JOURNAL OF CLINICAL MICROBIOLOGY, Sept. 2006, p. 3213–3217
Copyright © 2006, American Society for Microbiology. All Rights Reserved.
Vol. 44, No. 9
Genital Candida Species Detected in Samples from Women in Melbourne,
Australia, before and after Treatment with Antibiotics
Marie V. Pirotta1* and Suzanne M. Garland2,3
Department of General Practice1and Department of Obstetrics and Gynaecology,2University of Melbourne, Carlton, and
Department of Microbiology and Infectious Diseases, Royal Women’s Hospital, Melbourne,3Victoria, Australia
Received 31 January 2006/Returned for modification 27 February 2006/Accepted 14 June 2006
Vulvovaginal candidiasis (VVC) remains a common cause of morbidity, with three-quarters of women
affected during their lifetimes. Use of antibiotics is an acknowledged trigger for VVC, which adversely affects
women’s physical and emotional health. Knowledge of patterns of genital Candida species-level identification
is important for management, as Candida species other than Candida albicans often fail first-line treatment. A
community sample of women with no vaginal symptoms, and who were prescribed antibiotics, was recruited
into this study, where the incidence of genital colonization by various Candida species was documented, as well
as symptoms of VVC plus relevant associations, before and after treatment with antibiotics. Self-collected low
vaginal swabs were taken prior to and 8 days after completion of antibiotic treatment, and data on various
potential risk factors for VVC were collected simultaneously, with complete data being available for 233
participants. Baseline Candida species colonization was present in 21% of women (95% confidence intervals
[CI], 17% to 27%), rising to 37% (95% CI, 31% to 44%) after antibiotic treatment. The primary species detected
for either period was C. albicans (73%), with Candida glabrata detected in around 20%. Self-assessed proneness
to VVC after antibiotic treatment and baseline colonization with Candida spp. were significantly associated
with symptomatic VVC after antibiotic treatment. For microbiologically proven candidiasis, VVC symptoms
had a sensitivity of 57% and a specificity of 91%. When physicians prescribe antibiotics, the history of risk of
VVC is one issue that physicians should discuss with women, particularly those who are self-identified as being
prone to VVC. Furthermore, we recommend that definitive microbiological diagnoses be made for women with
recurrent symptoms or those failing initial treatment, to guide appropriate therapy.
Epidemiology. Vulvovaginal candidiasis (VVC) is a common
problem for women and may affect their physical and emo-
tional health, as well as relationships with their partners (6).
Lifetime prevalence figures for VVC are around 70%; this
number may be inaccurate, as many studies are based on pa-
tient self-reporting, without microbiological confirmation (18).
Prevalence studies of genital tract colonization (asymptom-
atic) by Candida species with microbiological evidence are
difficult to compare, as many studies examine tertiary hospital
populations and may include or target only those with vaginitis
symptoms. Worldwide estimates of rates of genital Candida
colonization range from 17% in Turkey to up to 30% in a U.S.
study of asymptomatic young women followed over 12 months
(2, 3, 7, 11, 13, 17, 20).
Knowledge of patterns of genital Candida species-level iden-
tification for VVC is important for clinicians, as Candida spe-
cies other than Candida albicans often fail first-line treatment.
Despite fears that the advent of over-the-counter antifungal
agents would encourage the emergence of relatively resistant
non-C. albicans Candida species, the dominant Candida spe-
cies in the United Kingdom remains Candida albicans, with
non-C. albicans Candida species staying at a level of approxi-
mately 5% over the past decade (20). The proportion of genital
C. albicans in symptomatic women ranges from approximately
90% in U.S. and Australian samples (11, 13) to approximately
65% in Belgium (2), Turkey (7), and Saudi Arabia (1).
Candida and antibiotics. Previous work has identified VVC
after antibiotic treatment as a concern for many women,
which may affect their compliance with prescribed antibiotic
treatments (14). However, in a comprehensive literature
review, using a combination of “candida,” “vagina,” “epide-
miology,” and/or “Candida spp.” as search terms in Decem-
ber 2005, we found only one prospective community-based
study that examined the incidence of VVC after antibiotic
treatment. In that study of 74 women who took a variety of
antibiotics for nongenital infections, the incidence of vulvo-
vaginitis after antibiotic use was 32% (95% confidence in-
tervals [CI], 22% to 44%) (5).
