Volume 33 Number 3

Introduction

The emergence of microorganisms with antimicrobial resistance (AMR) threatens clinicians’ and other heathcare professionals’ ability to treat common and more serious infections,¹ and it is a growing global health threat that is characterised by the ability of microorganisms to withstand the effects of antimicrobial agents that once killed or inhibited their growth. There are several concerns associated with AMR (Table 1) and, to combat AMR, areas such as the prudent use of existing antimicrobials, new drug development, and infection prevention and control measures require attention.²

 

Table 1. Major concerns associated with antimicrobial resistance

 

The “5Rs” of antimicrobial stewardship (responsibility, reduction, refinement, replacement, review)³ are part of a broader framework of continuous improvement for the use of antimicrobials for both human and animal health, and help guide the appropriate use of antimicrobials.

AMR is of such global concern that the World Health Organization (WHO) has developed a global strategy on AMS which includes a focus on the prevention of infections, ensuring universal access to health services for diagnosis and appropriate treatment.⁴ Part of the WHO’s drive to address AMR is the promotion of antimicrobial stewardship (AMS), a systematic approach to educate and support healthcare professionals to follow evidence-based guidelines for the prescribing and administration of antimicrobial agents.⁵ To improve access to appropriate treatment and reduce inappropriate use of antibiotics, WHO developed the AWaRe (Access, Watch, Reserve) classification of antibiotics which provides concise, evidence-based guidance on the choice of antimicrobials (antibiotics), dose, route of administration, and duration of treatment for more than 30 of the most common clinical infections in both primary health care and hospital settings.⁶ The WHO endeavours to guide countries to develop and implement AMS programmes (AMSPs) as one of the most cost-effective interventions to optimise the use of antimicrobial medicines, improve patient outcomes and reduce AMR and health care-associated infections.⁷

More locally, the Australian Government has recently released a national AMR strategy, Australia’s National Antimicrobial Resistance Strategy – 2020 and Beyond,⁸ which sets out a 20-year vision to protect health by minimising the development and spread of AMR while being able to provide effective antimicrobials for treatment. Furthermore, the development of tools (such as the Antimicrobial Stewardship Self-Assessment Tool⁹ designed to help providers and clinicians review their AMSPs in residential aged care environments), is an example new ways to provide standardised, continual AMSP improvement. A recent UK Government Policy Paper, Confronting Antimicrobial Resistance 2024 to 2029 (Updated 8 May 2024)¹⁰ stated that, as a target, “by 2029, we aim to reduce total antibiotic use in human populations by 5% from the 2019 baseline” (Outcome 4 – Antimicrobial Stewardship and Disposal). Therefore, it is important that interventions are implemented effectively, and that there is also an imperative that there are measures of success in place regarding outcomes. However, there are a number of unique challenges in implementing AMSPs in developing versus developed countries (including those with underdeveloped healthcare systems, poor supply chains, lack of good professional capability, and unstable local political situations).^11,12 There are also differences between introducing programmes in metropolitan versus. rural areas (for example with less onsite AMS specialist expertise, and more staff recruitment and retention challenges).¹³ Together, there are a number of core elements for any outpatient AMSP in order to deliver the optimal care. These include a commitment to optimising antimicrobial prescribing and patient safety, continual improvement in the prescribing of antimicrobials, the ability to monitor prescribing practices, and the provision of educational resources and access to this information to clinicians and patients.¹⁴

AMSPs have a significant impact on the treatment of infections, including wound infections.^15,16 These AMSPs aim to optimise the use of antimicrobial agents to reduce microbial resistance, improve patient outcomes, and decrease unnecessary costs associated with improper antimicrobial use,¹⁶ with nurses playng a key role in implementing AMSPs.^17‑19 Key areas in which AMSPs impact treatment of wound infections include: the improvement of patient outcomes; enhancement of antimicrobial use including through better use optimisation; reducing inappropriate prescribing; cost savings; and improvements in education and awareness (Table 2).¹⁶ The impact of AMSPs may apply more broadly to infections other than wound infections, and may include microorganisms, such as fungal and viral infections.

