*Article* **Antimicrobial Stewardship Program Implementation in a Saudi Medical City: An Exploratory Case Study**

**Saleh Alghamdi <sup>1</sup> , Ilhem Berrou 2,\* , Eshtyag Bajnaid <sup>3</sup> , Zoe Aslanpour <sup>4</sup> , Abdul Haseeb <sup>5</sup> , Mohamed Anwar Hammad <sup>1</sup> and Nada Shebl <sup>4</sup>**


**Abstract:** Antimicrobial stewardship programs (ASPs) in hospitals have long been shown to improve antimicrobials' use and reduce the rates of antimicrobial resistance. However, their implementation in hospitals, especially in developing countries such as Saudi Arabia, remains low. One of the main barriers to implementation is the lack of knowledge of how to implement them. This study aims to explore how an antimicrobial stewardship programme was implemented in a Saudi hospital, the challenges faced and how they were overcome, and the program outcomes. A key stakeholder case study design was used, involving in-depth semi-structured interviews with the core members of the ASP team and analysis of 35 ASP hospital documents. ASP implementation followed a topdown approach and involved an initial preparatory phase and an implementation phase, requiring substantial infectious diseases and clinical pharmacy input throughout. Top management support was key to the successful implementation. ASP implementation reduced rates of multi-drug resistance and prescription of broad-spectrum antimicrobials. The implementation of ASPs in hospital is administrator rather than clinician driven. Outsourcing expertise and resources may help hospitals address the initial implementation challenges.

**Keywords:** antimicrobial stewardship programs; hospitals; multi-drug resistance

### **1. Introduction**

Antimicrobial stewardship programs (ASP) in hospital are interventions to reduce risks of antimicrobial treatment failures, adverse events, hospital acquired infections, rates of antimicrobial resistance and costs associated with antimicrobial prescriptions and prolonged length of stay in hospital [1]. These programs focus on optimizing the choice, dosing and route of administration of antimicrobials, monitoring their prescription and resistance patterns, and continuous provision of education and feedback to prescribers.

The programs were first implemented in the USA in the late 1990s, and started to gain popularity in Europe soon after that [2]. In an international survey carried out in 2015 by the ESCMID Study Group for Antimicrobial Policies (ESGAP) and ISC Group on Antimicrobial Stewardship, 52% of the countries had a national antimicrobial stewardship plan, 58% had ASPs in hospitals and 4% of the countries were planning antimicrobial stewardship strategies [3]. The Netherlands, France [4] and England [5] reported high rates of ASP implementation in hospitals. In the USA, a recent study suggests that 51% of the leading hospitals in the country have an active ASP. Around 59% of these hospitals had

**Citation:** Alghamdi, S.; Berrou, I.; Bajnaid, E.; Aslanpour, Z.; Haseeb, A.; Hammad, M.A.; Shebl, N. Antimicrobial Stewardship Program Implementation in a Saudi Medical City: An Exploratory Case Study. *Antibiotics* **2021**, *10*, 280. https:// doi.org/10.3390/antibiotics10030280

Academic Editor: Seok Hoon Jeong

Received: 7 February 2021 Accepted: 8 March 2021 Published: 9 March 2021

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**Copyright:** © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

ASP for more than 5 years [6]. However, the status of ASP implementation in hospitals in developing countries is less clear. Various reports point to low levels of implementation [7–9] for various reasons including: a lack of diagnostic testing and antimicrobials, sub-optimal infection prevention and control practices and the prevalent inappropriate prescribing practices [10,11]. Resistant microorganisms may spread from one person to another, one health care facility to another and one country to another [12]. Tackling antimicrobial resistance in developing countries is critical to reduce its burden in those countries, and to strengthen the global effort to contain this threat.

Like in many other developing countries, Saudi hospitals report low levels of ASP implementation, mainly in tertiary hospitals, despite having a national antimicrobial stewardship plan to implement ASPs in hospitals [13]. This is in contrast to reports of high prevalence of antimicrobial resistance and the emergence of new and rare multidrug resistant strains [14]. Worryingly, these pathogens can spread globally given that Saudi Arabia is a popular destination for millions of international travelers annually for pilgrimage (Hajj).

We recently reported that one of the factors behind the lagging implementation of ASPs in Saudi hospitals is the lack of "know how" to implement them [13]. ASPs are novel to Saudi hospitals, and their implementation would require a significant change to routine practice, where antimicrobials are heavily prescribed, often inappropriately [15,16]. A recent guide by Mendelson et al. details a generic protocol for the implementation and/ or optimization of ASP in hospitals in both developing and developed countries' contexts [17]. However, three issues may be considered. First, the protocol may provide a useful outline of the resources needed and what the programs usually entail, but it may not be sufficiently practical, and may not highlight how implementation challenges can be practically overcome. Second, although the protocol recognises the resource limitations in developing countries, it does not differentiate between implementation in developing vs. developed contexts. Third, the protocol is clinician-oriented; however, in various developing countries, such as Saudi Arabia, it is hospital administrators, not clinicians, who often make decisions about policy implementation [15]. This study aims to explore how an antimicrobial stewardship programme was implemented in a Saudi hospital, the challenges faced and how they were overcome, and the program outcomes. Findings would improve the current knowledge of ASP implementation in developing countries, and provide hospitals in the region with a practical guide to implement these programs.

#### **2. Results**

A number of areas emerged as key themes from the interviews: motives for ASP adoption, development and implementation of ASP, implementation challenges, and outcomes. Where useful, we included quotes from the participants to illustrate key points.

#### *2.1. Motives for ASP Adoption in the Medical City*

The decision to adopt and implement an antimicrobial stewardship programme was initially made by the chief executive officer (CEO) of the medical city in 2015.

"Leadership support is the biggest thing we have here (at the hospital). It was all from the leadership to begin with. After 2–3 weeks from my appointment, the CEO came to me and said I want to start this (antimicrobial stewardship) programme, and it has to be up and running . . . "

Various factors (stated in no particular order of importance) seem to have influenced this decision. First, the CEO's surgical background heightened the need to improve infection prevention and control, and reduce the prevalence of multi-drug resistant strains in the facility. The CEO's training in an international hospital with a longstanding experience of ASPs influenced their conviction of the benefits of ASPs in the organisation. Second, the CEO perceived the medical city, one of the largest and most highly specialist tertiary centres in the country, to be a pioneer, and an exemplary model for other hospitals in the region to follow suite in relation to implementing ASPs. Third, the special context of

the medical city, being a referral facility from other hospitals in the region, means that they often admit patients with complex care needs, who would have spent months in the referring hospitals. These patients tend to be colonized with multi–drug resistant strains, which are then transferred to the medical city. Fourth, the medical city is home to advanced neurosurgery and oncology centres, whose patients are immunocompromised and vulnerable to severe outcomes of multi-drug resistant infections. This context necessitated the adoption and implementation of interventions, such as ASPs, that can reduce the prevalence of multi–drug resistance and optimise the use of antimicrobials.

From the infectious diseases' consultant, clinical microbiologist, the lead antimicrobial pharmacist and infection control consultant's perspectives, the strongest motive to adopt and implement ASPs was the high prevalence of multi-drug resistant (MDR) microorganisms, particularly among Gram–negative bacteria. This was fueled by the high and inappropriate use of antimicrobials. The high prevalence of MDR organisms may have contributed to increased mortality rates, failure of surgical procedures, and may have compromised the safety of immunocompromised patients receiving specialist oncology, cardiac and neurosurgery services. The hospital was also planning to set up a transplant centre and was desperate to reduce the rates of multi-drug resistance.

"They were prescribing very expensive and inappropriate antibiotics and antifungals . . . ICU patients were mostly on 3, 4, or 5 antibiotics. It was not justifiable at all . . . We needed to start a strong antimicrobial stewardship programme for the patient's sake, and also to educate prescribers".

"We were having outbreaks of multi-drug resistant organisms and there was overuse of antibiotics. We had a major issue with drug resistant *Acinetobacter baumannii* which was sensitive to colistin, and then it became resistant to colistin. So, it became pan-drug resistant *Acinetobacter baumannii*. The infection control experts (in the hospital) said that this was because of the overuse of carbapenems in the ICU, and then the overuse of even colistin in the ICU".

"We have the oncology centre and we wanted to start the transplant centre, and of course the immunocompromised patients needed to have much fewer resistant microorganisms".

It is noteworthy that the MOH antimicrobial stewardship plan does not appear to be a motive for ASP adoption and implementation despite the medical city being a "flagship" MOH organisation.

### *2.2. Development and Implementation of the Antimicrobial Stewardship Programme* Phases of ASP Implementation

The ASP is part of the hospital's patient safety portfolio (PSP) of 10 strategic patient safety programs to address patient safety issues within the hospital and to improve the quality and safety of care. These are shown in Figure 1.

There were two phases of ASP implementation in the medical city.

