Journal of Hospital Infection 94 (2016) 175e181 Available online at www.sciencedirect.com
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Assessment of a multi-modal intervention for the prevention of catheter-associated urinary tract infections ˜o-Romero a, H.G. Ternavasio-de la Vega a, b, *, A. Barbosa Ventura a, F. Castan ´zar a, A. Vicente Sa ´nchez a, F.D. Sauchelli a, A. Prolo Acosta a, F.J. Rodrı´guez Alca ´nez c, M. Marcos a, b, J. Laso a, b E. Ruiz Antu a
Internal Medicine Department, University Hospital of Salamanca, Salamanca, Spain Institute of Biomedical Research of Salamanca (IBSAL), Salamanca, Spain c Training, Development and Innovation Area, University Hospital of Salamanca, Salamanca, Spain b
A R T I C L E
I N F O
Article history: Received 28 February 2016 Accepted 19 July 2016 Available online 25 July 2016 Keywords: Urinary tract infection Urinary catheter Prevention
S U M M A R Y
Background: Catheter-associated urinary tract infections (CAUTIs) represent an important healthcare burden. Aim: To assess the effectiveness of an evidence-based multi-modal, multi-disciplinary intervention intended to improve outcomes by reducing the use of urinary catheters (UCs) and minimizing the incidence of CAUTIs in the internal medicine department of a university hospital. Methods: A multi-modal intervention was developed, including training sessions, urinary catheterization reminders, surveillance systems, and mechanisms for staff feedback of results. The frequency of UC use and incidence of CAUTIs were recorded in three-month periods before (P1) and during the intervention (P2). Findings: The catheterization rate decreased significantly during P2 [27.8% vs 16.9%; relative risk (RR): 0.61; 95% confidence interval (CI): 0.57e0.65]. We also observed a reduction in CAUTI risk (18.3 vs 9.8%; RR: 0.53; 95% CI: 0.30e0.93), a reduction in the CAUTI rate per 1000 patient-days [5.5 vs 2.8; incidence ratio (IR): 0.52; 95% CI: 0.28 e0.94], and a non-significant decrease in the CAUTI rate per 1000 catheter-days (19.3 vs 16.9; IR: 0.85; 95% CI: 0.46e1.55). Conclusion: The multi-modal intervention was effective in reducing the catheterization rate and the frequency of CAUTIs. ª 2016 The Healthcare Infection Society. Published by Elsevier Ltd. All rights reserved.
Introduction * Corresponding author. Address: Servicio de Medicina Interna, Hospital Clı´nico de Salamanca, C/Paseo San Vicente, 58-156, Salamanca 37007, Espan ˜a. Tel.: þ34 923291437; fax: þ34 923294739. E-mail address:
[email protected] (H.G. Ternavasiode la Vega).
Urinary tract infections (UTIs) are among the most frequently occurring hospital-acquired infections, representing 20e30% of all infections occurring in acute care hospitals.1 Virtually all hospital-acquired UTI cases are related to manipulation of the urinary tract, and catheter-associated UTI (CAUTI) is the most
http://dx.doi.org/10.1016/j.jhin.2016.07.011 0195-6701/ª 2016 The Healthcare Infection Society. Published by Elsevier Ltd. All rights reserved.
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Before intervention period (P1)
Intervention period (P2)
Training sessions
Awareness-raising campaign Reminders
P1 observation
P2 observation
P2 indicators
P1 indicators
Comparison of data results
Feedback and diffusion of results Figure 1. Design, periods and activities of the study.
