Abstract
Purpose
Endocrine-related diseases and disorders are on the rise globally. Synthetically produced environmental chemicals (endocrine-disrupting chemicals (EDCs)) mimic hormones like oestrogen and alter signalling pathways. Endometriosis is an oestrogen-dependent condition, affecting 10–15% of women of the reproductive age, and has substantial impacts on the quality of life. The aetiology of endometriosis is believed to be multifactorial, ranging from genetic causes to immunologic dysfunction due to environmental exposure to EDCs. Hence, we undertook a systematic review and investigated the epidemiological evidence for an association between EDCs and the development of endometriosis. We also aimed to assess studies on the relationship between body concentration of EDCs and the severity of endometriosis.
Method
Following PRISMA guidelines, a structured search of PubMed, Embase and Scopus was conducted (to July 2018). The included studies analysed the association between one or more EDCs and the prevalence of endometriosis. The types of EDCs, association and outcome, participant characteristics and confounding variables were extracted and analysed. Quality assessment was performed using standard criteria.
Results
In total, 29 studies were included. Phthalate esters were positively associated with the prevalence of endometriosis. The majority (71%) of studies revealed a significant association between bisphenol A, organochlorinated environmental pollutants (dioxins, dioxin-like compounds, organochlorinated pesticides, polychlorinated biphenyls) and the prevalence of endometriosis. A positive association between copper, chromium and prevalence of endometriosis was demonstrated in one study only. Cadmium, lead and mercury were not associated with the prevalence of endometriosis. There were conflicting results for the association between nickel and endometriosis. The relationship of EDCs and severity of endometriosis was not established in the studies.
Conclusion
We found some evidence to suggest an association between phthalate esters, bisphenol A, organochlorinated environmental pollutants and the prevalence of endometriosis. Disentangling these exposures from various other factors that affect endometriosis is complex, but an important topic for further research.
Acknowledgements
We are thankful to Mr. Scott Macintyre (Librarian – School of Public Health, The University of Queensland) for rendering assistance in formulating the search strategy and guiding us through the database search.
Research funding: Authors state no funding involved.
Author contributions: All authors have accepted responsibility for the entire content of this manuscript and approved its submission.
Competing interests: Authors state no conflict of interest.
Informed consent: Informed consent is not applicable.
Ethical approval: The conducted research is not related to either human or animal use.
Abbreviation used for authors in the main text: Diksha Sirohi (DS); Ruqaiya Al Ramadhani (RA).
References
1. Crain, DA, Janssen, SJ, Edwards, TM, Heindel, J, Ho, S-M, Hunt, P, et al. Female reproductive disorders: the roles of endocrine-disrupting compounds and developmental timing. Fertil Steril 2008;90:911–40. https://doi.org/10.1016/j.fertnstert.2008.08.067.Search in Google Scholar
2. United Nations Environment Programme (UNEP); WHO.State of the Science of endocrine disrupting chemicals – 2012. An assessment of the state of the science of endocrine disruptors prepared by a group of experts for the United Nations Environment Programme (UNEP) and WHO, Geneva, Switzerland; 2013.Search in Google Scholar
