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Implementing interventions to reduce antibiotic use: a qualitative study in high-prescribing practices

Implementing interventions to reduce antibiotic use: a qualitative study in high-prescribing... Background: Trials have shown that delayed antibiotic prescriptions (DPs) and point-of-care C-Reactive Protein testing (POC-CRPT) are effective in reducing antibiotic use in general practice, but these were not typically implemented in high-prescribing practices. We aimed to explore views of professionals from high-prescribing practices about uptake and implementation of DPs and POC-CRPT to reduce antibiotic use. Methods: This was a qualitative focus group study in English general practices. The highest antibiotic prescribing practices in the West Midlands were invited to participate. Clinical and non-clinical professionals attended focus groups co-facilitated by two researchers. Focus groups were audio-recorded, transcribed verbatim and analysed thematically. Results: Nine practices (50 professionals) participated. Four main themes were identified. Compatibility of strategies with clinical roles and experience – participants viewed the strategies as having limited value as ‘clinical tools’, perceiving them as useful only in ‘rare’ instances of clinical uncertainty and/or for those less experienced. Strategies as ‘social tools’– participants perceived the strategies as helpful for negotiating treatment decisions and educating patients, particularly those expecting antibiotics. Ambiguities – participants perceived ambiguities around when they should be used, and about their impact on antibiotic use. Influence of context – various other situational and practical issues were raised with implementing the strategies. Conclusions: High-prescribing practices do not view DPs and POC-CRPT as sufficiently useful ‘clinical tools’ in a way which corresponds to the current policy approach advocating their use to reduce clinical uncertainty and improve antimicrobial stewardship. Instead, policy attention should focus on how these strategies may instead be used as ‘social tools’ to reduce unnecessary antibiotic use. Attention should also focus on the many ambiguities (concerns and questions) about, and contextual barriers to, using these strategies that need addressing to support wider and more consistent implementation. Keywords: General practice, Antibiotic resistance, Antimicrobial stewardship, Antibiotics, Back-up prescription, Point- of-care testing, Focus groups * Correspondence: Aleksandra.borek@phc.ox.ac.uk Aleksandra J. Borek and Anne Campbell are joint first authors. Monsey McLeod and Sarah Tonkin-Crine are joint last authors. Nuffield Department of Primary Care Health Sciences, University of Oxford, Radcliffe Observatory Quarter, Woodstock Road, Oxford OX2 6GG, UK Full list of author information is available at the end of the article © The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Borek et al. BMC Family Practice (2021) 22:25 Page 2 of 11 Background evidence shows that POC-CRPT helps safely reduce anti- Mitigating the spread of antimicrobial resistance by more biotic prescribing [16] (e.g., by 15% in acute cough [17] prudent antibiotic use is a public health priority. Most antibi- and by 22% for chronic obstructive pulmonary disease otics are prescribed in general practice (72% in 2018) [1], exacerbations [18] compared to usual care). NICE sup- largely for respiratory tract infections (RTIs) which are often ports using POC-CRPT in adults with cough [19]. How- self-limiting [2, 3]. England has seen a gradual reduction in ever, both interventions have not been routinely antibiotic prescribing but with significant variation in pre- implemented in UK general practice, and the influences scribing rates within and between practices, even after on uptake, implementation and effectiveness of these accounting for factors such as comorbidities and deprivation strategies outside of clinical trials have not been [2–5]. Moreover, there is wide variation in prescribing to less adequately researched. unwell patients [6]. It is now important to identify ways to Many qualitative studies have explored clinicians’ facilitate (further) optimisation of antibiotic prescribing in views on antibiotic stewardship interventions, but often practices that have remained high-prescribing. as process evaluations within clinical trials [20–24]. Considerable evidence supports various interventions to These identified that general practitioners (GPs) prefer safely reduce antibiotic prescribing for RTIs [7–9]. Among multifaceted interventions which decrease diagnostic them are delayed (back-up, deferred) antibiotic prescrip- uncertainty, help provide patient-centred care and are tions (henceforth DPs) and point-of-care C-Reactive easy to implement [25], and that they experience inter- Protein testing (POC-CRPT) (Table 1). Trial evidence ventions as ‘supportive aids’ but also potentially as a shows that DPs can help safely reduce antibiotic use for compromise, source of distress, or unnecessary [26]. Few acute RTIs, with only 33–39% of patients given DPs using qualitative studies have focussed on implementing DPs antibiotics [10–13]. The National Institute for Health and [27, 28] and POC-CRPT [29–31] in the UK outside of Care Excellence (NICE) recommends considering DPs for trials. One study found prescribers used DPs infre- selected common infections [14, 15]. Similarly, trial quently, mainly to avoid anticipated conflict and because of feeling uncomfortable with burdening patients with Table 1 Definitions of DPs and POC-CRPT and related clinical responsibility, and perceiving DPs as a conflict- guidelines ing message [28]. Another study found DP use was influ- Delayed (also referred to as back-up or deferred) antibiotic pre- enced by: GPs’ prior experiences of using DPs, views on scriptions (DPs) how to protect the doctor-patient relationship, lack of The NICE defines DP as a prescription “given in a way to delay the agreed prescribing strategies within and between prac- use of [the antibiotic], and with advice to only use it if symptoms tices, and lack of feedback on how DP affects antibiotic worsen or don’t improve within a specified time. The prescription may be given during the consultation (which may be a post-dated prescribing data [27]. Studies found the implementation prescription) or left at an agreed location for collection at a later date of POC-CRPT as influenced by: cost/reimbursement, ”. (NICE Glossary) time, effect on workload and flow, access to equipment, NICE guidance recommends considering DPs for: � acute cough in patients with higher risk of complications, physical and operational constraints, quality control and � acute sore throat (with FeverPAIN scores of 2 or more or Centor score training, practitioner attitudes and experiences, local 3–4), champions, and gaps in evidence [29–31]. � acute otitis media (unless systemically very unwell or high risk of complications), This study aimed to explore the views of professionals � sinusitis if there is no improvement for more than 10 days (unless in high-prescribing general practices on use and imple- systemically very unwell or high risk of complications), mentation of DPs and POC-CRPT. In doing so, we build � lower urinary tract infections for non-pregnant women. (Summary of antimicrobial prescribing guidance – managing common on, and extend, previous studies by identifying how these infections; updated in March 2020, available on: https://www.nice.org. two strategies could be implemented to optimise antibi- uk/Media/Default/About/what-we-do/NICE-guidance/antimicrobial%2 otics in the ‘real world’ outside clinical trials and in prac- 0guidance/summary-antimicrobial-prescribing-guidance.pdf) tices that remain high-prescribing despite other initiatives Point-of-care C-Reactive Protein Testing (POC-CRPT) used to reduce prescribing (e.g. national data monitoring C-reactive protein (CRP) is a marker of inflammation that increases 4– and targets). We also specifically sought to explore views 6 h after the onset of inflammation or acute tissue injury and peaks at and suggestions to guide implementation and uptake of 36–90 h (1.5–4 days). Various point-of-care CRP tests are available that require a small blood sample from a finger prick and that produce a both strategies for commissioners, practices and/or clini- quantitative or semi-quantitative result within approx. 3 to 10 min. cians who may be considering using them. NICE clinical guideline [CG191] supports the use of POC-CRPT to help differentiate a serious infection from a self-limiting RTI in adults with acute cough (lower RTI) when, after clinical assessment, a diagnosis of Methods pneumonia has not been made. It suggests interpreting POC-CRPT re- Participants sults as follows: We identified general practices which were in the top � CRP < 20 mg/l: no routine antibiotic � CRP between 20 and 100 mg/l: delayed/back-up antibiotic 20% for antibiotic prescribing in the West Midlands � CRP > 100 mg/l: immediate antibiotic. Clinical Research Network (CRN), based on 2017 Borek et al. BMC Family Practice (2021) 22:25 Page 3 of 11 PrescQIPP data (antibiotic items per STAR-PU (Specific Data analysis Therapeutic group Age-sex Related Prescribing Unit)) Data were analysed inductively using thematic analysis [32]. We used the antibiotic items per STAR-PU as it is [33] with coding in NVivo software (v.12). We used the- commonly used in England to compare antibiotic pre- matic analysis because it is a systematic qualitative data scribing across practices and against prescribing targets. analysis method, suitable for applied health research, Study invitations were sent to 139 practices and then and allows the analysis to be driven by the data (by followed-up by email and/or phone. Additionally, the inductive coding) as well as the development of interpre- study was promoted by CRN Facilitators. Interested tations (themes) that extend understanding beyond just practices were asked to identify suitable date(s) for a a summary of data. Initially four researchers (AB, AC, focus group with at least three professionals (comprising STC, ED) coded the same 2–3 transcripts, discussed at least two prescribers and any other clinical or admin- coding and categories for the initial codes, and agreed istrative staff). Participants gave written consent at the on a coding framework. The coding framework was then start of focus groups. Practices were offered £500 reim- used by AC and AB to code all remaining transcripts bursement for one focus group. independently, adding new codes when needed, and then combining their analyses. Themes were identified, dis- cussed and agreed with a multidisciplinary team (AB, Data collection AC, STC, MM, ED), and then reviewed by the wider study We collected data through focus groups in participating team (including GPs, epidemiologists and behavioural practices to facilitate discussions among professionals economists). and elicit shared as well as divergent views on the use of the antibiotic optimisation strategies and practice-level Results implementation (rather than only individual use). Focus Nine practices participated, including 50 professionals groups took place in general practices between Decem- (3–11 per practice) (Table 2). Focus groups lasted 49–87 ber 2018 and April 2019. They were facilitated by two (mean 71) minutes. No practice had used POC-CRPT, researchers (AB, AC) – each leading a part of the focus although two (FG2, FG3) had the equipment. Four main group, while the other made notes. Discussions followed themes were identified; additional quotes are available in a semi-structured topic guide (see Additional file 1) Additional File 2. which was piloted with three GPs. The topics included: making antibiotic prescribing decisions, experiences of Compatibility of strategies with clinical role and using DPs, views on POC-CRPT (with three types of