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Live birth rates in the different combinations of the Bologna criteria poor ovarian responders: a validation study

Journal of Assisted Reproduction and Genetics volume 32, pages 931–937 (2015)Cite this article

Abstract

Purpose

to compare the baseline characteristics and chance of live birth in the different categories of poor responders identified by the combinations of the Bologna criteria and establish whether these groups comprise a homogenous population.

Methods

database containing clinical and laboratory information on IVF treatment cycles carried out at the Mother-Infant Department of the University Hospital of Modena between year 2007 and 2011 was analysed. This data was collected prospectively and recorded in the registered database of the fertility centre. Eight hundred and thirty women fulfilled the inclusion/ exclusion criteria of the study and 210 women fulfilled the Bologna criteria definition for poor ovarian response (POR). Five categories of poor responders were identified by different combinations of the Bologna criteria.

Results

There were no significant differences in female age, AFC, AMH, cycle cancellation rate and number of retrieved oocytes between the five groups. The live birth rate ranged between 5.5 and 7.4 % and was not statistically different in the five different categories of women defined as poor responders according to the Bologna criteria.

Conclusion

The study demonstrates that the different groups of poor responders based on the Bologna criteria have similar IVF outcomes. This information validates the Bologna criteria definition as women having a uniform poor prognosis and also demonstrates that the Bologna criteria poor responders in the various subgroups represent a homogenous population with similar pre-clinical and clinical outcomes.

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References

  1. La Marca A, Sunkara SK. Individualization of controlled ovarian stimulation in IVF using ovarian reserve markers: from theory to practice. Hum Reprod Update. 2014;20(1):124–40.

    PubMed  Article  Google Scholar 

  2. Ferraretti AP, La Marca A, Fauser BC, Tarlatzis B, Nargund G, Gianaroli L. ESHRE working group on POR definition. Hum Reprod. 2011;26(7):1616–24.

    CAS  PubMed  Article  Google Scholar 

  3. La Marca A, Sighinolfi G, Radi D, Argento C, Baraldi E, Artenisio AC, et al. Anti-mullerian hormone (AMH) as a predictive marker in assisted reproductive technology (ART). Hum Reprod Update. 2010;16(2):113–30.

    PubMed  Article  Google Scholar 

  4. La Marca A, Grisendi V, Giulini S, Argento C, Tirelli A, Dondi G, et al. Individualization of the FSH starting dose in IVF/ICSI cycles using the antral follicle count. J Ovarian Res. 2013;6(1):11.

    PubMed Central  PubMed  Article  Google Scholar 

  5. La Marca A, Dondi G, Sighinolfi G, Giulini S, Papaleo E, Cagnacci A, et al. The ovarian response to controlled stimulation in IVF cycles may be predictive of the age at menopause. Hum Reprod. 2014;29(11):2530–5.

    PubMed  Article  Google Scholar 

  6. Garcia JE, Jones GS, Acosta AA, Wright G. HMG/hCGfollicularmaturation for oocytes aspiration: phase II, 1981. Fertil Steril. 1983;39:174–9.

    CAS  PubMed  Google Scholar 

  7. Raga F, Bonilla-Musoles F, Casan EM, Bonilla F. Recombinant follicle stimulating hormone stimulation in poor responders with normal basal concentrations of follicle stimulating hormone and oestradiol: improved reproductive outcome. Hum Reprod. 1999;14:1431–4.

    CAS  PubMed  Article  Google Scholar 

  8. Faber BM, Mayer J, Cox B, Jones D, Toner JP, Oehninger S, et al. Cessation of gonadotropin-releasing hormone agonist therapy combined with high-dose gonadotropin stimulation yields favorable pregnancy results in low responders. Fertil Steril. 1998;69:826–30.

    CAS  PubMed  Article  Google Scholar 

  9. Shaker A, Yates R, Flemming R, Coutts J, Jamieson M. Absence of effect of adjuvant growth hormone therapy on follicular responses to exogenous gonadotrophins in women: normal and poor responders. Fertil Steril. 1992;58:919–23.

