In this systematic review, data from all the included studies were analysed from over 64,000 patients prescribed antibiotics PP and DP between January 2000 and March 2021 in acute care settings. It aimed to investigate the AMS strategies and measures PP and DP [34]. Potential overuse and irrational antimicrobial prescribing have become a complex conundrum for healthcare [35]. This can impact patient safety, progressive AMR, and an incremental economic burden on the healthcare system [12]. The leading cause of respiratory tract infections, mainly upper respiratory tract infections (URTI), are viruses [36]. According to the WHO’s statement, 71% of URTIs are usually treated with antimicrobials [37]. Interestingly, findings from Chung et al. (2013) study reported a lack of strong scientific evidence for most antimicrobial stewardship interventions, which has led to confusion and disagreement about their effectiveness. Both experts and professional bodies continue to reiterate the need for more effective AMS research [1].
Although COVID-19 is a viral disease, prescribing antimicrobials has become a more common practice since the onset of the pandemic [38]. This high antimicrobial consumption in COVID-19 patients was initiated after early reports from China revealed that 50% of patients died from secondary bacterial infection [39]. There was a variation in the AMS implementation strategies and measures among different studies, which can be attributed to several factors. For instance, the core AMS implementation strategies, such as prospective audit & feedback, formulary restriction and multidisciplinary team, were the most common strategies used by PP and DP, as they have been implemented in 70% of the studies PP. Then they decreased to 23% DP [19, 29] (Table 5).
Meanwhile, the AMS supplemental strategies, such as clinical decision support, clinical practice guidelines and education, were the most used, as they were applied in 33% of the included studies PP. Then they decreased to 17% DP [16, 18]. This means that the AMS strategies that require organisational collaboration or hospital-wide implementation were more effective than the AMS strategies on the individual level during a crisis or emergency, such as the COVID-19 pandemic.
Significantly, AMS education using active learning activities was a helpful AMS core strategy PP. For example, in Weston et al. study (2012), it was reported that the use of the AMS educational program entitled ‘Building Stewardship: A Team Approach Enhancing Antibiotic Stewardship in Acute Care Hospitals’ offered by the Agency for Healthcare Research and Quality (AHRQ) safety program was highly effective, as it focused on the importance of Antimicrobial Stewardship Programs (ASPs), strategies for implementation, and operational issues, including an understanding of pharmacodynamics, business models, and electronic surveillance [40]. Notably, the national study that mandated the presence of ASPs in the state of California has revealed successful outcomes in this arena [21]. Additionally, the educational program in Massachusetts also had a significant effect on the implementation of ASPs and the improvement of existing programs [40]. During the COVID-19 pandemic, there was a critical need for structured ASP education to deal effectively with this crisis as AMS education decreased by 50% DP [26, 28, 41].
Using clinical practice guidelines, DP was essential to decreasing AMR [41, 28, 25]. In addition, adherence to the local, national, and international guideline recommendations is vital to prevent over- and inappropriate prescribing of antimicrobials. For example, the study of Ashiru-Oredope (2021) suggested the importance of the updated antimicrobial guidelines National Institute for Health and Care Excellence (NICE), as well as international guidelines from the World Health Organization (WHO) and International Pharmaceutical Federation (FIP), were highly effective DP [28]. The local or organisational clinical practice guidelines should be adapted based on the local antibiograms and resistogram in order to maintain the relevance of the antimicrobial guidelines, as recommended by Surat et al. (2021) study, which will decrease the inappropriate use of antibiotics and decrease the AMR [25]. Additionally, the management of clinical pathways, such as pneumonia and respiratory tract infections in COVID-19 patients, should be updated [28].
During the pandemic, the use of technology in the clinical decision support system was very interesting, as it provided an innovative and simple way for the AMS implementation. For example, it enhanced electronic access to antimicrobial prescribing guidelines. Additionally, its use in the novel metrics, such as the PCT in an electronic ‘COVID order set’, facilitated AMS measures and surveillance [29]. The use of integrated computerised systems was still effective in reducing AMR. Interestingly, the use of new technology ideas such as mobile applications in updating the antimicrobial guidelines was effective, such as the Commonwealth Partnerships for Antimicrobial Stewardship (CwPAMS) App [28], antibiotic order forms, prescribing and availability of guidelines on smartphones [29, 25]. The use of technology was effectively considered in the AMS measures, such as KPIs, and the use of novel PCT lab tests significantly improved antibiotic prescribing and enhanced the proper communication of hospital-wide DP [29].
As mentioned in the result section, it must be measured by identifying the measures that can be used to evaluate the outcome of AMS implementation to improve antibiotic use and AMS intervention. These measures or metrics can be used for many purposes, such as quality assurance, improvement, comparisons, and benchmarking. Before 2019, there were no reliable means for measuring antimicrobial usage. The WHO promoted measurable tools, such as the defined daily dose (DDD) and Day of Therapy (DOT), to allow comparisons for antimicrobial usage among hospitals and countries [37, 42]. In the included studies, the DDD and DOT are the most common AMS measures, as it was used in 53% of PP and 28% of DP. Significantly, Ashiru-Oredope et al. (2021) study promoted the use of KPIs, such as the AMR local indicators - produced by the UKHSA among the National Health Service (NHS) hospitals in England, and it showed a significant outcome in AMS and provided a comparative measure for the antibiotic prescribing among different periods DP [28, 43].
