You are viewing the site in preview mode

Skip to main content

Sexually transmitted infections and bacterial vaginosis in women of child-bearing age in Antananarivo, Madagascar: prevalence and risk factors from a cross-sectional study

Abstract

Background

Recent data on sexually transmitted infections (STIs) and bacterial vaginosis (BV) in the general population of Madagascar is scarce. Our objective is to estimate the Chlamydia trachomatis (CT), Neisseria gonorrhoeae (NG), Trichomonas vaginalis (TV), Mycoplasma genitalium (MG), and BV prevalence among women and to determine associated risk factors.

Methods

We recruited women aged 18–45 years consulting at a hospital in Antananarivo in a cross-sectional study. We collected socio-demographic and behavioral data. Vaginal swabs were collected for each individual. STIs were detected by qPCR and BV using the Nugent score. We explored factors associated with having an STI using logistic regressions.

Results

Of the 501 recruited women, 242 (48%) were married. Only one woman in three ever used condoms. The prevalence of CT was 11.8% (95% Confidence Interval: 9.0, 14.6), NG: 4.2% (2.4, 5.9), TV: 14.8% (11.7, 17.9), MG: 8.2% (5.8, 10.6), and BV: 39.6% (35.3, 43.9). Factors associated with an STI were having sex in exchange for favors (adjusted Odds Ratio (aOR): 4.25, 95%CI: 1.27, 16.6), BV (aOR: 2.14, 95%CI: 1.34, 3.47) or intermediate vaginal microbiota (aOR: 2.10, 95%CI: 1.19, 3.72), and being in a non-marital relationship compared to married (aOR: 1.86, 95%CI: 1.16, 2.98).

Conclusions

To address the high prevalence of STIs, prevention programs should target women who are more likely to engage in sex in exchange for favors and empower them with negotiation skills on condom use. Given the elevated prevalence of dysbiosis and its association with STIs, it is crucial to prioritize research efforts toward a comprehensive understanding of this relationship.

Peer Review reports

Background

Women in Africa are strongly affected by STIs, with more than 34 million prevalent cases of Chlamydia trachomatis (CT), Neisseria gonorrhoeae (NG), and Trichomonas vaginalis (TV) [1]. At the global level, women in Africa bear the highest prevalence of gonorrhea and trichomoniasis [1]. Only few studies have estimated the prevalence of Mycoplasma genitalium (MG) among women in Africa which was estimated to 3.20% in Tanzania [2]and 2.70% in Madagascar [3].

These STIs may result in urethritis, cervicitis, and pelvic inflammatory disease (PID). PID, in particular, can evolve into infertility, ectopic pregnancy, and chronic pelvic pain [4]. Infection during pregnancy is related to adverse pregnancy outcomes such as miscarriage or preterm delivery and in the newborn, low birth weight and neonatal infections such as pneumonia and conjunctivitis [5,6,7].

BV is a dysbiosis of the vaginal microbiota characterized by a replacement of Lactobacilli spp. by anaerobic bacteria such as Gardnerella vaginalis, Fannyhessea vaginae, and Mycoplasma hominis [8]. Global prevalence of BV ranges from 23 to 29% across regions and reaches 25% in sub-Saharan Africa [9]. Similarly to STIs, BV can lead to adverse health outcomes. During pregnancy, BV is associated with an increased risk of preterm birth, fetal death, and perinatal infections [8].

Multiple factors influence the risk of STI acquisition. In African countries, inconsistent condom use, multiple sexual partners, new relationships, lack of knowledge about STIs, and alcohol consumption have been reported to be associated with STIs [10,11,12,13].

Specifically in Madagascar, epidemiological data on STIs in the general population remains scarce. Although some studies on syphilis and HPV in the country have recently been published [14,15,16], to the best of our knowledge, the latest study on CT, NG, TV, MG, and BV was published in 2005 on a study conducted in 2002 [3], more than two decades ago. This study also explored risk factors and found that women and young age (15–24 years) were associated with STIs; however, it did not investigate social, behavioral, or biological factors.

This paper thus addresses the current lack of epidemiological data and understanding of factors associated with STIs in Madagascar. We provide recent estimates on the prevalence of CT, NG, TV, MG, and BV in women of child-bearing age who attended a hospital in Antananarivo. Additionally, we investigated the factors associated with the presence of at least one of the four tested STIs.

Methods

Study design

We conducted a cross-sectional study between March and November 2022 at the outpatient and family planning departments of the Gyneco-Obstetrics Befelatanana University Hospital (CHUGOB) in Antananarivo, the capital city of Madagascar. We chose this University teaching hospital since it serves as the primary referral center for gynecology and obstetrics. This study was a feasibility study for a larger trial on the evaluation of a rapid diagnostic test, the Genital InFlammation Test (GIFT), which aims to detect genital inflammation in women.

Study procedures

Our inclusion criteria were women aged 18 to 45 years, excluding pregnant women. Women with metrorrhagia or bleeding during examination or swabbing were also excluded because the presence of blood on the swab could interfere with pathogen detection. Menstruating women or women who had their last day of menstruation in the past three days were invited to return at a later date to the hospital for enrolment. Lastly, we excluded women who had taken antibiotics in the past 30 days as they would have cleared the pathogen but fragments of pathogens’ DNA could still be detectable and would yield false positive cases.

