Female reproductive tract infections (FRTIs) have a high incidence among various gynecological diseases (Yan et al., 2018). FRTIs comprise (i) endogenous infection such as bacterial vaginosis (BV) and vulvovaginal candidiasis; (ii) sexually transmitted infections (STIs) such as syphilis, gonorrhea, and chlamydia; and (iii) iatrogenic infections (Moragianni et al., 2019). Worldwide, FRTIs are a major public health problem and affect predominantly young women (Torondel et al., 2018). It has been observed that the prevalence of these infections varies a lot between countries and even among regions belonging to the same country (Rabiu et al., 2010). Sequelae of untreated FRTIs affect the well-being of women, such as infertility, cervical cancer, ectopic pregnancy, stillbirth, and spontaneous abortion (Diadhiou et al., 2019). Interestingly, FRTIs seriously impact women in the Sub-Saharan African region causing around 85% infertility (Hussen et al., 2018). Helminth infections could expose the person to various infections, protect from auto-immune diseases, or decrease disease severity and influence vaccine efficacity (Moreau and Chauvin, 2010; Hartmann et al., 2019). Helminthic infections which are predominantly prevalent in Africa could therefore contribute to the establishment of infectious diseases (Arndts et al., 2015; Katawa et al., 2015; Ritter et al., 2018, 2019). The impact of helminthiasis on female reproductive health and associated diseases is widely documented. For instance, (i) Wuchereria bancrofti and Schistosoma haematobium infections were associated with an increased risk of HIV infection, and (ii) an increased prevalence of human papilloma virus (HPV) infection has been observed in the soil-transmitted helminths-endemic area of Peru (Chetty et al., 2020).

Both FRTIs and helminthic infections are co-endemic and have been shown to be highest in low- and middle-income countries (Chetty et al., 2020). Thus, this study was designed to investigate the association between FRTIs, hookworm infections, and sociodemographic factors in the central region of Togo.

This study revealed that STIs were predominantly prevalent (74.38%) in six rural villages of the central region of Togo. Serious complications of STIs are ectopic pregnancy, pelvic inflammatory disease, preterm labor, miscarriage, stillbirth, and congenital infection, and they may lead to chronic disability (such as infertility and genital cancer) and death. Here, we diagnosed 27 germs incriminated in STIs. In detail, U. parvum was the most prevalent affecting 50% of women, followed by U. urealyticum (26.5%) and M. hominis (17.5%). Those three species belong to the gender Mycoplasma, a gender of bacteria frequently isolated from the genital tract of both men and women (Kokkayil and Dhawan, 2015). In Italy, Leli et al. (2018) found that U. parvum was the most isolated mycoplasma among women with a prevalence of 38.3%, and a study in South Africa revealed that U. parvum was isolated from 72.4% vaginal samples of pregnant women (Redelinghuys et al., 2013). In general, U. parvum is associated with intrauterine inflammation (Kasper et al., 2010).

Among viruses found in the cohort, human CMV was predominately prevalent (5%). In Africa, CMV is a neglected pathogen, but its burden is important with a seroprevalence close to 100% (Bates and Brantsaeter, 2016). CMV is a member of Herpesviridae family and is classified as an emerging STI (Kent, 2017) that is transmitted through direct contact with multiple fluids of the body like saliva, urine, milk, and genital secretions. In addition, it can also be transmitted from an infected mother to her fetus (CDC, 2020b). The virus can stay latent in infected persons until the immune system weakening allows the virus to reactivate (Grinde, 2013).

In regards to risk factors, this study revealed that the use of contraceptive methods appeared as a high risk of STIs. Contraceptives are used for birth control and have a socio-economic impact. According to Deese et al. (2018) some contraceptive methods have related to STIs, but robust studies should be conducted to provide accurate information and facilitate contraceptive choice by women. Moreover, the presence of STIs was also associated with alcohol consumption, confirming other studies showing that increased risk of STIs was influenced by alcohol drinking across a wide variety of populations (Arasteh et al., 2008; Hutton et al., 2008). That is justified by the fact that alcohol drinking can lead to immune deficiency and increase sensitivity to infectious diseases (Zitkute and Bumbuliene, 2016). Another independent factor associated with STIs was the type of relationship and sexual behavior, especially the number of sexual partners during the lifetime, confirming a study in Brazil among rural women, which revealed that a higher number of partners in life was a risk factor for STIs (Oliveira et al., 2008). In addition, having had more than one partner during the lifetime appeared as a high-risk factor for HPV infections, confirming a previous study from Molano et al. (2002) who found that having had more than one regular sexual partner increased HPV infection risk (OR 1.9).

