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Oliver J. Dyar, Bojana Beovic, Vera Vlahovic-Palcevski, Theo Verheij & Céline
Pulcini
To cite this article: Oliver J. Dyar, Bojana Beovic, Vera Vlahovic-Palcevski, Theo Verheij & Céline
Pulcini (2016): How can we improve antibiotic prescribing in primary care?, Expert Review of Anti-
infective Therapy, DOI: 10.1586/14787210.2016.1151353
To link to this article: http://dx.doi.org/10.1586/14787210.2016.1151353
Article views: 14
DOI: 10.1586/14787210.2016.1151353
How can we improve antibiotic prescribing in primary care?
Oliver J. Dyar1, Bojana Beovic2, Vera Vlahovic-Palcevski3, Theo Verheij4, Céline Pulcini5*,
1
Global Health - Health Systems and Policy (HSP): Improving the use of medicines, Dept of
Sweden
2
Department of Infectious Diseases, University Medical Centre Ljubljana and Faculty of
E-mail: celine.pulcini@univ-lorraine.fr
* Corresponding author
Summary
Outpatient antibiotic use represents around 90% of total antibiotic use, with more than half of
professionals’ behaviour, and modifying the healthcare system. In this review, we present a
broad perspective on antibiotic stewardship in primary care in high and high-middle income
country settings, focussing on studies published in the last five years. We present the limitations
of available literature, discuss perspectives, and provide suggestions for where future work
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should be concentrated.
antimicrobials, is leading to increased morbidity, mortality and healthcare costs [1]. Antibiotic
use is the main driver for the development and spread of antibiotic resistance, and the vast
consumption accounted for between 85 to 95% of total antibiotic use in 2012 in the European
Union, according to countries contributing data on both ambulatory and intra-hospital antibiotic
use to the European Centre for Disease Prevention and Control (ECDC) [2]. The main
prescribers of antibiotics in primary care settings are general practitioners (GPs), paediatricians
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and dentists, but in many countries a growing number of prescriptions are written by nurses,
midwives and pharmacists, typically for specific patient groups or infections [3].
or inappropriate. For both adults and children, misuse has been most often reported in acute
respiratory infections, which usually represent two-thirds of all infections with which patients
are seen in primary care [4,5]. The rate of unnecessary prescribing for respiratory infections
(RTIs) for which antibiotics are rarely indicated ranges from one half to 90% [4-7]. Less is
known about inappropriate or unnecessary prescribing for other types of infections. French
authors recently reported that only 20% of prescriptions for urinary tract infections (UTIs) were
compliant with guidelines [8]. For skin infections, authors from Colorado (USA) reported that
methodologies used to collect and aggregate data. Nevertheless, it is clear that there are large
fold difference between the countries with the highest and the lowest consumption [2]. The
outpatient antibiotic use in the USA, measured in prescriptions per 1000 inhabitants per year,
is comparable to the highest consumers in Europe [10]. There are even greater variations in
antibiotic prescribing between prescribers in the same country, and this is a strong rationale for
improving antibiotic prescribing practices in ambulatory care [12]. Since then, a few narrative
and systematic reviews have focussed on different aspects of antibiotic stewardship in the
outpatient setting [13-18], the most recent of which included articles published up until
In this narrative review, we will describe the global context of antibiotic prescribing in
improve antibiotic use. We will do this from a purposefully broader perspective than previously
published reviews. In order to present the latest evidence and developments, we mostly discuss
articles published between 2010 and 2015. Our target audience are practitioners and researchers
in primary care settings in high and high-middle income country settings; for this reason, our
review is restricted to articles relevant to this context. We do recognise the global need for
collating evidence relevant to less developed settings, and we acknowledge that such data is
part of a more general programme, and may be implemented locally and/or nationally. In many
countries we cannot yet speak about nationwide antibiotic stewardship programmes, but merely
more or less coordinated activities. The countries with the lowest outpatient antibiotic use, such
programme for primary care is planned for the coming year. Antibiotic prescribing guidelines
are widely used, and prescription habits are monitored in general in primary care, but not for
antibiotics in particular. Strong medical education efforts also underlie the prudent use of
antibiotics. The Swedish model, known as the Strama network, relies on multi-sectorial
programmes targeting primary care prescribers are in place, combining different interventions,
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prescribing tend to be multifaceted, and combine physician, patient and public education [12].
