Clinical Microbiology and Infection 25 (2019) 20e25

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Position paper

Developing core elements and checklist items for global hospital

antimicrobial stewardship programmes: a consensus approach
C. Pulcini 1, 2, *, F. Binda 1, 2, 3, A.S. Lamkang 4, A. Trett 4, E. Charani 5, D.A. Goff 6,
S. Harbarth 7, S.L. Hinrichsen 8, G. Levy-Hara 9, M. Mendelson 10, D. Nathwani 11,
R. Gunturu 12, S. Singh 13, A. Srinivasan 14, V. Thamlikitkul 15, K. Thursky 16,
E. Vlieghe 17, 18, 19, H. Wertheim 20, M. Zeng 21, S. Gandra 4, R. Laxminarayan 4, 22
1)
Universit
e de Lorraine, APEMAC, Nancy, France
2)
Universit
e de Lorraine, CHRU-Nancy, Infectious Diseases Department, Nancy, France
3)
University of Milan, Department of Biomedical and Clinical Sciences «Luigi Sacco», Milan, Italy
4)
Center for Disease Dynamics, Economics & Policy (CDDEP), New Delhi, India
5)
Imperial College London, Department of Medicine, NIHR Health Protection Research Unit in Healthcare Associated Infections and Antimicrobial
Resistance, London, UK
6)
The Ohio State University Wexner Medical Center, Columbus, OH, USA
7)
Geneva University Hospitals, Infection Control Program and WHO Collaborating Center, Faculty of Medicine, Geneva, Switzerland
8)
Universidade Federal de Pernambuco (UFPE), Tropical Diseases Department, Recife, Brazil
9)
Hospital Carlos G Durand, Unit of Infectious Diseases, Buenos Aires, Argentina
10)
Groote Schuur Hospital, University of Cape Town, Department of Medicine, Division of Infectious Diseases & HIV Medicine, Cape Town, South Africa
11)
Ninewells Hospital and Medical School, Dundee, UK
12)
The Aga Khan University Hospital, Dept. of Pathology, Division of Clinical Microbiology, Nairobi, Kenya
13)
Amrita Institute of Medical Sciences, Kochi, Kerala, India
14)
Centers for Disease Control and Prevention, Atlanta, GA, USA
15)
Mahidol University, Faculty of Medicine Siriraj Hospital, Bangkok, Thailand
16)
National Centre for Antimicrobial Stewardship, Royal Melbourne Hospital at the Peter Doherty Institute, Melbourne, Australia
17)
University Hospital Antwerp, Department of General Internal Medicine, Infectious Diseases & Tropical Medicine, Antwerp, Belgium
18)
University of Antwerp, Global Health Institute, Antwerp, Belgium
19)
Institute of Tropical Medicine, Department of Clinical Sciences, Antwerp, Belgium
20)
Radboudumc, Department of Medical Microbiology and Radboud Center for Infectious Diseases, Nijmegen, The Netherlands
21)
Children's Hospital of Fudan University, Department of Infectious Diseases, Shanghai, China
22)
Princeton University, Princeton, NJ, USA

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

Article history:
Received 5 February 2018 Objectives: With increasing global interest in hospital antimicrobial stewardship (AMS) programmes,
Received in revised form there is a strong demand for core elements of AMS to be clearly defined on the basis of principles of
18 March 2018 effectiveness and affordability. To date, efforts to identify such core elements have been limited to
Accepted 22 March 2018 Europe, Australia, and North America. The aim of this study was to develop a set of core elements and
Available online 3 April 2018 their related checklist items for AMS programmes that should be present in all hospitals worldwide,
regardless of resource availability.
Editor: L Leibovici
Methods: A literature review was performed by searching Medline and relevant websites to retrieve a list
of core elements and items that could have global relevance. These core elements and items were
Keywords:
evaluated by an international group of AMS experts using a structured modified Delphi consensus
Antimicrobial resistance
Antimicrobial stewardship
procedure, using two-phased online in-depth questionnaires.
Hospital Results: The literature review identified seven core elements and their related 29 checklist items from 48
Low-income country references. Fifteen experts from 13 countries in six continents participated in the consensus procedure.
Middle-income country Ultimately, all seven core elements were retained, as well as 28 of the initial checklist items plus one that
was newly suggested, all with
80% agreement; 20 elements and items were rephrased.