experience tests shown to prompt discussion), practice communica- Participants’ views on DPs and POC-CRPT were influ- tion and other antibiotic stewardship strategies used. As enced by their perceptions on how these strategies fit DPs are used by prescribers (although variably), we ex- with their clinical role and experience. They reported plored participants’ experiences; as POC-CRPT is rarely how the core clinical role in general practice (developed available in UK practices, we explored views about hypo- through training and experience) involved clinical thetical use. Focus groups were audio-recorded and assessment based on history-taking, examination and transcribed verbatim. Transcripts were anonymised, social factors. The clinical assessment could be also checked for accuracy with audio-recordings, and informed by, but prioritised over, clinical scores (e.g. speakers’ professional roles were added based on notes. Centor, FeverPAIN) and diagnostic tests. Table 2 Practice characteristics a b Focus group Urban / rural Deprivation (decile) FG participants FG1 Rural (village) Medium (5) 2 GPs, Nurse, HCA, Practice Manager FG2 Rural (town and fringe) Medium (5) GP, Pharmacist Prescriber, Business Partner FG3 Urban (major conurbation) High (2) 2 GPs, Prescribing Clerk, Practice Manager FG4 Rural (town and fringe) Medium (4) 2 GPs, Nurse, Practice Manager FG5 Rural (town and fringe) Low (7) 3 GPs, 2 GP Trainees, Nurse Prescriber, Practice Manager FG6 Urban (major conurbation) High (3) 4 GPs, Medicines Coordinator FG7 Urban (major conurbation) High (2) 3 GPs, Nurse FG8 Urban (major conurbation) High (2) 6 GPs, 1 GP Trainee, 2 Nurses, Practice Manager, Deputy Practice Manager FG9 Urban (major conurbation) High (1) 2 GPs, 2 GP Trainees, HCA, 2 Receptionists a b Index of multiple deprivation decile. GP – General Practitioner, HCA – Healthcare Assistant (non-prescriber), Nurse – Practice Nurse (non-prescriber) Borek et al. BMC Family Practice (2021) 22:25 Page 4 of 11 DPs and POC-CRPT were described as fitting with the GP1: I think [GP trainees would] test everybody… clinical role and useful when there is clinical uncertainty Because you give them any equipment and they use over diagnosis or prognosis, such that DPs could provide it religiously… they don’t look at the patient… a safety-net and POC-CRPT additional clinical informa- tion. Such uncertainty was described as quite rare, GP2: I think it would probably make them less though this depended on the experience of the clinical. prescriber. GP1: They’re so reliant now on the machines and When I use a deferred script it’s normally because I the templates… tick, tick, tick, do the test and then feel it’s a bit more of a borderline case… a patient treat. You haven’t actually looked at your patient where you’re not entirely sure and so it’s there for yet. [FG3] the patient if they worsen… [GP, FG2] Strategies used as social tools to negotiate treatment and Those people that are right on the fence, where educate patients you’re uhming and ahhing… it’s quite rare for a doc- Participants frequently described (perceived) patient tor not to know what type of infection you’ve got. expectations for antibiotics as a driver for unnecessary [GP, FG4] antibiotic use; some described reducing antibiotic pre- scriptions as beyond their control. GPs described their roles as ‘holistically’‘treating patients, not numbers’ [FG1] and that POC-CRPT would Antimicrobial resistance is beyond the surgery’s con- unlikely add much to, or change, their clinical judgment trol a lot of the time because it is patient expecta- if not uncertain. In contrast with secondary care, partici- tions (…) the patient insists and insists and that’s pants highlighted that diagnostic testing was not routine not the clinician’s fault that antibiotics are pre- in general practice. scribed in the end. [GP, FG2] A lot of your training in primary care is diagnos- They discussed using DPs and POC-CRPT as social tools ing patients without test interpretation. If you go to negotiate treatment with patients perceived as difficult into hospital, you get a battery of tests (…)It to reassure when not needing antibiotics (‘regular makes you more reliant on test results… Then the returners’ [FG6], ‘frequent offenders’ [FG8]). Most GPs more of these things are used I think maybe it reported using DPs as a compromise when they consid- does somehow take away from the clinicians… ered antibiotics unnecessary but felt that patients wanted [Manager: Art.] Yes, it may take [away] some of antibiotics; a GP trainee [FG5] described how with your clinical judgement. [GP, FG2] increasedexperienceheusedDPs less as a safety-net and more often as a compromise. Participants also envisaged Clinical experience seemed to influence perceptions of using POC-CRPT as ‘evidence’ to convince patients when usefulness of DPs and POC-CRPT. Some GP trainees re- antibiotics are unnecessary and ‘deny patients antibiotics… ported using DPs more (one accounted it to lower confi- more than deciding on antibiotics’ [GP, FG9]. Both strat- dence in clinical decisions); with more experienced GPs egies were seen as helping avoid lengthy negotiations, reporting using DPs less frequently, preferring immediate conflict, complaints and re-consultations; and helping or no prescription. GPs and nurses described POC-CRPT maintain good relationships, patient satisfaction and more as likely to be used more by trainees, and GPs perceived patient-centeredness (‘equal footing within the consult- POC-CRPT as more helpful for nurses and pharmacists ation’ [FG7]). They were also seen as strategies to educate who may rely more on test results to reduce clinical un- patients that antibiotics are unnecessary. certainty. More experienced clinicians described feeling more confident using their clinical judgment irrespective GP1: I tend to use [DP] in the people you just cannot of tests. They were concerned that dependence on POC- convince that they don’t need antibiotics. (…) some- CRPT by trainees might lead to loss of clinical skills. times it’s just the route of least resistance… It’s difficult at the start of training in that you’ve not GP2: …you’re using it as a trade-off… saying, ‘come got that much experience and (…) you’re more wor- on, give my way a bit of a chance, let’s see how it ried about making a mistake. I probably had a big- goes’… andiftheninafewdaysthey’re starting to ger range of ones that were in the middle and (…) feel a little bit better, they say, ‘okay, we’re on the felt more comfortable having that safety-net [of DPs]. right track’,and that’s when they don’tcome infor [GP Trainee, FG5] the antibiotics. (…) I suppose it leads to improved Borek et al. BMC Family Practice (2021) 22:25 Page 5 of 11 patient satisfaction, because they feel they’re not Table 3 Using ‘social tools’ to help address perceived patient expectations being fobbed off… it’s the key to not getting com- plaints. [FG4] � Perceived that patients expect to leave ‘with something’– use of prescriptions and leaflets I have a very simple rule… They’ve made the effort to come and see Participants described patients as expecting a pre- a doctor, give them a bit of advice, or even a prescription or a form scription and preferring tests and numbers, and for physio or something like that, it’s the key to not getting some reported already using clinical scores or tests complaints. Everybody gets a prize, even if it’s just a bit of written paper. [GP, FG4] to negotiate treatment decisions (Table 3). Others felt that patients were accepting of no-antibiotic I like to print out a post-dated prescription because actually giving them something in their hand to go away with gives them a sense decisions and reassurance with effective communica- that something’s happening. [GP, FG6] tion. Participants were also concerned that using …patients are used to have something to take away with them, so POC-CRPT may have unintended consequences, when they come they need something... whether it is a such as unexpectedly high test results, raising prescription... Sometimes what may help is on EMIS you’ve got patients’ expectations for tests and ‘medicalising’ patient information leaflets…[GP, FG7] common infections. They tend to like to leave with something and if it’s not antibiotics and not what they want, they seem to want to leave with some form of prescription be it an over the counter medicine or be it It’s funny, the amount of times that you’re advised to something else... I’m seeing more requests for things like nasal sprays treat the patient not the number, the patient will be and linctus… [GP, FG9] much happier with the number than your clinical � Perceived that patients want tests and numbers – use of POC judgement. [GP, FG2] tests It’s funny, the amount of times that you’re advised to treat the Nurse: Here it’s a small population and it’ll get patient not the number, the patient will be much happier with the number than your clinical judgement. [GP, FG2] around the patients and they’ll say, ‘well why did I could also use [POC-CRPT] on these frequent offenders who come they have that test and I didn’t’? in saying ‘I want antibiotics’… if you show them it’s not this and it’s not 100 and that convinces them in some ways psychologically not GP: Yeah… so then you’ll end up having to do it. to get the antibiotic. [GP, FG8] [FG4] A really good thing is to have a tool to demonstrate to patients why they don’t need antibiotics. I use my SATS probe quite a lot as a... it’s not really a tool but it helps me, I’ll kind of say ‘Well your oxygen saturations are very good.’ Which is why I’m very interested in testing Ambiguities about usefulness and impact of strategies CRP ‘cause I think that’s a really good evidence based tool, which if Participants considered pros and cons of DPs and patients understand, are going to be more receptive and accepting of your decision not to give them antibiotics, if you can actually POC-CRPT, and situations and patients when these demonstrate numerically that there’s no reason to. [GP, FG6] strategies should or should not be used, with appar- …like urine samples, they come in for urine symptoms when you ent ambiguity and contradictions. DPs were seen as think ‘This is not’– and then you dip it and say ‘Look, there’s none.’ helping relieve patients’ anxiety by improving access But that’s cheap… [GP, FG6] to antibiotics (e.g., before weekends) while reducing If you got a printout, you can give them a copy, it’s a prize, they’ve the need to re-consult. Some prescribers reported had a test… They think tests are how we do medicine, and they’re not…‘oh, I need a test, I need a scan’. [GP, FG4] using DPs for adults and children with RTIs and patients with additional risks (e.g. immuno- � Perceived that patients need ‘evidence’– use of clinical scores compromised); in contrast, others (sometimes the I use the FeverPAIN to not give them antibiotics because it’s just – same participants) reported not using DPs for adults it’s helpful to be like ‘well the computer says you don’t need them!’ And sometimes that works [laughter] better than ‘the doctor with RTIs (preferring to either prescribe or not), says you don’t need them!’…it does unfortunately bite me in the children (preferring to re-consult) or at-risk patients bottom sometimes when they come back again and say: ‘well what (preferring to prescribe or re-consult). does your score say?’ And it comes out saying ‘you need a delayed prescription!’ So they go away with a delayed prescription when probably clinically I wouldn’t have given them anything at all. [GP, If it’s for a child, then I’d rather review them. If you FG3] have a compromised patient or a diabetic patient, Sometimes what can help in sore throat is the Centor or the then I might issue the script because I know they are FeverPAIN, so you can actually show them the scoring criteria and say, ‘X, Y and Z, because you haven’t got any of those criteria, at a higher risk so it all depends. It’s not a fixed evidence shows us that it’s very unlikely that this is bacterial and this thing. It just depends on the individual. [GP, FG8] is in fact viral.’ [GP, FG7] Some participants reported using DPs with ‘sensible’ patients – those they perceived to ‘understand the use of antibiotics’ [FG8] and ‘on board with [DP]’ [FG6] Borek et al. BMC Family Practice (2021) 22:25 Page 6 of 11 (Table 4). Although no participant described patients as exacerbations. Some participants questioned the useful- ‘insensible’, some reported concerns about potential ness of CRP as a biological marker and the sensitivity intentional or unintentional misuse (i.e. they or others and specificity of tests. They were uncertain about inter- using the antibiotics immediately or in the future with- preting the results (particularly medium values) and how out consulting). For these patients, they reported being to act on results inconsistent with clinical judgment. more likely to add a ‘second step (…) [or] any slight im- pediment in their way [so] they won’t use it if they don’t I want to know what’s the evidence? What kind of need to’ [FG4] or ‘an extra layer of awkwardness’ [FG5], infections have they looked at? How do they know if for example, by leaving the prescription at reception to it’s viral or bacterial? I don’t really know. CRP is so be collected in a few days or post-dating it. non-specific… [GP, FG6] Participants were unclear about the effectiveness of DPs on reducing inappropriate antibiotic use; some ex- Participants had mixed views about the effectiveness of pected DPs to reduce antibiotic use, others thought they POC-CRPT on antibiotic prescribing. Some envisaged may increase it (i.e. when used instead of not prescrib- limited impact as they expected it not to change clinical ing). Participants were also uncertain if DPs count to- decisions, while some thought it may increase prescrib- wards prescribing rates if unused. Practices had no set ing due to perceived pressure to act on unexpectedly ways of issuing DPs and prescribers discussed with inter- raised test results. Nevertheless, most expressed interest est what their colleagues did. Prescribers reported in trying POC-CRPT, and generally thought that it could choosing DP formats to facilitate ease of antibiotic ac- reduce prescribing associated with perceived patient cess if it was helpful (e.g., giving verbal advice to wait pressure. when handing a prescription before a weekend/travel) with patients whom they trusted to use DPs appropri- I would worry that by doing [POC-CRPT] and then ately. Conversely, they reported choosing DP formats getting a result that I wasn’t necessarily expecting, I that deterred patients from using the antibiotic immedi- would then feel obliged to prescribe something ately (e.g., by post-dating) when they doubted that pa- because otherwise I’m not acting on an abnormal tients would use DPs appropriately. result. [GP, FG1] The biggest disadvantage is that unless it’s post- If I want to prescribe, I don’t think I’d even do the dated, a proportion of people will go and cash it. test. [GP, FG3] That’s what they wanted. [GP, FG5] Influence of context on use of strategies Ambiguity about when and how POC-CRPT should be Context, including practice characteristics and situ- used was also apparent. Some participants considered ational factors, influenced care and use of both strategies whether they could use it when deciding about hospital (for summary see Table S1 in Additional File 3). High admission; to monitor recovery over time; to screen and prescribing was felt to be partially a result of practice/ triage patients and for patients with COPD staff characteristics (e.g. more locums/trainees and staff turnover) and patient characteristics (e.g. comorbidities, culture/languages, deprivation). Table 4 Participants reporting using DP with ‘sensible’ patients Practice context influenced whether and how DPs I only give delayed antibiotics if I feel like the patient or the patient’s were used. Prescribers from practices with ‘good access’ parent is very sensible and on board with it. [GP, FG6] (where patients could get appointments quickly), tele- Generally [DP] is for chest complaints that I would issue it, or if they’ve phone triage and other available services (e.g., extended had recurrent tonsillitis that has required antibiotics that it’s been access) preferred to re-consult rather than give DPs. Pre- appropriate for and they’re starting to become unwell and you’ve got a sensible family, then I might do it then as well… [GP, FG7] scribers from rural practices preferred to give DPs, or provide antibiotics from the on-site dispensary, with [DP] would be useful for patients who understand the use of advice to delay taking antibiotics to minimise patients’ antibiotics, who are bit more sensible but not for everybody I would say, considering we’ve got some population who doesn’t burden of returning to the practice. understand when to use it. Some population groups in this practice who don’t understand when to use antibiotics so they’ll still be feeling I don’t think we do very many delayed scripts at all okay and will still get antibiotics and take it because they are used to that. [GP, FG8] because of the way we work, because of the easy access and the dispensary. [GP, FG1] I also probably gauge which ones I think are more likely to be sensible hopefully. [Patient’s father] said ‘Yes, I think that sounds reasonable’. He seemed a bit reassured about that. Let’s see how she Moreover, DPs were described as used less in practices goes in the next few days. [GP trainee, FG9] in areas with higher deprivation and patients from Borek et al. BMC Family Practice (2021) 22:25 Page 7 of 11 certain cultures or non-English speakers (perceived as ‘sensible’ patients, often choosing the format of DP to less likely to use DPs appropriately). The desire to avoid make things easier for patients they trusted or create additional workload for the administrative staff and barriers for patients they perceived to expect antibiotics potential conflict with patients made prescribers less but who did not require them. Participants also reported likely to ask patients to collect DPs from the practice mixed views and doubts about the perceived impact of reception. DP and POC-CRPT on antibiotic prescribing/use in the Participants raised many practical challenges with real world, outside of trial settings. Participants dis- implementing POC-CRPT, particularly around time, cussed many contextual and practical issues with imple- logistics and cost. GPs considered consultations too menting DPs and POC-CRPT. There was a prevalent short for POC-CRPT and envisaged asking nurses or sense of ambiguity and mixed views about the strategies: healthcare assistants to perform the tests. Some con- how they fit in general practice; when and how they sidered triaging patients with the tests before their should be used; and to what extent the benefits outweigh appointment. Participants discussed training and barriers to implementation. logistical difficulties in storing and maintaining equip- ment – difficulties they envisaged would disrupt Strengths and limitations workflows, add workload, and require carefully de- We recruited a high number of participants from a vised implementation protocols. relatively diverse range of practices and the nine focusgroupsprovideduswith rich datatoanswer Because it’s so ad-hoc it would be quite difficult for our research question and develop the reported you to know when you’ve got patients and you want themes and findings. The quality of data collection to do it and how you’re going to fit it in… in amongst and analysis was strengthened by involving multiple other patients that you’re already seeing, it could be experienced qualitative researchers and discussions quite tricky. [Nurse, FG4] with a multidisciplinary team. The analysis was data- driven and data saturation was achieved, with mul- Participants reported limited ability for practices to fund tiple quotesacrossall focusgroupssupportingthe POC-CRPT, seeing additional commissioners’ or govern- findings (see also Additional File 2). The study was ment funding as necessary for adoption. Some described reported following relevant standards (with the how wider contextual influences drove the uptake of reporting checklist and additional details in POC-CRPT, such as needing to ‘keep up’ with other Additional File 3)[34]. practices and countries adopting POC-CRPT, and Transferability of the findings may be limited as we expecting to be increasingly required to use POC-CRPT included high antibiotic prescribing practices from one as evidence for prescribing audits and medico-legal area in England and some practices had reduced their reasons. prescribing rate before the focus group. We used the antibiotic items per STAR-PU as a measure to identify …we’d use it because if everyone else is doing it… high prescribing practices that may particularly benefit and you’re the only one and something goes wrong, from strategies to support optimising their antibiotic then it’s indefensible… In a court of law they’ll say, prescribing. High antibiotics/STAR-PU may suggest “well everyone else in the patch is using it, why don’t some suboptimal prescribing but it does not take into you use it”? “Because I don’t need to”. “I know, but consideration potential valid reasons for high prescribing in this case you were wrong…” What are you going rates such as those practices with high numbers of to say then? [GP, FG4] patients with co-morbidities [5]. In our study, we did not explore in more detail the (in)appropriateness of Discussion antibiotic prescribing and only used the antibiotics/ Participants reported mixed views about whether or not STAR-PU as a proxy to identify practices that may have each strategy would be useful and in what circum- more scope for and benefit from implementing stances. Overall, they perceived the strategies to be of additional strategies to optimise antibiotics. While focus limited value as ‘clinical tools’, helpful only in ‘rare’ situ- groups allowed participants to discuss and address dif- ations of clinical uncertainty and for less experienced ferent views and experiences, the presence of colleagues prescribers. By contrast, both strategies were seen as with different roles might have influenced what individ- helpful ‘social tools’ to negotiate treatment while main- uals shared and led to a dominance of GPs’ views (who taining relationships or educating patients that antibi- tended to speak more). As the practices had not used otics may not be necessary, especially for patients POC-CRPT, participants’ views were hypothetical and perceived to expect antibiotics. However, many pre- might differ from actual experiences of using POC- scribers described DPs as a strategy to be used only with CRPT as evidenced previously [23, 24, 35]. Borek et al. BMC Family Practice (2021) 22:25 Page 8 of 11 Comparison with existing literature expecting antibiotics, likely to use DPs inappropriately, Similar to existing literature, both strategies were seen and that DPs are suitable only for selective (‘sensible’) as ‘clinical tools’ to help manage clinical uncertainty, patients [27, 28, 36, 40, 41], and that patients are con- especially for those still developing clinical skills/experi- vinced by tests and numbers. Contrary to their own res- ence: DPs were used to safety-net instead of re- ervations about POC-CRPT, GPs described stressing the consulting [27, 28, 36] and POC-CRPT to help assess ill- certainty of POC-CRPT to patients. Despite the impact ness severity and whether antibiotics are needed [23, 24, of clinicians’ perceptions of patient expectations on pre- 29, 30, 35, 37–39]. However, we found that clinical scribing, studies show that these perceptions tend to be uncertainty about RTIs among experienced clinicians overestimated or misjudged [43–45]. Moreover, evidence was seen as relatively ‘rare’. This