Background/Aims: To analyze whether the presence of endometriosis per se is associated with inferior pregnancy rates in women undergoing in vitro fertilization (IVF). Methods: Between July 2005 and November 2012, a total of 485 patients with endometriosis under the age of 38 years undergoing their first IVF attempt at our center were included; 72 patients had minimal-mild disease and the remaining 413 patients had moderate-severe disease. 131 patients with laparoscopically confirmed tubal factor infertility not harboring endometriosis and hydrosalpinx under the age of 38 years undergoing their first IVF attempt at our center served as the control group. Results: The bilateral antral follicle count and controlled ovarian hyperstimulation response were diminished in the moderate-severe group. However, the implantation, clinical pregnancy, miscarriage and live birth rates were comparable among the three groups. The recurrence of endometrioma following pre-IVF cystectomy was not associated with inferior pregnancy rates. Female age, bilateral antral follicle count and number of embryos transferred were noted to be significant independent predictors of live birth. Conclusion: We conclude that neither the presence nor the extent of endometriosis have any detrimental effect on IVF pregnancy rates.

1.
Eskenazi B, Warner ML: Epidemiology of endometriosis. Obstet Gynecol Clin North Am 1997;24:235-258.
2.
Berube S, Marcoux S, Maheux R: Characteristics related to the prevalence of minimal or mild endometriosis in infertile women. Canadian Collaborative Group on Endometriosis. Epidemiology 1998;9:504-510.
3.
Kennedy S, Bergqvist A, Chapron C, et al: ESHRE guideline for the diagnosis and treatment of endometriosis. Hum Reprod 2005;20:2698-2704.
4.
Kuivasaari P, Hippelainen 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.
5.
Koch J, Rowan K, Rombauts L, Yazdani A, Chapman M, Johnson N: Endometriosis and infertility - a consensus statement from ACCEPT (Australasian CREI Consensus Expert Panel on Trial evidence). Aust NZ J Obstet Gynaecol 2012;52:513-522.
6.
Coccia ME, Rizzello F, Mariani G, Bulletti C, Palagiano A, Scarselli G: Impact of endometriosis on in-vitro fertilization and embryo transfer cycles in young women: a stage-dependent interference. Acta Obstet Gynecol Scand 2011;90:1232-1238.
7.
Barnhart K, Dunsmoor-Su R, Coutifaris C: Effect of endometriosis on in vitro fertilization. Fertil Steril 2002;77:1148-1155.
8.
Harb HM, Gallos ID, Chu J, Harb M, Coomarasamy A: The effect of endometriosis on in vitro fertilisation outcome: a systematic review and meta-analysis. BJOG 2013;120:1308-1320.
10.
Opoien HK, Fedorcsak P, Omland AK, et al: In vitro fertilization is a successful treatment in endometriosis-associated infertility. Fertil Steril 2012;97:912-918.
11.
Revised American Society for Reproductive Medicine classification of endometriosis: 1996. Fertil Steril 1997;67:817-821.
12.
Savelli L: Transvaginal sonography for the assessment of ovarian and pelvic endometriosis: how deep is our understanding? Ultrasound Obstet Gynecol 2009;33:497-501.
13.
Gelbaya TA, Gordts S, D'Hooghe TM, Gergolet M, Nardo LG: Management of endometrioma prior to IVF: compliance with ESHRE guidelines. Reprod Biomed Online 2010;21:325-330.
14.
Garcia-Velasco JA, Mahutte NG, Corona J, 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.
15.
Garcia-Velasco JA, Somigliana E: Management of endometriomas in women requiring IVF: to touch or not to touch. Hum Reprod 2009;24:496-501.
16.
Surrey ES: Endometriosis and assisted reproductive technologies: maximizing outcomes. Semin Reprod Med 2013;31:154-163.
17.
Yarali H, Esinler I, Polat M, Bozdag G, Tiras B: Antagonist/letrozole protocol in poor ovarian responders for intracytoplasmic sperm injection: a comparative study with the microdose flare-up protocol. Fertil Steril 2009;92:231-235.
18.
Bozdag G, Esinler I, Yarali H: Pretreatment with oral contraceptive pills does not influence the pregnancy rate in the long leuprolide acetate protocol. Gynecol Obstet Invest 2012;73:53-57.
19.
Esinler I, Bozdag G, Arikan I, Demir B, Yarali H: Endometrioma ≤3 cm in diameter per se does not affect ovarian reserve in intracytoplasmic sperm injection cycles. Gynecol Obstet Invest 2012;74:261-264.
20.
Wardle PG, Mitchell JD, McLaughlin EA, Ray BD, McDermott A, Hull MG: Endometriosis and ovulatory disorder: reduced fertilisation in vitro compared with tubal and unexplained infertility. Lancet 1985;2:236-239.
21.
Arici A, Oral E, Bukulmez O, Duleba A, Olive DL, Jones EE: The effect of endometriosis on implantation: results from the Yale University in vitro fertilization and embryo transfer program. Fertil Steril 1996;65:603-607.
22.
Matson PL, Yovich JL: The treatment of infertility associated with endometriosis by in vitro fertilization. Fertil Steril 1986;46:432-434.
23.
