Jpn. J. Infect. Dis., 54, 1031107, 2001
Original Article
lncreased Incidence of Vulvovaglnal Candidiasis Caused
by Candida glabrata in Jordan
Khaled H. Abu-Elteen*
Department of Biological Sciences, Faculo, of Science, Hashemite University,
PO.Box 330077- Zarqa 13133, Jordan
(Received May 28, 2001. Accepted July 16, 2001)
SUMMARY: Due to the rislng Importance Of Candida glabrata and other non-albicans Candida as prlnCiple
human opportunistic pathogens, 356 Women with abnormal vaglnal discharge who attended a prlVate Obstetrics
and gynecology clinic in Amman, Jordan, between January 1 999 and February 2001 were examined･ The isolation
rate of Candida spp･ from high-vaglnal swabs was 44･9%･ CHROMagar Candida and conventional mycologlCal
methods identified six isolated Candida spp., including C. albicans, C. glabrata, C. tropicalis, C･ parapsilosis,
C･ krusei, and C･ kefyr･ The percentages of C･ albicans, C･ glabrat.a, and C･ tropicalis isolates were 43･1%,
32･5%, and 8･ 1%, respectively･ C･ albicans was isolated in combinatlOn With C･ tropicalis and C･ krusei in two
patients･ Statistical analysts Of the present results clearly show an increase in the incidence of vulvovaglnal
candidiasis caused by C. glabrata in the two study periods, 199411996 and 1999-2001 (P- 0･0186)･ In contrast,
Comparlng the proportions of vulvovaglnal candidiasis caused by C･ albicans in the two periods, there was no
slgnificant difference･ These results may have slgniflCant Clinical implications, as C･ glabrata are innately less
susceptible to most antifungal agents than C･ albicans; these findings support viewing this organism as a major
pathogen.
fluconazole (15-18).
INTRODUCT10N
Several studies have suggested that血e increased丘equency
ofvulvovaglnal candidiasis is caused by non-albicans Candida
Vaginal candidiasis is a widespread, Common disease
affecting a substantial proportion of women of childbearlng
spp･ (19-21)･ One such study demonstrated that the propor-
age ( 1 )A The pathogenFsis of this frequent clinical problem,
tion Ofvulvovaglnal candidiasis cases caused by non-albicans
however, remains elusIVe, and its incidence can be expected
Candida spp. rose from 9.9% in 1988 to 17･2% in 1995 (20)I
to continue rislng, aS risk factors are not diminishing. While
Evidence regarding the selectivity of these species, especially
approximately 75% of women experience a slngle episode of
C･ glabrata, comes from HIV-seropositive women receivlng
fluconazole (4); the yaginalflora in w?men receiving
Candida vaglnitis in their lifetime, a slgni丘cant percentage of
women (5-7%) experience recurrent infection (2-4)･ Candida
albicans is responsible for 80194% of vulvovaglnal candidi-
fluconazole shifts to an lnCreaSe in absolute Isolation rates of
C. glabrata, but with low attack rates of clinical vaginitis (22)･
asis (5), the remaining cases being due to other Candida spp･
A number of investlgatOrS have emphasized the role of
such as C. glabrata, C. tropicalis, C. parapsilosis, C. krusei,
species other than C. albicans as emergent pathogens in
and C. keji,r (5). In recent years, the incidence in the human
population of infection with human immunodeficiency virus
urinary tract candidal infection (23 ,24). A dramatic increase
in the carriage Of C. glabrata has also been demonstrated in
(HIV), organ transplantation, Widespread and increased use
dentate individuals over 80 years of age; the proportion of
of immunosuppressive therapy together with broad-spectrum
individuals with dentures carrylng C. glabrata in one study
antimycotic therapy have血amatically increased the incidence
was greater than 50% (25). Because of differences in their
of candidiasis caused by C. glabrata and other non-albicans
Candida spp. (6- 10). C. glabrata represents the second-most
common Candida spp. causing bloodstream infection (7,9, 1 1 ).
