, Volume 162, Issue 2, pp 83–89 | Cite as

Species diversity of yeast in oral colonization of insulin-treated diabetes mellitus patients

  • Regina Helena Pires Gonçalves
  • Elaine Toscano Miranda
  • José Eduardo Zaia
  • Maria José Soares Mendes Giannini


The aim of this study was to investigate oral yeast colonization, antifungal susceptibility and strain diversity in insulin-dependent diabetes mellitus patients (175), as well as to evaluate the influence of dental prostheses. Oral rinse samples were cultured on selective media, in order to isolate, count and identify the yeasts recovered. More than half of the diabetic subjects (53%) carried significant amounts of Candida cells in the buccal cavity and these organisms were recovered at higher densities in diabetics wearing dentures. A total of 93 yeast strains were isolated from these patients, including: Candida spp. (n = 89); Pichia (n = 02); Trichosporon (n = 1), and Geotrichum (n = 1). C. albicans represented 56% of these strains, non-albicans Candida 39.8%, and other genera of yeast 4.3%. C. albicans was prevalent, followed by C. parapsilosis, C. tropicalis, C. glabrata, C. krusei, C. rugosa and C. guilliermondii. Agar disk-diffusion tests of the susceptibility of non-albicans Candida and other genera of yeast to fluconazole showed resistance in 21.9%, mainly in C. rugosa (100%), C. glabrata (57%) and C. krusei (50%). Local oral factors, such as the presence of dentures, in association with diabetes, seemed to have the effect of increasing the amount and variety of Candida species in the oral cavities, mainly those with lower drug susceptibilities.