Phase 1

The ASP aims to improve antimicrobial prescribing practices, reduce the high prevalence of multi–drug resistance in the hospital and the high costs associated with antimicrobials' prescribing.

Initially, the ASP programme was suggested to be part of the medication safety program, but the CEO insisted that the ASP programme should be an independent, standalone programme with its own key performance indicators.

"When we started discussing antimicrobial stewardship, the idea was that it should be part of the medications (safety) programme, but I said no, it needs to be done independently, it needs to stand out, to be very obvious and very evident"

*2.2. Development and Implementation of the Antimicrobial Stewardship Programme* 

quality and safety of care. These are shown in Figure 1.

The ASP is part of the hospital's patient safety portfolio (PSP) of 10 strategic patient safety programs to address patient safety issues within the hospital and to improve the

Phases of ASP Implementation

**Figure 1.** Patient safety portfolio of programs. **Figure 1.** Patient safety portfolio of programs.

The hospital had no expert staff "in house" to set up and implement the ASP, so it outsourced a locum infectious disease pharmacist, who trained in a hospital in the USA. The locum ID pharmacist reviewed current practices and the potential implementation barriers, and provided practical guidelines on how these could be overcome. The hospital then appointed an antimicrobial lead pharmacist, who worked with the locum ID pharmacist, and the ID consultant to draft the hospital ASP policy (based on the Infectious Diseases

Society of America (IDSA) ASP guidelines) [1,18], the formulary restriction list (based on local antibiogram and MDROs surveillance reports), and set up the ASP team.

"we started with first thing formulary restriction based on the MDR (multi-drug resistance) pattern at the hospital. What are the medicines that we need to restrict firstWe started with broad spectrum antibiotics . . . carbapenems, meropenem, imipenem, colistin . . . and then with the antifungals voriconazole, posaconazole . . . then we included caspofungin, micafungin and anidulafungin since they have a high cost . . . "

The core members of the ASP team at the medical city were:


The roles and responsibilities of each team member are presented in Figure 2. The ASP team maintained direct (and frequent) communication with key stakeholders such as the heads of ICU, hematology and oncology departments (where antimicrobials' use and resistance were high), and the head nurse (whose team is directly affected by the change in how antimicrobials will be obtained and administered). Those key stakeholders were often invited to take part in ASP team meetings, and become members of the bigger ASP team. telling, understanding, and providing feedback…it will be applied and implemented as restricted antibiotics will not be approved unless it is necessary. If it (restricted antibiotic) is prescribed, it will not be approved by the ID team (unless the form is filled in)" Training members of the ID team and the clinical pharmacists on how to carry out the daily ASP tasks once the programme goes live at beginning of January 2016.


**Figure 2.** Roles and responsibilities of core members of the ASP team. ASP (antimicrobial stewardship programme); ID (Infectious Diseases); DOT (Days of Therapy). **Figure 2.** Roles and responsibilities of core members of the ASP team. ASP (antimicrobial stewardship programme); ID (Infectious Diseases); DOT (Days of Therapy).

intervention and feedback) of ASPs were implemented. In January 2016, the plan was to introduce the restriction form into hospital departments with the least prescriptions of broad-spectrum antimicrobials (neuroscience and surgery) to identify potential implementation issues, and manage the workload of the small ID team at the time. However, the hospital decided to roll out the form into all the remaining departments including ICU, hematology and oncology because of the recruitment of more ID clinicians, which expanded the capacity of the ID team to review and authorize physicians' requests of restricted antimicrobials. Furthermore, the ID team provided 24 h, 7 days a week "on call"

"Each unit is covered by ID (Infectious disease team) for these forms. They meet every morning. They meet with the clinical pharmacist in that unit. They will also review

cover dedicated to reviewing and authorising (or not) restriction forms.

Phase 2

The team developed an antimicrobial restriction form and discussed it with hospital physicians, and clinical and hospital pharmacists. The form was introduced on a trial basis, to get physicians used to filling in the form and discussing prescription decisions with the ID consultant. It was then updated based on prescribers' and pharmacists' feedback, before approval by the medical records committee. A copy of the antimicrobial restriction form and the associated workflow is included in Supplementary File S1.

The remaining steps of the implementation plan were then agreed; these included:

Raising awareness of antimicrobial resistance and the outcomes of inappropriate antimicrobials' use through a hospital-wide health promotion event lasting for a week and coinciding with the World Antimicrobial Awareness Week (18–24 November 2015).

"everyday was targeted to specific people or specific departments. We published a newsletter about antimicrobial stewardship and we had small antimicrobial stewardship contests".

Antimicrobials prescribing training sessions for physicians:

"We let people get used to filling the forms, and know which antibiotics are restricted. Before there was resistance, and now everyone knew that it is just a matter of telling, understanding, and providing feedback . . . it will be applied and implemented as restricted antibiotics will not be approved unless it is necessary. If it (restricted antibiotic) is prescribed, it will not be approved by the ID team (unless the form is filled in)"

Training members of the ID team and the clinical pharmacists on how to carry out the daily ASP tasks once the programme goes live at beginning of January 2016.

Phase 2

The two core strategies (restriction and preauthorization, and prospective audit with intervention and feedback) of ASPs were implemented. In January 2016, the plan was to introduce the restriction form into hospital departments with the least prescriptions of broad-spectrum antimicrobials (neuroscience and surgery) to identify potential implementation issues, and manage the workload of the small ID team at the time. However, the hospital decided to roll out the form into all the remaining departments including ICU, hematology and oncology because of the recruitment of more ID clinicians, which expanded the capacity of the ID team to review and authorize physicians' requests of restricted antimicrobials. Furthermore, the ID team provided 24 h, 7 days a week "on call" cover dedicated to reviewing and authorising (or not) restriction forms.

"Each unit is covered by ID (Infectious disease team) for these forms. They meet every morning. They meet with the clinical pharmacist in that unit. They will also review all the (restriction) forms, and if it is justified they will approve it. If they are not satisfied, they look into the patient's file, and then discuss with the prescribers. The discussion with the prescriber is mainly because we want the education to play a role (in the programme)".

In addition to antimicrobials' restriction, the ASP team conducted regular auditing of antimicrobials' prescribing, communicated rates of antimicrobials' prescribing to relevant heads of departments, and provided feedback to prescribers. Prospective audit and feedback were also carried out by the pharmacy team to ensure adherence to antimicrobials' guidelines and optimise antimicrobials' dosing before input from the ID team; the infectious disease physicians and the clinical pharmacists maintained regular contact with the medical team regarding patients on antibiotics. The clinical pharmacists were responsible for documenting the daily follow ups or recommendations on the patients' files. They would document their input under the title "ASP Pharmacy Assessment".

The microbiology team started selective reporting of antibiotic susceptibility testing to reduce physicians' prescribing of restricted antimicrobials such as meropenem and imipenem:

"We follow cascade reporting . . . microbiology (started) to minimise the disclosure of all susceptibility reporting".

The ASP team continued to meet monthly to review rates of antimicrobial resistance, DOT (days of therapy) data and the list of restricted antimicrobials. Feedback from physicians and heads of department regarding antimicrobials' prescribing needs was discussed and addressed. Examples include drafting guidelines on the prescribing of oral fosfomycin for UTIs, surgical prophylaxis, granulocytopenia and vancomycin dosing.

imipenem:

all susceptibility reporting".

"Most of our physicians do not use Fosfomycin because they do not believe that oral medication can be used against multi-drug resistant organisms like ESPL (Extended-Spectrum Beta-Lactamases) or CRB (Chlorine-Resistant Bacteria) . . . we have a lot of patients now deescalating to fosfomycin" "Most of our physicians do not use Fosfomycin because they do not believe that oral medication can be used against multi-drug resistant organisms like ESPL (Extended-Spectrum Beta-Lactamases) or CRB (Chlorine-Resistant Bacteria)…we have a lot of patients now deescalating to fosfomycin"

all the (restriction) forms, and if it is justified they will approve it. If they are not satisfied, they look into the patient's file, and then discuss with the prescribers. The discussion with the prescriber is mainly because we want the education to play a role (in the programme)". In addition to antimicrobials' restriction, the ASP team conducted regular auditing of antimicrobials' prescribing, communicated rates of antimicrobials' prescribing to relevant heads of departments, and provided feedback to prescribers. Prospective audit and feedback were also carried out by the pharmacy team to ensure adherence to antimicrobials' guidelines and optimise antimicrobials' dosing before input from the ID team; the infectious disease physicians and the clinical pharmacists maintained regular contact with the medical team regarding patients on antibiotics. The clinical pharmacists were responsible for documenting the daily follow ups or recommendations on the patients' files. They

The microbiology team started selective reporting of antibiotic susceptibility testing to reduce physicians' prescribing of restricted antimicrobials such as meropenem and

"We follow cascade reporting…microbiology (started) to minimise the disclosure of

The ASP team continued to meet monthly to review rates of antimicrobial resistance, DOT (days of therapy) data and the list of restricted antimicrobials. Feedback from physicians and heads of department regarding antimicrobials' prescribing needs was discussed and addressed. Examples include drafting guidelines on the prescribing of oral fosfomycin for UTIs, surgical prophylaxis, granulocytopenia and vancomycin dosing.

would document their input under the title "ASP Pharmacy Assessment".

