Hostname: page-component-745bb68f8f-mzp66 Total loading time: 0 Render date: 2025-01-18T19:46:29.588Z Has data issue: false hasContentIssue false
  • English
  • Français

The ovarian dysgenesis syndrome

Published online by Cambridge University Press:  07 January 2011

G. M. Buck Louis ,
M. A. Cooney  and
C. M. Peterson
G. M. Buck Louis*
Affiliation:
Division of Epidemiology, Statistics & Prevention Research, National Institute of Child Health & Human Development, Rockville, MD, USA
M. A. Cooney
Affiliation:
Division of Epidemiology, Statistics & Prevention Research, National Institute of Child Health & Human Development, Rockville, MD, USA
C. M. Peterson
Affiliation:
Division of Reproductive Endocrinology and Infertility, Department of Obstetrics and Gynecology, University of Utah Health Sciences Center, Salt Lake City, UT, USA
*
*Address for correspondence: G. M. Buck Louis, Division of Epidemiology, Statistics & Prevention Research, National Institute of Child Health & Human Development, 6100 Executive Blvd., Room 7B03, Rockville, MD 20852, USA. (Email [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

New thinking has arisen about the origin of adult onset diseases stemming from a collective body of evidence commonly referred to as the developmental origins of health and disease. This conceptual paradigm posits that certain adult onset diseases arise during critical or sensitive windows of human development or even transgenerationally. The testicular dysgenesis hypothesis (TDS) postulates an in utero origin for adverse male reproductive outcomes, and is an excellent example of the early origins of the paradigm. Despite similarities in the development of the male and female reproductive tracks, noticeably absent is a collective body of evidence focusing on the plausibility of an early origin for gynecologic outcomes and later onset of adult diseases. Using the TDS paradigm, we synthesized the available literature relative to the ovarian dysgenesis syndrome (ODS), which we define as alterations in ovarian structure or function that may manifest as fecundity impairments, gynecologic disorders, gravid diseases or later onset adult diseases. We evaluated environmental exposures, particularly the role of endocrine disrupting chemicals, in relation to these outcomes, and found evidence (although fragmented) consistent with an in utero origin of gynecologic outcomes, which in turn is associated with later onset of adult diseases. The findings are interpreted within the ODS paradigm while delineating methodological challenges and future research opportunities designed to answer critical data gaps regarding the origin of fecundity, gravid health and chronic diseases affecting the female population.

Keywords

early originsexposomeovarian dysgenesis
Type
Themed Content: Role of Environmental Stressors in the Developmental Origins of Disease
Information
Journal of Developmental Origins of Health and Disease , Volume 2 , Issue 1: Including Themed Content: Role of Environmental Stressors in the Developmental Origins of Disease , 23 February 2011 , pp. 25 - 35
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2011 This is the work of the U.S. Government and is not subject to copyright protection in the United States

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1.Barker, DJ. Mothers, Babies, and Disease Later in Life, 1984. BMJ Publishing Group, London.Google Scholar
2.Ben-Shlomo, Y, Kuh, D. A life course approach to chronic disease epidemiology: conceptual models, empirical challenges and interdisciplinary perspectives. Int J Epidemiol. 2002; 31, 285–293.CrossRefGoogle ScholarPubMed
3.Buck Louis, GM, Cooney, MA. Effects of environmental contaminants on ovarian function and fertility. In Novel Concepts in Ovarian Endocrinology (ed. Gonzalez-Bulnes A), 2007; pp. 249–268. Transworld Research Network, Kerala.Google Scholar
4.Gluckman, PD, Hanson, MA. Living with the past: evolution, development, and patterns of disease. Science. 2004; 305, 1733–1736.CrossRefGoogle ScholarPubMed
