Top

Journal of Assisted Reproduction and Genetics

Published in:

01-11-2020 | Fertility | Assisted Reproduction Technologies

Follicular fluid anti-Müllerian hormone (AMH) concentrations and outcomes of in vitro fertilization cycles with fresh embryo transfer among women at a fertility center

Authors: Caitlin R. Sacha, Jorge E. Chavarro, Paige L. Williams, Jennifer Ford, LiHua Zhang, Patricia K. Donahoe, Irene C. Souter, Russ Hauser, David Pépin, Lidia Mínguez-Alarcón, EARTH Study Team

Published in: Journal of Assisted Reproduction and Genetics | Issue 11/2020

Abstract

Purpose

To enhance the understanding of the clinical significance of anti-Müllerian hormone (AMH) in follicular fluid, we aimed to determine the variability of AMH concentrations in follicular fluid within and across IVF cycles and whether high follicular fluid AMH concentrations are associated with improved clinical IVF outcomes.

Methods

This was a retrospective cohort study of companion follicular fluid and serum samples from 162 women enrolled in the Environment and Reproductive Health (EARTH) Study between 2010 and 2016. AMH concentrations were quantified using a sandwich enzyme-linked immunosorbent assay. Spearman correlation and intra-class correlation (ICC) were calculated to assess variability of follicular fluid AMH, and generalized linear mixed models were used to evaluate the associations of FF AMH with IVF outcomes.

Results

The median (interquartile range, IQR) age of the 162 women was 34.0 years (32.0, 37.0). Follicular fluid AMH concentrations were highly correlated between follicles within each IVF cycle (Spearman r = 0.78 to 0.86) and across cycles for each woman (ICC 0.87 (95% CI 0.81 to 0.92)). Compared with women in the highest tertile of FF AMH (mean AMH = 2.3 ng/ml), women in the lowest tertile (mean AMH = 0.2 ng/ml) had lower serum AMH (T1 = 0.1 ng/ml vs. T3 = 0.6 ng/ml, p < 0.0001). In adjusted models, higher tertiles of follicular fluid AMH concentrations were associated with lower mean endometrial thickness and higher probability of clinical pregnancy.

Conclusions

Follicular fluid AMH concentrations show little variability between pre-ovulatory follicles, and higher pre-ovulatory follicular fluid AMH may predict a higher probability of clinical pregnancy.

Available only for authorised users

Jeppesen JV, Anderson RA, Kelsey TW, Christiansen SL, Kristensen SG, Jayaprakasan K, et al. Which follicles make the most anti-Müllerian hormone in humans? Evidence for an abrupt decline in AMH production at the time of follicle selection. Mol Hum Reprod. 2013;19(8):519–27. https://doi.org/10.1093/molehr/gat024.CrossRef

Homburg R, Crawford G. The role of AMH in anovulation associated with PCOS: a hypothesis. Hum Reprod. 2014;29(6):1117–21. https://doi.org/10.1093/humrep/deu076.CrossRef

van Rooiji IA, Broekmans FJ, te Velde ER, Fauser BC, Bancsi LF, de Jong FH, et al. Serum anti-Müllerian hormone levels: a novel measure of ovarian reserve. Hum Reprod. 2002;17(12):3065–71.CrossRef

Seifer DB, MacLaughlin DT, Christian BP, Feng B, Sheldon RM. Early follicular serum Müllerian-inhibiting substance levels are associated with ovarian response during assisted reproductive technology cycles. Fertil Steril. 2002;77(3):468–71.CrossRef

Buyuk E, Seifer DB, Younger J, Grazi RV, Lieman H. Random anti-Müllerian hormone (AMH) is a predictor of ovarian response in women with elevated baseline early follicular follicle-stimulating hormone levels. Fertil Steril. 2011;95(7):2369–72. https://doi.org/10.1016/j.fertnstert.2011.03.071.CrossRef

Andersen CY, Byskov AG. Estradiol and regulation of anti-Müllerian hormone, inhibin-A, and inhibin-B secretion: analysis of small antral and preovulatory human follicles’ fluid. J Clin Endocrinol Metab. 2006;91(10):4064–9. https://doi.org/10.1210/jc.2006-1066.CrossRef

Pellatt L, Rice S, Dilaver N, Heshri A, Galea R, Brincat M, et al. Anti-Müllerian hormone reduces follicle sensitivity to follicle-stimulating hormone in human granulosa cells. Fertil Steril. 2011;96(5):1246–51.e1. https://doi.org/10.1016/j.fertnstert.2011.08.015.CrossRef

Schenk M, Kropfl JM, Obermayer-Pietsch B, Feldmeier E, Weiss G. Anti-Müllerian hormone concentrations in individual follicular fluids within one stimulated IVF cycle resemble blood serum values. J Assist Reprod Genet. 2017;34(9):1115–20. https://doi.org/10.1007/s10815-017-0908-4.CrossRef

Fallat ME, Siow Y, Marra M, Cook C, Carrillo A. Müllerian-inhibiting substance in follicular fluid and serum: a comparison of patients with tubal factor infertility, polycystic ovary syndrome, and endometriosis. Fertil Steril. 1997;67(5):962–5.CrossRef

10.