 

Table 2. Impact of antimicrobial stewardship programs on treatment of infection

 

Dona et al²⁰ and Davey et al²¹ conducted evidence-based reviews assessing the impact of the implementation of AMSPs. In a scoping review of AMSP implementation in paediatrics, Donà et al²⁰ identified that the introduction of AMSPs had a significant impact on reducing targeted and empiric antimicrobial use and associated heathcare costs and AMR in both in-patients and outpatient settings. Davey et al²¹ performed a review of 16 studies on the impact of AMSPs on hospital prescribing of antimicrobials and the prevalence of AMR. Only four studies provided strong evidence that AMSP’s resulted in improvements in prescribing habits and a decrease in antimicrobial resistance. A further finding of the latter review was that several studies were of poor design, limiting firm conclusions. The aim of this scoping review is to determine the impact of the implementation of AMS on the effect of antimicrobial use in surgical and chronic wounds.

Review questions

This scoping literature review was undertaken to determine the impact of antimicrobial stewardship implementation in wound care. The specific review question to be addressed was:

• What is the impact of the implementation of antimicrobial stewardship on clinical outcomes

Methods

A scoping review^22,23 was conducted to map the research to date on the impact of the implementation of antimicrobial stewardship on the treatment of a variety of wound types (acute and chronic). The review was designed to identify what impact the introduction of the AMS strategy had on working practice. The analysis followed the PRISMA Extension for Scoping Reviews (PRISMA-ScR) checklist  published in 2018 by Tricco et al.²⁴

Search strategy

The PICO format was developed to assist with the search strategy:

• P (Patient or population) — infected wounds
• I (Intervention) — implementation of antimicrobial stewardship
• C (Comparison) — not relevant for this review
• O (Outcome) — improvement of clinical outcomes related to infection

The electronic database MEDLINE (PubMed) was searched for relevant articles published between January 1970 and February 2024. We feel that searching only MEDLINE (PubMed), a powerful search tool for medical literature,²⁵ is appropriate for this review. Access to literature databases is often limited and only available on subscription basis.²⁶ Studies have investigated the value of different databases used to search on different topics, and some have concluded only one database can be sufficient^27,28 particularly in cases of reviews that are not systematic reviews²⁹ where multiple databases are advised.^30-32 Studies have noted that the vast majority of relevant studies appear within a limited number of databases.³³ Furthermore, Selective searching may not introduce bias³³ and it is not always necessary to find all relevant references to draw valid conclusions.²⁶ To identify further published papers, this search included a search of the reference lists of all identified papers. Additional relevant articles not identified through MEDLINE were added manually.

The search strategy was as follows: “stewardship AND (wound* OR “surgical site” OR postoperative OR perioperative OR surg*)” and with a search date range from 01-Jan-1970 to 28-Feb-2024. Below expands the search strategy as indicated by PubMed:

((“stewardship”[All Fields] OR “stewardships”[All Fields]) AND (“wound*”[All Fields] OR “surgical site”[All Fields] OR (“postoperative period”[MeSH Terms] OR (“postoperative”[All Fields] AND “period”[All Fields]) OR “postoperative period”[All Fields] OR “postop”[All Fields] OR “postoperative”[All Fields] OR “postoperatively”[All Fields] OR “postoperatives”[All Fields]) OR (“perioperative”[All Fields] OR “perioperatively”[All Fields]) OR “surg*”[All Fields])) AND (1970/1/1:2024/2/28[pdat])

To ensure relevant articles were included in the review, inclusion and exclusion criteria were used (Table 3).

 

Table 3. Inclusion and exclusion criteria

 

Screening

Article titles and abstracts were assessed by two authors (MR and AR) according to the inclusion and exclusion criteria. The full-text versions of potentially relevant studies were obtained and screened against the inclusion criteria. Following screening of the full text articles, consensus between reviewers in relation to the studies to be included was then obtained.

Data extraction

Descriptive data were extracted from the full text versions and added to a pre-designed data extraction table recording author and year, country, setting, design, population, sample and intervention.

Results

Study inclusion

The study selection process is illustrated in the PRISMA flow diagram (Figure 1). The initial search identified 2458 potential articles, and 13 articles were identified from other sources, giving a total of 2471 articles to screen. Following screening of the articles, including a title and abstract review, 120 articles were identified for full-text review. Then 80 articles were retrieved and included in the narrative review.