5.Heindel, JJ. Role of exposure to environmental chemicals in the developmental basis of reproductive disease and dysfunction. Semin Reprod Med. 2006; 24, 168–177.CrossRefGoogle ScholarPubMed
6.De Stavola, BL, Nitsch, D, dos, SSI, et al. Statistical issues in life course epidemiology. Am J Epidemiol. 2006; 163, 84–96.CrossRefGoogle ScholarPubMed
7.Carlin, BP, Louis, TA. Bayesian Methods for Data Analysis, 3rd edn, 2009. Chapman & Hall/CRC Press, Boca Raton, FL.Google Scholar
8.Lutz, W, O'Neill, BC, Scherbov, S. Demographics. Europe's population at a turning point. Science. 2003; 299, 1991–1992.CrossRefGoogle ScholarPubMed
9.Skakkebaek, NE, Rajpert-De, ME, Main, KM. Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects. Hum Reprod. 2001; 16, 972–978.CrossRefGoogle ScholarPubMed
10.Andersen, AG, Jensen, TK, Carlsen, E, et al. High frequency of sub-optimal semen quality in an unselected population of young men. Hum Reprod. 2000; 15, 366–372.CrossRefGoogle Scholar
11.Carlsen, E, Giwercman, A, Keiding, N, Skakkebaek, NE. Evidence for decreasing quality of semen during past 50 years. BMJ. 1992; 305, 609–613.CrossRefGoogle ScholarPubMed
12.Chilvers, C, Pike, MC, Forman, D, Fogelman, K, Wadsworth, ME. Apparent doubling of frequency of undescended testis in England and Wales in 1962–81. Lancet. 1984; 2, 330–332.CrossRefGoogle ScholarPubMed
13.Paulozzi, LJ, Erickson, JD, Jackson, RJ. Hypospadias trends in two US surveillance systems. Pediatrics. 1997; 100, 831–834.CrossRefGoogle ScholarPubMed
14.Moller, H. Trends in sex-ratio, testicular cancer and male reproductive hazards: are they connected? APMIS. 1998; 106, 232–238.CrossRefGoogle ScholarPubMed
15.Baker, JA, Buck, GM, Vena, JE, Moysich, KB. Fertility patterns prior to testicular cancer diagnosis. Cancer Causes Control. 2005; 16, 295–299.CrossRefGoogle ScholarPubMed
16.Prener, A, Engholm, G, Jensen, OM. Genital anomalies and risk for testicular cancer in Danish men. Epidemiology. 1996; 7, 14–19.CrossRefGoogle ScholarPubMed
17.Leon, DA, Lithell, HO, Vagero, D, et al. Reduced fetal growth rate and increased risk of death from ischaemic heart disease: cohort study of 15 000 Swedish men and women born 1915–29. BMJ. 1998; 317, 241–245.CrossRefGoogle Scholar
18.Lithell, HO, McKeigue, PM, Berglund, L, et al. Relation of size at birth to non-insulin dependent diabetes and insulin concentrations in men aged 50–60 years. BMJ. 1996; 312, 406–410.CrossRefGoogle ScholarPubMed
19.McCormack, VA, dos, SSI, De Stavola, BL, et al. Fetal growth and subsequent risk of breast cancer: results from long term follow up of Swedish cohort. BMJ. 2003; 326, 248.CrossRefGoogle ScholarPubMed
20.Barker, DJ. Fetal and Infant Origins of Adult Disease, 1992. BMJ Publication, London.Google Scholar
21.Wilson, VS, Blystone, CR, Hotchkiss, AK, Rider, CV, Gray, LE Jr. Diverse mechanisms of anti-androgen action: impact on male rat reproductive tract development. Int J Androl. 2008; 31, 178–187.CrossRefGoogle ScholarPubMed
22.Mendola, P, Buck Louis, GM. Environmental contaminants, female reproductive health and fertility. In Environmental Impacts on Reproductive Health and fertility (eds. Woodruff TJ, Janssen SJ, Guilette LJ, Giudice LC), 2010; pp. 161–172. Cambridge University Press, Cambridge.Google Scholar
23.Wood, J. Dynamics of Human Reproduction: Biology, Biometry, and Demography, 1994. Aldine de Gruyter, New York.Google Scholar
24.Chapin, RE, Robbins, WA, Schieve, LA, et al. Off to a good start: the influence of pre- and periconceptional exposures, parental fertility, and nutrition on children's health. Environ Health Perspect. 2004; 112, 69–78.CrossRefGoogle ScholarPubMed
25.Calabrese, EJ. Sex differences in susceptibility to toxic industrial chemicals. Br J Ind Med. 1986; 43, 577–579.Google ScholarPubMed
26.Kuh, D, Ben-Shlomo, Y. A Lifecourse Approach to Chronic Disease Epidemiology, 2005. Oxford University Press, Inc., New York.Google Scholar