resonates with existing shows that effective communication skills can help literature, with RTI consultations described as ‘simple’ understand and address patient concerns and expecta- [28]. Other types of uncertainty were apparent. For tions, maintain good relationships, and educate patients POC-CRPT, this was not only regarding the quality of about infections and antibiotics, and may be more sus- tests, but also how results should be interpreted and the tainable long-term [17, 46, 47]. perceived pressure to act on results inconsistent with clinical judgement [29, 30, 39] – which were seen to po- Implications tentially threaten a prescriber’s clinical role and skills. The Covid-19 pandemic has brought forth new uncer- For DP, other types of uncertainty were regarding how tainties and challenges for healthcare systems across the patients may use them [28, 36, 40] and how useful DP world [48, 49], including for prescribers in primary care. was as a strategy to reduce inappropriate antibiotic use. Mitigating the spread of antimicrobial resistance by Despite clinical guidelines, participants were unclear and more prudent antibiotic use is an even greater public had mixed views about when these strategies were clin- health priority for pandemic response and preparedness. ically suitable. In all, the use of these strategies as ‘clin- A first step in managing the new uncertainties around ical tools’ in high-prescribing practices was viewed as Covid-19 is to identify which uncertainties are already limited. This compares with previous studies which ‘known’ and to minimize these where possible [49]. found that GPs from low-prescribing practices perceived However, many policies tend to advocate use of DPs DPs as more useful as a safety-net than GPs from high- and POC-CRPT to only reduce clinical uncertainty. Based prescribing practices whose use of DP was instead more on our study findings, this approach lacks sufficient atten- influenced by social/patient factors [27, 40]. Importantly, tion to other types of uncertainties and ambiguities rele- it differs in showing that simply providing POC-CRPT vant to prescribers. It also does not acknowledge nor equipment or guidelines for use of DPs or POC-CRPT advise how these strategies may or may not be used as to address ‘clinical uncertainty’ may be insufficient to ‘social tools’ in practice. High-prescribing practices may optimise antibiotic prescribing and prescribers in high- benefit from implementing DPs and POC-CRPT but prac- prescribing practices may need to challenge their current tice staff would first need to be clearer on the benefit of ‘confidence’ about prescribing. these strategies, in what contexts/situations, and how they Participants seemed more convinced about the useful- would fit with practice. Presenting clinical trial evidence ness of both strategies as ‘social tools’, especially with alone is insufficient to motivate intervention adoption. patients perceived as expecting antibiotics. Counter to Moreover, it is currently unclear how transferrable the guidance, previous studies also describe clinicians using trial evidence is to routine practice in terms of implemen- DPs as a compromise – to maintain relationships, avoid tation as well as effectiveness of these strategies outside of conflict and complaints [27, 28, 40, 41], and to educate research contexts. Evaluating these strategies in the ‘real patients that antibiotics are not always necessary [10, 27, world’ of (high-prescribing) practices would provide a bet- 41, 42], especially in high-prescribing practices [27]; and ter understanding of whether, when and how these strat- POC-CRPT to convince and reassure patients of no egies might be useful. need for antibiotics [24, 29, 30, 35, 37–39]. Our partici- Despite the uncertainties, ambiguities and doubts pants contrasted unnecessary antibiotic prescribing about these strategies, our participants also perceived which resulted from perceived patient expectations with them as potentially helpful in certain contexts and situa- high antibiotic prescribing arising from contextual fac- tions. As antibiotic prescribing and use are complex tors including patient characteristics and staff/patient behaviours influenced by various determinants, it is turnover. As ‘social tools’, DPs and POC-CRPT were unlikely that one or two strategies would ‘solve’ the perceived as particularly helpful in high-prescribing issue. While DPs and POC-CRPT may be insufficient as practices with higher patient expectations and need for stand-alone strategies, they might be useful in addition antibiotics. Some participants displayed a paternalistic to other strategies (e.g. audit and feedback, communica- approach and described their patients as mostly tion skills), or more acceptable to clinicians and/or Borek et al. BMC Family Practice (2021) 22:25 Page 9 of 11 patients than some strategies (e.g. a no-antibiotic strat- Koen B. Pouwels, Julie V. Robotham, Laurence S. J. Roope, Sarah Tonkin- Crine, Ann Sarah Walker, Sarah Wordsworth, Carla Wright, Sara Yadav, Anna egy). To support implementation, research should focus Zalevski. on developing and testing implementation strategies; specifically, develop evidence on optimal approaches to Authors’ contributions AB contributed to the design of the protocol, conducted interviews, implementation; training in when and how to use DPs conducted the analysis, and was a major contributor to writing the and POC-CRPT and how to effectively discuss strategies manuscript through critical review, commentary and revision. AC contributed with patients; and investigate (intended and unintended) to the design of the protocol, conducted interviews, conducted the analysis, and was a major contributor to writing the manuscript through critical consequences of using these strategies routinely in high- review, commentary and revision. ED conducted analysis. CCB obtained prescribing practices. Similarly, commissioners and prac- funding and led the study throughout to achieve goals. He supervised the tices/clinicians wanting to increase the use of these strat- research team conducting the study. AH obtained funding and led the study throughout to achieve goals. She supervised the research team conducting egies need to address the perceived ambiguities about the study. MM obtained funding, critically reviewed the manuscript, and led DPs and POC-CRPT and practical challenges; for the study throughout to achieve goals. He supervised the research team example, disseminate relevant evidence and guidelines; conducting the study. ASW obtained funding and led the study throughout to achieve goals. She supervised the research team conducting the study. fund POC-CRPT equipment; help problem-solve prac- MMc conceived the study, contributed to the design of the protocol, tical challenges to use; provide feedback on how patients supported the analysis, and was a major contributor to writing the use DPs; and develop practice-specific protocols for manuscript through critical review, commentary and revision, obtained funding, and led the study throughout to achieve goals. STC conceived the using these strategies consistently. study, contributed to the design of the protocol, conducted the analysis, and was a major contributor to writing the manuscript through critical review, commentary and revision, obtained funding, and led the study throughout Conclusions to achieve goals. All authors read and approved the manuscript. In conclusion, our findings extend current knowledge regarding how DPs and POC-CRPT are used as ‘clinical Funding tools’ or ‘social tools’ in UK/English general practice The study was funded by the Economic and Social Research Council (ESRC) through the Antimicrobial Resistance Cross Council Initiative supported by and in other countries [23, 24, 35, 36, 38–41]. They the seven research councils in partnership with other funders (grant highlight the ambiguities and complexities which teams reference: ES/P008232/1) and supported by the National Institute for Health in high-prescribing practices consider when thinking Research (NIHR) Health Protection Research Unit (HPRU) in Healthcare Associated Infections and Antimicrobial Resistance in partnership with Public about implementing these strategies and their impact Health England [HPRU-2012-10041], and the NIHR Oxford Biomedical on antibiotic prescribing/use. Most notably, they Research Centre. ASW and CCB are NIHR Senior Investigators. The support of explain why high-prescribing practices may not value the funders is gratefully acknowledged. The funding bodies played no role in the design of the study and collection, such strategies as ‘clinical tools’ and thus have import- analysis, and interpretation of data, and in writing the manuscript. The views ant implications for policy advocating for all prescribing expressed are those of the authors and not necessarily those of the NHS, the to be based on testing [50]. NIHR, the Department of Health and Social Care or Public Health England. Availability of data and materials Supplementary Information The dataset analysed during this study is available from the corresponding The online version contains supplementary material available at https://doi. author on reasonable request. org/10.1186/s12875-021-01371-6. Ethics approval and consent to participate The University of Oxford research ethics committee (ref. R59812) and NHS Additional file 1: Focus group topic guide Health Research Authority (ref. 19/HRA/0434) approved the study. All Additional file 2: Additional quotes supporting the findings participants provided written informed consent for participation in the study. Additional file 3: Summary of views on contextual influences on DP and POC-CRPT Consent for publication Additional file 4: Reporting checklist Not applicable. Competing interests Abbreviations The authors declare that they have no competing interests. COPD: Chronic obstructive pulmonary disease; CRN: Clinical research network; CRP: C-reactive protein; DPs: Delayed antibiotic prescriptions; Author details GP: General practitioner; HCA: Healthcare assistant; NICE: National Institute for Nuffield Department of Primary Care Health Sciences, University of Oxford, Health and Care Excellence; POC-CRPT: Point-of-care C-reactive protein test- Radcliffe Observatory Quarter, Woodstock Road, Oxford OX2 6GG, UK. ing; RTIs: Respiratory tract infections; STAR-PU: Specific therapeutic group National Institute for Health Research (NIHR) Health Protection Research age-sex related prescribing unit; UK: United Kingdom Unit in Healthcare Associated Infections and Antimicrobial Resistance, Imperial College London, London, UK. Primary Care Population Sciences and Acknowledgements Medical Education, Faculty of Medicine, University of Southampton, We thank the general practice professionals for participating in the study. We Southampton, UK. NIHR Health Protection Research Unit in Healthcare also acknowledge, and thank for, the support with recruitment of the Associated Infections and Antimicrobial Resistance, University of Oxford, 5 6 National Institute for Health Research Clinical Research Network. Oxford, UK. NIHR Oxford Biomedical Research Centre, Oxford, UK. Nuffield This paper is part of the work of the STEP-UP study team comprising: Philip Department of Medicine, University of Oxford, Oxford, UK. Centre for E. Anyanwu, Aleksandra J. Borek, Nicole Bright, James Buchanan, Christopher Medication Safety and Service Quality, Pharmacy Department, Imperial C. Butler, Anne Campbell, Ceire Costelloe, Benedict Hayhoe, Alison Holmes, College Healthcare NHS Trust, London, UK. NIHR Imperial Patient Safety Susan Hopkins, Azeem Majeed, Monsey Mcleod, Michael Moore, Liz Morrell, Translational Research Centre, Imperial College London, London, UK. Borek et al. 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Commissioned by HM Government and supported by the Wellcome Trust; 2016 [cited 2020 Jun 29]. Available from: https://amr- review.org/home.html Publisher’sNote Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png BMC Family Practice Springer Journals

