Clinical Aspects of Endometriosis

  • Attila Bokor
  • Christel Meuleman
  • Thomas D’Hooghe
Chapter

Abstract

Endometriosis is a common, benign, estrogen-dependent, gynecological disorder associated with pelvic pain and infertility. The prevalence of this condition can reasonably be assumed to be around 10%. Endometriosis should be suspected in women with dysmenorrhea, dyspareunia, chronic pelvic pain, or subfertility; it may also be asymptomatic and can be present as a chronic disease in a subset of patients. Visual recognition during laparoscopy is required for the definitive diagnosis of endometriosis. Treatment must be individualized, taking into consideration the clinical problem in its entirety, including the impact of the disease and the effect of its treatment on quality of life. Endometriosis-associated pain can be effectively treated by surgery and by hormonal suppression. Endometriosis-associated subfertility can be effectively treated by surgery and by assisted reproduction, but not by hormonal suppression. Endometriosis can recur after treatment, and the risk increases with the severity of endometriosis and the time interval since the last surgery. However, patients with recurrent pain do not always have endometriosis and may require a multidisciplinary approach involving a pain clinic, and counseling should be considered early in the treatment plan.

Keywords

Endometriosis Infertility Etiology Diagnosis Treatment Guidelines 

References

  1. 1.
    Sampson JA (1927) Peritoneal endometriosis due to menstrual dissemination of endometrial tissue into the pelvic cavity. Am J Obstet Gynecol 14:422-469Google Scholar
  2. 2.
    D’Hooghe TM, Hill JA (2006) Chapter 29. Endometriosis. In: Williams and Wilkins, Berek JS (eds) Novak’s gynecology, 14th edn. Philadelphia, USA, pp 1137-1184Google Scholar
  3. 3.
    Halme J, Becker S, Hammond MG et al (1984) Retrograde menstruation in healthy women and in patients with endometriosis. Obstet Gynecol 64:151-154PubMedGoogle Scholar
  4. 4.
    Liu DTY, Hitchcock A (1986) Endometriosis: its association with retrograde menstruation, dysmenorrhoea and tubal pathology. BJOG 93:859-862CrossRefGoogle Scholar
  5. 5.
    Koninckx PR, De Moor P, Brosens IA (1980) Diagnosis of the luteinized unruptured follicle syndrome by steroid hormone assays in peritoneal fluid. BJOG 87:929-934CrossRefGoogle Scholar
  6. 6.
    Kruitwagen RFPM, Poels LG, Willemsen WNP et al (1991) Endometrial epithelial cells in peritoneal fluid during the early follicular phase. Fertil Steril 55:297-303PubMedGoogle Scholar
  7. 7.
    D’Hooghe TM, Bambra CS, Isahakia M et al (1995) Intrapelvic injection of menstrual endometrium causes endometriosis in baboons (Papio cynocephalus, Papio anubis). Am J Obstet Gynecol 173:125-134PubMedCrossRefGoogle Scholar
  8. 8.
    Olive DL, Henderson DY (1987) Endometriosis and müllerian anomalies. Obstet Gynecol 69:412-415PubMedGoogle Scholar
  9. 9.
    Pinsonneault O, Goldstein DP (1985) Obstructing malformations of the uterus and vagina. Fertil Steril 44:241-247PubMedGoogle Scholar
  10. 10.
    D’Hooghe TM, Bambra CS, Suleman MA et al (1994) Development of a model of retrograde menstruation in baboons (Papio anubis). Fertil Steril 62:635-638PubMedGoogle Scholar
  11. 11.
    Dinulescu DM, Ince TA, Quade BJ et al (2005) Role of K-ras and Vten in the development of mouse models of endometriosis and endometrioid ovarian cancer. Nat Med 11:63-70PubMedCrossRefGoogle Scholar
  12. 12.
    Levander G, Normann P (1955) The pathogenesis of endometriosis: an experimentál study. Acta Obstet Gynecol Scand 34:366-398PubMedCrossRefGoogle Scholar
  13. 13.
    Merrill JA (1966) Endometrial induction of endometriosis across millipore filters. Am J Obstet Gynecol 94:780-789PubMedGoogle Scholar
  14. 14.
    Kennedy SH (2004) Genetics of endometriosis. In: Tulandi T, Redwine D (eds) Endometriosis: advances and controversies. Marcel Dekker Publishing, New York, NY, pp 55-68Google Scholar
  15. 15.
    Simpson JL, Elias S, Malinak LR et al (1980) Heritable aspects of endometriosis. I. Genetics studies. Am J Obstet Gynecol 137:327-331PubMedGoogle Scholar
  16. 16.
