Pa Patient Saf Advis 2015 Dec;12(4):149-57.
Strategies to Turn the Tide against Inappropriate Antibiotic Utilization
Infectious Diseases; Internal Medicine and Subspecialties; Pharmacy; Surgery; Urology
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JoAnn Adkins, BSN, RN, CIC
Infection Prevention Analyst

Sharon Bradley, RN, CIC
Senior Infection Prevention Analyst

Edward Finley, BS

Data Analyst

Pennsylvania Patient Safety Authority

Corresponding Author
JoAnn Adkins


Focusing on antibiotic utilization practices is a vital strategy to minimize the increasing incidence of both multidrug-resistant organisms (MDROs) and Clostridium difficile infections. Pennsylvania Patient Safety Authority staff analyzed the incidence of MDROs and C. difficile in Pennsylvania hospitals and long-term care facilities (LTCFs), identified antibiotic prescribing practices in LTCFs, and researched strategies to help healthcare facilities build or enhance antibiotic stewardship. From April 2014 through March 2015, 19.0% of the total healthcare-associated infections in Pennsylvania were caused by MDROs, and 17.1% by C. difficile. Over the same time period, 1.9% of infections in LTCFs were associated with MDROs, and 7.3% with C. difficile. Analysis of Pennsylvania’s LTCF infection events identified frequent use of fluoroquinolones and cephalosporins as initial antibiotics in multiple infection categories. A review of the literature revealed detailed strategies, including engaging physicians and senior leadership, developing and using an antibiogram, and providing education to healthcare workers to address identified practice gaps and barriers. Implementing these strategies will promote appropriate antibiotic use and help facilities develop and sustain a robust stewardship program to decrease the incidence of MDRO and C. difficile infections.


The increasing incidence of multidrug-resistant organism (MDRO) infections has become a safety concern for patients in hospitals and long-term care facilities (LTCFs) in Pennsylvania as well as nationally. Infections caused by drug-resistant organisms are more difficult to treat, incur greater treatment costs, and have greater morbidity and mortality than infections caused by organisms susceptible to antibiotics.1-3 Inappropriate antibiotic usage contributes to the development of MDROs and Clostridium difficile infections, which together are responsible for more than two million infections and at least 37,000 deaths annually in the United States.3C. difficile infection, while not caused by an MDRO, is another adverse outcome related to antibiotic use. Antibiotics kill beneficial bacteria normally found in the colon; the absence of normal bacteria then allows C. difficile bacteria to multiply and cause gastrointestinal infection.4 The antibiotics that are particularly associated with MDROs and C. difficile include clindamycin and antibiotics in the fluoroquinolone and extended-spectrum cephalosporin drug classes.5-7

Multiple professional societies and regulatory agencies have identified the need to address the threat of drug-resistant organisms and inappropriate antibiotic usage. Several organizations have released guidelines to assist in developing antibiotic stewardship programs to improve antibiotic utilization processes.2,8-10 The National Action Plan for Combating Antibiotic-Resistant Bacteria, released by the White House in March 2015, includes specific goals and objectives to address drug resistance.11 The Centers for Disease Control and Prevention (CDC) defines MDROs as epidemiologically significant organisms or pathogens that have one or more of the following characteristics: a tendency for transmission within healthcare facilities, antibiotic resistance, increased morbidity and mortality, or a newly discovered or reemerging pathogen.12

Focusing on antibiotic utilization practices is a vital component of strategies to minimize the incidence of both multidrug resistance and C. difficile infection. Many facilities are working toward antibiotic stewardship, but the implementation of a robust program is a complex undertaking. Based on facility responses to the Pennsylvania Patient Safety Authority’s 2015 Antibiotic Stewardship Questionnaire, opportunities for improvement were identified in the areas of leadership support, accountability, expertise and support, action, tracking and reporting, and education.13 To assist in implementing an antibiotic stewardship program, facilities can perform a gap analysis to evaluate their existing resources, identify key stakeholders, evaluate current antibiotic use, and determine potential barriers and data to be collected for analysis.1,2,9 A process improvement team can assist in developing and sustaining a successful program. Tools to perform a gap analysis of antibiotic prescribing practices and assist facilities in targeting resources are provided in the Pennsylvania Patient Safety Advisory article “Antibiotic Stewardship in Hospitals and Long-Term Care Facilities: Building an Effective Program.”13


