Antimicrobial stewardship education in US colleges and schools of pharmacy

Abstract

Background

Pharmacists are key members of antimicrobial stewardship (AS) teams. It is unknown if and how US colleges and schools of pharmacy incorporate AS into their Doctor of Pharmacy (PharmD) curricula.

Methods

This study was a cross-sectional, multicentre, electronic survey distributed to infectious diseases faculty or department chairs of 137 accredited and candidate-status PharmD programmes.

Results

One hundred and sixteen programmes participated, representing an 84.7% response rate. AS education was integrated into the required didactic, elective didactic and experiential education components of the curricula in 79 (68.1%), 43 (37.1%) and 97 (83.6%) PharmD programmes, respectively. The most common AS topics in required and elective didactic curricula were AS definitions, principles and purpose (98.7% and 86.0%) and the pharmacist’s role in AS (93.7% and 83.7%). In the required and elective didactic curricula, lecture (93.7% and 86.0%) and case-based instruction (57.0% and 83.7%) were the most common instructional methods. For experiential education, the pharmacist’s role in AS (96.9%), de-escalation of antimicrobials (96.9%) and antimicrobial dose optimization (95.9%) were the most common AS topics. PharmD programmes employing a faculty member who specializes in AS were more likely to offer AS experiential education than programmes without AS faculty (88.1% versus 71.9%, P = 0.049).

Conclusions

Integration of AS education in US PharmD curricula is variable and there are considerable differences in the AS activities and topics delivered. PharmD programmes should attempt to expose students to AS education to prepare future pharmacists for AS practice. Efforts should be made to incorporate interprofessional collaboration into AS education.

Introduction

Resistance to antimicrobial agents is a well-recognized public health threat that has a large impact on patient outcomes.¹ In an effort to mitigate the development of antimicrobial resistance and decrease inappropriate use of antimicrobials, multiple organizations have recommended the creation of antimicrobial stewardship (AS) programmes (ASPs) in the USA.^2–4 ASPs function in several different healthcare settings including hospitals, critical access hospitals, nursing care centres, emergency departments and outpatient clinics for both adult and paediatric patient populations.^5–8 Ideally, an interprofessional team including physicians, pharmacists, microbiologists, infection control personnel, informatics personnel and nurses collaborate to develop and implement an ASP, yet this is largely dependent on available resources and practice settings.^2,9 One of the many efforts of ASPs is to provide education to healthcare professionals, patients and families about the adverse outcomes associated with antimicrobial use and the purpose of AS, yet effective dissemination of this education remains a challenge.^2,10

Currently, clinicians’ exposure and orientation to AS have primarily occurred during postgraduate training or in clinical practice, yet the content and depth of AS education is largely undetermined.^11,12 Limited data describe AS education during medical, pharmacy and nursing school.^13,14 Studies of medical students and pharmacy students from the USA, Australia, South Africa, the UK and other European countries have identified students’ concern regarding antimicrobial resistance, considerable differences in infectious diseases (ID) knowledge and the desire for further education in ID and AS.^11,15–24 However, the incorporation of AS education into the curricula of these professional schools has yet to be clearly described. The next generation of healthcare professionals, even those without formalized ID training, are likely to fill many AS roles in a variety of practice settings.^25–27 Unlike some drug classes (i.e. chemotherapy and specific antipsychotics), antimicrobials are essentially prescribed by all providers in a variety of practice settings, regardless of training and knowledge in ID.²⁸ Furthermore, new regulatory standards for ASPs will likely make institutions more acutely aware of the need for AS-trained pharmacists.⁵ Thus, AS education within these schools’ curricula is necessary to educate future healthcare professionals about AS and the importance of appropriate antimicrobial prescribing.

While AS education is a need in healthcare professional schools, integration within the curricula of Doctor of Pharmacy (PharmD) programmes necessitates important consideration, particularly since postgraduate training is not required for pharmacists as it is with physicians, who are required to complete postgraduate training.²⁹ As a result, pharmacists may not be exposed to the education and training, specifically for AS. General ID pharmacotherapy education is required in the pharmacy school curricula by the Accreditation Council for Pharmacy Education and the Center for Advancement of Pharmacy Education, yet there are no specific criteria for the inclusion of AS content.^30,31 This study aimed to evaluate the extent, content and methodology by which AS education was incorporated into the curricula of colleges and schools of pharmacy in the USA.

