Alterations in Gut Microbiome Composition and Barrier Function Are Associated with Reproductive and Metabolic Defects in Women with Polycystic Ovary Syndrome (PCOS): A Pilot Study
Open accessAbstract
BACKGROUND: Polycystic ovary syndrome (PCOS) is a common female endocrinopathy of unclear origin characterized by hyperandrogenism, oligo-/anovulation, and ovarian cysts. Women with PCOS frequently display overweight, insulin resistance, and systemic low-grade inflammation. We hypothesized that endotoxemia resulting from a leaky gut is associated with inflammation, insulin resistance, fat accumulation, and hyperandrogenemia in PCOS. In this pilot study, we compared the stool microbiome, gut permeability, and inflammatory status of women with PCOS and healthy controls. METHODS: 16S rRNA gene amplicon sequencing was performed on stool samples from 24 PCOS patients and 19 healthy controls. Data processing and microbiome analysis were conducted in mothur and QIIME using different relative abundance cut-offs. Gut barrier integrity, endotoxemia, and inflammatory status were evaluated using serum and stool markers and associations with reproductive, metabolic, and anthropometric parameters were investigated. RESULTS: The stool microbiome of PCOS patients showed a lower diversity and an altered phylogenetic composition compared to controls. We did not observe significant differences in any taxa with a relative abundance>1%. When looking at rare taxa, the relative abundance of bacteria from the phylum Tenericutes, the order ML615J-28 (phylum Tenericutes) and the family S24-7 (phylum Bacteroidetes) was significantly lower and associated with reproductive parameters in PCOS patients. Patients showed alterations in some, but not all markers of gut barrier function and endotoxemia. CONCLUSION: Patients with PCOS have a lower diversity and an altered phylogenetic profile in their stool microbiome, which is associated with clinical parameters. Gut barrier dysfunction and endotoxemia were not driving factors in this patient cohort, but may contribute to the clinical phenotype in certain PCOS patients.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The microbiomes of individuals with PCOS have generally been found to have lower alpha diversity than controls, and most studies describe an altered composition of taxa relative to controls.
“Similar to microbiomes associated with obesity, the microbiomes of individuals with PCOS have generally been found to have lower alpha diversity (lower numbers of bacterial taxa) than controls, and most studies describe an altered composition of taxa relative to controls [140,143].”
From Polycystic Ovary Syndrome: An Evolutionary Adaptation to Lifestyle and the Environment (2022) · cites this paper as [143]
The Results (‘Characterizing the stool microbiome in PCOS’; page not available) report approximately 15% lower alpha diversity in PCOS patients than controls, as well as differences in rare taxa. The Discussion reports a shift in microbiome composition but describes this as a pilot study providing a first description in women with PCOS. It does not establish that these findings hold generally or that most studies report altered taxa. (LLM, conf=0.86)
Experimental — accuracy not yet measuredDysbiosis has consistently been found to correlate with different physiological parameters, such as obesity, sex hormones and metabolic defects, although most studies are small.
“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 [143]
The Results report associations between bacterial taxa and serum androgens, and the Discussion describes this as a small pilot study. The Introduction reports an association between the gut microbiome and obesity, but the Discussion says this study found no significant microbiome differences attributable to BMI or insulin sensitivity and that microbiome patterns in obesity vary across studies. Thus, the source does not support the claim of consistent correlations across all the listed parameters. (LLM, conf=0.87)
Experimental — accuracy not yet measuredDysbiosis is a consistent finding in the microbiome of women with PCOS.
“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 [143]
The Discussion reports lower microbial diversity and shifts in the stool microbiome profile of women with PCOS compared with controls, supporting an association with dysbiosis in this cohort. But it calls this a pilot study and the first description of the stool microbiome in women with PCOS; it cannot establish that dysbiosis is a consistent finding across studies or cohorts. (LLM, conf=0.85)
Experimental — accuracy not yet measuredAlternative mechanisms of the pathogenesis of prediabetes and T2D in subjects with PCOS are muscle mitochondrial dysfunction and the gut microbiome.
“Alternative mechanisms of the pathogenesis of prediabetes and T2D in subjects with PCOS are muscle mitochondrial dysfunction [28] and the gut microbiome [29].”
From From Prediabetes to Type 2 Diabetes Mellitus in Women with Polycystic Ovary Syndrome: Lifestyle and Pharmacological Management (2020) · cites this paper as [29]
All diets that aim to reduce weight are considered beneficial.
“However, all diets that aim to reduce weight are considered beneficial [29].”
From From Prediabetes to Type 2 Diabetes Mellitus in Women with Polycystic Ovary Syndrome: Lifestyle and Pharmacological Management (2020) · cites this paper as [29]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
QIIME allows analysis of high-throughput community sequencing data
Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Peña, A. G., Goodrich, J. K., Gordon, J. I., et al. (2010) · Nature Methods · doi:10.1038/nmeth.f.303 · Cited by 34,887 · see citing works
Search and clustering orders of magnitude faster than BLAST
Edgar, R. C. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq461 · Cited by 20,617 · see citing works
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 · see citing works
Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB
DeSantis, T. Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E. L., Keller, K., Huber, T., Dalevi, D., Hu, P., & Andersen, G. L. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.03006-05 · Cited by 10,891 · cited 1× · see citing works
“Open reference operational taxonomic unit (OTU) picking was performed in QIIME 1.8.0 using UCLUST against the greengenes 13.8 database [30–32].”
Influential(2004) · Fertility and Sterility · doi:10.1016/j.fertnstert.2003.10.004 · Cited by 9,050 · see citing works
UniFrac: a New Phylogenetic Method for Comparing Microbial Communities
Lozupone, C., & Knight, R. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.12.8228-8235.2005 · Cited by 8,227 · see citing works
A core gut microbiome in obese and lean twins
Turnbaugh, P. J., Hamady, M., Yatsunenko, T., Cantarel, B. L., Duncan, A., Ley, R. E., Sogin, M. L., Jones, W. J., Roe, B. A., Affourtit, J. P., et al. (2009) · Nature · doi:10.1038/nature07540 · Cited by 7,823 · see citing works
Kozich, J. J., Westcott, S. L., Baxter, N. T., Highlander, S. K., & Schloss, P. D. (2013) · Applied and Environmental Microbiology · doi:10.1128/aem.01043-13 · Cited by 7,004 · see citing works
A metagenome-wide association study of gut microbiota in type 2 diabetes
Qin, J., Li, Y., Cai, Z., Li, S., Zhu, J., Zhang, F., Liang, S., Zhang, W., Guan, Y., Shen, D., et al. (2012) · Nature · doi:10.1038/nature11450 · Cited by 6,762 · see citing works
Metabolic Endotoxemia Initiates Obesity and Insulin Resistance
Cani, P. D., Amar, J., Iglesias, M. A., Poggi, M., Knauf, C., Bastelica, D., Neyrinck, A. M., Fava, F., Tuohy, K. M., Chabo, C., et al. (2007) · Diabetes · doi:10.2337/db06-1491 · Cited by 6,638 · see citing works
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 · see citing works
The Rotterdam ESHRE/ASRM-sponsored PCOS consensus workshop group (2004) · Human Reproduction · doi:10.1093/humrep/deh098 · Cited by 6,138 · see citing works
Cani, P. D., Bibiloni, R., Knauf, C., Waget, A., Neyrinck, A. M., Delzenne, N. M., & Burcelin, R. (2008) · Diabetes · doi:10.2337/db07-1403 · Cited by 4,819 · cited 2× · see citing works
“[16–18].”