3. United Nations Department of Economic Social Affairs. World fertility patterns 2015. United Nations Department (Population Division) 2015 of Economic and Social Affairs; New York, USA; 2015.Search in Google Scholar
4. Darbre, PD. What are endocrine disrupters and where are they found? Endocrine disruption and human health. Netherlands: Elsevier; 2015.10.1016/B978-0-12-801139-3.00001-6Search in Google Scholar
5. Donnez, J, Nisolle, M. Peritoneal, ovarian and recto-vaginal endometriosis: the identification of three separate diseases. New York, USA: CRC Press; 1996.Search in Google Scholar
6. Canis, M, Donnez, J, Guzick, D, Halme, J, Rock, J, Schenken, R, et al. Revised American society for reproductive medicine classification of endometriosis: 1996. Fertil Steril 1997;67:817–21. https://doi.org/10.1016/S0015-0282(97)81391.Search in Google Scholar
7. Simoens, S, Dunselman, G, Dirksen, C, Hummelshoj, L, Bokor, A, Brandes, I, et al. The burden of endometriosis: costs and quality of life of women with endometriosis and treated in referral centres. Hum Reprod 2012;27:1292–9. https://doi.org/10.1093/humrep/des073.Search in Google Scholar
8. Lozano, R, Naghavi, M, Foreman, K, Lim, S, Shibuya, K, Aboyans, V, et al. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the global burden of disease study 2010. Lancet 2012;380:2095–128. https://doi.org/10.1016/S0140-6736(12)61728-0.Search in Google Scholar
9. Eriksen, MB, Frandsen, TF. The impact of patient, intervention, comparison, outcome (PICO) as a search strategy tool on literature search quality: a systematic review. JMLA 2018;106:420. https://doi.org/10.5195/jmla.2018.345.Search in Google Scholar
10. Moher, D, Liberati, A, Tetzlaff, J, Altman, DG, Group, P. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 2009;6:e1000097. https://doi.org/10.1371/journal.pmed.1000097.Search in Google Scholar
11. Signorile, PG, Spugnini, EP, Mita, L, Mellone, P, D’Avino, A, Bianco, M, et al. Pre-natal exposure of mice to bisphenol A elicits an endometriosis-like phenotype in female offspring. Gen Comp Endocrinol 2010;168:318–25. https://doi.org/10.1016/j.ygcen.2010.03.030.Search in Google Scholar
12. Bazot, M, Lafont, C, Rouzier, R, Roseau, G, Thomassin-Naggara, I, Darai, E. Diagnostic accuracy of physical examination, transvaginal sonography, rectal endoscopic sonography, and magnetic resonance imaging to diagnose deep infiltrating endometriosis. Fertil Steril 2009;92:1825–33. https://doi.org/10.1016/j.fertnstert.2008.09.005.Search in Google Scholar
13. Upson, K, Sathyanarayana, S, De Roos, AJ, Koch, HM, Scholes, D, Holt, VL. A population-based case–control study of urinary bisphenol A concentrations and risk of endometriosis. Hum Reprod 2014;29:2457–64. https://doi.org/10.1093/humrep/deu227.Search in Google Scholar
14. Stang, A. Critical evaluation of the Newcastle–Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 2010;25:603–5. https://doi.org/10.1007/s10654-010-9491-z.Search in Google Scholar
15. National Toxicology Program. OHAT risk of bias rating tool for human and animal studies. Office of health assessment and translation (OHAT); 2015. Available from: http://ntpniehs.nihgov/pubhealth/hat/noms/index-2 html [Accessed 2 Jan 2015].Search in Google Scholar
16. Reddy, BS, Rozati, R, Reddy, S, Kodampur, S, Reddy, P, Reddy, R. High plasma concentrations of polychlorinated biphenyls and phthalate esters in women with endometriosis: a prospective case control study. Fertil Steril 2006;85:775–9. https://doi.org/10.1016/j.fertnstert.2005.08.037.Search in Google Scholar
