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The University of Manchester Research Factors associated with antibiotic prescribing for adults with acute conditions: an umbrella review across primary care and a systematic review focusing on primary dental care DOI: 10.1093/jac/dkz152 Document Version Final published version Link to publication record in Manchester Research Explorer Citation for published version (APA): Thompson, W., Tonkin-Crine, S., Pavitt, S. H., McEachan, R. R. C., Douglas, G. V. A., Aggarwal, V. R., & Sandoe, J. A. T. (2019). Factors associated with antibiotic prescribing for adults with acute conditions: an umbrella review across primary care and a systematic review focusing on primary dental care. Journal of Antimicrobial Chemotherapy. https://doi.org/10.1093/jac/dkz152 Published in: Journal of Antimicrobial Chemotherapy Citing this paper Please note that where the full-text provided on Manchester Research Explorer is the Author Accepted Manuscript or Proof version this may differ from the final Published version. If citing, it is advised that you check and use the publisher's definitive version. General rights Copyright and moral rights for the publications made accessible in the Research Explorer are retained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these rights. Takedown policy If you believe that this document breaches copyright please refer to the University of Manchester’s Takedown Procedures [http://man.ac.uk/04Y6Bo] or contact [email protected] providing relevant details, so we can investigate your claim. Download date:23. Aug. 2020

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Page 1: Factors associated with antibiotic prescribing for adults with … · 2020-06-19 · Factors associated with antibiotic prescribing for adults with acute conditions: an umbrella review

The University of Manchester Research

Factors associated with antibiotic prescribing for adultswith acute conditions: an umbrella review across primarycare and a systematic review focusing on primary dentalcareDOI:10.1093/jac/dkz152

Document VersionFinal published version

Link to publication record in Manchester Research Explorer

Citation for published version (APA):Thompson, W., Tonkin-Crine, S., Pavitt, S. H., McEachan, R. R. C., Douglas, G. V. A., Aggarwal, V. R., & Sandoe,J. A. T. (2019). Factors associated with antibiotic prescribing for adults with acute conditions: an umbrella reviewacross primary care and a systematic review focusing on primary dental care. Journal of AntimicrobialChemotherapy. https://doi.org/10.1093/jac/dkz152Published in:Journal of Antimicrobial Chemotherapy

Citing this paperPlease note that where the full-text provided on Manchester Research Explorer is the Author Accepted Manuscriptor Proof version this may differ from the final Published version. If citing, it is advised that you check and use thepublisher's definitive version.

General rightsCopyright and moral rights for the publications made accessible in the Research Explorer are retained by theauthors and/or other copyright owners and it is a condition of accessing publications that users recognise andabide by the legal requirements associated with these rights.

Takedown policyIf you believe that this document breaches copyright please refer to the University of Manchester’s TakedownProcedures [http://man.ac.uk/04Y6Bo] or contact [email protected] providingrelevant details, so we can investigate your claim.

Download date:23. Aug. 2020

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Factors associated with antibiotic prescribing for adults with acuteconditions: an umbrella review across primary care and a

systematic review focusing on primary dental care

W. Thompson 1*, S. Tonkin-Crine 2, S. H. Pavitt1, R. R. C. McEachan3, G. V. A. Douglas1, V. R. Aggarwal1 andJ. A. T. Sandoe4

1University of Leeds, School of Dentistry, Leeds, UK; 2University of Oxford, NIHR Health Protection Research Unit in HealthcareAssociated Infections and Antimicrobial Resistance, Oxford, UK; 3Bradford Institute for Health Research, Bradford Royal Infirmary,

Bradford, UK; 4University of Leeds/Leeds Teaching Hospitals NHS Trust, Leeds, UK

*Corresponding author. E-mail: [email protected] orcid.org/0000-0001-6799-4087

Received 9 January 2019; returned 25 February 2019; revised 14 March 2019; accepted 18 March 2019

Introduction: One way to slow the spread of resistant bacteria is by improved stewardship of antibiotics: usingthem more carefully and reducing the number of prescriptions. With an estimated 7%–10% of antibiotic pre-scriptions globally originating from dental practices and up to 80% prescribed unnecessarily, dentistry has animportant role to play. To support the design of new stewardship interventions through knowledge transfer be-tween contexts, this study aimed to identify factors associated with the decision to prescribe antibiotics to adultspresenting with acute conditions across primary care (including dentistry).

Methods: Two reviews were undertaken: an umbrella review across primary healthcare and a systematic reviewin dentistry. Two authors independently selected and quality assessed the included studies. Factors wereidentified using an inductive thematic approach and mapped to the Theoretical Domains Framework(TDF). Comparisons between dental and other settings were explored. Registration number: PROSPERO_CRD42016037174.

Results: Searches identified 689 publications across primary care and 432 across dental care. Included studies(nine and seven, respectively) were assessed as of variable quality. They covered 46 countries, of which 12 werelow and middle-income countries (LMICs). Across the two reviews, 30 factors were identified, with ‘patient/con-dition characteristics’, ‘patient influence’ and ‘guidelines & information’ the most frequent. Two factors wereunique to dental studies: ‘procedure possible’ and ‘treatment skills’. No factor related only to LMICs.

Conclusions: A comprehensive list of factors associated with antibiotic prescribing to adults with acute condi-tions in primary care settings around the world has been collated and should assist theory-informed design ofnew context-specific stewardship interventions.

Introduction

Use of antibiotics is contributing to the rise in drug-resistant infec-tions.1,2 One way to slow the spread of resistant bacteria is byimproved stewardship of antibiotics: using them more carefullyand reducing the number of prescriptions. Globally, dentists aremajor prescribers of antibiotics, accounting for an estimated 7%–10% of all antibiotic prescriptions.3 Worryingly, some countries,including the USA and Canada, are currently seeing increases indental antibiotic use.3–6 Across NHS England during 2017, 5.2% ofantibiotic prescriptions were from primary dental care.7 Most of

these were systemic drugs prescribed for adult patients presentingat urgent appointments with severe pain and/or acute infection.8,9

Antibiotics are not, however, appropriate for the treatment of painand guidance states that a dental procedure is more usually indi-cated to remove the source of the problem; antibiotics are onlyrequired in the presence of a spreading or systemic infection.10–12

It has been estimated that antibiotics may be prescribed unneces-sarily for as many as 80% of dental patients in the UK.13,14 Dentalantibiotic stewardship interventions are therefore necessary.

