Arch Gynecol Obstet (2008) 278:463–466 DOI 10.1007/s00404-008-0593-8
O R I G I N A L A R T I CL E
Prevalence of Candida albicans and bacterial vaginosis in asymptomatic pregnant women in South Yorkshire, United Kingdom Outcome of a prospective study A. A. Akinbiyi · Robert Watson · Paul Feyi-Waboso
Received: 31 December 2007 / Accepted: 29 January 2008 / Published online: 26 February 2008 © Springer-Verlag 2008
Abstract Objective The aim of the study was to determine the prevalence and age distribution of Candida albicans and bacterial vaginosis in asymptomatic pregnant women. Method One thousand and seventy-three (1,073) consecutive women who attended the antenatal clinic at Barnsley District General Hospital, Barnsley, UK, over a 15-month period were studied. Endo-cervical and high vaginal swabs for Candida albicans were obtained. Results Sixty-Wve percent (65%) were in the age group of 21–30 years, and the smallest group was of age 40 years and above. Maternal age of all the women was 25.8 years (SD 5.5) with a range of 33. Prevalence of Candida albicans was 12.5%, and the highest percentage of 65.7% (88 patients) was in the age group of 21–30 years. Prevalence of bacterial vaginosis was 3.54%, with almost 90% among the age group of 21–30 years. There is no Wnancial support from an individual or pharmaceutical company. A. A. Akinbiyi (&) Department of Obstetrics and Gynecology, Regina General Hospital, Regina, Saskatchewan, Canada e-mail:
[email protected] A. A. Akinbiyi 217-2125, 11th Avenue, Regina, Saskatchewan, Canada R. Watson Department of Obstetrics, Barnsley District General Hospital, Pogmoor Road, Barnsley S75 2EP, S. Yorkshire, UK e-mail:
[email protected] P. Feyi-Waboso Department of Obstetrics and Gynecology, Abia State University Teaching Hospital, P.M.B. 2002, Aba, Abia State, Nigeria
Conclusion Prevalence of Candida albicans and bacteria vaginosis among asymptomatic pregnant women was 12.5 and 3.54%, respectively. Keywords Candida albicans · Bacterial vaginosis · Asymptomatic pregnant women · ELISA (enzyme-linked immunosorbent assay)
Introduction In the United States and many developed world, bacterial vaginosis is currently the most common cause of vaginosis, accounting for 40–50% of cases in women of childbearing age [1]. Accurate prevalence is diYcult because one third to three quarters of aVected women ‘feel’ asymptomatic; high pH and Wshy smell are symptoms according to Amsel and Spiegel, which determines the diagnosis [2–4]. In addition, reported prevalences vary based on the population studied. Bacterial vaginosis has been found in 15–19% of ambulatory gynecology patients, 10–30% of pregnant patients and 24–40% of patients in sexually transmitted disease clinics [5, 6]. The most common etiologies in adults resulting in symptoms of vaginitis include Candida albicans, Trichomonas vaginalis and bacterial vaginosis. An association has been established between Candida albicans and bacterial vaginosis infections in symptomatic women, but the relationship between C. trachomatis and bacterial vaginosis is at best controversial. Establishing Candida species as the cause of vaginitis can be diYcult, because as many as 50% of asymptomatic women have Candida organisms as part of their endogenous vaginal Xora; hence, limitations of symptoms and signs in the diagnosis of vaginal infections had been recognized [5, 7, 8]. Our study is mainly focused on the prevalence of these infections in our predominant
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Caucasian population with a view of future research of cost-analysis and recommendations.
