Mapping educational opportunities for healthcare workers on antimicrobial resistance and stewardship around the world

Background Antimicrobial resistance is an important global issue facing society. Healthcare workers need to be engaged in solving this problem, as advocates for rational antimicrobial use, stewards of sustainable effectiveness, and educators of their patients. To fulfill this role, healthcare workers need access to training and educational resources on antimicrobial resistance. Methods To better understand the resources available to healthcare workers, we undertook a global environmental scan of educational programs and resources targeting healthcare workers on the topic of antimicrobial resistance and antimicrobial stewardship. Programs were identified through contact with key experts, web searching, and academic literature searching. We summarized programs in tabular form, including participating organizations, region, and intended audience. We developed a coding system to classify programs by program type and participating organization type, assigning multiple codes as necessary and creating summary charts for program types, organization types, and intended audience to illustrate the breadth of available resources. Results We identified 94 educational initiatives related to antimicrobial resistance and antimicrobial stewardship, which represent a diverse array of programs including courses, workshops, conferences, guidelines, public outreach materials, and online-resource websites. These resources were developed by a combination of government bodies, professional societies, universities, non-profit and community organizations, hospitals and healthcare centers, and insurance companies and industry. Most programs either targeted healthcare workers collectively or specifically targeted physicians. A smaller number of programs were aimed at other healthcare worker groups including pharmacists, nurses, midwives, and healthcare students. Conclusions Our environmental scan shows that there are many organizations working to develop and share educational resources for healthcare workers on antimicrobial resistance and antimicrobial stewardship. Governments, hospitals, and professional societies appear to be driving action on this front, sometimes working with other types of organizations. A broad range of resources have been made freely available; however, we have noted several opportunities for action, including increased engagement with students, improvements to pre-service education, recognition of antimicrobial resistance courses as continuing medical education, and better platforms for resource-sharing online.


Background
Antimicrobial resistance (AMR) is a looming global health problem; misuse and overuse of antimicrobials in the past 50 years has accelerated the development of resistance to antibiotics and other antimicrobial drugs [1]. With few new antibiotics in development [2][3][4], it is essential that we preserve the usefulness of existing antimicrobials. In their capacity as prescribers and educators, healthcare workers (HCWs) will need to shoulder much of the burden in stewarding the preservation and longevity of antimicrobial agents. The inappropriate use of antimicrobials-such as prescribing antibiotics for viral illnesses or prescribing broad spectrum antibiotics where a narrow spectrum antibiotic would be preferable [5]-drives the development of resistance [6]. In making smart prescribing choices, HCWs can reduce genetic selection pressures that drive the development of resistance [1]. Beyond prescribing, HCWs have roles in infection prevention and control (IPC), in advocating for rational antibiotic use, and in educating their patients on the responsible use of antibiotics.
Changing HCW and patient habits will require substantial effort to ensure that all prescribers and patients are aware of the challenges associated with AMR. Surveys suggest that many HCWs receive too little training on AMR and rational antibiotic use. In Saudi Arabia, nearly half of surveyed physicians felt that they had inadequate knowledge of antibiotic prescribing [7]. The Infectious Disease Society of America has previously stated that clinician training on antimicrobial use in the United States of America (USA) is highly variable and non-standardized [8], and medical students in both Europe and the USA have reported a desire for increased training on choosing antibiotic therapies [9,10]. The lack of coordinated approaches to AMR education of HCWs poses a challenge to ensuring prudent antimicrobial prescribing.
The WHO Global Action Plan on Antimicrobial Resistance expresses a need for all countries to include antibiotic resistance as a core component of both HCW training and continuing education [11]. To better understand this field, we present an illustrative mapping of educational programs and resources on AMR and antimicrobial stewardship (AMS) aimed at HCWs. This effort included an investigation of resources for AMR/AMS education, opportunities for continuing education, and actors in the field. This mapping exercise has allowed us to understand existing efforts and identify key areas for action in AMR education.

