Recent Semen Exposure Impacts the Cytokine Response and Bacterial Vaginosis in Women

BackgroundThe presence of semen in the vagina from unprotected sex may influence the immune and microbial environment of the female genital tract. Inflammatory cytokine concentrations and BV-associated bacteria in female genital secretions may influence HIV risk, although the effect of recent sexual...

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Main Authors: Khanyisile Mngomezulu, Gugulethu F. Mzobe, Andile Mtshali, Farzana Osman, Lenine J. P. Liebenberg, Nigel Garrett, Ravesh Singh, Anne Rompalo, Adrian Mindel, Salim S. Abdool Karim, Quarraisha Abdool Karim, Cheryl Baxter, Sinaye Ngcapu
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-06-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2021.695201/full
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author Khanyisile Mngomezulu
Gugulethu F. Mzobe
Andile Mtshali
Farzana Osman
Lenine J. P. Liebenberg
Lenine J. P. Liebenberg
Nigel Garrett
Nigel Garrett
Ravesh Singh
Ravesh Singh
Anne Rompalo
Adrian Mindel
Salim S. Abdool Karim
Salim S. Abdool Karim
Quarraisha Abdool Karim
Quarraisha Abdool Karim
Cheryl Baxter
Cheryl Baxter
Sinaye Ngcapu
Sinaye Ngcapu
author_facet Khanyisile Mngomezulu
Gugulethu F. Mzobe
Andile Mtshali
Farzana Osman
Lenine J. P. Liebenberg
Lenine J. P. Liebenberg
Nigel Garrett
Nigel Garrett
Ravesh Singh
Ravesh Singh
Anne Rompalo
Adrian Mindel
Salim S. Abdool Karim
Salim S. Abdool Karim
Quarraisha Abdool Karim
Quarraisha Abdool Karim
Cheryl Baxter
Cheryl Baxter
Sinaye Ngcapu
Sinaye Ngcapu
author_sort Khanyisile Mngomezulu
collection DOAJ
description BackgroundThe presence of semen in the vagina from unprotected sex may influence the immune and microbial environment of the female genital tract. Inflammatory cytokine concentrations and BV-associated bacteria in female genital secretions may influence HIV risk, although the effect of recent sexual intercourse on incident BV and the cytokine milieu of cervicovaginal secretions has rarely been measured in previous studies. Here, we investigated the extent to which partner semen impacts the cytokine response and incident BV.MethodsAt baseline, we assessed the recency of semen exposure in menstrual cup supernatants by quantifying prostate specific antigen (PSA) levels using ELISA in 248 HIV-uninfected women at high risk for HIV infection. Luminex was used to measure 48 cytokines in menstrual cup supernatants and vaginal swabs to diagnose BV by Nugent score. Point-of-care screening for Chlamydia trachomatis and Neisseria gonorrhoeae was conducted using GeneXpert while OSOM was used for Trichomonas vaginalis detection. Multivariable models, adjusted for age, sexually transmitted infections, BV, current contraception use and condom use, were used to assess the impact of semen exposure on biomarkers of inflammation and BV.ResultsPresence of PSA, indicating recent semen exposure within 48 hours prior to sampling, was observed in menstrual cup supernatants of 17% (43/248) of women. Of these women, 70% (30/43) had self-reported condom use at their last sex act and 84% (36/43) had BV (Nugent score >7). PSA presence was significantly associated with prevalent BV (Relative Risk (RR), 2.609; 95% Confidence Interval (CI), 1.104 - 6.165; p = 0.029). Furthermore, women with detectable PSA had high median concentrations of macrophage inflammatory protein- beta (MIP-1α, p=0.047) and low median concentration of the stem cell growth factor beta (SCGF-β, p=0.038) compared to those without PSA.ConclusionA degree of discordance between self-reports of consistent condom use and PSA positivity was observed. There was also evidence of a relationship between recent semen exposure, BV prevalence and altered cytokine concentrations. These findings suggest that PSA, as a semen biomarker, should be taken into consideration when investigating biological markers in the female genital tract and self-reported condom use in studies on reproductive and sexual health.
