Development and validation of potential structure indicators for evaluating antimicrobial stewardship programmes in European hospitals

  • F. M. Buyle
  • S. Metz-Gercek
  • R. Mechtler
  • W. V. Kern
  • H. Robays
  • D. Vogelaers
  • M. J. Struelens
  • on behalf of members of the Antibiotic Strategy International (ABS) Quality Indicators Team


This study describes the development of structure indicators for hospital antimicrobial stewardship programmes and pilot validation across European hospitals. A multi-disciplinary panel from four European countries developed structure indicators in three steps: identification and listing of indicators, remote ranking of indicators using multi-criteria scoring, selection of indicators in a face-to-face consensus meeting. Additionally, the top-ten indicators were identified as a minimal set of key indicators. A survey was sent to the directors of antimicrobial stewardship programmes in European hospitals. The yes/no answers for the indicators were transformed into numbers in order to calculate the total scores. A list of 58 indicators was selected and categorised into the following topics: antimicrobial stewardship services (12 items), tools (16 items), human resources and mandate (6 items), health care personnel development (4 items), basic diagnostic capabilities (6 items), microbiological rapid tests (2 items), evaluation of microbiological drug resistance data (3 items), antibiotic consumption control (5 items) and drug use monitoring (4 items). The indicator scores, reported by 11 pilot hospitals from five European countries, ranged from 32 to 50 (maximum score = 58) and from 5 to 10 points (maximum score = 10) for, respectively, the complete and the top-ten list. An international panel selected 58 potential structure indicators, among which was a minimal set of ten key structure indicators, that could be useful for assessment of the comprehensiveness and resource-intensity of antimicrobial stewardship programmes. There was significant heterogeneity among participating centres with regard to their score for structural components of effective antimicrobial stewardship.


Quality Indicator Clostridium Difficile Infection Antimicrobial Stewardship Structure Indicator Stewardship Programme 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank all the members of the ABS Quality Indicators Team: F. Allerberger, B. Byl, M. Costers, C. Ernes, A. Frank, R. Gareis, E. Hendrickx, R. Krause, A. Lechner, H. Mittermayer.

We thank our dedicated and hard-working colleagues from the antibiotic stewardship teams in the participating hospitals for contributing their data and Benedicte Delcoigne for the data analysis assistance with compiling the expert multi-criteria scores.

We thank the external reviewers from the ABS International - Work package 5: I. Gyssens, C.Suetens, H. Goossens.

Transparency declarations

None to declare.


