Advances in the Prevention and Control of HAIs

Developing the Capacity to Implement Antimicrobial Stewardship: Opportunities for the Future

Table of Contents

Carol VanDeusen Lukas, Elisa Koppelman, Belinda Ostrowsky, Zeynep Sumer, Hillary Jalon, Cynthia Araujo, Rafael Ruiz, Shakara Brown, Brian Currie.


Multiple initiatives and major campaigns around infection control and environmental cleaning are underway to control healthcare-associated infections (HAIs). However, as new and increasingly resistant strains of bacteria emerge, the problem persists, and additional strategies are necessary. Antimicrobial stewardship programs (ASPs) show promise as one of those additional strategies for addressing HAIs. The ERASE C. difficile Project was designed to implement and evaluate ASP interventions, with a focus on reducing Clostridium difficile infection (CDI) in a mixed-methods study design. ERASE C. difficile worked with six hospitals with early ASPs that were recruited by Greater New York Hospital Association (GNYHA)/United Hospital Fund (UHF) on the basis of their successful participation in a prior C. difficile-focused collaborative. All six hospitals succeeded in reducing the use of antibiotics targeted by the ASP on one or more measures. However, ASP implementation was typically more complex, faced greater challenges, and took longer than expected. The study showed that using limited case-control methods for antibiotic selection was a feasible, practical, and acceptable approach for facilities to identify potential antibiotic targets for the ASP. Moreover, ASP activities were broader than restrictions on targeted antibiotics. Sites varied by staffing and who carried out ASP roles; however, in all cases ASP activities were multidisciplinary. Many ASPs were implemented with limited, dedicated staff and a prohibition on hiring new staff. These findings suggest that while each hospital needs to tailor its ASP to its unique staffing, resources, culture, and existing practices and relationships, there are common lessons to guide implementation across hospitals.


Reducing healthcare-associated infections (HAIs), especially in hospital settings, is a major health and public health imperative in today's health care environment. HAIs are the most common complication of hospital care and one of the 10 leading causes of death in the United States.1 New sources of infection and increasingly resistant strains of well-known bacteria are increasing the dangers of HAIs. For example, Clostridium difficile infection (CDI) is a serious public health problem that has recently increased in both incidence and severity. From 2000 to 2009, the number of hospitalized patients with a CDI diagnosis more than doubled, from 139,000 to 336,600.2,3 There are also indications of recent increases in the severity of CDI, including increased complications, with CDI linked to 14,000 deaths in the United States each year and CDI-related mortality rising by 400 percent between 2000 and 2007.4 Studies have found that, in addition to personal harm to patients, there are major costs associated with CDI, such as longer inpatient lengths of stay and a significant increase in costs both for inpatient care and at 180 days after the initial hospitalization when the CDI occurred.5,6 The major risk factors for CDI, in addition to advanced age, are exposure to antimicrobials and hospitalization.7

Multiple initiatives and major campaigns around infection control and environmental cleaning are underway to control HAIs;8,9 however, as new and increasingly resistant strains of bacteria emerge, the problem persists, and additional strategies are necessary. Antimicrobial stewardship targeted to HAI reduction shows promise as a complementary strategy for infections such as CDI, where increased rates are associated with inappropriate antibiotic use. An antimicrobial stewardship program (ASP) is a systematic approach for developing coordinated interventions to reduce the overuse and inappropriate selection of antibiotics and to achieve optimal outcomes for patients in cost-efficient ways. Through both monitoring and, when necessary, altering current antimicrobial prescribing practices, antimicrobial stewardship has been shown to improve patient care, reduce antimicrobial use, reduce pharmacy and overall hospital operating costs, and potentially reduce antimicrobial resistance.10

Despite the expanding evidence that ASPs could reduce HAIs, many health care institutions continue to identify barriers to implementing ASP strategies. Many of these barriers are related to obtaining institutional support for these kinds of programs. Stewardship activities involve complex organizational change because they require individuals to alter both the way they work and the way they interact with each other and, thus, require changes in both individual behavior and processes within the organization. Complex organizational change is difficult to accomplish.11

In this paper, we profile the experiences of six hospitals in implementing ASPs targeted to reducing CDI in order to offer lessons to other medical centers interested in developing their own ASPs. The six hospitals served as intervention sites in a recent initiative sponsored by the Agency for Healthcare Quality and Research (AHRQ) and supported by the Centers for Disease Control and Prevention (CDC). The initiative, Evaluation & Research on Antimicrobial Stewardship's Effect on Clostridium difficile (ERASE C. difficile) Project, was led by a collaborative team from Montefiore Medical Center (MMC), the Greater New York Hospital Association (GNYHA)/United Hospital Fund (UHF), and the Boston University School of Public Health (BUSPH).


