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Endometriosis reduces ovarian response in controlled ovarian hyperstimulation independent of AMH, AFC, and women’s age measured by follicular output rate (FORT) and number of oocytes retrieved

  • Kristin Nicolaus
  • Dominik Bräuer
  • Robert Sczesny
  • Jorge Jimenez-Cruz
  • Klaus Bühler
  • Ines Hoppe
  • Ingo B. RunnebaumEmail author
Gynecologic Endocrinology and Reproductive Medicine
  • 32 Downloads

Abstract

Purpose

To determine the influence of endometriosis on the ovarian response during controlled ovarian hyperstimulation measured by number of oocytes retrieved and the follicular output rate (FORT).

Methods

A retrospective, single center study included 96 women, who underwent ICSI treatments for male factor infertility according to World Health Organisation between 2016 until 2018. A total of 96 patients were included in the study with 205 fresh ICSI cycles. The study group included 26 patients with endometriosis after surgical and medical treatment; the control group included 70 patients without endometriosis. The women with endometriosis underwent 47 and the control group 158 ICSI cycles. Women underwent fresh intracytoplasmatic sperm injection cycles after controlled ovarian hyperstimulation following a GnRH-antagonist protocol. The FORT was calculated as the ratio of pre-ovulatory follicle count × 100/small antral follicle count at baseline.

Results

A lower number of retrieved oocytes (5.89 vs. 7.25, p = 0.045), lower FORT (75.67 vs. 94.63, p = 0.046), lower number of metaphase II oocytes (4.87 vs. 6.04, p = 0.046), and lower fertilization rate after intracytoplasmatic sperm injection (40.61 vs. 57.76, p = 0.003) were found in women with endometriosis compared to women without endometriosis. The number of oocyctes retrieved was 0.71 lower in the group with endometriosis than in the group without (p = 0.026). The FORT was 24.55% lower in the group with endometriosis (p = 0.025).

Conclusions

Endometriosis reduces the FORT and the number of metaphase-II oocytes after controlled ovarian hyperstimulation independly of women’s age, antral follicle count and anti-Müllerian hormone.

Keywords

Endometriosis Follicular output rate Ovarian response Retrieved oocytes Controlled ovarian hyperstimulation 

Notes

Acknowledgements

The authors wish to thank Dr. Thomas Lehmann, Institute of Medical Statistics, Informatics and Documentation, University Hospital, Friedrich-Schiller-University Jena, Germany for assistance with statistical analysis.

Author contributions

KN: protocol/project development, data collection and data management and manuscript writing/editing. DB: data collection. RS: data collection. JJ-C: statistics and data management. IH: providing the embryological data. KB: project development. IBR: manuscript writing/editing.

Compliance with ethical standards

Conflict of interest

The authors have no conflicts of interest to declare.

