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Insights into Candida tropicalis nosocomial infections and virulence factors

European Journal of Clinical Microbiology & Infectious Diseases volume 31, pages 1399–1412 (2012)Cite this article

Abstract

Candida tropicalis is considered the first or the second non-Candida albicans Candida (NCAC) species most frequently isolated from candidosis, mainly in patients admitted in intensive care units (ICUs), especially with cancer, requiring prolonged catheterization, or receiving broad-spectrum antibiotics. The proportion of candiduria and candidemia caused by C. tropicalis varies widely with geographical area and patient group. Actually, in certain countries, C. tropicalis is more prevalent, even compared with C. albicans or other NCAC species. Although prophylactic treatments with fluconazole cause a decrease in the frequency of candidosis caused by C. tropicalis, it is increasingly showing a moderate level of fluconazole resistance. The propensity of C. tropicalis for dissemination and the high mortality associated with its infections might be strongly related to the potential of virulence factors exhibited by this species, such as adhesion to different host surfaces, biofilm formation, infection and dissemination, and enzymes secretion. Therefore, the aim of this review is to outline the present knowledge on all the above-mentioned C. tropicalis virulence traits.

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References

  1. Hota B (2004) Contamination, disinfection, and cross colonization: are hospital surfaces reservoirs for nosocomial infection? Clin Infect Dis 39(8):1182–1189. doi:10.1086/424667

    PubMed  Article  Google Scholar 

  2. 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(9):1172–1177. doi:10.1086/378745

    PubMed  Article  Google Scholar 

  3. Bassetti M, Righi E, Costa A, Fasce R, Molinari M, Rosso R, Pallavicini F, Viscoli C (2006) Epidemiological trends in nosocomial candidemia in intensive care. BMC Infect Dis 6(1):21. doi:10.1186/1471-2334-6-21

    PubMed  Article  Google Scholar 

  4. Cheng M-F, Yang Y-L, Yao T-J, Lin C-Y, Liu J-S, Tang R-B, Yu K-W, Fan Y-H, Hsieh K-S, Ho M, Lo H-J (2005) Risk factors for fatal candidemia caused by Candida albicans and non-albicans Candida species. BMC Infect Dis 5(1):22. doi:10.1186/1471-2334-5-22

    PubMed  Article  Google Scholar 

  5. Dimopoulos G, Ntziora F, Rachiotis G, Armaganidis A, Falagas ME (2008) Candida albicans versus non-albicans intensive care unit-acquired bloodstream infections: differences in risk factors and outcome. Anesth Analg 106(2):523–529. doi:10.1213/ane.0b013e3181607262

    PubMed  Article  Google Scholar 

  6. Meric M, Willke A, Caglayan C, Toker K (2005) Intensive care unit-acquired infections: incidence, risk factors and associated mortality in a Turkish university hospital. Jpn J Infect Dis 58(5):297–302

    PubMed  Google Scholar 

  7. Lass-Flörl C (2009) The changing face of epidemiology of invasive fungal disease in Europe. Mycoses 52(3):197–205. doi:10.1111/j.1439-0507.2009.01691.x

    PubMed  Article  Google Scholar 

  8. Eggimann P, Garbino J, Pittet D (2003) Epidemiology of Candida species infections in critically ill non-immunosuppressed patients. Lancet Infect Dis 3(11):685–702. doi:10.j.clp.2007.1/S1473-3099(03)00801-6

    PubMed  Article  Google Scholar 

  9. Snydman DR (2003) Shifting patterns in the epidemiology of nosocomial Candida infections. Chest 123(5 Suppl):500S–503S. doi:10.1378/chest.123.5_suppl.500S

    PubMed  Article  Google Scholar 

  10. Lundstrom T, Sobel J (2001) Nosocomial Candiduria: a review. Clin Infect Dis 32(11):1602–1607. doi:10.1086/320531

    PubMed  CAS  Article  Google Scholar 

  11. Krcmery V, Barnes AJ (2002) Non-albicans Candida spp. causing fungaemia: pathogenicity and antifungal resistance. J Hosp Infect 50(4):243–260. doi:10.1053/jhin.2001.1151

    PubMed  CAS  Article  Google Scholar 

  12. Colombo AL, Nucci M, Park BJ, Nouer SA, Arthington-Skaggs B, da Matta DA, Warnock D, Morgan J, for the Brazilian Network Candidemia S (2006) Epidemiology of Candidemia in Brazil: a nationwide sentinel surveillance of Candidemia in eleven medical centers. J Clin Microbiol 44(8):2816–2823. doi:10.1128/jcm.00773-06

    PubMed  CAS  Article  Google Scholar 

  13. Chakrabarti A, Chatterjee SS, Rao KLN, Zameer MM, Shivaprakash MR, Singhi S, Singh R, Varma SC (2009) Recent experience with fungaemia: change in species distribution and azole resistance. Scand J Infect Dis 41(4):275–284. doi:10.1080/00365540902777105

