, 162:45

Species Distribution and Antifungal Susceptibility Profile of Oral Candida Isolates from HIV-infected Patients in the Antiretroviral Therapy Era

  • Carolina Rodrigues Costa
  • Janine Aquino de Lemos
  • Xisto Sena Passos
  • Crystiane Rodrigues de Araújo
  • Ana Joaquina Cohen
  • Lúcia Kioko Hasimoto e Souza
  • Maria do Rosário Rodrigues Silva


In this study, we investigated the yeasts colonization of genus Candida, including C. dubliniensis, isolated of HIV-infected patients oral cavities and we accessed in vitro susceptibility pattern of the Candida isolates to four antifungal agents. Out of 99 patients investigated, 62 (62.6%) were colonized with yeasts. C. albicans was the prevailing species (50%). C. dubliniensis isolates were not recovered in our study. We verified that 8.1% of the yeasts isolated were resistant to fluconazole, 8.1% to itraconazole and 3.2% to voriconazole. The isolates demonstrated very low voriconazole MICs, in which 79% (49/62) presented values of 0.015 μg/ml. All Candida isolates were susceptible to amphotericin B. The results reported here showed that although C. albicans continues to be present in one-half of oral Candida carriage of HIV-infected patients, Candida non-albicans species are increasing among these patients. Besides, the findings of resistant isolates endorse the role of antifungal susceptibility testing whenever antifungal treatment with azoles is planned.


antifungal susceptibility asymptomatic oropharyngeal carriage Candida HIV-infected patients 



