Skip to main content
SpringerLink
Log in

Anti-Müllerian Hormone and Assessment of Ovarian Reserve After Ovarian Toxic Treatment: A Systematic Narrative Review

  • Review
  • Published:
Reproductive Sciences Aims and scope Submit manuscript

Abstract

Since serum anti-Müllerian hormone (AMH) levels enable quantitative evaluation of ovarian damage, we conducted a computer-based search, using key words, of all articles published in English through the PubMed database from inception until September 2013 to summarize available studies evaluating ovarian reserve after ovarian toxic interventions to discuss the usefulness of serum AMH levels. We found that most of the studies demonstrated a decline in serum AMH levels when compared to control or pretreatment levels, with levels dependent on the type of treatment modality. Measurement of serum AMH levels enables quantitative evaluation of ovarian damage caused by ovarian toxic interventions, such as chemotherapy and radiotherapy, instead of qualitative evaluation using menstrual condition or basal follicle-stimulating hormone levels. Serum AMH levels are becoming indispensable to assess the ovarian reserve of patients who desire preservation of ovarian function for fertility and endogenous sex steroid hormones.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Broekmans FJ, Kwee J, Hendriks DJ, Mol BW, Lambalk CB. A systematic review of tests predicting ovarian reserve and IVF outcome. Hum Reprod Update. 2006;12(6):685–718.

    Article  CAS  PubMed  Google Scholar 

  2. Bancsi LF, Broekmans FJ, Mol BW, Habbema JD, te Velde ER. Performance of basal follicle-stimulating hormone in the prediction of poor ovarian response and failure to become pregnant after in vitro fertilization: a meta-analysis. Fertil Steril. 2003;79(5): 1091–1100.

    Article  PubMed  Google Scholar 

  3. Nelson SM. Biomarkers of ovarian response: current and future applications. Fertil Steril. 2013;99(4):963–969.

    Article  CAS  PubMed  Google Scholar 

  4. Loh JS, Maheshwari A. Anti-Mullerian hormone—is it a crystal ball for predicting ovarian ageing? Hum Reprod. 2011;26(11): 2925–2932.

    Article  CAS  PubMed  Google Scholar 

  5. Durlinger AL, Gruijters MJ, Kramer P, et al. Anti-Mullerian hormone inhibits initiation of primordial follicle growth in the mouse ovary. Endocrinology. 2002;143(3):1076–1084.

    Article  CAS  PubMed  Google Scholar 

  6. Weenen C, Laven JS, Von Bergh AR, et al. Anti-Mullerian hormone expression pattern in the human ovary: potential implications for initial and cyclic follicle recruitment. Mol Hum Reprod. 2004;10(2):77–83.

    Article  CAS  PubMed  Google Scholar 

  7. Anderson RA, Nelson SM, Wallace WH. Measuring anti-Mullerian hormone for the assessment of ovarian reserve: when and for whom is it indicated? Maturitas. 2012;71(1):28–33.

    Article  CAS  PubMed  Google Scholar 

  8. de Vet A, Laven JS, de Jong FH, Themmen AP, Fauser BC. Antimullerian hormone serum levels: a putative marker for ovarian aging. Fertil Steril. 2002;77(2):357–362.

    Article  PubMed  Google Scholar 

  9. Fanchin R, Schonauer LM, Righini C, Guibourdenche J, Frydman R, Taieb J. Serum anti-Mullerian hormone is more strongly related to ovarian follicular status than serum inhibin B, estradiol, FSH and LH on day 3. Hum Reprod. 2003;18(2):323–327.

    Article  CAS  PubMed  Google Scholar 

  10. van Rooij IA, Broekmans FJ, Scheffer GJ, et al. Serum antimullerian hormone levels best reflect the reproductive decline with age in normal women with proven fertility: a longitudinal study. Fertil Steril. 2005;83(4):979–987.

    Article  PubMed  CAS  Google Scholar 

  11. La Marca A, Sighinolfi G, Radi D, et al. Anti-Mullerian hormone (AMH) as a predictive marker in assisted reproductive technology (ART). Hum Reprod Update. 2010;16(2):113–130.

    Article  CAS  PubMed  Google Scholar 

  12. van Disseldorp J, Lambalk CB, Kwee J, et al. Comparison of inter- and intra-cycle variability of anti-Mullerian hormone and antral follicle counts. Hum Reprod. 2010;25(1):221–227.

    Article  PubMed  Google Scholar 

  13. Stroup DF, Berlin JA, Morton SC, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Metaanalysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA. 2000;283(15):2008–2012.

