
==== Front
Sci Rep
Sci Rep
Scientific Reports
2045-2322
Nature Publishing Group UK London

72644
10.1038/s41598-024-72644-0
Article
Prevalence of bacterial vaginosis and its associated factors among pregnant women attending antenatal care clinics at public hospitals in West Shoa Zone, Oromia, Ethiopia
Regassa Belay Tafa belaytf@gmail.com

1
Kumsa Chala 1
Wondimu Fikadu 2
Yilma Shemeket 3
Moreda Ammar Barba 4
Shuulee Abarra Ol’aanaa 1
Wondie Wubet Tazeb 5
Desisa Sileshi Lamesa 6
Debelo Bikila Tefera 2
1 https://ror.org/02e6z0y17 grid.427581.d 0000 0004 0439 588X Department of Medical Laboratory Sciences, College of Health Sciences and Referral Hospital, Ambo University, Ambo, Ethiopia
2 https://ror.org/02e6z0y17 grid.427581.d 0000 0004 0439 588X Department of Midwifery, College of Health Sciences and Referral Hospital, Ambo University, Ambo, Ethiopia
3 https://ror.org/02e6z0y17 grid.427581.d 0000 0004 0439 588X Department of Obstetrics/Gynecology, College of Health Sciences and Referral Hospital, Ambo University, Ambo, Ethiopia
4 https://ror.org/02e6z0y17 grid.427581.d 0000 0004 0439 588X Department of Pediatrics and Child Health, College of Health Sciences and Referral Hospital, Ambo University, Ambo, Ethiopia
5 https://ror.org/02e6z0y17 grid.427581.d 0000 0004 0439 588X Department of Pediatrics and Child Health Nursing, College of Health Sciences and Referral Hospital, Ambo University, Ambo, Ethiopia
6 https://ror.org/02e6z0y17 grid.427581.d 0000 0004 0439 588X Clinical Laboratory Services Unit, Ambo University Referral Hospital, Ambo, Ethiopia
14 9 2024
14 9 2024
2024
14 214748 5 2024
9 9 2024
© The Author(s) 2024
2024
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Bacterial vaginosis is a polymicrobial syndrome characterized by the decrease of Lactobacilli and an overgrowth of facultative and anaerobic bacteria in vaginal fluid. Though it has received little attention, it has been associated with poor pregnancy outcomes, such as pre-term labor and delivery, premature rupture of membranes, low birth weight, spontaneous abortion, and postpartum infections. This study aimed to determine the prevalence of bacterial vaginosis and its associated factors among pregnant women attending antenatal care clinics from September 15 to December 14, 2021, at public hospitals in West Shoa Zone, Oromia, Ethiopia. An institutional-based cross-sectional study was conducted on 260 pregnant women, and systematic random sampling was employed to recruit the study participants. Data were collected through a structured questionnaire and the vaginal swab was collected using a sterile cotton swab. The gram staining result was interpreted using the Nugent scoring system. Data was entered into an Excel spreadsheet and exported to STATA-14 for analysis. Data were presented using tables and graphs. Binary and multivariable logistic regressions were performed. Variables with a P value ≤ 0.25 at the binary logistic regression were entered into the multivariable logistic regression. Finally, variables with a P value ≤ 0.05 were considered predictors of bacterial vaginosis and interpreted using adjusted Odds Ratios (AOR) with a 95% confidence interval (CI). A total of 260 pregnant women attending antenatal care were included in the study. The prevalence of bacterial vaginosis according to the Nugent scoring system was 22.3% (95% CI 17.4 to 27.9%). Pregnant women with other marital status were at reduced risk of bacterial vaginosis as compared with married pregnant women (AOR = 0.260, 95% CI 0.068 to 0.9995; P = 0.05). Rural residence (AOR = 2.1, 95% CI 1.05 to 4.24; P = 0.036), use of one pant per week (AOR = 2.7, 95% CI 1.04 to 7.2; P = 0.041), and use of two or more pants per week (AOR = 4.96, 95% CI 1.49 to 16.57; P = 0.009) were significantly associated with bacterial vaginosis. In the current study, a high magnitude of bacterial vaginosis was reported. Residence, marital status, and number of pants used per week were found significantly associated among pregnant women. Hence, screening for the disease should be integrated into the recommended basic laboratory investigations during antenatal visits.

Keywords

Antenatal care
Associated factors
Bacterial vaginosis
Pregnant women
Subject terms

Microbiology
Diseases
Health care
Medical research
Risk factors
http://dx.doi.org/10.13039/501100016392 Ambo University issue-copyright-statement© Springer Nature Limited 2024
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pmcIntroduction

Bacterial vaginosis is a polymicrobial syndrome where the complex balance of microflora in the vagina is changed. There is a depletion of Lactobacilli and an overgrowth of facultative and anaerobic bacteria either singly or in combination. These bacteria include Gardnerella vaginalis, Bacteroides fragilis, Mobiluncus species, and many more others. This list continues to expand, and the specific causes of bacterial vaginosis are poorly understood1,2. It is an extremely common reproductive tract disorder worldwide accounting for one-third of vaginal infections3. It can occur in any age group but it is more prevalent in females of reproductive age groups worldwide4. It has been shown that nearly 5–10 million females every year seek gynecologic advice for vaginitis5.

The prevalence of bacterial vaginosis ranges between 8 and 75%6 with higher magnitudes in parts of Africa7. Commonly, the problem occurs among pregnant women, and studies have consistently shown BV to be a risk factor for adverse obstetric and gynecological outcomes such as pre-term labor and delivery8–10, premature rupture of membranes, and low birth weight11, spontaneous abortion12, postpartum infections such as endometritis13, and cesarean section wound infections14.

Regarding the associated factors, researchers reported that marital status15, residence2, multiparity15, history of abortion16,17, frequency of douching2,18 as well as multiple sexual partners15–17 are associated with bacterial vaginosis. However, the associated factors of bacterial vaginosis are poorly understood as reports have been conflicting. Some of the studies reported that socio-demographic, behavioral, and clinical characteristics of pregnant women are associated with bacterial vaginosis8,18–21, while another study reported no association with some of these factors22. Bacterial vaginosis is still prevalent among pregnant women. Since most cases remain asymptomatic, early detection is essential for timely treatment and prevention of related complications and poor pregnancy outcomes. Hence, screening of symptomatic and asymptomatic pregnant women by taking vaginal swabs plays a vital role15,23.

For many years, bacterial vaginosis has been given little attention. In recent years, however, the association of bacterial vaginosis with ascending genital tract infection on one hand and sexually transmitted diseases (STDs) on another has made the infection a major global problem as women with bacterial vaginosis are at increased risk for STDs24. Furthermore, it has been documented that bacterial vaginosis propagates viral replication25–27, and vaginal shedding of the HIV-1 and HSV-2 (herpes simplex virus-2)28 thereby further enhancing the spread of these viruses. In general, bacterial vaginosis has emerged as a public health problem due to its association with sexually transmitted infections3,29,30.

In low-income countries like Ethiopia, pregnant women on antenatal care are often screened for sexually transmitted infections (STIs) including syphilis and HIV but rarely other treatable STIs or BV. In some instances, pregnant women with vaginal discharge are treated for vaginal candidiasis without laboratory investigations2. To avoid pregnancy complications and poor outcomes due to BV, information on its prevalence and associated factors is important for treatment and prevention. Currently, there is limited information on the prevalence and associated factors of BV in Ethiopia; to our knowledge, a few studies were done among pregnant women16,17, and no study was done in West Shoa. Therefore, this study was conducted to determine the prevalence of bacterial vaginosis and associated factors among pregnant women receiving antenatal care at public hospitals in the West Shoa zone, Oromia region, Ethiopia.

Materials and methods

Study design and period

An institutional-based cross-sectional study was conducted from September 15 to December 14, 2021.

Description of study area

West Shoa is one of the 20 zones of the Oromia regional state which is located to the west of the capital city of Ethiopia, Addis Ababa. The study was conducted at selected four public hospitals (Ambo University Referral Hospital, Gedo General Hospital, Bako Primary Hospital, and Inchini Primary Hospital).