Participants answered a questionnaire in Malagasy that was administered in a dedicated consultation room by either a nurse or a midwife, both of whom had clinical research experience. The questionnaire included questions on socio-demographic data, sexual history, and risk behavior information. Following the interview, a gynecologist or midwife inquired about symptoms, conducted a genital examination, and documented clinical signs.

Clinicians followed established procedures and prescribed treatment for suspected STIs. If the clinician did not initially suspect an STI but the laboratory (Experimental Bacteriology Unit (UBEX), Institut Pasteur in Madagascar (IPM)) later identified it on samples, participants were notified by phone to collect treatment at the hospital for free. Testing and enrollment did not involve any charges or incentives for the participants.

The gynecologist and the midwives collected three vaginal specimens with a speculum in place. One cotton and two Copan flocked® swabs (Copan, Brescia, Italy) were used to collect vaginal fluid from the lateral vaginal wall. The two flocked swabs were introduced simultaneously to detect CT, NG, TV, MG, and the fungal infection by Candida albicans (CA). The national STI/AIDS program offered HIV testing with capillary blood [17].

To test for BV, a cotton swab was used to prepare immediately after collection a vaginal smear for Nugent scoring. The vaginal smear was heat-fixated for 1 min on a heating plate at 40 °C and stored at room temperature until transport to UBEX at IPM.

Copan flocked swabs were kept at 2–8 °C until transport. The transport of swabs to UBEX was done on the same day using a cool box and icepacks, where they were stored at -20 °C until testing.

Laboratory methods

After thawing one flocked swab per participant, the vaginal secretions were eluted for at least 15 s in 1.2 ml of diluted phosphate-buffered saline (dPBS) (pH 7.4–1:9, PBS: saline). We extracted the DNA from an aliquot of 200 µL using the QUICK-DNA HMW magbead kit (Zymo Research, USA) according to the manufacturer’s instructions. We used Presto CT/NG (Goffin Molecular Technologies, Beesd, The Netherlands) for the detection of CT and NG, according to the manufacturer’s procedure. We used previously published methods for the detection of TV, MG, and CA [18,19,20]. We utilized the CFX platform (Bio-Rad, California, USA) for all amplifications.

We Gram-stained the fixated vaginal smear and examined it using the Nugent score. BV was defined by a Nugent score of above or equal to 7, an intermediate microbiota by a score between 4 and 6, and optimal vaginal microbiota by a score below 4.

Statistical methods

We determined the sample size using the prevalence of CT, NG, TV, MG, and BV from former studies conducted in Madagascar [3, 21]. For each pathogen, we employed a precision of 0.05 for prevalence rates equal to or exceeding 10% and a precision of 0.025 for rates below 10%, using two-sided 95% confidence intervals. The largest required sample size, 470, was retained and it was increased to 515 in order to accommodate potential attrition or sample loss.

We determined the prevalence of the infections and their Wald 95% confidence intervals (CI). We defined the outcome as having an STI, i.e., a positive test for either CT, NG, TV, or MG. We described the socio-demographic characteristics, behaviors, and medical features of participants. We compared those infected by an STI and those with no STI using Chi-2 or, in the case the application conditions were not met, the Fisher test. We created three age groups using standard categories for ease of comparison with other studies: 18–24, 25–34, and 35-45 [3, 12, 22]. We conducted univariable analyses to explore the associations between socio-demographic and behavioral characteristics of the participant and the outcome. Finally, we performed multivariable logistic regression to examine associations with STI infection, adjusting for age. We included the variables with p ≤ 0.2 in the univariable analyses to build the final model using a backward approach. For all the logistic regressions conducted, our measures of effect were odd ratios (OR) in univariable analysis and adjusted odd ratios (aOR) for multivariable analysis. The statistical significance of variables in the final model was assessed at the 0.05 level. We used R (version 4.1.1) to perform the analyses.

This study followed the STROBE statement.

Ethical consideration

The ethical committee (Comité d’Ethique de la Recherche Biomédicale, CERBM) in Madagascar approved the study protocol (N° 124-MSANP/SG/AMM/CERBM). All participants gave their informed consent prior to joining the study.

Results

Between March and November 2022, 529 eligible women attended the CHUGOB. Among them, 14 did not consent to participate in the study, five bled during vaginal swabbing, three were positive for pregnancy after testing, three were lost to follow-up between the interview and sampling, and three withdrew consent, resulting in 501 included women (Fig. 1). Two-thirds of the women were recruited at the outpatient department (339/501, 68%), and a third were recruited at the family planning service (162/501, 32%). The main reasons for attending the outpatient department were abnormal vaginal discharge (220/339, 64.9%), lower abdominal pain (89/339, 26.3%), infertility (57/339, 16.8%), gynecological check-up (39/339, 11.5%), and abnormal vaginal bleeding (32/339, 9.4%) (Supplementary Fig. 1). We compared the most common reasons for attendance among women with STIs or BV and women without these conditions and found that 17% women with no STI/BV came for a gynecological check-up versus 6.8% of women with STI/BV (p = 0.003) (Supplementary Table 1). Additionally, we compared the prevalence of each STI, CA, and BV in the outpatient and family planning department and found no evidence of a difference, except for CA (19.2% at the outpatient department versus 8.6% at the family planning, p = 0.004) (Supplementary Fig. 2).

