Increased levels of dioxin-like substances in adipose tissue in patients with deep infiltrating endometriosis

Human Reproduction

Volumn 30, Issue 5, 2015, Pages 1059-1068

  Martinez Zamora M A ^a   Mattioli, L ^b   Parera, J ^b   Abad, E ^b   Coloma, J L ^a   Van Babel, B ^c   Galceran, M T ^a   Balasch, J ^a   Carmona, F ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b INSTITUTE OF ENVIRONMENTAL ASSESSMENT AND WATER RESEARCH   (Spain)

^c ÖREBRO UNIVERSITY   (Sweden)

Author keywords

adipose tissue; deep infiltrating endometriosis; dioxin like substances; dioxins; endometriosis

Indexed keywords

1,2,3,7,8 PENTACHLORODIBENZO PARA DIOXIN; 2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; DIBENZOFURAN DERIVATIVE; DIOXIN; POLYCHLORINATED BIPHENYL DERIVATIVE; UNCLASSIFIED DRUG; BENZOFURAN DERIVATIVE; DIBENZO(1,4)DIOXIN; DIBENZOFURAN; POLYCHLORINATED BIPHENYL;

ADIPOSE TISSUE; ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOMETRIOSIS; FEMALE; HISTOLOGY; HUMAN; HUMAN TISSUE; LAPAROSCOPIC SURGERY; NUCLEAR MAGNETIC RESONANCE IMAGING; OMENTUM; PATHOGENESIS; TRANSVAGINAL ECHOGRAPHY; ADOLESCENT; BODY MASS; CASE CONTROL STUDY; CHEMISTRY; ECHOGRAPHY; LAPAROSCOPY; LIMIT OF DETECTION; METABOLISM; PATHOPHYSIOLOGY; VAGINA; YOUNG ADULT;

ADIPOSE TISSUE; ADOLESCENT; ADULT; BENZOFURANS; BODY MASS INDEX; CASE-CONTROL STUDIES; DIOXINS; ENDOMETRIOSIS; FEMALE; HUMANS; LAPAROSCOPY; LIMIT OF DETECTION; MAGNETIC RESONANCE IMAGING; POLYCHLORINATED BIPHENYLS; ULTRASONOGRAPHY; VAGINA; YOUNG ADULT;

EID: 84929747689     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/dev026     Document Type: Article

References (64)