Source population

The source population for this study was all pregnant women attending ANC (antenatal care) clinics in the West Shoa zone.

Study population

The study population for this study was the selected pregnant women attending the ANC clinics of the selected hospitals in the west Shoa zone.

Inclusion and exclusion criteria

Pregnant women ≥ 18 years of age attending ANC clinics and willing to participate in the study were included. Pregnant women with vaginal bleeding, genital malignancy, who inserted some drugs in their vagina, have already ruptured membranes, with antepartum hemorrhage, and if for some reason(s) she was unable to consent despite the eligibility, and those on antibiotic treatment in the preceding two weeks were excluded.

Sample size determination and sampling techniques

For determining the sample size of pregnant women, a single population proportion formula was used with the following assumptions.

n = sample size;

Zα/2 = standard value for 95% confidence level of two sides normal = 1.96;

d = margin of error, 5% = 0.05;

P = prevalence rate = 19.4% = 0.194, was taken from the study conducted in Addis Ababa, Tikur Anbessa Specialized Hospital16;n=zα/22p1-Pd2=1.962×0.1941-0.1940.052=240.

Considering the 10% non-response rate, the final sample size became 264. The number of pregnant women was proportionally allocated to each hospital. Considering that the yearly attendants of ANC at the selected hospitals was 2044 (data from Zonal Health Department of 2012 E.C), and with the assumption that data collection would be completed within three months, the average attendants were estimated to become 511 pregnant women during data collection period where N = 511 and the calculated sample size, n = 264; giving K = 2. Hence, a systematic random sampling technique was used to include every other pregnant woman in the study (Fig. 1).Fig. 1 Proportional allocation of study participants and sampling technique.

Data collection and laboratory investigations

Data were collected by midwives from the study participants using a pre-tested structured questionnaire that included socio-demographic characteristics, obstetric history and gynecological characteristics, hygienic behaviors/practices, sexual behaviors/practices, history of antibiotic use, history of previous medical conditions, and current situation of medical conditions. Upon admission to the study, midwives performed a clinical examination of each participant and recorded signs and symptoms of vaginal abnormalities such as the presence of vaginal discharge, vaginal itching, and vaginal burnings. The participants were also assessed by history for different medical conditions, like sexually transmitted diseases, urinary tract infections, hypertension, and diabetic mellitus.

After the interview, the midwives performed vaginal swabbing by instructing the participant to assume a lithotomy position, and a sterile disposable speculum was inserted into the vagina. A sterile cotton swab was used to swab the vaginal walls (lateral, anterior, and posterior fornices), and the swab was streaked on a clean grease-free slide for gram staining by trained Midwives and sent to the respective hospital laboratories for staining, microscopic examination, and interpretations of the results by Medical Laboratory Professionals.

For the diagnosis of bacterial vaginosis, the smeared vaginal slides were air dried, heat fixed, and then gram-stained and examined under an oil immersion objective (100× magnification), and it was graded as per standardized, quantitative, morphological classification method developed by Nugent et al.31. The method involves assigning a score between 0 and 10 based on the quantitative assessment of the Gram stain for three different bacterial morphotypes:Large Gram-positive rods (indicative of Lactobacillus spp),

Small Gram-negative or variable rods (indicative of Gardnerella, Bacteroides, and other anaerobic bacteria), and

Curved, Gram-variable rods (indicative of Mobiluncus spp).

Each morphotype was quantified from 1 to 4 + concerning the number of morphotypes per oil immersion field (zero, no morphotypes; 1+, less than 1 morphotypes; 2+, 1 to 4 morphotypes; 3+, 5 to 30 morphotypes; 4+, 30 or more morphotypes). Then, the results of the three different morphotypes were added to give the final score. The scores between 0 and 3 represented normal vaginal flora; between 4 and 6, intermediate vaginal flora; and scores between 7 and 10 were considered diagnostic for bacterial vaginosis (BV). In this study, the microbiological definition of BV was a score of 7–10 according to the Nugent’s criteria. As previously described by Shayo and others22, two experienced medical laboratory professionals were recruited at each study hospital to score the vaginal smears independently, and in case of discrepancy, a third opinion was sought for confirmation and her/his opinion was the final.

Data quality assurance and management

Data quality was ensured through the use of pre-tested tools for data collection, proper data collection, and processing of all activities. Training was given to midwives on specimen collection, and smear preparation. Every activity in the laboratory was done in adherence to standard operational procedures. To ensure good and uniform practice in the preparation and reading of gram stains, Medical laboratory technologists were trained on Nugent scoring before the study.

Data processing and analysis

After data collection, each questionnaire was checked for completeness, and missing, and edited for other errors. Data was entered into an Excel spreadsheet and exported to STATA-14 for analysis. Data were organized and presented using tables and graphs. Binary and multivariable logistic regressions were performed to examine the presence of association between a dependent variable and independent variables. Data were presented using Odds ratios (OR) and their 95% confidence intervals (CIs). Variable with a P value ≤ 0.25 at the bivariate logistic regression model were entered into a multivariate logistic regression model. Finally, a multivariate logistic regression model was carried out to identify predictors of bacterial vaginosis. AOR was used to explain the strength of the association, and a P value ≤ 0.05 was considered statistically significant.

Results

Socio-demographic characteristics of study subjects

This study was conducted in four hospitals; two primary, one general, and one referral hospital. The response rate was 98.5% (260 out of 264); four participants were excluded because of poor smear quality, and hence, data presentation, analysis, and interpretations were performed on a total of 260 pregnant women attending antenatal care. The mean age of the participants was 25.32 years (standard deviation = 0.33). The majority of the study participants, 54.6% (142/260), were in the age category of 21–29 years. By religion, Protestants were dominating, 64.23% (167/260). Most of the participants, 60% (156/260) were housewives by occupation. Rural and urban residents accounted for 51.54% and 48.46%, respectively (Table 1).Table 1 Socio-demographic characteristics of study subjects.

Variables	Categories	Frequency	Percent	
Study site	Ambo University referral Hospital	96	36.92	
Gedo General Hospital	54	20.77	
Bako Primary Hospital	51	19.62	
Inchi Primary Hospital	59	22.69	
Age category	≤ 20	61	23.46	
21–29	142	54.62	
≥ 30	57	21.92	
Marital status	Married	247	95.00	
Others	13	5.00	
Religion	Orthodox	73	28.08	
Protestant	167	64.23	
Others	20	7.69	
Educational level	Illiterate	34	13.08	
Able to read and write	56	21.54	
Primary school	50	19.23	
Secondary school	63	24.23	
College and above	57	21.92	
Occupation	Housewife	156	60.00	
Employed	47	18.08	
Trader	19	7.31	
Student	13	5.00	
Others	25	9.62	
Residence	Urban	126	48.46	
Rural	134	51.54	

Obstetric history and gynecological characteristics of study subjects

The majority of the study participants, 65% (169/260) were multigravida. Regarding parity, over half of the participants, 56.92% (148/260), were with low multiparity (1–4 deliveries). By gestational age, study participants in the 2nd trimester accounted for 45.77% (119/260) followed by the 3rd trimester, which accounted for 39.23% (102/260). Only 15.38% (40/260) of the participants had a history of abortion; of which 80% (32/40) encountered it only once while the rest 20% (8/40) had it twice. Stillbirth was reported by 7.31% (19/260) of the participants (Table 2).Table 2 Obstetric history and gynecological characteristics of study subjects.

