European Antibiotic Awareness Day 2017: training the next generation of health care professionals in antibiotic stewardship

Antimicrobial stewardship (AMS) aims to optimise treatment, minimise the risk of adverse effects and reduce health care costs. In addition, it is recognised as a key component to stop the current spread of antimicrobial resistance in Europe. Educational programmes are particularly important for the successful implementation of AMS. Training should start during medical school, continue during clinical training and be reinforced throughout postgraduate training. National core curricula for paediatric training should include passive and active training of competencies needed for AMS and future paediatricians should be skilled in taking leadership roles in AMS initiatives. Other core members of the paediatric AMS team should also receive training focused on the unique medical needs of the paediatric patient.Conclusion: Ideally, all communities, hospitals and health regions in Europe should have AMS that serve all patient types, including children. We all have the responsibility to ensure that existing antibiotics remain effective.

# Introduction
Antimicrobial resistance (AMR) poses a serious and increasing threat to public health as infections caused by bacteria that are resistant to antimicrobials lead to approximately 25,000 deaths in the European Union every year. In children, a significant increase in the prevalence of multidrug-resistant bacterial infections has occurred during the past couple of decades [bib_ref] Antimicrobial-resistant pathogens: an emerging pediatric threat, Elliot [/bib_ref]. Over the last few years, there have been significant shortages in the development and availability of new antibiotics, and the number of targeted studies on antibiotics in children remains strikingly low [bib_ref] Antimicrobial stewardship in paediatrics, Principi [/bib_ref]. Therefore, the implementation of strategies to preserve the efficacy of existing antibiotics is an urgent public health priority, both in hospital and community settings.
Antimicrobial stewardship (AMS) aims to appropriately and safely prescribe antibiotics to patients, while reducing unnecessary or suboptimal use of antibiotics, thus maximising outcomes for the patient [bib_ref] Effect of antibiotic stewardship on the incidence of infection and colonisation with..., Baur [/bib_ref]. AMS is recognised as a key component to stop the current spread of AMR in Europe. AMS programmes have the ultimate goal of minimising selective pressure on the emergence of drug-resistant strains. Successful AMS programmes are characterised by the ability to break down activities into specific interventions that can be more easily implemented, monitored and evaluated [bib_ref] Antimicrobial stewardship for neonates and children: a global approach, Bielicki [/bib_ref]. Successfully implemented AMS programmes have a significant impact on reducing antimicrobial use in paediatric patients, costs and prescribing errors without negative impacts on patient safety, and actually resulting in improved patient outcomes [bib_ref] Antimicrobial stewardship programs in freestanding children's hospitals, Hersh [/bib_ref] [bib_ref] Antimicrobial stewardship in paediatrics, Principi [/bib_ref] [bib_ref] Inpatient antimicrobial stewardship in pediatrics: a systematic review, Smith [/bib_ref]. The identification of paediatric conditions with both frequent and variable antimicrobial use could guide the prioritisation of high-impact targets for AMS interventions [bib_ref] Identifying targets for antimicrobial stewardship in children's hospitals, Gerber [/bib_ref]. Paediatric AMS should not be limited to the hospital setting and collaboration among hospital and outpatient health care facilities is of paramount importance [bib_ref] New horizons for pediatric antibiotic stewardship, Goldman [/bib_ref] [bib_ref] Antimicrobial stewardship in pediatrics: how every pediatrician can be a steward, Hyun [/bib_ref]. Indeed, AMS can be effective in reducing antibiotic misuse in community settings [bib_ref] Impact of a 16-community trial to promote judicious antibiotic use in Massachusetts, Finkelstein [/bib_ref] [bib_ref] Effect of an outpatient antimicrobial stewardship intervention on broad-spectrum antibiotic prescribing by..., Gerber [/bib_ref] , and potential strategies to promote these programmes in community-based settings have been published [bib_ref] Antimicrobial stewardship in pediatrics: how every pediatrician can be a steward, Hyun [/bib_ref].

