Endometriosis and Oxidative Stress

  • Lucky H. Sekhon
  • Ashok AgarwalEmail author
Part of the Oxidative Stress in Applied Basic Research and Clinical Practice book series (OXISTRESS)


Endometriosis is a chronic gynecologic disease process with multifactorial etiology. Increased oxidative stress, a result of increased production of free radicals or depletion of the body’s endogenous antioxidant defense, has been implicated in its pathogenesis. Oxidative stress is thought to promote angiogenesis and the growth and proliferation of endometriotic implants. Oxidative stress in the reproductive tract microenvironment is known to negatively affect sperm count and quality and may also arrest fertilized egg division leading to embryo death. Increased DNA damage in sperm, oocytes, and resultant embryos may account for the increase in miscarriages and fertilization and implantation failures seen in patients with endometriosis. The evidence linking endometriosis and infertility to endogenous pro-oxidant imbalance provides a rationale for the empiric use of antioxidant therapy. Vitamin C and E deficiency has been demonstrated in women with endometriosis. Observational and randomized controlled studies have shown vitamin C and E combination therapy to decrease markers of oxidative stress.


Endometriosis  Oxidative stress OS induced infertility  Antioxidant treatment  Curcumin  Melatonin  Pentoxifylline 


  1. 1.
    Snesky TE, Liu DT (1980) Endometriosis: associations with menorrhagia, infertility, and oral contraceptives. Int J Gynaecol Obstet 17:573–576Google Scholar
  2. 2.
    Cramer DW (1987) Epidemiology of endometriosis in adolescents. In: Wilson EA (ed) Endometriosis, vol 1. Alan Liss, New York, pp 5–8Google Scholar
  3. 3.
    Giudice L, Kao L (2004) Endometriosis. Lancet 364:1789–1799PubMedCrossRefGoogle Scholar
  4. 4.
    Koninckx PR (1999) The physiopathology of endometriosis: pollution and dioxin. Gynecol Obstet Invest 47:47–49PubMedCrossRefGoogle Scholar
  5. 5.
    Donnez J, Chantraine F, Nisolle M (2002) The efficacy of medical and surgical treatment of endometriosis-associated infertility: arguments in favour of a medico-surgical approach. Hum Reprod Update 8:89–94PubMedCrossRefGoogle Scholar
  6. 6.
    Nisolle M, Donnez J (1997) Peritoneal endometriosis, ovarian endometriosis, and adenomyotic nodules of the rectovaginal septum are three different entities. Fertil Steril 68:585–596PubMedCrossRefGoogle Scholar
  7. 7.
    Van Langendonckt A, Casanas-Roux F, Dolmans MM, Donnez J (2002) Potential involvement of hemoglobin and heme in the pathogenesis of peritoneal endometriosis. Fertil Steril 77:561–570PubMedCrossRefGoogle Scholar
  8. 8.
    Heilier JF, Donnez J, Lison D (2008) Organochlorines and endometriosis: a mini-review. Chemosphere 71:203–210PubMedCrossRefGoogle Scholar
  9. 9.
    Halme J, Hammond MG, Hulka JF, Raj SG, Talbert LM (1984) Retrograde menstruation in healthy women and in patients with endometriosis. Obstet Gynecol 64:151–154PubMedGoogle Scholar
  10. 10.
    Nap AW, Groothuis PG, Demir AY, Evers JL, Dunselman GA (2004) Pathogenesis of endometriosis. Best Pract Res Clin Obstet Gynaecol 18:233–244PubMedCrossRefGoogle Scholar
  11. 11.
    Van Langendonckt A, Casanas-Roux F, Donnez J (2002) Iron overload in the peritoneal cavity of women with pelvic endometriosis. Fertil Steril 78:712–718PubMedCrossRefGoogle Scholar
  12. 12.
    Yamaguchi K, Mandai M, Toyokuni S, Hamanishi J, Higuchi T, Takakura K, Fujii S (2008) Contents of endometriotic cysts, especially the high concentration of free iron, are a possible cause of carcinogenesis in the cysts through the iron-induced persistent oxidative stress. Hum Cancer Biol 14(1):32–40Google Scholar
  13. 13.
