Identifying Opportunities for Antimicrobial Stewardship in a Tertiary Intensive Care Unit: A Qualitative Study

Abstract

Background: Antimicrobial stewardship (AMS) encompasses numerous interventions that seek to improve antimicrobial usage, as inappropriate use of antimicrobials may result in the promotion of antimicrobial resistance, patient harm, and increased costs. AMS is of particular interest in intensive care units (ICUs) where antimicrobial use is extensive. Few qualitative studies have sought to identify the perceived attitudes and beliefs of intensive care clinicians around AMS.

Objectives: To understand ICU nursing and physician priorities and preferences around AMS and possible AMS interventions for implementation in the ICU.

Methods: Using consecutive sampling, semi-structured one-to-one interviews were conducted with ICU nursing and physician staff at a tertiary hospital in BC, Canada.

Results: Nine participants (seven nurses and two physicians) were interviewed, and themes were identified and categorized as: opportunities to improve AMS in the ICU, barriers to AMS in the ICU, and possible future AMS interventions for implementation in the ICU. Opportunities identified included: clinician activities (improved communication, de-escalation, ICU nurse assessment) and support (infectious disease and antibiotic experts, AMS presence).  Barriers identified included: knowledge gaps (infectious disease and antibiotic knowledge, AMS awareness), AMS and ICU integration (nursing role in AMS, AMS efficacy in ICU), and environment (competing priorities, critical care context).  Interventions identified included: organisational (EMR modifications,

checklists, algorithms), learning (infectious disease and antimicrobial education, audit, and feedback), and nursing intervention (antibiotic review, prompting reassessment).

Groumoutis, J. Y., Gorman, S. K., & Beach, J. E. (2023). Identifying opportunities for antimicrobial stewardship in a tertiary intensive care unit: A qualitative study. The Canadian Journal of Critical Care Nursing, 34(2), 8–14. DOI: 10.5737/23688653-3428

Implications for nurses

• Both the definition of antimicrobial stewardship and nursing’s role in antimicrobial stewardship are not always clear to nurses.
• Nurses are keen on receiving education about antimicrobials and infectious diseases to improve their patient assessment-related skills.
• The implementation of various clinical tools and interventions may help nurses better contribute to antimicrobial stewardship efforts.
• Future research should be conducted investigating the effect of antimicrobial stewardship activities performed by nurses on outcomes related to antimicrobial usage and patient care.

Background

Antimicrobial stewardship (AMS) is defined as “coordinated interventions designed to improve and measure

the appropriate use of [antibiotic] agents by promoting the selection of the optimal [antibiotic] drug regimen

including dosing, duration of therapy, and route of administration” (Barlam et al., 2016, p. e51). AMS interventions have been categorized, as was done in a 2017 Cochrane review, according to the following functions: education, persuasion, restriction, environmental restructuring, and enablement (Davey et al., 2017).

The importance of AMS is highlighted by data qualifying the use of antimicrobials. Various studies have suggested that roughly 30–50% of antimicrobials are inappropriately used in hospital settings (Hecker et al., 2003; Magill et al., 2021; Núñez-Núñez et al., 2022; Park et al., 2022). These results are consistent with what has been measured for inappropriate antimicrobial use in the intensive care unit (ICU; Chiotos et al., 2022; Cusini et al., 2010; Macera et al., 2021). This is of interest, as antimicrobial usage in the ICU is a risk factor for developing antimicrobial resistance (Ang & Sun, 2018), and hospital-acquired infections by antibiotic-resistant organisms may increase the risk of mortality and readmissions (Barrasa-Villar et al., 2017). Furthermore, antimicrobial usage in ICU patients has been suggested to potentially contribute to patient harm related to mitochondrial and organ dysfunction, opportunistic fungal and C. difficile infections, adverse drug reactions and toxicities, and drug-drug interactions (Arulkumaran et al., 2020; Granowitz & Brown, 2008). Beyond the clinical implications of antimicrobial usage, reducing unnecessary usage in hospitals may reduce healthcare-associated costs (Nathwani et al., 2019).

Various strategies and interventions have been implemented and studied to optimize antimicrobial use in the ICU. Key strategies in the ICU include prospective audit and feedback, antibiotic time-outs, rapid diagnostics and laboratory testing, clinical pathways, computerized-decision support, and infection control (Chiotos et al., 2019; Pickens & Wunderlink, 2019). While the outcomes associated with these various strategies differ, the potential benefits include: decreased antibiotic use, reduced rates of C. difficile infections, decreased length of ICU or hospital stay, and cost savings without a negative impact on mortality (Pickens & Wunderlink, 2019).

