Review
Engaging Pharmacy Students, Residents, and Fellows in Antimicrobial Stewardship
Journal of Pharmacy Practice 1-7 ª The Author(s) 2013 Reprints and permission: sagepub.com/journalsPermissions.nav DOI: 10.1177/0897190013516506 jpp.sagepub.com
Elias B. Chahine, PharmD, BCPS (AQ-ID)1, Rania M. El-Lababidi, PharmD, BCPS (AQ-ID), AAHIVP2, and Mariette Sourial, PharmD1
Abstract Antimicrobial stewardship programs are mainly established by infectious diseases physicians and infectious diseases-trained clinical pharmacists with the goal of optimizing patients’ outcomes while halting antimicrobial resistance, decreasing adverse events, and controlling health care cost. The role of the infectious diseases-trained clinical pharmacist in antimicrobial stewardship is well established; however, there are not enough formally trained pharmacists to assume the challenging responsibilities of the steward coordinator. The purpose of this article was to review the available literature and resources and propose a model to engage introductory pharmacy practice experience students, advanced pharmacy practice experience students, postgraduate year (PGY) 1 pharmacy residents, PGY2 infectious diseases pharmacy residents, and PGY2 or PGY3 infectious diseases pharmacy fellows in antimicrobial stewardship. Further studies are needed to assess and document the impact of pharmacy students and postgraduate trainees on antimicrobial stewardship programs. Keywords antimicrobial stewardship, pharmacy students, residents, fellows, pharmacy education
Introduction The World Health Organization has identified antimicrobial resistance as a global concern and has devoted the theme for World Health Day 2011 ‘‘No Action Today, No Cure Tomorrow’’ to combat antimicrobial resistance.1,2 The Centers for Disease Control and Prevention have stated that some bacteria have developed mechanisms of resistance for which there are currently no available effective antibiotics. They have dedicated an annual event ‘‘Get Smart About Antibiotics Week’’ since November 2008 to raise awareness about this problem.3,4 The Infectious Diseases Society of America (IDSA) had launched a campaign in 2004 highlighting the crisis resulting from an alarming increase in antimicrobial resistance coupled with a drastic decline in antimicrobial research and development.5,6 In an effort to promote the judicious and appropriate use of antimicrobials, the IDSA and the Society for Healthcare Epidemiology of America (SHEA) have released guidelines to assist institutions in developing programs to enhance antimicrobial stewardship with the goals of optimizing patients’ outcomes while limiting the spread of antimicrobial resistance, minimizing adverse events, and controlling health care costs.7 The IDSA/SHEA guidelines emphasize 2 proactive core strategies as the foundation of antimicrobial stewardship. The first is prospective audit with intervention and feedback and the second is formulary restriction and preauthorization. Prospective audit with intervention and feedback preserves the autonomy of the prescriber while allowing the steward coordinator to evaluate the appropriateness of antimicrobial agents and recommend alternative therapy. Formulary restriction
and preauthorization involve limiting the use of an antimicrobial agent to certain indications, patient populations, or services based on local antimicrobial resistance patterns, patients’ characteristics, and cost. Other interventions that can be used in conjunction with these core principles include educating prescribers, developing guidelines and clinical pathways, using antimicrobial order forms, assessing combination therapy, streamlining or de-escalation of therapy, dose optimization, and parenteral-to-oral conversion.7 According to the IDSA/SHEA guidelines, infectious diseases physicians and infectious diseases-trained clinical pharmacists should be the core members of a multidisciplinary antimicrobial stewardship team that may also include clinical microbiologists, information system specialists, infection control professionals, and hospital epidemiologists.7 Due to lack of infectious diseasestrained clinical pharmacists, pharmacists at various stages of training have taken the initiative to further develop their knowledge, skills, values, and attitudes in infectious diseases pharmacotherapy and have successfully implemented antimicrobial stewardship programs at their institutions.8-14 Insights from the Society of
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Palm Beach Atlantic University, West Palm Beach, FL, USA Cleveland Clinic Abu Dhabi, Abu Dhabi, United Arab Emirates
Corresponding Author: Elias B. Chahine, Palm Beach Atlantic University, 901 S. Flagler Dr, West Palm Beach, FL 33416, USA. Email: [email protected]
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Table 1. Proposed Involvement of Pharmacy Students, Residents, and Fellows in Antimicrobial Stewardship Programs. Didactic students Prospective audit with intervention and feedback Formulary restriction and preauthorization Education Guidelines and clinical pathways Antimicrobial order forms Combination therapy Streamlining/de-escalation of therapy Dose optimization Parenteral-to-oral conversion
X
IPPE students
X
X X
APPE students
X X X X X X X
PGY1 residents
PGY2 ID residents
PGY2/3 ID fellows
X
X
X
X X X X X X X X
X X X X X X X X
X X X X X X X X
Abbreviations: IPPE, introductory pharmacy practice experience; APPE, advanced pharmacy practice experience; PGY1, postgraduate year 1; PGY2, postgraduate year 2; ID, infectious diseases; PGY2/3, postgraduate year 2 and 3.
Infectious Diseases Pharmacists (SIDP) and a statement from the American Society of Health-System Pharmacists (ASHP) supporting the vital role of the pharmacist in antimicrobial stewardship were released in 2009 and 2010, respectively.15,16 Recommendations for training and certification of pharmacists in infectious diseases pharmacotherapy were provided by a joint opinion paper between SIDP and the American College of Clinical Pharmacy (ACCP) emphasizing the importance of residency training and board certification in pharmacotherapy for future pharmacists seeking a clinical position as infectious diseases-trained clinical pharmacists.17 Antimicrobial stewardship certificate programs are available to pharmacy residents, fellows, and practitioners through SIDP and Making a Difference in Infectious Diseases Pharmacotherapy.18,19 However, little has been written about the integration of pharmacy students and postgraduate trainees into antimicrobial stewardship services. This article reviews the role of pharmacy students, residents, and fellows in antimicrobial stewardship services. Table 1 highlights their proposed role at each stage of training.