    Templeton DM, Liu Y (2003) Genetic regulation of cell function in response to iron overload or chelation. Biochim Biophys Acta 1619:113–124PubMedCrossRefGoogle Scholar
  14. 14.
    Lachapelle MH, Hemmings R, Roy DC, Falcone T, Miron P (1996) Flow cytometric evaluation of leukocyte subpopulations in the follicular fluids of infertile patients. Fertil Steril 65:1135–1140PubMedGoogle Scholar
  15. 15.
    Seli E, Arici A (2003) Endometriosis: interaction of immune and endocrine systems. Semin Reprod Med 21:135–144PubMedCrossRefGoogle Scholar
  16. 16.
    Pellicer A, Albert C, Mercader A, Bonilla-Musoles F, Remohi J, Simon C (1998) The follicular and endocrine environment in women with endometriosis: local and systemic cytokine production. Fertil Steril 70:425–431PubMedCrossRefGoogle Scholar
  17. 17.
    Garrido N, Navarro J, Remohi J, Simon C, Pellicer A (2000) Follicular hormonal environment and embryo quality in women with endometriosis. Hum Reprod Update 6:67–74PubMedCrossRefGoogle Scholar
  18. 18.
    Wunder DM, Mueller MD, Birkhauser MH, Bersinger NA (2006) Increased ENA-78 in the follicular fluid of patients with endometriosis. Acta Obstet Gynecol Scand 85:336–342PubMedCrossRefGoogle Scholar
  19. 19.
    Bedaiwy MA, Falcone T, Sharma RK, Goldberg JM, Attaran M, Nelson DR, Agarwal A (2002) Prediction of endometriosis with serum and peritoneal fluid markers: a prospective controlled trial. Hum Reprod 17:426–431PubMedCrossRefGoogle Scholar
  20. 20.
    Darai E, Detchev R, Hugol D, Quang NT (2003) Serum and cyst fluid levels of interleukin (IL) -6, IL-8 and tumour necrosis factor-alpha in women with endometriomas and benign and malignant cystic ovarian tumours. Hum Reprod 18:1681–1685PubMedCrossRefGoogle Scholar
  21. 21.
    Ulukus M, Ulukus EC, Seval Y, Zheng W, Arici A (2005) Expression of interleukin-8 receptors in endometriosis. Hum Reprod 20:794–801PubMedCrossRefGoogle Scholar
  22. 22.
    Agarwal A, Gupta S (2005) Role of reactive oxygen species in female reproduction. Part I. Oxidative stress: a general overview. Women Health 1:21–25Google Scholar
  23. 23.
    de Lamirande E, Gagnon C (1995) Impact of reactive oxygen species on spermatozoa: a balancing act between beneficial and detrimental effects. Hum Reprod 10:15–21PubMedGoogle Scholar
  24. 24.
    Alul RH, Wood M, Longo J, Marcotte AL, Campione AL, Moore MK, Lynch SM (2003) Vitamin C protects low-density lipoproteins from homocysteine-mediated oxidation. Free Radic Biol Med 34(7):881–891PubMedCrossRefGoogle Scholar
  25. 25.
    Olek RA, Ziolkowski W, Kaczor JJ, Greci L, Popinigis J, Antosiewicz J (2004) Antioxidant activity of NADH and its analogue––an in vivo study. J Biochem Mol Biol 37:416–421PubMedCrossRefGoogle Scholar
  26. 26.
    Reubinoff BE, Har-El R, Kitrossky N, Friedler S, Levi R, Lewin A, Chevion M (1996) Increased levels of redox-active iron in follicular fluid: a possible cause of free radical mediated infertility in beta-thalassemia major. Am J Obstet Gynecol 174(3):914–918PubMedCrossRefGoogle Scholar
  27. 27.
    Arumugam K, Yip YC (1995) De novo formation of adhesions in endometriosis: the role of iron and free radical reactions. Fertil Steril 64(1):62–64PubMedGoogle Scholar
  28. 28.