Pellatt L, Hanna L, Brincat M, Galea R, Brain H, Whitehead S, et al. Granulosa cell production of anti-Müllerian hormone is increased in polycystic ovaries. J Clin Endocrinol Metab. 2007;92(1):240–5. https://doi.org/10.1210/jc.2006-1582.CrossRef

11.

Desforges-Bullet V, Gallo C, Lefebvre C, Pigny P, Dewailly D, Catteau-Jonard S. Increased anti-Müllerian hormone and decreased FSH levels in follicular fluid obtained in women with polycystic ovaries at the time of follicle puncture for in vitro fertilization. Fertil Steril. 2010;94(1):198–204. https://doi.org/10.1016/j.fertnstert.2009.03.004.CrossRef

12.

Kucera R, Babuska V, Ulcova-Gallova Z, Kulda V, Topolcan O. Follicular fluid levels of anti-Müllerian hormone, insulin-like growth factor 1 and leptin in women with fertility disorders. Syst Biol Reprod Med. 2018;64(3):220–3. https://doi.org/10.1080/19396368.2018.1450906.CrossRef

13.

Mashiach R, Amit A, Hasson J, Amzalzg S, Almog B, Ben-Yosef D, et al. Follicular fluid levels of anti-Müllerian hormone as a predictor of oocyte maturation, fertilization rate, and embryonic development in patients with polycystic ovary syndrome. Fertil Steril. 2010;93(7):2299–302. https://doi.org/10.1016/j.fertnstert.2009.01.125.CrossRef

14.

Kim JH, Lee JR, Chang HJ, Jee BC, Suh CS, Kim SH. Anti-Müllerian hormone levels in the follicular fluid of the preovulatory follicle: a predictor for oocyte fertilization and quality of embryo. J Korean Med Sci. 2014;29(9):1266–70. https://doi.org/10.3346/jkms.2014.29.9.1266.CrossRef

15.

Fanchin R, Mendez Lozano DH, Frydman N, Gougeon A, di Clemente N, Frydman R, et al. Anti-Müllerian hormone concentrations in the follicular fluid of the preovulatory follicle are predictive of the implantation potential of the ensuing embryo obtained by in vitro fertilization. J Clin Endocrinol Metab. 2007;92(5):1796–802. https://doi.org/10.1210/jc.2006-1053.CrossRef

16.

Messerlian C, Williams PL, Ford JB, Chavarro JE, Minguez-Alarcon L, Dadd R et al. The Environment and Reproductive Health (EARTH) Study: a prospective preconception cohort. Hum Reprod Open. 2018;2018(2). https://doi.org/10.1093/hropen/hoy001.

17.

Souter I, Smith KW, Dimitriadis I, Ehrlich S, Williams PL, Calafat AM, et al. The association of bisphenol-A urinary concentrations with antral follicle counts and other measures of ovarian reserve in women undergoing infertility treatments. Reprod Toxicol. 2013;42:224–31. https://doi.org/10.1016/j.reprotox.2013.09.008.CrossRef

18.

SART. Preliminary sart clinic summary report. 2015.

19.

Chavarro JE, Ehrlich S, Colaci DS, Wright DL, Toth TL, Petrozza JC, et al. Body mass index and short-term weight change in relation to treatment outcomes in women undergoing assisted reproduction. Fertil Steril. 2012;98(1):109–16.CrossRef

20.

Gaskins AJ, Fong KC, Abu Awad Y, Di Q, Minguez-Alarcon L, Chavarro JE, et al. Time-varying exposure to air pollution and outcomes of in vitro fertilization among couples from a fertility clinic. Environ Health Perspect. 2019;127(7):77002. https://doi.org/10.1289/EHP4601.CrossRef

21.

Sacha CR, Harris AL, James K, Basnet K, Freret TS, Yeh J et al. Placental pathology in live births conceived with in vitro fertilization after fresh and frozen embryo transfer. Am J Obstet Gynecol. 2019.

