Risk factors of recurrent bacterial vaginosis among women of reproductive age: A cross-sectional study

Abstract

Background: Bacterial vaginosis (BV) is the most common cause of vaginitis and is associated with an increased risk of health problems. Our study aims to explore risk factors of recurrent BV (RBV) among women of reproductive age and offer references for clinical prevention and treatment of BV.

Methods: This cross-sectional study was carried out in Gynecology Outpatient Clinic of the First Affiliated Hospital of Xi’an Jiaotong University from June 2016 to June 2019 in real-world conditions. Women with RBV were selected，and simultaneously uncomplicated BV (UBV) patients and those who underwent routine gynecological examination and had normal vaginal microflora (NVM) were also recruited as the control. We conducted a face-to-face questionnaire survey and a multivariate logistic regression analysis to uncover the related risk factors of RBV and UBV.

Results: Totally, 316 participants were enrolled in the present study, including 68 RBV patients, 135 UBV patients and 113 NVM women. Univariate analysis showed that unemployment, desserts and wiping were the risk factors for UBV (P2<0.05), while education, high BMI index, smoking and sedentary lifestyle were risk factors for both RBV and UBV (P1<0.05). In addition, history of HPV infection, contraceptive methods, age at FSI and not cleaning vulva during sexual actvity were the risk factors for UBV (P2<0.05), while history of other vaginitis and number of sexual partners in the previous year were risk factors for both RBV and UBV (P1<0.05). Multivariate Logistic regression analysis revealed that lower educational level increased the risk of suffering RBV (OR =2.842, 95% CI = 1.177-6.859, P =0.020). Interestingly, no smoking was a protective factor (OR =0.371, 95% CI = 0.152-0.885, P =0.026). Moreover, absence of other vaginitis and exclusive sexual partner could also weaken the risk of incurring RBV. However, there was no statistical difference between non-sedentary lifestyle, BMI and RBV.

Conclusions: Risk factors of RBV are various, involving women's socioeconomic status, hygienic habits, disease history and other aspects. It is necessary to take corresponding measures to avoid risk factors and to help lessening the prevalence of RBV among women of reproductive age.

This study was registered in the Thai Clinical Trials Registry (www.clinicaltrials.in.th) on 24 February 2018, and the registered number was, TCTR20180223002, retrospectively registered

Plain Language Summary

Among various vaginitis, bacterial vaginosis (BV) is the most common one. Recurrent BV (RBV) causes great physical and psychosocial impacts on women. Thus, the aim of this present cross-sectional study is to exploring risk factors of RBV among women of reproductive age. To achieve it, a face-to-face questionnaire survey and the multivariate logistic regression analysis were used to uncover the related risk.

Eventually, 316 participants were enrolled in the present study, including 68 RBV patients, 135 UBV patients and 113 healthy women. The results showed education, high BMI index, smoking and sedentary lifestyle were risk factors for both RBV. In addition, history of other vaginitis and number of sexual partners in the previous year were risk factors for both RBV. Multivariate Logistic regression analysis revealed that lower educational level and smoking increased the risk of suffering RBV. Moreover, absence of other vaginitis and exclusive sexual partner could also weaken the risk of incurring RBV. However, there was no statistical difference between non-sedentary lifestyle, BMI and RBV. 

In conclusion, lower educational level and smoking were the risk factors for RBV. While, absence of other vaginitis and exclusive sexual partner weaken the risk of suffering RBV.

Background

Bacterial vaginosis (BV) is the most common vaginal inflammatory disease, which frequently occurs in women of childbearing age. BV is considered to be a disorder of vaginal microbiota characterized by a shift from the Lactobacillus-dominant vaginal microbiota to the anaerobes and facultative anaerobes, including Gardnerella vaginalis, Atopobium vaginae, Mobiluncus curtisii and Mycoplasma hominis. Clinically, BV can be diagnosed by satisfying three out of the four characteristics which include white discharge (thin, homogenous, uniformly adherent), vaginal pH > 4.5, fishy odor on addition of 10% potassium hydroxide and 20% clue cells in vaginal smear microscopy. However, the definition of recurrent BV (RBV) is still not widely accepted, yet generally it is defined as a confirmed diagnosis of BV three or more times within the same year[1].

