WHO Tootlkit

A N T I M I C R O B I A L S T E WA R D S H I P P R O G R A M M E S
I N H E A LT H - C A R E FA C I L I T I E S I N L O W - A N D
MIDDLE-INCOME COUNTRIES
A WHO PRACTICAL TOOLKIT
ANTIMICROBIAL
STEWARDSHIP
ii ANTIMICROBIAL STEWARDSHIP PROGRAMMES IN HEALTH-CARE FACILITIES IN LOW- AND MIDDLE-INCOME COUNTRIES
A N T I M I C R O B I A L S T E WA R D S H I P P R O G R A M M E S
I N H E A LT H - C A R E FA C I L I T I E S I N L O W - A N D
MIDDLE-INCOME COUNTRIES
A WHO PRACTICAL TOOLKIT

Antimicrobial stewardship programmes in health-care facilities in low- and middle-income countries.
A WHO practical toolkit
ISBN 978-92-4-151548-1
© World Health Organization 2019
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CONTENTS
List of figures, tables and boxes. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . v

Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . vii
Foreword . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . viii
List of abbreviations. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ix
Glossary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . x

1. Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . xii
1.1 Background . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
1.2 Antimicrobial stewardship – an integral component of health systems. . . . . . . . . . . 2
1.3 Establishing AMS programmes at a glance. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
2. Structures for national (state/regional) AMS programmes . . . . . . . . . . . . . . . . . . . . . . . . 5

2.1 Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
2.2 Selecting the national core elements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
2.3 How to use the national core elements list . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
3. Structures for health-care facility AMS programmes . . . . . . . . . . . . . . . . . . . . . . . . . . . 11

3.1 Background . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
3.2 Selecting the health-care facility core elements. . . . . . . . . . . . . . . . . . . . . . . . . . 12
3.3 How to use the health-care facility core elements list . . . . . . . . . . . . . . . . . . . . . 12
4. Planning an AMS programme in a health-care facility. . . . . . . . . . . . . . . . . . . . . . . . . . 17

4.1 Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18
4.2 Conducting a situational or SWOT analysis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
4.3 Identifying human resources. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20
4.4 Link between IPC and AMS. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22
4.5 Use of antibiotics in health-care facilities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24
4.5.1 Quantity – AMC data. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24
4.5.2 Quality – antibiotic use data (PPS). . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25
4.5.3 Quality – antibiotic audit data. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26
4.7 The EML and AWaRe classification. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26
4.7 Microbiology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28
5. Performing AMS interventions in a health-care facility. . . . . . . . . . . . . . . . . . . . . . . . . . 30

5.1 Implementing an AMS programme. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31
5.2 AMS interventions, implementation and behaviour change . . . . . . . . . . . . . . . . . 31
5.3 Identifying local targets for improving antibiotic use . . . . . . . . . . . . . . . . . . . . . . 32
5.4 A systematic approach to implementing AMS interventions. . . . . . . . . . . . . . . . . 32
5.5 Basic AMS interventions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34
5.6 Moving beyond basic AMS interventions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35
5.7 More detailed AMS interventions to improve antibiotic prescribing. . . . . . . . . . . . 37
5.8 Audit with feedback . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43
5.8.1 Prospective (real-time) audit with feedback . . . . . . . . . . . . . . . . . . . . . . 43
5.8.2 Retrospective audit with feedback. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43
5.8.3 Selecting one or more infections for audit. . . . . . . . . . . . . . . . . . . . . . . 43
5.8.4 Selecting antibiotic(s) for audit . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 44
5.9 Role of IT in an AMS programme. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 46
ANTIMICROBIAL STEWARDSHIP PROGRAMMES IN HEALTH-CARE FACILITIES IN LOW- AND MIDDLE-INCOME COUNTRIES iii
6. Assessing AMS programmes. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 47
6.1 Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 48
6.2 Structural measures/indicators . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 48
6.3 Process measures/indicators. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 48
6.4 Outcome measures/indicators. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 49
6.5 How to begin assessing AMS programmes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 49
7. Education and training . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 53

7.1 AMS competencies. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 54
7.2 Education and training . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 58
7.4 Effectiveness of different training and education delivery. . . . . . . . . . . . . . . . . . . 61
Annex I: Sample terms of reference – national AMS technical working group. . . . . . . . . 63

Annex II: Sample terms of reference – health-care facility AMS committee. . . . . . . . . . . 64
Annex III: Sample terms of reference – health-care facility AMS team. . . . . . . . . . . . . . . 66
Annex IV: Sample AMS review form . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 67
Annex V: Sample pre-authorization/restricted prescribing form. . . . . . . . . . . . . . . . . . . 68
Annex VI: Sample medical chart. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69
Annex VII: Sample bug-drug chart. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 70
Annex VIII: Sample cumulative antibiogram for gram-negative bacteria. . . . . . . . . . . . . . . 71
iv ANTIMICROBIAL STEWARDSHIP PROGRAMMES IN HEALTH-CARE FACILITIES IN LOW- AND MIDDLE-INCOME COUNTRIES

L I S T O F F I G U R E S , TA B L E S A N D B OX E S
Figure 1. Integrated approach to optimizing use of antimicrobials towards universal

health coverage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
Figure 2. National (state/regional) core elements for AMS programmes in LMICs . . . . . . . . . . 6
Figure 3. Guide to navigating the national core elements checklist to identify,
prioritize and develop a stepwise implementation plan over the short and
medium/long term. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
Figure 4. Health-care facility core elements for AMS programmes in LMICs . . . . . . . . . . . . . 12
Figure 5. Guide to navigating the health-care facility core elements checklist to identify,
prioritize and develop a stepwise implementation plan over the short and
medium/long term. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
Figure 6. Example of a SWOT analysis for AMS readiness in a health-care facility. . . . . . . . . 19
Figure 7. Example of an AMS governance structure for health-care facilities in LMICs. . . . . . 21
Figure 8. Links between IPC and AMS in delivering quality health care and
optimizing antibiotic use. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23
Figure 9. Linkage of AMS and the IPC core components . . . . . . . . . . . . . . . . . . . . . . . . . . . 23
Figure 10. Pharmaceutical value chain indicating potential data sources for
surveillance of antimicrobial consumption and use . . . . . . . . . . . . . . . . . . . . . . . . 24
Figure 11. Overview of the WHO AWaRe groups and essential antibiotics on the
WHO EML. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27
Figure 12. Proportional consumption (%) of antibiotics by AWaRe classification in six
countries of the Western Pacific Region, 2015 . . . . . . . . . . . . . . . . . . . . . . . . . . . 28
Figure 13. Questions to address when applying the quality improvement model for
AMS interventions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33
Figure 14. The quality-improvement model following the continuous improvement cycle:
Plan, Do, Study, Adjust . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33
Figure 15. The quality-improvement model in more detail. . . . . . . . . . . . . . . . . . . . . . . . . . . 34
Figure 16. Appropriate antibiotic surgical prophylaxis – indication, and prescribe and
stop prophylaxis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 36
Figure 17. Structural, process and outcome measures for assessing AMS programmes . . . . . . 48
Figure 18. Education and training delivery modes for AMS-related competencies. . . . . . . . . . 59
Table 1. WHO toolkit for AMS programmes in health-care facilities in LMICs. . . . . . . . . . . . . 3

Table 2. Checklist of essential national* core elements for AMS programmes in
LMICs – basic (white) and advanced (grey) core elements. . . . . . . . . . . . . . . . . . . . . 8
Table 3. Indicators from the Tripartite M&E framework for the Global Action Plan on
AMR relevant to AMS programmes. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
Table 4. Checklist of essential health-care facility core elements for AMS programmes
in LMICs – basic (white) and advanced (grey) core elements. . . . . . . . . . . . . . . . . . 14
Table 5. Preparation for developing and implementing an AMS programme in a
health-care facility . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18
Table 6. Nine common areas for improving antibiotic prescribing . . . . . . . . . . . . . . . . . . . . 32
Table 7. Types of AMS interventions for improving antibiotic prescribing practices. . . . . . . . 37
Table 8. Comprehensive list of AMS interventions for improving antibiotic
prescribing practices. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38
Table 9. Areas where IT can benefit AMS interventions. . . . . . . . . . . . . . . . . . . . . . . . . . . . 46
Table 10. Outcome measures/indicators related to antimicrobial use . . . . . . . . . . . . . . . . . . 50
ANTIMICROBIAL STEWARDSHIP PROGRAMMES IN HEALTH-CARE FACILITIES IN LOW- AND MIDDLE-INCOME COUNTRIES v

Table 11. Outcome measures/ indicators related to patients and microbiology. . . . . . . . . . . . 51
Table 12. Process measures/indicators of antimicrobial use . . . . . . . . . . . . . . . . . . . . . . . . . 52
Table 13. Competencies for HCWs involved in AMS programmes in
health-care facilities in LMICs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 55
Table 14. Teaching methods for AMS interventions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61
Box 1. Key steps in establishing a national AMS programme to enable facility AMS. . . . . . . 3
Box 2. Key steps to establishing a health-care facility AMS programme. . . . . . . . . . . . . . . . 4
Box 3. Case study: How a facility outbreak underpinned the establishment of
facility AMS in Barbados. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
Box 4. Core components of IPC and the link to AMS. . . . . . . . . . . . . . . . . . . . . . . . . . . . 23
Box 5. Step-by-step guide for setting up an AMC surveillance programme at
the facility level. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25
Box 6. Step-by-step guide for setting up a health-care facility PPS . . . . . . . . . . . . . . . . . . 26
Box 7. Snapshot of GLASS. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29
Box 8. Basic AMS interventions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35
Box 9. Core steps for implementing an educational programme. . . . . . . . . . . . . . . . . . . . 60
vi ANTIMICROBIAL STEWARDSHIP PROGRAMMES IN HEALTH-CARE FACILITIES IN LOW- AND MIDDLE-INCOME COUNTRIES

ACKNOWLEDGEMENTS
This document was written by Ingrid Smith and Sarah Paulin (WHO, Antimicrobial Resistance Division) under the
supervision of Peter Beyer (WHO, Antimicrobial Resistance Division) and with guidance from Sue Hill (WHO, Science
Division) and Hanan Balkhy (WHO, Antimicrobial Resistance Division). Administrative support was provided by Sandra
Kotur Corliss (WHO, Antimicrobial Resistance Division).
It would not have been possible to produce this document without the support of an international group of experts and
practitioners who contributed through participation in working groups, meetings, provision of strategic direction and
content, and peer review. These experts include (in alphabetical order):
Paul Bonnar, Dalhousie University, Canada; Kirsty Buising, Doherty Institute, Australia; Enrique Castro-Sanchez,
Imperial College London, UK; Sujith Chandy, Christian Medical College Vellore, India; Sabiha Yusuf Essack, University
of KwaZulu-Natal, South Africa; Sumanth Gandra, Center for Disease Dynamics, Economics & Policy, USA; Debbie Goff,
Ohio State University Wexner Medical Center, USA; Gabriel Levy Hara, Hospital Carlos G. Durand, Argentina; Benedikt
Huttner, Geneva University Hospitals, Switzerland; Andrea Kent, Nova Scotia Health Authority, Canada; Marc Mendelson,
University of Cape Town, South Africa; Mirfin Mpundu, ReAct Africa, Kenya; Dilip Nathwani, University of Dundee, UK;
Benjamin Park, United States Centers for Disease Control and Prevention, DC, USA; Celine Pulcini, University of Lorraine,
France; Dena van den Bergh, Netcare Hospitals Ltd, South Africa; Vera Vlahovic-Palcevski, University Hospital Rijeka,
Croatia
In addition, we would like to thank Corey Ford for providing the case study from Barbados and Jens Thomsen for providing
an example of an antibiogram.
Feasibility studies
We would like to thank Marcus Zervos (Henry Ford Health System) for the overall coordination of the feasibility studies of
this toolkit in Bhutan, Malawi, Federated States of Micronesia and Nepal, supported by Linda Kaljee, Tyler Prentiss and
Gina Maki (Henry Ford Health System). We would also like to thank the following national experts and WHO country office
staff involved in the feasibility studies: Pem Chuki, Sonam Yangchen and Pema Yangzom (Bhutan); Watipaso Kasambara,
Kelias Msyamboza and Jessie Mlotha Namarika (Malawi); Lisa Barrow and Eunyoung Ko (Federated States of Micronesia);
and Deepak C. Bajracharya, Rajan Rayamajhi, Rueban Samuel and Dipendra Raman Singh (Nepal).
Reviewers
We would like to thank all WHO colleagues who reviewed the document for their valuable feedback and comments (in
alphabetical order):
Onyema Ajuebor; Benedetta Allegranzi; Anand Balachandran; Bernadette Cappello; Alessandro Cassini; Jose Luis Castro;
Sergey Eremin; Walter Fuller; Omotayo Hamzat; Verica Ivanovska; Ketevan Kandelaki; Nicola Magrini; Arno Muller; Pilar
Ramon-Pardo; Wenjing Tao; Elizabeth Tayler; Anthony Twyman.
This document was edited by Giselle Weiss.
Financial support
Funding for this report was kindly provided by the Government of Germany. The feasibility studies of this document
were supported by the Government of Germany and GARDP (the Global Antibiotic Resistant Research and Development
Partnership).
ANTIMICROBIAL STEWARDSHIP PROGRAMMES IN HEALTH-CARE FACILITIES IN LOW- AND MIDDLE-INCOME COUNTRIES vii
FOREWORD
On any given day, in a given country, a mother comes The toolkit provides guidance on where to get started,
into a health-care facility when her child has a high fever, including the structures and resources that should be
hoping that the child will get effective treatment and be put in place at the national and health-care facility level,
cured. With increasing rates of antimicrobial resistance through a stepwise approach in low-resource settings.
(AMR), treatment options diminish, and her hopes may As the ultimate goal of an AMS programme is sustainable
be dashed if the bacteria have become resistant and behaviour change in physicians’ antibiotic prescribing
available antibiotics no longer work. practices, the toolkit also provides detailed guidance on
how to plan, perform and assess AMS interventions –
Like access to clean water and air, we have taken including feedback on antibiotic use over time. Finally,
antibiotics for granted for too long. Since the discovery of the toolkit provides an overview of the competencies an
penicillin in 1928, antibiotics have significantly improved AMS team needs to guide health-care professionals in
global health. Indeed, they have been a cornerstone of changing their antibiotic prescribing behaviours.
modern medicine, including cancer chemotherapy and
advanced surgical procedures. And while decades of It is my sincerest hope that this toolkit will be helpful to
overuse and misuse of antibiotics have accelerated the countries in implementing their national action plans on
emergence and spread of resistant bacteria, access to AMR, in particular in optimizing their use of antibiotics.
antibiotics remains a major issue in many parts of the Time is running out, but we still have a window of
world. opportunity to turn the tide on AMR and ensure
continued effective treatment of bacterial infections for
At the same time, not enough new antibiotics are being future generations. Let us act now.
developed to fight resistant bacteria. Therefore, existing
antibiotics must be used more responsibly and managed
carefully to extend their lifespan while being made
available to the patients who truly need them. They should
be prescribed only when indicated, also because they
may cause serious side effects. This practical toolkit for Dr Hanan Balkhy
implementing antimicrobial stewardship (AMS) in health- Assistant Director-General for
care facilities is meant to help low- and middle-income Antimicrobial Resistance
countries achieve this goal. It provides practical guidance World Health Organization
to support the implementation of Objective 4 of the Global
Action Plan on AMR: optimizing the use of antimicrobial
medicines.
viii ANTIMICROBIAL STEWARDSHIP PROGRAMMES IN HEALTH-CARE FACILITIES IN LOW- AND MIDDLE-INCOME COUNTRIES
L I S T O F A B B R E V I AT I O N S
AMC antimicrobial consumption LMIC low- and middle-income country
AMR antimicrobial resistance M&E monitoring and evaluation
AMS antimicrobial stewardship MDR multidrug-resistant
AWaRe ACCESS, WATCH, RESERVE PDR pan drug-resistant
CAP community-acquired pneumonia PPS point prevalence survey
DDD defined daily dose SMART specific, measurable, achievable, relevant, time-
bound
DOTs days of therapy
SSTI skin and soft tissue infection
EML essential medicines list
SWOT strengths, weaknesses, opportunities and
GLASS Global Antimicrobial Resistance Surveillance threats
System
TrACSS Tripartite AMR country self-assessment survey
GNI gross national income
TWG technical working group
HCW health-care worker
UTI urinary tract infection
ICU intensive care unit
WASH water, sanitation and hygiene
IPC infection prevention and control
XDR extensively drug-resistant
IT information technology
ANTIMICROBIAL STEWARDSHIP PROGRAMMES IN HEALTH-CARE FACILITIES IN LOW- AND MIDDLE-INCOME COUNTRIES ix

G L O S S A RY
Antibiotic: An agent or substance that is produced by or derived from a microorganism that kills or inhibits the growth of another
living microorganism. Antibiotic substances that are synthetic, semi-synthetic, or derived from plants or animals are, strictly
speaking, not antibiotics. However, for the purposes of the toolkit they are included. In this document “antibiotic” refers to an
antimicrobial agent with the ability to kill or inhibit bacterial growth.1
Antimicrobial:1 An agent or substance derived from any source (microorganisms, plants, animals, synthetic or semi-synthetic)
that acts against any type of microorganism, such as bacteria (antibacterial), mycobacteria (anti-mycobacterial), fungi (antifungal),
parasite (anti-parasitic) and viruses (antiviral). All antibiotics are antimicrobials, but not all antimicrobials are antibiotics.
Antimicrobial resistance (AMR):2 Microorganisms such as bacteria, fungi, viruses and parasites change when exposed to
antimicrobial drugs such as antibiotics (= antibacterials), antifungals, antivirals, antimalarials and anthelmintics. As a result, the
medicines become ineffective.
Antimicrobial stewardship (AMS):3,4 A coherent set of actions which promote the responsible use of antimicrobials. This
definition can be applied to actions at the individual level as well as the national and global level, and across human health, animal
health and the environment.
Antimicrobial stewardship programme (AMS programme): An organizational or system-wide health-care strategy to promote
appropriate use of antimicrobials through the implementation of evidence-based interventions.
Community-acquired infection: An infection acquired in the community, outside of a health-care setting.
Competencies:5 The development of observable ability of a person (or individual health worker) that integrates knowledge, skills
and attitudes in their performance of tasks. Competencies are durable, trainable and, through the expression of behaviours,
measurable.
Days of therapy (DOTs): The number of days a patient receives an antibiotic independent of dose.
Defined daily dose (DDD): Assumed average maintenance dose per day for a medicine used for its main indication in adults as
established by the WHO Collaborating Centre for Drug Statistics and Methodology.
Empirical antibiotic treatment: Initial antibiotic treatment targeted at the most probable causative microorganism. The
recommendations should be based on local susceptibility data, available scientific evidence or expert opinion, when evidence is
lacking.
Health-care-associated infection (also referred to as “nosocomial” or “hospital infection”):6 An infection occurring in a patient
during care in a hospital or other health-care facility, which was not present or incubating at the time of admission. Health-care-
associated infections can also appear after discharge. They represent the most frequent adverse event associated with patient
care.
Low- and middle-income country (LMIC): A collective term for low income-, lower-middle-income- and higher-middle-income
countries, based on the World Bank’s grouping of countries according to gross national income (GNI) per capita for a specified
year. For 2019, low-income countries are defined as having a GNI per capita of US$ 995 or less in 2017, and lower-middle-
income countries a GNI per capita of US$ 996–US$ 3 895.
x ANTIMICROBIAL STEWARDSHIP PROGRAMMES IN HEALTH-CARE FACILITIES IN LOW- AND MIDDLE-INCOME COUNTRIES

Multidrug-resistant bacteria:7 Bacteria that are resistant to at least one agent in three or more antibiotic categories. Extensively
drug-resistant (XDR) is non-susceptibility to at least one agent in all but two or fewer antibiotic categories (i.e. bacterial isolates
remain susceptible to only one or two categories), and pan drug-resistant (PDR) is non-susceptibility to all agents in all antibiotic
categories.
Outcome measures/indicators for AMS programmes: Outcome measures/indicators are used in AMS activities to capture
quantitative change in e.g. patient or economic outcomes, but most of all in antibiotic use. Antibiotic consumption is expressed
with a numerator indicating the quantity used (i.e. DDDs or DOTs) per defined denominator (i.e. patient-days, admissions,
consultations), to enable comparisons over time in the same setting or with other settings.
Process measures/indicators for AMS programmes: Process measures/indicators aim to capture information about the key
processes that contribute to achieving the desired outcome(s). An example in AMS would be the proportion of patients prescribed
antibiotic treatment in compliance with standard treatment guidelines.
Situational or SWOT analysis: A SWOT (strengths, weaknesses, opportunities and threats) analysis (alternatively called a
situational analysis) is a popular method of identifying internal and/or present strengths and weaknesses, and external and/or
future opportunities and threats to aid a decision-making process.
Structural measures/indicators for AMS programmes: Structure refers to the characteristics (capacity, systems and processes)
of the setting in which AMS programmes are conducted. Structures may be material or human resources, such
as availability of financial resources, number of personnel, availability of guidelines, availability of information technology tools,
etc.
1
Critically important antimicrobials for human medicine. 5th revision. Geneva: World Health Organization; 2017.
2
Antimicrobial resistance. Fact sheet. Geneva: World Health Organization; 2018 (https://www.who.int/en/news-room/fact-sheets/detail/antimicrobial-resistance,
accessed 3 September 2019).
3
Mendelson M, Balasegaram M, Jinks T, Pulcini C, Sharland M. Antibiotic resistance has a language problem. Nature. 2017;545(7652):23-25; McGowan JE,
Gerding DN. Does antibiotic restriction prevent resistance? New Horiz. 1996;4:370–6.
4
Dyar OJ, Huttner B, Schouten J, Pulcini C. What is antimicrobial stewardship? Clin Microbiol Infect. 2017;23(11):793–8.
5
Sioban Fitzpatrick, Health Workforce Department, Geneva WHO (personal communication).
6
Guidelines on core components of infection prevention and control programmes at the national and acute health care facility level. Geneva: World Health
Organization; 2016.
7
Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an
international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18(3):268–81.
ANTIMICROBIAL STEWARDSHIP PROGRAMMES IN HEALTH-CARE FACILITIES IN LOW- AND MIDDLE-INCOME COUNTRIES xi

1. INTRODUCTION
1.1 Background 1.2 Antimicrobial stewardship
– an integral component of health systems
For decades microbes, in particular bacteria, have become
increasingly resistant to various antimicrobials. The World Stewardship is defined as “the careful and responsible
Health Assembly’s endorsement of the Global Action Plan management of something entrusted to one’s care”.13 It
on Antimicrobial Resistance (AMR)8 in May 2015, and the was originally applied in the health-care setting as a tool
Political Declaration of the High-Level Meeting of the Gen- for optimizing antimicrobial use, termed “antimicrobial
eral Assembly on AMR9 in September 2017, both recognize stewardship” (AMS).14 Stewardship has since been applied
AMR as a global threat to public health. These policy initia- in the context of governance of the health sector as a
tives acknowledge overuse and misuse of antimicrobials as a whole, taking responsibility for the health and well-being
main driver for development of resistance, as well as a need of the population and guiding health systems at the na-
to optimize the use of antimicrobials. The Global Action Plan tional and global level.15
on AMR sets out five strategic objectives as a blueprint for
countries in developing national action plans (NAPs) on AMR: Today, AMS is one of three “pillars” of an integrated ap-
proach to health systems strengthening. The other two
Objective 1: Improve awareness and understanding of are infection prevention and control (IPC) and medicine
AMR through effective communication, education and and patient safety. When applied in conjunction with an-
training. timicrobial use surveillance, and the WHO essential med-
icines list (EML) AWaRe16 classification (ACCESS, WATCH,
Objective 2: Strengthen the knowledge and evidence base RESERVE), AMS helps to control AMR by optimizing the
through surveillance and research. use of antimicrobials. Linking all three pillars to other key
components of infection management and health systems
Objective 3: Reduce the incidence of infection through strengthening, such as AMR surveillance and adequate
effective sanitation, hygiene and infection prevention supply of quality assured medicines, promotes equitable
measures. and quality health care towards the goal of achieving uni-
versal health coverage (Figure 1).
Objective 4: Optimize the use of antimicrobial medicines
in human and animal health. AMS principles also apply to the use of antimicrobials in
the animal and agriculture sectors, typically with an em-
Objective 5: Develop the economic case for sustainable phasis on the responsible and prudent use of these agents.
investment that takes account of the needs of all coun- Although increasing levels of viral, fungal and parasite re-
tries, and increase investment in new medicines, diagnos- sistance to antimicrobials are of concern, this document
tic tools, vaccines and other interventions. will focus on the public health challenges of bacterial re-
sistance to antibiotics. The specific aim of the toolkit is to
This toolkit aims to support countries in implementing Ob- enable AMS in health-care facilities in LMICs.
jective 4 of the Global Action Plan – ‘‘optimize the use of
antimicrobial medicines” – by providing practical guidance 8
Resolution WHA 68-7. Global action plan on antimicrobial resistance. In:
Sixty-eighth World Health Assembly, Geneva, 26 May 2015. Annex 3.
on how to implement antimicrobial stewardship (AMS)
Geneva: World Health Organization; 2015.
programmes in the human health sector at the national 9
A/RES/71/3. Political declaration of the high-level meeting of the General
and health-care facility level in low- and middle-income Assembly on antimicrobial resistance. New York: United Nations; 2016.
10

