Metabolic features of the reproductive phenotypes of polycystic ovary syndrome

Moran, Lisa; Teede, Helena

doi:10.1093/humupd/dmp008

Cited by 362Ovarian function and disordersDiabetes, Cardiovascular Risks, and LipoproteinsGenetic and Kidney Cyst Diseases

Metabolic features of the reproductive phenotypes of polycystic ovary syndrome

Moran, Lisa, Teede, Helena·2009·Human Reproduction Update

DOI 10.1093/humupd/dmp008

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Abstract

BACKGROUND Polycystic ovary syndrome (PCOS) is a common condition in women of reproductive age with well established metabolic abnormalities. There are numerous diagnostic criteria generating several reproductive diagnostic phenotypes [National Institute of Health (NIH) hyperandrogenic anovulatory PCOS and non-NIH PCOS including hyperandrogenic ovulatory or non-hyperandrogenic anovulatory PCOS]. There is ongoing debate regarding the optimal diagnostic criteria for PCOS and on the metabolic implications of newer non-NIH PCOS phenotypes. METHODS We reviewed the literature on the presence of risk factors for type 2 diabetes (DM2) and cardiovascular disease (CVD) across the reproductive diagnostic phenotypes of PCOS with the aims of comparing the metabolic features of the NIH and non-NIH groups and identifying potential high metabolic risk phenotypes of PCOS. RESULTS NIH PCOS patients present with greater obesity, abdominal obesity, insulin resistance (IR) and risk factors for DM2 and CVD compared with non-NIH ovulatory and non-hyperandrogenic PCOS patients. Where differences in metabolic features exist between the phenotypes, they are generally related to the degree of total and abdominal obesity. There is emerging evidence suggesting ovulatory and non-hyperandrogenic PCOS have greater metabolic abnormalities than controls primarily linked to abdominal adiposity. There is currently no evidence that non-hyperandrogenic PCOS is associated with a less adverse metabolic profile than ovulatory PCOS. CONCLUSIONS Current metabolic evidence appears to justify the inclusion of both non-NIH PCOS groups (ovulatory and non-hyperandrogenic) as PCOS subgroups. NIH PCOS is associated with a more adverse metabolic profile including greater total and abdominal obesity, IR and risk factors for CVD and DM2 than non-NIH phenotypes.

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PCOS has potential for major metabolic consequences, including obesity and related type 2 diabetes mellitus (DM2) as well as cardiovascular disease (CVD).
“PCOS has potential for major metabolic consequences, including obesity and related type 2 diabetes mellitus (DM2) as well as cardiovascular disease (CVD)”
From Assessment and management of polycystic ovary syndrome: Summary of an evidence-based guideline (2011) · cites this paper as [2]

