Human Reproduction, Vol. 18, No. 2, 323-327,
February 2003
© 2003 European Society of Human Reproduction and Embryology
Serum anti-Müllerian hormone is more strongly related to ovarian follicular status than serum inhibin B, estradiol, FSH and LH on day 3
Departments of 1 Obstetrics and Gynecology and Reproductive Medicine, Clamart, France, and 2 Biochemistry and 3 Hormonology, Paris and Clamart, France
4 To whom correspondence should be addressed at: Department of Obstetrics and Gynecology and Reproductive Medicine, Hôpital Antoine Béclère, 157, rue de la Porte de Trivaux, 92141, Clamart, France. e-mail: renato.fanchin{at}abc.ap-hop-paris.fr
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Abstract |
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BACKGROUND: The study aim was to compare the relationship between serum anti-Müllerian hormone (AMH) levels and other markers of ovarian function with early antral follicle count on day 3. METHODS: A total of 75 infertile women was studied prospectively. On cycle day 3, serum levels of AMH, inhibin B, estradiol (E2), FSH and LH levels were measured, and the number of early antral follicles (2–10 mm in diameter) estimated at ultrasound scanning to compare the strengths of hormonal–follicular correlations. RESULTS: Median (range) serum levels of AMH, inhibin B, E2, FSH and LH were 1.39 ng/ml (0.24–6.40), 90 (16–182) pg/ml, 31 (15–111) pg/ml, 7.0 (2.9–19.3) mIU/ml and 4.7 (1.2–11.7) mIU/ml respectively, and follicular count was 12 (1–35). Serum AMH levels were more strongly correlated (P < 0.001) with follicular count (r = 0.74, P < 0.0001) than were serum levels of inhibin B (r = 0.29, P < 0.001), E2 (r = –0.08, P = NS), FSH (r = –0.29, P < 0.001) and LH (r = 0.05, P = NS). CONCLUSIONS: Serum AMH levels were more robustly correlated with the number of early antral follicles than inhibin B, E2, FSH and LH on cycle day 3. This suggests that AMH may reflect ovarian follicular status better than the usual hormone markers.
Key words: anti-Müllerian hormone/antral follicles/endocrine profile/Müllerian-inhibiting substance (MIS)/ovarian reserve
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Introduction |
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Anti-Müllerian hormone (AMH) is a glycoprotein hormone that belongs to the transforming growth factor
superfamily (Pepinsky et al., 1988
) and is chiefly expressed in the fetal testis to drive differentiation of the mammalian reproductive tract (Lee and Donahoe, 1993). In women, granulosa cell production of AMH (Vigier et al., 1984) is barely detectable at birth (Rajpert-De Meyts et al., 1999) and reaches the highest values after puberty (Hudson et al., 1990). During adulthood, although AMH continues to be expressed at basal and similar levels by both the Sertoli and granulosa cells (Hudson et al., 1990), its biological role is poorly understood.
Basic research data obtained from the adult ovary indicate that AMH is likely to be involved in the regulation of follicular steroidogenesis. Experiments conducted in animals suggest that AMH reduces aromatase activity and the number of LH receptors in FSH-stimulated granulosa cells (Josso et al., 1998), and also influences testosterone production by theca cells (Ingraham et al., 2000). In addition, growing evidence indicates that AMH mainly is expressed in pre-antral and early antral follicles (Baarends et al., 1995) and has either direct or indirect roles in various phases of folliculogenesis, from the primordial (Durlinger et al., 2002) to FSH-sensitive (Durlinger et al., 2001; McGee et al., 2001) follicular stages, probably via specific AMH type II receptors that are expressed in granulosa and theca cells. This suggests that, in contrast to other hormonal markers of ovarian function, AMH secretion might concurrently reflect the activity of pre-antral and early antral follicles, which makes it a promising parameter in the evaluation of ovarian follicular reserve.
