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 twopatients･ 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 lesssusceptible 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 diseaseaffecting 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, especiallyapproximately 75% of women experience a slngle episode ofC･ 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 ofwomen (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 ofC. 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 ofsuch as C. glabrata, C. tropicalis, C. parapsilosis, C. krusei,

species other than C. albicans as emergent pathogens inand C. keji,r (5). In recent years, the incidence in the humanpopulation of infection with human immunodeficiency virus

urinary tract candidal infection (23 ,24). A dramatic increasein 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 ofof 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 theirof candidiasis caused by C. glabrata and other non‑albicans
Candida spp. (6‑ 10). C. glabrata represents the second‑mostcommon 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 theest. We, therefore, felt that it would be ofvalue to assess theIt accounts fわr 8% of all cases of candidemia involving

frequency of isolation of various Candida spp･from Jordanianpatients with cancer (12), 13% of cases involving non‑

women with abnormal vaginal discharge during the period ofne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 fromet al. (15) noted an increase in colonization with C･ glabrata

356 women (aged between 1 8‑52) attending obstetrics andamong bone‑marrow transplant recIPlentS glVenfluconazole

gynecology clinics in Amman, Jordan with variable degreesof abnormal vaglnal discharge between January 1999 andFebruary 2001. After slgnlng an informed consent to carryas an antifungal prophylactic drug. Furthermore, C･ glabrataaccounts 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 topicalhu. edu.j olo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 showsnia), and the type (mucous, creamy, lumpy, foamy), as yellthat 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 theaid of a sterile plain cotton‑tlpped swab and was immediately

Table 1. Prcvalcncc ofvulvovaglnalinfcctions among womeninoculated into Sabouraud dextrose broth (Difco, Detroit,according to age

Mich., USA) Containing 50 mgL t ofchloramphenicol. Tubes

Age (years)

No. cxamincd No. infcctcd

were incubated at 300C fわr up to 48 h, and were then cultured% infbctcdlヽJ ltJ I 1

≦19

68

20‑29

65

30‑40

1 25

2 5 5 42 0 6 L 1 0 0 0

1 tJ 7 4

into Sabouraud Dextrose agar (SDA) and CHROM a甲r (CA)(CHROM agar, Paris, France). Following inoculatlOn, theculture 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

were identified by colony morphology and pigmentation

3 56

according to the manufacturer's instructions and as has beenpreviously 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.

negative, the results of conventional biochemical and assimila‑

1994‑I 996

1 999‑2001

69 (43.1)

tion tests camied out according to established procedures (27).

Candida albicans

40 (51.3)

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 inprevalence 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()dRES UIXS

A total of 356 Women with variable degrees of abnomal
Table 3. Association of symptoms observed in positive cases ofvaglnal discharge were examined between January 1 999 andFebruary 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 byby the patientspatients of the 20‑29 ye?rs age group (50･8%) (Table 1)･ The

Asymptom ati cprevalence of vulvovaglnal infections at ≧40 and ≦ 1 9 years

One

symptom

was 4 1.8% and 22. 1 %, respectively. Based on statistical analystsof the results, a slgnificant difference between age groups

S

ymptomsD

Pcrc

403752L32 463L243243

cn

ta苦c

27 84 2 6 94｣2 ｣24624

Dys

30‑40 and ≦19 and age groups 30‑40 and ≧40 in the numberLof vulvovaginal infections (P ‑ 0.000 and 0.0266, respec‑atively) 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, anda‑L

C. parapsilosis on the basis of colony color. However, there

D‑B

was no difference in the sensitivityofCA and SDA. There wasa lOO% correlation between CA and the Apt test for identiflCa‑tion of C. albicans, C. tropicalis, and C. krusei, and 88% for

