A Tiered Approach for Preventing Catheter-Associated Urinary Tract Infection
Authors: Jennifer Meddings, Milisa Manojlovich, Karen E. Fowler, Jessica M. Ameling, Linda Greene, Sue Collier, Jay Bhatt, Sanjay Saint
Journal: Annals of Internal Medicine (2019)

Supplement: STRIVE1 October 2019A Tiered Approach for Preventing Catheter-Associated Urinary Tract InfectionFREEJennifer Meddings, MD, MSc, Milisa Manojlovich, PhD, RN, Karen E. Fowler, MPH, Jessica M. Ameling, MPH, Linda Greene, RN, MPS, CIC, Sue Collier, MSN, RN, Jay Bhatt, DO, MPH, MPA, and Sanjay Saint, MD, MPHJennifer Meddings, MD, MScUniversity of Michigan Medical School and Veterans Affairs Ann Arbor Healthcare System, Ann Arbor, Michigan (J.M., S.S.)Search for more papers by this author, Milisa Manojlovich, PhD, RNUniversity of Michigan School of Nursing, Ann Arbor, Michigan (M.M.)Search for more papers by this author, Karen E. Fowler, MPHCenter for Clinical Management Research, Veterans Affairs Ann Arbor Healthcare System, Ann Arbor, Michigan (K.E.F.)Search for more papers by this author, Jessica M. Ameling, MPHUniversity of Michigan Medical School, Ann Arbor, Michigan (J.M.A.)Search for more papers by this author, Linda Greene, RN, MPS, CICUniversity of Rochester Highland Hospital, Rochester, New York (L.G.)Search for more papers by this author, Sue Collier, MSN, RNHealth Research & Educational Trust, American Hospital Association, Chicago, Illinois (S.C., J.B.)Search for more papers by this author, Jay Bhatt, DO, MPH, MPAHealth Research & Educational Trust, American Hospital Association, Chicago, Illinois (S.C., J.B.)Search for more papers by this author, and Sanjay Saint, MD, MPHUniversity of Michigan Medical School and Veterans Affairs Ann Arbor Healthcare System, Ann Arbor, Michigan (J.M., S.S.)Search for more papers by this authorAuthor, Article, and Disclosure Informationhttps://doi.org/10.7326/M18-3471 SectionsAboutVisual AbstractPDF ToolsAdd to favoritesDownload CitationsTrack CitationsPermissions ShareFacebookTwitterLinkedInRedditEmail Success in reducing rates of catheter-associated urinary tract infection (CAUTI) and unnecessary urinary catheter use has varied over time, by clinical setting, by CAUTI definition, and by data source used for tracking these metrics (1–6). Although meta-analyses of the published peer-reviewed literature indicate that up to approximately 50% of CAUTIs can be prevented, many hospitals have had less success (7, 8).To help hospitals that still struggle with CAUTI, as well as other health care–associated infections (HAIs), the Centers for Disease Control and Prevention (CDC) funded the STRIVE (States Targeting Reduction in Infections via Engagement) initiative (9). Beginning in June 2016, the STRIVE initiative rapidly engaged multiple state organizations to partner and facilitate the implementation of a curriculum to prevent HAIs among 4 cohorts of hospitals experiencing high burdens of HAIs, as defined by National Healthcare Safety Network (NHSN) metrics reported by the CDC (Appendix Table). This curriculum included a focus on horizontal infection prevention practices as the foundation (13), as well as vertical approaches targeting prevention of specific HAIs, including CAUTI, central line-associated bloodstream infection (CLABSI), Clostridioides difficile, and hospital-onset methicillin-resistant Staphylococcus aureus bloodstream infection.Appendix Table. The CAUTI MetricWith an increasing number of studies describing multicomponent strategies to prevent CAUTI, it can be difficult for hospital teams to choose among interventions to reduce CAUTI. Informed by recent literature reviews and guidelines for prevention of CAUTI in multiple clinical settings, our multidisciplinary team applied a tiered approach to organize and prioritize CAUTI prevention interventions for STRIVE hospitals. This article summarizes the evidence base and development of the tiered approach to prioritize CAUTI interventions.Project StructureWith extensive experience in performing and publishing literature reviews focused on CAUTI prevention, team members from the University of Michigan reviewed and summarized several recent and comprehensive literature reviews as well as recent guidelines. This literature review included 3 systematic reviews funded in recent years by the Agency for Healthcare Research and Quality (AHRQ) to summarize the evidence for CAUTI prevention in the acute care, intensive care unit (ICU), and long-term care settings (7, 14, 15). The studies reviewed–including design, intervention details, and outcomes–are described thoroughly in these publications and their appendix tables. Multiple guidelines were also reviewed and consulted: the 2009 guideline from the Healthcare Infection Control Practices Advisory Committee (HICPAC) that provides guidance to the U.S. Department of Health and Human Services and the CDC (16), including application of the GRADE (Grading of Recommendations Assessment, Development