Clinical Microbiology and Infection 23 (2017) 793e798

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Clinical Microbiology and Infection

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Review

What is antimicrobial stewardship?

O.J. Dyar 1, *, B. Huttner 2, J. Schouten 3, C. Pulcini 4, on behalf of ESGAP (ESCMID Study
Group for Antimicrobial stewardshiP)
1)
Global HealthdHealth Systems and Policy, Department of Public Health Sciences, Karolinska Institutet, Stockholm, Sweden
2)
Division of Infectious Diseases and Infection Control Programme, Geneva University Hospitals and Faculty of Medicine, University of Geneva, Geneva,
Switzerland
3)
IQ Healthcare, Radboud University Medical Center, Geert Grote Plein 2, Nijmegen, The Netherlands
4)
Service des maladies infectieuses et tropicales, Centre hospitalier r

egional universitaire (CHRU) de Nancy, and EA 4360 APEMAC, Universit

e de Lorraine,
Nancy, France

a r t i c l e i n f o a b s t r a c t

Article history: Background: The use of the term ‘antimicrobial stewardship’ has grown exponentially in recent years,
Received 26 April 2017 typically referring to programmes and interventions that aim to optimize antimicrobial use. Although
Received in revised form antimicrobial stewardship originated within human healthcare, it is increasingly applied in broader
28 August 2017
contexts including animal health and One Health. As the use of the term ‘antimicrobial stewardship’
Accepted 29 August 2017
Available online 4 September 2017
becomes more common, it is important to consider what antimicrobial stewardship is, as well as what it
is not.
Editor: Professor L. Leibovici Aims: To review the emergence and evolution of the term ‘antimicrobial stewardship’.
Sources: We searched and reviewed existing literature and official documents, which mostly focused on
Keywords: antibiotics. We contacted the authors of the first publications that mentioned antimicrobial stewardship.
Antibiotic stewardship Content: We describe the historical background behind how antimicrobial stewardship came into use in
One Health clinical settings. We discuss challenges emerging from the varied descriptions of antimicrobial stew-
Rational antibiotic use ardship in the literature, including an over-emphasis on individual prescriptions, an under-emphasis on
Responsible antibiotic use
the societal implications of antimicrobial use, and language translation problems.
Veterinary Antimicrobial stewardship
Implications: To help address these challenges, we suggest viewing antimicrobial stewardship as a
strategy, a coherent set of actions which promote using antimicrobials responsibly. We stress the
continuous need for ‘responsible use’ to be defined and translated into context-specific and time-specific
actions. Furthermore, we present examples of actions that can be undertaken within antimicrobial
stewardship across human and animal health. O.J. Dyar, Clin Microbiol Infect 2017;23:793
© 2017 European Society of Clinical Microbiology and Infectious Diseases. Published by Elsevier Ltd. All
rights reserved.

Introduction
The term ‘antimicrobial stewardship’ is encountered in a
growing number and increasingly diverse range of contexts, from
antimicrobial stewardship programmes in hospitals and the com-
munity [1,2], to veterinary antimicrobial stewardship [3,4], One
Health antimicrobial stewardship [5,6] and the WHO global stew-
ardship framework [7]. Although the term has now become
commonly accepted, there are some challenges associated with it.
* Corresponding author. O.J. Dyar, Global HealthdHealth Systems and Policy,
Department of Public Health Sciences, Karolinska Institutet, Tomtebodav€
agen 18A,
Stockholm 171 77 Sweden.
E-mail address: oliver.dyar@ki.se (O.J. Dyar).
Due to the rapidly increasing use of the term without a sole clear
definition, it has evolved differently in different settings, influenced
by local interpretations; this legacy shapes discussions, perceptions
and assumptions surrounding antimicrobial stewardship. This has
produced two inter-related problems: it can be difficult to classify
what is and what is not antimicrobial stewardship, and conse-
quently stewardship practitioners can face difficulties defining and
communicating what their roles are. Importantly, there is potential
for the term to become a meaningless catchword. An additional
challenge of the term is that its meaning is often not self-evident to
lay people and professionals who are not specialists in infectious
diseases. This is partly because ‘stewardship’ is rarely used in other
clinical fields: we do not talk about ‘Anti-hypertensive stewardship’
or ‘Diabetic drug stewardship’ for example. This is logical, because

