Skip to main content
Top
Published in: BMC Endocrine Disorders 1/2020

Open Access 01-12-2020 | Testosterone | Research article

Role of anti-Müllerian hormone and testosterone in follicular growth: a cross-sectional study

Authors: Ping-Ping Lv, Min Jin, Jin-Peng Rao, Jian Chen, Li-Quan Wang, Chang-Chang Huang, Song-Qing Yang, Qiu-Ping Yao, Lei Feng, Jin-Ming Shen, Chun Feng

Published in: BMC Endocrine Disorders | Issue 1/2020

Login to get access

Abstract

Background

Anti-Müllerian hormone (AMH) is now considered the best serum biomarker of ovarian reserve, while basal sex hormones are classic markers used for assessing ovarian reserve. The interaction between AMH and sex hormones are complicated and not sufficiently addressed. In this study, we took diminished ovarian reserve (DOR) and polycystic ovarian syndrome (PCOS) as two extremes of ovarian reserve (deficient and excessive respectively) to investigate the role of AMH and sex hormones in follicular growth.

Methods

A retrospective cross-sectional survey was performed. The patients assessed AMH and basal sex hormones in the Second Hospital of Zhejiang University from April 2016 to March 2019 were involved in this study. Serum AMH and sex hormone concentrations were tested with electrochemiluminescence method. Stepwise linear regression and binary logistic regression was used to determine the predictors of AMH level and to explore the involved factors determining DOR and PCOS.

Results

In the present study, we found that age and follicle-stimulating hormone (FSH) were main negative correlation factors, and luteinizing hormone (LH) and testosterone (T) were main positive factors of AMH. In DOR group, age, FSH and estradiol (E2) increased and T decreased, while in PCOS group, LH and T increased. Binary logistic regression found that age, weight, FSH, E2, and T were the significant factors which independently predicted the likelihood of DOR, and that age, body mass index (BMI), AMH, LH, and T predicted the likelihood of PCOS.

