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Linking antimicrobial resistance surveillance to antibiotic policy in healthcare settings: the COMBACTE-Magnet EPI-Net COACH project

Pezzani, Maria Diletta; Mazzaferri, Fulvia; Compri, Monica; Galia, Liliana; Mutters, Nico T.; Kahlmeter, Gunnar; Rodríguez-Baño, Jesús; Neth, Olaf

Abstract

Objectives: To systematically summarize the evidence on how to collect, analyse and report antimicrobial resistance (AMR) surveillance data to inform antimicrobial stewardship (AMS) teams providing guidance on empirical antibiotic treatment in health care settings. Methods: The research group identified 10 key questions about the link between AMR surveillance and AMS using a checklist of 9 elements for good practice in health research priority settings and a modified 3D combined approach matrix, and conducted a systematic review of published original studies and guidelines on the link between AMR surveillance and AMS. Results: The questions identified focused on AMS team composition; minimum infrastructure requirements for AMR surveillance; organisms, samples and susceptibility patterns to report; data stratification strategies; reporting frequency; resistance thre sholds to drive empirical therapy; surveillance in high-risk hospital units, long-term care, outpatient and veterinary settings; and surveillance data from other countries. Twenty guidelines and sevenoriginal studies on the implementation of AMR surveillance aspart of an AMS programme were included in the literature review. Conclusions: The evidence summarized in this review provides a useful basis for a more integrated process of developing procedures to report AMR surveillance data to drive AMS interventions. These procedures should be extended to settings outside the acute-care institutions, such as long-term care, outpatient and veterinary. Without proper AMR surveillance, implementation of AMS policies cannot contribute effectively to the fight against MDR pathogens and may even worsen the burden of adverse events from such interventions.

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Linking antimicrobial resistance surveillance to antibiotic policy in healthcare settings: the COMBACTE-Magnet EPI-Net COACH project Maria Diletta Pezzani 1 †, Fulvia Mazzaferri 1 †, Monica Compri 1 *, Liliana Galia 1 , Nico T. Mutters 2 , Gunnar Kahlmeter 3 , Theoklis E. Zaoutis 4 , Mitchell J. Schwaber 5 , Jesu´s Rodrı´guez-Ba~ no 6 , Stephan Harbarth 7 ‡ and Evelina Tacconelli 1,8,9 ‡ on behalf of the COACH working group§ 1 Infectious Diseases Section, Department of Diagnostic and Public Health, University of Verona, Verona, Italy; 2 Bonn University Hospital, Institute for Hygiene and Public Health, Bonn, Germany; 3 Department of Clinical Microbiology, Va¨xjo¨ Central Hospital, Va¨xjo¨, Sweden; 4 Perelman School of Medicine at the University of Pennsylvania, Infectious Diseases Division, The Children’s Hospital of Philadelphia, Philadelphia, Pennsylvania, USA; 5 National Centre for Infection Control, Israel Ministry of Health and Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel; 6 Division of Infectious Diseases, Microbiology and Preventive Medicine, Hospital Universitario Virgen Macarena/Department of Medicine, University of Seville/Biomedicine Institute of Seville (IBiS), Seville, Spain; 7 Infection Control Program, World Health Organization Collaborating Centre on Patient Safety, Geneva University Hospitals and Faculty of Medicine, Geneva, Switzerland; 8 Infectious Diseases, Department of Internal Medicine I, Tu¨bingen University Hospital, Tu¨bingen, Germany; 9 German Centre for Infection Research (DZIF), Clinical Research Unit for Healthcare Associated Infections, Tu¨bingen, Germany *Corresponding author. E-mail: [email protected] †Equally contributing authors. ‡Equally contributing last authors. §Members are listed in the Acknowledgements section. Objectives: To systematically summarize the evidence on how to collect, analyse and report antimicrobial resistance (AMR) surveillance data to inform antimicrobial stewardship (AMS) teams providing guidance on empirical antibiotic treatment in healthcare settings. Methods: The research group identified 10 key questions about the link between AMR surveillance and AMS using a checklist of 9 elements for good practice in health research priority settings and a modified 3D combined approach matrix, and conducted a systematic review of published original studies and guidelines on the link between AMR surveillance and AMS. Results: The questions identified focused on AMS team composition; minimum infrastructure requirements for AMR surveillance; organisms, samples and susceptibility patterns to report; data stratification strategies; reporting frequency; resistance thresholds to drive empirical therapy; surveillance in high-risk hospital units, long-term care, outpatient and veterinary settings; and surveillance data from other countries. Twenty guidelines and seven original studies on the implementation of AMR surveillance as part of an AMS programme were included in the literature review. Conclusions: The evidence summarized in this review provides a useful basis for a more integrated process of developing procedures to report AMR surveillance data to drive AMS interventions. These procedures should be extended to settings outside the acute-care institutions, such as long-term care, outpatient and veterinary. Without proper AMR surveillance, implementation of AMS policies cannot contribute effectively to the fight against MDR pathogens and may even worsen the burden of adverse events from such interventions. Introduction High-quality and timely antimicrobial resistance (AMR) surveillance plays a pivotal role in administering appropriate empirical antimicrobial therapy and implementing antimicrobial stewardship (AMS) programmes. Although IDSA 1,2 and European Commission (EC) 3 guidelines emphasize the importance of AMR surveillance in assisting AMS teams to develop empirical therapy protocols, no clear guidance exists on AMR surveillance or reporting for this purpose. 2,3 Major limitations include lack of adequate and comprehensive AMR surveillance systems as well as poor integration between laboratory and clinical data due to limited information technology platforms. 4 V CThe Author(s) 2020. Published by Oxford University Press on behalf of the British Society for Antimicrobial Chemotherapy. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http:// creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.p[email protected] ii2 J Antimicrob Chemother 2020; 75 Suppl 2: ii2–ii19 doi:10.1093/jac/dkaa425 Downloaded from https://academic.oup.com/jac/article/75/Supplement_2/ii2/6024993 by guest on 26 May 2025 This work is part of the Epidemiology Network (EPI-Net) project and the basis for the development of the collaboration between EPI-Net and the JPIAMR ARCH network (http://archnet-surveil lance.eu). EPI-Net was launched in 2015 to improve surveillance of AMR and healthcare-associated infections in Europe, under the COMBACTE-MAGNET consortium of the New Drugs for Bad Bugs (ND4BB) programme (https://www.combacte.com/about/epi-net). ND4BB is funded by the Innovative Medicines Initiative with the EC and the European Federation of Pharmaceutical Industries and Associations to address the European AMR crisis and accelerate development of and access to new medications (http://www. nd4bb.eu). Our objective was to systematically summarize the evidence on collection, analysis and reporting of AMR surveillance data to optimize antibiotic recommendations and empirical prescribing policies by AMS teams. Methods The research group set priorities for our recommendations using a checklist of nine elements for good practice in health research priority settings 5 and a modified 3D combined approach matrix. 