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The effect of endometriosis on the antimüllerian hormone level in the infertile population

Abstract

Purpose

To determine whether the presence of endometriosis in infertile women without prior ovarian surgery influences markers of ovarian reserve, AMH and FSH.

Methods

A retrospective cohort study included three groups of women who presented for IVF treatment at our tertiary care center from 04/27/2015 to 05/31/2017: women with endometriosis and prior ovarian surgery (EnSx), women with endometriosis without prior ovarian surgery (En), and women with a primary diagnosis of male factor infertility (MF; reference group).

Results

There were 671 patients that met inclusion criteria (78 EnSx, 60 En, and 533 MF). Compared to the MF group (3.6 ± 3.0), a lower mean AMH level (ng/mL) was observed in the EnSx group (2.5 ± 2.5; aβ − 1.21; 95% CI [− 1.79, −0.62]) and in the En group (2.5 ± 2.2; aβ − 1.11; 95% CI [− 1.68, − 0.54]). Both endometriosis groups had a statistically significantly higher proportion of patients with an AMH < 1 (EnSx, 24.4%; OR, 2.39 [95% CI, 1.31, 4.36]; En, 28.3%; OR, 2.67 [95% CI, 1.41, 5.08]) compared to the MF group (13.9%). The mean baseline FSH level (lU/L) was statistically significantly higher in both endometriosis groups (EnSx, 8.6 ± 4.3; β, 1.37 [95% CI, 0.39, 2.34]; En, 8.4 ± 3.7; β, 0.96 [95% CI, 0.04, 1.87]) compared to the MF group (7.3 ± 2.2).

Conclusions

Among infertility patients with endometriosis, with and without a history of ovarian surgery, ovarian reserve markers were worse (lower AMH and higher FSH) and a higher proportion had decreased ovarian reserve as measured by AMH compared to women with MF.

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References

  1. Gleicher N, Weghofer A, Barad DH. Defining ovarian reserve to better understand ovarian aging. Reprod Biol Endocrinol. 2011;9:23.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Elgindy EA, El-Haieg DO, El-Sebaey A. Anti-Mullerian hormone: correlation of early follicular, ovulatory and midluteal levels with ovarian response and cycle outcome in intracytoplasmic sperm injection patients. Fertil Steril. 2008;89:1670–6.

    Article  CAS  PubMed  Google Scholar 

  3. Yang YS, Hur MH, Kim SY, Young K. Correlation between sonographic and endocrine markers of ovarian aging as predictors for late menopausal transition. Menopause. 2011;18:138–45.

    PubMed  Google Scholar 

  4. Fanchin R, Taieb J, Lozano DH, Ducot B, Frydman R, Bouyer J. High reproducibility of serum anti-Müllerian hormone measurements suggests a multi-staged follicular secretion and strengthens its role in the assessment of ovarian follicular status. Hum Reprod. 2005;20:923–7.

    Article  CAS  PubMed  Google Scholar 

  5. Hehenkamp WJ, Looman CW, Themmen AP, de Jong FH, Te Velde ER, Broekmans FJ. Anti-Mullerian hormone levels in the spontaneous menstrual cycle do not show substantial fluctuation. J Clin Endocrinol Metab. 2006;91:4057–63.

    Article  CAS  PubMed  Google Scholar 

  6. Seifer DB, Baker VL, Leader B. Age-specific serum anti-Mullerian hormone values for 17,120 women presenting to fertility centers within the United States. Fertil Steril. 2011;95:747–50.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  8. Somigliana E, Berlanda N, Benaglia L, Vigano P, Vercellini P, Fedele L. Surgical excision of endometriomas and ovarian reserve: a systematic review on serum antimüllerian hormone level modifications. Fertil Steril. 2012;98:1531–8.

    Article  CAS  PubMed  Google Scholar 

  9. Uncu G, Kasapoglu I, Ozerkan K, Seyhan A, Oral Yilmaztepe A, Ata B. Prospective assessment of the impact of endometriomas and their removal on ovarian reserve and determinants of the rate of decline in ovarian reserve. Hum Reprod. 2013;28:2140–5.

    Article  CAS  PubMed  Google Scholar 

  10. Kasapoglu I, Ata B, Uyaniklar O, Seyhan A, Orhan A, Yildiz Oguz S, et al. Endometrioma-related reduction in ovarian reserve (ERROR): a prospective longitudinal study. Fertil Steril. 2018;110:122–7.

    Article  PubMed  Google Scholar 

  11. Freeman EW, Sammel MD, Lin H, Boorman DW, Gracia CR. Contribution of the rate of change of antimullerian hormone in estimating time to menopause for late reproductive-age women. Fertil Steril. 2012;98:1254–9.e1-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Jacobsen BK, Heuch I, Kvale G. Age at natural menopause and all-cause mortality: a 37-year follow-up of 19,731 Norwegian women. Am J Epidemiol. 2003;157:923–9.

