Fertility and Sterility
Volume 92, Issue 1 , Pages 75-87 , July 2009

The effect of surgical treatment for endometrioma on in vitro fertilization outcomes: a systematic review and meta-analysis

  • Ioanna Tsoumpou, M.B., Ch.B.

      Affiliations

    • Department of Obstetrics and Gynecology, Royal Lancaster Infirmary, Lancaster, United Kingdom
  • ,
  • Maria Kyrgiou, M.D.

      Affiliations

    • Department of Obstetrics and Gynecology, Lancashire Teaching Hospitals, Preston, United Kingdom
  • ,
  • Tarek A. Gelbaya, M.D.

      Affiliations

    • Department of Reproductive Medicine, St. Mary's Hospital, Central Manchester and Manchester Children's University Hospitals, Manchester, United Kingdom
  • ,
  • Luciano G. Nardo, M.D.

      Affiliations

    • Department of Reproductive Medicine, St. Mary's Hospital, Central Manchester and Manchester Children's University Hospitals, Manchester, United Kingdom
    • Corresponding Author InformationReprint requests: Luciano G. Nardo, M.D., Department of Reproductive Medicine, St. Mary's Hospital, Whitworth Park, Manchester M13 0JH, United Kingdom (FAX: 44-161-224-0957).

Received 26 March 2008 ,Revised 7 May 2008 ,Accepted 15 May 2008.