VC The Author(s) 2019. Published by Oxford University Press on behalf of the British Society for Antimicrobial Chemotherapy.This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided theoriginal work is properly cited. For commercial re-use, please contact [email protected]

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The behavioural and social sciences are increasingly appreci-ated as fundamental to the development of interventions aimedat improving people’s health and modifying clinician/patientbehaviours.15 Although interventions attempting to change anti-biotic prescribing behaviour are regularly reported in the scientificliterature, largely in hospital and primary medical care settings,few have been explicitly designed using behaviour change the-ory16,17 or tested in primary dental care.18 A more comprehensiveunderstanding of the determinants of antibiotic prescribing behav-iour should improve the effectiveness and sustainability of futureinterventions.19

With antibiotic resistance being a global problem that requiresa global solution, the health research community has turned itsfocus towards understanding specific issues for its emergence andspread in hotspots such as South-East Asia.20,21 An increase ininterest about antibiotic prescribing in these areas has become ap-parent, including from the WHO and a number of low- and middle-income countries (LMICs).20–22 Including international studies inthe review enabled comparisons between factors in different partsof the world.

Prescribing of antibiotics for paediatric patients is particularlyhigh in primary medical care.23 In contrast, NHS England prescrib-ing statistics show 87% of dental antibiotics in 2015/16 were pre-scribed to adults, with most linked to urgent rather than routinedental care.8,9 This study aimed, therefore, to identify the factorsassociated with decisions about whether to prescribe systemicantibiotics for adult patients during urgent appointments/withacute conditions. In order to maximize the opportunity to translateexisting knowledge between primary care settings, first the factorsinfluencing antibiotic prescribing decisions for urgent consultationsin all primary care settings were explored. Owing to the plethora ofstudies relating to antibiotic prescribing across primary medicalcare, an umbrella review (systematic review of systematic reviews)was chosen as an efficient way to identify factors and summarizethe extensive evidence base. Next, a systematic review was under-taken to collate the sparse dental-specific evidence base. Finally,the factors were compared and contrasted between clinical set-tings and between countries (including LMICs) in order to informthe development of future antibiotic stewardship interventions.

Methods

Protocol and research questions

The protocol for this two-part systematic review was registered inPROSPERO CRD42016037174. An umbrella review (also known as a system-atic review of systematic reviews or overview of systematic reviews) wasundertaken to answer the first research question: ‘What is known from pub-lished systematic reviews about the factors associated with the decisionwhether to prescribe systemic antibiotics to adult patients across urgentprimary care?’. A systematic review was undertaken for the second: ‘Whatis known from the published literature about the factors associated withthe decision to prescribe systemic antibiotics to adult patients in urgent pri-mary dental care?’. Primary care was defined as ‘the first point of contact inthe healthcare system . . .. including general practice, community phar-macy, dental and optometry services.’.24 Urgent primary dental careincluded out-of-hours (OOH)/emergency dental services provided in com-munity settings.

Both reviews conformed to the Preferred Reporting Items forSystematic Reviews and Meta-Analyses (PRISMA) statement.25 In addition,

the umbrella review was guided by the Joanna Briggs Institute method-ology for umbrella reviews.26

Search strategiesIn July 2018, five databases were searched from their earliest dates: OvidMEDLINE, Ovid EMBASE, Ovid PsychINFO, Web of Science and the BritishLibrary e-thesis on-line service (EThOS). Separate search strategies and in-clusion/exclusion criteria were developed for each review in collaborationwith an information specialist (Tables S1 and S2, available asSupplementary data at JAC Online). The search strategies used a ‘human’search limit as animal studies were not eligible for the reviews and an‘English language’ limit due to a lack of resources for translation. The refer-ence lists of included studies were manually searched for additional poten-tially relevant studies; other papers were also identified through discussionamong the authors. After performing the full search for each review, titlesand abstracts retrieved from each database were combined in EndNote X7and duplicates were removed. Separate EndNote libraries were used for theumbrella review across primary care and the systematic review in primarydental care.

Study selectionStudies published as original research articles in peer-reviewed journalswere included if they contained factors associated with decisions aboutwhether to prescribe systemic antibiotics for the treatment of adultpatients with acute conditions in non-specialist primary care settings.Studies related to specialist care delivered in primary care settings and/orprimary care services delivered in hospital settings were excluded.

For the umbrella review, a sensitive approach to the search wasemployed: systematic reviews were included if they reported, as a min-imum, factors relating to the provision of care for adults with acute condi-tions in primary care settings. Two authors (W. T. and J. A. T. S.) screened alltitles and abstracts independently for potential relevance. The full texts ofall studies identified as potentially relevant were then assessed for inclusioneligibility independently by the same two authors. Discrepancies or dis-agreements were resolved through discussion.

For the systematic review, a more specific application of the eligibilitycriteria was employed: primary research studies (qualitative, quantitativeand mixed methods) were included only if they reported on the provision ofcare for adults with acute dental conditions (pain and/or infection) in pri-mary dental care settings. Studies that included additional types of care,such as prophylactic use of antibiotics for routine procedures or the provi-sion of care in specialist as well as primary dental care settings, wereexcluded. Case studies were also excluded. Two authors (W. T. and G. V. A.D.) screened all titles and abstracts independently for potential relevance.The full texts of all studies identified as potentially relevant were thenassessed for inclusion eligibility independently by the same two authors.Discrepancies or disagreements were resolved through discussion.

Quality assessmentQuality assessment of the systematic reviews included in the umbrella re-view used the Critical Appraisal Skills Programme (CASP) Checklist forSystematic Reviews (Table S3).27 Two authors (W. T. and J. A. T. S.) inde-pendently quality assessed the studies included in the umbrella review,with discrepancies or disagreements resolved through discussion.

Quality assessment of the primary research studies included in the sys-tematic review of primary dental care used the 16 criteria of the QualityAssessment Tool for Studies with Diverse Design (QATSDD) (Table S4).28

One author (W. T.) quality assessed all of the studies included in the sys-tematic review and another author (V. R. A.) independently assessed .50%(4/7), with discrepancies or disagreements resolved through discussion.

