Purpose The impact of an interprofessional mentoring program to advance antimicrobial stewardship programs (ASPs) in selected U.S. hospitals and lessons learned are described.
Summary A seven-step mentoring process with self-assessment, telephone calls, continuing education, a one-day onsite visit, action plan, and outcome data collection and analysis was provided to ASP teams at nine hospitals. Six hospitals completed the program. A significant improvement in the timeliness and appropriateness of i.v. antibiotic therapy (defined as a hang time within one hour after prescriber order entry and broad-spectrum coverage for gram-negative pathogens administered first when combination therapy was used) was observed in patients with sepsis over the 12-month period after implementation of the mentoring program. As a result of requiring hospital administration’s participation in the mentoring program, increased funding became available at three hospitals for the microbiology laboratory to provide new rapid diagnostic tests and for pharmacist and physician time to devote to ASP activities. The collaboration and engagement of ASP team members, inclusion of hospital administrators and pharmacy directors in the onsite mentoring visits, and an experienced mentor team with an infectious diseases (ID) physician and ID pharmacist contributed to ASP success. Challenges included insufficient time to collect outcome metrics due to competing hospital priorities and loss of momentum over time.
Conclusion A mentoring program for antimicrobial stewardship provided the perspective that comes from experience. Engagement of hospital administration was a key factor for both developing and sustaining a stewardship program.
The Centers for Disease Control and Prevention (CDC) has estimated that antibiotic-resistant bacteria cause 2 million illnesses and approximately 23,000 deaths each year in the United States.1 In 2014, the chance that a healthcare-associated infection was caused by an antibiotic-resistant organism was one in seven in short-term acute care hospitals.1 CDC has also determined that 20–50% of all antibiotics prescribed in U.S. acute care hospitals are unnecessary or inappropriate.2 Because antibiotics are a finite resource, antimicrobial stewardship programs (ASPs) are part of the 2014 White House National Strategy for Combating Antibiotic-Resistant Bacteria.3
ASPs are defined as “coordinated interventions designed to improve and measure the appropriate use of antimicrobial agents by promoting the selection of the optimal antimicrobial drug regimen including dosing, duration of therapy, and route of administration.”4 Guidelines for developing an institutional program to enhance antimicrobial stewardship were first published by the Infectious Diseases Society of America (IDSA) and the Society for Healthcare Epidemiology of America (SHEA) in 2007,5 with an update in 2016.6 Despite the availability of numerous antimicrobial stewardship guidelines, toolkits, webinars, online courses, and websites from CDC, IDSA, SHEA, and ASHP, staff at hospitals and health systems are still struggling to implement ASPs.7 According to CDC, only 39.2% of all hospitals in the United States had an ASP at the end of 2014; the national goal is 100% by 2020.8 Stewardship concepts are relatively easy to understand and embrace but implementation is more difficult, especially when experience is lacking in the use of outcome metrics. One of the potential barriers to a successful ASP that has not been widely acknowledged is a lack of mentoring.
The value of mentoring is recognized in all fields. Mentorship has been defined as “a dynamic, reciprocal relationship in a work environment between an advanced-career incumbent (mentor) and a beginner (mentee) aimed at promoting the career development of both.”9 The literature in the fields of business, education, and medicine supports the value of mentoring; however, literature on antimicrobial stewardship and mentoring is scarce. As stated by Crosby,10 “Mentoring is a brain to pick, an ear to listen, and a push in the right direction.”
Mentoring, an approach whereby experienced practitioners who are respected and trusted serve as role models and provide teaching and counseling to less-experienced persons, has the potential to facilitate the implementation and advancement of ASPs.11 Traditionally, mentoring has been conducted by senior members of a profession to ease the transition of relatively inexperienced persons into the profession.11 However, mentoring on antimicrobial stewardship can be conducted on an interprofessional basis among members of different health professions. Given the fundamental principle that a role of the mentor is to facilitate the realization of a goal, it is important to identify all potential mentors who might contribute to the successful implementation of an ASP, including hospital administrators.12 An interprofessional approach to ASP implementation in hospitals can be used to obtain “buy in” and avoid placing an excessive burden on one department.
