Safely reducing antibiotic prescriptions to help contain antibiotic resistance.
Submitting Institution
Cardiff UniversityUnit of Assessment
Public Health, Health Services and Primary CareSummary Impact Type
HealthResearch Subject Area(s)
Medical and Health Sciences: Medical Microbiology, Public Health and Health Services
Summary of the impact
Research by Cardiff University is contributing to initiatives within the
NHS and across Europe to safely reduce unnecessary antibiotic prescribing
and thus help contain antimicrobial resistant bacteria. Our researchers
conducted observational studies of prescribing patterns linked to local
resistance data and qualitative research with GPs and patients on their
perceptions of acute respiratory tract infections and antibiotic use and
resistance. This enabled the Cardiff team to develop clinician training
and patient education resources (covering issues such as communication
skills, point of care testing, and typical duration of infections) to
reduce unnecessary prescribing. Our trials proved these interventions were
effective, at times cutting prescribing by as much as two-thirds. Our
research has provided the basis for new clinical guidelines, antibiotic
stewardship initiatives and policies, and educational tools for clinicians
and patients that are being used in the UK and internationally.
Underpinning research
Antibiotic prescribing practices and perceptions
Cardiff University researchers, including Chris Butler (Clinical Fellow,
1993; Professor of Primary Care Medicine, 2001-present), Nick Francis
(Clinical Lecturer, 2003-2010; Senior Clinical Research Fellow,
2010-present), Fiona Wood (Lecturer, 2003-2013; Senior Lecturer 2013-
present), Kerry Hood (Senior Lecturer 2002-2007; Reader, 2007-2009,
Professor, 2009-present), Frank Dunstan (Professor of Medical Statistics,
2002-present) and Stephen Rollnick (Research Fellow, 1993; Professor of
Healthcare Communication, 2013-present), have developed and evaluated
effective, evidence-based tools which improve the clinical management of
respiratory tract infections (RTIs) and help to reduce inappropriate
antibiotic use.
Butler and Rollnick provided the earliest insights into clinicians' and
patients' perspectives on why antibiotics were prescribed for sore throats
[3.1]. This research, published in the British Medical Journal (BMJ) in
1998, revealed several drivers for inappropriate prescribing, including GP
perceptions that community antibiotic prescribing was incidental to
resistance (`resistance is not a problem in my practice') and a lack of
tools to support clinicians to change their prescribing habits.
Butler, Dunstan and colleagues then produced the first ever evidence that
showed antibiotic use was linked to antibiotic resistance at a local
(practice) level. Analysing data from urine samples submitted by Welsh
GPs, they found that antibiotic resistance was common in primary care;
patients infected with resistant strains were sicker for longer and
consumed more healthcare resources compared to patients infected with
bacteria sensitive to antibiotic treatment. The research also revealed
that reducing antibiotic prescribing was associated with reduced
resistance at the general practice level [3.2].
In 2003 and 2006 Butler and Francis produced new data on the normal
illness course of upper RTIs in children and acute sore throat in adults.
This data is used to help set realistic expectations about likely illness
course. Butler, Francis, Wood and colleagues also conducted qualitative
research to describe the perceptions of both general practitioners (GPs)
and the general public regarding antibiotic use and resistance, including
interviews with GPs about their rationale for using broad-spectrum
antibiotics (which generally cause greater `collateral damage') and
parents about their information needs regarding their child's RTI.
Butler (as a work package leader), supported by others from Cardiff,
played a central role in the EU-funded FP6 project `Genomics to combat
resistance to antibiotics in Community-acquired lower respiratory tract
infections in Europe' which ran from 2006 to 2011. This project provided
evidence that there is `unhelpful' variation in the antibiotic prescribing
practices of doctors between 14 European sites. The project has produced
the most reliable data so far on the prognostic value of signs, symptoms
and point of care testing for RTIs in primary care [3.3], as well as trial
data on the effectiveness of antibiotics in adults with acute cough [3.4].