Implementing interventions to reduce antibiotic use: a qualitative study in high-prescribing practices

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10.1186/s12875-021-01371-6
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Abstract

Background: Trials have shown that delayed antibiotic prescriptions (DPs) and point-of-care C-Reactive Protein testing (POC-CRPT) are effective in reducing antibiotic use in general practice, but these were not typically implemented in high-prescribing practices. We aimed to explore views of professionals from high-prescribing practices about uptake and implementation of DPs and POC-CRPT to reduce antibiotic use. Methods: This was a qualitative focus group study in English general practices. The highest antibiotic prescribing practices in the West Midlands were invited to participate. Clinical and non-clinical professionals attended focus groups co-facilitated by two researchers. Focus groups were audio-recorded, transcribed verbatim and analysed thematically. Results: Nine practices (50 professionals) participated. Four main themes were identified. Compatibility of strategies with clinical roles and experience – participants viewed the strategies as having limited value as ‘clinical tools’, perceiving them as useful only in ‘rare’ instances of clinical uncertainty and/or for those less experienced. Strategies as ‘social tools’– participants perceived the strategies as helpful for negotiating treatment decisions and educating patients, particularly those expecting antibiotics. Ambiguities – participants perceived ambiguities around when they should be used, and about their impact on antibiotic use. Influence of context – various other situational and practical issues were raised with implementing the strategies. Conclusions: High-prescribing practices do not view DPs and POC-CRPT as sufficiently useful ‘clinical tools’ in a way which corresponds to the current policy approach advocating their use to reduce clinical uncertainty and improve antimicrobial stewardship. Instead, policy attention should focus on how these strategies may instead be used as ‘social tools’ to reduce unnecessary antibiotic use. Attention should also focus on the many ambiguities (concerns and questions) about, and contextual barriers to, using these strategies that need addressing to support wider and more consistent implementation. Keywords: General practice, Antibiotic resistance, Antimicrobial stewardship, Antibiotics, Back-up prescription, Point- of-care testing, Focus groups * Correspondence: Aleksandra.borek@phc.ox.ac.uk Aleksandra J. Borek and Anne Campbell are joint first authors. Monsey McLeod and Sarah Tonkin-Crine are joint last authors. Nuffield Department of Primary Care Health Sciences, University of Oxford, Radcliffe Observatory Quarter, Woodstock Road, Oxford OX2 6GG, UK Full list of author information is available at the end of the article © The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Borek et al. BMC Family Practice (2021) 22:25 Page 2 of 11 Background evidence shows that POC-CRPT helps safely reduce anti- Mitigating the spread of antimicrobial resistance by more biotic prescribing [16] (e.g., by 15% in acute cough [17] prudent antibiotic use is a public health priority. Most antibi- and by 22% for chronic obstructive pulmonary disease otics are prescribed in general practice (72% in 2018) [1], exacerbations [18] compared to usual care). NICE sup- largely for respiratory tract infections (RTIs) which are often ports using POC-CRPT in adults with cough [19]. How- self-limiting [2, 3]. England has seen a gradual reduction in ever, both interventions have not been routinely antibiotic prescribing but with significant variation in pre- implemented in UK general practice, and the influences scribing rates within and between practices, even after on uptake, implementation and effectiveness of these accounting for factors such as comorbidities and deprivation strategies outside of clinical trials have not been [2–5]. Moreover, there is wide variation in prescribing to less adequately researched. unwell patients [6]. It is now important to identify ways to Many qualitative studies have explored clinicians’ facilitate (further) optimisation of antibiotic prescribing in views on antibiotic stewardship interventions, but often practices that have remained high-prescribing. as process evaluations within clinical trials [20–24]. Considerable evidence supports various interventions to These identified that general practitioners (GPs) prefer safely reduce antibiotic prescribing for RTIs [7–9]. Among multifaceted interventions which decrease diagnostic them are delayed (back-up, deferred) antibiotic prescrip- uncertainty, help provide patient-centred care and are tions (henceforth DPs) and point-of-care C-Reactive easy to implement [25], and that they experience inter- Protein testing (POC-CRPT) (Table 1). Trial evidence ventions as ‘supportive aids’ but also potentially as a shows that DPs can help safely reduce antibiotic use for compromise, source of distress, or unnecessary [26]. Few acute RTIs, with only 33–39% of patients given DPs using qualitative studies have focussed on implementing DPs antibiotics [10–13]. The National Institute for Health and [27, 28] and POC-CRPT [29–31] in the UK outside of Care Excellence (NICE) recommends considering DPs for trials. One study found prescribers used DPs infre- selected common infections [14, 15]. Similarly, trial quently, mainly to avoid anticipated conflict and because of feeling uncomfortable with burdening patients with Table 1 Definitions of DPs and POC-CRPT and related clinical responsibility, and perceiving DPs as a conflict- guidelines ing message [28]. Another study found DP use was influ- Delayed (also referred to as back-up or deferred) antibiotic pre- enced by: GPs’ prior experiences of using DPs, views on scriptions (DPs) how to protect the doctor-patient relationship, lack of The NICE defines DP as a prescription “given in a way to delay the agreed prescribing strategies within and between prac- use of [the antibiotic], and with advice to only use it if symptoms tices, and lack of feedback on how DP affects antibiotic worsen or don’t improve within a specified time. The prescription may be given during the consultation (which may be a post-dated prescribing data [27]. Studies found the implementation prescription) or left at an agreed location for collection at a later date of POC-CRPT as influenced by: cost/reimbursement, ”. (NICE Glossary) time, effect on workload and flow, access to equipment, NICE guidance recommends considering DPs for: � acute cough in patients with higher risk of complications, physical and operational constraints, quality control and � acute sore throat (with FeverPAIN scores of 2 or more or Centor score training, practitioner attitudes and experiences, local 3–4), champions, and gaps in evidence [29–31]. � acute otitis media (unless systemically very unwell or high risk of complications), This study aimed to explore the views of professionals � sinusitis if there is no improvement for more than 10 days (unless in high-prescribing general practices on use and imple- systemically very unwell or high risk of complications), mentation of DPs and POC-CRPT. In doing so, we build � lower urinary tract infections for non-pregnant women. (Summary of antimicrobial prescribing guidance – managing common on, and extend, previous studies by identifying how these infections; updated in March 2020, available on: https://www.nice.org. two strategies could be implemented to optimise antibi- uk/Media/Default/About/what-we-do/NICE-guidance/antimicrobial%2 otics in the ‘real world’ outside clinical trials and in prac- 0guidance/summary-antimicrobial-prescribing-guidance.pdf) tices that remain high-prescribing despite other initiatives Point-of-care C-Reactive Protein Testing (POC-CRPT) used to reduce prescribing (e.g. national data monitoring C-reactive protein (CRP) is a marker of inflammation that increases 4– and targets). We also specifically sought to explore views 6 h after the onset of inflammation or acute tissue injury and peaks at and suggestions to guide implementation and uptake of 36–90 h (1.5–4 days). Various point-of-care CRP tests are available that require a small blood sample from a finger prick and that produce a both strategies for commissioners, practices and/or clini- quantitative or semi-quantitative result within approx. 3 to 10 min. cians who may be considering using them. NICE clinical guideline [CG191] supports the use of POC-CRPT to help differentiate a serious infection from a self-limiting RTI in adults with acute cough (lower RTI) when, after clinical assessment, a diagnosis of Methods pneumonia has not been made. It suggests interpreting POC-CRPT re- Participants sults as follows: We identified general practices which were in the top � CRP < 20 mg/l: no routine antibiotic � CRP between 20 and 100 mg/l: delayed/back-up antibiotic 20% for antibiotic prescribing in the West Midlands � CRP > 100 mg/l: immediate antibiotic. Clinical Research Network (CRN), based on 2017 Borek et al. BMC Family Practice (2021) 22:25 Page 3 of 11 PrescQIPP data (antibiotic items per STAR-PU (Specific Data analysis Therapeutic group Age-sex Related Prescribing Unit)) Data were analysed inductively using thematic analysis [32]. We used the antibiotic items per STAR-PU as it is [33] with coding in NVivo software (v.12). We used the- commonly used in England to compare antibiotic pre- matic analysis because it is a systematic qualitative data scribing across practices and against prescribing targets. analysis method, suitable for applied health research, Study invitations were sent to 139 practices and then and allows the analysis to be driven by the data (by followed-up by email and/or phone. Additionally, the inductive coding) as well as the development of interpre- study was promoted by CRN Facilitators. Interested tations (themes) that extend understanding beyond just practices were asked to identify suitable date(s) for a a summary of data. Initially four researchers (AB, AC, focus group with at least three professionals (comprising STC, ED) coded the same 2–3 transcripts, discussed at least two prescribers and any other clinical or admin- coding and categories for the initial codes, and agreed istrative staff). Participants gave written consent at the on a coding framework. The coding framework was then start of focus groups. Practices were offered £500 reim- used by AC and AB to code all remaining transcripts bursement for one focus group. independently, adding new codes when needed, and then combining their analyses. Themes were identified, dis- cussed and agreed with a multidisciplinary team (AB, Data collection AC, STC, MM, ED), and then reviewed by the wider study We collected data through focus groups in participating team (including GPs, epidemiologists and behavioural practices to facilitate discussions among professionals economists). and elicit shared as well as divergent views on the use of the antibiotic optimisation strategies and practice-level Results implementation (rather than only individual use). Focus Nine practices participated, including 50 professionals groups took place in general practices between Decem- (3–11 per practice) (Table 2). Focus groups lasted 49–87 ber 2018 and April 2019. They were facilitated by two (mean 71) minutes. No practice had used POC-CRPT, researchers (AB, AC) – each leading a part of the focus although two (FG2, FG3) had the equipment. Four main group, while the other made notes. Discussions followed themes were identified; additional quotes are available in a semi-structured topic guide (see Additional file 1) Additional File 2. which was piloted with three GPs. The topics included: making antibiotic prescribing