Summary of Core Elements for Hospital Antibiotic Stewardship Programs

Though the primary goal of stewardship programs is to improve patient care, many studies have shown that they will pay for themselves, through savings in both antibiotic expenditures and indirect costs (7, 17).

Hospital Leadership Commitment

Support from the senior leadership of the hospital, especially the chief medical officer, chief nursing officer, and director of pharmacy, is critical to the success of antibiotic stewardship programs. A lack of necessary resources is commonly cited as the top barrier to success by stewardship programs. Hospital leadership can play a critical role in helping the stewardship program get the resources needed to accomplish its goals.

Priority examples of leadership commitment include:

  • Giving stewardship program leader(s) time to manage the program and conduct daily stewardship interventions.
  • Providing resources, including staffing, to operate the program effectively. Staffing suggestions for hospital antibiotic stewardship programs are available from the Veteran’s Administration (18) and a survey published in 2018 (19).
  • Having regular meetings with leaders of the stewardship program to assess the resources needed to accomplish the hospital’s goals for improving antibiotic use.
  • Appointing a senior executive leader to serve as a point of contact or “champion” for the stewardship program to help ensure that the program has resources and support to accomplish its mission.
  • Reporting stewardship activities and outcomes (including key success stories) to senior leadership and the hospital board on a regular basis (e.g. including stewardship measures in hospital quality dashboard reports).

Other examples of leadership commitment include:

  • Integrating antibiotic stewardship activities into other quality improvement and patient safety efforts, such as sepsis management and diagnostic stewardship.
  • Having clear expectations for the leaders of the program on responsibilities and outcomes.
  • Making formal statements of support for efforts to improve and monitor antibiotic use.
  • Outlining stewardship-related duties in job descriptions and annual performance reviews for program leads and key support staff.
  • Supporting training and education for program leaders (e.g. attendance of stewardship training courses and meetings) and hospital staff.
  • Supporting enrollment in and reporting to the National Healthcare Safety Network (NHSN) Antimicrobial Use and Resistance (AUR) Module (20), including information technology support.
  • Supporting participation in local, state, and national antibiotic stewardship quality improvement collaboratives.
  • Ensuring that staff from key support departments (outlined below) have sufficient time to contribute to stewardship activities.

Key Support

Hospital leadership can help ensure that other groups and departments in the hospital are aware of stewardship efforts and collaborate with the stewardship program. Stewardship programs are greatly enhanced by strong support from the following groups:

Clinicians: It is vital that all clinicians are fully engaged in and supportive of efforts to improve antibiotic use. Hospitalists are especially important to engage because they are one of the largest prescribers of antibiotics in hospitals. They also often have experience with quality improvement work (21, 22).

Department or program heads: Support from clinical department heads, as well as the director of pharmacy, is especially important in embedding stewardship activities in daily workflow.

Pharmacy and therapeutics committee can play a key role in helping to develop and implement policies that will improve antibiotic use (e.g. incorporating stewardship into order sets and clinical pathways). Some hospitals have created a multidisciplinary stewardship subcommittee of the Pharmacy and Therapeutics Committee.

Infection preventionists and hospital epidemiologists can assist with educating staff and with analyzing and reporting data on antibiotic resistance and C. difficile infection trends (23, 24). They can also support reporting to the NHSN AUR Module by updating monthly reporting plans, adding AUR users, and assisting with data upload.

Quality improvement, patient safety and regulatory staff can help advocate for adequate resources and integrate stewardship interventions into other quality improvement efforts, especially sepsis management. They might also be able to support implementation and outcome assessments.

Microbiology laboratory staff can:

  • Guide the proper use of tests and the flow of results as part of “diagnostic stewardship” (25).
  • Help optimize empiric antibiotic prescribing by creating and interpreting a facility cumulative antibiotic resistance report or antibiogram. Laboratory and stewardship personnel can work collaboratively to present data from lab reports in a way that supports optimal antibiotic use and is consistent with hospital guidelines.
  • Guide discussions on the potential implementation of rapid diagnostic tests and new antibacterial susceptibility test interpretive criteria (e.g., antibiotic breakpoints) that might impact antibiotic use. Microbiology labs and stewardship programs can work together to optimize the use of such tests and the communication of results.
  • Collaborate with stewardship program personnel to develop guidance for clinicians when changes in laboratory testing practices might impact clinical decision making (26).
  • Hospitals where microbiology services are contracted to an external organization should ensure that information is available to inform stewardship efforts.

Information technology staff are critical to integrating stewardship protocols into existing workflow. Some examples include:

  • Embedding relevant information and protocols at the point of care (e.g., order sets, access to facility-specific guidelines).
  • Implementing clinical decision support for antibiotic use and creating prompts for action to review antibiotics in key situations.
  • Facilitating and maintaining NHSN AUR reporting.

Nurses: There is growing recognition of the importance of engaging nurses in hospital stewardship efforts (27-29). Nurses can play an especially important role in:

  • Optimizing testing, or diagnostic stewardship. For example, nurses can inform decisions about whether or not a patient has symptoms that might justify a urine culture.
  • Assuring that cultures are performed correctly before starting antibiotics.
  • Prompting discussions of antibiotic treatment, indication, and duration.
  • Improving the evaluation of penicillin allergies.

Accountability

The antibiotic stewardship program must have a designated leader or co-leaders who are accountable for program management and outcomes. Most hospitals have found a co-leadership model to be effective, according to the 2019 NHSN hospital survey, 59% of hospitals in the United States have stewardship programs that are co-led by a physician and pharmacist. Effective leadership, management and communication skills are essential for the leaders of a hospital antibiotic stewardship program (30).

Programs with co-leaders should have a clear delineation of responsibilities and expectations. This can be especially important for physician leaders who do not work full time at the hospital. Antibiotic prescribing is ultimately under the direction of the medical staff. If a non-physician is the leader of the program, it is important that the hospital designate a physician who can serve as a point of contact and support for the non-physician program leader. Regular “stewardship rounds” for the co-leaders, or the non-physician lead and the supporting physician can strengthen program leadership. Expanding these rounds to include discussions with prescribers (also called “handshake stewardship”) has been shown to improve antibiotic use and is an effective way to enhance the visibility and support of the stewardship program (31, 32).

Training in infectious diseases and/or antibiotic stewardship benefits stewardship program leaders (2, 33). Larger facilities have achieved success by hiring full-time staff to develop and manage stewardship programs while smaller facilities report other arrangements, including use of part-time or even off-site expertise, sometimes referred to as tele-stewardship (34, 35). Hospitalists have also proven to be effective physician leaders or supporters for efforts to improve antibiotic use, especially in smaller hospitals, given their increasing presence in inpatient care, the frequency with which they use antibiotics and their experience with leading hospital quality improvement projects (21, 22).

5 ways hospital pharmacists can Be Antibiotics Aware.

Pharmacists: See Patient and Healthcare Provider Information for posters highlighting key stewardship interventions.

Pharmacy Expertise

Highly effective hospital antibiotic stewardship programs have strong engagement of pharmacists, either as a leader or co-leader of the program (36, 37). It is important to identify a pharmacist who is empowered to lead implementation efforts to improve antibiotic use. Infectious diseases trained pharmacists are highly effective in improving antibiotic use and often help lead programs in larger hospitals and healthcare systems (38, 39).

