# Challenges and success stories of the implementation of infection control and antimicrobial stewardship strategies: proceedings of the 5th Global Ministerial Summit on Patient Safety, 2023

Andrea C Büchler, Murielle Haddad Galas, Niccolò Buetti, Emine Alp, Anucha Apisarnthanarak, Gerald Dziekan, Valeria Fabre, Simon Gottwalt, Kazuaki Jindai, Babacar Ndoye, et al.

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Andrea C Büchler, Murielle Haddad Galas, Niccolò Buetti, Emine Alp, Anucha Apisarnthanarak, et al.. Challenges and success stories of the implementation of infection control and antimicrobial stewardship strategies: proceedings of the 5th Global Ministerial Summit on Patient Safety, 2023. Antimicrobial Resistance and Infection Control, 2024, 13 (1), pp.16. 10.1186/s13756-023-01344-7. hal-04586638

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# Challenges and success stories of the implementation of infection control and antimicrobial stewardship strategies: proceedings of the 5th Global Ministerial Summit on Patient Safety, 2023

Andrea C Büchler, Murielle Haddad Galas, Niccolò Buetti, Emine Alp, Anucha Apisarnthanarak, Gerald Dziekan, Valeria Fabre, Simon Gottwalt, Kazuaki Jindai, Babacar Ndoye, et al.

## ► To cite this version:

Andrea C Büchler, Murielle Haddad Galas, Niccolò Buetti, Emine Alp, Anucha Apisarnthanarak, et al.. Challenges and success stories of the implementation of infection control and antimicrobial stewardship strategies: proceedings of the 5th Global Ministerial Summit on Patient Safety, 2023. Antimicrobial Resistance and Infection Control, 2024, 13 (1), pp.16. 10.1186/s13756-023-01344-7. hal-04586638

HAL Id: hal-04586638

https://u-paris.hal.science/hal-04586638v1

Submitted on 24 May 2024

HAL is a multi-disciplinary open access archive for the deposit and dissemination of scientific research documents, whether they are published or not. The documents may come from teaching and research institutions in France or abroad, or from public or private research centers.

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<figure><img src="image_1.png" /></figure>

Distributed under a Creative Commons Attribution 4.0 International License
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# Challenges and success stories of the implementation of infection control and antimicrobial stewardship strategies: proceedings of the 5th Global Ministerial Summit on Patient Safety, 2023

Andrea C. Büchler¹, Murielle Haddad Galas¹, Niccolò Buetti¹,², Emine Alp³, Anucha Apisarnthanarak⁴, Gerald Dziekan⁵, Valeria Fabre⁶, Simon Gottwalt⁵, Kazuaki Jindai⁷,⁸, Babacar Ndoye⁹, Hilda Márquez Villareal¹⁰, Fernando Otaiza¹¹, Didier Pittet¹, Natalie Schellack¹², Céline Gardiol⁵ and Stephan Harbarth¹*

**Abstract**

The 5th edition of the Global Ministerial Summit on Patient Safety was held in Montreux, Switzerland, in February 2023, delayed by three years due to the COVID-19 pandemic. The overarching theme of the summit was "Less Harm, Better Care – from Resolution to Implementation", focusing on the challenges of implementation of infection prevention and control (IPC) strategies as well as antimicrobial stewardship programs (ASP) around the world. IPC strategies and ASP are of increasing importance due to the substantial burden of healthcare-associated infections and antimicrobial resistance threatening patient safety. Here, we summarize countries' and regional experiences and activities related to the implementation of IPC strategies and ASP shared at the meeting. Full implementation of effective programs remains a major challenge in all settings due to limited support by political and healthcare leaders, and human and financial constraints. In addition, the COVID-19 pandemic challenged already well-established programs. By enforcing sustained implementation by dedicated, cross-disciplinary healthcare personnel with a broad skill set, a reduction in healthcare-associated infections and multidrug-resistant pathogens can be achieved, leading ultimately to improved patient safety.

**Keywords** Infection control, Antibiotic stewardship, Antimicrobial resistance, Health plan implementation, Global ministerial summit on patient safety

Full list of author information is available at the end of the article

<footnote>*Correspondence:
Stephan Harbarth
stephan.harbarth@hcuge.ch</footnote>
<figure><img src="image_2.png" /></figure>

Check for
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# Challenges and success stories of the implementation of infection control and antimicrobial stewardship strategies: proceedings of the 5th Global Ministerial Summit on Patient Safety, 2023

Andrea C. Büchler¹, Murielle Haddad Galas¹, Niccolò Buetti¹,², Emine Alp³, Anucha Apisarnthanarak⁴, Gerald Dziekan⁵, Valeria Fabre⁶, Simon Gottwalt⁵, Kazuaki Jindai⁷,⁸, Babacar Ndoye⁹, Hilda Márquez Villareal¹⁰, Fernando Otaiza¹¹, Didier Pittet¹, Natalie Schellack¹², Céline Gardiol⁵ and Stephan Harbarth¹*

**Abstract**

The 5th edition of the Global Ministerial Summit on Patient Safety was held in Montreux, Switzerland, in February 2023, delayed by three years due to the COVID-19 pandemic. The overarching theme of the summit was "Less Harm, Better Care – from Resolution to Implementation", focusing on the challenges of implementation of infection prevention and control (IPC) strategies as well as antimicrobial stewardship programs (ASP) around the world. IPC strategies and ASP are of increasing importance due to the substantial burden of healthcare-associated infections and antimicrobial resistance threatening patient safety. Here, we summarize countries' and regional experiences and activities related to the implementation of IPC strategies and ASP shared at the meeting. Full implementation of effective programs remains a major challenge in all settings due to limited support by political and healthcare leaders, and human and financial constraints. In addition, the COVID-19 pandemic challenged already well-established programs. By enforcing sustained implementation by dedicated, cross-disciplinary healthcare personnel with a broad skill set, a reduction in healthcare-associated infections and multidrug-resistant pathogens can be achieved, leading ultimately to improved patient safety.

**Keywords** Infection control, Antibiotic stewardship, Antimicrobial resistance, Health plan implementation, Global ministerial summit on patient safety

Full list of author information is available at the end of the article

<footnote>*Correspondence:
Stephan Harbarth
stephan.harbarth@hcuge.ch</footnote>
## Introduction

In 2016, the first edition of the Global Ministerial Summit on Patient Safety was held in London. Over the years, these summits have been raising awareness for this crucial public health issue by bringing together political leaders with experts of the field. The 5th edition of the Global Ministerial Summit on Patient Safety was held in Montreux, Switzerland, in February 2023. The overarching theme of the summit was "Less Harm, Better Care – from Resolution to Implementation". The event covered a wide spectrum of patient safety related topics including challenges of implementation of infection prevention and control (IPC) strategies as well as antimicrobial stewardship programs (ASP) around the world. Over 500 international participants with various backgrounds such as medical professionals, civil servants, patient representatives and academia shared their insights on sustainable implementation of patient safety measures with official high-level delegations from about 80 countries from all regions around the world.

IPC strategies and ASP are of high importance due to the substantial burden of healthcare-associated infections (HAI) and antimicrobial resistance (AMR) threatening patient safety. HAI are the most frequent adverse event in healthcare, affecting 5–15% of patients in acute care hospitals, leading to high morbidity and mortality with incalculable economic costs [1–3]. AMR is an additional major menace, listed as one of the ten most urgent health threats in 2019 by the World Health Organization (WHO) [4]. Recently, it was estimated that 1.3 million deaths attributable to AMR occurred in 2019 [5]. The implementation of effective prevention strategies for AMR is ongoing, focusing mostly on improved hand hygiene, ASP, IPC strategies, and environmental hygiene, but also improving development of and access to rapid diagnostics and prescriptions as well as mass media campaigns.

This paper summarizes the main proceedings of eight countries and regions from different parts of the world, who were invited to this Global Ministerial Summit on Patient Safety to report their experiences on the implementation of IPC strategies and ASP with the overarching aim to reduce the burden of HAI and AMR in various healthcare settings.

## Implementation of IPC strategies and ASP: challenges and successes

### Implementing IPC core components: experiences from four countries

The WHO global strategy on IPC is based on two main pillars: political action, supported by the World Health Assembly resolution "Global Strategy on IPC" of 2022 [6], and healthcare facility-centered action. The latter is based on the eight core components recommended

by the WHO [7] (Table 1). However, uncertainty exists about real-life implementation of the WHO resolution as efforts might be variable. Four countries provided an insight in their practices at the 5th Global Ministerial Summit on Patient Safety 2023. The overview of the country experiences is presented in Table 2.

## Senegal

Senegal's healthcare system is predominantly public. The healthcare costs were 77 USD per capita in 2020 [8]. Since 2004, a national IPC program has been progressively implemented. The main achievements of the program have been to train healthcare workers in a specialized training facility, the establishment of IPC committees in all hospitals, the completion of three national HAI prevalence surveys, a dedicated program to improve hand hygiene and basic hygiene measures, as well as the regulation of the healthcare waste management. Unfortunately, the activities were not sustainable after the withdrawal of funding provided by external partners due to lack of human, material, and operational resources. In 2017, after 13 years of an active IPC program, Senegal achieved an overall performance score of 15% in the IPCAT2 WHO tool [9], during an international IPC training workshop, showing lack of implementation. However, in the following five years, the overall performance increased to 52% of the minimum requirements with an increase in IPC program and guideline implementation, education and training, surveillance, and multimodal strategies. It should be noted that during this period, the majority of activities implemented were financed and directed by partners, instead of following a well-structured national action plan with well-defined objectives, strategies and indicators. This last assessment was carried out during a national workshop held in 2022, which also helped to develop a new IPC strategic plan for the period 2023–2027. However, these results need to be interpreted with caution, as it compares the full IPC requirements to the minimum requirements, and the latter was assessed by a self-assessment approach possibly overestimating the performance.

## Mexico

In Mexico, the healthcare system is integrated by different public and private institutions and different amendments are currently being made to the model of care. The healthcare costs were 539 USD per capita in 2020 [8]. There is no overarching national IPC strategy, but 15 IPC initiatives are currently promoted including 6 regulatory frameworks and 9 manuals or guidelines [10]. Examples for these IPC initiatives are the national standard for epidemiological surveillance and a manual of standardized procedures for hospital surveillance. The biggest challenges in patient safety experienced in Mexico are the
**Introduction**

In 2016, the first edition of the Global Ministerial Sum-
mit on Patient Safety was held in London. Over the years,
these summits have been raising awareness for this cru-
cial public health issue by bringing together political
leaders with experts of the field. The 5th edition of the
Global Ministerial Summit on Patient Safety was held in
Montreux, Switzerland, in February 2023. The overarch-
ing theme of the summit was "Less Harm, Better Care –
from Resolution to Implementation". The event covered a
wide spectrum of patient safety related topics including
challenges of implementation of infection prevention and
control (IPC) strategies as well as antimicrobial steward-
ship programs (ASP) around the world. Over 500 inter-
national participants with various backgrounds such as
medical professionals, civil servants, patient representa-
tives and academia shared their insights on sustainable
implementation of patient safety measures with official
high-level delegations from about 80 countries from all
regions around the world.

