Prevalence and risk factors associated with sexually transmitted infections (STIs) among women of reproductive age in Swaziland

Globally, sexually transmitted infections (STIs) remain a significant public health problem mainly in low-income countries [1, 2]. Currently, approximately half a billion new cases occur worldwide each year [3], and more than one million STIs are acquired per day [4]. Of the estimated total of 357 million incident cases of the curable STIs world-wide, 131 million are from Chlamydia trachomatis (CT), 78 million are from Neisseria gonorrhea (NG), 5.6 million are from syphilis and 143 million are from Trichomonas vaginalis (TV) cases [3, 4]. The World Health Organization (WHO) further estimated that 8.3, 21.1 and 59.7 million new cases of CT, NG and TV infections respectively, occur in sub-Saharan Africa (SSA), with the majority of new STIs occurring among the population aged 15 to 49 years [5].

Depending on which STI and the population, in low-income countries largely in SSA, NG, CT, TV, Human papillomavirus (HPV), herpes, and syphilis increase the risk of HIV acquisition and transmission between two to eight fold [4, 6‐9]. Furthermore, the inflammation resulting from viral and non-viral STIs increases viral shedding of HIV-1 in the genital tract [10‐12] and also increases the risk of HIV-1 transmission to the sex partners [13, 14]. It is estimated that the probability of HIV transmission per sexual contact is 6% if either partner has another STI other than HIV [15] as compared to 0.2% in the absence of STIs [16]. The impact of co-infection of HPV with HIV in the SSA has increased the burden of cervical diseases (such as cervical lesions and cancer), since HIV infected women have a higher prevalence of hr-HPV [17]. Furthermore, STIs such as NG and CT are the major causes of pelvic inflammatory disease (PID) and infertility in women [4]. In low-income countries, impairments associated with STIs are a major cause of mother and child mortality and morbidity in adolescence and also during pregnancy [18, 19].

Factors affecting the spread of STIs, including HIV, have been documented in many epidemiological studies across different populations [20‐24]. STIs and HIV share the same behavioral, socioeconomic and demographic risk factors [20, 25], including age at first sexual intercourse, inconsistent condom use, having multiple sexual partners, female sex, being single and the partner’s sexual behaviour, location and culture. Furthermore, HIV infection increases the of other STIs [20, 24‐28].

There is limited information on the prevalence and risk factors associated with STIs at population level in Swaziland, the country which has the highest prevalence of HIV infection worldwide. The availability of epidemiological data on STIs and associated risk factors in this population is essential for the development of successful prevention, diagnosis and management strategies in the country [29]. This study was therefore, conducted to determine the prevalence and risk factors associated with STIs among women of reproductive age in Swaziland.

The current study in Swaziland shows a high prevalence of STIs (19.4%), corresponding to 72 990 women of reproductive age with STIs. Our data suggests that TV was the most prevalent curable STI (8.4%) among those examined in this study. Furthermore, the prevalence of HIV remains significantly high (42.7%) in this population. The prevalence of the STIs decreased with increasing age however, differences by age groups were not statistically significant. A high percentage of women infected with hr-HPV had one STI (18.8%), while 6.3% had multiple STIs. Single women were at higher risk of being infected with STIs compared to married women (26.4% vs 11.2%, p = 0.001). A proportion of the women had triple co-infection (6.3%), interact either directly with one another or indirectly via the host’s resources or immune system. Studies have demonstrated that, as compared to infections of single pathogen species, these interactions within coinfected hosts can alter the transmission, clinical progression and control of multiple infectious diseases [39, 40]. In the final logistic regression model, being employed, self-employed and hr-HPV infection status were risk factors positively associated with STIs.

