Epidemiology of Candidemia at a University Hospital in Colombia, 2008-2014
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Dec 18, 2018
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Abstract
Introduction: Candida species are commensal yeasts of the human microbiota. However, due to several host’s conditions, bloodstream infections may arise causing high morbimortality. Methods: Retrospective cross-sectional analytical study of positive blood cultures for Candida spp. between 2008-2014 at a university hospital in Bogota, Colombia. We evaluated clinical and microbiological characteristics prior to the first positive blood sample was obtained and determined associations with non-C. albicans (NCA) species infections. Results: We included 123 candidemia cases. C. albicans was the most frequently isolated species (42%). However, NCA species as a group were observed more often. Over 70% of cases were managed at the ICU, with a median stay of 14 days. Several medical factors were frequently observed, however none appeared to be associated with NCA species candidemia. Resistance to at least one antifungal agent was observed in 29% of cases, although a reduced sample of susceptibility tests was available. Conclusions: Our results support a worldwide shift towards NCA candidemia. However, clinical features were not associated with NCA infections. The identification of risk factors and the improvement of prediction scores must be prioritized, in order to identify patients at high risk who may benefit of pre-emptive therapy.
Keywords
candida; candidemia; fungal drug resistance; epidemiology; risk factorsCandida; candidemia; farmacorresistencia fúngica; epidemiología; factores de riesgo
References
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2. Colombo AL, Cortes JA, Zurita J, et al. Recommendations for the diagnosis of candidemia in Latin America. Rev Iberoam Micol. 2013;30(3):150-7.
3. Mikulska M, Del Bono V, Ratto S, Viscoli C. Occurrence, presentation and treatment of candidemia. Expert Rev Clin Immunol. 2012;8(8):755-65.
4. Arendrup MC. Epidemiology of invasive candidiasis. Curr Opin Crit Care. 2010;16:445-52.
5. Zhang X-BB, Yu S-JJ, Yu J-XX, et al. Retrospective analysis of epidemiology and prognostic factors for candidemia at a hospital in China, 2000-2009. Jpn J Infect Dis. 2012;65(6):510-5.
6. Cortés JA, Reyes P, Gómez CH, et al. Clinical and epidemiological characteristics and risk factors for mortality in patients with candidemia in hospitals from Bogotá, Colombia. Brazilian J Infect Dis. 2014;18(6):631-7.
7. Quindós G. Epidemiology of candidaemia and invasive candidiasis: A changing face. Rev Iberoam Micol. 2014;31(1):42-8.
8. Botero MC, Puentes-Herrera M, Cortés JA. [Lipid formulations of amphotericin]. Rev Chilena Infectol. 2014;31(5):518-27.
9. Cortés JA, Reyes P, Gómez C, Buitrago G, Leal AL. Fungal bloodstream infections in tertiary care hospitals in Colombia. Rev Iberoam Micol. 2011;28(2):74-8.
10. Guinea J. Global trends in the distribution of Candida species causing candidemia. Clin Microbiol Infect. 2014;20(Suppl 6):5-10.
11. Antinori S, Milazzo L, Sollima S, Galli M, Corbellino M. Candidemia and invasive candidiasis in adults: A narrative review. Eur J Intern Med. 2016;34:21-8.
12. Hermsen ED, Zapapas MK, Maiefski M, et al. Validation and comparison of clinical prediction rules for invasive candidiasis in intensive care unit patients: A matched case-control study. Crit Care. 2011;15(4):R198.
13. Ostrosky-Zeichner L, Pappas PG, Shoham S, et al. Improvement of a clinical prediction rule for clinical trials on prophylaxis for invasive candidiasis in the intensive care unit. Mycoses. 2011;54(1):46-51.
14. León C, Ruiz-Santana S, Saavedra P, et al. A bedside scoring system (“Candida score”) for early antifungal treatment in nonneutropenic critically ill patients with Candida colonization. Crit Care Med. 2006;34(3):730-7.
15. Eggimann P, Garbino J, Pittet D. Epidemiology of Candida species infections in critically ill non-immunosuppressed patients. Lancet Infect Dis. 2003;3(11):685-702.