Methods An electronic search of the PubMed database (from 2000 to July 2013) and Google Scholar using the terms antimicrobial stewardship, pharmacy students, pharmacy residents, pharmacy fellows, pharmacy education, and variant of these words was completed. Electronic searching was supplemented by manual searches of reference lists of relevant articles as well as information available from professional pharmacy organizations Web sites.
Didactic Instruction Educating pharmacy students about microorganisms, infectious diseases, and antimicrobials is an essential part of the pharmacy curriculum. According to the Accreditation Council for Pharmacy Education (ACPE) standards for the professional program leading to the doctor of pharmacy degree, students must complete college-level coursework that includes biological sciences before enrollment in the pharmacy program.20 Throughout the
professional program, the pharmacy curriculum must be designed to ‘‘prepare graduates with the professional competencies to enter pharmacy practice in any setting to ensure optimal medication therapy outcomes and patient safety’’ and must have both required and elective courses and experiences.20 In addition, according to the American Association of Colleges of Pharmacy Center for the Advancement of Pharmacy Education (CAPE), pharmacy students should be able to provide patient-centered care as well as population-based care.21 Although all pharmacy schools across the nation incorporate infectious diseases into their curricula, the extent and depth of instruction vary among institutions. For example, at Palm Beach Atlantic University, prepharmacy students are required to successfully complete a 4-credit microbiology course including laboratory before enrollment in the professional program.22 During the third professional year, pharmacy students are required to successfully complete a 5credit infectious diseases pharmacotherapy course where medicinal chemistry and pharmacology of antimicrobials are taught with therapeutics in an integrated fashion.23 The key learning outcome of the course is to ‘‘educate patients and health care professionals about the judicious and appropriate use of antimicrobials to optimize patients’ outcomes while halting resistance, decreasing adverse events, and controlling health care cost.’’ Pharmacy students may sometimes have the opportunity to take an elective course to further refine their abilities in antimicrobial pharmacotherapy before they go on advanced practice experiences.24,25 Colleges of pharmacy should consider not only integrating antimicrobial stewardship into their required therapeutics courses but also incorporating elective courses into their curricula to further prepare students for the antimicrobial stewardship services that they are likely to encounter during clinical practice.
Experiential Education Pharmacy practice experiences provide students an opportunity to apply what they learned in a classroom setting to patient care under the direct supervision of a preceptor. They
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are currently divided into introductory pharmacy practice experiences (IPPEs) and advanced pharmacy practice experiences (APPEs).20
IPPE Students According to the ACPE standards and the CAPE educational outcomes, IPPE students can be given the opportunity to shadow infectious disease specialists or any health care worker involved in infection control. This will enable them to have a preliminary overview of the duties involved in managing patients with infectious diseases and allow for interprofessional interactions, the basis for a team-based approach in antimicrobial stewardship. Students may also participate in activities such as conducting patient interviews, creating patient profiles, responding to drug information questions focusing on infectious diseases under the supervision of a licensed health care professional, collaborating with other health care professionals, participating in educational offerings, and learning how to use resources of the health care system to coordinate safe, accurate, and time-sensitive medication distribution.20,21 Specifically, IPPE students can help with interviewing patients to acquire a comprehensive medications list and patient information, for which they can identify patient-specific factors affecting health or pharmacotherapy. Utilizing all the information acquired, they can then put together and present a patient case within the realm of infectious diseases. Across all practice settings, IPPE students can be involved in performing the calculations required to compound and administer antimicrobials. They can also play a role in stressing adherence to antimicrobials. For example, they can participate in calling patients to ensure completion of therapy or simply confirm understanding of how to appropriately take a specific antimicrobial. Furthermore, they can participate in offering educational services designed to improve health and wellness of the general public with regard to infectious diseases, immunizations, and antimicrobial pharmacotherapy.
APPE Students As students advance in their pharmacy education, they acquire the necessary knowledge, skills, values, and attitudes to enable them to be more involved in direct patient care as required by ACPE.20 APPE students are also well positioned to fulfill the CAPE educational outcomes in the realm of patient care, systems management, and public health.21 Under the supervision of a licensed health care professional, students should be able to provide patient-centered care in collaboration with other health care providers in a team-based approach.21 They should relate therapeutic principles guided by evidence-based information while taking into account patient and populationspecific factors that may influence therapeutic outcomes.21 They should also assist in analyzing pharmacoeconomic data and conducting medication use review as well as proposing risk reduction strategies.21 Furthermore, APPE students should focus on promoting wellness and infectious disease
prevention.21 They should determine the validity of a prescription, calculate the correct dose, and develop a monitoring plan for a particular patient.21 Building upon IPPEs, APPE students are more equipped to assess the judicious and appropriate use of antimicrobials as part of a multidisciplinary team. During several APPEs, and on a daily basis, students can assess appropriateness of antimicrobial therapy including dose, route of administration, frequency, and duration of therapy as part of delivering care to their patients. Students can also monitor patients on antimicrobial therapy for efficacy and safety. For example, as part of an antimicrobial stewardship team, students can help interpret microbiology culture and sensitivity reports, recommend appropriate treatments, and document their interventions in patients’ profiles. Students can also conduct antibiotic drug use review and participate in the health system’s formulary process and therapeutic protocol development for antimicrobials. Similar to IPPE students, APPE students can also provide education to the public and health care professionals about various infectious diseases including patient education and counseling about antimicrobials and vaccines. By supporting existing antimicrobial stewardship programs during their clerkships, students will be better prepared to demonstrate the abilities necessary to practice as competent pharmacists upon graduation. Colleges of pharmacy should consider offering elective APPEs in antimicrobial stewardship for students interested to learn more about infectious diseases pharmacy practice.