Three symptoms

D‑I‑Dys

LD‑Dys
L‑D‑aidentification 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 theL̲1‑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 patientsfor 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 fromhigh‑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 theepidemiologlCal 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 occurrenceof C. glabrata was found to increase from 17･9% in 1994‑
1996 to 32.5% in 1999‑2001. Statistical analyses indicatedSpinillo et al. (20) showed that the proportion of vulvovaginal

candidiasis cases caused by non‑albicans Candida spp. rosefrom 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, andcant 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 glabrataand 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 proportionsof vulvovaglnal candidiasis caused by C. albicans duringprophylaxis, the isolation of C. albicans decreased by 60%,
while the isolation of C. glabrata was >70% higher inthe t.wo study periods (1994‑1996 and 1999‑2001) showedpatients 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 resistancecaused by C. glabrata between the periods 199411996 and199912001. The isolation rate of C. krusei remained atto 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 ergosteroIstood. 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 clearlycaused by C. glabrata between the periods 1994‑1996 and1999‑2001, With the results agreelng Well with those of theabove‑mentioned studies.

DISCUSSION

This study has also revealed that the symptoms mostDuring the past two decades, several investlgatOrS havefrequently complained of by the majority Of women with areported that the frequency of yeast infections, especially withpositive culture for yeast are leukorrhea, a burnlng Sensa‑

the Candida spp., has increased dramatically (9, 1 0,29)･ Thistion, 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 ofof 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 theal. (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 todischarge. 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)･ Vaginitisof5‑53.3% 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 wasglabrata 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 theresults of other studies (26,3 1 ‑33). Isolates of C. glabrata, thelactic 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 ison CA. The results of this study confirmthe difficulties withgreatly appreciated. I would like to thank Dr･ Ali Z･ Elkami

C. glabrata identification encountered with CA reported byfor critically reading the manuscrlPt･

105

This study was partially supported by the Hashemite

Agents Chemother., 37, 1 847‑1849.

University Research Council.

1 6. Abi‑Said, D., Anaissie, E., Uzun, 0., Ra且d, 1., Pinzcowski,

H. and Vartivarian, S. (1997): The epidemiology ofhematogenous candidiasis caused by different Candida
species. Clin. Infect. Dis., 24, 1 12211 128.

REFERENCES
1. Sobel, ∫. D. (1992): Pathogenesis and treatment of

17. Price, M. F., LaRocco, M. T. and Gentry,し. 0.(1994):

recurrentvulvovaglnal candidiasis. Clin. Infect･ Dis., 14

Fluconazole susceptibilities of Candida species and(Suppl.), S148‑S153.

distribution of species recovered from blood cultures overa 5‑year period. Antimicrob. Agents Chemother., 38,

2. Giraldo, P., Yon Nowaskonski, A., Gomes, F. A., Linhares,

1., Neves, N. A. and Witkin, S. S. (2000): Vaginal coloni‑

1422‑1424.

zation by Candida in asymptomatic women with and

18. Rex, J. H., Rinaldi, M. G. and Pfaller, M. A. (1995):

without a history of recurrent vulvovaglnal candidiasis.

Resistance of Candida species tofluconazole.Antimicrob.

Obstet. Gyneco1., 95, 413‑416.
3. Ringdahl, E. N. (2000): Treatment of recurrent vulvovagi‑
nal candidiasis. Am. Fan. Phys., 61, 3306‑3312.

Agents Chemother., 39, 1‑8.
19. Sinofsky, F. E. (1999): Vulvovaginal candidiasis: topicalversus oral therapy. The Female Patient, 24, 19‑23･

4･ Sobel, J･ D･ (1999)･ Limitatioヮs ofantifungal agents in

20. Spinillo, A., Capuzzo, E., Gulminetti, R･, Marone, P･,

the treatment of Candida vaglnitis: future challenges.
Drug Resist. Updates, 2, 148‑152.

risk factors for fungal vaglnitis caused by non‑albicans

Colonna,し. and Piazzi, G. (1997): Prevalence of and5. Odds, F. C. (1988): Candidiasis of the genitalia. p.124‑

species. Am. ∫. Obstet. Gyneco1., 176, 138‑141.

