Infectious Diseases Physicians: Leading the Way in Antimicrobial Stewardship

Transcription

1 Clinical Infectious Diseases IDSA FEATURES Infectious Diseases Physicians: Leading the Way in Antimicrobial Stewardship Belinda Ostrowsky, 1 Ritu Banerjee, 2 Robert A. Bonomo, 3,4,5 Sara E. Cosgrove, 6 Lisa Davidson, 7 Shira Doron, 8 David N. Gilbert, 9,10 Amanda Jezek, 11 John B. Lynch III, 12 Edward J. Septimus, 13,14 Javeed Siddiqui, 15 and Nicole M. Iovine 16 ; for the Infectious Diseases Society of America, Pediatric Infectious Diseases Society, and the Society for Healthcare Epidemiology of America 1 Montefiore Medical Center, Albert Einstein Medical Center, Bronx, New York; 2 Vanderbilt University Medical Center, Nashville, Tennessee; 3 Research and Medical Services Veterans Affairs Medical Center, 4 Departments of Medicine, Pharmacology, Molecular Biology and Microbiology, Case Western Reserve University, and 5 Cleveland Geriatric Research Education and Clinical Center, Case Western Reserve University Cleveland Veterans Affairs Medical Center, Center for Antimicrobial Resistance and Epidemiology, Ohio; 6 Johns Hopkins University School of Medicine, Baltimore, Maryland; 7 Carolinas Health Care System, Charlotte, North Carolina; 8 Tufts Medical Center, Boston, Massachusetts; 9 Providence-Portland Medical Center and 10 Oregon Health Sciences University, Portland; 11 Infectious Diseases Society of America, Arlington, Virginia; 12 Harborview Medical Center, University of Washington, Seattle; 13 HCA Healthcare, Nashville, Tennessee; 14 Texas A&M College of Medicine, Houston; 15 TeleMed2U, Roseville, California; and 16 University of Florida College of Medicine, Gainesville Keywords. antimicrobial; stewardship; resistance; infectious diseases; infection prevention. Antimicrobial resistance is a well-documented public health crisis that seriously threatens patient outcomes and national security. Further, the World Health Organization has recognized antimicrobial resistance as a threat to global stability [1]. The overuse and misuse of antimicrobial agents are key drivers of the development of resistance. Antimicrobial stewardship programs (ASPs) optimize patient outcomes while minimizing unintended consequences of antimicrobial use. Antimicrobial stewardship has been defined as coordinated interventions designed to improve and measure the appropriate use of antimicrobial agents by promoting the selection of the optimal antimicrobial drug regimen including dosing, duration of therapy, and route of administration. [2] Given new regulatory requirements and political support for stewardship, healthcare facilities will benefit from expert guidance to develop and improve ASPs. Effective ASPs use the expertise and essential contributions of multiple experts including physicians, pharmacists [3], nurses [4], microbiologists, and infection preventionists. With this white paper (outline of paper in Table 1), the Infectious Diseases Society of America (IDSA), the Society for Healthcare Epidemiology of America (SHEA), and the Pediatric Infectious Diseases Society (PIDS) demonstrate how infectious diseases (ID) physicians are uniquely qualified to develop and lead multidisciplinary teams across all healthcare settings. The following clinical vignette is an example of how the lack of ID physician leadership of an ASP may contribute to a poor clinical outcome for an individual patient, to an extended and Received 7 November 2017; editorial decision 9 November 2017; accepted 16 January Correspondence: N. M. Iovine, University of Florida College of Medicine, 1600 SW Archer Road, R2-124, Gainesville, FL (nicole.iovine@medicine.ufl.edu). Clinical Infectious Diseases 2018;XX(00):1 9 The Author(s) Published by Oxford University Press for the Infectious Diseases Society of America. All rights reserved. For permissions, journals.permissions@oup.com. DOI: /cid/cix1093 likely poorly reimbursed length of stay, and to collateral damage to the larger patient community. At the end of this white paper, an alternative vignette highlights the potential positive impact of an ID physician led ASP. Case Vignette A 60-year-old man with type II diabetes mellitus was admitted from home with the diagnosis of severe sepsis. Blood cultures were obtained, broad-spectrum antimicrobials were started in the emergency department, and the patient was admitted to the intensive care unit (ICU). The next day, the blood cultures grew highly susceptible bacteria as determined by a new polymerase chain reaction based rapid identification method. The pharmacist charged with managing the hospital s ASP appropriately recommended a change to a narrower-spectrum antimicrobial. However, the patient s physician was reticent to act on advice of a nonphysician and continued broad-spectrum antimicrobials. The pharmacist was frustrated as she did not have an ID physician leader to help support her recommendation by reaching out to this provider. While the patient was recovering from the bloodstream infection, he developed Clostridium difficile colitis. Due to severe colonic inflammation, the patient next developed a second bloodstream infection, this time caused by an intestinal organism that was highly antimicrobial resistant, another consequence of broad-spectrum antimicrobial use. Although he eventually was stabilized after a 3-week hospital stay, he was unable to care for himself at home and was sent to a long-term care facility. While there, his C. difficile was transmitted to his roommate, whose discharge was delayed due to this complication. ID physicians form the frontline for diagnosing and treating complex infections, prescribing antimicrobial agents, and managing the impact of their use. Their clinical practice requires them to build strong relationships with facility leaders and physicians ID Physicians: Leading Stewardship CID 2018:XX (XX XXXX) 1