6 From this analysis, we identified 10 key questions about the link between AMR surveillance and AMS and conducted a systematic literature review. Relevant English-language articles published from July 2008 to August 2019 were retrieved through searches of PubMed, Embase, the Cochrane Central Register of Controlled Trials, the Database of Abstracts of Reviews of Effects and the Cochrane Database of Systematic Reviews. A combination of Medical Subject Headings and equivalent terms was used in the search strategy (Figure1). The review protocol is available on the EPI-Net website (https://EPI-net.eu). Reviewers used a two-stage selection process. First, abstracts were screened against eligibility criteria and duplicate and irrelevant documents were excluded. Next, full-text articles were assessed, study data (design, setting, population, intervention, comparison, outcomes) were extracted from eligible articles, and references were screened on titles and abstracts for further inclusion (Figure1).Norestrictiononstudydesign,populationor setting was applied. We included both original articles assessing implementation of AMR surveillance reports as part of an AMS programme and guidelines providing recommendations on reporting AMR surveillance data to the AMS team. The PICO framework is shown in Table 1. Quality of original articles was assessed using the Effective Practice and Organisation of Care quality criteria for interrupted time series 7 and the Newcastle-Ottawa Scale for cohort and before–after studies. 8 Results and discussion We identified 20 guidelines with recommendations on the implementation of AMR surveillance as part of an AMS programme. All recommendations were supported by only low-quality evidence (expert opinion or small observational studies) 1–3,9–25 (Table 2). Database searching retrieved 2182 unique study records. Initial screening identified 182 full-text articles, of which 7 studies were eligible: 2 interrupted time series analyses, 26,27 1 prospective cohort study, 28 1 retrospective cohort study, 29,30 1controlledbefore–after study 31 and 2 uncontrolled before–after studies. 32,33 Six studies found that AMS interventions linked to surveillance were effective in reducing AMR rates, 26,27,29–33 and two studies showed a significant reduction in 30day mortality. 28,33 Study design, sample size, type of intervention, outcome and quality assessment are shown in Table 3. Basic and additional requirements for providing AMR data are summarized in Table 4. 1. What is the most appropriate AMS team composition to facilitate implementation of surveillance systems and inform AMS interventions? Seven guidelines underlined the benefits of a multidisciplinary AMS team, including infectious diseases specialist, clinical microbiologist, pharmacist, nurse, psychologist, epidemiologist and infection control specialist 1,3,9,11–14 Six studies assessed an AMS intervention with a clinical microbiologist included in the team. 26,28–33 To link surveillance data with clinical recommendations, involvement of a clinical microbiologist, pharmacist and infectious diseases specialist is fundamental. In settings where these specialists are not available, educational activities supporting establishment of qualified personnel trained in AMR and antimicrobial use should be a priority. The hub-and-spoke network model, in which a primary centre (hub) supports secondary centres with limited services(spokes),is often used to optimize the utilization of healthcare services in resource-constrained settings. 34 For AMS, experts in infectious diseases, clinical microbiologists and pharmacists in a hub hospital assist trained personnel in spoke hospitals to overcome resource limitations and implement effective, efficient collaboration and quality control of AMS activities. 2. What are the minimum infrastructure requirements of AMR surveillance to inform AMS interventions? No guidelines or studies addressed structural requirements for appropriate hospital AMR surveillance to inform AMS intervention. Fulfilment of good laboratory practices (i.e. processes that assure the integrity, safety and efficacy of laboratory activities) is the cornerstone. A quality management system should supervise the coordination and realization of quality objectives. 34–36 According to the research group, the medical director should be responsible for ensuring that adequate staffing and resources are allocated to support the functions and efforts of the quality management system. The international core set of quality-system essentials includes the following components: organization; facilities and safety; personnel and customer focus; purchasing, inventory and equipment; process management; documents and records and information management; occurrence management and assessment; and continual improvement (Table 5). For AMR surveillance, it is useful to establish a memorandum of understanding for data sharing with other national/regional institutions and a linkage with a national/central reference laboratory for technical support. The connection between hospital patient data from different healthcare settings allows comparison of AMR rates and helps AMS teams develop recommendations for patients with a history of hospitalization elsewhere. External sources of AMR rates in European countries include EARS-Net for invasive isolates and the EPI-Net website (https://EPI-net.eu), on which all publicly available AMR surveillance data (including monitoring of AMR to new antibiotics) are continually updated. Still, these international standards are not always applicable. Logistic barriers (e.g. geographical spread of hospitals) can affect communication and reporting by limiting access to laboratory services. 37 Low/middle income countries (LMICs) are often characterized by small-scale laboratories, lack of appropriate training and Antimicrobial resistance surveillance and antimicrobial stewardship JAC ii3 Downloaded from https://academic.oup.com/jac/article/75/Supplement_2/ii2/6024993 by guest on 26 May 2025 the absence of laboratory information systems. Development of national quality regulations based on international standards but also informed by country-specific characteristics and available resources is encouraged. 38,39 3. Which bacteria and samples should be included in the AMR surveillance report and how should susceptibility patterns be reported to inform AMS interventions? Six guidelines indicated that the criteria for the selection of pathogens to target in AMR surveillance should be based on local epidemiology and the major clinical impact attributable to a specific AMR profile, 3,9,11,14,16,21 one specified priority specimens for microbiological analysis, 16 and one underlined the relevance of separate reporting of screening samples. 9 One guideline specifically stated a minimum number of isolates for the construction of cumulative antibiograms, 16 and two recommended molecular diagnostics as a tool to focus appropriate AMS interventions. 9,11 Five studies assessed an AMS intervention providing an MIC based on cumulative antibiograms. 