide direct, rapid feedback to staff
Disadvantages
Detect the presence of both viable and nonviable bioburden on
surfaces, so the presence of ATP does not necessarily indicate
viable pathogens on the tested surface
Cutoff level to be used as a surrogate measure of an increased risk
for health care–associated infections has not yet been defined

PCR
PCR-based assays for assessing environmental contamination are currently Advantages
investigational. These assays are done in the microbiology laboratory Rapid turnaround time for specific organisms
after sampling of surfaces, usually via swabs. Disadvantages
Do not differentiate between viable versus nonviable organisms
Cost
ATP = adenosine triphosphate; EVS = environmental services; MRSA = methicillin-resistant Staphylococcus aureus; PCR = polymerase chain
reaction; UV = ultraviolet; VRE = vancomycin-resistant enterococcus.

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 Appendix Figure. Summary of evidence search and selection.

Studies identified through

database searching
(n = 4087)

Studies excluded at title/abstract level

(n = 3868)

Full-text studies assessed

for eligibility Excluded (n = 131)
(n = 219) Not location/setting of interest: 44
Not a publication type of interest: 21
Duplicate population: 18
Not a population of interest: 1
Not a pathogen of interest: 3
Does not address a guiding question: 44
Full-text studies retrieved (n = 80)*
Clinical studies: 80

Included in literature scan (n = 80)

Primary studies: 76
Systematic reviews: 4

* Gray literature included 6 clinical practice guidelines and 2 background articles. These were used for background information and were not
included in the systematic overview.

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 Appendix Table 5. Clinical Practice Guidelines

Organization Reference Country Methods

(Evidence-Based or
Consensus-/
Narrative-Based)
American College of Surawicz CM et al. Guidelines for diagnosis, treatment, and prevention of United States Evidence-based
Gastroenterology Clostridium difficile infections. Am J Gastroenterol. 2013 Apr;108(4):478-98.
AHE, formerly known as Association for the Healthcare Environment. Practice guidance for healthcare United States Evidence-based
ASHES (part of the environmental cleaning, 2nd edition. Chicago (IL): American Hospital Association;
American Hospital 2010.
Association)
AHRQ Collins AS. Chapter 41. Preventing health care–associated infections. In: Hughes RG, United States Evidence-based
editor. Patient safety and quality: An evidence-based handbook for nurses.
Rockville (MD): Agency for Healthcare Research and Quality; 2008. p. 547-75.
Also available: www.ncbi.nlm.nih.gov/books/NBK2683/pdf/ch41.pdf.
APIC Association for Professionals in Infection Control and Epidemiology. APIC position United States Consensus/narrative
on mandatory public reporting of HAIs. Washington (DC): Association for
Professionals in Infection Control and Epidemiology; 2005 Mar 14. 3 p. Also
available: www.apic.org/Resource_/TinyMceFileManager/Position_Statements
/MandRpt_posnPaoper_2005.pdf.
Greene LR et al. APIC Position Paper: The importance of surveillance technologies United States Evidence-based
in the prevention of healthcare-associated infections (HAIs). Washington (DC):
2009 May 29. 7 p.
Cardo D et al. Moving toward elimination of healthcare-associated infections: a call United States Consensus/narrative
to action. [White paper]. Am J Infect Control. 2010 Nov;38(9):671-5. “A joint white
paper between APIC, SHEA, Infectious Diseases Society of America, Association
of State and Territorial Health Officials, Council of State and Territorial
Epidemiologists, Pediatric Infectious Diseases Society, and the Centers for
Disease Control and Prevention.”
Friedman C et al. APIC/CHICA-Canada infection prevention, control, and Canada Consensus/narrative
epidemiology: Professionals and practice standards. Washington (DC):
Association for Professionals in Infection Control and Epidemiology; 2008. 5 p.
Association for Professionals in Infection Control and Epidemiology, Inc. Guide to United States Consensus/narrative
preventing Clostridium difficile infections. Washington (DC): Association for
Professionals in Infection Control and Epidemiology, Inc.; 2013 Feb. 100 p. Also
available: www.apic.org/Resource_/EliminationGuideForm/59397fc6-3f90-43d1
-9325-e8be75d86888/File/2013CDiffFinal.pdf.
Association for Professionals in Infection Control and Epidemiology. Guide to the United States Evidence-based
elimination of methicillin-resistant Staphylococcus aureus (MRSA) transmission in
hospital settings, 2nd edition. Washington (DC): Association for Professionals in
Infection Control and Epidemiology; 2010. 65 p. Also available: www.apic.org
/Resource_/EliminationGuideForm/631fcd91-8773-4067-9f85-ab2a5b157eab
/File/MRSA-elimination-guide-2010.pdf.
Association for Professionals in Infection Control and Epidemiology. Guide to the United States Consensus/narrative
elimination of methicillin-resistant Staphylococcus aureus (MRSA) transmission in
hospital settings. California supplement 2009. Washington (DC): Association for
Professionals in Infection Control and Epidemiology, Inc.; 2009 Apr 3. 12 p. Also
available: www.apic.org/Resource_/EliminationGuideForm/16c7a44f-55fe-4c7b
-819a-b9c5907eca72/File/APIC-MRSA-California.pdf.
Association for Professionals in Infection Control and Epidemiology. Guide to the United States Evidence-based
elimination of methicillin-resistant Staphylococcus aureus (MRSA) in the long-term
care facility. Washington (DC): Association for Professionals in Infection Control
and Epidemiology; 2009. 74 p. Also available: www.apic.org/Resource_/
EliminationGuideForm/08b12595-9f92-4a64-ad41-4afdd0088224/File/APIC-
MRSA-in-Long-Term-Care.pdf.
AORN Association of Perioperative Registered Nurses. Recommended practices for United States Evidence-based
environmental cleaning. In: 2014 perioperative standards and recommended
practices. Denver (CO): Association of perioperative Registered Nurses; 2013
Sep. p. 255-76. NGC summary.
Allen G. Implementing AORN recommended practices for environmental cleaning. United States Evidence-based
AORN J. 2014 May;99(5):570-82. See: http://dx.doi.org/10.1016/j.aorn
.2014.01.023.
ASID Stuart RL et al. ASID/AICA position statement: Infection control guidelines for Australia Consensus/narrative
patients with Clostridium difficile infection in healthcare settings. Healthc Infect.
Mar 2011;16(1):33-9. Also available: http://dx.doi.org/10.1071/HI11011.
Cheng AC et al. Australasian Society for Infectious Diseases guidelines for the Australia Evidence-based
diagnosis and treatment of Clostridium difficile infection. Med J Aust. 2011 Apr
4;194(7):353-8.
CIBMTR Tomblyn M et al. Guidelines for preventing infectious complications among Multinational Evidence-based
hematopoietic cell transplantation recipients: a global perspective. Biol Blood
Marrow Transplant. 2009 Oct;15(10):1143-238.
Continued on following page

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 Appendix Table 5—Continued

Organization Reference Country Methods

(Evidence-Based or
Consensus-/
Narrative-Based)
CDC, including HICPAC Rutala WA, Weber DJ, Healthcare Infection Control Practices Advisory Committee. United States Evidence-based
Guideline for disinfection and sterilization in healthcare facilities, 2008. Atlanta
(GA): Centers for Disease Control and Prevention; 2008. 158 p. Also available:
www.cdc.gov/hicpac/Disinfection_Sterilization/17_00Recommendations.html. See
also: Recommendations for disinfection and sterilization in health-care facilities.
Centers for Disease Control and Prevention. Antibiotic resistance threats in the United States Evidence-based
United States, 2013. Atlanta (GA): Centers for Disease Control and Prevention;
2013. 114 p. Also available: www.cdc.gov/drugresistance/threat-report-2013/pdf
/ar-threats-2013-508.pdf.
Guh A. Carling P, Environmental Evaluation Workgroup. Division of Healthcare United States Consensus/narrative
Quality Promotion; National Center for Emerging, Zoonotic and Infectious
Diseases. Options for evaluating environmental cleaning. [Toolkit]. 2010. Atlanta
(GA): Centers for Disease Control and Prevention; 2010 Dec.15 p. Also available:
www.cdc.gov/HAI/pdfs/toolkits/Environ-Cleaning-Eval-Toolkit12-2-2010.pdf.
Note: Additional resources.
McKibben L et al. Guidance on public reporting of healthcare-associated infections: United States Consensus/narrative
Recommendations of the Healthcare Infection Control Practices Advisory
Committee. Am J Infect Control. 2005 May;33(4):217-26.
Recommendations for Preventing the Spread of Vancomycin Resistance United States Consensus/narrative
Recommendations of the Hospital Infection Control Practices Advisory Committee
(HICPAC). MMWR Recomm Rep. 1995 Sep 22;44(RR-12):1-13.
Sehulster L et al. Guidelines for environmental infection control in healthcare United States Evidence-based
facilities. Recommendations of CDC and the Healthcare Infection Control
Practices Advisory Committee (HICPAC) [Published errata appear in MMWR
Recomm Rep 2003 Oct 24;52(42):1025-6]. MMWR Recomm Rep. 2003 Jun
6;52(RR-10):1-42.
Siegel J et al. Guideline for isolation precautions: preventing transmission of United States Evidence-based
infectious agents in healthcare settings. Atlanta (GA): Centers for Disease Control
and Prevention; 2007 Jun. 219 p.
Siegel JD et al. Management of multidrug-resistant organisms in healthcare settings. United States Evidence-based
2006. 74 p.
Umscheid C et al. Updating the Guideline Methodology of the Healthcare Infection United States Evidence-based
Control Practices Advisory Committee (HICPAC). Atlanta (GA): Centers for
Disease Control and Prevention; 31 p. Also available: www.cdc.gov/hicpac/pdf
/guidelines/2009-10-29HICPAC_GuidelineMethodsFINAL.pdf. Publication date
not available.
ECDC Vonberg RP et al. Infection control measures to limit the spread of Clostridium Europe Evidence-based
difficile. Clin Microbiol Infect. 2008 May;14:2-20. Also available:
http://dx.doi.org/10.1111/j.1469-0691.2008.01992.x.
ESCMID European Society of Clinical Microbiology and Infectious Diseases. ESCMID Europe Consensus/narrative
consensus statements. Basel (Switzerland): European Society of Clinical
Microbiology and Infectious Diseases; MRSA expert consensus documents, 2013
Feb 14. www.escmid.org/escmid_library/medical_guidelines/escmid_consensus
_statements/. Accessed 2014 Oct 7. Note: See Humphreys H et al. Workshop 2 for
cleaning.
EPA U.S. Environmental Protection Agency. Antimicrobial testing program – guideline United States Evidence-based
methodology. Washington (DC): U.S. Environmental Protection Agency; 2014
Aug 21. www.epa.gov/oppad001/antimicrobial-testing-program.html. Accessed
2014 Oct 7. Note: includes test results from August 2014.
See also: The antimicrobial testing program. Hospital disinfectant and tuberculocidal
products tested or pending testing. [List of products]. 2014 Aug 21.
GAO Bascetta CA. Health-care-associated infections in hospitals: Leadership needed from United States Evidence-based
HHS to prioritize prevention practices and improve data on these infections:
Report to the Chairman, Committee on Oversight and Government Reform,
House of Representatives. Washington (DC): U.S. Government Accountability
Office; 2008 Mar. 61 p. Also available: www.gao.gov/assets/280/274314.pdf.
Healthcare-Associated Healthcare-Associated Infection Working Group of the Joint Public Policy United States Evidence-based
Infection Working Committee. Essentials of public reporting of HAIs, Healthcare-Associated
Group of the Joint Infection Working Group of the Joint Public Policy Committee toolkit. 4 p. Also
Public Policy available: www.apic.org/Resource_/TinyMceFileManager/Position_Statements
Committee (APIC, /Essentials_Tool_Kit.pdf. Publication date not provided.
CDC, CSTE, and SHEA)
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 Appendix Table 5—Continued

