Advertisement

Prognostic factors for assisted reproductive technology in women with endometriosis-related infertility

  • Author Footnotes
    1 These authors contributed equally to this article.
    Chloé Maignien
    Footnotes
    1 These authors contributed equally to this article.
    Affiliations
    Université Paris Descartes, Sorbonne Paris Cité, Faculté de Médecine, Assistance Publique–Hôpitaux de Paris, Hôpital Universitaire Paris Centre, Centre Hospitalier Universitaire Cochin, Department of Gynaecology Obstetrics II and Reproductive Medicine, Paris, France
    Search for articles by this author
  • Author Footnotes
    1 These authors contributed equally to this article.
    Pietro Santulli
    Correspondence
    Corresponding author: Pietro Santulli, MD, PHD.
    Footnotes
    1 These authors contributed equally to this article.
    Affiliations
    Université Paris Descartes, Sorbonne Paris Cité, Faculté de Médecine, Assistance Publique–Hôpitaux de Paris, Hôpital Universitaire Paris Centre, Centre Hospitalier Universitaire Cochin, Department of Gynaecology Obstetrics II and Reproductive Medicine, Paris, France

    Institut Cochin, Institut National de la Santé et de la Recherche Médicale U1016, Laboratoire d’Immunologie and Département de Génetique, Développement et Cancer, Université Paris Descartes, Sorbonne Paris Cité, Paris, France
    Search for articles by this author
  • Vanessa Gayet
    Affiliations
    Université Paris Descartes, Sorbonne Paris Cité, Faculté de Médecine, Assistance Publique–Hôpitaux de Paris, Hôpital Universitaire Paris Centre, Centre Hospitalier Universitaire Cochin, Department of Gynaecology Obstetrics II and Reproductive Medicine, Paris, France
    Search for articles by this author
  • Marie-Christine Lafay-Pillet
    Affiliations
    Université Paris Descartes, Sorbonne Paris Cité, Faculté de Médecine, Assistance Publique–Hôpitaux de Paris, Hôpital Universitaire Paris Centre, Centre Hospitalier Universitaire Cochin, Department of Gynaecology Obstetrics II and Reproductive Medicine, Paris, France
    Search for articles by this author
  • Diane Korb
    Affiliations
    Université Paris Descartes, Sorbonne Paris Cité, Faculté de Médecine, Assistance Publique–Hôpitaux de Paris, Hôpital Universitaire Paris Centre, Centre Hospitalier Universitaire Cochin, Department of Gynaecology Obstetrics II and Reproductive Medicine, Paris, France
    Search for articles by this author
  • Mathilde Bourdon
    Affiliations
    Université Paris Descartes, Sorbonne Paris Cité, Faculté de Médecine, Assistance Publique–Hôpitaux de Paris, Hôpital Universitaire Paris Centre, Centre Hospitalier Universitaire Cochin, Department of Gynaecology Obstetrics II and Reproductive Medicine, Paris, France
    Search for articles by this author
  • Louis Marcellin
    Affiliations
    Université Paris Descartes, Sorbonne Paris Cité, Faculté de Médecine, Assistance Publique–Hôpitaux de Paris, Hôpital Universitaire Paris Centre, Centre Hospitalier Universitaire Cochin, Department of Gynaecology Obstetrics II and Reproductive Medicine, Paris, France

    Institut Cochin, Institut National de la Santé et de la Recherche Médicale U1016, Laboratoire d’Immunologie and Département de Génetique, Développement et Cancer, Université Paris Descartes, Sorbonne Paris Cité, Paris, France
    Search for articles by this author
  • Dominique de Ziegler
    Affiliations
    Université Paris Descartes, Sorbonne Paris Cité, Faculté de Médecine, Assistance Publique–Hôpitaux de Paris, Hôpital Universitaire Paris Centre, Centre Hospitalier Universitaire Cochin, Department of Gynaecology Obstetrics II and Reproductive Medicine, Paris, France
    Search for articles by this author
  • Charles Chapron
    Affiliations
    Université Paris Descartes, Sorbonne Paris Cité, Faculté de Médecine, Assistance Publique–Hôpitaux de Paris, Hôpital Universitaire Paris Centre, Centre Hospitalier Universitaire Cochin, Department of Gynaecology Obstetrics II and Reproductive Medicine, Paris, France

