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Editor's Pick Epidemiology and Surveillance

A Propensity Score Matched Study of the Positive Impact of Infectious Diseases Consultation on Antimicrobial Appropriateness in Hospitalized Patients with Antimicrobial Stewardship Oversight

Jacqueline T. Bork, Kimberly C. Claeys, Emily L. Heil, Mary Banoub, Surbhi Leekha, John D. Sorkin, Michael Kleinberg
Jacqueline T. Bork
aUniversity of Maryland School of Medicine, Division of Infectious Diseases, Baltimore, Maryland, USA
gUniversity of Maryland Medical Center, Department of Medicine, Baltimore, Maryland, USA
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Kimberly C. Claeys
bUniversity of Maryland School of Pharmacy, Baltimore, Maryland, USA
cUniversity of Maryland Medical Center, Department of Pharmacy, Baltimore, Maryland, USA
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Emily L. Heil
bUniversity of Maryland School of Pharmacy, Baltimore, Maryland, USA
cUniversity of Maryland Medical Center, Department of Pharmacy, Baltimore, Maryland, USA
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Mary Banoub
cUniversity of Maryland Medical Center, Department of Pharmacy, Baltimore, Maryland, USA
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Surbhi Leekha
aUniversity of Maryland School of Medicine, Division of Infectious Diseases, Baltimore, Maryland, USA
dUniversity of Maryland School of Epidemiology and Public Health, Baltimore, Maryland, USA
gUniversity of Maryland Medical Center, Department of Medicine, Baltimore, Maryland, USA
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John D. Sorkin
eBaltimore VA Medical Center, Geriatric Research, Education, and Clinical Center, Baltimore, Maryland, USA
fUniversity of Maryland School of Medicine, Division of Gerontology and Geriatric Medicine, Baltimore, Maryland, USA
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Michael Kleinberg
aUniversity of Maryland School of Medicine, Division of Infectious Diseases, Baltimore, Maryland, USA
gUniversity of Maryland Medical Center, Department of Medicine, Baltimore, Maryland, USA
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DOI: 10.1128/AAC.00307-20
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ABSTRACT

Hospital-based antibiotic stewardship (AS) programs provide oversight and guidance for appropriate antimicrobial use in acute care settings. Infectious disease expertise is beneficial in the care of hospitalized patients with infections. The impact of infectious diseases consultation (IDC) on antimicrobial appropriateness in a large tertiary hospital with an established AS program was investigated. This was a cross-sectional study from October 2017 to March 2019 at a large academic hospital with an AS-directed prospective audit and feedback process and multiple IDC services. Antimicrobial appropriateness was adjudicated by an AS team member after antimicrobial start. Antimicrobial appropriateness was compared among antimicrobial orders with and without IDC using propensity score matching and multivariable logistic regression. Analyses were stratified by primary services caring for the patients. There were 10,508 antimicrobial orders from 6,165 unique patient encounters. Overall appropriateness was 92%, with higher appropriateness among patients with IDC versus without IDC (94% versus 84%; P < 0.0001). After propensity score matching and adjustment for certain antibiotics, organisms, syndromes, and locations, IDC was associated with a greater antimicrobial appropriateness odds ratio (OR) of 2.4 (95% confidence interval [CI], 1.9 to 3.0). Stratification by primary service showed an OR of 2.9 (95% CI, 2.1 to 3.8) for surgical specialties and an OR of 1.6 (95% CI, 1.1 to 2.2) for medical specialties. Even with a high overall antimicrobial appropriateness, patients with IDC had greater odds of antimicrobial appropriateness than those without IDC, and this impact was greater in surgical specialties. Infectious diseases consultation can be synergistic with antimicrobial stewardship programs.

INTRODUCTION

Antimicrobial stewardship (AS) reduces the inappropriate use of antimicrobial agents and is associated with improved outcome measures, such as decreased antimicrobial usage, lower health care cost, decreased antimicrobial resistance, and decreased length of hospital stay (1–4). AS programs improve outcome measures by providing oversight for antimicrobial prescriptions leading to more appropriate use. Due to regulations imposed by governing bodies such as the Centers for Disease Control and Prevention (CDC) and The Joint Commission, AS presence in acute care hospitals is increasing in the United States with the national goal of 100% by 2020 (5; see also https://www.jointcommission.org/en/resources/patient-safety-topics/infection-prevention-and-control/antimicrobial-stewardship/ and https://www.cdc.gov/antibiotic-use/core-elements/hospital.html).