Organization Reference Country Methods

(Evidence-Based or
Consensus-/
Narrative-Based)
Healthcare Infection Coia JE et al. Guidelines for the control and prevention of methicillin-resistant United Evidence-based
Society (United Staphylococcus aureus (MRSA) in healthcare facilities. J Hosp Infect. 2006 Kingdom
Kingdom) (formerly, May;63:1-44. Also available: http://dx.doi.org/10.1016/j.jhin.2005.10.014.
the Hospital Infection Cookson BD et al. Guidelines for the control of glycopeptide-resistant enterococci United Evidence-based
Society) in hospitals. J Hosp Infect. 2006 Jan;62(1):6-21. Also available: http://dx.doi Kingdom
.org/10.1016/j.jhin.2005.02.016.
Loveday HP et al. epic3: national evidence-based guidelines for preventing United Evidence-based
healthcare-associated infections in NHS Hospitals in England. J Hosp Infect. 2014 Kingdom
Jan;86. Also available: http://dx.doi.org/10.1016/S0195-6701(13)60012-2.
National Clostridium difficile Standards Group: Report to the Department of Health. United Evidence-based
J Hosp Infect. 2004 Feb;56 Suppl 1:1-38. Kingdom
Pratt RJ et al. epic2: National Evidence-Based Guidelines for Preventing United Evidence-based
Healthcare-Associated Infections in NHS Hospitals in England. J Hosp Infect. 2007 Kingdom
Feb;65. Also available: http://dx.doi.org/10.1016/S0195-6701(07)60002-4.
Steer JA et al. Guidelines for prevention and control of group A streptococcal United Evidence-based
infection in acute healthcare and maternity settings in the UK. J Infect. 2012 Kingdom
Jan;64(1):1-18. Also available: http://dx.doi.org/10.1016/j.jinf.2011.11.001.
Infection Control Working Neely AN et al. Computer equipment used in patient care within a multihospital United States Evidence-based
Group system: recommendations for cleaning and disinfection. Am J Infect Control.
2005 May;33(4):233-7. Also available: http://dx.doi.org/10.1016/j.ajic
.2005.03.002.
IPS, formerly ICNA Infection Prevention Society. Care setting process improvement tool in & out patient United States Evidence-based
areas/departments. Bathgate (Scotland): Infection Prevention Society; 44 p. Also
available: www.ips.uk.net/files/8213/8044/9268/In_-_Out_Patient_Area
_Departments_PIT.pdf. No publication date.
IOM Institute of Medicine. Initial national priority for comparative effectiveness research. United States Evidence-based
[book online]. Washington (DC): National Academies Press; 2009 Jan 1. [accessed
2010 Mar 3] [various].
IFIC Damani N. Information resources in infection control, 6th edition. Armagh (Ireland): United Evidence-based
International Federation of Infection Control; 2009. 96 p. Also available: Kingdom
www.theific.org/pdf_files/resource_IFIC_Sept_2009.pdf.
Jhpiego Corporation, an Tietjen L et al. Infection prevention guidelines for healthcare facilities with limited United States Evidence-based
affiliate of Johns resources. Jhpiego Corporation; 2003. 419 p. Also available:
Hopkins University http://pdf.usaid.gov/pdf_docs/Pnact433.pdf.
Joint Commission It's all the on the surface: establishing protocols for cleaning and disinfecting United States Evidence-based
environmental surface areas. Environ Care News. 2010 Mar;13(3):6-11. Also
available: www.jointcommission.org/assets/1/18/Its_All_on_the_Surface.pdf.
The Joint Commission. National patient safety goals effective January 1, 2014. United States Evidence-based
Hospital accreditation program. Oakbrook Terrace (IL): The Joint Commission;
2013. 17 p. See: www.jointcommission.org/assets/1/6
/HAP_NPSG_Chapter_2014.pdf.
Massachusetts Nurses Massachusetts Nurses Association. Exposure to environmental cleaning chemicals in United States Consensus/narrative
Association healthcare settings. Canton (MA): Massachusetts Nurses Association; 2007 Oct 1.
www.massnurses.org/nursing-resources/position-statements/env-cleaning-chem.
Accessed 2014 Oct 7.
Mehta et al Mehta Y et al. Guidelines for prevention of hospital acquired infections. Indian J Crit India Evidence-based
Care Med. 2014 Mar;18(3):149–63. Also available: http://dx.doi.org/10.4103
/0972-5229.128705.
NICE Prevention and control of healthcare-associated infections: quality improvement United Evidence-based
guide. PH36. London (UK): National Institute for Health and Care Excellence Kingdom
(NICE); 2011 Nov 1. http://publications.nice.org.uk/prevention-and-control-of
-healthcare-associated-infections-ph36. Accessed 2013 Oct 1. See: Quality
improvement statement 5: Environmental cleanliness.
NPSA United Kingdom National Patient Safety Agency. National specifications for cleanliness: primary United Consensus/narrative
medical and dental premises. London (UK): National Patient Safety Agency; 2010 Kingdom
Aug. 44 p. Also available: www.nrls.npsa.nhs.uk/EasySiteWeb/getresource
.axd?AssetID=75245%20.
NPSA National Patient Safety Agency. The revised healthcare cleaning manual. London: United Evidence-based
National Patient Safety Agency; 2009 Jun. 174 p. Also available: Kingdom
www.nrls.npsa.nhs.uk/EasySiteWeb/getresource.axd?AssetID=61814.
PIDAC Provincial Infectious Diseases Advisory Committee. Routine practices and additional Canada Evidence-based
precautions in all health care settings, 3rd edition. Ottawa (Ontario): Public Health
Ontario; 2012 Nov.113 p. Also available: www.publichealthontario.ca/en/
eRepository/RPAP_All_HealthCare_Settings_Eng2012.pdf.
Provincial Infectious Diseases Advisory Committee. Best practices for environmental Canada Evidence-based
cleaning for prevention and control of Infections In all health care settings-2nd
edition. Ottawa (Ontario): Public Health Ontario; 2012 May.183 p.
Provincial Infectious Diseases Advisory Committee. Review of literature for Canada Evidence-based
evidence-based best practices for VRE control. Ottawa (Ontario): Public Health
Ontario; 2012. 24 p. Also available: www.publichealthontario.ca/en/eRepository
/PIDAC-IPC_VRE_Evidence-based_Review_2012_Eng.pdf.
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 Appendix Table 5—Continued

