Reproductive BioMedicine Online (2010) 20, 861– 865

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ARTICLE

Effect of cigarette smoking upon reproductive

hormones in women of reproductive
age: a retrospective analysis
a,*
AL Waylen , GL Jones b, WL Ledger c

a
University of Sheffield School of Medicine and Biomedical Sciences, Beech Hill Road, Sheffield S10 2RX, UK; b Health
Services Research Section, ScHARR, Regent Court, 30 Regent Street, Sheffield S1 4DA, UK; c Academic Unit of Reproductive
and Developmental Medicine, Jessop Wing Hospital, Tree Root Walk, Sheffield S10 2TJ, UK
* Corresponding author. E-mail addresses: mda03aw@doctors.org.uk, mda03aw@sheffield.ac.uk (AL Waylen).

Anna Waylon attended the University of Sheffield School of Medicine from September 2003 to July 2009 during
which time she completed a Bachelor of Medical Science degree in the Academic Unit of Reproductive and
Developmental Medicine. Her research involved investigating the effects of cigarette smoking on female
reproductive hormones and on the clinical outcomes of assisted reproduction, and a qualitative assessment of
women’s knowledge of factors that could affect their fertility.

Abstract There is continuing debate concerning the relationship between cigarette smoking and premature ovarian failure. The aim
of this retrospective data analysis was to investigate whether smoking has a measurable effect on early follicular serum concentra-
tions of inhibin B hormone, FSH and anti-Müllerian hormone (AMH) in women of reproductive age. A database containing data on age,
smoking status and serum concentrations of inhibin B, FSH and AMH was analysed. Pearson’s correlation coefficient was calculated
to determine the correlation between hormone concentrations and age. One-way analysis of variance was used to determine any
significant difference in age between smoking categories and a univariate general linear model was used to compare geometric
means and geometric mean ratios of hormone concentrations in relation to smoking status. Serum concentrations of inhibin B were
significantly lower in women who had ever smoked cigarettes: F(2,332) = 3.371, P = 0.036. There was no statistically significant dif-
ference in FSH or AMH concentrations although a trend towards lower AMH concentrations in smokers was observed. This analysis
provides evidence of an advancement of ovarian ageing in women who smoke cigarettes and is relevant to women of childbearing
age who wish to avoid premature decline in fertility. RBMOnline
ª 2010, Reproductive Healthcare Ltd. Published by Elsevier Ltd. All rights reserved.
KEYWORDS: cigarette, infertility, inhibin B, ovarian reserve, smoking

Introduction giving birth for the first time inside marriage increasing by
almost 6 years since 1971 (Office for National Statistics,
There is a trend in the UK towards deferral of childbearing 2007). Postponement of childbearing and societal changes
until older maternal age, with the average age of women in family planning have led to a significant increase in the

1472-6483/$ - see front matter ª 2010, Reproductive Healthcare Ltd. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.rbmo.2010.02.021
862 AL Waylen et al.