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Fasting Serum Insulin Concentration and Early Insulin Response as Risk Determinants for Developing Diabetes
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Ethnic differences in insulin and glucose response to glucose between white and Indian women with polycystic ovary syndrome
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Vascular Dysfunction and Metabolic Parameters in Polycystic Ovary Syndrome
Meyer, C., McGrath, B. P., Cameron, J., Kotsopoulos, D., & Teede, H. J. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-1487 · Cited by 101 · see citing works
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Polycystic ovaries in hirsute women with normal menses
Carmina, E., & Løbo, R. A. (2001) · The American Journal of Medicine · doi:10.1016/s0002-9343(01)00979-2 · Cited by 101 · see citing works
Do hyperandrogenic women with normal menses have polycystic ovary syndrome?
Carmina, E., & Løbo, R. A. (1999) · Fertility and Sterility · doi:10.1016/s0015-0282(98)00455-5 · Cited by 100 · see citing works
Evidence for metabolic and reproductive phenotypes in mothers of women with polycystic ovary syndrome
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Endocrinology: Subjects with polycystic ovaries without hyperandrogenaemia exhibit similar disturbances in insulin and lipid profiles as those with polycystic ovary syndrome
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Plasma homocysteine in polycystic ovary syndrome: does it correlate with insulin resistance and ethnicity?
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Glucose intolerance, insulin resistance and cardiovascular risk factors in first degree relatives of women with polycystic ovary syndrome
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Impaired Carotid Viscoelastic Properties in Women With Polycystic Ovaries
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Differences in dyslipidemia between American and Italian women with polycystic ovary syndrome
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Brothers of women with polycystic ovary syndrome are characterised by impaired glucose tolerance, reduced insulin sensitivity and related metabolic defects
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Characteristics of different phenotypes of polycystic ovary syndrome in a Bulgarian population
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Correlation of plasma insulin and insulin‐like growth factor‐I with indices of androgen transport and metabolism in women with polycystic ovary syndrome
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Do polycystic-appearing ovaries affect the risk of cardiovascular disease among women with polycystic ovary syndrome?
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Comparison of clinical and laboratory characteristics of cases with polycystic ovarian syndrome based on Rotterdam’s criteria and women whose only clinical signs are oligo/anovulation or hirsutism
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Metabolic syndrome in females with polycystic ovary syndrome and International Diabetes Federation criteria
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Hyperinsulinemia and circulating dehydroepiandrosterone sulfate in white and Mexican American women with polycystic ovary syndrome
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Insulin levels in insulin resistance: phantom of the metabolic opera?
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The Combination of Increased Ovarian Volume and Follicle Number is Associated with More Severe Hyperandrogenism in German Women with Polycystic Ovary Syndrome
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Flutamide Suppresses Adrenal Steroidogenesis but Has No Effect on Insulin Resistance and Secretion and Lipid Levels in Overweight Women with Polycystic Ovary Syndrome
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Insulin Responses to the Oral Glucose Tolerance Test in Women of Different Ethnicity With Polycystic Ovary Syndrome
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Clinical and metabolic characteristics of polycystic ovary syndrome without polycystic ovary: a pilot study on Chinese women
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Insulin resistance in polycystic ovary syndrome: hyperandrogenemia versus normoandrogenemia
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Does ovarian blood flow distinguish between ovulatory and anovulatory patients with polycystic ovary syndrome?
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Investigation of hypothalamo-pituitary-gonadal axis and glucose intolerance among the first-degree female relatives of women with polycystic ovary syndrome
