Skip to main content
Top
Published in: Reproductive Biology and Endocrinology 1/2019

Open Access 01-12-2019 | Miscarriage | Research

IVF outcomes of women with discrepancies between age and serum anti-Müllerian hormone levels

Authors: Bingqian Zhang, Yueru Meng, Xiao Jiang, Chao Liu, Huihui Zhang, Linlin Cui, Zi-Jiang Chen

Published in: Reproductive Biology and Endocrinology | Issue 1/2019

Login to get access

Abstract

Background

To determine the effects of age and the serum anti-Müllerian hormone (AMH) level on in vitro fertilization (IVF) outcomes, especially among young women with low serum AMH levels and older women with high AMH levels.

Methods

This study was a cohort study in which a total of 9431 women aged 20–51 years who were undergoing their first IVF cycles were recruited. Ovarian response parameters included the number of retrieved oocytes, the number of 2 pronuclear zygotes (2PN), and the frequency of good-quality embryos (GQE). Pregnancy outcomes included the clinical pregnancy rate (CPR), live birth rate (LBR), miscarriage rate (MR), and cumulative CPR and LBR (CCPR and CLBR).

Results

Among women under 35 years of age, the ovarian response, CPR, CCPR, LBR and CLBR (p < 0.01) were significantly lower in the low-AMH group than in the average-AMH and high-AMH groups. In women above 35 years of age, the ovarian response, CPR, CCPR and CLBR (p < 0.01) were significantly higher in the average-AMH and low-AMH groups. The LBR in the older high-AMH group was significantly higher (37.45% vs 20.34%, p < 0.01) than that in the older low-AMH group, but there was no difference (37.45% vs 32.46%, p = 0.11) compared with the older average-AMH group. When there was a discrepancy between age and the AMH level, the young low-AMH group showed a poorer ovarian response but a better CPR (58.01% vs 49.44%, p < 0.01) and LBR (48.52% vs 37.45%, p < 0.01) than the older high-AMH group. However, the CCPR (65.37% vs 66.11%, p = 0.75) and CLBR (56.35% vs 52.89%, p = 0.15) between the two groups were comparable. The conservative CLBR in the two discrepancy groups increased until the third embryo transfer and reached a plateau thereafter.

Conclusion(s)