27.Lucifero, D, Chaillet, JR, Trasler, JM. Potential significance of genomic imprinting defects for reproduction and assisted reproductive technologies. Hum Reprod Update. 2004; 10, 3–18.CrossRefGoogle Scholar
28.Latham, KE. Epigenetic modification and imprinting of the mammalian genome during development. Curr Top Dev Biol. 1999; 43, 1–49.Google ScholarPubMed
29.Obata, Y, Kaneko-Ishino, T, Koide, T, et al. Disruption of primary imprinting during oocyte growth leads to the modified expression of imprinted genes during embryogenesis. Development. 1998; 125, 1553–1560.CrossRefGoogle Scholar
30.Owen, CM, Segars, JH. Imprinting disorders and assisted reproductive technology. Semin Reprod Med. 2009; 27, 417–428.CrossRefGoogle ScholarPubMed
31.Dorais, J, Peterson, CM. Mullerian (Paramesonephric) Anomalies and associated Wolffian (Mesonephric) Duct malformations. In Reproductive Endocrinology and Infertility Integrating Modern Clinical and Laboratory Practice (eds. Carrell DT, Peterson CM), 2010; pp. 265–280. Springer, Philadelphia, PA.CrossRefGoogle Scholar
32.Witschi, E. Migration of the germ cells of human embryos from the yolk sac to the primitive gonadal folds. Contrib Embryol. 1948, 67–80.Google Scholar
33.Acien, P, Acien, M, Sanchez-Ferrer, M. Complex malformations of the female genital tract. New types and revision of classification. Hum Reprod. 2004; 19, 2377–2384.CrossRefGoogle ScholarPubMed
34.Hammoud, AO, Gibson, M, Peterson, CM, et al. Quantification of the familial contribution to mullerian anomalies. Obstet Gynecol. 2008; 111(Pt 1), 378–384.CrossRefGoogle ScholarPubMed
35.Gondos, B, Westergaard, L, Byskov, AG. Initiation of oogenesis in the human fetal ovary: ultrastructural and squash preparation study. Am J Obstet Gynecol. 1986; 155, 189–195.CrossRefGoogle ScholarPubMed
36.Van, SL. From epigenesis to epigenetics: the case of C. H. Waddington. Ann N Y Acad Sci. 2002; 981, 61–81.Google Scholar
37.Peterson, CM, Carrell, DT, Varner, M, et al. The environment and reproduction: endocrine disruption, reproductive impairment, and epigenetics. In Reproductive Endocrinology and Infertility Integrating Modern Clinical and Laboratory Practice (eds. Carrell DT, Peterson CM), 2010; pp. 781–803. Springer, Philadelphia, PA.CrossRefGoogle Scholar
38.Hennig, B, Meerarani, P, Slim, R, et al. Proinflammatory properties of coplanar PCBs: in vitro and in vivo evidence. Toxicol Appl Pharmacol. 2002; 181, 174–183.CrossRefGoogle ScholarPubMed
39.Ivnitski-Steele, ID, Sanchez, A, Walker, MK. 2,3,7,8-tetrachlorodibenzo-p-dioxin reduces myocardial hypoxia and vascular endothelial growth factor expression during chick embryo development. Birth Defects Res A Clin Mol Teratol. 2004; 70, 51–58.CrossRefGoogle ScholarPubMed
40.Long, X, Burke, KA, Bigsby, RM, Nephew, KP. Effects of the xenoestrogen bisphenol A on expression of vascular endothelial growth factor (VEGF) in the rat. Exp Biol Med (Maywood). 2001; 226, 477–483.CrossRefGoogle ScholarPubMed
41.Bredhult, C, Backlin, BM, Olovsson, M. Effects of some endocrine disruptors on the proliferation and viability of human endometrial endothelial cells in vitro. Reprod Toxicol. 2007; 23, 550–559.CrossRefGoogle ScholarPubMed
42.Muhlhauser, A, Susiarjo, M, Rubio, C, et al. Bisphenol A effects on the growing mouse oocyte are influenced by diet. Biol Reprod. 2009; 80, 1066–1071.CrossRefGoogle ScholarPubMed
43.Jirtle, RL, Skinner, MK. Environmental epigenomics and disease susceptibility. Nat Rev Genet. 2007; 8, 253–262.CrossRefGoogle ScholarPubMed
44.Newbold, RR, Hanson, RB, Jefferson, WN, et al. Increased tumors but uncompromised fertility in the female descendants of mice exposed developmentally to diethylstilbestrol. Carcinogenesis. 1998; 19, 1655–1663.CrossRefGoogle ScholarPubMed
45.Skinner, MK. Endocrine disruptors and epigenetic transgenerational disease etiology. Pediatr Res. 2007; 61(Pt 2), 48R–50R.CrossRefGoogle ScholarPubMed
46.Steinberg, RM, Walker, DM, Juenger, TE, Woller, MJ, Gore, AC. Effects of perinatal polychlorinated biphenyls on adult female rat reproduction: development, reproductive physiology, and second generational effects. Biol Reprod. 2008; 78, 1091–1101.CrossRefGoogle ScholarPubMed