decisions, experiences of Compatibility of strategies with clinical role and using DPs, views on POC-CRPT (with three types of experience tests shown to prompt discussion), practice communica- Participants’ views on DPs and POC-CRPT were influ- tion and other antibiotic stewardship strategies used. As enced by their perceptions on how these strategies fit DPs are used by prescribers (although variably), we ex- with their clinical role and experience. They reported plored participants’ experiences; as POC-CRPT is rarely how the core clinical role in general practice (developed available in UK practices, we explored views about hypo- through training and experience) involved clinical thetical use. Focus groups were audio-recorded and assessment based on history-taking, examination and transcribed verbatim. Transcripts were anonymised, social factors. The clinical assessment could be also checked for accuracy with audio-recordings, and informed by, but prioritised over, clinical scores (e.g. speakers’ professional roles were added based on notes. Centor, FeverPAIN) and diagnostic tests. Table 2 Practice characteristics a b Focus group Urban / rural Deprivation (decile) FG participants FG1 Rural (village) Medium (5) 2 GPs, Nurse, HCA, Practice Manager FG2 Rural (town and fringe) Medium (5) GP, Pharmacist Prescriber, Business Partner FG3 Urban (major conurbation) High (2) 2 GPs, Prescribing Clerk, Practice Manager FG4 Rural (town and fringe) Medium (4) 2 GPs, Nurse, Practice Manager FG5 Rural (town and fringe) Low (7) 3 GPs, 2 GP Trainees, Nurse Prescriber, Practice Manager FG6 Urban (major conurbation) High (3) 4 GPs, Medicines Coordinator FG7 Urban (major conurbation) High (2) 3 GPs, Nurse FG8 Urban (major conurbation) High (2) 6 GPs, 1 GP Trainee, 2 Nurses, Practice Manager, Deputy Practice Manager FG9 Urban (major conurbation) High (1) 2 GPs, 2 GP Trainees, HCA, 2 Receptionists a b Index of multiple deprivation decile. GP – General Practitioner, HCA – Healthcare Assistant (non-prescriber), Nurse – Practice Nurse (non-prescriber) Borek et al. BMC Family Practice (2021) 22:25 Page 4 of 11 DPs and POC-CRPT were described as fitting with the GP1: I think [GP trainees would] test everybody… clinical role and useful when there is clinical uncertainty Because you give them any equipment and they use over diagnosis or prognosis, such that DPs could provide it religiously… they don’t look at the patient… a safety-net and POC-CRPT additional clinical informa- tion. Such uncertainty was described as quite rare, GP2: I think it would probably make them less though this depended on the experience of the clinical. prescriber. GP1: They’re so reliant now on the machines and When I use a deferred script it’s normally because I the templates… tick, tick, tick, do the test and then feel it’s a bit more of a borderline case… a patient treat. You haven’t actually looked at your patient where you’re not entirely sure and so it’s there for yet. [FG3] the patient if they worsen… [GP, FG2] Strategies used as social tools to negotiate treatment and Those people that are right on the fence, where educate patients you’re uhming and ahhing… it’s quite rare for a doc- Participants frequently described (perceived) patient tor not to know what type of infection you’ve got. expectations for antibiotics as a driver for unnecessary [GP, FG4] antibiotic use; some described reducing antibiotic pre- scriptions as beyond their control. GPs described their roles as ‘holistically’‘treating patients, not numbers’ [FG1] and that POC-CRPT would Antimicrobial resistance is beyond the surgery’s con- unlikely add much to, or change, their clinical judgment trol a lot of the time because it is patient expecta- if not uncertain. In contrast with secondary care, partici- tions (…) the patient insists and insists and that’s pants highlighted that diagnostic testing was not routine not the clinician’s fault that antibiotics are pre- in general practice. scribed in the end. [GP, FG2] A lot of your training in primary care is diagnos- They discussed using DPs and POC-CRPT as social tools ing patients without test interpretation. If you go to negotiate treatment with patients perceived as difficult into hospital, you get a battery of tests (…)It to reassure when not needing antibiotics (‘regular makes you more reliant on test results… Then the returners’ [FG6], ‘frequent offenders’ [FG8]). Most GPs more of these things are used I think maybe it reported using DPs as a compromise when they consid- does somehow take away from the clinicians… ered antibiotics unnecessary but felt that patients wanted [Manager: Art.] Yes, it may take [away] some of antibiotics; a GP trainee [FG5] described how with your clinical judgement. [GP, FG2] increasedexperienceheusedDPs less as a safety-net and more often as a compromise. Participants also envisaged Clinical experience seemed to influence perceptions of using POC-CRPT as ‘evidence’ to convince patients when usefulness of DPs and POC-CRPT. Some GP trainees re- antibiotics are unnecessary and ‘deny patients antibiotics… ported using DPs more (one accounted it to lower confi- more than deciding on antibiotics’ [GP, FG9]. Both strat- dence in clinical decisions); with more experienced GPs egies were seen as helping avoid lengthy negotiations, reporting using DPs less frequently, preferring immediate conflict, complaints and re-consultations; and helping or no prescription. GPs and nurses described POC-CRPT maintain good relationships, patient satisfaction and more as likely to be used more by trainees, and GPs perceived patient-centeredness (‘equal footing within the consult- POC-CRPT as more helpful for nurses and pharmacists ation’ [FG7]). They were also seen as strategies to educate who may rely more on test results to reduce clinical un- patients that antibiotics are unnecessary. certainty. More experienced clinicians described feeling more confident using their clinical judgment irrespective GP1: I tend to use [DP] in the people you just cannot of tests. They were concerned that dependence on POC- convince that they don’t need antibiotics. (…) some- CRPT by trainees might lead to loss of clinical skills. times it’s just the route of least resistance… It’s difficult at the start of training in that you’ve not GP2: …you’re using it as a trade-off… saying, ‘come got that much experience and (…) you’re more wor- on, give my way a bit of a chance, let’s see how it ried about making a mistake. I probably had a big- goes’… andiftheninafewdaysthey’re starting to ger range of ones that were in the middle and (…) feel a little bit better, they say, ‘okay, we’re on the felt more comfortable having that safety-net [of DPs]. right track’,and that’s when they don’tcome infor [GP Trainee, FG5] the antibiotics. (…) I suppose it leads to improved Borek et al. BMC Family Practice (2021) 22:25 Page 5 of 11 patient satisfaction, because they feel they’re not Table 3 Using ‘social tools’ to help address perceived patient expectations being fobbed off… it’s the key to not getting com- plaints. [FG4] � Perceived that patients expect to leave ‘with something’– use of prescriptions and leaflets I have a very simple rule… They’ve made the effort to come and see Participants described patients as expecting a pre- a doctor, give them a bit of advice, or even a prescription or a form scription and preferring tests and numbers, and for physio or something like that, it’s the key to not getting some reported already using clinical scores or tests complaints. Everybody gets a prize, even if it’s just a bit of written paper. [GP, FG4] to negotiate treatment decisions (Table 3). Others felt that patients were accepting of no-antibiotic I like to print out a post-dated prescription because actually giving them something in their hand to go away with gives them a sense decisions and reassurance with effective communica- that something’s happening. [GP, FG6] tion. Participants were also concerned that using …patients are used to have something to take away with them, so POC-CRPT may have unintended consequences, when they come they need something... whether it is a such as unexpectedly high test results, raising prescription... Sometimes what may help is on EMIS you’ve got patients’ expectations for tests and ‘medicalising’ patient information leaflets…[GP, FG7] common infections. They tend to like to leave with something and if it’s not antibiotics and not what they want, they seem to want to leave with some form of prescription be it an over the counter medicine or be it It’s funny, the amount of times that you’re advised to something else... I’m seeing more requests for things like nasal sprays treat the patient not the number, the patient will be and linctus… [GP, FG9] much happier with the number than your clinical � Perceived that patients want tests and numbers – use of POC judgement. [GP, FG2] tests It’s funny, the amount of times that you’re advised to treat the Nurse: Here it’s a small population and it’ll get patient not the number, the patient will be much happier with the number than your clinical judgement. [GP, FG2] around the patients and they’ll say, ‘well why did I could also use [POC-CRPT] on these frequent offenders who come they have that test and I didn’t’? in saying ‘I want antibiotics’… if you show them it’s not this and it’s not 100 and that convinces them in some ways psychologically not GP: Yeah… so then you’ll end up having to do it. to get the antibiotic. [GP, FG8] [FG4] A really good thing is to have a tool to demonstrate to patients why they don’t need antibiotics. I use my SATS probe quite a lot as a... it’s not really a tool but it helps me, I’ll kind of say ‘Well your oxygen saturations are very good.’ Which is why I’m very interested in testing Ambiguities about usefulness and impact of strategies CRP ‘cause I think that’s a really good evidence based tool, which if Participants considered pros and cons of DPs and patients understand, are going to be more receptive and accepting of your decision not to give them antibiotics, if you can actually POC-CRPT, and situations and patients when these demonstrate numerically that there’s no reason to. [GP, FG6] strategies should or should not be used, with appar- …like urine samples, they come in for urine symptoms when you ent ambiguity and contradictions. DPs were seen as think ‘This is not’– and then you dip it and say ‘Look, there’s none.’ helping relieve patients’ anxiety by improving access But that’s cheap… [GP, FG6] to antibiotics (e.g., before weekends) while reducing If you got a printout, you can give them a copy, it’s a prize, they’ve the need to re-consult. Some prescribers reported had a test… They think tests are how we do medicine, and they’re not…‘oh, I need a test, I need a scan’. [GP, FG4] using DPs for adults and children with RTIs and patients with additional risks (e.g. immuno- � Perceived that patients need ‘evidence’– use of clinical scores compromised); in contrast, others (sometimes the I use the FeverPAIN to not give them antibiotics because it’s just – same participants) reported not using DPs for adults it’s helpful to be like ‘well the computer says you don’t need them!’ And sometimes that works [laughter] better than ‘the doctor with RTIs (preferring to either prescribe or not), says you don’t need them!’…it does unfortunately bite me in the children (preferring to re-consult) or at-risk patients bottom sometimes when they come back again and say: ‘well what (preferring to prescribe or re-consult). does your score say?’ And it comes out saying ‘you need a delayed prescription!’ So they go away with a delayed prescription when probably clinically I wouldn’t have given them anything at all. [GP, If it’s for a child, then I’d rather review them. If you FG3] have a compromised patient or a diabetic patient, Sometimes what can help in sore throat is the Centor or the then I might issue the script because I know they are FeverPAIN, so you can actually show them the scoring criteria and say, ‘X, Y and Z, because you haven’t got any of those criteria, at a higher risk so it all depends. It’s not a fixed evidence shows us that it’s very unlikely that this is bacterial and this thing. It just depends on the individual. [GP, FG8] is in fact viral.’ [GP, FG7] Some participants reported using DPs with ‘sensible’ patients – those they perceived to ‘understand the use of antibiotics’ [FG8] and ‘on board with [DP]’ [FG6] Borek et al. BMC Family Practice (2021) 22:25 Page 6 of 11 (Table 4). Although no participant described patients as exacerbations. Some participants questioned the useful- ‘insensible’, some reported concerns about potential ness of CRP as a biological marker and the sensitivity intentional or unintentional misuse (i.e. they or others and specificity of tests. They were uncertain about inter- using the antibiotics immediately or in the future with- preting the results (particularly medium values) and how out consulting). For these patients, they reported being to act on results inconsistent with clinical judgment. more likely to add a ‘second step (…) [or] any slight im- pediment in their way [so] they won’t use it if they don’t I want to know what’s the evidence? What kind of need to’ [FG4] or ‘an extra layer of awkwardness’ [FG5], infections have they looked at? How do they know if for example, by leaving the prescription at reception to it’s viral or bacterial? I don’t really know. CRP is so be collected in a few days or post-dating it. non-specific… [GP, FG6] Participants were unclear about the effectiveness of DPs on reducing inappropriate antibiotic use; some ex- Participants had mixed views about the effectiveness of pected DPs to reduce antibiotic use, others thought they POC-CRPT on antibiotic prescribing. Some envisaged may increase it (i.e. when used instead of not prescrib- limited impact as they expected it not to change clinical ing). Participants were also uncertain if DPs count to- decisions, while some thought it may increase prescrib- wards prescribing rates if unused. Practices had no set ing due to perceived pressure to act on unexpectedly ways of issuing DPs and prescribers discussed with inter- raised test results. Nevertheless, most expressed interest est what their colleagues did. Prescribers reported in trying POC-CRPT, and generally thought that it could choosing DP formats to facilitate ease of antibiotic ac- reduce prescribing associated with perceived patient cess if it was helpful (e.g., giving verbal advice to wait pressure. when handing a prescription before a weekend/travel) with patients whom they trusted to use DPs appropri- I would worry that by doing [POC-CRPT] and then ately. Conversely, they reported choosing DP formats getting a result that I wasn’t necessarily expecting, I that deterred patients from using the antibiotic immedi- would then feel obliged to prescribe something ately (e.g., by post-dating) when they doubted that pa- because otherwise I’m not acting on an abnormal tients would use DPs appropriately. result. [GP, FG1] The biggest disadvantage is that unless it’s post- If I want to prescribe, I don’t think I’d even do the dated, a proportion of people will go and cash it. test. [GP, FG3] That’s what they wanted. [GP, FG5] Influence of context on use of strategies Ambiguity about when and how POC-CRPT should be Context, including practice characteristics and situ- used was also apparent. Some participants considered ational factors, influenced care and use of both strategies whether they could use it when deciding about hospital (for summary see Table S1 in Additional File 3). High admission; to monitor recovery over time; to screen and prescribing was felt to be partially a result of practice/ triage patients and for patients with COPD staff characteristics (e.g. more locums/trainees and staff turnover) and patient characteristics (e.g. comorbidities, culture/languages, deprivation). Table 4 Participants reporting using DP with ‘sensible’ patients Practice context influenced whether and how DPs I only give delayed antibiotics if I feel like the patient or the patient’s were used. Prescribers from practices with ‘good access’ parent is very sensible and on board with it. [GP, FG6] (where patients could get appointments quickly), tele- Generally [DP] is for chest complaints that I would issue it, or if they’ve phone triage and other available services (e.g., extended had recurrent tonsillitis that has required antibiotics that it’s been access) preferred to re-consult rather than give DPs. Pre- appropriate for and they’re starting to become unwell and you’ve got a sensible family, then I might do it then as well… [GP, FG7] scribers from rural practices preferred to give DPs, or provide antibiotics from the on-site dispensary, with [DP] would be useful for patients who understand the use of advice to delay taking antibiotics to minimise patients’ antibiotics, who are bit more sensible but not for everybody I would say, considering we’ve got some population who doesn’t burden of returning to the practice. understand when to use it. Some population groups in this practice who don’t understand when to use antibiotics so they’ll still be feeling I don’t think we do very many delayed scripts at all okay and will still get antibiotics and take it because they are used to that. [GP, FG8] because of the way we work, because of the easy access and the dispensary. [GP, FG1] I also probably gauge which ones I think are more likely to be sensible hopefully. [Patient’s father] said ‘Yes, I think that sounds reasonable’. He seemed a bit reassured about that. Let’s see how she Moreover, DPs were described as used less in practices goes in the next few days. [GP trainee, FG9] in areas with higher deprivation and patients from Borek et al. BMC Family Practice (2021) 22:25 Page 7 of 11 certain cultures or non-English speakers (perceived as ‘sensible’ patients, often choosing the format of DP to less likely to use DPs appropriately). The desire to avoid make things easier for patients they trusted or create additional workload for the administrative staff and barriers for patients they perceived to expect antibiotics potential conflict with patients made prescribers less but who did not require them. Participants also reported likely to ask patients to collect DPs from the practice mixed views and doubts about the perceived impact of reception. DP and POC-CRPT on antibiotic prescribing/use in the Participants raised many practical challenges with real world, outside of trial settings. Participants dis- implementing POC-CRPT, particularly around time, cussed many contextual and practical issues with imple- logistics and cost. GPs considered consultations too menting DPs and POC-CRPT. There was a prevalent short for POC-CRPT and envisaged asking nurses or sense of ambiguity and mixed views about the strategies: healthcare assistants to perform the tests. Some con- how they fit in general practice; when and how they sidered triaging patients with the tests before their should be used; and to what extent the benefits outweigh appointment. Participants discussed training and barriers to implementation. logistical difficulties in storing and maintaining equip- ment – difficulties they envisaged would disrupt Strengths and limitations workflows, add workload, and require carefully de- We recruited a high number of participants from a vised implementation protocols. relatively diverse range of practices and the nine focusgroupsprovideduswith rich datatoanswer Because it’s so ad-hoc it would be quite difficult for our research question and develop the reported you to know when you’ve got patients and you want themes and findings. The quality of data collection to do it and how you’re going to fit it in… in amongst and analysis was strengthened by involving multiple other patients that you’re already seeing, it could be experienced qualitative researchers and discussions quite tricky. [Nurse, FG4] with a multidisciplinary team. The analysis was data- driven and data saturation was achieved, with mul- Participants reported limited ability for practices to fund tiple quotesacrossall focusgroupssupportingthe POC-CRPT, seeing additional commissioners’ or govern- findings (see also Additional File 2). The study was ment funding as necessary for adoption. Some described reported following relevant standards (with the how wider contextual influences drove the uptake of reporting checklist and additional details in POC-CRPT, such as needing to ‘keep up’ with other Additional File 3)[34]. practices and countries adopting POC-CRPT, and Transferability of the findings may be limited as we expecting to be increasingly required to use POC-CRPT included high antibiotic prescribing practices from one as evidence for prescribing audits and medico-legal area in England and some practices had reduced their reasons. prescribing rate before the focus group. We used the antibiotic items per STAR-PU as a measure to identify …we’d use it because if everyone else is doing it… high prescribing practices that may particularly benefit and you’re the only one and something goes wrong, from strategies to support optimising their antibiotic then it’s indefensible… In a court of law they’ll say, prescribing. High antibiotics/STAR-PU may suggest “well everyone else in the patch is using it, why don’t some suboptimal prescribing but it does not take into you use it”? “Because I don’t need to”. “I know, but consideration potential valid reasons for high prescribing in this case you were wrong…” What are you going rates such as those practices with high numbers of to say then? [GP, FG4] patients with co-morbidities [5]. In our study, we did not explore in more detail the (in)appropriateness of Discussion antibiotic prescribing and only used the antibiotics/ Participants reported mixed views about whether or not STAR-PU as a proxy to identify practices that may have each strategy would be useful and in what circum- more scope for and benefit from implementing stances. Overall, they perceived the strategies to be of additional strategies to optimise antibiotics. While focus limited value as ‘clinical tools’, helpful only in ‘rare’ situ- groups allowed participants to discuss and address dif- ations of clinical uncertainty and for less experienced ferent views and experiences, the presence of colleagues prescribers. By contrast, both strategies were seen as with different roles might have influenced what individ- helpful ‘social tools’ to negotiate treatment while main- uals shared and led to a dominance of GPs’ views (who taining relationships or educating patients that antibi- tended to speak more). As the practices had not used otics may not be necessary, especially for patients POC-CRPT, participants’ views were hypothetical and perceived to expect antibiotics. However, many pre- might differ from actual experiences of using POC- scribers described DPs as a strategy to be used only with CRPT as evidenced previously [23, 24, 35]. Borek et al. BMC Family Practice (2021) 22:25 Page 8 of 11 Comparison with existing literature expecting antibiotics, likely to use DPs inappropriately, Similar to existing literature, both strategies were seen and that DPs are suitable only for selective (‘sensible’) as ‘clinical tools’ to help manage clinical uncertainty, patients [27, 28, 36, 40, 41], and that patients are con- especially for those still developing clinical skills/experi- vinced by tests and numbers. Contrary to their own res- ence: DPs were used to safety-net instead of re- ervations about POC-CRPT, GPs described stressing the consulting [27, 28, 36] and POC-CRPT to help assess ill- certainty of POC-CRPT to patients. Despite the impact ness severity and whether antibiotics are needed [23, 24, of clinicians’ perceptions of patient expectations on pre- 29, 30, 35, 37–39]. However, we found that clinical scribing, studies show that these perceptions tend to be uncertainty about