Organization Reference Country Methods

(Evidence-Based or
Consensus-/
Narrative-Based)
Public Health Agency of Public Health Agency of Canada. Clostridium difficile infection-infection prevention Canada Evidence-based
Canada and control guidance for management in acute care settings. Ottawa (Ontario):
Public Health Agency of Canada; 2013 Jan 1. www.phac-aspc.gc.ca/nois-sinp
/guide/c-dif-acs-esa/index-eng.php. Accessed 2014 Oct 7. See the section: 14.
Environmental cleaning.
Public Health Agency of Canada. Routine practices and additional precautions for Canada Evidence-based
preventing the transmission of infection in healthcare settings. Ottawa (ON):
Public Health Agency of Canada; 2012. 195 p. Also available: http://publications
.gc.ca/collections/collection_2013/aspc-phac/HP40-83-2013-eng.pdf.
Royal College of Nursing Royal College of Nursing. Creating a safe environment for care: Defining the United Consensus/narrative
relationship between cleaning and nursing staff. London: Royal College of Kingdom
Nursing; 2013. 11 p. Also available: www.rcn.org.uk/__data/assets/pdf_file/0007
/548719/004492.pdf.
Royal College of Nursing. Essential practice for infection prevention and control: United Consensus/narrative
guidance for nursing staff. London: Royal College of Nursing; 2012. 36 p. Also Kingdom
available: www.rcn.org.uk/__data/assets/pdf_file/0008/427832/004166.pdf. Note:
See sections: 3.2 Decontamination of equipment; and 3.3 Achieving and
maintaining a clean clinical environment.
Royal College of Nursing. Selection and use of disinfectant wipes. RCN guidance. United Evidence-based
London: Royal College of Nursing; 2011. 20 p. Also available: www.rcn.org Kingdom
.uk/__data/assets/pdf_file/0011/382538/003873.pdf.
Public Health England/ Department of Health, Health Protection Agency. Clostridium difficile infection: how United Evidence-based
Department of Health to deal with the problem. [Guidance]. London (UK): Healthcare Associated Kingdom
Infection and Antimicrobial Resistance, Department of Health; 2008 Dec. 140 p.
Note: See chapter 6: Prevention through environmental cleaning and disinfection.
Wilcox M. Updated guidance on the management and treatment of C. difficile United Evidence-based
infection. London: Public Health England; 2013. 29 p. Also available: Kingdom
www.gov.uk/government/uploads/system/uploads/attachment_data/file/321891/
Clostridium_difficile_management_and_treatment.pdf.
Rudolf Schuelke Gebel J et al. The role of surface disinfection in infection prevention. [Consensus Germany Evidence-based
Foundation (Germany) paper]. GMS Hyg Infect Control. 2013;8(1):Doc10. Also available:
http://dx.doi.org/10.3205/dgkh000210.
SHEA Society for Healthcare Epidemiology of America. Compendium of strategies to United States Evidence-based
prevent healthcare-associated infections in acute care hospitals—overview page.
Arlington (VA): Society for Healthcare Epidemiology of America; 2014 Jan 1.
www.shea-online.org/PriorityTopics/CompendiumofStrategiestoPreventHAIs.aspx.
Accessed 2014 Oct 7. Note: This is an overview page. The recommendation
sections related to this Technical Brief are listed in the next two documents.
Calfee DP et al. Strategies to prevent methicillin-resistant Staphylococcus aureus United States Evidence-based
transmission and infection in acute care hospitals: 2014 update. Infect Control
Hosp Epidemiol. 2014 Jul;35(7):772-96. Also available: http://dx.doi.org/10
.1086/676534. Note: from the 2014 Compendium.
Dubberke ER et al. Strategies to prevent Clostridium difficile infections in acute care United States Evidence-based
hospitals: 2014 update. Infection control and hospital epidemiology: the official
journal of the Society of Hospital Epidemiologists of America. 2014
Jun;35(6):628-45. Also available: http://dx.doi.org/10.1086/676023. Note: from
the 2014 Compendium.
Calfee DP et al. Strategies to Prevent Transmission of Methicillin-Resistant United States Evidence-based
Staphylococcus aureus in Acute Care Hospitals. Infect Control Hosp Epidemiol.
2008 Oct;29 Suppl 1:S62-80. Note: from the 2008 Compendium.
Dubberke ER et al. Strategies to Prevent Clostridium difficile Infections in Acute Care United States Evidence-based
Hospitals. Infect Control Hosp Epidemiol. 2008 Oct;29 Suppl 1:S81-92. Note:
from the 2008 Compendium.
Cohen SH, et al. Clinical practice guidelines for Clostridium difficile infection in United States Evidence-based
adults: 2010 Update by the Society for Healthcare Epidemiology of America
(SHEA) and the Infectious Diseases Society of America (IDSA). Infect Control Hosp
Epidemiol. 2010 May;31(5):431-55.
Muto CA, et al. SHEA guideline for preventing nosocomial transmission of United States Evidence-based
multidrug-resistant strains of Staphylococcus aureus and Enterococcus. Infect
Control Hosp Epidemiol. 2003 May;24(5):362-86. Also available:
www.journals.uchicago.edu/doi/pdf/10.1086/502213.
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 Appendix Table 5—Continued

Organization Reference Country Methods

(Evidence-Based or
Consensus-/
Narrative-Based)
CMS U.S. Centers for Medicare and Medicaid Services. State operations manual: United States Consensus/narrative
Appendix A—survey protocol, regulations and interpretive guidelines for
hospitals. (Rev. 116, 06-06-14). Baltimore (MD): U.S. Centers for Medicare and
Medicaid Services; 2014 Jun 6. 471 p. (CMS State Operations Manuals). Also
available: www.cms.gov/Regulations-and-Guidance/Guidance/Manuals
/downloads/som107ap_a_hospitals.pdf.
Also may be of interest: Peasah SK et al. Medicare non-payment of
hospital-acquired infections: infection rates three-years post-implementation.
MMWR 2013;3(3).
HHS U.S. Department of Health and Human Services. National action plan to prevent United States Evidence-based
health care-associated infections: road map to elimination. Washington (DC):
U.S. Department of Health and Human Services (HHS). www.health.gov/hai
/prevent_hai.asp#hai_plan. Accessed 2014 Oct 7.
WHO Ducel G et al. Prevention of hospital-acquired infections: a practical guide. 2nd International Evidence-based
edition. Geneva (Switzerland): World Health Organization; 2002. 72 p.
Also available: www.who.int/csr/resources/publications/drugresist/en
/whocdscsreph200212.pdf?ua=1.
AHE = Association for the Healthcare Environment; AHRQ = Association for Healthcare Research and Quality; AORN = Association of Perioperative
Registered Nurses; APIC = Association for Professionals in Infection Control and Epidemiology; ASHES = American Society for Healthcare Environ-
mental Services; ASID = Australasian Society for Infectious Diseases; CDC = Centers for Disease Control and Prevention; CIBMTR = Center for
International Blood and Marrow Transplant Research; CMS = Centers for Medicare & Medicaid Services; CSTE = Council of State and Territorial
Epidemiologists; ECDC = European Centre for Disease Control and Prevention; EPA = U.S. Environmental Protection Agency; ESCMID = European
Society of Clinical Microbiology and Infectious Diseases; GAO = Government Accounting Office; HHS = U.S. Department of Health and Human
Services; HICPAC = Healthcare Infection Control Practices Advisory Committee; ICNA = Infection Control Nurses Association; IFIC = International
Federation for Infection Control; IOM = Institute of Medicine; IPS = Infection Prevention Society; NGC = National Guideline Clearinghouse; NICE =
National Institute for Health and Care Excellence; NPSA = National Patient Safety Agency; PIDAC = Public Health Ontario, Provincial Infectious
Diseases Advisory Committee; SHEA = Society for Healthcare Epidemiology of America; WHO = World Health Organization.

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 Appendix Table 6. Ongoing Clinical Trials

ClinicalTrials Sponsor Study Purpose Start Date Expected Completion Estimated Primary Outcomes

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.gov Design Date Enrollment
Identifier
NCT01579370 Duke University Randomized, To determine the efficacy and feasibility of April 2012 October 2014 50 000 Incidence rate of 4 target organisms
controlled enhanced terminal room disinfection (MRSA, VRE, Clostridium difficile,
strategies to prevent health care– and MDR-acinetobacter) among
associated infections and to determine patients admitted to a study room
the impact of environmental Incidence rate of C. difficile among

Annals of Internal Medicine • Vol. 163 No. 8 • 20 October 2015

contamination on acquisition of MDR patients admitted to a study room
pathogens among hospitalized patients.
The intervention group includes
quaternary ammonium, bleach,
quaternary ammonium and UV-C light,
and bleach and UV-C light.
NCT01349192 University of North Randomized, To determine whether an early eradication April 2011 July 2015 80 Percentage of participants in each
Carolina, Chapel controlled protocol is effective for eradicating group with MRSA-negative
Hill MRSA and will provide an opportunity to respiratory cultures at day 28
obtain data about early clinical impact of
new isolation of MRSA.
The intervention group includes an
environmental decontamination
component, including wiping down
high-touch surfaces and medical
equipment with surface disinfecting
wipes daily for 21 d.
NCT02348346 Dr. B. de Jong Observational To study the efficacy of MVX on the March December 2015 NR –
microbial colonization of surfaces in the 2015
ICU.
ICU = intensive care unit; MDR = multidrug-resistant; MRSA = methicillin-resistant Staphylococcus aureus; MVX = titanium dioxide; NR = not reported; UV-C = ultraviolet-C; VRE = vancomycin-
resistant enterococci.

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 Appendix Table 7. Characteristics of Systematic Reviews
Study, Year Objective Search Strategy Key Inclusion/Exclusion Evidence Base Interventions Relevant Findings Authors’ Conclusions

www.annals.org
(Reference) Criteria

Amodio and To systematically Searches were completed Articles were excluded Studies: 12 studies published ATP devices were ATP measurements before “Although the use of ATP
Dino, review the in PubMed and Scopus. for not pertaining to from 2000–2011 were provided by 3M (5), cleaning (RLUs): Ranged from 0 bioluminescence can be
2014 (60) evidence Bibliographies of hospital surfaces, included. Studies were done in Biotrace (4), and to >500 000. considered a quick and
on ATP articles retrieved were being an experimental the United Kingdom (8), United Hygiena (3). ATP measurements after cleaning objective method for
bioluminescence also searched. 31 design, or being States (3), and Brazil (1). ATP thresholds (RLUs): (RLUs): Ranged from 3 to 500 assessing hospital cleanliness,
articles were considered published before Methods: Surfaces were 100: 2 (16.7%) 000 it appears to be still poorly
for inclusion. 1990. monitored after cleaning (4 250: 5 (41.7%) Failure rates before cleaning: standardized at both the
studies), before and after 500: 4 (33.3%) 21.2%–93.1%. national and international
cleaning (6 studies), or NR (2). Both 250 and 500: 1 Failure rates after cleaning: level.”
Pathogens were not described. (8.3%) 5.3%–96.5%.
Mitchell To describe Searches in MEDLINE, Article addressing the 124 articles were reviewed. Visual inspection, Visual inspection (6 studies): Poor “Methods that evaluate cleaning
et al, monitoring CINAHL, and PubMed efficacy of cleaning. Number of articles include: NR. fluorescent gel marker, performance at identifying performance are useful in