2 Table 1. Outline of Sections to Follow Introduction National Policy Context Unique Value and Expertise of ID Physicians Unique Role of ASP Leadership: Distinct from ID Consultation and Infection Prevention Models for Access to ID Physician Led ASPs Summary of Rationale for ID Physician Leadership of ASPs Recommendations Conclusions The intended readers of this white paper are healthcare stakeholders including federal policymakers, hospital executives, quality and patient safety leaders, and third-party payers Increasing regulatory requirements for ASPs extend across many healthcare facility types and are linked to patient safety and quality measures ID physicians possess the clinical knowledge and leadership qualities required to lead a successful ASP ID physicians can assist facilities that lack ASPs to become compliant with new regulatory requirements through innovation and technology ID physicians are best qualified to lead effective ASPs, which will lead to benefits in clinical outcomes, patient safety, quality metrics, and public health Abbreviations: ASP, antimicrobial stewardship program; ID, infectious diseases. across many specialties and to facilitate team-based care. Many ID physicians leadership skills have already been recognized through their roles as hospital epidemiologists, infection preventionists, and quality improvement and patient safety directors in many institutions. ASPs develop health system based guidance on antimicrobial prescribing built on local susceptibility and microbiology data and perform interventions through which they provide direct feedback to physicians regarding antimicrobial choices. On the basis of their leadership experience, system-wide relationships, and medical training, many ID physicians are well suited to lead multidisciplinary ASP teams. hospitals, critical access hospitals, and nursing care centers to establish and maintain ASPs that are aligned with the CDC core elements. Further, the standard calls for an ID physician to serve on the ASP team and reiterates CDC s assertion that physician leadership is effective [8]. However, current data from the CDC s National Healthcare Safety Network suggests that almost half of acute care hospitals do not yet have an ASP and that the proportion of other healthcare facilities (eg, outpatient clinics, dialysis centers) without ASPs is even greater. Further, only 48% of hospitals surveyed have all of CDC s recommended 7 core elements in place [9]. NATIONAL POLICY CONTEXT The federal government recognizes the potential of ASPs to improve patient outcomes and reduce the development of antimicrobial resistance. In 2014, the Centers for Disease Control and Prevention (CDC) published its Core Elements of Hospital Antibiotic Stewardship Programs [5] and subsequently published similar documents geared toward long-term care and outpatient facilities [6, 7]. The initial document summarizes fundamental components of successful hospital-based programs and complements the guidelines on ASPs from IDSA and SHEA (Table 2). The CDC document notes that ASPs should have a single leader with accountability and that physician-led programs have demonstrated success. The Joint Commission published a new antimicrobial stewardship standard, effective 1 January 2017, that requires UNIQUE VALUE AND EXPERTISE OF ID PHYSICIANS Established Leaders For many years, ID physicians have served in formal and informal leadership roles with quality improvement and patient safety initiatives, including system-wide efforts to improve the care of patients with infections through participation in the Centers for Medicare and Medicaid Services (CMS) core measures initiatives. ASP ID physicians are adept at ascertaining best medical practices, developing guidelines, interpreting new scientific information, implementing interventions, and communicating with stakeholders. Because many publicly reportable measures pertain to infectious diseases, ID physicians frequently serve as quality leaders at their institution (Table 3). With such roles, ID physicians are accustomed to maintaining a long-term perspective, aligning systems to Table 2. Centers for Disease Control and Prevention Core Elements of an Effective Antimicrobial Stewardship Program Leadership commitment: adequate personnel, financial, and information technology resources are available Accountability: a single leader is responsible for program outcomes Drug expertise: ASP-dedicated pharmacists are responsible for assisting with the implementation of ASP goals and initiatives Action: recommendations are implemented that are supported by scientific evidence and endorsed by professional societies Monitoring: antimicrobial prescribing and local resistance patterns are tracked Feedback: data on antimicrobial use and resistance are reported to physicians and nonphysician prescribers Education: physicians and nonphysician prescribers receive education regarding rational antimicrobial prescribing and local resistance patterns Abbreviation: ASP, antimicrobial stewardship program. 2 CID 2018:XX (XX XXXX) Ostrowsky et al