* Corresponding author. C. Pulcini, Centre Hospitalier Re
gional Universitaire de Nancy, Service de Maladies Infectieuses et Tropicales, Ho
^pitaux de Brabois, alle

e du Morvan,
54511 Vandoeuvre-Le s-Nancy, France.
E-mail address: [email protected] (C. Pulcini).

https://doi.org/10.1016/j.cmi.2018.03.033
1198-743X/© 2018 European Society of Clinical Microbiology and Infectious Diseases. Published by Elsevier Ltd. All rights reserved.
 C. Pulcini et al. / Clinical Microbiology and Infection 25 (2019) 20e25 21

Conclusions: This consensus on core elements for hospital AMS programmes is relevant to both high- and
low-to-middle-income countries and could facilitate the development of national AMS stewardship
guidelines and adoption by healthcare settings worldwide. C. Pulcini, Clin Microbiol Infect 2019;25:20
© 2018 European Society of Clinical Microbiology and Infectious Diseases. Published by Elsevier Ltd. All
rights reserved.

Introduction in addition to a website searchdrelevant agencies and organiza-

tions such as the WHO or the European Centre for Disease Pre-
Antimicrobial resistancedparticularly antibiotic resistance in vention and Control (ECDC)dto search for existing core elements
bacteriadis a global threat, making antimicrobial stewardship for hospital AMS programmes. Only reviews, guidance/guidelines
(AMS) programmes necessary in all hospitals worldwide [1e3]. A and consensus documents were included. Additional references
recent review conducted by ESGAP (ESCMID Study Group for were identified by the 15 experts, with no language restriction (all
Antimicrobial Stewardship) found that many definitions exist for authors assisted with translation when required). Data were
the abbreviation AMS [2]. The authors suggested that it is best to extracted by two junior researchers and double-checked by two
view the collective daily actions within AMS as a strategy, and they senior researchers. On the basis of the final list of references [3e50],
proposed the following definition: “Antimicrobial stewardship is a the steering committee compiled summary tables (listing all core
coherent set of actions which promote using antimicrobials in ways elements and checklist items found, with their corresponding ref-
that ensure sustainable access to effective therapy for all who need erences), which were made available to the experts. CP and SG
them” [2]. The absence of a universal definition for AMS combined developed an initial set of core elements and their related checklist
with a lack of international guidance and standards are among the items, to be assessed by the experts, based on the summary tables,
many barriers to the implementation of these programmes glob- selecting the elements and items they thought might be relevant
ally, especially in low- and middle-income countries [2,4]. In North worldwide. A core element was defined as a broad category of ac-
America, Europe, and Australia, collaborative groups have through tions/a strategy within an AMS programme (e.g. education),
a consensual approach identified core elements considered essen- whereas checklist items described specific actions/interventions
tial for successful AMS programmes [10]. These core elements, within a specific core element. Several checklist items were then
often bundled into checklists, offer healthcare providers a prag- listed under each core element.
matic and measurable means of developing, implementing, and
measuring the impact of hospital AMS programmes. Their appli-
Consensus procedure
cability, contextual relevance, and value in other geographies, cul-
tures, and resource settingsdparticularly in low- and middle-
The list of core elements and checklist items based on the
income countriesdhave not been previously explored.
literature review and the website search (as well as the detailed
Our objective was to identify existing core elements for hospital
summary tables) were presented to the group of 15 experts for a
AMS programmes and to assess their broader global relevance. This
modified Delphi consensus procedure [51]; this consisted of two
was done by undertaking a literature review followed by a struc-
surveys (first and second rounds). Invitation to participate in the
tured consensus procedure involving experts.
survey was sent by email. A teleconference was organized by the
steering committee early in November to explain the objectives and
Methods
methods to all experts, and to reply to their questions.
For the first round (November 2017), the list of core elements
Our objective was to identify a set of core elements and their
and checklist items were converted into an internet-based ques-
related checklist items [6], describing the essential and minimum
tionnaire using SurveyMonkey (Palo Alto, CA, USA). Respondents
standards for AMS programmes in hospitals worldwide.
were asked to select all core elements and checklist items they felt
were essential worldwide and should be part of AMS programmes
Group of experts in all hospitals and in all countries, using a ‘yes/no’ option; a
‘comments’ box was provided for each element/item, including
The steering committee (CP, FB, ASL, AT, SG, RL) invited 15 ex- suggestions for rephrasing. Elements and items were (a) selected if
perts (all the other co-authors) to participate in this study. Experts agreement was
80% (i.e.,
12 experts), (b) held for reassessment
from different backgrounds (infectious disease specialists, clinical during the second round if agreement was between 70% and 79%
microbiologists and clinical pharmacists) were selected on the basis (11 experts), and (c) rejected if agreement was <70% (fewer than 11
of their recognized expertise in AMS across various geographic experts). Experts were also asked to suggest new elements and
settings in six continentsdNorth America (2), South America (2), items for further assessment, in addition to rephrasing. Newly
Europe (5), Africa (2), Asia (3), Australia (1)dall having extensive suggested elements and items were considered for inclusion in the
hands-on experience with AMS in low-to middle-income countries, second round if at least three experts made the same suggestion.
and most of them serving as experts for health authorities and During the second round (December 2017) all previously
policy-makers on the topic of AMS. accepted, newly added, and rephrased elements and items were
presented in a second internet-based questionnaire which was sent
Literature review and website search to all the experts who had participated in the first round. Experts
were asked to rate the newly suggested items and the items held for
In August to September 2017, the steering committee (six re- reassessment, as well as to choose the best phrasing when appro-
searchers) performed a narrative literature review of PubMed with priate (the selected phrasing was the one with >50% agreement). A
the following key words: (antibiotic or antimicrobial) and stew- ‘comments’ box for open-ended feedback was available for all el-
ardship and (review or guidelines or standard or core or checklist), ements and items.
22 C. Pulcini et al. / Clinical Microbiology and Infection 25 (2019) 20e25

