NCBI Bookshelf. A service of the National Library of Medicine, National Institutes of Health.
Leas BF, Sullivan N, Han JH, et al. Environmental Cleaning for the Prevention of Healthcare-Associated Infections [Internet]. Rockville (MD): Agency for Healthcare Research and Quality (US); 2015 Aug. (Technical Briefs, No. 22.)
Environmental Cleaning for the Prevention of Healthcare-Associated Infections [Internet].
Show detailsOur search of the published literature identified 4,087 potentially relevant studies. We excluded 3,868 studies during title and abstract screening. These studies were not relevant to the Guiding Questions or did not meet our criteria for publication type. This resulted in full-text screening of 219 articles. We excluded 131 studies at the full-text level. See Appendix B for a list of studies organized by reason for exclusion.
Of the 88 remaining documents, 2 were used for background information and 6 were identified as clinical practice guidelines. Information on 63 other clinical practice guidelines (many provided in the Topic Triage documentation) or guidance documents (e.g., tool kits) identified in the gray literature are summarized in Appendix D. Figure 1 presents a PRISMA flow diagram of our study screening.

Figure 1
PRISMA flow diagram of study screening.
Our searches identified 4 systematic reviews and 76 published studies that fit our inclusion criteria and addressed modalities for cleaning, disinfecting, assessing cleanliness, or implementing EC processes. We did not identify for inclusion any conference abstracts presented within the past 2 years. A search of ClinicalTrials.gov identified three clinical trials categorized as “currently recruiting,” “ongoing, but not recruiting,” and “not yet open for participant recruitment,” respectively. We also identified one trial (NCT00566306) completed in August 2008. No outcome data were reported, and no publications are available from this trial. For more information on the ongoing trials, see Table D-2 in Appendix D.
Overview of Cleaning and Disinfection Modalities (Guiding Question 1)
Three distinct modalities exist for routine disinfection of hard surfaces in patient rooms: chemical disinfectants, self-disinfecting surfaces, and no-touch technologies.
Chemical Disinfectants
Five categories of chemical agents are currently used in hospitals. These disinfectants are usually applied with a spray, wipes soaked in a disinfectant-filled bucket, textile or microfiber cloth, or premoistened wipe; some formulations can also be used as a liquid for mopping floors. Selecting a chemical agent for routine disinfection of the patient room environment can be a complex process that includes careful consideration of its advantages and drawbacks.
For an effective disinfection protocol, consideration should be given to the microorganisms being targeted, type of surface, the characteristics of a specific disinfectant (e.g., compatibility on various surfaces/materials), cost and ease of use, and safety of EVS personnel. Thus, selecting specific disinfectants commonly involves input of multiple stakeholders (e.g., infection control committees, EVS personnel) and can often be institution-dependent.
Importantly, the effectiveness of all disinfectants, regardless of category, is significantly affected by how it is used in the real-world hospital environment (e.g., sufficient contact time, temperature, concentration).23 For example, manufacturer-recommended dwell times are established in the laboratory setting, but in the hospital environment, where there is often pressure to turn rooms around quickly, allowing for appropriate dwell times can be challenging. Lastly, as opposed to newer disinfection technologies such as hydrogen peroxide vapor, use of these chemical disinfectants are not recommended in preparations for spraying or fogging application.
Quaternary Ammonium
QACs are widely used EPA-registered health care disinfectants and are generally regarded as effective, surface-compatible agents with some persistent antimicrobial activity when left undisturbed on surfaces. These compounds frequently are used for routine cleaning and disinfection of noncritical environmental surfaces (e.g., floors, HTOs such as bed rails and tray tables, medical equipment that contacts intact skin [such as blood pressure cuffs]). These agents are bactericidal, virucidal against enveloped viruses (e.g., HIV), and fungicidal.
However, they are not sporicidal and generally not mycobactericidal or virucidal against nonenveloped viruses. High water hardness and materials such as cotton towels and cloths can diminish microbicidal activity.24-26 Finally, case reports of occupational asthma have been documented due to use of benzalkonium chloride.27,28
Hypochlorite
Hypochlorites are EPA-registered surface disinfectants and the most commonly used of the chlorine disinfectants. For example, commercially available concentrations of 4% to 6% sodium hypochlorite solutions are formulated as concentrated household bleach, which are typically diluted by a factor of 10 for a final-use concentration of 0.4% to 0.6%. Hypochlorites are bactericidal, fungicidal, virucidal, mycobactericidal, and sporicidal. They are commonly used for disinfecting surfaces in bathrooms and surfaces used in food preparation and are generally included in recommendations for disinfecting surfaces or objects contaminated with hepatitis viruses, HIV, and C. difficile. Hypochlorites are also used to disinfect blood spills in the hospital setting. Depending on the surface being cleaned and the pathogens targeted, instructions for specific formulations, concentrations, and contact times must be followed. Hypochlorites must be freshly prepared when diluting from higher concentrations and proper dilution protocols must be followed to reduce chemical irritation or decreased efficacy. Hypochlorites are unaffected by water hardness, relatively stable and fast-acting, and generally safe with a low incidence of serious toxicity.29,30
However, sodium hypochlorite (i.e., household bleach) may cause skin and eye irritation, as well as oropharyngeal, esophageal, and gastric burns.31-33 Hypochlorites also are corrosive to metals in high concentrations (>500 ppm) and can discolor fabrics. Finally, given that their activity is significantly reduced by organic matter (e.g., blood, fecal matter), surfaces must be precleaned before disinfection.29,30
Accelerated Hydrogen Peroxide
Accelerated hydrogen peroxide products are recently introduced EPA-registered surface disinfectants; they are bactericidal, virucidal, fungicidal, sporicidal, and mycobactericidal. These products have a generally short contact time, with some products having a 30-second to 1-minute bactericidal and virucidal claim, and a 5-minute mycobactericidal claim.34 Lower-level concentrations are used for disinfecting hard surfaces, while higher-level concentrations (2%) are used for high-level disinfection. These compounds are commonly used, considered safe for EVS staff (i.e., lowest EPA toxicity category IV), surface compatible, noncorrosive, and unaffected by organic material.34 In addition, accelerated hydrogen peroxide products are generally considered benign for the environment. However, they are more expensive than other disinfectants such as quaternary ammonium.
Phenolics
Phenolics are EPA-registered and bactericidal, mycobactericidal, fungicidal, and virucidal and are used for surface disinfection (e.g., bedrails, tables) and for disinfecting noncritical medical devices.35 While inexpensive, they are less commonly used because of several disadvantages, including absorption by porous materials, ability for residual product to irritate tissue, and depigmentation of skin. In addition, phenolics are not sporicidal and can cause hyperbilirubinemia in infants when they are not prepared per manufacturers' recommendations.36,37
Peracetic Acid
Peracetic acid preparations are EPA-registered disinfectants with rapid activity against microorganisms and are bactericidal, fungicidal, virucidal, mycobactericidal, and sporicidal. Peracetic acid generally remains active in the presence of organic material and lacks harmful decomposition materials (e.g., oxygen, hydrogen peroxide). Disadvantages include lack of stability, particularly following dilution, and potential to corrode metals such as copper and brass. Peracetic acid is 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.
Self-Disinfecting Surfaces
Coating surfaces with heavy metals may protect against bacterial contamination and render items “self-disinfecting.” Copper and silver have been investigated for self-disinfecting properties in hospital settings. Many surfaces can be coated with copper or silver, including bed rails, trays, call buttons, IV poles, and other objects.
