Intensive Care Medicine

, Volume 41, Issue 2, pp 285–295 | Cite as

Incidence, characteristics and outcome of ICU-acquired candidemia in India

  • Arunaloke ChakrabartiEmail author
  • Prashant Sood
  • Shivaprakash M. Rudramurthy
  • Sharon Chen
  • Harsimran Kaur
  • Malini Capoor
  • Deepinder Chhina
  • Ratna Rao
  • Vandana Kalwaje Eshwara
  • Immaculata Xess
  • Anupama J. Kindo
  • P. Umabala
  • Jayanthi Savio
  • Atul Patel
  • Ujjwayini Ray
  • Sangeetha Mohan
  • Ranganathan Iyer
  • Jagdish Chander
  • Anita Arora
  • Raman Sardana
  • Indranil Roy
  • B. Appalaraju
  • Ajanta Sharma
  • Anjali Shetty
  • Neelam Khanna
  • Rungmei Marak
  • Sanjay Biswas
  • Shukla Das
  • B. N. Harish
  • Sangeeta Joshi
  • Deepak Mendiratta



A systematic epidemiological study on intensive care unit (ICU)-acquired candidemia across India.


A prospective, nationwide, multicentric, observational study was conducted at 27 Indian ICUs. Consecutive patients who acquired candidemia after ICU admission were enrolled during April 2011 through September 2012. Clinical and laboratory variables of these patients were recorded. The present study is an analysis of data specific for adult patients.


Among 1,400 ICU-acquired candidemia cases (overall incidence of 6.51 cases/1,000 ICU admission), 65.2 % were adult. Though the study confirmed the already known risk factors for candidemia, the acquisition occurred early after admission to ICU (median 8 days; interquartile range 4–15 days), even infecting patients with lower APACHE II score at admission (median 17.0; mean ± SD 17.2 ± 5.9; interquartile range 14–20). The important finding of the study was the vast spectrum of agents (31 Candida species) causing candidemia and a high rate of isolation of Candida tropicalis (41.6 %). Azole and multidrug resistance were seen in 11.8 and 1.9 % of isolates. Public sector hospitals reported a significantly higher presence of the relatively resistant C. auris (8.2 vs. 3.9 %; p = 0.008) and C. rugosa (5.6 vs. 1.5 %; p = 0.001). The 30-day crude and attributable mortality rates of candidemia patients were 44.7 and 19.6 %, respectively. Logistic regression analysis revealed significant independent predictors of mortality including admission to public sector hospital, APACHE II score at admission, underlying renal failure, central venous catheterization and steroid therapy.


The study highlighted a high burden of candidemia in Indian ICUs, early onset after ICU admission, higher risk despite less severe physiology score at admission and a vast spectrum of agents causing the disease with predominance of C. tropicalis.


Candidemia Intensive care unit Candida tropicalis Risk factor Mortality 



We wish to acknowledge Prof. Niranjan Nayak, President SIHAM for providing us invaluable logistic support and continuous encouragement to accomplish this study. Other members of the SIHAM Candidemia Network include (participating centres in parenthesis; in alphabetical order): Purva Mathur (All India Institute of Medical Sciences, New Delhi, India); Ratnamani (Apollo Hospital, Hyderabad, India); Aroma Oberoi, Ashu Sara Mathai (Christian Medical College and Hospital, Ludhiana, India); Shweta Sharma (Fortis Escorts Heart Institute, New Delhi, India); DC Thamke (Mahatma Gandhi Institute of Medical Sciences, Wardha, India); A Krishna Prasad (Nizam’s Institute of Medical Sciences, Hyderabad, India); Camilla Rodrigues, Mahesh Lakhe, Mehul Panchal, Niyati Desai (PD Hinduja, Mumbai, India); Gagandeep Singh, Ashutosh Nath Aggarwal, Neerja Bhardwaj, L N Yaddanapudi, Joseph Jillwin, A Shamnath (Postgraduate Institute of Medical Education and Research, Chandigarh); Pradeep Kumar Verma, Harish Chand Sachdeva (Safdarjang Hospital, New Delhi, India); Sriram Sampath (St John’s Medical College, Bangalore, India) are also acknowledged for their help. This work was supported by the MSD Pharmaceuticals Pvt. Ltd Educational Grant through the Society for Indian Human and Animal Mycologists, an affiliate of the International Society of Human and Animal Mycology. MSD did not play any role in study design, data analysis or manuscript writing.

