Intensive Care Medicine

, Volume 35, Issue 1, pp 91–100 | Cite as

Surveillance of microbial resistance in European Intensive Care Units: a first report from the Care-ICU programme for improved infection control

  • Håkan HanbergerEmail author
  • Dilek Arman
  • Hans Gill
  • Vlastimil Jindrák
  • Smilja Kalenic
  • Andrea Kurcz
  • Monica Licker
  • Paul Naaber
  • Elizabeth A. Scicluna
  • Václav Vanis
  • Sten M. Walther



To report initial results from a European ICU surveillance programme focussing on antibiotic consumption, microbial resistance and infection control.


Thirty-five ICUs participated during 2005. Microbial resistance, antibiotic consumption and infection control stewardship measures were entered locally into a web-application. Results were validated locally, aggregated by project leaders and fed back to support local audit and benchmarking.


Median (range) antibiotic consumption was 1,254 (range 348–4,992) DDD per 1,000 occupied bed days. The proportion of MRSA was median 11.6% (range 0–100), for ESBL phenotype of E. coli and K. pneumoniae 3.9% (0–80) and 14.3% (0–77.8) respectively, and for carbapenem-resistant P. aeruginosa 22.5% (0–100). Screening on admission for alert pathogens was commonly omitted, and there was a lack of single rooms for isolation.


The surveillance programme demonstrated wide variation in antibiotic consumption, microbial resistance and infection control measures. The programme may, by providing rapid access to aggregated results, promote local and regional audit and benchmarking of antibiotic use and infection control practices.


Intensive care Antibiotic consumption Microbial resistance Infection control 



We wish to express our gratitude to all contributors in the CareICU network (see below), Fredrik Husander for web design and Mercedes Palomar and Dominique Monnet for valuable help with design of the questionnaire. The network was funded by the European Commission Directorate General for Health and Consumer Protection (DG SANCO) through the project Improving Patient Safety in Europe (IPSE, Funding was also received from the Swedish Institute for Infectious Disease Control ( Contributors: Ante Sekulic, Kresimir Oremus, Ljiljana Betica Radic, Marina Payerl Pal, Radovan Radonic, and Smilja Kalenic in Croatia; Václav Vaniš and Vlastimil Jindrak in the Czech Republic; Paul Naaber and Piret Mitt in Estonia; Anikó Farkas, Karolina Böröcz, Andrea Kurcz, Piroska Orosi, Erzsébet Rákay and Erika Rauth in Hungary; Elizabeth Scicluna in Malta; Monica Licker in Romania; Anita Johansson, Anne-Li Öhlin Gustafsson, Hans Blomqvist, Jonas Swanberg and Margareta Lannér Sjöberg in Sweden and Cengiz Uzun, Dilek Arman, Davut Ozdemir and Murat Dizbay in Turkey.