17. Heilier, J-F, Donnez, J, Nackers, F, Rousseau, R, Verougstraete, V, Rosenkranz, K, et al. Environmental and host-associated risk factors in endometriosis and deep endometriotic nodules: a matched case–control study. Environ Res 2007;103:121–9. https://doi.org/10.1016/j.envres.2006.04.004.Search in Google Scholar
18. Schiattarella, A, Colacurci, N, Morlando, M, Ammaturo, FP, Genovese, G, Miraglia, N, et al. Plasma and urinary levels of lead and cadmium in patients with endometriosis. Italian J Gynaecol Obst 2018;30:47–52. Available from: https://hdl.handle.net/11591/392280.Search in Google Scholar
19. Rashidi, BH, Amanlou, M, Lak, TB, Ghazizadeh, M, Eslami, B. A case–control study of bisphenol A and endometrioma among subgroup of Iranian women. J Res Med Sci: Off J Isfahan Univ Med Sci 2017;22. https://doi.org/10.4103/2F1735-1995.199086.Search in Google Scholar
20. Simonelli, A, Guadagni, R, De Franciscis, P, Colacurci, N, Pieri, M, Basilicata, P, et al. Environmental and occupational exposure to bisphenol A and endometriosis: urinary and peritoneal fluid concentration levels. Int Arch Occup Environ Health 2017;90:49–61. https://doi.org/10.1007/s00420-016-1171-1.Search in Google Scholar
21. Buck Louis, GM, Peterson, CM, Chen, Z, Croughan, M, Sundaram, R, Stanford, J, et al. Bisphenol A and phthalates and endometriosis: the endometriosis: natural history, diagnosis and outcomes study. Fertil Steril 2013;100. https://doi.org/10.1016/j.fertnstert.2013.03.026.Search in Google Scholar
22. Quignot, N, Arnaud, M, Robidel, F, Lecomte, A, Tournier, M, Cren-Olivé, C, et al. Characterization of endocrine-disrupting chemicals based on hormonal balance disruption in male and female adult rats. Reprod Toxicol 2012;33:339–52. https://doi.org/10.1016/j.reprotox.2012.01.004.Search in Google Scholar
23. Bergqvist, A, Fernö, M. Endometriosis: oestrogen and progesterone receptors in endometriotic tissue and endometrium: comparison of different cycle phases and ages. Hum Reprod 1993;8:2211–7. https://doi.org/10.1093/oxfordjournals.humrep.a138005.Search in Google Scholar
24. Attia, GR, Zeitoun, K, Edwards, D, Johns, A, Carr, BR, Bulun, SE. Progesterone receptor isoform A but not B is expressed in endometriosis. J Clin Endocrinol Metabol 2000;85:2897–902. https://doi.org/10.1210/jcem.85.8.6739.Search in Google Scholar
25. Honma, S, Suzuki, A, Buchanan, DL, Katsu, Y, Watanabe, H, Iguchi, T. Low dose effect of in utero exposure to bisphenol A and diethylstilbestrol on female mouse reproduction. Reprod Toxicol 2002;16:117–22. https://doi.org/10.1016/s0890-6238(02)00006-0.Search in Google Scholar
26. Markey, CM, Coombs, MA, Sonnenschein, C, Soto, AM. Mammalian development in a changing environment: exposure to endocrine disruptors reveals the developmental plasticity of steroid‐hormone target organs. Evol Dev 2003;5:67–75. https://doi.org/10.1046/j.1525-142x.2003.03011.x.Search in Google Scholar
27. Huang, R-P, Liu, Z-H, Yin, H, Dang, Z, Wu, P-X, Zhu, N-W, et al. Bisphenol A concentrations in human urine, human intakes across six continents, and annual trends of average intakes in adult and child populations worldwide: a thorough literature review. Sci Total Environ 2018;626:971–81. https://doi.org/10.1016/j.scitotenv.2018.01.144.Search in Google Scholar
