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Bacterial vaginosis among women with tubal factor infertility in Nigeria
IJG-08435; No of Pages 4 International Journal of Gynecology and Obstetrics xxx (2015) xxx–xxx
Contents lists available at ScienceDirect
International Journal of Gynecology and Obstetrics journal homepage: www.elsevier.com/locate/ijgo
CLINICAL ARTICLE
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Bacterial vaginosis among women with tubal factor infertility in Nigeria
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Innocent l. Durugbo a, Tamunomie K. Nyengidiki a,⁎, Goddy Bassey a, Kennedy T. Wariso b a
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Article history: Received 8 November 2014 Received in revised form 26 April 2015 Accepted 10 August 2015
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Keywords: Bacterial vaginosis Nigeria Tubal infertility
Department of Obstetrics and Gynaecology, University of Port Harcourt Teaching Hospital, Port Harcourt, Rivers State, Nigeria Department of Microbiology, University of Port Harcourt Teaching Hospital, Port Harcourt, Rivers State, Nigeria
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Objective: To determine the prevalence of bacterial vaginosis among women with tubal factor infertility. Methods: A cross-sectional prospective study of women with tubal factor infertility was conducted at a Nigerian teaching hospital between March and September 2014. An equal number of fertile women attending the family planning clinic were recruited as controls. Interviews were conducted to collect data on sociodemographic characteristics, history and characteristics of vaginal discharge, knowledge, and practices. Bacterial vaginosis was diagnosed using the Amsel criteria. Odds ratios (ORs) with 95% confidence intervals (CIs) were calculated to determine predisposing factors. Results: Overall, 178 women with tubal factor infertility were recruited. Bacterial vaginosis was noted in 50 (28.1%) of these women, compared with 14 (7.9%) of 178 fertile women (P b 0.001). Patients with tubal factor infertility had an increased risk of bacterial vaginosis when they were of low socioeconomic class (OR 11.89; 95% CI 5.20–27.69), practiced vaginal douching (OR 19.15; 95% CI 7.26–47.75), used vaginal drying agents (OR 17.04; 95% CI 6.91–43.24), had an early sexual debut (OR 32.08; 95% CI 12.02–88.89), and had a history of sexually transmitted infections (OR 12.42; 95% CI 5.36–29.35). Conclusion: The prevalence of bacterial vaginosis was high among patients with tubal factor infertility. Socioeconomic and cultural factors contribute to the risk of the condition. © 2015 Published by Elsevier Ireland Ltd. on behalf of International Federation of Gynecology and Obstetrics.
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1. Introduction
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Tubal factors constitute a leading cause of infertility, which is an important reproductive health problem in low-income countries [1,2]. The main etiology of tubal damage is pelvic inflammatory disease, which can arise after induced abortion, intrauterine procedures, or pelvic surgeries. One episode of pelvic inflammatory disease confers a 10% risk of future tubal factor infertility; the risk increases after further infections [1]. The prevalence of infertility in Nigeria has been reported to be as high as 15%–16%, with approximately 60% of infertility being caused by pelvic infections [3,4]. The role of bacterial vaginosis in the etiology of infertility has been demonstrated in various studies worldwide. In a review of infertile patients in Nigeria [5], bacterial vaginosis was observed in 35.3% of cases; a similar review in Egypt [6] noted a prevalence of bacterial vaginosis of 36.6%. By contrast, a prevalence of 8.6% was observed in the Netherlands [7], giving credence to the notion that the occurrence of bacterial vaginosis varies by geographical location. The organism Lactobacillus is the main contributor to vaginal acidity and prevents the growth of pathologic organisms in the vagina. Bacterial vaginosis occurs when the number of lactobacilli is reduced, the pH rises, and the number of pathogenic bacteria increases. These potential
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⁎ Corresponding author at: Department of Obstetrics and Gynaecology, University of Port Harcourt Teaching Hospital, Port Harcourt, Rivers State, 500001, Nigeria. Tel.: +234 8037109486. E-mail address: [email protected] (T.K. Nyengidiki).
pathogens include Gardnerella vaginalis, Bacteroides spp., Escherichia coli, group B streptococci, and the anaerobes Peptostreptococcus and Mycoplasma hominis. The anaerobic organisms and G. vaginalis are thought to act synergistically to cause vaginal infection. Anukam et al. [8] also observed the polymicrobial nature of bacterial vaginosis among Nigerian women. Bacterial vaginosis is characterized by a creamy vaginal discharge that is homogenous, is adherent to the vaginal wall, and has a fishy smell, without extensive evidence of inflammation. It is thought to lead to infertility because the natural defense mechanisms of the vagina are disturbed, leading to the spread of infectious agents toward the upper genital tract and resulting in tubal damage, blockage, or tubal motility disorder [9,10]. There is paucity of data in Nigeria concerning the actual contribution of bacterial vaginosis to the tubal component of infertility. The present study therefore sought to determine the prevalence of bacterial vaginosis and the predisposing factors among women with tubal factor infertility in Nigeria.
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2. Materials and methods
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A cross-sessional prospective study was undertaken at the University of Port Harcourt Teaching Hospital in Port Harcourt, Nigeria, between March 3 and September 30, 2014. All consecutive women with tubal factor infertility who presented for follow-up at the gynecology clinic were recruited. Women with tubal factor infertility had been previously
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http://dx.doi.org/10.1016/j.ijgo.2015.05.031 0020-7292/© 2015 Published by Elsevier Ireland Ltd. on behalf of International Federation of Gynecology and Obstetrics.