Copper
High levels of copper ions are toxic to most microorganisms due to generation of reactive oxygen species, resulting in damage of nucleic acids, proteins, and lipids and, ultimately, cell death. In the health care setting, copper has been used to control Legionella spp. in water supplies and, more recently, incorporated into self-disinfecting surfaces used in hospital rooms. Given its bactericidal properties, contact with copper has been examined as a mechanism to kill many clinically important pathogens, including MRSA, Escherichia coli, Enterococcus spp., and Mycobacterium tuberculosis.
However, no standardization exists as to type of alloy and selection of specific surfaces. The effectiveness of copper-containing surfaces in reducing the risk of HAIs is under active investigation, and real-world experience remains limited to date. A study performed in three hospitals demonstrated a significant reduction in the microbial burden of certain intensive care unit (ICU) surfaces following installation of copper-impregnated surfaces.38 Furthermore, a recent randomized controlled trial (RCT) evaluating the use of copper alloy-coated surfaces for several HTOs (e.g., bed rails, tray tables) in the ICU demonstrated decreased rates of HAIs and MRSA and VRE colonization.39
Silver
Silver ions have the greatest level of antimicrobial activity of all the heavy metals. While its mechanism of action has not been completely elucidated, its bactericidal properties likely involve binding of disulfide and sulfhydryl groups present in the proteins of microbial cell walls. The use of silver-impregnated environmental surfaces has recently been studied and shown to reduce experimental surface contamination, but the clinical impact of this modality has not been evaluated.39,40
Altered Topography
Materials with altered surface topography to inhibit bacterial biofilm formation are currently under investigation. An example of this design is Sharklet AF (Sharklet Technologies, Alachua, FL), which uses topography similar to shark skin and has been shown to reduce biofilm formation and growth of S. aureus on molds utilizing Sharklet technology.41 However, 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 Coatings
Light-activated antimicrobial coatings have been recently studied for self-disinfection of surfaces. 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. These surfaces may provide a less toxic approach than the use of chemical disinfectants and are broadly microbicidal.42-44 However, a constant source of photoactivation is required, and it is unclear whether these surfaces are sporicidal. Studies are still required on long-term disinfecting properties of these surfaces in the real-world hospital environment.
No-Touch Modalities
Two kinds of devices have been developed and commercially produced to disinfect hospital rooms. One type of device emits UV light, and another produces a mist or vapor of hydrogen peroxide. These devices are often referred to as no-touch or automated modalities because they disinfect via a stand-alone machine instead of manual application of chemical agents. Experts indicate that no-touch modalities should be used only as adjunctive infection control measures.
Ultraviolet Light
The use of a UV wavelength light as a no-touch, automated modality for hospital room disinfection has received significant recent attention. The UV-C wavelength of 200 to 270 nanometers is germicidal and involves breaking of molecular bonds in DNA, resulting in microorganism death. Advantages of UV-C technology include its microbicidal activity against a wide range of health-care-associated pathogens, including C. difficile, and the ability for more rapid room decontamination compared to hydrogen peroxide systems. Automated UV-C systems have most commonly been tested for postdischarge terminal disinfection in hospital rooms of patients with C. difficile infection.
This technology's disadvantages include the requirement for the room to be vacated and disinfected before decontamination, its use only for terminal disinfection (vs. daily disinfection), and its significant cost. Also, equipment and furniture must be moved away from walls to prevent shadowing because UV-C systems cannot disinfect areas without a direct or indirect line of sight. Finally, these units require significant time for effective disinfection and can therefore adversely affect bed turnover time. While dependent on many factors (e.g., system being used, dose, organism being targeted), the turnaround time for these devices can range from approximately 15 to 20 minutes for vegetative bacteria to approximately 50 to 100 minutes for C. difficile spores. A recent study utilizing a UV-reflective wall coating resulted in significantly decreased decontamination times, from ∼25 minutes to ∼3 minutes for MRSA, and from ∼43 minutes to ∼9 minutes for C. difficile spores.45
Hydrogen Peroxide-Producing Systems
The use of hydrogen peroxide-producing systems for disinfecting hospital room surfaces and objects has been recently studied. Several systems that produce hydrogen peroxide using differing methods are available (e.g., dry mist, hydrogen peroxide vapor). Advantages of these include reliable microbicidal activity against a variety of pathogens associated with HAIs, including C. difficile, as well as uniform distribution in the room via an automated dispersal system, such that furniture and equipment do not need to be moved away from walls.
However, as with UV-C devices, all patients and health care staff must leave the room before decontamination, and these devices are used for terminal room disinfection (i.e., not for daily disinfection). Costs of these devices can also be substantial, and a lot of time is required for effective disinfection. High-level training is required to operate these devices. Air vents, doors, and windows must be isolated and sealed, and active monitoring with sensors is necessary to monitor for leaks and ensure that the room is safe for personnel to enter. A safety concern with improper use is airway and mucous membrane irritation. As with UV-C devices, hydrogen peroxide–producing systems are a relatively recent disinfection technology and, pending further studies, are not yet routinely used for disinfecting hospital rooms.
Overview of Monitoring Modalities (Guiding Question 1)
Visual Inspection
Visual inspection of hospital room surfaces is often used to assess adequacy of routine cleaning and disinfection practices. However, direct visual inspection can assess only visible cleanliness (e.g., removal of organic debris, dust, moisture) from surfaces and not microbial contamination.46-48 Covert visual monitoring of EVS staff during actual cleaning and disinfection provides an objective assessment of an individual staff member's adherence to protocols, particularly when in conjunction with direct feedback and educational interventions. This method is straightforward, easy to implement in hospitals, and often performed by EVS managers.
Visual inspection can also occur following completion of room cleaning and disinfection by EVS staff; while assessing the subjective cleanliness of surfaces, this method precludes the ability to determine whether these surfaces were actually cleaned. Furthermore, adequacy of cleaning and disinfection as assessed by visual inspection may increase patients' perceptions of cleanliness and therefore satisfaction levels. However, limitations of this monitoring method include interobserver variability and biases secondary to the Hawthorne effect (when the presence of observation affects observed behavior).
Microbiologic Methods
Microbiologic methods have been used to evaluate microbial contamination of environmental surfaces. Methods typically utilize swab cultures, in which a moistened sterile swab is used to sample a surface and then inoculate agar, often with broth enrichment. Swab cultures are easy to use and are often used to sample irregular surfaces, medical equipment, and health care workers' hands. Swab cultures are most often used to identify specific pathogens during epidemiologic investigation of an outbreak. Importantly, the use of aerobic culture (with or without enumerating colony counts) is the only method that can provide information about the viability of our pathogens of interest (e.g. MRSA, VRE).
Another method for sampling is the use of Rodac contact plates, which are small petri plates filled with agar. Sampling of flat environmental surfaces is performed via direct application of the plate to the surface, with the surface area typically measuring 25 cm2. Advantages of contact plates include ease of use and standardization of an approach for quantitative measurement (e.g., results are often expressed as colony-forming units per cm2). However, contact plates can be expensive and allow for sampling of only a small area per plate.
