Diversity & Dynamics of the Human Vaginal Microbiota. Johanna B. Holm, PhD University of Maryland Baltimore Institute for Genome Sciences
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1 Diversity & Dynamics of the Human Vaginal Microbiota Johanna B. Holm, PhD University of Maryland Baltimore Institute for Genome Sciences
2 Host - Microbe Interactions, The Metaorganism Bosch & McFall-Ngai, Zoology 2013
3 Human Vagina - Microbe Interactions Bosch & McFall-Ngai, Zoology 2013
4 Host epithelial cell What is the vaginal microbiota? Patient with Normal Clinical Exam L: Lactobacillus type p b Spiegel, Amsel, Holmes, 1983
5 What is the vaginal microbiota? Patient with Normal Clinical Exam L: Lactobacillus type g: Gardnerella type Spiegel, Amsel, Holmes, 1983
6 What is the vaginal microbiota? Patient with Normal Clinical Exam L: Lactobacillus type g: Gardnerella type p: gram-positive cocci b: gram-negative rods Patient diagnosed with Bacterial Vaginosis p b Spiegel, Amsel, Holmes, 1983
7 Bacterial Vaginosis Condition of unknown etiology Disturbance of vaginal microbial ecology Replacement of Lactobacillus predominant flora with an overgrowth of Gardnerella vaginalis and mixed anaerobic organisms The most common cause of symptomatic vaginal discharge in reproductive age women Associated with a variety of conditions including post-surgical infection, pelvic inflammatory disease, preterm birth and HIV acquisition Definition modified from Klebanoff et al. 2010
8 What is the vaginal microbiota? Patient with Normal Clinical Exam L: Lactobacillus type g: Gardnerella type p: gram-positive cocci b: gram-negative rods Patient diagnosed with Bacterial Vaginosis p b Spiegel, Amsel, Holmes, 1983
9 Vaginal - Microbe Interactions Mechanisms of protection by microbiota: Fermentation of sugars to lactic acid => low ph Lactobacillus spp., but also : Atopobium, Streptococcus, Staphylococcus, Megasphaera, and Leptotrichia Produce antimicrobials (i.e. bacteriocin peptides) Lactobacillus competitively exclude other bacteria and yeast from adhering to epithelial cells (Boris et al. 1998) Simplified for clarity Lactobacillus absent Lactobacillus present # Adhering to vaginal epithelial cells Candida albicans Gardnerella vaginalis 22.5 ± ± ± 3 8 ± 3
10 Metataxonomic Profiling, 16S rrna gene A dot is one sequenced amplicon Taxonomic Assignment Lactobacillus crispatus Lactobacillus iners BVAB1 Bifidobacterium breve Mycoplasma genitalium Atopobium Megasphaera
11 Species come and go over time Within a woman, microbial composition can be dynamic. Lactobacillus iners Lactobacillus crispatus Prevotella Anaerococcus Aerococcus Sneathia Lactobacillus jensenii Gardnerella Gemella Actinomyces Proportion of Microbiota Gajer, Brotman, et al Compare one time point across many women
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13 Proportion of Microbiome Ravel et al. 2011
14 Microbial compositions can be diverse. 396 Women: 97 Hispanic 97 Asian 104 Black 98 White Proportion of Microbiome Vaginal Community State Types CST I: Lactobacillus crispatus CST II: Lactobacillus gasseri CST III: Lactobacillus iners CST IV: non-lactobacillus CST V: Lactobacillus jensenii Ravel et al. 2011
15 Microbial compositions can be diverse. Proportion of Microbiome Vaginal Community State Types Many taxa = High Diversity = High Diversity Index Diversit y Index 1 0 Ravel et al. 2011
16 Microbial compositions can be diverse. CST distribution differ among ethnic groups (χ 2 = 36.8 on 10 df P <.0001)
17 What affects dynamics and diversity of vaginal microbiota?
18 What affects dynamics and diversity of vaginal microbiota? Host Physiology Host Behavior Age Menstrual Cycle Pregnancy Smoking Exposure to HIV Exposure to Chlamydia
19 Age Reviewed by Petrova, et al. 2013
20 Age - Menopause Vulvovaginal Atrophy (VVA) Thinning Sturdee et al. 2010
21 Age - Menopause Vulvovaginal Atrophy (VVA) Lack of lubrication Dryness Soreness Spotting Thinning
22 Age - Menopause Genitourinary Syndrome of Menopause Vulvovaginal Atrophy (VVA) Lack of lubrication Dryness Soreness Spotting Thinning
23 Age - Menopause Genitourinary Syndrome of Menopause Vulvovaginal Atrophy (VVA) Thinning What happens to the microbiota in menopausal women?
