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Journal of Clinical Endocrinology & Metabolism , doi:10.1210/jc.2007-2093
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The Journal of Clinical Endocrinology & Metabolism Vol. 93, No. 6 2129-2134
Copyright © 2008 by The Endocrine Society

Relationship of Serum Antimüllerian Hormone Concentration to Age at Menopause

J. van Disseldorp, M. J. Faddy, A. P. N. Themmen, F. H. de Jong, P. H. M. Peeters, Y. T. van der Schouw and F. J. M. Broekmans

Department of Reproductive Medicine and Gynaecology (J.v.D., F.J.M.B.) and Julius Center for Health Sciences and Primary Care (P.H.M.P., Y.T.v.d.S.), University Medical Center Utrecht, 3508 GA Utrecht, The Netherlands; School of Mathematical Sciences (M.J.F.), Queensland University of Technology, Brisbane, Queensland 4000, Australia; and Department of Internal Medicine (A.P.N.T., F.H.d.J.), Erasmus Medical Center, 3015 GD Rotterdam, The Netherlands

Address all correspondence and requests for reprints to: J. van Disseldorp, University Medical Center Utrecht, P.O. Box 85500, Room F.05.126, 3508 GA, Utrecht, The Netherlands. E-mail: j.vandisseldorp-2{at}umcutrecht.nl.


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
Background: Serum antimüllerian hormone (AMH) levels are highly correlated with antral follicle counts, while being menstrual cycle independent and easily measurable. However, AMH, unlike antral follicle counts, has not been tested as yet as a predictor of reproductive status. By relating AMH levels to the age distribution of reproductive events like onset of menopause, we tested this hypothesis.

Methods: AMH levels were measured in 144 fertile normal volunteers and used to determine an estimate of mean AMH as a function of age. Data on the onset of menopause were obtained from the population-based Prospect-European Prospective Investigation into Cancer and Nutrition [Prospect-EPIC] cohort. Estimation of an AMH threshold to predict menopause was done by maximum likelihood using the observed (Prospect-EPIC) distribution of age at menopause and the predictive distribution from this AMH threshold. Predictions of age at menopause follow from an individual woman’s AMH relative to percentiles of the distribution of AMH for a given age, and the corresponding percentiles of the predictive distribution of age at menopause.

Results: There was good conformity between the observed distribution of age at menopause and that predicted from declining AMH levels.

Conclusions: The similarity between observed and predictive distributions of age at menopause supports the hypothesis that AMH levels are related to onset of menopause. Results of this study suggest that AMH is able to specify a woman’s reproductive age more realistically than chronological age alone.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
Antimüllerian hormone (AMH) (or müllerian inhibiting substance) is considered a quantitative marker for ovarian reserve (1, 2, 3). Animal studies have shown AMH to play a role in the primary follicle depletion rate by inhibiting the transition from primordial follicles into primary follicles (4). AMH appears to correspond well with antral follicle counts (AFCs) and ovarian response to hyperstimulation in in vitro fertilization (IVF) (3, 5, 6). In addition, AMH has been the marker that best reflects the gradual decline in reproductive capacity with increasing age (2, 3, 7, 8, 9, 10). Because of its presumed menstrual cycle independence, it is valued as a marker for ovarian reserve that may become the test of choice over other tests like those based on AFCs (5, 11, 12).

The decrease of female reproductive capacity with age is believed to be a consequence of the similar decline in follicle numbers (13, 14, 15). AFCs have been considered to reflect reproductive status because they are related to age at menopause and age at birth of the last child (16). However, only low AFCs provide clinically useful estimates of reproductive status. Moreover, AFCs show some cycle to cycle variation and may be prone to observer bias (16, 17). AMH on the other hand does not vary so much between cycles (18), is easily measurable, and is highly correlated with AFCs (3, 12). In this paper we consider whether AMH does reflect reproductive status, by modeling its relation to age at menopause.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Subjects

To relate age-dependent changes in AMH measured in an ovulatory cycle with variation in age at menopause, we combined two sources of information.

First, for AMH measurement, a group of 144 healthy, regularly cycling, fertile, predominantly Caucasian female volunteers aged 25–46 yr was recruited through advertisements in local newspapers (17). Volunteers were enrolled in the study protocol if they met all of the following criteria: 1) regular menstrual cycles, with mean length varying from 21–35 d; 2) biphasic basal body temperature; 3) proven natural fertility by having carried at least one pregnancy to term; 4) each achieved pregnancy was established within 1 yr after the interruption of contraceptive methods; 5) no evidence of endocrine disease; 6) no history of ovarian surgery; 7) no ovarian abnormalities, as assessed by vaginal ultrasound; and 8) cessation of hormonal contraception at least 2 months before entering the study protocol. From all volunteers an AMH blood sample was obtained at cycle day 3. The study was approved by the institutional review board. All participants gave written informed consent and received monetary compensation for participating.