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Analysis and synthesisAll included papers were imported into NVivo 11 as electronic pdf versionsfor thematic coding and synthesis. Thematic synthesis was an inductive, it-erative process that broadly consisted of three stages: (i) free line-by-linecoding of the Results and Discussion sections of the included papers; (ii) or-ganization of these ‘free codes’ into related areas; and (iii) the identification,development and refinement of detailed descriptions of the factors associ-ated with antibiotic prescribing.29 To assist the organization of the freecodes into related areas, they were first grouped according to whether theyrelated to clinician, patient, clinical context or wider social/political context,as this structure was presented in several of the systematic reviewsincluded in the umbrella review across primary care.30–32 To assist the iden-tification, development and refinement of the factors associated with anti-biotic prescribing, the Theoretical Domains Framework (TDF) was used toensure clarity of meaning for each influence on behaviour being character-ized. The TDF is a theory-informed approach to identify determinants of be-haviour and support behaviour change intervention design.33

Given the heterogeneous nature of the included studies, many of thefindings in these studies were irrelevant to the research question; only find-ings of direct relevance to the aims of the umbrella and systematic reviewwere coded.

Synthesis of the studies in the umbrella review acrossprimary careCodes were produced initially for the umbrella review across primary careby two authors (W. T. and J. A. T. S.) working independently; discrepanciesor disagreements were resolved through discussion. To ensure that the fac-tors identified related to the population of interest, identified factors werecross-checked back to the underpinning references within the umbrellareview’s constituent systematic reviews. Codes that were found not to re-late to the specific criteria of this review (e.g. studies only about paediatricpatients, hospital settings or prophylactic prescribing) were excluded fromthe synthesis.

Synthesis of studies in the systematic review of primarydental careThe dental care studies were analysed using the bank of codes producedfrom the umbrella review across primary care by two authors (W. T. and G.V. A. D.) working independently; discrepancies or disagreements wereresolved through discussion. Where necessary, additional codes wereincluded for new factors as they emerged from the dental studies.

Independent checksFollowing completion of synthesis of the umbrella and systematic reviews,a group of authors (W. T., S. H. P., R. R. C. M., G. V. A. D. and J. A. T. S.) and thestudy’s patient and public involvement (PPI) representatives undertook asense check of the full list of identified factors. An independent check of thefactors/definitions and how they mapped to the TDF was then undertakenby S. T.-C. Discrepancies or disagreements were resolved throughdiscussion.

Comparing the factorsThe final stage was to compare and contrast the factors identified betweenthe settings: across primary care versus primary dental care specific; andbetween countries (including UK versus other countries and high-incomecountries versus LMICs).34

Results

Study selection

For the umbrella review across primary care, 689 studies wereidentified for possible inclusion in the review. Of these, nine studiesmet the inclusion criteria and were included in the final synthe-sis.30–32,35–40 Details of the study selection process are shown inFigure 1.

For the systematic review of primary research studies, 432studies were identified for possible inclusion in the review. Of these,seven studies met the inclusion criteria and were included in thefinal synthesis.13,14,41–45 Details of the study selection process areshown in Figure 2.

Study characteristics

Umbrella review: characteristics of the includedsystematic reviews

The characteristics of the nine systematic reviews included in theumbrella review across primary care are described in Table 1.Within these systematic reviews, a total of 98 qualitative andquantitative primary research studies contributed factors relatingto adult patients with acute conditions in primary care settings.Across these 98 studies, the participants were primary care profes-sionals (including doctors, nurses and pharmacists) working in 45countries. Eleven of the countries were LMICs and 26 studies wereundertaken in the UK (Table S5). The studies had a date range of1990–2017.

Systematic review: characteristics of the included primaryresearch studies

The characteristics of the seven studies included in the systematicreview of primary dental care are described in Table 2. The studyparticipants were all dentists working in primary dental care(including OOH dental clinics). Two of the studies took place inLMICs (Turkey and Iran) and the other five were UK studies. Thestudies had a date range of 2000–16.

Overlap between the reviews

None of the seven dental studies of the systematic review wasincluded in any of the nine systematic reviews within the umbrellareview.

Overlap within the systematic reviews of the umbrellareview

Analysis of the overlap between primary research studies withinthe umbrella review’s systematic reviews found that 12/98 studiesappeared in two of the systematic reviews, 5/98 appeared in threeof them and none appeared in more than three (Table S5).

Quality assessment

For the umbrella review, the included systematic reviews weregenerally good quality. All of the CASP criteria were fulfilled (or notapplicable) for seven of the nine. The other two systematic reviewsfailed to show quality assessment of their included studies.

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For the systematic review within primary dental care, quality ofthe included studies was more variable, with QATSDD scores rang-ing from 11 to 39 out of a possible total of 40. General weaknessesacross the studies concerned identification of a theoretical frame-work, sample size, validity of measurement tools and evidence ofuser involvement in study design. Detailed results of these assess-ments are presented in Tables S3 and S4. No papers were excludedbased on these assessments as all included results that were rele-vant to meeting the aims of the systematic review.

Thematic analysis

A total of 30 factors associated with prescribing were identifiedacross both the umbrella review of primary care and the systemat-ic review of primary dental studies. Descriptors of each of thesefactors and how they map to the domains of the TDF are presentedin Table 3. Details of which factors were identified from each re-view are shown in Tables S6 and S7, respectively.

Three factors did not map to the TDF: clinician characteristics,patient/condition characteristics and practice characteristics.Upon inspection it was agreed by the authors that they should beclassed as non-modifiable factors. The most frequently identifiednon-modifiable factor, ‘patient/condition characteristics’, wasfound in all systematic reviews included within the umbrella

review and six out of seven dental studies within the systematicreview.

Identifying potential determinants of behaviour

The 27 factors that mapped to the TDF were classed as potentiallymodifiable determinants of antibiotic prescribing in primary care.Of these, 20 were identified in both reviews; 5 factors were identi-fied only from the umbrella review across primary care and 2 fac-tors only from the systematic review in primary dental care(Table 4). As with previously published systematic reviews aboutantibiotic prescribing, the factors were found to group intoclinician-related, patient-related, clinical context-related andwider social–political context-related.30–32,36

Potentially modifiable factors: across primary care

The ‘patient influence’ factor was found in all of the systematicreviews of the umbrella review (Table 2). As described in Table 1,this included but was not limited to demand for antibiotics and/orthe clinician’s perception of the patient’s desire for them. Five fac-tors were found only in the umbrella review: ‘accountability’, ‘anti-biotic awareness’, ‘antibiotic beliefs’, ‘conflict’ and ‘financialburden’ (Table 4).