The infectious diseases consultation (IDC) service is a clinical service that provides infectious diseases expertise at the patient bedside for difficult diagnostic and treatment decisions. Patient outcome measures, such as mortality and length of hospital stay, are improved when IDC is obtained (6, 7). One possible explanation for the clinical impact of IDC on patient care is the reduction of inappropriate use of antimicrobial agents.

We studied the role of the IDC in the context of AS activities at a large academic medical center. Our aims were to (i) describe the antimicrobial appropriateness in hospitalized patients with AS oversight, (ii) compare the proportion of antimicrobial appropriateness with and without IDC, and (iii) evaluate the impact of IDC on antimicrobial appropriateness among the different primary services. We hypothesized that antimicrobial orders audited by the AS program in patients with IDC were more likely appropriate compared to those without IDC.

RESULTS

There were 84,418 total antimicrobial prescriptions of which 10,507 (representing 6,615 unique patient encounters) met inclusion criteria and were reviewed by the AS team (Fig. 1). Baseline characteristics are described and compared among the IDC and no-IDC groups in Table 1. IDC was present in 72% of AS team-reviewed antibiotics. There were several differences between prescriptions written with and without IDC consultation. Antimicrobial prescriptions with IDC were more likely to be written for patients on surgical services, in the ICU, with positive cultures, and receiving restricted antimicrobials. Antimicrobial prescriptions without IDC were more likely to be written for patients on medical services, receiving a broad-spectrum antibiotic, and treated for either community-acquired pneumonia or genitourinary infections.

FIG 1
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FIG 1

Sample selection. HIV, human immunodeficiency virus; HCV, hepatitis C virus; HBV, hepatitis B virus; ID, infectious diseases. Note overlap in data with prophylaxis, pediatrics, and missing.

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TABLE 1

Distribution of patient, antibiotic, infection, prescriber, and reviewer characteristics among antibiotics prescribed with and those prescribed without ID consult

After propensity score matching, the sample size decreased to 3,566, with more equal distribution of baseline characteristics globally demonstrated by the propensity score mean changes (Table 1). The propensity-score models’ c-statistics had a range of 0.6 to 0.67.

Outcome with crude, propensity score matched, and adjusted analyses.Using all data (i.e., not propensity score matched) 92% (9,644/10,508) of prescribed antibiotics were found to be appropriately used. Appropriateness was 94% (7,593/9,644) and 84% (2,051/2,436) for antimicrobials with IDC and without IDC, respectively (P < 0.0001). In unadjusted bivariate analysis, IDC was found to be significantly and positively associated with antimicrobial appropriateness (odds ratio [OR] 3.0; 95% confidence interval [CI], 2.6 to 3.5; P < 0.0001) (Table 2).

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TABLE 2

Unadjusted, propensity score matched, and adjusted propensity score matched association between antibiotic appropriateness and infectious diseases consult, along with significant confounders

In the propensity score matched sample, IDC remained positively associated with antimicrobial appropriateness with an OR of 2.5 (95% CI, 2.1 to 3.0), with overall appropriateness of 89% (3,171/3,566), 93% (1,658/1,783) with IDC, and 85% (1,512/1,783) without IDC (P < 0.0001). After adjustment for the remaining confounders, the magnitude of the IDC association with antimicrobial appropriateness changed very little, with an OR of 2.4 (95% CI, 1.9 to 3.0) (Table 2).

Stratification by primary service.Stratification by primary service was carried out and is summarized in Table 3. Surgical specialties overall had higher ORs for antimicrobial appropriateness than the medical specialties; after propensity score matching, the surgical and medical specialties had an OR of 2.9 (95% CI, 2.1 to 3.8) and 1.6 (95% CI, 1.1 to 2.2), respectively, with vascular and transplant surgery demonstrating the highest ORs.