Conflicts of interest

The authors declare that they have no conflicts of interest and no financial relationship with the funding agency.

Supplementary material

134_2014_3603_MOESM1_ESM.docx (25 kb)
Supplementary material 1 (DOCX 25 kb)
134_2014_3603_MOESM2_ESM.tif (209 kb)
Supplementary material 2 (TIFF 208 kb)


  1. 1.
    Meyer E, Geffers C, Gastmeier P et al (2013) No increase in primary nosocomial candidemia in 682 German intensive care units during 2006–2011. Euro Surveill 18(24):20505PubMedGoogle Scholar
  2. 2.
    Gonzalez de Molina FJ, Leon C, Ruiz-Santana S et al (2012) Assessment of candidemia-attributable mortality in critically ill patients using propensity score matching analysis. Crit Care 16(3):R105PubMedCentralPubMedCrossRefGoogle Scholar
  3. 3.
    Nolla-Salas J, Sitges-Serra A, Leon-Gil C et al (1997) Candidemia in non-neutropenic critically ill patients: analysis of prognostic factors and assessment of systemic antifungal therapy. Study group of fungal infection in the ICU. Intensive Care Med 23(1):23–30PubMedCrossRefGoogle Scholar
  4. 4.
    Charles PE, Doise JM, Quenot JP et al (2003) Candidemia in critically ill patients: difference of outcome between medical and surgical patients. Intensive Care Med 29(12):2162–2169PubMedCrossRefGoogle Scholar
  5. 5.
    Guery BP, Arendrup MC, Auzinger G et al (2009) Management of invasive candidiasis and candidemia in adult non-neutropenic intensive care unit patients: part I. Epidemiology and diagnosis. Intensive Care Med 35(1):55–62PubMedCrossRefGoogle Scholar
  6. 6.
    Lass-Florl C (2009) The changing face of epidemiology of invasive fungal disease in Europe. Mycoses 52(3):197–205PubMedCrossRefGoogle Scholar
  7. 7.
    Pfaller MA, Diekema DJ (2007) Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev 20(1):133–163PubMedCentralPubMedCrossRefGoogle Scholar
  8. 8.
    Maubon D, Garnaud C, Calandra T et al (2014) Resistance of Candida spp. to antifungal drugs in the ICU: where are we now? Intensive Care Med 40(9):1241–1255PubMedCrossRefGoogle Scholar
  9. 9.
    CLSI (2008) Reference method for broth dilution antifungal susceptibility testing of yeasts, approved standard. CLSI document M27-A3, 3rd edn. Clinical and Laboratory Standards Institute (CLSI), Wayne, PAGoogle Scholar
  10. 10.
    CLSI (2012) Reference method for broth dilution antifungal susceptibility testing of yeasts, fourth informational supplement. CLSI document M27-S4. Clinical and Laboratory Standards Institute, Wayne, PAGoogle Scholar
  11. 11.
    Playford EG, Marriott D, Nguyen Q et al (2008) Candidemia in nonneutropenic critically ill patients: risk factors for non-albicans Candida spp. Crit Care Med 36(7):2034–2039PubMedCrossRefGoogle Scholar
  12. 12.
    Leroy G, Lambiotte F, Thevenin D et al (2011) Evaluation of Candida score in critically ill patients: a prospective, multicenter, observational, cohort study. Ann Intensive Care 1(1):50PubMedCentralPubMedCrossRefGoogle Scholar
  13. 13.
    Kett DH, Azoulay E, Echeverria PM et al (2011) Candida bloodstream infections in intensive care units: analysis of the extended prevalence of infection in intensive care unit study. Crit Care Med 39(4):665–670PubMedCrossRefGoogle Scholar
  14. 14.
    Bassetti M, Merelli M, Righi E et al (2013) Epidemiology, species distribution, antifungal susceptibility, and outcome of candidemia across five sites in Italy and Spain. J Clin Microbiol 51(12):4167–4172PubMedCentralPubMedCrossRefGoogle Scholar
  15. 15.
    Chow JK, Golan Y, Ruthazer R et al (2008) Risk factors for albicans and non-albicans candidemia in the intensive care unit. Crit Care Med 36(7):1993–1998PubMedCrossRefGoogle Scholar
  16. 16.
    Leroy O, Gangneux JP, Montravers P et al (2009) Epidemiology, management, and risk factors for death of invasive Candida infections in critical care: a multicenter, prospective, observational study in France (2005–2006). Crit Care Med 37(5):1612–1618PubMedCrossRefGoogle Scholar
  17. 17.