    Murphy AA, Palinski W, Rankin S, Morales AJ, Parthasarathy S (1998) Evidence for oxidatively modified lipid-protein complexes in endometrium and endometriosis. Fertil Steril 69(6):1092–1094PubMedCrossRefGoogle Scholar
  29. 29.
    Donnez J, Van Langendonckt A, Casanas-Roux F et al (2002) Current thinking on the pathogenesis of endometriosis. Gynecol Obstet Invest 54(Suppl 1):52–58. Discussion 9–62Google Scholar
  30. 30.
    Foyouzi N, Berkkanoglu M, Arici A, Kwintkiewicz J, Izquierdo D, Duleba AJ (2004) Effects of oxidants and antioxidants on proliferation of endometrial stromal cells. Fertil Steril 82(3):1019–1022PubMedCrossRefGoogle Scholar
  31. 31.
    Park JK, Song M, Dominguez CE, Walter MF, Santanam N, Parthasarathy S, Murphy AA (2006) Glycodelin mediates the increase in vascular endothelial growth factor in response to oxidative stress in the endometrium. Am J Obstet Gynecol 195(6):1772–1777PubMedCrossRefGoogle Scholar
  32. 32.
    Wu Y, Kajdacsy-Balla A, Strawn E, Basir Z, Halverson G, Jailwala P, Wang Y, Wang X, Ghosh S, Guo SW (2006) Transcriptional characterizations of differences between eutopic and ectopic endometrium. Endocrinology 147(1):232–246PubMedCrossRefGoogle Scholar
  33. 33.
    Seo SK, Yang HI, Lee KE, Kim HY, Cho S, Choi YS, Lee BS (2010) The roles of thioredoxin and thioredoxin-binding protein-2 in endometriosis. Hum Reprod 25(5):1251–1258PubMedCrossRefGoogle Scholar
  34. 34.
    Zeller JM, Henig I, Radwanska E, Dmowski WP (1987) Enhancement of human monocyte and peritoneal macrophage chemiluminescence activities in women with endometriosis. Am J Reprod Immunol Microbiol 13:78–82PubMedGoogle Scholar
  35. 35.
    Ota H, Igarashi S, Tanaka T (2001) Xanthine oxidase in eutopic and ectopic endometrium in endometriosis and adenomyosis. Fertil Steril 75:785–790PubMedCrossRefGoogle Scholar
  36. 36.
    Saito H, Seino T, Kaneko T, Nakahara K, Toya M, Kurachi H (2002) Endometriosis and oocyte quality. Gynecol Obstet Invest 53(1):46–51PubMedCrossRefGoogle Scholar
  37. 37.
    Szczepanska M, Kozlik J, Skrzypczak J, Mikolajczyk M (2003) Oxidative stress may be a piece in the endometriosis puzzle. Fertil Steril 79:1288–1293PubMedCrossRefGoogle Scholar
  38. 38.
    Gupta S, Agarwal A, Krajcir N, Alvarez JG (2006) Role of oxidative stress in endometriosis. Reprod Biomed Online 13(1):126–134PubMedCrossRefGoogle Scholar
  39. 39.
    Polak G, Koziol-Montewka M, Gogacz M, Blaszkowska I, Kotarski J (2001) Total antioxidant status of peritoneal fluid in infertile women. Eur J Obstet Gynecol Reprod Biol 94(2):261–263PubMedCrossRefGoogle Scholar
  40. 40.
    Dong M, Shi Y, Cheng Q, Hao M (2001) Increased nitric oxide in peritoneal fluid from women with idiopathic infertility and endometriosis. J Reprod Med 46:887–891PubMedGoogle Scholar
  41. 41.
    Lambrinoudaki IV, Augoulea A, Christodoulakos GE, Economou EV, Kaparos G, Kontoravdis A, Papadias C, Creatsas G (2009) Measurable serum markers of oxidative stress response in women with endometriosis. Fertil Steril 91(1):46–50PubMedCrossRefGoogle Scholar
  42. 42.