Analysts reviewed Pennsylvania hospital events reported through the National Healthcare Safety Network (NHSN) and LTCF events reported through the Pennsylvania Patient Safety Reporting System (PA-PSRS) for the 12-month period from April 2014 through March 2015 to determine the most common healthcare-associated infections (HAIs) and the rates of infection caused by epidemiologically significant organisms in Pennsylvania facilities. Analysts reviewed the PA-PSRS data of the same time frame to ascertain antibiotic prescribing patterns in LTCFs. Comparable information on prescribing patterns is not reported by hospitals.

Of the 230 hospitals actively reporting to NHSN as of March 31, 2015, data from 203 (88.3%) met validation criteria. Twenty-seven facilities were excluded from analysis:

  • Twenty-four hospitals because patient-day entries were absent for at least one month of the time period
  • Three hospitals because either the number of catheter-associated urinary tract infections (CAUTIs) was submitted without accompanying catheter-day entries or the number of central-line-associated bloodstream infections was submitted without accompanying central-line-day entries

Of the 702 LTCFs active in PA-PSRS as of March 31, 2015, data from 591 (84.2%) met validation criteria. One hundred eleven LTCFs were excluded from analysis:

  • Eighty-one LTCFs because resident-day entries were absent for at least one month of the time period
  • Twenty-nine LTCFs because occupancy was either above 100% or below 50% for at least one month of the time period*
  • One LTCF because the number of CAUTIs was submitted without accompanying catheter-day entries

* Facility occupancy is calculated as the number of resident-days divided by the number of beds listed for each facility for each month. Then the quotient is divided by the number of days in the month.



For the 12-month period, Pennsylvania hospitals reported 24,145 HAIs. The predominant types of infections reported were surgical site infection, gastrointestinal infection (GI), urinary tract infection (UTI), bloodstream infection (BSI), and pneumonia. See Figure 1.

Figure 1. Pennsylvania Healthcare-Associated Infections by Category


Figure 1. Pennsylvania Healthcare-Associated Infections by Category


Focusing further on epidemiologically significant organisms reveals that 4,594 (19.0%) of the reported infections were caused by MDROs and 4,121 (17.1%) by C. difficile. For the 12-month period, in Pennsylvania hospitals, this would average 23.6 new antibiotic-associated infections occurring each day: 12.3 by MDROs and 11.3 by C. difficile. See Figure 2.

Figure 2. Hospital-Reported Healthcare-Associated Infections caused by Epidemiological Significant Organisms by Category

Figure 2. Hospital-Reported Healthcare-Associated Infections caused by Epidemiological Significant Organisms by Category 

Long-Term Care

For the 12-month period, LTCFs reported 29,108 HAIs through PA-PSRS. The predominant type of infections was respiratory tract infections (39.7%). See Figure 3.

Figure 3. Nursing Home Infections by Category

Figure 3. Nursing Home Infections by Category

Of those HAIs, 1.9% (n = 545 of 29,108) were associated with MDROs. The most common MDRO was methicillin-resistant Staphylococcus aureus, and the category of HAI with the highest percentage of MDROs was BSIs (19.7%, n = 14 of 71). While C. difficile accounted for 7.3% (n = 2,109 of 29,108) of the total number of nursing home infections, 54.0% (n = 2,109 of 3,908) of GI infections were associated with C. difficile.

Analysis of Pennsylvania LTCFs’ prescribing patterns in the identified time frame demonstrates frequent use of fluoroquinolones and cephalosporins as an initial antibiotic in multiple infection categories. See Figure 4.