In this study, we collected primary data and biological specimens using a standardized methodology. This is the first study evaluating the prevalence of STIs among women of reproductive age not attending antenatal care in Swaziland. We were able to extrapolate our results on the prevalence of STIs as well as genital warts to the female population in the same age groups of 15–49 years-old using the 2007–2030 population projections aligned to the 2014 population estimates [37]. Another strength of our study is that STIs such as NG, TV and CT were detected using the Gene Xpert PCR (Xpert CT/NG and Xpert TV) which, is a highly sensitive laboratory method for detecting genital infection. An important limitation of the study is the lack of generalizability of the results to the general Swazi female population beyond the age groups studied (15–49 years). In addition, since the study subjects were recruited from heath care facilities, it is arguable that they may not be truly representative of the general population. This could have introduced a selection bias. However, weighting was applied when reporting the summary results for the whole study sample. Lastly, the study participants were required to recall past events, which could result in compromising the accuracy of information provided, due to recall bias. Finally, due to limited resources for our study we did not genotype or test for LR-HPVs.

The high prevalence of STIs (19.4%) in this population indicates that STIs are a serious public health problem in Swaziland. Our findings were consistent with previous studies from similar populations across the Southern African Development Community region (SADC) and other sub-Saharan regions [13, 15, 41‐43]. The prevalence of each of the STIs detected among the study population was less than 10% (7.0% for CT, 6.0% for NG, 8.4% for TV and 1.4% for syphilis), but this is still high, which compared to global estimates, where the prevalence for CT among women range from 2.4 to 6.9%, NG from 0.3% to 1.2, TV from 1.9 to 7.8% and syphilis from 0.2 to 1.3 [44]. Results from the firstand second STI sentinel surveillance surveys conducted in 2003 and 2005 respectively in Swaziland, showed that the prevalence of STIs, such as CT, NG, TV and syphilis, and other reproductive tract infections, such as bacterial vaginosis and candidiasis, continue to be among the highest in the country [45, 46]. However, a decline in syphilis has been noted in recent years. According to the 11th Sentinel Surveillance report 2008, recent syphilis infection was tested using Treponema pallidum haemagglutination (TPHA), and the prevalence was 1.9% while 4.7% showed a history of syphilis infection by RPR results [47]. A comparison between the 2008 report and recent syphilis infection shows a decreasing trend (1.9%) compared to current study findings (1.4%). The high prevalence of the curable STIs in this population might be linked to the limitation of syndromic STI management, which does not give specific aetiological diagnosis; therefore, most infections are missed by this approach [48, 49]. Although syndromic management has proven to be cost-effective in resource limited settings, our findings demonstrate the evidence for the need of a strong national STIs’ surveillance system.

HIV remains one of the major public health challenges in Swaziland, with the highest prevalence among women of reproductive age [50, 51]. This high prevalence reported in our study was consistent with other studies. However, our results were slightly higher as compared to Bicego et al’s study on recent patterns in population–based HIV among women age 18–49 years (42.7% vs. 39%) [50]. In a country that has the highest HIV prevalence in the world, the challenge remains to assist uninfected individuals in gaining access to high quality prevention services, including early detection and treatment of curable STIs.

The observed high prevalence of STIs in the younger age groups as compared to the older age groups in our study is consistent with other studies [41, 52, 53]. The decreasing STIs prevalence with increasing age observed in our study, might be the results of the high susceptibility of younger women, lack of protective immune response development, and more risky behavior, such as an earlier age at first intercourse, a high number of sexual partners, and unprotected sex [52].

In this current study, single women and women living with partners (but not married) had the highest prevalence of STIs. Similar evidence has been found in other studies [54, 55]. In our multivariate analysis, married women were 60% less likely to be at risk of STIs as compared to single women (OR = 0.4). A similar outcome was found in others studies showing being married is a protective factor [48, 56].

As far as education is concerned, our findings have shown that women with a lower level of education are most likely to have an STI. Studies have shown that women with less education have an increased risk of STIs [13, 57, 58]. Kakaire et al. highlighted that women with lower education tend to lack formal employment and may be completely dependent on the male sexual partner and unable to negotiate safer sex. They are less likely to access STI preventative information and healthcare services [13]. According to Muula, unemployment may leave women with limited alternatives where they may resort to engaging in high risk behavior such as becoming sex workers or to engaging in transactional sex in which they provide sex in exchange for money and material resources from a partner [59]. However, our study found that employed and self-employed women were at high risk of STIs (OR: 2.2 and OR: 2.8 respectively) as compared to unemployed women. The types of employment might explain the high risk of STIs among employed and self-employed women in our study and the in which businesses they are involved. There is evidence suggesting that women working in high-risk occupation such bars, food facilities, guesthouses and similar facilities are at high risk of STI infection [48].