Fig. 1. The Delphi consensus procedure: flow chart.

Results
Box 2
Literature review and website search Core element 2: Accountability and responsibilities

We identified 48 relevant references (written in Chinese, En-

glish, French or Spanish) [3e50] and came up with an initial set of Checklist item 2.1:
seven core elements and 29 checklist items. Does your hospital have a formal/written antimicrobial stewardship
programme/strategy accountable for ensuring appropriate
antimicrobial use?
Accompanying comment: This should be based on existing national/
Consensus procedure
international guidelines and/or an existing national strategy
Checklist item 2.2:
All 15 experts participated in the two rounds of the survey. Does your hospital have a formal organizational multidisciplinary
During the first round, all seven core elements were selected, as structure responsible for antimicrobial stewardship (e.g., a
well as 27 of the 29 checklist items, while one item was held for committee focused on appropriate antimicrobial use, pharmacy
committee, patient safety committee or other relevant structure)?
reassessment, one was rejected, and two additional items were Accompanying comment: This antimicrobial stewardship committee
newly suggested by three experts. Rephrasing was suggested for 27 can be either stand-alone or embedded into another committee
elements/items, and comments were added for 14 of them. During structure (e.g. pharmacy committee, patient safety committee or
the second round, two out of three items were selected, and the other relevant structure). In all cases, this antimicrobial stewardship
committee is explicitly in charge of setting and coordinating the
final phrasing was decided upon (newly suggested phrasing was
antimicrobial stewardship programme/strategy in its mandate/
chosen in 20 out of 27 cases). The procedure is summarized in Fig. 1, terms of reference
with the final set of seven core elements and 29 checklist items Checklist item 2.3:
presented in Boxes 1e7 (Appendix S1 presents the full details of the Is there a healthcare professional identified as a leader for
procedure). The core elements were as follows: senior hospital antimicrobial stewardship activities at your hospital and
responsible for implementing the programme?
management leadership towards AMS (Box 1, three checklist Checklist item 2.4:
items), accountability and responsibilities (Box 2, seven items), Is there a document clearly defining roles, procedures of collaboration
available expertise on infection management (Box 3, two items), and responsibilities of the antimicrobial stewardship team
education and practical training (Box 4, two items), other actions members?
Accompanying comment: We refer here to the core operational team
of healthcare professionals (led by the clinical leader) who will
implement the antimicrobial stewardship strategy ‘daily on the
Box 1 ground’. This is different from the antimicrobial stewardship
Core element 1: Senior hospital management leadership towards committee, which is a larger formal organizational structure that
antimicrobial stewardship includes antimicrobial stewardship team members and other
relevant professionals and administrators. In resource-limited
settings or small hospitals, although desirable, it is sometimes
difficult to have an antimicrobial stewardship team; in that case, the
Accompanying comment: This section relates to governance of the antimicrobial stewardship clinical leader will implement the
programme by hospital executives, and specifies how senior antimicrobial stewardship programme. The composition of the
hospital management supports the antimicrobial stewardship (usually multidisciplinary) antimicrobial stewardship team is
programme flexible and should be based on existing international
Checklist item 1.1: recommendations and adapted to the local context
Has your hospital management formally identified antimicrobial Checklist item 2.5:
stewardship as a priority objective for the institution and included it Are clinicians, other than those part of the antimicrobial stewardship
in its key performance indicators? team (e.g. from the ICU, Internal Medicine and Surgery) involved in
Checklist item 1.2: the antimicrobial stewardship committee?
Is there dedicated, sustainable and sufficient budgeted financial Checklist item 2.6:
support for antimicrobial stewardship activities (e.g., support for Does the antimicrobial stewardship committee produce regularly
salary, training, or IT (information technology) support)? (indicate minimum time) a dedicated report which includes e.g.