A less commonly used method is the agar slide culture, in which an agar-coated slide with finger holds is used for sampling of flat, hard surfaces. These systems are often used in conjunction with aerobic colony counts (ACCs), a microbiologic method used to quantify microbial contamination of environmental surfaces. The sensitivity of these techniques for recovery of microorganisms depends on many factors, including the type of surface being sampled, specific pathogen, and user technique. For example, a study comparing a swab technique to Rodac plates demonstrated that the sensitivity of swabs for recovery of gram-positive cocci was lower than that of Rodac plates (54% vs. 70%). In contrast, the sensitivity of the swab technique for recovery of gram-negative bacteria was 74% compared to 43% with Rodac plates.49
An overall limitation of methods utilizing ACCs is the lack of accepted criteria for defining a surface as “clean” using ACCs. Additional limitations include the cost of processing (e.g., identifying isolates in the microbiology laboratory), delay in results, small sample area per swab or slide, and the need to determine precleaning levels of microbial contamination for each object or surface being evaluated. In addition, clinical microbiology laboratories do not always perform quality-control assessments in use of ACCs, including maintenance of certification for environmental microbiologic testing. As such, testing using microbiologic methods for environmental monitoring in the hospital setting could benefit from oversight by a certified environmental microbiology laboratory.
UV-Visible Surface Marker
Fluorescent markers can be used in powder or gel form to mark high-touch surfaces before room cleaning and disinfection. Following cleaning and disinfection, UV light inspection is used to determine adequate removal of the fluorescent markers on these surfaces. Fluorescent gel is the most commonly used formulation because it dries to a transparent finish on surfaces, is abrasion-resistant, and unlike powder, is not easily disturbed. For these reasons, the fluorescent gel formulation has been the most well-studied method to assess surface disinfection and to quantify the impact of educational interventions.
Advantages of UV-visible surface markers include relative low cost of use and ease of implementation, including as a feedback tool for EVS staff. Importantly, because fluorescent markers are designed to correlate with physical removal of an applied substance, surfaces that are effectively disinfected (i.e., decreased microbial contamination) but less effectively “cleaned” may be noted as failing to meet quality standards of cleaning. An additional limitation of this assessment method is that unlike ACCs, fluorescent gel cannot be used to detect the presence of a specific organism; therefore, its utility during a pathogen-specific outbreak may be adjunctive.
ATP Assays
ATP bioluminescence assays are commonly used in the hospital setting. ATP assays detect the presence of organic debris on surfaces, are easy to use, and can provide direct, rapid feedback to EVS staff. A special swab is used to sample the surface of interest and placed in a reaction tube. The reaction tube is subsequently entered into a device luminometer, with results expressed in relative light units (RLUs). However, ATP assays 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.
Along these lines, a few studies have shown poor agreement between ATP readings and ACCs in regard to defining surfaces as “clean.”48,50 Furthermore, some studies have shown that certain disinfectants can interfere with ATP readings. Nevertheless, ATP assay measurements can serve as a general measure of cleanliness, and given their ease of use, have utility as teaching and monitoring tools.
A cutoff level that can be used as a surrogate measure of an increased risk of HAIs has not yet been validated. Cutoffs used to classify surfaces as “clean” by ATP assays depend on the assay system used, and universal cutoffs for ATP levels and “cleanliness” have not been established. The sensitivity and specificity of different luminometers/assay systems can differ significantly.
Polymerase Chain Reaction–Based Technology
Polymerase chain reaction (PCR)–based assays for assessing EC are currently investigational. PCR-based assays offer rapid turnaround time for detecting the presence of specific organisms (e.g., MRSA, C. difficile) and are performed in the microbiology laboratory following sampling of surfaces, usually via swabs.
However, these assays currently do not differentiate between the presence of viable versus nonviable microorganisms. As these technologies become less expensive, they may have a larger role in assessing effectiveness of cleaning and disinfection, particularly in the outbreak setting.
Interaction of Cleaning, Disinfecting, and Monitoring Strategies (Guiding Question 1)
The integration of cleaning, disinfecting, and monitoring strategies is important in reducing environmental contamination and the risk of transmission of nosocomial pathogens. The physical action of cleaning removes foreign material from environmental surfaces and HTOs. Disinfection is needed to eliminate many pathogens following the cleaning process. Finally, implementing systems to monitor the appropriateness of cleaning and disinfection is critical in optimizing the effectiveness of these processes on a regular basis. Integration of cleaning, disinfection, and monitoring strategies requires a multidisciplinary approach and often depends on the surface type, patient population, hospital environment, and pathogen(s) being targeted.
Defining “Clean” Surfaces (Guiding Question 1)
Despite the importance of EC and disinfection in reducing microbial contamination on hospital surfaces, no current benchmarks exist to define “clean.” While microbiologic and chemical tools provide a more objective assessment of cleanliness than visual inspection, a lack of consensus still exists on how to correlate results from these monitoring modalities to the “cleanliness” of a surface.
It is clear that an appropriate benchmark for defining a surface as “clean” is needed for effective monitoring of cleaning and disinfection processes. This benchmark should be defined using an evidence-based approach and should indicate whether the “cleanliness” of a surface will lead to a reduction in important patient-level outcomes, including acquisition of hospital pathogens and HAI rates. Benchmarks for “cleanliness” likely will need to be adapted to the patient population, type of surface under study, and specific pathogen(s) being targeted. Lastly, establishment of such benchmarks and integration into EC strategies will allow for more standardized and evidence-based monitoring of cleaning and disinfection processes.
Overview of the Context in Which Cleaning, Disinfection, and Monitoring Modalities Are Implemented (Guiding Question 2)
Key Points
- Implementation of environmental control strategies is highly influenced by appropriate preparation, application, and contact time of disinfectants; adherence to best practices (e.g., checklists); proper education and training; and clearly defined roles for cleaning HTOs.
- Key Informants suggested that institutional leaders should place less importance on room turnover time and more importance on the value of EVS staff.
- Despite pressures on compliance with evidence-based policies and procedures from various health care organizations (e.g., CDC), only one study reported on the influence of external factors in EC.
- Institutional collaboration between Infection Prevention and Control and EVS Management is critical while developing EC programs. Five studies described participation in planning and processes by individuals (e.g., infection prevention nurses), committees, and departments.
- Educational tools, training tools, and protocols should be language-appropriate and written in a manner commensurate with education level. Twenty-four (32%) studies reported integrating implementation and management tools into their EC strategies; educational tools were the most commonly integrated tool.
- Understanding local hospital culture is key when outsourcing EC services.
We present below insight from KIs on the influence of context on implementation followed by a description of a conceptual or analytic framework for identifying high-priority contexts. Lastly, we present contextual factors relevant for implementation of EC from all 76 studies followed by detailed information on the 17 studies primarily focused on implementation.51-67
Key Informant Feedback
Key Informants frequently emphasized the impact of contextual factors on the effectiveness of EC and monitoring. Several KIs suggested that selecting any particular disinfecting agent or monitoring modality versus another was less important than implementation processes at the local level. A common sentiment was that “it's not what you use, it's how you use it.”
Key Informants identified several aspects of implementation that can influence the effectiveness of EC. One important concern is basic compliance with appropriate preparation and application of disinfectants. Some agents must be diluted before use, and one KI noted that “if you have 20 EVS personnel, you have 20 ways to dilute bleach.” After preparation, a disinfectant must remain in contact with a surface for the labeled contact time for optimal effectiveness, but in daily practice contact time may fall short of labeled instructions.
A related challenge described by KIs is the inconsistency of workflow, especially during daily room cleaning and disinfection, as EVS personnel must respect patients' personal needs and preferences while working around clinical staff interventions, meal delivery, linen services, visitors, and other routine “interruptions.”