incidence of unwanted infertility due to the diminished (de Vet et al., 2002; Tremellen et al., 2005). Serum AMH
ovarian reserve associated with female reproductive ageing concentrations also show little inter-cycle variability in wo-
(Broekmans et al., 2006). men of reproductive age (Fanchin et al., 2005).
Ovarian reserve can be defined as the remaining func- Conflicting evidence exists regarding the effect of ciga-
tional capacity of the ovary, reflecting both the quantity rette smoking upon existing measures of ovarian reserve
and the quality of oocytes that remain (Nikolaou and (Kinney et al., 2007). Consequently, the aim of this retro-
Templeton, 2004). Ovarian reserve is observed to decline spective data analysis was to determine whether women
with age as a woman approaches menopause, as a result who have a previous or current history of cigarette smoking
of atresia and recruitment to ovulation, in addition to a de- are at an increased risk of premature ovarian failure com-
cline in oocyte quality (Nikolaou and Templeton, 2003). It is pared with age-matched non-smoking controls.
widely recognized that the onset of menopause and total
loss of fertility is preceded by a period of subfertility and,
assuming that this period of time is fixed, women with early Materials and methods
onset of menopause will also be expected to experience
earlier onset of subfertility, recognized as early ovarian Data collection
ageing (Johnson et al., 2006).
Age is not the only factor that contributes to ovarian age- An existing database containing data on age, smoking status
ing (Cramer et al., 2002; Gracia et al., 2005; Kinney et al., and serum concentrations of inhibin B, FSH and AMH was
2007; Lambert-Messerlian and Harlow, 2006). In the light of used to investigate whether there was a significant effect
increasing maternal age at first birth and the associated of cigarette smoking on these hormones. The data had been
increased risk of infertility, knowledge of other factors that collected from women who had purchased a test for assess-
can increase the risk of early ovarian ageing and thus affect ment of ovarian reserve, which involved a blood sample
ovarian reserve becomes more significant to women who taken on day 2 or 3 of the menstrual cycle. Women all
wish to make informed lifestyle decisions about factors that had cycle length of 27–34 days, with a minimum of 1 month
may affect their fertility. between last taking contraceptive pills and testing. Permis-
Cigarette smoking is one such factor that has been asso- sion to use anonymous data for research purposes had been
ciated with premature ovarian failure, indicated by the fact given and recorded at the time of testing.
that female cigarette smokers enter the menopause on
average 1.5–2 years earlier than non-smokers (Practice
Committee of the American Society for Reproductive Hormone assays
Medicine, 2004). However, it is not known whether this
effect is mediated by a reduction in ovarian follicle number Hormone concentrations stored in the database had been
before menopause and there is little evidence available to determined from venous blood samples taken on day 2 or
determine the exact mechanisms that underlie this prema- 3 of the menstrual cycle.
ture decline in fertility. Inhibin B samples were assayed in duplicate using a com-
Ovarian reserve testing provides a means for measuring mercial ELISA kit (Oxford Bio-Innovation, Oxford, UK)
such an effect. Over the past two decades, a wealth of ovar- according to the manufacturer’s protocol. The functional
ian reserve tests have been designed that allow the impact sensitivity of the assay was 15.6 pg/ml. The intra- and in-
of factors that can affect fertility to be measured. These ter-assay variability were <7%. Serum FSH concentrations
tests are also used to predict outcomes of assisted repro- were determined using a two-site immunoradiometric assay
duction technologies and to determine when the most principle (Oxford Bio-Innovation). The functional sensitivity
appropriate time to start a family may be. Many ovarian re- of FSH was 0.11 mIU/ml and intra- and inter-assay variabil-
serve tests are based upon hormonal measurements made at ity were <4% and <8%, respectively. Anti-Müllerian hormone
specific times of a woman’s menstrual cycle. samples were assayed in duplicate using a commercial ELISA
Three hormones often used in ovarian reserve testing are kit (Oxford Bio-Innovation) according to the manufacturer’s
inhibin B, FSH and anti-Müllerian hormone (AMH): each of protocol. The sensitivity of the assay was 0.017 ng/ml. The
these is considered useful in the assessment of ovarian intra- and inter-assay variability were <5 and 8%, respec-
reserve. Inhibin B is reduced in women with a diminished tively. There is currently no international reference stan-
ovarian reserve (Erdem et al., 2004) and has been shown dard for AMH. Using this assay, less than 5 pmol is low, 5–
to be a more sensitive and specific marker of ovarian re- 15 is normal and over 15 is high, with the conversion factor
serve than other parameters, including FSH, oestradiol for ng/ml to pmol/l of approximately · 7.
and antral follicle count (Ficicioglu et al., 2003; Seifer
et al., 1999). A rise in early follicular FSH concentrations
have been shown to reflect a quantitative decline in ovarian Statistical analysis
reserve (Abdalla and Thum, 2004), and the hormone is re-
garded as a superior marker of follicle depletion in compar- All statistical analyses were performed using the Statistical
ison to age (Toner et al., 1991). As AMH is produced by the Package for Social Sciences version 14.0 for Windows (SPSS,
granulosa cells of secondary, pre-antral and early antral fol- Chicago, USA).
licles of the ovary, day 2–3 serum AMH concentrations have Descriptive statistics were applied to the data to analyse
a strong correlation with other markers of ovarian ageing age and hormonal assays for women in each of the smoking
such as antral follicle count (van Rooij et al., 2002) and is categories (never smoked, ex-smoker and current smoker).
thought to be an early marker of a decline in ovarian reserve Mean values and measures of distribution including standard
The effect of cigarette smoking on reproductive hormones 863