Figure 4. Nursing Home Initial Antibiotic Orders, by Infection Site

Figure 4. Nursing Home Initial Antibiotic Orders, by Infection Site 


Antibiograms Encourage Responsible Use of Antibiotics

The antibiogram is a facility-specific, cumulative antimicrobial susceptibility data report that provides valuable information to guide antibiotic prescribing practices in both hospitals and LTCFs. This report utilizes microbiologic data from patient specimens to identify facility- and/or unit-specific antibiotic resistance patterns. Regular distribution of the current antibiogram provides useful information to help prescribing clinicians (1) select the most appropriate agents for initial empirical antimicrobial therapy, (2) improve outcomes among patients with infections, and (3) reduce inappropriate antibiotic use. Antibiograms are inexpensive, easily accessible, and facilitate identification of changes in facility or unit resistance patterns. Final selection of empiric therapy should be based on the patient’s infection history and past antimicrobial use, as well as the local antibiogram.

General steps to plan, develop, and implement an antibiogram include the following:8,14,15

  • Engage team members who have knowledge and understanding of culturing practices and infection control, such as the laboratory microbiologist, infectious-disease consultant, medical director, pharmacist, and infection preventionist or infection prevention designee.
  • Determine if the antibiogram will be unit- or facility-based.
  • Develop the antibiogram with culture information, including the patient/resident name and identification number, culture identification number, date completed, and organisms and antibiotic sensitivities identified.
  • Review the antibiogram to monitor trends in antimicrobial resistance within different areas of the facility.
  • Distribute the antibiogram to all prescribing clinicians, and accompany distribution with education and instructions for use and interpretation.
  • Monitor the use of the antibiogram in conjunction with culture sensitivity results to aid in antibiotic selection.

Antibiotic Stewardship Program Core Elements

Many of the interventions to implement an antibiotic stewardship program are appropriate for both hospital and long-term care settings. The method of implementation of these elements will depend on the individual facility and staffing. Both acute and long-term care settings can benefit from performing a gap analysis of the current state of their antibiotic stewardship program. Appropriate measures for implementation can be selected from the CDC’s core elements checklists and the Institute for Healthcare Improvement’s Driver Diagram and Change Package.8,16 While the number of published core elements may seem daunting, it is suggested that a facility begin with implementation of one or two strategies and then gradually add new strategies over time.

The Authority has developed a crosswalk of strategies for both hospitals and LTCFs that outlines stewardship activities in the areas of leadership, provider engagement, clinical action to improve antibiotic use, multidisciplinary support, and tracking and reporting antibiotic usage. See the Table.