prevalent device-associated hospital-acquired infection.1,2 In Spain, 24e30% of all diagnosed UTI cases in patients hospitalized in non-intensive care unit wards are associated with the presence of a permanent urinary catheter (UC), and 18% of cases are associated with long-term UC use.3,4 CAUTIs may lead to severe complications such as pyelonephritis, bacteraemia, and endocarditis, extending hospital stays and increasing morbidity, mortality, and healthcare costs.2,5,6 In the USA, it is estimated that more than 13,000 deaths each year are related to CAUTIs.5 There are specific recommendations to prevent the occurrence of CAUTI in patients requiring indwelling bladder catheters.7,8 Since the most important predictive factor for UTI in these cases is the duration of use, a reduction in catheterization-days is a useful means of reducing CAUTI cases, complications, and associated mortality.2,9e12 Several tools (such as the implementation of reminders or surveillance systems) have been described in the literature and have been effective in the control of device-associated hospital-acquired infections.7,11,13e16 As far as we are aware, there have been no published efforts in Spain to reduce the frequency of CAUTI by implementing a comprehensive package of evidence-based measures. The aim of this study was to assess the impact of a multi-modal intervention designed to improve UC use and to reduce the frequency of CAUTI.
Methods Study location and design A prospective study with a preepost design was carried out in the Department of Internal Medicine at the University Hospital of Salamanca.
Inclusion and exclusion criteria Patients who were admitted to the internal medicine ward with an existing long-term UC, those who had a UC placed within 48 h prior to admission, and those in whom a UC was placed during their stay were included in the study. Patients with non-indwelling catheters, those with catheters for urinary diversion, and those with suprapubic UCs were excluded.
Study protocols The study was divided into period P1 (January to March 2013, prior to implementation of the multi-modal intervention) and period P2 (April 2013 to April 2014) during which the multimodal intervention was implemented (Figure 1).
H.G. Ternavasio-de la Vega et al. / Journal of Hospital Infection 94 (2016) 175e181 Period 1 During the three months of P1, daily observations of patients with UCs were carried out to gain a better understanding of the use of these devices and their associated complications (Figure 1). In order to ensure that the information was obtained under realistic conditions, the staff caring for the patients were unaware of the protocol during the observation period. Period 2 The multi-modal intervention implemented during P2 included: (1) training sessions from April to November 2013 for the medical staff, nursing staff, and nursing assistants (Figure 1) on the use of UCs. The sessions involved: (i) dissemination of the results obtained during P1, (ii) adequate and inadequate indications for the use of UCs, (iii) appropriate techniques for placement, maintenance, and timely removal of UCs, and (iv) information on the study protocol and the implementation of record-keeping and reminder systems to be implemented during the monitoring stage of P2; (2) daily observation of patients with UCs (January to March 2014), this time with the prior knowledge of the staff involved; (3) placement of reminders of the presence of UCs (January to March 2014) in the patient’s progress record and treatment record and in a nursing care log; (4) implementation of an awareness-raising campaign for the healthcare staff with posters and leaflets containing information on ways to optimize the use of UCs and reinforce the recommendations described above (January to March 2014); and (5) feedback of the results to the healthcare staff through meetings and reports (April 2014). All of the previous measures, with the exception of the awarenessraising campaign, were based on recommendations in the 2009 guidelines for the prevention of CAUTIs issued by the Healthcare Infection Control Practices Advisory Committee of the Centers for Disease Control and Prevention (CDC).7 The team carrying out these activities consisted of three staff physicians, four medical interns, and three nurses who had received additional training.
Observation system and data registration Information was systematically collected during daily observation of patients with UCs admitted to our department. The inclusion of patients in the study and the data collection were carried out for three months in each period; thus the observations occurred during all of P1 and only part of P2. In order to reduce biases associated with seasonal effects, observation and data collection in P2 were carried out from January to March 2014, the same months as P1. Recorded information included demographic and clinical data, indications for UC placement, presentation of CAUTI criteria, days of hospitalization, days of catheterization per patient, appearance of macroscopic haematuria after urinary catheterization, UC obstruction, and acute urinary retention after UC removal requiring new catheterization. The daily number of occupied beds in the Department of Internal Medicine was also recorded. The total number of days of urinary catheterization per patient was recorded as catheter-days, and the total number of beds occupied per day in the Department of Internal Medicine of the University Hospital of Salamanca,
177
which includes patients with and without UCs, was recorded as patient-days.
