A systematic scoping review of interventions to improve appropriate prescribing of oral nutritional supplements in primary care

Clinical Nutrition xxx (xxxx) xxx

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Clinical Nutrition journal homepage: http://www.elsevier.com/locate/clnu

Review

A systematic scoping review of interventions to improve appropriate prescribing of oral nutritional supplements in primary care n Fitzgerald a, Clare A. Corish c, d, Cathal A. Cadogan a, *, Rachel Dharamshi b, Sea Patricia Domínguez Castro c, d, Cristín Ryan e a

School of Pharmacy, Royal College of Surgeons in Ireland, Dublin, Ireland School of Medicine, Royal College of Surgeons in Ireland, Dublin, Ireland School of Public Health, Physiotherapy and Sports Science, University College Dublin, Dublin, Ireland d Institute of Food and Health, University College Dublin, Dublin, Ireland e School of Pharmacy and Pharmaceutical Sciences, Trinity College Dublin, Ireland b c

a r t i c l e i n f o

s u m m a r y

Article history: Received 16 October 2018 Accepted 5 March 2019

Background & aims: Oral nutritional supplements (ONS) are commonly used to treat malnutrition. Many patients are prescribed ONS without assessment of nutritional status. This conflicts with prescribing guidelines and has considerable cost implications. This scoping review aimed to provide an overview of interventions to improve appropriate ONS prescribing in primary care. Methods: A systematic scoping review was undertaken. PubMed, EMBASE and CINAHL were searched from inception to September 2018. Studies meeting inclusion criteria had to: evaluate interventions targeting ONS prescribing in primary care; use a comparative evaluation; be published in English. Two reviewers independently screened abstracts and extracted data relating to study design, intervention characteristics, outcome assessments and key findings. Extracted data were collated using figures, tables and accompanying descriptive summaries. Results: 10 studies met inclusion criteria. All studies involved uncontrolled before-and-after designs. Interventions ranged from dietitian-led reviews of patients prescribed ONS to transfer of ONS prescribing privileges from general practitioners to dietitians. Post-intervention results showed improvements in ONS prescribing based on study-specific assessments of prescribing appropriateness and absolute reductions in prescribing, as well as potential cost-savings. Conclusions: This review provides a detailed overview of interventions aimed at improving appropriate ONS prescribing in primary care. Interventions evaluated to date most commonly involved dietitians. However, use of controlled experimental design was lacking. Lack of consistency in defining appropriate ONS prescribing and assessment outcomes was apparent. Future research should attend to rigour during intervention development, evaluation and reporting in order to generate findings which could inform relevant policy and practice. © 2019 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.

Keywords: Nutrition Malnutrition Oral nutritional supplements Prescribing Primary care

1. Background Protein-energy malnutrition, arising from a deficiency in energy and protein intake, causes measurable adverse effects on body composition, function and clinical outcomes, and is common across healthcare settings in developed countries [1e3]. For example, in the UK, it is estimated that at any given time, more than three

* Corresponding author. E-mail address: [email protected] (C.A. Cadogan).

million people are malnourished or at risk of malnutrition, most of whom are community-dwelling [4]. Oral nutritional supplements (ONS) are commonly prescribed in clinical practice to treat diseaserelated malnutrition; however, their nutritional and clinical benefits in adults vary, and the patient groups most likely to benefit from ONS remain to be characterised [5]. This creates challenges in ensuring appropriate prescribing of ONS. Appropriate prescribing is a general term that encompasses a range of values and behaviours relating to the quality of prescribing [6]. In the context of medical prescribing, comprehensive evaluations of prescribing appropriateness typically encompass the

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Please cite this article as: Cadogan CA et al., A systematic scoping review of interventions to improve appropriate prescribing of oral nutritional supplements in primary care, Clinical Nutrition, https://doi.org/10.1016/j.clnu.2019.03.003

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domains of misprescribing (prescribing that significantly increases patients' risk of adverse events, including incorrect dosing, frequency or duration), overprescribing (prescribing in the absence of a clinical indication) and underprescribing (omission of treatments for specific clinical indications aimed at treatment or prevention) [7]. Currently, there is no universally accepted definition of appropriate prescribing for ONS. Key aspects of appropriate ONS prescribing involve patient screening and assessment to ensure that a clinical indication for nutrition support exists (i.e. malnutrition, high risk of malnutrition), global assessment of the underlying causes of malnutrition, setting goals in terms of nutrition support treatment (e.g. target weight gain), providing food first advice and regular monitoring of patients subsequently prescribed ONS to assess continued need [8]. The Global Leadership Initiative on Malnutrition (GLIM) [9] has recently proposed criteria for the diagnosis of malnutrition involving a combination of phenotypic factors (weight loss, reduced muscle mass and reduced body mass index [BMI]) and aetiological factors (reduced food intake/ assimilation and disease burden/inflammation) [9]. Malnutrition screening tools can be used to identify patients requiring nutrition support [10]. Inappropriate ONS prescribing encompasses a range of clinical scenarios, including: prescribing in the absence of a clinical indication (overprescribing); prescribing incorrect doses or durations of treatment that extend beyond the original clinical indication (misprescribing); and failure to prescribe for patients with a clinical indication for ONS (underprescribing). Previous research indicates that inappropriate ONS prescribing is common in community settings with the prevalence ranging between 30 and 70% based on assessments involving the application of guidelines and studyspecific criteria [11e13]. ONS can generally be discontinued when malnutrition risk status has returned to normal, weight has stabilised, further weight loss is unlikely, and nutritional requirements are being met through normal diet [14]. Inappropriate ONS prescribing has significant cost implications, as well as potential clinical implications, and targeted interventions are needed to improve appropriate prescribing of ONS in primary care [11,15]. However, there is no current review of existing research which limits our understanding of the available evidence base. This scoping review aimed to examine existing interventions to improve appropriate prescribing of ONS in primary care. This will help to identify whether gaps exist in the current literature and highlight areas to explore further, and in greater depth, in future research. 1.1. Objective and review questions The objective of this scoping review was to provide an overview of evaluations of interventions aimed at improving appropriate prescribing of ONS in primary care. The review was conducted in accordance with relevant methodological guidance [16,17] and was led by the following review questions: 1. What types of study designs have been used to evaluate interventions to improve appropriate prescribing of ONS in primary care settings to date? 2. What types of interventions to improve appropriate prescribing of ONS in primary care settings have been evaluated to date? 3. Who were the interventions targeted at? (i.e. patients and/or healthcare professionals) 4. Who delivered the interventions? 5. What outcome measures were used to evaluate the interventions? 6. What have the key findings of these evaluations been?

