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Gut Microbiota and the Polycystic Ovary Syndrome: Influence of Sex, Sex Hormones, and Obesity
Open accessAbstract
Context: Gut microbiota play a major role in health and disease by influencing physiology, metabolism, nutrition, and immune function. Objective: To evaluate the composition of gut microbiota in women with polycystic ovary syndrome (PCOS), focusing on the influence of sex, sex hormones and obesity on the associations found. Design: Cross-sectional study. Setting: Academic hospital. Participants: We recruited 15 women with PCOS, 16 nonhyperandrogenic control women, and 15 control men. Participants were classified as nonobese (<30 kg/m2) or obese (≥30 kg/m2) according to their body mass index. Interventions: Standardization of diet for 3 consecutive days (at least 300 g of carbohydrates per day) followed by fecal sampling and a standard 75-g oral glucose tolerance test. Main Outcome Measures: Analysis of bacterial abundance and composition of gut microbiota by massive sequencing of 16S ribosomal DNA amplicons in a MiSeq platform (Illumina). Results: α Bacterial diversity was reduced in women compared with men, and β diversity was reduced particularly in obese patients with PCOS. Women with PCOS presented with specific abnormalities in gut microbiota consisting of an increased abundance of the Catenibacterium and Kandleria genera. When all participants as a whole were considered, indexes of bacterial diversity and the abundance of several bacterial genera correlated positively with serum androgen concentrations and negatively with estradiol levels. Conclusions: The diversity and composition of the gut microbiota of young adults are influenced by the combined effects of sex, sex hormone concentrations, and obesity, presenting with specific abnormalities in women with PCOS.
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“Dysbiosis is a consistent finding when looking at the microbiome of women with PCOS [140,141,142,143].”
From Polycystic Ovary Syndrome: An Evolutionary Adaptation to Lifestyle and the Environment (2022) · cites this paper as [141]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
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“Although most studies are small, dysbiosis has consistently been found to correlate with different physiological parameters, such as obesity, sex hormones and metabolic defects [140,141,143].”
From Polycystic Ovary Syndrome: An Evolutionary Adaptation to Lifestyle and the Environment (2022) · cites this paper as [141]
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“He et al.(26) did not find a statistically significant association between estradiol and alpha diversity (richness and Shannon indexes) in a cohort of healthy women and women affected by either osteopenia or osteoporosis (see Tables 2-3).”
From Association Between Sex Hormone Levels and Gut Microbiota Composition and Diversity—A Systematic Review (2022) · cites this paper as [26]
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“Two studies did not find an association between estrogens and the microbiota composition (see Tables 2-3).(26, 32)”
From Association Between Sex Hormone Levels and Gut Microbiota Composition and Diversity—A Systematic Review (2022) · cites this paper as [26]
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“Decreased α-diversity has been described in women with PCOS [109, 110].”
From Polycystic Ovary Syndrome: Pathophysiology, Presentation, and Treatment With Emphasis on Adolescent Girls (2019) · cites this paper as [109]
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Matthews, D. R., Hosker, J. P., Rudenski, A. S., Naylor, B. A., Treacher, D. F., & Turner, R. C. (1985) · Diabetologia · doi:10.1007/bf00280883 · Cited by 31,502
An obesity-associated gut microbiome with increased capacity for energy harvest
Turnbaugh, P. J., Ley, R. E., Mahowald, M. A., Magrini, V., Mardis, E. R., & Gordon, J. I. (2006) · Nature · doi:10.1038/nature05414 · Cited by 12,444
Linking long-term dietary patterns with gut microbial enterotypes