Records identified throughdatabase searching

(n= 859)

Additional records identifiedthrough other sources

(n= 1)

Records after duplicates removed(n= 689)

Records screened(n= 689)

Records excluded basedon titles, abstracts or both

(n= 669)

Full-text articles assessedfor eligibility

(n= 20)

Full-text articles excluded (n= 11):

No factors associated with prescribing = 7Not primary care = 3

Not able to access reference = 1

Studies included innarrative synthesis

(n= 9)

Figure 1. PRISMA flow chart detailing selection of the systematic reviews included in the umbrella review of factors associated with the decisionwhether to prescribe systemic antibiotics for adult patients with acute conditions across primary care.

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Potentially modifiable factors: primary dental care

Only ‘guidelines & information’ was found in all of the dental stud-ies (Table 3). Two factors were found only in dental studies: ‘pro-cedure possible’ and ‘treatment skills’.13,42,43 Dentists’ beliefsabout whether it was possible to deliver operative dental proce-dures in accordance with guidelines (due to issues beyond the den-tist’s skill) were identified as important (‘procedure possible’).13,43

Similarly, ‘treatment skills’ to undertake difficult elements of ur-gent dental procedures, such as ‘achieving adequate anaesthesia’and ‘how to lance an abscess when swelling is present’, wereincluded in two of the dental studies.13,42,43 Antibiotics were identi-fied as a way of balancing the ‘competing demands’ of a busy listof patients booked for routine dental care with the addition of un-scheduled patients, sometimes as ‘sit and wait’ due to lack ofavailable appointment slots.13,14,41,43,44

Comparing potentially modifiable factors: betweenprimary care settings including dental care

Twenty factors were found in both the umbrella review across pri-mary care and the systematic review in primary dental care(Table 4). Of these, ‘patient influence’ was the most frequentlyidentified factor, being found in all of the systematic reviews of theumbrella review and six of the seven dental studies of the system-atic review (Table 3).

Communication with patients during urgent appointments,including managing anxious patients and negotiation towards ashared decision, were found to be important to the prescribing de-cision in both dental and wider healthcare settings (‘patient man-agement’).14,32,36,38,43 Clinicians’ fear about the potential foradverse outcomes, including when the patient had reduced accessto medical/dental services (such as when going away on holiday orat weekends/bank holidays) were frequently identified (‘fear aboutoutcome’ and ‘access’).30–32,35,38–41,43 Maintaining a good patient–clinician relationship, including by avoiding conflict, was an import-ant goal shared across primary care and primary dental care,where enduring relationships are central to the model of care pro-vision (‘relationship’).31,35,36,38,39,43

Potentially modifiable factors: comparing countries

‘Accountability’ was the only factor not identified from any of theUK-based studies included within the umbrella review’s systematicreviews.36 It has, however, been reported as important in at leastone recent UK study. When exploring the experience of prescribersin OOH primary care settings, it was found that nurse practitionersfelt greater accountability for their antibiotic prescribing than gen-eral practitioners (GPs).46

Eleven factors were identified from studies involving LMICs; nofactors were identified only from studies undertaken in LMICs(Table 5). Exploring the detail within the factors, however, found

Records identified throughdatabase searching

(n= 790)

Additional records identifiedthrough other sources

(n= 0)

Records after duplicates removed(n= 432)

Records screened(n= 432)

Records excluded based on titles,abstracts or both

(n= 373)

Full-text articles assessedfor eligibility

(n= 59)

Full-text articles excluded (n= 52):

No factors associated with prescribing = 11Included specialist/hospital care = 15Included non-acute conditions = 24

Can’t access reference = 2

Studies included innarrative synthesis

(n= 7)

Figure 2. PRISMA flow chart detailing selection of the primary research studies included in the systematic review of factors associated with the deci-sion whether to prescribe systemic antibiotics for adult patients with acute dental conditions/during urgent primary dental care appointments.

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uen

ces

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icro

bia

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ua

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g.

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ysic

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ents

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ctio

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des

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ors

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uen

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g

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ing

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ysic

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ma

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nd

ia,

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kin

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nd

erst

an

dh

ow

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per

ceiv

e

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rib

ing

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of

pa

tien

tsw

ith

acu

teco

nd

itio

ns

pri

ma

ryca

re5

20

02

–10

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giu

m,F

ran

ce,I

cela

nd

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ther

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ds,

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rwa

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in,U

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ua

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tive

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die

s

Co

nti

nu

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that access to internet-based ‘guidelines & information’ waslower in LMICs compared with high-income countries.38

Furthermore, pharmaceutical industry medical representativeswere identified by several non-UK studies as being an importantsource of ‘guidelines & information’, especially in LMICs wherelocal guidelines were not always available.30,32,35,38 Upon closerexamination of the studies included in the reviews, the medicalrepresentatives most often influenced decisions about what toprescribe; only one of the studies referenced within the umbrellareview’s systematic reviews was about whether to prescribeantibiotics.32,47

The ability to use a prescription more than once was identifiedfrom studies involving LMICs.32,38,48 Further differences betweenUK-based and other studies were found within the ‘healthcarecontext’ factor, including the availability of antibiotics without aprescription.35,42

Discussion

A comprehensive list of potentially modifiable and non-modifiable factors associated with the decision whether to pre-scribe systemic antibiotics for adults with acute conditions inprimary care has been collated. Mapping of the potentially modi-fiable factors to the TDF has provided a resource for those wish-ing to develop new antibiotic stewardship interventionsinformed by behavioural theory. By identifying variation withinnon-modifiable factors between clinical contexts, it providesaddition information to enable targeting of specific interventionsat specific groups. By comparing and contrasting the potentiallymodifiable factors between settings, the results should informthe design of future antibiotic stewardship interventions. Itshould also enable the identification of elements of existing anti-biotic stewardship interventions which could be amenable fortranslation into new settings.