In hospitals without infectious disease trained pharmacists, general clinical pharmacists are often co-leaders or pharmacy leaders. General clinical pharmacists are more effective when they have specific training and/or experience in antibiotic stewardship.

There are a variety of resources to support the antibiotic stewardship efforts of clinical pharmacists, ranging from posters highlighting key stewardship interventions for pharmacists (40) to formal training and certificate programs in stewardship for pharmacists.

Action

Antibiotic stewardship interventions improve patient outcomes (7, 9). An initial assessment of antibiotic prescribing can help identify potential targets for interventions.

Priority Interventions to Improve Antibiotic Use

Stewardship programs should choose interventions that will best address gaps in antibiotic prescribing and consider prioritizing prospective audit and feedback, preauthorization and facility-specific treatment guidelines.

Published evidence demonstrates that prospective audit and feedback (sometimes called post-prescription review) and preauthorization are the two most effective antibiotic stewardship interventions in hospitals (16). They are both strongly recommended in evidenced-based guidelines and can be considered “foundational” interventions for hospital stewardship programs.

Prospective audit and feedback is an external review of antibiotic therapy by an expert in antibiotic use, accompanied by suggestions to optimize use, at some point after the agent has been prescribed (16). Prospective audit and feedback is different from an antibiotic “timeout” because the stewardship program rather than the treating team conducts the audits.

Audit and feedback can be implemented in a variety of ways, depending on the level of expertise available. Stewardship programs with limited infectious diseases expertise might choose to focus reviews on comparing prescribed treatment courses to recommendations in hospital specific treatment guidelines and focus on common conditions, such as community-acquired pneumonia, urinary tract infection, or skin and soft tissue infection. Programs with more advanced infectious diseases expertise might elect to review more complex antibiotic treatment courses.

The effectiveness of prospective audit with feedback can be enhanced by providing feedback in face-to-face meetings with providers, referred to as “handshake stewardship” (32) (41).

Preauthorization requires prescribers to gain approval prior to the use of certain antibiotics. This can help optimize initial empiric therapy because it allows for expert input on antibiotic selection and dosing, which can be lifesaving in serious infections, like sepsis. It can also prevent unnecessary initiation of antibiotics (42).

Decisions on which antibiotics to place under preauthorization should be made in consultation with providers to focus on opportunities to improve empiric use, rather than on drug costs (43). This intervention requires the availability of expertise and staff who can complete authorizations in a timely manner (44). Hospitals can tailor the agents, situations, and mechanisms (e.g. preauthorization through an electronic order entry system) to implement preauthorization based on program goals, available expertise, and resources in a way that does not delay therapy for serious infections. Stewardship programs should monitor potential unintended consequences of preauthorization, especially treatment delays.

Two studies have compared these two interventions directly and found prospective audit and feedback to be more effective than preauthorization (42, 44). However, many experts suggest that these interventions should both be priorities for implementation since preauthorization can help optimize initiation of antibiotics and prospective audit and feedback can help optimize continued therapy. Hospitals can use local data and knowledge of practices to determine which antibiotics should be subject to prospective audit and feedback and/or preauthorization.

Facility specific treatment guidelines are also considered a priority because they can greatly enhance the effectiveness of both prospective audit and feedback and preauthorization by establishing clear recommendations for optimal antibiotic use at the hospital. These guidelines can optimize antibiotic selection and duration, particularly for common indications for antibiotic use like community-acquired pneumonia, urinary tract infection, intra-abdominal infection, skin and soft tissue infection and surgical prophylaxis. Recommendations may be based on national guidelines but should reflect hospital treatment preferences based on local susceptibilities, formulary options, and patient mix.

Ideally, the recommendations should also address diagnostic approaches, such as when to send diagnostic samples and what tests to perform, including indications for rapid diagnostics and non-microbiologic tests (e.g. imaging, procalcitonin). The development of treatment guidelines is a good way for the stewardship program to engage prescriber stakeholders to develop consensus on antibiotic use.

Hospital guidelines can also facilitate prospective audit with feedback and preauthorization as prescriptions and/or requests for antibiotics can be compared to hospital recommendations. Stewardship programs can prioritize the development of guidelines based on the infections most commonly encountered. Adherence to hospital guidelines can be enhanced by embedding treatment recommendations in order sets and clinical pathways.

Common Infection-based Interventions

More than half of all antibiotics given to treat active infections in hospitals are prescribed for three infections where there are important opportunities to improve use: lower respiratory tract infection (e.g. community acquired pneumonia), urinary tract infection and skin and soft tissue infection (45). Optimizing the duration of therapy can be especially important because many studies show infections are often treated for longer than guidelines recommend and data demonstrate that each additional day of antibiotics increases the risk of patient harm (4, 46). Examples of interventions are below and summarized in Table 1.

Community-acquired pneumonia: Interventions have focused on:

  • Improving diagnostic accuracy
  • Tailoring of therapy to culture results
  • Optimizing the duration of treatment to ensure compliance with guidelines

The use of viral diagnostics and/or procalcitonin might help identify patients in whom antibiotics can be stopped because bacterial pneumonia is unlikely (47). Optimizing the duration of therapy at hospital discharge is especially important as most excess antibiotic use in the treatment of community-acquired pneumonia occurs after discharge (48, 49) .

Urinary tract infection (UTI): Many patients who are prescribed antibiotics for UTIs have asymptomatic bacteriuria that generally does not need to be treated. Successful stewardship interventions focus on avoiding obtaining unnecessary urine cultures and avoiding treatment of patients who are asymptomatic, unless there are specific reasons to treat (50). For patients who need treatment, interventions can focus on ensuring patients receive appropriate therapy based on local susceptibilities for the recommended duration (51).

Skin and soft tissue infection: Interventions have focused on ensuring patients with uncomplicated infections do not receive antibiotics with overly broad spectra (e.g. unnecessary coverage for methicillin-resistant Staphylococcus aureus (MRSA) and gram-negative pathogens) and prescribing the correct route, dosage and duration of treatment (52, 53).

Table 1. Key Opportunities to Improve Antibiotic Use

CAPTION
Condition Diagnostic Considerations Empiric Therapy Definitive Therapy
Tailor to culture results and define
duration, including discharge prescription.
Community-acquired pneumonia(54) Review cases after initiation of therapy to confirm pneumonia diagnosis versus non-infectious etiology. Avoid empiric use of antipseudomonal beta-lactams and/or MRSA agents unless clinically indicated. Guidelines suggest that in adults, most cases of uncomplicated pneumonia can be treated for 5 days when a patient has a timely clinical response (55, 56).

Data also suggest that negative results of MRSA nasal colonization testing can help guide decisions to discontinue empiric therapy for MRSA pneumonia (57).

Urinary tract infection (UTI) Implement criteria for ordering urine cultures to ensure that positive cultures are more likely to represent infection than bladder colonization (58).

Examples include:

  • Order a urine culture only if the patient has signs and symptoms consistent with UTI such as urgency, frequency, dysuria, suprapubic pain, flank pain, pelvic discomfort or acute hematuria.