Education efforts were ongoing throughout the second phase of implementation. Prescribers' education has been a fundamental component for ASP success at the medical city. Figure 3 shows the timeline for implementing the ASP in the medical city. Education efforts were ongoing throughout the second phase of implementation. Prescribers' education has been a fundamental component for ASP success at the medical city. Figure 3 shows the timeline for implementing the ASP in the medical city.

**Figure 3.** The timeline for implementing the ASP in the medical city. **Figure 3.** The timeline for implementing the ASP in the medical city.

*Antibiotics* **2021**, *10*, x FOR PEER REVIEW 7 of 17

#### *2.3. ASP Implementation Challenges*

*2.3. ASP Implementation Challenges*  Various factors affected the implementation of ASP in the medical city. Various factors affected the implementation of ASP in the medical city.

#### 2.3.1. Shortage of ASP Staff

2.3.1. Shortage of ASP Staff During the initial phase, the availability of only one ID consultant, and no other clinician with ID expertise forced the ASP team to optimise ID input, and resulted in an initial "short" list of restricted antimicrobials requiring approval from the ID consultant.

"We started with one ID consultant, we did not have anyone else. That's why we needed as much concise shortlist as we can".

During phase 2, the hospital recruited more ID clinicians, resulting in rolling out the ASP across all hospital departments. The shortage of ID physicians has been attributed to the lack of infectious diseases training programs for physicians in the Middle East and most Asian countries.

Shortage of microbiology personnel and facilities at the medical city also challenged the implementation of the programme. The medical city had only one consultant clinical microbiologist, heading a team of microbiology technicians. Supply issues of laboratory consumables and equipment, due to financial pressures, placed constraints on how quickly susceptibility tests were reported:

"we do not have items coming regularly. Sometimes we even run out of gram stain reagents and we need to borrow them from other hospitals . . . we would like to have some key equipment like MALDI/TOF (matrix-assisted laser desorption ionization time-of-flight mass spectrometry)... we all know there are financial constraints . . . so we have supply issues, space issues and financial issues".

#### 2.3.2. Incompatible IT Systems

One of the biggest challenges to ASP implementation at the medical city, as reported by the participants, was the incompatibility of the electronic medical system in the hospital with the requirements of the ASP, so several data had to be generated manually (antimicrobials' costs data, DOT data and data for the hospital antibiogram). Furthermore, the restriction forms could not be submitted electronically, they had to be filled in manually, and hard copies had to be collected by pharmacists, and reviewed and authorised by ID physicians:

"we have some constraints in our hospital information system . . . we are trying to work around that";

"The health information system at the hospital is not supportive enough, to get accurate data, as we collect data manually (in all departments), which consumes time and manpower".

Physicians' resistance to ASP formulary restrictions and policies

The physicians were initially resistant to formulary restrictions and the need to obtain ID approval for the prescription of restricted antimicrobials for numerous reasons:

1. Physicians' worry about complications given that their patients tend to be complex, immunocomprosied and systemically unwell.

"At the beginning we faced resistance, especially in the critical areas in haematology and oncology because they (physicians) say our patients are sick".

2. During phase 1, the resistance appears to be mainly towards ID clinicians' involvement. The physicians at the hospital were routinely making antimicrobial prescription decisions without seeking input from the only ID consultant; who would not have been able to provide input to all departments. During phase 2, after the ID consultant, and later the ID team, became more involved in decisions about antimicrobial prescriptions, the physicians started to seek more consultations and input from the ID team:

"Now the doctors trust more the ID (infectious diseases) team with their consultations. I think also since the ID team started to be more involved with the restriction and talking to convince the doctors that this needs de-escalation . . . ".

3. Resistance to change: Before the implementation of the ASP, the physicians routinely prescribed antimicrobials empirically and prescribed more than one broad-spectrum antimicrobial, without much reliance on susceptibility reporting. The restriction of prescribing options, and the need to rely on susceptibility reporting and ID approval, was a significant change to their routine practice.

"People tend to treat empirically instead of trying to diagnose".

#### *2.4. Critical Factors for the Sucessful Implementaion of ASP in the Medical City*

A number of factors have been identified as key to the implementation of the ASP in the hospital.

#### 2.4.1. Top Management Support

The decision to adopt and implement ASP in the medical city was made by the CEO. Top management support ensured dedicated financial resources for ID clinicians' and locum ASP pharmacist recruitment. Furthermore, senior managers instructed the hospital departments to engage with the ASP team's educational events and process changes. This support was provided throughout the implementation phases, and was perceived by the participants to be a key determinant of the successful implementation of the ASP:

"There is a lot of commitment from the administration and the leadership";

"Leadership support is the biggest thing we have here".

#### 2.4.2. Project Management Training

When the PSP programmes and projects were outlined, the hospital administration provided project management training (outsourced) to clinicians involved in these projects including the ASP project. This entailed training on how to write policies and project proposals, identify project outcomes, carrying out relevant data analysis, and strategies to influence behavior change.

#### 2.4.3. A Dedicated ASP Team

A key facilitator to ASP implementation was setting up a dedicated ASP team. This meant that there was a specific person (or group) that maintained open, constant communication with the hospital staff regarding ASP, and was always available for assistance with the implementation of the program. The group members had clear roles and responsibilities and communicated frequently to track the progress of the implementation plan and evaluate its outcomes.

#### 2.4.4. Increased ID Clinicians' Involvement in the Prescribing and Monitoring of Antimicrobials

The implementation of ASP in the hospital aimed to change physicians' antimicrobial prescription behaviors, through the restriction of certain antimicrobials, the prescribing of which would require the input of an ID clinician. The ID team ensured that an ID clinician was available over 24 h, 7 days a week to review restriction forms, authorise requests if appropriate and suggest alternative antimicrobials if needed. This increased provision facilitated physicians' cooperation and reduced their resistance to the process changes:

"even weekends they (ID team) come to just sign and review the forms, and there is always an ID on call for antimicrobial stewardship beside the ID on call".

The ID team also delegated antimicrobials' dose optimisation to the pharmacy team in recognition of clinical pharmacists' skills and expertise, and to manage the workload associated with the increased cover:

"The ID consultant sent a memo to the whole hospital that the ID consultant, ID doctors and hospital physicians will recommend the regimen, and the dosing will be the responsibility of the pharmacist. That was a huge thing, and everyone was following this recommendation".

Figure 4 summarizes the nine essential steps for ASP implementation in hospital, fostered by strong senior management support and governed by key implementation strategies. Hospitals in the region should first start by setting up the ASP program as a stand-alone program with defined aims and outcome measures. Then, an ASP team needs to be set up with clear roles and responsibilities, especially in relation to the day-to-day management of the implementation and oversight of the program. The ASP team would need to be trained on how to manage the project, carry out the implementation steps, evaluate interventions and modify the implementation plans based on feedback from users. Relevant ASP interventions would then have to be designed and refined based on clinicians and administrators' feedback, followed by education campaigns and training sessions with the clinicians to improve their engagement and reduce their resistance. Throughout the constant engagement with clinicians and hospital administrators, barriers to implementation need to be identified and addressed prior to implementation. The ASP program can be piloted in departments with the least antimicrobial prescribing and resistance issues, before launching it throughout the remaining departments. This is a cyclical process, and sustaining successful outcomes and good practice may require refining the ASP aims and outcomes, adding more members to the ASP team, further education and training and ongoing exploration and identification of barriers to adherence to ASP policies and procedures. Senior management support is paramount throughout the implementation process. The ASP team should have autonomy in managing and refining the ASP, should focus on achieving the defined ASP outcomes, and employ an education approach to help clinicians adhere to the restrictive requirements of the program.

proach to help clinicians adhere to the restrictive requirements of the program.

management of the implementation and oversight of the program. The ASP team would need to be trained on how to manage the project, carry out the implementation steps, evaluate interventions and modify the implementation plans based on feedback from users. Relevant ASP interventions would then have to be designed and refined based on clinicians and administrators' feedback, followed by education campaigns and training sessions with the clinicians to improve their engagement and reduce their resistance. Throughout the constant engagement with clinicians and hospital administrators, barriers to implementation need to be identified and addressed prior to implementation. The ASP program can be piloted in departments with the least antimicrobial prescribing and resistance issues, before launching it throughout the remaining departments. This is a cyclical process, and sustaining successful outcomes and good practice may require refining the ASP aims and outcomes, adding more members to the ASP team, further education and training and ongoing exploration and identification of barriers to adherence to ASP policies and procedures. Senior management support is paramount throughout the implementation process. The ASP team should have autonomy in managing and refining the ASP, should focus on achieving the defined ASP outcomes, and employ an education ap-

**Figure 4.** ASP implementation process model. **Figure 4.** ASP implementation process model.

#### *2.5. Outcomes of ASP implementation 2.5. Outcomes of ASP implementation*

The ASP implementation outcomes set out by the ASP team were: reduction of antimicrobial resistance rates, rates of multi-drug resistant microorganisms, antimicrobials' usage (DOTs) and costs (we were not able to obtain data for all the outcomess). These were used as key performance indicators (KPIs) and were regularly monitored by the ASP committee. The ASP implementation outcomes set out by the ASP team were: reduction of antimicrobial resistance rates, rates of multi-drug resistant microorganisms, antimicrobials' usage (DOTs) and costs (we were not able to obtain data for all the outcomess). These were used as key performance indicators (KPIs) and were regularly monitored by the ASP committee.