http://dx.doi.org/10.1016/j.cmi.2017.08.026
1198-743X/© 2017 European Society of Clinical Microbiology and Infectious Diseases. Published by Elsevier Ltd. All rights reserved.
794 O.J. Dyar et al. / Clinical Microbiology and Infection 23 (2017) 793e798

antimicrobials are the only class of drugs with potential clinical
impact on both the treated individual and the community. The term
antimicrobial stewardship is also difficult to translate into many
languages due to the lack of an equivalent for ‘stewardship’, so
many non-native English speakers find it hard to grasp.
In this narrative review, we will discuss the emergence and
evolution of the concept of antimicrobial stewardship, and attempt
to synopsize whatdin our opiniondis and is not antimicrobial
stewardship. At its essence, we suggest that antimicrobial stew-
ardship is about using antimicrobials responsibly, which involves
promoting actions that balance both the individual's need for
appropriate treatment and the longer-term societal need for sus-
tained access to effective therapy. Our main intention for this
review is for it to act as a guide for newcomers to antimicrobial
stewardship, whether their backgrounds be in human or animal
health, clinical practice or policy and governance. For those already
familiar with antimicrobial stewardship, we hope that this review
will be of interest in charting the history of this rapidly expanding
term, and reflecting on the characteristics that unite stewardship
activities in different settings.
The emergence of antimicrobial stewardship
Results for the search term ‘(antimicrobial OR antibiotic) AND
stewardship’ first appear on Pubmed in 1996, reaching over ten hits
per year in 2005, over 50 hits per year in 2008, and over 100 per
year in 2011. The total number of citations identified by this search
term is now over 2500 (Fig. 1), due to its exponential use in the last
5 years.
The first article using the term ‘antimicrobial stewardship’ was
published by John E. McGowan Jr and Dale N. Gerding in the USA
[8]. They wanted to highlight that we should consider antimicro-
bials a precious non-renewable resource, using a term that incor-
porated both the appropriate use of antimicrobials when they are
indicated, as well as avoiding unnecessary use, while moving away
from the exclusive goal of cost containment that was prevalent at
that time (personal communication). According to McGowan and
Gerding, the term was inspired by a Sunday homily about the
gospel of the ‘good steward’ and the use of the term ‘being a good
steward’ or ‘stewardship’ as part of contributing regularly to the
support of the church. ‘Antimicrobial stewardship’ was then
included by these two American colleagues in the 1997 Society for
Healthcare Epidemiology of America (SHEA) and Infectious Dis-
eases Society of America (IDSA) guidelines for the prevention of
antimicrobial resistance in hospitals [9]. The term then crossed the
Atlantic Ocean, taken up by two European colleagues in 1999, Ian
Gould and Jos van der Meer [10], following informal contacts
among these colleagues. In 1998, Ian Gould and Jos van der Meer
founded ESGAP (the European Society of Clinical Microbiology and
Infectious Diseases Study Group for Antimicrobial stewardshiP),
which helped to amplify the use of ‘antimicrobial stewardship’
worldwide.
Antimicrobial stewardship matures
Historically, ‘antimicrobial stewardship’ was mostly used in the
narrow context of programmes within individual hospitals [11].
During the 1990s and 2000s, programmes were developed and
implemented in many countries, often led by pharmacists in the
USA, and in Europe by specialists in infectious diseases or clinical
microbiology, often together with a pharmacist. These programmes
were not always called antimicrobial stewardship programmes, in
part due to the lack of an equivalent for ‘stewardship’ in many
languages. As examples, antimicrobial stewardship is usually
translated into (programme de) bon usage des antibiotiques (¼ pro-
gramme of good antibiotic use) in French, Strategien zum rationalen
Einsatz von Antiinfektiva (¼ strategy of rational use of anti-
infectives) in German, and rationeel antibiotica beleid/gebruik (¼
rational antibiotic policy/use) in Dutch.
Efforts have existed outside hospitals for many years too, but
often without being explicitly referred to as antimicrobial stew-
ardship. For example, Strama, the Swedish strategic programme
against antibiotic resistance, was formed in the 1990s with a strong
emphasis on improving antibiotic use in community settings, and
involving coordination at regional levels [12]. Similarly, efforts to
improve antimicrobial use among livestock were already present in
Denmark and Sweden in the 1990s, for example through restriction
of their use as growth promoters [4]. The term ‘veterinary antimi-
crobial stewardship’ is now increasingly referred to in the context
of animal health, both livestock and companion animals [3,13].