    Institut Cochin, Institut National de la Santé et de la Recherche Médicale U1016, Laboratoire d’Immunologie and Département de Génetique, Développement et Cancer, Université Paris Descartes, Sorbonne Paris Cité, Paris, France
    Search for articles by this author
  • Author Footnotes
    1 These authors contributed equally to this article.
Published:November 26, 2016DOI:https://doi.org/10.1016/j.ajog.2016.11.1042

      Background

      Assisted reproductive technology is one of the therapeutic options offered for managing endometriosis-associated infertility. Yet, published data on assisted reproductive technology outcome in women affected by endometriosis are conflicting and the determinant factors for pregnancy chances unclear.

      Objective

      We sought to evaluate assisted reproductive technology outcomes in a series of 359 endometriosis patients, to identify prognostic factors and determine if there is an impact of the endometriosis phenotype.

      Study Design

      This was a retrospective observational cohort study, including 359 consecutive endometriosis patients undergoing in vitro fertilization or intracytoplasmic sperm injection, from June 2005 through February 2013 at a university hospital. Endometriotic lesions were classified into 3 phenotypes–superficial peritoneal endometriosis, endometrioma, or deep infiltrating endometriosis–based on imaging criteria (transvaginal ultrasound, magnetic resonance imaging); histological proof confirmed the diagnosis in women with a history of surgery for endometriosis. Main outcome measures were clinical pregnancy rates and live birth rates per cycle and per embryo transfer. Prognostic factors of assisted reproductive technology outcome were identified by comparing women who became pregnant and those who did not, using univariate and adjusted multiple logistic regression models.

      Results

      In all, 359 endometriosis patients underwent 720 assisted reproductive technology cycles. In all, 158 (44%) patients became pregnant, and 114 (31.8%) had a live birth. The clinical pregnancy rate and the live birth rate per embryo transfer were 36.4% and 22.8%, respectively. The endometriosis phenotype (superficial endometriosis, endometrioma, or deep infiltrating endometriosis) had no impact on assisted reproductive technology outcomes. After multivariate analysis, history of surgery for endometriosis (odds ratio, 0.14; 95% confidence ratio, 0.06–0.38) or past surgery for endometrioma (odds ratio, 0.39; 95% confidence ratio, 0.18–0.84) were independent factors associated with lower pregnancy rates. Anti-müllerian hormone levels <2 ng/mL (odds ratio, 0.51; 95% confidence ratio, 0.28–0.91) and antral follicle count <10 (odds ratio, 0.27; 95% confidence ratio, 0.14–0.53) were also associated with negative assisted reproductive technology outcomes.

      Conclusion

      The endometriosis phenotype seems to have no impact on assisted reproductive technology results. An altered ovarian reserve and a previous surgery for endometriosis and/or endometrioma are associated with decreased pregnancy rates.

