Reproductive BioMedicine Online
Volume 20, Issue 5 , Pages 681-688 , May 2010

Increased exposure to dioxin-like compounds is associated with endometriosis in a case–control study in women

  • Peter Simsa

      Affiliations

    • Leuven University Fertility Center, Department of Obstetrics and Gynaecology, University Hospital Gasthuisberg, Leuven B-3000, Belgium
    • Department of Obstetrics and Gynaecology, National Institute of Health, Budapest 1139, Hungary
    • ,
  • Attila Mihalyi

      Affiliations

    • Leuven University Fertility Center, Department of Obstetrics and Gynaecology, University Hospital Gasthuisberg, Leuven B-3000, Belgium
    • ,
  • Greet Schoeters

      Affiliations

    • Flemish Institute of Technological Research (VITO), Environmental Toxicology, Mol, Belgium
    • ,
  • Gudrun Koppen

      Affiliations

    • Flemish Institute of Technological Research (VITO), Environmental Toxicology, Mol, Belgium
    • ,
  • Cleophas M. Kyama

      Affiliations

    • Leuven University Fertility Center, Department of Obstetrics and Gynaecology, University Hospital Gasthuisberg, Leuven B-3000, Belgium
    • Division of Reproduction, Institute of Primate Research, PO Box 24481, Karen, Nairobi, Kenya
    • ,
  • Elly M. Den Hond

      Affiliations

    • Flemish Institute of Technological Research (VITO), Environmental Toxicology, Mol, Belgium
    • ,
  • Vilmos Fülöp

      Affiliations

    • Department of Obstetrics and Gynaecology, National Institute of Health, Budapest 1139, Hungary
    • ,
  • Thomas M. D’Hooghe

      Affiliations

    • Leuven University Fertility Center, Department of Obstetrics and Gynaecology, University Hospital Gasthuisberg, Leuven B-3000, Belgium
    • Division of Reproduction, Institute of Primate Research, PO Box 24481, Karen, Nairobi, Kenya
    • Corresponding Author InformationCorresponding author.

Received 6 July 2009 ,Revised 10 September 2009 ,Accepted 17 December 2009.