Engagement of hospital administration is a key factor for developing and sustaining a stewardship program.
Mentoring by individuals with stewardship experience or with the authority to advance stewardship goals advances the learning curve, removes barriers limiting progress, and expedites the maturation of a stewardship program.
Collaboration of the entire stewardship team, including regularly scheduled face-to-face meetings, takes advantage of the concept of “wisdom of the crowd” and facilitates optimal effectiveness.
We sought to advance ASPs at hospitals in the United States using an innovative interprofessional mentoring program. This article summarizes the impact of the mentoring program for ASPs, lessons learned, and insights gained through the mentoring process.
Description of the mentoring program
In 2011, ASHP launched a multifaceted, interprofessional mentoring initiative designed to help pharmacists, physicians, and nurses implement ASPs or improve an existing ASP at their institutions. More than 100 applications were received for 5 funded, onsite visits. The high demand for antimicrobial stewardship mentoring in addition to favorable feedback from the 5 ASP program sites led to the development of plans for a second initiative with antimicrobial stewardship mentoring.
In 2013, a steering committee comprising an infectious diseases (ID)-trained physician and a pharmacist who were experts in antimicrobial stewardship and a pharmacist expert in outcomes measurement was established to plan the second initiative, the ASHP MENTORED QUALITY IMPROVEMENT IMPACT PROGRAM℠: Accelerating Antimicrobial Stewardship Activities. A nationwide call for applications to participate in the program at no cost to the institutions was put forth in 2014 via e-mail to ASHP members and ID professionals and online advertisements on the ASHP and Journal of Infectious Diseases websites. Only U.S. hospitals with existing ASPs were eligible to participate. As part of the application, applicants were required to name an interprofessional team that included members of the hospital administration as well as the health professionals recommended in the IDSA/SHEA guidelines (i.e., an ID physician and pharmacist, clinical microbiologist, infection control professional, information system specialist, and hospital epidemiologist) and describe their current ASP and proposed goals for program advancement.5
Applications were evaluated by the steering committee and ASHP staff, taking into consideration hospital administrative support, the antimicrobial stewardship team, infrastructure, proposed improvements in antimicrobial stewardship, and perceived patient care benefits. A weighted ranking system was used to evaluate each of these characteristics (0 points for not evident to 3 points for highly evident). The highest-ranked applications were further evaluated by the ID-trained physician and pharmacist members of the steering committee, who would serve as the faculty mentors. Nine hospitals were selected by the faculty mentors based on hospital size and type, training and credentials of the clinical pharmacist and ID physician serving as core team members, and geographic location.
On acceptance into the program in early 2014, each hospital participated in a seven-step mentoring process (Table 1). In step 1, each site completed an antimicrobial stewardship self-assessment survey (eAppendix, available at www.ajhp.org), which provided information for the faculty mentors to use to evaluate current stewardship activities. The survey also addressed barriers to improving current practices. Step 2 consisted of a presite visit telephone call with the mentors and the mentees on the ASP team to discuss the logistics of the onsite visit, plans for a collaborative continuing-education activity for all healthcare professionals at the hospital, and current barriers to the advancement of the ASP.
Step 3 was a one-day onsite program involving the mentors, mentees, ASP interprofessional team, information system specialist, pharmacy director, and hospital administrators. Faculty mentors conducted an in-depth evaluation of the hospital’s ASP, identified challenges and opportunities for improvement in antimicrobial use, and proposed activities to enhance patient care. The visits were individualized, taking into account the needs and structure of each hospital. The ASHP steering committee chose appropriateness of i.v. antibiotic “hang time” (defined as the time elapsed from the electronic antibiotic order entry to administration) in patients with and without sepsis and appropriateness of the sequence of administration (i.e., antibiotic providing broad-spectrum coverage for gram-negative pathogens administered first) when combination therapy was used as required outcome metrics. The appropriate i.v. antibiotic hang time was defined as within one hour after prescriber order entry for patients with sepsis and within two hours for patients without sepsis. Our definition of timely initiation of i.v. antibiotics in patients with sepsis was based on the “International Guidelines for Management of Severe Sepsis and Septic Shock” call for initiation of effective i.v. antibiotic therapy within one hour after the recognition of severe sepsis and septic shock.13 Prompt initiation of antibiotic therapy within one hour after writing orders has been shown to minimize mortality in patients with sepsis.14 In patients with septic shock, each hour of delay in initiating antibiotic therapy is associated with a 7.6% decrease in patient survival.15 When combination antibiotics were prescribed, such as piperacillin–tazobactam plus vancomycin, the broader-spectrum antibiotic was recommended to be infused first to improve the odds of providing an effective antibiotic rapidly.