Participating Hospitals

The six intervention sites, in four health care systems, are all located in the greater New York region. All are major teaching hospitals, with the number of licensed beds ranging from 396 to 871. Each was recruited by GNYHA/UHF for ERASE C. difficile based, first, on the hospital's successful participation in an earlier GNYHA/UHF C. difficile Collaborative to establish basic ASPs;12,13 second, on its high level of compliance with infection control and environmental practices (but still having high CDI rates); and third, on its commitment to developing its ASP to target CDI reduction further.

Conceptual Framework

Figure 1 provides an overview of the ASP implementation in ERASE C. difficile based on an implementation science conceptual model14 that guided the project. The logic underlying the model is that external facilitation influences the local implementation strategies used by ASP teams to create and implement the clinical interventions undertaken to target antibiotic use. The implementation of the clinical intervention then determines the process outcome, which is measured by reduction in the use of the targeted antibiotics and, over the longer term, by reduction of CDI in the facility. All this work is influenced by the organizational context in which the implementation efforts take place. The context relationships are shown in Figure 1 with double-headed arrows to signal a potential reverse influence as the implementation strategies and interventions demonstrate success that results in increased organizational support.

In this paper, we focus on the local implementation strategies. The organizational context influences the strategies and the interventions targeted, as discussed below in the sections on local implementation strategies and the lessons learned in the project. The findings in the other model domains, highlighted in the overview of the ERASE C. difficile intervention, provide the backdrop for those analyses.

Figure 1. Implementing antimicrobial stewardship

This figure is an algorithm that represents the factors that were considered in implementing an antimicrobial stewardship program as part of this project. These were external facilitation, local implementation strategies, clinical intervention, process outcome, and organizational context.

Data Sources

Data were drawn from four sources, which are discussed below.

Data on antibiotic use. Antibiotic usage data were used for case-control and to assess changes in the volumes of antibiotics targeted in the intervention. Each intervention hospital performed its own limited case-control study on adult (18 years of age or older) inpatients to identify the antibiotics or antibiotic classes associated with CDI (but not to extensively explore other factors associated with CDI). A minimum of 33 CDI cases were obtained from the National Healthcare Safety Network (NHSN) between March 2010 and May 2010. Control cases were adult inpatients free of CDI for 3 months before or after their diagnosis, matched by age (± 5 years) and admission date (± 5 days) to achieve a 2:1 control-to-case ratio. Additional details regarding the preliminary work performed to determine the best strategies for matching controls, length of time, and data elements needed are reported elsewhere.15 Odds ratios were used to compare antibiotic use between the case and control groups at each hospital. Statistically significant odds ratios and evaluation of prescription frequency were used to identify preliminary antibiotic targets. Final targets were selected after an internal medication review of prescribing patterns (e.g., who prescribed the drug, for what types of patients, for which diagnoses), which informed the selection of appropriate antimicrobial stewardship interventions. All intervention sites provided data regularly on antibiotic usage, employing a format standardized by MMC and GNYHA. The format was chosen based on the feasibility of extracting antibiotic data from the electronic medical records (EMRs) and informed by interviews with information technology (IT) and ASP staff at each of the sites. Antibiotic consumption was measured with three distinct measures—defined daily dose (DDD), days of therapy (DOT), and number of courses (NOCs) prescribed.6,16 We examined total antibiotic usage, total target antibiotic usage, total non-target antibiotic usage, and usage for each individual target antibiotic/class.

The measure of implementation effectiveness is based on the usage data. The project team also regularly collected standard data on environmental cleaning, infection control practices, and CDI rates.

Site data on the timing and focus of interventions. Comprehensive qualitative data were collected from each site to identify details about the kinds of ASP strategies implemented within each institution. The data were collected through frequent ad hoc conversations between project team members and the intervention sites, requests from project team members for intervention sites to document the details of their implementation, and individualized meetings between intervention site staff and the infectious disease (ID) physicians on the project team, as well as the project team documentation detailed below. This information was used to develop site profiles of ASP interventions and implementation strategies (summarized in the Appendix), and contributed to the analysis of the implementation process.

Project team documentation. Project team documentation came from two sources. First, GNYHA facilitated monthly conference calls with the intervention sites, during which detailed notes were taken by a project team member on specific project activities from the perspective of the site participants. Second, core project team meetings were held via conference calls regularly throughout the project. The standing agenda included reports about interactions with the hospitals around their data collection and analysis and their activities to implement ASP. Detailed notes provided a running log of project activities, discussion decisions, tasks, and responsibilities. Data from these sources were categorized by type of intervention provided to describe the external facilitation provided and the site implementation processes and to contribute to the analysis of factors that affected implementation.