3 Table 3. Attributes of an Effective Leader Commands the respect of peers Inspires trust with all stakeholders Motivates the team Maintains a long-range perspective Aligns and improves systems or develops new ones Creates, anticipates, and recognizes opportunity maximize goal attainment, and recognizing opportunities for change and improvement. ID physicians possess unique skills by virtue of their training that make them well suited to lead ASPs and maximize the potential of members of the multidisciplinary ASP team (Table 4). Ability to Impact Prescriber Decision-Making Most antimicrobials are prescribed by non-id physicians and nonphysician prescribers. Changing their prescribing behaviors is the lynchpin of any successful effort to reduce inappropriate antimicrobial use [10]. ASP ID physicians can influence antimicrobial prescribing patterns by raising awareness of harms associated with unnecessary antimicrobial use and by drawing on their experience as leaders of multidisciplinary teams to build trust and consensus [11]. For example, physician-to-physician discussions occur naturally and constantly in the course of caring for patients. This type of interaction regarding antimicrobial use is more likely to be effective, particularly when major changes to antimicrobial therapy are warranted. Further, direct interactions are an opportunity to teach colleagues the basis for the suggested management plan. In addition to directly interacting with prescribers, ID physician leaders of ASPs can support pharmacists and other members of the ASP teams during prospective audits of specific patient management or antimicrobial prescribing by providing guidance and intervening in complex or challenging cases. Many examples of ASPs with strong ID physician leadership demonstrate improved patient outcomes and lower antimicrobial use while reducing costs [12]. Clinical Expertise ID physicians possess unique firsthand experience in directing care of challenging cases across the spectrum of healthcare delivery venues. In practical terms, the ASP ID physician guides identification of patients who would benefit from an official ID consultation, may be at increased risk for adverse events, may need closer monitoring, or may have an enhanced response to alternate approaches. Microbiology and Diagnostics The Accreditation Council for Graduate Medical Education requires that ID fellowship training facilitate direct and frequent interactions with microbiology laboratory personnel to develop among the trainees in-depth knowledge of microbiologic principles that inform antimicrobial prescribing [13]. ID physicians, with strong support from microbiologists, use diagnostics and microbiologic data to drive ASP goals (Table 5) by guiding selection of appropriate diagnostics, avoiding unnecessary laboratory testing, accurately interpreting test results, and ensuring that results lead to appropriate prescribing behavior. For example, use of molecular technology to identify C. difficile infections (CDIs) may detect more CDI cases but also may detect colonization in asymptomatic patients, leading to inappropriate treatment and an increase in the hospital s reported rate of CDI (which is tied to reimbursement) [14, 15]. Finally, the clinical expertise of the ID physician leader of the ASP can allay concerns of nonexperts about missing something ; such a fear often drives inappropriate antimicrobial prescribing. Table 4. Unique Expertise and Skills of Infectious Diseases Physicians as Leaders of Antimicrobial Stewardship Programs Area of Expertise Leadership Clinical expertise Microbiology and diagnostics Antimicrobials Quality Examples Experience managing multidisciplinary teams as quality leaders and hospital epidemiologists Regular interaction with hospital administration Ability to influence the prescribing practices of other physicians Routine connection with local and state health departments, the Centers for Disease Control and Prevention, and the World Health Organization Expertise in monitoring and managing patients with infections at all levels of complexity and across all healthcare settings Understanding of appropriate prophylactic and other infection prevention strategies Appreciation for the role of ASP in promoting and protecting public health Knowledge of microbiologic principles that inform rational antimicrobial prescribing Knowledge of national and local resistance patterns Ability to use diagnostic results to optimize antimicrobial prescribing Expert knowledge about appropriate testing indications, interpretation of results, and cost Understanding of traditional and next-generation diagnostics Comprehensive knowledge of antimicrobial use, side effects, cost, and adverse consequences Awareness of national prescribing trends Understanding of trends in national and local antimicrobial prescribing and resistance Ability to drive quality improvement and improve patient safety through optimal antimicrobial use Awareness of the link between rational antimicrobial prescribing and quality measures (eg, central line associated bloodstream infections, Clostridium difficile infection) Ability to use quality measures and quality improvement activities to maximize ASP objectives Abbreviation: ASP, antimicrobial stewardship program. ID Physicians: Leading Stewardship CID 2018:XX (XX XXXX) 3

