Background

Globally, an estimated 7.1 million new syphilis infections were reported in 2020 and the African region accounts for more than 30% of these new infections [1]. Syphilis are sexually transmitted infections (STIs) caused by Treponema pallidum, but can also be transmitted vertically, leading to adverse birth outcomes in exposed infants [1, 2]. Furthermore, syphilis is the second leading cause of preventable stillbirths worldwide and can lead to high morbidity and mortality in adults, including neurologic complications [1, 2]. In the last decade, there is a resurgence of syphilis in many parts of the world [3].

Despite the lack of global and regional data on the burden of syphilis seropositivity in people living with HIV (PLHIV), due to shared transmission routes, syphilis is one of the common coinfections in this population [3, 4]. Given these challenges, the World Health Organization (WHO) has called for the triple elimination of HIV, viral hepatitis B, and syphilis [5,6,7]. However, the global effort to eliminate syphilis as a major public health problem by 2030 is hampered by several challenges facing the health system in low-income countries [7]. Consequently, many studies in low-income countries have shown high rates of syphilis among PLHIV, reinforcing the need for robust syphilis screening programs in sub-Saharan Africa [8,9,10,11,12].

Sierra Leone has 1.7% of its population living with HIV [13]. But there are no national estimates for other STIs, including syphilis. However, data extrapolated from antenatal clinics reported a prevalence of 0.9% and estimated over 2,000 cases of congenital syphilis [14]. Studies of blood donors and military personnel have reported prevalence rates of 0.8 and 7.3%, respectively [15, 16]. Older age, HIV positivity and residence in rural settings were risk factors associated with seropositivity for syphilis in these populations [15, 16]. Nonetheless, a PubMed search on May 31, 2023 reported only one single-center study on the prevalence of syphilis in PLHIV in Sierra Leone [17]. As a low-income country with enormous health challenges and high STI risk behaviors, it is expected that the impact of syphilis on PLHIV in Sierra Leone may be more severe than reported [14, 18]. Despite these gaps in the response against syphilis and the availability of guidelines for syphilis treatment and prevention, its prevention and control has not improved in Sierra Leone. Based on these challenges, the Sierra Leone National AIDS Control Program introduced routine syphilis screening of pregnant women using a dual test kit, although coverage was limited, reaching only 50% of pregnant women [14]. Sierra Leone does not have a PLHIV-specific syphilis screening program despite recommendations from international guidelines [7]. Thus, data are needed to inform public practices. In this study, we aimed to determine the prevalence of syphilis seropositivity and factors associated with syphilis seropositivity in PLHIV in 10 public hospitals in Sierra Leone.

Materials and methods

Study design and setting

A cross-sectional study was conducted at 10 health facilities in Sierra Leone, including two primary hospitals (Jenner Wright Clinic and Waterloo Community Health Center), two secondary hospitals (Rokupa and Lumley Government hospitals), and six tertiary/regional hospitals (Connaught Hospital, Kenema Government Hospital, Makeni Government Hospital, Bo Government Hospital, Princess Christian Maternity Hospital and 34 Military Hospital).

Sierra Leone is divided into five geographic regions. The Western Area is the most populous region and includes Freetown (the capital). Of a population of 7 million, 22% (1.5 million) reside in the Western Area [19]. About 42% of the 10,350 healthcare workers employed by the government are in the Western Area [20]. Sierra Leone's public health system is divided into three levels of care, such as primary, secondary and tertiary care. The national and regional hospitals provide tertiary care [20]. There are 25 public hospitals in Sierra Leone, 10 of which provide tertiary services.

Study population and sampling technique

Adult HIV patients aged 18 years or older were sequentially recruited into the study. We excluded patients who refused consent or were in these facilities for a temporary pick up of their antiretroviral drugs. Between September 2022 and January 2023, we recruited a total of 3539 PLHIV into the study, but patients with missing data were excluded from the analysis. Consequently, details of only 3082 PLHIV were included in the final analysis. (Fig. 1).

Fig. 1
figure 1

Study participant flow diagram

Exclusion criteria for the selection of samples with complete data

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Laboratory procedure

Approximately 2–4 mL of venous blood samples were aseptically collected into sterile EDTA vacutainer tubes and analyzed at the Infectious Disease Prevention Center of the 34 Military Hospital. Plasma was separated by centrifugation at 2000 rpm for 10 min. Wondfo one step Syphilis Test Cassette (Wondfo, Guangzhou, China), a rapid test based on immunochromatography assay, was used to detect antibodies of Treponema Pallidum according to the manufacturer’s instructions. The test kit was CE (European Conformity) certified, and the sensitivity and specificity were 100% and 98%, respectively.

