American Journal of Health-System Pharmacy

Rico, Matthew; Sulaiman, Rand; MacLeod, Rachel

doi: 10.1093/ajhp/zxab220pmid: 34037694

Abstract Purpose The purpose of this study was to evaluate the effect of an antimicrobial stewardship bundle on the management of asymptomatic bacteriuria (ASB). Methods In this quasi-experimental study, patients were selected by retrospective, consecutive sampling of patients with a positive urine culture report in 3 separate groups: preintervention, postdiagnostic intervention, and posteducation. Patients met the prespecified criteria for non–catheter-associated ASB. The diagnostic intervention involved a new urinalysis/urine culture ordering process in place of urinalysis with reflex to urine culture. Additionally, an educational intervention involved pharmacist-led sessions to educate providers with patient cases and guideline-based recommendations. The primary outcome of this study was the difference in the rate of inappropriate management of ASB, defined as the use of antimicrobial agents intended to treat ASB. Secondary outcomes included length of antimicrobial therapy, length of stay, and change in urine culture orders per 1,000 patient-days. Results A total of 120 patients were included. There was a significant reduction in the inappropriate management of ASB between the preintervention and postdiagnostic intervention groups (P = 0.0349). This was not seen when comparing the postdiagnostic intervention and posteducation groups (P = 0.93). Additionally, there was a significant difference in urinalysis/urine culture ordering between the preintervention and postdiagnostic intervention groups (370 vs 224 urinalysis orders per 1,000 days present, P < 0.0001; 131 vs 54 urine culture orders per 1,000 days present, P < 0.0001). Conclusion An antimicrobial stewardship bundle involving a diagnostic stewardship intervention and pharmacist-led education reduced treatment of ASB in patients without urinary catheters. antimicrobial stewardship, asymptomatic bacteriuria, diagnostic stewardship, pharmacist education, UTI Because of the increasing prevalence of antimicrobial resistance in the United States, implementing antimicrobial stewardship initiatives has become a key focus across health systems. One target for many inpatient antimicrobial stewardship programs is to limit the use of antimicrobials for asymptomatic bacteriuria (ASB).1,2 The Infectious Diseases Society of America (IDSA) recently published new recommendations on treatment of ASB as an update to their 2005 guidelines, further reiterating the unnecessary nature of antimicrobial use in the management of ASB in most patient populations.3 Despite these efforts, studies have reported that upwards of 65% of patients are treated with antimicrobials for ASB.4 Several antimicrobial stewardship programs across the United States have described the use of multifactorial approaches to reduce the use of antimicrobials in this patient population. Two different institutions used real-time clinical surveillance software to identify patients with positive urine cultures and/or abnormal urinalysis results, in turn prompting pharmacist-driven intervention to assess the appropriateness of antimicrobial therapy in each case. Results for the 2 studies were similar, showing an average reduction of 3 days of inappropriate treatment.5,6 Other interventions entailed pharmacist education of various healthcare providers to assess for changes in inappropriate management of ASB. These educational sessions commonly included guideline-based recommendations, information on diagnostic testing, and treatment algorithms to assist physicians in understanding the proper treatment of urinary tract infections (UTIs).7 Matthew Rico, PharmD, is the current postgraduate year 2 infectious diseases pharmacy resident at Beaumont Hospital in Royal Oak, MI. Dr. Rico received his bachelor of science degree in biology in 2016 and doctor of pharmacy degree in 2019 from Ferris State University in Big Rapids, MI. He completed a postgraduate year 1 pharmacy residency at Ascension Genesys Hospital in Grand Blanc, MI. His current research interests are in the areas of antimicrobial stewardship, therapeutic drug monitoring, and Gram-negative resistance. Additionally, some institutions have targeted a reduction in antimicrobial use based on modifying their electronic health record (EHR) to discourage the inappropriate ordering of urine cultures. Keller and colleagues8 implemented an alert to providers that accompanied all urinalysis orders, urine culture orders, and orders of common antimicrobials used to treat UTIs that recommended against urinary tests if the patient did not present with symptoms. This led to an overall reduction in urine culture orders and antimicrobial ordering within the first 24 hours after receipt of urinalysis results. Furthermore, Narayanan and colleagues9 implemented guided urine culture ordering in their EHR that forced prescribers to select indications for urine culture orders. This was