    Moen MH, Magnus P (1993) The familial risk of endometriosis. Acta Obstet Gynecol Scand 72:560-564PubMedCrossRefGoogle Scholar
  17. 17.
    Shin JC, Ross HL, Elias S et al (1997) Detection of chromosomal aneuploidy in endometriosis by multicolor in situ hybridization. Hum Genet 100:401-406PubMedCrossRefGoogle Scholar
  18. 18.
    Kosugi Y, Elias S, Malinak LR et al (1999) Increased heterogeneity of chromosome 17 aneuploidy in endometriosis. Am J Obstet Gynecol 180:792-797PubMedCrossRefGoogle Scholar
  19. 19.
    Gogusev J, Bouquet de Joliniere J, Telvi L et al (1999) Detection of DNA copy number changes in human endometriosis by comparative genomic hybridisation. Hum Genet 105:444-451PubMedCrossRefGoogle Scholar
  20. 20.
    Falconer H, D’Hooghe T, Fried G (2007) Endometriosis and genetic polymorphisms. Obstet Gynecol Surv 62(9):616-628PubMedCrossRefGoogle Scholar
  21. 21.
    D’Hooghe TM, Hill JA (1996) Immunobiology of endometriosis. In: Bronston R, Anderson DJ (eds) Immunology of reproduction. Blackwell Scientific, Cambridge, MA, pp 322-356Google Scholar
  22. 22.
    Dmowski WP, Steele RN, Baker GF (1981) Deficient cellular immunity in endometriosis. Am J Obstet Gynecol 141:377-383PubMedGoogle Scholar
  23. 23.
    Oosterlynck D, Cornillie FJ, Waer M et al (1991) Women with endometriosis show a defect in natural killer cell activity resulting in a decreased cytotoxicity to autologous endometrium. Fertil Steril 56:45-51PubMedGoogle Scholar
  24. 24.
    D’Hooghe TM, Scheerlinck JP, Koninckx PR et al (1995) Anti-endometrial lymphocytotoxicity and natural killer activity in baboons with endometriosis. Hum Repród 10:558-562PubMedGoogle Scholar
  25. 25.
    Hill JA (1992) Immunology and endometriosis. Fertil Steril 58:262-264PubMedGoogle Scholar
  26. 26.
    Zeller JM, Henig I, Radwanska E et al (1987) Enhancement of humán monocyte and peritoneal macrophage chemiluminescence activities in women with endometriosis. Am J Reprod Immunol Microbiol 13:78-82PubMedGoogle Scholar
  27. 27.
    Halme J, Becker S, Haskill S (1987) Altered maturation and function of peritoneal macrophages: possible role in pathogenesis of endometriosis. Am J Obstet Gynecol 156:783-789PubMedGoogle Scholar
  28. 28.
    D’Hooghe TM, Nugent N, Cuneo S, et al (2001) Recombinant human TNF binding protein (r-hTBP-1) inhibits the development of endometriosis in baboons: a prospective, randomized, placebo- and drug-controlled study. Paper presented at Annual Meeting of the American Society for Reproductive Medicine, Orlando, Florida, 22-24 Oct 2001Google Scholar
  29. 29.
    Hill JA, Cohen J, Anderson DJ (1989) The effects of lymphokines and monokines on human sperm fertilizing ability in the zona-free hamster egg penetration test. Am J Obstet Gynecol 160:1154-1159PubMedGoogle Scholar
  30. 30.
    Zhang R, Wild RA, Ojago JM (1993) Effect of tumor necrosis factor-alpha on adhesion of human endometrial stromal cells to peritoneal mesothelial cells: an in vitro system. Fertil Steril 59:1196-1201PubMedGoogle Scholar
  31. 31.
    Halme J, White C, Kauma S et al (1988) Peritoneal macrophages from patients with endometriosis release growth factor activity in vitro. J Clin Endocrinol Metab 66:1044-1049PubMedCrossRefGoogle Scholar
  32. 32.
    Kauma S, Clark MR, White C et al (1988) Production of fibronectin by peritoneal macrophages and concen-tration of fibronectin in peritoneal fluid from patients with or without endometriosis. Obstet Gynecol 72:13-18PubMedGoogle Scholar
  33. 33.
    Sharpe-Timms KL, Keisler LW, Mclntush EW et al (1998) Tissue inhibitor of metailoproteinase-1 concentra-tions are attenuated in peritoneal fluid and sera of women with endometriosis and restored in sera by gonadotropin-releasing hormone agonist therapy. Fertil Steril 69:1128-1134PubMedCrossRefGoogle Scholar
  34. 34.
    Kokorine I, Nisolle M, Donnez J et al (1997) Expression of interstitial collagenase (MMP-1) is related to the activity of human endometriotic lesions. Fertil Steril 68:246-251PubMedCrossRefGoogle Scholar
  35. 35.