Of these, 32 (40%) of the articles included in this review were from developing countries (as defined by Australian Government Department of Foreign Affairs and Trade).³⁴

 

Figure 1. PRISMA flow diagram of literature review

 

Characteristics of included studies

An overview of the wound types featured in the reviewed studies indicated that the majority^{20,36-41,43-58,66-98,100-119} (76/80, 95.0%) were in relation to surgical wounds. Three (3.75%) studies^49,61,120 were chronic wound  related, and one (1.25%) study⁹⁹ was burn related.

All studies indicated the introduction of specific AMS guidelines and/or protocols that affected treatment regimens with 32 (32/80, 40.0%) studies ^{20,36,37,41,43,44,47,49,54,56,57,61,67,68,74,81,82,84,86,87,92,94,95,98,100,101,105,108,110,117} specifically indicating training/education, and 35 (35/80, 43.8%) studies^{36,37,40,41,43, 44,47,49,50,53,54, 57,61,66-68,72,76,77,80,83-86,89,92,94,99,100,106,108,110,111,114,117} indicating some form of audit/feedback as part of the AMSPs.

Impact of AMSP implementation on antimicrobial usage was reported in most studies^{20,36-41,43,44,47,49-55,57-59,61,66-86,89, 91-108,110-114,116-120} (71/80, 88.8%) resulting in a de-escalation of antimicrobial use (such as intravenous versus oral, broad- or narrow-spectrum^{20,36,37,39-41,43,49,51-55,57-59,66,67,69,70,72,75,78-86,89,91-102, 104-107,110,112,117-120} (54/80, 67.5%), changes in antimicrobial dosage^{43,44,50,54,68,71,73,75,80,86,89,91,94,95,102,103,105,108,113,114} (20/80, 25.0%), as well as length of antimicrobial use (37/80, 46.3%).^{20,36-38,40,43,44,47,53,57,61,67-69,71,73,79,80,82,83,85,86,89,92,94,95,97-99,102,103,105,106,108,111,114,116} No studies focused specifically on topical antimicrobials. Table 4 summarises the main clinical outcomes assessed with the introduction of AMSPs.

 

Table 4. Summary of main clinical outcomes assessed in the studies

 

One of the criteria during the screening of the evidence was that studies should be before-and-after studies in which clinical treatment was assessed prior to and after AMSP implementation. All studies (n=80) introduced AMS guidelines/protocols as part of their study procedures. The introduction of AMSPs has been supported by additional education and training on AMS, and has been specifically noted in a number of studies as being introduced as part of the implementation of AMS (32/80, 40.0%).^{20,36,37,41,43,44,47, 49,54,56,57,61,67,68,74,81,82,84,86,87,92,94,95,98,100,101,105,108,110,117} Audits and feedback to enable data-driven improvement were noted in 35/80 (43.8%) to support the introduction of AMSPs.^{36,37,40, 41,43,44,47,49,50,53,54,57,61,66-68,72,76,77,80,83-86,89,92,94,99,100,106,108,110,111,114,117}

Discussion

This scoping review examined the evidence regarding the influence of AMS on wound infection management, and wider clinical outcomes. Several clinical studies supported the benefits of AMSP implementation for treatment of wound infections and on clinical outcomes. This review found that surgical wounds were the predominate focus, with other wounds (such as chronic wounds (including diabetic foot ulcers) and burns)) being less frequently studied. This review and discussion focuses on two key aspects: first, the impact of AMSP on antimicrobial usage and, second, their effect on a number of important clinical outcomes.

Impact of AMS implementation on antimicrobial usage

The studies reviewed assessed various aspects of antimicrobial prescribing, including measuring the way in which antimicrobials are prescribed, reducing the number of antimicrobials used, their dosage, and duration of therapy (Table 5).

Antimicrobial use was measured in 71 of the 80 studies.^{20,36-41,43,44,47,49-55,57-59,61,66-86,89,91-108,110-114,116-120} Changes in antimicrobial use included a revision in the route of antimicrobial administration (e.g., from intravenous injection to an oral path of delivery), and selection of a narrow-spectrum antimicrobial from a broad-spectrum example).

