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Ultrasound Obstet Gynecol 2008; 31: 210–217
Published online 15 January 2008 in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/uog.5241
Correspondence to: Prof. L. Valentin, Department of Obstetrics and Gynecology, Malmö University Hospital, SE 205 02 Malmö, Sweden
(e-mail: lil.valentin@obst.mas.lu.se)
Accepted: 4 October 2007
Copyright 2008 ISUOG. Published by John Wiley & Sons, Ltd. ORIGINAL PAPER
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The menopausal transition 211
contacted by telephone and asked if they would agree venous blood sample was drawn. The blood samples were
to participate. The inclusion criteria were: fairly regular immediately centrifuged at 3000 g for 10 min. Serum was
vaginal bleeding, no estrogen or gestagen treatment, then separated, frozen and stored at −30◦ C until analyzed
no intrauterine contraceptive device, no known uterine after the conclusion of the study. Follicle-stimulating
myomas, not having undergone treatment for invasive hormone (FSH) and progesterone were analyzed using the
TM
gynecological cancer, hysterectomy or bilateral salpingo- Access (R) Immunoassay System on a UniCel DxI 800
oophorectomy. Forty women were recruited. All denied from Beckman Coulter (Chaska, MI, USA). Progesterone
having any gynecological problems or known uterine or was analyzed in blood samples taken when the ultrasound
ovarian anomalies. image was clearly compatible or possibly compatible with
The women underwent ultrasound examination by the the presence of a corpus luteum. Progesterone levels
second author (L.V.), who had had more than 10 years’ ≥ 10 nmol/L were taken to indicate that ovulation had
experience in gynecological ultrasonography at the start occurred15 . FSH was analyzed in blood samples taken
of the study. They were examined every 3 months on any at 3 and 6 months after the last vaginal bleeding, values
‘cycle day’ until 12 months had elapsed since their last ≥ 17 IU/L indicating postmenopausal status according to
vaginal bleeding, then every 6 months until the conclusion the reference values of our laboratory.
of the study. The study was completed after 6 years All the women noted their vaginal bleedings on
when 20 women had been examined from approximately a dedicated form during the whole study period.
2 years pre- to approximately 2 years postmenopause. Retrospectively, they were classified as being in early
All the sonograms were performed transvaginally in the or late menopausal transition using the STRAW criteria7 ,
lithotomy position with an empty bladder. The examina- according to which, during early menopausal transition,
tions included measurements of uterine anteroposterior menstrual cycles remain regular but with duration
diameter and width, endometrial thickness, length (L), changed by 7 days or more. Two or more skipped
depth (D), and width (W) of both ovaries (three orthog- menstrual cycles and at least one intermenstrual interval
onal diameters), and of the largest follicle-like cystic of ≥ 60 days are characteristic of the late menopausal
structure or corpus luteum in each ovary and of any transition. Women who did not have any vaginal bleeding
adnexal lesion (three orthogonal diameters). The ovar- for 12 months were considered to be postmenopausal,
ian volume in mL was calculated using the formula provided that their serum FSH was ≥ 17 IU/L in blood
V = L × D × W/2. All intraovarian cystic structures with samples taken 3 and 6 months after their last vaginal
ultrasound morphology compatible with a follicle and bleed.
with a diameter (mean of three orthogonal diameters) of The pattern of change over time for each ultrasound
3 to 40 mm were counted as follicles, no distinction being variable studied was described separately for each woman
made between follicles and ‘functional cysts’. Cystic struc- by inspection of plots of results against time. The
tures with a mean diameter ≤ 2 mm were not taken into percentage change over time in measured variables was
account. A corpus luteum was determined to be present if calculated as (1 − the value at time B/the value at time A)
an intraovarian structure with the typical gray-scale ultra- ×100, where time A precedes time B. Depending on the
sound morphology of a corpus luteum and surrounded distribution of the percentage change, results are presented
by a typical ‘color ring’ at color Doppler examination as mean or median percentage change.
was seen10 – 13 . The anteroposterior diameter of the uterus Statistical analyses were carried out using the Statview
TM
was measured on a sagittal view of the uterus where it 4.5 statistical program (Abacus Concepts, Inc., Berke-
appeared to be at its thickest, and the width of the uterus ley, CA, USA, 1992–1995). Because our data mani-
was measured on a transverse view of the uterus where fested a skewed distribution, the statistical test used was
it appeared to be at its widest. Endometrial thickness Wilcoxon’s test for paired data. A two-tailed P-value
was measured as described earlier using the double-layer < 0.05 was considered statistically significant.