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 · cited 1× · see citing works
“A reduction in stool bacterial diversity of up to 30% has previously been reported in individuals with obesity and metabolic dysfunction [10,35].”
Human Genetics Shape the Gut Microbiome
Goodrich, J. K., Waters, J. L., Poole, A. C., Sutter, J. L., Koren, O., Blekhman, R., Beaumont, M., Van Treuren, W., Knight, R., Bell, J. T., et al. (2014) · Cell · doi:10.1016/j.cell.2014.09.053 · Cited by 3,164 · see citing works
Gut metagenome in European women with normal, impaired and diabetic glucose control
Karlsson, F. H., Tremaroli, V., Nookaew, I., Bergström, G., Behre, C. J., Fagerberg, B., Nielsen, J., & Bäckhed, F. (2013) · Nature · doi:10.1038/nature12198 · Cited by 3,115 · see citing works
Vrieze, A., Van Nood, E., Holleman, F., Salojärvi, J., Kootte, R. S., Bartelsman, J. F. W. M., Dallinga–Thie, G. M., Ackermans, M. T., Serlie, M. J., Oozeer, R., et al. (2012) · Gastroenterology · doi:10.1053/j.gastro.2012.06.031 · Cited by 2,913 · see citing works
Disentangling type 2 diabetes and metformin treatment signatures in the human gut microbiota
MetaHIT consortium, Forslund, K., Hildebrand, F., Nielsen, T., Falony, G., Le Chatelier, E., Sunagawa, S., Prifti, E., Vieira-Silva, S., Gudmundsdottir, V., et al. (2015) · Nature · doi:10.1038/nature15766 · Cited by 2,116 · cited 1× · see citing works
“In patients with type 2 diabetes, a reduction of putatively beneficial butyrate-producing bacteria has been reported, while alpha diversity was found to be unchanged [37–39].”
March, W. A., Moore, V. M., Willson, K. J., Phillips, D. I. W., Norman, R. J., & Davies, M. J. (2010) · Human Reproduction · doi:10.1093/humrep/dep399 · Cited by 1,799 · see citing works
Criteria, Prevalence, and Phenotypes of Polycystic Ovary Syndrome
Lizneva, D., Suturina, L., Walker, W., Brakta, S., Gavrilova-Jordan, L., & Azziz, R. (2016) · Fertility and Sterility · doi:10.1016/j.fertnstert.2016.05.003 · Cited by 1,358 · cited 2× · see citing works
“The phenotype D has been reported to have less reproductive dysfunction and metabolic risk than the remaining phenotypes [41].”
Dumesic, D. A., Oberfield, S. E., Stener-Victorin, E., Marshall, J. C., Laven, J. S., & Legro, R. S. (2015) · Endocrine Reviews · doi:10.1210/er.2015-1018 · Cited by 1,020 · see citing works
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 · cited 1× · see citing works
“Recent meta-analyses have concluded that there is a significant, yet very modest, decrease in alpha diversity in obesity, while differences in community composition and specific taxa are highly study-dependent and do not show a statistically significant overarching pattern [12,36].”
Looking for a Signal in the Noise: Revisiting Obesity and the Microbiome
Sze, M. A., & Schloss, P. D. (2016) · mBio · doi:10.1128/mbio.01018-16 · Cited by 600 · see citing works
Evans, C. C., LePard, K. J., Kwak, J. W., Stancukas, M. C., Laskowski, S., Dougherty, J., Moulton, L., Glawe, A., Wang, Y., Leone, V., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0092193 · Cited by 587 · cited 1× · see citing works
“In another study, the relative abundance of bacteria from the family S24-7 was decreased in mice receiving a high-fat diet and increased after exercise [40].”
Díz, P., Otero-González, A., Rodríguez‐Álvarez, M. X., Gudé, F., López, F. J. G., de Francisco, A., & González‐Quintela, A. (2013) · BMC Endocrine Disorders · doi:10.1186/1472-6823-13-47 · Cited by 554 · cited 1× · see citing works
“2.3 provided by the Diabetes Trial Unit, University of Oxford, UK (www.dtu.ox.ac.uk/ homacalculator/, last accessed Dec 17, 2015) and insulin resistance defined as a HOMA2-IR (cid:21) 2 [27].”
InfluentialSapone, A., de Magistris, L., Pietzak, M. M., Clemente, M. G., Tripathi, A. K., Cucca, F., Lampis, R., Kryszak, D., Cartenı̀, M., Generoso, M., et al. (2006) · Diabetes · doi:10.2337/db05-1593 · Cited by 550 · see citing works
Circulating inflammatory markers in polycystic ovary syndrome: a systematic review and metaanalysis
Escobar-Morreale, H. F., Luque‐Ramírez, M., & González, F. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.11.036 · Cited by 522 · see citing works
Power and sample-size estimation for microbiome studies using pairwise distances and PERMANOVA
Kelly, B. J., Gross, R., Bittinger, K. L., Sherrill-Mix, S. A., Lewis, J. D., Collman, R. G., Bushman, F. D., & Li, H. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btv183 · Cited by 456 · see citing works
Tremellen, K., & Pearce, K. (2012) · Medical Hypotheses · doi:10.1016/j.mehy.2012.04.016 · Cited by 359 · see citing works
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 · see citing works
The effect of heritability and host genetics on the gut microbiota and metabolic syndrome
Lim, M. Y., You, H. J., Yoon, H. S., Kwon, B., Lee, J. Y., Lee, S., Song, Y., Lee, K., Sung, J., & Ko, G. (2016) · Gut · doi:10.1136/gutjnl-2015-311326 · Cited by 340 · see citing works
Lactose intolerance: diagnosis, genetic, and clinical factors
Mattar, R., Mazo, & Carrilho (2012) · Clinical and Experimental Gastroenterology · doi:10.2147/ceg.s32368 · Cited by 246 · see citing works
Heritable components of the human fecal microbiome are associated with visceral fat
Beaumont, M., Goodrich, J. K., Jackson, M. A., Yet, İ., Davenport, E., Vieira‐Silva, S., Debelius, J. W., Pallister, T., Mangino, M., Raes, J., et al. (2016) · Genome biology · doi:10.1186/s13059-016-1052-7 · Cited by 239 · see citing works
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 · see citing works
Yang, Y., Chen, M.-K., Yang, B., Huang, X.-J., Zhang, X., He, L., Zhang, J., & Hua, Z. (2015) · Applied and Environmental Microbiology · doi:10.1128/aem.01906-15 · Cited by 203 · cited 1× · see citing works
“[34].”