Group interviews with clinical staff. Project team members from BUSPH with extensive qualitative research experience and no involvement in facilitating the intervention conducted group telephone interviews with members of the ASP team and other involved clinicians at each participating site. Four group interview sessions lasting between 45 and 60 minutes were conducted with staff at the six intervention sites about 6 months after the ASP interventions were introduced; two of the group interviews included staff from two sites within the same system. Group size ranged from 7 to 14, depending on the number of staff involved in ASP implementation in a site and availability to participate in the discussion. Guided by an institutional review board-approved semi-structured protocol, the interviews were designed to explore qualitatively the processes, dynamics, and factors affecting the implementation of the antimicrobial stewardship program, including the challenges the staff faced. Detailed notes of each session, supported by audio recordings, were analyzed qualitatively using a structured analytic framework that provided the initial organization and coding of data. In the framework approach, which was used previously by the BUSPH team in multiple other projects, key constructs from the conceptual model were defined operationally and arrayed as rows headings in a matrix. Narrative evidence about the presence of each construct was recorded for each site in the matrix cells. Data from the interviews were then used to describe the site implementation processes and to identify the factors that affected implementation. A summary of the analyses from these sessions is included in the Appendix.

Overview of the ERASE C. difficile Intervention

The six participating hospitals received comparable external facilitation from project team members from MMC, GNYHA, and UHF. The hospitals conducted limited case-control studies, collected data in standard format and provided the data to GNYHA, and implemented ASP interventions targeted to reduce use of the antibiotics identified through the limited case-control studies. All had some success in reducing the use of those antibiotics, as described below.

External Facilitation

The project team provided limited external facilitation to support local implementation. The six intervention sites participated in an in-person kick-off learning session early in the project, monthly conference calls throughout the project, and informal meetings with the project's ID physician. The project team also provided ongoing technical assistance in setting up data files and conducting the case-control activities through the monthly conference calls and through interactions with individual sites by phone, email correspondence, or face-to-face small meetings.

Clinical Intervention to Reduce Targeted Antibiotics

Antimicrobial stewardship begins with the identification of antibiotics associated with HAIs, in this case CDI. Consistent with the ASP approach, all sites conducted limited case-control analyses to identify target antibiotics as planned. Each hospital then selected specific interventions to reduce the use of the target antibiotics at their site. Each facility identified between one and four potential target antibiotics and many potential interventions (refer to Appendix). Three antibiotics were associated with CDI in some combination at four of the six intervention sites: piperacillin/tazobactam, fluoroquinolones, and cefepime.

As shown in the Appendix, hospitals implemented up to three interventions to reduce the use of these antibiotics, most of which affected the entire hospital, with a back-end audit and feedback approach adopted as a viable intervention at all the intervention sites (i.e., allowing initiation of empiric antibiotic but assisting prescribers in reevaluating the antibiotic choice to potentially stop, narrow the spectrum of, or shorten the antibiotic course based on preset criteria, such as cultures, clinical status, or duration of antibiotics). The hospitals' staggered rollout, with variable time periods to fully implement their interventions, resulted in a total rollout period of approximately 15 months.

Process Outcomes: Reduction of Targeted Antibiotics

Intervention sites were able to reduce at least one of their antibiotic targets on at least one of the measures. The full analyses of ASP reductions in antibiotic use and the impact on CDI reduction are presented in the final project report to AHRQ.17,18

Local Implementation Strategies

Despite the relative success of all sites in reducing targeted antibiotics, achieving those levels of success was not easy, and the details of implementation varied across sites. The implementation of the ASP interventions was typically more complex than expected. Guidance for antimicrobial stewardship offers general principles for a program but not a detailed blueprint. There is no one-size-fits-all model nor a single "right way" to structure and carry out the program. ASP activities take place in the context of the larger hospital and health system organization. Typically, ASP programs are expected to demonstrate a strong business case based on cost savings. Organizational factors, such as IT support for ASP and staffing resources available, can affect implementation, serving either as facilitators or as barriers that present challenges to be overcome.

As expected, each hospital tailored the details of its ASP to its unique staffing and culture, existing practices and relationships, and available resources. This section describes the different approaches the participating hospitals used to put the ASP principles into practice. The Appendix presents a profile of the implementation strategies, interventions, and resources for the participating hospitals (information for hospitals from the same system is combined). The next section offers lessons—including frequent challenges—that were common across hospitals.

ASP Staffing

Intervention sites differed in the details of their ASP staffing (refer to Appendix). However, in all cases, ASP activities were multidisciplinary. Sites varied in whether the leadership of the ERASE C. difficile ASP resided primarily in Pharmacy or Infectious Disease. In five sites, ID physicians played the lead role, although with variation in the details of their working relationships with Pharmacy. In the sixth site, an ID-trained clinical pharmacist led the ASP with backup from an ID physician, but the pharmacist primarily drove the ASP together with pharmacy residents. ID fellows and pharmacy residents played important roles in all sites, although in different configurations and with different lengths of rotation. Five of the six sites had ID fellows who participated in the ASP. All sites had pharmacy residents but on limited rotations—two sites had 5-week rotations (one with two residents and the other with four)—so the ASP had access to this resource for only part of the year. All four sites had pharmacists who filled prominent roles in the ASP. Additionally, all sites had ID physicians, but the size of the departments varied as did the proportion that were on staff versus private physicians who provided their services through consulting. All facilities had an infection control team, with a ratio of no less than one infection prevention and control practitioner (ICP) per 250 beds (but this varied among facilities). The ICPs may have collaborated with the ASP staff, but on the whole they worked in parallel.