Definitions A CAUTI was defined according to the criteria established in the protocols and definitions of the device-associated infections module of the CDC (Supplementary Table I).5 In short, CAUTI was defined for patients who had a current UC or had previously had a catheter up to 48 h before the onset of the UTI (defined either as clinical onset or as identification in the laboratory, whichever occurred first) and who met the clinical, laboratory, and microbiological criteria (Supplementary Table I). There was no established minimum UC placement time before a UTI was considered catheter-associated. Barthel index was used to estimate the functional status or ability to perform activities of daily living, and Charlson index was used as a measure of comorbidity of patients.17,18 We also recorded variables from the patients’ medical history such as urological manipulation or any surgery in the last 30 days, hospitalizations in the last 90 days, use of antibiotics in the last 90 days, the presence of congenital or acquired immunosuppression, chemotherapy in the last 30 days, treatment with 20 mg/day of prednisone or an equivalent dose of other corticosteroids for >10 days in the previous month, previous placement of a long-term UC, and repeated UTIs (3 in the last year, either with or without microbiological isolation, but with antibiotic treatment). The study also considered prior exposure to healthcare settings under the following criteria: (1) hospitalization for >48 h in the last 90 days, (2) long-term stay in a care facility, (3) treatment under an in-home care regimen, (4) treatment in a day hospital, (5) outpatient treatment of skin wounds, or (6) participation in a haemodialysis programme.
Data analysis A descriptive and comparative analysis of the cohorts in P1 and P2 was carried out based on mean values and standard deviations for quantitative variables and frequency and percentage for categorical variables. Student’s t-test was used for the comparison of continuous variables and the c2-test (or Fisher’s exact test if necessary) was used for the comparison of categorical variables. Indicators selected for comparison included (Supplementary Table II): (i) length of stay in the hospital and in the Department of Internal Medicine; (ii) average time of UC use per patient; (iii) total time of UC use per patient (catheter-days); (iv) bed occupancy in the Department of Internal Medicine (patient-days); (v) catheterization rate; (vi) occurrence of UC placement with inadequate indications (inadequate motives for urinary catheterization are listed in Supplementary Table III); (vii) risk of permanent UC during the entire in-hospital stay; (viii) CAUTI rate per 1000 catheterdays; (ix) CAUTI rate per 1000 patient-days; (x) risk of CAUTI; and (xi) risk of other complications such as macroscopic haematuria after UC insertion, obstruction requiring manipulation or replacement of the catheter, and acute urinary retention after UC removal. Measures of association [either relative risk (RR) or incidence rate (IR), depending on the case] were obtained with a 95% confidence interval (95% CI), using the data from P1 as a reference. Statistical significance was assessed
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using the SPSS 19 software with values of P < 0.05 indicating significance.
Ethical considerations The Ethics Committee from the University Hospital of Salamanca approved the study and, given its nature, an informed consent form was deemed unnecessary.
