297

ORIGINAL
Variation of urinary follicle-stimulating hormone level after
menopause : From the results of Japan Nurses’ Health Study
Toshiyuki Yasui1), Yuki Ideno2), Yoko Onizuka3), Junko Nakajima-Shimada3), Hiromitsu Shinozaki3),
and Kunihiko Hayashi3)
Department of Reproductive and Menopausal Medicine, Institute of Biomedical Sciences, Tokushima University Graduate School, Tokushima, Japan, 2)Big Data Centre for Integrative Analysis, Gunma University Initiative for Advanced Research, Gunma, Japan, 3)Department of
Basic Medical Sciences, School of Health Sciences, Gunma University, Gunma, Japan
1)

Abstract : The change in follicle-stimulating hormone (FSH) during the menopausal transition and associationsof FSH with various diseases have been assessed by using blood samples. We examined cross-sectionally the variation of FSH levels, associations of estrone and estradiol with FSH, and associations of BMI with these hormonesby using urinary samples from peri- and postmenopausal women in Japan. Of 4472 participants in the Urinary
Isoflavone Concentration Survey of the Japan Nurses’ Health Study, we analyzed urinary levels of estrone, estradiol and FSH in 547 women aged from 45 to 54 years. Urinary FSH levels varied widely in postmenopausal
women and the pattern of change in urinary FSH levels seems to be similar to that in blood FSH levels in previous studies. There were no significant differences in age, body mass index (BMI), estradiol, estrone and estradiol/
estrone ratio among three groups according to the tertile of FSH. In postmenopausal women, there were significant associations of BMI with levels of estrone and estradiol, but there was no significant association of BMI with
FSH. Studies using urinary samples will allow us to establish a study project as a large-scale population-based
study to determine associations between FSH and various diseases after menopause. J. Med. Invest. 66 : 297-302,
August, 2019
Keywords : Urinary FSH, urinary estrogen, menopause, Japanese women

INTRODUCTION
Estradiol level shows a drastic decrease throughout the menopausal transition and is less than the sensitivity level after
menopause. Follicle-stimulating hormone (FSH), which is necessary for follicular growth initiation and regulation of ovarian
estrogen synthesis, increases in women during the menopausal
transition and postmenopausal period through a feedback mechanism, but the level varies from low to high. Tepper et al. showed
in a longitudinal observation study that the patterns of increasein FSH have three unique trajectories : high rising, medium rising and low rising (1). FSH may play important roles other thanfollicular growth initiation and regulation of ovarian estrogensynthesis. Recently, various studies have shown extragonadal
effects of FSH. A higher FSH level was shown to be associatedwith an increase in frequencies of hot flashes and night sweats(2) and with an increase in subclinical atherosclerosis progression in women at midlife (3). On the other hand, low FSH levels
were shown to be significantly associated with diabetes (4),metabolic syndrome (5) and non-alcoholic fatty liver disease inpostmenopausal women (6).
Although changes in estradiol and FSH and associations ofthese hormonal levels with menopausal symptoms and various
diseases have usually been assessed by using blood samples, it
is easier to collect urinary samples for large population-based
studies. In epidemiological studies, the collection of urinary samples has several advantages compared with blood samples. The
Received for publication April 8, 2019 ; accepted June 24, 2019.
Address correspondence and reprint requests to Toshiyuki Yasui,
Department of Reproductive and Menopausal Medicine, Institute of
Biomedical Sciences, Tokushima University Graduate School, Tokushima, 3-18-15 Kuramoto-cho, Tokushima 770-8503, Japan andFax : +81-88-631-2630.

collection of urinary samples is noninvasive and can be conducted by the subjects without the health professional assistance,
and urinary samples can be easily stored. There were several
studies regarding estrogen and estrogen metabolites by measuring urinary samples (7, 8, 9). However, there have been very few
reports on changes in FSH determined by using urinary samples (10). In addition, it has been suggested that differences inrace and body mass index (BMI) are involved in the differencesin FSH trajectories (1). The variation of FSH levels in Japanesewomen may be different from that in the previous report in theprevious report (1). The change in FSH level and the associationof BMI with FSH during the menopausal transition and postmenopausal period in Japanese women have not been clarified.
We have been conducting a survey of the Japan Nurses’
Health Study (JNHS) since 2001 as a nationwide prospective
cohort study, in which reproductive health-related conditions
have been investigated in female nurses (11). A cross-sectional
baseline survey was conducted from 2001 to 2007. As a projectfor determining the associations between FSH and various diseases, we have planned to measure levels of estrogen and FSH
by using urinary samples in peri- and postmenopausal women.
In the present study, we examined the urinary levels of estradiol,
estrone and FSH in women, associations of estrone and estradiol
with FSH, and associations of BMI with these hormones.