Terminal room cleaning and disinfection, after a patient has been moved or discharged, has its own challenges. Many KIs expressed concern that hospital leaders may place too great a premium on room turnover time, resulting in suboptimal adherence to cleaning and disinfection protocols. Pressure to achieve rapid room turnover may also discourage use of technologies that require more time to implement, such as no-touch modalities.
Key Informants cited training as vital to ensure that EVS staff recognize the clinical significance of adhering to proper work procedures and guiding them on how to manage routine workflow. Staff in some hospitals undergo extensive initial and ongoing education, including training on how to foster a “customer service” atmosphere when interacting with patients. Institutions may also use simulation to map workflow and design systems that are less user-dependent and more intuitive.
Several KIs also regarded checklists used by EVS personnel as a useful tool to standardize procedures and encourage adherence to best practices. The impact of these training strategies may be lower in work environments where staff turnover is high. Additionally, one KI noted that while many EVS staff may not speak English as their primary language, training materials and protocols are rarely available in other languages.
Another related factor that KIs discussed is the individual hospital patient safety culture. A positive culture can foster collaboration and respect among clinical and support services staff and nurture supportive relationships between supervisors and frontline personnel. Conversely, failure to build a positive culture can contribute to suboptimal work performance. Institutional leadership and the value that executives place on EVS are important contributing factors in organizational culture. KIs described examples of hospitals whose leadership embraced and emphasized EC's importance, resulting in better compliance with best practices. Alternatively, a few KIs cautioned that when faced with financial challenges, some hospital executives may view room cleaning and disinfection as low priority and resort to reducing staff and supplies.
An important aspect of the work culture is how clinical and administrative professionals in the hospital perceive the role of EVS staff. Almost every KI indicated that staff are often underappreciated despite playing a critical role in the infection prevention community. Some KIs suggested that hospitals consider EVS staff as “environmental cleaning technicians” or use a similar title that reflects the technical complexity of their responsibilities (e.g., preparing and applying an array of disinfection agents, operating newer technological modalities) and the important contribution of their work to effective infection prevention. Others described the importance of sharing HAI rates with EVS departments to reaffirm the importance of EVS staff.
Conceptual Framework for Contextual Factors
The influence of contextual factors on implementation was a major theme of the March 2013 AHRQ report, “Making Health Care Safer II: An Updated Critical Analysis of the Evidence for Patient Safety Practices.”68 In earlier work, “Assessing the Evidence for Context-Sensitive Effectiveness and Safety of Patient Safety Practices: Developing Criteria,” Shekelle et al. laid out a framework for assessing evidence for context-sensitive interventions.69 The report recommends assessing the “high-priority contexts” of four domains: (1) structural organizational characteristics (e.g., size, location, financial status); (2) external factors (e.g., regulatory requirement, pressure from penalties such as pay-for-performance); (3) patient safety culture (e.g., teamwork and leadership at the unit level); and (4) availability of implementation and management tools (e.g., staff education and training, dedicated time for training, use of internal audit and feedback).
Structural Organizational Characteristics
An important approach some hospitals have adopted is outsourcing EVS. Environmental support services provided by outside contractors can include training and development programs, designing of comprehensive protocols, competency testing, and participation on infection prevention teams.70,71 While supporting a large EVS department (over 650 employees) at Mount Sinai Hospital (New York, NY), one supplier implemented multiple interventions, including retraining staff (e.g., chemical dilution and use), updating departmental processes (e.g., hospitality training), and introducing new technologies (e.g., a UV irradiation device).71 One study, Brakovich et al. 2013,57 indicated that followup disinfection of rooms formerly occupied by patients with C. difficile infection was outsourced to a company that provided hydrogen peroxide vapor devices and services.
Outsourcing has grown in recent years, according to several KIs, although national economic patterns may partly drive cycles of expansion and decline in use of outsourced service companies. One KI felt that while outsourcing may be cost-effective, better guidance is needed on process monitoring and standardization. Some KIs discouraged outsourcing because outside contractors may not understand local hospital culture, which is a major component of any patient safety program. Lastly, one KI commented that how EVS is organized in a hospital (e.g., location of EVS in the administrative hierarchy) is an important structural factor that can affect the success of EC processes.
External Factors
Compliance with “evidence-based policies and procedures” from organizations such as CDC, EPA, CMS, Joint Commission, FDA, and OSHA are important external factors. In its 2008 “Guideline for Disinfection and Sterilization in Healthcare Facilities,” CDC notes that health care workers need to understand requirements pertaining to them when applying disinfectants and sterilants as well as the relative roles of CDC, EPA, FDA and others in regulating these agents. EPA plays a particularly important role as the agency charged with setting national regulations for the safety and appropriate use of many of the disinfection agents reviewed in this Technical Brief (http://www2.epa.gov/pesticide-registration/antimicrobial-pesticide-registration). For a list of EPA and OSHA regulations related to sterilants and disinfectants, see Table 2.72
Table 2
EPA and OSHA regulations for disinfectants.
CMS reimbursement policies will begin to shape EC efforts in the near future. Beginning in 2017, payment penalties under the Hospital Value-based Purchasing Program will be linked to National Quality Forum-endorsed measures of MRSA and C. difficile infection.73
Patient Safety Culture
Institutional culture has been described as “the accumulation of invisible, often unspoken ideas, values, and approaches that permeate organizational life.”74 Clarke et al. 200675 adds that culture may be partially formed by leadership decisions that ultimately result in cultural norms. Five (7%) studies reported on this domain; three recently published studies (2013–2014) described participation in planning and managing of EC processes by leaders from Infection Control,54 Quality and Safety,57 and EVS.58 Two earlier studies reported the influence of project directors64 and the Department of Infection Control.66
Collaboration between infection prevention and control and EVS management during implementation phases (both planning and ongoing) is one of several key components presented by CDC in a two-level program to evaluate EC. The 2010 toolkit, “Options for Evaluating Environmental Cleaning,”76 presents context (specific to terminal room cleaning) to assist hospitals in developing programs to improve HTO cleaning. The toolkit recommends that institutions start with a basic program that is consistent with previously issued guidelines.23,77 It stresses the importance of the two disciplines working together to set expectations for staff, to develop metrics for competency evaluation and educational programs for hospital and EVS staff.
Administrative leadership is also “critical in managing outbreak situations,” according to APIC's “Guide to Preventing Clostridium difficile Infections.”78 The administrator's responsibilities include ensuring staff have sufficient time to thoroughly clean (including adequate contact time for cleaning agents) and working with EVS and infection prevention staff to develop a monitoring program that provides desired information and timely feedback.
Implementation and Management Tools
Another component of CDC's program is the development of a hospital-specific program (consistent with CDC standards23,77) and use of a checklist for cleaning “objects in the patient zone.” Cleaning checklists for HTOs were used in five studies;52,54,56,57,60 one study used a 43-point room cleaning checklist.54 CDC also specifies that the responsibilities for cleaning HTOs should be clearly defined to avoid miscommunication among staff. One KI noted that roles are not usually clearly defined—for example, nursing staff believe that EVS personnel are responsible for cleaning an undesignated area of a patient's room and vice versa, which may result in inadequate room cleaning.
Next, CDC encourages “structured education for EVS staff” and outlines educational elements for EVSs frontline personnel such as:
- Provide an overview of the importance of HAIs in a manner commensurate with their educational level.
- Review specific terminal room cleaning practice expectations.
- Discuss the manner in which their practice will be monitored.
- Repeatedly reinforce the importance of their work.