Data for i.v. antibiotic hang time were obtained at baseline and 12 months after the start of the mentoring program from the charts of adult patients (at least 18 years old at time of admission) who were hospitalized for at least 24 hours and receiving at least one antibiotic. During each time frame, auditors were instructed to select a convenience sample of 25 charts in three different patient care units and to complete the audit within one week, unless a longer period was needed in small hospitals, for a total of 75 chart audits. The preferred units were intensive care, general medicine, and general surgical, though hospitals could select other units if necessary. In addition to the required outcome metrics, each site could select additional outcome metrics provided by the mentors (Table 2); the results of these outcome projects are ongoing and beyond the scope of this article.
During the site visit, the mentors also presented an accredited one-hour continuing-education activity for all healthcare professionals at the hospital to foster interprofessional awareness of and support for antimicrobial stewardship efforts within the institution. The physician or pharmacist mentee copresented with the mentors to provide hospital-specific ASP data. Current barriers to improving the ASP, including a lack of operational and faculty support, were identified.
In step 4, mentors prepared a formal report with recommendations for advancing the ASP and an action plan. Steps 5–7 involved outcomes data collection, analysis, and reporting. Collaborative strategies to reduce the incidence of Clostridium difficile infection (CDI), a common cause of morbidity and mortality in the United States often associated with recent antibiotic use, were discussed by the mentors with ASP team members.16,17 Since each hospital’s infection preventionists already collected monthly rates of CDI based on clinical practice guideline definitions and several of the optional outcome projects proposed by the mentors could potentially affect the rates of CDI, all sites were asked to report monthly data on the incidence of healthcare facility–onset, healthcare facility–associated CDI starting in the month before or first month of the program for use as a baseline measure, with 12 additional monthly measurements (i.e., 13 months of data).17 The appendix lists the optional process improvement initiatives suggested by the mentors to prevent and manage CDI.
Deidentified data for hang time and rates of CDI were collected from all sites via an online data management tool that was used by an ASHP project manager to monitor the progress of the mentoring program. Data collection for all outcomes was to be completed in mid-2015. At the end of the mentoring program, project leaders from each site completed an online questionnaire about the mentoring process. Mentees were asked to list examples of how the mentoring program resulted in process changes or improved patient outcomes. The questionnaire also addressed barriers to advancing ASPs. Because this was a quality-improvement program, institutional review board approval was not necessary.
Baseline data were compared with 12-month follow-up data in aggregate as well as at each individual site using a two-tailed Fisher’s exact test or chi-square test with Yates correction as appropriate. A subgroup analysis comparing baseline data with 12-month follow-up data in patients with sepsis was also performed. The a priori level of significance was 0.05.
Experience with the program
A total of 84 applications were received. Nine hospital sites were accepted into the program and had a site visit in 2014. Three sites withdrew from the program in 2015: one had severe financial difficulties resulting in resignation of the team leader, staff reassignments, and reductions in work force; one lacked the resources and administrative support needed to continue after the team leader departed the hospital; and the third site withdrew due to the team leader’s personal health problems and a change in management resulting in different priorities. Data from the six sites that completed the mentoring program were included in the analysis.