The project was co-financed by the European Commission, Directorate General Health and Consumer Protection through the Community Action Programme for Public Health (2003–2008), contract number 2005208, and by the participating institutions through their programmes of antibiotic use improvement.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. 1.
    Council of the European Union (2002) Council recommendation of 15 November 2001 on the prudent use of antimicrobial agents in human medicine (2002/77/EC). OJEU 45:13–16Google Scholar
  2. 2.
    Allerberger F, Gareis R, Jindrák V, Struelens MJ (2009) Antibiotic stewardship implementation in the EU: the way forward. Expert Rev Anti Infect Ther 7:1175–1183PubMedCrossRefGoogle Scholar
  3. 3.
    Allerberger F, Lechner A, Wechsler-Fördös A, Gareis R; on behalf of ABS International (2008) Optimization of antibiotic use in hospitals—antimicrobial stewardship and the EU project ABS international. Chemotherapy 54:260–267PubMedCrossRefGoogle Scholar
  4. 4.
    Buyle FM, Metz-Gercek S, Mechtler R, Kern WV, Robays H, Vogelaers D, Struelens MJ; Antibiotic Strategy International—ABS Quality Indicators Team (2012) Prospective multicentre feasibility study of a quality of care indicator for intravenous to oral switch therapy with highly bioavailable antibiotics. J Antimicrob Chemother 67:2043–2046PubMedCrossRefGoogle Scholar
  5. 5.
    Donabedian A (1988) The quality of care. How can it be assessed? JAMA 260:1743–1748PubMedCrossRefGoogle Scholar
  6. 6.
    Lawrence M, Olesen F (1997) Indicators of quality in health care. Eur J Gen Pract 3:103–108CrossRefGoogle Scholar
  7. 7.
    Hoven JL, Haaijer-Ruskamp FM, Vander Stichele RH; DURQUIM Scientific Committee (2005) Indicators of prescribing quality in drug utilisation research: report of a European meeting (DURQUIM, 13-15 May 2004). Eur J Clin Pharmacol 60:831–834PubMedCrossRefGoogle Scholar
  8. 8.
    Dellit TH, Owens RC, McGowan JE Jr, Gerding DN, Weinstein RA, Burke JP, Huskins WC, Paterson DL, Fishman NO, Carpenter CF, Brennan PJ, Billeter M, Hooton TM; Infectious Diseases Society of America; Society for Healthcare Epidemiology of America (2007) Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America guidelines for developing an institutional program to enhance antimicrobial stewardship. Clin Infect Dis 44:159–177PubMedCrossRefGoogle Scholar
  9. 9.
    MacDougall C, Polk RE (2005) Antimicrobial stewardship programs in health care systems. Clin Microb Rev 18:638–656CrossRefGoogle Scholar
  10. 10.
    Sourdeau L, Struelens MJ, Peetermans WE, Costers M, Suetens C; Hospital Care Working Group of Belgian Antibiotic Policy Coordination Committee (BAPCOC) (2006) Implementation of antibiotic management teams in Belgian hospitals. Acta Clin Belg 61:58–63PubMedGoogle Scholar
  11. 11.
    Davey P, Brown E, Fenelon L, Finch R, Gould I, Hartman G, Holmes A, Ramsay C, Taylor E, Wilcox M, Wiffen P (2005) Interventions to improve antibiotic prescribing practices for hospital inpatients. Cochrane Database Syst Rev 19(4):CD003543Google Scholar
  12. 12.
    Knox K, Lawson W, Holmes A (2005) Multidisciplinary antimicrobial management teams and the role of the pharmacist in management of infection. In: Gould IM, van der Meer JWM (eds) Antibiotic policies: theory and practice. Springer US, New York, pp 227–249CrossRefGoogle Scholar
  13. 13.
    Nathwani D (1999) How do you measure the impact of an antibiotic policy? J Hosp Infect 43:S265–S268PubMedCrossRefGoogle Scholar
  14. 14.
    Nathwani D, Gray K, Borland H (2002) Quality indicators for antibiotic control programmes. J Hosp Infect 50:165–169PubMedCrossRefGoogle Scholar
  15. 15.
    Struelens MJ, Costers M; Belgian Antibiotic Policy Coordination Committee (BAPCOC)-Hospital Care Working Group (2008) Hospital antibiotic management in Belgium—results of the ABS maturity survey of the ABS International group. Wien Klin Wochenschr 120:284–288PubMedCrossRefGoogle Scholar
  16. 16.
    Van Gastel E, Costers M, Peetermans WE, Struelens MJ; Hospital Medicine Working Group of the Belgian Antibiotic Policy Coordination Committee (2010) Nationwide implementation of antibiotic management teams in Belgian hospitals: a self-reporting survey. J Antimicrob Chemother 65:576–580PubMedCrossRefGoogle Scholar
  17. 17.
