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Hall KK, Shoemaker-Hunt S, Hoffman L, et al. Making Healthcare Safer III: A Critical Analysis of Existing and Emerging Patient Safety Practices [Internet]. Rockville (MD): Agency for Healthcare Research and Quality (US); 2020 Mar.

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Making Healthcare Safer III: A Critical Analysis of Existing and Emerging Patient Safety Practices [Internet].

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5Infections Due to Other Multidrug-Resistant Organisms

, M.H.S., , M.P.H., and , M.D., M.S.

Introduction

Background

Multidrug-resistant organisms (MDROs) are microorganisms, mainly bacteria, that are resistant to one or more classes of antimicrobial agents.1 These include methicillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant Enterococci species (VRE), carbapenemase-producing Enterobacteriaceae, and Gram-negative bacteria that produce extended spectrum beta-lactamases (ESBLs). These last two types of pathogens produce chemicals that allow them to resist the effect of certain antimicrobials, and this adaptation is easily passed between different species.

Other species of note include MDR Escherichia coli and Klebsiella pneumoniae, Acinetobacter baumannii (abbreviated AB; some strains are resistant to all antimicrobial agents), and organisms such as Stenotrophomonas maltophilia that are intrinsically resistant to the broadest-spectrum antimicrobial agents.1 MDROs’ resistances limit treatment options for patients, making infection critical to preventing further harms.

Importance of Harm Area

The World Health Organization (WHO) now recognizes that MDROs are a growing threat in every geographic region of the world.2 Drug-resistant bacteria pose a significant public health risk both domestically and abroad due to their ability to colonize individuals without causing symptoms, their endurance in the environment, and the clinical threat they pose.3 The growing presence of resistant microbes is of particular concern for vulnerable patients, such as those who have received organ transplantation, those with cancer, preterm infants, and immune-suppressed and other medically vulnerable individuals.2

With treatment complicated by the limited availability of antimicrobials to treat these infections, MDROs are responsible for approximately 23,000 deaths annually from antibiotic-resistant pathogens in the United States alone.4 The Centers for Disease Control and Prevention (CDC) (2018) states that 11 percent of individuals screened in healthcare facilities are asymptomatic carriers for a transmissible, “hard-to-treat” microorganism.5

Drug-resistant organisms are becoming increasingly present in all settings and geographic areas. As cited in Tacconelli et al. (2014), carbapenem resistance increased in five European countries from 2008 to 2011.6 In the United States, infections caused by multidrug-resistant, Gram-negative bacteria have increased over the past decade, and one out of five hospitals reporting invasive infections implicated a carbapenem-resistant K. pneumoniae, one of the most common MDROs.6 While rates of hospital-onset, MRSA-related bacteremia in the United States have declined, community-onset MRSA-related bacteremia has increased in recent years.7

The patient safety practices (PSPs) in this report have universal application for reducing the burden of colonization and infection. When differences are significant (e.g., Enterococci in the digestive tract vs. S. aureus on patient skin), we make a note in the findings. The large benefit of these practices, however, comes from this universality: whether the organism is an extremely drug resistant A. baumannii or methicillin-susceptible S. aureus, infection prevention reduces risks and prevents patient harms.

Methods for Selecting PSPs

To determine the optimal methods for controlling MDROs and preventing MDRO-related infection, we reviewed CDC guidelines8 and the compendium of strategies from the Society for Healthcare Epidemiology of America.9,10 Using these systematic reviews and reports, we developed an initial list of 23 PSPs that target diagnostic errors, and the Technical Expert Panel, Advisory Group, and AHRQ reviewed it.

Based on the reviewers’ recommendations, we identified six priority PSPs:

  • Chlorhexidine bathing to control MDROs
  • Hand hygiene to reduce MDRO transmission
  • Active surveillance strategies for MDROs
  • Environmental cleaning and disinfection strategies
  • Minimizing exposure to invasive devices and reducing device-associated MDRO risks
  • Communication of patients’ MDRO status

What’s New/Different Since the Last Report

The previous Making Health Care Safer reports included recommendations for infection control practices, including multicomponent interventions for device-associated infections as well as general infection prevention. In this report, we focus on the evidence for those practices (and some new practices) to reduce the transmission of and infections caused by MDROs.

As noted in previous Making Health Care Safer reports, the epidemiology of MRSA, VRE, and other MDROs has continued to evolve; this report updates the literature with responses to that emerging, evolving resistance in the following ways:

  • Chlorhexidine bathing is a practice that can be combined with others (such as active surveillance and contact precautions) in response to MDRO outbreaks or added to routine patient bathing to control MDROs and prevent infection. Current guidelines focus mainly on acute care populations, especially critical care. In this report, we include studies of non-critical care populations and some studies on chlorhexidine in community settings. This review also includes information on chlorhexidine resistance and important considerations when adding chlorhexidine bathing to routine patient care.
  • Hand hygiene is a universal strategy for preventing transmission of MDROs and MDRO-related infection, regardless of patient care risk factors. This review also includes new findings on the role of patient hand hygiene and mathematical models to measure the impact of hand hygiene (in combination with other PSPs or alone).
  • For active surveillance, this review looks at specific strategies for identify MDRO-infected and MDRO-colonized patients, particularly active surveillance cultures/testing of patients and their environment, to prevent MDRO transmission.
  • Environmental cleaning is a new practice in this report, and our review focuses both on the efficacy of different cleaning products and strategies to ensure thorough cleaning.
  • Many practices and resources for minimizing the risk of harm due to device use were covered in the previous version of Making Health Care Safer; this review includes updated literature and any additional resources since that publication was written.
  • Finally, communicating patients’ MDRO status (also new in this report) allows facilities to take appropriate infection prevention precautions from the start of the patient encounter. This report provides evidence on the negative effects of missed communication and some examples of communication strategies.

References for Introduction

1.
Siegel JD, Rhinehart E, Jackson M, Chiarello L. Management of multidrug-resistant organisms in healthcare settings, 2006. Atlanta, GA: Centers for Disease Control and Prevention; 2006. https://www​.cdc.gov/infectioncontrol​/guidelines/mdro/index​.html.
2.
Chan M. Ten Years in Public Health, 2007–2017: A Global Health Guardian: Climate Change, Air Pollution and Antimicrobial Resistance. Geneva: World Health Organization; 2017. https://www​.who.int/publications​/10-year-review​/chapter-guardian.pdf?ua=1.
3.
Palmore TN, Henderson DK. Managing transmission of carbapenem-resistant Enterobacteriaceae in healthcare settings: A view from the trenches. Clin Infect Dis. 2013;57(11):1593–9. doi: 10.1093/cid/cit531. [PMC free article: PMC3888298] [PubMed: 23934166] [CrossRef]
4.
Trick WE, Lin MY, Cheng-Leidig R, et al. Electronic public health registry of extensively drug-resistant organisms, Illinois, USA. Emerg Infect Dis. 2015;21(10):1725–32. doi: 10.3201/eid2110.150538. [PMC free article: PMC4593443] [PubMed: 26402744] [CrossRef]
5.
Centers for Disease Control and Prevention. Containing Unusual Resistance. CDC Vital Signs. Atlanta, GA: April 2018. https://www​.cdc.gov/vitalsigns​/pdf/2018-04-vitalsigns.pdf.
6.
Tacconelli E, Cataldo MA, Dancer SJ, et al. ESCMID guidelines for the management of the infection control measures to reduce transmission of multidrug-resistant Gram-negative bacteria in hospitalized patients. Clin Microbiol Infect. 2014;20: Suppl 1:1–55. doi: 10.1111/1469-0691.12427. [PubMed: 24329732] [CrossRef]
7.
Kourtis AP, Hatfield K, Baggs J, et al. Vital signs: Epidemiology and recent trends in methicillin-resistant and in methicillin-susceptible Staphylococcus aureus bloodstream infections - United States. MMWR Morb Mortal Wkly Rep. 2019;68(9):214–9. doi: 10.15585/mmwr.mm6809e1. [PMC free article: PMC6421967] [PubMed: 30845118] [CrossRef]
8.
Centers for Disease Control and Prevention. Interim Guidance for a Public Health Response To Contain Novel or Targeted Multidrug-Resistant Organisms (MDROs) Atlanta, GA: Centers for Disease Control and Prevention; January 2019. https://www​.cdc.gov/hai​/pdfs/containment​/Health-Response-Contain-MDRO-H.pdf.
9.
Yokoe DS, Anderson DJ, Berenholtz SM, et al. A compendium of strategies to prevent healthcare-associated infections in acute care hospitals: 2014 updates. Infect Control Hosp Epidemiol. 2014;35(8):967–77. doi: 10.1086/677216. [PMC free article: PMC4223864] [PubMed: 25026611] [CrossRef]
10.
Calfee DP, Salgado CD, Milstone AM, et al. Strategies to prevent methicillin-resistant Staphylococcus aureus transmission and infection in acute care hospitals: 2014 update. Infect Control Hosp Epidemiol. 2014;35(7):772–96. doi: 10.1086/676534. [PubMed: 24915205] [CrossRef]

5.1. PSP: Chlorhexidine Bathing To Control MDROs

Authors

Sam Watson, M.H.A.

Key Findings

  • The strongest evidence supports using chlorhexidine bathing to reduce colonization and infection, particularly by multidrug—resistant Gram-positive bacteria (MDR-GPB) such as MRSA and VRE, and for healthcare-associated infections (HAIs) related to medical devices that create a break in the skin (e.g., central lines).
  • Less evidence is available to support chlorhexidine bathing for preventing infection from MDR Gram-negative bacteria (MDR-GNB), such as carbapenem-resistant Enterobacteriaceae (CRE), and for other types of HAIs.
  • As an intervention, chlorhexidine is low cost to implement (especially if routine bathing is already in place) and generally well received by staff, but compliance with bathing can wane over time.
  • While the literature has not described any clinical effects of chlorhexidine resistance, this practice should continue to be monitored.

Chlorhexidine solutions have broad antimicrobial activity and are already commonly in use as topical disinfectants and antiseptics as part of recommended strategies for MDRO control and infection prevention.13 Either universal or targeted chlorhexidine bathing can complement other infection control methods of screening, isolation, and eradication.4

This chapter examines specific efficacy of chlorhexidine to prevent different infections (by organism, by type of infection), the mode and frequency of successful chlorhexidine bathing for disease prevention, and considerations for or unintended consequences of general chlorhexidine use. The review’ key findings are located in the box to the right.

5.1.1. Practice Description

For the purpose of this review, we define “chlorhexidine bathing” as application of chlorhexidine to the skin or oropharyngeal surfaces to promote decolonization and to prevent infection. As described below, oropharyngeal surfaces represent a reservoir for MDROs in mechanically ventilated patients who cannot perform their own oral care. Since chlorhexidine bathing is recommended for patients at high risk for MDRO-related infections—generally intensive-care patients, many of whom may be mechanically-ventilated as part of their care—we include oral care as part of a chlorhexidine bathing routine.3

5.1.2. Methods

To investigate the current literature for chlorhexidine bathing—for which patients, in what form, how often, and with what effectiveness—we searched three databases (CINAHL, MEDLINE, and Cochrane) for a combination of the keywords “chlorhexidine bathing” and MeSH terms related to “cross infection prevention,” “drug resistance, multiple, bacterial,” and “drug resistance, microbial.” Articles from 2008 through December 31, 2018, were included. (Any relevant articles published after the original search are included in the PRISMA diagram as additional sources.)

The initial search yielded 323 results (including 6 articles from other sources); after duplicates were removed, 300 were screened for inclusion, and 124 full-text articles were retrieved. Of those, 42 were selected for inclusion in this review. Articles were excluded if they did not mention chlorhexidine’s role in preventing MDROs, mentioned a PSP other than bathing, or discussed use of chlorhexidine outside the healthcare environment. Chlorhexidine oral care was included in this review, as were in vitro studies that assessed the impact of chlorhexidine use on the selection or development of resistant organisms.

General methods for this report are described in the Methods section of the full report.

For this patient safety practice, a PRISMA flow diagram and evidence table, along with literature-search strategy and search-term details, are included in the report appendixes A through C.

5.1.3. Review of Evidence

One of the aims of this review is to better understand the nuances of chlorhexidine’s efficacy for controlling and preventing infection caused by MDROs.

The questions of interest for this review are: Which chlorhexidine applications are most effective for decolonization and for infection control, against which organisms is chlorhexidine the most effective, and what are the potential outcomes related to chlorhexidine resistance? Further, which patients benefit the most from chlorhexidine bathing?

Many of the studies included in this report and in systematic reviews focus on intensive care unit (ICU) patients, who have the most risk factors for MDRO colonization and infection. While these patient populations show benefits in terms of reduced colonization, carriage, and infection, the studies that include relatively healthy populations (both in community and hospital settings) show more nuanced results without a clear benefit.

The studies summarized in this section include several well-designed, rigorous studies, some of which have very large populations (tens or hundreds of thousands). When findings are nuanced, we note where limitations may have contributed a null finding or if mediating factors showed benefit for one subgroup but not the whole population.

This summary indicates the best-supported uses of chlorhexidine and the level of evidence for other uses. Section 5.3.4 provides a list of resources for implementing chlorhexidine bathing protocols. Where the evidence is not definitive, such as using chlorhexidine bathing to prevent infection for relatively healthy patient populations or reduce MDROs in community settings, we hope this review will help clinical staff make their own determination on implementing chlorhexidine bathing.

5.1.3.1. Efficacy for Controlling MDROs and Preventing Infection

In the sections below, we summarize the clinical results of chlorhexidine bathing for major MDROs (MRSA, VRE, CRE), HAIs, and other results. This summary is accompanied by a table that briefly describes the supporting evidence for each section. Additional information can be found in the Chlorhexidine Bathing Evidence Table (see Appendix B).

5.1.3.1.1. MRSA

Evidence suggests that chlorhexidine bathing in the hospital setting reduces MRSA acquisition and carriage but may not always result in fewer MRSA infections. Three systematic reviews found evidence that chlorhexidine bathing alone reduces MRSA acquisition and carriage.57 This finding is supported by five strong studies (four experimental, one quasi-experimental) that also found chlorhexidine bathing reduced MRSA carriage and acquisition.812 While most of these studies found that bathing also reduced MRSA infections, Derde and colleagues’ review (2012) included some studies that found no significant reduction in infections.6

One prospective cohort study found no reduction in MRSA colonization rates, specifically, but did find a significant reduction in the rates of infections caused by all MDROs (measured in aggregate, not by specific MDRO).13 Interpreting these results is made more difficult by the fact that chlorhexidine bathing is recommended as part of a multicomponent strategy that includes nasal mupirocin and, in a few studies, oral antibiotics, as described in general MDRO and MRSA control guidelines.3,14

In long-term care facilities, Peterson and colleagues’ cluster-randomized study (2016) demonstrated that a thorough decolonization protocol that includes chlorhexidine bathing can reduce MRSA colonization without the need for patient isolation.12 This is an important finding for implementation, because extended patient isolation and gown and glove use may not be feasible or desirable in long-term or residential care settings.

Table 5.1 below presents the results from each study.

Table 5.1. Summary of MRSA Results.

Table 5.1

Summary of MRSA Results.

5.1.3.1.2. VRE

Several studies found evidence that chlorhexidine can reduce VRE acquisition and colonization. One rigorous, multicenter study found that chlorhexidine bathing can reduce VRE acquisition.8 Three systematic reviews found that chlorhexidine can reduce VRE carriage in hospital patients.57 Finally, two quasi-experimental studies found reduced VRE colonization among patients who were bathed daily with chlorhexidine, and the Mendes and colleagues study (2016) additionally observed reduced VRE infections.11,15 Table 5.2 below presents the results from each study.

Table 5.2. Summary of VRE Results.

Table 5.2

Summary of VRE Results.

5.1.3.1.3. CRE

Few studies directly addressed chlorhexidine effects on CRE specifically (a number focused on the larger category of MDR-GNB). Of those that did, two observational cohort studies found that chlorhexidine bathing could reduce CRE colonization.13,16 Table 5.3 below presents the results from each study.

Table 5.3. Summary of CRE Results.

Table 5.3

Summary of CRE Results.

5.1.3.1.4. HAIs

Many studies examined the effect of chlorhexidine bathing on rates of various HAIs, such as catheter-associated urinary tract infection (CAUTI), ventilator-associated pneumonia (VAP)g, and central line-associated blood stream infection (CLABSI). Where possible, we specify whether all infections or MDRO-only infections are noted in the results, but not all studies provided that level of detail. Based on the studies included, chlorhexidine bathing is most effective at reducing colonization by and HAIs from Gram-positive MDROs in patients who have a break in the skin due to a needed medical device (e.g., central line). Table 5.3 and the paragraphs below summarize these findings.

One review and several studies, including two large studies (Huang et al., 2013, and Huang et al., 2019) with more than 10,000 patients and 400,000 patients, respectively, have found evidence that chlorhexidine bathing can reduce the risk of HAIs, especially in intensive care units.9,10 Huang and colleagues’ 2013 REDUCE MRSA trial found universal decolonization involving daily chlorhexidine bathing throughout the patient’s entire ICU stay and twice-daily intranasal mupirocin for 5 days was more effective than targeted decolonization or screening and isolation in reducing MRSA-positive clinical cultures and all-cause bloodstream infections.10

In a subsequent study (the ABATE Infection trial, 2019), Huang et al. evaluated the impact of universal chlorhexidine bathing and targeted mupirocin use for MRSA carriers in non-ICU settings.9 The authors found that the intervention did not significantly reduce MRSA- or VRE-positive clinical cultures for the overall study population. In a post-hoc analysis, patients with medical devices (including central lines, midline catheters, and lumbar drains) were found to experience a significantly greater benefit from the intervention.

Similarly, Denny and Munroe’s systematic review (2017) found the strongest evidence for reducing surgical site infection (SSI) and CLABSI rates, as well as acquisition, colonization, and infection for MRSA and VRE.5 Among ICU patients, Climo and colleagues’ 2013 study found a significant reduction in CLABSIs (the only HAI outcome included in that study).8 As mentioned above, only a few studies included in this review examined chlorhexidine bathing for CRE, and only one, Abboud and colleagues’ observational cohort study (2016), looked at CRE-related HAIs. Abboud and colleagues found reductions in those HAIs in CRE-colonized patients after chlorhexidine bathing was implemented.16

While some studies did not show an effect of chlorhexidine bathing on HAIs, most of these studies were considerably smaller than the two studies by Huang and colleagues. A rigorous cluster-randomized trial by Noto and colleagues (2015) found no impact on CLABSI, CAUTI, VAP, or Clostridioides difficile infection rates among the 9,340 patients in the study.17 Ruiz et al. (2017) reduced MDRO colonization with chlorhexidine wipes, but this did not lead to a reduction in HAIs in their single-site study. Ruiz and colleagues also noted that longer ICU stays (in one Spanish hospital) were associated with overall incidence of HAIs, suggesting that chlorhexidine bathing alone was not sufficient to reduce the infection risk posed by extended stays in intensive care.13

Two studies directly compared the use of chlorhexidine bathing against bathing with soap and water, finding no improvement in HAI rates when chlorhexidine was used. Kengen et al.’s study of 6,634 ICU patients (2016, Australia) found no statistically significant difference in HAIs when patients received daily bathing with chlorhexidine instead of soap and water.18

Similarly, Boonyasiri and colleagues’ smaller study of 418 Thai ICU patients (2016) found no benefit to chlorhexidine bathing over soap and water bathing on HAI rates in environments where most HAIs were caused by MDR-GNB.19 However, Camus and colleagues (2014) reduced HAIs from MDR-GNB by adding mupirocin application to chlorhexidine bathing.20

Most studies of chlorhexidine for HAI prevention focused on BSIs, but a few looked at VAP and SSIs. Duszynska and colleagues’ observation study (2017) also found no reduction in intubation-related pneumonia, nor in UTIs, although overall infections and catheter-related infections were significantly lower.21 A randomized trial of oropharyngeal decontamination using chlorhexidine found no effect on reduced BSIs from MDR-GNB in mechanically ventilated patients.22

Although chlorhexidine is routinely used for preoperative antisepsis in surgical settings, Abboud and colleagues (2016) found no supporting literature that chlorhexidine bathing reduced SSIs (although they did observe a reduction in SSIs among CRE-colonized patients in their study).16 In their systematic review, Denny and Munroe (2017) did not find clear evidence of the efficacy of chlorhexidine bathing for preventing SSIs.5

Finally, Urbanic and colleagues (2018) raise an important limitation that applies to all these studies: because of other HAI prevention initiatives, the absolute number of HAIs is, in some cases, very low.23 The number needed to treat with chlorhexidine bathing in order to significantly reduce HAIs may be, in some cases, larger than the number of patients enrolled in studies. This finding suggests that chlorhexidine bathing has limited benefit for HAI reduction in settings where HAIs are already well controlled by other means.

Table 5.4 below presents the results from each study.

Table 5.4. Summary of HAI Results.

Table 5.4

Summary of HAI Results.

5.1.3.1.5. Other Results

This section summarizes other relevant results that do not fall under the categories above. Most of these studies focused on MDRO generally or MDR-GNB specifically. The studies we reviewed do not support chlorhexidine use but also do not warrant a recommendation against using it for MDR-GNB, although it may not be the most effective precaution for those organisms. Table 5.5 below presents the studies and their results.

None of the systematic reviews recommended chlorhexidine bathing for preventing/reducing MDR-GNB colonization.6,7,24 One review (Tacconelli et al., 2014) found only temporary decolonization of MDR-GNB using chlorhexidine, and one randomized, open-label controlled trial (Boonyasiri et al., 2016) found that chlorhexidine bathing offered no reduction or delay in MDR-GNB acquisition.19,24 Kengen and colleagues’ retrospective time study (2018) found no difference in MDRO acquisition with chlorhexidine bathing compared with soap and water, whereas Ruiz and colleagues (2017) saw a reduction in MDRO acquisition, including MDR-GNB.13,18

Musuuza and colleagues’ pre-post study (2017) found lower colonization with MDR-GNB (specifically, fluoroquinolone-resistant GNB) after chlorhexidine bathing, but Mendes and colleagues’ quasi-experimental observational study (2016) did not.15,25 Maxwell and colleagues (2017) found no difference between chlorhexidine and soap bathing for lowering MDRO infection rates (from GNB or GPB).26 Pedreira and colleagues (2009) observed no reduction in MDRO colonization rates when chlorhexidine was added to standard oral care (toothbrushing) in pediatric ICU patients.27

Table 5.5. Summary of Other Results.