    Article  PubMed  Google Scholar 

  13. Mondul AM, Rodriguez C, Jacobs EJ, Calle EE. Age at natural menopause and cause-specific mortality. Am J Epidemiol. 2005;162:1089–97.

    Article  PubMed  Google Scholar 

  14. American Society for Reproductive Medicine. Revised American Society for Reproductive Medicine classification of endometriosis: 1996. Fertil Steril. 1997;67:817–21.

    Article  Google Scholar 

  15. Li HWR, Wong BPC, Ip WK, Yeung WSB, Ho PC, Ng EHY. Comparative evaluation of three new commercial immunoassays for anti-Müllerian hormone measurement. Hum Reprod. 2016;31:2796–802.

    Article  CAS  PubMed  Google Scholar 

  16. Freeman EW, Gracia CR, Sammel MD, Lin H, Lim LC, Strauss JF 3rd. Association of anti-mullerian hormone levels with obesity in late reproductive-age women. Fertil Steril. 2007;87:101–6.

    Article  CAS  PubMed  Google Scholar 

  17. Backonja U, Hediger ML, Chen Z, Lauver DR, Sun L, Peterson CM, et al. Beyond body mass index: using anthropometric measures and body composition indicators to assess odds of an endometriosis diagnosis. J Womens Health (Larchmt). 2017;26:941–50.

    Article  Google Scholar 

  18. Plante BJ, Cooper GS, Baird DD, Steiner AZ. The impact of smoking on antimüllerian hormone levels in women aged 38 to 50 years. Menopause. 2010;17:571–6.

    PubMed  PubMed Central  Google Scholar 

  19. Seifer DB, Golub ET, Lambert-Messerlian G, Benning L, Anastos K, Watts DH, et al. Variations in serum müllerian inhibiting substance between white, black, and Hispanic women. Fertil Steril. 2009;92:1674–8.

    Article  PubMed  Google Scholar 

  20. Lemos NA, Arbo E, Scalco R, Weiler E, Rosa V, Cunha-Filho JS. Decreased anti-Müllerian hormone and altered ovarian follicular cohort in infertile patients with mild/minimal endometriosis. Fertil Steril. 2008;89:1064–8.

    Article  CAS  PubMed  Google Scholar 

  21. Bulun SE. Endometriosis. N Engl J Med. 2009;360:268–79.

    Article  CAS  PubMed  Google Scholar 

  22. Jayaprakasan K, Becker C, Mittal M. The effect of surgery for endometriomas on fertility: scientific impact paper no. 55. BJOG. 2018;125:e19–28.

    Article  Google Scholar 

  23. Nelson LM. Primary ovarian insufficiency. N Engl J Med. 2009;360:606–14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Hoek A, Schoemaker J, Drexhage HA. Premature ovarian failure and ovarian autoimmunity. Endocr Rev. 1997;18:107–34.

    CAS  PubMed  Google Scholar 

  25. Faubion SS, Kuhle CL, Shuster LT, Rocca WA. Long-term health consequences of premature or early menopause and considerations for management. Climacteric. 2015;18:483–91.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Shuster LT, Rhodes DJ, Gostout BS, Grossardt BR, Rocca WA. Premature menopause or early menopause: long-term health consequences. Maturitas. 2010;65:161–6.

    Article  PubMed  Google Scholar 

  27. Vercellini P, Fedele L, Aimi G, Pietropaolo G, Consonni D, Crosignani PG. Association between endometriosis stage, lesion type, patient characteristics and severity of pelvic pain symptoms: a multivariate analysis of over 1000 patients. Hum Reprod. 2007;22:266–71.

    Article  CAS  PubMed  Google Scholar 

  28. Steiner AZ, Pritchard D, Stanczyk FZ, Kesner JS, Meadows JW, Herring AH, et al. Association between biomarkers of ovarian reserve and infertility among older women of reproductive age. JAMA. 2017;318:1367–76.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Correspondence to Phillip A. Romanski.

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Mark D. Hornstein is an author for UpToDate.com and is on the medical advisory board for WinFertility, Aetion, and AbbVie. The remaining authors declare that they have no conflicts of interest.

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Romanski, P.A., Brady, P.C., Farland, L.V. et al. The effect of endometriosis on the antimüllerian hormone level in the infertile population. J Assist Reprod Genet 36, 1179–1184 (2019). https://doi.org/10.1007/s10815-019-01450-9

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  • DOI: https://doi.org/10.1007/s10815-019-01450-9

Keywords

  • Endometriosis
  • Antimüllerian hormone
  • AMH
  • Ovarian reserve
  • Infertility