2. Methods This review is reported in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines for scoping reviews (Appendix 1) [18]. The review protocol is available from the authors on request. 2.1. Search strategy The following electronic databases were searched from inception to September 2018 to identify relevant publications using established search methods for scoping reviews: PubMed, EMBASE and CINAHL [16]. Briefly, preliminary database searches were undertaken to identify keywords and index terms for articles relating to the review topic. This informed the development of a comprehensive search strategy. The search strategies were reviewed by a research librarian before being finalised (Appendix 2). Key search terms included: oral nutritional supplements, malnutrition and prescribing. Following database searching, reference lists of all studies meeting inclusion criteria, as well as relevant review articles were screened for additional studies. Only studies published in the English language were considered for inclusion in this review. No date limitations were imposed. 2.2. Inclusion criteria 2.2.1. Type of participants The review included interventions targeting ONS prescribing for any primary care-based patient population. For the purpose of this review, primary care was defined as the first-point of contact with the healthcare system which is accessible at the time of need, comprehensive, coordinated and available on an ongoing basis [19]. Interventions were eligible for inclusion if they targeted either patients or healthcare practitioners in a primary care setting (e.g. general practice, community pharmacy). Studies involving multiple settings were eligible for inclusion provided that the primary carebased component was readily identifiable. Studies based exclusively in non-primary care settings (e.g. nursing homes, hospitals) were excluded. 2.2.2. Types of interventions The review included any intervention targeting ONS prescribing in primary care. Interventions targeting the prescribing of artificial nutrition (i.e. enteral nutrition, parenteral nutrition) were excluded from the review. Interventions targeting the prescribing of combinations of ONS and artificial nutrition were eligible for inclusion provided that ONS prescribing was assessed and reported on separately. 2.2.3. Types of studies In order to meet inclusion criteria, studies had to include some form of comparative evaluation (e.g. inclusion of a control group or use of a before/after design) of an intervention targeting ONS prescribing in primary care. Only studies published in the English language were included in the review. 2.2.4. Types of outcomes As there is no existing overview of outcomes of interventions aimed at improving appropriate prescribing of ONS in primary care, all outcomes for studies that met the above inclusion criteria were included in the review. This allowed an overview to be provided of the range of outcomes investigated on this topic.

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2.3. Study selection Abstracts were screened for inclusion by two authors independently. All abstracts were screened by the lead review author (CC). The double screening of abstracts was divided between two additional review authors (RD, PDC). If a study appeared to meet inclusion criteria, full-text articles were retrieved and assessed for inclusion by two authors working independently. Any disagreements were resolved through consensus discussion with another author (CR) [15]. 2.4. Charting, collating and summarising the data

IdenƟficaƟon

Data extraction (referred to as ‘charting’ in the scoping review literature [16]) was performed independently by two authors (CC, RD) using a purposefully developed data extraction that was constructed in accordance with relevant methodological guidance (Appendix 3) [16]. Data were extracted relating to: year of publication; source origin/country of origin; study design; setting; aims/purpose; study population and sample size; intervention details; control group (if applicable); study outcomes; key findings. This enabled a logical and descriptive summary of the review findings to be presented that aligned with the review objective and questions. The Effective Practice and Organisation of Care taxonomy of health systems interventions was used to categorise interventions into four key domains: ‘Delivery arrangements’, ‘Financial arrangements’, ‘Governance arrangements’, ‘Implementation strategies’ [20].

Records idenƟfied through database searching (n =3511)

3

As the aim of a scoping review is to provide a broad overview of the existing literature relating to a particular research question, formal assessments of methodological quality of included studies are not routinely undertaken [16]. Data collation focused on summarising the information presented across included studies. Three strategies were used to aid the reporting and presentation of results: (i) a Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) flow diagram [18] was used to present the search results; (ii) tables and accompanying descriptive summaries were used to provide an account of the data charted from each included study; and [21] a content analysis of the charted data relating to the interventions' components, deliverers/recipients and study outcomes was undertaken to map the data. This process was led by the primary review author and the findings were reviewed by the wider team. Any disagreements were resolved through discussion. 3. Results 3.1. Study designs used in evaluating interventions (review question 1) The electronic searches identified 3329 citations. Following title and abstract screening, 85 articles were then reviewed for eligibility. Ten studies met inclusion criteria, all of which involved an uncontrolled before-and-after design (Fig. 1) [12,13,22e29]. Six studies were published as conference abstracts for which no further published reports were identified [13,22,23,27,28,30]. This limited

AddiƟonal records idenƟfied through other sources (n =1)

Included

Eligibility

Screening

Records aŌer duplicates removed (n = 3329)

Records screened (n =3329)

Records excluded (n = 3244)

ArƟcles assessed for eligibility (n =85)

ArƟcles excluded, with reasons (n =73) No appropriate data (n=28); unsuitable design (n=24); intervenƟon did not target ONS prescribing (n=7); not conducted in a primary carebased seƫng (n=7); non-English language publicaƟon (n=7)

Studies included in qualitaƟve synthesis (n =10*)

* Two included studies had mulƟple linked references Fig. 1. PRISMA flow diagram.