    CAS  PubMed  Google Scholar 

  10. Manzi D, Thorton K, Scott L, Nulsen J. The value of increasing the dose of HMG in women who initially demonstrate a poor response. Fertil Steril. 1994;62:251–6.

    CAS  PubMed  Google Scholar 

  11. Yarmolinskaya M, Land J, Dumoulin J, Evers J. High-dose human menopausal gonadotropin stimulation in poor responders does not improve in vitro fertilization outcome. Fertil Steril. 1996;65:961–5.

    PubMed  Google Scholar 

  12. Bancsi LF, Broekmans FJ, Looman CW, Habbema JD, te Velde ER. Impact of repeated antral follicle counts on the prediction of POR in women undergoing in vitro fertilization. Fertil Steril. 2004;81(1):35–41.

    PubMed  Article  Google Scholar 

  13. Hazout A, Bouchard P, Seifer DB, Aussage P, Junca AM, Cohen-Bacrie P. Serum antimullerian hormone/mullerian- inhibiting substance appears to be a more discriminatory marker of assisted reproductive technology outcome than follicle-stimulating hormone, inhibin B, or estradiol. Fertil Steril. 2004;82:1323–9.

    CAS  PubMed  Article  Google Scholar 

  14. Ebner T, Sommergruber M, Moser M, Shebl O, Schreier-Lechner E, Tews G. Basal level of anti-Mu¨llerian hormone is associated with oocyte quality in stimulated cycles. Hum Reprod. 2006;21:2022–6.

    CAS  PubMed  Article  Google Scholar 

  15. Lekamge DN, Barry M, Kolo M, Lane M, Gilchrist RB, Tremellen KP. Anti-Müllerian hormone as a predictor of IVF outcome. Reprod BioMed Online. 2007;14:602–10.

    CAS  PubMed  Article  Google Scholar 

  16. Sahu B, Oztutrk O, Serhal P, Jayaprakasan K. Do ORTs predict miscarriage in women undergoing assisted reproduction treatment? Eur J Obstet Gynecol Reprod Biol. 2010;153(2):181–4.

    PubMed  Article  Google Scholar 

  17. Younis JS, Jadaon J, Izhaki I, Haddad S, Radin O, Bar-Ami S, et al. A simple multivariate score could predict ovarian reserve, as well as pregnancy rate, in infertile women. Fertil Steril. 2010;94(2):655–61.

    PubMed  Article  Google Scholar 

  18. Karande V, Gleicher N. A rational approach to the management of low responders in IVF. Hum Reprod. 1999;14:1744–9.

    CAS  PubMed  Article  Google Scholar 

  19. Galey-Fontaine J, Cedrin-Durnerin I, Chaibi R, Massin N, Hugues JN. Age andovarian reserve are distinct predictive factors of cycle outcome in low responders. Reprod BioMed Online. 2005;10:94–9.

    PubMed  Article  Google Scholar 

  20. Zhen XM, Qiao J, Li R, Wang LN, Liu P. The clinical analysis of POR in in-vitro-fertilization embryo-transfer among Chinese couples. J Assist Reprod Genet. 2008;25:17–22.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  21. La Marca A, Sighinolfi G, Giulini S, Traglia M, Argento C, Sala C, et al. Normal serum concentrations of anti-Müllerian hormone in women with regular menstrual cycles. Reprod BioMed Online. 2010;21(4):463–9.

    PubMed  Article  Google Scholar 

  22. Timeva T, Milachich T, Antonova I, Arabaji T, Shterev A, Omar HA. Correlation between number of retrieved oocytes and pregnancy rate after in vitro fertilization/intracytoplasmic sperm infection. Sci World J. 2006;6:686–90.

    Article  Google Scholar 

  23. van der Gaast MH, Eijkemans MJ, van der Net JB, de Boer EJ, Burger CW, van Leeuwen FE, et al. Optimum number of oocytes for a successful first IVF treatment cycle. Reprod BioMed Online. 2006;13:476–80.

