Intensive Care Medicine

, Volume 34, Issue 2, pp 292–299 | Cite as

Candidemia and candiduria in critically ill patients admitted to intensive care units in France: incidence, molecular diversity, management and outcome

  • Marie-Elisabeth Bougnoux
  • Guillaume Kac
  • Philippe Aegerter
  • Christophe d’Enfert
  • Jean-Yves Fagon
  • CandiRea Study Group
Original

Abstract

Objective

To determine the concomitant incidence, molecular diversity, management and outcome of nosocomial candidemia and candiduria in intensive care unit (ICU) patients in France.

Design

A 1-year prospective observational study in 24 adult ICUs.

Patients

Two hundred and sixty-two patients with nosocomial candidemia and/or candiduria.

Measurements and results

Blood and urine samples were collected when signs of sepsis were present. Antifungal susceptibility of Candida strains was determined; in addition, all blood and 72% of urine C. albicans isolates were analyzed by using multi-locus sequence type (MLST). The mean incidences of candidemia and candiduria were 6.7 and 27.4/1000 admissions, respectively. Eight percent of candiduric patients developed candidemia with the same species. The mean interval between ICU admission and candidemia was 19.0 ± 2.9 days, and 17.2 ± 1.1 days for candiduria. C. albicans and C. glabrata were isolated in 54.2% and 17% of blood and 66.5% and 21.6% of urine Candida-positive cultures, respectively. Fluconazole was the most frequently prescribed agent. In all candidemic patients, the prescribed curative antifungal agent was active in vitro against the responsible identified strain. Crude ICU mortality was 61.8% for candidemic and 31.3% for candiduric patients. Seventy-five percent of the patients were infected with a unique C. albicans strain; cross-transmission between seven patients was suggested in one hospital.

Conclusions

Candidemia is late-onset ICU-acquired infection associated with high mortality. No difference in susceptibility and genetic background were found between blood and urine strains of Candida species.

Keywords

Candidemia Candiduria Nosocomial infections Critically ill patients Molecular typing 

Supplementary material

134_2007_865_MOESM1_ESM.doc (37 kb)
Electronic Supplementary Material (DOC 37K)
134_2007_865_MOESM2_ESM.ppt (78 kb)
Electronic Supplementary Material (PPT 80K)