IPC strategies and ASP are of high importance due to
the substantial burden of healthcare-associated infec-
tions (HAI) and antimicrobial resistance (AMR) threat-
ening patient safety. HAI are the most frequent adverse
event in healthcare, affecting 5–15% of patients in acute
care hospitals, leading to high morbidity and mortality
with incalculable economic costs [1–3]. AMR is an addi-
tional major menace, listed as one of the ten most urgent
health threats in 2019 by the World Health Organiza-
tion (WHO) [4]. Recently, it was estimated that 1.3 mil-
lion deaths attributable to AMR occurred in 2019 [5].
The implementation of effective prevention strategies
for AMR is ongoing, focusing mostly on improved hand
hygiene, ASP, IPC strategies, and environmental hygiene,
but also improving development of and access to rapid
diagnostics and prescriptions as well as mass media
campaigns.

This paper summarizes the main proceedings of eight
countries and regions from different parts of the world,
who were invited to this Global Ministerial Summit on
Patient Safety to report their experiences on the imple-
mentation of IPC strategies and ASP with the overarch-
ing aim to reduce the burden of HAI and AMR in various
healthcare settings.

Implementation of IPC strategies and ASP:
challenges and successes

Implementing IPC core components: experiences from four countries

The WHO global strategy on IPC is based on two main
pillars: political action, supported by the World Health
Assembly resolution “Global Strategy on IPC” of 2022
[6], and healthcare facility-centered action. The latter
is based on the eight core components recommended

by the WHO [7] (Table 1). However, uncertainty exists
about real-life implementation of the WHO resolution
as efforts might be variable. Four countries provided
an insight in their practices at the 5th Global Ministere-
rial Summit on Patient Safety 2023. The overview of the
country experiences is presented in Table 2.

Senegal

Senegal's healthcare system is predominantly public. The healthcare costs were 77 USD per capita in 2020 [8]. Since 2004, a national IPC program has been progressively implemented. The main achievements of the program have been to train healthcare workers in a specialized training facility, the establishment of IPC committees in all hospitals, the completion of three national HAI prevalence surveys, a dedicated program to improve hand hygiene and basic hygiene measures, as well as the regulation of the healthcare waste management. Unfortunately, the activities were not sustainable after the withdrawal of funding provided by external partners due to lack of human, material, and operational resources. In 2017, after 13 years of an active IPC program, Senegal achieved an overall performance score of 15% in the IPCAT2 WHO tool [9], during an international IPC training workshop, showing lack of implementation. However, in the following five years, the overall performance increased to 52% of the minimum requirements with an increase in IPC program and guideline implementation, education and training, surveillance, and multimodal strategies. It should be noted that during this period, the majority of activities implemented were financed and directed by partners, instead of following a well-structured national action plan with well-defined objectives, strategies and indicators. This last assessment was carried out during a national workshop held in 2022, which also helped to develop a new IPC strategic plan for the period 2023–2027. However, these results need to be interpreted with caution, as it compares the full IPC requirements to the minimum requirements, and the latter was assessed by a self-assessment approach possibly overestimating the performance.

Mexico

In Mexico, the healthcare system is integrated by differ-
ent public and private institutions and different amend-
ments are currently being made to the model of care. The
healthcare costs were 539 USD per capita in 2020 [8].
There is no overarching national IPC strategy, but 15 IPC
initiatives are currently promoted including 6 regulatory
frameworks and 9 manuals or guidelines [10]. Examples
for these IPC initiatives are the national standard for epi-
demiological surveillance and a manual of standardized
procedures for hospital surveillance. The biggest chal-
lenges in patient safety experienced in Mexico are the
<table><caption>**Table 1** Summary of the eight core components for infection prevention and control programs by the World Health Organization (WHO) with focus on healthcare-facility level recommendations. Table adapted from https://www.who.int/teams/integrated-health-services/infection-prevention-control/core-components. IPC: infection prevention and control; AMR: antimicrobial resistance; HAI: healthcare-associated infections</caption><thead><tr><td></td><td>Core component by WHO</td><td>Recommendation and good practice statement</td></tr></thead><tbody><tr><td>1</td><td>IPC programs</td><td>IPC program with a dedicated, trained team should be in place in each acute health care facility for the purpose of preventing HAI and combating AMR through good IPC practices.</td></tr><tr><td>2</td><td>IPC guidelines</td><td>Evidence-based guidelines should be developed and implemented for the purpose of reducing HAI and AMR. The education and training of relevant health care workers on the guideline recommendations and the monitoring of adherence with guideline recommendations should be undertaken to achieve successful implementation</td></tr><tr><td>3</td><td>IPC education and training</td><td>IPC education should be in place for all health care workers by utilizing team- and task-based strategies that are participatory and include bedside and simulation training to reduce the risk of HAI and AMR.</td></tr><tr><td>4</td><td>Surveillance</td><td>Facility-based HAI surveillance should be performed to guide IPC interventions and detect outbreaks, including AMR surveillance with timely feedback of results to health care workers and stakeholders and through national networks.</td></tr><tr><td>5</td><td>Multimodal strategies</td><td>IPC activities using multimodal strategies should be implemented to improve practices and reduce HAI and AMR.</td></tr><tr><td>6</td><td>Monitoring /audit of IPC practices and feedback</td><td>Regular monitoring/audit and timely feedback of health care practices according to IPC standards should be performed to prevent and control HAI and AMR at the health care facility level. Feedback should be provided to all audited persons and relevant staff.</td></tr><tr><td>7</td><td>Workload, staffing and bed occupancy (acute health care facility only)</td><td>The following elements should be adhered to in order to reduce the risk of HAI and the spread of AMR:<br/>(1) Bed occupancy should not exceed the standard capacity of the facility.<br/>(2) Health care worker staffing levels should be adequately assigned according to patient workload.</td></tr><tr><td>8</td><td>Built environment, materials, and equipment for IPC at the facility level (acute health care facility only)</td><td>Patient care activities should be undertaken in a clean and/or hygienic environment that facilitates practices related to the prevention and control of HAI, as well as AMR, including all elements around the WASH infrastructure and services and the availability of appropriate IPC materials and equipment. Materials and equipment to perform appropriate hand hygiene should be readily available at the point of care.</td></tr></tbody></table>

development and implementation of collaborative strategies and the overall reduction of HAI, whose attributable case-fatality rate is estimated to be around 5%. Due to the complex structure of the healthcare system, there are multiple initiatives to improve IPC, but continuous and unified education and training as well as implementation remains a challenge. This challenge is mainly addressed by local efforts by institutions or universities, which are often not shared across the country or even disseminated in scientific journals. Monitoring of IPC tools and effects are variable and inconsistent, and actions are not always sustainable.

Chile

Chile's healthcare system is mostly based on public institutions, covering roughly two thirds of the yearly hospitalizations. The healthcare costs were 1,479 USD per capita in 2021 [8]. Already in 1983, Chile implemented a comprehensive national IPC program involving all public and private sectors. The IPC program became mandatory for all healthcare facilities in 1986. During the COVID-19

pandemic, Chile's healthcare system was heavily challenged by an increased number of outbreaks of HAI including outbreaks caused by multidrug-resistant bacteria, leading to a higher AMR incidence [11, 12]. Managing these outbreaks was challenging due to an unexpected high number of patients and healthcare workers affected by COVID-19 itself leading to staff shortages. Despite the great progress in reducing the incidence of HAI during the last 25 years [13–15], almost all types of HAI increased during the pandemic. Despite these challenges, Chile managed to train an eight-fold higher number of healthcare workers in IPC during 2020 compared to previous years. The training focused on standard precaution measures, the use of personal protective equipment and hand hygiene, but also covered more specific topics such as outbreak management and prevention of ventilator-associated pneumonia. In online and short face-to-face sessions, healthcare workers were educated and tools for the assessment of IPC needs were introduced. Feedback was provided to the healthcare providers every 4–6 months, also offering practical solutions.
<table><caption>**Table 1** Summary of the eight core components for infection prevention and control programs by the World Health Organization (WHO) with focus on healthcare-facility level recommendations. Table adapted from https://www.who.int/teams/integrated-health-services/infection-prevention-control/core-components. IPC: infection prevention and control; AMR: antimicrobial resistance; HAI: healthcare-associated infections</caption><thead><tr><td></td><td>Core component by WHO</td><td>Recommendation and good practice statement</td></tr></thead><tbody><tr><td>1</td><td>IPC programs</td><td>IPC program with a dedicated, trained team should be in place in each acute health care facility for the purpose of preventing HAI and combating AMR through good IPC practices.</td></tr><tr><td>2</td><td>IPC guidelines</td><td>Evidence-based guidelines should be developed and implemented for the purpose of reducing HAI and AMR. The education and training of relevant health care workers on the guideline recommendations and the monitoring of adherence with guideline recommendations should be undertaken to achieve successful implementation</td></tr><tr><td>3</td><td>IPC education and training</td><td>IPC education should be in place for all health care workers by utilizing team- and task-based strategies that are participatory and include bedside and simulation training to reduce the risk of HAI and AMR.</td></tr><tr><td>4</td><td>Surveillance</td><td>Facility-based HAI surveillance should be performed to guide IPC interventions and detect outbreaks, including AMR surveillance with timely feedback of results to health care workers and stakeholders and through national networks.</td></tr><tr><td>5</td><td>Multimodal strategies</td><td>IPC activities using multimodal strategies should be implemented to improve practices and reduce HAI and AMR.</td></tr><tr><td>6</td><td>Monitoring /audit of IPC practices and feedback</td><td>Regular monitoring/audit and timely feedback of health care practices according to IPC standards should be performed to prevent and control HAI and AMR at the health care facility level. Feedback should be provided to all audited persons and relevant staff.</td></tr><tr><td>7</td><td>Workload, staffing and bed occupancy (acute health care facility only)</td><td>The following elements should be adhered to in order to reduce the risk of HAI and the spread of AMR:<br/>(1) Bed occupancy should not exceed the standard capacity of the facility.<br/>(2) Health care worker staffing levels should be adequately assigned according to patient workload.</td></tr><tr><td>8</td><td>Built environment, materials, and equipment for IPC at the facility level (acute health care facility only)</td><td>Patient care activities should be undertaken in a clean and/or hygienic environment that facilitates practices related to the prevention and control of HAI, as well as AMR, including all elements around the WASH infrastructure and services and the availability of appropriate IPC materials and equipment. Materials and equipment to perform appropriate hand hygiene should be readily available at the point of care.</td></tr></tbody></table>

development and implementation of collaborative strategies and the overall reduction of HAI, whose attributable case-fatality rate is estimated to be around 5%. Due to the complex structure of the healthcare system, there are multiple initiatives to improve IPC, but continuous and unified education and training as well as implementation remains a challenge. This challenge is mainly addressed by local efforts by institutions or universities, which are often not shared across the country or even disseminated in scientific journals. Monitoring of IPC tools and effects are variable and inconsistent, and actions are not always sustainable.

