Cited by 555Ovarian function and disordersSexual Differentiation and DisordersReproductive Biology and Fertility

The DOI matches its Crossref record; 226 of the 231 references it cites were found in a registry or an index.

Androgen excess fetal programming of female reproduction: a developmental aetiology for polycystic ovary syndrome

Abbott, D.H., Barnett, D.K., Bruns, C.M., Dumesic, D.A.·2005·Human Reproduction Update

Open this paper in CoChat — free account

Abstract

The aetiology of polycystic ovary syndrome (PCOS) remains unknown. This familial syndrome is prevalent among reproductive-aged women and its inheritance indicates a dominant regulatory gene with incomplete penetrance. However, promising candidate genes have proven unreliable as markers for the PCOS phenotype. This lack of genetic linkage may represent both extreme heterogeneity of PCOS and difficulty in establishing a universally accepted PCOS diagnosis. Nevertheless, hyperandrogenism is one of the most consistently expressed PCOS traits. Animal models that mimic fetal androgen excess may thus provide unique insight into the origins of the PCOS syndrome. Many female mammals exposed to androgen excess in utero or during early post-natal life typically show masculinized and defeminized behaviour, ovulatory dysfunction and virilized genitalia, although behavioural and ovulatory dysfunction can coexist without virilized genitalia based upon the timing of androgen excess. One animal model shows particular relevance to PCOS: the prenatally androgenized female rhesus monkey. Females exposed to androgen excess early in gestation exhibit hyperandrogenism, oligomenorrhoea and enlarged, polyfollicular ovaries, in addition to LH hypersecretion, impaired embryo development, insulin resistance accompanying abdominal obesity, impaired insulin response to glucose and hyperlipidaemia. Female monkeys exposed to androgen excess late in gestation mimic these programmed changes, except for LH and insulin secretion defects. In utero androgen excess may thus variably perturb multiple organ system programming and thereby provide a single, fetal origin for a heterogeneous adult syndrome.

Integrity signals

Registry

Crossref · 10.1093/humupd/dmi013

Cites

226 of 226 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome
(2004) · Fertility and Sterility · doi:10.1016/j.fertnstert.2003.10.004 · Cited by 9,050
Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome (PCOS)
The Rotterdam ESHRE/ASRM-sponsored PCOS consensus workshop group (2004) · Human Reproduction · doi:10.1093/humrep/deh098 · Cited by 6,138
A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif
Sinclair, A. H., Berta, P., Palmer, M. S., Hawkins, J. R., Griffiths, B. L., Smith, M. J., Foster, J. W., Frischauf, A., Lovell-Badge, R. H., & Goodfellow, P. N. (1990) · Nature · doi:10.1038/346240a0 · Cited by 3,234
Insulin Resistance and the Polycystic Ovary Syndrome: Mechanism and Implications for Pathogenesis
Dunaif, A. E. (1997) · Endocrine Reviews · doi:10.1210/edrv.18.6.0318 · Cited by 2,776
The Prevalence and Features of the Polycystic Ovary Syndrome in an Unselected Population
Azziz, R., Woods, K. S., Reyna, R., Key, T. J., Knochenhauer, E. S., & Yıldız, B. O. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-032046 · Cited by 2,715
Estrogen Resistance Caused by a Mutation in the Estrogen-Receptor Gene in a Man
Smith, E. P., Boyd, J., Frank, G. R., Takahashi, H., Cohen, R. M., Specker, B., Williams, T. C., Lubahn, D. B., & Korach, K. S. (1994) · New England Journal of Medicine · doi:10.1056/nejm199410203311604 · Cited by 2,471
Polycystic Ovary Syndrome
Franks, S. (1995) · New England Journal of Medicine · doi:10.1056/nejm199509283331307 · Cited by 2,463
Prevalence and predictors of risk for type 2 diabetes mellitus and impaired glucose tolerance in polycystic ovary syndrome: A prospective, controlled study in 254 affected women
Legro, R. S. (1999) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.84.1.165 · Cited by 1,743
Androgen Receptor Defects: Historical, Clinical, and Molecular Perspectives*
Quigley, C. A., Bellis, A. D., Marschke, K. B., Awady, M. K. E., Wilson, E. M., & French, F. S. (1995) · Endocrine Reviews · doi:10.1210/edrv-16-3-271 · Cited by 1,459
Aromatase deficiency in male and female siblings caused by a novel mutation and the physiological role of estrogens
Morishima, A., Grumbach, M. M., Simpson, E. R., Fisher, C., & Qin, K. (1995) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.80.12.8530621 · Cited by 1,416

Flagged first, then by citations

Show all 231 references

5 of the 231 references couldn’t be matched to a known paper.