4 Table 5. Effective Use of Diagnostics to Support Antimicrobial Stewardship Programs Evaluate the impact of new technologies and molecular techniques on patient care and quality measures Create targeted order bundles in the electronic medical record for patients with pneumonia, bloodstream infections, urinary tract infections, and others Coordinate clinical microbiology and information technology services to ensure prompt electronic communication of pertinent test results to patient caregivers and the antimicrobial stewardship programs team Create and maintain educational programs that clarify the strengths and weaknesses of new and traditional diagnostic methods Alignment of ASP Principles With Public Health and Emerging Infections ASP ID physicians routinely track and follow trends in antimicrobial use and microbiology and thus are at the frontline to identify and manage emerging infections. For example, when high volumes of patients presented with H1N1 influenza in 2009 and a nationwide shortage of oseltamivir ensued, public health authorities required facilities to designate individuals to authorize release of oseltamivir to appropriate patients. Not only did ASP ID physicians typically fill this role, they also reviewed evolving guidelines, tailored guidelines to local patient populations and circumstances including choice of testing and criteria for prioritizing testing and treatment, disseminated guidelines, educated prescribers and the public, and served as liaisons to state and local public health systems [16]. UNIQUE ROLE OF ASP LEADERSHIP: DISTINCT FROM ID CONSULTATION AND INFECTION PREVENTION The role of the ID physician who performs formal consultation one patient at a time is distinct from that of ASP leadership. Since many more patients receive antimicrobial agents than formal ID consultation, the ASP ID physician improves the health and safety of an expanded patient population. Specifically, the ASP ID physician provides unique ID expertise, develops the program s goals and assesses progress, develops and updates recommendations for antimicrobial use, triages more complicated cases, works with a variety of prescribers, provides peer-to-peer education, and provides program leadership that includes cultivating a culture that supports stewardship as well as obtaining and maintaining commitment to, and critical support of, ASPs from administrators and fellow physicians. These duties are distinct from those of the hospital epidemiologist or director of the institution s infection prevention program, even when an ID physician serves in these roles. For example, typical duties of the hospital epidemiologist include monitoring and reducing healthcare-associated infections, responding to outbreaks, and developing infection control policies, all of which are distinct but complementary to the function of ASPs. ID physicians are well suited to each of these roles, but the distinction is important. Compensation Model for ASP To ensure sufficient time and resources for quality ASPs, compensation for ASP ID-trained physician directors should be separate from that for leaders of hospital epidemiology and infection prevention programs. Payment models must appropriately compensate all ASP team members for time spent on stewardship activities [17]. Similarly, ASP ID physicians require protected time and full-time staff (appropriately scaled to facility size) to ensure their ability to conduct their ASP responsibilities balanced with other clinical, research, and teaching duties. In making the business case for an ID physician led ASP, it is appropriate to focus on the ASP s return on investment, manifested as better patient care and reduced antimicrobial use [18]. ASPs should track improvements in a variety of outcomes including fewer adverse drug reactions, less antimicrobial resistance, fewer CDIs, reduced overall harm, improved clinical outcomes, and less expense to the facility. As physician reimbursement is changing from a relative value unit (RVU) to a value-based purchasing model, the compensation model for the ID physician leaders of ASPs should also change from RVU-based to value-based. A 2008 article recommended that $250/hour may be an appropriate rate for an ID physician for leading an ASP [19], an amount that would need to be adjusted to 2017 dollars. Further, one should consider that stewardship is an evolving field, and this recommendation likely underestimates the true effort and expertise needed to implement ASP activities, properly measure progress and outcomes, and ensure compliance with regulatory mandates. Other ASP compensation options may provide a flat fee or stipend for ASP leadership. It is critical, however, that facilities not require a one-to-one ratio of cost savings to compensation, as many of the positive benefits of an ASP are not directly quantifiable. The optimal number of full-time equivalents (FTEs) allotted to stewardship duties depends on several variables (Table 6) [20, 21]. These variables include the type of ASP activities to be undertaken, the depth to which those activities will be pursued, and the type and magnitude of the desired outcomes. Because of these many variables, no exact formula exists for calculating the most appropriate number of FTEs and potential associated overhead costs. Below are possible models for the role of the ID physician leader and illustrative examples of ASPs throughout the United States that highlight ID physician leaders and the successes realized under their direction. Examples of FTE Support for ID Physician Leaders of ASPs The distribution of ID physician and ID pharmacist FTEs depends on the time and skill sets of the ASP professionals. For example, if the ASP includes an ID-trained pharmacist, the 4 CID 2018:XX (XX XXXX) Ostrowsky et al