135. J〃 F.C. Odds (ed.), Candida and Candidosis. A

21. Sobel, ∫. D., Faro, S., Force, 良., Foxman, 良., Ledger, W.

Review and Bibliography, 2nd ed., Balliere‑Tindal,J., Nyirjesy, P. R., Reed, B. D. and Summers, P. R. (1998):
Vulvovaglnal candidiasis: epidemiologic, diagnosis, andthe therapeutic considerations. Am. J･ Obstet･ Gyneco1.,

London.

6. Knoke, M., Schulz, K. and Bernhardt, H. (1997):
Dynamics of Candida isolationsfrom humansfrom 1 9921
1995 in Greifswald, Germany. Mycoses, 40, 105‑I 10.

178, 203‑211.

22. Schuman, P., Capps, L and Peng, G. (1997): Weekly

7. Pfaller, M. A. (1996): Nosocomial candidiasis: emerging

fluconazole for the treatment of mucosal candidiasis in

species, reservoirs, and modes. Clin. Infect. Dis., 22,

women with HIV infection. A randomized, double blind,placebo controlled trial.Ann. Intern. Med., I 26, 689‑696.

Supp1., 89‑94.

8. Fidel, P. L., Vazquez, J.A.and Sobel, J. D. (1999): Candida

23. Hazen, K. C., Theisz, G. W. and Howelly, S. A. (1999):

glabrata: review of epidemiology, pathogenesis, andChronic urinary tract infection due to Candida utilis. J.

Clin. Microbio1., 37, 824‑827.

clinical disease with comparison to C. albicans. Clin.

Microbiol. Rev., 12, 80‑96.
9. Berrouane, Y. F., Herwaldt, L A. and Pfaller, M. A. (1999):

24. Febre, N., Silva, V, Medeiros, E. A. S., Wey, 良., Colombo,

A･ L･ and Fisclman, 0･ (1 999): Microbiological character‑

Trends in antifungal use and epidemiology ofnosocomial

istics of yeasts isolated from urinary tracts of intensive

yeast infTectionsina universityhospital. J. Clin. Microbiol.,care unlt Patients undergolng urinary catheterization. J.

Clin. Microbio1., 37, 1584‑1586.
25. Lockhart, S. R., Joly, S., Vargas, K., Swails‑Wenger, J.,

37, 531‑537.

10. Hazen, K. C. (1995): New and emerging yeast species.

Clin. Microbiol. Rev., 8, 462‑478.
ll. Nguyen, M. H., Peacock, J. E" MomiS,A. J., Tanner, D.
C., Nguyen, M. L., Snydman, D. R., Wagener, M. M.,
Rinaldi, M. G. and Yu, V. L. (1996): The changing face

Enger, L･ and Soll, D･ R･ (I 999)= Natural defenses P!ainst
Candida colonization breakdown in the oral cavltleS Of
the elderly. ∫. Dent. Res., 78, 857‑868.

of candidemia: emergence of non‑Candida albicans

26. Odds, F. C. and Bemaerts, R. (1994): CHROMagar
Candida, a new differential isolation medium forspecies and antifungal resistance.Am. J. Med., 100, 6 I 7‑

presumptlVe identi丘cation of clinically important Candida623.

species. ∫. Clin. Microbio1., 32, 1923‑1929.

12･ Wingard, J･ R. (1995): Importance of Candida species

27. Warren, N. G･ and Hazen, K･ C. (1995): Candida, CTWtO‑

other than C. albicans as pathogens in oncology patients.

cocc〟∫, and other yeasts of medical importance. p 723‑

Clin. Infect. Dis., 20, 115‑125.
13･ Rex, J･ H･, Bennett, J. E., Sugar,A. M., Pappas, P. G., vanTenover and 良. H. Yolken (eds), Manual of Clinicalder Horst, C. M., Edwards, ∫. E., Washbum, R. G., Scheld,

Microbiology.American SocietyofMicrobiology, Wash‑

W. M., Karchmer, A. W., Dine, A. P., Levenstein, M. J.
and Webb, C. D. (1994): A randomized trial comparing

28･ Pfaller, M･ A･ (1989): Infection. control: Opportunistic

737. In P. R. Murray, E. J. 0. Baron, M. A. Pfaller, F. C.

ington, D.C.
fungal infections‑the increasing Importance Of Candida
species. Infect. Control Hosp. Epidemiol., 1 0, 2701273.

nuconazole with amphotericin B for the treatment ofcandidemia in patients without neutropenia. N. Engl. ∫.