16. Pappas PG, Kauffman CA, Andes D, et al. Clinical practice guidelines for the management of candidiasis: 2009 update by the Infectious Diseases Society of America. Clin Infect Dis. 2009;48:503-35.
17. Chen CY, Huang SY, Tsay W, et al. Clinical characteristics of candidaemia in adults with haematological malignancy, and antimicrobial susceptibilities of the isolates at a medical centre in Taiwan, 2001-2010. Int J Antimicrob Agents. 2012;40:533-8.
18. Chi H-W, Yang Y-S, Shang S-T, et al. Candida albicans versus non-albicans bloodstream infections: The comparison of risk factors and outcome. J Microbiol Immunol Infect. 2011;44(5):369-75.
19. Vincent J-L, Rello J, Marshall J, et al. International study of the prevalence and outcomes of infection in intensive care units. JAMA. 2009;302:2323-9.
20. Ruan S-YY, Hsueh P-RR. Invasive candidiasis: An overview from Taiwan. J Formos Med Assoc. 2009;108(6):443-51.
21. Pfaller M, Neofutos D, Diekema D, et al. Epidemiology and outcomes of candidemia in 3648 patients: data from the Prospective Antifungal Therapy (PATH Alliance®) registry, 2004-2008. Diagn Microbiol Infect Dis. 2012;74(4):323-31.
22. Pfaller MA, Diekema DJ, Jones RN, et al. International surveillance of bloodstream infections due to Candida species: frequency of occurrence and in vitro susceptibilities to fluconazole, ravuconazole, and voriconazole of isolates collected from 1997 through 1999 in the SENTRY antimicrobial surv. J Clin Microbiol. 2001;39(9):3254-9.
23. Erdem I, Oguzoglu N, Ozturk Engin D, et al. Incidence, etiology and risk factors associated with mortality of nosocomial candidemia in a tertiary care hospital in Istanbul, Turkey. Med Princ Pract. 2010;19:463-7.
24. Nucci M, Thompson-Moya L, Guzman-Blanco M, et al. Recommendations for the management of candidemia in adults in Latin America. Rev Iberoam Micol. 2013;30(3):179-88.
25. Ben-Ami R, Olshtain-Pops K, Krieger M, et al. Antibiotic exposure as a risk factor for fluconazole-resistant Candida bloodstream infection. Antimicrob Agents Chemother. 2012;56(5):2518-23.
26. Zilberberg MD, Shorr AF, Kollef MH. Growth and geographic variation in hospitalizations with resistant infections, United States, 2000-2005. Emerg Infect Dis. 2008;14:1756-8.
27. Nucci M, Queiroz-Telles F, Alvarado-Matute T, et al. Epidemiology of Candidemia in Latin America: A Laboratory-Based Survey. PLoS One. 2013;8.
28. Adhikary R, Joshi S. Species distribution and anti-fungal susceptibility of Candidaemia at a multi super-specialty center in Southern India. Indian J Med Microbiol. 29:309-11.
29. Jutiamornlerd N, Chusri S, Sirsipaitoon P. Epidemiology of candidemia in Songklanagarind hospital. J Med Assoc Thail. 2011;94:927-32.
30. Boonyasiri A, Jearanaisilavong J, Assanasen S. Candidemia in Siriraj Hospital: epidemiology and factors associated with mortality. J Med Assoc Thai. 2013;96 Suppl 2(Suppl 2):S91-7.
31. Diazgranados CA, Martínez A, Deaza C, Valderrama S. An outbreak of Candida spp. bloodstream infection in a tertiary care center in Bogotá, Colombia. Braz J Infect Dis. 2008;12(5):390-4.
32. Ortiz Ruiz G, Osorio J, Valderrama S, et al. Risk factors for candidemia in non-neutropenic critical patients in Colombia. Med intensiva. 2016;40(3):139-44.
33. Rodríguez-Morales AJ, Sabogal-Román JA, Álvarez-Moreno CA. What has been researched about MDR-Candida auris? A bibliometric analysis on the “new kid on the block” in hospital-associated infections. J Infect Public Health. 2017;11(2):295-6.