Even with a relatively low AMH level, young women still had better pregnancy outcomes following IVF than older women. However, increasing the AMH level improves the cumulative outcomes of the older group to a comparable level through a notable and superior ovarian response.
Appendix
Available only for authorised users
Literature
1.
go back to reference Broekmans FJ, Soules MR, Fauser BC. Ovarian aging: mechanisms and clinical consequences. Endocr Rev. 2009;30:465–93.CrossRef Broekmans FJ, Soules MR, Fauser BC. Ovarian aging: mechanisms and clinical consequences. Endocr Rev. 2009;30:465–93.CrossRef
2.
go back to reference Durlinger AL, Visser JA, Themmen AP. Regulation of ovarian function: the role of anti-Mullerian hormone. Reproduction. 2002;124:601–9.CrossRef Durlinger AL, Visser JA, Themmen AP. Regulation of ovarian function: the role of anti-Mullerian hormone. Reproduction. 2002;124:601–9.CrossRef
3.
go back to reference Weenen C, Laven JS, Von Bergh AR, Cranfield M, Groome NP, Visser JA, Kramer P, Fauser BC, Themmen AP. Anti-Mullerian hormone expression pattern in the human ovary: potential implications for initial and cyclic follicle recruitment. Mol Hum Reprod. 2004;10:77–83.CrossRef Weenen C, Laven JS, Von Bergh AR, Cranfield M, Groome NP, Visser JA, Kramer P, Fauser BC, Themmen AP. Anti-Mullerian hormone expression pattern in the human ovary: potential implications for initial and cyclic follicle recruitment. Mol Hum Reprod. 2004;10:77–83.CrossRef
4.
go back to reference Carlsson IB, Scott JE, Visser JA, Ritvos O, Themmen AP, Hovatta O. Anti-Mullerian hormone inhibits initiation of growth of human primordial ovarian follicles in vitro. Hum Reprod. 2006;21:2223–7.CrossRef Carlsson IB, Scott JE, Visser JA, Ritvos O, Themmen AP, Hovatta O. Anti-Mullerian hormone inhibits initiation of growth of human primordial ovarian follicles in vitro. Hum Reprod. 2006;21:2223–7.CrossRef
5.
go back to reference Cui L, Qin Y, Gao X, Lu J, Geng L, Ding L, Qu Z, Zhang X, Chen ZJ. Antimullerian hormone: correlation with age and androgenic and metabolic factors in women from birth to postmenopause. Fertil Steril. 2016;105:481–5 e481.CrossRef Cui L, Qin Y, Gao X, Lu J, Geng L, Ding L, Qu Z, Zhang X, Chen ZJ. Antimullerian hormone: correlation with age and androgenic and metabolic factors in women from birth to postmenopause. Fertil Steril. 2016;105:481–5 e481.CrossRef
6.
go back to reference Iliodromiti S, Anderson RA, Nelson SM. Technical and performance characteristics of anti-Mullerian hormone and antral follicle count as biomarkers of ovarian response. Hum Reprod Update. 2015;21:698–710.CrossRef Iliodromiti S, Anderson RA, Nelson SM. Technical and performance characteristics of anti-Mullerian hormone and antral follicle count as biomarkers of ovarian response. Hum Reprod Update. 2015;21:698–710.CrossRef
7.
go back to reference Broer SL, Dolleman M, Opmeer BC, Fauser BC, Mol BW, Broekmans FJ. AMH and AFC as predictors of excessive response in controlled ovarian hyperstimulation: a meta-analysis. Hum Reprod Update. 2011;17:46–54.CrossRef Broer SL, Dolleman M, Opmeer BC, Fauser BC, Mol BW, Broekmans FJ. AMH and AFC as predictors of excessive response in controlled ovarian hyperstimulation: a meta-analysis. Hum Reprod Update. 2011;17:46–54.CrossRef
8.
go back to reference Broer SL, van Disseldorp J, Broeze KA, Dolleman M, Opmeer BC, Bossuyt P, Eijkemans MJ, Mol BW, Broekmans FJ. Added value of ovarian reserve testing on patient characteristics in the prediction of ovarian response and ongoing pregnancy: an individual patient data approach. Hum Reprod Update. 2013;19:26–36.CrossRef Broer SL, van Disseldorp J, Broeze KA, Dolleman M, Opmeer BC, Bossuyt P, Eijkemans MJ, Mol BW, Broekmans FJ. Added value of ovarian reserve testing on patient characteristics in the prediction of ovarian response and ongoing pregnancy: an individual patient data approach. Hum Reprod Update. 2013;19:26–36.CrossRef
9.