Fig. 1
figure 1

Number and selection of women attending CHUGOB, Antananrivo, 2022

* These women already participated in the study and were no longer eligible to participate again. Per study design, women could be included only once

Study participants characteristics

The median age was 27 years (interquartile range (IQR): 23–32). More than half of the participants went at least to high school (132/501, 26%) or had higher education (189/501, 38%) (Table 1). A third of the participants (160/501, 32%) were employed by the public service or companies, whereas 151/501 (30%) owned their own businesses. The majority of them were either married (242/501, 48%) or in a non-marital relationship (191/501, 38%). In contrast, 68/501 (14%) were single or divorced. Most never used condoms (355/501, 71%). Although the majority of the women declared that they had a permanent partner (471/501, 94%) and lived with them for more than a year (444/501, 89%), concomitant partners were not uncommon with 61/444 (14%) of the latter stating they had other partners in the past 12 months. Similarly, 127/444 (28%) indicated that their permanent partner had other partners in the past 12 months. Circumcision among permanent partners was extremely common (460/471, 98%). Previous STIs were self-reported by 46/501 (9%) of the participants. Of note, 74/501 (15%) of the women declared having ever experienced forced sexual intercourse.

Table 1 Characteristics of women attending CHUGOB included in the study, stratified by infection status, Antananarivo, 2022

Prevalence of CT, NG, TV, MG, BV, and vaginal CA

The prevalence of CT was 11.8% (59/501, 95% CI: 9.0, 14.6), for NG 4.2% (21/501, 95%CI: 2.4, 5.9), for TV 14.8% (74/501, 95%CI: 11.7, 17.9), and for MG 8.2% (41/501, 95%CI: 5.8, 10.6). For BV, 11 vaginal smears contained too little material; consequently, the Nugent score could not be interpreted. Of the available samples, the prevalence was 39.6% (194/490, 95%CI: 35.3, 43.9). The prevalence of vaginal CA was 15.8% (79/501, 95%CI: 12.6, 19.0). Due to a shortage of HIV tests, only the first 281 women were tested, and among them, two were HIV seropositive, resulting in an HIV prevalence of 0.7% (95%CI: 0.1, 2.5).

We identified that 152/501 (30.3%) women had at least one infection by CT, NG, TV, or MG. Thirty women (35/501, 7.0%) had a dual infection, with the combinations of CT-NG and CT-TV being the most common co-infections (8/30 each).

When stratifying by age category, we observed that as age increased, CT prevalence decreased (p = 0.004). A similar but not significant trend was observed for TV and MG (Fig. 2).

Fig. 2
figure 2

Prevalence of CT, NG, TV, MG, CA, and BV by age groups, with 95% confidence intervals, among women attending CHUGOB, Antananarivo, 2022

* Denominator is 182 for BV in 18–24 age group

† Denominator is 218 for BV in 25–34 age group

‡ Denominator is 90 for BV in 35–45 age group

Among women with an STI, 92/152 (60.5%) had at least one symptom that corresponded to the entry points of the WHO syndromic management algorithms for the investigated STIs: vaginal discharge syndrome (which includes: abnormal vaginal discharge and/or irritation and/or pruritus) and lower abdominal pain [23]. Of the infected women, 60/152 (39.5%) were asymptomatic. Among the women with abdominal pain, 25% were infected by TV.

Risk factors associated with STIs

We conducted the analyses on complete data (n = 463), excluding participants with missing BV results (11/501, 2.2%) and those who preferred not to answer or did not know the response to specific questions (27/501, 5.4%). We compared age, education, marital status, activity, and STI status between those excluded and included in the risk factors analysis and found no differences in the socio-demographic characteristics (Supplementary Table 2).

In the multivariable analysis, adjusting for age, we found that women in a relationship but not married had 86% increased odds of having an STI compared to married women (aOR: 1.86, 95%CI: 1.16, 2.98, p = 0.01) (Table 2). We found that the odds of having an STI were 2.14 higher in those with BV compared to those with an optimal microbiota (95%CI: 1.34, 3.47, p = 0.002); likewise, women with intermediate microbiota had twice the odds of having an STI (aOR: 2.10, 95%CI: 1.19, 3.72, p = 0.010). Lastly, women who had sex in exchange for favors (e.g., money, goods, or jobs) had 4-fold increased odds of having an STI (aOR: 4.25, 95%CI: 1.27, 16.6, p = 0.019). Following this result, we then compared the socio-demographic characteristics of women who had sex in exchange for favors with those who did not. We found that women who had sex in exchange for favors had a lower education level than the other women (p = 0.008). Analysis of factors associated with each STI separately showed that CT was associated with younger age, NG with sex in exchange for favors and TV with sex in exchange for favors and perturbation of the vaginal microbiota (Supplementary Tables 35). No factor was found to be associated with MG.

Table 2 Factors associated with at least one of CT, NG, TV, or MG among 463 women attending CHUGOB in Antananarivo, 2022

Discussion

We identified a high prevalence of STIs in women of child-bearing age attending CHUGOB in Antananarivo. One third of the women were infected with at least one STI.