    Bulun SE, Yang S, Fang Z, Gurates B, Tamura M, Sebastian S (2002) Estrogen production and metabolism in endometriosis. Ann N Y Acad Sci 955:75-85; discussion 86-88, 396-406PubMedCrossRefGoogle Scholar
  36. 36.
    Bulun SE, Zeitoun K, Takayama K et al (2000) Molecular basis for treating endometriosis with aromatase inhibitors. Hum Reprod Update 6:413-418PubMedCrossRefGoogle Scholar
  37. 37.
    Agic A, Xu H, Finas D et al (2006) Is endometriosis associated with systemic subclinical inflammation? Gynecol Obstet Invest 62(3):139-147PubMedCrossRefGoogle Scholar
  38. 38.
    Guo SW (2004) The link between exposure to dioxin and endometriosis: a critical reappraisal of primate data. Gynecol Obstet Invest 57:157-173PubMedCrossRefGoogle Scholar
  39. 39.
    D’Hooghe TM, Debrock S (2003) Future directions in endometriosis research. Obstet Gynecol Clin North Am 30:221-244PubMedCrossRefGoogle Scholar
  40. 40.
    Giudice LC, Kao LC (2004) Endometriosis. Lancet 364(9447):1789-1799PubMedCrossRefGoogle Scholar
  41. 41.
    Koninckx PR, Meuleman C, Demeyere S et al (1991) Suggestive evidence that pelvic endometriosis is a progressive disease, whereas deeply infiltrating endometriosis is associated with pelvic pain. Fertil Steril 55:759-765PubMedGoogle Scholar
  42. 42.
    Mahmood TA, Templeton A (1991) Prevalence and genesis of endometriosis. Hum Reprod 6:544-549PubMedGoogle Scholar
  43. 43.
    Moen MH (1987) Endometriosis in women at interval sterilization. Acta Obstet Gynecol Scand 66:451-454PubMedCrossRefGoogle Scholar
  44. 44.
    Kennedy S, Bergqvist A, Chapron C, on behalf of the ESHRE Special Interest Group for Endometriosis and Endometrium Guideline Development Group et al (2005) ESHRE guideline for the diagnosis and treatment of endometriosis. Hum Reprod 20(10):2698-2704PubMedCrossRefGoogle Scholar
  45. 45.
    Arumugam K, Lim JMH (1997) Menstrual characteristics associated with endometriosis. BJOG 104:948-950CrossRefGoogle Scholar
  46. 46.
    Vercellini P, De Giorgi O, Aimi G et al (1997) Menstrual characteristics in women with and without endometriosis. Obstet Gynecol 90:264-268PubMedCrossRefGoogle Scholar
  47. 47.
    Matalliotakis IM, Cakmak H, Fragouli YG, Goumenou AG, Mahutte NG, Arici A (2008) Epidemiological characteristics in women with and without endometriosis in the Yale series. Arch Gynecol Obstet 277(5):389-393PubMedCrossRefGoogle Scholar
  48. 48.
    Filer RB, Wu CH (1989) Coitus during menses. Its effect on endometriosis and pelvic inflammatory disease. J Reprod Med 34(11):887-890PubMedGoogle Scholar
  49. 49.
    Mathias JR, Franklin R, Quast DC et al (1998) Relation of endometriosis and neuromuscular disease of the gastrointestinal tract: new insights. Fertil Steril 70:81-88PubMedCrossRefGoogle Scholar
  50. 50.
    Hadfield RM, Mardon H, Barlow D et al (1996) Delay in the diagnosis of endometriosis: a survey of women from the USA and the UK. Hum Reprod 11:878-880PubMedGoogle Scholar
  51. 51.
    Dmowski WP, Lesniewicz R, Rana N et al (1997) Changing trends in the diagnosis of endometriosis: a comparative study of women with endometriosis presenting with chronic pain or infertility. Fertil Steril 67:238-243PubMedCrossRefGoogle Scholar
  52. 52.
    Chapron C, Fauconnier A, Dubuisson JB et al (2003) Deep infiltrating endometriosis: relation between severity of dysmenorrhoea and extent of disease. Hum Reprod 18:760-766PubMedCrossRefGoogle Scholar
  53. 53.
    Barlow DH, Glynn CJ (1993) Endometriosis and pelvic pain. Baillieres Clin Obstet Gynaecol 7:775-790PubMedCrossRefGoogle Scholar
  54. 54.
    Anaf V, Simon Ph, El Nakadi I et al (2000) Relationship between endometriotic foci and nerves in rectovaginal endometriotic nodules. Hum Reprod 15:1744-1750PubMedCrossRefGoogle Scholar
  55. 55.