26–30,32 The most common Gram-negative (e.g. Escherichia coli)and Gram-positive (e.g. Staphylococcus aureus) pathogens have been suggested as proxies for hospitals unable to compute their AMR rates on a Gram-stain basis, although this practice is less precise and accurate. 40 Pathogens can be selected on the basis of hospital case mix composition and service type. Knowledge of the highest priorities at international and national levels can be taken as a first step of selection. 41 Data on Clostridioides difficile infections should be included in the surveillance programme because they have been shown to be an important quality indicator for assessment of AMS intervention impact at the patient level. 42,43 Whether antibiograms are an appropriate tool to measure AMS intervention effectiveness on AMR rates is debatable. 44 Records identified through database searchinga (n=4678) Screening Included Eligibility Identification Additional records identified through other sources (n=16) Records after duplicates removed (n=2182) Records screened (n=2100) Records excluded (n=1911) Full-text articles assessed for eligibility (n= 189) Full-text articles excluded, with reasons (n=182) Surveillance studies not involving AMS (69) AMS studies not involving surveillance (58) AMS studies focusing on target therapy only (45) In vitro studies (10) Studies included (n=7) • • • • Figure 1. Study selection process. a Index search terms: (surveillance) AND (epidemiol* OR prevalence OR incidence OR rate) AND (susceptib* OR resist* OR isolat* OR pathogen OR pathogens OR bacteri*) AND (antimicrobial stewardship OR anti-microbial stewardship OR antibiotic stewardship OR antimicrobial policy OR antimicrobial policies OR anti-microbial policy OR antimicrobial policies OR antibiotic policy OR antibiotic policies OR antimicrobial prescript* OR anti-microbial prescript* OR antibiotic prescript*). Pezzani et al. ii4 Downloaded from https://academic.oup.com/jac/article/75/Supplement_2/ii2/6024993 by guest on 26 May 2025 Antibiograms are usually reported as cumulative results of all susceptibility tests, 45,46 based on different stratification criteria and over predefined time intervals. Reporting of a cumulative antibiogram with 30 isolates tested during the analysis period is recommended to produce an appropriate statistical estimate of cumulative susceptibility rates. 46 Smaller numbers are generally not suitable because random fluctuations of uncertain significance may occur and AMR rates are thus easily biased. To achieve this minimum, it may be appropriate to either include isolates collected over a longer period or limit the combination of stratification criteria. Invasive isolates should always be included, and screening isolates from surveillance cultures should be reported separately. 9,47 Colonization status data should be interpreted carefully and may be taken into account only in selected cases (e.g. for post-transplantation infection prophylaxis or neutropenic fever treatment). 48,49 The choice among strategies depends strongly on what is most feasible and least time-consuming for the laboratory. 46,50 The first-isolate strategy, which includes the first isolate of a given species per patient per analysis period (e.g. 1 year), is simple and is generally recommended. 46,50 However, eliminating subsequent isolates from the same patient does not account for subsequent occurrence of resistant mutants or strains, which may be particularly important for some pathogens, such as Enterobacter species, Serratia species, Pseudomonas aeruginosa and Acinetobacter baumannii. Antimicrobial susceptibility test data can be displayed using qualitative categories (susceptible/intermediate/resistant) or MIC. 46,51 Qualitative results are simpler for clinicians but are poorly comparable among different laboratories because of the variety of testing methods and adoption of different interpretative criteria. Importantly, the latest EUCAST interpretative categories classify non-resistant isolates in relation to antimicrobial exposure level on the basis of administration route, dose, dosing interval, infusion time and pharmacokinetics profile, emphasizing the relationship between the drug exposure of the microorganism at the infection site and the interpretative breakpoint. 51 Despite the known clonal distribution of antibiotic resistance in many bacteria, empirical antibiotic selection still relies heavily on cumulative antibiograms, resulting in overuse of broad-spectrum agents. Antibiotic selection based on a genotype-specific antibiogram merges epidemiological surveillance and antimicrobial stewardship, possibly reducing the relative likelihood of antibiotic/ pathogen mismatch. 1,9,11 Genotyping is relevant for both infection control and AMS intervention, so it can be useful to guide therapy for severe infections (i.e. sepsis), 10 but it is not strictly essential for AMS interventions. Some guidelines suggest rapid diagnostic typing methods for investigation of clonality among resistant strains to drive AMS interventions. 1,9,11 4. How should AMR surveillance data be stratified to inform AMS interventions? Four guidelines suggested AMR rates stratified by hospital unit or department, 1,2,9,11 specimen type 9 or age group. 2 Five studies evaluated AMS interventions with AMR surveillance data stratified by hospital unit or department, 26,28,31,33 specimen type, 27,28 risk of MDR pathogen colonization/infection 28,31 or infection type. 32 Observational studies assessed AMR rates against different stratification criteria, revealing substantial differences across hospital units, specimen type, infection type and population characteristics, specifically inpatient versus outpatient and adult versus paediatric. 40,47,52–55 Stratification is recommended to enhance data consistency, assuming adequate numbers of tested organisms (Table6). Stratification based on timing of specimen collection during the course of hospitalization has revealed significant differences in AMR data. It is essential to provide better guidance for empirical therapy decisions, representing a valuable proxy for infection acquisition (community acquired versus hospital acquired). 52,54–56 Hospital-acquired infections are defined as infections that occur 48h after admission. 40,57 Nevertheless, patients with earlyonset hospital-acquired infections, variably defined as occurring within 4–7 days after admission, have lower AMR rates than patients with late onset. Unitor department-based stratification addresses case-mix differences more appropriately than hospital-wide data, representing a valuable proxy for stratifying by both age and immune status with no need for integrated demographic or background data. 40,52,55,58–60 However, in units or departments where samples are collected only for severe infections or those not responding to first-line treatment, AMR rates might be inflated and lead to inappropriate therapy choice and increased AMR and cost. Sample type-based stratification is another option. 