Reducing Vancomycin Use in a Level IV NICU Rana F. Hamdy, MD, MPH, MSCE,a,b Sopnil Bhattarai, BS,c Sudeepta K. Basu, MD,b,d Andrea Hahn, MD, MS,a,b Brian Stone, MD, MBA,b,d Eleanor D. Sadler, PharmD,e Benjamin M. Hammer, PharmD,e John Galiote, MD,b,d Julie Slomkowski, PharmD,f Anne M. Casto, MSN, NNP-BC,d,g Katelyn P. Korzuch, MMS, PA-C,d Hannah Chase, BS,h,i Nneka Nzegwu, DO, MPH,b,d Isabella Greenberg, MPH,c Noelle Ortiz, MPH, MBS,h,i Carmen Blake, RN,g Jaeho Chang, MA,c James E. Bost, MS, PhD,h,i Asha S. Payne, MD, MPH,d,j Rahul K. Shah, MD, MBA,c,k Lamia Soghier, MD, MEdb,d

BACKGROUND AND OBJECTIVES: Vancomycin remains one of the most commonly abstract prescribed antibiotics in NICUs despite recommendations to limit its use for known resistant . Baseline data revealing substantially higher vancomycin use in our NICU compared to peer institutions informed our quality improvement initiative. Our aim was to reduce the vancomycin prescribing rate in neonates hospitalized in our NICU by 50% within 1 year and sustain for 1 year. METHODS: In the 60-bed level IV NICU of an academic referral center, we used a quality improvement framework to develop key drivers and interventions including (1) education with benchmarking antibiotic prescribing rates; (2) -initiated 48-hour antibiotic time-outs on rounds; (3) development of clinical pathways to standardize empirical antibiotic choices for early-onset , late-onset sepsis, and necrotizing enterocolitis; coupled with (4) daily prospective audit with feedback from the antimicrobial stewardship program. RESULTS: We used statistical process u-charts to show vancomycin use declined from 112 to 38 days of per 1000 patient-days. After education, pharmacy-initiated 48-hour time-outs, and development of clinical pathways, vancomycin use declined by 29%, and by an additional 52% after implementation of prospective audit with feedback. Vancomycin-associated acute kidney injury also declined from 1.4 to 0.1 events per 1000 patient- days. CONCLUSIONS: Through a sequential implementation approach of education, standardization of care with clinical pathways, pharmacist-initiated 48-hour time-outs, and prospective audit with feedback, vancomycin days of therapy declined by 66% over a 1-year period and has been sustained for 1 year. hChildren’s National Research Institute and iDivisions of Biostatistics and Study Methodology, aInfectious Diseases, cQuality and Patient Safety, dNeonatology, ePharmacy, jEmergency , and kOtolaryngology, and g Antibiotics are the most commonly 2 Department of , Children’s National , overuse is common. Overuse of Washington, District of Columbia; bDepartment of , prescribed class of medications in antibiotics in newborns is associated School of Medicine and Health Sciences, George Washington NICUs1,2 and are often prescribed with an increased risk of mortality5,6 and University, Washington, District of Columbia; and fPharmacy with great variability between Preceptor Program, Boston Medical Center, morbidities including necrotizing Boston, Massachusetts providers and institutions.2,3 enterocolitis (NEC),5 candidiasis,7 Although antibiotic use has proven resistant pathogens,8,9 and adverse drug successful in reducing effectssuchasnephrotoxicity.10 To cite: Hamdy RF, Bhattarai S, Basu SK, et al. 4 Reducing Vancomycin Use in a Level IV NICU. mortality from bacterial infections, Antibiotic exposure in neonates is also Pediatrics. 2020;146(2):e20192963

Downloaded from www.aappublications.org/news by guest on September 28, 2021 PEDIATRICS Volume 146, number 2, August 2020:e20192963 QUALITY REPORT associated with additional long-term morbidities such as asthma,11 inflammatory bowel disease,12 and obesity.13