Table 5.5

Summary of Other Results.

5.1.3.2. Process Outcomes

5.1.3.2.1. Application

Chlorhexidine bathing, as described in the literature, covers a range in terms of concentration used, mode of application, and frequency. Of those studies that described the frequency of application (24 of 42), almost all described daily chlorhexidine bathing, with a smaller number using multiple applications per day (4 out of 24, of which one was an oropharyngeal-only application of chlorhexidine).

In terms of concentration, the vast majority of reviews and studies used a 2% chlorhexidine gluconate solution (either in prepackaged wipes or applied using a soaked washcloth). The exception was one oropharyngeal application (Camus et al., 2016) that used a 4% aqueous solution.28 For otherwise healthy patients outside a hospital setting, Whitman and colleagues (2010) found daily bathing with 2% chlorhexidine cloths to be ineffective in reducing soft skin and tissue infection.29 Chlorhexidine’s effectiveness includes prolonged residual disinfection, so it is important not to rinse after use.5

5.1.3.2.2. Adverse Effects

The most common adverse effect in the literature was skin irritation, as seen in one systematic review and several studies.5,10,19 When use of chlorhexidine wipes was discontinued, pruritus stopped. Oral mucosa lesions were observed in 9.8 percent of the 8,665 mechanically ventilated patients in Wittekamp and colleagues’ chlorhexidine mouthwash study (2018).22

More serious adverse effects can occur with exposure to sensitive areas (eyes, esophagus, intestinal lining, inner ear), as noted in one systematic review.5 Severe anaphylaxis is possible but rare (only found in case reports), as reported in reviews by Denny and Munroe (2017).5

5.1.3.3. Economic Outcomes

Only one study (Peterson et al., 2016) addressed the cost of chlorhexidine bathing, which was negligible when chlorhexidine was incorporated into an established daily bathing routine.12 Since staff are already accustomed to daily bathing, no additional time is required, and the only potential cost is the difference between chlorhexidine supplies and previous bathing solutions.

5.1.3.4. Evaluations of Chlorhexidine Resistance

The most important unintended consequence of the wide use of chlorhexidine is the development of resistance to chlorhexidine and other biocides.30 None of the MDROs in the studies in this review showed biocide resistance at the concentrations typically used for chlorhexidine bathing; the in vitro studies compared survivability of resistant MDROs in low concentrations of chlorhexidine. An equal number of studies supported or refuted the hypothesis that chlorhexidine bathing increases the prevalence of resistance genes in hospitals; however, many of these studies looked at isolates from a single hospital and may have limited generalizability. Regardless of changes in prevalence, these authors hypothesize that overdiluted concentrations or residual chlorhexidine may be selecting for resistant organisms (either resistant clones/strains or organisms less susceptible to chlorhexidine) and should be monitored for clinical impact.3133

5.1.3.4.1. In Vitro Studies

Resistance to chlorhexidine is detected by observing higher minimum inhibitory concentrations (MICs) to inhibit bacterial growth and higher minimum bactericidal concentrations (MBCs) to eliminate the organisms. One Scottish and one U.S. study found chlorhexidine resistance to be more common in settings where chlorhexidine bathing was routine.34,35 In one in vitro study of MDRO isolate cultures from U.S. ICUs with and without daily bathing, Suwantarat and colleagues (2014) found that hospital ICU units that bathed patients were more likely to have CLABSI-causing organisms that could withstand higher levels of chlorhexidine (compared with units that did not conduct bathing).35

Hijazi and colleagues’ (2016) in vitro study of samples collected over 7 years from Scottish ICUs found that implementing chlorhexidine bathing increased the prevalence of resistance genes in those organisms.34 One retrospective cohort study in the United States found no conclusive trends in the prevalence of chlorhexidine-resistant MDROs after implementing chlorhexidine bathing, but the authors hypothesize that some increases may be due to readmitted patients who were unsuccessfully decolonized in previous hospitalizations.36

McNeil and colleagues’ study of S. aureus in a U.S. pediatric hospital environment (2014) showed that organisms with resistance genes had MICs twice as high and MBCs 8 to 16 times as high as the more susceptible organisms (p<0.005).37 However, several studies found that prevalence of resistance genes did not always result in measurable resistance. One in vitro study of cultures from an ICU after implementing chlorhexidine bathing found that resistance genes were linked to higher MICs in one MRSA strain but not another.38

Similarly, Musuuza and colleagues’ pre-post study (2017) did not show increased MICs in MRSA and fluoroquinolone-resistant GNB after a daily bathing intervention in their U.S. hospital.11 While not genetically resistant, oral MRSA biofilms studied in vitro by Smith and colleagues (2013) show considerable resistance to chlorhexidine mouthwashes, which may account for failure of mouth washing to prevent VAP and for frequent MRSA recolonization.39

5.1.3.4.2. Clinical Implications

The clinical impact of chlorhexidine resistance genes is unclear. One in vitro study of MRSA isolates in a U.S. hospital found that MRSA strains showed more resistance to chlorhexidine than methicillin-susceptible strains.40 Similarly, Alotaibi and colleagues (2017) found more chlorhexidine resistance in VRE than in vancomycin-susceptible Enteroccoci strains in isolates from Danish hospitals.41 Hayashi and colleagues (2017) found that A. baumanii epidemic strains from Japanese isolates showed increased resistance to chlorhexidine in vitro but not at concentrations typically used for disinfection.42

Two studies found evidence that might suggest that chlorhexidine bathing can favor chlorhexidine-resistant MDROs (particularly MDR-GNB) by eliminating the “competition” from chlorhexidine-susceptible MDROs. Abboud and colleagues (2016) found an increase in colonization with Pseudomonas aeruginosa and A. baumanii after chlorhexidine bathing was implemented in a Brazilian hospital ICU.16 However, Camus and colleagues (2016, France) found no increase in MDR-GNB after implementation of a multicomponent chlorhexidine bathing intervention for ventilated patients that also included oral care, mupirocin ointment, and oral antibiotics.28 In that study, however, it is unclear what effect the additional components, particularly mupirocin ointment use, had on MDR-GNB rates. Cho and colleagues (2018) and McNeil and colleagues (2014) also found that chlorhexidine resistance genes were associated with mupirocin resistance in both South Korean and U.S. isolates; this finding may be due to the frequent combination of chlorhexidine and mupirocin in hospitals’ decolonization strategies.37,43

Importantly, no studies suggested that chlorhexidine bathing was ineffective due to resistance; at the concentrations typically used (1–4%), chlorhexidine still kills even the most resistant organisms. However, overdiluted solutions may fail to kill organisms as intended and create unwanted transmission and infection, especially in cases where biofilms have formed.

5.1.3.4.3. Alternatives to Chlorhexidine

Several of the studies mentioned above examined multiple biocides and alternatives to chlorhexidine. Some alternatives, such as triclosan and hydrogen peroxide, have their own risk of resistance selection, as detailed in Wesgate and colleagues’ in vitro study (2016).44 Grare and colleagues’ (2010) in vitro study shows the effectiveness of alternative cationic compoundsh that show promising effectiveness against MDROs, but it will be some time before these products are commercially available.45

5.1.4. Implementation

As described above, the most common frequency of chlorhexidine bathing was daily, and the most common application was a 2% chlorhexidine gluconate solution, either in prepackaged wipes or in soaked washcloths. One important aspect of chlorhexidine use is to allow long-term contact with the skin. Ekizoğlu and colleagues (2016) recommended a contact time of at least 5 minutes, and no-rinse applications can further take advantage of chlorhexidine’s persistent antimicrobial effects on the skin.31 DeBaun and colleagues’ in vitro study of MRD isolates (2008) suggests that extreme dilutions (between 1:2,048 and 1:8,192) of chlorhexidine may still be effective against MRSA and A. baumanii, but such extreme dilutions may not always be sufficiently bactericidal or inhibitory for resistant organisms (as discussed above under chlorhexidine resistance).46

Chlorhexidine can be successfully used for MRSA decontamination, when combined with mupirocin and active surveillance.6 However, the effectiveness of decolonization for otherwise healthy populations is unclear. While Whitman and colleagues (2010) successfully reduced skin and soft tissue infections in healthy populations by instituting daily bathing with 2% chlorhexidine-impregnated clothes, Huang and colleagues (2019) did not find benefits to introducing chlorhexidine in a non-critical care hospital setting.9,29

Interestingly, a study by Fritz and colleagues (2012) found that a household intervention of S. aureus decolonization and personal care hygiene (i.e., relegating personal care items to a single individual and frequent, hot-water washing of linens and towels) reduced skin and soft tissue infections in household members but not the index case patients. Fritz et al. hypothesized that the acquisition of new S. aureus strains may put someone at higher risk for infection, rather than simply being colonized; 20 percent of the index patients (pediatric patients with a skin or soft tissue infection) were not colonized with S. aureus at screening, despite having an S. aureus culture from the infection site.47

5.1.4.1. Barriers and Facilitators to Implementation

In general, daily chlorhexidine bathing is a low-cost strategy that is well received by staff. Chlorhexidine bathing also has the advantage of being easy and quick to implement, as noted by Huang and colleagues (2013).10 Two studies found that the staff responsible for implementing a chlorhexidine bathing intervention rated chlorhexidine bathing positively (Boonyasiri et al., 2016; Duszynska et al., 2017), and Huang and colleagues noted high rates of compliance (over 80%) in their MRSA decolonization study (2013).10,19,21 However, Musuuza and colleagues (2017) noted that compliance can wane over time.11

In a survey of Thai hospitals, Apisarnthanarak and colleagues (2017) found that good leadership support for an infection control program was statistically significantly associated with regular use of chlorhexidine bathing (that is, hospitals without that support were less likely to use chlorhexidine bathing).48 When facilities implement chlorhexidine bathing, leadership support for infection prevention programs can help sustain compliance with bathing over time.

5.1.4.2. Resources To Assist With Implementation

5.1.5. Gaps and Future Directions

As covered in Denny and colleagues’ systematic review (2017), additional research could include5:

  • Studies on the frequency and duration of bathing (how many times a day, for what period);
  • Evaluations of chlorhexidine bathing’s role in multicomponent programs (also suggested in commentary by Horner et al., 2012)49; and
  • Continued research on chlorhexidine resistance and related clinical outcomes, especially the role of biofilms (as noted in commentary by Grascha, 2014) and Gram-negative bacteria (also suggested in commentary from Strich & Palmore, 2017).50,51

Although none of the studies included in this report indicated negative clinical outcomes due to chlorhexidine resistance, commentary by Kampf (2016) cautions against use of chlorhexidine for general, nonspecific applications such as hand hygiene or instrument soaking, where insufficient concentrations are more likely to occur.52 Further studies to prevent these vulnerabilities in chlorhexidine bathing would be valuable to establishing bathing protocols.

References for Section 5.1

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Alotaibi SMI, Ayibiekea A, Pedersen AF, Jakobsen L, Pinholt M, Gumpert H, et al. Susceptibility of vancomycin-resistant and -sensitive Enterococcus faecium obtained from Danish hospitals to benzalkonium chloride, chlorhexidine and hydrogen peroxide biocides. J Med Microbiol. 2017;66(12):1744–51. doi: 10.1099/jmm.0.000642. [PubMed: 29134935] [CrossRef]
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5.2. PSP: Hand Hygiene To Reduce MDRO Transmission

Authors

Editors: Andrea Hassol, M.S.P.H. and Sam Watson, M.H.A.

Key Findings

  • Hand hygiene is indispensable for preventing the transmission of MDROs. Hand hygiene compliance and compliance with other PSPs are complementary: high compliance with one practice is associated with high compliance with others.
  • The World Health Organization’s “My Five Moments for Hand Hygiene” was recommended or used by many studies in this review as the most effective tool for improving hand hygiene compliance, but many effective campaign materials are available.
  • Staff can make existing campaigns even more effective by personalizing the implementation with educational and promotional materials and supporting each other in observing hand hygiene.
  • The biggest barriers to hand hygiene compliance are: (1) realizing an opportunity for hand hygiene is occurring and (2) remembering to complete hand hygiene protocol, consistently, at every opportunity. Education can help with the first, and direct observation with immediate feedback helps improve the second.

Hand hygiene is one of the most fundamental and cost-effective infection control practices.1 Yet despite over 150 years of efficacy evidence, hand hygiene opportunities continue to be missed in healthcare settings, with hand hygiene rates of only 40 to 60 percent in intensive care settings.2 Johnston and Bryce (2009) identified several factors that support or impede hand hygiene compliance: environmental factors (making handwashing supplies accessible and convenient), individual factors (whether the person believes in the need for handwashing at the indicated opportunities), and organizational factors (whether a person’s workflow allows proper handwashing to take place).3

The reasons for these missed opportunities are complex: patient care workload and limited time; inadequate staff education or knowledge about transmission risk; lack of convenient, accessible cleaning products and sinks; and even awareness that an opportunity for hand hygiene is occurring. In a nonsystematic review, Otter et al. (2013) found that although several MDROs (notably, A. baumannii) are known to contaminate the patient environment and survive on dry surfaces, healthcare personnel are less likely to conduct hand hygiene after environmental contact than after patient contact.4 In addition, long artificial or natural nails can harbor harmful organisms, as can rings worn during care.57

New technology in the healthcare setting can aid hand hygiene (such as “smart badges” that remind staff to clean hands), but technological changes to workflow also introduce new hand hygiene opportunities (such as the use of personal cell phones in the clinical setting, as studied in Graveto and colleagues’ 2018 review).8 Hand hygiene interventions are generally well received and inexpensive to implement, and they align with medicine’s principle of “first do no harm.”9 Several studies in this review demonstrate that it is possible to achieve very high rates of hand hygiene compliance. We include lessons learned from those studies for consideration when seeking to not just achieve but maintain those very high rates. The review’s key findings are located in the box above.

5.2.1. Practice Description

Hand hygiene, as defined by the Centers for Disease Control and Prevention (CDC), is “cleaning your hands by using either handwashing (washing hands with soap and water), antiseptic hand wash, antiseptic hand rub (i.e., alcohol-based hand sanitizer including foam or gel), or surgical hand antisepsis.”i In this review, we include evidence-supported methods for disinfecting the skin of hands by using a cleaning solution (with or without water), with or without concurrent use of medical gloves. (This chapter does not focus on glove use.)

5.2.2. Methods

To investigate the role of hand hygiene in preventing transmission of MDROs and containing MDRO outbreaks, we searched three databases (CINAHL, MEDLINE, and Cochrane) for a combination of the keywords “hand hygiene,” “hand disinfection,” “hand sanitization,” and “hand washing,” as well as MeSH terms “cross infection prevention,” “drug resistance, multiple, bacterial,” and “drug resistance, microbial.” Articles from January 1, 2008, through December 31, 2018, were included. (Any relevant articles published after the original search are included in the PRISMA diagram as additional sources.)

The initial search yielded 225 results (including 11 articles from other sources); after duplicates were removed, 207 were screened for inclusion, and 168 full-text articles were retrieved. Of those, 17 were selected for inclusion in this review. Articles were excluded if they did not mention hand hygiene’s role in preventing MDRO transmission, described gown and glove use without also mentioning handwashing or hand disinfection, or did not include implementation in a healthcare setting. Outbreak response case studies are included in this review if they describe the role of hand hygiene in ending the outbreak.

General methods for this report are described in the Methods section of the full report.

For this patient safety practice, a PRISMA flow diagram and evidence table, along with literature-search strategy and search-term details, are included in the report appendixes A through C.

5.2.3. Review of Evidence

Consistent hand hygiene at all opportunities in patient care is essential, since MDROs can be acquired from contact with a colonized patient or contaminated surface and transferred to new patients or surfaces.6,9 In their systematic review of prevention for MDR Gram-negative bacteria (MDR-GNB), Tacconelli and colleagues (2014) strongly recommend correct hand hygiene before and after patient contact, as well as before and after contact with the patient environment, regardless of gown and glove use.6 Even in facilities where hand hygiene compliance rates are high (above 80%), outbreaks can be opportunities to achieve near-perfect compliance. Palmore and Henderson (2013) note, however, that compliance will eventually return to baseline levels after an outbreak ends, highlighting the challenge of sustaining universal hand hygiene.10

Of the 17 studies and reviews included in this report, 5 studies and 1 review explicitly examined the causal relationship between better hand hygiene compliance and reduced MDRO transmission. An additional four studies used mathematical models to estimate the role of hand hygiene in multicomponent MDRO prevention strategies. Two studies looked at the role of patient hand hygiene in preventing MDROs, one study reviewed hand hygiene costs and cost savings (due to infection prevention), and one review looked at hand hygiene opportunities related to cell phone use. Finally, two reviews and one study looked at factors influencing hand hygiene and best practices for increasing compliance.

5.2.3.1. Reducing MDRO Rates Through Hand Hygiene

Four studies found that improved hand hygiene reduced MDRO transmission and one found that the association between hand hygiene and reduced MDRO transmission varied by MDRO, as summarized in the table below. One review by Taconnelli et al. (2014) did not provide statistical findings but recommended hand hygiene for MDR-GNB based on the evidence of frequent hand contamination during patient care, MDRO survivability on hands, and risk of contamination due to fomites (objects or surfaces that are likely to carry infectious pathogens) in the patient environment.6

Table 5.6 summarizes the findings from studies evaluating the efficacy of hand hygiene for reducing MDRO transmission and infection.

Table 5.6. Summary of Clinical Outcomes of Hand Hygiene Interventions.

Table 5.6

Summary of Clinical Outcomes of Hand Hygiene Interventions.

De la Rosa-Zamboni and colleagues (2018) studied the efficacy of a hand hygiene intervention in a pediatric teaching hospital in Mexico. Alcohol-based hand rubs were placed in every patient unit and periodic education programs were individualized for each group of healthcare workers (attending physicians, nurses, residents, students, and ancillary staff) to highlight the mortality and costs associated with healthcare-associated infections and the evidence about efficacy of hand hygiene. Monthly monitoring and feedback were provided to each group about infection rates and hand hygiene compliance.

Hand hygiene adherence increased from 34.9 percent during the baseline period to 80.6 percent in the last 3 months of the pre-post study. The overall infection rate decreased from 7.54 to 6.46 per 1,000 patient-days (p=0.004), with central line-associated bloodstream infections declining from 4.84 to 3.66 per 1,000 central line-days (p=0.05).11

Sopirala and colleagues (2014) used a hand hygiene program that trained staff nurses in infection control and linked them to infection prevention staff for ongoing monthly education, achieving very high rates of hand hygiene compliance (93%) and reducing MRSA rates by almost half in the pre-post study.12

Pires dos Santos and colleagues (2011) studied multiple strategies to reduce CR-PA infections in a hospital in Brazil. They found that antibiotic stewardship had little impact, but improved hand hygiene (as measured by hospitalwide use of alcohol-based hand rub) was significantly associated with reduced infection rates.13

Vernaz and colleagues (2008) conducted an interrupted time series study of the temporal relationship between increased alcohol-based hand rub use (as part of multicomponent intervention) and reduced MRDOs. The authors established a temporal association between increased alcohol-based hand rub use and reductions in MRSA rates but not C. difficile rates. (This finding is consistent with evidence in this report and in the guidelines reviewed, that alcohol-based hand rubs are not effective for spore-forming bacteria such as C. difficile.)14

Finally, one study of nine hospitals in Australia found that results varied across facility and different MDROs. McLaws and colleagues (2009) found mixed results across the sites included in their pre-post study of hospital regions in Australia. Hand hygiene rates increased in six of the nine hospital systems in the study. For the remaining three hospitals, one had a decrease and the other two had no observed change. Although hand hygiene increased overall, two of four clinical indicators of MRSA infection remained unchanged. The authors concluded that concurrent clinical and infection control practices at different facilities possibly influenced MRSA infection rates and modified the effects of hand hygiene compliance across the different locations.15

5.2.3.1.1. Mathematical Models of Hand Hygiene’s Impact

We reviewed four studies that used mathematical models to estimate the impact of changes in hand hygiene compliance on MDRO acquisition and infection, controlling for the influence of other concurrent infection control or antibiotic stewardship interventions. To create these models, these studies used measurement from an existing facility or ICU; because these were based on single sites, the generalizability of these models may be limited. Still, these models offer examples of how to retroactively assess the effectiveness of individual components of multicomponent interventions, a common challenge given that few hand hygiene compliance programs are implemented without other concurrent practices or programs.16

Barnes and colleagues (2014) simulated scenarios of patient-to-patient transmission via the hands of transiently contaminated healthcare workers to quantify the effects of hand hygiene versus environmental cleaning on rates of MDRO acquisition. For all organisms studied (A. baumannii, MRSA, and VRE), increases in hand-hygiene compliance outperformed equal increases in thoroughness of terminal environmental cleaning. The authors estimated that a 20 percent improvement in terminal cleaning would be required to match the reduction in organism-acquisition achieved by a 10 percent improvement in hand hygiene compliance.17

D’Agata and colleagues (2012) modeled the impact of several distinct strategies for infection control. They found that improved hand hygiene compliance reduced MDRO colonization slightly more than improved compliance with contact precautions. They estimated that a 20 percent increase in hand hygiene compliance reduced colonization between 8 and 12 percent, while a similar 20 percent increase in contact precaution compliance reduced colonization between 6 and 10 percent.9

Harris and colleagues (2017) randomly assigned 20 ICUs to infection control interventions and used the resulting data to understand the relative contribution of the interventions. They found that approximately 44 percent of the subsequent decrease in the MRSA acquisition rate was due to universal glove and gown use, 38.1 percent of the decrease was due to improvement in hand hygiene compliance after exiting patient rooms, and 14.5 percent of the decrease was due to the reduction in physical contacts between healthcare workers and patients.18

Wares and colleagues (2016) modeled transmission in an outpatient dialysis unit and found that even with perfect compliance with hand hygiene, 13.4 percent of patients remained colonized with MDRO. They concluded that although the hands of healthcare workers are among the main vectors of MDRO spread, transmission of MDRO occurs through numerous paths, including a contaminated environment and hospital-acquired colonization.19

5.2.3.1.2. Patient Hand Hygiene

Two studies examined the role of patient hand hygiene in reducing MDROs. Cheng and colleagues conducted two studies in Hong Kong of patient hand hygiene: one pre-post study (2015) in a hospital setting and one cluster-randomized trial (2018) in nursing homes.20,21 In the hospital study, an intervention of single room isolation, strict contact precautions, and directly observed hand hygiene in conscious patients immediately before receiving meals and medications resulted in reduced bacteremia caused by MDR-AB. The rate decreased from 14 cases in 2013 to 1 case in the first 6 months of 2014 (p<0.001).20

In the second study, directly observed hand hygiene was performed in intervention nursing homes at 2-hour intervals during the daytime and before meals and medication rounds. The volume of alcohol-based hand rub used per resident per week was three times higher in the intervention nursing homes than in the controls (p=0.006), suggesting that hand hygiene education was effective in increasing use. Serial monitoring of environmental specimens revealed a significant reduction in MRSA in the intervention versus control nursing homes (13.2 percent vs. 32.8 percent; p<0.001) and a reduction in CR-AB species (9.3 percent vs. 15.7 percent; p=0.001).21

5.2.3.2. Process Outcomes

One study and one guideline review measured factors that can affect the efficacy of hand hygiene interventions. These factors include awareness of the need for hand hygiene in a given opportunity, knowledge of proper hand hygiene technique, and knowledge of what can make hand hygiene less effective even when performed correctly.