47.Walker, BE, Haven, MI. Intensity of multigenerational carcinogenesis from diethylstilbestrol in mice. Carcinogenesis. 1997; 18, 791–793.CrossRefGoogle ScholarPubMed
48.Buck Louis, GM, Lynch, CD, Cooney, MA. Environmental influences on female fecundity and fertility. Semin Reprod Med. 2006; 24, 147–155.CrossRefGoogle ScholarPubMed
49.McLachlan, JA, Simpson, E, Martin, M. Endocrine disrupters and female reproductive health. Best Pract Res Clin Endocrinol Metab. 2006; 20, 63–75.CrossRefGoogle ScholarPubMed
50.Mendola, P, Messer, LC, Rappazzo, K. Science linking environmental contaminant exposures with fertility and reproductive health impacts in the adult female. Fertil Steril. 2008; 89(Suppl 2), e81–e94.CrossRefGoogle ScholarPubMed
51.Miller, KP, Borgeest, C, Greenfeld, C, Tomic, D, Flaws, JA. In utero effects of chemicals on reproductive tissues in females. Toxicol Appl Pharmacol. 2004; 198, 111–131.CrossRefGoogle ScholarPubMed
52.Toft, G, Hagmar, L, Giwercman, A, Bonde, JP. Epidemiological evidence on reproductive effects of persistent organochlorines in humans. Reprod Toxicol. 2004; 19, 5–26.CrossRefGoogle ScholarPubMed
53.Nichols, HB, Trentham-Dietz, A, Hampton, JM, et al. From menarche to menopause: trends among US women born from 1912–1969. Am J Epidemiol. 2006; 164, 1003–1011.CrossRefGoogle Scholar
54.Karpati, AM, Rubin, CH, Kieszak, SM, Marcus, M, Troiano, RP. Stature and pubertal stage assessment in American boys: The 1988–1994 Third National Health and Nutrition Examination Survey. J Adoles Health. 2002; 30, 205–212.CrossRefGoogle ScholarPubMed
55.Herman-Giddens, ME, Slora, EJ, Wasserman, RC, et al. Secondary sexual characteristics and menses in young girls seen in office practice: a study from the Pediatric Research Office Settings network. Pediatr. 1997; 99, 505–512.CrossRefGoogle Scholar
56.North American Menopause Society. Menopause Core Curriculum Study Guide, 2002. North American Menopause Society, Cleveland, OH.Google Scholar
57.de Bruin, JP, Dorland, M, Bruinse, HW, et al. Fetal growth retardation as a cause of impaired ovarian development. Early Hum Dev. 1998; 51, 39–46.CrossRefGoogle ScholarPubMed
58.Ibanez, L, Potau, N, Enriquez, G, de, ZF. Reduced uterine and ovarian size in adolescent girls born small for gestational age. Pediatr Res. 2000; 47, 575–577.CrossRefGoogle ScholarPubMed
59.Ibanez, L, Potau, N, Ferrer, A, et al. Reduced ovulation rate in adolescent girls born small for gestational age. J Clin Endocrinol Metab. 2002; 87, 3391–3393.CrossRefGoogle ScholarPubMed
60.Jensen, TK, Joffe, M, Scheike, T, et al. Early exposure to smoking and future fecundity among Danish twins. Int J Androl. 2006; 29, 603–613.CrossRefGoogle ScholarPubMed
61.Taylor, KC, Jackson, LW, Lynch, CD, Kostyniak, PJ, Buck Louis, GM. Preconception maternal polychlorinated biphenyl concentrations and the secondary sex ratio. Environ Res. 2007; 103, 99–105.CrossRefGoogle ScholarPubMed
62.Weisskopf, MG, Anderson, HA, Hanrahan, LP. Decreased sex ratio following maternal exposure to polychlorinated biphenyls from contaminated Great Lakes sport-caught fish: a retrospective cohort study. Environ Health. 2003; 2, 2.CrossRefGoogle ScholarPubMed
63.del Rio Go, mez IMarshall, T, Tsai, P, Shao, YS, Guo, YL. Number of boys born to men exposed to polychlorinated byphenyls. Lancet. 2002; 360, 143–144.Google Scholar
64.Mocarelli, P, Gerthoux, PM, Ferrari, E, et al. Paternal concentrations of dioxin and sex ratio of offspring. Lancet. 2000; 355, 1858–1863.CrossRefGoogle ScholarPubMed
65.Buck Louis, GM, Dmochowski, J, Lynch, C, et al. Polychlorinated biphenyl serum concentrations, lifestyle and time-to-pregnancy. Hum Reprod. 2009; 24, 451–458.CrossRefGoogle ScholarPubMed
66.Law, DC, Klebanoff, MA, Brock, JW, Dunson, DB, Longnecker, MP. Maternal serum levels of polychlorinated biphenyls and 1,1-dichloro-2,2-bis(p-chlorophenyl)ethylene (DDE) and time to pregnancy. Am J Epidemiol. 2005; 162, 523–532.CrossRefGoogle Scholar