Wu, G. D., Chen, J., Hoffmann, C., Bittinger, K., Chen, Y.-Y., Keilbaugh, S. A., Bewtra, M., Knights, D., Walters, W. A., Knight, R., et al. (2011) · Science · doi:10.1126/science.1208344 · Cited by 6,513
The gut microbiota as an environmental factor that regulates fat storage
Bäckhed, F., Ding, H., Wang, T., Hooper, L. V., Koh, G. Y., Nagy, A., Semenkovich, C. F., & Gordon, J. I. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407076101 · Cited by 6,245
Matsuda, M., & DeFronzo, R. A. (1999) · Diabetes Care · doi:10.2337/diacare.22.9.1462 · Cited by 5,621
Diversity, stability and resilience of the human gut microbiota
Lozupone, C. A., Stombaugh, J. I., Gordon, J. I., Jansson, J. K., & Knight, R. (2012) · Nature · doi:10.1038/nature11550 · Cited by 5,533
Richness of human gut microbiome correlates with metabolic markers
Le Chatelier, E., Nielsen, T., Qin, J., Prifti, E., Hildebrand, F., Falony, G., Almeida, M., Arumugam, M., Batto, J.-M., Kennedy, S., et al. (2013) · Nature · doi:10.1038/nature12506 · Cited by 4,662
The impact of the gut microbiota on human health: an integrative view
Clemente, J. C., Ursell, L. K., Parfrey, L. W., & Knight, R. (2012) · Cell · doi:10.1016/j.cell.2012.01.035 · Cited by 3,710
The Effect of Diet on the Human Gut Microbiome: A Metagenomic Analysis in Humanized Gnotobiotic Mice
Turnbaugh, P. J., Ridaura, V. K., Faith, J. J., Rey, F. E., Knight, R., & Gordon, J. I. (2009) · Science Translational Medicine · doi:10.1126/scitranslmed.3000322 · Cited by 3,058
Diet–microbiota interactions as moderators of human metabolism
Sonnenburg, J. L., & Bäckhed, F. (2016) · Nature · doi:10.1038/nature18846 · Cited by 2,257
Azziz, R., Carmina, E., Dewailly, D., Diamanti-Kandarakis, E., Escobar-Morreale, H. F., Futterweit, W., Janssen, O. E., Legro, R. S., Norman, R. J., Taylor, A. E., et al. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.06.035 · Cited by 2,132
Self-citationStatistical Methods for Detecting Differentially Abundant Features in Clinical Metagenomic Samples
White, J. R., Nagarajan, N., & Pop, M. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000352 · Cited by 1,599
Everard, A., Lazarevic, V., Derrien, M., Girard, M., Muccioli, G. G., Neyrinck, A. M., Possemiers, S., Van Holle, A., François, P., de Vos, W. M., et al. (2011) · Diabetes · doi:10.2337/db11-0227 · Cited by 1,076
Wild, R. A., Carmina, E., Diamanti-Kandarakis, E., Dokras, A., Escobar-Morreale, H. F., Futterweit, W., Lobo, R., Norman, R. J., Talbott, E., & Dumesic, D. A. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-2724 · Cited by 1,010
Self-citationGender Bias in Autoimmunity Is Influenced by Microbiota
Yurkovetskiy, L., Burrows, M. P., Khan, A. A., Graham, L., Volchkov, P., Becker, L., Antonopoulos, D. A., Umesaki, Y., & Chervonsky, A. V. (2013) · Immunity · doi:10.1016/j.immuni.2013.08.013 · Cited by 943
Meta‐analyses of human gut microbes associated with obesity and IBD
Walters, W. A., Xu, Z., & Knight, R. (2014) · FEBS Letters · doi:10.1016/j.febslet.2014.09.039 · Cited by 836
Sex differences and hormonal effects on gut microbiota composition in mice
Org, E., Mehrabian, M., Parks, B. W., Shipkova, P., Liu, X., Drake, T. A., & Lusis, A. J. (2016) · Gut Microbes · doi:10.1080/19490976.2016.1203502 · Cited by 796
Templeton, G. F. (2011) · Communications of the Association for Information Systems · doi:10.17705/1cais.02804 · Cited by 696
Intestinal Microbiota Is Influenced by Gender and Body Mass Index
Haro, C., Rangel-Zúñiga, O. A., Alcalá-Díaz, J. F., Gómez-Delgado, F., Pérez-Martínez, P., Delgado-Lista, J., Quintana-Navarro, G. M., Landa, B. B., Navas-Cortés, J. A., Tena-Sempere, M., et al. (2016) · PLOS ONE · doi:10.1371/journal.pone.0154090 · Cited by 671
Lu, Y., Fan, C., Li, P., Lu, Y., Chang, X., & Qi, K. (2016) · Scientific Reports · doi:10.1038/srep37589 · Cited by 638
Kasai, C., Sugimoto, K., Moritani, I., Tanaka, J., Oya, Y., Inoue, H., Tameda, M., Shiraki, K., Ito, M., Takei, Y., et al. (2015) · BMC Gastroenterology · doi:10.1186/s12876-015-0330-2 · Cited by 581
Alterations in the Gut Microbiota Associated with HIV-1 Infection