Process changes in hang time for i.v. antibiotics were implemented at all six hospitals as a result of the mentoring program. None of the hospitals had i.v. antibiotic hang time data other than pharmacy delivery times before program participation. Each ASP provided i.v. antibiotic hang time and sepsis education to its nursing and medical staff at the beginning of the mentoring program (i.e., baseline). For patients diagnosed with sepsis, the five hospitals reporting baseline and follow-up data documented significant improvements at 12 months in the timeliness of i.v. antibiotic administration (i.e., hang time) as well as the appropriate sequencing of the infusion of broad-spectrum antibiotics first when combination therapy was used (Table 3). One rehabilitation hospital did not report data because it did not treat patients with sepsis. Examination of the data from the entire patient cohort revealed no improvement overall in the timeliness and sequencing of antibiotic administration; two hospitals documented a significant improvement, two showed a nonsignificant improvement, and two reported significant worsening. Process changes included (1) modifying the computerized prescriber-order-entry (CPOE) system for i.v. antibiotics so that rolling administration times are used instead of standard default administration times and all first i.v. antibiotic doses are ordered on a stat basis, (2) adding piperacillin–tazobactam to the automated dispensing cabinets to expedite access by the nursing staff, and (3) implementing a code sepsis team in the emergency department. No significant changes in CDI rates were reported over the 13-month observation period. Rates varied from 2.69 to 23.3 new cases per 10,000 patient-days among the six hospitals.
Mentee engagement with the hospital administration resulted in increased compensation for one ID physician. Three sites received approval of protected ASP time for the pharmacist, and one site received approval for a new ASP pharmacist position. The mentors provided a strategy to help justify the cost of a rapid diagnostic test to be used in ASP interventions for Staphylococcus aureus bacteremia. As a result, the hospital administrators at three hospitals approved additional funding for the microbiology laboratory.
At five hospitals the mentors recommended and program participants implemented updated ASP reports to the hospital administration as a way to keep administrators engaged. The sixth hospital already had this process in place. To minimize the extra time burden associated with data collection, the mentors recommended that information technology (IT) staff build specific queries into the CPOE and electronic health record systems to facilitate collection of outcome metrics data and identification of patients with CDI. Five hospitals’ ASPs developed and distributed a mission statement and team photograph to promote the ASP among hospital staff. The other hospital already had a mission statement before the mentoring program. To improve the ID knowledge of the ASP pharmacists in two hospitals, the mentors recommended that the pharmacists complete an ASP certification course. The hospital administration agreed to pay the fees for participation by each pharmacist.
The postmentoring survey from participating hospitals identified three factors that contributed to success in advancing their ASPs: (1) the collaboration and face-to-face engagement of all ASP team members, (2) the inclusion of hospital administration and pharmacy directors in the onsite mentoring day as well as in follow-up efforts, and (3) an experienced mentor team with an ID physician and ID pharmacist to provide insights and guidance. Challenges included insufficient time to collect outcome metrics due to competing hospital priorities and loss of program momentum over time.
Insights and lessons learned
To our knowledge, a formal evaluation regarding the impact of and lessons learned from an interprofessional ASP mentoring program has not been previously reported. All six hospitals reported improvements in structures (use of technology and people) and processes (the way stewardship activities were performed each day), though improvements in the required hang time outcome metric for patients with and without sepsis were not as robust as expected. Several important lessons about the effectiveness of stewardship programs were learned through the mentoring program.
The first lesson learned was the need for collaboration and engagement of each team member through face-to-face meetings. Before the mentoring program, communication with the IT staff was generally via e-mail. This often led to delays in or misunderstandings about requests for information. Similarly, ID physicians often believed they were routinely consulted about all patients with certain ID diagnoses, only to be informed by the pharmacist and infection preventionists that there were many cases about which the ID physician did not have knowledge. This disconnect led to the mentor’s recommendations to more efficiently link the stewardship team’s involvement in the management of complicated cases that cross multiple disciplines (e.g., patients with S. aureus bacteremia, patients with urine cultures positive for certain problematic pathogens).