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spelling doaj.art-9f9a685a0da24e9399e8117d550dc24e2022-12-21T19:23:40ZengFrontiers Media S.A.Frontiers in Immunology1664-32242021-06-011210.3389/fimmu.2021.695201695201Recent Semen Exposure Impacts the Cytokine Response and Bacterial Vaginosis in WomenKhanyisile Mngomezulu0Gugulethu F. Mzobe1Andile Mtshali2Farzana Osman3Lenine J. P. Liebenberg4Lenine J. P. Liebenberg5Nigel Garrett6Nigel Garrett7Ravesh Singh8Ravesh Singh9Anne Rompalo10Adrian Mindel11Salim S. Abdool Karim12Salim S. Abdool Karim13Quarraisha Abdool Karim14Quarraisha Abdool Karim15Cheryl Baxter16Cheryl Baxter17Sinaye Ngcapu18Sinaye Ngcapu19Centre for the AIDS Programme of Research in South Africa (CAPRISA), Nelson R Mandela School of Medicine, University of KwaZulu-Natal, Durban, South AfricaCentre for the AIDS Programme of Research in South Africa (CAPRISA), Nelson R Mandela School of Medicine, University of KwaZulu-Natal, Durban, South AfricaCentre for the AIDS Programme of Research in South Africa (CAPRISA), Nelson R Mandela School of Medicine, University of KwaZulu-Natal, Durban, South AfricaCentre for the AIDS Programme of Research in South Africa (CAPRISA), Nelson R Mandela School of Medicine, University of KwaZulu-Natal, Durban, South AfricaCentre for the AIDS Programme of Research in South Africa (CAPRISA), Nelson R Mandela School of Medicine, University of KwaZulu-Natal, Durban, South AfricaDepartment of Medical Microbiology, Nelson R Mandela School of Medicine, University of KwaZulu-Natal, Durban, South AfricaCentre for the AIDS Programme of Research in South Africa (CAPRISA), Nelson R Mandela School of Medicine, University of KwaZulu-Natal, Durban, South AfricaDepartment of Public Health, University of KwaZulu-Natal, Durban, South AfricaDepartment of Medical Microbiology, Nelson R Mandela School of Medicine, University of KwaZulu-Natal, Durban, South AfricaDepartment of Microbiology, National Health Laboratory Services, KwaZulu-Natal Academic Complex, Inkosi Albert Luthuli Central Hospital, Durban, South AfricaDepartment of Gynecology and Obstetrics, Johns Hopkins University, Baltimore, MD, United StatesCentre for the AIDS Programme of Research in South Africa (CAPRISA), Nelson R Mandela School of Medicine, University of KwaZulu-Natal, Durban, South AfricaCentre for the AIDS Programme of Research in South Africa (CAPRISA), Nelson R Mandela School of Medicine, University of KwaZulu-Natal, Durban, South AfricaDepartment of Epidemiology, Columbia University, New York, NY, United StatesCentre for the AIDS Programme of Research in South Africa (CAPRISA), Nelson R Mandela School of Medicine, University of KwaZulu-Natal, Durban, South AfricaDepartment of Epidemiology, Columbia University, New York, NY, United StatesCentre for the AIDS Programme of Research in South Africa (CAPRISA), Nelson R Mandela School of Medicine, University of KwaZulu-Natal, Durban, South AfricaDepartment of Public Health, University of KwaZulu-Natal, Durban, South AfricaCentre for the AIDS Programme of Research in South Africa (CAPRISA), Nelson R Mandela School of Medicine, University of KwaZulu-Natal, Durban, South AfricaDepartment of Medical Microbiology, Nelson R Mandela School of Medicine, University of KwaZulu-Natal, Durban, South AfricaBackgroundThe presence of semen in the vagina from unprotected sex may influence the immune and microbial environment of the female genital tract. Inflammatory cytokine concentrations and BV-associated bacteria in female genital secretions may influence HIV risk, although the effect of recent sexual