As important as identifying interventions and strategies with supportive evidence to optimize antimicrobial usage is, an equally important task is determining the feasibility of

implementing proven interventions in a busy critical care environment. Few qualitative studies have sought to identify the perceived opportunities and barriers to the implementation of AMS interventions and attitudes of clinicians toward implementing antimicrobial stewardship programs and interventions, particularly in the intensive care setting (Jeffs et al., 2018; Steinberg et al., 2016). Understanding perceived opportunities

and barriers towards AMS interventions enables design and implementation of targeted implementation strategies that enhance facilitators and modify barriers. Moreover, this will also help to prioritize AMS interventions to deliver in the ICU setting. Therefore, the aim of this study was to identify ICU staff perspectives and help to identify priorities for AMS interventions at our institution.

Methods

This study was a prospective, qualitative descriptive study conducted at a 259-bed tertiary hospital within a regional health authority in British Columbia, Canada. The hospital’s intensive care unit is mixed; medical, and surgical and, at the time of initiation of this study, consisted of 11 inpatient beds. Annual admissions to the unit were roughly 500 per year. There were four physicians employed in the ICU to cover the unit in a

closed-unit model of intensive care service. The rounding team consisted of the physician, bedside nurse, clinical pharmacist, dietician, respiratory therapist, and patient care coordinator, with ad hoc participation of a physiotherapist, social worker, and Aboriginal patient navigator (APN). The health authority had an established regional AMS program staffed by two members – the medical director and pharmacy coordinator, who are not located in our hospital. The AMS program is governed by the health authority’s Pharmacy and Therapeutics Committee and institutes restrictive drug policies, provides education to physicians, pharmacists, and nurses, creates and

implements clinical decision support tools and pre-printed orders to guide appropriate antimicrobial use, performs antimicrobial quality improvement projects, and advises on

antimicrobial issues for the pharmacy and therapeutics committee. The regional health authority’s Research Ethics Board granted this research a certificate of approval (REB approval number: H19-03268).  All ICU staff were invited to participate via email invites or through in-person announcements at ICU morning huddles.

Inclusion criteria were any physician, nurse, patient care coordinator, nurse educator, manager or respiratory therapist working in the ICU. Learners (students, trainees, interns) and staff with casual employment status were excluded. Semistructured,

one-on-one in-person, audio-recorded interviews of 20-30 minutes were conducted at the hospital. An interview guide (Appendix 1) was developed in referring to semi-structured interviews used in similar qualitative literature. Question development for the interview guide was informed by categorizations of AMS interventions suggested by Davey et al. (2017), as well as the Effective Practice and Organisation of Care (EPOC) taxonomy (2015). Interview questions sought to capture participant beliefs and perceptions on AMS and usage within the ICU and the perceived potential impact of

various AMS interventions on improving antimicrobial use in the ICU. Interviews were conducted and transcribed by one author (JG, a pharmacy resident who received research training during their pharmacy education). This author did not have any prior relationships with the ICU team. Transcripts were independently coded by two authors (JG, JB). The transcripts were each coded twice via two different methods. Initially, two-thirds of the transcripts were openly coded in an inductive, semantic way, followed by axially to organize the codes into broader categories. It was then noted that the codes and categories created thus far aligned well with and could be further categorized under the domains present within the Theoretical Domains Framework (TDF) (Atkins et al. 2017). The decision was then made to openly code the initial transcripts again, though this time with a more deductive approach guided by the TDF concepts. Lastly, the last third of transcripts were coded twice each via the two previously stated methods, with codes being added to the master list of codes, one transcript at a time, to note the generation of any new codes and assess for data saturation. Data saturation was defined as: “the point in coding in which no new codes occur in the data” (Urquhart, 2013, p.194). Consensus on codes was confirmed via discussion between the two authors. A thematic analysis was then performed to identify and classify emergent themes, agreed upon by both authors involved with coding (JG, JB) and later reviewed by the other study author (SG). Themes were derived inductively from codes, within the parameters of this study’s objectives (identifying opportunities, barriers, and interventions). The COREQ reporting guidelines for qualitative research interviews were

reviewed and used to inform the reporting of the results of this study (Tong et al., 2007).

Results

A total of nine participants were recruited and interviewed, with interviews conducted in December 2019. Their characteristics are described in Table 1. None of these participants reported any formal training or education in infectious diseases beyond what they would have covered in their profession’s standard education and training. Themes relating to opportunities, barriers, and interventions to optimize antimicrobial usage in the intensive care setting were identified and are summarized in Tables 2, 3, and 4, respectively.