During the pandemic, some measures were of limited use, such as re-admission, antimicrobial utilisation, surveillance reports, and parenteral-to-oral switch. Hence, it is difficult to determine which of these measures are effective, and further investigation is required. Additionally, some measures only used PP, such as the LOS and cost [31, 21]; however, there is insufficient information in the literature regarding their use in pandemics DP (Table 5).
This review has also identified how HCPs were involved in leading AMS in acute care settings, where their work had potentially influenced the AMS implementation in acute care settings. Both microbiology and infection control practitioners represented around 70% of leading AMS, either PP or DP. The infection control champion practitioner has a vital role in Point Prevalence Surveys (PPS), implementation of the infection prevention and control (IPC) bundles, and preventive measures, such as hand hygiene and other personal protective equipment (PPE) measures [28]. On the other hand, the microbiology roles in an antibiotic review (48–72 Hours), antibiogram, antimicrobial resistance reports (resistogram), novel lab test measures such as PCT, and multidrug resistance incidence were highly effective DP [25]. Although pharmacists are antibiotic experts, they were underutilised in leading AMS, as the pharmacist AMS champion was represented in only 22% PP and 17%. Pharmacists have a thorough knowledge of medications, and their emerging role in medication safety is crucial in AMS implementation. In Weston et al. (2012) study, pharmacists led AMS implementation; the hospitals reported a positive outcome after initiation of ASP education; pharmacists were able to perform the “low-hanging fruit" outcomes to facilitate ASP intervention. In addition, they were dedicated to applying AMS supplemented strategies, such as antimicrobial review and antibiotic restriction [40]. Pharmacists also have an essential role in the interdisciplinary rounds (IDR) [44], which enable them to review patients prescribed antibiotics using the electronic medical record, in addition to monitoring the antibiotics used, culture results, and therapy duration. The involvement of pharmacists in the multidisciplinary meetings and leading AMS was so helpful [45]. Pharmacists working in collaboration with other health care professionals have an essential role in the global mandate of AMS implementation.
Limitations of the Systematic Review
Searching only published databases could have resulted in missing some potentially relevant but unpublished studies from the review. Secondly, limiting studies to being published in the English language could have resulted in missing essential studies published in other languages.
Limitations of the Evidence
To the knowledge of the authors, this is the first systematic review to assess the AMS implementation of PP and DP. However, there are insufficient studies using the AMS strategies and measures. Authors did their best to compare the AMS strategies and measures, but variation in their use affected the comparability of findings across studies.
Comparison with Existing Literature
A few reviews have assessed the AMS in hospitalised patients. However, none of the reviewers has focused on the core and supplemental AMS strategies, nor the AMS measures in Secondary care and acute care settings PP and DP as explored in this present systematic review.
Implications for Research and Practice
Few studies identified the AMS measures, the use of AMS indicators and quality improvement projects which are relevant to this systematic review. Therefore, further studies are required to provide measurable indicators for assessing AMS implementation. It will also enable the planning and evaluation of suitable AMS interventions. Secondly, further research is required to develop methods for standardised measurements for AMS implementation that will allow greater comparability of AMS outcomes and measures across studies. Lastly, there was evidence that antibiotic use is best achieved with organisational collaboration, especially during an emergency or pandemic. All HCPs have an effective role to play in this.
Summary and recommendations
This systematic literature review showed promising outcomes in selecting the appropriate AMS intervention strategies. However, the ongoing global crisis of AMR must not be neglected. The present systematic review included studies showing the AMS strategies and measures used PP and DP in acute care settings. There are so many lessons learnt from the COVID-19 pandemic. Each hospital should use relevant AMS strategies and measures during a crisis or emergency. This will ensure effective AMS implementation and decrease the AMR threat. Urgent actions are required to provide better preparedness for future pandemics. Advocacy for AMS must continue in the post-pandemic era to assure the safety of patient care. Results from studies in AMS implementation need to be robust to provide a basis for clinical decision-making and policymakers. Therefore guidance development is needed for AMS implementation, as summarised in the following recommendations:
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Reliability of the AMS implementation strategies can be country-specific, such as the UKHSA national indicators. Appropriate tools must be used in each country to achieve reliable outcomes.
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Presently, though DDD and DOT are the most common AMS measures, other measures are used PP and DP. There is thus a need to standardise systems as this will allow better comparison of outcomes and planning of effective AMS interventions.
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Appropriate use of antibiotics and use of the proper AMS strategy result in the reduction of AMR and achieve the action plan goal, such as the UK government released a 5 Year AMR Strategy 2013–2018 in 2013 and a five-year National Action Plan 2014–2019 in 2019, with ambitions to reduce UK antimicrobial use in humans by 15% by 2024.
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Collaboration among health care professionals in planning and implementing the AMS interventions is required for optimal results of decreasing AMR.
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Novel AMS measures, such as PCT and the proper use of technology, provide a promising effect on AMS.
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Collaborative AMS implementation, such as multidisciplinary team, AMS education, and country-level KPIs, showed promising outcomes rather than individual AMS strategies, such as antibiotic review and de-escalation, especially during an emergency or pandemic.
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During a crisis, or emergency, such as the COVID-19 pandemic, antibiotics appeared to be over-used in hospitalised people. There should be an action plan for AMS to be prepared for any further or future emergencies.