Research works printed but not linked: 8

Dewailly D, Cortet-Rudelli C and Deroubaix-Allard D (1997) Definition, clinical manifestations, and prevalence of PCOS. In Azziz R, Nestler JE, and Dewailly D (eds) Androgen Excess Disorders in Women. Lippincott-Raven Publishers, Philadelphia, PA, pp 259–268.
Fischer DA (2003) Endocrinology of fetal development. In Larsen PR, Kronenberg HM, Melmed S, and Polonsky KS (eds) Williams Textbook of Endocrinology. 10th edn. WB Saunders, Philadelphia, PA, pp 811–841.
Goy RW and Kemnitz JW (1983) Early, persistent, and delayed effects of virilizing substances delivered transplacentally to female rhesus fetuses. In Zbinden G, Cuomo V, Racagni G, and Weiss B (eds) Application of Behavioral Pharmacology in Toxicology. Raven Press, New York, pp 303–314.
Goy RW, Uno H and Sholl SA (1988) Psychological and anatomical consequences of prenatal exposure to androgens in female rhesus. In Mori T and Nagasawa H (eds) Toxicity of Hormones in Perinatal Life. CRC Press, Inc., Boca Raton, Florida, pp 127–142.
Hoar RM and Monie IW (1981) Comparative development of specific organ systems. In Kimmel CA and Buelke-Sam J (eds) Developmental Toxicology. Raven Press, New York, pp 13–33.
Knobil E and Hotchkiss J (1994) The menstrual cycle and its neuroendocrine control. In Knobil E, Neill J, Ewing LL, Greenwald GS, Markert CL, and Pfaff DW (eds) The Physiology of Reproduction, Vol 2. Raven Press, New York, pp 1971–1994.
Short RV (1974) Sexual differentiation of the brain of the sheep. In Forest MG and Bertrand J (eds) Sexual endocrinology of the perinatal period, Colloque International INSERM, Lyon. INSERM, Paris, France pp. 121–142.
Sperling MA (1994) Carbohydrate metabolism: insulin and glucagons. In Tulchinsky D and Little AB (eds) Maternal–Fetal Endocrinology. 2nd edn. WB Saunders, Philadelphia, PA, pp 380–400.

