Intensive Care Medicine

, Volume 39, Issue 4, pp 672–681 | Cite as

Potentially resistant microorganisms in intubated patients with hospital-acquired pneumonia: the interaction of ecology, shock and risk factors

  • Ignacio Martin-Loeches
  • Maria Deja
  • Despoina Koulenti
  • George Dimopoulos
  • Brian Marsh
  • Antonio Torres
  • Michael S. Niederman
  • Jordi RelloEmail author
  • EU-VAP Study Investigators



As per 2005 American Thoracic Society and Infectious Disease Society of America (ATS/IDSA) guidelines for managing hospital-acquired pneumonia, patients with early-onset pneumonia and without risk factors do not need to be treated for potentially resistant microorganisms (PRM).


This was a secondary analysis of a prospective, observational, cohort, multicentre study conducted in 27 ICUs from nine European countries.


From a total of 689 patients with nosocomial pneumonia who required mechanical ventilation, 485 patients with confirmed etiology and antibiotic susceptibility were further analysed. Of these patients, 152 (31.3 %) were allocated to group 1 with early-onset pneumonia and no risk factors for PRM acquisition, and 333 (68.7 %) were classified into group 2 with early-onset pneumonia with risk factors for PRM or late-onset pneumonia. Group 2 patients were older and had more chronic renal failure and more severe illness (SAPS II score, 44.6 ± 16.5 vs. 47.4 ± 17.8, p = 0.04) than group 1 patients. Trauma patients were more frequent and surgical patients less frequent in group 1 than in group 2 (p < 0.01). In group 1, 77 patients (50.7 %) had PRM in spite of the absence of classic risk factors recognised by the current guidelines. A logistic regression analysis identified that presence of severe sepsis/septic shock (OR = 3.7, 95 % CI 1.5–8.9) and pneumonia developed in centres with greater than 25 % prevalence of PRM (OR = 11.3, 95 % CI 2.1–59.3) were independently associated with PRM in group 1 patients.


In patients admitted to ICUs with a prevalence of PRM greater than 25 % or with severe sepsis/septic shock, empiric therapy for group 1 nosocomial pneumonia requiring mechanical ventilation should also include agents likely to be effective for PRM pathogens.


HAP VAP Multidrug-resistant organisms Septic shock Guidelines Antibiotic treatment 



Supported by AGAUR 2005/SGR/920, CibeRes 06/06/0036.

Conflicts of interest

The authors declare no conflict of interest regarding the present manuscript.