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Polycystic Ovary Syndrome: Definition, Aetiology, Diagnosis and Treatment
Escobar-Morreale, H. F. (2018) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2018.24 · Cited by 2,083 · see citing works
Consensus on women’s health aspects of polycystic ovary syndrome (PCOS): the Amsterdam ESHRE/ASRM-Sponsored 3rd PCOS Consensus Workshop Group
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Insulin Resistance and the Polycystic Ovary Syndrome Revisited: An Update on Mechanisms and Implications
Diamanti-Kandarakis, E., & Dunaif, A. (2012) · Endocrine Reviews · doi:10.1210/er.2011-1034 · Cited by 1,947 · see citing works
Polycystic ovary syndrome: a complex condition with psychological, reproductive and metabolic manifestations that impacts on health across the lifespan
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Self-citation
Polycystic ovary syndrome: etiology, pathogenesis and diagnosis
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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 · see citing works
Impaired Glucose Tolerance, Type 2 Diabetes and Metabolic Syndrome in Polycystic Ovary Syndrome: A Systematic Review and Meta-Analysis
Moran, L. J., Misso, M. L., Wild, R. A., & Norman, R. J. (2010) · Human Reproduction Update · doi:10.1093/humupd/dmq001 · Cited by 1,108 · see citing works
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Assessment of Cardiovascular Risk and Prevention of Cardiovascular Disease in Women with the Polycystic Ovary Syndrome: A Consensus Statement by the Androgen Excess and Polycystic Ovary Syndrome (AE-PCOS) Society
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Overweight, obesity and central obesity in women with polycystic ovary syndrome: a systematic review and meta-analysis
Lim, S. S., Davies, M. J., Norman, R. J., & Moran, L. J. (2012) · Human Reproduction Update · doi:10.1093/humupd/dms030 · Cited by 939 · see citing works
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Women with polycystic ovary syndrome have intrinsic insulin resistance on euglycaemic-hyperinsulaemic clamp
Stepto, N. K., Cassar, S., Joham, A. E., Hutchison, S. K., Harrison, C. L., Goldstein, R. F., & Teede, H. J. (2013) · Human Reproduction · doi:10.1093/humrep/des463 · Cited by 747 · see citing works
Self-citation
Lifestyle changes in women with polycystic ovary syndrome
Lim, S. S., Hutchison, S. K., Van Ryswyk, E., Norman, R. J., Teede, H. J., & Moran, L. J. (2019) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd007506.pub4 · Cited by 725 · see citing works
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Prevalence, phenotype and cardiometabolic risk of polycystic ovary syndrome under different diagnostic criteria
Yildiz, B. O., Bozdag, G., Yapici, Z., Esinler, I., & Yarali, H. (2012) · Human Reproduction · doi:10.1093/humrep/des232 · Cited by 704 · see citing works
Definition and significance of polycystic ovarian morphology: a task force report from the Androgen Excess and Polycystic Ovary Syndrome Society
Dewailly, D., Lujan, M. E., Carmina, E., Cedars, M. I., Laven, J., Norman, R. J., & Escobar-Morreale, H. F. (2014) · Human Reproduction Update · doi:10.1093/humupd/dmt061 · Cited by 551 · see citing works
Diagnosis of polycystic ovary syndrome (PCOS): revisiting the threshold values of follicle count on ultrasound and of the serum AMH level for the definition of polycystic ovaries
Dewailly, D., Gronier, H., Poncelet, É., Robin, G., Leroy, M., Pigny, P., Duhamel, A., & Catteau-Jonard, S. (2011) · Human Reproduction · doi:10.1093/humrep/der297 · Cited by 483 · see citing works
Extra- and intra-ovarian factors in polycystic ovary syndrome: impact on oocyte maturation and embryo developmental competence
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GLP-1 Receptor Agonists: Beyond Their Pancreatic Effects
Zhao, X., Wang, M., Wen, Z., Lu, Z., Cui, L., Fu, C., Xue, H., Liu, Y., & Zhang, Y. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.721135 · Cited by 463 · see citing works
Assessment and management of polycystic ovary syndrome: Summary of an evidence-based guideline
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Dysbiosis of Gut Microbiota [DOGMA]—A novel theory for the development of Polycystic Ovarian Syndrome
Tremellen, K., & Pearce, K. (2012) · Medical Hypotheses · doi:10.1016/j.mehy.2012.04.016 · Cited by 359 · see citing works
Deconstructing a Syndrome: Genomic Insights Into PCOS Causal Mechanisms and Classification
Dapas, M., & Dunaif, A. (2022) · Endocrine Reviews · doi:10.1210/endrev/bnac001 · Cited by 300 · see citing works
Distinct subtypes of polycystic ovary syndrome with novel genetic associations: An unsupervised, phenotypic clustering analysis
Dapas, M., Lin, F. T. J., Nadkarni, G. N., Sisk, R., Legro, R. S., Urbanek, M., Hayes, M. G., & Dunaif, A. (2020) · PLOS Medicine · doi:10.1371/journal.pmed.1003132 · Cited by 297 · see citing works