    PubMed  CAS  Article  Google Scholar 

  14. Tortorano AM, Peman J, Bernhardt H, Klingspor L, Kibbler CC, Faure O, Biraghi E, Canton E, Zimmermann K, Seaton S, Grillot R, the EWGoC (2004) 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 23(4):317–322. doi:10.1007/s10096-004-1103-y

    PubMed  CAS  Article  Google Scholar 

  15. Nucci M, Colombo AL (2007) Candidemia due to Candida tropicalis: clinical, epidemiologic, and microbiologic characteristics of 188 episodes occurring in tertiary care hospitals. Diagn Microbiol Infect Dis 58(1):77–82. doi:10.j.clp.2007.1/j.diagmicrobio.2006.11.009

    PubMed  CAS  Article  Google Scholar 

  16. Hsueh P-R, Graybill JR, Playford EG, Watcharananan SP, Oh M-D, Já alam K, Huang S, Nangia V, Kurup A, Padiglione AA (2009) Consensus statement on the management of invasive candidiasis in intensive care units in the Asia-Pacific Region. Int J Antimicro Ag 34(3):205–209. doi:10.j.clp.2007.1/j.ijantimicag.2009.03.014, 34

    CAS  Article  Google Scholar 

  17. Álvarez-Lerma F, Nolla-Salas J, León C, Palomar M, Jordá R, Carrasco N, Bobillo F (2003) Candiduria in critically ill patients admitted to intensive care medical units. Intensive Care Med 29(7):1069–1076. doi:10.1007/s00134-003-1807-y

    PubMed  Article  Google Scholar 

  18. 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. Clin Infect Dis 30(1):14–18. doi:10.1086/313583

    PubMed  CAS  Article  Google Scholar 

  19. Krcmery VJ (1999) Candidemia in cancer patients: Risk factors and outcome in 140 episodes from a single cancer institution. Acta Chemoth 5:133–145

    Google Scholar 

  20. Kontoyiannis Dimitrios P, Vaziri I, Hanna Hend A, Boktour M, Thornby J, Hachem R, Bodey Gerald P, Raad Issam I (2001) Risk factors for Candida tropicalis fungemia in patients with cancer. Clin Infect Dis 33(10):1676–1681. doi:10.1086/323812

    Article  Google Scholar 

  21. Okawa Y, Miyauchi M, Kobayashi H (2008) Comparison of pathogenicity of various Candida tropicalis strains. Biol Pharm Bull 31(8):1507–1510. doi:10.1248/bpb.31.1507

    PubMed  CAS  Article  Google Scholar 

  22. Negri M, Martins M, Henriques M, Svidzinski T, Azeredo J, Oliveira R (2010) Examination of potential virulence factors of Candida tropicalis clinical isolates from hospitalized patients. Mycopathologia 169(3):175–182. doi:10.1007/s11046-009-9246-0

    PubMed  CAS  Article  Google Scholar 

  23. Bizerra FC, Nakamura CV, de Poersch C, Svidzinski TIE, Quesada RMB, Goldenberg S, Krieger MA, Yamada-Ogatta SF (2008) Characteristics of biofilm formation by Candida tropicalis and antifungal resistance. FEMS Yeast Res 8(3):442–450. doi:10.1111/j.1567-1364.2007.00347.x

    PubMed  CAS  Article  Google Scholar 

  24. Zaugg C, Borg-von Zepelin M, Reichard U, Sanglard D, Monod M (2001) Secreted aspartic proteinase family of Candida tropicalis. Infect Immun 69(1):405–412. doi:10.1128/iai.69.1.405-412.2001

    PubMed  Article  Google Scholar 

  25. Galan-Ladero MA, Blanco MT, Sacristan B, Fernandez-Calderan MC, Perez-Giraldo C, Gomez-Garcia AC (2010) Enzymatic activities of Candida tropicalis isolated from hospitalized patients. Med Mycol 48(1):207–210. doi:10.1080/13693780902801242

    PubMed  CAS  Article  Google Scholar 

  26. Larone D (2002) Medically important fungi; a guide to identification, 4th edn. ASM Press, Washington

    Google Scholar 

  27. Kurtzman CP, Fell JW (1998) The yeasts, a taxonomic study, 4th edn. Elsevier Science Ltd, New York

    Google Scholar 

  28. Basu S, Gugnani H, Joshi S, Gupta N (2003) Distribution of Candida species in different clinical sources in Delhi, India, and proteinase and phospholipase activity of Candida albicans isolates. Rev Iberoam Micol 20(4):137–140

    PubMed  Google Scholar 

  29. Oksuz S, Sahin I, Yildirim M, Gulcan A, Yavuz T, Kaya D, Koc A (2007) Phospholipase and proteinase activities in different Candida species isolated from anatomically distinct sites of healthy adults. Jpn J Infect Dis 60(5):280–283