1. Abad E, Saulo J, Caixach J, Rivera J. Evaluation of a new automated cleanup system for the analysis of polychlorinated dibenzo-p-dioxins and dibenzofurans in environmental samples. J Chromatogr A 2000; 893:383-391.
2. Allam MF, Lucena RA. Breast cancer and PCBs: true or false association?. Eur J Cancer Prev 2001;10:539-540.
3. Arisawa K, Takeda H, Mkasa H. Background exposure to PCDDs/PCDFs/PCBs and its potential health effects: a review of epidemiologic studies. J Med Invest 2005;52:10-21.
4. Aronson KJ, Miller AB, Woolcott CG, Sterns EE, McCready DR, Lickley LA, Fish EB, Hiraki GY, Holloway C, Ross T et al. Breast adipose tissue concentrations of polychlorinated biphenyls and other organochlorines and breast cancer risk. Cancer Epidemiol Biomarkers Prev 2000;9:55-63.
5. Axelrad DA, Goodman S, Woodruf TJ. PCB body burdens in US women of childbearing age 2001-2002: an evaluation of alternate summary metrics of NHANES data. Environ Res 2009;109:368-378.
6. Birnbaum LS. The mechanism of dioxin toxicity: relationship to risk assessment. Environ Health Perspect 1994;102:157-167.
7. Bruner-Tran KL, Osteen KG. Dioxin-like PCBs and endometriosis. Syst Biol Reprod Med 2010;56:132-146.
8. Buck Louis GM, Chen Z, Peterson M, Hediger ML, Croughan MS, Sundaram R, Stanford JB, Varner MW, Fujimoto VY, Giudice LC et al. Persistent lipophilic environmental chemicals and endometriosis: the ENDO study. Environ Health Perspect 2012;120:811-816.
9. Cai LY, Izumi S, Suzuki T, Goya K, Nakamura E, Sugiyama T, Kobayashi H. Dioxins in ascites and serum of women with endometriosis: a pilot study. Hum Reprod 2011;26:117-126.
10. Carmona F, Martinez-Zamora A, Gonzalez X, Gines A, Bunesch L, Balasch J. Does the learning curve of conservative laparoscopic surgery in women with rectovaginal endometriosis impair the recurrence rate?. Fertil Steril 2009;92:868-875.
11. Carmona F, Martinez-Zamora MA, Rabanal A, Martinez-Roman S, Balasch J. Ovarian cystectomy versus laser vaporization in the treatment of ovarian endometriomas: a randomized clinical trial with five-year follow-up. Fertil Steril 2011;96:251-254.
12. Carmona F, Martinez-Zamora A, Bassols ML, Balasch J. Environmental influences on the development of endometriosis. J Endom Pelv Pain Dis 2013;5:49-61.
13. Caspersen IH, Knutsen HK, Brantsaeter AL, Haugen M, Alexander J, Meltzer HM, Kvalem HE. Dietary exposure to dioxins and PCBs in a large cohort of pregnant women: results from the Norwegian Mother and Child Cohort Study (MoBa). Environ Int 2013;59: 398-407.
14. Chapron C, Dubuisson JB, FritelX, Fernandez B, Poncelet C, Beguin S, Pinelli L. Operative management of deep endometriosis infiltrating the uterosacral ligaments. J Am Assoc Gynecol Laparosc 1999; 6:31-37.
15. Cornillie FJ, Oosterlynck D, Lauweryns JM, Konincks PR. Deeply infiltrating pelvic endometriosis: histology and clinical significance. Fertil Steril 1990; 53:978-983.
16. Daya S. Methodological issues in infertility research. Best Pract Res Clin Obstet Gynaecol 2006;20:779-797.
17. Dinse GE, Jusko TA, HO LA, Annam K, Graubard BI, Hertz-Picciotto I, Miller FW, Gillespie BW, Weinberg CR. Accommodating measurements below a limit of detection: a novel application of cox regression. Am J Epidemiol 2014;179:10181024.
18. Fauconnier A, Chapron C, Dubuisson JB, Vieira M, Dousset B, Breart G. Relation between pain symptoms and the anatomic location of deep infiltrating endometriosis. Fertil Steril 2002;78:719-726.
19. Fauconnier A, Chapron C. Endometriosis and pelvic pain: epidemiological evidence of the relationship and implications. Hum Reprod Update 2005; 11:595-606.
20. Fierens S, Mairesse H, Heilier JF, De Burbure C, Focant JF, Eppe G, DePauwE, Bernard A. Dioxin/polychlorinated biphenyl body burden, diabetes and endometriosis: findings in a population-based study in Belgium. Biomarkers 2003;8:529-534.
21. Gennings C, Sabo R, Carney E. Identifying subsets of complex mixtures most associated with complex diseases: polychlorinated biphenyls and endometriosis as a case study. Epidemiology 2010;21:S77-S84.
22. Guo SW, Ximsa P, Kyama CM, Mihalyi A, Fulop V, Othman EER, D'Hooghe TM. Reassessing the evidence for the link between dioxin and endometriosis: from molecular biology to clinical epidemiology. Mol Hum Reprod 2009;15:609-624.