Postgraduate Training Postgraduate pharmacy residencies are structured 1-year programs for graduates seeking additional training in pharmacy practice. At the time of writing, there were 833 PGY1 pharmacy residency programs and 54 PGY2 infectious diseases pharmacy residency programs with an ASHP accreditation status.26 PGY2/3 pharmacy fellowships are structured 2-year programs for graduates seeking additional training in pharmacy practice and research. At the time of writing, there were 9 infectious diseases fellowship programs including 4 that are peer reviewed by ACCP.27
PGY1 Pharmacy Residents Role of Pharmacy Residents in Resource-Limited Settings. According to the IDSA/SHEA guidelines, antimicrobial stewardship teams should be multidisciplinary in nature, with core members consisting of an infectious diseases physician and an infectious diseases-trained clinical pharmacist.7 Although this structure may be attainable in larger academic medical centers, in smaller private nonteaching hospitals with limited resources, this structure may not be feasible. The inclusion of pharmacy residents on the antimicrobial stewardship team may be one strategy to overcome resource limitations in such settings. For example, one report described an experience with antimicrobial stewardship in a 545-bed community teaching hospital.28 The team consisted of a noninfectious diseases-trained clinical
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pharmacist and 3 infectious diseases physicians. In all, 14 PGY1 residents and 2 PGY2 residents were also incorporated into the daily activities of this program. Pharmacy residents were assigned to the hospital’s antimicrobial stewardship service year round as part of their infectious diseases and internal medicine experiences. Residents performed most of the data collection and analysis prior to rounds under the supervision of the clinical pharmacist. The team made 550 recommendations over a 2-year period, 68% of which were accepted. The authors did not report on the impact on patient outcomes or cost savings resulting from the implementation of this program, although they did report that involvement of pharmacy residents minimized the time commitment of the infectious diseases physicians and the clinical pharmacist. Role of Pharmacy Residents in Initiating Antimicrobial Stewardship Programs. Pharmacy residents can be instrumental in helping initiate and sustain new antimicrobial stewardship programs. Residents can function as service extenders by providing daily patient profile review, renal dosing of antimicrobials, and intravenous to oral antimicrobial therapy conversion. In addition, as part of their research requirement, residents may assist in starting a new program by performing the needs assessment to identify resources and potential barriers during the early phases of program implementation.29 Such activities when performed by a resident occur at a minimum cost to the institution and may have the potential to produce cost savings. Steinberg JG et al described the impact of a pharmacist-initiated antibiotic review service in 2 general medicine inpatient units at a 550-bed community hospital.30 In this study, a PGY1 pharmacy resident supervised by 2 clinical pharmacists performed most of the antibiotic order review and patient evaluation during weekdays over an 18-week study period, which included a retrospective chart review phase followed by an intervention phase. Fiftyfive recommendations were made to physicians during the intervention phase of the study, 71% of which were accepted. The majority of recommendations made were for intravenous to oral antibiotic conversions (17 of 55), followed by renal dose antibiotic adjustments (15 of 55), and interventions for antibiotic therapy lacking an indication (13 of 55). Total dollar savings recorded during the study period were US$12 000. There was no difference between the average length of stay recorded for patients monitored in this program (8.53 days vs 8.15 days, P ¼ 0.495). No other patient outcomes were recorded in this study. Of note is that this institution had in place automatic renal dose adjustment protocols and intravenous to oral conversion protocols for a selected group of antimicrobials, prior to the study implementation. In this study, the PGY1 pharmacy resident was employed in the early phases of implementation of a pharmacist-led antibiotic stewardship service. Furthermore, involvement of residents-assisted staff pharmacists in completing clinical tasks may not have been routinely addressed due to staffing shortages or workload challenges. In another report, pharmacy residents were incorporated during the initiation phases of an antimicrobial stewardship program. Ijo and Feyerharm reported their experience in providing
prospective audit and feedback over a 4-month period in the intensive care unit of a 378-bed community hospital.31 In this report, pharmacy residents were included as part of a pharmacist-led antimicrobial stewardship team and assisted clinical pharmacists in the intensive care unit in performing prospective audit and feedback to prescribers. Although therapy interventions were only performed during weekdays, this pharmacy team was able to document 93 recommendations. The majority of interventions in this study were for dose optimization (43%). Drug substitution, streamlining, and drug discontinuation accounted for 17%, 13%, and 11%, respectively. The authors reported a mortality rate of 14% and a mean length of stay of 6 days for the patients monitored in this program. Acceptance rates of antibiotic therapy interventions were not reported in this study, and a financial loss of US$192 was documented, which the authors attributed to the limited number of interventions captured during the study period.
PGY2 Infectious Diseases Pharmacy Residents Maintaining and Expanding Existing Antimicrobial Stewardship Programs. Pharmacy residents and in particular PGY2 infectious diseases residents can also be instrumental in maintaining or expanding antimicrobial stewardship services as part of their training. Current ASHP standards for PGY2 residencies and in particular infectious diseases require residents to take a leadership role in improving medication use systems at their institutions, which includes antimicrobial utilization.32 In addition, involvement of residents in antimicrobial stewardship teams fosters further growth and development of stewardship programs. Daily Activities of PGY2 Residents in Antimicrobial Stewardship Programs. Some examples of how PGY2 residents, in particular those training in infectious diseases, may be involved in the daily activities of an antimicrobial stewardship program include participating in prospective audit and feedback to prescribers, performing antimicrobial de-escalation, optimizing antimicrobial therapy dosing, performing intravenous to oral therapy conversion, providing extended clinical coverage hours through on-call programs, and educational opportunities to pharmacists and other health care providers. In addition to contributing to the daily activities of an antimicrobial stewardship program, PGY2 residents, and in particular those training in infectious diseases, also foster innovation and research that help elucidate new findings or contribute to confirm already established concepts. Role of PGY2 Residents in Extending Antimicrobial Stewardship Services. Acute care institutions often struggle to provide high-level clinical care, including antimicrobial stewardship services, at all times, particularly on evenings, weekends, and holidays. In this setting, pharmacy residents during their PGY2 training can be especially helpful in extending the provision of antimicrobial stewardship services after business hours through on-call residency programs. Such a program is described in the