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2013 (61) methods for English-language Environmental ATP, microbial cultures microbial load with 17%–93% assessing adherence to
used in publications. A search of cleanliness was more surfaces identified as cleaning protocols, whereas
environmental the gray literature categorized as “clean” than other assessment methods that sample
cleaning included infection- process evaluation methods. bio-burden provide a more
control professional (visual inspection, use Fluorescent gel marker (7 studies): relevant indication of infection
organization Web sites, of fluorescent gel Frequently shows a “lack of risk. Fast, reproducible,
Australian state marker) and outcome attention to high-risk surfaces in cost-effective and reliable
government sites, and evaluation (use of ATP the near-patient zone.” methods are needed for
international guidelines. or microbial cultures). ATP: ATP measurements have low routine environmental
specificity and sensitivity in cleaning evaluation in order to
detecting bacteria (1 study predict timely clinical risk.”
reported sensitivity/specificity
of 57%).
Factors that may affect ATP
readings include residual
detergents or disinfectants,
including sodium
hydrochloride, eroded surfaces,
plasticizers found in microfiber
cloths or ammonium
compounds found in laundry
products.
Microbiological sampling:
Sampling to detect specific
bacteria is “generally only
recommended as part of an
ongoing outbreak investigation,
as a research study, or as part of
a policy or process evaluation”
because the process may take
at least 2 d, requires expertise
and lab access.
Falagas To review the Searches were completed Included studies focused Studies: 10 studies were 7 studies evaluated the Disinfection: Contamination of “Data from several relevant
et al, effectiveness in PubMed through on the effectiveness of included. Pathogens BioQuell HPV system sampled environmental sites studies indicate that
2011 (58) of airborne December 2009. airborne hydrogen addressed were MRSA (5), (BioQuell) Before cleaning (9 studies): 39.0% disinfection of the hospital
hydrogen Bibliographies of peroxide for reducing Clostridium difficile (3), and 3 studies evaluated a (range: 18.9%–81.0%) environment using airborne
peroxide in a relevant articles were bacterial burden in the multiple pathogens (2). hydrogen peroxide After terminal cleaning (6 studies): hydrogen peroxide in vapour
clinical setting also searched. hospital setting and Settings: Surgical wards, ward dry-mist system or “dry 28.3% (range: 11.9%–66.1%) or dry mist formulations,
discussed pathogens side rooms, single isolation fog” (Gloster Sante After airborne hydrogen peroxide appears to provide additional
naturally dispersed in rooms, multiple-bed ward Europe) (10 studies): 2.2% (range: benefits to currently used
this setting. bays, bathrooms, and other 0%–4.0%) cleaning regimens, including
utility rooms. Infection control: 1 study inactivation of bacterial
High-touch areas: Chairs, bed indicated eradication of MRSA spores. Few studies have
frames, control panels, in one 20-bed surgical ward. evaluated the use of airborne
bedside tables, remote Another study indicated hydrogen peroxide
controls, door handles, bed significant reductions in C. disinfection as an adjunctive
rails, telephones, sink taps, difficile–associated disease in a infection control measure in
toilet seats, and sites handled 500-bed university-affiliated actual hospital practice. These
by HCWs. hospital. limited relevant data are
Pathogens: MRSA, C. difficile, and favourable, but further studies
others. are needed to assess the
effectiveness, safety, costs,
and applicability of this novel
method against other
available cleaning methods.”

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 Appendix Table 7—Continued

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Study, Year Objective Search Strategy Key Inclusion/Exclusion Evidence Base Interventions Relevant Findings Authors’ Conclusions
(Reference) Criteria

Dettenkofer To review Biological Abstracts/ Randomized, controlled 4 trials discussed impact of Dharan study: QAC, an Dharan study “Disinfectants may pose a
et al, evidence for BIOSIS Previews trials and cohort, disinfectant vs. detergent on active oxygen-based Detergent only: Increase in danger to staff, patients, and
2004 (59) the effects of (1980–1988/1989– case–control, and environmental surfaces. compound, and an bacterial surface counts the environment and require
disinfection of 2001); Cochrane Library observational studies Dharan study compared NI rates alcohol solution QAC: No reduction in bacterial special safety precautions.
environmental (2001, Issue 4) in English, German, in 2 different wings of a Danforth study: counts However, targeted
surfaces on Cochrane Clinical Trials French, Italian, and medical unit over 4 mo. Disinfectant Active oxygen-based disinfection of certain
hospital- Register; HECLINET Spanish evaluating Danforth study used a crossover ortho-benzyl compound, the alcohol environmental surfaces is in

Annals of Internal Medicine • Vol. 163 No. 8 • 20 October 2015

acquired (1969–2000); MEDLINE use of disinfectant or design to examine NI rates parachlorophenol or solution, and the certain instances an
infection rates (Ovid, 1966–2001); detergent for in 8 wards in a tertiary-care detergent dust-attracting floor mop: established component of
Science Citation Index “inanimate surfaces” in teaching hospital over 3 mo. Daschner study: Significant reduction of hospital infection control.
(1991–1996); SwetScan health care settings Daschner study examined NI Disinfectant (0.5% bacterial counts Given the complex,
(1997–2001); Web of were included. rates in ICU units over 12 aldehyde) and Dharan, Danforth, and Dashner multifactorial nature of
Science (Science mo. detergent studies nosocomial infections,
Citation Index Mayfield study examined use of 2 Mayfield study: QAC or Occurrence of NI: No significant well-designed studies that
Expanded, 1997–2001); disinfectants on incidence of 1:10 hypochlorite difference systematically investigate the
EMBASE (1974–2001) C. difficile in bone marrow solution Mayfield study role of surface disinfection are
and EMBASE alert; and transplant patients and CDAD incidence: Significant required.”
Somed (1978–2000). patients in neurosurgical decrease in rates in bone
General Internet search ICU and general medicine marrow transplant patients,
was also undertaken. units. no reduction in patients on
High-touch areas: neurosurgical ICU or general
Floors, furniture, bathrooms, medicine unit
toilets, and isolation rooms
(Dharan)
Floor (Danforth)
Floor, patient care equipment,
bedside tables, and bed
frame (Daschner)
Not described (Mayfield)
Pathogens: MRSA, C. difficile, and
others

ATP = adenosine triphosphate; CDAD = Clostridium difficile–associated diarrhea; HCW = health care worker; HECLINET = Health Care Literature Information Network; HPV = hydrogen peroxide
vapor; ICU = intensive care unit; MRSA = methicillin-resistant Staphylococcus aureus; NI = nosocomial infection; NR = not reported; QAC = quaternary ammonium compound; RLU = relative light
unit.

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 www.annals.org
Appendix Table 8. Characteristics of Cleaning and Disinfecting Studies
Study, Country Study Design General Study Study Size Primary Setting Pathogen HTOs Primary Outcome Authors’ Conclusions
Year Cleaning Length (Secondary
(Reference) Method Outcomes)

Best et al, United Before/after SC and 20 wk 342 sites Rehabilitation Clostridium Bed, curtain track, Sites positive for “HPD, after deep cleaning with a detergent/chlorine
2014 (39) Kingdom AC ward difficile wall trunking, C. difficile*, CDI agent, was highly effective for removing
patient line incidence† (C. environmental
boxes, tops of difficile ribotypes) C. difficile contamination. Long-term follow-up
hoist rail demonstrated that a CDI-symptomatic patient can
rapidly recontaminate the immediate
environment. Determining a role for HPD should

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include long-term cost-effectiveness evaluations.”
Boyce et al, United Before/after EC 4 wk 9 rooms Ward not NR Bed rail, remote Mean ACC* “Cultures of surfaces obtained before daily cleaning
2014 (55) States 1155 samples specified control, toilet, with a quaternary ammonium disinfectant showed
tray table, no significant residual antimicrobial activity of the
telephone, organosilane products, although a modest
doorknob, sink reduction could not be excluded.”
Haas et al, United Before/after AC 2y 11 389 rooms Ward not C. difficile, MRSA, NR Incidence rate of “During the time period UVD was in use, there was a
2014 (30) States specified VRE HAIs† significant decrease in overall hospital-acquired
MDRO plus CD in spite of missing 24% of
opportunities to disinfect contact precautions
rooms. This technology was feasible to use in our
acute care setting and appeared to have a
beneficial effect.”
Jinadatha United Nonrandomized, SC and 2 mo 20 rooms (10 Ward not MRSA Bed rail, call ACC*, total MRSA† “PPX-UV technology appears to be superior to
et al, States controlled AC per group) specified buttons, toilet, (individual surface manual cleaning alone for MRSA and HPC.
2014 (11) tray table, counts, cleaning Incorporating 15 minutes of PPX-UV exposure
bathroom time in minutes) time to current hospital room cleaning practice
handrail can improve the overall cleanliness of patient
rooms with respect to selected micro-organisms.”
Mitchell Australia Interrupted time SC and 6y 3600 Ward not MRSA Bed, vent, sink, Incidence of MRSA† “Use of HP disinfection led to a decrease in residual
et al, series AC discharge specified console, chair, MRSA contamination in patient rooms compared
2014 (13) cleans table, locker, with detergent. It may also have encouraged the
mattress, pillow reduction in patient MRSA acquisition despite
several confounders including staff feedback on
terminal cleaning, additional MRSA screening and
quicker laboratory methods. Infection control is
best served by concurrent interventions targeting
both the patient and healthcare environment.”
Sjöberg Sweden Before/after SC 8 mo 10 rooms NR C. difficile Bed rail, call Sites positive for “We demonstrated a moderate spread of CD spores
et al, 150 samples button, side culture* to the environment despite routine cleaning
2014 (24) table, toilet, procedures involving Vikron.”
doorknob
Stewart United Before/after SC 4 mo 30 bed spaces Elderly care MRSA and MSSA Bedside locker, CFU* “Cleaning with electrolyzed water reduced ACC and
et al, Kingdom left/right (recontamination) staphylococci on surfaces beside patients. ACC
2014 (57) cotside, remained below precleaning levels at 48 hours,
overbed table but MSSA/MRSA counts exceeded original levels
at 24 hours after cleaning. Although disinfectant
cleaning quickly reduces bioburden, additional
investigation is required to clarify the reasons for
rebound contamination of pathogens at near
patient sites.”
Wiemken United Randomized, SC 1 mo 9 rooms Ward not Hardy pathogens Side table, toilet, Adherence to room “In conclusion, this study supports the use of RTU
et al, States controlled specified sink protocol* (time CD wipes over the traditional bucket method.
2014 (28) needed to clean) Enhancing environmental processes may reduce
the environmental bioburden, leading to
reductions in HAIs because of environmentally
hardy pathogens.”