Please cite this article as: Durugbo I, et al, Bacterial vaginosis among women with tubal factor infertility in Nigeria, Int J Gynecol Obstet (2015), http://dx.doi.org/10.1016/j.ijgo.2015.05.031
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75 76 77
103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130 131
135 136 137 138 139 140 141
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Age, y b20 20–24 25–29 30–34 ≥35 Educational status None Primary Secondary Tertiary Social classb Low (IV, V)c Middle (III) High (I, II)
t1:3
BV (n = 50)
No BV (n = 128)
BV (n = 14)
No BV (n = 164)
t1:4
0 6 (12.0) 22 (44.0) 19 (38.0) 3 (6.0)
0 14 (10.9) 55 (43.0) 41 (32.0) 18 (14.1)
1 (7.1) 1 (7.1) 5 (35.7) 4 (28.6) 3 (21.5)
5 (3.0) 19 (11.6) 61 (37.2) 56 (34.1) 23 (14.0)
0 38 (76.0) 8 (16.0) 4 (8.0)
0 17 (13.3) 59 (46.1) 52 (40.6)
0 9 (64.3) 3 (21.4) 2 (14.3)
0 31 (18.9) 84 (51.2) 49 (29.9)
8 (57.1) 4 (28.6) 2 (14.3)
23 (14.0) 99 (60.4) 42 (25.6)
35 (70.0) 12 (24.0) 3 (6.0)
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A total of 178 women with tubal factor infertility were recruited. Bacterial vaginosis was recorded among 50 (28.1%) of these women, compared with 14 (7.9%) of the 178 fertile women recruited as controls (χ2 = 24.69, P b 0.001). Table 1 shows sociodemographic characteristics of women with and without bacterial vaginosis. The mean age of the women with tubal factor infertility was 28 ± 5 years (range 22–36). Table 2 shows the analysis of risk factors for bacterial vaginosis. Vaginal douching and use of vaginal tightening and drying products
85 86
Fertile women (control group)
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84
Women with tubal infertility
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3. Results
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Variable
21 (16.4) 61 (47.7) 46 (35.9)
t1:5 t1:6 t1:7 t1:8 t1:9 t1:10 t1:11 t1:12 t1:13 t1:14 t1:15 t1:16 t1:17 t1:18 t1:19
Abbreviation: BV, bacterial vaginosis. a Values are given as number (percentage). b Age and education level were used to compute the social class of participants and thus it was not necessary to perform a statistical analysis on these variables. c BV was significantly more likely among women with tubal infertility who were of low socioeconomic class than among those who were of middle or high socioeconomic class 2 (χ = 47.89, P b 0.001; odds ratio 11.89, 95% confidence interval 5.20-27.69).
t1:20 t1:21 t1:22 t1:23 t1:24 t1:25 t1:26
were significantly associated with bacterial vaginosis among women with tubal factor infertility (P b 0.001 for both). In this population, a young age at sexual debut and a history of STIs were also both significantly associated with bacterial vaginosis (P b 0.001 for both). Only having had one sexual partner was a protective factor, reducing the likelihood of bacterial vaginosis among women with tubal factor infertility (P b 0.001). Smoking was not found to be associated with bacterial vaginosis in this population. Similar findings were recorded among fertile women (Table 2). Few women with tubal factor infertility were aware of bacterial vaginosis, irrespective of whether they had the condition (Table 3). Two (8.3%) of the 24 women with tubal factor infertility who were aware of bacterial vaginosis knew that bacterial vaginosis is a risk factor for tubal factor infertility. No woman was aware that bacterial vaginosis is a risk factor for premature rupture of fetal membranes and preterm delivery.
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4. Discussion
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In the present study, the prevalence of bacterial vaginosis among women with tubal factor infertility was 28.1%. As among fertile women, vaginal douching, the use of vaginal tightening or drying products, early age at sexual debut, a high number of sexual partners, and history of STIs were associated with bacterial vaginosis. The prevalence of bacterial vaginosis among women with tubal factor infertility in the present study is higher than the prevalence of 12%–12.9% noted among women attending infertility clinics in Rwanda [14] and Mozambique [15]. The high prevalence noted in the present study could be attributed to the fact that the women in the present study constituted a highly selected population compared with more generalized samples of infertile patients in the Rwandan and Mozambican studies. A metaanalysis by van Oostrum et al. [9] showed that the prevalence of bacterial vaginosis was higher among women with tubal factor infertility than among women with infertility due to other causes of infertility, even though most studies reviewed failed to establish causal relationships between bacterial vaginosis and tubal infertility. Patients of a lower socioeconomic class had an increased risk of bacterial vaginosis in the present survey. In studies from the USA [16] and Bangladesh [17], a lower socioeconomic class has been associated with poor health-seeking behavior and a higher risk of STIs, which in turn
159 160
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133
80 81
t1:1 t1:2
Table 1 Sociodemographic characteristics, by presence of BV.a
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diagnosed by hysterosalpingography. Women were excluded if they had received metronidazole or clindamycin for a disease or condition other than bacterial vaginosis within the previous 90 days, irrespective of the route of administration; had experienced vaginal bleeding; had infertility due to causes other than tubal factors; or had undergone bilateral salpingectomy. An equal number of fertile women attending the family planning clinic were also recruited as controls. Ethics clearance for the present study was obtained from the Ethics Review Committee of the teaching hospital. All participants provided informed consent. Each patient was interviewed using a structured study form that was completed by the interviewers. Information about age, tribe, occupation, level of education, husband’s occupation, and parity was obtained. The social class of each participant was determined on the basis of the woman’s educational status and her husband’s occupation, as proposed by Olusanya et al. [11]. Other collected information included the history of abnormal vaginal discharge, practice of vaginal douching, use of vaginal tightening or drying