Evaluation of tools
From 2005-2011 the Cardiff team collated the insights from their
empirical investigations. Informed by complementary research strengths in
motivational interviewing, shared decision making, and other behaviour
change theories, the team developed a set of communication skills
strategies to help clinicians adopt a non-prescribing approach while
enhancing patient empowerment and maintaining patient satisfaction. Output
from this work included a communications skills training programme [3.3],
a blended learning package (http://www.stemmingthetide.org/) [3.6], and
interactive patient information booklets, supported by online clinician
training, for children (www.whenshouldiworry.com) [3.5] and adults [3.7]
with RTIs.
The team also led or played a central role in four major trials of the
tools developed by the research. The tools under investigation included
`blended learning' (combining multi-media and interactive learning),
enhanced communication skills training, point of care testing, and
interactive booklets. The trials demonstrated statistically significant,
clinically important, safe, and acceptable reductions in antibiotic
prescribing through use of the tools [3.3, 3.5-3.7]. The paper describing
the blended learning (STAR) study was one of six papers internationally
shortlisted for the BMJ Research Paper of the Year Award 2013.
References to the research
Note: All Cardiff researchers in bold
Key References
1. Butler CC, Rollnick S, Pill R, Maggs-Rapport F,
Stott N. Understanding the culture of prescribing: Qualitative study
of general practitioners' and patients' perceptions of antibiotics for
sore throats. British Medical Journal. 1998;317(7159):637-42. doi:
http://dx.doi.org/10.1136/bmj.317.7159.637
2. Butler CC, Dunstan F, Heginbothom M, Mason B,
Roberts Z, Hillier S, et al. Containing antibiotic resistance:
decreased antibiotic-resistant coliform urinary tract infections with
reduction in antibiotic prescribing by general practices. The British
Journal of General Practice. 2007;57(543):785-92
http://www.ncbi.nlm.nih.gov/pubmed/17925135
3. Cals JW, Butler CC, Hopstaken RM, Hood K, Dinant GJ.
Effect of point of care testing for C reactive protein and training in
communication skills on antibiotic use in lower respiratory tract
infections: cluster randomised trial. BMJ. 2009;338:b1374 doi:
http://dx.doi.org/10.1136/bmj.b1374
4. Butler CC, Hood K, Verheij TJ, Little P, Melbye H, Nuttall
J, et al. Variation in antibiotic prescribing and its impact on
recovery in patients with acute cough in primary care: prospective study
in 13 countries. British Medical Journal. 2009;338:b2242 doi:
http://dx.doi.org/10.1136/bmj.b2242
5. Francis NA, Butler CC, Hood K, Simpson S,
Wood F, Nuttall J. Effect of using an interactive booklet
about childhood respiratory tract infections in primary care consultations
on reconsulting and antibiotic prescribing: a cluster randomised
controlled trial. BMJ. 2009;339:b2885 doi:
http://dx.doi.org/10.1136/bmj.b2885
6. Butler CC, Simpson SA, Dunstan F, Rollnick
S, Cohen D, Gillespie D, et al. Effectiveness of
multifaceted educational programme to reduce antibiotic dispensing in
primary care: practice based randomised controlled trial. BMJ.
2012;344:d8173. doi: http://dx.doi.org/10.1136/bmj.d8173
7. Little P, Stuart B, Francis N, Douglas E, Tonkin-Crine S,
Anthierens S, Cals JW, Melbye H, Santer M, Moore M, Coenen S, Butler C,
Hood K, Kelly M, Godycki-Cwirko M, Mierzecki A, Torres A,
Llor C, Davies M, Mullee M, O'Reilly G, van der Velden A, Geraghty AW,
Goossens H, Verheij T, Yardley L; on behalf of the GRACE consortium.
Effects of internet-based training on antibiotic prescribing rates for
acute respiratory-tract infections: a multinational, cluster, randomised,
factorial, controlled trial. Lancet. 2013 Oct 5;382(9899):1175-1182. doi:
http://dx.doi.org/10.1016/S0140-6736(13)60994-0 Epub 2013 Jul 31.
Key funding
SAVIT Study: The effect of intranasal sodium cromoglycate on symptoms of
suspected acute viral URTI in children. Butler. MRC (1999-2000).
£98,012. www.controlled- trials.com/ISRCTN21562211/
The link between antibiotic prescribing and resistance in the community:
definition, dynamics, and influences. Howard, Palmer, Magee, Dunstan
(2000-2003). NHS Wales Office of Research and Development for Health and
Social Care. £199,713.