We previously undertook a randomized placebo-controlled
factorial trial, to test whether the popular probiotic Lactoba-
cillus acidophilus was effective in the prevention of vulvovagi-
nitis after antibiotic use (16). As the intervention was not
effective, and there was no difference in outcome between the
oral and vaginal probiotic groups, trial data have been exam-
ined post hoc. We describe the incidence of genital Candida
spp. present before and after antibiotic treatment, and associ-
ations with Candida colonization as well as VVC after antibi-
otic treatment, in a community sample of women.
MATERIALS AND METHODS
Participants. The sample was recruited largely through a wide network of
family physicians in Melbourne, Australia (15). Women aged 18 to 50 years, with
a nongynecological infection requiring short-term oral antibiotic treatment, were
recruited just prior to or within 48 h of commencement of antibiotic treatment.
* Corresponding author. Mailing address: Department of General
Practice, University of Melbourne, 200 Berkeley Street, Carlton, Victoria
3053, Australia. Phone: 61 3 8344 9723. Fax: 61 3 9347 6136. E-mail:
The study received ethics approval from the Royal Australian College of General
Practitioners and the Royal Women’s Hospital, Melbourne, Australia.
Design. After written and verbal instruction, women provided self-collected
low vaginal swabs at baseline and after antibiotic use. Post-antibiotic treatment
specimens were generally collected 8 days after the end of antibiotic treatment or
at the time of developing symptoms of VVC, if that occurred. Participants also
completed questionnaires at baseline and after antibiotic treatment (demo-
graphic information, self-assessed likelihood of developing vulvovaginitis after
antibiotic treatment, antimicrobial prescribed, infection indication, body mass
index, whether sexually active and sexual activity during the trial, other medical
conditions, adherence to the antibiotic regimen, any symptoms of VVC, and time
to onset of these symptoms).
One laboratory, the Royal Women’s and Children’s microbiology laboratory
based at the Royal Children’s Hospital site, managed all microbiological speci-
mens, to ensure consistency of processing and reporting. Vaginal swabs were
initially rolled onto a glass slide for microscopic examination following Gram stain-
ing. The swab was then rolled onto a half CHROMagar medium (CHROMagar,
France) (4) and incubated at 35°C for 2 days. C. albicans, Candida glabrata, and
Candida krusei were identified by the specific color of colonies on CHROMagar;
other Candida spp. were identified by use of the ID32C kit (bioMerieux) (12).
The primary outcome of the trial was symptomatic VVC: this was defined as
both participants’ report of appropriate symptoms (that is, an answer of “yes” or
“maybe” to a question about symptoms of vaginal itch and irritation, with or
without a discharge) and a post-antibiotic treatment vaginal specimen positive
for Candida spp. Participants who did not return a post-antibiotic use question-
naire or a vaginal specimen were followed up by telephone and letter, whereby
it was usually possible to attain minimal information about occurrence of VVC
symptoms. Women who recorded no symptoms of vulvovaginitis after antibiotic
use but had Candida spp. in the post-antibiotic treatment swab were contacted at
least 1 week after they completed the trial, to exclude development of symptoms
Statistical analysis. Candida colonization was measured before and after
antibiotic treatment for each woman. To account for the pairing of the test
results from each woman, McNemar’s chi-squared test was used to test for any
change in Candida colonization before and after antibiotic use. The matched
odds ratio (OR) was also calculated using the ratio of discordant pairs, when
Candida colonization differed before and after antibiotic treatment: that is, the
odds of changing from negative to positive for Candida compared to changing
from positive to negative. The concordant pairs provided no information about
the association. The odds ratio is reported with the respective 95% CI.
Risk factors for VVC by culture results were summarized as frequencies and
percentages. Associations between symptoms of VVC and culture results were
examined using Pearson’s chi-squared statistic.
Logistic regression was used to examine association with potential risk factors
of the two main binary outcomes, Candida colonization at baseline and vulvo-
vaginitis after antibiotic treatment. Vulvovaginitis after antibiotic treatment was
defined as women who had Candida colonization and reported typical symptoms
after antibiotic use. Multivariable logistic regression was used to adjust for
possible confounders. Risk factors that showed weak evidence of association
(P ? 0.1) were left in a multivariable model. For the first outcome, Candida
colonization, none of the risk factors were found to be statistically significant in
the multivariable logistic model and hence we have only reported the unadjusted
ORs. Associations were reported as OR with respective 95% CI and P values. All
reported P values are two-sided. Participants who withdrew and did not provide
outcome data were excluded from the analysis, which was performed using
STATA version 8.