For patients with urinary catheters, avoid obtaining urine cultures based solely on cloudy appearance or foul smell in the absence of signs and symptoms of UTI. Nonspecific signs and symptoms such as delirium, nausea and vomiting should be interpreted with caution as, by themselves, they have a low specificity for UTI.

Establish criteria to distinguish between asymptomatic and symptomatic bacteriuria.

Avoid antibiotic therapy for asymptomatic bacteriuria except in certain clinical situations where treatment is indicated, such as for pregnant women and those undergoing an invasive genitourinary procedure.

Use the shortest duration of antibiotic therapy that is clinically appropriate.
Skin and soft tissue infection Develop diagnostic criteria to distinguish purulent and non-purulent infections and severity of illness (i.e., mild, moderate and severe) so that skin and soft tissue infections can be managed appropriately according to guidelines. Avoid empiric use of antipseudomonal beta-lactams and/or anti-anaerobic agents unless clinically indicated.

Use of therapy specific for MRSA may not be necessary in uncomplicated non-purulent cellulitis (53).

Guidelines suggest that most cases of uncomplicated bacterial cellulitis can be treated for 5 days if the patient has a timely clinical response (53).

Other Infection-based Interventions

Sepsis: Early administration of effective antibiotics is lifesaving in sepsis. Antibiotic stewardship programs should work with sepsis experts in the hospital, along with the pharmacy and microbiology lab, to optimize the treatment of sepsis. Important issues to address are:

  • Developing antibiotic recommendations for sepsis that are based on local microbiology data.
  • Ensuring protocols are in place to administer antibiotics quickly in cases of suspected sepsis.
  • Ensuring there are mechanisms in place to review antibiotics started for suspected sepsis so that therapy can be tailored or stopped if deemed unnecessary.

Staphylococcus aureus infection: In many cases, therapy for MRSA can be stopped if the patient does not have an MRSA infection or changed to a beta-lactam if the cause is MRSA. Studies have also shown that treatment protocols and, where available, infectious diseases consultation, can improve outcomes in patients with S. aureus bloodstream infections (59, 60).

C. difficile infection: Treatment guidelines recommend providers stop unnecessary antibiotics in all patients diagnosed with C. difficile infection. Reviewing antibiotics in patients with new diagnoses of C. difficile infection can identify opportunities to stop unnecessary antibiotics, which improves the clinical response of these infections to treatment and reduces the risk of recurrence (61-63). Stewardship programs can also make sure that patients are receiving guideline recommended therapy for their C. difficile infection (64).

Culture proven invasive infection: Invasive infections (e.g. blood stream infections) present opportunities for interventions to improve antibiotic use because they are easily identified from microbiology results and sub-optimal therapy often leads to worse outcomes. Prospective audit and feedback of new culture or rapid diagnostic results may be particularly beneficial to reduce the time needed to discontinue, narrow, or broaden antibiotic therapy as appropriate.

Review of planned outpatient parenteral antibiotic therapy (OPAT): In some cases, OPAT can be optimized or even avoided altogether following a review by the antibiotic stewardship program (65).

Provider-based Interventions

Antibiotic “timeouts”: Antibiotics are commonly started empirically in hospitalized patients. However, providers often do not revisit the selection of the antibiotic after more data (including culture results) become available. An antibiotic timeout is a provider-led reassessment of the continuing need and choice of antibiotics when the clinical picture is clearer and more diagnostic information, especially results of cultures and rapid diagnostics, is available.

Antibiotic timeouts are different from prospective audit and feedback because the providers, not the stewardship team, are doing the reviews. A trial demonstrated that antibiotic timeouts at 48-72 hours of therapy improved the appropriateness of antibiotic selection, but did not reduce overall antibiotic use (66). Antibiotic timeouts are a useful supplemental intervention but should not be considered a substitute for prospective audit and feedback by the stewardship program.

The optimal timing of antibiotic timeouts has not been established. Experts suggest that daily reviews of antibiotic selection, until a definitive diagnosis and treatment duration are established, can optimize treatment. Provider-led reviews of antibiotics can focus on four key questions (67):

  • Does this patient have an infection that will respond to antibiotics?
  • Have proper cultures and diagnostic tests been performed?
  • Can antibiotics be stopped or improved by narrowing the spectrum (also referred to as “de-escalation”) or changing from intravenous to oral?
  • How long should the patient receive the antibiotic(s), considering both the hospital stay and any post-discharge therapy?

Assessing penicillin allergy: About 15% of hospitalized patients report an allergy to penicillin (68). However, less than 1% of the US population has a serious penicillin allergy that would preclude treatment with a beta lactam antibiotic (69). There are several effective approaches to properly assess penicillin allergies, including history and physical examination, challenge doses, and skin testing (69, 71). Nurses may be able to play an important role in improving penicillin allergy assessments (27).

Pharmacy-based Interventions

The following interventions are often initiated by pharmacists and/or embedded into pharmacy sections of electronic health records:

  • Documentation of indications for antibiotics: Requiring an indication for antibiotic prescriptions can facilitate other interventions, like prospective audit and feedback and optimizing post-discharge durations of therapy, and, in and of itself, can improve antibiotic use (72).
  • Automatic changes from intravenous to oral antibiotic therapy: This change can improve patient safety by reducing the need for intravenous access in appropriate situations and for antibiotics with good absorption.
  • Dose adjustments: when needed, such as in cases of organ dysfunction, especially renal, or based on therapeutic drug monitoring.
  • Dose optimization: for example, extended-infusion administration of beta-lactams, particularly for patients who are critically-ill and patients infected with drug-resistant pathogens.
  • Duplicative therapy alerts: Alerts in situations where therapy might be unnecessarily duplicative including simultaneous use of multiple agents with overlapping spectra (e.g. anaerobic activity and resistant Gram-positive activity) (73, 74).
  • Time-sensitive automatic stop orders: for specified antibiotic prescriptions, especially antibiotics administered for surgical prophylaxis.
  • Detection and prevention of antibiotic-related drug-drug interactions: for example, interactions between some orally administered fluoroquinolones and certain vitamins.

Microbiology-based Interventions

The microbiology lab in consultation with the stewardship program often implement the following interventions:

  • Selective reporting of antimicrobial susceptibility testing results: tailoring hospital susceptibility reports to show antibiotics that are consistent with hospital treatment guidelines or recommended by the stewardship program (75) (76).
  • Comments in microbiology reports: for example, to help providers know which pathogens might represent colonization or contamination (77).

Nursing-based interventions

Bedside nurses often initiate the following interventions:

  • Optimizing microbiology cultures: Knowing proper techniques to reduce contamination and indications for when to obtain cultures, especially urine cultures (27).
  • Intravenous to oral transitions: Nurses are most aware of when patients are able to tolerate oral medications and can initiate discussions on switching to oral antibiotics.
  • Prompting antibiotic reviews (“timeouts”): Nurses often know how long a patient has been receiving an antibiotic and when laboratory results become available. They can play a key role in prompting reevaluations of therapy at specified times, such as after 2 days of treatment and/or when culture results are available (29).

Tracking

Measurement is critical to identify opportunities for improvement and to assess the impact of interventions. Measurement of antibiotic stewardship interventions may involve evaluation of both processes and outcomes. For example, a program will need to evaluate if policies and guidelines are being followed as expected (processes) and if interventions have improved patient outcomes and antibiotic use (outcomes).