BV causes thorny public health problems as it increases the risk of health sequelae, especially for childbearing women, their offspring as well as their sexual partners. The adverse concerns include severe reproductive tract infection, abortion, premature birth, premature rupture of membranes, low birth weight infant, neonatal infection, sexually transmitted diseases, cervical lesions, etc.[2–5]. In addition, BV seriously affects the socioeconomic status and quality of life of patients. What's worse, with the potential to easily cause anxiety and depression, RBV heavily affects women's work and life[6]. Recent estimates suggest a 30% prevalence of BV among reproductive women globally[6, 7]. While variations in prevalence exist among different races and ethnicities. For example, the rate in sub-Saharan Africa may exceed 50%[8].

Unfortunately, although short-term cure rates are generally comparable, approximately 80–90%, in 3 to 4 weeks after receiving currently guideline-recommended treatments, yet more than 50% of women recur within a year or even within 6 months. Nevertheless, the possible mechanism of RBV has not been fully demonstrated. Although the majority of patients with BV can be treated effectively with antibiotics[9, 10]. What’s worse, recent study validated that standard of care of oral metronidazole has poor efficacy among recurrent, showing alarming 76% refractory or recurrent responses[11].

RBV has significant psychosocial impacts on women, including severely affecting self-esteem and sex life, and carries a high economic burden[6]. Needless to say, RBV is the source of considerable frustration to both practitioners and patients[6]. The frustration expressed by the unfortunate patients remains enormous.

Considering the morbidity of BV and a series of economic, psychological and social burdens caused by BV, it is urgent to explore new strategies to settle plight. Naturally, etiological prevention is the fundamental approach to decrease the high morbidity and recurrent rate of BV. Therefore, this study aims at screening the risk factors of RBV and UBV among women of reproductive age expecting to offer reference for clinical prevention and treatment.

Materials And Methods

Participants

According to the Strobe guidelines, we carried out this cross-sectional study in Gynecology Outpatient Clinic of the First Affiliated Hospital of Xi'an Jiaotong University from June 2016 to June 2019. Inclusion criteria: (1) women who were 18-50 years old with a history of sexual life; (2) women who had a normal vaginal microflora (NVM) or were diagnosed with UBV, RBV; (3) women whose menstruation lasts for at least 3 days, no vaginal irrigation or drug delivery in the vagina within 7 days and no sexual intercourse within 3 days before examination. Exclusion criteria[12]. Women who were in the period of pregnancy, menstruation or lactation; women who had hysterectomy or bilateral salpingo-oophorectomy. Besides, patients with incomplete medical records were also excluded. Then, all women with RBV were included in this present study, at the same time women with UBV and NVM were also enrolled at a ratio of 1:2. After obtaining each interviewee’s written informed consent, we conducted a face-to-face questionnaire survey of the three groups and analyzed the risk factors of RBV. The study protocol was performed with approval of the ethics committee of the First Affiliated Hospital of Xi’an Jiaotong University.  

Diagnostic criteria

BV could be diagnosed using either the Nugent score or the modified Amsel standard regardless of clinical symptoms given the high prevalence of asymptomatic BV. The prevalence of BV was 29% among women at the age of 15 to 49 when diagnosed by the Nugent score, but only 15.7% of the women had clinical symptoms [13]. While A survey amongst 255 African women found that the prevalence of BV was as high as 95% by the Nugent score during 2 years of follow-up, but there existed no association between BV and clinical symptoms [14]. In this study, BV was diagnosed by the Nugent score. Vaginal smears were Gram stained and then evaluated under oil immersion (×1000 magnification) by a single reader and scored using the Nugent scoring criteria (Table 1). Women who had a score of 7 or above was graded as BV. Certainly, a score of 4–6 was graded as intermediate BV, and a Nugent score of 0–3 was graded as a normal vaginal microflora (NVM). All the vaginal smears were reevaluated by a second microscopist who was blind to the initial results. If the score differed by more than 2 or resulted in a change in Nugent category (eg, from NVM to intermediate BV, then a third reader who was blind to the preceding results was invited to evaluate the smear. At the same time, a meeting was arranged among these three readers to reach a final consensus on any controversial smears. RBV is defined as a confirmed diagnosis of BV three or more times within the same year.  Refractory patients were defined as women with persistent BV at the first follow-up visit occurring within 30 days of initiating therapy. 

