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Menopausal transition and changes of body composition: a prospective study in Chinese perimenopausal women

Abstract

Objectives:

Whether age or menopause per se influences fat distribution remains controversial. This study aimed to investigate the change of body composition, particularly body fat distribution, in relation to menopausal transition in a 30-month prospective study of perimenopausal women.

Methods:

A total of 438 community-based healthy women aged 44–55 years participated in the Hong Kong Perimenopausal Women Osteoporosis Study. Data were obtained at baseline, and at 9-, 18- and 30-month during the follow-up. Soft tissue measurements consisting of fat mass and lean muscle mass of the trunk and whole body were obtained by the dual energy X-ray absorptiometry. Percentage change of body measurements over the follow-up period was compared between women who remained premenopausal, those who went through menopausal transition, and those who were menopausal since baseline.

Results:

A slight decrease in the lean mass but an increase in the total fat mass and trunk fat mass (TFM) over the follow-up period were noted. Multivariate linear regression analysis showed that age was negatively associated with an increase in central obesity. Adjusted for the important predictors—age, age of menarche and education level, menopausal status was a significant and independent predictor of the decrease in lean mass and the increase in percent of body fat, TFM and trunk–leg fat mass ratio.

Conclusion:

Our 30-month longitudinal study showed that menopause has an independent effect on an increase in fat mass, and an increase in central obesity in perimenopausal Chinese women.

Introduction

Abdominal fat accumulation at the time of menopause has been shown to be associated with metabolic syndrome and increased risks for cardiovascular diseases.1, 2, 3, 4 Studies have noted the adverse changes in body composition and fat distribution, including loss of lean mass,5, 6 increase in fat mass6, 7, 8, 9 and redistribution of fat from periphery to the center7, 8, 9, 10 during midlife.

Menopause signifies a critical endocrine and metabolic phase11, 12 but it remains unclear if changes of body composition are related to menopausal transition per se or due to the effects of aging.1, 13, 14, 15 Although some cross-sectional studies have observed greater fat mass and less lean mass in postmenopausal women,6, 7, 9, 10, 16 others have not.14, 17, 18 The findings have been inconsistent even after separating age from menopause.9, 18, 19 Only a few longitudinal studies on changes in body composition during the menopausal transition have been conducted.1, 20, 21, 22 Although the study by Wing et al.1 and the Massachusetts Women’s Health Study20 found no effect of menopausal transition on weight increase in the US midlife women, Lovejoy et al.22 observed weight gain in transitional women over a 4-year follow-up. A recent 6-year study in midlife women observed marked changes in body composition in African-American and Caucasian women transitioning to the menopause; and reported that both chronological age and ovarian age contributed to an increase in fat mass and waist circumference, and a decrease in skeletal muscle mass.23 Differences in study design and characteristics of target populations might explain the inconsistent findings.

The Study of Women’s Health Across the Nation24 has noted differences in body size and reproductive hormones among different ethnic groups with the lowest unadjusted estradiol and sex hormone-binding globulin (SHBG) concentrations among the Chinese Americans. There has yet no published longitudinal data on changes of body composition during menopausal transition in Asian women. Thus, this study aimed to investigate the changes of body composition and body fat distribution in relation to menopause in a 30-month prospective study of perimenopausal Chinese women.

Methods

The study population

Women aged 45–55 years were recruited into the Hong Kong Perimenopausal Women Osteoporosis Study (HKPOST). The source of recruitment was from eligible women identified from a population-based telephone survey on health of midlife women (based on a randomized sample of telephone numbers from residential telephone directory).25 In addition, eligible women registered with the University Family Medicine Clinic were invited to join the study. Women with the use of exogenous estrogens for at least 3 months, use of corticosteroids and other medications known to affect bone; previous history of fracture: oophorectomy, chronic conditions leading to secondary osteoporosis: renal failure, malabsorption disorders, cancer, metabolic bone disease were excluded. Details of the study subject recruitment have previously been reported.26

Written informed consent was obtained from all individuals who agreed to participate. This study has obtained approval from the Chinese University of Hong Kong Faculty of Medicine Ethics Committee. After the baseline study (N=483), subjects were invited to return for follow-up interviews and measurements at 9, 18 and 30 months. The subject numbers at each time point were 340, 297 and 265, respectively.

