What are the nursing competencies related to antimicrobial stewardship and how they have been assessed? Results from an integrative rapid review

Abstract

Background

Antimicrobial resistance issues, and the consequent demand for antimicrobial stewardship (AMS) programs, need to be investigated urgently and clearly. Considering the large amount of time nurses spend at patients’ bedside, the aim of the present study was to examine recent literature on nursing competency in AMS.

Methods

Drawing from Tricco and colleagues’ seven-stage process, a rapid review was performed. MEDLINE, CINAHL and EMBASE databased were searched from December 1st, 2019 until December 31st, 2021. Article screening and study selection were conducted independently by three reviewers. Data were analyzed narratively and categorized adopting an inductive thematic coding.

Results

Sixteen studies met the inclusion criteria and were included. Publications were mainly authored in USA (n = 4), Australia and New Zealand (n = 4) and Asia (n = 4), followed by Europe (n = 2) and Africa (n = 2). Ten studies were quantitative in design, followed by qualitative (n = 4) and mixed-methods studies (n = 2). Nursing competency in AMS seems to be influenced by a two-dimensional model: on the one hand, internal factors which consisted in knowledge, attitudes and practices and, on the other hand, external aspects which are at environmental level in terms of structures and processes.

Conclusion

This study provided a map of dimensions for researchers and practitioners to consider when planning clinical governance, educational activities, and research programs. Significant opportunities exist for nurses to contribute to practice, education, research, and policy efforts aimed at reducing antimicrobial resistance.

Background

Antimicrobial resistance (AMR) is considered a global threat whose magnitude has grown to the point that the World Health Organization (WHO) has taken the lead for a coordinated and multisectoral response [1]. The dramatic increase in the incidence of infectious syndromes goes hand-in-hand with health expenditures. At patient level, recent data suggest that there were nearly five million deaths associated with bacterial AMR in 2019 and that, by 2050, 10 million people per year are expected to be killed by AMR [2]. Six pathogens (i.e., Escherichia coli, Staphylococcus aureus, Klebsiella pneumoniae, Streptococcus pneumoniae, Acinetobacter baumannii, and Pseudomonas aeruginosa) account for 73.4% of deaths attributable to bacterial AMR [2]. As to expenditures, AMR not only exhausts more than nine billion euros per year in Europe but also an additional 20 billion dollars in direct healthcare costs in the US [3], with a projection of over 100 trillion US dollars to the worldwide economy by 2050 [4].

Antimicrobial stewardship (AMS) refers to the proper use of antimicrobials–including antibiotics, antivirals, antimalarials, and antifungals–to preserve their future effectiveness [5]. Nurses’ involvement in AMS is widely recommended [6] as they make up most of the healthcare workforce at the patient’s bedside. This provides the theme for several reviews that have been recently developed and that document the role of nurses as antimicrobial stewards, in both generic [6,7,8,9] and specific contexts of care (e.g., intensive care unit) [10]. The most recent review on nurse role and nurse contribution to AMS, which was published in 2021, covers the period from 2008 to November 2019. The authors examined 52 papers hghlighting that nurses’ involvement might be increased if they were formally welcomed into the AMS team and given the necessary training and support [8].

The first objective of the WHO Global Action Plan on Antimicrobial Resistance, which was adopted in 2015, prioritizes AMR claiming that the key approach to address the lack of expertise in antimicrobial misuse is to ensure that healthcare workers are educated and trained to develop the necessary competencies [5]. This can be achieved through the standardization of educational sources for AMR based on global evidence and best practices [5]. Limited research on nursing competency in AMS and its impact on patients’ outcomes resulted in the lack of an unambiguous definition of which actors are likely to influence nurses’ competency and involvement in AMS [6]. Moreover, especially in the last two years, the coronavirus disease 2019 (COVID-19) pandemic has had a significant impact on the undertaken AMS activities whose long-term outcomes are not yet known [11]. As critically ill COVID-19 patients suffer more frequent bacterial or fungal healthcare associated infections, an increased use of antimicrobials inevitably occurs. Therefore, identifying the up-to-date evidence is an issue of great relevance and it may help both nurse managers and educators to develop strategies for sustaining and enhancing nurses’ competencies in antimicrobial use and optimization.

A preliminary search aimed to explore available knowledge on nurses’ competency in AMS in the field was conducted by examining the MEDLINE database (via PubMed) and PROSPERO in November 2021. No recently published or ongoing reviews emerged on this specific topic (= nurses’ competency on AMS); meanwhile, a high number of AMS articles regarding stewardship in nursing field were published in the last years. The intent of this rapid review was to examine the extant and current literature on nursing competency in AMS, to develop strategies to enhance nurse’s participation in AMS programs, and to identify the gaps in education that can consequently be closed and guide training and educational programs.