Following the implementation of the ASP in 2016, the hospital achieved a reduction in resistance rates (Table 1) and antimicrobials' usage (Table 2). The hospital either sustained or slightly increased levels of the susceptibility of microorganisms to antimicrobials throughout 2017–2019. However, antimicrobial usage seems to have increased over the years. DOT data of 2019 shows a particularly marked increase compared to data from 2018 Following the implementation of the ASP in 2016, the hospital achieved a reduction in resistance rates (Table 1) and antimicrobials' usage (Table 2). The hospital either sustained or slightly increased levels of the susceptibility of microorganisms to antimicrobials throughout 2017–2019. However, antimicrobial usage seems to have increased over the years. DOT data of 2019 shows a particularly marked increase compared to data from 2018 (data shown in Tables S1 and S2 of Supplementary File S2) This increase has been attributed to a number of reasons (suggested through personal communication) including: setting up a solid organ transplant center in 2018 and the associated increase in patient numbers and prescribing antimicrobials, an incremental 20% increase in patients' numbers annually and increased numbers of extended-spectrum β-lactamase (ESBL) isolates due to the restriction of prescribing board spectrum antimicrobials, which led to increased use of piperacillin/tazobactam, cefepime and quinolones. Furthermore, Meropenem's use doubled, and micafungin's use tripled from 2018 to 2019. In 2019, the hospital decided to reduce the use of imipenem and limit its use to resistant *Enterococcus facium*, due to cost. The alternative, Meropenen, was more cost-effective, and was being prescribed instead. Similarly, Micafungin was being prescribed as an alternative to the more expensive antifungals caspofungin and anidulafungin in late 2018. Later in 2019, anidulafungin was re-added to the formulary for limited patients with liver impairment.


**Table 1.** Hospital antibiogram data (2015–2016) showing the percentage of sensitive susceptibilities between specific microorganisms (columns) and antibiotics (rows).

**Table 2.** Hospital DOT data for July–Dec 2015 (before ASP implementation) and January–June 2016 (after).


In late 2020, we sought updates on the status and outcomes of the ASP in the hospital. Supplementary File S3 includes a summary of personal communications with the hospital' s ASP team.

#### **3. Discussion**

Top management initiation and support of ASP implementation in the hospital, combined with a team approach to planning, implementing and monitoring of the ASP has led to the successful implementation of the program in the hospital. The implementation challenges reported in this study have been reported nationally in Saudi Arabia [13], but this hospital demonstrates that implementation remains possible if key players (top management and ASP team members) work together, effectively, to address those challenges.

In this case study, we demonstrate how managerial and clinical interests can be aligned to reduce antimicrobial resistance rates, and pioneer the implementation of ASPs to enhance the hospital's reputation. Alignment of managerial and clinical interests has been shown to be a key determinant of the success of quality improvement interventions [19]. Furthermore, in contrast to a typical top-down order delegation approach, the CEO empowered the members of the ASP team to take over the responsibility of ASP, monitor its key performance indicators, and make autonomous decisions. This empowering leadership strategy was key to the successful implementation of ASP in our study, and was also reported in Steinmann et al. study [20].

The initial lack of "know how" to implement ASPs and the national shortage of ASP team members have widely been reported to hinder ASP implementation [15,21]. However, top management support ensured the allocation of the necessary funds and resources, and outsourcing expert staff to help hospital staff implement ASPs. Other reported examples also include outsourcing laboratory services [22] or pharmacy services [23]. ASP implementation in the hospital could only occur once more ID clinicians were recruited. Other hospitals may not be able follow example given the national shortage of these specialists. To overcome the shortage of ID clinicians, hospitals in South Africa implemented

an alternative pharmacist-led ASP [24], highlighting the need to adapt ASP programs and interventions to maximise the use of scarce resources. We also suggested in [13] that regional/local ASP hubs can be set up so that ID and clinical pharmacists' resources are shared to improve ASP implementation in hospitals.

The lack of and/or incompatibility of information technology (IT) systems with antimicrobial stewardship interventions hinders ASP implementation [15,25]. Innovation and integration of compatible IT systems improves the processes and outcomes of ASPs in hospitals [26]. Moreover, physicians' resistance to ASP restrictions on prescribing antimicrobials also affects ASP implementation. In their study, Perozziello et al. [27] suggests that ASP education interventions, instead of restrictive ones, can improve physicians' engagement with ASP implementation. In our study, education, early engagement with physicians, and trialing interventions prior to full implementation increased physicians' engagement despite the initial resistance. This was also shown by Alawi et al. 2016 [28].

ASP implementation in the hospital reduced antimicrobial consumption and rates of some resistant strains, which further strengthens the evidence base for their effectiveness [28–30]. However, restricting antimicrobials may reduce resistance of some strains but increase the resistance of other strains, also known as the "'squeeze the balloon effect" [31]. Resistance rates are also affected by the duration of antimicrobial treatment [32]. These should be considered when evaluating ASP outcomes. It is also important that hospitals monitor resistant rates, especially those of MDR, to target efforts to curb it [33]. Interesting perspectives are emerging, calling for a radical rethinking of what antimicrobial stewardship programs should entail, such as Vickers et al. calling for innovative commercial models to stimulate novel antimicrobial development, and integrating rapid diagnostics and infection control practices within the program [34]. Furthermore, given the enormity of the antimicrobial resistance threat, all possible strategies to identify novel or repurpose old agents to confer antimicrobial properties should be considered, including exploring the antimicrobial properties of essential oils [35].

The findings of our study can help Saudi hospitals develop and implement ASPs. We identified a number of challenges and the strategies to overcome them. Our findings, however, need to be interpreted with caution. First, our case study involves a single hospital. Although there are various lessons to be learnt on ASP implementation, there is no "one size fits all" approach, and other hospitals need to adapt the recommendations of our study before adopting this implementation model. Future research could use a comparative case study approach to analyze the similarities, differences and patterns across different hospitals. Second, we have not explored the effectiveness of ASP post implementation. Although we demonstrate that the ASP led to reduced antimicrobial consumption and a reduction in rates of resistance, an analysis of long-term effects is needed, through a longitudinal study, to understand if ASP processes and outcomes can be sustained. Third, our key informants included ASP team members and the hospital's CEO. Exploring input from other ASP key players, such as hospital information technologists and middle managers could provide further insights on how interventions can be successfully implemented.

#### **4. Methods**

This study used a key stakeholder case study design [36], focusing on a tertiary care center (medical city) that implemented an antimicrobial stewardship program in 2016. The hospital has a 1500 bed capacity, consists of a coronary care unit (CCU), cardiac surgery intensive care unit (CSICU) and provides cardiac, hematology, oncology, neuroscience, medical and specialized surgery services. Qualitative methods were used, focusing on indepth semi-structured interviews and analysis of relevant documents. The core members of the ASP team, including an ID consultant (Director of the ASP), a clinical pharmacist (Manager of the ASP), a consultant clinical microbiologist, an infection control consultant, and the CEO of the medical city were interviewed in July 2017, for 29–45 min. The interviews were conducted face-to-face in the participants' main language (Arabic or

English), audio recorded and transcribed verbatim. Additional data were collected through content analysis of 35 ASP hospital documents.

The interview schedule was developed following a review of the literature and discussions with three ASP pharmacists (two from Saudi Arabia and one from the UK) and two ID consultants (from Saudi Arabia). Questions in the schedule were all open-ended to obtain in-depth views and perspectives of the study participants. The interview schedule has two main sections. The first is a section on background information (three questions), such as the position of healthcare professionals, gender and years of experience. In the second section, 12 open-ended questions were used to explore the components of the ASP in the medical city, members of the ASP team and their responsibilities, the adoption and implementation process of the ASP, and the factors influencing the adoption and implementation process of the ASP in the medical city. Probing questions were also asked based on the responses of the participants to obtain further details.