    PubMed  Google Scholar 

  30. Biasoli MS, Tosello ME, Bottai H, Cuesta C, Magaró HM (2002) Adherence of Candida strains isolated from the human gastrointestinal tract. Mycoses 45(11–12):465–469. doi:10.1046/j.1439-0507.2002.00793.x

    PubMed  Google Scholar 

  31. Tamura NK, Negri MFN, Bonassoli LA, Svidzinski TIE (2007) Fatores de virulência de Candida spp isoladas de cateteres venosos e mãos de servidores hospitalares. Rev Soc Bras Med Trop 40(1):91–93. doi:10.1590/S0037-86822007000100021

    PubMed  Article  Google Scholar 

  32. Shurtleff DB, Peterson W, Sherris JC (1963) Systemic Candida tropicalis infection treated with amphotericin. N Engl J Med 269:1112–1115. doi:10.1056/NEJM196311212692102

    PubMed  CAS  Article  Google Scholar 

  33. HO D (1960) The pathogenicity of Candida tropicalis. Can Med Assoc J 83(27):1439–1440

    Google Scholar 

  34. Nucci M, Silveira M, Spector N, Silveira F, Velasco E, Martins C, Derossi A, Colombo A, Pulcheri W (1998) Fungemia in cancer patients in Brazil: Predominance of non-albicans species. Mycopathologia 141(2):65–68. doi:10.1023/A:1006951619245

    PubMed  CAS  Article  Google Scholar 

  35. Rho J, Shin J, Song J, Park M, Kee S, Jang S, Park Y, Suh S, Ryang D (2004) Molecular investigation of two consecutive nosocomial clusters of Candida tropicalis candiduria using pulsed-field gel electrophoresis. J Microbiol 42(2):80–86

    PubMed  CAS  Google Scholar 

  36. Kliemann DA, Pasqualotto AC, Falavigna M, Giaretta T, Severo LC (2008) Candida esophagitis: species distribution and risk factors for infection. Rev Inst Med Trop Sao Paulo 50:261–263. doi:10.1590/S0036-46652008000500002

    PubMed  Article  Google Scholar 

  37. Silva EHd, Ruiz LdS, Matsumoto FE, Auler ME, Giudice MC, Moreira D, Szeszs W, Paula CR (2007) Candiduria in a public hospital of São Paulo (1999–2004): characteristics of the yeast isolates. Rev Inst Med Trop Sao Paulo 49(6):349–353. doi:10.1590/S0036-46652007000600003

    PubMed  Article  Google Scholar 

  38. Silva EH, Ruiz LS, Matsumoto FE, Auler ME, Giudice MC, Moreira D, Szeszs W, Paula CR (2007) Candiduria in a public hospital of São Paulo (1999–2004): characteristics of the yeast isolates. Rev Inst Med Trop Sao Paulo 49(6):349–353. doi:10.1590/S0036-46652007000600003

    PubMed  Article  Google Scholar 

  39. Calderone RA (2002) Introduction and historical perspectives. In: Calderone R (ed) Candida and candidiasis. ASM Press, Washington D.C., pp 15–25

    Google Scholar 

  40. Yoshio O, Kouji G (2006) Antigenicity of Candida tropicalis strain cells cultured at 27 and 37°C. FEMS Immunol Med Microbiol 46(3):438–443

    Article  CAS  Google Scholar 

  41. Martin MV (1979) Germ-tube formation by oral strains of Candida tropicalis. J Med Microbiol 12(2):187–194. doi:10.1099/00222615-12-2-187

    PubMed  CAS  Article  Google Scholar 

  42. Butler G, Rasmussen MD, Lin MF, Santos MAS, Sakthikumar S, Munro CA, Rheinbay E, Grabherr M, Forche A, Reedy JL, Agrafioti I, Arnaud MB, Bates S, Brown AJP, Brunke S, Costanzo MC, Fitzpatrick DA, de Groot PWJ, Harris D, Hoyer LL, Hube B, Klis FM, Kodira C, Lennard N, Logue ME, Martin R, Neiman AM, Nikolaou E, Quail MA, Quinn J, Santos MC, Schmitzberger FF, Sherlock G, Shah P, Silverstein KAT, Skrzypek MS, Soll D, Staggs R, Stansfield I, Stumpf MPH, Sudbery PE, Srikantha T, Zeng Q, Berman J, Berriman M, Heitman J, Gow NAR, Lorenz MC, Birren BW, Kellis M, Cuomo CA (2009) Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459(7247):657–662. doi:10.1038/nature08064

    PubMed  CAS  Article  Google Scholar 

  43. Bennett RJ (2009) A Candida-based view of fungal sex and pathogenesis. Genome Biol 10(7):230. doi:10.1186/gb-2009-10-7-230

    PubMed  Article  CAS  Google Scholar 

  44. Zhang J, Hollis RJ, Pfaller MA (1997) Variations in DNA subtype and antifungal susceptibility among clinical isolates of Candida tropicalis. Diagn Microbiol Infect Dis 27(3):63–67