deviation and range were calculated for each parameter in and current smokers (64.4 pg/ml). The geometric mean ra-
all groups. tio for never smokers compared with ex-smokers was 1.19
The distribution of the residuals of each parameter was (95% CI 1.01–1.41, P = 0.038) and for never smokers com-
modelled and examined for normality of distribution. Data pared with current smokers was 1.24 (95% CI 1.00–1.52,
with a distribution deviating from normal (all hormonal P = 0.046).
parameters) were logarithmically transformed before anal- There was no statistically significant difference be-
ysis and reported in the form of geometric means with any tween mean serum FSH concentration between the smok-
significant differences between groups reported as a geo- ing categories, after adjustment for age (in ANCOVA):
metric mean ratio. Levene’s test was used to assess homo- F(2,332) = 0.173.
geneity of variance and used to evaluate the assumptions of ANCOVA revealed no statistically significant difference in
the parametric tests. mean serum AMH concentration between the smoking cate-
Pearson’s correlation coefficient was calculated to gories after adjustment for age: F(2,332) = 0.895. However,
determine any correlation between the hormone concentra- a trend towards a decreasing serum AMH concentration with
tions and age, and between the hormone concentrations an increasingly active smoking status was observed.
themselves.
Demographic data for age was analysed using a one-way Discussion
analysis of variance (ANOVA) to determine any significant
difference between smoking categories. The analysis of hor-
monal assays with regard to smoking status was carried out The results of this retrospective data analysis provide evi-
using a univariate general linear model (ANCOVA), in which dence of a significant effect of cigarette smoking upon early
age was entered as a covariate to exclude any confounding follicular-phase serum inhibin B concentration. Day 2–3
effect. Geometric mean ratios were calculated with 95% serum inhibin B concentrations were significantly lower in
confidence intervals where a statistically significant differ- women of reproductive age who had either a previous or
ence existed. current history of cigarette smoking, compared with women
The level of statistical significance for all tests was who had never smoked cigarettes. There was no evidence of
determined at P < 0.05. a significant effect of smoking upon serum concentrations of
FSH or AMH.
The significant decrease observed in serum inhibin B con-
Results centration is analogous to the fall in inhibin B usually ob-
served with age (Welt et al., 1999), suggesting that
Demographic data cigarette smoking contributes to early ovarian ageing. The
findings of the current study are consistent with those of
Hormone concentrations from a total of 335 women were Lambert-Messerlian and Harlow (2006), who reported for
analysed with regard to smoking status. Of these women, the first time that smoking history had a significant negative
202 were non-smokers, 86 were ex-smokers and 47 were association with inhibin B concentrations. The validity of
current smokers. The mean age of the total sample was the results from the latter study is high: the sample size
37.1 years (range 24–48, SD 4.1). Analysis by one-way ANO- was large (404 women, of whom 203 had a history of ciga-
VA revealed no significant difference in mean age observed rette smoking), the smokers reported a strong history of cig-
between the different smoking groups: F(2,332) = 0.049 arette smoking (an average of 17 cigarettes daily for an
(Table 1). average of 17 years) and inhibin B measurements were
based on a mean calculated from at least three blood sam-
Hormone assay correlations ples per patient over a period of 18 months. However, other
literature regarding the effect of cigarette smoking upon in-
hibin B is inconsistent, with other researchers failing to find
A Pearson’s correlation coefficient was calculated for each
any significant effect of cigarette smoking upon serum con-
of the hormones to determine any correlation between
centrations of this hormone (Gracia et al., 2005; Kinney
these values and age. All measures were significantly corre-
et al., 2007).
lated with age: log inhibin B (r = –0.202), log FSH (r = 0.276)
Cigarette smoking has long been associated with a nega-
and log AMH (r = –0.461); all P < 0.01. Log FSH was nega-
tive effect on fertility and has been identified by several
tively correlated with the other hormones: log inhibin B
studies to be a causative factor for an earlier onset of men-
(r = –0.227) and log AMH (r = –0.503). Log AMH was posi-
opause (Practice Committee of the American Society for
tively correlated with log inhibin B (r = 0.468); all P < 0.001.
Reproductive Medicine, 2004). However, the exact mecha-
nism by which cigarette smoking diminishes reproductive
Hormone assays and smoking status capacity is currently unknown. Findings from the current
study provide evidence of a direct effect of smoking on
The geometric mean values and 95% CI for each of the hor- ovarian follicles, indicated by the significant effect upon
monal assays by smoking group were calculated (Table 1). serum inhibin B concentrations. Inhibin B is produced by
The geometric mean serum concentrations of inhibin B the granulosa cells of early antral follicles of the cohort
were significantly different between the smoking groups: recruited in each menstrual cycle and therefore a fall in
F(2,332) = 3.371, P = 0.036. The mean serum concentration inhibin B is likely to reflect a reduction in antral follicle
was highest in the group that had never smoked cigarettes count: a finding usually observed with reproductive ageing
(79.8 pg/ml), compared with the ex-smokers (67.0 pg/ml) (Erdem et al., 2004). Therefore, cigarette smoking may lead
864 AL Waylen et al.