Antibiotic Use Measures

It is important for hospitals to monitor and benchmark antibiotic use by electronically reporting to the National Healthcare Safety Network (NHSN) Antimicrobial Use (AU) Option. The NHSN AU Option is available to hospitals that have information system capability to submit electronic medication administration records (eMAR) and/or bar-coding medication administration records (BCMA) using an HL7 standardized clinical document architecture (20).

There are a variety of health information technology companies that can facilitate the reporting of antibiotic use data to the AU Option (78). Stewardship programs can work with their information technology staff to explore options for reporting data to the AU Option. Enrolling hospitals in the NHSN AU Option was a priority goal set forth in the National Strategy for Combating Antibiotic-Resistant Bacteria and by the President’s Advisory Committee on Combating Antibiotic Resistant Bacteria (79).

The NHSN AU Option provides rates of antibiotic use expressed as days of therapy (DOTs) per days present for nearly all antibiotics for individual inpatient care locations, select outpatient care locations (e.g. emergency department and observation units), and for the entire hospital. Days of therapy are the sum of days for which any amount of a specific antibiotic agent is administered to a patient.

The AU Option also provides a risk-adjusted benchmark of antibiotic use referred to as the Standardized Antimicrobial Administration Ratio or “SAAR”. Benchmarking has proven to be a powerful tool in hospital quality improvement and was a top priority for stewardship experts who advised CDC on the development of the NHSN AU Option. The SAAR compares observed antibiotic use to predicted use, where use is predicted based on risk adjust models of data submitted to the NHSN AU Option (80). SAARs were developed for a variety of groups of antibiotics for both adult, pediatric and neonatal care locations in response to suggestions from stewardship experts on the types of data that would be most actionable (20). Stewardship programs are using the NHSN AU Option to both inform and assess interventions (81-83).

Hospitals that are not yet reporting to the NHSN AU Option can often get antibiotic use data from their pharmacy record systems, usually either as days of therapy or as defined daily doses (DDDs). The DDD estimates antibiotic use in hospitals by aggregating the total number of grams of each antibiotic purchased, ordered, dispensed, or administered during a period of interest divided by the World Health Organization-assigned DDD (84). United States guidelines recommend the use of days of therapy rather than DDDs as the preferred numerator metric for hospital antibiotic use (16).

Outcome measures

C. difficile  infections are an important target for stewardship programs, given the evidence that improved antibiotic use can prevent these infections (85, 86). Most acute care hospitals are already monitoring and reporting information on C. difficile infection to NHSN as part of payment programs for CMS and/or for state requirements. C. difficile infection prevention is multifaceted and creates an opportunity for stewardship programs to collaborate with other groups, such as the laboratory and infection prevention.

Antibiotic Resistance. Improving antibiotic use is important to reduce antibiotic resistance and presents another option for measurement. The development and spread of antibiotic resistance is multi-factorial and studies assessing the impact of improved antibiotic use on resistance rates have shown mixed results (7, 87, 88). The impact of stewardship interventions on resistance is best assessed when measurement is focused on pathogens that are recovered from patients after admission when they are under the influence of hospital stewardship interventions (16). Monitoring resistance at the patient level (i.e. what percent of patients develop resistant super-infections) has also been shown to be useful. Hospitals can also track antibiotic resistance though the NHSN Antimicrobial Resistance (AR) Option (20).

Financial Impact. Stewardship programs can achieve significant cost savings, particularly drug cost savings. (89, 90). Costs should not be the primary outcome measure of a program’s success; but demonstrating savings can be helpful in obtaining resources for antibiotic stewardship programs. If hospitals monitor antibiotic costs, they should assess the pace at which antibiotic costs were rising before the start of the stewardship program (91). After an initial period of marked savings, costs often stabilize. However, it is important to continue support for stewardship programs since costs can increase if programs are terminated (17).

Process Measures for Quality Improvement

Process measures can focus on the specific interventions being implemented at the hospital. Priority process measures include:

  • Tracking the types and acceptance of recommendations from prospective audit and feedback interventions, which can identify areas where more education or additional focused interventions might be useful.
  • Monitoring of preauthorization interventions by tracking agents that are being requested for certain conditions and ensuring that preauthorization is not creating delays in therapy.
  • Monitoring adherence to facility-specific treatment guidelines. If feasible, consider tracking adherence by each prescriber.

Additional process measures for quality improvement include:

  • Monitoring the performance of antibiotic timeouts to assess how often they are preformed and if opportunities to improve use are being identified and acted on.
  • Performing a medication use evaluation to assess courses of therapy for select antibiotics or infections to identify opportunities to improve use. Standardized tools or antibiotic audit forms can assist in these reviews (92) (76).
  • Monitoring how often patients are converted from intravenous to oral therapy to identify missed opportunities to convert.
  • Assessing how often patients are prescribed unnecessary duplicate therapy, for example if a patient is prescribed two antibiotics to treat anaerobes.
  • Assessing how often patients are discharged on the correct antibiotics for the recommended duration.

Reporting

Antibiotic stewardship programs should provide regular updates to prescribers, pharmacists, nurses, and leadership on process and outcome measures that address both national and local issues, including antibiotic resistance. Antibiotic resistance information should be prepared in collaboration with the hospital’s microbiology lab and infection control and healthcare epidemiology department. The local or state health department’s healthcare infection control and antibiotic resistance program is also an important resource for local information on antibiotic resistant threats (93). Summary information on antibiotic use and resistance along with antibiotic stewardship program work should be shared regularly with hospital leadership and the hospital board.

Findings from medication use evaluations along with summaries of key issues that arise during prospective audit and feedback reviews and preauthorization requests can be especially useful to share with prescribers. Sharing facility-specific information on antibiotic use is a tool to motivate improved prescribing, particularly if wide variations in the patterns of use exist among similar patient care locations (94). Provider specific reports with peer comparisons have been effective in improving antibiotic use in outpatient settings (95), but there is limited experience with these reports for hospital-based providers.

Education

Education is a key component of comprehensive efforts to improve hospital antibiotic use; however, education alone is not an effective stewardship intervention (16). There are many options for providing education on antibiotic use such as didactic presentations, which can be done in formal and informal settings, messaging through posters, flyers and newsletters, or electronic communication to staff groups.

Free continuing education Training on Antibiotic Stewardship

CDC has a variety of educational resources, including a Training on Antibiotic Stewardship that includes a module focused on improving antibiotic use in hospitals (96).

Education is most effective when paired with interventions and measurement of outcomes. Case-based education can be especially powerful, so prospective audit with feedback and preauthorization are both good methods to provide education on antibiotic use. This can be especially effective when the feedback is provided in person, for example through handshake stewardship. Some hospitals review de-identified cases with providers to help identify changes in antibiotic therapy that could have been made. Education is most effective when tailored to the action(s) most relevant to the provider group, such as education on community acquired pneumonia guidelines for hospitalists or education on culture techniques for nurses. There are also a variety of educational materials on hospital antibiotic use and stewardship available from the Agency for Healthcare Research and Quality’s Safety Program for Improving Antibiotic Use (97). patient education efforts. They should be engaged in developing educational materials and educating patients about appropriate antibiotic use.