Fifty-four (67.5%) studies^{20,36,37,39-41,43,49,51-55,57-59,66,67,69,70, 72,75,78-86,89,91-102,104-107,110,112,117-120} were identified where the implementation of AMSPs led to a modification of antimicrobial usage in terms of changes in choice of administration and de-escalation (Table 5). This review identified 21 (29.6%) studies^{20,36,43,54,66,67,69,78,82-84,86,91,92,96,99,105, 107,117,119,120} where the choice of antimicrobial agent was affected by the introduction of AMSPs (Table 5). For example, a retrospective quasi-experimental before-and-after study (n=2439) evaluated antimicrobial selection and duration in surgical prophylaxis prescriptions over six months before and after a five-year AMSP intervention. Results showed an increase in appropriate antibiotic selection (20% to 80%, p<0.001), a decrease in certain antibtioics (p=0.019), and improved duration compliance (69.1% to 78.0%, p<0.001).³⁶ The AMSP included implementation of a surgical prophylaxis guideline, education sessions, prospective and retrospective audits, and the provision of feedback. Notably, no increases in surgical site infections were observed post-intervention. Similarly, a prospective, interventional cohort before-and-after study (n=32,499 surgical patients, with 5458 prescriptions from 3912 patients analysed) found that AMS interventions (included training, creation of stewardship teams and audit and feedback) led to improvements in antimicrobial treatment duration, a maintenance or reduction of antimicrobial treatment, or change in route of application of antimicrobial.³⁷ As a result, recommendations for discontinuation (35%), maintenance (40%) or de-escalation (15.5%) of antimicrobial usage were issued, with a significant decrease in percentage of prolonged treatments (p<0.001).

 

Table 5. Effect of AMSP implementation on antimicrobial use (n=71)

 

Surat et al³⁸ conducted a retrospective observational before-and-after study of 767 patients (n=495 pre-AMS, and n=272 in the the AMS period) undergoing intra-abdominal surgery to evaluate the impact of AMS measures. These measures included guideline implementation, antimicrobial usage monitoring, and restricted antimicrobial use. Following AMSP implementation, total days of therapy per 100 patient days decreased from 47 to 42.2 days (p=0.035). The proportion of patients receiving postoperative therapy declined from 56.8% to 45.2% (p=0.002), and there was a significant decline in the rate of inappropriate indications (17.4% to 8.1 %, p=0.015). Additionally, the use of broad-spectrum antibiotics for post-operative therapy fell from 28.8% to 6.5% (p≤0.001), with a shift toward narrower-spectrum agents. Importantly, these reductions in antibiotic use did not negatively impact clinical outcomes or post-operative wound complications.

De-escalation

De-escalation was a common outcome following AMSP implementation, with 44 studies reporting improvements. ^{20,37,39-41,49,51-55,57-59,66,70,72,75,78-82,85,89,91-102,104-106,110,112,117,118} For example, Gruber et al³⁹ analysed 574 patients and found that AMSPs improved de-escalation rates of antimicrobial therapy (p=0.081), and a decrease in overall antimicrobial consumption, without negatively affecting patient outcomes, and that overall antimicrobial usage remained stable where AMS measures were no longer provided. A subsequent study (n=301) that included weekly AMS ward rounds based upon an audit and feedback process underlined these earlier results.⁴⁰ In addition, Gruber et al⁴⁰ also showed an increasing trend for antimicrobial treatment guideline concordance (such as choice of appropriate antimicrobial). In a single-centre retrospective before-and-after study (n=331, 182 and 149 patients for the pre-AMSP and AMSP, respectively) in a surgical intensive care unit (ICU), antimicrobial guidelines, prospective audits, and regular feedback meetings led to significant improvements.⁴¹ De-escalation improved (63.2% vs. 94.6%, p<0.001), while the use of anti-pseudomonal beta-lactams decreased (68.7% vs. 57.7%, OR 0.62, 95% CI 0.40–0.98). The study concluded that AMSPs not only reduced antimicrobial usage but also improved patient outcomes, including mortality and readmission rates).