Rupp and colleagues’ 2008 crossover trial in two ICUs demonstrated that hand hygiene compliance improved when alcohol-based hand rub was available on the unit. However, no improvement was seen in the rates of device-associated infection, infection due to multidrug-resistant pathogens, or infection due to C. difficile (for which alcohol-based hand rubs are not recommended). In addition, cultures of samples from the hands of nursing staff revealed that an increased number of both microbes and microbe species was associated with longer fingernails, wearing of rings, and lack of access to hand gel.22

Even after hand hygiene is improved, sustainability remains a challenge. In Palmore and Henderson’s outbreak case study (2013), the authors achieved nearly perfect hand hygiene compliance from the hospital’s already-high rate of 85 percent that was sustained for 6 months after the outbreak. However, after that point, the authors observed a return to baseline in the followup period.10

Ongoing observation and feedback are recommended for both increasing and sustaining compliance, but Ellingson and colleagues’ (2014) guideline review notes a few challenges in carrying out this type of measurement and evaluation.16 First, direct observation requires a trained observer, and no current guidelines note how frequently observation should take place to increase or sustain hand hygiene compliance. Indirect measurement can also be done by measuring the volume of hand hygiene solution used, with or without technological solutions such as “smart counters” that track and report dispenser use. These and other technological solutions, such as smart badges that alert remind healthcare personnel about an opportunity for hand hygiene, have programmatic limitations. They may be able to alert on entry/exit but not for contact with surfaces or patients. In addition, there are costs in buying, installing, and maintaining this technology.

5.2.3.3. Economic Outcomes

Hand hygiene promotion programs can be very cost-effective in that they help reduce all infections (not just MDROs). One observational study provided economic findings: Sickbert-Bennett and colleagues studied a large U.S. teaching hospital (2016) before and after implementation of a hospitalwide initiative that included education about hand hygiene and instruction that all staff should provide immediate feedback and reminders to each other.

During the 17-month study period, there was a significant increase in the overall hand hygiene compliance rate (p<0.001) and a significant decrease in the overall HAI rate (p=0.0066). There were 197 fewer healthcare-associated infections and an estimated 22 fewer deaths, for an estimated saving of U.S. $5 million. The authors noted that while infections declined, there was no similar reduction in MDRO infections. They posit that many MDRO infections occur in patients who are colonized before admission to the hospital and cannot be prevented through better hand hygiene.23

5.2.4. Implementation

5.2.4.1. Summary of Evidence on Implementation

When practiced consistently, hand hygiene is an effective tool in reducing MDRO colonization and infections. The challenge is finding cost-effective strategies to increase hand hygiene compliance and sustain it over time. Lee and colleagues’ systematic review (2019) found that, overall, implementing any infection control program reduces HAI rates; however, the greatest reductions come from interventions with multiple, reinforcing components that address:

  • Knowledge (education),
  • Consistency (monitoring and feedback), and
  • Accessibility (providing supplies in places that make sense given the patient care workflow and hand hygiene opportunities).24

Maintaining hand hygiene requires education and culture change, creating workflows that support hand hygiene and technological solutions to automate monitoring and feedback. In some hospital settings, however, the time required for meticulous hand hygiene is a barrier. In their 2017 nonsystematic review, Strich and Palmore point out that if hand hygiene were performed in compliance with WHO guidelines (including 20–30 seconds per hand hygiene episode), each nurse would spend an estimated 58 to 70 minutes on hand hygiene for each patient during a 12-hour ICU shift, which conflicts with patient care duties. They also note that early-generation electronic monitoring systems have had mixed results in improving and sustaining hand hygiene compliance.2

In their guidelines for preventing HAIs through hand hygiene (including MDRO infections), Ellingson and colleagues (2014) recommend direct observation as the primary method for measuring hand hygiene compliance, combined with at least one other measurement method (self-report, technologically-automated tracking) to strengthen measurement against limitations from any single method.16

5.2.4.2. Barriers and Facilitators

Trautner and colleagues (2017) surveyed nursing home staff across 13 States and found large gaps in knowledge about proper hand hygiene procedures. Although all respondents reported receiving training in hand hygiene, less than 30 percent knew the correct length of time to rub hands (28.5 percent of licensed personnel and 25.2 percent of unlicensed personnel understood this fact) or the most effective hand cleaning agent to use (11.7 percent of licensed personnel and 10.6 percent of unlicensed personnel understood).25

One way to address the issue of organizational culture is to personalize a well-supported intervention to promote hand hygiene compliance. Luangasanatip and colleagues’ systematic review (2015) recommends the WHO’s “My Five Moments” intervention for its efficacy in increasing hand hygiene compliance. They also suggest that this intervention is even more effective and sustainable when goal setting, incentive rewards for achievement, and mechanisms to ensure accountability are added.26

A study of general infection prevention practices by Clock and colleagues (2010) found that individuals who adhered to one set of infection control behaviors were likely to adhere to all. They recommend focusing on changing the behaviors of those likely to be systematically noncompliant, such as visitors and staff not directly involved in patient care.27

Several studies in this review addressed compliance by improving access to hand hygiene equipment and supplies. However, if hand hygiene equipment becomes contaminated, the equipment itself can become a source of transmission. As observed by Hota and colleagues (2009) in their CR-PA outbreak response, handwashing sinks increased environmental contamination due to splashing from contaminated drains. In their study of ICU and transplant units, contaminated sink drains were implicated in 36 infections over a 15-month period, by organisms that were phenotypically similar; 17 of these patients died.28

Kotsanas and colleagues’ (2013) investigation of a CR-K. pneumoniae outbreak found that once an MDRO is established in sink drains, it is difficult to eradicate without complete removal and redesign of sinks.29 (Johnson et al., 2018, investigated a 2016 hospital outbreak of Sphingomonas koreensis and identified facility plumbing as a reservoir.30) The authors recommend that preventive efforts focus on appropriate sink design to minimize “spray” and enforcement of clear policies to use designated sinks for hand hygiene only, not for waste disposal. They also recommend frequent surveillance/testing of sink drains and surrounding environment for contamination.

5.2.4.3. Resources To Assist With Implementation

Since hand hygiene has a long, established history of efficacy and implementation, many promotional tools and campaigns have been developed. Below, we present the tools and campaigns described or evaluated in the above studies and reviews.

5.2.5. Gaps and Future Directions

As described in the process outcomes section above, it is important to understand the systemic reasons that hand hygiene is not successfully completed at all opportunities. One of these is awareness that a hand hygiene opportunity is occurring, such as touching contaminated surfaces (as mentioned in Otter and colleagues’ 2013 nonsystematic review).4

Graveto and colleagues’ systematic review (2018) found that in addition to known fomites such as patient linens and healthcare personnel’s clothing, cell phones are frequently used in clinical settings, are often colonized with infectious organisms, and are rarely sanitized.8 While this finding represents a threat to successful hand hygiene, cell phones have important clinical utility, and it would be impractical to ban cell phones in all healthcare settings. The authors note that data are limited about the connection between cell phone contamination and HAIs. The authors recommend that cell phone use be incorporated into hand hygiene promotion, including handwashing before and especially after cell phone use, and routine disinfection of cell phones.

Even when hand hygiene compliance is nearly perfect, resistance to antimicrobial solutions is an increasing concern, given the widespread and rapid rise of antibiotic resistance. In Kampf’s nonsystematic review (2016), the frequency of handwashing events greatly increased the exposure of MDROs to low levels of chlorhexidine and the selective pressure for resistance.32 Although Ho and Brantley’s commentary (2012) on a pre-post study of chlorhexidine resistance genes in MRSA did not demonstrate a correlation between increased antiseptic use for hand hygiene and increased resistance gene prevalence, the authors note that other studies have shown some association and recommend further study.33

Outside the clinical setting, alcohol-based hand rubs are also used as a hand hygiene alternative when soap and water washing is not available. At the time of this report, the Food and Drug Administration was investigating benzalkonium chloride, ethyl alcohol, and isopropyl alcohol for safety and efficacy in over-the-counter hand rubs when used in place of soap and water washing among the general population. These ingredients are deferred from further rulemaking as data are gathered on their general safety and efficacy, and future research should include considerations about which solutions to use or avoid in community settings.k

References for Section 5.2

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Otter JA, Yezli S, Salkeld JA, French GL. Evidence that contaminated surfaces contribute to the transmission of hospital pathogens and an overview of strategies to address contaminated surfaces in hospital settings. Am J Infect Control. 2013;41:(5 Suppl):S6–11. doi: 10.1016/j.ajic.2012.12.004. [PubMed: 23622751] [CrossRef]
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Tacconelli E, Cataldo MA, Dancer SJ, De Angelis G, Falcone M, Frank U, et al. Escmid guidelines for the management of the infection control measures to reduce transmission of multidrug-resistant Gram-negative bacteria in hospitalized patients. Clin Microbiol Infect. 2014;20: Suppl 1:1–55. doi: 10.1111/1469-0691.12427. [PubMed: 24329732] [CrossRef]
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Altimier L, Warner B, Eichel M, Tedeschi L, Kamp T, Halverstadt A, et al. Implementing best practices through staff education to eradicate gentamicin-resistant staphylococcus aureus in a neonatal intensive care unit. Newborn Infant Nurs Rev. 2009;9(2):117–23. doi: 10.1053/j.nainr.2009.03.013. [CrossRef]
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Graveto JM, Costa PJ, Santos CI. Cell phone usage by health personnel: Preventive strategies to decrease risk of cross infection in clinical context. Texto & Contexto-Enfermagem. 2018;27(1). doi: 10.1590/0104-07072018005140016. [CrossRef]
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D’Agata EM, Horn MA, Ruan S, Webb GF, Wares JR. Efficacy of infection control interventions in reducing the spread of multidrug-resistant organisms in the hospital setting. PLoS One. 2012;7(2):e30170. doi: 10.1371/journal.pone.0030170. [PMC free article: PMC3282714] [PubMed: 22363420] [CrossRef]
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Palmore TN, Henderson DK. Managing transmission of carbapenem-resistant Enterobacteriaceae in healthcare settings: A view from the trenches. Clin Infect Dis. 2013;57(11):1593–9. doi: 10.1093/cid/cit531. [PMC free article: PMC3888298] [PubMed: 23934166] [CrossRef]
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De la Rosa-Zamboni D, Ochoa SA, Laris-Gonzalez A, Cruz-Cordova A, Escalona-Venegas G, Perez-Avendano G, et al. Everybody hands-on to avoid ESKAPE: Effect of sustained hand hygiene compliance on healthcare-associated infections and multidrug resistance in a paediatric hospital. J Med Microbiol. 2018;67(12):1761–71. doi: 10.1099/jmm.0.000863. [PubMed: 30372411] [CrossRef]
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Sopirala MM, Yahle-Dunbar L, Smyer J, Wellington L, Dickman J, Zikri N, et al. Infection control link nurse program: An interdisciplinary approach in targeting health care-acquired infection. Am J Infect Control. 2014;42(4):353–9. doi: 10.1016/j.ajic.2013.10.007. [PMC free article: PMC4104989] [PubMed: 24548456] [CrossRef]
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Pires dos Santos R, Jacoby T, Pires Machado D, Lisboa T, Gastal SL, Nagel FM, et al. Hand hygiene, and not ertapenem use, contributed to reduction of carbapenem-resistant Pseudomonas aeruginosa rates. Infect Control Hosp Epidemiol. 2011;32(6):584–90. doi: 10.1086/660100. [PubMed: 21558771] [CrossRef]
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Vernaz N, Sax H, Pittet D, Bonnabry P, Schrenzel J, Harbarth S. Temporal effects of antibiotic use and hand rub consumption on the incidence of MRSA and Clostridium difficile. J Antimicrob Chemother. 2008;62(3):601–7. doi: 10.1093/jac/dkn199. [PubMed: 18468995] [CrossRef]
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McLaws ML, Pantle AC, Fitzpatrick KR, Hughes CF. More than hand hygiene is needed to affect methicillin-resistant Staphylococcus aureus clinical indicator rates: Clean Hands Save Lives, Part IV. Med J Aust. 2009;191(S8):S26–31. doi: 10.5694/j.1326-5377.2009.tb02902.x. [PubMed: 19835528] [CrossRef]
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Ellingson K, Haas JP, Aiello AE, Kusek L, Maragakis LL, Olmsted RN, et al. Strategies to prevent healthcare-associated infections through hand hygiene. Infect Control Hosp Epidemiol. 2014;35: Suppl 2:S155–78. doi: 10.1017/s0899823x00193900. [PubMed: 25376074] [CrossRef]
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Barnes SL, Morgan DJ, Harris AD, Carling PC, Thom KA. Preventing the transmission of multidrug-resistant organisms: Modeling the relative importance of hand hygiene and environmental cleaning interventions. Infect Control Hosp Epidemiol. 2014;35(9):1156–62. doi: 10.1086/677632. [PMC free article: PMC4204209] [PubMed: 25111924] [CrossRef]
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Harris AD, Morgan DJ, Pineles L, Perencevich EN, Barnes SL. Deconstructing the relative benefits of a universal glove and gown intervention on MRSA acquisition. J Hosp Infect. 2017;96(1):49–53. doi: 10.1016/j.jhin.2017.03.011. [PMC free article: PMC6839451] [PubMed: 28410760] [CrossRef]
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Wares JR, Lawson B, Shemin D, D’Agata EM. Evaluating infection prevention strategies in out-patient dialysis units using agent-based modeling. PLoS One. 2016;11(5):e0153820. doi: 10.1371/journal.pone.0153820. [PMC free article: PMC4873022] [PubMed: 27195984] [CrossRef]
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Cheng VC, Chen JH, Poon RW, Lee WM, So SY, Wong SC, et al. Control of hospital endemicity of multiple-drug-resistant Acinetobacter baumannii st457 with directly observed hand hygiene. Eur J Clin Microbiol Infect Dis. 2015;34(4):713–8. doi: 10.1007/s10096-014-2281-x. [PubMed: 25413926] [CrossRef]
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Cheng VCC, Chen H, Wong SC, Chen JHK, Ng WC, So SYC, et al. Role of hand hygiene ambassador and implementation of directly observed hand hygiene among residents in residential care homes for the elderly in Hong Kong. Infect Control Hosp Epidemiol. 2018;39(5):571–7. doi: 10.1017/ice.2018.21. [PMC free article: PMC6225785] [PubMed: 29485019] [CrossRef]
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Rupp ME, Fitzgerald T, Puumala S, Anderson JR, Craig R, Iwen PC, et al. Prospective, controlled, cross-over trial of alcohol-based hand gel in critical care units. Infect Control Hosp Epidemiol. 2008;29(1):8–15. doi: 10.1086/524333. [PubMed: 18171181] [CrossRef]
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Sickbert-Bennett EE, DiBiase LM, Willis TM, Wolak ES, Weber DJ, Rutala WA. Reduction of healthcare-associated infections by exceeding high compliance with hand hygiene practices. Emerg Infect Dis. 2016;22(9):1628–30. doi: 10.3201/eid2209.151440. [PMC free article: PMC4994356] [PubMed: 27532259] [CrossRef]
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Lee MH, Lee GA, Lee SH, Park YH. Effectiveness and core components of infection prevention and control programmes in long-term care facilities: A systematic review. J Hosp Infect. 2019;102(4):377–93. doi: 10.1016/j.jhin.2019.02.008. [PubMed: 30794854] [CrossRef]
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Trautner BW, Greene MT, Krein SL, Wald HL, Saint S, Rolle AJ, et al. Infection prevention and antimicrobial stewardship knowledge for selected infections among nursing home personnel. Infect Control Hosp Epidemiol. 2017;38(1):83–8. doi: 10.1017/ice.2016.228. [PMC free article: PMC5828502] [PubMed: 27697086] [CrossRef]
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Luangasanatip N, Hongsuwan M, Limmathurotsakul D, Lubell Y, Lee AS, Harbarth S, et al. Comparative efficacy of interventions to promote hand hygiene in hospital: Systematic review and network meta-analysis. Bmj. 2015;351:h3728. doi: 10.1136/bmj.h3728. [PMC free article: PMC4517539] [PubMed: 26220070] [CrossRef]
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Clock SA, Cohen B, Behta M, Ross B, Larson EL. Contact precautions for multidrug-resistant organisms: Current recommendations and actual practice. Am J Infect Control. 2010;38(2):105–11. doi: 10.1016/j.ajic.2009.08.008. [PMC free article: PMC2827623] [PubMed: 19913329] [CrossRef]
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Hota S, Hirji Z, Stockton K, Lemieux C, Dedier H, Wolfaardt G, et al. Outbreak of multidrug-resistant Pseudomonas aeruginosa colonization and infection secondary to imperfect intensive care unit room design. Infect Control Hosp Epidemiol. 2009;30(1):25–33. doi: 10.1086/592700. [PubMed: 19046054] [CrossRef]
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Kotsanas D, Wijesooriya WR, Korman TM, Gillespie EE, Wright L, Snook K, et al. “Down the drain”: Carbapenem-resistant bacteria in intensive care unit patients and handwashing sinks. Med J Aust. 2013;198(5):267–9. doi: 10.5694/mja12.11757. [PubMed: 23496403] [CrossRef]
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Johnson RC, Deming C, Conlan S, Zellmer CJ, Michelin AV, Lee-Lin S, et al. Investigation of a cluster of Sphingomonas koreensis infections. N Engl J Med. 2018;379(26):2529–39. doi: 10.1056/NEJMoa1803238. [PMC free article: PMC6322212] [PubMed: 30586509] [CrossRef]
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Landers T, Abusalem S, Coty MB, Bingham J. Patient-centered hand hygiene: The next step in infection prevention. Am J Infect Control. 2012;40(4 Suppl 1):S11–7. doi: 10.1016/j.ajic.2012.02.006. [PubMed: 22546268] [CrossRef]
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Kampf G. Acquired resistance to chlorhexidine - is it time to establish an ‘antiseptic stewardship’ initiative? J Hosp Infect. 2016;94(3):213–27. doi: 10.1016/j.jhin.2016.08.018. [PubMed: 27671220] [CrossRef]
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Ho J, Branley J. Prevalence of antiseptic resistance genes qacA/B and specific sequence types of methicillin-resistant Staphylococcus aureus in the era of hand hygiene. J Antimicrob Chemother. 2012;67(6):1549–50. doi: 10.1093/jac/dks035. [PubMed: 22334609] [CrossRef]

5.3. PSP: Active Surveillance for MDROs

Authors

Editors: Luba Katz, Ph.D. and Sam Watson, M.H.A.

Key Findings

  • Targeted active surveillance performs as well as universal active surveillance for many MDROs and uses fewer resources. However, in places where universal active surveillance is already in place, screening for other MRDOs using the same sample may be cost-effective, as patients colonized with an MDRO share risk factors for others.
  • Some consensus exists for screening high-risk patients (those with a history of MDROs or risk factors associated with MDRO colonization/infection) on admission, but any screening approach will require compliance with infection prevention protocols when a patient’s culture result is positive.
  • Surveillance may improve compliance with other PSPs when it is part of a multicomponent intervention, but more research is needed on the mechanisms and circumstances of this association, as it can be confounded by the coimplementation of other, bundled practices.

“Active surveillance” is a broad practice that encompasses many activities, including sample collection, laboratory testing, data collection, data analysis, and reporting and feedback. Active surveillance helps prevent the spread of infection by identifying when an MDRO enters a healthcare facility and quickly triggering infection control measures. Active surveillance can also help with diagnosis and appropriate treatment of infections and antibiotic stewardship by generating data that can be used to create a local profile of antibiotic susceptibility or antibiogram.1

5.3.1. Practice Description

With the infection prevention and healthcare practitioner in mind, this report provides evidence to support strategies for “active surveillance”—the collection and culturing of samples specifically for identifying MDRO colonization and infection among patients. However, “active surveillance” is a broad practice that encompasses many activities (sample collection, lab testing, data collection, data analysis, and reporting and feedback) and occurs at many levels.1

Considering the broad scope, we also include best practices for active surveillance that continue beyond obtaining laboratory results. Where described in the literature, we include best practices in using active surveillance results to:

  • Direct infection prevention responses;
  • Evaluate the effectiveness of IP practices;
  • Track and communicate MDRO status, prevalence, and risk to prevent intra- and inter-facility transmission; and
  • Develop local, regional, and global datasets of MDRO prevalence that inform risk-based approaches to active surveillance and infection prevention.

Epidemiologically, genotyping of active surveillance samples can help identify potential modes of transmission or assess need for patient bathing/deeper environmental cleaning by identifying related organisms from multiple sample sites.1,2 These genotyping data can also be used to identify whether the MDROs identified in screening are endemic to the environment or are imported by asymptomatic carriers. However, this practice requires access to labs with the capacity to do quick-turnaround, real-time genotyping.1

Integration of active surveillance programs into electronic medical records can help automate identification and analysis but requires facilities with those capacities or access to them. However, generating larger, regional and even global surveillance systems allows individual facilities to identify risk factors for incoming patients (for example, knowing what areas of the world have high prevalence of certain MDROs).1

Many resource challenges arise in creating sophisticated laboratory and data integration systems that can identify, genotype, and share information on MDROs. At the same time, investing in these systems benefits other infection control practices by generating the data that allow facilities to take a risk-based approach to screening, isolation, and contact precautions, which represent an opportunity for cost saving.1 Finally, facilities must make decisions about when to stop active surveillance, balancing the costs of an active surveillance program against the possibilities of failed eradication and recolonization.3 Key findings are located in the box above.