Opportunities [see Table 2]

Clinician activities

The majority of participants noted the need for thorough communication of the antimicrobial treatment plan between healthcare professionals. They perceived this would help facilitate stewardship efforts by enabling nurses to assess patients more effectively. Participants highlighted the importance of documenting antimicrobial indications and intended durations of therapy and the need for consistency in recording antimicrobial treatment details within nursing reports and handover tools. Additionally, the handover of care was identified as a key time requiring appropriate communication of the antimicrobial plan.

Table 1

Participant Demographics

Experience               Attending                 Nurses                      Total (%)

   in ICU                   Physicians                (n = 7)

   (years)                       (n = 2)

    0–4.9                            1                                2                               2 (22%)

    5–9.9                            1                                2                                 3 (33%)

    >10                                                                  2                               3 (33%)

  Unknown                                                          1                           1 (11%)

Nursing staff perceived that antimicrobial usage was too high in the ICU, while ICU physicians felt that antimicrobial usage was largely appropriate, though admitted there could be potential for improvement. A key possible area for improvement mentioned by participants was that broad-spectrum antibiotics may be overused as empiric therapy, and that narrowing of therapy should occur. There was also a belief among some nursing participants that either empiric therapy or broad-spectrum antibiotics should not be prescribed until preliminary culture results have returned. IV-to-PO stepdown of antimicrobials was also mentioned as something that could occur in a timelier manner.

The majority of nursing participants felt that the ICU nurse’s abilities and competencies around performing assessments were an important aspect to a patient’s antimicrobial care. With the appropriate knowledge of infectious diseases, clinical presentations, and antimicrobial uses and harms, nurses believed they could more comprehensively and efficiently conduct assessments of their patients’ statuses and review their progress.

They believed that their ability to know what should be flagged for a physician to review and their timeliness in doing so would be improved.

Table 2

Opportunities for antimicrobial stewardship in the intensive care unit

Theme                       Sub-themes             Quotes

Clinician                    Improved                    “I guess like if somebody moved in quite

Activities                    communication         quickly from another part of the hospital, or if it

was failed to be reported what they might have – an antibiotic resistant bug – or some other thing going on with them… Like that would kind of be something we’d address at the time but also it’d be better to know before they came in, right? Cause then you could handle this appropriately – isolation set up, or… yeah” (RN #3)

De-escalation           “So the length is one thing, and then switching from IV to PO, or stepping down to a narrower antibiotic from a broader spectrum antibiotic – those are all things that I suspect everybody can improve on.” (MD #1)

ICU nurse

Assessment              “I would prioritize the nurses touching on it [antimicrobials] in the morning during rounds so that the pharmacist can hear about what antimicrobials the patient is on. Assess how that’s going, how long they been on it, how effective it is, and – yeah. That will – even just doing that would be a big improvement from what we’re doing right now, I think.” (RN #7)

Support                      Infectious                   “…I guess, like, an infectious disease

disease and                           consultant. In other words, like, learning

antibiotic                    or having a second opinion from infectious

experts                       disease is helpful.”  (MD #1)

“The pharmacist had a lot of input as to different opinions and what the doctor wanted and they could have it out and whatever… Just having that other opinion and someone else looking at it. I think that’d be great.” (RN #6)

AMS presence          “…there is an antimicrobial stewardship program in [regional health authority], I understand, but they do not – I wouldn’t say that they really have any – like, their presence is not felt in our ICU whatsoever.” (MD #2)

Support

Most participants referenced the many ways the infectious diseases specialists contribute to the ICU, as well as how their role could be further expanded in providing a second opinion for a patient case. Physicians, while feeling confident in their own skills and antimicrobial knowledge, noted that input from an infectious diseases expert could be valuable in updating their knowledge on infectious disease topics. Various formats of

infectious diseases specialist oversight over cases in the ICU were suggested, including having infectious diseases automatically consulted in the case of Gram-positive bacteremias, all culture-positive bacteremias, all antimicrobial orders, and all infectious disease cases transferred in from external sites. The participation of the ICU pharmacist in multidisciplinary rounds was acknowledged, with comments as to how ICU pharmacists could or already do perform stewardship activities. Participants noted their utility in reviewing, assessing, and providing input on the antimicrobial care plan, and nurses identified ICU pharmacists as candidates for providing antimicrobial education.

