Female reproductive disorders, diseases, and costs of exposure to endocrine disrupting chemicals in the European Union

Journal of Clinical Endocrinology and Metabolism

Volumn 101, Issue 4, 2016, Pages 1562-1570

  Hunt, Patricia A ^a   Sathyanarayana, Sheela ^b,c   Fowler, Paul A ^d   Trasande, Leonardo ^e,f,g,h  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF ABERDEEN   (United Kingdom)

^e NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f NEW YORK UNIVERSITY   (United States)

^g NEW YORK UNIVERSITY   (United States)

^h NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIPHENYLDICHLOROETHENE; ENDOCRINE DISRUPTOR; PHTHALIC ACID; UNCLASSIFIED DRUG; POLLUTANT;

ADOLESCENT; ADULT; ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; ENDOMETRIOSIS; EUROPEAN UNION; FEMALE; GYNECOLOGIC DISEASE; HEALTH CARE COST; HUMAN; MAJOR CLINICAL STUDY; MATERNAL EXPOSURE; PUBLIC HEALTH; UTERUS MYOMA; ADVERSE EFFECTS; CHEMICALLY INDUCED; COST OF ILLNESS; ECONOMICS; ENVIRONMENTAL EXPOSURE; POLLUTANT; YOUNG ADULT;

ADULT; COST OF ILLNESS; ENDOCRINE DISRUPTORS; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL POLLUTANTS; EUROPEAN UNION; FEMALE; GENITAL DISEASES, FEMALE; HUMANS; YOUNG ADULT;

EID: 85011275778     PISSN: 0021972X     EISSN: 19457197     Source Type: Journal    
DOI: 10.1210/jc.2015-2873     Document Type: Article

References (90)

