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Current opinion in HIV and AIDS
Sep 01, 2024;19 (5): 234-240.

The vaginal microbiome and HIV transmission dynamics.

Emily M Cherenack, Courtney A Broedlow, Nichole R Klatt
Author Information
  1. Emily M Cherenack: Department of Psychiatry and Behavioral Sciences, University of Miami Miller School of Medicine, Miami, Florida.
  2. Courtney A Broedlow: Division of Surgical Outcomes and Precision Medicine Research, Department of Surgery, University of Minnesota, Minneapolis, Minnesota, USA.
  3. Nichole R Klatt: Division of Surgical Outcomes and Precision Medicine Research, Department of Surgery, University of Minnesota, Minneapolis, Minnesota, USA.
PMID: 38935063 DOI: 10.1097/COH.0000000000000869

Abstract

PURPOSE OF REVIEW: Among women, having a nonoptimal, highly diverse vaginal microbiome dominated by bacteria other than optimal Lactobacillus species such as L. crispatus or L. jensenii predicts HIV transmission. Reducing HIV acquisition among women requires a better understanding of the mechanisms through which the vaginal microbiome impacts HIV transmission dynamics and how to more effectively treat and intervene. Technological advancements are improving the ability of researchers to fully characterize interacting host-bacteria mechanisms. Consequently, the purpose of this review was to summarize the most innovative research on the vaginal microbiome and its role in HIV transmission in the past year.
RECENT FINDINGS: Studies combining multiomics, experimental, and translational approaches highlight the associations of a nonoptimal microbiome with maladaptive alterations in immune cell functioning, vaginal metabolites, host cell transcription, mucosal immunity, and epithelial barrier integrity. While there are multiple mechanisms proposed to increase HIV acquisition risk, there are virtually zero acceptable and effective treatments to improve the vaginal microbiome and immunity.
SUMMARY: Women-centered solutions to modify the vaginal microbiome and bacterial metabolites should continue to be explored as a mechanism to reduce HIV acquisition.

References

  1. UNAIDS. UNAIDS Data 2021. Geneva, Switzerland: Joint United Nations Programme on HIV/AIDS; 2021 [cited 2024 Feb 28]. Available at: https://www.unaids.org/en/resources/documents/2021/2021_unaids_data .
  2. Armstrong E, Kaul R, Cohen CR. Optimizing the vaginal microbiome as a potential strategy to reduce heterosexual HIV transmission. J Intern Med 2023; 293:433–444.
  3. Moreno De Lara L, Parthasarathy RS, Rodriguez-Garcia M. Mucosal immunity and HIV acquisition in women. Curr Opin Physiol 2021; 19:32–38.
  4. Mtshali A, Ngcapu S, Mindel A, et al. HIV susceptibility in women: the roles of genital inflammation, sexually transmitted infections and the genital microbiome. J Reprod Immunol 2021; 145:103291.
  5. Armstrong E, Kaul R. Beyond bacterial vaginosis: vaginal lactobacilli and HIV risk. Microbiome 2021; 9:239.
  6. Atashili J, Poole C, Ndumbe PM, et al. Bacterial vaginosis and HIV acquisition: a meta-analysis of published studies. AIDS 2008; 22:1493–1501.
  7. Brown BP, Feng C, Tanko RF, et al. Copper intrauterine device increases vaginal concentrations of inflammatory anaerobes and depletes lactobacilli compared to hormonal options in a randomized trial. Nat Commun 2023; 14:499.
  8. Gosmann C, Anahtar MN, Handley SA, et al. Lactobacillus-deficient cervicovaginal bacterial communities are associated with increased HIV acquisition in young South African women. Immunity 2017; 46:29–37.
  9. McClelland RS, Lingappa JR, Srinivasan S, et al. Evaluation of the association between the concentrations of key vaginal bacteria and the increased risk of HIV acquisition in African women from five cohorts: a nested case-control study. Lancet Infect Dis 2018; 18:554–564.
  10. Wang Y, Noël-Romas L, Perner M, et al. Non Lactobacillus -dominant and polymicrobial vaginal microbiomes are more common in younger South African women and predictive of increased risk of human immunodeficiency virus acquisition. Clin Infect Dis 2023; 76:1372–1381.
  11. Arnold KB, Burgener A, Birse K, et al. Increased levels of inflammatory cytokines in the female reproductive tract are associated with altered expression of proteases, mucosal barrier proteins, and an influx of HIV-susceptible target cells. Mucosal Immunol 2016; 9:194–205.
  12. Hladik F, Sakchalathorn P, Ballweber L, et al. Initial events in establishing vaginal entry and infection by human immunodeficiency virus type-1. Immunity 2007; 26:257–270.
  13. Cheu RK, Gustin AT, Lee C, et al. Impact of vaginal microbiome communities on HIV antiretroviral-based preexposure prophylaxis (PrEP) drug metabolism. PLoS Pathog 2020; 16:e1009024.
  14. Klatt NR, Cheu R, Birse K, et al. Vaginal bacteria modify HIV tenofovir microbicide efficacy in African women. Science 2017; 356:938–945.
  15. Serebrenik J, Wang T, Hunte R, et al. Differences in vaginal microbiota, host transcriptome, and proteins in women with bacterial vaginosis are associated with metronidazole treatment response. J Infect Dis 2021; 224:2094–2104.
  16. Holm JB, France MT, Gajer P, et al. Integrating compositional and functional content to describe vaginal microbiomes in health and disease. Microbiome 2023; 11:259.
  17. Lee CY, Dillard LR, Papin JA, Arnold KB. New perspectives into the vaginal microbiome with systems biology. Trends Microbiol 2023; 31:356–368.
  18. Cheu RK, Mohammadi A, Schifanella L, et al. Altered innate immunity and damaged epithelial integrity in vaginal microbial dysbiosis. Front Reprod Health 2022; 4:876729.
  19. Costa-Fujishima M, Yazdanpanah A, Horne S, et al. Nonoptimal bacteria species induce neutrophil-driven inflammation and barrier disruption in the female genital tract. Mucosal Immunol 2023; 16:341–356.
  20. Van Teijlingen NH, Eder J, Sarrami-Forooshani R, et al. Immune activation of vaginal human Langerhans cells increases susceptibility to HIV-1 infection. Sci Rep 2023; 13:3283.
  21. Clayton K, Vallejo AF, Davies J, et al. Langerhans cells—programmed by the epidermis. Front Immunol 2017; 8:1676.
  22. Schwecht I, Nazli A, Gill B, Kaushic C. Lactic acid enhances vaginal epithelial barrier integrity and ameliorates inflammatory effects of dysbiotic short chain fatty acids and HIV-1. Sci Rep 2023; 13:20065.
  23. Schaefer A, Yang B, Schroeder HA, et al. Broadly neutralizing antibodies consistently trap HIV-1 in fresh cervicovaginal mucus from select individuals. Acta Biomater 2023; 169:387–397.
  24. Agarwal K, Choudhury B, Robinson LS, et al. Resident microbes shape the vaginal epithelial glycan landscape. Sci Transl Med 2023; 15:eab9599.
  25. Edfeldt G, Kaldhusdal V, Czarnewski P, et al. Distinct cervical tissue-adherent and luminal microbiome communities correlate with mucosal host gene expression and protein levels in Kenyan sex workers. Microbiome 2023; 11:67.
  26. Cezar-de-Mello PFT, Ryan S, Fichorova RN. The microRNA cargo of human vaginal extracellular vesicles differentiates parasitic and pathobiont infections from colonization by homeostatic bacteria. Microorganisms 2023; 11:551.
  27. Farr Zuend C, Lamont A, Noel-Romas L, et al. Increased genital mucosal cytokines in Canadian women associate with higher antigen-presenting cells, inflammatory metabolites, epithelial barrier disruption, and the depletion of L. crispatus . Microbiome 2023; 11:159.
  28. Berard AR, Brubaker DK, Birse K, et al. Vaginal epithelial dysfunction is mediated by the microbiome, metabolome, and mTOR signaling. Cell Rep 2023; 42:112474.
  29. Gustin A, Cromarty R, Schifanella L, Klatt NR. Microbial mismanagement: how inadequate treatments for vaginal dysbiosis drive the HIV epidemic in women. Semin Immunol 2021; 51:101482.
  30. Nogueira NF, Luisi NEd>, Salazar AS, et al. PrEP awareness and use among reproductive age women in Miami, Florida. PLoS One 2023; 18:e0286071.
  31. Buchbinder SP. Maximizing the benefits of HIV preexposure prophylaxis. Top Antivir Med 2018; 25:138–142.
  32. Abbe C, Mitchell CM. Bacterial vaginosis: a review of approaches to treatment and prevention. Front Reprod Health 2023; 5:1100029.
  33. Division of STD Prevention, National Center for HIV, Viral Hepatitis, STD, and TB Prevention, Centers for Disease Control and Prevention. Sexually Transmitted Infectious Treatment Guidelines, 2021. Centers for Disease Control and Prevention; 2021. Available at: https://www.cdc.gov/std/treatment-guidelines/bv.htm .
  34. Verwijs MC, Agaba SK, Darby AC, Van De Wijgert JHHM. Impact of oral metronidazole treatment on the vaginal microbiota and correlates of treatment failure. Am J Obstet Gynecol 2020; 222:157e1–157e13.
  35. Koumans EH, Markowitz LE, Hogan V, CDC BV Working Group. Indications for therapy and treatment recommendations for bacterial vaginosis in nonpregnant and pregnant women: a synthesis of data. Clin Infect Dis 2002; 35 (S2):S152–S172.
  36. Muñoz-Barreno A, Cabezas-Mera F, Tejera E, Machado A. Comparative effectiveness of treatments for bacterial vaginosis: a network meta-analysis. Antibiotics 2021; 10:978.
  37. Wei G, Liu Q, Wang X, et al. A probiotic nanozyme hydrogel regulates vaginal microenvironment for Candida vaginitis therapy. Sci Adv 2023; 9:eadg0949.
  38. Zhao X, Boyd P, Bashi YD, et al. Two into one does go: formulation development of a multipurpose combination vaginal ring releasing dapivirine and metronidazole for prevention of HIV infection and treatment of bacterial vaginosis. Int J Pharm 2023; 648:123572.
  39. Liu R, Armstrong E, Constable S, et al. Soluble E-cadherin: A marker of genital epithelial disruption. Am J Rep Immunol 2023; 89:e13674.
  40. Lebeer S, Ahannach S, Gehrmann T, et al. A citizen-science-enabled catalogue of the vaginal microbiome and associated factors. Nat Microbiol 2023; 8:2183–2195.
  41. Dixon M, Dunlop AL, Corwin EJ, Kramer MR. Joint effects of individual socioeconomic status and residential neighborhood context on vaginal microbiome composition. Front Public Health 2023; 11:1029741.

Grants

  1. R01 AI128782/NIAID NIH HHS

MeSH Term

Humans
Vagina
Female
HIV Infections
Microbiota
Journal Article Review

Word Cloud

Created with Highcharts 10.0.0vaginalmicrobiomeHIVtransmissionacquisitionmechanismswomennonoptimalLdynamicscellmetabolitesimmunityPURPOSEOFREVIEW:AmonghighlydiversedominatedbacteriaoptimalLactobacillusspeciescrispatusjenseniipredictsReducingamongrequiresbetterunderstandingimpactseffectivelytreatinterveneTechnologicaladvancementsimprovingabilityresearchersfullycharacterizeinteractinghost-bacteriaConsequentlypurposereviewsummarizeinnovativeresearchrolepastyearRECENTFINDINGS:StudiescombiningmultiomicsexperimentaltranslationalapproacheshighlightassociationsmaladaptivealterationsimmunefunctioninghosttranscriptionmucosalepithelialbarrierintegritymultipleproposedincreaseriskvirtuallyzeroacceptableeffectivetreatmentsimproveSUMMARY:Women-centeredsolutionsmodifybacterialcontinueexploredmechanismreduce

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