Second, to estimate the distribution of age at menopause, a sample of Dutch women participating in the Prospect-European Prospective Investigation into Cancer and Nutrition (EPIC) study was used (19, 20). For the Prospect-EPIC study, a total of 17,357 women 50–70 yr of age was recruited from an ongoing nationwide breast cancer screening program conducted in The Netherlands. Data on reproductive history were obtained from a questionnaire. Menopause was defined according to the World Health Organization classification as a condition of absence of spontaneous menstrual bleeding for more than 12 months. For the current study, a cross-sectional cohort (n = 5449) of women with a natural menopause and who conceived at least one child was selected from the initial prospective cohort to create a high level of comparability with the other women used in this study. Furthermore, only women 58 yr and older were selected to prevent underrepresentation of women who reached menopause late in their life, leaving 3384 women who met all these criteria to be included in the present analysis.

Hormone assays

AMH concentrations were measured in serum from blood samples stored at –20 C until processed. In all samples, AMH levels were estimated using an enzyme-immunometric assay (Diagnostic Systems Laboratories, Inc., Webster, TX). Interassay and intraassay coefficients of variation were less than 5% at the level of 3 µg/liter and less than 11% at the level of 13 µg/liter. The detection limit of the assay was 0.026 µg/liter. Repeated freezing and thawing of the samples or storage at 37 C for 1 h did not affect the results of the assay (10). The current assay was compared with the ultrasensitive Immunotech-Coulter assay (Marseilles, France) in a previous publication (21). To be able to compare our results with earlier published data, all results need to be multiplied by a factor of 2.0.

Analysis

The AMH values obtained from the study of normal fertile volunteers were plotted against age, and locally quadratic smoothing (22) was used to estimate the change in mean AMH level with age. A smoothed distribution of the residual deviations of the actual AMH levels from this estimated mean was then determined using methods described by Faddy (23). This residual distribution and the estimated change in mean AMH with age formed a model for age-related change of AMH. Moreover, it was hypothesized that this variation in AMH would correspond to variation in the future occurrence of reproductive events, such as menopause.

Assuming that menopause is triggered by AMH decreasing below a certain threshold, the model was used to obtain a predictive distribution of age at menopause. This distribution was then matched to the Prospect-EPIC data on age at menopause to derive an estimate of the AMH menopausal threshold level. Agreement between this predictive distribution and the observed distribution of age at menopause was assessed by a visual comparison of the distributional shapes, and a quantile-quantile plot, in which quantiles of the observed distribution are plotted against corresponding quantiles of the predictive distribution.

For individual women, predictions of age at menopause could then be done using quantiles of the predictive distribution. From each woman’s data on AMH and age, she was placed in a percentile band (lower 5, 5–10, 10–25, 25–50, 50–75, 75–90, 90–95, or upper 95%) from the model for age-related change of AMH using the estimated residual distribution (e.g. a woman aged 33 yr would have an AMH of 0.6 or less with probability 0.1, and 1.9 or less with probability 0.25, etc.). From the corresponding quantiles of the predictive distribution of age at menopause, classification into one of eight categories for age at menopause then follows. In this way, predictions of age at menopause can be made on the basis of AMH level and age.


   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
Figure 1Go shows the AMH data plotted against the women’s ages, and the smoothed estimate of mean AMH levels. The use of a logarithmic transformation of AMH here reflects the heterogeneity in AMH variation (high levels showing more variation than low levels) with more homogeneous variation apparent on the logarithmic scale. The distribution of the residual deviations of the data points about this estimated mean was markedly left skewed (more points showing less dispersion above the estimated mean than below it in Fig. 1Go). This residual distribution and the estimated mean provide a model for age-dependent change in AMH levels: a woman with a low value at a young age will have depleted her follicle pool at an earlier age than a woman with a high value and the same age. The mean AMH only declines after about age 30 (±3) yr, so AMH can only be regarded as being correlated with declining ovarian reserve after this age.