Mazer, N. A. (2009) · Steroids · doi:10.1016/j.steroids.2009.01.008 · Cited by 189 · cited 1× · see citing works
“Free testosterone and free DHT were calculated from total testosterone/DHT and SHBG according to Mazer, assuming a blood albumin concentration of 6.2 μmol/l [28].”
InfluentialŻak‐Gołąb, A., Kocełak, P., Aptekorz, M., Zientara, M., Juszczyk, Ł., Martirosian, G., Chudek, J. T., & Olszanecka‐Glinianowicz, M. (2013) · International Journal of Endocrinology · doi:10.1155/2013/674106 · Cited by 159 · cited 1× · see citing works
“The serum zonulin increase observed in our study is in accordance with recent studies in PCOS patients and obese individuals, where serum zonulin was correlated with measures of insulin resistance and fecal bacterial colony count [21,47].”
Yin, Y., Wang, Y., Zhu, L., Liu, W., Liao, N., Jiang, M., Zhu, B., Yu, H. D., Xiang, C., & Wang, X. (2012) · The ISME Journal · doi:10.1038/ismej.2012.128 · Cited by 155 · cited 1× · see citing works
“In humans, an age-related decline in stool SFB abundance has been observed and SFB are rarely detected in adult stool [45].”
Souter, I. C., Baltagi, L. M., Kuleta, D., Meeker, J. D., & Petrozza, J. C. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.11.062 · Cited by 139 · see citing works
The phenotype of polycystic ovary syndrome ameliorates with aging
Brown, Z. A., Louwers, Y. V., Fong, S. L., Valkenburg, O., Birnie, E., de Jong, F. H., Fauser, B. C. J. M., & Laven, J. S. E. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.09.002 · Cited by 139 · cited 1× · see citing works
“It has been reported that PCOS symptoms can be more pronounced in young patients and attenuated with age [43].”
Münzker, J., Hofer, D., Trummer, C., Ulbing, M., Harger, A., Pieber, T. R., Owen, L. J., Keevil, B. G., Brabant, G. E., Lerchbaum, E., et al. (2014) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2014-2523 · Cited by 104 · see citing works
Self-citationInduction of Th17 cells by segmented filamentous bacteria in the murine intestine
Farkas, A. M., Panea, C., Goto, Y., Nakato, G., Galán-Díez, M., Narushima, S., Honda, K., & Ivanov, I. I. (2015) · Journal of Immunological Methods · doi:10.1016/j.jim.2015.03.020 · Cited by 100 · see citing works
Zhang, D., Zhang, L., Yue, F., Zheng, Y., & Russell, R. (2014) · European Journal of Endocrinology · doi:10.1530/eje-14-0589 · Cited by 84 · cited 2× · see citing works
“The serum zonulin increase observed in our study is in accordance with recent studies in PCOS patients and obese individuals, where serum zonulin was correlated with measures of insulin resistance and fecal bacterial colony count [21,47].”
The Lipid Accumulation Product Is Associated with Impaired Glucose Tolerance in PCOS Women
Wehr, E., Gruber, H., Giuliani, A., Möller, R., Pieber, T. R., & Obermayer-Pietsch, B. M. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-0031 · Cited by 79 · see citing works
Self-citationKollmann, M., Klaritsch, P., Martins, W. P., Guenther, F., Schneider, V., Herzog, S. A., Craciunas, L., Lang, U. E., Obermayer-Pietsch, B. M., Lerchbaum, E., et al. (2015) · Human Reproduction · doi:10.1093/humrep/dev187 · Cited by 77 · see citing works
Self-citationLerchbaum, E., Schwetz, V., Giuliani, A., & Obermayer-Pietsch, B. (2013) · Human Reproduction · doi:10.1093/humrep/det255 · Cited by 73 · see citing works
Self-citationOwen, L. J., Wu, F. C. W., & Keevil, B. G. (2013) · Annals of Clinical Biochemistry International Journal of Laboratory Medicine · doi:10.1177/0004563213501478 · Cited by 44 · cited 1× · see citing works
“[22–25].”
Owen, L. J., Wu, F. C. W., Büttler, R. M., & Keevil, B. G. (2015) · Annals of Clinical Biochemistry International Journal of Laboratory Medicine · doi:10.1177/0004563215621096 · Cited by 39 · see citing works
Chadwick, C., Owen, L. J., & Keevil, B. G. (2005) · Annals of Clinical Biochemistry International Journal of Laboratory Medicine · doi:10.1258/000456305774538175 · Cited by 36 · see citing works
Flagged first, then by citations
1 of the 50 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Estrogen–gut microbiome axis: Physiological and clinical implications
Baker, J. M., Al‐Nakkash, L., & Herbst‐Kralovetz, M. M. (2017) · Maturitas · doi:10.1016/j.maturitas.2017.06.025 · Cited by 1,024 · see citing works
Gut microbiota–bile acid–interleukin-22 axis orchestrates polycystic ovary syndrome
Qi, X., Yun, C., Sun, L., Xia, J., Wu, Q., Wang, Y., Wang, L., Zhang, Y., Liang, X., Wang, L., et al. (2019) · Nature Medicine · doi:10.1038/s41591-019-0509-0 · Cited by 860 · see citing works
The role of the gut microbiome and its metabolites in metabolic diseases
Wu, J., Wang, K., Wang, X., Pang, Y., & Jiang, C. (2020) · Protein & Cell · doi:10.1007/s13238-020-00814-7 · Cited by 584 · see citing works
“In 2017, a study demonstrated that patients with PCOS have reduced diversity and an altered phylogenetic profile in their stool microbiome, which is associated with clinical parameters (Lindheim et al., 2017).”
