(Circulation. 1996;94:61-66.)
© 1996 American Heart Association, Inc.
Articles |
Effects of Menopause on Trends of Serum Cholesterol, Blood Pressure, and Body Mass Index
From the Department of Clinical Studies, Radiation Effects Research Foundation, Nagasaki (M.A., M.S., K.S.); the Department of Statistics, Radiation Effects Research Foundation, Hiroshima (E.N.); and the Third Department of Internal Medicine, Nagasaki University School of Medicine (S.S., K.Y.), Japan.
Correspondence to Masazumi Akahoshi, MD, PhD, Department of Clinical Studies, Radiation Effects Research Foundation, 8-6 Nakagawa 1-chome, Nagasaki 850, Japan.
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Abstract |
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Background To elucidate the impact of menopause on coronary risk factors, we determined the trends of serum cholesterol (mg/dL), blood pressure (BP, mm Hg), and body mass index (BMI, kg/m2) and investigated whether menopause affects these trends in women in Nagasaki, Japan.
Methods and Results Trends of cholesterol, systolic BP (SBP), and BMI from 9 years before menopause through 9 years after menopause in 579 women with natural menopause (ranging in age from 40.2±3.1 to 57.9±3.1 years; age at menopause, 49.4±3.0 years) and 134 women with surgical menopause (hysterectomy with or without bilateral oophorectomy; ranging in age from 34.9±4.5 to 51.7±5.1 years; age at menopause, 42.9±5.0 years) and those in 579 and 134 age- and time-matched male subjects (ranging in age from 40.1±3.1 to 57.8±3.2 years and from 35.2±4.5 to 51.6±5.0 years, respectively) in Nagasaki were determined by rearrangement of the data from 1958 to 1989 with time of menopause as the datum line. Although cholesterol tended to increase with age in both sexes, it increased significantly in women from 3 years before natural menopause to 1 year after natural menopause and from 1 year before surgical menopause to 1 year after surgical menopause. SBP and BMI did not exhibit a significant increase in relation to natural or surgical menopause. In male subjects, no significant increase of cholesterol, SBP, or BMI was observed at the age corresponding to natural or surgical menopause.
Conclusions Natural menopause and surgical menopause exert an effect only on cholesterol, and an increase in cholesterol precedes natural menopause by 3 years and occurs at the time of surgical menopause.
Key Words: women • cholesterol • blood pressure
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Introduction |
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The incidence of cardiovascular disease and coronary heart disease in women increases after both natural and surgical menopause.1 2 3 4 Many investigators have studied the impact of menopause on coronary risk factors, such as serum cholesterol level, BP, and obesity.5 6 7 8 9 10 11 12 13 14 15 It has been shown consistently that menopause causes an increase in serum cholesterol, but the effects of menopause on BP and body weight remain unclear.5 6 7 8 9 10 11 12 13 14 15
Earlier research was based on cross-sectional studies5 6 7 8 9 10 or comparative cross-sectional studies conducted at intervals of several years to review the intervening changes in coronary risk factors in relation to menopausal status.11 12 13 14 15 Little is known about the trends of coronary risk factors in the perimenopausal period, and the impact of menopause has not been studied by evaluation of its effects on the trends of these coronary risk factors.
In the present prospective population study, we (1) determined the trends of serum cholesterol, BP, and BMI from the premenopausal to postmenopausal state for 18 years in both naturally and surgically menopausal subjects and (2) investigated whether natural or surgical menopause affects the trends of these coronary risk factors to accurately assess the impact of menopause on coronary risk.