Methods
We sought to identify AMR educational programs targeting HCWs. For breadth, programs were identified through multiple methods, including contact with key experts, web searching, and academic literature searching. An initial literature search in August and September 2016 identified educational programs and key academic researchers who had published in the field over the previous decade. We emailed these and other key experts identified by WHO regional office contacts to request information on AMR and AMS-related educational programs. Additional experts were identified via a snowball strategy and web-searching. Experts were asked to identify recent or ongoing educational programs on AMR/AMS.
We further identified educational programs through online web-searching. We hand-searched the websites of several relevant organizations to identify past and current educational initiatives. We also conducted a non-systematic web search using combinations of a range of search-terms including "antimicrobial resistance", "antibiotic resistance", "antimicrobial stewardship," "antibiotic stewardship", "education", "course", "curriculum", and "workshop" and region or country in September and October 2016. Relevant articles, project reports, course flyers, and other resources were reviewed to identify programs. We examined national action plans concerning AMR in search of references to educational initiatives. Once identified, these programs were followed up with additional online research as necessary.
We summarized the identified programs in tabular form, including participating organizations, program types, region, and intended audience. We created codes to classify programs by program type, organization type, and WHO region. Programs that were not associated with any specific region (such as resources that were globally available and without a geographical target population) were classified as "global". Multiple program codes were assigned as necessary. Program type and organization codes were developed and updated iteratively as programs were identified to identify commonalities between initiatives.

Mapping educational initiatives
In total, we identified 94 educational initiatives related to AMR/AMS. The 94 initiatives represent a diverse array of programs including formal courses, workshops, conferences, guidelines, public outreach materials, and online-resource websites. The complete list of initiatives is presented in Table 1.
We identified 24 multi-component umbrella programs, which typically included web-based resources, videos, references to guidelines, and promotional materials, such as posters, pamphlets, or infographics. Programs that incorporated four or more program types were defined as umbrella programs. Umbrella programs tended to have broader target audiences and wider scopes; in many cases, their awareness campaign materials were targeted The DOH Manual of Procedures for Implementing AMS in Hospitals is an operational guide that is also used as a reference for developing training programs and materials. Information courtesy of the WHO WPRO regional office. Healthcare professionals This pledge designed by the World Health Organization Western Pacific regional office discusses a commitment to the use of antibiotics as prescribed, good hygiene, and encouraging responsible use in friends and family. Includes information on AMR. https://apps.wpro.who.int/amr/pledge.aspx The resource was for continuing professional development credit or provided a certificate of completion or counted towards a degree program towards a general audience, while online reading and guidelines were more often aimed at HCWs. Many umbrella programs targeted their messaging at HCWs-including physicians, pharmacists, and sometimes nurses-as a group, rather than targeting professions or specialties individually. Of the programs identified (see Fig. 1), the most common program type was websites; typically, however, online resources were only part of a larger program. This is unsurprising as online resources are effective platforms for sharing other program types, including videos, guidelines, pamphlets, and workbooks. Guidelines and handbooks were also a common resource, often shared online in government and hospital education initiatives; these described information about key patient populations and prescribing guidelines and were intended as reference resources. By contrast, we also identified a small number of workbooks and question sets intended as a teaching resource.
Other teaching resources available online included videos, webinars, and lecture slides. Online courses, including massive open online courses (MOOCs), are becoming common and often incorporate online videos and discussion boards to engage participants. In Fall 2016, there were two MOOCs on the FutureLearn platform (see Initiatives #44 and #90). The MOOC run by the University of Dundee and British Society for Antimicrobial Chemotherapy (Initiative #90) has gained global popularity. Several experts referenced this course as a resource used in their country; the course has been offered three times to date and participants have come from more than 41 countries. Figure 2 shows participating organizations grouped by type. Overall, the most commonly identified organizations were governmental bodies, often the national/ provincial/state-level body responsible for health and/ or education. We also found that health insurance companies often partnered with other organizations in the USA to support AMR education campaigns. Collaborations with industry came almost entirely from North America. Outside of the USA, the only other campaigns that partnered with a health insurance provider were in France. The European Centre for Disease Control contributed to the bulk of Professional societies, particularly those with a strong tie to AMR, were heavily involved in the creation and provision of resources for HCWs. Three examples are the British Society for Antimicrobial Chemotherapy, which has been involved in the creation of resource websites (Initiative #48), coordination of a MOOC (Initiative #90), and provision of funding for AMR education; the European Society of Clinical Microbiology and Infectious Diseases, which runs a study group on antimicrobial resistance, develops and coordinates courses, and carries out collaborative academic research; and the Infection Control Africa Network which organized a free distance learning course for HCWs in Africa in 2014. Many professional bodies with broader mandates, for example, medical associations and pediatric societies, have partnered with others to support larger projects, but were rarely the lead organization in the projects that we identified. For example, the NPSMedicineWise project (Initiative #82) in Australia engaged the Australian College of Nursing, Australian Association of Consultant Pharmacy, the Australian College of Rural & Remote Medicine, and the Australian Nursing and Midwifery Federation and many others alongside government bodies to produce resources and course content for the website.
University-led projects were typically related to online or in-person courses or to resource websites. Many of these sites provide lecture slides, or recorded video lectures (e.g. Initiative #16), as well as information on guidelines and policies (e.g. Initiative #35). Other types of organization were engaged in a wide variety of projects. Hospitals and healthcare centers, for example, engaged with umbrella programs, courses and workshops, intervention studies, and resource guides.
Most programs targeted HCWs as a broadly defined group. Figure 3 shows the target audiences for the 94 programs identified. Several programs also included components aimed at patients and the public. We found 33 programs aimed at physicians, including a small number that targeted specialists such as infectious disease physicians and pediatricians. Fewer programs specifically targeted nurses, pharmacists, and midwives, though these groups were targeted in the more general HCW programs. A small number of predominantly We identified programs from around the world, though, as expected, the programs were unequally distributed between countries and regions, with a larger share of the programs from North America and Europe. Figure 4 shows a map of the number of programs identified from each region. Many of the large-scale AMR/ AMS educational campaigns took place in wealthy American and European countries (e.g. Initiatives #15 and #59), whereas many of the programs in Africa and Asia were workshop or course based (e.g. Initiatives #1, #78, #83). The interconnected nature of some programs made them more easily producible on the part of the organizations and more easily identifiable on our part as researchers. This strategy facilitated the growth of programming in specific regions, and has made online information about AMR/AMS widely available to HCWs and the public. For instance, state-specific AMR educational initiatives, such as "Get Smart Colorado: Use Antibiotics Wisely" (Initiative #17), appeared to tailor resources or share/endorse existing resources from the comprehensive national "Get Smart" program (Initiative #15) produced by the CDC in the USA.