technique14 . One measurement of each distance was taken The ethics committee of the Medical Faculty of Lund
using calipers on the frozen ultrasound image. The fol- University, Sweden, approved the study and written
lowing were also noted: the ultrasound morphology of the consent was obtained from all the participants.
endometrium (midline echo, triple layer, hyperechogenic,
cystic) the number of follicle-like cystic structures and
RESULTS
corpora lutea, and the presence, location, size, and mor-
phology of any uterine or adnexal lesions. All ultrasound Of the 40 women who entered the study eight withdrew
examinations were documented on hard copies. for unknown reasons and 12 women were excluded for the
The ultrasound examinations were performed using an following reasons: one woman had a gestagen intrauterine
Acuson 128XP ultrasound system (Acuson Inc., Mountain device inserted during the study period, three women
View, CA, USA) with a 4–7.5-MHz transvaginal started hormone replacement therapy, six women still
transducer. Doppler ultrasound, both in color and spectral had fairly regular vaginal bleedings at the conclusion of
modes, was performed at a frequency of 5 MHz. the study, and two women underwent only one or two
At each ultrasound examination the women were asked examinations before menopause.
about any medication and about menopausal symptoms Twenty women were included in the study. All were
(hot flashes, palpitations, etc.) and other symptoms, and a white Scandinavian, all were 50 years old when they
Copyright 2008 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2008; 31: 210–217.
14690705, 2008, 2, Downloaded from https://obgyn.onlinelibrary.wiley.com/doi/10.1002/uog.5241 by Indian Council of Medical Research, Wiley Online Library on [12/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
212 Sokalska and Valentin
entered the study and none had a history compatible Table 1 Individual patterns of change for ultrasound variables
with polycystic ovary syndrome. Three women were
nulliparous, all three being voluntarily childless, the Decrease Increase No clear
remaining 17 had delivered one, two or three babies. Parameter (n (%)) (n (%)) change (n (%))
Five women were on medication(s) throughout the study
Uterine width 19 (95) 0 1 (5)*
period, and all except three were on medication(s) for
Uterine AP diameter 20 (100) 0 0
some time during the study period (e.g. antihypertensive Endometrial thickness 16 (80) 0 4 (20)
or anti-arrhythmic drugs, antihistamines, psychotropic Volume of largest ovary 14 (70) 1 (5) 5 (25)
drugs, and/or immunosuppressants, the latter given Total number of follicles 17 (85) 0 3 (15)
against rheumatoid arthritis). (right and left ovaries)
Despite all subjects denying having uterine or ovarian
*This woman had six myomas. AP, anteroposterior.
disorders, 12 (60%) were found to have uterine fibroids
at ultrasound examination, eight having one fibroid
< 20 mm in diameter, and four having 2–8 fibroids significantly before menopause. However, the volume of
ranging from 10 to 65 mm in diameter. One woman the largest ovary was smaller 24 months after menopause
had ultrasound findings compatible with adenomyosis, than at menopause (P = 0.05) or 24 months before
and in two women one or more 15–20-mm extraovarian menopause (P = 0.05). The median volume of the largest
cysts were seen. No other gynecological abnormalities ovary 24 months before menopause was 6.3 (range,
were detected. 2.0–15.7) mL vs. 3.4 (range, 1.3–10.8) mL 24 months
For 18 of the 20 women the period of observa- after the menopause. Median changes in left and right
tion before menopause was at least 24 months (up to ovarian volume from 24 months before to 24 months after
54 months). One woman was examined from 15 months the menopause were a 45% decrease (P = 0.075) and a
before to 24 months after menopause, one from 20% decrease (P = 0.056), respectively. The diameter of
21 months before to 24 months after menopause, one the largest intraovarian follicle-like cystic structure was
from 54 months before to 18 months after menopause, similar until menopause, median diameter at 24 months
and the remaining 17 women from 24 to 51 months before menopause being 14 mm, at 12 months before
before to 24 months after menopause. Only the results menopause 15 mm, and at menopause 16 mm.