Definitions and measures

We define viral suppression as HIV RNA < 1000 copies per mL and unsuppressed viral load as HIV RNA ≥ 1000 copies per mL. ‘’Previously married women’ are PLHIV who were married, but are now divorced, widowed, or separated. PLHIV who are taking antiretroviral drugs are said to be currently on treatment, regardless of duration.

Data collection, management and statistical analysis

Demographic and HIV related information, including age, sex, marriage, ART regimen, HIV viral load, duration of ART treatment, and hospital level of care, were collected through paper questionnaires containing de-identified variables by trained research assistants. The collected information was entered into a password-protected Microsoft Excel sheet, accessible only to the research team.

Data were cleaned, coded and transferred to R-software version 4.2.3 (R Core Team, Vienna, Austria) for analysis. Demographic characteristics were presented as the number (%). Pearson’s χ2 test, Fisher’s exact test and Kruskal–Wallis H test were applied to assess the differences in syphilis seropositivity between groups as appropriate. Parameters of interest were antiretroviral therapy (ART), HIV viral load, duration of treatment, syphilis seropositivity, hospital level of care, marital status and age. Univariate and multivariable logistic regression analyses were used to assess factors associated with syphilis seropositivity. The multivariate logistic regression analysis adjusted for age, sex, marriage, ART regimen, duration of ART, HIV viral load and type of hospital. All statistical tests were two sided, and the level of statistical significance was set at P < 0.05.

Results

Demographic and HIV characteristics of enrolled individuals

A total of 3082 PLHIV were enrolled in our study. The demographic information is shown in Table 1. The median age was 36 years. Patients aged under 30 years and 30–40 years accounted for 32.9% and 30.7%, respectively. Most of the participants were female (74.4%), 1430 (46.4%) were married and 2867 (93.0%) were receiving ART. HIV viral load was unsuppressed in 531 (17.2%) PLHIV.

Table 1 Sociodemographic characteristics and syphilis seroprevalence among enrolled individuals in this study
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Seroprevalence of syphilis among PLHIV

Of the 3082 PLHIV screened for syphilis, 211 (6.8%, 95%CI 6.0–7.7) were positive (Fig. 2 and Table 1). The prevalence of syphilis is highest in people aged 60 and over (21.1%, 95%CI 14.7–29.2), followed by people aged 50–60 (15.5%, 95%CI 11.9–19.9). Syphilis prevalence was higher in the widowed population (11.9%, 95%CI 8.9–15.8), but there were no differences in gender, ART status, ART regimen, duration of ART, HIV viral load and level of hospital.

Fig. 2
figure 2

Syphilis seroprevalence for the combined measure by demographic variables in people living with HIV

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Factors associated with the positivity of syphilis

Older age (50–60 years: OR 3.77, 95%CI 2.49—5.72 P < 0.001; 60–100 years: OR 5.48, 95%CI 3.26—9.07, P < 0.001) was significant factors for syphilis seropositivity in univariate logistic regression analysis. On multivariable logistic regression analysis (Table 2), older age (50–60 years: adjusted OR 3.49, 95%CI 2.09—5.85 P < 0.001; 60–100 years: adjusted OR 4.28, 95%CI 2.21—8.17, P < 0.001) was still an independent predictor of seropositive syphilis. However, there were no statistical differences in gender, marital status, ART regimen, HIV viral load and level of hospital care.

Table 2 Factors associated with the risk of a positive serology of syphilis
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Discussion

We observed that the seroprevalence of syphilis among PLHIV was 6.8%. Older adults in this study were more likely to be seropositive for syphilis than younger adults but no statistical significance in the gender, ART status, marital status, and the level of HIV viral load and hospital care.

Our study has several strengths. First, it is the first large-scale study to determine the seroprevalence of syphilis among PLHIV in Sierra Leone. Second, its findings add to the global context of triple elimination of syphilis, HIV, and viral hepatitis B [21]. Third, it was a country-wide assessment of the seroprevalence of syphilis among PLHIV in the national referral, regional and district hospitals, and are likely representative of the epidemiologic situation of syphilis in Sierra Leone. Furthermore, our study provides data for comparison with findings of other studies in Africa and elsewhere. Finally, understanding the burden of syphilis is relevant to achieving the Sustainable Development Goals, particularly those focused on reducing communicable disease [22].