700
Number of publicaƟons per year

600

500

400

300

200

100

0
1996
1997
1998
1999
2000
2001
2002
2003
2004
2005
2006
2007
2008
2009
2010
2011
2012
2013
2014
2015
2016

Year
Fig. 1. Pubmed citations on antimicrobial or antibiotic stewardship over the past 20 years.
 O.J. Dyar et al. / Clinical Microbiology and Infection 23 (2017) 793e798 795

With the growing recognition of the interconnectedness of human
and animal health there are also recent examples of ‘One Health
antimicrobial stewardship’ in Minnesota, USA, and Cornwall, UK,
demonstrating further broadening of the term [5,6].
What does stewardship mean?
Looking at other disciplines on Web of Science, ‘stewardship’ has
mostly been used in the ethics, policy, economics, theology and
environment domains, and it had rarely been used until the 1990s.
According to the Merriam-Webster dictionary [14], stewardship
refers to: ‘1: the office, duties, and obligations of a steward;’ and
‘2: the conducting, supervising, or managing of something; espe-
cially: the careful and responsible management of something
entrusted to one's care’. It also mentions that:
‘When stewardship first appeared in English during the Middle
Ages, it functioned as a job description, denoting the office of a
steward, or manager of a large household. Over the centuries, its
range of reference spread to the oversight of law courts,
employee unions, college dining halls, Masonic lodges, and
many other organizations. In recent years, the long-established
“management” sense of stewardship has evolved a positive
meaning, “careful and responsible management”.’
The most frequently cited description of antimicrobial stew-
ardship in recent years is that put forward by IDSA in 2007, which
described antimicrobial stewardship in terms of its goals (Table 1)
[15]. IDSA updated this in 2012, writing that ‘antimicrobial stew-
ardship refers to coordinated interventions designed to improve
and measure the appropriate use of antimicrobial agents by pro-
moting the selection of the optimal antimicrobial drug regimen
including dosing, duration of therapy and route of administration’
[16]. This conceptualizes antimicrobial stewardship as a set of
interventions targeted towards a specific purpose; however, by
remaining focused on individual prescriptions it overlooks the
stewardship roles of non-prescribers, and it encounters another
problem common with many other descriptions: the terms
‘appropriate’, ‘rational’ or ‘optimal’ do not explicitly consider the
need to balance individual and societal needs, and so play down the
inherent value judgment implied by ‘responsible’ [17]. Table 1
shows that the term antimicrobial stewardship has previously
been illustrated in a variety of ways, including expressions of its
objectives, its approaches, and its broader purposes. The breadth of
descriptions of antimicrobial stewardship has expanded over time,
mirroring its application in an increasing number and diversity of
contexts. As this has happened, the focus has moved away from
technical descriptions (drug, dose, duration, etc.), towards concepts
of responsibility.
Blurred borders: what is not antimicrobial stewardship?
Before attempting to specify what antimicrobial stewardship is,
it is helpful to look at examples of overlapping concepts. The term
‘conservation’ has sometimes been used synonymously with
stewardship, but there are important differences. Conservation of
antimicrobial effectiveness is a broader concept than antimicrobial
stewardship in that it includes strategies not directly related to the
use of antimicrobials, such as vaccines, the use of vaccines, infection
prevention and control, and public health interventions such as
sanitation [18,19]. In contrast, antimicrobial stewardship is specif-
ically about how antimicrobials are used. Furthermore, the concept
of antimicrobial stewardship includes elements that are not
explicitly captured within conservation, such as the aim of