Methods

Study design and population

This study was a cross-sectional, multicentre, electronic survey designed to evaluate the incorporation of AS education within PharmD programmes. Accreditation Council for Pharmacy Education accredited and candidate status PharmD programmes were included in this study (n = 137). Pre-candidate status PharmD programmes (n = 4) were excluded because students may not have enrolled in the programme yet, and pharmacist faculty recruitment and curricula development may still be in progress.³²

Ethics

This study was approved by the University of North Carolina Institutional Review Board. A survey invitation letter with the appropriate informed consent information was attached to the survey instrument and was distributed electronically via email to the respondents. By selecting to enter the survey, the respondent had agreed to participate in this study.

Survey instrument

A 27-item survey (available as Supplementary data at JAC Online) was designed to collect information from the responding PharmD programmes about AS education within their curricula. This survey was developed using expert opinion of the ID pharmacist faculty and a previous educational research survey to determine the extent, content and methodology of a particular educational topic within PharmD programmes.³³ Qualtrics (Qualtrics, Inc., Provo, UT, USA) was used to design and collect survey responses.

Data collected from the survey included PharmD programme demographic information as well as the extent, content and methodology of AS education in the following components of the PharmD curricula: required didactic, elective didactic and experiential education (see the Supplementary data). Geographical location was grouped into four regions defined by the US Census Bureau.³⁴ Data were also collected for the number of class hours designated to AS instruction, type of didactic instruction used to deliver AS education and AS topics taught for the required and elective didactic components. AS topics or activities were separated into core and supplemental based on previous AS topics described in the literature and expert opinion.³⁵ Data collected for experiential education included the type of AS experience offered in which >50% of experiential hours were spent on AS-related activities, presence of an affiliated ID pharmacist preceptor who spends >50% of time in AS-related activities and AS-related activities or topics that pharmacy students were engaged in. Respondents were able to select multiple responses for teaching delivery methods as well as core and supplementary AS topics. Skip logic was integrated to minimize survey fatigue and reduce completion time. Thus, the exact number of questions requiring answers depended on previous responses.

Survey administration

The survey was pilot tested before dissemination to ensure validity, logistical integrity and question clarity. The faculty responsible for the ID curriculum at each pharmacy school were identified via each respective PharmD programme website. In circumstances in which a PharmD programme did not have a designated ID pharmacist faculty, or identification of an ID pharmacist faculty was not possible, the chair of the pharmacy practice department or corresponding department was identified. When a PharmD programme employed more than one ID pharmacist faculty member, the survey was distributed to one of the ID pharmacist faculty members at the discretion of the investigators.

The electronic survey was initially distributed directly to ID pharmacist faculty members or department chairs via email from April to May 2017. A reminder email was sent each week over a 5 week period to the faculty members who did not respond initially. In an effort to increase the survey response rate, surveys were distributed in August 2017 to ID pharmacist faculty members or department chairs within non-responding PharmD programmes over a 4 week period.

Statistical analysis

Survey responses were collected via Qualtrics survey software and analysed using SPSS Statistics, version 24 (IBM Corp., Armonk, NY, USA). Frequencies and percentages were used to describe demographic and AS curriculum data. Categorical demographic and AS curriculum variables were compared using a χ² test. For all tests of statistical significance, a two-tailed α value was set at 0.05.

Results

One hundred and sixteen respondents from 137 (84.7%) PharmD programmes completed the survey. The demographic characteristics of PharmD programmes are displayed in Table 1. PharmD programmes from multiple geographical locations in the USA were well represented. AS education was part of the didactic curriculum for 68.1% of PharmD programmes and part of the elective curriculum for 37.1% (Table 2). Less than 8% of PharmD programmes dedicated five or more required contact hours to the topic. Conversely, 42% of programmes that covered AS content in an elective dedicated five or more contact hours to the topic. Lecture was the most common method of didactic instruction for both required and elective content. Content in the elective curriculum was more commonly delivered through non-lecture methods including patient cases, discussion groups, problem-based learning and journal clubs. Topics most commonly covered within didactic and elective curriculum were AS definitions, principles and purpose, the pharmacist’s role in AS, evidence-based strategies, clinical pathways, de-escalation of antimicrobials, duration of therapy and dose optimization.