Methods

Study design

An integrative rapid review as a knowledge synthesis approach capable of providing timely information [12] has been carried out in January 2022. The field of AMS is rapidly changing. Hence, timely reviews can offer a description of current research to report on modifications at both clinical and organizational levels [13].

Needs assessment and topic selection

The primary need was to map the most recent data on nurses’ knowledge of AMS with the intent to summarize the level of nursing competence and to highlight the methods and metrics for evaluating it. Thus, the review questions were: Which dimensions have been recently studied in their influence on AMS competency in nurses? How were these aspects measured? According to the WHO competency framework for healthcare workers’ education and training on antimicrobial resistance, competencies are a “combination of knowledge, skills, motives and personal traits”, whose development should help individuals to constantly improve their performance and to work more effectively [5]. For the purpose of this review, competency included level of knowledge, perceptions, beliefs, behaviors, roles, opinions, and attitudes [5].

Study development

According to the methodological process inspired firstly by Tricco and colleagues in 2017 [13], which was then further developed by Langlois and collegues in 2019 [14], the following seven-stage process was implemented: (1) needs assessment and topic selection; (2) study development; (3) literature search; (4) screening and study selection; (5) data extraction; (6) risk-of-bias assessment; and (7) knowledge synthesis. In addition, the Preferred Reporting Items for Systematic reviews and Meta-Analysis (PRISMA) guidelines were applied [15]. The review was pre-registered with the international prospective register of systematic reviews (PROSPERO registration number CRD42022311711).

Literature search

MEDLINE (via PubMed), Cumulative Index to Nursing and Allied Health Literature (CINAHL), and EMBASE databases were searched from December 1st, 2019 until December 31st, 2021. This timeframe was selected in order to capture the most recent trends in the research topic. Furthermore, 2019 was chosen as a year because a similar review (= nurses’ role and contribution to AMS) had already searched up to November 2019 [8]. This research included studies: (a) assessing nursing competency in AMS; (b) using both primary quantitative and qualitative study designs; (c) regarding any clinical setting; and (d) published in English. As in some countries (e.g., USA, Netherlands, Australia) prescribing competencies are directly integrated in nursing curricula, studies on nurse prescribers or nurse practitioners were included, as well as studies on nursing students. In addition, studies with multidisciplinary team members were included only if specific findings pertained also to nurses. As a consequence, Medical Subject Headings [MeSH] and free-text words used were: ‘Antimicrobial Stewardship’, ‘Nursing’, ‘Attitudes’, ‘Perceptions’, ‘Role’, ‘Believes’, ‘Knowledge’, and ‘Behaviors’. All these terms have been combined into the search strings with the Boolean Operator ‘AND’. Electronic database searches were completed on January 25th, 2022.

Screening and study selection

The screening of titles and abstracts was performed by three researchers (MD, TBW, DR) to identify articles’ eligibility in relation to the inclusion criteria. Then, an independent full-text evaluation was performed by the same researchers to determine if studies fully met the inclusion criteria. When disagreements occurred (e.g., nurses not recognizable among the multidisciplinary team members in the sample), the final decision to include or exclude an article was made by consensus. As reported in the PRISMA flow diagram (Fig. 1), the flow of study inclusion is summarized, together with the reasons for exclusion. At the end of the process, 16 papers were retrieved.

Fig. 1

Review flow diagram

Data extraction

Data were extracted in a Microsoft Excel® spreadsheet. The following data were extracted from each selected study and reported in the grid: (a) author(s), journal, publication year and country; (b) study design, setting (e.g., acute hospital), aims and participants’ profile; (c) item(s) under study (e.g., nurses’ performance of antibiotic stewardship activities); (d) metrics used (e.g., a web-based questionnaire); and (d) key findings. The full grid is available as Table 1.

Table 1 Data extraction process: steps performed

Risk-of-bias assessment

The review team shared in advance the decisions about inclusion and exclusion to prevent information and selection bias. In addition, to ensure consistency of results, the following methodological requirements [16] were respected: (a) at least one major scientific database was accessed (= three database: MEDLINE, CINAHL, EMBASE); (b) verification of the study selection and data extraction were performed by at least two reviewers (= three reviewers [MD, TBW, DR]); (c) the narrative synthesis and the summary table were provided and checked by an additional independent researcher (= a fourth researcher was involved [MM, expert in AMS]). Lastly, quality appraisal of studies was performed. The methodological quality of quantitative, qualitative and mixed-methods studies was independently assessed by three of the authors (MD, TBW, DR) by adopting the Mixed Methods Appraisal Tool (MMAT) developed by Hong et al. [17] (Table 2). The methodological quality score was not a reason to exclude studies.