References 

  1. AFS Revised American Fertility Society classification of endometriosis, 1985. Fertil. Steril. 43, 351–352.
  2. Agency for Toxic Substances and Disease Registry–ATSDR, Comprehensive Environmental Response, Compensation, and Liability Act–CERCLA 2007. Available from: http://www.atsdr.cdc.gov/cercla/ Retrieved August 1, 2008.
  3. Ahmed S, Shibazaki M, Takeuchi T, et al. Protein kinase Ctheta activity is involved in the 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced signal transduction pathway leading to apoptosis in L-MAT, a human lymphoblastic T-cell line. FEBS J. 2005;272:903–915
  4. Attar E, Bulun SE. Aromatase and other steroidogenic genes in endometriosis: translational aspects. Hum. Reprod. Update. 2006;12:49–56
  5. Birnbaum LS, Cummings AM. Dioxins and endometriosis: a plausible hypothesis. Environ. Health Perspect. 2002;110:15–21
  6. Bischoff F, Simpson JL. Genetic basis of endometriosis. Ann. NY Acad. Sci. 2004;1034:284–299
  7. Bock KW, Kohle C. Ah receptor: dioxin-mediated toxic responses as hints to deregulated physiologic functions. Biochem. Pharmacol. 2006;72:393–404
  8. Boyd, J.A., Clark, G.C., Walmer, D.K., et al., 1995. Endometriosis and environment: biomarkers of toxin exposure. In: Conference on Endometriosis 2000 15–17, May 1995, Bethesda, MD.
  9. Carter JE. Combined hysteroscopic and laparoscopic findings in patients with chronic pelvic pain. J. Am. Assoc. Gynecol. 1994;2:43–47
  10. Clark GC, Blank JA, Germolec DR, et al. 2,3,7,8-Tetrachlorodibenzo-p-dioxin stimulation of tyrosine phosphorylation in B lymphocytes: potential role in immunosuppression. Mol. Pharmacol. 1991;39:495–501
  11. Colles A, Koppen G, Hanot V, et al. Fourth WHO-coordinated survey of human milk for persistent organic pollutants (POPs): Belgian results. Chemosphere. 2008;73:907–917
  12. D’Hooghe TM, Mihalyi AM, Simsa P, et al. Why we need a noninvasive diagnostic test for minimal to mild endometriosis with a high sensitivity. Gynecol. Obstet. Invest. 2006;63:136–138
  13. De Felip E, Porpora MG, di Domenico A, et al. Dioxin-like compounds and endometriosis: a study on Italian and Belgian women of reproductive age. Toxicol. Lett. 2004;150:203–209
  14. Eskenazi B, Mocarelli P, Warner M, et al. Serum dioxin concentrations and endometriosis: a cohort study in Seveso, Italy. Environ. Health Perspect. 2002;110:629–634
  15. Fierens S, Mairesse H, Heilier JF, et al. Dioxin/polychlorinated biphenyl body burden, diabetes and endometriosis: findings in a population-based study in Belgium. Biomarkers. 2003;8:529–534
  16. Foster WG. Endocrine toxicants including 2,3,7,8-terachlorodibenzo-p-dioxin (TCDD) and dioxin-like chemicals and endometriosis: is there a link?. J. Toxicol. Environ. Health B Crit. Rev. 2008;11:177–187
  17. Gerhard I, Runnebaum B. Grenzen der Hormonsubstitutio bei Schadstoffbelastung und Fertilitätsstorungen. Zentralblatt Gynäkol. 1992;114:593–602(in German)
  18. Guo SW. The link between exposure to dioxin and endometriosis: a critical reappraisal of primate data. Gynecol. Obstet. Invest. 2004;57:157–173
  19. Halme J, Hammond MG, Hulka JF, et al. Retrograde menstruation in healthy women and in patients with endometriosis. Obstet. Gynecol. 1984;64:151–154
  20. Hays SM, Aylward LL. Dioxin risks in perspective: past, present, and future. Regul. Toxicol. Pharmacol. 2003;37:202–217
  21. Heilier JF, Donnez J, Lison D. Organochlorines and endometriosis: a mini-review. Chemosphere. 2008;71:203–210
  22. 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
  23. Jusko TA, Koepsell TD, Baker RJ, et al. Maternal DDT exposures in relation to fetal and 5-year growth. Epidemiology. 2006;17:692–700
  24. Kardinaal AF, Kok FJ, Kohlmeier L, et al. Association between toenail selenium and risk of acute myocardial infarction in European men: The EURAMIC Study. Am. J. Epidemiol. 1997;145:373–379
  25. Koninckx PR. The physiopathology of endometriosis: pollution and dioxin. Gynecol. Obstet. Invest. 1999;47:47–49
  26. Lawrence BP, Vorderstrasse BA. Activation of the aryl hydrocarbon receptor diminishes the memory response to homotypic influenza virus infection but does not impair host resistance. Toxicol. Sci. 2004;79:304–314
  27. Lebel G, Dodin S, Ayotte P, et al. Organochlorine exposure and the risk of endometriosis. Fertil. Steril. 1998;69:221–228
  28. Lee DH, Lee IK, Jin SH, et al. Association between serum concentrations of persistent organic pollutants and insulin resistance among nondiabetic adults: results from the National Health and Nutrition Examination Survey 1999–2002. Diabetes Care. 2007;30:622–628