Table 1.

Demographics of US PharmD programmes participating in the survey about AS in pharmacy (n = 116)

Demographics	Number (%)
ID faculty survey response
yes	107 (92.2)
other	9 (7.8)
Accreditation status
candidate	10 (8.6)
accredited	106 (91.4)
Public/private
public	54 (46.6)
private	62 (53.4)
Regional distributiona
north-east	19 (16.4)
south	46 (39.7)
mid-west	26 (22.4)
west	23 (19.8)
otherb	2 (1.7)
Number of years in existence
<5	13 (11.2)
6–10	21 (18.1)
11–20	17 (14.7)
>20	65 (56.0)
Number of students per graduating class
<50	2 (1.7)
51–100	58 (50.0)
101–200	44 (37.9)
>200	12 (10.3)
Number of faculty members (full-time or adjunct) who spend >50% of time in AS
0	32 (27.6)
1	48 (41.4)
2	26 (22.4)
≥3	10 (8.6)

a

Based on the US Census Bureau regions.³⁴

b

PharmD programme located in Puerto Rico and Hawaii.

Table 2.

Extent, content and methodology of AS education within the didactic curricula (n = 116)

Extent, content and methodology	Required didactic, number (%)	Elective didactic, number (%)
AS education within the didactic curricula	79 (68.1)	43 (37.1)
Number of class hours designated to ASa
1	34 (43.0)	10 (23.2)
2	19 (24.1)	11 (25.6)
3	11 (13.9)	3 (7.0)
4	9 (11.4)	1 (2.3)
≥5	6 (7.6)	18 (41.9)
Type of didactic instruction used to deliver AS educationa
lecture	74 (93.7)	37 (86.0)
case-based instruction/learning	45 (57.0)	36 (83.7)
team-based learning	19 (24.1)	15 (34.9)
discussion, large group (>12 students)	13 (16.5)	19 (44.2)
laboratory/simulation	11 (13.9)	7 (16.3)
discussion, small group (<12 students)	9 (11.4)	21 (48.8)
independent learning (ex: pre-class reading)	9 (11.4)	13 (30.2)
problem-based learning	6 (7.6)	17 (39.5)
journal club	3 (3.8)	8 (18.6)
Core AS-related topics or strategiesa
AS definitions, principles and purpose	78 (98.7)	37 (86.0)
description of the pharmacist’s role in AS	74 (93.7)	36 (83.7)
core evidence-based AS strategies	58 (73.4)	32 (74.4)
key personnel and departments of AS team	57 (72.2)	12 (27.9)
case-based AS examples and scenarios	51 (64.6)	33 (76.7)
CDC core elements of AS programme	48 (60.8)	31 (72.1)
AS legislative and regulatory aspects	37 (46.8)	29 (67.4)
rapid diagnostic testing within AS	35 (44.3)	27 (62.8)
identification and retrieval of key AS resources	29 (36.7)	23 (53.5)
antimicrobial use measurements	29 (36.7)	23 (53.5)
Supplemental AS-related topics or activitiesa
clinical pathways and guidelines for specific ID states	60 (75.9)	41 (95.3)
parenteral to enteral antimicrobial therapy conversion	55 (69.6)	32 (74.4)
de-escalation and streamlining of antimicrobials	69 (87.3)	41 (95.3)
duration of antimicrobial therapy for common ID states	68 (86.1)	37 (86.0)
antimicrobial dose optimization	59 (74.7)	36 (83.7)

a

Of the colleges or schools of pharmacy that incorporate AS education within the didactic curricula (required: 79; elective: 43).

Ninety-seven (83.6%) of responding PharmD programmes included AS education within experiential education (Table 3). A wide variety of responses were described by respondents regarding the number of clinical rotation sites where >50% of the time was spent in AS-related activities, ranging from one to more than five sites. However, 39.2% of respondents were unsure of the number of clinical rotation sites available. An ID pharmacist preceptor who spends >50% of their time in AS-related activities was available in all but 4 (4.1%) responding PharmD programmes. Most PharmD programmes had both faculty members and non-faculty members present at the clinical rotation sites to deliver AS education. All of the listed AS-related activities and topics during the clinical rotation experience were represented by the survey. More than 90% of respondents indicated that pharmacy students were involved in de-escalation and streamlining of antimicrobials, appropriate antimicrobial durations and antimicrobial dose optimization during the clinical rotation experience.