## Chile

Chile's healthcare system is mostly based on public institutions, covering roughly two thirds of the yearly hospitalizations. The healthcare costs were 1,479 USD per capita in 2021 [8]. Already in 1983, Chile implemented a comprehensive national IPC program involving all public and private sectors. The IPC program became mandatory for all healthcare facilities in 1986. During the COVID-19

pandemic, Chile's healthcare system was heavily challenged by an increased number of outbreaks of HAI including outbreaks caused by multidrug-resistant bacteria, leading to a higher AMR incidence [11, 12]. Managing these outbreaks was challenging due to an unexpected high number of patients and healthcare workers affected by COVID-19 itself leading to staff shortages. Despite the great progress in reducing the incidence of HAI during the last 25 years [13–15], almost all types of HAI increased during the pandemic. Despite these challenges, Chile managed to train an eight-fold higher number of healthcare workers in IPC during 2020 compared to previous years. The training focused on standard precaution measures, the use of personal protective equipment and hand hygiene, but also covered more specific topics such as outbreak management and prevention of ventilator-associated pneumonia. In online and short face-to-face sessions, healthcare workers were educated and tools for the assessment of IPC needs were introduced. Feedback was provided to the healthcare providers every 4–6 months, also offering practical solutions.
<table><caption>**Table 2** Implementing the core components for infection prevention and control: Four country experiences from all over the world with focus on successes and challenges. USD: United States Dollar. IPC: infection prevention and control, HAI: healthcare-associated infections, COVID-19 Coronavirus Disease 2019</caption><thead><tr><th>Country</th><th>Healthcare costs per capita in USD (year) [8]</th><th>Global Health Security Index 2021 [50]</th><th>Established infection prevention and control program</th><th>Success</th><th>Challenges</th></tr></thead><tbody><tr><td>Senegal</td><td>77 (2020)</td><td>Overall: 32.8<br>Prevent: 11.0<br>Detect: 28.3<br>Respond: 41.3<br>Health: 14.6<br>Norms: 54.0<br>Risk: 47.8</td><td>National IPC program introduced in 2004</td><td>Overall performance of 52% of the minimum requirements. Well established IPC program at all levels of the healthcare system with a national budget</td><td>Lack of implementation and operational problems after more than a decade of active IPC program</td></tr><tr><td>Mexico</td><td>539 (2020)</td><td>Overall: 57.0<br>Prevent: 41.9<br>Detect: 54.3<br>Respond: 64.8<br>Health: 54.7<br>Norms: 68.1<br>Risk: 57.9</td><td>15 IPC initiatives: - 6 regulatory frameworks - 9 manuals or guidelines</td><td>Sentinel Surveillance System for HAI since 1997. Local and individual achievements by institutions or universities.</td><td>Development and implementation of collaborative strategies and overall reduction of HAI</td></tr><tr><td>Chile</td><td>1,479 (2021)</td><td>Overall: 56.2<br>Prevent: 47.2<br>Detect: 58.1<br>Respond: 59.5<br>Health: 52.9<br>Norms: 53.1<br>Risk: 66.2</td><td>National IPC program introduced in 1983 (mandatory since 1986)</td><td>Well established IPC program since decades.</td><td>COVID-19 pandemic with increase in HAI outbreaks and incidence of multidrug-resistant microorganisms while human resources were drastically reduced</td></tr><tr><td>Türkiye</td><td>395 (2020)</td><td>Overall: 50.0<br>Prevent: 51.1<br>Detect: 41.4<br>Respond: 36.6<br>Health: 53.9<br>Norms: 59.7<br>Risk: 57.2</td><td>National IPC program introduced in 2005<br>National action plan for prevention and control of antimicrobial resistance and sepsis introduced in 2019</td><td>Well established surveillance system for healthcare-associated infections and multidrug-resistant microorganisms.</td><td>Implementation of multimodal strategies, improving workload and staffing as well as bed occupancy</td></tr></tbody></table>

## Türkiye

In Türkiye, the healthcare system is covered by public funding by roughly 75% based on the number of beds available [16]. In 2020, healthcare costs were 395 USD per capita [8]. The most important patient safety challenge in Türkiye during the past years was the high incidence of HAI, illustrated by the rates of ventilator-associated events, catheter-associated urinary tract infections, and central line-associated bloodstream infections of 17.7, 5.0, and 5.7 per 1000 device-days, respectively, in 2008, which already decreased to 4.9, 1.6, and 2.8 per 1000 device-days, respectively, in 2017 [17]. In 2005, a structured IPC program has been put in place on a national scale, covering detailed IPC strategies, training, web-based surveillance, and promotion of hand hygiene [17]. Since then, the rate of HAI has been reduced significantly in hospitals of all sizes [17]. In addition to this success, the Ministry of Health focused on the implementation of more core components, such as a general system and culture change, training and education, as well as monitoring and feedback. This resulted in an advanced IPC level in 73.5% of all healthcare facilities as shown by the

IPCAF results in 2019 [18]. As remaining issues, multimodal strategies, workload, staffing, and bed occupancy were identified. In addition, AMR remains an endemic problem in Türkiye, with carbapenem-resistant Gram-negatives in 10–90% of all infecting isolates depending on the respective microorganisms and settings. To combat this, a national action plan for prevention and control of AMR and sepsis has been launched in 2019.

## Challenges in implementing ASP, perspectives from three countries and one region

The main pillar of combatting AMR remains ASP. The main objective of ASP is to improve clinical outcomes and patient safety by ensuring the right antimicrobial is given to the right patient at the right time, for the right duration, in a cost-effective manner [19]. The core elements of an ASP are: leadership commitment, accountability, pharmacy expertise, action to improve antibiotic use, monitoring and reporting of antibiotic use and AMR rates, and education [20]. An overview of the selected country and regional experiences is presented in Table 3.
<table><caption>**Table 2** Implementing the core components for infection prevention and control: Four country experiences from all over the world with focus on successes and challenges. USD: United States Dollar. IPC: infection prevention and control, HAI: healthcare-associated infections, COVID-19 Coronavirus Disease 2019</caption><thead><tr><th>Country</th><th>Healthcare costs per capita in USD (year) [8]</th><th>Global Health Security Index 2021 [50]</th><th>Established infection prevention and control program</th><th>Success</th><th>Challenges</th></tr></thead><tbody><tr><td>Senegal</td><td>77 (2020)</td><td>Overall: 32.8<br>Prevent: 11.0<br>Detect: 28.3<br>Respond: 41.3<br>Health: 14.6<br>Norms: 54.0<br>Risk: 47.8</td><td>National IPC program introduced in 2004</td><td>Overall performance of 52% of the minimum requirements. Well established IPC program at all levels of the healthcare system with a national budget</td><td>Lack of implementation and operational problems after more than a decade of active IPC program</td></tr><tr><td>Mexico</td><td>539 (2020)</td><td>Overall: 57.0<br>Prevent: 41.9<br>Detect: 54.3<br>Respond: 64.8<br>Health: 54.7<br>Norms: 68.1<br>Risk: 57.9</td><td>15 IPC initiatives: - 6 regulatory frameworks - 9 manuals or guidelines</td><td>Sentinel Surveillance System for HAI since 1997. Local and individual achievements by institutions or universities.</td><td>Development and implementation of collaborative strategies and overall reduction of HAI</td></tr><tr><td>Chile</td><td>1,479 (2021)</td><td>Overall: 56.2<br>Prevent: 47.2<br>Detect: 58.1<br>Respond: 59.5<br>Health: 52.9<br>Norms: 53.1<br>Risk: 66.2</td><td>National IPC program introduced in 1983 (mandatory since 1986)</td><td>Well established IPC program since decades.</td><td>COVID-19 pandemic with increase in HAI outbreaks and incidence of multidrug-resistant microorganisms while human resources were drastically reduced</td></tr><tr><td>Türkiye</td><td>395 (2020)</td><td>Overall: 50.0<br>Prevent: 51.1<br>Detect: 41.4<br>Respond: 36.6<br>Health: 53.9<br>Norms: 59.7<br>Risk: 57.2</td><td>National IPC program introduced in 2005<br>National action plan for prevention and control of antimicrobial resistance and sepsis introduced in 2019</td><td>Well established surveillance system for healthcare-associated infections and multidrug-resistant microorganisms.</td><td>Implementation of multimodal strategies, improving workload and staffing as well as bed occupancy</td></tr></tbody></table>

## Türkiye

In Türkiye, the healthcare system is covered by public funding by roughly 75% based on the number of beds available [16]. In 2020, healthcare costs were 395 USD per capita [8]. The most important patient safety challenge in Türkiye during the past years was the high incidence of HAI, illustrated by the rates of ventilator-associated events, catheter-associated urinary tract infections, and central line-associated bloodstream infections of 17.7, 5.0, and 5.7 per 1000 device-days, respectively, in 2008, which already decreased to 4.9, 1.6, and 2.8 per 1000 device-days, respectively, in 2017 [17]. In 2005, a structured IPC program has been put in place on a national scale, covering detailed IPC strategies, training, web-based surveillance, and promotion of hand hygiene [17]. Since then, the rate of HAI has been reduced significantly in hospitals of all sizes [17]. In addition to this success, the Ministry of Health focused on the implementation of more core components, such as a general system and culture change, training and education, as well as monitoring and feedback. This resulted in an advanced IPC level in 73.5% of all healthcare facilities as shown by the

IPCAF results in 2019 [18]. As remaining issues, multimodal strategies, workload, staffing, and bed occupancy were identified. In addition, AMR remains an endemic problem in Türkiye, with carbapenem-resistant Gram-negatives in 10–90% of all infecting isolates depending on the respective microorganisms and settings. To combat this, a national action plan for prevention and control of AMR and sepsis has been launched in 2019.