34. Chen S, Slavin M, Nguyen Q, et al. Active surveillance for candidemia, Australia. Emerg Infect Dis. 2006;12:1508-16.
35. Asmundsdottir LR, Erlendsdottir H, Gottfredsson M. Nationwide study of candidemia, antifungal use, and antifungal drug resistance in Iceland, 2000 to 2011. J Clin Microbiol. 2013;51:841-8.
36. Yapar N, Pullukcu H, Avkan-Oguz V, et al. Evaluation of species distribution and risk factors of candidemia: a multicenter case-control study. Med Mycol. 2011;49:26-31.
37. Yapar N. Epidemiology and risk factors for invasive candidiasis. Ther Clin Risk Manag. 2014;10:95-105.
38. Tortorano AM, Peman J, Bernhardt H, et al. Epidemiology of candidaemia in Europe: results of 28-month European Confederation of Medical Mycology (ECMM) hospital-based surveillance study. Eur J Clin Microbiol Infect Dis. 2004;23(4):317-22.
39. Kreusch A, Karstaedt AS. Candidemia among adults in Soweto, South Africa, 1990-2007. Int J Infect Dis. 2013;17.
40. Deeks SG, Overbaugh J, Phillips A, Buchbinder S. HIV infection. Nat Rev Dis Prim. 2015;15035.
41. de Bedout C, Ayabaca J, Vega R, et al. Evaluation of Candida species’ susceptibility to fluconazole with the disk diffusion method. Biomedica. 2003;23(1):31-7.
42. Chen P-LL, Lo H-JJ, Wu C-JJ, et al. Species distribution and antifungal susceptibility of blood Candida isolates at a tertiary hospital in southern Taiwan, 1999-2006. Mycoses. 2011;54(4):17-23.
43. Pfaller MA, Diekema DJ. Twelve years of fluconazole in clinical practice: Global trends in species distribution and fluconazole susceptibility of bloodstream isolates of Candida. Clin Microbiol Infect. 2004;10 Suppl 1:11-23.
44. Underhill DM, Iliev ID. The mycobiota: interactions between commensal fungi and the host immune system. Nat Rev Immunol. 2014;14(6):405-16.
45. Martínez-Álvarez JA, Pérez-García LA, Flores-Carreón A, Mora-Montes HM. The immune response against Candida spp. and Sporothrix schenckii. Rev Iberoam Micol. 2013;31(1):1-5.
46. Lionakis MS, Kontoyiannis DP. Glucocorticoids and invasive fungal infections. Vol. 362, Lancet. 2003. p. 1828-38.
47. Guastalegname M, Russo A, Falcone M, Giuliano S, Venditti M. Candidemia subsequent to severe infection due to Clostridium difficile: is there a link? Clin Infect Dis. 2013;57(5):772-4.
48. Papadimitriou-Olivgeris M, Spiliopoulou A, Fligou F, et al. Association of KPC-producing Klebsiella pneumoniae colonization or infection with Candida isolation and selection of non-albicans species. Diagn Microbiol Infect Dis. 2014;80(3):227-32.
49. Russo A, Falcone M, Fantoni M, et al. Risk factors and clinical outcomes of candidaemia in patients treated for Clostridium difficile infection. Clin Microbiol Infect. 2015;21(5):493.e1-4.
50. Clancy CJ, Nguyen MH. Finding the “missing 50%” of invasive candidiasis: how nonculture diagnostics will improve understanding of disease spectrum and transform patient care. Clin Infect Dis. 2013;56(9):1284-92.
51. Haas M, Grenouillet F, Loubersac S, et al. Identification of cryptic Candida species by MALDI-TOF mass spectrometry, not all MALDI-TOF systems are the same: focus on the C. parapsilosis species complex. Diagn Microbiol Infect Dis. 2016;86(4):385-6.
52. Tsay S, Kallen A, Jackson BR, Chiller TM, Vallabhaneni S. Approach to the investigation and management of patients with Candida auris, an emerging multidrug-resistant yeast. Clin Infect Dis. 2018;66(2):306-11.
53. Parra-Giraldo CM, Valderrama SL, Cortes-Fraile G, et al. First report of sporadic cases of Candida auris in Colombia. Int J Infect Dis. 2018;69:63-7.