Our study has several policy and public health implications. It is encouraging that the reported prevalence of syphilis in this study is similar to the prevalence of syphilis among PLHIV reported in Ethiopia [23]. Although the prevalence of syphilis in our study may have been overestimated due to the limitations of the test kits in reacting to non-treponemal infections, studies in other African countries such as Nigeria (14.0%), Ghana (14.8%), Morocco (16.4%), Chad (14.0%), and Tanzania (9.6%) reported a higher prevalence [8,9,10, 24,25,26]. The disparities in these findings may be due to the different composition of the study populations and differences in the methods applied for the detection of syphilis or perhaps may reflect the variations in the risky behavioral practices across the African region.

Although there is no relevant local report on syphilis infection rates among PLHIV and non-HIV individuals. The higher incidence of syphilis in PLHIV compared with non-HIV individuals has been reported by others and is partly due to the shared risk behaviors associated with both infections [9, 24]. Therefore, the high prevalence of syphilis in PLHIV in our study indicates an ongoing involvement of this population in high-risk sexual behaviors, highlighting the need for continuous counseling of this group on consistent safe sex practices and routine screening for syphilis, given the clinical implications of this coinfection.

A slight male preponderance was observed, although it did not reach statistical significance (P = 0.6). These findings are similar to studies in Morocco and Ethiopia, but different from studies in Taiwan, Huston Texas, Brazil, Tanzania and Nigeria. We can partly explain this by the higher number of females enrolled in our study and higher number of MSM (high risk group for not only syphilis but STIs in general) enrolled in the other studies [8, 10, 23, 24, 26,27,28].

The study also noted that the prevalence of syphilis increases with age, a finding that contrasts with findings from Uganda, which reported high prevalence among young people [29]. Our findings can be explained by the fact that in our country, most STI and safe sex campaigns are targeted towards young people and key populations compared to the elderly, who because of the effectiveness and availability of ART, now live longer and healthier, with tendencies to practice unsafe sex [30]. In addition, we cannot rule out a role for the differences in health education and the service they received between young and old people. In addition, the decline in immunity with age might further compound the fragile immunity of PLHIV. Overall, this finding presents a unique opportunity to study the risk factors for syphilis and /or STIs in elderly PLHIV.

Syphilis seropositivity was lower in never married participants and high in previously married PLHIV with the highest prevalence seen in widowed PLHIV. This parallels studies in Ghana and Ethiopia [9, 31]. The reasons for the difference in syphilis prevalence between married and unmarried participants are unclear, but a Chinese study reported that marriage had a limited effect in reducing high-risk sexual behaviors [32]. This may explain the lower prevalence of syphilis among unmarried participants.

Despite its statistical insignificance, our study showed a higher seropositivity in ART naive clients, similar to studies in Canada and China [10, 11, 31]. Observations from some studies have implicated ART in enhancing susceptibility to syphilis infection, by suppressing proinflammatory response, while other studies have reported high risk sexual behaviors of PLHIV on ART due to low-risk perception, individual knowledge of HIV positivity, new HIV diagnosis, longer duration on ART and non-disclosure of HIV status to partner with counter findings in another study [33,34,35,36,37,38,39,40,41].

Finally, the seroprevalence of syphilis was higher in virally unsuppressed patients, a finding analogous to that in Tanzania [26]. Clinical stability and viral suppression may give a false sense of recovery in PLHIV which may lead them to involvement in high-risk sexual behavior [42, 43]. This calls for continuous STI and safe sex education in all PLHIV regardless of their clinical, virological or immunological success.

Our study has limitations. We did not collect clinical information related to syphilis, which made it difficult to determine the clinical presentation. The test kits used in this study did not differentiate between active or past exposure to syphilis. In addition, we only determined the syphilis seroprevalence in PLHIV, not in healthy controls. And we did not evaluate the high-risk sexual behavior of PLWH in our study. Finally, since the kit used in this study was for screening, there may be false positive reactions for non-treponemal infections such as yaws, leading to an overestimation of the burden of syphilis among PLHIV Sierra Leone. Nonetheless, we present evidence that could inform the introduction of routine screening for syphilis in PLHIV in Sierra Leone.

Conclusion

We observed a high prevalence of syphilis in PLHIV and that older adults were more likely than young people to be seropositive for syphilis. It calls for the integration of syphilis screening, treatment and prevention in HIV services as studies have reported asymptomatic and atypical presentations which can be easily missed if routine screenings are not done.