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the amount of available information for data extraction. Two studies had more than one reference. [25,29e31] Three studies made attempts to compare intervention group data with data from non-intervention groups; however, these comparisons were either not set out a priori or clearly reported [27,29,31]. Reasons for exclusion of the remaining articles were: no appropriate data (28 studies); unsuitable study design (24 studies); intervention did not target ONS prescribing (seven studies); not conducted in a primary care setting (seven studies); non-English language publication (seven studies). The included studies were conducted in three countries: Ireland [25,31], England [12,23,26,28e30] and Scotland [13,22,24,27] (Table 1). Nine studies were conducted in general practice settings, ranging from a single practice initiative to a project targeting ONS prescribing across 265 general practices (Table 1). One study involved a combination of general practice and nursing home settings [25]. The population of patients receiving ONS prescriptions ranged from 25 to 5000 patients (Table 1). Patients' demographic details were available in three studies [24,25,31] and were limited to age and gender, with one study also reporting on residential status [24]. Baseline clinical information was available in three studies [12,29,31] and included information on patients' BMI, duration of ONS prescriptions and chronic health conditions. 3.2. Intervention details (review question 2) Intervention details are summarised in Table 2 and outlined below. Based on the EPOC taxonomy [20], interventions were classified as either ‘delivery arrangements’ (nine studies) or ‘governance arrangements’ (one study). Four interventions classified as delivery arrangements involved dietitian prescribing support [13,23,28,29]. In these interventions, dietitians reviewed ONS prescribing to ensure that it aligned with relevant guidelines/criteria [13,29], invited patients to consultations or clinics for reviews [13,28,29] and provided training to primary care staff on nutritional care [23]. In the studies that did not specifically refer to dietitian prescribing support, interventions involved clinical reviews of patients receiving ONS [24,26], the use of guidelines/formularies to ensure appropriate ONS prescribing [12,22], education and training on nutrition care [12,25] and the introduction of nutrition care pathways [24,25]. The only intervention classified as a ‘governance arrangement’ involved the implementation of contractual changes for preferred ONS [27]. Community-based dietitian prescribing support was also provided to facilitate prescription changes. Only one study alluded to, but did not describe, the intervention development process [25]. In the remaining cases, it was unclear how intervention components had been selected. None of the studies referred to the application of theory in informing the selection of intervention components. 3.3. Intervention recipients and deliverers (review questions 3 and 4) Interventions targeted patients receiving ONS prescriptions and/or primary care healthcare professionals, including general practitioners (GPs) and community nurses, involved in their treatment (Table 2). Dietitians were involved in delivering seven of the nine interventions classified as ‘delivery arrangements’. However, the mode of intervention delivery was not always clearly described or apparent from study descriptions. In six studies where mode of

intervention delivery was identifiable, it involved face-to-face and/ or written delivery. The only intervention that was classified as a ‘governance arrangement’ involved a number of healthcare professionals [27]. In this study, which involved implementation of contractual changes regarding preferred ONS, community-based dietitians developed a protocol for the general practice-based pharmacists and pharmacy technicians to review medical records of patients prescribed ONS and recommended changes to prescribers where appropriate. Support dietitians reviewed patients for whom changes in ONS might not have been suitable for clinical reasons. The only studies that referred to intervention duration were those involving education/training sessions [12,25,31]. None of the included studies provided detailed information on intervention costs and resource requirements (Table 2). 3.4. Study outcomes (review question 5) Outcome measures were poorly described across studies and none of the studies differentiated between primary and secondary outcomes. Study outcomes consisted of assessments of the appropriateness of ONS prescribing (nine studies), changes in ONS expenditure (six studies), prescribing of preferred/contracted ONS (one study), referrals to dietetics services (one study), body mass index (one study) and healthcare professionals' nutrition-related knowledge (two studies) [Table 2]. Four studies also gathered feedback from patients or healthcare professionals in relation to aspects of care. Of the nine studies that included assessments of the appropriateness of ONS prescribing, three studies explicitly defined appropriate ONS prescribing [12,24,25]. Each of these studies listed explicit criteria relating to clinical situations in which ONS prescribing was indicated and appropriate (e.g. presence of diseaserelated malnutrition or nutritional risk). Four studies referred to assessments of the appropriateness of ONS prescribing involving either guidelines from the National Institute for Health and Care Excellence (NICE) [1,32] on the use of nutrition support in adults [25,29], or local guidelines and formularies [13,22]. Three studies did not clearly outline how the appropriateness of ONS was determined [23,26,28]. Only three studies clearly stated the time points at which outcomes were assessed [12,27,31]. These assessment time points ranged from one week to one-year post-intervention. 3.5. Key study findings (review question 6) Key study findings relating to the review question are summarised in Table 3 and outlined below. 3.5.1. Baseline assessments A lack of documented nutritional assessments or available information on nutritional status was commonly identified across studies. For example, four studies reported that the proportion of patients for whom nutritional status was unknown ranged from 33% to 73% [13,22,23,30]. The reported prevalence of inappropriate ONS prescribing whereby patients did not meet relevant ONS guidelines/prescribing criteria ranged from 29% to 50% [13,23,24,28e30]. One study reported that 45% (148/328) of patients receiving ONS warranted a dietetic review [13]. 3.5.2. Post-intervention assessments All nine studies that evaluated interventions classified as ‘delivery arrangements’ reported improvements in ONS prescribing post-intervention. These improvements consisted of reductions in total ONS prescribing or reductions in inappropriate ONS

Please cite this article as: Cadogan CA et al., A systematic scoping review of interventions to improve appropriate prescribing of oral nutritional supplements in primary care, Clinical Nutrition, https://doi.org/10.1016/j.clnu.2019.03.003

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Table 1 Overview of key study characteristics. Study ID

Country

Setting

Aim/purpose

Cummins 2015a

Scotland Uncontrolled before and after study

Study design

General practice

328 patients across To improve clinical management of Patients prescribed ONS across GP practices 10 general practices ONS prescribing and reduce with the highest ONS associated costs using dietetic cost per patient prescribing support

Study population

Sample size

Cummins 2015b

Scotland Uncontrolled before and after study

General practice

To review ONS prescribing and ensure that prescribing complied with local ONS guidelines and formulary

Patients prescribed ONS in GP practices

434 patients across 26 general practices

Gall 2001

England

Uncontrolled before and after study

General practice

To determine if ONS prescribing guidelines and primary care team education could improve ONS prescribing

GPs and community nurses involved in ONS prescribing for general practice patients

438 patients across 50 general practices involving 212 GPs and 139 community nurses

Gilson 2015

England

Uncontrolled before and after study

General practice

To fund increased community dietetic support by reducing inappropriate ONS prescribing

Community-based patients prescribed ONS

1123 patients across 64 general practices

Gratton 2016

England

Uncontrolled before and after study

General practice

To evaluate a dietetic service for optimising ONS use

Patients prescribed ONS in GP practices

398 patients across 15 general practices

Jones 2003

Scotland Uncontrolled before and after study

General practice

To audit the appropriateness of ONS prescribing To introduce a nutritional care pathway to enable primary care staff to identify and treat patients at risk of malnutrition General To provide high quality ONS practice prescribing services To extend dietitians' role in ONS prescribing To reduce total spend on ONS through appropriate prescribing To reduce GP workload To evaluate a community dietetics General intervention practice and nursing To investigate the nutrition care practices of GPs who used the homes community dietetics referral service and had participated in a nutrition education programme