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 Appendix Table 8—Continued
Study, Country Study Design General Study Study Size Primary Setting Pathogen HTOs Primary Outcome Authors’ Conclusions
Year Cleaning Length (Secondary
(Reference) Method Outcomes)

Anderson United Prospective AC 15 mo 27 rooms Ward not Various Bed rail, floor, Total number of “Our data confirm that automated UV-C-emitting
et al, States cohort 142 samples specified pathogens, side table, CFUs, median devices can decrease the bioburden of important
2013 (40) including C. toilet, chair number of CFUs pathogens in real-world settings such as hospital
difficile, VRE arm, overbed per sample* rooms.”
table, sink
counter
Boyce and United Before/after SC NR 72 rooms Ward not NR Bed rail, remote CFU* (RLU, adverse “The activated hydrogen peroxide wipe product
Havill, States specified control, toilet, effects) evaluated in our study proved to be an effective
2013 (26) tray table, surface disinfectant, as reflected by ACC and ATP
phone, bioluminescence assays. ATP bioluminescence
bedside panel, assays can be used as a tool to monitor the
chair arm, effectiveness of cleaning practices while using an

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blood pressure activated hydrogen peroxide disinfectant.
cuff, grab bar, Additional studies are warranted to determine
and faucet whether ATP and ACC cutoff points used to
handle classify surfaces as clean should vary depending
on the surface sampled.”
Friedman Australia Interrupted time SC 10 d 21 rooms Cancer ward VRE Floor, remote VRE-positive samples* “During use of a chlorine-based, 3-staged protocol,
et al, series 1026 samples control, toilet, (VRE colonization significantly higher residual levels of VRE
2013 (17) tray table, rates, rates per contamination were identified, compared with
phone, locker 1000 patient-days) levels detected during use of a benzalkonium
drawer handle, chloride based product for disinfection. This
bathroom tap reduction in VRE may be due to a new

Annals of Internal Medicine • Vol. 163 No. 8 • 20 October 2015

disinfection product, more attention to the
thoroughness of cleaning, or other
supplementary efforts in our institution.”
Gillespie Australia Before/after SC 3 mo 10 rooms General medical C. difficile, VRE Not specified RLU‡ “Our pilot study supports using ultramicrofiber cloth
et al, 200 samples ward, and steam technology as an alternative to
2013 (18) residential cleaning with chemicals.”
aged care ward
Hess et al, United Randomized, SC 10 mo 132 rooms ICU, surgical ward Various Bed rail, call Contamination rates “Intense enhanced daily cleaning of ICU rooms
2013 (25) States controlled 4444 samples pathogens, button, light for health care occupied by patients colonized with MRSA or
including MRSA switch, tray worker gowns and MDRAB was associated with a nonsignificant
table, bed gloves‡ reduction in contamination of HCW gowns and
control, desk, gloves after routine patient care activities. Further
IV poles and research is needed to determine whether intense
infusion environmental cleaning will lead to significant
pumps, phone, reductions and fewer infections.”
room sink,
supply cart,
and others
Levin et al, United Interrupted time AC 1y NR ICU, contact C. difficile Patient room, Hospital-associated “In 2010, the HA-CDI rate was 9.46 per 10,000
2013 (29) States series precaution and including CDI rate per 10 000 patient-days; in 2011, the HA-CDI rates was 4.45
other rooms bathroom patient days† per 10,000 patient-days (53% reduction, P =
(HA-CDI 0.01). The number of deaths and colectomies
attributable deaths attributable to hospital-associated C difficile
and colectomies) infection also declined dramatically.”
Mahida United Before/after AC NR 6 rooms Intensive therapy Various Not specified CFU* (disinfection “UV-C is an emerging decontamination technology
et al, Kingdom 32 locations unit, OR, and pathogens, times) that is effective in reducing bacterial
2013 (50) ward isolation including contamination in the clinical environment. There
room MRSA, VRE are significant advantages to using UV-C, and,
based on the results of this study we would
recommend using Tru-D at the higher reflected
dose setting of 22,000 mWs/cm2 for terminal
room disinfection in most healthcare settings.”
Manian United Before/after SC and 3y 870 rooms Ward not C. difficile Bed rail, call CDAD rate per 1000 “Implementation of an enhanced hospital-wide
et al, States AC 1123 rounds specified button, light patient-days† terminal cleaning program revolving around HPV
2013 (31) of cleaning switch, decontamination of targeted hospital rooms was
telephone, practical, safe, and associated with a significant
doorknob, sink reduction in the endemic rate of CDAD at our
hospital. Further studies are needed to delineate
better the role of HPV decontamination in
reducing the endemic rate of transmission of
other pathogens with significant environmental
presence in hospitals.”

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Appendix Table 8—Continued
Study, Country Study Design General Study Study Size Primary Setting Pathogen HTOs Primary Outcome Authors’ Conclusions
Year Cleaning Length (Secondary
(Reference) Method Outcomes)

Passaretti United Prospective SC and 30 mo 1039 rooms ICU Various Bed rail, Adjusted incidence “HPV decontamination reduced environmental
et al, States cohort AC 6607 patients pathogens, computer rate ratio† contamination and the risk of acquiring MDROs
2013 (42) including C. keyboard, (proportion of compared with standard cleaning protocols.”
difficile, MRSA, electronic contaminated
VRE monitoring rooms, MDRO
equipment concordance with
current room
occupant)

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Salgado United Randomized, SC and 11 mo 16 rooms (8 ICU C. difficile, MRSA, Bed rail, overbed Rate of colonization§ “Patients cared for in ICU rooms with copper alloy
et al, States controlled EC copper, 8 VRE table, bed (length of stay, surfaces had a significantly lower rate of incident
2013 (32) standard) footboard, IV mortality) HAI and/or colonization with MRSA or VRE than
614 patients poles, and did patients treated in standard rooms.
(294 cared arms of the Additional studies are needed to determine the
for in visitor's chair clinical effect of copper alloy surfaces in
rooms with additional patient populations and settings.”
copper)
Schmidt United Nonrandomized, AC and 3 mo 75 beds ICU Various pathogens Bed rail Bacterial burden* “Copper, when used to surface hospital bed rails,
et al, States controlled EC was found to consistently limit surface bacterial
2013 (33) burden before and after cleaning through its
continuous antimicrobial activity.”
Sigler and United Before/after SC NR 10 rooms Rooms occupied Various Bed rail, call PCR positive for “Overall, genetic markers for several staphylococci
Hensley, States by patients with pathogens, button, floor, staphylococci* known to colonize and infect humans remained
2013 (41) staphylococcal including MRSA tray table, sink, ubiquitous in each room following daily
infections TV button, disinfection practices.”
(usually MRSA) telephone
Sitzlar United Interrupted time SC and 21 mo NR General medical C. difficile Bed rail, call Percent of targets “An intervention that included education as
et al, States series AC ward, surgical button, toilet, cleaned* well as monitoring and feedback improved
2013 (19) ward tray table, (disinfection as thoroughness of cleaning but did not significantly
telephone measured by improve CDI room disinfection. The use of an
cultures) automated UV device improved disinfection, but
35% of rooms remained culture positive after use.
Disinfection was dramatically improved through
formation of a dedicated daily disinfection team
and implementation of a standardized process for
clearing CDI rooms.”
Goldenberg United Before/after SC 4 mo 13 wards General medical C. difficile Bed rail, call Number of “The prevalence of environmental contamination
et al, Kingdom ward, surgical button, floor, contaminated sites* was unaffected with a rate of 8% (9/120) before
2012 (14) ward, plastic remote control, (CDI rate) and 8% (17/212) following the change. Rates of
surgery, toilet, patient infection were also unchanged during
orthopedics, telephone, these periods.”
elderly care, locker, chair,
acute sluice room,
admissions side room,
mop bucket,
and others
Grabsch Australia Interrupted time SC 24 mo NR ICU, cancer ward, VRE Call button, VRE colonization§ “The Bleach-Clean programme was associated with
et al, series liver transplant, curtain, locker (newly recognized marked reductions in new VRE colonizations in
2012 (51) renal handle, chair, VRE colonization, high-risk patients, and VRE bacteraemia across
chart, supplies total burden of the entire hospital. These findings have important
trolley, phone inpatient VRE implications for VRE control in endemic health
colonization) care settings.”
Havill et al, United Nonrandomized, AC NR 15 rooms Ward not Various Bed rail, remote ACC* “Both HPV and UVC reduce bacterial contamination,
2012 (52) States controlled specified pathogens, control, toilet, including spores, in patient rooms, but HPV is
including C. tray table significantly more effective. UVC is significantly
difficile less effective for sites that are out of direct line of
sight.”

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Annals of Internal Medicine • Vol. 163 No. 8 • 20 October 2015

 Appendix Table 8—Continued
Study, Country Study Design General Study Study Size Primary Setting Pathogen HTOs Primary Outcome Authors’ Conclusions
Year Cleaning Length (Secondary
(Reference) Method Outcomes)

Karpanen United Crossover EC 24 wk 19 rooms General medical C. difficile, MRSA, 14 HTOs, CFU* “Copper alloys (greater than or equal to 58%
et al, Kingdom ward VRE including toilet copper), when incorporated into various hospital
2012 (37) seat, grab rail, furnishings and fittings, reduce the surface
and door microorganisms. The use of copper in
handle combination with optimal infection-prevention
strategies may therefore further reduce the risk
that patients will acquire infection in healthcare
environments.”
Kundrapu United Randomized, SC NR 70 patients Ward not C. difficile, MRSA Bed rail, call CFU* (frequency of “In a randomized nonblinded trial, we demonstrated
et al, States controlled specified button, side health care that daily disinfection of high-touch surfaces in

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2012 (43) table, toilet, worker hand rooms of patients with Clostridium difficile
telephone, contamination) infection and methicillin-resistant Staphylococcus
chair, aureus colonization reduced acquisition of the
wall-mounted pathogens on hands after contacting high-touch
vital signs surfaces and reduced contamination of hands of
equipment, IV healthcare workers caring for the patients.”
medication
stand, door
knobs and
handles
Schmidt United Randomized, SC and 3 mo NR Ward not Various Bed rail CFU* (overall “There was no difference in effectiveness, with a