    D’Hooghe TM, Debrock S, Hill JA et al (2003) Endometriosis and subfertility: is the relationship resolved? Sem Reprod Med 21:243-254CrossRefGoogle Scholar
  56. 56.
    Practice Committee of American Society for Reproductive Medicine. Treatment of pelvic pain associated with endometriosis. (2008) Fertil Steril. Nov;90(5 Suppl):S260-S269. ReviewGoogle Scholar
  57. 57.
    American Fertility Society (1985) Revised American Fertility Society classification of endometriosis. Fertil Steril 43:351-352Google Scholar
  58. 58.
    Haney AF (1993) Endometriosis-associated infertility. Baillieres Clin Obstet Gynaecol 7:791-812PubMedCrossRefGoogle Scholar
  59. 59.
    D’Hooghe TM, Bambra CS, Raeymaekers BM et al (1996) Serial laparoscopies over 30 months show that endometriosis is a progressive disease in captive baboons (Papio anubis, Papio cynocephalus). Fertil Steril 65:645-649PubMedGoogle Scholar
  60. 60.
    Vercammen E, D’Hooghe TM, Hill JA (2000) Endometriosis and recurrent miscarriage. Semin Reprod Med 18:363-368PubMedCrossRefGoogle Scholar
  61. 61.
    Cahill DJ, Hull MGR (2000) Pituitary-ovarian dysfunction and endometriosis. Hum Reprod Update 6:56-66PubMedCrossRefGoogle Scholar
  62. 62.
    Marcoux S, Maheux R, Bérubé S (1997) The Canadian Collaborative Group on Endometriosis. Laparoscopic surgery in infertile women with minimal or mild endometriosis. N Engl J Med 337:217-222PubMedCrossRefGoogle Scholar
  63. 63.
    Gruppo Italiano per lo Studio deli’ Endometriosi (1999) Ablation of lesions or no treatment in minimal-mild endometriosis in infertile women: a randomized trial. Hum Reprod 14:1332-1334CrossRefGoogle Scholar
  64. 64.
    Propst AM, Storti K, Barbieri RL (1998) Lateral cervical displacement is associated with endometriosis. Fertil Steril 70:568-570PubMedCrossRefGoogle Scholar
  65. 65.
    Koninckx PR, Oosterlynck D, D’Hooghe TM et al (1994) Deeply infiltrating endometriosis is a disease whereas mild endometriosis could be considered a non-disease. Ann N Y Acad Sci 734:333-341PubMedCrossRefGoogle Scholar
  66. 66.
    Koninckx PR, Meuleman C, Oosterlynck D et al (1996) Diagnosis of deep endometriosis by clinical examina-tion during menstruation and plasma CA 125 concentration. Fertil Steril 65:280-287PubMedGoogle Scholar
  67. 67.
    Rock JA, Markham SM (1987) Extra pelvic endometriosis. In: Wilson EA (ed) Endometriosis. AR liss, New York, NY, pp 185-206Google Scholar
  68. 68.
    Guerriero S, Paoletti AM, Mais V et al (1996) Transvaginal ultrasonography combined with CA125 plasma levels in the diagnosis of endometrioma. Fertil Steril 65:293-298PubMedGoogle Scholar
  69. 69.
    Fedele L, Bianchi S, Portuese A et al (1998) Transrectal ultrasonography in the assessment of rectovaginal endometriosis. Obstet Gynecol 91:444-448PubMedCrossRefGoogle Scholar
  70. 70.
    Moore J, Copley S, Morris J et al (2002) A systematic review of the accuracy of ultrasound in the diagnosis of endometriosis. Ultrasound Obstet Gynecol 20:630-634PubMedCrossRefGoogle Scholar
  71. 71.
    McBean JH, Gibson M, Brumsted JR (1996) The association of intrauterine filling defects on HSG with endometriosis. Fertil Steril 66:522-526PubMedGoogle Scholar
  72. 72.
    Bast RC, Klug TL, St. John E et al (1983) A radio-immunoassay using a monoclonal antibody to monitor the course of epithelial ovarian cancer. N Engl J Med 309:883-887PubMedCrossRefGoogle Scholar
  73. 73.
    Pittaway DE, Fayez JA (1986) The use of CA125 in the diagnosis and management of endometriosis. Fertil Steril 46:790-795PubMedGoogle Scholar
  74. 74.
    Pittaway DE, Fayez JA (1987) Serum CA125 levels increase during menses. Am J Obstet Gynecol 156:75-76PubMedGoogle Scholar
  75. 75.
    Moloney MD, Thornton JG, Cooper EH (1989) Serum CA125 antigen levels and disease severity in patients with endometriosis. Obstet Gynecol 73:767-769PubMedGoogle Scholar
  76. 76.