    Schouten JA, Hulscher ME, Wollersheim H, Braspennning J, Kullberg BJ, van der Meer JW, Grol RP (2005) Quality of antibiotic use for lower respiratory tract infections at hospitals: (how) can we measure it? Clin Infect Dis 41:450–460PubMedCrossRefGoogle Scholar
  18. 18.
    Bruce J, MacKenzie FM, Cookson B, Mollison J, van der Meer JW, Krcmery V, Gould IM; ARPAC Steering Group (2009) Antibiotic stewardship and consumption: findings from a pan-European hospital study. J Antimicrob Chemother 64:853–860PubMedCrossRefGoogle Scholar
  19. 19.
    Society for Healthcare Epidemiology of America; Infectious Diseases Society of America; Pediatric Infectious Diseases Society (2012) Policy statement on antimicrobial stewardship by the Society for Healthcare Epidemiology of America (SHEA), the Infectious Diseases Society of America (IDSA), and the Pediatric Infectious Diseases Society (PIDS). Infect Control Hosp Epidemiol 33:322–327CrossRefGoogle Scholar
  20. 20.
    Nathwani D, Sneddon J, Malcolm W, Wiuff C, Patton A, Hurding S, Eastaway A, Seaton R, Watson E, Gillies G; Scottish Antimicrobial Prescribing Group (2011) Scottish Antimicrobial Prescribing Group (SAPG): development and impact of the Scottish National Antimicrobial Stewardship Programme. Int J Antimicrob Agents 38:16–26PubMedCrossRefGoogle Scholar
  21. 21.
    Kern WV, Metz-Gercek S, Buyle F, Jindrak V, Lechner A, Mittermayer H, Seifert H, Wechsler-Fördös A, Wenisch C, Zupanc-Leijko T, Mechtler R, Struelens M (2009) Staphylococcus aureus bloodstream infection management indicators as quality indicators for hospital antibiotic stewardship: feasibility study by the ABS International Quality Indicators (ABS QI) team. Abstract of the 19th European Congress of Clinical Microbiology and Infectious Diseases, Helsinki, Finland, May 2009. Abstract number P764Google Scholar
  22. 22.
  23. 23.
    McGowan JE Jr (2012) Antimicrobial stewardship—the state of the art in 2011: focus on outcome and methods. Infect Control Hosp Epidemiol 33(4):331–337PubMedCrossRefGoogle Scholar
  24. 24.
    Malcolm W, Nathwani D, Davey P, Cromwell T, Patton A, Reilly J, Cairns S, Bennie M (2013) From intermittent antibiotic point prevalence surveys to quality improvement: experience in Scottish hospitals. Antimicrob Resist Infect Control 2(1):3PubMedCrossRefGoogle Scholar
  25. 25.
    NSW Therapeutic Advisory Group Inc., Clinical Excellence Commission. Indicators for quality use of medicines in Australian hospitals, Version 1, 2007. Available online at:
  26. 26.
    Morris AM, Brener S, Dresser L, Daneman N, Dellit TH, Avdic E, Bell CM (2012) Use of a structured panel process to define quality metrics for antimicrobial stewardship programs. Infect Control Hosp Epidemiol 33:500–506PubMedCrossRefGoogle Scholar
  27. 27.
    Dumartin C, Rogues AM, Amadeo B, Pefau M, Venier AG, Parneix P, Maurain C (2011) Antibiotic stewardship programmes: legal framework and structure and process indicator in Southwestern French hospitals, 2005–2008. J Hosp Infect 77:123–128PubMedCrossRefGoogle Scholar
  28. 28.
    Rello J, Lode H, Cornaglia G, Masterton R; VAP Care Bundle Contributors (2010) A European care bundle for prevention of ventilator-associated pneumonia. Intensive Care Med 36:773–780PubMedCrossRefGoogle Scholar
  29. 29.
    Pope SD, Dellit TH, Owens RC, Hooton TM; Infectious Diseases Society of America; Society for Healthcare Epidemiology of America (2009) Results of survey on implementation of Infectious Diseases Society of America and Society for Healthcare Epidemiology of America guidelines for developing an institutional program to enhance antimicrobial stewardship. Infect Control Hosp Epidemiol 30:97–98PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • F. M. Buyle
    • 1
  • S. Metz-Gercek
    • 2
  • R. Mechtler
    • 2
  • W. V. Kern
    • 3
  • H. Robays
    • 1
  • D. Vogelaers
    • 4
  • M. J. Struelens
    • 5
  • on behalf of members of the Antibiotic Strategy International (ABS) Quality Indicators Team
  1. 1.Pharmacy DepartmentGhent University HospitalGhentBelgium
  2. 2.Institute for Health System ResearchJohannes Kepler UniversityLinzAustria
  3. 3.Center for Infectious Diseases and Travel MedicineUniversity HospitalFreiburgGermany
  4. 4.Department of Internal Medicine, Infectious Diseases and Psychosomatic MedicineGhent University HospitalGhentBelgium
  5. 5.Microbiology Coordination SectionEuropean Centre for Disease Prevention and Control (ECDC)StockholmSweden

Personalised recommendations