Materials and methods This study was a randomized prospective study carried out at the Barnsley District General Hospital, Barnsley, United Kingdom, over a 15-month period. Approval was obtained from the Institutional Review Board of the hospital. Patients were recruited from the Antenatal Clinic of the hospital. The Departments of Obstetrics and Microbiology, Nursing and Microbiology were actively involved in the study. Eligible participants were pregnant women between the gestational ages of 15 and 24 weeks. A cut-oV of 24 weeks was taken based on the fact that all Wrst prenatal visits were normally registered by this gestational age. One thousand and seventy-three (1,073) consecutive asymptomatic pregnant patients at gestational ages of 15–24 weeks were included in the study after obtaining their informed consents. The ages of the patients ranged from 15 to 49 years. These patients were from Barnsley, which is a small town in South Yorkshire, United Kingdom, with a population of 250,000, and areas near by it. The 1,073 consecutive patients were screened after the procedure was explained to them, and their written consents were obtained. All the three consultant obstetricians and gynecologists in addition to two resident doctors were involved in the screening the patients following adequate training about proper specimen collection and storage. All eligible women who were referred to the Antenatal Clinic were included in the study. The exclusion criteria were those unwilling or incapable of giving informed consent to participate in the study. Patients with vaginal bleeding, threatened abortion and those currently on antibiotics that are sensitive to Candida albicans and bacterial vaginosis were excluded. Patients who were receiving other treatments were allowed to continue to do so, but the dose, timing, duration and reason for administration of any concomitant medication were documented. The primary outcome measure was the prevalence of these infections in relation to the age of the asymptomatic pregnant women. Laboratory tests were performed within 24 h of collections with an excellent storage. A dedicated microbiologist and two laboratory technicians were in charge of the tests. The diagnosis of Candida albicans was done by slide smear examination and yeast culture of the vaginal Xuid to distinguish the diVerent species of Candida. Smears taken from the vagina and endocervix were examined by Gram’s stain method. Smears were taken by gently applying the swab on to the cervix. The vagina smear was examined under the microscope, and Candida was detected
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Arch Gynecol Obstet (2008) 278:463–466
by Wnding hyphae and blastospores. Further analysis to distinguish Candida albicans from the others were done by CHROMagar Candida medium supplemented with Pal’s agar, which allowed us to make a rapid and easy diVerentiation of Candida. Bacterial vaginosis was screened by slide smear examination. Bacterial vaginosis was diagnosed when at least three of the following criteria were fulWlled according to Spiegel: vaginal pH > 4.5; homogenous appearance with low viscosity and milky consistency; the presence of clue cells and an amine odor (positive WhiV test) [4]. Bacterial vaginosis was, however, not treated unless the patients are symptomatic or have a history of preterm deliveries.
Statistical analysis Results were expressed as mean § standard deviation (SD). The 2 test or Fisher’s test was used to determine the statistical signiWcance of diVerences in each of the characteristics. Statistical software package SPSS (SPSS 12.0 Incorporated Chicago, IL) was used for all data analysis. The two-sample P value of less than 0.05 was considered signiWcant and with a Chi-square of one degree of freedom.
Results A prospective study of consecutive one thousand and seventy-three (1,073) pregnant patients of gestational ages 15– 24 weeks were studied over the 15-month period for Candida albicans and bacterial vaginosis. No participants were lost to follow-up, and there were no dropouts. The ethnicity of the population studied was 99.9% Caucasians. The mean maternal age of all the women was 25.8 years (SD 5.5) with a range of 33. Out of one thousand and seventy-three (1,073) women studied, 65% were in the age group of 21– 30 years, and the smallest group was 0.1% (13) among the age group of 40 years and above (Table 1, Fig. 1). The overall prevalence of Candida albicans was 12.5%, and the highest percentage of 65.7% (88) found in the age group of 21–30 years compared to the lowest percentage of 2.2% (3) Table 1 Age distribution of study group Age group (years)
Number of cases
Percentage (%)
11–20
186
17
21–30
695
65
31–35
135
13
36–40
44
4
>40
13
1
1,073
100
Total
Arch Gynecol Obstet (2008) 278:463–466
465
100 Candida albicans Bacterial vaginosis
90 80
Prevalence
70 60 50 40 30 20 10 0 11-20
21-30
31-35
36-40
>40
Age in years
Fig. 1 Age distribution of patients with Candida albicans and bacterial vaginosis
in the age group of 40 years and above (Table 2). The overall prevalence of bacterial vaginosis was 3.54%, and the highest rate of 2.79% (30) was in the age group of 21– 30 years, with no case reported amongst women over the age of 35 years (Table 3).