Importantly, we are now starting to see a growing number of reports from ‘real world
improvements in antibiotic usage across large populations [19]. In a recent systematic review
focussing on RTIs, 77% of 87 interventions contained more than one element, most commonly
The authors in the 2005 Cochrane review concluded that the effectiveness of
interventions depended largely on prescribing behaviour and on the barriers to change [12].
This indicates that the design of interventions should be based on behavioural strategies [20].
The local cultural context also has an important influence on physicians and patients’
behaviours. Hofstede's model of cultural dimensions, one of the most popular models assessing
cultural differences, has been used to explore the differences in outpatient antibiotic use in
European countries. A positive correlation was found between power distance index,
which is a marker of a hierarchical society, and outpatient antibiotic consumption, including
self-medication. Antibiotics were also used more frequently in countries with high index of
uncertainty avoidance, i.e. countries in which people and organisations have a low tolerance for
interventions both at the provider-level and at the level of the healthcare system.
broader package of continuing medical education for prescribers. Educational sessions can
involve training in core principles of prudent antibiotic usage, introductions to new supporting
tools (such as guidelines and point of care tests), and training in communication with patients.
Several recent major studies have shown positive outcomes on antibiotic prescribing in
response to educational interventions, although the sizes of the effects have generally been quite
modest [22-26]. The STAR programme in the UK developed internet-based resources and in-
person training, as well as practice-specific feedback, and led to a 4.2% reduction in the adjusted
oral antibiotic prescribing rate compared with control practices [22]. Respondents in a
qualitative assessment of the programme reported that the most effective components were the
up to date research evidence, the training in communication skills, and the feedback on their
own practice’s antibiotic dispensing rates and resistance patterns [23]. The GRACE- INTRO
study included one intervention arm that received internet-based communication skills training,
antibiotic prescribing rates for RTIs [24]. Qualitative and quantitative analyses of participating
GPs and patients showed high levels of satisfaction with the communication skills intervention,
with GPs perceiving reducing antibiotic prescribing as more important and less risky after the
Importantly, a small number of studies have recently shown that educational sessions
improvements in antibiotic usage that are sustained over two to four years [27,28], and even in
response to single seminars [29]. We now have examples of educational interventions that are
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both low-cost and easily scalable, as well as interventions that have long-term effects on
prescribing.
Guidelines are an important way to support prescribers in translating the best evidence
into clinical practice. Many countries have issued national guidelines to help improve antibiotic
prescribing in both inpatient and outpatient care, however there have been very few recent
assessments of the effects of national guidelines on prescribing behaviour. Three studies in the
USA found that publication of national guidelines had minimal or no impact on rates of
antibiotic prescriptions for acute otitis media, otitis externa or sinusitis, although there were
some improvements in antibiotic selection [30-32]. Stronger evidence exists for the
implementation of guidelines at a regional or local level [33]. One study conducted at two out
of hours primary care centres in Belgium provides insight into the local implementation and
clinical adoption of a guideline for treatment of UTIs [34]: in addition to the distribution of
posters and information leaflets at the centre, individual prescribers were emailed a copy of the
guideline before starting clinical sessions with patients. This led to a significant rise in the
proportion of UTIs treated with guideline appropriate antibiotics; however, a follow-up review
after a 17 month washout period found that guideline adherence had returned to near baseline
levels.