    Article  CAS  PubMed  Google Scholar 

  14. Lee SJ, Schover LR, Partridge AH, et al. American Society of Clinical Oncology recommendations on fertility preservation in cancer patients. J Clin Oncol. 2006;24(18):2917–2931.

    Article  PubMed  Google Scholar 

  15. McLaren JF, Bates GW. Fertility preservation in women of reproductive age with cancer. Am J Obstet Gynecol. 2012;207(6): 455–462.

    Article  PubMed  Google Scholar 

  16. Lee S, Ozkavukcu S, Heytens E, Moy F, Oktay K. Value of early referral to fertility preservation in young women with breast cancer. J Clin Oncol. 2010;28(31):4683–4686.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Lutchman Singh K, Muttukrishna S, Stein RC, et al. Predictors of ovarian reserve in young women with breast cancer. Br J Cancer. 2007;96(12):1808–1816.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Partridge AH, Ruddy KJ, Gelber S, et al. Ovarian reserve in women who remain premenopausal after chemotherapy for early stage breast cancer. Fertil Steril. 2010;94(2):638–644.

    Article  PubMed  Google Scholar 

  19. Su HI, Sammel MD, Green J, et al. Antimullerian hormone and inhibin B are hormone measures of ovarian function in late reproductive-aged breast cancer survivors. Cancer. 2010;116(3): 592–599.

    Article  CAS  PubMed  Google Scholar 

  20. Anderson RA, Cameron DA. Pretreatment serum anti-mullerian hormone predicts long-term ovarian function and bone mass after chemotherapy for early breast cancer. J Clin Endocrinol Metab. 2011;96(5):1336–1343.

    Article  CAS  PubMed  Google Scholar 

  21. Anderson RA, Themmen AP, Al-Qahtani A, Groome NP, Cameron DA. The effects of chemotherapy and long-term gonadotrophin suppression on the ovarian reserve in premenopausal women with breast cancer. Hum Reprod. 2006;21(10): 2583–2592.

    Article  CAS  PubMed  Google Scholar 

  22. Anders C, Marcom PK, Peterson B, et al. A pilot study of predictive markers of chemotherapy-related amenorrhea among premenopausal women with early stage breast cancer. Cancer Invest. 2008;26(3):286–295.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Su HI, Flatt SW, Natarajan L, DeMichele A, Steiner AZ. Impact of breast cancer on anti-Mullerian hormone levels in young women. Breast Cancer Res Treat. 2013;137(2):571–577.

    Article  CAS  PubMed  Google Scholar 

  24. Lee S, Ozkavukcu S, Heytens E, Moy F, Alappat RM, Oktay K. Anti-Mullerian hormone and antral follicle count as predictors for embryo/oocyte cryopreservation cycle outcomes in breast cancer patients stimulated with letrozole and follicle stimulating hormone. J Assist Reprod Genet. 2011;28(7):651–656.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Rosendahl M, Andersen CY, Ernst E, et al. Ovarian function after removal of an entire ovary for cryopreservation of pieces of cortex prior to gonadotoxic treatment: a follow-up study. Hum Reprod. 2008;23(11):2475–2483.

    Article  PubMed  Google Scholar 

  26. Giuseppe L, Attilio G, Edoardo DN, Loredana G, Cristina L, Vincenzo L. Ovarian function after cancer treatment in young women affected by Hodgkin disease (HD). Hematology. 2007;12(2): 141–147.

    Article  PubMed  Google Scholar 

  27. van Beek RD, van den Heuvel-Eibrink MM, Laven JS, et al. Anti-Mullerian hormone is a sensitive serum marker for gonadal function in women treated for Hodgkin’s lymphoma during childhood. J Clin Endocrinol Metab. 2007;92(10):3869–3874.

    Article  PubMed  CAS  Google Scholar 

  28. Decanter C, Morschhauser F, Pigny P, Lefebvre C, Gallo C, Dewailly D. Anti-Mullerian hormone follow-up in young women treated by chemotherapy for lymphoma: preliminary results. Reprod Biomed Online. 2010;20(2):280–285.

    Article  CAS  PubMed  Google Scholar 

  29. Lie Fong S, Lugtenburg PJ, Schipper I, et al. Anti-mullerian hormone as a marker of ovarian function in women after chemotherapy and radiotherapy for haematological malignancies. Hum Reprod. 2008;23(3):674–678.