5 Table 6. Variables Influencing Full-Time Equivalent Needs Facility Type Facility and patient complexity Number of beds Case mix index Number and diversity of prescribers Average daily census Referral patterns Pharmacy support Level of pharmacist training Amount of ASP-dedicated full-time equivalents Local resistance patterns Clinical laboratory support Determination of desired ASP activities Compliance with ASP core elements Enhanced approaches Abbreviation: ASP, antimicrobial stewardship program. time required of the ID physician may be less. If, however, the ASP pharmacist is not ID trained, the ID physician will have to assume a larger role in providing content expertise in infectious diseases and in performing daily interventions and should be reimbursed appropriately. The following examples demonstrate possible scenarios and staffing considerations: Example 1: Facility A is a community hospital with 300 acute care beds, of which 25 are intensive care unit (ICU) beds. The hospital has a case mix index (CMI) of 0.6 and exhibits low rates of infections caused by multidrug-resistant organisms (MDROs) and C. difficile. The hospital s ASP consists of a pharmacist who is not ID trained and who is allotted 0.2 FTEs for stewardship duties. Since the ID physician who leads the program must take on additional tasks that the pharmacist is not trained to perform, the physician is given 0.3 FTEs to ensure the effectiveness of the program. Example 2: Facility B is a tertiary care academic medical center with 800 acute care beds, of which 185 are designated as ICU beds. It is a major referral center for a large catchment area, including several long-term acute care hospitals, skilled nursing facilities, and rehabilitation facilities. In addition to medical, surgical, neonatal, pediatric, and cardiac ICUs, additional specialty services include adult and pediatric bone marrow transplantation, a congenital heart center, a burn unit, and trauma, neonatal, and neurosurgical ICUs. Its CMI is The hospital normally operates at 90% 95% capacity. The hospital is located in an area where rates of infections due to MDROs and C. difficile are elevated and increasing. To meet the needs of this highly complex institution, an ASP was begun with 2 ID-trained Doctors of Pharmacy (PharmDs) with 1.75 FTEs allotted to stewardship duties and 2 ID physicians (1 adult trained and 1 pediatric trained) to co-lead the ASP and share 1.25 FTEs. Example 3: Facility C is a skilled nursing facility with 64 beds. Many patients are transferred from hospital B and spend an average of 2 4 weeks at hospital C. Because of the close relationship with hospital B, hospital C shares the same problem of elevated rates of infections due to MDROs and C. difficile. It operates at >95% capacity. Hospital C does not have ID-trained pharmacists and has a single ID physician who was not interested in providing stewardship services. Therefore, the hospital contracted for 0.15 FTEs with 1 of the ID-trained pharmacists and 0.1 FTEs for 1 of the ID physician leaders of the ASP at hospital B to provide stewardship services to hospital C. The ID Physician Leadership of ASPs in Action Throughout the country, many ASPs are already using ID physician leadership to deliver robust results. The examples below explicitly illustrate the role of ID ASP physicians in several different institutions. Example 1: The ID physician-led ASP at Miami Valley Hospital in Dayton, Ohio, reduced broad-spectrum antibiotic use in the ICU by 18% in its first year and by 28% after 2 years without a negative impact in regard to ICU mortality or length of stay. Antimicrobial days of therapy within the entire hospital dropped 5% 7% each of the first 2 years, with a cost savings of more than $1 million. The physician leader conducts most of the physician education and communication with providers on complex cases and issues. He also leads the ASP meetings, which are attended by all ID physicians at the facility and within the network. The ASP committee has been working to develop local guidelines for cellulitis, urinary tract infection, and pneumonia to help use appropriate antimicrobial selection and duration of therapy. In conjunction with the information technology department, the ASP provider has helped develop tools within the electronic medical record to rapidly clarify recent antimicrobial exposures during the current and past admissions to improve appropriate antimicrobial selection. Quarterly meetings are held with the hospital physicians to ensure familiarity between the ASP service and providers who are being contacted with the recommendations. Secure texting has made the ASP service more efficient and allowed 2-way communication in real time without relying of phone calls for each recommendation. Example 2: Under an ASP at the North Shore University Health System in Illinois, an ID physician reviews all new antimicrobial prescriptions and uses an antimicrobial assist tool to agree with the regimen started by the primary care physician or to suggest a therapeutic change or a formal ID consult. Pharmacists can directly recommend such changes, and ID physicians can mediate disagreements that may arise between ASP pharmacists and treating physicians. This ASP initially found that 25% of antimicrobial treatment in the facility was unnecessary. Importantly, more than 70% of the ASP ID physician and pharmacist recommendations were accepted, significantly reducing unnecessary antimicrobial ID Physicians: Leading Stewardship CID 2018:XX (XX XXXX) 5