#### **5. Conclusions**

Successful ASP implementation in Saudi hospitals is administrator-driven and requires a hospital leadership that empowers clinicians to take responsibility for implementing the program. Outsourcing expertise and resources could help hospitals address some of the implementation challenges. However, a compatible IT infrastructure that integrates ASP interventions is key to improving implementation and monitoring outcomes.

**Supplementary Materials:** The following are available online at https://www.mdpi.com/2079-638 2/10/3/280/s1, Supplementary File S1: A copy of the hospital's antimicrobial restriction form and the associated workflow is included; Supplementary File S2: Hospital antibiogram data (2015–2019) and DOT data (2018–2019) are included under Tables S1 and S2, respectively. Supplementary File S3: Hospital ASP updates.

**Author Contributions:** Conceptualization, S.A., I.B. and N.S.; methodology, S.A., I.B. and N.S.; software, S.A. and M.A.H.; validation, S.A., I.B. and N.S.; formal analysis, S.A. and I.B.; investigation, S.A. and E.B.; resources, S.A.; data curation, S.A., E.B., A.H.; writing—original draft preparation, S.A., I.B. and N.S.; writing—review and editing, S.A., I.B., N.S., Z.A.; visualization, S.A., N.S., I.B.; supervision, I.B., N.S., Z.A.; project administration, S.A.; funding acquisition, S.A. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research is part of S.A. PhD studentship. The PhD studentship of S.A. is funded by Albaha University (Albaha, Saudi Arabia).

**Institutional Review Board Statement:** This study was approved by the Health and Human Sciences Ethics Committee of the University of Hertfordshire (Hatfield, UK) (protocol no. LMS/PGR/UH/02344). Official permissions to conduct this research was granted by the hospital taking part in this study.

**Informed Consent Statement:** Informed consent was obtained from all subjects involved in the study.

**Data Availability Statement:** Data are contained within the article or Supplementary Material (Appendices 1 and 2).

**Acknowledgments:** We would like to thank all the participants for taking part in this study.

**Conflicts of Interest:** The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

#### **References**


### *Article* **Development of and User Feedback on a Board and Online Game to Educate on Antimicrobial Resistance and Stewardship**

**Diane Ashiru-Oredope 1,\* , Maxencia Nabiryo <sup>1</sup> , Andy Yeoman <sup>2</sup> , Melvin Bell <sup>2</sup> , Sarah Cavanagh <sup>1</sup> , Nikki D'Arcy <sup>1</sup> , William Townsend <sup>3</sup> , Dalius Demenciukas <sup>2</sup> , Sara Yadav <sup>1</sup> , Frances Garraghan <sup>1</sup> , Vanessa Carter <sup>1</sup> , Victoria Rutter <sup>1</sup> and Richard Skone-James <sup>3</sup>**


**Abstract:** Antimicrobial resistance (AMR), particularly antibiotic resistance, is one of the most challenging global health threats of our time. Tackling AMR requires a multidisciplinary approach. Whether a clinical team member is a cleaner, nurse, doctor, pharmacist, or other type of health worker, their contribution towards keeping patients safe from infection is crucial to saving lives. Existing literature portrays that games can be a good way to engage communities in joint learning. This manuscript describes an educational antimicrobial stewardship (AMS) game that was co-created by a multidisciplinary team of health professionals spanning across high- and low- to middleincome countries. The online AMS game was promoted and over 100 players across 23 countries registered to participate on 2 occasions. The players were asked to share feedback on the game through a short online form. Their experiences revealed that the game is relevant for creation of awareness and understanding on antimicrobial stewardship in both high- and low-to-middle income settings worldwide.

**Keywords:** antimicrobial resistance (AMR); antimicrobial stewardship (AMS); AMS Game; board game; online game; Commonwealth Partnerships for Antimicrobial Stewardship; CwPAMS; gaming; game-based learning; gamification

### **1. Introduction**

Antimicrobial resistance (AMR), particularly antibiotic resistance, is one of the most challenging global health threats of our time [1]. Even under the shadow of COVID-19, AMR posed a substantial threat to patients who developed secondary bacterial infections [2]. AMR causes challenges to the treatment of infections and infectious diseases, including HIV/AIDS, typhoid, cholera, tuberculosis, gonorrhoea, hospital-associated infections, and malaria, which disproportionately affect low- and middle-income countries (LMICs) [1]. AMR is also particularly prevalent and problematic in LMICs where health systems and medical resources, including access to water, sanitation, and hygiene (WASH), are limited, as well as where socioeconomic drivers, such as extreme poverty, increase the risk of communicable diseases exponentially [3]. The Fleming Fund was created in response to this need, and has funded many programmes of work, including the Commonwealth Partnerships for Antimicrobial Stewardship Programme (CwPAMS). CwPAMS addresses AMR through antimicrobial stewardship interventions in eight African Fleming Fund priority countries, using a health partnership approach.

**Citation:** Ashiru-Oredope, D.; Nabiryo, M.; Yeoman, A.; Bell, M.; Cavanagh, S.; D'Arcy, N.; Townsend, W.; Demenciukas, D.; Yadav, S.; Garraghan, F.; et al. Development of and User Feedback on a Board and Online Game to Educate on Antimicrobial Resistance and Stewardship. *Antibiotics* **2022**, *11*, 611. https://doi.org/10.3390/ antibiotics11050611

Academic Editor: Albert Figueras

Received: 12 March 2022 Accepted: 24 April 2022 Published: 1 May 2022

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

**Copyright:** © 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

Tackling AMR requires a multidisciplinary approach. Whether a clinical or healthcare team member is a nurse, doctor, pharmacist, cleaner, or other type of health worker, their contribution towards keeping patients safe from infection and the spread of resistant organisms is crucial to saving lives.

Existing literature portrays that games can be a good way to engage communities in joint learning [4,5]. Evidence shows that games have been used to promote health and wellbeing in regard to both infectious and non-infectious diseases [6]. As a health education tool, games have proven to be an enjoyable method that enhances learning through stimulating players' interests and motivation [6,7]. While existing studies largely point to games as an impactful educational tool for children and students, some studies have demonstrated that games can be used as a capacity-building intervention for health professionals [8]. Games can be used for improving health professionals' knowledge and skills, changing their attitudes and performance, and improving how they care for their patients [8]. Despite the strong indication that games can improve knowledge, several studies including those conducted among health professionals do not show sufficient evidence that games can improve performance or change behaviour [7,9–11]. To this end, there is a need for more research with a focus on outcomes that go beyond knowledge assessment, to include outcomes such as skills, behaviour, and patient outcomes [10].

Few existing studies highlight that AMS games can be an innovative way of spreading awareness on AMR. A study conducted in Saudi Arabia among students concluded that gamification using an AMS board game can significantly improve AMR knowledge, with better retention than a conventional lecture [12]. In another study conducted in the UK among children aged 7–15 years, it was reported that antibiotic games improved knowledge on the use of antibiotics for bacterial versus viral infections and ensured that the course of antibiotics was completed [13]. The antimicrobial stewardship (AMS) game described in this manuscript was developed to encourage players (healthcare teams including students, doctors, laboratory staff, pharmacists, and nurses) to discuss AMS and learn what they can do personally, and collectively, to improve stewardship in their organisation and their community. The intention was to create a game for groups to play, and in order to make the game more widely accessible, a physical printed tabletop board game was developed with an online version for groups working remotely. Further, it is intended that the game would encourage the player to understand the scale of the AMR problem and that everyone who uses, dispenses or prescribes antimicrobials is part of the solution to reduce the impact of AMR. Effective training and capacity building are vital to the success of stewardship programmes, particularly when staff are new to the concept. The AMS game is intended to make stewardship training engaging and inclusive, generating fun and enthusiasm with a serious purpose and clear outcomes.

Focus Games Ltd. was the game development partner for this project. Focus Games Ltd. has been a leading developer of 'serious' educational games/game-based learning and simulations since 2004. They have developed over 100 different games for staff, patients, and the public that address a wide range of clinical, health, and wellbeing issues.

Independent evaluations of these games demonstrate that they can improve knowledge and encourage beneficial changes in thinking and behaviour [14].

Subject matter expertise, technical competency, and decision-making are diluted when individuals cannot communicate effectively with the people around them. These interpersonal skills can be learned and developed in the same way that subject matter expertise is developed. However, because these interpersonal 'soft' skills are largely intangible, we need to find appropriate ways of teaching.

Although there is not a definitive theoretical framework for the development of serious games, key elements of good practice have previously been summarised [15]. In development of the AMS game several elements of published good practice [15], were considered for incorporation:

• Competition and goals, with players competing against other players both for the physical and online games.

	- Mechanics: the elements of the game that control gameplay.