Dimetyl sulfoxide


Hospital de Doenças Tropicais


Human Immunodeficiency Virus


Minimal Inhibitory Concentrations


Morpholinepropanesulfonic acid


National Committee for Clinical Laboratory Standards


Oropharyngeal candidiasis


Sabouraud Dextrose Agar


  1. 1.
    Kirkpatrick, WR, Revankar, SG, Mcatee, RK, Lopez-Ribot, JL, Fothergill, AW, McCarthy, DL, Sanches, SE, Cantu, RA, Rinaldi, MG, Patterson, TF 1998Detection of Candida dubliniensis in oropharyngeal samples from human immunodeficiency virus-infected patients in North America by primary CHROMagar Candida screening and susceptibility testing of isolatesJ Clin Microbiol3630073012PubMedGoogle Scholar
  2. 2.
    Sullivan, DJ, Westerneng, TJ, Haynes, KA, Bennett, DE, Coleman, D 1995Candida dubliniensis sp. Nov: Phenotypic and molecular characterization of a novel species associated with oral candidosis in HIV-infected individualsMicrobiology14115071521PubMedGoogle Scholar
  3. 3.
    Fotedar, R, Al-Hedaithy, SSA 2005Comparison of phospholipase and proteinase activity in Candida albicans and C. dubliniensisMycoses486267PubMedCrossRefGoogle Scholar
  4. 4.
    Schorling, SR, Kortinga, HC, Froschb, M, Mühlsclegel, FA 2000The role of Candida dubliniensis in oral candidiasis in human immunodeficiency virus-infected individualCrit Rev Microbiol265968PubMedCrossRefGoogle Scholar
  5. 5.
    Dolapaci, I, Tekeli, A, Gocmen, JS, Aysev, D, Guriz, H 2002Investigation of Candida dubliniensis in Candida spp –positive hemoculturesAPMIS110391395CrossRefGoogle Scholar
  6. 6.
    Nenoff, P, Oswald, U, Haustein, UF 1999In vitro susceptibility of yeasts for fluconazole and itraconazole. Evaluation of a microdilution testMycoses42629639PubMedCrossRefGoogle Scholar
  7. 7.
    Colombo, AL, Da Matta, D, Almeida, LP, Rosas, R 2002Fluconazole susceptibility of Brazilian Candida isolates assessed by a disk diffusion methodJ Infect Dis6118123CrossRefGoogle Scholar
  8. 8.
    Sojakova, M, Liptajova, D, Borovsky, M, Subik, J 2004Fluconazole and itraconazole susceptibility of vaginal yeast isolates from SlovakiaMycopathologia157163169PubMedCrossRefGoogle Scholar
  9. 9.
    Kurtzman, CP, Fell, JW 1998The Yeasts: a taxonomic study4ElsevierAmsterdam77100Google Scholar
  10. 10.
    Tekeli, A, Koyuncu, E, Dolapaci, I, Guven, GS, Sahin, GO, Uzin, O 2005Detection of Candida dubliniensis in oropharyngeal samples of Turkish HIV-positive patientsMycoses48197201PubMedCrossRefGoogle Scholar
  11. 11.
    NCCLS-National Committee for Clinical Laboratory Standards 2002. Reference method for broth dilution antifungal susceptibility testing of yeasts: approved standard. Document M27-A2. Villanova, PA, v. 17, n. 9Google Scholar
  12. 12.
    Nguyen, MH, Chancy, CJ, Yu, VL, Yu, YC, Morris, AJ, Snydman, DR 1998Do in vitro susceptibility data predict the microbiological response to Amphotericin B? Results of a prospective study of patients with Candida fungemiaJ Infect Dis177425430PubMedCrossRefGoogle Scholar
  13. 13.
    Pfaller, MA, Diekman, DJ, Jones, RN, Sader, HS, Fluit, AC, Hollis, RJ 2001International surveillance of bloodstream infections due to Candida species, frequency of occurrence and in vitro susceptibilities to fluconazole, ravuconazole, voriconazole of isolates collected from 1997 through 1999 in the SENTRY antimicrobial surveillance programJ Clin Microbiol3932543259PubMedCrossRefGoogle Scholar
  14. 14.
    Fidel, PL,Jr, Vazquez, JA, Sobel, JD 1999Candida glabrata: review of epidemiology, pathogenesis and clinical disease with comparison to C. albicansRev Clin Microbiol128096Google Scholar
  15. 15.
    Melo, NR, Taguchi, H, Jorge, J, Pedro, RJ, Almeida, OP, Fukushinma, K, Nishimura, K, Muyaji, M 2004Oral Candida from Brazilian Human Immunodeficiency virus-infected patients in the highly active antiretroviral therapy eraMem Inst Oswaldo Cruz99425431PubMedCrossRefGoogle Scholar
  16. 16.
    Drondra, F, Alonso-Sanz, M, Laguna, F, Chavez, F, Martinez-Suarez, JV, Rodríguez-Tudella, JL, Gonzalez-Lopez, A, Valencia, E 1996Mixed oropharyngeal candidiasis due to Candida albicans and non albicans Candida strains in HIV-infected patientsEur J Clin Microbiol Infect Dis19446452CrossRefGoogle Scholar
  17. 17.
    Redding, SW, Kirkpatrick, WR, Dib, O, Fothergill, AW, Rinaldi, MG, Patterson, TF 2000The epidemiology of non albicans Candida in oropharyngeal candidiasis in HIV-patientsSpec Care Dentist207881Google Scholar
  18. 18.
    Fotos, PG, Hellstein, JW 1992Candida and candidosisEpidemiology, diagnosis and therapeutic management Dent Clin North Am36857858Google Scholar