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literature, where extended clinical hours were supported by pharmacy residents through a 24-hour on-call program, at a large teaching hospital with an existing antimicrobial stewardship team.33 Although this on-call residency program provided a broad range of clinical pharmacy services, the program largely supported the hospital’s existing antimicrobial management team through the provision of antimicrobial therapy recommendations and pharmacokinetic dosing recommendations for antibiotics, after business hours, as evidenced by the number of encounters recorded. Although not widely described in the literature, PGY2 residents, through an on-call program, may also provide extended hours for pharmacist-led priorapproval systems for restricted antimicrobials in hospitals that have such a system in place. Such a program may assist in preventing the phenomenon of ‘‘Stealth Dosing’’—which is waiting until after the prior-approval period ends to prescribe restricted antimicrobials—as recently described by LaRosa et al.34 Education. Education is recognized as an essential component of any antimicrobial stewardship program.7 Part of the ASHP residency training requirements includes the ability to provide education to various groups, in both small and large formats. PGY2 residents can be instrumental in leading educational programs related to antimicrobial stewardship, resulting in the education of pharmacists, pharmacy technicians, nurses, physicians, and other individuals in the organization. When education is used along with active interventions, it can help influence prescribing behaviors. Scholarship and Innovation. According to the ASHP residency accreditation standards, residents are required to cultivate their own project management skills.32 Such skill development may take the form of formal research, continuous quality improvement initiatives, medication use evaluations, or practice service implementation (eg, protocol implementation with measurement of impact or quality assurance initiatives) that benefits the host institution. Examples of such resident-led antimicrobial stewardship research initiatives can be found in the literature.35-38
PGY2/3 Infectious Diseases Pharmacy Fellows Pharmacy fellowship programs are highly individualized and variable with respect to practice experiences. In 2004, ACCP developed guidelines for research fellowship training programs that wish to be voluntarily peer-reviewed by the College.39 A recent report outlines the involvement of infectious diseases pharmacy fellows in an institution’s antimicrobial stewardship program, although no details were provided on the specifics of this involvement.40 Although, fellowship programs are not deemed as being equivalent to PGY2 residency programs in terms of clinical practice competency,15 fellows have contributed to antimicrobial stewardship advancement primarily through research and scholarship, examples of which can be found in the pharmacy and the infectious diseases literature.41-45
Pharmacy Practice Model Initiative The Pharmacy Practice Model Initiative (PPMI) recommends curricular changes in colleges of pharmacy to prepare students for a larger role in drug therapy management, pharmacy informatics, medication safety, and transitions of care which are essential for effective antimicrobial stewardship services.46 Pharmacy educators should follow the example of medical educators and assess pharmacy students’ perceptions, attitudes, and knowledge of antimicrobial stewardship and implement changes in pharmacy curricula based on the PPMI recommendations.47 Pharmacists should utilize students and residents as pharmacist extenders in the provision of antimicrobial stewardship services provided that the appropriate level of training, oversight, and quality assurance is met in alignment with the critical requirements for health-system pharmacy practice models to achieve optimal use of antimicrobials.48 This layered learning practice model from attending pharmacist to resident to student has already been implemented in several institutions across the nation49,50; however, further studies are needed to assess and document the impact of pharmacy students and postgraduate trainees on antimicrobial stewardship programs.
Conclusions Didactic instruction in antimicrobial pharmacotherapy provides students with the foundational knowledge and skills necessary for experiential education. IPPEs and APPEs give students the opportunity to get involved in antimicrobial stewardship programs. PGY1 pharmacy residency and PGY2 infectious diseases pharmacy residency enable postgraduate trainees to serve on antimicrobial stewardship programs. Infectious diseases pharmacy fellowships empower postgraduate trainees to contribute to the research and scholarship of antimicrobial stewardship. At each stage of training, students, residents, and fellows should take full advantage of their roles in antimicrobial stewardship, document their activities, and disseminate their findings. In light of expected stricter regulatory requirements for the judicious and appropriate use of antimicrobials in the upcoming years, the demand for infectious diseasestrained clinical pharmacists is likely to rise. Therefore, adequate training of pharmacy students and expansion of residency and fellowship programs are essential to prepare the necessary manpower to sustain and further develop antimicrobial stewardship programs. Declaration of Conflicting Interests The author(s) declared the following potential conflicts of interest with respect to the research, authorship, and/or publication of this article: Dr Chahine serves on the speakers’ bureaus for Cubist Pharmaceuticals, Inc and Forest Pharmaceuticals, Inc. Drs El-Lababidi and Sourial have nothing to disclose.
Funding The author(s) received no financial support for the research, authorship, and/or publication of this article.
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31. Ijo I, Feyerharm J. Pharmacy intervention on antimicrobial management of critically ill patients. Pharm Pract. 2011;9(2): 106-109. 32. American Society of Health-System Pharmacists. Educational outcomes, goals, and objectives for postgraduate year two pharmacy residencies in infectious diseases, August 2007. http:// www.ashp.org/menu/Accreditation/ResidencyAccreditation. aspx. Accessed April 13, 2013. 33. Smith KM, Hecht KA, Armistead JA, et al. Evolution and operation of a pharmacy residency on-call program. Am J Health-Syst Pharm. 2003;60(21):2236-2241. 34. LaRosa LA, Fishman NO, Lautenbach E, et al. Evaluation of antimicrobial therapy orders circumventing an antimicrobial stewardship program: investigating the strategy of ‘‘stealth dosing’’. Infect Control Hosp Epidemiol. 2007;28(5):551-556. 35. Ryzner KL. Evaluation of aminoglycoside clearance using the modification of diet in renal disease equation versus the cockcroft-gault equation as a marker of glomerular filtration rate. Ann Pharmacother. 2010;44(6):1030-1037. 36. Novell MJ, Morreale CA. The relationship between inpatient fluoroquinolone use and Clostridium difficile-associated diarrhea. Ann Pharmacother. 2010;44(5):826-831. 37. O’DellKM, Shah SA. Evaluation of pharmacy practice residents’ research abstracts and publication rate. J Am Pharm Assoc. 2012; 52(4):524-527. 38. Wong JR, Bauer KA, Mangino JE. Antimicrobial stewardship pharmacist interventions for coagulase-negative staphylococci positive blood cultures using rapid polymerase chain reaction. Ann Pharmacother. 2012;46(11):1484-1490. 39. American College of Clinical Pharmacy. Guidelines for clinical research fellowship training programs; October 2004. http:// www.accp.com/resandfel/guidelines.aspx. Accessed July 31, 2013. 40. Palmer HR, Weston J, Gentry L, et al. Improving patient care through the implementation of an antimicrobial stewardship program. Am J Health Syst Pharm. 2011;68(22):2170-2174.