Recent clinical evidence is in agreement with this hypothesis. One group (de Vet et al., 2002) demonstrated that serum AMH levels on cycle day 3 decrease progressively along with age and become undetectable after menopause. This suggests that peripheral AMH levels are a valuable parameter to monitor the relative follicular exhaustion due to ovarian ageing. Consistently, others (Seifer et al., 2002) showed that day 3 AMH levels are positively related with the number of oocytes retrieved after controlled ovarian hyperstimulation (COH). Taken together, these results indicate that circulating AMH levels reflect the number of selectable follicles during the early follicular phase. Indeed, the early antral follicle count has been shown to reliably predict the fertility potential of women (Reuss et al., 1996) and their responsiveness to COS (Chang et al., 1998; László et al., 2002).
However, the question of whether serum AMH measurements on cycle day 3 reflect ovarian follicular status better than the usual hormonal parameters remains unanswered. Hence, the present investigation was designed to weigh the relationship between early antral follicles and AMH levels against that between early antral follicles and other putative markers of ovarian function and fertility potential, including serum levels of inhibin B, estradiol (E2), FSH and LH on cycle day 3.
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Materials and methods |
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Subjects
A total of 75 infertile women (age range 25–40 years) was studied prospectively. In order to be included, the women had to meet the following criteria: (i) regular, ovulatory menstrual cycles every 25–35 days; (ii) both ovaries present; (iii) no current or past diseases affecting ovaries or gonadotrophin or sex steroid secretion, clearance or excretion; (iv) a body mass index (BMI) of 18–27 kg/m2; (v) no current hormone therapy; and (vi) adequate visualization of ovaries at transvaginal ultrasound scanning. All patients were undergoing routine explorations before IVF–embryo transfer. Informed consent was obtained from all women, and the investigation was approved by the authors’ internal Institutional Review Board.
Study protocol
On day 3 of the menstrual cycle, each woman underwent blood sampling by venipuncture for measurement of serum levels of AMH, inhibin B, E2, FSH and LH at approximately 09:00 h. Later in the morning, ovarian ultrasound scanning (Figure 1) was performed using a 4.5–7.2 MHz multi-frequency transvaginal probe (Siemens Elegra; Siemens S.A.S., Saint-Denis, France) by one operator (R.F.), who was blinded to the results of the hormone assays. The objective of the ultrasound examination was to evaluate the number and sizes of early antral follicles and to calculate the mean ovarian volume. The sum of all follicles measuring 2–10 mm in mean diameter (mean of two orthogonal diameters) in both ovaries was considered. In an attempt to optimise the reliability of ovarian follicular assessment, the ultrasound scanner used was equipped with a tissue harmonic imaging system (Thomas and Rubin, 1998); this allowed improved image resolution and adequate recognition of follicular borders. Ovarian volumes, calculated according to the formula for an ellipsoid (0.526xlengthx heightxwidth) (Sharara and McClamrock, 1999), corresponded to the mean volume for both ovaries. Intra-analysis coefficients of variation (CV) for follicular and ovarian measurements were <5%, and their lower limit of detection was 0.1 mm.
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Hormone measurements
Serum was separated from all blood samples and frozen in aliquots at –20°C until used for subsequent centralized analysis. Serum AMH levels were determined using an ultrasensitive enzyme-linked immunosorbent assay (ELISA) (Beckman-Coulter, Villepinte, France) as described previously (Long et al., 2000
). For AMH, functional sensitivity was 0.24 ng/ml and intra-assay and inter-assay CV were <5 and <8% respectively. Serum inhibin B levels were determined using a double antibody ELISA (Serotec, Varilhes, France) as described previously (Groome et al., 1996). For inhibin B, functional sensitivity was 15 pg/ml and intra-assay and inter-assay CV were <6 and <9% respectively. Serum levels of E2, FSH and LH were determined using an automated multi-analysis system with chemiluminescence detection (ACS-180; Bayer Diagnostics, Puteaux, France). For E2, functional sensitivity was 15 pg/ml and intra-assay and inter-assay CV were 8 and 9% respectively. For FSH and LH, functional sensitivity was 0.1 mIU/ml and intra-assay and inter-assay CV were 3 and 5% respectively.
Statistical analysis
The measure of central tendency used was the median, and data variability was expressed by the ranges. Relationship between two different continuous variables was assessed by correlation. The Fisher r to z-test was used to determine if the coefficient of correlation (r) was significantly different from zero. Comparison of strength of correlations was performed using the Hotelling’s t-test (Hotelling, 1940), which assesses the difference between coefficients of correlation for correlated samples that share a common variable. A P-value < 0.05 was considered statistically significant.