The impact of the gut microbiota on the reproductive and metabolic endocrine system
Qi, X., Yun, C., Pang, Y., & Qiao, J. (2021) · Gut Microbes · doi:10.1080/19490976.2021.1894070 · Cited by 573 · see citing works
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 · see citing works
“Our results agree with the two aforementioned studies that demonstrated changes in b diversity between healthy women and women with PCOS according to unweighted Unifrac and Bray-Curtis analyses (11, 12).”
Uterine Microbiota: Residents, Tourists, or Invaders?
Baker, J. M., Chase, D. M., & Herbst‐Kralovetz, M. M. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00208 · Cited by 390 · see citing works
Serum level of sex steroid hormone is associated with diversity and profiles of human gut microbiome
Shin, J.-H., Park, Y.-H., Sim, M., Kim, S.-A., Joung, H., & Shin, D.-M. (2019) · Research in Microbiology · doi:10.1016/j.resmic.2019.03.003 · Cited by 334 · see citing works
“Also, there are only a few human studies which have examined the changes in the bacterial communities by the sex steroid hormone [16,20], and the results remain controversial in some murine studies [21,22].”
Obesity induces ovarian inflammation and reduces oocyte quality
Snider, A. P., & Wood, J. R. (2019) · Reproduction · doi:10.1530/rep-18-0583 · Cited by 321 · see citing works
Gut microbiota and the polycystic ovary syndrome: influence of sex, sex hormones, and obesity
Insenser, M., Murri, M., del Campo, R., Martínez-García, M. Á., Fernández-Durán, E., & Escobar-Morreale, H. F. (2018) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2017-02799 · Cited by 312 · see citing works
He, F.-F., & Li, Y.-M. (2020) · Journal of Ovarian Research · doi:10.1186/s13048-020-00670-3 · Cited by 289 · see citing works
“Several studies have reported a decrease in α diversity and a change in β diversity in patients with PCOS [18, 20].”
Zhang, J., Sun, Z., Jiang, S., Bai, X., Ma, C., Peng, Q., Chen, K., Chang, H., Fang, T., & Zhang, H. (2019) · mSystems · doi:10.1128/msystems.00017-19 · Cited by 287 · see citing works
“These studies involved women from Europe and China diagnosed with PCOS (25, 26).”
Lifestyle management in polycystic ovary syndrome – beyond diet and physical activity
Cowan, S., Lim, S. S., Alycia, C., Pirotta, S., Thomson, R. L., Gibson‐Helm, M. E., Blackmore, R., Naderpoor, N., Bennett, C., Ee, C., et al. (2023) · BMC Endocrine Disorders · doi:10.1186/s12902-022-01208-y · Cited by 285 · see citing works
“These findings may be linked to lower microbial diversity and increased intestinal permeability in women with PCOS [230, 231].”
Metabolic Syndrome and PCOS: Pathogenesis and the Role of Metabolites
Chen, W., & Pang, Y. (2021) · Metabolites · doi:10.3390/metabo11120869 · Cited by 228 · see citing works
Sex, microbes, and polycystic ovary syndrome
Thackray, V. G. (2019) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2018.11.001 · Cited by 203 · see citing works
“In addition, one study observed a decrease in bacteria from the Tenericutes phylum (order ML615J) [49], a group of bacteria previously associated with obesity and metabolic dysregulation [56].”
Zeng, B., Lai, Z., Sun, L., Zhang, Z., Yang, J., Li, Z., Lin, J., & Zhang, Z. (2018) · Research in Microbiology · doi:10.1016/j.resmic.2018.09.002 · Cited by 190 · see citing works
Molina, N. M., Sola‐Leyva, A., Sáez‐Lara, M. J., Plaza‐Díaz, J., Tubić-Pavlović, A., Romero, B., Clavero, A., Mozas‐Moreno, J., Fontes, J., & Altmäe, S. (2020) · Biomolecules · doi:10.3390/biom10040593 · Cited by 189 · see citing works
The Gut Microbiome and Sex Hormone-Related Diseases
He, S., Li, H., Yu, Z., Zhang, F., Liang, S., Liu, H., Chen, H., & Lü, M. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.711137 · Cited by 176 · see citing works
Ostadmohammadi, V., Jamilian, M., Bahmani, F., & Asemi, Z. (2019) · Journal of Ovarian Research · doi:10.1186/s13048-019-0480-x · Cited by 174 · see citing works
“On the other hand, extensive evidence reveal that dysbiosis of gut microflora is involved in the pathogenesis of metabolic disturbances in PCOS [18].”
Microbiome and PCOS: State-of-Art and Future Aspects
Giampaolino, P., Foreste, V., Filippo, C. D., Gallo, A., Mercorio, A., Serafino, P., Improda, F. P., Verrazzo, P., Zara, G., Buonfantino, C., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22042048 · Cited by 169 · see citing works
“There are significant differences in the composition of the microbiome between healthy adults, and these differences may underlie the susceptibility to various diseases [23].”
Jobira, B., Frank, D. N., Pyle, L. L., Silveira, L. J., Kelsey, M. M., Garcia‐Reyes, Y., Robertson, C. E., Ir, D., Nadeau, K. J., & Cree‐Green, M. (2020) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgz263 · Cited by 164 · see citing works
Prenatal androgen exposure causes hypertension and gut microbiota dysbiosis
Sherman, S. B., Sarsour, N. Y., Salehi, M., Schroering, A. G., Mell, B., Joe, B., & Hill, J. W. (2018) · Gut Microbes · doi:10.1080/19490976.2018.1441664 · Cited by 160 · see citing works
“Recent studies have found that the profiles of bacterial abundance exhibit similarities between the orders Clostridales and Bacteroidales.(22,31,32) Obese and non-obese women with PCOS had enriched Bacteroidetes and a decreased abundance of Akkermansia (of the phylum Verrucomicrobia), Alistipes, Corprococcus, and Rumi…”
Mayneris‐Perxachs, J., Arnoriaga‐Rodríguez, M., Luque-Córdoba, D., Priego‐Capote, F., Pérez‐Brocal, V., Moyá, A., Burokas, A., Maldonado, R. J., & Fernández‐Real, J. M. (2020) · Microbiome · doi:10.1186/s40168-020-00913-x · Cited by 162 · see citing works
A New Approach to Polycystic Ovary Syndrome: The Gut Microbiota
Depboylu, G. Y., & Akdevelıoğlu, Y. (2019) · Journal of the American College of Nutrition · doi:10.1080/07315724.2019.1657515 · Cited by 161 · see citing works
“In a pilot study that compared the stool microbiome of 24 women with PCOS with that of 16 healthy controls, Lindheim et al. reported a decrease in relative abundance of bacteria from the Tenericutes phylum, ML615J-28 (belonging to the phylum Tenericutes), and S247 (belonging to phylum Bacteroidetes) (38).”