54. Morales-López SE, Parra-Giraldo CM, Ceballos-Garzón A, et al. Invasive infections with multidrug-resistant yeast Candida auris, Colombia. Emerg Infect Dis. 2017;23(1):162-4.
55. Mizusawa M, Miller H, Green R, et al. Can multidrug-resistant Candida auris be reliably identified in clinical microbiology laboratories? J Clin Microbiol. 2017;55(2):638-40.
2. Colombo AL, Cortes JA, Zurita J, et al. Recommendations for the diagnosis of candidemia in Latin America. Rev Iberoam Micol. 2013;30(3):150-7.
3. Mikulska M, Del Bono V, Ratto S, Viscoli C. Occurrence, presentation and treatment of candidemia. Expert Rev Clin Immunol. 2012;8(8):755-65.
4. Arendrup MC. Epidemiology of invasive candidiasis. Curr Opin Crit Care. 2010;16:445-52.
5. Zhang X-BB, Yu S-JJ, Yu J-XX, et al. Retrospective analysis of epidemiology and prognostic factors for candidemia at a hospital in China, 2000-2009. Jpn J Infect Dis. 2012;65(6):510-5.
6. Cortés JA, Reyes P, Gómez CH, et al. Clinical and epidemiological characteristics and risk factors for mortality in patients with candidemia in hospitals from Bogotá, Colombia. Brazilian J Infect Dis. 2014;18(6):631-7.
7. Quindós G. Epidemiology of candidaemia and invasive candidiasis: A changing face. Rev Iberoam Micol. 2014;31(1):42-8.
8. Botero MC, Puentes-Herrera M, Cortés JA. [Lipid formulations of amphotericin]. Rev Chilena Infectol. 2014;31(5):518-27.
9. Cortés JA, Reyes P, Gómez C, Buitrago G, Leal AL. Fungal bloodstream infections in tertiary care hospitals in Colombia. Rev Iberoam Micol. 2011;28(2):74-8.
10. Guinea J. Global trends in the distribution of Candida species causing candidemia. Clin Microbiol Infect. 2014;20(Suppl 6):5-10.
11. Antinori S, Milazzo L, Sollima S, Galli M, Corbellino M. Candidemia and invasive candidiasis in adults: A narrative review. Eur J Intern Med. 2016;34:21-8.
12. Hermsen ED, Zapapas MK, Maiefski M, et al. Validation and comparison of clinical prediction rules for invasive candidiasis in intensive care unit patients: A matched case-control study. Crit Care. 2011;15(4):R198.
13. Ostrosky-Zeichner L, Pappas PG, Shoham S, et al. Improvement of a clinical prediction rule for clinical trials on prophylaxis for invasive candidiasis in the intensive care unit. Mycoses. 2011;54(1):46-51.
14. León C, Ruiz-Santana S, Saavedra P, et al. A bedside scoring system (“Candida score”) for early antifungal treatment in nonneutropenic critically ill patients with Candida colonization. Crit Care Med. 2006;34(3):730-7.
15. Eggimann P, Garbino J, Pittet D. Epidemiology of Candida species infections in critically ill non-immunosuppressed patients. Lancet Infect Dis. 2003;3(11):685-702.
16. Pappas PG, Kauffman CA, Andes D, et al. Clinical practice guidelines for the management of candidiasis: 2009 update by the Infectious Diseases Society of America. Clin Infect Dis. 2009;48:503-35.
17. Chen CY, Huang SY, Tsay W, et al. Clinical characteristics of candidaemia in adults with haematological malignancy, and antimicrobial susceptibilities of the isolates at a medical centre in Taiwan, 2001-2010. Int J Antimicrob Agents. 2012;40:533-8.
18. Chi H-W, Yang Y-S, Shang S-T, et al. Candida albicans versus non-albicans bloodstream infections: The comparison of risk factors and outcome. J Microbiol Immunol Infect. 2011;44(5):369-75.
19. Vincent J-L, Rello J, Marshall J, et al. International study of the prevalence and outcomes of infection in intensive care units. JAMA. 2009;302:2323-9.