23. Guyatt GH, Mills EJ, Elbourne D. In the era of systematic reviews, does the size of an individual trial still matter?. PLoS Med 2008;5:e4.
24. Heilier J, HA AT, Lison D, Donnez J, Tonglet R, Nackers F. Increased serum polychlorobiphenyl levels in Belgian women with adenomyotic nodules of the rectovaginal septum. Fertil Steril 2004;81:456-458.
25. Heilier JF, Nackers F, Verougstraerte V, Tonglet R, LisonD, Donnez J. Increased dioxin-like compounds in the serum of women with peritoneal endometriosis and deep endometriotic (adenomyotic) nodules. Fertil Steril 2005;84:305-312.
26. Heilier JF, Donnez J, Lison D. Organochlorines and endometriosis: a mini-review. Chemosphere 2008;71:203-210.
27. Hoffman CS, Small CM, Blanck HM, Tolbert P, Rubin C, Marcus M. Endometriosis among women exposed to polybrominated biphenyls. Ann Epidemiol 2007;17:503-510.
28. Huff JE, SalmonAG, HooperNK, Zeise L. Long-Termcarcinogenesis studieson 2, 3, 7, 8-Tetrachlorodibenzo-p-dioxin and hexachlorodibenzo-p-dioxins. Cell Biol Toxicol 1991;7:67-94.
29. Humblet O, Williams PL, Korrick SA, Sergeyev O, Emond C, Birnbaum LS, Burns JS, Altshul L, Patterson DG, Turner WE et al. Predictors of serum dioxin, furan and PCB concentrations among women from Chapaevsk, Russia. Environ Sci Technol 2010;44:5633-5640.
30. IARC monographs on the evaluation of carcinogenic risks to humans. Volume 69-Polychlorinated Dibenzo-Para-Dioxins and Polychlorinated Dibenzofurans. World Health Organization. International Agency for Research and Cancer, 1997.
31. Kitamura K, NagaoM, YamadaT, Sunaga M, Hata J, Watanae S. Dioxins in bile in relation to those in the human liver and blood. J Toxicol Sci 2001; 26:327-336.
32. Kitamura K, Takazawa Y, Takei Y, Zhou X, Hashimoto S, Choi J, Ito H, Morita M. Development of a method for dioxin analysis of small samples with reduced risk of volatilization. Anal Chem 2005;77:1727-1733.
33. Kogevinas M. Human health effects of dioxins: cancer, reproductive and endocrine system effects. Hum Reprod Update 2001;7:331-339.
34. Koppen G, Covaci A, VanCleuvenbergen R, Schepens P, WinnekeG, NelenV, van Larebeke N, Vlietinck R, Schoeters G. Persistent organochlorine pollutants in human serum of 56-65 years old women in the Flanders Environmental and Health Study (FLEHS). Part 1: concentrations and regional differences. Chemosphere 2002;48:811-825.
35. LebelG, Dodin S, Ayotte P, Marcoux S, Ferron LA, Dewailly E.Organochlorine exposure and the risk of endometriosis. Fertil Steril 1998;69:221-228.
36. Louis GM, Weiner JM, Whitcomb BW, Sperrazza R, Schisterman EF, Lobdell DT, Crickard K, Greizerstein H, Kostyniak PJ. Environmental PCB exposure and risk of endometriosis. Hum Reprod 2005;20:279-285.
37. Mayani A, Barel S, Soback S, Almagor M. Dioxin concentrations in women with endometriosis. Hum Reprod 1997;12:373-375.
38. Mimura J, Fujii-Kuriyama Y. Functional role of AhR in the expression of toxic effects by TCDD. Biochim Biophys Acta 2003;1619:263-268.
39. Nelson EA, Hui LL, WongTW, Hedley AJ. Demographic and lifestyle factors associated with dioxin-like activity (CALUX-TEQ) in human breast milk in Hong Kong. Environ Sci Technol 2005;40:1432-1438.
40. Niskar AS, Needham LL, Rubin C, Turner WE, Martin CA, Patterson DG Jr, Hasty L, Wong LY, Marcus M. Serum dioxins, polychlorinated biphenyls, and endometriosis: a case-control study in Atlanta. Chemosphere 2009; 74:944-999.
41. Nisolle M, Donnez J. Peritoneal endometriosis, ovarian endometriosis, and adenomyotic nodules of the rectovaginal septum are three different entities. Fertil Steril 1997;68:585-596.
42. Park H, Hertz-Picciotto I, Sovcikova E, Kocan A, Drobna B, Trnovec T. Neurodevelopmental toxicity of prenatal polychlorinated biphenyls (PCBs) by chemical structure and activity: a birth cohort study. Environ Health 2010;9:1-13.
43. Pauwels A, Schepens PJ, d'Hooge T, Delbeke L, Dhont M, Brouwer A, Weyler J. The risk of endometriosis and exposure to dioxins and polychlorinated biphenyls: a case-control study of infertile women. Hum Reprod 2001;16:2050-2055.