InfluentialCharacteristic gut microbiota and predicted metabolic functions in women with PCOS
Zhou, L., Ni, Z., Cheng, W., Yu, J., Sun, S., Zhai, D., Yu, C., & Cai, Z. (2020) · Endocrine Connections · doi:10.1530/ec-19-0522 · Cited by 141 · see citing works
Nutritional Supplements and Complementary Therapies in Polycystic Ovary Syndrome
Alesi, S., Ee, C., Moran, L., Rao, V. S., & Mousa, A. (2021) · Advances in Nutrition · doi:10.1093/advances/nmab141 · Cited by 180 · see citing works
Correlation Between Fecal Metabolomics and Gut Microbiota in Obesity and Polycystic Ovary Syndrome
Zhou, L., Ni, Z., Yu, J., Cheng, W., Cai, Z., & Yu, C. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00628 · Cited by 148 · see citing works
Yu, J. S., Youn, G. S., Choi, J., Kim, C., Kim, B., Yang, S., Lee, J., Park, T., Kim, B. K., Kim, Y. B., et al. (2021) · Clinical and Translational Medicine · doi:10.1002/ctm2.634 · Cited by 143 · see citing works
Dysregulation of immune response in PCOS organ system
Wang, J., Yin, T., & Liu, S. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1169232 · Cited by 148 · see citing works
Gut microbiota: novel therapeutic target for nonalcoholic fatty liver disease
Suk, K. T., & Kim, D. J. (2019) · Expert Review of Gastroenterology & Hepatology · doi:10.1080/17474124.2019.1569513 · Cited by 133 · see citing works
Xu, L., Zhang, Y., Li, X., Li, C., Hu, H., Hu, J., Liu, M., Yang, Q. Z., Gu, P., Li, J., et al. (2025) · iMeta · doi:10.1002/imt2.270 · Cited by 138 · see citing works
Quaranta, G., Sanguinetti, M., & Masucci, L. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02653 · Cited by 131 · see citing works
Lee, N. Y., Yoon, S. J., Han, D. H., Gupta, H., Youn, G. S., Shin, M. J., Ham, Y. L., Kwak, M. J., Kim, B., Yu, J. S., et al. (2020) · Gut Microbes · doi:10.1080/19490976.2020.1712984 · Cited by 127 · see citing works
Chu, W., Han, Q., Xu, J., Wang, J., Sun, Y., Li, W., Chen, Z.-J., & Du, Y. (2020) · Fertility and Sterility · doi:10.1016/j.fertnstert.2020.01.027 · Cited by 121 · see citing works
Female reproductive dysfunctions and the gut microbiota
Chadchan, S. B., Singh, V., & Kommagani, R. (2022) · Journal of Molecular Endocrinology · doi:10.1530/jme-21-0238 · Cited by 120 · see citing works
“Additionally, PCOS patients showed alterations in some, but not all, markers of gut barrier function and endotoxemia (Lindheim et al. 2017).”
Sun, Y., Gao, S., Ye, C., & Zhao, W. (2023) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2023.1142041 · Cited by 133 · see citing works
“Compared with healthy people, the gut microbial diversity of PCOS patients decreased, the composition changed, and the intestinal mucosal barrier was damaged (Lindheim et al., 2017).”
Systematic low-grade chronic inflammation and intrinsic mechanisms in polycystic ovary syndrome
Deng, H., Chen, Y., Xing, J., Zhang, N., & Xu, L. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1470283 · Cited by 137 · see citing works
Lorenzo, M. D., Cacciapuoti, N., Lonardo, M. S., Nasti, G., Gautiero, C., Belfiore, A., Guida, B., & Chiurazzi, M. (2023) · Current Nutrition Reports · doi:10.1007/s13668-023-00479-8 · Cited by 129 · see citing works
Polycystic Ovary Syndrome: An Evolutionary Adaptation to Lifestyle and the Environment
parker, J., O'Brien, C., Hawrelak, J., & Gersh, F. (2021) · doi:10.20944/preprints202112.0088.v1 · Cited by 113 · see citing works
Zhao, X., Jiang, Y., Xi, H., Chen, L., & Feng, X. (2020) · Geburtshilfe und Frauenheilkunde · doi:10.1055/a-1081-2036 · Cited by 124 · see citing works
“Lindheim et al. [31] found that compared with the control group, the relative abundance of Tenericutes ML615J-28 and Bacteroi-detes S24-7 was lower in PCOS patients.”
Polycystic Ovary Syndrome: An Evolutionary Adaptation to Lifestyle and the Environment
Parker, J., O’Brien, C., Hawrelak, J., & Gersh, F. L. (2022) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph19031336 · Cited by 114 · see citing works
“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).”
Hussain, T., Murtaza, G., Kalhoro, D. H., Kalhoro, M. S., Metwally, E., Chughtai, M. I., Mazhar, M. U., & Khan, S. A. (2021) · Animal Nutrition · doi:10.1016/j.aninu.2020.11.005 · Cited by 110 · see citing works
“Furthermore, the literature has placed an emphasis on estrogen (Flores et al., 2012; Menon et al., 2013; Lindheim et al., 2017) while only some studies documented the link between intestinal microbial composition and the concentration of testosterone (Al-Asmakh et al.”
Torres, P. J., Ho, B., Arroyo, P., Sau, L., Chen, A., Kelley, S. T., & Thackray, V. G. (2019) · Endocrinology · doi:10.1210/en.2019-00050 · Cited by 109 · see citing works
Xue, J., Li, X., Liu, P., Li, K., Sha, L., Yang, X., Zhu, L., Wang, Z., Dong, Y., Zhang, L., et al. (2019) · Endocrine Journal · doi:10.1507/endocrj.ej18-0567 · Cited by 107 · see citing works
He, Y., Wang, Q., Xiu, L., Wang, G., Zhao, J., Zhang, H., & Chen, W. (2020) · Food & Function · doi:10.1039/c9fo02554e · Cited by 105 · see citing works
Li, P., Shuai, P., Shen, S., Zheng, H., Sun, P., Zhang, R., Lan, S., Lan, Z., Jayawardana, T. C., Yang, Y., et al. (2023) · BMC Medicine · doi:10.1186/s12916-023-02975-8 · Cited by 115 · see citing works
Intersection of Polycystic Ovary Syndrome and the Gut Microbiome
Rizk, M. G., & Thackray, V. G. (2021) · Journal of the Endocrine Society · doi:10.1210/jendso/bvaa177 · Cited by 104 · see citing works
“In the healthy gut, the phyla Firmicutes, Bacteroidetes, Actinobacteria, and Verrucomicrobia are the most dominant, while Proteobacteria and Tenericutes exist at low abundance [45].”