Antibiotic Resistance in Community Urinary Tract Infection. Palmer,
Butler, Dunstan. Wellcome Trust (2002-2005). £271,9320.
The development and evaluation of an interactive leaflet for children
with acute respiratory tract infections. Butler, Simpson,
Hood, Francis. MRC (2005-2009). £307,860.
STAR: Stemming
the Tide of Antimicrobial Resistance. Butler, Evans, Hood,
Simpson, Palmer, Rollnick, Dunstan. MRC
(2006-2009). £509,753.
GRACE: Genomics to combat resistance against antibiotics in
community-acquired lower respiratory tract infections in Europe. Butler,
Hood. EC FP6 project (2006-2011). Total project grant €11.5
million; £804,740 to Cardiff University.
Details of the impact
The findings and recommendations of the Cardiff research team have
provided the basis for new educational materials, training programmes and
other decision management tools used by clinicians in the UK and abroad.
The Cardiff research has also informed new clinical guidelines in the UK
and elsewhere on the management of RTI. The widespread dissemination of
Cardiff's research is helping to improve antibiotic stewardship across
Europe. Our four trials (see Section 3) all demonstrated the effectiveness
of different tools to reduce antibiotic prescribing. The reductions ranged
from 32% to 67% in trial participants and a 4.2% reduction in overall
antibiotic prescribing (and a 5.5% reduction in antibiotic dispensing
costs) over a one-year period at the whole general practice level. This
equates to a saving of £830 per annum for an average sized UK general
practice. Given the widespread adoption of Cardiff's tools and training in
NHS initiatives to reduce GP antibiotic prescribing (see below), if 50% of
all UK GP practices achieved just half of the average savings observed in
the trials, the direct costs savings across the country since publication
of the NICE guidelines would total £9 million.
Guidelines
The NICE guidelines on managing acute RTI were published in 2009 and were
distributed to all GPs in the UK. They highlighted the importance of
eliciting patient expectations; GPs are encouraged to achieve a shared
understanding regarding the management and treatment of the infection.
This recommendation stems directly from the Cardiff research, which is
cited in the NICE publication [5.1]. Aspects of Cardiff's research have
also informed a revision of the Dutch national guidelines on RTIs [5.4].
Patient educational materials
In 2009 the Cardiff team published the results of a trial revealing that
use of the interactive booklet for children about RTIs, which was
developed by the Cardiff team, resulted in a two-thirds reduction in
antibiotic use [3.5, see `What this study adds' summary, p7]. The results
were picked up by the UK medical media, including Pulse, Healthcare Today
and Onmedica; the publicity stimulated widespread uptake of the booklet
around the UK. The booklet has been available for purchase at the Royal
College of GPs bookshop since 2010. Over 90,000 copies have been purchased
by or sent to general practices since 2009. In September 2009, for
example, NHS Forth Valley highlighted the `When Should I Worry?' booklet
as a potential aid to management of self- limiting upper respiratory
infections through the Whole System Working initiative in 2009-10. 27,000
copies of the booklet have been distributed to practices to date [5.2]. In
2012, Welsh Government sent 30,000 copies to all general practices in
Wales as part of European Antibiotic Awareness Day activities [5.3].
Training clinicians
The evaluation of Cardiff's training package showed that communication
skills training (to improve interactions with patients and enhance their
experience) and the promotion of a point-of-care blood test, used alone or
in combination, led to significant reductions in antibiotic prescribing.
The results of this study led directly to a change in the Dutch national
guidelines on lower respiratory tract infections; a training package on
the updated guidelines was sent to 11,000 GPs [5.6] and made freely
available online [5.4, 5.5]. The study also helped convince the Dutch
health insurance system to pay for C-reactive protein (CRP) point of care
testing [5.6].