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Results |
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The median age of participants was 34 (range 25–40) years, BMI was 21.3 (range 16–27) kg/m2, and menstrual cycle length 28 (range 25–35) days. Data distribution of serum hormone levels and of the number of early antral follicles on cycle day 3 is shown in Figure 2. Median serum levels of AMH, inhibin B, E2, FSH and LH were 1.39 (range 0.24–6.40) ng/ml, 90 (range 16–182) pg/ml, 31 (range 15–111) pg/ml, 7.0 (range 2.9–19.3) mIU/ml and 4.7 (range 1.2–11.7) mIU/ml respectively. Ultrasound scans revealed a median number of early antral follicles of 12 (range 1–35), and an ovarian volume of 6 (range 4.4–8.0) cm3. In addition, serum levels of AMH were slightly and negatively correlated with age (r = –0.22, P < 0.04), but this did not apply to serum levels of either inhibin B, E2, FSH or LH (r = 0.06, r = 0.09, r = –0.13 and r = –0.02 respectively).
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Relationships between the number of antral follicles and serum levels of AMH, inhibin B, E2, FSH and LH on cycle day 3 are shown in Figure 3. Unlike serum levels of E2 and LH (r = –0.08 and r = 0.05), those of AMH, inhibin B and FSH were significantly correlated with the number of early antral follicles on cycle day 3. It is noteworthy that the correlation between serum AMH levels and the number of early antral follicles (r = 0.74, P < 0.0001) was significantly stronger (P < 0.001) than correlations between serum levels of inhibin B and FSH and the same parameter (r = 0.29, P < 0.001; r = 0.29, P < 0.001 respectively). In agreement with this, serum AMH levels showed a stronger correlation (P < 0.001) with ovarian volume (r = 0.43, P < 0.0001) than did those of inhibin B (r = 0.11, P = NS), E2 (r = 0.13, P = NS), FSH (r = –0.27, P < 0.02) and LH (r = 0.02, P = NS). Incidentally, serum AMH levels were correlated with those of inhibin B (r = 0.26, P < 0.02) and FSH (r = –0.27, P < 0.02), but not with those of E2 and LH.
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Discussion |
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The present investigation was designed to evaluate the direct relationship between peripheral AMH levels, measured by an ultrasensitive ELISA technique, and the ovarian follicular status on cycle day 3, and to compare the strength of correlations between the number of early antral follicles and some hormonal parameters implicated directly or indirectly in the eventual stages of folliculogenesis. It was observed that serum AMH levels are tightly related to early antral follicle count, with a relationship that was remarkably more intense than those obtained with serum levels of inhibin B, E2, FSH and LH.
These results not only corroborate but also expand clinical data reported previously by other investigators (de Vet et al., 2002; Seifer et al., 2002). First, the age-related decrease in AMH levels (de Vet et al., 2002) probably results from the relative follicular attrition that characterizes the decline of ovarian function, with a noticeable reduction in the number of early antral follicles (Reuss et al., 1996). The negative relationship between day 3 serum AMH levels and the women’s age seen in the present study supports this hypothesis. Second, the reported correlation between serum AMH levels on cycle day 3 and the number of oocytes retrieved after COS (Seifer et al., 2002) is in keeping with the relationship between AMH and the number of early antral follicles shown in the present study. Indeed, the number of early antral follicles is a putative predictor of COS outcome (Chang et al., 1998; László et al., 2002). Third, the correlation between serum AMH levels and early antral follicle count confirms preliminary data reported by others (de Vet et al., 2002), though the latter authors observed similar coefficients of correlation for this relationship (0.71) as in the present study (0.74).
