Abstract
BackgroundSchistosoma mansoni infection has been associated with increased risk of HIV transmission in African women. This association might be causal or mediated through shared socio-behavioural factors and associated co-infections. We tested the latter hypothesis in a cross-sectional pilot study in a cohort of women from a S. mansoni endemic region of Uganda. To validate the immunological effects of S. mansoni in this cohort, we additionally assessed known schistosomiasis biomarkers.MethodsHIV-uninfected non-pregnant adult women using public health services were tested for schistosomiasis using the urine circulating cathodic antigen test, followed by serology and Schistosoma spp.-specific PCR. Blood was obtained for herpes simplex virus (HSV)-2 serology, eosinophil counts and cytokine analysis. Samples collected from the genitourinary tract were used to test for classical sexually transmitted infections (STI), for bacterial vaginosis and to assess recent sexual activity via prostate-specific antigen testing. Questionnaires were used to capture a range of socio-economic and behavioral characteristics.ResultsAmong 58 participants, 33 (57%) had schistosomiasis, which was associated with elevated levels of interleukin (IL)-10 (0.32 vs. 0.19 pg/ml; p = 0.038) and a trend toward increased tumour necrosis factor (TNF) (1.73 vs. 1.42 pg/ml; p = 0.081). Eosinophil counts correlated with levels of both cytokines (r = 0.53, p = 0.001 and r = 0.38, p = 0.019, for IL-10 and TNF, respectively); the association of eosinophilia with schistosomiasis was not significant (OR = 2.538, p = 0.282). Further, schistosomiasis was associated with lower age (per-year OR = 0.910, p = 0.047), being unmarried (OR = 0.263, p = 0.030), less frequent hormonal contraceptive (HC) use (OR = 0.121, p = 0.002, dominated by long acting injectable contraceptives) and a trend to longer time since penile-vaginal sex (OR = 0.350, p = 0.064). All women infected by Chlamydia trachomatis (n = 5), were also positive for schistosomiasis (Fisher’s exact p = 0.064).ConclusionsIntestinal schistosomiasis in adult women was associated with systemic immune alterations, suggesting that associations with immunological correlates of HIV susceptibility warrant further investigation. S. mansoni associations with socio-behavioral parameters and C. trachomatis, which may alter both genital immunity and HIV exposure and/or acquisition risk, means that future studies should carefully control for potential confounders. These findings have implications for the design and interpretation of clinical studies on the effects of schistosomiasis on HIV acquisition.
Highlights
Schistosoma mansoni infection has been associated with increased risk of HIV transmission in African women
One vaginal swab was tested for Trichomonas vaginalis (Tv) using the OSOM rapid test (Sekisui Diagnostics, Framingham, USA), and a second vaginal swab was smeared onto a glass slide, air-dried and Gram’s stained to diagnose bacterial vaginosis (BV) using Nugent criteria [27]
We observed that S. mansoni in this cohort was associated with differences in several socio-behavioral factors, including hormonal contraceptive (HC) use, and C. trachomatis prevalence, which could influence genital immunity and HIV susceptibility
Summary
Schistosoma mansoni infection has been associated with increased risk of HIV transmission in African women This association might be causal or mediated through shared socio-behavioural factors and associated coinfections. Accumulating evidence suggests that schistosomiasis may increase the risk of HIV transmission through complex effects on mucosal immunity and antiviral defenses [2,3,4]. This association is seen for infection by Schistosoma haematobium, the cause of genitourinary schistosomiasis, and for S. mansoni, which predominantly affects the gut and causes intestinal/hepatic schistosomiasis [5,6,7,8,9,10]. These effects of S.mansoni on HIV acquisition in the Tanzanian studies were only seen in women, but not men [9, 11], implying that the effects on HIV susceptibility are mediated by either biological or socio-behavioral factors specific to women
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