RTIs among experienced clinicians overestimated or misjudged [43–45]. Moreover, evidence was seen as relatively ‘rare’. This resonates with existing shows that effective communication skills can help literature, with RTI consultations described as ‘simple’ understand and address patient concerns and expecta- [28]. Other types of uncertainty were apparent. For tions, maintain good relationships, and educate patients POC-CRPT, this was not only regarding the quality of about infections and antibiotics, and may be more sus- tests, but also how results should be interpreted and the tainable long-term [17, 46, 47]. perceived pressure to act on results inconsistent with clinical judgement [29, 30, 39] – which were seen to po- Implications tentially threaten a prescriber’s clinical role and skills. The Covid-19 pandemic has brought forth new uncer- For DP, other types of uncertainty were regarding how tainties and challenges for healthcare systems across the patients may use them [28, 36, 40] and how useful DP world [48, 49], including for prescribers in primary care. was as a strategy to reduce inappropriate antibiotic use. Mitigating the spread of antimicrobial resistance by Despite clinical guidelines, participants were unclear and more prudent antibiotic use is an even greater public had mixed views about when these strategies were clin- health priority for pandemic response and preparedness. ically suitable. In all, the use of these strategies as ‘clin- A first step in managing the new uncertainties around ical tools’ in high-prescribing practices was viewed as Covid-19 is to identify which uncertainties are already limited. This compares with previous studies which ‘known’ and to minimize these where possible [49]. found that GPs from low-prescribing practices perceived However, many policies tend to advocate use of DPs DPs as more useful as a safety-net than GPs from high- and POC-CRPT to only reduce clinical uncertainty. Based prescribing practices whose use of DP was instead more on our study findings, this approach lacks sufficient atten- influenced by social/patient factors [27, 40]. Importantly, tion to other types of uncertainties and ambiguities rele- it differs in showing that simply providing POC-CRPT vant to prescribers. It also does not acknowledge nor equipment or guidelines for use of DPs or POC-CRPT advise how these strategies may or may not be used as to address ‘clinical uncertainty’ may be insufficient to ‘social tools’ in practice. High-prescribing practices may optimise antibiotic prescribing and prescribers in high- benefit from implementing DPs and POC-CRPT but prac- prescribing practices may need to challenge their current tice staff would first need to be clearer on the benefit of ‘confidence’ about prescribing. these strategies, in what contexts/situations, and how they Participants seemed more convinced about the useful- would fit with practice. Presenting clinical trial evidence ness of both strategies as ‘social tools’, especially with alone is insufficient to motivate intervention adoption. patients perceived as expecting antibiotics. Counter to Moreover, it is currently unclear how transferrable the guidance, previous studies also describe clinicians using trial evidence is to routine practice in terms of implemen- DPs as a compromise – to maintain relationships, avoid tation as well as effectiveness of these strategies outside of conflict and complaints [27, 28, 40, 41], and to educate research contexts. Evaluating these strategies in the ‘real patients that antibiotics are not always necessary [10, 27, world’ of (high-prescribing) practices would provide a bet- 41, 42], especially in high-prescribing practices [27]; and ter understanding of whether, when and how these strat- POC-CRPT to convince and reassure patients of no egies might be useful. need for antibiotics [24, 29, 30, 35, 37–39]. Our partici- Despite the uncertainties, ambiguities and doubts pants contrasted unnecessary antibiotic prescribing about these strategies, our participants also perceived which resulted from perceived patient expectations with them as potentially helpful in certain contexts and situa- high antibiotic prescribing arising from contextual fac- tions. As antibiotic prescribing and use are complex tors including patient characteristics and staff/patient behaviours influenced by various determinants, it is turnover. As ‘social tools’, DPs and POC-CRPT were unlikely that one or two strategies would ‘solve’ the perceived as particularly helpful in high-prescribing issue. While DPs and POC-CRPT may be insufficient as practices with higher patient expectations and need for stand-alone strategies, they might be useful in addition antibiotics. Some participants displayed a paternalistic to other strategies (e.g. audit and feedback, communica- approach and described their patients as mostly tion skills), or more acceptable to clinicians and/or Borek et al. BMC Family Practice (2021) 22:25 Page 9 of 11 patients than some strategies (e.g. a no-antibiotic strat- Koen B. Pouwels, Julie V. Robotham, Laurence S. J. Roope, Sarah Tonkin- Crine, Ann Sarah Walker, Sarah Wordsworth, Carla Wright, Sara Yadav, Anna egy). To support implementation, research should focus Zalevski. on developing and testing implementation strategies; specifically, develop evidence on optimal approaches to Authors’ contributions AB contributed to the design of the protocol, conducted interviews, implementation; training in when and how to use DPs conducted the analysis, and was a major contributor to writing the and POC-CRPT and how to effectively discuss strategies manuscript through critical review, commentary and revision. AC contributed with patients; and investigate (intended and unintended) to the design of the protocol, conducted interviews, conducted the analysis, and was a major contributor to writing the manuscript through critical consequences of using these strategies routinely in high- review, commentary and revision. ED conducted analysis. CCB obtained prescribing practices. Similarly, commissioners and prac- funding and led the study throughout to achieve goals. He supervised the tices/clinicians wanting to increase the use of these strat- research team conducting the study. AH obtained funding and led the study throughout to achieve goals. She supervised the research team conducting egies need to address the perceived ambiguities about the study. MM obtained funding, critically reviewed the manuscript, and led DPs and POC-CRPT and practical challenges; for the study throughout to achieve goals. He supervised the research team example, disseminate relevant evidence and guidelines; conducting the study. ASW obtained funding and led the study throughout to achieve goals. She supervised the research team conducting the study. fund POC-CRPT equipment; help problem-solve prac- MMc conceived the study, contributed to the design of the protocol, tical challenges to use; provide feedback on how patients supported the analysis, and was a major contributor to writing the use DPs; and develop practice-specific protocols for manuscript through critical review, commentary and revision, obtained funding, and led the study throughout to achieve goals. STC conceived the using these strategies consistently. study, contributed to the design of the protocol, conducted the analysis, and was a major contributor to writing the manuscript through critical review, commentary and revision, obtained funding, and led the study throughout Conclusions to achieve goals. All authors read and approved the manuscript. In conclusion, our findings extend current knowledge regarding how DPs and POC-CRPT are used as ‘clinical Funding tools’ or ‘social tools’ in UK/English general practice The study was funded by the Economic and Social Research Council (ESRC) through the Antimicrobial Resistance Cross Council Initiative supported by and in other countries [23, 24, 35, 36, 38–41]. They the seven research councils in partnership with other funders (grant highlight the ambiguities and complexities which teams reference: ES/P008232/1) and supported by the National Institute for Health in high-prescribing practices consider when thinking Research (NIHR) Health Protection Research Unit (HPRU) in Healthcare Associated Infections and Antimicrobial Resistance in partnership with Public about implementing these strategies and their impact Health England [HPRU-2012-10041], and the NIHR Oxford Biomedical on antibiotic prescribing/use. Most notably, they Research Centre. ASW and CCB are NIHR Senior Investigators. The support of explain why high-prescribing practices may not value the funders is gratefully acknowledged. The funding bodies played no role in the design of the study and collection, such strategies as ‘clinical tools’ and thus have import- analysis, and interpretation of data, and in writing the manuscript. The views ant implications for policy advocating for all prescribing expressed are those of the authors and not necessarily those of the NHS, the to be based on testing [50]. NIHR, the Department of Health and Social Care or Public Health England. Availability of data and materials Supplementary Information The dataset analysed during this study is available from the corresponding The online version contains supplementary material available at https://doi. author on reasonable request. org/10.1186/s12875-021-01371-6. Ethics approval and consent to participate The University of Oxford research ethics committee (ref. R59812) and NHS Additional file 1: Focus group topic guide Health Research Authority (ref. 19/HRA/0434) approved the study. All Additional file 2: Additional quotes supporting the findings participants provided written informed consent for participation in the study. Additional file 3: Summary of views on contextual influences on DP and POC-CRPT Consent for publication Additional file 4: Reporting checklist Not applicable. Competing interests Abbreviations The authors declare that they have no competing interests. COPD: Chronic obstructive pulmonary disease; CRN: Clinical research network; CRP: C-reactive protein; DPs: Delayed antibiotic prescriptions; Author details GP: General practitioner; HCA: Healthcare assistant; NICE: National Institute for Nuffield Department of Primary Care Health Sciences, University of Oxford, Health and Care Excellence; POC-CRPT: Point-of-care C-reactive protein test- Radcliffe Observatory Quarter, Woodstock Road, Oxford OX2 6GG, UK. ing; RTIs: Respiratory tract infections; STAR-PU: Specific therapeutic group National Institute for Health Research (NIHR) Health Protection Research age-sex related prescribing unit; UK: United Kingdom Unit in Healthcare Associated Infections and Antimicrobial Resistance, Imperial College London, London, UK. Primary Care Population Sciences and Acknowledgements Medical Education, Faculty of Medicine, University of Southampton, We thank the general practice professionals for participating in the study. We Southampton, UK. NIHR Health Protection Research Unit in Healthcare also acknowledge, and thank for, the support with recruitment of the Associated Infections and Antimicrobial Resistance, University of Oxford, 5 6 National Institute for Health Research Clinical Research Network. Oxford, UK. NIHR Oxford Biomedical Research Centre, Oxford, UK. Nuffield This paper is part of the work of the STEP-UP study team comprising: Philip Department of Medicine, University of Oxford, Oxford, UK. Centre for E. Anyanwu, Aleksandra J. Borek, Nicole Bright, James Buchanan, Christopher Medication Safety and Service Quality, Pharmacy Department, Imperial C. Butler, Anne Campbell, Ceire Costelloe, Benedict Hayhoe, Alison Holmes, College Healthcare NHS Trust, London, UK. NIHR Imperial Patient Safety Susan Hopkins, Azeem Majeed, Monsey Mcleod, Michael Moore, Liz Morrell, Translational Research Centre, Imperial College London, London, UK. Borek et al. 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