28. Huang, PC, Tsai, EM, Li, WF, Liao, PC, Chung, MC, Wang, YH, et al. Association between phthalate exposure and glutathione S-transferase M1 polymorphism in adenomyosis, leiomyoma and endometriosis. Hum Reprod 2010;25:986–94. https://doi.org/10.1093/humrep/deq015.Search in Google Scholar
29. Reddy, BS, Rozati, R, Reddy, BV, Raman, NV. Association of phthalate esters with endometriosis in Indian women. BJOG An Int J Obstet Gynaecol 2006;113:515–20. https://doi.org/10.1111/j.1471-0528.2006.00925.x.Search in Google Scholar
30. Rozati, R, Simha, B, Bendi, N, Sekhar, C. Evaluation of the phthalate esters in South Indian women with endometriosis. Int J Fert Steril 2008;1:165–70.Search in Google Scholar
31. Upson, K, Sathyanarayana, S, De Roos, AJ, Thompson, ML, Scholes, D, Dills, R, et al. Phthalates and risk of endometriosis. Environ Res 2013;126:91–7. https://doi.org/10.1016/j.envres.2013.07.003.Search in Google Scholar
32. Kim, SH, Chun, S, Jang, JY, Chae, HD, Kim, CH, Kang, BM. Increased plasma levels of phthalate esters in women with advanced-stage endometriosis: a prospective case-control study. Fertil Steril 2011;95:357–9. https://doi.org/10.1016/j.fertnstert.2010.07.1059.Search in Google Scholar
33. Reinsberg, J, Wegener-Toper, P, van der Ven, K, van der Ven, H, Klingmueller, D. Effect of mono-(2-ethylhexyl) phthalate on steroid production of human granulosa cells. Toxicol Appl Pharmacol 2009;239:116–23. https://doi.org/10.1016/j.taap.2009.05.022.Search in Google Scholar
34. Davis, B, Maronpot, R, Heindel, J. Di-(2-ethylhexyl) phthalate suppresses estradiol and ovulation in cycling rats. Toxicol Appl Pharmacol 1994;128:216–23. https://doi.org/10.1006/taap.1994.1200.Search in Google Scholar
35. Gupta, RK, Singh, JM, Leslie, TC, Meachum, S, Flaws, JA, Yao, HH. Di-(2-ethylhexyl) phthalate and mono-(2-ethylhexyl) phthalate inhibit growth and reduce estradiol levels of antral follicles in vitro. Toxicol Appl Pharmacol 2010;242:224–30. https://doi.org/10.1016/j.taap.2009.10.011.Search in Google Scholar
36. Li, N, Liu, T, Zhou, L, He, J, Ye, L. Di-(2-ethylhcxyl) phthalate reduces progesterone levels and induces apoptosis of ovarian granulosa cell in adult female ICR mice. Environ Toxicol Pharmacol 2012;34:869–75. https://doi.org/10.1016/j.etap.2012.08.013.Search in Google Scholar
37. Weuve, J, Hauser, R, Calafat, AM, Missmer, SA, Wise, LA. Association of exposure to phthalates with endometriosis and uterine leiomyomata: findings from NHANES. Environ Health Perspect 1999-2004 2010;118:825–32. https://doi.org/10.1289/ehp.0901543.Search in Google Scholar
38. Pollack, AZ, Louis, GM, Chen, Z, Peterson, CM, Sundaram, R, Croughan, MS, et al. Trace elements and endometriosis: the ENDO study. Reprod Toxicol 2013;42:41–8. https://doi.org/10.1016/j.reprotox.2013.05.009.Search in Google Scholar
39. Darbre, P. Metalloestrogens: an emerging class of inorganic xenoestrogens with potential to add to the oestrogenic burden of the human breast. J Appl Toxicol: Int J 2006;26:191–7. https://doi.org/10.1002/jat.1135.Search in Google Scholar
40. Silva, N, Senanayake, H, Waduge, V. Elevated levels of whole blood nickel in a group of Sri Lankan women with endometriosis: a case control study. BMC Res Notes 2013;6:13. https://doi.org/10.1186/1756-0500-6-13.Search in Google Scholar
41. Check, L, Marteel-Parrish, A. The fate and behavior of persistent, bioaccumulative, and toxic (PBT) chemicals: examining lead (Pb) as a PBT metal. Rev Environ Health 2013;28:85–96. https://doi.org/10.1515/reveh-2013-0005.Search in Google Scholar
42. Foster, WG. Reproductive toxicity of chronic lead exposure in the female cynomolgus monkey. Reprod Toxicol 1992;6:123–31. https://doi.org/10.1016/0890-6238(92)90113-8.Search in Google Scholar