    O’Shaughnessy A, Check JH, Nowroozi K et al (1993) CA125 levels measured in different phases of the menstrual cycle in screening for endometriosis. Obstet Gynecol 81:99-103PubMedGoogle Scholar
  77. 77.
    Pittaway DE (1990) The use of serial CA125 concentrations to monitor endometriosis in infertile women. Am J Obstet Gynecol 163:1032-1037PubMedGoogle Scholar
  78. 78.
    Nisolle M, Paindaveine B, Bourdin A et al (1990) Histological study of peritoneal endometriosis in infertile women. Fertil Steril 53:984-988PubMedGoogle Scholar
  79. 79.
    Moen MH, Halvorsen TB (1992) Histologic confirmation of endometriosis in different peritoneal lesions. Acta Obstet Gynecol Scand 71:337-342PubMedCrossRefGoogle Scholar
  80. 80.
    Vercellini P, Aimi G, Panazza S et al (2000) Deep endometriosis conundrum: evidence in favor of a peritoneal origin. Fertil Steril 73:1043-1046PubMedCrossRefGoogle Scholar
  81. 81.
    Redwine DB (1999) Ovarian endometriosis: a marker for more extensive pelvic and intestinal disease. Fertil Steril 72:310-315PubMedCrossRefGoogle Scholar
  82. 82.
    Walter AJ, Hentz JG, Magtibay PM et al (2001) Endometriosis: correlation between histologic and visual findings at laparoscopy. Am J Obstet Gynecol 184:1407-1413PubMedCrossRefGoogle Scholar
  83. 83.
    Czernobilsky B (1987) Endometriosis. In: Fox H (ed) Obstetrical and gynecological pathology. Churchill Livingstone, New York, NY, pp 763-777Google Scholar
  84. 84.
    Donnez J, Nisolle M, Casanas-Roux F (1992) Three-dimensional architectures of peritoneal endometriosis. Fertil Steril 57:980-983PubMedGoogle Scholar
  85. 85.
    McArthur JW, Ulfelder H (1965) The effect of pregnancy upon endometriosis. Obstet Gynecol Surv 20:709-733PubMedCrossRefGoogle Scholar
  86. 86.
    D’Hooghe TM, Bambra CS, De Jonge I et al (1997) Pregnancy does not affect endometriosis in baboons (Papio anubis, Papio cynocephalus). Arch Gynecol Obstet 261:15-19PubMedCrossRefGoogle Scholar
  87. 87.
    Italian Endometriosis Study Group (1999) Oral contraceptive use and risk of endometriosis. BJOG 106:695-699CrossRefGoogle Scholar
  88. 88.
    Mahmood TA, Templeton A (1990) The impact of treatment on the natural history of endometriosis. Hum Reprod 5:965-970PubMedGoogle Scholar
  89. 89.
    Abbott JA, Hawe J, Clayton RD et al (2003) The effects and effectiveness of laparoscopic excision of endometriosis: a prospective study with 2-5 year follow-up. Hum Reprod 18:1922-1927PubMedCrossRefGoogle Scholar
  90. 90.
    Chapron C, Fauconnier A, Vieira M et al (2003) Anatomical distribution of deeply infiltrating endometriosis: surgical implications and proposition for a classification. Hum Reprod 18:157-161PubMedCrossRefGoogle Scholar
  91. 91.
    Fedele L, Bianchi S, Zanconato G et al (2004) Long-term follow-up after conservative surgery for rectovaginal endometriosis. Am J Obstet Gynecol 190:1020-1024PubMedCrossRefGoogle Scholar
  92. 92.
    Redwine DB, Wright JT (2001) Laparoscopic treatment of complete obliteration of the cul-de-sac associated with endometriosis: long-term follow-up of en bloc resection. Fertil Steril 76:358-365PubMedCrossRefGoogle Scholar
  93. 93.
    Tulandi T, Al Took S (1998) Reproductive outcome after treatment of mild endometriosis with laparoscopic excision and electrocoagulation. Fertil Steril 69:229-231PubMedCrossRefGoogle Scholar
  94. 94.
    Vercellini P, Aimi G, Busacca M et al (2003) Laparoscopic uterosacral ligament resection for dysmenorrhea associated with endometriosis: results of a randomized, controlled trial. Fertil Steril 80(2):310-319PubMedCrossRefGoogle Scholar
  95. 95.
    Chapron C, Vercellini P, Barakat H et al (2002) Management of ovarian endometriomas. Hum Reprod Update 8:6-7CrossRefGoogle Scholar
  96. 96.
    Watson A, Vandekerckhove P, Lilford R (2000) Liquid and fluid agents for preventing adhesions after surgery for subfertility. Cochrane Database Syst Rev 3:CD001298PubMedGoogle Scholar
  97. 97.