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TABLE 3

Unadjusted and propensity score matched association of infectious diseases consult with appropriateness stratified by primary service

Antimicrobial appropriateness subanalysis.Among the appropriate antimicrobial reviews (9,644) in the unmatched sample, 9.1% (879) were “discordant but justified.” Discordant but justified reviews occurred more frequently with IDC versus no-IDC groups (9% versus 5%; P < 0.0001). The reason for justification was most often due to allergy (53%) in the no-IDC group. In the IDC group, antimicrobial failure (29%), culture (29%), and toxicity (16%) were the most frequent reasons for justification.

DISCUSSION

IDC was associated with more appropriate usage of antibiotics in a hospital with AS oversight. The odds of appropriate usage after IDC ranged from 2.4 (propensity matched, adjusted analyses) to 3.0 (unadjusted analysis using all data). The increase was seen across most services with a trend toward higher OR for the surgical specialties (2.9) versus medical specialties (1.6). It is important to note that IDC improved the appropriate use of antibiotics in an institution where antimicrobials are generally properly prescribed (92% appropriateness) and where most antimicrobials are overseen by IDC (72% IDC penetrance).

IDC and outcomes.Front-line providers are faced with challenges prescribing antibiotics due to resistant organisms, the development of new antimicrobials, and medical and surgical treatments that alter the host immune system and anatomy (8). Infectious disease physicians are consulted for complex infections related to these influences, which may lead to lower mortality and decreased length of stay (6, 7). Although clinical outcomes were not examined, antimicrobial appropriateness, as measured by AS review, may be a determinant of clinical outcomes and an important process measure that can be captured by AS programs (9). We found a significantly higher proportion of appropriate antimicrobial prescription in patients with IDC compared to no IDC, even after propensity matching and accounting for relevant confounders. Based on our evaluation of potential confounders and confounders identified in the literature, such as genitourinary infections, intensive care unit (ICU) location, and weekend prescriptions (10, 11), we included several variables into the propensity score matching, which made for a robust analysis. In addition, while other studies in different settings have demonstrated a similar positive impact of IDC on antimicrobial appropriateness (unadjusted OR range, 2.3 to 4.2; see Supplemental Table S3 at https://www.researchgate.net/publication/341459328) (12–14), our study is unique in demonstrating this benefit globally in the context of an existing AS system.

Despite compelling evidence that IDC improves patient outcomes and antimicrobial prescribing, staffing IDC positions is challenging due to low interest in infectious diseases specialization, which is reflective of the low compensation paid to infectious diseases physicians (15). Our hospital values the infectious diseases specialty and promotes its influence, as demonstrated by the high penetrance of IDC. In the face of resource limitation, prioritization of IDC in select situations that have demonstrated a benefit of IDC involvement, such as Staphylococcus aureus bacteremia (13, 14, 16), resistant Enterobacteriaceae infections (17), Pseudomonas bacteremia and candidemia (16), septic shock (18) and high-level antimicrobial prescription (19), may be a suitable approach for some hospitals. Although infectious disease expertise in the form of remote AS prospective audit and feedback (PAF) alone has clear benefits (1–4), our study suggests that IDC improves the use of antimicrobials overall due to expertise brought to the bedside. This is congruent with a study looking at outcomes of S. aureus bacteremia, which demonstrated an augmented benefit when IDC was at the bedside versus by telephone (20). This difference might be due to (i) improved information ascertainment (i.e., more specific data gathering from physical exam and outside hospital data), or (ii) integration of IDC into the care team and influencing decisions more readily.

Our study demonstrated that IDC had the greatest impact on antimicrobial appropriateness in the surgical specialties, though both medical and surgical specialties exhibited benefit. Vascular and transplant surgery had the highest ORs after propensity matching; however, the effect was not measured with great precision exemplified by the estimates’ wide confidence interval. Nonetheless, these data suggest that there may be a greater benefit of IDC in surgical specialties and that it deserves further investigation. Qualitative data suggest that surgical specialties have an individualistic approach to antibiotic prescribing that leads to inefficiencies and inappropriate antimicrobial prescribing (21). Integration of IDC into surgical care teams may help disrupt this individualistic approach and improve antimicrobial prescribing.

