A major global public health threat today is the development of antimicrobial resistance, which can emerge through the inappropriate use of antimicrobial agents. Up to 50% of antimicrobial use is inappropriate in the hospital setting.Reference Dellit, Owens and McGowan 1 , 2 In an effort to reduce the rates of antimicrobial resistance, the Joint Commission mandates that all hospitals and critical-access hospitals establish an evidence-based antimicrobial stewardship program. 2 Antimicrobial stewardship programs are an effective strategy to prevent the development of antimicrobial resistance, and antimicrobial stewardship programs have significant benefit in reducing mortality, length of stay, and healthcare costs.Reference Barlam, Cosgrove and Abbo 3 – Reference Kelley, Aaronson and Poon 7
Antimicrobial stewardship programs should be led by infectious diseases–trained physicians and pharmacistsReference Dellit, Owens and McGowan 1 , Reference Barlam, Cosgrove and Abbo 3 ; however, this demand is challenging to meet. The National Resident Matching Program revealed that 51 of the 151 (33.8%) training positions in infectious diseases medical fellowship programs in the United States remained unfilled in 2018. 8 This high percentage is consistent with previous years.Reference Chandrasekar 9 The declining rate of applicant interest for a career in infectious diseases is concerning and may be attributed to factors such as a growing number of hospital-based positions, lack of mentorship in infectious diseases, and lower salary compared to other subspecialties.Reference Chandrasekar, Havlichek and Johnson 10 , Reference Bonura, Lee, Ramsey and Armstrong 11 Likewise, current infectious diseases training opportunities, such as residencies, fellowships, and certificate programs for pharmacists in the United States are considered inadequate to meet the demand for pharmacists with advanced training in antimicrobial stewardship (AS).Reference Gauthier, Worley and Laboy 12 Due to the demand, lack of infectious diseases training programs and personnel, and high prevalence of infections, it is likely that all physicians, pharmacists, and trainees will be involved with AS to some degree.
Therefore, healthcare practitioners should receive education on AS principles and practices during their didactic studies and throughout their postgraduate training. By receiving sufficient education and learning experiences, practitioners gain the knowledge and ability to perform AS during their training and as independent practitioners. Although specific AS education and curricula of trainees is not explored, this review summarizes the implementation of various AS practices by physician and pharmacist trainees.
Search strategy and selection criteria
An electronic search through PubMed was conducted (January 2000 to June 2018) using the following terms: antimicrobial stewardship, antibiotic stewardship, trainees, students, postgraduate education, medical education, fellowship, and education. All articles available in English and their references were reviewed for additional publications as well. All articles identified were included in this review.
Trainee definitions
Medical trainees can be classified as residents (including interns) or fellows. For the purposes of this article, medical residents are those trainees who are completing an internal medicine residency (usually post graduate years [PGY] 1–3) and fellows are those completing an infectious diseases fellowship after satisfactory completion of an internal medicine residency (PGY4 and up). 13
The American Society of Health-System Pharmacists, the organization that accredits most pharmacy residencies, clearly differentiates between pharmacy residencies and pharmacy fellowships. 14 Pharmacy residencies are postgraduate training programs in an area of pharmacy practice, while pharmacy fellowships are postgraduate training programs designed to prepare the individual to be a researcher. Pharmacy residencies are further divided by year: PGY1 residencies usually focus on general clinical pharmacy practice; PGY2 residencies are focused on a single area of practice (eg, infectious diseases, critical care, ambulatory care).
Results
Role of medical trainees in AS
In total, we identified 6 publications that describe the use of medical trainees in AS activities.Reference Foral, Anthone and Destache 15 – Reference Chou, Graber and Jones 20 Table 1 lists the details of 4 of the publications.Reference Foral, Anthone and Destache 15 – Reference Rimawi, Mazer and Siraj 18 Medical trainees were used to conduct AS activities in diverse patient populations (eg, hematology/oncology and medical ICU) with differing outcomes, and all publications were from academic medical centers or veterans affairs hospitals. The most common AS strategies used by medical trainees in these publications were streamlining and/or de-escalation of therapy and prospective audit with intervention and feedback. Strategies with no published studies in medical trainees were guidelines and clinical pathways and antimicrobial order sets.