Patients prescribed ONS in GP practices

94 patients across 24 general practices

Patients prescribed ONS by GPs

Not clearly reported: 757 ONS prescriptions identified

Patients prescribed ONS in GP practices Primary care staff (GPs, practice nurses, community nurses)

42 patients across 7 general practices

Kakarlapudi 2016 England

Uncontrolled before and after study

Kennelly 2010

Ireland

Uncontrolled before and after study

Ragubeer 2011

England

Uncontrolled before and after design

General practice

To ensure appropriate ONS prescribing and to reduce the cost associated with inappropriate ONS prescribing

Patients prescribed ONS in a single GP practice

25 patients from a single general practice

Welch 2012

Scotland Uncontrolled before and after study

General practice

To report on implementation of a change in preferred (contracted) ONS

Patients prescribed ONS in GP practices

5000 patients (approximately) across 265 general practices

prescribing based on study-specific assessments. For example, Gall et al. reported that the proportion of patients prescribed ONS inappropriately (according to study-specific criteria) reduced from 73% (211 patients) at baseline to 54% (131 patients) three months post-intervention [12]. In addition to reporting an overall reduction in ONS prescribing post-intervention, Kennelly et al. reported that a significantly higher proportion of patients deemed at high risk of malnutrition were receiving ONS post-intervention compared to pre-intervention (88% vs 37%, p < 0.001) [25].

Outcome measures Appropriateness of ONS prescribing (based on guideline and formulary) ONS expenditure Appropriateness of ONS prescribing (based on guideline and formulary) ONS expenditure Appropriateness of ONS prescribing (using study specific criteria) Primary care team staff knowledge of nutrition screening/assessment Appropriateness of ONS prescribing (no criteria/ guidelines specified) ONS expenditure Appropriateness of ONS prescribing (based on guidelines) ONS expenditure BMI Patient satisfaction Appropriateness of ONS prescribing (using study specific criteria) Healthcare professionals' views on care pathway Not clearly described/ reported: abstract lists various measures used to monitor performance, including ONS use and expenditure Appropriateness of ONS prescribing (based on guidelines) Referral of patients to dietetics services ONS expenditure Healthcare professionals' nutritional knowledge Appropriateness of ONS prescribing (no criteria/ guidelines specified) Views/experiences of healthcare professionals and patients on nutritional screening and ONS prescribing Prescribing of preferred (contracted) ONS

Five of the six studies that assessed ONS expenditure postintervention reported cost savings based on reductions in inappropriate ONS prescribing [13,22,23,28,29]. In one study, these cost savings were reportedly used to fund a dietetic service [23]. Kennelly et al. reported no significant change in ONS expenditure by participating GPs twelve months post-intervention (3% reduction, p ¼ 0.499) [31]. Only one study reported on a post-intervention clinical assessment of patients' BMI [29]. This study reported no difference in

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Table 2 Intervention characteristics. Study ID

Intervention summary

EPOC classification

Underpinning evidence/ theory base

Intervention targets

Intervention deliverer and mode of delivery

Intervention duration

Intervention costs/ resource requirements

Cummins 2015a

Dietetic prescribing support involving review of ONS prescribing and dietetic clinics

Delivery arrangements

None stated

Patients prescribed ONS

Not stated

Unclear if other resource requirements in addition to dietitian

Cummins 2015b

Review of ONS prescribing to ensure compliance with local guidelines and formulary

Delivery arrangements

None stated

Not stated

Not specified

Gall 2001

ONS prescribing guidelines supported by training for healthcare professionals

Delivery arrangements

None stated

GPs and patients prescribing/ receiving ONS GPs and community nurses

Intervention delivered face-toface by prescribing support dietitian Unclear

Training sessions lasted 1 h

Not specified

Gilson 2015

Community dietetic support service to reduce inappropriate ONS prescribing including delivery of training for primary care staff Dietetic prescribing support involving review of ONS prescribing and dietetic clinics

Delivery arrangements

None stated

Not stated

Summary of increases in dietetic service staff resources over time provided

Delivery arrangements

Baseline audit undertaken prior to service to assess ONS prescribing and identify patients warranting review Baseline audit undertaken prior to service to establish ONS prescribing practices

Not stated

Unclear if other resource requirements in addition to dietitian

Not stated

Not clearly stated: dietitians involved in developing and implementing care pathway

Not stated

Unclear if other resource requirements in addition to dietitian Overview of reported costs associated with implementing the intervention outlined

Gratton 2016

Primary care staff and patients prescribing/ receiving ONS Patients prescribed ONS

Primary care staff and patients prescribing/ receiving ONS

Jones 2003

Dietitian-led review of patients receiving ONS and introduction of care pathway for identification and treatment of malnutrition

Delivery arrangements

Kakarlapudi 2016

Dietitian-led review of ONS prescribing

Delivery arrangements

None stated

Patients prescribed ONS

Kennelly 2010

Nutrition education programme for healthcare professionals and a care pathway for dietetic referrals

Delivery arrangements

Primary care staff involved in identifying and treating patients at risk of malnutrition

Ragubeer 2011

Clinical dietetic review of patients receiving ONS

Delivery arrangements

Format and content of education programme developed based on consultation with key health professional groups and previous research. No theory base reported None stated

Welch 2012

Contractual change regarding preferred (contracted) ONS and community-based dietitian prescribing support provided to facilitate prescription changes

Governance arrangements

None stated

Patients prescribed ONS

Patients prescribed ONS

Training sessions delivered face-toface but unclear who delivered these sessions Written intervention material also provided Intervention delivered by dietitians but unclear how it was delivered Intervention delivered face-toface by dietitian

Community dietitians developed and implemented the nutritional care pathway but unclear how it was delivered Intervention delivered face-toface by dietitian Intervention delivered face-toface by a dietitian

Intervention delivered face-toface and involved a community dietitian and practice pharmacist Unclear how intervention was delivered Roles of dietitians, prescribers, pharmacists and pharmacy technicians in implementing prescribing changes outlined

Educational component: session lasted 1e3 h Dietetics service component: duration unclear

Not stated

Unclear

Not clearly stated. Authors acknowledge that reported savings did not account for core healthcare professionals' costs Not clearly stated

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Table 3 Overview of key study findings. Study ID