Clinical decision support tools and systems (CDSS) have become more prevalent over
the past decade, particularly in primary care settings where electronic health records and e-
prescribing are common. A recent systematic review examined the effects of CDSS on
antibiotic prescribing in primary care, identifying seven studies which all focussed on RTIs and
were all conducted in the USA: there was great variation in the rates of triggering of the CDSS
(2.8% to 62.8% of eligible encounters), and five of the studies reported a slight to moderate
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effect on improving antibiotic prescribing behaviour [35]. These improvements were mostly
associated with increased selection of recommended antibiotics, but not reductions in rates of
antibiotic prescribing. In the UK, a CDSS was integrated into the electronic health record
patients with RTIs as part of the eCRT study [36]. Compared with 51 control practices, there
was a slight reduction in the rate of consultations involving an antibiotic prescription (1.9%),
and a larger reduction in the rate of antibiotic prescription for RTIs (9.7%). GPs in the
intervention group were satisfied with the CDSS and reported higher levels of self-efficacy in
managing patients with RTIs according to recommended guidelines; actual usage of the CDSS,
however, was highly variable and was lower than expected by the investigators [36,37].
prescibes a course of antibiotics, but specifies that they should only be taken if symptoms persist
or deteriorate after a given time period (typically around 48 hours). Depending on how
prescriptions are handled within the particular health system, the patient may either be unable
to collect the prescription or unable to have the antibiotics dispensed before this time period has
elapsed; in other settings, they may be able to collect antibiotics on the same day that they
visited the clinician, but are simply advised to delay starting taking the antibiotics. These health
system differences may impact on the value of delayed prescribing for a particular setting.
prescriptions for acute RTIs [38]. They reported that the use of delayed prescriptions led to
complication rates. Overall patient satisfaction was slightly lower for delayed antibiotics than
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In an observational study of patients with sore throat in the UK, Little et al. found a low
overall rate of complications for delayed prescribing (1.4%, mostly otitis media, sinusitis) [39].
complications compared with no antibiotics, and were more effective than immediate
antibiotics at reducing reconsultations. In another study in patients with all types of acute RTIs
in the UK, different strategies for delayed prescription were compared with either no antibiotics
or immediate antibiotics [40]. Symptom severity, duration of symptoms, and patient satisfaction
were similar across all groups, but delayed prescription and no antibiotics resulted in lower
antibiotic use and lower levels of patient belief in the need for antibiotics, compared with
immediate antibiotics.
Delayed prescribing is now recommended in some national guidelines, such as the UK.
Despite this, observational studies have reported low usage of delayed prescriptions in practice
[41,42]. A qualitative study with GPs in the UK suggested that they mostly use delayed
responsibility to patients, and the use of delayed prescribing was felt to communicate
conflicting messages to patients about the general efficacy of antibiotics for respiratory tract
infections [42]. Mixed opinions were also found among Norwegian GPs, with some viewing it
is as an opportunity to educate patients and engage in shared decision making; in contrast, those
who were more negative towards delayed prescribing viewed it mainly as a tool to use for
patients who were putting them under pressure to prescribe antibiotics [43]. Interestingly, 89%
of patients who received a delayed prescription in the same Norwegian study said they would
3.1.4. Patient materials: dedicated forms to prescribe antibiotics, non-prescription pads and
To the best of our knowledge, antibiotic prescriptions in primary care are almost never
individualized on a specific prescription form given to the patient [17]; the patient usually
receives a prescription with all the drugs put together. The idea of using a dedicated form on
which only antibiotics are prescribed is currently being discussed in France, since it has several
theoretical advantages: highlighting that antibiotics are special drugs, being a tool facilitating
the patient-doctor relationship (since educational messages can be added to the form), and
ultimately decreasing antibiotic use. It would also enable patients to easily identify the
Non-prescription pads are currently used in several countries [17], including the UK.
The pad looks like a normal prescription pad and includes ‘non-prescription’ forms that can be
given to patients who present with an infection, but who do not need a prescription for
antibiotics. The forms provide physicians with an aid to explain why antibiotics are not part of
treatment for a particular condition, and may also include descriptions of the usual duration of
symptoms, such as cough or fatigue, and suggestions of symptomatic therapies [13]. This
educational and communication tool can be tailored to a specific clinical situation, facilitates
the patient-doctor relationship, and can replace a drug prescription in countries where patients
Patient information leaflets have also become increasingly popular in primary care over
the past decade. These can be used as a reference by clinicians during consultations, and patients
are able to take them away to review later. The EQUIP study in the UK showed that antibiotic
prescribing rates for children with RTIs could be reduced with the help of a patient information
booklet [45]. An in depth qualitative follow-up with GPs and parents concluded that the booklet
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was easy to use, with parents valuing most the information on recognising signs of serious
illness and on the usual duration of illness [46]. Although many GPs reported increased
knowledge and confidence as a result of using the booklet, some also mentioned important
barriers to use, such as a lack of time and difficulty in modifying their style of consultation.
