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ORIGINAL RESEARCH |
From the Division of Immunology and Infectious Diseases, Department of Obstetrics and Gynecology, Weill Medical College of Cornell University, New York, New York; the Department of Gynecology and Obstetrics, University of Campinas, São Paulo, Brazil; Hospital das Clínicas, São Paulo, Brazil; and the Federal University of Bahia, Salvador, Brazil.
Address reprint requests to: Paulo Giraldo, MD Division of Immunology and Infectious Diseases Department of Obstetrics and Gynecology Weill Medical College of Cornell University 515 East 71st Street New York, NY 10021 E-mail: switkin{at}mail.med.cornell.edu
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Abstract |
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Methods: Vaginal swabs from 50 women with a history of recurrent vulvovaginal candidiasis and 45 women with one or fewer episodes of candidal vaginaitis within the past 12 months were evaluated for Candida by wet mount/Gram stain, culture, and polymerase chain reaction (PCR). All women were asymptomatic for at least 30 days.
Results: Candida was identified in 28 women by PCR, in 14 women by culture, and in 13 women by wet mount/Gram stain. Candida was identified by PCR in a similar proportion of patients with previous recurrent vulvovaginal candidiasis (30%) and in controls (28.8%). However, Candida was identified by culture in more women with previous recurrent vulvovaginal candidiasis (22%) than in controls (6.6%, P = .04); it also was identified by wet mount/Gram stain in more women with recurrent vulvovaginal candidiasis (22%) than in controls (4.4%, P = .01). For the recurrent vulvovaginal candidiasis patients, culture and wet mount/Gram stain had a sensitivity of 66.6% compared with PCR. For the controls, the sensitivity of the two former assays relative to PCR was only 15.3%.
Conclusion: Women with a history of recurrent vulvovaginal candidiasis have more easily detectable Candida in their vagina, even when asymptomatic, than do other women. A relative inefficiency in regulating the proliferation of Candida in the vagina may increase susceptibility to periodic symptomatic recurrences.
Approximately 13 million cases of vulvovaginal candidiasis occur annually in the United States, prompting 10 million gynecologic office visits and $1 billion in direct costs.1 A significant percentage of women with vulvovaginal candidiasis will experience subsequent episodes, and 5% will develop frequent recurrent episodes. This condition is defined as clinical and laboratory evidence of three or more acute vaginal Candida infections per year and most often occurs in reproductive age sexually active women.1,2 The frequency of acute episodes of vulvovaginal candidiasis per year is variable. Some women experience recurrent vulvovaginal candidiasis as often as every month.
The significance of Candida in the vagina of asymptomatic women between episodes of recurrent vulvovaginal candidiasis is not clear. Prevalence studies indicate that 10% to 55% of healthy women who are completely asymptomatic have vaginal cultures positive for Candida albicans.3–5 The finding of this organism during the symptom-free periods could indicate previous inadequate treatment, insufficient use of antifungical medication, resistance of the organism to complete eradication by the drug, or recolonization. It has been suggested that the complete eradication of Candida from the microflora habitat of the vagina is virtually impossible at the present time.6
The prevailing view regarding the pathogenesis of recurrent vulvovaginal candidiasis is that repeated episodes are not the result of more frequent introduction of the organism into the lower genital tract or infection with a more virulent organism but, rather, differences in host susceptibility factors.7 Although 90% of recurrent vulvovaginal candidiasis patients undergoing maintenance antifungal therapy are protected from symptoms and recurrence, acute episodes reappear in nearly 50% of cases after termination of therapy.8
Unfortunately, recognizable and reversible exogenous factors influencing susceptibility to recurrent vulvovaginal candidiasis have not been identified for most patients. The majority of studies on recurrent vulvovaginal candidiasis have focused on the acute episodes, neglecting the asymptomatic periods. To compare the prevalence of vaginal Candida colonization in asymptomatic patients with and without a history of recurrent vulvovaginal candidiasis, microbiologic evaluations for Candida by wet mount/Gram stain, culture, and polymerase chain reaction (PCR) were performed.
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Materials and Methods |
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A sample of secretions from the vagina was obtained by scraping the vaginal walls with a cotton swab and immediately transferring it to two glass slides. A drop of saline solution was added to the first slide. The second slide was fixed and stained by the Gram technique. The diagnosis of Candida was based on the presence of hypha or blastoconidia in one or both slides on microscopic examination.
The pH of vaginal secretions was measured by color-pHast indicator sticks (MCLB Manufactoring Chemists Inc., Cincinnati, OH) applied directly against the lateral vaginal wall, avoiding contact with cervical mucus.
The vaginal secretions were cultured for 72 hours at 37C on Sabouraud agar. Growth was identified as C albicans by germ-tube testing and substrate assimilation using API strips (Sherwood Medical, Plainview, NY).
Vaginal wash samples were obtained by flushing 3-mL sterile saline into the vaginal cavity, scraping the vaginal walls with a cotton swab, and aspirating the liquid with a 5-mL syringe. The mixture was centrifuged and the pellets and supernatants frozen at -70C until sent to a laboratory on dry ice for testing.