  1. 1.
    American Thoracic Society (2005) Guidelines for the management of adults with hospital-acquired pneumonia, ventilator-associated pneumonia, and healthcare-associated pneumonia. Am J Respir Crit Care Med 17:388–416Google Scholar
  2. 2.
    Rello J, Gallego M, Mariscal D, Soñora R, Valles J (1997) The value of routine microbial investigation in ventilator-associated pneumonia. Am J Respir Crit Care Med 156:196–200PubMedGoogle Scholar
  3. 3.
    Alvarez-Lerma F, ICU-Acquired Pneumonia Study Group (1996) Modification of empiric antibiotic treatment in patients with pneumonia acquired in the intensive care unit. Intensive Care Med 22:387–394PubMedCrossRefGoogle Scholar
  4. 4.
    Luna CM, Vujacich P, Niederman MS, Vay C, Gherardi C, Matera J, Jolly EC (1997) Impact of BAL data on the therapy and outcome of ventilator-associated pneumonia. Chest 111:676–685PubMedCrossRefGoogle Scholar
  5. 5.
    Vincent JL, Rello J, Marshall J, Silva E, Anzueto A, Martin CD, Moreno R, Lipman J, Gomersall C, Sakr Y, Reinhart K, EPIC II Group of Investigators (2009) International study of the prevalence and outcomes of infection in intensive care units. JAMA 302:2323–2329PubMedCrossRefGoogle Scholar
  6. 6.
    Koulenti D, Lisboa T, Brun-Buisson C, Krueger W, Macor A, Sole-Violan J, Diaz E, Topeli A, DeWaele J, Carneiro A, Martin-Loeches I, Armaganidis A, Rello J, EU-VAP/CAP Study Group (2009) Spectrum of practice in the diagnosis of nosocomial pneumonia in patients requiring mechanical ventilation in European intensive care units. Crit Care Med 37:2360–2368PubMedCrossRefGoogle Scholar
  7. 7.
    Von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP et al (2007) The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. Epidemiology 18:800–804CrossRefGoogle Scholar
  8. 8.
    McCabe JR, Jackson GG (1962) Gram-negative bacteraemia I: etiology and ecology. Arch Intern Med 110:847–855CrossRefGoogle Scholar
  9. 9.
    Le-Gall JR, Lemeshow S, Saulnier F (1993) A new simplified physiology score (SAPS II) based on a European/North American multicentre study. JAMA 270:2957–296314PubMedCrossRefGoogle Scholar
  10. 10.
    American College of Chest Physicians/Society of Critical Care Medicine Consensus Conference (1992) Definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. Crit Care Med 20:864–874CrossRefGoogle Scholar
  11. 11.
    Vincent JL, Moreno R, Takala J, Willatts S, De Mendonça A, Bruining H, Reinhart CK, Suter PM, Thijs LG (1996) The SOFA (Sepsis-related Organ Failure Assessment) score to describe organ dysfunction/failure. Intensive Care Med 22:707–710PubMedCrossRefGoogle Scholar
  12. 12.
    Pugin J, Auckenthaler R, Mili N, Janssens JP, Lew PD, Suter PM (1991) Diagnosis of ventilator–associated pneumonia by bacteriologic analysis of bronchoscopic and non bronchoscopic ‘blind’ bronchoalveolar lavage fluid. Am Rev Respi Dis 143:1121–1129Google Scholar
  13. 13.
    American College of Chest Physicians/Society of Critical Care Medicine Consensus Conference (1992) Definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. Crit Care Med 20:864–874CrossRefGoogle Scholar
  14. 14.
    Chastre J, Fagon JY (2002) Ventilator-associated pneumonia. Am J Respir Crit Care Med 165:867–903PubMedGoogle Scholar
  15. 15.
    Ferrer M, Liapikou A, Valencia M, Esperatti M, Theessen A, Antonio Martinez J, Mensa J, Torres A (2010) Validation of the American Thoracic Society-Infectious Diseases Society of America guidelines for hospital-acquired pneumonia in the intensive care unit. Clin Infect Dis 50:945–952PubMedCrossRefGoogle Scholar
  16. 16.
    Heyland DK, Dodek P, Muscedere J, Day A, Cook D, Canadian Critical Care Trials Group (2008) Randomized trial of combination versus monotherapy for the empiric treatment of suspected ventilator-associated pneumonia. Crit Care Med 36:737–744PubMedCrossRefGoogle Scholar
  17. 17.
    Rello J, Torres A (1996) Microbial causes of ventilator-associated pneumonia. Semin Respir Infect 11:24–31PubMedGoogle Scholar
  18. 18.
    Rello J, Ausina V, Ricart M, Puzo C, Quintana E, Net A, Prats G (1994) Risk factors for infection by Pseudomonas aeruginosa in patients with ventilator-associated pneumonia. Intensive Care Med 20:193–198PubMedCrossRefGoogle Scholar
  19. 19.
    Sirvent JM, Torres A, El-Ebiary M, Castro P, de Batlle J, Bonet A (1997) Protective effect of intravenously administered cefuroxime against nosocomial pneumonia in patients with structural coma. Am J Respir Crit Care Med 155:1729–1734PubMedGoogle Scholar
  20. 20.
    Nseir S, Blazejewski C, Lubret R, Wallet F, Courcol R, Durocher A (2011) Risk of acquiring multidrug-resistant Gram-negative bacilli from prior room occupants in the intensive care unit. Clin Microbiol Infect 17:1201–1208PubMedCrossRefGoogle Scholar
  21. 21.
    Grundmann H, Bärwolff S, Tami A, Behnke M, Schwab F, Geffers C, Halle E, Göbel UB, Schiller R, Jonas D, Klare I, Weist K, Witte W, Beck-Beilecke K, Schumacher M, Rüden H, Gastmeier P (2005) How many infections are caused by patient-to-patient transmission in intensive care units? Crit Care Med 33:946–951PubMedCrossRefGoogle Scholar
  22. 22.
    Rello J, Sa-Borges M, Correa H, Leal SR, Baraibar J (1999) Variations in etiology of ventilator-associated pneumonia across four treatment sites: implications for antimicrobial prescribing practices. Am J Respir Crit Care Med 160:608–613PubMedGoogle Scholar
  23. 23.
    Namias N, Samiian L, Nino D, Shirazi E, O’Neill K, Kett DH, Ginzburg E, McKenney MG, Sleeman D, Cohn SM (2000) Incidence and susceptibility of pathogenic bacteria vary between ICU within a single hospital: implications for empiric antibiotic strategies. J Trauma 49:638–645PubMedCrossRefGoogle Scholar
  24. 24.
    Rello J, Ulldemolins M, Lisboa T, Koulenti D, Mañez R, Martin-Loeches I, De Waele JJ, Putensen C, Guven M, Deja M, Diaz E, EU-VAP/CAP Study Group (2011) Determinants of prescription and choice of empirical therapy for hospital-acquired and ventilator-associated pneumonia. Eur Respir J 37:1332–1339PubMedCrossRefGoogle Scholar
  25. 25.
    Depuydt PO, Vandijck DM, Bekaert MA, Decruyenaere JM, Blot SI, Vogelaers DP, Benoit DD (2008) Determinants and impact of multidrug antibiotic resistance in pathogens causing ventilator-associated-pneumonia. Crit Care 12:R142PubMedCrossRefGoogle Scholar
  26. 26.
    Tseng CC, Liu SF, Wang CC, Tu ML, Chung YH, Lin MC, Fang WF (2012) Impact of clinical severity index, infective pathogens, and initial empiric antibiotic use on hospital mortality in patients with ventilator-associated pneumonia. Am J Infect Control 40(7):648–652PubMedCrossRefGoogle Scholar
  27. 27.
    Damas P, Layios N, Seidel L, Nys M, Melin P, Ledoux D (2011) Severity of ICU-acquired pneumonia according to infectious microorganisms. Intensive Care Med 37:1128–1135PubMedCrossRefGoogle Scholar
  28. 28.
    Kumar A, Safdar N, Kethireddy S, Chateau D (2010) A survival benefit of combination antibiotic therapy for serious infections associated with sepsis and septic shock is contingent only on the risk of death: a meta-analytic/meta-regression study. Crit Care Med 38:1651–1664PubMedCrossRefGoogle Scholar
  29. 29.
    Kollef KE, Schramm GE, Wills AR, Reichley RM, Micek ST, Kollef MH (2008) Predictors of 30-day mortality and hospital costs in patients with ventilator-associated pneumonia attributed to potentially antibiotic-resistant gram-negative bacteria. Chest 134:281–287PubMedCrossRefGoogle Scholar
  30. 30.
    Lisboa T, Diaz E, Sa-Borges M, Socias A, Sole-Violan J, Rodríguez A, Rello J (2008) The ventilator-associated pneumonia PIRO score: a tool for predicting ICU mortality and health-care resources use in ventilator-associated pneumonia. Chest 134:1208–1216PubMedCrossRefGoogle Scholar
  31. 31.
    Kumar A, Roberts D, Wood KE, Light B, Parrillo JE, Sharma S, Suppes R, Feinstein D, Zanotti S, Taiberg L, Gurka D, Kumar A, Cheang M (2006) Duration of hypotension before initiation of effective antimicrobial therapy is the critical determinant of survival in human septic shock. Crit Care Med 34:1589–1596PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg and ESICM 2013