Several recent studies have included patient information leaflets as part of a broader set of
in conjunction with training in communication [26]. Almost all patients who received the
booklet recounted using it, and these patients later reported the highest levels of satisfaction and
enablement across all the study intervention groups (which included a point of care testing arm),
consulting rooms decreased inappropriate antibiotic prescribing for RTIs (20% absolute
percentage reduction) [50]. In the letter, the individual clinicians stated personal commitments
to avoiding inappropriate antibiotic prescribing for acute respiratory infections. The efficacy of
this innovative strategy likely relies on the psychological tendency for people to prefer to act in
ways that are consistent with their previous commitments, particularly when these are public.
This strategy is currently implemented nationwide in hospitals in France, with the support of
the French Infectious Diseases society, and will probably be rolled out in all settings in France
Rapid antigen diagnostic tests (RADTs) have long been recommended in some countries
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to identify the presence of group A streptococcal pharyngitis; however, their use is quite
context-dependent. In a pragmatic parallel group randomised control trial in the UK, Little et
al. found that using a clinical score for patients with a sore throat reduced antibiotic usage
compared with a strategy of delayed prescribing, but that there was no additional benefit from
also using a rapid antigen test in conjunction with the clinical score [51]. In France, RADTs are
Two meta-analyses have been published on the effects of POC CRP testing on reducing
antibiotic use in patients with upper or lower respiratory tract infections in primary care [53,54].
Both analyses concluded that CRP testing reduces the rate of antibiotic prescriptions at the
recovery; however, there was a high level of heterogeneity among the individual studies
included. A recent narrative review by Cooke et al. reports that GPs and patients find the CRP
POC test acceptable, and that its use is economically justifiable in high- income country settings
[55]. The authors caution, though, that it remains unclear to what extent CRP testing can
distinguish between viral and bacterial infections; indeed most studies show that CRP testing
behaviour, and selective reporting is a powerful antibiotic stewardship tool that is probably
underused. Studies conducted among GPs have demonstrated that the antibiotics reported by
the microbiology laboratory are preferentially prescribed [56]. Moreover, a randomised case-
vignette study conducted among French doctors training in general practice showed that
selective reporting improved the appropriateness of antibiotic prescriptions for urinary tract
antibiotic use in primary care, and are currently used for national reporting [57]. As part of the
HAPPY AUDIT project, a group of international experts reached consensus through a modified
Delphi method on 41 quality indicators for the diagnosis and treatment of respiratory tract
infections in primary care [58]. Out of these indicators, 14 were on the decision to start antibiotic
treatment (e.g. proportion of patients with lower RTI and CRP <20 mg/L who are treated with
antibiotics) and 27 were on the choice of antibiotic (e.g. proportion of patients with acute
the diagnostic process had been proposed initially, but none were included in the final selection
due to a lack of agreement. In a follow-up study, 58 Danish GPs were asked if they agreed on
the 41 indicators; none of the indicators were agreed on by all of the GPs, and only 33 of the 58
GPs agreed on more than 50% of the indicators [59]. Almost all indicators published in the
literature need data on clinical diagnoses, even though some countries (such as France and
currently working on a consensual inventory of quality indicators assessing antibiotic use in the
The increasing use of electronic health records in primary care settings has facilitated
data capture of prescriptions and the ease with which such data can be converted into feedback
for prescribers. Many recent studies have included some aspect of prescription feedback as part
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of a package of interventions, providing data either at the level of the individual or primary care
prescriptions was sufficient to cause improvements in guideline adherence across 140 Swiss
primary care practices in the context of newly developed guidelines for both respiratory tract
infections and urinary tract infections [62]. Individual feedback was provided to prescribers in
24 primary care practices in the USA in a study focussing on improving adherence to otitis
media management guidelines [63]. This monthly feedback had a stronger effect on
improvements in care than a clinical decision support tool that was trialled at the same time.