5.3.2. Methods

To investigate how active surveillance has been implemented to prevent transmission of MDROs and contain MDRO outbreaks, we searched three databases (CINAHL, MEDLINE, and Cochrane) for a combination of the keywords “monitoring,” “surveillance,” and “monitoring and surveillance,” as well as MeSH terms “cross infection prevention,” “drug resistance, multiple, bacterial,” and “drug resistance, microbial.” Articles from January 1, 2008, through December 31, 2018, were included. (Any relevant articles published after the original search are included in the PRISMA diagram as additional sources.)

The initial search yielded 392 results (including 24 articles from other sources); after duplicates were removed, 352 were screened for inclusion, and 175 full-text articles were retrieved. Of those, 23 were selected for inclusion in this review. Articles were excluded if they did not mention active surveillance’s role in preventing MDRO transmission, only described surveillance for determining treatment, or did not include implementation in a healthcare setting.

General methods for this report are described in the Methods section of the full report.

For this patient safety practice, a PRISMA flow diagram and evidence table, along with literature-search strategy and search-term details, are included in the report appendixes A through C.

5.3.3. Review of Evidence

The Key Findings box presents a high-level summary of the findings in this review. Although the ideal method for active surveillance varies by MDRO (based on how the organism is acquired and shed by patients), one common theme is using targeted, active surveillance based on MDRO risk factors, such as recent hospitalization or history of MDRO colonization. Screening results should then be used to guide other infection control practices, such as contact precautions or decolonization protocols. Without adherence to these practices, the value of active surveillance is limited.

Screening decisions for facilities should be based on the available epidemiological surveillance data on which organisms are likely to be prevalent in a facility’s patient population. Rare MDROs will result in far higher screening costs to prevent one infection/colonization event, compared with MDROs with higher prevalence. For MDROs or other pathogens frequently present on admission (such as MRSA or C. difficile), screening results may be useful in identifying a patient at risk for other MDROs. Conducting tests for multiple MDROs on one sample may reduce the materials and time needed for sample collection but may increase costs related to lab processing.

Where active surveillance may provide the most value is in improving compliance with other PSPs in multicomponent interventions. However, it is not clear how strong that association may be or why an association appears in some studies but not others. As mentioned above, identifying patients colonized or infected with an MDRO is only valuable if the correct procedures to reduce transmission (such as hand hygiene or decolonization) are followed consistently based on that knowledge. More research is needed to understand the synergistic effect of active surveillance to maximize its benefits.

5.3.3.1. Active Surveillance To Control MDRO Transmission

Active surveillance for MDROs is necessary because routine surveillance of clinical samples will undercount colonized or infected patients.3,4 The proportion of clinically evident cases also varies by organism and susceptibility of the patient population, which means many asymptomatic carriers will go unnoticed without active surveillance.4 In addition, an accurate screening process will reduce the number of patients on isolation or contact precautions unnecessarily.5 In an outbreak of an MDRO in an otherwise low-prevalence setting, active surveillance is needed to verify that the outbreak has been successfully contained.6

It should be noted that in each of the studies included, active surveillance was combined with other infection control preventions. Tacconelli et al. (2014) strongly recommend always pairing surveillance with other infection prevention practices.4 Cipolla et al., in their 2011 commentary, suggest that active surveillance results can be used to build a local antibiogram to complement antibiotic stewardship initiatives.7 Gasink and Brennan’s nonsystematic review (2009) further found that active surveillance without preemptive isolation has not been shown to be effective.8

This variation in practice makes it difficult to evaluate the effect of infection prevention with and without active surveillance, as noted in Strich and Palmore’s commentary (2017).9 While Strich and Palmore suggest that universal contact precautions may ultimately be more effective for MDRO prevention than active surveillance, these universal measures come with extra costs and potential for additional negative outcomes (discussed below).

In this summary, we present ways healthcare facilities used these strategies, including both successful and unsuccessful approaches. Several organizations have produced evidence-based recommendations on the best ways to use active surveillance to identify and contain MDROs, links to which can be found in section 5.3.4.4. However, the field of MDRO research continues to evolve, and we provide recent findings to supplement existing recommendations. We also present lessons learned from outbreak responses, especially lessons learned about challenges that threaten the validity and effectiveness of active surveillance.

5.3.3.1.1. Screening Methods for Detecting MDROs

Although screening is widely used, findings are mixed as to the correct screening method (patient sites, type of swabs used), frequency, target population, and culturing of samples. The sensitivity and specificity of a sample collection site or type varies by type of MDRO.

Given the costs associated with active surveillance and subsequent patient isolation, Freire and colleagues (2017; prospective cohort study) recommend universal surveillance in facilities where the incidence of MDROs is moderate to high and for patients for whom the rate of conversion from colonization to infection is high (e.g., transplant patients).10 In universal surveillance, Barbadoro and colleagues’ 2017 time series analysis found that skin, blood, and respiratory samples performed better at initially identifying the presence of an MDRO than did urine samples.11 The CDC (2019) offers guidelines for surveillance based on different categories of organisms and resistance mechanisms, with a recommended approach for each.12

Based on the findings in our review, we summarize the evidence for active surveillance around five topic areas, comparing both universal and targeted approaches (when findings are available):

  • Surveillance for general MDR Gram negative bacteria (MDR-GNB)
  • Surveillance for methicillin-resistant Staphylococcus aureus (MRSA)
  • Surveillance for vancomycin-resistant Enterococci (VRE)
  • Surveillance for carbapenem-resistant or carbapenemase-producing Enterobacteriaceae (CRE/CPE)
  • Surveillance for MDROs using environmental sampling

General MDR-GNB: No consensus exists on frequency of screening or timing of screening for MDR-GNB. A nonsystematic review by Gasink and Brennan (2009) showed that screening during admission with weekly followup prevented the spread of MDR-A. baumanii.8 However, a similar program for MDR-K. pneumoniae was not successful.4 In epidemic settings, targeted screening on admission for high-risk patients is recommended. Screening can also be used to reinforce other prevention practices in the outbreak response, such as hand hygiene.

In the endemic setting, active surveillance should be used as an additional measure to control the spread of MDR-GNB between facilities or units. Otter and colleagues, in their 2015 commentary review, suggest using surveillance data from endemic settings to build risk assessment protocols and implement targeted screening policies that will catch MDR-GNB carried by transferred patients without adding unnecessary costs or burden.

As far as sampling sites, Tacconelli and colleagues (2014) found that rectal swabs, urine, or respiratory secretions were sufficient for almost all MDR-GNB, with rectal swabs being the most sensitive and groin being most specific. However, one study in that systematic review showed that sensitivity of screening is low (29%) even when six body sites are included. Finally, Tacconelli and colleagues note that (as of writing in 2014) rapid polymerase chain reaction-based methods to identify MDR-GNB were still in development, so culture-based tests remain the standard.4

Once an MDR-GNB pathogen is identified, Tacconelli and colleagues recommend weekly screening until no cases of colonization/infection or cross-transmission are observed.4 Several outbreak responses have noted that MDR-GNB pathogens, particularly MDR-AB, produce significant environmental contamination due to their method of shedding (shed skin cells, stool, and/or urine).13,14 However, the mean colonization time for MDR-GNB in their reviewed studies was 144 days, representing a significant length of time. Tacconelli and colleagues also noted that the efficacy of screening was linked to the level of compliance, so screening must be maintained over time.4

Methicillin-resistant Staphylococcus aureus (MRSA): Given the increasingly endemic nature of MRSA in both healthcare and community settings, questions have emerged about the clinical value of screening for MRSA, especially among asymptomatic carriers.15,16 If conducting screening for MRSA, Lin and colleagues (2018) found nasal screening to be most sensitive: nasal culturing alone identified 84 percent (327/388) of MRSA positive patients; only 61 patients (16%) were both nasal-culture negative and groin-culture positive. Nasal screening also had a strong negative predictive value of 98 percent (95% CI, 97.6% to 98.5%).16

MRSA screening may be a useful tool for identifying colonization of other, nonendemic MDROs. Evidence supports some association between MRSA status at admission and later discovery of MDRO colonization. Jones and colleagues’ retrospective cohort study (2015) found that 2.4 percent of patients with positive MRSA screening later had a positive MDR-GNB culture, compared with 0.9 percent of patients with a negative MRSA screening (p<0.001). This association was strongest for Acinetobacter species of MDR-GNB. Jones et al. also found that 85.5 percent of those with a subsequent MDR-GNB negative culture also had an MRSA-negative screen.17

In facilities where universal MRSA screening is already in place, a positive result may be considered a risk factor for other MDROs. By knowing risk factors associated with colonization by MDROs other than MRSA, hospitals and other facilities can develop risk-based testing approaches for screening on admission, reducing costs in time and materials.18

Vancomycin-resistant Enterococci (VRE): Active surveillance for VRE can help detect asymptomatic carriers, but the clinical benefit of this strategy is unclear and methods for VRE surveillance can vary widely in practice.19 Active surveillance helps detect asymptomatic VRE colonization in patients with C. difficile infection (CDI) in facilities with a high VRE prevalence, given high correlation between colonization with the two organisms. More than 50 percent of patients with CDI were also colonized with VRE.20

Despite this finding, it is not clear whether surveillance for asymptomatic VRE carriers reduces VRE-related infections. Almyroudis and colleagues’ interrupted time series study (2016) found that active surveillance with precautions for sporadic (not horizontally-transmitted) VRE did not protect patients against VRE bacteremia.21 Huskins et al. (2011) also observed no difference in mean colonization and infection rates between the active surveillance and control groups in a cluster-randomized trial of active VRE and MRSA surveillance upon admission.22

Carbapenem-resistant/carbapenemase-producing Enterobacteriaceae (CRE/CPE): Although the global prevalence of CRE/CPE is increasing, not all regions or all facilities in a region share the same risk for CRE outbreaks. Active surveillance following identification of CRE can reveal additional asymptomatic cases, as Banach and colleagues learned in their 2014 observational study using C. difficile samples to test for concurrent CRE carriage. Rescreening of clinical samples collected for other testing (such as Banach et al.’s approach to perform testing for CRE on C. difficile stool samples) is one way to efficiently screen patients who have risk factors for multiple MDROs and identify asymptomatic carriers.23

Karampatakis and colleagues’ quasi-experimental study (2018) showed that a multicomponent intervention, including active surveillance, reduced rates of K. pneumoniae and P. aeruginosa infection but not of other MDR-GNB (A. baumannii), further highlighting the importance of tailoring infection prevention response to the organisms.24 As described below in environmental surveillance, A. baumannii may require enhanced environmental cleaning protocols compared with CRE, due to the increased environmental contamination from colonized patients.

In light of no clear evidence for or against universal screening for CRE, one commentary by Asensio and colleagues (2014) recommends active surveillance on admission for patients in any of the following elevated risk groups:

  • Patients transferred from a healthcare facility in any foreign country (in light of a lack of data on global CRE prevalence
  • Patients transferred from acute or long-term care facilities with known high CRE prevalence
  • Patients previously colonized or infected with CRE
  • Patients who have had close contact with a person with CRE.

Finally, any surveillance must have clear definitions to avoid under- or over-reporting of CRE cases.25 In Mayer and colleagues’ retrospective laboratory audit (2016), underreporting due to misunderstanding definitions was far more frequent than overreporting.26

Environmental Sampling for MDRO Surveillance: Active surveillance of the environment, in addition to patients, combined with monitoring staff’s adherence to infection control practices, can identify the transmission patterns and expose areas for improvement. For example, Sui and colleagues’ 2013 outbreak response found that, compared with MRSA, MDR-AB patients were more likely to contaminate their environment.27

Environmental sampling as part of active surveillance can be used to identify areas in need of intensive cleaning or where cleaning has been missed, as identified by Lesho and colleagues (2018) and Liu and colleagues (2014) in their respective outbreak responses.28,29 Nusair and colleagues’ observational study (2008) found that evaluating the outcomes of different types of sampling (such as the most frequently positive patient body sites) can also help streamline the sample collection process for future surveillance.30

Cheng and colleagues (2018; outbreak response case study) found that environmental surveillance may serve as an indicator of MDRO carriers, at least in the case of MDR-AB, where the organism is consistently shed by patients.31 In another outbreak (of MDR-E. coli), however, environmental surveillance failed to identify an environmental source.32 The outbreak was successfully contained only after it was moved to a temporary neonatal ICU, showing that negative environmental samples do not reliably indicate that the environment is free of MDROs. In addition, the Healthcare Infection Control Practices Advisory Committee recommends culturing environmental samples when epidemiological evidence shows an environmental source of ongoing transmission.33

5.3.3.1.2. Genotyping MDRO Cultures

Genotypic testing can help determine whether MRDOs identified in active surveillance are horizontally transmitted between patients, coming from a common environmental reservoir, or are imported from other facilities. One interrupted time series study of active screening of high-risk patients by Borer and colleagues (2011) found that 45 percent of CR-K. pneumoniae infections and 57 percent of all positive cultures were community acquired.34 Benenson and colleagues’ 2013 screening of neonates in an Israeli ICU found both imported and horizontally-transmitted strains of ESBL-producing K. pneumoniae. The authors significantly decreased the number of positive cultures using surveillance in combination with cohorting of neonates with positive cultures.35

In Kohlenberg and colleagues’ outbreak report (2010), active surveillance detected environmental reservoirs of CR-PA unrelated to the outbreak strain, based on genotyping results of the cultured organisms.36 Finally, Wendel and colleagues’ MDR-P. aeruginosa outbreak response case study (2015) used genotyping to confirm transmission through shared hair washbasins, which allowed the authors to halt the epidemic and prevent further transmission by discontinuing their use.37

5.3.3.2. Surveillance for Process Outcomes

Surveillance, by its nature, is a practice that gathers process and outcome data, allowing evaluation of other patient safety practices. This section describes how different modes of active surveillance have been evaluated for effectiveness and how active surveillance can be used to evaluate the effectiveness of other practices or bundles.

Tracking MDRO isolates over time and between different units allows hospitals to evaluate the effectiveness of their infection control protocols. In Ahern and Kemper’s 2009 case study, the authors showed reduction in MDROs despite increased rate of antibiotic prescription.l Bryce and colleagues’ pre-post study (2015) found that risk-based active surveillance could be as effective as universal surveillance in reducing the target MDRO, VRE, as well as MRSA and C. difficile infection.38 In D’Agata and colleagues’ mathematical model simulation (2012), targeted screening for MRSA and VRE for patients receiving antimicrobials (a known risk factor for MDRO acquisition) reduced MDRO acquisition while universal screening did not.39

Active surveillance programs have been observed indirectly enhancing compliance with other patient safety practices, but more research is needed to understand when and why adding active surveillance helps compliance with other practices, as our review also uncovered examples of no association.40 For example, Evans et al. (2017) observed decreases in transmission and HAIs related to MRSA in U.S. Veterans Affairs hospitals after implementing an infection prevention bundle. The authors speculate that universal screening for MRSA as part of the bundle served as a reminder to comply with other practices such as hand hygiene and contact precautions. Other hand hygiene and device-placement bundles were already in place, but MRSA transmission and infection rates did not drop until the active surveillance bundle was implemented.41

Mawdsley et al. (2010) found that weekly surveillance rounding successfully improved compliance with contact isolation initiation and required minimal resources (two person-hours of work per week, split among six infection preventionists).42 Compliance surveillance in Palmore and colleagues’ outbreak response effort (2011) helped identify a staff subpopulation that were more likely to fail to comply with infection control policies (in this case, physicians).43

Conversely, Huskins et al. (2011) observed that reporting culture results did not yield high compliance with contact precaution requirements. Despite being aware of patient’s colonization status, healthcare providers used clean gloves only 82 percent of the time, gowns 77 percent of the time, and hand hygiene 69 percent of the time during observed periods.22 Similarly, Lin and colleagues’ observational study of 25 Illinois hospitals (2018) found that only 54 percent of patients whose point prevalence culture was positive for MRSA were on contact precautions, despite new State legislation mandating active MRSA surveillance on admission and contact precautions for any patients with a positive result.16

5.3.3.3. Economic Outcomes

Cost-effectiveness of active surveillance interventions depends on how many infections are reduced (or are likely to be reduced) by the intervention, which varies by facility and even within facilities. Early detection and containment of MDROs reduces the costs associated with decontamination and eradication.44 In cases where an MDRO is already endemic, such as in Zarpellon and colleagues’ (2018) prospective study of active surveillance, the authors took a modified, risk-based approach. MRSA was considered endemic in the study hospital, except in pediatric and neonatal wards. Accordingly, the authors screened for MRSA only in pediatric and neonatal wards, where the MDRO was not yet established.45

Cost avoidance in targeted active surveillance can also take the form of reduction in products needed for contact isolation (gloves, gowns, hospital linens), laboratory reagents, and lost revenue (due to needing private rooms for patient isolation), as described by Bryce and colleagues in their 2015 pre-post study of targeted monitoring for VRE.38 Johnston and Bryce’s nonsystematic review (2009) found that screening patients at high risk for colonization with MRSA or VRE may be cost-effective if coupled with barrier precautions.3

The more accurate the active surveillance methodology, the fewer patients will be put on contact precautions unnecessarily.46 Morgan and colleagues’ 2009 systematic review also notes that faster screening tests can reduce the time patients are kept on preemptive precautions or in single-patient rooms.47

Finally, Banach and colleagues’ observational study (2014) demonstrated the efficacy of a low-cost strategy to screen for CRE using sampling already being done for CDI, as both organisms share risk factors. The total cost of detecting one CRE-colonized patient ranged from $580 to $649 and required between 68 and 76 samples to be tested (based on the prevalence at the facilities in the study).23

5.3.3.4. Unintended Consequences

5.3.3.4.1. Negative

Active surveillance is used to identify patients to be placed on contact precautions, which reduce transmission but may have unintended adverse effects on the patient. Morgan and colleagues’ systematic review (2009) found that contact precautions were associated with less contact from healthcare workers, delays in care, adverse events (non-infection- associated), increased symptoms of depression and anxiety, and decreased patient satisfaction with care.47 This finding was also noted in commentary from Lemmen & Lewalter (2018).5

A study by Day and colleagues (2013) found that patients on contact precautions were not at any greater risk of developing depression or anxiety, although they may have more symptoms of anxiety and depression at the start of contact precautions.48 Rapid-result genetic testing can also reduce any potential adverse effects of contact isolation by limiting the time spent in preemptive isolation pending screening results.8

Palmore and Henderson found an unintended negative consequence of public education in their 2013 outbreak response report: coverage of the outbreak in the wider media emphasized mortality rates, which increased community anxiety when information was shared about the outbreak.49 When sharing information on outbreaks and infection prevention responses with patients and families, one must convey the importance of preventing transmission and managing patients’ understanding of their individual morbidity and mortality risk. Publications on techniques used to control the outbreak in a facility as well as media coverage of the outbreak, for example, could be shared.

5.3.3.4.2. Positive

Active surveillance has shown positive unintended effects. Bryce and colleagues’ pre-post study (2015) found that risk-management surveillance reduced other infections (MRSA, CDI) in addition to the target organism (VRE).38 In one observational study, environmental surveillance for MDROs led to discovery of a leaking water pipe that led to significant mold growth that could have resulted in additional harm among the immunocompromised patients.30 Finally, Sánchez García and colleagues’ active surveillance for MRSA during an outbreak (2010) identified a novel strain that was resistant to linezolid and allowed implementation of protocols to contain and ultimately eliminate it.50

5.3.4. Implementation

5.3.4.1. Summary of Evidence on Implementation

Reduction in MDRO infection rates does not come from active surveillance alone; rather, it should guide healthcare staff in informed decision making, such as implementing patient isolation and contact precautions. Regular monitoring through clinical sampling is a simple way to detect emergent pathogens, but it has limitations. Orsi et al. (2011) and Sandora et al. (2010) describe tradeoffs between routine surveillance of clinical samples and active surveillance.51,52

Routine clinical surveillance of already-collected samples is less costly in terms of collection time, but active surveillance testing can determine presence on admission or temporality of colonization, as well as identifying asymptomatic carriers (as mentioned above). Therefore, Orsi et al. (2011) recommend active surveillance to close the gaps in clinical sampling during outbreaks or for MDROs not endemic in a facility.51

5.3.4.2. Barriers and Facilitators

Adding weekly dissemination of the results of active surveillance (MDRO rates, location of acquisition) was key to successfully controlling MDROs. Although other components (active surveillance, patient isolation) had been in place already, Quan and colleagues (2015) demonstrated that automated systems could support enforcement of contact precautions and save considerable infection preventionist time.53

Horizontal transmission of MDRO strains may not need universal active surveillance, but MDRO acquisition or infection between facilities warrants communication to identify patients at elevated risk. In a retrospective analysis using a regional surveillance system for MDROs based on an existing MRSA and VRE alert system, Rosenman and colleagues (2014) observed several crossovers between institutions.54

Coordination with regional and national public health agencies can help with interfacility transmission by coordinating notification and infection prevention efforts across all facilities. Grundmann’s 2014 commentary recommends a stepwise approach (local to regional to national to global) for creating a global surveillance network.55

Investing in active surveillance can require expenditures for laboratory and computer resources, as noted in O’Brien and Stelling’s systematic review (2011), but these investments can help reduce the cost of other infection prevention efforts.1 If a facility cannot absorb the costs of running a laboratory, partnering with public health agencies for surveillance may be an option.

In addition to the costs associated with conducting active surveillance, a few other challenges are described in the literature. Faster results can be available using molecular testing methods such as polymerase-chain reaction, but these tests can be costly, have limited specificity in some cases, and are not available in all facilities.51

5.3.4.3. Additional Important Contextual Factors

Santos et al., in their 2008 commentary review, note that although active surveillance for MDROs has significant benefits for infection prevention and treatment for the patient, it can also be considered quality improvement (research). Therefore, surveillance and isolation precautions do not require specific patient consent.56 However, education and clear communication about the need for and impact of active surveillance on patients are critical. In addition, the financial burden of active surveillance should be assumed by the facility, not the patient.