Checklist item 1.3: antimicrobial use data and/or prescription improvement initiatives,
Does your hospital follow any (national or international) staffing with time-committed short term and long term measurable goals/
standards for antimicrobial stewardship activities (e.g. number of targets for optimising antimicrobial use?
full-time equivalent (FTE) per 100 beds for the different members of Checklist item 2.7:
the antimicrobial stewardship team)? Is there a document clearly defining the procedures of collaboration of
Accompanying comment: These staffing standards should ideally be the antimicrobial stewardship team/committee with the infection
set at national level [56] prevention and control team/committee?
 C. Pulcini et al. / Clinical Microbiology and Infection 25 (2019) 20e25 23

Box 3 Box 5
Core element 3: Available expertise on infection management Core element 5: Other actions aiming at responsible antimicro-
bial use

Checklist item 3.1:

Do you have access to laboratory/imaging services and to timely Checklist item 5.1:
results to be able to support the diagnosis of the most common Is a multidisciplinary antimicrobial stewardship team available at your
infections at your hospital? hospital (e.g., greater than one trained staff member supporting
Accompanying comment: A separate checklist on laboratory capacity clinical decisions to ensure appropriate antimicrobial use)?
and presence of quality assurance should be developed at national/ Checklist item 5.2:
international level [49,57]. These services can be onsite or not Does your hospital support the antimicrobial stewardship activities/
Checklist item 3.2: strategy with adequate information technology services?
In your hospital are there, or do you have access to, trained and Accompanying comment: The level of requirement needs to be
experienced healthcare professionals (medical doctor, pharmacist, defined at local/regional/national level. This could include, for
nurse …) in infection management (diagnosis, prevention and example, measurement of antimicrobial use
treatment) and stewardship willing to constitute an antimicrobial Checklist item 5.3:
stewardship team? Does your hospital have an antimicrobial formulary (i.e. a list of
antimicrobials that have been approved for use in a hospital,
specifying whether the drugs are unrestricted, restricted (approval
of an antimicrobial stewardship team member is required) or
permitted for specific conditions)?
Box 4 Accompanying comment: This might be based on national
recommendations, or the WHO Essential Medicines List.
Core element 4: Education and practical training Checklist item 5.4:
Does your hospital have available and up-to-date recommendations
for infection management (diagnosis, prevention and treatment),
based on international/national evidence-based guidelines and
Checklist item 4.1:
local susceptibility (when possible), to assist with antimicrobial
Does your hospital offer a range of educational resources to support
selection (indication, agent, dose, route, duration) for common
staff training on how to optimize antimicrobial prescribing?
clinical conditions?
Accompanying comment: These resources can be developed locally or
Checklist item 5.5:
not, and can use multiple formats
Does your hospital have a written policy that requires prescribers to
Checklist item 4.2:
document an antimicrobial plan (includes indication, name, dosage,
Do the antimicrobial stewardship team members receive regular
duration, route and interval of administration) in the medical record
training in antimicrobial prescribing and stewardship?
or during order entry for all antimicrobial prescriptions?
Accompanying comment: This training is usually not offered at the
Checklist item 5.6:
hospital level, but likely to be at a regional, national or international
Does the antimicrobial stewardship team review/audit courses of
level. The hospital should however ensure that members of the
therapy for specified antimicrobial agents or clinical conditions at
antimicrobial stewardship team are adequately trained, according to
your hospital?
local/regional/national requirements
Checklist item 5.7:
Is advice from antimicrobial stewardship team members easily
available to prescribers?
Checklist item 5.8:
Are there regular infection and antimicrobial prescribing focused ward
aiming at responsible antimicrobial use (Box 5, eight items), rounds in specific departments in your hospital?
monitoring and surveillance (Box 6, four items), and reporting and
feedback (Box 7, three items).