40,47,52,55 Using data from sterile sites obviates the need for integrated clinical data on case definition, which requires specific software not available in most laboratories. Reporting data from non-sterile sites (e.g. wounds) should be avoided because it can inflate AMR rates. Adoption of AMR surveillance based either on infection type [e.g. pneumonia, intra-abdominal infections or urinary tract infections (UTIs)] or on groups of patients at high/low risk of MDR pathogen colonization/infection (e.g. solid or haematological malignancies, cystic fibrosis, recent antibiotic administrations or recent hospitalizations) has been shown to provide informative reports by combining laboratory data with clinical or background Table 1. The PICO framework Patients Any patient in any community or healthcare setting undergoing antibiotic prophylaxis or treatment Interventions Articles pertaining to surveillance interventions that aimed to improve antibiotic prescribing in healthcare settings Comparison Standard of care Outcome Any assessed AMS outcome: •Process measures (DDD, DOT) •Clinical outcomes (mortality, LOS) •Microbiological outcomes •Unintended consequences (CDI) DOT, days of therapy; CDI, Clostridioides difficile infection; LOS, length of stay. Antimicrobial resistance surveillance and antimicrobial stewardship JAC ii5 Downloaded from https://academic.oup.com/jac/article/75/Supplement_2/ii2/6024993 by guest on 26 May 2025 Table 2. Recommendations and/or statements from guidelines (2007–18) on how to link antimicrobial resistance surveillance data to antimicrobial stewardship, classified into 10 key questions First author, year Title Recommendation Question 1 - What is the most appropriate AMS team composition to facilitate implementation of surveillance systems and to inform AMS interventions? Dellit, 2007 1 Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America guidelines for developing an institutional programme to enhance antimicrobial stewardship •Infectious diseases physician •Clinical pharmacist with infectious diseases training •Clinical microbiologist •Information system specialist •Infection control professional •Hospital epidemiologist National Institute for Health and Care Excellence, 2015 13 Antimicrobial stewardship: systems and processes for effective antimicrobial medicine use •Core members (including an antimicrobial pharmacist and a medical microbiologist) and additional members depending on the care setting and the antimicrobial issue being considered de With, 2016 9 Strategies to enhance rational use of antibiotics in hospital: a guideline by the German Society for Infectious Diseases •Infectious diseases physician (or clinician with infectious diseases training) •Experienced clinical pharmacist/hospital pharmacist •Specialist in microbiology, virology and infection epidemiology •Physician locally responsible for infection control Department of Health, Republic of South Africa, 2017 14 Guidelines on implementation of the antimicrobial strategy in South Africa: one health approach & governance •Chair should be the highest-ranking management representative of the hospital •Senior physician of the hospital •Head of pharmacy services •IPC practitioner of the hospital •Head of nursing or highest-ranking nurse manager •Medical microbiologist Australian Commission on Safety and Quality in Health Care, 2018 11 Antimicrobial stewardship in Australian healthcare TERTIARY CARE •Infectious diseases physician or a clinical microbiologist •Pharmacist with allocated time for AMS •If feasible, include also: •Infection control practitioners •Prescribing clinicians from key departments (e.g. intensive care) •Nurses and midwives SMALL HOSPITALS (on site or within the local hospital network/local health district) •Pharmacist with allocated time for AMS •Prescribing clinician, nurse or midwife •Infectious diseases physician or a clinical microbiologist British Society for Antimicrobial Chemotherapy, 2018 12 Antimicrobial stewardship: from principles to practice •Medical microbiologist: laboratory knowledge, clinical knowledge •Infectious diseases physician: clinical knowledge, infectious diseases knowledge •Antibiotic pharmacist: in-depth knowledge of antibiotics, PK/PD, formulary maintenance, clinical pharmacy knowledge •Infection control nurse: input into infection control agenda, liaison with IPC committee •Consultant physician and consultant surgeon: clinical knowledge, representation of consultant physician staff group, ‘shop floor’ experience •Nurse: input from and representation of nursing staff; could provide patient’s perspective •Junior doctor representative: insight from the ‘shop floor’ of the organization; liaison with other junior medical staff; feedback •Pharmacy representative: additional insight from pharmacy staff Continued Pezzani et al. ii6 Downloaded from https://academic.oup.com/jac/article/75/Supplement_2/ii2/6024993 by guest on 26 May 2025 Table 2. Continued First author, year Title Recommendation •Primary care representatives •Data analyst: support for data analysis, information technology skills Castro-Sa´nchez, 2018 3 European Commission guidelines for the prudent use of antimicrobials in human health •Senior management support •Clinician with training, expertise and professional involvement in the diagnosis, prevention and treatment of infections (if possible, an infectious disease specialist) •Hospital pharmacist •Microbiologist (if possible, a clinical microbiologist) Question 2 - What are the minimum infrastructural requirements of AMR surveillance to inform AMS interventions? •No guideline reports specifically on this topic Question 3 - Which bacteria and samples should be included in the AMR surveillance report and how should susceptibility patterns be reported to inform AMS interventions? SARI Hospital Antimicrobial Stewardship Working Group, 2009 16 Guidelines for antimicrobial stewardship in hospitals in Ireland •Provide susceptibility data for key pathogens de With, 2016 9 Strategies to enhance rational use of antibiotics in hospital: a guideline by the German Society for Infectious Diseases •Report should include at least S. aureus,E. coli and other Enterobacteriaceae, P. aeruginosa and Candida species by specimen type (blood, urine, miscellaneous samples) and C. difficile •Report screening culture separately •Use up-to-date molecular diagnostic methods for rapid pathogen detection if they improve the quality of care Department of Health, Republic of South Africa, 2017 14 Guidelines on implementation of the antimicrobial strategy in South Africa: one health approach & governance •Focus surveillance on ESKAPE pathogens and Candida •Include only blood isolates in AMR surveillance reports •If there are <30 isolates of a given species, do not present the results unless there are compelling reasons to do so •Report the antibiotics that are routinely tested and that are appropriate for the clinical management Australian Commission on Safety and Quality in Health Care, 2018 11 Antimicrobial stewardship in Australian health care •Consider the following antibiotic-resistant bacteria for surveillance: vancomycin resistant Enterococci,Enterococcus species non-susceptible to linezolid, MRSA, linezolid or daptomycin-resistant S. aureus, vancomycin intermediate or resistant S. aureus, CRE, S. pneumoniae with MIC > 0.016 to penicillin, N. gonorrhoeae resistant to ceftriaxone or azithromycin, MDR Shigella,Salmonella resistant to ceftriaxone, S. pyogenes non-susceptible to penicillin •Report relevant molecular mechanisms of resistance Castro-Sa´nchez, 2018 3 European Commission guidelines for the prudent use of antimicrobials in human health •Ensure that susceptibility testing and reporting are in accordance with treatment guidelines and European and national standards •Report common bacterial pathogens Centers for Disease Control and Prevention, 2018 15 Antimicrobial stewardship