We estimated the prevalence of CT and NG to be 11.8% (95%CI: 9.0, 14.6) and 4.2% (2.4, 5.9), respectively. Our findings are similar to those determined in rural Madagascar (for which we calculated the 95%CI): 9.3% (95%CI: 6.4, 13.0) and 5.4% (3.2, 8.4), respectively [3]. In our study, the prevalence of MG exceeded that reported in this study (8.2% [5.8, 10.6] compared to 2.7% [1.2, 5.1]). Conversely, the prevalence of TV was lower in our investigation (14.8% [11.7, 17.9]) compared to the cited study (23.4% [19.0, 28.3]). However, these estimates must be compared critically, since the two studies were conducted 20 years apart, and one in the capital city and the other in rural areas. BV prevalence in our study (39.6% [35.3, 43.9]) was consistent with findings among women in rural Madagascar (33.0% [28.0, 38.4]) [3] and very similar to estimates found in the rest of Africa [24].

In a meta-analysis that estimated STI prevalence among women in different African regions, our figures were closer to the estimates found among young women in East Africa and at high risk, i.e., recruited from recreational facilities or engaged in transactional sex [24]. The prevalence of CT in our study was similar to the estimate for this high-risk group: 10.3% (7.4, 14.1). Likewise, we found a TV prevalence of 14.8% (11.7, 17.9), comparable to the 12.7% (7.5, 20.6) estimate among women at risk.

The prevalence of MG in our study was 8.2% (5.8, 10.6), which was higher than the estimate found in Tanzania (3.2% [2.8, 4.2]) [2], but comparable to those in pregnant women in Sub-Saharan Africa (13.5% [4.0, 27.2]) [25]. However, it was lower than estimates from adolescents and young women at risk (< 25 years) in South Africa (22.1% [19.3, 25.2]) [26] but more than six times higher than in countries with high development index (1.3% [1.0 to 1.8]) [27].

Our results raise concerns about the broad circulation of STIs among Malagasy women of child-bearing age. The average level of education in the participants of our study was higher than the level representative samples of women from Antananarivo [28], which may lead them to be better informed of their health issues or STI-associated risk behaviors and consult more often. Thus, we may have not captured women with intermediate to high risk of STI, and consequently the true prevalence of STI may be even more substantial than the one we observed.

6% of the women were co-infected by two STIs or more, a result that is much lower in our study in Madagascar than other studies conducted in Tanzania (19%) [29] and South Africa (14%) [30]. Consequences of a dual infection remain unclear. The simultaneous presence of STIs can complicate diagnosis and treatment, and the potential effects on long-term health outcomes have yet to be studied.

Among factors related to having an STI, we found that being in a relationship was associated with an increased odds of having an STI, using being married as the reference. This association can be explained by a higher number of concurrent partners among unmarried women in couple: our data shows that 5.7% of the married women had other partners in the past 12 months, compared with 20.3% of unmarried women in a relationship. Relationships that overlap in time are not uncommon among unmarried young individuals in Madagascar [31] and have been shown to be associated with an increased risk of STIs compared to single relationships [32].

Although sex in exchange for favors concerned only less than 3% of the participants, the magnitude of this association was the highest among all explored risk factors. The proportion of women who declared having ever exchanged sex for favors in our study was comparable to another study conducted in Antananarivo among the 15-24-year (5.9%).31 The proportion of women who exchanged sex for favors in our study is consistent with demographic health surveys (DHS) data in Africa summarized in a meta-analysis where 4.34% (3.16, 5.51) of the women were concerned [33]. Analyses of the features of those women in our data showed an association with low education, a factor also stressed in the meta-analysis [33]. Women with low education may have difficulty finding a job or have jobs with low pay, and they may therefore turn to selling sex as a complementary income.

Lastly, we found that the women with BV or intermediate microbiota had twice the odds of having an STI compared to women with an optimal microbiota, an association extensively documented in previous studies [34, 35] However, it remains unclear whether BV increases susceptibility to STIs or if STIs predispose individuals to BV. Several cohort studies have investigated the incidence of STIs in women with BV, reporting a higher risk of CT, NG, and TV infections [36]. From a biological standpoint, this association may be attributed to BV-associated reductions in lactobacilli, which normally produce antimicrobial compounds, as well as the activity of sialidase and mucinase enzymes produced by BV-associated bacteria that compromise immune and physical barriers [37]. Conversely, other studies have reported an elevated risk of BV among women with STIs [38]. Further research is needed to elucidate the underlying immunological and mechanistic pathways by which these conditions influence each other.

Our findings provide additional context on the demographic distribution of STIs. Women aged 18–24 years were more likely to have a CT infection than those aged 35–45. This asymmetric burden among people below 25 years has also been documented in national surveillance data in the United States [39] and in a large study in China [22]. This increased risk among young women can be explained by behavioral factors such as a higher number of sexual partners, but also biological factors such as cervical ectopy [40].

We also observed that condoms were rarely used, a finding shared by other studies conducted in Madagascar [41, 42]. In the study conducted by Rahamefy et al., low condom use was justified by steady relationships; [42] however, our study did not find a difference in condom use between married and unmarried women. According to the last DHS conducted in Madagascar, condom uptake with a partner that was neither the spouse nor the person they were living with increases with education: it ranges from 1.2% among those who have never been to school to 12.6% among those who went to university [28]. When comparing with other African countries, a study pointed out that, out of 18 countries, Madagascar has the lowest condom use among men aged 15–29 years at last intercourse and the lowest percentage of men who know about condoms [41]. Historically, the Malagasy society was influenced by Christian values and condom use was not favorably regarded. This attitude may have endured over time, shaping cultural perceptions and impacting sexual health practices [43].

