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Modified endometriosis fertility index is more accurate to predict the non-ART pregnancy rate following surgery: a cohort of Chinese women

  • Gynecologic Endocrinology and Reproductive Medicine
  • Published:
Archives of Gynecology and Obstetrics Aims and scope Submit manuscript

Abstract

Objective

To examine whether a modified endometriosis fertility index (EFI) can better predict the rate of pregnancy without assisted reproductive technologies (ART) after laparoscopic surgery in infertile Chinese women with endometriosis.

Methods

564 infertile women undergoing laparoscopy for endometriosis were retrospectively collected from January 2014 to December 2018. 472 patients were used to modify the EFI based on new, optimal cutoffs for its predictor variables. The predictive accuracy of the modified EFI was examined in the other 92 patients.

Results

Among the patients for the EFI modification, the multivariable Cox regression results showed that historical factors made more contribution in predicting non-ART pregnancy rate than surgical factors both in modified EFI (C-index: historical factors 0.617 vs surgical factors 0.558) and original EFI (C-index: historical factors 0.600 vs surgical factors 0.549). No significant relationship between the prior pregnancy and post-operative non-ART pregnancy rates was detected by both modified EFI and original EFI (p = 0.530 and 0.802, respectively). To assess the predictive effect of modified EFI, the two versions of modified EFI not only had higher predictive accuracy (C-index: 0.627 and 0.632) for non-ART pregnancy rates than that of the original EFI (C-index: 0.602) in the patients undergoing surgery during 2014–2017, but also higher than that of the original EFI (C-index: 0.638 and 0.612 vs 0.560) in the externally validated population in 2018.

Conclusions

A modified EFI based on population-specific optimal cutoffs and weights might be more suitable for estimating the rate of non-ART pregnancy after laparoscopic surgery in infertile women with endometriosis.

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References

  1. de Ziegler D, Borghese B, Chapron C (2010) Endometriosis and infertility: pathophysiology and management. Lancet 376:730–738

    Article  PubMed  CAS  Google Scholar 

  2. Eisenberg VH et al (2018) Epidemiology of endometriosis: a large population-based database study from a healthcare provider with 2 million members. BJOG : an international journal of obstetrics and gynaecology 125:55–62

    Article  CAS  Google Scholar 

  3. Dunselman GA et al (2014) ESHRE guideline: management of women with endometriosis. Hum Reprod 29:400–412

    Article  CAS  PubMed  Google Scholar 

  4. Hughes E et al (2007) Ovulation suppression for endometriosis. Cochrane Database Syst Rev 2007:CD000155

    PubMed Central  Google Scholar 

  5. Chern CJ, Beutler E (1976) Biochemical and electrophoretic studies of erythrocyte pyridoxine kinase in white and black Americans. Am J Hum Genet 28:9–17

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Marcoux S, Maheux R, Berube S (1997) Laparoscopic surgery in infertile women with minimal or mild endometriosis. Canadian Collaborative Group on Endometriosis. N Engl J Med 337:217–222

    Article  CAS  PubMed  Google Scholar 

  7. Parazzini F (1999) Ablation of lesions or no treatment in minimal-mild endometriosis in infertile women: a randomized trial. Gruppo Italiano per lo Studio dell’Endometriosi. Hum Reprod 14:1332–1334

    Article  CAS  PubMed  Google Scholar 

  8. Darai E et al (2005) Fertility after laparoscopic colorectal resection for endometriosis: preliminary results. Fertil Steril 84:945–950

    Article  PubMed  Google Scholar 

  9. Meuleman C et al (2014) Clinical outcome after radical excision of moderate-severe endometriosis with or without bowel resection and reanastomosis: a prospective cohort study. Ann Surg 259:522–531

    Article  PubMed  Google Scholar 

  10. de Ziegler D et al (2019) Assisted reproduction in endometriosis. Best Pract Res Clin Endocrinol Metab 33:47–59

    Article  PubMed  Google Scholar 

  11. Hargreave M et al (2019) Association between fertility treatment and cancer risk in children. JAMA 322:2203–2210

    Article  PubMed  PubMed Central  Google Scholar 

  12. (1997) Revised American Society for Reproductive Medicine classification of endometriosis: 1996. Fertility and sterility 67:817–821