    PubMed  CAS  Article  Google Scholar 

  45. Fricke S, Fricke C, Schimmelpfennig C, Oelkrug C, Schönfelder U, Blatz R, Zilch C, Faber S, Hilger N, Ruhnke M, Rodloff AC (2010) A real-time PCR assay for the differentiation of Candida species. J Appl Microbiol 109(4):1150–1158. doi:10.1111/j.1365-2672.2010.04736.x

    PubMed  CAS  Article  Google Scholar 

  46. Williams DW, Wilson MJ, Lewis MA, Potts AJ (1995) Identification of Candida species by PCR and restriction fragment length polymorphism analysis of intergenic spacer regions of ribosomal DNA. J Clin Microbiol 33(9):2476–2479

    PubMed  CAS  Google Scholar 

  47. Kanbe T, Horii T, Arishima T, Ozeki M, Kikuchi A (2002) PCR-based identification of pathogenic Candida species using primer mixes specific to Candida DNA topoisomerase II genes. Yeast 19(11):973–989. doi:10.1002/yea.892

    PubMed  CAS  Article  Google Scholar 

  48. Schabereiter-Gurtner C, Selitsch B, Rotter ML, Hirschl AM, Willinger B (2007) Development of novel real-time PCR assays for detection and differentiation of eleven medically important Aspergillus and Candida species in clinical specimens. J Clin Microbiol 45(3):906–914. doi:10.1128/JCM.01344-06

    PubMed  CAS  Article  Google Scholar 

  49. Quiles-Melero I, Garcia-Rodriguez J, Romero-Gomez MP, Gomez-Sanchez P, Mingorance J (2010) Rapid identification of yeasts from positive blood culture bottles by pyrosequencing. Eur J Clin Microbiol Infect Dis. doi:10.1007/s10096-010-1045-5

  50. Liguori G, Lucariello A, Colella G, De Luca A, Marinelli P (2007) Rapid identification of Candida species in oral rinse solutions by PCR. J Clin Pathol 60(9):1035–1039. doi:10.1136/jcp.2006.040782

    PubMed  CAS  Article  Google Scholar 

  51. Bustamante CI (2005) Treatment of Candida infection: a view from the trenches! Curr Opin Infect Dis 18(6):490–495

    PubMed  Article  Google Scholar 

  52. Bougnoux ME, Kac G, Aegerter P, Fagon JY, d’Enfert C (2008) Candidemia and candiduria in critically ill patients admitted to intensive care units in France: incidence, molecular diversity, management and outcome. Intensive Care Med 34(2):292–299. doi:10.1007/s00134-007-0865-y

    PubMed  Article  Google Scholar 

  53. Carey AJ, Saiman L, Polin RA (2008) Hospital-acquired infections in the NICU: epidemiology for the new millennium. Clin Perinatol 35(1):223–249. doi:10.j.clp.2007.1/j.clp.2007.11.014

    PubMed  Article  Google Scholar 

  54. Shorr AF, Tabak YP, Johannes RS, Sun X, Spalding J, Kollef MH (2009) Candidemia on presentation to the hospital: development and validation of a risk score. Crit Care 13(5):R156. doi:10.1186/cc8110

    PubMed  Article  Google Scholar 

  55. Cisterna R, Ezpeleta G, Telleria O, Guinea J, Regueiro B, Garcia-Rodriguez J, Esperalba J (2010) Nationwide sentinel surveillance of bloodstream Candida infections in 40 tertiary care hospitals in Spain. J Clin Microbiol 48(11):4200–4206. doi:10.1128/JCM.00920-10

    PubMed  CAS  Article  Google Scholar 

  56. Nucci M, Queiroz-Telles F, Tobon AM, Restrepo A, Colombo AL (2010) Epidemiology of opportunistic fungal infections in Latin America. Clin Infect Dis 51(5):561–570. doi:10.1086/655683

    PubMed  Article  Google Scholar 

  57. Kojic EM, Darouiche RO (2004) Candida infections of medical devices. Clin Microbiol Rev 17(2):255–267. doi:10.1128/cmr.17.2.255-267.2004

    PubMed  Article  Google Scholar 

  58. Achkar JM, Fries BC (2010) Candida infections of the genitourinary tract. Clin Microbiol Rev 23(2):253–273. doi:10.1128/CMR.00076-09

    PubMed  Article  Google Scholar 

  59. Jain N, Kohli R, Cook E, Gialanella P, Chang T, Fries BC (2007) Biofilm formation by and antifungal susceptibility of Candida isolates from urine. Appl Environ Microbiol 73(6):1697–1703. doi:10.1128/aem.02439-06

    PubMed  CAS  Article  Google Scholar 

  60. Pfaller MA (1992) Laboratory aids in the diagnosis of invasive candidiasis. Mycopathologia 120(2):65–72

    PubMed  CAS  Article  Google Scholar 

  61. Viale P (2009) Candida colonization and candiduria in critically ill patients in the intensive care unit. Drugs 69:51–57. doi:10.2165/11315640-000000000-00000