Stewardship Activities

Each site's staffing, IT resources, and education and training structures contributed to the interventions that were chosen and implemented at each site to address the antibiotics targeted for reduction, as detailed in the Appendix. While all sites targeted piperacillin/tazobactam, and two of the six sites chose to use audit and feedback to reduce usage, the unique characteristics of each site resulted in very different stewardship activities. For example, one site used data mining software, with one pharmacist guiding the work of residents, who in turn interacted with the medical staff around ID issues. Another site's ASP lead, an ID physician, trained fellows who examined computer-generated lists of data by hand for antibiotic use patterns. This site had a high proportion of consulting IDs, making buy-in of ASP particularly challenging. One system with two sites led by an ID physician and pharmacist used specially trained ID pharmacists to work closely with physicians. These sites devoted extensive resources to education to augment the audit and feedback effort, and they were moving toward formalizing their ASP, using the ASP to drive institutional policy. Each site, in addition, used resources specific to its institution to develop processes that complemented its ASP activities, illustrating the unique characteristics of each site's ASP activities and overall program.

Education, Training, and Coaching

ASP activities had a broader scope than just restrictions on targeted antibiotics. Substantial training and education were needed, first, to highlight the important role of antibiotic restrictions and their interconnectedness to other infection control practices, and second, to explain the stewardship approaches being used and the roles of different professional groups in implementing them. The intervention sites differed in the details of their education approaches, but all used multiple approaches to inform prescribers and clinical staff about the ASP (refer to Appendix). For example, most sites combined formal lectures, grand rounds, and faculty development forums or guest speakers, with individual conversations, visits to the floors, and coaching in implementing the interventions to reinforce the formal education.

Information System Support

IT software that screens patients for the targeted antibiotics or for other specific criteria for stewardship is a clear implementation facilitator. For example, one site used MedMined® Surveillance Advisor,19 which was provided by resources from the city hospital oversight system; other electronic ASP surveillance software systems are available. Without investment in these systems, which are costly, the human resources needed to monitor targeted antibiotics are substantial. Participating systems differed in the extent of their systems support, as shown in the Appendix. All sites required substantial IT assistance to extract the data needed for the case-control study and antibiotic usage tracking. Though many sites had EMRs or a computerized physician order entry (CPOE) system, the data typically available were not aggregated or in a format useful to the ASP team. One site had developed an internal template iteratively over several months with its IT team. The template and strategy were ultimately shared with IT staff at each of the sites, allowing ASP teams to learn from each other about how to physically obtain and leverage their data for the ASP activities that followed data collection. In all cases, managing the data was labor intensive.


The experiences of the intervention sites illustrate a number of common lessons about implementing ASP, including both facilitators and challenges to ASP development and success.

The limited case-control methods for antibiotic selection were less complicated than anticipated, but the data burden of antimicrobial targeting was typically heavy. Utilizing limited case-control methods for antibiotic selection is a feasible, practical, and acceptable approach for facilities to identify potential antibiotic targets for ASP. Tools such as an antibiogram can be simple to use and effective in encouraging prescribers to change practice quickly. However, all aspects of acquiring data from ASP activities may be challenging. Obtaining the data in the format needed for the analyses was one of the biggest hurdles the sites faced. Likewise, discerning trends in antibiotic prescribing or simply identifying specific patients to target for ASP activities (i.e., audits) was challenging. Having additional (data mining/data surveillance) software to assist in exploration of clinical information can be helpful, but it always needs to be complemented by an astute ASP member who can interpret and prioritize the results.

Finding strategies where enough of the prescribing could be impacted was difficult. Most sites selected antibiotic targets that were used at a very high rate. However, it was difficult to develop strategies that could address the most highly prescribed antibiotics because they are often prescribed in many different ways, even within one facility (i.e., for different indications, for different populations, and by prescribers of varying types and with varying expertise). For some facilities, limiting the scope of certain interventions was the only feasible option. For example, two sites set up an auditing system to review patients prescribed at least 72 hours of piperacillin/tazobactam. However, it would have been overwhelming to attempt to audit and intervene on all piperacillin/tazobactam at prescribing initiation. Therefore, the ASP teams focused their efforts on services with the highest likelihood of de-escalation of antibiotic use and clinicians' acceptance of the intervention—in these cases, the medical teaching and medical hospitalist non-teaching services. This was a practical strategy, but it was able to impact only a segment (estimated at less than 50 percent) of piperacillin/tazobactam prescribing.