Results In total, 333 episodes of urinary catheterization were included during the observation periods, 169 in P1 and 164 in P2. As shown in Table I, the patients included had an average age of 79.8 years, a large burden of disease, evidenced by the Charlson index (mean 3.6, SD ¼ 2.0), and a significant dependence to perform activities of daily living evidenced by the Barthel index (mean 52, SD ¼ 38). Also, a large number of patients presented with diabetes mellitus (107, 32.1%) or with previous recent experiences with healthcare (154, 46.4%) (Table I). No significant differences were noted between observation periods with regard to the admission characteristics of patients, with the exception of a significantly higher frequency of immunosuppression and benign prostatic hyperplasia, and a non-significant trend to suffer from diabetes mellitus and to have received prior antibiotic therapy in P2 (Table I). The total in-hospital length of stay and the length of stay in the Internal Medicine Department of patients with UCs were significantly reduced during P2, by an average of 3.1 and 2.6 days, respectively (Table II). Reduced use of UCs was also observed in P2 (average of 4.5 days, P < 0.0001) for all patients, during both the total in-hospital and the internal medicine length of stay (Table II). When patients who had
undergone UC placement after admission (N ¼ 280) were analysed separately, a significant decrease (close to 50%) in the average time of urinary catheterization also occurred in P2, both during the total in-hospital stay (P1 13.1 vs P2 7.3 days, P < 0.0001) and during the internal medicine stay (P1 12.2 vs P2 6.4 days, P < 0.0001). In P2, the risk of maintaining a UC inserted throughout the hospital stay was significantly reduced in the entire cohort (P1 43.2% vs P2 29.3%; RR: 0.68; 95% CI: 0.50e0.91), and when the analysis was restricted to the subgroup of patients who were not chronic carriers of UC (N ¼ 280; P1 36.6% vs P2 19.5%; RR: 0.53; 95% CI: 0.36e0.80). During P1 there were 5684 total patient-days of hospitalization in our department, including 1582 catheter-days for the 169 patients with UCs. In this group, there were 31 episodes of CAUTI. In P2 there were 5695 patient-days, and the 164 patients with UC included in the study accounted for 965 catheter-days and 16 episodes of CAUTI (Table II). During P2 the catheterization rate was significantly reduced by 11% (RR: 0.61; 95% CI: 0.57e0.65), the risk of CAUTI (RR: 0.53; 95% CI: 0.30e0.93) and the CAUTI rate per 1000 patient-days (RI: 0.52; 95% CI: 0.28e0.94) were significantly reduced by one-half, but the decrease in the rate of CAUTI per 1000 catheter-days (P1 19.6 to P2 16.9) did not reach statistical significance (Table II). No significant differences were observed regarding other complications associated with the handling of UC, although there was a non-significant increase in the number of episodes of acute urinary retention following the removal of UCs in P2 (Table II). The main reasons for UC placement in each period are listed in Table III. Diuresis control in a critical patient was the most frequent reason for urinary catheterization (66.4%). In P1, 14 cases of inadequately indicated catheterization were found (8.3%), 10 due to urinary incontinence and four for the collection of a urine sample in a continent patient. This number
Table I Characteristics of the patients who carried a urinary catheter according to the observation period Characteristics
Men Age (years), mean (SD) Charlson index score, mean (SD) Barthel index score, mean (SD) Origin House Socio-healthcare centre Hospital referral Background Relation with healthcare Diabetes mellitus Previous use of antibiotics (90 days) Previous hospitalization (90 days) Long-term permanent UC on arrival Immunosuppression Previous urological manipulation or surgery (30 days) Corticoids administered Repeated UTI (365 days) Prostatic hyperplasia (N ¼ 185)
Total (N ¼ 333)
185 79.8 3.6 52.9
(55.6%) (12.7) (2.0) (38.0)
220 (66.1%) 110 (33.0%) 2 (0.6%) 154 107 92 78 53 24 23 23 17 69
(46.4%) (32.1%) (27.7%) (23.5%) (15.9%) (7.2%) (6.9%) (6.9%) (5.1%) (37.5%)
Observation period
P
P1 (N ¼ 169)
P2 (N ¼ 164)
101 79.0 3.7 54.4
84 80.7 3.5 51.4
(59.8%) (13.5) (1.9) (38.5)
114 (67.5%) 55 (32.5%) 0 74 (44.0%) 46 (27.2%) 39 (23.2%) 36 (21.4%) 27 (16%) 6 (3.6%) 12 (7.1%) 11 (6.5%) 9 (5.4%) 31 (30.7%)
(51.2%) (11.8) (2.2) (37.4)
0.117 0.227 0.299 0.472 0.359
106 (64.6%) 55 (33.5%) 2 (1.2%) 80 61 53 42 26 18 11 12 8 38
(48.8%) (37.2%) (32.3%) (25.6%) (15.9%) (11.0%) (6.7%) (7.3%) (4.9%) (45.8%)
0.387 0.051 0.064 0.369 0.976 0.009 0.888 0.771 0.843 0.035
P1, period 1 or observation period before the multi-modal intervention; P2, period 2 or observation period during multi-modal intervention; UC, urinary catheter; UTI, urinary tract infection.