Discussion The prevalence of Candida albicans and bacterial vaginosis in asymptomatic pregnant women vary from one population to another. DiVerent prevalence rates of asymptomatic women with genital tract infections have been widely reported [9–11]. It is controversial whether the prevalence Table 2 Age distribution of patients with Candida albicans Age group (years)
Number of patients
Percentage (%)
11–20
19
14.2
21–30
88
65.7
31–35
17
12.7
36–40
7
5.2
>40
3
2.2
134
100
Total
Table 3 Age distribution of patients with bacterial vaginosis Age group (years)
Number of patients
Percentage (%)
11–20
6
15.79
21–30
30
78.95
31–35
2
5.26
36–40
0
0
>40
0
0
Total
38
100
is higher among black women compared to white women even in the same socio-economic group [12]. In a recent study from a University Teaching Hospital, Benin City, Nigeria, a high prevalence (65%) of Candida albicans among asymptomatic pregnant was reported [2]. This may be a reXection of the diVerences in the nutritional status and socioeconomic class of the study group. A study conducted in Portugal showed that the overall prevalence of C. albicans in the vaginal Xuid of asymptomatic pregnant women was 10.4%, while bacterial vaginosis occurred in 5% of the women [9]. This latter result compared favorably with an overall prevalence of 12.4% (P · 0.5118) and 3.54% (P · 0.6255) for Candida albicans and bacterial vaginosis, respectively, in our study. There was no signiWcant diVerence between their study and ours. Candidosis is a common fungal infection in women of childbearing age, which often results in pruritus, and a thick, white vaginal discharge. Candida albicans is the infecting agent in 80–90% of patients; however, recent reports showed a shift to colonization with C. glabrata [9, 12, 13]. Only one patient had colonization with C. glabrata in our study. Currently, peptide nucleic acid Xuorescent in situ hybridization (PNA-FISH) is one of the most reliable methods used to distinguish C. albicans from non-Candida albicans species, but is not widely used because it is expensive. Patients often have a history of recurrent yeast infections or recent antibiotic treatment. Women who are symptomatic are easily diagnosed and treated appropriately. Asymptomatic women are not even tested, how much more of being treated. Recurrent episodes may indicate underlying immunodeWciency, prolonged steroid usage, pregnancy or diabetes [11]. It has been stated that Candida albicans can be cultured from the vagina in about 25% of pregnant women approaching term, whereas asymptomatic women do not require any treatment [13]. Prevalence of 12.4% compared to the above rate of 25% colonization among all women is signiWcantly diVerent (P < 0.0003). Diagnosis is usually based on history and microscopic examination of wetmount. Positive result may be obtained in about 50–70% of patients with the infection, while those with negative microscopy could be conWrmed with Gram stain or cultured with Sabourad’s medium [14, 15]. Symptomatic pregnant women are usually treated with topical antifungal agents such as nystatin, clotrimazole or miconazole. Oral antifungal agent such as DiXucan is usually avoided in pregnancy for fear of teratogenicity [16, 17]. Bacterial vaginosis is asymptomatic in up to 50% of women [18]. If a discharge is present, it is typically in homogeneous grayish white or yellowish white according to Spiegel’s criteria [4]. There are conXicting reports in the literatures with regard to reliability of diagnosis of bacterial vaginosis [4, 19, 20].
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Bacterial vaginosis is common in pregnant women and is associated with preterm birth. Typically, women complaining of Wshy odor when tested in pregnancy have a prevalence that is between 10 and 30% [13, 20, 21]. Our study showed a prevalence of 3.54%, which was quite low and does not justify routine screening. Treating symptomatic pregnant women with a history of preterm birth early in pregnancy has been shown to decrease the incidence of preterm delivery [22]. Treatment with metronidazole has been found to reduce cervical concentrations of interleukins-1, -8 and -6; however, screening and treatment have not been shown to prevent preterm birth [16]. Evidence suggests that bacterial vaginosis is a risk factor for premature rupture of membranes, preterm labor and chorioamnionitis. There is no evidence that metronidazole is teratogenic in pregnant humans; however, initial studies conWrmed teratogenicity in rats [16, 23]. Even though higher rates of bacterial vaginosis have been reported in sexually transmitted disease clinics and in women with multiple sexual partners, the role of sexual transmission is unclear. Studies indicate that treating the male sexual partner of a woman with bacterial vaginosis is not beneWcial and that even women who are not sexually active can have the infection [24, 25]. Prevalence of Candida albicans and bacterial vaginosis in our study compared favorably with a lot of studies from some other western countries, but diVered from some of the reports from the underdeveloped/developing countries where high rates prevail [2, 8]. Acknowledgments We are indebted to the Institutional Review Board of the Barnsley District General Hospital, Barnsley, for the approval of the protocol for the study. The invaluable service and the enthusiasm shown by Dr. Mera Osman and her staV at the Microbiology Department and the nursing staV of Obstetrics and Gynecology Department are highly commendable.
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10. 11.
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