Sampling and tests[12]

The patient was in the bladder lithotomic position. One researcher put a speculum lubricated by saline into the vagina, swabbed a bit of vaginal secretion from the posterior fornix by a dry cotton, coated it on the slide from left to right evenly and put the cotton swab into a clean tube with little saline. Then, the researcher scraped vaginal secretion from the same place by another dry cotton and put the cotton swab into a clean dry tube. The sample was tested by laboratory technicians within 30 minutes. All the samples were collected by the same researcher and tested by two experienced inspectors at the same time. If the results of the two inspectors were inconsistent, we resorted to a third veteran for the final diagnosis.  

Investigation of risk factors

Based on the epidemiological principle, we designed a structured questionnaire survey. Recently, the emerging advancement of molecular and high-throughput sequencing technologies [e.g., next-generation sequencing (NGS)] has revealed that BV is a multifactorial condition influenced by social, epidemiological, microbiological and host factors[15]. The survey contains demographic data, such as age, address, profession, education and body mass index (BMI); living habits such as eating sweets, desserts, smoking and physical exercise state; hygienic habits such as menstrual care, bath way, underwear material and the forward direction of wiping (forward wiping); previous history such as history of human papillomavirus (HPV) infection, history of other vaginitis and reproductive history; sexual behavior such as contraceptive methods, the age at first sexual intercourse (FSI), the number of sexual partners in the last year and frequency of sexual life. Each eligible interviewee was surveyed individually in view of privacy-protection by a trained interviewer. Data on the target factors were collected by two researchers separately. Participants were classified by BMI based on National Institutes of Health and World Health Organization recommendations: underweight (<18.5 kg/m ²), lean (18.5~24.9 kg/m ²), overweight (25~29.9 kg/m ²), and obese (>30 kg/m ²).  

Statistical analysis[12]

All statistical analyses were performed with SPSS version 20.0 and P<0.05 was considered to be of great statistical difference. Univariate analysis was used to calculate crude odds ratios (OR) and 95% confidence intervals (CI). A multiple logistic regression model was used to control confounding factors and to determine which factor still remained statistically significant. Only the factor with great statistical difference between RBV and BV after univariate analysis was entered into the multivariate Logistic regression analysis.

Results

Demographic characteristics

Totally, 316 participants were included in this study under the inclusion and exclusion criteria, including 68 RBV patients, 135 UBV patients and 113 NVM women. They were at the age of 18-50 and had a regular menstruation. Among women with RBV，45.58% (31/68) had vulva pruritus, 16.17% (11/68) vulva discomfort, 27.94 (19/68) manifested yellow leucorrhea and 7.35% (5/68) showed odor leucorrhea. Among women with UBV, 28.89% (39/135) of them had vulva pruritus, 28.15% (38/135) presented vulva discomfort, 31.11% (42/135) manifested yellow leucorrhea and 11.85% (16/135) showed odor leucorrhea. While amongst women with NVM, 10.62% (12/113) of women came to see a doctor for routine gynecological examinations, 62.83% (71/113) had vulva pruritus, 7.96% (9/113) presented vulva discomfort, 18.58% (21/113) had the symptom of yellow leucorrhea. Majority of the enrolled women (258/316, 81.65%) were less than 45 years old and 58/316 (18.35%) were above the age of 45. There were 126/316 (39.87%) women from rural areas and 190/316 (60.13%) women from urban areas, respectively.  

Association of RBV with socio-economic factors and hygienic habits

Univariate analysis showed that unemployment, low educational level (secondary or below), high BMI value, frequent smoking, desserts, sedentary lifestyle, forward wiping were risk factors for BV, no matter RBV or UBV, with great statistical differences (P3<0.05) (see in Table 2). Careful screening showed unemployment, desserts and wiping were the risk factors for UBV (P2<0.05), but not for RBV, while education, BMI index, smoking and sedentary lifestyle were risk factors for both RBV and UBV (P1<0.05). 

Association of RBV with previous history, reproductive history and sexual behaviors

Univariate analysis indicated that history of other vaginitis, history of HPV infection, nonutility of condoms, age at FSI, number of sexual partners in the last year, and not cleaning vulva before or after sexual life were risk factors for BV with great statistical differences (P3<0.05) (see in Table 3). Rigorous analysis showed history of HPV infection, contraceptive methods, age at FSI and not cleaning vulva before or after sexual life were the risk factors for UBV (P2<0.05), but not for RBV, while history of other vaginitis and number of sexual partners in the last year were risk factors for both RBV and UBV (P1<0.05).