Vancomycin is one of the most commonly prescribed antibiotics in NICUs.14 It is primarily indicated for treatment of methicillin-resistant staphylococcal infections because its use for other indications is often unwarranted because less toxic alternatives are preferable.14–17 Vancomycin is associated with acute kidney injury in up to 9% of neonates.10 Because of the aforementioned risk, the American Academy of Pediatrics and the Pediatric Infectious Disease Society, through the Choosing Wisely campaign, recommend judicious use of vancomycin and avoiding empirical vancomycin in newborns unless there FIGURE 1 – is a known risk for resistance to Baseline indications for vancomycin use in the NICU, July 2017 September 2017. This Pareto chart of 18 indications for vancomycin show that 76% of all vancomycin courses were for necrotizing entero- narrower-spectrum agents. colitis (with negative MRSA screen), Rule Out Sepsis, or Culture Negative Sepsis (negative MRSA screen).. CONS, coagulase negative Staphylococci; h/o, history of. When compared to peer , vancomycin usage in the Children’s National Hospital (CNH) NICU in outborn and transferred for were reviewed to identify indications “ 2016 was 3 times higher (95th care. After admission, all for vancomycin. An indication of rule ” fi percentile) than the mean use in receive a nasal methicillin- out sepsis was de ned as Staphylococcus aureus , children’s hospitals contributing to the resistant (MRSA) vancomycin use 72 hours for “ ” Pediatric Health Information System polymerase chain reaction surveillance suspected sepsis pending culture “ database (112 vs 34 days of therapy test at the time of admission and weekly results, whereas culture-negative ” fi [DOTs] per 1000 patient-days). thereafter. The incidence rate of MRSA sepsis was de ned when $ Informed by this benchmarking data colonization during the study period vancomycin use was continued 72 19 and by preliminary data revealing that was 0.92 per 1000 patient-days. A hours despite negative culture results “ ” approximately half of vancomycin use hospital-wide antimicrobial stewardship when the terms suspected sepsis or “ ” was for indications for which our team program (ASP) had been developed culture-negative sepsis were believed vancomycin was unnecessary within1yearoftheonsetofthisproject documented. For clinical indications (empirical use for NEC and culture- and focused on the development of for which culture results would not negative sepsis), our specificaimwas clinical pathways but had not yet drive antibiotic choices, the result of ’ to reduce vancomycin DOT per incorporated NICU stewardship the patient s routine MRSA 1000 patient-days by 50% in 1 year interventions. This project was surveillance swab was noted. The andsustainthisreductionfor1year. undertaken as a QI initiative at CNH; it most common indications for did not constitute human subjects vancomycin use were NEC, rule out research and was not under the sepsis, and culture-negative late- METHODS oversight of the institutional onset sepsis (LOS) (Fig 1). Baseline review board. data informed the development of Setting clinical pathways for common This prospective single-center quality Planning of Key Interventions conditions resulting in empirical improvement (QI) project was To understand the indications for vancomycin courses. conducted in a 60-bed level IV NICU vancomycin, a chart review was in an urban academic freestanding completed from July to September of Interventions children’s hospital. All infants 2017, with 514 days of vancomycin The Institute for Healthcare admitted to the CNH NICU were therapy identified. Physician notes Improvement Model for Improvement