## Training in antimicrobial stewardship
As active participation of clinical professionals at all levels of care is required for AMS to succeed, educational programmes are particularly important for the successful implementation of AMS. Education of health care providers on appropriate antibiotic prescribing has been shown to enhance other antimicrobial stewardship interventions [bib_ref] Health care provider education as a tool to enhance antibiotic stewardship practices, Ohl [/bib_ref]. Therefore, the European Academy of Paediatrics (EAP) Curriculum for Common Trunk Training in Paediatricsincludes specific knowledge and skills related to AMR and the European Society for Paediatric Infectious Diseases (ESPID) and other national (paediatric) infectious diseases groups run specific courses on AMR [fig_ref] Table 2: Available e-learning tools AMS [/fig_ref]. The syllabus for Core Training sets out a European road map for common paediatric training. It is intended as a guide for national paediatric societies to help them understand the principles of core training. The EAP recognises that in many countries in Europe, training does not conform to these recommendations, but as such differences gradually diminish, quality, content and assessment of training, including training related to the principles AMR, will become more uniform across Europe. At the same time, it is recognised that differences in regional epidemiology and healthcare infrastructure require a tailor-made approach, also for AMS. Recently, recommendations were published for key points to be included in clinical curricula, in order to develop the necessary skills to participate in AMS [bib_ref] The intersection of antimicrobial stewardship and microbiology: educating the next generation of..., O&apos;donnell [/bib_ref] [bib_ref] Health care provider education as a tool to enhance antibiotic stewardship practices, Ohl [/bib_ref]. These are summarised in [fig_ref] Table 1: Key points to include in clinical AMS curricula [adapted from[20,22] [/fig_ref]. It is important that assimilation of knowledge about AMS starts already during medical school, is continued during clinical training and is reinforced throughout postgraduate training. Passive educational techniques like large and small group presentations are modestly effective for increasing knowledge. However, interactive or dynamic techniques influence prescribing behaviour. This includes education associated with specific episodes of patient care. Interactive small group sessions, e-learning, educational outreach, periodic retrospective audit and feedback and one-on-one patient-directed education have been shown to be moderately to highly effective in optimising antibiotic use and patient outcomes [bib_ref] Health care provider education as a tool to enhance antibiotic stewardship practices, Ohl [/bib_ref]. In particular, internet-based education shows encouraging results [bib_ref] Effects of internet-based training on antibiotic prescribing rates for acute respiratory-tract infections:..., Little [/bib_ref] [bib_ref] Antibiotic Awareness Day 2012: general practitioners encouraged to TARGET antibiotics through guidance,..., Mcnulty [/bib_ref] [bib_ref] Scottish Antimicrobial Prescribing Group (SAPG): development and impact of the Scottish National..., Nathwani [/bib_ref]. The advantages of e-learning include improved access to education in rural or low-resource areas and the potential to develop an interactive platform. Several examples of e-learning tools are listed in [fig_ref] Table 2: Available e-learning tools AMS [/fig_ref]. In addition, AMS was recently taught during the EAP MasterCourse 2017 and is included in the upcoming European Academy of Paediatric Societies congress in Paris, 2018. In addition, AMS is always covered during the annual residential ESPID-Oxford Course.
Although many of the overarching principles of AMS apply to children and adults alike, many factors related to paediatric AMS are unique to children. Children have high rates of infection and frequently present with non-specific symptoms adding to diagnostic uncertainty. Patterns of infection The participant learns how to de-escalate antibiotic use in order to more effectively treat an infection while limiting exposure to broad-spectrum antimicrobials Determine and verify antibiotic allergies Consider local antibiotic susceptibility Specify expected duration of therapy based on evidence and national and hospital guidelines Ensure appropriate administration (intravenous versus oral) Give antibiotics at the right dose and interval and resistance vary significantly by age, thus age-specific antibiotic panels for antibiograms should preferably be used to guide antibiotic choices for selected infections. Children are more prone to infection with resistant organisms due to a future lifetime of antibiotic exposure. In addition, considerations related to age-appropriate dosing and formulations pose challenges to the prescription of antibiotics in children [bib_ref] Dose optimisation of antibiotics in children: application of pharmacokinetics/pharmacodynamics in paediatrics, Downes [/bib_ref]. Children may respond differently to antibiotics compared to adults. Finally, immunisation initiatives should be included in AMS programmes as a preventive strategy in both in-and outpatient paediatric settings, in order to decrease the likelihood of serious illness and to decrease AMR. Therefore, other core members of the paediatric AMS team, like the microbiologist, paediatric infectious disease specialist and clinical pharmacist, should receive training focused on the unique medical needs of the paediatric patient [bib_ref] Making a case for pediatric antimicrobial stewardship programs, Magsarili [/bib_ref] [bib_ref] Advocacy Committee for the Pediatric Pharmacy Advocacy Group (2017) Pediatric antimicrobial stewardship..., Nichols [/bib_ref]. In addition, future paediatricians should be skilled in taking leadership roles in AMS initiatives and develop practical solutions rooted in the general principles of AMS, as it is important to further expand AMS activities from the hospital to paediatric offices and communities [bib_ref] Antimicrobial stewardship in pediatrics: how every pediatrician can be a steward, Hyun [/bib_ref].