The development of the AMS game involved a wide range of stakeholders from across the globe, who represented the target audience for which the game was being developed. To test the usability of the developed AMS game, we used online platforms to invite interested individuals including healthcare teams to play the AMS game and asked them to share their experiences through an online feedback survey form. across nine countries (Ghana, Kenya, Malawi, Nigeria, Sierra Leone, Tanzania, Uganda, United Kingdom, and Zambia) that were all part of the countries of focus for the CwPAMS programme. Phase 3—Prototype and Testing: A rapid prototyping approach was used, incorpo-

#### **2. Materials and Methods** rating data from the pilot scenario and interviews with subject matter experts (SMEs). The

The game was developed by the Commonwealth Partnerships for Antimicrobial Stewardship Programme (CwPAMS), led by the Commonwealth Pharmacists Association (CPA) and Tropical Health and Education Trust (THET) in partnership with Focus Games Ltd. The CPA was the overall technical lead for developing the antimicrobial stewardship concepts (questions and answers) used in the game. Focus Games Ltd. was responsible for programming the AMS concepts into a playable game. THET's coordination expertise was leveraged in bringing together relevant partners to support the development of the game. game mechanism and design were finalised. The written content was drafted and loaded into the game mechanism. The game was subsequently tested in workshops with SMEs whose feedback informed design iterations. Phase 4—Refine, Rework, and Launch: production of the final design and implementation of the distribution and commercialisation strategy. The model and process used are based on practical experience of developing 100 educational games that are being actively used by healthcare professionals around the world. Focus Games have previously evaluated third-party frameworks and models and

#### *2.1. AMS Game Development* have found many of them impractical for the purpose of developing game-based learning

The AMS game used the Focus Games Ltd. development process/pathway (Figure 1). for the healthcare setting.

**Figure 1.** Focus Games Ltd's Game development process/pathway [16]. **Figure 1.** Focus Games Ltd's Game development process/pathway [16].

*2.2. Target Audience for the AMS Game* The AMS game is intended to support education on antimicrobial stewardship among current and future healthcare team members, including doctors, nurses, pharmacy teams, laboratory staff, and students. In order to optimise relationships and collaboration between stakeholders and programme team, Focus Games Ltd. used a range of project management tools to ensure that resources and priorities were managed efficiently and that they were overseen by a programme manager.

The game was co-created between partners in the UK and eight African countries

The four broad areas addressed in the game are introduction to antimicrobial resistance and stewardship, appropriate use of antimicrobial agents, infection prevention and con-

*2.3. Stakeholder Engagement*

trol, and stewardship and surveillance.

At the beginning of the project, a project plan and milestones were agreed upon as well as a specification document which included deliverables pertinent to the project. These deliverables formed the sign-off and approval for the completion of the project.

Focus Games used agile project management processes and tools (Jira). All code development was managed in Bitbucket (GIT repository), ensuring a strong development, test, and live approach. All staff are suitably qualified in their respective disciplines.

The development process for the AMS game included four key phases previously developed by Focus Games Ltd. (Figure 1).

Phase 1—Define Objectives: Requirements for the game outcomes were derived from interviews with and feedback from individual stakeholders, ranging from national to frontline health professionals including pharmacists, doctors, and nurses from eight African countries and the UK. They acted as subject matter experts as well as representatives for the target audience of the game through the development and user testing phases, which included syntax and grammar that was considered acceptable across multiple countries. This identified the learning objectives for the narrative structure of the factual content and how the game design and mechanism will facilitate engagement and learning.

Phase 2—Develop Storyboards: Specific learning objectives and game dynamics were identified based on best practice derived from experience of previous games developed by Focus Games Ltd. This involved the creation of graphic design mock-ups of the game and a written storyboard outline of the factual content. These were discussed and agreed upon by the project team, which included subject matter experts as well as stakeholders across nine countries (Ghana, Kenya, Malawi, Nigeria, Sierra Leone, Tanzania, Uganda, United Kingdom, and Zambia) that were all part of the countries of focus for the CwPAMS programme.

Phase 3—Prototype and Testing: A rapid prototyping approach was used, incorporating data from the pilot scenario and interviews with subject matter experts (SMEs). The game mechanism and design were finalised. The written content was drafted and loaded into the game mechanism. The game was subsequently tested in workshops with SMEs whose feedback informed design iterations.

Phase 4—Refine, Rework, and Launch: production of the final design and implementation of the distribution and commercialisation strategy.

The model and process used are based on practical experience of developing 100 educational games that are being actively used by healthcare professionals around the world. Focus Games have previously evaluated third-party frameworks and models and have found many of them impractical for the purpose of developing game-based learning for the healthcare setting.

#### *2.2. Target Audience for the AMS Game*

The AMS game is intended to support education on antimicrobial stewardship among current and future healthcare team members, including doctors, nurses, pharmacy teams, laboratory staff, and students.

#### *2.3. Stakeholder Engagement*

The game was co-created between partners in the UK and eight African countries that were part of the CwPAMS programme to ensure that the game is relevant, effective, and was designed to be used in either a high-income or low- to middle-income setting. The four broad areas addressed in the game are introduction to antimicrobial resistance and stewardship, appropriate use of antimicrobial agents, infection prevention and control, and stewardship and surveillance.

Partners and their network of health professionals were asked to share insights on the game. Twenty-seven stakeholders ranging from national to frontline health professionals, including pharmacists, doctors, and nurses across nine countries (Ghana, Kenya, Malawi, Nigeria, Sierra Leone, Tanzania, Uganda, United Kingdom, and Zambia), were consulted on the type of the game—snakes and ladders, the question cards for the AMS game, and

case studies to include in the AMS game. Stakeholders were asked to share broad comments about content and accuracy of the answers to the questions in the game within their context and also asked to suggest any additional questions. To guide the feedback process, a structured feedback form (available as Supplementary File S1) was developed in Microsoft Word and shared with the stakeholders via email. The feedback form covered the following sections: demographics of the respondent (name, title, country, profession, job title, and email address), relevancy of the questions to the country, responsiveness of the questions to the key aspects of AMS, and also provided space for them to suggest other potential topics for inclusion in the game. game, and case studies to include in the AMS game. Stakeholders were asked to share broad comments about content and accuracy of the answers to the questions in the game within their context and also asked to suggest any additional questions. To guide the feedback process, a structured feedback form (available as Supplementary File S1) was developed in Microsoft Word and shared with the stakeholders via email. The feedback form covered the following sections: demographics of the respondent (name, title, country, profession, job title, and email address), relevancy of the questions to the country, responsiveness of the questions to the key aspects of AMS, and also provided space for them to suggest other potential topics for inclusion in the game.

Partners and their network of health professionals were asked to share insights on the game. Twenty-seven stakeholders ranging from national to frontline health professionals, including pharmacists, doctors, and nurses across nine countries (Ghana, Kenya, Malawi, Nigeria, Sierra Leone, Tanzania, Uganda, United Kingdom, and Zambia), were consulted on the type of the game—snakes and ladders, the question cards for the AMS

*Antibiotics* **2022**, *10*, x 5 of 14

Demonstration of the board and online games (Figure 2) are available via https:// commonwealthpharmacy.org/press-release-launch-of-the-antimicrobial-stewardship-amsgame/ accessed on 27 April 2022. Demonstration of the board and online games (Figure 2) are available via https://commonwealthpharmacy.org/press-release-launch-of-the-antimicrobial-stewardship-ams-game/ accessed on 27 April 2022.

#### **Figure 2.** Board and online AMS games [17]. **Figure 2.** Board and online AMS games [17].

A guide was developed for the facilitators to provide direction on how to host the game (available in Supplementary File S2). Sample questions and answers are available in Supplementary File S3. A prize was planned for the participants of the game. The participants who completed the evaluation form of the game were entered into a draw to win access to the online AMS game for a period of one year A guide was developed for the facilitators to provide direction on how to host the game (available in Supplementary File S2). Sample questions and answers are available in Supplementary File S3. A prize was planned for the participants of the game. The participants who completed the evaluation form of the game were entered into a draw to win access to the online AMS game for a period of one year

#### *2.4. Recruitment of Participants and Playing the Game 2.4. Recruitment of Participants and Playing the Game*

The AMS game was first launched and played in August 2021, and then played again during the World Antimicrobial Awareness Week in November 2021 as part of a global tournament (Supplementary File S4). On both occasions, the game was promoted globally through online channels including email, websites, and social media to encourage people across the globe to register as players or facilitators. The facilitators had a technical background in antimicrobial resistance and stewardship and the project team provided a short The AMS game was first launched and played in August 2021, and then played again during the World Antimicrobial Awareness Week in November 2021 as part of a global tournament (Supplementary File S4). On both occasions, the game was promoted globally through online channels including email, websites, and social media to encourage people across the globe to register as players or facilitators. The facilitators had a technical background in antimicrobial resistance and stewardship and the project team provided a short briefing session on how to steer the session between the playing teams.

briefing session on how to steer the session between the playing teams. The game was hosted on Zoom, where participants received a Zoom link upon registration and used it to join the game session. Players were allocated to different breakout rooms with facilitators. In each breakout room, players were divided into two teams. The game was hosted on Zoom, where participants received a Zoom link upon registration and used it to join the game session. Players were allocated to different breakout rooms with facilitators. In each breakout room, players were divided into two teams. Teams took turns to answer and discuss a series of questions and case studies about AMR and AMS that were being shown after the facilitators rolled the dice. The game lasted for 45 min. The facilitators were responsible for organizing players into teams, and moderating the game by displaying questions, encouraging players to discuss the questions and agree on the response, and displaying the correct answer after the players' responses. The facilitator guide is available as Supplementary File S2.

