Skip to main content
Log in

Candidemia by Species of the Candida parapsilosis Complex in Children’s Hospital: Prevalence, Biofilm Production and Antifungal Susceptibility

  • Published:
Mycopathologia Aims and scope Submit manuscript

Abstract

Opportunistic infections are an increasingly common problem in hospitals, and the yeast Candida parapsilosis has emerged as an important nosocomial pathogen. The aims of this study were to determine and compare (i) the prevalence rate among C. parapsilosis complex organisms isolated from blood in a public children’s hospital in São Paulo state, (ii) the ability of the complex C. parapsilosis species identified to produce biofilm and (iii) the antifungal susceptibility profiles. Forty-nine (49) specimens of isolated blood yeast were analyzed, previously identified as C. parapsilosis by conventional methods. After the molecular analysis, the isolates were characterized as C. parapsilosis sensu stricto (83.7 %), C. orthopsilosis (10.2 %) and C. metapsilosis (6.1 %). All species were able to form biofilm. The species with the highest biofilm production was C. parapsilosis sensu stricto, followed by C. orthopsilosis and further by C. metapsilosis. All of the strains have demonstrated similar susceptibility to fluconazole, caspofungin, voriconazole, cetoconazole and 5-flucytosine. Only one strain of C. parapsilosis was resistant to amphotericin B. Regarding itraconazole, 66.6 and 43.9 % isolates of C. metapsilosis and C. parapsilosis, respectively, have demonstrated to be susceptible dose-dependent, with one isolate of the latter species resistant to the drug. Candida parapsilosis sensu stricto has demonstrated to be the less susceptible, mainly to amphotericin B, caspofungin and “azoles” such as fluconazole. Therefore, C. metapsilosis and C. orthopsilosis are still involved in a restricted number of infections, but these data have become essential for there are very few studies of these species in Latin America.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Gudlaugsson O, Gillespie S, Lee K, Vandeberg J, Hu J, Messer S, Herwaldt L, Pfaller M, Diekema D. Attributable mortality of nosocomial candidemia, revisited. Clin Infect Dis. 2003;37(9):1172–7.

    Article  PubMed  Google Scholar 

  2. 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.

    Article  PubMed  Google Scholar 

  3. Marol S, Yücesoy M. Molecular epidemiology of Candida species isolated from clinical specimens of intensive care unit patients. Mycoses. 2008;51:40–9.

    PubMed  CAS  Google Scholar 

  4. Levy I, Rubin LG, Vasishtha S, Tucci V, Sood SK. Emergence of Candida parapsilosis as the predominant species causing candidemia in children. Olin Infect Dis. 1998;26:1086–8.

    Article  CAS  Google Scholar 

  5. Colombo AL, Guimarães T. Epidemiologia das infecções hematogênicas por Candida sp. Rev Soc Bras Med Trop. 2003;36:599–607.

    Article  PubMed  Google Scholar 

  6. Ruiz LS, Sugizaki MF, Montelli AC, Matsumoto FE, Pires MFC, Da Silva BCM, Silva EH, Gandra RF, Gonçalves Da Silva E, Auler ME, Paula CR. Fungemia by yeasts in Brazil: occurrence and phenotypic study of strains isolated at the Public Hospital, Botucatu, São Paulo. J Mycol Medical. 2005;15:13–21.

  7. Pappas PG, Rex JH, Lee J, Hamill RJ, Larsen RA, Powderly W, Kauffman CA, Hyslop N, Mangino JE, Chapman S, Horowitz HW, Edwards JE, Dismukeswe Niaid Mycoses Study Group. A prospective observational study of candidemia: epidemiology, therapy, and influences on mortality in hospitalized adult and pediatric patients. Clin Infect Dis. 2003;37:634–43.

    Google Scholar 

  8. Roilides E, Farmaki E, Evdoridou J, Dotis J, Hatziioannidis E, Tsivitanidou M, Bibashi E, Filioti I, Sofianou D, Gil-Lamaignere C, Mueller FM, Kremenopoulos G. Neonatal candidiasis: analysis of epidemiology, drug susceptibility, and molecular typing of causative isolates. Eur J Clin Microbiol Infect Dis. 2004;23(10):745–50.