The vaginal pellets were thawed and resuspended in 0.5-mL phosphate-buffered saline and digested with 1% lyticase, 1% 2-mercaptoethanol, and 10 mmol/L ethylenediaminetetra-acetic acid to remove the Candida cell wall, followed by treatment with 1% Brij 35 detergent (Sigma Chemical Co., St. Louis, MO) and 200 mg/mL proteinase K to lyse the cells and expose the DNA. Candida albicans was detected by PCR using primer pairs specific for a region of the 90-kDa heat shock protein gene.10
Fisher exact test and McNemar test were used to analyze differences in discrete variables. Findings were considered significant at P < .05.
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Results |
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). Only 14 (14.7%) of the women tested (all PCR-positive) were positive for Candida by culture, and 13 (13.6%) were positive by wet mount/Gram stain (P < .02 compared with PCR).
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With the exception of a history of recurrent vulvovaginal candidiasis, there were no differences between women positive or negative for Candida detected by any technique and social, demographic, and behavioral variables (Table 2). The increased prevalence of Candida colonization in black women did not reach statistical significance.
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). Conversely, in the control population the sensitivity of culture and wet mount/Gram stain relative to PCR was only 15.3%. Specificity and positive predictive values of culture and wet mount/Gram stain were high for both groups of subjects.
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Discussion |
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In contrast with the observations made with control subjects, in the asymptomatic women with a history of recurrent vulvovaginal candidiasis, PCR positivity was paralleled in the majority of cases with an abnormal culture and an abnormal wet mount/Gram stain. This strongly indicates that the number of organisms present during the asymptomatic carriage of Candida in these women was higher than in women without a history of recurrent vulvovaginal candidiasis.
It remains to be experimentally determined whether those asymptomatic recurrent vulvovaginal candidiasis patients with Candida colonization will have more frequent acute episodes of Candida vaginitis than asymptomatic recurrent vulvovaginal candidiasis patients who are Candida negative. These studies are in progress. On the basis of previous studies,13–15 a likely possibility is that the asymptomatic recurrent vulvovaginal candidiasis patients with vaginal Candida detected by PCR, culture, and wet mount/Gram stain are inefficient in regulating Candida proliferation because of local immunosuppressive factors. This group, therefore, may be most susceptible to the development of recurrences of clinically apparent Candida vaginal infections.
If asymptomatic Candida colonization proves to be a predisposing factor for recurrent vulvovaginal candidiasis, then studies to bolster host immune mechanisms in these women to further limit Candida proliferation in the vagina, as well as the development of more effective antibiotic protocols, are warranted.
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Footnotes |
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Received May 10, 1999. Received in revised form September 7, 1999. Accepted September 10, 1999.
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References |
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2. Sobel JD. Pathogenesis and epidemiology of vulvovaginal candidiasis. Ann N Y Acad Sci 1988;544:547–57.[Abstract]
3. Lindnen GEM, Plantema FHF, Hoogkamp-Korstanje JRA. Quantitative studies of the vaginal flora of health women and of obstetrics and gynecological women. J Med Microbiol 1978;11:233–41.[Medline]
4. Bartlett JG, Polk BF. Bacterial vaginal flora of the vagina: Quantitative study. Rev Infect Dis 1984;6:S67–72.
5. Sobel JD. Candidal vaginitis. Clin Obstet Gynecol 1993;36:153–65.[Medline]
6. Sobel JD, Faro S, Force RW, Foxman B, Ledger WJ, Nyirjesy PR, et al. Vulvovaginal candidiasis: Epidemiologic, diagnostic and therapeutic considerations. Am J Obstet Gynecol 1998;178:203–11.[Medline]
7. Witkin SS. Immunologic factors influencing susceptibility to recurrent candidal vulvovaginitis. Clin Obstet Gynecol 1991;34:662–8.[Medline]
8. Sobel JD. Recurrent vulvovaginal candidiasis: A prospective study of the efficacy of maintenance ketoconazole therapy. N Engl J Med 1986;315:1455–8.[Abstract]
9. Giraldo P, Neuer A, Korneeva IL, Ribeiro-Filho A, Simões JA, Witkin SS. Vaginal heat shock protein expression in symptom-free women with a history of recurrent vulvovaginitis. Am J Obstet Gynecol 1999;180:524–9.[Medline]
10. Crampin AC, Mathews RC. Application of the polymerase chain reaction to the diagnosis of candidosis by amplification of an HSP 90 gene fragment. J Med Microbiol 1993;39:233–8.[Abstract]
11. Ryley JF. Pathogenicity of Candida albicans with particular reference to the vagina. J Med Vet Mycol 1986;24:5–22.[Medline]
12. Odds FC. Genital candidosis. Clin Exp Dermatol 1982;7:345–54.[Medline]
13. Witkin SS, Hirsch J, Ledger WJ. A macrophage defect in women with recurrent Candida vaginitis and its reversal in vitro by prostaglandin inhibitors. Am J Obstet Gynecol 1986;155:790–5.[Medline]
14. Witkin SS, Jeremias J, Ledger WJ. A localized vaginal allergic response in women with recurrent vaginitis. J Allergy Clin Immunol 1988;81:412–6.[Medline]
15. Witkin SS, Kalo-Klein A, Galland L, Teich M, Ledge WJ. Effect of Candida albicans plus histamine on prostaglandin E2 production by peripheral blood mononuclear cells from healthy women and women with recurrent candidal vaginitis. J Infect Dis 1991;164: 396–9.[Medline]
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