Studies by Gerber et al. in paediatric primary care practices in the USA have highlighted the
importance of continuing audit and feedback in order to sustain improvements in the longer
term: initially, reductions were seen in the use of non- guideline broad-spectrum antibiotics for
prescription feedback [64]. A follow-up study after 18 months without audit and feedback then
showed that broad-spectrum antibiotic use had returned to baseline levels in the intervention
practices [65].
3.1.10. Restrictive antibiotic prescribing measures
This topic has been recently reviewed [17]. Implementing restrictive measures in the
outpatient setting is not easy, and few countries have done so. As examples, in Slovenia,
primary care prescribers pay a fine if certain antibiotic prescriptions do not comply with existing
national guidelines (e.g. prescriptions that inappropriately include amoxicillin- clavulanic acid,
Institute is auditing medical records in order to enforce this policy [66]. In Turkey, specific
antibiotics cannot be prescribed without approval from an infectious diseases specialist. In the
Netherlands, insurance companies look at prescription rates and types of antibiotics; when the
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use of second-choice agents is above a certain limit (based on national/regional averages), this
can have financial consequences for the primary care practice involved in the form of reduced
budgets.
Prescribers and primary care practices are subjected to a number of rules and regulations
that may have an impact on their antibiotic prescribing behaviour [67]. Quite surprisingly, this
topic has not been extensively studied so far, even though changing these systems might have
quite a large, widespread and sustainable impact on antibiotic consumption. The interventions
we describe in this section are more complex than interventions at the level of the provider; for
instance, they may require a far broader group of stakeholders to be involved in decision-
making, and their implementation may take a comparatively longer time. This may partly
explains the limited number of published assessments of their effectiveness so far. The recent
World Health Assembly commitment that many countries have made to developing national
action plans for combating antibiotic resistance may help stimulate research efforts into health
system-level interventions.
3.2.1. Over-the-counter antibiotics
In many countries, antibiotics are available without any prescription (i.e. over-the-
counter), from pharmacies, the Internet, family, friends or at home [67-69]; it is estimated that
19–100% of antimicrobial use outside of northern Europe and North America is non-
prescription based [68]. When this practice is legally prohibited and the laws are appropriately
enforced, antibiotic use is reduced [68-70]. There are several countries in which non-
prescription use is now illegal, but in which the practice remains widespread (for example,
Spain and Greece) [71]. As a general rule, antibiotics should not be available without a
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prescription, and a regulated list of authorised and adequately trained antibiotic prescribers
Unit dispensing of antibiotics (i.e. the pharmacist gives the exact number of antibiotic
pills to the patient, according to the prescription) has been associated with a lower risk of future
self-medication with leftover antibiotics [72]. This measure is already in place in some countries
(such as the UK, the Netherlands and the USA), and is under evaluation in others (for example,
France).
Limiting the number of antibiotics available in the outpatient setting, or increasing their
price, might reduce antibiotic use [67]. Monnet et al. found that the more oral antibacterial trade
names (whether generic or branded versions) that are on the market, the higher the outpatient
studies.
The relationship between the price of antibiotics and antibiotic use is complex, and
depends on the healthcare system regulation. In countries where patients pay partly or totally
for their own medicine, it is likely that when prices go down, products become affordable for a
larger proportion of the population, which leads to increased consumption; this association was
was seen after a reimbursement reform was introduced, making fluoroquinolones less expensive
[76]. Conversely, a reduction in reimbursement for antibiotics can lead to decreased use [69,77].
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Two studies, conducted in Denmark and in Germany, have also shown that generics can
lead to increased antibiotic use, either by increasing the number of marketed versions of the
drug and/or by decreasing the price of the antibiotic [77,78]. Interestingly, the incentives were
different in both countries: Danish patients receive a relatively low reimbursement for
outpatient medication, whereas German ambulatory care physicians are generally self-
employed, and the national health insurance reimburses fixed budgets for pharmaceuticals.