43. Henson, MC, Chedrese, PJ. Endocrine disruption by cadmium, a common environmental toxicant with paradoxical effects on reproduction. Exp Biol Med 2004;229:383–92. https://doi.org/10.1177/153537020422900506.Search in Google Scholar
44. Vahter, M, Berglund, M, Åkesson, A, Liden, C. Metals and women’s health. Environ Res 2002;88:145–55. https://doi.org/10.1006/enrs.2002.4338.Search in Google Scholar
45. Heilier, JF, Donnez, J, Verougstraete, V, Donnez, O, Grandjean, F, Haufroid, V, et al. Cadmium, lead and endometriosis. Int Arch Occup Environ Health 2006;80:149–53. https://doi.org/10.1007/s00420-006-0114-7.Search in Google Scholar
46. Heilier, JF, Verougstraete, V, Nackers, F, Tonglet, R, Donnez, J, Lison, D. Assessment of cadmium impregnation in women suffering from endometriosis: a preliminary study. Toxicol Lett 2004;154:89–93. https://doi.org/10.1016/j.toxlet.2004.07.006.Search in Google Scholar
47. Itoh, H, Iwasaki, M, Nakajima, Y, Endo, Y, Hanaoka, T, Sasaki, H, et al. A case-control study of the association between urinary cadmium concentration and endometriosis in infertile Japanese women. Sci Total Environ 2008;402:171–5. https://doi.org/10.1016/j.scitotenv.2008.05.006.Search in Google Scholar
48. MacMahon, B, Trichopoulos, D, Cole, P, Brown, J. Cigarette smoking and urinary oestrogens. N Engl J Med 1982;307:1062–5. https://doi.org/10.1056/nejm198210213071707.Search in Google Scholar
49. Cramer, DW, Wilson, E, Stillman, RJ, Berger, MJ, Belisle, S, Schiff, I, et al. The relation of endometriosis to menstrual characteristics, smoking, and exercise. JAMA 1986;255:1904–8. https://doi.org/10.1001/jama.1986.03370140102032.Search in Google Scholar
50. Jackson, LW, Zullo, MD, Goldberg, J. The association between heavy metals, endometriosis and uterine myomas among premenopausal women: national health and nutrition examination survey 1999–2002. Hum Reprod 2008;23:679–87. https://doi.org/10.1093/humrep/dem394.Search in Google Scholar
51. White, M. A comparison of inductively coupled plasma mass spectrometry with electrothermal atomic absorption spectrophotometry for the determination of trace elements in blood and urine from non occupationally exposed populations. J Trace Elem Med Biol 1999;13:93–101. https://doi.org/10.1016/s0946-672x(99)80030-3.Search in Google Scholar
52. Olmedo, P, Pla, A, Hernández, A, López-Guarnido, O, Rodrigo, L, Gil, F. Validation of a method to quantify chromium, cadmium, manganese, nickel and lead in human whole blood, urine, saliva and hair samples by electrothermal atomic absorption spectrometry. Anal Chim Acta 2010;659:60–7. https://doi.org/10.1016/j.aca.2009.11.056.Search in Google Scholar
53. Nehru, B, Kaushal, S. Effect of lead on hepatic microsomal enzyme activity. J Appl Toxicol 1992;12:401–5. https://doi.org/10.1002/jat.2550120607.Search in Google Scholar
54. Taupeau, C, Poupon, J, Treton, D, Brosse, A, Richard, Y, Machelon, V. Lead reduces messenger RNA and protein levels of cytochrome p450 aromatase and oestrogen receptor β in human ovarian granulosa cells. Biol Reprod 2003;68:1982–8. https://doi.org/10.1095/biolreprod.102.009894.Search in Google Scholar
55. Donnez, J, Van Langendonckt, A, Casanas-Roux, F, Van Gossum, J-P, Pirard, C, Jadoul, P, et al. Current thinking on the pathogenesis of endometriosis. Gynecol Obstet Invest 2002;54:52–62. https://doi.org/10.1159/000066295.Search in Google Scholar