Variables	Categories	Frequency	Percent	
Gravidity (number of pregnancy)	Primigravida	91	35.00	
Multigravida	169	65.00	
Parity (number of deliveries)	Nulliparity (0)	92	35.38	
Low multiparity (1–4)	148	56.92	
High multiparity (≥ 5)	20	7.69	
Gestational age	1st trimester	39	15.00	
2nd trimester	119	45.77	
3rd trimester	102	39.23	
History of abortion	No	220	84.62	
Yes	40	15.38	
Abortion frequency (n = 40)	Once	32	80.00	
Twice	8	20.00	
History of stillbirth	No	241	92.69	
Yes	19	7.31	
Stillbirth frequency (n = 19)	Once	15	78.95	
Twice	4	21.05	

Hygienic behaviors and practices of study subjects

More than three-fourths of the study participants, 76.54% (199/260), reported douching their vagina more than once a day. Of the participants, 42.31% (110/260) used soap for douching. Fifteen percent of the study subjects reported using disinfectants for washing their pants, while the majority of them (70%; 182/260) wore only a single pant for a week. Regarding frequency of showering, 55.38% (144/260) of the subjects took only once per week (Table 3).Table 3 Hygienic behaviors and practices of study subjects.

Variables	Categories	Frequency	Percent	
Vaginal douching per day	Once	61	23.46	
More than once	199	76.54	
Use of soup for douching	Yes	110	42.31	
No	150	57.69	
Washing pants with disinfectants	Yes	39	15.00	
No	221	85.00	
Number of pants used per week	None	20	7.69	
One	182	70.00	
Two or more	58	22.31	
Showering frequency per week	Once	144	55.38	
Twice	69	26.54	
Three or more	47	18.08	

Sexual behaviors and practices of study subjects

The sexual behaviors and practices of study participants are depicted in Table 4. Among the study participants, a few, 2.31% (6/260), had two or more sexual partners in the last 12 months. Almost, two-thirds of the participants (65.38%) have had only one sexual partner in their lifetime. Regarding condom use, 77.69%, 17.69%, and 4.62% of the participants had not used, used sometimes, and used usually, respectively.Table 4 Sexual behaviors and practices of study subjects.

Variables	Categories	Frequency	Percent	
Number of sexual partners in the last 12 months	One	254	97.69	
Two or more	6	2.31	
Number of lifetime sexual partners	One	170	65.38	
2–4	53	20.38	
5 or more	37	14.23	
Condom use	None	202	77.69	
Sometimes (< 50%)	46	17.69	
Usually (> 50%)	12	4.62	

Previous and current medical conditions of study subjects

Among the study participants, only 11.15%, 11.54%, and 2.69% reported having sexually transmitted diseases, urinary tract infections, and diabetes mellitus, respectively. History of antibiotic use was reported in 7.31% of the participants. During the study, the presence of vaginal discharge, itching, and burning were reported by 28.46%, 17.69%, and 18.08% of the participants, respectively. Of the study participants, 11.54% were presented with symptomatic STD, 8.08% with hypertension, and 2.69% with diabetic mellitus during the study. The majority of the participants knew their HIV serostatus; 83.85% (218/260) were non-reactive and 3.85% (10/260) were reactive for HIV, while 12.31% (32/260) were with unknown serostatus (Table 5).Table 5 Previous and current medical conditions of study subjects.

Variables	Categories	Frequency	Percent	
History of STD	Yes	29	11.15	
No	231	88.85	
History of UTI	Yes	30	11.54	
No	230	88.46	
History of DM	Yes	7	2.69	
No	253	97.31	
History of antibiotic use	Yes	19	7.31	
No	241	92.69	
Presence of vaginal discharge	Yes	74	28.46	
No	186	71.54	
Milky and homogenous vaginal discharge (74)	Yes	56	75.68	
No	18	24.32	
Vaginal itching	Yes	46	17.69	
No	214	82.31	
Vaginal burning	Yes	47	18.08	
No	213	81.92	
Current situation of STD	None, or asymptomatic	230	88.46	
Symptomatic	30	11.54	
Current situation of UTI	None, or asymptomatic	233	89.62	
Symptomatic	27	10.38	
HIV serostatus	Reactive	10	3.85	
Non-reactive	218	83.85	
Status not known	32	12.31	
Hypertension	Yes	21	8.08	
No	239	91.92	
Diabetic mellitus	Yes	7	2.69	
No	253	97.31	
STD, sexually transmitted disease; UTI, urinary tract infection; DM, diabetic mellitus; HIV, human immunodeficiency virus.

Prevalence of bacterial vaginosis among the study subjects

According to the Nugent scoring criteria, 22.3% (58/260) of the participants were with depleted vaginal flora (score of 7–10), 25% (65/260) were with intermediate vaginal flora (score of 4–6) and 52.7% (137/260) were with normal vaginal flora (score of 0–3). Both intermediate and normal vaginal floras were interpreted as negative for bacterial vaginosis according to the Nugent scoring system. The prevalence of bacterial vaginosis was, therefore, 22.3% (95% CI 17.4 to 27.9%) (Fig. 2).Fig. 2 Prevalence of bacterial vaginosis among study subjects.

Factors associated with bacterial vaginosis

For the statistical analysis using logistic regression models, variables were segregated according to their relatedness: socio-demographic variables, obstetric characteristics, hygienic behaviors and practices, sexual behaviors, and practices as well as previous and current medical conditions. In each category, binary logistic regression analysis was performed, and variables with a P value of ≤ 0.25 were selected as candidates for multiple logistic regression analysis (Table 6).Table 6 Binary and multiple logistic regression analysis results of factors associated with bacterial vaginosis among pregnant women.