Table. Antibiotic Stewardship Core Elements
Core Elements Acute Long-Term Care
Improve Leadership, Culture, and Accountability
    Urge administrative and clinical directors to develop and champion goals to improve the use of antibiotics.
    Communicate facility stewardship goals to clinicians and physicians in writing, in person, and
    at staff meetings.
    Incorporate stewardship-related tasks in job descriptions and performance reviews.
    Recruit a physician champion to be accountable for the antibiotic stewardship program.
    Identify a facility leader accountable for antibiotic stewardship activities (e.g., medical director, director/assistant director of nursing, consultant pharmacist).
    Monitor if antibiotic stewardship policies are followed.
Encourage Provider Engagement
    Engage physicians in the development of the program.
    Assist in developing guidelines and addressing reluctant physicians.
    Promote the focus of optimal antibiotic use into the current process of care.
    Work with providers, and follow up to address questions or concerns.
    Monitor and provide regular, personalized feedback to physicians and advanced practice providers on antibiotic usage, prescribing habits, the incidence of drug-resistant organisms, and Clostridium difficile infections.
    Require preauthorization and documented justification for broad-spectrum antibiotics.
    Introduce specific treatment recommendations that are consistent with national guidelines, including recommendations to change intravenous (IV) to oral (PO) therapy.
    Use prospective audit and provider feedback to monitor adherence to national guidelines for treatment.
    Use a standard assessment and communication tool for residents suspected to have infections.
Improve Antibiotic Use
    Institute a policy that requires prescribers to document dose, duration, and indication for all antibiotic prescriptions.
    Develop and institute infection-specific treatment guidelines, and monitor adherence to them.
    Develop standardized diagnostic criteria for identifying patients with signs and syndromes suggesting specific types of infections and situations for which antibiotics are clearly not indicated.
    Implement a formal procedure for all clinicians to review the appropriateness of empiric antibiotics 48 hours after the initial order (an "antibiotic time-out").
    Consider having the physician lead or pharmacist review courses of antibiotic therapy for specific agents (prospective audit with feedback).
    Produce a cumulative antibiotic susceptibility report (antibiogram).
    Preauthorize dispensing of specific antibiotic agents.
    Institute pharmacy-driven interventions (e.g., automatic IV to PO changes, automatic alert of duplicative therapy, time-sensitive stop orders, dose adjustment and optimization).
    Develop a facility-specific algorithm for assessing residents and performing appropriate diagnostic testing (e.g., cultures) for specific infections.
    Implement a process for communicating antibiotic information on transfer or discharge.
    Implement an infection-specific intervention to improve antibiotic use.
Core Elements Acute Long-Term Care
Engage Multidisciplinary Support
    Identify unit champions to assist with education and monitoring.
    Actively involve members of the team to develop an action plan and goals that are consistent with national stewardship guidelines.
    Create a clear task list for each member of the stewardship team.
    Engage quality improvement and safety committees in approving antibiotic stewardship goals.
    Populate the stewardship program team with administrative, infection control, nursing, and physician personnel.
    Include the pharmacist, laboratory staff, and infectious-diseases physician, as they have antibiotic expertise.
    Work with the consultant pharmacist staff to review microbiology culture data to assess and guide antibiotic selection.
    Partner with the antibiotic stewardship team at the local hospitals.
    Engage an external infectious-diseases/stewardship consultant.
Track and Report Antibiotic Usage and Clinical Outcomes to Measure Impact of Interventions
    Monitor for increasing rates of drug-resistant and C. difficile infections, and benchmark rates with comparable facilities.
    Track adherence to prescribing and documenting the appropriate dose, duration, and use of the recommended agent for the indication.
    Measure antibiotic usage in days of therapy by dividing the amount of each specific antibiotic administered to a patient by a standardized denominator (e.g., patient-days).
    Track adverse reactions to antibiotics.
    Monitor adherence to clinical assessment documentation and facility-specific treatment recommendations.
    Provide facility-specific reports on antibiotic use and outcomes to clinical and nursing staff.
    Evaluate antibiotic cost increases, and determine if the increases are caused by an increase in the actual cost of the drug or increased usage.
    Track antibiotic usage in patients who are colonized or asymptomatic and in situations in which cultures have not been ordered.
    Evaluate appropriate use of broad-spectrum versus narrow-spectrum drugs.
    If in Pennsylvania, utilize Pennsylvania Patient Safety Reporting System analytic tools to benchmark facility data with peer and state rates.
    Monitor rates of new antibiotic starts per 1,000 resident-days.
    Perform point prevalence surveys of antibiotic use.
Overcome Funding, Information Technology, Time and Education Challenges
    Engage senior leadership to dedicate personnel, financial, and information technology resources to the program.
    Prioritize identified gaps, and develop action plans to address them with the stewardship team.
    Work with departmental leadership to allow staff time to participate in stewardship projects.
    Access national antibiotic stewardship guidelines.
    Offer varying types of formal and informal education to clinical providers and nursing staff.
    Use messaging, posters, and newsletters to communicate with staff.
    Make a business case for antibiotic stewardship, and present it to leadership to demonstrate how stewardship leads to a return on investment.
    Provide educational resources to clinicians and other relevant staff about antibiotic resistance.

Sources: Centers for Disease Control and Prevention. The core elements of antibiotic stewardship for nursing homes [online]. 2015 [cited 2015 Sep 1].