Candida spp. diabetes mellitus disk diffusion prostheses oral carriage 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Ghannoum, MA, Radwan, SS 1990Candida Adherence to Epithelial CellsCRCBoca RatonGoogle Scholar
  2. 2.
    Knight, L, Fletcher, J 1971Growth of Candida albicans in saliva: stimulation by glucose associated with antibiotics, corticosteroids, and diabetes mellitusJ Infect Dis123321377Google Scholar
  3. 3.
    Darwazeh, AMG, Lamey, PL, Samaranayake, LP, MacFarlane, TW, Fisher, BM, Macrury, SM 1990The relationship between colonization, secretor status and in-vitro adhesion of Candida albicans to buccal epithelial cells from diabeticsJ Med Microbiol334349PubMedCrossRefGoogle Scholar
  4. 4.
    Guggenheimer, J, Moore, PA, Rossie, K, Myers, D, Mongeluzzo, M, Block, HM, Weyant, R, Orchard, T 2000Insulin-dependent diabetes mellitus and oral soft tissue pathologies. II. Prevalence and characteristics of Candida and candidal lesionsOral Surg Oral Med Oral Pathol Oral Radiol Endod89570576PubMedGoogle Scholar
  5. 5.
    Bridges, CG, DaSilva, GL, Yamamura, M, Valdimarsson, M 1980A radiometric assay for the combined measurement of phagocytosis and intracellular killing of Candida albicans Clin Exp Immunol42226233PubMedGoogle Scholar
  6. 6.
    Ueta, E, Osaki, T, Yoneda, AK, Yamamoto, T 1993Prevalence of diabetes mellitus in odontogenic infections and oral candidiasis: an analysis of neutrophil suppressionJ Oral Pathol Med22168174PubMedCrossRefGoogle Scholar
  7. 7.
    Calderone, RA 2002Candida and CandidiasisASM PressWashington, DCGoogle Scholar
  8. 8.
    Manfredi, M, Al-karaawi, Z, McCullough, MJ, Hurel, S, Porter, SR 2002The isolation, identification and molecular analysis of Candida spp. isolated from the oral cavities of patients with diabetes mellitusOral Microbiol Immunol17181185PubMedCrossRefGoogle Scholar
  9. 9.
    Willis, AM, Coulter, WA, Sullivan, DJ, Coleman, DC, Hayes, JR, Bell, PM, Lamey, PJ 2000Isolation of C. dubliniensis from insulin-using diabetes mellitus patientsJ Oral Pathol Med298690PubMedCrossRefGoogle Scholar
  10. 10.
    Bart-Delabesse, E, Boiron, P, Carlotti, A, Dupont, B 1993 Candida albicans genotyping in studies with patients with AIDS developing resistance to fluconazoleJ Clin Microbiol1129332937Google Scholar
  11. 11.
    Aly, FZM, Blackwell, CC, Mackenzie, DAC, Weir, DM, Elton, RA, Cumming, CG, Sofaer, J, Clarke, BF 1991Chronic atropic oral candidiasis among patients with diabetes mellitus – role of secretor statusEpidemiol Infect106355363PubMedGoogle Scholar
  12. 12.
    Willis, AM, Coulter, WA, Fulton, CR, Hayes, J, Bell, PM, Lamey, PJ 1999Oral candidal carriage and infection in insulin-treated diabetic patientsDiabet Med16675679PubMedCrossRefGoogle Scholar
  13. 13.
    Pfaller, MA 1994Strain delineation and antifungal susceptibilities of epidemiologically related and unrelated isolates of Candida lusitanae Diagn Microbiol Infect Dis20127133PubMedCrossRefGoogle Scholar
  14. 14.
    White, TC, Kieren, AM, Bowden, RA 1998Clinical, cellular, and molecular factors that contribute to antifungal drug resistanceClin Microbiol Rev11382402PubMedGoogle Scholar
  15. 15.
    Xu, J, Ramos, AR, Vilgalys, R, Mitchell, TG 2000Clonal and spontaneous origins of fluconazole resistance in Candida albicans J Clin Microbiol3812141220PubMedGoogle Scholar
  16. 16.
    Brun, S, Aubry, C, Lima, O, Filmon, R, Bergès, T, Chabasse, D, Bouchara, J-P 2003Relationships between respiration and susceptibility to azole antifungals in Candida glabrata Antimicrob Agents Chemother47847853PubMedCrossRefGoogle Scholar
  17. 17.
    Dib, JC, Dube, M, Kelly, C, Rinaldi, MG, Patterson, JE 1996Evaluation of pulsed-field gel electrophoresis as a typing system for Candida rugosa: comparison of karyotype and restriction fragment length polymorphismsJ Clin Microbiol3414941496PubMedGoogle Scholar
  18. 18.
    Nho, S, Anderson, MJ, Moore, CB, Denning, DW 1997Species differentiation by internally transcribed spacer PCR and HhaI digestion of fluconazole-resistance Candida krusei, Candida inconspicua, and Candida norvegensis strainsJ Clin Microbiol410361039Google Scholar
  19. 19.
    Samaranayake, LP, MacFarlane, TW, Lamey, PJ, Ferguson, MM 1986A comparison of oral rinse and imprint sampling techniques for the detection of yeast, coliform and Staphylococcus aureus carriage in the oral cavityJ Oral Pathol15386388PubMedCrossRefGoogle Scholar
  20. 20.
    Kurtzman, CP, Fell, JW 1998The Yeasts: a Taxonomic StudyElsevierAmsterdamGoogle Scholar
  21. 21.
    Gales, AC, Pfaller, MA, Houston, AK, Joly, S, Sullivan, DJ, Coleman, DC, Soll, DR 1999Identification of Candida dubliniensis based on temperature and utilization of xylose and α-methyl-D-glucoside as determined with API 20C AUX and Vitek YBC SystemsJ Clin Microbiol3738043808PubMedGoogle Scholar
  22. 22.
    National Committee for Clinical Laboratory Standards. Method for antifungal disk diffusion susceptibility testing of yeasts: proposed guideline M44-P. National Committee for Clinical Laboratory Standards, Wayne, Pa., 2003.Google Scholar
  23. 23.
    Zar, JH 1999Biostatistical Analysis4Prentice HallNew JerseyGoogle Scholar
  24. 24.
    Odds, FC 1988Candida and Candidosis: a Review and Bibliography,2Ballière TindallLondonGoogle Scholar
  25. 25.
    Tapper-Jones, LM, Aldred, MJ, Walker, DM, Hayes, TM 1981Candidal infections and populations of Candida albicans in mouths of diabeticsJ. Clin. Pathol.34706711PubMedGoogle Scholar
  26. 26.