5.3.4.4. Resources To Assist With Implementation

5.3.5. Gaps and Future Directions

The greatest challenge to active surveillance cultures/testing for MDROs is understanding which surveillance protocols are the most sensitive and specific for correctly identifying carriers while minimizing the burden for collecting samples and processing data. Although evidence-based recommendations exist for MRSA, VRE, and CRE, numerous pathogens (particularly other MDR-GNB such as K. pneumoniae and emerging MDR pathogens such as Candida auris) lack a consistent recommendation for whom and when to screen.

Duffy and colleagues (2011), in their synopsis of a working group of infection prevention professionals, recommend strengthening partnerships between healthcare facilities and public health departments to build capacity for identifying and tracking emerging MDROs.57 Further studies that evaluate targeted surveillance protocols based on risk factor analysis would give healthcare facilities another tool for effective, lower cost surveillance.

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Evans ME, Kralovic SM, Simbartl LA, et al. Eight years of decreased methicillin-resistant Staphylococcus aureus health care-associated infections associated with a Veterans Affairs prevention initiative. Am J Infect Control. 2017;45(1):13–6. doi: 10.1016/j.ajic.2016.08.010. [PubMed: 28065327] [CrossRef]
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Mawdsley EL, Garcia-Houchins S, Weber SG. Back to basics: Four years of sustained improvement in implementation of contact precautions at a university hospital. Jt Comm J Qual Patient Saf. 2010;36(9):418–23. doi: 10.1016/s1553-7250(10)36061-2. [PubMed: 20873675] [CrossRef]
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Palmore TN, Michelin AV, Bordner M, et al. Use of adherence monitors as part of a team approach to control clonal spread of multidrug-resistant Acinetobacter baumannii in a research hospital. Infect Control Hosp Epidemiol. 2011;32(12):1166–72. doi: 10.1086/662710. [PMC free article: PMC4785863] [PubMed: 22080654] [CrossRef]
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Zarpellon MN, Viana GF, Mitsugui CS, et al. Epidemiologic surveillance of multidrug-resistant bacteria in a teaching hospital: A 3-year experience. Am J Infect Control. 2018;46(4):387–92. doi: 10.1016/j.ajic.2017.10.012. [PubMed: 29217187] [CrossRef]
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Djibre M, Fedun S, Le Guen P, et al. Universal versus targeted additional contact precautions for multidrug-resistant organism carriage for patients admitted to an intensive care unit. Am J Infect Control. 2017;45(7):728–34. doi: 10.1016/j.ajic.2017.02.001. [PubMed: 28285725] [CrossRef]
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5.4. PSP: Environmental Cleaning and Disinfection

Authors

Sam Watson, M.H.A.

Key Findings

  • Cleaning with chlorine-based solutions (e.g., bleach) was studied as part of enhanced cleaning methods for MDROs. Research is lacking on cleaning with bleach as a single intervention.
  • Moderate evidence supports the use of quaternary ammonium compounds for certain MDROs, although evidence is mixed in support of their usefulness in the targeted disinfection of high-touch surfaces.
  • More studies are needed in clinical settings that examine the different cleaning and disinfecting agents.
  • No-touch disinfection technologies are promising additions to disinfection practices but must be further studied to determine the most efficacious and cost-effective options.
  • Environmental screening is a useful tool for auditing and monitoring ongoing cleaning practices and for identifying highly contaminated surfaces for targeted cleaning during outbreak scenarios.
  • Efficacy of approaches varied against different species of bacteria and for sensitivity versus drug-resistant strains.

This section reviews research from 2008 to 2018 on environmental cleaning and disinfection as a strategy to prevent the transmission of multidrug-resistant organisms (MDROs) and reduce healthcare-associated infections (HAIs). Following a practice description and methods, the evidence summary reviews the research on different disinfectant agents, no-touch decontamination methods, and antimicrobial surfaces. Next, we explore several implementation facilitators, including environmental screening, audit and feedback, education, and facility policies. Finally, we look at gaps and future directions. Key findings are located in the box on the right.

5.4.1. Practice Description

Environmental surfaces serve as an intermediate vector for transmitting MDROs in healthcare settings.1 Environmental contamination can occur from contact with MDRO-infected individuals or their body fluids and can result in transmission to another individual. The “environment” includes furniture and other surfaces in patient rooms; medical equipment; personal items belonging to patients, visitors, or staff; and structural components of the facility (e.g., sinks, air vents).

To remove MDROs or disinfect the environment, healthcare facilities use specific cleaning and disinfection practices. Enhanced or standard cleaning may be implemented on a daily basis or when a patient vacates a room (called terminal cleaning). In the event of an outbreak or increased rate of transmission, facilities may perform a more thorough, one-time environmental cleaning. The latter is frequently done when other infection control practices or standard environmental cleaning does not reduce infection rates or when a specific source of contamination is suspected or identified by environmental screening. Enhanced environmental measures also include reinforcing training of environmental services staff and monitoring adherence to environmental cleaning protocols.2

Before a disinfectant is applied, cleaning is required to manually scrub and wash any visibly soiled surfaces because disinfectants cannot typically penetrate organic matter or thick substances to eradicate microbes beneath.3 After cleaning, a disinfectant is applied and left in contact with a surface for the amount of time designated by the manufacturer as necessary to kill/deactivate microorganisms. The variations and efficacy of these environmental cleaning and disinfection practices—highlighting MDROs in healthcare settings—are the focus of the following systematic literature review.

5.4.2. Methods

To determine the most effective environmental cleaning and disinfection practices for reducing the spread of MDROs, three databases (CINAHL, MEDLINE, and Cochrane) were searched for “bacterial drug resistance,” “microbial drug resistance,” and synonyms, in combination with “disinfection methods,” “environmental monitoring,” “environmental cleaning,” and associated phrases. Articles from 2008 through 2018 were included.

The initial search yielded 375 results (including 9 from other sources); after duplicates were removed, 347 were screened for inclusion, and 130 full-text articles were retrieved. Of those, 58 were selected for inclusion in this review. Articles were excluded if they were outside the scope of this review, included insufficient detail on a patient safety practice, did not describe an intervention (e.g., surveillance only), demonstrated insufficient rigor, or were included in another PSP section of this report.

General methods for this report are described in the Methods section of the full report.

For this patient safety practice, a PRISMA flow diagram and evidence table, along with literature-search strategy and search-term details, are included in the report appendixes A through C.

5.4.3. Review of Evidence

This review includes evidence from 4 systematic reviews and 54 studies. Of the studies:

  • Twenty-one were before-and-after intervention studies (one of which was a mathematically modelled and simulated intervention),
  • Thirteen were outbreak studies,
  • Nine were laboratory studies,
  • Five were cross-sectional surveys,
  • Two were cluster-randomized controlled trials,
  • Two were cluster-randomized crossover studies,
  • One was a prospective cohort study, and
  • One was a prospective controlled quasi-experimental study.

Of all included articles, 25 took place or reviewed studies that took place in the United States, 31 occurred outside the United States, and 2 included studies from both the United States and abroad. The included studies focused on cleaning and decontamination agents to reduce MDROs and infection from MDROs, as well as facilitators and barriers to cleaning and sterilization in the healthcare environment.

5.4.3.1. Disinfection Products

5.4.3.1.1. Chlorine-Based Disinfectants

The most commonly referenced disinfectants were chlorine-based products (e.g., bleach), which were used in various studies for deep, terminal, or daily routine cleaning and often as part of multicomponent interventions.

Standard or enhanced environmental cleaning with chlorine-based disinfectants has been associated with controlling outbreaks and reducing MDROs.46 In one study, a sink trap was determined as the likely source of an increased number of patient infections with multidrug-resistant A. baumannii.4 As a response to the outbreak and the results of environmental sampling, bleach was used to disinfect sinks and plumbing. During the 6 months after the intervention, the number of new cases greatly declined. In an in vitro study, sodium hypochlorite at 0.5% concentration, standing for 30 seconds, was found to successfully eradicate imipenem-resistant A. baumannii, but the article noted that an overdiluted bleach solution (0.08%) was insufficient to reduce environmental contamination.7

Cleaning with chlorine-based agents was a component of several multicomponent interventions to decrease MDRO transmission.816 For example, cleaning with chlorine-based disinfectants was part of a multicomponent intervention to reduce pandrug-resistant A. baumannii.16 The intervention included hand hygiene, surveillance, and patient isolation. In another multicomponent intervention, enhanced cleaning with a chlorine-based detergent, combined with patient isolation, chlorhexidine bathing, and staff education was associated with ending an outbreak of linezolid-resistant Enterococcus faecium.17

A multifacility cluster-randomized crossover study in nine U.S. hospitals compared bleach with the detergent used at baseline (quaternary ammonium),m ultraviolet-C light (UV-C), and a combination of bleach and UV-C in preventing transmission of several MDROs. The incidence of target organisms among exposed patients was not significantly changed with the use of bleach alone, or the combination of bleach and UV-C, compared with quaternary ammonium.18

A before-and-after study in a burn ICU found that adding a chlorohexidine-alcohol disinfectant to standard cleaning with sodium hypochlorite was more effective than standard cleaning with sodium hypochlorite alone, although other implementation variables (e.g., frequency of cleaning, targeted cleaning) were also altered and may have contributed to the results.19

5.4.3.1.2. Quaternary Ammonium Compounds

Quaternary ammonium compounds (QACs) have demonstrated mixed success in environmental cleaning and disinfection. In one study, terminal cleaning with QAC reduced environmental contamination with MDR-AB in patient rooms within ICUs at an American teaching hospital.20 QACs were also incorporated into environmental cleaning practices as a part of successful multicomponent outbreak interventions for MDR-AB.11,15 Lastly, in one before-and-after study, the use of Bio-Kil (which contained QAC) compared with manual surface cleaning with 500 ppm sodium hypochlorite was found to disinfect and provide ongoing microbial activity, resulting in reduced environmental bacterial contamination and sepsis incidence in the ICU.21

QACs have also been included in interventions that use enhanced environmental cleaning practices. One cluster-randomized controlled trial supplemented routine cleaning of ICU rooms with a one-time disinfection of high-touch surfaces in each room. Both routine and enhanced cleaning used a QAC disinfectant. Adding the supplementary cleaning did not result in a significant difference in the subsequent colonization of healthcare workers’ gowns and gloves with MRSA or MDR-AB and thus was not determined to add value to environmental cleaning and disinfection practices.22 While no clinical outcomes were reported, the contamination of healthcare workers’ gowns and gloves is a suspected source of transmission to patients. This study did not provide sufficient evidence to support the use of QACs to target high-touch surfaces.

QACs are not sporicidal and thus should not be relied on to eradicate spore-producing organisms such as C. difficile from the environment.18 They are also considered to have very low, if any, toxicity to humans.21 Lastly, a cross-sectional in vitro study of 12 vancomycin-susceptible E. faecium and 37 vancomycin-resistant E. faecium isolates found that the resistant isolates had decreased susceptibility to benzalkonium chloride. Further research is needed to investigate the potential for MDRO cross-resistance with antibiotic resistance and QAC-based disinfectants.23

5.4.3.1.3. Hydrogen Peroxide

Several studies examined hydrogen peroxide in various forms for reducing/eliminating MDROs. Hydrogen peroxide was tested in four variations in a laboratory study. In this study, a novel hydrogen peroxide disinfectant including anionic and nonionic surfactants in an acidic product was compared in vitro with traditional hydrogen peroxide disinfectants. The “improved” hydrogen peroxide product was more effective in reducing bacteria than QAC or any of three tested concentrations of hydrogen peroxide.24

In a cross-sectional study of clinical isolates, vancomycin-resistant and vancomycin-sensitive bacteria were not found to differ in their minimum inhibitory concentrations for hydrogen peroxide (in contrast to chlorohexidine and benzalkonium chloride).23 No further studies directly addressed the use of hydrogen peroxide in its liquid state for environmental disinfection of clinical settings. We discuss the use of hydrogen peroxide vapor and no-touch methods below.

Silver ions are used on antimicrobial surfaces and in cleaning products for their antibacterial properties. One in vitro study by De Giglio et al. (2014) investigated the use of a combination of 0.1% silver ion and 5% hydrogen peroxide disinfectant on sensitive and resistant strains of Staphylococcus aureus and P. aeruginosa. The disinfectant was effective for both sensitive and multidrug-resistant strains, although it took twice as long for the latter (10 minutes versus 5 minutes). The efficacy decreased in the presence of organic matter, doubling the required contact time for both sensitive and resistant strains.

This study indicates that use of silver ion solutions for disinfecting surfaces should be preceded by cleaning of any soiling or organic matter. In addition, close attention should be paid to contact time of the disinfectant, especially if multidrug-resistant strains are known to be contaminating the environment.25

5.4.3.1.4. Chlorhexidine

We found several before-and-after and outbreak studies of chlorhexidine and alcohol-based disinfectants, used separately or in conjunction. For example, one before-and-after study in an Italian burn ICU compared standard environmental cleaning using sodium hypochlorite with a chlorohexidine-60% isopropyl alcohol disinfectant. Additional changes were made to the daily cleaning regimen, including increased focus on high-touch surfaces and more frequent disinfection.

After the intervention, there was a decline in the percentage of positive carbapenem-resistant A. baumannii environmental cultures from 13 percent to 4 percent and a reduction in samples exceeding the acceptable adenosine triphosphate (ATP) limits from 21.7 percent to 14 percent.19 A cross-sectional study of chlorohexidine for vancomycin-sensitive and vancomycin-resistant Enterobacteriaceae clinical isolates found a lower susceptibility to chlorohexidine in vancomycin-resistant isolates than in the drug-sensitive isolates.23

5.4.3.1.5. Multiple Disinfectants

Chlorine-based disinfectants have been used in combination with other disinfectant chemicals in outbreak settings. Enhanced cleaning was initiated at the start of an outbreak of A. baumannii during which the organism was isolated from 22 neonates in a neonatal ICU.26 Infection control measures included disinfection with bleach for surfaces, hydrogen peroxide gas plasma for reusable equipment, and disinfection of nursery incubators with 4% chlorhexidine. The intervention also included closure of the ward and hand hygiene promotion. The last case occurred 8 months after the first identified A. baumannii isolate. The source of the outbreak was likely a mother admitted to the adult ICU.26 The researchers credit control of the outbreak to enhanced infection control measures.

5.4.3.1.6. Other Disinfectant Agents

Sodium dichloroisocyanurate was used as part of a multicomponent intervention in a Korean ICU to stop an outbreak of carbapenem-resistant A. baumannii. The disinfectant was used for terminal and indepth cleaning, and effectiveness was audited with environmental cultures. Additional measures included contact precautions, patient isolation, and change to a closed suctioning mechanical ventilation system. Within 5 months of implementing these more intensive disinfection and isolation practices, there were no new colonizations or infections,27 but it is not possible to separate whether this finding was due mainly to the disinfectants used or to other components of the intervention.

Glucoprotamin was investigated in one in vitro laboratory study included in our review. This disinfectant had varying levels of efficacy against several MDROs. For example, glucoprotamin was more effective against Gram-negative than Gram-positive bacteria. In addition, tetracycline-resistant P. aeruginosa was found to be more resistant to glucoprotamin disinfectant than was tetracycline-sensitive P. aeruginosa, but not at levels typically used in environmental cleaning.28

Phenolic agents were used in one pre-post intervention study in a large Thai tertiary care hospital. In the baseline period, no interventions were performed other than standard infection control practices. In the second intervention stage, sodium hypochlorite (bleach) was used for environmental cleaning. In the third intervention stage, phenolic agents with detergent were used for environmental cleaning instead of bleach, without any other changes to the intervention.

Compared with the pre-intervention period, the second stage that used sodium hypochlorite had a 67 percent reduction in colonization and infections by pandrug-resistant A. baumannii (from 3.6 to 1.2 cases per 1,000 patient-days; p<0.001) and the third stage using phenolic agents with detergent had a 76 percent reduction in infections and colonizations (from 3.6 to 0.85 cases per 1,000 patient-days; p<0.001).16

A separate before-and-after study tested similar stages for control of extensively drug-resistant A. baumannii (XDR-AB). The same researchers found that the use of sodium hypochlorite decreased clinical and surveillance isolates of XDR-AB compared with the use of detergent-disinfectant in the baseline period. The rate decreased from 11.1 to 1.74 cases per 1,000 patient-days for clinical isolates (p<0.001); and from 2.11 to 0.98 per 1,000 patient-days for surveillance isolates (p<0.001).8

5.4.3.1.7. No-Touch Disinfection Methods

While traditional methods of disinfection require the manual application of chemicals to a contaminated surface, new no-touch disinfection methods are being developed. These techniques often supplement existing cleaning and disinfection policies or are implemented in outbreak situations in which routine cleaning practices have not been sufficient to reduce transmission. The two most common no-touch disinfection methods are hydrogen peroxide vaporization (HPV) and ultraviolet light-C decontamination (UV-C). We also briefly discuss studies about no-touch methods that use gas plasma, argon, helium, hydrogen peroxide/peracetic acid, and steam.

Ultraviolet disinfection was investigated by one before-and-after study, one cluster-randomized crossover study, three in vitro studies, two systematic reviews, and three nonsystematic reviews. One systematic review recommended that no-touch technologies such as UV (wavelength range not specified) should be used to augment traditional cleaning methods, especially for C. difficile and VRE.29 A second systematic review stated that there is very low-quality evidence to support the efficacy of UV-C or xenon UV disinfection.30

Only two studies on no-touch methods included in this review took place in clinical settings. One before-and-after study found that UV-C radiation at close range was effective in reducing Gram-negative bacilli, C. difficile, S. aureus, and Enterococcus on computer keyboards.31 The other study, a cluster-randomized crossover study found that adding UV-C room decontamination after standard cleaning reduced incidence of several target organisms, including three MDROs and C. difficile. The incidence of colonization or infection among exposed patients was lower after the addition of UV-C disinfection (relative risk [RR] 0.70, 95% CI 0.50–0.98; p=0.036).18

Two in vitro studies found UV-C disinfection effectively reduced bacterial load on environmental surfaces, although both concluded that the technology was more effective against MRSA than for Candida or C. difficile.32,33 Presence of organic matter was also found to reduce UV-C efficacy,33 indicating the importance of thoroughly cleaning soiled surfaces before UV-C disinfection.

Another study in a laboratory setting found 405 nanometer violet light (a slightly longer wavelength than UV light) was effective in reducing presence of ampicillin-resistant E. coli.34 In summary, some evidence suggests that UV disinfection of patient rooms can reduce hospital-acquired infections caused by common MDROs and C. difficile, but much of the evidence comes from laboratory research and not clinical settings. In addition, standard cleaning and disinfection practices should be augmented and not replaced by this technology, especially if there is soiling of the surface being disinfected.

HPV was the focus of five before-and-after studies, one prospective cohort study, one cluster-randomized crossover study, and one systematic review. The five before-and-after studies3539 found HPV effectively reduced contamination from MRSA (two studies), VRE (one study), multidrug-resistant A. baumannii (four studies), multidrug-resistant Gram negative bacteria (MDR-GNB) (one study), and OXA-48 carbapenemase-producing Enterobacteriaceae (one study). HPV was also found to inactivate spores and to be effective for both porous and nonporous surfaces.35

A cluster-randomized crossover study by Blazejewski et al. (2015) found that HPV reduced MDRO contamination in patient rooms.40 A prospective cohort study found patients admitted to rooms decontaminated using HPV were 64 percent less likely to acquire any MDRO (p<0.001) and 80 percent less likely to acquire VRE (p<0.001); acquisition of C. difficile, MRSA, and MDR-GNB were also reduced, although not statistically significantly.n In addition, one systematic review found evidence to support HPV effectiveness in decreasing VRE colonization and infection.29 The studies suggest that HPV room decontamination both reduced environmental contamination by MDROs and MDRO transmission/acquisition in healthcare facilities.

Other no-touch technologies were each mentioned by one study, and additional research and evidence are needed before their safety and efficacy can be validated for use in reducing MDROs in healthcare settings. First, in a laboratory setting, Park et al. (2015) demonstrated that two types of plasma (an ionized gas), argon gas-feeding dielectric barrier discharge and nano-second pulsed plasma, effectively inactivated sensitive and resistant bacteria. The article did not discuss implementation or clinical applications.41

Helium and helium-air plasma are two other plasma decontamination technologies that were found by one in vitro study to reduce S. aureus and methicillin-resistant bacteria on glass surfaces,42 but this technology was not effective for C. difficile spores. One last plasma technology, hydrogen peroxide gas plasma, was used as part of a multicomponent infection control intervention to stop an outbreak of XDR-AB in an Italian neonatal ICU.26 This plasma technology successfully decontaminated the assisted-ventilation equipment that was partially implicated in the outbreak.

Another technology, aerosolized hydrogen peroxide and peracetic acid, had similar efficacy as HPV, in one cluster-randomized crossover study in a French ICU.40 Lastly, steam vapor has been tested in laboratory studies on MDROs and has been found to be successful at decontaminating glass surfaces, even in the presence of organic matter.43

At present, HPV and UV decontamination are the most well-studied no-touch technologies and are discussed in the implementation section below because they differ in the time and effort each requires in a clinical setting. While other no-touch technologies have been developed and successfully tested in vitro to disinfect surfaces contaminated with MDROs, more studies will be needed before these can be applied in clinical settings.

5.4.3.2. Tools: Microfiber Cloths and Mops

Three before-and-after studies investigated the use of microfiber cloths in combination with one or more strategies to enhance cleaning. The use of microfiber cloths in daily cleaning and disinfection, in addition to patient cohorting, was implemented in a before-and-after study in a Spanish ICU. Care was taken not to reuse dirty cloths, and clean microfiber cloths were soaked in a bleach solution prior to use. This intervention was associated with a significant reduction in XDR-AB carriage.44

Another before-and-after study found that using microfiber cloths to clean along with fluorescent markers to identify the presence of organic matter to aid with cleaning reduced MDRO environmental contamination of high-touch surfaces significantly, compared with a baseline period.45 As part of another multicomponent intervention, microfiber cloths were used for daily cleaning in an ICU in the United States, resulting in decreased incidence of MDRO infections.9

5.4.3.3. Antimicrobial and Easy-To-Disinfect Objects and Surfaces

While certain contaminated areas are easy to clean and disinfect because of their accessibility and composition (e.g., flat, untextured, nonporous surfaces), other surfaces in a healthcare facility are more prone to harbor bacteria and are more difficult to decontaminate. Several innovations may decrease MDRO contamination of the environment and make cleaning and disinfection more efficient and effective.