    Wang Y, Sharma RK, Falcone T, Goldberg J, Agarwal A (1997) Importance of reactive oxygen species in the peritoneal fluid of women with endometriosis or idiopathic infertility. Fertil Steril 68:826–830PubMedCrossRefGoogle Scholar
  43. 43.
    Ho HN, Wu MY, Chen SU, Chao KH, Chen CD, Yang YS (1997) Total antioxidant status and nitric oxide do not increase in peritoneal fluids from women with endometriosis. Hum Reprod 12:2810–2815PubMedCrossRefGoogle Scholar
  44. 44.
    Ota H, Igarashi S, Hatazawa J, Tanaka T (1999) Endometriosis and free radicals. Gynecol Obstet Invest 48:29–35PubMedCrossRefGoogle Scholar
  45. 45.
    Murphy AA, Santanam N, Morales AJ, Parthasarathy S (1998) Lysophosphatidyl choline, a chemotactic factor for monocytes/T-lymphocytes is elevated in endometriosis. J Clin Endocrinol Metabol 83:2110–2113CrossRefGoogle Scholar
  46. 46.
    Ota H, Igarashi S, Hatazawa J, Tanaka T (1999) Immunohistochemical assessment of superoxide dismutase expression in the endometrium in endometriosis and adenomyosis. Fertil Steril 72:129–134PubMedCrossRefGoogle Scholar
  47. 47.
    Ota H, Igarashi S, Kato N, Tanaka T (2000) Aberrant expression of glutathione peroxidase in eutopic and ectopic endometrium in endometriosis and adenomyosis. Fertil Steril 74:313–318PubMedCrossRefGoogle Scholar
  48. 48.
    Jackson L, Schisterman E, Day-Rao R, Browne R, Armstrong D (2005) Oxidative stress and endometriosis. Hum Reprod 20:2014–2020PubMedCrossRefGoogle Scholar
  49. 49.
    Portz DM, Elkins TE, White R, Warren J, Adadevoh S, Randolph J (1991) Oxygen free radicals and pelvic adhesion formation: I. Blocking oxygen free radical toxicity to prevent adhesion formation in an endometriosis model. Int J Fertil 36:39–42PubMedGoogle Scholar
  50. 50.
    ASRM (2004) Endometriosis and infertility. Fertil Steril 82(1):S40–S45Google Scholar
  51. 51.
    Mahutte NG, Arici A (2002) New advances in the understanding of endometriosis related infertility. J Reprod Immunol 55:73–83PubMedCrossRefGoogle Scholar
  52. 52.
    Alpay Z, Saed GM, Diamond MP (2006) Female infertility and free radicals: potential role in adhesions and endometriosis. J Soc Gynecol Investig 13(6):390–398PubMedCrossRefGoogle Scholar
  53. 53.
    Doody MC, Gibbons WE, Buttram VC Jr (1988) Linear regression analysis of ultrasound follicular growth series: evidence for an abnormality of follicular growth in endometriosis patients. Fertil Steril 49:47–51PubMedGoogle Scholar
  54. 54.
    Grant A (1966) Additional sterility factors in endometriosis. Fertil Steril 17:514–519PubMedGoogle Scholar
  55. 55.
    Wardle PG, Mitchell JD, McLaughlin EA, Ray BD, McDermott A, Hull MG (1985) Endometriosis and ovulatory disorder: reduced fertilisation in vitro compared with tubal and unexplained infertility. Lancet 2:236–239PubMedCrossRefGoogle Scholar
  56. 56.
    Garrido N, Navarro J, Garcia-Velasco J, Remoh J, Pellice A, Simon C (2002) The endometrium versus embryonic quality in endometriosis-related infertility. Hum Reprod Update 8:95–103PubMedCrossRefGoogle Scholar
  57. 57.
    Osborn B, Haney AF, Misukonis M, Weinberg JB (2002) Inducible nitric oxide synthase expression by peritoneal macrophages in endometriosis-associated infertility. Fertil Steril 77:46–51PubMedCrossRefGoogle Scholar
  58. 58.