References

  1. 1.
    Martin GS, Mannino DM, Eaton S, Moss M (2003) The epidemiology of sepsis in the United States from 1979 through 2000. N Engl J Med 348:1546–1554PubMedCrossRefGoogle Scholar
  2. 2.
    Richards MJ, Edwards JR, Culver DH, Gaynes RP, the National Nosocomial Infections Surveillance System (1999) Nosocomial infections in medical intensive care units in the United States. Crit Care Med 27:887–892PubMedCrossRefGoogle Scholar
  3. 3.
    Wisplinghoff H, Bischoff T, Tallent SM, Seifert H, Wenzel RP, Edmond MB (2004) Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin Infect Dis 39:309–317PubMedCrossRefGoogle Scholar
  4. 4.
    Pfaller MA, Diekema DJ (2007) Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev 20:133–163PubMedCrossRefGoogle Scholar
  5. 5.
    Eggimann P, Garbino J, Pittet D (2003) Epidemiology of Candida species infections in critically ill non-immunosuppressed patients. Lancet Infect Dis 3:685–702PubMedCrossRefGoogle Scholar
  6. 6.
    Wenzel RP, Gennings C (2005) Bloodstream infections due to Candida species in the intensive care unit: identifying especially high-risk patients to determine prevention strategies. Clin Infect Dis 41 Suppl 6:S389–393CrossRefGoogle Scholar
  7. 7.
    Zaoutis TE, Argon J, Chu J, Berlin JA, Walsh TJ, Feudtner C (2005) The epidemiology and attributable outcomes of candidemia in adults and children hospitalized in the United States: a propensity analysis. Clin Infect Dis 41:1232–1239PubMedCrossRefGoogle Scholar
  8. 8.
    Gudlaugsson O, Gillespie S, Lee K, Vande Berg J, Hu J, Messer S, Herwaldt L, Pfaller M, Diekema D (2003) Attributable mortality of nosocomial candidemia, revisited. Clin Infect Dis 37:1172–1177PubMedCrossRefGoogle Scholar
  9. 9.
    Wey SB, Mori M, Pfaller MA, Woolson RF, Wenzel RP (1988) Hospital-acquired candidemia: the attributable mortality and excess length of stay. Arch Intern Med 148:2642–2645PubMedCrossRefGoogle Scholar
  10. 10.
    Fridkin SK, Jarvis WR (1996) Epidemiology of nosocomial fungal infections. Clin Microbiol Rev 9:499–511PubMedGoogle Scholar
  11. 11.
    Edmond MB, Wallace SE, McClish DK, Pfaller MA, Jones RN, Wenzel RP (1999) Nosocomial bloodstream infections in United States hospitals: a three-year analysis. Clin Infect Dis 29:239–244PubMedCrossRefGoogle Scholar
  12. 12.
    Blumberg HM, Jarvis WR, Soucie JM, Edwards JE, Patterson JE, Pfaller MA, Rangel-Frausto MS, Rinaldi MG, Saiman L, Wiblin RT, Wenzel RP (2001) Risk factors for candidal bloodstream infections in surgical intensive care unit patients: the NEMIS prospective multicenter study. The National Epidemiology of Mycosis Survey. Clin Infect Dis 33:177–186PubMedCrossRefGoogle Scholar
  13. 13.
    Harris AD, Castro J, Sheppard DC, Carmeli Y, Samore MH (1999) Risk factors for nosocomial candiduria due to Candida glabrata and Candida albicans. Clin Infect Dis 29:926–928PubMedCrossRefGoogle Scholar
  14. 14.
    Kauffman CA (2005) Candiduria. Clin Infect Dis 41 Suppl 6:S371–376CrossRefGoogle Scholar
  15. 15.
    Kauffman CA (2006) Fungal infections. Proc Am Thorac Soc 3:35–40PubMedCrossRefGoogle Scholar
  16. 16.
    Pappas PG, Andes D, Schuster M, Hadley S, Rabkin J, Merion RM, Kauffman CA, Huckabee C, Cloud GA, Dismukes WE, Karchmer AW (2006) Invasive fungal infections in low-risk liver transplant recipients: a multi-center prospective observational study. Am J Transplant 6:386–391PubMedCrossRefGoogle Scholar
  17. 17.
    Bougnoux ME, Morand S, d'Enfert C (2002) Usefulness of multilocus sequence typing for characterization of clinical isolates of Candida albicans. J Clin Microbiol 40:1290–1297PubMedCrossRefGoogle Scholar
  18. 18.
    Le Gall JR, Lemeshow S, Saulnier F (1993) A new Simplified Acute Physiology Score (SAPS II) based on a European/North American multicenter study. JAMA 270:2957–2963PubMedCrossRefGoogle Scholar