A key goal of AMSPs is to reduce the use of antimicrobials while ensuring appropriate dosing.⁴² As well as affecting the route of administration, targeting the use of specific antimicrobials, and increasing the use of narrow-spectrum antimicrobial agents, antimicrobial usage can be improved through better management of dosage and length of therapy. This review identified 20 (25%) studies^{43,44,50,54,68,71,73,75,80,86,89,91,94,95,102,103,105,108,113,114} that assessed antimicrobial dosage, and 37 (46.3%) studies ^{20,36-38,40,43,44,47,53,57,61,67-69,71,73,79,80,82,83,85,86,89,92,94,95,97-99,102,103,105,106,108,111, 114,116} that evaluated duration of antimicrobial use as part of the AMS outcome assessments. In a single-centre prospective before-and-after study of gastrointestinal surgery patients (n=362), AMSP interventions — including the development of surgical antimicrobial prophylaxis guidelines, educational meetings, and the monthly revision of prescriptions — led to improvements in correct antimicrobial use. These included better prescribing of appropriate doses, timings, choice of route of administration, and duration of prophylaxis.⁴³ Singh et al⁴⁴ evaluated the long-term impact of an AMSP in a mixed medical and surgical ICU. AMSP interventions, such as introduction of a program of guidelines, expert consultation, and audit and feedback processes, significantly altered antimicrobial use over nine years (p<0.011). There was a notable decrease in defined daily dose (p<0.0001) and a reduction in the use of most antimicrobial classes.

Additional (clinical and economic) outcomes

In addition to the antimicrobial use outcomes, several clinical and economic outcomes were identified in this review that were affected by the introduction of AMSPs (Table 7).

Surgical site infections (SSIs)

Of the 80 studies included in this review, 23 monitored changes in SSIs.^{20,36,43,45,46,48,51,54,55,66,72,73,82,85,87,88,90,97,101,109,114-116} Despite significant reductions in antimicrobial use following the implementation of AMSPs, none of these studies reported an increase in SSIs (Table 7). Approximately half (11/23, 47.8%) of SSI-reporting studies found a reduction in infection rates.^{43,45,46,48,54,73,85,87,88,97,101} For example, Brink et al⁴⁵ conducted a prospective observational before-and-after study on 24,206 surgical cases, demonstrating 19.7% decrease in SSI rates after introducing a pharmacist-driven antimicrobial stewardship model for perioperative antimicrobial prophylaxis, which included audit and feedback. The SSI rate dropped from a mean of 2.46 (95% CI 2.18–2.73) pre-intervention to 1.97 post-intervention. Similarly, SSI rates were also reduced with the implementation of an AMSP in a prospective before-and-after study in 327 patients undergoing pancreatoduodenectomy.⁴⁶ Changes in antibiotic prophylaxis policies under an AMSP led to a significant reduction in the overall SSI rate (26.4% vs. 14.8%, p=0.01). The study also found a reduction in the organ/space SSI rate (15.3% versus 8.6%, p=0.03).

 

Table 6. Definitions

 

Table 7. Effect of AMSP implementation on clinical outcomes (n=80)

 

Length of stay

Length of stay in hospital, which has significant cost implications (see below), was examined as an outcome in 20 studies (Table 7).^{46-50,52,53,59,61,69,83,85,88,89,92,103,106,107,110,117} Among these, 11 studies found no impact of AMSPs on length of stay,^{49,50,52,53,59,61,69,103,106,110,117} while nine studies reported a significant reduction.^{46-48,83,85,88,89,92,107} One single-centre retrospective, observational before-and-after study of 8029 patients across a number of hospital departments including medical, surgical and intensive care unit (ICU) departments, found that AMS interventions (such as guidelines, formulary restriction, antimicrobial use assessments, audits, feedback, education, and infection control measures) reduced the average length of stay from 4.18 days to 1.4 days (p=0.004).⁴⁷ Similarly, Sasaki et al⁴⁸ evaluated the impact of AMS protocols as modifications in clinical pathways on SSIs and post-operative hospital stay. Their study showed both a decrease in SSIs, and a significant reduction in length of stay (p<0.001). Only one study (1/20, 5%) reported an increase in the length of hospital stay following the introduction of an AMSP.⁴⁹ This retrospective observational study of 2422 ICU patients, found a significant increase in median hospital length of stay (p=0.04), though ICU stay remained unchanged.