Centers for Disease Control and Prevention. Core elements of hospital antibiotic stewardship programs [online]. 2014 [cited 2015 Sep 1].

Institute for Healthcare Improvement. Antibiotic stewardship driver diagram and change package [online]. 2012 Jul [cited 2015 Sep 1].

Improve Prescribing Practices

In a patient with a suspected infection, best practices associated with optimal antibiotic use include the following:6,8,16,17

  • Ensure that the patient always exhibits clinical symptoms consistent with state and national site-specific infection criteria.
  • Complete the lab work required by the national criteria (e.g., culture and sensitivity, quick test, chest x-ray).
  • Select the appropriate empiric antibiotic for the specific site of infection (narrowest-spectrum drug, dose, and duration consistent with state and national clinical syndrome and site-specific guidelines).
  • Ensure a 48-hour time-out identifies the organism and culture sensitivities and assesses the quality of the culture. Ensure the quality of the lab test meets nationally accepted criteria (e.g., correct colony count, number of organisms, specimen type).
  • Order the appropriate, narrowest-spectrum antibiotic based on the test results, national guidelines, and the facility’s susceptibility patterns.

There are multiple opportunities in the prescribing decision process to stray from optimal practices. Inappropriate antibiotic use includes prescribing drugs that are unnecessary, no longer necessary (e.g., failure to change an empiric drug order), or incorrectly dosed, as well as using broad-spectrum agents when narrow-spectrum agents are appropriate for susceptible bacteria.3 An example of this is ordering antibiotics for a patient with asymptomatic bacteriuria. A positive urine culture by itself does not denote an infection. These cases may not be being tracked for antibiotic usage because reporting is not necessary. Figure 5 may assist healthcare facility clinicians with antibiotic prescribing decisions.

Figure 5. Antibiotic Use Best Practices and Suboptimal Practices

Figure 5. Antibiotic Use Best Practices and Suboptimal Practices

Additional resources from federal and national agencies to assist hospitals and LTCFs implement a facility-specific antibiotic stewardship program are listed in “Antibiotic Stewardship Resources.”


For hospitals and LTCFs, reporting does not provide information on treatment changes based on culture results and treatment effectiveness. LTCFs have only been reporting antibiotic usage since April 2014, so trends are not yet apparent. Hospital reporting into NHSN identifies the organism cultured and the sensitivity information but does not collect prescribing patterns. Pennsylvania facilities do not report specific information on the impact of antibiograms and antibiotic stewardship programs. The Patient Safety Authority’s 2015 Antibiotic Stewardship Questionnaire was a small sample study of 12 hospitals and 12 LTCFs.


Pennsylvania healthcare facilities deal with a substantial number of infections caused by drug-resistant organisms and C. difficile, and inappropriate antibiotic usage is a key factor in the development of these infections. Implementing an antibiotic stewardship program will help direct the appropriate use of antibiotics; and improved patient care, decreased liability, and decreased survey deficiencies are powerful arguments for antibiotic stewardship. Antibiotic stewardship programs in both hospitals and LTCFs can be enhanced by identifying opportunities for improvement, engaging teams in implementing the core elements of antibiotic stewardship, using the facility-specific antimicrobial susceptibility data report, and improving prescribing practices.


Howard Newstadt, JD, MBA, CGCIO, finance director and chief information officer, Pennsylvania Patient Safety Authority, contributed to the development of the figures for this article.