Conclusions

Our study demonstrated that age, FSH, and T were factors that most closely correlated with AMH level, and T was involved in both DOR and PCOS. Since DOR and PCOS are manifested with insufficient AMH and excessive AMH respectively, it is suggested that total testosterone correlated with AMH closely and plays an important role in follicular growth. More attention should be given to testosterone level during controlled ovarian hyperstimulation (COH) process.
Literature
1.
go back to reference Broer SL, Broekmans FJ, Laven JS, Fauser BC. Anti-Müllerian hormone: ovarian reserve testing and its potential clinical implications. Hum Reprod Update. 2014;20(5):688–701.CrossRef Broer SL, Broekmans FJ, Laven JS, Fauser BC. Anti-Müllerian hormone: ovarian reserve testing and its potential clinical implications. Hum Reprod Update. 2014;20(5):688–701.CrossRef
2.
go back to reference Hansen KR, Hodnett GM, Knowlton N, Craig LB. Correlation of ovarian reserve tests with histologically determined primordial follicle number. Fertil Steril. 2011;95(1):170–5.CrossRef Hansen KR, Hodnett GM, Knowlton N, Craig LB. Correlation of ovarian reserve tests with histologically determined primordial follicle number. Fertil Steril. 2011;95(1):170–5.CrossRef
3.
go back to reference 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):221–7.CrossRef 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):221–7.CrossRef
4.
go back to reference Fanchin R, Taieb J, Lozano DH, Ducot B, Frydman R, Bouyer J. High reproducibility of serum anti-Mullerian hormone measurements suggests a multi-staged follicular secretion and strengthens its role in the assessment of ovarian follicular status. Hum Reprod. 2005;20(4):923–7.CrossRef Fanchin R, Taieb J, Lozano DH, Ducot B, Frydman R, Bouyer J. High reproducibility of serum anti-Mullerian hormone measurements suggests a multi-staged follicular secretion and strengthens its role in the assessment of ovarian follicular status. Hum Reprod. 2005;20(4):923–7.CrossRef
5.
go back to reference Deb S, Campbell BK, Pincott-Allen C, Clewes JS, Cumberpatch G, Raine-Fenning NJ. Quantifying effect of combined oral contraceptive pill on functional ovarian reserve as measured by serum anti-Müllerian hormone and small antral follicle count using three-dimensional ultrasound. Ultrasound Obstet Gynecol. 2012;39(5):574–80.CrossRef Deb S, Campbell BK, Pincott-Allen C, Clewes JS, Cumberpatch G, Raine-Fenning NJ. Quantifying effect of combined oral contraceptive pill on functional ovarian reserve as measured by serum anti-Müllerian hormone and small antral follicle count using three-dimensional ultrasound. Ultrasound Obstet Gynecol. 2012;39(5):574–80.CrossRef
6.
go back to reference van Helden J, Evliyaoglu O, Weiskirchen R. Has GnRH a direct role in AMH regulation. Clin Endocrinol. 2019;90(6):827–33.CrossRef van Helden J, Evliyaoglu O, Weiskirchen R. Has GnRH a direct role in AMH regulation. Clin Endocrinol. 2019;90(6):827–33.CrossRef
7.
go back to reference Su HI, Maas K, Sluss PM, Chang RJ, Hall JE, Joffe H. The impact of depot GnRH agonist on AMH levels in healthy reproductive-aged women. J Clin Endocrinol Metab. 2013;98(12):E1961–6.CrossRef Su HI, Maas K, Sluss PM, Chang RJ, Hall JE, Joffe H. The impact of depot GnRH agonist on AMH levels in healthy reproductive-aged women. J Clin Endocrinol Metab. 2013;98(12):E1961–6.CrossRef
8.
go back to reference Kereilwe O, Pandey K, Borromeo V, Kadokawa H. Anti-Müllerian hormone receptor type 2 is expressed in gonadotrophs of postpubertal heifers to control gonadotrophin secretion. Reprod Fertil Dev. 2018;30(9):1192–203.CrossRef Kereilwe O, Pandey K, Borromeo V, Kadokawa H. Anti-Müllerian hormone receptor type 2 is expressed in gonadotrophs of postpubertal heifers to control gonadotrophin secretion. Reprod Fertil Dev. 2018;30(9):1192–203.CrossRef
9.
go back to reference Bédécarrats GY, O'Neill FH, Norwitz ER, Kaiser UB, Teixeira J. Regulation of gonadotropin gene expression by Mullerian inhibiting substance. Proc Natl Acad Sci U S A. 2003;100(16):9348–53.CrossRef Bédécarrats GY, O'Neill FH, Norwitz ER, Kaiser UB, Teixeira J. Regulation of gonadotropin gene expression by Mullerian inhibiting substance. Proc Natl Acad Sci U S A. 2003;100(16):9348–53.CrossRef