Box 6
Discussion Core element 6: Monitoring and surveillance (on a continuous
basis)
Based on a pragmatic literature review and a structured
consensus procedure, we developed minimum core elements and
checklist items that could be relevant to hospital AMS programmes
Checklist item 6.1:
worldwide. Even though most of these checklist items may not
Does your hospital monitor the quality of antimicrobial use at the unit
currently exist in most hospitals in low-income countries, we and/or hospital wide level?
included all of them on the list because our main objective was to Accompanying comment: This can be done for example by
identify universally relevant, essential elements and items based on undertaking point prevalence surveys or audits, assessing
appropriateness of infection management and antimicrobial
the best available evidence. These seven core elements and their
prescription (e.g. indication, choice and duration of antibiotic
related 29 checklist items could be adapted and adopted locally therapy in pneumonia or surgical prophylaxis according to policy/
depending on factors such as clinical setting and resource avail- guidance)
ability. They provide a baseline of key elements required to start Checklist item 6.2:
hospital AMS programmes, and could be further modified and used Does your stewardship programme monitor compliance with one or
more of the specific interventions put in place by the stewardship
for the purposes of accreditation/certification, benchmarking, or
team (e.g. indication captured in the medical record for all
scrutiny/performance [52,53]. We were deliberately as generic as antimicrobial prescriptions)?
possible in the phrasing of elements and items so that countries Checklist item 6.3:
could adapt them to their own situations: for example, regarding Does your hospital monitor antibiotic susceptibility rates for a range
of key bacteria?
the composition of AMS teams.
Checklist item 6.4:
When comparing our seven core elements and 29 checklist Does your hospital monitor the quantity of antimicrobials prescribed/
items with the list developed by the Centers for Disease Control and dispensed/purchased at the unit and/or hospital wide level?
Prevention (CDC) in the United States, we found that both lists of
core elements are very similar in content, even though the phrasing
24 C. Pulcini et al. / Clinical Microbiology and Infection 25 (2019) 20e25

Box 7 qatar.org) to compensate for his time on this project. However,

Core element 7: Reporting and feedback (on a continuous basis) the funder had no role in the conduct of our research.
The opinions expressed in this article are those of the authors
and do not necessarily reflect the views of the Centers for Disease
Accompanying comment: All these reports should also be shared with Control and Prevention, the NHS, the NIHR, the Department of
the hospital management leadership Health, or Public Health England.
Checklist item 7.1:
Does your stewardship programme share hospital-specific reports on
the quantity of antimicrobials prescribed/dispensed/purchased Appendix A. Supplementary data
with prescribers?
Checklist item 7.2:
Does your stewardship programme share facility-specific reports on Supplementary data related to this article can be found at
antibiotic susceptibility rates with prescribers? https://doi.org/10.1016/j.cmi.2018.03.033.
Checklist item 7.3:
Are results of audits/reviews of the quality/appropriateness of
antimicrobial use communicated directly with prescribers? References

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