Multivariate Logistic regression analysis

Backward stepwise regression was used to assess multivariable effects on RBV. Multivariate Logistic regression analysis revealed that lower educational level increased the risk of suffering RBV (OR =2.842, 95% CI = 1.177-6.859, P =0.020). Interestingly, no smoking was a protective factor (OR =0.371, 95% CI = 0.152-0.885, P =0.026). In addition, absence of other vaginitis and exclusive sexual partner could weaken the risk of incurring RBV. However, there was no statistical difference between non-sedentary lifestyle, BMI and RBV (see in Table 4). 

Discussion

In women of childbearing age, BV is the most common vaginal infection and occurs in up to 70% of women. Globally, the prevalence of BV varies considerably between countries, regions, races and ethnic groups. Although antibiotics are recommended as the first-line therapy, 20–30% of women have a recurrence of symptoms after completing the first round of treatment.[16]

Univariate analysis showed that the unemployment and a low educational degree were risk factors for UBV, and particularly, lower educational level was a risk factor for RBV (P1 = 0.0024). The great statistical difference still exited under multivariate logistic regression analysis (P = 0.020). Certain studies have believed that the prevalence of lower reproductive tract infections was higher among people with lower socioeconomic status and lower educational background. An epidemiological study in Brazil also argued that high income was a protective factor for BV [17]. This may be due to women with high socioeconomic status and high educational level have more opportunities to gain a knowledge of preventing BV and other vaginal infectious diseases. Therefore, they could avoid the occurrence of BV effectively. However, there was a lack of clear relationship between BV and patients' age or setting.

Univariate analysis showed that the smoking was a risk factor for RBV(P1 = 0.0303), and the great statistical difference still exited under multivariate logistic regression analysis (P = 0.026). Our results were in accordance with previous literature stating there was a higher number of women who were diagnosed with BV and had smoking habits[18]. This finding could be interpreted as that smoking promotes an antiestrogen environment and elevates vaginal amines, which predisposes women to BV[19]. Besides, tobacco is thought to alter the physiology and structure of the flora of the vagina, increasing bacterial virulence. A previous study found that compared with lean women, overweight and obese women had a higher frequency of BV[20]. While our result revealed that BMI was statistically different among women with RBV, UBV and NVM(P3 = 0.014). While this difference faded away under multivariate analysis.

This was the first time to take diet and sedentary life style into consideration when analyzing the risk factors of BV. Univariate analysis revealed frequent desserts and a sedentary lifestyle were risk factors for BV, and particularly, a sedentary lifestyle was a risk factor for RBV (P1 = 0.0364). While this great statistical difference disappeared under the multivariate logistic regression analysis (P = 0.078). The fact that the anus is close to the vagina anatomically providing much convenience for the migration of gut organisms to the vagina. It is hypothesized that overeating desserts and sweets may disrupt intestinal microflora, leading to the imbalance of vaginal microflora, resulting in becoming chief culprit of RBV. Moreover, a sedentary lifestyle is not beneficial to enhancing the body's immunity, leaving the body a weakened protective immunity, recalcitrance to overgrown anaerobes and the hotbed of RBV.

Besides, this study found no statistical relationship between RBV and the menstruation care, underwear materials, frequency of underwear replacement and bath way. A longitudinal study in Britain also found no significant difference between BV and underwear material and menstrual pads[21]. While backward wiping was a protective factor for UBV, which has never been studied before. The reason may be attributed to the fact that the intestinal microflora on the contaminated toilet paper could pollute the vulva and then disturb the vaginal microflora.

This study hinted that history of other vaginitis and history of HPV infection were risk factors for UBV, consistent with another study which showed that women with BV were twice as likely to acquire trichomonal vaginitis compared with women without BV.[22] Specially, when it comes to history of other vaginitis, there existed a significant statistical difference (P1 = 0.0088). Reproductive history and menstrual cycle had little effect on UBV, but one study found luteal phase to be a protective factor of BV [17]. Many studies hold that use of intrauterine device (IUD) was a risk factor for BV [23, 24]. This is perhaps because the tail of IUD exposed in cervical vagina and vagina provided colonization conditions for anaerobic bacteria. Other studies suggested that the use of contraceptives was a protective factor for BV [17, 25]. This may due to the fact that estrogen increases epithelial glycogen, which can metabolize into lactic acid, with antimicrobial activity against BV-associated bacteria. In view of the small number of women who used contraceptives conventionally, it was unscientific to conduct an analysis between contraceptives and BV here. Also, a study stated that hormonal contraception and condom use were protective against BV[26].