Variables	Categories	BV status	COR	95% CI	P value	AOR (95% CI)	P value	
Positive N (%)	Negative N (%)	
Socio-demographic characteristics	
 Age category	≤ 20 (ref.)	12 (19.7)	49 (80.3)	–	–	–	–	–	
21–29	27 (19.0)	115 (81.0)	1.043	0.489 to 2.225	0.913	1.101 (0.490 to 2.470)	0.816	
≥ 30	19 (33.3)	38 (66.7)	0.490	0.212 to 1.132	0.095*	0.573 (0.225 to 1.457)	0.242	
 Marital status	Married (ref.)	53 (21.4)	195 (78.6)						
Others	5 (38.5)	8 (61.5)	0.437	0.137 to 1.391	0.161*	0.260 (0.068 to 0.9995)	0.050**	
 Religion	Orthodox (ref.)	18 (24.7)	55 (75.3)						
Protestant	37 (22.2)	130 (77.8)	1.150	0.603 to 2.193	0.672			
Others	3 (15.0)	17 (85.0)	1.854	0.487 to 7.067	0.366			
 Educational level	Illiterate (ref.)	10 (29.4)	24 (70.6)						
Able to read & write	7 (12.5)	49 (87.5)	2.917	0.988 to 8.608	0.053*	1.847 (0.573 to 5.954)	0.304	
Primary school	14 (28.0)	36 (72.0)	1.071	0.409 to 2.804	0.888	0.817 (0.283 to 2.360)	0.708	
Secondary school	14 (22.2)	49 (77.8)	1.458	0.566 to 3.760	0.435	1.167 (0.385 to 3.540)	0.785	
College and above	13 (22.8)	44 (77.2)	1.410	0.538 to 3.694	0.484	1.204 (0.375 to 3.859)	0.755	
 Occupation	Housewife (ref.)	35 (22.4)	121 (77.6)						
Employed	12 (25.5)	35 (74.5)	0.843	0.396 to 1.797	0.659	1.010 (0.399 to 2.557)	0.983	
Trader	2 (10.5)	17 (89.5)	2.459	0.542 to 11.160	0.244*	4.023(0.766 to 21.129)	0.100	
Student	2 (15.4)	11 (84.6)	1.591	0.337to 7.517	0.558	2.045 (0.408 to 10.257)	0.384	
Others	7 (28.0)	18 (72.0)	0.744	0.287 to 1.924	0.542	0.666 (0.240 to 1.846)	0.434	
 Residence	Urban (ref.)	34 (27.0)	92 (73.0)						
Rural	24 (17.9)	110 (82.1)	1.694	0.938 to 3.060	0.081*	2.108 (1.049 to 4.236)	0.036**	
Obstetric history and gynecological characteristics	
 Gravidity	Primigravida (ref.)	14 (15.4)	77 (84.6)						
Multigravida	44 (26.0)	125 (74.0)	0.517	0.266to 1.004	0.052*	0.102 (0.009 to 1.213)	0.071	
 Parity	Nulliparity (ref.)	16 (17.4)	76 (82.6)						
Low multiparity (1–4)	36 (24.3)	112 (75.7)	0.655	0.340 to 1.263	0.207*	5.707 (0.509 to 63.997)	0.158	
High multiparity (≥ 5)	6 (30.0)	14 (70.0)	0.491	0.164 to 1.473	0.204*	4.416 (0.339 to 57.475)	0.257	
 Gestational age	1st trimester (ref.)	9 (23.1)	30 (76.9)						
2nd trimester	25 (21.0)	94 (79.0)	1.128	0.475 to 2.681	0.785			
3rd trimester	24 (23.5)	78 (76.5)	0.975	0.407 to 2.337	0.955			
 History of abortion	No (ref.)	46 (20.9)	174 (79.1)						
Yes	12 (30.0)	28 (70.0)	0.617	0.291 to 1.306	0.207*	0.805 (0.358 to 1.807)	0.598	
 History of stillbirth	No (ref.)	54 (22.4)	187 (77.6)						
Yes	4 (21.1)	15 (78.9)	1.083	0.345 to 3.399	0.891			
Hygienic behaviors and practices	
 Vaginal douching/day	Once (ref.)	19 (31.1)	42 (68.9)						
More than once	39 (19.6)	160 (80.4)	1.856	0.974 to 3.538	0.060*	1.638 (0.831 to 3.229)	0.154	
 Use of soup for douching	No (ref.)	33 (22.0)	117 (78.0)						
Yes	25 (22.7)	85 (77.3)	0.959	0.532 to 1.730	0.889			
 Washing pants with disinfectants	No (ref.)	45 (20.4)	176 (79.6)						
Yes	13 (33.3)	26 (66.7)	0.511	0.244 to 1.074	0.076	0.630 (0.292 to 1.358)	0.238	
 Number of pants used per week	None (ref.)	9 (45.0)	11 (55.0)						
One	42 (23.1)	140 (76.9)	2.727	1.059 to 7.024	0.038*	2.743 (1.044 to 7.205)	0.041**	
Two or more	7 (12.1)	51 (87.9)	5.961	1.826 to 19.463	0.003*	4.965 (1.487 to 16.573)	0.009**	
 Showering frequency per week	Once (ref.)	34 (23.6)	110 (76.4)						
Twice	14 (20.3)	55 (79.7)	1.214		0.588			
Three or more	10 (21.3)	37 (78.7)	1.144		0.741			
Sexual behaviors and practices	
 Number of sexual partners in the last 12 months	One (ref.)	56 (22.0)	198 (78.0)						
Two or more	2 (33.3)	4 (66.7)	0.566	0.101 to 3.169	0.517			
 Number of lifetime sexual partners	Only one (ref.)	32 (18.8)	138 (81.2)						
2–4	14 (26.4)	39 (73.6)	0.646	0.314 to1.329	0.235*	0.555 (0.246 to 1.252)	0.156	
5 or more	12 (32.4)	25 (67.6)	0.483	0.220 to 1.063	0.071*	0.551 (0.226 to 1.343)	0.190	
 Condom use	Usually (> 50%) (ref.)	6 (50.0)	6 (50.0)						
Sometimes (< 50%)	9 (19.6)	37 (80.4)	4.111	1.070 to 15.792	0.040*	4.042 (0.977 to 16.732)	0.054	
None	43 (21.3)	159 (78.7)	3.698	1.135 to 12.042	0.030*	2.603 (0.718 to 9.434)	0.145	
Previous and current medical conditions	
 History of STD	No (ref.)	50 (21.6)	181 (78.4)						
Yes	8 (27.6)	21 (72.4)	0.725	0.303 to 1.735	0.470			
 History of UTI	No (ref.)	48 (20.9)	182 (79.1)						
Yes	10 (33.3)	20 (66.7)	0.527	0.232 to 1.201	0.128*	0.709 (0.256 to 1.968)	0.510	
 History of DM	No (ref.)	57 (22.5)	196 (77.5)						
Yes	1 (14.3)	6 (85.7)	1.745	0.206 to 14.793	0.610			
 History of antibiotic use	No (ref.)	51 (21.2)	190 (78.8)						
Yes	7 (36.8)	12 (63.2)	0.460	0.172 to 1.229	0.121*	0.634 (0.183 to 2.191)	0.471	
 Presence of vaginal discharge	No (ref.)	38 (20.4)	148 (79.6)						
Yes	20 (27.0)	54 (73.0)	0.693	0.3714 to 1.295	0.250*	0.829 (0.423 to 1.625)	0.586	
 Vaginal itching	No (ref.)	49 (22.9)	165 (77.1)						
Yes	9 (19.6)	37 (80.4)	1.221	0.551 to 2.704	0.623			
 Vaginal burning	No (ref.)	46 (21.6)	167 (78.4)						
Yes	12 (25.5)	35 (74.5)	0.803	0.386to 1.671	0.558			
 Current situation of STD	None or asymptomatic (ref.)	49 (21.3)	181 (78.7)						
Symptomatic	9 (30.0)	21 (70.0)	0.632	0.272 to 1.466	0.285			
 Current situation of UTI	None or asymptomatic (ref.)	50 (21.5)	183 (78.5)						
Symptomatic	8 (29.6)	19 (70.4)	0.649	0.268 to 1.570	0.337			
 HIV serostatus	Non-reactive (ref.)	48 (22.0)	170 (78.0)						
Reactive	3 (30.0)	7 (70.0)	0.659	0.164 to 2.645	0.556			
Status not known	7 (21.9)	25 (78.1)	1.008	0.411 to 2.473	0.985			
 Hypertension	No (ref.)	51 (21.3)	188 (78.7)						
Yes	7 (33.3)	14 (66.7)	0.543	0.208 to 1.415	0.211*	0.612 (0.225 to 1.669)	0.338	
 Current situation of DM	No (ref.)	56 (22.1)	197 (77.9)						
Yes	2 (28.6)	5 (71.4)	0.711	0.134 to 3.762	0.688			
DM, diabetes mellitus; HIV, human immunodeficiency virus; STD, sexually transmitted disease; UTI, urinary tract infection. *Candidate variables for multiple logistic regression; **statistically significant.

In the binary logistic regression analysis of socio-demographic characteristics, the age category of ≥ 30 years old (P = 0.095), marital status other than married (P = 0.161), educational level of ‘able to read and write’ (P = 0.053), occupation category of trader (P = 0.244), and residence (P = 0.081) were found candidates for multiple logistic regression analysis. In the multiple logistic regressions, marital status other than married women and residence were found predictors of bacterial vaginosis. The odds of having bacterial vaginosis among marital status other than married were reduced by 74% (AOR = 0.260, 95% CI 0.068 to 0.9995; P = 0.05) as compared with married pregnant women. The odds of having bacterial vaginosis among rural residents was 2.1 (AOR: 2.1 (95% CI 1.05 to 4.24); P = 0.036) times the odds of having bacterial vaginosis among urban residents.

Concerning the obstetric and gynecologic characteristics, gravidity (multigravida, P = 0.052), parity (low multiparity, P = 0.207; High multiparity, P = 0.204), and history of abortion (P = 0.207) were found candidates for multiple logistic regressions in binary logistic regressions, but none of them were predictors of bacterial vaginosis.

In the binary logistic regression of hygienic behaviors and practices, vaginal douching (more than once per day, P = 0.060), washing pants with disinfectants (P = 0.076), and number of pants worn per week (one pant per week, P = 0.038; two or more pants per week, P = 0.003) were candidates for multiple logistic regression model. In the multiple logistic regression analysis, the number of pants was found predictor for bacterial vaginosis. The odds of having bacterial vaginosis among those wearing one pant per week was 2.7 (AOR = 2.7, 95% CI 1.04 to 7.20; P = 0.041) times the odds of having bacterial vaginosis among those not wearing pants. Those wearing two or more pants per week were 4.5 more likely to develop bacterial vaginosis as compared with those not wearing pants (AOR = 4.5, 95% CI 1.49 to 16.57; P = 0.009).