Sorted by citations

Items 301–400 of 554

Follicle Selection in Mammalian Ovaries
Findlay, J. K., Dunning, K. R., Gilchrist, R. B., Hutt, K. J., Russell, D. L., & Walters, K. A. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-813209-8.00001-7 · Cited by 20
AMH in PCOS: Controlling the ovary, placenta, or brain?
Moolhuijsen, L. M. E., & Visser, J. A. (2020) · Current Opinion in Endocrine and Metabolic Research · doi:10.1016/j.coemr.2020.04.006 · Cited by 20
Prenatal hyperandrogenism and lipid profile during different age stages: an experimental study
Heber, M. F., Ferreira, S. R., Vélez, L. M., & Motta, A. B. (2012) · Fertility and Sterility · doi:10.1016/j.fertnstert.2012.10.017 · Cited by 19
“This finding is in agreement with previous reports (10, 11, 13, 24).”
Testosterone induces activation of porcine primordial follicles in vitro
Magamage, M. P. S., Zengyo, M., Moniruzzaman, M., & Miyano, T. (2010) · Reproductive Medicine and Biology · doi:10.1007/s12522-010-0068-z · Cited by 19
“There are some reports in primates [29, 30] and cows [31] showing that exposure of the fetal ovary to androgens may cause an increase in the number of primary or secondary follicles.”
Background
Female Offspring From Chronic Hyperandrogenemic Dams Exhibit Delayed Puberty and Impaired Ovarian Reserve
Wang, Z., Shen, M., Xue, P., DiVall, S. A., Segars, J. H., & Wu, S. (2018) · Endocrinology · doi:10.1210/en.2017-03078 · Cited by 18
Endocrine and metabolic interactions in healthy pregnancies and hyperinsulinemic pregnancies affected by polycystic ovary syndrome, diabetes and obesity
Neven, A. C. H., Mousa, A., Boyle, J. A., & Teede, H. J. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.993619 · Cited by 24
Perturbateurs endocriniens – Reproduction et cancers hormono-dépendants
Fénichel, P., Brücker-Davis, F., & Chevalier, N. (2015) · La Presse Médicale · doi:10.1016/j.lpm.2015.10.017 · Cited by 18
A Hyperandrogenic Mouse Model to Study Polycystic Ovary Syndrome
Xue, P., Wang, Z., Fu, X., Wang, J., Punchhi, G., Wolfe, A., & Wu, S. (2018) · Journal of Visualized Experiments · doi:10.3791/58379 · Cited by 18
The relationship between the second to fourth digit ratio and acne vulgaris
Bilgiç, Ö., Doğdu, M., İslamoğlu, Z. G. K., & Altınyazar, C. (2013) · Journal of the European Academy of Dermatology and Venereology · doi:10.1111/jdv.12287 · Cited by 18
Disrupting Amh and androgen signaling reveals their distinct roles in zebrafish gonadal differentiation and gametogenesis
Wu, K., Yiming, Y. U. E., Zhou, L., ZHANG, Z., Shan, H., He, H., & Ge, W. (2025) · Communications Biology · doi:10.1038/s42003-025-07719-3 · Cited by 17
Gut microbiota-derived short-chain fatty acids promote follicular maturation via gWAT-ovary axis in mammals
Xu, B., Qin, W., Chen, Y., Yan, Z., Tang, Y., Zhou, S., Huang, J., Ma, L., & Yan, X. (2025) · Microbiome · doi:10.1186/s40168-025-02174-y · Cited by 19
“Since estradiol in follicular fluid is a marker of preovulatory oocyte quality [52], the continued significant increase in estradiol concentration throughout the third estrous cycle attracted our attention.”
Positive Effects of α-Lactalbumin in the Management of Symptoms of Polycystic Ovary Syndrome
Cardinale, V., Lepore, E., Basciani, S., Artale, S. A., Nordio, M., Bizzarri, M., & Unfer, V. (2022) · Nutrients · doi:10.3390/nu14153220 · Cited by 18
“The prenatal exposure to maternal hyperandrogenic milieu in pregnant women with PCOS results in increased androgen secretion, insulin resistance and weight gain at birth, supporting the hypothesis of a transmission of PCOS dysbiotic microbiota from the mother to neonates [89,90].”
Background
An Evolutionary Model for the Ancient Origins of Polycystic Ovary Syndrome
Dumesic, D. A., Abbott, D. H., & Chazenbalk, G. D. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12196120 · Cited by 17
“They exhibit increased abdominal subcutaneous and visceral adiposity [128,133,135], adipose insulin resistance and impaired insulin secretion [136], and an increased incidence of T2DM [137].”
Background
Ovarian Germ Cells
Bukovský, A., Virant‐Klun, I., Svetlikova, M., & Willson, I. (2006) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(06)19010-2 · Cited by 17
Effects of Perinatal Testosterone on Infant Health, Mother–Infant Interactions, and Infant Development
Cho, J., & Holditch‐Davis, D. (2013) · Biological Research For Nursing · doi:10.1177/1099800413486340 · Cited by 17
Chronic anovulation and the polycystic ovary syndrome
KASE, N. G. (2013) · Cambridge University Press eBooks · doi:10.1017/cbo9781139003254.012 · Cited by 16
Very low dose spironolactone protects experimentally-induced polycystic ovarian syndrome from insulin-resistant metabolic disturbances by suppressing elevated circulating testosterone
Adeyanju, O. A., Falodun, T. O., Fabunmi, O. A., Olatunji, L. A., & Soladoye, A. O. (2019) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2019.108742 · Cited by 17
Prenatal Androgens Affect Development and Behavior in Primates
Smith, A. S., Birnie, A. K., & French, J. A. (2012) · Springer eBooks · doi:10.1007/978-1-4614-4060-4_5 · Cited by 17
“5.3.2.1 , Abbott et al. 2005 ) that results in a signi fi cant elevation of androgens in fetal circulation (Resko et al. 1987 ; Abbott et al. 2008 ) .”
BackgroundInfluential
Developmental androgenization programs metabolic dysfunction in adult mice: Clinical implications
Mauvais-Jarvis, F. (2014) · Adipocyte · doi:10.4161/adip.27746 · Cited by 15
Are 2D:4D finger-length ratios an indicator of androgenetic alopecia in males?
Bilgiç, Ö., Altinyazar, H. C., Eryılmaz, D., & Tuğrul, Z. A. (2016) · Anais Brasileiros de Dermatologia · doi:10.1590/abd1806-4841.20164622 · Cited by 15
Androgen and Anti-Mullerian Hormone Concentrations at Term in Newborns and Their Mothers with and without Polycystic Ovary Syndrome
Kollmann, M., Obermayer-Pietsch, B. M., Lerchbaum, E., Lang, U., Herzog, S. A., Trummer, C., Scheuchenegger, A., Ulrich, D., & Klaritsch, P. (2019) · Journal of Clinical Medicine · doi:10.3390/jcm8111817 · Cited by 16