Annals of Internal Medicine • Vol. 163 No. 8 • 20 October 2015

et al, States controlled AC specified pathogens, microbial burden) mean relative reduction of microbial burden of
2012 (23) including 84% for the traditional method versus 88% for the
MRSA, VRE PureMist method.”
Schmidt United Before/after SC and 43 mo 1587 rooms ICU C. difficile, MRSA, Bed rail, call CFU* “The introduction of copper surfaces to objects
et al, States EC 9522 objects VRE button, tray formerly covered with plastic, wood, stainless
2012 (12) table, IV stand, steel, and other materials found in the patient
visitor chair, care environment significantly reduced the
computer overall MB on a continuous basis, thereby
mouse, data providing a potentially safer environment for
input device hospital patients, health care workers (HCWs),
and visitors.”
Boyce et al, United Before/after AC NR 25 rooms Ward not C. difficile Bed rail, toilet, Mean ACC (CFU per “The mobile UV-C light unit significantly reduced
2011 (105) States specified tray table, plate)* (proportion aerobic colony counts and C. difficile spores on
television of surfaces yielding contaminated surfaces in patient rooms.”
remote a positive culture
result [>1 CFU];
number of surfaces
yielding >2.5
CFUs/cm2 for the
ACC)
Carter and United Before/after SC 18 mo NR NR C. difficile Light switch, CDI rate per 1000 “The introduction of sporicidal wipes resulted in a
Barry, Kingdom toilet, furniture, patients, overall significant reduction in C. difficile rates. This
2011 (15) bed frame, IV rate of CDI† supports the need to review and enhance
pump traditional environmental cleaning regimens for
preventing and controlling C difficile in acute
settings.”
Chan et al, Australia Nonrandomized, SC and NR NR Ward not VRE Call button, side, CFU* “These results showed that dry hydrogen peroxide
2011 (45) controlled AC specified toilet, arm rest, vapour room decontamination is highly effective
cotside on a range of surfaces, although the cleanliness
data obtained by these methods cannot be easily
compared among the different surfaces as
recovery of organisms is affected by the nature of
the surface.”
Orenstein United Before/after SC 2y NR General medical C. difficile Not specified C. difficile incidence “We found that daily room cleaning with 0.55%
et al, States ward rates† germicidal bleach wipes led to a sustained
2011 (27) reduction in hospital-acquired CDI on units with
high endemic incidence of CDI. Targeting the use
of daily bleach wipe cleaning to units with an
increased C. difficile colonization pressure is an
effective method to wipe out healthcare-acquired
CDI.”

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 Appendix Table 8—Continued
Study, Country Study Design General Study Study Size Primary Setting Pathogen HTOs Primary Outcome Authors’ Conclusions
Year Cleaning Length (Secondary
(Reference) Method Outcomes)

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Sexton United Before/after Steam 2d 8 rooms Long-term care Various Bed rail, side CFU* (log10 “The steam vapor system reduced bacterial levels by
et al, States vapor wing pathogens, table, guest reduction) >90% and reduced pathogen levels on most
2011 (44) including C. chair arm, sink, surfaces to below the detection limit. The steam
difficile, MRSA door push vapor system provides a means to reduce levels
panel of microorganisms on hospital surfaces without
the drawbacks associated with chemicals, and
may decrease the risk of cross-contamination.”
Wilson United Randomized SC and 1y 20 736 ICU Various Bed rail, drawer Number of bed areas “Enhanced cleaning reduced environmental
et al, Kingdom crossover “enhanced samples pathogens, handle, chart, from which target contamination and hand carriage, but no
2011 (47) cleaning” 1152 including C. keyboard, pathogens were significant effect was observed on patient
bed-days difficile, MRSA, syringe driver, isolated at least acquisition of methicillin-resistant Staphylococcus
VRE nurse's hand, once during a aureus.”
monitor sampling day‡
(unpooled results

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of screening for the
target pathogens in
bed/communal
areas, total ACC)
Alfa et al, Canada Before/after SC 19 mo 243 patients Ward not C. difficile Toilet CFU* “Our data indicate that the AHP formulation
2010 (48) 714 samples specified evaluated that has some sporicidal activity was
significantly better than the currently used SHP
formulation. This AHP formulation provides a
one-step process that significantly lowers the C.
difficile spore level in toilets during non-outbreak
conditions without the workplace safety concerns
associated with 5,000 ppm bleach.”
Casey et al, United Nonrandomized, EC 10 wk NR General medical Various Toilet, sink, door Median CFU/cm2* “The results of this trial clearly demonstrate that
2010 (35) Kingdom controlled ward, common pathogens, push plate copper-containing items offer the potential to
area including C. significantly reduce the numbers of
difficile, MRSA, micro-organisms in the clinical environment.
VRE However, the use of antimicrobial surfaces should
not act as a replacement for cleaning in clinical
areas, but as an adjunct in the fight against HCAI.”
Hacek et al, United Before/after SC 3y All rooms Ward not C. difficile Bed, bed rail, bed C. difficile cases per “The implementation of a thorough, all-surface
2010 (20) States occupied specified control, floor, 1000 patient-days† terminal bleach cleaning program in the rooms of
by patients side table, patients with CDI has made a sustained,
with C. toilet, tray significant impact on reducing the rate of
difficile in 3 table, nosocomial CDI in our health care system.”
hospitals; doorknob, sink,
number not wall
specified
Hamilton et United Nonrandomized, SC 7 wk NR Ward not NR Bed, floor, tray Total viable bacterial “Cleaning with UMF reduces TVC in the hospital
al, Kingdom controlled specified table counts* environment and this effect is significantly
2010 (34) enhanced (about two-fold) with additional
CuWB50. The copper-based biocide has two
beneficial effects: (i) a residual effect that requires
2-3 weeks of cleaning to establish, and (ii) an
immediate effect on reducing TVC that is most
evident shortly after cleaning.”
Hedin et al, Sweden Nonrandomized, EC 3 wk 12 rooms Infectious disease Various Side table Total ACC* “Significantly fewer bacteria were found on
2010 (36) controlled 36 samples ward pathogens, Appeartex-treated surfaces compared with
including MRSA untreated surfaces.”
Nerandzic United Before/after AC NR 66 rooms Ward not C. difficile, MRSA, Call light, Positive cultures* “The Tru-D Rapid Room Disinfection device is a
et al, States 261 sites specified VRE bedside table, (ease of use) novel, automated, and efficient environmental
2010 (56) telephone, and disinfection technology that significantly reduces
bed rail C. difficile, VRE and MRSA contamination on
commonly touched hospital surfaces.”
Rutala et al, United Before/after AC 8 mo 8 rooms Ward not C. difficile, MRSA Bed rail, floor Total CFUs per site* “This UV-C device was effective in eliminating
2010 (53) States specified vegetative bacteria on contaminated surfaces
both in the line of sight and behind objects within
approximately 15 minutes and in eliminating C.
difficile spores within 50 minutes.”
Andersen Norway Nonrandomized, SC NR 4 rooms Geriatric ward Various Floor CFU* (CFU in air, ease “Wet, moist and dry mopping seemed to be more
et al, controlled 192 samples pathogens, of use of ATP) effective in reducing bacteria on the floor, than
2009 (49) including C. the spray mopping (P = 0.007, P = 0.002 and P =
difficile, MRSA, 0.011, respectively). The burden of bacteria in air
VRE increased for all methods just after mopping. The
overall best cleaning methods seemed to be
moist and wet mopping.”

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Annals of Internal Medicine • Vol. 163 No. 8 • 20 October 2015

 Appendix Table 8—Continued
Study, Country Study Design General Study Study Size Primary Setting Pathogen HTOs Primary Outcome Authors’ Conclusions
Year Cleaning Length (Secondary
(Reference) Method Outcomes)

McMullen United Nonrandomized, SC 2.5 y Entire medical ICU, common C. difficile Not specified Cases of CDAD per “These findings are further evidence that use of
et al, States controlled and area 1000 patient-days† sodium hypochlorite solution may be an effective
2007 (21) surgical means of reducing the occurrence of CDAD in
ICUs acute care facilities where the disease is epidemic
included or hyperendemic.”

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for 2.5 y
Whitaker United Before/after SC 2y NR Ward not C. difficile “Every lateral CDI rate per 1000 “A combination of automated daily isolation reports,
et al, States specified surface” patient-days† use of a standardized methodology for isolation
2007 (16) rounds, as well as development of a 10%
hypochlorite disinfection protocol resulted in a
dramatic decrease in health care-associated C.
difficile cases.”
“Weekly nursing director reports and daily rounds
by nursing leadership keep the direct line
supervisors abreast of infection control issues on
their respective nursing units. The addition of the

Annals of Internal Medicine • Vol. 163 No. 8 • 20 October 2015

dual-chamber bleach container ensured that the
proper dilution was achieved when disinfecting
reusable equipment.”
De Lorenzi Italy Nonrandomized, Mopping 5d 2 rooms Surgical ward NR Floor ACC* “Dry wiping followed by damp washing did not
et al, controlled methods produce any significant reduction in the average
2006 (22) bacterial load. However, damp washing followed
by dry wiping reduced the bacterial load for both
types of flooring. The difference was statistically
significant.”
Wilcox United Nonrandomized, SC 2y 1128 samples 2 “elderly C. difficile Bed rail, floor, Incidence rate of “Our results provide some evidence that
et al, Kingdom controlled medicine toilet CDI† (surface hypochlorite environmental cleaning may
2003 (54) wards” colonization) significantly reduce CDI incidence, but also
emphasize the potential for confounding factors.”
Byers et al, United Before/after SC NR 10 conven- Ward not VRE Bed rail, floor, Number of colonized “Sixteen percent of hospital room surfaces remained
1998 (38) States tional specified side table, IV sites§ (cost of labor colonized by VRE after routine terminal
rooms, 4 pole, phone, and supplies, cost disinfection. Disinfection with a new “bucket
bucket blood pressure of keeping room method” resulted in uniformly negative cultures.
method; cuff, wall panel empty) Conventional cleaning took an average of 2.8
376 conven- control disinfections to eradicate VRE from a hospital
tional room, while only one cleaning was required with
samples, the bucket method.”
135 bucket
samples

AC = automated cleaning; ACC = aerobic colony counts; AHP = accelerated hydrogen peroxide; ATP = adenosine triphosphate; CD = cleaning and disinfection; CDAD = Clostridium difficile–
associated diarrhea; CDI = C. difficile infection; CFU = colony-forming unit; EC = enhanced coating; HA-CDI = hospital-associated C. difficile infection; HAI = hospital-associated infection;
HCAI = health care–associated infection; HCW = health care worker; HP = hydrogen peroxide; HPC = heterotrophic plate counts; HPD = hydrogen peroxide decontamination; HPV = hydrogen
peroxide vapor; HTO = high-touch object; ICU = intensive care unit; IV = intravenous; MB = microbial burden; MDRAB = multidrug-resistant Acinetobacter baumannii; MDRO = multiple-drug–
resistant organisms; MRSA = methicillin-resistant Staphylococcus aureus; MSSA = methicillin-susceptible Staphylococcus aureus; NR = not reported; OR = operating room; PCR = polymerase chain
reaction; PPX-UV = pulsed xenon ultraviolet light; RLU = relative light unit; RTU = ready-to-use; SC = surface cleaning; SHP = stabilized hydrogen peroxide; TVC = total viable (bacterial) counts;
UMF = ultramicrofiber; UV = ultraviolet; UV-C = ultraviolet C; UVD = ultraviolet environmental disinfection; VRE = vancomycin-resistant enterococci.
* Primary outcome focused on surface contamination.
† Primary outcome focused on infection rate.
‡ Primary outcome focused on outcomes other than surface contamination, colonization, and infection rate.
§ Primary outcome focused on colonization.