Other services were less frequently mentioned for providing antimicrobial expertise and included the medical microbiologist and the infection prevention and control program. One nurse also suggested that leadership may come from a designated nurse AMS champion.

Neither physician felt that the AMS program had a strong presence within the ICU but noted their openness to receiving feedback from a stewardship team. One physician noted their hope that in the future the AMS program would be more involved in the ICU. Nursing participants were unaware of the existence of the AMS program and its role. Though unfamiliar with the program, nurses were generally enthusiastic to the idea of the AMS program collaborating with the local ICU staff to improve antimicrobial usage after being given a general idea of the program’s structure and functions.

Barriers [see Table 3]

Knowledge gaps

Nursing participants perceived themselves to be lacking in general infectious diseases and antimicrobials knowledge, as this was felt to be minimally covered in their nursing education and critical care training. This was felt to be a limitation to their ability to review and assess their infectious diseases cases. While participants mostly spoke of general knowledge gaps, some specific knowledge gaps identified were in the understanding of microbiology and therapeutic considerations for antimicrobials.

Table 3

Barriers to antimicrobial stewardship in the intensive care unit

Theme                       Sub-themes             Quotes

Knowledge gaps       ID and                        “I just did a BSN. I didn’t do a science degree

Antibiotic                  antibiotic                    or anything. Our schooling in particular was

Knowledge                pretty lacking in the microbiology aspect. Not a lot of infectious disease.” (RN #1)

AMS                           “Not sure if I know exactly what antimicrobial

Awareness                stewardship is.” (RN #2)

AMS and ICU            Nursing role              “I guess we have a very small, like integration

in AMS                       fundamental education on it [antimicrobials] but

ultimately, it’ll come down to the pharmacists and physicians.” (RN #3)

“Not a lot of value, to be honest, in targeting nursing just because I think it is unreasonable to expect that they are going to, you know, be, you know – be providing feedback to the prescribers. So, I think it – the only two roles that would benefit from this would be like, the ICU pharmacist and the ICU physicians.” (MD #2)

AMS efficacy             “I think that all of these sort of stewardship

in ICU                         interventions are going to probably have higher impact in the medical-surgical wards… if you were to have a, you know, audit and feedback, and they looked at a patient and they were like really really ill, there’s not going to be that many recommendations to narrow and to truncate duration of therapy…” (MD #2)

“ICU has so many resources that I think – I think they’re already doing it anyway, right? Like, you have pharmacists on rounds that’s going through the chart and looking at all the drugs that they’re on and – “Is this appropriate dosing?” and all that….” (RN #5)

Environment             Competing                 “I think the algorithms work, and pathways –

priorities                     clinical pathways – work. Definitely. As long as there’s not pages and pages and pages of stuff  because it can get to be sensory overload, right? Because there’s so many protocols and procedures and it gets to be just brain matter after a while and people just ignore it and it’s not that effective, right?” (RN #5)

Critical care               “And the other is, maybe, duration. It’s, you

Context                      know – there’s actually not a lot of good data on how long somebody should be treated for a pneumonia, for example. Whether it’s community-acquired or hospital-acquired. And a lot of infection disease stuff – there’s not

a lot of really hard data to say, “you must treat for two weeks for a bloodstream infection or etcetera.” So, people tend to err on the side of caution and give longer duration if they’re not sure or feel uncomfortable.” (MD #1)

None of the nursing participants were aware of the existence of an AMS program at our health authority or what role it could play in the ICU. Additionally, no nurses were formally aware of the term “antimicrobial stewardship” and its functions, though some were able to correctly guess as to some of the outcomes associated with antimicrobial stewardship (e.g., decreasing antimicrobial resistance, appropriate use of antimicrobials).

AMS Integration into the ICU

Participants did not generally believe stewardship to be a nursing role, rather perceiving the decision-making surrounding a patient’s antimicrobials to ultimately be the duty of the physician or clinical pharmacist. Suggestions were made that it is unreasonable to expect nursing to provide antimicrobial feedback to prescribers and that the culture in the ICU is such that nurses do not question or provide input to antimicrobial orders.