Table 1 Mean age and serum hormone concentrations according to smoking status.
Non-smoker Ex-smoker Current smoker ANOVA/ANCOVAa

Sample size 202 86 47 –

Age (years)b 37.1 (4.2) 37.0 (4.1) 37.0 (3.7) 0.049, NS
Inhibin B (pg/ml)c 79.8 (72.8–87.3) 67.0 (58.2–76.9) 64.4 (53.5–77.8) 3.371, P = 0.036d
FSH (IU/l)c 5.1 (4.8–5.5) 5.3 (4.8–5.8) 5.3 (4.7–6.0) 0.173, NS
AMH (ng/ml)c 1.074 (0.925–1.245) 0.955 (0.760–1.199) 0.869 (0.638–1.183) 0.895, NS

Values are mean (standard deviation) or mean (95% CI).

ANOVA = analysis of variance; ANCOVA = analysis of co-variance.
AMH = anti-Müllerian hormone; FSH = follicle-stimulating hormone; NS = not statistically significant.
a
ANOVA model used for comparison of mean age. ANCOVA model used with age as covariate for comparison of geometric
mean hormone concentrations. F(2,332).
b
Arithmetic mean.
c
Geometric mean.
d
P-value for comparison between non-smokers, ex-smokers and current smokers.

to a premature depletion of the follicle pool available for increased production of this hormone due to a quantitative
recruitment, causing premature ovarian failure. However, diminishment of the ovarian follicular pool (Abdalla and
it is still unclear whether cigarette smoking reduces Thum, 2004). Serum concentrations of AMH and inhibin B
the quality as well as quantity of follicles available for were negatively correlated with age, consistent with the
recruitment. Further studies are required to confirm the correlation of these hormones known to be associated with
relationship between cigarette smoking and inhibin B con- reproductive ageing (Lee et al., 1996; Welt et al., 1999).
centrations and to further explain the mechanisms of any A significant limitation of this study is the inability to ac-
such action. count for demographic and clinical heterogeneity in the
The present study found no significant effect of cigarette data, due to the lack of socio-demographic and clinical data
smoking (either past or current) on early follicular-phase that had been collected for the women from whom the
FSH concentrations, despite a wealth of evidence suggesting blood samples had been taken. It was therefore not possible
that such an effect does in fact exist (Cooper et al., 1995; to further analyse the data with regard to factors, such as
Cramer et al., 2002; El-Nemr et al., 1998; Kinney et al., past medical, reproductive and menstrual cycle history or
2007). Serum FSH concentrations are known to rise with ethnicity. It was also not possible to account for body mass
increasing ovarian age, therefore acting as a marker of ovar- index, alcohol or caffeine intake, all of which have previ-
ian ageing (Kline et al., 2005), but this rise is considered to ously been shown to affect reproductive hormones and fer-
be a late marker of a diminished ovarian reserve (Broekmans tility (Gracia et al., 2005; Kinney et al., 2007). Furthermore,
et al., 1998; Burger et al., 1999; Kline et al., 2005). It is data regarding other potential measures of ovarian reserve
therefore possible that the inconsistency between the re- including AFC and oestradiol were not included in the data-
sults observed in the present study and the main body of evi- base and thus not available for analysis.
dence to date may be a reflection of differences in the The data regarding smoking status were also inadequate
mean age of women involved in these studies: the mean to enable an in-depth analysis of smoking history: there was
age of the sample in the present study was 37.1 years (range no information available on the number of cigarettes
24–48) and thus included many young women for whom a smoked per day, duration of smoking habit, time since stop-
smoking related decline in ovarian reserve may not yet be ping smoking or passive smoking exposure. It is therefore
reflected by serum FSH concentrations. not possible to comment on the effect of smoking according
No statistically significant difference was observed for to the number smoked per day, but rather to report results