Key findings

Cummins 2015a

52% of patients identified as clinically malnourished, 36% unknown and 12% not malnourished 71 (±17)% of ONS prescriptions complied with the ONS prescribing formulary Dietitian recommended that 148/328 (45%) patients receive a dietetic review 54% (80/148) of ONS prescriptions discontinued following review Dietetic prescribing support initiative reportedly contributed to reducing ONS expenditure: cost per 1000 ONS patients in accordance with Scottish average and estimated annual spend reduction of 22% in 2012/13 compared to 2010/11 63 (±16)% of patients identified as clinically malnourished, 4 (±7)% were not malnourished and 33 (±16)% unknown 28% of patients had ONS prescription reduced/discontinued and 8%of patients referred to dietitian 45 (±28)% patients provided with food fortification advice ONS prescribing changes yielded annual saving of £133,289, with an average saving of £5127 (±5580) per GP practice 15% reduction in proportion of patients prescribed ONS between baseline audit and three-month post-intervention follow-up (p < 0.001) Proportion of patients prescribed ONS inappropriately reduced from 73% (211 patients) at baseline to 54% (131 patients) at follow-up Lack of documented nutritional status assessment: MUST score documented in only 27% of patients receiving ONS who were reviewed Inappropriate ONS prescribing identified in 44% of patients ONS prescribing changes yielded cost-saving of £103,798 in 2012e13 64% (n ¼ 398) of patients receiving ONS were not under the care of existing dietetic services and did not have clearly documented indications for ONS or nutritional care plans with clear treatment goals (as recommended by malnutrition guidelines) Prescribing changes implemented: ONS discontinued (268 patients); ONS reduced or switched to a more cost-effective product (2 patients); ONS increased/switched to more expensive products (2 patients); no changes made (4 patients) All patients seen in clinic post-intervention had an up-to-date BMI (or alternative measurement) documented along with a nutritional care plan and treatment aim Costs savings associated with reductions in ONS prescribing in general practices providing dietetic reviews Twelve patients returned satisfaction questionnaires: all were likely (3/12) or extremely likely (9/12) to recommend the service to friends or family Lack of recorded information for patients receiving ONS prescriptions: Weight recorded for 34% (104) and BMI recorded for 18% (55) before receiving a ONS prescription; 23% (71) of patients had details of nutritional monitoring documented in their notes Inappropriate ONS prescribing: Approximately 50% of patients receiving ONS had a normal or increased BMI and were classed as well nourished 28 patients (30%) had ONS discontinued 280/757 ONS prescriptions identified as inappropriate and discontinued Improved quality of care for patients reported with reduced access times and 100% patients receiving dietetic support Reduction in ONS expenditure by 27%, delivering annual savings >£1,200,000 (£400,000 of which invested in dietetics) High levels of patient satisfaction reported 18% reduction in proportion of patients prescribed ONS post-intervention compared to pre-intervention (p ¼ 0.074) ONS prescribed to a higher proportion of patients deemed at high risk of malnutrition post-intervention compared to pre-intervention (88% vs 37%, p < 0.001) No significant change in ONS expenditure by participating GPs post-intervention (3% reduction, p ¼ 0.499) Baseline audit identified a lack of robust data collection in relation to ONS prescribing (e.g. no record of original assessments, lack of recorded information on height/weight/BMI etc) Inappropriate ONS prescribing practices identified: without dietitian intervention, 25 patients would have continued on their current ONS Patients reporting never having had ONS reviewed Healthcare professionals expressed desire for training and involvement of dietitian in ONS prescribing Four months following implementation of contract change, prescribing of preferred sip feed increased from 8% of all sip feeds to 83% In all other health boards the change was smaller; although it was observed that two were already using the preferred version

Cummins 2015b

Gall 2001 Gilson 2015

Gratton 2016

Jones 2003

Kakarlapudi 2016

Kennelly 2010

Ragubeer 2011

Welch 2012

patients' BMI between baseline and follow-up. However, the time point of the post-intervention assessment was unclear. The only study that evaluated an intervention classified as a ‘governance arrangement’, which involved the implementation of a change in preferred (contracted), ONS found that the prescribing of preferred ONS increased from 8% of all ONS in the month prior to the change to 83% of all ONS four months later [27]. 4. Discussion This review provides the first systematic overview of interventions aimed at improving appropriate prescribing of ONS in primary care. Despite long-standing recognition of inappropriate ONS prescribing [33] and the high associated costs [15], as well as potential clinical implications, the review has identified a paucity of rigorous evaluations of interventions targeting this issue. All included studies used an uncontrolled design (Table 1) which limits their capacity to provide a robust evidence-base to inform policy and practice. Notwithstanding this fundamental limitation, the review provides an important summary of current literature to help inform future research. Included studies identified sizeable proportions of patients lacking clinical nutritional assessments and/or receiving

inappropriate ONS prescriptions. This aligns with previous research and confirms the need for targeted interventions [11,34]. Relatively little research has been published on primary care clinicians' views and experiences of providing nutritional care and factors contributing to inappropriate ONS prescribing have yet to be identified [35]. Based on qualitative interviews with healthcare professionals exploring nutritional screening and management practices, plausible factors include: lack of time and resources; lack of knowledge and awareness of malnutrition and appropriate management; and lack of clear roles, responsibilities and procedures within the primary care team for the identification and management of patients with malnutrition [36,37]. Commonly identified components of the interventions included: dietitian prescribing support and clinician education/ training (Table 2). However, intervention descriptions were often poor and information was lacking on how they were developed and delivered. This is consistent with the findings of other related reviews [38,39]. Thus, it was not clear to what extent, if any, these interventions drew on relevant literature. For example, in the studies involving baseline audits of ONS prescribing, there was no reporting on the delivery of feedback which is an integral part of effective audits. A large body of evidence on the effects of audit and feedback interventions on clinicians' professional practice has