Be Antibiotics Aware: Smart Use, Best Care

CDC’s national campaign, Be Antibiotics Aware, helps healthcare providers educate their patients about appropriate antibiotic use. Handouts include You’ve Been Prescribed an Antibiotic in the Hospital for an Infection pdf icon[PDF – 2 pages].

Patient education is also an important focus for antibiotic stewardship programs. It is important for patients to know what antibiotics they are receiving and for what reason(s). They should also be educated about adverse effects and signs and symptoms that they should share with providers. Patients should be alerted to side effects that may occur after they have been discharged and even after they have stopped taking antibiotics. Engaging patients in the development and review of educational materials can make these items more effective. Nurses are an especially important partner for patient education efforts. They should be engaged in developing educational materials and educating patients about appropriate antibiotic use.

References

  1. Rhodes A, Evans LE, Alhazzani W, Levy MM, Antonelli M, Ferrer R, et al. Surviving Sepsis Campaign: International Guidelines for Management of Sepsis and Septic Shock: 2016. Intensive care medicine. 2017 Mar;43(3):304-77.
  2. Dellit TH, Owens RC, McGowan JE, Jr., Gerding DN, Weinstein RA, Burke JP, et al. Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America guidelines for developing an institutional program to enhance antimicrobial stewardship. Clin Infect Dis. 2007 Jan 15;44(2):159-77.
  3. Fridkin SK, Baggs J., Fagan R., Magill S., Pollack L.A., Malpiedi P., Slayton R. Vital Signs: Improving Antibiotic Use Among Hospitalized Patients. MMWR Morb Mortal Wkly Rep. 2014;63(9):194-200.
  4. Tamma PD, Avdic E, Li DX, Dzintars K, Cosgrove SE. Association of Adverse Events With Antibiotic Use in Hospitalized Patients. JAMA Intern Med. 2017 Sep 1;177(9):1308-15.
  5. Huttner A, Harbarth S, Carlet J, Cosgrove S, Goossens H, Holmes A, et al. Antimicrobial resistance: a global view from the 2013 World Healthcare-Associated Infections Forum. Antimicrobial resistance and infection control. 2013 Nov 18;2(1):31.
  6. Brown K, Valenta K, Fisman D, Simor A, Daneman N. Hospital ward antibiotic prescribing and the risks of Clostridium difficile infection. JAMA Intern Med. 2015 Apr;175(4):626-33.
  7. Davey P, Marwick CA, Scott CL, Charani E, McNeil K, Brown E, et al. Interventions to improve antibiotic prescribing practices for hospital inpatients. The Cochrane database of systematic reviews. 2017 Feb 9;2:Cd003543.
  8. Karanika S, Paudel S, Grigoras C, Kalbasi A, Mylonakis E. Systematic Review and Meta-analysis of Clinical and Economic Outcomes from the Implementation of Hospital-Based Antimicrobial Stewardship Programs. Antimicrobial agents and chemotherapy. 2016 Aug;60(8):4840-52.
  9. Baur D, Gladstone BP, Burkert F, Carrara E, Foschi F, Dobele S, et al. Effect of antibiotic stewardship on the incidence of infection and colonisation with antibiotic-resistant bacteria and Clostridium difficile infection: a systematic review and meta-analysis. The Lancet Infectious diseases. 2017 Sep;17(9):990-1001.
  10. Centers for Disease Control and Prevention. U.S. National Action Plan for Combating Antibiotic-Resistant Bacteria (National Action Plan). Available from: https://www.cdc.gov/drugresistance/us-activities/national-action-plan.html
  11. National Quality Forum. National Quality Partners Playbook: Antibiotic Stewardship in Acute Careexternal icon. Available from: http://www.qualityforum.org/NQP/Antibiotic_Stewardship_Playbook.aspx
  12. Centers for Disease Control and Prevention. Implementation of Antibiotic Stewardship Core Elements at Small and Critical Access Hospitals. Available from: https://www.cdc.gov/antibiotic-use/core-elements/small-critical.html
  13. DNV-GL. National Integrated Accreditation for Healthcare Organizations (NIAHO®) DNV [PDF – 238 pages]external icon. Available from: http://bit.ly/DNVGLNIAHOAcute#page=150
  14. Centers for Medicare and Medicaid Services. Medicare and Medicaid Programs; Regulatory Provisions To Promote Program Efficiency, Transparency, and Burden Reduction; Fire Safety Requirements for Certain Dialysis Facilities; Hospital and Critical Access Hospital (CAH) Changes To Promote Innovation, Flexibility, and Improvement in Patient Careexternal icon. Available from: https://www.federalregister.gov/documents/2019/09/30/2019-20736/medicare-and-medicaid-programs-regulatory-provisions-to-promote-program-efficiency-transparency-and
  15. Centers for Disease Control and Prevention. CDC Patient Safety Portal.
  16. Barlam TF, Cosgrove SE, Abbo LM, MacDougall C, Schuetz AN, Septimus EJ, et al. Implementing an Antibiotic Stewardship Program: Guidelines by the Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America. Clin Infect Dis. 2016 May 15;62(10):e51-77.
  17. Standiford HC, Chan S, Tripoli M, Weekes E, Forrest GN. Antimicrobial stewardship at a large tertiary care academic medical center: cost analysis before, during, and after a 7-year program. Infection control and hospital epidemiology : the official journal of the Society of Hospital Epidemiologists of America. 2012 Apr;33(4):338-45.
  18. Department of Veterans Affairs. VHA Directive 1031 Antimicrobial Stewardship Programs (ASP) [PDF – 12 pages]external icon. Available from: https://www.va.gov/vhapublications/ViewPublication.asp?pub_ID=8195
  19. Doernberg SB, Abbo LM, Burdette SD, Fishman NO, Goodman EL, Kravitz GR, et al. Essential Resources and Strategies for Antibiotic Stewardship Programs in the Acute Care Setting. Clin Infect Dis. 2018 Sep 28;67(8):1168-74.
  20. Centers for Disease Control and Prevention. Surveillance for Antimicrobial Use and Antimicrobial Resistance Options. Available from: https://www.cdc.gov/nhsn/acute-care-hospital/aur/index.html
  21. Rohde JM, Jacobsen D, Rosenberg DJ. Role of the Hospitalist in Antimicrobial Stewardship: A Review of Work Completed and Description of a Multisite Collaborative. Clinical therapeutics. 2013 Jun 5.
  22. Srinivasan A. Engaging hospitalists in antimicrobial stewardship: the CDC perspective. Journal of hospital medicine : an official publication of the Society of Hospital Medicine. 2011 Jan;6 Suppl 1:S31-3.
  23. Manning ML, Septimus EJ, Ashley ESD, Cosgrove SE, Fakih MG, Schweon SJ, et al. Antimicrobial stewardship and infection prevention-leveraging the synergy: A position paper update. American journal of infection control. 2018 Apr;46(4):364-8.