Prescribing should be separated from dispensing of antibiotics [67], since there is a clear
motivation to increase prescribing in situations when prescribers can sell or dispense antibiotics
for profit, such as China and Switzerland. In these countries dispensing physicians can increase
their revenues by inducing drug consumption [67]. “Zero-markup” schemes specifically for
antibiotics may weaken the economic incentive, and are now being implemented in China;
unfortunately, many healthcare institutions have become heavily reliant on profits from
countries in recent times, such as Taiwan and South Korea, and has led to reduced drug
expenditure [69].
capitation or salary. These systems can have a great influence on prescribing practices [67], and
it has been shown in a European study that a capitation system is associated with decreased
antibiotic use [75]. An interventional study conducted in China further showed that
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3.2.6. Pay-for-performance
incentives are given to prescribers when they meet specific quality of care targets, including
systems is debated, however, and should be carefully assessed in each specific context [81].
and healthcare professionals) has been used as an instrument to improve the quality of care
[67]. Existing evidence shows this has mixed effects, and may be useful in certain settings [82].
Visiting a doctor for a self-limiting infection increases the chances of being prescribed
an antibiotic. In some countries, such as the Netherlands, primary care providers are not
responsible for issuing sick certificates. Instead, sickness certification is carried out by fully
independent dedicated doctors and nurses, who are not involved in actual diagnosis and
treatment of patients. In other countries, such as France and Slovenia, a certificate is arranged
by the patient’s GP and is usually needed as soon as possible. Such differences might be
contributing to the existing variations in outpatient antibiotic use seen across countries.
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representatives to prescribers are risk factors for increased antibiotic use [14,67,74]. In their
European-wide cross-sectional study, Blommaert et al. found that the presence of restrictions
on the conduct of pharmaceutical companies towards physicians was associated with less
antibiotic use at the country level [74]. Many countries are now implementing restrictions on
these practices.
the community, pharmacists are ideally positioned as frontline healthcare providers to promote
prudent antibiotic use. Similarly, there is a growing understanding of the potential roles that
nurses may be able to take on within antibiotic stewardship programmes, both inside and
outside of hospitals. Whilst it is clear that nurses and pharmacists should be able to
contribute to antimicrobial stewardship in primary care in many ways, a detailed assessment
UTIs and sore throats, and play an important role in patient education, particularly in explaining
when antibiotics are useful and how antibiotics should be taken. In the UK, patient access to
instructions for uncomplicated UTIs [84]. Recently, pilot projects have been launched in 3 states
in the USA, stimulating collaboration between physicians and community pharmacists to treat
patients with influenza and group A streptococcal pharyngitis. Under this model, community
pharmacists are entitled to use RADTs to guide clinical decision-making and to initiate
treatment under a physician-led, evidence-based protocol [85]. These initiatives show how
strong collaboration between physicians and pharmacists in the outpatient setting can help
4.2. Nurses
With appropriate training, nurses can contribute to educating patients on the prudent and
appropriate use of antibiotics, as well as non-antibiotic treatment options for minor, self-
embraced in efforts to reduce costs in primary care, with many patients now undergoing first
assessment by nurses in some countries. Despite this, we failed to identify any published studies
primary care.
One recent study analysed patterns of antibiotic prescribing by nurses working in
primary care in Scotland over the 2007-2013 period [86]. On average, antibiotics were present
prescribed was not assessed in detail in this study, but the results showed improving trends in
during the observed period of time (reduction in the proportion of broader-spectrum agents,
more frequent appropriate duration of treatment of adult females with urinary tract infection
5. Conclusions
total antibiotic use. The majority of antibiotics in outpatients are prescribed for respiratory tract
infections. Several studies have shown that antibiotic prescriptions are either unnecessary or
stewardship in primary care, and to keeping them updated throughout their careers. At the
undergraduate level, curricula and teaching should be strengthened, particularly since a large
proportion of graduates of medical, nursing and pharmacy courses will later work in primary
care [3]. However, education alone will be insufficient to deliver the broad improvements that
are now urgently needed. Improving antibiotic prescribing relies on two complementary
strategies: changing healthcare professionals’ behaviour, which is often not easy to achieve, and
modifying the healthcare system. Given the breadth of potential methods and targets for
improvement, it is perhaps not surprising that multifaceted interventions have proved useful in
interventions from one setting in another is greatly strengthened by taking time to tailor them
to the relevant socio-cultural context, which influences prescribers’, patients’ and even
Most antibiotic stewardship efforts have focussed on hospitals so far, even though 90%
of antibiotics are prescribed in primary care. It is time to make antibiotic stewardship in primary
care a priority.