    Curtis P, Lindsay P, Jackson AE, Shaw RW (1993) Adverse effects on sperm movement characteristic in women with minimal and mild endometriosis. Br J Obstet Gynaecol 100:165–169PubMedCrossRefGoogle Scholar
  59. 59.
    Oak MK, Chantler EN, Wiliams CA, Elstein M (1985) Sperm survival studies in peritoneal fluid from infertile women with endometriosis and unexplained infertility. Clin Reprod Fertil 3:297–303PubMedGoogle Scholar
  60. 60.
    Mansour G, Aziz N, Sharma R, Falcone T, Goldberg J, Agarwal A (2009) The impact of peritoneal fluid from healthy women and from women with endometriosis on sperm DNA and its relationship to the sperm deformity index. Fertil Steril 92:61–67PubMedCrossRefGoogle Scholar
  61. 61.
    Mansour G, Agarwal A, Radwan E, Sharma R, Goldberg J, Falcone T (2007) DNA damage in metaphase II oocytes is induced by peritoneal fluid from endometriosis patients. ASRM 63rd annual meetingGoogle Scholar
  62. 62.
    Mansour G, Radwan E, Sharma R, Agarwal A, Falcone T, Goldberg J (2007) DNA damage to embryos incubated in the peritoneal fluid of patients with endometriosis: role in infertility. ASRM 63rd annual meetingGoogle Scholar
  63. 63.
    Agarwal A, Gupta S, Sikka S (2006) The role of free radicals and antioxidants in reproduction. Curr Opin Obstet Gynecol 18:325–332PubMedCrossRefGoogle Scholar
  64. 64.
    Polak G, Rola R, Gogacz M, Koziol-Montewka M, Kotarski J (1999) Malonyldialdehyde and total antioxidant status in the peritoneal fluid of infertile women. Ginecol PII 70:135–140Google Scholar
  65. 65.
    Toya M, Saito H, Ohta N, Saito T, Kaneko T, Hiroi M (2000) Moderate and severe endometriosis is associated with alterations in the cell cycle of granulosa cells in patients undergoing in vitro fertilization and embryo transfer. Fertil Steril 73:344–350PubMedCrossRefGoogle Scholar
  66. 66.
    Nakahara K, Saito H, Saito T, Ito M, Ohta N, Sakai N et al (1997) Incidence of apoptotic bodies in membrana granulosa of the patients participating in an in vitro fertilization program. Fertil Steril 67:302–308PubMedCrossRefGoogle Scholar
  67. 67.
    Sifer C, Benifla JL, Bringuier AF, Porcher R, Blanc-Layrac G, Madelenat P, Feldman G (2002) Could induced apoptosis of human granulosa cells predict in vitro fertilization-embryo transfer outcome? A preliminary study of 25 women. Eur J Obstet Gynecol Reprod Biol 103:150–153PubMedCrossRefGoogle Scholar
  68. 68.
    Cahill DJ, Wardle PG, Maile LA, Harlow CR, Hull MG (1997) Ovarian dysfunction in endometriosis-associated and unexplained infertility. J Assist Reprod Genet 14:554–557PubMedCrossRefGoogle Scholar
  69. 69.
    Tummon IS, Maclin VM, Radwanska E, Binor Z, Dmowski WP (1988) Occult ovulatory dysfunction in women with minimal endometriosis or unexplained infertility. Fertil Steril 50:716–720PubMedGoogle Scholar
  70. 70.
    Trinder J, Cahill DJ (2002) Endometriosis and infertility: the debate continues. Hum Fertil 5:S21–S27CrossRefGoogle Scholar
  71. 71.
    Mahmood TA, Templeton A (1991) Folliculogenesis and ovulation in infertile women with mild endometriosis. Hum Reprod 6:227–231PubMedGoogle Scholar
  72. 72.
    Marcoux S, Maheux R, Berube S (1997) Laparoscopic surgery in infertile women with minimal or mild endometriosis. Canadian collaborative group on endometriosis. N Engl J Med 337:217–222PubMedCrossRefGoogle Scholar
  73. 73.