The present study showed that there was no significant relationship between sexual intercourse during menstruation, the frequency of sexual life and RBV. Univariate analysis showed that the age of FSI less than 20 and not cleaning the vulva during sexual activity were risk factors for UBV, but not for RBV. Although BV is not belonging to sexually transmitted disease, it is really associated with unprotected sexual activity[27]. As what this study showed multiple sexual partners increase susceptibility to both RBV and UBV, which was also manifested in another study[1, 26]

Interpretations of findings of this study are to be extrapolated cautiously because of its limitations. The primary drawback was that the sample size was not large enough and the data on smoking, alcohol consumption, number of sexual partners and sexually transmitted diseases was inadequate. Then, the study population was hospital-based and the result might not necessarily be applicable to the whole population. Therefore, community-based studies are needed. Additionally, all responses received on the baseline questionnaire were self-reported and subject to recall and social desirability bias. Consequently, sexual risk behavior may have been underreported in view of privacy protection. There is also limited generalizability of results since only Chinese women were included in the analysis.

Conclusions

In conclusion, BV poses a great threat to women's reproductive health, emotional burden and economic burden. Risk factors of RBV are various, involving women's hygienic habits, socioeconomic status, disease history and other aspects. Therefore, it is necessary to take corresponding measures, such as improving living conditions, popularization healthy hygienic education, cultivating personal hygienic behavior habits, to strengthen the consciousness of self-protection and avoid risk factors, expecting to help to lessen the prevalence of RBV and then unload psychosocial and economic burden.

Abbreviations

RBV: recurrent bacterial vaginosis; UBV: uncomplicated bacterial vaginosis; NVM: normal vaginal microflora; BMI: body mass index; OR: odds ratios; CI: confidence interval; P1: difference between RBV and UBV; P2: difference between UBV and NVM; P3: difference among RBV: UBV and NVM; OR: odds ratios; CI: confidence interval.

Declarations

Authors’ contributions 

XZ: study design, data management, analysis and manuscript writing. HL: data analysis and manuscript editing. HL and YZ: data collection and management. RA: study design, project development and manuscript editing. All authors read and approved the final manuscript. 

Funding 

This study was supported by Shaanxi Science and Technology Coordinating Innovation Plan (no. 2016KTCL03-06) and the National Natural Science Foundation of China (no. 81671491; no. 81172489).  

Availability of data and materials

All data generated or analyzed are included in this article. 

Ethics approval and consent to participate

All procedures carried out in this study involving all participants were in accordance with the ethical standards of the institutional ethics review board of the First Hospital of Xi’an Jiaotong University and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. The subjects’ rights were adequately protected, and there was no potential risk to the subjects. 

Consent for publication

Not applicable. 

Competing interests

The authors declare that they have no competing interests.

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Tables

Table 1 

Nugent scoring criteria

0 = No morphotypes present; 1+ = <1 morphotype present; 2+ = 1 to 4 morphotypes present; 3+ = 5 to 30 morphotypes present; 4+ = 30 or more morphotypes present.

TABLE 2

Association of RBV with socio-economic factors and hygienic habits

  RBV = recurrent bacterial vaginosis; UBV = uncomplicated bacterial vaginosis; NVM = normal vaginal microflora; BMI = body mass index; OR = odds ratios; CI = confidence interval; P1 = difference between RBV and UBV; P2 = difference between UBV and NVM; P3 = difference among RBV = UBV and NVM; OR = odds ratios; CI = confidence interval.   

TABLE 3

 Association of RBV with previous history, reproductive history and sexual behaviors

 RBV = recurrent bacterial vaginosis; UBV = uncomplicated bacterial vaginosis; NVM = normal vaginal microflora; HPV = human papillomavirus; IUD = intrauterine device; FSI = first sexual intercourse; COC = combined oral contraceptive; *Number of sexual partners in the previous year; ^#Cleaning the vulva during sexual activity; P1 = difference between RBV and UBV; P2 = difference between UBV and NVM; P3 = difference among RBV = UBV and NVM; OR = odds ratios; CI = confidence interval.

TABLE 4

Determinants of RBV in a multivariate multinomial logistic regression analysis

RBV = recurrent bacterial vaginosis; BMI = body mass index; OR = odds ratios; CI = confidence interval.