41. Esterly J, Richardson CL, Eltoukhy NS, et al.Genetic mechanisms of antimicrobial resistance of Acinetobacter baumanii. Ann Pharmacother. 2011;45(2):218-222. 42. DeRyke CA, Kuti JL, Mansfield D. Pharmacoeconomics of continuous versus intermittent infusion of piperacillin-tazobactam for the treatment of complicated intraabdominal infection. Am J Health Syst Pharm. 2006:63(8);750-755. 43. DeRyke CA, Sutherland C, Zhang B. Serum bactericidal activities of high-dose daptomycin with and without coadministration of gentamicin against isolates of Staphylococcus aureus and enterococcus species. Antimicrob Agents Chemother. 2006;50(11): 3529-3534. 44. Clay PG, Rathbun RC, Siater LN. Management protocol for abacavir-related hypersensitivity reaction. Ann Pharmacother. 2000;34(2):247-249. 45. Gums JG, Tancey Jr RW, Hamilton CA, et al. A randomized, prospective study measuring outcomes after antibiotic therapy intervention by a multidisciplinary consult team. Pharmacotherapy. 1999;19(12):1369-1377. 46. The consensus of the pharmacy practice model summit. Am J Health-Syst Pharm. 2011;68(12):1148-1152. 47. Abbo LM, Cosgrove SE, Pottinger PS, et al. Medical students’ perceptions and knowledge about antimicrobial stewardship: how are we educating our future prescribers? Clin Infect Dis. 2013; 57(5):631-638. 48. Shane R. Critical requirements for health-system pharmacy practice models that achieve optimal use of medicines. Am J Health Syst Pharm. 2011;68(12):1101-1111. 49. ASHP Intersections. With students’ help, pharmacists reach every patient at Cleveland Clinic Florida. http://www.ashpintersections. org/2013/03/with-students-help-pharmacists-reach-every-patientat-cleveland-clinic-florida/. Accessed August 1, 2013. 50. ASHP Intersections. The layered learning practice model: toward a consistent model of pharmacy practice. http://www.ashpfoundation.org/PinelliAbstract. Accessed August 1, 2013.
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Engaging Pharmacy Students, Residents, and Fellows in Antimicrobial Stewardship
Journal of Pharmacy Practice 1-7 ª The Author(s) 2013 Reprints and permission: sagepub.com/journalsPermissions.nav DOI: 10.1177/0897190013516506 jpp.sagepub.com
Elias B. Chahine, PharmD, BCPS (AQ-ID)1, Rania M. El-Lababidi, PharmD, BCPS (AQ-ID), AAHIVP2, and Mariette Sourial, PharmD1
Abstract Antimicrobial stewardship programs are mainly established by infectious diseases physicians and infectious diseases-trained clinical pharmacists with the goal of optimizing patients’ outcomes while halting antimicrobial resistance, decreasing adverse events, and controlling health care cost. The role of the infectious diseases-trained clinical pharmacist in antimicrobial stewardship is well established; however, there are not enough formally trained pharmacists to assume the challenging responsibilities of the steward coordinator. The purpose of this article was to review the available literature and resources and propose a model to engage introductory pharmacy practice experience students, advanced pharmacy practice experience students, postgraduate year (PGY) 1 pharmacy residents, PGY2 infectious diseases pharmacy residents, and PGY2 or PGY3 infectious diseases pharmacy fellows in antimicrobial stewardship. Further studies are needed to assess and document the impact of pharmacy students and postgraduate trainees on antimicrobial stewardship programs. Keywords antimicrobial stewardship, pharmacy students, residents, fellows, pharmacy education
Introduction The World Health Organization has identified antimicrobial resistance as a global concern and has devoted the theme for World Health Day 2011 ‘‘No Action Today, No Cure Tomorrow’’ to combat antimicrobial resistance.1,2 The Centers for Disease Control and Prevention have stated that some bacteria have developed mechanisms of resistance for which there are currently no available effective antibiotics. They have dedicated an annual event ‘‘Get Smart About Antibiotics Week’’ since November 2008 to raise awareness about this problem.3,4 The Infectious Diseases Society of America (IDSA) had launched a campaign in 2004 highlighting the crisis resulting from an alarming increase in antimicrobial resistance coupled with a drastic decline in antimicrobial research and development.5,6 In an effort to promote the judicious and appropriate use of antimicrobials, the IDSA and the Society for Healthcare Epidemiology of America (SHEA) have released guidelines to assist institutions in developing programs to enhance antimicrobial stewardship with the goals of optimizing patients’ outcomes while limiting the spread of antimicrobial resistance, minimizing adverse events, and controlling health care costs.7 The IDSA/SHEA guidelines emphasize 2 proactive core strategies as the foundation of antimicrobial stewardship. The first is prospective audit with intervention and feedback and the second is formulary restriction and preauthorization. Prospective audit with intervention and feedback preserves the autonomy of the prescriber while allowing the steward coordinator to evaluate the appropriateness of antimicrobial agents and recommend alternative therapy. Formulary restriction
and preauthorization involve limiting the use of an antimicrobial agent to certain indications, patient populations, or services based on local antimicrobial resistance patterns, patients’ characteristics, and cost. Other interventions that can be used in conjunction with these core principles include educating prescribers, developing guidelines and clinical pathways, using antimicrobial order forms, assessing combination therapy, streamlining or de-escalation of therapy, dose optimization, and parenteral-to-oral conversion.7 According to the IDSA/SHEA guidelines, infectious diseases physicians and infectious diseases-trained clinical pharmacists should be the core members of a multidisciplinary antimicrobial stewardship team that may also include clinical microbiologists, information system specialists, infection control professionals, and hospital epidemiologists.7 Due to lack of infectious diseasestrained clinical pharmacists, pharmacists at various stages of training have taken the initiative to further develop their knowledge, skills, values, and attitudes in infectious diseases pharmacotherapy and have successfully implemented antimicrobial stewardship programs at their institutions.8-14 Insights from the Society of
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Palm Beach Atlantic University, West Palm Beach, FL, USA Cleveland Clinic Abu Dhabi, Abu Dhabi, United Arab Emirates
Corresponding Author: Elias B. Chahine, Palm Beach Atlantic University, 901 S. Flagler Dr, West Palm Beach, FL 33416, USA. Email: [email protected]
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Table 1. Proposed Involvement of Pharmacy Students, Residents, and Fellows in Antimicrobial Stewardship Programs. Didactic students Prospective audit with intervention and feedback Formulary restriction and preauthorization Education Guidelines and clinical pathways Antimicrobial order forms Combination therapy Streamlining/de-escalation of therapy Dose optimization Parenteral-to-oral conversion
X
IPPE students
X
X X
APPE students
X X X X X X X
PGY1 residents
PGY2 ID residents
PGY2/3 ID fellows
X
X
X
X X X X X X X X
X X X X X X X X
X X X X X X X X
Abbreviations: IPPE, introductory pharmacy practice experience; APPE, advanced pharmacy practice experience; PGY1, postgraduate year 1; PGY2, postgraduate year 2; ID, infectious diseases; PGY2/3, postgraduate year 2 and 3.