coupled with pharmacist-driven education encompassing ASB and appropriate utilization of urine culture ordering that took place over a 1-month time period shortly after implementation of the EHR modifications. The authors saw an overall reduction in the percentage of patients who received antimicrobials for ASB in the posteducation period as compared to baseline (35% vs 42%). Current literature suggests the continued need for strategies to limit inappropriate ordering of urine cultures, which can lead to the overuse of antimicrobials. Much of the current data are from pharmacist-driven interventions that show promise for the reduction of inappropriate management of ASB. This study sought to further clarify the effect of pharmacist-led education coupled with a diagnostic stewardship intervention. The primary objective of the study was to evaluate the effect of our antimicrobial stewardship bundle, which primarily focused on diagnostic stewardship and pharmacist-driven education, on the management of ASB. Our study assessed the prescribing patterns of antimicrobial therapy for ASB before and after implementation of a diagnostic stewardship intervention as well as after targeted educational sessions. Methods This study was conducted at a 441-bed community teaching hospital in Michigan with institutional review board approval. Patients included in the study were hospitalized adults who were 18 years or older and met the definition of being treated for ASB. Patients were identified by consecutive sampling of patients with positive urine culture reports and retrospective chart review. ASB was defined as the identification of bacteria in a urine culture without documented signs or symptoms of urinary infection. A non–catheter-associated UTI was defined as meeting the following 3 criteria: (1) no catheter used for 2 or more days on the inpatient setting; (2) at least 1 of the following symptoms: fever of more than 100.4°F, suprapubic tenderness, costovertebral angle tenderness, urinary urgency, urinary frequency, or dysuria; and (3) 2 or fewer species of bacteria (>100,000 colony-forming units/mL) in the urine culture. Patients were excluded if they were pregnant, had a history of urinary stents, had a planned urologic procedure, had a concomitant infection, or had a history of spinal cord injury. Before the intervention, urine specimen ordering included the option for a provider to order a urinalysis with a urine culture reflex. If the urinalysis was found to have leukocyte esterase (positive), nitrites (positive), or white blood cells (11-25 white blood cells/high-power field), the urine would be further tested using a urine culture. Urinalyses were not assessed for contamination (ie, squamous cells); if a urine culture grew 3 or more organisms, the organisms were not identified and susceptibility testing was not performed. However, a message was entered under the urine culture result indicating probable contamination. To reduce the inappropriate treatment of ASB, a new protocol was put into place that sought to eliminate urinalysis with reflex to urine culture. This protocol included collection of a urine specimen in a sterile cup along with a separate tube for urine that was to be preserved for 48 hours. The urine collected in the sterile cup was used for urinalysis. If necessary, the provider could order a urine culture on the remaining urine in the test tube if there was a suspected or confirmed UTI within the next 48 hours. Alternatively, an immediate urine culture could be ordered if the patient presented with a confirmed UTI, based on clinician judgement. Of note, the collection method for the urine specimen was included as a mandatory checkbox (clean-catch, straight catheter, etc), with free text as an alternative option. In addition to the intervention within the electronic medical record, communication with preidentified provider champions was also an element of the bundle; this communication focused on helping institutional leaders understand our progress toward reducing inappropriate management of ASB. These champions included department leadership, nursing leadership, and the chief medical officer. Before initiation of the study, internal medicine, family medicine, and emergency department providers were educated about the treatment of ASB. This educational session was conducted by a pharmacist who provided an update on the IDSA recommendations for ASB management along with a detailed description of the diagnostic stewardship intervention. These formal educational sessions were performed separately over 3 months; a log of providers who attended the sessions was not collected. Providers were also supplied with a flyer that included a summary of the updated IDSA recommendations for ASB management along with an overview of the changes that would be made to the urinalysis/urine culture ordering process. Preintervention data were collected from admissions between October 2018 and January 2019, while postdiagnostic intervention data were collected