  19. 19.
    Sullivan, DJ, Coleman, DC 1998Candida dubliniensis: characteristics and identificationJ Clin Microbiol36329334PubMedGoogle Scholar
  20. 20.
    Meis, JFGM, Ruhnke, M, Pauw, BED, Odds, FC, Siegert, W, Verweij, PE 1999Candida dubliniensis candidemia in patients with chemotherapy-induced neutropenia and bone marrow transplantationEmerg. Infect Dis5150153PubMedCrossRefGoogle Scholar
  21. 21.
    Brandt, ME, Harrison, LH, Pass, M, Sofair, NA, Huje, S, Li, R, Morrison, CJ, Warnock, DW, Hajjeh, RA 2000Candida dubliniensis fungemia: the first four cases in North AmericaEmerg Infect Dis64649PubMedGoogle Scholar
  22. 22.
    Willis, AM, Coulter, WA, Sullivan, DJ, Coleman, DC, Hayes, JR, Bell, PM, Lamey, PJ 2000Isolation of Candida dubliniensis from insulin diabetes mellitus patientsJ Oral Pathol Med298690PubMedCrossRefGoogle Scholar
  23. 23.
    Müller, TJ, Jabra-Riszk, MA, Baqui, A, Kelley, JI, Meeks, VI, Merz, WG, Falkler, WA 1999Oral Candida dubliniensis as a clinically important species in HIV-seropositive patients in the United StatesOral Surg Oral Med Oral Pathol Oral Radiol Endod88573580CrossRefGoogle Scholar
  24. 24.
    Mariano, PLS, Milan, EP, Matta, DA, Colombo, AL 2003Candida dubliniensis identification in Brazil yeast stock collectionMem Inst Oswaldo Cruz98533538CrossRefGoogle Scholar
  25. 25.
    Godoy, P, Tiraboshi, IN, Severo, LC, Bustamante, B, Calvo, B, Almeida, LP, Matta, DA, Colombo, AL 2003Species distribution and antifungal susceptibility profile of Candida spp bloodstream isolates from Latin American HospitalsMem Inst Oswaldo Cruz98401405PubMedCrossRefGoogle Scholar
  26. 26.
    Ribeiro, MA, Dietze, R, Paula, CR, Matta, DA, Colombo, AL 2000Susceptibility profile of vaginal yeast isolates from BrazilMycopathologia151510CrossRefGoogle Scholar
  27. 27.
    Pfaller, MA, Messer, SA, Hollis, RJ 1994Strain delineation and antifungal susceptibilities of epidemiologically related and unrelated isolates of Candida lusitaniaeDiagn Microbiol Infect Dis20127133PubMedCrossRefGoogle Scholar
  28. 28.
    Hardfield, TL, Smith, MB, Winn, RE, Rinaldi, MG, Guerra, C 1997Mycoses caused by Candida lusitaniaeRev Infect Dis910061012Google Scholar
  29. 29.
    Pfaller, MA, Diekema, DJ, Messer, SA, Boyken, L, Hollis, RJ, Jones, RN 2003International Fungal Surveillance Participant Group. In vitro activities of voriconazole, posaconazole and four licensed systemic antifungal agents against Candida species infrequently isolated from bloodJ Clin Microbiol417883PubMedCrossRefGoogle Scholar
  30. 30.
    Favel, A, Michel-Nguyen, A, Datry, A, Charllier, S, Leclerc, F, Chastin, C, Fallague, K, Regli, P 2004Susceptibility of clinical isolates of Candida lusitaniae to five systemic antifungal agentsJ Antimicrobial Chemother53526529CrossRefGoogle Scholar
  31. 31.
    Martins, MD, Lozano-Chiu, M, Rex, JH 1997Point prevalence of carriage of fluconazole in the oropharyngeal of HIV infected patientsClin Infect Dis25843846PubMedGoogle Scholar
  32. 32.
    Lattif, AB, Banerjee, U, Prasad, R, Biswas, A, Wig, N, Sharma, N, Haque, A, Gupta, N, Baquer, NZ, Mukhopadhyay, G 2004Susceptibility pattern and molecular type of species-specific Candida in oropharyngeal lesions of Indian Human Immunodeficiency Virus-positive patientsJ Clin Microbiol4212601262PubMedCrossRefGoogle Scholar
  33. 33.
    Wildfener, A, Seidl, HP, Paule, I, Haberreiter, A 1998In vitro evaluation of voriconazole against clinical isolates of yeast, moulds and dermatophytes in comparison with itraconazole, ketoconazole, amphotericin B and griseofulvinMycoses41309319CrossRefGoogle Scholar
  34. 34.
    Sabo, JA, Abdel-Rahman, SM 2000Voriconazole a new triazole antifungalAnn Pharmacother3410321043PubMedCrossRefGoogle Scholar
  35. 35.
    Cuenca-Estrela, M, Mellado, E, Guerra, TMD, Monzón, , Tudela, JLR 2000Susceptibility of fluconazole-resistant clinical isolates of Candida spp. to echinocandin LY303366, itraconazol and amphotericin BJ Antimicrob Chemother46475477CrossRefGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • Carolina Rodrigues Costa
    • 1
  • Janine Aquino de Lemos
    • 1
  • Xisto Sena Passos
    • 1
  • Crystiane Rodrigues de Araújo
    • 1
  • Ana Joaquina Cohen
    • 2
  • Lúcia Kioko Hasimoto e Souza
    • 1
  • Maria do Rosário Rodrigues Silva
    • 1
    • 3
  1. 1.Instituto de Patologia Tropical e Saúde Pública daUniversidade Federal de GoiásGoiásBrazil
  2. 2.Hospital de Doenças Tropicais de GoiásGoiásBrazil
  3. 3.Maria do Rosário Rodrigues SilvaGoianiaBrasil

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