67.Eskenazi, B, Warner, M, Marks, AR, et al. Serum dioxin concentrations and time to pregnancy. Epidemiology. 2010; 21, 224–231.CrossRefGoogle ScholarPubMed
68.Harley, KG, Marks, AR, Chevrier, J, et al. PBDE concentrations in women's serum and fecundability. Environ Health Perspect. 2010; 118, 699–704.CrossRefGoogle ScholarPubMed
69.Cole, DC, Wainman, B, Sanin, LH, et al. Environmental contaminant levels and fecundability among non-smoking couples. Reprod Toxicol. 2006; 22, 13–19.CrossRefGoogle ScholarPubMed
70.Stephen, EH, Chandra, A. Updated projections of infertility in the United States: 1995–2025. Fertil Steril. 1998; 70, 30–34.CrossRefGoogle ScholarPubMed
71.Stephen, EH, Chandra, A. Declining estimates of infertility in the United States: 1982–2002. Fertil Steril. 2006; 86, 516–523.CrossRefGoogle ScholarPubMed
72.Daguet, F. Un Siecle de Fecondite Francaise: 1901–1999, 2010. INSEE, Paris.Google Scholar
73.Leridon, H. Can assisted reproduction technology compensate for the natural decline in fertility with age? A model assessment. Hum Reprod. 2004; 19, 1548–1553.CrossRefGoogle ScholarPubMed
74.Menken, J, Trussell, J, Larsen, U. Age and infertility. Science. 1986; 233, 1389–1394.CrossRefGoogle ScholarPubMed
75.Olsen, J, Rachootin, P. Invited commentary: monitoring fecundity over time – if we do it, then let's do it right. Am J Epidemiol. 2003; 157, 94–97.CrossRefGoogle Scholar
76.Joffe, M. Invited commentary: the potential for monitoring of fecundity and the remaining challenges. Am J Epidemiol. 2003; 157, 89–93.CrossRefGoogle ScholarPubMed
77.Herbst, AL, Bern, HA. Developmental Effects of Diethylstilbestrol (DES) in Pregnancy, 1981. Thieme-Stratton, New York.Google Scholar
78.Kaufman, RH, Adam, E, Binder, GL, Gerthoffer, E. Upper genital tract changes and pregnancy outcome in offspring exposed in utero to diethylstilbestrol. Am J Obstet Gynecol. 1980; 137, 299–308.CrossRefGoogle ScholarPubMed
79.Saravelos, SH, Cocksedge, KA, Li, TC. Prevalence and diagnosis of congenital uterine anomalies in women with reproductive failure: a critical appraisal. Hum Reprod Update. 2008; 14, 415–429.CrossRefGoogle ScholarPubMed
80.Dorland, . Dorland's Medical Dictionary and Illustrations, 31st edn, 2007. W.B. Saunders, Philadelphia, PA.Google Scholar
81.Buttram, VC Jr, Reiter, RC. Uterine leiomyomata: etiology, symptomatology, and management. Fertil Steril. 1981; 36, 433–445.Google ScholarPubMed
82.Stewart, EA. Uterine fibroids. Lancet. 2001; 357, 293–298.CrossRefGoogle ScholarPubMed
83.Wallach, EE, Vlahos, NF. Uterine myomas: an overview of development, clinical features, and management. Obstet Gynecol. 2004; 104, 393–406.CrossRefGoogle ScholarPubMed
84.Viswanathan, M, Hartmann, K, McKoy, N, et al. Management of uterine fibroids: an update of the evidence. Evid Rep Technol Assess (Full Rep). 2007, 1–122.Google ScholarPubMed
85.Baird, DD, Dunson, DB, Hill, MC, Cousins, D, Schectman, JM. High cumulative incidence of uterine leiomyoma in black and white women: ultrasound evidence. Am J Obstet Gynecol. 2003; 188, 100–107.CrossRefGoogle ScholarPubMed
86.Ishikawa, H, Reierstad, S, Demura, M, et al. High aromatase expression in uterine leiomyoma tissues of African-American women. J Clin Endocrinol Metab. 2009; 94, 1752–1756.CrossRefGoogle ScholarPubMed
87.Klatsky, PC, Tran, ND, Caughey, AB, Fujimoto, VY. Fibroids and reproductive outcomes: a systematic literature review from conception to delivery. Am J Obstet Gynecol. 2008; 198, 357–366.CrossRefGoogle ScholarPubMed
88.Newbold, RR, Moore, AB, Dixon, D. Characterization of uterine leiomyomas in CD-1 mice following developmental exposure to diethylstilbestrol (DES). Toxicol Pathol. 2002; 30, 611–616.CrossRefGoogle ScholarPubMed
89.Baird, DD, Newbold, R. Prenatal diethylstilbestrol (DES) exposure is associated with uterine leiomyoma development. Reprod Toxicol. 2005; 20, 81–84.CrossRefGoogle ScholarPubMed