Nonetheless, the central result of the present investigation was that AMH correlated more intensely with early antral follicular counts than did the other hormonal markers of follicular status and development that were monitored. The reasons for this striking phenomenon are unclear, but it may be related to possible different regulation of AMH as compared with inhibin B, E2 and FSH. During the luteal–follicular transition, the secretion of inhibin B (Welt et al., 1997) and E2 (Mais et al., 1987) by the early antral follicles modulates their own stimulation by FSH. This implies that inhibin B and E2 levels depend not only on the bulk of active granulosa cells available, as represented by follicular number and sizes, but also on their stimulation by FSH. Although little is known about FSH effects on AMH expression during the early follicular phase, it can be presumed that this hormone is less FSH-sensitive than inhibin B and E2. Indeed, AMH is also secreted by follicles that are barely sensitive to FSH, such as pre-antral follicles (Baarends et al., 1995). Therefore, AMH may represent a more independent and reliable marker of early antral follicle activity than inhibin B and E2, and FSH on cycle day 3. Further studies are required to investigate whether AMH measurements on day 3 reflect not only the activity of early antral follicles but also that of follicles during earlier stages of folliculogenesis.
Nevertheless, a negative relationship was observed between FSH and AMH levels. Whereas these data challenge the hypothesis of a stimulating role of FSH on granulosa cell production of AMH, they do not rule out its potential inhibiting action on AMH production. Indeed, the results of studies conducted in rats treated with GnRH antagonist and FSH have indicated that FSH inhibits AMH and its type II receptor expression in pre-antral and early antral follicles (Baarends et al., 1995). However, since in the present series AMH and FSH levels were both correlated with a third common parameter (early antral follicular count), their mutual correlation might be merely indirect and not causative. Likewise, the correlation observed between AMH and inhibin B levels may not correspond to a direct relationship between both hormones.
Another issue deserving consideration is the observed lack of influence of endogenous LH concentrations on peripheral AMH levels. Indeed, the present data agree with previous results obtained in normo-ovulating and polycystic ovary syndrome (PCOS) patients (Cook et al., 2002). In PCOS, basal AMH levels are significantly higher as compared with normal controls (Cook et al., 2002). Although these results may be attributed to the large number of antral follicles that characterizes PCOS, they do not permit the exclusion of a possible influence of LH on AMH regulation. Experiments conducted in rats and pigs have shown that AMH inhibits the number of LH receptors in FSH-stimulated granulosa cells (Josso et al., 1998, 2001). Further studies involving pituitary-desensitized women treated with controlled FSH and/or LH doses will undoubtedly contribute to clarifying the possible regulation of AMH by pituitary gonadotrophins.
Similarly, conclusive data on AMH secretion patterns during more advanced stages of the follicular phase and during the luteal phase of the menstrual cycle are still lacking. A preliminary study showed that serum AMH levels are slightly and significantly higher at mid-cycle as compared with early follicular and mid-luteal phase values in women (Cook et al., 2000). However, these data did not detail the possible relationship between AMH production and eventual follicular development and/or corpus luteum activity. Also, they contrast with in-vitro studies that demonstrated a progressive decrease of AMH expression during the final steps of follicular maturation from pre-antral to pre-ovulatory follicles (Baarends et al., 1995). Hence, further characterization of subtle changes in serum AMH levels throughout the menstrual cycle is required. Likewise, investigation of possible effects of COS with exogenous gonadotrophins on peripheral AMH levels may provide further insights into AMH regulation and its pathophysiological role in adult women.
In conclusion, the present results indicate not only that serum AMH levels are strongly correlated with ovarian follicular status during the early follicular phase, but also that this relationship is more strict than that obtained with other hormonal markers of the follicular functioning. This leads to the conclusion that serum AMH measurements on cycle day 3 are a better predictor of the number of early antral follicles than conventional hormone measurements. However, further studies aimed at weighing the predictability of AMH levels against conventional day 3 inhibin B, E2 and FSH measurements on COS and assisted reproductive technology outcomes are needed to challenge this conclusion. Moreover, uncertainties persist with respect to the control of granulosa cell AMH production and its physiological role during folliculogenesis. The understanding of these key issues will be helpful to refine future clinical applications of AMH measurements in evaluating the fertility potential of women and monitoring infertility treatments.
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Submitted on July 5, 2002; accepted on September 25, 2002.