    Article  PubMed  CAS  Google Scholar 

  9. Almirante B, Rodriguez D, Park, BJ, Cuenca-Estrella M, Planes AM, Almela M, Mensa J, Sanchez F, Ayats J, Gimenez M, Saballs P, Fridlkin SK, Morgan J, Rodriguez-Tudela JL, Warnock DW, Pahissa A, The Barcelona Candidemia Project Study Group. 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. 2005;43(4):1829–35.

    Google Scholar 

  10. Miranda Ld, Rodrigues EC, Costa SF, van der Heijden IM, Dantas KC, Lobo RD, Basso M, Varkulja GF, Krebs VL, Gibelli MA, Criado PR, Levin AS. Candida parapsilosis candidaemia in a neonatal unit over 7 years: a case series study. BMJ Open. 2012. doi:10.1136/bmjopen-2012-000992.

  11. Brito LR, Guimaraes T, Nucci M, Rosas RC. Paula Almeida L, Da Matta DA, Colombo AL. Clinical and microbiological aspects of candidemia due to Candida parapsilosis in Brazilian tertiary care hospitals. Med Mycol. 2006;44:261–6.

    Article  PubMed  Google Scholar 

  12. Pfaller MA, Diekema DJ. Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev. 2007;20:133–63.

    Article  PubMed  CAS  Google Scholar 

  13. Swindell K, Lattif AA, Chandra J, Mukherjee PK, Ghannoum MA. Parenteral lipid emulsion induces germination of Candida albicans and increases biofilm formation on medical catheter surfaces. J Infect Dis. 2009;200:473–80.

    Article  PubMed  CAS  Google Scholar 

  14. Krcmery V, Barnes AJ. Non-albicans Candida spp. causing fungaemia: pathogenicity and antifungal resistance. J Hosp Infect. 2002;50:243–60.

    Article  PubMed  CAS  Google Scholar 

  15. Clark TA, Slavinski SA, Morgan J, Lott T, Arthington-Skaggs BA, Brandt ME, Webb RM, Currier M, Flowers RH, Fridkin SK, Hajjeh RA. Epidemiologic and molecular characterization of an outbreak of Candida parapsilosis bloodstream infections in a community hospital. J Clin Microbiol. 2004;42(10):4468–72.

    Article  PubMed  CAS  Google Scholar 

  16. Bonassoli LA, Bertoli M, Svidzinski TIE. High frequency of Candida parapsilosis on the hands of healthy hosts. J Hosp Infect. 2005;59:159–62.

    Article  PubMed  CAS  Google Scholar 

  17. Ruiz LS, Montelli AC, Sugizaki MF, Gonçalves da Silva E, Batista GCM, Moreira D, Paula CR. Outbreak of fungaemia due to Candida parapsilosis in a neonatal intensive care unit: molecular genotyping by analysis microsatellite markers. Rev Iberoam Micol. 2012. doi:10.1016/j.riam.2012.10.003.

  18. Tamura NK, Gasparetto A, Svidzinski TI. Evaluation of the adherence of Candida species to urinary catheters. Mycopathologia. 2003;156(4):269–72.

    Article  PubMed  CAS  Google Scholar 

  19. Tavanti A, Davidson AD, Gow NAR, Maiden MCJ. Candida orthopsilosis and Candida metapsilosis spp. Nov. to replace Candida parapsilosis groups II and III. J Clin Microbiol. 2005;43:284–92.

    Article  PubMed  CAS  Google Scholar 

  20. Lockhart SR, Messer SA, Pfaller MA, Diekema DJ. Geographic distribution and antifungal susceptibility of the newly described species Candida orthopsilosis and Candida metapsilosis in comparison to the closely related species Candida parapsilosis. J Clin Microbiol. 2008;46:2659–64.

    Article  PubMed  CAS  Google Scholar 

  21. Van Asbeck E, Clemons KV, Martinez M, Tong AJ, Stevens D. Significant differences in drug susceptibility among species in the Candida parapsilosis group. Diagn Microbiol Infect Dis. 2008;62:106–9.

