Abstract
Pregnancy and diabetes are regarded as individual risk factors for vaginal candidiasis. The high prevalence of vaginal candidiasis in pregnant diabetic women can be explained by disruption of the balance of the vaginal normal flora. However, little is known about the overall structure and composition of the vaginal fungal flora in pregnant diabetic women. In the present study, the diversity and richness of the vaginal fungal flora in healthy non-pregnant women (group HN), healthy pregnant women (group HP), women with gestational diabetes mellitus (group GDM), and pregnant women with diabetes mellitus type I (group T1DM) were investigated using an 18S rRNA gene clone library method. Our data demonstrated that the composition of the vaginal fungal flora in the four groups could be divided into two phyla (Ascomycetes, 20/26, and Basidiomycetes, 6/26). The most predominant vaginal fungal species belonged to the Candida and Saccharomyces genera, uncultured fungi, and a large number of low-abundance taxa that were unrecorded or underrepresented in previous studies using cultivation-dependent methods. Variation in operational taxonomic units (OTUs) between the study cohorts was generally high in the clone libraries, as 9, 13, 17, and 20 phylotypes were identified in groups HN, HP, GDM, and T1DM, respectively. The Shannon indices of groups GDM and T1DM (with poorer glycemic control) were significantly higher compared to groups HN and HP (p < 0.05). The data presented here revealed an increased diversity and varied composition of the vaginal fungal flora in pregnant diabetic women and demonstrated that poor glycemic control might be associated with disturbances in the vaginal fungal flora.
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Nowakowska D, Kurnatowska A, Stray-Pedersen B, Wilczyński J (2004) Activity of hydrolytic enzymes in fungi isolated from diabetic pregnant women: is there any relationship between fungal alkaline and acid phosphatase activity and glycemic control? APMIS 112:374–383
Guzel AB, Ilkit M, Burgut R, Urunsak IF, Ozgunen FT (2011) An evaluation of risk factors in pregnant women with Candida vaginitis and the diagnostic value of simultaneous vaginal and rectal sampling. Mycopathologia 172:25–36
Goswami R, Dadhwal V, Tejaswi S, Datta K, Paul A, Haricharan RN, Banerjee U, Kochupillai NP (2000) Species-specific prevalence of vaginal candidiasis among patients with diabetes mellitus and its relation to their glycaemic status. J Infect 41:162–166
Nowakowska D, Kurnatowska A, Stray-Pedersen B, Wilczyński J (2004) Species distribution and influence of glycemic control on fungal infections in pregnant women with diabetes. J Infect 48:339–346
Segal E, Soroka A, Schechter A (1984) Correlative relationship between adherence of Candida albicans to human vaginal epithelial cells in vitro and candidal vaginitis. Sabouraudia 22:191–200
Cotch MF, Hillier SL, Gibbs RS, Eschenbach DA; Vaginal Infections and Prematurity Study Group (1998) Epidemiology and outcomes associated with moderate to heavy Candida colonization during pregnancy. Am J Obstet Gynecol 178:374–380
Frerich W, Gad A (1977) The frequency of Candida infections in pregnancy and their treatment with clotrimazole. Curr Med Res Opin 4:640–644
Hay P, Czeizel AE (2007) Asymptomatic trichomonas and Candida colonization and pregnancy outcome. Best Pract Res Clin Obstet Gynaecol 21:403–409
Goswami D, Goswami R, Banerjee U, Dadhwal V, Miglani S, Lattif AA, Kochupillai N (2006) Pattern of Candida species isolated from patients with diabetes mellitus and vulvovaginal candidiasis and their response to single dose oral fluconazole therapy. J Infect 52:111–117
Sobel JD, Faro S, Force RW, Foxman B, Ledger WJ, Nyirjesy PR, Reed BD, Summers PR (1998) Vulvovaginal candidiasis: epidemiologic, diagnostic, and therapeutic considerations. Am J Obstet Gynecol 178:203–211
Borman AM, Linton CJ, Miles SJ, Johnson EM (2008) Molecular identification of pathogenic fungi. J Antimicrob Chemother 61(Suppl 1):i7–i12
Staley JT, Konopka A (1985) Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Annu Rev Microbiol 39:321–346
Zhou X, Bent SJ, Schneider MG, Davis CC, Islam MR, Forney LJ (2004) Characterization of vaginal microbial communities in adult healthy women using cultivation-independent methods. Microbiology 150(Pt 8):2565–2573
Zhou ZX, Jiang H, Yang C, Yang MZ, Zhang HB (2010) Microbial community on healthy and diseased leaves of an invasive plant Eupatorium adenophorum in Southwest China. J Microbiol 48:139–145
American Diabetes Association (2011) Diagnosis and classification of diabetes mellitus. Diabetes Care 34(Suppl 1):S62–S69
Eckert LO, Hawes SE, Stevens CE, Koutsky LA, Eschenbach DA, Holmes KK (1998) Vulvovaginal candidiasis: clinical manifestations, risk factors, management algorithm. Obstet Gynecol 92:757–765