56. Marinov, B, Tsachev, K, Doganov, N, Dzherov, L, Atanasova, B, Markova, M. The copper concentration in the blood serum of women with ovarian tumors (a preliminary report). Akusherstvo i ginekologiia 2000;39:36–7. Available from: https://europepmc.org/article/med/10948620.Search in Google Scholar
57. Guney, M, Oral, B, Demirin, H, Karahan, N, Mungan, T, Delibas, N. Protective effects of vitamins C and E against endometrial damage and oxidative stress in fluoride intoxication. Clin Exp Pharmacol Physiol 2007;34:467–74. https://doi.org/10.1111/j.1440-1681.2007.04596.x.Search in Google Scholar
58. Cano-Sancho, G, Ploteau, S, Matta, K, Adoamnei, E, Louis, GB, Mendiola, J, et al. Human epidemiological evidence about the associations between exposure to organochlorine chemicals and endometriosis: systematic review and meta-analysis. Environ Int 2019;123:209–23. https://doi.org/10.1016/j.envint.2018.11.065.Search in Google Scholar
59. Buck Louis, GM, Chen, Z, Matthew Peterson, C, Hediger, ML, Croughan, MS, Sundaram, R, et al. Persistent lipophilic environmental chemicals and endometriosis: the ENDO study. Environ Health Perspect 2012;120:811–6. https://doi.org/10.1289/ehp.1104432.Search in Google Scholar
60. Neilson, AH. An environmental perspective on the biodegradation of organochlorine xenobiotics. Int Biodeterior Biodegrad 1996;37:3–21. https://doi.org/10.1016/0964-8305(95)00092-5.Search in Google Scholar
61. Bretveld, RW, Thomas, CM, Scheepers, PT, Zielhuis, GA, Roeleveld, N. Pesticide exposure: the hormonal function of the female reproductive system disrupted?. Reprod Biol Endocrinol 2006;4:30. https://doi.org/10.1186/1477-7827-4-30.Search in Google Scholar
62. VoPham, T, Bertrand, KA, Jones, RR, Deziel, NC, DuPré, NC, James, P, et al. Dioxin exposure and breast cancer risk in a prospective Cohort study. Environ Res 2020;186: 109516. https://doi.org/10.1016/j.envres.2020.109516.Search in Google Scholar
63. Bao, Y, Zhang, L, Liu, X, Shi, L, Li, J, Meng, G, et al. Dioxin-like compounds in paired maternal serum and breast milk under long sampling intervals. Ecotoxicol Environ Safety 2020;194:110339. https://doi.org/10.1016/j.ecoenv.2020.110339.Search in Google Scholar
64. Cai, LY, Izumi, S, Suzuki, T, Goya, K, Nakamura, E, Sugiyama, T, et al. Dioxins in ascites and serum of women with endometriosis: a pilot study. Hum Reprod 2011;26:117–26. https://doi.org/10.1093/humrep/deq312.Search in Google Scholar
65. Heilier, JF, Nackers, F, Verougstraete, V, Tonglet, R, Lison, D, Donnez, J. Increased dioxin-like compounds in the serum of women with peritoneal endometriosis and deep endometriotic (adenomyotic) nodules. Fertil Steril 2005;84:305–12. https://doi.org/10.1016/j.fertnstert.2005.04.001.Search in Google Scholar
66. Martinez-Zamora, MA, Mattioli, L, Parera, J, Abad, E, Coloma, JL, van Babel, B, et al. Increased levels of dioxin-like substances in adipose tissue in patients with deep infiltrating endometriosis. Hum Reprod 2015;30:1059–68. https://doi.org/10.1093/humrep/dev026.Search in Google Scholar
67. Ploteau, S, Cano-Sancho, G, Volteau, C, Legrand, A, Vénisseau, A, Vacher, V, et al. Associations between internal exposure levels of persistent organic pollutants in adipose tissue and deep infiltrating endometriosis with or without concurrent ovarian endometrioma. Environ Int 2017;108:195–203. https://doi.org/10.1016/j.envint.2017.08.019.Search in Google Scholar
68. Simsa, P, Mihalyi, A, Schoeters, G, Koppen, G, Kyama, CM, Den Hond, EM, et al. Increased exposure to dioxin-like compounds is associated with endometriosis in a case-control study in women. Reprod Biomed Online 2010;20:681–8. https://doi.org/10.1016/j.rbmo.2010.01.018.Search in Google Scholar