Of the 24 (32%) studies that integrated implementation tools, 23 (96%) studies reported education as a key component while five studies specifically reported on training staff.54,57,79-81 Smith et al. 201456 reported integrating educational interventions such as hands-on education with ATP devices and use of the “Clean Sweep” electronic game in which users rank three high-touch surfaces (from cleanest to least clean) from a drop-down menu, then submit the data for feedback. In 2007, Whitaker et al. provided education for staff, patients, and visitors,82 while other studies used a training DVD, competency-based training,79 training on preparation, use and storage of products,80 and training on the use of chemicals.57
Next, CDC recommends developing measures for monitoring staff competency and performance that may include evaluations and utilize patient satisfaction surveys. One approach to evaluate skill acquisition is the Dreyfus model.83 This model describes five levels of expertise from novice to expert level and can be used “(a) to provide a means of assessing and supporting progress in the development of skills or competencies, and (b) to provide a definition of an acceptable level for the assessment of competence or capability.” Five studies (all published since 2012) described audits.58-60,80,84 One study included a UV monitoring audit tool,59 while another integrated monthly EC audits.80 Ramphal et al. 201453 implemented “blinded monitoring with transparent reporting of the results in a positive, engaging manner,” while Hota et al. 200962 utilized “intensified” monitoring “providing immediate, specific feedback.” One KI recommended leveraging organizations such as APIC (http://www.apic.org/) and Infection Control and Prevention-Canada (http://www.ipac-canada.org/) to inform and encourage “translation of knowledge” to frontline staff. Another KI emphasized the importance of identifying those who can best communicate to EVS staff, particularly when staff knowledge deficits or other concerns are identified.
According to CDC, each “cycle of evaluation” should be followed by feedback to EVS staff, with results “shared widely within and beyond the institution.” Distinct methods of feedback described in primary studies were weekly electronic feedback (e.g., unit rates, rankings) to EVS, hospital leadership, and unit administrators;85 feedback of UV-powder and gel surveillance results to EVS staff, hospital leadership, and unit administrators,85 feedback from staff focus groups;86 and feedback to EVS staff (monthly meetings, small group meetings, and individual meetings).87 To optimize the thoroughness of terminal room cleaning and disinfection, CDC recommends discussing the results of monitoring programs and interventions as “a standing agenda item for the Infection Control Committee.”
One acute care hospital used patient satisfaction surveys to measure patient satisfaction after the introduction of a pulsed xenon ultraviolet (PX-UV) device.88 Satisfaction scores were measured on the Hospital Consumer Assessment of Healthcare Providers and Systems survey on a quarterly basis over 13 quarters. Forwalt and Riddell noted that “after the introduction of the PX-UV system, the score for cleanliness and the overall rating of the hospital rose from below the [50th] to the [99th] percentile,” which ultimately resulted in financial benefits to the hospital.
Evidence of the Effectiveness of Strategies for Implementing Cleaning, Disinfection, and Monitoring Modalities (Guiding Question 2)
Key Points
- Seventeen implementation studies were conducted primarily in the United States and were designed as before-and-after studies.
- Fourteen (82%) studies implemented single-component strategies to prevent HAIs due to multiple pathogens. Infection rate was the primary outcome for two (14%) studies. Surface contamination-related outcomes were the primary focus of 12 (86%) studies.
- Three (18%) studies reported positive results from implementing multicomponent strategies to prevent C. difficile infections.
- Five studies reporting on sustainability of preventive strategies described ongoing education, direct feedback, and commitment and flexibility of administrative leaders as key components to successful implementation.
Primary Studies
We next present detailed information on the studies focused specifically on implementing infection control interventions and contextual factors. Seventeen studies were published between 2006 and September 2014; nine (53%) studies were published since 2012. Most studies were conducted in the United States, and others were conducted in Australia58 and Canada.59,60 Complete information on these studies is available in Appendix C.
Study Characteristics
Thirteen studies used historical controls, including before-and-after study designs (9), and interrupted time series (4).52,53,57,63 Three studies used nonrandomized concurrent controls,56,59,61 and one was an uncontrolled, descriptive study.55 Study length ranged from 8 weeks to 4 years. Three studies implemented multicomponent strategies.52,53,57 One study implemented an infection prevention bundle that included contact precautions for patients with diarrhea and sign placement for patients with confirmed/suspected C. difficile infection.52 Other studies incorporated hand hygiene53 and antibiotic stewardship57 with their EC strategies.
The unit of analysis in order of most to least common were patient rooms, HTOs, hospital units, hospitals, beds, and patients. The primary setting for six studies was the ICU.55,60-63,89 Other settings included burn units,52 telemetry units,52 long-term acute care hospitals,57 general medical wards,59 respiratory step-down units,65 and a surgical ward.66 Wards were not specified in three studies.51,53,58
C. difficile was the primary focus of three studies.52,57,59 VRE was the primary focus of two studies.62,67 The remaining studies focused on at least two of the three pathogens of interest. Five studies reported cleaning and disinfection of more than 15 HTOs.52,53,55,56,65 One study's sole focus was the bathroom.59 Most commonly reported HTOs included bed rails, call buttons, light switches, tray tables, and toilets, but there was substantial variety in selection of HTOs across studies.
Use of ATP bioluminescence and fluorescent/UV markers was widely integrated into implementation strategies as monitoring and educational tools. Cleaning and disinfection methods reported by some studies included hypochlorite-based disinfectant,52 QAC,56,61,62 hydrogen peroxide vapor, and microfiber mops.57
Study Outcomes
Primary outcomes for most studies were variants of surface contamination (e.g., surfaces cleaned, positive cultures, compliance with room cleaning and disinfection protocols). Acquisition of pathogens was reported as a primary outcome in two studies.61,67 Infection rate was reported as a primary outcome in three studies57,61,67 and as a secondary outcome in two studies.52,53
All three studies implementing multicomponent preventive strategies reported positive results. Koll et al. 201452 reported significant reductions in hospital-onset C. difficile infection rates at 35 participating New York metropolitan regional hospitals. Ramphal et al. 201453 reported statistically significant improvements in cleaning rates due to repeated training, while Brakovich et al. 201357 reported success in decreasing C. difficile incidence.
Of the remaining 14 implementation studies, the study length of 6 studies was 6 months or fewer. Two studies (2 months in duration)51,60 reported that use of ATP and fluorescent markers as monitoring tools resulted in “rapid improvements in cleaning thoroughness”60 and “enhanced collaboration, communication and education.”51 One 4-month trial (Rupp et al. 2014)55 identified a subgroup of housekeepers or “optimum outliers” who were significantly more efficient and effective than their coworkers. The authors hoped to use their exemplary performance to increase overall performance improvement. Three studies described various monitoring methods (e.g., swab cultures,66 fluorescent markers,58 UV markers59) as useful tools to audit and educate staff.
One recently conducted 4-year study (Rupp et al. 2014)54 concluded that monthly feedback and face-to-face meetings with frontline staff were crucial to EC success. Hayden et al.67 demonstrated that a multimodal intervention to improve EC and hand hygiene reduced VRE acquisition in an endemic setting. Datta et al. 201161 concluded that enhanced cleaning (bucket immersion of cloths into QAC) may reduce MRSA and VRE transmission and eliminate risk of MRSA acquisition from a room previously occupied by a patient colonized with MRSA. Results from three studies demonstrated improvements in cleaning rates,63,65 with an expectation that the decrease in environmental contamination would help control spread of multi-drug-resistant organisms (MDROs).67
Lastly, Hota et al. 200962 purported that VRE contamination is caused by poor adherence to procedures and use of products “rather than to a faulty cleaning procedure or product.” Carling et al. 200864 conducted the largest study (a collaborative of 36 hospitals) and concluded that an EC program's success relies on support by administrative leadership and institutional flexibility.