Sample characteristics and participant flow have been de-
scribed previously (16). Complete data are presented for 272
participants at baseline and 233 women after antibiotic treat-
ment. In addition, post-antibiotic treatment symptom data
are available for 257 participants. Most women (96%) self-
reported good compliance (“took most or all”) with prescribed
antibiotics. Moreover, only six women (2%) were recruited
more than 24 h after commencing their antibiotic treatments.
All vaginal specimens were processed in the study laboratory,
except for three specimens sent to external laboratories.
Candida species. At baseline, 21% (59/275; 95% CI, 17% to
27%) of the asymptomatic women were colonized with Can-
dida spp. Of these, C. albicans was the primary species in 43
(73%), 12 (20%) had C. glabrata (one of whose specimens also
grew C. albicans), three (5%) had Candida parapsilosis (from
one of whose specimens Rhodotorula mucilaginosa was also
cultured), and Candida fomata was cultured from one woman’s
Table 1 shows results of Candida growth from baseline and
post-antibiotic treatment specimens for women who supplied
both (n ? 233). Approximately 2 weeks after baseline and 8
days after completing a course of antibiotics, 37% (86/233;
95% CI, 31% to 44%) of women had specimens culture posi-
tive for a Candida species. In 63 women (73%), the main
growth was C. albicans, while in 18 women (21%) C. glabrata
was predominant. The odds ratio of a positive result for Can-
dida after antibiotic treatment, if the baseline test was negative,
was 5.5 (CI, 2.6 to 13.5; P ? 0.001), compared to having an
initial positive result followed by a negative one.
TABLE 1. Candida cultured at baseline and in
post-antibiotic treatment swabs
Type of result
for Candida for
No. of baseline swabs
(% of total swabs) with
result for Candida
Total50 (21) 183 (79)233
aBaseline swabs positive for Candida included 36 for C. albicans, 11 for C.
glabrata, and 3 for C. parapsilosis.
bPost-antibiotic treatment swabs positive for Candida included 63 for C.
albicans, 18 for C. glabrata, 1 for C. parapsilosis, and 4 for other species.
TABLE 2. Risk factors for vulvovaginal candidiasis in women colonized and not colonized with Candida species at baseline (n ? 272)
No. (%) colonized with
Candida spp. (n ? 58a)
No. (%) not colonized with
Candida spp. (n ? 214a)
ratio (95% CI)
Using estrogen-based contraception
Current sexual relationship
Regular yogurt consumption
aSome missing data.
bBMI, body mass index.
cAnswered “half the time,” “often,” or “always” to the question “How often would you estimate you get thrush when taking antibiotics?”
3214PIROTTA AND GARLANDJ. CLIN. MICROBIOL.
Association of possible risk factors for VVC and Candida
colonization at baseline. Table 2 shows associations between
possible risk factors for VVC and Candida species colonization
at baseline. Only self-reported proneness to developing VVC
after antibiotic use was associated with baseline Candida col-
onization in univariate analysis.
Association of possible risk factors for VVC and post-anti-
biotic use symptoms of vaginitis. A final report of vaginitis
symptoms was established in 257 women. Participants report-
ing no symptoms of VVC were classified as noncases. Table 3
shows characteristics of women who developed VVC after
antibiotic treatment compared with those who did not. Can-
dida spp. in a preintervention swab (OR, 5.79; CI, 2.99 to
11.18) and self-assessed proneness to vulvovaginitis after anti-
biotic use (OR, 3.11; CI, 1.63 to 5.94) were the only charac-
teristics to be significantly associated with the development of
vulvovaginitis after antibiotic use in univariate analysis. More-
over, after adjustment for possible confounders, these two fac-
tors remained strong predictors of vulvovaginitis after antibi-
otic use. There was no evidence of an interaction between
baseline Candida colonization and self-assessed proneness to
vulvovaginitis after antibiotic use.