Discussion
Our environmental scan shows that many organizations are working to develop and share course content and educational resources for HCW training and continuing education around the world. We identified several types of resources, from traditional in-person courses to workshops and conferences, to MOOCs, to online campaign materials, to handbooks, and to workbooks. Governments, hospitals, and professional societies appear to be driving action on this front, and these three types of organization have successfully built partnerships with others including non-profits, insurance companies, and WHO regional offices.
This level of collaborative work is promising; however, we have identified opportunities for action on several fronts. First, there is an opportunity for the development of better resources and training opportunities for students in the healthcare professions. Early engagement can provide a strong foundation of AMR knowledge that students draw upon as they progress through their careers as prescribers and patient educators. Second, it appears that training for current HCWs is probably under-recognized by professional development and continuing education programs. HCWs need to have their AMR learning efforts formally recognized, as they may lack incentives to engage in substantial additional training on a purely volunteer basis. Below we discuss how addressing these two elements of training, both pre-service and continuing education, can improve the content, delivery, uptake, and scale-up of AMR/AMS education, and identify programs that are interesting models for development of further resources.

Pre-service student engagement
We identified a small number resources for students in healthcare disciplines, though research suggests that medical students in Europe and the USA have a desire for increasing training on AMR [11,12]. Researchers from the ESCMID Study Group for Antibiotic Policies have Fig. 4 Map of AMR education programs by region. Map was generated using Microsoft Excel and Bing suggested that undergraduate training should be focused on principles of AMS and building good prescribing habits [12]. Resources on these topics are available, as the MOOCs we identified often included lectures, videos, and case studies on these themes. Students, however, are unlikely to have the time to pursue these courses outside their educational program. Educational research also suggests that training at the undergraduate level should ideally be delivered through active learning sessions which allow students to integrate knowledge with practice [12,13]. We note that the small number of programs specifically targeting students have embraced opportunities for active student participation and interaction. To support their curriculum for medical students (Initiative #16), Wake Forest University designed series of smallgroup case studies with facilitator guides to allow group discussions of AMR issues. In Canada, the Do Bugs Need Drugs? Program (Initiative #14) has engaged students from medicine, pharmacy, nursing, and dentistry in delivering educational messages on AMR to students in elementary school. Canadian medical students have also been active in developing their own opportunities for AMR/AMS learning. In 2014, students at the University of Toronto created the Students for Antimicrobial Stewardship Society, which has now expanded to include students in dentistry and pharmacy and at other medical schools. The students have launched an annual awareness campaign on AMR, and organized educational lectures and interprofessional panels on stewardship to provide students with opportunities to ask questions (Initiative #37). Given the small number of programs that engage with students, there are undoubtedly more opportunities to develop resources for students. These might include the creation of educational curricula and support resources including videos and case studies, or engagement of students and student societies in broader educational programs.