Davey P, Brown E, Charani E, Fenelon L, Gould IM, Ramsay CR et al.
countries (LMICs). Interventions to improve antibiotic prescribing practices for hospital
inpatients. Cochrane Database Syst Rev. 2013 Apr 30;4:CD003543.
Update in Davey P, Marwick CA, Scott CL, Charani E, McNeil K, Brown E
Antimicrobial stewardship programmes optimize the use of et al. Interventions to improve antibiotic prescribing practices for hospital
antimicrobials, improve patient outcomes, reduce AMR and inpatients. Cochrane Database Syst Rev. 2017 Feb 9;2:CD003543.
11

Schuts EC, Hulscher ME, Mouton JW, Verduin CM, Stuart JWTC, Overdiek
health-care-associated infections, and save health-care costs HWPM et al. Current evidence on hospital antimicrobial stewardship
amongst others.10,11 According to the Organisation for Eco- objectives: a systematic review and meta-analysis. Lancet Infect Dis.
2016;16:847–56.
nomic Co-operation and Development (OECD) report Stem- 12

Stemming the superbug tide: just a few dollars more. Paris: OECD; 2018.
ming the superbug tide: just a few dollars more,12 implement- 13

Global framework for development and stewardship to combat antimicrobial
ing AMS programmes together with other policies to reduce resistance: draft roadmap. Geneva: World Health Organization; 2017.
14

McGowan JE, Gerding DN. Does antibiotic restriction prevent resistance?
overuse of antibiotics and promote hospital hygiene could save New Horiz. 1996;4:370–6.
up to 1.6 million lives by 2050 and US$ 4.8 billion per year in 15

Towards better stewardship: concepts and critical issues. Geneva: World
Health Organization; 2002.
the 33 OECD countries. 16

WHO Model List of Essential Medicines, 20th List. Geneva: World Health
Organization; 2017:8–15.
ANTIMICROBIAL STEWARDSHIP PROGRAMMES IN HEALTH-CARE FACILITIES IN LOW- AND MIDDLE-INCOME COUNTRIES 1

With rates of AMR increasing worldwide, and very few • t o improve quality of care and patient outcomes;
new antibiotics being developed, existing antibiotics are • to save on unnecessary health-care costs;
becoming a limited resource. It is therefore essential that • to reduce further emergence, selection and spread of AMR;
antibiotics only be prescribed – and that last-resort antibi- • to prolong the lifespan of existing antibiotics;
otics (AWaRe RESERVE group) be reserved – for patients • to limit the adverse economic impact of AMR; and
who truly need them. Hence, AMS and its defined set of • to build the best-practices capacity of health-care pro-
actions for optimizing antibiotic use are of paramount im- fessionals regarding the rational use of antibiotics.
portance.4,17
Many countries around the world have developed and 17

Dellit TH, Owens RC, McGowan JE Jr, Gerding DN, Weinstein RA, Burke
JP et al. IDSA/SHEA guidelines for developing an institutional program to
are implementing their NAPs on AMR,18 in which AMS enhance antimicrobial stewardship. Clin Infect Dis. 2007;44:159–77.
is a key priority. Although there is a scientific evidence 18

Antimicrobial resistance: a manual for developing national action plans.
Geneva: World Health Organization; 2016.
base for AMS,19 and national, regional and global guid- 19

Baur D, Gladstone BP, Burkert F, Carrara E, Foschi F, Döbele S et al. Effect
ance documents exist,20,21,22,23 there is a growing need for of antibiotic stewardship on the incidence of infection and colonisation with
more specific guidance on how to establish, implement antibiotic-resistant bacteria and Clostridium difficile infection: a systematic
review and meta-analysis. Lancet Infect Dis. 2017;17(9):990–1001.
and evaluate effective AMS programmes at the national 20

Core elements of antibiotic stewardship programs in resource-limited
and health-care-facility level, especially in LMICs.24,25,26 settings. Atlanta, GA: US Centers for Disease Control and Prevention; 2018
21

Recommendations for implementing antimicrobial stewardship programs in
To meet this need, WHO, in collaboration with global Latin America and the Caribbean: manual for public health decision-makers.
AMS experts, has developed this practical toolkit for im- Washington, DC: PAHO, FIU; 2018.
22

A practical guide to antimicrobial stewardship programs in Ethiopian
plementing AMS programmes in health-care facilities in Hospitals. Addis Ababa: AFMHACA; 2018.
LMICs (summarized in Table 1). This is only the first step in 23

Antimicrobial stewardship program in hospitals. Manual of procedures.
Manila: Department of Health; 2016.
a dynamic process of sharing the evidence and experience 24
Cox JA, Vlieghe E, Mendelson M, Wertheim H, Ndegwa L, Villegas MV et al.
required to run these programmes effectively. Antibiotic stewardship in low- and middle-income countries: the same but
different? Clin Microbiol Infect. 2017; 23:812–8.
25

Van Dijck C, Vlieghe E, Cox A. Antibiotic stewardship interventions in low-
The aim of an AMS programme is: and middle-income countries: a systematic review. Bull World Health Organ.
• to optimize the use of antibiotics; 2018;96:266–80.
26

Wilkins A, Ebata A, MacGregor H. Interventions to reduce antibiotic
• to promote behaviour change in antibiotic prescribing prescribing in LMICs: a scoping review of evidence from human and animal
and dispensing practices; health systems. Antibiotics. 2019;8(1):1–25.
FIGURE 1
Integrated approach
to optimizing use Supply chain
Regulations management
of antimicrobials
towards universal
health coverage
IPC Opti mi ze use

Clean water, $ UHC Access to
sanitation antibiotics
and hygiene
Immunization Antibiotics use
Serveillance of antimicrobial
resistance and antibiotics
2 ANTIMICROBIAL STEWARDSHIP PROGRAMMES IN HEALTH-CARE FACILITIES IN LOW- AND MIDDLE-INCOME COUNTRIES

TA B L E 1
WHO toolkit for AMS programmes in health-care facilities in LMICs
The core elements (Chapters 2 and 3) that should be in place to support AMS programmes at
1. Structures the national (state/regional) and facility level, i.e. AMS team, clinical treatment guidelines, and
surveillance of resistance and antibiotics
Guidance on how to plan, perform and assess AMS interventions in a health-care facility settings
2. Interventions
(Chapters 4–6)
Outline of competencies for health-care professionals performing AMS activities (Chapter 7)

3. Education and training Available online: Resources to support educational workshops and training programmes on AMS
with educational material and a compilation of e-learning AMS resources relevant to LMICs
1.3 Establishing AMS programmes

at a glance
To support readers and implementers at the national AMS programmes can be driven through various pro-
and health-care facility level to navigate the toolkit when cesses and people. The key is to build on existing struc-
implementing AMS programmes, Boxes 1 and 2 provide tures and to utilize entry points and champions. Box 3
brief step-by-step guides on setting up, implementing describes how a health-care facility in Barbados set up its
and monitoring national and health-care facility AMS AMS programme based on an outbreak of a drug-resist-
programmes, respectively. ant bacterium.
B OX 1
Key steps in establishing a national AMS programme to enable facility AMS
Audience: Ministry and/or department/s responsible for delivering quality-assured medical care and access to and
rational use of medicines
1. Establish a governance structure – e.g. a national AMS technical working group (TWG) (Annex I) linked to the national
AMR steering committee.
2. Review and prioritize the national core elements (Chapter 2):
2.1. Identify what is already in place and the level of implementation required.
2.2. Identify the short- and medium/long-term priority core elements.
2.3. Identify the resources required.
3. Identify pilot health-care facilities (public and private) for initial AMS rollout:
3.1. Tertiary teaching facilities;
3.2. Regional/state and/or district facilities; and
3.3. Primary care and/or community (as part of community AMS programmes not covered in this toolkit).
4. Develop a national AMS strategy* with national indicators.
5. Dedicate financial and human resources as required.
6. Monitor and evaluate implementation of the national AMS strategy (Chapter 6).
7. Facilitate access to and/or support pre- and in-service training on optimized antibiotic prescribing (Chapter 7).
* Include community and/or primary care AMS programmes (not covered in this toolkit).

B OX 2
Key steps to establishing a health-care facility AMS programme

Audience: Health-care facility leadership, AMS committee and/or AMS team
1. Undertake a facility AMS situational/SWOT analysis (Chapter 4) of:
1.1. Health-care facility core elements – identify what is in place and the implementation level required (Chapter 3);
1.2. Available data on antimicrobial consumption (AMC) and/or use, prescription audits and AMR surveillance data
(Chapter 4); and
1.3. Existing AMS competencies at the facility (Chapter 7).
2. Establish a sustainable AMS governance structure based on existing structures (Chapter 4; Annexes II and III).
3. Prioritize the health-care facility core elements based on the situational analysis (Chapter 3):
3.1. Identify the immediate priorities.
3.2. Identify the resources required.
4. Identify AMS interventions starting with the low-hanging fruit (Chapter 5):
4.1. Identify who, what, where and when.
5. Develop a health-care facility AMS action plan that specifies the human and financial resources required (Chapter 4).
6. Implement AMS interventions (Chapter 5).
7. Monitor and evaluate AMS interventions (Chapter 6).
8. Offer basic and continued educational resources and training on optimized antibiotic prescribing (Chapter 7).
B OX 3
Case study:
How a facility outbreak underpinned the establishment of facility AMS in Barbados
In a 600-bed health-care facility in Barbados, an outbreak of carbapenemase-resistant Klebsiella pneumoniae (KPC)

resulted in the establishment of an AMS programme linked to the existing IPC programme. In 2012 an all-facility PPS (point
prevalence survey) was undertaken which showed that one in five patients was colonized with KPC, and one in seven of the
KPC-affected patients had an active infection. The results also showed a statistically significant correlation between KPC
colonization and average length of hospital stay and antibiotic use of piperacillin/tazobactam and fluoroquinolones, resulting
in increased hospital costs.
At the time of the outbreak, the facility’s IPC programme consisted of a single nurse, but was then expanded with an
infectious disease ID physician and a pharmacist. The IPC team used data to demonstrate to the hospital management
that an AMS programme was critically needed and that it would involve minimal cost. Leadership commitment led to
establishing an AMS team consisting of an infectious disease physician, pharmacist and microbiologist, as well as IPC-trained
personnel who were all already employed in the facility.
The AMS team determined that the KPC outbreak and the three antibiotics associated with it accounted for 64% of
the hospital costs of antibiotics during the preceding 6 months. The AMS set a target for decreasing the overall cost of
antibiotics and hospital length of stay over the next 6–12 months. The AMS intervention began in the surgical intensive care
unit (ICU) because of eager support from the head anaesthesiologist, an AMS champion. The targets were achieved faster
than anticipated, and interest grew from other wards to be included in the AMS programme. A 60% decline in the use of
carbapenems and vancomycin was documented.
Additional core elements that led to the success of AMS in the facility included facility-wide training on AMS; development
of a facility antibiogram with regular feedback to the prescribers; a strong relationship and trust built between health-care
professionals and the laboratory, which allowed for timely delivery of laboratory reports to inform prescribing; and media
engagement.

2 . S T RU C T U R E S F O R NAT I O NA L
( S TAT E / R E G I O NA L ) A M S P R O G R A M M E S

Key audience: Ministry and/or department/s responsible for delivering quality-assured
medical care and access to rational use of medicines
2.1 Introduction
Experience shows that AMS programmes can be success- EMLs and treatment guideline reviews. Ultimately, it is up
fully implemented when certain structures are in place.27 A to each country to decide how best to set priorities at the
list of essential national core elements (Figure 2) has been local, regional and/or national level. The core elements
developed to help countries build the necessary structures have been stratified as basic, which require fewer resourc-
at the national (state/regional) level to enable health-care es, and advanced, which require more resources, but these
facility AMS programmes, taking into account the local elements may vary for each country.
context.
“Overall, the first priority will be on antimicrobial
Putting key stewardship elements in place is essential to
stewardship, because when there is antimicro-
enabling sustainable action in this area.28 The checklist of
bial stewardship instituted in the hospitals and
national (state/regional) core elements aims to guide coun-
the Ministry as a whole, then everything – the
tries in identifying the most critical elements for their na-
monitoring, the surveillance – everything comes
tional context, supporting the implementation of the NAP
on AMR and subsequently AMS (Table 2). However, the after that.”
list is a guide, and it is important for countries, states and (Bhutan, Government Official)
regions to build on structures that are already in place and
to use them as entry points for AMS initiatives, e.g. basic
health-care package review and implementation, national 2.2 Selecting the national core elements
In developing the essential national core elements, a group

of international experts conducted a literature review to
FIGURE 2 identify key publications.19,20,29,30,31,32,33 A structured con-
sensus procedure (>80%) was then used to identify core
NATIONAL CORE
in LMICs ELEMENTS
National (state/regional) core elements
for AMS programmes
elements relevant to national AMS programmes to enable
health-care facility AMS, and these elements were strati-
fied based on the resources required (basic and advanced).
National plan Regulation

& strategies & guidelines 27

Core elements of hospital antibiotic stewardship programs. Atlanta, GA: US
Department of Health and Human Services, CDC; 2014.
28

Pulcini C, Binda F, Lamkang AS, Trett A, Charani E, Goff DA et al. Developing
core elements and checklist items for global hospital antimicrobial
stewardship programmes: a consensus approach. Clin Microbiol Infect.
2018;25:20–25.
29

Draft WPRO – AMS training package. Geneva: World Health Organization;
2019.
30

Step-by-step approach for development and implementation of hospital
antibiotic policy and standard treatment guidelines. New Delhi: World Health
Organization; 2011.
31

Drug and therapeutics committees – a practical guide. Geneva: World Health
Organization; 2003.
32

Promoting rational use of medicines: core components. Geneva: World
Health Organization; 2002.
Awareness, Supporting 33

WHO guidelines on core components of infection prevention and control
education & training technologies & data programmes at the national and acute health care facility level. Geneva:
World Health Organization; 2016.

2.3 How to use the national core
elements list
Decision makers responsible for national AMS programmes A recommended place to start for establishing a nation-
are encouraged to go through the checklist, identify what al (state/regional) AMS programme is to ensure leader-
is already in place and the level of implementation (Figure ship commitment to AMS by providing dedicated funding
3), which core elements require accelerated implementa- and human resources for NAP and AMS activities, and by
tion (partially implemented) and what is missing. A step- putting in place a national TWG on AMS, education and
wise short- and medium/long-term implementation plan training, surveillance of antibiotic use as part of a national
should be developed for the core elements that are prior- monitoring system and standard treatment guidelines.
itized as important based on the country context.
FIGURE 3
Guide to navigating the national core elements checklist to identify, prioritize and develop a stepwise
implementation plan over the short and medium/long term
I s i t f u l l y i m p l e m e n te d ?
YES
Is the national
I s i t p a r t i a l l y i m p l e m e n te d ?
core element
in place in
your country*? I s t h i s a p r i o r i t y f o r t h e s h o r t te r m ?
NO
I s t h i s a p r i o r i t y f o r t h e m e d i u m o r l o n g te r m ?
* “Country” can be substituted by “state” or “region” depending on the context.

TA B L E 2
Checklist of essential national* core elements for AMS programmes in LMICs – basic (light grey) and
advanced (dark grey) core elements
NATIONAL CORE ELEMENTS Yes No

1. National action plan on AMR that states AMS is a priority
The government endorses a national action plan on AMR explicitly stating that AMS is a national priority.  
2. Dedicated funding for the national action plan on AMR
1. NATIONAL PLAN AND STRATEGIES
The national action plan on AMR has been costed and includes national activities for implementing AMS  
activities in the short to medium term (1–3 years) and/or long term (5 years).
3. Technical working group on AMS established with clear terms of reference

The national multisectoral coordination group has established a TWG or subcommittee on AMS that includes
at least one ministry of health focal point and is linked to the AMC and AMR surveillance and IPC technical  
working groups. For sample terms of reference, see Annex I.
4. National AMS implementation plan or policy endorsement

An achievable national implementation plan for AMS with defined goals, outcomes, timelines, structures
(national and hospital core elements) and responsibilities has been developed. It is linked to the national IPC  
plan or policy if it exists and is integrated into the government’s annual action plan as appropriate.
5. Monitoring and evaluation mechanism in place for the national action plan on AMR
A mechanism is in place to monitor and evaluate progress on implementing the national action plan on AMR  
with the explicit inclusion of AMS and IPC activities.
6. Integration of the AWaRe classification of antibiotics in the national EML and formulary
Develop or review and adapt the antibiotics contained in the national EML and the national formulary  
with reference to the WHO EML AWaRe groups of antibiotics and outline AMS strategies for each group.
7. Up-to-date clinical guidelines that include AMS principles and integrate the AWaRe classification
of antibiotics
The government endorses and makes available up-to-date standard treatment guidelines for infection
management, based on national susceptibility surveillance data (where possible) to assist with antibiotic
selection for common clinical conditions. These guidelines should be based on and explicitly include
stewardship principles. Incorporate the WHO EML AWaRe classification of antibiotics into the next update  
of the guidelines. Where guidelines exist, a first step is to review them and to identify missing guidelines with
2. REGULATION AND GUIDELINES
an initial focus on empirical treatment. Where guidelines do not exist, the government provides human and
financial resources to support the development of such national standard treatment guidelines and their
dissemination as a priority activity. Coherence between guidelines and EMLs should be ensured.
8. Regulations on fixed-dose combinations of antibiotics

The government puts in place regulations that ban fixed-dose antibiotic combinations not approved by national  
or international guidelines.
9a. Regulations on prescription-only sale of antibioticsi

The government puts in place legislation or regulations that require antibiotics to be dispensed only on  
prescription by a qualified health-care professional (where access to health care is not an issue).
9b. Regulation and enforcement of prescription-only dispensing of antibioticsi

Legislation or regulation is actively implemented and enforced that requires antibiotics to be dispensed only on  
prescription by a qualified health-care professional (where access to health care is not an issue).
10. Measures in place to ensure continued availability of quality-assured antibioticsi

The government acts to ensure that available antibiotics are of suitable quality and that substandard or  
falsified drugs are not being sold.
11. Measures in place to ensure affordability of essential antibioticsi

The government acts to ensure that antibiotics are made available in suitable dosages (including paediatric  
formulations when appropriate) at a reasonable price to the public.

NATIONAL CORE ELEMENTS Yes No
12. Regular public antibiotic awareness campaigns
Antibiotic awareness campaigns such as World Antibiotic Awareness Week and other targeted campaigns are  
regularly organized to address specific national or local issues and communities.
13. Education in schools on basic infection principles

 
3. AWARENESS, TRAINING AND EDUCATION
The government ensures that schools provide education on basic IPC principles, including hand hygiene.
14. Training on AMS competencies for AMS team members

The government and/or health-care facilities facilitate access to in-service training in antimicrobial prescribing
and stewardship for AMS team members in facilities. Use existing core competencies and set standards or  
adapt curricula.
15. Education and training for all health-care professionals on AMS

The government and/or other relevant bodies (e.g. professional societies) facilitate access to and/or support
pre- and in-service training on how to optimize antibiotic prescribing, dispensing and administration for all
relevant health-care professional groups (e.g. doctors, pharmacists, nurses). Use existing core competencies  
and set standards or adapt curricula (e.g. adaptation of the WHO core competencies and the AMR education
and training curriculum guide).
16. Incentives to support implementation of AMS programmes in all health-care facilities, including
staffing standards, training and accreditation
The government sets staffing standards for the AMS programme, makes implementation of AMS programmes
in all facilities (public and private) a requirement, ensures that the health-care facility core elements (detailed  
in Chapter 3) are in place (e.g. by requiring certification/accreditation) and sets criteria to secure specific
government funding for AMS in all facilities.
17. National surveillance system on AMC in placei,ii

The government supports programmes to compile and analyse appropriate data on the quantity and types
of antibiotics purchased or distributed in the country (distinguishing between the health-care facility and  
4. SUPPORTING TECHNOLOGIES AND DATA
community sector, if possible), following the WHO methodology on surveillance of AMC.
18. National surveillance system on AMR in place with laboratory capacity to guide optimal use of
antibiotics in clinical practice and update clinical guidelines
Laboratory capacity is in place at the health-care facility or off-site (reference laboratory) to identify
pathogens and their antibiotic susceptibility, to guide optimal use of antibiotics in clinical practice and to
update guidelines. The laboratory further supports identification of key pathogens or syndromes to target  
AMS interventions. The government supports programmes to collate, compile and compare data from
different facilities to identify trends over time and possibly to identify facilities that are outliers and might
warrant investigation and assistance.
19. Diagnostic tests available and capacity building undertaken to optimize antibiotic use
Governments are encouraged to procure and promote the use of relevant diagnostic tests to optimize
antibiotic use. The government acts to ensure that relevant and essential investigations (e.g. biology,  
microbiology, imaging) are available for all health-care facilities (either on-site, or with available access
off-site).
* “National” can be substituted by “state” or “region” depending on the context.

i
Indicator in the Tripartite M&E framework for the Global Action Plan on AMR.
ii
Indicator tracked on an annual basis through the TrACSS.

The Tripartite M&E framework for the Global Action Plan
World Health Organization, Food and Agriculture Organization of the
34
United Nations, World Organisation for Animal Health [the Tripartite].

on AMR34 includes outcome indicators for optimizing use Monitoring and evaluation of the Global Action Plan on Antimicrobial
of antimicrobials (Table 3) that may be useful in monitor- Resistance: framework and recommended indicators. Geneva: World Health
Organization; 2019.
ing national AMS programmes. These indicators are also 35

Global database for antimicrobial resistance: country self
expected to aid reporting to the annual Tripartite AMR assessment. Geneva: World Health Organization; 2018 (https://www.
amrcountryprogress.org/, accessed 3 September 2019).
country self-assessment survey35 (TrACSS), in particular
regarding a “national monitoring system for consumption
and rational use of antimicrobials in human health”.
TA B L E 3
Indicators from the Tripartite M&E framework for the Global Action Plan on AMR relevant to AMS
programmes32
SOURCE OF DATA AT THE GLOBAL

MEASUREMENT INDICATOR NAME
LEVEL
4.1 Use of a. Total human consumption of antibiotics for systemic use GLASS (Global Antimicrobial Resistance
antimicrobials in (Anatomical Therapeutic Chemical classification code J01) in Surveillance System)
humans DDDs per 1000 population (or Cross-sectional PPS
inhabitants) per day (b–d. see ref. 34.)
4.2 Access to Percentage of health facilities that have a core set of relevant Sustainable Development Goal indicator
antibiotics antibiotics available and affordable on a sustainable basis 3.b.3, with ACCESS antibiotics
disaggregated
4.3 Appropriate use Percentage of inpatient surgical procedures with appropriate PPSs
of antimicrobials timing and duration of surgical antibiotic prophylaxis
4.7 Optimize Legislation or regulation that requires antimicrobials for TrACSS

antimicrobial use human use to be dispensed only with a prescription from an
and regulation authorized health worker

3 . S T RU C T U R E S F O R H E A LT H - C A R E FA C I L I T Y
AMS PROGRAMMES

Key audience: Health-care facility leadership, AMS committee and/or AMS team
3.1 Background undertaken to develop the final list of core elements for
health-care facilities. The list was then stratified based on
At the health-care facility level, different contexts and the resources required (basic or advanced).
types of facilities will face different challenges. A list of
health-care facility core elements has been developed
(Figure 4) to guide facility management in building the
structures needed to enable implementation of sustaina- 3.3 How to use the health-care facility core
ble AMS programmes in their facility. elements list
The essential health-care facility core elements in the

checklist shown in Table 4 have been stratified into ba-
3.2 Selecting the health-care facility core sic core elements requiring fewer resources and more ad-
elements vanced core elements requiring more resources. However,
this differentiation may vary from country to country and
In developing the health-care facility core elements for facility to facility based on size, needs, priorities, resources
AMS programmes in LMICs, an international group of and context. Even within a small facility, the health-care fa-
experts reviewed the key literature,18,19,20,21,21,22,23,24,25 in cility administrator/manager, AMS committee and/or AMS
particular the approach of Pulcini et al.,28 suggesting ad- team/person are encouraged to go through the checklist,
ditions and deletions and taking into account the low- and identify which core elements are already in place and the
middle-income setting. Following the first round of sug- level of implementation, what requires accelerated imple-
gestions, a structured consensus procedure (>80%) was mentation and what is missing (Figure 5).
HEALTH-CARE FACILITY
FIGURE 4
CORE
Health-care facilityELEMENTS
core elements for AMS programmes in LMICs
Leadership Accountability
AMS actions
commitment & responsibilities
Education & Monitoring Reporting

training & surveillance & feedback

FIGURE 5
Guide to navigating the health-care facility core elements checklist to identify, prioritize and develop a
stepwise implementation plan over the short and medium/long term
I s i t f u l l y i m p l e m e n te d ?
YES
Is the core
I s i t p a r t i a l l y i m p l e m e n te d ?
element
in place
in your I s t h i s a p r i o r i t y f o r t h e s h o r t te r m ?
facility? NO
I s t h i s a p r i o r i t y f o r t h e m e d i u m o r l o n g te r m ?
This information will help in developing a stepwise imple-

mentation plan over the short and medium/long term for
the prioritized missing core elements and accelerate im-
plementation of existing ones. For a small facility, it may
be necessary to collaborate with other health-care facili-
ties to put certain core elements in place, e.g. AMS exper-
tise, education and training, standard treatment guidelines
and AMC surveillance.

TA B L E 4
Checklist of essential health-care facility core elements for AMS programmes in LMICs – basic (light
grey) and advanced (dark grey) core elements
HEALTH-CARE FACILITY CORE ELEMENTS Yes No

1. AMS identified as a priority for health-care facility management
The facility management has formally identified AMS as a priority objective for the facility and included it in  
1. LEADERSHIP COMMITMENT
its key performance indicators. Financial and human resources have been allocated for AMS activities.
2. Health-care facility AMS action plan endorsed that prioritizes activities and measures progress and
accountability
A health-care facility AMS action plan is endorsed that prioritizes activities and measures progress and  
accountability for ensuring appropriate antibiotic use, based on existing national or international guidelines
and/or an existing national strategy. The AMS action plan is updated regularly as required.
3. Dedicated financial support for the health-care facility AMS action plan
There is dedicated, sustainable and budgeted financial support for AMS activities in the action plan (e.g.  
support for salary, training and information technology (IT) support).
4. Multidisciplinary AMS leadership committee in place with clear terms of reference*

This AMS committee can be either stand-alone or embedded in another existing committee structure
(e.g. drug and therapeutics committee, pharmacy committee, infection control committee, patient safety
committee). If embedded in another committee, AMS must be a standing item on the committee’s agenda.  
The AMS committee is explicitly in charge of setting and coordinating the AMS programme/strategy
according to its terms of reference.
5. Dedicated AMS leader/champion identified for the health-care facility

A health-care professional has been identified as a leader/champion for AMS activities at the facility and is  
responsible for leading the AMS team in implementing the AMS programme.
6. Multidisciplinary AMS team with terms of reference*

An AMS team of multidisciplinary health-care professionals who will implement the day-to-day AMS
2. ACCOUNTABILITY AND RESPONSIBILITIES
activities in the health-care facility. In resource-limited settings or small facilities it is often difficult to have
an AMS team, and an AMS champion can be identified instead. The composition of the AMS team is flexible
and should be based on existing recommendations and adapted to the local context:  
• o ption 1: >2 health-care professionals constituting a multidisciplinary team (e.g. tertiary hospitals);
• o ption 2: a prescriber and a nurse or pharmacist (e.g. secondary or small hospitals); or
• o ption 3: an AMS champion, e.g. a physician, nurse or pharmacist leading the stewardship programme,
with access to expert advice.
7. Other health professionals identified and involved in AMS activities

Other health-care professionals apart from the AMS team (e.g. from the ICU, internal medicine and surgery,
health informatics, or pharmacy or nursing personnel) participate in AMS activities based on the priorities  
of the health-care facility AMS action plan.
8. Clearly defined collaboration between the AMS and IPC programmes

A document clearly specifies the process of collaboration between the AMS team/committee and the IPC
programme and/or committee. In many low-resource settings the IPC and AMS committees may be merged  
into one.
9a. Regular (descriptive) activity reports on the implementation of the AMS programme
Regular activity reports are produced and disseminated to health-care facility personnel and regional/
national AMS TWGs. These reports include data on antibiotic use/consumption and describe the  
interventions implemented by the AMS team.
9b. Regular activity reports (status and outcomes) on the implementation of the AMS programme
Regular activity reports are produced and disseminated to health-care facility personnel and regional/
national AMS TWGs with timelines for measurable short- and long-term targets/goals, based on analysis of  
local antibiotic use and evaluation of the impact of stewardship interventions.

10. Up-to-date standard treatment guidelines
The health-care facility has available, up-to-date recommendations for infection management based on
international/national evidence-based guidelines and local/national susceptibility patterns (where possible),
to assist with antibiotic selection for common clinical conditions (indication, agent, dose, route, interval,  
duration). A process is in place for regular review and updating of the guidelines based on new evidence or
other external input.
11. Regular AMS team review/audit of specified antibiotic therapy or clinical conditions at the health-
care facility  
Depending on available resources, this can be conducted by prioritizing wards or specific patient conditions.
12. Advice/feedback from AMS team members is easily accessible/available to all prescribers
This can be achieved through various methods, including facility ward rounds, bedside consultations and  
dedicated telephone lines.
13. The AMS team conducts regular ward rounds and other AMS interventions in select health-care
facility departments
The AMS team conducts regular ward rounds (in one or more wards) and other AMS interventions in select  
facility departments (one or more) identified in the health-care facility AMS action plan.
14a. Health-care facility formulary with a list of approved antibiotics

3. AMS ACTIONS
The health-care facility has a formulary with a list of approved antibiotics that may be based on national  
recommendations or the WHO EML.
14b. Health-care facility formulary with a list of restricted antibiotics

The health-care facility has a formulary with a list of antibiotics approved for use in the facility and specifies
a list of restricted antibiotics that require approval by the designated AMS team member (or infectious  
disease physician if available, physician or AMS champion) when used and/or are only permitted for specific
conditions, e.g. the WATCH and RESERVE groups of antibiotics.
15. Laboratory and imaging services accessible to support AMS interventions

The health-care facility has access to (on-site or off-site) laboratory and imaging services, and to timely,  
quality-assured results to support diagnosis of the most common infections.
16. Health-care facility access to IT services to support AMS activities

The specific requirements need to be defined at local/regional/national level. This could include, for  
example, measurement of antibiotic use.
17a. Standardized facility prescription chart and medical records

The health-care facility ensures the availability and use of standardized prescription charts, medical records  
and transfer notes.
17b. Health-care facility policy for documenting prescribed medicines

The health-care facility has a written policy that requires prescribers to clearly document the indication
and antibiotics prescribed (agent, dose, route, interval, duration and review dates) in the prescription chart,  
medical record and transfer notes to other health-care institutions.

18. Basic training in optimal antibiotic use for health-care professionals
The health-care facility offers basic induction training (e.g. sensitization on AMR and use of standard  
4. EDUCATION AND TRAINING
treatment guidelines) to staff on how to optimize antibiotic prescribing, dispensing and administration.
19. Continued training in optimal antibiotic use for health-care professionals

The health-care facility offers continued educational resources (e.g. regular training on infection  
management) to train staff on how to optimize antibiotic prescribing, dispensing and administration.
20. Initial and regular training of the AMS team in infection management
The health-care facility offers initial and regular training of the AMS team in infection management
(diagnosis, prevention and treatment) and AMS. This training is usually not offered at the facility level, but is  
likely to be available at the regional, national or international level. The facility should, however, ensure that
members of the AMS team are adequately trained, according to local/national requirements.
21. Monitoring appropriateness of antibiotic use at the unit and/or facility-wide level through audits or
PPSsi
The AMS team undertakes audits or PPSs, at the unit and/or health-care facility level, to assess the
appropriateness of infection management and antibiotic prescription (e.g. indication, agent, dose and  
5. MONITORING AND SURVEILLANCE
duration of antibiotic therapy in specific infectious conditions such as pneumonia or surgical prophylaxis)
according to policy/guidance.
22. Monitoring quantity and types of antibiotic use (purchased/prescribed/dispensed) at the unit and/or
facility-wide level
In collaboration with the facility pharmacy, the AMS team monitors the quantity and types of antibiotic use  
(purchased/prescribed/dispensed) at the unit and/or health-care-facility level.
23. Monitoring of antibiotic susceptibility and resistance rates for a range of key indicator bacteria
The AMS team monitors antibiotic susceptibility and resistance rates for a range of key indicator bacteria at
the health-care facility-wide level, in alignment with national and/or international surveillance systems (e.g.  
GLASS).
24. Monitoring compliance of AMS interventions by the AMS committee

The AMS committee monitors compliance with one or more of the specific interventions put in place by the  
AMS team (e.g. indication captured in the medical record for all patients on antibiotics).
25. Regular evaluation and sharing of health-care facility data on antibiotic use with prescribers
Health-care-facility reports on the quantity of antibiotics purchased/prescribed/dispensed are reviewed and  
analysed, and key findings are shared with prescribers along with specific action points.
6. REPORTING AND FEEDBACK
26. Regular evaluation and sharing of health-care facility resistance rates with prescribers
The facility reports on antibiotic susceptibility rates are reviewed, and analyses and key findings are shared  
with prescribers along with specific action points.
27. Evaluation of appropriateness of data on antibiotic use is shared with prescribers

Findings from audits/reviews of the quality/appropriateness of antibiotic use are communicated directly to  
prescribers along with specific action points.
28. Health-care facility antibiogram for key antibiotics informed by data on antibiotic use and resistance
The health-care facility aggregate antibiogram is developed and regularly updated based on a review and
analysis of facility antibiotic use and antibiotic-resistant bacteria. The antibiogram may help to inform  
updates of clinical guidelines.
* In resource-limited settings, the functions of the AMS committee and AMS team may fall under the same team.
i
Indicator in the Tripartite M&E framework for the Global Action Plan on AMR.

4. PLANNING AN AMS PROGRAMME
I N A H E A LT H - C A R E FA C I L I T Y

4.1 Introduction Independent of the characteristics of the health-care facil-

ity, including size, an AMS programme should be adapted
AMS programmes in health-care facilities should not be to the facility’s human, financial, structural and organi-
vertical programmes. Rather, they should cut across oth- zational resources, and to the patient mix. An AMS pro-
er existing programmes to optimize antibiotic use, thereby gramme in a large tertiary hospital with different speciali-
improving quality of care and infection management. ties will necessarily be larger and more complex than one
in a district hospital. It is therefore important that health-
Health-care facilities are often differentiated as follows: care facility management and an AMS committee and/or
• private, not for profit, or public health-care facilities; AMS team together decide which strategies best fit their
• district, regional, tertiary or quaternary/central health- local setting, based on a situational analysis and develop-
care facilities (size, patient mix and available resources); ment of an action plan (Table 5). The implementation of an
• health-care facilities with or without a fixed financial AMS programme is a step-by-step dynamic process, with
budget; each facility building on what they already have in place.
• health-care facilities with or without their own This chapter provides insights that can help inform the de-
pharmacy; and sign of health-care-facility AMS programmes.36
• health-care facilities with or without an on-site
microbiology laboratory.

36
Mendelson M, Morris A, Thursky K, Pulcini C. How to start an antimicrobial
stewardship programme in a hospital. Clin Microbiol Infect. 2019 Aug 21.
[Epub ahead of print]
TA B L E 5
Preparation for developing and implementing an AMS programme in a health-care facility
Situational or Conduct a situational or SWOT analysis using the checklist of health-care facility core elements to identify existing
SWOT analysis and missing (but priority) elements, as well as possible enablers for and barriers to implementing a facility AMS
programme. Pay attention to:
• Structures, policies and guidelines: Identify which structures, policies and guidelines are in place and which are
critically in need of being put in place according to the checklist of facility core elements (see Chapter 3).
• Human resources: Identify the existing and required human resources (including competencies) needed for a
functioning governance structure for AMS, including the AMS committee and/or AMS team, and clinical and
other staff to be involved in implementing the AMS activities.
• Antimicrobial use and resistance data: Review data on antimicrobial consumption and/or use, and identify
challenges related to antibiotic prescribing practices in the facility and/or departments. Review existing
surveillance data on AMR and aggregate antibiograms from the facility.
• AMS activities: Identify any existing AMS activities (including ad hoc) in the facility/wards that can be built on
and made sustainable.
Facility AMS Based on the situational analysis, develop a health-care facility AMS action plan to ensure accountability, prioritize
action plan activities and measure progress. This should include the following key components:
• Core elements: Determine priority core elements to be implemented in the short and medium term, including
accountability, timeline and indicator.
• Governance: Identify leadership commitment and oversight, and establish an AMS committee (new or
incorporated into an existing structure) and an AMS team that is endorsed by the facility leadership.
• AMS activities: Identify areas for improvement, implement AMS interventions (who, what, where, when and
how), monitor and evaluate, and report and feed back the results.
• Health-care facility-wide engagement: Ensure facility-wide engagement in the AMS programme, and empower
the AMS committee and/or AMS team to undertake the AMS interventions and monitor their implementation.
• Education and training: Identify competencies that need to be strengthened to effectively implement AMS, and
develop a facility AMS education and training plan.
• Budget: Develop a budget for the AMS programme, including human and financial resources required for the
day-to-day running of the programme as well as for education and training on AMS of the AMS team and health-
care professionals. The budget should be endorsed by the health-care facility leadership.

4.2 Conducting a situational or SWOT analysis The situational and/or SWOT analysis will help the health-
care facility in developing a stepwise AMS action plan that
Before an AMS programme is developed and implement- identifies what is already in place (health-care facility core
ed, a situational or SWOT analysis should be performed. elements), what needs to be put in place over time (short-
For AMS programmes, this information is important in de- and medium/long-term priorities), the human resources
termining what needs to be done and what can be done. needed (including champions), the composition of an AMS
This analysis does not need to be a complex exercise, but team and other core elements (including guidelines) based
rather a pragmatic one that includes the following: on the facility core elements checklist and priorities.
• mapping which core elements are in place in the facility; Figure 6 provides an example of a SWOT analysis for planning
• u ndertaking a baseline antibiotic use analysis; an AMS programme in a health-care facility. It lays out the
• identifying main challenges related to antibiotic pre- strengths, weaknesses, opportunities and threats involved in
scribing and use; and determining how ready the facility is to implement AMS and
• identifying available human and financial resources. paves the way for developing a facility AMS action plan.
The situational analysis should include: Putting the core elements in place in the facility enables sus-
• s trengths, weaknesses, opportunities and threats tainable action on AMS, even if that means through collabo-
(SWOT) at different levels in the facility; and ration with neighbouring facilities. For example, if there is
• p ossible barriers and enablers for the full participation no facility antibiotic guideline or a pharmacist to analyse anti-
of the different health-care professionals and depart- microbial consumption data, an option may be to adopt the
ments in the AMS programme. guideline from a neighbouring facility with a similar context and
collaborate with their pharmacist to analyse the AMC data.
FIGURE 6
Example of a SWOT analysis for AMS readiness in a health-care facility
HELPFUL HARMFUL
Strengths Weaknesses
Core elements: Core elements:
INTERNAL/PRESENT FACTORS
• A MR and AMS are a leadership priority. • No medical record or prescription pad is available.
• IPC programme/committee is active. Human resources:
Human resources: • No dedicated health-care professional is available to lead
• T
here is enthusiasm for AMS in the facility/wards. the AMS team.
• T
here is clinical knowledge of AMS. Antimicrobial use and resistance data:
Antimicrobial use and resistance data: • The supply of microbiology reagents is poor.
• P
rescription audit is conducted in one ward. • The supply of antibiotics is poor.
• F
acility aggregate antibiogram is available. AMS activities:
AMS activities: • Health-care professionals have competing priorities and
• A pharmacist is involved in some AMS activities in little time for AMS work.
one ward.
SWOT
Opportunities Threats
Core elements: Core elements:
EXTERNAL/FUTURE FACTORS
• A ctive implementation of the NAP on AMR • Unstable access to essential antibiotics

• Increasing national awareness of AMR and its • Increased costs for antibiotics
consequences for health • Prioritization of issues other than AMS in the facility
Human resources: • Low facility budget
• Incorporating AMS responsibility into the IPC committee Human resources:
Antimicrobial use and resistance data: • Too many nonfunctional committees in the health-care facility
• F unds for conducting a facility PPS Antimicrobial use and resistance data:
AMS activities: • Increasing AMR rates, including carbapenem-resistant
• P
resenting findings from AMS activities to other wards/ Enterobacteriaceae (CRE)
health-care professionals AMS activities:
• Opposition from clinical leaders

4.3 Identifying human resources In addition, a clinical leader for the AMS team should be
identified who has sufficient training in AMS or infection
It is essential to have a governance structure (Figure 7) management to manage the most common issues.
that includes the different functions needed to effectively
implement a health-care facility AMS programme.37 The In smaller health-care facility, the AMS clinical leader may
governance structure may vary in size and complexity de- sometimes be the only member of the AMS programme.
pending on the facility. Most important is to identify the Where the AMS clinical lead is not a doctor, one (inside or
responsibility and accountability of the hospital manage- outside the facility) should be identified (on-site or off-site)
ment, and of those who are to coordinate and implement to provide medical advice and support to the AMS team,
the AMS programme. which can be led by a pharmacist or nurse, when required.
Similarly, if a pharmacist is not a member of the AMS team
The health-care facility leadership/management should on-site, it is useful to identify a pharmacist (inside or out-
formally endorse the facility AMS action plan and provide side the facility) from whom advice can be sought.
organizational and structural support by allocating the re-
quired financial and human resources for AMS activities. In many settings a hierarchical health-care facility struc-
It is essential that the health-care facility leadership/man- ture may pose a barrier for this kind of teamwork. In such
agement endorse the health-care facility AMS governance cases it may be important to formally endorse pharma-
structure to empower the AMS committee, AMS team and/ cists and nurses as part of the AMS team. Moreover, the
or AMS champions to implement the AMS programme ef- AMS team members should be given the responsibility and
fectively. authority required to perform AMS activities, recognizing
a team of different individuals and professions with com-
An AMS committee in the health-care facility should pro- plementary competencies provides for more opportunities
vide leadership and overall coordination of the AMS pro- to perform AMS interventions adapted to local clinical set-
gramme. The AMS committee can be a stand-alone com- tings. In this regard, health-care facility administrative and
mittee or be integrated into an existing structure, such as managerial support is essential.
the infection control, patient safety or drug and therapeu-
tics committee with clear terms of reference. It can be an The skill sets of professionals who traditionally under-
opportunity to revitalize or empower existing committees. take roles in AMS are defined below. How these human
If integrated into an existing committee, AMS must be a resources are secured and how AMS tasks are assigned de-
standing item on the committee’s agenda (see the sample pend on the local context, needs, resources, health-care
AMS committee terms of reference in Annex II). The chair landscape and availability of expertise. Roles often require
of the AMS committee (representing the facility manage- adaptation, with different professionals taking on different
ment) should be responsible for providing leadership sup- or multiple roles. Nevertheless, the emphasis must be to
port and is accountable for the overall implementation of ensure that whoever undertakes the core tasks has the re-
the AMS programme. quired generic skill sets and competencies (see Chapter 7).
A multidisciplinary AMS team (or individual, depending Expertise in infection management is provided by an in-
on availability and the size of the health-care facility) of fectious disease or infection specialist, or a physician with
different health-care professionals17 should be established, interest and experience in infectious diseases. In the AMS
who collectively possess the competencies and undertake team this person is the main source for supporting pre-
functions to successfully deliver and implement AMS pro- scribers in diagnosing and managing patients, including
grammes in health-care facilities. Ideally, the AMS team optimal use of antibiotics to treat infections.38 In addition,
should comprise a prescribing clinician, a pharmacist, a the infection management expert supports guideline de-
nurse and a (clinical) microbiologist or laboratory techni- velopment, pre-authorization and post-prescription AMS
cian in facilities with a microbiology laboratory (see the interventions, including review and feedback, and solicited
checklist of health-care facility core elements in Chapter or unsolicited consultations, as well as review and analysis
3). If available, an infectious disease physician, a clinical of progress reports. The person also supports the devel-
pharmacologist, and/or a nurse with expertise in infec- opment, coordination, dissemination, delivery and evalua-
tions or IPC are also recommended. The AMS team should tion of educational programmes, which are then included
have a clear terms of reference (see the sample terms of in the implementation of the AMS education strategy and
reference for an AMS team in Annex III). The nominated
staff in the team need dedicated time to implement the
37
Colligan P, Beggs JJ, Walsh TR, Gandra S, Laxminarayan R. Anthropological
and socioeconomic factors contributing to global antimicrobial
programme, and their AMS role should be in their job de- resistance: a univariate and multivariable analysis. Lancet Planet Health.
scription and performance contract. 2018;2:e398–e405.

AN EXAMPLE OF A
FIGURE 7
HEALTH-CARE FACILITY AMS
GOVERNANCE STRUCTURE
Example of an AMS governance structure for health-care facilities in LMICs
Drug & therapeutics Health-care

Heads of departments
committee facility leadership
Patient safety
AMS committee IPC committee
committee
Microbiology AMS team AMS champions
Pharmacists, Medical
Surgeon
nurses etc. practitioner

framework (see Chapter 7). The physician often leads the For effective and sustainable stewardship initiatives, the
AMS team. But increasingly pharmacists and nurses are roles individual team members undertake may naturally
taking on this role, while recognizing the need to be able to change over time. For example, a nurse who initially had a
consult with a physician in certain areas of infection man- supporting role in the AMS programme may develop skills
agement. that will allow him or her to undertake surveillance, or an
education or safety role, and a pharmacist may move from
Expertise in antimicrobials is often the domain of a phar- implementation to more of a governance role over time.
macist or pharmacologist (if available).39 In health-care
facilities they traditionally help to develop guidelines and Additional expertise is essential to complement the skills
formularies and oversee the purchasing and supply of an- of the AMS team, such as local champions and health-care
timicrobials, dispense antimicrobials in wards/units and professionals who can participate in performing and facil-
review the prescription order, identify and find solutions itating stewardship interventions on their wards. Also, if
to stock-outs and shortages, perform surveillance of AMC a health-care facility has a quality improvement, patient
and use (e.g. AMC data, PPS or prescription audits), and safety or IPC programme (Box 3) with dedicated staff, se-
participate in their analyses. In wards they perform re- curing some of their time to focus on AMS activities is ad-
views of antibiotics prescribed (through prospective or ret- vantageous.
rospective audit with feedback), optimize antibiotic dosing
in patients with organ dysfunction and comorbidities, and
promote best practice in prescribing, dispensing and ad-
ministering medicines, including antibiotics. 4.4 Link between IPC and AMS
Expertise in patient care is typically provided by nurses.40 The case study from Barbados (Box 3) is a good illustration
They are considered crucial because they have first-hand of how AMS programmes are often initiated in facilities or
information about patients. Focusing more on support- even countries due to an outbreak of multidrug-resistant
ing optimal care and patient safety rather than strictly (MDR) bacteria. Likewise, it is often the same people in-
on antibiotic prescriptions may facilitate greater engage- volved in issues related to IPC and AMS both at the facility
ment from nurses, as this is part of quality nursing care.41 level and the national (state/regional) level. This is because
This AMS team member should promote timely antibiotic IPC and AMS are two sides of the same coin when it comes
administration without missing doses, therapeutic drug to development and spread of AMR, optimizing antibiotic
monitoring (if available), quality microbiological sampling use and providing quality health care, as shown in Figure
and communication of laboratory results to prescribers to 8 and Box 4.
support antibiotic prescription decisions. Furthermore,
nurses should encourage monitoring of patients’ clinical
progress and the side effects or ineffectiveness of medi-
cines, identify opportunities to switch antibiotics from IV
to oral and to monitor the correct handling of patients’
invasive devices. Nurses may engage in data collection
for audits and surveillance of antimicrobial consumption
and use, and educate patients, families and colleagues
(if empowered by the health-care facility leadership to
do so) about optimal antimicrobial use as well as recom-
mended IPC and water, sanitation and hygiene (WASH)
39

Goff DA, Rybak MJ. Global antimicrobial stewardship: challenges and
behaviours and practices. successes from frontline stewards. Infect Dis Ther. 2015;4:1–3.
40

Brink A, Van den Bergh D, Mendelson M, Richards GA. Passing the baton
to pharmacists and nurses: new models of antibiotic stewardship for South
Expertise in microbiology is often provided by a micro-
Africa? S Afr Med J. 2016;106(10):947–8.
biologist or laboratory technician to process samples for 41

Cotta MO, Robertson MS, Marshall C, Thursky KA, Liew D, Buising KL.
diagnosis and antibiotic susceptibility testing, and to feed Implementing antimicrobial stewardship in the Australian private hospital
system: a qualitative study. Aust Health Rev. 2015;39:315–22.
back the results to the prescribers as well as to develop 42

Improving infection prevention and control at the health facility. Interim
and regularly update the health-care facility’s aggregate practical manual supporting implementation of the WHO Guidelines
on Core Components of Infection Prevention and Control Programmes.
antibiogram. Not all health-care facilities have a micro- Geneva: World Health Organization; 2018 (https://www.who.int/infection-
biology laboratory; for smaller health-care facilities, this prevention/tools/core-components/en/, accessed 3 September 2019).
43

Adapted from Figure 2 in ref. 42 (https://www.who.int/infection-prevention/
service could be provided through collaboration with other tools/core-components/ipc-cc_visual.pdf?ua=1, accessed 3 September
facilities. 2019).

FIGURE 8
Links between IPC and AMS in delivering quality health care and optimizing antibiotic use
IPC AMS
Prevent spread Prevent antibiotic
o f b a c te r i a selection pressure
and infections and optimize use
B OX 4
Core components of IPC and the link to AMS
IPC is a practical, evidence-based approach which aims to prevent patients and health-care workers (HCWs) from being
colonized with bacteria or getting infections. The implementation of IPC interventions not only prevents health-care-
associated infections and deaths, but also saves money, reduces the spread of AMR and supports high-quality, people-
centred health services. Comprehensive and effective IPC consists of establishing IPC programmes with strong links
to other programmes, e.g. AMS programmes and other initiatives addressing AMR. According to the relevant WHO
core components guidelines,
implementing IPC promotes
adoption of appropriate IPC
practices during health-care
delivery, thus enhancing patient
safety and quality of care42
(Figure 9). This approach is
complementary to that of AMS, IPC Program m es
and all relevant programme linkages
which aims to prevent the spread
AMS
of MDR bacteria and infections
by reducing overuse and misuse
of antibiotics. Both IPC and
AMS are interdependent
programmes that require EDUCATION AND
MONITORING,
GUIDELINES SURVEILLANCE AUDIT AND
coordinated efforts and TRAINING
FEEDBACK
interventions to achieve the
greatest impact.
Enab ling e nv ironm e nt

WORKLOAD, STAFFING, AND BED OCCUPANCY
FIGURE 9 BUILT ENVIRONMENT, MATERIALS AND EQUIPMENT
Linkage of AMS and the IPC

core components43

4.5 Use of antibiotics in health-care facilities Using these data for AMS programmes requires certain
drug expertise as well as knowledge and training in data
The main purpose of collecting data on the use of antibi- collection, management and analysis. For more detailed
otics is to assess the extent and quality of antibiotic use, information on how to assess the impact of AMS pro-
identify problematic prescribing practices, and compare grammes, see the structural indicators detailed in the
appropriate use across health-care facilities and within a health-care facility core elements checklist (Table 4), and
health-care facility, department or ward over time. Meas- advice on assessing AMS programmes in Chapter 6.44
uring the quantity and appropriateness of antibiotic pre-
scribing and use will identify where there is room for im- 4.5.1 Quantity – AMC data
provement in targeting and monitoring AMS interventions. The term “consumption” refers to estimates that are de-
rived from aggregated data sources, mainly procurement
The human and IT resources required for collecting this data and dispensing data, and serves as a proxy for actual anti-
are often regarded as a barrier to effective measurement. biotic use. These data sources do not contain any patient
Therefore, it is advised to collect only the data essential for information or treatment indications, but they can provide
providing feedback to health-care professionals on their an- an estimate on the quantity and types of medicines con-
tibiotic use and to try to get them involved in the data collec- sumed at the national, subnational or facility level over
tion. Integrating data collection as part of the requirements time. Data should be collected according to a protocol from
for other initiatives (e.g. infection control, patient safety and a recognized international methodology such as the WHO
antisepsis programmes) is also an efficient way to collect crit- methodology on national/hospital surveillance of AMC.45
ical data without duplication. Data should be collected ac- This can be collected at the national or health-care facility
cording to a protocol, and the data quality should be validat- level and stratified using the AWaRe classification and/or
ed. Although electronic data collection is ideal, paper-based other relevant clinical categories. A step-by-step guide on
collection is very common and acceptable. setting up a national AMC surveillance programme at the
facility level is shown in Box 5.
Three main types of antibiotic data are used to provide
baseline information and evaluate AMS interventions.
Each type of data – antibiotic consumption, antibiotic use
44

Harbarth S, Hackett J. Introduction: DRIVE-AB’s definitions and indicators to
and antibiotic audit data – has advantages and disadvan- monitor responsible antibiotic use. J Antimicrob Chemother. 2018;1:vi2.
tages (see Chapter 4.5.1–3). Different data sets require 45

WHO methodology for a global programme on surveillance of
antimicrobial consumption. Version 1.0. Geneva: World Health
different data sources, as shown in Figure 10 on antimi- Organization; n.d. (http://www.who.int/medicines/areas/rational_use/
crobial consumption vs antibiotic use data sources. WHO_AMCsurveillance_1.0.pdf, accessed 4 February 2019).
FIGURE 10
Pharmaceutical value chain indicating potential data sources for surveillance of antimicrobial
consumption and use
A nt i bio t ic
Co n su m p t io n Data
Appropriate
Dispensing Use
Prescribing
Procurement
Selection, and supply
Market pricing and
registration reimbursement
Manufacturing
R&D
A ntibio tic
Use Data

B OX 5
Step-by-step guide for setting up an AMC surveillance programme at the facility level46
Step 1: Structures and governance

• A
ppoint a person/team to manage and coordinate the local surveillance system at the facility level
(part of an already existing structure such as the AMS or IPC committee).
• A
ssign tasks and responsibilities with clear terms of reference.
Step 2: Objectives and methodology

• D efine the objectives and outputs of the facility surveillance programme.
• D etermine the surveillance framework with respect to hospital structure, antimicrobial classes and frequency of
data collection.
• Identify the sources of consumption data and the type of hospital activity indicator.
Step 3: Data collection and validation

• C
ollect consumption and hospital activity data.
• V
alidate and clean the data.
Step 4: Data analysis and reporting

• Identify the target groups for the results.
• A nalyse and report data, taking into account the identified target groups.
• If applicable, report the data to the national surveillance system.
Step 5: Use of the data and follow-up

• S upport the AMS and hospital medicines management in analysing the data.
• Improve the system to meet the requirements of the target groups.
Benefit: Data on antimicrobial consumption are often 4.5.2. Quality – antibiotic use data (PPS)
readily available and measured using the WHO ATC/DDD The expression “antibiotic use data” refers to estimates
(Anatomical Therapeutic Chemical Classification/ Defined derived from individual patient data and may include in-
Daily Dose) methodology. This method refers to routine formation on patient characteristics and indications for
surveillance of existing data at no additional cost. Data at treatment. Collection of use data is more resource de-
the facility level are collected from procurement, and dis- manding than consumption data, but the additional infor-
pensing data are ascertained from the facility pharmacy or mation provided is important for e.g. AMS programmes
other available sources along with the number of occupied and to identify areas for improving antibiotic use. “Point
beds or patient admissions during the study period. prevalence survey” refers to the collection of antibiotic
treatment data from hospitalized inpatients (all patients
Limitation: Independent of how the data are obtained, there or a sample) at a point in time according to a recognized
are several possible sources of error. For example, the facil- international methodology such as the WHO methodolo-
ity purchase data may not capture all the antibiotics used in gy for PPS on antibiotic use in hospitals.48 A step-by-step
the facility, or the facility may accept donations outside the guide for setting up a health-care facility PPS is shown in
formal procurement process. If there is no fixed population Box 6.
per health-care facility, it may be difficult to calculate the
denominator.47 Because the information is not as detailed
as in a PPS or audit study, and the indication is missing, con-
sumption data ensure only the quantity and types of antibi- 46

Draft WHO methodology for antimicrobial consumption surveillance in
hospitals. Geneva: World Health Organization; 2019.
otics, not the quality of prescribing. Nonetheless, this meth- 47

Chandy S et al. Patterns of antibiotic use in the community and challenges of
od still provides a valuable estimate, especially for analysing antibiotic surveillance in a lower-middle-income country setting: a repeated
cross-sectional study in Vellore, South India. J. Antimicrob Chemother.
trends. Expressing antimicrobial consumption in DDDs for 2013;68(1):229–36.
paediatric populations is biased, as dosage is often age and 48

WHO methodology for point prevalence survey on antibiotic use in hospitals.
Version 1.1. Geneva: World Health Organization; 2019.
weight dependent, with marked differences to adult DDDs.

Benefit: Facility PPS data provide an overview of how an- prescribers. Though auditing may sometimes be laborious,
tibiotics are used in a facility. A PPS also allows assess- it is an essential part of any AMS programme and should
ment of compliance to guidelines because it includes more be encouraged.49 This method can begin with weekly or
specific data, such as indications for antibiotic treatment, bimonthly quick audits (only a few patients) during ward
prescribed antibiotic(s), dosage, timing of administration rounds, with real-time feedback to the prescribers, similar
of first dose, dose interval and drug administration route, to a repeated and small-scale PPS. For more detailed infor-
though not duration of treatment. It is recommended that mation and examples, see Chapter 5.8 on prospective and
local PPSs be performed regularly. A PPS can be integrat- retrospective audit with feedback.
ed with other surveys (e.g. of surgical site infections) to
optimize resources.
Limitation: Data are collected at a point in time (5–7 days) 4.7 The EML and AWaRe classification
and may not be representative, as less frequent practices
might be missed. Conversely, if data are collected during The WHO EML AWaRe50 classification of commonly used
outbreaks, higher use would be reported. Doing a PPS is antibiotics into three groups – ACCESS, WATCH and RE-
more resource-intensive than collecting antimicrobial con- SERVE – provides a tool to support antibiotic monitoring
sumption data, as data are collected on individual patients. and AMS activities, with recommendations on when to use
4.5.3. Quality – antibiotic audit data 49

Ivers N, Jamtvedt G, Flottort S, Young JM, Odgaard-Jensen J, French SD
“Auditing” refers to the prospective (real-time) or retrospec- et al. Audit and feedback: effects on professional practice and healthcare
outcomes. Cochrane Database Syst Rev. 2012 June 13;6:CD00259.
tive collection of antibiotic prescription data on hospitalized 50

Executive summary: the selection and use of essential medicines 2019.
patients. The data are analysed and then fed back to the Geneva: World Health Organization; 2019.
B OX 6
Step-by-step guide for setting up a health-care facility PPS48
Step 1: Structures and governance

• Identify the team/committee in the facility with the overarching responsibility for the PPS, often the committee also
responsible for AMS.
• A s part of this team/committee, appoint a facility PPS focal point responsible for coordination and day-to-day
management of the survey and investigators (surveyors).
Step 2: Objectives and methodology

• D efine the objectives and output of the PPS in the facility.
• S elect a standardized PPS protocol for the survey, e.g. WHO PPS protocol, Global PPS.
• T rain the hospital PPS focal point, team and investigators in the methodology.
Step 3: Preparation
• O
btain ethical approval and other necessary permissions to undertake the survey.
• A
gree on the days for conducting the surveys in the respective wards.
• P
repare the necessary materials for undertaking the survey.
Step 4: Data collection and validation

• U ndertake a pilot survey in one ward to validate the data, and operationalize the survey procedures.
• C onduct the survey in all wards according to predefined timelines.
• r ansfer data from paper to electronic format when applicable, and validate the data.
Step 5: Data analyses and reporting

• C lean and analyse the data based on a predefined data analysis plan according to target groups.
• R eport results to the responsible team/committee, the facility management, etc.
• Identify areas for improving antimicrobial prescribing and use based on results, and agree on AMS interventions to
address these areas.
• M onitor and evaluate the AMS interventions with e.g. a targeted PPS or audits.

FIGURE 11
Overview of the WHO AWaRe groups and essential antibiotics on the WHO EML50
A CCESS GROUP
Amikac in Ce fazolin Nitrofurantoin
This group includes antibiotics and antibiotic classes
that have activity against a wide range of commonly Amox ic illin Chloramp he nicol P he noxy methyl-
encountered susceptible pathogens while showing pe nic illin
Amox ic illin + Clindamyc in
lower resistance potential than antibiotics in Watch clav ulanic ac id P rocaine
and Reserve groups. Access antibiotics should be Cloxac illin be nzylpe nic illin
Ampic illin
widely available, affordable and quality-assured to Doxyc ycline Spec tinomyc in
improve access and promote appropriate use. Be nzathine
be nzylpe nic illin Ge ntamic in Sulfamethoxazol e
Selected Access group antibiotics (shown here) are Metronidazole + tr imethop r im
Be nzylpe nic illin
included on the WHO EML as essential first-choice or
second-choice empirical treatment options for specific Ce falex in
infectious syndromes.
WA T C H GROUP
This group includes antibiotics and antibiotic classes that have higher Azithromyc in Cip rofloxac in
resistance potential and includes most of the highest priority agents among Ce f ix ime Clar ithromyc in
the Critically Important Antimicrobials (CIA) for Human Medicine and/or
antibiotics that are at relatively high risk of selection of bacterial resistance. Ce fotax ime Me rope ne m
Watch group antibiotics should be prioritized as key targets of national and Ce ftazidime P ipe rac illin +
local stewardship programmes and monitoring. tazobac tam
Ce ftr iaxone
Selected Watch group antibiotics (shown here) are included on the WHO EML Ce furox ime
Vancomyc in
as essential first-choice or second-choice empirical treatment options for a
limited number of specific infectious syndromes.
R E S E RV E GROUP
This group includes antibiotics and antibiotic classes that should be reserved for treatment Ce ftazidime + av ibac tam
of confirmed or suspected infections due to multi drug-resistant organisms, and treated as Colistin
“last-resort” options. Their use should be tailored to highly specific patients and settings,
when all alternatives have failed or are not suitable. They could be protected and prioritized Fosfomyc in ( intrave nous)
as key targets of national and international stewardship programmes, involving monitoring L inezolid
and utilization reporting, to preserve their effectiveness.
Me rope ne m + vaborbac tam
Selected Reserve group antibiotics (shown here) are included on the WHO EML when they P lazomic in
have a favourable risk-benefit profile and proven activity against “Critical Priority” or “High
Priority” pathogens identified by the WHO Priority Pathogens List, notably carbapenem- Poly my x in B
resistant Enterobacteriaceae.
the antibiotics in each category. Selected AWaRe antibiot- the national level to enable health-care facility AMS in-
ics are included on the WHO Model EMLs as recommend- clude the following:
ed treatment options for specific infectious syndromes
(Figure 11). • r eview/update national EMLs with AWaRe groups;
• r eview/update Sustainable Development Goals with
The full AWaRe database, along with further guidance AWaRe groups;
on how to apply the WHO AWaRe classification for de- • align empirical antibiotic treatment guidelines with
veloping and updating national EMLs, developing and ACCESS antibiotics;
updating treatment guidelines, and for monitoring anti- • target WATCH and RESERVE groups for AMS;
microbial consumption and use (including more intense • review antimicrobial consumption and use surveillance
surveillance of the RESERVE antibiotics), will be made data with AWaRe; and/or
available on the WHO website. However, some examples • include in health professional curricula.
of how the AWaRe classifications can be incorporated at

Stratifying total antimicrobial consumption data by the and which antibiotics the causative bacteria are sensitive
AWaRe groups can be undertaken at multiple levels, in- to. Microbiology laboratories play a key role in informing
cluding at the national (state/regional), facility and ward the appropriate use of (ACCESS) antibiotics, ensuring first-
level. This allows benchmarking and overall monitoring of and second-line antibiotics are used whenever possible.
national and global progress towards WHO’s goal of in- The quality of the clinical diagnosis is still essential, as the
creasing the proportion of global consumption of antibi- tests need to be interpreted in light of it.
otics in the ACCESS group to ≥60%.51 Figure 12 shows an
example of how the AWaRe groups can be integrated into Many countries lack microbiology laboratories with exter-
national AMC surveillance data to highlight the proportion nal quality assurance and microbiology expertise altogeth-
of antimicrobial consumption across the categories. er. However, with the implementation of national action
plans on AMR, countries are encouraged to collect and
analyse local resistance data and establish national AMR
surveillance systems reporting to GLASS.53 A brief intro-
4.7 Microbiology duction to GLASS is provided in Box 7.
Most patients, both in health-care facilities and in pri-

mary health-care settings, receive initial antibiotic treat-
ment based on a clinical assessment, without the use of
microbiological tests. Treatment is chosen according to
which microbes are most likely to cause different infec-
tions. This strategy works well when resistance rates are
low, or AMR surveillance can guide recommendations for 51

Thirteenth general programme of work 2019−2023. Geneva: World Health
empirical antibiotic treatment. There is a great need for Organization; 2018.
affordable, sensitive, specific and rapid diagnostic tests 52

WHO report on surveillance of antibiotic consumption: 2016–2018 early
implementation. Geneva: World Health Organization; 2018.
that provide prescribers with quality-assured information 53

Global antimicrobial resistance surveillance system (GLASS): manual for early
about whether or not a patient has a bacterial infection, implementation. Geneva: World Health Organization; 2015.
FIGURE 12
Proportional consumption (%) of antibiotics by AWaRe classification in six countries of the Western
Pacific Region, 201552
100
90
80
70
60
Proportion (%)
50
40
30
20
10
0
Brunei Japan Mongolia New Philippines Republic
Darussalama Zealandb of Korea
Other Watch
Reserve Access
a
Only public sector reported.
b
Only community consumption reported.

B OX 7
Snapshot of GLASS53
Launched in 2015, GLASS is being developed to support the Global Action Plan on AMR. The aim is to support global
surveillance and research in order to strengthen the evidence base on AMR and antimicrobial use and to help inform
decision-making and drive national, regional and global actions.
GLASS promotes and supports a standardized approach to the collection, analysis and sharing of AMR and antimicrobial
use data at a global level. GLASS does this by encouraging and facilitating the establishment of national AMR surveillance
systems capable of monitoring AMR and antimicrobial use trends and producing reliable and comparable data.
GLASS objectives:
• foster national surveillance systems and harmonized global standards;

• analyse and report global data on AMR and antimicrobial use on a regular basis;
• estimate the extent and burden of AMR globally by selected indicators;
• detect emerging resistance and its international spread;
• inform implementation of targeted prevention and control programmes; and
• assess the impact of interventions
Countries benefit from participation in GLASS through enhanced capacity building, access to training and implementation
tools, and support in collecting AMR and antimicrobial use data at the local and national level.
Efforts are being made to meet country needs, including in developing antibiotic guidelines and policy based on lo-
capacity building for specimen collection, antibiotic sus- cal resistance surveillance, and to educate clinical staff on
ceptibility testing and IT systems for analysing AMR pa- quality sampling for microbiology testing and AMR rates.
tient data.54 In addition, microbiologists require support from the AMS
team to ensure they receive basic demographic and clin-
The main function of microbiologists (or laboratory tech- ical data to help in analysing laboratory results. Finally,
nicians) in an AMS programme is to interpret and commu- where possible, microbiologists support the AMS team by
nicate microbiology results to prescribers, and to develop reporting on MDR organisms and selectively reporting sus-
and update antibiograms and communicate their value ceptibility data to the facility management and prescribers.
and limitations. An example of an aggregate antibiogram
(only for gram- negative bacteria) can be found in Annex
54
Diagnostic stewardship: a guide to implementation in antimicrobial resistance
VIII. Microbiologists also serve to support the AMS team surveillance sites. Geneva: World Health Organization; 2016.

5 . P E R F O R M I N G A M S I N T E RV E N T I O N S
I N A H E A LT H - C A R E FA C I L I T Y

Key audience: AMS team
5.1 Implementing an AMS programme However, intrinsic factors may also influence antibiotic
prescribing behaviour and need to be addressed. Exam-
One main outcome of performing AMS interventions in a ples of intrinsic factors include the following:58
health-care facility is behaviour change in antibiotic pre-
scribing practices, leading to more responsible use of an- • p erception that AMR is an immediate threat (lack of
tibiotics. Implementing AMS programmes is a strategy for awareness and knowledge about AMR);
changing this behaviour over time.55 • fear of losing a patient;
• belief that broad-spectrum antibiotics are very effective
The health-care facility core elements reflect some of and low risk;
the evidence that has been shown to inform clinical/pro- • influence of a senior physician’s preferences on a junior
fessional practice, e.g. leadership commitment, data on physician’s prescribing;
antimicrobial consumption and use, standard treatment • physician autonomy in prescribing what he or she
guidelines, and AMS teams and champions. SWOT analy- thinks is best; and
sis is important in highlighting possible barriers and ena- • uncertainty due to inadequate microbiology services.
blers to implementation of an AMS programme (e.g. data
on antimicrobial consumption and use), helping to identify Consequently, when performing AMS interventions, im-
areas for improvement and monitoring use over time. The plementation requires that they be tailored to address the
health-care facility AMS action plan provides an overview different factors that may influence antibiotic prescribing
of the facility AMS programme with overall goals, how they and use in a specific context.59 Two ways of tailoring AMS
will be reached and by whom, and how progress will be interventions are to involve clinical staff in identifying lo-
measured. However, having a plan is not enough – it has to cal targets for improving antibiotic use (Chapter 5.3) and
be implemented. to have a systematic approach to implementing AMS in-
terventions, review progress over time and make changes
“It is not just what you do, it is how you do it.” when appropriate (Chapter 5.4).
(Dr Hanan Balkhy, Assistant Director-General for

Antimicrobial Resistance, WHO)
5.2. Implementing AMS interventions and

behaviour change
It is said that using evidence-based interventions is no

guarantee of success, because success depends on im-
plementing the interventions. Implementation research is
defined as “methods to promote the uptake of proven clin-
ical treatments, practices, organizational and management 55

Hulscher MEJL, Prins JM. Antibiotic stewardship: does it work in
hospital practice? A review of the evidence base. Clin Microbiol Infect.
interventions into routine practice, and hence to improve 2017;23:799–805.
health.” It identifies the behavior of healthcare profession- 56

Implementation Science (https://implementationscience.biomedcentral.
com/about, accessed 3 September 2019).
als and healthcare organizations as key sources of vari- 57

Teixeira Rodrigues A, Roque F, Falcão A, Figueiras A, Herdeiro MT.
ance requiring improved empirical and theoretical under- Understanding physician antibiotic prescribing behaviour: a systematic review
standing before effective uptake can be reliably achieved56 of qualitative studies. Int J Antimicrob Agents. 201e;41:203–12.
58

Krockow EM, Colman AM, Chattoe-Brown E, Jenkins DR, Perera N, Mehtar
Hence, implementing evidence-based AMS interventions10 S et al. Balancing the risks to individual and society: a systematic review
to change prescribing behaviour means taking into account and synthesis of qualitative research on antibiotic prescribing behavior in
hospitals. J Hosp Infect. 2019;101:428–39.
factors that influence prescribing and use at the facility/de- 59

Flottorp SA, Oxman AD, Krause J, Musila NR, Wensing M, Godycki-Cwirko
partment/ward level. Many structural and organizational M et al. A checklist for identifying determinants of practice: a systematic
review and synthesis of frameworks and taxonomies of factors that prevent
factors, also called extrinsic factors, are addressed in de- or enable improvements in healthcare professional practice. Implement Sci.
veloping a facility AMS programme/action plan.57 2013;8:35.

5.3 Identifying local targets for improving context, and assessing their success (Figures 13–15). This
antibiotic use model can be applied at the facility level in small facilities
or at departmental or ward level in larger facilities. For
Table 6 lists some common, very generic areas for improv- assessing the outcomes of AMS interventions, see Chapter
ing antibiotic prescribing. In a smaller facility, the overall 6. It is important to agree on a set time period (e.g. 3–6
goal identified in the AMS action plan may be sufficient, months) for reviewing the impact of the AMS interventions
and the same AMS interventions may be implemented and adjusting them.
over the whole facility. However, in a larger facility, a sur-
gical department may have different priorities to a medical Key message:
department. In that case, it is more meaningful for each AMS interventions should be implemented
department to set their own SMART (specific, measurable, in a stepwise approach, build on existing
achievable, relevant, time-bound) goals. structures and reporting, maximize
teamwork, and encourage champions and
clinical staff – including prescribers – to
participate. Start small and keep it simple
5.4 A systematic approach to implementing and doable.
AMS interventions
The continuous quality improvement model60 provides

a systematic approach for involving clinical staff in AMS

60
Langley GL, Moen R, Nolan KM, Nolan TW, Norman CL, Provost LP. The
team efforts to set SMART goals for change, tailoring improvement guide: a practical approach to enhancing organizational
and implementing interventions appropriate for the local performance. 2nd edition. San Francisco: Jossey-Bass; 2009.
TA B L E 6
Nine common areas for improving antibiotic prescribing
PRESCRIPTIONS WHAT TO IMPROVE
1. Overprescribing Antibiotics are prescribed when not needed, e.g. fever without evidence of infection, asymptomatic urinary
tract colonization, viral infections, malaria, inflammatory conditions.
2. Overly broad More broad-spectrum antibiotics (WATCH and RESERVE antibiotics) are prescribed than are necessary (e.g.
spectrum surgical prophylaxis).
3. Unnecessary Multiple antibiotics are used, particularly with overlapping spectra and in combinations that have not been
combination therapy, shown to improve clinical outcomes.
including certain fixed-
dose combinations
4. Wrong antibiotic Wrong antibiotic(s) are prescribed for particular indications/infections.

choice
5. Wrong dose Antibiotics are prescribed with the wrong dose (over- or underdosing).
6. Wrong dose interval Antibiotics are prescribed with the wrong dose interval (too much time between doses).
7. Wrong route Antibiotics are prescribed by the wrong route (e.g. IV instead of oral).
8. Wrong duration Duration of antibiotic treatment should be optimized (e.g. antibiotics prescribed for too long a period,
prolonged surgical prophylaxis).
9. Delayed Administration of the antibiotic(s) is delayed from the time of prescription. Repeat doses are not administered
administration in a timely way, which is critical in the case of septic shock and other serious infections.

FIGURE 13
Questions to address when applying the quality improvement model for AMS interventions
What are you trying S e t a g o a l f o r c h a n g e i n a n t i b i o t i c u s e t h a t i s S M A RT ( i . e .

to a c h i e v e ? specif ic, measurable, achievable, relevant and time -bound).
How will you know

that the change D e te r m i n e w h a t q u a n t i t a t i v e m e a s u r e s to u s e to s h o w
is an improvement? improvement (measurements).
What changes can you No t a l l c h a n g e s a r e a n i m p r o v e m e n t .

make that will result I d e n t i f y t h e b e h av i o u r c h a n g e s t h a t w i l l r e s u l t i n
in improvement? i m p r o v e m e n t ( A M S i n te r v e n t i o n s ) .
F I G U R E 14
PERFORMING AMS INTERVENTIONS

The quality-improvement model following the continuous improvement cycle: Plan, Do, Study, Adjust
1. Prepare
2. Plan
5. Adjust 4. Study 3. Do

FIGURE 15
The quality-improvement model in more detail
– M ap poss i bl e en ab l ers (ch a m pio n s) a n d ba r r ie rs i n t h e u n i t .

1 – Obtai n m an agers’ an d ch a m pio n s’ co m m i t m e nt to ch a n ge.
Prepare
– P repare to tal k about A M R , t h e u n i t’s a nt i bio t ic use a n d “ wh at ca n be d o n e” ( A MS) .
– P res ent t h e A M R p rob l em , ch a l l e n ges i n a nt i bio t ic use a n d d i s c uss “ wh at we ca n do”.

2
– Set SM A RT goal s fo r ch an g i n g t h e u n i t’s a nt i bio t ic us e.
Plan
– D ecid e on A M S i nterventio n s , h ow to i m p l e m e nt t h e m a n d h ow to m ea su re ch a n ge.
3 – P
erform A M S i ntervent io n s ( e. g. ed u cat io n , wa rd rou n d s a n d au d i t) a n d
Do m easurem ents (A M S rev iew fo r m : see A n n ex I V) .
– A n alys e t h e m easures (p ro cess a n d ou tco m e) . W h at d o t h ey s h ow ?

4 – Evaluate A M S i ntervent io n s a n d t h e i r i m p l e m e ntat io n . To be co nt i nu ed o r ch a n ged?
Study – P repare to d i s cuss t h e resu l ts , A MS i nte r ve nt io n s a n d i m p l e m e ntat io n w i t h t h e u nits.
– Rev iew res ource us e an d costs , a n d d ete r m i n e wh et h e r t h e re h ave bee n sav i n gs .
– D i s cuss t h e resul ts an d AMS i nte r ve nt io n s w i t h t h e u n i t .

5 – A gree on any adjustments to the AMS interventions, implementation and measurements.
Adjust
– Fol l ow up wi t h a cont i nuous i m p rove m e nt c ycl e ( Pl a n , Do, S tu dy, Ad j ust) .

5.5. Basic AMS interventions
AMS interventions can be performed in all types of health- The AMS review form in Annex IV can be used/adapted to
care facilities. The interventions should align with local collect data needed to measure change in the areas listed
needs and address areas where observations or data sug- in Box 8 for improvement involving reviews.
gest the need for improvement, and/or where the out-
comes of the implemented interventions are measurable.
In facilities where many core elements are not yet in place,

the simple interventions shown in Box 8 may be a place to
start to improve antibiotic prescribing. These interventions
can be implemented one at a time or in a bundle.
B OX 8
Basic AMS interventions
1. Educate prescribers and health personnel involved in antibiotic use (see Chapter 7).
2. Develop and update a standardized medical record and medical chart to ensure that information on patients’ medicines
is all in one place (see Annex VI).
3. Review whether patients who receive antibiotic treatment have written indications.
4. Review antibiotic treatment for patients prescribed three or more broad-spectrum antibiotics.
5. Review the dose of antibiotics prescribed.
6. Review surgical antibiotic prophylaxis where it is prescribed for >24 hours and where a single dose is appropriate.
7. Develop local guidelines for surgical prophylaxis and treatment of common clinical conditions such as community-
acquired pneumonia, UTIs, skin and soft tissue infection (SSTIs), as well as common health-care-associated infections
such as pneumonia, UTIs and catheter-related infections.
8. Work to ensure leadership and identify expertise in infection management.
9. Improve the supply and management of medicines, including essential antibiotics, e.g. by establishing a drug and
therapeutics committee.
10. Work to establish basic microbiology laboratory facilities.
11. Work to establish regular surveillance activities (e.g. AMR, AMC, health-care-associated infections).

5.6 Moving beyond basic AMS interventions
To fully benefit from an AMS programme, facilities should ment more AMS interventions aimed at improving anti-
aspire to put core elements for health-care facilities in biotic prescribing61 related to treatment – diagnosis, and
place, including to secure supplies of essential antibiotics, prescribe, review and stop treatment (Figure 16) – and to
provide treatment guidelines and establish a multidiscipli- surgical prophylaxis – indication, and prescribe and stop
nary AMS team. An option for smaller health-care facil- prophylaxis (Figure 17). This in turn will improve not only
ities may be to collaborate with other health-care facili- antibiotic prescribing, but also dispensing and use.
ties on certain areas, i.e. developing guidelines, expertise,

61
Tamma PD, Miller MA, Cosgrove SE. Rethinking how antibiotics are
microbiology laboratory services, etc. This will facilitate prescribed: incorporating the 4 moments of antibiotic decision making Into
the necessary structures, expertise and skills to imple- clinical practice. JAMA. 2019;321(2):139–40.
FIGURE 16
APPROPRIATE ANTIBIOTIC PRESCRIBING

Appropriate antibiotic treatment – indication and prescribe, review and stop treatment
Antibiotic
treatment
APPROPRIATE ANTIBIOTIC PRESCRIBING

Antibiotic
treatment
Indication Prescribe Review Stop
Bacterial infection? Probable pathogen? Right indication? Treatment duration?

Viral infection? Empirical treatment? Right antibiotic(s)? ...
Colonization? Severe disease? IV-to-oral switch?
Inﬂammation? Comorbidities? Microbiology results?
Indication Prescribe Review Stop
Microbiology testing? Allergy? ...
... ...
Bacterial infection? Probable pathogen? Right indication? Treatment duration?
Viral infection?
Antibiotic surgical Empirical treatment? Right antibiotic(s)? ...
F I GColonization?
U R E 17
prophylaxis Severe disease? IV-to-oral switch?
Inﬂammation? Comorbidities? Microbiology results?
Microbiology testing? Allergy? ...
Appropriate ... antibiotic surgical prophylaxis
... – indication, and prescribe and stop prophylaxis
Antibiotic surgical
prophylaxis
Indication Prescribe Stop
What surgical Right antibiotic(s)? > 24hrs after surgery?

procedure? Right time? ...
... Right duration?
Risk factors?
Indication Prescribe Stop
...
What surgical Right antibiotic(s)? > 24hrs after surgery?

procedure? Right time? ...
... Right duration?
Risk factors?
...
* Antibiotic prophylaxis should not be prescribed for more than 24 hours after surgery. Beyond that, evidence is lacking to show reduced rates of
complications, including surgical site infections.

5.7. More detailed AMS interventions to im- ity, department and ward can try different ways to target
prove antibiotic prescribing change, and tailor the AMS interventions to their own set-
ting.
Different types of AMS interventions (Table 7) included in
facility AMS programmes to improve antibiotic prescribing Table 8 identifies AMS interventions to improve antibiotic
have proven successful.10 To bring about change in antibi- prescribing practices. The ease or difficulty of implemen-
otic prescribing, a bundle62 of AMS interventions is often tation will depend on the availability of local resources and
implemented. These may include (Table 8) educational competencies. Facilities need to prioritize interventions
outreach63 (formal or informal), and/or audit and feedback based on resources available, and to ensure that local or
activities (real-time, either written or oral, or retrospec- regional networking and sharing of resources, including
tive),64 and/or restrictive interventions, such as pre-au- e-learning resources,65 are considered to support their im-
thorization of targeted antibiotics. Restrictive interven- plementation.
tions have been shown to provide quick positive results in
reducing antibiotic use. However, after around 6 months,
restrictive and persuasive interventions are equally effec- 62

Pulcini C, Defres S, Aggarwal I, Nathwani D, Davey P. Design of a “day
tive. Finally, structural interventions – which often refer to 3 bundle” to improve the reassessment of inpatient empirical antibiotic
IT interventions – have also proven to promote more ap- prescriptions. J Antimicrob Chemother. 2008;61:1384–8.
63

Gyssens IC. Role of education in antimicrobial stewardship. Med Clin North
propriate antibiotic prescribing. Am. 2018;102:855–71.
64

Barlam TF, Cosgrove SE, Abbo LM, MacDougall C, Schuetz AN, Septimus
EJ et al. Implementing an antibiotic stewardship program: guidelines by the
It may be useful to change things up over time, either to IDSA/SHEA. Clin Infect Dis. 2016;62:e51–77.
switch the target for change and/or what interventions are 65

Nathwani D, editor. Antimicrobial stewardship: from principles to practice.
British Society for Antimicrobial Chemotherapy; 2018 (http://www.bsac.
performed, and/or how they are performed. This is where org.uk/antimicrobialstewardshipebook/BSAC-AntimicrobialStewardship-
local context and local expertise come in play. Each facil- FromPrinciplestoPractice-eBook.pdf, accessed 3 September 2019).
TA B L E 7
Types of AMS interventions for improving antibiotic prescribing practices
INTERVENTION WHAT IT IS
Persuasive • E ducational meetings (e.g. basics on antibiotic use, case-based discussions, morbidity and mortality,
(education) significant event analysis, lectures on specified topics)
• Distribution of and training on educational material (e.g. clinical practice guidelines)
• Using local key opinion leaders (champions) to advocate for key messages
• Reminders provided verbally, on paper or electronically
• AMS e-learning resources made available to all health-care personnel
• AMS education as part of continuing medical education
Persuasive • udit with feedback to prescribers on their prescribing practice

A
(feedback) • AMS as a component of ward rounds (real-time feedback with educational component)
• Patient handover meetings between two shifts with real-time feedback by consultants
• Local consensus processes for changes in antibiotic treatment or surgical prophylaxis
Restrictive • ormulary restrictions

F
• Restricted prescribing of identified antibiotics (expert approval prior to prescription) (see Annex V)
• Compulsory order forms for targeted antibiotics
• Automatic stop orders (e.g. after a single dose of surgical prophylaxis)
• Selective susceptibility reporting from the lab
Structural • R apid laboratory testing made available

• Therapeutic drug monitoring

TA B L E 8
Comprehensive list of AMS interventions for improving antibiotic prescribing practices
INTERVENTION HOW TO DO IT ADVANTAGES DISADVANTAGES
INTERVENTION
EDUCATION66 Basic and continuous education Can be performed by well-informed Few AMS team members a
Formal or informal of clinical staff, clinical case HCWs in informal settings (i.e. ward barrier for formal training
teaching and training discussions, classes and regular rounds). of HCWs.
to engage prescribers sharing of information, reminders Necessary for better adoption of
and other HCWs in and AMS e-learning resources. most AMS interventions.
improving antibiotic Results in improved prescribing
prescribing, dispensing behaviours when combined with
and administration other AMS interventions (bundle).
practices.
TREATMENT WHO manual for developing Empirical antibiotic prescribing Requires broad
GUIDELINES antibiotic policy guidance.67,68 guidelines and standard treatment dissemination through
Facility treatment guidelines lead to improved, multiple formats and
recommendations for standardized care for common channels to ensure uptake.
common infection infectious diseases, help prescribers
syndromes based on select initial therapy, improve
national or facility antibiotic use, and decrease cost and
clinical guidelines, and length of stay.
on local susceptibility
data, if available.
SURGICAL Adapt surgical prophylaxis guidelines Ensure timely administration and Require coordination and
PROPHYLAXIS to local needs, providing antibiotic stop of appropriate antibiotic(s). collaboration of many
GUIDELINES choice, dose and duration. Significantly reduce surgical site disciplines in the facility.
Facility Disseminate well: poster in the infections.
recommendations operating theatre, leaflet, apps, Easier to implement than other
for common surgical electronic platform. guidelines due to few controversies
procedures. Automatic stop orders might be around the recommendations.
incorporated (see below). Need to be disseminated to surgeons
and/or anaesthetists, and supervised
by pharmacists.
Low-hanging fruit: once the
process is optimized, only periodic
monitoring and feedback are
required.
66

Nathwani D, editor. Antimicrobial stewardship: from principles to practice. British Society for Antimicrobial Chemotherapy; 2018 (http://www.bsac.org.uk/
antimicrobialstewardshipebook/BSAC-AntimicrobialStewardship-FromPrinciplestoPractice-eBook.pdf, accessed 3 September 2019).
67

Pulcini C, Gyssens IC. How to educate prescribers in antimicrobial stewardship practices. Virulence. 2013;4:192–202.
68

Step-by-step approach for development and implementation of hospital antibiotic policy and standard treatment guidelines. Geneva: World Health Organization;
2011 (http://apps.who.int/medicinedocs/documents/s19184en/s19184en.pdf, accessed 4 February 2019).

FEEDBACK INTERVENTIONS
AUDIT WITH See Annex IV: AMS review form Essential to prescribers’ education; Time-consuming.
FEEDBACK69 and Chapter 5 for details on how to provides specific feedback on what Can be perceived as
Refers to the perform audits, with feedback and antibiotics they prescribe and how intrusive; if so, ensure data
assessment of examples. they prescribe them. is only used confidentially
prescribed antibiotic Identifies antibiotic prescribing for improvement in the
treatment, with challenges in the unit, and shows unit.
feedback on antibiotic the impact of AMS interventions on
treatment considered antibiotic prescribing and use (e.g.
as inappropriate. de-escalation, duration).
Prospective (preferred) Data may include information on
or retrospective indication for treatment, prescribed
assessment of antibiotic antibiotic(s), dosage, interval,
therapy in in-patients, administration route, timing of
performed by trained administration of first dose and
HCWs or AMS team duration if collected after stop of
members. treatment.
Can be performed from very basic
(only indication and antibiotics
prescribed per patient) to more
advanced.
WARDS ROUNDS70,71 Assess appropriateness of prescribed Provide real-time feedback on Ward rounds are often
Real-time assessment antibiotics for all inpatients or a inpatient antibiotic treatment and performed by AMS teams.
of antibiotics to be group of patients (ICU, surgery, etc.), training of prescribers. Frequency of ward rounds
prescribed, or which and provide real-time feedback. Can be performed by clinical experts depends on human
are already prescribed, AMS members do ward rounds who are not AMS team members resources and burden of
with instant feedback to preferably with clinical staff, (e.g. on handover meetings between antibiotic use.
prescriber. providing oral or written feedback. shifts).
Issues to consider are redundant
therapy, antibiotics prescribed
(compliance with guidelines or
microbiology test results), dose
optimization, IV-to-oral switch and
duration (see below) (see also Annex
IV: AMS review form).
ANTIBIOTIC SELF- Involves prescribers performing Directly involves prescribers in Opposition from
REVISION BY a post-prescription review of charge of patients in reviewing prescribers and lack
PRESCRIBERS antibiotics, combined with audit and prescribed antibiotic treatment. of facility policy for
Scheduled re- feedback. Facilitates prescriber education and implementing it.
assessment of need A checklist may improve compliance maintains prescriber autonomy. May not happen if
for and choice of (see Annex IV: AMS review form). Less resource-intensive than audit prescribers are not
antibiotics.62 Consider indication for treatment, and feedback. prompted or comfortable
redundant therapy, antibiotics with making changes.
prescribed (compliance with May not lead to improved
guidelines or microbiology test appropriateness if
results), dose optimization, IV-to-oral prescribers lack expertise
switch, duration (see below). in infection management.
69
Akpan MR, Ahmad R, Shebl NA, Ashiru-Oredope D. A review of quality measures for assessing the impact of antimicrobial stewardship programs in hospitals.
Antibiotics (Basel). 2016;5:5.
70
Li DX, Cosgrove SE. Efficacy and implementation of strategies to address antimicrobial overuse and resistance. In: Pulcini C, Ergönül Ö, Can F, Beović B, editors.
Antimicrobial stewardship. Amsterdam: Elsevier; 2017:13–28.
71
Chung GW. Antimicrobial stewardship: a review of prospective audit and feedback systems and an objective evaluation of outcomes. Virulence. 2013;4:151–7.

REDUNDANT A quick review of a patients’ A relatively easy target for AMS Need for trained staff
THERAPY antibiotic therapy may reveal interventions. who can review antibiotic
Review of antibiotic undesirable antibiotic combinations: Cost savings on antibiotics, and therapy and provide expert
therapy, revealing duplication of treatment, potentially reduces AMR. advice.
unnecessary or overlapping bacterial spectra (e.g. Reduces adverse events (e.g.
undesirable therapy. metronidazole and clindamycin) or nephrotoxicity, gastrointestinal side
interactions with other medicines. effects).
REVIEW OF
PRESCRIBED
ANTIBIOTICS
1. DE-ESCALATION 1. Self-revision by prescriber Can reduce costs for broad-spectrum 1–2. May not occur
by prescribers. irrespective of time and availability of antibiotics, and potentially reduces if prescribers are not
microbiology test results. AMR and further facility and patient prompted or are not
costs. comfortable making
2. DE-ESCALATION 2. Self-revision by prescribers
changes.
according to guidelines. or review on ward rounds on
whether empirical treatment
is according to guidelines
(diagnosis, drug, dose, interval,
administration route, duration)
and patient characteristics.
3. DE-ESCALATION 3. When microbiological 3. Requires that
according to results become available, microbiology sampling
microbiology test antibiotic treatment should be done correctly, as
results +/– 48 hours be streamlined accordingly: well as quality-assured
after prescription. choose the most active microbiology testing,
timely release of results
antibiotic(s) with least toxicity,
and good communication
narrowest spectrum and lowest
with trained prescribers.
cost.72
De-escalation is safe for
sepsis and septic shock, and
is associated with decreased
mortality.73
DOSE OPTIMIZATION Optimize dose based on age, weight, Improves patient outcomes, Requires patient-specific
Review of antibiotic organ dysfunction (kidney) and tissue and reduces suboptimal drug data to perform the
doses based on penetration. concentrations and adverse events assessment, e.g. weight,
infection, patient Consider therapeutic drug (mainly nephrotoxicity). renal function, indication
characteristics, monitoring, if available, especially and recommendations for
antibiotic(s) and for nephrotoxic antibiotics dosing in special patient
guidelines. (aminoglycosides). populations (e.g. obesity,
Evaluate the need for loading dose renal dysfunction), which
and/or prolonged/continuous are not always available.
infusions. May also require
Integrate into pharmacists’ review microbiology laboratory
during ward rounds or other audit results (minimum inhibitory
processes. concentration) for correct
dose.
72
Levy Hara G, Kanj SS, Pagani L, Abbo L, Endimiani A, Wertheim HF et al. Ten key points for the appropriate use of antibiotics in hospitalized patients: a consensus
from the AMS and Resistance Working Groups of the International Society of Chemotherapy. Int J Antimicrob Agents. 2016;48:239–46.
73
Garnacho-Montero J, Gutiérrez-Pizarraya A, Escoresca-Ortega A, Corcia-Palomo Y, Fernández-Delgado E, Herrera-Melero I et al. De-escalation of empirical
therapy is associated with lower mortality in patients with severe sepsis and septic shock. Intensive Care Med. 2014;40:32–40.

IV-TO-ORAL SWITCH Consider based on: Reduces unnecessary days of IV lines May meet opposition from
Promotes the use of • clinical condition and availability of and common complications. prescriber (and patient).
oral antibiotics instead adequate oral antibiotic; Reduces length of stay, as patients
of IV when clinically • oral intake and gastrointestinal can complete antibiotic treatment at
indicated. absorption (not impaired); home.
• adequacy of oral intake in terms
of diagnosis (e.g. not in the case of
endocarditis or meningitis).74
DURATION Can be performed: Addresses a common area for May need to be

Review (real-time or • by prescribers during self-revision; improvement with regard to antibiotic individualized in e.g.
retrospective) of stop • the entire AMS team during ward prescribing. immune-compromised
dates for antibiotic rounds; Improves patient outcomes, and patients or patients with
treatment in patients. • pharmacists collecting prevents selection of MDR bacteria central nervous system or
prescriptions in every unit; and adverse events (i.e. Clostridium bone infection.
• retrospectively. difficile infection and nephrotoxicity).
RESTRICTIVE INTERVENTIONS (LIMITATIONS TO PRESCRIBING TARGETED ANTIBIOTICS)
RESTRICTION Restrictions on antibiotics are by Controlling targeted antibiotics May delay initiation of
Restricted dispensing diagnosis or unit. defined by the AMS team or hospital treatment.
of targeted antibiotics Selection of restricted antibiotics is formulary. Opposition from
on the hospital’s done by facility authorities, the AMS Shown to be highly effective, prescribers due to lack of
formulary, according team and heads of units based on especially in the early stages of an autonomy.
to approved criteria spectrum, cost or toxicities. AMS programme, in an outbreak Risk of misusing other
(e.g. use the AWaRe Antibiotics are restricted before situation or as part of a response to antibiotics that do not
categories). use; ensures expert approval before an increase in or current high use of require authorization.64
initiation. certain antibiotics in the facility.10 Labour-intensive and
Use of restricted Practical approach that allows Has been shown to reduce medicine time-consuming because it
antibiotics may be attending physician to use the drug costs for hospitals over time. requires enforcement to be
limited to certain pending approval by physician or effective.
indications, prescribers, AMS team after +/− 48 hours.
services, patient See Annex V for an example of a pre-
populations or a authorization form.
combination of these.
Selective susceptibility Report susceptible first-line narrow- May reduce use of broad-spectrum Opposition from
reporting. spectrum antibiotics to regular antibiotics. prescribers, lack of
wards. guidelines, poor system
support, insufficient
resources.
AUTOMATIC STOP Automatic stop orders are mostly A simple measure, considering IT is needed, which is often
ORDERS used for a single dose of surgical the high burden of antibiotics missing.
Stop dates antibiotic prophylaxis, or prescribing unnecessarily used for surgical Unintended treatment
automatically applied some antibiotics. prophylaxis. interruptions if not
to an antibiotic order Useful in small facilities and with properly supervised by the
when the duration is limited pharmacy staff. AMS team.
not specified to ensure Use only in a context with good
that antibiotics are control mechanisms to avoid unsafe
continued no longer treatment interruptions.27 Nurses can
than necessary. play a role in alerting the attending
physician.
van den Bosch CM, Geerlings SE, Natsch S, Prins JM, Hulscher ME. Quality indicators to measure appropriate antibiotic use in hospitalized adults. Clin Infect Dis.
74
2015;60:281–91.

RESTRICTIVE INTERVENTIONS (LIMITATIONS TO PRESCRIBING TARGETED ANTIBIOTICS)
RAPID LABORATORY Rapid diagnostic tests allow for more Provides quicker diagnostic results Tests are often expensive
TESTING accurate diagnosis and targeted than traditional microbiology testing and/or require advanced,
Stop dates antibiotic treatment. expensive equipment that
automatically applied is not available in many
to an antibiotic order facilities.
when the duration is
not specified to ensure
that antibiotics are
continued no longer
than necessary.
THERAPEUTIC DRUG There should be a standardized Fewer adverse events related to Therapeutic drug
MONITORING procedure for collecting blood specific antibiotic treatments. monitoring is not available
To be performed samples. in many health-care
for concentration- The concentration of the antibiotic facilities.
dependent antibiotics is measured in blood to allow for
when used >3 days. optimal adjustment of daily dose.
COMPUTERIZED Allows users to place electronic Orders made and the online medical Requires health-care IT
PHYSICIAN ORDER orders, and the facility to maintain an records, incl. medical charts, can systems which are not
ENTRY (CPOE) online medical record. be read and reviewed by HCWs available in many health-
Replaces a facility’s attending to a patient. care facilities.
paper-based ordering
system with an
electronic one.
ANTIBIOTIC ALLERGY Establish guidance for antibiotic Promote the use of old narrow- Equipment and/or
ASSESSMENTS75 allergy assessment, e.g. a penicillin spectrum antibiotics, which are also expertise to perform
Replaces a facility’s allergy assessment protocol, with potentially more effective. allergy testing may not be
paper-based ordering recommendations on which patients available in the facility.
system with an might benefit from skin testing.
electronic one.
Blumenthal KG, Peter JG, Trubiano JA, Phillips EJ. Antibiotic allergy. Lancet. 2019;393:183–198.
75

5.8. Audit with feedback How to choose which infections to audit?
• Common infections, such as community-acquired pneu-
5.8.1 Prospective (real-time) audit with feedback monia (CAP), UTIs, and SSTIs.
Prospective audit with feedback (e.g. on ward rounds) in-
volves the assessment of antibiotic therapy by trained indi- • W
hen a problem is detected, a specific intervention
viduals (usually physicians and/or pharmacists), who make might be designed. For example, an increase in infec-
recommendations to prescribers in real time when therapy tions after surgery or in urine cultures referred to the
is considered suboptimal. microbiology lab, which might indicate that patients with
asymptomatic bacteriuria are wrongly being treated for
A prospective audit should be prioritized over a retrospec- UTIs.
tive audit. It may be performed alongside clinical per-
sonnel on ward rounds, providing oral recommendations • Infections treated for a long duration (e.g. >7 days).
for changes in antibiotic treatment in real time. Alterna-
tively, the physician and/or pharmacist in the AMS team Example #1:
may perform ward rounds on their own, providing writ- The AMS team pharmacist notes that during the past
ten recommendations for changes in antibiotic treatment. week, three patients admitted to the internal medicine
See Annex IV for an AMS review (audit) form and Chapter unit with non-severe CAP received a combination of cef-
5.8.4 for an example of patient audit data. triaxone and clarithromycin. Clinical guidelines at your
hospital recommend ampicillin alone for most non-se-
5.8.2 Retrospective audit with feedback vere CAPs.
Retrospective audit with feedback is a method of collecting
antibiotic data to evaluate the impact of AMS interventions What can be done?
(baseline and follow-up data) on antibiotic use, but is in-
ferior to a prospective audit and real-time feedback. An 1. List all patients admitted with non-severe CAP
audit involves assessing antibiotic therapy in hospitalized to the internal medicine unit during the last 2–3
patients, and is often coordinated by a physician or ad- months.
ministrator but performed by pharmacists and/or nurses.
Antibiotic audit data are collected as follows: 2. If samples (i.e. sputum, blood cultures) have
been submitted, review medical records for severity
• a t baseline to identify areas for improvement of antibi- (e.g. CRB-65) as well as microbiology test results.
otic prescribing for the whole hospital, a department or Also note down recorded reasons for prescribing
ward; ceftriaxone/clarithromycin and whether a review
(de-escalation) of treatment has been carried out.
• for a defined period of time to evaluate any improve-
ments; and 3. Hold a meeting with a smaller group of pre-
scribers on the ward to discuss your initial findings.
• to provide regular and structured feedback both on the Discuss further steps and possible actions (training
quality and quantity of antibiotic prescribing and use to of health personnel, ward rounds, audit, etc.).
prescribers.
4. Hold a further meeting with the heads of the unit
Audit with feedback provides an opportunity for clinical and all the medical staff (including residents and
staff to discuss their own prescribing practices, to identify fellows) to discuss why broad-spectrum antibiotics
priority areas for change and to set specific goals for them- and frequent combinations should be avoided for
selves at the facility, department and/or ward level. CAP. Agree on further action, such as targets for
changes to prescribing, training and other AMS
5.8.3 Selecting one or more infections for audit interventions.
To what degree are infections treated according to guide-
lines? 5. Continue active surveillance through audit for a
The audit should provide figures on compliance with the specified time period and meet again with the unit
guidelines and suggest where there is room for improve- to discuss progress.
ment. Data are collected on ward rounds or directly from
patients’ medical charts. A sample medical record form
can be found in Annex VI.

Example #2: 7. Once these first analyses are done, discuss the
During ward rounds or in specific patient consultations, a results with the medical staff on the ward, suggest-
member of the AMS team has the impression that many ing targets for change and which data to collect for
patients with urinary catheters are being treated with an- a specified time period. Agree on further interven-
tibiotics. tions (i.e. any necessary training and follow-up) and
on when to meet again to discuss the results of the
What can be done? new audit.
1. Together with ward staff, list all patients with 5.8.4 Selecting antibiotic(s) for audit
a urinary catheter. Draw up a chart (table) that To what degree is an antibiotic used according to guide-
includes the main variables to be evaluated (see the lines?
following points). The audit should provide figures on who is receiving antibi-
otic(s), indications for treatment and whether the patient is
2. Review every patient history looking for signs of receiving the right antibiotic treatment (see the audit sam-
UTI, including fever or sepsis without another focus ple below).
of infection.
How to choose which antibiotics to audit?
3. Determine which patients (with or without clini-
cal signs of infection) have had urine samples taken • A
ntibiotics where consumption has increased significant-
for culture, to find out whether patients without ly over time.
clinical signs of UTI have had urine cultures taken as
well as whether no urine or blood culture has been • A
ntibiotics with a higher potential of inducing and prop-
taken when a true infection is suspected. agating resistance (e.g. WATCH and RESERVE antibiot-
ics).
4. Review any prescription of antibiotics for
patients with a urinary catheter, whether asymp- • B
road-spectrum antibiotics (e.g. piperacillin/tazobac-
tomatic or symptomatic. Again, this will detect the tam, ticarcillin/clavulanate, carbapenems).
prevalence of prescriptions in both circumstances.
• Last-resort antibiotics (e.g. polymyxins, linezolid).
5. For patients with clinical signs of UTI, assess
whether the treatment is appropriate according to • Expensive antibiotics.
local epidemiology and/or guidelines (selection of
antibiotic(s), dose, de-escalation and duration). Note: Keep in mind that restricting one antibiotic may in-
crease the use of others
6. Depending on sample size, extend the assess-
ment retrospectively (e.g. 1 month) by searching Depending on the strategy adopted in the facility, audit
patient medical records. might be done via ward rounds, pharmacy alerts, a process
of pre- or post-authorization, self-revision by physicians or
a combination of all of these.
Department/ward: Year:
Week Pat. ID Age Gender Indication Medicine(s) Dose Adm. Adm. Guideline Comments:
(M/F) interval route compliance allergy, etc.
15 01 55 M Cellulitis Ceftriaxone 1g x1 IV No No allergy
“ 02 18 M Meningitis Ceftriaxone 2g x2 IV Yes
“ 02 42 F Gastro- Ceftriaxone 1g x1 IV No No fever or
enteritis bloody stool
“ 02 25 F UTI Ceftriaxone 1g x1 IV Yes
“ 03 36 M CAP Ceftriaxone 1g x1 IV No CRB65 = 1

Example #1: Example #2:
The pharmacist who picks up medication request forms As part of the stewardship strategy, the AMS team de-
in the ICU has noted that for some time now, there has cides to assess what is happening with antibiotic surgical
been an increase in the use of meropenem in higher doses prophylaxis. Your hospital has not yet updated clinical
and of colistin. practice guidelines for this indication, but national guide-
lines are in place.
What can be done?
What can be done?
1. Hold a meeting with the head of the ICU to con-
vey your concern and suggest a meeting to gather 1. Review the list of all surgical procedures done
most of the ICU staff, including physicians who only or performed over at least the last 2 weeks (de-
are on call in the ICU. pending the number of surgical procedures per-
formed by different specialties).
2. Discuss with prescribers their perception of
this increase (e.g. more severe septic patients, an 2. Produce a form (e.g. Excel or electronic plat-
increase in MDR gram-negative pathogens). form) that includes essential issues for evaluation:
indication (type of surgery), gender and age of the
3. Review and discuss the patients receiving treat- patients, main comorbidities, antibiotic(s) pre-
ment with one or both antibiotics studied. scribed as prophylaxis, dose, time of administration
and duration.
4. Perform a retrospective audit of patients who
were treated with one or both antibiotics. 3. Review the appropriateness of the prophy-
laxis: the antibiotic(s) prescribed, dose, timing and
5. Analyse with the AMS team the appropriateness duration.
of the prescriptions: indication, dose, duration, mi-
crobiology test results and the existence (or not) of 4. Hold a meeting with the surgical services and
alternative treatments with regard to both ecology anaesthesia for feedback on the findings. The meet-
and cost. ing might be general (the whole surgical depart-
ment) or by specialty depending on the results and
8. Once this analysis is done, meet again with the the size of the department.
ICU medical team to discuss the results. Try to
reach agreement regarding what changes are feasi- 5. Adapt national or international guidelines to
ble, what training and other interventions might be your facility situation (epidemiology and drug availa-
useful, and how to measure change through active bility), and involve every specialty in developing the
surveillance (audit) for a specified time period. guidelines to increase ownership.
9. Meet once again to discuss the results of the new 6. Repeat the audit after a specified time (e.g.
audit. 4–6 months) after implementing new guidelines for
surgical antibiotic prophylaxis in the facility.

5.9 Role of IT in an AMS programme
Even a successful AMS programme needs to be adequately analysed without technology. Point prevalence surveys are
measured to be efficient. The use of proper and updated an example of this. Table 9 identifies areas where IT can be
information is essential. Often data can be collected and of additional benefit.
TA B L E 9
Areas where IT can benefit AMS interventions
BASIC LEVEL INTERMEDIATE LEVEL ADVANCED LEVEL
Database on procurement and ward Calculation of antimicrobial consumption CPOE system

dispensing at the facility pharmacy level (e.g. in DDD/1000 inpatients/day) Estimations of clinical outcomes related to
Database of AMR surveillance in different Alerts on specific antibiotic use antibiotic treatment
units Time-sensitive automatic stop orders for Apps for national, regional or facility
surgical prophylaxis guidelines
Electronic guidelines (via electronic Point-of-care access to microbiological
mailings to prescribers, intranet) results from all units
Apps for doing a PPS Clinical decision-support systems
(commercial or self-developed) of different
levels of complexity
Computerized patient dispensing billing
data
Automatic submissions/reporting of
computerized facility-level data to the
national centre

6. ASSESSING AMS PROGRAMMES
6.1 Introduction 6.2 Structural measures/indicators
Data play an important role in assessing AMS interven- Structural measures are used to assess the capacity, sys-
tions (to identify problems or evaluate the benefits of AMS tems and processes in a facility or an organization. The
interventions), although qualitative improvement can be national and health-care facility core elements present
achieved even in the absence of data (Chapter 5.5). How- essential structures for implementing national and health-
ever, from a mid- to long-term perspective, efficiently pri- care facility level AMS programmes.
oritizing interventions and allocating resources for AMS
requires data to identify key challenges in antibiotic use
and to demonstrate the impact of targeted interventions.
Indicators of antibiotic use are thus an essential part of any 6.3 Process measures/indicators
AMS strategy.64
The implementation of AMS interventions aims to optimize
This chapter aims to advise on metrics (Figure 18) for antibiotic prescribing and use. It is therefore recommend-
assessing the impact of AMS interventions. Because as- ed to also include process indicators as a proxy measure
sessing all indicators is unrealistic,76,77 the collection of infor improvement (Table 12). Process measures may specify
dicators shown in Tables 10–12 is not intended to be com- how patient medical charts are reviewed (e.g. how many
prehensive. AMS programmes are encouraged to select times a week over a given period of time) and how anti-
the most relevant and feasible metrics for a particular local biotic prescribing and use is improving. Apply the process
setting. Note also that the resources required for assessing indicator that corresponds to the AMS intervention(s) im-
the indicators will vary, depending on the setting and the plemented. For an example, see Chapter 6.5.
available infrastructure. Nonetheless, given the complexity
of antibiotic use, a single indicator will probably not suffice.
How to assess structural indicators of AMS programmes 76
Kallen MC, Prins JM. A systematic review of quality indicators for
(e.g. leadership commitment, human resources and guide- appropriate antibiotic use in hospitalized adult patients. Infect Dis Rep.
lines) is covered in Chapters 2 and 3. Finally, in as much 2017;9:6821.
77
Stanic Benić M, Milanič R, Monnier AA, Gyssens IC, Adriaenssens N,
as local indicators will vary, this toolkit does not specify Versporten A et al. Metrics for quantifying antibiotic use in the hospital
targets or methods, which are available in reviews.78 setting: results from a systematic review and international multidisciplinary
consensus procedure. J Antimicrob Chemother. 2018;73:vi50–vi58. .
78
De Kraker MEA, Abbas M, Huttner B, Harbarth S. Good epidemiological
practice: a narrative review of appropriate scientific methods to evaluate
the impact of antimicrobial stewardship interventions. Clin Microbiol Infect.
2017;23:819–25.
79
Donabedian A. Quality of care. JAMA 1988;12:1743–8.
ASSESSING AMS
F I G U R E 17
INTERVENTIONS
Structural, process and outcome measures for assessing AMS programmes 79
Structure measures Process measures Outcome measures

6.4 Outcome measures/indicators 6.5 How to begin assessing AMS programmes
The aim of an AMS programme is often achieved by re- Below is an example of a stepwise approach for applying
ducing overall AMC and perhaps reducing overall use of different indicators when assessing an AMS programme.
specific (broad-spectrum) antibiotics. However, it is equal-
ly important to document that this reduction is not asso- Structural measures/indicators:
ciated with unintended negative patient outcomes. Fur- The national and health-care facility core elements can be
thermore, AMS aims not only to prevent negative patient used as checklists for assessing the structures of national
outcomes, but also to improve patient outcomes, providing and health-care facility AMS programmes.
further arguments for assessing outcome measures.
Initial outcome measures/indicators:
In health-care settings without established surveillance An essential part of any AMS programme, both national
programmes for AMR and health-care associated infec- and facility, is to study antibiotic prescribing and use over
tions, or electronic health records, it may be difficult to time. Either antimicrobial consumption surveillance data,
obtain reliable data about clinical outcome measures (Ta- PPS data or audit data can be applied. The most sustain-
ble 11). Given the sound evidence for the safety and effec- able and least laborious way to measure antibiotic use
tiveness of AMS programmes, it may be justifiable as a first over time is through routine collection of antimicrobial
step to focus on outcome measures related to antimicro- consumption data. The study of the indicators DDD per
bial use (Table 10).10,11,19 100(0) patient-days and/or DDD per admission should be
prioritized. A simple way to initiate further analyses of the
Regardless of whether electronic prescribing is available, consumption data is to look at the proportion of DDDs in
many facilities have pharmacy systems that can provide AWaRe and OTHER groups or any other relevant clinical
information on antimicrobials supplied to wards and oth- categories. It is recommended that antibiotic use should
er clinical areas. These data can be collected manually be expressed in at least two metrics simultaneously.
and used as a proxy for antimicrobials given to patients.
In an AMS programme, when it comes to measuring and Other outcome measures/indicators:
expressing antibiotic use in numerical terms, a standard- Although evidence shows that AMS interventions do not
ized measure is required. The most common standardized lead to increased mortality, study of clinical patient out-
measure is DDDs. Other outcome measures used are de- comes – e.g. mortality and length of stay – is recommend-
scribed in Tables 11 and 12. ed to ensure that implemented interventions do not have
unintended consequences for patients.
The potential cost savings (direct and indirect) as a result
of the shift from more expensive broad-spectrum to less Process measures/indicators:
expensive first-line narrow-spectrum antibiotics should be Process indicators are often used as a proxy measure of
partly used/reinvested in sustaining/maintaining the AMS improvement, e.g. that antibiotic prescribing practices are
programme in the facility. moving in the right direction. For example, if the target
is to improve adherence to recommended empirical treat-
ment of a particular infection, a corresponding process
measure would be the proportion of all patients with this
particular infection who receive recommended empirical
treatment.

TA B L E 1 0
Outcome measures/indicators related to antimicrobial use
INDICATOR POSSIBLE D
INDICATOR CONSTRUCTION ATA SOURCES COMMENT
DDD per 100(0) Numerator: DDD of Pharmacy dispensing DDD per 100(0) patient-days is the most commonly used
patient-days an agent (based on data quantity measure of antibiotic use, because the data
ATC code) purchased/ Health-care facility needed to calculate it are available in many settings (unlike
dispensed/consumed in a purchasing data days of therapy, DOTs); no individual-level data are needed.
period of time (i.e. total Nursing chart It should, however, be noted that differences in data
antibiotic used) administrative data sources and definitions may influence this indicator, for
Denominator: Total (paper) instance:
number of patient-days Electronic drug • the list of antibiotics included (e.g. all ATC class J01
within that period of time administrative data antibiotics, or subsets of ATC class J01, or additional
Multiplier: x 100(0) to E-prescribing records antibiotics and antimicrobials not included in ATC class
obtain data per 100(0) J01);
patient-days • the data source used – it has, for example, been shown
that pharmacy dispensing data tend to overestimate
antibiotic use compared with actual drug administration
data;80 and
• how patient-days are calculated (e.g. “days present”, an
alternative measure).81
Detailed guidance on how to calculate DDDs is available
elsewhere.82
DDDs can be calculated for overall use, specific antibiotic,
classes or other categories (such as AWaRe). It is very
important to clearly define how the metric is calculated (i.e.
antibiotics included, data sources, ATC version and year,
calculation of patient-days) and to be consistent over time.
DDD per Numerator: See above See above DDD per admission gives different information than does
admission Denominator: Total DDD per patient-days.
number of patients The length of stay may affect patient days and admissions
admitted within a period differently.
of time
DOTs per 1000 Numerator: Days of Nursing chart The major disadvantage of DOTs compared with DDDs
patient-days therapy with an agent administrative data is the need for individual-level patient data (instead
during a period of time (paper) of aggregated data, such as pharmacy data, which are
Denominator: Total Electronic drug sufficient to calculate DDDs).
number of patient-days administrative data (On the other hand individual-level data make it possible to
within that period of time E-prescribing records assess the duration of treatment, redundant therapy, etc.).
Multiplier: x 1000 to
obtain data per 1000
patient-days
80

Dalton BR. Assessment of antimicrobial utilization metrics: days of therapy versus defined daily doses and pharmacy dispensing records versus nursing
administration data. Infect Control Hosp Epidemiol. 2015;36:688–94.
81

Moehring RWl. Denominator matters in estimating antimicrobial use: a comparison of days present and patient days. Infect Control Hosp Epidemiol.
2018;39:612–15.
82

DDD indicators. In: Essential medicines and health products: ATC/DDD toolkit. Geneva: World Health Organization; n.d. (http://www.who.int/medicines/
regulation/medicines-safety/toolkit_indicators/en/index1.html, accessed 4 February 2019).

INDICATOR POSSIBLE DATA
INDICATOR CONSTRUCTION SOURCES COMMENT
Proportion of Classify DDDs according Pharmacy dispensing

DDDs in AWaRe to AWaRe and OTHER data
and OTHER groups, and calculate the Hospital drug purchase
groups percentage of each data
Nursing chart
administrative data
(paper)
Electronic drug
administrative data
E-prescribing records
TA B L E 1 1
Outcome measures/ indicators related to patients and microbiology
INDICATOR POSSIBLE
INDICATOR CONSTRUCTION DATA SOURCES COMMENT
Patient outcomes In-hospital mortality: In-hospital mortality: Can be assessed as in-hospital mortality (i.e.
Number of deaths during hospital administrative data death during hospitalization) or mortality at
hospitalization / Total number 30-day mortality: population a specific time point after admission (e.g. 30
of hospitalizations office administrative data days). The latter has better face validity since
Infection-specific it is not influenced by differences in length of
mortality: chart review and stay, but the data needed to calculate it are
administrative data more difficult to obtain in most settings.
Ideally, infection-specific mortality rates (e.g.
for CAP) would also be calculated. Since it
is difficult to assess whether a specific death
was caused by an infection or by AMR, the
assessment of infection-specific mortality can
be tricky (and time-consuming).
The numerator and denominator must be
clearly defined.
Length of stay: Days of Infection-specific chart There are many different ways of defining
hospitalization by type of review and administrative length of stay. It is important to use consistent
infection / Total number of data definitions over time.
patients with that infection
Readmission within 30 days Infection-specific chart Only unscheduled readmissions should be

after discharge: Patients with review and administrative counted (e.g. a planned admission for a
infections readmitted <30 days data surgical intervention should not be counted).
after discharge / Total number
of patients discharged with that
specific infection

INDICATOR POSSIBLE
INDICATOR CONSTRUCTION DATA SOURCES COMMENT
Microbiology Clostridium difficile: Number • Microbiology data C. difficile definitions may vary, and a detailed
outcomes of health-care-associated C. • Epidemiology data discussion is beyond the scope of this
difficile infections in a period of • Infection control document. Interested readers may consult
time / Total number of patient- surveillance data the respective surveillance protocols and
days within that period x • Administrative data guidelines.83,84
100 000 • Chart review A detailed discussion is beyond the scope of
• Microbiology data this document. See also GLASS
MDR organisms (e.g. • Epidemiology data (http://www.who.int/glass/en/).
MRSA, ESBL-E/CPE, • Infection control
MDR Pseudomonas and surveillance data
Acinetobacter spp., • Administrative data
vancomycin-resistant • Chart review
enterococci): Number of health-
care-associated infections in a
period of time / Total number of
patient-days within that period
x 100 000
83
European surveillance of Clostridium difficile infections. Surveillance protocol version 2.3. Stockholm: European Centre for Disease Prevention and Control; 2017
(https://ecdc.europa.eu/sites/portal/files/documents/European-surveillance-clostridium-difficile-v2point3-FINAL_PDF3.pdf, accessed 8 February 2019).
84
McDonald LC, Gerding DN, Johnson S, Bakken JS, Carroll KC, Coffin SE et al. Clinical practice guidelines for Clostridium difficile infection in adults and children:
2017 update by the IDSA and SHEA. Clin Infect Dis. 2018;55:e1–e48 (https://academic.oup.com/cid/advance-article/doi/10.1093/cid/cix1085/4855916, accessed
8 February 2019).
TA B L E 1 2
Process measures/indicators of antimicrobial use
INDICATOR INDICATOR CONSTRUCTION
Documented indication Number of patients with a written indication for antibiotic treatment / Total number of patients
for antibiotic use treated with antibiotic(s)
Stop/review date Number of patients with a written stop/review date for antibiotic treatment / Total number of
patients treated with antibiotic(s)
Compliance with current Number of patients with an indication receiving empirical treatment with antibiotic(s) according
clinical treatment guidelines to clinical guidelines / Total number of patients with this indication
Length of therapy by indication Total number of days of antibiotic treatment for a specific indication / Total number of patients
treated with antibiotic(s) for that indication
48-hour review Number of patients where a 48-hour review is performed / Total number of patients treated
with antibiotic(s) hospitalized >48 hours
De-escalation Number of patients where a de-escalation from the initial therapy is performed / Total number
of indicated empirical treatments
IV-to-oral switch Number of regimens switched to oral route / Total number of regimens that can be switched to
oral route based on predefined criteria
Compliance with current Number of patients receiving surgical antibiotic prophylaxis according to guidelines /
guidelines for surgical Total number of surgical patients receiving antibiotic prophylaxis
prophylaxis (antibiotics)
Surgical prophylaxis within the Surgeries with prophylaxis administered within 60 minutes prior to surgery / Total number of
previous 60 minutes surgeries that require prophylaxis
Surgical prophylaxis stopped Surgeries with prophylaxis stopped within 24 hours after surgery / Total number of surgeries
within 24 hours after surgery that require prophylaxis

7. E D U C AT I O N A N D T R A I N I N G

Key audience: Ministries and/or departments, health-care facilities, institutions and/or
related entities responsible for planning and delivering pre-service and in-service education
and training.
7.1 AMS competencies
Competencies5 are defined as the development of observ- Individuals must objectively assess their current level of
able ability of a person (or individual health worker) that knowledge and skills (basic, competent, advanced) related
integrates knowledge, skills and attitudes in their perfor- to the topics and their ability to apply them in practice.
mance of task. Competencies are durable, trainable and, Table 13 provides a comprehensive set of competencies
through the expression of behaviours, measurable. AMS in five core domains at three different levels. Local pro-
competencies are the guiding set of knowledge, skills and grammes need to decide what level of competency is ex-
attitudes that result in durable, trainable and measurable pected depending on the health-care professional. These
behaviours facilitating better prescribing of antibiotics (Ta- competencies may change or evolve over time depending
ble 13). on the job function/role.85,86,87 Once a realistic assessment
of competencies (knowledge, skills and attitudes) has been
Some of the key concepts to keep in mind when prescrib- established, learning needs (e.g. training curricula88 and
ing antibiotics include the following: learning materials), and how these needs can be met, are
then determined.
• a wareness of the health-care facility’s standard treat-
ment guidelines;
• the importance and rationale for using recommended

empirical antibiotic agents for patients, but also the po-
tential immediate and long-term harm of broad-spec-
trum therapy; 85
WPRO-AMS training package. Geneva: World Health Organization; 2018.
86
WHO global interprofessional AMR competency framework for health
workers education and training. Geneva, World Health Organization; 2018.
• the benefit and safety of de-escalation antibiotic treat- 87
Dyar O, Beović B, Pulcini C, Tacconelli E, Hulscher M, Cookson B et al.
ment after cultures; and ESCMID generic competencies in antimicrobial prescribing and stewardship:
towards a European consensus. Clin Microbiol Infect. 2019;25:13–19.
88
WHO competency framework for health workers’ education and training on
• the opportunity and benefits of IV-to-oral switching. antimicrobial resistance. Geneva: World Health Organization; 2018.

TA B L E 1 3
Competencies for HCWs involved in AMS programmes in health-care facilities in LMICs
LEVEL OF COMPETENCY:
• Basic: The professional is aware of, has knowledge of or understands the core principles of an area.
• Intermediate: The professional is aware of the core principles of an area, understands them and knows how to apply them in his/her
practice.
• Advanced – expert: The professional is aware of the core principles of an area, understands them, knows how to apply them in his/her
practice, can show others how to apply them and provides leadership, expertise or support to others in this area.
TOPIC
1. Introduction to AMR
Global situation of AMR Understand the morbidity, mortality and economic threat of AMR to human health.
and AMS
Drivers of AMR • Use of antibiotics in humans, animals, plants and environment:
• Understand the development and main drivers of AMR.
• Know the importance of optimizing use of antimicrobials in the human and animal sectors to prevent
development of resistance.
• Understand that travel, recent hospitalization or previous microbiology findings of resistant bacteria are
factors that predispose to colonization/infection with a resistant pathogen.
WASH and IPC Advocate for WASH and scaling up vaccines for common infections.
Understand the link between AMS and IPC.
Understand the infection chain: organism, source, route of transmission and susceptible host, and the
importance of practicing hand hygiene to prevent transmission.
Call for action Promote awareness of AMR and appropriate antimicrobial use amongst all HCWs, patients and the general
public to protect the effectiveness of antimicrobials as a public good.
2. Antibiotics
Different antibiotic Understand the clinically relevant spectrum of activity for commonly prescribed antibiotics, and use this
classes knowledge when prescribing.
Understand the mechanisms of actions for commonly prescribed antibiotics.
PK/PD, formulations Understand the basic principles of pharmacokinetics and pharmacodynamics (PK/PD), and use this
and knowledge when prescribing.
patient characteristics Understand the use of antibiotics in special care groups (e.g. paediatrics, pregnancy, breastfeeding, renal
diseases and obese persons).
Prescribing principles Understand the principles of empirical, syndromic or culture-based treatment options in relation to the
Prophylaxis, empirical selection of antibiotics.
therapy, definitive Understand single prophylactic antibiotic dosing for surgical and other procedures for which prophylaxis has
therapy and drivers of been shown to be effective, and use this knowledge when prescribing.
excess antibiotic use Understand that an inflammatory response can be due to both infectious and noninfectious causes (e.g. acute
pancreatitis).
Understand when not to prescribe antibiotics (e.g. for viral infections, or when there is bacterial colonization).
Understand best practices for some infections may not include antibiotic treatment (e.g. incision and drainage
of abscesses, removal of foreign material, most upper respiratory tract infections).
Understand key elements for initiating antibiotic therapy:
• Indication for antibiotic therapy, including assessment of the severity of the infection (sepsis syndrome
recognition) to inform urgency of therapy.
• Bacterial infection, infection site, probable causative bacteria.
• Antibiotic choice, dosage, interval, duration, preparation and administration of antibiotics, review and stop
dates.
• Importance of avoiding unnecessary use of antibiotics.
• Empirical treatment guided by local antibiotic susceptibility patterns.
• Broad- and narrow-spectrum antibiotics and the importance of avoiding unnecessary use, especially of
those with broad-spectrum activity.

2. Antibiotics
Documentation and Understand the need to document important details of the antibiotic treatment plan (e.g. agent, dosing,
communication on administration route, clinical indication, duration and review dates) in the prescription chart, medical records
antibiotic prescription and transfer notes to other health-care institutions.
and use Ensure appropriate documentation of antibiotics dispensed, including route, time, dose, therapeutic drug
monitoring and response for individual patients.
Be able to communicate with patients on the appropriate use of antibiotics, including patient counselling
etiquette, discussion techniques and psychology for patient communication:
• Promote better patient understanding of all treatment issues, such as safety concerns (including alerts) and
adherence.
• Promote a standard for the appropriate use of antibiotics, and manage patient expectations and demands
especially when the use of antibiotics is not indicated.
Allergies, cross- Understand the significance of common antimicrobial and drug/food interactions, and utilize strategies to
reactions, avoid interactions.
adverse effects Understand that optimizing antimicrobial use can limit common side effects and collateral damage related to
treatment (e.g. disruptive effects on host normal flora, which may lead to C. difficile infection, superinfection
with Candida spp.).
Understand common side effects of antimicrobials, including allergy, and use this knowledge when
prescribing:
• Understand allergy types: immediate, non-life-threatening, severe adverse drug reactions (e.g. Stevens-
Johnson syndrome).
• Understand the mechanisms and risks of beta-lactam cross-reactions.
Understand how to monitor common side effects, and use this knowledge when prescribing.
Understand what to do when common side effects of antimicrobial therapy are suspected (e.g. documenting
allergic reactions in patient records, reporting side effects).
EML and the AWaRe Encourage adherence to antimicrobial formulary/protocol restrictions.
classification Discourage use of fixed-dose combinations of different antibiotics that have not been shown to improve
clinical outcome.
Ensure regular and timely supply of appropriate medicines.
Understand that antimicrobials have different resistance potential (AWaRE groups).
Understand the importance of promoting appropriate use of antimicrobials according to their AWaRe groups
to implement specific resistance-prevention actions for these antimicrobials.
3. Microbiology
Important terms Understand the differences between colonization (e.g. isolation of bacteria from a skin wound or urine with
no sign of inflammation or infection) and infection.
Understand the difference in microorganisms and resistance patterns for infections acquired in the
community compared with hospital settings.
Common causative Understand the common and important gram-positive and gram-negative bacteria (WHO priority pathogens
agents list plus C. difficile).
and resistance Understand the nature and classification of microorganisms that commonly cause infections in humans.
mechanisms Recognize common mechanisms of resistance within an institution for different antimicrobial/organism
combinations. Understand their impact on resistance to other antimicrobials.
Understand local AMR epidemiology, resistance and susceptibility patterns.
Data collection and Be able to collect microbiology samples correctly.
analysis Ensure timeliness in the handling of microbiology samples and communication of susceptibility results.
Act as first line of surveillance in the correct use and reporting of microbiological tests and diagnostic tools.
Be able to interpret and use basic antimicrobial susceptibility testing results (in settings where they are
commonly used) and other microbiology testing tools: blood cultures, urine samples, wound samples and
screening cultures.
Be able to interpret and use new, more advanced microbiology samples, biomarkers, point-of-care tests:
• Understand how to use and interpret investigations that can help inform diagnosis of an infection (e.g.
microbiological investigations, biomarkers, point-of-care tests).
• Understand how to use and interpret investigations (e.g. microbiological investigations, biomarkers, point-of-
care tests) that can help in monitoring the response to treatment of infections.

3. Microbiology
Selective sensitivity Advocate for and comply with guidelines regarding antimicrobial susceptibility testing.
reporting/antibiogram Understand how to implement selective sensitive reporting to minimize broad-spectrum antimicrobial use.
Understand the basic principles of antibiograms and other reporting tools and their interpretation.
Understand the use of antibiograms in detecting and reporting AMR patterns.
Bug-drug combination Understand the common microbiological etiology and treatment of human infections.
chart
4. Clinical syndromes
Guidance and best Understand how and where to access relevant guidance on antimicrobial prescribing and AMS, and use this
practice knowledge when prescribing.
in antibiotic prescribing Understand that empirical treatment should be guided by local antimicrobial susceptibility patterns.
Promote best practice approaches by developing and implementing guidelines and/or clinical pathways.
Common infections Understand the decision process for appropriate antibiotic use: clinical assessment and clinical symptoms→
probable diagnosis, causative agents, diagnostics incl. microbiology sampling, patient characteristics incl.
comorbidities and risk factors for AMR, whether or not to treat with antibiotics, and how to choose antibiotics
to treat or prevent common infections incl. but not limited to:
• CAP
• UTI
• Diarrhoea
• SSTI
• Sepsis
• Surgical antibiotic prophylaxis
• Bacterial infections that resolve by themselves e.g. sinusitis and otitis media
• Influenza, malaria and other nonbacterial infections
• Symptoms not indicative of a bacterial infection, e.g. nonspecific uro-gynaecological symptoms
• Common health-care-associated infections e.g. UTIs, surgical site infections, catheter-related infections
5. AMS
Planning an AMS Plan AMS activities:
programme • Provide clear mechanisms for the governance of AMS, including addressing responsibility and
accountability for the quality and quantity of antimicrobials prescribed within a system.
• Ensure that health workers have the knowledge and awareness of effective approaches/interventions to
control AMR, and have the skills to implement change according to their role.
• Understand basic principles of behaviour change in the context of prescribing antimicrobials and model
good prescribing behaviour to colleagues.
• Understand the use of quality-improvement frameworks to address gaps and to improve antimicrobial use.
Performing Understand the key elements of a logical approach to continuation and appropriateness of antimicrobial
AMS interventions therapy and be able to implement AMS interventions:
• Adjusting doses (e.g. for patients with renal impairment), and where to seek advice about this.
• Monitoring antibiotic levels when indicated, and where to seek advice about this.
• Reviewing antibiotic therapy at 48–72 hours and regularly thereafter in hospitalized patients, and in
appropriate situations in the community.
• Switching antibiotics from intravenous to oral administration as soon as possible when indicated (according
to guidelines).
• Changing antibiotics, ideally to a narrower spectrum (de-escalation) or broader (escalation) spectrum,
according to microbiology results and clinical condition.
• Stopping antibiotics if there is no evidence of infection based on clinical findings and investigations, e.g.
negative microbial cultures, imaging reports.

5. AMS
Assessing an AMS • nderstand the types of indicators (structure, process and outcome measures).
U
programme • Identify sources of data, recognizing the benefits and limitations of each.
• Be able to use PPSs.
• Understand how to measure and calculate antimicrobial use metrics (DDDs, DOTs, etc.).
• Ensure timely and appropriate feedback to prescribers and other care groups.
• Understand and engage with any locally or nationally agreed quality measures for assessing antibiotic
prescriptions (e.g. compliance with guidance, adverse events, reviews of antibiotic therapy at 48–72 hours
in hospitalized patients).
• Understand the principles of AMR surveillance and the use of surveillance data.
• Understand and implement balancing measures.
• Understand the importance and stages of evaluation.
• Be able to monitor and report on the performance of hospital AMR and related AMS programmes.
7.2 Education and training
Once the facility has outlined the competencies required Practical training at centres of excellence
for the different staff groups, it needs to develop a training As centres of excellence and WHO collaborating centres
delivery plan, in other words, identify a leader, teachers for AMS are established globally, AMS teams and AMS
and participants, and make a time plan.89 The opportuni- champions are encouraged to gain practical hands-on
ty to use real-world clinical opportunities for training (e.g. training through these centres. Countries can also set up
ward rounds, clinical case discussions) should be empha- twinning or mentoring programmes with successful coun-
sized. In addition, those in training should be encouraged terparts, using context-relevant examples to support the
to access external training opportunities, including availa- establishment, implementation and monitoring of stew-
ble e-learning options (Figure 19). ardship interventions.
Key message: Integrated learning translates On the job learning

into integrated practice. A common approach to successful training makes use of
both existing structures and opportunities that arise in
Pre- and in-service training the clinical environment. For example, a member of the
AMS linked with IPC should be incorporated or strength- AMS team is reviewing a patient with sepsis who has been
ened in preservice training, curricula and textbooks.88 Vol- started empirically on broad-spectrum antibiotics (pipera-
untary or mandatory in-service training on AMS and IPC cillin/tazobactam), in contradiction to the antibiotic com-
is also encouraged, such as through inclusion of relevant bination recommended by the local treatment guidelines
AMS and IPC competencies in continuing medical educa- (amoxicillin/gentamicin and metronidazole). The empirical
tion. treatment was continued despite blood cultures that re-
vealed Escherichia coli susceptible to amoxicillin. A brief
Face-to-face workshops discussion with the attending physicians and nurses could
A possible structure for a face-to-face workshop, with provide an opportunity for training in one or more areas:
content aligned with the required competencies for AMS,
is presented in Table 12. However, this is a “menu” of
options which can be used to design a local training pro-
gramme that meets local needs, contexts and resources.
Blended learning
Blended learning, with its mix of technology and traditional 89

Practical approach to care kit – PACK. London: BMJ Publishing (https://
face-to-face instruction, is an approach that is commonly pack.bmj.com/, accessed 4 February 2019).
90

Antimicrobial resistance and stewardship. BSAC Virtual Learning
used. Blended learning combines classroom learning with Environment. British Society for Antimicrobial Chemotherapy (http://bsac-
online learning90,91 and is becoming increasingly popular, vle.com/, accessed online 3 September 2019).
91

Antimicrobial stewardship: a competency-based approach. WHO e-learning
as students can partly control the time, pace and place of course. Geneva: World Health Organization; n.d. (https://openwho.org/
their learning. courses/AMR-competency, accessed 3 September 2019).

FIGURE 18
EDUCATION AND TRAINING

Education and training delivery modes for AMS-related competencies
Professional Educational
University
organizations workshops
Continuing medical
Networks
education
Elearning Other On-the-job training

• raising awareness of the facility’s standard treatment opportunities for students while simultaneously enhancing
guidelines; faculty effectiveness and efficiency. However, this poten-
tial of e-learning assumes a certain level of institutional
• the importance and rationale for using recommended readiness in human and infrastructural resources that is
empirical agents for patients, but also the potential im- not always present in LMICs. Institutional readiness for
mediate and long-term harm of broad-spectrum therapy; e-learning adoption ensures the alignment of new tools to
the educational and economic context.94
• the benefit and safety of de-escalation antibiotic treat-
ment following cultures; and Other
Other examples of facility structures and meetings where
• the opportunity and benefits of IV-to-oral switching. training could be provided include morbidity and mortality
meetings, audit meetings, quality improvement and safety
As described in Chapter 5, holding ward rounds jointly with briefs, significant event analysis, risk management meet-
the unit health personnel and the AMS team is among the ings and journal clubs. Where possible and relevant, us-
most dynamic instances of learning. Every member of the ing team-based or multidisciplinary teaching and training
team attending to the patient has the opportunity to give events also provides an excellent opportunity for interpro-
their opinion, debate the pros and cons of each diagnostic fessional learning. As infection prevention and manage-
or therapeutic decision, and understand what is best for ment is very much a team-based approach, it enhances
this and future patients. the philosophy of learning together and delivering care
together to achieve better patient outcomes.
Recently, the organizational, resource-related and fiscal
benefits of learning for health-care professionals have The challenge for AMS facility training is to ensure that
been outlined in an excellent systematic review.92 This the capacity and capability exist for delivering a quality, ef-
pragmatic approach to on-the-job training and its rele- fective and sustainable programme or course. Therefore,
vance for optimal patient management can be instructive, having a simple model to ensure implementation of this
valued and is often retained. programme is important (Box 9).
E-learning 92
Al-Shorbaji N, Atun R, Car J, Majeed A, Wheeler E, editors. eLearning for
The importance of directing participants to local, nation- undergraduate health professional education: a systematic review informing
al and international e-learning resources is important in a radical transformation of health workforce development. Geneva: World
Health Organization; 2015 (https://whoeducationguidelines.org/sites/
ensuring the long-term sustainability of these education- default/files/uploads/eLearning-healthprof-report.pdf, accessed 4 February
al activities, and various resources already exist.91,93 In- 2019).
93
JAC-Antimicrobial Resistance. Open access journal on education and
deed, e-learning has been commended as one important research in AMS and AMR (https://academic.oup.com/jacamr, accessed 3
form of effectively delivering education in AMS. However, September 2019).
94
Frehywot S, Vovides Y, Talib Z, Mikhail N, Ross H, Wohltjen H et al.
e-learning is a means to an end, rather than the end in E-learning in medical education in resource constrained low- and middle-
itself. Using e-learning can result in greater educational income countries. Hum Resour Health. 2013;11:4.
B OX 9
Core steps for implementing an educational programme
1. Programme leaders (often the AMS team) are identified and should have acquired the advanced competencies to lead
and deliver local or regional training.
2. Training of programme leaders may require 2–3 days of face-to-face workshops using local, regional, national or
external resources.
3. Access to e-learning resources to support this is recommended. These leaders will require skill sets that have been
identified in train-the-trainer models.
4. The programme leaders in each facility or region identify a multidisciplinary faculty of trainers for advanced training in
AMS. Again, access to e-learning resources to support this effort is recommended. The faculty will develop the local
programme. It is always helpful to include at least one prescribing non-specialist as part of this group.
5. The faculty identifies the broad needs of the prescribing and related health-care professionals in their facility or
network. They devise a programme cycle that includes the target audience, course content and evaluation.

7.3 Effectiveness of different training and of “digital literacy” and on the capacity of providing insti-
education delivery tutions. These considerations must be taken into account
when developing e-learning courses.
While face-to-face training methods are the norm in many
LMICs, more active methods such as e-learning are in- A range of teaching methods, described in Table 14, are
creasingly used. Furthermore, blended programmes that used to deliver training. Broadly speaking, active methods
encompass some or many components of e-learning to are more effective than passive methods in changing pre-
augment traditional face-to-face training are becoming scribing behaviour.
more popular. There is evidence that the use of online and
mobile digital education in the management of antibiotics
for post-registration health-care professionals is associat-
ed with increased professional knowledge compared with 95
Kyaw BM, Car LT, van Galen LS, van Agtmael MA, Costelloe CE,
traditional education.95 E-learning approaches have been Ajuebor O et al. Health professions digital education for antibiotic
management: systematic review and meta-analysis by the Digital Health
shown to provide flexible, low-cost, user-centred and easily Education Collaboration. J Med Internet Res., accepted (http://dx.doi.
updated learning.96 However, the effectiveness of e-learn- org/10.2196/14984, accessed 3 September 2019).
96
E-learning for undergraduate health professional education: a systematic
ing varies from context to context and has been shown to review informing a radical transformation of health workforce development.
make considerable demands on users’ motivation, levels Geneva: World Health Organization; 2015.
TA B L E 14
Teaching methods for AMS interventions
CATEGORY METHOD
Passive • rinted educational materials
P
• Clinical practice guidelines
• Formal lectures
• Seminars, conferences
• Educational courses
• Reminders
• Distance learning, e-learning
Active • iscussion groups, journal clubs
D
• Educational outreach visits and academic discussions
• Audit and feedback
• Interactive role play, case scenarios, interactive educational workshops
• Sequenced educational sessions (learn-work-learn), learning by working (practice)
• Distance learning, e-learning

ANNEXES

Annex I: Sample terms of reference – national AMS technical working group
Purpose
• Provide strategic leadership on AMS (and IPC) measures under the national action plan on AMR.
• Provide a coordinated approach for national, health-care facility and community AMS (rational use of antimicrobials)
programmes.
• Support national and international efforts as appropriate.
The overall aim of the AMS TWG is to optimize the use of existing antimicrobials and prevent the spread of resistant infections.
Accountable to
• National AMR Steering Committee
• Professional organizations and others as applicable
Responsibilities and activities

• Oversees and co-ordinates the development and implementation of national strategy and/or policy for controlling AMR
by optimizing the use of antimicrobials through the implementation of AMS programmes.
• Ensures sufficient resources (human and financial) to achieve the objectives and outcomes of the national AMS strategy
or policy.
• Ensures that relevant education and training on AMS are provided to pre- and in-service health-care professionals.
• Undertakes M&E of AMS interventions at the national, health-care facility and community level based on the national
AMS strategy or plan on an annual or biannual basis.
Membership (to be adapted based on the country context)

The membership of the national AMS TWG should be composed of members representing the relevant departments within
the ministry of health responsible for the selection, procurement, supply, distribution, prescribing and use of antimicrobials at
the national level. Inclusion of additional sectors, notably the animal health, food and environment sectors, is advisable. Rep-
resentatives should be given sufficient authority by their institutions to make decisions. The TWG should remain small enough
to be functional, striking a balance between full representation and the functionality of the group to coordinate a national AMS
strategy, policy or plan and be linked with other relevant groups/TWGs (AMR and AMC surveillance, etc.).
Frequency of meetings
The meeting format and rules should conform to national norms. Standard operating procedures may be elaborated trans-
parently and according to the principles of best practice to guide the activities of the TWG. A chairperson should be selected
based on his or her expertise in leadership. Rotation of the chair among members of the TWG could be considered. The TWG
should meet on a regular basis, at a minimum quarterly or biannually.
Conflict of interest
It is recommended that the group have a mechanism (with appropriate records) to ensure that its members have no conflicts
of interests and that the work of the TWG in the interests of public health is transparent.

Annex II: Sample terms of reference – health-care facility AMS committee
Purpose
The health-care facility AMS committee provides oversight and coordination of the implementation and review of the AMS
programme at the facility. The AMS programme involves a systematic approach to optimizing the use of antimicrobials in the
facility to improve patient outcomes, reduce inappropriate antimicrobial prescribing and reduce adverse consequences of
antimicrobial use (including AMR and unnecessary costs).
Accountable to (adapted to the national context)

1. National AMS TWG (or as applicable)
2. Health-care facility leadership/management

• Liaises closely with other existing committees, including the drug and therapeutics committee,
IPC committee and patient safety committee.
• Reviews the health-care facility core elements checklist, undertakes a SWOT analysis.
• Develops, endorses and implements a stepwise facility plan of action for AMS that includes setting targets for
optimized antimicrobial use.
• Ensures that an education and training plan on AMS is in place for clinical staff in the facility.
• Ensures allocation of financial and human resources for implementing an AMS programme in the facility.
• Formalizes a health-care facility AMS team that reports to the AMS committee.
• Endorses the implementation of systems to monitor AMC and/or use and resistance.
• Reviews, endorses and implements clinical guidelines for antimicrobial prescribing.
• Endorses the implementation of an education programme for appropriate prescribing and AMS, in liaison with
clinical educators in the facility.
• Monitors and evaluates compliance with one or more of the specific interventions put in place by the AMS team
and reports back to the AMS team and prescribers on a regular basis.
• Facilitates the development and dissemination of regular activity reports that include data on antibiotic use and
describe the interventions implemented by the AMS team.
• Undertakes risk assessment and plans action to improve the effectiveness of the AMS programme.
Membership and roles (to be adapted based on the facility context)

The membership of the health-care facility AMS committee will consist of the following:
• health-care facility administrator (executive sponsor/chair)

• director medical services (deputy chair)
• infectious diseases physician and/or clinical microbiologist (AMS team clinical lead)
• AMS pharmacist or physician (secretary);
• directors of other departments
• patient safety and clinical quality manager
• nursing representative
• pharmacy representative
• medical staff representatives from the different wards
• microbiology representative
• IT representatives (if applicable)
• drug and therapeutics committee representative (if the AMS committee is not embedded in the drug and
therapeutics committee)
• IPC committee representative (if the AMS committee is not embedded in the IPC committee)
• Patient safety committee representative (if the AMS committee is not embedded in the patient safety committee).
Other personnel may be co-opted as required to assist the work of the committee.

The meetings should be held on a regular basis, ideally monthly, with a minimum of quarterly. It is advised that regular meet-
ings also be held either with other relevant groups (e.g. drug and therapeutics committee, IPC) or that members from those
other groups be invited to participate in the AMS committee meeting as needed.
Agenda preparation and circulation of minutes

Papers for the committee will be prepared by the AMS committee secretary and circulated 1 week prior to the meeting date.
The agenda will be determined by the AMS committee chair prior to meetings. Minutes will be distributed to members within
2 weeks of the meeting date by the AMS committee secretary.
In addition to committee members, minutes will be made available to:

• the drug and therapeutics committee;
• the IPC committee;
• the patient safety committee; and
• others as needed.

Annex III: Sample terms of reference – health-care facility AMS team
Purpose
• To implement the health-care facility AMS action plan and to facilitate optimized use of antimicrobials in the departments
and wards.
Accountable to
1. Health-care facility AMS committee

• Delineates the roles and responsibilities of each team member in the AMS team.
• Implements day-to-day AMS activities, including conducting regular ward rounds and other AMS interventions
in select facility departments identified in the health-care facility AMS action plan.
• Undertakes audits or PPSs to assess the appropriateness of infection management and antibiotic prescription
according to policy/guidance.
• In collaboration with the facility pharmacy, monitors, analyses and interprets the quantity and types of antibiotic
use at the unit and/or facility-wide level.
• Monitors antibiotic susceptibility and resistance rates for a range of key indicator bacteria at the facility-wide level or
uses the data from existing groups that are monitoring this information.
• Facilitates education and training on AMS in the facility.
Membership (to be adapted based on the country context)

Option 1: >2 health-care professionals constituting a multidisciplinary team (e.g. tertiary hospitals). The multidisciplinary
team should comprise a physician, a pharmacist or clinical pharmacologist, a nurse with expertise in infections or IPC, and in
facilities with a microbiology laboratory, a microbiologist or laboratory technician.
Option 2: a physician and a nurse or pharmacist, with access to expert advice (e.g. secondary or small facilities).
Option 3: a nurse or pharmacist leading the stewardship programme, with access to expert advice (e.g. secondary or small
facilities with limited resources).
• Weekly to two times a month

Annex IV: Sample AMS review form
Annex IV: Sample AMS review form
Patient information
Date: Department: Ward:
Patient name: Age: Sex: Male ☐ or Female ☐
Antibiotic prescriptions
Antibiotics prescribed Dose Route Interval Start date
Indication for antibiotic treatment

Prophylaxis ☐ Urinary tract Pneumonia ☐ Gastrointestinal Bloodstream
infection ☐ infection ☐ infection ☐
CNS ☐ Skin infection ☐ Bone infection ☐ Other:
Initial review of antibiotic treatment

Is indication for antibiotic Is antibiotic treatment prescribed Comments
treatment documented? according to guideline?
Yes ☐ Yes ☐
No ☐ No ☐ Why not? Comment
Correct dose? Appropriate route? Treatment duration or review date stated?
Yes ☐ Yes ☐ Yes ☐
No ☐ No ☐ No ☐
48-‐hour review of antibiotic treatment

Is antibiotic treatment reviewed? Yes ☐ No ☐ If yes, what action?
Escalate ☐ Continue ☐ De-‐escalate ☐ Stop ☐ IV-‐oral switch ☐
Why is antibiotic treatment being continued?
Continuing clinical signs of Confirmed infection ☐ Other (comment):

infection ☐
Microbiology specimens collected? Microbiology results received? Microbiology results acted upon?
☐ Date: ☐ Date: ☐ Comment:
General comments:
Date:_____________ Name/signature (reviewer) ______________________________________________
77

Annex V: Sample
Annex pre-authorization/restricted
V: Sample prescribing
pre-authorization/restricted
Annex form
prescribing
V: Sample form
pre-authorization/restricted p
Date:__________________
Patient information Patient information
Patient name: Department: Patient name: Ward: Department: Ward
Age: Sex: Male ☐ Female ☐

Age: Allergies: Sex: Male ☐ Female ☐ Aller
Indication for antibiotic treatment Indication for antibiotic treatment
Request for pre-authorized/restricted antibiotics

Request for pre-authorized/restricted antibiotics
Dose and Administration Dose and Administration
Antibiotic(s) requested Interval
Antibiotic(s) requested Reason for request Inte
duration route duration route
Are microbiology test results with sensitivity testing

Are amvailable? es r ☐
icrobiology t Yest Nw
esults ☐ sensitivity testing available?
o ith Yes
If yes, provide details: If yes, provide details:
Date Specimen Pathogen identified and susceptibility
Date Specimen results Pathogen identified and susc
Yes t☐
Has the patient already received antibiotic(s)? Has ☐ If yes,
Npo atient
he what? received antibiotic(s)? Yes ☐ No ☐ If yes, w
already
Dose and Administration Why ias nd
Dose the treatment
Administration
Antibiotic(s) prescribed Interval
Antibiotic(s) prescribed Inte
duration route not adequate? route
duration
Requesting physician’s name/contact number:_______________________________________________________________

Requesting physician’s name/contact number:________________________
Comments from the AMS team/Drug and therapeutics

Comments committee/Pharmacy department
from the AMS team/Drug and therapeutics committee/
Approver Approver
☐ APPROVED ☐
☐ NOT APPROVED
APPROVED ☐ NOT APPROVED
Remarks: Remarks:
Name/signature of specialist:__________________________ Date:____________________
Name/signature of specialist:__________________________ Date:_____________
78

Annex VI: Sample medical chart
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wtard
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name,
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no.:
no.:

Weight:
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0 Weight:
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kg0 7k0 gkg
Date oDate
f birth:
Date
Date
of 1bo0/08/1948
irth:
f obf irth:
b1irth:
0/08/1948
10/08/1948
10/08/1948 Dates:Dates:
Dates:
Dates:
Height:
Height:
Height:
1Height:
68
c m
168
1 68
c 1m68
cmcm
19/09/2018
19/09/2018
19/09/2018
19/09/2018
20/09/2018
20/09/2018
20/09/2018
20/09/2018
21/09/2018
21/09/2018
21/09/2018
21/09/2018
22/09/2018
22/09/2018
22/09/2018
22/09/2018
23/09/2018
23/09/2018
23/09/2018
23/09/2018
24/09/2018
24/09/2018
24/09/2018
24/09/2018
30/09/2018
30/09/2018
30/09/2018
30/09/2018
Date aDate
dmiZed:
Date
Date
admiZed:
a dmiZed:
a1dmiZed:
9/09/2018
19/09/2018
1 9/09/2018
19/09/2018
P* P* P*P*
T* T* T*T*
Diagnosis:
Diagnosis:
Diagnosis:
Diagnosis:
Allergies:
Allergies:
Allergies:
Allergies:
130 130130
130
40 40° 4040 ° ° °
Pneumonia-‐Ca
Pneumonia-‐Ca
Pneumonia-‐Ca
Pneumonia-‐Ca None None None None ° ° ° °
* * ** ° ° ° °
110 110110
110
39 39 3939 * * **
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Co morbidiJes
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38 38 3838 * * **
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° ° ° °
70 70 7070
37 37 3737 ° ° ° ° ° ° ° °
* * ** * * **
50 36 3636 50 5050
36
BP: BP:BP: BP: BP: BP:BP: BP: BP: BP:BP: BP: BP: BP:BP: BP: BP: BP:BP: BP: BP: BP:BP: BP: BP: BP:BP: BP:
Dose interval
Dose
Dose
Dose
interval
interval
interval
Date oDate
f Date
Date
of of of Adm. Adm.
Adm.
Adm. RR: RR:RR: RR: RR: RR:RR: RR: RR: RR:RR: RR: RR: RR:RR: RR: RR: RR:RR: RR: RR: RR:RR: RR: RR: RR:RR: RR:
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ANTIMICROBIAL STEWARDSHIP PROGRAMMES IN HEALTH-CARE FACILITIES IN LOW- AND MIDDLE-INCOME COUNTRIES

69
70
Annex VII: Sample bug-drug chart
Site of Infection Skin and soft tissue Respiratory Gastrointestinal / Urinary

Gut
Beta-hemolytic Streptococcus Enterococcus Enterococcus Resistant Gram-negatives
“Common pathogens” MRSA MSSA E. coli Klebsiella anaerobes
streptococci pneumoniae faecalis faecium Pseudomonas ESCAPPM ESBLs
Penicillin +
Amoxicillin /
Penicillins + + +
Ampicillin
Cloxacillin + + +/-
Cephalexin /
+ + +/- +/-
Cefazolin
Cephalosporins Ceftriaxone /
+ + + +
Cefotaxime
Ceftazidime + + +
Beta-lactam / Co-amoxiclav + + + + + + +
beta-lactamase Piperacillin-
inhibitors + + + + + + + +
tazobactam
Ertapenem + + + + + + + +
Carbapenems Meropenem /
+ + + + + + + + +
Imipenem
Glycopeptides Vancomycin + + + + + +
Doxycycline + + +/- +/- +/- +/- +/-
Trimethoprim-
+ + +/- +/- +/- +/-
sulfamethoxazole
Moxifloxacin + + + + + + +/-
Ciprofloxacin +/- +/- +/- +/- +/- +/- +/-
Aminoglycosides + + + + +/-
Miscellaneous
Daptomycin /
+ + + + + +

Linezolid
Clindamycin +/- +/- +/- +/-
Polymyxin /
+ + + +/- +
Colistin*
Metronidazole +
* Serratia, Proteus, Providencia, Morganella, B. cepacia are intrinsically resistant to polymyxin/colistin.
Annex VIII: Sample cumulative antibiogram for gram-negative bacteria
β-Lactams
Gram-negative Bacteria Isolates Penicillins Cephalosporins Carbapenems Aminoglycosides FQ Other
(N) AMP AMC TZP CZO CXM CTX CAZ FEP IPM MEM ETP AMK GEN TOB CIP ATM SXT NIT
Gram-negative bacteria (all) 34 932 28 69 89 59 63 73 – 83 91 95 96 95 880 85 68 69 68 76
Haemophilus influenzae 900 85 93 – – 96 – – – – – – – – – 96 – 92 –
Moraxella catarrhalis 211 – 95 – – 100 – – – – – – – – – 95 – 99 –
Enterobacteriaceae 27 972 28 70 92 60 – 75 – 84 95 99 98 98 89 87 67 79 68 –
Citrobacter koseri (diversus) 550 R 95 98 90 80 95 – 98 98 99 99 100 99 99 96 91 98 87
Enterobacter cloacae 802 R R 86 R 51 79 – 92 91 98 94 99 93 93 86 86 89 48
Enterobacter aerogenes 543 R R 85 R R 82 – 95 65 98 98 100 95 94 85 88 92 25
Escherichia coli 16 810 36 74 93 59 66 71 – 81 99 99 99 99 89 86 62 76 60 94
Klebsiella pneumoniae 5 713 R 79 87 60 70 76 – 85 97 97 97 98 91 86 73 80 77 32
Klebsiella oxytoca 236 R 90 93 – 75 88 – 91 98 98 99 98 95 88 83 83 88 86
Morganella morganii 305 R R 96 R R 68 – 92 53 99 99 100 79 79 44 77 61 R
Proteus mirabilis 878 66 93 99 84 92 92 – 94 22 98 96 98 82 87 65 91 62 R
Providencia spp. 111 R R 95 R – 92 – 97 59 95 90 100 79 71 68 – 84 R
Salmonella spp. (non-typhoid) 566 86 92 99 – – 97 – 99 – – – – – – – – 96 –
Salmonella Typhi/Paratyphi 267 73 81 92 – – 81 – 71 – – – – – – – – 73 –

Serratia marcescens 652 R R 95 R R 91 – 97 71 98 98 100 97 89 87 98 98 R
Shigella spp. 79 37 72 98 – – 65 – 78 – – – – – – 52 – 48 91
Non-fermenting gram-neg rods 5 638 R R 77 – – – 82 80 76 76 R 82 82 80 73 56 72 –
Acinetobacter baumannii 750 R R 72 – – – 70 70 78 76 R 89 77 77 73 R 82 –
Pseudomonas aeruginosa 3 728 R R 91 – R R 87 90 84 83 R 95 91 95 82 68 R R
Stenotrophomonas maltophilia 479 R R R – – R 66 – R R R R R R – R 87 –
FQ = fluoroquinolones, N = number, spp. = species, R = intrinsically resistant, (–) = no data available, or small number of isolates tested (N<30), or antimicrobial agent is not indicated, or not effective clinically.
Interpretation standard: CLSI M100 ED29:2019. Presentation standard: CLSI M39-A4:2014.
AMC = Amoxicillin/Clavulanic acid, AMK = Amikacin, AMP = Ampicillin, ATM = Aztreonam, CAZ = Ceftazidime, CIP = Ciprofloxacin, CTX = Cefotaxime, CXM = Cefuroxime, CZO = Cefazolin, ETP = Ertapenem, FEP =

Cefepime, GEN = Gentamicin, IPM = Imipenem, MEM = Meropenem, NIT = Nitrofurantoin, SXT = Trimethoprim/Sulfamethoxazole, /Clavulanic acid, TOB = Tobramycin, TZP = Piperacillin/Tazobactam.
71
World Health Organization
Antimicrobial Resistance Division
20 Avenue Appia
1211 Geneva 27
Switzerland
https://www.who.int/antimicrobial-resistance/en/
ISBN 978-92-4-151548-1

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A N T I M I C R O B I A L S T E WA R D S H I P P R O G R A M M E S

A WHO PRACTICAL TOOLKIT

A WHO PRACTICAL TOOLKIT

© World Health Organization 2019

Suggested citation. Antimicrobial stewardship programmes in health-care facilities in low- and

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List of figures, tables and boxes. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . v

2. Structures for national (state/regional) AMS programmes . . . . . . . . . . . . . . . . . . . . . . . . 5

3. Structures for health-care facility AMS programmes . . . . . . . . . . . . . . . . . . . . . . . . . . . 11

4. Planning an AMS programme in a health-care facility. . . . . . . . . . . . . . . . . . . . . . . . . . 17

5. Performing AMS interventions in a health-care facility. . . . . . . . . . . . . . . . . . . . . . . . . . 30

7. Education and training . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 53

Annex I: Sample terms of reference – national AMS technical working group. . . . . . . . . 63

iv ANTIMICROBIAL STEWARDSHIP PROGRAMMES IN HEALTH-CARE FACILITIES IN LOW- AND MIDDLE-INCOME COUNTRIES

Figure 1.  Integrated approach to optimizing use of antimicrobials towards universal

Table 1. WHO toolkit for AMS programmes in health-care facilities in LMICs. . . . . . . . . . . . . 3

ANTIMICROBIAL STEWARDSHIP PROGRAMMES IN HEALTH-CARE FACILITIES IN LOW- AND MIDDLE-INCOME COUNTRIES v

vi ANTIMICROBIAL STEWARDSHIP PROGRAMMES IN HEALTH-CARE FACILITIES IN LOW- AND MIDDLE-INCOME COUNTRIES

This document was edited by Giselle Weiss.

AMC antimicrobial consumption LMIC low- and middle-income country

AMR antimicrobial resistance M&E monitoring and evaluation

AMS antimicrobial stewardship MDR multidrug-resistant

AWaRe ACCESS, WATCH, RESERVE PDR pan drug-resistant

CAP community-acquired pneumonia PPS point prevalence survey

ANTIMICROBIAL STEWARDSHIP PROGRAMMES IN HEALTH-CARE FACILITIES IN LOW- AND MIDDLE-INCOME COUNTRIES ix

Community-acquired infection: An infection acquired in the community, outside of a health-care setting.

x ANTIMICROBIAL STEWARDSHIP PROGRAMMES IN HEALTH-CARE FACILITIES IN LOW- AND MIDDLE-INCOME COUNTRIES

ANTIMICROBIAL STEWARDSHIP PROGRAMMES IN HEALTH-CARE FACILITIES IN LOW- AND MIDDLE-INCOME COUNTRIES xi

ANTIMICROBIAL STEWARDSHIP PROGRAMMES IN HEALTH-CARE FACILITIES IN LOW- AND MIDDLE-INCOME COUNTRIES 1

Many countries around the world have developed and 17

IPC Opti mi ze use

Immunization Antibiotics use

2 ANTIMICROBIAL STEWARDSHIP PROGRAMMES IN HEALTH-CARE FACILITIES IN LOW- AND MIDDLE-INCOME COUNTRIES

WHO toolkit for AMS programmes in health-care facilities in LMICs

Outline of competencies for health-care professionals performing AMS activities (Chapter 7)

1.3 Establishing AMS programmes

Key steps in establishing a national AMS programme to enable facility AMS

ANTIMICROBIAL STEWARDSHIP PROGRAMMES IN HEALTH-CARE FACILITIES IN LOW- AND MIDDLE-INCOME COUNTRIES 3

Key steps to establishing a health-care facility AMS programme

In a 600-bed health-care facility in Barbados, an outbreak of carbapenemase-resistant Klebsiella pneumoniae (KPC)

4 ANTIMICROBIAL STEWARDSHIP PROGRAMMES IN HEALTH-CARE FACILITIES IN LOW- AND MIDDLE-INCOME COUNTRIES

ANTIMICROBIAL STEWARDSHIP PROGRAMMES IN HEALTH-CARE FACILITIES IN LOW- AND MIDDLE-INCOME COUNTRIES 5

In developing the essential national core elements, a group

National plan Regulation

6 ANTIMICROBIAL STEWARDSHIP PROGRAMMES IN HEALTH-CARE FACILITIES IN LOW- AND MIDDLE-INCOME COUNTRIES

* “Country” can be substituted by “state” or “region” depending on the context.

ANTIMICROBIAL STEWARDSHIP PROGRAMMES IN HEALTH-CARE FACILITIES IN LOW- AND MIDDLE-INCOME COUNTRIES 7

NATIONAL CORE ELEMENTS Yes No

3. Technical working group on AMS established with clear terms of reference

4. National AMS implementation plan or policy endorsement

8. Regulations on fixed-dose combinations of antibiotics

9a. Regulations on prescription-only sale of antibioticsi

9b. Regulation and enforcement of prescription-only dispensing of antibioticsi

10. Measures in place to ensure continued availability of quality-assured antibioticsi

11. Measures in place to ensure affordability of essential antibioticsi

8 ANTIMICROBIAL STEWARDSHIP PROGRAMMES IN HEALTH-CARE FACILITIES IN LOW- AND MIDDLE-INCOME COUNTRIES

13. Education in schools on basic infection principles

14. Training on AMS competencies for AMS team members

15. Education and training for all health-care professionals on AMS

17. National surveillance system on AMC in placei,ii

community sector, if possible), following the WHO methodology on surveillance of AMC.

Figure 1. Integrated approach to optimizing use of antimicrobials towards universal

Table 1. WHO toolkit for AMS programmes in health-care facilities in LMICs. . . . . . . . . . . . . 3

• A ctive implementation of the NAP on AMR • Unstable access to essential antibiotics