The antibiotics taken by study participants were grouped
into narrow-, moderate-, or broad-spectrum drugs, according
to Australian antibiotic guidelines (19). There were no statis-
tically significant differences in development of VVC after
antibiotic treatment by antibiotic group in univariate analysis.
Of women taking the most frequently prescribed antibiotic,
amoxicillin (n ? 80), 18% (14 women) developed VVC com-
pared to 21% of those taking any other antibiotic (OR, 0.81;
95% CI, 0.38 to 1.65). Fewer participants used other antibiot-
ics: the second most common group was cephalexin (n ? 28).
Compared to narrow-spectrum antimicrobials, women taking
broad-spectrum antibiotics had an OR of 1.24 (95% CI, 0.55 to
2.78) for VVC; compared to those taking moderate-spectrum
antimicrobials, the OR was 0.79 (95% CI, 0.36 to 1.7) using
Table 4 shows women’s report of vulvovaginitis symptoms
and results for post-antibiotic treatment swabs. Overall, 23%
(55/235; 95% CI, 18% to 29%) of women developed vulvovag-
initis with a post-antibiotic treatment swab culture positive for
a Candida species. Women with symptoms of vaginitis were
three to four times as likely to be culture positive as negative.
C. albicans was detected in 49 (89%) cases of VVC, with
C. glabrata accounting for a further four cases. The final two
cases’ specimens were processed at outside laboratories: one
was reported to be a Candida species other than C. albicans
and the other was not identified to species level.
Of 51 women with a baseline specimen positive for Candida
spp., 42 (82%) also had a positive swab after antibiotic treat-
ment. Of these 42 participants, 27 (53%) also had symptoms
and were therefore defined as cases of post-antibiotic treat-
ment vulvovaginitis. Of women reporting definite post-anti-
biotic treatment vulvovaginitis symptoms, 79% (48/61) had a
post-antibiotic treatment swab positive for Candida spp., whereas
28% (7/25) of women reporting possible symptoms had a Can-
dida species in such specimens.
Reporting of definite symptoms of vaginitis after antibiotic
use had a sensitivity of 57% and specificity of 91% for a
post-antibiotic treatment swab with Candida spp. The positive
and negative predictive values of symptoms of VVC after an-
tibiotic use for culture of Candida spp. in this study were 79%
and 78%, respectively.
Further observations (to be interpreted with caution due to
small numbers) were those of women with Candida spp. cul-
tured from baseline swabs: 56% (24/43) with C. albicans and
25% (3/12) with C. glabrata developed vulvovaginitis after an-
tibiotic use (OR, 5.1; 95% CI, 1.1 to 31.0). Of those with
Candida spp. cultured from post-antibiotic treatment swabs,
78% (49/63) of those with C. albicans and 22% (4/18) of those
with C. glabrata had VVC symptoms (OR, 12.3; CI, 3.1 to
TABLE 3. Risk factors for vulvovaginal candidiasis by postantibiotic vulvovaginitis cases and noncases (n ? 257)
No. (%) of postantibiotic
(n ? 55)
No. (%) of postantibiotic
(n ? 202a)
ratios (95% CI)
ratios (95% CI)b
Current sexual relationship
Intercourse during trial
Candida spp. cultured at baseline
Broad-spectrum antibiotic use
Regular yogurt consumption
aOmits participants who provided outcome data inadequate for ascertaining case status.
bCalculated using multivariable logistic regression.
cBMI, body mass index.
dAnswered “half the time,” “often,” or “always” to the question “How often would you estimate you get thrush when taking antibiotics?”
TABLE 4. Symptoms of vulvovaginal candidiasis and
postantibiotic culture results (n ? 228)a
No. (%) of
for Candida spp.
No. (%) of
for Candida spp.
aMissing data: three women reported definite symptoms but used treatment
before obtaining a specimen; four did not provide post-antibiotic treatment
specimens but reported symptoms of VVC on follow-up.
bThree in this group reported symptoms after the conclusion of the trial.
cUsing Pearson’s chi-squared statistic.
VOL. 44, 2006GENITAL CANDIDA SPP. BEFORE AND AFTER ANTIBIOTIC USE 3215
57.2). No other detected Candida spp. were implicated in vul-
vovaginitis after antibiotic treatment.