Antimicrobial appropriateness measurement.Reports of antimicrobial appropriateness range from 20 to 94% in acute care (Table S3 at https://www.researchgate.net/publication/341459328) (10, 12–14, 22–24). Our hospital’s antimicrobial appropriateness is higher than most studies. This overall high rate of antimicrobial appropriateness likely reflects our hospital’s appropriate culture of antimicrobial prescribing, which may be due to a combination of AS and IDC influence. In our study, the appropriateness measurement relied on real-time assessment by AS team members via a PAF process in contrast to most other studies, which were retrospectively evaluated. In addition, we did not include errors in dose, duration, or route, which may inflate the appropriateness measure. A comparable appropriateness measure based on indication and selection of antimicrobial prescription was found to be 89% in a point prevalence study from 8 pediatric hospitals in Australia (12). However, there are notable differences from our study in population, location, and study design.

Measuring antimicrobial appropriateness is inconsistent, and standardization is needed (11, 25). One study comparing expert opinion to strict guidelines demonstrated significant differences in measuring antimicrobial appropriateness (20% versus 75%) (10). Although guidelines provide a foundation for appropriate antimicrobial prescription, complex cases that are discordant with guidelines but justified on clinical grounds are difficult to adjudicate within an AS PAF framework. We found that antimicrobials that are guideline discordant but justified based on clinical grounds are more common among patients with IDC. Including this subcategory of appropriateness may improve the measure of antimicrobial prescription in the hospital.

Strengths and limitations.This study is the largest single-center study to our knowledge evaluating the impact of IDC on antimicrobial appropriateness in a hospital with AS PAF. Propensity score matching was used to rigorously adjust for differences in patient population with and without IDC. However, there are several limitations. As a cross-sectional study, the temporality of the IDC cannot be determined, and thus, whether the IDC influenced the antimicrobial choice at the time of order is unknown. In addition, only antimicrobials ordered for durations ≥3 days were evaluated, so antimicrobials ordered and reordered or stopped before 3 days were not included in the analysis, which may lead to overestimation of overall appropriateness. Reviewer bias is another limitation, since AS team members were not blinded to IDC, and it is possible that the appropriateness adjudication may have favored IDC, leading to misclassification and overestimating the OR in favor of IDC. In addition, there is an extra discretionary day for review of antimicrobials with IDC, which could also impact appropriateness adjudication in favor of IDC. To adjust for this difference, time until antibiotic review was included in the propensity score. Additionally, there may be unresolved confounding, such as patient severity, that could affect the association. Finally, due to single-center experience with high IDC penetrance, generalizations to other centers should be approached cautiously. Nonetheless, a major strength of this study is a demonstration that the availability of infectious disease providers is a powerful AS tool leading to improved prescriptions of antimicrobials.

Conclusion.We demonstrated a positive impact of IDC on antimicrobial appropriateness in a large academic medical center. Our results suggest that infectious disease expertise is needed at the bedside and can be synergistic with AS efforts. Further work is needed to evaluate the impact of IDC in conjunction with AS PAF on clinical outcomes.

MATERIALS AND METHODS

Study design and setting.We conducted a cross-sectional study using data collected as part of the AS program at the University of Maryland Medical Center (UMMC). UMMC is a 750-bed tertiary care center in downtown Baltimore City with active solid organ and hematologic stem cell transplant and oncology programs and eight specialized intensive care units (ICUs). There are 32 infectious diseases physicians that practice within six inpatient adult infectious diseases (ID) consult services (general, ICU, transplant, surgical, oncology, and trauma), as well as a primary ID service. Monthly subspecialty service meetings are held to standardize practice. At UMMC, at any time, there are approximately 500 active antimicrobial orders daily. Per hospital policy, an IDC is required within 24 h of ordering a restricted antimicrobial. Antimicrobials included in the restricted category were based on breadth of spectrum, cost, and toxicity potential of the drug. Mandatory IDC upon starting antimicrobial therapy (except prophylaxis) is required for patients in the oncology ward, medical ICU, and trauma services, regardless of antimicrobial restriction classification. The above policies were in place during the entire study period.