  1. 1.
    Vincent JL (2000) Microbial resistance: lessons from the EPIC study European Prevalence of Infection. Intensive Care Med 26(suppl 1):S3–S8PubMedCrossRefGoogle Scholar
  2. 2.
    Hanberger H, Diekema D, Fluit A, Jones R, Struelens M, Spencer R, Wolff M (2001) Surveillance of antibiotic resistance in European ICUs. J Hosp Infect 48:161–176PubMedCrossRefGoogle Scholar
  3. 3.
    Deplano A, Denis O, Poirel L, Hocquet D, Nonhoff C, Byl B, Nordmann P, Vincent JL, Struelens MJ (2005) Molecular characterization of an epidemic clone of panantibiotic-resistant Pseudomonas aeruginosa. J Clin Microbiol 43:1198–1204PubMedCrossRefGoogle Scholar
  4. 4.
    Vincent JL, Sakr Y, Sprung CL, Ranieri VM, Reinhart K, Gerlach H, Moreno R, Carlet J, Le Gall JR, Payen D (2006) Sepsis in European intensive care units: results of the SOAP study. Crit Care Med 34:344–353PubMedCrossRefGoogle Scholar
  5. 5.
    Wroblewska MM, Rudnicka J, Marchel H, Luczak M (2006) Multidrug-resistant bacteria isolated from patients hospitalised in intensive care units. Int J Antimicrob Agents 4:285–289CrossRefGoogle Scholar
  6. 6.
    Gastmeier P, Sohr D, Geffers C, Behnke M, Ruden H (2007) Risk factors for death due to nosocomial infection in intensive care unit patients: findings from the Krankenhaus Infektions Surveillance System. Infect Control Hosp Epidemiol 4:466–472CrossRefGoogle Scholar
  7. 7.
    Hanberger H, Burman LG, Cars O, Erlandsson M, Gill H, Nilsson LE, Nordlinder D, Walther SM, ICU STRAMA Study Group (2007) Low antibiotic resistance rates in Staphylococcus aureus, Escherichia coli and Klebsiella spp but not in Enterobacter spp and Pseudomonas aeruginosa: a prospective observational study in 14 Swedish ICUs over a 5-year period. Acta Anaesthesiol Scand 51:937–941PubMedCrossRefGoogle Scholar
  8. 8.
    Tato M, Coque TM, Ruíz-Garbajosa P, Pintado V, Cobo J, Sader HS, Jones RN, Baquero F, Cantón R (2007) Complex clonal and plasmid epidemiology in the first outbreak of Enterobacteriaceae infection involving VIM-1 metallo-beta-lactamase in Spain: toward endemicity? Clin Infect Dis 45:1171–1178PubMedCrossRefGoogle Scholar
  9. 9.
    Damas P, Ledoux D, Nys M, Monchi M, Wiesen P, Beauve B, Preiser JC (2008) Intensive care unit acquired infection and organ failure. Intensive Care Med 34:856–864PubMedCrossRefGoogle Scholar
  10. 10.
    Brun-Buisson C (2008) ICU-acquired infections and sepsis: more of a deadly duo. Intensive Care Med 34:793–795Google Scholar
  11. 11.
    Monnet DL (2000) Toward multinational antimicrobial resistance surveillance systems in Europe. Int J Antimicrob Agents 15:91–101PubMedCrossRefGoogle Scholar
  12. 12.
    Hanberger H, Arman D, Gill H, Kalenic S, Naaber P, Scicluna E, Suetens C (2008) CARE-ICU—Controlling Antibiotic REsistance in Intensive Care Units—First report from a web-based program for improved infection control in European ICUs. In: Programme of the 18th European congress of clinical microbiology and infectious diseases, BarcelonaGoogle Scholar
  13. 13.
    Hanberger H, Erlandsson M, Burman LG, Cars O, Gill H, Lindgren S, Nilsson LE, Olsson-Liljequist B, Walther S, the ICU-STRAMA Study Group (2004) High antibiotic susceptibility among bacterial pathogens in Swedish ICUs. Report from a nation-wide surveillance program using TA90 as a novel index of susceptibility. Scand J Infect Dis 36:24–30PubMedCrossRefGoogle Scholar
  14. 14.
    Hanberger H, Monnet DL, Nilsson LE (2005) Intensive care unit. In: Gould I, van der Meer J (eds) Antibiotic policies. Theory and practice. Kluwer Academic/Plenum Publishers, New York, pp 261–271CrossRefGoogle Scholar
  15. 15.
    Erlandsson M, Burman LG, Cars O, Gill H, Nilsson LE, Walther SM, Hanberger H, the STRAMA ICU Study Group (2007) Prescription of antibiotic agents in Swedish intensive care units is empiric and precise. Scand J Infect Dis 39:63–69PubMedCrossRefGoogle Scholar
