Abstract
Background
Antimicrobial stewardship programs (ASPs) promote optimal antimicrobial use to prevent resistance, improve outcomes, and reduce costs. We explored how pediatric ASPs enact prospective audit and feedback (PAF) and preauthorization and characterized programs’ perceptions of how these choices affected attainment of stewardship goals.
Methods
We conducted focus groups with US pediatric ASP practitioners, organized by predominant strategy: PAF, preauthorization, or a hybrid. We asked open-ended questions about organization, staffing, and operation of these strategies, as well as rationales for and perceived advantages and disadvantages of these choices. We used applied thematic analysis to analyze transcripts, organizing coded text into themes and categories. We formulated a conceptual model for how the design and performance of PAF and preauthorization affect stewardship goals and stewards’ work experiences.
Results
Eighteen physicians and 14 pharmacists from 24 hospitals participated in five focus groups. Stewards described myriad advantages and limitations of PAF and preauthorization that support or detract from stewardship goals. For example, PAF uncovered institutional trends in antibiotic use and fostered relationship building but was time-consuming. Preauthorization efficiently reduced broad-spectrum antimicrobial use, yet offered limited educational opportunities. How these strategies facilitated or impeded appropriate antimicrobial use in turn affected stewards’ professional satisfaction, creating a feedback loop that could reinforced positive or negative outcomes.
Conclusions
ASPs reported differing emphasis on and implementation of PAF and preauthorization. Each strategy entailed contrasting benefits and trade-offs for steward satisfaction and perceived efficacy, suggesting that a hybrid approach could enable ASPs to maximize strengths of each to mitigate drawbacks of the other.
Keywords: antimicrobial stewardship, focus groups, preauthorization, prospective audit and feedback
Focus groups with pediatric antimicrobial stewards demonstrated variable implementation of prospective audit and feedback and preauthorization. We developed a model identifying how key drivers and mediators associated with these strategies affect perceived antimicrobial stewardship program (ASP) efficacy and steward satisfaction.
BACKGROUND
Antimicrobial resistance is a grave public health threat: >2.8 million antibiotic-resistant infections occur in the USA annually, leading to >35 000 deaths [1]. Antimicrobial stewardship programs (ASPs) promote judicious, effective, and safe antimicrobial use, thereby preventing emergence of resistance, improving outcomes, and reducing costs [2–4]. The World Health Organization and United Nations have identified ASPs as crucial to tackle antimicrobial overuse [5–7].
The Centers for Disease Control and Prevention (CDC) provide guidelines on core elements of ASPs [1]. Prospective audit and feedback (PAF), in which stewards review prescribed antimicrobials and offer recommendations, and preauthorization, which requires approval to use certain antimicrobials, are two priority evidenced-based interventions identified as most effective [1]. Both approaches are recommended by the Pediatric Infectious Diseases Society, Infectious Diseases Society of America (IDSA), and Society for Healthcare Epidemiology of America (SHEA) [8, 9]. Evaluating and comparing benefits and limitations of these strategies is paramount to practicing effective stewardship.
The CDC acknowledges that “There is no single template for a program to optimize antibiotic prescribing…” [1]. Evidence comparing the merits of PAF versus preauthorization is scant, and minimal qualitative data describe stewards’ perceptions of facilitators and barriers to implementation and efficacy. We explored choices pediatric ASPs make in enacting PAF and preauthorization and characterized perceived implications of these choices in achieving stewardship goals.
METHODS
Participants
US pediatric stewards were recruited to participate in 1-h focus groups via videoconferencing. Participants were invited from dedicated pediatric ASPs at hospitals that participated in the Pediatric Health Information System® database and Sharing Antimicrobial Reports for Pediatric Stewardship collaborative [10, 11]. Multiple participants per institution were permitted. We included both pharmacists and physicians in each focus group, anticipating that each would have unique perspectives, leading to richer discussion.
We grouped participants by whether their programs emphasized PAF, preauthorization or a hybrid, based on self-report, because we thought this might facilitate interaction and insights that would not otherwise emerge. Most programs (22/24) self-identified as either predominantly focused on PAF or a hybrid. Only 2 programs self-designated as predominantly using preauthorization. We asked hybrid participants to report their approximate number of restricted antimicrobials, leaving the definition of “restricted” to interpretation. Among hybrid participants, the number of restricted antimicrobials clustered between 8 and 23, with the majority of participants (11) restricting 14–18 (Supplementary material). No participants restricted 24–28 drugs, and only 4 restricted ≥29. We therefore used ≥29 restricted antimicrobials as the cut-off for inclusion in the preauthorization group.