go back to reference La Marca A, Sighinolfi G, Radi D, Argento C, Baraldi E, Artenisio AC, Stabile G, Volpe A. Anti-Mullerian hormone (AMH) as a predictive marker in assisted reproductive technology (ART). Hum Reprod Update. 2010;16:113–30.CrossRef La Marca A, Sighinolfi G, Radi D, Argento C, Baraldi E, Artenisio AC, Stabile G, Volpe A. Anti-Mullerian hormone (AMH) as a predictive marker in assisted reproductive technology (ART). Hum Reprod Update. 2010;16:113–30.CrossRef
10.
go back to reference Alson SSE, Bungum LJ, Giwercman A, Henic E. Anti-mullerian hormone levels are associated with live birth rates in ART, but the predictive ability of anti-mullerian hormone is modest. Eur J Obstet Gynecol Reprod Biol. 2018;225:199–204.CrossRef Alson SSE, Bungum LJ, Giwercman A, Henic E. Anti-mullerian hormone levels are associated with live birth rates in ART, but the predictive ability of anti-mullerian hormone is modest. Eur J Obstet Gynecol Reprod Biol. 2018;225:199–204.CrossRef
11.
go back to reference Tal R, Seifer DB, Wantman E, Baker V, Tal O. Antimullerian hormone as a predictor of live birth following assisted reproduction: an analysis of 85,062 fresh and thawed cycles from the Society for Assisted Reproductive Technology Clinic Outcome Reporting System database for 2012-2013. Fertil Steril. 2018;109:258–65.CrossRef Tal R, Seifer DB, Wantman E, Baker V, Tal O. Antimullerian hormone as a predictor of live birth following assisted reproduction: an analysis of 85,062 fresh and thawed cycles from the Society for Assisted Reproductive Technology Clinic Outcome Reporting System database for 2012-2013. Fertil Steril. 2018;109:258–65.CrossRef
12.
go back to reference Gleicher N, Kushnir VA, Sen A, Darmon SK, Weghofer A, Wu YG, Wang Q, Zhang L, Albertini DF, Barad DH. Definition by FSH, AMH and embryo numbers of good-, intermediate- and poor-prognosis patients suggests previously unknown IVF outcome-determining factor associated with AMH. J Transl Med. 2016;14:172.CrossRef Gleicher N, Kushnir VA, Sen A, Darmon SK, Weghofer A, Wu YG, Wang Q, Zhang L, Albertini DF, Barad DH. Definition by FSH, AMH and embryo numbers of good-, intermediate- and poor-prognosis patients suggests previously unknown IVF outcome-determining factor associated with AMH. J Transl Med. 2016;14:172.CrossRef
13.
go back to reference de Kat AC, van der Schouw YT, Eijkemans MJ, Herber-Gast GC, Visser JA, Verschuren WM, Broekmans FJ. Back to the basics of ovarian aging: a population-based study on longitudinal anti-Mullerian hormone decline. BMC Med. 2016;14:151.CrossRef de Kat AC, van der Schouw YT, Eijkemans MJ, Herber-Gast GC, Visser JA, Verschuren WM, Broekmans FJ. Back to the basics of ovarian aging: a population-based study on longitudinal anti-Mullerian hormone decline. BMC Med. 2016;14:151.CrossRef
14.
go back to reference Gizzo S, Andrisani A, Esposito F, Oliva A, Zicchina C, Capuzzo D, Gangemi M, Nardelli GB. Ovarian reserve test: an impartial means to resolve the mismatch between chronological and biological age in the assessment of female reproductive chances. Reprod Sci. 2014;21:632–9.CrossRef Gizzo S, Andrisani A, Esposito F, Oliva A, Zicchina C, Capuzzo D, Gangemi M, Nardelli GB. Ovarian reserve test: an impartial means to resolve the mismatch between chronological and biological age in the assessment of female reproductive chances. Reprod Sci. 2014;21:632–9.CrossRef
15.
go back to reference Revelli A, Biasoni V, Gennarelli G, Canosa S, Dalmasso P, Benedetto C. IVF results in patients with very low serum AMH are significantly affected by chronological age. J Assist Reprod Genet. 2016;33:603–9.CrossRef Revelli A, Biasoni V, Gennarelli G, Canosa S, Dalmasso P, Benedetto C. IVF results in patients with very low serum AMH are significantly affected by chronological age. J Assist Reprod Genet. 2016;33:603–9.CrossRef
16.
go back to reference Qin Y, Zhao Z, Sun M, Geng L, Che L, Chen ZJ. Association of basal serum testosterone levels with ovarian response and in vitro fertilization outcome. Reprod Biol Endocrinol. 2011;9:9.CrossRef Qin Y, Zhao Z, Sun M, Geng L, Che L, Chen ZJ. Association of basal serum testosterone levels with ovarian response and in vitro fertilization outcome. Reprod Biol Endocrinol. 2011;9:9.CrossRef