Skepticism towards the effectiveness of AMS initiatives in improving antimicrobial usage in the ICU setting was expressed widely by participants, driven by perceptions that

either AMS initiatives would be ineffective and enact no change or that the ICU was already accomplishing antimicrobial stewardship. Common beliefs were that the ICU pharmacist on rounds already acted as an antimicrobial steward and interventions like audit and feedback would be less effective in the ICU setting than they would on non-critical care, medical or surgical wards. One physician additionally expressed that: clinical pathways from the local regional health authority’s AMS program were not utilized by ICU physicians; the local antibiogram as provided (a small laminate brochure) was not easily accessible and, therefore, not useful; that restriction criteria

applied to certain antimicrobials did not influence their decision to prescribe the antimicrobial; and that there is little value in targeting nurses for antimicrobial education. Some nurses additionally expressed that they felt education was unlikely to change their practice.

Environment

Participants highlighted the high workload at times in the ICU and how distractions to maintaining workflow were a potential barrier to antimicrobial optimization. These included any procedures or workflows that are excessively complex as a result of

paperwork or instructions. Participants felt that task complexity leads to staff eventually ignoring protocols altogether and, thus, any antimicrobial-related workflows would need to be simple to be of any use. Other competing priorities identified as barriers related to timeliness, such as the delay in collecting specimens and receiving results and the delay in reassessing antimicrobial treatment plans.

Challenges inherent to the critical care practice environment were identified by both physicians and nurses. Physicians note the difficulty in selecting appropriate antimicrobials when diagnostic uncertainty is present and the potential consequences to

the patient if undertreated are great. This consequently leads to a hesitation to narrow therapy in critically ill patients. The lack of adequate data to guide antimicrobial prescribing in critical care patients and knowing when to consult the infectious diseases team were also identified barriers. Nurses highlighted the challenge of acquiring timely sputum cultures as well as lack of viable IV access points on some patients as challenges that impact the reassessment and timely administration of antimicrobials.

AMS Interventions [see Table 4]

Organizational

Both physicians provided suggestions on modifications to the EMR. These suggestions included embedding various clinical tools into the EMR such as local resistance patterns and the local antibiogram to help guide antimicrobial selection at the point of prescribing. Also suggested were EMR functions to assist with antimicrobial dosing and interaction checking at the time of ordering.

Participants felt the implementation of checklists for nursing staff that prompt antimicrobial reassessment could be valuable. They felt this would enable the nurse to ask questions on rounds that would facilitate reconsideration of details such as the indication or spectrum coverage. A suggestion was that an antimicrobial checklist could be integrated into the nursing report tool to become a standard of work.

The potential adoption of algorithms and clinical pathways was the most popular intervention among nurses. They noted that they preferred algorithms for their perceived efficacy, as well as their ease of use.

Learning

Most nurses were keen to receive infectious disease and antimicrobial education to address their self-perceived knowledge gaps in these areas. Educational modalities suggested for delivery of the information were varied and diverse, including nursing inservices, newsletters, and seminars. Suggestions were made on who should be providing the teaching, with the most frequent mentions being infectious diseases physicians, pharmacists, and the nurse educator.

Both physicians referred to prospective audit and feedback as a known AMS intervention that could be implemented to improve their antimicrobial knowledge, with this being the most highly preferred intervention by one physician. This physician stated they would be open to feedback from any healthcare professional, including pharmacists, microbiologists, and nurses, but preferentially would like to receive it

from an infectious diseases specialist. While nurses were not formally aware of audit and feedback as an AMS intervention prior to interviews, upon being given a basic overview of the concept most nurses believed audit and feedback to sound like an intervention that would be useful.

Nursing intervention

A common suggested nursing intervention to potentially aid with antimicrobial optimization was the nurse’s review of the patient and the antimicrobial treatment plan. Nurses felt they could clinically assess their patients’ progress and review details

such as the need for ongoing therapy or upcoming antimicrobial auto-stops and share these details on rounds. One nurse felt that, if equipped with the right knowledge, they could act as a second set of eyes and review the appropriateness of new antimicrobial orders.

Table 4

Interventions for possible implementation in the intensive care unit to promote antimicrobial stewardship

Theme                       Sub-themes             Quotes

Organisational          EMR modifications   “So what will be nice, and maybe that will be a

part of our new EMR when that news is – you know we’re getting a new EMR eventually, right? So, it would be nice if when a culture comes up that local resistance patterns are acceptable – accessible, with a click. “Oh, I’ve got – I don’t know what – growing Klebsiella in the urine. What’s our local resistance patterns?” So, it just makes it easier to just, right from the get-go, decide what antibiotic you’re going to do…” (MD #1)

Checklists                  “And that is one where I feel like nursing staff could be very helpful. If  that – they’re assigned to a patient they could sort of go through those questions like “Do we have microbiology? Are we on the right drug? Do we still need to be on therapy?”…and I think that would be super helpful” (MD #2)