core elements at small and critical access hospitals •Track data on C. difficile and antibiotic-resistant infections Question 4 - How should AMR surveillance data be stratified to inform AMS interventions? SARI Hospital Antimicrobial Stewardship Working Group 16 Guidelines for antimicrobial stewardship in hospitals in Ireland •Provide antibiograms for specific patient care areas, such as intensive care units Continued Antimicrobial resistance surveillance and antimicrobial stewardship JAC ii7 Downloaded from https://academic.oup.com/jac/article/75/Supplement_2/ii2/6024993 by guest on 26 May 2025 Table 2. Continued First author, year Title Recommendation Barlam, 2016 2 Implementing an antimicrobial stewardship programme: guidelines by the Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America •Develop stratified antibiograms to develop guidelines for empirical therapy (e.g. by location or age) de With, 2016 9 Strategies to enhance rational use of antibiotics in hospital: a guideline by the German Society for Infectious Diseases •Provide antimicrobial susceptibility data on a hospital-wide level and separately for general and intensive care units, or department specific •Stratify the AMR surveillance data by pathogen and type of specimen (e.g. blood, urine, miscellaneous samples) Australian Commission on Safety and Quality in Health Care, 2018 11 Antimicrobial stewardship in Australian health care •Report changes in AMR surveillance data on multidrug-resistant organisms for intensive care, transplantation, haematology and oncology units Question 5 - What is the frequency of reporting AMR surveillance data to inform AMS interventions? Dellit, 2007 1 Infectious Diseases Society of America and the Society of Healthcare Epidemiology of America guidelines for developing an institutional program to enhance antimicrobial stewardship •Update local antibiograms with pathogen-specific susceptibility data at least annually to optimize expert-based recommendations for empirical therapy SARI Hospital Antimicrobial Stewardship Working Group, 2009 16 Guidelines for antimicrobial stewardship in hospitals in Ireland •Carry out local surveillance of AMR, including annual review of antibiograms where appropriate de With, 2016 9 Strategies to enhance rational use of antibiotics in hospital: a guideline by the German Society for Infectious Diseases •Update pathogen-specific susceptibility data at least annually Department of Health Republic of South Africa, 2017 14 Guidelines on implementation of the antimicrobial strategy in South Africa: one health approach & governance •Present AMR rates at least annually. When more frequent analysis is performed, do not present results if <30 isolates of a particular species are present Australian Commission on Safety and Quality in Health Care, 2018 11 Antimicrobial stewardship in Australian health care •Provide annual analyses of AMR data to groups with responsibility for local antimicrobial therapy guidelines to inform recommendations for local empirical therapy and formulary management Question 6 - What are the threshold levels of resistance for changing the empirical antimicrobial treatment recommendation? Gupta, 2011 17 International clinical practice guidelines for the treatment of acute uncomplicated cystitis and pyelonephritis in women: a 2010 update by the Infectious Diseases Society of America and the European Society for Microbiology and Infectious Diseases •Do not use cotrimoxazole empirically where the resistance rate is >20% in urinary tract infections •Do not use fluoroquinolones empirically for pyelonephritis in areas where >10% of pathogens are resistant Kalil, 2016 18 Management of adults with hospitalacquired and ventilator-associated pneumonia: 2016 clinical practice guidelines by the Infectious Diseases Society of America and the American Thoracic Society •Include an agent active against MRSA for the empirical treatment of suspected HAP/VAP in patients who are being treated in units where >10%–20% of S. aureus isolates are MRSA •Prescribe two antibiotics active against P. aeruginosa for the empirical treatment of suspected VAP in patients who are being treated in units where >10% of Gram-negative isolates are resistant to the agent considered for monotherapy Continued Pezzani et al. ii8 Downloaded from https://academic.oup.com/jac/article/75/Supplement_2/ii2/6024993 by guest on 26 May 2025 Table 2. Continued First author, year Title Recommendation Torres, 2017 19 International ERS/ESICM/ESCMID/ALAT guidelines for the management of hospital-acquired pneumonia and ventilatorassociated pneumonia: guidelines for the management of hospital-acquired pneumonia (HAP)/ventilator-associated pneumonia (VAP) of the European Respiratory Society (ERS), European Society of Intensive Care Medicine (ESICM), European Society of Clinical Microbiology and Infectious Diseases (ESCMID) and Asociacio´n Latinoamericana del To´rax (ALAT) •Consider a prevalence of resistant pathogens in local microbiological data >25% as a high-risk situation for both Gram-negative and MRSA Hawkey, 2018 10 Treatment of infections caused by multidrug-resistant Gram-negative bacteria: report of the British Society for Antimicrobial Chemotherapy •Managing urinary tract infections, consider 5% as an appropriate threshold when the risk of the patient becoming bacteraemic is increased Question 7 - How should AMR surveillance be tailored to AMS in settings with patients at high risk of AMR colonization and infection? •No guideline reports specifically on this topic Question 8 - Should AMR surveillance reports include data from long-term care facility and outpatient settings to inform AMS interventions? Johnson, 2016 25 Improving feedback of surveillance data on antimicrobial consumption, resistance and stewardship in England: putting the data at your fingertips •Include the proportions of E. coli and non-specified coliforms from outpatient urine specimens that are tested and reported as resistant to trimethoprim and nitrofurantoin, at indicated geographies in the country Centers for Disease Control and Prevention, 2017 15 The core elements for antimicrobial stewardship in nursing homes •Provide a facility-specific antibiogram, at least each 18 months •Monitor rates of C. difficile infection and of antibiotic-resistant organisms (such as MRSA, CRE and resistant E. coli) Jump, 2017 20 Template for an antimicrobial stewardship policy for post-acute and long-term care settings •Provide a facility-specific antibiogram, stratified by type of sample, yearly (some long-term facilities may only have sufficient data to develop a urine antibiogram) •Track MRSA, CRE and C. difficile (only infection) Klepser, 2017 23 A call to action for outpatient antimicrobial stewardship •Track antibiotic susceptibility patterns, community-associated Clostridium difficile infections, infection rates with multidrug-resistant organisms •Track pathogens and susceptibility patterns from various specimens and different locations, such as emergency departments, clinics and long-term sites McElligott, 2017 22 Antimicrobial stewardship in nursing facilities •Provide a facility-specific antibiogram, at least quarterly •Include the monthly number of residents colonized or infected with different multidrug-resistant organisms (e.g. MRSA), C. difficile and the facility antibiogram Australian Commission on Safety and Quality in Health Care, 2018 11 Antimicrobial stewardship in Australian health care •Provide annual outpatient AMR data report Quality Innovation Network National Coordinating Center (USA), 2018 24 A field guide to antimicrobial stewardship in outpatient settings •Track AMR trends among common outpatient bacterial pathogens, quarterly or bi-annually Continued Antimicrobial resistance surveillance and antimicrobial stewardship JAC ii9 Downloaded from https://academic.oup.com/jac/article/75/Supplement_2/ii2/6024993 by guest on 26 May 2025 data. 18,47,55,61–63 Nevertheless, the lack of information system support together with the need for a more intensive workload in the case of manual data entry often represents a serious barrier to implementation, making this option unrealistic on a routine basis in the absence of sophisticated computerized decision support systems. Age categories (i.e. paediatrics, adults, elderly) are a feasible stratification strategy and may help to avoid AMR overestimation in paediatrics and AMR underestimation in the elderly, in whom high rates of MDR E. coli and S. aureus are well documented. 