17.
go back to reference Chen ZJ, Shi Y, Sun Y, Zhang B, Liang X, Cao Y, Yang J, Liu J, Wei D, Weng N, et al. Fresh versus frozen embryos for infertility in the polycystic ovary syndrome. N Engl J Med. 2016;375:523–33.CrossRef Chen ZJ, Shi Y, Sun Y, Zhang B, Liang X, Cao Y, Yang J, Liu J, Wei D, Weng N, et al. Fresh versus frozen embryos for infertility in the polycystic ovary syndrome. N Engl J Med. 2016;375:523–33.CrossRef
18.
go back to reference Bungum M, Humaidan P, Axmon A, Spano M, Bungum L, Erenpreiss J, Giwercman A. Sperm DNA integrity assessment in prediction of assisted reproduction technology outcome. Hum Reprod. 2007;22:174–9.CrossRef Bungum M, Humaidan P, Axmon A, Spano M, Bungum L, Erenpreiss J, Giwercman A. Sperm DNA integrity assessment in prediction of assisted reproduction technology outcome. Hum Reprod. 2007;22:174–9.CrossRef
19.
go back to reference McLernon DJ, Maheshwari A, Lee AJ, Bhattacharya S. Cumulative live birth rates after one or more complete cycles of IVF: a population-based study of linked cycle data from 178,898 women. Hum Reprod. 2016;31:572–81.CrossRef McLernon DJ, Maheshwari A, Lee AJ, Bhattacharya S. Cumulative live birth rates after one or more complete cycles of IVF: a population-based study of linked cycle data from 178,898 women. Hum Reprod. 2016;31:572–81.CrossRef
20.
go back to reference Sunkara SK, Rittenberg V, Raine-Fenning N, Bhattacharya S, Zamora J, Coomarasamy A. Association between the number of eggs and live birth in IVF treatment: an analysis of 400 135 treatment cycles. Hum Reprod. 2011;26:1768–74.CrossRef Sunkara SK, Rittenberg V, Raine-Fenning N, Bhattacharya S, Zamora J, Coomarasamy A. Association between the number of eggs and live birth in IVF treatment: an analysis of 400 135 treatment cycles. Hum Reprod. 2011;26:1768–74.CrossRef
21.
go back to reference Drakopoulos P, Blockeel C, Stoop D, Camus M, de Vos M, Tournaye H, Polyzos NP. Conventional ovarian stimulation and single embryo transfer for IVF/ICSI. How many oocytes do we need to maximize cumulative live birth rates after utilization of all fresh and frozen embryos? Hum Reprod. 2016;31:370–6.PubMed Drakopoulos P, Blockeel C, Stoop D, Camus M, de Vos M, Tournaye H, Polyzos NP. Conventional ovarian stimulation and single embryo transfer for IVF/ICSI. How many oocytes do we need to maximize cumulative live birth rates after utilization of all fresh and frozen embryos? Hum Reprod. 2016;31:370–6.PubMed
22.
go back to reference Yang Y, Sun X, Cui L, Sheng Y, Tang R, Wei D, Qin Y, Li W, Chen ZJ. Younger poor ovarian response women achieved better pregnancy results in the first three IVF cycles. Reprod BioMed Online. 2016;32:532–7.CrossRef Yang Y, Sun X, Cui L, Sheng Y, Tang R, Wei D, Qin Y, Li W, Chen ZJ. Younger poor ovarian response women achieved better pregnancy results in the first three IVF cycles. Reprod BioMed Online. 2016;32:532–7.CrossRef
23.
go back to reference Xu B, Chen Y, Geerts D, Yue J, Li Z, Zhu G, Jin L. Cumulative live birth rates in more than 3,000 patients with poor ovarian response: a 15-year survey of final in vitro fertilization outcome. Fertil Steril. 2018;109:1051–9.CrossRef Xu B, Chen Y, Geerts D, Yue J, Li Z, Zhu G, Jin L. Cumulative live birth rates in more than 3,000 patients with poor ovarian response: a 15-year survey of final in vitro fertilization outcome. Fertil Steril. 2018;109:1051–9.CrossRef
24.
go back to reference Keefe D, Kumar M, Kalmbach K. Oocyte competency is the key to embryo potential. Fertil Steril. 2015;103:317–22.CrossRef Keefe D, Kumar M, Kalmbach K. Oocyte competency is the key to embryo potential. Fertil Steril. 2015;103:317–22.CrossRef
25.
go back to reference Duncan FE, Jasti S, Paulson A, Kelsh JM, Fegley B, Gerton JL. Age-associated dysregulation of protein metabolism in the mammalian oocyte. Aging Cell. 2017;16:1381–93.CrossRef Duncan FE, Jasti S, Paulson A, Kelsh JM, Fegley B, Gerton JL. Age-associated dysregulation of protein metabolism in the mammalian oocyte. Aging Cell. 2017;16:1381–93.CrossRef