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 Appendix Table 9. Characteristics of Monitoring Studies
Study, Year Country Study Design Monitoring Method Study Sample Size Primary Setting Pathogens HTO(s) Primary Outcome Authors’ Conclusions

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(Reference) Length (Secondary Outcomes)

Luick et al, United Nonrandomized, ATP bioluminescence, 2 mo 50 rooms, 250 Ward not specified NR Bed rail, call button, Sensitivity to detect “In a simultaneous assessment of
2013 (70) States controlled fluorescent/UV total surfaces toilet, tray table, pathogens (specificity of 250 environmental surfaces
markers, visual telephone tests, PPV, NPV) after terminal cleaning using
observation aerobic cultures as a gold
standard, both fluorescent
marker and an adenosine
triphosphate bioluminescence
assay system demonstrated
better diagnosticity compared
with subjective visual
inspection.”
Smith et al, United Nonrandomized, ATP bioluminescence, NR 10 rooms Ward not specified Various Bed rail, call button, RLU/cm2; CFU/cm2 “Although quantitative

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2013 (71) States controlled visual observation, pathogens, light switch, side microbiology and ATP
swab cultures including table, toilet, sink, detection measure somewhat
Clostridium telephone, door different aspects of
difficile, MRSA, handle environmental contamination,
VRE they both generally agree in
distinguishing clean from dirty
surfaces.”
Snyder et al, United Nonrandomized, ATP bioluminescence, 3 mo 20 rooms, 290 Ward not specified NR Bed rail, call button, Percentage of targets cleaned “In assessing the effectiveness of
2013 (62) States controlled fluorescent/UV surfaces light switch, side (test characteristics of UV, PDC, there was poor
markers, visual table, toilet, tray table, ATP, and visual inspection) correlation between the two
observation door knob, most frequently studied
telephone, sink commercial methods and a
microbiologic comparator.
Visual inspection performed
at least as well as commercial
methods, directly addresses
patient perception of
cleanliness, and is economical
to implement.”
Mulvey et al, United Nonrandomized, ATP bioluminescence, 4 wk 90 samples General medical MRSA Bed, bed rail, floor, tray Cleaning rate (surface “Microbiological and ATP
2011 (63) Kingdom controlled visual observation, and surgical table contamination [measured monitoring confirmed
agar slide cultures wards by ATP and dipslides]) environmental contamination,
persistence of hospital
pathogens and measured the
effect on the environment
from current cleaning
practices. This study has
provided provisional
benchmarks to assist with
future assessment of hospital
cleanliness. Further work is
required to refine practical
sampling strategy and choice
of benchmarks.”
Munoz-Price United ITS Fluorescent/UV 20 wk 284 rooms, ICU Various pathogens Bed rail, bed control, Cleaning rate “We found that regular
et al, States markers 2292 surfaces call button, light surveillance using an
2011 (64) switch, monitor inexpensive technology
control panel, remote coupled with regular
control, side table, feedback of results produced
toilet, tray table sustained improvements in
environmental cleaning, which
may explain the coincident
reduction in hospital-acquired
infections. The ability of this
brief (12 weeks) intervention
to produce rapid benefits
(within 4 weeks) and
prolonged benefits (more
than 20 weeks) speaks to its
efficacy. Further studies aimed
at optimizing reintroduction of
the intervention to optimize
cleaning rates should be
considered.”

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Annals of Internal Medicine • Vol. 163 No. 8 • 20 October 2015

 Appendix Table 9—Continued
Study, Year Country Study Design Monitoring Method Study Sample Size Primary Setting Pathogens HTO(s) Primary Outcome Authors’ Conclusions
(Reference) Length (Secondary Outcomes)

Carling et al, United Before/after Fluorescent/UV NR 260 rooms, ICU NR NR Percentage of targets cleaned “Significant improvements in
2010 (65) States markers 3532 intensive care unit room
samples, 27 cleaning can be achieved in
hospitals most hospitals by using a
structured approach that
incorporates a simple, highly
objective surface targeting
method and repeated

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performance feedback to
environmental services
personnel.”
Alfa et al, Not Descriptive Fluorescent/UV 8 mo 20 patients, 201 Ward not specified C. difficile Toilet Cleaning rate “Our data demonstrated the
2008 (68) specified markers samples value of UVM for monitoring
the compliance of
housekeeping staff with the
facility's toilet cleaning
protocol. In addition to
providing good physical
cleaning action, agents with

Annals of Internal Medicine • Vol. 163 No. 8 • 20 October 2015

some sporicidal activity
against C. difficile may be
needed to effectively reduce
the environmental reservoir.”
Alhamad and United Before/after and Agar slide cultures, 4 wk 130 samples ICU and “high MRSA Bed rail, monitor control Number of samples with “There was no direct correlation
Maxwell, Kingdom correlation of “wipe-rinse dependency panel, cabinet, door positive culture (overall between the findings of total
2008 (72) 2 monitoring method,” used an unit” handle, telephone, CFU/cm2) aerobic count and MRSA
methods assay keyboard isolation. We suggest,
however, that combining both
standards will give a more
effective method of assessing
the efficacy of cleaning/
disinfection strategy. Further
work is required to evaluate
and refine these standards in
order to assess the frequency
of cleaning required for a
particular area, or for
changing the protocol or
materials used.”
Blue et al, Canada Before/after Fluorescent/UV 4 mo 364 samples Ward not specified VRE Bed rail, call buttons Percentage of targets cleaned “The GlitterBug product is an
2008 (66) markers light switch, toilet, tray (VRE infection rate) effective tool to evaluate
table, doorknob environmental cleaning and
adherence to policies and
procedures and this method
was superior to previous
visual inspection methods.
The use of GlitterBug potion
improved physical cleaning
and enhanced staff
contribution. The Brevis
GlitterBug product was
incorporated into the CSS
environmental cleaning
program at Hamilton Health
Sciences as a quality indicator
to monitor environmental
cleaning practices.”

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Appendix Table 9—Continued
Study, Year Country Study Design Monitoring Method Study Sample Size Primary Setting Pathogens HTO(s) Primary Outcome Authors’ Conclusions
(Reference) Length (Secondary Outcomes)

Carling et al, United Descriptive study Fluorescent/UV 12 wk 1119 rooms, ICU and other units NR Bed rail, call button, Cleaning rate “We identified significant
2008 (69) States of UV markers 13 369 “high light switch, side opportunities in all
fluorescent risk-objects” table, toilet, tray table, participating hospitals to
monitoring sink, telephone, improve the cleaning of
doorknob frequently touched objects in

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the patient's immediate
environment. The information
obtained from such
assessments can be used to
develop focused
administrative and
educational interventions that
incorporate ongoing
feedback to the
environmental services staff,
to improve cleaning and
disinfection practices in
healthcare institutions.”
Carling et al, United Descriptive study Fluorescent/UV NR 157 rooms, Ward not specified NR Bed rail, call button, side Percentage of targets cleaned “The use of a novel target
2006 (67) States of fluorescent markers 1404 samples table, toilet, tray table, compound to evaluate
marker sink, doorknob, housekeeping practices
monitoring telephone confirmed high rates of
cleaning of traditional sites
but poor cleaning of many
sites that have significant
potential for harboring and
transmitting microbial
pathogens. This methodology
has the potential for being
used to evaluate objectively
the cleaning/disinfecting
activities in various health care
settings.”
Malik et al, United Nonrandomized, ATP bioluminescence, NR 8 hospital wards Ward not specified NR Not specified RLU, CFU/cm2 “The data suggest that visual
2003 (73) Kingdom controlled visual observation, assessment is a poor indicator
agar slide cultures of cleaning efficacy and that
the ACE audit gives a better
assessment of cleaning
programs compared with the
other 2 audit methods in
relation to microbial surface
counts. It is recommended
that hospital cleaning regimes
be designed to ensure that
surfaces are cleaned
adequately and that efficacy is
assessed with use of internal
auditing and rapid hygiene
testing.”

ACE = audit for cleaning efficacy; ATP = adenosine triphosphate; CFU = colony-forming unit; CSS = infection control and customer support services; HTO = high-touch object; ICU = intensive care
unit; ITS = interrupted time series; MRSA = methicillin-resistant Staphylococcus aureus; NPV = negative predictive value; NR = not reported; PDC = postdischarge cleaning; PPV = positive
predictive value; RLU = relative light unit; UV = ultraviolet; UVM = ultraviolet visible marker; VRE = vancomycin-resistant enterococci.