## Challenges in implementing ASP, perspectives from three countries and one region

The main pillar of combatting AMR remains ASP. The main objective of ASP is to improve clinical outcomes and patient safety by ensuring the right antimicrobial is given to the right patient at the right time, for the right duration, in a cost-effective manner [19]. The core elements of an ASP are: leadership commitment, accountability, pharmacy expertise, action to improve antibiotic use, monitoring and reporting of antibiotic use and AMR rates, and education [20]. An overview of the selected country and regional experiences is presented in Table 3.
<table><caption>**Table 3** Challenges in implementing an antibiotic stewardship program in four countries or regions. AMR: antimicrobial resistance, ASP: antibiotic stewardship program, TrACSS: Tracking AMR Country Self-Assessment Survey, IPC: infection prevention and control, EML: essential medicine list, NA: not available. TrACSS Country Report grading: A: none, B: limited, C: developed, D: demonstrated, E: sustained</caption><thead><tr><td>Country/Region</td><td>AMR burden</td><td>TrACSS 2022 Country reports [51]</td><td>Established antimicrobial stewardship program</td><td>Success</td><td>Challenges</td></tr></thead><tbody><tr><td>Thailand</td><td>Estimated to cause 88,000 infections, 3.24 additional hospitalizations, and 38,000 deaths in 2010 (21)</td><td>Training and Education on AMR in human healthcare sector: C<br>Monitoring antimicrobial consumption in human health C<br>National surveillance system for AMR in human health: D<br>IPC in human health: D<br>Adoption of AWaRe classification into national EML: D [52]</td><td>National AMR Surveillance Centre founded in 1998<br>Additional antibiotics smart use program added in 2007<br>Antibiotic awareness day introduced 2013</td><td>80% of hospitals have an established ASP</td><td>Evaluation of effectiveness of ASP is ongoing</td></tr><tr><td>Japan</td><td>Disability-adjusted life years due to bloodstream infections caused by nine major antimicrobial-resistant bacteria: 195.2/100,000 population (2021) [53]</td><td>Training and Education on AMR in human healthcare sector: E<br>Monitoring antimicrobial consumption in human health E<br>National surveillance system for AMR in human health: E<br>IPC in human health: E<br>Adoption of AWaRe classification into national EML: NA [54]</td><td>Action plan on antimicrobial resistance introduced in 2016<br>Updated national action plan on antimicrobial resistance in 2023</td><td>Immediate effect seen on use of antimicrobials</td><td>No sustainable effect, despite ongoing downward trend in use of antimicrobials</td></tr><tr><td>South Africa</td><td>According to the Global Burden of Disease study, sub-Saharan Africa had the highest mortality (23.7 deaths per 100,000) attributable to AMR (5).</td><td>Training and Education on AMR in human healthcare sector: C<br>Monitoring antimicrobial consumption in human health B<br>National surveillance system for AMR in human health: D<br>IPC in human health: B<br>Adoption of AWaRe classification into national EML: B [55]</td><td>Antimicrobial resistance National Strategy Framework introduced in 2014 (2014–2024)<br>Guidelines on Implementation of the Antimicrobial Strategy in South Africa: One Health Approach &amp; Governance (February 2017)<br>South African Antimicrobial Resistance National Strategy Framework; a one Health approach (2018–2024): Guidelines for the Prevention and Containment of AMR in South African Hospitals: One Health Approach and Governance 2018</td><td>Ministerial Advisory Board for Antimicrobial Resistance has been appointed by the Minister of Health, in 2015. A nationwide surveillance of antimicrobial use by a web-based application.</td><td>South Africa's national action plan against antibiotic resistant bacterial infections remains unfunded. The prevalence of infections caused by difficult-to-treat resistant Gram-negative bacteria (DTR-GNB) is rapidly increasing.</td></tr><tr><td>Latin America</td><td>Estimated to cause 338,000 deaths associated with and 84,300 deaths attributable to AMR in Latin America and the Caribbean (5).</td><td>NA</td><td>In 22 out of 33 countries in Latin America, 50% have not implemented an ASP yet, whereas in the other half, an ASP is currently being implemented.</td><td>Cost-effectiveness of ASP in Latin America are proven</td><td>Limited support by federal governments and local healthcare facility administrators to establish resources for ASP</td></tr></tbody></table>

Thailand

AMR was estimated to cause 88,000 infections resulting in 3.24 million additional hospitalization days and 38,000 deaths in Thailand in 2010 [21]. The first IPC program was launched in 1971, augmented by a national AMR Surveillance Centre in 1998. In 2007, the antibiotics

smart use program was started with the aim to reduce unnecessary antibiotic use for common self-limiting diseases, such as upper respiratory tract infections. To raise additional public awareness, an antibiotic awareness day has been introduced in 2013 [22]. The Thai strategy for tackling AMR includes six strategies covering governance
<table><caption>**Table 3** Challenges in implementing an antibiotic stewardship program in four countries or regions. AMR: antimicrobial resistance, ASP: antibiotic stewardship program, TrACSS: Tracking AMR Country Self-Assessment Survey, IPC: infection prevention and control, EML: essential medicine list, NA: not available. TrACSS Country Report grading: A: none, B: limited, C: developed, D: demonstrated, E: sustained</caption><thead><tr><td>Country/Region</td><td>AMR burden</td><td>TrACSS 2022 Country reports [51]</td><td>Established antimicrobial stewardship program</td><td>Success</td><td>Challenges</td></tr></thead><tbody><tr><td>Thailand</td><td>Estimated to cause 88,000 infections, 3.24 additional hospitalizations, and 38,000 deaths in 2010 (21)</td><td>Training and Education on AMR in human healthcare sector: C Monitoring antimicrobial consumption in human health C National surveillance system for AMR in human health: D IPC in human health: D Adoption of AWaRe classification into national EML: D [52]</td><td>National AMR Surveillance Centre founded in 1998 Additional antibiotics smart use program added in 2007 Antibiotic awareness day introduced 2013</td><td>80% of hospitals have an established ASP</td><td>Evaluation of effectiveness of ASP is ongoing</td></tr><tr><td>Japan</td><td>Disability-adjusted life years due to bloodstream infections caused by nine major antimicrobial-resistant bacteria: 195.2/100,000 population (2021) [53]</td><td>Training and Education on AMR in human healthcare sector: E Monitoring antimicrobial consumption in human health E National surveillance system for AMR in human health: E IPC in human health: E Adoption of AWaRe classification into national EML: NA [54]</td><td>Action plan on antimicrobial resistance introduced in 2016 Updated national action plan on antimicrobial resistance in 2023</td><td>Immediate effect seen on use of antimicrobials</td><td>No sustainable effect, despite ongoing downward trend in use of antimicrobials</td></tr><tr><td>South Africa</td><td>According to the Global Burden of Disease study, sub-Saharan Africa had the highest mortality (23.7 deaths per 100,000) attributable to AMR (5).</td><td>Training and Education on AMR in human healthcare sector: C Monitoring antimicrobial consumption in human health B National surveillance system for AMR in human health: D IPC in human health: B Adoption of AWaRe classification into national EML: B [55]</td><td>Antimicrobial resistance National Strategy Framework introduced in 2014 (2014–2024) Guidelines on Implementation of the Antimicrobial Strategy in South Africa: One Health Approach &amp; Governance (February 2017) South African Antimicrobial Resistance National Strategy Framework; a one Health approach (2018–2024): Guidelines for the Prevention and Containment of AMR in South African Hospitals: One Health Approach and Governance 2018</td><td>Ministerial Advisory Board for Antimicrobial Resistance has been appointed by the Minister of Health, in 2015. A nationwide surveillance of antimicrobial use by a web-based application.</td><td>South Africa's national action plan against antibiotic resistant bacterial infections remains unfunded. The prevalence of infections caused by difficult-to-treat resistant Gram-negative bacteria (DTR-GNB) is rapidly increasing.</td></tr><tr><td>Latin America</td><td>Estimated to cause 338,000 deaths associated with and 84,300 deaths attributable to AMR in Latin America and the Caribbean (5).</td><td>NA</td><td>In 22 out of 33 countries in Latin America, 50% have not implemented an ASP yet, whereas in the other half, an ASP is currently being implemented.</td><td>Cost-effectiveness of ASP in Latin America are proven</td><td>Limited support by federal governments and local healthcare facility administrators to establish resources for ASP</td></tr></tbody></table>

Thailand

AMR was estimated to cause 88,000 infections resulting in 3.24 million additional hospitalization days and 38,000 deaths in Thailand in 2010 [21]. The first IPC program was launched in 1971, augmented by a national AMR Surveillance Centre in 1998. In 2007, the antibiotics

smart use program was started with the aim to reduce unnecessary antibiotic use for common self-limiting diseases, such as upper respiratory tract infections. To raise additional public awareness, an antibiotic awareness day has been introduced in 2013 [22]. The Thai strategy for tackling AMR includes six strategies covering governance
mechanisms to implement and sustain AMR actions, AMR surveillance using a One Health approach, IPC and ASP, regulation of antimicrobial distribution, public awareness, and antimicrobial use in agriculture and animals [23]. As a result of these efforts, more than 80% of Thai hospitals have an established, multi-disciplinary ASP [24]. Diagnostic stewardship is more frequently performed in hospitals with a broader expertise in antimicrobial stewardship. The evaluation of the effectiveness of these programs is still ongoing.

## Japan

As of 2016, oral antimicrobials accounted for >90% of antimicrobials prescribed over the past decade in Japan; and the younger generation, particularly those aged ≤15 years, were prescribed more antimicrobials than adults [25]. As a reaction to it, a national AMR action plan was introduced in 2016 focusing on clinical guidance for acute respiratory tract infections and diarrhea, financial incentives for pediatricians and family physicians, and communication of risks to the public. By focusing on the first two, an immediate reduction in the outpatient antimicrobial prescription rate was observed [26]. Nevertheless, the effect was not sustainable. Even though a steady downward trend could be shown in the overall use of antimicrobials [25], the targeted reduction of 33% was not achieved until 2020. It remains unknown to what extent this change was based on the reduction of inappropriate prescribing. To better understand the appropriateness of antimicrobial use in Japan, more detailed quantitative and qualitative investigations and surveillance systems are needed as a next step. The updated national action plan was published in 2023. The government of Japan continues to tackle the AMR issues through synergetic collaboration with multiple sectors, namely by strengthening and implementing integrated One Health surveillance on humans, animals, food, and the environment. Furthermore, in addition to human health and the food production sector, the updated national action plan also emphasizes ASP in veterinary medicine [27].

## South Africa

South Africa approved a national AMR Strategy Framework (2014–2024) and consecutively implemented the following key components: definition of measurable goals to track progress and evaluate the effectiveness, a pharmacist-driven prospective audit and feedback strategy, prescription audits and usage, antimicrobial formulary management, IPC programs, and clinical workforce education [28]. The public healthcare that serves 86% of the population in South Africa still mostly uses a paper-based system. A situational analysis was conducted on antimicrobial utilization and policies. Public sector data were obtained from contracting data arising from tenders from

wholesalers where the National Department of Health solicits bids from suppliers. Antimicrobial use increased from 2013 to 2018, especially oral broad-spectrum penicillins, oral and intravenous cephalosporins, and certain reserve antibiotics, such as daptomycin, linezolid, and tigecycline. The latter is partly explainable by the emergence of multidrug-resistant tuberculosis requesting therapy with these antibiotics. Unfortunately, a sub-optimal compliance to the strategy by the public healthcare sector has been observed [29]. As a result, the creation of interdisciplinary teams including microbiologists, infection preventionists, nurses, pharmacists, and infectious diseases specialists were supported. Adapted to the local characteristics, a web-based application to collect data on antimicrobial utilization has been developed, improving the overall surveillance of antibiotic consumption [30]. Future targets to improve antimicrobial usage were also identified: use of watch antibiotics, surgical prophylaxis, and extended antimicrobial prophylaxis amongst others.