    Article  CAS  Google Scholar 

  30. Lawrenz B, Fehm T, von Wolff M, et al. Reduced pretreatment ovarian reserve in premenopausal female patients with Hodgkin lymphoma or non-Hodgkin-lymphoma—evaluation by using antimullerian hormone and retrieved oocytes. Fertil Steril. 2012;98(1):141–144.

    Article  CAS  PubMed  Google Scholar 

  31. Bath LE, Wallace WH, Shaw MP, Fitzpatrick C, Anderson RA. Depletion of ovarian reserve in young women after treatment for cancer in childhood: detection by anti-Mullerian hormone, inhibin B and ovarian ultrasound. Hum Reprod. 2003; 18(11):2368–2374.

    Article  CAS  PubMed  Google Scholar 

  32. Lie Fong S, Laven JS, Hakvoort-Cammel FG, et al. Assessment of ovarian reserve in adult childhood cancer survivors using anti-Mullerian hormone. Hum Reprod. 2009;24(4):982–990.

    Article  CAS  Google Scholar 

  33. van Waas M, Neggers SJ, Te Winkel ML, Beishuizen A, Pieters R, van den Heuvel-Eibrink MM. Endocrine late sequelae in long-term survivors of childhood non-Hodgkin lymphoma. Ann Oncol. 2012;23(6):1626–1632.

    Article  PubMed  Google Scholar 

  34. Hamre H, Kiserud CE, Ruud E, Thorsby PM, Fossa SD. Gonadal function and parenthood 20 years after treatment for childhood lymphoma: a cross-sectional study. Pediatr Blood Cancer. 2012;59(2):271–277.

    Article  PubMed  Google Scholar 

  35. Morse H, Elfving M, Lindgren A, Wolner-Hanssen P, Andersen CY, Ora I. Acute onset of ovarian dysfunction in young females after start of cancer treatment. Pediatr Blood Cancer. 2013; 60(4):676–681.

    Article  PubMed  CAS  Google Scholar 

  36. Dillon KE, Sammel MD, Prewitt M, et al. Pretreatment antimullerian hormone levels determine rate of posttherapy ovarian reserve recovery: acute changes in ovarian reserve during and after chemotherapy. Fertil Steril. 2013;99(2):477–483.

    Article  CAS  PubMed  Google Scholar 

  37. Gracia CR, Sammel MD, Freeman E, et al. Impact of cancer therapies on ovarian reserve. Fertil Steril. 2012;97(1): 134–140 e131.

    Article  PubMed  Google Scholar 

  38. Cuny A, Trivin C, Brailly-Tabard S, et al. Inhibin B and anti-Mullerian hormone as markers of gonadal function after treatment for medulloblastoma or posterior fossa ependymoma during childhood. J Pediatr. 2011;158(6):1016–1022. e1011.

    Article  CAS  PubMed  Google Scholar 

  39. Iwase A, Sugita A, Hirokawa W, et al. Anti-Mullerian hormone as a marker of ovarian reserve in patients with ovarian malignancies who have undergone fertility-preserving surgery and chemotherapy. Gynecol Endocrinol. 2013;29(4):357–360.

    Article  CAS  PubMed  Google Scholar 

  40. Iwase A, Sugita A, Hirokawa W, et al. Anti-Mullerian hormone as a marker of ovarian reserve following chemotherapy in patients with gestational trophoblastic neoplasia. Eur J Obstet Gynecol Reprod Biol. 2013;167(2):194–198.

    Article  CAS  PubMed  Google Scholar 

  41. Mok CC, Chan PT, To CH. Anti-mullerian hormone and ovarian reserve in systemic lupus erythematosus. Arthritis Rheum. 2013; 65(1):206–210.

    Article  CAS  PubMed  Google Scholar 

  42. Morel N, Bachelot A, Chakhtoura Z, et al. Study of anti-Mullerian hormone and its relation to the subsequent probability of pregnancy in 112 patients with systemic lupus erythematosus, exposed or not to cyclophosphamide. J Clin Endocrinol Metab. 2013; 98(9):3785–3792.

    Article  CAS  PubMed  Google Scholar 

  43. Smolen JS, Aletaha D, Bijlsma JW, et al. Treating rheumatoid arthritis to target: recommendations of an international task force. Ann Rheum Dis. 2010;69(4):631–637.

    Article  PubMed  Google Scholar 

  44. Franco JG Jr, Oliveira JB, Petersen CG, Mauri AL, Baruffi R, Cavagna M. Adjuvant therapy with GnRH agonists/tamoxifen in breast cancer should be a good council for patients with hormone receptor-positive tumours and wish to preserve fertility. Med Hypotheses. 2012;78(4):442–445.