In response to an outbreak of A. baumannii, an ICU in the United Kingdom implemented deep cleaning and disinfection, replaced items that were difficult to clean, and devised strategies to prevent contamination of regularly used medical equipment. For example:

  • Patient binders were replaced with plastic-coated binders that could be wiped with disinfectant;
  • Dressing trolleys—movable storage cabinets—were replaced with trolleys that had sealable doors to ensure they were only externally decontaminated; and
  • Single-use bags were used to store equipment that was previously exposed. No additional cases of A. baumannii occurred after these interventions.14

Although not statistically rigorous, this study demonstrates that innovative strategies that replace everyday objects and tools can reduce MDRO transmission and make environmental disinfection simpler and more efficient.

Textiles, especially those frequently touched by infected or colonized patients (e.g., gowns, bed sheets, and blankets), can become contaminated and may be overlooked during standard cleaning operations. Two studies evaluated interventions that included replacing, decontaminating, or improving the antimicrobial properties of textiles found in patient rooms.

One before-and-after trial by Lee et al. (2017) disinfected all textiles and nurses’ clothing in addition to other objects and surfaces with Bio-Kil (3-[Trimethoxysilyl] propyloctadecyldimethyl ammonium chloride), and found a statistically significant decline in the environmental bacterial burden compared with control rooms without this extra disinfection.21

Copper-oxide-impregnated woven linens were tested in six hospitals in a before-and-after study (the only textile intervention that was not combined with other interventions).46 This fabric was used to produce patient gowns, pillowcases, sheets, washcloths, towels, and blankets. Compared with a prior period, after 180 days, there was a statistically nonsignificant 36.4 percent reduction in HAIs caused by MDROs (p>0.05). Using the combined metric of HAIs from both MDROs and C. difficile, the intervention had a statistically significant 39.9 percent reduction (p<0.05).

The use of antimicrobial materials for environmental surfaces was mentioned in one systematic literature review. Copper or silver ion surfaces were found by Tacconelli et al. (2014) to have ambiguous support in the literature reviewed in their study.1

5.4.4. Implementation

Overall, many of the studies reviewed included environmental cleaning and disinfection as part of a multicomponent intervention. With the use of multicomponent interventions, it is difficult to attribute the success of the intervention to any one component. However, in general, multicomponent interventions have been demonstrated to be very effective when measuring reductions in a variety of MDRO-related clinical outcomes. In one systematic review, researchers found that environmental cleaning interventions were most effective when implemented in conjunction with antimicrobial stewardship, evaluation of standard care, and source control for reducing acquisition of several MDROs.47

5.4.4.1. No-Touch Disinfection Implementation

In a cross-sectional survey of healthcare workers and patients in a hospital testing UV-C disinfection, 84 percent responded that the purpose of UV-C room decontamination was well explained to them. However, 39 percent of responding patients had at some time refused UV-C disinfection in their room or bathroom due to not feeling well (25%), wanting to sleep (13%), not wanting to be bothered (11%), and not liking the smell (5%).48 This survey demonstrates the importance of educating patients that may be affected by no-touch disinfection interventions that take place in occupied patient rooms.

Time requirements need to be considered when selecting no-touch disinfection methods. HPV requires sealing off rooms and vents and can take as long as 1 hour and 45 to run. However, HPV is a favored no-touch method for some who cite its advantages of portability, lack of harmful residue, and low vapor temperature.38

5.4.4.2. Environmental Screening Methods

Detecting the presence of MDROs in the environment can be helpful as a tool to audit the thoroughness of cleaning and disinfection, determine a source of contamination and targeted cleaning and disinfection during outbreaks,49 and test or compare methods of cleaning and disinfection.

Healthcare facilities can monitor the thoroughness and efficacy of cleaning and disinfection by testing for MDROs on environmental surfaces using fluorescent gel, microbial culturing, UV detectable powder, or ATP detection. For example, fluorescent gels and powders are visible only with UV light and can be applied to a variety of surfaces before environmental cleaning to illuminate surfaces that are missed.

We reviewed six studies that used one of these methods to monitor cleaning and disinfection thoroughness. Five studies used microbial cultures to monitor cleaning7,20,4951 and three studies used UV-detectable powders or gels for monitoring purposes.22,49,50

In outbreak and endemic settings, environmental screening may be useful in some situations, for example, to help determine a point source of contamination contributing to new cases or to enhance general cleaning and disinfection to prevent additional cases. One systematic review recommends environmental screening only if standard infection control practices (e.g., contact precautions, enhanced cleaning and disinfection) fail to stop an ongoing outbreak.1

Microbial culturing as a method of environmental screening is helpful in endemic situations where the environmental strain must be compared with the outbreak strain to understand their relatedness. ATP testing can also differentiate between bacterial species, although it does not provide an isolate that can be sequenced to compare strains. Five studies in this review used microbial culturing in outbreak or endemic situations to locate point sources contributing to new cases, or gaps in routine cleaning, and target those surfaces for disinfection.7,11,20,52,53

In addition, two studies used environmental screening to inspect rooms for bacterial contamination before new admissions. If any samples were positive, new patients were not admitted to those rooms. These studies used microbial culturing27 and ATP detection9 for this purpose. However, microbial culturing can take hours to complete after collection of environmental samples, and although fluorescent substances provide a real-time method of monitoring cleaning practices, they are not as useful in detecting the presence of bacteria.

5.4.4.3. Unintended Outcomes

Deep environmental cleaning of patient rooms, cleaning or replacement of equipment, and other major changes or interventions can impact daily activities within healthcare facilities. During an outbreak, one ICU had to relocate all patients for 1 week during an intensive cleaning, with accompanying logistical challenges and inconveniences.14

The implementation of no-touch technology for room decontamination has budget and staffing implications. As mentioned by Haas et al. (2014), the regular use of technology such as UV disinfection requires planning to ensure that resources are not depleted, staff are trained and available, and attention is not diverted from other tasks and responsibilities.54

It is important to assess the appropriateness of a cleaning or disinfection strategy for the specific pathogens of concern in a facility. One report by Passaretti et al. (2013) noted that HPV demonstrated “incompatibility” with the paint in some hospital rooms. It may be prudent to investigate compatibility of new disinfection methods with paint or other sensitive surfaces in rooms where they will be used.55 Testing could also be done in a small number of rooms before widely implementing a new technique, to avoid widespread damage.

In general, efficacy against MDROs should not be the only outcome of interest in laboratory or preliminary clinical studies. Biodegradability, toxicity, and phenotypic changes to pathogens of interest should be studied and considered when introducing new chemicals or technologies.

A cross-sectional study of environmental service workers in U.S. hospitals found that only 60 percent of respondents reported “always” knowing the type of isolation precautions to be followed when entering a room to perform terminal cleaning; 27 percent also responded that they were “often” or “always” worried that cleaning products might be harmful to them.56 These responses highlight the importance of the health and safety of staff performing environmental cleaning and disinfection.

5.4.4.4. Education, Monitoring, and Feedback

Education, reeducation, monitoring, and feedback all contribute to successful interventions. One before-and-after study examined a monitoring and feedback program for 27 facilities and their environmental cleaning staff. After an initial education period and several feedback cycles of analysis and objective performance feedback, thoroughness of cleaning improved from 50 percent of surfaces cleaned to 85 percent of surfaces cleaned.57

In another before-and-after trial, staff were reeducated with detailed instructions for cleaning and disinfection. This approach resulted in decreased incidence of carbapenem-resistant K. pneumoniae.10 Reeducation was also featured in other studies found in this review.12,52 A modeled intervention study also found that improving terminal cleaning thoroughness reduced patient acquisition of MDROs.58

Monitoring and feedback can help address any confusion that environmental cleaning workers may have. In a cross-sectional study of U.S. hospital environmental workers, 28 percent reported “never” or “sometimes” knowing when to use UV disinfection, 37 percent reported that it was “always” clear what items they were responsible for cleaning, 39 percent reported that they “often” or “always” avoided cleaning near patients to avoid disturbing them, and 40 percent reported that the over-bed table was “often” or “always” too cluttered to clean properly during daily cleaning.56

Monitoring and feedback of daily cleaning and disinfection practices could help identify and change these simple lapses in cleaning procedures and reduce HAIs. Unannounced audits were implemented in one outbreak study to encourage ongoing, thorough cleanliness.14 After a pass rate was achieved for 3 consecutive weeks, auditing was stopped. This strategy could be useful for improving thoroughness of cleaning and during the initial phase of implementing new practices or policies.

Specific staff training to target problematic practices has also been studied in effective before-and-after study interventions. One study in a U.S. hospital used an initial observation period to identify problem areas, then educated staff on hemodialysis-related cleaning and disinfection and avoiding cross-contamination with personal objects.49 Paired with other changes, this intervention significantly reduced colonization with K. pneumoniae carbapenemase-producing isolates.

Monitoring and auditing can be done via visual inspection of cleaning and disinfection practices or with the use of any of the environmental screening methods described above. Fluorescent markers and ATP detection are more commonly used for cleaning and disinfection auditing than are microbial cultures.45,49,59

5.4.4.5. Facility Policies

Policy changes in healthcare facilities can also help reduce environmental contamination and improve patient outcomes. In endemic or outbreak situations, some facilities have implemented policies requiring that rooms be certified as clean either by inspection10 or by a series of negative environmental cultures before new patients can be assigned to the vacated room.27 Some facilities also may determine that current cleaning and disinfection practices are insufficient and choose to revamp entire policies for environmental cleaning and disinfection. This approach is most common in outbreak situations when traditional practices have not been enough to stem transmission.51,53

With the implementation of no-touch disinfection technologies or other labor-intensive interventions, management may need to readjust staffing and assignments49,60 and otherwise ensure appropriate staffing levels. These changes in policies may require additional staff education (e.g., how to set up a room and use an HPV machine) or additional funding for new staff or equipment purchases.54,59

5.4.4.6. Resources To Assist With Implementation

The following resources include information on environmental cleaning, monitoring, program implementation, and other infection control:

5.4.5. Gaps and Future Directions

Most of the evidence presented above is taken from outbreak studies and before-and-after interventions or from in vitro studies, and the evidence is weak to draw conclusions about efficacy and implementation. Randomized studies are a more rigorous approach and should ideally be designed with one or two variable changes between the study and control groups. Multicomponent interventions make it difficult to understand which specific elements are responsible for success. More single intervention studies on environmental cleaning for MDROs would be useful.

Of particular importance for future research is comparing disinfectants for use in environmental disinfection. A handful of studies have found that QACs reduce environmental contamination with MDROs and provide residual antimicrobial properties. Although they are low toxicity to humans, evidence is mixed to support their usefulness in disinfecting high-touch surfaces and textiles that are in close contact with HCWs and patients. In addition, they cannot be used for spore-forming organisms, such as C. difficile, and are not yet used or studied as commonly as sodium hypochlorite. Lastly, many of the no-touch disinfection technologies are relatively new and have not been rigorously compared with traditional cleaning methods in clinical settings to determine which are most advantageous.

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5.5. PSP: Minimizing Exposure to Invasive Devices and Reducing Device-Associated Risks

Authors

Editors: Katharine Witgert, M.P.H. and Sam Watson, M.H.A.

Key Findings

  • Using devices minimally and appropriately and practicing hygiene and infection control precautions when inserting them are basic steps that can be taken to reduce device-associated infections.
  • Further research is needed to determine the safest and most effective uses of antimicrobial locking solutions and catheter materials.
  • Antimicrobial resistance has not been eliminated as a concern when using antibiotics in antibiotic locking solutions, impregnated catheters, or prophylactic treatment to prevent infections.
  • Ongoing implementation education, monitoring, and feedback for medical staff, patients, and caregivers are recommended for improving adherence to recommended PSPs.

An invasive device is any medical device that is introduced into the body, either through a break in the skin or an opening in the body. Invasive devices include catheters, such as urinary catheters or central venous catheters, and endotracheal tubes used for mechanical ventilation. Medical catheters are tubes that serve purposes such as administering fluids, blood products, medications, and nutritional solutions; providing hemodynamic monitoring; and collecting urine and measuring urinary output.1,2,o Endotracheal tubes are inserted into a patient’s trachea to provide an unobstructed passageway for oxygen and other gases (e.g., anesthesia) while a patient is mechanically ventilated.

The use of invasive devices in patients, while often medically necessary, has been associated with increased risk of invasive infections (e.g., bloodstream infections) and overall mortality.3 From 2011 to 2014, catheter-associated urinary tract infections (CAUTIs), central-line associated blood stream infections (CLABSIs), and ventilator-associated pneumonias (VAPs) accounted for 38 percent, 24 percent, and 2 percent of all healthcare-associated infections, respectively.4 The treatment of these infections is often complicated by resistance to commonly used antibiotics. Within these three categories of infections (i.e., CAUTIs, CLABSIs, and VAPs), the percentage of pathogens that exhibited drug resistance varied depending on species and antibiotic, but an estimated 14 percent were caused by an antibiotic-resistant pathogen.4

5.5.1. Practice Description

Because medical devices provide direct access for bacteria to enter the human body, they pose a significant risk for invasive MDRO infections. Although many of the studies in this review focus on infections that are not specifically MDROs, they were included for their relevance to the prevention and control of MDROs. This review identifies and discusses opportunities to reduce device-associated risks during a patient’s care in a health facility. Key findings are presented in the box above.

5.5.2. Methods

To answer the question, “What are the best device reduction and harm minimization practices?” three databases (CINAHL, MEDLINE, and Cochrane) were searched for “catheter-related infections,” “endotracheal tubes,” and synonyms in combination with “infection control,” “microbial drug resistance,” and associated phrases. Articles from 2009 to December 2018 were included.

The initial search yielded 396 results; after duplicates were removed, 342 were screened for inclusion, and 139 full-text articles were retrieved. Of those, 17 were selected for inclusion in this review. Articles were excluded if they were outside the scope of this review, included insufficient detail on a PSP, were unable to be retrieved, or were used in the review of another PSP.

General methods for this report are described in the Methods section of the full report.

For this patient safety practice, a PRISMA flow diagram and evidence table, along with literature-search strategy and search-term details, are included in the report appendixes A through C.

5.5.3. Review of Evidence

The resulting 17 studies that were selected for review include 6 systematic reviews, 4 laboratory studies, 3 before-and-after intervention studies, 3 retrospective cohort studies, and 1 randomized control trial. The six systematic reviews included studies from various international settings. Of the 11 individual studies, 5 took place in the United States or its territories, and 6 took place abroad.

The settings for these individual studies include patient homes, surgical wards, ICUs, dialysis units, tertiary care hospitals, teaching hospitals, and laboratories. The settings covered in this review span community and primary care, long-term acute care hospitals, rehabilitation centers, hospitals, and general healthcare settings.

5.5.3.1. Least Harmful Device Use—Catheters

To reduce the harms associated with catheter use (intravascular or urinary catheters), interventions can target several stages of their use:

  • Avoiding unnecessary and inappropriate catheter use,
  • Ensuring aseptic placement of catheters,
  • Maintaining awareness and proper care of catheters in place, and
  • Promptly removing unnecessary catheters.5

A systematic review by Patel et al. (2018) reviewed 102 studies with interventions aiming to reduce CAUTIs and CLABSIs. The review determined that the most successful interventions targeted multiple stages. For both CAUTIs and CLABSIs, successful interventions included protocols to remove by default based on certain criteria (e.g., time).5 Other aspects of successful interventions (e.g., monitoring, auditing, and staffing) will be addressed in section 5.5.4.

The CDC also has a published set of guidelines for reducing both intravascular catheter-related infections and CAUTIs.1,6 These guidelines have various recommendations for reducing harm throughout the phases of the patient’s care, including:

  • Timing of catheter placement,
  • Selection of the appropriate catheter device,
  • Use of hand hygiene,
  • Aseptic technique strategies,
  • Barrier precautions during device placement and care, and
  • Use of systemic antibiotics (not recommended) and antibiotic lock solutions.

Several of these interventions will be addressed below, with additional information provided in section 5.5.4.4.

5.5.3.1.1. Urinary Catheters

Specific to urinary catheters, Mody et al (2017) conducted a large-scale before-and-after intervention study of 404 nursing homes that implemented a multicomponent strategy that included targeting multiple stages of device use. This study of community-based nursing homes used the Comprehensive Unit-based Safety Program (CUSP) toolkit for CAUTI, developed as part of the Agency for Healthcare Research and Quality Safety Program for Long-Term Care. The intervention targeted urinary catheter removal, aseptic insertion, incontinence care planning, and various training programs for staff, patients, and family.

The intervention reduced UTIs, perhaps indicating success in aseptic techniques, but did not reduce overall catheter utilization. The authors theorized that catheter utilization in nursing homes across the country was already relatively low at the start of the study, leaving little room for further reductions.7

The low utilization of urinary catheters in nursing homes was also confirmed in a systematic review by Meddings et al. (2017). The same review found that nursing home interventions involving improving hand hygiene, reducing catheter use, and enhancing barrier precautions were all effective at reducing UTIs in nursing home residents.8 In an ICU setting, Patel et al. (2018) assessed that many successful interventions included a focus on removing a urinary catheter.5

Another systematic review compared methods of short-term (14 days or less) bladder catheterization (indwelling urethral catheterization, intermittent urethral catheterization, and suprapubic catheterization) in hospitalized adults.9 For the outcome of UTI, evidence was not sufficient enough to support the use of one route of catheterization over the others to reduce infections.

Meddings et al. (2015) used the RAND/UCLA Appropriateness Method, a method for evaluating the appropriateness of medical technology, to refine criteria for the use of urinary catheters (indwelling Foley catheters, intermittent straight catheters, and external condom catheters) in hospitalized medical patients. Using the literature, the authors developed a list of potential indications for each catheter type and created different scenarios illustrating their use. A multidisciplinary panel of subject matter experts ranked the scenarios as appropriate, inappropriate, or uncertain; appropriateness is defined as use for which benefits outweigh risks. The authors conclude that Foley catheters should only be used to measure urine or manage incontinence if other methods have been exhausted or if there are medical indications where nonbarrier methods would increase harm (e.g., to improve healing of sacral ulcers).10

5.5.3.1.2. Intravascular Catheters

With respect to intravascular catheters, certain patient safety practices can be used to reduce the risk of infection when vascular access cannot be avoided. The practices included in our review focus on the use of antibiotics or specialized catheters that contain antimicrobial substances. The section below discusses these practices in further detail and their implications for antimicrobial resistance and other potential patient harm.

The CDC guidelines for preventing intravascular catheter-related infections provide recommendations for antibiotic and antiseptic use.6 In general, for intravascular catheters, the CDC does not recommend the use of systemic antimicrobial prophylaxis. Instead, the CDC recommends the use of certain antiseptic ointments at the catheter exit site for dialysis catheters and recommends antibiotic locking solutions (discussed below) in certain situations.6 For details on the strength of the evidence for each of these recommendations, please view the CDC guidelines referenced in section 5.5.4.

Regarding site placement of central venous catheters (CVCs), one systematic review of published ICU infection outbreaks found strong evidence to support the use of subclavian insertion sites compared with jugular or femoral sites to reduce the risk of CLABSI.11 This practice is strongly supported by the CDC guidelines to avoid use of jugular or femoral insertion sites.6

As with most medical procedures that are physically invasive, sanitary practices are necessary and may reduce the risk of infected wounds and invasive infections. While no study in this review specifically addressed sanitary practices as an intervention, the CDC guidelines include detailed instructions on appropriate infection control procedures for intravascular catheters.6 The strongest CDC recommendations include:

  • Using sterile gloves when inserting arterial, central, and midline vascular catheters;
  • Frequently performing hand hygiene,
  • Using sterile gauze or sterile, transparent, semipermeable dressing to cover the catheter site; and
  • Using chlorhexidine antisepsis for insertion sites in specific cases (see guidelines for details).6

One method of combating invasive infections associated with catheters is to reduce and restrict the growth of bacteria within the catheter itself. Bacteria often form biofilms within catheters that can inhibit catheter function and increase the risk of infection. In addition to preventing bacterial infections and biofilm formation, antibiotic lock (ABL) therapy reduces costs and vein damage associated with device replacement. ABL therapy is the insertion of a concentrated antibiotic solution into a catheter lumen (its internal channel or tube) to prevent the development of microbial biofilm on catheter surfaces.

In a study by Dixon et al. (2012), ABL therapy, as an adjunct to systemic antibiotic therapy, vs. systemic antibiotic therapy alone in patients with tunneled hemodialysis catheters, reduced CLABSI incidence by over 50 percent (RR 0.50 +/− 0.03; p<0.0001) and reduced treatment failure and relapses in the study group compared with the control group.12 The CDC recommends that ABL prophylaxis only be used for hemodialysis patients with long-term catheters who have a history of multiple CLABSIs despite appropriate aseptic techniques during catheter care and insertion.6

In two studies identified in this review, no antibiotic resistance was found to be associated with their use in ABLs. One retrospective cohort study in the homes of patients in the Netherlands found taurolidine to be safe for up to 702 days.13 Another retrospective cohort study in a dialysis unit in the United Kingdom found no increased risk of drug resistance when using vancomycin and gentamicin ABL solutions paired with systemic vancomycin and gentamicin.12 However, increased prevalence of S. aureus and antimicrobial-resistant Enterobacteriaceae was found.