    Wilson, RM, Reeves, WG 1986Neutrophil phagocytosis and killing in insulin-dependent diabetesClin. Exp. Immunol.63478484PubMedGoogle Scholar
  27. 27.
    Aly, FZ, Blackwell, CC, Mackenzie, DA, Weir, DM 1995Identification of oral yeast species isolated from individuals with diabetes mellitusMycoses38107110PubMedCrossRefGoogle Scholar
  28. 28.
    Jorge, AOC, Koga-Ito, CY, Gonçalves, CR, Fantinato, V, Unterkircher, CS 1997Presença de leveduras do gênero Candida na saliva de pacientes com diferentes fatores predisponentes e de indivíduos controleRev Odontol Univ São Paulo11279284Google Scholar
  29. 29.
    Bartholomew, GA, Rodu, B, Bell, DS 1987Oral candidiasis in patients with diabetes mellitus: a thorough analysisDiabetes Care10607612PubMedGoogle Scholar
  30. 30.
    Quirino, MRS, Birman, EG, Paula, CR 1995Oral manifestations of diabetes mellitus in controlled and uncontrolled patientsBraz Dent J6131136PubMedGoogle Scholar
  31. 31.
    Torres, SR, Peixoto, CB, Caldas, DM, Silva, EB, Magalhães, FA, Uzeda, M, NucciI, M 2003Clinical aspects of Candida species carriage in saliva of xerostomic subjectsMed Mycol41411415PubMedCrossRefGoogle Scholar
  32. 32.
    Colombo, AL, Matta, D, Almeida, LP, Rosas, R 2002Fluconazole susceptibility of Brazilian Candida isolates assessed by a disk diffusion methodBraz J Infect Dis6118123PubMedCrossRefGoogle Scholar
  33. 33.
    Stenderup, A 1990Oral mycologyActa Odontol Scand8310Google Scholar
  34. 34.
    Kleinegger, CL, Lockhart, SR, Vargas, K, Soll, DR 1996Frequency, intensity, species, and strains of oral Candida vary as a function of host ageJ Clin Microbiol3422462254PubMedGoogle Scholar
  35. 35.
    Fongsmut, T, Deerochanawong, C, Prachyabrued, W 1998Intraoral Candida in Thai diabetes patientsJ Med Assoc Thai81449453PubMedGoogle Scholar
  36. 36.
    Wright, PS, Clark, P, Hardie, JM 1985The prevalence and significance of yeasts in persons wearing complete dentures with soft-lining materialsJ Dent Res64122125PubMedGoogle Scholar
  37. 37.
    Biafasiewicz, D, Kurnatowska, A, Smiech-Slombowska, G 1993Characteristics of fungi and attempts of their elimination from the oral cavity in children treated with orthodontic appliancesMed Dosw Mikrobiol45389392Google Scholar
  38. 38.
    Clayton, YM, Shao, J, Brubaker, G 1991Oral yeast flora of a population in an area of Tanzania borderin an AIDS endemic zoneEast Afr Med J68975979PubMedGoogle Scholar
  39. 39.
    Singh, K, Chakrabarti, A, Narang, A, Gopalan, S 1999Yeast colonization & fungemia in preterm neonates in a tertiary care centreIndian J Med Res110169173PubMedGoogle Scholar
  40. 40.
    Krcmery, V, Barnes, AJ 2002Non-albicans Candida spp. causing fungaemia: pathogenicity and antifungal resistanceJ Hosp Infect50243260PubMedCrossRefGoogle Scholar
  41. 41.
    Rex, JH, Rinaldi, MG, Pfaller, MA 1995Resistance of Candida species to fluconazoleAntimicrob Agents Chemother1918Google Scholar
  42. 42.
    Sandven, P 1999Detection of fluconazole-resistant Candida strains by a disc diffusion screening testJ Clin Microbiol3738563859PubMedGoogle Scholar
  43. 43.
    Rex, JH, Pfaller, MA, Walsh, TJ, Chaturvedi, V, Espinel-Ingroff, A, Ghannoum, MA, Gosey, II, Odds, FC, Rinaldi, MG, Sheehan, DJ, Warnock, DW 2001Antifungal susceptibility testing: practical aspects and current challengesClin Microbiol Rev14643658PubMedCrossRefGoogle Scholar
  44. 44.
    Barry, AL, Brown, SD 1996Fluconazole disk diffusion procedure for determining susceptibility of Candida speciesJ Clin Microbiol3421542157PubMedGoogle Scholar
  45. 45.
    Bille, J, Glauser, MP 1997Evaluation of the susceptibility of pathogenic Candida species to fluconazole. Fluconazole Global Susceptibility Study GroupEur J Clin Microbiol Infect Dis16924928PubMedCrossRefGoogle Scholar
  46. 46.
    Meis, J, Petrou, M, Bille, J, Ellis, D, Gibbs, D 2000Global Antifungal Surveillance Group. A global evaluation of the susceptibility of Candida species to fluconazole by disk diffusionDiagn Microbiol Infect Dis36215223PubMedCrossRefGoogle Scholar
  47. 47.
    Morace, G, Amato, G, Bistoni, F, Fadda, G, Marone, P, Montagna, MT, Oliveri, S, Polonelli, L, Rigoli, R, Mancuso, I, Face, S, Masucci, L, Romano, L, Napoli, C, Tato, D, Buscema, MG, Belli, CMC, Piccirillo, MM, Conti, S, Covan, S, Fanti, F, Cavanna, C, D’Alo, F, Pitzurra, L 2002Multicenter comparative evaluation of six commercial systems and the National Committee for Clinical Laboratory Standards M27-A broth microdilution method for fluconazole susceptibility testing of Candida speciesJ Clin Microbiol4029532958PubMedCrossRefGoogle Scholar
  48. 48.
    Testore, GP, Falco, F, Sarrechia, C, Sordillo, P, Bontempo, G, Andreoni, M 2001Two-year surveillance on fluconazole susceptibility of Candida isolates in a general and university hospital in RomeDiagn Microbiol Infect Dis412327PubMedCrossRefGoogle Scholar
  49. 49.
    Colombo, AL, Melo, ASA, Rosas, RFC, Salomão, R, Briones, M, Hollis, RJ, Messer, AS, Pfaller, MA 2003Outbreak of Candida rugosa candidemia: an emerging pathogen that may be refractory to amphotericin B therapyDiagn Microbiol Infect Dis46253257PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • Regina Helena Pires Gonçalves
    • 1
  • Elaine Toscano Miranda
    • 1
  • José Eduardo Zaia
    • 2
  • Maria José Soares Mendes Giannini
    • 1
    • 3
  1. 1.Faculdade de Ciências Farmacêuticas, Departamento de Análises ClínicasUNESPAraraquaraBrasil
  2. 2.Universidade de FrancaUNIFRANFrancaBrasil
  3. 3.Maria José Soares Mendes GianniniAraraquara, SãoPauloBrasil

Personalised recommendations