The Centers for Disease Control and Prevention (CDC) Core Elements of Antibiotic Hospital Antibiotic Stewardship (“Core Elements”) allows healthcare systems to select specific elements from a list of tracking metrics and interventions.Reference Pollack and Srinivasan1 This recommendation leaves room for flexibility in program implementation, but it also allows hospitals to satisfy all Core Elements while still having an ineffective antimicrobial stewardship program (ASP). This concern is greatest for resource-limited rural community hospitals.Reference Stenehjem, Hyun and Septimus2
In this study, we evaluated the implementation of ASPs in Missouri using a survey, and we assessed facilitators and barriers to ASP implementation through semistructured qualitative interviews.
Methods
Survey
A 93-question, online survey based on the CDC Core Elements was developed by our research team of infectious diseases physicians, ASP pharmacists, and dissemination and implementation scientists to assess the characteristics of ASPs in Missouri (Qualtrics, Provo, Utah; see the Supplement online).
We distributed the survey to ASP leadership in all 125 hospitals in Missouri. Only 1 survey was accepted per hospital. Incomplete surveys were excluded from the analysis. Stewardship pharmacists covering >1 hospital were instructed to complete the survey for each hospital supervised. Survey responses were collected from April 9, 2019, to July 31, 2019. No incentives for participation were offered.
Statistical analysis was performed using SAS version 9.4 software (SAS Institute, Cary, North Carolina). Statistical testing was performed with the Fisher exact test and the Mann-Whitney U test. A P value <.05 was considered significant.
Semistructured interviews
An interview guide based on the Core Elements was also developed by our research team to assess facilitators and barriers of implementing ASPs. We recruited ASP pharmacists from smaller, rural, and critical access hospitals to take part in 30–60-minute semistructured interviews. We conducted interviews from April 4, 2019, to July 11, 2019, until we reached thematic saturation.
Interviews were recorded, transcribed, and then coded by 2 independent coders using NVivo version 12 software (QSR International, Melbourne, Australia). The code book and themes were piloted, revised, and approved by the research team.
Results
Survey
In total, 45 completed surveys were received from the 125 eligible Missouri hospitals (response rate, 36%). For survey respondents, hospital size ranged from 12 to 1,378 beds, with a median of 113 (interquartile range [IQR], 55–242). Nonresponding hospitals were smaller, with a median number of 58 beds (IQR, 32–155; P = .04). Of responding hospitals, 16% were critical access hospitals (CAHs) compared to 34% of nonresponding hospitals (P = .04). Also, of responding hospitals, 67% reported fulfilling all 7 Centers for Disease Control and Prevention (CDC) Core Elements (Supplementary Table 1 online). Only 3 of 7 CAHs (43%) had implemented all 7 Core Elements, compared to 27 of 38 non-CAHs (71%; P = .19).
Leadership commitment
All but 1 responding hospital reported a hospital leadership commitment to antimicrobial stewardship. Only 57% reported that leadership ensured that relevant staff were given sufficient time for stewardship activities.
Accountability and drug expertise
Moreover, 59% of responding hospitals reported appointing a single pharmacy leader dedicated for the ASP. Of these programs, 91% reported having no protected time for stewardship activities. Only 29% of the CAHs reported having a dedicated pharmacist leader.
Policies and interventions to improve antibiotic use
All respondents reported performing some type of stewardship intervention (Table 1); however, the number of interventions varied widely, from 2 to 12 (Supplementary Table 2 online).
Comparison of Antimicrobial Stewardship Interventions Implemented at Missouri Hospitals Stratified by Critical Access Hospital Status
a This result was statistically significant, with P = .03.
Tracking and reporting antibiotic use and outcomes
Also, 61% of responding hospitals reported submitting data to the National Healthcare Safety Network (NHSN) Antibiotic Utilization and Resistance (AUR) module, and 29% of hospitals utilized the NHSN standardized antimicrobial administration ratios for antimicrobial tracking.
Education
Hospitals provided stewardship education in a variety of ways; the most popular was facility-specific feedback on antibiotic prescribing trends (Supplementary Table 3 online). Targets of education were commonly physicians, pharmacists, and nurses. However, 16 hospitals involved patients in their educational efforts.
Tracking outcomes
Tracking of antimicrobial-associated outcomes was performed by 93% of responding hospitals, and 1–4 measures were tracked (Supplementary Table 4 online).
Stewardship resources
The most commonly used resources for ASPs were state-based collaboratives and ASP tool kits (Table 2). Of the respondents using state-based collaboratives, 45% found them very or extremely useful, whereas only 23% of those using regional and national collaboratives rated them similarly. The CDC ASP tool kit was used most frequently, and 85% found it very or extremely useful.
Resources Used By Responding Hospitals
Semistructured interviews
We interviewed 8 pharmacists from 8 hospitals. Hospital size ranged from 55 to 496 beds, and 6 hospitals had <150 beds. Overall, 14 codes were used to thematically analyze the interviews (Supplementary Table 5 online). The 5 key themes (Supplementary Table 6 online) are discussed below.
Theme 1: Stewardship is highly collaborative but pharmacy driven. Everyone interviewed noted that their ASPs were led by pharmacists with other disciplines collaborating, often with semiregular team meetings. Pharmacists felt underprepared for ASP responsibilities, and these responsibilities were often uncompensated.
Theme 2: There is need for internal resources and support. Pharmacists typically agreed that insufficient internal resources, including staffing, time, and salary support, were provided to the ASP. This factor hindered the pharmacist’s contribution to the ASP. Pharmacists noting low leadership support also lacked resources to support the ASP.
Theme 3: Resistant physicians hinder program success. Interviewees noted that stewardship activities often strained relationships between ASP pharmacists and practicing physicians, which harmed educational efforts.
Theme 4: Importance of proper tracking tools. The sophistication of tools, their user-friendliness, and staff comfort with them were commonly linked to tracking and reporting. Pharmacists with difficult tools compiled reports on paper or used Excel software (Microsoft, Redmond, WA) for workarounds.
Theme 5: Common desire for networked relationships and platforms. Most pharmacists wanted a way to share resources by connecting to other hospitals and pharmacists. Common requests included sharing educational materials and tools, learning from hospitals of similar sizes, and sharing other stewardship information.
Discussion
The survey and interview results show that despite broad ASP uptake, there was significant variability in ASP implementation. Programs varied in the scope and complexity of their interventional and tracking efforts, as well as in the degree of support and resources afforded to them. Programs that are more involved tend to be more effective. Stenehjem et alReference Stenehjem, Hersh and Buckel3 showed that stewardship programs that promoted daily engagement with the stewardship team achieved a significant reduction in antibiotic usage.Reference Stenehjem, Hersh and Buckel3
Leadership support and dedicated resources remain substantial barriers to effective stewardship in many hospitals. Although most ASPs had documented support statements, minimal dedicated time was allotted to ASP pharmacists. CAHs may be of particular concern because pharmacy ASP leadership was largely not available among CAHs and none compensated pharmacist time for stewardship activities. The new recommended ASP staffing guidance from CMS may help improve resource allocation in the future.4
A major limitation of this study was its low response rate despite aggressive reminders. The large proportion of smaller hospitals and CAHs among nonparticipants highlights the difficulty of disseminating stewardship resources to more rural facilities. Although respondents represented a large geographic and size distribution of hospitals in the state, the data capture for CAHs was inadequate to fully evaluate unique issues in the state’s most resource-limited hospitals. Other limitations included self-reporting bias and possible duplication due to multiple hospitals using the same system ASP resources.
In conclusion, continued barriers to implementing ASPs in community settings are related to inadequate leadership commitment, resource allocation, and the need for improved physician communication.
Supplementary material
To view supplementary material for this article, please visit https://doi.org/10.1017/ice.2020.318
Acknowledgments
We thank the Missouri Department of Health and Senior Services and the Missouri Hospital Association for assisting with contacting stewardship pharmacists. We would also like to thank Donna Jeffe PhD and Maria Perez MA at the Health Behavior, Communication, and Outreach Core at Washington University in St Louis. We also thank Angela Hoelscher PharmD and Michael Geisler PharmD for pilot testing our survey tool. We also thank David Ruppel, BA, for assistance in recruiting hospital ASP pharmacists to complete our survey. The findings and conclusions of this article do not necessarily represent the official views of the CDC. Research reported in this publication was supported by the National Center for Advancing Translational Sciences of the National Institutes of Health under Award Number “KL2R002346”. The content is solely the responsibility of the authors and does not necessarily represent the official view of the National Institutes of Health.
Financial support
This work was supported by the CDC Epidemiology and Laboratory Capacity (ELC) program.
Conflicts of interest
The authors report no relevant conflicts of interest.