Table 3.

Extent, content and methodology of AS education within the experiential education curricula (n = 116)

Extent, content and methodology	Number (%)
ID clinical rotation at an affiliated clinical practice site where >50% of the time is spent in AS-related activities	97 (83.6)
Number of clinical rotation sites (AS or ID clinical experiences) available for students to select where >50% of the time is spent in AS-related activitiesa
0	3 (3.1)
1	12 (12.4)
2	19 (19.6)
3	8 (8.2)
4	4 (4.1)
≥5	13 (13.4)
number of clinical rotation sites unknown	38 (39.2)
Presence of an affiliated ID pharmacist preceptor who spends >50% of their time in AS-related activitiesa
both faculty and non-faculty membersb	33 (34.0)
faculty member(s)b	31 (32.0)
non-faculty member(s)b	29 (29.9)
no available preceptor currently	4 (4.1)
AS-related activities students are involved in during clinical rotation experiencea
de-escalation and streamlining of antimicrobials appropriately	94 (96.9)
antimicrobial dose optimization	93 (95.9)
duration of antimicrobial therapy optimization for common ID states	88 (90.7)
core evidence-based AS strategiesc	86 (88.7)
parenteral to enteral antimicrobial therapy conversion	83 (85.6)
meetings with AS team leadership	75 (77.3)
development or use of clinical pathways and guidelines for specific ID states	71 (73.2)
AS programme education and dissemination of knowledge to healthcare practitioners	63 (64.9)
rapid diagnostic testing and other AS tools	62 (63.9)
retrospective time outs for specific antimicrobials	41 (42.3)
AS-related topics or activities students are exposed to during clinical rotationa
description of the pharmacist’s role in AS	94 (96.9)
AS elements, members, administrative support and multidisciplinary team	79 (81.4)
identification and retrieval of key AS resources	65 (67.0)
AS reporting for process and outcome measures	64 (66.0)
CDC core elements for AS programmes	62 (63.9)
AS legislative and regulatory aspects	30 (30.9)

a

Of the 97 colleges or schools of pharmacy that incorporate AS education within the experiential education curricula.

b

At least one preceptor available.

c

Examples include prospective audit with intervention and feedback, formulary restriction and preauthorization requirements for specific antimicrobials (included on survey question).

Ninety-seven (83.6%) respondents indicated AS education was incorporated at some level of the curriculum, either in the didactic (required or elective) or experiential components. Twenty-nine (25.0%) PharmD programmes had both required and elective didactic AS education and 28 of these programmes offered required, elective and experiential AS education. Among the 37 (31.9%) PharmD programmes that did not incorporate AS education within the required didactic curricula, 14 offered an elective with AS content and 26 had experiential AS education.

Table 4 compares PharmD programme demographic characteristics and AS educational content offered. PharmD programmes employing an AS faculty were more likely to offer experiential AS education than programmes without AS faculty (88% versus 72%, P = 0.049). Comparisons across accreditation status, funding model, age of PharmD programme or class size did not identify differences in how AS was taught in the curriculum.

Table 4.

Comparison of college or school demographics and rates of AS education within the required didactic, elective didactic and experiential curricula

Component of curriculum	College or school demographic for comparison, n (%)		P
	accredited (n = 106)	candidate (n = 10)
AS in required didactic	72 (67.9)	7 (70.0)	1.000
AS in elective didactic	39 (36.8)	4 (40.0)	1.000
AS in experiential education	90 (84.9)	7 (70.0)	0.210
	private (n = 62)	public (n = 54)
AS in required didactic	47 (75.8)	32 (59.3)	0.073
AS in elective didactic	22 (35.5)	21 (38.9)	0.847
AS in experiential education	55 (88.7)	42 (77.8)	0.135
	age >20 years (n = 65)	age <20 years (n = 51)
AS in required didactic	43 (66.2)	36 (70.6)	0.690
AS in elective didactic	27 (41.5)	16 (31.4)	0.333
AS in experiential education	54 (83.1)	43 (84.3)	1.000
	class size <100 (n = 60)	class size >100 (n = 56)
AS in required didactic	41 (68.3)	38 (67.9)	1.000
AS in elective didactic	19 (31.7)	24 (42.9)	0.251
AS in experiential education	48 (80.0)	49 (87.5)	0.322
	AS faculty present (n = 84)	AS faculty not present (n = 32)
AS in required didactic	56 (66.7)	23 (71.9)	0.660
AS in elective didactic	31 (36.9)	12 (37.5)	1.000
AS in experiential education	74 (88.1)	23 (71.9)	0.049