## Keep antibiotics working
Limiting the further spread of AMR is one of EAP's child health priorities for 2017-2018. We will work together with the European Centre for Disease Prevention and Control to raise awareness about the relevance and benefits of costeffective AMS policies [bib_ref] Antimicrobial stewardship initiatives throughout Europe: proven value for money, Oberje [/bib_ref] and training in child health and to advocate for sustained implementation of these across Europe. Europe would greatly benefit from a uniform adoption of AMR and infection prevention best practice across countries. This includes harmonisation and simplification of the various treatment guidelines that currently exist across Europe. Moreover, there is an urgent need to conduct research on new antibiotic (classes) for critical multi-drug-resistant pathogens and on the effects of AMS programmes in lowincome countries in which emerging resistance are particularly alarming [bib_ref] The role of antimicrobial stewardship programmes in children: a systematic review, Araujo Da Silva [/bib_ref]. In addition, limited access to high-quality antibiotics is particularly of concern in these countries. Continuous education and training of health care professionals on appropriate antibiotic use is crucial. We therefore welcome the new European Action Plan, which was launched this summer. The European Commission intends, among others, to develop training programmes on AMR for health professionals through the ECDC and the EU health programme.

# Conclusion
Prevention of AMR needs rigorous actions in the community, at practice, ward, institutional, national and international levels. Best practices should be applied cross-border and healthcare institutions and communities should collaborate regionally and internationally, in order to fight AMR successfully. Effective Europe-wide implementation and sustained use of cost-effective antimicrobial policies can consequently lead to improved safety and quality of care while contributing to more sustainable healthcare. Ideally, all communities, hospitals and health regions in Europe should have AMS programmes that serve all patient types, including children. This includes adult academic and community hospitals and outpatient care centres that primarily care for children. Therefore, the EAP is interested to discuss interdisciplinary approaches of education with other stakeholders. Prudent use of antibiotics is very important to address the global challenges posed by AMR. We all have the responsibility to ensure that existing antibiotics remain effective.
Authors' contributions Lenneke Schrier initiated the EAP statement (together with HJD), wrote the draft and agrees on its final wording. Adamos Hadjipanayis commented on the draft and agrees on its final wording. Stefano del Torso commented on the draft and agrees on its final wording. Tom Stiris commented on the draft and agrees on its final wording. Marieke Emonts commented on the draft and agrees on its final wording. Hans Juergen Dornbusch initiated the EAP statement (together with LS), commented on the draft and agrees on its final wording.

## Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of interest.
Ethical approval This article does not contain any studies with human participants or animals performed by any of the authors and therefore neither ethical approval nor informed consent applies. Open Access This article is distributed under the terms of the Creative Comm ons Attribution 4.0 International License (http:// creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
[table] Table 1: Key points to include in clinical AMS curricula [adapted from[20,22] [/table]
[table] Table 2: Available e-learning tools AMS (general) Collection of AMS online courses made by the European Centre for Disease Prevention and Control: https://ecdc.europa.eu/en/publications-data/directory-guidance-prevention-and-control/training-antimicrobial-stewardship Massive Open Online Course on Antimicrobial Stewardship (University of Dundee, UK): https://www.futurelearn.com/courses/antimicrobial-stewardship Antimicrobial Stewardship Online CME Courses (Stanford University School of Medicine, USA): https://med.stanford.edu/cme/learning-opportunities/antimicrobialstewardship.html Paediatric AMS European Society for Paediatric Infectious Diseases (ESPID) online course on paediatric AMS: http://www.espid.org/content.aspx?Page=ESPID%20Online%20Antibiotic%20Management%20Course [/table]