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Table II Comparative results of the indicators obtained during the pre-intervention observation period (January to March 2013) and the intervention observation period (January to March 2014) in patients with urinary catheter
No. of patients with UC In-hospital stay (daysa) Stay in IM department (daysa) Permanence of UC during in-hospital stay (daysa) Permanence of UC during stay in IM department (daysa) Patients with UC during the entire stayb Catheter-daysc (N) Patient-daysd (N) Catheterization rate (%) CAUTIb Rate of CAUTI (per 1000 catheter-days) Rate of CAUTI (per 1000 patient-days) Inadequate indication of UCb Obstruction of UCb Haematuria after insertion of UCb Acute urinary retention after removal of UCb
P1
P2
169 16.8 (11.4) 15.3 (11.0) 12.7 (10.4) 11.7 (10.1) 73 (43.2) 1582 5684 27.8 31 (18.3) 19.6 5.5 17 (10.1) 8 (4.7) 10 (5.9) 6 (3.5)
164 13.7 (11.0) 12.7 (9.3) 8.1 (8.2) 7.2 (6.4) 48 (29.3) 965 5695 16.9 16 (9.8) 16.6 2.8 4 (2.4) 8 (3.7) 12 (7.3) 13 (7.9)
RR or IR (95% CI)
P
0.68 (0.50e0.91)
0.011 0.022 <0.0001 <0.0001 0.008
0.61 0.53 0.85 0.52 0.24 0.77 1.24 2.23
<0.0001 0.025 0.587 0.028 0.004 0.626 0.608 0.086
(0.57e0.65) (0.30-0.93) (0.46e1.55) (0.28e0.94) (0.08e0.74) (0.27e2.18) (0.55e2.78) (0.87e5.73)
P1, period 1 or observation period before the multi-modal intervention; P2, period 2 or observation period during multi-modal intervention; RR, relative risk; IR, incidence rate; CI, confidence interval; UC, urinary catheter; IM, internal medicine; CAUTI, catheter-associated urinary tract infection. a Mean value (standard deviation). b Frequency (percentage). c Total days of permanence of UC per patient during the monitoring period. d Total bed occupancy of all patients admitted in the Department of Internal Medicine of the University Hospital of Salamanca during the observation period.
increases to 17 cases (10.1%) if we include three patients in whom no justified indication for catheterization was provided (Table III). The frequency of inappropriate catheterization decreased to four in P2 (2.4%), with two cases of urinary incontinence and two for sample collection in a continent patient, making the RR of an inadequate indication for UC placement 0.24 (95% CI: 0.08e0.71) (Tables II and III). Table III Reasons for urinary catheter insertion per observation period Reasons for UC insertion
Total (N ¼ 333)
Observation period P1 (N ¼ 169) P2 (N ¼ 164)
Diuresis control 221 (66.4%) 105 (62.1%) 116 (70.7%) in a critical patient AUR without haematuria 64 (19.2%) 32 (18.9%) 32 (19.5%) Urinary incontinence 12 (3.6%) 10 (5.9%) 2 (1.2%) Haematuria with AUR 8 (2.4%) 5 (3%) 3 (1.8%) Urinary incontinence and 7 (2.1%) 4 (2.4%) 3 (1.8%) sacral or perineal wound Sample collection 6 (1.8%) 4 (2.4%) 2 (1.2%) in continent patient Sample collection 5 (1.5%) 2 (1.2%) 3 (1.8%) in incontinent patient Prolonged immobilization 4 (1.2%) 2 (1.2%) 2 (1.2%) Palliative care 2 (0.6%) 1 (0.6%) 1 (0.6%) Perioperative 1 (0.3%) 1 (0.6%) 0 management Unknown 3 (0.9%) 3 (1.8%) 0 UC, urinary catheter; P1, period 1 or observation period before the multi-modal intervention; P2, period 2 or observation period during multi-modal intervention; AUR, acute urinary retention.