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shown that these interventions generally lead to small but potentially important practice improvements, and that their effectiveness may partly depend on how feedback is provided as part of the overall intervention [40]. Failure to consider this evidence when developing and delivering interventions targeting ONS prescribing could have considerable implications on the interventions' effect on clinical practice. Although GPs and community nurses have previously been identified as the main healthcare professionals responsible for identifying and managing patients requiring ONS in primary care [12], dietitians were also involved in a number of studies (Table 2). Despite reported positive impact of dietitian prescribing support on ONS prescribing across a number of studies, information was lacking on the extent of the collaboration as no feedback was reported from the key stakeholders. Collaboration between healthcare professionals in primary care is a key factor in terms of implementation of recommendations stemming from clinical reviews of patients' prescriptions [41]. This is of particular importance in the context of uptake of the recently published GLIM criteria for the diagnosis of malnutrition [9]. These criteria are intended to be relatively simple and easy for clinicians and other health practitioners to apply, with only modest training required to diagnose malnutrition initially, before more comprehensive assessments are undertaken by skilled nutrition practitioners, such as dietitians, to develop individualised care plans [9]. Direct feedback from patients was also largely absent across studies. There may be scope for more active involvement of patients in future research, in line with the concept of patient and public involvement, an area of increasing interest within healthcare research [42]. Most studies included assessments of ONS prescribing, commonly involving guidelines or formularies. However, there was a lack of consistency in the reporting of prescribing-related outcomes. For example, improvements in ONS prescribing were reported either at the level of patient or prescription, and in terms of either absolute reduction in ONS prescribing or reduction in inappropriate prescribing (Table 3). This is a recognised issue in nutrition research [43] and would have hampered the pooling of outcome data had the study designs lent themselves to statistical synthesis. In addition, only one study alluded to underprescribing of ONS whereby a higher proportion of patients deemed at high risk of malnutrition was prescribed ONS postintervention compared to pre-intervention [31]. Previous research has identified that high proportions of older patients with non-volitional weight loss were untreated [44]. In improving appropriate prescribing of ONS, it is important to ensure that underuse of ONS is also assessed. Another important consideration for future related research is the terminology that is used. As previously outlined, a universally accepted definition of appropriate prescribing of ONS is lacking and this was illustrated by the absence of any formal definition in many of the included studies. We have attempted to outline key concepts of appropriate prescribing as they relate to ONS, drawing on established terminology used in the context of medical prescribing. However, further work is needed to develop a consensus-based definition of appropriate ONS prescribing. It would also be important to consider whether ONS prescriptions are labelled as “inappropriate” or “potentially inappropriate”. A key challenge in assessing appropriate ONS prescribing is that full details of patients' nutritional status have not always been available in primary care settings [45]. It is possible that those prescribing ONS in the first instance may have had additional clinical or contextual information about individual patients that was not captured accurately or in sufficient detail in the patients' notes. Given the lack of detailed reporting of how ONS prescribing was reviewed across studies and the sufficiency of the information obtained from prescribing

records, it is difficult to determine what the most suitable terms would have been. Follow-up assessments were limited to short durations and, therefore, the sustainability of intervention effects is largely unknown. There was also a lack of post-intervention clinical assessments in terms of weight gain, BMI, quality of life, morbidity and mortality. This may reflect a historical perspective whereby approaches to improve appropriate ONS prescribing were potentially driven by a cost agenda as opposed to a more holistic strategy to tackle malnutrition using a person-centred approach. In addition, none of the studies measured patient adherence to ONS despite it also being a significant issue with the potential to negatively impact on nutritional outcomes such as weight [46]. It has previously been reported that one in five community-dwelling patients prescribed ONS are non-adherent [47]. In enhancing future-related research, more robust processes need to be adopted during the stages of intervention development, evaluation and reporting. Various frameworks and guidelines exist that could be operationalised to beneficial effect within each of these stages, such as the UK Medical Research Council's framework on developing and evaluating complex interventions [48]. Future research could benefit from the application of implementation science and framing the clinical problem to be addressed as a behaviour (e.g. implementation of ONS prescribing guideline recommendations) in order to allow systematic examination of barriers to, and facilitators of, that behaviour to be identified and targeted as part of an intervention using evidence-based techniques. This type of systematic approach has been applied in previous primary care-based research [49,50]. Comparative studies involving rigorous designs are needed in order to ensure more robust evaluations, reduce risk of bias and strengthen confidence in the findings. These evaluations should ensure inclusion of a comprehensive range of outcomes that are relevant to all key stakeholders (i.e. patients, healthcare professionals, policy makers). There may be scope to use innovative evaluation methods, such as stepped-wedge designs in future studies, thereby, enabling outcome evaluation using routinely collected data [51]. The stepped wedge design has previously been successfully implemented in primary care settings [52,53]. Finally, more detailed reporting of interventions is required. In the current review, this was hindered by the fact that six studies were only published as conference abstracts. Attending to the issues raised in this review relating to methodological rigour could enhance the quality of research in this field and facilitate publication of future research on interventions targeting ONS prescribing in primary care in high quality journals. However, even for studies where full-text evaluations had been published, key information was often lacking in terms of the intervention components and how they were delivered. This has considerable implications in terms of the potential for replication. The TIDieR (Template for Intervention Description and Replication) checklist provides useful guidance that may help to address this [54]. The main strengths of this scoping review are that it provides a broad overview of the available published literature in this area and followed rigorous methods [16]. It has also helped to show that, currently, there is no value in conducting a systematic review on the effectiveness of interventions to improve ONS prescribing in primary care. The findings and discussion points could help in developing an agenda for future research in this field, particularly in terms of defining appropriate ONS prescribing and identifying outcomes to include in future evaluation studies. In the event that trials are undertaken in this area in the future, the review's methods and search strategies may serve to inform the development of a protocol for a comprehensive systematic review that would focus on controlled evaluations. The notable limitations of