53,54,64,65 Nevertheless, unit/department-based AMR surveillance represents a valuable proxy for stratification by age because it considers paediatrics as well as units that focus on elderly patients (e.g. general medicine). 5. What is the frequency of reporting AMR surveillance data to inform AMS interventions? Five guidelines recommended reporting AMR surveillance data at least annually to inform AMS interventions. 1,9,11,14,16 Three studies assessed a bundled AMS intervention providing AMR surveillance reports monthly to yearly 26,31 or yearly. 32 AMR surveillance reports should provide regularly updated overviews of local epidemiology. Nevertheless, a recent review of European surveillance systems highlighted that most AMR surveillance systems provide outdated reports, thus reducing their value in driving clinical decisions. 4 Delayed reporting leads to suboptimal empirical prescribing that may jeopardize patient outcomes and increase MDR bacteria transmission risk. Annual reporting provides sufficient data to drive AMS, 1,9,11,14,16 but in the presence of a new intervention or outbreak a higher frequency might be considered. 14 The suitable time interval for reporting AMR data in high-risk patients (i.e. immunocompromised hosts) is still a matter of debate. Of note, development of automated information systems providing real-time updates on AMR data allows AMS interventions tailored to real-time antibiotic consumption data. 66 6. What are the threshold levels of resistance for changing the empirical antimicrobial treatment recommendation? Four guidelines defined a resistance level above which further empirical use of an antimicrobial drug is no longer appropriate for uncomplicated UTIs, 17 hospital-acquired pneumonia (HAP), ventilator-associated pneumonia (VAP) 18,19 and sepsis. 10 IDSA guidelines on uncomplicated UTIs recommend against empirical use of cotrimoxazole when the resistance rate exceeds 20%, 17 on the basis of trials showing that in women with acute cystitis caused by cotrimoxazole-resistant pathogens the drug has a failure rate of approximately 50%. 63,67–69 Fluoroquinolones are also not recommended as empirical therapy for pyelonephritis in areas where more than 10% of UTI pathogens demonstrate resistance, primarily based on expert opinion. 17 IDSA guidelines on HAP/VAP management suggest including an agent active against MRSA, either vancomycin or linezolid, for empirical treatment of suspected HAP/VAP when >10%–20% of S. aureus are MRSA. 18 Prescription of two antibiotics active against P. aeruginosa is recommended for empirical treatment of suspected VAP when >10% of P. aeruginosa are resistant to the monotherapy agent. The ERS/ESICM/ESCMID/ ALAT guidelines for HAP/VAP management recommend a higher cut-off rate of 25% for both Gram-negative pathogens and MRSA 19 on the basis of a study identifying a resistance rate >25% as an independent variable associated with treatment failure of monotherapies for HAP caused by resistant pathogens. 70 In patients with sepsis, experts suggest applying a lower threshold, not exceeding 10%–20%, which should be further reduced to 5% for immunocompromised patients. 10 One study assessed resistance thresholds in the framework of an AMS intervention, changing the recommendation when the resistance rate to an antibiotic was over 25% of all isolates for the same infection during the previous year. 28 Threshold definition needs to balance the risk of excessive antibiotic use against the need for effective initial antibiotic therapy, especially for invasive infections. 57,67,68,71,72 Furthermore, thresholds should be adjusted for high-risk groups and vary according to infection type and severity. On the basis of the limited evidence available, 25% may represent a reasonable threshold level of resistance for using alternative agents, whereas 5%–10% may be considered for higher-risk situations, such as septic shock and neutropenia with severe infections. These or similar thresholds can be applied to updated, appropriately stratified and carefully deduplicated AMR surveillance data at the local level. Although there is evidence to recommend a change in surgical prophylaxis in settings with a high risk of MRSA surgical site infections when nasal and skin decolonization is not performed, a clear threshold definition is lacking. 73,74 There are also uncertainties regarding whether AMR surveillance should drive antibiotic surgical prophylaxis against MDR Gram-negative bacteria, although more Table 2. Continued First author, year Title Recommendation Question 9 - Should AMR surveillance include data from other countries to inform AMS interventions? No guideline reports specifically on this topic Question 10 - Should AMR surveillance reports include regional and/or national surveillance data from companion and food-producing animals to inform AMS interventions in human healthcare? No guideline reports specifically on this topic CRE, carbapenem-resistant Enterobacteriaceae; ESKAPE, Enterococcus species, Staphylococcus aureus,K. pneumoniae,A. baumannii,P. aeruginosa, E. coli; IPC; infection prevention and control; PD, pharmacodynamics; PK, pharmacokinetics. Pezzani et al. ii10 Downloaded from https://academic.oup.com/jac/article/75/Supplement_2/ii2/6024993 by guest on 26 May 2025 Practice Guidelines by the Infectious Diseases Society of America and the American Thoracic Society. Clin Infect Dis 2016; 63: e61–111. 19 Torres A, Niederman MS, Chastre J et al. International ERS/ESICM/ ESCMID/ALAT guidelines for the management of hospital-acquired pneumonia and ventilator-associated pneumonia: guidelines for the management of hospital-acquired pneumonia (HAP)/ventilator-associated pneumonia (VAP) of the European Respiratory Society (ERS), European Society of Intensive Care Medicine (ESICM), European Society of Clinical Microbiology and Infectious Diseases (ESCMID) and Asociacio´n Latinoamericana del To´rax (ALAT). Eur Respir J 2017; 50: pii: 1700582. 20 Jump RLP, Gaur S, Katz MJ et al. Template for an antibiotic stewardship policy for post-acute and long-term care settings. JAmMedDirAssoc2017; 18: 913–20. 21 Centers for Disease Control and Prevention. The Core Elements for Antibiotic Stewardship in Nursing Homes. https://www.cdc.gov/longtermcare/ pdfs/core-elements-antibiotic-stewardship.pdf. 22 McElligott M, Welham G, Pop-Vicas A et al. Antibiotic stewardship in nursing facilities. Infect Dis Clin North Am 2017; 31: 619–38. 