Downloaded from www.aappublications.org/news by guest on September 28, 2021 2 HAMDY et al was used as the framework for our QI pharmacists to perform a “48-hour thereafter. The clinical pathways initiative. The key driver diagram antibiotic time-out.”21 Using Sentri7 incorporated these MRSA screen (Fig 2) provided a guide for project (Pharmacy OneSource, Inc, Madison, results to identify infants at low risk implementation. This project had 4 WI), all clinical pharmacists’ for MRSA . The clinical major interventions, described below. personalized dashboard identified pathways recommended patients who had been on antibiotics discontinuing vancomycin in infants Intervention 1: Development of an for $48 hours. Monday through without MRSA colonization if no Interdisciplinary Team and Provider Friday, the clinical pharmacist pathogens warranting vancomycin Education evaluated the patient list and therapy were isolated from cultures The interdisciplinary QI team prompted discussion of the antibiotic after 48 hours. The clinical pathways included practitioners from plan on rounds. Providers were were revised on the basis of , infectious diseases (ID), encouraged to either discontinue stakeholder feedback. Final approval pharmacy, nursing, and QI. The team vancomycin orders or to switch to was provided by the stakeholders and leader was an ID physician. a narrower-spectrum antibiotic as the institutional antimicrobial indicated. subcommittee of the pharmacy and An education session codelivered by therapeutics committee. The an ID and neonatology physician Intervention 3: Clinical Pathway pathways were posted in the NICU at summarized institutional antibiotic Development workstations, mobile computers, and prescribing practices compared to Derived from this initiative, new on the intranet and disseminated via peer hospitals and the rationale for clinical pathways for LOS and NEC e-mail to neonatology staff and stewardship. During this session, were developed with consensus from reviewed in educational sessions for neonatology providers were polled neonatology, ID, and faculty neonatology practitioners and about their prescribing practices. A (Supplemental Figs 7 and 8). The trainees. postcourse evaluation form sent to all clinical pathways were developed participants indicated that all after reviewing existing literature, Intervention 4: ASP Prospective Audit respondents were likely to change national consensus guidelines, local and Feedback practice after the education session. antibiotic susceptibility data from A member of the ASP (ID physician or clinical cultures of hospitalized pharmacist) reviewed all vancomycin Intervention 2: Pharmacist-Initiated neonates over the past several years, orders in the NICU daily (Monday 48-Hour Time-Out and guidelines implemented at other through Friday). If opportunities to – The division of pharmacy institutions.22 26 At our institution, it de-escalate were identified, implemented a formal policy is standard to perform universal recommendations were requiring clinical pharmacy MRSA surveillance for all infants after communicated either via the NICU specialists and unit-based admission to the NICU and weekly pharmacist or directly with phone calls to the medical team. If the recommendation was not followed within 24 hours, the ASP medical director contacted the neonatology attending directly.

Measures Outcome Measure The primary outcome measure was vancomycin DOTs per 1000 patient- days. A DOT was defined as $1 doses of intravenous vancomycin administered to the patient on a calendar day. Antibiotic data were obtained from the hospital pharmacy dispense database. NICU patient-days FIGURE 2 were obtained from the hospital daily Key driver diagram for vancomycin reduction in the NICU. Levels of reliability (LOR) of 1 (helping census. teams develop a standardized workflow) and 2 (developing error-proof systems to prevent work- arounds) were implemented20; no level 3 interventions were used. a A 50% reduction by September A secondary outcome measure was 2018 as compared to September 2016 through August 2017. vancomycin-associated acute kidney