A “wisdom-of-the-crowd” approach, whereby solutions proposed by a group (e.g., an interprofessional antimicrobial stewardship committee) are more effective for problem solving and decision-making than those put forth by individuals, may help overcome barriers to advancing ASPs.18 The importance of a team effort was evident in our program because each mentored ASP team made noteworthy improvements during the onsite mentored visit that had not been accomplished through prior individual efforts.
The second lesson learned was the need to include hospital administration and pharmacy directors at the onsite mentoring day as well as in follow-up activities. The support of these individuals led to increased funding for the microbiology laboratory, new rapid diagnostic tests, and pharmacist and physician time to devote to ASP activities. One hospital administrator did not see the value of the ASP until the mentors explained the high probability of importing multidrug-resistant organisms into the hospital from the country where the institution was marketing a new medical tourism solid organ transplantation program. The surgeon in charge of this new transplantation program acknowledged that such an incident would be devastating to patient care and outcomes. This acknowledgment by the hospital administrator for the importance of the ASP was made possible by a face-to-face conversation and the wisdom-of-the-crowd approach. Our findings are consistent with the recent National Healthcare Safety Network’s survey of ASPs in U.S. acute care hospitals.19 The survey found written support from administration was the single strongest, independent predictor of hospitals having a comprehensive ASP.
Effectiveness declined in the stewardship initiative at some sites when hospital administration ceased to remain engaged after the site visit. Because of the recognized importance of administrative support, a requirement for participation in this mentoring program was signed support in the application process by the hospital’s chief executive officer. Over the course of the site visits, a reassessment of the traditional interpretation of mentoring was required. In his analysis, Levinson12 stated that the developmentally crucial function of a mentor is to support and facilitate the realization of the dream. With stewardship, the primary goal (or as stated by Levinson, the dream) to be supported and facilitated is improving quality. Members of the administrative team have the opportunity to support and facilitate the stewardship goal instead of serving solely in standard roles, such as controlling resources and setting priorities. In this mentoring program, we encountered several instances in which members of the administrative team played roles that were consistent with mentoring. These included approving the purchase of rapid diagnostic testing equipment, funding protected time for antimicrobial stewardship interventions for both pharmacists and physicians on the stewardship team, and providing the opportunity for members of the stewardship team to attend national meetings and receive training in the principles of stewardship.
A recent opinion piece identified the gaps in the behaviors of mentors that negatively affect mentees.20 In the ASHP mentoring program, one such gap of disengagement by hospital administration was the bottleneck.20 In such a situation, the high demands on hospital administration result in internal preoccupation with limited time and perhaps even limited interest in remaining engaged in the stewardship process. This often takes the form of limited time for face-to-face meetings, inadequate response to requests for help, and delays in feedback. With such absence comes the missed opportunity to contribute to the attainment of the desired quality goal espoused by the stewardship committee and required of the hospital.
There were several instances when more senior members of the stewardship team who had years of experience were the recipients of mentoring by younger individuals who had administrative positions that allowed them to facilitate the realization of the stewardship goals. The 2016 IDSA/SHEA stewardship guideline states that ASPs are “best led by ID physicians with additional stewardship training.”6 In practice, an ID physician who recently completed a fellowship and has formal training in stewardship or a young member of the administrative team who can advocate for funding or other program development opportunities might serve as the mentor for individual ASP team members whose years of job experience and chronological age exceed those of the mentor.
The third lesson learned relates to the benefits of an experienced ID physician and ID pharmacist in providing mentoring, insights, and guidance. During their interactions with mentors, mentees expressed their perspectives about issues specific to their hospital and received feedback from a mentor who could validate, refine, or reframe those perceptions. For example, mentees described a lack of physician buy in when antibiotic use was restricted. In an attempt to make stewardship an inclusive approach for all healthcare providers who prescribe antimicrobial agents, it was suggested that the stewardship program should evolve from the practice of restricted use of antibiotics to the concept of protected use of antibiotics. Such innovation in conceptual approach becomes increasingly important for meeting the Joint Commission’s new antimicrobial stewardship standard applicable to hospitals and critical access hospitals effective January 1, 2017.21 Using a patient care perspective—in contrast to a cost perspective—was identified by the mentees as valuable for obtaining additional financial support for the ASP.