69. De Felip, E, Porpora, MG, di Domenico, A, Ingelido, AM, Cardelli, M, Cosmi, EV, et al. Dioxin-like compounds and endometriosis: a study on Italian and Belgian women of reproductive age. Toxicol Lett 2004;150:203–9. https://doi.org/10.1016/j.toxlet.2004.01.008.Search in Google Scholar
70. Niskar, AS, Needham, LL, Rubin, C, Turner, WE, Martin, CA, Patterson, DGJr, et al. Serum dioxins, polychlorinated biphenyls, and endometriosis: a case-control study in Atlanta. Chemosphere 2009;74:944–9. https://doi.org/10.1016/j.chemosphere.2008.10.005.Search in Google Scholar
71. Pauwels, A, Schepens, PJ, D’Hooghe, T, Delbeke, L, Dhont, M, Brouwer, A, et al. The risk of endometriosis and exposure to dioxins and polychlorinated biphenyls: a case-control study of infertile women. Hum Reprod 2001;16:2050–5. https://doi.org/10.1093/humrep/16.10.2050.Search in Google Scholar
72. Porpora, MG, Medda, E, Abballe, A, Bolli, S, De Angelis, I, di Domenico, A, et al. Endometriosis and organochlorinated environmental pollutants: a case-control study on Italian women of reproductive age. Environ Health Perspect 2009;117:1070–5. https://doi.org/10.1289/ehp.0800273.Search in Google Scholar
73. Eskenazi, B, Mocarelli, P, Warner, M, Samuels, S, Vercellini, P, Olive, D, et al. Serum dioxin concentrations and endometriosis: a cohort study in Seveso, Italy. Environ Health Perspect 2002;110:629–34. https://doi.org/10.1289/ehp.02110629.Search in Google Scholar
74. Mayani, A, Barel, S, Soback, S, Almagor, M. Dioxin concentrations in women with endometriosis. Hum Reprod 1997;12:373–5. https://doi.org/10.1093/humrep/12.2.373.Search in Google Scholar
75. Hahn, ME. Evolutionary and physiological perspectives on Ah receptor function and dioxin toxicity. In: Dioxins and Health, 2nd ed. Hoboken, New Jersey: John Wiley & Sons, Inc.; 2003:559–602. https://doi.org/10.1002/0471722014.ch14.10.1002/0471722014.ch14Search in Google Scholar
76. Koninckx, P, Kennedy, S, Barlow, D. Endometriotic disease: the role of peritoneal fluid. Hum Reprod Update 1998;4:741–51. https://doi.org/10.1093/humupd/4.5.741.Search in Google Scholar
77. van Cleuvenbergen, R. Dioxins (PCDDs and PCDFs) in human milk from Flanders, Belgium: concentration levels and congener profile. Organohalogen Compounds 1994;20:215.Search in Google Scholar
78. Safe, S. Polychlorinated biphenyls (PCBs), dibenzo-p-dioxins (PCDDs), dibenzofurans (PCDFs), and related compounds: environmental and mechanistic considerations which support the development of toxic equivalency factors (TEFs). Crit Rev Toxicol 1990;21:51–88. https://doi.org/10.3109/10408449009089873.Search in Google Scholar
79. Buck Louis, GM, Weiner, JM, Whitcomb, BW, Sperrazza, R, Schisterman, EF, Lobdell, DT, et al. Environmental PCB exposure and risk of endometriosis. Hum Reprod 2005;20:279–85. https://doi.org/10.1093/humrep/deh575.Search in Google Scholar
80. Porpora, MG, Ingelido, AM, Domenico, AD, Ferro, A, Crobu, M, Pallante, D, et al. Increased levels of polychlorobiphenyls in Italian women with endometriosis. Chemosphere 2006;63:1361–7. https://doi.org/10.1016/j.chemosphere.2005.09.022.Search in Google Scholar
81. Trabert, B, Chen, Z, Kannan, K, Peterson, CM, Pollack, AZ, Sun, L, et al. Persistent organic pollutants (POPs) and fibroids: results from the ENDO study. J Expos Sci Environ Epidemiol 2015;25:278–85. https://doi.org/10.1038/jes.2014.31.Search in Google Scholar