&equency and distribution of Candida spp･ are of great inter-
susceptibility agalnSt Certain ant血ngal dmgs, changes in the
est. We, therefore, felt that it would be ofvalue to assess the
It accounts fわr 8% of all cases of candidemia involving
frequency of isolation of various Candida spp･from Jordanian
patients with cancer (12), 13% of cases involving non-
women with abnormal vaginal discharge during the period of
neワtrOPenic patients (13,14), and 1 1% of cases involving
1 999-200 1 and to compare these results with those obtained
patlentS With candidemia (7). Nosocomial yeast infections
during the period 1994-1996･
caused by C. glabrata have increased substantially, while yeast
infections caused by C. albicans have decreased according
MATERIALS AND METHODS
to a Universlty OHowa Hospltals and Clinics study between
the years 1987-1988 and 1993-1994 (9). Moreover, Wingard
Study subjects: High-vaglnal swabs were collected from
et al. (15) noted an increase in colonization with C･ glabrata
356 women (aged between 1 8-52) attending obstetrics and
among bone-marrow transplant recIPlentS glVenfluconazole
gynecology clinics in Amman, Jordan with variable degrees
of abnormal vaglnal discharge between January 1999 and
February 2001. After slgnlng an informed consent to carry
as an antifungal prophylactic drug. Furthermore, C･ glabrata
accounts for 75% offungemia cases among patients receivlng
out the procedure, each patient completed a questionnaire
about age, work, use of contraceptlVeS, history of pelvic
*Co汀eSpOnding author: Fax:+962-6-4 1 28772, E-mail: Salma@
inflammatory disease, history of diabetes, and theuse of topical
hu. edu.j o
loョ
antifungal agents and/or antibiotics. The gynecologlCal history
most frequent associations of the vulvovaglnal symptoms
and examination of subjects, noted vulvovaglnal symptoms
were leuko汀hea (36.6%), buming sensation (25.3%), and
(leukorrhea, buming sensation, itching, dysuria, dyspareu-
dysuria (I 9.7%), as presented in Table 3･ The Table also shows
nia), and the type (mucous, creamy, lumpy, foamy), as yell
that the percentages of patients manifesting one, two, or three
as the presence or absence of odor of the vaglnal secretlOnS
symptoms ofvulvovaglnitis were 21 ･3%, 27･8%, and 25･2%,
were also reported.
respectively. Bumlng Sensation and leuko汀hea were the
Isolation and identification of Candida spp.: A sample
of vaginal material (posteriPr fomiX) was obtained with the
aid of a sterile plain cotton-tlpped swab and was immediately
Table 1. Prcvalcncc ofvulvovaglnalinfcctions among women
inoculated into Sabouraud dextrose broth (Difco, Detroit,
according to age
Mich., USA) Containing 50 mgL t ofchloramphenicol. Tubes
Age (years) No. cxamincd No. infcctcd % infbctcd
were incubated at 300C fわr up to 48 h, and were then cultured
lヽJ ltJ I 1
≦19 68
2 5 5 42 0 6 L
1 tJ 7 4
1 0 0 0
into Sabouraud Dextrose agar (SDA) and CHROM a甲r (CA)
20-29 65
(CHROM agar, Paris, France). Following inoculatlOn, the
30-40 1 25
culture plates were incubated in air at 300C and were inspected
≧41 98
daily fわr a total or 7 days. All yeast isolates observed on CA
Tbta1 3 56
were identified by colony morphology and pigmentation
according to the manufacturer's instructions and as has been
previously described (26). Isolates from CA and SDA plates
Table 2. Proportion ofvulvovaglnal candidiasis caused by diffcrcnt
were identified according to their morphologleS On COmmeal
Candida spp. during 1994-1996 and I999- 2001
agar (CMA), their formation of germ tube in serum, and, for
Number of culture-positive (%)
isolates that were chlamydospore negative and/or gem-tube
CandL-da spp.
1994-I 996 1 999-2001
negative, the results of conventional biochemical and assimila-
tion tests camied out according to established procedures (27).
Candida albicans
40 (51.3) 69 (43.1)
ln cases where identification was ambiguous, the Apt 20C
Candt'da glabrata
14 (17.9) 52 (32.5)
system (bioMerieux SA, Lyon, France) was employed.
Candida lropicalis
10(12.8) 13 (8.I)
Statistical analysis: The slgnificance of differences in
prevalence rates was evaluated using 2 X 2 contingency tables
with the chi-square test; values ofP < 0.05 Were considered
statistically slgnificant.
Candida parapsilosis
2 (2.6) 6 (3.8)
CandL'da kruseL'
5 (6.4) 1 1 (6.9)
Candida kqbr
5 (6.4) 9 (5.6)
Candida guilliermondii
2 (2.6) ND
Tbta1 78
(100) 160
(100)
ND- Not detect()d
RES UIXS
A total of 356 Women with variable degrees of abnomal
Table 3. Association of symptoms observed in positive cases of
vaglnal discharge were examined between January 1 999 and
February 2001･ Ofthese, 160 women (44･9%) were y?ast-
yeast infections
culture positive. The prevalence of vulvovaglnal infectlOnS
No. of symptoms claimed
in the 30-40 years age group was 56.8%, followed by
by the patients
patients of the 20-29 ye?rs age group (50･8%) (Table 1)･ The
Asymptom ati c
prevalence of vulvovaglnal infections at ≧40 and ≦ 1 9 years
One
symptom
was 4 1.8% and 22. 1 %, respectively. Based on statistical analysts
of the results, a slgnificant difference between age groups
S
ymptoms
D
Pcrc
4 0 3 7 5 2 L 3 2 4 6 3 L 2 4 3 2 4 3
cn
ta苦c
2 7 8 4 2 6 9 4 ｣ 2 ｣ 2 4 6 2 4
Dys
30-40 and ≦19 and age groups 30-40 and ≧40 in the number
L
of vulvovaginal infections (P - 0.000 and 0.0266, respec-
a
tively) was established. Furthermore, there was no significant
difference between age groups 30-40 and 20-29 in the number
Two symptoms
1-D
1-Dys
ofvulvovaginal infections (P - 0.43).