Generational Health Impact of PCOS on Women and Their Children
Hart, R. J. (2019) · Medical Sciences · doi:10.3390/medsci7030049 · Cited by 15
“The consequent higher exposure to androgens may program PCOS in the offspring [23] as evidence derived from animal studies suggests treating pregnant rhesus monkeys with testosterone leads to the development of a PCOS-like phenotype in the offspring [24], providing a further potential transgenerational mechanism for t…”
Background
Epigenetic pattern changes in prenatal female Sprague-Dawley rats following exposure to androgen
Xia, Y., Shen, S., Zhang, X., Deng, Z., Zou, X., Wang, H., Yi, L., Gao, Q., & Wang, Y. (2015) · Reproduction Fertility and Development · doi:10.1071/rd14292 · Cited by 15
“Because it has been reported that the female reproductive system is influenced by the timing of androgen exposure (Abbott et al. 2005), the morphology of the genitalia was also examined.”
Background
Pubertal development among girls with classical congenital adrenal hyperplasia initiated on treatment at different ages
Ammini, A., Kulshreshtha, B., & Eunice, M. (2012) · Indian Journal of Endocrinology and Metabolism · doi:10.4103/2230-8210.98018 · Cited by 19
“Prenatal androgen exposure in nonhuman primates and sheep produces many features of polycystic ovary syndrome (PCOS).[1-4] Androgens act on the brain to induce major sex differences in neural structure and function.”
Characteristics of polycystic ovary syndrome rat models induced by letrozole, testosterone propionate and high-fat diets
Hu, R., Huang, Y., Liu, Z., Dong, H., Ma, W., Song, K., Xu, X., Wu, X. W., Geng, Y., Li, F., et al. (2024) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2024.104296 · Cited by 16
Reproductive medicine and inheritance of infertility by offspring: the role of fetal programming
Díaz‐García, C., Estella, C., Perales‐Puchalt, A., & Simón, C. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.06.066 · Cited by 14
Animal Models and Fetal Programming of the Polycystic Ovary Syndrome
Abbott, D. H., Dumesic, D. A., Levine, J. E., Dunaif, A. E., & Padmanabhan, V. (2007) · Humana Press eBooks · doi:10.1007/978-1-59745-179-6_23 · Cited by 14
“Compared with other animal models for PCOS, models of fetal programming have one clear advantage: simultaneous exposure of multiple organ systems to a specific developmental insult during differentiation and maturation (Fig. 1). Altered structure and function is commonly permanent, such as fetal androgen excess virili…”
BackgroundInfluential
Endocrine control of epigenetic mechanisms in male reproduction
Ankolkar, M., & Balasinor, N. (2016) · Hormone Molecular Biology and Clinical Investigation · doi:10.1515/hmbci-2016-0007 · Cited by 14
Regulation of zebrafish gonadal sex differentiation
Pradhan, A., & Olsson, P. (2016) · AIMS molecular science · doi:10.3934/molsci.2016.4.567 · Cited by 14
“cardiovascular, inflammatory, oncological and sleep systems [148].”
Background
A Comparison of Sexual Function in Women with Polycystic Ovary Syndrome (PCOS) Whose Mothers Had PCOS During Their Pregnancy Period with Those Without PCOS
Noroozzadeh, M., Tehrani, F. R., Khomami, M. B., & Azizi, F. (2017) · Archives of Sexual Behavior · doi:10.1007/s10508-016-0919-8 · Cited by 14
Hair cortisol in polycystic ovary syndrome
González, D., Maidana, P. N. A., Ibar, C., Jamardo, J., Jacobsen, D., Fritzler, A., Fortuna, F., Fernandez, G., Majek, E. L., Mallea-Gil, S., et al. (2022) · Scientific Reports · doi:10.1038/s41598-022-14061-9 · Cited by 15
Anogenital distance and anti-Müllerian hormone combined improves the diagnosis of polycystic ovary syndrome
Prieto‐Sánchez, M. T., Peñalver, A. I. H., Sánchez-Ferrer, M. L., Mendiola, J., & Torres-Cantero, A. M. (2020) · Human Fertility · doi:10.1080/14647273.2020.1795574 · Cited by 13
“Although there are other hypotheses on the pathogenesis of this disorder, the role of the intrauterine hormonal environment is gaining acceptance (Abbott et al., 2005).”
Background
Models and Mechanisms of Metabolic Regulation: Genes, Stress, and the HPA and HPG Axes
Boersma, G. J., Salton, S. R., Spritzer, P. M., Steele, C. T., & Carbone, D. L. (2012) · Hormone and Metabolic Research · doi:10.1055/s-0032-1311576 · Cited by 13
Achieving a Successful Pregnancy in Women with Polycystic Ovary Syndrome
Araki, T., Elias, R. T., Rosenwaks, Z., & Poretsky, L. (2011) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/j.ecl.2011.08.003 · Cited by 13
Polycystic ovary syndrome or hyperprolactinaemia: a study of mild hyperprolactinaemia
Su, H.-W., Chen, C., Chou, S.-Y., Liang, S.-J., Hsu, C.-S., & Hsu, M.-I. (2010) · Gynecological Endocrinology · doi:10.3109/09513590.2010.487606 · Cited by 13
“The lack of a genetic link and PCOSs extreme heterogeneity cause difficulties in establishing a universally acceptable PCOS diagnosis [2], which is still based mainly on clinical and physical findings.”
Background
Prenatal Androgen Excess Induces Multigenerational Effects on Female and Male Descendants
Abruzzese, G. A., Ferreira, S. R., Ferrer, M. J., Silva, A. F., & Motta, A. B. (2023) · Clinical Medicine Insights Endocrinology and Diabetes · doi:10.1177/11795514231196461 · Cited by 12
PCOS and the Genome: Is the Genetic Puzzle Still Worth Solving?
Palumbo, M., Corte, L. D., Colacurci, D., Ascione, M., D’Angelo, G., Baldini, G. M., Giampaolino, P., & Bifulco, G. (2025) · Biomedicines · doi:10.3390/biomedicines13081912 · Cited by 14
“Nonetheless, to acknowledge the foundational importance of these genes in PCOS pathogenesis, we have included a dedicated summary table (Table 3) within the manuscript, which presents their biological functions and associated molecular pathways in a structured and comparative format [2,7,24].”
Gender Differences in Cannabis Addiction and Dependence
Davis, C. A., & Fattore, L. (2015) · Springer eBooks · doi:10.1007/978-1-4939-2294-9_12 · Cited by 12
The abnormal expression of kisspeptin regulates pro-inflammatory cytokines, cell viability and apoptosis of macrophages in hyperandrogenism induced by testosterone