Figure 1
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  		FIG. 1. Age-dependent AMH levels (•) plotted on a logarithmic scale to show more homogeneous variation (n = 144). The solid line indicates the smoothed estimate of mean AMH level as a function of age.

 
The Prospect-EPIC data set showed a mean age at which women experienced menopause of 50.4 yr (SD = 4.1; median = 51). The distribution of age at menopause was left skewed (Fig. 2Go), probably because premature ovarian failure caused menopause to occur early in life in some women, and similar in shape to the AMH residual distribution referred to previously.


Figure 2
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  		FIG. 2. Comparison of the observed distributions of age at menopause from the Prospect-EPIC data (bars) and the predicted age at menopause using the AMH threshold model (- - -), indicating good concordance between the two distributions, particularly between the ages of 42 and 56 yr as evidenced by the quantile-quantile plot (inset).

 
Because there is an age difference between the AMH and Prospect-Epic cohorts, Table 1Go displays some environmental and generational characteristics of both cohorts.


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  		TABLE 1. Baseline characteristics of the AMH and Prospect-EPIC cohorts

 
Maximum likelihood estimation using the data on age at menopause and a predictive distribution derived from a threshold AMH level (measured with the Diagnostic Systems Laboratories assay) below which women experience menopause (cf.16) resulted in an estimated threshold of 0.086 µg/liter (using the Immunotech-Coulter assay, the AMH threshold level would be 0.172 µg/liter). The distribution of menopausal ages so predicted from declining AMH levels and this threshold was in good concordance with the Prospect-EPIC data distribution, as shown by the plots in Fig. 2Go. Thus, the observed age distribution is well matched by the predictive distribution, except possibly at very low (≤41yr) and very high (≥57 yr) ages.

Estimated percentile categories for AMH and age are shown in Fig. 3Go, with AMH again on a logarithmic scale (cf. Fig. 1Go), together with the corresponding estimated ages at which menopause would be expected to occur (AMP) in the inset (with SEs in parentheses). This figure illustrates that a woman with an AMH low for her age (*) is likely to experience menopause at a younger age (between 41 and 44 yr) or some 7 (±0.4) to 10 (±0.5) yr before the median age of 51 yr, which would be the expectation without the additional information provided by AMH. Similarly, one with higher AMH for her age (#) can expect to become menopausal at a later age (between 51 and 53 yr), or up to 2 (±0.1) yr after the median age.


Figure 3
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  		FIG. 3. The relationship between AMH and age presented in terms of the 5th and 95th (· · · · · ·), 10th and 90th (- · - · -), and 25th and 75th (- - -) percentiles, and the median (——), with the menopausal threshold for AMH indicated by the solid vertical line. Corresponding percentiles (± SE) for predicted age at menopause (AMP) are shown in the inset. The examples indicated by the asterisk (*) and number sign (#) show that a woman with an AMH low for her age (*) is likely to experience menopause at a younger age than the median age of 51 yr, which would be the expectation without the additional information provided by AMH. Similarly, one with higher AMH for her age (#) can expect to become menopausal at a later age.

 

   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
In this study it has been shown that there was a good level of conformity between the distribution of observed age at menopause and the predictive distribution based on a modeled mean decline of AMH with age and the application of a menopausal threshold AMH level. This approach assumes that changes in reproductive status and AMH levels are related. The close correspondence between actual and predictive distributions of age at menopause supports such a relationship.

AMH levels of postmenopausal women have been mostly undetectable (24). However, in women followed into menopause prospectively, the finding of one or two antral follicles by ultrasound is not exceptional (25, 26). Therefore, a threshold AMH level of 0.086 µg/liter, not far from the detection limit of the assay of 0.026 µg/liter, would seem to be a plausible cutoff for the occurrence of menopause. Moreover, in a recent study, AMH levels in women with cancelled IVF cycles due to poor response, a condition regarded as close to the onset of the menopausal transition (27), ranged from 0.098–0.63 µg/liter, with a mean of 0.175 ± 0.04 µg/liter on the Immunotech-Coulter assay (28). Because the menopausal transition is considered to precede menopause by some 4–6 yr (29) and because the decline in AMH in this period is quite slow, the calculated threshold seems to fit quite well between the observed levels for the postmenopausal state and the onset of the menopausal transition (30).

The reliability of the Prospect-EPIC cohort in providing a distribution for age at onset of menopause has already been addressed (16). The Prospect-EPIC distribution of age at menopause is similar to that observed in other epidemiological studies (31).