Distribution of Candida spp.: Using the manufacturer's
トB
L-D
guidelines fわr CA Candida and published criteria by Odds
L-Dys
and Bemaerts (26), We were able to identify the following
L-I
species: C. albicans, C. glabrata, C. tropicalis, C. krusei, and
a-L
C. parapsilosis on the basis of colony color. However, there
D-B
was no difference in the sensitivityofCA and SDA. There was
a lOO% correlation between CA and the Apt test for identiflCation of C. albicans, C. tropicalis, and C. krusei, and 88% for
Three symptoms
D-I-Dys
LD-Dys
L-D-a
identification of C. glabrata and C. parapsilosis (confirmed
by Apt test)･ A single-ye.a.st species was cultured from 160
L-Dys-1
patients in the culture-posltlVe population. C. albicans was the
L_1-B
most frequent isolate, accountlng for 43. 1% of all isolates,
while C. glabrata and C. tropicalis accounted for 32.5% and
B-D-Dys
L-D-1
B-D-I
8･ 1% of isolates, respectively (Table 2)･ Furtherヮore, C･
Four symptoms
albicans was isolated in combination with C. krusel and C
1-良-D-L
10.5
The data reprcsentthe percentage of total positive cases observed
tropicalis in two cases.
in the infected women. B: bunllng Sensation, D: dysuria, Dys:
Symptoms associatedwith vulvovaginal infections: The
dyspareunia, I: itching, L: leuko汀hea.
104
others (26,32), who felt that further Tethods were required
symptoms most frequently complained of by the patients
for confirmation of C. glabrata identlty･
C. albicans was isolatedfrom 43. 1 % of the culture-positive
during the clinical examination; they accounted fわr 23%
of symptoms, followed by itching and leukorrhea (17･6%)･
Asymptomatic cases and cases with more than three symp-
patients, followed by C. glabrata 32.5%, and C･ tropicalis
toms accounted fわr 15.2% and 10.5%, respectively, of all
8. 1 % patients; these results are consistent with仇ose presented
patients (Table 3).
Trends invulvovaginal infections caused by yeast species:
previousy (29). The high isolation rate of C･ glabrata from
high-vaginal swab specimens has been reported by others
Table 2 shows the frequency distribution of Candida spp･ ln
(7,8,10,20,34). In fact, depending on the site of infection, C.
yeast-positive patients during two study periods ( 1 994- 1996
glabrata is often the second or third most common cause of
and 1999-2001); C. albicans was the most common species
candidiasis after C･ albicans (7)･ Howeyer, more recent
among the isolates identified to the species level during the
epidemiologlCal studies showed a mycologlCal shift from C･
albicans to non-albicans Candida spp. such as C. glabrata,
C. tropicalis, C. parapsilosis and C. krusei (6,9, I 5, 1 7,20,35)･
two study periods. Overall, the proportion ofvulvovaglnal yeast
infections caused by C. albicans decreased from 5113% in
1994-1996 to 43.1% in 1999-2001. ln contrast, the occurrence
of C. glabrata was found to increase from 17･9% in 19941996 to 32.5% in 1999-2001. Statistical analyses indicated
Spinillo et al. (20) showed that the proportion of vulvovaginal
candidiasis cases caused by non-albicans Candida spp. rose
from 9.9% in 1988 to 17.2% in 1995. All of these studies
that in the period 1994-1996 there was a statistically slgnifi-
have found that C. glabrata has risen in incidence, and
cant difference between the proportion of vulvovaglnal
researchers have suggested that the use of nuconazole may
candidiasis caused by C. albicans and by C･ glabrata (P -
have contributed to the increase in the isolation of C glabrata
and the decrease in C. albicans isolation. Vazquez et al. (34)
0.000). Furthermore, there was no significant difference
reported that within 6 months of initiation offluconazole
between C. albicans and C. glabrata during the 1999-2001
study period (P - 0.05). On the other hand, the proportions
of vulvovaglnal candidiasis caused by C. albicans during
prophylaxis, the isolation of C. albicans decreased by 60%,
while the isolation of C. glabrata was >70% higher in
the t.wo study periods (1994-1996 and 1999-2001) showed
patients asslgnedfluconazole than in those asslgned placebo･
no slgnificant difference. There was a significant difference;
These results are similar to those reported by other investlga-
however, in the proportions of vulvovaglnal candidiasis
tors (4,9,24). C. glabrata is of special importance because of
caused by C･ glabrata in the twp study periods (P - 0101 86),