Downloaded from www.aappublications.org/news by guest on September 28, 2021 PEDIATRICS Volume 146, number 2, August 2020 3 injury (AKI), defined according to the as a death in the setting of a blood was used as a washout period. For the neonatal modified Kidney Disease culture with growth of a Gram- third process measure, a p-chart was Improving Global Outcomes positive bacterial pathogen within 14 used to evaluate the proportion of criteria,27 as either $50% increase in days. Positive blood culture results pharmacist-initiated 48-hour time- serum creatinine above the baseline were extracted from the microbiology outs for vancomycin documented (lowest in the 6 months before laboratory database, and mortality each month, using all vancomycin initiating vancomycin), with the data were collected from our courses prescribed for .48 hours as increased value above a threshold of institution’s database maintained as the denominator, excluding those 0.5 mg/dL or an absolute increase of part of the Children’s Hospital opportunities that occurred on 0.3 mg/dL that occurred during the Neonatal Consortium. a weekend when a pharmacist would course of vancomycin or up to not be available. To monitor the effect of these 48 hours after its discontinuation. interventions on overall and alternate Process Measures antibiotic use, additional balancing Balancing Measures measures included total antibiotic Gram-positive sepsis-related Compliance with the clinical pathway DOTs per 1000 NICU patient-days mortality rates and incidence rates of for NEC and LOS pathways was and clindamycin, oxacillin, and S aureus bacteremia episodes per determined by measuring ampicillin DOTs per 1000 NICU 1000 patient-days with 95% CIs vancomycin DOTs beyond 48 hours patient-days. for (1) NEC and (2) culture-negative estimated for a Poisson distribution sepsis in patients with a negative Analysis were compared between the baseline (September 2016–September 2017) MRSA screen result. These were Outcome Measure considered subgroup outcome and the periods after implementation – measures. Three 3-month audits were Statistical process control charts (October 2017 September 2019). performed through chart review by tracked outcome measures over time Antibiotic DOTs per 1000 patient- reviewing the medical records of all and were created by using Process days were monitored by using infants prescribed vancomycin. For Improvement Products software (QI a u-chart. each audit, all vancomycin courses for Charts) and QI Macros for Excel. that period were reviewed to identify Statistical process control charts rules the vancomycin indication. Each were applied for differentiating RESULTS vancomycin DOT was associated with special- versus common-cause 28 Primary Outcome Measure a specific indication. To provide variation. A u-chart was used for context for possible changes in the outcome measures vancomycin During the 1-year baseline period – antibiotic prescribing practices for DOTs per 1000 patient-days and (September 2016 September 2017), NEC, rates of NEC per 1000 patient- vancomycin-associated AKI events mean vancomycin use was 112 DOTs days were collected from the per 1000 patient-days. per 1000 patient-days. After Children’s Hospital Neonatal establishing the QI team and Process Measures fi Consortium. implementing the rst 3 Modified control charts were used for interventions (provider education, A third process measure, the number the first 2 process measures, pharmacist-initiated 48-hour time- of vancomycin orders per month for evaluating vancomycin DOTs beyond outs, and clinical pathway rollouts), which a 48-hour time-out was the first 48 hours of therapy for special-cause variation was detected, performed and documented by the patients with NEC with negative resulting in a 29% decrease in unit-based pharmacist (and whether MRSA screen results and culture- vancomycin use to 80 DOTs per it was followed), was used to monitor negative sepsis with negative MRSA 1000 patient-days. After pharmacist compliance with the 48- screen results. NEC rates per implementation of ASP team daily hour time-out policy. 1000 patient-days with 95% review, a second centerline shift was confidence intervals (CIs) were detected, with further decline in Balancing Measures calculated for a Poisson distribution vancomycin use to 38 DOTs per To ensure no patient harm resulted and compared between the pre- and 1000 patient-days. Over a period of from reduction of vancomycin use, postintervention periods. Because the 12 months (October 2017–September the incidence of S aureus bloodstream date of event (NEC) was not available 2018), these interventions resulted in infections and Gram-positive sepsis- but rather linked to the date of a 66% reduction in overall related mortality per 1000 patient- patient admission, 3 months vancomycin use from baseline. These days was monitored. Gram-positive (representing .95th percentile for results were sustained for 1 year sepsis-related mortality was defined NICU length of stay at our institution) (Fig 3).