Lozupone, C., Li, M., Campbell, T., Flores, S. C., Linderman, D. J., Gebert, M. J., Knight, R. D., Fontenot, A. P., & Palmer, B. E. (2013) · Cell Host & Microbe · doi:10.1016/j.chom.2013.08.006 · Cited by 505
Microbial steroid transformations: current state and prospects
Donova, M. V., & Egorova, O. V. (2012) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-012-4078-0 · Cited by 504
Sato, J., Kanazawa, A., Ikeda, F., Yoshihara, T., Goto, H., Abe, H., Komiya, K., Kawaguchi, M., Shimizu, T., Ogihara, T., et al. (2014) · Diabetes Care · doi:10.2337/dc13-2817 · Cited by 441
The Molecular-Genetic Basis of Functional Hyperandrogenism and the Polycystic Ovary Syndrome
Escobar-Morreale, H. F., Luque‐Ramírez, M., & Millán, J. L. S. (2005) · Endocrine Reviews · doi:10.1210/er.2004-0004 · Cited by 426
Self-citationLindheim, L., Bashir, M., Münzker, J., Trummer, C., Zachhuber, V., Leber, B., Horvath, A., Pieber, T. R., Gorkiewicz, G., Stadlbauer, V., et al. (2017) · PLOS ONE · doi:10.1371/journal.pone.0168390 · Cited by 416
Gut microbial diversity in women with polycystic ovary syndrome correlates with hyperandrogenism
Torres, P. J., Siakowska, M., Banaszewska, B., Pawelczyk, L., Duleba, A. J., Kelley, S. T., & Thackray, V. G. (2018) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2017-02153 · Cited by 399
Abdominal adiposity and the polycystic ovary syndrome
Escobar-Morreale, H. F., & Millán, J. L. S. (2007) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2007.07.003 · Cited by 386
Self-citationDysbiosis of Gut Microbiota Associated with Clinical Parameters in Polycystic Ovary Syndrome
Liu, R., Zhang, C., Shi, Y., Zhang, F., Li, L., Wang, X., Ling, Y., Fu, H., Dong, W., Shen, J., et al. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.00324 · Cited by 386
Association between polycystic ovary syndrome and gut microbiota
Guo, Y., Qi, Y., Yang, X., Zhao, L., Wen, S., Liu, Y., & Tang, L. (2016) · PLOS ONE · doi:10.1371/journal.pone.0153196 · Cited by 350
Impact of the gut microbiota on the development of obesity and type 2 diabetes mellitus
Moreno‐Indias, I., Cardona, F., Tinahones, F. J., & Queipo‐Ortuño, M. I. (2014) · Frontiers in Microbiology · doi:10.3389/fmicb.2014.00190 · Cited by 325
Colonic Microbiota Signatures across Five Northern European Countries
Lay, C., Rigottier‐Gois, L., Holmstrøm, K., Rajilić-Stojanović, M. D., Vaughan, E. E., de Vos, W. M., Collins, M. D., Thiel, R., Namsolleck, P., Blaut, M., et al. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.7.4153-4155.2005 · Cited by 296
Dunaif, A., Heindel, J. J., & Chang, R. (2002) · CRC Press eBooks · doi:10.3109/9780203910948 · Cited by 283
Escobar-Morreale, H. F., Santacruz, E., Luque‐Ramírez, M., & Botella-Carretero, J. I. (2017) · Human Reproduction Update · doi:10.1093/humupd/dmx012 · Cited by 248
Self-citationGenotype Is a Stronger Determinant than Sex of the Mouse Gut Microbiota
Kovacs, A., Ben-Jacob, N., Tayem, H., Halperin, E., Iraqi, F. A., & Gophna, U. (2010) · Microbial Ecology · doi:10.1007/s00248-010-9787-2 · Cited by 226
Schaffrinna, M. G. (1991) · Journal of Adolescent Health · doi:10.1016/0197-0070(91)90048-q · Cited by 214
Moya-Pérez, A., Neef, A., & Sanz, Y. (2015) · PLOS ONE · doi:10.1371/journal.pone.0126976 · Cited by 211
The gut microbiome is altered in a letrozole-induced mouse model of polycystic ovary syndrome
Kelley, S. T., Skarra, D. V., Rivera, A. J., & Thackray, V. G. (2016) · PLOS ONE · doi:10.1371/journal.pone.0146509 · Cited by 205
Phylogenetic diversity and ecophysiology of Candidate phylum Saccharibacteria in activated sludge
Kindaichi, T., Yamaoka, S., Uehara, R., Ozaki, N., Ohashi, A., Albertsen, M., Nielsen, P. H., & Nielsen, J. L. (2016) · FEMS Microbiology Ecology · doi:10.1093/femsec/fiw078 · Cited by 194
Escobar-Morreale, H. F., Sánchón, R., & Millán, J. L. S. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-2053 · Cited by 179
Self-citationLin, H., An, Y., Hao, F., Wang, Y., & Tang, H. (2016) · Scientific Reports · doi:10.1038/srep21618 · Cited by 169
Jönsson, V., Österlund, T., Nerman, O., & Kristiansson, E. (2016) · BMC Genomics · doi:10.1186/s12864-016-2386-y · Cited by 136
Kageyama, A., & Benno, Y. (2000) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/00207713-50-4-1595 · Cited by 124