1. Buck Louis G, Cooney M. Effects of environmental contaminants on ovarian function and fertility. In:Gonzalez-Bulnes A, ed. Novel Concepts in Ovarian Endocrinology. Kerala, India: Transworld Research Network; 2007.
2. Buck Louis G, Cooney MA, Peterson CM. Ovarian dysgenesis syndrome. J Dev Orig Health Dis. 2011;2:25-35.
3. Skakkebaek NE, Rajpert-De Meyts E, Main KM. Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects. Hum Reprod. 2001;16:972-978.
4. Herbst AL, Green TH Jr, Ulfelder H. Primary carcinoma of the vagina. An analysis of 68 cases. Am J Obstet Gynecol. 1970;106:210-218.
5. Herbst AL, Scully RE. Adenocarcinoma of the vagina in adolescence. A report of 7 cases including 6 clear-cell carcinomas (so-called mesonephromas). Cancer. 1970;25:745-757.
6. Hatch EE, Troisi R, Wise LA, Titus-Ernstoff L, et al. Preterm birth, fetal growth, and age at menarche among women exposed prenatally to diethylstilbestrol (DES). Reprod Toxicol. 2011;31:151-157.
7. Hoover RN, Hyer M, Pfeiffer RM, et al. Adverse health outcomes in women exposed in utero to diethylstilbestrol. N Engl J Med. 2011;365:1304-1314.
8. Palmer JR, Herbst AL, Noller KL, et al. Urogenital abnormalities in men exposed to diethylstilbestrol in utero: a cohort study. Environ Health. 2009;8:37.
9. Troisi R, Hyer M, Hatch EE, et al. Medical conditions among adult offspring prenatally exposed to diethylstilbestrol. Epidemiology. 2013;24:430-438.
10. Mitchell RT, Sharpe RM, Anderson RA, et al. Diethylstilboestrol exposure does not reduce testosterone production in human fetal testis xenografts. PLoS One. 2013;8:e61726.
11. D'Aloisio AA, Baird DD, DeRoo LA, Sandler DP. Early-life exposures and early-onset uterine leiomyomata in black women in the Sister Study. Environ Health Perspect. 2012;120:406-412.
12. Mahalingaiah S, Hart JE, Wise LA, Terry KL, Boynton-Jarrett R, Missmer SA. Prenatal diethylstilbestrol exposure and risk of uterine leiomyomata in the Nurses' Health Study II. Am J Epidemiol. 2014;179:186-191.
13. Baird DD, Newbold R. Prenatal diethylstilbestrol (DES) exposure is associated with uterine leiomyoma development. Reprod Toxicol. 2005;20:81-84.
14. 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.
15. Greathouse KL, Cook JD, Lin K, et al. Identification of uterine leiomyoma genes developmentally reprogrammed by neonatal exposure to diethylstilbestrol. Reprod Sci. 2008;15:765-778.
16. Fowler PA, Childs AJ, Courant F, et al. In utero exposure to cigarette smoke dysregulates human fetal ovarian developmental signalling. Hum Reprod. 2014;29:1471-1489.
17. Tobias DK, Gaskins AJ, Missmer SA, et al. History of infertility and risk of type 2 diabetes mellitus: a prospective cohort study. Diabetologia. 2015;58:707-715.
18. Barry JA, Azizia MM, Hardiman PJ. Risk of endometrial, ovarian and breast cancer in women with polycystic ovary syndrome: a systematic review and meta-analysis. Hum Reprod Update. 2014;20:748-758.
19. de Wilde MA, Veltman-Verhulst SM, Goverde AJ, et al. Preconception predictors of gestational diabetes: a multicentre prospective cohort study on the predominant complication of pregnancy in polycystic ovary syndrome. Hum Reprod. 2014;29:1327-1336.
20. Fauser BC, Tarlatzis BC, Rebar RW, et al. Consensus on women's health aspects of polycystic ovary syndrome (PCOS): the Amsterdam ESHRE/ASRM-Sponsored 3rd PCOS Consensus Workshop Group. Fertil Steril. 2012;97:28-38.e25.
21. Joham AE, Boyle JA, Zoungas S, Teede HJ. Hypertension in reproductive-aged women with polycystic ovary syndrome and association with obesity. Am J Hypertens. 2015;28:847-851.
22. Kim JJ, Hwang KR, Choi YM, et al. Complete phenotypic and metabolic profiles of a large consecutive cohort of untreated Korean women with polycystic ovary syndrome. Fertil Steril. 2014;101:1424-1430.
23. Verit FF, Yucel O. Endometriosis, leiomyoma and adenomyosis: the risk of gynecologic malignancy. Asian Pac J Cancer Prev. 2013;14:5589-5597.
24. 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.
25. Jensen A, Sharif H, Kjaer SK. Use of fertility drugs and risk of uterine cancer: results from a large Danish population-based cohort study. Am J Epidemiol. 2009;170:1408-1414.