Several studies reported on the sustainability of their preventive strategies. Ramphal et al. 201453 reported sustaining gains for 6 months. Trajtman et al. 201359 described use of graphs posted on the wards and in the EVS office to assist in “sustained improvement in cleaning compliance.” In 2011, Murphy et al.58 reported unsustainable gains without ongoing education. In 2008, Carling et al.64 reported results of collaborative efforts by 36 hospitals to improve cleaning practices. Eight hospitals that had participated for over 2 years in the program reported data on sustainability. They found that the thoroughness of cleaning decreased by 10% to 20% within 6 to 18 months of the last feedback session. Of the remaining 59 studies, only 1 study reported sustainability of its EVS strategy and reported “prolonged benefits” from 12-week use of fluorescent markers combined with regular feedback of results.85
Evidence of the Effectiveness of Strategies for Environmental Cleaning and Disinfection (Guiding Question 3)
Key Points
- Study designs for primary studies focusing on cleaning and disinfection were mostly limited to nonrandomized concurrent or historical controls.
- Use of QAC, chlorine-based disinfectants, and UV or hydrogen peroxide vapor devices were well studied, while use of peracetic acid/hydrogen peroxide wipes, enhanced coatings, or microfiber cloths were not.
- C. difficile, MRSA, and VRE were most to least well studied, respectively.
- Primary outcomes included variants of surface contamination (40 studies), infection rate (13 studies), and colonization (3 studies).
- Studies examining chemical disinfectants reported mixed findings. Results from six studies examining chlorine-based products reported improvements in infection rates with bleach (4 studies);82,90-92 ineffectiveness of Difficil-S in reducing infection rates (1 study)80 and no difference in reducing microbial burden when comparing Virex with QAC (1 study).93 One study reported that use of a potassium monopersulfate-based product was ineffective in reducing C. difficile spores.94
We identified 4 systematic reviews and 59 primary studies that met the inclusion criteria for this question. The focus of 2 systematic reviews108,109 and 47 primary studies9,38,79-82,84,86,87,90-107,110-129 was cleaning and disinfection.
Systematic Reviews
Two systematic reviews addressed this topic. First, Falagas et al. 2011108 reviewed the effectiveness of airborne hydrogen peroxide (vapor and dry mist formulations) in hospital settings in 10 studies published before December 2009. Seven studies evaluated the delivery of hydrogen peroxide in the form of vapor while three studies evaluated delivery of hydrogen peroxide in the form of a dry-mist system or “dry fog.” Pathogens addressed included MRSA (5 studies) and C. difficile (3 studies). Settings included surgical wards, “ward side rooms,” and bathrooms. Results indicated significant reductions in contamination of sampled environmental sites after use of hydrogen peroxide compared with standard terminal cleaning and disinfection (39.0% [range 18.9% to 81.0%] baseline, 28.3% [range 11.9% to 66.1%] after standard terminal cleaning, 2.2% [range 0% to 4.0%] after addition of airborne hydrogen peroxide). Two studies reported on effectiveness of hydrogen peroxide on infection rates. One study (conducted in a 20-bed surgical ward) indicated “eradication of MRSA,” while the other study (conducted in a 500-bed hospital) indicated “significant reductions in C. difficile-associated disease.” Despite favorable results for the use of airborne hydrogen peroxide for disinfection and infection control, the authors called for additional studies to “assess the effectiveness, safety, costs, and applicability of this novel method against other available cleaning methods.”108
Second, Dettenkofer et al. 2004109 evaluated the effects of disinfection compared with cleaning with “detergent only” of environmental surfaces on HAI rates. The review included four clinical trials published through 2001. Settings included tertiary hospitals, medical units, and ICUs. Disinfectants included QAC, orthobenzyl-parachlorophenol, 0.5% aldehyde, and a 1:10 hypochlorite solution. Three studies indicated no significant difference in the rates of nosocomial infections. Results from the fourth study indicated a significant decrease in HAI rates in bone marrow transplant patients but no decrease in rates in patients in the neurosurgical ICU or a general medicine unit. The authors concluded that targeted disinfection is an “established component of hospital infection control,” but future research will require well-designed studies due to the “complex, multifactorial nature of nosocomial infection.”109 The two systematic reviews are summarized in Appendix C.
Primary Studies
Of the 47 primary studies addressing this topic, 27 (57%) were conducted in the United States. The remaining 20 (43%) studies were conducted in the United Kingdom,80,81,104,105,107,111,119,122,126,129 Australia,79,84,86,117,123 Sweden,94,106 Canada,120 Norway,121 and Italy.92 Studies were published between 1998 and September 2014, but 28 (59%) were published since 2012, reflecting recently growing interest in EC. Cleaning and disinfection methods were generally categorized as surface cleaning and disinfection, automated processes, or enhanced coatings or surfaces. Two studies examined steam vapor116 and mopping methods.92 Of the remaining studies, 33 focused solely on either surface cleaning/disinfection (21 studies), automated technologies (8 studies), or enhanced coatings (4 studies), while 12 studies reported on a combination of methods.
Reported touch modalities included QAC, chlorine-based disinfectants (e.g., Chlor-Clean, Difficil-S, Oxivir, Virex, bleach), wipes (e.g., accelerated hydrogen peroxide wipes, disposable V-wipes, peracetic acid wipes), other detergents (e.g., potassium monopersulfate), and neutral electrolyzed water.129 Seventeen studies evaluated the effectiveness of no-touch modalities, including automated UV light, hydrogen peroxide vapor, or steam vapor to reduce microbial burden. Ten studies (published since 2010) examined UV-C devices such as Tru-D 87,112,118,122,124,125,128 or PPX-UV.9,99,100 Seven studies evaluated use of hydrogen peroxide vapor systems such as BioQuell79,101,111,114,117,124 or steam vapor using the VaporJet PC 2400.116 Enhanced coatings or surfaces included copper,38,102-105,107 organosilane antimicrobial,127 and “Appeartex,” an antimicrobial coating.106 Lastly, two distinct studies compared cleaning methods (i.e., mopping methods,121 quaternary ammonium delivery by spray or bucket110). Table 3 summarizes key characteristics of the primary studies identified by our search. Further information about the primary studies is presented in Appendix C. The systematic reviews are summarized in Table C-1.
Table 3
Summary of cleaning and disinfection primary studies.
Study Characteristics
Five studies were RCTs, and one was a randomized crossover study. Fourteen studies used nonrandomized concurrent controls, while 27 used historical controls, including 22 before/after study designs and 5 interrupted time series. Study length ranged from 4 weeks to 43 months. Three studies implemented multicomponent strategies (i.e., integrated an additional non-EC-related strategy).79,119,123 The multicomponent strategies in one study included monitoring of hand-hygiene compliance and antimicrobial usage, additional active MRSA surveillance with more rapid turnaround of laboratory results, and implementation of isolation precautions.79 Preventive strategies in another study included hand-hygiene education and enforcement of an antibiotic policy.119 The third study integrated modified protocols to rely on alcohol-based hand hygiene and sleeveless aprons in place of long-sleeved gowns and gloves.123 One study (Byers et al. 1998)110 was a description of disinfection practices in the context of an outbreak.