Table 2 Summary of mixed methods appraisal tool (MMAT) methodological quality assessment

Knowledge synthesis

Given the descriptive nature of the research question and the methodological heterogeneity of the included studies, data were narratively analyzed and categorized adopting an inductive thematic coding [18]. In particular, as first step, the dimensions of nursing competency under study were categorized according to their common organizational or clinical significance. Then, the second step consisted of identifying subthemes and themes. Categorization was performed according to (a) the Donabedian model dimensions, namely structure (e.g., setting, human resources), process (e.g., activities, co-operation) and outcomes (e.g., nursing sensitive outcomes) [19] and (b) the knowledge, attitudes and practice model, commonly used to explain how individual knowledge and attitudes can affect behavioral changes [20]. Each phase of this process was the result of the discussions among the authors.

Results

Study characteristics

Database searching returned 1169 articles, of which 568 were screened. Out of 118 articles assessed for eligibility, 16 studies met the inclusion criteria (Fig. 1). Reasons for full-text exclusion are given in Fig. 1. The specific characteristics of each study that met the inclusion criteria are presented in Table 1. Publications were mainly authored in the USA (n = 4, 25.0%; Missouri, Pennsylvania [multiple regions of the States], Utah, Wisconsin) [21,22,23,24], Australia and New Zealand (n = 4, 25.0%; Auckland, New South Wales, Victoria [two studies]) [25,26,27,28], and Asia (n = 4, 25.0%; Indonesia, Saudi Arabia, Singapore, Thailand) [29,30,31,32], followed by Europe (n = 2, 12.5%; Italy, UK [multiple European countries] [33, 34] and Africa (n = 2, 12.5%; Malawi, South Africa) [35, 36]. With regard to the research method, ten studies (62.5%) were quantitative in design, using surveys in all cases [21,22,23, 25, 26, 29,30,31, 33, 34]. Qualitative research included interviews (n = 3, 18.8%) [27, 28, 35] and focus groups (n = 1, 6.2%) [32]. The remaining two studies (12.5%) were mixed-methods in design, including multiple data sources (e.g., interviews, direct observations) [24, 36].

Table 2 displays the overall methodological quality of the included studies. The majority of them were good in quality clearly showing the methodology comprising sampling strategy, data collection and analysis.

Dimensions affecting AMS competency

Upon the analysis of the 16 selected studies, 13 dimensions, which were grouped in five subthemes and two themes, were identified (Fig. 2). An overview of all dimensions included in this review (dimension(s) under study, subthemes and themes) is presented in Table 3.

Fig. 2

Dimensions affecting Antimicrobial Stewardship competency

Table 3 Data synthesis by extracting and abstracting findings in common categories and themes

Internal/personal factors

As to internal and personal factors, dimensions affecting AMS competency were measured at (a) knowledge, (b) attitudes and (c) practice levels. Factors at knowledge level were found to have the most influence on AMS competence (e.g., knowledge of antibiotics, knowledge regarding nurses’ role in AMS). Factors at attitudes level were instead studied with regards to attitudes (e.g., in antibiotic selection), opinions (e.g., regarding antibiotic resistance), perceptions (e.g., benefit of AMS) and beliefs (e.g., awareness in AMS). Factors referred to the practice were measured as behaviors (e.g., concerning antibiotic resistance) and professional performance (e.g., experiences of AMS).

External/environmental factors

Studies evaluating the external and environmental factors included two subthemes namely (a) structures and (b) processes. Dimensions referred to the structures were evaluated as context of care (e.g., physical environment), education, resources and specific guidelines, and policies availability. Lastly, the processes were evaluated as leadership support (e.g., governance influence) and group dynamics (e.g., multidisciplinary teamwork challenges).

Discussion

We identified 16 articles which related to nursing competency in AMS and were published in the last two years. The existence of such a large number of studies to our review reinforces the notion of an up-and-coming and meaningful interest on this particular research field. It is interesting to notice that these articles are spread across both low-income countries, such as Indonesia [30] and Malawi [36], and high-income states, such as Italy [34] and Missouri [23], which indicates that AMR is a contemporary global health threat. Moreover, it should be noted that qualitative research, which is more demanding than survey research, is limited; however qualitative studies is better methods to reveal facilitators and barriers to AMS implementation as they explore nurses’ perceptions of their experiences and roles within clinical settings in-depth [37].

The majority of the research examined in this review emphasized the significant contribution that nurses provide to AMS in hospital and community settings, where a high level of awareness among healthcare professionals has been documented [e.g., 31]. Healthcare students also proved to be acquainted with antibiotics and the related resistance, however their knowledge about the appropriate use was limited [29]. An international expert panel has recently developed a framework that addresses AMS to guide undergraduate nursing education (e.g., infection prevention and control) [38]. Several factors, such as the awareness of antibiotic resistance, the level of education, and beliefs, could influence students’ knowledge. It is important to engage healthcare students in communication and staff negotiations which address the issue of AMR with the aim of cultivating their knowledge, even in their earliest years of the undergraduate degree [25]. Moreover, the potential to prepare nurses for competencies and actions related to AMS is also ideal during university [38]. Improving the awareness of and the education on AMS and AMR also among registered nurses is an essential component in infection and prevention control. Nurses’ competency can be further strengthened by integrating fundamental education on AMS in the post-graduate studies and by providing continuing education in the clinical settings to enhance patient outcomes [31].