26. Peretz J, Vrooman L, Ricke WA, et al. Bisphenol a and reproductive health: update of experimental and human evidence, 2007-2013. Environ Health Perspect. 2014;122:775-786.
27. Ehrlich S, Williams PL, Hauser R, et al. Urinary bisphenol A concentrations and cytochrome P450 19 A1 (Cyp19) gene expression in ovarian granulosa cells: an in vivo human study. Reprod Toxicol. 2013;42:18-23.
28. Marino JL, Eskenazi B, Warner M, et al. Uterine leiomyoma and menstrual cycle characteristics in a population-based cohort study. Hum Reprod. 2004;19:2350-2355.
29. Downes E, Sikirica V, Gilabert-Estelles J, et al. The burden of uterine fibroids in five European countries. Eur J Obstet Gynecol Reprod Biol. 2010;152:96-102.
30. Eskenazi B, Warner ML. Epidemiology of endometriosis. Obstet Gynecol Clin North Am. 1997;24:235-258.
31. Viganò P, Parazzini F, Somigliana E, Vercellini P. Endometriosis: epidemiology and aetiological factors. Best Pract Res Clin Obstet Gynaecol. 2004;18:177-200.
32. Rogers PA, D'Hooghe TM, Fazleabas A, et al. Priorities for endometriosis research: recommendations from an international consensus workshop. Reprod Sci. 2009;16:335-346.
33. Adamson DG, Kennedy S, Hummelshoj L. Creating solutions in endometriosis: global collaboration through the World Endometriosis Research Foundation. J Endometr. 2010;2:3-6.
34. Matorras R, Rodríguez F, Pijoan JI, et al. Women who are not exposed to spermatozoa and infertile women have similar rates of stage I endometriosis. Fertil Steril. 2001;76:923-928.
35. Balasch J, Creus M, Fábregues F, et al. Visible and non-visible endometriosis at laparoscopy in fertile and infertile women and in patients with chronic pelvic pain: a prospective study. Hum Reprod. 1996;11:387-391.
36. Rawson JM. Prevalence of endometriosis in asymptomatic women. J Reprod Med. 1991;36:513-515.
37. Williams TJ, Pratt JH. Endometriosis in 1,000 consecutive celiotomies: incidence and management. Am J Obstet Gynecol. 1977;129:245-250.
38. Sangi-Haghpeykar H, Poindexter AN 3rd. Epidemiology of endometriosis among parous women. Obstet Gynecol. 1995;85:983-992.
39. Zimmermann A, Bernuit D, Gerlinger C, Schaefers M, Geppert K. Prevalence, symptoms and management of uterine fibroids: an international internet-based survey of 21,746 women. BMC Womens Health. 2012;12:6.
40. Khan AT, Shehmar M, Gupta JK. Uterine fibroids: current perspectives. Int J Womens Health. 2014;6:95-114.
41. Gao X, Yeh YC, Outley J, Simon J, Botteman M, Spalding J. Health-related quality of life burden of women with endometriosis: a literature review. Curr Med Res Opin. 2006;22:1787-1797.
42. Fernandez H, Farrugia M, Jones SE, Mauskopf JA, Oppelt P, Subramanian D. Rate, type, and cost of invasive interventions for uterine myomas in Germany, France, and England. J Minim Invasive Gynecol. 2009;16:40-46.
43. Prast J, Oppelt P, Shamiyeh A, Shebl O, Brandes I, Haas D. Costs of endometriosis in Austria: a survey of direct and indirect costs. Arch Gynecol Obstet. 2013;288:569-576.
44. Simoens S, Dunselman G, Dirksen C, et al. The burden of endometriosis: costs and quality of life of women with endometriosis and treated in referral centres. Hum Reprod. 2012;27:1292-1299.
45. Hansen KE, Kesmodel US, Baldursson EB, Schultz R, Forman A. The influence of endometriosis-related symptoms on work life and work ability: a study of Danish endometriosis patients in employment. Eur J Obstet Gynecol Reprod Biol. 2013;169:331-339.
46. Haas D, Chvatal R, Reichert B, et al. Endometriosis: a premenopausal disease? Age pattern in 42,079 patients with endometriosis. Arch Gynecol Obstet. 2012;286:667-670.
47. Gore AC, Chappell VA, Fenton SE, et al. EDC-2: The Endocrine Society's second scientific statement on endocrine-disrupting chemicals. Endocr Rev. 2015;36:E1-E150.
48. Bellanger M, Demeneix B, Grandjean P, Zoeller RT, Trasande L. Neurobehavioral deficits, diseases, and associated costs of exposure to endocrine-disrupting chemicals in the European union. J Clin Endocrinol Metab. 2015;100:1256-1266.