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M. McIlveen, J.D. Skull, and W.L. Ledger Evaluation of the utility of multiple endocrine and ultrasound measures of ovarian reserve in the prediction of cycle cancellation in a high-risk IVF population Hum. Reprod., March 1, 2007; 22(3): 778 - 785. [Abstract] [Full Text] [PDF]
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G. Meduri, N. Massin, J. Guibourdenche, A. Bachelot, O. Fiori, F. Kuttenn, M. Misrahi, and P. Touraine Serum anti-Mullerian hormone expression in women with premature ovarian failure Hum. Reprod., January 1, 2007; 22(1): 117 - 123. [Abstract] [Full Text] [PDF]
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A. Maheshwari, P. Fowler, and S. Bhattacharya Assessment of ovarian reserve--should we perform tests of ovarian reserve routinely? Hum. Reprod., November 1, 2006; 21(11): 2729 - 2735. [Abstract] [Full Text] [PDF]
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W. J. K. Hehenkamp, C. W. N. Looman, A. P. N. Themmen, F. H. de Jong, E. R. te Velde, and F. J. M. Broekmans Anti-Mullerian Hormone Levels in the Spontaneous Menstrual Cycle Do Not Show Substantial Fluctuation J. Clin. Endocrinol. Metab., October 1, 2006; 91(10): 4057 - 4063. [Abstract] [Full Text] [PDF]
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C. Y. Andersen and A. G. Byskov Estradiol and Regulation of Anti-Mullerian Hormone, Inhibin-A, and Inhibin-B Secretion: Analysis of Small Antral and Preovulatory Human Follicles' Fluid J. Clin. Endocrinol. Metab., October 1, 2006; 91(10): 4064 - 4069. [Abstract] [Full Text] [PDF]
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R.A. Anderson, A.P.N. Themmen, A.A. -Qahtani, N.P. Groome, and D.A. Cameron The effects of chemotherapy and long-term gonadotrophin suppression on the ovarian reserve in premenopausal women with breast cancer Hum. Reprod., October 1, 2006; 21(10): 2583 - 2592. [Abstract] [Full Text] [PDF]
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 K. Oktay, O. Oktem, A. Reh, and L. Vahdat Measuring the Impact of Chemotherapy on Fertility in Women With Breast Cancer J. Clin. Oncol., August 20, 2006; 24(24): 4044 - 4046. [Full Text] [PDF]
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T. Sir-Petermann, E. Codner, M. Maliqueo, B. Echiburu, C. Hitschfeld, N. Crisosto, F. Perez-Bravo, S. E. Recabarren, and F. Cassorla Increased Anti-Mullerian Hormone Serum Concentrations in Prepubertal Daughters of Women with Polycystic Ovary Syndrome J. Clin. Endocrinol. Metab., August 1, 2006; 91(8): 3105 - 3109. [Abstract] [Full Text] [PDF]
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T. Ebner, M. Sommergruber, M. Moser, O. Shebl, E. Schreier-Lechner, and G. Tews Basal level of anti-Mullerian hormone is associated with oocyte quality in stimulated cycles Hum. Reprod., August 1, 2006; 21(8): 2022 - 2026. [Abstract] [Full Text] [PDF]
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 M. E. Kevenaar, M. F. Meerasahib, P. Kramer, B. M. N. van de Lang-Born, F. H. de Jong, N. P. Groome, A. P. N. Themmen, and J. A. Visser Serum Anti-Mullerian Hormone Levels Reflect the Size of the Primordial Follicle Pool in Mice Endocrinology, July 1, 2006; 147(7): 3228 - 3234. [Abstract] [Full Text] [PDF]
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 N. S. Macklon, R. L. Stouffer, L. C. Giudice, and B. C. J. M. Fauser The Science behind 25 Years of Ovarian Stimulation for in Vitro Fertilization Endocr. Rev., April 1, 2006; 27(2): 170 - 207. [Abstract] [Full Text] [PDF]
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P. Pigny, S. Jonard, Y. Robert, and D. Dewailly Serum Anti-Mullerian Hormone as a Surrogate for Antral Follicle Count for Definition of the Polycystic Ovary Syndrome J. Clin. Endocrinol. Metab., March 1, 2006; 91(3): 941 - 945. [Abstract] [Full Text] [PDF]
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 J. A Visser, F. H de Jong, J. S E Laven, and A. P N Themmen Anti-Mullerian hormone: a new marker for ovarian function Reproduction, January 1, 2006; 131(1): 1 - 9. [Abstract] [Full Text] [PDF]