Europe or North America, and included interventions aimed only at GPs. Almost all studies
focussed exclusively on respiratory tract infections. Many studies confirm that it is easier to
reduce rates of antibiotic prescribing (i.e. limiting unnecessary treatments). It is very clear that
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we must find effective ways to reach this second target. Information on durations of treatment
was almost never reported in studies, even though shortening treatments’ duration is probably
a low-hanging fruit. In practice, many interventions (guidelines, CDSS, POC tests, delayed
prescribing) had low usage rates compared with potentially eligible encounters, possibly
because barriers to use were not assessed and addressed beforehand. Data regarding
sustainability and scalability of interventions were limited, as found by Drekonja et al. in their
recent systematic review [18]. Assessment of impact of any intervention on resistance rates was
absent. Finally, publication bias is also likely, since negative findings were rarely reported.
We recommend that all healthcare professionals (e.g. all physicians working in primary
projects. A global approach is needed as we use in hospitals, taking into account the contextual
and cultural specificities as well as the complex interactions between healthcare professionals,
their patients and the healthcare system. Solid methodologies are also needed [87], with data on
practice. The recent study by van der Velden et al. in the Netherlands
provides a good example of a pragmatic multifaceted intervention embedded into many aspects
of a primary care practice: this combined prescriber education, audit/feedback and patient
leaflets, with accreditation of primary care practices [7]. The model used in Sweden may be a
source of inspiration for other countries. It consists of regional organisations that are capable
of: a) driving and innovating behavioural change at the individual/local level, and b) pooling
We must also ‘think outside the box’, and test innovative strategies, including changes
in the organisation of the healthcare system. For example, few studies have used simulated
patients (i.e. individuals trained to act as a real patient in order to simulate a set of symptoms
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or problems, and who could be used to assess care and compliance with relevant standards in a
blinded way) or quality circles (meetings with peers/pharmacists to discuss practices, using
quality improvement strategies) [88]. Most interventions published so far have focussed on the
international political priority, given the worldwide crisis on antimicrobial resistance. Political
restrictive measures are to be implemented. The WHO Global Action Plan adopted at the World
Health Assembly in 2015 requires all countries to develop national action plans, and is likely
to stimulate the development of more regional and national antibiotic stewardship programmes
decision-making and to automate monitoring of key indicators, with regular feedback and
benchmarking. Enhanced access to such data for research will allow more studies to look at
communication specialists, will be more frequently involved in order to design innovative and
engagement will develop, and the general public will be included in these initiatives. We will
also have a better idea of the types of multifaceted interventions that can lead to scalable,
sustainable real-world improvements in antibiotic use, across a far broader range of settings.
Key issues
Around 90% of antibiotics used in human medicine are prescribed in primary care. At
they should be adapted to the context (‘One size does not fit all’ and ‘No magic bullet’
concepts). Behaviour change theories are helpful for designing interventions that target
healthcare professionals.
described here (Table 1): education, guidelines, clinical decision support systems,
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tests, selective susceptibility reporting, quality indicators, audit and feedback and
Interventions targeting the healthcare system have been overlooked so far, even though
their impact can be large and sustained. Some examples are given here, including:
Most published studies come from Europe or North America. We need studies from a
Most interventions have focussed on general practitioners. In the future, all healthcare
possible for other conditions, and how well suited our current interventions are to
achieving this.
tested.
Financial and competing interests disclosure
The authors have no relevant affiliations or financial involvement with any organization or
entity with a financial interest in or financial conflict with the subject matter or materials
discussed in the manuscript. This includes employment, consultancies, honoraria, stock
ownership or options, expert testimony, grants or patents received or pending, or royalties.
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REFERENCES
Reference annotations
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skills training
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Restrictive Low
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prescribing measures