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 Appendix Table 10. Characteristics of Implementation Studies
Study, Year, Study Single or Sample Size Primary Setting Pathogen(s) HTO(s) Implementation Tools Primary Outcome Authors’ Conclusions
Country Design; Multicomponent Described (Secondary
(Reference) Length Strategy Outcomes)

Branch-Elliman Before/after; Single 820 surfaces, 210 Ward not MRSA, VRE Side rail, overbed rail, Education, monitoring, Proportion of “We successfully implemented a quality
et al, 2014, 2 mo rooms specified toilet seat feedback surfaces cleaned improvement and education project
United (NR) to improve environmental cleaning in
States (74) our hospital. Our study demonstrates
that quality-assessment tools, such as
the ATP luminometer, can be used at
the point of cleaning to improve
cleaning performance. Use of the tool
in a positive feedback loop directly
with front-line EVS staff resulted in
enhanced collaboration,
communication, and education

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among services.”
Koll et al, 2014, ITS; 22 mo Multicomponent infection 35 hospitals Burn, telemetry, Clostridium difficile >20 HTOs, including Cleaning checklists Adherence to “The use of a collaborative model to
United prevention bundle, and medical bed, bed rail, call room cleaning implement a multifaceted infection
States (75) including contact surgical unit button, floor, toilet, protocol (CDI prevention strategy was temporally
precautions for patients tray table, over 20 rates) associated with a significant
with diarrhea and sign HTOs reduction in hospital-onset CDI rates
placement for patients in participating New York
with confirmed/ metropolitan regional hospitals.”
suspected CDI
Ramphal et al, ITS; 14 mo Multicomponent/hand 3185 HTOs Ward not Various pathogens, 20 HTOs, including bed Education, training, Percentage of “The percentage of cleaned surfaces
2014, United hygiene, improved kits specified including rail, call button, “blinded monitoring targets cleaned improved incrementally between the

Annals of Internal Medicine • Vol. 163 No. 8 • 20 October 2015

States (76) for line-changing C. difficile remote control, and with transparent (C. difficile rates) three trials—with values of 20%, 49%,
procedures tray table reporting of the and 82%—showing that repeat
results in a positive, training favorably changed behavior
engaging manner” in the staff (P = 0.007). During the
study period, during which other
infection control interventions were
also introduced, there was a decline
from 0.27 to 0.21 per 1000 patient
days for Clostridium difficile infection,
0.43 to 0.21 per 1000 patient days for
ventilator-associated infections, 1.8%
to 1.2% for surgical site infections,
and 1.2 to 0.7 per 1000 central
venous line days for central
line–associated bloodstream
infections.”
Rupp et al, Before/after; Single 90 rooms, 1117 Medical/surgical NR Bed rail, tray table, 43-point room-cleaning Adherence to “Over a 4-year period, we observed that
2014, United 4y surface critical care room door handle, checklist, room cleaning monthly feedback of performance
States (77) measurements units thermometer, housekeeper protocol (NR) data in face-to-face meetings with
monitor, bed rail, educational program, frontline personnel was crucial in
release button, nurse training DVD, maintaining environmental-cleaning
call monitor, and face-to-face meetings effectiveness in adult critical care
other items with housekeeping units.”
Rupp et al, Observational; Single 292 rooms, 17 Surgical/medical NR 18 HTOs, including bed NR Housekeeper “A subgroup of housekeepers was
2014, United 4 mo housekeepers ICU rail, call button, light efficiency and identified who were significantly
States (78) switch, and toilet effectiveness more effective and efficient than their
based on RLUs coworkers. These optimum outliers
(NR) may be used in performance
improvement to optimize
environmental cleaning.”
Smith et al, Non-RCT; 20 Single 13 345 sites 5 units, including C. difficile, MRSA, 16 HTOs, including Educational Cleaning score “The ATP detection device combined
2014, United mo telemetry, ICU, VRE toilet seat, light interventional measures over with educational feedback for EVS
States (79) medical/ switch, call light, activities such as time (trends in workers resulted in significant
surgical, and mattress, and bedrail hands-on training and HAIs) improvement in cleaning efficacy of
cardiac education with ATP the hospital room environment.”
devices, education via
“Clean Sweep”
electronic game,
laminated pocket-size
cleaning order, and
high-touch surface
lists in both English
and Spanish

Continued on following page

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Appendix Table 10—Continued
Study, Year, Study Single or Sample Size Primary Setting Pathogen(s) HTO(s) Implementation Tools Primary Outcome Authors’ Conclusions
Country Design; Multicomponent Described (Secondary
(Reference) Length Strategy Outcomes)

Brakovich et al, ITS; 7 mo Multicomponent/a tiered 50 beds Long-term acute C. difficile Not specified Lipstick challenge, Incidence rate of “This program was successful in
2013, United approach that included care hospital checklists, training on CDI (cost) decreasing the incidence of CDI in
States (80) environmental cleaning use of chemicals, the LTACH creating a safe and
and disinfection, color-coded cost-effective environment for
diagnostics and microfiber cloths, patients, families, and the
surveillance, and database output of community.”

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infection control quarterly reports
measures, including
antibiotic stewardship
Trajtman et al, Non-RCT; Single 7680 sites General medical C. difficile Bathroom Feedback and UVM Adherence to “The use of UVM as an audit tool
2013, United 24 wk ward audit tool room cleaning combined with weekly feedback of
States (81) protocol (NR) results to housekeeping staff resulted
in significant, sustained improvement
in the overall level of cleaning
compliance of housekeeping staff.”
Ragan et al, Before/after; Single 823 HTOs ICU C. difficile, MRSA, Light switch, toilet, tray Audit and feedback, Percentage of “We demonstrate that auditing with
2012, 8 wk VRE table, IV pole, drawer check list for HTOs targets cleaned fluorescent targeting can be
Canada (82) handle, door knob (NR) implemented in both the ward and
and other items intensive care unit settings using only
modest resources, resulting in rapid
improvements in cleaning
thoroughness.”
Datta et al, Retrospective Single 17 652 patients ICU MRSA, VRE Not specified Education Infection rate: “Enhanced intensive care unit cleaning
2011, United cohort; 19 MRSA and VRE using the intervention methods may
States (83) mo (acquisition by reduce MRSA and VRE transmission.
prior occupant It may also eliminate the risk for
status) MRSA acquisition due to an
MRSA-positive prior room occupant.”
Murphy et al, Before/after; Single 37 rooms, 986 Ward not MRSA, VRE Light switch, toilet, Audit and feedback, Adherence to “The [fluorescent marker] was useful to
2011, 17 wk HTOs specified bedroom door education to EVS room cleaning assess HTO cleaning thoroughness. It
Australia (84) handle, bedroom staff, survey of EVS protocol facilitated relevant feedback and
soap dispenser, staff (percentage of education and motivated staff to
bedroom tap handle, targets cleaned) strive for continual improvements in
paper towel environmental cleaning. Without
dispenser on-going education, preliminary
improvements were unsustained.
However, investigators better
understood flaws in cleaning and
policy/procedure conflicts.”
Hota et al, 2009, Before/after; Single 2901 sites for ICU VRE Bed rail, tray table, Education, intensified Percentage of “These findings suggest that surface
United 25 wk thoroughness infusion pump; monitoring targets cleaned contamination with VRE is due to a
States (85) of cleaning, countertop; soap (contamination failure to clean rather than to a faulty
1472 sites for dispenser, and other of sites cleaning procedure or product.”
contamination items postcleaning,
VRE prevalence)
Po et al, 2009, ITS; 9 mo Single 16 beds ICU C. difficile, VRE Computer keyboard on Education and Cleaning rate (NR) “Following a series of educational and
United wheels feedback, process programmatic interventions, we were
States (86) improvement able to improve the thoroughness of
interventions (e.g., cleaning to 100%.”
assigned 1 specific
individual to clean
COWS), modification
to cleaning protocols

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 Appendix Table 10—Continued
Study, Year, Study Single or Sample Size Primary Setting Pathogen(s) HTO(s) Implementation Tools Primary Outcome Authors’ Conclusions
Country, Design; Multicomponent Described (Secondary
(Reference) Length Strategy Outcomes)

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Carling et al, Before/after; Single 20 646 HTOs General medical C. difficile, MRSA, 14 HTOs, including bed Audit and feedback Percentage of “Significant improvements in
2008, United NR ward, special VRE rail, toilet, and tray targets cleaned disinfection cleaning can be achieved
States (87) care areas table (NR) in most hospitals, without a
substantial added fiscal commitment,
by the use of a structured approach
that incorporates a simple, highly
objective surface targeting method,
repeated performance feedback to
environmental services personnel,
and administrative interventions.
However, administrative leadership

Annals of Internal Medicine • Vol. 163 No. 8 • 20 October 2015

and institutional flexibility are
necessary to achieve success, and
sustainability requires an ongoing
programmatic commitment from
each institution.”
Goodman et al, Before/after; Single 85 rooms, 1121 Respiratory MRSA, VRE 15 HTOs, including bed Education, monitoring, Positive cultures “Increasing the volume of disinfectant
2008, United 8 mo surfaces step-down unit rail, curtain, light and feedback (number of applied to environmental surfaces,
States (88) switch, and toilet rooms with providing education for
positive culture) Environmental Services staff, and
instituting feedback with a black-light
marker improved cleaning and
reduced the frequency of MRSA and
VRE contamination.”
Eckstein et al, Before/after; Single 17 rooms Surgical ward C. difficile, VRE Bed rail, call button, Audit and feedback, Percentage of “Our findings provide additional
2007, United 16 wk side table, toilet, and education, positive cultures evidence that simple educational
States (89) door knob housekeeping staff (NR) interventions directed at
asked for input on housekeeping staff can result in
additional resources improved decontamination of
needed to perform environmental surfaces. Such
job well interventions should include efforts to
monitor cleaning and disinfection
practices and provide feedback to
the housekeeping staff.”
Hayden et al, Before/after; NR 485 cleaning ICU VRE Bed rail, infusion pump, Educational in services, Colonization with “Decreasing environmental
2006, United 255 d episodes countertop, door increased monitoring, VRE (time to contamination may help to control
States (90) handle, telephone, audit, and feedback clean, antibiotic the spread of some antibiotic
and other items use) resistant bacteria in hospitals.”

ATP = adenosine triphosphate; CDI = Clostridium difficile infection; COWS = computer-on-wheels; EVS = environmental services; HAIs = health care–associated infections; HTO = high-touch
object; ICU = intensive care unit; ITS = interrupted time series; IV = intravenous; LTACH = long-term acute care hospital; MRSA = methicillin-resistant Staphylococcus. aureus; NR = not reported;
RCT = randomized, controlled trial; RLU = relative light unit; UVM = ultraviolet marker; VRE = vancomycin-resistant enterococci.

www.annals.org
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