  24. Moody J, Cosgrove SE, Olmsted R, Septimus E, Aureden K, Oriola S, et al. Antimicrobial stewardship: a collaborative partnership between infection preventionists and health care epidemiologists. American journal of infection control. 2012 Mar;40(2):94-5.
  25. Morgan DJ, Malani P, Diekema DJ. Diagnostic Stewardship—Leveraging the Laboratory to Improve Antimicrobial Use. JAMA. 2017;318(7):607-8.
  26. Timbrook TT, Morton JB, McConeghy KW, Caffrey AR, Mylonakis E, LaPlante KL. The effect of molecular rapid diagnostic testing on clinical outcomes in bloodstream infections: A systematic review and meta-analysis. Clinical Infectious Diseases. 2017;64(1):15-23.
  27. Centers for Disease Control and Prevention and The American Nurses Association. Redefining the Antibiotic Stewardship Team: Recommendations from the American Nurses Association/Centers for Disease Control and Prevention Workgroup on the Role of Registered Nurses in Hospital Antibiotic Stewardship Practices pdf iconpdf icon[PDF – 14 pages]. Available from: https://www.cdc.gov/antibiotic-use/healthcare/pdfs/ANA-CDC-whitepaper.pdf
  28. Edwards R, Drumright L, Kiernan M, Holmes A. Covering more Territory to Fight Resistance: Considering Nurses’ Role in Antimicrobial Stewardship. Journal of infection prevention. 2011 Jan;12(1):6-10.
  29. Olans RN, Olans RD, DeMaria A, Jr. The Critical Role of the Staff Nurse in Antimicrobial Stewardship–Unrecognized, but Already There. Clin Infect Dis. 2016 Jan 1;62(1):84-9.
  30. Cosgrove SE, Hermsen ED, Rybak MJ, File TM, Jr., Parker SK, Barlam TF. Guidance for the knowledge and skills required for antimicrobial stewardship leaders. Infection control and hospital epidemiology : the official journal of the Society of Hospital Epidemiologists of America. 2014 Dec;35(12):1444-51.
  31. Baker DW, Hyun D, Neuhauser MM, Bhatt J, Srinivasan A. Leading Practices in Antimicrobial Stewardship: Conference Summary. Joint Commission journal on quality and patient safety. 2019 Jul;45(7):517-23.
  32. Hurst AL, Child J, Pearce K, Palmer C, Todd JK, Parker SK. Handshake Stewardship: A Highly Effective Rounding-based Antimicrobial Optimization Service. 2016;35(10):1104-10.
  33. Graber CJ, Jones MM, Chou AF, Zhang Y, Goetz MB, Madaras-Kelly K, et al. Association of Inpatient Antimicrobial Utilization Measures with Antimicrobial Stewardship Activities and Facility Characteristics of Veterans Affairs Medical Centers. Journal of hospital medicine : an official publication of the Society of Hospital Medicine. 2017 May;12(5):301-9.
  34. Stenehjem E, Hersh AL, Buckel WR, Jones P, Sheng X, Evans RS, et al. Impact of Implementing Antibiotic Stewardship Programs in 15 Small Hospitals: A Cluster-Randomized Intervention. Clinical Infectious Diseases. 2018;67(4):525-32.
  35. Wilson BM, Banks RE, Crnich CJ, Ide E, Viau RA, El Chakhtoura NG, et al. Changes in antibiotic use following implementation of a telehealth stewardship pilot program. Infection control and hospital epidemiology : the official journal of the Society of Hospital Epidemiologists of America. 2019 Jul;40(7):810-4.
  36. Heil EL, Kuti JL, Bearden DT, Gallagher JC. The Essential Role of Pharmacists in Antimicrobial Stewardship. Infection control and hospital epidemiology : the official journal of the Society of Hospital Epidemiologists of America. 2016 Jul;37(7):753-4.
  37. Kelly AA, Jones MM, Echevarria KL, Kralovic SM, Samore MH, Goetz MB, et al. A Report of the Efforts of the Veterans Health Administration National Antimicrobial Stewardship Initiative. Infection control and hospital epidemiology : the official journal of the Society of Hospital Epidemiologists of America. 2017 May;38(5):513-20.
  38. Bessesen MT, Ma A, Clegg D, Fugit RV, Pepe A, Goetz MB, et al. Antimicrobial Stewardship Programs: Comparison of a Program with Infectious Diseases Pharmacist Support to a Program with a Geographic Pharmacist Staffing Model. Hospital pharmacy. 2015 Jun;50(6):477-83.
  39. Yu K, Rho J, Morcos M, Nomura J, Kaplan D, Sakamoto K, et al. Evaluation of dedicated infectious diseases pharmacists on antimicrobial stewardship teams. American journal of health-system pharmacy: AJHP: official journal of the American Society of Health-System Pharmacists. 2014 Jun 15;71(12):1019-28.
  40. Centers for Disease Control and Prevention. Five Ways Pharmacists Can Be Antibiotics Aware pdf iconpdf icon[PDF – 1 page]. Available from: https://www.cdc.gov/antibiotic-use/community/pdfs/Hospital-Pharmacist-Poster-508.pdf
  41. MacBrayne CE, Williams MC, Levek C, Child J, Pearce K, Birkholz M, et al. Sustainability of Handshake Stewardship: Extending a Hand Is Effective Years Later. Clin Infect Dis. 2019 Oct 4.
  42. Tamma PD, Avdic E, Keenan JF, Zhao Y, Anand G, Cooper J, et al. What Is the More Effective Antibiotic Stewardship Intervention: Preprescription Authorization or Postprescription Review With Feedback? Clin Infect Dis. 2017 Mar 1;64(5):537-43.
  43. Athans V, Santarossa M, Kenney RM, Davis SL. Systematic approach to antimicrobial restriction. American journal of health-system pharmacy : AJHP : official journal of the American Society of Health-System Pharmacists. 2015 Aug 1;72(15):1264-5.
  44. Anderson DJ, Watson S, Moehring RW, Komarow L, Finnemeyer M, Arias RM, et al. Feasibility of Core Antimicrobial Stewardship Interventions in Community Hospitals. JAMA Network Open. 2019;2(8):e199369-e.
  45. Magill SS, Edwards JR, Beldavs ZG, Dumyati G, Janelle SJ, Kainer MA, et al. Prevalence of antimicrobial use in US acute care hospitals, May-September 2011. Jama. 2014 Oct 8;312(14):1438-46.
  46. Branch-Elliman W, O’Brien W, Strymish J, Itani K, Wyatt C, Gupta K. Association of Duration and Type of Surgical Prophylaxis With Antimicrobial-Associated Adverse Events. JAMA Surgery. 2019;154(7):590-8.
  47. Branche AR, Walsh EE, Vargas R, Hulbert B, Formica MA, Baran A, et al. Serum Procalcitonin Measurement and Viral Testing to Guide Antibiotic Use for Respiratory Infections in Hospitalized Adults: A Randomized Controlled Trial. The Journal of infectious diseases. 2015 Dec 1;212(11):1692-700.
  48. Vaughn VM, Flanders SA, Snyder A, Conlon A, Rogers MAM, Malani AN, et al. Excess Antibiotic Treatment Duration and Adverse Events in Patients Hospitalized With Pneumonia: A Multihospital Cohort Study. Annals of internal medicine. 2019 Aug 6;171(3):153-63.