Ling Z, Kong J, Liu F, Zhu H, Chen X, Wang Y, Li L, Nelson KE, Xia Y, Xiang C (2010) Molecular analysis of the diversity of vaginal microbiota associated with bacterial vaginosis. BMC Genomics 11:488
Schabereiter-Gurtner C, Piñar G, Lubitz W, Rölleke S (2001) Analysis of fungal communities on historical church window glass by denaturing gradient gel electrophoresis and phylogenetic 18S rDNA sequence analysis. J Microbiol Methods 47:345–354
Smit E, Leeflang P, Glandorf B, Van Elsas JD, Wernars K (1999) Analysis of fungal diversity in the wheat rhizosphere by sequencing of cloned PCR-amplified genes encoding 18S rRNA and temperature gradient gel electrophoresis. Appl Environ Microbiol 65:2614–2621
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Suau A, Bonnet R, Sutren M, Godon JJ, Gibson GR, Collins MD, Doré J (1999) Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Appl Environ Microbiol 65:4799–4807
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Gomes NC, Fagbola O, Costa R, Rumjanek NG, Buchner A, Mendona-Hagler L, Smalla K (2003) Dynamics of fungal communities in bulk and maize rhizosphere soil in the tropics. Appl Environ Microbiol 69:3758–3766
Ott SJ, Kühbacher T, Musfeldt M, Rosenstiel P, Hellmig S, Rehman A, Drews O, Weichert W, Timmis KN, Schreiber S (2008) Fungi and inflammatory bowel diseases: alterations of composition and diversity. Scand J Gastroenterol 43:831–841
Burton JP, Reid G (2002) Evaluation of the bacterial vaginal flora of 20 postmenopausal women by direct (Nugent score) and molecular (polymerase chain reaction and denaturing gradient gel electrophoresis) techniques. J Infect Dis 186:1770–1780
Guo R, Zheng N, Lu H, Yin H, Yao J, Chen Y (2012) Increased diversity of fungal flora in the vagina of patients with recurrent vaginal candidiasis and allergic rhinitis. Microb Ecol 64:918–927
Wright AD, Auckland CH, Lynn DH (2007) Molecular diversity of methanogens in feedlot cattle from Ontario and Prince Edward Island, Canada. Appl Environ Microbiol 73:4206–4210
Reed BD (1992) Risk factors for Candida vulvovaginitis. Obstet Gynecol Surv 47:551–560
Kelekci S, Kelekci H, Cetin M, Inan I, Tokucoglu S (2004) Glucose tolerance in pregnant women with vaginal candidiasis. Ann Saudi Med 24:350–353
Nowakowska D, Kurnatowska A, Stray-Pedersen B, Wilczynski J (2004) Prevalence of fungi in the vagina, rectum and oral cavity in pregnant diabetic women: relation to gestational age and symptoms. Acta Obstet Gynecol Scand 83:251–256
Haynes K (2001) Virulence in Candida species. Trends Microbiol 9(12):591–596
Bohannon NJ (1998) Treatment of vulvovaginal candidiasis in patients with diabetes. Diabetes Care 21:451–456
Wilson RM, Tomlinson DR, Reeves WG (1987) Neutrophil sorbitol production impairs oxidative killing in diabetes. Diabet Med 4:37–40
Rayfield EJ, Ault MJ, Keusch GT, Brothers MJ, Nechemias C, Smith H (1982) Infection and diabetes: the case for glucose control. Am J Med 72:439–450
Carrara MA, Bazotte RB, Donatti L, Svidzinski TI, Consolaro ME, Patussi EV, Batista MR (2009) Effect of experimental diabetes on the development and maintenance of vulvovaginal candidiasis in female rats. Am J Obstet Gynecol 200:659.e1–659.e4
Darwazeh AM, MacFarlane TW, McCuish A, Lamey PJ (1991) Mixed salivary glucose levels and candidal carriage in patients with diabetes mellitus. J Oral Pathol Med 20:280–283
Reinhart H, Muller G, Sobel JD (1985) Specificity and mechanism of in vitro adherence of Candida albicans. Ann Clin Lab Sci 15:406–413
Samaranayake LP, MacFarlane TW (1982) The effect of dietary carbohydrates on the in-vitro adhesion of Candida albicans to epithelial cells. J Med Microbiol 15:511–517
Ehrström S, Yu A, Rylander E (2006) Glucose in vaginal secretions before and after oral glucose tolerance testing in women with and without recurrent vulvovaginal candidiasis. Obstet Gynecol 108:1432–1437
Willis AM, Coulter WA, Hayes JR, Bell P, Lamey PJ (2000) Factors affecting the adhesion of Candida albicans to epithelial cells of insulin-using diabetes mellitus patients. J Med Microbiol 49:291–293
Antonio MA, Rabe LK, Hillier SL (2005) Colonization of the rectum by Lactobacillus species and decreased risk of bacterial vaginosis. J Infect Dis 192:394–398
Miles MR, Olsen L, Rogers A (1977) Recurrent vaginal candidiasis. Importance of an intestinal reservoir. JAMA 238:1836–1837
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This work was supported by the Traditional Chinese Medicine Foundation of Zhejiang Province, China (no. 2011ZA064).
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Zheng, NN., Guo, XC., Lv, W. et al. Characterization of the vaginal fungal flora in pregnant diabetic women by 18S rRNA sequencing. Eur J Clin Microbiol Infect Dis 32, 1031–1040 (2013). https://doi.org/10.1007/s10096-013-1847-3
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DOI: https://doi.org/10.1007/s10096-013-1847-3