Discussion Several means of limiting extended use of UCs and lowering the incidence of CAUTIs, such as continuing training of healthcare professionals on the efficient use of UC, use of systems of active monitoring or reminders during UC use, stop orders, and combinations of previous measures have been described in the literature.2,11,13,19e25 Our study used a multimodal evidence-based approach that followed current clinical guidelines for the prevention of CAUTIs.5 To our knowledge, this is the first study that reports on experiences in Spain involving monitoring and a reminder system to reduce UC use specifically in an internal medicine unit. The most relevant result of this study is the decrease in UC use and in CAUTI frequency following implementation of the multi-modal intervention. This is in line with the findings reported by previous studies carried out in other countries and confirms that its application in the context of the Spanish health system is viable.2,13 Once urinary catheterization takes place, the residence time of the UC is the most important modifiable risk factor for the appearance of CAUTI, reinforcing the notion that the most widely used indicator for the assessment of preventive interventions of these infections is the catheterization rate.10,14 In our study, this indicator fell by 39% during P2, which is comparable with the 7e51% reported in the literature for various multi-modal interventions.2,13,26 The capacity of these interventions to reduce this indicator may be influenced, among other factors, by the frequency of UC placement before the intervention and by the characteristics of the patient population. The heterogeneity of these two aspects makes it very difficult to offer a direct comparison between studies. However, it is remarkable that in our study the
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patients were older and the initial catheterization rate and residence time of the UC were higher compared to other studies in neighbouring countries.2,13 Our study, based on a multi-modal intervention approach, demonstrated a reduction in the risk and the rate of CAUTI and also supports the findings of previous studies. Published reports have noted that 2e45% of patients with a UC experience a CAUTI, and the CAUTI rate ranges from 2 to 36 per 1000 catheter-days.11 In addition, a recent meta-analysis indicated that the RR for CAUTI decreased by 28% and episodes of CAUTI per 1000 catheter-days were reduced by 53% in the intervention group (with the use of reminder systems or stop orders), compared to a reference group.11 In the present study it is also relevant that during P2 there was a significant decrease of 76% in the use of UCs with inadequate indication. This reduction is in line with other studies, which is particularly remarkable given the fact that in our study the rate of UC placement with inadequate indication before the multi-modal intervention was lower than is normally reported in the literature (10% vs 25%).19,20,27,28 Interestingly, a significant fall in the in-hospital length of stay during P2 was observed. This effect had also been previously reported as a result of interventions of this type.2 However, we cannot draw further conclusions due to a lack of adjustment for variables related to in-hospital length of stay such as severity of illness in the included patients. In fact, we believe that it is unlikely that this decrease in the in-hospital length of stay may be attributed to the reduction in the frequency of CAUTIs previously mentioned, because it was observed in catheterized patients both with and without CAUTIs (data not shown), and we should consider the possibility that the Hawthorne effect has exerted an influence on these results.29 Although the preepost test design is the most widely used model in studies assessing this type of intervention, the inclusion of a historical cohort as a comparison group may be interpreted as a limitation of this work.2,22,23 Accordingly, in an attempt to minimize this bias, our observations were performed during the same months in two consecutive years. Also, despite the methodology used in the study, there were no relevant differences between periods regarding bed occupancy, the number of episodes of urinary catheterization, and the characteristics of the patients. Further, in P2 there was a higher frequency of some known risk factors for UTI such as diabetes.30 Therefore, we consider that the decrease in the frequency of CAUTI during P2 could mainly be attributed to the reduction in the use of UCs due to the multi-modal intervention. Implementation of this project exclusively in a department of internal medicine of a university hospital might limit the generalization of these results. However, similar initiatives instituted in emergency departments, surgical departments, or intensive care units, or which included different services in the same centre, or multi-centre studies, have achieved similar results.2,13,19,20,23e26,31 In conclusion, the implementation of a multi-modal intervention including an array of evidence-based measures has been effective in reducing the catheterization rate and the frequency of CAUTIs. Accordingly, the implementation of this type of intervention should be considered in units with high rates of UC use and/or a high risk of CAUTI. Conflict of interest statement None declared.