and Evaluation) system approach for evaluating quality of evidence and determining strength of recommendations; the 2009 CAUTI International Clinical Practice Guidelines from the Infectious Diseases Society of America (IDSA) (17); the 2014 CAUTI guideline update coming jointly from the IDSA and the Society for Healthcare Epidemiology of America (18); the 2008 European and Asian guidelines for CAUTI prevention (19); and the 2015 evidence-based tool and guidance document from the American Nurses Association (20). We were also guided by the literature review performed and expert recommendations generated in the published Ann Arbor criteria (21), as well as the preliminary results of a similarly performed literature review and appropriateness panel ratings for use of catheters in general surgery and orthopedic surgery patients (22).In contrast to the literature assessing prevention of CLABSI, the great majority of the current literature on CAUTI prevention reports nonrandomized study designs that are of relatively low quality (14). Only a few CAUTI studies used the more robust randomized, controlled trial design, and those were often limited to the evaluation of single technological interventions, such as a new securement device or antimicrobial catheter (14–16, 18). Consequently, in the 2009 CAUTI prevention guideline from HICPAC–where formal study quality assessment was performed (16)–even the most basic and often perceived as critical interventions for CAUTI prevention (for example, placing indwelling catheters only for appropriate reasons, promptly removing when no longer needed, aseptic insertion and maintenance technique, and implementing quality improvement programs for reducing CAUTI) were given a HICPAC category 1B recommendation (defined as a strong recommendation supported by low- to very-low-quality evidence). No CAUTI prevention strategies were given the strongest recommendation of category 1A, reserved for interventions supported by high- to moderate-quality evidence. Other strategies (such as using alternatives to indwelling catheters, improving urine culture stewardship, conducting catheter rounds to survey appropriateness and care adherence, and CAUTI surveillance with regular unit-specific feedback to staff) were recommended as category II, defined as a weak recommendation supported by any quality evidence suggesting a tradeoff between clinical benefits and harms.More recent literature reviews have not found a change in the types of study designs used for CAUTI prevention interventions (14). In a 2018 systematic review summarizing 28 studies of interventions for CAUTI prevention in the ICU setting, only 2 were randomized, controlled trials, whereas 26 were nonrandomized before-and-after designs (14). Furthermore, most studies of CAUTI prevention include multicomponent interventions, with no capability to quantify the impact of individual intervention components (8, 14).Measuring adherence to CAUTI prevention interventions is also rarely reported in studies, probably because it is quite resource-intensive and hard to standardize, as it requires observations of busy frontline clinicians. Many studies involving CAUTI prevention are limited to one or a few units, with the majority being single-hospital studies, often of short duration. Thus, many studies are probably underpowered to detect statistically significant changes in either process or outcome measures for CAUTI prevention. It is also often impossible to discern in these types of studies how much a change in CAUTI outcome was due to the intervention itself, versus a decreasing secular trend (which requires longer preintervention data collection, and ideally a concurrent control group). In addition, how much outcome change is related to changes in diagnosis and documentation of CAUTI symptoms, testing due to urine culture stewardship interventions, or even a Hawthorne effect.On the basis of lessons learned from a prior collaborative that successfully used a tiered approach for CAUTI prevention in Veterans Affairs hospitals (23), our team believed that a tiered approach for implementing interventions would also benefit STRIVE hospitals. The idea with a tiered approach is to recommend lower-cost interventions with higher evidence and impact in the first tier of implementation, with more expensive and resource-intensive interventions reserved for the second tier.Given the increasing number of interventions for preventing CAUTI, we also applied an existing framework of a catheter “life cycle” for organizing and prioritizing interventions that was initially developed for organizing CAUTI prevention interventions (24). This catheter life cycle model was more recently adapted to be applicable to reducing both urinary and vascular catheter–associated complications, as recently published in a systematic review of ICU interventions for preventing catheter-associated infections (14).Disrupting the life cycle of a catheter