Authors and Affiliations

  • Ignacio Martin-Loeches
    • 1
    • 2
    • 3
    • 12
  • Maria Deja
    • 4
  • Despoina Koulenti
    • 5
  • George Dimopoulos
    • 6
  • Brian Marsh
    • 3
  • Antonio Torres
    • 7
    • 12
  • Michael S. Niederman
    • 8
  • Jordi Rello
    • 9
    • 10
    • 11
    • 12
    Email author
  • EU-VAP Study Investigators
  1. 1.Critical Care CentreCoporació Sanitaria Parc TauliSabadellSpain
  2. 2.Institut Universitari UABBarcelonaSpain
  3. 3.Critical Care DepartmentMater Misericordiae University HospitalDublinIreland
  4. 4.Department of Anesthesiology and Critical Care MedicineCharité Medical Center, Campus Virchow-ClinicBerlinGermany
  5. 5.Critical Care DepartmentUniversity Hospital AttikonHaidariGreece
  6. 6.Department of Critical Care Medicine, University Hospital ATTIKON, Medical SchoolUniversity of AthensAthensGreece
  7. 7.Pneumology Department, Hospital ClinicBarcelonaSpain
  8. 8.Department of MedicineWinthrop-University HospitalMineolaUSA
  9. 9.Critical Care DepartmentHospital Vall d’HebronBarcelonaSpain
  10. 10.Vall d’ Hebron Research Institute (VHIR)BarcelonaSpain
  11. 11.Universitat Autónoma de BarcelonaBarcelonaSpain
  12. 12.CIBERESBarcelonaSpain

Personalised recommendations