      Key words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to American Journal of Obstetrics & Gynecology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Sampson J.A.
        Metastatic or embolic endometriosis, due to the menstrual dissemination of endometrial tissue into the venous circulation.
        Am J Pathol. 1927; 3: 93-110.43
        • Practice Committee of the American Society for Reproductive Medicine
        Endometriosis and infertility: a committee opinion.
        Fertil Steril. 2012; 98: 591-598
        • Chapron C.
        • Santulli P.
        • Cabri P.
        The pain and daily consequences of living with endometriosis: a qualitative online survey of women in China, France and Russia.
        J Endometr Pelvic Pain Disord. 2015; 7: 89-94
        • Dong X.
        • Liao X.
        • Wang R.
        • Zhang H.
        The impact of endometriosis on IVF/ICSI outcomes.
        Int J Clin Exp Pathol. 2013; 6: 1911-1918
        • de Ziegler D.
        • Borghese B.
        • Chapron C.
        Endometriosis and infertility: pathophysiology and management.
        Lancet. 2010; 376: 730-738
        • Santulli P.
        • Lamau M.C.
        • Marcellin L.
        • et al.
        Endometriosis-related infertility: ovarian endometrioma per se is not associated with presentation for infertility.
        Hum Reprod. 2016; 31: 1765-1775
        • 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
        • Lazzeri L.
        • Di Giovanni A.
        • Exacoustos C.
        • et al.
        Preoperative and postoperative clinical and transvaginal ultrasound findings of adenomyosis in patients with deep infiltrating endometriosis.
        Reprod Sci. 2014; 21: 1027-1033
        • Landi S.
        • Mereu L.
        • Pontrelli G.
        • et al.
        The influence of adenomyosis in patients laparoscopically treated for deep endometriosis.
        J Minim Invasive Gynecol. 2008; 15: 566-570
        • Opøien H.K.
        • Fedorcsak P.
        • Omland A.K.
        • et al.
        In vitro fertilization is a successful treatment in endometriosis-associated infertility.
        Fertil Steril. 2012; 97: 912-918
        • Gupta S.
        • Agarwal A.
        • Agarwal R.
        • Loret de Mola J.R.
        Impact of ovarian endometrioma on assisted reproduction outcomes.
        Reprod Biomed Online. 2006; 13: 349-360
        • Matalliotakis I.M.
        • 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
        • Barbosa M.A.
        • Teixeira D.M.
        • Navarro P.A.
        • Ferriani R.A.
        • Nastri C.O.
        • Martins W.P.
        Impact of endometriosis and its staging on assisted reproduction outcome: systematic review and meta-analysis.
        Ultrasound Obstet Gynecol. 2014; 44: 261-278
        • Barnhart K.
        • Dunsmoor-Su R.
        • Coutifaris C.
        Effect of endometriosis on in vitro fertilization.
        Fertil Steril. 2002; 77: 1148-1155
        • 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
        • Coccia M.E.
        • 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
        • Harb H.M.
        • Gallos I.D.
        • Chu J.
        • Harb M.
        • Coomarasamy A.
        The effect of endometriosis on in vitro fertilization outcome: a systematic review and meta-analysis.
        BJOG. 2013; 120: 1308-1320
        • Hamdan M.
        • Omar S.Z.
        • Dunselman G.
        • Cheong Y.
        Influence of endometriosis on assisted reproductive technology outcomes: a systematic review and meta-analysis.
        Obstet Gynecol. 2015; 125: 79-88
        • Rossi A.C.
        • Prefumo F.
        The effects of surgery for endometriosis on pregnancy outcomes following in vitro fertilization and embryo transfer: a systematic review and meta-analysis.
        Arch Gynecol Obstet. 2016; 294: 647-655
      1. Revised American Society for Reproductive Medicine classification of endometriosis: 1996.
        Fertil Steril. 1997; 67: 817-821
        • Vercellini P.
        • Consonni D.
        • Dridi D.
        • Bracco B.
        • Frattaruolo M.P.
        • Somigliana E.
        Uterine adenomyosis and in vitro fertilization outcome: a systematic review and meta-analysis.
        Hum Reprod. 2014; 29: 964-977
        • Chapron C.
        • Santulli P.
        • de Ziegler D.