  49. Madaras-Kelly KJ, Burk M, Caplinger C, Bohan JG, Neuhauser MM, Goetz MB, et al. Total duration of antimicrobial therapy in veterans hospitalized with uncomplicated pneumonia: Results of a national medication utilization evaluation. Journal of hospital medicine : an official publication of the Society of Hospital Medicine. 2016 Dec;11(12):832-9.
  50. Trautner BW, Grigoryan L, Petersen NJ, Hysong S, Cadena J, Patterson JE, et al. Effectiveness of an Antimicrobial Stewardship Approach for Urinary Catheter-Associated Asymptomatic Bacteriuria. JAMA Intern Med. 2015 Jul;175(7):1120-7.
  51. Slekovec C, Leroy J, Vernaz-Hegi N, Faller JP, Sekri D, Hoen B, et al. Impact of a region wide antimicrobial stewardship guideline on urinary tract infection prescription patterns. International journal of clinical pharmacy. 2012 Apr;34(2):325-9.
  52. Jenkins TC, Knepper BC, Sabel AL, Sarcone EE, Long JA, Haukoos JS, et al. Decreased antibiotic utilization after implementation of a guideline for inpatient cellulitis and cutaneous abscess. Archives of internal medicine. 2011 Jun 27;171(12):1072-9.
  53. Stevens DL, Bisno AL, Chambers HF, Dellinger EP, Goldstein EJC, Gorbach SL, et al. Practice Guidelines for the Diagnosis and Management of Skin and Soft Tissue Infections: 2014 Update by the Infectious Diseases Society of America. Clinical Infectious Diseases. 2014;59(2):e10-e52.
  54. Metlay JP, Waterer GW, Long AC, Anzueto A, Brozek J, Crothers K, et al. Diagnosis and Treatment of Adults with Community-acquired Pneumonia. An Official Clinical Practice Guideline of the American Thoracic Society and Infectious Diseases Society of America. American journal of respiratory and critical care medicine. 2019 Oct 1;200(7):e45-e67.
  55. McCabe C, Kirchner C, Zhang H, Daley J, Fisman DN. Guideline-concordant therapy and reduced mortality and length of stay in adults with community-acquired pneumonia: playing by the rules. Archives of internal medicine. 2009 Sep 14;169(16):1525-31.
  56. Murray C, Shaw A, Lloyd M, Smith RP, Fardon TC, Schembri S, et al. A multidisciplinary intervention to reduce antibiotic duration in lower respiratory tract infections. The Journal of antimicrobial chemotherapy. 2014 Feb;69(2):515-8.
  57. Parente DM, Cunha CB, Mylonakis E, Timbrook TT. The Clinical Utility of Methicillin-Resistant Staphylococcus aureus (MRSA) Nasal Screening to Rule Out MRSA Pneumonia: A Diagnostic Meta-analysis With Antimicrobial Stewardship Implications. Clin Infect Dis. 2018 Jun 18;67(1):1-7.
  58. Nicolle LE, Gupta K, Bradley SF, Colgan R, DeMuri GP, Drekonja D, et al. Clinical Practice Guideline for the Management of Asymptomatic Bacteriuria: 2019 Update by the Infectious Diseases Society of Americaa. Clinical Infectious Diseases. 2019;68(10):e83-e110.
  59. Holland TL, Raad I, Boucher HW, Anderson DJ, Cosgrove SE, Aycock PS, et al. Effect of Algorithm-Based Therapy vs Usual Care on Clinical Success and Serious Adverse Events in Patients with Staphylococcal Bacteremia: A Randomized Clinical Trial. Jama. 2018 Sep 25;320(12):1249-58.
  60. Paulsen J, Solligard E, Damas JK, DeWan A, Asvold BO, Bracken MB. The Impact of Infectious Disease Specialist Consultation for Staphylococcus aureus Bloodstream Infections: A Systematic Review. Open forum infectious diseases. 2016 Mar;3(2):ofw048.
  61. Drekonja DM, Amundson WH, Decarolis DD, Kuskowski MA, Lederle FA, Johnson JR. Antimicrobial use and risk for recurrent Clostridium difficile infection. The American journal of medicine. 2011 Nov;124(11):1081 e1-7.
  62. Harpe SE, Inocencio TJ, Pakyz AL, Oinonen MJ, Polk RE. Characterization of continued antibacterial therapy after diagnosis of hospital-onset Clostridium difficile infection: implications for antimicrobial stewardship. Pharmacotherapy. 2012 Aug;32(8):744-54.
  63. Shaughnessy MK, Amundson WH, Kuskowski MA, DeCarolis DD, Johnson JR, Drekonja DM. Unnecessary antimicrobial use in patients with current or recent Clostridium difficile infection. Infection control and hospital epidemiology : the official journal of the Society of Hospital Epidemiologists of America. 2013 Feb;34(2):109-16.
  64. McDonald LC, Gerding DN, Johnson S, Bakken JS, Carroll KC, Coffin SE, et al. Clinical Practice Guidelines for Clostridium difficile Infection in Adults and Children: 2017 Update by the Infectious Diseases Society of America (IDSA) and Society for Healthcare Epidemiology of America (SHEA). Clinical Infectious Diseases. 2018;66(7):e1-e48.
  65. Norris AH, Shrestha NK, Allison GM, Keller SC, Bhavan KP, Zurlo JJ, et al. 2018 Infectious Diseases Society of America Clinical Practice Guideline for the Management of Outpatient Parenteral Antimicrobial Therapya. Clinical Infectious Diseases. 2018;68(1):e1-e35.
  66. Thom KA, Tamma PD, Harris AD, Dzintars K, Morgan DJ, Li S, et al. Impact of a Prescriber-driven Antibiotic Time-out on Antibiotic Use in Hospitalized Patients. Clin Infect Dis. 2019 Apr 24;68(9):1581-4.
  67. Tamma PD, Miller MA, Cosgrove SE. Rethinking How Antibiotics Are Prescribed: Incorporating the 4 Moments of Antibiotic Decision Making Into Clinical Practice. JAMA. 2019 Jan 15;321(2):139-40.
  68. Lee CE, Zembower TR, Fotis MA, Postelnick MJ, Greenberger PA, Peterson LR, et al. The incidence of antimicrobial allergies in hospitalized patients: implications regarding prescribing patterns and emerging bacterial resistance. Archives of internal medicine. 2000 Oct 9;160(18):2819-22.
  69. Centers for Disease Control and Prevention. Evaluation and Diagnosis of Penicillin Allergy for Healthcare Professionals. Available from: https://www.cdc.gov/antibiotic-use/community/for-hcp/Penicillin-Allergy.html
  70. Jeffres MN, Narayanan PP, Shuster JE, Schramm GE. Consequences of avoiding beta-lactams in patients with beta-lactam allergies. The Journal of allergy and clinical immunology. 2016 Apr;137(4):1148-53.
  71. Shenoy ES, Macy E, Rowe T, Blumenthal KG. Evaluation and Management of Penicillin Allergy: A Review. Jama. 2019 Jan 15;321(2):188-99.
  72. Timmons V, Townsend J, McKenzie R, Burdalski C, Adams-Sommer V. An evaluation of provider-chosen antibiotic indications as a targeted antimicrobial stewardship intervention. American journal of infection control. 2018 Oct;46(10):1174-9.
  73. Rattanaumpawan P, Morales KH, Binkley S, Synnestvedt M, Weiner MG, Gasink LB, et al. Impact of antimicrobial stewardship programme changes on unnecessary double anaerobic coverage therapy. The Journal of antimicrobial chemotherapy. 2011 Nov;66(11):2655-8.