to prevent complications includes 4 stages. The first and most important stage—stage 0—is avoiding catheter placement if possible, by application of appropriateness criteria as well as optimizing use of alternatives. The next stage (stage 1) is ensuring aseptic catheter insertion. Stage 2 is maintaining awareness and proper care of catheters in use, and stage 3 is promptly removing catheters when no longer necessary. In addition to improving knowledge and technical skills needed for each stage, clinical experience and the literature support the benefit of socioadaptive interventions to aid in implementing and sustaining changes made in clinical practice to disrupt the life cycle of the urinary catheter (14).Tier FrameworkTeam members from the University of Michigan presented a summary of the literature review, guidelines, and a draft of a tiered approach to CAUTI prevention to a multidisciplinary panel at the STRIVE kick-off meeting in March 2016. The meeting included physicians, nurses, and infection prevention specialists who agreed on the tiered approach to CAUTI prevention and the major components of both tiers. The CAUTI tier components, descriptions, and instructions underwent further refinement in discussion by the multidisciplinary STRIVE content development committee, for use in STRIVE educational content modules prepared for clinicians working in acute care, long-term acute care, as well as critical access hospitals.The Figure shows the final components of tier 1 and tier 2 interventions for preventing CAUTI as implemented in the STRIVE collaborative. Below, we summarize the evidence base and rationale for each tier component (1A to 1E in tier 1 and 2A to 2E in tier 2). Of note, these tiers were primarily developed for acute-care patients, in whom the majority of urinary catheter use is anticipated to be temporary. However, many of the strategies are also applicable to patients with long-term urinary management needs, such as improving catheter maintenance and performing periodic reassessments to determine whether an alternative to indwelling catheter use would be more appropriate (for example, changing to intermittent straight catheterization or an external catheter). A 2017 systematic review of the literature offers additional guidance on prevention of CAUTIs in patients who need long-term catheter placement and patients in long-term care settings (15). The 2015 Ann Arbor criteria also provide more detailed recommendations comparing urinary management strategies for patients with chronic urinary retention or incontinence (21).Figure. Tiered approach to prioritize interventions to prevent CAUTI.This material was expanded, enhanced, and adapted from materials developed for CAUTI prevention by faculty and staff at the Department of Veterans Affairs and the University of Michigan with funding support from the Agency for Healthcare Research and Quality. Further adaptation was done with funding support from the Centers for Disease Control and Prevention. CAUTI = catheter-associated urinary tract infection; GPS = guide to patient safety; TAP = Targeted Assessment for Prevention; UTI = urinary tract infection. Download figure Download PowerPoint Tier 1 Practices to Prevent CAUTITier 1 consists of standardizing basic supplies, procedures, and processes to address steps to disrupt the life cycle of urinary catheters and avoiding urine culture ordering when asymptomatic.Tier 1A: Place Indwelling Urinary Catheter Only for Appropriate ReasonsTier 1 begins with a commonly used strategy: restricting the use of indwelling urinary catheters to appropriate indications (tier 1A). This strategy was supported by all guidelines that were reviewed (16–18, 20). Several guidelines (20–22) provided more specific guidance on indications than earlier guidelines, particularly with respect to clarification of when indwelling catheters were needed in critical illness, wound care, or management of incontinence, as well as perioperative use of catheters. Tables detailing and comparing appropriateness of indwelling catheters, external catheters, and noncatheter strategies for addressing urinary management issues, as well as an ICU checklist for urinary catheter appropriateness, are provided in the 2015 Ann Arbor criteria (21). Several studies have shown that using an approved indication list helps reduce urinary catheter use (25–32). Requiring a urinary catheter placement order by a physician has also shown some success in encouraging appropriate catheter use (30, 33). Of individual studies that included assessing appropriateness as an intervention, 9 showed a decrease in CAUTIs (25–33), including 3 with statistically significant reductions (25, 26, 28).Tier 1B: Encourage Use of Alternatives to Indwelling Urinary CathetersEncouraging use of alternatives to indwelling urinary catheters (tier 1B) was selected as an intervention to decrease not only risk for CAUTIs but also noninfectious complications of