Downloaded from www.aappublications.org/news by guest on September 28, 2021 4 HAMDY et al (August–October 2018) with an overall reduction of 88%. Excluding the first 2 DOTs, vancomycin DOTs for culture-negative sepsis decreased from 22 DOTs per month in the baseline period to 13 DOTs per month (February–April 2018) and subsequently to 8 DOTs per month (August–October 2018) (overall 63% reduction) (Fig 5). The incidence rate of NEC in the preintervention period (September 2016–July 2017) was 4.31 per 1000 patient-days (95% CI: 3.24–5.73) and was 2.63 per 1000 patient-days (95% CI: FIGURE 3 1.88–3.67) in the postintervention Vancomycin use in the Children’s National NICU, 2016–2019: U-chart for vancomycin DOTs per period (December 2017–December 1000 patient-days. The green dashed line indicates target vancomycin DOTs per 1000 patient-days 2018). The incidence rate ratio of the (50% of baseline; 56 DOTs per 1000 patient-days). The red solid line indicates mean vancomycin DOTs postintervention period compared to per 1000 patient-days for neonatal services (34 DOTs per 1000 patient-days) among 40 children’s hospitals contributing data to Pediatric Health Information System. LCL, lower control limit; UCL, the preintervention period was 0.61 upper control limit. (95% CI: 0.39–0.95). After implementation, the proportion of documented pharmacist-initiated Secondary Outcome Process Measures 48-hour time-out interventions out of For the baseline period, the rate of Vancomycin DOTs for NEC beyond all possible opportunities averaged vancomycin-associated AKI was 1.4 the first 48 hours of therapy declined 49% with wide variation month to events per 1000 patient-days. After from 66 per month during the month (Supplemental Figs 9 and 10). the interventions, special-cause baseline period (July–September variation was noted with a decline to 2017) to 20 DOTs per month Balancing Measures 0.1 events per 1000 patient-days (February–April 2018) and S aureus bacteremia incidence ranged (Fig 4). subsequently to 8 DOTs per month from 0 to 1 episode per month, with no significant difference in incidence from the preintervention period (0.42 episodes per 1000 patient-days) to the postintervention period (0.31 episodes per 1000 patient-days) (P = .57). The Gram-positive sepsis-related mortality rate was 0.089 deaths per 1000 patient-days in the preintervention period (September 2016–September 2017) and 0.099 deaths per 1000 patient-days in the postintervention period (October 2017–January 2019), with an incident rate ratio of 1.10 (95% CI: 0.12–10.1). Antibiotic prescribing for all antibiotics in the NICU declined by 20% from 600 in the baseline period to 480 DOTs per 1000 patient-days in the postintervention period. Ampicillin use remained the same, FIGURE 4 whereas the clindamycin and Vancomycin-associated AKI events per 1000 NICU patient-days (u-chart). LCL, lower control limit; UCL, oxacillin prescribing rates increased upper control limit. (Fig 6).

Downloaded from www.aappublications.org/news by guest on September 28, 2021 PEDIATRICS Volume 146, number 2, August 2020 5 basis of benchmarking data, but because vancomycin continues to be 1 of the most commonly prescribed antibiotics in NICUs across the United States, the interventions we have described are likely to be of interest to other centers.

Authors of previous studies evaluating judicious vancomycin use in the NICU setting have used strategies focusing on both limiting empirical starts of vancomycin29,30 and de-escalation from vancomycin,31 which was the primary focus in our study. To our knowledge, this is the first work to reveal a significant change in vancomycin-associated AKI in neonates. Admittedly, this is not a surprising result given the high baseline vancomycin prescribing rate and substantial decrease in opportunities to develop vancomycin- associated AKI. Two retrospective chart reviews of blood culture positive for LOS revealed that not using vancomycin empirically for LOS did not negatively impact clinical outcomes including sepsis duration 29,30 32 FIGURE 5 and mortality rate. Chiu et al A, Control chart for vancomycin DOTs for NEC beyond the first 48 hours and with negative MRSA implemented a guideline in 2 tertiary- screen results. B, Control chart for vancomycin DOTs for culture-negative result for LOS beyond the care NICUs with low rates of MRSA fi rst 48 hours and with negative MRSA screen results. LCL, lower control limit; UCL, upper fi control limit. infection and found both a signi cant decrease in the number of vancomycin starts as well as DISCUSSION AKI without a change in Gram- a reduction in the number of infants positive sepsis-related mortality or S treated with vancomycin per In the level IV NICU of an urban aureus infections. Although 1000 patient-days. Compared to their academic freestanding children’s vancomycin DOTs per 1000 patient- study, our initiative resulted in hospital with a high baseline days decreased by 66%, an overall a greater reduction in vancomycin vancomycin prescribing rate, 20% reduction in total antibiotic DOTs while focusing primarily on de- a sequential approach of education DOTs per 1000 patient-days was escalation of vancomycin rather than (level 1 reliability), standardization of noted, suggesting that not all limiting initiation of empirical 31 care with clinical pathways (level 2 vancomycin reduction was achieved vancomycin. Holzmann-Pazgal et al reliability), pharmacist-initiated 48- through replacement with an evaluated the effectiveness of hour time-outs (level 2 reliability), alternate antibiotic. a combination of education, guideline and prospective audit with feedback development, and prospective audit (level 2 reliability) lowered the rate of The relevance of these results are with feedback in a single-center vancomycin DOTs per 1000 patient- highlighted by a recent large tertiary-care NICU. They found days by 66% over a 1-year period. retrospective review of .300 NICUs significant decreases in vancomycin This exceeded the target and has been across the United States identifying use after education and guideline sustained for 1 year. The patient vancomycin as the fourth most development but no additional safety implications of this common medication used.14 We decreases after adding audit with achievement are highlighted by found an acute need to decrease the feedback. Our study, on the other decrease in vancomycin-associated vancomycin within our NICU on the hand, revealed initial 30% reduction