Algorithms                 “I think the algorithms work, and pathways… If it’s simple and easy to  follow, then it will get used.” (RN #5)

Learning                    Infectious disease    “I wouldn’t mind an inservice actually on the

                                    antimicrobial             differences – I mean kind of a basic knowledge

education                   of Gram-negative versus Gram-positives and

learning about different sensitivities. Which, I don’t know, if they have like really red flags with different signs and symptoms or if we’re always just looking for temperature and white blood cells kind of thing. I think that might help us with kind of detecting and you know, then letting the doctor know what we’re seeing.” (RN #2)

Audit and Feedback            “So, I think like, if in an ideal world, there would be audit and feedback or some guidance from somebody who is – like that is their specific role. They have a particular interest in it. They have particular training in it. Cause otherwise it’s just, you know, the usual ICU clinicians, you know, doing the best that we can.” (MD #2)

Nursing          Antibiotic review                   Antibiotic review “Like say, my patient was on

Intervention                                                   Pip-Taz for pneumonia, and today we decided  

to stop it. I’m not running around trying to find a sputum spec. But I am going to go through the thought process of wondering “Oh, are her lungs still, you know – is it resolved?”… Instead of the antibiotics just stopping and going “Great! Whatever that problem was is over.” But maybe it’s not, cause I don’t really know what the antibiotics are for.” (RN #6)

Prompting reassessment    “even if nursing staff is not, you know, making the decision like “Hey, we should –we should narrow spectrum” or “Do we still need this antibiotic? Because we have an alternate explanation for the syndrome” – if they’re just at least prompting those questions in rounds and – I can see that being helpful as well.” (MD #2)

In addition to reviewing the antimicrobial treatment plan, participants felt there were opportunities to prompt physicians to reassess the antimicrobial treatment plan. Prompting on rounds to reconsider details such as antimicrobial indication, spectrum, need for ongoing therapy, and IV-to-PO stepdown were all mentioned as interventions that could potentially improve antimicrobial usage.

Discussion

This study explored ICU staff perceptions around AMS opportunities, barriers, and interventions in the ICU. The qualitative nature of this study allowed for the gathering of elaborative data from which themes were identified.

A main opportunity for AMS in the ICU was in the completion of clinician activities that would facilitate and promote antimicrobial stewardship. Improving communication between members of the ICU care team, as well as between care teams on transfer of care, was felt to be important and vital to ensuring that staff are well-informed of relevant antimicrobial details. The importance of the communication process has been highlighted in a systematic review of staff-reported barriers and facilitators when considering the implementation of interventions (Geerligs et al., 2018). They noted particularly the importance of communication between different disciplines, a finding consistent with our own. The implementation of organizational interventions to standardize the documentation and reporting of antimicrobial details, as well as nursing initiatives to review and share these details, have been identified as possibly

useful interventions within our study.

Another important activity highlighted by our participants was the de-escalation of broad-spectrum antimicrobials. De-escalation activities included narrowing the antibiotic spectrum for a more targeted and pathogen-directed antimicrobial therapy, and switching from intravenous to oral route of administration. De-escalating therapy in the ICU setting can be challenging given the acuity of illness present and the perception

of high risk of therapeutic failure with this activity. It has been well-established in sepsis guidelines that clinical presentation alone can warrant the prescribing of empiric antimicrobial therapy to treat vulnerable, critically ill patients (Evans et al, 2021). Interestingly, several nurses in our study commented that they believed broad-spectrum antimicrobials or empiric antimicrobial therapies should not be prescribed until at least preliminary microbiology results had returned. This may suggest that there are misunderstandings among some ICU staff as to the appropriate indications for empiric, broad-spectrum therapy, as well as the importance of their timely administration in sepsis. Interventions to help ICU clinicians understand the role of broad-spectrum

antimicrobials, as well as comfortably de-escalate them when appropriate, are needed. Education and feedback from expert resources are identified as key interventions within our study that may address these points and facilitate de-escalation.

Lastly, nurse assessments were highlighted in our study as an activity to promote AMS. Nurses felt their assessments of the patient’s status and progress were valuable in aiding with antimicrobial-related decision-making when shared with the care team on rounds or when used to prompt a reassessment of the antimicrobial treatment. In a study on nurse-driven antimicrobial stewardship, the nurse’s capacity to assess patients for IV-to-PO stepdown was identified as an AMS enabler (Fisher et al., 2018). Interventions with the potential to facilitate and enhance nursing assessments should be sought. This may include education initiatives to increase nursing competencies in AMS and the integration of standard organizational tools and reports into nursing workflows that enhance nurse assessments of antimicrobial care.