    Koninckx PR, Timmermans B, Meuleman C et al (1996) Complications of CO-2 laser endoscopic excision of deep endometriosis. Hum Reprod 11:2263-2268PubMedGoogle Scholar
  98. 98.
    Redwine DB, Koning M, Sharpe DR (1996) Laparoscopically assisted transvaginal segmental resection of the rectosigmoid colon for endometriosis. Fertil Steril 65:193-197PubMedGoogle Scholar
  99. 99.
    Namnoum AB, Hickman TN, Goodman SB et al (1995) Incidence of symptom recurrence after hysterectomy for endometriosis. Fertil Steril 64:898-902PubMedGoogle Scholar
  100. 100.
    Lefebvre G, Allaire C, Jeffrey J et al (2002) SOGC clinical guidelines: hysterectomy. J Obstet Gynaecol Can 24:37-61PubMedGoogle Scholar
  101. 101.
    Yap C, Furness S, Farquhar C (2004) Pre and post operatíve medical therapy for endometriosis surgery. Cochrane Database Syst Rev 3:CD003678PubMedGoogle Scholar
  102. 102.
    Audebert A, Descampes P, Marret H et al (1998) Pre or post operatíve medical treatment with nafarelin in stage III-IV endometriosis: a French multicentered study. Eur J Obstet Gynecol Reprod Biol 79:145-148PubMedCrossRefGoogle Scholar
  103. 103.
    Matorras R, Elorriaga MA, Pijoan JI et al (2002) Recurrence of endometriosis in women with bilateral adnexectomy (with or without total hysterectomy) who received hormone replacement therapy. Fertil Steril 77:303-308PubMedCrossRefGoogle Scholar
  104. 104.
    Abou-Setta AM, Al-Inany HG, Farquhar CM (2006) Levonorgestrel-releasing intrauterine device (LNG-IUD) for symptomatic endometriosis following surgery. Cochrane Database Syst Rev 4:CD005072PubMedGoogle Scholar
  105. 105.
    Feste JR (1985) Laser laparoscopy: a new modality. J Reprod Med 30:413-417PubMedGoogle Scholar
  106. 106.
    Nezhat C, Winer W, Crowgey S et al (1989) Videolaparoscopy for the treatment of endometriosis associated with infertility. Fertil Steril 51:237-240PubMedGoogle Scholar
  107. 107.
    Sutton CJG, Hill D (1990) Laser laparoscopy in the treatment of endometriosis: a 5 year study. BJOG 97:181-185CrossRefGoogle Scholar
  108. 108.
    Vercellini P, Cortesi I, Trespidi L et al (1996) Endometriosis and pelvic pain: relation to disease stage and localization. Fertil Steril 65:299-304PubMedGoogle Scholar
  109. 109.
    Guzick DS, Canis M, Silliman NP et al (1997) Prediction of pregnancy in infertile women based on the ASRM’s revised classification for endometriosis. Fertil Steril 67:822-836PubMedCrossRefGoogle Scholar
  110. 110.
    Attar E, Bulun SE (2006) Aromatase inhibitors: the next generation of therapeutics for endometriosis? Fertil Steril 85(5):1307-1318PubMedCrossRefGoogle Scholar
  111. 111.
    Canis M, Pouly JL, Wattiez A et al (1992) Incidence of bilateral adnexal disease in severe endometriosis (revised American Fertility Society [AFS] stage IV): should a stage V be included in the AFS classification? Fertil Steril 57:691-692PubMedGoogle Scholar
  112. 112.
    Badawy SZA, El Bakry MM, Samuel D et al (1988) Cumulative pregnancy rates in infertile women with endometriosis. J Reprod Med 33:757-760PubMedGoogle Scholar
  113. 113.
    Vercellini P, Crosignani PG, Fadini R et al (1999) A gonadotropin-releasing hormone agonist compared with expectant management after conservative surgery for symptomatic endometriosis. BJOG 106:672-677CrossRefGoogle Scholar
  114. 114.
    Parazzini F, Fedele L, Busacca M et al (1994) Postsurgical treatment of advanced endometriosis: results of a randomized clinical trial. Am J Obstet Gynecol 171:1205-1207PubMedGoogle Scholar
  115. 115.
    Kyama CM, Mihályi A, Mwenda JM et al (2005) The role of immunologic factors in the development of endometriosis: indications for treatment strategies. Therapy 4:623-639Google Scholar
  116. 116.
    Davis L, Kennedy SS, Moore J, Prentice A. (2007) Modern combined oral contraceptives for pain associated with endometriosis. Cochrane Database Syst Rev. 18;(3):CD001019Google Scholar
  117. 117.