90.D'Aloisio, AA, Baird, DD, Deroo, LA, Sandler, DP. Association of intrauterine and early-life exposures with diagnosis of uterine leiomyomata by 35 years of age in the sister study. Environ Health Perspect. 2010; 118, 375–381.CrossRefGoogle ScholarPubMed
91.Wise, LA, Palmer, JR, Rowlings, K, et al. Risk of benign gynecologic tumors in relation to prenatal diethylstilbestrol exposure. Obstet Gynecol. 2005; 105, 167–173.CrossRefGoogle ScholarPubMed
92.Azziz, R, Woods, KS, Reyna, R, et al. The prevalence and features of the polycystic ovary syndrome in an unselected population. J Clin Endocrinol Metab. 2004; 89, 2745–2749.CrossRefGoogle Scholar
93.Goodarzi, MO, Quinones, MJ, Azziz, R, et al. Polycystic ovary syndrome in Mexican-Americans: prevalence and association with the severity of insulin resistance. Fertil Steril. 2005; 84, 766–769.CrossRefGoogle ScholarPubMed
94.The Rotterdam ESHRE/ASRM-sponsored PCOS Consensus Working Group. Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome (PCOS). Hum Reprod. 2004; 19, 41–47.CrossRefGoogle Scholar
95.Kumarapeli, V, Seneviratne, RA, Wijeyaratne, CN, Yapa, RM, Dodampahala, SH. A simple screening approach for assessing community prevalence and phenotype of polycystic ovary syndrome in a semi-urban population in Sri Lanka. Am J Epidemiol. 2008; 168, 321–328.CrossRefGoogle Scholar
96.Cresswell, JL, Barker, DJ, Osmond, C, et al. Fetal growth, length of gestation, and polycystic ovaries in adult life. Lancet. 1997; 350, 1131–1135.CrossRefGoogle ScholarPubMed
97.Wickenheisser, JK, Nelson-DeGrave, VL, McAllister, JM. Human ovarian theca cells in culture. Trends Endocrinol Metab. 2006; 17, 65–71.CrossRefGoogle ScholarPubMed
98.Abbott, DH, Barnett, DK, Bruns, CM, Dumesic, DA. Androgen excess fetal programming of female reproduction: a developmental aetiology for polycystic ovary syndrome? Hum Reprod Update. 2005; 11, 357–374.CrossRefGoogle ScholarPubMed
99.Takeuchi, T, Tsutsumi, O, Ikezuki, Y, Takai, Y, Taketani, Y. Positive relationship between androgen and the endocrine disruptor, bisphenol A, in normal women and women with ovarian dysfunction. Endocr J. 2004; 51, 165–169.CrossRefGoogle ScholarPubMed
100.Tsutsumi, O. Assessment of human contamination of estrogenic endocrine-disrupting chemicals and their risk for human reproduction. J Steroid Biochem Mol Biol. 2005; 93, 325–330.CrossRefGoogle ScholarPubMed
101.Abbott, DH, Dumesic, DA, Franks, S. Developmental origin of polycystic ovary syndrome – a hypothesis. J Endocrinol. 2002; 174, 1–5.CrossRefGoogle ScholarPubMed
102.Eisner, JR, Barnett, MA, Dumesic, DA, Abbott, DH. Ovarian hyperandrogenism in adult female rhesus monkeys exposed to prenatal androgen excess. Fertil Steril. 2002; 77, 167–172.CrossRefGoogle ScholarPubMed
103.Leibson, CL, Good, AE, Hass, SL, et al. Incidence and characterization of diagnosed endometriosis in a geographically defined population. Fertil Steril. 2004; 82, 314–321.CrossRefGoogle Scholar
104.Houston, DE. Evidence for the risk of pelvic endometriosis by age, race and socioeconomic status. Epidemiol Rev. 1984; 6, 167–191.CrossRefGoogle ScholarPubMed
105.Olive, DL, Schwartz, LB. Endometriosis. N Engl J Med. 1993; 328, 1759–1769.CrossRefGoogle ScholarPubMed
106.Carter, JE. Combined hysteroscopic and laparoscopic findings in patients with chronic pelvic pain. J Am Assoc Gynecol Laparosc. 1994; 2, 43–47.CrossRefGoogle ScholarPubMed
107.Mahmood, TA, Templeton, A. Prevalence and genesis of endometriosis. Hum Reprod. 1991; 6, 544–549.CrossRefGoogle ScholarPubMed
108.Moen, MH, Muus, KM. Endometriosis in pregnant and non-pregnant women at tubal sterilization. Hum Reprod. 1991; 6, 699–702.CrossRefGoogle ScholarPubMed
109.Strathy, JH, Molgaard, CA, Coulam, CB, Melton, LJ III. Endometriosis and infertility: a laparoscopic study of endometriosis among fertile and infertile women. Fertil Steril. 1982; 38, 667–672.CrossRefGoogle ScholarPubMed
110.Wardle, PG, Hull, MG. Is endometriosis a disease? Baillieres Clin Obstet Gynaecol. 1993; 7, 673–685.CrossRefGoogle ScholarPubMed