With antibiotic resistance recognized as an important elem-ent of global sustainable development, a strength of this study isits inclusion of international studies, including studies fromLMICs.21,49 Most of the sparse dental literature base (five out ofseven studies) originated in the UK (Table 2). This pattern wasalso identified in a systematic review of dental antibiotic stew-ardship interventions, where all five of the intervention tests ingeneral dental practices were UK based.18 Researchers planningto implement existing dental antibiotic stewardship interven-tions in other countries (or to develop new ones) should first seekto understand which factors are relevant to the prescribers’ deci-sions in their specific context.

Owing to the heterogeneous nature of the included studies,attribution of causality between the factors found to be associ-ated with antibiotic prescribing and actual prescribing rates wasnot possible. Similarly, it was not possible to say whether factorsidentified from the umbrella review across primary care but notidentified in the systematic review of dental studies were rele-vant in dental settings; it could only be concluded that these fac-tors were not found in the published dental studies within thisreview. Although the 30 factors identified have been presentedas distinct, many are interlinked, such as the relationships be-tween ‘patient satisfaction’, ‘conflict’ and ‘incentives’. There wasa risk of the factors being either too generic to be useful or toospecific (and hence too numerous) to be manageable. ToTa

ble

1.

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nti

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uen

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ece,

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ng

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ha

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Tab

le2

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ha

ract

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tics

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r(l

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fect

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rib

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ey5

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ded

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fect

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no

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ear

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est

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ich

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act

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era

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ga

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ate

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ent

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lar

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tal

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tics

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ner

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tic

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.

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Tab

le3

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cto

rsa

sso

cia

ted

wit

hp

resc

rib

ing

of

an

tib

ioti

csfo

ra

cute

con

dit

ion

sin

pri

ma

ryca

rese

ttin

g:s

ho

rtn

am

e,d

escr

ipto

ra

nd

ma

pp

ing

toth

eTD

F

Fact

or

sho

rtn

am

eD

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ipto

rTD

Fd

om

ain

Acc

ess

Acc

ess

toth

eri

gh

tca

refo

rth

eri

gh

tp

ati

ent

at

the

rig

ht

tim

e,in

clu

din

gw

hen

the

pra

ctic

eis

shu

t(e

.g.w

eeke

nd

s),

wh

ilst

the

pa

tien

tis

on

ho

lida

y,fo

rp

ati

ents

wh

oliv

ea

dis

tan

cefr

om

the

pra

ctic

eco

nti

nu

ity

of

care

by

asi

ng

lecl

in-

icia

n,a

nd

ifn

eces

sary

acc

ess

tosp

ecia

list

care

thro

ug

hre

ferr

als

ervi

ces

an

dla

bo

rato

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uip

men

ta

nd

/or

test

ing

.

Envi

ron

men

talc

on

text

&

reso

urc

es

Acc

ou

nta

bili

tyC

linic

ian

sh

eld

acc

ou

nta

ble

(or

feel

like

they

are

hel

da

cco

un

tab

le)

for

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ra

nti

bio

tic

pre

scri

bin

gp

att

ern

s.B

elie

fsa

bo

ut

con

seq

uen

ces

An

tib

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ca

wa

ren

ess

Leve

lof

clin

icia

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ow

led

ge

ab

ou

tth

ere

lati

on

ship

bet

wee

na

nti

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tic

use

an

dre

sist

an

tin

fect

ion

s.K

no

wle

dg

e

An

tib

ioti

cb

elie

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velo

fp

erso

na

lres

po

nsi

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an

tib

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cs,i

ncl

ud

ing

bla

min

go

ther

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rm

isu

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fa

nti

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tics

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fect

ion

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at

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tib

ioti

csa

relo

wri

sk:d

escr

ibin

gu

sea

s‘B

ette

rsa

feth

an

sorr

y’.

Bel

iefs

ab

ou

tco

nse

qu

ence

s

Clin

icia

nch

ara

cter

isti

csC

linic

ian

ag

e,se

x,ye

ars

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ract

ice,

loca

tio

no

fp

rim

ary

den

talq

ua

lifica

tio

n,p

revi

ou

scl

inic

ale

xper

ien

ce.

Do

esn

ot

ma

pto

TDF

Co

mp

etin

gd

em

an

ds

Ava

ilab

ility

of

suffi

cien

tti

me

totr

eat

pa

tien

tin

acc

ord

an

cew

ith

gu

idel

ines

,in

clu

din

g‘s

ita

nd

wa

it’a

pp

roa

chto

bo

oki

ng

urg

ent

pa

tien

tsa

nd

oth

er

pa

tien

tsw

ait

ing

.

Envi

ron

men

talc

on

text

&

reso

urc

es

Co

nfl

ict

Fea

ro

fco

nfl

ict

wit

hp

ati

ent

du

eto

dis

sati

sfa

ctio

na

nd

sub

seq

uen

tlo

sso

fth

ep

ati

ent

toth

ep

ract

ice.

Emo

tio

n

Effi

cacy

of

op

tio

ns

Bel

iefs

ab

ou

tth

eef

fica

cyo

fd

iffe

ren

ttr

eatm

ent

op

tio

ns,

incl

ud

ing

,ab

ility

of

an

tib

ioti

csve

rsu

so

ther

ap

pro

ach

/pro

-

ced

ure

tore

solv

eco

nd

itio

ns

an

db

elie

fth

at

ap

roce

du

rem

ay

wo

rsen

sym

pto

ms.

Bel

iefs

ab

ou

tco

nse

qu

ence

s

Fea

ra

bo

ut

ou

tco

me

Fea

ra

bo

ut

ad

vers

eo

utc

om

es,i

ncl

ud

ing

an

xiet

ya

bo

ut

ma

kin

ga

mis

take

an

dth

ep

rosp

ect

of

seri

ou

sco

mp

lica

tio

ns

ifp

ati

ents

wit

hsy

mp

tom

sg

ow

ith

ou

ta

nti

bio

tics

.Des

crib

eda

s‘ju

st-i

n-c

ase

’or

‘bel

t-a

nd

-bra

ces’

.

Emo

tio

n

Feel

ing

sa

bo

ut

dec

isio

ns

Feel

ing

ab

ou

tth

ea

pp

oin

tmen

ta

nd

dec

isio

ns,

incl

ud

ing

fru

stra

tio

na

tla

cko

fco

nse

nt

for

go

ldst

an

da

rdtr

eatm

ent

or

clin

icia

n’s

emo

tio

na

lsta

tea

tth

ea

pp

oin

tmen

tst

art

.