References 

  1. Farquhar CM. Extracts from the “clinical evidence”. Endometriosis BMJ. 2000;320:1449–1452
  2. Sampson JA. Peritoneal endometriosis due to menstrual dissemination of endometrial tissue into the pelvic cavity. Am J Obstet Gynecol. 1927;14:422–469
  3. Hughesdon PE. The structure of endometrial cysts of the ovary. J Obstet Gynaecol Br Emp. 1957;64:481–487
  4. Brosens IA, Puttemans PJ, Deprest J. The endoscopic localization of endometrial implants in the ovarian chocolate cyst. Fertil Steril. 1994;63:1034–1038
  5. 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
  6. Hachisuga T, Kawarabayashi T. Histopathological analysis of laparoscopically treated ovarian endometriotic cysts with special reference to loss of follicles. Hum Reprod. 2002;17:432–435
  7. Jenkins S, Olive DL, Haney AF. Endometriosis: pathogenetic implications of the anatomic distribution. Obstet Gynecol. 1986;67:335–338
  8. Redwine DB. Ovarian endometriosis: a marker for more extensive pelvic and intestinal disease. Fertil Steril. 1999;72:310–315
  9. Kodama H, Fukuda J, Karube H, Matsui T, Shimizu Y, Tanaka T. Benefit of in vitro fertilization treatment of endometriosis associated infertility. Fertil Steril. 1996;66:974–979
  10. Pal L, Shrifren JL, Isaacson KB, Chang Y, Leykin L, Toth TL. Impact of varying stages of endometriosis on the outcome of in vitro fertilization-embryo transfer. J Assist Reprod Genet. 1998;15:27–31
  11. Rana N, Thomas S, Rotman C, Dmowski WP. Decrease in the size of ovarian endometriomas during ovarian suppression in Stage IV endometriosis. Role of preoperative medical treatment. J Reprod Med. 1996;41:384–392
  12. Farquhar C, Sutton C. The evidence for the management of endometriosis. Curr Opin Obstet Gynecol. 1998;10:321–332
  13. Jones KD, Sutton CJG. Laparoscopic management of ovarian endometriomas: a critical review of current practice. Curr Opin Obstet Gynecol. 2000;12:309–315
  14. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, et al. Meta-analysis of observational studies in epidemiology. A proposal for reporting. JAMA. 2000;283:2008–2012
  15. Dersimonian R, Laird NM. Meta-analysis in the clinical trials. Control Clin Trials. 1986;7:177–188
  16. Garcia-Velasco JA, Mahutte NG, Corona J, Zuniga V, Giles J, Arici A, et al. Removal of endometriomas before in vitro fertilization does not improve fertility outcomes: a matched, case-control study. Fertil Steril. 2004;81:1194–1197
  17. Wong BC, Gillman NC, Oehninger S, Gibbons WE, Stadtmauer LA. Results of in vitro fertilization in patients with endometriomas: is surgical removal beneficial?. Am J Obstet Gynecol. 2004;191:598–607
  18. Huang HY, Lee CL, Lai YM, Chang MY, Chang SY, Soong YK. The outcome of in vitro fertilization and embryo transfer in women with endometriosis failing to conceive after laparoscopic conservative surgery. J Am Assoc Gynecol Laparosc. 1997;4:299–303
  19. Canis M, Pouly JL, Tamburro S, Mage G, Wattiez A, Bruhat MA. Ovarian response during IVF-embryo transfer cycles after laparoscopic ovarian cystectomy for endometriotic cysts of >3cm in diameter. Hum Reprod. 2001;16:2583–2586
  20. dos Reis RM, Correa ILA, De Angelo AG, Manetta LA, de Moura MD, Ferriani RA. In vitro fertilization in patients with ovarian endometrioma. J Assist Reprod Genet. 2004;21:311–314
  21. Isaacs JD, Hines RS, Sopelak VM, Cowan BD. Ovarian endometriomas do not adversely affect pregnancy success following treatment with in vitro fertilization. J Assist Reprod Genet. 1997;14:551–553
  22. Feldberg D, Ashkenazi J, Dicker D, Yeshaya A, Voliovitch I, Goldman JA. Ovarian cyst aspiration during in vitro fertilization/embryo transfer (IVF/ET) cycles. J In Vitro Fert Embryo Transf. 1998;5:372–375
  23. Yanushpolsky E, Best C, Jackson K, Clarke R, Barbieri R, Hornstein M. Effect of endometriomas on oocyte quality, embryo quality, and pregnancy rates in in vitro fertilization cycles: a prospective, case-controlled study. J Assist Reprod Genet. 1998;15:193–197
  24. Aboulghar MA, Mansour RT, Serour GI, Al-Inany HG, Aboulghar MM. The outcome of in vitro fertilization in advanced endometriosis with previous surgery: a case-controlled study. Am J Obstet Gynecol. 2003;188:371–375
  25. Suzuki T, Izumi S, Matsubayashi H, Awaji H, Yoshikata K, Makino T. Impact of ovarian endometrioma on oocytes and pregnancy outcome in in vitro fertilization. Fertil Steril. 2005;83:908–913
  26. Donnez J, Wyns C, Nisolles M. Does ovarian surgery for endometriomas impair the ovarian response to gonadotrophin?. Fertil Steril. 2001;76:662–665
  27. Wyns C, Donnez J. Laser vaporization of ovarian endometriomas: the impact on the response to gonadotrophin stimulation. Gynecol Obstet Fertil. 2003;31:337–342
  28. Ruhlmann C, Vetrano R, Bernaldo DG, Basso F, Rolla E, Delger R. Comparison of laparoscopic versus conventional treatment of ovarian endometrioma. J Am Assoc Gynecol Laparosc. 1996;3(4 Suppl):S44