Paradoxically, despite high proportions of STIs, the prevalence of HIV in our study was low (0.7%) and consistent with the estimate found in a study conducted between 2010 and 2015 in Madagascar (0.4%) [15]. Low HIV prevalence could be explained by the isolated island status of Madagascar and the fact that most men are circumcised. While evidence that circumcision is protective against HIV has been established, a recent review found mixed evidence against the acquisition and transmission of CT or NG and no evidence against MG [44].

One of our important results is that nearly 40% of the women with an STI did not present with symptoms of the WHO syndromic management guidelines. This result indicates that, outside the context of our study, a substantial fraction of the women with an STI would remain untreated, as they showed no symptoms, and they may develop complications and sustain the transmission of STIs. We also noted that among women with lower abdominal pain, one in four were infected by TV. Other studies have also reported an association between TV and lower abdominal pain [45, 46]. However, the WHO guidelines recommend treatment only for only for CT, NG, bacteria associated with BV, and MG in case of lower abdominal pain [23]. The importance of lower abdominal pain in TV infection warrants further investigation.

Our study had several limitations. Firstly, we conducted this study in the capital city, and the results may not be representative of the women in Madagascar. In our study population, 88% of the participants went to middle school or above, whereas at the national level, only 31% of girls do [28]. However, the DHS shows that knowledge on HIV prevention and condom uptake increases with the level of education [28]. Therefore, women included in our study may be less at risk for STIs, and our estimates, which were already high, may be even higher in the Malagasy female population.

Secondly, our questionnaire contained sensitive questions which have likely caused social desirability bias. This bias may have affected the associations in our analysis.

Despite these limitations, this study has several strengths. It is the first study on CT, NG, TV, and MG among women who are not sex workers, in the past twenty years [3]. Additionally, we had no missing data for determining the prevalence rates except for BV, for which the inability to analyze the samples was due to random events. We found no difference in characteristics between the 95% of participants with complete data and the 5% with incomplete data. Thus, we believe our results are strongly reliable. Finally, the laboratory team was rigorously trained, and emphasis was made on the quality of the procedures using the most recent recommendation for the detection of the pathogens.

In conclusion, the high prevalence of STIs in this urban, educated female population showed a need for intervention and prevention, such as the promotion of and negotiation skills on condom use for both men and women who have occasional partners, especially those who exchange sex for favors. Young people should be targeted in priority due to their higher likelihood of being infected and their misconceptions about condoms [47].

Further studies on the prevalence of STIs and HIV in other cities and rural areas should be considered, especially in Southern regions where polygamy and extramarital relationships are far more common. Similarly, STI diffusion could follow a different pattern in coastal cities where sex tourism is common [48]. A comprehensive picture of the epidemiology of STIs, including HIV, at the country level is needed to serve as a guide for future public health prevention and intervention programs.

Data availability

The datasets used and analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

aOR:

Adjusted Odds Ratio

BV:

Bacterial vaginosis

CA:

Candida albicans

CT:

Chlamydia trachomatis

CHUGOB:

Gyneco-Obstetrics Befelatanana University Hospital

DHS:

Demographic and Health Surveys

HIV:

Human Immunodeficiency Virus

IPM:

Institut Pasteur de Madagascar

MG:

Mycoplasma genitalium

NG:

Neisseria gonorrhoeae

STIs:

Sexually Transmitted infections

TV:

Trichomonas vaginalis

UBEX:

Experimental Bacteriology Unit

WHO:

World Health Organization

References

  1. Newman L, Rowley J, Vander Hoorn S, et al. Global estimates of the prevalence and incidence of four curable sexually transmitted infections in 2012 based on systematic review and global reporting. PLoS ONE. 2015;10(12):e0143304. https://doiorg.publicaciones.saludcastillayleon.es/10.1371/journal.pone.0143304.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Kapiga SH, Sam NE, Mlay J, et al. The epidemiology of HIV-1 infection in northern Tanzania: results from a community-based study. AIDS Care. 2006;18(4):379–87. https://doiorg.publicaciones.saludcastillayleon.es/10.1080/09540120500465012.

    Article  CAS  PubMed  Google Scholar 

  3. Leutscher P, Jensen JS, Hoffmann S, et al. Sexually transmitted infections in Rural Madagascar at an early stage of the HIV Epidemic: a 6-Month Community-Based Follow-Up study. Sex Transm Dis. 2005;32(3):150–5. https://doiorg.publicaciones.saludcastillayleon.es/10.1097/01.olq.0000152820.17242.17.

    Article  PubMed  Google Scholar 

  4. Van Gerwen OT, Muzny CA, Marrazzo JM. Sexually transmitted infections and female reproductive health. Nat Microbiol. 2022;7(8):1116–26. https://doiorg.publicaciones.saludcastillayleon.es/10.1038/s41564-022-01177-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. He W, Jin Y, Zhu H, Zheng Y, Qian J. Effect of Chlamydia trachomatis on adverse pregnancy outcomes: a meta-analysis. Arch Gynecol Obstet. 2020;302(3):553–67. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s00404-020-05664-6.