Figure 1 demonstrates the time to onset of post-antibiotic
treatment vulvovaginitis symptoms, which was a median of 5.3
days (interquartile range, 3.0 to 7.0 days) from enrollment into
the study for those with proven vulvovaginitis after antibiotic
use and a median of 5.1 days for those with suggestive symp-
toms but no candidal growth.
We report the results for Candida colonization and VVC
after antibiotic treatment of a prospective community sample
taking antibiotics for nongenital infections. At baseline, 21% of
asymptomatic women aged 18 to 50 years had Candida spp.
cultured from a self-collected vaginal swab; this figure reached
37% after antibiotic treatment, with 20% of women symptom-
atic for VVC. C. albicans was the dominant species (nearly
three-quarters of both pre- and post-antibiotic treatment
swabs) as described in other studies. Adjusted self-reported
proneness to vulvovaginitis after antibiotic use and Candida
colonization at baseline predicted later symptomatic vulvovag-
inal candidiasis after antibiotic use, whereas use of estrogen-
based contraception and recent sexual activity did not.
Our results should be generalizable to other primary care
populations, as recruitment was across a large city, covered a
wide range of sociodemographic areas, and was done through
primary care clinics.
It is difficult to compare our findings of asymptomatic colo-
nization by Candida spp., as most other studies have been in
selected populations, often those with gynecological problems.
Our findings of 21% Candida colonization (95% CI, 17% to
27%) in otherwise asymptomatic women at baseline lie within
the range of incidences reported from other countries.
The incidence of vulvovaginitis after antibiotic treatment in
our series of 23% (55/235; 95% CI, 18% to 29%) is in the lower
range of the value from the only comparable prospective com-
munity study, 32.4% (95% CI, 22% to 44%) (5). This sample
was also drawn from a primary care setting and had the ad-
vantage of women being examined at the time of recruitment
but was a much smaller sample size (n ? 74) and the average
length of antibiotic courses was longer, 9 days. In that study,
Candida colonization at baseline was not predictive of vulvo-
vaginitis after antibiotic treatment (risk ratio, 0.58; CI, 0.25 to
1.37). However, a further study in a pregnant population found
a lower rate of VVC after antibiotic treatment at 6% (7/115;
95% CI, 2% to 12%), but with a risk ratio of 3.3 (CI, 1.68 to
6.49) if an initial swab was positive for Candida spp. (10).
Another interesting finding of our study was that C. albicans
at baseline was more likely to be associated with VVC after
antibiotic treatment than other species were, suggesting greater
potential for clinical disease. However, C. glabrata accounted
for at least 7% of VVC cases. Therefore, it is important that
clinicians make a definitive diagnosis for candidiasis and that
microbiology laboratories culturing Candida identify organ-
isms to species level, for those women with recurrent symp-
toms or those failing initial treatment, so that appropriate
antifungal medications are prescribed. The results also confirm
previous work reporting that symptoms of VVC are not accu-
rate predictors of Candida presence (3).
The implications for practice of this study are that women’s
self-reporting of proneness to vulvovaginitis after antibiotic
treatment is a good predictor of the condition. In the absence
of evidence to guide management of these women, one ap-
proach may be to consider antifungal chemoprophylaxis when
antibiotics are to be prescribed for them.
This project was funded by a Quality Use of Medicine Scholarship
funded by the Australian Commonwealth Department of Health and
Aging, the Shepherd Foundation, the Royal Australian College of
General Practitioners, Nutrition Care, Institut Rosell, Health Care
Network, and Sean Howard.
Sincere thanks go to Patty Chondros for statistical assistance and to
all the women and doctors who took part in the study, as well as all
microbiology laboratory staff who processed the clinical samples.
1. Al-Hedaithy, S. 2002. Spectrum and proteinase production of yeasts causing
vaginitis in Saudi Arabian women. Med. Sci. Monit. 8:498–501.
2. Bauters, T. G., M. A. Dhont, M. I. Temmerman, and H. J. Nelis. 2002.
Prevalence of vulvovaginal candidiasis and susceptibility to fluconazole in
women. Am. J. Obstet. Gynecol. 187:569–574.
3. Beigi, R., L. Meyn, D. Moore, M. Krohn, and S. Hillier. 2004. Vaginal yeast
colonization in non-pregnant women: a longitudinal study. Obstet. Gynecol.