Collaboration among clinical staff strengthens the ASP process. ASP at the clinical level is the heart of the program. Strong stewardship leadership is critical, but the involvement of other staff needs to be considered. ASP does not stand on its own, but rather it must work in partnership with other departments. ASP should complement infection control and environmental cleaning protocols. Involving infection prevention staff and epidemiologists in the interdisciplinary team will strengthen the link between ASP implementation and infection reduction and prevention efforts. The link between ID physicians and pharmacists is critical, and their roles are complementary: pharmacists are needed to fully understand the clinical implications of different antibiotics, and physicians are credible sources in talking with prescribers. Some sites had a long history of close relationships between pharmacy and ID—for example, they round and teach together—while others had to build such relationships. One recommendation for future consideration is to make prescribing a distinct and specialized area of expertise through an integrated ID physician and pharmacist stewardship.

Changing physician practice can be difficult. Often prescribers and house staff are not, initially, fully receptive to being told what to do and how to do it. In most cases, acceptance grows as they learn more about ASP and as relationships with ID and Pharmacy are built and strengthened. A history of antibiotic restrictions and acceptance of those practices usually paves the way for ASP acceptance, but prescribers may not understand ASP at first, even after education. Also, in some cases, additional effort is needed to reduce adversarial positions between prescribers, pharmacists, and ASP and to increase prescriber acceptance of pharmacy residents' recommendations. Resistance is often strongest among private consulting physicians, who are at the hospital less frequently and whose ties are weaker than facility-employed physicians. Communication and education are crucial in the process of gaining prescriber buy-in. Communications with physicians need to come from a credible source and include consistent messages from clinical leaders. Calls from ASP team members can be used for educational purposes as well as a specific communication about the antibiotic in question.

Residents and fellows are important resources for ASP but also bring limitations. All intervention sites relied on ID fellows and/or pharmacy residents to implement the antibiotic restrictions for ASP, but this reliance has shortcomings. First, fellows and residents are only part-time staff, sometimes on very limited rotations, resulting in varying levels of ASP activities from month to month. Even in sites where the pharmacy residents are there for a full year, their time is not dedicated fully to ASP because they have multiple roles and responsibilities. Moreover, postgraduate year 1 (PGY1) pharmacy residents have not yet specialized and therefore may not be interested in ID. Second, when residents are new, physician acceptance of their recommendations is often low. As residents become known to the physicians and gain confidence in working with them, the acceptance of their recommendations increases. It takes time to build confidence and trust; when rotations are short, it is difficult. There was interest among some in changing fellowship and residency rotations to have a longer period, at least 6 months, available for ASP. However, others suggested that this may not be realistic, and that these types of rotations may be more applicable to a PGY2 pharmacy resident specializing in ID.

ASP may require other changes in professional training programs and educational materials. Shifting antibiotic approvals away from ID fellows to the dedicated ASP team (pharmacists and ID physicians) at least for portions of the day may change what has been a cornerstone of many ID fellowship training models. It allows the ID fellows more dedicated time to spend on consults and the ability to do more consults. When the fellows are involved in the approval process during evenings/weekends or as special rotations with the ASP team, their activity is supervised and can become an educational activity. As a result, aspects of the training program may need to be redesigned, including developing lectures/ curriculum for fellows on ASP topics. For other trainees (medical residents, medical students), there may be other advantages to having a small team from ASP taking all calls; it allows for a more consistent approach, provides some continuity for patient care, and allows the interactions to be more educational (there are now individuals whose primary responsibility is to approve antibiotics, rather than relying on fellows to be responsible for this activity, in addition to many others). Educational material may be needed that can be shared with callers regarding their patients and questions.

ASP brings organization and leverage. Having a formal ASP for reducing CDI allows more progress than the individual activities that may have been in place previously. For example, members of one ASP team reported that as ASP became more formalized, there was more organization to the ASP activities, including more specific roles for the pharmacists. The team felt the program had an impact on pushing institutional policies, with more success than before the ASP. The role of microbiology labs in ASP, for example, is illustrated by one site's recognition that when the microbiology laboratory implemented a more sensitive testing algorithm for CDI, the ASP team's input and involvement were welcomed. The ASP team helped educate providers on the proper use and interpretation of the testing, which in turn had implications for prescribing and other clinical practice decisions, including guiding treatment for CDI. This added to clinicians' confidence in the newer, more sensitive CDI methods and discouraged wasteful, repetitive CDI testing. As another example, during the seasonal or H1N1 influenza high activity times, the ASP teams helped clinicians understand the limitations of influenza testing and helped prescribers identify which patients to test and treat with antivirals.

Each hospital needs to prioritize and negotiate the scope of its ASP. The scope of ASP is potentially very broad; there are extensive questions about which responsibilities can realistically be assumed by stewardship. Several sites talked about wanting ASP to be an overarching program that would be more than simply approving drugs and lowering costs. But going beyond prescribing may lead to pushback, though it may also spark thoughtful consideration of procedures. In one site, the ASP committee wanted to perform piperacillin/tazobactam extended infusion therapy as an additional ASP strategy. However, nursing staff resisted because the nursing time required to set up the pumps with each patient would be lengthy as would the time each patient would require with the pump; the end result was believed to be unmanageable. Aside from the question of time and resource commitment, discussion of the recommendation revealed research20 indicating that the medical outcomes from extended infusion were not quite as convincing as first believed.