its imate resistance to antifungal agents, specifically to azoles
indicatlng a marked increase ln Vulvovaglnal candidiasis
(3,7-9,36,37). The specific mechanisms ofantifungal resistance
caused by C. glabrata between the periods 199411996 and
199912001. The isolation rate of C. krusei remained at
to the azole class of antifungal agents are not yetfullyunder-
approximately 6.4%; rates of C. tropicalis isolation were
have been identified: increased P-450-dependent ergosteroI
stood. In C. glabrata, several mechanisms of azole resistance
12.8% and 8.1% in the 1994-1996 and 1999-2001 periods,
synthesis and an energy-dependent emux pump offluconazole,
respectively. Other Candida spp. causlng aS follows: fewer
than 10. 1% ofall vulvovaglnal infections during the two study
r!ossibly via.a multi-azole cross-resistance (8,34)･ The statis-
periods were C. parapsilosis, 3.4%; C･ kefyr 5･9%, and C･
guilliermondii Ol 8%･
shows an increase in血e incidence ofvulvovaglnal candidiasis
tlCal analysis Of data obtained in the present study clearly
caused by C. glabrata between the periods 1994-1996 and
1999-2001, With the results agreelng Well with those of the
above-mentioned studies.
DISCUSSION
This study has also revealed that the symptoms most
During the past two decades, several investlgatOrS have
frequently complained of by the majority Of women with a
reported that the frequency of yeast infections, especially with
positive culture for yeast are leukorrhea, a burnlng Sensa-
the Candida spp., has increased dramatically (9, 1 0,29)･ This
tion, itching, and dysuria. Willmott (38) found that symptoms,
increase has been accompanied by an increase in the number
particularly vaglnal irritation, Were reported by over half of
of Candida spp. recognized to cause disease (6,7,10,16,23)･
patients having yeast-containlng Vaglnal cultures･ Geiger et
In this study, yeast was recovered from 160 (44.9%) of the
al. (39) showed that abnomal discharge was less丘equent in
356 patients with variable degrees of abnormal vaglnal
women with symptomatic vaglnitis due to C. glabrata than to
discharge. These flndings agree with the observations reported
C. albicans, which may reflect the effects ofa lack ofhypha
by other investlgatOrS that yeast can be recovered in the range
fomation by the C. glabrata blastoconidia (8, 1 0)･ Vaginitis
of5-53.3% in healthy women (29,30). The highest infection
due to C. glabrata was reported to be the main indolent
rate (56･8%) was detected among woヤen in the 30-40 age
with reduced inflammation and hence less dyspareunia (39).
group, which represents the most actlVe Sexual age･ The
Moreover, patients with C. glabrata vaglnitis frequently
incidence of vulvovaglnal yeast infections decreased in older
reported a buming sensation rather than itching (2,8,39)･
age groTps (1,5)･
ConsIStent With previous findings (26,3 1 -33), there was
glabrata vaglnitis has increased from 17･9% in 1994-1996 to
The results presented indicate that the frequency of C･
no difference in the sensitivlty Of CA and SDA･ We were
32.5% in 1 999-2001. The described increase in the occu汀enCe
able to identifyto the species level 100% of the isolates of C.
of C･ glabrata and other non-albicans Candida spp･ occurred
albicans, C. hlOPicalis,and C. kT7iSei on CA, which confirms the
results of other studies (26,3 1 -33). Isolates of C. glabrata, the
lactic agents f♭r use by patients with vulvovaglnal candidiasis･
some years after the introduction offluconazole as a prophyl
second-most common yeast isolated in our suⅣey, presented
more difficulties. Dark pink-purple colonies with a pale edge
ACKNOWLEDGMENTS
were usually C. glabrata, but 12% (confirmed by API 20C)
did not present enough constant definitive colonial features
The technical assistance provided by Mr. M. Ghaleb is
on CA. The results of this study confirmthe difficulties with
greatly appreciated. I would like to thank Dr･ Ali Z･ Elkami
C. glabrata identification encountered with CA reported by
for critically reading the manuscrlPt･
105
This study was partially supported by the Hashemite
Agents Chemother., 37, 1 847-1849.
University Research Council.
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H. and Vartivarian, S. (1997): The epidemiology of
hematogenous candidiasis caused by different Candida
species. Clin. Infect. Dis., 24, 1 12211 128.
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