  29. Levin M, Morsey B, Mori C, et al. Non-coplanar PCB-mediated modulation of human leukocyte phagocytosis: a new mechanism for immunotoxicity. J. Toxicol. Environ. Health. 2005;68:1977–1993
  30. Liem AKD, Ahlborg UG, Beck H, et al. Levels of PCBs, PCDDs and PCDFs in human milk. Results from the second round of a WHO-coordinated exposure study. Organohalogen Compd. 1996;30:269–273
  31. Mayani A, Barel S, Soback S, et al. Dioxin concentrations in women with endometriosis. Hum. Reprod. 1997;2:373–375
  32. Mihalyi A, Mutinda KC, Simsa P, et al. Role of immunologic and inflammatory factors in the development of endometriosis: indications for treatment strategies. Therapy. 2005;2:623–639
  33. Mimura J, Fujii-Kuriyama Y. Functional role of AhR in the expression of toxic effects by TCDD. Biochim. Biophys. Acta. 2003;1619:263–268
  34. Navas-Acien A, Silbergeld EK, Sharrett R, et al. Metals in urine and peripheral arterial disease. Environ. Health Perspect. 2005;113:164–169
  35. Neubert R, Jacob-Muller U, Helge H, et al. Polyhalogenated dibenzo-p-dioxins and dibenzofurans and the immune system. 2. In vitro effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on lymphocytes of venous blood from man and a non-human primate (Callithrix jacchus). Arch. Toxicol. 1991;65:213–219
  36. Oh E, Lee E, Im H, et al. Evaluation of immuno- and reproductive toxicities and association between immunotoxicological and genotoxicological parameters in waste incineration workers. Toxicology. 2005;210:65–80
  37. Ohtake F, Takeyama K, Matsumoto T, et al. Modulation of oestrogen receptor signalling by association with the activated dioxin receptor. Nature. 2003;423:545–550
  38. Pauwels A, Shepens PJC, D’Hooghe T, et al. The risk of endometriosis and exposure to dioxins and polychlorinated biphenyls: a case–control study of infertile women. Hum. Reprod. 2001;16:2050–2055
  39. Puebla-Osorio N, Ramos KS, Falahatpisheh MH, et al. 2,3,7,8-Tetrachlorodibenzo-p-dioxin elicits aryl hydrocarbon receptor-mediated apoptosis in the avian DT40 pre-B-cell line through activation of caspases 9 and 3. Comp. Biochem. Physiol. Toxicol. Pharmacol. 2004;138:461–468
  40. Rier S, Foster WG. Environmental dioxins and endometriosis. Toxicol. Sci. 2002;70:161–170
  41. Rier SE, Martin DC, Bowman RE, et al. Endometriosis in rhesus monkeys (Macaca mulatta) following chronic exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Fundam. Appl. Toxicol. 1993;21:433–441
  42. Sampson JA. Peritoneal endometriosis due to menstrual dissemination of endometrial tissue into the peritoneal cavity. Am. J. Obstet. Gynecol. 1927;14:422–469
  43. Schecter A, Birnbaum L, Ryan JJ, et al. Dioxins: an overview. Environ. Res. 2006;101:419–428
  44. Tsukino H, Hanaoka T, Sasaki H, et al. Associations between serum levels of selected organochlorine compounds and endometriosis in infertile Japanese women. Environ. Res. 2005;99:118–121
  45. Van Cleuvenbergen R, Wevers M, Schoeters J, et al. Dioxins (PCDDs and PCDFs) in human milk from Flanders, Belgium: concentration levels and congener profile. Organohalogen Compd. 1994;20:215–220
  46. Van Leeuwen FXR, Malisch R. Results of the third round of the WHO-coordinated exposure study on the levels of PCBs, PCDDs and PCDFs in human milk. Organohalogen Compd. 2002;56:311–315
  47. Van Wouwe N, Debacker N, Sasse A, et al. Application of the CALUX bioassay for epidemiological study: analyses of Belgian human plasma. Organohalogen Compd. 2004;66:642–648
  48. Vessey MP, Villard-Mackintosh L, Painter R. Epidemiology of endometriosis in women attending family planning clinics. Brit. Med. J. 1993;306:182–184
  49. Wheeler JM. Epidemiology of endometriosis-associated infertility. J. Reprod. Med. 1989;34:41–46
  50. Wheeler JM. Epidemiology and prevalence of endometriosis. Infertil. Reprod. Med. Clin. North Am. 1992;3:545–549

 Peter Simsa graduated in 1998 and then did research in the area of breast cancer and B cell infiltration at Semmelweis University, Hungary. From 2004 to 2007, he worked as an international research scholar on toxicological aspects of endometriosis under supervision of Professor Dr Thomas D’Hooghe (Leuven University, Belgium). He is currently finalizing his PhD thesis in Hungary and studying immunological aspects of recurrent spontaneous abortion.

PII: S1472-6483(10)00054-4

doi: 10.1016/j.rbmo.2010.01.018

Reproductive BioMedicine Online
Volume 20, Issue 5 , Pages 681-688 , May 2010

Article Tools

* Image Usage & Resolution