10.
go back to reference Cimino I, Casoni F, Liu X, et al. Novel role for anti-Müllerian hormone in the regulation of GnRH neuron excitability and hormone secretion. Nat Commun. 2016;7:10055.CrossRef Cimino I, Casoni F, Liu X, et al. Novel role for anti-Müllerian hormone in the regulation of GnRH neuron excitability and hormone secretion. Nat Commun. 2016;7:10055.CrossRef
11.
go back to reference Durlinger AL, Visser JA, Themmen AP. Regulation of ovarian function: the role of anti-Müllerian hormone. Reproduction. 2002;124(5):601–9.CrossRef Durlinger AL, Visser JA, Themmen AP. Regulation of ovarian function: the role of anti-Müllerian hormone. Reproduction. 2002;124(5):601–9.CrossRef
12.
go back to reference Dewailly D, Robin G, Peigne M, Decanter C, Pigny P, Catteau-Jonard S. Interactions between androgens, FSH, anti-Müllerian hormone and estradiol during folliculogenesis in the human normal and polycystic ovary. Hum Reprod Update. 2016;22(6):709–24.CrossRef Dewailly D, Robin G, Peigne M, Decanter C, Pigny P, Catteau-Jonard S. Interactions between androgens, FSH, anti-Müllerian hormone and estradiol during folliculogenesis in the human normal and polycystic ovary. Hum Reprod Update. 2016;22(6):709–24.CrossRef
13.
go back to reference Pellatt L, Rice S, Dilaver N, et al. Anti-Müllerian hormone reduces follicle sensitivity to follicle-stimulating hormone in human granulosa cells. Fertil Steril. 2011;96(5):1246–51.e1.CrossRef Pellatt L, Rice S, Dilaver N, et al. Anti-Müllerian hormone reduces follicle sensitivity to follicle-stimulating hormone in human granulosa cells. Fertil Steril. 2011;96(5):1246–51.e1.CrossRef
14.
go back to reference Gleicher N, Weghofer A, Barad DH. Anti-Müllerian hormone (AMH) defines, independent of age, low versus good live-birth chances in women with severely diminished ovarian reserve. Fertil Steril. 2010;94(7):2824–7.CrossRef Gleicher N, Weghofer A, Barad DH. Anti-Müllerian hormone (AMH) defines, independent of age, low versus good live-birth chances in women with severely diminished ovarian reserve. Fertil Steril. 2010;94(7):2824–7.CrossRef
15.
go back to reference Tremellen K, Zander-Fox D. Serum anti-Mullerian hormone assessment of ovarian reserve and polycystic ovary syndrome status over the reproductive lifespan. Aust N Z J Obstet Gynaecol. 2015;55(4):384–9.CrossRef Tremellen K, Zander-Fox D. Serum anti-Mullerian hormone assessment of ovarian reserve and polycystic ovary syndrome status over the reproductive lifespan. Aust N Z J Obstet Gynaecol. 2015;55(4):384–9.CrossRef
16.
go back to reference Practice Committee of the American Society for Reproductive Medicine. Testing and interpreting measures of ovarian reserve: a committee opinion. Fertil Steril. 2015;103(3):e9–e17..CrossRef Practice Committee of the American Society for Reproductive Medicine. Testing and interpreting measures of ovarian reserve: a committee opinion. Fertil Steril. 2015;103(3):e9–e17..CrossRef
17.
go back to reference group Csooagegage. Chinese guidelines for diagnosis and treatment of polycystic ovary syndrome. Chinese J Obstetr Gynecol. 2018;53(1):2–6. group Csooagegage. Chinese guidelines for diagnosis and treatment of polycystic ovary syndrome. Chinese J Obstetr Gynecol. 2018;53(1):2–6.
18.
go back to reference Female age-related fertility decline. Committee Opinion. Fertil Steril. 2014;101(3):633–4.CrossRef Female age-related fertility decline. Committee Opinion. Fertil Steril. 2014;101(3):633–4.CrossRef
19.
go back to reference Hudecova M, Holte J, Olovsson M, Sundström PI. Long-term follow-up of patients with polycystic ovary syndrome: reproductive outcome and ovarian reserve. Hum Reprod. 2009;24(5):1176–83.CrossRef Hudecova M, Holte J, Olovsson M, Sundström PI. Long-term follow-up of patients with polycystic ovary syndrome: reproductive outcome and ovarian reserve. Hum Reprod. 2009;24(5):1176–83.CrossRef
20.