    Article  CAS  PubMed  Google Scholar 

  6. Vallely LM, Egli-Gany D, Wand H, et al. Adverse pregnancy and neonatal outcomes associated with Neisseria gonorrhoeae: systematic review and meta-analysis. Sex Transm Infect. 2021;97(2):104–11. https://doiorg.publicaciones.saludcastillayleon.es/10.1136/sextrans-2020-054653.

    Article  PubMed  Google Scholar 

  7. Van Gerwen OT, Craig-Kuhn MC, Jones AT, et al. Trichomoniasis and adverse birth outcomes: a systematic review and meta-analysis. BJOG Int J Obstet Gynaecol. 2021;128(12):1907–15. https://doiorg.publicaciones.saludcastillayleon.es/10.1111/1471-0528.16774.

    Article  Google Scholar 

  8. Abou Chacra L, Fenollar F, Diop K. Bacterial Vaginosis: What Do We Currently Know? Front Cell Infect Microbiol. 2022;11. Accessed September 8, 2022. https://www.frontiersin.org/articles/https://doiorg.publicaciones.saludcastillayleon.es/10.3389/fcimb.2021.672429

  9. Peebles K, Velloza J, Balkus JE, McClelland RS, Barnabas RV. High global burden and costs of bacterial vaginosis: a systematic review and Meta-analysis. Sex Transm Dis. 2019;46(5):304–11. https://doiorg.publicaciones.saludcastillayleon.es/10.1097/OLQ.0000000000000972.

    Article  PubMed  Google Scholar 

  10. Chadambuka A, Chimusoro A, Maradzika JC, Tshimanga M, Gombe NT, Shambira G. Factors associated with contracting sexually transmitted infections among patients in Zvishavane urban, Zimbabwe; 2007. Afr Health Sci. 2011;11(4):535–42.

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Ohene O, Akoto IO. Factors associated with sexually transmitted infections among young Ghanaian women. Ghana Med J. 2008;42(3). https://doiorg.publicaciones.saludcastillayleon.es/10.4314/gmj.v42i3.43619.

  12. Kassie BA, Yenus H, Berhe R, Kassahun EA. Prevalence of sexually transmitted infections and associated factors among the University of Gondar students, Northwest Ethiopia: a cross-sectional study. Reprod Health. 2019;16(1):163. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12978-019-0815-5.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Oyeyemi OT, Fadipe O, Oyeyemi IT. Trichomonas vaginalis infection in Nigerian pregnant women and risk factors associated with sexually transmitted infections. Int J STD AIDS. 2016;27(13):1187–93. https://doiorg.publicaciones.saludcastillayleon.es/10.1177/0956462415611292.

    Article  PubMed  Google Scholar 

  14. Seña AC, Wolff M, Behets F, et al. Rate of decline in Nontreponemal Antibody Titers and Seroreversion after treatment of early Syphilis. Sex Transm Dis. 2017;44(1):6–10. https://doiorg.publicaciones.saludcastillayleon.es/10.1097/OLQ.0000000000000541.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Bigoni J, Catarino R, Benski C, et al. High burden of human papillomavirus infection in Madagascar: comparison with other sexually transmitted infections. Infect Dis Res Treat. 2018;11:1178633717752686. https://doiorg.publicaciones.saludcastillayleon.es/10.1177/1178633717752686.

    Article  Google Scholar 

  16. Kutz JM, Rausche P, Rasamoelina T, et al. Female genital schistosomiasis, human papilloma virus infection, and cervical cancer in rural Madagascar: a cross sectional study. Infect Dis Poverty. 2023;12(1):89. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s40249-023-01139-3.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Direction de la Lutte contre les IST. et le Sida. Politique, Normes, et Procédure des Services de Depistage du VIH à Madagascar. Published online 2018.

  18. Crucitti T, Van Dyck E, Tehe A, et al. Comparison of culture and different PCR assays for detection of Trichomonas Vaginalis in self collected vaginal swab specimens. Sex Transm Infect. 2003;79(5):393–8. https://doiorg.publicaciones.saludcastillayleon.es/10.1136/sti.79.5.393.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Müller EE, Venter JME, Magooa MP, Morrison C, Lewis DA, Mavedzenge SN. Development of a rotor-gene real-time PCR assay for the detection and quantification of Mycoplasma genitalium. J Microbiol Methods. 2012;88(2):311–5. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.mimet.2011.12.017.

    Article  CAS  PubMed  Google Scholar 

  20. Cools P, Jespers V, Hardy L, et al. A multi-country cross-sectional study of vaginal carriage of Group B Streptococci (GBS) and Escherichia coli in Resource-Poor settings: Prevalences and Risk factors. PLoS ONE. 2016;11(1):e0148052. https://doiorg.publicaciones.saludcastillayleon.es/10.1371/journal.pone.0148052.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Behets F, Andriamiadana J, Rasamilalao D, et al. Sexually transmitted infections and associated socio-demographic and behavioural factors in women seeking primary care suggest Madagascar’s vulnerability to rapid HIV spread. Trop Med Int Health. 2001;6(3):202–11. https://doiorg.publicaciones.saludcastillayleon.es/10.1046/j.1365-3156.2001.00690.x.