Table 1
Descriptions of antimicrobial stewardship from the literature

Types of description of Examples from the literature

antimicrobial stewardship

Descriptions of activities
Descriptions of goals
As a programme or set of
interventions
As an approach or method
As a means to tackle resistance
As responsible use
Descriptions of good stewardship
Antimicrobial stewardship includes optimal selection, dose and duration of treatment, as well as control of antibiotic use [9]
Antimicrobial stewardship refers to the responsible use of antimicrobials by healthcare professionals, and more specifically, to
selection of the most appropriate antibiotic, duration, dose and route of administration for a given patient with a demonstrated
or suspected infection [36]
The primary goal of antimicrobial stewardship is to optimize clinical outcomes while minimizing unintended consequences of
antimicrobial use, including toxicity, the selection of pathogenic organisms, and the emergence of resistance [15]
Antimicrobial stewardship refers to coordinated interventions designed to improve and measure the appropriate use of
antimicrobial agents by promoting the selection of the optimal antimicrobial drug regimen including dosing, duration of therapy
and route of administration [16,37]
Antimicrobial stewardship is defined as interventions to improve the appropriate use of antimicrobials through promotion of
optimal agent selection, dosing, duration and route of administration [38]
Antimicrobial stewardship refers to a programme or series of interventions to monitor and direct antimicrobial use at a
healthcare institution, so providing a standard, evidence-based approach to judicious antimicrobial use [1]
A programme that supports selection, dosing, routes of administration and duration of antimicrobial therapy [39]
Antimicrobial stewardship refers to the multifaceted approach (including policies, guidelines, surveillance, prevalence reports,
education and audit of practice) that healthcare organizations have adopted to optimize prescribing [40]
Antimicrobial stewardship is a method of overseeing antimicrobial use in healthcare facilities to ensure that every patient
requiring antimicrobial therapy receives optimal therapy [22]
Antimicrobial stewardship is a key component of a multifaceted approach to preventing the emergence of antimicrobial
resistance [41]
A proposed solution to the combined problems of increasing antibiotic resistance, the dwindling number of antimicrobial agents,
and the suboptimal use of antibiotics in clinical practice is the strategy of antimicrobial stewardship [38]
A critical mission of preservation of antimicrobial utility [39]
Antimicrobial stewardship programmes are a set of interventions that aim to ensure the judicious use of antimicrobials by
preventing their unnecessary use, and by providing targeted and limited therapy in situations where they are wanted [42]
[Stewardship] refers to how the judicious use of antibiotics can maximize both their current effects and the chances of their
being available for future generations [18]
Good antimicrobial stewardship is the optimal selection, dose, and duration of an antimicrobial that results in the best clinical
outcome for the treatment or prevention of infection, with minimal toxicity to the patient and minimal impact on subsequent
resistance. Good antimicrobial stewardship is akin to motherhood and apple pie [24]
Good antimicrobial stewardship involves selecting an appropriate drug and optimizing its dose and duration to cure an infection
while minimizing toxicity and conditions for selection of resistant bacterial strains [41]
796 O.J. Dyar et al. / Clinical Microbiology and Infection 23 (2017) 793e798
optimizing therapy for the individual patient today. Another
concept that overlaps with stewardship is ‘good clinical practice’;
this involves many of the elements of optimizing treatment for
individual patients (drug, dose, duration), but emphasizes the so-
cietal responsibility dimension less. ‘Diagnostic stewardship’ is an
expression that has been increasingly used lately [20]. It refers to
‘modifying the process or ordering, performing and reporting
diagnostic tests to improve the treatment of infections’ [20]. We
believe the use of ‘stewardship’ here is less appropriate, as we do
not ‘steward’ diagnostics; we steward antimicrobials, by using di-
agnostics properly. Indeed, improving the diagnostic process
(clinically, microbiologically, or in other ways) is an inherent part of
any antimicrobial stewardship programme, since a good prescrip-
tion starts with a good diagnosis.
What is antimicrobial stewardship?
Antimicrobial stewardship has been conceptualized in many
ways, including as a set of coordinated interventions, as a pro-
gramme, as a philosophy, and as an ethic. The origin of the word
‘stewardship’ is grounded in daily actions that are often multi-
faceted: the steward of a large household carefully and respon-
sibly manages the household. As antimicrobial stewards, we need
to carefully and responsibly manage antimicrobials. We suggest
that it is best to view the collective daily actions within antimi-
crobial stewardship as a strategy. Strategy comes from the Greek
strategos meaning a general, but coherent, set of manoeuvres car-
ried out to overcome an enemy [21]. A key word here is ‘general’,