82. Lebel, G, Dodin, S, Ayotte, P, Marcoux, S, Ferron, LA, Dewailly, E. Organochlorine exposure and the risk of endometriosis. Fertil Steril 1998;69:221–8. https://doi.org/10.1016/s0015-0282(97)00479-2.Search in Google Scholar
83. Fierens, S, Mairesse, H, Heilier, JF, De Burbure, C, Focant, JF, Eppe, G, et al. Dioxin/polychlorinated biphenyl body burden, diabetes and endometriosis: findings in a population-based study in Belgium. Biomarkers 2003;8:529–34. https://doi.org/10.1080/1354750032000158420.Search in Google Scholar
84. Gerhard, I, Runnebaum, B. The limits of hormone substitution in pollutant exposure and fertility disorders. Zentralbl Gynakol 1992;114:593–602. Available from: https://pubmed.ncbi.nlm.nih.gov/1285483/.Search in Google Scholar
85. Tsukino, H, Hanaoka, T, Sasaki, H, Motoyama, H, Hiroshima, M, Tanaka, T, et al. Associations between serum levels of selected organochlorine compounds and endometriosis in infertile Japanese women. Environ Res 2005;99:118–25. https://doi.org/10.1016/j.envres.2005.04.003.Search in Google Scholar
86. Carpenter, DO, Shen, Y, Nguyen, T, Le, L, Lininger, LL. Incidence of endocrine disease among residents of New York areas of concern. Environ Health Perspect 2001;109(6 Suppl):845–51. https://doi.org/10.2307/3454646.Search in Google Scholar
87. Baranova, H, Canis, M, Ivaschenko, T, Albuisson, E, Bothorishvilli, R, Baranov, V, et al. Possible involvement of arylamine N-acetyltransferase 2, glutathione S-transferases M1 and T1 genes in the development of endometriosis. Mol Hum Reprod 1999;5:636–41. https://doi.org/10.1093/molehr/5.7.636.Search in Google Scholar
88. Cooney, MA, Buck Louis, GM, Hediger, ML, Vexler, A, Kostyniak, PJ. Organochlorine pesticides and endometriosis. Reprod Toxicol (Elmsford, NY) 2010;30:365–9. https://doi.org/10.1016/j.reprotox.2010.05.011.Search in Google Scholar
89. Bernert, JT, Jacob, P, Holiday, DB, Benowitz, NL, Sosnoff, CS, Doig, MV, et al. Interlaboratory comparability of serum cotinine measurements at smoker and nonsmoker concentration levels: a round-robin study. Nicotine Tob Res 2009;11:1458–66. https://doi.org/10.1093/ntr/ntp161.Search in Google Scholar
90. Wójtowicz, AK, Milewicz, T, Gregoraszczuk, EŁ. DDT and its metabolite DDE alter steroid hormone secretion in human term placental explants by regulation of aromatase activity. Toxicol Lett 2007;173:24–30. https://doi.org/10.1016/j.toxlet.2007.06.005.Search in Google Scholar
91. Holloway, AC, Stys, KA, Foster, WG. DDE-induced changes in aromatase activity in endometrial stromal cells in culture. Endocrine 2005;27:45–50. https://doi.org/10.1385/endo:27:1:045.10.1385/ENDO:27:1:045Search in Google Scholar
92. Korrick, SA, Chen, C, Damokosh, AI, Ni, J, Liu, X, Cho, SI, et al. Association of DDT with spontaneous abortion: a case-control study. Ann Epidemiol 2001;11:491–6. https://doi.org/10.1016/s1047-2797(01)00239-3.Search in Google Scholar
93. Weiss, JM, Bauer, O, Blüthgen, A, Ludwig, AK, Vollersen, E, Kaisi, M, et al. Distribution of persistent organochlorine contaminants in infertile patients from Tanzania and Germany. J Assist Reprod Genet 2006;23:393–9. https://doi.org/10.1007/s10815-006-9069-6.Search in Google Scholar
94. Loganathan, BG, Kannan, K. Global organochlorine contamination trends: an overview. Ambio 1994:187–91. Available from: https://www.jstor.org/stable/4314197?seq=1.Search in Google Scholar
Supplementary Material
The online version of this article offers supplementary material (https://doi.org/10.1515/reveh-2020-0046).
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