    Article  CAS  PubMed  Google Scholar 

  45. Dieudonne AS, Vandenberghe J, Geerts I, et al. Undetectable antimullerian hormone levels and recovery of chemotherapy-induced ovarian failure in women with breast cancer on an oral aromatase inhibitor. Menopause. 2011;18(7):821–824.

    Article  PubMed  Google Scholar 

  46. Jantke A, Rendtorff R, Dittrich R, et al. Association between self-reported questionnaire data on fertility and results of hormone analyses in women after childhood cancer: a cross-sectional study. J Obstet Gynaecol Res. 2012;38(10):1254–1259.

    Article  PubMed  Google Scholar 

  47. Brougham MF, Crofton PM, Johnson EJ, Evans N, Anderson RA, Wallace WH. Anti-Mullerian hormone is a marker of gonadotoxicity in pre- and postpubertal girls treated for cancer: a prospective study. J Clin Endocrinol Metab. 2012; 97(6):2059–2067.

    Article  CAS  PubMed  Google Scholar 

  48. Brouwer J, Laven JS, Hazes JM, Schipper I, Dolhain RJ. Levels of serum anti-Mullerian hormone, a marker for ovarian reserve, in women with rheumatoid arthritis. Arthritis Care Res (Hoboken). 2013;65(9):1534–1538.

    Article  CAS  Google Scholar 

  49. Domingues TS, Rocha AM, Serafini PC. Tests for ovarian reserve: reliability and utility. Curr Opin Obstet Gynecol. 2010; 22(4):271–276.

    PubMed  Google Scholar 

  50. Lambalk CB, van Disseldorp J, de Koning CH, Broekmans FJ. Testing ovarian reserve to predict age at menopause. Maturitas. 2009;63(4):280–291.

    Article  CAS  PubMed  Google Scholar 

  51. Li HW, Ng EH, Wong BP, Anderson RA, Ho PC, Yeung WS. Correlation between three assay systems for anti-Mullerian hormone (AMH) determination. J Assist Reprod Genet. 2012; 29(12): 1443–1446.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Rustamov O, Smith A, Roberts SA, et al. The measurement of anti-Mullerian hormone: a critical appraisal. J Clin Endocrinol Metab. 2014;99(3):723–732.

    Article  CAS  PubMed  Google Scholar 

  53. Decanter C, Peigne M, Mailliez A, et al. Toward a better follow-up of ovarian recovery in young women after chemotherapy with a hypersensitive anti-Mullerian hormone assay. Fertil Steril. 2014;102(2):483–487.

    Article  CAS  PubMed  Google Scholar 

  54. Su HI, Sammel MD, Homer MV, Bui K, Haunschild C, Stanczyk FZ. Comparability of antimullerian hormone levels among commercially available immunoassays. Fertil Steril. 2014;101(6): 1766–1772.e1761.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Welsh P, Smith K, Nelson SM. A single-centre evaluation of two new anti-Mullerian hormone assays and comparison with the current clinical standard assay. Hum Reprod. 2014;29(5):1035–1041.

    Article  PubMed  Google Scholar 

  56. Donnez J, Squifflet J, Dolmans MM. Frozen-thawed ovarian tissue retransplants. Semin Reprod Med. 2009;27(6):472–478.

    Article  PubMed  Google Scholar 

  57. Smith GD, Serafini PC, Fioravanti J, et al. Prospective randomized comparison of human oocyte cryopreservation with slow-rate freezing or vitrification. Fertil Steril. 2010;94(6):2088–2095.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Obstetrics and Gynecology, Nagoya University Graduate School of Medicine, 65 Tsurumai-cho, 466-8550, Showa-ku, Nagoya, Japan

    Akira Iwase MD, Tomoko Nakamura MD, Tatsuo Nakahara MD, Maki Goto MD & Fumitaka Kikkawa MD

  2. Department of Maternal and Perinatal Medicine, Nagoya University Hospital, Showa-ku, Nagoya, Japan

    Akira Iwase MD

Authors
  1. Akira Iwase MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tomoko Nakamura MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tatsuo Nakahara MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maki Goto MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fumitaka Kikkawa MD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Akira Iwase MD.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Iwase, A., Nakamura, T., Nakahara, T. et al. Anti-Müllerian Hormone and Assessment of Ovarian Reserve After Ovarian Toxic Treatment: A Systematic Narrative Review. Reprod. Sci. 22, 519–526 (2015). https://doi.org/10.1177/1933719114549856

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1177/1933719114549856

Keywords

Search

Navigation