Emo

tio

n

Fin

an

cia

lbu

rden

Bel

iefs

ab

ou

tfi

na

nci

alb

urd

eno

np

ati

ents

,in

clu

din

ga

bili

tyto

pa

yfo

rcl

inic

alc

on

sult

ati

on

or

fees

for

lab

ora

tory

test

s.

Bel

iefs

ab

ou

tco

nse

qu

ence

s

Fix

the

pro

ble

mG

oa

lfo

rth

ea

pp

oin

tmen

tis

tofi

xth

ep

ati

ent’

sp

rob

lem

:sym

pto

ma

tic

relie

fa

nd

/or

pre

ven

tin

gth

ep

rob

lem

retu

rnin

g.

Go

als

Gu

ida

nce

–pra

ctic

eg

ap

Ga

pb

etw

een

gu

ida

nce

an

dcl

inic

alp

ract

ice,

incl

ud

ing

clin

icia

nco

nce

rns

ab

ou

tth

ea

pp

lica

tio

no

fth

eg

uid

elin

esto

spec

ific

clin

ica

len

cou

nte

rsa

nd

bel

ief

ab

ou

tw

het

her

thei

rcl

inic

alp

ract

ice

(su

cha

sd

ela

yed

pre

scri

bin

gin

den

tist

ry)

ad

her

esto

rele

van

tg

uid

an

ce.

Bel

iefs

ab

ou

tco

nse

qu

ence

s

Gu

idel

ines

&in

form

ati

on

Kn

ow

led

ge

ab

ou

tre

leva

nt

gu

idel

ines

an

do

ther

sou

rces

of

info

rma

tio

n(s

uch

as

fro

mth

ein

tern

eta

nd

ph

arm

ace

ut-

ica

lco

mp

an

ym

edic

alr

epre

sen

tati

ves)

,in

clu

din

ga

pp

rop

ria

tetr

eatm

ent

of

acu

teco

nd

itio

ns/

pre

scri

bin

g.

Kn

ow

led

ge

Ha

bit

sPr

escr

ibin

gh

ab

its

of

clin

icia

n,i

ncl

ud

ing

pa

tter

ns

of

pre

scri

bin

ga

nd

pra

ctit

ion

er-l

evel

vari

ati

on

.M

emo

ry,a

tten

tio

n&

dec

isio

n

pro

cess

es

Hea

lth

care

con

text

Hea

lth

care

syst

emco

nte

xtin

rela

tio

nto

pre

scri

pti

on

of

an

tib

ioti

cs,i

ncl

ud

ing

per

ceiv

edp

ress

ure

tore

du

cea

nti

bio

tic

pre

scri

bin

g,a

bili

tyto

reu

sea

pre

scri

pti

on

,an

da

vaila

bili

tyo

fa

nti

bio

tics

wit

ho

ut

ap

resc

rip

tio

n.

Envi

ron

men

talc

on

text

&

reso

urc

es

Ince

nti

ves

Ince

nti

ves

for

an

da

ga

inst

an

tib

ioti

cu

se,i

ncl

ud

ing

the

imp

act

of

a‘t

ime

ism

on

ey’b

usi

nes

sa

pp

roa

cho

nu

nsc

hed

-

ule

d/u

rgen

ta

pp

oin

tmen

tsa

nd

the

fin

an

cia

lris

ko

flo

sin

gd

issa

tisfi

edp

ati

ents

.

Rei

nfo

rcem

ent

Pati

ent/

con

dit

ion

cha

ract

eris

tics

Ch

ara

cter

isti

cso

fth

ep

ati

ent

(ag

e,se

x,et

hn

icit

y),t

hei

rp

rese

nti

ng

con

dit

ion

(sig

ns,

sym

pto

ms

an

dd

iag

no

sis)

,th

eir

med

ica

lhis

tory

/co

mo

rbid

itie

sa

nd

thei

rso

cio

eco

no

mic

ba

ckg

rou

nd

(lev

elo

fed

uca

tio

n,a

fflu

ence

/dep

riva

tio

net

c.).

Do

esn

ot

ma

pto

TDF

Pati

ent

infl

uen

ceIn

flu

ence

of

(per

cep

tio

ns

ab

ou

t)p

ati

ents

,in

clu

din

g:a

nti

bio

tic-

seek

ing

beh

avi

ou

r(e

xpec

tati

on

s/d

ema

nd

);n

ego

tia

t-

ing

skill

s;p

ati

ent

kno

wle

dg

e/a

ttit

ud

esto

wa

rds

an

tib

ioti

cs;f

ear

of

ad

vers

eo

utc

om

esw

ith

ou

ta

nti

bio

tics

;an

dw

ill-

ing

nes

s/a

bili

tyto

acc

ept

op

era

tive

den

talp

roce

du

re.A

lso

the

infl

uen

ceo

fp

oo

r/ir

reg

ula

ra

tten

der

sa

nd

the

imp

act

of

late

-ru

nn

ing

un

sch

edu

led

ap

po

intm

ents

ma

kin

go

ther

pa

tien

tsw

ho

are

wa

itin

gfo

rth

eir

sch

edu

led

ap

po

intm

ent

an

gry

.

Soci

ali

nfl

uen

ces

Co

nti

nu

ed

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Tab

le3

.C

on

tin

ued

Fact

or

sho

rtn

am

eD

escr

ipto

rTD

Fd

om

ain

Pati

en

tm

an

ag

eme

nt

Skill

sin

pa

tien

tm

an

ag

emen

t,d

iag

no

sis,

trea

tmen

tp

lan

nin

ga

nd

con

sen

t,in

clu

din

gel

icit

ing

con

cern

s,in

terp

reti

ng

the

pa

tien

t’s

des

crip

tio

no

fth

eir

sym

pto

ms,

ma

na

gin

ga

nxi

ou

sp

ati

ents

,ma

na

gin

gex

pec

tati

on

sa

nd

avo

idin

gco

n-

fro

nta

tio

n.N

ego

tia

tio

n,p

ersu

asi

on

,ed

uca

tio

na

nd

hed

gin

g.C

om

mu

nic

ati

on

skill

s.