go back to reference Beltadze K, Barbakadze L. Ovarian reserve in women of late reproductive age by the method of treatment of PCOS. Iran J Reprod Med. 2015;13(5):263–8.PubMedPubMedCentral Beltadze K, Barbakadze L. Ovarian reserve in women of late reproductive age by the method of treatment of PCOS. Iran J Reprod Med. 2015;13(5):263–8.PubMedPubMedCentral
21.
go back to reference Hsu MI. Changes in the PCOS phenotype with age. Steroids. 2013;78(8):761–6.CrossRef Hsu MI. Changes in the PCOS phenotype with age. Steroids. 2013;78(8):761–6.CrossRef
22.
go back to reference Schmidt J, Brännström M, Landin-Wilhelmsen K, Dahlgren E. Reproductive hormone levels and anthropometry in postmenopausal women with polycystic ovary syndrome (PCOS): a 21-year follow-up study of women diagnosed with PCOS around 50 years ago and their age-matched controls. J Clin Endocrinol Metab. 2011;96(7):2178–85.CrossRef Schmidt J, Brännström M, Landin-Wilhelmsen K, Dahlgren E. Reproductive hormone levels and anthropometry in postmenopausal women with polycystic ovary syndrome (PCOS): a 21-year follow-up study of women diagnosed with PCOS around 50 years ago and their age-matched controls. J Clin Endocrinol Metab. 2011;96(7):2178–85.CrossRef
23.
go back to reference Pellatt L, Rice S, Mason HD. Anti-Müllerian hormone and polycystic ovary syndrome: a mountain too high. Reproduction. 2010;139(5):825–33.CrossRef Pellatt L, Rice S, Mason HD. Anti-Müllerian hormone and polycystic ovary syndrome: a mountain too high. Reproduction. 2010;139(5):825–33.CrossRef
24.
go back to reference Pigny P, Merlen E, Robert Y, et al. Elevated serum level of anti-mullerian hormone in patients with polycystic ovary syndrome: relationship to the ovarian follicle excess and to the follicular arrest. J Clin Endocrinol Metab. 2003;88(12):5957–62.CrossRef Pigny P, Merlen E, Robert Y, et al. Elevated serum level of anti-mullerian hormone in patients with polycystic ovary syndrome: relationship to the ovarian follicle excess and to the follicular arrest. J Clin Endocrinol Metab. 2003;88(12):5957–62.CrossRef
25.
go back to reference Pierre A, Peigné M, Grynberg M, et al. Loss of LH-induced down-regulation of anti-Müllerian hormone receptor expression may contribute to anovulation in women with polycystic ovary syndrome. Hum Reprod. 2013;28(3):762–9.CrossRef Pierre A, Peigné M, Grynberg M, et al. Loss of LH-induced down-regulation of anti-Müllerian hormone receptor expression may contribute to anovulation in women with polycystic ovary syndrome. Hum Reprod. 2013;28(3):762–9.CrossRef
26.
go back to reference Homburg R, Ray A, Bhide P, et al. The relationship of serum anti-Mullerian hormone with polycystic ovarian morphology and polycystic ovary syndrome: a prospective cohort study. Hum Reprod. 2013;28(4):1077–83.CrossRef Homburg R, Ray A, Bhide P, et al. The relationship of serum anti-Mullerian hormone with polycystic ovarian morphology and polycystic ovary syndrome: a prospective cohort study. Hum Reprod. 2013;28(4):1077–83.CrossRef
27.
go back to reference Sova H, Unkila-Kallio L, Tiitinen A, et al. Hormone profiling, including anti-Müllerian hormone (AMH), for the diagnosis of polycystic ovary syndrome (PCOS) and characterization of PCOS phenotypes. Gynecol Endocrinol. 2019;35:1–6.CrossRef Sova H, Unkila-Kallio L, Tiitinen A, et al. Hormone profiling, including anti-Müllerian hormone (AMH), for the diagnosis of polycystic ovary syndrome (PCOS) and characterization of PCOS phenotypes. Gynecol Endocrinol. 2019;35:1–6.CrossRef
28.
go back to reference Garg D, Tal R. The role of AMH in the pathophysiology of polycystic ovarian syndrome. Reprod BioMed Online. 2016;33(1):15–28.CrossRef Garg D, Tal R. The role of AMH in the pathophysiology of polycystic ovarian syndrome. Reprod BioMed Online. 2016;33(1):15–28.CrossRef
29.
go back to reference Pellatt L, Hanna L, Brincat M, et al. Granulosa cell production of anti-Müllerian hormone is increased in polycystic ovaries. J Clin Endocrinol Metab. 2007;92(1):240–5.CrossRef Pellatt L, Hanna L, Brincat M, et al. Granulosa cell production of anti-Müllerian hormone is increased in polycystic ovaries. J Clin Endocrinol Metab. 2007;92(1):240–5.CrossRef