SUBJECTS AND METHODS
Data collection

Of 4472 participants in the Urinary Isoflavone Concentration
Survey of the JNHS in 2015, we identified 1,752 women whoseages ranged from 45 to 54 years. After excluding 92 women who
were receiving hormone therapy, we decided to use data for one
third of the remaining women. Thus, urinary levels of estrone,

The Journal of Medical Investigation Vol. 66 2019

T. Yasui, et al. Urinary FSH in postmenopausal women

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estradiol and FSH in 570 non-hormone users who were randomly selected were measured. The details of the study design for
JNHS were shown previously (11). We asked about menopausal
status, age at the final menstrual period (FMP), cause of menopause (natural menopause, surgical menopause, menopause
secondary to radiation therapy or chemotherapy and other therapies), and past history of unilateral/bilateral oophorectomy andhysterectomy. Women in whom the duration from the FMP wasless than 1 year were defined as premenopausal women, andwomen in whom the duration from the FMP was more than 1
year were defined as postmenopausal women. The Ethics Committee of Gunma University reviewed and approved the study.

Measurements of the concentrations of estradiol, estrone and FSH
in urine
Participants were given urine collection kits and asked to provide early morning urine specimens immediately after waking
up. Urine specimens were basically fasted samples. Participants
collected urine by themselves by using the urine collection kitsin the morning at home and mailed a urinary specimen to ourlaboratory at Gunma University. The urine aliquots were stored
at -70℃ until using in assays. Urinary concentrations of estrone
and estradiol were measured by a radioimmunoassay (12). It
has been reported that urinary estradiol concentrations werecorrelated with serum estradiol concentrations, and urinary
estrone concentrations were also correlated with serum estrone
concentrations (12). Intra-assay and inter-assay coefficients ofvariation ranged from 7.3% to 11.5% and from 6.9% to 10.6%,
respectively, for the estradiol assay, and they ranged from 6.5%
to 9.7% and from 9.6% to 11.6%, respectively, for the estrone
assay. Sensitivities in the estradiol and estrone assays were0.20 and 0.40 ng/ml, respectively. Urinary FSH concentrations
were measured by a chemiluminescence immunoassay. The
concentrations of estradiol, estrone and FSH were adjusted byurinary creatinine. Urinary samples (each 25 μl) were reactedwith mouse anti-FSH monoclonal antibodies, which were immobilized magnetism microparticles (50 μl). After removing
unreacted materials, acridinium-labeled mouse anti-FSH monoclonal antibodies (50 μl) were added. Unreacted materials were
removed and fluorescence intensity at 400-500 nm was mea-

sured after addition of hydrogen peroxide (300 μl). Calibrators
were also reacted by the same methods as that used for urinary
samples, and we obtained values of FSH based on the obtained
standard curve. In a previous study, urinary FSH level was measured by an immunoenzymometric assay (13). The results of achemiluminescence immunoassay correlate well with the resultsof an immunoenzymometric assay.

Data analysis
Of the 570 women, 7 women who had received hysterectomy, one woman who had received bilateral oophorectomy, one
woman with breast-feeding, and 22 women in whom periods
from the FMP were unknown were excluded, and we analyzed
data for 547 women. We compared urinary FSH concentrationsin premenopausal women and postmenopausal women by using
the Mann-Whitney test. We examined differences in age, years
since menopause, BMI, urinary estrone and estradiol levels, andestradiol/estrone ratio between the three groups of urinary FSH
levels by using the Kruskal-Wallis test. Spearman’s correlation
coefficient was used to examine the correlations between estradiol level and estrone level, between BMI and estradiol level, between BMI and estrone level, and between BMI and FSH level.
P < 0.05 was considered statistically significant. All statisticalanalyses were carried out using SAS ver 9.4 (SAS Institute Inc.,
Cary, NC).