49. Hauser R, Skakkebaek NE, Hass U, et al. Male reproductive disorders, diseases, and costs of exposure to endocrine-disrupting chemicals in the European union. J Clin Endocrinol Metab. 2015;100:1267-1277.
50. Legler J, Fletcher T, Govarts E, et al. Obesity, diabetes, and associated costs of exposure to endocrine-disrupting chemicals in the European union. J Clin Endocrinol Metab. 2015;100:1278-1288.
51. Trasande L, Zoeller RT, Hass U, et al. Estimating burden and disease costs of exposure to endocrine-disrupting chemicals in the European union. J Clin Endocrinol Metab. 2015;100:1245-1255.
52. Alwis ID, Maroni DM, Hendry IR, et al. Neonatal diethylstilbestrol exposure disrupts female reproductive tract structure/function via both direct and indirect mechanisms in the hamster. Reprod Toxicol. 2011;32:472-483.
53. Atkins D, Eccles M, Flottorp S, et al. Systems for grading the quality of evidence and the strength of recommendations I: critical appraisal of existing approaches The GRADE Working Group. BMC Health Serv Res. 2004;4:38.
54. Schünemann HJ, Schünemann AH, Oxman AD, et al. Grading quality of evidence and strength of recommendations for diagnostic tests and strategies. BMJ. 2008;336:1106-1110.
55. European Union. Roadmap for evaluation of endocrine disruptor chemicals. 2014. Available at http://ec.europa.eu/smart-regulation/impact/planned-ia/docs/2014-env-009-endocrine-disruptors-en.pdf. Accessed October 15, 2014.
56. Hass U, Christiansen S, Axelstad M, et al. Evaluation of 22 SIN List 2.0 substances according to the Danish proposal on criteria for endocrine disrupters. 2012. Available at http://eng.mst.dk/media/mst/67169/SIN%20report%20and%20Annex.pdf. Accessed May 12, 2014.
57. Intergovernmental Panel on Climate Change. Guidance notes for lead authors of the IPCC Fourth Assessment Report on addressing uncertainties. 2005. Available at http://www.ipcc.ch/meetings/ar4-workshops-express-meetings/uncertainty-guidance-note.pdf. Accessed May 12, 2014.
58. Govarts E, Nieuwenhuijsen M, Schoeters G, et al. Birth weight and prenatal exposure to polychlorinated biphenyls (PCBs) and dichlorodiphenyldichloroethylene (DDE): a meta-analysis within 12 European Birth Cohorts. Environ Health Perspect. 2012;120:162-170.
59. Den Hond E, Govarts E, Willems H, et al. First steps toward harmonized human biomonitoring in Europe: demonstration project to perform human biomonitoring on a European scale. Env Health Perspect. 2015;123:255-263.
60. Trabert B, Chen Z, Kannan K, et al. Persistent organic pollutants (POPs) and fibroids: results from the ENDO study. J Expo Sci Environ Epidemiol. 2015;25:278-285.
61. United Nations Economic Commission for Europe. Population, 5-year age groups, by sex. 2014. Available at http://w3.unece.org/PXWeb2015/pxweb/en/STAT/STAT-30-GE-01-Pop. Accessed August 26, 2014.
62. Buck Louis GM, Peterson CM, Chen Z, et al. Bisphenol A and phthalates and endometriosis: the Endometriosis: Natural History, Diagnosis and Outcomes Study. Fertil Steril. 2013;100:162-169.e161-e162.
63. Abbas S, Ihle P, Köster I, Schubert I. Prevalence and incidence of diagnosed endometriosis and risk of endometriosis in patients with endometriosis-related symptoms: findings from a statutory health insurance-based cohort in Germany. Eur J Obstet Gynecol Reprod Biol. 2012;160:79-83.
64. World Bank. GDP per capita, PPP (current international $). 2014. Available at http://data.worldbank.org/indicator/NY.GDP.PCAP.PP.CD. Accessed May 22, 2014.
65. Erixon F, van der Mare E. What is driving the rise in health care expenditures? An inquiry into the nature and causes of the cost disease. ECIPE working paper number 05/2011. 2011. Available at http://www.ecipe.org/media/publication-pdfs/what-is-driving-the-rise-in-health-care-expenditures-an-inquiry-into-the-nature-and-causes-of-the-cost-disease-1.pdf. Accessed September 3, 2014.
66. Klein S, D'Hooghe T, Meuleman C, Dirksen C, Dunselman G, Simoens S. What is the societal burden of endometriosis-associated symptoms? A prospective Belgian study. Reprod Biomed Online. 2014;28:116-124.