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T. Silberstein, D.T. MacLaughlin, I. Shai, J.R. Trimarchi, G. Lambert-Messerlian, D.B. Seifer, D.L. Keefe, and A.S. Blazar Mullerian inhibiting substance levels at the time of HCG administration in IVF cycles predict both ovarian reserve and embryo morphology Hum. Reprod., January 1, 2006; 21(1): 159 - 163. [Abstract] [Full Text] [PDF]
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E. H. Y. Ng, O. S. Tang, C. C. W. Chan, and P. C. Ho Ovarian stromal blood flow in the prediction of ovarian response during in vitro fertilization treatment Hum. Reprod., November 1, 2005; 20(11): 3147 - 3151. [Abstract] [Full Text] [PDF]
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T. Eldar-Geva, A. Ben-Chetrit, I. M. Spitz, R. Rabinowitz, E. Markowitz, T. Mimoni, M. Gal, E. Zylber-Haran, and E. J. Margalioth Dynamic assays of inhibin B, anti-Mullerian hormone and estradiol following FSH stimulation and ovarian ultrasonography as predictors of IVF outcome Hum. Reprod., November 1, 2005; 20(11): 3178 - 3183. [Abstract] [Full Text] [PDF]
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 D. Meirow, J. Levron, T. Eldar-Geva, I. Hardan, E. Fridman, Y. Zalel, E. Schiff, and J. Dor Pregnancy after Transplantation of Cryopreserved Ovarian Tissue in a Patient with Ovarian Failure after Chemotherapy N. Engl. J. Med., July 21, 2005; 353(3): 318 - 321. [Full Text] [PDF]
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T. Eldar-Geva, E. J. Margalioth, M. Gal, A. Ben-Chetrit, N. Algur, E. Zylber-Haran, B. Brooks, M. Huerta, and I. M. Spitz Serum anti-Mullerian hormone levels during controlled ovarian hyperstimulation in women with polycystic ovaries with and without hyperandrogenism Hum. Reprod., July 1, 2005; 20(7): 1814 - 1819. [Abstract] [Full Text] [PDF]
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T. Piltonen, L. Morin-Papunen, R. Koivunen, A. Perheentupa, A. Ruokonen, and J. S. Tapanainen Serum anti-Mullerian hormone levels remain high until late reproductive age and decrease during metformin therapy in women with polycystic ovary syndrome Hum. Reprod., July 1, 2005; 20(7): 1820 - 1826. [Abstract] [Full Text] [PDF]
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E. H. Y. Ng, C. C. W. Chan, O. S. Tang, and P. C. Ho Antral follicle count and FSH concentration after clomiphene citrate challenge test in the prediction of ovarian response during IVF treatment Hum. Reprod., June 1, 2005; 20(6): 1647 - 1654. [Abstract] [Full Text] [PDF]
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A. La Marca, S. Giulini, R. Orvieto, V. De Leo, and A. Volpe Anti-Mullerian hormone concentrations in maternal serum during pregnancy Hum. Reprod., June 1, 2005; 20(6): 1569 - 1572. [Abstract] [Full Text] [PDF]
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R. Fanchin, J. Taieb, D. H. M. Lozano, B. Ducot, R. Frydman, and J. Bouyer 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., April 1, 2005; 20(4): 923 - 927. [Abstract] [Full Text] [PDF]
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J. Penarrubia, F. Fabregues, D. Manau, M. Creus, G. Casals, R. Casamitjana, F. Carmona, J. A. Vanrell, and J. Balasch Basal and stimulation day 5 anti-Mullerian hormone serum concentrations as predictors of ovarian response and pregnancy in assisted reproductive technology cycles stimulated with gonadotropin-releasing hormone agonist-gonadotropin treatment Hum. Reprod., April 1, 2005; 20(4): 915 - 922. [Abstract] [Full Text] [PDF]
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R. Fanchin, D. H. Mendez Lozano, N. Louafi, N. Achour-Frydman, R. Frydman, and J. Taieb Dynamics of serum anti-Mullerian hormone levels during the luteal phase of controlled ovarian hyperstimulation Hum. Reprod., March 1, 2005; 20(3): 747 - 751. [Abstract] [Full Text] [PDF]