        • et al.
        Ovarian endometrioma: severe pelvic pain is associated with deeply infiltrating endometriosis.
        Hum Reprod. 2012; 27: 702-711
        • Abrao M.S.
        • Gonçalves M.O.
        • Dias Jr., J.A.
        • Podgaec S.
        • Chamie L.P.
        • Blasbalg R.
        Comparison between clinical examination, transvaginal sonography and magnetic resonance imaging for the diagnosis of deep endometriosis.
        Hum Reprod. 2007; 22: 3092-3097
        • Piketty M.
        • Chopin N.
        • Dousset B.
        • et al.
        Preoperative work-up for patients with deeply infiltrating endometriosis: transvaginal ultrasonography must definitely be the first-line imaging examination.
        Hum Reprod. 2009; 24: 602-607
        • Guerriero S.
        • Ajossa S.
        • Minguez J.A.
        • et al.
        Accuracy of transvaginal ultrasound for diagnosis of deep endometriosis in uterosacral ligaments, rectovaginal septum, vagina and bladder: systematic review and meta-analysis.
        Ultrasound Obstet Gynecol. 2015; 46: 534-545
        • Kinkel K.
        • Frei K.A.
        • Balleyguier C.
        • Chapron C.
        Diagnosis of endometriosis with imaging: a review.
        Eur Radiol. 2006; 16: 285-298
        • Corwin M.T.
        • Gerscovich E.O.
        • Lamba R.
        • Wilson M.
        • McGahan J.P.
        Differentiation of ovarian endometriomas from hemorrhagic cysts at MR imaging: utility of the T2 dark spot sign.
        Radiology. 2014; 271: 126-132
        • Millischer A.-E.
        • Salomon L.J.
        • Santulli P.
        • Borghese B.
        • Dousset B.
        • Chapron C.
        Fusion imaging for evaluation of deep infiltrating endometriosis: feasibility and preliminary results.
        Ultrasound Obstet Gynecol. 2015; 46: 109-117
        • Medeiros L.R.
        • Rosa M.I.
        • Silva B.R.
        • et al.
        Accuracy of magnetic resonance in deeply infiltrating endometriosis: a systematic review and meta-analysis.
        Arch Gynecol Obstet. 2015; 291: 611-621
        • Chapron C.
        • Lafay-Pillet M.-C.
        • Monceau E.
        • et al.
        Questioning patients about their adolescent history can identify markers associated with deep infiltrating endometriosis.
        Fertil Steril. 2011; 95: 877-881
        • Chapron C.
        • Pietin-Vialle C.
        • Borghese B.
        • Davy C.
        • Foulot H.
        • Chopin N.
        Associated ovarian endometrioma is a marker for greater severity of deeply infiltrating endometriosis.
        Fertil Steril. 2009; 92: 453-457
        • Chapron C.
        • Chopin N.
        • Borghese B.
        • et al.
        Deeply infiltrating endometriosis: pathogenetic implications of the anatomical distribution.
        Hum Reprod. 2006; 21: 1839-1845
        • Dueholm M.
        • Lundorf E.
        Transvaginal ultrasound or MRI for diagnosis of adenomyosis.
        Curr Opin Obstet Gynecol. 2007; 19: 505-512
        • Tocci A.
        • Lucchini C.
        WHO reference values for human semen.
        Hum Reprod Update. 2010; 16: 559
        • Damario M.A.
        • Barmat L.
        • Liu H.C.
        • Davis O.K.
        • Rosenwaks Z.
        Dual suppression with oral contraceptives and gonadotrophin releasing-hormone agonists improves in-vitro fertilization outcome in high responder patients.
        Hum Reprod. 1997; 12: 2359-2365
        • Zegers-Hochschild F.
        • Adamson G.D.
        • de Mouzon J.
        • et al.
        The International Committee for Monitoring Assisted Reproductive Technology (ICMART) and the World Health Organization (WHO) revised glossary on ART terminology, 2009.
        Hum Reprod. 2009; 24: 2683-2687
        • Kolte A.M.
        • Bernardi L.A.
        • Christiansen O.B.
        • et al.
        Terminology for pregnancy loss prior to viability: a consensus statement from the ESHRE early pregnancy special interest group.
        Hum Reprod. 2015; 30: 495-498
        • Sibiude J.
        • Santulli P.
        • Marcellin L.
        • Borghese B.
        • Dousset B.
        • Chapron C.
        Association of history of surgery for endometriosis with severity of deeply infiltrating endometriosis.
        Obstet Gynecol. 2014; 124: 709-717
        • Pabuccu R.
        • Onalan G.