  16. 16.
    de With K, Bergner J, Buhner R, de With K, Bergner J, Bühner R, Dörje F, Gonnermann C, Haber M, Hartmann M, Rothe U, Strehl E, Steib-Bauert M, Kern WV et al (2004) Antibiotic use in German university hospitals 1998–2000 (Project INTERUNI-II). Int J Antimicrob Agents 24:213–221PubMedCrossRefGoogle Scholar
  17. 17.
    Muller A, Monnet DL, Talon D, Hénon T, Bertrand X (2006) Discrepancies between prescribed daily doses and WHO defined daily doses of antibacterials at a university hospital. Br J Clin Pharmacol 61:585–591PubMedCrossRefGoogle Scholar
  18. 18.
    Meyer E, Schwab F, Gastmeier P, Rueden H, Daschner FD, Jonas D (2006) Stenotrophomonas maltophilia and antibiotic use in German intensive care units: data from Project SARI (Surveillance of Antimicrobial Use and Antimicrobial Resistance in German Intensive Care Units). J Hosp Infect 64:238–243PubMedCrossRefGoogle Scholar
  19. 19.
    Loeffler JM, Garbino J, Lew D, Harbarth S, Rohner P (2003) Antibiotic consumption, bacterial resistance and their correlation in a Swiss University Hospital and its adult intensive care units. Scand J Infect Dis 35:843–850PubMedCrossRefGoogle Scholar
  20. 20.
    Lemmen SW, Häfner H, Kotterik S, Lütticken R, Töpper R (2000) Influence of an infectious disease service on antibiotic prescription behaviour and selection of multiresistant pathogens. Infection 28:384–387PubMedCrossRefGoogle Scholar
  21. 21.
    Monnet DL SC, Jepsen OB (2000) Overall antimicrobial use and control strategies in intensive care units from 6 European countries. Abstract; 4th Decennial International Conference on Nosocomial and Healthcare-Associated Infections. CDC/SHEA, AtlantaGoogle Scholar
  22. 22.
    Goldmann DA, Weinstein RA, Wenzel RP, Tablan OC, Duma RJ, Gaynes RP, Schlosser J, Martone WJ (1996) Strategies to prevent and control the emergence and spread of antimicrobial-resistant microorganisms in hospitals. A challenge to hospital leadership. JAMA 275:234–240PubMedCrossRefGoogle Scholar
  23. 23.
    Björholt I, Haglind E (2004) Cost-savings achieved by eradication of epidemic methicillin-resistant Staphylococcus aureus (EMRSA)-16 from a large teaching hospital. Eur J Clin Microbiol Infect Dis 23:688–695PubMedCrossRefGoogle Scholar
  24. 24.
    Lucet J-C, Paoletti X, Lolom I, Paugam-Burtz C, Trouillet J-L, Timsit J-F, Deblangy C, Andremont A, Regnier B (2005) Successful long-term program for controlling methicillin-resistant Staphylococcus aureus in intensive care units. Intensive Care Med 31:1051–1057Google Scholar
  25. 25.
    Raineri E, Crema L, De Silvestri A, Acquarolo A, Albertario F, Carnevale G, Latronico N, Petrosillo N, Tinelli C, Zoncada A, Pan A (2007) Meticillin-resistant Staphylococcus aureus control in an intensive care unit: a 10 year analysis. J Hosp Infect 67:308–315PubMedCrossRefGoogle Scholar
  26. 26.
    Nulens E, Broex E, Ament A, Deurenberg RH, Smeets E, Scheres J, van Tiel FH, Gordts B, Stobberingh EE (2008) Cost of the meticillin-resistant Staphylococcus aureus search and destroy policy in a Dutch University Hospital. J Hosp Infect 68:301–307PubMedCrossRefGoogle Scholar
  27. 27.
    Harbarth S, Fankhauser C, Schrenzel J, Christenson J, Gervaz P, Bandiera-Clerc C, Renzi G, Vernaz N, Sax H, Pittet D (2008) Universal screening for methicillin-resistant Staphylococcus aureus at hospital admission and nosocomial infection in surgical patients. JAMA 299:1149–1157PubMedCrossRefGoogle Scholar
  28. 28.
    Cepeda JA, Whitehouse T, Cooper B, Hails J, Jones K, Kwaku F, Taylor L, Hayman S, Cookson B, Shaw S, Kibbler C, Singer M, Bellingan G, Wilson AP (2005) Isolation of patients in single rooms or cohorts to reduce spread of MRSA in intensive-care units: prospective two-centre study. Lancet 365:295–304PubMedGoogle Scholar