A second foremost opportunity identified within our study was external support for the ICU to facilitate AMS. Participants often alluded to antimicrobial expert resources such as the infectious diseases service to help guide local ICU teams. Physicians in our study were generally confident in their abilities and practices as stewards, but acknowledged there could be potential for improvement and were generally open to receiving feedback. This is consistent with findings by Steinberg et al. (2016), in which a survey of critical care physicians revealed that the majority agreed or strongly agreed that having an AMS program is beneficial to ICU patients and that an AMS program

increases knowledge of appropriate antimicrobial usage in the ICU. The findings also highlight the importance of an enhanced AMS presence within the ICU, another key form of support identified within our study. Interventions identified within our study that may seek to add support would be enhancing the role of the infectious diseases service in the ICU, as well as facilitating an audit and feedback program through the AMS program to positively impact antimicrobial usage in the ICU, as previous literature supports (DiazGranados, 2012; Elligsen et al., 2012; Khdour et al., 2018).

Three barriers to AMS in the ICU were identified in our study. The first barrier was knowledge gaps. Nurses were aware of their infectious diseases and antibiotics knowledge gaps and were keen to address them through teaching and various educational modalities. This is consistent with the findings by Olans et al. (2016) in their study to define the role of nurse education and staff nurse participation in AMS. Their survey of hospital nurses revealed that some of the most important issues to be addressed were proper technique for culture sample collection, basic microbiology interpretation, basic knowledge about IV-to-PO stepdown, when to de-escalate broad-spectrum antibiotics, and improving confidence in discussing antimicrobial usage with prescribers. Our study identified educational initiatives facilitated by antimicrobial experts as interventions that may address these nursing knowledge gaps. In addition

to general infectious diseases and antibiotic knowledge, nurses formally lacked an awareness of the term “antimicrobial stewardship.” A previous survey of hospital nurses revealed that the majority of hospital nurses are unfamiliar with the term “antimicrobial stewardship” or have heard the term, but do not know what it means (Merrill et al., 2019); a finding very consistent with our own. To promote AMS awareness and practices by nursing, an AMS program should have a strong presence within the ICU and be involved with staff education and feedback, as we have identified as opportunities.

A second barrier identified in our study related to integrating AMS into the ICU. Participants expressed doubts that AMS would be effective in the ICU, perceiving that AMS is either already accomplished or that it would be increasingly difficult to accomplish in the ICU context. Additionally, our participants have also expressed skepticism as to the nurse’s role in AMS. Participants felt that AMS is accomplished by and is the role of physicians and pharmacists. Previous studies have revealed that nurses believe they should be involved in AMS (Broom et al., 2017; Merrill et al., 2019). These views around AMS efficacy and roles in ICU by our participants contradict some of our opportunities identified, where our participants suggested various activities, supports, and specific interventions that would promote and facilitate AMS in the ICU. It is noted that psycho-social factors are frequent and often unaddressed elements that influence antimicrobial practices (Donisi et al., 2019). It is possible that this cognitive dissonance in our participants could be driven by simultaneous and contradicting enthusiasm and appreciation for AMS outcomes as well as fear and risk perceptions of undertreating critically ill patients. Further research into understanding this cognitive dissonance would be beneficial. Behavioural change science approaches may be needed to address this type of barrier. In their study of ICU nurses, Jeffs et al. (2018) identified that the key to engaging nurses in optimal antimicrobial usage was to engage them in their local AMS programs by leveraging their interests and passions. A more substantial AMS presence to engage nurses in the ICU may help to clarify the nurse’s role and overcome this barrier, as well as create the opportunity for nurses to assume leadership roles in AMS.

The third barrier identified in our study related to the ICU environment. Participants identified that the critical care context, with high acuity of illness, diagnostic uncertainty, and lack of practice-guiding data, was a barrier to AMS in the ICU. Increased guidance and support from infectious disease and antimicrobial experts for challenging infectious disease cases may help address this barrier. Additionally, competing priorities in the ICU concerning workflow and workload were identified as barriers. Identified interventions that may address workflow management challenges and facilitate AMS practices include EMR and nursing tools modification, so long that they simplify and expedite tasks and increase efficiency rather than add to the cognitive and physical workload. These environmental barriers identified are consistent with what has been found in the literature (Chiotos et al., 2019; Pickens & Wunderlink, 2019; Geerligs et al., 2018).