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this review were that it was limited to studies published in the English language and no grey literature was searched for. 5. Conclusion This scoping review provides a detailed and systematic overview of interventions aimed at improving appropriate prescribing of ONS in primary care. A range of interventions targeting ONS prescribing in primary care has been evaluated to date, commonly involving dietitians. However, use of controlled experimental designs was lacking. There was also a lack of consistency in terms of how appropriate ONS prescribing was defined and the outcomes that were evaluated in included studies. Future research needs to attend to rigour during the stages of intervention development, evaluation and reporting in order to generate findings which could serve to inform policy and practice relating to ONS prescribing in primary care. Author contributions CC designed the review protocol and led the conduct and writing of the review. RD contributed to study identification, data extraction, and data synthesis. SF contributed to data extraction. PDC contributed to study identification and provided clinical expertise. CAC reviewed drafts of the review and provided clinical expertise. CR contributed to the development of the review protocol and reviewed drafts of the review. All authors reviewed drafts of the review and approved the final submission. Funding None. Conflict of interest None. Acknowledgements inne McCabe, Assistant Librarian, The authors are grateful to Gra RCSI Library for her assistance in reviewing the search strategy. PDC is funded by an Irish Health Research Board grant under a Research Collaborative in Quality and Patient Safety (RCQPS) stream. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.clnu.2019.03.003. References [1] National Collaborating Centre for Acute Care (UK). Nutrition support for adults: oral nutrition support, enteral tube feeding and parenteral nutrition. London: National Collaborating Centre for Acute Care (UK); 2006. [2] Abizanda P, Sinclair A, Barcons N, Lizan L, Rodriguez-Manas L. Costs of malnutrition in institutionalized and community-dwelling older adults: a systematic review. J Am Med Dir Assoc 2016;17(1):17e23. [3] Ruiz AJ, Buitrago G, Rodriguez N, Gomez G, Sulo S, Gomez C, et al. Clinical and economic outcomes associated with malnutrition in hospitalized patients. Clin Nutr 2018. https://doi.org/10.1016/j.clnu.2018.05.016. pii: S0261-5614(18) 30201-30202 [Epub ahead of print]. [4] Elia M, Russell C. Combating malnutrition: recommendations for action. Report from the advisory group on malnutrition, led by BAPEN. 2009. [5] de van der Schueren MA, Wijnhoven HA, Kruizenga HM, Visser M. A critical appraisal of nutritional intervention studies in malnourished, community dwelling older persons. Clin Nutr 2016;35(5):1008e14. [6] Spinewine A, Schmader KE, Barber N, Hughes C, Lapane KL, Swine C, et al. Appropriate prescribing in elderly people: how well can it be measured and optimised? Lancet 2007;370(9582):173e84.

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[7] O'Connor MN, Gallagher P, O'Mahony D. Inappropriate prescribing: criteria, detection and prevention. Drugs Aging 2012;29(6):437e52. [8] Cudjoe A, Dhir RA. Guide to prescribing adult oral nutritional supplements (ONS) in the community. London, UK: Wandsworth Clinical Commissioning Group; 2013. Available from: http://www.wandsworthccg.nhs.uk/aboutus/ wandsworth%20clinical%20effectiveness%20group/adult%20oral%20nutrition %20supplements%20prescribing%20guide%20apr%202013.pdf. [9] Cederholm T, Jensen GL, Correia M, Gonzalez MC, Fukushima R, Higashiguchi T, et al. GLIM criteria for the diagnosis of malnutrition e a consensus report from the global clinical nutrition community. Clin Nutr 2018. https://doi.org/10.1016/j.clnu.2018.08.002. pii: S0261-5614(18)31344X [Epub ahead of print]. [10] Power L, Mullally D, Gibney ER, Clarke M, Visser M, Volkert D, et al. A review of the validity of malnutrition screening tools used in older adults in community and healthcare settings e a manual study. Clin Nutr ESPEN 2018;24:1e13. [11] Kennelly S, Kennedy NP, Rughoobur GF, Slattery CG, Sugrue S. The use of oral nutritional supplements in an Irish community setting. J Hum Nutr Diet 2009;22(6):511e20. [12] Gall MJ, Harmer JE, Wanstall HJ. Prescribing of oral nutritional supplements in primary care: can guidelines supported by education improve prescribing practice? Clin Nutr 2001;20(6):511e5. [13] Cummins P, Thomson M. A dietetic prescribing support initiative leads to significant cost saving efficiencies, by improving the clinical management of oral nutritional supplement prescribing in primary care. Clin Nutr ESPEN 2015;10(5):e204. [14] Todorovic V. Evidence-based strategies for the use of oral nutritional supplements. Br J Community Nurs 2005;10(4). 158, 160, 162e4. [15] Creighton S. Optimisation of prescribing practice for adult oral nutritional supplements (ONS) across London. Pharm Manag 2014;30(1):15e21. [16] Peters MD, Godfrey CM, Khalil H, McInerney P, Parker D, Soares CB. Guidance for conducting systematic scoping reviews. Int J Evid Based Healthc 2015;13(3):141e6. [17] Peters MDJ, Godfrey CM, McInerney P, Baldini Soares C, Khalil H, Parker D. Methodology for JBI scoping reviews. In: Adelaide AE, editor. The Joanna Briggs Institute reviewers' manual. Australia: The Joanna Briggs Institute; 2015. Available from: http://joannabriggs.org/assets/docs/sumari/reviewersmanual_methodology-for-jbi-scoping-reviews_2015_v2.pdf. [18] Tricco AC, Lillie E, Zarin W, O'Brien KK, Colquhoun H, Levac D, et al. PRISMA extension for scoping reviews (PRISMA-ScR): checklist and explanation. Ann Intern Med 2018;169(7):467e73. [19] World Health Organization (WHO). Primary health care e main terminology. 2019. Available from: http://www.euro.who.int/en/health-topics/healthsystems/primary-health-care/main-terminology. [20] Effective Practice and Organisation of Care (EPOC). EPOC taxonomy2015; 2015. Available at: https://epoc.cochrane.org/epoc-taxonomy. [21] Zahra A, Fath MA, Opat E, Mapuskar KA, Bhatia SK, Ma DC, et al. Consuming a ketogenic diet while receiving radiation and chemotherapy for locally advanced lung cancer and pancreatic cancer: the University of Iowa experience of two phase 1 clinical trials. Radiat Res 2017;187(6):743e54. [22] Cummins P, Thomson M, Tyson S. Significant improvement in clinical and cost efficiencies following the implementation of prescribing guidelines for oral nutritional supplement in primary care. Clin Nutr ESPEN 2015;10(5):e206e7. [23] Gilson A, Rochford A. Reducing inappropriate oral nutritional supplement prescribing to fund community dietetic support. Clin Nutr ESPEN 2015;10(5): e204e5. [24] Jones J. Tackling undernutrition through appropriate supplement prescribing. Br J Community Nurs 2003;8(8):343e52. [25] Kennelly S, Kennedy NP, Rughoobur GF, Slattery CG, Sugrue S. An evaluation of a community dietetics intervention on the management of malnutrition for healthcare professionals. J Hum Nutr Diet 2010;23(6):567e74. [26] Ragubeer R, Patel HJ. Pilot to improve the appropriate prescription of oral nutritional supplements within the walsall area. Proc Nutr Soc 2011;70:E272. [27] Welch V, MacBride-Stewart S. The implementation of sip feed contract changes in primary care. Pharmacoepidemiol Drug Saf 2012;21(7):797e8. [28] Kakarlapudi S, Morgan C, Lakin S. Dietetic nutritional prescribing project that delivers improved quality of care, appropriate prescribing, & pound; 400,000 investment into dietetics and a yearly saving of & pound; 816,000 for commissioners. Rev Esp Nutr Humana Diet 2016;20:391. [29] Gratton E, Donovan G. An evaluation of the impact of an integrated dietitianled service on economic, clinical and patient satisfaction outcomes in patients prescribed oral nutritional supplements. Pharmacoepidemiol Drug Saf 2016;25:10e1. [30] Gratton E, Donovan G. Is prescribing of oral nutritional supplements in general practice in line with national guidance? Pharmacoepidemiol Drug Saf 2016;25:9e10. [31] Kennelly S, Kennedy NP, Corish CA, Flanagan-Rughoobur G, GlennonSlattery C, Sugrue S. Sustained benefits of a community dietetics intervention designed to improve oral nutritional supplement prescribing practices. J Hum Nutr Diet 2011;24(5):496e504. [32] National Institute for Health and Clinical Excellence. Nutrition support in adults: oral nutrition support, enteral tube feeding and parenteral nutrition. Clinical Guideline 32. London: National Institute for Health and Clinical Excellence (NICE); 2006. [33] Ponte CD, Lipman AG, Moran CP. Use review of nutritionally complete liquid diets. Am J Hosp Pharm 1978;35(2):159e62.