rather than specific. Specific sets of manoeuvres (i.e. types of
intervention) are within the local jurisdiction of those who trans-
late strategy into operations. Furthermore, if the actions are not
coherent, then they risk being in conflict with one another.
We suggest that antimicrobial stewardship can be defined
as:
A coherent set of actions which promote using antimicro-
bials responsibly.
This definition can be applied from individual level actions to
global level actions, and across human health, animal health and
the environment. Placing less emphasis on individual pre-
scriptions helps to emphasize a broader concept of antimicrobial
management that values the contributions of non-prescribers
[22]. This definition recognizes that both the coherent set of ac-
tions and their objective (using antimicrobials responsibly) are
inherently context-specific and will vary depending on who is
doing them: the evidence base of interventions evolves over time,
what works in one place may not work or be coherent in others,
and what is considered responsible use at one time-point may not
be considered responsible at another. For these reasons, we have
not stated more explicitly what ‘responsible use’ is. Our definition
could be combined with a recent description of responsibility [17]
to produce:
‘Antimicrobial stewardship is a coherent set of actions which
promote using antimicrobials in ways that ensure sustainable
access to effective therapy for all who need them.’
A more comprehensive description of responsible use has been
developed through an expert consensus procedure within the
DRIVE-AB project, producing 22 separate domains [23].
The return of the good antimicrobial steward
In 2001 Gerding wrote that we should be ‘good antimicrobial
stewards’ [24]. In Table 2 we illustrate ways in which different
‘actors’ (individuals, organizations, governments) can do this,
translating the definition of antimicrobial stewardship into action.
We suggest that the middle column can be used for when different
actors want to convey what antimicrobial stewardship means for
them.
Actions within antimicrobial stewardship
In this section, we will provide examples of antimicrobial
stewardship actions. Another review in this series discusses the
available evidence base for interventions in hospital settings [25].
Fig. 2 illustrates examples of actions by different individuals and
organizations, focusing on human healthcare.
Actions that attempt to directly influence the behaviour of pre-
scribers, patients, vets and farmers are often clearly aiming to either
enable responsible antimicrobial use (e.g. decision support tools,
audit and feedback) or to restrict inappropriate or unnecessary
antimicrobial use (e.g. selective reporting of susceptibility testing,
formulary restrictions) [26]. These actions may be specifically
termed ‘stewardship interventions’ in the context of inpatient hos-
pital care, and they are frequently coordinated by a multidisciplinary
team who lead an antimicrobial stewardship programme that se-
lects from a menu of potential interventions that are adaptable and
customizable concepts [27], designed to fit the institutional infra-
structure: how an antimicrobial stewardship team is embedded in
the hospital infrastructure, who is on the team, who is supporting
the team, what clinical data are available to the team, and to what
extent the stewardship team is able to directly influence prescribers.
As stewardship teams are usually directly responsible for imple-
menting antimicrobial stewardship interventions, hospital quality
officers or advisors can support their work with knowledge of
effective implementation methodology (e.g. the Plan-Do-Study-Act
[PDSA] Cycle, Six Sigma, Theory of constraints [TOC]) and involving
implementation specialists.
As the distance between an actor and the prescriber or user of an
antimicrobial grows, the actions tend to become more supportive
or structural in nature, capable of both enabling responsible anti-
microbial use and restricting inappropriate or unnecessary use to
varying degrees. Examples of these actions include institutions
resourcing and prioritizing antimicrobial stewardship teams;
regional networks providing benchmarking and support on
compliance to antimicrobial guidelines; pharmaceutical companies
limiting advertising of antimicrobials but ensuring continuous
availability of needed drugs; regulatory authorities requiring fixed
pack dispensing and restricting the use of certain antimicrobials in
human or animal health; national health authorities delivering
public awareness campaigns and setting licensing requirements for
healthcare professionals; legislation separating prescribing from
dispensing of antimicrobials; governments using Quality Indicators
for antimicrobial prescribing in reimbursement systems and
funding national surveillance systems on antimicrobial use and
resistance patterns [28e35].
Many of these actions require cyclical collection, analysis and
feedback of data to assess their effectiveness. Broadly, useful data
includes antimicrobial consumption data (days of therapy; or
defined daily doses denominated by patient days, admissions,
numbers of inhabitants; or grams of antimicrobials consumed per
kilogram of animal biomass) per class of antimicrobials; resistance
 O.J. Dyar et al. / Clinical Microbiology and Infection 23 (2017) 793e798 797