Table 1 Publications About Medical Trainees’ Involvement in Antimicrobial Stewardship EffortsReference Foral, Anthone and Destache 15 – Reference Rimawi, Mazer and Siraj 18
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Note. AS, antimicrobial stewardship; ID, infectious diseases; APPE, advanced pharmacy practice experience; IV, intravenous; PO, enteral route; ICU, intensive care unit; MICU, medical intensive care unit
a Academic medical center, community hospital, long-term care, etc.
b Student, resident, fellow.
Additionally, Graber et alReference Graber, Jones and Chou 19 evaluated AS activities at all 130 Veterans Affairs (VA) medical centers with acute-care services in 2012. Based on these results, the VA National Antimicrobial Stewardship Task Force and the VA Healthcare Analysis and Information Group assessed for common variables because there is no common model among all VA centers. The variables associated with decreased inappropriate antibiotic use were (1) postgraduate physician/pharmacy training programs (although they did not specifically identify infectious disease programs), (2) general ward teams that involved pharmacists and/or infectious disease attendings, (3) the involvement of infectious disease attendings and/or fellows in antibiotic approvals, and (4) formally AS-trained pharmacist at the facility. A similar analysis by Chou et alReference Chou, Graber and Jones 20 further described AS activities in postgraduate training programs at VA acute-care centers. A 9% reduction in antibiotic use occurred if the facility had an infectious disease fellowship program and a 10% reduction occurred with an infectious disease trained pharmacist. However, no details were given about the activities that trainees performed within the AS programs, only details about the activities that the programs performed as a whole.
Role of pharmacy trainees in AS
Overall, 5 articles specific to pharmacy trainee involvement in AS were identified.Reference Chahine, El-Lababidi and Sourial 21 – Reference Siegfried, Merchan and Scipione 25 Table 2 describes 4 of the articles in detail. The most common AS strategies used by pharmacy trainees in these publications were dose optimization and prospective audit with intervention and feedback. Strategies with no published studies in pharmacy trainees were guidelines and clinical pathways and antimicrobial order sets. The published studies showed significant process outcomes (ie, interventions made and accepted) as well as clinical outcomes (ie, reduced drug costs and days of therapy).
Table 2 Publications about Pharmacy Trainees’ Involvement in AS EffortsReference Benson 22 - Reference Siegfried, Merchan and Scipione 25
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Note. AS, antimicrobial stewardship; APPE, advanced pharmacy practice experience; ID, infectious diseases; PGY, postgraduate year.
a Academic medical center, community hospital, long-term care, etc.
b Student, resident, fellow.
Additionally, the fifth article found in the search was a review by Chahine et alReference Chahine, El-Lababidi and Sourial 21 that focused on the currently available published data on pharmacy trainees (students, PGY1 residents, PGY2 infectious diseases residents, and fellows) in AS activities; they also proposed a model to further engage pharmacy trainees in AS. Because of the limited clinical studies published at the time, most of the article reviewed academic standards for students and postgraduate trainees as they applied to AS activities. They proposed that even early on in training, pharmacy students completing their introductory pharmacy practice experiences (IPPE) could be involved in some aspects of AS (eg, education, dose optimization, and parenteral-to-oral conversion). Accordingly, as pharmacy students advance through advanced pharmacy practice experiences (APPE), they could also participate in creating guidelines and clinical pathways and antimicrobial order forms, as wells as recommending streamlining and/or de-escalation of antimicrobial therapy. The authors proposed that postgraduate pharmacy trainees (PGY1 residents, PGY2 infectious diseases residents, and PGY2/3 infectious diseases fellows) be incorporated into all aspects of AS, including prospective audit with feedback and formulary restriction/preauthorization.