A panel of infectious diseases specialists developed UMMC antimicrobial guidelines based on institutional adaptations (formulary, antibiogram, patient population, etc.) of locally published best-practice guidelines. UMMC antimicrobial guidelines were published originally in 2015 and updated annually or more frequently as needed. The guidelines are posted on the hospital intranet site and are available for download on smartphones. In addition, providers have access to the online Sanford Guide to Antimicrobial Therapy (26).

The UMMC AS program consists of 2 infectious diseases physicians (combined equivalent of 0.3 full-time) and 3 infectious diseases pharmacists (combined equivalent of 1.5 full-time). A prospective audit and feedback (PAF) process was introduced in July 2017 and is the mainstay of the program. PAF is carried out with the goal of reviewing all active antimicrobial orders within 3 to 5 days of starting therapy for patients without IDC and 4 to 6 days for patients with IDC. An AS PAF at 3 days was chosen to replicate the CDC-endorsed “antibiotic timeout” as microbiological and clinical information is available that can be intervened at https://www.cdc.gov/antibiotic-use/core-elements/hospital.html. An additional discretionary day for AS review was given to IDC in order to ensure that IDC communication and documentation were carried out. A list of new antimicrobial orders is obtained daily from the electronic medical record EPIC (Verona, WI). Each new selected prescription is evaluated for its appropriateness against UMMC antimicrobial guidelines by an AS team member who communicates as needed with the provider. The appropriateness of each new antimicrobial, indication, and interventions, and whether recommendations were accepted, are documented in the electronic medical record.

Study period, population, and data collection.The current analysis used data collected for the AS PAF activity from October 2017 to March 2019. The first 3 months of the AS PAF activity (i.e., when the antimicrobial review process was first piloted) were excluded from the current analysis. Antimicrobials eligible for inclusion into the study included all unique prescriptions (i) for adults age 18 years and older admitted to the hospital, and (ii) that were active for ≥3 days duration. Antimicrobials were excluded if they (i) had any missing data (e.g., indication), (ii) were delivered by nonenteral or nonintravenous route (e.g., topical), or (iii) were for prophylaxis.

Study measures, outcomes, and analysis.IDC was defined by the presence of an IDC order or an IDC progress note at the time of PAF review. IDC may have been ordered at any point from admission to the time of AS review. IDC is ordered by the primary service or is automatically ordered with a restricted antimicrobial and in designated required locations (oncology ward, medical ICU, and trauma).

Our primary outcome measure was antimicrobial appropriateness, which was operationalized as a binary variable (yes, no). Antimicrobial therapy was considered appropriate if (i) there was an indication for antimicrobial therapy (i.e., antimicrobial therapy was necessary, as determined by the AS reviewer), and (ii) the correct antimicrobial was used based on UMMC antimicrobial guidelines. However, therapy was also deemed to be appropriate if antimicrobial prescription was discordant with guidelines but justified by expert AS review (e.g., meropenem in a patient with sepsis and a history of an extended-spectrum, beta lactamase-producing, Gram-negative). Guideline-discordant antimicrobial prescriptions that were unjustified by expert AS review were considered inappropriate.

Other variables that could influence antimicrobial prescribing were collected and classified in the following five categories: (i) patient related (sex, age, multidrug-resistant organism [MDRO] colonization, location), (ii) antibiotic related (type, route of administration), (iii) infection related (indication, culture positivity), (iv) prescriber related (primary service), and (v) reviewer related (days till antibiotic review) (see Supplemental Table S1 at https://www.researchgate.net/publication/341459328 for full descriptions).

Statistical analysis.Data analysis was performed using SAS v9.4 (SAS Institute; Cary, NC). We quantified the unadjusted association of IDC and antibiotic appropriateness using logistic regression. Our adjusted multivariable model of the association between IDC and antibiotic appropriateness included variables, which, in bivariate analyses, were related both to our outcome (appropriateness) and exposure (IDC). The bivariate analyses were conducted using Pearson’s χ2 statistic or Fisher’s exact test for categorical variables and Mann-Whitney U test or Student's t test for continuous variables, as appropriate.