    Article  PubMed  Google Scholar 

  22. Gomez-Lopez A, Alastruey-Izquierdo A, Rodriguez D, Almirante B, Pahissa A, Rodriguez-Tudela JL, Barcelona Candidemia Project Study Group. Prevalence and susceptibility profile of Candida metapsilosis and Candida orthopsilosis: results from population-based surveillance of candidemia in Spain. Antimicrob Agents Chemother. 2008;52(4):1506–9.

    Article  PubMed  CAS  Google Scholar 

  23. Kurtzman CP, Fell JW. The yeasts: a taxonomic study. 5th. Burlington, MA, EUA. Amsterdam: Elsevier Science; 2011.

  24. Melo AS, Bizerra FC, Freymüller E, Arthington-Skaggs BA, Colombo AL. Biofilm production and evaluation of antifungal susceptibility amongst clinical Candida spp. isolates, including strains of the Candida parapsilosis complex. Med Mycol. 2011;49(3):253–62.

    Article  PubMed  CAS  Google Scholar 

  25. Clinical and Laboratory Standards Institute. Reference method for broth dilution antifungal susceptibility testing of yeasts; approved standard NCCLS document M27–A2. Wayne, Pa: CLSI; 2002.

    Google Scholar 

  26. Clinical and Laboratory Standards Institute. Reference method for broth dilution antifungal susceptibility testing for yeasts. Approved standard NCCLS. Wayne, Pa. Document M27-A3. CLSI, 2008.

  27. Nguyen MH, Clancy CJ, Yu VL, Yu YC, Morris AJ, Snydman DR, Sutton DA, Rinaldi MG. Do in vitro susceptibility data predict the microbiologic response to amphotericin B? Results of a prospective study of patients with Candida fungemia. J Infect Dis. 1998;177(2):425–30.

    Article  PubMed  CAS  Google Scholar 

  28. Guinea J, Recio S, Escribano P, Torres-Narbona M, Peláez T, Sánchez-Carrillo C, Rodríguez-Créixems M, Bouza E. Rapid antifungal susceptibility determination for yeast isolates by use of Etest performed directly on blood samples from patients with fungemia. J Clin Microbiol. 2010;48(6):2205–12.

    Article  PubMed  CAS  Google Scholar 

  29. Feng X, Ling B, Yang G, Yu X, Ren D, Yao Z. Prevalence and distribution profiles of Candida parapsilosis, Candida orthopsilosis and Candida metapsilosis responsible for superficial candidiasis in a Chinese university hospital. Mycopathologia. 2012;173(4):229–34.

    Article  PubMed  Google Scholar 

  30. Blyth CC, Chen SC, Slavin MA, Serena C, Nguyen Q, Marriott D, Ellis D, Meyer W, Australian Candidemia Study. Not just little adults: candidemia epidemiology, molecular characterization, and antifungal susceptibility in neonatal and pediatric patients. Pediatrics. 2009;123(5):1360–8.

    Article  PubMed  Google Scholar 

  31. Cantón E, Pemán J, Quindós G, Eraso E, Miranda-Zapico I, Álvarez M, Merino P, Campos-Herrero I, Marco F, de la Pedrosa EG, Yagüe G, Guna R, Rubio C, Miranda C, Pazos C, Velasco D, FUNGEMYCA Study Group. Prospective multicenter study of the epidemiology, molecular identification, and antifungal susceptibility of Candida parapsilosis, Candida orthopsilosis, and Candida metapsilosis isolated from patients with candidemia. Antimicrob Agents Chemother. 2011;55(12):5590–6.

    Article  PubMed  Google Scholar 

  32. Garcia-Effron G, Canton E, Pemán J, Dilger A, Romá E, Perlin DS. Epidemiology and echinocandin susceptibility of Candida parapsilosis sensu lato species isolated from bloodstream infections at a Spanish university hospital. J Antimicrob Chemother. 2012;67:2739–2748.

    Google Scholar 

  33. Tay ST, Na SL, Chong J. Molecular differentiation and antifungal susceptibilities of Candida parapsilosis isolated from patients with bloodstream infections. J Med Microbiol. 2009;58:185–91.

