The influence of sexual activity on the vaginal microbiota and Gardnerella vaginalis clade diversity in young women

Abstract

Objectives: To examine the influence of sexual activity on the composition and consistency of the vaginal microbiota over time, and distribution of Gardnerella vaginalis clades in young women.

Methods: Fifty-two participants from a university cohort were selected. Vaginal swabs were self-collected every 3-months for up to 12 months with 184 specimens analysed. The vaginal microbiota was characterised using Roche 454 V3/4 region 16S rRNA sequencing, and G.vaginalis clade typing by qPCR.

Results: A Lactobacillus crispatus dominated vaginal microbiota was associated with Caucasian ethnicity (adjusted relative risk ratio[ARRR] = 7.28, 95%CI:1.37,38.57,p = 0.020). An L.iners (ARRR = 17.51, 95%CI:2.18,140.33,p = 0.007) or G.vaginalis (ARRR = 14.03, 95%CI:1.22,160.69, p = 0.034) dominated microbiota was associated with engaging in penile-vaginal sex. Microbiota dominated by L.crispatus, L.iners or other lactobacilli exhibited greater longitudinal consistency of the bacterial communities present compared to ones dominated by heterogeneous non-lactobacilli (p<0.030); sexual activity did not influence consistency. Women who developed BV were more likely to have clade GV4 compared to those reporting no sex/practiced non-coital activities (OR = 11.82, 95%CI:1.87,74.82,p = 0.009). Specimens were more likely to contain multiple G.vaginalis clades rather than a single clade if women engaged in penile-vaginal sex (RRR = 9.55, 95%CI:1.33,68.38,p = 0.025) or were diagnosed with BV (RRR = 31.5, 95%CI:1.69,586.87,p = 0.021).

Conclusions: Sexual activity and ethnicity influenced the composition of the vaginal microbiota of these young, relatively sexually inexperienced women. Women had consistent vaginal microbiota over time if lactobacilli were the dominant spp. present. Penile-vaginal sex did not alter the consistency of microbial communities but increased G.vaginalis clade diversity in young women with and without BV, suggesting sexual transmission of commensal and potentially pathogenic clades.

Fig 1. Flow chart of number of specimens assessed according to sexual activity categories at enrolment and over the study duration.

Total specimens = 184. At least one act of penile-vaginal sex had to be unprotected (no condoms used) to be selected for the applicable categories. ^aincludes women engaging in digital or receptive oral sex or 100% condom use for penile-vaginal sex in addition to these practices; ^bthe number of specimens shown for each category of sexual activity are from women who remained static within a category or progressed to a new category.

Fig 2. Heat map depicting vaginal bacterial communities analysed in this study.

Heat map of proportions of bacterial taxa identified from 184 specimens from 52 participants. Values are expressed as arcsine transformed relative abundances. Nugent score categories and sexual activity categories for each specimen are indicated. Community state type (CST) groupings shown based on previous literature [4, 6, 16], where CST I aligns with specimens dominated by Lactobacillus crispatus, CST II with specimens dominated by L. gasseri, CST III with specimens dominated by L. iners, CST IV with specimens dominated by G. vaginalis and CST V with specimens dominated by L. jensenii. CST VI represents specimens dominated by other heterogeneous non-lactobacilli (predominantly Atopobium vaginae and Prevotella spp.) and CST VII specimens dominated by Bifidobacterium breve.

Fig 3. Distribution of Bray-Curtis dissimilarity scores for specimens dominated by one of five species groups.

Bray-Curtis dissimilarity scores were calculated between consecutive paired longitudinal samples over multiple time points from each participant (i.e. enrolment specimen [reference] vs month 3, month 3 [reference] vs month 6 etc.). Boxplots demonstrate the distribution of Bray-Curtis dissimilarity values (box = interquartile range; black line in box = median value; T bars = range of values) for each reference specimen dominated by Lactobacillus crispatus (LC), L. iners (LI), other Lactobacillus spp. (L. gasseri or L. jensenii; LG/LJ), Gardnerella vaginalis (GV), or other heterogeneous non-lactobacillus spp. (primarily Atopobium vaginae and Prevotella spp.; ONL).