Funding sources None.
Appendix A. Supplementary data Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.jhin.2016.07.011.
References 1. Sociedad Espan ˜ola de Medicina Preventiva Salud Pu ´blica e Higiene. Estudio EPINE-EPPS 2015. Informe Global de Espan ˜a, Sociedad Espan ˜ola de Medicina Preventiva Salud Pu ´blica e Higiene, 2015. 2. Marigliano A, Barbadoro P, Pennacchietti L, D’Errico MM, Prospero E, CAUTI Working Collaborative Group. Active training and surveillance: 2 good friends to reduce urinary catheterization rate. Am J Infect Control 2012;40:692e695. 3. Esparcia A, Artero A, Eiros JM, et al. Influence of inadequate antimicrobial therapy on prognosis in elderly patients with severe urinary tract infections. Eur J Intern Med 2014;25:523e527. 4. Garcia Viejo MA, Noguerado Asensio A. Grupo de Trabajo de las Infecciones Urinarias del Grupo de Trabajo de Enfermedades Infecciosas de la Sociedad Espanola de Medicina I. [Urinary tract infections in internal medicine.] Rev Clin Esp 2010;210:537e544. 5. Centers for Disease Control and Prevention. Catheter-associated urinary tract infection (CAUTI) event, device-associated module. NHSN patient safety component manual. Atlanta: CDC; 2012. 6. Kennedy EH, Greene MT, Saint S. Estimating hospital costs of catheter-associated urinary tract infection. J Hosp Med 2013;8:519e522. 7. Gould CV, Umscheid CA, Agarwal RK, Kuntz G, Pegues DA, Healthcare Infection Control Practices Advisory Committee. Guideline for prevention of catheter-associated urinary tract infections 2009. Infect Control Hosp Epidemiol 2010;31:319e326. 8. Hooton TM, Bradley SF, Cardenas DD, et al. Diagnosis, prevention, and treatment of catheter-associated urinary tract infection in adults: 2009 International Clinical Practice Guidelines from the Infectious Diseases Society of America. Clin Infect Dis 2010;50:625e663. 9. Platt R, Polk BF, Murdock B, Rosner B. Risk factors for nosocomial urinary tract infection. Am J Epidemiol 1986;124:977e985. 10. Crouzet J, Bertrand X, Venier AG, Badoz M, Husson C, Talon D. Control of the duration of urinary catheterization: impact on catheter-associated urinary tract infection. J Hosp Infect 2007;67:253e257. 11. Meddings J, Rogers MA, Krein SL, Fakih MG, Olmsted RN, Saint S. Reducing unnecessary urinary catheter use and other strategies to prevent catheter-associated urinary tract infection: an integrative review. BMJ Qual Saf 2014;23:277e289. 12. Wald HL, Kramer AM. Nonpayment for harms resulting from medical care: catheter-associated urinary tract infections. JAMA 2007;298:2782e2784. 13. Leblebicioglu H, Ersoz G, Rosenthal VD, et al. Impact of a multidimensional infection control approach on catheter-associated urinary tract infection rates in adult intensive care units in 10 cities of Turkey: International Nosocomial Infection Control Consortium findings (INICC). Am J Infect Control 2013;41:885e891. 14. Lo E, Nicolle LE, Coffin SE, et al. Strategies to prevent catheterassociated urinary tract infections in acute care hospitals: 2014 update. Infect Control Hosp Epidemiol 2014;35:464e479. 15. Safdar N, Abad C. Educational interventions for prevention of healthcare-associated infection: a systematic review. Crit Care Med 2008;36:933e940. 16. Talaat M, Hafez S, Saied T, Elfeky R, El-Shoubary W, Pimentel G. Surveillance of catheter-associated urinary tract infection in 4 intensive care units at Alexandria university hospitals in Egypt. Am J Infect Control 2010;38:222e228.