44. Porpora MG, Ingelido AM, di Domenico A, Ferro A, Crobu M, Pallante D, Cardelli M, Cosmi EV, De Felip E. Increased levels of polychlorobiphenyls in Italian women with endometriosis. Chemosphere 2006;63:1361-1367.
45. Porpora MG, Medda E, Abballe A, Bolli S, De Angelis I, di Domenico A, Ferro A, Ingelido AM, Maggi A, Panici PB et al. Endometriosis and organochlorinated environmental pollutants: a case-control study on Italian women of reproductive age. Environ Health Perspect 2009; 117:1070-1075.
46. Quintana PJ, Delfino RJ, Korrick S, Ziogas A, Kutz FW, Jones EL, Laden F, Garshick E. Adipose tissue levels of organochlorine pesticides and polychlorinated biphenyls and risk of non-Hodgkin's lymphoma. Environ Health Perspect 2004;112:854-861.
47. 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;85:775-779.
48. Rier S, Foster WG. Environmental dioxins and endometriosis. Semin Reprod Med 2003;21:145-153.
49. Ro hring B, du Prel JB, Wachtlin D, Kwiecien R, Blettner M. Sample size calculation in clinical trials. Btsch Arztebl Int 2010;107:552-556.
50. 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.
51. Sasamoto T, Horii S, Ibe A, Takada N, Shirota K. Concentration changes of PCDDs, PCDFs, and dioxin-like PCBs in human breast milk samples as shown by a follow-up survey. Chemosphere 2006;64:642-649.
52. Simsa P, Mihalyi A, Schoeters G, Koppen G, Kyama CM, Den Hond EM, Fulop V, D'Hooghe TM. Increased exposure to dioxin-like compounds is associated with endometriosis in a case-control study in women. Reprod Biomed Online 2010;20:681-688.
53. Trabert B, De Roos AJ, Schwartz SM, Peters U, Scholes D, Barr DB, Holt VL. Non-dioxin-like polychlorinated biphenyls and risk of endometriosis. Environ Health Perspect 2010;118:1280-1285.
54. Treloar SA, Wicks J, Nyholt DR, Montgomery GW, Bahlo M, Smith V, Dawson G, Mackay IJ, Weeks DE, Bennett ST et al. Genomewide linkage study in 1176 affected sister pair families identifies a significant susceptibility locus for endometriosis on chromosome 10q26. Am J Hum Genet 2005;77:365-376.
55. Tsukino H, Hanaoka T, Sasaki H, Motoyama H, Hiroshima M, Tanaka T, Kabuto M, Niskar AS, Rubin C, Patterson DG Jr et al. Associations between serum levels of selected organochlorine compounds and endometriosis in infertile Japanese women. Environ Res 2005;99: 118-125.
56. Uemura H, Arisawa K, Hikoshi M, Satoh H, Sumiyoshi Y, Morinaga K, Kodama K, Suzuki T, Nagai M, Suzuki T. PCDDs/PCDFs and dioxin-like PCBs: recent body burden levels and their determinants among general inhabitants in Japan. Chemosphere 2008;73:307.
57. Upson K, De roos AJ, Thompson ML, Sathyanarayana S, Scholes D, Boyd Barr D, Holt VL. Organochlorine pesticides and risk of endometriosis: findings from a population-based case-control study. Environ Heath Perspect 2013;121:1319-1324.
58. Upson K, Sathyanarayana S, De Roos AJ, Thompson ML, Scholes D, Dills R, Holt VL. Phthalates and risk of endometriosis. Environ Res 2013; 126:91-97.
59. 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;29:2457-2464.
60. Van den Berg M, Birnbaum L, Denison M, De Vito M, FarlandW, Feeley M, Fiedler H, Hakansson H, Hanberg A, Haws L et al. The 2005World Health Organization reevaluation of human and mammalian toxic equivalency factors for dioxins and dioxin-like compounds. Toxicol Sci 2006; 93:223-241.
61. Varol N, Maher P, Healey M, Woods R, Wood C, Hill D, Lolatgis N, Tsaltas J. Rectal surgery for endometriosis-should we be aggressive?. J Am Assoc Gynecol Laparosc 2003;10:182-189.
62. Vercellini P, Crosignani PG, Abbiati A, Somigliana E, Vigano P, Fedele L. The effect of surgery for symptomatic endometriosis: the other side of the story. Hum Reprod Update 2009;15:177-188.
63. Whitcomb BW, Shisterman EF, Buck GM, Weiner JM, Greixerstein H, Kostyniak PJ. Relative concentrations of organochlorines in adipose tissue and serum among reproductive age women. Environ Toxiol Pharmacol 2005;19:203-213.
64. Zubero MB, Ibarluzea JM, Aurrekoetxea JJ, Rivera J, Parera J, Abad E, Goni F, Lopez R, Etxeandia A, Rodriguez C et al. Serum levels of polychlorinated dibenzodioxins and dibenzofurans and PCBs in the general population living near an urban waste treatment plant in Biscay, Basque Country. Chemosphere 2009;76:784-791.