  13. Adamson GD et al (1993) Laparoscopic endometriosis treatment: is it better? Fertil Steril 59:35–44

    Article  CAS  PubMed  Google Scholar 

  14. Guzick DS et al (1997) Prediction of pregnancy in infertile women based on the American Society for Reproductive Medicine’s revised classification of endometriosis. Fertil Steril 67:822–829

    Article  CAS  PubMed  Google Scholar 

  15. Vercellini P et al (2006) Reproductive performance, pain recurrence and disease relapse after conservative surgical treatment for endometriosis: the predictive value of the current classification system. Hum Reprod 21:2679–2685

    Article  PubMed  Google Scholar 

  16. Adamson GD (2011) Endometriosis classification: an update. Curr Opin Obstet Gynecol 23:213–220

    Article  PubMed  Google Scholar 

  17. Adamson GD, Pasta DJ (2010) Endometriosis fertility index: the new, validated endometriosis staging system. Fertil Steril 94:1609–1615

    Article  PubMed  Google Scholar 

  18. Boujenah J et al (2015) External validation of the endometriosis fertility index in a French population. Fertil Steril 104(119–123):e111

    Google Scholar 

  19. Tomassetti C et al (2013) External validation of the endometriosis fertility index (EFI) staging system for predicting non-ART pregnancy after endometriosis surgery. Hum Reprod 28:1280–1288

    Article  CAS  PubMed  Google Scholar 

  20. Zhang X et al (2018) Prediction of Endometriosis Fertility Index in patients with endometriosis-associated infertility after laparoscopic treatment. Reprod Biomed Online 37:53–59

    Article  PubMed  CAS  Google Scholar 

  21. Li X et al (2017a) Endometriosis fertility index for predicting pregnancy after endometriosis surgery. Chin Med J 130:1932–1937

    Article  PubMed  PubMed Central  Google Scholar 

  22. Maheux-Lacroix S et al (2017) Endometriosis fertility index predicts live births following surgical resection of moderate and severe endometriosis. Hum Reprod 32:2243–2249

    Article  CAS  PubMed  Google Scholar 

  23. Hobo R et al (2018) The endometriosis fertility index is useful for predicting the ability to conceive without assisted reproductive technology treatment after laparoscopic surgery, regardless of endometriosis. Gynecol Obstet Invest 83:493–498

    Article  PubMed  Google Scholar 

  24. Kim JS et al (2019) Use of the endometriosis fertility index to predict natural pregnancy after endometriosis surgery: a single-center study. Gynecol Obstet Invest 84:86–93

    Article  PubMed  Google Scholar 

  25. Boujenah J et al (2017) Use of the endometriosis fertility index in daily practice: a prospective evaluation. Eur J Obstet Gynecol Reprod Biol 219:28–34

    Article  CAS  PubMed  Google Scholar 

  26. Camp RL, Dolled-Filhart M, Rimm DL (2004) X-tile: a new bio-informatics tool for biomarker assessment and outcome-based cut-point optimization. Clin Cancer Res 10:7252–7259

    Article  CAS  PubMed  Google Scholar 

  27. Johnson NP et al (2017) World Endometriosis Society consensus on the classification of endometriosis. Hum Reprod 32:315–324

    Article  PubMed  Google Scholar 

  28. Ford WC (2010) Comments on the release of the 5th edition of the WHO Laboratory Manual for the Examination and Processing of Human Semen. Asian J Androl 12:59–63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Zegers-Hochschild F et al (2009) The International Committee for Monitoring Assisted Reproductive Technology (ICMART) and the World Health Organization (WHO) Revised Glossary on ART Terminology, 2009. Hum Reprod 24:2683–2687

    Article  CAS  PubMed  Google Scholar 

  30. Brosens I, Gordts S, Benagiano G (2013) Endometriosis in adolescents is a hidden, progressive and severe disease that deserves attention, not just compassion. Hum Reprod 28:2026–2031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Hans Evers JL (2013) Is adolescent endometriosis a progressive disease that needs to be diagnosed and treated? Hum Reprod 28:2023

    Article  CAS  PubMed  Google Scholar 

  32. Aboulghar MA, Mansour RT, Serour GI (2002) Spontaneous intrauterine pregnancy following salpingectomy for a unilateral hydrosalpinx. Hum Reprod 17:1099–1100

    Article  CAS  PubMed  Google Scholar 

  33. Ragni G et al (2005) Damage to ovarian reserve associated with laparoscopic excision of endometriomas: a quantitative rather than a qualitative injury. Am J Obstet Gynecol 193:1908–1914