H.G. Ternavasio-de la Vega et al. / Journal of Hospital Infection 94 (2016) 175e181 17. Murcia J, Llorens P, Sanchez-Paya J, et al. Functional status determined by Barthel Index predicts community acquired pneumonia mortality in general population. J Infect 2010;61: 458e464. 18. Charlson M, Szatrowski TP, Peterson J, Gold J. Validation of a combined comorbidity index. J Clin Epidemiol 1994;47:1245e1251. 19. Fakih MG, Heavens M, Grotemeyer J, Szpunar SM, Groves C, Hendrich A. Avoiding potential harm by improving appropriateness of urinary catheter use in 18 emergency departments. Ann Emerg Med 2014;63:761e768.e761. 20. Scott RA, Oman KS, Makic MB, et al. Reducing indwelling urinary catheter use in the emergency department: a successful qualityimprovement initiative. J Emerg Nurs 2014;40:237e244. 21. Delgado-Rodriguez M, Gomez-Ortega A, Sillero-Arenas M, Martinez-Gallego G, Medina-Cuadros M, Llorca J. Efficacy of surveillance in nosocomial infection control in a surgical service. Am J Infect Control 2001;29:289e294. 22. Chen YY, Chi MM, Chen YC, Chan YJ, Chou SS, Wang FD. Using a criteria-based reminder to reduce use of indwelling urinary catheters and decrease urinary tract infections. Am J Crit Care 2013;22:105e114. 23. Unawane AV, Patel K, Bhullar JS, Subhas G, Mittal VK, Cheung LY. Success of reminder systems in reducing catheter-associated urinary tract infections. Am Surg 2013;79:745e746. 24. Clarke K, Tong D, Pan Y, et al. Reduction in catheter-associated urinary tract infections by bundling interventions. Int J Qual Health Care 2013;25:43e49.
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25. Rosenthal VD, Todi SK, Alvarez-Moreno C, et al. Impact of a multidimensional infection control strategy on catheterassociated urinary tract infection rates in the adult intensive care units of 15 developing countries: findings of the International Nosocomial Infection Control Consortium (INICC). Infection 2012;40:517e526. 26. Marra AR, Sampaio Camargo TZ, Goncalves P, et al. Preventing catheter-associated urinary tract infection in the zero-tolerance era. Am J Infect Control 2011;39:817e822. 27. Caramujo N, Carvalho M, Caria H. Prevalence of inappropriate urinary catheterization: a preventable risk factor. Acta Med Port 2011;24(Suppl 2):517e522. 28. Fernandez-Ruiz M, Calvo B, Vara R, Villar RN, Aguado JM. Inappropriate use of urinary catheters in patients admitted to medical wards in a university hospital. Enferm Infecc Microbiol Clin 2013;31:523e525. 29. Srigley JA, Furness CD, Baker GR, Gardam M. Quantification of the Hawthorne effect in hand hygiene compliance monitoring using an electronic monitoring system: a retrospective cohort study. BMJ Qual Saf 2014;23:974e980. 30. Temiz E, Piskin N, Aydemir H, et al. Factors associated with catheter-associated urinary tract infections and the effects of other concomitant nosocomial infections in intensive care units. Scand J Infect Dis 2012;44:344e349. 31. Murphy C, Fader M, Prieto J. Interventions to minimise the initial use of indwelling urinary catheters in acute care: a systematic review. Int J Nurs Stud 2014;51:4e13.