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Evidence for a nurse-led protocol for removing urinary catheters: A scoping review

  • Angela E Jones
    Correspondence
    Corresponding author.
    Affiliations
    James Cook University, Centre for Nursing and Midwifery Research, 1 James Cook Drive, Townsville, QLD, 4814, Australia

    Royal Melbourne Hospital, 300 Grattan St, Parkville, VIC, 3050, Australia
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  • Cate Nagle
    Affiliations
    James Cook University, Centre for Nursing and Midwifery Research, 1 James Cook Drive, Townsville, QLD, 4814, Australia

    Townsville Hospital and Health Service, Townsville Institute of Health Research and Innovation, 100 Angus Smith Drive, Douglas QLD, 4814, Australia
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  • Tracey Ahern
    Affiliations
    James Cook University, Centre for Nursing and Midwifery Research, 1 James Cook Drive, Townsville, QLD, 4814, Australia
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  • Wendy Smyth
    Affiliations
    James Cook University, Centre for Nursing and Midwifery Research, 1 James Cook Drive, Townsville, QLD, 4814, Australia

    Townsville Hospital and Health Service, Townsville Institute of Health Research and Innovation, 100 Angus Smith Drive, Douglas QLD, 4814, Australia
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Open AccessPublished:September 12, 2022DOI:https://doi.org/10.1016/j.colegn.2022.08.008

      ABSTRACT

      Background

      Catheter-associated urinary tract infections significantly contribute to hospital acquired complications globally, with adverse implications for patient outcomes, healthcare, and fiscal resources. Nurse-led protocols for early removal of urinary catheters to reduce the incidence of catheter-associated urinary tract infections have been trialled.

      Aim

      To report the evidence for nurse-led practices of removing urinary catheters within the acute healthcare setting.

      Methods

      Five databases (CINAHL, MEDLINE, SCOPUS, EMCARE, and INFORMIT) were systematically searched in a scoping review of all peer reviewed publications up to 12/03/2021.

      Findings

      Thirteen studies met the inclusion criteria. Eleven studies described a reduction in catheter-associated urinary tract infections regardless of the type of intervention, one study did not demonstrate a change and one study reported an increase in catheter-associated urinary tract infections. Settings, study duration and sample size varied substantially between the included studies. Interventions were exclusive nurse-led protocol for removal of urinary catheters, computerised reminder systems, bundle approaches or comprehensive packages. Outcome measures and definitions of catheter-associated urinary tract infections were varied or absent.

      Discussion

      The quality of evidence of included studies in this review was low, attributed to by a number of methodological issues related to sample size and statistical analyses. Whilst the introduction of nurse-led protocols showed some improvements, the methodological inconsistencies make it difficult to highlight a specific protocol.

      Conclusion

      Given the quality of existing evidence, caution is required in translating these findings to policy and practice.

      Keywords

      Summary of relevance

      Problem or issue

      Catheter-associated urinary tract infections are avoidable and contribute to poor patient outcomes in hospitalised adults. Since 2010, an up-to-date systematic review for nurse-led protocols for removal of urinary catheters has not yet been conducted.

      What is already known

      Several interventions have been reported to reduce incidence of catheter-associated urinary tract infections in hospitalised adults.

      What this paper adds

      New evidence showed that a reduction in catheter-associated urinary tract infection incidence could be achieved by utilising nurse-led protocols for removal of urinary catheters. Interventions that could reduce catheter-associated urinary tract infection incidence are exclusive nurse-led protocols, electronic reminder systems, bundle packages, and comprehensive care packages.

      1. Background

      Catheter-associated urinary tract infections (CAUTI) place a significant burden on healthcare systems globally and can lead to significant patient morbidity as well as having resource and fiscal implications for health services. In the United States of America (USA), hospital acquired infections have been estimated to cost up to $45 billion (USD) annually and account for approximately 100,000 deaths per year (
      • Kennedy E.H.
      • Greene M.T.
      • Saint S.
      Estimating hospital costs of catheter-associated urinary tract infection.
      ). Approximately one-third of those hospital acquired infections are CAUTIs, with an estimated 15%–25% of patients in hospitals catheterised during their admission (
      • Daniels K.R.
      • Lee G.C.
      • Frei C.R.
      Trends in catheter-associated urinary tract infections among a national cohort of hospitalized adults, 2001-2010.
      ). In Australian hospitals during the financial year of 2018–2019, 13.90% of hospital separations (the process by which an episode of care for an admitted patient ceases) had a hospital acquired complication, of which 9.96% were urinary tract infections (UTI) (

      Australian Commission on Safety and Quality in Health Care. (2021). The national safety and quality health service standards. Australian Government.accessed 25 September 2021 Available from: https://www.safetyandquality.gov.au/publications-and-resources/resource-library/national-safety-and-quality-health-service-standards-second-edition

      ;

      Australian Institute of Health and Welfare [AIHW]. (2022). Separation: identifying and definitional attributes. Australian Government. accessed 11 May 2022 Available from: https://meteor.aihw.gov.au/content/327268

      ). Of all hospital acquired complications, UTIs represent the third largest number of occurrences following delirium and unspecified complications (

      Australian Institute of Health and Welfare [AIHW]. (2021). Admitted patient care 2018 - 2019 8: Information related to safety and quality of the health system. Australian Government. accessed 24 January 2021 from https://www.aihw.gov.au/getmedia/c865a772-aab0-4ef5-bc43-efd9b213befd/admitted-patient-care-2018-19-chapter-8-tables.xls.aspx