6 use. This same group also identified that 5% of patients not needing antimicrobial therapy go on to develop CDIs when they are given unnecessary treatment. Example 3: The ID physician led multicampus ASP at Montefiore Medical Center in Bronx, Ne York, showed a 10% 15% reduction in antimicrobial use across all classes and estimated direct pharmacy savings of more than $ in its first 2 years. This has translated into greater appropriateness of antimicrobial use across several syndromes. For example, the use of appropriate antimicrobial agents for community-acquired pneumonia, which was a CMS core measure at the time, improved by more than 30%. The program has evolved since its inception in The ASP also more recently reduced CDI rates by up to 40% at campuses within the system. The antibiogram at all sites improved as well, with quinolone susceptibility of gram-negative bacilli improving by more than 10%. ID physicians (both adult and pediatric) oversee all aspects of this ASP, including education, development of prescribing tools, integration of diagnostics, prior authorization, and case review. Education activities are tailored to different prescriber types and include distribution of local microbiology data and a prescribing application for personal electronic devices. This includes activities tailored to the pediatric population at the children s hospital and across the spectrum of care (eg, emergency room, ambulatory care, and outpatient antimicrobial therapy program). The pediatric program includes a pediatric ID physician and focuses on traditional specialized dosing systems for children and more complex algorithms for high-risk pediatric populations such as those undergoing bone marrow transplantation and requiring ICU care. Example 3: The ASP at Vanderbilt University Medical Center, Nashville, Tennessee, includes separate ASPs for the adult hospital and free-standing children s hospital. Each ASP includes an ID physician medical director and ID pharmacist co-leader. The adult and pediatric ASPs function independently but report to the same institutional pharmacy and therapeutics and quality committees. The children s hospital ASP conducts daily audit and feedback of broad-spectrum antimicrobial prescriptions on all inpatients and communicates recommendations through face-to-face discussions with hospital teams during daily handshake stewardship rounds. Both the physician and pharmacist co-leaders perform the stewardship interventions. In the 5 years since the ASP started at the children s hospital, the days of therapy/1000 patient-days have decreased by 50% and annual antimicrobial costs have decreased by $ MODELS FOR ACCESS TO ID PHYSICIAN-LED ASPS Ideally all types of facilities could implement their own ID physician led ASPs, but on-site ID presence may be a limited resource, particularly in small and rural hospitals and in other healthcare settings apart from acute care hospitals. Several models exist that can extend the reach of the ID physician to direct ASP activities at all types of facilities. For example, contractual agreements can permit ID physicians to provide off-site leadership combined with limited in-person services in collaboration with on-site personnel. These arrangements can be low tech and scaled according to facility size and resources. A recent review of ASPs in small hospitals suggested multiple strategies for increasing ID physician leadership in these settings, including pooling resources among multiple facilities, using healthcare system resources, taking advantage of state-based efforts and collaboratives, and using telehealth [22]. Although not essential to development of a remote stewardship program, innovative technologies can be used to develop a tele-antimicrobial stewardship program (TASP) in healthcare settings where an ID physician may not be regularly present (Table 6). A TASP allows physicians in urban centers to connect to other hospitals and facilities regardless of geography, allowing a single ID physician to lead multiple ASPs outside their home institution. TASP technology is fully capable of ensuring compliance with privacy and security requirements, and options exist in every price sector (Table 7). ID physician led TASPs have been demonstrated to result in measurable clinical benefits (Table 8). In one example, the Ukiah Valley Medical Center (UVMC) in California initiated an ASP in 2013 that used TASP to facilitate ID physician leadership. The program began with a comprehensive review of current prescribing, the hospital antibiogram, and the antimicrobial formulary. An ASP committee was assembled that then developed treatment guidelines. In addition, the TASP ID Table 7. Healthcare Settings Amenable to Tele-Antimicrobial Stewardship Programs Long-term acute care hospitals/facilities Rehabilitation facilities Dialysis centers Small and rural hospitals Correctional facilities Ambulatory surgical centers Outpatient clinics Hospitals that care for children but do not have pediatric antimicrobial stewardship programs or pediatric infectious diseases services Table 8. Benefits of Infectious Diseases Physician-Led Tele- Antimicrobial Stewardship Programs Allows access to infectious diseases physician expertise Single forum for communication Reduces fatigue due to travel Acts as a workforce multiplier 6 CID 2018:XX (XX XXXX) Ostrowsky et al