products, and age of sexual debut. The number of lifetime sexual partners, history of sexually transmitted infections (STIs), and history of smoking were also ascertained. After the interview, each participant underwent a procedure to obtain a vaginal sample in the presence of a female assistant, who also served as a chaperone. The patient was placed in a dorsal position on an examination table. Guided by an angle point light, a bivalve speculum was introduced into the vagina (without lubrication). A wooden spatula was used to take a sample of the vaginal discharge/secretion from the vaginal walls and the posterior vaginal fornix. The vaginal discharge or secretion was then assessed on the basis of the Amsel criteria [12]. Initially, three of the criteria were assessed. The discharge/secretion was examined visually to establish whether it was characteristic of bacterial vaginosis (homogenous and creamy). The pH value of the vaginal fluid was then determined with a pH meter, after adding 1 mL of normal saline to the collected vaginal secretion in a sterile test tube and mixing it thoroughly. A vaginal fluid pH of more than 4.5 is indicative of bacterial vaginosis. Thereafter, a drop of the solution was placed on a clean glass slide and one drop of 10% potassium hydroxide in aqueous solution was added to it. The slide was then smelt to determine whether the mixture had a fishy odor (“whiff test”). This odor, when present, is strongly suggestive of bacterial vaginosis. For participants with at least two positive results for these three assessments, a microscopic examination of the prepared slide was then performed to determine whether “clue cells” were present (fourth Amsel criterion). The diagnosis of bacterial vaginosis was confirmed if more than 20% of the epithelial cells had adherent bacteria. The sample size was determined using a formula proposed by Kish for the estimation of single proportions [13]. The minimum sample size was calculated to be 162. Allowing for an attrition of 10% (i.e. 16 women), 178 women with tubal factor infertility were recruited. The data were analyzed using SPSS version 20.0 (IBM, Amonk, NY, USA) and Epi Info version 7.0 (Centers for Disease Control and Prevention, Atlanta, GA, USA). Frequency tables were generated and the results were tested for significance using the Student t test and the χ2 test. P b 0.05 was considered statistically significant. An assessment of the risk factors for bacterial vaginosis among patients with tubal infertility and among control individuals was estimated by calculating odds ratios (ORs) with 95% confidence intervals (CIs).
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Please cite this article as: Durugbo I, et al, Bacterial vaginosis among women with tubal factor infertility in Nigeria, Int J Gynecol Obstet (2015), http://dx.doi.org/10.1016/j.ijgo.2015.05.031
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Women with tubal factor infertility
20 (15.6) 108 (84.4)
41 (82.0) 9 (18.0)
27 (21.1) 101(78.9)
5 (10.0) 45 (90.0)
12 (9.4) 116 (90.6)
42 (84.0) 8 (16.0)
18 (14.1) 110 (85.9)
10 (20.0) 40 (80.0)
106 (82.8) 22 (17.2)
38 (76.0) 12 (24.0)
26 (20.3) 102 (79.7)
OR (95% CI)
b0.001
19.15 (7.26–47.75)
b0.001
0.889
b0.001
b0.001
b0.001
increase the risk of tubal factor infertility. The poor health-seeking behavior among this group means that any bacterial vaginosis goes untreated, hence creating the necessary milieu for ascending organisms to cause tubal damage. Vaginal douching, which women in Nigeria practice for various reasons, contributed significantly to the development of bacterial vaginosis. This is in agreement with the findings of a previous study [18], in which vaginal douching was identified as the greatest predictor of bacterial vaginosis. A study by Hutchinson et al. [16] demonstrated a 5.1fold increase in the risk of bacterial vaginosis with vaginal douching, which is far lower than the 19-fold increase among women with tubal factor infertility that was observed in the present study. The wide disparity in the risk between the two study populations could be because the present study included only patients with tubal factor infertility, who have been shown during epidemiological studies to have an increased incidence of bacterial vaginosis and pelvic inflammatory disease [19]. Despite being discouraged, vaginal douching is still a common practice in Nigeria, and is used by women and girls to “clean” the vagina for hygienic purposes to remove odor during or after menses and to prevent STIs. The use of vaginal tightening or drying products increased the risk of bacterial vaginosis 17 times in the present population. Other researchers have observed similar results. In a survey of 250 women in the USA, Schwebke et al. [20] identified a 5.11-fold increase in the risk of developing vaginal vaginosis among women who douche for the purpose of vaginal tightening. The reason for the use of tightening or drying products is essentially a cultural preference for a dry vagina to improve sexual satisfaction, but these agents disrupt the normal bacterial flora [21]. Similarly, the distortion of the vaginal flora not only decreases the lactobacilli population but also encourages the growth of pathogenic strains of bacteria that are responsible for tubal damage [10].
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t3:1 t3:2
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Table 3 Awareness of BV and its associated risks among patients with tubal factor infertility.a
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Awareness
BV (n = 50)
No BV (n = 128)
P value
Odds ratio (95% CI)
t3:4 t3:5
Aware Unaware
6 (12.0) 44 (88.0)
18 (14.1) 110 (85.9)
0.71
0.83 (0.27–2.42)
t3:6 t3:7
Abbreviations: BV, bacterial vaginosis; CI, confidence interval. a Values are given as number (percentage) unless indicated otherwise.
12 (85.7) 2 (14.3)
39 (23.8) 125 (76.2)
11 (78.6) 3 (21.4)
45 (27.4) 119 (72.6)
2 (14.3) 12 (85.7)
19 (11.6) 145 (88.4)
10 (71.4) 4 (28.6)
34 (20.7) 130 (79.3)
17.04 (6.91–43.24)
P value
OR (95% CI)
b0.001
19.23 (3.82–130.43)
b0.001
9.70 (2.35–46.15)
1.07 (0.31–3.54)
0.511
32.08 (12.02–88.89)
0.05 (0.02–0.13)
12.42 (5.36–29.35)
11 (78.6) 3 (21.4)
Abbreviations: BV, bacterial vaginosis; OR, odds ratio; CI, confidence interval. a Values are given as number (percentage) unless indicated otherwise.