      ).
      Most UTIs are preventable and urinary catheters (UC) have long been regarded as a significant contributor to the development of a hospital acquired UTI (
      • Foxman B.
      Epidemiology of urinary tract infections: incidence, morbidity, and economiccosts.
      ;
      • Meddings J.
      • Rogers M.A.M.
      • Macy M.
      • Saint S.
      Systematic review and meta-analysis: reminder systems to reduce catheter-associated urinary tract infections and urinary catheter use in hospitalized patients.
      ). Complications of CAUTIs include prolonged hospital stays (
      • Hu F.W.
      • Yang D.C.
      • Huang C.C.
      • Chen C.H.
      • Chang C.M.
      Inappropriate use of urinary catheters among hospitalized elderly patients: clinician awareness is key.
      ), more complex care requirements (
      • Daniels K.R.
      • Lee G.C.
      • Frei C.R.
      Trends in catheter-associated urinary tract infections among a national cohort of hospitalized adults, 2001-2010.
      ), pyelonephritis (
      • Foxman B.
      Epidemiology of urinary tract infections: incidence, morbidity, and economiccosts.
      ;
      • Nicolle L.E.
      Urinary tract infection.
      ), potential increased risk for delirium (
      • Balogun S.A.
      • Philbrick J.T.
      Delirium, a symptom of UTI in the elderly: fact or fable? A systematic review.
      ;
      • Eriksson I.
      • Gustafson Y.
      • Fagerström L.
      • Olofsson B.
      Urinary tract infection in very old women is associated with delirium.
      ;
      • Mayne S.
      • Bowden A.
      • Sundvall P.-D.
      • Gunnarsson R.
      The scientific evidence for a potential link between confusion and urinary tract infection in the elderly is still confusing - a systematic literature review.
      ), sepsis (
      • Kennedy E.H.
      • Greene M.T.
      • Saint S.
      Estimating hospital costs of catheter-associated urinary tract infection.
      ), septic shock and death (
      • Nicolle L.E.
      Urinary tract infection.
      ). Urinary tract infections are a predictor of sepsis and are a part of sepsis pathways for determining the source of pathology (
      • Nicolle L.E.
      Urinary tract infection.
      ). The use of antimicrobial agents to treat CAUTIs contributes to the ongoing global problem of antimicrobial resistance, further burdening the poor outcomes of patients, making infections more difficult to treat by narrowing the spectrum of antibiotics able to be used (
      • Linhares I.
      • Raposo T.
      • Rodrigues A.
      • Almeida A.
      Frequency and antimicrobial resistance patterns of bacteria implicated in community urinary tract infections: a ten-year surveillance study (2000-2009).
      ;
      • Nicolle L.E.
      Urinary tract infection.
      ;
      • Shin H.-R.
      • Moon J.
      • Lee H.S.
      • Ahn S.J.
      • Kim T.-J.
      • Jun J.-S.
      • et al.
      Increasing prevalence of antimicrobial resistance in urinary tract infections of neurological patients, Seoul, South Korea, 2007–2016.
      ). Because of the impact of CAUTIs on healthcare, some governments have ceased providing funding for CAUTIs in an attempt to incentivise hospitals to proactively reduce the incidence of this infection (
      • Wald H.
      • Kramer A.
      Nonpayment for harms resulting from medical care: catheter- associated urinary tract infections.
      ;
      • Wald H.
      • Richard A.
      • Dickson V.V.
      • Capezuti E.
      Chief nursing officers' perspectives on Medicare's hospital-acquired conditions non-payment policy: Implications for policy design and implementation.
      ).
      The Australian Commission on Safety and Quality in Health Care provides a set of standards against which hospital performance is measured (

      Australian Commission on Safety and Quality in Health Care. (2019). Australian Commission on Safety and Quality in Health Care: about us. Australian Government. accessed 26 January 2021 Available from: https://www.safetyandquality.gov.au/about-us

      ). As a part of the National Safety and Quality Health Service Standards Standard 3: Preventing and Controlling Healthcare Associated Infections, the prevalence of CAUTIs must by audit by hospitals and data made available to governing bodies (

      Australian Commission on Safety and Quality in Health Care. (2021). The national safety and quality health service standards. Australian Government.accessed 25 September 2021 Available from: https://www.safetyandquality.gov.au/publications-and-resources/resource-library/national-safety-and-quality-health-service-standards-second-edition

      ). Organisations have the potential to experience additional financial penalties from the mismatch between reported data from coding systems compared to actual CAUTI events ().
      Many initiatives have been developed with an aim of reducing the incidence of CAUTIs and improving patient outcomes. The objectives underpinning these initiatives include: reducing the number of insertions of UCs by determining the appropriateness of the intervention; identifying the ongoing need for the UC; alerts to remind clinicians of the presence of a UC; electronic reminders to review the UC; and protocols for the early removal of UCs by clinicians (
      • DePuccio M.J.
      • Gaughan A.A.
      • Sova L.N.
      • MacEwan S.R.
      • Walker D.M.
      • Gregory M.E.
      • et al.
      An examination of the barriers to and facilitators of implementing nurse-driven protocols to remove indwelling urinary catheters in acute care hospitals.
      ;
      • Giles M.
      • Graham L.
      • Ball J.
      • King J.
      • Watts W.
      • Harris A.
      • et al.
      Implementation of a multifaceted nurse-led intervention to reduce indwelling urinary catheter use in four Australian hospitals: apre- and postintervention study.
      ;
      • Meddings J.
      • Rogers M.A.M.
      • Macy M.
      • Saint S.
      Systematic review and meta-analysis: reminder systems to reduce catheter-associated urinary tract infections and urinary catheter use in hospitalized patients.
      ). Nurse-led removal of UC protocols allows nurses to have the autonomy to make the clinical decision to remove the UC according to a predetermined list of criteria (
      • DePuccio M.J.
      • Gaughan A.A.
      • Sova L.N.
      • MacEwan S.R.
      • Walker D.M.
      • Gregory M.E.
      • et al.
      An examination of the barriers to and facilitators of implementing nurse-driven protocols to remove indwelling urinary catheters in acute care hospitals.
      ). By introducing these preventative measures, there may be benefits such as the reduction of costs of CAUTIs and their health sequelae by up to 50% (
      • Kennedy E.H.
      • Greene M.T.
      • Saint S.
      Estimating hospital costs of catheter-associated urinary tract infection.
      ).
      The evidence underpinning nurse-led removal of UC protocols needs to be collated, tabulated and summarised to describe best practice. To this end, a scoping review protocol was developed to guide the synthesis of evidence for nurse-led practices in removing UCs within an acute healthcare setting.

      2. Aim

      The aim of this scoping review was to report the evidence for nurse-led practices of removing UCs within the acute healthcare setting.