Discussion

Given the importance of pharmacists as essential interprofessional members of ASPs and the limited number of postgraduate training opportunities for pharmacists in ID, pharmacy graduates will likely engage in AS practices in various settings and rely on the AS knowledge gained during pharmacy school.^{25,26,29,36–38} Thus, teaching AS principles and practices should begin during pharmacy school as many pharmacists without specific ID training will need to practise AS and understand appropriate antimicrobial prescribing.²⁶ AS education within the professional curricula has previously been suggested,^11,15,39 yet formal curricula evaluation of medical and pharmacy schools regarding AS education has been limited, particularly in the USA.^23,24 To our knowledge, this is the first study to investigate the extent, content and methodology of AS education within the PharmD curricula at US colleges or schools of pharmacy.

Based on responding PharmD programmes, there was considerable variability regarding AS education throughout the PharmD curricula. It is encouraging that the majority of PharmD programmes integrated AS education within the required didactic curricula, since this is the only component of the curricula that students are guaranteed to be exposed to throughout pharmacy school. Exposure in didactic curricula also gives interested pharmacy students the option of enrolling in an AS or ID elective course with an emphasis on AS or selecting a clinical rotation experience focused on AS, if available.^35,40–42

Of the three main components of the PharmD curricula, AS education was integrated the least in the elective didactic component. This may be owing to limited resources for elective didactic courses including necessary ID pharmacist faculty, distribution of teaching responsibilities and sufficient numbers of interested students. However, pharmacy students as well as medical students display a desire for more education on antimicrobial prescribing and AS.^11,15 Multiple examples of elective AS and ID pharmacy courses are described in the literature.^35,40–42 These resources serve as an excellent foundation to develop an elective didactic course focused on AS and ID pharmacotherapy to expose further the students to AS.

Although AS education was incorporated into the experiential education component of the curricula in the majority of PharmD programmes, it is not guaranteed that PharmD students will have the opportunity to engage in these AS experiences. PharmD students are limited in the number of clinical rotations that are potentially available and that they can select. Furthermore, a potentially limited number of ID pharmacist preceptors are available to precept students for the clinical rotation as described in Table 3.¹⁵ Thus, many students may not have access or exposure to these ID clinical rotations that have an emphasis on AS. Consideration should be given to exposing or increasing AS and ID content in other clinical rotations such as internal medicine and ambulatory care as well as to encourage AS pharmacists to precept pharmacy students for experiential education.¹⁵

There is considerable variability in didactic instruction and learning experiences in AS and ID clinical services, which may contribute to ineffective learning of essential concepts. Furthermore, pharmacy and medical students’ perceptions and knowledge of antimicrobials, including AS, suggest that deficiencies are present in pharmacy and medical schools’ curricula.^11,15–17 In a survey of medical students, only 40% were familiar with the term AS, yet medical students are future prescribers of antimicrobials and will likely engage in AS activities throughout their career in clinical practice.¹¹

Previous literature recognizes the need for standardized education regarding appropriate antimicrobial use and AS principles for students in the medical school curricula in addition to establishing convenient access to information resources and opportunities to engage in AS learning experiences.^{11,13,39,43,44} In a joint effort by the Wake Forest School of Medicine, the CDC and the Associations of American Medical Colleges, an AS curriculum was developed to highlight key AS principles in an effort to standardize AS education in medical schools.¹⁴ A similar AS education curriculum for US PharmD programmes would be a valuable resource to improve standardized AS education. The American College of Clinical Pharmacy Pharmacotherapy Didactic Curriculum Toolkit attempts to provide valuable guidance for developing, maintaining and modifying the PharmD curricula.⁴⁵ This document recommends that students receive education and training in AS, but does not provide any guidance regarding what components of AS should be taught nor how the knowledge or skills should be assessed. A framework for incorporating AS education into pharmacy school curricula has been previously identified and may be useful for standardization, yet implementation has yet to be described.⁴⁶ The results from our survey may also provide structure for important AS topics and concepts to consider incorporating into PharmD programmes.