183 184
No BV (n = 164)
2 (14.3) 12 (85.7)
t2:24 t2:25
181 182
BV (n = 14)
1.27 (0.00–6.75)
b0.001
9.56 (2.54–38.92)
b0.001
0.04 (0.01–0.18)
b0.001
21.39 (4.99–105.30)
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39 (78.0) 11 (22.0)
Fertile women (control group)
P value
O
Vaginal douching Yes No Use of vaginal tightening and drying products Yes No Smoking Yes No Age at sexual debut, y ≤15 N15 Number of lifetime sexual partners 1 ≥2 History of sexually transmitted infection Yes No
No BV (n = 128)
R O
t2:6 t2:7 t2:8 t2:9 t2:10 t2:11 t2:12 t2:13 t2:14 t2:15 t2:16 t2:17 t2:18 t2:19 t2:20 t2:21 t2:22 t2:23
BV (n = 50)
135 (82.3) 29 (17.7) 24 (14.6) 140 (85.4)
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Variable
t2:4 t2:5
Investigators differ in their opinion on the effect of smoking on the risk of bacterial vaginosis [22,23]. In the present survey, smoking was not a significant risk factor for the development of bacterial vaginosis. Cultural restrictions preventing women from smoking in the present environment could have highly reduced the contributory influence of smoking among the group with tubal factor infertility. Ness et al. [22] identified smoking as a marker of sexual behavior, because women who were smokers had more lifetime sexual partners than nonsmokers did and were thus at risk of pelvic inflammatory disease, a known cause of tubal infertility. In the present study, however, the number of lifetime partners was noted to be related to the occurrence of bacterial vaginosis: having only one sexual partner significantly reduced the risk of bacterial vaginosis. This gives credence to the fact that the frequency of intercourse increases with the number of partners, which changes the vaginal environment for the occurrence of bacterial vaginosis. Sexual debut before the age of 15 years was observed to significantly increase the risk of bacterial vaginosis. Early initiation of sexual intercourse as a contributory factor to bacterial vaginosis has also been noted in other studies [24,25]. The increase in risk associated with an early sexual debut was more than three times higher among women with tubal factor infertility than among control women in the present study. Initiation of intercourse before puberty—mean age at puberty in Nigeria is 15.26 years [26]—during a period of low lactobacilli colonization therefore increases the risk of bacterial vaginosis and also the rate of tubal infertility. However, it should noted that bacterial vaginosis has also been found in virgins, implicating other risk factors that are not related to intercourse [27]. In line with the findings of Vaca et al. [27], the present study also revealed a strong association between a history of STIs and bacterial vaginosis. Bacterial vaginosis renders women vulnerable to STIs and consequent pelvic inflammatory disease, tubal blockage, and infertility [28]. The level of awareness of bacterial vaginosis and its associated complications among the participants was surprisingly low among women with tubal factor infertility. Poor awareness was exhibited by women across all levels of education and occupation irrespective of bacterial vaginosis status. This finding supports the theory that the high prevalence of bacterial vaginosis is not driven by a lack of awareness but by high-risk behaviors. The present study was limited by the fact that the study population was hospital-based and the result might not necessarily be applicable to the whole population. Hence, community-based prevalence studies are
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Table 2 Risk factors for BV.a
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t2:1 t2:2
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Please cite this article as: Durugbo I, et al, Bacterial vaginosis among women with tubal factor infertility in Nigeria, Int J Gynecol Obstet (2015), http://dx.doi.org/10.1016/j.ijgo.2015.05.031
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The authors have no conflicts of interest.
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References
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advocated. Tubal blockage was diagnosed by hysterosalpingography as opposed to a laparoscopy and dye test, which is the recommended gold standard method of diagnosis. However, financial, equipment, and expertise challenges in the present environment made this diagnostic modality the only realistic method. The high prevalence of bacterial vaginosis among women with tubal factor infertility in the present study should be a wake-up call to clinicians to adopt strategies to reduce its prevalence. It is also an indication that there is a potentially large number of women with bacterial vaginosis in Nigeria who remain undiagnosed because of its largely asymptomatic nature. The contribution of certain socioeconomic factors and cultural practices—e.g. poverty, vaginal douching, application of vaginal tightening agents, and early sexual debut—to the risk of bacterial vaginosis cannot be overemphasized. On the basis of the present findings, women with tubal factor infertility should be routinely screened for bacterial vaginosis, and offered counseling and treatment when necessary. This will help to prevent some of the health consequences of bacterial vaginosis, especially when these women eventually become pregnant. The government should ensure improvements in the education for girls and women and in the overall welfare of citizens in a bid to improve women’s socioeconomic status. Efforts should be made to enlighten girls and women on the need to avoid the risk factors that predispose them to bacterial vaginosis. Girls and women should also be encouraged to improve their health-seeking behavior, because this will enhance the early identification, treatment, and prevention of bacterial vaginosis. There is an urgent need to raise the public health profile of bacterial vaginosis in relation to tubal infertility in Nigeria.