  29. Hemmings R, Bissonnette F, Bouzayen . Results of laparoscopic treatment of ovarian endometriomas: laparoscopic ovarian fenestration and coagulation. Fertil Steril. 1998;70:527–529
  30. Beretta P, Franchi M, Ghezzi F, Busacca M, Zupi E, Bolis P. Randomized clinical trials of two laparoscopic treatments of endometriomas: cystectomy versus drainage and coagulation. Fertil Steril. 1998;70:1176–1180
  31. Porpora MG, Pultrone DC, Bellavia M, Franco C, Crobu M, Cosmi EV. Reproductive outcome after laparoscopic treatment of endometriosis. Clin Exp Obstet Gynecol. 2002;29:271–273
  32. Yoshida S, Harada T, Iwabe T, Terakawa N. Laparoscopic management of ovarian endometrioma. Gynecol Obstet Invest. 2002;54(Suppl. 1):24–27
  33. Alborzi S, Momtahan M, Parsanezhad ME, Dehbashi S, Zolghadri J, Alborzi S. A prospective randomized study comparing laparoscopic ovarian cystectomy versus fenestration and coagulation in patients with endometriomas. Fertil Steril. 2004;82:1633–1637
  34. Kucera E, Herman H. Reproductive outcome in women with ovarian endometriosis-retrospective analytical study. Ceska Gynekol. 2005;70:431–435
  35. Muzii L, Bellati F, Palaia I, Plotti F, Manci N, Zullo MA, et al. Laparoscopic stripping of endometriomas: a randomized trial on different surgical techniques. Part I: clinical results. Hum Reprod. 2005;20:1981–1986
  36. Fedele L, Bianchi S, Zanconato G, Berlanda N, Raffaelli R, Fontana E. Laparoscopic excision of recurrent endometriomas: long-term outcome and comparison with primary surgery. Fertil Steril. 2006;85:694–699
  37. Muzii L, Bianchi A, Croce C, Manci N. Benedetti Panici PB. Laparoscopic excision of ovarian cysts: is the stripping technique a tissue-sparing procedure?. Fertil Steril. 2002;77:609–614
  38. Matson PL, Yovich JL. The treatment of infertility associated with endometriosis by in vitro fertilization. Fertil Steril. 1986;46:432–434
  39. Begendal A, Naffah S, Nagy C, Bergqvist A, Sjoblom P, Hillensjo T. Outcome of IVF in patients with endometriosis in comparison with tubal-factor infertility. J Assist Reprod Genet. 1998;15:530–534
  40. Azem F, Lessing JB, Geva E, Shahar A, Lerner-Geva L, Yovel I, et al. Patients with stages III and IV endometriosis have a poorer outcome of in vitro fertilization-embryo transfer than patients with tubal infertility. Fertil Steril. 1999;72:1107–1109
  41. Al-Azemi M, Bernal AL, Steele J, Gramsbergen I, Barlow D, Kennedy S. Ovarian response to repeated controlled stimulation in in-vitro fertilization cycles in patients with ovarian endometriosis. Hum Reprod. 2000;15:72–75
  42. Dmowski WP, Pry M, Ding J, Rana N. Cycle-specific and cumulative fecundity in patients with endometriosis who are undergoing controlled ovarian hyperstimulation-intrauterine insemination or in vitro fertilization-embryo transfer. Fertil Steril. 2002;78:750–756
  43. Somigliana E, Infantino M, Benedetti F, Arnoldi M, Calanna G, Ragni G. The presence of ovarian endometriomas is associated with a reduced responsiveness to gonadotrophins. Fertil Steril. 2006;86:192–196
  44. Werbrouck E, Spiessens C, Meuleman C, D'Hooghe T. No difference in cycle pregnancy rate and in cumulative live-birth rate between women with surgically treated minimal to mild endometriosis and women with unexplained infertility after controlled ovarian hyperstimulation and intrauterine insemination. Fertil Steril. 2006;86:566–571
  45. Alborzi S, Ravanbakhsh R, Parsanerzhad ME, Alborzi M, Alborzi S, Dehbashi S. A comparison of follicular response of ovaries to ovulation induction after laparoscopic ovarian cystectomy or fenestration and coagulation versus normal ovaries in patients with endometrioma. Fertil Steril. 2007;88:507–509
  46. Geber S, Ferreira DP, Prates LF, Sales L, Sampaio M. Effects of previous ovarian surgery for endometriosis on the outcome of assisted reproduction treatment. Reprod Biomed Online. 2002;5:162–166
  47. Kuivasaari P, Hippeläinen M, Anttila M, Heinonen S. Effect of endometriosis on IVF/ICSI outcome: stage III/IV endometriosis worsens cumulative pregnancy and live-born rates. Hum Reprod. 2005;20:3130–3135
  48. Fuchs F, Raynal P, Salama S, Guillot E, Le Tohic A, Chis C, et al. Reproductive outcome after laparoscopic treatment of endometriosis in an infertile population. J Gynecol Obstet Biol Reprod (Paris). 2007;36:354–359
  49. Nakagawa K, Ohgi S, Kojima R, Sugawara K, Ito M, Horikawa T, et al. Impact of laparoscopic cystectomy on fecundity of infertile patients with ovarian endometrioma. J Obstet Gynaecol Res. 2007;33:671–676
  50. Marconi G, Vilela M, Quintana R, Sueldo C. Laparoscopic ovarian cystectomy of endometriomas does not affect the ovarian response to gonadotrophin stimulation. Fertil Steril. 2002;78:876–878
  51. Pabuccu R, Onalan G, Goktolga U, Kucuk T, Orhon E, Ceyhan T. Aspiration of ovarian endometriomas before intracytoplasmic sperm injection. Fertil Steril. 2004;82:705–711