All variables were evaluated for potential confounding. In addition, stratification by primary service was carried out to further assess the impact of the association of IDC and antimicrobial appropriateness in different settings in the hospital. Medical and surgical specialties were analyzed in additional to subspecialties (e.g., vascular, cardiology).

To decrease the probability of confounding by indication in our nonrandomized study, all of our analyses, those in the entire population and the stratified analyses, were conducted using data in which prescriptions written with IDC consult present versus those that were written without IDC consult present were 1:1 propensity score matched. Separate matching was carried out for the overall sample and within each primary service stratum. Variables included in the propensity score were those variables found in the bivariate analysis to be significantly related to receiving IDC (with P ≤ 0.05) or deemed to be clinically relevant. The nonstratified data included the following covariates in the propensity score model: restricted antimicrobial, culture positivity, intravenous route, MDRO, days until antimicrobial start, days until antimicrobial review, community-acquired pneumonia, genitourinary infection, endocarditis, osteomyelitis, oncology ward, and surgical specialty. We present crude unadjusted analyses run using all study data, results run using the propensity score matched data that have no further adjustment, and results run using the propensity score matched data adjusted for variables that remained imbalanced in the propensity score matched data, which included oncology ward, culture positivity, community-acquired pneumonia, and surgical specialties. Stratified analyses included variables in a propensity matched score that were found in the bivariate analysis to be significant (with P ≤ 0.05) with respect to surgical and medical specialty stratum (see Table S2 at https://www.researchgate.net/publication/341459328), and there was no additional adjustment.

Antimicrobial appropriateness subanalysis.Due to a possible overestimation of antimicrobial inappropriateness with strict guideline concordance, the proportion of antimicrobial reviews that were guideline discordant but justified on clinical grounds was investigated. All antimicrobials that were appropriate were further categorized as either “guideline concordant” or “guideline discordant but justified” at the time of AS review. Reasons for justification of appropriateness (i.e., allergy, antibiotic failure), despite discordance with guidelines, were documented. The proportion of “guideline discordant but justified” antimicrobial prescriptions among all appropriate antimicrobials was compared among the IDC and no-IDC groups.

ACKNOWLEDGMENTS

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

J.S.’s work on this project was supported by the Baltimore VA Medical Center Geriatric Research, Education, and Clinical Center and NIA P30AG028747.

We have no reported conflicts of interest to declare. We have all submitted the International Committee of Medical Journal Editors (ICMJE) Form for Disclosure of Potential Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed.

We give special thanks to all the infectious diseases attendings and fellows at the UMMC, as well as the current and past division chiefs, Shyamasundaran Kotteilil and Robert Redfield, respectively, and the current clinical infectious diseases chief Anthony Amoroso.

FOOTNOTES

    • Received 20 February 2020.
    • Returned for modification 4 April 2020.
    • Accepted 2 May 2020.
    • Accepted manuscript posted online 18 May 2020.
  • Copyright © 2020 American Society for Microbiology.

All Rights Reserved.

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A Propensity Score Matched Study of the Positive Impact of Infectious Diseases Consultation on Antimicrobial Appropriateness in Hospitalized Patients with Antimicrobial Stewardship Oversight
Jacqueline T. Bork, Kimberly C. Claeys, Emily L. Heil, Mary Banoub, Surbhi Leekha, John D. Sorkin, Michael Kleinberg
Antimicrobial Agents and Chemotherapy Jul 2020, 64 (8) e00307-20; DOI: 10.1128/AAC.00307-20

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A Propensity Score Matched Study of the Positive Impact of Infectious Diseases Consultation on Antimicrobial Appropriateness in Hospitalized Patients with Antimicrobial Stewardship Oversight
Jacqueline T. Bork, Kimberly C. Claeys, Emily L. Heil, Mary Banoub, Surbhi Leekha, John D. Sorkin, Michael Kleinberg
Antimicrobial Agents and Chemotherapy Jul 2020, 64 (8) e00307-20; DOI: 10.1128/AAC.00307-20
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KEYWORDS

antibiotic appropriateness
antimicrobial stewardship
infectious disease

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