Cost

The introduction of AMSPs and the associated reductions in outcomes such as antimicrobial use, SSI rates, and length of stay have significant cost implications. In this review, 25 studies assessed the financial impact of AMSPs (Table 7).^{43,47-51,53,57,66,68,71,73,76,78-80,85,92,94,104,107,109,114,118,119} Of these, 24 (96.0%) studies reported cost savings,^{43,47-51,53,57,66,68,71,73,76,78-80,85,92,94,104,107,109,114,119} while two (8%) found no overall cost changes.^50,118 One study, Taggart et al,⁵⁰ observed cost reductions in a trauma/neurosurgery ICU but no change in a medical/surgery ICU. In a retrospective study,⁴⁷ AMSP implementation led to a 54.2% reduction in antimicrobial use and an 81.7% decrease in parenteral antimicrobial costs. A cluster-randomised controlled trial evaluating a computerised AMS intervention in 2470 surgical patients,⁵¹ compared antimicrobial costs between intervention and control groups. The intervention group had significantly lower median antimicrobials costs (p<0.01), reinforcing the financial benefits of AMSPs.

Readmission

Of the 80 studies reviewed, 11 assessed readmission rates as an outcome (Table 7).^{41,49,50,52,61,69,79,92,94,105,107} Seven (63.6%) found no significant change after AMSP implementation,^{41,49,50,61,69,94,105} while four (36.4%) reported a decrease.^52,79,92,107 Zaffagnini et al⁵² conducted a retrospective/prospective observational study on 467 paediatric surgical patients and found that AMPS implementation reduced the 30-day readmission rate from 4.9 to 2.8 per 100 admissions (p<0.001). Similarly, an 11-year study of 61,333 medical/surgical ICU patients showed a reduction in ICU readmission rates within 48 hours of discharge after AMSP implementation (418 versus 372, p<0.001).⁷⁹

Antimicrobial resistance

AMSPs have received special support as the prevalence of antimicrobial resistance has increased. Twelve studies assessed antimicrobial-resistant microorganisms as part of a broader impact evaluations.^{41,44,50,52,53,81,87,91,96,97,106,110}

In a retrospective cohort study at a transplant centre, Shafekhani et al⁵³ examined resistance patterns before and after AMSP implementation, focusing on multidrug resistant pathogens such as Acinetobacter baumannii, Escherichia coli, Klebsiella pneumonia, Pseudomonas aeruginosa, Methicillin-resistant Staphylococcus aureus, and vancomycin-resistant enterococci (VRE). As well as improvements in outcomes, such as a reduction in the use of all classes of antibiotic (p=0.04), mean duration of use reduction (p=0.04), and antibiotic cost reduction (p=0.03), this study found a decrease in multidrug resistant isolates. In addition, a single-centre prospective before-and-after study found significant improvements in antibiotic resistance among gram-negative bacilli.⁹¹ Resistance rates to several antimicrobials in Enterobacteriaceae isolates decreased (significant p-values ranged from p=0.018 to p<0.001), as did resistance in non-fermenting gram-negative rods (significant p-values ranged from p=0.026 to p=0.007). In addition, the percentage of isolate resistance to several antimicrobials also decreased for non-fermenting gram-negative rods (significant p-values ranged from p=0.026 to p=0.007). However, resistance levels in gram-positive cocci remained unchanged. No studies reported an increase antimicrobial resistance following AMSP implementation.

Mortality

Mortality was evaluated as a clinical outcome in 20 studies (Table 7).^{41,44,49,50,52-54,59,61,76,79,89,92,94,97,105-107,110,117} No study reported an increase in mortality following AMSP implementation, and 12 (60.0%) found no significant change.

However, some studies reported improved mortality rates. For example, Quirós et al⁵⁴ conducted a prospective, quasi-experimental before-and-after study across 77 medical/surgical ICUs in nine countries (n=10058). They found that AMPS implementation, combined with online training, audit and feedback, significantly reduced all-cause ICU mortality from 17.7% to 15.9% (p<0.0001).