The units of analysis were most commonly patient rooms or microbiologic samples. Numbers of rooms ranged from 4121 to 11,389.100 Numbers of samples ranged from 142112 to 20,736.119 The primary setting for most studies was the ICU or general medical or surgical wards. Other settings included cancer wards,84,123 “intensive therapy unit,”122 transplant ward,123 and a long-term care ward.116
Monitoring methods used in these studies were categorized as swab cultures (13 studies), contact plates (9 studies), agar slide cultures (8 studies), fluorescent/UV markers (5 studies), and visual observation (3 studies). Other monitoring methods were described as sponge/wipe cultures, agar contact plates for aerobic bacteria, surface contact plates and seeded petri dishes, wipes, glove and hand plate cultures, and wipe/swatch cultures.
C. difficile was the primary focus of 13 studies.80,81,87,90,91,94,97,99,101,111,118,120,126 VRE was the primary focus of four studies,84,110,117,123 and MRSA was the focus of two studies.9,79 The remaining studies focused on at least two pathogens, including one of the three pathogens of interest (C. difficile, MRSA, VRE). Most commonly reported HTOs were bed rails, side/tray tables, toilets, and floors. Table 3 includes the modalities by type of pathogen.
Study Outcomes
The primary outcome for 31 (66%) studies was surface contamination (e.g., bacterial burden, number of surfaces cleaned, positive cultures).9,38,80,84,86,87,92-94,96,98,103-107,111-113,115-118,120-122,124,125,127-129 Sixteen (34%) studies reported infection rate (e.g., incidence rate expressed per 1,000 patient-days)9,79,81,82,90,91,97,99-101,111,114,126 or colonization80,102,123 as a primary outcome. Eight studies reported on C. difficile, two studies reported on MRSA, one study reported VRE infection rates, and three studies reported overall HAI rates. Other reported primary outcomes included compliance with room cleaning protocol,98 contamination rates for health care worker gowns/gloves,95 and number of bed areas where target pathogens were isolated during a sampling day.119
Secondary outcomes of interest included C. difficile ribotypes,111 cleaning time,9,98 adverse effects,96 hospital-acquired C. difficile infection–attributable deaths/colectomies,99 ease of use of ATP and Tru-D device,121,128 and recontamination.129
Studies examining chemical disinfectants reported mixed findings. Grabsch et al. 2012123 found marked reductions in new VRE colonization after implementing the Bleach-Clean program (a multicomponent strategy). Four studies examining bleach82,90-92 reported reduced C. difficile rates. One study examining the effectiveness of accelerated hydrogen peroxide versus stabilized hydrogen peroxide suggested that the accelerated hydrogen peroxide formulation was significantly better.120
Other studies, however, reported no difference or identified strategies that were ineffective. One study reported that use of Difficil-S, a chlorine-based product, was ineffective in reducing C. difficile contamination and C. difficile infection rates.80 Sjoberg et al. 201494 reported a “moderate spread of C. difficile spores despite use of a potassium monopersulfate-based disinfectant (Virkon™).”94 One randomized trial by Schmidt et al. 201293 reported no difference in “mean relative reduction of microbial burden” after use of Virex soaked on a washcloth or quaternary ammonium as a microdroplet from the PureMist system. Lastly, Stewart et al.129 reported that while electrolyzed water significantly reduced microbial counts (including MRSA) 1-hour postcleaning, microbial counts exceeded original levels at 24 hours.
Studies integrating wipes into their cleaning and disinfection regimens reported positive findings. Friedman et al. 201384 studied the application of a QAC (Viraclean) or V-wipe against VRE contamination. The authors reported significantly lower residual levels of VRE compared with earlier levels using a benzalkonium chloride-based product for disinfection. Other studies integrating wipes into a surface-cleaning routine reported a nonsignificant reduction in contamination of health care worker gowns and gloves after routine patient care activities,95 a significant reduction in C. difficile rates,81 effectiveness as a surface disinfectant,96 and sustained reductions in hospital-acquired C. difficile infection.97 They supported the use of ready-to-use wipes over a traditional bucket method.98
Authors of the 10 studies examining UV light devices87,112,118,122,124,125,128 or PPX-UV devices9,99,100 as adjunctive infection control measures, concluded that the devices effectively reduced bacterial bioburden,87,112,118,122,125,128 significantly reduced hospital-acquired C. difficile infection rates,99 significantly decreased overall hospital-acquired MDRO rates,100 or was superior to manual disinfection.9 One study stated that integration of education, monitoring, feedback, a dedicated daily disinfection team, and implementation of a standardized process played a role in improved thoroughness.87 One study comparing UV-C to hydrogen peroxide vapor124 indicated effectiveness of both devices in reducing bacterial bioburden, but indicated that hydrogen peroxide vapor was significantly more effective due to UV-C's ineffectiveness “for sites out of direct line of sight.”
Of the six remaining studies evaluating hydrogen peroxide vapor79,101,111,114,117 or steam vapor,116 investigators reported reductions in MRSA contamination from a multicomponent strategy,79 significant reductions in C. difficile-associated diarrhea rates,101 reduced environmental contamination and risk of acquiring MDROs compared with standard cleaning/disinfection,114 and >90% or highly effective reduction in bacterial levels.111,116,117
Of the eight studies examining enhanced coatings or surfaces, authors indicated significantly lower rates of incident HAI and/or colonization compared with patients in standard rooms;102 that the integration of copper reduced103,104 or significantly reduced38,105-107 surface bacterial bioburden, and no sustained impact on antimicrobial activity for organosilane products tested.127
Anderson et al. 2009121 compared various modes of mopping and indicated that wet, moist, and dry mopping more effectively reduced bacterial burden on the floor than spray mopping. Lastly, Byers et al. 1998110 indicated that the “new bucket method” of delivering quaternary ammonium resulted in “uniformly negative cultures.”
Evidence of the Effectiveness of Strategies for Monitoring of Cleanliness (Guiding Question 3)
Key Points
- Fluorescent/UV markers and ATP bioluminescence were well-studied monitoring methods, while visual observation, agar slide cultures, and swab cultures were not.
- Ten (83%) studies were designed with nonrandomized concurrent or historical controls.
Of the 4 systematic reviews and 59 primary studies that met the inclusion criteria for this question, the focus of 2 systematic reviews130,131 and 12 primary studies was monitoring.17,18,85,132-140
Systematic Reviews
Two systematic reviews examined monitoring tools for cleaning and disinfection. The sole focus of one systematic review (Amodio and Dino 2014)130 was ATP bioluminescence. The other review (Mitchel et al. 2013)131 took a broader approach and addressed visual inspection, fluorescent gel markers, ATP bioluminescence, and microbiological sampling.
Amodio and Dino 2014130 included 12 studies published from 2000 to 2011 and conducted in the United Kingdom (8 studies), the United States (3 studies), and Brazil (1 study). Surfaces were monitored after cleaning and disinfection (4 studies), before and after (6 studies), or time of monitoring was not reported (2 studies). No study included concurrent surface cultures to correlate with microbial burden. ATP thresholds for RLUs ranged from 100 to 500. One study evaluated two thresholds (250 and 500 RLUs). Reported ATP threshold failure rates before cleaning ranged from 21.2% to 93.1% while after cleaning ranged from 5.3% to 96.5%. The authors concluded that while ATP was a quick and objective method for evaluating hospital cleanliness, it appeared to be poorly standardized at both the national and international level.