    PubMed  Article  Google Scholar 

  24. Hendriks DJ, te Velde ER, Looman CW, Bancsi LF, Broekmans FJ. Expected poorovarian response in predicting cumulative pregnancy rates: a powerful tool. Reprod BioMed Online. 2008;17:727–36.

    PubMed  Article  Google Scholar 

  25. Oudendijk JF, Yarde F, Eijkemans MJ, Broekmans FJ, Broer SL. The poor responder in IVF: is the prognosis always poor?: a systematic review. Hum Reprod Update. 2012;18(1):1–11.

    CAS  PubMed  Article  Google Scholar 

  26. Broekmans FJ, Knauff EA, Valkenburg O, Laven JS, Eijkemans MJ, Fauser BC. PCOS according to the Rotterdam consensus criteria: change in prevalence among WHO-II anovulation and association with metabolic factors. BJOG. 2006;113:1210–7.

    CAS  PubMed  Article  Google Scholar 

  27. Papathanasiou A. Implementing the ESHRE ‘poor responder’ criteria in research studies: methodological implications. Hum Reprod. 2014;29(9):1835–8.

    PubMed  Article  Google Scholar 

  28. Venetis CA. The Bologna criteria for POR: the good, the bad and the way forward. Hum Reprod. 2014;29(9):1839–41.

    PubMed  Article  Google Scholar 

  29. Domar A, Gordon K, Garcia-Velasco J, La Marca A, Barriere P, Beligotti F. Understanding the perceptions of and emotional barriers to infertility treatment: a survey in four European countries. Hum Reprod. 2012;27(4):1073–9.

    PubMed  Article  Google Scholar 

  30. Polyzos NP, Nwoye M, Corona R, Blockeel C, Stoop D, Haentjens P, et al. Live birth rates in Bologna poor responders treated with ovarian stimulation for IVF/ICSI. Reprod BioMed Online. 2014;28(4):469–74.

    PubMed  Article  Google Scholar 

  31. Tarlatzis BC, Zepiridis L, Grimbizis G, Bontis J. Clinical management of low ovarian response to stimulation for IVF: a systematic review. Hum Reprod Update. 2003;9:61–76.

    CAS  PubMed  Article  Google Scholar 

  32. Klinkert ER, Broekmans FJ, Looman CW, Te Velde ER. A poor response in the first in vitro fertilization cycle is not necessarily related to a poor prognosis in subsequent cycles. Fertil Steril. 2004;81(5):1247–53.

    PubMed  Article  Google Scholar 

  33. Moolenaar LM, Mohiuddin S, Munro Davie M, Merrilees MA, Broekmans FJ, Mol BW, et al. High live birth rate in the subsequent IVF cycle after first-cyclepoor response among women with mean age 35 and normal FSH. Reprod BioMed Online. 2013;27:362–6.

    PubMed  Article  Google Scholar 

  34. Broer SL, Mol BW, Hendriks D, Broekmans FJ. The role of antimullerian hormone in prediction of outcome after IVF: comparison with the antral follicle count. Fertil Steril. 2009;91(3):705–14.

    CAS  PubMed  Article  Google Scholar 

  35. La Marca A, Nelson SM, Sighinolfi G, Manno M, Baraldi E, Roli L, et al. Anti-Müllerian hormone-based prediction model for a live birth in assisted reproduction. Reprod BioMed Online. 2011;22(4):341–9.

    PubMed  Article  Google Scholar 

  36. Holte J, Brodin T, Berglund L, Hadziosmanovic N, Olovsson M, Bergh T. Antral follicle counts are strongly associated with live-birth rates after assisted reproduction, with superior treatment outcome in women with polycystic varies. Fertil Steril. 2011;96:594–9.