      3. Methods

      A scoping review provides a rigorous and transparent method for mapping areas of research (
      • Pham M.T.
      • Rajić A.
      • Greig J.D.
      • Sargeant J.M.
      • Papadopoulos A.
      • McEwen S.A.
      A scoping review of scoping reviews: advancing the approach and enhancing the consistency.
      ). The purpose of scoping reviews includes summarising and disseminating the research findings to inform practitioners, consumers and policy makers (
      • Arksey H.
      • O'Malley L
      Scoping studies: towards a methodological framework.
      ). This scoping review was guided by the framework of Arksey and O'Malley with modifications by Levac and colleagues (
      • Arksey H.
      • O'Malley L
      Scoping studies: towards a methodological framework.
      ;
      • Levac D.
      • Colquhoun H.
      • O'Brien K.K
      Scoping studies: advancing the methodology.
      ). The five stages of the framework are: developing a research question; identifying relevant studies; study selection; charting the data; and collating, summarising and reporting the results (
      • Arksey H.
      • O'Malley L
      Scoping studies: towards a methodological framework.
      ;
      • Levac D.
      • Colquhoun H.
      • O'Brien K.K
      Scoping studies: advancing the methodology.
      ).
      The research question for this scoping review was, ‘What is the evidence for nurse-led removal of urinary catheters in adults within the acute hospital setting?’ A search strategy was developed using key words and, where relevant, controlled vocabulary for each of the databases: CINAHL; MEDLINE; SCOPUS; EMCARE and INFORMIT (Supplementary 1). Boolean operators ‘AND’ and ‘OR’ were used to combine terms (Supplementary 2). Alternative sources of articles included a manual search of the reference lists of included studies and the table of contents of key journals.

      3.1 Selection criteria

      Eligibility criteria were articles that specified a nurse-led practice for urinary catheter removal in an acute hospital setting with reference to the impact on CAUTI rates. All peer reviewed publications published up to 12/03/2021 were included with no restrictions for year of publication, language or study design and therefore quality improvement projects were also included. Articles were excluded if full text was not available. Letters to the editor, commentaries, reviews and editorials were excluded. Studies involving the following contexts were also excluded: aged care facilities; community settings; physician-led; paediatrics; suprapubic and long-term urinary catheters.

      3.2 Data extraction

      Results were collated using reference software (EndNote X9.3) and duplicates were removed. Titles and abstracts were screened for eligibility independently by one team member. The second screening involved a full text read conducted independently by two team members. A third team member was available and required to resolve one discrepancy relating to selection. Data extraction was conducted by one team member and reviewed by three other team members. Data extracted were author, year, study type, setting and country, sample size, aims, intervention type, study duration, outcome measure, definition of CAUTI, self-evaluation tool, and key findings. The extracted data was recorded and summarised using Microsoft Excel and was reviewed by all team members.