23 Klepser ME, Dobson EL, Pogue JM et al. A call to action for outpatient antibiotic stewardship. J Am Pharm Assoc 2017; 57: 457–63. 24 Quality Innovation Network National Coordinating Center. A Field Guide to Antibiotic Stewardship in Outpatient Settings. https://qioprogram.org/sites/ default/files/editors/141/C310_Field_Guide_20180730_FNL.pdf. 25 Johnson AP, Muller-Pebody B, Budd E et al. Improving feedback of surveillance data on antimicrobial consumption, resistance and stewardship in England: putting the data at your fingertips. JAntimicrobChemother2016; 72: 953–6. 26 Meyer E, Lapatschek M, Bechtold A et al. Impact of restriction of third generation cephalosporins on the burden of third generation cephalosporin resistant K. pneumoniae and E. coli in an ICU. IntensiveCareMed2009; 35: 862–70. 27 Tuon FF, Gasparetto J, Wollmann LC et al. Mobile health application to assist doctors in antibiotic prescription—an approach for antibiotic stewardship. Braz J Infect Dis 2017; 21: 660–4. 28 Rodriguez-Maresca M, Sorlozano A, Grau M et al. Implementation of a computerized decision support system to improve the appropriateness of antibiotic therapy using local microbiologic data. Biomed Res Int 2014; 2014: 395434. 29 Palmer HR, Weston J, Gentry L et al. Improving patient care through implementation of an antimicrobial stewardship program. Am J Health Syst Pharm 2011; 68: 2170–4. 30 Tam VH, Gamez EA, Weston JS et al. Outcomes of bacteremia due to Pseudomonas aeruginosa with reduced susceptibility to piperacillintazobactam: implications on the appropriateness of the resistance breakpoint. Clin Infect Dis 2008; 46: 862–7. 31 KnudsenJD, Andersen SE; Bispebjerg Intervention Group. A multidisciplinary intervention to reduce infections of ESBL-and AmpC-producing, gramnegative bacteria at a university hospital. PLoS One 2014; 9: e86457. 32 Wong-Beringer A, Nguyen LH, Lee M et al. An antimicrobial stewardship program with a focus on reducing fluoroquinolone overuse. Pharmacotherapy 2009; 29: 736–43. 33 Nachtigall I, Tafelski S, Deja M et al. Long-term effect of computerassisted decision support for antibiotic treatment in critically ill patients: a prospective ‘before/after’ cohort study. BMJ Open 2014; 4: e005370. 34 Elrod JK, Fortenberry JL. The hub-and-spoke organization design: an avenue for serving patients well. BMC Health Serv Res 2017; 17 Suppl 1: 25–33. 35 World Health Organization. Laboratory Quality Management System: Handbook. 2011. https://www.who.int/ihr/publications/lqms/en/. 36 CLSI. Quality Management System: A Model for Laboratory Services— Fourth Edition: QMS01-A4. 2011. 37 SkodvinB,AaseK,BrekkenALet al. Addressing the key communication barriers between microbiology laboratories and clinical units: a qualitative study. J Antimicrob Chemother 2017; 72: 2666–72. 38 Datema TAM, Oska L, Klatser PR. Review and comparison of quality standards, guidelines and regulations for laboratories. Afr J Lab Med 2012; 1:3. 39 WorldHealthOrganizationRegionalOfficeforAfrica.Guide for Establishing Laboratory-Based Surveillance for Antimicrobial Resistance. https://www.afro.who.int/sites/default/files/2017-06/guide-for-establishinglab-based-surveillance-for-amr.pdf. 40 Green DL. Selection of an empiric antibiotic regimen for hospital-acquired pneumonia using a unit and culture-type specific antibiogram. JIntensive Care Med 2005; 20: 296–301. 41 Tacconelli E, Carrara E, Savoldi A et al. Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis. Lancet Infect Dis 2018; 18: 318–27. 42 Moehring RW, Anderson DJ, Cochran RL et al. Expert consensus on metrics to assess the impact of patient-level antimicrobial stewardship interventions in acute-care settings. Clin Infect Dis 2016; 64: 377–83. 43 Baur D, Gladstone BP, Burkert F et al. Effect of antibiotic stewardship on the incidence of infection and colonisation with antibiotic-resistant bacteria and Clostridium difficile infection: a systematic review and meta-analysis. Lancet Infect Dis 2017; 17: 990–1001. 44 Schulz LT, Fox BC, Polk RE. Can the antibiogram be used to assess microbiologic outcomes after antimicrobial stewardship interventions? A critical review of the literature. Pharmacotherapy 2012; 32: 668–76. 45 Cornaglia G, Hryniewicz W, Jarlier V et al. European recommendations for antimicrobial resistance surveillance. Clin Microbiol Infect 2004; 10: 349–83. 46 CLSI. Analysis and Presentation of Cumulative Antimicrobial Susceptibility Test Data—Fourth Edition: M39-A4. 2014. 47 Kohlmann R, Gatermann SG. Analysis and presentation of cumulative antimicrobial susceptibility test data—the influence of different parameters in a routine clinical microbiology laboratory. PLoS One 2016; 11: e0147965. 48 Abbo LM, Ariza-Heredia EJ. Antimicrobial stewardship in immunocompromised hosts. Infect Dis Clin North Am 2014; 28: 263–79. 49 Gyssens IC, Kern WV, Livermore DM et al. Theroleofantibioticstewardship in limiting antibacterial resistance among hematology patients. Haematologica 2013; 98: 1821–5. 50 Hindler JF, Stelling J. Analysis and presentation of cumulative antibiograms: a new consensus guideline from the Clinical and Laboratory Standards Institute. Clin Infect Dis 2007; 44: 867–73. 51 European Committee on Antimicrobial Susceptibility Testing. Redefining Susceptibility Testing Categories S, I and R. http://www.eucast.org/fileadmin/ src/media/PDFs/EUCAST_files/EUCAST_Presentations/2018/EUCAST_-_Inter mediate_category_-_information_for_all.pdf. 52 Kuster SP, Ruef C, Zbinden R et al. Stratification of cumulative antibiograms in hospitals for hospital unit, specimen type, isolate sequence and duration of hospital stay. J Antimicrob Chemother 2008; 62: 1451–61. 53 Boggan JC, Navar-Boggan AM, Jhaveri R. Pediatric-specific antimicrobial susceptibility data and empiric antibiotic selection. Pediatrics 2012; 130: e615. 54 Swami S, Liesinger J, Shah N et al. Incidence of antibiotic-resistant Escherichia coli bacteriuria according to age and location of onset: a population-based study from Olmsted County, Minnesota. Mayo Clin Proc 2012; 87: 753–9. 55 Center for Diseases Control, Atlanta. Multidrug-Resistant Organism & Clostridioides difficile Infection (MDRO/CDI) Module. 2020. https://www.cdc. gov/nhsn/PDFs/pscManual/12pscMDRO_CDADcurrent.pdf. 56 Archibald L, Phillips L, Monnet D et al. Antimicrobial resistance in isolates from inpatients and outpatients in the United States: increasing importance of the intensive care unit. Clin Infect Dis 1997; 24: 211–15. Antimicrobial resistance surveillance and antimicrobial stewardship JAC ii17 Downloaded from https://academic.oup.com/jac/article/75/Supplement_2/ii2/6024993 by guest on 26 May 2025 57 Leone M, Garcin F, Bouvenot J et al. Ventilator-associated pneumonia: breaking the vicious circle of antibiotic overuse. Crit Care Med 2007; 35: 379–85. 58 Binkley S, Fishman NO, LaRosa LA et al. Comparison of unit-specific and hospital-wide antibiograms potential implications for selection of empirical antimicrobial therapy. Infect Control Hosp Epidemiol 2006; 27: 682–7. 59 Fridkin SK, Steward CD, Edwards JR et al. Surveillance of antimicrobial use and antimicrobial resistance in US hospitals: project ICARE phase 2. Clin Infect Dis 1999; 29: 245–52. 60 Stratton CW, Ratner H, Johnston PE et al. Focused microbiologic surveillance by specific hospital unit: practical application and clinical utility. Clin Ther 1993; 15 Suppl A: 12–20. 