Defining characteristics of genital health in South African adolescent girls and young women at high risk for HIV infection

PLoS One. 2019 Apr 4;14(4):e0213975. doi: 10.1371/journal.pone.0213975. eCollection 2019.

Abstract

The genital tract of African women has been shown to differ from what is currently accepted as 'normal', defined by a pH≤4.5 and lactobacilli-dominated microbiota. Adolescent girls and young women (AGYW) from sub-Saharan Africa are at high risk for HIV, and we hypothesized that specific biological factors are likely to be influential. This study aimed to compare characteristics of vaginal health in HIV-negative AGYW (16-22-years-old), from two South African communities, to international norms. We measured plasma hormones, vaginal pH, presence of BV (Nugent scoring), sexually transmitted infections (multiplex PCR for Chlamydia trachomatis, Neisseria gonorrhoea, Trichomonas vaginalis, Mycoplasma genitalium) and candidiasis (Gram stain) in AGYW (n = 298) from Cape Town and Soweto. Cervicovaginal microbiota was determined by 16S pyrosequencing; 44 genital cytokines were measured by Luminex; and cervical T-cell activation/proliferation (CCR5, HLA-DR, CD38, Ki67) was measured by multiparametric flow cytometry. 90/298 (30.2%) AGYW were negative for BV, candidiasis and bacterial STIs. L. crispatus and L. iners were the dominant bacteria in cervicovaginal swabs, and the median vaginal pH was 4.7. AGYW with L. crispatus-dominant microbiota (42.4%) generally had the lowest cytokine concentrations compared to women with more diverse microbiota (34/44 significantly upregulated cytokines). Frequencies of CCR5+CD4+ T-cells co-expressing CD38 and HLA-DR correlated positively with interleukin (IL)-6, TNF-α, GRO-α, macrophage inflammatory protein (MIP)-1α, and IL-9. While endogenous oestrogen had an immune-dampening effect on IL-6, TNF-related apoptosis-inducing ligand (TRAIL) and IL-16, injectable hormone contraceptives (DMPA and Net-EN) were associated with significantly lower endogenous hormone concentrations (p<0.0001 for oestrogen and progesterone) and upregulation of 34/44 cytokines. Since genital inflammation and the presence of activated CD4+ T cells in the genital tract have been implicated in increased HIV risk in South African women, the observed high levels of genital cellular activation and cytokines from AGYW may point towards biological factors increasing HIV risk in this region.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • CD4-Positive T-Lymphocytes / immunology
  • Cervix Uteri / cytology
  • Cervix Uteri / immunology
  • Cervix Uteri / microbiology
  • Cohort Studies
  • Cytokines / immunology
  • Cytokines / metabolism
  • Estrogens / blood
  • Estrogens / immunology
  • Female
  • HIV Infections / immunology*
  • HIV Infections / prevention & control
  • Humans
  • Hydrogen-Ion Concentration
  • Lactobacillus crispatus / immunology
  • Lactobacillus crispatus / isolation & purification
  • Microbiota / immunology*
  • Progesterone / blood
  • Progesterone / immunology
  • Risk Factors
  • South Africa / epidemiology
  • Vagina / cytology
  • Vagina / immunology
  • Vagina / microbiology*
  • Vaginosis, Bacterial / blood
  • Vaginosis, Bacterial / epidemiology*
  • Vaginosis, Bacterial / immunology
  • Women's Health / statistics & numerical data*
  • Young Adult

Substances

  • Cytokines
  • Estrogens
  • Progesterone

Grants and funding

This study was supported by grants from the European and Developing Countries Clinical Trials Partnership (EDCTP) Strategic Primer grant [SP·2011·41304·038] and the South African Department of Science and Technology [DST/CON 0260/2012]. SD was supported by the National Research Foundation (NRF) of South Africa and the Poliomyelitis Research Foundation. SLB was supported by the HIV Vaccine Trials Network SHAPe Program, the Fogarty Foundation and the South African Medical Research Council (MRC). ALW is supported by the South African Research Chairs Initiative of the Department of Science and Technology and National Research Foundation. The Desmond Tutu HIV Foundation recognizes the support from ViiV health care in their Youth Shield program. The Perinatal HIV Research Unit was supported through funding from the South African Medical Research Council. KSL was supported by the National Research Foundation of South Africa. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.