intercourse on incident BV and the cytokine milieu of cervicovaginal secretions has rarely been measured in previous studies. Here, we investigated the extent to which partner semen impacts the cytokine response and incident BV.MethodsAt baseline, we assessed the recency of semen exposure in menstrual cup supernatants by quantifying prostate specific antigen (PSA) levels using ELISA in 248 HIV-uninfected women at high risk for HIV infection. Luminex was used to measure 48 cytokines in menstrual cup supernatants and vaginal swabs to diagnose BV by Nugent score. Point-of-care screening for Chlamydia trachomatis and Neisseria gonorrhoeae was conducted using GeneXpert while OSOM was used for Trichomonas vaginalis detection. Multivariable models, adjusted for age, sexually transmitted infections, BV, current contraception use and condom use, were used to assess the impact of semen exposure on biomarkers of inflammation and BV.ResultsPresence of PSA, indicating recent semen exposure within 48 hours prior to sampling, was observed in menstrual cup supernatants of 17% (43/248) of women. Of these women, 70% (30/43) had self-reported condom use at their last sex act and 84% (36/43) had BV (Nugent score >7). PSA presence was significantly associated with prevalent BV (Relative Risk (RR), 2.609; 95% Confidence Interval (CI), 1.104 - 6.165; p = 0.029). Furthermore, women with detectable PSA had high median concentrations of macrophage inflammatory protein- beta (MIP-1α, p=0.047) and low median concentration of the stem cell growth factor beta (SCGF-β, p=0.038) compared to those without PSA.ConclusionA degree of discordance between self-reports of consistent condom use and PSA positivity was observed. There was also evidence of a relationship between recent semen exposure, BV prevalence and altered cytokine concentrations. These findings suggest that PSA, as a semen biomarker, should be taken into consideration when investigating biological markers in the female genital tract and self-reported condom use in studies on reproductive and sexual health.https://www.frontiersin.org/articles/10.3389/fimmu.2021.695201/fullsemen exposureprostate specific antigengenital inflammationcytokinesbacterial vaginosis
spellingShingle Khanyisile Mngomezulu
Gugulethu F. Mzobe
Andile Mtshali
Farzana Osman
Lenine J. P. Liebenberg
Lenine J. P. Liebenberg
Nigel Garrett
Nigel Garrett
Ravesh Singh
Ravesh Singh
Anne Rompalo
Adrian Mindel
Salim S. Abdool Karim
Salim S. Abdool Karim
Quarraisha Abdool Karim
Quarraisha Abdool Karim
Cheryl Baxter
Cheryl Baxter
Sinaye Ngcapu
Sinaye Ngcapu
Recent Semen Exposure Impacts the Cytokine Response and Bacterial Vaginosis in Women
Frontiers in Immunology
semen exposure
prostate specific antigen
genital inflammation
cytokines
bacterial vaginosis
title Recent Semen Exposure Impacts the Cytokine Response and Bacterial Vaginosis in Women
title_full Recent Semen Exposure Impacts the Cytokine Response and Bacterial Vaginosis in Women
title_fullStr Recent Semen Exposure Impacts the Cytokine Response and Bacterial Vaginosis in Women
title_full_unstemmed Recent Semen Exposure Impacts the Cytokine Response and Bacterial Vaginosis in Women
title_short Recent Semen Exposure Impacts the Cytokine Response and Bacterial Vaginosis in Women
title_sort recent semen exposure impacts the cytokine response and bacterial vaginosis in women
topic semen exposure
prostate specific antigen
genital inflammation
cytokines
bacterial vaginosis
url https://www.frontiersin.org/articles/10.3389/fimmu.2021.695201/full
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