Xiao, L., Li, L., Ouyang, D., Zhu, Y., & Yuan, T. (2020) · Gynecological Endocrinology · doi:10.1080/09513590.2020.1811964 · Cited by 12
Intergenerational Influences between Maternal Polycystic Ovary Syndrome and Offspring: An Updated Overview
Zhang, F.-F., Zhang, Q., Wang, Y.-L., Wang, F., Hardiman, P., & Qu, F. (2021) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2021.01.018 · Cited by 14
Syndrome des ovaires polymicrokystiques : une pathologie à risque obstétrical ?
Bruyneel, A., Catteau-Jonard, S., Decanter, C., Clouqueur, É., Tomaszewski, C., Subtil, D., Dewailly, D., & Robin, G. (2014) · Gynécologie Obstétrique & Fertilité · doi:10.1016/j.gyobfe.2014.01.001 · Cited by 13
“[62] Abbott DH, Barnett DK, Bruns CM, Dumesic DA.”
A Randomized Clinical Trial on Comparing The Cycle Characteristics of Two Different Initiation Days of Letrozole Treatment in Clomiphene Citrate Resistant PCOS Patients in IUI Cycles.
Ghomian, N., Khosravi, A., & Mousavifar, N. (2015) · PubMed Central · doi:10.22074/ijfs.2015.4204 · Cited by 12
“The other effect of hyperandrogenism in PCOS pregnant patients at the early embryonic stage has been proposed as a developmental etiology for PCOS in female fetus (27).”
Background
The association of TAAAAn repeat polymorphism in sex hormone-binding protein gene with polycystic ovary syndrome in Chinese population
Liu, Q., Gu, W., Cui, B., Hong, J., Zhang, Y., Chi, Z.-N., Su, Y., & Ning, G. (2008) · Endocrine · doi:10.1007/s12020-008-9104-8 · Cited by 12
Prenatal Testosterone Exposure Disrupts Insulin Secretion and Promotes Insulin Resistance
Carrasco, A., Recabarren, M. P., Rojas-García, P. P., Gutiérrez, M., Morales, K., Sir-Petermann, T., & Recabarren, S. E. (2020) · Scientific Reports · doi:10.1038/s41598-019-57197-x · Cited by 10
Role of the mitophagy‐apoptosis axis in the pathogenesis of polycystic ovarian syndrome
Kobayashi, H., Shigetomi, H., Matsubara, S., Yoshimoto, C., & Imanaka, S. (2024) · Journal of obstetrics and gynaecology research · doi:10.1111/jog.15916 · Cited by 14
Polycystic ovary syndrome induced by exposure to testosterone propionate and effects of sympathectomy on the persistence of the syndrome
Morales‐Ledesma, L., Ramos, J. A. D., & Trujillo, A. (2017) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-017-0267-0 · Cited by 11
Fetal androgen excess provides a developmental origin for polycystic ovary syndrome
Abbott, D. H., & Dumesic, D. A. (2009) · Expert Review of Obstetrics & Gynecology · doi:10.1586/17474108.4.1.1 · Cited by 11
Self-citation
Does the sex of one’s co-twin affect height and BMI in adulthood? A study of dizygotic adult twins from 31 cohorts
Bogl, L. H., Jelenkovic, A., Vuoksimaa, E., Ahrenfeldt, L. J., Pietiläinen, K. H., Stazi, M. A., Fagnani, C., D’Ippolito, C., Hur, Y., Jeong, H., et al. (2017) · Biology of Sex Differences · doi:10.1186/s13293-017-0134-x · Cited by 11
“Female rhesus monkeys exposed to increased levels of testosterone during early-to-mid gestation develop metabolic abnormalities found in PCOS women, including insulin resistance, increased visceral fat accumulation, impaired pancreatic beta-cell function, and type 2 diabetes [28, 31, 35].”
Background
Prenatal undernutrition affects the phenotypes of PCOS model rats
Iwasa, T., Matsuzaki, T., Yano, K., Mayila, Y., Yanagihara, R., Yamamoto, Y., Kuwahara, A., & Irahara, M. (2018) · Journal of Endocrinology · doi:10.1530/joe-18-0335 · Cited by 11
Sex differences in androgen regulation of metabolism in nonhuman primates
True, C., Abbott, D. H., Roberts, C. T., & Varlamov, O. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-70178-3_24 · Cited by 10
Microbial Dysbiosis and Pathogenic Interplay in the Gut-Vaginal Axis: Implications for Polycystic Ovary Syndrome: A Critical Review
Sudhakaran, G., Sreekutty, A. R., Choi, K. C., Arasu, M. V., Guru, A., Namasivayam, S. K. R., & Arockiaraj, J. (2026) · Current Microbiology · doi:10.1007/s00284-026-04749-w · Cited by 11
Trends in Acupuncture Therapy for Microcirculation and Hemorheology from 1998 to 2023: A Bibliometric and Visualized Study
Wang, Q., Zhang, Q., Lu, F., Hu, H., & Zhu, M. (2024) · Journal of Pain Research · doi:10.2147/jpr.s441512 · Cited by 10
Polycystic Ovary Syndrome in Adolescents
Saleh, F., Starkman, H., Furness, A., Pfeifer, S. M., & Kives, S. L. (2024) · Obstetrics and Gynecology Clinics of North America · doi:10.1016/j.ogc.2024.08.005 · Cited by 12
Neuropeptide Network of Polycystic Ovary Syndrome – A Review
Jayamurali, D., Ravishankar, N., Manoharan, N., Parasuraman, R., Jayashankar, S. K., & Govindarajulu, S. N. (2024) · Protein and Peptide Letters · doi:10.2174/0109298665309949240822105900 · Cited by 13
Management of Polycystic Ovary Syndrome in Childhood and Adolescence
Ojaniemi, M., Tapanainen, P. J., & Morin-Papunen, L. C. (2010) · Hormone Research in Paediatrics · doi:10.1159/000320388 · Cited by 10
Organizational Effects of Gonadal Hormones on Human Sexual Orientation
Swift‐Gallant, A., Aung, T., Rosenfield, K. A., Dawood, K., & Puts, D. A. (2023) · Adaptive Human Behavior and Physiology · doi:10.1007/s40750-023-00226-x · Cited by 11
“Genetic and prenatal environmental causes of PCOS have been suggested (Abbott et al., 2005; Barry et al., 2010; Bronstein et al., 2011; Goodarzi et al., 2007), and evidence implicates elevated early androgens (Gur et al., 2015; Homburg, 2009 ; Homburg et al., 2017; Xita & Tsatsoulis, 2006).”
Background
Microarray analysis of neonatal rat anteroventral periventricular transcriptomes identifies the proapoptotic Cugbp2 gene as sex-specific and regulated by estradiol
del Pino, J., Krishnan, S., Aggison, L. K., Adams, H. L., Mane, S., López‐Giráldez, F., & Petersen, S. L. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.07.008 · Cited by 10
Investigation of the Association of the Second-to-Fourth Digit Ratio with Skin Sebum Levels in Females with Acne Vulgaris
Bilgiç, Ö., Altınyazar, C., Hıra, H., & Doğdu, M. (2015) · American Journal of Clinical Dermatology · doi:10.1007/s40257-015-0147-3 · Cited by 10