    Prentice A, Deary AJ, Goldbeck WS, et al (2004) Gonadotrophin-releasing hormone analogues for pain associated with endometriosis. In: The Cochrane Library, Issue 3. John Wiley & Sons, Ltd, Chichester, UKGoogle Scholar
  118. 118.
    Prentice A, Deary AJ, Bland E (2004) Progestagens and anti-progestagens for pain associated with endometriosis. In: The Cochrane Library, Issue 3. John Wiley & Sons, Ltd, Chichester, UKGoogle Scholar
  119. 119.
    Davis L, Kennedy SS, Moore J, Prentice A (2007) Modern combined oral contraceptives for pain associated with endometriosis. Cochrane Database Syst Rev 18(3):CD001019Google Scholar
  120. 120.
    Harcison RF, Barry-Kinsella C (2000) Efficacy of medroxy-progesterone treatment in infertile women with endometriosis: a prospective, randomized, placebo-controlled study. Fertil Steril 74:24-30CrossRefGoogle Scholar
  121. 121.
    Brosens IA, Verleyen A, Cornillie FJ (1987) The morphologic effect of short-term medical therapy of endometriosis. Am J Obstet Gynecol 157:1215-1221PubMedGoogle Scholar
  122. 122.
    Gestrinone Italian Study Group (1996) Gestrinone versus a GnRHa for the treatment of pelvic pain associated with endometriosis: a multicenter, randomized, double-blind study. Fertil Steril 66:911-919Google Scholar
  123. 123.
    Barbieri RL, Ryan KJ (1981) Danazol: endocrine pharmacology and therapeutic applications. Am J Obstet Gynecol 141:453-463PubMedGoogle Scholar
  124. 124.
    Igarashi M, Iizuka M, Abe Y et al (1998) Novel vaginal danazol ring therapy for pelvic endometriosis, in particular deeply infiltrating endometriosis. Hum Reprod 13:1952-1956PubMedCrossRefGoogle Scholar
  125. 125.
    Borroni R, Di Blasio AM, Gaffuri B et al (2000) Expression of GnRH receptor gene in human ectopic endometrial cells and inhibition of their proliferation by leuprolide acetate. Mol Cell Endocrinol 159:37-43PubMedCrossRefGoogle Scholar
  126. 126.
    Wingfíeld M, Healy DL (1993) Endometriosis: medical therapy. Baillieres Clin Obstet Gynecol 7:813-838CrossRefGoogle Scholar
  127. 127.
    Hornstein MD, Surrey ES, Weisberg GW et al (1998) Leuprolide acetate depot and hormonal add-back in endometriosis: a 12-month study. Obstet Gynecol 91:16-24PubMedCrossRefGoogle Scholar
  128. 128.
    Riis BJ, Christiansen C, Johansen JS et al (1990) Is it possible to prevent boné loss in young women treated with luteinizing hormone-releasing agonists? J Clin Endocrinol Metab 70:920-924PubMedCrossRefGoogle Scholar
  129. 129.
    Pierce SJ, Gazvani MR, Farquharson RG (2000) Long-term use of gonadotropin-releasing hormoné analogs and hormone replacement therapy in the management of endometriosis: a randomized trial with a 6-year follow-up. Fertil Steril 74:964-968PubMedCrossRefGoogle Scholar
  130. 130.
    Tahara M, Matsuoka T, Yokoi T et al (2000) Treatment of endometriosis with a decreasing dosage of gonadotropin-releasing hormoné agonist (nafarelin): a pilot study with low-dose agonist therapy (“draw-back” therapy). Fertil Steril 73:799-804PubMedCrossRefGoogle Scholar
  131. 131.
    Stovall DW, Bowser LM, Archer DF et al (1997) Endometriosis-associated pain: evidence for an association between the stage of disease and a history of chronic pelvic pain. Fertil Steril 68:13-18PubMedCrossRefGoogle Scholar
  132. 132.
    Marjoribanks J, Proctor ML, Farquhar C (2003) Nonsteroidal anti-inflammatory drugs for primary dysmen-orrhoea. Cochrane Database Syst Rev 4:CD001751PubMedGoogle Scholar
  133. 133.
    Duffy DM, Stouffer RL (2002) Follicular administration of a cyclooxygenase inhibitor can prevent oocyte release without alteration of normál luteal function in rhesus monkeys. Hum Reprod 17:2825-2831PubMedCrossRefGoogle Scholar
  134. 134.
    Murphy AA, Zhou MH, Malkapuram S et al (2000) RU486-induced growth inhibition of human endometrial cells. Fertil Steril 74:1014-1019PubMedCrossRefGoogle Scholar
  135. 135.
    Buelke SJ, Bryant HU, Francis PC (1998) The selective estrogen receptor modulátor, raloxifene: an overview of nonclinical pharmacology and reproductive and developmental testing. Reprod Toxicol 12:217-221CrossRefGoogle Scholar
  136. 136.