7 physician conducted a series of educational activities and daily tele-stewardship ASP rounds to review antibacterial therapies. In the first 6 months of this program, UVMC experienced a 1.4% reduction in antimicrobial days and a savings in antimicrobial costs of $16 per patient-day, translating to a savings of $ In 2014, the number of antimicrobial days was further reduced by 2.3% and antimicrobial cost decreased by an additional $27 per patient-day. The result has been a total reduction of $43 per patient-day compared to 2012 levels, translating to a savings of $ in antimicrobial costs at UVMC [23]. of their involvement in hospital epidemiology, quality improvement, infection prevention, and patient safety activities. ID physicians are best suited to drive the culture change necessary to establish stewardship as a valuable, widely accepted practice across the healthcare community that changes the behaviors of fellow clinicians (Figure 1). Further, ID physicians have a distinct understanding of the public health impacts of antimicrobial stewardship and antimicrobial resistance and enjoy a connection to the broader public health system, all of which give them the ability to impact population health. SUMMARY OF RATIONALE FOR ID PHYSICIAN LEADERSHIP OF ASPS ID physicians are well equipped to lead multidisciplinary ASPs given their training, expertise, and experience. An ASP should also include at least 1 pharmacist, ideally with subspecialty training in ID. While ID physicians and pharmacists may often have the most central roles in an ASP, all members of the ASP team, including microbiologists and infection preventionists, provide distinct skills of great value. ID physicians possess unique expertise regarding the diagnosis and treatment of infections. They are already viewed as leaders in many institutions because RECOMMENDATIONS IDSA, SHEA, and PIDS are committed to optimizing patient outcomes and minimizing the unintended consequences of antimicrobial use through proper and effective antimicrobial stewardship. Implementing the following recommendations will ensure that ASPs are well developed and properly led. 1: ID physicians should lead multidisciplinary ASP teams and can help maximize the contributions of all team members. Pharmacists, ideally those trained in infectious diseases, are essential partners. Nurses, microbiologists, and infection Figure 1. The multiple skills of an infectious diseases physician as the antimicrobial stewardship programs leader translate into positive impacts for both the patient and the institution. Abbreviations: CLABSI, central line associated bloodstream infections; C. difficile, Clostridium difficile. ID Physicians: Leading Stewardship CID 2018:XX (XX XXXX) 7

8 Table 9. Potential Positive Impact of an Infectious Diseases Physician-Led Antimicrobial Stewardship Program Initial Clinical Vignette: A patient with sepsis in a hospital without an ID Physician-Led ASP Modified Clinical Vignette: A patient with sepsis in a hospital with an ID Physician-Led ASP Potential Points of Impact: An ASP ID physician has the ability to: Patient Smith, a 60-year-old man with type 2 diabetes mellitus, was hospitalized from home with sepsis. The admitting team in the ICU ordered blood cultures and broad-spectrum antimicrobials. The next day, the blood cultures were positive. The hospital used a new PCR-based rapid identification method that indicated that the bloodstream organism was highly antimicrobial susceptible. The pharmacist charged with managing the hospital s ASP appropriately recommended a change to a narrower-spectrum antimicrobial based on the susceptibility test results. However, the patient s physician was not comfortable relying on the advice of a nonphysician and therefore continued broad-spectrum antimicrobials. While the patient was recovering from the bloodstream infection, he developed Clostridium difficile colitis consequent to the exposure to the broad-spectrum antimicrobials. Due to colonic inflammation, Mr. Smith next developed a second bloodstream infection, this time caused by an intestinal organism that was highly antimicrobial resistant, another consequence of the broad-spectrum antimicrobials. Although he was eventually stabilized after a 3-week hospital stay, he was unable to care for himself at home and so was sent to a long-term acute care hospital. While at the acute care hospital, his C. difficile was transmitted to his roommate, whose discharge was delayed due to this infection. Patient Smith is a 60-year-old man with type 2 diabetes mellitus who was admitted from home with sepsis. The admitting team in the ICU ordered blood cultures and empiric antimicrobial. Their initial antimicrobial choice is directed by educational materials and the antibiogram developed by the ID physician led ASP team, the microbiology lab, and the ICU Improvement team. The next day, the blood cultures were positive. The hospital used a new PCR-based rapid identification method that indicated that the bloodstream organism was highly antibiotic susceptible. Prior to implementation of this technology, the ID physician leader of the ASP created a protocol by which these results trigger an immediate review of the ordered antimicrobials. The ASP pharmacist contacts the primary team to discuss narrowing antibiotic therapy. When the patient s physician is reluctant to alter treatment, the pharmacist brings the issue to the attention of the ASP ID physician leader, who then contacts the primary team and provides the physician support of the recommendations given by the pharmacist. The interaction also provides broader education