References

  1. 1.
    Kennedy S, Bergqvist A, Chapron C, D’Hooghe T, Dunselman G, Greb R, Hummelshoj L, Prentice A, Saridogan E (2005) ESHRE guideline for the diagnosis and treatment of endometriosis. Hum Reprod 20:2698–2704CrossRefGoogle Scholar
  2. 2.
    Giudice LC, Kao LC (2004) Endometriosis. Lancet 364:1789–1799CrossRefGoogle Scholar
  3. 3.
    Ozkan S, Murk W, Arici A (2008) Endometriosis and infertility: epidemiology and evidence-based treatments. Ann NY Acad Sci 1127:92–100CrossRefGoogle Scholar
  4. 4.
    Mio Y, Toda T, Harada T, Terakawa N (1992) Luteinized unruptured follcile in the early stages of endometriosis as a cause of unexplained infertility. Am J Obstet Gynecol 167:271–273CrossRefGoogle Scholar
  5. 5.
    Yoo JH, Cha SH, Park CW, Kim JY, Yang KM, Song IO, Koong MK, Kang IS, Kim HO (2011) Serum anti-Mullerian hormone is a better predictor of ovarian response than FSH and age in IVF patients with endometriosis. Clin Exp Reprod Med 38:222–227CrossRefGoogle Scholar
  6. 6.
    Opøien HK, Fedorcsak P, Omland AK, Abyholm T, Bjercke S, Ertzeid D, Oldereid N, Mellembakken JR, Tanbo T (2012) In vitro fertilization is a successful treatment in endometriosis-associated infertility. Fertil Steril 97:912–918CrossRefGoogle Scholar
  7. 7.
    Ozkan S, Arici A (2009) Advanced in treatment options of endometriosis. Gynecol Obstet Invest 67:81–91CrossRefGoogle Scholar
  8. 8.
  9. 9.
    Fauser BC, Diedrich K, Devroey P, Evian Annual Reproduction Workshop Group 2007 (2008) Predictors of ovarian response: progress towards individualized treatment in ovulation induction and ovarian stimulation. Hum Reprod Update 14(1):1–14CrossRefGoogle Scholar
  10. 10.
    Tsakos E, Tolikas A, Daniilidis A, Asimakopoulos B (2014) Predictive value of anti-Müllerian hormone, follicle-stimulating hormone and antral follicle count on the outcome of ovarian stimulation in women following GnRH-antagonist protocol for IVF/ET. Arch Gynecol Obstet 290:1249–1253CrossRefGoogle Scholar
  11. 11.
    Zhu M, Wang S, Yi S, Huang X, Meng J, Chen L, Sun H, Zhou J (2019) A predictive formula for selecting individual FSH starting dose based on ovarian reserve markers in IVF/ICSI cycles. Arch Gynecol Obstet.  https://doi.org/10.1007/s00404-019-05156-2 CrossRefPubMedGoogle Scholar
  12. 12.
    Nelson SM, Yates RW, Lyall H, Jamieson M, Traynor I, Gaudoin M, Mitchell P, Ambrose P, Fleming R (2009) Anti-Müllerian hormone-based approach to controlled ovarian stimulation for assisted conception. Hum Reprod 24(4):867–875CrossRefGoogle Scholar
  13. 13.
    Broer SL, Broekmans FJ, Laven JS, Fauser BC (2014) Anti-Müllerian hormone: ovarian reserve testing and its potential clinical implications. Hum Reprod Update 20(5):688–701CrossRefGoogle Scholar
  14. 14.
    Pellicer A, Oliveira N, Ruiz A, Remohi J, Simon C (1995) Exploring the mechanism(s) of endometriosis-related infertility: an analysis of embryo development and implantation in assisted reproduction. Hum Reprod 2:91–97CrossRefGoogle Scholar
  15. 15.
    Panidis DK, Matalliotakis IM (1998) Subfertility associated with minimal to mid endometriosis. Main mechanisms. J Reprod Med 43:1034–1042PubMedGoogle Scholar
  16. 16.
    Yovich JL, Matson PL, Richardson PA, Hilliard C (1988) Hormonal profiles and embryo quality in women with severe endometriosis treated by in vitro fertilization and embryo transfer. Fertil Steril 50:308–313CrossRefGoogle Scholar
  17. 17.
    Aboulghar MA, Mansour RT, Serour GI, Al-Inany HG, Aboulghar MM (2003) The outcome of in vitro fertilization in advanced endometriosis with previous surgery: a case-controlled study. Am J Obstet Gynecol 188:371–375CrossRefGoogle Scholar
  18. 18.
    Grynberg M, Labrosse J (2019) Understanding follicular output rate (FORT) and its Implications for POSEIDON criteria. Front Endocrinol (Lausanne) 10:246CrossRefGoogle Scholar
  19. 19.
    Genro VK, Grynberg M, Scheffer JB, Roux I, Frydman R, Fanchin R (2011) Serum anti-Mullerian hormone levels are negatively related to follicular output rate (FORT) in normo-cycling women undergoing controlled ovarian hyperstimulation. Hum Reprod 26:671–677CrossRefGoogle Scholar
  20. 20.
    Matalliotakis I, Cakmal H, Mahutte N, Fragouli Y, Arici A, Sakkas D (2007) 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 88:1568–1572CrossRefGoogle Scholar
  21. 21.
    Nakamura M, Yamashita Y, Hayashi A, Saito N, Yu M, Hayashi M, Terai Y, Ohmichi M (2017) Analyzing the risk factors for a diminished oocyte retrieval rate under controlled ovarian stimulation. Reprod Med Biol 16:40–44CrossRefGoogle Scholar
  22. 22.
    Dong X, Liao X, Wang R, Zhang H (2013) The impact of endometriosis on IVF/ICSI outcomes. Int J Clinc Exp Pathol 6:1911–1918Google Scholar
  23. 23.
    Barnhart K, Dunsmoor-Su R, Coutifaris C (2002) Effect of endometriosis on in vitro fertilization. Fertil Steril 77:1148–1155CrossRefGoogle Scholar
  24. 24.
    Garrido N, Navarro J, Remohi J, Simon C, Pellicer A (2000) follicular hormonal environment and embryo quality in women with endometriosis. Reprod Update 6:67–74CrossRefGoogle Scholar
  25. 25.
    Safdarian L, Ghalandarpoor Attar SN, Aleyasin A, Aghahosseini M, Sarfjoo FS, Hosseinimousa S (2018) Investigation of anti-mullerian hormone (AMH) level and ovarian response in infertile women with endometriosis in IVF cycles. Int J Reprod Biomed 16(11):719–722Google Scholar
  26. 26.
    Ashrafi M, Fakheri T, Kiani K, Sadeghi M, Akhoond MR (2014) Impact oft he endometrioma on ovarian response and pregnancy rate in in vitro fertilization cycles. Int J Fertil Steril 8:29–34PubMedPubMedCentralGoogle Scholar
  27. 27.
    Senapti S, Barnhart K (2011) Managing endometriosis-associated infertility. Clin Obstet Gynecol 54:720–726CrossRefGoogle Scholar
  28. 28.
    Harb HM, Gallos ID, Chu J, Harb M, Coomarasamy A (2013) The effect of endometriosis on in vitro fertilzation outcome: a systematic review and meta-analysis. BJOG 120:1308–1320CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Gynecology and Reproductive Medicine, University Women’s Hospital Jena, Jena University HospitalFriedrich-Schiller-University JenaJenaGermany
  2. 2.Department of Obstetrics and Prenatal MedicineUniversity Women’s Hospital BonnBonnGermany

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