  19. 19.
    Brun-Buisson C, Abrouk F, Legrand P, Huet Y, Larabi S, Rapin M (1987) Diagnosis of central venous catheter-related sepsis. Critical level of quantitative tip cultures. Arch Intern Med 147:873–877PubMedCrossRefGoogle Scholar
  20. 20.
    Chryssanthou E, Cuenca-Estrella M (2002) Comparison of the Antifungal Susceptibility Testing Subcommittee of the European Committee on Antibiotic Susceptibility Testing proposed standard and the E-test with the NCCLS broth microdilution method for voriconazole and caspofungin susceptibility testing of yeast species. J Clin Microbiol 40:3841–3844PubMedCrossRefGoogle Scholar
  21. 21.
    Rex JH, Pfaller MA, Galgiani JN, Bartlett MS, Espinel-Ingroff A, Ghannoum MA, Lancaster M, Odds FC, Rinaldi MG, Walsh TJ, Barry AL (1997) Development of interpretive breakpoints for antifungal susceptibility testing: conceptual framework and analysis of in vitro-in vivo correlation data for fluconazole, itraconazole, and candida infections. Subcommittee on Antifungal Susceptibility Testing of the National Committee for Clinical Laboratory Standards. Clin Infect Dis 24:235–247PubMedGoogle Scholar
  22. 22.
    Pfaller MA, Diekema DJ, Rex JH, Espinel-Ingroff A, Johnson EM, Andes D, Chaturvedi V, Ghannoum MA, Odds FC, Rinaldi MG, Sheehan DJ, Troke P, Walsh TJ, Warnock DW (2006) Correlation of MIC with outcome for Candida species tested against voriconazole: analysis and proposal for interpretive breakpoints. J Clin Microbiol 44:819–826PubMedCrossRefGoogle Scholar
  23. 23.
    Deresinski SC, Stevens DA (2003) Caspofungin. Clin Infect Dis 36:1445–1457PubMedCrossRefGoogle Scholar
  24. 24.
    Pujol C, Pfaller M, Soll DR (2002) Ca3 fingerprinting of Candida albicans bloodstream isolates from the United States, Canada, South America, and Europe reveals a European clade. J Clin Microbiol 40:2729–2740PubMedCrossRefGoogle Scholar
  25. 25.
    Bougnoux ME, Aanensen DM, Morand S, Theraud M, Spratt BG, d'Enfert C (2004) Multilocus sequence typing of Candida albicans: strategies, data exchange and applications. Infect Genet Evol 4:243–252PubMedCrossRefGoogle Scholar
  26. 26.
    Blignaut E, Pujol C, Lockhart S, Joly S, Soll DR (2002) Ca3 fingerprinting of Candida albicans isolates from human immunodeficiency virus-positive and healthy individuals reveals a new clade in South Africa. J Clin Microbiol 40:826–836PubMedCrossRefGoogle Scholar
  27. 27.
    Richet H, Roux P, Des Champs C, Esnault Y, Andremont A (2002) Candidemia in French hospitals: incidence rates and characteristics. Clin Microbiol Infect 8:405–412PubMedCrossRefGoogle Scholar
  28. 28.
    Almirante B, Rodriguez D, Park BJ, Cuenca-Estrella M, Planes AM, Almela M, Mensa J, Sanchez F, Ayats J, Gimenez M, Saballs P, Fridkin SK, Morgan J, Rodriguez-Tudela JL, Warnock DW, Pahissa A (2005) Epidemiology and predictors of mortality in cases of Candida bloodstream infection: results from population-based surveillance, barcelona, Spain, from 2002 to 2003. J Clin Microbiol 43:1829–1835PubMedCrossRefGoogle Scholar
  29. 29.
    Alvarez-Lerma F, Nolla-Salas J, Leon C, Palomar M, Jorda R, Carrasco N, Bobillo F (2003) Candiduria in critically ill patients admitted to intensive care medical units. Intensive Care Med 29:1069–1076PubMedCrossRefGoogle Scholar
  30. 30.
    Garbino J, Lew DP, Romand JA, Hugonnet S, Auckenthaler R, Pittet D (2002) Prevention of severe Candida infections in nonneutropenic, high-risk, critically ill patients: a randomized, double-blind, placebo-controlled trial in patients treated by selective digestive decontamination. Intensive Care Med 28:1708–1717PubMedCrossRefGoogle Scholar
  31. 31.
    Kauffman CA, Vazquez JA, Sobel JD, Gallis HA, McKinsey DS, Karchmer AW, Sugar AM, Sharkey PK, Wise GJ, Mangi R, Mosher A, Lee JY, Dismukes WE (2000) Prospective multicenter surveillance study of funguria in hospitalized patients. The National Institute for Allergy and Infectious Diseases (NIAID) Mycoses Study Group. Clin Infect Dis 30:14–18PubMedCrossRefGoogle Scholar