Of the sexual behavior and practice variables, number of lifetime sexual partners (2–4 partners in life, P = 0.235 and 5 or more partners in life, P = 0.071), and condom use (not using at all, P = 0.03 and using sometimes, P = 0.040) were found candidates for multiple logistic regression analysis. However, these variables were found insignificant predictors of bacterial vaginosis. Again, none of the variables related to the previous and current medical conditions were found significant in the multiple logistic regressions although history of urinary tract infection, history of antibiotics use, presence of vaginal discharge, and hypertension were candidates in the binary logistic regression analysis with P values of 0.128, 0.121, 0.250, and 0.211, respectively.

Discussion

In the current study, the prevalence of bacterial vaginosis among pregnant women using the Nugent scoring system was 22.3% (95% CI 17.4 to 27.9%). This result is comparable with the prevalence of bacterial vaginosis recently reported from Harar City, Eastern Ethiopia, 20.6%17. It is also in line with the previous report with the prevalence of 19.4% for bacterial vaginosis from Addis Ababa16. Comparable prevalences of bacterial vaginosis with our recent result were also reported from other African countries, such as Kenya, 19.3%32, Northeastern Nigeria, 17.3%33, South Africa, 17.7%34, and Cameroon, 26%2. The consistency of our findings with these reports may be due to the consideration of similar study participants. Our current result is also comparable with the report from India, 23%23. The similarities could be suggested that there may be related lifestyles, and hygienic behaviors/practices among Ethiopian and Indian pregnant women.

The detection rate of bacterial vaginosis among pregnant women was 49.8% in Sudan35. This result is much higher than the result of our current study though similar study subjects were included, and the same study design was employed. The variations could suggest that there might be differences in hygienic behaviors and practices. A higher prevalence of bacterial vaginosis (30.9%) was also reported in Ghana36 compared with our current result (22.3%). The inconsistencies could be due to the utilization of a larger sample size with convenient sampling techniques in the study from Ghana while a smaller sample size with systematic random sampling was employed in our study. As a study from Southeastern Nigeria indicated, a higher prevalence was reported, 38%37; this could be due to a smaller sample of the study from southeastern Nigeria. Compared with our current result, higher magnitudes of bacterial vaginosis were also reported from Tanzania and Zimbabwe, 28.5% and 32.6%, respectively22,38. The differences might be the inclusion of study subjects during their 3rd trimester only in the study from Zimbabwe and during delivery in the case of Tanzania while our study included all gestational ages of women during antenatal follow-up.

In contrast to our current study, a slightly smaller prevalence of bacterial vaginosis, 16%, was reported from southwestern Nigeria15. This variation might be due to the consecutive recruitment of a larger number of study subjects in the case of southwestern Nigeria while a relatively smaller sample size was employed using systematic random sampling in the current study, in addition to geographical and/or hygienic variations. The prevalence of bacterial vaginosis in Portugal was 3.88%39, which is much smaller than our report. The inconsistent results might be population and/or geographical differences.

Our study revealed that the marital status of pregnant women other than married were at reduced risk of bacterial vaginosis (AOR = 0.260, 95% CI 0.068 to 0.9995; P = 0.05) as compared with married pregnant women. In agreement with our finding, a statistically significant association was found between marital status and bacterial vaginosis according to a report from Southwestern Nigeria15. However, contrasting findings were reported from eastern Ethiopia17, Addis Ababa18, Ghana36, Cameroon2 and Tanzania22. Our result also showed that rural residents had 2.1 (AOR = 2.1, 95% CI 1.05 to 4.24; P = 0.036) times more risk of developing bacterial vaginosis as compared with urban residents. In line with this, a study from Cameroon indicated that bacterial vaginosis was significantly higher in women from rural parts than those from urban areas2. On the contrary, residence was not associated with bacterial vaginosis as reported from eastern Ethiopia17 and Tanzania22. The variations might be due to the differences in the lifestyle of the participants from different areas.

Obstetric and gynecologic variables considered in our study, such as gravidity, parity, gestational age, history of abortion, and history of stillbirth were not significantly associated with bacterial vaginosis. In line with our findings, no significant associations were revealed between gravidity and the prevalence of bacterial vaginosis from India40 and Cameroon2. But, a study from Ghana reported that high multigravidas were at reduced risk of bacterial vaginosis36. In agreement with the current study, no association of parity with bacterial vaginosis was reported from Cameroon2. On the other hand, a study from southwestern Nigeria reported that multiparity was significantly associated with bacterial vaginosis15. Regarding the gestational age, contrasting results were reported to our finding. From Ghana, the study reported that 3rd trimester was at a reduced risk of bacterial vaginosis36, while the study from South Africa revealed that both 2nd and 3rd trimesters were associated with a reduced risk of the disease as compared with the 1st trimester34. Conflicting with these studies34,36, other studies from Cameroon2 and Northeastern Nigeria33, reported that 2nd trimester was at increased risk of bacterial vaginosis. Consistent with our recent study, a history of abortion was not significantly associated with bacterial vaginosis as reported by Bitew and others from Addis Ababa18, and Ghana36. However, another study from Addis Ababa16 and eastern Ethiopia17 indicated that a history of abortion was significantly associated with bacterial vaginosis.

In the current study, hygienic behaviors and practices of pregnant women, such as frequency of vaginal douching per day, use of soup for douching, washing pants with disinfectants, and showering frequency per week were not significantly associated with bacterial vaginosis. However, the number of pants worn per week was found significantly associated with bacterial vaginosis. Wearing one pant for a week was 2.7 (AOR = 2.7, 95% CI 1.04 to 7.20; P = 0.041) times more associated with developing bacterial vaginosis as compared with those not wearing. Again, the risk of developing bacterial vaginosis also increased 5 times (AOR = 4.96, 95% CI 1.49 to 16.57; P = 0.009) among those wearing two or more pants per week as compared with those not wearing. This could be explained that the chemical ingredients of cleansing agents used to wash the pants may affect the vaginal flora as frequently exposed to chemical residues. In agreement with our result, douching was not significantly associated with bacterial vaginosis according to a study from Ghana36. Inconsistent with our finding, a study from Cameroon reported significantly higher bacterial vaginosis in those practicing douching2, and frequent douching (≥ 4 per day) was significantly associated with bacterial vaginosis as a report from Addis Ababa, Ethiopia18. Like our result, a Cameroon study reported that the use of soap for douching was not significantly associated with bacterial vaginosis2. In contrast to our study, participants who did not wash their pants with disinfectants were significantly infected with bacterial vaginosis as reported from Cameroon2.

In our study, the sexual behavior/practice variables, such as the number of sexual partners in the last 12 months, lifetime sexual partners, and use of condoms were found insignificant predictors of bacterial vaginosis. Similar to our finding, a study from Addis Ababa by Bitew and colleagues reported that the number of lifetime sexual partners was not significantly associated with bacterial vaginosis18. However, other studies from Ethiopia, Addis Ababa16, and Harar City17, reported that multiple sexual partners were significantly associated with bacterial vaginosis, and a study from southwestern Nigeria15 also supported these findings opposing our result. This could be suggested that bacterial vaginosis may be enhanced through frequent sexual activities as it can disturb the vaginal flora.

As any study may not be free from limitation(s), our study has a limitation. Clinical diagnosis of bacterial vaginosis using ‘Amsel’s Criteria’ was not performed because a kit for determining vaginal pH was not found in the market during the purchasing process of materials and reagents for this research project. However, it had little effect on our work since the ‘Nugent scoring criteria’, a gold standard method for the diagnosis of bacterial vaginosis, was used, which was one of the strengths of our study. Hence, the objectives of our study have been answered in line with the plan. The other strength was that our study was a multicenter study, conducted in four hospitals which were selected from eight hospitals found in the West Shoa zone. Furthermore, a random sampling technique was employed to recruit study participants allowing the generalizability of the findings of our study.