Downloaded from www.aappublications.org/news by guest on September 28, 2021 6 HAMDY et al FIGURE 6 A, Total antibiotic DOTs per 1000 patient-days, u-chart for September 2016–December 2018. B, Ampicillin DOTs per 1000 patient-days, u-chart for September 2016–December 2018. C, Oxacillin DOTs per 1000 patient-days, u-chart for September 2016–December 2018. D, Clindamycin DOTs per 1000 patient-days, u-chart for September 2016–December 2018. CL, centerline; LCL, lower control limit; UCL, upper control limit. in vancomycin use after education opinion because clear evidence to opportunities; this may have been in and clinical pathway implementation, support 1 antibiotic regimen over part because of pharmacist personnel but it was only after implementing another is lacking. Interestingly, rates shortage for several months and prospective audit with feedback that of NEC were lower in the represents an opportunity for our target was achieved with postintervention period compared to improvement for the future. Lastly, a decline in vancomycin use of .50%. the preintervention period, implying although balancing measures are One notable difference is that in their that other factors may have important components of any QI study, prospective audit with contributed to the decline in project to monitor potential feedback was performed by NICU vancomycin use for NEC (process unintended consequences, it should staff , whereas in our measure). Second, although the be noted that this was not intended to model, the antimicrobial stewardship definition of vancomycin-associated be a study powered to detect team (ID physician and/or AKI is one frequently used in a difference in S aureus infections or pharmacist) provided the feedback to published literature,33,34 additional Gram-positive sepsis-related NICU physicians to de-escalate factors contributing to AKI were not mortality. Because these are rare vancomycin when indicated. accounted for, such as concomitant events, a difference may not have nephrotoxic drugs and severity of been detected by this methodology. There are several limitations to this illness. Additionally, 48-hour time- study. First, the clinical pathways outs were only documented as having Future directions of our initiative developed for NEC and LOS were been performed approximately one- include using clinical decision based on best practice and expert half of the time for all potential support within the electronic health

Downloaded from www.aappublications.org/news by guest on September 28, 2021 PEDIATRICS Volume 146, number 2, August 2020 7 record to provide alerts after a potentially nephrotoxic drug that ABBREVIATIONS 48 hours and risk stratifying which should be reserved for treatment of patients should be started empirically known antibiotic resistant infections. AKI: acute kidney injury on vancomycin.32 ASP: antimicrobial stewardship program ACKNOWLEDGMENTS CI: confidence interval CONCLUSIONS We acknowledge the additional QI CNH: Children’s National Through a sequential implementation team members Marsha Conroy, Hospital approach of education, PharmD, and Anna Espeland, DOT: day of therapy standardization of care with clinical PharmD, as well as Sofia Perazzo, ID: infectious diseases pathways, pharmacist-initiated 48- Guillermo Miyashita, and Matthew LOS: late-onset sepsis hour time-outs, and prospective audit Tsao for assistance with data MRSA: methicillin-resistant with feedback, vancomycin DOTs collection and Drs Robin Steinhorn, Staphylococcus aureus declined by .60% over a 1-year Billie Lou Short, and Roberta DeBiasi NEC: necrotizing enterocolitis period. This QI initiative safely for their executive support of this QI: quality improvement decreased unnecessary exposure to project.

