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Kevin Messacar, Kristen Campbell, Kelly Pearce, Laura Pyle, Amanda L. Hurst, Jason Child, Sarah K. Parker, A Handshake From Antimicrobial Stewardship Opens Doors for Infectious Disease Consultations, Clinical Infectious Diseases, Volume 64, Issue 10, 15 May 2017, Pages 1449–1452, https://doi.org/10.1093/cid/cix139
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Abstract
Implementation of a unique in-person pediatric antimicrobial stewardship program was associated with a significant increase in infectious disease consultations at a quaternary care children’s hospital. This study demonstrates that antimicrobial stewardship programs support, and do not compete with, infectious disease programs.
Antimicrobial stewardship programs (ASPs) succeed in improving patient outcomes, reducing antimicrobial adverse events, decreasing antimicrobial resistance, and optimizing resource utilization [1]. In the inpatient setting, most of these hard-fought successes are realized through unsolicited, unbilled interventions with healthcare providers via prior authorization of antimicrobials or prospective audit with feedback mechanisms. Although the successes of antimicrobial stewardship are increasingly recognized, the potential for unintended effects on infectious disease clinical services raises concerns among infectious disease providers. Do antimicrobial stewardship interventions supplant formal infectious disease consultations? Is increasing recognition and compensation for antimicrobial stewardship activities coming at the expense of infectious disease revenues? Is a cursory antimicrobial stewardship audit with antimicrobial recommendations replacing the comprehensive chart review and bedside evaluation by infectious disease providers? In this study, we investigate the impact of a pediatric ASP on infectious disease consultations across a quaternary care children’s hospital.
METHODS
Study Design
This is a pre-post quasi-experimental retrospective cohort study comparing rates of initial infectious disease consultations before and after implementation of an ASP.
Setting and Description of ASP Activities
Children’s Hospital Colorado Anschutz Medical Campus (CHCO) is an academic quaternary care children’s hospital in Aurora, Colorado, operating 444 inpatient beds with >15000 inpatient admissions in 2015. More than 2000 medical staff and 230 medical residents and fellows provide care to patients on the general medical (48 beds), pulmonary and cystic fibrosis (38 beds), hematology/oncology (48 beds), surgical (58 beds), neonatal intensive care (74 beds), pediatric intensive care (32 beds) and cardiac intensive care units (32 beds). Heart, renal, liver, and bone marrow transplantations are performed. The CHCO ASP program consists of 1 pediatric infectious disease trained physician at 0.5 full-time equivalent (FTE) and 2 infectious disease trained pharmacists who share 1.0 FTE for ASP activities; the FTEs increased over the period of the study [2].
The CHCO ASP uses a unique rounding-based strategy, known as “handshake stewardship,” a highly successful, expanded form of prospective audit and feedback [2]. The expanded elements involve daily review of prescribed antimicrobials at 24 and 72 hours, real-time decision support for rapid diagnostic result reporting, and in-person feedback on the inpatient units between the antimicrobial stewards and a member of the attending service [2]. All 16 inpatient teams are contacted daily in person, Monday–Friday, regardless of whether there are ASP interventions.
Definitions
The preimplementation phase refers to the era before the onset of ASP activities, with data collected from October 2010 to September 2011. The postimplementation period included the handshake stewardship ASP activities described above, from October 2013 to the present, with consultation data collected to September 2015. Between these 2 periods, the planning period involved sequential implementation of ASP activities and was not included in the statistical analysis [2].
No formal criteria were in place to recommend or require formal infectious disease consultation. However, ASP interventions that involve more than a cursory chart review or detailed management questions from the primary team typically trigger this recommendation.
Data Collection and Statistical Analysis
The number of initial infectious disease consultations per unit was gathered from the electronic medical record by capturing templated initial infectious disease consultation notes. To account for hospital growth and fluctuations in patient volumes, rates were normalized per 1000 admissions based on administrative hospital census data. Two-sample t tests were used to compare mean infectious disease consultation rates between the pre- and postimplementation periods overall and by inpatient unit. All hypothesis tests were 2-sided with significance set at P < .05. R software (version 3.3.1; R Foundation for Statistical Computing; http://www.R-project.org/) was used for all statistical analysis and data manipulation.
RESULTS
Infectious disease consultations in the preimplementation, planning, and postimplementation phases are depicted by quarter per 1000 admissions from 2010 to 2015 in Figure 1A. Overall, mean monthly infectious disease consultations per 1000 admissions increased from 31.0 (95% confidence interval, 26.1–35.9) in the preimplementation to 42.0 (38.5–45.5) in the postimplementation phase (P < .001). A subanalysis of normalized infectious disease consultation rates in 6 individual units demonstrated that none had significant decreases, and the medical and cardiac units had significant increases.

A, Infectious disease consultations per 1000 admissions before, during, and after implementation of an antimicrobial stewardship program (ASP) at Children’s Hospital Colorado. B, Comparison of mean monthly infectious disease consultations before versus after implementation of an ASP at Children’s Hospital Colorado. Abbreviation: CI, confidence interval.