Discussion
Recent studies show that improvements in AS education for trainees are warranted. Abbo et alReference Abbo, Cosgrove and Pottinger 26 surveyed fourth-year students at various medical schools in the United States and found that 90% of respondents would prefer more education on appropriate antimicrobial use. Although medical students who finished a clinical infectious diseases rotation felt they had a higher quality of AS-related education compared to those who did not (mean Likert score, 3.93 vs 3.44; P = .0003), only one-third of students felt adequately prepared in fundamental principles of antimicrobial use. Justo et al. surveyed the knowledge and attitudes of graduating pharmacy students at various colleges of pharmacy in the United States toward appropriate antimicrobial use.Reference Justo, Gauthier and Scheetz 27 Roughly 90% and 80% of pharmacy students wanted more education on appropriate use of antimicrobials and on antimicrobial resistance, respectively. Approximately two-thirds of pharmacy students felt that their education related to antimicrobial therapy initiation and selection was satisfactory. Additionally, only 68% of US doctor of pharmacy programs integrated AS education into the required didactic curricula. Notably, there are wide variances in AS principles taught.Reference Kufel, Jeffres and MacDougall 28 Similar results were found in studies assessing AS-related knowledge and perceptions of medical and pharmacy students across international programs.Reference Yang, Wu and Tan 29 – Reference Dyar, Pulcini and Howard 32
Luther et alReference Luther, Shnekendorf and Abbo 33 captured the perspectives of adult infectious diseases medical fellowship directors in the United States regarding their fellows’ AS training. Although 50% of programs had a formal curriculum dedicated to AS, only 20% of directors were either very or extremely satisfied with the medical fellow’s training. Also, 12% of fellowship directors felt that their fellows were either very or extremely well prepared to initiate an antimicrobial stewardship program. Approximately 75% of fellowship directors were very or extremely satisfied with their fellow’s ability to serve as a leader in an existing antimicrobial stewardship program and incorporate AS principles during their own practice. The lack of improvement of their fellow’s training was attributed to the deficit of curricular materials related to AS. Improvements to the core curriculum and trainee’s programs related to AS content are necessary to develop future AS leaders and promote optimal AS practices.
The studies reviewed in this article demonstrate the impact medical and pharmacy trainees can have in relation to AS. The review identified few published articles for both medical and pharmacy trainee involvement in AS. There are likely more activities that medical and pharmacy trainees perform in AS that have yet to be published. For example, the review did not show any publications that described medical and pharmacy trainees being involved in the more administrative tasks of AS, such as facility-specific guideline and clinical pathway development and/or review, despite this being a recommended component of AS programs in the guidelinesReference Dellit, Owens and McGowan 1 , Reference Barlam, Cosgrove and Abbo 3 and an objective for PGY2 infectious diseases pharmacy residencies. 34 The lack of publication of the more administrative tasks is likely related to the difficulty in measuring process-based and clinical outcomes. Additionally, all of the publications identified in the search were conducted in acute-care or long-term acute-care settings, with none coming from outpatient AS. The authors encourage more published accounts of the extent of the AS activities of trainees in all health disciplines in all healthcare settings.
An unanswered question related to this topic includes the impact of AS training programs by tracking the AS impact of graduates at their future places of employment. Also, a unique question is to what degree changes in didactic trainee AS education versus “hands on” AS training (as described in this article) successfully prepare trainees to participate in AS in their careers.
Given the worldwide threat of antimicrobial resistance, the importance of effective AS programs has become paramount. To enact such AS programs, training programs in medicine, pharmacy, and other health professions need to incorporate both AS education and AS activities to ensure that AS principles are followed beyond graduation. Additional documentation of these activities and impact of trainees’ involvement in AS in the published literature is also greatly needed to serve as exemplars for other training programs.
Acknowledgments
Financial support
No financial support was provided relevant to this article.
Conflicts of interest
J.C. has served as a member of the Speakers Bureau for Allergan. All authors report no conflicts of interest relevant to this article.