Compliance

Compliance with established guidelines is a key component of effective clinical care. Education and audits, two common aspects of AMSPs, have been shown to enhance compliance. In this review, 28 (35.0%) studies evaluated compliance with documentation as an AMSP outcome (Table 7).^{36,40,45,47,54-56,58,61,66,67,70,73,74,76,80,85,86,92,93,95,98,99,101,104,106,111,112}

For example, a retrospective/prospective comparative study in elective paediatric surgery assessed compliance before and after AMSP implementation.⁵⁵ Following implementation, perioperative antibiotic prophylaxis (PAP) violations significantly decreased (45.5% vs. 4.8%, p<0.001). Tunio et al⁵⁶ highlighted the complexity of compliance in a prospective before-and-after intervention study of 616 surgical ward patients. Their goal was to achieve 90% compliance with evidence-based perioperative antimicrobial prophylaxis guidelines. AMSP implementation and education increased overall compliance from 38.8% to 59.0% (p<0.001). While agent selection compliance remained unchanged (60.7% to 62.8%, p=0.68), dose compliance improved significantly (39.6% to 89.2%p<0.001).

Documentation

Improvements in documentation following AMSP implementation were observed in four (5%) studies (Table 7).^57,58,99,100 A single-centre retrospective, quasi-experimental before-and-after study (n=269) assessed the impact of an AMSP incorporating education, audit, and feedback.⁵⁷ Post-implementation, ICU chart documentation became more detailed, with a significant increase in charts specifying antimicrobial regimen and indication (26% versus 71%, p<0.0001). Additionally, there was an 18% absolute increase in regimens with documented stop dates (53% versus 71%, p<0.0001).

Similarly, a single-centre observational before-and-after study (n=2135) in a surgical setting demonstrated improvements in antimicrobial prescribing documentation after AMSP introduction.⁵⁸ Initially, documentation rates were low pre-AMSP (51.6%, 97/188), but by the study’s conclusion, all prescriptions included documentation (p<0.001). Stop/review dates were documented in only 25.5% (48/188) of prescriptions pre-AMSP, increasing to 100% post-AMSP (p<0.001). Significant improvements were also noted in the documentation of prescribing indications (p<0.001) and stop/review dates for surgical antimicrobial prophylaxis (p<0.001).

Chronic wounds and antimicrobial stewardship

Of the 80 studies reviewed, only three evaluated the impact of AMS on patients with chronic wounds, including diabetic foot ulcers (Table 8).^59,61,120 All three studies were single-centre, prospective or retrospective before-and-after studies, involving on a total of 627 patients. AMS guidelines were introduced, and outcomes related to antimicrobial use, and broader clinical outcomes were assessed. Although the number of outcomes assessed was limited, AMSP implementation resulted in positive outcomes on antimicrobial use.

 

Table 8. Effect of AMSP implementation in clinical outcomes in difficult-to-heal wounds (n=3)

 

For instance, Torvikoski et al⁵⁹ introduced a selective reporting protocol for wound cultures as part of an AMS initiative in a primary care hospital’s wound care ward. This reduced the frequency of antimicrobial escalation from 63% pre-intervention to 37% post-intervention (p<0.001), suggesting that selective reporting is an effective to reduce antimicrobial use. While AMSP implementation showed no significant improvements in length of stay, mortality or readmission rates for patients with chronic wounds, it did improve clinical processes by increasing compliance with treatment guidelines (Table 8).

In another study, a single-centre retrospective analysis of 193 patients with diabetic foot ulcers (DFUs) assessed the impact of AMSP implementation, which included the introduction of new clinical guidelines, education initiatives, audit and feedback.⁶¹ As well as a reduction in number of days of antimicrobial treatment, the study found an increase in adherence to antimicrobial use guidelines from 39% pre-implementation to 68% post-implementation (p<0.001), and a reduction in the duration of antimicrobial use. There was no detrimental effect on other outcomes such as length of stay, readmission, mortality, or amputation rates.