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Methods |
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General Procedure
A total of 7564 subjects (3374 men and 4190 women) have received biennial examinations in Nagasaki since 1958 as a part of the follow-up program of the Radiation Effects Research Foundation (formerly the Atomic Bomb Casualty Commission). A detailed description of this program has been published elsewhere (Reference 1616 and Radiation Effects Research Foundation, Research Plan for RERF Adult Health Study, Hiroshima and Nagasaki, RERF Research Protocol 2-75, 1975). At each examination, sitting BP (in mm Hg) was measured by sphygmomanometer on the left arm after a sufficient sedentary period, standing height (in meters) and body weight (in kilograms) were measured without socks or outer clothing, and a fasting blood sample was drawn to measure serum cholesterol (mg/dL) in all subjects. The first Korotkoff phase was used for SBP. BMI (kg/m2) was calculated as body weight divided by the square of standing height. Data from 1958 to 1959 (the first examination) through 1988 to 1989 (the 16th examination) were analyzed in the present study.
Calculation of Age at Menopause
The last menstrual period was recorded for all female
subjects at each examination. When amenorrhea was observed for more
than 12 months, except for pregnancy, the last menstrual period was
defined as the time of menopause. We calculated the age at menopause to
be the difference between the calendar date at menopause and the date
of birth. If the date of the last menstrual period could not be
remembered exactly, we took the stated age at the last menstrual period
and calculated age at menopause as the stated age plus 0.5 year.
Natural Versus Surgical Menopause
Information was also collected on whether menopause occurred
naturally or was surgically induced by hysterectomy but not whether
hysterectomy was accompanied by bilateral oophorectomy. The reasons
for hysterectomy were uterine myomata in 107 cases, uterine cancer in
12 cases, ovarian tumor in 6 cases, other causes in 8 cases,
and an unknown cause in 1 case. During the 30-year period covered by
our study (1958 to 1989), hysterectomy with unilateral oophorectomy
usually was performed in cases of uterine myomata.
Subject Selection
Of the 4190 female subjects, we excluded women who (1) were >53
years old in 1958 (>50 years old in 1955), (2) had already experienced
menopause by 1955, (3) had not experienced menopause as of 1989, or (4)
were not included because of death, migration, or refusal to undergo
examinations. In addition, to ensure the accuracy of the date of the
last menstrual period, subjects who were examined more than 4 years
after the last reported menstrual period (menopause) were excluded. As
a result, only 1501 women were included in subsequent
analyses.
The following standardizing methods were used to clarify the trends of
serum cholesterol, BP, and BMI in relation to menopause.
First, the data on serum cholesterol, BP, and BMI were
rearranged with time of menopause as a new datum line (Fig 1
) and assigned new SECs as follows. Examination cycles
before menopause were referred to as "minus" cycles (the
examination cycle just before menopause is SEC -1, two
examination cycles before menopause is SEC -2, and so on) and
examination cycles after menopause as "plus" cycles (the
examination cycle just after menopause is SEC +1, two examination
cycles after menopause is SEC +2, and so on). Second, since we are
interested in the impact of menopause on trends in coronary
risk factors, analyses were limited to subjects observed at
least two times during the period from SEC -5 to SEC -1 and
from SEC +1 to SEC +5. Therefore, the number of women included in
further analyses was reduced to 1386 (1193 natural menopause
and 193 surgical menopause).
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indicates that
examinations occurred. Blank spaces mean that examinations did not
occur. 
indicates menopause.To show that the impact of menopause on the trends of risk factors, if observed, was not a superficial phenomenon based merely on our selection method or cohort effect, male subjects were selected according to the following process: (1) the women and men were age-matched according to age at the examination cycle just before menopause; (2) the ages of the male subjects were categorized in 5-year intervals (0 to 4, 5 to 9, 10 to 14, and so on) and an age-matched male subject was selected randomly for each female subject; (3) the data for these age-matched male subjects were standardized by rearranging the examination cycles with ages adjusted to SEC -1; and (4) to adjust the selection bias, male subjects who were examined at least two times during the period from SEC -5 to SEC -1 and from SEC +1 to SEC +5 were selected in the same way as female subjects. As a result, 579 and 134 male subjects were selected as controls for naturally and surgically menopausal subjects, respectively. To adjust the time between female and male subjects, the 579 naturally menopausal subjects and 134 surgically menopausal subjects and their corresponding 579 and 134 age-matched male subjects were compared.