    Pappas PG, Rex JH, Lee J et al (2003) A prospective observational study of candidemia: epidemiology, therapy, and influences on mortality in hospitalized adult and pediatric patients. Clin Infect Dis 37(5):634–643PubMedCrossRefGoogle Scholar
  18. 18.
    Chen S, Slavin M, Nguyen Q et al (2006) Active surveillance for candidemia, Australia. Emerg Infect Dis 12(10):1508–1516PubMedCentralPubMedCrossRefGoogle Scholar
  19. 19.
    Leroy O, Mira JP, Montravers P et al (2010) Comparison of albicans vs. non-albicans candidemia in French intensive care units. Crit Care 14(3):R98PubMedCentralPubMedCrossRefGoogle Scholar
  20. 20.
    Pfaller MA, Messer SA, Moet GJ et al (2011) Candida bloodstream infections: comparison of species distribution and resistance to echinocandin and azole antifungal agents in intensive care unit (ICU) and non-ICU settings in the SENTRY antimicrobial surveillance program (2008–2009). Int J Antimicrob Agents 38(1):65–69PubMedCrossRefGoogle Scholar
  21. 21.
    White MH (1997) The contribution of fluconazole to the changing epidemiology of invasive candidal infections. Clin Infect Dis 24(6):1129–1130PubMedCrossRefGoogle Scholar
  22. 22.
    Lortholary O, Renaudat C, Sitbon K et al (2014) Worrisome trends in incidence and mortality of candidemia in intensive care units (Paris area, 2002–2010). Intensive Care Med 40(9):1303–1312PubMedCentralPubMedCrossRefGoogle Scholar
  23. 23.
    Chakrabarti A, Chatterjee SS, Rao KL et al (2009) Recent experience with fungaemia: change in species distribution and azole resistance. Scand J Infect Dis 41(4):275–284PubMedCrossRefGoogle Scholar
  24. 24.
    Mootsikapun P, Hsueh PR, Talwar D et al (2013) Intravenous anidulafungin followed optionally by oral voriconazole for the treatment of candidemia in Asian patients: results from an open-label phase III trial. BMC Infect Dis 13:219PubMedCentralPubMedCrossRefGoogle Scholar
  25. 25.
    Fournier P, Schwebel C, Maubon D et al (2011) Antifungal use influences Candida species distribution and susceptibility in the intensive care unit. J Antimicrob Chemother 66(12):2880–2886PubMedCrossRefGoogle Scholar
  26. 26.
    Blot S, Janssens R, Claeys G et al (2006) Effect of fluconazole consumption on long-term trends in candidal ecology. J Antimicrob Chemother 58(2):474–477PubMedCrossRefGoogle Scholar
  27. 27.
    Lockhart SR, Messer SA, Gherna M et al (2009) Identification of Candida nivariensis and Candida bracarensis in a large global collection of Candida glabrata isolates: comparison to the literature. J Clin Microbiol 47(4):1216–1217PubMedCentralPubMedCrossRefGoogle Scholar
  28. 28.
    Leon C, Ostrosky-Zeichner L, Schuster M (2014) What’s new in the clinical and diagnostic management of invasive candidiasis in critically ill patients. Intensive Care Med 40(6):808–819PubMedCrossRefGoogle Scholar
  29. 29.
    Blot SI, Vandewoude KH, Hoste EA et al (2002) Effects of nosocomial candidemia on outcomes of critically ill patients. Am J Med 113(6):480–485PubMedCrossRefGoogle Scholar
  30. 30.
    Nucci M, Anaissie E, Betts RF et al (2010) Early removal of central venous catheter in patients with candidemia does not improve outcome: analysis of 842 patients from 2 randomized clinical trials. Clin Infect Dis 51(3):295–303PubMedCrossRefGoogle Scholar
  31. 31.
    Gudlaugsson O, Gillespie S, Lee K et al (2003) Attributable mortality of nosocomial candidemia, revisited. Clin Infect Dis 37(9):1172–1177PubMedCrossRefGoogle Scholar
  32. 32.
    Das I, Nightingale P, Patel M et al (2011) Epidemiology, clinical characteristics, and outcome of candidemia: experience in a tertiary referral center in the UK. Int J Infect Dis 15(11):e759–e763PubMedCrossRefGoogle Scholar
  33. 33.
    Colombo AL, Guimaraes T, Sukienik T et al (2014) Prognostic factors and historical trends in the epidemiology of candidemia in critically ill patients: an analysis of five multicenter studies sequentially conducted over a 9-year period. Intensive Care Med 40(10):1489–1498PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg and ESICM 2014