RESULTS
Ages, BMIs, levels of estrone, levels of estradiol, estradiol/
estrone ratios and levels of FSH in pre- and postmenopausal
women (< 3 years, 3-5 years and ≥ 6 years) are shown in Table
1. Estradiol levels in postmenopausal women were extremely
low, about 1 ng/mg creatinine. The median (25-75 percentiles)of estrone levels in postmenopausal women was 4.47 (3.37-6.17)
ng/mg creatinine, which was lower than the estrone level in premenopausal women. The median (25-75 percentiles) of estradiol/
estrone ratios in postmenopausal women was 0.27 (0.21-0.36),
which was lower than that in premenopausal women. The median FSH level in postmenopausal women was significantly higher

Table 1. Levels of estrone, estradiol, estradiol/estrone and FSH in pre- and postmenopausal women
Premenopause

Postmenopause< 3 years

3-5 years≥ 6 years

Number

248

154

102

43

Age (years)

48 (46 – 50)

52 (50 – 53)

53 (51 – 54)

53 (52 – 54)

1.8 (1.1 – 2.0)

4.0 (3.0 – 4.5)

8.0 (6.2 – 8.0)

Years sincemenopause (years)
BMI

20.9
(19.6 – 22.9)

21.3(19.6 – 23.6)

21.2(19.5 – 23.2)

21.1(19.5 – 22.4)

Estrone (ng/mg
creatinine)

11.46(5.86 – 20.41)

4.84(3.47 – 6.50)

4.21(3.46 – 6.13)

3.82(3.03 – 4.87)

Estradiol (ng/mg
creatinine)

6.38(3.37 – 10.08)

1.29(0.88 – 1.65)

1.18(0.87 – 1.64)

0.94(0.77 – 1.43)

E2/E1 ratio

0.51(0.37 – 0.64)

0.27(0.21 – 0.36)

0.28(0.22 – 0.36)

0.26(0.20 – 0.32)

FSH (mIU/mg
creatinine)

5.1(2.1 – 13.0)

33.2(11.5 – 64.9)

40.3(12.1 – 67.0)

19.3(7.9 – 53.3)

Values are indicated as medians (25-75%).
E1 : estrone, E2 : estradiol, FSH : follicle-stimulating hormone, BMI : body mass index

299

The Journal of Medical Investigation Vol. 66 August 2019
than that in premenopausal women (p < 0.001). Changes in levels of estradiol, estrone and FSH according to duration since the
FMP are shown in Figure 1. In postmenopausal women, FSH
levels varied widely from 0.2 to 172.8 mIU/mg creatinine, thoughlevels of estrone and estradiol remained low in most postmenopausal women. Estradiol levels showed significant positive correlations with estrone levels in premenopausal women (r = 0.93,
p < 0.01) and postmenopausal women (r = 0.67, p < 0.01).
The correlations between estradiol and FSH and between estrone and FSH in postmenopausal women are shown in Figure
2. There was no significant correlation between estrone andFSH (r = -0.02, p = 0.72) or between estradiol and FSH (r = -0.01,
p = 0.92) in postmenopausal women. FSH levels varied widely
even in postmenopausal women with low estradiol and estrone

levels.
We divided the postmenopausal women into three groups, alow FSH group, a middle FSH group and a high FSH group, according to the tertile of FSH (Table 2). There were no significant
differences in age, years since the FMP, BMI, estradiol level,
estrone level and estradiol/estrone ratio among the three groups
in postmenopausal women.
In postmenopausal women, there were significant associations of BMI with estrone (r = 0.14, p = 0.02) and estradiol(r = 0.19, p < 0.01), but there was no significant association of
BMI with FSH (r = -0.07, p = 0.21) (Figure 3). In premenopausal
women, there was no significant association of BMI with estrone(r = 0.06, p = 0.38), estradiol (r = 0.02, p = 0.77) or FSH (r = -0.08,
p = 0.24).