“rhesus monkeys and sheep exposed to induced fetal androgen [26].”
Background
Polycystic ovary syndrome in adolescents: a review of past year evidence
Javed, A., Chelvakumar, G., & Bonny, A. E. (2016) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/gco.0000000000000301 · Cited by 10
“Normative testosterone levels are ill defined in this age group [3], and PCOM can occur without any evidence of PCOS [4].”
Background
Premature adrenarche, polycystic ovary syndrome and intrauterine growth retardation: does a relationship exist?
van Weissenbruch, M. M. (2007) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0b013e328013da7d · Cited by 10
POLYCYSTIC OVARY SYNDROME: ORIGINS AND IMPLICATIONS: Polycystic ovary syndrome: an evolutionary metabolic adaptation
Dumesic, D. A., Padmanabhan, V., & Abbott, D. H. (2025) · Reproduction · doi:10.1530/rep-25-0021 · Cited by 11
Polycystic ovary syndrome in Latin American populations: What is known and what remains unresolved
Abruzzese, G. A., Velázquez, M. E., Cerrone, G. E., & Motta, A. B. (2022) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2022.106195 · Cited by 13
Ameliorative effects of quercetin on endocrine and metabolic abnormalities associated with experimentally induced polycystic ovary syndrome in mice
Shah, M. Z. U. H., & Shrivastava, V. K. (2023) · Comparative Clinical Pathology · doi:10.1007/s00580-023-03446-5 · Cited by 9
Role of diacerein on steroidogenesis and folliculogenesis related genes in ovary of letrozole-induced PCOS mice
Shah, M. Z. U. H., Shrivastava, V. K., Mir, M. A., & Olaniyi, K. S. (2023) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2023.110468 · Cited by 9
STUDY ON FOLLICLE STIMULATING HORMONE RECEPTOR GENE POLYMORPHISMS IN SOUTH INDIAN WOMEN WITH POLYCYSTIC OVARIAN SYNDROME
Kambalachenu (2013) · Current Research in Medicine · doi:10.3844/amjsp.2013.160.167 · Cited by 9
“Diagnosis of PCOS is primarily based on clinical and biochemical findings (Abbott et al., 2005).”
Influence of having a male twin on body mass index and risk for dyslipidemia in middle-aged and old women
Alexanderson, C., Henningsson, S., Lichtenstein, P., Holmäng, A. B., & Eriksson, E. (2011) · International Journal of Obesity · doi:10.1038/ijo.2011.18 · Cited by 9
Polycystic ovary syndrome as a developmental disorder
Goverde, A. J., Westerveld, H. E., Veltman-Verhulst, S. M., & Fauser, B. C. J. M. (2008) · Expert Review of Obstetrics & Gynecology · doi:10.1586/17474108.3.6.775 · Cited by 8
Androgens: they don’t just make a man out of you
Sen, A., & Hammes, S. R. (2010) · Expert Review of Obstetrics & Gynecology · doi:10.1586/eog.10.73 · Cited by 8
Genetic and Environmental Factors in the Etiology of Polycystic Ovary Syndrome
Barber, T. M., & Franks, S. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-813209-8.00027-3 · Cited by 10
Thada Is Dispensable for Female Fertility in Mice
Han, S., Zhang, Y., Zheng, Y., Liu, C., Jiang, Y., Zhao, S., & Zhao, H. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.787733 · Cited by 8
Beneficial effects of Teucrium polium hydroalcoholic extract on letrozole-induced polycystic ovary syndrome (PCOS) in rat model
Khosrowpour, Z., Fahimi, S., Jafari, F., Tansaz, M., Sahranavard, S., & Faizi, M. (2022) · Obstetrics & Gynecology Science · doi:10.5468/ogs.22129 · Cited by 8
“Polycystic ovaries can be induced by excess secondary endogenous androgen [20].”
Background
Low birth weight may increase body fat mass in adult women with polycystic ovarian syndrome
Minooee, S., Tehrani, F. R., Mirmiran, P., & Azizi, F. (2016) · International Journal of Reproductive BioMedicine (IJRM) · doi:10.29252/ijrm.14.5.335 · Cited by 8
“he etiology of Polycystic Ovarian Syndrome (PCOS) as the commonst endocrine disorder in reproductive aged women is not clear, although, the genetic and environmental factors are known to have an important role (1, 2).”
Background
Emerging Topics in Cardiometabolic and Psychologic Sequelae, Pathogenesis, and Treatment of Polycystic Ovarian Syndrome: A Review
Shah, R. D. (2019) · Children · doi:10.3390/children6080089 · Cited by 9
“In the rhesus monkey, exposure to androgen excess early in gestation led to PCOS phenotype with hyperandrogenism, oligomenorrhea, LH hypersecretion, enlarged multi-follicular ovaries in addition to insulin resistance, hyperlipidemia, and increased abdominal adiposity [59].”
Background
Polycystic Ovary Syndrome
Paschou, S. Α., Goulis, D. G., & Tarlatzis, B. C. (2019) · ISGE series · doi:10.1007/978-3-030-14358-9_5 · Cited by 8
The relationship of urocortin-2 with insulin resistance patients having PCOS
Temür, M., Yılmaz, Ö., Aksun, S., Çalan, M., Özbay, P. Ö., Kumbasar, S., & Sever, E. (2016) · Gynecological Endocrinology · doi:10.1080/09513590.2016.1240772 · Cited by 8
Paracrine and intracrine contributions of androgens and estrogens to adipose tissue biology: physiopathological aspects
Waraich, R. S., & Mauvais-Jarvis, F. (2013) · hmbci · doi:10.1515/hmbci-2013-0022 · Cited by 8
Anogenital Distance: Features, Measures, and Uses as a Biomarker for Toxicity In Utero
Svingen, T., Hass, U., Schwartz, C. L., & Christiansen, S. (2023) · Biomarkers in disease · doi:10.1007/978-3-031-07392-2_37 · Cited by 7
Accounting for the Follicle Population in the Polycystic Ovary
Dumesic, D. A., & Abbott, D. H. (2008) · Humana Press eBooks · doi:10.1007/978-1-59745-108-6_2 · Cited by 7
“Androgen effects on early follicle growth also can be induced by reprogramming adult ovarian morphology during prenatal development ( 28 ).”
Background
Antimullerian Hormone and Its Receptor Gene Expression in Prenatally Androgenized Female Rats
Daneshian, Z., Tehrani, F. R., Zarkesh, M., Zadeh, M. N., Mahdian, R., & Zadeh–Vakili, A. (2013) · Intern J Endocrinol Metab · doi:10.5812/ijem.19511 · Cited by 7
“Experimental induction of androgen excess during prenatal life in female rhesus monkeys, ewes, and rats has been shown to exert appropriate PCOS-like phenotypes (4-6).”
Background