Postgraduate training opportunities for pharmacists specializing in ID and AS are available but only a limited number of programmes currently exist.^25,38 Additionally, AS certificate training programmes for pharmacists are also offered by professional organizations including the Society of Infectious Diseases Pharmacists and Making A Difference in Infectious Diseases.^47,48 An expert professional practice curriculum on infection and AS was also developed for pharmacists in the UK by the Clinical Pharmacy Association Infection Network and endorsed by the Royal Pharmaceutical Society.^49,50 All of these training programmes are optional, which further emphasizes the importance of incorporating AS education into the PharmD curricula.

Available studies also suggest that pharmacy and medical students demonstrate similar attitudes and knowledge towards AS, antimicrobial use and antimicrobial resistance.^11,15 This overlap in exposure highlights the opportunity for increased interprofessional education in AS, particularly considering the interdisciplinary efforts of ASPs in various clinical settings.¹⁵ One academic medical centre describes their creation of an integrated and interdisciplinary curriculum to provide education to multiple learners in the areas of AS and infection prevention.⁴³ MacDougall et al.⁵¹ demonstrated that a formal, organized interprofessional AS curriculum improves knowledge and attitudes towards antimicrobial use among pharmacy and medical students. Interest in AS education among PharmD programmes, and other interprofessional schools, is a growing area of research to further the development of successful ASPs and combat antimicrobial resistance. Our survey instrument may serve as a template that could be used to identify further the extent, content and methodology of AS education within medical and nursing schools.

Based on our survey results, the future demand of pharmacists practising AS in various settings, the limited number of postgraduate opportunities for AS education and the American College of Clinical Pharmacy Pharmacotherapy Didactic Curriculum Toolkit recommendations, we strongly encourage AS education to be further incorporated into PharmD curricula. Pharmacists need to be prepared to practise AS consistent with the skills and knowledge identified in the IDSA and the Society of Healthcare Epidemiology of America Antibiotic Stewardship guidelines.⁴

One of the strengths of our study was the high survey response rate. We had a survey response rate of 84.7% and all regions of the USA were well represented to minimize the risk of selection bias. However, several limitations should be considered. Although the majority of respondents were ID pharmacist faculty, 7.8% had an alternative role and may not be best equipped to complete accurately an AS education survey. Additionally, our threshold of >50% of time spent in AS-related activities may be too much time devoted to clinical practice for some ID pharmacist faculty. Although AS-related topics and activities were drafted based on AS topics in previous literature and author opinion, some questions may have been subjective, thus introducing the risk of response bias (i.e. what one respondent views as ‘AS’ another may not).³⁵ Additionally, a considerable portion of respondents (39.2%) could not accurately identify the number of experiential education sites with AS learning experiences available to pharmacy students. Lastly, PharmD programmes vary considerably in resources and goals including number of ID pharmacist faculty, didactic class time devoted to ID and AS, and number of clinical rotation sites that offer AS learning experiences that may have influenced our survey results.

Conclusions

Our study demonstrates that AS education is incorporated into the required didactic, elective didactic and experiential education components of most US PharmD programmes, yet considerable variability exists in the content and delivery methods, and inconsistency and gaps in AS education remain. Efforts should be implemented to address the inconsistencies in AS education in PharmD programmes to ensure future pharmacists are prepared to engage in and recognize the importance of AS. Educational standardization, effective dissemination of best practices and interprofessional education delivery methods may be strategies to promote consistent AS education across healthcare professions.

Funding

This study was carried out as part of our routine work.

Transparency declarations

C. M. has served as a consultant for Allergan and Shionogi, and has received grant support from Merck. J. C. C. has served on the Speaker’s Bureau for Allergan plc. All other authors: none to declare.

Supplementary data

The survey is available as Supplementary data at JAC Online.

Author notes

orcid.org/0000-0001-7703-096X