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 K. Lutchman Singh, M. Davies, and R. Chatterjee Fertility in female cancer survivors: pathophysiology, preservation and the role of ovarian reserve testing Hum. Reprod. Update, January 1, 2005; 11(1): 69 - 89. [Abstract] [Full Text] [PDF]
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P. Oppelt, P.L. Strissel, A. Kellermann, S. Seeber, A. Humeny, M.W. Beckmann, and R. Strick DNA sequence variations of the entire anti-Mullerian hormone (AMH) gene promoter and AMH protein expression in patients with the Mayer-Rokitanski-Kuster-Hauser syndrome Hum. Reprod., January 1, 2005; 20(1): 149 - 157. [Abstract] [Full Text] [PDF]
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S. Jonard, P. Pigny, L. Jacquesson, C. Demerle-Roux, Y. Robert, and D. Dewailly The ovarian markers of the FSH insufficiency in functional hypothalamic amenorrhoea Hum. Reprod., January 1, 2005; 20(1): 101 - 107. [Abstract] [Full Text] [PDF]
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A. La Marca, S. Malmusi, S. Giulini, L. F. Tamaro, R. Orvieto, P. Levratti, and A. Volpe Anti-Mullerian hormone plasma levels in spontaneous menstrual cycle and during treatment with FSH to induce ovulation Hum. Reprod., December 1, 2004; 19(12): 2738 - 2741. [Abstract] [Full Text] [PDF]
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D. Nikolaou and C. Gilling-Smith Early ovarian ageing: are women with polycystic ovaries protected? Hum. Reprod., October 1, 2004; 19(10): 2175 - 2179. [Abstract] [Full Text] [PDF]
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A. G.M.G.J. Mulders, J. S.E. Laven, M. J.C. Eijkemans, F. H. de Jong, A. P.N. Themmen, and B. C.J.M. Fauser Changes in anti-Mullerian hormone serum concentrations over time suggest delayed ovarian ageing in normogonadotrophic anovulatory infertility Hum. Reprod., September 1, 2004; 19(9): 2036 - 2042. [Abstract] [Full Text] [PDF]
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E. H. Y. Ng, C. C. W. Chan, W. S. B. Yeung, and P. C. Ho Effect of age on ovarian stromal flow measured by three-dimensional ultrasound with power Doppler in Chinese women with proven fertility Hum. Reprod., September 1, 2004; 19(9): 2132 - 2137. [Abstract] [Full Text] [PDF]
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S. Jonard and D. Dewailly The follicular excess in polycystic ovaries, due to intra-ovarian hyperandrogenism, may be the main culprit for the follicular arrest Hum. Reprod. Update, March 1, 2004; 10(2): 107 - 117. [Abstract] [Full Text] [PDF]
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J. S. E. Laven, A. G. M. G. J. Mulders, J. A. Visser, A. P. Themmen, F. H. de Jong, and B. C. J. M. Fauser Anti-Mullerian Hormone Serum Concentrations in Normoovulatory and Anovulatory Women of Reproductive Age J. Clin. Endocrinol. Metab., January 1, 2004; 89(1): 318 - 323. [Abstract] [Full Text] [PDF]
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P. Pigny, E. Merlen, Y. Robert, C. Cortet-Rudelli, C. Decanter, S. Jonard, and D. Dewailly 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., December 1, 2003; 88(12): 5957 - 5962. [Abstract] [Full Text] [PDF]
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L.E. Bath, W.H.B. Wallace, M.P. Shaw, C. Fitzpatrick, and R.A. Anderson 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., November 1, 2003; 18(11): 2368 - 2374. [Abstract] [Full Text] [PDF]
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E. H. Y. Ng, W. S. B. Yeung, D. Y. T. Fong, and P. C. Ho Effects of age on hormonal and ultrasound markers of ovarian reserve in Chinese women with proven fertility Hum. Reprod., October 1, 2003; 18(10): 2169 - 2174. [Abstract] [Full Text] [PDF]
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R. Fanchin, L. M. Schonauer, C. Righini, N. Frydman, R. Frydman, and J. Taieb Serum anti-Mullerian hormone dynamics during controlled ovarian hyperstimulation Hum. Reprod., February 1, 2003; 18(2): 328 - 332. [Abstract] [Full Text] [PDF]
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