22.

Mok-Lin E, Ehrlich S, Williams PL, Petrozza J, Wright DL, Calafat AM, et al. Urinary bisphenol A concentrations and ovarian response among women undergoing IVF. Int J Androl. 2010;33(2):385–93. https://doi.org/10.1111/j.1365-2605.2009.01014.x.CrossRef

23.

Kano M, Sosulski AE, Zhang L, Saatcioglu HD, Wang D, Nagykery N, et al. AMH/MIS as a contraceptive that protects the ovarian reserve during chemotherapy. Proc Natl Acad Sci U S A. 2017;114(9):E1688–E97. https://doi.org/10.1073/pnas.1620729114.CrossRef

24.

Hudson PL, Dougas I, Donahoe PK, Cate RL, Epstein J, Pepinsky RB, et al. An immunoassay to detect human Müllerian inhibiting substance in males and females during normal development. J Clin Endocrinol Metab. 1990;70(1):16–22.CrossRef

25.

Pepin D, Hoang M, Nicolaou F, Hendren K, Benedict LA, Al-Moujahed A, et al. An albumin leader sequence coupled with a cleavage site modification enhances the yield of recombinant C-terminal Müllerian inhibiting substance. Technology. 2013;1(1):63–71. https://doi.org/10.1142/S2339547813500076.CrossRef

26.

Ferguson JM, Pepin D, Duru C, Matejtschuk P, Donahoe PK, Burns CJ. Towards international standardization of immunoassays for Müllerian inhibiting substance/anti-Müllerian hormone. Reprod BioMed Online. 2018;37(5):631–40. https://doi.org/10.1016/j.rbmo.2018.08.012.CrossRef

27.

Minguez-Alarcon L, Chiu YH, Messerlian C, Williams PL, Sabatini ME, Toth TL, et al. Urinary paraben concentrations and in vitro fertilization outcomes among women from a fertility clinic. Fertil Steril. 2016;105(3):714–21. https://doi.org/10.1016/j.fertnstert.2015.11.021.CrossRef

28.

Veeck L, Zaninovic N. An atlas of human blastocysts. New York: Parthenon Publishing Group; 2003.CrossRef

29.

Searle SR, Speed FM, Milliken GA. Population marginal means in the linear model: an alternative to least squares means. AmStat. 1980;34(4):216–21.

30.

Rooney KL, Domar AD. The impact of lifestyle behaviors on infertility treatment outcome. Curr Opin Obstet Gynecol. 2014;26(3):181–5.CrossRef

31.

Sharma R, Biedenham KR, Fedor JM, Agarwal A. Lifestyle factors and reproductive health: taking control of your fertility. Reprod Biol Endocrinol: RB&E. 2013;11(66):1–15.

32.

Cai J, Liu L, Zheng J, Zhang L, Jiang X, Li P, et al. Differential response of AMH to GnRH agonist among individuals: the effect on ovarian stimulation outcomes. J Assist Reprod Genet. 2018;35(3):467–73. https://doi.org/10.1007/s10815-017-1095-z.CrossRef

33.

Seifer DB, MacLaughlin DT, Penzias AS, Behrman HR, Asmundson L, Donahoe PK, et al. Gonadotropin-releasing hormone agonist-induced differences in granulosa cell cycle kinetics are associated with alterations in follicular fluid Müllerian-inhibiting substance and androgen content. JCEM. 1993;76(3):711–4.

34.

Silberstein T, MacLaughlin DT, Shai I, Trimarchi JR, Lambert-Messerlian G, Seifer DB, et al. Müllerian inhibiting substance levels at the time of HCG administration in IVF cycles predict both ovarian reserve and embryo morphology. Hum Reprod. 2006;21(1):159–63. https://doi.org/10.1093/humrep/dei270.CrossRef

35.

Zhang B, Meng Y, Jiang X, Liu C, Zhang H, Cui L, et al. IVF outcomes of women with discrepancies between age and serum anti-Müllerian hormone levels. Reprod Biol Endocrinol: RB&E. 2019;17(1):58. https://doi.org/10.1186/s12958-019-0498-3.CrossRef

36.

Nelson SM, Yates RW, Fleming R. Serum anti-Müllerian hormone and FSH: prediction of live birth and extremes of response in stimulated cycles--implications for individualization of therapy. Hum Reprod. 2007;22(9):2414–21. https://doi.org/10.1093/humrep/dem204.CrossRef

37.