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Please cite this article as: Durugbo I, et al, Bacterial vaginosis among women with tubal factor infertility in Nigeria, Int J Gynecol Obstet (2015), http://dx.doi.org/10.1016/j.ijgo.2015.05.031
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Contents lists available at ScienceDirect
International Journal of Gynecology and Obstetrics journal homepage: www.elsevier.com/locate/ijgo
CLINICAL ARTICLE
2Q1
Bacterial vaginosis among women with tubal factor infertility in Nigeria
3Q2
Innocent l. Durugbo a, Tamunomie K. Nyengidiki a,⁎, Goddy Bassey a, Kennedy T. Wariso b a
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Article history: Received 8 November 2014 Received in revised form 26 April 2015 Accepted 10 August 2015
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Keywords: Bacterial vaginosis Nigeria Tubal infertility
Department of Obstetrics and Gynaecology, University of Port Harcourt Teaching Hospital, Port Harcourt, Rivers State, Nigeria Department of Microbiology, University of Port Harcourt Teaching Hospital, Port Harcourt, Rivers State, Nigeria
a b s t r a c t
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Objective: To determine the prevalence of bacterial vaginosis among women with tubal factor infertility. Methods: A cross-sectional prospective study of women with tubal factor infertility was conducted at a Nigerian teaching hospital between March and September 2014. An equal number of fertile women attending the family planning clinic were recruited as controls. Interviews were conducted to collect data on sociodemographic characteristics, history and characteristics of vaginal discharge, knowledge, and practices. Bacterial vaginosis was diagnosed using the Amsel criteria. Odds ratios (ORs) with 95% confidence intervals (CIs) were calculated to determine predisposing factors. Results: Overall, 178 women with tubal factor infertility were recruited. Bacterial vaginosis was noted in 50 (28.1%) of these women, compared with 14 (7.9%) of 178 fertile women (P b 0.001). Patients with tubal factor infertility had an increased risk of bacterial vaginosis when they were of low socioeconomic class (OR 11.89; 95% CI 5.20–27.69), practiced vaginal douching (OR 19.15; 95% CI 7.26–47.75), used vaginal drying agents (OR 17.04; 95% CI 6.91–43.24), had an early sexual debut (OR 32.08; 95% CI 12.02–88.89), and had a history of sexually transmitted infections (OR 12.42; 95% CI 5.36–29.35). Conclusion: The prevalence of bacterial vaginosis was high among patients with tubal factor infertility. Socioeconomic and cultural factors contribute to the risk of the condition. © 2015 Published by Elsevier Ireland Ltd. on behalf of International Federation of Gynecology and Obstetrics.
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1. Introduction
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Tubal factors constitute a leading cause of infertility, which is an important reproductive health problem in low-income countries [1,2]. The main etiology of tubal damage is pelvic inflammatory disease, which can arise after induced abortion, intrauterine procedures, or pelvic surgeries. One episode of pelvic inflammatory disease confers a 10% risk of future tubal factor infertility; the risk increases after further infections [1]. The prevalence of infertility in Nigeria has been reported to be as high as 15%–16%, with approximately 60% of infertility being caused by pelvic infections [3,4]. The role of bacterial vaginosis in the etiology of infertility has been demonstrated in various studies worldwide. In a review of infertile patients in Nigeria [5], bacterial vaginosis was observed in 35.3% of cases; a similar review in Egypt [6] noted a prevalence of bacterial vaginosis of 36.6%. By contrast, a prevalence of 8.6% was observed in the Netherlands [7], giving credence to the notion that the occurrence of bacterial vaginosis varies by geographical location. The organism Lactobacillus is the main contributor to vaginal acidity and prevents the growth of pathologic organisms in the vagina. Bacterial vaginosis occurs when the number of lactobacilli is reduced, the pH rises, and the number of pathogenic bacteria increases. These potential
43 44 45 46 47 48 49 50 51 52 53
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41 42
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39 40
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34
37 38
15 16 17 18 19 20 21 22 23 24 25 26 27 28 29
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1
⁎ Corresponding author at: Department of Obstetrics and Gynaecology, University of Port Harcourt Teaching Hospital, Port Harcourt, Rivers State, 500001, Nigeria. Tel.: +234 8037109486. E-mail address: [email protected] (T.K. Nyengidiki).
pathogens include Gardnerella vaginalis, Bacteroides spp., Escherichia coli, group B streptococci, and the anaerobes Peptostreptococcus and Mycoplasma hominis. The anaerobic organisms and G. vaginalis are thought to act synergistically to cause vaginal infection. Anukam et al. [8] also observed the polymicrobial nature of bacterial vaginosis among Nigerian women. Bacterial vaginosis is characterized by a creamy vaginal discharge that is homogenous, is adherent to the vaginal wall, and has a fishy smell, without extensive evidence of inflammation. It is thought to lead to infertility because the natural defense mechanisms of the vagina are disturbed, leading to the spread of infectious agents toward the upper genital tract and resulting in tubal damage, blockage, or tubal motility disorder [9,10]. There is paucity of data in Nigeria concerning the actual contribution of bacterial vaginosis to the tubal component of infertility. The present study therefore sought to determine the prevalence of bacterial vaginosis and the predisposing factors among women with tubal factor infertility in Nigeria.
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2. Materials and methods
72
A cross-sessional prospective study was undertaken at the University of Port Harcourt Teaching Hospital in Port Harcourt, Nigeria, between March 3 and September 30, 2014. All consecutive women with tubal factor infertility who presented for follow-up at the gynecology clinic were recruited. Women with tubal factor infertility had been previously
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http://dx.doi.org/10.1016/j.ijgo.2015.05.031 0020-7292/© 2015 Published by Elsevier Ireland Ltd. on behalf of International Federation of Gynecology and Obstetrics.