    Parazzini F (1999) Ablation of lesions or no treatment in minimal–mild endometriosis in infertile women: a randomized trial. Gruppo Italiano per lo Studio dell’Endometriosi. Hum Reprod 14:1332–1334PubMedCrossRefGoogle Scholar
  74. 74.
    Garcia-Velasco JA, Arici A (2004) Surgery for the removal of endometriomas before in vitro fertilization does not increase implantation and pregnancy rates. Fertil Steril 81:1206PubMedCrossRefGoogle Scholar
  75. 75.
    Suzuki T, Izumi S, Matsubayashi H, Awaji H, Yoshikata K, Makino T (2005) Impact of ovarian endometrioma on oocytes and pregnancy outcome in in vitro fertilization. Fertil Steril 83:908–913PubMedCrossRefGoogle Scholar
  76. 76.
    Parazzini F, Chiaffarino F, Surace M, Chatenoud L, Cipriani S, Chiantera V et al (2004) Selected food intake and risk of endometriosis. Hum Reprod 19:1755–1759PubMedCrossRefGoogle Scholar
  77. 77.
    Mier-Cabrera J, Genera-Garcia M, De la Jara-Diaz J, Perichart-Perera O, Vadillo-Ortega F, Hernandez-Guerrero C (2008) Effect of vitamins C and E supplementation on peripherals oxidative stress markers and pregnancy rate in women with endometriosis. Int J Gynecol Obstet 100:252–256CrossRefGoogle Scholar
  78. 78.
    Westphal LM, Polan ML, Trant AS, Mooney SB (2004) A nutritional supplement for improving fertility in women: a pilot study. J Reprod Med 49:289–293PubMedGoogle Scholar
  79. 79.
    National Academy of Sciences (1989) Recommended dietary allowances. 10th edn. National Academy Press, WashingtonGoogle Scholar
  80. 80.
    Ehrenkranz R (1980) Vitamin E and the neonate. Am J Dis Child 134:1157–1168PubMedGoogle Scholar
  81. 81.
    Palamanda JR, Kehrer JR (1993) Involvement of vitamin E and protein thiols in the inhibition of microsomal lipid peroxidation by glutathione. Lipids 28:427–431PubMedCrossRefGoogle Scholar
  82. 82.
    Burton GW, Traber MG (1990) Vitamin E: antioxidant activity, biokinetics, and bioavailability. Annu Rev Nutr 10:357–382PubMedCrossRefGoogle Scholar
  83. 83.
    Hernandez-Guerrero CA, Bujalil-Montenegro L, De la Jara-Diaz J, Mier-Cabrera J, Bouchan-Valencia P (2006) Endometriosis and deficient intake of antioxidant molecules related to peripherals and peritoneal oxidative stress. Ginecol Obstet Mex 74:20–28PubMedGoogle Scholar
  84. 84.
    Jackson D, Craven RA, Hutson RC, Graze I, Lueth P, Tonge RP, Hartley JL, Nickson JA, Rayner SJ, Johnston C, Dieplinger B, Hubalek M, Wilkinson N, Perren TJ, Kehoe S, Hall GD, Daxenbichler G, Dieplinger H, Selby PJ, Banks RE (2007) Proteomic profiling identifies afamin as a potential biomarker for ovarian cancer. Clin Cancer Res 13:7370–7379PubMedCrossRefGoogle Scholar
  85. 85.
    Dieplinger H, Ankerst DP, Burges A, Lenhard M, Lingenhel A, Fineder L, Buchner H, Stieber P (2009) Afamin and apolipoprotein A-IV: novel protein markers for ovarian cancer. Cancer Epidemiol Biomarkers Prev 18:1127–1133PubMedCrossRefGoogle Scholar
  86. 86.
    de Muñoz CM, Antonio RJ, Angel LJ, Eduardo M, Adolfo C, Fernando P-G, Sonia H, Alejandra C (1996) Tablas de valor nutritivo de los alimentos. Editorial Pax México, México D.F.Google Scholar
  87. 87.