    PubMed  Article  Google Scholar 

  62. Paul N, Mathai E, Abraham OC, Michael JS, Mathai D (2007) Factors associated with candiduria and related mortality. J Infect 55(5):450–455. doi:10.j.clp.2007.1/j.jinf.2007.06.010

    PubMed  Article  Google Scholar 

  63. Binelli CA, Moretti ML, Assis RS, Sauaia N, Menezes PR, Ribeiro E, Geiger DC, Mikami Y, Miyaji M, Oliveira MS, Barone AA, Levin AS (2006) Investigation of the possible association between nosocomial candiduria and candidaemia. Clin Microbiol Infect 12(6):538–543. doi:10.1111/j.1469-0691.2006.01435.x

    PubMed  CAS  Article  Google Scholar 

  64. Munoz P, Giannella M, Fanciulli C, Guinea J, Valerio M, Rojas L, Rodriguez-Creixems M, Bouza E (2010) Candida tropicalis fungaemia: incidence, risk factors and mortality in a general hospital. Clin Microbiol Infect. doi:10.1111/j.1469-0691.2010.03338.x

  65. Kothavade RJ, Kura MM, Valand AG, Panthaki MH (2010) Candida tropicalis: its prevalence, pathogenicity and increasing resistance to fluconazole. J Med Microbiol 59(Pt 8):873–880. doi:10.1099/jmm.0.013227-0

    PubMed  CAS  Article  Google Scholar 

  66. Colombo AL, Guimarães T, Silva LRBF, Monfardini LPA, Cunha AKB, Rady P, Alves T, Rosas RC (2007) Prospective observational study of candidemia in São Paulo, Brazil: Incidence rate, epidemiology, and predictors of mortality. Infect Control Hosp Epidemiol 28(5):570–576. doi:10.1086/513615

    PubMed  Article  Google Scholar 

  67. Falagas ME, Roussos N, Vardakas KZ (2010) Relative frequency of albicans and the various non-albicans Candida spp among candidemia isolates from inpatients in various parts of the world: a systematic review. Int J Infect Dis 14(11):954–966. doi:10.j.clp.2007.1/j.ijid.2010.04.006

    Article  Google Scholar 

  68. Paulo C, Mourão C, Veiga PM, Marques JM, Rocha G, Alves AF, Querol A, Meliço-Silvestre AA, Gonçalves I, Flores O, Clemente C, Gonçalves T (2009) Retrospective analysis of clinical yeast isolates in a hospital in the centre of Portugal: spectrum and revision of the identification procedures. Med Mycol 19(1):1–10. doi:10.1080/13693780802709081

    Article  Google Scholar 

  69. Pfaller MA, Diekema DJ (2007) Epidemiology of invasive Candidiasis: a persistent public health problem. Clin Microbiol Rev 20(1):133–163. doi:10.1128/cmr.00029-06

    PubMed  CAS  Article  Google Scholar 

  70. Chen K, Chen Y, Lin Y, Chou H, Li S (2009) The molecular epidemiology of serial Candida tropicalis isolates from ICU patients as revealed by multilocus sequence typing and pulsed-field gel electrophoresis. Infect Genet Evol 9(5):912–920. doi:10.j.clp.2007.1/j.meegid.2009.06.011

    Google Scholar 

  71. Pappas Peter G, Kauffman Carol A, Andes D, Benjamin J, Daniel K, Calandra Thierry F, Edwards John E, Filler Scott G, Fisher John F, Kullberg BJ, Ostrosky-Zeichner L, Reboli AC, Rex John H, Walsh Thomas J, Sobel Jack D (2009) Clinical practice guidelines for the management of Candidiasis: 2009 update by the infectious diseases society of America. Clin Infect Dis 48(5):503–535. doi:10.1086/596757

    PubMed  CAS  Article  Google Scholar 

  72. Pfaller MA, Boyken L, Hollis RJ, Kroeger J, Messer SA, Tendolkar S, Diekema DJ (2009) Comparison of results of fluconazole and voriconazole disk diffusion testing for Candida spp. with results from a central reference laboratory in the ARTEMIS DISK Global Antifungal Surveillance Program. Diagn Microbiol Infect Dis 65(1):27–34. doi:10.j.clp.2007.1/j.diagmicrobio.2009.05.007

    PubMed  CAS  Article  Google Scholar 

  73. Negri M, Henriques M, Svidzinski TIE, Paula CR, Oliveira R (2009) Correlation between Etest®, disk diffusion, and microdilution methods for antifungal susceptibility testing of Candida species from infection and colonization. J Clin Lab Anal 23(5):324–330. doi:10.1002/jcla.20337