In general, HPV plays an important role as a leading cause of most cervical cancers. More than 100 types of HPV have been identified and at least 14 of them are associated as risk factors for cancer and especially 2 types (HPV 16 and HPV 18) cause 70% of cervical cancers and pre-cancerous cervical lesions (WHO, 2019). Nevertheless, in our cohort, HPV 16 and HPV 18 were less prevalent (respectively, 1.54 and 1.03%), but associations to cancer diseases need to be investigated in future studies.

Interestingly, the impact of helminth immune regulation on susceptibility to STIs is known. Given the global incidence of helminths and their detrimental impact on public health (WHO, 2017), the geographical overlap between helminth exposure and STIs might be a result of parasite-induced changes on female reproductive health (Gopinath et al., 2000; Wolday et al., 2002) and helminth-induced immunomodulation (Brown et al., 2005). Indeed, here we showed that women who had hookworm infections had a 2.22 times risk of HPV infection than those who were not infected by hookworm. Gravitt et al. (2015) found that women infected with soil-transmitted helminths (STHs) had 60% higher prevalence of HPV, compared with those without STHs infection with a prevalence ratio of 1.6. The helminth-induced Th2 response in vagina could explain the plausibility of high HPV occurrence (Gravitt et al., 2015).

Concerning endogenous infections, 31.79% of women were affected by BV and 9.85% had candidiasis. In Sokodé, the principal city of the central region of Togo, Tchelougou et al. (2013) found on pregnant women a prevalence of 55.31% of Gardnerella vaginalis and 50.77% of candidiasis, which is caused by Candida species and has been shown to be responsible for inflammatory changes in the vaginal and vulvar epithelium (Jeanmonod and Jeanmonod, 2020). However, the differences between the studies could be due to pregnancy status with unbalance vaginal flora.

In addition, BV, which is the most common vaginal condition in women aged between 15 and 44 years (CDC, 2020a), is known to increase predisposition to STIs (Lata et al., 2010; Bautista et al., 2017). In detail, it is characterized by an altered vaginal microflora including an increase in the vaginal pH, reduced lactobacilli species, and increased hydrogen peroxide producing species and facultative and anaerobic bacteria numbers and/or types (Eschenbach et al., 2000).

Interestingly, the risk probability of BV was high among those who were not married or not in a relationship and those who had multiple partners. Ranjit et al. (2018) found that 100% of unmarried women were more prone to BV, and indeed, another study revealed that BV has been associated with having three or more male sexual partners in the past 12 months (OR = 1.60, 95% CI: 1.19–2.04) (Smart et al., 2004). Moreover, the number of pregnancies more than 4 was a protective factor against BV infections. This was in line with a study conducted in Ghana where Konadu et al. (2019) found that the fact of having more than four pregnancies was protective for BV.

In a logistic regression model with monthly income and practicing paid sexual intercourse, we found that women who practiced paid sexual intercourse were at high probability risk of candidiasis. Unlike our results, Konadu et al. (2019) did not find any possible risk factor associated with candidiasis, although they did not include the practice of paid sexual intercourse as a possible risk factor. We can notice that the study population of Konadu et al. (2019) was pregnant women attending antenatal clinic, whereas our study population was exclusively non-pregnant women.

Finally, the use of condoms was a protective factor against STIs, confirming a previous study (Ginindza et al., 2017). Moreover, several studies revealed that consistent condom use was also associated with significantly decreased risk of gonorrhea, chlamydia, genital ulcer disease, BV, HPV, and pelvic inflammatory disease but did not have an impact on candidiasis (Baeten et al., 2001).

The present study had some limitations including the final samples size and one stool sample per participant.

This study depicted a high prevalence of FRTIs in six villages of the central region of Togo. Among them, STIs were predominately prevalent, and factors such as helminth infection, the use of contraceptives, the number of pregnancies, the number of partners, the monthly income, the methods of cleansing, the marital status, and alcohol drinking were associated with the occurrence of FRTIs. Local healthcare authorities must focus on women education and sensitization strategies based on these risk factors to optimize prevention and control measures against FRTIs.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

The studies involving human participants were reviewed and approved by the Comité de Bioéthique pour la Recherche en Santé (CBRS) du ministère de la santé du Togo. The patients/participants provided their written informed consent to participate in this study.

GK, AHA, CNT, PT, CV, AN’d, SA, HK, BM, and OA carried out the survey and the field work. CV, MR, GK, AHA, MO, CNT, and PT analyzed the samples. GK, MR, LEL, AH, WH, MK, YA, and SK designed the study protocol, analyzed, interpreted, and validated all the data. GK, WH, MR, CNT, and LEL wrote the manuscript which was then read and approved by all other authors. All authors contributed to the article and approved the submitted version.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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