InfluentialThe latest reports and treatment methods on polycystic ovary syndrome
Stańczak, N. A., Grywalska, E., & Dudzińska, E. (2024) · Annals of Medicine · doi:10.1080/07853890.2024.2357737 · Cited by 147 · see citing works
“Similar ovarian morphology has been observed in women with congenital adrenal hyperplasia (CAH) and female-to-male transgender individuals [17].”
Gut microbiota alterations reveal potential gut–brain axis changes in polycystic ovary syndrome
Liang, Z., Di, N., Li, L., & Yang, D. (2021) · Journal of Endocrinological Investigation · doi:10.1007/s40618-020-01481-5 · Cited by 109 · see citing works
Gut Microbiota in Patients with Polycystic Ovary Syndrome: a Systematic Review
Guo, J., Shao, J., Yang, Y., Niu, X., Liao, J., Zhao, Q. S., Wang, D., Li, S., & Hu, J. (2021) · Reproductive Sciences · doi:10.1007/s43032-020-00430-0 · Cited by 98 · see citing works
“Table 1 Characteristics of the observational studies included in the systematic review Study Year Country Type of specimen Definite of PCOS Study design Group Population Age Microbiome assessment method Qi 2019 China Fecal samples Rotterdam criteria Cohort PCOS 50 20–40 Whole-genome shotgun sequencing HC 43 20–40 Inse…”
InfluentialGut and Vaginal Microbiomes in PCOS: Implications for Women’s Health
Gu, Y., Zhou, G., Zhou, F., Li, Y. O., Wu, Q., He, H., Zhang, Y., Ma, C., Ding, J., & Hua, K. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.808508 · Cited by 102 · see citing works
The Gut Microbiome and Female Health
Siddiqui, R., Makhlouf, Z., Alharbi, A. M., Alfahemi, H. H., & Khan, N. A. (2022) · Biology · doi:10.3390/biology11111683 · Cited by 101 · see citing works
“As can be seen in Table 1 and Figure 1, PCOS patients have a less diverse gut microbiome, which is correlated with hyperandrogenism [25,27,28].”
Yun, C., Yan, S., Liao, B., Ding, Y., Qi, X., Zhao, M., Wang, K., Zhuo, Y., Nie, Q., Ye, C., et al. (2024) · Nature Metabolism · doi:10.1038/s42255-024-01041-8 · Cited by 103 · see citing works
“Typically, the gut microbiota of patients with PCOS exhibit reduced alpha diversity 9,10 .”
Sex hormones influence the intestinal microbiota composition in mice
Wu, Y., Peng, X., Li, X., Li, D., Tan, Z., & Yu, R. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.964847 · Cited by 92 · see citing works
“Studies showed that abnormal androgen levels can lead to intestinal dysbacteria, including enzymes involved in androgen metabolism, which further interfere with androgen metabolism, and are associated with diseases such as polycystic ovary syndrome (Lindheim et al., 2017; Liu et al., 2017; Torres et al., 2018; Zeng et…”
Zhu, Y., Li, Y., Liu, M., Hu, X., & Zhu, H. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00575 · Cited by 80 · see citing works
“Besides, PCOS-related insulin resistance and chronic inflammation is independent of obesity (10, 11).”
Khan, R., Jiang, X., Hameed, U., & Shi, Q. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.639704 · Cited by 79 · see citing works
Female reproductive tract-organ axes
Takada, K., Melnikov, V. G., Kobayashi, R., Komine‐Aizawa, S., Tsuji, N. M., & Hayakawa, S. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1110001 · Cited by 82 · see citing works
Gut microbiota: a hidden player in polycystic ovary syndrome
Senthilkumar, H., & Arumugam, M. (2025) · Journal of Translational Medicine · doi:10.1186/s12967-025-06315-7 · Cited by 85 · see citing works
The interplay between PCOS pathology and diet on gut microbiota in a mouse model
Paris, V. R., Wong, X. Y. D., Solon‐Biet, S. M., Edwards, M. C., Aflatounian, A., Gilchrist, R. B., Simpson, S. J., Handelsman, D. J., Kaakoush, N. O., & Walters, K. A. (2022) · Gut Microbes · doi:10.1080/19490976.2022.2085961 · Cited by 79 · see citing works
“Several studies have reported altered microbial composition in PCOS rodent models17,18,20,23 and women with PCOS.13,14,24 One potential explanation for this shift is the presence of elevated levels of androgens, as a study in women with PCOS identified that β-diversity was negatively correlated with hyperandrogenism.1…”
InfluentialObesity-Related Hypogonadism in Women
Eng, P. C., Phylactou, M., Qayum, A., Woods, C., Lee, H., Aziz, S., Moore, B., Miras, A. D., Comninos, A. N., Tan, T., et al. (2023) · Endocrine Reviews · doi:10.1210/endrev/bnad027 · Cited by 79 · see citing works
Fox, C. W., Zhang, L., Sohni, A., Doblado, M., Wilkinson, M., Chang, R. J., & Dulęba, A. J. (2019) · Endocrinology · doi:10.1210/en.2019-00588 · Cited by 78 · see citing works
The Gut Microbiome in Polycystic Ovary Syndrome and Its Association with Metabolic Traits
Lüll, K., Arffman, R. K., Sola‐Leyva, A., Molina, N. M., Aasmets, O., Herzig, K., Plaza‐Díaz, J., Franks, S., Morin-Papunen, L. C., Tapanainen, J. S., et al. (2020) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgaa848 · Cited by 78 · see citing works
Impact of genistein on the gut microbiome of humanized mice and its role in breast tumor inhibition
Paul, B., Royston, K. J., Li, Y., Stoll, M. L., Skibola, C. F., Wilson, L. S., Barnes, S., Morrow, C. D., & Tollefsbol, T. O. (2017) · PLoS ONE · doi:10.1371/journal.pone.0189756 · Cited by 74 · see citing works
“A recent study has also found that patients with polycystic ovarian syndrome have lower gut diversity as compared to control [51].”