urinary catheters, such as urethral trauma from placement and removal resulting in pain, hematuria, and scars in the form of urethral strictures (34–36). Common interventions to promote alternatives to urinary catheters include education about external catheters (25–27, 32, 37–40), urinary retention protocols (26, 29, 33, 39), and bladder scanner simulation training (27). All 10 of these studies showed a decrease in CAUTI, with 5 being statistically significant (25, 26, 37, 39, 40). Participants in the STRIVE initiative were provided education on indications for use of external catheters and straight catheters (21), and examples of alternative options, such as use of bladder scanners and incontinence products. We also provided STRIVE participants with solutions to overcome common barriers, such as the need for accurate intake and output measurement and lack of available or appropriate catheter alternative supplies.Tier 1C: Ensure Proper Aseptic Insertion Technique and Maintenance ProceduresEnsuring proper aseptic insertion and maintenance (tier 1C) is considered standard of practice. However, the evidence base for aseptic insertion and maintenance is not well developed, nor is it anticipated to ever be further developed. It would be difficult to obtain approval and recruit participants for a randomized controlled study of aseptic indwelling catheter insertion versus “clean” technique (currently used for intermittent straight catheterization in the nonacute setting) because the leading infection prevention organizations have long-established recommendations of aseptic insertion of indwelling catheters in the acute care setting (16–18). In addition, such a study could put hospitals at risk because their CAUTI rates are compared and they are penalized for Medicare payment on that basis (11). It is believed that adherence to aseptic insertion practices is vital to CAUTI prevention, because one of the ways that organisms can enter the bladder is during catheter insertion (41, 42). Maintenance care is equally important, because organisms also enter through the catheter lumen (from a colonized drainage bag) and along the external surface of the catheter (41, 42). Interventions focused on this aspect of CAUTI prevention include the use of a urinary catheter insertion cart (43), use of a standardized urinary catheter kit (21, 25, 26), aseptic insertion training (21, 25, 26, 32, 33, 37, 39, 40, 44–47), use of a commercial securement device (26, 38), urinary catheter maintenance care training (21, 25–27, 29, 32, 33, 37–40, 44–47), and use of a urinary tract infection bundle checklist (43, 45, 47) during patient care rounds. Of the 16 studies that included an intervention to ensure proper aseptic insertion or urinary catheter maintenance care, 15 showed a decrease in CAUTIs (25–27, 29, 32, 33, 37–40, 43–47), including 7 studies showing a statistically significant decrease in CAUTIs (25, 26, 37, 39, 40, 43, 47).Despite the wealth of available evidence on ensuring proper aseptic insertion, a recent study (48) in which researchers observed 81 catheter insertion attempts in a level 1 trauma center emergency department showed that 59% of attempts had at least 1 major break in aseptic insertion technique, demonstrating room for improvement in this domain. Participants in the STRIVE initiative were encouraged to utilize a simple checklist developed by the American Nurses Association to guide the insertion process (20). A CAUTI maintenance bundle checklist was also included in the education for this STRIVE intervention (49).Tier 1D: Optimize Prompt Removal of Unneeded CathetersInterventions to prompt removal of catheters when no longer necessary were included in tier 1 (as tier 1D) because physicians are often unaware when their patients have a urinary catheter; thus, catheters are often not removed promptly when no longer needed (50, 51). Given that prolonged catheterization is the number 1 risk factor for CAUTI (42), much research has focused on promptly removing urinary catheters that are no longer needed. Two main types of removal strategies have been studied extensively and have been shown to reduce CAUTI rates by more than 50%: urinary catheter removal reminders and urinary catheter removal stop orders (7). Of the 15 studies reviewed, CAUTI rates were reduced in 14 (25–31, 33, 38, 46, 47, 52–54) and the reduction was statistically significant in 6 (25, 26, 28, 47, 52, 53).Tier 1E: Urine Culture Stewardship: Culture Only if Symptoms of UTI Are PresentBecause suspected urinary tract infection is the most common cause of inappropriate antibiotic prescribing in the inpatient setting (55) and 20% to 80% of patients with asymptomatic bacteriuria receive antibiotics for a positive urine culture (56), improving urine culture stewardship was included in tier 1 (as tier 1E).In brief, urine culture stewardship interventions focus on avoiding sending urine cultures for asymptomatic patients except in a few rare