20. Ruan S-YY, Hsueh P-RR. Invasive candidiasis: An overview from Taiwan. J Formos Med Assoc. 2009;108(6):443-51.
21. Pfaller M, Neofutos D, Diekema D, et al. Epidemiology and outcomes of candidemia in 3648 patients: data from the Prospective Antifungal Therapy (PATH Alliance®) registry, 2004-2008. Diagn Microbiol Infect Dis. 2012;74(4):323-31.
22. Pfaller MA, Diekema DJ, Jones RN, et al. International surveillance of bloodstream infections due to Candida species: frequency of occurrence and in vitro susceptibilities to fluconazole, ravuconazole, and voriconazole of isolates collected from 1997 through 1999 in the SENTRY antimicrobial surv. J Clin Microbiol. 2001;39(9):3254-9.
23. Erdem I, Oguzoglu N, Ozturk Engin D, et al. Incidence, etiology and risk factors associated with mortality of nosocomial candidemia in a tertiary care hospital in Istanbul, Turkey. Med Princ Pract. 2010;19:463-7.
24. Nucci M, Thompson-Moya L, Guzman-Blanco M, et al. Recommendations for the management of candidemia in adults in Latin America. Rev Iberoam Micol. 2013;30(3):179-88.
25. Ben-Ami R, Olshtain-Pops K, Krieger M, et al. Antibiotic exposure as a risk factor for fluconazole-resistant Candida bloodstream infection. Antimicrob Agents Chemother. 2012;56(5):2518-23.
26. Zilberberg MD, Shorr AF, Kollef MH. Growth and geographic variation in hospitalizations with resistant infections, United States, 2000-2005. Emerg Infect Dis. 2008;14:1756-8.
27. Nucci M, Queiroz-Telles F, Alvarado-Matute T, et al. Epidemiology of Candidemia in Latin America: A Laboratory-Based Survey. PLoS One. 2013;8.
28. Adhikary R, Joshi S. Species distribution and anti-fungal susceptibility of Candidaemia at a multi super-specialty center in Southern India. Indian J Med Microbiol. 29:309-11.
29. Jutiamornlerd N, Chusri S, Sirsipaitoon P. Epidemiology of candidemia in Songklanagarind hospital. J Med Assoc Thail. 2011;94:927-32.
30. Boonyasiri A, Jearanaisilavong J, Assanasen S. Candidemia in Siriraj Hospital: epidemiology and factors associated with mortality. J Med Assoc Thai. 2013;96 Suppl 2(Suppl 2):S91-7.
31. Diazgranados CA, Martínez A, Deaza C, Valderrama S. An outbreak of Candida spp. bloodstream infection in a tertiary care center in Bogotá, Colombia. Braz J Infect Dis. 2008;12(5):390-4.
32. Ortiz Ruiz G, Osorio J, Valderrama S, et al. Risk factors for candidemia in non-neutropenic critical patients in Colombia. Med intensiva. 2016;40(3):139-44.
33. Rodríguez-Morales AJ, Sabogal-Román JA, Álvarez-Moreno CA. What has been researched about MDR-Candida auris? A bibliometric analysis on the “new kid on the block” in hospital-associated infections. J Infect Public Health. 2017;11(2):295-6.
34. Chen S, Slavin M, Nguyen Q, et al. Active surveillance for candidemia, Australia. Emerg Infect Dis. 2006;12:1508-16.
35. Asmundsdottir LR, Erlendsdottir H, Gottfredsson M. Nationwide study of candidemia, antifungal use, and antifungal drug resistance in Iceland, 2000 to 2011. J Clin Microbiol. 2013;51:841-8.
36. Yapar N, Pullukcu H, Avkan-Oguz V, et al. Evaluation of species distribution and risk factors of candidemia: a multicenter case-control study. Med Mycol. 2011;49:26-31.
37. Yapar N. Epidemiology and risk factors for invasive candidiasis. Ther Clin Risk Manag. 2014;10:95-105.
38. Tortorano AM, Peman J, Bernhardt H, et al. Epidemiology of candidaemia in Europe: results of 28-month European Confederation of Medical Mycology (ECMM) hospital-based surveillance study. Eur J Clin Microbiol Infect Dis. 2004;23(4):317-22.