      4. Results

      A PRISMA flowchart (
      • McGowan J.
      • Straus S.
      • Moher D.
      • Langlois E.V.
      • O'Brien K.K.
      • Horsley T.
      • et al.
      Reporting scoping reviews—PRISMA ScR extension.
      ) was used to report the study retrieval and selection as displayed in Figure 1. Thirteen studies met the criteria (
      • Adams D.
      • Bucior H.
      • Day G.
      • Rimmer J.A.
      HOUDINI: make that urinary catheter disappear - nurse-led protocol.
      ;
      • Dumigan D.G.
      • Kohan C.A.
      • Reed C.R.
      • Jekel J.F.
      • Fikrig M.K.
      Utilizing national nosocomial infection surveillance system data to improve urinary tract infection rates in three intensive-care units.
      ;
      • Elpern E.H.
      • Killeen K.
      • Ketchem A.
      • Wiley A.
      • Patel G.
      • Lateef O.
      Reducing use of indwelling urinary catheters and associated urinary tract infections.
      ;
      • Johnson P.
      • Gilman A.
      • Lintner A.
      • Buckner E.
      Nurse-driven catheter-associated urinary tract infection reduction process and protocol.
      ;
      • Major-Joynes B.
      • Pegues D.
      • Bradway C.
      A nurse-driven protocol for removal of indwelling urinary catheters across a multi-hospital academic healthcare system.
      ;
      • Mori C.
      A-voiding catastrophe: implementing a nurse-driven protocol.
      ;
      • Parry M.F.
      • Grant B.
      • Sestovic M.
      Successful reduction in catheter-associated urinary tract infections: focus on nurse-directed catheter removal.
      ;
      • Russell J.A.
      • Leming-Lee T.S.
      • Watters R.
      Implementation of a nurse-driven CAUTI prevention algorithm.
      ;
      • Topal J.
      • Conklin S.
      • Camp K.
      • Morris V.
      • Balcezak T.
      • Herbert P.
      Prevention of nosocomial catheter-associated urinary tract infections through computerized feedback to physicians and a nurse-directed protocol.
      ;
      • Tyson A.F.
      • Campbell E.F.
      • Spangler L.R.
      • Ross S.W.
      • Reinke C.E.
      • Passaretti C.L.
      • et al.
      Implementation of a nurse-driven protocol for catheter removal to decrease catheter-associated urinary tract infection rate in a surgical trauma ICU.
      ;
      • Underwood L.
      The effect of implementing a comprehensive unit-based safety program on urinary catheter use.
      ;
      • Wenger J.F.
      Cultivating quality: reducing rates of catheter-associated urinary tract infection: one magnet hospital implemented a nurse-managed approach.
      ;
      • Yatim J.
      • Wong K.S.
      • Ling M.L.
      • Tan S.B.
      • Tan K.Y.
      • et al.
      A nurse-driven process for timely removal of urinary catheters.
      ) for inclusion in this scoping review (Fig. 1) and are described in the data extraction table (Table 1). Twelve studies were classified as research studies and one study was a quality improvement project (
      • Russell J.A.
      • Leming-Lee T.S.
      • Watters R.
      Implementation of a nurse-driven CAUTI prevention algorithm.
      ). Articles were published between 1998 and 2020.
      Table 1Data extraction table.
      Author;yearStudy/project TypeSetting & country; sample sizeAimsIntervention type; durationOutcome measureDefinition of CAUTI; self-evaluation toolKey findings
      • Adams D.
      • Bucior H.
      • Day G.
      • Rimmer J.A.
      HOUDINI: make that urinary catheter disappear - nurse-led protocol.
      Point prevalence3 wards (elderly care, gastroenterology, respiratory) small acute general hospital, UK; Not reportedEvaluate nurse-led HOUDINI UC removal protocol reducing days of UC usage and associated risk of CAUTINurse-led early removal; 2-monthsE.coli in urineNil; Plan-Do-Study-ActUC use decreased >17%, E.coli decreased 70% in intervention group, 25% in control group
      • Dumigan D.G.
      • Kohan C.A.
      • Reed C.R.
      • Jekel J.F.
      • Fikrig M.K.
      Utilizing national nosocomial infection surveillance system data to improve urinary tract infection rates in three intensive-care units.
      Prospective cohort3 ICUs, USA; 102Reduce infection rates in 3 ICUsNurse-led UC removal; 18-monthsCAUTIs/1000 catheter daysPresence of E.coli or Enterococcus in urine; FOCUS-PDCA2 of 3 ICUs had significant decreases of 45% and 29% in CAUTI incidence, the third decreased by 17% but not statistically significant
      • Mori C.
      A-voiding catastrophe: implementing a nurse-driven protocol.
      Pre/post intervention observational150 bed community hospital, USA; 389 pre, 282 postEvaluate effectiveness of a nurse-led removal protocol on incidence, duration of UC use and CAUTINurse-led removal protocol; 6-monthsUC usage = catheter days/patient days, Dwell time = catheter days/total patients with catheter, CAUTIs/patients with UCCAUTI definition given by Gray, M. (2010); Donabedian's modelReduction in CAUTI from 0.77% to 0.35% (3 cases per 389 patients to 1 case per 282 patients)
      • Johnson P.
      • Gilman A.
      • Lintner A.
      • Buckner E.
      Nurse-driven catheter-associated urinary tract infection reduction process and protocol.
      Pre-/postintervention observational4 x ICUs, USA; Not reportedDemonstrate the collaborative relationship between academic nurses and clinical nurses in implementing evidence-based nurse-led protocol for decreasing the rate of CAUTIsNurse-led orders for UC discontinuation, UC care, education of staff; 16-monthsCAUTIs/month, catheter days/monthNil; ICARE28% reduction in CAUTIs for all ICUs. CAUTIs reduction 36%, rates of catheter days 11% reduction. CAUTI rates 0.60% pre-intervention, 0.43% post-intervention. CAUTIs detected at 8.9 days pre to 16.5 days post
      • Major-Joynes B.
      • Pegues D.
      • Bradway C.
      A nurse-driven protocol for removal of indwelling urinary catheters across a multi-hospital academic healthcare system.
      Pre-/postintervention observational3 urban acute care hospitals, USA; Not reportedReduce UC utilisation and CAUTI ratesTwo options 1) time and condition then nurse can remove UC, 2) provider will assess then provide order for UC removal; 12-monthsCAUTIs/1000 catheter days or patient days, UC utilisation rateCDC CAUTI surveillance criteria; NilHospital 1 - UC utilisation reduction by 6%, reduction in CAUTIs/1000 catheter days 28%. Hospital 2 - CAUTI and UC rates increased. Hospital 3 - no change