Three broad categories of interventions have been identified as potential targets for implementation in the ICU and have been alluded to thus far. Firstly, organizational interventions in the form of EMR modifications and nursing checklists and algorithms have emerged as preferred interventions for implementation. However, some participants expressed concerns that existing tools can either unnecessarily add to workload or are simply not used at all. These types of tools have been identified as being moderately effective in changing practice habits (Canadian Patient Safety Institute, 2012). Clinical decision support systems have demonstrated the ability to improve patient safety and clinical management, but excessive and inappropriate alerts can lead to alert fatigue (Sutton et al., 2020). This can create distrust in alerts altogether and dismissal of them regardless of appropriateness. These various organizational tools must be implemented with careful consideration in their design. Collaboration with the ICU team to design relevant, effective, and simple tools should be done to ensure they are used by ICU staff and effectively promote AMS.

Secondly, interventions for learning through education, audit, and feedback were also preferred. The enhanced presence and guidance from antimicrobial experts in the ICU could address knowledge-related barriers and skepticism towards AMS efficacy and roles in the ICU. Indeed, a study of infectious disease and ICU physician collaboration in the ICU demonstrated a significant reduction in antibiotic consumption (Rimawi et al., 2013). This could guide clinicians and empower them to accomplish de-escalation in the ICU successfully.

Thirdly, our participants preferred nursing interventions – antibiotic reviews and prompting reassessments – to facilitate AMS. A systematic review has suggested that nursing initiatives can potentially optimize antimicrobial usage in the ICU (Padigos

et al., 2021). Consistent with this literature, participants in our study, while formally skeptical of the nurse’s role in AMS, still highlighted nursing interventions they believed could be performed to contribute to AMS efforts. A key to engaging nurses in AMS further will be to increase nursing exposure to the AMS program and initiatives and include them in AMS leadership and champion roles (Padigos et al., 2021, Jeffs et al., 2018). This study has several limitations. This study sought to recruit a minimum consecutive sample of 10 interviews, but fell short of this target with only nine interviews completed. Of all the interviews completed, only two physicians were recruited, which could result in a possible underrepresentation of physician perspectives within our data. Additionally, the perspectives of other members of the ICU multi-disciplinary team, such as pharmacists and respiratory therapists should be represented.  Conversely, because seven of nine interviewees were nurses, nursing perspectives were likely well captured in our data. Per the definition used to define data saturation in our protocol, data

saturation was not achieved, though the incidence of new codes significantly dropped as coding progressed. Only one new code was identified from the coding of the final transcript, suggesting data saturation may have been nearly met. There may have been observer expectancy bias, given that the interviewer was a pharmacist. The results of this study may be limited in their generalizability, as all participants were recruited from one centre.

Further research can explore the feasibility of implementing the AMS interventions identified within our study and the impact of these interventions on outcomes related to antimicrobial stewardship.

Conclusions

ICU staff perspectives on AMS allowed for identifying opportunities, barriers, and priority interventions to improve antimicrobial usage in the ICU. Opportunities for improvement

included clinician activities that could be performed by ICU staff to facilitate AMS, as well as external supports that could be put in place to provide expertise and guidance. Identified barriers to optimal antimicrobial usage were knowledge gaps in infectious

disease syndromes and antimicrobials, the perceived inability to integrate AMS practice into the ICU, and the complexities and demands of the ICU environment itself. Suggested interventions for implementation included the modification or adoption of

organisational tools, learning in the ICU provided by experts, and nursing initiatives related to antimicrobial care. Considering the themes identified in this study may allow for the feasible and effective implementation of AMS initiatives in the ICU.

Author Notes

John Y. Groumoutis, BSc (Pharm), ACPR, Royal Inland Hospital, Kamloops, BC

Sean K. Gorman, BSc (Pharm), ACPR, PharmD, Interior Health Pharmacy Services, Kelowna BC

Jessica E. Beach, BSc (Pharm), ACPR, PharmD, Kelowna General Hospital, Kelowna BC

Address for correspondence

Jessica E. Beach, BSc (Pharm), ACPR, PharmD, Clinical Pharmacy Specialist in Critical Care at Kelowna General Hospital 2268 Pandosy St, Kelowna, BC V1Y 1T2.

Phone: 778-214-0345 Email: jessica.beach@interiorhealth.ca

Acknowledgments

The authors would like to thank Piera Calissi for her participation and useful discussion in the development of this study’s protocol.

Funding and Conflict of Interest

The authors have no conflict of interest to disclose.

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