Conclusions

The current study revealed a high prevalence of bacterial vaginosis among pregnant women attending antenatal care in the study settings. Pregnant women in rural areas were at increased risk of bacterial vaginosis. Marital status other than married was significantly associated with reduced bacterial vaginosis. Considering the high prevalence of bacterial vaginosis, we recommend that pregnant women attending antenatal care should be screened and treated to prevent possible adverse outcomes. Hence, screening for the disease should be integrated into the recommended basic laboratory investigations during antenatal visits.

Abbreviations

ANC Antenatal care

AOR Adjusted odds ratio

AURH Ambo University Referral Hospital

BV Bacterial vaginosis

CI Confidence interval

COR Crude odds ratio

HIV Human immunodeficiency virus

HSV Herpes simplex virus

OR Odds ratio

STDs Sexually transmitted diseases

STIs Sexually transmitted infections

Acknowledgements

Authors have special thanks to Ambo University for the opportunity given to us to carry out this research. The authors also thank data collectors for their unreserved contribution; and study participants who shared their valuable information for this study.

Author contributions

B.T.R., the principal investigator, contributed to the conception, study design, execution, and acquisition of data, analysis, and interpretation of data, manuscript drafting, and revising of the manuscript. C.K., F.W., S.Y., A.B.M., and A.O.S. contributed to the study design, execution, acquisition of data, and revising of the manuscript. W.T.W., S.L.D., and B.T.D. contributed to the analysis and interpretation, manuscript drafting, and revising of the manuscript. All authors read and approved the final manuscript.

Funding

Ambo University funded this study. However, it has no role in the decision to publish, manuscript preparation, and publication.

Data availability

Data will be available upon reasonable request from the corresponding author.

Declarations

Competing interests

The authors declare no competing interests.

Ethics approval and consent to participate

Ethical clearance was obtained from Ambo University, the College of Health Sciences, and the Referral Hospital Institutional Review Board with a reference number of “CMHS/R-MLT/06/13”. Permissions were also secured from the included hospital administration offices and oral informed consent was taken from all study participants. The laboratory procedures for diagnosing bacterial vaginosis were performed following relevant guidelines. Data were collected anonymously and the privacy of the information was kept and protected from unintended manipulations.

Consent for publication

Not applicable.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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References