Cardiff developed a blended learning package (e-learning,
practice based outreach, experiential learning, and reflections) about
antibiotic prescribing for RTIs. Research demonstrated this approach
reduced practice-level antibiotic prescribing, not just in those patients
included in the trial. The Cardiff team's research, including the learning
package, formed the basis of the Royal College of General Practitioners
Managing Acute Respiratory Tract Infections (MARTI) course, which by
December 2012 had been completed by over 4,300 clinical users and results
in an average 24% increase in test scores between pre and post course
evaluation [5.7]. A contract has just been signed where Cardiff's SME
partners involved in the trial of the blended learning are investing
£50,000 in further development and its commercialisation. Cardiff's
research has influenced national and international antimicrobial
stewardship programmes and campaigns. For example, Cardiff's interactive
booklet for children and training in its use, and the MARTI module form
part of the TARGET antibiotic toolkit [5.8], which was developed in 2012
by the Antimicrobial Stewardship in Primary Care collaboration (ASPIC) and
has been accessed by more than 5,400 unique users since November 2012.
Public awareness and policy
The Cardiff team's development and trial of the blended learning package
were picked up by local and national media. Articles in The Telegraph
[5.9] and Professor Chris Butler's contributions to discussions on Radio
4's Women's Hour [5.10], Radio 4's Inside Health, and BBC Wales's Jason
Mohammed Show all helped to disseminate the message about reducing
antibiotic prescribing for RTIs to the general public. Butler, Francis and
Stanton also advise the Health Protection Agency, the Department of
Health, the Advisory Committee on Antimicrobial Resistance and Healthcare
Associated Infection, and the Welsh Antimicrobial Resistance Programme.
Sources to corroborate the impact
- NICE clinical guideline on Respiratory Tract Infections, July 2008:
www.nice.org.uk/nicemedia/pdf/CG69FullGuideline.pdf Corroborates the
importance of Cardiff research in informing UK clinical guidelines.
Cardiff research directly cited (pp.14, 88, 93).
- Statement from Clinical Lead, NHS Forth Valley. Confirms the use and
usefulness of the `When should I worry?' interactive booklet developed
by Cardiff in NHS Forth Valley.
- Corroborative statement from Head of Welsh Antimicrobial Resistance
Programme, Public Health Wales, about the use of the interactive booklet
in Welsh General Practice.
- Dutch Primary Care Guideline on Acute Cough 2013:
http://nhg.artsennet.nl/kenniscentrum/k_richtlijnen/k_nhgstandaarden/Samenvattingskaartje-NHGStandaard/M78_svk.htm Confirms the influence of the Cardiff research in the updating of
guidelines for training Dutch GPs. Cardiff research directly cited
(Notes 18, 34, 37 and references). [Translated version saved as a pdf on
11/04/2013].
- Educational website for Dutch GPs: http://www.acutehoest.nl/praktijk.
Confirms Cardiff research as informing the education and training for
Dutch GPs on antibiotic prescribing for respiratory tract infections.
Cardiff research directly cited in Literature section. [Translated
version saved as a pdf on 11/04/2013].
- Corroborative statement from Assistant Professor, Maastricht
University Medical Centre about the impact of the Cardiff research on
Dutch clinical guidelines on lower respiratory tract infections and
health insurance reimbursements.
- RCGP online course - Managing Acute Respiratory Tract Infections
http://elearning.rcgp.org.uk/course/info.php?id=17&nopopup=1
Confirms Cardiff research informed Royal College of General Practitioner
guidance on patients presenting with acute ear pain, acute sore throat,
sinusitis and acute cough. Cardiff research directly cited in References
section. [Saved as a pdf on 11/04/2013].
- RCGP TARGET antibiotic prescribing toolkit:
http://www.rcgp.org.uk/clinical-and-research/target-
antibiotics-toolkit/training-resources.aspx. Corroborates the use of
Cardiff research in the antibiotics training and resources for UK GPs.
Cardiff research directly cited in `Training Resources' and `Patient
information leaflet'
http://www.rcgp.org.uk/clinical-and-research/target-
antibiotics-toolkit/patient-information-leaflets.aspx sections [Saved as
a pdf on 11/04/2013].
- `GPs could prescribe 1.6m fewer antibiotics' The Telegraph, 09
Feb 2012. Article in The Telegraph reporting Cardiff research:
www.telegraph.co.uk/health/healthnews/9071706/GPs-
could-prescribe-1.6m-fewer-antibiotics.html [Saved as a pdf on
11/04/2013].
- Woman's Hour, Radio 4, 16/08/2011.
http://www.bbc.co.uk/programmes/b0135z1k Professor Butler provides
expert comment on antibiotic resistance.