Dr Hamdy conceptualized and designed the study, designed the data collection and management plan, coordinated and supervised data collection, analyzed the data, and drafted the initial manuscript; Mr Bhattarai contributed to the study design and data management plan, performed data interpretation, and drafted sections of and critically revised the manuscript; Dr Basu contributed to the study design and data management plan, supervised data interpretation, and drafted sections of and critically reviewed the manuscript; Dr Hahn contributed to the study design, performed data collection, and drafted portions of and critically reviewed the manuscript; Dr Galiote, Dr Stone, Ms Casto, and Ms Korzuch contributed to the study design, performed data collection, and critically reviewed the manuscript; Dr Sadler performed data collection and data interpretation, drafted portions of the manuscript, implemented interventions, and critically revised the full manuscript; Dr Hammer contributed to the study design, drafted portions of the manuscript, and critically reviewed the manuscript; Dr Slomkowski contributed to the study design, collected data, implemented interventions, and critically reviewed the manuscript; Ms Chase and Mr Chang performed data collection and data analysis and critically reviewed the manuscript; Dr Nzegwu performed data analysis and interpretation and critically revised the manuscript; Ms Greenberg, Ms Ortiz, and Dr Bost performed data analysis and critically reviewed the manuscript; Ms Blake contributed to the study design and conceptualization, performed data collection, and critically reviewed the manuscript; Dr Payne contributed to the study design, performed data interpretation, and critically revised the manuscript; Dr Shah contributed to the study design and critically reviewed the manuscript; Dr Soghier conceptualized and designed the study, designed the data collection and management plan, analyzed and interpreted the data, and critically reviewed the manuscript; and all authors approved the final manuscript as submitted. DOI: https://doi.org/10.1542/peds.2019-2963 Accepted for publication Mar 23, 2020 Address correspondence to Rana F. Hamdy, MD, MPH, MSCE, Division of Infectious Diseases, Children’s National Hospital, 111 Michigan Ave NW, West Wing 3.5, Suite 100, Washington, DC 20010. E-mail: [email protected] PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275). Copyright © 2020 by the American Academy of Pediatrics FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose. FUNDING: No external funding. POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conflicts of interest to disclose.

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Downloaded from www.aappublications.org/news by guest on September 28, 2021 PEDIATRICS Volume 146, number 2, August 2020 9 Reducing Vancomycin Use in a Level IV NICU Rana F. Hamdy, Sopnil Bhattarai, Sudeepta K. Basu, Andrea Hahn, Brian Stone, Eleanor D. Sadler, Benjamin M. Hammer, John Galiote, Julie Slomkowski, Anne M. Casto, Katelyn P. Korzuch, Hannah Chase, Nneka Nzegwu, Isabella Greenberg, Noelle Ortiz, Carmen Blake, Jaeho Chang, James E. Bost, Asha S. Payne, Rahul K. Shah and Lamia Soghier Pediatrics originally published online July 1, 2020;

Updated Information & including high resolution figures, can be found at: Services http://pediatrics.aappublications.org/content/early/2020/06/29/peds.2 019-2963 References This article cites 30 articles, 7 of which you can access for free at: http://pediatrics.aappublications.org/content/early/2020/06/29/peds.2 019-2963#BIBL Subspecialty Collections This article, along with others on similar topics, appears in the following collection(s): Administration/Practice Management http://www.aappublications.org/cgi/collection/administration:practic e_management_sub Quality Improvement http://www.aappublications.org/cgi/collection/quality_improvement_ sub Fetus/Newborn Infant http://www.aappublications.org/cgi/collection/fetus:newborn_infant_ sub Neonatology http://www.aappublications.org/cgi/collection/neonatology_sub Permissions & Licensing Information about reproducing this article in parts (figures, tables) or in its entirety can be found online at: http://www.aappublications.org/site/misc/Permissions.xhtml Reprints Information about ordering reprints can be found online: http://www.aappublications.org/site/misc/reprints.xhtml

Downloaded from www.aappublications.org/news by guest on September 28, 2021 Reducing Vancomycin Use in a Level IV NICU Rana F. Hamdy, Sopnil Bhattarai, Sudeepta K. Basu, Andrea Hahn, Brian Stone, Eleanor D. Sadler, Benjamin M. Hammer, John Galiote, Julie Slomkowski, Anne M. Casto, Katelyn P. Korzuch, Hannah Chase, Nneka Nzegwu, Isabella Greenberg, Noelle Ortiz, Carmen Blake, Jaeho Chang, James E. Bost, Asha S. Payne, Rahul K. Shah and Lamia Soghier Pediatrics originally published online July 1, 2020;

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