    PubMed  Article  Google Scholar 

  74. Desnos-Ollivier M, Bretagne S, Bernede C, Robert V, Raoux D, Chachaty E, Forget E, Lacroix C, Dromer F (2008) Clonal population of flucytosine-resistant Candida tropicalis from blood cultures, Paris, France. Emerg Infect Dis 14(4):557–565

    PubMed  CAS  Article  Google Scholar 

  75. Bedini A, Venturelli C, Mussini C, Guaraldi G, Codeluppi M, Borghi V, Rumpianesi F, Barchiesi F, Esposito R (2006) Epidemiology of candidaemia and antifungal susceptibility patterns in an Italian tertiary-care hospital. Clin Microbiol Infect 12(1):75–80. doi:10.1111/j.1469-0691.2005.01310.x

    PubMed  CAS  Article  Google Scholar 

  76. Krcmery V (1999) Torulopsis glabrata an emerging yeast pathogen in cancer patients. Int J Antimicrob Agents 11(1):1–6

    PubMed  CAS  Article  Google Scholar 

  77. Kumar C, Kumar S, Menon T (2006) Phospholipase and proteinase activities of clinical isolates of Candida from immunocompromised patients. Mycopathologia 161(4):213–218. doi:10.1007/s11046-005-0157-4

    PubMed  CAS  Article  Google Scholar 

  78. Hoyer LL, Fundyga R, Hecht JE, Kapteyn JC, Klis FM, Arnold J (2001) Characterization of agglutinin-like sequence genes from non-albicans Candida and phylogenetic analysis of the ALS family. Genetics 157(4):1555–1567

    PubMed  CAS  Google Scholar 

  79. Yang Y (2003) Virulence factors of Candida species. J Microbiol Immunol Infect 36(4):223–228

    PubMed  CAS  Google Scholar 

  80. Silva S, Negri M, Henriques M, Oliveira R, Williams D, Azeredo J (2010) Silicone colonization by non-Candida albicans Candida species in the presence of urine. J Med Microbiol 59(Pt 7):747–754. doi:10.1099/jmm.0.017517-0

    PubMed  CAS  Article  Google Scholar 

  81. Silva S, Hooper SJ, Henriques M, Oliveira R, Azeredo J, Williams DW (2011) The role of secreted aspartyl proteinases in Candida tropicalis invasion and damage of oral mucosa. Clin Microbiol Infect 17(2):264–272. doi:10.1111/j.1469-0691.2010.03248.x

    PubMed  CAS  Article  Google Scholar 

  82. Silva S, Negri M, Henriques M, Oliveira R, Williams DW, Azeredo J (2011) Adherence and biofilm formation of non-Candida albicans Candida species. Trends Microbiol 19(5):241–247. doi:10.j.clp.2007.1/j.tim.2011.02.003

    PubMed  CAS  Article  Google Scholar 

  83. Biasoli MS, Tosello ME, Luque AG, Magaró HM (2010) Adherence, colonization and dissemination of Candida dubliniensis and other Candida species. Med Mycol 48(2):291–297. doi:10.1080/13693780903114942

    PubMed  Article  Google Scholar 

  84. Negri M, Silva S, Henriques M, Azeredo J, Svidzinski T, Oliveira R (2011) Candida tropicalis biofilms: artificial urine, urinary catheters and flow model. Med Mycol 49(7):739–747

    PubMed  CAS  Google Scholar 

  85. Hasan F, Xess I, Wang X, Jain N, Fries BC (2009) Biofilm formation in clinical Candida isolates and its association with virulence. Microbes Infect 11(8–9):753–761. doi:10.j.clp.2007.1/j.micinf.2009.04.018

    PubMed  CAS  Article  Google Scholar 

  86. Blankenship JR, Mitchell AP (2006) How to build a biofilm: a fungal perspective. Curr Opin Microbiol 9(6):588–594. doi:10.j.clp.2007.1/j.mib.2006.10.003

    PubMed  CAS  Article  Google Scholar 

  87. Kumamoto CA (2002) Candida biofilms. Curr Opin Microbiol 5(6):608–611. doi:10.j.clp.2007.1/S1369-5274(02)00371-5

    PubMed  CAS  Article  Google Scholar 

  88. Douglas LJ (2003) Candida biofilms and their role in infection. Trends Microbiol 11(1):30–36. doi:10.j.clp.2007.1/S0966-842X(02)00002-1

    PubMed  CAS  Article  Google Scholar 

  89. Al-Fattani MA, Douglas LJ (2006) Biofilm matrix of Candida albicans and Candida tropicalis: chemical composition and role in drug resistance. J Med Microbiol 55(8):999–1008. doi:10.1099/jmm.0.46569-0

    PubMed  CAS  Article  Google Scholar 

  90. Silva S, Henriques M, Martins A, Oliveira R, Williams D, Azeredo J (2009) Biofilms of non-Candida albicans Candida species: quantification, structure and matrix composition. Med Mycol 47(7):681–689. doi:10.1080/13693780802549594