Spread and sustainability require organizational support. Support from senior medical center leaders is a clear facilitator for ASP. In two systems, a person was specifically brought in to lead the stewardship initiative, suggesting its priority to the organization. However, in some other sites, clinical ASP leads were stretched thin with little administrative support. In certain other sites, the ASP leads fulfilled that role in addition to all their other duties. More broadly, beyond relying on fellows and residents, most sites had to be creative in finding staff resources.

Making the business case for ASP, usually by demonstrating cost savings, is critical although it may not always be successful. ASP is not always a high priority for senior leaders when it is competing against other initiatives for staff and IT resources. In one case, ASP did not make the capital budget list to obtain needed software applications—even though it could demonstrate a solid business case—because other resource needs were deemed more important.


ASPs offer potential for important benefits for reducing the use of targeted antibiotics that are strategically selected. Simple methods of conducting limited case-control studies are effective in identifying targeted antibiotics. At the same time, intervention implementation was typically more complex than envisioned, with most interventions taking longer to implement than expected. Each facility acknowledged that several supplementary stewardship activities, including widespread education, were needed to implement the intervention. Gaining necessary approval for plans from committees, obtaining assistance from information technology staff, developing materials, getting buy-in from other prescribers, and educating involved staff about the intervention or intervention modification after pilot testing all served to extend the time required to fully implement the interventions. In some cases, a specific planned intervention had to be scuttled or received lower priority because of the success of other interventions or the need for other stewardship activities. While each participating hospital had to tailor its ASP to its unique staffing, resources, culture, and existing practices and relationships, there are common lessons to guide implementation. For hospitals and systems that want to pursue an antimicrobial stewardship program, the toolkit developed from the ERASE C. difficile Project can help guide them through the complexities of implementation.21


The project was funded under contract HHSA290200600012i (TO#10) from the Agency for Healthcare Research and Quality (AHRQ), U.S. Department of Health and Human Services via the AHRQ ACTION II initiative to Boston University. The findings and conclusions in this document are those of the authors, who are responsible for its content, and do not necessarily represent the views of AHRQ. No statement in this report should be construed as an official position of AHRQ or of the U.S. Department of Health and Human Services.

We appreciate the ongoing guidance and feedback throughout the project from Katherine Crosson, MPH; Darryl T. Gray, M.D., Sc.D., FAHA; James I. Cleeman, M.D.; our AHRQ Task Order Officers; and Carolyn Gould, M.D., the CDC project advisor. We also wish to recognize the invaluable contributions in the early phases of the project by Maria Woods, Esq., and Gina Shin from the Greater New York Hospital Association, and Mari-Lynn Drainoni, Ph.D., from the Boston University School of Public Health. Finally, we are grateful for the participation of the 10 hospitals that joined the project and greatly admire their ongoing efforts to combat the spread of C. difficile in their facilities.

Authors' Affiliations

Boston University School of Public Health, Boston, MA (CVL, EK). Center for Organization, Leadership and Management Research, Department of Veterans Affairs, Boston, MA (CVL). Montefiore Medical Center, Bronx, NY (BO, SB, BC). Albert Einstein College of Medicine, Bronx, NY (BO, BC). Greater NY Hospital Association (GNYHA), New York, NY (ZS, CA, RR). United Hospital Fund (UHF), New York, NY (HJ).

Address correspondence to: Carol VanDeusen Lukas, Ed.D., Clinical Associate Professor, Department of Health Policy and Management, Boston University School of Public Health, 715 Albany Street, T3W, Boston MA 02118; Email:


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21. Toolkit for Reduction of Clostridium difficile Infections Through Antimicrobial Stewardship: The Evaluation and Research on Antimicrobial Stewardship's Effect on Clostridium difficile (ERASE C. difficile) Project. AHRQ Publication No. 12-0082-EF. Rockville, MD: Agency for Healthcare Research and Quality; September 2012.

Appendix. ASP local implementation strategies, interventions and resources

Site No. Staffing Details Education / Training / IT Resources Antibiotic Targets and Interventions Stewardship Activity Details
1 & 6
  • ID MD leadership, working closely with Pharmacy.
  • Residents have ID rotation but do not participate in ASP.
  • ID fellows participate in ASP for CDI; approve antibiotics on nights/weekends.
  • Large ID department, all on hospital staff: simple to disseminate ASP information but difficult to standardize prescribing (different teaching services).
ID MD ASP lead:

  • Provides extensive education, supported by informal individual conversations with house staff. Approval calls often lead to case discussions, which furthers education.
  • Provides education to nurses/nursing attendants to ensure they and prescribers understand interconnectedness of infection control, antibiotic use, and their own roles in those processes.
  • Works with coaches' interdisciplinary group—nurses, technicians who are not prescribers but serve as champions—to assist with promoting sensible infection control practices on the floors and to support stewardship activities.
Fluoroquinolones: Hospital-wide changes to azithromycin restriction to move prescribers away from fluoroquinolones.
PIP/TAZO (and other broad-spectrum empiric antibiotics): Medicine services audit and feedback (sites 1 [mainly] and 6.
Sepsis protocol in ED and Critical Care (site 1).
Details: ID MD and PharmD initially trained ID fellow, then trained clinical pharmacists; PIP/TAZO audit mainly on Medicine services.
How done:

  • Specially trained ID PharmDs work closely with ID MD; complementary because difficult for PharmDs to approach MDs, hard for MDs to know all dosing specifics that PharmDs do.
  • Many services unified across sites for ASP.
  • As ASP is increasingly formalized, more organization in ASP activities and specific role for PharmDs.
  • ASP pushing institutional policies; harder to establish without ASP.
  • Interdepartmental collaborations with Intensive Care and Microbiology.
  • Site-specific details: house staff go between sites; pharmacy systemwide; infection control unified; Microbiology unified under lab at Site 1 with satellites at other locations.

Supporting activities:

  • Review by P&T committee, formal medication reviews.
  • Algorithm preparation.
  • Extensive educational programs (talks, one-on-one discussions, dissemination materials, train-the-trainer).

Other stewardship activities during timeframe:

  • Changes to surgical prophylaxis.
  • Ongoing work with ED—sepsis, community-acquired pneumonia.
  • PIP/TAZO extended infusion.
  • Extensive outreach/education on CDI and antibiotic use
  • PhD (RPh) leadership with ID/MD backup.
  • Pharmacy residents on limited rotations; coverage only part of year.
  • No fellows, viewed by site ASP lead as limiting resources considerably.
  • Uses medical residents to help with ASP.
  • ASP committee meets quarterly and reports to P&T committee.
  • Weekly grand rounds are ongoing opportunity to discuss ASP.
  • Guest speakers from ASPs at other facilities.
  • ASP lead distributes brochures to staff to reinforce learning.


  • CPOE for past 3 years.
  • As part of electronic system, site uses externally-developed proprietary medication monitoring application that provides certain types of computer alerts, including hard stop for certain antibiotics.

Process not controlled by pharmacy; alerts force MDs to think about intended use of antibiotics and thus contain use.

PIP/TAZO (and other broad-spectrum antibiotics): Hospital-wide audit of longer antibiotic courses (8-14 days).

  • Hospital-wide computer prompting for intravenous to oral therapy switches and also asks for reassessment of indications for drug.
  • Change antibiotic policy/algorithms from Ciprofloxacin for empiric antibiotics for urinary tract infection (UTI) and hospital-acquired pneumonia (HCAP).
Details: Audits supported by use of purchased data mining / data surveillance software. Interventions supported by one PhD (RPh) and chief residents.
How done: PharmD residents taught monitoring and how to interact with medical staff around ID issues and how to use the software; weekend rotations for both managerial and clinical role.
Supporting activities:

  • Preparation of new treatment algorithm for UTI.
  • Preparation of updated treatment guidelines for HCAP.
  • Information technology support.
  • Review by P&T committee.
  • Extensive educational programs and train-the trainer sessions.

Other stewardship activities during timeframe: Implemented requirement for indication for antibiotic orders.

  • ID MD chief provides overall leadership with day-to-day operational leadership by ID MD and clinical pharmacist (driving forces for ASP).
  • Pharmacy residents on limited rotations—only part of year covered.
  • ID consultants consist of full-time, part-time, and adjunct ID faculty members.
ASP lead:

  • Trains fellows, including talking with them individually.
  • Gives lectures, talks on the floor to hospitalist, residents, and attending.
  • Looks for patterns in prescribing that are then brought to faculty development forum for feedback and review.

Senior ID MD:

  • Provides "clinical cover" to assure physicians that changes are not having negative clinical outcomes.


  • Computer system generates daily lists of patients on broad-spectrum agents along with demographic and diagnosis information.
  • No data mining software; dependent on human followup rather than computer alerts.
  • Clinicians prefer more targeted information, for example, regular reports that show data specific to their departments.
PIP/TAZO (and other broad-spectrum antibiotics): Hospital-wide restriction and audit and feedback. Details: Overall limited resources: part-time pharmacist and ID physician; involvement of ID fellows. Interventions carried out by ID MD, PharmD, and ID fellows.
How done:

  • Two ID rounding teams separate from ASP team; all in close physical proximity and work closely; formal discussions via twice weekly meetings/conferences and/or informally in day-to-day conversations.
  • Junior fellows spend time on floors; carry pager 1 of 4 weeks for consults, emergencies, and antibiotic approvals; discuss appropriateness of requested antibiotic with prescriber and screen for potential problems; month-long turns to (1) review cultures (thus more flexibility for phone consults; and (2) go on floors to track down house staff.
  • Fellows make recommendations on those cases where ID official consultation is already involved in case (fellows not called if antibiotic approved by ID faculty member); senior personnel readily available for consults.
  • Fellows carry list of patients and currently prescribed antibiotic; aware of restricted agents; approval number needed for computer entry, and there is a stop on pharmacy end if something is not on approved list.
  • Audit/review: ID MD and pharmacy make recommendations re: dose adjustment, de-escalation, and early discontinuation of antibiotics as indicated. Interventions made on wide range of antimicrobial agents including cefepime (cefepime increase when PIP/TAZO restricted), carbapenems, fluoroquinolones.