Lee, J.-C., Lee, H.-Y., Kim, T. K., Kim, M., Park, Y. M., Kim, J., Park, K., Kweon, M., Kim, S., Bae, J., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0187515 · Cited by 114
Metabolism of androgens and estrogens by human fecal microorganisms
Lombardi, P., Goldin, B., Boutin, E., & Gorbach, S. L. (1978) · Journal of Steroid Biochemistry · doi:10.1016/0022-4731(78)90203-0 · Cited by 113
Escobar-Morreale, H. F., Samino, S., Insenser, M. R., Vinaixa, M., Luque‐Ramírez, M., Lasunción, M. A., & Correig, X. (2012) · Clinical Chemistry · doi:10.1373/clinchem.2011.176396 · Cited by 109
Self-citationEscobar-Morreale, H. F., Alvarez-Blasco, F., Botella-Carretero, J. I., & Luque‐Ramírez, M. (2014) · Human Reproduction · doi:10.1093/humrep/deu198 · Cited by 105
Self-citationThe effects of the Lactobacillus casei strain on obesity in children: a pilot study
Nagata, S., Chiba, Y., Wang, C., & Yamashiro, Y. (2017) · Beneficial Microbes · doi:10.3920/bm2016.0170 · Cited by 72
Salvetti, E., Felis, G. E., Dellaglio, F., Castioni, A., Torriani, S., & Lawson, P. A. (2010) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.029231-0 · Cited by 53
Polycystic Ovary Syndrome as a Paradigm for Prehypertension, Prediabetes, and Preobesity
Luque‐Ramírez, M., & Escobar-Morreale, H. F. (2014) · Current Hypertension Reports · doi:10.1007/s11906-014-0500-6 · Cited by 44
Self-citationWagner, B. D., Frank, D. N., & Zipris, D. (2015) · Diabetes · doi:10.2337/dbi15-0009 · Cited by 3
Mejía-León, M. E., & de la Barca, A. M. C. (2015) · Diabetes · doi:10.2337/db15-0848 · Cited by 3
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Qi, X., Yun, C., Pang, Y., & Qiao, J. (2021) · Gut Microbes · doi:10.1080/19490976.2021.1894070 · Cited by 587
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Snider, A. P., & Wood, J. R. (2019) · Reproduction · doi:10.1530/rep-18-0583 · Cited by 326
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Metadata
- Authors
- Insenser, M., Murri, M., del Campo, R., Martínez-García, M. Á., Fernández-Durán, E., & Escobar-Morreale, H. F.
- Affiliations
- Universidad de Alcalá (ES)
- Department of Microbiology, Hospital Universitario Ramón y Cajal, Instituto Ramón y Cajal de Investigación Sanitaria (IRYCIS), Madrid, Spain
- Diabetes Obesity and Human Reproduction Research Group, Department of Endocrinology and Nutrition, Hospital Universitario Ramón y Cajal & Universidad de Alcalá, Centro de Investigación Biomédica en Red Diabetes y Enfermedades Metabólicas Asociadas (CIBERDEM), Instituto Ramón y Cajal de Investigación Sanitaria (IRYCIS), Madrid, Spain
- Corresponding author
- Escobar-Morreale, Héctor F
- Venue
- The Journal of Clinical Endocrinology & Metabolism
- Publisher
- The Endocrine Society
- Published
- 2018-04-20
- Volume
- 103
- Issue
- 7
- Pages
- 2552-2562
- ISSN
- 0021-972X (ISSN-L)
- 1945-7197
- OpenAlex
- W2799415441
- Cited by
- 312
- References
- 52
- Citations by year
- 2026: 37 · 2025: 40 · 2024: 51 · 2023: 54 · 2022: 41 · 2021: 42 · 2020: 29 · 2019: 16 · 2018: 1
- FWCI
- 7.82
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Journal of Clinical Endocrinology & Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Funders
- European Commission
- Ministerio de Economía y Competitividad
- Centro de Investigación Biomédica en Red Diabetes y Enfermedades Metabólicas Asociadas
- Instituto de Salud Carlos III (PI11/, PIE1600050, PI1100357)
- European Regional Development Fund (PIE16/00050)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Reproductive Medicine › Ovarian function and disorders
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Keywords
- gut microbiota, polycystic ovary syndrome, sex differences, sex hormones, obesity, bacterial diversity, androgens, estradiol, Catenibacterium, hyperandrogenism
- MeSH terms
- Gastrointestinal Microbiome, Adult, Androgens, Cross-Sectional Studies, Diet, Estradiol, Feces, Female, Glucose Tolerance Test, Humans, Male, Obesity, Polycystic Ovary Syndrome, Sex Factors, Gonadal Steroid Hormones, Body Mass Index, Case-Control Studies, Young Adult
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