  29. 29.
    Humphreys H (2008) Can we do better in controlling and preventing methicillin-resistant Staphylococcus aureus (MRSA) in the intensive care unit (ICU)? Eur J Clin Microbiol Infect Dis 27:409–413 Feb 13 (Epub ahead of print)PubMedCrossRefGoogle Scholar
  30. 30.
    Landman D, Bratu S, Alam M, Quale J (2005) Citywide emergence of Pseudomonas aeruginosa strains with reduced susceptibility to polymyxin B. J Antimicrob Chemother 55:954–957PubMedCrossRefGoogle Scholar
  31. 31.
    Falagas ME, Bliziotis IA (2007) Pandrug-resistant Gram-negative bacteria: the dawn of the post-antibiotic era? Int J Antimicrob Agents 29:630–636PubMedCrossRefGoogle Scholar
  32. 32.
    Jonas D, Meyer E, Schwab F, Grundmann H (2008) Genodiversity of resistant Pseudomonas aeruginosa isolates in relation to antimicrobial usage density and resistance rates in intensive care units. Infect Control Hosp Epidemiol 29:350–357PubMedCrossRefGoogle Scholar
  33. 33.
    Carmeli Y, Troillet N, Eliopoulos GM, Samore MH (1999) Emergence of antibiotic-resistant Pseudomonas aeruginosa: comparison of risks associated with different anti-pseudomonal agents. Antimicrob Agents Chemother 43:1379–1382PubMedGoogle Scholar
  34. 34.
    Peña C, Guzmán A, Suarez C, Dominguez MA, Tubau F, Pujol M, Gudiol F, Ariza J (2007) Effects of carbapenem exposure on the risk for digestive tract carriage of intensive care unit-endemic carbapenem-resistant Pseudomonas aeruginosa strains in critically ill patients. Antimicrob Agents Chemother 51:1967–1971PubMedCrossRefGoogle Scholar
  35. 35.
    Erlandsson M, Gill H, Nilsson LE, Giske, Jonas, Nordlinder D, Walther SM, Hanberger H (2008) Antibiotic susceptibility patterns and clones of Pseudomonas aeruginosa from patients in Swedish ICUs. Scand J Infect Dis 40:487–494Google Scholar
  36. 36.
    Bonten MJ, Weinstein RA (2006) Antibiotic cycling in intensive care units: the value of organized chaos? Crit Care Med 34:549–551PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Håkan Hanberger
    • 1
    • 13
    Email author
  • Dilek Arman
    • 2
  • Hans Gill
    • 3
  • Vlastimil Jindrák
    • 4
  • Smilja Kalenic
    • 5
  • Andrea Kurcz
    • 6
  • Monica Licker
    • 7
  • Paul Naaber
    • 8
  • Elizabeth A. Scicluna
    • 9
  • Václav Vanis
    • 4
  • Sten M. Walther
    • 10
    • 11
    • 12
  1. 1.Swedish Institute for Infectious Disease ControlSolnaSweden
  2. 2.Department of Clinical Microbiology and Infectious DiseasesGazi University School of MedicineAnkaraTurkey
  3. 3.Medical Informatics, Department of Biomedical EngineeringLinköpings UniversitetLinköpingSweden
  4. 4.Department of Clinical Microbiology Antibiotic CentreNa Homolce HospitalPrahaCzech Republic
  5. 5.Reference Centre for Hospital Infections, Clinical Hospital CentreZagrebCroatia
  6. 6.National Centre for EpidemiologiaBudapestHungary
  7. 7.Department of Microbiology“Victor Babes” University of Medicine and PharmacyTimisoaraRomania
  8. 8.Department of Clinical Microbiology, United LaboratoriesTartu University ClinicsTartuEstonia
  9. 9.Infection Control UnitMater Dei HospitalMsidaMalta 
  10. 10.Department of Cardiovascular Anaesthesia and Intensive Care Linköping University HospitalLinköpingSweden
  11. 11.Division of Cardiovascular Medicine, Department of Medical and Health Sciences, Faculty of Health Sciences Linköpings UniversitetLinköpingSweden
  12. 12.Depatment of Anaesthesia, Faculty Division Ullevaal University Hospital, Faculty of MedicineUniversity of OsloOsloNorway
  13. 13.Division of Infectious Diseases, Institution of Clinical and Experimental Medicine, Faculty of Health SciencesLinköpings UniversitetLinköpingSweden

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