Iliodromiti S, Kelsey TW, Wu O, Anderson RA, Nelson SM. The predictive accuracy of anti-Müllerian hormone for live birth after assisted conception: a systematic review and meta-analysis of the literature. Hum Reprod Update. 2014;20(4):560–70. https://doi.org/10.1093/humupd/dmu003.CrossRef

38.

Tal R, Tal O, Seifer BJ, Seifer DB. Anti-Müllerian hormone as predictor of implantation and clinical pregnancy after assisted conception: a systematic review and meta-analysis. Fertil Steril. 2015;103(1):119–30.e3. https://doi.org/10.1016/j.fertnstert.2014.09.041.CrossRef

39.

Tal R, Seifer DB, Wantman E, Baker V, Tal O. Anti-Müllerian 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(2):258–65. https://doi.org/10.1016/j.fertnstert.2017.10.021.CrossRef

40.

Hsu JY, James KE, Bormann CL, Donahoe PK, Pepin D, Sabatini ME. Müllerian-inhibiting substance/anti-Müllerian hormone as a predictor of preterm birth in polycystic ovary syndrome. J Clin Endocrinol Metab. 2018;103(11):4187–96. https://doi.org/10.1210/jc.2018-01320.CrossRef

41.

Saatcioglu HD, Kano M, Horn H, Zhang L, Samore W, Nagykery N, et al. Single-cell sequencing of neonatal uterus reveals an Misr2+ endometrial progenitor indispensable for fertility. Elife. 2019;8. https://doi.org/10.7554/eLife.46349.

42.

Hu KL, Liu FT, Xu H, Li R, Qiao J. High anti-Müllerian hormone levels are associated with preterm delivery in patients with polycystic ovary syndrome. Fertil Steril. 2020;113:444–452.e1. https://doi.org/10.1016/j.fertnstert.2019.09.039.CrossRef

43.

Hamilton BE, Martin JA, Osterman MJK, Rossen LM. Births: Provisional Data for 2018: Division of Vital Statistics, National Center for Health Statistics2019 Contract No.: 007

44.

Ishihara O, Adamson GD, Dyer S, de Mouzon J, Nygren KG, Sullivan EA, et al. International Committee for Monitoring Assisted Reproductive Technologies: World Report on Assisted Reproductive Technologies, 2007. Fertil Steril. 2015;103(2):402–13.e11. https://doi.org/10.1016/j.fertnstert.2014.11.004.CrossRef

45.

Schieve LA, Devine O, Boyle CA, Petrini JR, Warner L. Estimation of the contribution of non–assisted reproductive technology ovulation stimulation fertility treatments to US singleton and multiple births. Am J Epidemiol. 2009;170(11):1396–407. https://doi.org/10.1093/aje/kwp281.CrossRef

46.

Dyer S, Chambers GM, de Mouzon J, Nygren KG, Zegers-Hochschild F, Mansour R, et al. International Committee for Monitoring Assisted Reproductive Technologies world report: assisted reproductive technology 2008, 2009 and 2010. Hum Reprod. 2016;31(7):1588–609. https://doi.org/10.1093/humrep/dew082.CrossRef

Title: Follicular fluid anti-Müllerian hormone (AMH) concentrations and outcomes of in vitro fertilization cycles with fresh embryo transfer among women at a fertility center
Authors: Caitlin R. Sacha
Jorge E. Chavarro
Paige L. Williams
Jennifer Ford
LiHua Zhang
Patricia K. Donahoe
Irene C. Souter
Russ Hauser
David Pépin
Lidia Mínguez-Alarcón
EARTH Study Team
Publication date: 01-11-2020
Publisher: Springer US
Keywords: Fertility
ICSI
Published in: Journal of Assisted Reproduction and Genetics / Issue 11/2020
Print ISSN: 1058-0468
Electronic ISSN: 1573-7330
DOI: https://doi.org/10.1007/s10815-020-01956-7

2024 ASCO Annual Meeting

Springer Medicine

Follicular fluid anti-Müllerian hormone (AMH) concentrations and outcomes of in vitro fertilization cycles with fresh embryo transfer among women at a fertility center

Abstract

Purpose

Methods

Results

Conclusions

2024 ASCO Annual Meeting

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 11/2020

When pregnancy is a research risk

Association study between single-nucleotide variants rs12097821, rs2477686, and rs10842262 and idiopathic male infertility risk in Serbian population with meta-analysis

Navigating assisted reproduction treatment in the time of COVID-19: concerns and considerations

Mitochondrial metabolic substrate utilization in granulosa cells reflects body mass index and total follicle stimulating hormone dosage in in vitro fertilization patients

Recent trends in embryo disposition choices made by patients following in vitro fertilization

Letter to editor