between October 2019 and January 2020. The diagnostic intervention went into effect on August 30, 2019. After preintervention and postdiagnostic intervention patient data were collected, the primary investigator coordinated educational sessions with provider champions, internal medicine, family medicine, and the department of medicine to give an update on the institution’s overall progress in 3 separate sessions in March 2020. The educational sessions included a PowerPoint presentation (Microsoft Corporation, Redmond, WA) in which providers were reminded of how to appropriately manage ASB as well as how to utilize the new protocol’s order sets. Furthermore, 2 patient cases were included in the presentation to promote the identification of ASB through case-based questions. These questions were focused on identifying UTIs vs ASB. Providers received copies of the PowerPoint presentation, which included the urinalysis/urine culture ordering algorithm, and were encouraged to follow up with the corresponding author on further questions. Additional patient data collection began 1 week after completion of the educational sessions to assess the effect of the sessions on ASB management. The primary outcome of this study was the difference in the rate of inappropriate management of ASB, defined as the use of antimicrobial agents intended to treat ASB. Secondary outcomes included length of therapy for ASB, length of stay, urine cultures per 1,000 days present, and urinalysis orders per 1,000 days present. Statistical analysis. Data from the Michigan Hospital Medicine Safety Consortium (HMS) indicated a site-specific predicted treatment rate for ASB of 83% between 2018 and 2019. The goal set for HMS participants was a rate of less than 70%. It was determined that 100 patients needed to be included to detect a 20% difference in inappropriate ASB management between the preintervention and postdiagnostic intervention groups at 90% power (with a significance level of <0.05) using a t test for percentages. Twenty additional patients were included in the posteducation group to examine the retention behavior of the provider groups educated. The statistical tests used, including Wilcoxon rank-sum tests, Pearson’s χ2 tests, and Student’s t tests, are noted in Tables 1 and 2 for the variables included in this study; these tests were performed using R (version 4.0.0; R Foundation for Statistical Computing, Vienna, Austria) and evaluated at a significance level of 0.05. Results A total of 120 patients were included in the analysis. Fifty patients each were included in the preintervention and postdiagnostic intervention groups, while 20 patients were identified for inclusion in the posteducation group. Patient demographics are listed in Table 1. Patients in the preintervention group were significantly older than those in the postdiagnostic intervention and posteducation groups. Table 1. Patient Demographics Characteristic . Preintervention (n = 50) . Postdiagnostic Intervention (n = 50) . Posteducation (n = 20) . P Valuea . . . . . . . PI vs PE . PI vs PDI . PDI vs PE . Age, median (IQR), years 81 (76-85.75) 67.5 (61.25-79) 65 (63.5-69.5) <0.0001 <0.0001 0.33 Female sex, No. (%) 43 (86) 38 (76) 13 (65) 0.047 0.2 0.34 Characteristic . Preintervention (n = 50) . Postdiagnostic Intervention (n = 50) . Posteducation (n = 20) . P Valuea . . . . . . . PI vs PE . PI vs PDI . PDI vs PE . Age, median (IQR), years 81 (76-85.75) 67.5 (61.25-79) 65 (63.5-69.5) <0.0001 <0.0001 0.33 Female sex, No. (%) 43 (86) 38 (76) 13 (65) 0.047 0.2 0.34 Abbreviations: IQR, interquartile range; PDI, postdiagnostic intervention; PE, posteducation; PI, preintervention. aValues for age were evaluated by Wilcoxon rank-sum test while those for sex were evaluated by Pearson’s χ2 test. Open in new tab Table 1. Patient Demographics Characteristic . Preintervention (n = 50) . Postdiagnostic Intervention (n = 50) . Posteducation (n = 20) . P Valuea . . . . . . . PI vs PE . PI vs PDI . PDI vs PE . Age, median (IQR), years 81 (76-85.75) 67.5 (61.25-79) 65 (63.5-69.5) <0.0001 <0.0001 0.33 Female sex, No. (%) 43 (86) 38 (76) 13 (65) 0.047 0.2 0.34 Characteristic . Preintervention (n = 50) . Postdiagnostic Intervention (n = 50) . Posteducation (n = 20) . P Valuea . . . . . . . PI vs PE . PI vs PDI . PDI vs PE . Age, median (IQR), years 81 (76-85.75) 67.5 (61.25-79) 65 (63.5-69.5) <0.0001 <0.0001 0.33 Female sex, No. (%) 43 (86) 38 (76) 13 (65) 0.047 0.2 0.34 Abbreviations: IQR, interquartile range; PDI, postdiagnostic intervention; PE, posteducation; PI, preintervention. aValues for age were evaluated by Wilcoxon rank-sum test while those for sex were evaluated by Pearson’s χ2 test. Open in new tab When comparing the preintervention group and the posteducation group to assess the primary outcome, there was a difference in the percentage of cases with inappropriate management of ASB (88% vs 55%, P = 0.005). Additionally, there was a difference in median length of antimicrobial therapy for ASB between these groups (5.75 vs 