111.Rier, SE, Martin, DC, Bowman, RE, Dmowski, WP, Becker, JL. Endometriosis in rhesus monkeys (Macaca mulatta) following chronic exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Fundam Appl Toxicol. 1993; 21, 433–441.CrossRefGoogle Scholar
112.Rier, SE, Turner, WE, Martin, DC, et al. Serum levels of TCDD and dioxin-like chemicals in Rhesus monkeys chronically exposed to dioxin: correlation of increased serum PCB levels with endometriosis. Toxicol Sci. 2001; 59, 147–159.CrossRefGoogle ScholarPubMed
113.Heilier, JF, Nackers, F, Verougstraete, V, et al. Increased dioxin-like compounds in the serum of women with peritoneal endometriosis and deep endometriotic (adenomyotic) nodules. Fertil Steril. 2005; 84, 305–312.CrossRefGoogle ScholarPubMed
114.Mayani, A, Barel, S, Soback, S, Almagor, M. Dioxin concentrations in women with endometriosis. Hum Reprod. 1997; 12, 373–375.CrossRefGoogle ScholarPubMed
115.Jackson, LW, Zullo, MD, Goldberg, JM. The association between heavy metals, endometriosis and uterine myomas among premenopausal women: National Health and Nutrition Examination Survey 1999–2002. Hum Reprod. 2008; 23, 679–687.CrossRefGoogle ScholarPubMed
116.Cobellis, L, Latini, G, De, FC, et al. High plasma concentrations of di-(2-ethylhexyl)-phthalate in women with endometriosis. Hum Reprod. 2003; 18, 1512–1515.CrossRefGoogle ScholarPubMed
117.Reddy, BS, Rozati, R, Reddy, S, et al. High plasma concentrations of polychlorinated biphenyls and phthalate esters in women with endometriosis: a prospective case control study. Fertil Steril. 2006; 85, 775–779.CrossRefGoogle ScholarPubMed
118.Gerhard, I, Runnebaum, B. The limits of hormone substitution in pollutant exposure and fertility disorders. Zentralbl Gynakol. 1992; 114, 593–602.Google ScholarPubMed
119.Louis, GM, Weiner, JM, Whitcomb, BW, et al. Environmental PCB exposure and risk of endometriosis. Hum Reprod. 2005; 20, 279–285.CrossRefGoogle ScholarPubMed
120.Porpora, MG, Ingelido, AM, di, DA, et al. Increased levels of polychlorobiphenyls in Italian women with endometriosis. Chemosphere. 2006; 63, 1361–1367.CrossRefGoogle ScholarPubMed
121.Quaranta, MG, Porpora, MG, Mattioli, B, et al. Impaired NK-cell-mediated cytotoxic activity and cytokine production in patients with endometriosis: a possible role for PCBs and DDE. Life Sci. 2006; 79, 491–498.CrossRefGoogle ScholarPubMed
122.Richardson, DB, Ciampi, A. Effects of exposure measurement error when an exposure variable is constrained by a lower limit. Am J Epidemiol. 2003; 157, 355–363.CrossRefGoogle ScholarPubMed
123.Schisterman, EF, Whitcomb, BW, Louis, GM, Louis, TA. Lipid adjustment in the analysis of environmental contaminants and human health risks. Environ Health Perspect. 2005; 113, 853–857.CrossRefGoogle ScholarPubMed
124.Schisterman, EF, Vexler, A, Whitcomb, BW, Liu, A. The limitations due to exposure detection limits for regression models. Am J Epidemiol. 2006; 163, 374–383.CrossRefGoogle ScholarPubMed
125.Missmer, SA, Hankinson, SE, Spiegelman, D, et al. In utero exposures and the incidence of endometriosis. Fertil Steril. 2004; 82, 1501–1508.CrossRefGoogle ScholarPubMed
126.Hediger, ML, Hartnett, HJ, Louis, GM. Association of endometriosis with body size and figure. Fertil Steril. 2005; 84, 1366–1374.CrossRefGoogle ScholarPubMed
127.Vitonis, AF, Baer, HJ, Hankinson, SE, Laufer, MR, Missmer, SA. A prospective study of body size during childhood and early adulthood and the incidence of endometriosis. Hum Reprod. 2010; 25, 1325–1334.CrossRefGoogle ScholarPubMed
128.Buck Louis, GM, Hediger, ML, Pena, JB. Intrauterine exposures and risk of endometriosis. Hum Reprod. 2007; 22, 3232–3236.CrossRefGoogle ScholarPubMed
129.Colditz, GA, Sellers, TA, Trapido, E. Epidemiology – identifying the causes and preventability of cancer? Nat Rev Cancer. 2006; 6, 75–83.CrossRefGoogle ScholarPubMed
130.Garcia, M, Jemal, A, Ward, EM, et al. Global Cancer Facts and Figures 2007, 2007. American Cancer Society, Atlanta, GA.Google Scholar