day-2–3 serum AMH concentrations in women with a history for smoking history in general at time of hormone
of smoking compared with those that had never smoked. measurement.
However, a trend towards a decrease in both previous and Finally, the smoking status of the women was ascer-
current smokers was observed. A recent review found serum tained by self-report and not confirmed by any other mea-
AMH concentrations to have only moderate sensitivity in sure, such as urinary cotinine. It is possible that due to
detecting diminished ovarian reserve (Broekmans et al., the sensitive nature of ovarian reserve testing and the neg-
2006), which may account for the lack of a definitive finding ative effects associated with cigarette smoking upon gen-
in this study. Literature to date has shown a significant ef- eral health, the women did not divulge their true smoking
fect of smoking upon serum AMH concentrations (Freour status. Despite these concerns, findings of a study by Patrick
et al., 2008), but the paucity of research demands future et al. (1994) report the validity of self-reported smoking to
studies to determine whether the trend observed in the be good.
present study is also indicative of any significant effect Longitudinal prospective studies measuring serum hor-
and to further investigate the underlying mechanisms. monal concentrations including inhibin B are required in co-
Consistent with current literature, the hormone profiles horts of smoking and non-smoking women of reproductive
generated in this study were all significantly associated with age to determine the difference in hormone concentrations
age. FSH was positively correlated with age, reflecting the in these groups throughout the reproductive lifespan. Stud-
The effect of cigarette smoking on reproductive hormones 865

ies should endeavour to collect socio-demographic and clin- Ficicioglu, C., Kutlu, T., Demirbasoglu, S., et al., 2003. The role of
ical information about participants in order to allow inhibin B as a basal determinant of ovarian reserve. Gynecol.
researchers to identify and account for heterogeneity and Endocrinol. 17, 287–293.
confounding factors, and to ensure generalizability of re- Freour, T., Masson, D., Mirallie, S., et al., 2008. Active smoking
compromises IVF outcome and affects ovarian reserve. Reprod.
sults to the general population. Findings from such studies
Biomed. Online 16, 96–102.
will have greater power than retrospective data analyses. Gracia, C., Freeman, E.W., Sammel, M.D., et al., 2005. The
In conclusion, this study provides further evidence that relationship between obesity and race on inhibin B during the
cigarette smoking increases the risk of premature ovarian menopause transition. Menopause 12, 559–566.
failure in women of reproductive age. The fall in serum con- Johnson, N.P., Bagrie, E.M., Coomarasamy, A., et al., 2006.
centrations of inhibin B observed with smoking is compara- Ovarian reserve tests for predicting fertility outcomes for
ble to that associated with increasing age and therefore assisted reproductive technology: the International Systematic
indicates a risk of premature ovarian failure. Whilst no sig- Collaboration of Ovarian Reserve Evaluation protocol for a
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Kinney, A., Kline, J., Kelly, A., et al., 2007. Smoking, alcohol and
AMH concentrations was seen and further investigation is re-
caffeine in relation to ovarian age during the reproductive years.
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Declaration: The authors report no financial or commercial
Fanchin, R., Taieb, J., Lozano, D.H., et al., 2005. High reproduc-
conflicts of interest.
ibility of serum anti-Mullerian hormone measurements suggests
a multi-staged follicular secretion and strengthens its role in the
Received 11 August 2009; refereed 2 November 2009; accepted 25
assessment of ovarian follicular status. Hum. Reprod. 20, 923–
January 2010.
927.