#### *2.5. Feedback from Players of the Game*

We collected feedback from individuals who played the AMS game on 24 November 2021. The feedback was collected using an online questionnaire with quantitative and open/free response text-based options hosted on Survey Monkey. This was a short questionnaire with 13 questions that: collected the players' demographic information, examined their experience in antimicrobial stewardship, assessed their knowledge gain and confidence in antimicrobial stewardship after playing the game, and assessed their perceptions on the game in terms of enjoyment and whether they would share lessons from the game and also recommend it to others.

#### *2.6. Data Management*

Data were collected anonymously, although survey respondents could voluntarily provide their name and email address should they wish to be contacted afterwards, e.g., for information about game prize winners and future relevant AMR events. All data were anonymised prior to data analysis. The data were held securely by the project team and in line with the General Data Protection Regulation 2016/679 [18].

#### *2.7. Data Analysis*

Descriptive statistics on the frequency distributions and percentages were used to analyse the responses. Data were analysed using Stata 14.

#### **3. Results**

#### *3.1. Developing the Game: Feedback on Relevance*

#### 3.1.1. Demographics of Respondents

Twenty-six stakeholders ranging from national to frontline health professionals, including pharmacists [18], doctors [4], nurses [3], and an epidemiologist [1], across nine countries (Kenya 3, Malawi 3, Nigeria 3, Sierra Leone 3, Tanzania 2, United Kingdom 4, Uganda 3, and Zambia 6), provided responses on the relevance of the game (Table 1).

**Table 1.** Respondents' feedback on relevance of questions.


#### 3.1.2. Feedback on Relevance of Questions of the Game

When asked whether the questions were broadly relevant to their countries, all 25 respondents who answered this question said "yes". However, 40% of the 25 respondents mentioned that some questions were not at all relevant or were inaccurate to their countries (Table 1). To this end, respondents shared some of the following suggestions, including questions that could be added to the game:

"*What is antibiotic resistance? The response needs to be modified to include inappropriate antibiotic use as a driver of antibiotic resistance not optimal use of the same. The response should also include that antibiotics are not effective against parasites*."

"*Perhaps consider adding some more questions on the role of IPC and the MTC in AMS*."

"*I would suggest to add the following topics on hospital-associated infections. Diagnostics on how to identify the presence of a microbe in a patient specimen*."

On the other hand, the questions and case studies were found to address the key aspects of AMS, as indicated by all 24 respondents that answered the question.

#### *3.2. Players' Feedback on the AMS Game*

#### 3.2.1. Demographics of Respondents

In total, 328 individuals from 23 countries registered to join the online game sessions at the launch of the game in August 2021, and during World Antimicrobial Awareness Week in November 2021. More than 120 attended the two live sessions and 74 participants responded to the AMS game evaluation form. The respondents represented 13 countries across 4 regions: Africa [7], Europe [2], South-East Asia [2], and the Western Pacific region [1] (Table 2). More than half (62.2%) of the respondents were pharmacists. The majority of respondents had experience in AMS, with 20.3% recorded as AMS specialists. However, 10.8% of the respondents were new to AMS.



**Table 2.** *Cont*.


#### 3.2.2. Player Enjoyment of the AMS Game

When asked whether they enjoyed playing the AMS game, almost all (91.9%) of the respondents agreed that they enjoyed it (Table 3). The reasons for enjoyment were mainly attributed to: the simplicity of the design of the game, making it easy to play, and the game was viewed as a novel, unique, interactive, and fun approach for empowering participants to tackle AMR. Comments included:

"*The game was highly entertaining and enriching. You get to learn more of the AMS or rather, fine-tune your knowledge via the game. Will really love to partake again. Kindly keep me posted. Thanks*."

"*The game was very interesting, straight forward and all-round included the One Health aspect which I am really interested in that I think is the way to go if mitigation of antimicrobial resistance is to be achieved*."

"*The game is a good way of bringing the awareness to health workers. It should be rolled out across and include students in medicine, nursing, pharmacy, and laboratory*."

"*What I loved most was that the answers provided by the game were simple, understandable and straightforward to the point and also there was more valuable information attached to the answer thus giving more understanding and meaning*."


**Table 3.** Enjoyment playing the AMS game.

On the other hand, time was a common reason stated as a limitation to enjoyment of the game. The reason for this was attributed towards the short time allocated for the demonstration and not the game itself, whereby players would usually enjoy the game at their own pace. In this perspective, respondents felt that if given more time, the game would be a valuable tool for learning.

"*The demonstration was a bit rushed so difficult to get a real feel for the game. I can see it could be a useful tool to facilitate discussion around AMS with more junior/inexperienced staff. The game needs to be seen in this light because I feel if the focus becomes on playing the game, answering questions as quickly as possible, etc., then it's true value will be lost*."

"*A good fun, learned few things for a very short time*."

"*Cross talking among participants making it difficult to respond* . . . *time constraints* . . . *facilitators should not talk much*."

#### 3.2.3. Knowledge Gain after Playing the Game

The majority (75.7%) of respondents agreed that they got to know more about AMS after playing the game (Table 4). In this regard, respondents from the African Region agreed more than respondents from the European Region by a difference of 12.1% (Table 5). Qualitatively, respondents mentioned to mainly have gained knowledge on the relevance of One Health in AMS and others perceived the game as an opportunity to refresh the principles and strengthen their knowledge on AMS.


**Table 4.** Knowledge and confidence gain after playing the game.

**Table 5.** Knowledge gain according to geographic region.


"*I understood that not only human health must be emphasised so as to end antimicrobial resistance but also animal and environmental health. Interacting with more informed players was more informing*."

"*The game was a quick mind check for the principles on AMR*."

Further, when asked to highlight the most important things they learned from the game, respondents commonly stated aspects related to improved understanding of One Health and handwashing as key aspects in AMS. Additionally, respondents acknowledged the gain of understanding of key AMS terminologies, such as "biosecurity" and "watchful waiting". Overall, there were expressions of increase in knowledge on the causes and preventive measures of AMR. It was also realised that there is a need to create more awareness on AMR and AMS and it was commonly stated that games can be a fun and interactive approach for empowering health professionals and other team members to improve AMS.

"*Actually, it's funny to say but today I learnt that there is a difference between antibiotics and antimicrobials. At first, I thought there was no difference. And I have also learnt about antimicrobial and antibiotic resistance*."

"*I learned that simple practices such as handwashing play a big role in fighting AMR*."

"*Learning is fun when made simple in such innovative ways. I also think it can stick to the brain and allows easy replication in actual practice settings*."

Relatedly, more than three quarters (79.5%) of respondents expressed having more confidence about AMS after playing the game. Respondents associated gaining confidence with acquiring knowledge from the game, thus making them better positioned to create awareness on AMS, as explained by the participants' comments below:

"*I can now educate my colleagues, the nation and the entire world about the goodness of antimicrobial stewardship*."

"*I think the game is great, since am just an undergraduate student but I have been able to reason out different things with people already in the profession. This has boosted my confidence*."

3.2.4. Sharing Lessons Gained from Playing the Game

The majority (93.3%) (Table 6) of participants responded in agreement about sharing lessons from the game with colleagues. Some voiced reasons as to why they would share lessons and others mentioned platforms they would use for sharing, such as those highlighted below:


**Table 6.** Sharing lessons gained after playing the game.

"*I have to share what I have learnt with others so as to facilitate continuation of learning and flow of information*."

"*I will share during our grants meetings and AMS meeting*."

"*I will promote for use in WAAW (World Antimicrobial Awareness Week)*."

"*It was such an engaging experience and will be helpful for bonding in our hospital teams*."

Concerning sharing lessons from the game with patients, more than half (72.6%) (Table 6) of the respondents expressed willingness to do so for some of the following reasons: "*Completing one's dosage as prescribed by a trained health personnel helps minimise antimicrobial resistance*."

"*The patients can use the game to learn more about AMS*."

Further, almost all (97.3%) of the respondents mentioned that they would recommend the game to their colleagues (Table 6).

#### **4. Discussion**

This paper has documented the process of developing the AMS game, and reflections by players. Overall, the healthcare teams who played the game found it enjoyable and reported that it can impart knowledge and confidence in AMS and facilitate shared learning with colleagues and patients.