from 24 months before to 24 months after menopause Changes in the total number of follicle-like cystic
are presented. structures/corpora lutea are illustrated in Figure 2b. The
According to the STRAW criteria7 , seven women total number at 24 months before menopause did not
passed from early to late menopausal transition during differ significantly from that at menopause but was
the 24 months preceding menopause, while 13 women significantly lower 12 and 24 months after menopause
were in late menopausal transition during the whole than at menopause. The number at 24 months before
24 months’ study period preceding menopause. Mean menopause varied from 0 to 5, at the time of menopause
age at menopause was 52.8 ± 1.01 (SD) years. In all from 0 to 7 and at 1 and 2 years after menopause from
women FSH levels at 3 and 6 months after the last menses 0 to 4 and from 0 to 2, respectively. Cystic intraovarian
confirmed that the last bleed was indeed the menopause, structures were observed in the postmenopausal period in
FSH levels ranging from 38 to 148 IU/L. 14 women; in ten women they were seen only in the first
Inspection of individual plots of results against time postmenopausal year (size ≥ 11 mm in six women), in four
revealed that for each measured ultrasound variable there women they were also seen in the second postmenopausal
were three individual patterns of change: decrease over year (size ≥ 11 mm in three women).
time; increase over time; or no clear change over time. The A summary of all the ultrasound findings is presented
individual patterns of change for the variables studied are in Table 2, while Table 3 shows the number of women
summarized in Table 1. In most of the women, uterine with antral follicles, corpora lutea, or follicles > 11 mm in
and ovarian size, endometrial thickness and total number diameter and a triple-layer endometrium in relation to the
of intraovarian follicle-like cystic structures (i.e. the sum time pre- or postmenopause. Ultrasound findings compat-
of the number in the right and left ovary) decreased during ible with the late follicular phase (follicle ≥ 11 mm and
the study period, but a substantial decrease did not occur triple-layer endometrium) could be found on virtually any
until after the menopause. cycle day. During the 24 months preceding menopause,
Changes in uterine size and endometrial thickness the most common ultrasound finding was that of ovaries
during the 4-year study period are illustrated in Figure 1. containing either a few cystic structures with at least one
The decrease in uterine size and endometrial thickness measuring ≥ 11 mm, or no follicle-like structures, and
between 24 months before and 24 months after the simultaneously a slightly hyperechogenic endometrium of
menopause was statistically significant, the mean change varying thickness but not manifesting any midline echo or
in uterine anteroposterior diameter being a 22% decrease triple-layer appearance. There was no obvious relation-
and in uterine width a 19% decrease. The median ship between the number or size of follicle-like cystic struc-
change in endometrial thickness was a 28% decrease. tures seen in the ovaries and the presence of a triple-layer
Changes in the size of the largest ovary are illustrated in endometrium, but when a triple-layer endometrium was
Figure 2a. The volume of the largest ovary did not change seen, at least one follicle-like cystic structure ≥ 7 mm was
Copyright 2008 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2008; 31: 210–217.
14690705, 2008, 2, Downloaded from https://obgyn.onlinelibrary.wiley.com/doi/10.1002/uog.5241 by Indian Council of Medical Research, Wiley Online Library on [12/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
The menopausal transition 213
P = 0.0004 P = 0.001
(b)
(a) 8 P = 0.0218 P = 0.0006
8
7
Uterine AP diameter (cm)
6
5
5
4
4
3
(n = 18) (n = 20) (n = 19) (n = 20) (n = 19)
(n = 18) (n = 20) (n = 19) (n = 20) (n = 19)
0 0
−24 −12 MP +12 +24 −24 −12 MP +12 +24
23 (6−179) 54 (3−121) 44 (5−209) 23 (6−179) 54 (3−121) 44 (5−209)
Cycle day (median (range))
Cycle day (median (range))
Copyright 2008 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2008; 31: 210–217.
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214 Sokalska and Valentin
Copyright 2008 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2008; 31: 210–217.
14690705, 2008, 2, Downloaded from https://obgyn.onlinelibrary.wiley.com/doi/10.1002/uog.5241 by Indian Council of Medical Research, Wiley Online Library on [12/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
The menopausal transition 215
Table 2 Ultrasound findings at examinations performed longitudinally from 2 years before to 2 years after menopause (MP)
−24 to −12 months* −9 months to MP† +3 to +12 months‡ +18 to +24 months§
Examinations with: (n = 83) (n = 67) (n = 76) (n = 39)
*Examinations performed from 24 to 12 months before MP. †Examinations performed from 9 months before MP to MP. ‡Examinations
performed from 3 to 12 months after MP. §Examinations performed from 18 to 24 months after MP. ¶Confirmed by a progesterone value
≥ 10 (range, 10.5–34) nmol/L. N/A, not applicable.