The limited evidence suggests that AMSPs can improve both antimicrobial use and clinical outcomes for chronic wounds, similar to their benefits in surgical wounds. The lack of available evidence for chronic wounds is surprising, and raises the question of why more studies have not been conducted. One possible reason is that while AMS principles are not new, they have only recently gained traction in chronic wound management. The primary focus of chronic wound care has traditionally been on wound healing, and there may be limited awareness among health care providers (HCPs) about how AMS implementation can improve both wound healing and antimicrobial use simultaneously.

To increase AMS adoption in chronic wound management, several strategies can be implemented. These include enhanced and appropriate education and/or training for HCPs on AMS principles, regular audits and feedback to reinforce the benefits of AMSPs, and greater ownership of AMSPs. Furthermore, conducting well-designed before-and-after studies could strengthen the evidence base for AMSP implementation in chronic wound care. If AMS guidelines become standard practice, they could help reduce antimicrobial use while improving wound management outcomes.

The subjective nature of diagnosing chronic wound infections may limit the number of studies on AMSP effectiveness.^62-64 Factors such as the reliance on visual inspection, the subtle signs of infection, and subjective patient reporting make infection diagnosis challenging. That most chronic wounds are treated in the community rather than in hospitals may also contribute to the limited number of studies in this area.⁶⁴

Limitations

A limitation to the methodology is that the literature source for this review was limited to one electronic database, PubMed, a comprehensive free-to-view electronic database of biomedical research; thus, there is the potential to not capture all relevant studies on a topic and can miss research published in other databases which may lead to biased results and incomplete information. However, the authors did hand-search reference lists of included papers, and search relevant journals known not to be included in the PubMed database.

A further limitation with this review is that only three studies were identified related to chronic wounds despite the high infection rates seen in chronic wound management. We recommend that there should be further clinical studies investigating the effect of implementation of AMSPs in chronic wound management.

Conclusions

Antimicrobial resistance is a serious development in wound care as it reduces treatment options for those with wound infections, and is associated with increased risk of severe, extended illness or even death. The introduction of antimicrobial stewardship programs aims to optimise the use of antimicrobial agents to reduce microbial resistance, as well as improve patient outcomes. Evidence on the impact of these programs demonstrates that implementation of antimicrobial stewardship does have several positive clinical patient outcomes, including a reduction in surgical site infections and antimicrobial resistance. But that more research is needed to further understand of the impact of stewardship programs for those with chronic wound infections.

Conflict of interest

The authors declare no conflict of interest.

Ethics statement

An ethics statement is not applicable.

Funding

This study was supported and funded by Essity Group, Sweden.

Author contribution

KO, JB and KW conceived the study design. MGR and AAR developed the review protocol and developed the search strategy and inclusion/exclusion criteria, conducted the review and synthesis of the literature. All authors provided critical revisions and feedback on the manuscript.

Abbreviations

AMR antimicrobial resistance

AMS antimicrobial stewardship

AMSP antimicrobial stewardship programme

DFU diabetic foot ulcer

HCP healthcare providers

ICU intensive care unit

PRISMA
preferred reporting items for systematic reviews and meta-analyses

PRISMA-ScR PRISMA for scoping review

SSI surgical site infection

WHO World Health Organisation

Author(s)

Karen Ousey¹, Mark G Rippon*², Alan A Rogers³, Joanna Blackburn⁴, Kate Williams^5
1Professor of Skin Integrity, Director for the Institute of Skin Integrity, and Infection Prevention, also Department of Nursing and Midwifery, University of Huddersfield, Huddersfield, UK; Adjunct Professor, School of Nursing, Faculty of Health, Queensland University of Technology, Australia; Visiting Professor, Royal College of Surgeons in Ireland, Dublin, Ireland; Chair, International Wound Infection Institute; President Elect, International Skin Tear Advisory Panel.
²Visiting Clinical Research Associate, Medical Marketing Consultant; University of Huddersfield, Huddersfield, UK; Daneriver Consultancy Ltd, Holmes Chapel, UK.
³Independent Wound Care Consultant; Flintshire, North Wales, UK.
⁴Research Fellow, Institute of Skin Integrity and Infection Prevention, University of Huddersfield, UK
⁵Associate Director of Wound Care, Accelerate CIC, UK

*Corresponding author email markgeoffreyrippon@gmail.com

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