Skill

s

Pati

ent

sati

sfa

ctio

nB

elie

fa

bo

ut

pa

tien

tsa

tisf

act

ion

,in

clu

din

gim

pa

cto

ffa

ilin

gto

mee

tp

ati

ent

exp

ecta

tio

ns,

imp

act

of

rep

eat

visi

ts

an

dfa

ilure

tore

lieve

sym

pto

ms.

Bel

iefs

ab

ou

tco

nse

qu

ence

s

Peer

s&

colle

ag

ues

Infl

uen

ceo

fp

eers

an

do

ther

colle

ag

ues

inp

ract

ice,

incl

ud

ing

:pre

scri

bin

gp

att

ern

slo

cally

;pro

fess

ion

alc

ou

rtes

yb

y

avo

idin

gen

cro

ach

ing

wh

entr

eati

ng

an

oth

ercl

inic

ian

’sp

ati

ent;

con

fusi

on

cau

sed

by

dif

fere

nt

trea

tmen

tp

att

ern

s

by

dif

fere

nt

clin

icia

ns

(pa

tien

tsu

nce

rta

inw

ha

tis

corr

ect)

;an

du

tilit

yo

fp

eer

sup

po

rtw

hen

dea

ling

wit

hd

ema

nd

ing

situ

ati

on

s.

Soci

ali

nfl

uen

ces

Pla

nn

ing

&co

nse

nt

Bel

ief

ab

ou

ta

bili

tyto

pla

ntr

ea

tmen

ta

nd

ga

inco

nse

nt

du

rin

gu

rgen

ta

pp

oin

tmen

ts,i

ncl

ud

ing

‘do

no

thin

g’o

pti

on

s

an

dm

an

ag

ing

an

xio

us/

ph

ob

icp

ati

ents

.

Bel

iefs

ab

ou

tca

pa

bili

ties

Pra

ctic

ech

ara

cter

isti

csC

ha

ract

eris

tics

of

the

pra

ctic

e,in

clu

din

gp

ub

lic/p

riva

te/i

nsu

ran

cep

rovi

sio

n,g

eog

rap

hic

loca

tio

n(r

ura

lver

sus

urb

an

)

an

dco

un

try.

Do

esn

ot

ma

pto

TDF

Pro

ced

ure

po

ssib

leB

elie

fa

bo

ut

wh

eth

erit

isp

oss

ible

top

rovi

de

trea

tmen

td

ue

tois

sues

bey

on

dth

ed

enti

st’s

skill

sd

uri

ng

urg

ent

ap

po

intm

ents

,in

clu

din

gth

ea

bili

tyto

ach

ieve

ad

equ

ate

loca

lan

aes

thes

iaa

nd

/or

top

rovi

de

op

era

tive

trea

tmen

t

(in

acc

ord

an

cew

ith

gu

idel

ines

)to

den

tally

ph

ob

icp

ati

ents

wit

ho

ut

sed

ati

on

.

Bel

iefs

ab

ou

tca

pa

bili

ties

Pro

fess

ion

alr

ole

Infl

uen

ceo

fp

rofe

ssio

na

lro

leo

nm

an

ag

ing

urg

ent

ap

po

intm

ents

,in

clu

din

gw

ha

tis

the

mea

ns

toca

refo

rp

ati

ents

,

an

dfe

elin

g‘m

ora

llyo

blig

ed’t

oo

ffer

som

eth

ing

tan

gib

le(t

o‘d

on

oth

ing

’is

dif

ficu

lt).

The

ab

ility

top

resc

rib

ea

nti

bio

t-

ics

an

du

seo

wn

‘ru

les

of

thu

mb

’are

bo

thsi

gn

so

fex

per

tise

an

dp

ow

er.

Pro

fess

ion

al/

soci

alr

ole

&id

enti

ty

Rel

ati

on

ship

Des

ire

tob

uild

/ma

inta

ina

go

od

clin

icia

n-p

ati

ent

rela

tio

nsh

ip.

Go

als

Ris

kp

erce

pti

on

Bel

iefs

ab

ou

tri

sks

wh

enm

an

ag

ing

the

pa

tien

t’s

con

dit

ion

,in

clu

din

gw

ors

enin

go

fth

eco

nd

itio

n,f

ailu

reo

f(o

rin

ab

il-

ity

toco

mp

lete

)a

no

per

ati

vep

roce

du

re,a

nd

pa

ind

uri

ng

or

aft

erp

rovi

sio

no

fa

pro

ced

ure

or

med

ico

leg

al

com

pla

int.

Bel

iefs

ab

ou

tco

nse

qu

ence

s

Trea

tmen

tsk

ills

Skill

sin

pro

vid

ing

urg

ent

pro

ced

ure

s,in

clu

din

gp

laci

ng

loca

lan

aes

thet

icb

yin

ject

ion

ind

iffi

cult

clin

ica

lsit

ua

tio

ns

or

lan

cin

ga

na

bsc

ess

inth

ep

rese

nce

of

swel

ling

.

Skill

s

Wo

rklo

ad

Bel

ief

ab

ou

tim

pa

cto

nw

ork

loa

d,i

ncl

ud

ing

tim

eta

ken

toex

pla

intr

eatm

ent

op

tio

ns,

ga

inin

form

edco

nse

nt,

del

iver

trea

tmen

to

pti

on

sa

nd

/or

trea

tth

ep

ati

ent

an

oth

erd

ay

on

reca

ll.

Bel

iefs

ab

ou

tco

nse

qu

ence

s

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address this, synthesis was guided iteratively through reference tothe TDF.

Social scientists are part of the contexts they study and it is notpossible to step outside in order to study the topic entirely

objectively.50 The authors were acutely aware, therefore, of theirunique knowledge, attitudes and expectations in relation to anti-biotic use. Recognizing this, the authors attempted to remainexact, sincere and impartial when handling the data.51 Resultswere checked for sense and understanding with non-clinical col-leagues, including the study’s PPI advisers. Nevertheless, theauthors acknowledge that the conclusions were inherently relatedto their specific interpretations and that other equally valid conclu-sions could be drawn from the same data.