1. Ryan KJRC Ahmad N Drew WL Plorde JJ Sherris Medical Microbiology 2009 5 Mcgraw-Hill
Ryan, K. J. R. C., Ahmad, N., Drew, W. L. & Plorde, J. J. Sherris Medical Microbiology 5th edn. (Mcgraw-Hill, 2009).
2. Kamga YM Ngunde JP Akoachere J-FT Prevalence of bacterial vaginosis and associated risk factors in pregnant women receiving antenatal care at the Kumba Health District (KHD), Cameroon BMC Pregnancy Childbirth 2019 19 1 1 8 10.1186/s12884-019-2312-9 30606156
Kamga, Y. M., Ngunde, J. P. & Akoachere, J.-F.T. Prevalence of bacterial vaginosis and associated risk factors in pregnant women receiving antenatal care at the Kumba Health District (KHD), Cameroon. BMC Pregnancy Childbirth 19(1), 1–8 (2019).30606156 10.1186/s12884-019-2312-9
3. Bertini M Serdaroglu S Kutlubay Z Bacterial vaginosis and sexually transmitted diseases: relationship and management Fundamentals of Sexually Transmitted Infections 2017 InTech 75
Bertini, M. Bacterial vaginosis and sexually transmitted diseases: relationship and management. In Fundamentals of Sexually Transmitted Infections (eds Serdaroglu, S. & Kutlubay, Z.) 75 (InTech, 2017).
4. Moreira Mascarenhas RE Sacramento Cunha Machado M Borges da Costa e Silva BF Fernandes Weyll Pimentel R Teixeira Ferreira T Silva Leoni FM Prevalence and risk factors for bacterial vaginosis and other vulvovaginitis in a population of sexually active adolescents from Salvador, Bahia, Brazil Infect. Dis. Obstet. Gynecol. 2012 2012 1 6 10.1155/2012/378640
Moreira Mascarenhas, R. E. et al. Prevalence and risk factors for bacterial vaginosis and other vulvovaginitis in a population of sexually active adolescents from Salvador, Bahia, Brazil. Infect. Dis. Obstet. Gynecol. 2012, 1–6 (2012).10.1155/2012/378640
5. Donders GG Vereecken A Bosmans E Dekeersmaecker A Salembier G Spitz B Definition of a type of abnormal vaginal flora that is distinct from bacterial vaginosis: Aerobic vaginitis BJOG Int. J. Obstet. Gynaecol. 2002 109 1 34 43 10.1111/j.1471-0528.2002.00432.x
Donders, G. G. et al. Definition of a type of abnormal vaginal flora that is distinct from bacterial vaginosis: Aerobic vaginitis. BJOG Int. J. Obstet. Gynaecol. 109(1), 34–43 (2002).10.1111/j.1471-0528.2002.00432.x
6. Murta EF Silva AO Silva EA Adad SJ Frequency of infectious agents for vaginitis in non- and hysterectomized women Arch. Gynecol. Obstet. 2005 273 152 156 10.1007/s00404-005-0023-0 16021494
Murta, E. F., Silva, A. O., Silva, E. A. & Adad, S. J. Frequency of infectious agents for vaginitis in non- and hysterectomized women. Arch. Gynecol. Obstet. 273, 152–156 (2005).16021494 10.1007/s00404-005-0023-0
7. Kenyon C Colebunders R Crucitti T The global epidemiology of bacterial vaginosis: A systematic review Am. J. Obstet. Gynecol. 2013 209 6 505 523 10.1016/j.ajog.2013.05.006 23659989
Kenyon, C., Colebunders, R. & Crucitti, T. The global epidemiology of bacterial vaginosis: A systematic review. Am. J. Obstet. Gynecol. 209(6), 505–523 (2013).23659989 10.1016/j.ajog.2013.05.006
8. Afolabi BB Moses OE Oduyebo OO Bacterial vaginosis and pregnancy outcome in Lagos, Nigeria Open Forum Infect. Dis. 2016 3 1 ofw030 10.1093/ofid/ofw030 26989754
Afolabi, B. B., Moses, O. E. & Oduyebo, O. O. Bacterial vaginosis and pregnancy outcome in Lagos, Nigeria. Open Forum Infect. Dis. 3(1), ofw030 (2016).26989754 10.1093/ofid/ofw030
9. Das TR Fatema K Chowdhury S Farah N Ara R Chakma B Association of bacterial vaginosis with preterm delivery J. Bangladesh Coll. Phys. Surg. 2016 34 4 188 10.3329/jbcps.v34i4.32408
Das, T. R. et al. Association of bacterial vaginosis with preterm delivery. J. Bangladesh Coll. Phys. Surg. 34(4), 188 (2016).10.3329/jbcps.v34i4.32408
10. Yzeiraj-Kalemaj L Shpata V Vyshka G Manaj A Bacterial vaginosis, educational level of pregnant women, and preterm birth: A case-control study Int. Sch. Res. Not. 2013 2013 1 4
Yzeiraj-Kalemaj, L., Shpata, V., Vyshka, G. & Manaj, A. Bacterial vaginosis, educational level of pregnant women, and preterm birth: A case-control study. Int. Sch. Res. Not. 2013, 1–4 (2013).
11. Kiran CK Kandati J Ponugoti M Prevalence of bacterial vaginosis in preterm and termlabour: A one year study Int. J. Reprod. Contracept. Obstet. Gynecol. 2017 6 6 2292 2296 10.18203/2320-1770.ijrcog20172072
Kiran, C. K., Kandati, J. & Ponugoti, M. Prevalence of bacterial vaginosis in preterm and termlabour: A one year study. Int. J. Reprod. Contracept. Obstet. Gynecol. 6(6), 2292–2296 (2017).10.18203/2320-1770.ijrcog20172072
12. Işik G Demirezen Ş Dönmez HG Beksaç MS Bacterial vaginosis in association with spontaneous abortion and recurrent pregnancy losses J. Cytol. 2016 33 3 135 10.4103/0970-9371.188050 27756985
Işik, G., Demirezen, Ş, Dönmez, H. G. & Beksaç, M. S. Bacterial vaginosis in association with spontaneous abortion and recurrent pregnancy losses. J. Cytol. 33(3), 135 (2016).27756985 10.4103/0970-9371.188050
13. Haggerty CL Hillier SL Bass DC Ness RB Bacterial vaginosis and anaerobic bacteria are associated with endometritis Clin. Infect. Dis. 2004 39 7 990 995 10.1086/423963 15472851
Haggerty, C. L., Hillier, S. L., Bass, D. C. & Ness, R. B. Bacterial vaginosis and anaerobic bacteria are associated with endometritis. Clin. Infect. Dis. 39(7), 990–995 (2004).15472851 10.1086/423963
14. Mullick S Watson-Jones D Beksinska M Mabey D Sexually transmitted infections in pregnancy: prevalence, impact on pregnancy outcomes, and approach to treatment in developing countries Sex. Transm. Infect. 2005 81 4 294 10.1136/sti.2002.004077 16061534
Mullick, S., Watson-Jones, D., Beksinska, M. & Mabey, D. Sexually transmitted infections in pregnancy: prevalence, impact on pregnancy outcomes, and approach to treatment in developing countries. Sex. Transm. Infect. 81(4), 294 (2005).16061534 10.1136/sti.2002.004077
15. Aduloju OP Akintayo AA Aduloju T Prevalence of bacterial vaginosis in pregnancy in a tertiary health institution, south western Nigeria Pan Afr. Med. J. 2019 33 9 10.11604/pamj.2019.33.9.17926 31303954
Aduloju, O. P., Akintayo, A. A. & Aduloju, T. Prevalence of bacterial vaginosis in pregnancy in a tertiary health institution, south western Nigeria. Pan Afr. Med. J. 33, 9 (2019).31303954 10.11604/pamj.2019.33.9.17926
16. Mengistie Z Woldeamanuel Y Asrat D Adera A Prevalence of bacterial vaginosis among pregnant women attending antenatal care in Tikur Anbessa University Hospital, Addis Ababa, Ethiopia BMC Res. Notes. 2014 7 1 5 10.1186/1756-0500-7-822 24382056
Mengistie, Z., Woldeamanuel, Y., Asrat, D. & Adera, A. Prevalence of bacterial vaginosis among pregnant women attending antenatal care in Tikur Anbessa University Hospital, Addis Ababa, Ethiopia. BMC Res. Notes. 7, 1–5 (2014).24382056 10.1186/1756-0500-7-822
17. Ahmed M Admassu Ayana D Abate D Bacterial vaginosis and associated factors among pregnant women attending antenatal care in Harar City, Eastern Ethiopia Infect. Drug Resist. 2022 15 3077 86 10.2147/IDR.S364229 35754781
Ahmed, M., Admassu Ayana, D. & Abate, D. Bacterial vaginosis and associated factors among pregnant women attending antenatal care in Harar City, Eastern Ethiopia. Infect. Drug Resist. 15, 3077–86 (2022).35754781 10.2147/IDR.S364229
18. Bitew A Abebaw Y Bekele D Mihret A Prevalence of bacterial vaginosis and associated risk factors among women complaining of genital tract infection Int. J. Microbiol. 2017 2017 1 8 10.1155/2017/4919404
Bitew, A., Abebaw, Y., Bekele, D. & Mihret, A. Prevalence of bacterial vaginosis and associated risk factors among women complaining of genital tract infection. Int. J. Microbiol. 2017, 1–8 (2017).10.1155/2017/4919404
19. Akomoneh EA Foche FF Aseneck CA Abong RA Ajonina MU Prevalence of bacterial vaginosis among sexually active women attending the CDC central clinic Tiko, south west region, Cameroon Afr. J. Infect. Dis. 2016 10 2 96 101 10.21010/ajid.v10i2.4 28480443
Akomoneh, E. A., Foche, F. F., Aseneck, C. A., Abong, R. A. & Ajonina, M. U. Prevalence of bacterial vaginosis among sexually active women attending the CDC central clinic Tiko, south west region, Cameroon. Afr. J. Infect. Dis. 10(2), 96–101 (2016).28480443 10.21010/ajid.v10i2.4
20. Desseauve D Chantrel J Fruchart A Khoshnood B Brabant G Ancel P Prevalence and risk factors of bacterial vaginosis during the first trimester of pregnancy in a large French population-based study Eur. J. Obstet. Gynecol. Reprod. Biol. 2012 163 1 30 34 10.1016/j.ejogrb.2012.04.007 22572215
Desseauve, D. et al. Prevalence and risk factors of bacterial vaginosis during the first trimester of pregnancy in a large French population-based study. Eur. J. Obstet. Gynecol. Reprod. Biol. 163(1), 30–34 (2012).22572215 10.1016/j.ejogrb.2012.04.007
21. Li XD Tong F Zhang XJ Pan WJ Chen ML Wang CC Incidence and risk factors of bacterial vaginosis among pregnant women: A prospective study in Maanshan city, Anhui Province, China J. Obstet. Gynaecol. Res. 2015 41 8 1214 1222 10.1111/jog.12704 25913643
Li, X. D. et al. Incidence and risk factors of bacterial vaginosis among pregnant women: A prospective study in Maanshan city, Anhui Province, China. J. Obstet. Gynaecol. Res. 41(8), 1214–1222 (2015).25913643 10.1111/jog.12704