      • Elpern E.H.
      • Killeen K.
      • Ketchem A.
      • Wiley A.
      • Patel G.
      • Lateef O.
      Reducing use of indwelling urinary catheters and associated urinary tract infections.
      Pre/post intervention observationalMedical ICU, USA; 337Reduce CAUTIs by decreasing use of UCsNurse-led indications for UC; 6-monthsCAUTIs/1000 catheter daysCDC CAUTI surveillance criteria / Nil4.7 CAUTIs/1000 catheter days pre-intervention, O during intervention phase 6 months (p < 0.001). Reduction of 73.1 catheter days per month. (p = 0.01)
      • Parry M.F.
      • Grant B.
      • Sestovic M.
      Successful reduction in catheter-associated urinary tract infections: focus on nurse-directed catheter removal.
      Pre-/postintervention observational300 bed community teaching hospital, USA; Not reportedReduce UC use and CAUTIsNurse-led UC removal; 36-monthsCAUTIs/catheter day (%), CAUTIs/patient days (%)CDC CAUTI surveillance criteria; NilReduction CAUTIs/catheter day 3.3% per month and CAUTI/patient day 5.29%, 50% reduction in UC use
      • Russell J.A.
      • Leming-Lee T.S.
      • Watters R.
      Implementation of a nurse-driven CAUTI prevention algorithm.
      Quality Improvement ProjectCardiovascular thoracic stepdown unit, urban academic medical centre, USA; 54 with UCs, 31 met algorithm criteriaImplement a nurse-led, evidence-based CAUTI reduction algorithm for 6 weeks to decrease the risk of CAUTIs and reduce the CAUTI rate by 50% from 4.80 to 2.40 per 1000 catheter daysDaily nurse UC rounds, nurse-led algorithm for UC removal; 6 weeksCAUTIs/1000 catheter daysCDC CAUTI surveillance criteria; Model for Improvement37% reduction CAUTI rates, 3.32 CAUTIs/1000 catheter days preintervention, 3.05 CAUTIs/1000 catheter days postintervention
      • Topal J.
      • Conklin S.
      • Camp K.
      • Morris V.
      • Balcezak T.
      • Herbert P.
      Prevention of nosocomial catheter-associated urinary tract infections through computerized feedback to physicians and a nurse-directed protocol.
      Pre/post intervention observational4 general medical units, USA; 164 pre, 81 postNilPhysician ordered [1) discontinue the device, 2) UC for 48 hours or 3) maintain UC] or Nurse-led UC removal; 159 daysDevice utilisation (catheter days/1000 patient days %), CAUTIs/1000 catheter daysCDC CAUTI surveillance criteria; NilCAUTIs decreased 47% (p=0.054), 36 pre to 19 post CAUTIs/1000 days. 81% reduction in UC use
      • Tyson A.F.
      • Campbell E.F.
      • Spangler L.R.
      • Ross S.W.
      • Reinke C.E.
      • Passaretti C.L.
      • et al.
      Implementation of a nurse-driven protocol for catheter removal to decrease catheter-associated urinary tract infection rate in a surgical trauma ICU.
      Retrospective cohortSurgical trauma ICU, large tertiary care centre, USA; 11490 catheter- days in 27208 patient days.Compare CAUTI rate and UC utilisation pre/post nurse-led UC removalMultimodal CAUTI prevention bundle; 19-month control, 15-month interventionCAUTIs/1000 catheter days, UC utilisation (catheter days/patient days)CDC CAUTI surveillance criteria; Nil59 patients with CAUTI pre-intervention, 16 patients with CAUTI post-intervention, UC utilisation decreased from 0.78 to 0.70 (p < 0.05, risk ratio post vs pre 0.89, 95% confidence interval [CI]: 0.86–0.91). CAUTI reduced from 5.1/1000 catheter days to 2.0/1000 catheter days (p < 0.01, risk ratio: 0.38 with 95% CI: 0.21–0.65)
      • Underwood L.
      The effect of implementing a comprehensive unit-based safety program on urinary catheter use.
      Pre-/postintervention observationalNeurosurgical, neurological ICU, USA; 936 pre, 902 postEvaluate effect of targeted intervention to decrease CAUTIs and UC utilization by implementing quality improvement initiativesComprehensive unit-based safety program; 12-monthsCatheter days, UC utilisation (catheter days/patient days), number of CAUTIs, CAUTIs/1000 catheter daysCDC CAUTI surveillance criteria / Nil14% decrease in catheter days (p = 0.001), UC utilisation decreased 14% (89% pre to 75% post intervention) (p = 0.001), 21 CAUTIs pre to 17 CAUTIs post (19% decrease although not significantly different, p = 0.95), CAUTIs/1,000 catheter days (7.6 vs 7.2) (p = 0.84) remained unchanged
      • Wenger J.F.
      Cultivating quality: reducing rates of catheter-associated urinary tract infection: one magnet hospital implemented a nurse-managed approach.
      Retrospective cohort9 units of Lancaster General Hospital, USA; Not reportedNil3-prong model - Education, products, nurse-led UC removal; 2-month pilot, 2-years postCAUTIs/1000 catheter daysCDC CAUTI surveillance criteria; Plan-Do-Study-Act ModelStatistically significant reduction (2008 & 2009) of 1.23 CAUTIs/1000 catheter days (95% CI, 0.6-1.87, p=0.001). Statistically significant reduction (2007 & 2009) of 1.72 CAUTIs/1000 catheter days (95% CI, 0.68-2.77, p =< 0.001). No statistical significance 2007 & 2008
      • Yatim J.
      • Wong K.S.
      • Ling M.L.
      • Tan S.B.
      • Tan K.Y.
      • et al.
      A nurse-driven process for timely removal of urinary catheters.
      Pre-/postintervention observationalGeneral Medicine Ward (75 beds) at General Hospital, Singapore; Not reportedEvaluate effectiveness of nurse-led removal process in reducing the duration of UC and CAUTI rateNurse-led UC removal protocol; 15-monthsCatheter days utilisation ratio (total catheter days: total patient days), CAUTIs/1000 catheter daysCDC CAUTI surveillance criteria / NilReduction of 4 CAUTIs/1000 catheter days to 0 CAUTIs/1000 catheter days (p = 0.06). Utilisation rate increased from 0.12 to 0.18
      The primary objective of all studies was to reduce incidence of CAUTIs. Secondary objectives were to reduce UC usage and/or to reduce duration UC in situ, to assess nurses’ perceptions and behaviours for UC removal, and to measure uptake of a nurse-led protocol. All studies took place in the United States, with the exception of two, one from the United Kingdom (
      • Adams D.
      • Bucior H.
      • Day G.
      • Rimmer J.A.
      HOUDINI: make that urinary catheter disappear - nurse-led protocol.
      ) and the other from Singapore (