Lifestyle changes in women with polycystic ovary syndrome
Moran, L. J., Hutchison, S. K., Norman, R. J., & Teede, H. J. (2011) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd007506.pub3 · Cited by 292 · see citing works
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Complications and challenges associated with polycystic ovary syndrome: current perspectives
Palomba, S., Santagni, S., Falbo, A., & La Sala, G. B. (2015) · International Journal of Women's Health · doi:10.2147/ijwh.s70314 · Cited by 287 · see citing works
Association of metabolic and inflammatory markers with polycystic ovarian syndrome (PCOS): an update
Gnanadass, S. A., Prabhu, Y. D., & Gopalakrishnan, A. V. (2021) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-020-05951-2 · Cited by 299 · see citing works
Exercise therapy in polycystic ovary syndrome: a systematic review
Harrison, C. L., Lombard, C. B., Moran, L. J., & Teede, H. J. (2011) · Human Reproduction Update · doi:10.1093/humupd/dmq045 · Cited by 267 · see citing works
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Vitamin D deficiency is common and associated with metabolic risk factors in patients with polycystic ovary syndrome
Li, R., Brereton, R. E., Anderson, R. A., Wallace, A. M., & Ho, C. K. M. (2011) · Metabolism · doi:10.1016/j.metabol.2011.03.002 · Cited by 264 · see citing works
Divergences in insulin resistance between the different phenotypes of the polycystic ovary syndrome
Moghetti, P., Tosi, F., Bonin, C., Di Sarra, D., Fiers, T., Kaufman, J.-M., Giagulli, V. A., Signori, C., Zambotti, F., Dall'Alda, M., et al. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-3908 · Cited by 262 · see citing works
Metabolic risk in PCOS: Phenotype and adiposity impact
Moran, L. J., Norman, R. J., & Teede, H. J. (2015) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2014.12.003 · Cited by 245 · see citing works
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Physiological Aspects of Female Fertility: Role of the Environment, Modern Lifestyle, and Genetics
Hart, R. J. (2016) · Physiological Reviews · doi:10.1152/physrev.00023.2015 · Cited by 231 · see citing works
Should all women with PCOS be treated for insulin resistance?
Marshall, J. C., & Dunaif, A. E. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.11.036 · Cited by 219 · see citing works
Polycystic ovary syndrome as a metabolic disease
Helvacı, N., & Yıldız, B. O. (2024) · Nature Reviews Endocrinology · doi:10.1038/s41574-024-01057-w · Cited by 201 · see citing works
Cardiovascular disease in a nationwide population of Danish women with polycystic ovary syndrome
Glintborg, D., Rubin, K. H., Nybo, M., Abrahamsen, B., & Andersen, M. (2018) · Cardiovascular Diabetology · doi:10.1186/s12933-018-0680-5 · Cited by 200 · see citing works
Development and Risk Factors of Type 2 Diabetes in a Nationwide Population of Women With Polycystic Ovary Syndrome
Rubin, K. H., Glintborg, D., Nybo, M., Abrahamsen, B., & Andersen, M. (2017) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2017-01354 · Cited by 195 · see citing works
The Polycystic Ovary Post-Rotterdam: A Common, Age-Dependent Finding in Ovulatory Women without Metabolic Significance
Johnstone, E. B., Rosen, M. P., Neril, R., Trevithick, D., Sternfeld, B., Murphy, R. C., Addauan-Andersen, C., McConnell, D. S., Pera, R. A. R., & Cedars, M. I. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2010-0202 · Cited by 200 · see citing works
The management of patients with polycystic ovary syndrome
Jayasena, C. N., & Franks, S. (2014) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2014.102 · Cited by 196 · see citing works
Effects of Exercise on Insulin Resistance and Body Composition in Overweight and Obese Women with and without Polycystic Ovary Syndrome
Hutchison, S. K., Stepto, N. K., Harrison, C. L., Moran, L. J., Strauss, B. J., & Teede, H. J. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2010-0828 · Cited by 192 · see citing works
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Diabetes and cardiovascular events in women with polycystic ovary syndrome: a 20‐year retrospective cohort study
Mani, H., Levy, M. J., Davies, M. J., Morris, D. H., Gray, L. J., Bankart, J., Blackledge, H., Khunti, K. K., & Howlett, T. A. (2012) · Clinical Endocrinology · doi:10.1111/cen.12068 · Cited by 192 · see citing works
Comorbidities and complications of polycystic ovary syndrome: An overview of systematic reviews
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Ovarian Function and Obesity—Interrelationship, Impact on Women’s Reproductive Lifespan and Treatment Options
Rachoń, D., & Teede, H. (2010) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2009.09.026 · Cited by 161 · see citing works