Please cite this article as: Durugbo I, et al, Bacterial vaginosis among women with tubal factor infertility in Nigeria, Int J Gynecol Obstet (2015), http://dx.doi.org/10.1016/j.ijgo.2015.05.031
56 57 58 59 60 61 62 63 64 65 66 67 68 69 70 71
75 76 77
103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130 131
135 136 137 138 139 140 141
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101 102
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99 100
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97 98
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95 96
O
93 94
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91 92
N
89 90
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87 88
Age, y b20 20–24 25–29 30–34 ≥35 Educational status None Primary Secondary Tertiary Social classb Low (IV, V)c Middle (III) High (I, II)
t1:3
BV (n = 50)
No BV (n = 128)
BV (n = 14)
No BV (n = 164)
t1:4
0 6 (12.0) 22 (44.0) 19 (38.0) 3 (6.0)
0 14 (10.9) 55 (43.0) 41 (32.0) 18 (14.1)
1 (7.1) 1 (7.1) 5 (35.7) 4 (28.6) 3 (21.5)
5 (3.0) 19 (11.6) 61 (37.2) 56 (34.1) 23 (14.0)
0 38 (76.0) 8 (16.0) 4 (8.0)
0 17 (13.3) 59 (46.1) 52 (40.6)
0 9 (64.3) 3 (21.4) 2 (14.3)
0 31 (18.9) 84 (51.2) 49 (29.9)
8 (57.1) 4 (28.6) 2 (14.3)
23 (14.0) 99 (60.4) 42 (25.6)
35 (70.0) 12 (24.0) 3 (6.0)
F
A total of 178 women with tubal factor infertility were recruited. Bacterial vaginosis was recorded among 50 (28.1%) of these women, compared with 14 (7.9%) of the 178 fertile women recruited as controls (χ2 = 24.69, P b 0.001). Table 1 shows sociodemographic characteristics of women with and without bacterial vaginosis. The mean age of the women with tubal factor infertility was 28 ± 5 years (range 22–36). Table 2 shows the analysis of risk factors for bacterial vaginosis. Vaginal douching and use of vaginal tightening and drying products
85 86
Fertile women (control group)
O
134
84
Women with tubal infertility
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3. Results
82 83
Variable
21 (16.4) 61 (47.7) 46 (35.9)
t1:5 t1:6 t1:7 t1:8 t1:9 t1:10 t1:11 t1:12 t1:13 t1:14 t1:15 t1:16 t1:17 t1:18 t1:19
Abbreviation: BV, bacterial vaginosis. a Values are given as number (percentage). b Age and education level were used to compute the social class of participants and thus it was not necessary to perform a statistical analysis on these variables. c BV was significantly more likely among women with tubal infertility who were of low socioeconomic class than among those who were of middle or high socioeconomic class 2 (χ = 47.89, P b 0.001; odds ratio 11.89, 95% confidence interval 5.20-27.69).
t1:20 t1:21 t1:22 t1:23 t1:24 t1:25 t1:26
were significantly associated with bacterial vaginosis among women with tubal factor infertility (P b 0.001 for both). In this population, a young age at sexual debut and a history of STIs were also both significantly associated with bacterial vaginosis (P b 0.001 for both). Only having had one sexual partner was a protective factor, reducing the likelihood of bacterial vaginosis among women with tubal factor infertility (P b 0.001). Smoking was not found to be associated with bacterial vaginosis in this population. Similar findings were recorded among fertile women (Table 2). Few women with tubal factor infertility were aware of bacterial vaginosis, irrespective of whether they had the condition (Table 3). Two (8.3%) of the 24 women with tubal factor infertility who were aware of bacterial vaginosis knew that bacterial vaginosis is a risk factor for tubal factor infertility. No woman was aware that bacterial vaginosis is a risk factor for premature rupture of fetal membranes and preterm delivery.
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4. Discussion
158
In the present study, the prevalence of bacterial vaginosis among women with tubal factor infertility was 28.1%. As among fertile women, vaginal douching, the use of vaginal tightening or drying products, early age at sexual debut, a high number of sexual partners, and history of STIs were associated with bacterial vaginosis. The prevalence of bacterial vaginosis among women with tubal factor infertility in the present study is higher than the prevalence of 12%–12.9% noted among women attending infertility clinics in Rwanda [14] and Mozambique [15]. The high prevalence noted in the present study could be attributed to the fact that the women in the present study constituted a highly selected population compared with more generalized samples of infertile patients in the Rwandan and Mozambican studies. A metaanalysis by van Oostrum et al. [9] showed that the prevalence of bacterial vaginosis was higher among women with tubal factor infertility than among women with infertility due to other causes of infertility, even though most studies reviewed failed to establish causal relationships between bacterial vaginosis and tubal infertility. Patients of a lower socioeconomic class had an increased risk of bacterial vaginosis in the present survey. In studies from the USA [16] and Bangladesh [17], a lower socioeconomic class has been associated with poor health-seeking behavior and a higher risk of STIs, which in turn
159 160
P
133
80 81
t1:1 t1:2
Table 1 Sociodemographic characteristics, by presence of BV.a
T
132
diagnosed by hysterosalpingography. Women were excluded if they had received metronidazole or clindamycin for a disease or condition other than bacterial vaginosis within the previous 90 days, irrespective of the route of administration; had experienced vaginal bleeding; had infertility due to causes other than tubal factors; or had undergone bilateral salpingectomy. An equal number of fertile women attending the family planning clinic were also recruited as controls. Ethics clearance for the present study was obtained from the Ethics Review Committee of the teaching hospital. All participants provided informed consent. Each patient was interviewed using a structured study form that was completed by the interviewers. Information about age, tribe, occupation, level of education, husband’s occupation, and parity was obtained. The social class of each participant was determined on the basis of the woman’s educational status and her husband’s occupation, as proposed by Olusanya et al. [11]. Other collected information included the history of abnormal vaginal discharge, practice of vaginal douching, use of vaginal tightening or drying products, and age of sexual debut. The