Meden-Vrtovec H, Tomazevic T, Verdenik I: Infertility treatment by in vitro fertilization in patients with minimal or mild endometriosis. Clin Exp Obstet Gynecol 2000;27:191-193.
24.
Pal L, Shifren 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.
25.
Tanbo T, Omland A, Dale PO, Abyholm T: In vitro fertilization/embryo transfer in unexplained infertility and minimal peritoneal endometriosis. Acta Obstet Gynecol Scand 1995;74:539-543.
26.
Azem F, Lessing JB, Geva E, 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.
27.
Oehninger S, Acosta AA, Kreiner D, Muasher SJ, Jones HW Jr, Rosenwaks Z: In vitro fertilization and embryo transfer (IVF/ET): an established and successful therapy for endometriosis. J In Vitro Fert Embryo Transf 1988;5:249-256.
28.
Al-Fadhli R, Kelly SM, Tulandi T, Tanr SL: Effects of different stages of endometriosis on the outcome of in vitro fertilization. J Obstet Gynaecol Canada 2006;28:888-891.
29.
Matalliotakis IM, Cakmak H, Mahutte N, Fragouli Y, Arici A, Sakkas D: Women with advanced-stage endometriosis and previous surgery respond less well to gonadotropin stimulation, but have similar IVF implantation and delivery rates compared with women with tubal factor infertility. Fertil Steril 2007;88:1568-1572.
30.
Bergendal 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.
31.
Somigliana E, Arnoldi M, Benaglia L, Iemmello R, Nicolosi AE, Ragni G: IVF-ICSI outcome in women operated on for bilateral endometriomas. Hum Reprod 2008;23:1526-1530.
32.
Reinblatt SL, Ishai L, Shehata F, Son WY, Tulandi T, Almog B: Effects of ovarian endometrioma on embryo quality. Fertil Steril 2011;95:2700-2702.
33.
Yanushpolsky EH, Best CL, Jackson KV, Clarke RN, Barbieri RL, Hornstein MD: Effects of endometriomas on ooccyte quality, embryo quality, and pregnancy rates in in-vitro fertilization cycles: a prospective, case-controlled study. J Assist Reprod Genet 1998;15:193-197.
34.
Pellicer A, Oliveira N, Ruiz A, Remohi J, Simon C: Exploring the mechanism(s) of endometriosis-related infertility: an analysis of embryo development and implantation in assisted reproduction. Hum Reprod 1995;10(suppl 2):91-97.
35.
Kumbak B, Kahraman S, Karlikaya G, Lacin S, Guney A: In vitro fertilization in normoresponder patients with endometriomas: comparison with basal simple ovarian cysts. Gynecol Obstet Invest 2008;65:212-216.
36.
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.
37.
Tinkanen H, Kujansuu E: In vitro fertilization in patients with ovarian endometriomas. Acta Obstet Gynecol Scand 2000;79:119-122.
38.
Tocci A, Lucchini C, Minasi MG, Greco E: Unilateral ovarian endometriotic cysts do not impair follicles development, oocyte and embryo quality: report on eight controlled ovarian hyperstimulations and ICSI cycles. Hum Reprod 2010;25:288-289; author reply 289.
39.
Cakmak H, Taylor HS: Implantation failure: molecular mechanisms and clinical treatment. Hum Reprod Update 2011;17:242-253.
40.
Diaz I, Navarro J, Blasco L, Simon C, Pellicer A, Remohi J: Impact of stage III-IV endometriosis on recipients of sibling oocytes: matched case-control study. Fertil Steril 2000;74:31-34.
41.
Prapas Y, Goudakou M, Matalliotakis I, et al: History of endometriosis may adversely affect the outcome in menopausal recipients of sibling oocytes. Reprod Biomed Online 2012;25:543-548.
42.
Dan H, Limin F: Laparoscopic ovarian cystectomy versus fenestration/coagulation or laser vaporization for the treatment of endometriomas: a meta-analysis of randomized controlled trials. Gynecol Obstet Invest 2013;76:75-82.
43.
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;191:597-606; discussion 607.
44.
Ballester M, Oppenheimer A, Mathieu d'Argent E, et al: Deep infiltrating endometriosis is a determinant factor of cumulative pregnancy rate after intracytoplasmic sperm injection/in vitro fertilization cycles in patients with endometriomas. Fertil Steril 2012;97:367-372.
45.
Barri PN, Coroleu B, Tur R, Barri-Soldevila PN, Rodriguez I: Endometriosis-associated infertility: surgery and IVF, a comprehensive therapeutic approach. Reprod Biomed Online 2010;21:179-185.
46.
Douay-Hauser N, Yazbeck C, Walker F, Luton D, Madelenat P, Koskas M: Infertile women with deep and intraperitoneal endometriosis: comparison of fertility outcome according to the extent of surgery. J Minim Invasive Gynecol 2011;18:622-628.
47.
Xue Q, Zeng C, Xu Y, et al: Clinical effect on women with different types of endometriosis-related infertility treated by conservative surgery (in Chinese). Zhonghua Fu Chan Ke Za Zhi 2013;48:16-19.
48.
Schliep KC, Stanford JB, Chen Z, et al: Interrater and intrarater reliability in the diagnosis and staging of endometriosis. Obstet Gynecol 2012;120:104-112.
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