    Gao X, Martin A, Lin H, Bermudez OI, Tucker KL (2006) α-tocopherol intake and plasma concentrations of hispanic and non-hispanic white elders is associated with dietary intake patters. J Nutr 136:2574–2579PubMedGoogle Scholar
  88. 88.
    Dennehy CE (2006) The use of herbs and dietary supplements in gynecology: an evidence-based review. J Midwifery Womens Health 51:402–409PubMedCrossRefGoogle Scholar
  89. 89.
    Ziaei S, Faghihzadeh S, Sohrabvand F, Lamyian M, Emamgholy T (2001) A randomised placebo-controlled trial to determine the effect of vitamin E in treatment of primary dysmenorrhoea. Br J Obstet Gynecol 108:1181–1183CrossRefGoogle Scholar
  90. 90.
    Bruno RS, Leonard SW, Atkinson J, Montine TJ, Ramakrishnan R, Bray TM, Traber MG (2006) Faster plasma vitamin E disappearance in smokers is normalized by vitamin C supplementation. Free Radic Biol Med 40:689–697PubMedCrossRefGoogle Scholar
  91. 91.
    Zhang X, Sharma RK, Agarwal A, Falcone T (2005) Effect of pentoxifylline in reducing oxidative stress-induced embryotoxicity. J Assist Reprod Genet 22(11–12):415–417PubMedCrossRefGoogle Scholar
  92. 92.
    Lv D, Song H, Clarke J, Shi G (2009) Pentoxifylline versus medical therapies for subfertile women with endometriosis. Cochrane Database Syst Rev 8(3):CD007677Google Scholar
  93. 93.
    Swarnaker S, Paul S (2009) Curcumin arrests endometriosis by downregulation of matrix metalloproteinase-9 activity. Indian J Biochem Biophys 46(1):59–65Google Scholar
  94. 94.
    Paul S, Sharma AV, Mahapatra PS, Bhattacharya P, Reiter RJ, Swarnakar S (2008) Role of melatonin in regulating matrix metalloproteinase-9 via tissue inhibitors of metalloproteinase-1 during protection against endometriosis. J Pineal Res 44(4):439–449PubMedCrossRefGoogle Scholar
  95. 95.
    Guney M, Oral B, Karahan N, Mungan T (2008) Regression of endometrial explants in a rat model of endometriosis treated with melatonin. Fertil Steril 89(4):934–942PubMedCrossRefGoogle Scholar
  96. 96.
    Xu H, Liu WT, Chu CY, Ng PS, Wang CC, Rogers MS (2009) Antiangiogenic effects of green tea catechin on an experimental endometriosis mouse model. Hum Reprod 24(3):608–618PubMedCrossRefGoogle Scholar
  97. 97.
    Defre`re S, Van Langendonckt A, Vaesen S, Jouret M, Gonza′lez Ramos R, Gonzalez D, Donnez J (2006) Iron overload enhances epithelial cell proliferation in endometriotic lesions induced in a murine model. Hum Reprod 21:2810–2816Google Scholar
  98. 98.
    Sanfilippo JS, Wakim NG, Schikler KN, Yussman MA (1986) Endometriosis in association with uterine anomaly. Am J Obstet Gynecol 154:39–43PubMedGoogle Scholar
  99. 99.
    Arumugam K, Lim JM (1997) Menstrual characteristics associated with endometriosis. Br J Obstet Gynaecol 104:948–950PubMedCrossRefGoogle Scholar
  100. 100.
    Guney M, Nasir S, Oral B, Karahan N, Mungan T (2007) Effect of caffeic acid phenethyl ester on the regression of endometrial explants in an experimental rat model. Reprod Sci 14(3):270–279PubMedCrossRefGoogle Scholar
  101. 101.
    Murphy AA, Zhou MH, Malkapuram S, Santanam N, Parthasarathy S, Sidell N (2000) RU486-induced growth inhibition of human endometrial cells. Fertil Steril 71:1014–1019CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Department of Obstetrics and GynecologyMount Sinai School of MedicineNew YorkUSA
  2. 2.Center for Reproductive MedicineLerner College of Medicine, Cleveland ClinicClevelandUSA

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