39. Kreusch A, Karstaedt AS. Candidemia among adults in Soweto, South Africa, 1990-2007. Int J Infect Dis. 2013;17.
40. Deeks SG, Overbaugh J, Phillips A, Buchbinder S. HIV infection. Nat Rev Dis Prim. 2015;15035.
41. de Bedout C, Ayabaca J, Vega R, et al. Evaluation of Candida species’ susceptibility to fluconazole with the disk diffusion method. Biomedica. 2003;23(1):31-7.
42. Chen P-LL, Lo H-JJ, Wu C-JJ, et al. Species distribution and antifungal susceptibility of blood Candida isolates at a tertiary hospital in southern Taiwan, 1999-2006. Mycoses. 2011;54(4):17-23.
43. Pfaller MA, Diekema DJ. Twelve years of fluconazole in clinical practice: Global trends in species distribution and fluconazole susceptibility of bloodstream isolates of Candida. Clin Microbiol Infect. 2004;10 Suppl 1:11-23.
44. Underhill DM, Iliev ID. The mycobiota: interactions between commensal fungi and the host immune system. Nat Rev Immunol. 2014;14(6):405-16.
45. Martínez-Álvarez JA, Pérez-García LA, Flores-Carreón A, Mora-Montes HM. The immune response against Candida spp. and Sporothrix schenckii. Rev Iberoam Micol. 2013;31(1):1-5.
46. Lionakis MS, Kontoyiannis DP. Glucocorticoids and invasive fungal infections. Vol. 362, Lancet. 2003. p. 1828-38.
47. Guastalegname M, Russo A, Falcone M, Giuliano S, Venditti M. Candidemia subsequent to severe infection due to Clostridium difficile: is there a link? Clin Infect Dis. 2013;57(5):772-4.
48. Papadimitriou-Olivgeris M, Spiliopoulou A, Fligou F, et al. Association of KPC-producing Klebsiella pneumoniae colonization or infection with Candida isolation and selection of non-albicans species. Diagn Microbiol Infect Dis. 2014;80(3):227-32.
49. Russo A, Falcone M, Fantoni M, et al. Risk factors and clinical outcomes of candidaemia in patients treated for Clostridium difficile infection. Clin Microbiol Infect. 2015;21(5):493.e1-4.
50. Clancy CJ, Nguyen MH. Finding the “missing 50%” of invasive candidiasis: how nonculture diagnostics will improve understanding of disease spectrum and transform patient care. Clin Infect Dis. 2013;56(9):1284-92.
51. Haas M, Grenouillet F, Loubersac S, et al. Identification of cryptic Candida species by MALDI-TOF mass spectrometry, not all MALDI-TOF systems are the same: focus on the C. parapsilosis species complex. Diagn Microbiol Infect Dis. 2016;86(4):385-6.
52. Tsay S, Kallen A, Jackson BR, Chiller TM, Vallabhaneni S. Approach to the investigation and management of patients with Candida auris, an emerging multidrug-resistant yeast. Clin Infect Dis. 2018;66(2):306-11.
53. Parra-Giraldo CM, Valderrama SL, Cortes-Fraile G, et al. First report of sporadic cases of Candida auris in Colombia. Int J Infect Dis. 2018;69:63-7.
54. Morales-López SE, Parra-Giraldo CM, Ceballos-Garzón A, et al. Invasive infections with multidrug-resistant yeast Candida auris, Colombia. Emerg Infect Dis. 2017;23(1):162-4.
55. Mizusawa M, Miller H, Green R, et al. Can multidrug-resistant Candida auris be reliably identified in clinical microbiology laboratories? J Clin Microbiol. 2017;55(2):638-40.
How to Cite
Barahona Correa, J. E., Calvo Valderrama, M. G., Romero Alvernia, D. M., Angulo Mora, J., Alarcón Figueroa, L. F., Rodríguez Malagón, M. N., & Garzón Herazo, J. R. (2018). Epidemiology of Candidemia at a University Hospital in Colombia, 2008-2014. Universitas Medica, 60(1). https://doi.org/10.11144/Javeriana.umed60-1.cand
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