The Boston Children’s Hospital Institutional Review Board found the study exempt from federal human subjects regulations.
Focus Groups
We asked open-ended questions about programs’ organization, staffing, and operation, as well as rationales for and perceived advantages and disadvantages of their choices (Supplementary material). The principal investigator (CSM) was the facilitator, while a co-investigator (NM) served as an independent observer (audio muted and camera off). Sessions were recorded and professionally transcribed, with roles and identities anonymized to “interviewer” and “interviewee” to protect privacy and confidentiality.
Analysis
CSM and NM reviewed all transcripts, using applied thematic analysis to identify key concepts and develop initial codes. Deductive codes explored ASP characteristics and perceived advantages and disadvantages of PAF, preauthorization, and hybrid approaches. Codes and their definitions were iteratively refined and assembled with illustrative quotations into a codebook using NVivo version 1.6.2. Deductive and inductive coding processes identified and elaborated on the structure and practices of ASPs while exploring unanticipated and emergent concepts. CSM and NM coded transcripts in parallel and adjudicated discrepancies in discussion. Through immersion/crystallization, a process in which researchers iteratively (1) immerse themselves in collected data and (2) suspend analysis to articulate patterns or themes, recurrent themes were identified in coded text and organized into categories; from these, a conceptual model for how the design and performance of PAF and preauthorization affect attainment of stewardship goals and steward experiences was formulated [12]. CSM and NM held triangulation sessions in which they compared and confirmed their multiple observations and conclusions, and iteratively refined the conceptual model in discussion with JIC and MMN [13, 14]. We used the Consolidated Criteria for Reporting Qualitative Research (COREQ) to report analyses and findings [15].
RESULTS
Participants comprised 32 stewards (18 physicians and 14 pharmacists) from 24 hospitals, divided into 5 focus groups, mixing physicians and pharmacists (Table 1).
Table 1.
Size and Composition of Focus Groups
| Predominant Strategy Type | ||
|---|---|---|
| Prospective Audit and Feedback | Hybrid | Preauthorization |
| Group 1 | Group 3 | Group 5 |
| 3 Pharmacists | 4 Pharmacists | 2 Pharmacists |
| 4 Physicians | 2 Physicians | 4 Physicians |
| Group 2 | Group 4 | |
| 2 Pharmacists | 3 Pharmacists | |
| 4 Physicians | 4 Physicians | |
Stewards described differing emphasis on PAF or preauthorization and a variety of implementation approaches. They noted advantages and opportunity costs for each strategy, perceiving that aspects of each served as facilitators (positive mediators) of achieving appropriate antibiotic use, while other aspects acted as barriers (negative mediators).
Participants described how PAF and preauthorization enhanced or detracted from stewardship aims, which in turn affected their experiences and satisfaction as stewards (Figure 1). This interplay between achieving improved antimicrobial use and experiencing a sense of success and self-efficacy could create a feedback loop that reinforced positive or negative outcomes, that is, a virtuous or vicious cycle. Influencing prescriber actions motivated stewards and reinforced their belief in the value of their interventions, while lack of change engendered feelings of futility and created tension in interactions with prescribers, sometimes leading stewards to reduce engagement in a strategy.
Figure 1.
Conceptual model of stewards’ perceptions of how the core stewardship strategies of prospective audit and feedback and preauthorization result in factors that promote (positive mediators) or impede (negative mediators) the key outcomes of appropriate antimicrobial use and steward satisfaction (center of figure). Positive mediators are shown on left side of figure, while negative mediators are shown on right side of figure. Each core strategy leads to positive or negative mediators of appropriate antimicrobial use or steward satisfaction via a variety of specific mechanisms (drivers). EMR, electronic medical record; FTE, full-time equivalent; ID, Infectious Diseases.
Positive Mediators of Appropriate Antimicrobial Use
The themes of persuasion, efficiency, and pharmacy support positively mediated appropriate antimicrobial use.
Persuasion
Using PAF, stewards encouraged appropriate antibiotic choices through practice pattern recognition, guideline creation, and changing prescriber culture. PAF respondents highlighted the ability to identify trends in antimicrobial use. Expanding from a solely patient-level to systematic view of stewardship inspired systems-level interventions, illustrating the reciprocal reinforcement between effective strategies and motivated stewards. A participant said, “in addition to building . . . collaborative relationships . . . it’s allowing us to do better stewardship by mak[ing] stewardship a higher-level idea and not just patient by patient.”