30.
go back to reference Tal R, Seifer DB, Khanimov M, Malter HE, Grazi RV, Leader B. Characterization of women with elevated antimüllerian hormone levels (AMH): correlation of AMH with polycystic ovarian syndrome phenotypes and assisted reproductive technology outcomes. Am J Obstet Gynecol. 2014;211(1):59.e1–8.CrossRef Tal R, Seifer DB, Khanimov M, Malter HE, Grazi RV, Leader B. Characterization of women with elevated antimüllerian hormone levels (AMH): correlation of AMH with polycystic ovarian syndrome phenotypes and assisted reproductive technology outcomes. Am J Obstet Gynecol. 2014;211(1):59.e1–8.CrossRef
31.
go back to reference Vendola KA, Zhou J, Adesanya OO, Weil SJ, Bondy CA. Androgens stimulate early stages of follicular growth in the primate ovary. J Clin Invest. 1998;101(12):2622–9.CrossRef Vendola KA, Zhou J, Adesanya OO, Weil SJ, Bondy CA. Androgens stimulate early stages of follicular growth in the primate ovary. J Clin Invest. 1998;101(12):2622–9.CrossRef
32.
go back to reference Weil S, Vendola K, Zhou J, Bondy CA. Androgen and follicle-stimulating hormone interactions in primate ovarian follicle development. J Clin Endocrinol Metab. 1999;84(8):2951–6.CrossRef Weil S, Vendola K, Zhou J, Bondy CA. Androgen and follicle-stimulating hormone interactions in primate ovarian follicle development. J Clin Endocrinol Metab. 1999;84(8):2951–6.CrossRef
33.
go back to reference Grossman MP, Nakajima ST, Fallat ME, Siow Y. Müllerian-inhibiting substance inhibits cytochrome P450 aromatase activity in human granulosa lutein cell culture. Fertil Steril. 2008;89(5 Suppl):1364–70.CrossRef Grossman MP, Nakajima ST, Fallat ME, Siow Y. Müllerian-inhibiting substance inhibits cytochrome P450 aromatase activity in human granulosa lutein cell culture. Fertil Steril. 2008;89(5 Suppl):1364–70.CrossRef
34.
go back to reference Jacob SL, Field HP, Calder N, Picton HM, Balen AH, Barth JH. Anti-Müllerian hormone reflects the severity of polycystic ovary syndrome. Clin Endocrinol. 2017;86(3):395–400.CrossRef Jacob SL, Field HP, Calder N, Picton HM, Balen AH, Barth JH. Anti-Müllerian hormone reflects the severity of polycystic ovary syndrome. Clin Endocrinol. 2017;86(3):395–400.CrossRef
35.
go back to reference Fraissinet A, Robin G, Pigny P, Lefebvre T, Catteau-Jonard S, Dewailly D. Use of the serum anti-Müllerian hormone assay as a surrogate for polycystic ovarian morphology: impact on diagnosis and phenotypic classification of polycystic ovary syndrome. Hum Reprod. 2017;32(8):1716–22.CrossRef Fraissinet A, Robin G, Pigny P, Lefebvre T, Catteau-Jonard S, Dewailly D. Use of the serum anti-Müllerian hormone assay as a surrogate for polycystic ovarian morphology: impact on diagnosis and phenotypic classification of polycystic ovary syndrome. Hum Reprod. 2017;32(8):1716–22.CrossRef
42.
go back to reference Ferraretti AP, La Marca A, Fauser BC, Tarlatzis B, Nargund G, Gianaroli L, ESHRE working group on Poor Ovarian Response Definition. ESHRE consensus on the definition of ‘poor response’ to ovarian stimulation for in vitro fertilization: the Bologna criteria. Hum Reprod. 2011;26(7):1616–24. https://doi.org/10.1093/humrep/der092.CrossRefPubMed Ferraretti AP, La Marca A, Fauser BC, Tarlatzis B, Nargund G, Gianaroli L, ESHRE working group on Poor Ovarian Response Definition. ESHRE consensus on the definition of ‘poor response’ to ovarian stimulation for in vitro fertilization: the Bologna criteria. Hum Reprod. 2011;26(7):1616–24. https://​doi.​org/​10.​1093/​humrep/​der092.CrossRefPubMed
Metadata
Title
Role of anti-Müllerian hormone and testosterone in follicular growth: a cross-sectional study
Authors
Ping-Ping Lv
Min Jin
Jin-Peng Rao
Jian Chen
Li-Quan Wang
Chang-Chang Huang
Song-Qing Yang
Qiu-Ping Yao
Lei Feng
Jin-Ming Shen
Chun Feng
Publication date
01-12-2020
Publisher
BioMed Central
Published in
BMC Endocrine Disorders / Issue 1/2020
Electronic ISSN: 1472-6823
DOI
https://doi.org/10.1186/s12902-020-00569-6

Other articles of this Issue 1/2020

BMC Endocrine Disorders 1/2020 Go to the issue