number of lifetime sexual partners, history of sexually transmitted infections (STIs), and history of smoking were also ascertained. After the interview, each participant underwent a procedure to obtain a vaginal sample in the presence of a female assistant, who also served as a chaperone. The patient was placed in a dorsal position on an examination table. Guided by an angle point light, a bivalve speculum was introduced into the vagina (without lubrication). A wooden spatula was used to take a sample of the vaginal discharge/secretion from the vaginal walls and the posterior vaginal fornix. The vaginal discharge or secretion was then assessed on the basis of the Amsel criteria [12]. Initially, three of the criteria were assessed. The discharge/secretion was examined visually to establish whether it was characteristic of bacterial vaginosis (homogenous and creamy). The pH value of the vaginal fluid was then determined with a pH meter, after adding 1 mL of normal saline to the collected vaginal secretion in a sterile test tube and mixing it thoroughly. A vaginal fluid pH of more than 4.5 is indicative of bacterial vaginosis. Thereafter, a drop of the solution was placed on a clean glass slide and one drop of 10% potassium hydroxide in aqueous solution was added to it. The slide was then smelt to determine whether the mixture had a fishy odor (“whiff test”). This odor, when present, is strongly suggestive of bacterial vaginosis. For participants with at least two positive results for these three assessments, a microscopic examination of the prepared slide was then performed to determine whether “clue cells” were present (fourth Amsel criterion). The diagnosis of bacterial vaginosis was confirmed if more than 20% of the epithelial cells had adherent bacteria. The sample size was determined using a formula proposed by Kish for the estimation of single proportions [13]. The minimum sample size was calculated to be 162. Allowing for an attrition of 10% (i.e. 16 women), 178 women with tubal factor infertility were recruited. The data were analyzed using SPSS version 20.0 (IBM, Amonk, NY, USA) and Epi Info version 7.0 (Centers for Disease Control and Prevention, Atlanta, GA, USA). Frequency tables were generated and the results were tested for significance using the Student t test and the χ2 test. P b 0.05 was considered statistically significant. An assessment of the risk factors for bacterial vaginosis among patients with tubal infertility and among control individuals was estimated by calculating odds ratios (ORs) with 95% confidence intervals (CIs).
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Please cite this article as: Durugbo I, et al, Bacterial vaginosis among women with tubal factor infertility in Nigeria, Int J Gynecol Obstet (2015), http://dx.doi.org/10.1016/j.ijgo.2015.05.031
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161 162 163 164 165 166 167 168 169 170 171 172 173 174 175 176 177 178 179
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Women with tubal factor infertility
20 (15.6) 108 (84.4)
41 (82.0) 9 (18.0)
27 (21.1) 101(78.9)
5 (10.0) 45 (90.0)
12 (9.4) 116 (90.6)
42 (84.0) 8 (16.0)
18 (14.1) 110 (85.9)
10 (20.0) 40 (80.0)
106 (82.8) 22 (17.2)
38 (76.0) 12 (24.0)
26 (20.3) 102 (79.7)
OR (95% CI)
b0.001
19.15 (7.26–47.75)
b0.001
0.889
b0.001
b0.001
b0.001
increase the risk of tubal factor infertility. The poor health-seeking behavior among this group means that any bacterial vaginosis goes untreated, hence creating the necessary milieu for ascending organisms to cause tubal damage. Vaginal douching, which women in Nigeria practice for various reasons, contributed significantly to the development of bacterial vaginosis. This is in agreement with the findings of a previous study [18], in which vaginal douching was identified as the greatest predictor of bacterial vaginosis. A study by Hutchinson et al. [16] demonstrated a 5.1fold increase in the risk of bacterial vaginosis with vaginal douching, which is far lower than the 19-fold increase among women with tubal factor infertility that was observed in the present study. The wide disparity in the risk between the two study populations could be because the present study included only patients with tubal factor infertility, who have been shown during epidemiological studies to have an increased incidence of bacterial vaginosis and pelvic inflammatory disease [19]. Despite being discouraged, vaginal douching is still a common practice in Nigeria, and is used by women and girls to “clean” the vagina for hygienic purposes to remove odor during or after menses and to prevent STIs. The use of vaginal tightening or drying products increased the risk of bacterial vaginosis 17 times in the present population. Other researchers have observed similar results. In a survey of 250 women in the USA, Schwebke et al. [20] identified a 5.11-fold increase in the risk of developing vaginal vaginosis among women who douche for the purpose of vaginal tightening. The reason for the use of tightening or drying products is essentially a cultural preference for a dry vagina to improve sexual satisfaction, but these agents disrupt the normal bacterial flora [21]. Similarly, the distortion of the vaginal flora not only decreases the lactobacilli population but also encourages the growth of pathogenic strains of bacteria that are responsible for tubal damage [10].
194 195 196 197 198 199 200 201 202 203 204 205 206 207 208 209 210
t3:1 t3:2
C
E
R
193
R
191 192
N C O
189 190
U
187 188
T
180
185 186
Table 3 Awareness of BV and its associated risks among patients with tubal factor infertility.a
t3:3
Awareness
BV (n = 50)
No BV (n = 128)
P value
Odds ratio (95% CI)
t3:4 t3:5
Aware Unaware
6 (12.0) 44 (88.0)
18 (14.1) 110 (85.9)
0.71
0.83 (0.27–2.42)
t3:6 t3:7
Abbreviations: BV, bacterial vaginosis; CI, confidence interval. a Values are given as number (percentage) unless indicated otherwise.
12 (85.7) 2 (14.3)
39 (23.8) 125 (76.2)
11 (78.6) 3 (21.4)
45 (27.4) 119 (72.6)
2 (14.3) 12 (85.7)
19 (11.6) 145 (88.4)
10 (71.4) 4 (28.6)
34 (20.7) 130 (79.3)
17.04 (6.91–43.24)
P value
OR (95% CI)
b0.001
19.23 (3.82–130.43)
b0.001
9.70 (2.35–46.15)
1.07 (0.31–3.54)
0.511
32.08 (12.02–88.89)
0.05 (0.02–0.13)
12.42 (5.36–29.35)
11 (78.6) 3 (21.4)
Abbreviations: BV, bacterial vaginosis; OR, odds ratio; CI, confidence interval. a Values are given as number (percentage) unless indicated otherwise.