    Article  PubMed  Google Scholar 

  34. de Ziegler D et al (2010) Use of oral contraceptives in women with endometriosis before assisted reproduction treatment improves outcomes. Fertil Steril 94:2796–2799

    Article  PubMed  Google Scholar 

  35. Orazov MR et al (2019) Oocyte quality in women with infertility associated endometriosis. Gynecol Endocrinol 35:24–26

    Article  PubMed  Google Scholar 

  36. Jacobson TZ et al (2002) Laparoscopic surgery for subfertility associated with endometriosis. Cochrane Database Syst Rev 2002:CD001398

    Google Scholar 

  37. Practice Committee of the American Society for Reproductive M (2012) Endometriosis and infertility: a committee opinion. Fertil Steril 98:591–598

    Article  Google Scholar 

  38. Steiner AZ, Jukic AM (2016) Impact of female age and nulligravidity on fecundity in an older reproductive age cohort. Fertil Steril 105(1584–1588):e1581

    Google Scholar 

  39. Faddy MJ et al (1992) Accelerated disappearance of ovarian follicles in mid-life: implications for forecasting menopause. Hum Reprod 7:1342–1346

    Article  CAS  PubMed  Google Scholar 

  40. Prescott J et al (2016) A prospective cohort study of endometriosis and subsequent risk of infertility. Hum Reprod 31:1475–1482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. American College of O, Gynecologists Committee on Gynecologic P, Practice C (2014) Female age-related fertility decline. Committee Opinion No. 589. Fertil Steril 101:633–634

    Article  Google Scholar 

  42. Poseidon G et al (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  Google Scholar 

  43. Guerriero S et al (2016) Age-related differences in the sonographic characteristics of endometriomas. Hum Reprod 31:1723–1731

    Article  PubMed  Google Scholar 

  44. Sanchez AM et al (2017) Is the oocyte quality affected by endometriosis? A review of the literature. J Ovar Res 10:43

    Article  CAS  Google Scholar 

  45. Muzii L et al (2018) Antimullerian hormone is reduced in the presence of ovarian endometriomas: a systematic review and meta-analysis. Fertil Steril 110(932–940):e931

    Google Scholar 

  46. Abuzeid MI et al (2007) The prevalence of fimbrial pathology in patients with early stages of endometriosis. J Minim Invasive Gynecol 14:49–53

    Article  PubMed  Google Scholar 

  47. Zheng X, Han H, Guan J (2015) Clinical features of fallopian tube accessory ostium and outcomes after laparoscopic treatment. Int J Gynaecol Obstet 129:260–263

    Article  PubMed  Google Scholar 

  48. Peterson CM et al (2013) Risk factors associated with endometriosis: importance of study population for characterizing disease in the ENDO Study. Am J Obstet Gynecol 208(451):e451–e411

    Google Scholar 

  49. Buck Louis GM et al (2016) Women’s Reproductive History before the diagnosis of incident endometriosis. J Women’s Health 25:1021–1029

    Article  Google Scholar 

  50. Li X et al (2017b) Chemical remodeling cell surface glycans for immunotargeting of tumor cells. Carbohyd Res 452:25–34

    Article  CAS  Google Scholar 

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Acknowledgements

We warmly thank Ms. Jiexin Zhang and Ms. Tong Wu for performing the post-operative telephone interview.

Funding

This study received no external funding.

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Authors and Affiliations

Authors

Contributions

JF, KQ, QL, KL, QH and HL designed the study. XL, YL, JX and YY prepared the data. KQ performed the statistical analysis. JF and KQ drafted the manuscript. QL, KL and ANM reviewed the manuscript and contributed important intellectual inputs. All the authors read and approved the final version of the manuscript.

Corresponding author

Correspondence to Qingfeng Li.

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Conflict of interest

All authors declare that they have no competing interests. Completed disclosure of interest forms are available to view online as supporting information.

Ethical approval

This study was approved by the Guangzhou Women and Children’s Medical Center Ethics Committee (No. 2017102709) and written informed consent was obtained from all participants.

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Fan, J., Qin, K., Li, K. et al. Modified endometriosis fertility index is more accurate to predict the non-ART pregnancy rate following surgery: a cohort of Chinese women. Arch Gynecol Obstet 303, 1353–1361 (2021). https://doi.org/10.1007/s00404-020-05871-1

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  • DOI: https://doi.org/10.1007/s00404-020-05871-1

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