5.5.3.1.3. Catheter Innovations To Reduce Risk of Infection

Various catheter materials have been studied to determine their effectiveness at reducing biofilm formation and preventing catheter-related infections. Urinary catheters can be made of hydrophilic materials—which reduce friction during insertion, thus reducing the need for lubrication and the risk of urethral damage—or impregnated with antimicrobial chemicals to prevent colonization of the catheter with bacteria or fungi. Catheters can be constructed of latex, silicone, or other components; however, antimicrobial silver alloys may bind more readily to latex than to other materials.14

Table 5.7 summarizes the evidence found in two systematic reviews and five studies regarding the use of alternative urinary and intravascular catheter materials and antimicrobial-impregnated catheters. Three technologies were found to be successful in laboratory experiments: gum arabic capped-silver nanoparticle-coated devices15; catheters impregnated with rifampicin, triclosan, and trimethoprim16; and CVCs impregnated with minocycline and rifampicin (M/R) + chlorohexidine (CHX).17 One review found gel reservoir and hydrophilic catheters to be safer than traditional sterile noncoated catheters.18

Silver-impregnated catheters were determined to have mixed evidence.11 Catheters impregnated with both silver and chlorohexidine have been demonstrated to reduce colonization and CLABSIs, especially in settings with high background rates of CLABSIs11 and are highly recommended by CDC if the CVC is expected to stay in place for more than 5 days.6

Lastly, M/R-impregnated catheters were the most well studied, cumulatively mentioned in five different abstracted articles. Use of these antimicrobial catheters was backed by one laboratory study19 and one retrospective cohort study.20 One systematic review concluded that evidence was mixed to support the use of M/R catheters.11 Another innovation for increasing catheter safety is the use of needleless connectors, which were mentioned in one review as having mixed evidence regarding their efficacy.11

While some studies found a reduction in catheter contamination with needleless connectors, others observed an increase in infection rates temporally associated with their introduction. If needleless connectors are used, the CDC strongly recommends that an antiseptic be used to scrub the access port and that it be accessed only with sterile devices.6

The CDC guidelines previously referenced also include recommendations on urinary catheter materials. The CDC acknowledges the benefits of antibiotic-impregnated or antiseptic-impregnated urinary catheters in certain situations but also addresses a mix or lack of evidence demonstrating that they reduce UTI. The CDC also states that silicone and hydrophilic catheters may be preferable in certain situations (e.g., hydrophilic catheter use for intermittent catheterization).1

Table 5.7. Studies of Alternative Materials and Antimicrobial-Impregnated Catheters.

Table 5.7

Studies of Alternative Materials and Antimicrobial-Impregnated Catheters.

5.5.3.2. Reducing Ventilator-Associated Infections

A small number of articles identified and abstracted in this literature review focused on ventilator-associated infections, mainly referring to pneumonia. This is not an intensive review of ventilator-associated infection reduction, but several PSPs were identified as well-supported or somewhat supported by the current literature to reduce risk of infection. The references listed below have up-to-date recommendations.

Supraglottic suction refers to suctioning that removes bacteria-laden secretions to reduce the risk of aspiration pneumonia or upper-respiratory tract pneumonia. A systematic literature review by Doyle et al. (2011) found that the current literature supported the PSP of supraglottic suction in a patient’s endotracheal tube. Doyle et al. (2011) also found overall support in the literature for bed elevation of 30 to 45 degrees for mechanically ventilated patients. Finally, Doyle et al. (2011) found supporting evidence for selectively decontaminating patients’ digestive tract to prevent VAPs. All three of these PSPs—supraglottic suction, bed elevation, and selective decontamination—aim to reduce aspiration of bacteria in respiratory fluid and thus reduce pneumonia in ventilated patients.11

Subglottic secretion suctioning is a similar method to reduce ventilator-associated infections and was found by one randomized control study to be associated with lower rates of VAP and overall lower length of required ventilation.21

The same systematic literature review found only mixed evidence to support using topical antibiotics to decontaminate the oropharynx of patients on mechanical ventilation.11 A before-and-after intervention study of 925 patients in an ICU administered polymyxin/tobramycin/amphotericin B in the oropharynx and the gastric tube plus a mupirocin/chlorhexidine regimen in all intubated patients. This regimen lowered the incidence rates of intubation-related pneumonia (5.1 vs. 17.1 per 1,000 ventilator-days; p<0.001) in the experimental group.22

The Society for Healthcare Epidemiology of America (SHEA) and Infectious Diseases Society of America (IDSA) guidelines, “Strategies to Prevent Ventilator-Associated Pneumonia in Acute Care Hospitals,” includes several recommendations covering the topics addressed by this literature review, as well as other PSPs. The recommendations are delineated for different populations (e.g., adults vs. neonates) and can be viewed at the link referenced in section 5.5.4.4 below.

The SHEA/IDSA guidelines state that there is moderate evidence to support the use of endotracheal tubes with a subglottic suction catheter for patients ventilated for more than 2 to 3 days but do not recommend closed/inline endotracheal suctioning. These guidelines also note that the quality of evidence was low to support the bed elevation discussed by Doyle et al. and that the quality of evidence was high for selective oral or digestive decontamination.

Additional guidelines from the SHEA/IDSA publication suggest additional PSPs for adult patients. PSPs with high quality of evidence include:

  • Assessing the readiness to extubate daily,
  • Interrupting sedation daily,
  • Performing spontaneous breathing trials with sedatives turned off, and
  • Changing the ventilation circuit only if visibly soiled or malfunctioning.

PSPs with moderate quality of evidence include managing patients without sedation whenever possible, facilitating early mobility, administering regular oral care with chlorhexidine, and providing prophylactic probiotics.23

5.5.3.3. Evaluation and Monitoring of Device Use

To reduce duration of device use, clinicians often must regularly reevaluate the need for the device and monitor any changes (e.g., the patient’s dependence on the device). In the previously referenced systematic review, Patel et al. (2018) found that successful interventions aiming to reduce CLABSIs and CAUTIs often used checklists, auditing, and monitoring and focused on removal of devices. These checklists and monitoring procedures help reduce human error during the maintenance and removal of devices.5

The CDC guidelines for intravascular catheters also provide recommendations on device removal and care. These include assessment of an insertion site infection, removal of unnecessary catheters, quick replacement of catheters when aseptic technique cannot be ensured, and appropriate length of time to use certain types of catheters (e.g., up to 14 days for umbilical venous catheters).6

The CDC also has various recommendations on the evaluation and monitoring of device use for urinary catheters. These guidelines include the removing urinary catheters for operative patients as quickly as possible (<24 hours if possible), reducing kinking and obstruction of catheter tubes, and implementing guidelines to advise on proper catheter maintenance.

Lastly, the SHEA/IDSA guidelines include several recommendations on evaluation and monitoring of ventilator use. Some of these recommendations include changing the ventilator circuit if it is visibly soiled or malfunctioning, minimizing breaks in the ventilator circuit, and assessing the readiness to extubate daily. These recommendations are expanded on and delineated for certain populations in the full report, which can be viewed at the link provided in section 5.5.4.4 below.23

5.5.4. Implementation

5.5.4.1. Unintended Outcomes

Some of the above interventions, such as ABL solutions, topical skin ointments, and oropharynx decontamination involve the use of antibiotics. As with any antimicrobial use, overuse and inappropriate use can lead to increased drug resistance and increased risk of MDRO colonization or infection.

Regarding ventilator-associated antibiotic use, one before-and-after study discussed the effectiveness of selective digestive decontamination using polymyxin, tobramycin, and amphotericin B in the oropharynx and the gastric tube plus a mupirocin and chlorhexidine regimen in intubated patients. This study maintained that use of antibiotics in this scenario did not confer antibiotic resistance, but evidence showed that this practice increased the risk of MRSA infection and tobramycin resistance in aerobic Gram-negative bacilli such as P. aeruginosa and Enterobacteriaceae.22 The SHEA/IDSA guidelines recommend that facilities with high levels of antimicrobial resistance not use digestive decontamination until higher quality, long-term studies are performed to assess the risks.23

Regarding ABL solutions, a retrospective cohort study in a dialysis unit found that after vancomycin and gentamicin catheter lock solutions were used, there was no statistically significant evidence of increased antimicrobial resistance. However, there was some change in the antimicrobial resistance profiles of monitored pathogens, showing that the drug pressure did influence microbial flora and may need to be studied for longer periods.12

Another study investigated resistance to the antibiotic taurolidine and found that it was safe for use for up to 1,394 days. Resistance to the drug was most commonly seen in Candida albicans, although bloodstream infections were more commonly caused by S. aureus and other Staphylococcus species.13 Although there is some evidence of the interaction of antibiotics in locking solutions and a patients’ microflora, the CDC suggests (as a lower priority guideline) ABL prophylaxis, antimicrobial catheter flush, and catheter lock prophylaxis only for high-risk patients. High-risk patients have long-term catheters, have a history of CLABSI, and already adhere to maximal aseptic precautions.6

For intravascular catheters, the CDC states that antibiotic ointments and creams should not be used on insertion sites (other than dialysis catheters) because of the risk of conferring antimicrobial resistance and fungal infections. Chlorhexidine dressings are appropriate in some cases.6

In summary, this review highlighted potential increases in the antimicrobial resistance prevalence of clinically important pathogens. When considering the use of antibiotics to prevent CLABSIs, CAUTIs, or VAPs, clinicians should exercise caution and be diligent about referencing the existing guidelines, which specifically warn against or promote antibiotics for certain uses and populations. Further research is needed on long-term effects of antibiotic use for selective digestive decontamination and long-term use of locking solutions.

5.5.4.2. Cost-Effectiveness

Although not the focus of this section, two articles touched on cost-effectiveness of interventions discussed above. Doyle et al. (2011) found evidence that antibiotic-impregnated catheters were cost-efficient compared with standard catheters in high-risk populations.11

In a systematic review of the evidence to support gel catheters or hydrophilic catheters versus clear noncoated catheters, Bermingham et al. (2013) found that clear noncoated catheters were more cost-effective than single-use gel reservoir catheters. The review identified evidence that these clear noncoated catheters were less effective in preventing UTIs, so this information on cost-effectiveness will be important when considering the implementation of alternative materials.18

5.5.4.3. Interventions and Education To Reduce Device-Related Infection Risk

Ongoing education of patients, staff, and caregivers can also help reduce the harms associated with device use. The CDC recommends several education and implementation interventions for staff and patients to help improve outcomes associated with device use. Further, the CDC advises allowing only individuals (including family and at-home caregivers) trained in appropriate techniques for catheter insertion and maintenance to perform these tasks. Other agency recommendations include quality improvement programs to provide ongoing training for staff on all the PSPs discussed above: automated alerts to reassess the need for device use, written guidelines, auditing and feedback of staff practices, and periodic training on insertion, maintenance, and removal.1

The SHEA/IDSA guidelines also state that staff education can help maintain high levels of compliance with recommended practices. Staff educational activities include workshops, hands-on training, and use of multiple modalities to convey information. Making information accessible in pocket pamphlets, posters, flowsheets, and other readily available modalities is also suggested. Finally, these guidelines state that educating patients and family on ventilator-associated guidelines can help them engage with and support the medical team’s care.23

Within this review, two studies addressed education interventions for preventing CAUTIs. In a multifacility intervention within U.S. nursing homes, Mody et al. (2017) found success in reducing CAUTIs with a multicomponent intervention that included patient training on catheter care and a socioadaptive bundle emphasizing leadership, resident and family engagement, and effective communication.7

Lastly, Saint et al. (2016) performed a multifacility before-and-after study of implementation of the CUSP for CAUTI protocol (also known as On the CUSP: Stop CAUTI) to reduce CAUTIs in 603 hospitals across the United States. The multicomponent intervention included staff education on technical and socioadaptive factors, providing feedback to the units on CAUTI rates and catheter use, and addressing gaps in knowledge of urinary management processes.24

5.5.4.4. Resources To Assist With Implementation

The following resources include information on prevention of device-related infections; proper catherization use, duration, and removal; insertion site assessment and infection prevention; and other precautions to be taken when using catheters:

5.5.5. Gaps and Future Directions

Gaps in evidence are listed within the guidelines cited above (e.g., CDC, SHEA/IDSA), and this review identified several gaps that require further research. In addition, further research is needed on the safety and efficacy of novel technologies such as GA-AgNPs,15 the triple antibiotic combination discussed by Bayston et al. (2009),16 and the newly developed M/R + CHX impregnated catheter discussed by Raad et al. (2012).17 Further study is also needed on ABL solutions. Specifically, long-term studies on antibiotics in ABLs are needed to determine the risk of conferring drug resistance and increasing risk of infection.12

Kidd et al. (2015) stated larger sample sizes are needed to create adequately powered studies on alternative catheterization methods, such as suprapubic catheterization and intermittent self-catheterization compared with indwelling urinary catheters.9 These methods are often cited as reducing risk of infections, but further research is needed to confirm and repeat the results of preliminary studies.

References for Section 5.5

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Gould C, Umscheid C, Agarwal E, Kuntz G, Pegues D. Guideline for prevention of catheter-associated urinary tract infections. Atlanta, GA: Centers for Disease Control and Prevention; 2009. https://www​.cdc.gov/infectioncontrol​/pdf​/guidelines/cauti-guidelines-H.pdf.
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Rajdev S, Rajdev B, Mulla S. Characterization of bacterial etiologic agents of biofilm formation in medical devices in critical care setup. Crit Care Res Pract. 2012;2012:945805. doi: 10.1155/2012/945805. [PMC free article: PMC3270516] [PubMed: 22312484] [CrossRef]
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Doyle JS, Buising KL, Thursky KA, Worth LJ, Richards MJ. Epidemiology of infections acquired in intensive care units. Semin Respir Crit Care Med. 2011;32(2):115–38. doi: 10.1055/s-0031-1275525. [PubMed: 21506049] [CrossRef]
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Dixon JJ, Steele M, Makanjuola AD. Anti-microbial locks increase the prevalence of Staphylococcus aureus and antibiotic-resistant Enterobacter: Observational retrospective cohort study. Nephrol Dial Transplant. 2012;27(9):3575–81. doi: 10.1093/ndt/gfs081. [PubMed: 22513704] [CrossRef]
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Olthof ED, Rentenaar RJ, Rijs AJ, Wanten GJ. Absence of microbial adaptation to taurolidine in patients on home parenteral nutrition who develop catheter related bloodstream infections and use taurolidine locks. Clin Nutr. 2013;32(4):538–42. doi: 10.1016/j.clnu.2012.11.014. [PubMed: 23267744] [CrossRef]
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Muzzi-Bjornson L, Macera L. Preventing infection in elders with long-term indwelling urinary catheters. J Am Acad Nurse Pract. 2011;23(3):127–34. doi: 10.1111/j.1745-7599.2010.00588.x. [PubMed: 21355945] [CrossRef]
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Ansari MA, Khan HM, Khan AA, Cameotra SS, Saquib Q, Musarrat J. Gum arabic capped-silver nanoparticles inhibit biofilm formation by multi-drug resistant strains of Pseudomonas aeruginosa. J Basic Microbiol. 2014;54(7):688–99. doi: 10.1002/jobm.201300748. [PubMed: 24403133] [CrossRef]
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Bayston R, Fisher LE, Weber K. An antimicrobial modified silicone peritoneal catheter with activity against both Gram-positive and Gram-negative bacteria. Biomaterials. 2009;30(18):3167–73. doi: 10.1016/j.biomaterials.2009.02.028. [PubMed: 19289248] [CrossRef]
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Raad I, Mohamed JA, Reitzel RA, Jiang Y, Raad S, Al Shuaibi M, et al. Improved antibiotic-impregnated catheters with extended-spectrum activity against resistant bacteria and fungi. Antimicrob Agents Chemother. 2012;56(2):935–41. doi: 10.1128/aac.05836-11. [PMC free article: PMC3264266] [PubMed: 22123686] [CrossRef]
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Bermingham S, Hodgkinson S, Wright S, Hayter E, Spinks J, Pellowe C. Intermittent self catheterisation with hydrophilic, gel reservoir, and non-coated catheters: A systematic review and cost effectiveness analysis. BMJ. 2013;346:e8639. doi: 10.1136/bmj.e8639. [PMC free article: PMC3541473] [PubMed: 23303886] [CrossRef]
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Raad I, Reitzel R, Jiang Y, Chemaly RF, Dvorak T, Hachem R. Anti-adherence activity and antimicrobial durability of anti-infective-coated catheters against multidrug-resistant bacteria. J Antimicrob Chemother. 2008;62(4):746–50. doi: 10.1093/jac/dkn281. [PubMed: 18653489] [CrossRef]
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Ramos ER, Reitzel R, Jiang Y, Hachem RY, Chaftari AM, Chemaly RF, et al. Clinical effectiveness and risk of emerging resistance associated with prolonged use of antibiotic-impregnated catheters: More than 0.5 million catheter days and 7 years of clinical experience. Crit Care Med. 2011;39(2):245–51. doi: 10.1097/CCM.0b013e3181feb83e. [PubMed: 21057308] [CrossRef]
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Damas P, Frippiat F, Ancion A, Canivet JL, Lambermont B, Layios N, et al. Prevention of ventilator-associated pneumonia and ventilator-associated conditions: A randomized controlled trial with subglottic secretion suctioning. Crit Care Med. 2015;43(1):22–30. doi: 10.1097/ccm.0000000000000674. [PubMed: 25343570] [CrossRef]
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Camus C, Salomon S, Bouchigny C, Gacouin A, Lavoue S, Donnio PY, et al. Short-term decline in all-cause acquired infections with the routine use of a decontamination regimen combining topical polymyxin, tobramycin, and amphotericin b with mupirocin and chlorhexidine in the ICU: A single-center experience. Crit Care Med. 2014;42(5):1121–30. doi: 10.1097/ccm.0000000000000140. [PubMed: 24365857] [CrossRef]
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Klompas M, Branson R, Eichenwald EC, Greene LR, Howell MD, Lee G, et al. Strategies to prevent ventilator-associated pneumonia in acute care hospitals: 2014 update. Infect Control Hosp Epidemiol. 2014;35(8):915–36. doi: 10.1086/677144. [PubMed: 25026607] [CrossRef]
24.
Saint S, Greene MT, Krein SL, Rogers MA, Ratz D, Fowler KE, et al. A program to prevent catheter-associated urinary tract infection in acute care. N Engl J Med. 2016;374(22):2111–9. doi: 10.1056/NEJMoa1504906. [PMC free article: PMC9661888] [PubMed: 27248619] [CrossRef]

5.6. PSP: Communication of Patients’ MDRO Status

Authors

Editors: Katharine Witgert, M.P.H. and Sam Watson, M.H.A.

Key Findings

  • Communication failures have been linked to poor patient outcomes, especially for vulnerable patient populations (e.g., immunosuppressed patients).
  • Multimodal and redundant communication policies can improve communication compliance in settings with complex communication (e.g., organ donation) or with multiple care providers (e.g., transfers). Modes of communication can include checklists, brightly colored leaflets attached to medical records, and electronic or automated communication.
  • Revisiting policies to ensure they are meeting a facility’s needs, performing ongoing monitoring and feedback of policy compliance, and involving staff from multiple disciplines in policymaking are all important for improving patient status communication.

A patient’s positive MDRO status must be promptly communicated to patient care staff to ensure proper infection control practices are implemented and to protect patients against improper treatment (e.g., inappropriate antibiotic use). The timely and accurate dissemination of this information to all clinicians, visitors, and others in the facility who interact with those patients protects these individuals against MDRO transmission. Communication of an individual’s past MDRO infections, documented asymptomatic carriage, and relevant high-risk healthcare exposures (such as transfer from a facility with a suspected or identified MDRO outbreak) should occur at every admission or transfer.

Effective communication also requires decisions about who needs to be notified, what information they need, and what privacy concerns exist in sharing this information. As soon as positive laboratory testing results are available, the laboratory should notify key clinicians and infection control personnel. These personnel should then communicate the appropriate precautions to all other staff, visitors, and others whose interaction with patients puts them at increased risk of MDRO acquisition. By implementing effective communication and infection control strategies, each healthcare facility can play a role in preventing local and ultimately global spread of MDROs. Key findings are presented in the box to the right.

5.6.1. Practice Description

The CDC recommends that all facilities have a system in place to communicate a patient’s MDRO status to all necessary personnel before transfer of the patient.1 Communicating a patient’s MDRO status occurs at several points during the patient’s interaction with the healthcare system. Intrafacility communication must begin when a positive laboratory test occurs or is highly suspected based on a patient’s risk or previous exposures. The information must be disseminated to all clinicians interacting with the patient, visitors, and anyone whose patient interaction increases his or her exposure risk.

When patients are transferred between facilities, interfacility communication of patient status is required. Special care and attention to patient status communication must be taken in situations where patients are immunosuppressed and vulnerable to infection and where facilities may not have preexisting relationships or communication channels. Examples of information sharing strategies from case studies include electronic communication, a highlighted or annotated medical record or patient file, a transfer form, a brightly colored leaflet, verbal communication, and an automated alert.

5.6.2. Methods

The question of interest for this review is: What are the methods of MDRO status communication in a healthcare setting?

To answer this question, we searched three databases (CINAHL, MEDLINE, and Cochrane) for “information dissemination,” “information sharing,” “patient transfer,” or “communication” in combination with “cross-infection,” “prevention and control,” “drug resistance,” and relevant synonyms or similar phrases. Articles from 2009 to December 2018 were included.

The initial search yielded 140 results (including 8 from other sources). After duplicates were removed, 128 were screened for inclusion, and 54 full-text articles were retrieved. Of those, we selected 12 for inclusion in this review. Articles were excluded if they were out of scope or had insufficient detail about the topic of status communication or if the full article was not accessible.

General methods for this report are described in the Methods section of the full report.

For this patient safety practice, a PRISMA flow diagram and evidence table, along with literature-search strategy and search-term details, are included in the report appendixes A through C.

5.6.3. Review of Evidence

Of the 12 articles were selected for review, 2 were case studies, 2 were outbreak studies, 2 were cross-sectional studies, 2 were retrospective cohort studies, 1 was a systematic review, 1 was a prospective interrupted time series study, 1 was a prospective observational study, and 1 was a randomized controlled trial. Nine of the 13 included studies that took place in the United States, 1 took place in Australia, 1 took place in Italy, and 1 took place in Denmark. The systematic literature review was a review of German studies.

5.6.3.1. Intrafacility Communication

Timely and accurate dissemination of a patient’s MDRO infection or carrier status is the first step that should be taken to control transmission within a healthcare facility. If a patient is high risk or highly suspected to harbor an MDRO, or if a positive test is received from a clinical laboratory as the result of active screening or routine clinical testing, steps should be taken to communicate the patient’s status to all necessary staff. Examples of ways to communicate a patient’s MDRO status include:

  • Physical signs at the entrance to a patient’s room or at the foot of the bed,
  • Documentation in a patient’s file (e.g., a brightly colored leaflet or note in the front of the file), and
  • Checklists, policies, or electronic notifications that prompt providers to check patients’ MDRO laboratory test results before interacting with and treating them.