183 184
No BV (n = 164)
2 (14.3) 12 (85.7)
t2:24 t2:25
181 182
BV (n = 14)
1.27 (0.00–6.75)
b0.001
9.56 (2.54–38.92)
b0.001
0.04 (0.01–0.18)
b0.001
21.39 (4.99–105.30)
F
39 (78.0) 11 (22.0)
Fertile women (control group)
P value
O
Vaginal douching Yes No Use of vaginal tightening and drying products Yes No Smoking Yes No Age at sexual debut, y ≤15 N15 Number of lifetime sexual partners 1 ≥2 History of sexually transmitted infection Yes No
No BV (n = 128)
R O
t2:6 t2:7 t2:8 t2:9 t2:10 t2:11 t2:12 t2:13 t2:14 t2:15 t2:16 t2:17 t2:18 t2:19 t2:20 t2:21 t2:22 t2:23
BV (n = 50)
135 (82.3) 29 (17.7) 24 (14.6) 140 (85.4)
P
Variable
t2:4 t2:5
Investigators differ in their opinion on the effect of smoking on the risk of bacterial vaginosis [22,23]. In the present survey, smoking was not a significant risk factor for the development of bacterial vaginosis. Cultural restrictions preventing women from smoking in the present environment could have highly reduced the contributory influence of smoking among the group with tubal factor infertility. Ness et al. [22] identified smoking as a marker of sexual behavior, because women who were smokers had more lifetime sexual partners than nonsmokers did and were thus at risk of pelvic inflammatory disease, a known cause of tubal infertility. In the present study, however, the number of lifetime partners was noted to be related to the occurrence of bacterial vaginosis: having only one sexual partner significantly reduced the risk of bacterial vaginosis. This gives credence to the fact that the frequency of intercourse increases with the number of partners, which changes the vaginal environment for the occurrence of bacterial vaginosis. Sexual debut before the age of 15 years was observed to significantly increase the risk of bacterial vaginosis. Early initiation of sexual intercourse as a contributory factor to bacterial vaginosis has also been noted in other studies [24,25]. The increase in risk associated with an early sexual debut was more than three times higher among women with tubal factor infertility than among control women in the present study. Initiation of intercourse before puberty—mean age at puberty in Nigeria is 15.26 years [26]—during a period of low lactobacilli colonization therefore increases the risk of bacterial vaginosis and also the rate of tubal infertility. However, it should noted that bacterial vaginosis has also been found in virgins, implicating other risk factors that are not related to intercourse [27]. In line with the findings of Vaca et al. [27], the present study also revealed a strong association between a history of STIs and bacterial vaginosis. Bacterial vaginosis renders women vulnerable to STIs and consequent pelvic inflammatory disease, tubal blockage, and infertility [28]. The level of awareness of bacterial vaginosis and its associated complications among the participants was surprisingly low among women with tubal factor infertility. Poor awareness was exhibited by women across all levels of education and occupation irrespective of bacterial vaginosis status. This finding supports the theory that the high prevalence of bacterial vaginosis is not driven by a lack of awareness but by high-risk behaviors. The present study was limited by the fact that the study population was hospital-based and the result might not necessarily be applicable to the whole population. Hence, community-based prevalence studies are
D
t2:3
Table 2 Risk factors for BV.a
E
t2:1 t2:2
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Please cite this article as: Durugbo I, et al, Bacterial vaginosis among women with tubal factor infertility in Nigeria, Int J Gynecol Obstet (2015), http://dx.doi.org/10.1016/j.ijgo.2015.05.031
211 212 213 214 215 216 217 218 219 220 221 222 223 224 225 226 227 228 229 230 231 232 233 234 235 236 237 238 239 240 241 242 243 244 245 246 247 248 249 250 251
275 276 277 278
281 282 283 284 285 286 287 288 289 290 291 292 293 294 295 296 297 298 299 360
The authors have no conflicts of interest.
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T
273 274
References
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Conflict of interest
256 257
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advocated. Tubal blockage was diagnosed by hysterosalpingography as opposed to a laparoscopy and dye test, which is the recommended gold standard method of diagnosis. However, financial, equipment, and expertise challenges in the present environment made this diagnostic modality the only realistic method. The high prevalence of bacterial vaginosis among women with tubal factor infertility in the present study should be a wake-up call to clinicians to adopt strategies to reduce its prevalence. It is also an indication that there is a potentially large number of women with bacterial vaginosis in Nigeria who remain undiagnosed because of its largely asymptomatic nature. The contribution of certain socioeconomic factors and cultural practices—e.g. poverty, vaginal douching, application of vaginal tightening agents, and early sexual debut—to the risk of bacterial vaginosis cannot be overemphasized. On the basis of the present findings, women with tubal factor infertility should be routinely screened for bacterial vaginosis, and offered counseling and treatment when necessary. This will help to prevent some of the health consequences of bacterial vaginosis, especially when these women eventually become pregnant. The government should ensure improvements in the education for girls and women and in the overall welfare of citizens in a bid to improve women’s socioeconomic status. Efforts should be made to enlighten girls and women on the need to avoid the risk factors that predispose them to bacterial vaginosis. Girls and women should also be encouraged to improve their health-seeking behavior, because this will enhance the early identification, treatment, and prevention of bacterial vaginosis. There is an urgent need to raise the public health profile of bacterial vaginosis in relation to tubal infertility in Nigeria.
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Please cite this article as: Durugbo I, et al, Bacterial vaginosis among women with tubal factor infertility in Nigeria, Int J Gynecol Obstet (2015), http://dx.doi.org/10.1016/j.ijgo.2015.05.031
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