Elevated hypothalamic aromatization at the onset of precocious puberty in transgenic female mice hypersecreting human chorionic gonadotropin: Effect of androgens
González, B., Ratner, L. D., Scerbo, M. J., Giorgio, N. P. D., POUTANEN, M. H., Huhtaniemi, I. T., Calandra, R. S., Lux-Lantos, V. A., Cambiasso, M. J., & Rulli, S. B. (2014) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2014.04.005 · Cited by 7
“The mechanisms by which androgens alter the female neuroendocrine function is not fully understood, but it has been shown that exposure of females to supraphysiological levels of androgens during critical periods of development may increase the risk of reproductive disorders, such as PP and polycystic ovarian syndrome…”
Metabolic evaluation of young women with congenital adrenal hyperplasia
Schnaider, G. S., de Lemos‐Marini, S. H. V., Baptista, M. T. M., Guerra‐Júnior, G., Morcillo, A. M., de Mello, M. P., de Oliveira, L. C., & D’Souza-Li, L. F. R. (2011) · Arquivos Brasileiros de Endocrinologia & Metabologia · doi:10.1590/s0004-27302011000800021 · Cited by 7
“Studies in animal models suggest that prenatal and neonatal androgen exposure increase adiposity and insulin resistance, and alters lipolysis in adulthood, indicating that androgens may induce metabolic reprogramming (4-7).”
BackgroundMethodInfluential
Polycystic Ovarian Syndrome
Hernández, M. I., & Verónica Mericq, G. (2009) · doi:10.1002/9781444316728.ch21 · Cited by 7
Utility of Childhood Glucose Homeostasis Variables in Predicting Adult Diabetes and Related Cardiometabolic Risk Factors: The Bogalusa Heart Study
d’Annunzio, G., Russo, C., & Lorini, R. (2010) · Diabetes Care · doi:10.2337/dc10-0827 · Cited by 7
Early Developmental Programming of the Ovarian Reserve, Ovarian Function, and Fertility
Mossa, F., Walsh, S. W., Evans, A., Jimenez-Krassel, F., & Ireland, J. (2017) · doi:10.1002/9781118881286.ch4 · Cited by 6
SERUM IRISIN AND LEPTIN LEVELS IN OBESE AND NON-OBESE WOMEN WITH POLYCYSTIC OVARY SYNDROME WITH REFERENCE TO GLUCOSE HOMEOSTASIS
Ali, S. H., Alnuaimi, A., & Al-Musawi, B. J. M. (2016) · International Journal of Pharmacy and Pharmaceutical Sciences · doi:10.22159/ijpps.2016v8i10.14160 · Cited by 6
In utero exposure to maternal stressful life events and risk of polycystic ovary syndrome in the offspring: The Raine Study
Koch, T., Doherty, D. A., Dickinson, J. E., Juul, A., Hart, R. J., Bräuner, E. V., & Hickey, M. (2020) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2020.105104 · Cited by 25
Manejo dietético e suplementar na fisiopatologia da síndrome dos ovários policísticos
Xavier, E. C. D. S., & Freitas, F. M. N. D. O. (2021) · Research Society and Development · doi:10.33448/rsd-v10i15.22975 · Cited by 6
Syndrome des ovaires polymicrokystiques
Robin, G., Proust-Richard, C., Jonard-Catteau, S., & Dewailly, D. (2007) · EMC - Endocrinologie - Nutrition · doi:10.1016/s1155-1941(07)35089-0 · Cited by 6
The impact of postnatal leuprolide acetate treatment on reproductive characteristics in a rodent model of polycystic ovary syndrome
Mujica, L. K. S., Bertolin, K., Bridi, A., Glanzner, W. G., Rissi, V. B., de Camargo, F. C. D. L. S., Zanella, R., Prestes, O. D., Moresco, R. N., Antoniazzi, A. Q., et al. (2016) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.12.015 · Cited by 6
Low birth-weight is a PCOS risk factor for Southern-Italian women
Stracquadanio, M., & Ciotta, L. (2017) · Gynecological Endocrinology · doi:10.1080/09513590.2017.1283487 · Cited by 6
“genism) occur when epigenetic changes take place during early gestation [25].”
Background
Testosterone exposure in prenatal life disrupts epithelial nuclear morphology, smooth muscle layer pattern, and FGF10 and Shh expression in prostate
Manso, L. A., Medeiros, B. C. M., Rodrigues, G. A., Ramos, J. G., Marques, M. R., Taboga, S. R., dos Santos, F. C. A., & Biancardi, M. F. (2021) · Life Sciences · doi:10.1016/j.lfs.2021.119198 · Cited by 6
Le syndrome des ovaires polymicrokystiques – ou les follicules dans tous leurs excès
Robin, G., Catteau-Jonard, S., Dewailly, D., & Decanter, C. (2010) · Gynécologie Obstétrique & Fertilité · doi:10.1016/j.gyobfe.2010.04.006 · Cited by 6
Nonalcoholic fatty liver disease in children and adolescents – Relationship with Polycystic Ovary Syndrome
Abruzzese, G. A., & Motta, A. B. (2015) · Current Pharmaceutical Design · doi:10.2174/1381612821666150928105959 · Cited by 6
Hyperandrogenism, Hirsutism, and Polycystic Ovary Syndrome
Barnes, R. B., Ehrmann, D. A., & Rosenfield, R. L. (2010) · Elsevier eBooks · doi:10.1016/b978-1-4160-5583-9.00132-5 · Cited by 6
Next-generation Approaches in Targeting Polycystic Ovarian Syndrome: Innovative Strategies
Narayanan, P. L., Sugumar, S., Rushendran, R., & Vellapandian, C. (2025) · Current Medicinal Chemistry · doi:10.2174/0109298673368951250404170052 · Cited by 5
Knowledge graph construction based on granulosa cells transcriptome from polycystic ovary syndrome with normoandrogen and hyperandrogen
Liu, W., Tang, T., Feng, J., Wang, C., Lin, L., Wang, S., Zeng, K., Zou, R., Yang, Z., & Zhao, Y. (2024) · Journal of Ovarian Research · doi:10.1186/s13048-024-01361-z · Cited by 5
“The animal model of PCOS also confirmed that high androgen level caused polycystic ovarian morphologic features [7, 8].”
Background
Endocrine Disruptors, Epigenetic Changes, and Transgenerational Transmission
Rizzo, R., Bortolotti, D., Rizzo, S., & Schiuma, G. (2023) · Springer eBooks · doi:10.1007/978-3-031-36494-5_3 · Cited by 5
[LH-FSH ratio and Polycystic Ovary Syndrome: A forgotten test?].
de la Llata, E. S., Sánchez, M. R. M., Sarrió, A. R., & Io, C.-R. (2016) · PubMed · Cited by 5
Associations of Maternal Testosterone and Cortisol Levels With Health Outcomes of Mothers and Their Very-Low-Birthweight Infants
Cho, J., Su, X., & Holditch‐Davis, D. (2017) · Biological Research For Nursing · doi:10.1177/1099800417703704 · Cited by 5
Environmental contaminants, female reproductive health and fertility
Mendola, P., & Louis, G. M. B. (2010) · Cambridge University Press eBooks · doi:10.1017/cbo9780511674686.013 · Cited by 5