67. McLachlan JA, Newbold RR, Bullock BC. Long-term effects on the female mouse genital tract associated with prenatal exposure to diethylstilbestrol. Cancer Res. 1980;40:3988-3999.
68. Suzuki A, Sugihara A, Uchida K, et al. Developmental effects of perinatal exposure to bisphenol-A and diethylstilbestrol on reproductive organs in female mice. Reprod Toxicol. 2002;16:107-116.
69. Newbold RR, Jefferson WN, Padilla-Banks E. Long-term adverse effects of neonatal exposure to bisphenol A on the murine female reproductive tract. Reprod Toxicol. 2007;24:253-258.
70. Newbold RR, Jefferson WN, Padilla-Banks E. Prenatal exposure to bisphenol a at environmentally relevant doses adversely affects the murine female reproductive tract later in life. Environ Health Perspect. 2009;117:879-885.
71. Fei X, Chung H, Taylor HS. Methoxychlor disrupts uterine Hoxa10 gene expression. Endocrinology. 2005;146:3445-3451.
72. Takayama S, Sieber SM, Dalgard DW, Thorgeirsson UP, Adamson RH. Effects of long-term oral administration of DDT on nonhuman primates. J Cancer Res Clin Oncol. 1999;125:219-225.
73. Bredhult C, Bäcklin BM, Bignert A, Olovsson M. Study of the relation between the incidence of uterine leiomyomas and the concentrations of PCB and DDT in Baltic gray seals. Reprod Toxicol. 2008;25:247-255.
74. Fowler PA, Bellingham M, Sinclair KD, et al. Impact of endocrine-disrupting compounds (EDCs) on female reproductive health. Mol Cell Endocrinol. 2012;355:231-239.
75. Pollack AZ, Buck Louis GM, Chen Z, et al. Bisphenol A, benzophenone-type ultraviolet filters, and phthalates in relation to uterine leiomyoma. Environ Res. 2015;137:101-107.
76. Lambertino A, Turyk M, Anderson H, Freels S, Persky V. Uterine leiomyomata in a cohort of Great Lakes sport fish consumers. Environ Res. 2011;111:565-572.
77. Eskenazi B, Warner M, Samuels S, et al. Serum dioxin concentrations and risk of uterine leiomyoma in the Seveso Women's Health Study. Am J Epidemiol. 2007;166:79-87.
78. Luisi S, Latini G, de Felice C, et al. Low serum concentrations of di-(2-ethylhexyl)phthalate in women with uterine fibromatosis. Gynecol Endocrinol. 2006;22:92-95.
79. Weuve J, Hauser R, Calafat AM, Missmer SA, Wise LA. Association of exposure to phthalates with endometriosis and uterine leiomyomata: findings from NHANES, 1999-2004. Environ Health Perspect. 2010;118:825-832.
80. Wise LA, Palmer JR, Reich D, Cozier YC, Rosenberg L. Hair relaxer use and risk of uterine leiomyomata in African-American women. Am J Epidemiol. 2012;175:432-440.
81. Cummings AM, Metcalf JL, Birnbaum L. Promotion of endometriosis by 2,3,7,8-tetrachlorodibenzo-p-dioxin in rats and mice: timedose dependence and species comparison. Toxicol Appl Pharmacol. 1996;138:131-139.
82. 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.
83. Rier SE, Turner WE, Martin DC, Morris R, Lucier GW, Clark GC. 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.
84. Upson K, Sathyanarayana S, De Roos AJ, et al. Phthalates and risk of endometriosis. Environ Res. 2013;126:91-97.
85. Rundle A, Hoepner L, Hassoun A, et al. Association of childhood obesity with maternal exposure to ambient air polycyclic aromatic hydrocarbons during pregnancy. Am J Epidemiol. 2012;175:1163-1172.
86. Huang PC, Tsai EM, Li WF, et al. Association between phthalate exposure and glutathione S-transferase M1 polymorphism in adenomyosis, leiomyoma and endometriosis. Hum Reprod. 2010;25:986-994.
87. Sadeu JC, Foster WG. The cigarette smoke constituent benzo[a]pyrene disrupts metabolic enzyme, and apoptosis pathway member gene expression in ovarian follicles. Reprod Toxicol. 2013;40:52-59.
88. Itoh H, Iwasaki M, Hanaoka T, Sasaki H, Tanaka T, Tsugane S. Urinary phthalate monoesters and endometriosis in infertile Japanese women. Sci Total Environ. 2009;408:37-42.
89. Reddy BS, Rozati R, Reddy BV, Raman NV. Association of phthalate esters with endometriosis in Indian women. BJOG. 2006;113:515-520.
90. Cobellis L, Latini G, De Felice C, et al. High plasma concentrations of di-(2-ethylhexyl)-phthalate in women with endometriosis. Hum Reprod. 2003;18:1512-1515.