PAF pinpointed domains to emphasize in development of practice guidelines. Moreover, participants noted that discussing susceptibility results in the context of guidelines helped to promote antimicrobial de-escalation.
Finally, stewards noted that PAF fostered beneficial hospital culture change, stimulating independent stewardship by prescribers, and affirmed stewards’ experiences of professional success. One participant characterized clinicians’ views on stewardship: “Somebody is watching . . . , but I know what to do anyway . . . I’ll just make the change.”
Efficiency
The efficiency of preauthorization positively mediated appropriate antimicrobial use. Preauthorization was easy to set up, provided antibiotic protection, and leveraged the electronic medical record (EMR). Participants regarded preauthorization as a “low-hanging-fruit” approach that targeted often-used antibiotics without excessive time investment.
Restricting antibiotics and creating pre-approved indications was perceived as straightforward and successful in reducing utilization. One steward hypothesized that the “extra checkpoint” of preauthorization had kept meropenem use “really low through the years.”
Another noted that carbapenem preauthorization was “initially a big deal” but had decreased from 12 to 2 calls per week.
Finally, use of the EMR streamlined processes, including communication among pharmacists, prescribers, and Infectious Diseases (ID) clinicians. A steward described a workflow in which restricted antimicrobial orders were forwarded to ID fellows for review and addition of the approved duration.
Pharmacy Support
Independent of their dominant stewardship strategies, participants characterized pharmacy support as a vital positive mediator of appropriate antimicrobial use. Participants described collaboration with unit-based pharmacists, referred to by some as “stewardship extenders,” who identified high-risk patients and provided antibiotic recommendations.
Negative Mediators of Appropriate Antimicrobial Use
Negative mediators associated with PAF were opportunity cost and lack of resources, while those arising from preauthorization were unintended downstream consequences and limited interaction with providers.
Opportunity Cost
Stewards perceived PAF as imposing an opportunity cost because it was time consuming, limiting pursuit of other interventions. One reported reducing PAF to 2 days per week, affording “a good 6–9 hours extra in the week to work on guidelines, projects, writing manuscripts,…. ”
Lack of Resources
Lack of resources for PAF—both insufficient staffing and a desire for more pharmacy full-time equivalents (FTE)—negatively mediated appropriate antibiotic use. Respondents reported competing responsibilities that impeded stewardship goals, limiting engagement in PAF and professional satisfaction. Understaffing precluded performing PAF broadly or consistently. One participant explained, “We don’t have the bandwidth to do every antibiotic hospital-wide.”
Unintended Downstream Consequences
A negative mediator associated with preauthorization was unintended downstream consequences. Misuse of pre-approved indications or durations led to inappropriate antimicrobial use, frustration, and impaired trust. One participant observed, “[P]eople will call anything sepsis . . . .” Preauthorization also led to increased use of unrestricted antimicrobials. For example, one participant reported that for “commonly used unrestricted drugs like cefepime, we’re 200% of our peers . . . .”
Limited Interaction with Providers
Preauthorization negatively mediated appropriate antibiotic use via limited interaction with providers. Main drivers of this theme were an inability to discuss duration, decreased opportunity for education, and need to make decisions with limited information. One steward noted, “Things change over time with the patient, and with prior authorization alone you can’t . . . address duration of antibiotics."
Another participant described the lack of educational opportunities and resulting perceived limited impact: “We don’t have a sense of the patient’s clinical trajectory. There’s only so much we can really say upfront like, ‘MRSA coverage, yes, no. Pseudomonas coverage, yes, no.’ . . . discussions are more educational and informative after we have . . . data.”
Making decisions with limited information led to a tendency to approve antimicrobials requested off-hours: “It’s hard for an ID physician . . . getting a call overnight to say, no, don’t use meropenem, when they don’t have data. So, things were often getting approved and it was really hard to discontinue . . . .” Stewards conveyed that such limited interaction and information restricted opportunities to optimize antimicrobial management, diminishing professional satisfaction.
Positive Mediators of Steward Satisfaction
Participants described how optimizing antimicrobial use influenced self-efficacy, and spoke about day-to-day experiences of PAF and preauthorization and resulting enthusiasm for stewardship work. Positive mediators of steward satisfaction were relationship building, engagement in education, and achieving a decreased burden of off-hours work.
Relationship Building
Relationship building was reported to be vital to PAF and a critical mediator of steward satisfaction. Interviewees noted that PAF was often bidirectional and promoted conversation. The drivers of relationship building were collegiality, decreasing barriers to ask questions, respecting physician autonomy, and opportunities for collaboration. One participant explained that “[PAF] is all about . . . knowing how they think and them knowing how we think and coming to trust us.” Another participant emphasized that a strength of PAF was “definitely relationship building . . . . Once they feel comfortable with you, then they . . . [ask] questions that you might not have asked yourself.”
Regarding physician autonomy and collaboration, a steward observed that PAF “allows more autonomy and letting providers understand they still have the choice to do whatever they feel is best and we’re there to partner and offer support.”
Education
Participants agreed that PAF allowed for more fluid educational opportunities than preauthorization, including teaching trainees to champion best practices. PAF reinforced the “culture of good behavior” and promoted future autonomous decision-making among prescribers, reinforcing stewards’ belief in the positive impact of their interventions and encouraging ongoing engagement with prescribers. A participant stated, “Not only are we giving advice on a specific patient, . . . but we’re also educating and hopefully changing future practices, . . . which is not accomplished by preauthorization.”
Decreased Burden of Off-Hours Work
Steward satisfaction in preauthorization was mediated by a decreased burden of off-hours work driven by overnight approval exception, pre-approved indications, and off-hours coverage by the ID service, leading to greater sustainability of stewardship efforts. One steward remarked, “We don’t want to be doing this 24 hours a day . . . so after 4:30 PM, they are allowed to enter a temporary approval code.…”
Negative Mediators of Steward Satisfaction
Negative mediators of steward satisfaction were lack of change with PAF, tension with providers with preauthorization, and burnout arising from both strategies.
Lack of Change
Dissatisfaction with PAF resulted from perceptions that recommendations were ignored, educational impact was short term, and “educating the hierarchy” was difficult. One participant described feeling like a “broken record talking to people and being like, you know you’re not supposed to do this.” Stewards relayed concern that teaching about the current case sometimes failed to achieve sustained practice changes. Moreover, because PAF usually involved front-line clinicians, influencing final decision-makers (ie, attending physicians) at the top of the hierarchy was challenging.
Tension with Providers
Tension with providers due to preauthorization, leading to a perception of ASPs as the “antibiotic police,” negatively mediated steward satisfaction, causing reluctance to engage with prescribers. One participant stated, “Certain services . . . are more resistant to stewardship than others, and saying . . . no . . . sometimes causes . . . friction or tension, which we don’t want . . . , we don’t want to be the antibiotic police.”
Burnout
Burnout associated with either PAF or preauthorization negatively mediated steward satisfaction. ASPs performing PAF expressed that a feeling of futility contributed to burnout. One participant stated that “if you have a consistent practice . . . that you can’t modify with [PAF], but . . . keep reviewing it over and over again, that is very frustrating.” Regarding preauthorization, stewards reported that overnight approvals affected quality of life, contributing to burnout.
DISCUSSION
In this study, we determined that PAF and preauthorization offer advantages and disadvantages that affect programs’ perceived efficacy and professional satisfaction. Our study was novel in exploring details of PAF and preauthorization implementation and resulting perceived benefits and drawbacks. Moreover, no prior literature has evaluated the interplay of steward satisfaction and traditional ASP outcomes. Our findings may be generalizable to all ASPs, given that participants’ observations and our conclusions were not pediatric-specific.
The IDSA/SHEA guidelines for ASP implementation recommend both preauthorization and PAF but state that ASPs should choose one or both strategies based on facility-specific resources [8]. Few studies have compared the two strategies. In a quasi-experimental trial comparing adult medical teams experiencing PAF vs preauthorization, Tamma et al[16] found no difference in clinical outcomes, including hospital stay and mortality, but showed lower antibiotic use and durations with PAF. They concluded that both approaches were useful and favored incorporating a combination [16, 17]. In a multicenter, historically controlled, prospective crossover-design trial in 4 community hospitals, PAF and “modified” preauthorization (first antibiotic dose given before ASP review) were determined to be feasible, but only PAF was associated with decreased antibiotic use [18]. While investigations to date have included valuable analyses of each strategy’s impact on stewardship goals, our study contributed new insights regarding the myriad approaches to enacting PAF and preauthorization, nuances of how and why each strategy leads (or fails to lead) to desired outcomes, and implications of combining them.
Our findings suggest that a combination of the two strategies could maximize positive mediators of appropriate antimicrobial use and steward satisfaction while minimizing negative mediators. For example, a program could harness the efficiency of preauthorization for protecting broad-spectrum antimicrobials, offsetting opportunity costs associated with PAF—thus leaving time for programmatic/systems-level interventions. PAF could reduce downstream consequences of preauthorization through auditing pre-approved indications and unrestricted antimicrobials. PAF could lessen tension with providers associated with preauthorization by facilitating relationship building and education—which could improve stewards’ professional satisfaction.
Positive mediators of appropriate antimicrobial use could create a virtuous cycle between improved ASP outcomes and steward satisfaction. Novel mediators of ASP impact emerged that affected both professional satisfaction and reduced antimicrobial use, including factors such as educational impact and collegiality. The importance of steward satisfaction as both an outcome and determinant of achieving stewardship goals, while unexpected, is unsurprising given that ASPs rely on social interactions among stewards and prescribers [19]. Participants’ statements revealed that as stewards attempted to influence behavior change, belief in their likelihood of success contributed to their motivation and reinforced their perceived efficacy.
With growing awareness of burnout in medicine, addressing steward satisfaction is vital for ASP sustainability [20]. Mitigating mediators of dissatisfaction may improve both stewards’ daily lives and appropriate antimicrobial use. Increased financial support for ASPs would improve both outcomes by addressing insufficient resources, such as understaffing and lack of pharmacy FTE. These changes could reduce burnout by supporting larger ASP teams who could share work and extend the reach of PAF and preauthorization, as well as undertake additional systems-level initiatives.
This study had strengths and limitations. Qualitative research can offer a rich understanding of contextual and human elements that impact ASP practices, but findings are not easily reproduced given their interpretive nature [21]. Inclusion of 32 pharmacists and physicians from 24 geographically distributed pediatric centers allowed for vibrant discussions about differing practices. However, our sample reflected only academic pediatric hospitals, whose experiences may differ from other hospitals. The study did not incorporate perspectives of clinicians who received stewardship interventions and thus could neither directly assess clinicians’ acceptance of interventions nor corroborate stewards’ perceptions of clinicians’ motivations and actions. To facilitate rich discussions, we organized focus groups by whether participants’ programs emphasized PAF, preauthorization, or a hybrid. However, consistent, objective definitions for these categories have not been established, antimicrobials defined as “restricted” may vary based on institutional factors, and we relied on self-report of predominant strategy and number of restricted antimicrobials. Nevertheless, preauthorization was discussed in the hybrid and preauthorization groups, regardless of the number of agents restricted, and PAF was likewise discussed in the hybrid and PAF groups. Furthermore, focus group assignments did not ultimately shape the qualitative analysis as coding was performed across all 5 focus groups and was strategy-specific rather than by focus group. Finally, while videoconferencing facilitated ease of participation, non-verbal cues and their inspired conversation might have been reduced compared with in-person meetings.
CONCLUSION
Focus groups with pediatric stewards demonstrated variability in emphasis on and implementation of PAF and preauthorization, with perceived advantages and trade-offs. We developed a model that identifies how key drivers and mediators associated with PAF and preauthorization contribute to a virtuous or vicious cycle of perceived ASP efficacy and steward satisfaction. A hybrid approach could enable ASPs to maximize strengths of each strategy. Future analyses could examine objective components of ASPs, such as pharmacist/physician FTE and FTE-to-bed ratios, and their association with steward satisfaction. Our findings have the potential to empower ASPs to make organizational decisions that optimize both antimicrobial use and stewards’ satisfaction and, in turn, influence recommendations and standards for ASPs.
Supplementary Material
Acknowledgments
Financial support . This work was supported by the National Institutes of Health [grant 1T32AI155391-01A1 grant to C.S.M and N.M].
Potential conflicts of interest . None of the authors of this manuscript have any conflicts of interest to disclose.
Financial disclaimer . The other authors have indicated they have no financial relationships relevant to this article to disclose.
Contributor Information
Christina S Manice, Division of Pediatric Infectious Diseases, Boston Children’s Hospital, Boston, Massachusetts, USA; Department of Pediatrics, Harvard Medical School, Boston, Massachusetts, USA.
Nivedita Muralidhar, Division of Pediatric Infectious Diseases, Boston Children’s Hospital, Boston, Massachusetts, USA.
Jeffrey I Campbell, Division of Pediatric Infectious Diseases, Boston Medical Center, Boston, Massachusetts, USA; Department of Pediatrics, Boston University Chobanian & Avedisian School of Medicine, Boston, Massachusetts, USA.
Mari M Nakamura, Division of Pediatric Infectious Diseases, Boston Children’s Hospital, Boston, Massachusetts, USA; Antimicrobial Stewardship Program, Boston Children’s Hospital, Boston, Massachusetts, USA; Department of Pediatrics, Harvard Medical School, Boston, Massachusetts, USA.
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