Table 3 Number of women with intraovarian follicle-like structures or corpora lutea in relation to menopause (MP)
the age of 50 years. The reason why we chose to start compatible with a particular phase of the menstrual cycle
scanning the women at this relatively advanced age was irrespective of the ‘cycle day’ on which the examination
that we hoped that all would be close to menopause at was performed; ultrasound findings compatible with the
the start of the study. late follicular phase were encountered on any ‘cycle day’;
The fact that all the women were in menopausal and ultrasound findings compatible with the luteal phase
transition during the 2 years preceding menopause as late as on ‘cycle day’ 56.
explains why it was not possible to perform all A methodological difficulty is how to discriminate
examinations on a predefined cycle day during this between a follicle, a functional cyst, an inclusion cyst,
period – for example, a few days after the start of a and a small neoplastic cyst. This is particularly difficult in
vaginal bleed. Had we performed all examinations a few the menopausal transition, when women no longer have
days after the start of a vaginal bleed, it would not have cycles but bleed irregularly and often very infrequently.
been possible to keep the ‘every-3-months schedule’ that Because of the uncertainty regarding the origin of intra-
was necessary to relate the examinations to time before ovarian cystic structures we chose to call all intraovarian
menopause with reasonable precision. The fact that our cystic structures 3–40 mm in diameter ‘follicle-like cystic
examinations were carried out on any ‘cycle day’ may structures’. Before the menopause, most of these cystic
have affected our results with regard to ovarian size and structures were probably follicles, but some may have
morphology and to a lesser extent those regarding uterine been functional cysts (none of the cystic structures of
size and endometrial thickness and morphology. We are 30–40 mm persisted), inclusion cysts or even neoplas-
not convinced, however, that this is the case, because, tic cysts.
during menopausal transition, many bleedings are almost The menopausal transition period is characterized
certainly anovulatory15,19 and ‘cycle day’ is not a reliable by significant hormonal fluctuations, and results of
marker of the menstrual phase or hormonal status. Our single hormonal measurements (estradiol, estrone, FSH,
results support this; most ultrasound findings were not leutinizing hormone or inhibin) during this period do not
Copyright 2008 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2008; 31: 210–217.
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216 Sokalska and Valentin
provide reliable information on menopausal status30,31 . 10. Jokubkiene L, Sladkevicius P, Rovas L, Valentin L. Assessment
of changes in volume and vascularity of the ovaries during the
Anti-Müllerian hormone, on the other hand, seems
normal menstrual cycle using three-dimensional power Doppler
to reflect the ‘ovarian reserve’ well32 . The hormonal ultrasound. Hum Reprod 2006; 21: 2661–2668.
fluctuations in the menopausal transition are secondary 11. Baerwald AR, Adams GP, Pierson RA. Form and function of the
to structural changes in the ovaries (ovarian volume, corpus luteum during the human menstrual cycle. Ultrasound
number of antral follicles)33 and possibly to changes Obstet Gynecol 2005; 25: 498–507.
12. Sladkevicius P, Valentin L, Marsal K. Blood flow velocity in the
in ovarian vascularization34 . These changes can be
uterine and ovarian arteries during menstruation. Ultrasound
studied non-invasively using ultrasonography. Today, a Obstet Gynecol 1994; 4: 421–427.
transvaginal ultrasound examination is often included in 13. Sladkevicius P, Valentin L, Marsal K. Blood flow velocity in the
a gynecological consultation. By supplementing clinical uterine and ovarian arteries during the normal menstrual cycle.
information with transvaginal ultrasound examination Ultrasound Obstet Gynecol 1993; 3: 199–208.
14. Sladkevicius P, Valentin L, Marsal K. Endometrial thickness
a quick and cheap answer as to whether a woman
and Doppler velocimetry of the uterine arteries as discriminators
is likely to be in the menopausal transition can be of endometrial status in women with postmenopausal bleeding:
obtained. The finding on any ‘cycle day’ of small a comparative study. Am J Obstet Gynecol 1994; 171:
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This study was supported by the Swedish Medi- 123–131.
17. Broekmans FJ, Faddy MJ, Scheffer G, te Velde ER. Antral
cal Research Council (grants nos. K2001-72X-11605- follicle counts are related to age at natural fertility loss and
06A, K2002-72X-11605-07B, K2004-73X-11605-09A age at menopause. Menopause 2004; 11: 607–614.
and K2006-73X-11605-11-3), two governmental grants 18. Faddy MJ. Follicle dynamics during ovarian ageing. Mol Cell
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and ALF-medel), and Funds administered by Malmö Uni- 19. Landgren BM, Collins A, Csemiczky G, Burger HG, Baksheev L,
Robertson DM. Menopause transition: Annual changes in
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