Table 2
How we can be good antimicrobial stewards

Actor What it means to be good antimicrobial stewards Example actions

Prescriber I use antimicrobials responsibly by  Making accurate diagnoses

Nurse
Patient
Antimicrobial stewardship
team
Hospital governance
Producer/farmer
Pharmaceutical company
National policy maker
I help ensure antimicrobials are used responsibly by
I use antimicrobials responsibly by
We help others in our institution use antimicrobials
responsibly by
Our institution uses antimicrobials responsibly by
I use antimicrobials responsibly by
Our company ensures antimicrobials are used
responsibly by
Our country uses antimicrobials by
 Following local antimicrobial guidelines
 Regularly reviewing the need for therapy
 Taking cultures at appropriate times
 Ensuring patients understand how to take antimicrobials on discharge
 Taking antimicrobial courses as recommended by the prescriber
 Not storing or using leftover antimicrobials
 Developing guidelines for antimicrobial use
 Supporting audit and feedback for prescribers
 Educating prescribers
 Ensuring sufficient sustainable and dedicated funding for antimicrobial
stewardship teams
 Monitoring antimicrobial use and resistance
 Investing in a Clinical Decision Support System
 Enabling formulary restrictions
 Diagnosing selectivity
 Not using antimicrobials as growth promoters
 Limiting advertising of antimicrobials, especially broad spectrum
 Helping ensure there is a continuous supply of antimicrobials
 Prioritizing and funding antimicrobial stewardship activities
 Supporting the use of quality metrics and pay for performance

Fig. 2. Examples of actors and actions within antimicrobial stewardship. AMS, Antimicrobial stewardship.

surveillance data on microorganisms; and most importantly, but actions to use antimicrobials responsibly, and if these actions are
often also hardest to obtain, data on the quality of antimicrobial use. coherent. Going forward, there is a continuous need for ‘respon-
sibly’ to be defined and translated into context-specific and time-
Conclusion specific actions.

Antimicrobial stewardship is central to efforts to ensure access

to effective antimicrobials for all who need them, today and
tomorrow. The term antimicrobial stewardship emerged relatively
recently, and is being applied in an increasingly diverse range of
contexts; many current definitions of antimicrobial stewardship are
technical and focus on prescriptions. We have suggested that it is
now best to view antimicrobial stewardship more broadly, as a
strategy, a coherent set of actions which promote using antimi-
crobials responsibly. The specific actions vary depending on the
actor, but share many commonalities at different levels within a
healthcare system, as well as between human and animal health.
Our suggested definition for antimicrobial stewardship is a tool:
each actor can ask if they or their organizations are undertaking
Transparency declaration
The authors have no conflict of interest to disclose. No external
funding was received for this work.
Acknowledgements
We thank Ian Gould, Jos van der Meer, John E. McGowan Jr and
Dale N. Gerding for describing the introduction of ‘stewardship’

raud
into the context of antimicrobial use. We thank Guillaume Be
and Bojana Beovi
c for their kind contribution in reading and
commenting on the draft of the article.
798 O.J. Dyar et al. / Clinical Microbiology and Infection 23 (2017) 793e798

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