Infectious Diseases Pharmacists (SIDP) and a statement from the American Society of Health-System Pharmacists (ASHP) supporting the vital role of the pharmacist in antimicrobial stewardship were released in 2009 and 2010, respectively.15,16 Recommendations for training and certification of pharmacists in infectious diseases pharmacotherapy were provided by a joint opinion paper between SIDP and the American College of Clinical Pharmacy (ACCP) emphasizing the importance of residency training and board certification in pharmacotherapy for future pharmacists seeking a clinical position as infectious diseases-trained clinical pharmacists.17 Antimicrobial stewardship certificate programs are available to pharmacy residents, fellows, and practitioners through SIDP and Making a Difference in Infectious Diseases Pharmacotherapy.18,19 However, little has been written about the integration of pharmacy students and postgraduate trainees into antimicrobial stewardship services. This article reviews the role of pharmacy students, residents, and fellows in antimicrobial stewardship services. Table 1 highlights their proposed role at each stage of training.
Methods An electronic search of the PubMed database (from 2000 to July 2013) and Google Scholar using the terms antimicrobial stewardship, pharmacy students, pharmacy residents, pharmacy fellows, pharmacy education, and variant of these words was completed. Electronic searching was supplemented by manual searches of reference lists of relevant articles as well as information available from professional pharmacy organizations Web sites.
Didactic Instruction Educating pharmacy students about microorganisms, infectious diseases, and antimicrobials is an essential part of the pharmacy curriculum. According to the Accreditation Council for Pharmacy Education (ACPE) standards for the professional program leading to the doctor of pharmacy degree, students must complete college-level coursework that includes biological sciences before enrollment in the pharmacy program.20 Throughout the
professional program, the pharmacy curriculum must be designed to ‘‘prepare graduates with the professional competencies to enter pharmacy practice in any setting to ensure optimal medication therapy outcomes and patient safety’’ and must have both required and elective courses and experiences.20 In addition, according to the American Association of Colleges of Pharmacy Center for the Advancement of Pharmacy Education (CAPE), pharmacy students should be able to provide patient-centered care as well as population-based care.21 Although all pharmacy schools across the nation incorporate infectious diseases into their curricula, the extent and depth of instruction vary among institutions. For example, at Palm Beach Atlantic University, prepharmacy students are required to successfully complete a 4-credit microbiology course including laboratory before enrollment in the professional program.22 During the third professional year, pharmacy students are required to successfully complete a 5credit infectious diseases pharmacotherapy course where medicinal chemistry and pharmacology of antimicrobials are taught with therapeutics in an integrated fashion.23 The key learning outcome of the course is to ‘‘educate patients and health care professionals about the judicious and appropriate use of antimicrobials to optimize patients’ outcomes while halting resistance, decreasing adverse events, and controlling health care cost.’’ Pharmacy students may sometimes have the opportunity to take an elective course to further refine their abilities in antimicrobial pharmacotherapy before they go on advanced practice experiences.24,25 Colleges of pharmacy should consider not only integrating antimicrobial stewardship into their required therapeutics courses but also incorporating elective courses into their curricula to further prepare students for the antimicrobial stewardship services that they are likely to encounter during clinical practice.
Experiential Education Pharmacy practice experiences provide students an opportunity to apply what they learned in a classroom setting to patient care under the direct supervision of a preceptor. They
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are currently divided into introductory pharmacy practice experiences (IPPEs) and advanced pharmacy practice experiences (APPEs).20
IPPE Students According to the ACPE standards and the CAPE educational outcomes, IPPE students can be given the opportunity to shadow infectious disease specialists or any health care worker involved in infection control. This will enable them to have a preliminary overview of the duties involved in managing patients with infectious diseases and allow for interprofessional interactions, the basis for a team-based approach in antimicrobial stewardship. Students may also participate in activities such as conducting patient interviews, creating patient profiles, responding to drug information questions focusing on infectious diseases under the supervision of a licensed health care professional, collaborating with other health care professionals, participating in educational offerings, and learning how to use resources of the health care system to coordinate safe, accurate, and time-sensitive medication distribution.20,21 Specifically, IPPE students can help with interviewing patients to acquire a comprehensive medications list and patient information, for which they can identify patient-specific factors affecting health or pharmacotherapy. Utilizing all the information acquired, they can then put together and present a patient case within the realm of infectious diseases. Across all practice settings, IPPE students can be involved in performing the calculations required to compound and administer antimicrobials. They can also play a role in stressing adherence to antimicrobials. For example, they can participate in calling patients to ensure completion of therapy or simply confirm understanding of how to appropriately take a specific antimicrobial. Furthermore, they can participate in offering educational services designed to improve health and wellness of the general public with regard to infectious diseases, immunizations, and antimicrobial pharmacotherapy.