## Latin America

Data from cross-sectional studies showed that ASPs in Latin American healthcare facilities currently face various problems, including limited leadership support, and dedicated, multi-disciplinary staff for an effective ASP including infectious disease trained pharmacists [31–33]. Furthermore, cultural and behavioral determinants pose a risk to sustainable ASP implementation as power distance and hierarchical relationships limit integration of pharmacists and non-physician roles in AS activities. While ASP are proven to decrease antimicrobial consumption on a facility level [34], data on national levels is missing for most Latin American countries. Even though studies support the (cost-) effectiveness of ASPs in Latin American countries [35, 36], further actions from the federal governments are needed to create the necessary resources to establish and implement effective ASPs, and for hospital leaders to make initial investments to set effective ASPs in motion. Several targets for improving antibiotic use in acute care hospitals have been identified including treatment of HAIs in the ICU, empiric treatments, adherence to treatment guidelines, and use of broad-spectrum antibiotics [37]. Given the increase in carbapenem resistance among Gram-negatives in the region in recent decades there is an urgent need to strengthen both IPC and ASP in hospitals in the region.

## Discussion

The implementation of the WHO IPC core components and ASP has been recognized as an essential step to battle the emerging burden of HAI and AMR. Experts from different countries and regions with different income levels gave their insights into their successes and problems in the implementation of national IPC programs. Even
mechanisms to implement and sustain AMR actions, AMR surveillance using a One Health approach, IPC and ASP, regulation of antimicrobial distribution, public awareness, and antimicrobial use in agriculture and animals [23]. As a result of these efforts, more than 80% of Thai hospitals have an established, multi-disciplinary ASP [24]. Diagnostic stewardship is more frequently performed in hospitals with a broader expertise in antimicrobial stewardship. The evaluation of the effectiveness of these programs is still ongoing.

## Japan

As of 2016, oral antimicrobials accounted for >90% of antimicrobials prescribed over the past decade in Japan; and the younger generation, particularly those aged ≤15 years, were prescribed more antimicrobials than adults [25]. As a reaction to it, a national AMR action plan was introduced in 2016 focusing on clinical guidance for acute respiratory tract infections and diarrhea, financial incentives for pediatricians and family physicians, and communication of risks to the public. By focusing on the first two, an immediate reduction in the outpatient antimicrobial prescription rate was observed [26]. Nevertheless, the effect was not sustainable. Even though a steady downward trend could be shown in the overall use of antimicrobials [25], the targeted reduction of 33% was not achieved until 2020. It remains unknown to what extent this change was based on the reduction of inappropriate prescribing. To better understand the appropriateness of antimicrobial use in Japan, more detailed quantitative and qualitative investigations and surveillance systems are needed as a next step. The updated national action plan was published in 2023. The government of Japan continues to tackle the AMR issues through synergetic collaboration with multiple sectors, namely by strengthening and implementing integrated One Health surveillance on humans, animals, food, and the environment. Furthermore, in addition to human health and the food production sector, the updated national action plan also emphasizes ASP in veterinary medicine [27].

## South Africa

South Africa approved a national AMR Strategy Framework (2014–2024) and consecutively implemented the following key components: definition of measurable goals to track progress and evaluate the effectiveness, a pharmacist-driven prospective audit and feedback strategy, prescription audits and usage, antimicrobial formulary management, IPC programs, and clinical workforce education [28]. The public healthcare that serves 86% of the population in South Africa still mostly uses a paper-based system. A situational analysis was conducted on antimicrobial utilization and policies. Public sector data were obtained from contracting data arising from tenders from

wholesalers where the National Department of Health solicits bids from suppliers. Antimicrobial use increased from 2013 to 2018, especially oral broad-spectrum penicillins, oral and intravenous cephalosporins, and certain reserve antibiotics, such as daptomycin, linezolid, and tigecycline. The latter is partly explainable by the emergence of multidrug-resistant tuberculosis requesting therapy with these antibiotics. Unfortunately, a sub-optimal compliance to the strategy by the public healthcare sector has been observed [29]. As a result, the creation of interdisciplinary teams including microbiologists, infection preventionists, nurses, pharmacists, and infectious diseases specialists were supported. Adapted to the local characteristics, a web-based application to collect data on antimicrobial utilization has been developed, improving the overall surveillance of antibiotic consumption [30]. Future targets to improve antimicrobial usage were also identified: use of watch antibiotics, surgical prophylaxis, and extended antimicrobial prophylaxis amongst others.

## Latin America

Data from cross-sectional studies showed that ASPs in Latin American healthcare facilities currently face various problems, including limited leadership support, and dedicated, multi-disciplinary staff for an effective ASP including infectious disease trained pharmacists [31–33]. Furthermore, cultural and behavioral determinants pose a risk to sustainable ASP implementation as power distance and hierarchical relationships limit integration of pharmacists and non-physician roles in AS activities. While ASP are proven to decrease antimicrobial consumption on a facility level [34], data on national levels is missing for most Latin American countries. Even though studies support the (cost-) effectiveness of ASPs in Latin American countries [35, 36], further actions from the federal governments are needed to create the necessary resources to establish and implement effective ASPs, and for hospital leaders to make initial investments to set effective ASPs in motion. Several targets for improving antibiotic use in acute care hospitals have been identified including treatment of HAIs in the ICU, empiric treatments, adherence to treatment guidelines, and use of broad-spectrum antibiotics [37]. Given the increase in carbapenem resistance among Gram-negatives in the region in recent decades there is an urgent need to strengthen both IPC and ASP in hospitals in the region.

## Discussion

The implementation of the WHO IPC core components and ASP has been recognized as an essential step to battle the emerging burden of HAI and AMR. Experts from different countries and regions with different income levels gave their insights into their successes and problems in the implementation of national IPC programs. Even
though their conditions differ significantly, from a well-established IPC program since decades in Chile to a bundle of different IPC initiatives in Mexico, most of them face problems in the continued implementation process. Starting with the sustainability of the programs and the financing in Senegal, other reports included the lack of coordination and issues of different initiatives in Mexico, and the COVID-19 pandemic challenging existing IPC structures due to increased workload while being understaffed at the same time in Chile. ASP as an integral part of any program to combat AMR were introduced in the last 15 years in several presenting countries. However, the effect of these programs is difficult to measure and interpret, as AMR is known to be influenced not only by human consumption of antibiotics, but also antibiotic use in livestock and environmental factors, such as wastewater treatment [38]. This is illustrated by the Japanese experience, where an immediate effect on human antibiotic consumption could be shown after the introduction of interventions, unfortunately without a sustainable effect. In South Africa, despite the extensive surveillance of antimicrobial use, an increase of antibiotic consumption was observed during the following five years. The reason for this remains unknown but is demanding further actions. In some regions of the world, essential parameters for estimating the effect of ASP on AMR are not routinely assessed, such as antimicrobial consumption, which makes it even more difficult to evaluate the effect of individual measures in these specific settings.

In the last decade, guidelines have been published by the WHO [39], the Centers for Disease Control and Prevention (CDC) [40], and the European Centre for Disease Prevention and control (ECDC) [41] on the requirements of effective ASP and IPC programs. However, the implementation of these guidelines remains a major challenge as the resources available depend on the individual setting. The basis for the successful implementation of IPC programs and ASP is the support of political and healthcare leaders through legislation and processes that facilitate creation of the necessary resources for these programs. Coordination of implementation within a country, but also within a healthcare institution, are key to efficiently use the available human and financial resources. Dedicated healthcare personnel with different skill sets are essential for effective IPC programs and ASP. While the introduction of automated or non-automated surveillance tools seems feasible in most settings, the implementation of more time-consuming activities, such as education and training, behavior change or multimodal strategies, remain challenging. However, these activities are key to spread knowledge about IPC and ASP among healthcare workers and get them engaged and motivated. There is a clear need to expand the clinical pharmacy workforce in the inpatient setting as

pharmacists have unique skill sets that are complementary to the expertise physicians have for optimal management of infectious diseases.

In contrast to hospital-based IPC programs, ASP face broader issues. As 80–90% of the antibiotic consumption takes place in the outpatient setting [42], there is a large, unmet need for promoting ASP in the ambulatory sector. Broad approaches for implementation are known in this setting, ranging from education of individual patients and general practitioners to electronic decision support tools to facilitate appropriate treatment decisions, and general education of the public [43]. As the targeted population is very broad, low participation and general time pressure are limiting factors of these approaches. Promising interventions are the introduction of small quality circles among primary care physicians, and the strengthening of the patient-physician relationship by point-of-care-testing and improved communication skills [44, 45].

Implementation science is still a young and developing field. Nevertheless, recent studies have shown that with the help of implementation specialists, evidence-based measures can be successfully introduced with increased sustainability [46, 47]. However, implementation is not a “one size fits all” model, as specific needs and expectations of involved healthcare personnel as well as setting specific characteristics need to be taken into account. As an example, the successful implementation of an IPC bundle to reduce central venous catheter-blood stream infections in Michigan, United States, could not be reproduced in another study conducted in England due to differences in the implementation process [48, 49].

In conclusion, the implementation of effective IPC and ASP guidelines remains a major challenge at all levels. Together, we can all work to reduce the burden of HAI and AMR. By enforcing sustained implementation by dedicated healthcare personnel with a broad skill set, a reduction in HAIs and multidrug-resistant pathogens can be achieved and, as a result, ultimately improve patient safety.

### Abbreviations

AMR antimicrobial resistance

ASP antibiotic stewardship program

CDC Centers for Disease Prevention and Control

ECDC European Centre for Disease Prevention and Control

EML essential medicine list

HAI healthcare-associated infections

IPC infection prevention and control

TrACSS Tracking AMR Country Self-Assessment Survey

WHO World Health Organization

### Acknowledgements

We thank the organizers of the 5th Global Ministerial Summit on Patient Safety. We thank all the speakers and participants for stimulating discussion. VF would like to acknowledge the CDC for funding to evaluate infection prevention and control and antimicrobial stewardship programs in hospitals in Latin America, and their collaborators at the Ministries of Health and healthcare facilities for participation in these projects.
though their conditions differ significantly, from a well-established IPC program since decades in Chile to a bundle of different IPC initiatives in Mexico, most of them face problems in the continued implementation process. Starting with the sustainability of the programs and the financing in Senegal, other reports included the lack of coordination and issues of different initiatives in Mexico, and the COVID-19 pandemic challenging existing IPC structures due to increased workload while being understaffed at the same time in Chile. ASP as an integral part of any program to combat AMR were introduced in the last 15 years in several presenting countries. However, the effect of these programs is difficult to measure and interpret, as AMR is known to be influenced not only by human consumption of antibiotics, but also antibiotic use in livestock and environmental factors, such as wastewater treatment [38]. This is illustrated by the Japanese experience, where an immediate effect on human antibiotic consumption could be shown after the introduction of interventions, unfortunately without a sustainable effect. In South Africa, despite the extensive surveillance of antimicrobial use, an increase of antibiotic consumption was observed during the following five years. The reason for this remains unknown but is demanding further actions. In some regions of the world, essential parameters for estimating the effect of ASP on AMR are not routinely assessed, such as antimicrobial consumption, which makes it even more difficult to evaluate the effect of individual measures in these specific settings.