The broad range of methodologies employed within theincluded studies [systematic reviews, meta-ethnographies andprimary research (both quantitative and qualitative)] complicatedthe quality assessment as well as extraction, interpretation andpresentation of the results. All of the included dental studies reliedon self-reporting by clinicians about real or simulated clinical casesthrough interviews and/or questionnaires. Studies that rely on self-reported perceptions are inherently at risk of bias in the way peopleaccount for their and others’ behaviour and people are usually notaware of what influences their unconscious/instinctive behav-iour.52 This was a recognized limitation of the included studies andcould account in part for the two most frequently found factorsacross the two reviews: ‘patient/condition characteristics’ and ‘pa-tient influence’. A study of clinical autonomy in relation to prescrib-ing in general practice found that to balance the requirements ofthe patients and the healthcare system, doctors may state ‘clinicalneed’ when it suits them to do so, otherwise they blame ‘patientdemand’.53 Studies of GP consultations and with patients havefound a mismatch between GP reports of patient expectations/de-mand for antibiotics and patient reports.54–56 Similar studies are

Table 4. Summary of potentially modifiable determinants of behaviour associated with the decision whether to prescribe systemic antibiotics foradult patients with acute conditions, showing a comparison between factors identified in the umbrella review across primary care and/or systematicreview of primary dental care

Both umbrella and systematic reviewUmbrella review across primary

care studies onlySystematic review of dental

care studies only

Access accountability procedure possible

Competing demands antibiotic awareness treatment skills

Efficacy of options antibiotic beliefs

Fear about outcome conflict

Feelings about decisions financial burden

Fix the problem

Guidance–practice gap

Guidelines & information

Habits

Healthcare context

Incentives

Patient influence

Patient management

Patient satisfaction

Peers & colleagues

Planning & consent

Professional role

Relationship

Risk perception

Workload

Table 5. Summary of potentially modifiable determinants of behaviourassociated with the decision whether to prescribe systemic antibioticsfor adult patients with acute conditions, showing a comparison betweenthose identified in studies of high-income countries and LMICs

High-income countries onlyHigh-income countries

and LMICs LMICs only

Accountability access

Antibiotic awareness antibiotic beliefs

Efficacy of options competing demands

Feeling about decisions conflict

Guidance–practice gap fear about outcome

Guidelines & information financial burden

Incentives fix the problem

Patient management habits

Patient satisfaction healthcare context

Peers & colleagues patient influence

Planning & consent treatment skills

Professional role

Relationship

Risk perception

Procedure possible

Workload

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required, therefore, to explore which factors influence actual pre-scribing decisions in general dental practice.

The results of these studies should assist the theory-informeddesign of new interventions (and the fine-tuning of existing inter-ventions) aimed at helping clinicians to optimize their prescribingof antibiotics during urgent appointments. They will draw on theexperience of existing multifactorial interventions developed forGPs that have been shown to be effective at reducing antibioticprescribing. One intervention for managing adults with acutecough, GRACE INTRO, used enhanced communication skills and apoint-of-care test for the C-reactive protein biomarker of bacterialinfection (CRP POCT). The intervention positively influenced threefactors identified in this review, as tested in the process evaluationof the trial: (i) increased clinician confidence to reduce antibioticprescribing (‘guidance–practice gap’); (ii) increased perceived im-portance of decreasing prescribing (‘antibiotic awareness’); and (iii)reduced perceived risk of decreasing prescriptions (‘riskperception’).50,51

Conclusions

This study provides a robust identification of the breadth of factorsassociated with the decision whether to prescribe systematic anti-biotics for adults presenting with acute conditions in a range of pri-mary care contexts around the world. Further studies are neededto provide more detailed understanding of which factors are rele-vant determinants of behaviour during actual clinical encountersto inform the theory-informed design of context-specific antibioticstewardship interventions.

AcknowledgementsThis research was carried out as part of a PhD by the first author. Withthanks to the PhD supervisors and PPI advisors, as well as to Judy Wrightand Natalie King for their guidance as information specialists.

FundingThis work was supported by a University of Leeds Anniversary ResearchScholarship as part of W. T.’s PhD research. W. T.’s on-going research issupported by the National Institute for Health Research (NIHR DoctoralResearch Fellowship, Mrs Wendy Thompson, DRF-2016–09-148). In add-ition, W. T., S. H. P., G. V. A. D. and J. A. T. S. are supported by the NIHR in-frastructure at Leeds. S. T.-C. is supported by NIHR through the HealthProtection Research Unit (NIHR HPRU) in Healthcare AssociatedInfections and Antimicrobial Resistance at the University of Oxford inpartnership with Public Health England (PHE)(HPRU-2012–10041).

Transparency declarationsW. T. received funds from Health Education England for speaking atcontinuing professional development events aimed at optimizing anti-microbial prescribing by primary care dentists and GPs in relation toacute dental conditions. W. T. had contracts with Bradford District CareNHS Trust, Cumbria Partnership NHS Trust and Integrated DentalHoldings Ltd to provide primary care dentistry on behalf of the NHS. S.H. P. oversees clinical trials/research funded by NIHR, industry (Solvay,GSK, Proctor & Gamble) and charities (Multiple Sclerosis Society andBritish Society for Oral & Dental Research). All other authors: none todeclare.

Author contributionsW. T. undertook all aspects of this study and production of this paper

for publication. All other authors contributed to design of the reviewsand the process of finalizing the set of potentially modifiable and non-modifiable behaviours, as well as more specifically: S. T.-C. provided inde-pendent assessment of the factors and their mapping to the TDF, con-tributed to analysis and drafting of the manuscript; S. H. P. provided asense check for the resulting themes and drafting of the manuscript; R.R. C. M. assisted with the iterative process of developing factors andmapping them to the TDF, contributed to analysis and drafting of themanuscript; G. V. A. D. provided independent assessment for elementsrelating to the systematic review of primary dental care studies anddrafting of the manuscript; V. R. A. participated in the quality assessmentof included studies for the systematic review of dental studies and critic-ally reviewed the manuscript from a clinical and methodological per-spective; J. A. T. S. provided independent assessments for all elementsrelating to the umbrella review across primary care, contributed to ana-lysis and drafting of the manuscript.

DisclaimerThe views expressed are those of the authors and not necessarily thoseof the NHS, NIHR or the Department of Health and Social Care.

Supplementary dataTables S1 to S7 are available as Supplementary data at JAC Online.

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