40

FSH level (mIU/mg creanine)

Estrone level (ng/mg creanine)

Estradiol level (ng/mg creanine)2000Premenopause

Postmenopause

Premenopause

Postmenopause

Premenopause

Postmenopause

Figure 1. Urinary levels of estradiol, estrone and FSH in pre- and postmenopausal womenLeft panel : estrone level, Middle panel : estradiol level, Right panel : FSH level

Spearman's correlaoncoefficientr = -0.02, p = 0.72

Spearman's correlaoncoefficientr = -0.01, p = 0.92

Figure 2. Correlations of urinary FSH levels with urinary levels of estradiol and estrone in postmenopausal womenLeft panel : correlation of FSH with estrone, Right panel : correlation of FSH with estradiol

T. Yasui, et al. Urinary FSH in postmenopausal women

300

Table 2. Estrone, estradiol and estradiol/estrone ratio according to tertile of FSH levels in postmenopausal women

Low FSH group(< 16.0)n = 99Middle FSH group(16.0-53.9)
n = 103

High FSH group(≥ 54.0)n = 97p value*Age (years)

52 (51 – 53)

52 (51 – 54)

53 (51 – 54)

0.27

Years sincemenopause (years)

3.0 (2.0 – 5.0)

2.5 (1.4 – 4.0)

2.5 (1.7 – 4.0)

0.13

BMI

21.2 (19.6 – 23.2)

21.0 (19.6 – 24.1)

21.2 (19.2 – 22.9)

0.51

Estrone (ng/mg
creatinine)4.55 (3.33 – 6.17)

4.31 (3.39 – 6.25)

4.47 (3.37 – 6.14)

0.72

Estradiol (ng/mg
creatinine)

1.20 (0.81 – 1.70)

1.20 (0.87 – 1.59)

1.20 (0.88 – 1.59)

0.98

E2/E1 ratio

0.27 (0.20 – 0.37)

0.27 (0.22 – 0.36)

0.27 (0.21 – 0.34)

0.78

FSH (mIU/mg
creatinine)

6.7 (3.2 – 11.2)

32.9 (25.2 – 42.5)

84.7 (66.7 – 105.0)

Values are indicated as medians (25-75%).
E1 : estrone, E2 : estradiol, FSH : follicle-stimulating hormone, BMI : body mass index*Kruskal-Wallis test

BMI (kg/m2)

BMI (kg/m2)

Spearman's
correla on
coefficientr = -0.07, p = 0.21

BMI (kg/m2)

Spearman's
correla on
coefficientr = 0.19, p < 0.01

Spearman's
correla on
coefficientr = 0.14, p = 0.02

Figure 3. Correlations of urinary levels of estrone, estradiol and FSH with BMI in postmenopausal womenLeft panel : correlation of estrone with BMI, Middle panel : correlation of estradiol with BMI
Right panel : correlation of FSH with BMIDISCUSSION
In the present study, we showed that urinary FSH levels inJapanese postmenopausal women varied widely as was shownfor blood FSH levels in previous studies, though estradiol levels
were lower than the sensitivity level. There have been very few
studies in which urinary FSH levels in postmenopausal women
were used for research. It has been suggested that urine collection might be preferable in large population-based surveys
which study participation rates have been reduced by therequirement of a blood draw (7). It has been reported that measurements using urinary samples were effective and efficientin a population-level study (10) based on the validations andstability of FSH measurement in urine (13).
Randolph et al. reported that increase in FSH from 8 years
before the FMP to 8 years after the FMP could be divided into 5
segments : no change, a gradual increase, a marked increase, aslower increase and stabilization (14). Sowers et al. reported that
FSH level had an acute increase from 2 years before the FMP to
one year after the FMP and showed a plateau thereafter (15). In
the present study, we showed that urinary FSH levels increased
until about 3-5 years after the FMP and that FSH levels inwomen whose years after the FMP was more than 6 years werelower than those in women whose years after the FMP were