Authors and Affiliations

  • Arunaloke Chakrabarti
    • 1
    • 2
    Email author
  • Prashant Sood
    • 1
  • Shivaprakash M. Rudramurthy
    • 1
  • Sharon Chen
    • 3
  • Harsimran Kaur
    • 1
  • Malini Capoor
    • 4
  • Deepinder Chhina
    • 5
  • Ratna Rao
    • 6
  • Vandana Kalwaje Eshwara
    • 7
  • Immaculata Xess
    • 8
  • Anupama J. Kindo
    • 9
  • P. Umabala
    • 10
  • Jayanthi Savio
    • 11
  • Atul Patel
    • 12
  • Ujjwayini Ray
    • 13
  • Sangeetha Mohan
    • 14
  • Ranganathan Iyer
    • 15
  • Jagdish Chander
    • 16
  • Anita Arora
    • 17
  • Raman Sardana
    • 18
  • Indranil Roy
    • 19
  • B. Appalaraju
    • 20
  • Ajanta Sharma
    • 21
  • Anjali Shetty
    • 22
  • Neelam Khanna
    • 23
  • Rungmei Marak
    • 24
  • Sanjay Biswas
    • 25
  • Shukla Das
    • 26
  • B. N. Harish
    • 27
  • Sangeeta Joshi
    • 28
  • Deepak Mendiratta
    • 29
  1. 1.Department of Medical MicrobiologyPostgraduate Institute of Medical Education ResearchChandigarhIndia
  2. 2.Center of Advance Research in Medical Mycology, WHO Collaborating Center for Reference and Research on Fungi of Medical ImportanceNational Culture Collection of Pathogenic FungiChandigarhIndia
  3. 3.Centre for Infectious Diseases and Microbiology Laboratory ServicesICPMR-Pathology WestWestmeadAustralia
  4. 4.VMMC and Safdarjang HospitalNew DelhiIndia
  5. 5.Dayanand Medical College and HospitalLudhianaIndia
  6. 6.Apollo HospitalHyderabadIndia
  7. 7.Kasturba Medical CollegeManipalIndia
  8. 8.All India Institute of Medical SciencesNew DelhiIndia
  9. 9.Sri Ramachandra Medical CollegeChennaiIndia
  10. 10.Nizam’s Institute of Medical SciencesHyderabadIndia
  11. 11.St. John’s Medical CollegeBangaloreIndia
  12. 12.Sterling HospitalAhmedabadIndia
  13. 13.Apollo Gleneagles HospitalKolkataIndia
  14. 14.Christian Medical College and HospitalLudhianaIndia
  15. 15.Global HospitalsHyderabadIndia
  16. 16.Government Medical CollegeChandigarhIndia
  17. 17.Fortis Escorts Heart InstituteNew DelhiIndia
  18. 18.Indraprasth Apollo HospitalNew DelhiIndia
  19. 19.Calcutta Medical Research InstituteKolkataIndia
  20. 20.PSG Institute of Medical Sciences and ResearchCoimbatoreIndia
  21. 21.Gauhati Medical CollegeGuwahatiIndia
  22. 22.PD Hinduja HospitalMumbaiIndia
  23. 23.Batra HospitalNew DelhiIndia
  24. 24.Sanjay Gandhi Postgraduate Institute of Medical SciencesLucknowIndia
  25. 25.Tata Memorial HospitalMumbaiIndia
  26. 26.University College of Medical SciencesDelhiIndia
  27. 27.Jawaharlal Institute of Postgraduate Medical Education and ResearchPondicherryIndia
  28. 28.Manipal HospitalBangaloreIndia
  29. 29.Mahatma Gandhi Institute of Medical SciencesWardhaIndia

Personalised recommendations