61 Bosso JA, Mauldin PD, Steed LL. Consequences of combining cystic fibrosisand non-cystic fibrosis-derived Pseudomonas aeruginosa antibiotic susceptibility results in hospital antibiograms. Ann Pharmacother 2006; 40: 1946–9. 62 Sartelli M, Chichom-Mefire A, Labricciosa FM et al. The management of intra-abdominal infections from a global perspective: 2017 WSES guidelines for management of intra-abdominal infections. World J Emerg Surg 2017; 12:29. 63 Bonkat G, Bartoletti R, Bruye`re F et al. European Association of Urology Guidelines on Urological Infections. https://uroweb.org/guideline/urologicalinfections/. 64 David M, Crawford S, Boyle-Vavra S et al. Contrasting pediatric and adult methicillin-resistant Staphylococcus aureus isolates. Emerg Infect Dis 2006; 12: 631–7. 65 Swami SK, Banerjee R. Comparison of hospital-wide and age and location-stratified antibiograms of S. aureus,E. coli,andS. pneumoniae: ageand location-stratified antibiograms. Springerplus 2013; 2: 63. 66 Lo´pez-Lozano JM, Lawes T, Nebot C et al. A nonlinear time-series analysis approach to identify thresholds in associations between population antibiotic use and rates of resistance. Nat Microbiol 2019; 4: 1160–72. 67 RazR,ChazanB,KennesYet al. Empiric use of trimethoprimsulfamethoxazole (TMP-SMX) in the treatment of women with uncomplicated urinary tract infections, in a geographical area with a high prevalence of TMP-SMX-resistant uropathogens. Clin Infect Dis 2002; 34: 1165–9. 68 Talan DA, Stamm WE, Hooton TM et al. Comparison of ciprofloxacin (7 days) and trimethoprim-sulfamethoxazole (14 days) for acute uncomplicated pyelonephritis in women: a randomized trial. JAMA 2000; 283: 1583–90. 69 McCarty JM, Richard G, Huck W et al. A randomized trial of short-course ciprofloxacin, ofloxacin or trimethoprim/sulfamethoxazole for the treatment of acute urinary tract infection in women. Ciprofloxacin Urinary Tract Infection Group. Am J Med 1999; 106: 292–9. 70 Martin-Loeches I, Deja M, Koulenti D et al. Potentially resistant microorganisms in intubated patients with hospital-acquired pneumonia: the interaction of ecology, shock and risk factor. Intensive Care Med 2013; 39: 672–81. 71 Luna CM, Vujacich P, Niederman MS et al. Impact of BAL data on the therapy and outcome of ventilator-associated pneumonia. Chest 1997; 111: 676–85. 72 Micek ST, Lloyd AE, Ritchie DJ et al. Pseudomonas aeruginosa bloodstream infection: importance of appropriate initial antimicrobial treatment. Antimicrob Agents Chemother 2005; 49: 1306–11. 73 Bratzler DW, Dellinger EP, Olsen KM et al. Clinical practice guidelines for antimicrobial prophylaxis in surgery. Surg Infect (Larchmt) 2013; 14: 73–156. 74 Cranny G, Elliott R, Weatherly H et al. Asystematicreviewand economic model of switching from non-glycopeptide to glycopeptide antibiotic prophylaxis for surgery. Health Technol Assess 2008; 12:iii–iv, xi–xii, 1–147. 75 WorldHealthOrganization.Global Guidelines for the Prevention of Surgical Site Infection,2nd edn. Geneva: WHO, 2018. 76 Dubinsky-Pertzov B, Temkin E, Harbarth S et al. Carriage of extendedspectrum b-lactamase–producing Enterobacteriaceae and the risk of surgical site infection after colorectal surgery: a prospective cohort study. Clin Infect Dis 2018; 68: 1699–704. 77 Harbarth S, Harris AD, Carmeli Y et al. Parallel analysis of individual and aggregated data on antibiotic exposure and resistance in gram-negative bacilli. Clin Infect Dis 2001; 33: 1462–8. 78 Kullar R, Goff DA. Transformation of antimicrobial stewardship programs through technology and informatics. Infect Dis Clin North Am 2014; 28: 291–300. 79 Lo´pez-Lozano JM, Monnet DL, Yagu¨e A et al. Modelling and forecasting antimicrobial resistance and its dynamic relationship to antimicrobial use: a time series analysis. Int J Antimicrob Agents 2000; 14: 21–31. 80 Rittmann B, Stevens MP. Clinical decision support systems and their role in antibiotic stewardship: a systematic review. Curr Infect Dis Rep 2019; 21: 29. 81 SuetensC,LatourK,Ka¨rki T et al. Prevalence of healthcare-associated infections, estimated incidence and composite antimicrobial resistance index in acute care hospitals and long-term care facilities: results from two European point prevalence surveys, 2016 to 2017. Euro Surveill 2018; 23: pii=1800516. 82 NicolleLE,BentleyDW,GaribaldiRet al.; SHEA Long-Term Care Committee. Antimicrobial use in long-term-care facilities. Infect Control Hosp Epidemiol 2000; 21: 537–45. 83 European Centre for Disease Prevention and Control. Risk Assessment on the Spread of Carbapenemase-Producing Enterobacteriaceae (CPE) through Patient Transfer between Healthcare Facilities, with Special Emphasis on Cross-border Transfer. Stockholm: ECDC, 2011. https://www.ecdc.europa.eu/ en/publications-data/risk-assessment-spread-carbapenemase-producingenterobacteriaceae-cpe-through. 84 Frost I, Van Boeckel TP, Pires J et al. Global geographic trends in antimicrobial resistance: the role of international travel. JTravelMed2019; 26:pii: taz036. 85 Armand-Lefe`vre L, Andremont A, Ruppe´ E. Travel and acquisition of multidrug-resistant Enterobacteriaceae. Med Mal Infect 2018; 48: 431–41. 86 Hassing RJ, Alsma J, Arcilla MS et al. International travel and acquisition of multidrug-resistant Enterobacteriaceae: a systematic review. Euro Surveill 2015; 20: pii=30074. 87 Grundmann H, Klugman K, Walsh T et al. A framework for global surveillance of antibiotic resistance. Drug Resist Updat 2011; 14: 79–87. 88 Barbe`B,YansouniCP,AffolabiDet al. Implementation of quality management for clinical bacteriology in low-resource settings. Clin Microbiol Infect 2017; 23: 426–33. 89 Pantosti A. Methicillin-resistant Staphylococcus aureus associated with animals and its relevance to human health. Front Microbiol 2012; 3: 127. 90 Becker K, Ballhausen B, Kahl BC et al. The clinical impact of livestockassociated methicillin-resistant Staphylococcus aureus of the clonal complex 398 for humans. Vet Microbiol 2017; 200:33–8. 91 Dahms C, Hu¨bner NO, Cuny C et al. Occurrence of methicillinresistant Staphylococcus aureus in farm workers and the livestock environment in Mecklenburg-Western Pomerania, Germany. Acta Vet Scand 2014; 56:53. Pezzani et al. ii18 Downloaded from https://academic.oup.com/jac/article/75/Supplement_2/ii2/6024993 by guest on 26 May 2025 92 Dahms C, Hu¨bner NO, Kossow A et al. Occurrence of ESBL-producing Escherichia coli in livestock and farm workers in Mecklenburg-Western Pomerania, Germany. PLoS One 2015; 10: e0143326. 93 Hammerum AM, Larsen J, Andersen VD et al. Characterization of extended-spectrum b-lactamase (ESBL)-producing Escherichia coli obtained from Danish pigs, pig farmers and their families from farms with high or no consumption of thirdor fourth-generation cephalosporins. JAntimicrob Chemother 2014; 69: 2650–7. 94 Leverstein-van Hall MA, Dierikx CM, Cohen Stuart J et al. Dutch patients, retail chicken meat and poultry share the same ESBL genes, plasmids and strains. Clin Microbiol Infect 2011; 17: 873–80. 95 Simjee S, McDermott P, Trott DJ et al. Present and future surveillance of antimicrobial resistance in animals: principles and practices. Microbiol Spectr 2018; 6: 595–618. 96 Guardabassi L, Prescott JF. Antimicrobial stewardship in small animal veterinary practice: from theory to practice. Vet Clin North Am Small Anim Pract 2015; 45: 361–76. Antimicrobial resistance surveillance and antimicrobial stewardship JAC ii19 Downloaded from https://academic.oup.com/jac/article/75/Supplement_2/ii2/6024993 by guest on 26 May 2025