      • Yatim J.
      • Wong K.S.
      • Ling M.L.
      • Tan S.B.
      • Tan K.Y.
      • et al.
      A nurse-driven process for timely removal of urinary catheters.
      ). No studies were conducted in Australia.
      Articles varied in study design: one point prevalence study (
      • Adams D.
      • Bucior H.
      • Day G.
      • Rimmer J.A.
      HOUDINI: make that urinary catheter disappear - nurse-led protocol.
      ); one prospective cohort study (
      • Dumigan D.G.
      • Kohan C.A.
      • Reed C.R.
      • Jekel J.F.
      • Fikrig M.K.
      Utilizing national nosocomial infection surveillance system data to improve urinary tract infection rates in three intensive-care units.
      ); seven observational pre and post intervention studies (
      • Elpern E.H.
      • Killeen K.
      • Ketchem A.
      • Wiley A.
      • Patel G.
      • Lateef O.
      Reducing use of indwelling urinary catheters and associated urinary tract infections.
      ;
      • Johnson P.
      • Gilman A.
      • Lintner A.
      • Buckner E.
      Nurse-driven catheter-associated urinary tract infection reduction process and protocol.
      ;
      • Major-Joynes B.
      • Pegues D.
      • Bradway C.
      A nurse-driven protocol for removal of indwelling urinary catheters across a multi-hospital academic healthcare system.
      ;
      • Parry M.F.
      • Grant B.
      • Sestovic M.
      Successful reduction in catheter-associated urinary tract infections: focus on nurse-directed catheter removal.
      ;
      • Topal J.
      • Conklin S.
      • Camp K.
      • Morris V.
      • Balcezak T.
      • Herbert P.
      Prevention of nosocomial catheter-associated urinary tract infections through computerized feedback to physicians and a nurse-directed protocol.
      ;
      • Underwood L.
      The effect of implementing a comprehensive unit-based safety program on urinary catheter use.
      ;
      • Yatim J.
      • Wong K.S.
      • Ling M.L.
      • Tan S.B.
      • Tan K.Y.
      • et al.
      A nurse-driven process for timely removal of urinary catheters.
      ); three retrospective studies (
      • Mori C.
      A-voiding catastrophe: implementing a nurse-driven protocol.
      ;
      • Tyson A.F.
      • Campbell E.F.
      • Spangler L.R.
      • Ross S.W.
      • Reinke C.E.
      • Passaretti C.L.
      • et al.
      Implementation of a nurse-driven protocol for catheter removal to decrease catheter-associated urinary tract infection rate in a surgical trauma ICU.
      ;
      • Wenger J.F.
      Cultivating quality: reducing rates of catheter-associated urinary tract infection: one magnet hospital implemented a nurse-managed approach.
      ) and one quality improvement project (
      • Russell J.A.
      • Leming-Lee T.S.
      • Watters R.
      Implementation of a nurse-driven CAUTI prevention algorithm.
      ). No randomised controlled trials were identified.
      Only one study was conducted across multiple hospital sites (
      • Major-Joynes B.
      • Pegues D.
      • Bradway C.
      A nurse-driven protocol for removal of indwelling urinary catheters across a multi-hospital academic healthcare system.
      ). Two studies were conducted in all areas of a single hospital (
      • Mori C.
      A-voiding catastrophe: implementing a nurse-driven protocol.
      ;
      • Parry M.F.
      • Grant B.
      • Sestovic M.
      Successful reduction in catheter-associated urinary tract infections: focus on nurse-directed catheter removal.
      ), five studies were conducted exclusively in intensive care units (
      • Dumigan D.G.
      • Kohan C.A.
      • Reed C.R.
      • Jekel J.F.
      • Fikrig M.K.
      Utilizing national nosocomial infection surveillance system data to improve urinary tract infection rates in three intensive-care units.
      ;
      • Elpern E.H.
      • Killeen K.
      • Ketchem A.
      • Wiley A.
      • Patel G.
      • Lateef O.
      Reducing use of indwelling urinary catheters and associated urinary tract infections.
      ;
      • Johnson P.
      • Gilman A.
      • Lintner A.
      • Buckner E.
      Nurse-driven catheter-associated urinary tract infection reduction process and protocol.
      ;
      • Tyson A.F.
      • Campbell E.F.
      • Spangler L.R.
      • Ross S.W.
      • Reinke C.E.
      • Passaretti C.L.
      • et al.
      Implementation of a nurse-driven protocol for catheter removal to decrease catheter-associated urinary tract infection rate in a surgical trauma ICU.
      ;
      • Underwood L.
      The effect of implementing a comprehensive unit-based safety program on urinary catheter use.
      ), and the remainder were conducted in a combination of medical, surgical or intensive care units (
      • Adams D.
      • Bucior H.
      • Day G.
      • Rimmer J.A.
      HOUDINI: make that urinary catheter disappear - nurse-led protocol.
      ;
      • Russell J.A.
      • Leming-Lee T.S.
      • Watters R.
      Implementation of a nurse-driven CAUTI prevention algorithm.
      ;
      • Topal J.
      • Conklin S.
      • Camp K.
      • Morris V.
      • Balcezak T.
      • Herbert P.
      Prevention of nosocomial catheter-associated urinary tract infections through computerized feedback to physicians and a nurse-directed protocol.
      ;
      • Wenger J.F.
      Cultivating quality: reducing rates of catheter-associated urinary tract infection: one magnet hospital implemented a nurse-managed approach.
      ;
      • Yatim J.
      • Wong K.S.
      • Ling M.L.
      • Tan S.B.
      • Tan K.Y.
      • et al.
      A nurse-driven process for timely removal of urinary catheters.
      ).
      There were considerable differences in study duration ranging from 6 weeks (
      • Russell J.A.
      • Leming-Lee T.S.
      • Watters R.
      Implementation of a nurse-driven CAUTI prevention algorithm.
      ) to 3 years (
      • Parry M.F.
      • Grant B.
      • Sestovic M.
      Successful reduction in catheter-associated urinary tract infections: focus on nurse-directed catheter removal.
      ). Sample sizes ranged from 16 (
      • Tyson A.F.
      • Campbell E.F.
      • Spangler L.R.
      • Ross S.W.
      • Reinke C.E.
      • Passaretti C.L.
      • et al.