clinical scenarios as recommended by IDSA (that is, for, pregnant patients and before urologic procedures where urethral mucosal bleeding is anticipated) (17, 57). Urine cultures should not be sent on the basis of a change in urine odor or cloudiness. Furthermore, the IDSA recommends that urine cultures be sent only if the patient has signs or symptoms compatible with urinary tract infection, such as new-onset fever or rigors, altered mental status, or malaise without another identified cause (for example, pneumonia); flank pain; costovertebral area tenderness; acute hematuria; or pelvic discomfort. Dysuria, urgency, frequency, or suprapubic pain are only considered qualifying symptoms in a patient whose urinary catheter has recently been removed, but not during catheter use, because these symptoms can be related to irritation from the catheter itself. Urine culture stewardship interventions also commonly include clinician education and reminder strategies regarding the detailed diagnostic and treatment criteria for symptomatic CAUTI, often summarized from the IDSA guidelines (17, 57).It is recognized that urine culture stewardship interventions can change documented CAUTI rates by reducing urine culture ordering without affecting either urinary catheter placement or the development of urinary tract infections. However, the primary goal of urine culture stewardship is to reduce inappropriate antibiotic prescribing and antibiotic-related adverse events, which unfortunately are not uncommon in often frail patient populations at risk for having urinary catheters placed (58).Studies supporting the benefit of urine culture stewardship interventions have been published in recent years (59–62). A before-and-after study of urine culture stewardship intervention with a contemporaneous control group, implemented in acute care and long-term care units, demonstrated statistically significant reductions in urine culture ordering in both settings, and significantly reduced antimicrobial prescribing for asymptomatic bacteriuria in the long-term care setting (60).Tier 2 Interventions to Prevent CAUTIHospitals were advised to first implement all of the tier 1 interventions and review and audit compliance with tier 1 measures. If CAUTI rates remained elevated despite standardizing supplies, procedures, and processes, hospitals were then instructed to proceed to tier 2 interventions.Tier 2A: Perform Needs Assessment With the CAUTI GPS and Targeted Assessment for Prevention StrategyFor use if CAUTI rates remain elevated, tier 2 consists of enhanced interventions, beginning with a self-administered and validated needs assessment survey (tier 2A) called the CAUTI guide to patient safety (GPS) (Figure). The CAUTI GPS is available at www.catheterout.org/cauti-gps.html (63–65) and is described in the accompanying article by Saint and colleagues (66) in this STRIVE supplement. On the basis of the results of the GPS, hospitals are provided guidance regarding basic prevention steps in tier 1 that may need additional attention to optimize prevention, as well as advice on prioritization of the more time- and resource-intensive enhanced practices of tier 2.The Targeted Assessment for Prevention (TAP) strategy is another resource for performing self-assessment and identifying resources to address identified gaps in prevention of CAUTI, CLABSI, and Clostridioides difficile infection (67). The CAUTI TAP strategy (68), for use by a single health care facility, consists of 3 components: 1) running TAP reports from NHSN to identify units with higher CAUTI rates than anticipated, 2) administering TAP facility assessment tools to identify gaps in infection prevention by location, and 3) accessing infection prevention resources in the TAP implementation guides to address any gaps.Tier 2B: Conduct Catheter Rounds With Targeted Education to Optimize Appropriate UseThe first enhanced prevention practice recommended was conducting catheter rounds with targeted education on appropriate use (tier 2B). Five studies included indwelling urinary catheter rounds as an intervention (26–28, 38, 43). All of the studies showed a reduction in CAUTI, with 3 showing a statistically significant reduction (26, 28, 43).Tier 2C: Feed Back Infection and Catheter Use to Frontline Staff in Real TimeThe next enhanced practice recommended was feeding back CAUTI and catheter use data to frontline staff in real time (tier 2C). We found 12 studies that used this intervention, with all but 2 reporting a reduction in CAUTI (21, 26, 27, 32, 33, 37–40, 43, 46, 69). Five of these studies reported a statistically significant reduction in CAUTI (26, 37, 39, 40, 43).Tier 2D: Observe and Document Competency of Catheter Insertion: Education and Observed BehaviorObserving catheter insertion to confirm procedural competency, along with providing education and feedback to optimize insertion, was also recommended (tier 2D). Although we anticipate that many hospitals