Skip to main content

Bologna criteria are predictive for ovarian response and live birth in subsequent ovarian stimulation cycles

Archives of Gynecology and Obstetrics volume 299, pages 571–577 (2019)Cite this article

Abstract

Purpose

The ESHRE Working Group on Poor Ovarian Response defined a set of variables to define poor responders, named as the Bologna Criteria, but several concerns have been raised regarding their applicability and prognostic significance. In order to evaluate the clinical relevance of the criteria, we retrospectively analyzed the ovarian response and live birth rates in women who had consecutive IVF attempts, according to their fulfillment of the criteria.

Methods

The study group comprised 1153 and 288 women who had two and three consecutive ovarian stimulation (OS) cycles between May 2010 and January 2017, respectively. We compared the ovarian response and live birth rates in subsequent IVF attempts of Bologna criteria-defined poor responder women and women who did not fulfill the Bologna criteria.

Results

Women who fulfilled the criteria achieved higher rates of poor ovarian response (76.2% vs 14.3% and 60.3% vs 13.4%) and lower live birth rates (14.6% vs 33.3% and 12.9% vs 34.3%) in their second and third OS cycles, respectively (both p < 0.001) compared to women who did not fulfill the criteria. The former group also had lower number of oocytes and lower likelihood of having embryo transfer in their subsequent OS cycles. The criteria were able to predict both ovarian response and clinical outcome in the subsequent cycle in < 40-year-old women, whereas they were predictive only for the ovarian response but not for the clinical outcome in women over 40 years of age, who exhibited very low live birth rates regardless of the fulfillment of the criteria.

Conclusions

The results of this study show that the Bologna criteria are clinically relevant in terms of prediction of ovarian response and clinical outcome in subsequent OS cycles.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1

References

  1. Ferraretti AP, La Marca A, Fauser BC, Tarlatzis B, Nargund G, Gianaroli L, On Behalf of the ESHRE Working Group on Poor Ovarian Response Definition (2011) ESHRE consensus on the definition of ‘poor response’ to ovarian stimulation for in vitro fertilization: the Bologna criteria. Hum Reprod 26:1616–1624

    Article  CAS  PubMed  Google Scholar 

  2. Boots CE, Bernardi LA (2018) Bologna criteria: clinically or academically relevant? Fertil Steril 109:59–60

    Article  PubMed  Google Scholar 

  3. De Ziegler D, Streuli I, Meldrum DR, Chapron C (2011) The value of growth hormone supplements in ART for poor ovarian responders. Fertil Steril 96:1069–1076

    Article  CAS  PubMed  Google Scholar 

  4. Frydman R (2011) Poor responders: still a problem. Fertil Steril 96:1057

    Article  PubMed  Google Scholar 

  5. La Marca A, Grisendi V, Giulini S, Sighinolfi G, Tirelli A, Argento C, Re C, Tagliasacchi D, Marsella T, Sunkara SK (2015) Live birth rates in the different combinations of the Bologna criteria poor ovarian responders: a validation study. J Assist Reprod Genet 32:931–937

    Article  PubMed  PubMed Central  Google Scholar 

  6. Papathanasiou A (2014) Implementing the ESHRE ‘poor responder’ criteria in research studies: methodological implications. Hum Reprod 29:1835–1838

    Article  PubMed  Google Scholar 

  7. Polyzos N, Devroey P (2011) A systematic review of randomized trials for the treatment of poor ovarian responders: is there any light at the end of the tunnel? Fertil Steril 96:1058–1061

    Article  PubMed  Google Scholar 

  8. Younis JS (2012) The Bologna criteria for poor ovarian response; has the job been accomplished? Hum Reprod 27:1874–1875

    Article  PubMed  Google Scholar 

  9. Younis JS, Ben-Ami M, Ben-Shlomo I (2015) The Bologna criteria for poor ovarian response: a contemporary critical appraisal. J Ovarian Res 8:76

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Boza A, Yildiz Oguz S, Misirlioglu S, Yakin K, Urman B (2018) Utilization of the Bologna criteria: a promise unfulfilled? A review of published and unpublished/ongoing trials. Fertil Steril 109:104–109

    Article  PubMed  Google Scholar 

  11. Busnelli A, Papaleo E, Del Prato D, La Vecchia I, Iachini E, Paffoni A, Candiani M, Somigliana E (2015) A retrospective evaluation of prognosis and cost-effectiveness of IVF in poor responders according to the Bologna criteria. Hum Reprod 30:315–322