  74. Schultz L, Lowe TJ, Srinivasan A, Neilson D, Pugliese G. Economic impact of redundant antimicrobial therapy in US hospitals. Infection control and hospital epidemiology : the official journal of the Society of Hospital Epidemiologists of America. 2014 Oct;35(10):1229-35.
  75. Langford BJ, Seah J, Chan A, Downing M, Johnstone J, Matukas LM. Antimicrobial Stewardship in the Microbiology Laboratory: Impact of Selective Susceptibility Reporting on Ciprofloxacin Utilization and Susceptibility of Gram-Negative Isolates to Ciprofloxacin in a Hospital Setting. Journal of clinical microbiology. 2016 Sep;54(9):2343-7.
  76. Centers for Disease Control and Prevention. Implementation Resources for Antibiotic Stewardship. Available from: https://www.cdc.gov/antibiotic-use/core-elements/implementation.html
  77. Musgrove MA, Kenney RM, Kendall RE, Peters M, Tibbetts R, Samuel L, et al. Microbiology Comment Nudge Improves Pneumonia Prescribing. Open forum infectious diseases. 2018 Jul;5(7):ofy162.
  78. Society of Infectious Diseases Pharmacists. AUR Vendorsexternal iconexternal icon. Available from: https://www.sidp.org/aurvendors
  79. United States Federal Government. National Strategy for Combating Antibiotic-resistant Bacteria pdf iconpdf icon[PDF – 37 pages]external iconexternal icon. Available from: https://obamawhitehouse.archives.gov/sites/default/files/docs/carb_national_strategy.pdf
  80. van Santen KL, Edwards JR, Webb AK, Pollack LA, O’Leary E, Neuhauser MM, et al. The Standardized Antimicrobial Administration Ratio: A New Metric for Measuring and Comparing Antibiotic Use. Clin Infect Dis. 2018 Jul 2;67(2):179-85.
  81. Griebel ME, Heintz B, Alexander B, Egge J, Goto M, Livorsi DJ. Understanding changes in the standardized antimicrobial administration ratio for total antimicrobial use after implementation of prospective audit and feedback. Infection control and hospital epidemiology : the official journal of the Society of Hospital Epidemiologists of America. 2018 Dec;39(12):1476-9.
  82. Livorsi DJ, O’Leary E, Pierce T, Reese L, van Santen KL, Pollock DA, et al. A Novel Metric to Monitor the Influence of Antimicrobial Stewardship Activities. Infection control and hospital epidemiology : the official journal of the Society of Hospital Epidemiologists of America. 2017 Jun;38(6):721-3.
  83. Centers for Disease Control and Prevention. AU Option Case Examples. Available from: https://www.cdc.gov/nhsn/au-case-examples/index.html
  84. World Health Organization Collaborating Centre for Drug Statistics Methodology. ATC Index with DDDs. Available from: http://www.whocc.no/atc_ddd_index/
  85. Dancer SJ, Kirkpatrick P, Corcoran DS, Christison F, Farmer D, Robertson C. Approaching zero: temporal effects of a restrictive antibiotic policy on hospital-acquired Clostridium difficile, extended-spectrum beta-lactamase-producing coliforms and meticillin-resistant Staphylococcus aureus. International journal of antimicrobial agents. 2013 Feb;41(2):137-42.
  86. Valiquette L, Cossette B, Garant MP, Diab H, Pepin J. Impact of a reduction in the use of high-risk antibiotics on the course of an epidemic of Clostridium difficile-associated disease caused by the hypervirulent NAP1/027 strain. Clin Infect Dis. 2007 Sep 1;45 Suppl 2:S112-21.
  87. Schechner V, Temkin E, Harbarth S, Carmeli Y, Schwaber MJ. Epidemiological interpretation of studies examining the effect of antibiotic usage on resistance. Clinical microbiology reviews. 2013 Apr;26(2):289-307.
  88. Schulz LT, Fox BC, Polk RE. Can the antibiogram be used to assess microbiologic outcomes after antimicrobial stewardship interventions? A critical review of the literature. Pharmacotherapy. 2012 Aug;32(8):668-76.
  89. Nowak MA, Nelson RE, Breidenbach JL, Thompson PA, Carson PJ. Clinical and economic outcomes of a prospective antimicrobial stewardship program. American journal of health-system pharmacy : AJHP : official journal of the American Society of Health-System Pharmacists. 2012 Sep 1;69(17):1500-8.
  90. Malani AN, Richards PG, Kapila S, Otto MH, Czerwinski J, Singal B. Clinical and economic outcomes from a community hospital’s antimicrobial stewardship program. American journal of infection control. 2013 Feb;41(2):145-8.
  91. Beardsley JR, Williamson JC, Johnson JW, Luther VP, Wrenn RH, Ohl CC. Show me the money: long-term financial impact of an antimicrobial stewardship program. Infection control and hospital epidemiology : the official journal of the Society of Hospital Epidemiologists of America. 2012 Apr;33(4):398-400.
  92. Department of Veterans Affairs. Medication Use Evaluation Resourcesexternal iconexternal icon. Available from: https://www.pbm.va.gov/pbm/vacenterformedicationsafety/vacenterformedicationsafetyresources.asp
  93. Centers for Disease Control and Prevention. State-based HAI prevention. Available from: https://www.cdc.gov/hai/state-based/index.html
  94. Patel SJ, Saiman L, Duchon JM, Evans D, Ferng YH, Larson E. Development of an antimicrobial stewardship intervention using a model of actionable feedback. Interdisciplinary perspectives on infectious diseases. 2012;2012:150367.
  95. Meeker D, Linder JA, Fox CR, Friedberg MW, Persell SD, Goldstein NJ, et al. Effect of Behavioral Interventions on Inappropriate Antibiotic Prescribing Among Primary Care Practices: A Randomized Clinical Trial. Jama. 2016 Feb 9;315(6):562-70.
  96. Centers for Disease Control and Prevention. CDC Training on Antibiotic Stewardship. Available from: https://www.cdc.gov/antibiotic-use/community/for-hcp/continuing-education.html
  97. Agency for Healthcare Research and Quality. AHRQ Safety Program for Improving Antibiotic Useexternal iconexternal icon. Available from: https://www.ahrq.gov/hai/tools/antibiotic-stewardship/index.html
  98. Centers for Disease Control and Prevention. The Core Elements of Antibiotic Stewardship for Nursing Homes. Available from: https://www.cdc.gov/longtermcare/prevention/antibiotic-stewardship.html
  99. Centers for Disease Control and Prevention. Core Elements of Outpatient Antibiotic Stewardship. Available from: https://www.cdc.gov/antibiotic-use/core-elements/outpatient.html
  100. Centers for Disease Control and Prevention. The Core Elements of Human Antibiotic Stewardship Programs in Resource-Limited Settings pdf iconpdf icon[PDF- 28 pages]. Available from: https://www.cdc.gov/antibiotic-use/healthcare/pdfs/18-295875-A-ASP-CE-Web-508.pdf