4. Bernal, S., E. Mazuelos, M. Garcia, A. Aller, M. Martinez, and M. Gutierrez.
1996. Evaluation of CHROMagar Candida medium for the isolation of
presumptive identification of species of Candida of clinical importance.
Diagn. Microbiol. Infect. Dis. 24:201–204.
5. Bluestein, D., C. Rutledge, and L. Lumsden. 1991. Predicting the occurrence
of antibiotic-induced candidal vaginitis (AICV). Fam. Pract. Res. J. 11:319–
6. Chapple, A., K. Hassell, M. Nicolson, and J. Cantrill. 2000. ‘You don’t really
feel you can function normally’: women’s perceptions and personal manage-
ment of vaginal thrush. J. Reprod. Infant Psychol. 18:309–319.
7. Erdem, H., M. Cetin, T. Timuroglu, A. Cetin, O. Yanar, and A. Pahsa. 2003.
Identification of yeasts in public hospital primary care patients with and
without clinical vaginitis. ANZJOG 434:312–316.
8. Reference deleted.
9. Reference deleted.
10. Glover, D. D., and B. Larsen. 1998. Longitudinal investigation of candida
vaginitis in pregnancy: role of superimposed antibiotic use. Obstet. Gynecol.
11. Holland, J., M. L. Young, O. Lee, and S. Chen. 2003. Vulvovaginal carriage
of yeasts other than Candida albicans. Sex. Transm. Infect. 79:249–250.
12. Hospenthal, D., C. Murray, M. Beckius, J. Green, and D. Dooley. 2002.
FIG. 1. Cumulative percentage of cases of post-antibiotic treat-
ment vulvovaginitis symptoms by days from enrollment into the study
(n ? 55).
3216PIROTTA AND GARLANDJ. CLIN. MICROBIOL.
Persistence of pigment production by yeast isolates grown on CHROMagar
Candida medium. J. Clin. Microbiol. 40:4768–4770.
13. Mathema, B., E. Cross, E. Dun, S. Park, J. Bedell, B. Slade, M. Williams, L.
Riley, V. Chaturvedi, and D. S. Perlin. 2001. Prevalence of vaginal coloni-
zation by drug-resistant Candida species in college-age women with previous
exposure to over-the-counter azole antifungals. Clin. Infect. Dis. 33:E23–
14. Pirotta, M., J. Gunn, and P. Chondros. 2003. “Not thrush again!” Women’s
experience of post-antibiotic vulvovaginitis. Med. J. Aust. 179:43–46.
15. Pirotta, M., J. Gunn, P. Chondros, S. Grover, S. Hurley, and S. Garland.
2004. Study protocol. The PAV trial: does lactobacillus prevent post-anti-
biotic vulvovaginal candidiasis? Protocol of a randomised controlled trial
[ISRCTN24141277]. BMC Fam. Pract. 5:5.
16. Pirotta, M., J. Gunn, P. Chondros, S. Grover, P. O’Malley, S. Hurley, and S.
Garland. 2004. Effect of lactobacillus in preventing post-antibiotic vulvovag-
inal candidiasis: a randomised controlled trial. BMJ 329:548–550.
17. Ribeiro, M. A., R. Dietze, C. R. Paula, D. A. Da Matta, and A. L. Colombo.
2001. Susceptibility profile of vaginal yeast isolates from Brazil. Mycopatho-
18. Sobel, J. D., S. Faro, R. W. Force, B. Foxman, W. J. Ledger, P. R. Nyirjesy,
B. D. Reed, and P. R. Summers. 1998. Vulvovaginal candidiasis: epidemio-
logic, diagnostic, and therapeutic considerations. Am. J. Obstet. Gynecol.
19. Therapeutic Guidelines. 2003. Therapeutic guidelines antibiotics, 12th ed.
Therapeutic Guidelines, Melbourne, Australia.
20. Walker, P. P., M. T. Reynolds, H. R. Ashbee, C. Brown, and E. G. Evans.
2000. Vaginal yeasts in the era of “over the counter” antifungals. Sex.
Transm. Infect. 76:437–438.
VOL. 44, 2006GENITAL CANDIDA SPP. BEFORE AND AFTER ANTIBIOTIC USE3217