Mitchel et al. 2013131 reviewed 124 articles for inclusion in the review (the final number of studies included was not reported). Findings from six studies evaluating visual inspection indicated “poor performance at identifying microbial load with 17% to 93% more surfaces identified as clean compared with other monitoring methods.” Findings from seven clinical trials evaluating fluorescent markers indicated a frequent lack of attention to “high-risk surfaces in the near-patient zone.” For ATP, Mitchel et al. 2013 described the low specificity and sensitivity in detecting bacteria. Lastly, microbiological sampling was recommended only in certain situations (e.g., ongoing outbreak investigations) since the process typically takes at least 2 days and requires technical expertise and laboratory capacity. For routine EC evaluation, the authors called for “fast, reproducible, cost-effective and reliable methods” to predict “timely clinical risk.” These systematic reviews are summarized in Table C-1 in Appendix C.
Primary Studies
Of the 12 primary studies focused on monitoring, seven (58%) studies were conducted in the United States. Other settings included the United Kingdom (3 studies) and Canada (1 study); one location was unspecified. Studies were published from 2003 to 2013; three (25%) studies were published since 2012. Fluorescent/UV markers and ATP bioluminescence were the most commonly evaluated monitoring methods and were included in eight (67%) and five (42%) studies, respectively. Other monitoring methods evaluated were visual observation (5 [42%]) studies), agar slide cultures (3 [25%]) studies), and swab cultures (1 [(8%]) study). Al-Hamad and Maxwell evaluated agar slide cultures and the wipe-rinse method and assays. Six studies85,132-136 focused on fluorescent/UV markers, and six other studies17,18,137-140 evaluated several monitoring methods. Information on cleaning and disinfection methods and implementation factors associated with these studies were mostly unreported. Table 4 summarizes the primary studies on monitoring modalities identified in our literature searches. Additional information on these studies is available in Appendix C. The systematic reviews are summarized in Table C-1.
Table 4
Summary of modalities examined and study designs used in primary monitoring studies.
Study Characteristics
Five studies used nonrandomized concurrent controls, four used historical controls, and three studies did not have comparison arms. One study (Al-Hamad and Maxwell 2008)139 was also designed to study the “correlation of two monitoring methods.” Study length ranged from 4 weeks to 8 months (4 studies did not report study length). All the studies implemented a single-component EC strategy. The reported units of analysis were rooms (7 studies) or microbiologic samples (6 studies). Numbers of rooms ranged from 10 to 1,119. Numbers of microbiologic samples ranged from 90 to 3,532. Other units of analysis included surfaces (3 studies), hospitals (1 study reported, including 27 hospitals),132 patients (1 study), and hospital wards (1 study). The unit of analysis in one study (Carling et al. 2008)136 was 13,369 high-risk objects. Of the studies reporting setting (4 did not), four studies were set in the ICU and one was set in a general medical and surgical ward. Four studies focused on a single pathogen.18,133,135,139 The most commonly reported HTOs were bed rails, tray/side table, toilet, call buttons, light switches, and door knobs.
Study Outcomes
Primary outcomes for eight studies were reported as percent of targets cleaned17,132-134 or cleaning rate.18,85,135,136 Two studies138,140 reported air or surface microbial burden counts (RLUs or colony-forming units [CFUs]), while other studies reported sensitivity to detect pathogens137 or number of positive cultures139 as the primary outcome of interest.
Six studies mainly focusing on fluorescent/UV markers85,132-136 reported positive results. The technologies were reported as useful, inexpensive, simple, highly objective surface targeting methods85,132,134 that helped achieve significant improvements 132,136 in cleaning and disinfection practices at their respective institutions. Blue et al. 2008133 reported that the fluorescent chemical GlitterBug was “superior to previous visual inspection methods.”
Results from the six studies17,18,137-140 evaluating various monitoring methods mostly described the inferiority of visual observation compared to other monitoring methods. Of the six studies, five had nonrandomized controls.17,18,137,138,140 Luick et al. 2013137 reported that fluorescent marker and ATP assay “demonstrated better diagnosticity” than visual inspection. Smith et al. 2013138 reported that despite measuring different aspects of environmental contamination, quantitative microbiology and ATP both “generally agree in distinguishing clean from dirty surfaces.” Snyder et al. 201317 reported poor correlation between ATP/fluorescent markers and a microbiologic comparator. One study18 proposed an ATP benchmark value of 100 RLUs since it would offer the closest correlation with microbial growth levels <2.5 CFU/cm2. A 2003 study140 recommended assessing effectiveness of hospital disinfection with internal audit and rapid hygiene testing. Lastly, results from a before/after study (Al-Hamad and Maxwell 2008)139 indicated a “poor correlation between the findings of total aerobic count and MRSA isolation.” See Appendix C for further details on the outcomes and conclusions reported in these studies.
Evidence Map (Guiding Questions 3 and 4)
The evidence map that follows is designed as a concise, visual summary of the evidence base and major evidence gaps on EC for preventing HAIs.
Figure 2 shows the number and research design of published studies that address major categories of cleaning and disinfection strategies. Figure 3 presents the number and research design of studies of monitoring modalities. Figure 4 and Figure 5 provide snapshots of how many studies address critical outcomes and major pathogens, respectively, from among articles that evaluate cleaning, disinfection, monitoring, or implementation of these strategies. Figure 6 depicts evidence gaps that suggest high-impact areas for future research, as recommended by our Key Informants or indicated by our analysis of the current evidence base. The interventions in Figure 6 are organized in a framework adapted from McDonald and Arduino's recently proposed “evidence hierarchy” for environmental infection control.141 This framework represents the progression of evidence for the effectiveness of EC interventions, from laboratory studies that measure surface contamination, to clinical studies that assess contamination in real-world settings, to studies of pathogen colonization and infection in patients.
Summary of Published Evidence
Figure 2Cleaning modalities: number of studies by study design
2 systematic reviews, 47 primary studies*
* Some studies evaluated more than one modality.
Figure 3Monitoring modalities: number of studies by study design
2 systematic reviews, 12 primary studies*
* Some studies evaluated more than one modality.
Figure 6Evidence needs
HP=hydrogen peroxide; HPV=Hydrogen peroxide vapor; PCR=Polymerase chain reaction; QAC=quaternary ammonia compounds; RCTs-randomized controlled trials; UV=ultraviolet Adapted from McDonald and Arduino. Climbing the Evidence Hierarchy for Environmental Infection Control141
- Overview of Cleaning and Disinfection Modalities (Guiding Question 1)
- Overview of Monitoring Modalities (Guiding Question 1)
- Interaction of Cleaning, Disinfecting, and Monitoring Strategies (Guiding Question 1)
- Defining “Clean” Surfaces (Guiding Question 1)
- Overview of the Context in Which Cleaning, Disinfection, and Monitoring Modalities Are Implemented (Guiding Question 2)
- Evidence of the Effectiveness of Strategies for Implementing Cleaning, Disinfection, and Monitoring Modalities (Guiding Question 2)
- Evidence of the Effectiveness of Strategies for Environmental Cleaning and Disinfection (Guiding Question 3)
- Evidence of the Effectiveness of Strategies for Monitoring of Cleanliness (Guiding Question 3)
- Evidence Map (Guiding Questions 3 and 4)
- Findings - Environmental Cleaning for the Prevention of Healthcare-Associated In...Findings - Environmental Cleaning for the Prevention of Healthcare-Associated Infections
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