Statistical Methods
Levels of serum cholesterol, SBP, and BMI were
compared between adjacent SECs (between SEC -5 and SEC -4,
SEC -4 and SEC -3, and so on) in each naturally and
surgically menopausal woman and her corresponding male subject.
Analyses were conducted by Wilcoxon rank sum test using
the Statistical Analysis System package of programs for
personal computers.17 The data were expressed as mean±SD.
Comparisons were conducted nine times between adjacent SECs from SEC
-5 to SEC +5, and a value of P<.005 (
.05÷9) was
considered significant (Fig 2).
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Results |
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Natural Menopause
Women with natural menopause were followed from the age of 40.2±3.1 years at SEC -5 to 57.9±3.1 years at SEC +5, and their mean age at menopause was 49.4±3.0 years (Table
).
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Although serum cholesterol tended to increase with age in
both sexes, a sharp increase in serum cholesterol in women
was noted when values from SEC -2 to SEC -1 and those from
SEC -1 to SEC +1 were compared (Fig 2
). Serum
cholesterol in men did not exhibit a significant increase
from SEC -2 to SEC -1 or from SEC -1 to SEC +1. An
increase in serum cholesterol in women appeared to start
3 years before the onset of natural menopause.
Natural menopause did not exert a significant effect on the trends of
either SBP or BMI (Fig 3). Neither SBP nor BMI in men
exhibited a significant increase at the age corresponding to natural
menopause.
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Surgical Menopause
Women with surgical menopause were followed from age 34.9±4.5
years at SEC -5 until age 51.7±5.1 years at SEC +5. The mean age
at menopause was 42.9±5.0 years (Table).
Although serum cholesterol tended to increase with age in
both sexes, in women it increased significantly only at the time of
menopause (from SEC -1 to SEC +1) (Fig 4). Serum
cholesterol in men did not exhibit a significant increase
from SEC -1 to SEC +1.
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Surgical menopause did not exert a significant effect on the trends of
SBP or BMI (Fig 5). Neither SBP nor BMI in men exhibited
a significant increase at the age corresponding to surgical
menopause.
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Discussion |
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It has been shown consistently that postmenopausal women have higher serum cholesterol levels than premenopausal women of the same age in cross-sectional studies.5 6 7 8 9 10 In longitudinal studies, the increase in serum cholesterol was greater in women who reached menopause while under study than in women who were still premenopausal at the end of the studies.11 12 13 14 15 The effects of natural or surgical menopause on SBP and BMI remain unclear, but many epidemiological studies have indicated that no significant changes in SBP and BMI are observed in relation to either natural or surgical menopause.6 7 11 12 13 14 15 In this longitudinal study, we showed that although serum cholesterol, SBP, and BMI increased as a result of advancing age, only serum cholesterol exhibited a sharp increase from
3 years before natural menopause until 1 year after
natural menopause and at the time of surgical menopause. Therefore,
both natural and surgical menopause affect only the trend in serum
cholesterol level, which is consistent with results
to date. Because data were collected over a 30-year period from 1958 through 1989, the following might have affected the observed trend of serum cholesterol: (1) Although data adjustment was performed each time, the method for serum cholesterol measurement changed four times during the study period. (2) A "cohort effect" has been observed in Japanese who were born more recently, ie, serum cholesterol measurements are higher despite being taken at the same chronological age as their predecessors.18 The significant increase in serum cholesterol observed in women with natural and surgical menopause might be due to the above factors or to the method of subject selection. Because we performed age matching of female subjects and male subjects using the age at the examination cycle just before menopause and excluded all female subjects without age-matched male subjects, not only the age but also the time was adjusted for the female and male subjects. No significant increase in serum cholesterol was observed in the men at ages corresponding to natural or surgical menopause among the women, indicating that increased serum cholesterol related to natural or surgical menopause is not a coincidental phenomenon.