Supporting activities:

  • IT support (for paper audit lists).
  • Review by P&T committee.
  • Extensive educational programs and train-the-trainer sessions (ID fellows trained to do approval review).

Other stewardship activities during timeframe:

  • Use of antibiotic prescribing data.
  • Select audit/review of other agents (cefepime increase when PIP/TAZO restricted).
  • Education of newer prescribers on staff.
4 & 5
  • ID MD chair works closely with interdisciplinary team (ID MD chair, clinical pharmacy manager, nurse epidemiologists, director of microbiology) that meets regularly to allocate resources, make assignments, and provide coverage when needed.
  • PGY-1 pharmacy residents with 1-year rotations and 3 ID fellows. ASP done as part of standard training or longitudinal rotation or projects.
  • The ID MD lead believes his longevity at hospital has permitted establishment of a strong rapport with all other ID MDs.
Senior ID MD:

  • Presents grand rounds on ASP to combined Departments of Medicine and Pharmacy.
  • Meets with pharmacy personnel on multiple occasions.

Clinical pharmacy manager:

  • Provides education for pharmacy residents, other pharmacy staff, and ID fellows.
  • Prepares educational materials related to ASP and to appropriate antibiotic usage and monitoring for distribution to all institution personnel via Pharmacy newsletter.

ID fellows:

  • Present to medical residents at general orientation; do approvals for restricted antibiotic agents that provide another opportunity for education.

Pharmacy residents:

  • Required to participate in trainings, readings, and participatory events hosted by Pharmacy Department.


  • No data mining/data surveillance to identify patients who might benefit from intervention at this time; current process of reviewing broader sets of patients is very time consuming.

Pharmacy is on the IT list to develop needed queries for patient clinical information systems; level of priority unclear. Some queries have now been formulated that lay the groundwork for future additional needed lists or IT support. The team may not have all needed IT information.

PIP/TAZO: Hospital-wide restriction.
Cefepime: Hospital-wide (sites 4 and 5) audit and feedback and expanded focus in MICU (site 5) (de-escalation).
Details: Overall limited resources.
Interventions: ID MD, PharmD, and pharmacy residents (limited dedicated time for ASP activities); ongoing prior activities, including highly restrictive formulary, resulted in significant decrease in CDI rates.
How done:

  • Pharmacy residents play key role in ASP by conducting prospective audit of target antibiotics with feedback to prescribers; target drugs and antibiotics; review all patients. If difficulty is encountered or suggested intervention is rejected, referred for review to higher level. (i.e., stewardship team oversight).
  • Pharmacy residents divide stewardship activities by geographic site; residents may be site-specific.
  • Pharmacy residents' interaction with MDs generally positive; easier when rounding in person, more difficult to suggest intervention by phone; face-to-face interactions facilitate acceptance of recommendations.
  • Interactions depend on service, MDs, and how they round; walking rounds and sitting rounds have different processes, and topics or concerns are brought up differently.
  • Residents may make recommendations in different ways: while rounding, from office if not on rounds; recommendations may go directly to the medical resident. Residents may page the stewardship member overseeing if recommendations are not accepted. The stewardship team member may need to reach out to house staff or the teaching attending on behalf of the ASP to influence change in prescribing.
  • Much of ASP work involves looking at many patients receiving an antibiotic to find the specific patient where an intervention is possible; not being advanced electronically is work intensive and inefficient (despite partial electronic medical record).

Supporting activities:

  • Information technology support (for paper audit lists).
  • Review by antibiotic subcommittee of P&T committee.
  • Extensive educational programs and train-the-trainer sessions (pharmacy residents), extensive ID MD education/mentoring in ICUs.

Other stewardship activities during timeframe:

  • Implemented additional education for house staff.
  • Implemented requirement for indication for antibiotic orders.

Abbreviations: ASP = antimicrobial stewardship program; CDI = Clostridium difficile infection; CPOE = computerized physician order entry ED = emergency department; HCAP = hospital-acquired pneumonia; ID: infectious disease; IT = information technology; MICU = medical intensive care unit; P&T = pharmacy and therapeutics; PGY-1 = postgraduate year 1; PIP/TAZO = piperacillin/tazobactam; UTI = urinary tract infection.

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Page last reviewed August 2018
Page originally created June 2014
Internet Citation: Developing the Capacity to Implement Antimicrobial Stewardship: Opportunities for the Future. Content last reviewed August 2018. Agency for Healthcare Research and Quality, Rockville, MD.
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