    Article  CAS  PubMed  Google Scholar 

  22. Chen H, Luo L, Wen Y, et al. Chlamydia trachomatis and human papillomavirus infection in women from Southern Hunan Province in China: a large observational study. Front Microbiol. 2020;11:827. https://doiorg.publicaciones.saludcastillayleon.es/10.3389/fmicb.2020.00827.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Guidelines for the management of symptomatic sexually transmitted infections – 2021. Accessed October 4. 2023. https://www.who.int/publications-detail-redirect/9789240024168

  24. Torrone EA, Morrison CS, Chen PL, et al. Prevalence of sexually transmitted infections and bacterial vaginosis among women in sub-saharan Africa: an individual participant data meta-analysis of 18 HIV prevention studies. PLOS Med. 2018;15(2):e1002511. https://doiorg.publicaciones.saludcastillayleon.es/10.1371/journal.pmed.1002511.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Nyemba DC, Haddison EC, Wang C, Johnson LF, Myer L, Davey DJ. Prevalence of curable STIs and bacterial vaginosis during pregnancy in sub-saharan Africa: a systematic review and meta-analysis. Sex Transm Infect. 2022;98(7):484–91. https://doiorg.publicaciones.saludcastillayleon.es/10.1136/sextrans-2021-055057.

    Article  PubMed  Google Scholar 

  26. Shipitsyna E, Kularatne R, Golparian D et al. Mycoplasma genitalium prevalence, antimicrobial resistance-associated mutations, and coinfections with non-viral sexually transmitted infections in high-risk populations in Guatemala, Malta, Morocco, Peru and South Africa, 2019–2021. Front Microbiol. 2023;14. Accessed December 7, 2023. https://www.frontiersin.org/articles/https://doiorg.publicaciones.saludcastillayleon.es/10.3389/fmicb.2023.1130762

  27. Baumann L, Cina M, Egli-Gany D, et al. Prevalence of Mycoplasma genitalium in different population groups: systematic review andmeta-analysis. Sex Transm Infect. 2018;94(4):255–62. https://doiorg.publicaciones.saludcastillayleon.es/10.1136/sextrans-2017-053384.

    Article  PubMed  Google Scholar 

  28. Statistique, Madagascar (EDSMD-V). (INSTAT) IN de la, ICF. Enquête démographique et de santé à 2021. Published online August 15, 2022. Accessed October 25, 2023. https://dhsprogram.com/publications/publication-FR376-DHS-Final-Reports.cfm

  29. Hokororo A, Kihunrwa A, Hoekstra P, et al. High prevalence of sexually transmitted infections in pregnant adolescent girls in Tanzania: a multi-community cross-sectional study. Sex Transm Infect. 2015;91(7):473–8. https://doiorg.publicaciones.saludcastillayleon.es/10.1136/sextrans-2014-051952.

    Article  PubMed  Google Scholar 

  30. Hoffman CM, Mbambazela N, Sithole P, et al. Provision of Sexually Transmitted Infection Services in a Mobile Clinic reveals high Unmet need in remote areas of South Africa: a cross-sectional study. Sex Transm Dis. 2019;46(3):206–12. https://doiorg.publicaciones.saludcastillayleon.es/10.1097/OLQ.0000000000000931.

    Article  PubMed  Google Scholar 

  31. Stoebenau K, Nair RC, Rambeloson V, Rakotoarison PG, Razafintsalama V, Labonté R. Consuming sex: the association between modern goods, lifestyles and sexual behaviour among youth in Madagascar. Glob Health. 2013;9:13. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/1744-8603-9-13.

    Article  Google Scholar 

  32. Kelley SS, Borawski EA, Flocke SA, Keen KJ. The role of sequential and concurrent sexual relationships in the risk of sexually transmitted diseases among adolescents. J Adolesc Health off Publ Soc Adolesc Med. 2003;32(4):296–305. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/s1054-139x(02)00710-3.

    Article  Google Scholar 

  33. Mihretie GN, Kassa BG, Ayele AD, et al. Transactional sex among women in Sub-saharan Africa: a systematic review and meta-analysis. PLoS ONE. 2023;18(6):e0286850. https://doiorg.publicaciones.saludcastillayleon.es/10.1371/journal.pone.0286850.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Wiesenfeld HC, Hillier SL, Krohn MA, Landers DV, Sweet RL. Bacterial vaginosis is a strong predictor of Neisseria gonorrhoeae and Chlamydia trachomatis infection. Clin Infect Dis off Publ Infect Dis Soc Am. 2003;36(5):663–8. https://doiorg.publicaciones.saludcastillayleon.es/10.1086/367658.

    Article  Google Scholar 

  35. Ness RB, Kip KE, Soper DE, et al. Bacterial vaginosis (BV) and the risk of incident gonococcal or chlamydial genital infection in a predominantly black population. Sex Transm Dis. 2005;32(7):413–7. https://doiorg.publicaciones.saludcastillayleon.es/10.1097/01.olq.0000154493.87451.8d.

    Article  PubMed  Google Scholar 

  36. Feldblum PJ, Lie CC, Weaver MA, et al. Baseline factors associated with incident HIV and STI in four microbicide trials. Sex Transm Dis. 2010;37(10):594–601.