        • Kaya C.
        GnRH agonist and antagonist protocols for stage I-II endometriosis and endometrioma in in vitro fertilization/intracytoplasmic sperm injection cycles.
        Fertil Steril. 2007; 88: 832-839
        • Rodriguez-Purata J.
        • Coroleu B.
        • Tur R.
        • Carrasco B.
        • Rodriguez I.
        • Barri P.N.
        Endometriosis and IVF: are agonists really better? Analysis of 1180 cycles with the propensity score matching.
        Gynecol Endocrinol. 2013; 29: 859-862
        • Streuli I.
        • de Ziegler D.
        • Gayet V.
        • et al.
        In women with endometriosis anti-müllerian hormone levels are decreased only in those with previous endometrioma surgery.
        Hum Reprod. 2012; 27: 3294-3303
        • Somigliana E.
        • Arnoldi M.
        • Benaglia L.
        • Iemmello R.
        • Nicolosi A.E.
        • Ragni G.
        IVF-ICSI outcome in women operated on for bilateral endometriomas.
        Hum Reprod. 2008; 23: 1526-1530
        • Roustan A.
        • Perrin J.
        • Debals-Gonthier M.
        • Paulmyer-Lacroix O.
        • Agostini A.
        • Courbiere B.
        Surgical diminished ovarian reserve after endometrioma cystectomy versus idiopathic DOR: comparison of in vitro fertilization outcome.
        Hum Reprod. 2015; 30: 840-847
        • Long Q.
        • Liu X.
        • Guo S.-W.
        Surgery accelerates the development of endometriosis in mice.
        Am J Obstet Gynecol. 2016; 215: 320.e1-320.e15
        • Liu X.
        • Long Q.
        • Guo S.-W.
        Surgical history and the risk of endometriosis: a hospital-based case-control study.
        Reprod Sci. 2016; 23: 1217-1224
        • Bianchi P.H.M.
        • Pereira R.M.A.
        • Zanatta A.
        • Alegretti J.R.
        • Motta E.L.A.
        • Serafini P.C.
        Extensive excision of deep infiltrative endometriosis before in vitro fertilization significantly improves pregnancy rates.
        J Minim Invasive Gynecol. 2009; 16: 174-180
        • Soriano D.
        • Adler I.
        • Bouaziz J.
        • et al.
        Fertility outcome of laparoscopic treatment in patients with severe endometriosis and repeated in vitro fertilization failures.
        Fertil Steril. 2016; 106: 1264-1269
        • Smith A.D.A.C.
        • Tilling K.
        • Nelson S.M.
        • Lawlor D.A.
        Live-birth rate associated with repeat in vitro fertilization treatment cycles.
        JAMA. 2015; 314: 2654-2662
        • Mijatovic V.
        • Florijn E.
        • Halim N.
        • Schats R.
        • Hompes P.
        Adenomyosis has no adverse effects on IVF/ICSI outcomes in women with endometriosis treated with long-term pituitary down-regulation before IVF/ICSI.
        Eur J Obstet Gynecol Reprod Biol. 2010; 151: 62-65
        • Costello M.F.
        • Lindsay K.
        • McNally G.
        The effect of adenomyosis on in vitro fertilization and intra-cytoplasmic sperm injection treatment outcome.
        Eur J Obstet Gynecol Reprod Biol. 2011; 158: 229-234
        • Martínez-Conejero J.A.
        • Morgan M.
        • Montesinos M.
        • et al.
        Adenomyosis does not affect implantation, but is associated with miscarriage in patients undergoing oocyte donation.
        Fertil Steril. 2011; 96: 943-950
        • Salim R.
        • Riris S.
        • Saab W.
        • Abramov B.
        • Khadum I.
        • Serhal P.
        Adenomyosis reduces pregnancy rates in infertile women undergoing IVF.
        Reprod Biomed Online. 2012; 25: 273-277
        • Maheshwari A.
        • Gurunath S.
        • Fatima F.
        • Bhattacharya S.
        Adenomyosis and subfertility: a systematic review of prevalence, diagnosis, treatment and fertility outcomes.
        Hum Reprod Update. 2012; 18: 374-392
        • Benaglia L.
        • Cardellicchio L.
        • Leonardi M.
        • et al.
        Asymptomatic adenomyosis and embryo implantation in IVF cycles.
        Reprod Biomed Online. 2014; 29: 606-611
        • Ballester M.
        • d’Argent E.M.
        • Morcel K.
        • Belaisch-Allart J.
        • Nisolle M.
        • Daraï E.
        Cumulative pregnancy rate after ICSI-IVF in patients with colorectal endometriosis: results of a multicenter study.
        Hum Reprod. 2012; 27: 1043-1049