The Journal of Medical Investigation Vol. 66 August 2019less than 6 years. The pattern of changes in urinary FSH levels
seems to be similar with the pattern of changes in FSH levels inblood samples. Tepper et al. reported that the variation in FSH
trajectories was evident after the FMP and that the FSH levels
varied widely from about 25 to 120 mIU/ml (1). In the present
study, urinary FSH levels also varied widely from 0.2 to 172.8
mIU/mg creatinine.
Estradiol secretion shifts from the ovary to a compensatory
source in fat in postmenopausal women (16). Even if estradiol
level is less than the sensitivity level, estrogenic activity may
be high in women with high BMI. Obese women tend to have ahigher estrone level, lower sex hormone-binding globulin level
and higher free estradiol level (5). A more significant correlation between estrone and BMI than that between estradiol and
BMI has been found (17). In the present study, the proportionof women whose BMI was more than 25 was only 11.4% andthere were significant associations of BMI with urinary levelsof estrone and estradiol even in these women. However, we did
not find a significant association between FSH level and BMI
in postmenopausal women, although urinary FSH levels also
varied widely. Tepper et al. reported that BMI affected the trajectory of FSH changes over the menopausal transition (1). It has
been reported that the change in FSH levels was markedly lesspronounced in obese women than in non-obese women (14). Also,
it has been reported that weight loss led to an increase in FSH
level in overweight postmenopausal women (18). A possible reason for the difference in the results between our study and previous studies is due to difference in BMIs in the subjects. In thoseprevious studies, the proportion of women with high BMI waslarge. In the SWAN study, the proportions of women in whom
BMI ranged from 25 to 29.9 and women in whom BMI was morethan 30 were 25.3% and 32.1%, respectively (1). Randolph et al.
reported that a difference in FSH levels was found in womenwith BMI between less than 30 and more than 30 (14). Estrone
and estradiol may be very sensitive to only a small amount of
adipose tissue in women with normal BMI, but FSH may not besensitive to a small amount of adipose tissue. Another reason isdue to the difference in the measurement between blood samples
and urinary samples.
In the present study, FSH levels varied from low to high and
FSH levels according to tertile were not associated with levels of
estrone and estradiol in postmenopausal women. Low FSH levels were shown to be associated with risk of prevalent prediabetes and diabetes (4), metabolic syndrome (5), non-alcoholic fatty
liver disease (6) and 10-year atherosclerotic cardiovascular diseases in postmenopausal women (19). The associations of FSH
with these diseases may be involved in BMI. On the other hand,
it has been reported that a higher level of FSH was associatedwith an increase in subclinical atherosclerosis progression in
women at midlife (3), and women in high and medium FSH trajectory groups had significantly larger intima-media thickness(20). In addition, Randolph et al. suggested that FSH levels may
be predictive of the frequency of hot flashes in women experiencing vasomotor symptoms (2). A longitudinal study suggested
that women with higher BMI have a higher risk of vasomotor
symptoms (21). Based on the associations of high FSH with these
diseases, the variation of FSH after menopause may be involvedin not only BMI but also other factors.
An increase in FSH levels may not indicate only the response
to a decrease in estrogen in the pituitary, and FSH may havean independent role. There have been studies on the role of FSH
in extragonadal tissues. At first, FSH was reported to havenon-gonadal effects such as direct regulation of bone mass (22).
It has also been shown that FSH receptors are expressed in theliver (23), adipose tissue (24) and blood vessels (25), providing
the basis for the extrareproductive function of FSH. Recently,

301

the ratio of FSH to estradiol has been used to screen for theoccurrence of mild cognitive function in postmenopausal women(26). Extragonadal effects of FSH should be further examined ina large epidemiological study.
We found that urinary FSH levels in postmenopausal womenvaried widely as do levels in serum FSH samples. Also, thechanges in and the pattern of changes in urinary FSH levels
were similar to those in serum FSH levels. Based on the results,
it is possible to examine the associations between the occurrenceof various diseases and urinary FSH levels. It is easier to collecturine samples for large population-based epidemiological studies, and results of studies using urinary samples may contributeto elucidation of the roles of FSH.
A limitation of this study is the use of spot urine samples forhormonal measurements rather than samples of total urine output over 24 hours, although morning first-void urine was used
to obtain concentrated urine. The period of urinary collection in
all premenopausal women could not be fixed at 1 to 10 days of
menstruation. Since the design of the study was cross-sectional,
investigation of longitudinal changes in urinary hormonal levels
may be needed.
In conclusion, we showed that urinary FSH levels in Japanesewomen varied widely. Studies using urinary samples will allow
us to establish a study project as a large population study todetermine associations between FSH and various diseases after
menopause.

DISCLOSURE STATEMENT
The authors declare that there is no conflict of interest for thiswork.

FUNDING
This study was partly supported by grants from the project for
Whole Implementation to Support and Ensure Female Life of theJapan Agency for Medical Research and Development (AMED).

ACKNOWLEDGEMENTS
The authors appreciate the cooperation of all of the nurses who
participated in the Urinary Concentration Survey of the Japan
Nurses’ Health Study. We also appreciate the assistance of Ms.
Satomi Shimizu and Ms. Naho Maruoka in specimen and data
management.

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