    PubMed  CAS  Article  Google Scholar 

  91. Al-Dhaheri RS, Douglas LJ (2008) Absence of amphotericin B-tolerant persister cells in biofilms of some Candida species. Antimicrob Agents Chemother 52(5):1884–1887. doi:10.1128/aac.01473-07

    PubMed  CAS  Article  Google Scholar 

  92. Loeffler J, Hagmeyer L, Hebart H, Henke N, Schumacher U, Einsele H (2000) Rapid detection of point mutations by fluorescence resonance energy transfer and probe melting curves in Candida species. Clin Chem 46(5):631–635

    PubMed  CAS  Google Scholar 

  93. Gotz F (2002) Staphylococcus and biofilms. Mol Microbiol 43(6):1367–1378

    PubMed  CAS  Article  Google Scholar 

  94. Bendel CM (2003) Colonization and epithelial adhesion in the pathogenesis of neonatal candidiasis. Semin Perinatol 27(5):357–364. doi:10.j.clp.2007.1/S0146-0005(03)00059-4

    PubMed  Article  Google Scholar 

  95. Bendel C, Hostetter M (1993) Distinct mechanisms of epithelial adhesion for Candida albicans and Candida tropicalis. Identification of the participating ligands and development of inhibitory peptides. J Clin Invest 92:1840–1849. doi:10.1172/JCI116775

    PubMed  CAS  Article  Google Scholar 

  96. Klotz SA, Drutz DJ, Harrison JL, Huppert M (1983) Adherence and penetration of vascular endothelium by Candida yeasts. Infect Immun 42(1):374–384

    PubMed  CAS  Google Scholar 

  97. Sohn K, Senyürek I, Fertey J, Königsdorfer A, Joffroy C, Hauser N, Zelt G, Brunner H, Rupp S (2006) An in vitro assay to study the transcriptional response during adherence of Candida albicans to different human epithelia. FEMS Yeast Res 6(7):1085–1093. doi:10.1111/j.1567-1364.2006.00130.x

    PubMed  CAS  Article  Google Scholar 

  98. Miyauchi M, Giummelly P, Yazawa S, Okawa Y (2007) Adhesion of Candida albicans to HeLa cells: studies using polystyrene beads. Biol Pharm Bull 30(3):588–590. doi:10.1248/bpb.30.588

    PubMed  CAS  Article  Google Scholar 

  99. Jayatilake J, Samaranayake Y, Cheung L, Samaranayake L (2006) Quantitative evaluation of tissue invasion by wild type, hyphal and SAP mutants of Candida albicans, and non-albicans Candida species in reconstituted human oral epithelium. J Oral Pathol Med 35(8):484–491. doi:10.1111/j.1600-0714.2006.00435.x

    PubMed  CAS  Article  Google Scholar 

  100. Arendrup M, Horn T, Frimodt-Moller N (2002) In vivo pathogenicity of eight medically relevant Candida species in an animal model. Infection 30(5):286–291. doi:10.1007/s15010-002-2131-0

    PubMed  CAS  Article  Google Scholar 

  101. Ghannoum MA (2000) Potential role of phospholipases in virulence and fungal pathogenesis. Clin Microbiol Rev 13(1):122–143. doi:10.1128/cmr.13.1.122-143.2000

    PubMed  CAS  Article  Google Scholar 

  102. Naglik JR, Challacombe SJ, Hube B (2003) Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol Mol Biol Rev 67(3):400–428. doi:10.1128/mmbr.67.3.400-428.2003

    PubMed  CAS  Article  Google Scholar 

  103. Prakobphol A, Leffler H, Fisher SJ (1994) Specific adherence of Candida tropicalis to lysophospholipids. Biochemistry 33(32):9496–9503

    PubMed  CAS  Article  Google Scholar 

  104. Kantarciôlu AS, Yücel A (2002) Phospholipase and protease activities in clinical Candida isolates with reference to the sources of strains. Mycoses 45(5–6):160–165. doi:10.1046/j.1439-0507.2002.00727.x

    Article  Google Scholar 

  105. Fu Y, Ibrahim AS, Fonzi W, Zhou X, Ramos CF, Ghannoum MA (1997) Cloning and characterization of a gene (LIP1) which encodes a lipase from the pathogenic yeast Candida albicans. Microbiology 143(Pt 2):331–340

    PubMed  CAS  Article  Google Scholar 

  106. Price M, Wilkinson I, Gentry L (1982) Plate method for detection of phospholipase activity in Candida albicans. Sabouraudia 20:7–14

    PubMed  CAS  Article  Google Scholar 

  107. da Costa K, Ferreira J, Komesu M, Candido R (2009) Candida albicans and Candida tropicalis in oral candidosis: quantitative analysis, exoenzyme activity, and antifungal drug sensitivity. Mycopathologia 167(2):73–79. doi:10.1007/s11046-008-9154-8