regarding testing, local microbiology, and prescribing for future patients. Mr. Smith s physician agrees to change his regimen to a single, narrow-spectrum agent. Mr. Smith rapidly improves. Be knowledgeable about local resistance and national prescribing trends Impact antimicrobial choice, dosage, duration Ability to work with and lead prescribers from multiple disciplines Lead the effort to use new diagnostics Work to integrate diagnostics and ASP Act as an experienced leader Act as an activator of change Integrate microbiology and diagnostic information Understand use, side effects, and cost of adverse outcomes of antimicrobials Create communication systems for timely receipt of results Ensure that other physicians understand the knowledge and skills of ASP pharmacists Communicate effectively regarding microbiological results and complex infectious scenarios to prescribers of different levels Influence the prescribing practice of other physicians and nonphysician prescribers Impact resistance, C. difficile, and other adverse outcomes Mr. Smith is discharged home in less than 1 week and makes a complete recovery. Drive quality improvement and patient safety through optimal antimicrobial prescribing The prospective roommate does not develop C. difficile and is discharged as scheduled. Have an understanding of the complementary nature of ASP and infection prevention and control issues Be able to work across the spectrum of care Potentially impact antimicrobial use, antimicrobial resistance, and other adverse effects of antimicrobial overuse in nonacute care settings The term antimicrobial includes antibiotics, antivirals, antifungals, and antiparasitics and biologic agents such as antibodies with activity against microorganisms. Abbreviations: ASP, antimicrobial stewardship programs; ICU, intensive care unit; ID, infectious diseases; PCR, polymerase chain reaction. 8 CID 2018:XX (XX XXXX) Ostrowsky et al

9 preventionists are also key ASP team members bringing valuable and unique expertise. 2: Appropriate resources, including reimbursement and protected time for stewardship activities, must be provided to ID physicians and other members of the stewardship team. Resource allocations, including FTEs, must be scaled to the facility type and size, as well as patient population. Duties required to lead ASPs must be recognized as distinct from other roles played by ID physicians. 3: Different models must be supported based on institutional needs for effective ID physician led stewardship that varies across all types of healthcare facilities in the continuum of care. Contractual agreements, part-time and off-site ID physician services, resource sharing among compatible facilities and across health systems, and use of telemedicine tools can all be helpful in achieving this goal. CONCLUSIONS The national landscape has changed rapidly to recognize the importance of ASPs across the spectrum of care. To be effective, ASPs must be multidisciplinary, with skilled leadership from professionals who are dedicated and compensated for ASP work. IDSA, SHEA, and PIDS are committed to providing the rationale, evidence and concrete examples to demonstrate that ID physicians are uniquely trained, experienced and best suited to lead ASPs. ID physician led ASPs can improve both individual patient outcomes and facility health measures, reducing harm and preserving antimicrobial effectiveness for the entire population. To this end, the case vignette from the beginning of this white paper is presented alongside a modified version to show the potential impact of an ID physician led ASP on the management and outcome of a patient with sepsis Table 9. The table highlights the key opportunities where an ID physician leading an ASP can intervene to make and enact meaningful improvements for this patient, which translates into positive outcomes for other patients and facilities. This document serves as a call to action for stakeholders. Recent ASP mandates can deliver their intended goals to reduce drivers of resistance, improve patient care, and provide great value to healthcare facilities and communities when implemented with appropriate leadership and resources. Notes R. A. B. reports compensation from the National Institutes of Health, Antibacterial Resistance Leadership Group; possesses a Veterans Affairs Merit Review Award; and reports compensation for preclinical studies unrelated to this manuscript from Merck, Wockhardt, Allergan, Allereca, and Roche. S. D. reports compensation for speakers bureau participation for Merck and Allergan and compensation for research support from Diatherix. D. N. G. reports compensation for consulting with Biomerieux, Biofire, Merck, and GlaxoSmithKline. S. A. C. reports compensation unrelated to this manuscript for consulting with Novartis and Theravance. E. J. S. reports receiving contributed product from Sage, Molnlycke, and Medline for ABATE and SWAP OUT trials (companies that contribute product have no role in design, conduct, analysis, or publication unrelated to this manuscript). All other authors: no reported conflicts. All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed. References 1. World Health Organization. Global Action Plan on Antimicrobial Resistance, Fishman N. Policy statement on antimicrobial stewardship by the Society for Healthcare Epidemiology of America (SHEA), the Infectious Diseases Society of America (IDSA), and the Pediatric Diseases Society (PIDS). 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