24 Age - Menopause 87 Women 30 pre-menopausal 29 peri-menopause 28 post-menopause Brotman, et al. 2014
25 Age - Menopause Postmenopausal women are more likely to be classified as CST IV versus CST I CST I L. crispatus CST II & CST V L. gasseri L. jensenii CST III L. iners CST IV non-lactobacillus Brotman, et al. 2014
26 Age - Menopause There is an association between non-lactobacillus vaginal microbiota and menopause stage
27 Age - Menopause There is an association between non-lactobacillus vaginal microbiota and menopause stage There is an association between non-lactobacillus vaginal microbiota Vulvovaginal Atrophy Reviewed by Petrova, et al. 2013
28 Age - Menopause Does lower Lactobacilli spp and VVA increase susceptibility to infection? There is an association between non-lactobacillus vaginal microbiota and menopause stage There is an association between non-lactobacillus vaginal microbiota Vulvovaginal Atrophy
29 Menstruatio n How are the vaginal microbiota affected by menstruation?
30 Menstruatio n 32 women Self Collected 2x/week 16 weeks
31 Menstruatio n Diversity Menses Diversity Menses Time (weeks) Time (weeks)
32 Menstruatio n Menses Gajer, Brotman, et al. 2014
33 Menstruatio n Instability Stability Menses Vaginal microbiota most dynamic during menses Gajer, Brotman, et al. 2014
34 Menstruatio n Vaginal microbiota most dynamic during menses Instability Stability Menses Does instability mean susceptibility? Gajer, Brotman, et al. 2014
35 Pregnancy How dynamic is the vaginal microbiota throughout pregnancy? Gajer, Brotman, et al. 2014
36 Pregnancy Pregnant / Not Pregnant 32 Non-pregnant 22 Pregnant More Lactobacillus in pregnant women Proportion of Microbiome Romero et al. 2014
37 Pregnancy Lc Lg Li db Lj More stability as pregnancy progresses Romero et al. 2014
38 What affects dynamics and diversity of vaginal microbiota? Host Physiology Age Microbial diversity increases with menopause (reduced estrogen) Menstrual Cycle Microbiota more dynamic with menses (unstable) Pregnancy Microbiota less diverse and dynamic with pregnancy
39 What affects dynamics and diversity of vaginal microbiota? Host Physiology Age Microbial diversity increases with menopause (reduced estrogen) Menstrual Cycle Microbiota more dynamic with menses (unstable) Pregnancy Microbiota less diverse and dynamic with pregnancy
40 What affects dynamics and diversity of vaginal microbiota? Host Physiology Host Behavior Age Menstrual Cycle Pregnancy Smoking Exposure to HIV Exposure to Chlamydia
41 What affects dynamics and diversity of vaginal microbiota? Host Physiology Host Behavior Age Menstrual Cycle Pregnancy Smoking Exposure to HIV Exposure to Chlamydia
42 Smoking Artist Kevin Berlin, East Meets West #2
43 Smoking Non-Smokers Smokers 20 Non-Smokers & 20 Smokers Brotman et al., 2014
44 Smoking 20 Non-Smokers & 20 Smokers Non-Smokers Smokers I III IV I III IV Smokers were 25-fold more likely to have low proportions of vaginal Lactobacillus sp. (CST IV) Proportion of Microbiota Brotman et al., 2014
45 Smoking Metabolome Biogenic Amines (BAs) can allow various bacteria to survive in low ph environments, and enhance growth rates of pathogens
46 Smoking Metabolome Biogenic Amines (BAs) can allow various bacteria to survive in low ph environments, and enhance growth rates of pathogens BA - Putrescine BA - Cadaverine Non-smoker Smoker Log Relative Concentration of Vaginal Metabolites +/- SE Biogenic Amines are Increased in Smokers Joanna Borgogna PhD student Carl Yeoman, PhD
47 Smoking Smoking increases the diversity of vaginal microbiota Brotman et al., 2014
48 Smoking Smoking increases the diversity of vaginal microbiota Do women who smoke have increased susceptibility? Brotman et al., 2014
49 Sexually Transmitted Infections Vaginal microbiota & HIV
50 STIs In 2020, million new HIV infections WHO, 2016
51 STIs - Cervicovaginal mucus (CVM), the vaginal microbiota and HIV-1 CVM is critical to reproductive health as a lubricant and possibly as a line of defense against STIs HIV must penetrate CVM to reach target cells in the vaginal epithelium CVM that immobilizes HIV virions can directly reduce or even prevent initial infection Some women appear better protected than others What role does CVM play in protection against HIV infection?
52 STIs - Cervicovaginal mucus (CVM), the vaginal microbiota and HIV-1 CVM collected from 31 women HIV-like Particles Mobile HIV-like Particles Trapped n=14 n=17 Nunn et al. 2015
53 STIs - Cervicovaginal mucus (CVM), the vaginal microbiota and HIV-1 What was the difference between CVM samples? Nunn et al. 2015
54 STIs - Cervicovaginal mucus (CVM), the vaginal microbiota and HIV-1 Nunn et al. 2015
55 L. crispatus L. iners G. vaginalis L. jensenii L. gasseri Others STIs - Cervicovaginal mucus (CVM), the vaginal microbiota and HIV Group Group Group Other Group 1 Group 2 Group 3 L. crispatus L. iners G. vaginalis L. jensenii L. gasseri Others Nunn et al. 2015
56 L. crispatus L. iners G. vaginalis L. jensenii L. gasseri Others STIs - Cervicovaginal mucus (CVM), the vaginal microbiota and HIV Group Group Group Other Group 1 Group 2 Group 3 L. crispatus L. iners G. vaginalis L. jensenii L. gasseri Others Nunn et al. 2015
57 L. crispatus L. iners G. vaginalis L. jensenii L. gasseri Others STIs - Cervicovaginal mucus (CVM), the vaginal microbiota and HIV Group Group Group Other Group 1 Group 2 Group 3 L. crispatus L. iners G. vaginalis L. jensenii L. gasseri Others Nunn et al. 2015
58 L. crispatus L. iners G. vaginalis L. jensenii L. gasseri Others STIs - Cervicovaginal mucus (CVM), the vaginal microbiota and HIV Group 1 Group 2 Group L. crispatus dominated communities enhance virus trapping relative to G. vaginalis and L. iners dominated communities Other Group 1 Group 2 Group 3 L. crispatus L. iners G. vaginalis L. jensenii L. gasseri Others What s the deal with Lactobacillus iners communities? Nunn et al. 2015
59 STIs - Cervicovaginal mucus (CVM), the vaginal microbiota and HIV-1 Vaginal microbiota alter the composition of CVM, enhancing protection from HIV infection Nunn et al. 2015
60 STIs - Cervicovaginal mucus (CVM), the vaginal microbiota and HIV-1 Vaginal microbiota alter the composition of CVM, enhancing protection from HIV infection All Lactobacillus species were not created equal Nunn et al. 2015
61 Sexually Transmitted Infections Vaginal microbiota & Chlamydia
62 Sexually Transmitted Infections A healthy vaginal microbiota is thought to be the first line of defense against STI Estimated rate of transmission after contact with a partner infected by C. trachomatis is estimated to be 25-40%, even lower for HIV (Katz et al. 1992)
63 STIs Chlamydia trachomatis (CT) infections 324 & Enrolled 222 CT + Visit 1 CHARM Project Questionnaire Vaginal/Cervical SamplesTreatment (Az) Visit 2 (3 months): 129 CT + 93 CT -
64 STIs Chlamydia trachomatis (CT) infections CHARM Project How did the microbiota differ between Visit 1 and Visit 2 for women that cleared CT?
65 STIs Chlamydia trachomatis (CT) infections
66 STIs Chlamydia trachomatis (CT) infections Following CT infection and azithromycin treatment women switch from CST IV to CST III
67 STIs Chlamydia trachomatis (CT) infections CT+ women (Visit 1) CT- (cleared) women (Visit 2)
68 STIs Chlamydia trachomatis (CT) infections CT+ women (Visit 1) Why are women with L. iners dominated microbiota susceptible to infection by CT?
69 STIs Chlamydia trachomatis (CT) infections CT+ women (Visit 1) Chlamydia infection is associated with a low Lactobacillus state. Following clearance of Chlamydia infection by antibiotics, Lactobacillus iners dominated states are common.
70 Conclusio ns Regarding factors of host physiology: Estrogen = Lactobacillus & Microbial Stability = Microbial Diversity
71 Conclusio ns CST IV: a normal state that carries risks? Smoking, reduced trapping of HIV by CVM, and Chlamydia infection associated But at any given time, 25% of women are in this state
72 Conclusio ns Lactobacillus iners dominated communities show less protective properties (higher ph, lower lactic acid) Strain-level differences All Lactobacilli are not created equal
73 Acknowledgmen ts Dr. Jacques Ravel Dr. Rebecca Brotman
74 California Golden gorgonian Prof Brian Cox! Golden gorgonian novel polyp symbionts Video: J. Holm Microbiota Kelp Water Golden gorgonian Brown gorgonian
75 Hormonal Contraceptives Hormonal Contraceptives are associated with decreased prevalence of Bacterial Vaginosis Rifkin, et al., 2009; Riggs et al., 2007; Baeten et al. 2001; Klebanoff
76
77
78 Hormonal Contraceptives
79 Hormonal Contraceptives Hormonal Contraceptives are associated with decreased prevalence of Bacterial Vaginosis How do the microbiota change? Rifkin, et al., 2009; Riggs et al., 2007; Baeten et al. 2001; Klebanoff
80 Hormonal Contraceptives 125 women Sampled prior to and after onset of oral HC use Preliminary Data: 11 women PI: Khalil Ghanem, MD, PhD Rebecca Brotman, PhD, MPH
81 Hormonal Contraceptives CST I: Lactobacillus crispatus CST II: Lactobacillus gasseri CST III: Lactobacillus iners CST IV: non-lactobacillus CST V: Lactobacillus jensenii PI: Khalil Ghanem, MD, PhD Time (normalized) Rebecca Brotman, PhD, MPH
82 Hormonal Contraceptives Trends of increasing Lactobacillus spp. and decreasing CST IV with oral HC s PI: Khalil Ghanem, MD, PhD CST I: Lactobacillus crispatus CST II: Lactobacillus gasseri CST III: Lactobacillus iners CST IV: non-lactobacillus CST V: Lactobacillus jensenii Time (normalized) Rebecca Brotman, PhD, MPH
83 Temporal Dynamics of Vaginal Microbiota 32 women self-collected, 2x/week 16 weeks Time (weeks) Gajer, Brotman, et al. 2014
84 Temporal Dynamics of Vaginal Microbiota JSD = Jensen-Shannon Divergence Index = Vaginal Community Stability over time = Stability (for this talk) Time (weeks) JSD (stability) Gajer, Brotman, et al. 2014
85 Temporal Dynamics of Vaginal Microbiota High JSD = Low Stability Regardless of community state type! Time (weeks) JSD (stability) Gajer, Brotman, et al. 2014
86 Longitudinal trajectories of 4 women who completed the 16-week smoking cessation intervention Brotman, BMC ID, 2014
87 Biogenic Amines are Increased in CST IV Smokers Putrescine Cadaverine Key Log Relative Concentration of Vaginal Metabolites +/- SE Non-smoker Smoke r Biosynthesis of BAs can allow various bacteria to survive in low ph environments. BAs have also been shown to enhance growth rates of various pathogenic bacteria, and shield them from host innate immunological defenses. Women who smoke, and particularly smokers with BV, may have increased susceptibilities to STIs. Joanna Borgogna PhD student Carl Yeoman, PhD
88 The feminine product aisle
89 Brotman et al, STI, 2010
90 Many lubricants and their ingredients have overall component concentrations (osmolalities) higher than those of the human body Wolf, Chemical and Engineering News 2012
91 Vaginal lubricants are widely used and vastly understudied Most lubricants are formulated with high concentrations of humectants (glycerol, propylene glycol) that make them markedly hypertonic to mucosal epithelia. These concentrated humectants make the lubricants feel comfortably warm when applied. Hypertonic lubricants have molecular concentrations higher than in the body s cells, causing cells to shrink and die, and increasing mucosal susceptibility to infection. There is little in vivo evidence available on how the vaginal or rectal ecosystems respond to lubricant use. Epidemiologic studies suggest vaginal lubricants are associated with development of BV.
92 Gynecology and Lubricant Effects Study (GALE) Recruiting women presenting for TVUS Standardized product and confirmation of dose and date Observational study of women enrolled in HMP Evaluating vaginal microbiota, lactic acid isomers, immunology and epithelial shell shedding
93 Hormonal Contraception Longitudinal (HCL) Study
94 Contraceptive Use: Immune Responses & Vaginal Microbiota PI: Khalil Ghanem N=125 women and >4500 samples Table 1. Association between hormonal contraception and community state type (CST) compared to women on no HC in a longitudinal study CST Dominant bacteria OCP Ring Implant I L. crispatus II L. gasseri III L. iners IV-A* Low-Lactobacillus IV-B* Low-Lactobacillus V L. jensenii CSTs reflect the clustering of samples based on bacterial composition and abundance. * CST IV-A is characterized by various species of anaerobic bacteria including Anaerococcus, Peptoniphilus and Prevotella spp., whereas CST IV-B had higher proportions of bacteria from the genera Gardnerella, Atopobium and Megasphaera among others. The "+" is increased, "-" is decreased and 0 is not statistically significant. Pre Enroll 2wk 4wk 3m 6m 12m 18m 24m -screen
95 Longitudinal profile of all women on the HCL study over 2 years. (n=108 women)
96 HCL study: Change in CST over time with OCP initiation, (n=11 women and 385 observations). There are drops in CST IV-B and increases in CST III.
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