Please cite this article as: Cadogan CA et al., A systematic scoping review of interventions to improve appropriate prescribing of oral nutritional supplements in primary care, Clinical Nutrition, https://doi.org/10.1016/j.clnu.2019.03.003

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C.A. Cadogan et al. / Clinical Nutrition xxx (xxxx) xxx

[34] Tahim AS, O'Gallagher D. Appropriate monitoring of oral nutritional supplementation: an audit within a large gp practice. Proc Nutr Soc 2011;70:E271. [35] Winter J, McNaughton SA, Nowson CA. Nutritional care of older patients: experiences of general practitioners and practice nurses. Aust J Prim Health 2017;23(2):178e82. [36] Hamirudin AH, Charlton K, Walton K, Bonney A, Albert G, Hodgkins A, et al. ‘We are all time poor’ e is routine nutrition screening of older patients feasible? Aust Fam Physician 2013;42(5):321e6. [37] Ziylan C, Haveman-Nies A, van Dongen EJI, Kremer S, de Groot LCPGM. Dutch nutrition and care professionals' experiences with undernutrition awareness, monitoring, and treatment among community-dwelling older adults: a qualitative study. BMC Nutr 2015;1(1):38. [38] Liljeberg E, Andersson A, Lovestam E, Nydahl M. Incomplete descriptions of oral nutritional supplement interventions in reports of randomised controlled trials. Clin Nutr 2018;37(1):61e71. [39] Ball LE, Sladdin IK, Mitchell LJ, Barnes KA, Ross LJ, Williams LT. Quality of development and reporting of dietetic intervention studies in primary care: a systematic review of randomised controlled trials. J Hum Nutr Diet 2018;31(1):47e57. [40] Ivers N, Jamtvedt G, Flottorp S, Young JM, Odgaard-Jensen J, French SD, et al. Audit and feedback: effects on professional practice and healthcare outcomes. Cochrane Database Syst Rev 2012;6:CD000259. [41] Kwint HF, Bermingham L, Faber A, Gussekloo J, Bouvy ML. The relationship between the extent of collaboration of general practitioners and pharmacists and the implementation of recommendations arising from medication review: a systematic review. Drugs Aging 2013;30(2):91e102. [42] Brett J, Staniszewska S, Mockford C, Herron-Marx S, Hughes J, Tysall C, et al. Mapping the impact of patient and public involvement on health and social care research: a systematic review. Health Expect 2014;17(5):637e50. rez A, Lozano-Montoya I, Volkert D, Visser M, Cruz-Jentoft A. Rele[43] Correa-Pe vant outcomes for nutrition interventions to treat and prevent malnutrition in older people: a collaborative senator-ontop and Manuel Delphi study. Eur Geriatric Med 2018;9(2):243e8.

[44] Arnaud-Battandier F, Malvy D, Jeandel C, Schmitt C, Aussage P, Beaufrere B, et al. Use of oral supplements in malnourished elderly patients living in the community: a pharmaco-economic study. Clin Nutr 2004;23(5):1096e103. [45] Gale CR, Edington J, Coles SJ, Martyn CN. Patterns of prescribing of nutritional supplements in the United Kingdom. Clin Nutr 2001;20(4):333e7. [46] Bruce D, Laurance I, McGuiness M, Ridley M, Goldswain P. Nutritional supplements after hip fracture: poor compliance limits effectiveness. Clin Nutr 2003;22(5):497e500. [47] Hubbard GP, Elia M, Holdoway A, Stratton RJ. A systematic review of compliance to oral nutritional supplements. Clin Nutr 2012;31(3):293e312. [48] Medical Research Council. Developing and evaluating complex interventions: new guidance. London: Medical Research Council; 2008. [49] French SD, Green SE, O'Connor DA, McKenzie JE, Francis JJ, Michie S, et al. Developing theory-informed behaviour change interventions to implement evidence into practice: a systematic approach using the theoretical domains framework. Implement Sci 2012;7:38. [50] Cadogan CA, Ryan C, Francis JJ, Gormley GJ, Passmore P, Kerse N, et al. Development of an intervention to improve appropriate polypharmacy in older people in primary care using a theory-based method. BMC Health Serv Res 2016;16(1):661. [51] Hemming K, Haines TP, Chilton PJ, Girling AJ, Lilford RJ. The stepped wedge cluster randomised trial: rationale, design, analysis, and reporting. Br Med J 2015;350:h391. [52] Dreischulte T, Donnan P, Grant A, Hapca A, McCowan C, Guthrie B. Safer prescribing e a trial of education, informatics, and financial incentives. N Engl J Med 2016;374(11):1053e64. [53] Sharp AL, Hu YR, Shen E, Chen R, Radecki RP, Kanter MH, et al. Improving antibiotic stewardship: a stepped-wedge cluster randomized trial. Am J Manag Care 2017;23(11):e360e5. [54] Hoffmann TC, Glasziou PP, Boutron I, Milne R, Perera R, Moher D, et al. Better reporting of interventions: template for intervention description and replication (TIDieR) checklist and guide. Br Med J 2014;348:g1687.

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