In the last decade, guidelines have been published by the WHO [39], the Centers for Disease Control and Prevention (CDC) [40], and the European Centre for Disease Prevention and control (ECDC) [41] on the requirements of effective ASP and IPC programs. However, the implementation of these guidelines remains a major challenge as the resources available depend on the individual setting. The basis for the successful implementation of IPC programs and ASP is the support of political and healthcare leaders through legislation and processes that facilitate creation of the necessary resources for these programs. Coordination of implementation within a country, but also within a healthcare institution, are key to efficiently use the available human and financial resources. Dedicated healthcare personnel with different skill sets are essential for effective IPC programs and ASP. While the introduction of automated or non-automated surveillance tools seems feasible in most settings, the implementation of more time-consuming activities, such as education and training, behavior change or multimodal strategies, remain challenging. However, these activities are key to spread knowledge about IPC and ASP among healthcare workers and get them engaged and motivated. There is a clear need to expand the clinical pharmacy workforce in the inpatient setting as

pharmacists have unique skill sets that are complementary to the expertise physicians have for optimal management of infectious diseases.

In contrast to hospital-based IPC programs, ASP face broader issues. As 80–90% of the antibiotic consumption takes place in the outpatient setting [42], there is a large, unmet need for promoting ASP in the ambulatory sector. Broad approaches for implementation are known in this setting, ranging from education of individual patients and general practitioners to electronic decision support tools to facilitate appropriate treatment decisions, and general education of the public [43]. As the targeted population is very broad, low participation and general time pressure are limiting factors of these approaches. Promising interventions are the introduction of small quality circles among primary care physicians, and the strengthening of the patient-physician relationship by point-of-care-testing and improved communication skills [44, 45].

Implementation science is still a young and developing field. Nevertheless, recent studies have shown that with the help of implementation specialists, evidence-based measures can be successfully introduced with increased sustainability [46, 47]. However, implementation is not a “one size fits all” model, as specific needs and expectations of involved healthcare personnel as well as setting specific characteristics need to be taken into account. As an example, the successful implementation of an IPC bundle to reduce central venous catheter-blood stream infections in Michigan, United States, could not be reproduced in another study conducted in England due to differences in the implementation process [48, 49].

In conclusion, the implementation of effective IPC and ASP guidelines remains a major challenge at all levels. Together, we can all work to reduce the burden of HAI and AMR. By enforcing sustained implementation by dedicated healthcare personnel with a broad skill set, a reduction in HAIs and multidrug-resistant pathogens can be achieved and, as a result, ultimately improve patient safety.

### Abbreviations

<table><tr><td>AMR</td><td>antimicrobial resistance</td></tr><tr><td>ASP</td><td>antibiotic stewardship program</td></tr><tr><td>CDC</td><td>Centers for Disease Prevention and Control</td></tr><tr><td>ECDC</td><td>European Centre for Disease Prevention and Control</td></tr><tr><td>EML</td><td>essential medicine list</td></tr><tr><td>HAI</td><td>healthcare-associated infections</td></tr><tr><td>IPC</td><td>infection prevention and control</td></tr><tr><td>TrACSS</td><td>Tracking AMR Country Self-Assessment Survey</td></tr><tr><td>WHO</td><td>World Health Organization</td></tr></table>

### Acknowledgements

We thank the organizers of the 5th Global Ministerial Summit on Patient Safety. We thank all the speakers and participants for stimulating discussion. VF would like to acknowledge the CDC for funding to evaluate infection prevention and control and antimicrobial stewardship programs in hospitals in Latin America, and their collaborators at the Ministries of Health and healthcare facilities for participation in these projects.
**Authors' contributions**

ACB and MGH conceived and drafted the manuscript, EA, AA, VF, KJ, BN, HMV, FO, NS, GD, SG, DP, and CG provided important intellectual content, NB and SH provided an extensive review of the manuscript, all authors have read and approved the final version of the manuscript.

**Funding**

This paper was part of the HUG's mandate in the context of the 5th Global Ministerial Summit on Patient Safety. The Summit was organized by the Federal Office of Public Health of Switzerland.

**Data Availability**

Not applicable.

**Declarations**

**Ethics approval and consent to participate**

Not applicable.

**Consent for publication**

Not applicable.

**Competing interests**

All authors declare no competing interests relevant for this article.

**Author details**

¹Infection Control Program, Faculty of Medicine, Geneva University Hospitals, WHO Collaborating Center, Rue Gabrielle-Perret-Gentil 4, Genève 1205, Switzerland

²JAME UMR 1137, INSERM, Université Paris-Cité, Paris, France

³Department of Infectious Diseases and Clinical Microbiology, Faculty of Medicine, Ankara Yildirim Beyazit University, Ankara, Türkiye

⁴Division of Infectious Diseases, Faculty of Medicine, Thammasat University Hospital, Pathum Thani, Thailand

⁵Communicable Disease Division, Federal Office of Public Health FOPH, Bern, Switzerland

⁶Department of Medicine, Division of Infectious Diseases, Johns Hopkins University School of Medicine, Baltimore, USA

⁷Department of Virology, Tohoku University Graduate School of Medicine, Sendai, Japan

⁸Department of Healthcare Epidemiology, School of Public Health, Kyoto University, Kyoto, Japan

⁹Infection Control and Patient Safety, WHO Afro Consultant, Brazzaville, Congo Republic

¹⁰Department of Public Health. University Center of Health Sciences, University of Guadalajara, Guadalajara, Mexico

¹¹Department of Quality of Healthcare and Patient Safety, National Infection Control Program, Ministry of Health of Chile, Santiago, Chile

¹²Departement of Pharmacology, Faculty of Health Sciences, University of Pretoria, Pretoria, South Africa

Received: 31 August 2023 / Accepted: 25 November 2023

Published online: 08 February 2024

**References**

1. World Health Organization (WHO). Global report on infection prevention and control. 2022.

2. Cassini A, Colzani E, Pini A, Mangen MJ, Plass D, McDonald SA et al. Impact of infectious Diseases on population health using incidence-based disability-adjusted life years (DALYs): results from the Burden of Communicable Diseases in Europe study, European Union and European Economic Area countries, 2009 to 2013. Euro Surveill. 2018;23(16):17.

3. Cassini A, Plachouras D, Eckmanns T, Abu Sin M, Blank HP, Ducomble T, et al. Burden of six Healthcare-Associated Infections on European Population Health: estimating incidence-based disability-adjusted life years through a Population prevalence-based Modelling Study. PLoS Med. 2016;13(10):e1002150.

4. World Health Organization (WHO). Ten threats to global health in 2019 [Available from: https://www.who.int/news-room/spotlight/ten-threats-to-global-health-in-2019].

5. Antimicrobial Resistance Collaborators. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet. 2022;399(10325):629–55.

6. World Health Organization (WHO). Global Strategy on Infection Prevention and Control. 2022.

7. World Health Organization (WHO). Minimum Requirements for infection prevention and control programmes. 2019.

8. World Health Organization (WHO). Global Health Expenditure Database [Available from: https://apps.who.int/nha/database/Select/Indicators/en].

9. World Health Organization (WHO). Assessment tool of the minimum requirements for infection prevention and control programmes at the national level. 2021.

10. Organización Panamericana de la Salud. Estado actual de la aplicación de los componentes básicos de prevención y control de infecciones en la Región de las Américas. 2022.

11. Allel K, Peters A, Conejeros J, Martinez JRW, Spencer-Sandino M, Riquelme-Neira R, et al. Antibiotic consumption during the Coronavirus Disease 2019 pandemic and emergence of carbapenemase-producing Klebsiella pneumoniae lineages among inpatients in a Chilean hospital: a Time-Series Study and Phylogenomic Analysis. Clin Infect Dis. 2023;77(Suppl 1):20–S8.

12. Araos R, Smith RM, Styczynski A, Sanchez F, Acevedo J, Maureira L, et al. High Burden of Intestinal colonization with antimicrobial-resistant Bacteria in Chile: an Antibiotic Resistance in communities and hospitals (ARCH) study. Clin Infect Dis. 2023;77(Suppl 1):75–S81.

13. Unidad de IAAS del Ministerio de Salud. Informe de Vigilancia de Infecciones Asociadas a la Atención en salud 2020. 2020.

14. Departamento de Epidemiología. Departamento de Calidad y Seguridad de la Atención. Informe epidemiológico: Características del personal de salud confirmados y probabilidades de COVID-19. 2020.

15. Ministerio de Salud Programa Nacional de control de Infecciones (Orsini M, PM, Quintanilla M, Lara C.)., Informe de Brotes Asociados a la Atención de Salud (IAAS) por SARS-CoV-2. 2021.

16. Atun R, Aydin S, Chakraborty S, Sumer S, Aran M, Gurol I, et al. Universal health coverage in Turkey: enhancement of equity. Lancet. 2013;382(9886):65–99.

17. Gozel MGHC, Gozel EY, Batir E, McLaws ML, Mese EA. National Infection Control Program in Turkey: the healthcare associated infection rate experiences over 10 years. Am J Infect Control. 2021;49(7):885–92.

18. Azak E, Sertcelik A, Ersoz G, Celebi G, Eser F, Batirel A, et al. Evaluation of the implementation of WHO Infection prevention and control core components in Turkish health care facilities: results from a WHO Infection prevention and control assessment framework (IPCAF)-based survey. Antimicrob Resist Infect Control. 2023;12(1):11.

19. Levy-Hara G, Amabile-Cuevas CF, Gould I, Hutchinson J, Abbo L, Saxynger L, et al. Ten commandments for the appropriate use of antibiotics by the practicing physician in an outpatient setting. Front Microbiol. 2011;2:230.

20. Centers for Disease Control and Prevention (CDC). Core Elements of Antibiotic Stewardship 2023 [Available from: https://www.cdc.gov/antibiotic-use/core-elements/index.html].

21. Phumart P, Phodha T, Thamlikitkul V, Riewpaiboon A, Prakongsai P, Limwattananon S. Health and Economic Impacts of Antimicrobial Resistant Infections in Thailand: a preliminary study. Journal of Health Services Research & Policy; 2012;6:352–60

22. Huttner B, Saam M, Moja L, Mah K, Sprenger M, Harbarth S, et al. How to improve antibiotic awareness campaigns: findings of a WHO global survey. BMJ Glob Health. 2019;4(3):e001239.

23. Sumpradit N, Wongkongkathep S, Malathum K, Janejai N, Paveenkittiporn W, Yingyong T, et al. Thailand's national strategic plan on antimicrobial resistance: progress and challenges. Bull World Health Organ. 2021;99(9):661–73.

24. Patel PK, Watari T, Todd Greene M, Fowler KE, Ratz D, Saint S, et al. The current state of antimicrobial and urine culture stewardship in Thailand: results from a National Survey. American Journal of Infection Control; 2023 (online ahead of print).