He, F., & Li, Y. (2021) · Journal of Ovarian Research · doi:10.1186/s13048-021-00799-9 · Cited by 74 · see citing works
Emanuel, R. H. K., Roberts, J., Docherty, P. D., Lunt, H., Campbell, R. E., & Möller, K. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.1017468 · Cited by 83 · see citing works
Alterations in the intestinal microbiome associated with PCOS affect the clinical phenotype
Wang, L., Zhou, J., Gober, H.-J., Leung, W. T., Huang, Z., Pan, X., Li, C., Zhang, N., & Wang, L. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.110958 · Cited by 73 · see citing works
Tesei, D., Jewczynko, A., Lynch, A., & Urbaniak, C. (2022) · Life · doi:10.3390/life12040495 · Cited by 75 · see citing works
Corrie, L., Awasthi, A., Kaur, J., Vishwas, S., Gulati, M., Kaur, I. P., Gupta, G., Kommineni, N., Dua, K., & Singh, S. K. (2023) · Pharmaceuticals · doi:10.3390/ph16020197 · Cited by 76 · see citing works
“In a cohort study, it was pointed out that the presence of family S24-7of Bacteroidetes was significantly lower in stools of PCOS patients and was associated with reproductive hormones such as thyroid stimulating hormone (TSH) and luteinizing hormone (LH) [93].”
Risk factors associated with intestinal permeability in an adult population: A systematic review
Leech, B., McIntyre, E., Steel, A., & Sibbritt, D. W. (2019) · International Journal of Clinical Practice · doi:10.1111/ijcp.13385 · Cited by 72 · see citing works
Arroyo, P., Ho, B., Sau, L., Kelley, S. T., & Thackray, V. G. (2019) · PLoS ONE · doi:10.1371/journal.pone.0223274 · Cited by 70 · see citing works
Dong, S., jiao, J., Jia, S., Li, G., Zhang, W., Yang, K., Wang, Z., Liu, C., Li, D., & Wang, X. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.634981 · Cited by 69 · see citing works
“Patients with PCOS have a decreased a diversity compared to healthy people (Lindheim et al., 2017; Insenser et al., 2018; Torres et al., 2018), while some studies showed no difference (Qi et al., 2019; Zeng et al., 2019).”
Role of Obesity in Female Reproduction
Yong, W., Wang, J., Leng, Y., Li, L., & Wang, H. (2023) · International Journal of Medical Sciences · doi:10.7150/ijms.80189 · Cited by 74 · see citing works
“This finding, along with observations that polycystic ovarian syndrome (PCOS) was associated with reduced diversity of the gut microbiome in patients from different countries [126-128], collectively support the idea that gut microbiome changes may impact fertility.”
Association between polycystic ovary syndrome and the vaginal microbiome: A case‐control study
Hong, X., Qin, P., Huang, K., Ding, X., Ma, J., Xuan, Y., Zhu, X., Peng, D., & Wang, B. (2020) · Clinical Endocrinology · doi:10.1111/cen.14198 · Cited by 68 · see citing works
Gut microbiome in PCOS associates to serum metabolomics: a cross-sectional study
Yu, Z., Qin, E., Cheng, S., Yang, H., Liu, R., Xu, T., Liu, Y., Yuan, J., Yu, S., Yang, J., et al. (2022) · Scientific Reports · doi:10.1038/s41598-022-25041-4 · Cited by 71 · see citing works
Wang, Y., Xu, L., Sun, X., Wan, X., Sun, G., Jiang, R., Li, W., Tian, Y., Liu, X., & Kang, X. (2020) · Research in Veterinary Science · doi:10.1016/j.rvsc.2020.01.020 · Cited by 67 · see citing works
Abnormal Endometrial Receptivity and Oxidative Stress in Polycystic Ovary Syndrome
Shan, H., Luo, R., Guo, X., Li, R., Ye, Z., Peng, T., Liu, F.-T., & Yang, Z. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.904942 · Cited by 66 · see citing works
“In addition, compared with that in healthy controls, the abundance of common Bacteroides vulgatus in women with PCOS was significantly increased (Lindheim et al., 2017; Liu et al., 2017; Torres et al., 2018; Qi et al., 2019; Zeng et al., 2019).”
Chu, W., Zhai, J., Xu, J., Li, S., Li, W., Chen, Z., & Du, Y. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.03145 · Cited by 65 · see citing works
Li, Y., Tan, Y., Xia, G., & Shuai, J. (2021) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2021.1951155 · Cited by 64 · see citing works
Spremović-Radjenović, S., Pupovac, M., Andjić, M., Bila, J. S., Sreckovic, S. D., Gudović, A., Dragaš, B., & Radunović, N. V. (2022) · Biomedicines · doi:10.3390/biomedicines10010131 · Cited by 64 · see citing works
“These unfavorable changes in the microbiome are linked to reproductive and metabolic defects in women with PCOS [81].”
Polycystic Ovary Syndrome: Challenges and Possible Solutions
Che, Y., Yu, J., Li, Y., Zhu, Y., & Tao, T. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12041500 · Cited by 65 · see citing works
“Current research suggests that gut microbiota dysfunction disrupts the intestinal mucosal barrier, activates chronic inflammation, and produces various molecule metabolites that are involved in the development of PCOS [19].”
Tan, S., Ge, W., Wang, J., Liu, W., Zhao, Y. M., Shen, W., & Li, L. (2019) · Chemosphere · doi:10.1016/j.chemosphere.2019.125493 · Cited by 63 · see citing works
Cozzolino, M., Vitagliano, A., Pellegrini, L., Chiurazzi, M., Andriasani, A., Ambrosini, G., & Garrido, N. (2020) · European Journal of Nutrition · doi:10.1007/s00394-020-02233-0 · Cited by 63 · see citing works
Fu, C., Chen, Z., Chen, M., Chen, G., Huang, Q., Yang, X., Yin, H., Chen, L., Zhang, W., Lin, H., et al. (2021) · npj Biofilms and Microbiomes · doi:10.1038/s41522-021-00231-6 · Cited by 63 · see citing works
Faith, D. P. (2018) · Springer eBooks · doi:10.1007/978-3-319-93145-6_1 · Cited by 63 · see citing works
“For example, Lindheim et al. (2017) in the study “Gut Microbial Diversity in Women with Polycystic Ovary Syndrome” found affected individuals to have reduced microbial PD of the gut microbiome.”