DISCUSSION
Across a quaternary care children’s hospital, infectious disease consultations increased by 57% (35% when standardized per 1000 admissions) after introduction of an ASP using the handshake stewardship approach. This is in the setting of overall decreasing antimicrobial use to among the lowest levels for a freestanding pediatric hospital [2]. Contrary to concerns of infectious disease providers, ASPs clearly do not decrease consultations and have the potential to increase consultations and revenues and improve outcomes.
Stewardship programs have raised various concerns from infectious disease practitioners and sections. A survey of 502 Infectious Disease Society of America Emerging Infections Network members found that 45% were concerned that infectious disease involvement in antimicrobial stewardship activities would lead to a loss in income owing to decreased requests for consultations [3]. These potential losses of revenue stem from “curbside” consultations provided by ASPs that are not converted to formal billable consultations [4]. In addition to financial concerns, curbside consultations also raise quality of care and medicolegal concerns. They have been demonstrated to lead to inaccurate management recommendations in complex clinical situations, owing to the incomplete, inaccurate details communicated by informal consultations [5, 6].
Contrary to these concerns, the current study demonstrated an increase in infectious disease consultations with implementation of an ASP. The findings in this pediatric study are consistent with those of the only other published study of ASP effects on infectious disease consultations, conducted at the Providence Veterans Affairs Medical Center, which showed a 72.2% increase per 1000 patient days and consultations that occurred a mean of 3.5 days sooner [7]. Although these studies were not designed to calculate financial impact, there is no doubt that the increased volume of billed consultations has generated increased revenue for infectious disease sections. At CHCO, this large increase required the addition of a second inpatient infectious disease consultation team to manage the volume of consultations.
Although the scope of this study did not include clinical outcomes, the literature supports that increasing infectious disease consultations should improve patient care, in addition to increasing revenue. Medicare claims data demonstrated decreased mortality and readmissions with formal infectious disease consultations for 11 serious infections (bacteremia, Clostridium difficile colitis, central catheter–associated bloodstream infections, endocarditis, complications of human immunodeficiency virus infection, meningitis, osteomyelitis, prosthetic joint infection, septic arthritis, septic shock, and vascular device infection) compared to cases with no consultation [8]. Multiple studies of infectious disease consultations for Staphylococcus aureus bacteremia demonstrate survival benefit and improved use of guideline-recommended strategies, compared with patients with no consultation [9].
In addition, formal bedside infectious disease consultation was superior to informal infectious disease telephone consultation with regard to mortality rates [10]. Infectious disease consultation before discharge on outpatient intravenous antimicrobials led to change in antimicrobial regimen in 89% of cases, with 39% able to transition to oral antimicrobials before discharge [11]. In transplant recipients admitted for infection, infectious disease consultation has been associated with improved survival and decreased rehospitalization rates [12]. In contrast to curbside consultation, formal infectious disease consultation with comprehensive chart review and bedside evaluation leads to improved outcomes.
Both direct and indirect mechanisms of ASPs likely lead to increased infectious disease consultations. When providers seek “curbside” infectious disease advice with detailed management questions for ASP, the best practice is to decline further input and recommend formal infectious disease consultation. This direct ASP intervention contributes significantly to appropriate infectious disease consultations, but does not entirely account for the large overall increase in consultation rates we observed. From October 2014 to April 2016, the CHCO ASP made 188 interventions to recommend infectious disease consultation, of which 165 (88%) were accepted. Therefore, ASP-recommended consultations would only account for just over half of the additional infectious diseases consultations per month observed after ASP implementation.
We hypothesize that another important driver is the indirect effect of improved relations with stakeholder departments developed during ASP implementation processes, as well as the in-person approach of handshake stewardship. Daily in-person rounds lead to visibility and familiarity among the inpatient medical teams, breaking down barriers to units that may previously have had little interaction with infectious disease providers. The handshake stewardship approach provides a unique opportunity for a bidirectional exchange of information and education, often resulting in consultation.
This study has inherent limitations. A single-center study conducted at an academic children’s hospital using an in-person ASP rounding strategy may not be generalizable to other settings or ASP programs. The pre-post retrospective design of this study does not allow differentiation of intervention-related impact on outcomes from unmeasured confounders.
Increased opportunities for interaction through handshake stewardship has transformed perceptions of infectious disease providers in our academic center and opened previously closed doors to infectious disease consultations. The aforementioned concerns on the part of infectious diseases practitioners should turn to enthusiasm. Going forward, ASPs should be supported and encouraged by the infectious disease community as a partner, not competitor, in improving antimicrobial use and the care of patients with suspected infections.
Note
Potential conflicts of interest. All authors: No reported conflicts. All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed.
References
Author notes
Correspondence: S. K. Parker, B055, Children’s Hospital Colorado, 13123 E 16th Ave, Aurora, CO 80045 ([email protected]).