  32. 32.
    Blot SI, Vandewoude KH, Hoste EA, Colardyn FA (2002) Effects of nosocomial candidemia on outcomes of critically ill patients. Am J Med 113:480–485PubMedCrossRefGoogle Scholar
  33. 33.
    Cuenca-Estrella M, Rodriguez D, Almirante B, Morgan J, Planes AM, Almela M, Mensa J, Sanchez F, Ayats J, Gimenez M, Salvado M, Warnock DW, Pahissa A, Rodriguez-Tudela JL (2005) In vitro susceptibilities of bloodstream isolates of Candida species to six antifungal agents: results from a population-based active surveillance programme, Barcelona, Spain, 2002–2003. J Antimicrob Chemother 55:194–199PubMedCrossRefGoogle Scholar
  34. 34.
    Antoniadou A, Torres HA, Lewis RE, Thornby J, Bodey GP, Tarrand JP, Han XY, Rolston KV, Safdar A, Raad II, Kontoyiannis DP (2003) Candidemia in a tertiary care cancer center: in vitro susceptibility and its association with outcome of initial antifungal therapy. Medicine (Baltimore) 82:309–321CrossRefGoogle Scholar
  35. 35.
    Almirante B, Rodriguez D, Cuenca-Estrella M, Almela M, Sanchez F, Ayats J, Alonso-Tarres C, Rodriguez-Tudela JL, Pahissa A (2006) Epidemiology, risk factors, and prognosis of Candida parapsilosis bloodstream infections: case–control population-based surveillance study of patients in Barcelona, Spain, from 2002 to 2003. J Clin Microbiol 44:1681–1685PubMedCrossRefGoogle Scholar
  36. 36.
    Rodriguez D, Almirante B, Park BJ, Cuenca-Estrella M, Planes AM, Sanchez F, Gene A, Xercavins M, Fontanals D, Rodriguez-Tudela JL, Warnock DW, Pahissa A (2006) Candidemia in neonatal intensive care units: Barcelona, Spain. Pediatr Infect Dis J 25:224–229PubMedCrossRefGoogle Scholar
  37. 37.
    Vazquez JA, Sanchez V, Dmuchowski C, Dembry LM, Sobel JD, Zervos MJ (1993) Nosocomial acquisition of Candida albicans: an epidemiologic study. J Infect Dis 168:195–201PubMedGoogle Scholar
  38. 38.
    Barchiesi F, Caggiano G, Falconi Di Francesco L, Montagna MT, Barbuti S, Scalise G (2004) Outbreak of fungemia due to Candida parapsilosis in a pediatric oncology unit. Diagn Microbiol Infect Dis 49:269–271PubMedCrossRefGoogle Scholar
  39. 39.
    Roilides E, Farmaki E, Evdoridou J, Francesconi A, Kasai M, Filioti J, Tsivitanidou M, Sofianou D, Kremenopoulos G, Walsh TJ (2003) Candida tropicalis in a neonatal intensive care unit: epidemiologic and molecular analysis of an outbreak of infection with an uncommon neonatal pathogen. J Clin Microbiol 41:735–741PubMedCrossRefGoogle Scholar
  40. 40.
    Lemaitre N, Sougakoff W, Masmoudi A, Fievet MH, Bismuth R, Jarlier V (1998) Characterization of gentamicin-susceptible strains of methicillin-resistant Staphylococcus aureus involved in nosocomial spread. J Clin Microbiol 36:81–85PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Marie-Elisabeth Bougnoux
    • 1
    • 2
    • 3
    • 4
    • 5
  • Guillaume Kac
    • 3
    • 6
  • Philippe Aegerter
    • 3
    • 7
  • Christophe d’Enfert
    • 4
  • Jean-Yves Fagon
    • 3
    • 5
    • 8
  • CandiRea Study Group
  1. 1.Service de Bactériologie, Virologie, Parasitologie et HygièneHôpital Necker-Enfants MaladesParis Cedex 15France
  2. 2.Laboratoire de Parasitologie–Mycologie, Service de MicrobiologieHôpital Necker Enfants MaladesParisFrance
  3. 3.Assistance PubliqueHôpitaux de ParisParisFrance
  4. 4.Unité Biologie et Pathogénicité Fongiques, INRA USC 2019Institut PasteurParisFrance
  5. 5.Faculté de MédecineUniversité René DescartesParisFrance
  6. 6.Unité d’Hygiène HospitalièreHôpital Européen Georges PompidouParisFrance
  7. 7.Informatique MédicaleHôpital Ambroise-ParéBoulogne BillancourtFrance
  8. 8.Service de Réanimation MédicaleHôpital Européen Georges PompidouParisFrance

Personalised recommendations