Continuing education
We found that many excellent courses already exist, and several are available online at low or no cost. As content is already available, improving roll-out is a matter of ensuring that these courses can run repeatedly; preparing a course for a single session is likely a waste of resources. Another way to improve roll-out is to facilitate translation of course materials to other languages. Consulted experts noted that translating available content, such as a MOOC, from English into other languages is a slow and difficult process. Beyond the translation of lecture slides, there is a need to obtain other resources, such as academic articles and video content, in the foreign language. Creation of a database that brings together resources on AMR/AMS in other languages would facilitate the adaptation of courses between languages. Improving uptake of existing educational opportunities is also key. We note that among the resources identified, very few are accredited as continuing professional education. This is probably a major oversight-and opportunity-as evidence suggests that HCWs are not receiving enough training on AMR/AMS [14]. HCWs would likely be incentivized to participate if the courses were accredited as CME, as HCWs in many countries must undertake several hours of CME per year. Experts that we consulted expressed a desire for courses qualifying as CME, but found the accreditation process challenging and slow. To date, most courses have been developed by academic societies and there is an opportunity here for greater collaboration between academic societies and professional societies. Academic societies have knowledge and resources at their disposal and, by partnering with professional societies such as pediatric societies or nurses associations, could adapt their existing programs to meet the specific training needs of these healthcare specializations and provide training to a larger number of HCWs. Regulators and professional councils should be engaged in devising strategies to facilitate the uptake and scale-up of AMR-related preservice education and in-service training initiatives.

Other mechanisms of engagement
Many of the programs that we identified made their content freely available online. In addition to courses, we found lecture slides, video lectures, case studies, facilitator guides, handbooks, posters, and other campaign materials online. The presence of these many high-quality resources online suggests that it is not necessary for new educational campaigns and courses to reinvent the wheel; a large amount of information is already available. However, much of this content is scattered across the web. It would be very useful to develop a resource site or database of good AMR content. Collecting this content would allow educators to build off of existing educational materials and focus their efforts on developing course content specific to the local context. The ReAct Toolbox (Initiative #94) is an excellent model, providing basic information on several aspects of AMR/AMS and links to other online resources that are relevant to both LMICs and high-income countries. The main limitation of the site, and many of the other educational resources that we have identified, is that many resources are only available in English.

Strengths and limitations of this study
This project is the first attempt that we know of to map educational resources for HCWs around the world. We contacted more than 50 experts and identified educational resources and projects in all WHO regions. By identifying and classifying programs, we can see the breadth of resources already available for training HCWs on AMR/AMS.
As we relied extensively on web searching in addition to expert advice, it is likely that we identified more of some types of resource than others. Therefore, the quantity of identified programs of this type should not be interpreted as proof that these resources are the most common program type. We paired our web searching with expert input to identify those other resources that are more difficult to identify online. We recognize that some web resources, such as guidelines, are more likely to endure on the internet than others, such as advertisements for courses and conferences. We included mobile apps specific to antibiotic resistance if they were identified by experts or identified in web searches. However, it was beyond the scope of the study to search within existing medical apps to locate AMR/AMS content; this has been done elsewhere by Goff et al. [15].
We conducted our web and academic searching in English and relied upon on expert contacts to provide information on educational programs in other languages. We identified and reviewed some educational programs where the detailed information online was in French, but did not translate articles from other languages, and therefore likely missed other educational resources posted online that are only available in other languages.
Finally, we note that longevity of resources on the internet is an issue. We found many broken links, where program information could no longer be obtained. We identified many courses through course advertisements posted to the web; however, the limitations of our search strategy make it likely that we mainly identified recent courses. Further, for most courses, we cannot comment as to whether the course content has been archived on the web. While much of the content from a larger course, such as a MOOC, is likely to remain on the web, it is unlikely that the course content of shorter, inperson courses will be retained in the same way. Resource sites must monitor content to ensure it remains up to date. To facilitate the sharing of resources between countries, it will also be important to find a mechanism such that content does not become inaccessible after removal from the website.

Conclusions
In mapping the available educational programs on AMR/AMS for HCWs, we have identified 94 existing programs and resources, and several opportunities for improvement and expansion on the existing resources. Many high-quality educational campaigns already exist and there are many opportunities to adapt these programs to meet educational needs in other contexts. But gaps exist, particularly when it comes to resources for healthcare students, and provision of accredited training for current HCWs. National and international stakeholders should advocate for increased accreditation, the creation of a series of competencies for undergraduate curricula, and support resource sharing platforms. Action on these fronts would support both the goals laid out in many national AMR action plans and the desires of many HCWs to ensure that all HCWs receive sufficient training on AMR and AMS.