131. Fast Stats: An interactive tool for access to SEER cancer statistics. Surveillance Reserach Program, National Cancer Institute. Retrieved 20 December 2010 from http://seer.cancer.gov/faststats.Google Scholar
132.Cossu, A, Budroni, M, Capobianco, G, et al. Epidemiological aspects of ovarian malignancies in North Sardinia in the period 1992–2001. Eur J Gynaecol Oncol. 2005; 26, 47–50.Google ScholarPubMed
133.Mok, SC, Kwong, J, Welch, WR, et al. Etiology and pathogenesis of epithelial ovarian cancer. Dis Markers. 2007; 23, 367–376.CrossRefGoogle ScholarPubMed
134.Grammatikakis, I, Zervoudis, S, Evangelinakis, N, Tziortzioti, V. Endometrium and ovarian cancer synchronous to endometriosis – a retrospective study of our experience of 7 years. J Med Life. 2010; 3, 76–79.Google Scholar
135.Ahlborg, UG, Lipworth, L, Titus-Ernstoff, L, et al. Organochlorine compounds in relation to breast cancer, endometrial cancer, and endometriosis: an assessment of the biological and epidemiological evidence. Crit Rev Toxicol. 1995; 25, 463–531.CrossRefGoogle ScholarPubMed
136.Sturgeon, SR, Brock, JW, Potischman, N, et al. Serum concentrations of organochlorine compounds and endometrial cancer risk (United States). Cancer Causes Control. 1998; 9, 417–424.CrossRefGoogle ScholarPubMed
137.Weiderpass, E, Adami, HO, Baron, JA, et al. Organochlorines and endometrial cancer risk. Cancer Epidemiol Biomarkers Prev. 2000; 9, 487–493.Google ScholarPubMed
138.Crain, DA, Janssen, SJ, Edwards, TM, et al. Female reproductive disorders: the roles of endocrine-disrupting compounds and developmental timing. Fertil Steril. 2008; 90, 911–940.CrossRefGoogle ScholarPubMed
139.Palmer, JR, Wise, LA, Hatch, EE, et al. Prenatal diethylstilbestrol exposure and risk of breast cancer. Cancer Epidemiol Biomarkers Prev. 2006; 15, 1509–1514.CrossRefGoogle ScholarPubMed
140.Xue, F, Michels, KB. Intrauterine factors and risk of breast cancer: a systematic review and meta-analysis of current evidence. Lancet Oncol. 2007; 8, 1088–1100.CrossRefGoogle ScholarPubMed
141.Strohsnitter, WC, Noller, KL, Titus-Ernstoff, L, et al. Breast cancer incidence in women prenatally exposed to maternal cigarette smoke. Epidemiology. 2005; 16, 342–345.CrossRefGoogle ScholarPubMed
142.Somigliana, E, Vercellini, P, Daguati, R, et al. Fibroids and female reproduction: a critical analysis of the evidence. Hum Reprod Update. 2007; 13, 465–476.CrossRefGoogle ScholarPubMed
143.Boomsma, CM, Eijkemans, MJ, Hughes, EG, et al. A meta-analysis of pregnancy outcomes in women with polycystic ovary syndrome. Hum Reprod Update. 2006; 12, 673–683.CrossRefGoogle ScholarPubMed
144.Brosens, IA, De, SP, Hamerlynck, T, et al. Endometriosis is associated with a decreased risk of pre-eclampsia. Hum Reprod. 2007; 22, 1725–1729.CrossRefGoogle ScholarPubMed
145.Sinaii, N, Cleary, SD, Ballweg, ML, Nieman, LK, Stratton, P. High rates of autoimmune and endocrine disorders, fibromyalgia, chronic fatigue syndrome and atopic diseases among women with endometriosis: a survey analysis. Hum Reprod. 2002; 17, 2715–2724.CrossRefGoogle ScholarPubMed
146.Kobayashi, H, Sumimoto, K, Moniwa, N, et al. Risk of developing ovarian cancer among women with ovarian endometrioma: a cohort study in Shizuoka, Japan. Int J Gynecol Cancer. 2007; 17, 37–43.CrossRefGoogle ScholarPubMed
147Brinton, LA, Gridley, G, Persson, I, Baron, J, Bergqvist, A. Cancer risk after a hospital discharge diagnosis of endometriosis. Am J Obstet Gynecol. 1997; 176, 572–579.CrossRefGoogle ScholarPubMed
148.Ogawa, S, Kaku, T, Amada, S, et al. Ovarian endometriosis associated with ovarian carcinoma: a clinicopathological and immunohistochemical study. Gynecol Oncol. 2000; 77, 298–304.CrossRefGoogle ScholarPubMed
149.Yoshikawa, H, Jimbo, H, Okada, S, et al. Prevalence of endometriosis in ovarian cancer. Gynecol Obstet Invest. 2000; 50(Suppl 1), 11–17.CrossRefGoogle ScholarPubMed
150.Wild, CP. Complementing the genome with an ‘exposome’: the outstanding challenge of environmental exposure measurement in molecular epidemiology. Cancer Epidemiol Biomarkers Prev. 2005; 14, 1847–1850.CrossRefGoogle ScholarPubMed