25. AMR clinical reference center. Statistics on antimicrobial use by age 2013–2020 (年齡別抗菌藥使量統計). 2021.

26. Jindai K, Itaya T, Ogawa Y, Kamitani T, Fukuhara S, Goto M, Yamamoto Y. Decline in oral antimicrobial prescription in the outpatient setting after nationwide implementation of financial incentives and provider education: an interrupted time-series analysis. Infect Control Hosp Epidemiol. 2023;44(2):253–9.
**Authors' contributions**

ACB and MGH conceived and drafted the manuscript, EA, AA, VF, KJ, BN, HMV, FO, NS, GD, SG, DP, and CG provided important intellectual content, NB and SH provided an extensive review of the manuscript, all authors have read and approved the final version of the manuscript.

**Funding**

This paper was part of the HUG's mandate in the context of the 5th Global Ministerial Summit on Patient Safety. The Summit was organized by the Federal Office of Public Health of Switzerland.

**Data Availability**

Not applicable.

**Declarations**

**Ethics approval and consent to participate**

Not applicable.

**Consent for publication**

Not applicable.

**Competing interests**

All authors declare no competing interests relevant for this article.

**Author details**

¹Infection Control Program, Faculty of Medicine, Geneva University Hospitals, WHO Collaborating Center, Rue Gabrielle-Perret-Gentil 4, Genève 1205, Switzerland

²JAME UMR 1137, INSERM, Université Paris-Cité, Paris, France

³Department of Infectious Diseases and Clinical Microbiology, Faculty of Medicine, Ankara Yildirim Beyazit University, Ankara, Türkiye

⁴Division of Infectious Diseases, Faculty of Medicine, Thammasat University Hospital, Pathum Thani, Thailand

⁵Communicable Disease Division, Federal Office of Public Health FOPH, Bern, Switzerland

⁶Department of Medicine, Division of Infectious Diseases, Johns Hopkins University School of Medicine, Baltimore, USA

⁷Department of Virology, Tohoku University Graduate School of Medicine, Sendai, Japan

⁸Department of Healthcare Epidemiology, School of Public Health, Kyoto University, Kyoto, Japan

⁹Infection Control and Patient Safety, WHO Afro Consultant, Brazzaville, Congo Republic

¹⁰Department of Public Health. University Center of Health Sciences, University of Guadalajara, Guadalajara, Mexico

¹¹Department of Quality of Healthcare and Patient Safety, National Infection Control Program, Ministry of Health of Chile, Santiago, Chile

¹²Departement of Pharmacology, Faculty of Health Sciences, University of Pretoria, Pretoria, South Africa

Received: 31 August 2023 / Accepted: 25 November 2023

Published online: 08 February 2024

**References**

1. World Health Organization (WHO). Global report on infection prevention and control. 2022.

2. Cassini A, Colzani E, Pini A, Mangen MJ, Plass D, McDonald SA et al. Impact of infectious Diseases on population health using incidence-based disability-adjusted life years (DALYs): results from the Burden of Communicable Diseases in Europe study, European Union and European Economic Area countries, 2009 to 2013. Euro Surveill. 2018;23(16):17.

3. Cassini A, Plachouras D, Eckmanns T, Abu Sin M, Blank HP, Ducomble T, et al. Burden of six Healthcare-Associated Infections on European Population Health: estimating incidence-based disability-adjusted life years through a Population prevalence-based Modelling Study. PLoS Med. 2016;13(10):e1002150.

4. World Health Organization (WHO). Ten threats to global health in 2019 [Available from: https://www.who.int/news-room/spotlight/ten-threats-to-global-health-in-2019].

5. Antimicrobial Resistance Collaborators. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet. 2022;399(10325):629–55.

6. World Health Organization (WHO). Global Strategy on Infection Prevention and Control. 2022.

7. World Health Organization (WHO). Minimum Requirements for infection prevention and control programmes. 2019.

8. World Health Organization (WHO). Global Health Expenditure Database [Available from: https://apps.who.int/nha/database/Select/Indicators/en].

9. World Health Organization (WHO). Assessment tool of the minimum requirements for infection prevention and control programmes at the national level. 2021.

10. Organización Panamericana de la Salud. Estado actual de la aplicación de los componentes básicos de prevención y control de infecciones en la Región de las Américas. 2022.

11. Allel K, Peters A, Conejeros J, Martinez JRW, Spencer-Sandino M, Riquelme-Neira R, et al. Antibiotic consumption during the Coronavirus Disease 2019 pandemic and emergence of carbapenemase-producing Klebsiella pneumoniae lineages among inpatients in a Chilean hospital: a Time-Series Study and Phylogenomic Analysis. Clin Infect Dis. 2023;77(Suppl 1):20–S8.

12. Araos R, Smith RM, Styczynski A, Sanchez F, Acevedo J, Maureira L, et al. High Burden of Intestinal colonization with antimicrobial-resistant Bacteria in Chile: an Antibiotic Resistance in communities and hospitals (ARCH) study. Clin Infect Dis. 2023;77(Suppl 1):75–S81.

13. Unidad de IAAS del Ministerio de Salud. Informe de Vigilancia de Infecciones Asociadas a la Atención en salud 2020. 2020.

14. Departamento de Epidemiología. Departamento de Calidad y Seguridad de la Atención. Informe epidemiológico: Características del personal de salud confirmados y probabilidades de COVID-19. 2020.

15. Ministerio de Salud Programa Nacional de control de Infecciones (Orsini M, PM, Quintanilla M, Lara C.)., Informe de Brotes Asociados a la Atención de Salud (IAAS) por SARS-CoV-2. 2021.

16. Atun R, Aydin S, Chakraborty S, Sumer S, Aran M, Gurol I, et al. Universal health coverage in Turkey: enhancement of equity. Lancet. 2013;382(9886):65–99.

17. Gozel MGHC, Gozel EY, Batir E, McLaws ML, Mese EA. National Infection Control Program in Turkey: the healthcare associated infection rate experiences over 10 years. Am J Infect Control. 2021;49(7):885–92.

18. Azak E, Sertcelik A, Ersoz G, Celebi G, Eser F, Batirel A, et al. Evaluation of the implementation of WHO Infection prevention and control core components in Turkish health care facilities: results from a WHO Infection prevention and control assessment framework (IPCAF)-based survey. Antimicrob Resist Infect Control. 2023;12(1):11.

19. Levy-Hara G, Amabile-Cuevas CF, Gould I, Hutchinson J, Abbo L, Saxynger L, et al. Ten commandments for the appropriate use of antibiotics by the practicing physician in an outpatient setting. Front Microbiol. 2011;2:230.

20. Centers for Disease Control and Prevention (CDC). Core Elements of Antibiotic Stewardship 2023 [Available from: https://www.cdc.gov/antibiotic-use/core-elements/index.html].

21. Phumart P, Phodha T, Thamlikitkul V, Riewpaiboon A, Prakongsai P, Limwattananon S. Health and Economic Impacts of Antimicrobial Resistant Infections in Thailand: a preliminary study. Journal of Health Services Research & Policy; 2012;6:352–60

22. Huttner B, Saam M, Moja L, Mah K, Sprenger M, Harbarth S, et al. How to improve antibiotic awareness campaigns: findings of a WHO global survey. BMJ Glob Health. 2019;4(3):e001239.

23. Sumpradit N, Wongkongkathep S, Malathum K, Janejai N, Paveenkittiporn W, Yingyong T, et al. Thailand's national strategic plan on antimicrobial resistance: progress and challenges. Bull World Health Organ. 2021;99(9):661–73.

24. Patel PK, Watari T, Todd Greene M, Fowler KE, Ratz D, Saint S, et al. The current state of antimicrobial and urine culture stewardship in Thailand: results from a National Survey. American Journal of Infection Control; 2023 (online ahead of print).

25. AMR clinical reference center. Statistics on antimicrobial use by age 2013–2020 (年齡別抗菌藥使量統計). 2021.

26. Jindai K, Itaya T, Ogawa Y, Kamitani T, Fukuhara S, Goto M, Yamamoto Y. Decline in oral antimicrobial prescription in the outpatient setting after nationwide implementation of financial incentives and provider education: an interrupted time-series analysis. Infect Control Hosp Epidemiol. 2023;44(2):253–9.
27. The Government of Japan. National Action Plan on Antimicrobial Resistance (AMR) 2023–2027. 2023.

28. Brink AJ, Messina AP, Feldman C, Richards GA, Becker PJ, Goff DA, et al. Antimicrobial stewardship across 47 South African hospitals: an implementation study. Lancet Infect Dis. 2016;16(9):1017–25.

29. Engler D, Meyer JC, Schellack N, Kurdi A, Godman B. Compliance with South Africa's Antimicrobial Resistance National Strategy Framework: are we there yet? J Chemother. 2021;33(1):21–31.

30. Kruger D, Dlamini NN, Meyer JC, Godman B, Kurdi A, Lennon M et al. Development of a web-based application to improve data collection of antimicrobial utilization in the public health care system in South Africa. Hosp Pract (1995). 2021;49(3):184–93.

31. Fabre V, Cosgrove SE, Secaira C, Tapia Torrez JC, Lessa FC, Patel TS, et al. Antimicrobial stewardship in Latin America: past, present, and future. Antimicrob Steward Health Epidemiol. 2022;2(1):e68.

32. Pan American Health Organization (PAHO). Latin American and Caribbean Network for Antimicrobial Resistance Surveillance - ReLAVRA+ [Available from: https://www.paho.org/en/topics/antimicrobial-resistance/latin-american-and-caribbean-network-antimicrobial-resistance].

33. Thomas GR, Corso A, Pasteran F, Shal J, Sosa A, Pillonetto M, et al. Increased Detection of Carbapenemase-Producing Enterobacterales Bacteria in Latin America and the Caribbean during the COVID-19 pandemic. Emerg Infect Dis. 2022;28(11):1–8.

34. Quiros RE, Bardossy AC, Angeleri P, Zurita J, Aleman Espinoza WR, Carneiro M, et al. Antimicrobial stewardship programs in adult intensive care units in Latin America: implementation, assessments, and impact on outcomes. Infect Control Hosp Epidemiol. 2022;43(2):181–90.

35. Carlos Bantar BS, Eduardo Vesco C, Heft M, Saul. Francisco Salamone, and Maria Eugenia Oliva. A Hospitalwide Intervention Program to optimize the quality of antibiotic use: impact on prescribing practice, antibiotic consumption, cost savings, and bacterial resistance. Clin Infect Dis. 2003;37:180–6.

36. Okumura LM, Riveros BS, Gomes-da-Silva MM, Veroneze I. A cost-effectiveness analysis of two different antimicrobial stewardship programs. Braz J Infect Dis. 2016;20(3):255–61.

37. Fabre V, Secaira C, Cosgrove SE, Lessa FC, Patel TS, Alvarez AA, et al. Deep dive into gaps and barriers to Implementation of Antimicrobial Stewardship Programs in hospitals in Latin America. Clin Infect Dis. 2023;77(Supplement1):S53–S61.