Comparability of the Prospect-EPIC and AMH cohorts (Table 1Go) can be assessed from the following considerations. First, there has not been identified a consistent set of lifestyle or nutritional factors that influence age at menopause, apart from smoking, which was comparable in both cohorts (Table 1Go) (17, 19). Second, both cohorts stem from the same female Caucasian society, albeit that they differ in age at inclusion by some 30 yr. Finally, although body mass index (BMI) and age at first child differed between the two cohorts, the first relates to the age at which BMI was determined and the latter to differences in reproductive behavior across generations. Therefore, it is unlikely that either genetic or environmental factors would have had a major influence on the results presented.

Previous studies addressing the validity of recalling age at menopause showed that 70% of women recall their age at menopause accurately within 1 yr, limiting the effect of recall bias (32, 33).

Considering that the large variation in AMH levels in normal fertile volunteers reflects an equally large variation in reproductive status of these women, AMH may be regarded as a useful predictor of an individual’s reproductive capacity. Moreover, in IVF, AMH has been a good predictor of ovarian response (6, 10, 28, 34, 35, 36). Because a poor response after ovarian hyperstimulation is regarded as a state of diminished ovarian reserve, prediction of this from AMH levels underlines its potential as a test for general reproductive status.

Recent research has shown that AFCs currently provide the best performance in predicting poor response in IVF treatment (37), while data on AMH have also started to accumulate. AMH and AFC values have been shown to be highly correlated (38), and levels of AMH, which is produced by granulosa cells of small antral follicles in the size range of 2–7 mm (39), are considered to be a reflection of the size of the primordial follicle pool (1, 17).

In an earlier report, modeling of AFC and the occurrence of menopause using an AFC threshold of zero or one follicle was described (16). This model and the present one using an AMH threshold both fitted the available data comparably well, and so the association of age at menopause with AMH is similar to that with AFC. However, a limitation of using AFC in the prediction of menopause is its intercycle variability (40), which causes only consistently low AFC values to be informative and of potential predictive value. AMH has been demonstrated to vary only minimally from cycle to cycle (18), and levels appear to be cycle independent (5, 12). Together, these findings indicate that AMH may be a marker for reproductive status at least as good as AFC.

The data presented here suggest that AMH is capable of specifying a woman’s reproductive status more realistically than chronological age alone. Because menopausal prediction using age and AMH level has been done using percentile categories, this prediction cannot be precise. Prediction for younger women may be more problematic because observed AMH levels are underrepresented at younger ages, and Fig. 1Go and a recent study in mice show that mean AMH levels do not decline at young ages (1). Longitudinal studies starting with women in their 20s, gathering any endocrine, ultrasound, and genetic information that may possibly relate to reproductive aging, and recording of natural menopause many years later, may be the only definitive way to develop testing for expected reproductive life span. Because such studies are unlikely in practice, prediction of reproductive life span depends on cross-sectional studies.

Recently, several studies have addressed possible relationships between endocrine, ultrasound, and genetic factors, and age at menopause. van Rooij et al. (2) showed a relationship between AMH and inhibin B and cycle irregularity, a proxy variable for the menopausal transition. Broekmans et al. (16) reported on the predictive capacity of AFC to predict age at last child and onset of menopause. Tempfer et al. (41) and Hefler et al. (42) found estrogen metabolizing gene polymorphisms and polymorphisms associated with thrombophilia and vascular homeostasis to be associated with earlier onset of menopause. Further research is necessary to determine which factors are the best predictors of menopause.

In conclusion, this study shows that AMH levels are related to reproductive events such as age of onset of menopause, at a population level. The results suggest that AMH reflects a woman’s reproductive age more realistically than chronological age alone.


   Acknowledgments
 
We thank the reviewers of an earlier draft for their many useful comments that have improved the present manuscript.


   Footnotes
 
The Prospect-European Prospective Investigation into Cancer and Nutrition cohort was funded by "European Commission: Public Health and Consumer Protection Directorate 1993–2004; Research Directorate-General 2005-," the Dutch Ministry of Health, the Dutch Cancer Society, ZonMw The Netherlands Organisation for Health Research and Development, and World Cancer Research Fund.

Disclosure Statement: The authors have nothing to disclose.

First Published Online March 11, 2008

Abbreviations: AFC, Antral follicle count; AMH, antimüllerian hormone; BMI, body mass index; EPIC, European Prospective Investigation into Cancer and Nutrition; IVF, in vitro fertilization.

Received September 18, 2007.

Accepted March 5, 2008.


   References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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