  1. Society for Healthcare Epidemiology of America, Infectious Diseases Society of America, Pediatric Infectious Diseases Society. Policy statement on antimicrobial stewardship by the Society for Healthcare Epidemiology of America (SHEA), the Infectious Diseases Society of America (IDSA), and the Pediatric Infectious Diseases Society (PIDS) [online]. 2012 Apr [cited 2015 Sep 1].
  2. Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America. Guidelines for developing an institutional program to enhance antimicrobial stewardship [online]. 2007 Jan [cited 2015 Sep 1].
  3. Centers for Disease Control and Prevention. Core elements of hospital antibiotic stewardship programs [online]. 2014 [cited 2015 Sep 1].
  4. Centers for Disease Control and Prevention. Healthcare-associated infections (HAIs): Clostridium difficile infection [online]. [cited 2015 Sep 1].
  5. Dubberke ER, Carling P, and Carrico R, et al. Strategies to prevent Clostridium difficile infections in acute care hospitals: 2014 update. Infect Control Hosp Epidemiol 2014 Jun;35(6):628-45.
  6. Centers for Disease Control and Prevention. Making health care safer [online]. Vital Signs 2014 Mar [cited 2015 Sep 1].
  7. Furuno, JP, Comer AC, Johnston JK, et al. using antibiograms to improve antibiotic prescribing in skilled nursing facilities. Infect Control Hosp Epidemiol 2014 Oct;35 Suppl 3:S56-61.
  8. Institute for Healthcare Improvement. Antibiotic stewardship driver diagram and change package [online]. 2012 Jul [cited 2015 Sep 1].
  9. Joint Commission Resources. Antimicrobial stewardship toolkit [online]. 2012 [cited 2015 Sep 1].
  10. Association of State and Territorial Health Officials. Combating antibiotic resistance: policies to promote antimicrobial stewardship programs [online]. [Cited 2015 Sep 1].
  11. White House. National action plan for combating antibiotic-resistant bacteria [online]. 2015 Mar [cited 2015 Sep 1].
  12. Centers for Disease Control and Prevention. Management of multidrug-resistant organisms in healthcare settings, 2006 [online]. Glossary—multidrug-resistant organisms [online]. [Cited 2015 Sep 2].
  13. Bradley S. Antibiotic stewardship in hospitals and long-term care facilities: building an effective program. Pa Patient Saf Advis [online] 2015 Jun [cited 2015 Sep 2].;12(2)/Pages/71.aspx
  14. Agency for Healthcare Research and Quality. US Department of Health and Human Services. Module 2: antibiograms: choosing an appropriate antibiotic [online]. [cited 2015 Sep 1].
  15. Hirshon M, Schurr J. Using nursing home antibiograms to improve antibiotic prescribing and delivery [online]. Agency for Healthcare Research and Quality 2012 annual conference slide presentation. 2012 Sep 10 [cited 2015 Sep 1].
  16. Centers for Disease Control and Prevention. The core elements of antibiotic stewardship for nursing homes [online]. 2014 [cited 2015 Sep 1].
  17. Stone ND, Ashraf MS, Calder J, et al. Surveillance definitions of infections in long-term care facilities: revisiting the McGeer criteria. Infect Control Hosp Epidemiol 2012 Oct;33(10):965-77.

 Supplemental Material

Antibiotic Stewardship Resources

Antibiotic Stewardship in Hospitals and Long-Term Care Facilities: Building an Effective Program

Pennsylvania Patient Safety Authority;12(2)/Pages/71.aspx 

Authority surveys of hospitals and long-term care facilities demonstrate opportunities for improvement in all facets of antibiotic stewardship. Inappropriate antibiotic use perpetuates and exacerbates antibiotic resistance. Antibiotic stewardship programs help to ensure optimal treatment for patients with infections and may enhance the length of time current antibiotics remain effective.

Appropriate Use of Medical Resources: Antimicrobial Stewardship Toolkit

American Hospital Association

This user guide provides information about how to start a new stewardship program or enhance an existing one, including tools, resources, references, and webinars for healthcare professionals, as well as patient resources.

National Action Plan for Combating Antibiotic-Resistant Bacteria

The White House 

The action plan outlines steps to implement the National Strategy for Combating Antibiotic-Resistant Bacteria and addresses the policy recommendations of the president’s Council of Advisors on Science and Technology.

Nursing Home Antimicrobial Stewardship Modules

Agency for Healthcare Research and Quality

These modules include four tested, evidence-based toolkits to help optimize antibiotic use.


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