When looking at European level, healthcare workers’ knowledge of antibiotics and their use was higher (97%) when compared to their knowledge of the development and spread of antibiotic resistance (75%) [33]. The main reason for prescribing antibiotics was the fear of patient deterioration or the onset of complications; moreover, community prescribers were almost twice as likely as hospital prescribers to suggest antibiotics to deal with time constraints or to maintain their relationships with the patients [33]. Among healthcare professionals, differences in knowledge and beliefs about antimicrobial stewardship vary widely; there is a positive correlation between knowledge and behaviors [30]. Therefore, the use of the Health Belief Model (HBM) theory, which assumes several constructs (perceived severity, perceived benefit, self-efficacy, action signals) can support research to predict health workers’ behaviors [30]. Hamilton et al. highlighted that the factors that influence the decisions about prescribing antibiotic included patient condition (79%) and patient cost (58%) [22]. While 63% of nurse practitioners claimed to base their decisions on antibiotic use focusing on the antibiogram, 56% maintained to begin with broad spectrum antibiotics which are later customized upon the reception of cultures. Nurse practitioners are aware that resistance (97%), harmful effects on patient (97%), and resistance reduction due to optimum antibiotic use (94%) are the consequences of inappropriate antibiotic use. While 94% of nurse practitioners were well informed about the importance of having the proper knowledge of antibiotics and 86% felt certain about using them, 94% agreed on their overuse at national level and 62% on their overuse at work [22].

As to frontline staff in inpatient care, nursing engagement in AMS presents a considerable yet currently underused opportunity [35, 36]. Nursing identity is well aligned with stewardship identity, thus, at the moment, significant opportunities exist for nurses to provide their contribution to the practice, education, research and policy efforts intended to reduce AMR. These opportunities exist largely because of interprofessional and collaborative interplay. Expanding AMS to more empower nurses is pivotal to ongoing efforts to limit the trouble of AMR by perfecting judicious use of antimicrobials [28]. In spite of nurses being powerful contributors to AMS, the organizational culture can negatively impact on their ability to effectively provide their contribution. Strengthening team interaction can increase interdisciplinary participation in stewardship [23].

Limitations

The primary limitation of our study is the lack of an univocal definition of nursing competency in AMS. Since the word “competency” has multiple interpretations, we avoided using it in search terms. In order to ensure the retrieval of studies having at least one dimension of nursing competency (e.g., knowledge, perceptions), a broad search-term strategy was utilized; however, it’s possible that not all relevant studies were found. Secondly, although there was a wide range of countries represented in this review, the number of included studies did not allow for conclusions concerning nursing competency in AMS in specific country contexts, especially in European countries, in which only two studies were found.

Moreover, regarding external and environmental factors, no study addressed also the outcome dimension. Most of the studies, which were included in this rapid review, referred to AMS in the hospital and community care; there were few studies taking place in long-term care facilities [27], where the incidence of antimicrobial resistance is as much as hospital resistance [39].

Implications for practice and research

We conducted this rapid review to provide a map of dimensions on which scholars and practitioners should ponder when planning clinical governance, educational activities and research programs. At the clinical level, nurses have diversified roles in AMS. They have a leading position in facilitating investigations of microbiological samples, contributing to prescribing antibiotics and ensuring that antibiotics are available at the point of care. However, to provide the structure and drive the change, a committed leadership is required. Implementing AMR and AMS in the university curriculum, doubled by a thorough professional training at the post graduate level, is important in equipping nurses to fully act their role, resulting in a behavioral change and a more appropriate usage of antimicrobials. Then, further research is needed to address the gap in the theory guiding the identification and measurement of nurse competency regarding AMS. Shared job descriptions on AMS are required, in order to create hospital and community policies and measure the contribution of nursing care to the patients’ outcomes.

Conclusion

The findings from this rapid review, mainly of surveys from observational studies, suggest that nursing competency in AMS seems to be influenced by a two-dimensional model, considering both internal/personal and external/environmental factors; the former consists in knowledge, attitudes and practice and at of the latter in structures and processes. However, there is little consensus regarding which competency dimensions are of importance to AMS and how these can be measured. Despite the emerging focus on the nurse’s role in AMS – which is well documented in the majority of the studies – there are still major challenges, such as defining specific and recognized competences, promoting multidisciplinary work, and coping with limited resources.