There have been reports, including the present study, from many countries (Japan,6 the Netherlands,12 Sweden,13 14 and the United States11 15 ) on the fact that natural and surgical menopause exert an effect on serum cholesterol but not on SBP and BMI. Consequently, there is probably no disparity on this point resulting from differences among countries conducting investigations. However, since there are differences in serum cholesterol levels, it is certainly possible that some disparity exists in the extent of the increase in serum cholesterol with menopause among the various countries. In studies conducted in the United States, serum cholesterol is significantly higher in postmenopausal than in premenopausal women in a white population, but the difference is not significant in a black population,19 20 suggesting that race may be a determining factor in the effect of menopause on serum cholesterol. Between Japanese and Caucasian women, however, there is no difference, at least in the fact that menopause exerts an effect on serum cholesterol.
On the basis of their cross-sectional study and comparative cross-sectional study, respectively, Weiss5 and Hjortland et al11 suggest that menopause precedes a rise in serum cholesterol. However, because of the cross-sectional nature of these studies, no definite conclusion can be drawn about the temporal sequence of these events. Jensen et al21 measured serum cholesterol every 3 months from 24 months before menopause to 6 months after menopause in 10 women and stated that serum cholesterol increased steeply within 3 to 6 months after menopause. However, the number of subjects is too small and the duration of follow-up too short to conclude anything about the trend of serum cholesterol in the perimenopausal period.
In the present study, we showed clearly that a significant increase
in serum cholesterol preceded natural menopause by 3
years. It has been reported that estrogen replacement therapy reduces
the relative risk of coronary heart disease22 23
and ameliorates the atherogenic cholesterol
profile24 25 26 27 in postmenopausal women. In addition,
cholesterol is negatively associated with estradiol in
premenopausal and postmenopausal women.8 Thus, it is
speculated that the increase in serum cholesterol
associated with natural or surgical menopause is related to estrogen
deprivation. Several endocrinological studies on the sex
steroid during menopausal transition show that urinary and serum
estradiol concentrations are lower in women approaching menopause than
in younger reproductive-age women,28 29 30
whereas other studies show that serum estradiol concentration does not
decrease in women approaching menopause.31 32 It has been
consistently shown, however, that serum
follicle-stimulating hormone is at higher levels in women
approaching menopause than in younger reproductive-age
women,28 29 31 suggesting that the serum estradiol
concentration is somewhat lower in women approaching menopause and low
enough to stimulate follicle-stimulating hormone. The decrease in
serum estradiol that starts in the mid 30s may reach a threshold level
and thereafter trigger a sharp increase in serum
cholesterol at 3 years before natural menopause.
Chakravarti et al33 reported that, 1 year after menopause,
serum estradiol concentration decreases abruptly to 20% of the
values during the early proliferative phase of the menstrual cycle in
young reproductive-age women. A slow increase in serum
cholesterol probably related to advancing age was observed
1 year after natural menopause when serum estradiol concentration was
considered to reach a minimum. Thus, a sharp increase in serum
cholesterol associated with menopause was observed when
serum estradiol was decreasing abruptly. This suggests that
dynamics (ie, the fact that the serum estrogen concentration is
decreasing) rather than statics (ie, the low level of serum estrogen
concentration per se) plays an important role in the increase in serum
cholesterol related to natural menopause.
Serum cholesterol increased significantly at the time of surgical menopause. In our study, however, this increase could not be definitively attributed simply to estrogen deprivation, because the reason for hysterectomy was uterine myomata in 107 of the 134 women with surgical menopause, and hysterectomy with unilateral oophorectomy was common practice in cases of uterine myomata during the study period. The Framingham Study showed that serum cholesterol increased during the transition from premenopausal to postmenopausal status in women with surgical menopause with bilateral oophorectomy (15 mg/dL, statistically significant) but not in women with surgical menopause without oophorectomy or with unilateral oophorectomy (9 mg/dL, not statistically significant).11 Demirovic et al19 also reported that serum cholesterol in white women who had a hysterectomy but retained at least one ovary was significantly higher than in white premenopausal women. These facts suggest that hysterectomy itself may be associated with an increase in serum cholesterol. Concerning the effects of hysterectomy on ovarian function, it is reported that hysterectomy with bilateral ovarian conservation reduces ovarian function because surgery affects the blood supply to the ovaries.34 35 Cattanach36 also demonstrated that tubal ligation reduced estrogen production. We think, therefore, that the sharp increase in serum cholesterol at the time of surgical menopause among our study participants might be related to the decrease in serum estradiol caused by hysterectomy in uterine myomata and bilateral oophorectomy in uterine cancer and ovarian tumors.