    Article  PubMed  CAS  Google Scholar 

  34. Bonfietti LX, Martins Mdos A, Szeszs MW, Pukiskas SB, Purisco SU, Pimentel FC, Pereira GH, Silva DC, Oliveira L, Melhem MS. Prevalence, distribution and antifungal susceptibility profiles of Candida parapsilosis, Candida orthopsilosis and Candida metapsilosis bloodstream isolates. J Med Microbiol. 2012;61:1003–8.

    Google Scholar 

  35. Gonçalves SS, Amorim CS, Nucci M, Padovan ACB, Briones MRS, Melo ASA, Colombo AL. Prevalence C. parapsilosis group: identification and epidemiology rates and antifungal susceptibility profiles of C. parapsilosis species complex: results from a nationwide surveillance of candidaemia in Brazil. Clin Microbiol Infect. 2010;16:885–7.

    PubMed  Google Scholar 

  36. Gácser A, Schäfer W, Nosanchuk JS, Salomon S, Nosanchuk JD. Virulence of Candida parapsilosis, Candida orthopsilosis, and Candida metapsilosis in reconstituted human tissue models. Fungal Genet Biol. 2007;44(12):1336–41.

    Article  PubMed  Google Scholar 

  37. Orsi CF, Colombari B, Blasi E. Candida metapsilosis as the least virulent member of the ‘C. parapsilosis’ complex. Med Mycol. 2010;48(8):1024–33.

    Article  PubMed  Google Scholar 

  38. Růzicka F, Holá V, Votava M, Tejkalová R. Importance of biofilm in Candida parapsilosis and evaluation of its susceptibility to antifungal agents by colorimetric method. Folia Microbiol (Praha). 2007;52(3):209–14.

    Article  Google Scholar 

  39. Kuhn DM, Ghannoum MA. Candida biofilms: antifungal resistance and emerging therapeutic options. Curr Opin Investig Drugs. 2004;5:186–97.

    PubMed  CAS  Google Scholar 

  40. Tavanti A, Hensgens LAM, GhelardI E, Campo M, Senesi S. Genotyping of Candida orthopsilosis clinical isolates by amplification fragment length polymorphism reveals genetic diversity among independent isolates and strain maintenance within patients. J Clin Microbiol. 2007;45:1455–62.

    Article  PubMed  CAS  Google Scholar 

  41. Song JW, Shin JH, Shint DH, Jung SI, Cho D, Kee SJ, Shin MG, Suh SP, Ryang DW. Differences in biofilm production by three genotypes of Candida parapsilosis from clinical sources. Med Mycol. 2005;43(7):657–61.

    Article  PubMed  CAS  Google Scholar 

  42. Lattif AA, Mukherjee PK, Chandra J, Swindell K, Lockhart SR, Diekema DJ, Pfaller MA, Ghannoum MA. Characterization of biofilms formed by Candida parapsilosis, C. metapsilosis, and C. orthopsilosis. Int J Med Microbiol. 2010;300(4):265–70.

    Article  PubMed  Google Scholar 

  43. Diekema DJ, Messer SA, Boyken LB, Hollis RJ, Kroeger J, Tendolkar S, Pfaller MA. In vitro activity of seven systemically active antifungal agents against a large global collection of rare Candida species as determined by CLSI broth microdilution methods. J Clin Microbiol. 2009;47(10):3170–7.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors express their thanks to PhD Marina Korte for her revision of the English text, to CNPQ and FAPESP for their financial support and to Dra. Angela Satie Nishikaku and Ms. Karina Bellinghausen Merseguel for support in the molecular study.

Conflict of interest

None.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Luciana da Silva Ruiz.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ruiz, L.S., Khouri, S., Hahn, R.C. et al. Candidemia by Species of the Candida parapsilosis Complex in Children’s Hospital: Prevalence, Biofilm Production and Antifungal Susceptibility. Mycopathologia 175, 231–239 (2013). https://doi.org/10.1007/s11046-013-9616-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11046-013-9616-5

Keywords

Navigation