Authors: Abbott, D. H., Barnett, D. K., Bruns, C. M., & Dumesic, D. A.
Corresponding author: Abbott, D.H.
ORCID: Abbott, D.H.
Dumesic, D.A.
Venue: Human Reproduction Update
Publisher: Oxford University Press (OUP)
Published: 2005-07-01
Volume: 11
Issue: 4
Pages: 357-374
ISSN: 1355-4786 (ISSN-L)
1460-2369
DOI: 10.1093/humupd/dmi013
OpenAlex: W2123009569
Cited by: 555
References: 231
Citations by year: 2026: 9 · 2025: 17 · 2024: 24 · 2023: 27 · 2022: 27 · 2021: 21 · 2020: 27 · 2019: 37 · 2018: 23 · 2017: 30 · 2016: 34 · 2015: 28 · 2014: 32 · 2013: 31 · 2012: 23
FWCI: 4.24
Type: journal article
Language: en
Open access: closed
Locations: Human Reproduction Update (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5u01hd044650-05)
National Institute on Aging (T32AG000268)
National Center for Research Resources (R01RR013635, R21RR014093, P51RR000167)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (P50HD044405, U01-HD044650)
Topics: Health Sciences › Medicine › Reproductive Medicine › Ovarian function and disorders
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Sexual Differentiation and Disorders
Health Sciences › Medicine › Reproductive Medicine › Reproductive Biology and Fertility
Keywords: polycystic ovary syndrome, hyperandrogenism, fetal programming, developmental origins of health and disease, rhesus monkeys, prenatal androgen exposure, ovulatory dysfunction, insulin resistance, hyperlipidemia
MeSH terms: Androgens, Animals, Female, Genitalia, Female, Humans, Polycystic Ovary Syndrome, Hyperandrogenism

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

Androgen excess fetal programming of female reproduction: a developmental aetiology for polycystic ovary syndrome

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks