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      Harnessing the power within: engineering the microbiome for enhanced gynecologic health

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          Abstract

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          Abstract

          Although numerous studies have demonstrated the impact of microbiome manipulation on human health, research on the microbiome’s influence on female health remains relatively limited despite substantial disease burden. In light of this, we present a selected review of clinical trials and preclinical studies targeting both the vaginal and gut microbiomes for the prevention or treatment of various gynecologic conditions. Specifically, we explore studies that leverage microbiota transplants, probiotics, prebiotics, diet modifications, and engineered microbial strains. A healthy vaginal microbiome for females of reproductive age consists of lactic acid-producing bacteria predominantly of the Lactobacillus genus, which serves as a protective barrier against pathogens and maintains a balanced ecosystem. The gut microbiota’s production of short-chain fatty acids, metabolism of primary bile acids, and modulation of sex steroid levels have significant implications for the interplay between host and microbes throughout the body, ultimately impacting reproductive health. By harnessing interventions that modulate both the vaginal and gut microbiomes, it becomes possible to not only maintain homeostasis but also mitigate pathological conditions. While the field is still working toward making broad clinical recommendations, the current studies demonstrate that manipulating the microbiome holds great potential for addressing diverse gynecologic conditions.

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          Manipulating the microbiome has recently entered popular culture, with various diets thought to aid the microbes that live within us. These microbes live in different locations of our body and accordingly help us digest food, modulate our immune system, and influence reproductive health. The role of the microbes living in and influencing the female reproductive tract remains understudied despite known roles in common conditions such as vulvovaginal candidiasis (affecting 75% of females in their lifetime), bacterial vaginosis (25% of females in their lifetime), cervical HPV infection (80% of females in their lifetime), endometriosis (6–10% of females of reproductive age), and polycystic ovary syndrome (10–12% of females of reproductive age). Here, we review four different approaches used to manipulate the female reproductive tract and gastrointestinal system microbiomes: microbiota transplants, probiotics, prebiotics, and dietary interventions, and the use of engineered microbial strains. In doing so, we aim to stimulate discussion on new ways to understand and treat female reproductive health conditions.

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          Structure, Function and Diversity of the Healthy Human Microbiome

          Studies of the human microbiome have revealed that even healthy individuals differ remarkably in the microbes that occupy habitats such as the gut, skin, and vagina. Much of this diversity remains unexplained, although diet, environment, host genetics, and early microbial exposure have all been implicated. Accordingly, to characterize the ecology of human-associated microbial communities, the Human Microbiome Project has analyzed the largest cohort and set of distinct, clinically relevant body habitats to date. We found the diversity and abundance of each habitat’s signature microbes to vary widely even among healthy subjects, with strong niche specialization both within and among individuals. The project encountered an estimated 81–99% of the genera, enzyme families, and community configurations occupied by the healthy Western microbiome. Metagenomic carriage of metabolic pathways was stable among individuals despite variation in community structure, and ethnic/racial background proved to be one of the strongest associations of both pathways and microbes with clinical metadata. These results thus delineate the range of structural and functional configurations normal in the microbial communities of a healthy population, enabling future characterization of the epidemiology, ecology, and translational applications of the human microbiome.
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            Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic.

            An expert panel was convened in October 2013 by the International Scientific Association for Probiotics and Prebiotics (ISAPP) to discuss the field of probiotics. It is now 13 years since the definition of probiotics and 12 years after guidelines were published for regulators, scientists and industry by the Food and Agriculture Organization of the United Nations and the WHO (FAO/WHO). The FAO/WHO definition of a probiotic--"live microorganisms which when administered in adequate amounts confer a health benefit on the host"--was reinforced as relevant and sufficiently accommodating for current and anticipated applications. However, inconsistencies between the FAO/WHO Expert Consultation Report and the FAO/WHO Guidelines were clarified to take into account advances in science and applications. A more precise use of the term 'probiotic' will be useful to guide clinicians and consumers in differentiating the diverse products on the market. This document represents the conclusions of the ISAPP consensus meeting on the appropriate use and scope of the term probiotic.
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              Vaginal microbiome of reproductive-age women.

              The means by which vaginal microbiomes help prevent urogenital diseases in women and maintain health are poorly understood. To gain insight into this, the vaginal bacterial communities of 396 asymptomatic North American women who represented four ethnic groups (white, black, Hispanic, and Asian) were sampled and the species composition characterized by pyrosequencing of barcoded 16S rRNA genes. The communities clustered into five groups: four were dominated by Lactobacillus iners, L. crispatus, L. gasseri, or L. jensenii, whereas the fifth had lower proportions of lactic acid bacteria and higher proportions of strictly anaerobic organisms, indicating that a potential key ecological function, the production of lactic acid, seems to be conserved in all communities. The proportions of each community group varied among the four ethnic groups, and these differences were statistically significant [χ(2)(10) = 36.8, P < 0.0001]. Moreover, the vaginal pH of women in different ethnic groups also differed and was higher in Hispanic (pH 5.0 ± 0.59) and black (pH 4.7 ± 1.04) women as compared with Asian (pH 4.4 ± 0.59) and white (pH 4.2 ± 0.3) women. Phylotypes with correlated relative abundances were found in all communities, and these patterns were associated with either high or low Nugent scores, which are used as a factor for the diagnosis of bacterial vaginosis. The inherent differences within and between women in different ethnic groups strongly argues for a more refined definition of the kinds of bacterial communities normally found in healthy women and the need to appreciate differences between individuals so they can be taken into account in risk assessment and disease diagnosis.
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                Author and article information

                Journal
                Reprod Fertil
                Reprod Fertil
                raf
                Reproduction & Fertility
                Bioscientifica Ltd (Bristol )
                2633-8386
                15 April 2024
                18 March 2024
                01 April 2024
                : 5
                : 2
                : e230060
                Affiliations
                [1 ]Department of Pediatrics , University of California San Diego, La Jolla, California, USA
                [2 ]Division of Biological Sciences , University of California San Diego, La Jolla, California, USA
                [3 ]Department of Bioengineering , University of California, San Diego, La Jolla, California, USA
                [4 ]Medical Scientist Training Program , University of California San Diego, La Jolla, California, USA
                [5 ]Division of Gastroenterology , University of California San Diego, La Jolla, California, USA
                [6 ]Biomedical Sciences Graduate Program , University of California San Diego, La Jolla, California, USA
                [7 ]Department of Obstetrics , Gynecology and Reproductive Sciences, University of California San Diego, La Jolla, California, USA
                [8 ]Center for Microbiome Innovation , University of California San Diego, La Jolla, California, USA
                [9 ]Jennifer Moreno Department of Veterans Affairs Medical Center , La Jolla, California, USA
                [10 ]Institute of Diabetes and Metabolic Health , University of California San Diego, La Jolla, California, USA
                [11 ]Department of Computer Science and Engineering , University of California, San Diego, La Jolla, California, USA
                [12 ]Halıcıoğlu Data Science Institute , University of California San Diego, La Jolla, California, USA
                Author notes
                Correspondence should be addressed to R Knight; Email: robknight@ 123456eng.ucsd.edu

                *(C Brennan, K Chan and T Kumar contributed equally to this work)

                Author information
                http://orcid.org/0000-0003-3943-6701
                http://orcid.org/0000-0003-3676-2333
                Article
                RAF-23-0060
                10.1530/RAF-23-0060
                11046331
                38513356
                bf33d3f8-883d-43c9-bde4-1a971f2c8358
                © the author(s)

                This work is licensed under a Creative Commons Attribution 4.0 International License.

                History
                : 28 December 2023
                : 18 March 2024
                Funding
                Funded by: U.S. Department of Veterans Affairs, doi http://dx.doi.org/10.13039/100000738;
                Categories
                Review
                Microbiome
                This paper forms part of a special series on the Microbiome. The guest editors for this series are Dr Siobhain M O’Mahony (University College Cork, Ireland) and Dr Pierre Comizzoli (Smithsonian’s National Zoo & Conservation Biology Institute, USA).

                microbiome manipulation,gynecologic health,polycystic ovary syndrome,bacterial vaginosis,endometriosis

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