In this study, the risk associated with STIs among women with two or more sexual life-time partners was five to eight times higher as compared to women with no sexual partners in the univariate analysis. Our findings were consistent with other studies which reported that sexual activity with many partners increases the odds of STIs [53, 54]. However, the association was not statistically significant in our study following adjustment for all possible confounding factors (age, marital status, level of education, occupation, history of pregnancy, age at first sex, history of STIs, STIs treated in the past 12 months, and HIV status), which negatively confounded this relationship. There was a very high collinearity between the number of sexual partners and some of the confounding factors, which may have further affected the coefficients in the stepwise multivariable regression. Though evidence from studies done in South Africa [41, 42], Zambia [60], and Tanzania [48] has demonstrated that having more than one or concurrent lifetime sexual partners was among the risk factors associated with STIs.

Inconsistent condom use as a risk factor for STIs in women has been demonstrated in other studies [61, 62]. In contrast to our study, not using condoms with regular partners was inversely associated with STIs. The possible plausible explanation of our findings might be that, women who reported not using condoms with regular partners had one faithful partner or they had been treated for STIs prior to data collection. However, this will require further investigation. Moreover, condoms remain a critical part in a comprehensive and practical approach to the prevention of STIs [63].

HIV positive status was not associated with STIs in both analyses but when assessed by individual STIs, a significant inverse association between HIV and CT, and significant positive association between HIV and syphilis were observed. No statistically significant association between HIV and NG or TV was observed in the current study. However, studies have indicated that depending on the STI involved and the population, NG, CT, TV, HPV and syphilis increase the risk of HIV acquisition and transmission from two to eight times or more [4, 6, 7]. Furthermore, biological findings support the mechanisms for STIs increasing HIV acquisition and transmission through direct mucosal disruption, recruitment of HIV target cells to the genital tract, and by increased HIV load in plasma and genital secretions [10]. High levels of untreated STIs in sub-Saharan countries are linked to high HIV transmission rates and have been postulated to have contributed to the high prevalence of HIV in the region [16].

A vital clinical and public health consequence of our findings is that hr-HPV was the most significant risk factor associated with STIs infection in both univariate and multivariate analysis (unadj-OR = 2.1 and Adj-OR = 2.0). When assessing the association between hr-HPV and individual STIs, there was a significant positive association between hr-HPV and NG and CT. The strong association between HPV infection and STIs has been demonstrated in previous studies, where infection with hr-HPV types, was a risk factor for CT and NG infection [64‐66]. These findings are significantly of high importance for policy and prevention programmes to include HPV infection in the existing STIs prevention programmes in the country.

The curable STIs (CT, NG, TV, and syphilis), and HIV and HPV are sexually transmitted infections, which share the same transmission route and behavioural risk factors. If the curable STIs are not treated, they can lead to a variety of different health risks and greatly increase HIV/HPV transmission risk with further chronic health implications. Collectively, our data have shown the significantly high prevalence of and association between STIs and HIV/HPV coinfection, which tends to subscribe to the new concept in which HIV and HPV infections may be bi-directional, each increasing the risk of the other [67‐69] STIs increase the risk of HIV/HPV co-infection. The high hr-HPV/HIV coinfection with the curable STIs and resultant high population burden has implications for both cervical cancer and also for the United Nations (UN) sustainable development goal 3, target 3.3 (SDG 3) [70] (goal 3 aims to reduce new HIV infection through ensuring health and well-being for all, at every stage of life). The STIs are positively increasing the risk of HIV/HPV acquisition, which will make it impossible for countries like Swaziland to achieve SDG 3 target 3.3. Therefore, STIs’ control and HPV vaccination, combined with periodic HIV screening and referral to early treatment is needed to end the HIV epidemic in Swaziland.

In conclusion, although STIs may be treated and are curable, they remain a major public health challenge in Swaziland where HIV infection is highly prevalent. Our study indicates that there is a need for a comprehensive STI screening, surveillance and treatment programme in the country.