4.45 days, P = 0.035). There was no significant difference in length of total inpatient stay between the groups (102.32 vs 94.20 hours, P = 0.79). Urinalysis and urine culture orders (Table 3) showed a significant decline between the preintervention and postdiagnostic intervention groups (data obtained from October 2018 to January 2019 and from October 2019 to January 2020, respectively) when evaluating orders per 1,000 days present (urinalyses: 370 vs 224, P < 0.0001; urine cultures: 131 vs 54, P < 0.0001). Table 3. Analysis of Diagnostic Ordering Test Ordered . Preintervention (n = 50) . Postdiagnostic Intervention (n = 50) . P Valuea . Urinalyses, No. per 1,000 days present 370 224 <0.0001 Urine cultures, No. per 1,000 days present 131 54 <0.0001 Test Ordered . Preintervention (n = 50) . Postdiagnostic Intervention (n = 50) . P Valuea . Urinalyses, No. per 1,000 days present 370 224 <0.0001 Urine cultures, No. per 1,000 days present 131 54 <0.0001 aValues evaluated by Student’s t test. Open in new tab Table 3. Analysis of Diagnostic Ordering Test Ordered . Preintervention (n = 50) . Postdiagnostic Intervention (n = 50) . P Valuea . Urinalyses, No. per 1,000 days present 370 224 <0.0001 Urine cultures, No. per 1,000 days present 131 54 <0.0001 Test Ordered . Preintervention (n = 50) . Postdiagnostic Intervention (n = 50) . P Valuea . Urinalyses, No. per 1,000 days present 370 224 <0.0001 Urine cultures, No. per 1,000 days present 131 54 <0.0001 aValues evaluated by Student’s t test. Open in new tab Further results of the analyses comparing the 3 groups can be found in Table 2. There was a significant difference in inappropriate management of ASB between the preintervention and postdiagnostic intervention groups (88% vs 58%, P = 0.0009). After adjusting for age and sex with a generalized linear model, this result remained significant (P = 0.0349). There were no significant differences between these 2 groups in terms of length of stay (102.32 vs 79.50 hours, P = 0.15). However, there was a significant difference in median length of antimicrobial therapy for ASB between the preintervention group and the postdiagnostic intervention group (5.75 vs 2.18 days, P = 0.0001). Table 2. Analysis of Inappropriate Management of Asymptomatic Bacteriuria, Length of Stay, and Antimicrobial Length of Therapy Clinical Characteristic . Preintervention (n = 50) . Postdiagnostic Intervention (n = 50) . Posteducation (n = 20) . P Valuea . . . . . . . PI vs PE . PI vs PDI . PDI vs PE . ASB treatment, No. (%) 44 (88) 29 (58) 11 (55) 0.005 0.0009 0.93 LOS, median (IQR), hours 102.32 (49.31-161.24) 79.50 (28.46-138.51) 94.20 (67.84-136.44) 0.79 0.15 0.27 LOT, median (IQR), days 5.75 (2.91-6.54) 2.18 (1.29-3.31) 4.45 (2.52-4.78) 0.035 0.0001 0.037 Clinical Characteristic . Preintervention (n = 50) . Postdiagnostic Intervention (n = 50) . Posteducation (n = 20) . P Valuea . . . . . . . PI vs PE . PI vs PDI . PDI vs PE . ASB treatment, No. (%) 44 (88) 29 (58) 11 (55) 0.005 0.0009 0.93 LOS, median (IQR), hours 102.32 (49.31-161.24) 79.50 (28.46-138.51) 94.20 (67.84-136.44) 0.79 0.15 0.27 LOT, median (IQR), days 5.75 (2.91-6.54) 2.18 (1.29-3.31) 4.45 (2.52-4.78) 0.035 0.0001 0.037 Abbreviations: ASB, asymptomatic bacteriuria; IQR, interquartile range; LOS, length of stay; LOT, antimicrobial length of therapy; PDI, postdiagnostic intervention; PE, posteducation; PI, preintervention. aValues for asymptomatic bacteriuria treatment and length of stay were evaluated by Pearson’s χ2 test while those for length of treatment were evaluated by Wilcoxon rank-sum test. Open in new tab Table 2. Analysis of Inappropriate Management of Asymptomatic Bacteriuria, Length of Stay, and Antimicrobial Length of Therapy Clinical Characteristic . Preintervention (n = 50) . Postdiagnostic Intervention (n = 50) . Posteducation (n = 20) . P Valuea . . . . . . . PI vs PE . PI vs PDI . PDI vs PE . ASB treatment, No. (%) 44 (88) 29 (58) 11 (55) 0.005 0.0009 0.93 LOS, median (IQR), hours 102.32 (49.31-161.24) 79.50 (28.46-138.51) 94.20 (67.84-136.44) 0.79 0.15 0.27 LOT, median (IQR), days 5.75 (2.91-6.54) 2.18 (1.29-3.31) 4.45 (2.52-4.78) 0.035 0.0001 0.037 Clinical Characteristic . Preintervention (n = 50) . Postdiagnostic Intervention (n = 50) . Posteducation (n = 20) . P Valuea . . . . . . . PI vs PE . PI vs PDI . PDI vs PE . ASB treatment, No. (%) 44 (88) 29 (58) 11 (55) 0.005 0.0009 0.93 LOS, median (IQR), hours 102.32 (49.31-161.24) 79.50 (28.46-138.51) 94.20 (67.84-136.44) 0.79 0.15 0.27 LOT, median (IQR), days 5.75 (2.91-6.54) 2.18 (1.29-3.31) 4.45 (2.52-4.78) 0.035 0.0001 0.037 Abbreviations: ASB, asymptomatic bacteriuria; IQR, interquartile range; LOS, length of stay; LOT, antimicrobial length of therapy; PDI, postdiagnostic intervention; PE, posteducation; PI, preintervention. aValues for asymptomatic bacteriuria treatment and length of stay were evaluated by Pearson’s χ2 test while those for length of treatment were evaluated by Wilcoxon rank-sum test. Open in new tab There was no significant