22. Shayo PA Kihunrwa A Massinde AN Mirambo M Rumanyika RN Ngwalida N Prevalence of bacterial vaginosis and associated factors among pregnant women attending at Bugando Medical Centre, Mwanza, Tanzania, Tanzan J. Health Res. 2012 14 3 175
Shayo, P. A. et al. Prevalence of bacterial vaginosis and associated factors among pregnant women attending at Bugando Medical Centre, Mwanza, Tanzania, Tanzan. J. Health Res. 14(3), 175 (2012).
23. Ambike AS Shelke Y Nakhate P Patil S Sankholkar C Prevalence of asymptomatic and symptomatic bacterial vaginosis in pregnant women attending antenatal clinic in a tertiary care rural hospital Int. J. Reprod. Contracept. Obstet. Gynecol. 2020 9 3672 10.18203/2320-1770.ijrcog20203838
Ambike, A. S., Shelke, Y., Nakhate, P., Patil, S. & Sankholkar, C. Prevalence of asymptomatic and symptomatic bacterial vaginosis in pregnant women attending antenatal clinic in a tertiary care rural hospital. Int. J. Reprod. Contracept. Obstet. Gynecol. 9, 3672 (2020).10.18203/2320-1770.ijrcog20203838
24. Verstraelen H Verhelst R Vaneechoutte M Temmerman M The epidemiology of bacterial vaginosis in relation to sexual behaviour BMC Infect. Dis. 2010 10 1 1 11 10.1186/1471-2334-10-81 20044936
Verstraelen, H., Verhelst, R., Vaneechoutte, M. & Temmerman, M. The epidemiology of bacterial vaginosis in relation to sexual behaviour. BMC Infect. Dis. 10(1), 1–11 (2010).20044936 10.1186/1471-2334-10-81
25. Cohn JA Hashemi FB Camarca M Kong F Xu J Beckner SK HIV-inducing factor in cervicovaginal secretions is associated with bacterial vaginosis in HIV-1–infected women J. Acquir. Immune Defic. Syndr. 2005 39 3 340 10.1097/01.qai.0000146599.47925.e0 15980696
Cohn, J. A. et al. HIV-inducing factor in cervicovaginal secretions is associated with bacterial vaginosis in HIV-1–infected women. J. Acquir. Immune Defic. Syndr. 39(3), 340 (2005).15980696 10.1097/01.qai.0000146599.47925.e0
26. Cu-Uvin S Hogan JW Caliendo AM Harwell J Mayer KH Carpenter CC Association between bacterial vaginosis and expression of human immunodeficiency virus type 1 RNA in the female genital tract Clin. Infect. Dis. 2001 33 6 894 896 10.1086/322613 11512096
Cu-Uvin, S. et al. Association between bacterial vaginosis and expression of human immunodeficiency virus type 1 RNA in the female genital tract. Clin. Infect. Dis. 33(6), 894–896 (2001).11512096 10.1086/322613
27. Sha BE Zariffard MR Wang QJ Chen HY Bremer J Cohen MH Female genital-tract HIV load correlates inversely with Lactobacillus species but positively with bacterial vaginosis and Mycoplasma hominis J. Infect. Dis. 2005 191 1 25 32 10.1086/426394 15592999
Sha, B. E. et al. Female genital-tract HIV load correlates inversely with Lactobacillus species but positively with bacterial vaginosis and Mycoplasma hominis. J. Infect. Dis. 191(1), 25–32 (2005).15592999 10.1086/426394
28. Cherpes TL Melan MA Kant JA Cosentino LA Meyn LA Hillier SL Genital tract shedding of herpes simplex virus type 2 in women: Effects of hormonal contraception, bacterial vaginosis, and vaginal group B streptococcus colonization Clin. Infect. Dis. 2005 40 10 1422 1428 10.1086/429622 15844064
Cherpes, T. L. et al. Genital tract shedding of herpes simplex virus type 2 in women: Effects of hormonal contraception, bacterial vaginosis, and vaginal group B streptococcus colonization. Clin. Infect. Dis. 40(10), 1422–1428 (2005).15844064 10.1086/429622
29. Bautista CT Wurapa E Sateren WB Morris S Hollingsworth B Sanchez JL Bacterial vaginosis: A synthesis of the literature on etiology, prevalence, risk factors, and relationship with chlamydia and gonorrhea infections Mil. Med. Res. 2016 3 1 4 26877884
Bautista, C. T. et al. Bacterial vaginosis: A synthesis of the literature on etiology, prevalence, risk factors, and relationship with chlamydia and gonorrhea infections. Mil. Med. Res. 3(1), 4 (2016).26877884
30. Forcey DS Vodstrcil LA Hocking JS Fairley CK Law M McNair RP Factors associated with bacterial vaginosis among women who have sex with women: A systematic review PLoS ONE 2015 10 12 e0141905 10.1371/journal.pone.0141905 26675816
Forcey, D. S. et al. Factors associated with bacterial vaginosis among women who have sex with women: A systematic review. PLoS ONE 10(12), e0141905 (2015).26675816 10.1371/journal.pone.0141905
31. Nugent RP Krohn MA Hillier SL Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation J. Clin. Microbiol. 1991 29 2 297 301 10.1128/jcm.29.2.297-301.1991 1706728
Nugent, R. P., Krohn, M. A. & Hillier, S. L. Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation. J. Clin. Microbiol. 29(2), 297–301 (1991).1706728 10.1128/jcm.29.2.297-301.1991
32. Masha SC Wahome E Vaneechoutte M Cools P Crucitti T Sanders EJ High prevalence of curable sexually transmitted infections among pregnant women in a rural county hospital in Kilifi, Kenya PLoS ONE 2017 12 3 e0175166 10.1371/journal.pone.0175166 28362869
Masha, S. C. et al. High prevalence of curable sexually transmitted infections among pregnant women in a rural county hospital in Kilifi, Kenya. PLoS ONE 12(3), e0175166 (2017).28362869 10.1371/journal.pone.0175166
33. Ibrahim S Bukar M Galadima G Audu B Ibrahim H Prevalence of bacterial vaginosis in pregnant women in Maiduguri, North-Eastern Nigeria Niger. J. Clin. Pract. 2014 17 2 154 158 10.4103/1119-3077.127424 24553023
Ibrahim, S., Bukar, M., Galadima, G., Audu, B. & Ibrahim, H. Prevalence of bacterial vaginosis in pregnant women in Maiduguri, North-Eastern Nigeria. Niger. J. Clin. Pract. 17(2), 154–158 (2014).24553023 10.4103/1119-3077.127424
34. Redelinghuys MJ Ehlers MM Dreyer AW Lombaard H Olorunju SA Kock MM A cross-sectional study on the relationship of age, gestational age and HIV infection to bacterial vaginosis and genital mycoplasma infection BMJ Open 2015 5 10 e008530 10.1136/bmjopen-2015-008530 26482771
Redelinghuys, M. J. et al. A cross-sectional study on the relationship of age, gestational age and HIV infection to bacterial vaginosis and genital mycoplasma infection. BMJ Open 5(10), e008530 (2015).26482771 10.1136/bmjopen-2015-008530
35. Abdelaziz ZA Ibrahim ME Bilal NE Hamid ME Vaginal infections among pregnant women at Omdurman Maternity Hospital in Khartoum, Sudan J. Infect. Dev. Ctries. 2014 8 04 490 497 10.3855/jidc.3197 24727516
Abdelaziz, Z. A., Ibrahim, M. E., Bilal, N. E. & Hamid, M. E. Vaginal infections among pregnant women at Omdurman Maternity Hospital in Khartoum, Sudan. J. Infect. Dev. Ctries. 8(04), 490–497 (2014).24727516 10.3855/jidc.3197
36. Konadu DG Owusu-Ofori A Yidana Z Boadu F Iddrisu LF Adu-Gyasi D Prevalence of vulvovaginal candidiasis, bacterial vaginosis and trichomoniasis in pregnant women attending antenatal clinic in the middle belt of Ghana BMC Pregnancy Childbirth 2019 19 1 1 10 10.1186/s12884-019-2488-z 30606156
Konadu, D. G. et al. Prevalence of vulvovaginal candidiasis, bacterial vaginosis and trichomoniasis in pregnant women attending antenatal clinic in the middle belt of Ghana. BMC Pregnancy Childbirth 19(1), 1–10 (2019).30606156 10.1186/s12884-019-2488-z
37. Olowe O Makanjuola O Olowe R Adekanle D Prevalence of vulvovaginal candidiasis, trichomoniasis and bacterial vaginosis among pregnant women receiving antenatal care in Southwestern Nigeria Eur. J. Microbiol. Immunol. 2014 4 4 193 197 10.1556/EUJMI-D-14-00027
Olowe, O., Makanjuola, O., Olowe, R. & Adekanle, D. Prevalence of vulvovaginal candidiasis, trichomoniasis and bacterial vaginosis among pregnant women receiving antenatal care in Southwestern Nigeria. Eur. J. Microbiol. Immunol. 4(4), 193–197 (2014).10.1556/EUJMI-D-14-00027
38. Kurewa NE Mapingure MP Munjoma MW Chirenje MZ Rusakaniko S Stray-Pedersen B The burden and risk factors of sexually transmitted infections and reproductive tract infections among pregnant women in Zimbabwe BMC Infect. Dis. 2010 10 1 8 10.1186/1471-2334-10-127 20044936
Kurewa, N. E. et al. The burden and risk factors of sexually transmitted infections and reproductive tract infections among pregnant women in Zimbabwe. BMC Infect. Dis. 10, 1–8 (2010).20044936 10.1186/1471-2334-10-127
39. Machado D Castro J Martinez-de-Oliveira J Nogueira-Silva C Cerca N Prevalence of bacterial vaginosis in Portuguese pregnant women and vaginal colonization by Gardnerella vaginalis PeerJ. 2017 5 e3750 10.7717/peerj.3750 28875084
Machado, D., Castro, J., Martinez-de-Oliveira, J., Nogueira-Silva, C. & Cerca, N. Prevalence of bacterial vaginosis in Portuguese pregnant women and vaginal colonization by Gardnerella vaginalis. PeerJ. 5, e3750 (2017).28875084 10.7717/peerj.3750
40. Dadhwal V Hariprasad R Mittal S Kapil A Prevalence of bacterial vaginosis in pregnant women and predictive value of clinical diagnosis Arch. Gynecol. Obstet. 2010 281 101 104 10.1007/s00404-009-1089-x 19381663
Dadhwal, V., Hariprasad, R., Mittal, S. & Kapil, A. Prevalence of bacterial vaginosis in pregnant women and predictive value of clinical diagnosis. Arch. Gynecol. Obstet. 281, 101–104 (2010).19381663 10.1007/s00404-009-1089-x