Med., 331, 1325‑1330.
14･ Rex, J. H., Pfaller, M. A., Barry,A. L., Nelson, P. W. andWebb, C. D. (1995): Antifungal susceptibility testing of

29. Abu‑Elteen, K. H., Abdul‑Malek, A. M. M. andAbdul‑
Wahid, N･ A･ (1997): Prevalence and susceptibility ofvaglnal yeast isolates in Jordan. Mycoses, 40, 179‑185.

isolatesfrom a randomized, multicenter trial offluconazole

30. Al‑Rawi, N. and Kavanagh, K. (1999): Characterization

versus amphotericin 良 as treatment of non‑neutropenicof yeasts implicated in vulvovaglnal candidiasis in Irish

patients withcandidemia.Antimicrob. Agents Chemother. ,women. Br. ∫. Biomed. S°i., 56, 99‑104.

31. Houang, E. T. S., Chu, K. C., Koehler,A. P. and Cheng,

39, 40‑44.
15. Wingard, ∫. 良., Merz, W G., Rinaldi, M. G., Miller, C. B.,

A. F. B. (1997): Use ofCHROMagar Candida for genitalKarp, J･ E･ and Saral, R. (1993):Association of Torulop‑

specimens in the diagnostic laboratory･ ∫. Clin. Patho1.,

sis glabrata infections withfluconazole prophylaxis in50, 563‑565.

32. Ainscough, S. and Kibbler, C. C. (1998): An evaluation

neutropenic bone ma汀OW transplant patients. Antimicrob.

106Intem. Med., 160, 2659‑2664.

of the cost‑effectiveness of using CHROMagar for yeast

36. Kronvall, G. and Karlsson, 1. (2001): Fluconazole andvoriconazole multidisk testlng Of Candida species for

identification in a routine microbiology laboratory. J.

Med. Microbio1., 47, 623‑628.
33. Pfaller, M. A., Houston, A. and Coffmann, S. (1996):
Application of CHROMagar Candida for rapid screen‑

disk test calibration and MIC estimation. ∫. Clin.

Microbio1., 39, 1422‑1428.

lng Ofclinical specimens for Candida albicans, Candida

37. Chang, H. C., Chang, J. J., Chan, S. H., Huang,A. H.,

tropicalis, Candida krusei, and Candida (Torulopsis)

Wu, T.し., Liれ, M. C. and C血ang, T. C. (2001): Evalua‑glabrata. J. Clin. Microbio1., 34, 58‑61.

tion of Etest for direct antifungal susceptibility testing
ofyeasts in positive blood cultures. ∫. Clin. Microbio1.,

34. Vazquez, ∫. A., Sobel, ∫. D., Peng, G., Steele‑Moore,し,Schum.an, P･, Holloway, W･ and Neaton, J･ D･ (1999):

39, 1328‑1333.

38. Willmott, F. E. (1975): Genital yeasts in female patients

EvolutlOn Of vaginal Candida species recovered fromhuman immunodeficiency virus‑infected women receiv‑

attending a VD clinic. Br. ∫. Vener. Dis., 51, 119‑122.

39. Geiger,A. M., Foxman, B. and Sobel, ). D. (1995): Chromic

lng nuCOnaZOle prophylaxis: the emergence of Candida

vulvovaglnal candidiasis: characteristics of women withglabrata. Clin. Infect. Dis., 28, 1025‑1031.

Candida albicans, Candida glabrata, and no Candida.

35. Abbas, ∫., Bodey, G. P., Hanna, H. A., Mardani, M.,

Genitourin. Med., 7 1, 304‑307.

Girgawy, E., Abi‑Said, D., Whimbey, E., Hachem, 良.

and Raad, I. (2000): Candida krusei fungemia. Arch.

107