  52. Ragni G, Somigliana E, Benedetti F, Paffoni A, Vegetti W, Restelli L, et al. Damage to ovarian reserve associated with laparoscopic excision of endometriomas: a quantitative rather than a qualitative injury. Am J Obstet Gynecol. 2005;193:1908–1914
  53. Demirol A, Guven S, Baykal C, Gurgan T. Effect of endometrioma cystectomy on IVF outcome: a prospective randomized study. Reprod Biomed Online. 2005;12:639–643
  54. Nargund G, Cheng WC, Parsons J. The impact of ovarian cystectomy on ovarian response to stimulation during in-vitro fertilization cycles. Hum Reprod. 1995;11:81–83
  55. Loh FH, Tan AT, Kumar J, Ng SC. Ovarian response after laparoscopic ovarian cystectomy for endometriotic cysts in 132 monitored cycles. Fertil Steril. 1999;72:316–321
  56. Takuma N, Sengoku K, Pan B, Wada K, Yamauchi T, Miyamoto T, et al. Laparoscopic treatment of endometrioma-associated infertility and pregnancy outcome. Gynecol Obstet Invest. 2002;54:30–35
  57. Somigliana E, Ragni G, Benedetti F, Borroni R, Vegetti W, Crosignani PG. Does laparoscopic excision of endometriotic ovarian cysts significantly affect ovarian reserve? Insights from IVF cycles. Hum Reprod. 2003;18:2450–2453
  58. Wu MH, Tsai SJ, Pan HA, Hsiao KY, Chang FM. Three-dimensional power Doppler imaging of ovarian stromal blood flow in women with endometriosis undergoing in vitro fertilization. Ultrasound Obstet Gynecol. 2003;21:480–485
  59. Loo TC, Lin M, Chen SH, Chung MT, Tang HH, Lin LY, et al. Endometrioma undergoing laparoscopic ovarian cystectomy: its influence on the outcome of in vitro fertilization and embryo transfer (IVF-ET). J Assist Reprod Genet. 2005;22:329–333
  60. Esinler I, Bozdag G, Aybar F, Bayar U, Yaradi H. Outcome of in vitro fertilization/intracytoplasmic sperm injection after laparoscopic cystectomy for endometriomas. Fertil Steril. 2006;85:1730–1735
  61. Yazbeck C, Madelenat P, Sifer C, Hazout A, Poncelet C. Ovarian endometriomas: effect of laparoscopic cystectomy on ovarian response in IVF-ET cycles. Gynecol Obstet Fertil. 2006;34:808–812
  62. Matalliotakis I, Cakmak H, Mahutte N, Fragouli Y, Arici A, Sakkas D. Women with advanced-stage endometriosis and previous surgery respond less well to gonadotrophin stimulation, but have similar IVF implantation and delivery rates compared with women with tubal factor infertility. Fertil Steril. 2007;88:1568–1572
  63. Tinkanen H, Kujansuu E. In vitro fertilization in patients with ovarian endometriomas. Acta Obstet Gynecol Scand. 2000;79:119–122
  64. Ho HY, Lee RK, Hwu YM, Lin MH, Su JT, Tsai YC. Poor response of ovaries with endometrioma previously treated with cystectomy to controlled ovarian hyperstimulation. J Assist Reprod Genet. 2002;19:507–511
  65. Suganuma N, Wakahara Y, Ishida D, Asano M, Kitagawa T, Katsumata Y, et al. Pretreatment for ovarian endometrial cyst before in vitro fertilization. Gynecol Obstet Invest. 2002;54(Suppl. 1):36–42
  66. Duru NK, Dede M, Acikel CH, Keskin U, Fidan U, Baser I. Outcome of in vitro fertilization and ovarian response after endometrioma stripping at laparoscopy and laparotomy. J Reprod Med. 2007;52:805–809
  67. Maneschi F, Marasa L, Incadela S, Mazzarese M, Zupi E. Ovarian cortex surrounding benign neoplasms: a histologic study. Am J Obstet Gynecol. 1993;169:388–393
  68. Padilla SL. Ovarian abscess following puncture of an endometrioma during ultrasound-guided oocyte retrieval. Hum Reprod. 1993;8:1282–1283
  69. Yaron Y, Peyser MR, Samuel D, Amit A, Lessing JB. Infected endometriotic cysts secondary to oocyte aspiration for in-vitro fertilization. Hum Reprod. 1994;9:1759–1760
  70. Nargund G, Parsons J. Infected endometriotic cysts secondary to oocyte aspiration for in-vitro fertilization. Hum Reprod. 1995;10:1555
  71. Zanetta G, Lissoni A, Dalla Valle C, Trio D, Pittelli M, Rangoni G. Ultrasound-guided aspiration of endometriomas: possible applications and limitations. Fertil Steril. 1995;64:709–713
  72. Busacca M, Riparini J, Somigliana E, Oggioni G, Izzo S, Vignali M, et al. Postsurgical ovarian failure after laparoscopic excision of bilateral endometriomas. Am J Obstet Gynecol. 2006;195:421–425
  73. Koga K, Takemura Y, Osuga Y, Yoshino O, Hirota Y, Hirata T, et al. Recurrence of ovarian endometrioma after laparoscopic excision. Hum Reprod. 2006;21:2171–2174
  74. Vercellini P, Chapron C, de Giorgi O, Consonni D, Frontino G, Crosignani PG. Coagulation of excision of ovarian endometriomas?. Am J Obstet Gynecol. 2003;188:606–610
  75. Sallam HN, Garcia-Velasco JA, Dias S, Arici A. Long-term pituitary down-regulation before in vitro fertilization (IVF) for women with endometriosis. Cochrane Database Syst Rev. 2006;25:CD004635

 I.T. has nothing to disclose. M.K. has nothing to disclose. T.A.G. has nothing to disclose. L.G.N. has nothing to disclose.

PII: S0015-0282(08)01158-8

doi: 10.1016/j.fertnstert.2008.05.049

Fertility and Sterility
Volume 92, Issue 1 , Pages 75-87 , July 2009