    Article  PubMed  Google Scholar 

  37. Briselden AM, Moncla BJ, Stevens CE, Hillier SL. Sialidases (neuraminidases) in bacterial vaginosis and bacterial vaginosis-associated microflora. J Clin Microbiol. 1992;30(3):663–6. https://doiorg.publicaciones.saludcastillayleon.es/10.1128/jcm.30.3.663-666.1992.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Cherpes TL, Meyn LA, Krohn MA, Lurie JG, Hillier SL. Association between acquisition of herpes simplex virus type 2 in women and bacterial vaginosis. Clin Infect Dis off Publ Infect Dis Soc Am. 2003;37(3):319–25. https://doiorg.publicaciones.saludcastillayleon.es/10.1086/375819.

    Article  Google Scholar 

  39. National Overview of STDs. 2021. May 16, 2023. Accessed December 11, 2023. https://www.cdc.gov/std/statistics/2021/overview.htm

  40. Quinn TC, Gaydos C, Shepherd M, et al. Epidemiologic and microbiologic correlates of Chlamydia trachomatis infection in sexual partnerships. JAMA. 1996;276(21):1737–42. https://doiorg.publicaciones.saludcastillayleon.es/10.1001/jama.1996.03540210045032.

    Article  CAS  PubMed  Google Scholar 

  41. Bankole A, Singh S, Hussain R, Oestreicher G. Condom use for preventing STI/HIV and unintended pregnancy among young men in Sub-saharan Africa. Am J Mens Health. 2009;3(1):60–78. https://doiorg.publicaciones.saludcastillayleon.es/10.1177/1557988308322394.

    Article  PubMed  Google Scholar 

  42. Rahamefy OH, Rivard M, Ravaoarinoro M, Ranaivoharisoa L, Rasamindrakotroka AJ, Morisset R. Sexual behaviour and condom use among university students in Madagascar. SAHARA J J Soc Asp HIVAIDS Res Alliance. 2008;5(1):28–35. https://doiorg.publicaciones.saludcastillayleon.es/10.1080/17290376.2008.9724899.

    Article  Google Scholar 

  43. Rakotomalala M. A coeur ouvert sur la sexualité Merina (Madagascar). Une anthropologie du non-dit. Karthala.; 2012. Accessed April 17, 2023. https://www.decitre.fr/livres/a-coeur-ouvert-sur-la-sexualite-merina-madagascar-9782811105990.html

  44. Matoga M, Hosseinipour MC, Jewett S, Hoffman IF, Chasela C. Effects of HIV Voluntary Medical Male Circumcision Programs on sexually transmitted infections. Curr Opin Infect Dis Published Online Dec. 2020;10. https://doiorg.publicaciones.saludcastillayleon.es/10.1097/QCO.0000000000000696.

  45. Kissinger P. Trichomonas vaginalis: a review of epidemiologic, clinical and treatment issues. BMC Infect Dis. 2015;15(1):307. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12879-015-1055-0.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Schwebke JR, Burgess D, Trichomoniasis. Clin Microbiol Rev. 2004;17(4):794–803. https://doiorg.publicaciones.saludcastillayleon.es/10.1128/CMR.17.4.794-803.2004.

  47. Klinger A, Asgary R. Perceptions and attitudes regarding sexually transmitted infection and family planning among adolescents in Northern Madagascar. Women Health. 2017;57(5):599–613. https://doiorg.publicaciones.saludcastillayleon.es/10.1080/03630242.2016.1178684.

    Article  PubMed  Google Scholar 

  48. Stoebenau K. Côtier sexual identity as constructed by the urban Merina of Antananarivo, Madagascar. Études Océan Indien. 2010;4593–115. https://doiorg.publicaciones.saludcastillayleon.es/10.4000/oceanindien.909.

Download references

Acknowledgements

The authors are grateful to the participants and thank the study doctors, midwives, and nurses at CHUGOB, and the IPM personnel.

Funding

This work was supported by the European Union (European and Developing Countries Clinical Trials 2 - EDCTP2 n° RIA2020I-3297). The views and opinions of authors expressed herein do not necessarily state or reflect those of EDCTP.

Author information

Authors and Affiliations

Authors

Contributions

CF designed the study, analyzed the data, and wrote the manuscript.ANH designed the study and supervised the coordination.SBR supervised the coordination.TFR coordinated the study.HLA coordinated the study.RTM supervised data quality.DTR developed the electronic case report forms and ensured data quality.LFR coordinated and carried out the biological analysis.TTR carried out the biological analysis.LR carried out the biological analysis. BTH contributed to the design, the analysis, the results, and the writing of the manuscript.RVR contributed to the design, the implementation, the analysis, the results and the writing of the manuscript, and supervised the field study.TC contributed to the design, the implementation, the analysis, the results and the writing of the manuscript, and supervised the biological analyses.

Corresponding author

Correspondence to Camille Fortas.

Ethics declarations

Ethics approval and consent to participate

The ethical committee (Comité d’Ethique de la Recherche Biomédicale, CERBM) in Madagascar approved the study protocol (N° 124-MSANP/SG/AMM/CERBM). All participants gave their informed consent prior to joining the study.

Consent for publication

Not applicable.

Disclosure

This work was, in part, presented at the STI & HIV 2023 world congress.

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Material 1

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fortas, C., Harimanana, A.N., Rasoanandrianina, S.B. et al. Sexually transmitted infections and bacterial vaginosis in women of child-bearing age in Antananarivo, Madagascar: prevalence and risk factors from a cross-sectional study. BMC Infect Dis 25, 262 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12879-025-10578-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12879-025-10578-2

Keywords