difference between the postdiagnostic intervention and posteducation groups in terms of the percentage of cases with inappropriate ASB management (58% vs 55%, P = 0.93). Patients included in the posteducation group had a significantly longer duration of therapy than those in the postdiagnostic intervention group (4.45 vs 2.18 days, P = 0.037). Discussion Implementation of an antimicrobial stewardship bundle including a diagnostic intervention and provider education led to a decrease in the inappropriate management of ASB along with a reduction in median length of antimicrobial therapy for ASB. While with the overall bundle there were reductions in inappropriate management between the preintervention group and the posteducation group, the results of the study indicate greater impact of the diagnostic intervention as compared to the educational intervention. There was a significant reduction in inappropriate ASB management when comparing the preintervention and postdiagnostic intervention groups that was not seen when comparing the postdiagnostic intervention and posteducation groups. This may be attributable to the forcing function of the diagnostic stewardship intervention, which required providers to review urinalysis results and the patient’s clinical presentation and order the reflex culture within the indicated time frame instead of an automatic reflex urine culture being conducted. These results suggest that the diagnostic intervention component may have driven the decrease in ASB treatment observed. However, it is unreasonable to say that education did not play a part in the appropriate management of ASB, as the diagnostic intervention may have decreased rates of inappropriate management to such a degree that educational intervention might not have resulted in further significant reduction. Pharmacist education may have been required more frequently or may have been more beneficial at prespecified points nearer to the beginning of the postdiagnostic intervention phase to truly examine the effect of diagnostic stewardship and education on the outcome. There were several limitations with this analysis, including the retrospective collection of patient information. Patients’ inclusion in this study primarily relied on provider documentation of their symptoms in the electronic medical record. Therefore, patients may have presented with signs and symptoms of a UTI who were not able to be assessed during retrospective review or patients may have had nonspecific symptoms (ie, altered mental status) that may have made providers more inclined to treat for UTI. This may have been a confounding factor that was not accounted for in the analysis. However, after adjusting for age and sex, there was still a significant difference between ASB treatment in the preintervention and postdiagnostic intervention groups. Additionally, length of therapy in all 3 groups was likely underestimated in this study. Only antimicrobials given to patients during their inpatient stay were included in the analysis. During the postdiagnostic intervention phase, a pharmacist-driven ceftriaxone utilization initiative began. Pharmacists received an electronic alert when patients were on ceftriaxone for an indication of UTI or community-acquired pneumonia for greater than 48 hours. This could have unintentionally been a significant confounder in the results of this group in terms of inappropriate ASB management and length of antimicrobial therapy. Furthermore, owing to the time constraints of this study, the time between the cessation of education and posteducation intervention data collection was likely not adequate. Providers were not able to be fully tracked to determine whether education was completed for all targeted groups, owing to one of the education sessions being conducted in a virtual format to comply with coronavirus disease 2019 gathering restrictions. It is not clear why there was a significant increase in length of therapy between the postdiagnostic education group and the posteducation group. The smaller sample size of the posteducation group may have led to a higher median duration of therapy as compared to the larger preintervention and postdiagnostic intervention groups. Conclusion Overall, our study demonstrated that the implementation of an antimicrobial stewardship bundle including a diagnostic stewardship intervention and pharmacist-led education improved the management of ASB. Additionally, it reinforced the need for continued stewardship focus on ASB in the future. Furthermore, this study identified an opportunity for pharmacist involvement in assessing discharge antibiotics, which could lead to a further reduction in the overuse of antimicrobial agents in this patient population. Acknowledgments The authors thank David Blair, PharmD. Disclosures The authors have declared no potential conflicts of interest. 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Published by Oxford University Press on behalf of the American Society of Health-System Pharmacists 2021.