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The metabolic syndrome - an ongoing story.
Duvnjak, L. S., & Duvnjak, M. (2009) · PubMed · Cited by 159 · see citing works
Insulin resistance and endocrine characteristics of the different phenotypes of polycystic ovary syndrome: a prospective study
Panidis, D., Tziomalos, K., Misichronis, G., Papadakis, E., Betsas, G., Katsikis, I., & Macut, D. (2012) · Human Reproduction · doi:10.1093/humrep/der418 · Cited by 155 · see citing works
Reconciling the Definitions of Polycystic Ovary Syndrome: The Ovarian Follicle Number and Serum Anti-Müllerian Hormone Concentrations Aggregate with the Markers of Hyperandrogenism
Dewailly, D., Pigny, P., Soudan, B., Catteau-Jonard, S., Decanter, C., Poncelet, É., & Duhamel, A. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2010-0334 · Cited by 155 · see citing works
Oxidative stress status in Chinese women with different clinical phenotypes of polycystic ovary syndrome
Zhang, R., Liu, H., Bai, H., Zhang, Y., Liu, Q., Guan, L., & Fan, P. (2016) · Clinical Endocrinology · doi:10.1111/cen.13171 · Cited by 139 · see citing works
Sleep disturbances in women with polycystic ovary syndrome: prevalence, pathophysiology, impact and management strategies
Fernandez, R., Moore, V., Van Ryswyk, E., Varcoe, T., Rodgers, R., March, W., Moran, L., Avery, J., McEvoy, D., & Davies, M. (2018) · Nature and Science of Sleep · doi:10.2147/nss.s127475 · Cited by 137 · see citing works
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Renaming PCOS—A Two-State Solution
Dunaif, A. E., & Fauser, B. C. J. M. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2013-2040 · Cited by 134 · see citing works
Criteria, phenotypes and prevalence of polycystic ovary syndrome
Belenkaia, L. V., Лазарева, Л. М., Walker, W., Lizneva, D., & Сутурина, Л. В. (2019) · Minerva Obstetrics and Gynecology · doi:10.23736/s0026-4784.19.04404-6 · Cited by 133 · see citing works
Serum antimullerian hormone (AMH) levels are elevated in adolescent girls with polycystic ovaries and the polycystic ovarian syndrome (PCOS)
Hart, R. J., Doherty, D. A., Norman, R. J., Franks, S., Dickinson, J. E., Hickey, M., & Sloboda, D. M. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2009.11.002 · Cited by 128 · see citing works
Physical activity and mental health in women with Polycystic Ovary Syndrome
Banting, L. K., Gibson-Helm, M., Polman, R., Teede, H. J., & Stepto, N. K. (2014) · BMC Women's Health · doi:10.1186/1472-6874-14-51 · Cited by 121 · see citing works
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Polycystic ovary syndrome: reviewing diagnosis and management of metabolic disturbances
Spritzer, P. M. (2014) · Arquivos Brasileiros de Endocrinologia & Metabologia · doi:10.1590/0004-2730000003051 · Cited by 118 · see citing works
The Role of Physical Activity in Preconception, Pregnancy and Postpartum Health
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Normo- and hyperandrogenic women with polycystic ovary syndrome exhibit an adverse metabolic profile through life
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Metabolic heterogeneity of polycystic ovary syndrome: from pathophysiology to phenotypic stratification
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Authors: Moran, L., & Teede, H.
Affiliations: Jean Hailes (AU)
Corresponding author: Moran, Lisa
ORCID: Moran, Lisa
Teede, Helena
Venue: Human Reproduction Update
Publisher: Oxford University Press (OUP)
Published: 2009
Volume: 15
Issue: 4
Pages: 477-488
ISSN: 1355-4786 (ISSN-L)
1460-2369
DOI: 10.1093/humupd/dmp008
OpenAlex: W2102318195
Cited by: 362
References: 113
Citations by year: 2026: 10 · 2025: 15 · 2024: 11 · 2023: 20 · 2022: 18 · 2021: 28 · 2020: 23 · 2019: 19 · 2018: 21 · 2017: 18 · 2016: 25 · 2015: 23 · 2014: 25 · 2013: 30 · 2012: 21
FWCI: 3.58
Type: journal article
Language: en
Open access: closed
Locations: Human Reproduction Update (publishedVersion)
PubMed (publishedVersion)
Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion)
Topics: Health Sciences › Medicine › Reproductive Medicine › Ovarian function and disorders
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes, Cardiovascular Risks, and Lipoproteins
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Kidney Cyst Diseases
Keywords: polycystic ovary syndrome, PCOS diagnostic criteria, metabolic abnormalities, insulin resistance, abdominal obesity, type 2 diabetes risk, cardiovascular risk
MeSH terms: Cardiovascular Diseases, Diabetes Mellitus, Type 2, Female, Humans, Insulin Resistance, Phenotype, Polycystic Ovary Syndrome, Risk Factors

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Metabolic features of the reproductive phenotypes of polycystic ovary syndrome

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