In a prospective observational study of 101 inpatient transfers to radiology, Ong and Coiera (2010) identified and quantified the errors that occurred during intrafacility transfer. The Australian teaching hospital used a transfer form for continuity of care and a patient identity verification process when transferring a patient’s care from one individual to another. The most common error that occurred during this process was “inadequate handover,” which occurred 43.1 percent of the time and included a missing transfer form or omitted or incorrect information on the form.

While the results did not specifically report on communication of patient MDRO status, these lapses and inaccuracies in communication demonstrate weaknesses or failures in current practices that likely impact the transfer of knowledge about a patient’s infectious status. This problem is reinforced by the fact that 2.9 percent of transfers had inappropriate infection control precautions, such as contact precautions.2 This study demonstrates that despite an existence of facility policy, implementation and compliance were inadequate, even though four redundant stages of the communication process were identified. Strategies for improving implementation will be discussed in section 5.6.4.

A randomized crossover study in the same hospital compared the use of a checklist with the use of a colored cue card to communicate that a patient was highly infectious. Both strategies improved compliance with infection control precautions similarly compared with the control group (38% compliance). The colored cue card increased compliance to 73 percent, and the pretransfer checklist increased compliance to 71 percent. However, adherence to the checklist was low at 40 percent and was anecdotally reported to be criticized by staff as annoying or redundant.3

One Danish university hospital used a leaflet in the front of each patient file and distributed it to the patient’s visitors, as well as positioning a sign at the patient’s bedpost so that anyone reviewing the file or entering the patient’s room was alerted to the patient’s status and appropriate precautions.4 This hospital placed patients on contact isolation precautions if they were positive for an MDRO, putting the patient in rooms only with other MDRO-positive patients, and using personal protective equipment (PPE) when in direct contact with the patient. This intervention of leaflets and signs contributed to a decrease in the number of patients needing isolation per 1,000 occupied bed-days, which declined from 0.94 (95% CI 0.74 to 1.14) to 0.65 (95% CI 0.43 to 0.87; p=0.021) for ESBL-K. pneumoniae (ESBL-KP). Researchers also noted a reduction in the rate of isolated ESBL-KP from 39.5 percent to 22.5 percent, although this finding was not statistically significant.4

This study showed that improved signage and documentation within a patient’s file can improve compliance with contact precautions, thus reducing transmission and the need for additional patients to be put on contact precautions. Ultimately, reducing the number of patients on contact precautions can allow hospitals to conserve resources, such as single-use gowns, gloves, and individual patient rooms. It can also conserve the time of staff who would otherwise need to don and doff PPE and thoroughly decontaminate surfaces and equipment.

Intrafacility communication can be crucial during an outbreak situation, when communicating a patient’s infection with a highly transmittable pathogen is necessary to implement proper infection control and prevent further spread. Enhanced communication was part of a multicomponent intervention implemented to stem an outbreak of carbapenem-resistant K. pneumoniae among severely immunocompromised ICU patients at the NIH Clinical Center in Maryland.5 An interdisciplinary team held daily staff meetings to discuss the outbreak investigation and control methods, held weekly meetings to share new findings or developments, and provided email notifications with updates and infection control reminders. An information sheet about transmission of MDROs was also given to patients upon admission.

This successful multicomponent intervention included educating staff, patients, and families on proper infection control practices and keeping everybody updated and informed about the selected infection control practices to ensure understanding and compliance. This intervention involved thorough and constant intrafacility communication using electronic, paper-based, and person-to-person communication.5 This case study demonstrates that redundant communication and education through multiple modes were effective at reducing transmission.

The studies above demonstrate several methods of intrafacility communication that contributed to successful interventions. These methods included a visual cue (leaflets, signage), electronic record alerts,6 continuity of care checklists (examples of which can be found in section 5.6.4, and intensive staff involvement and daily communication to heighten awareness during an outbreak among high-risk patients.

5.6.3.2. Interfacility Communication

Patients may be transferred between healthcare facilities for a variety of reasons, including a need for specialty care not offered at the current facility, cost or insurance coverage of medical procedures, or a shift from needing acute care to long-term care. These transfers become moments of vulnerability and possible failed communication regarding the status of a patient who may have an MDRO infection or colonization. Steps should be taken to strengthen communication between facilities in these situations to ensure that transmission does not occur. Specifically, the Council of State and Territorial Epidemiologists recommends that interfacility communication include information on patients’ infection or colonization status, the organism with which they are infected, the recent and current antibiotic treatments used, and risk factors (e.g., invasive medical devices).7

Several outbreaks have been associated with lapses of communication during patient transfers. One outbreak study in Oregon8 identified 21 cases of extensively drug-resistant A. baumannii in patients transferred between several skilled nursing facilities, acute care hospitals, and long-term acute care hospitals. Despite Oregon Health Department’s recommendations for interfacility status communication, diagnosed cases were transferred between facilities with no communication of the patients’ diagnosis. Transmission of the extensively drug resistant pathogen at other facilities was ultimately only detected due to voluntary surveillance and detection of other cases and a subsequent epidemiological investigation. This outbreak was the direct result of ineffective interfacility communication and the resulting failure to implement appropriate infection control practices.8

Oregon’s example cautions that despite policies on interfacility communication, implementation was not adequate and an individual facility’s own active surveillance program was needed to halt an outbreak. Implementation strategies such as periodic audits and monitoring and feedback may help improve compliance with existing facility guidelines.

Medicare and Medicaid require long-term care facilities (LTCFs) to communicate specific information when a patient is transferred to another facility or discharged.9 While this requirement is only for LTCFs, it can be used as an example for other healthcare facilities to ensure proper continuation of care, especially infection control precautions such as contact precautions.

5.6.3.3. Communication During the Process of Organ Transplantation

A unique infection prevention challenge is posed by organ donation. Several organ donation-associated transmissions have been documented, despite existing policies that require communication of positive culture results by organizations such as the United Network for Organ Sharing (UNOS) and the Organ Procurement and Transportation Network (OPTN).10

A retrospective cohort study by Miller et al. (2015) found that poor communication could be implicated in several adverse outcomes after organ transplantation. The researchers investigated 56 infection events due to donor-derived transmission over a 2-year period and found that 18 were associated with errors in communication. Of these 18 infection events, 12 resulted in poor patient outcomes, including 6 deaths.

The communication errors included:

  • A delay in communication of suspected donor-derived infection from the transplant center to the organ procurement organization (OPO) or OPTN,
  • A failure to communicate positive laboratory results from the laboratory to the OPO or OPTN,
  • A delay in communication from the OPO to the OPTN or transplant center, and
  • Incomplete communication or erroneous test results.

This study points out the many complexities of communication in the organ donation process due to the many organizations and players involved. To improve communication during organ transplantation, the authors recommend continuous education of all involved clinicians on communication policies, evaluation and monitoring of compliance and failures in the system, safeguards to prevent errors in medical records or lab result reporting, and expedited donor autopsies and lab results.11

Ariza-Heredia et al. (2012) documented a successful case of interfacility status communication, where four organ recipients were exposed to K. pneumoniae carbapenemase from a donor’s kidney, liver, and heart. The positive culture result of the donor was communicated before the transplants occurred, and appropriate antibiotics and contact precautions were implemented for the two recipients who developed infections. The donor’s institution initially contacted OPTN, who then facilitated the prompt interinstitutional communication.10

In another U.S. case study,12 two kidney transplants failed when the donor’s positive E. coli infection was miscommunicated. The donor’s laboratory results were incorrectly entered into the chart accompanying the donated organ, and no procedure was in place to ensure that the information was correct and communication of those results occurred. To prevent such failures in the future, the authors recommended multiple redundant communication strategies. These strategies include:

  • The donor facility highlighting any positive MDRO results in the charts that accompany an organ,
  • The donor facility noting expected dates of pending test results in documentation accompanying an organ, and
  • Both the donor and recipient facilities following up to obtain any pending test results.

Doublechecking the donor’s medical records for MDRO information is also a prudent step the OPO could take. These interfacility communication procedures and redundancies would protect organ donation recipients from life-threatening infection and failed organ transplants due to improper antibiotic administration or other inappropriate medical care.12

A retrospective cohort study performed in Italy (Mularoni et al., 2015) found that from 2012 to 2013, four organ recipients acquired a carbapenem-resistant Gram-negative bacterial infection due to donor infection that was not communicated, unrecognized, or underestimated.13 This error delayed the appropriate antibiotic treatment for these recipients. In one example, a patient was discharged from an ICU and antibiotic treatment was discontinued due to failed communication of the patient’s positive blood culture result. In another case, a donor had an unrecognized UTI that was detected with a positive urine culture but not communicated to the recipient’s caregivers. Lastly, underestimation of the risk of transmission from the donor’s MDR infection resulted in inappropriate medical treatment of the recipient.

Lapses in communication during organ transplants may pose a serious threat to recipients and can result in rejected or failed organs as demonstrated in these reports. By improving this process of communication, clinicians promote patient safety and can improve post-transplant outcomes.

5.6.3.4. Unintended Consequences

Negative outcomes associated with inefficient or inaccurate status communication were observed in a handful of the studies in this review. A statewide registry created for CRE carriers in Illinois demonstrates a resource burden imposed by a communication system. Participants reported that manual data entry and manual queries for patients were burdensome and time consuming, so researchers are working to create an automated notification system.14

5.6.4. Implementation

As several examples in this review have pointed out, having policies in place does not guarantee effective implementation of patient status communication, be it during transfers, during organ transplantation, or within a facility itself. Engaging staff in new procedures and educating them on the steps involved are all important when applying new policies.

Methods for engaging staff in implementation could include:

  • Performing needs assessments before developing new procedures,15
  • Hosting multidisciplinary meetings to facilitate collaborative thinking or elicit feedback,4,5
  • Distributing reports on infection rates and trends since implementation of communication procedures,4 and
  • Informing managers and other leaders of procedural changes.4

A cross-sectional survey of 448 infection control professionals in the United States reiterates the findings above. The factors that were found to improve implementation included:

  • Distribution of copies of the policy to providers (p=0.03),
  • Use of forms (i.e., checklists) to enhance infection control adherence (p=0.0008),
  • Administrator-directed infection control activities (p<0.0001),
  • A culture of data-driven decision making (p<0.0001),
  • Communication of antimicrobial resistance trends to physicians (p<0.0001), and
  • Interdepartmental coordination of patient care (p<0.0001).16

These tools used for changes in infection control policies can just as easily be applied to interfacility or intrafacility communication of patient MDRO status. Educating providers and staff on new policies by distributing educational resources can be part of continuing education on communication protocols. Checklists can be used to facilitate more thorough information exchange when patients are transferred within a facility. Improved communication and improved coordination of patient care foster an environment more conducive to continuity of information when interfacility communication occurs. Lastly, the reporting of data to demonstrate improvements in patient outcomes can reinforce making positive changes in facility practices that are connected to patient communication.

When implementing interfacility communication protocols, facilities may benefit from reaching out to State health departments or national organizations such as UNOS. Many already have relationships with healthcare facilities, know the appropriate contacts there, and can facilitate meetings or discussions among facilities. For example, the Oregon Health Department helped create a form and process for facilities to use with newly admitted and transferred patients. State health departments should continue to encourage and facilitate interfacility discussion about MDRO communication practices, and smaller local health departments or healthcare facilities should reach out to these larger organizations to ask for assistance in improving intrafacility communications.

5.6.4.1. Resources To Assist With Implementation

Additional resources and tools to aid in the implementation of patient status communication and infection control are listed below.

5.6.5. Gaps and Future Directions

More rigorous research studies in a variety of geographic areas and healthcare settings are needed to evaluate the most effective ways to communicate patient status (e.g., checklists vs. brightly colored leaflets in patient files). Facilities that often exchange patients or are part of larger health systems are encouraged to develop relationships with one another to develop strategies and policies for patient MDRO status communication, if not regulated by the government as in the case of LTCFs.

More research and innovation are needed to promote consistent use of technology-based and paper-based communication of patient MDRO status, such as laboratory results in organ transplantation. Lastly, an iterative review of status communication policies is important to ensure that policies are useful, easy to implement, and meet the needs of the ever-changing world of infection control and prevention.

References for Section 5.6

1.
Siegel JD, Rhinehart E, Jackson M, Chiarello L. Management of multidrug-resistant organisms in healthcare settings, 2006. Atlanta, GA: Centers for Disease Control and Prevention; 2006. https://www​.cdc.gov/infectioncontrol​/guidelines/mdro/index​.html.
2.
Ong MS, Coiera E. Safety through redundancy: A case study of in-hospital patient transfers. Qual Saf Health Care. 2010;19(5):e32. doi: 10.1136/qshc.2009.035972. [PubMed: 20671076] [CrossRef]
3.
Ong M-S, Magrabi F, Post J, Morris S, Westbrook J, Wobcke W, et al. Communication interventions to improve adherence to infection control precautions: A randomised crossover trial. BMC Infect Dis. 2013;13:72. doi: 10.1186/1471-2334-13-72. [PMC free article: PMC3599084] [PubMed: 23388051] [CrossRef]
4.
Andersen SE, Knudsen JD. A managed multidisciplinary programme on multi-resistant Klebsiella pneumoniae in a Danish university hospital. BMJ Qual Saf. 2013;22(11):907–15. doi: 10.1136/bmjqs-2012-001791. [PubMed: 23704083] [CrossRef]
5.
Palmore TN, Henderson DK. Managing transmission of carbapenem-resistant Enterobacteriaceae in healthcare settings: A view from the trenches. Clin Infect Dis. 2013;57(11):1593–9. doi: 10.1093/cid/cit531. [PMC free article: PMC3888298] [PubMed: 23934166] [CrossRef]
6.
Tacconelli E, Cataldo MA, Dancer SJ, De Angelis G, Falcone M, Frank U, et al. ESCMID guidelines for the management of the infection control measures to reduce transmission of multidrug-resistant Gram-negative bacteria in hospitalized patients. Clin Microbiol Infect. 2014;20: Suppl 1:1–55. doi: 10.1111/1469-0691.12427. [PubMed: 24329732] [CrossRef]
7.
Runningdeer E, Kainer M, Johnston H. Interfacility communication to prevent and control healthcare-associated infections and antimicrobial resistant pathogens across healthcare settings. Council of State and Territorial Epidemiologists 2016. https://cdn​.ymaws.com/www​.cste.org/resource​/resmgr/2016ps/16_ID_09.pdf.
8.
Buser GL, Cassidy PM, Cunningham MC, Rudin S, Hujer AM, Vega R, et al. Failure to communicate: Transmission of extensively drug-resistant bla OXA-237-containing Acinetobacter baumannii-multiple facilities in Oregon, 2012–2014. Infect Control Hosp Epidemiol. 2017;38(11):1335–41. doi: 10.1017/ice.2017.189. [PMC free article: PMC5783543] [PubMed: 28870269] [CrossRef]
9.
Steider K. CMS requires long-term care facilities to communicate infection prevention concerns during resident transfer/discharge. https://spice​.unc.edu​/2018/cms-requires-long-term-care-facilities-to-communicate-infection-prevention-concerns-during-resident-transfer-discharge/. Accessed October 25, 2019.
10.
Ariza-Heredia EJ, Patel R, Blumberg EA, Walker RC, Lewis R, Evans J, et al. Outcomes of transplantation using organs from a donor infected with Klebsiella pneumoniae carbapenemase (KPC)-producing K. pneumoniae. Transpl Infect Dis. 2012;14(3):229–36. doi: 10.1111/j.1399-3062.2012.00742.x. [PubMed: 22624726] [CrossRef]
11.
Miller R, Covington S, Taranto S, Carrico R, Ehsan A, Friedman B, et al. Communication gaps associated with donor-derived infections. Am J Transplant. 2015;15(1):259–64. doi: 10.1111/ajt.12978. [PubMed: 25376342] [CrossRef]
12.
Transmission of multidrug-resistant Escherichia coli through kidney transplantation --- California and Texas, 2009. MMWR Morb Mortal Wkly Rep. 2010;59(50):1642–6. [PubMed: 21178948]
13.
Mularoni A, Bertani A, Vizzini G, Gona F, Campanella M, Spada M, et al. Outcome of transplantation using organs from donors infected or colonized with carbapenem-resistant Gram-negative bacteria. Am J Transplant. 2015;15(10):2674–82. doi: 10.1111/ajt.13317. [PubMed: 25981339] [CrossRef]
14.
Trick WE, Lin MY, Cheng-Leidig R, Driscoll M, Tang AS, Gao W, et al. Electronic public health registry of extensively drug-resistant organisms, Illinois, USA. Emerg Infect Dis. 2015;21(10):1725–32. doi: 10.3201/eid2110.150538. [PMC free article: PMC4593443] [PubMed: 26402744] [CrossRef]
15.
Pfeiffer CD, Cunningham MC, Poissant T, Furuno JP, Townes JM, Leitz A, et al. Establishment of a statewide network for carbapenem-resistant Enterobacteriaceae prevention in a low-incidence region. Infect Control Hosp Epidemiol. 2014;35(4):356–61. doi: 10.1086/675605. [PubMed: 24602939] [CrossRef]
16.
Chou AF, Yano EM, McCoy KD, Willis DR, Doebbeling BN. Structural and process factors affecting the implementation of antimicrobial resistance prevention and control strategies in U.S. hospitals. Health Care Manage Rev. 2008;33(4):308–22. doi: 10.1097/01.HCM.0000318768.36901.ef. [PubMed: 18815496] [CrossRef]

Conclusion and Comment

In this review, we examine the evidence supporting the use of individual safety practices. However, many of the studies on the efficacy of patient safety practices examine bundled approaches or implementation of multiple practices at once, making it difficult to assess the effectiveness of any one practice. Further, improving compliance with one practice (for example, hand hygiene at every opportunity) can reinforce compliance with others, making each practice more successful when combined with others. Understanding the limitations of the available evidence, we make the following recommendations:

  • The level of evidence to support hand hygiene for MDRO infection prevention is high. What is needed is further study about the best ways to sustain high compliance with hand hygiene at every opportunity. Increasing compliance may require new technologies, institutional policies, and approaches to reducing the barriers that result in missed opportunities for hand hygiene.
  • While active surveillance has evidence to support its use in preventing MDRO acquisition and infection, there is no consensus on the optimal surveillance strategy, due to variation in patient risk factors, local epidemiology, and facility laboratory capability. Some cost-effective suggestions include active surveillance testing of samples (including routine clinical samples) for multiple MDROs and developing risk-based surveillance protocols based on which MDROs are likely to be encountered.
  • There is a high level of evidence supporting the use of chlorhexidine bathing, both for preventing MDRO acquisition and as part of decolonization strategy (to reduce transmission opportunities). Chlorhexidine bathing is relatively low cost to implement, and adverse events are rare and resolve when chlorhexidine use is stopped. There is some evidence that the use of chlorhexidine may be selecting for resistance, but no clinical impacts have been documented in the literature reviewed.
  • While some evidence supports the efficacy of different solutions for environmental cleaning in laboratory settings, more studies are needed evaluating the relative efficacy of disinfection agents against different MDROs in a clinical setting. These studies should also control for other infection control practices.
  • Bundle approaches for reducing device-associated infections have strong evidence to support their use for infection prevention, regardless of the type of pathogen. More evidence is needed to understand the risks of increased resistance introduced by the use of antimicrobial solutions and devices.
  • There is strong evidence to suggest that failure to communicate patients’ MDRO status can lead to poor patient outcomes, but there are no rigorous analyses or comparisons of optimal communication approaches for MDROs.

Footnotes

f

A hazard ratio represents the risk of a negative outcome (in this case, MRSA-positive clinical culture) at any point in the study, versus relative risk or odds ratio, both of which represent cumulative risk over the length of the study.

g

A note on terminology: ln this review, we used the authors’ words describing the HAIs they studied, which may be different from the terms currently in use (for example, ventilator-associated events or VAE is preferred over VAP due to difficulties with the definition of “VAP”).

h

Negatively charged chemical compounds that bind to proteins and can disrupt microorganisms’ membranes.

i

Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, National Center for Emerging and Zoonotic Infectious Diseases, Division of Healthcare Quality Promotion. Accessed February 12, 2020 from https://www​.cdc.gov/handhygiene​/providers/index.html.

j

Enterococcus faecium, S. aureus, K. pneumoniae, A. baumanii, and P. aeruginosa.

k
l

Ahern JW and Alston, WK (2009). Use of Longitudinal Surveillance Data to Assess the Effectiveness of Infection Control in Critical Care. Infection Control and Hospital Epidemiology, 30, 11, 1109–12 [PubMed: 19803721].

m

Quaternary ammonium is commonly used in ordinary sanitation of patient care equipment and healthcare facility surfaces. Manufacturers indicate that it is generally fungicidal, bactericidal, and active against some viruses, but not sporicidal or tuberculocidal. For more information, refer to Rutala WA, Weber DJ. Disinfection, sterilization, and control of hospital waste. In: Bennett JE, Dolin R, Blaser MJ, eds. Mandell, Douglas, and Bennett’s Principles and Practice of Infectious Diseases. 8th ed​. Philadelphia, PA; 2015.

n

Passaretti CL, Otter JA, Reich NG, et al. An evaluation of environmental decontamination with hydrogen peroxide vapor for reducing the risk of patient acquisition of multidrug-resistant organisms. Clin Infect Dis. 2013;56(1):27–35. doi: 10.1093/cid/cis839 [PubMed: 23042972] [CrossRef].

o

The most recent recommendations for catheter use (as of June 2019) from the CDC’s HICPAC generally recommend against using indwelling urinary catheters to manage urinary incontinence in place of nursing care. However, the committee also acknowledges that further research is needed for non-indwelling (e.g., condom-style) catheters and for patients at risk of skin breakdown. This approach is in keeping with the overarching recommendation for appropriate indwelling urinary catheter use: only when necessary and only for as long as needed. For more information, refer to Gould C, Umscheid C, Agarwal E, Kuntz G, Pegues D. Guideline for prevention of catheter-associated urinary tract infections Atlanta, GA: Centers for Disease Control and Prevention; 2009. https://www​.cdc.gov/infectioncontrol​/pdf​/guidelines/cauti-guidelines-H.pdf.

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