Zheng, Y., Yu, J., Liang, C., Li, S., Wen, X., & Li, Y. (2020) · Bioprocess and Biosystems Engineering · doi:10.1007/s00449-020-02320-w · Cited by 61 · see citing works
Torres, P. J., Skarra, D. V., Ho, B., Sau, L., Anvar, A. R., Kelley, S. T., & Thackray, V. G. (2019) · BMC Microbiology · doi:10.1186/s12866-019-1425-7 · Cited by 62 · see citing works
Elevation of markers of endotoxemia in women with polycystic ovary syndrome
Banaszewska, B., Siakowska, M., Chudzicka-Strugała, I., Chang, R. J., Pawelczyk, L. A., Zwoździak, B., Spaczyński, R., & Dulęba, A. J. (2020) · Human Reproduction · doi:10.1093/humrep/deaa194 · Cited by 60 · see citing works
Bai, X., Zheng, L., Li, D., & Xu, Y. (2021) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-021-00802-4 · Cited by 58 · see citing works
Characterization of gut microbiota in polycystic ovary syndrome: Findings from a lean population
Mammadova, G., Özkul, C., Işıkhan, S. Y., Açıkgöz, A., & Yıldız, B. O. (2020) · European Journal of Clinical Investigation · doi:10.1111/eci.13417 · Cited by 58 · see citing works
Jayasudha, R., Chakravarthy, S. K., Prashanthi, G. S., Sharma, S., Garg, P., Murthy, S. I., & Shivaji, S. (2018) · Journal of Biosciences · doi:10.1007/s12038-018-9798-6 · Cited by 56 · see citing works
The Gut-Prostate Axis: A New Perspective of Prostate Cancer Biology through the Gut Microbiome
Fujita, K., Matsushita, M., Velasco, M. A. D., Hatano, K., Minami, T., Nonomura, N., & Uemura, H. (2023) · Cancers · doi:10.3390/cancers15051375 · Cited by 58 · see citing works
Yang, Y., Cheng, J., Liu, C., Zhang, X., Ma, N., Zhou, Z., Lu, W., & Wu, C. (2024) · EClinicalMedicine · doi:10.1016/j.eclinm.2024.102884 · Cited by 59 · see citing works
“Notably, glycodeoxycholic acid can lead to the secretion of intestinal IL-22, thus alleviate PCOS development.”
Eyüpoğlu, D., Ergünay, K., Açıkgöz, A., Akyön, Y., Yılmaz, E., & Yıldız, B. O. (2020) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgaa600 · Cited by 56 · see citing works
Probiotics and Polycystic Ovary Syndrome: A Perspective for Management in Adolescents with Obesity
Calcaterra, V., Rossi, V., Massini, G., Casini, F., Zuccotti, G., & Fabiano, V. (2023) · Nutrients · doi:10.3390/nu15143144 · Cited by 54 · see citing works
“However, different compositional changes have been identified in other studies [85,90].”
Arnone, A. A., & Cook, K. L. (2022) · Endocrinology · doi:10.1210/endocr/bqac177 · Cited by 53 · see citing works
Clemente‐Suárez, V. J., Redondo-Flórez, L., Rubio-Zarapuz, A., Martín-Rodríguez, A., & Tornero-Aguilera, J. F. (2024) · Biomedicines · doi:10.3390/biomedicines12010221 · Cited by 57 · see citing works
“A study by Lindheim et al. (2017) found significant differences in the gut microbiota of women with PCOS compared to healthy controls, suggesting a potential role of the microbiome in this disorder [145].”
Eyüpoğlu, D., Guzelce, E. C., Açıkgöz, A., Uyanık, E., Bjørndal, B., Berge, R. K., Svardal, A. M., & Yıldız, B. O. (2019) · Clinical Endocrinology · doi:10.1111/cen.14101 · Cited by 51 · see citing works
Hong, X., Ma, J., Yin, J., Fang, S., Geng, J., Zhao, H., Zhu, M., Ye, M., Zhu, X., Xuan, Y., et al. (2020) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-020-05675-3 · Cited by 51 · see citing works
Sex, puberty, and the gut microbiome
Sisk-Hackworth, L., Kelley, S. T., & Thackray, V. G. (2022) · Reproduction · doi:10.1530/rep-22-0303 · Cited by 51 · see citing works
“…women and adolescent girls with PCOS had lower alpha diversity and differences in beta diversity compared to healthy women and adolescent girls (Lindheim et al. 2017, Liu et al. 2017, Torres et al. 2018, Qi et al. 2019, Jobira Testosterone levels in women with PCOS also correlated with alpha…”
Mukherjee, A. G., Wanjari, U. R., Kannampuzha, S., Murali, R., Namachivayam, A., Ganesan, R., Dey, A., Babu, A., Renu, K., Vellingiri, B., et al. (2023) · Metabolites · doi:10.3390/metabo13010129 · Cited by 52 · see citing works
“In PCOS females, heightened zonulin levels were identified [69,72].”
Haudum, C. W., Lindheim, L., Ascani, A., Trummer, C., Horvath, A., Münzker, J., & Obermayer-Pietsch, B. M. (2020) · Nutrients · doi:10.3390/nu12061622 · Cited by 48 · see citing works
“Serum total testosterone, androstenedione, dehydroepiandrosterone (DHEA), DHEA sulfate (DHEAS), and dihydrotestosterone (DHT) were measured by liquid chromatography–tandem mass spectrometry as described elsewhere [14].”
Self-citation
- Authors
- Lindheim, L., Bashir, M., Münzker, J., Trummer, C., Zachhuber, V., Leber, B., Horvath, A., Pieber, T. R., Gorkiewicz, G., Stadlbauer, V., & Obermayer-Pietsch, B.
- Affiliations
- Medical University of Graz (AT)
- University of Graz (AT)
- Corresponding author
- Lindheim, Lisa
- ORCID
- Venue
- PLOS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2017-01-03
- Volume
- 12
- Issue
- 1
- Pages
- e0168390
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC5207627
- OpenAlex
- W2568515092
- Cited by
- 416
- References
- 50
- Citations by year
- 2026: 51 · 2025: 43 · 2024: 55 · 2023: 70 · 2022: 52 · 2021: 56 · 2020: 44 · 2019: 23 · 2018: 18 · 2017: 3
- FWCI
- 27.94
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- Austrian Science Fund (W1241)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Ovarian function and disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- polycystic ovary syndrome, gut microbiota, intestinal barrier, endotoxemia, intestinal permeability, microbial diversity, Tenericutes, Bacteroidetes, S24-7, inflammation, insulin resistance, hyperandrogenemia, reproductive disorders, metabolic defects
- MeSH terms
- Gastrointestinal Microbiome, Adult, Anthropometry, Feces, Female, Humans, Inflammation, Tenericutes, Pilot Projects, Polycystic Ovary Syndrome, Surveys and Questionnaires, RNA, Ribosomal, 16S, Case-Control Studies, Principal Component Analysis, Bacteroidetes, Real-Time Polymerase Chain Reaction
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