APPE Students As students advance in their pharmacy education, they acquire the necessary knowledge, skills, values, and attitudes to enable them to be more involved in direct patient care as required by ACPE.20 APPE students are also well positioned to fulfill the CAPE educational outcomes in the realm of patient care, systems management, and public health.21 Under the supervision of a licensed health care professional, students should be able to provide patient-centered care in collaboration with other health care providers in a team-based approach.21 They should relate therapeutic principles guided by evidence-based information while taking into account patient and populationspecific factors that may influence therapeutic outcomes.21 They should also assist in analyzing pharmacoeconomic data and conducting medication use review as well as proposing risk reduction strategies.21 Furthermore, APPE students should focus on promoting wellness and infectious disease
prevention.21 They should determine the validity of a prescription, calculate the correct dose, and develop a monitoring plan for a particular patient.21 Building upon IPPEs, APPE students are more equipped to assess the judicious and appropriate use of antimicrobials as part of a multidisciplinary team. During several APPEs, and on a daily basis, students can assess appropriateness of antimicrobial therapy including dose, route of administration, frequency, and duration of therapy as part of delivering care to their patients. Students can also monitor patients on antimicrobial therapy for efficacy and safety. For example, as part of an antimicrobial stewardship team, students can help interpret microbiology culture and sensitivity reports, recommend appropriate treatments, and document their interventions in patients’ profiles. Students can also conduct antibiotic drug use review and participate in the health system’s formulary process and therapeutic protocol development for antimicrobials. Similar to IPPE students, APPE students can also provide education to the public and health care professionals about various infectious diseases including patient education and counseling about antimicrobials and vaccines. By supporting existing antimicrobial stewardship programs during their clerkships, students will be better prepared to demonstrate the abilities necessary to practice as competent pharmacists upon graduation. Colleges of pharmacy should consider offering elective APPEs in antimicrobial stewardship for students interested to learn more about infectious diseases pharmacy practice.
Postgraduate Training Postgraduate pharmacy residencies are structured 1-year programs for graduates seeking additional training in pharmacy practice. At the time of writing, there were 833 PGY1 pharmacy residency programs and 54 PGY2 infectious diseases pharmacy residency programs with an ASHP accreditation status.26 PGY2/3 pharmacy fellowships are structured 2-year programs for graduates seeking additional training in pharmacy practice and research. At the time of writing, there were 9 infectious diseases fellowship programs including 4 that are peer reviewed by ACCP.27
PGY1 Pharmacy Residents Role of Pharmacy Residents in Resource-Limited Settings. According to the IDSA/SHEA guidelines, antimicrobial stewardship teams should be multidisciplinary in nature, with core members consisting of an infectious diseases physician and an infectious diseases-trained clinical pharmacist.7 Although this structure may be attainable in larger academic medical centers, in smaller private nonteaching hospitals with limited resources, this structure may not be feasible. The inclusion of pharmacy residents on the antimicrobial stewardship team may be one strategy to overcome resource limitations in such settings. For example, one report described an experience with antimicrobial stewardship in a 545-bed community teaching hospital.28 The team consisted of a noninfectious diseases-trained clinical
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pharmacist and 3 infectious diseases physicians. In all, 14 PGY1 residents and 2 PGY2 residents were also incorporated into the daily activities of this program. Pharmacy residents were assigned to the hospital’s antimicrobial stewardship service year round as part of their infectious diseases and internal medicine experiences. Residents performed most of the data collection and analysis prior to rounds under the supervision of the clinical pharmacist. The team made 550 recommendations over a 2-year period, 68% of which were accepted. The authors did not report on the impact on patient outcomes or cost savings resulting from the implementation of this program, although they did report that involvement of pharmacy residents minimized the time commitment of the infectious diseases physicians and the clinical pharmacist. Role of Pharmacy Residents in Initiating Antimicrobial Stewardship Programs. Pharmacy residents can be instrumental in helping initiate and sustain new antimicrobial stewardship programs. Residents can function as service extenders by providing daily patient profile review, renal dosing of antimicrobials, and intravenous to oral antimicrobial therapy conversion. In addition, as part of their research requirement, residents may assist in starting a new program by performing the needs assessment to identify resources and potential barriers during the early phases of program implementation.29 Such activities when performed by a resident occur at a minimum cost to the institution and may have the potential to produce cost savings. Steinberg JG et al described the impact of a pharmacist-initiated antibiotic review service in 2 general medicine inpatient units at a 550-bed community hospital.30 In this study, a PGY1 pharmacy resident supervised by 2 clinical pharmacists performed most of the antibiotic order review and patient evaluation during weekdays over an 18-week study period, which included a retrospective chart review phase followed by an intervention phase. Fiftyfive recommendations were made to physicians during the intervention phase of the study, 71% of which were accepted. The majority of recommendations made were for intravenous to oral antibiotic conversions (17 of 55), followed by renal dose antibiotic adjustments (15 of 55), and interventions for antibiotic therapy lacking an indication (13 of 55). Total dollar savings recorded during the study period were US$12 000. There was no difference between the average length of stay recorded for patients monitored in this program (8.53 days vs 8.15 days, P ¼ 0.495). No other patient outcomes were recorded in this study. Of note is that this institution had in place automatic renal dose adjustment protocols and intravenous to oral conversion protocols for a selected group of antimicrobials, prior to the study implementation. In this study, the PGY1 pharmacy resident was employed in the early phases of implementation of a pharmacist-led antibiotic stewardship service. Furthermore, involvement of residents-assisted staff pharmacists in completing clinical tasks may not have been routinely addressed due to staffing shortages or workload challenges. In another report, pharmacy residents were incorporated during the initiation phases of an antimicrobial stewardship program. Ijo and Feyerharm reported their experience in providing
prospective audit and feedback over a 4-month period in the intensive care unit of a 378-bed community hospital.31 In this report, pharmacy residents were included as part of a pharmacist-led antimicrobial stewardship team and assisted clinical pharmacists in the intensive care unit in performing prospective audit and feedback to prescribers. Although therapy interventions were only performed during weekdays, this pharmacy team was able to document 93 recommendations. The majority of interventions in this study were for dose optimization (43%). Drug substitution, streamlining, and drug discontinuation accounted for 17%, 13%, and 11%, respectively. The authors reported a mortality rate of 14% and a mean length of stay of 6 days for the patients monitored in this program. Acceptance rates of antibiotic therapy interventions were not reported in this study, and a financial loss of US$192 was documented, which the authors attributed to the limited number of interventions captured during the study period.