      Implementation of a nurse-driven protocol for catheter removal to decrease catheter-associated urinary tract infection rate in a surgical trauma ICU.
      ) to 1838 (
      • Underwood L.
      The effect of implementing a comprehensive unit-based safety program on urinary catheter use.
      ) participants and the majority of studies described sample size in terms of total patient days or total catheter days. In seven studies, no sample size was reported. Six articles included a post-study self-evaluation tool for their studies and 11 studies presented the definition of CAUTI they used.
      Interventions varied across studies. The intervention for eight articles was exclusively a nurse-led protocol for removal of urinary catheters (
      • Adams D.
      • Bucior H.
      • Day G.
      • Rimmer J.A.
      HOUDINI: make that urinary catheter disappear - nurse-led protocol.
      ;
      • Dumigan D.G.
      • Kohan C.A.
      • Reed C.R.
      • Jekel J.F.
      • Fikrig M.K.
      Utilizing national nosocomial infection surveillance system data to improve urinary tract infection rates in three intensive-care units.
      ;
      • Elpern E.H.
      • Killeen K.
      • Ketchem A.
      • Wiley A.
      • Patel G.
      • Lateef O.
      Reducing use of indwelling urinary catheters and associated urinary tract infections.
      ;
      • Major-Joynes B.
      • Pegues D.
      • Bradway C.
      A nurse-driven protocol for removal of indwelling urinary catheters across a multi-hospital academic healthcare system.
      ;
      • Mori C.
      A-voiding catastrophe: implementing a nurse-driven protocol.
      ;
      • Parry M.F.
      • Grant B.
      • Sestovic M.
      Successful reduction in catheter-associated urinary tract infections: focus on nurse-directed catheter removal.
      ;
      • Russell J.A.
      • Leming-Lee T.S.
      • Watters R.
      Implementation of a nurse-driven CAUTI prevention algorithm.
      ;
      • Yatim J.
      • Wong K.S.
      • Ling M.L.
      • Tan S.B.
      • Tan K.Y.
      • et al.
      A nurse-driven process for timely removal of urinary catheters.
      ), one integrated a computerised reminder system with a nurse-led protocol (
      • Topal J.
      • Conklin S.
      • Camp K.
      • Morris V.
      • Balcezak T.
      • Herbert P.
      Prevention of nosocomial catheter-associated urinary tract infections through computerized feedback to physicians and a nurse-directed protocol.
      ), two articles presented a bundle approach for catheter removal and management (
      • Johnson P.
      • Gilman A.
      • Lintner A.
      • Buckner E.
      Nurse-driven catheter-associated urinary tract infection reduction process and protocol.
      ;
      • Wenger J.F.
      Cultivating quality: reducing rates of catheter-associated urinary tract infection: one magnet hospital implemented a nurse-managed approach.
      ) and two presented a comprehensive care package for all aspects of urinary catheter care including insertion, catheter care, urinary drainage bag, specimen collection, and removal (
      • Tyson A.F.
      • Campbell E.F.
      • Spangler L.R.
      • Ross S.W.
      • Reinke C.E.
      • Passaretti C.L.
      • et al.
      Implementation of a nurse-driven protocol for catheter removal to decrease catheter-associated urinary tract infection rate in a surgical trauma ICU.
      ;
      • Underwood L.
      The effect of implementing a comprehensive unit-based safety program on urinary catheter use.
      ).
      Outcome measures and definitions of CAUTIs also varied across studies. Nine articles used CAUTI per 1000 catheter days as an outcome measure; of these, eight used the Center for Disease Control and Prevention (CDC) definition for CAUTIs and one utilised the presence of Escherichia coli or Enterococcus spp. as the definition of CAUTI. One study utilised CAUTIs/catheter day and CAUTIs/patient days as percentages as the outcome measures and also used the CDC definition of CAUTI (
      • Parry M.F.
      • Grant B.
      • Sestovic M.
      Successful reduction in catheter-associated urinary tract infections: focus on nurse-directed catheter removal.
      ). In one study (
      • Mori C.
      A-voiding catastrophe: implementing a nurse-driven protocol.
      ), the number of CAUTIs per patient was used as the outcome measure in combination with a definition of CAUTI as described by
      • Gray M.
      Reducing catheter-associated urinary tract infection in the critical care unit.
      . The presence of Escherichia coli in urine was the outcome measure in one study (
      • Adams D.
      • Bucior H.
      • Day G.
      • Rimmer J.A.
      HOUDINI: make that urinary catheter disappear - nurse-led protocol.
      ), another used CAUTIs per month and catheter days per month (
      • Johnson P.
      • Gilman A.
      • Lintner A.
      • Buckner E.
      Nurse-driven catheter-associated urinary tract infection reduction process and protocol.
      ); neither of those studies included a definition of CAUTI. Eleven articles described a reduction in CAUTI incidence regardless of the type of intervention however only three studies had results that were statistically significant (
      • Elpern E.H.
      • Killeen K.
      • Ketchem A.
      • Wiley A.
      • Patel G.
      • Lateef O.
      Reducing use of indwelling urinary catheters and associated urinary tract infections.
      ;
      • Tyson A.F.
      • Campbell E.F.
      • Spangler L.R.
      • Ross S.W.
      • Reinke C.E.
      • Passaretti C.L.
      • et al.
      Implementation of a nurse-driven protocol for catheter removal to decrease catheter-associated urinary tract infection rate in a surgical trauma ICU.
      ;
      • Wenger J.F.
      Cultivating quality: reducing rates of catheter-associated urinary tract infection: one magnet hospital implemented a nurse-managed approach.
      ); one study did not demonstrate a change in CAUTI (
      • Underwood L.
      The effect of implementing a comprehensive unit-based safety program on urinary catheter use.
      ) and one study reported an increase in CAUTI incidence (
      • Major-Joynes B.
      • Pegues D.
      • Bradway C.
      A nurse-driven protocol for removal of indwelling urinary catheters across a multi-hospital academic healthcare system.
      ).