Evidence-based stewardship projects are exceedingly important. Our definition of timely initiation of i.v. antibiotics in patients with sepsis was based on the International Guidelines for Management of Severe Sepsis and Septic Shock call for initiation of effective i.v. antibiotic therapy within one hour after the recognition of severe sepsis or septic shock.13 Prompt initiation of antibiotic therapy within one hour after writing orders has been shown to minimize mortality in patients with severe sepsis or septic shock.14 For the hang time outcome project, such information was combined with lessons learned from a collaborative international mentoring program between U.S. ID pharmacists and South African pharmacists.22 In that 18-month study conducted in 33 South African hospitals, the percentage of patients with an antibiotic hang time of one hour or less increased from 41% before program implementation to 82% after program implementation (p < 0.01).
Mentees of our program attributed the lack of improvement in the required hang time outcome metric for patients without sepsis to a loss of momentum when long periods elapsed without action after the on-site visits and “too many other more pressing responsibilities competing for their time.” In addition, one site underwent major remodeling in the pharmacy department, which significantly worsened hang time compliance. The ASHP project manager provided quarterly follow-up telephone calls in contrast to the weekly follow-up provided by the South African project manager. This difference probably contributed to the failure to show improvement in the required outcome metric in patients without sepsis in all hospital sites. Interestingly, the three sites that withdrew from the program were also the three hospitals that had implemented an ASP a few months before the mentoring program. Despite enthusiasm and a desire to advance their ASPs, they were unable to sustain momentum and complete the outcome data collection. This speaks to the challenges faced by ASP pharmacists and physicians when stewardship interventions and data collection are added to existing job expectations without dedicated time for stewardship.
This assessment of our mentoring program has limitations. Three hospitals dropped out after the mentoring process, leaving only six hospitals to collect outcomes data. This small number of participating hospitals may not allow the extrapolation of findings to other hospital settings. The short data collection period was probably not sufficient to identify statistically significant changes in all outcomes. Assessing the required outcome metric after only 12 months did not allow adequate time at all sites for process improvement changes to take effect. Nevertheless, the six sites have continued using this and additional outcome metrics. Moreover, both the mentees and mentors learned many valuable lessons. Realizing that a one-on-one ASP mentoring program is not available to all hospitals, we believe the lessons learned can be applied by ASPs at any hospital.
A mentoring program for antimicrobial stewardship provided the perspective that comes from experience. Engagement of hospital administration was a key factor for both developing and sustaining a stewardship program.
Appendix Process improvements to prevent or manage CDIsa
Prevention of CDIs
PPIs removed from order sets.
Electronic alerts developed by IT department to identify patients concurrently receiving antibiotics plus a PPI.
Electronic alerts developed by IT department to identify patients receiving three or more antibiotics.
Weekly rounds conducted by ASP pharmacist to review all patients receiving PPIs.
Management of CDIs
CDI scoring system developed by IT department to identify mild-to-moderate and severe CDIs, and CDI score used by ASP team to determine appropriateness of antibiotic therapy for CDI.
CDI treatment algorithms posted at each pharmacy workstation.
Weekly audits performed by pharmacy residents to ensure compliance with CDI hospital guidelines.
↵a CDI = Clostridium difficile infection, IT = information technology, PPI = proton pump inhibitor, ASP = antimicrobial stewardship program.
Supplementary material is available with the full text of this article at www.ajhp.org.
The MENTORED QUALITY IMPROVEMENT IMPACT PROGRAM℠: Accelerating Antimicrobial Stewardship Activities was coordinated by ASHP and supported by an educational grant from GlaxoSmithKline. ASHP’s Office of Professional Development provided editorial assistance in the preparation of this article. Drs. Goff and Karam received honoraria for their participation in the site visits as mentors, and Dr. Haines received payment as a consultant related to data collection and analysis for the mentored program. None of the authors received an honorarium for preparation of this article. The authors have declared no other potential conflicts of interest.
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