    PubMed  Article  Google Scholar 

  37. Iliodromiti S, Kelsey TW, Wu O, Anderson RA, Nelson SM. The predictive accuracy of anti-Müllerian hormone for live birth after assisted conception: a systematic review and meta-analysis of the literature. Hum Reprod Update. 2014;20(4):560–70.

    CAS  PubMed  Article  Google Scholar 

  38. Arce JC, Klein BM, La Marca A. The rate of high ovarian response in women identified at risk by a high serum AMH level is influenced by the type of gonadotropin. Gynecol Endocrinol. 2014;30(6):444–50.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  39. Lukaszuk K, Kunicki M, Liss J, Lukaszuk M, Jakiel G. Use of ovarian reserve parameters for predicting live births in women undergoing in vitro fertilization. Eur J Obstet Gynecol Reprod Biol. 2013;168:173–7.

    PubMed  Article  Google Scholar 

  40. Brodin T, Hadziosmanovic N, Berglund L, Olovsson M, Holte J. Antimüllerian hormone levels are strongly associated with live-birth rates after assisted reproduction. J Clin Endocrinol Metab. 2013;98:1107–14.

    CAS  PubMed  Article  Google Scholar 

  41. Khader A, Lloyd SM, McConnachie A, Fleming R, Grisendi V, La Marca A, et al. External validation of anti-Müllerian hormone based prediction of live birth in assisted conception. J Ovarian Res. 2013;6:3.

    PubMed Central  PubMed  Article  Google Scholar 

  42. Merhi Z, Zapantis A, Berger DS, Jindal SK. Determining an anti-Mullerian hormone cutoff level to predict clinical pregnancy following in vitro fertilization in women with severely diminished ovarian reserve. J Assist Reprod Genet. 2013;30(10):1361–5.

    PubMed Central  PubMed  Article  Google Scholar 

  43. Elter K, Kavak ZN, Gokaslan H, Pekin T. Antral follicle assessment after down-regulation may be a useful tool for predicting pregnancy loss in in vitro fertilization pregnancies. Gynecol Endocrinol. 2005;21:33–7.

    PubMed  Article  Google Scholar 

  44. Gleicher N, Weghofer A, Barad DH. Anti-Müllerian hormone (AMH) defines, independent of age, low versus good live-birth chances in women with severelydiminished ovarian reserve. Fertil Steril. 2010;94:2824–7.

    CAS  PubMed  Article  Google Scholar 

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Author information

Affiliations

  1. Mother-Infant Department, Institute of Obstetrics and Gynecology, University of Modena and Reggio Emilia, Policlinico di Modena Largo del Pozzo, 41100, Modena, Italy

    Antonio La Marca, Valentina Grisendi, Simone Giulini, Giovanna Sighinolfi, Alessandra Tirelli, Cindy Argento, Claudia Re, Daniela Tagliasacchi & Tiziana Marsella

  2. (SKS) Royal Marsden Hospital, London, UK

    Sesh Kamal Sunkara

Authors
  1. Antonio La Marca
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  2. Valentina Grisendi
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  3. Simone Giulini
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  4. Giovanna Sighinolfi
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  5. Alessandra Tirelli
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  6. Cindy Argento
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  7. Claudia Re
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  8. Daniela Tagliasacchi
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  9. Tiziana Marsella
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  10. Sesh Kamal Sunkara
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Corresponding author

Correspondence to Antonio La Marca.

Additional information

Capsule Bologna criteria identifiy subgroups of poor responders with a homogeneous and low reproductive prognosis.

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Cite this article

La Marca, A., Grisendi, V., Giulini, S. et al. Live birth rates in the different combinations of the Bologna criteria poor ovarian responders: a validation study. J Assist Reprod Genet 32, 931–937 (2015). https://doi.org/10.1007/s10815-015-0476-4

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  • DOI: https://doi.org/10.1007/s10815-015-0476-4

Keywords

  • Poor response
  • Live birth rate
  • Bologna criteria
  • Ovarian reserve
  • AMH
  • AFC