PGY2 Infectious Diseases Pharmacy Residents Maintaining and Expanding Existing Antimicrobial Stewardship Programs. Pharmacy residents and in particular PGY2 infectious diseases residents can also be instrumental in maintaining or expanding antimicrobial stewardship services as part of their training. Current ASHP standards for PGY2 residencies and in particular infectious diseases require residents to take a leadership role in improving medication use systems at their institutions, which includes antimicrobial utilization.32 In addition, involvement of residents in antimicrobial stewardship teams fosters further growth and development of stewardship programs. Daily Activities of PGY2 Residents in Antimicrobial Stewardship Programs. Some examples of how PGY2 residents, in particular those training in infectious diseases, may be involved in the daily activities of an antimicrobial stewardship program include participating in prospective audit and feedback to prescribers, performing antimicrobial de-escalation, optimizing antimicrobial therapy dosing, performing intravenous to oral therapy conversion, providing extended clinical coverage hours through on-call programs, and educational opportunities to pharmacists and other health care providers. In addition to contributing to the daily activities of an antimicrobial stewardship program, PGY2 residents, and in particular those training in infectious diseases, also foster innovation and research that help elucidate new findings or contribute to confirm already established concepts. Role of PGY2 Residents in Extending Antimicrobial Stewardship Services. Acute care institutions often struggle to provide high-level clinical care, including antimicrobial stewardship services, at all times, particularly on evenings, weekends, and holidays. In this setting, pharmacy residents during their PGY2 training can be especially helpful in extending the provision of antimicrobial stewardship services after business hours through on-call residency programs. Such a program is described in the
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literature, where extended clinical hours were supported by pharmacy residents through a 24-hour on-call program, at a large teaching hospital with an existing antimicrobial stewardship team.33 Although this on-call residency program provided a broad range of clinical pharmacy services, the program largely supported the hospital’s existing antimicrobial management team through the provision of antimicrobial therapy recommendations and pharmacokinetic dosing recommendations for antibiotics, after business hours, as evidenced by the number of encounters recorded. Although not widely described in the literature, PGY2 residents, through an on-call program, may also provide extended hours for pharmacist-led priorapproval systems for restricted antimicrobials in hospitals that have such a system in place. Such a program may assist in preventing the phenomenon of ‘‘Stealth Dosing’’—which is waiting until after the prior-approval period ends to prescribe restricted antimicrobials—as recently described by LaRosa et al.34 Education. Education is recognized as an essential component of any antimicrobial stewardship program.7 Part of the ASHP residency training requirements includes the ability to provide education to various groups, in both small and large formats. PGY2 residents can be instrumental in leading educational programs related to antimicrobial stewardship, resulting in the education of pharmacists, pharmacy technicians, nurses, physicians, and other individuals in the organization. When education is used along with active interventions, it can help influence prescribing behaviors. Scholarship and Innovation. According to the ASHP residency accreditation standards, residents are required to cultivate their own project management skills.32 Such skill development may take the form of formal research, continuous quality improvement initiatives, medication use evaluations, or practice service implementation (eg, protocol implementation with measurement of impact or quality assurance initiatives) that benefits the host institution. Examples of such resident-led antimicrobial stewardship research initiatives can be found in the literature.35-38
PGY2/3 Infectious Diseases Pharmacy Fellows Pharmacy fellowship programs are highly individualized and variable with respect to practice experiences. In 2004, ACCP developed guidelines for research fellowship training programs that wish to be voluntarily peer-reviewed by the College.39 A recent report outlines the involvement of infectious diseases pharmacy fellows in an institution’s antimicrobial stewardship program, although no details were provided on the specifics of this involvement.40 Although, fellowship programs are not deemed as being equivalent to PGY2 residency programs in terms of clinical practice competency,15 fellows have contributed to antimicrobial stewardship advancement primarily through research and scholarship, examples of which can be found in the pharmacy and the infectious diseases literature.41-45
Pharmacy Practice Model Initiative The Pharmacy Practice Model Initiative (PPMI) recommends curricular changes in colleges of pharmacy to prepare students for a larger role in drug therapy management, pharmacy informatics, medication safety, and transitions of care which are essential for effective antimicrobial stewardship services.46 Pharmacy educators should follow the example of medical educators and assess pharmacy students’ perceptions, attitudes, and knowledge of antimicrobial stewardship and implement changes in pharmacy curricula based on the PPMI recommendations.47 Pharmacists should utilize students and residents as pharmacist extenders in the provision of antimicrobial stewardship services provided that the appropriate level of training, oversight, and quality assurance is met in alignment with the critical requirements for health-system pharmacy practice models to achieve optimal use of antimicrobials.48 This layered learning practice model from attending pharmacist to resident to student has already been implemented in several institutions across the nation49,50; however, further studies are needed to assess and document the impact of pharmacy students and postgraduate trainees on antimicrobial stewardship programs.
Conclusions Didactic instruction in antimicrobial pharmacotherapy provides students with the foundational knowledge and skills necessary for experiential education. IPPEs and APPEs give students the opportunity to get involved in antimicrobial stewardship programs. PGY1 pharmacy residency and PGY2 infectious diseases pharmacy residency enable postgraduate trainees to serve on antimicrobial stewardship programs. Infectious diseases pharmacy fellowships empower postgraduate trainees to contribute to the research and scholarship of antimicrobial stewardship. At each stage of training, students, residents, and fellows should take full advantage of their roles in antimicrobial stewardship, document their activities, and disseminate their findings. In light of expected stricter regulatory requirements for the judicious and appropriate use of antimicrobials in the upcoming years, the demand for infectious diseasestrained clinical pharmacists is likely to rise. Therefore, adequate training of pharmacy students and expansion of residency and fellowship programs are essential to prepare the necessary manpower to sustain and further develop antimicrobial stewardship programs. Declaration of Conflicting Interests The author(s) declared the following potential conflicts of interest with respect to the research, authorship, and/or publication of this article: Dr Chahine serves on the speakers’ bureaus for Cubist Pharmaceuticals, Inc and Forest Pharmaceuticals, Inc. Drs El-Lababidi and Sourial have nothing to disclose.
Funding The author(s) received no financial support for the research, authorship, and/or publication of this article.
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