      5. Discussion

      The aim of this study was to report the evidence for nurse-led practices of removing UCs within the acute healthcare setting and findings from a combination of research studies and a quality improvement project found limitations in methodologies with varied results. There was unclear evidence for use of a particular protocol as results varied depending on differing settings, patient groups, clinicians’ behaviours, perceptions, and culture. Twelve studies were classified as research studies based on the definition of research as the systematic investigation aimed at the discovery into and study of materials and sources in order to establish facts and reach new conclusions (
      • Burns N.
      • Grove S.K.
      The practice of nursing research: appraisal, synthesis, and generation of evidence.
      ). One study was a quality improvement project and was included as it used a planned approach and measured outcomes (
      • Russell J.A.
      • Leming-Lee T.S.
      • Watters R.
      Implementation of a nurse-driven CAUTI prevention algorithm.
      ). Quality assessment of the studies included in scoping reviews is considered contentious (
      • Peterson J.
      • Pearce P.F.
      • Ferguson L.A.
      • Langford C.A.
      Understanding scoping reviews: definition, purpose, and process.
      ) and after some consideration the team decided against conducting this assessment.
      A critical review of each included study identified methodological concerns related to sample size and statistical analyses. Whilst 11 studies displayed a reduction in CAUTI rates, small sample sizes in combination with small incidence rates of CAUTIs per population indicates that due diligence needs to be taken before implementing policy and procedural changes based on the available evidence. While several parameters need to be considered when calculating sample size, justification of sample size is required to determine the level of confidence in sample estimates (
      • Webb P.
      • Bain C.
      • Page A.
      • Kirk M.
      • Sleigh A.
      Essential epidemiology: an introduction for students and health professionals.
      ). No studies included how sample sizes were calculated and the implications of having an inadequate sample size are increasing the margin of error, less conclusive results, increasing the risk of developing a Type II error, falsely confirming a hypothesis when in fact the alternative hypothesis is true and decreasing the power of the study (
      • Delorme P.
      • Micheaux P.L.
      • Liquet B.
      • Riou J.
      Type-II generalized family-wise error rate formulas with application to sample size determination.
      ). From the included studies in this scoping review, the number of participants required to capture an adequate number of CAUTIs to determine the effectiveness of the intervention would be high given the low rate of CAUTI occurrence in the population. The duration of some studies was quite short, or point prevalence data collection utilised, which perhaps did not allow enough time to capture CAUTI events to demonstrate statistical significance.
      To gain an adequate sample size, given the frequency of CAUTI events, the duration of a study might be so long as to make it not feasible in the clinical context subject to research fatigue, conflicting priorities and loss of interest in the impact of the study (
      • Clark T.
      We're over-researched here!': exploring accounts of research fatigue within qualitative research engagements.
      ). Likewise, if a study proposed is of considerable length, approval might not be granted by the organisation if the cost of the study begins to outweigh the cost benefits of the intervention (
      • Yazdizadeh B.
      • Majdzadeh R.
      • Salmasian H.
      Systematic review of methods for evaluating healthcare research economic impact.
      ). In order to capture a larger sample size, multiple sites may be required, but this relies on cooperation and collaboration between different organisations, which may be difficult to coordinate and it would require consistent practices at each participating site.
      Of the included studies, it was noted that no randomised controlled trials or metanalyses existed for the research question. This lack of hierarchical evidence has implications for the robustness of the studies as they can be susceptible to bias and affects the validity of results (
      • Evans D.
      Hierarchy of evidence: a framework for ranking evidence evaluating healthcare interventions.
      ). However, given that hierarchy of evidence is based on the principles of effectiveness, feasibility and appropriateness (
      • Evans D.
      Hierarchy of evidence: a framework for ranking evidence evaluating healthcare interventions.
      ), prospective cohort observational studies may be the best study type to address the research objective as randomised controlled trials may not be clinically or ethically appropriate. For this reason, control data groups may need to be retrospective as having a control and intervention group concurrent may be subject to external influences and bias. Randomised controlled trials may also be considered unethical given the evidence that UCs contribute to the development of CAUTIs.
      The use of a specific definition of CAUTI is an important point as six studies did not offer a definition. The use of one definition may capture more or less CAUTI events compared to another definition, which may result in reported CAUTI events differing from actual CAUTI events. This may influence the effectiveness of an intervention that had success based on one definition to a context that utilises a different definition. Depending on the geographical context and the governing bodies responsible for accreditation and funding, the definition may impact the reporting rates to these bodies, which can result in over reporting in surveillance indicators which may be an overestimation of the actual numbers occurring (). If the organisational definition does not align with the governing body definition of CAUTI, this also can result in erroneous reporting of data (). The majority of the studies were conducted in the United States and this is likely due to the long-standing existence of penalties for organisations for CAUTIs as they are considered a preventable condition (
      • Wald H.
      • Kramer A.
      Nonpayment for harms resulting from medical care: catheter- associated urinary tract infections.
      ). There were no studies undertaken in Australia, which may limit the generalisability of protocols used overseas to an Australian healthcare context.
      The variation in settings may have an impact on the use of the interventions in settings that are different to where the studies were conducted. Intensive care units tend to have 1:1 or 1:2 nurse to patient ratios compared to acute wards which can range from 1:4 to 8 patients depending on public or private setting, workforce enterprise bargaining agreements and legislation (Safe Patient Care (; ). The net result of these variations in ratios and settings is the nursing time spent for involvement in each patient's care. The specialised training of nurses in these different settings will vary and potentially influence the knowledge and expertise of the nurse caring for the patient and may result in a greater awareness of symptoms and complications associated with UCs (
      • Tyson A.F.
      • Campbell E.F.
      • Spangler L.R.
      • Ross S.W.
      • Reinke C.E.
      • Passaretti C.L.
      • et al.
      Implementation of a nurse-driven protocol for catheter removal to decrease catheter-associated urinary tract infection rate in a surgical trauma ICU.
      ). Busier work environments combined with higher patient to nurse ratios, patients at different stages of their care, patients who can advocate for themselves or patients who rely on staff to advocate on their behalf, the clinical condition of the patient, and cognitive ability of patients, can all affect the timing of when a UC is removed. These factors, combined with the environment, experience and focus of nurses, may affect confidence and autonomy, behaviours and knowledge, which all are contributing factors to the effectiveness of an intervention being introduced (
      • Atkins L.
      • Sallis A.
      • Chadborn T.
      • Shaw K.
      • Schneider A.
      • Hopkins S.
      • et al.
      Reducing catheter-associated urinary tract infections: a systematic review of barriers and facilitators and strategic behavioural analysis of interventions.
      ).
      While most of the studies displayed results with a reduction in CAUTI rates, there were no convincing results that favoured any particular intervention type. There were no discernible differences between comprehensive bundles or nurse-led protocol by itself in terms of reduction of CAUTIs, although given the methods of implementation of the nurse-led protocol, it is possible that bringing the focus of UC to the forefront of nurses’ practice might mean that the other aspects of UC care and maintenance are also improved indirectly. Likewise, the analysis of this review was not able to distinguish which components of the comprehensive bundles had the most significant impact. Therefore, if policy makers were to adopt a comprehensive approach, the bundle would likely have to be implemented in its entirety to ensure the best possible outcomes. Given there were no statistically significant results, this poses difficulty choosing which strategy to implement.
      The final observation of this review was the absence of qualitative data and the experience of the consumers. While some articles included an evaluation post intervention (
      • Adams D.
      • Bucior H.
      • Day G.
      • Rimmer J.A.
      HOUDINI: make that urinary catheter disappear - nurse-led protocol.
      ;
      • Dumigan D.G.
      • Kohan C.A.
      • Reed C.R.
      • Jekel J.F.
      • Fikrig M.K.
      Utilizing national nosocomial infection surveillance system data to improve urinary tract infection rates in three intensive-care units.
      ;
      • Johnson P.
      • Gilman A.
      • Lintner A.
      • Buckner E.
      Nurse-driven catheter-associated urinary tract infection reduction process and protocol.
      ;
      • Mori C.
      A-voiding catastrophe: implementing a nurse-driven protocol.
      ;
      • Russell J.A.
      • Leming-Lee T.S.
      • Watters R.
      Implementation of a nurse-driven CAUTI prevention algorithm.
      ;
      • Wenger J.F.
      Cultivating quality: reducing rates of catheter-associated urinary tract infection: one magnet hospital implemented a nurse-managed approach.
      ), most did not present follow-up data. Evaluation of a study allows for reflection on possible changes to future interventions, allows for policies to be fine-tuned and changed to allow for problems noted during the intervention period (
      • Atkins L.
      • Sallis A.
      • Chadborn T.
      • Shaw K.
      • Schneider A.
      • Hopkins S.
      • et al.
      Reducing catheter-associated urinary tract infections: a systematic review of barriers and facilitators and strategic behavioural analysis of interventions.
      ). Utilising evaluation tools presents an opportunity to take into consideration the human aspects of nurses’ behaviour and perceptions and whether the intervention is something that can be maintained in the long term. It is not uncommon for performance and key performance indicators to slip when not under the scrutiny of direct observation; evaluation tools can assist in developing recommendations to ensure that compliance continues to occur after the observers have left.

      6. Limitations

      While the initial screening may have the potential for the inclusion of selection bias as titles and abstracts were screened by one author and thus a limitation of this review, however, it was conducted under the supervision of the other experienced team members. The inclusion of quality improvement projects, while accepted in scoping reviews, may limit the outcomes to specific clinical settings and may not be generalisable to a broader context. Only one of the 13 studies included was conducted over multiple sites, the others were at a single site and this is a limitation of those studies.

      7. Conclusion

      There is limited quality evidence for a nurse-led catheter removal protocol associated with reducing incidence of CAUTIs, however noting the methodological limitations identified, caution needs to be taken in the interpretation of these results to inform practice. Results can vary substantially depending on the setting, patient groups, clinicians’ behaviours, perceptions, and culture. The definition of CAUTI used may affect the results by over or under reporting CAUTI events, which may have a substantial impact if the reported data leads to financial penalties to organisations, therefore it is important to choose the protocol carefully that is in line with an evidence based standardised definition. The significance of CAUTIs cannot be underestimated, as the impacts reach patients, consumers, organisations, and governments.

      Authorship contribution statement

      All authors reviewed and approved the manuscript.

      Ethical statement

      An ethical statement is not applicable as no human or animal research was undertaken.

      Conflict of interest

      None.

      Acknowledgements

      Acknowledgments for the William Buckland Foundation that awarded the primary author with the $10,000 Lynly S Aitken Travelling Fellowship. The foundation was not involved in study design, collection of data, analysis, interpretation nor publication.

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