    D’Hooghe TM, Nugent N, Cuneo S, et al (2001) Recombinant human TNF binding protein (r-hTBP-1) inhibits the development of endometriosis in baboons: a prospective, randomized, placebo- and drug-controlled study. Paper presented at Annual Meeting of the American Society for Reproductive Medicine, Orlando, Florida, 22-24 October 2001Google Scholar
  137. 137.
    Balasch J, Creus M, Fabregues F et al (1997) Pentoxifylline versus placebo in the treatment of infertility associated with minimal or mild endometriosis: a pilot randomized clinical trial. Hum Reprod 12:2046-2050PubMedCrossRefGoogle Scholar
  138. 138.
    Evers JLH (1989) The pregnancy rate of the no-treatment group in randomized clinical trials of endometriosis therapy. Fertil Steril 52:906-909PubMedGoogle Scholar
  139. 139.
    Bayer SR, Seibel MM, Saffan DS et al (1988) Efficacy of danazol treatment for minimai endometriosis in infertile women: a prospective randomized study. J Reprod Med 33:179-183PubMedGoogle Scholar
  140. 140.
    Propst AM, Laufer M (1999) Endometriosis in adolescents: incidence, diagnosis and treatment. J Reprod Med 44:751-758PubMedGoogle Scholar
  141. 141.
    Vercellini P, Trespidi L, Colombo A et al (1993) A gonadotropin-releasing hormone agonist versus a low-dose oral contraceptive for pelvic pain associated with endometriosis. Fertil Steril 60:75-79PubMedGoogle Scholar
  142. 142.
    Fedele L, Bianchi S, Di Nola G et al (1994) The recurrence of endometriosis. Ann N Y Acad Sci 734:358-364PubMedCrossRefGoogle Scholar
  143. 143.
    Ghezzi F, Beretta P, Franchi M et al (2001) Recurrence of endometriosis and anatomical location of the primary lesion. Fertil Steril 75:136-140PubMedCrossRefGoogle Scholar
  144. 144.
    Simon C, Guttierez A, Vidal A et al (1994) Outcome of patients with endometriosis in assisted reproduction: results from in-vitro fertilization and oocyte donation. Hum Reprod 9:725-729PubMedGoogle Scholar
  145. 145.
    Arici A, Oral E, Bukulmez O et al (1996) The effect of endometriosis on implantation: results from the Yale University in vitro fertilization and embryo transfer program. Fertil Steril 65:603-607PubMedGoogle Scholar
  146. 146.
    Diaz I, Navarro J, Blasco L et al (2000) Impact of stage III-IV endometriosis on recipients of sibling oocytes: matched case-control study. Fertil Steril 74:31-34PubMedCrossRefGoogle Scholar
  147. 147.
    Barnhart K, Dunsmoor-Su R, Coutifaris C (2002) Effect of endometriosis on in vitro fertilization. Fertil Steril 77(6):1148-1155PubMedCrossRefGoogle Scholar
  148. 148.
    Bukulmez O, Yarali H, Gurgan T (2001) The presence and extent of endometriosis do not effect clinical pregnancy rate and implantation rates in patients undergoing ICSI. Eur J Obstet Gynecol Reprd Biol 96:102-107CrossRefGoogle Scholar
  149. 149.
    Rosen GE (1992) Treatment of endometriosis-associated infertility. Infert Reprod Med Clin North Am 3:721-730Google Scholar
  150. 150.
    Proctor ML, Smith CA, Farquhar CM, et al (2004) Transcutaneous electrical nerve stimulation and acupuncture for primary dysmenorrhoea (Cochrane Review). In: The Cochrane Library, Issue 3. John Wiley & Sons, Ltd, Chichester, UKGoogle Scholar
  151. 151.
    Ulrich U, Murano R, Skinner MA et al (1998) Women of reproductive age with endometriosis are not osteopenic. Fertil Steril 69:821-825PubMedCrossRefGoogle Scholar
  152. 152.
    Vercellini P, Aimi G, Panazza S et al (1999) A levonorgestrel-releasing intrauterine system for the treatment of dysmenorrhea associated with endometriosis: a pilot study. Fertil Steril 72:505-508PubMedCrossRefGoogle Scholar
  153. 153.
    Tummon IS, Asher LS, Martin JRB et al (1997) Randomized controlled trial of superovulation and insemination for infertility associated with minimai or mild endometriosis. Fertil Steril 68:8-12PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Attila Bokor
    • 1
  • Christel Meuleman
    • 1
  • Thomas D’Hooghe
    • 1
  1. 1.Leuven University Fertility Center, UZ GasthuisbergK.U. LeuvenBelgium

Personalised recommendations