26.
go back to reference May-Panloup P, Boucret L, Chao de la Barca JM, Desquiret-Dumas V, Ferre-L'Hotellier V, Moriniere C, Descamps P, Procaccio V, Reynier P. Ovarian ageing: the role of mitochondria in oocytes and follicles. Hum Reprod Update. 2016;22:725–43.CrossRef May-Panloup P, Boucret L, Chao de la Barca JM, Desquiret-Dumas V, Ferre-L'Hotellier V, Moriniere C, Descamps P, Procaccio V, Reynier P. Ovarian ageing: the role of mitochondria in oocytes and follicles. Hum Reprod Update. 2016;22:725–43.CrossRef
27.
go back to reference Agarwal A, Saleh RA, Bedaiwy MA. Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil Steril. 2003;79:829–43.CrossRef Agarwal A, Saleh RA, Bedaiwy MA. Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil Steril. 2003;79:829–43.CrossRef
28.
go back to reference Xu L, Sun H, Zhang M, Jiang Y, Zhang C, Zhou J, Ding L, Hu Y, Yan G. MicroRNA-145 protects follicular granulosa cells against oxidative stress-induced apoptosis by targeting Kruppel-like factor 4. Mol Cell Endocrinol. 2017;452:138–47.CrossRef Xu L, Sun H, Zhang M, Jiang Y, Zhang C, Zhou J, Ding L, Hu Y, Yan G. MicroRNA-145 protects follicular granulosa cells against oxidative stress-induced apoptosis by targeting Kruppel-like factor 4. Mol Cell Endocrinol. 2017;452:138–47.CrossRef
29.
go back to reference Tatone C. Oocyte senescence: a firm link to age-related female subfertility. Gynecol Endocrinol. 2008;24:59–63.CrossRef Tatone C. Oocyte senescence: a firm link to age-related female subfertility. Gynecol Endocrinol. 2008;24:59–63.CrossRef
30.
go back to reference Zhang X, Wu XQ, Lu S, Guo YL, Ma X. Deficit of mitochondria-derived ATP during oxidative stress impairs mouse MII oocyte spindles. Cell Res. 2006;16:841–50.CrossRef Zhang X, Wu XQ, Lu S, Guo YL, Ma X. Deficit of mitochondria-derived ATP during oxidative stress impairs mouse MII oocyte spindles. Cell Res. 2006;16:841–50.CrossRef
31.
go back to reference Tarasconi B, Tadros T, Ayoubi JM, Belloc S, de Ziegler D, Fanchin R. Serum antimullerian hormone levels are independently related to miscarriage rates after in vitro fertilization-embryo transfer. Fertil Steril. 2017;108:518–24.CrossRef Tarasconi B, Tadros T, Ayoubi JM, Belloc S, de Ziegler D, Fanchin R. Serum antimullerian hormone levels are independently related to miscarriage rates after in vitro fertilization-embryo transfer. Fertil Steril. 2017;108:518–24.CrossRef
32.
go back to reference Daney de Marcillac F, Pinton A, Guillaume A, Sagot P, Pirrello O, Rongieres C. What are the likely IVF/ICSI outcomes if there is a discrepancy between serum AMH and FSH levels? A multicenter retrospective study. J Gynecol Obstet Hum Reprod. 2017;46:629–35.CrossRef Daney de Marcillac F, Pinton A, Guillaume A, Sagot P, Pirrello O, Rongieres C. What are the likely IVF/ICSI outcomes if there is a discrepancy between serum AMH and FSH levels? A multicenter retrospective study. J Gynecol Obstet Hum Reprod. 2017;46:629–35.CrossRef
33.
go back to reference Shi Y, Sun Y, Hao C, Zhang H, Wei D, Zhang Y, Zhu Y, Deng X, Qi X, Li H, et al. Transfer of fresh versus frozen embryos in ovulatory women. N Engl J Med. 2018;378:126–36.CrossRef Shi Y, Sun Y, Hao C, Zhang H, Wei D, Zhang Y, Zhu Y, Deng X, Qi X, Li H, et al. Transfer of fresh versus frozen embryos in ovulatory women. N Engl J Med. 2018;378:126–36.CrossRef
Metadata
Title
IVF outcomes of women with discrepancies between age and serum anti-Müllerian hormone levels
Authors
Bingqian Zhang
Yueru Meng
Xiao Jiang
Chao Liu
Huihui Zhang
Linlin Cui
Zi-Jiang Chen
Publication date
01-12-2019
Publisher
BioMed Central
Keyword
Miscarriage
Published in
Reproductive Biology and Endocrinology / Issue 1/2019
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/s12958-019-0498-3

Other articles of this Issue 1/2019

Reproductive Biology and Endocrinology 1/2019 Go to the issue