    PubMed  Article  Google Scholar 

  108. Furlaneto-Maia L, Specian A, Bizerra F, de Oliveira M, Furlaneto M (2007) In vitro evaluation of putative virulence attributes of oral isolates of Candida spp. obtained from elderly healthy individuals. Mycopathologia 166(4):209–217. doi:10.1007/s11046-008-9139-7

    Article  CAS  Google Scholar 

  109. Cafarchia C, Romito D, Coccioli C, Camarda A, Otranto D (2008) Phospholipase activity of yeasts from wild birds and possible implications for human disease. Med Mycol 46(5):429–434. doi:10.1080/13693780701885636

    PubMed  CAS  Article  Google Scholar 

  110. Luo G, Samaranayake LP, Yau JYY (2001) Candida species exhibit differential in vitro hemolytic activities. J Clin Microbiol 39(8):2971–2974. doi:10.1128/jcm.39.8.2971-2974.2001

    PubMed  CAS  Article  Google Scholar 

  111. Watanabe T, Takano M, Murakami M, Tanaka H, Matsuhisa A, Nakao N, Mikami T, Suzuki M, Matsumoto T (1999) Characterization of a haemolytic factor from Candida albicans. Microbiology 145(3):689–694. doi:10.1099/13500872-145-3-689

    PubMed  CAS  Article  Google Scholar 

  112. Manns JM, Mosser DM, Buckley HR (1994) Production of a hemolytic factor by Candida albicans. Infect Immun 62(11):5154–5156

    PubMed  CAS  Google Scholar 

  113. Kumar VG, Latha R, Vedhagiri K, Sathiamoorthi T, Jayarani G, Sasikala R, Selvin J, Natarajaseenivasan K (2009) Phospholipase C, proteinase and hemolytic activities of Candida spp. isolated from pulmonary tuberculosis patients. J Mycol Med 19(1):3–10. doi:10.j.clp.2007.1/j.mycmed.2008.11.002

    Google Scholar 

  114. Chang HC, Leaw SN, Huang AH, Wu TL, Chang TC (2001) Rapid identification of yeasts in positive blood cultures by a multiplex PCR method. J Clin Microbiol 39(10):3466–3471. doi:10.1128/JCM.39.10.3466-3471.2001

    PubMed  CAS  Article  Google Scholar 

  115. Mokaddas EM, Al-Sweih NA, Khan ZU (2007) Species distribution and antifungal susceptibility of Candida bloodstream isolates in Kuwait: a 10-year study. J Med Microbiol 56(2):255–259. doi:10.1099/jmm.0.46817-0

    PubMed  CAS  Article  Google Scholar 

  116. Tortorano AM, Kibbler C, Peman J, Bernhardt H, Klingspor L, Grillot R (2006) Candidaemia in Europe: epidemiology and resistance. Int J Antimicrob Agents 27(5):359–366. doi:10.j.clp.2007.1/j.ijantimicag.2006.01.002

    PubMed  CAS  Article  Google Scholar 

  117. Pfaller MA, Castanheira M, Messer SA, Moet GJ, Jones RN (2010) Variation in Candida spp. distribution and antifungal resistance rates among bloodstream infection isolates by patient age: report from the SENTRY Antimicrobial Surveillance Program (2008–2009). Diagn Microbiol Infect Dis 68(3):278–283. doi:10.j.clp.2007.1/j.diagmicrobio.2010.06.015

    PubMed  Article  Google Scholar 

  118. Dorko E, Pilipčinec E, Tkáčiková L (2002) Candidal urinary tract infections caused by non-albicans Candida species. Folia Microbiol 47(2):182–184. doi:10.1007/BF02817679

    CAS  Article  Google Scholar 

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Acknowledgments

The authors acknowledge Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brazil, for supporting Melyssa Negri (BEX 4642/06-6) and Fundação para a Ciência e Tecnologia (FCT), Portugal, for supporting Sonia Silva (SFRH/BPD/71076/2010), and European Community fund FEDER, trough Program COMPETE under the Project FCOMP-01-0124-FEDER-007025 (PTDC/AMB/68393/2006) is gratefully acknowledged.

Conflicts of interest

None declared.

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  1. Institute for Biotechnology and Bioengineering (IBB), Centre of Biological Engineering, Universidade do Minho, Campus de Gualtar, 4710-057, Braga, Portugal

    M. Negri, S. Silva, M. Henriques & R. Oliveira

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  1. M. Negri
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  2. S. Silva
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  3. M. Henriques
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  4. R. Oliveira
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Correspondence to M. Henriques.

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Negri, M., Silva, S., Henriques, M. et al. Insights into Candida tropicalis nosocomial infections and virulence factors. Eur J Clin Microbiol Infect Dis 31, 1399–1412 (2012). https://doi.org/10.1007/s10096-011-1455-z

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  • DOI: https://doi.org/10.1007/s10096-011-1455-z

Keywords

  • Candida tropicalis
  • Epidemiology
  • Risk factors
  • Virulence factors
  • Candiduria
  • Candidemia