#### *4.1. AMS Game Development*

The AMS game was developed to attract a multidisciplinary team of players to discuss AMS and learn what they can do personally, and collectively, to improve stewardship in their organisation and community. A multi-country and multidisciplinary approach was used in the development of the game. This supported incorporation of the contextual educational needs of both high- and low- to middle-income countries as shared by diverse health professionals, including pharmacists, nurses, and doctors from Africa and Europe. With this, we addressed the gap reported in a scoping review on serious health education games targeting healthcare providers, patients, and public health users, where it was reported that LMICs have rarely been considered in the development of games [18]. Consequently, the AMS game described in this manuscript attracted diverse participants, players, and facilitators across 23 countries. Further, it is recommended that for effectiveness, games should be designed according to the requirements of specific groups of people [19]. The AMS game was designed for teams of healthcare staff at all levels. To cater for the needs of diverse staff members, the game was designed with different levels of complexity so the organiser can select questions to match the learning requirements of each group.

#### *4.2. Players' Feedback on the Game*

The results showed that the game was enjoyable, as indicated by almost all (91.9%) participants who shared feedback. As in other studies, the enjoyment of the game was attributed to its simplicity in design, making it easy to understand and play [13,19]. The AMS game was also found to be interactive and thus a component that participants enjoyed. The component of playing the game in teams encouraged discussion and learning among players, which also made it more engaging. A systematic review that explored user engagement features in digital games documented more engaging features that can be considered in digital games: the game should have an attractive storyline, be adaptable to gender and age, high-end realistic graphics, well-defined instructions, in combination with clear feedback and a balance of educational and fun content [20]. Whilst the AMS game described in this manuscript covered all these features in its design and appearance, the gender and age components were not considered and neither did the evaluation of the game cater for these variables. It would be important to explore such in future.

It was evidenced that the game can translate knowledge and create awareness on AMS among the players. Higher knowledge gain was recorded among participants from the African countries compared to those from the European countries by a difference of 12.1%. This could imply that the game is more beneficial to the African countries where there are lower levels of awareness on AMR and AMS, as indicated in several studies [12–23]. It was clear from the study findings that the role of One Health in AMS was one of the most common key lessons gained by players, and this is likely because many of the respondents focused on human health in healthcare settings and likely had less exposure to One Health principles. To this end, the AMS game was relevant in accelerating knowledge on the One Health approach, which is recommended by the WHO as a strategy for health workers to responsibly use antimicrobials [24].

The feedback on the game did not only further expose the inadequacy in knowledge on key terminologies in AMS among health professionals, but instantly created awareness and knowledge on terms such as 'antimicrobial stewardship', 'biosecurity', and 'watchful waiting'. Therefore, the AMS game could be a solution to challenges discovered in studies such as that of Higuita-Gutiérrez et al. [25], where 81.8% of 532 medical students had never heard of the term 'antimicrobial stewardship'. Generally, this AMS game may have the potential to increase awareness among health students and professionals across the globe. It can be considered as part of a wider AMR education programme within universities and health institutions. The online version provides an opportunity for use across multiple institutions.

Following the AMS game tournaments, a substantial portion (75.9%) of players who provided feedback indicated that they gained confidence in AMS and thus would participate in creation of awareness on AMS thereafter. This was further demonstrated when over 90% of the study respondents indicated that they would share lessons from the game with colleagues and patients.

#### *4.3. Strengths and Limitations*

Our AMS game was developed with consideration of perspectives from a multidisciplinary team of professionals across the UK and African countries. Hence, this game does not only promote One Health in antimicrobial stewardship but is also among the few games that cater for the antimicrobial stewardship awareness needs of both highand low- to middle-income countries. Whilst the study results indicated that our AMS game is very likely to improve awareness and understanding of AMS, as a limitation, it should be noted that this was a small study designed to collect initial feedback on the new board and online AMS game. Further, only subjective measurements were used to collect feedback on the educational potential of this AMS game, and the small number of players (respondents) makes statistical analysis infeasible. As such, the results of the current study need to be strengthened by studies employing stronger methodologies. We recommend that future studies consider a randomized controlled trial utilizing objective measurement to evaluate the AMS game among a higher number of respondents sampled from a group of individuals who played the game. It would be important that future studies consider: a greater representation of other types of health professionals as the current study had much higher representation ofpharmacists, evaluate the impact of the players' discussions in the breakout rooms (which was not evaluated in this study), and study the effectiveness of the AMS game in comparison to other AMS education interventions.

Despite these limitations, this study generated more evidence and demonstrated that a board and online AMS game is likely to improve knowledge of antimicrobial stewardship. The AMS board game continues to be promoted, made accessible, and used as an education tool among health professionals [26].

#### **5. Conclusions**

We provide a documentation of the process of developing a board and online game on antimicrobial resistance and stewardship; and its potential to educate diverse health care teams in high or low-to-middle- income countries. The game was co-created with a diverse group of stakeholders including national and frontline health professionals from high- and low-income countries. The feedback from the initial players (health professionals) of the game highlighted that the game is enjoyable. Also, that it provides an innovative and engaging opportunity for the players to discuss topics in AMR and AMS; whilst improving and strengthening their knowledge of key topics. Further studies will be useful in evaluating the impact of the AMS game as an educational tool for antimicrobial resistance and stewardship.

**Supplementary Materials:** The following supporting information can be downloaded at: https: //www.mdpi.com/article/10.3390/antibiotics11050611/s1. Supplementary File S1: Questions and comments review: Antimicrobial Stewardship Game. Supplementary File S2: A facilitator's guide was developed to guide the facilitator's on how to run the game. Supplementary File S3: Sample questions and answers from the game cards. Supplementary File S4: Poster for the global tournament.

**Author Contributions:** Conceptualisation, D.A.-O., and W.T.; data curation, D.A.-O., M.N., A.Y., D.D., S.Y., M.B. and R.S.-J.; formal analysis, D.A.-O. and M.N.; funding acquisition, D.A.-O., V.R. and R.S.-J.; methodology, D.A.-O., M.N. and F.G.; project administration, D.A.-O., M.N., D.D., M.B., N.D. and S.Y.; supervision, D.A.-O.; validation, D.A.-O.; writing—original draft, D.A.-O. and M.N.; writing—review and editing, D.A.-O., M.N., A.Y., M.B., S.C., F.G., R.S.-J. and V.C. All authors have read and agreed to the published version of the manuscript.

**Funding:** This project and partnership were part of the Commonwealth Partnerships for Antimicrobial Stewardship (CwPAMS) managed by the Tropical Health and Education Trust (THET) and Commonwealth Pharmacists Association (CPA). CwPAMS is a global health partnership programme funded by the Department of Health and Social Care (DHSC) using UK aid funding, managed by the Fleming Fund. The Fleming Fund is a £265 million UK aid investment to tackle AMR by supporting low- and middle-income countries to generate, use, and share data on AMR and is managed by the UK Department of Health and Social Care. The views expressed in this publication are those of the author(s) and not necessarily those of the Department of Health and Social Care, the UK National Health Service, the Tropical Health and Education Trust, or The Commonwealth Pharmacists Association.

**Institutional Review Board Statement:** Ethical approval was not required as per NHS Health Research Authority guidance and the NHS health research decision tool because this was a service evaluation of CPA's programme of activities to develop and implement the AMS game as part of the CwPAMS programme [27]. All respondents participated strictly in their professional capacity, no identifiable data were collected, and their participation in the survey was in all cases on the basis of informed consent.

**Informed Consent Statement:** Informed consent was obtained from all participants involved in the study.

**Data Availability Statement:** Data are contained within the article or Supplementary Material.

**Acknowledgments:** The authors acknowledge: The Commonwealth Partnerships for Antimicrobial Stewardship (CwPAMS) led by the Commonwealth Pharmacists Association and the Tropical Health and Education Trust (THET) who collaborated with the Focus Games Ltd. to co-develop the AMS Game. Stakeholders and partners from Nigeria: Mashood Lawal, Oluchi Maryann Ezeajughi, Grace Olatunde Olakunri, Jelili AdewaleKilani. Tanzania: Eva Muro and Rajabu Hamidu. Zambia: Derick Munkombwe, Andrew Bambala, Aubrey Kalungia, Brian Muyunda, Webrod Mufwambi, and Chabota Simweemba.Uganda: Winnie Nambatya, Komata Ronald, Vivian Twemanye, Florence Nakakembo, and Oscar Obiga. Kenya: Eric Muringu, Immaculate Kerubo, and Leon Ogoti. Ghana: Mohammed Kudus Moro, Emmanuel Amankrah, Dinah Aryeh-Do, and Afua Akuffo. Sierra Leone: Shuwary Barlatt. Jennet Buck, and Brima Lahai. UK: Abigail Scott, Amber Cavanagh, Amy Hai Yan Chan, Eleanor Bull, Esmita Charani, Elizabeth Beech, Hayley Wickens, Jacqui Sneddon, Lesley Cooper, Manjula Halai, Raymond Anderson, Tatiana Hardy.

**Conflicts of Interest:** The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

#### **References**