38. Allel K, Day L, Hamilton A, Lin L, Furuya-Kanamori L, Moore CE, et al. Global antimicrobial-resistance drivers: an ecological country-level study at the human-animal interface. Lancet Planet Health. 2023;7(4):e291–e303.

39. World Health Organization (WHO). Guidelines on core components of infection prevention and control programmes at the national and acute health care facility level. 2016.

40. Centers for Disease Control and Prevention (CDC). CDC's Core Infection Prevention and Control Practices for Safe Healthcare Delivery in All Settings [Available from: https://www.cdc.gov/infectioncontrol/guidelines/core-practices/index.html].

41. European Centre for Disease Prevention and Control (ECDC). Core competencies for infection control and hospital hygiene professionals in the European Union. 2013.

42. Centers for Disease Control and Prevention (CDC). Measuring Outpatient Antibiotic Prescribing [Available from: https://www.cdc.gov/antibiotic-use/data/outpatient-prescribing/index.html].

43. Suttels V, Van Singer M, Clack LC, Pluss-Suard C, Niquille A, Mueller Y et al. Factors influencing the implementation of Antimicrobial Stewardship in Primary Care: a narrative review. Antibiot (Basel). 2022;12(1).

44. Martinez-Gonzalez NA, Plate A, Jager L, Senn O, Neuner-Jehle S. The role of point-of-care C-Reactive protein testing in Antibiotic Prescribing for respiratory tract Infections: a Survey among Swiss General practitioners. Antibiot (Basel). 2022;11(5).

45. D'Hulster L, Abrams S, Bruyndonckx R, Anthierens S, Adriaenssens N, Butler CC, et al. Nationwide implementation of online communication skills training to reduce overprescribing of antibiotics: a stepped-wedge cluster randomized trial in general practice. JAC Antimicrob Resist. 2022;4(3):dlac070.

46. Wolfensberger A, Clack L, von Felten S, Faes Hesse M, Saleschus D, Meier MT et al. Prevention of non-ventilator-associated hospital-acquired Pneumonia in Switzerland: a type 2 hybrid effectiveness-implementation trial. Lancet Infect Dis. 2023;23(7):836–46.

47. Price L, Gozdzielewska L, Hendry K, McFarland A, Reilly J. Effectiveness of national and subnational interventions for prevention and control of health-care-associated Infections in acute hospitals in high-income and upper-middle-income counties: a systematic review update. Lancet Infect Dis. 2023;23(9):e347–e360

48. Bion J, Richardson A, Hibbert P, Beer J, Abrusci T, McCutcheon M, et al. Matching Michigan: a 2-year stepped interventional programme to minimise central venous catheter-blood stream Infections in intensive care units in England. BMJ Qual Saf. 2013;22(2):110–23.

49. Pronovost PJ, Goeschel CA, Colantuoni E, Watson S, Lubomski LH, Berenholtz SM, et al. Sustaining reductions in catheter related bloodstream Infections in Michigan intensive care units: observational study. BMJ. 2010;340:c309.

50. Nuclear Threat Initiative (NTI), Johns Hopkins Center for Health Security, Economist Impact. 2021 Global Health Security Index (GHS Index) 2021 [Available from: https://www.ghsindex.org/].

51. World Health Organization (WHO). Global Database for Tracking Antimicrobial Resistance (AMR) Country Self-Assessment Survey (TrACSS) [Available from: https://amrcountryprogress.org/#/map-view].

52. World Health Organization (WHO). Tracking AMR Country Self Assessment Survey (TrACSS) 2022 Country Report: Thailand. 2022.

53. Tsuzuki S, Koizumi R, Matsunaga N, Ohmagari N. Decline in Antimicrobial Consumption and Stagnation in reducing Disease Burden due to Antimicrobial Resistance in Japan. Infect Dis Ther. 2023;12(7):1823–34.

54. World Health Organization (WHO). Tracking AMR Country Self Assessment Survey (TrACSS) 2022 Country Report: Japan. 2022.

55. World Health Organization (WHO). Tracking AMR Country Self Assessment Survey (TrACSS) 2022 Country Report: South Africa. 2022.

## Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
27. The Government of Japan. National Action Plan on Antimicrobial Resistance (AMR) 2023–2027. 2023.

28. Brink AJ, Messina AP, Feldman C, Richards GA, Becker PJ, Goff DA, et al. Antimicrobial stewardship across 47 South African hospitals: an implementation study. Lancet Infect Dis. 2016;16(9):1017–25.

29. Engler D, Meyer JC, Schellack N, Kurdi A, Godman B. Compliance with South Africa's Antimicrobial Resistance National Strategy Framework: are we there yet? J Chemother. 2021;33(1):21–31.

30. Kruger D, Dlamini NN, Meyer JC, Godman B, Kurdi A, Lennon M et al. Development of a web-based application to improve data collection of antimicrobial utilization in the public health care system in South Africa. Hosp Pract (1995). 2021;49(3):184–93.

31. Fabre V, Cosgrove SE, Secaira C, Tapia Torrez JC, Lessa FC, Patel TS, et al. Antimicrobial stewardship in Latin America: past, present, and future. Antimicrob Steward Health Epidemiol. 2022;2(1):e68.

32. Pan American Health Organization (PAHO). Latin American and Caribbean Network for Antimicrobial Resistance Surveillance - ReLAVRA+ [Available from: https://www.paho.org/en/topics/antimicrobial-resistance/latin-american-and-caribbean-network-antimicrobial-resistance].

33. Thomas GR, Corso A, Pasteran F, Shal J, Sosa A, Pillonetto M, et al. Increased Detection of Carbapenemase-Producing Enterobacterales Bacteria in Latin America and the Caribbean during the COVID-19 pandemic. Emerg Infect Dis. 2022;28(11):1–8.

34. Quiros RE, Bardossy AC, Angeleri P, Zurita J, Aleman Espinoza WR, Carneiro M, et al. Antimicrobial stewardship programs in adult intensive care units in Latin America: implementation, assessments, and impact on outcomes. Infect Control Hosp Epidemiol. 2022;43(2):181–90.

35. Carlos Bantar BS, Eduardo Vesco C, Heft M, Saul. Francisco Salamone, and Maria Eugenia Oliva. A Hospitalwide Intervention Program to optimize the quality of antibiotic use: impact on prescribing practice, antibiotic consumption, cost savings, and bacterial resistance. Clin Infect Dis. 2003;37:180–6.

36. Okumura LM, Riveros BS, Gomes-da-Silva MM, Veroneze I. A cost-effectiveness analysis of two different antimicrobial stewardship programs. Braz J Infect Dis. 2016;20(3):255–61.

37. Fabre V, Secaira C, Cosgrove SE, Lessa FC, Patel TS, Alvarez AA, et al. Deep dive into gaps and barriers to Implementation of Antimicrobial Stewardship Programs in hospitals in Latin America. Clin Infect Dis. 2023;77(Supplement1):S53–S61.

38. Allel K, Day L, Hamilton A, Lin L, Furuya-Kanamori L, Moore CE, et al. Global antimicrobial-resistance drivers: an ecological country-level study at the human-animal interface. Lancet Planet Health. 2023;7(4):e291–e303.

39. World Health Organization (WHO). Guidelines on core components of infection prevention and control programmes at the national and acute health care facility level. 2016.

40. Centers for Disease Control and Prevention (CDC). CDC's Core Infection Prevention and Control Practices for Safe Healthcare Delivery in All Settings [Available from: https://www.cdc.gov/infectioncontrol/guidelines/core-practices/index.html].

41. European Centre for Disease Prevention and Control (ECDC). Core competencies for infection control and hospital hygiene professionals in the European Union. 2013.

42. Centers for Disease Control and Prevention (CDC). Measuring Outpatient Antibiotic Prescribing [Available from: https://www.cdc.gov/antibiotic-use/data/outpatient-prescribing/index.html].

43. Suttels V, Van Singer M, Clack LC, Plusz-Suard C, Niquille A, Mueller Y et al. Factors influencing the implementation of Antimicrobial Stewardship in Primary Care: a narrative review. Antibiot (Basel). 2022;12(1).

44. Martinez-Gonzalez NA, Plate A, Jager L, Senn O, Neuner-Jehle S. The role of point-of-care C-Reactive protein testing in Antibiotic Prescribing for respiratory tract Infections: a Survey among Swiss General practitioners. Antibiot (Basel). 2022;11(5).

45. D'Hulster L, Abrams S, Bruyndonckx R, Anthierens S, Adriaenssens N, Butler CC, et al. Nationwide implementation of online communication skills training to reduce overprescribing of antibiotics: a stepped-wedge cluster randomized trial in general practice. JAC Antimicrob Resist. 2022;4(3):dlac070.

46. Wolfensberger A, Clack L, von Felten S, Faes Hesse M, Saleschus D, Meier MT et al. Prevention of non-ventilator-associated hospital-acquired Pneumonia in Switzerland: a type 2 hybrid effectiveness-implementation trial. Lancet Infect Dis. 2023;23(7):836–46.

47. Price L, Gozdzielewska L, Hendry K, McFarland A, Reilly J. Effectiveness of national and subnational interventions for prevention and control of health-care-associated Infections in acute hospitals in high-income and upper-middle-income counties: a systematic review update. Lancet Infect Dis. 2023;23(9):e347–e360

48. Bion J, Richardson A, Hibbert P, Beer J, Abrusci T, McCutcheon M, et al. Matching Michigan: a 2-year stepped interventional programme to minimise central venous catheter-blood stream Infections in intensive care units in England. BMJ Qual Saf. 2013;22(2):110–23.

49. Pronovost PJ, Goeschel CA, Colantuoni E, Watson S, Lubomski LH, Berenholtz SM, et al. Sustaining reductions in catheter related bloodstream Infections in Michigan intensive care units: observational study. BMJ. 2010;340:c309.

50. Nuclear Threat Initiative (NTI), Johns Hopkins Center for Health Security, Economist Impact. 2021 Global Health Security Index (GHS Index) 2021 [Available from: https://www.ghsindex.org/].

51. World Health Organization (WHO). Global Database for Tracking Antimicrobial Resistance (AMR) Country Self-Assessment Survey (TrACSS) [Available from: https://amrcountryprogress.org/#/map-view].

52. World Health Organization (WHO). Tracking AMR Country Self Assessment Survey (TrACSS) 2022 Country Report: Thailand. 2022.

53. Tsuzuki S, Koizumi R, Matsunaga N, Ohmagari N. Decline in Antimicrobial Consumption and Stagnation in reducing Disease Burden due to Antimicrobial Resistance in Japan. Infect Dis Ther. 2023;12(7):1823–34.

54. World Health Organization (WHO). Tracking AMR Country Self Assessment Survey (TrACSS) 2022 Country Report: Japan. 2022.

55. World Health Organization (WHO). Tracking AMR Country Self Assessment Survey (TrACSS) 2022 Country Report: South Africa. 2022.

## Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.