The incidence of coronary heart disease in women increases
after both natural and surgical menopause.1 2 3 4 Among the
coronary risk factors investigated in the present study,
only serum cholesterol showed a significant increase in
relation to natural and surgical menopause. Looking at the temporal
sequence of menopause and the increase in coronary heart
disease incidence and serum cholesterol, the Framingham
Study suggested that the incidence starts to increase before the
complete cessation of menstruation.4 In the present
study, a marked increase in serum cholesterol occurred from
3 years before menopause. Although a definite conclusion cannot be
drawn in the present study because we did not investigate the rate
of cigarette smoking or estrogen supplementation in relation to
menopause, it is likely that the marked increase in serum
cholesterol associated with natural and surgical menopause
is involved to at least some extent in the increase in coronary
heart disease after menopause. It should be noted, however, that the
results of the present study do not negate the role of BP and body
weight in the development of coronary heart disease after
menopause.
Conclusions
Natural and surgical menopause exert an effect on the trend of
serum cholesterol but not on the trends of SBP or BMI. An
increase in serum cholesterol precedes natural menopause by
3 years and occurs at the time of surgical menopause.
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Selected Abbreviations and Acronyms |
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Acknowledgments |
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This publication is based on a manuscript (RP 5-88 and MS 4-95) resulting from research performed at the Radiation Effects Research Foundation (RERF), Hiroshima and Nagasaki, Japan. RERF is a private foundation funded equally by the Japanese Ministry of Health and Welfare and the US Department of Energy through the National Academy of Sciences. The authors thank Shinichiro Ichimaru for data processing and Kaoru Yoshida for preparing the manuscript.
Received May 9, 1995; revision received December 6, 1995; accepted December 10, 1995.
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Z. Fang, S. H. Carlson, Y. F. Chen, S. Oparil, and J. M. Wyss Estrogen depletion induces NaCl-sensitive hypertension in female spontaneously hypertensive rats Am J Physiol Regulatory Integrative Comp Physiol, December 1, 2001; 281(6): R1934 - R1939. [Abstract] [Full Text] [PDF]
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K. Matsuo, M. Akahoshi, E. Nakashima, A. Suyama, S. Seto, M. Hayano, and K. Yano The prevalence, incidence and prognostic value of the Brugada-type electrocardiogram: A population-based study of four decades J. Am. Coll. Cardiol., September 1, 2001; 38(3): 765 - 770. [Abstract] [Full Text] [PDF]
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V. Bittner Estrogens, lipids and cardiovascular disease: no easy answers J. Am. Coll. Cardiol., February 1, 2001; 37(2): 431 - 433. [Full Text] [PDF]
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A.S Fak, M Erenus, H Tezcan, O Caymaz, P AtagunduZ, S Oktay, and A Oktay Effects of simvastatin only or in combination with continuous combined hormone replacement therapy on serum lipid levels in hypercholesterolaemic post-menopausal women Eur. Heart J., February 1, 2000; 21(3): 190 - 197. [Abstract] [PDF]
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E. Sbarouni, Z. S. Kyriakides, and D. T. Kremastinos The effect of hormone replacement therapy alone and in combination with simvastatin on plasma lipids of hypercholesterolemic postmenopausal women with coronary artery disease J. Am. Coll. Cardiol., November 1, 1998; 32(5): 1244 - 1250. [Abstract] [Full Text] [PDF]
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