    Article  PubMed  Google Scholar 

  12. Busnelli A, Somigliana E (2018) Prognosis and cost-effectiveness of IVF in poor responders according to the Bologna criteria. Minerva Ginecol 70:89–98

    PubMed  Google Scholar 

  13. Eppsteiner EE, Sparks AET, Liu D, Van Voorhis BJ (2014) Change in oocyte yield in repeated in vitro fertilization cycles: effect of ovarian reserve. Fertil Steril 101:399–402

    Article  PubMed  Google Scholar 

  14. Oudendijk JF, Yarde F, Eijkemans MJC, Broekmans FJM, Broer SL (2012) The poor responders in IVF: is the prognosis always poor? A systematic review. Hum Reprod Update 18:1–11

    Article  CAS  PubMed  Google Scholar 

  15. Ferraretti AP, La Marca A, Fauser BC, Tarlatzis B, Nargund G, Gianaroli L (2012) Reply: The Bologna criteria for poor ovarian response; has the job been accomplished? Hum Reprod 27:1875–1876

    Article  Google Scholar 

  16. Ferraretti AP, Gianaroli L (2014) The Bologna criteria for the definition of poor responders: is there a need for revision? Hum Reprod 29:1942–1945

    Article  Google Scholar 

  17. Sallam HN, Ezzeldin F, Agameya AF, Abdel-Rahman AF, El-Garem YH (2012) The definition of “poor response”: Bologna criteria. Hum Reprod 27:626–627

    Article  PubMed  Google Scholar 

  18. Venetis CA (2014) The Bologna criteria for poor ovarian response: the good, the bad and the way forward. Hum Reprod 29:1839–1841

    Article  PubMed  Google Scholar 

  19. Papathanasiou A, Searle BJ, King NMA, Bhattacharya S (2016) Trends in ‘poor responder’ research: lessons learned from RCTs in assisted conception. Hum Reprod Update 22:306–319

    Article  PubMed  Google Scholar 

  20. Alviggi C, Andersen CY, Buehler K, Conforti A, De Placido G, Esteves SC, Fischer R, Galliano D, Polyzos NP, Sunkara SK, Ubaldi FM, Humaidan P, Poseidon Group (Patient-Oriented Strategies Encompassing Individualized Oocyte Number) (2016) A new more detailed stratification of low responders to ovarian stimulation: from a poor ovarian response to a low prognosis concept. Fertil Steril 105:1452–1453

    Article  PubMed  Google Scholar 

  21. Polyzos NP, Sunkara SK (2015) Sub-optimal responders following controlled ovarian stimulation: an overlooked group? Hum Reprod 30:2005–2008

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

None.

Author information

Affiliations

  1. The Division of Reproductive Endocrinology and Infertility, Department of Obstetrics and Gynecology, Koc University School of Medicine, Davutpasa Cad. No:4, Topkapi, 34010, Istanbul, Turkey

    Kayhan Yakin, Ozgur Oktem & Bulent Urman

  2. Assisted Reproduction Unit, American Hospital Women’s Health Center, Istanbul, Turkey

    Kayhan Yakin, Basak Balaban & Bulent Urman

Authors
  1. Kayhan Yakin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ozgur Oktem
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Basak Balaban
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bulent Urman
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

KY: Project development, data collection, manuscript writing. OO: Data analysis, manuscript writing. BB: Data collection. BU: Manuscript writing/editing.

Corresponding author

Correspondence to Kayhan Yakin.

Ethics declarations

Conflict of interest

Kayhan Yakin declares that he has no conflict of interest. Ozgur Oktem declares that he has no conflict of interest. Basak Balaban declares that she has no conflict of interest. Bulent Urman declares that he has no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. The study was approved by the Koc University Committee on Human Research: 2015.013.IRB2.006 (chr@ku.edu.tr).

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Yakin, K., Oktem, O., Balaban, B. et al. Bologna criteria are predictive for ovarian response and live birth in subsequent ovarian stimulation cycles. Arch Gynecol Obstet 299, 571–577 (2019). https://doi.org/10.1007/s00404-018-4987-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00404-018-4987-y

Keywords

  • Bologna criteria
  • Poor responder
  • Ovarian response
  • Live birth