require observation of catheter insertion technique in new clinician hires or recent graduates, periodic observation of catheter insertion for employees after their initial hire is not yet common in many hospitals, thus this was recommended as a tier 2 intervention. This was not recommended in tier 1 because periodic observations for clinicians who place urinary catheters can be resource-intensive. This could, for example, instead be done on an annual basis or as an additional intervention for units that are having difficulties with CAUTI. Ten study interventions included measurement of intervention compliance (26, 27, 32, 37, 39, 40, 44, 47, 69, 70), though the details of compliance that were measured beyond hand hygiene were often not specified; 9 of these studies showed a decrease in CAUTI, with 6 of them showing a statistically significant decrease (26, 37, 39, 40, 47, 70), supporting the value of measuring compliance. Participants in the STRIVE initiative were encouraged to use the American Nurses Association's CAUTI Prevention Tool, which can be used as both a checklist and a competency assessment for catheter insertion (20).Tier 2E: Perform Full Root-Cause Analysis or Focused Review of InfectionsTier 2 also included the enhanced practice of performing either a full root-cause analysis or a focused review of each CAUTI event (tier 2E), in order to review contributing factors and make further recommendations to clinicians and units to optimize future prevention. Although this practice was studied and was supported by a decrease in CAUTI in only 1 study (26), it is considered valuable and is part of the Comprehensive Unit-based Safety Program approach to HAI prevention (71). Participants in the STRIVE initiative were advised to use the AHRQ Learn from Defects tool to understand how to perform and learn from this enhanced practice (72).ConclusionInformed by recently published literature reviews, guidelines, and the clinical expertise of a multidisciplinary team, a tiered approach to prioritize and implement CAUTI prevention strategies was developed to inform intervention adoption by acute care, long-term acute care, and critical access hospitals participating in a national initiative funded by the CDC. Tier 1 consists of standardizing basic supplies, procedures, and processes to address steps to disrupt the life cycle of urinary catheters and avoiding urine culture ordering for asymptomatic patients. Tier 2 begins with a self-administered needs assessment survey to highlight tier 1 interventions that may need better implementation, as well as to select and prioritize among tier 2 enhanced practices and implement those that are more time- and resource-intensive.References1. Centers for Disease Control and Prevention. 2017 national and state healthcare associated infections progress report. 5 December 2017. Accessed at www.cdc.gov/hai/data/portal/progress-report.html on 12 November 2018. Google Scholar2. Agency for Healthcare Research and Quality. National scorecard on rates of hospital-acquired conditions 2010 to 2015: interim data from national efforts to make health care safer. December 2016. Accessed at www.ahrq.gov/sites/default/files/wysiwyg/professionals/quality-patient-safety/pfp/2015-natl-scorecard-hac-rates.pdf on 17 October 2018. Google Scholar3. Saint S, Greene MT, Krein SL, et al. A program to prevent catheter-associated urinary tract infection in acute care. N Engl J Med. 2016;374:2111-9. [PMID: 27248619] doi:10.1056/NEJMoa1504906 CrossrefMedlineGoogle Scholar4. Mody L, Greene MT, Meddings J, et al. A national implementation project to prevent catheter-associated urinary tract infection in nursing home residents. JAMA Intern Med. 2017;177:1154-62. [PMID: 28525923] doi:10.1001/jamainternmed.2017.1689 CrossrefMedlineGoogle Scholar5. Metersky ML, Eldridge N, Wang Y, et al. National trends in the frequency of bladder catheterization and physician-diagnosed catheter-associated urinary tract infections: results from the Medicare Patient Safety Monitoring System. Am J Infect Control. 2017;45:901-4. [PMID: 28625702] doi:10.1016/j.ajic.2017.03.008 CrossrefMedlineGoogle Scholar6. Magill SS, O'Leary E, Janelle SJ, et al; Emerging Infections Program Hospital Prevalence Survey Team. Changes in prevalence of health care-associated infections in U.S. hospitals. N Engl J Med. 2018;379:1732-44. [PMID: 30380384] doi:10.1056/NEJMoa1801550 CrossrefMedlineGoogle Scholar7. Meddings J, Rogers MA, Krein SL, et al. Reducing unnecessary urinary catheter use and other strategies to prevent catheter-associated urinary tract infection: an integrative review. BMJ Qual Saf. 2014;23:277-89. [PMID: 24077850] doi:10.1136/bmjqs-2012-001774 CrossrefMedlineGoogle Scholar8. Schreiber PW, Sax H, Wolfensberger A, et al; Swissnoso. The preventable proportion of healthcare-associated infections 2005-2016: systematic review and meta-analysis. Infect Control Hosp Epidemiol. 2018;39:1277-95. [PMID: 30234463] d