Data collection

Body composition and fat distribution

Physical measurements were obtained based on standardized protocol. Height was measured without shoes to the nearest cm, weight with only light clothing to the nearest 0.1 kg, waist and hip girth to the nearest mm. Body mass index (BMI) was calculated as weight in kg divided by the square of height in meters. Waist circumference was measured at the level yielding the minimum circumference between the umbilicus and xiphoid process. Hip circumference was measured at the maximum circumference around the buttocks posteriorly and indicated anteriorly by the symphysis pubis.

Body composition measurements were obtained using the dual-energy X-ray absorptiometry (DXA) (Hologic QDR-2000, Waltham, MA, USA) set in array beam mode. The sub-regions of each scan were manually adjusted according to the manufacturer's recommendations. The trunk region was delineated by an upper horizontal border below the chin, with vertical borders lateral to the ribs, and a lower border formed by the oblique lines passing through the hip joints. The leg region was defined as the tissue below the oblique lines passing through the hip joints, thus primarily reflecting the lower body segment region. Fat mass, fat-free mass or lean muscle mass (LM) and percent body fat (fat %) of whole body and by region were analyzed using the system’s software (version 7.20B). The ratio of trunk to leg fat mass was calculated as upper body fat mass/lower body fat mass. The precisions (coefficient of variance) based on 28 subjects after repositioning were 1.87, 1.84, 1.31 and 0.93 for trunk fat mass (TFM), leg fat mass, total fat mass and total LM, respectively.

Menopausal status, sociodemographic factors and other covariates

Information on sociodemographic background, menopausal status, medical and reproductive history (number of pregnancies, age of menarche, age of menopause, use of oral contraceptive), smoking, alcohol use and time spent in various categories of physical activities27, 28 were obtained with standardized questionnaire through face-to-face interview. Women at baseline were classified into pre-, peri- and postmenopausal status according to these criteria: premenopausal (no change in menstruation pattern); perimenopausal (period immediately before the menopause with change in menstrual pattern, irregular cycle (defined as changes in frequency compared with 12 months ago) or cessation of menstrual period for at least 3 months within the past 12 months); and postmenopausal (at least 12 months since the last menses) (WHO, 1981).26, 29 For the 30-month follow-up study, menopausal stage was classified into three categories: premenopausal or postmenopausal if the menstrual status remained in the respective stage throughout the follow-up period; transitional if women had undergone changes in menopausal status or were still in transition (that is, from pre-menopausal to peri- or post, or from peri- to post- or remained as perimenopausal). Sociodemographic background included age (in years), highest education level attained (at least some secondary level versus with or below some primary level), work status (housewife versus working part-time or full-time), occupation (or spouse’s occupation) and marital status (married versus unmarried). Age was based on the reported date of birth at baseline. Self-reported age of menarche and parity were also obtained. Dietary energy and dietary soy protein intakes were estimated based on food frequency questionnaire used in previous studies carried out in Hong Kong.26, 30, 31

Statistical analysis

Continuous variables and categorical variables were compared by t-test and χ2-test between baseline characteristics of women who remained in the study and those lost to follow-up. The comparisons of means between baseline and follow-up were analyzed by paired t-test. The comparisons of means among the three menopausal groups were analyzed using one-way analysis of variance, and test for trend. Repeated measures analysis of variance using the measurements at baseline, 9-, 18- and 30-month were used to determine changes of body composition over time. Multiple regression analysis technique was also applied to determine the effects of menopausal status and other predictors on percentage changes of LM, fat mass, percent body fat, TFM and trunk–leg fat mass ratio (T–LFMR) over the 30-month follow-up. Three dummy variables indicating menopausal status were created (pre- (reference), transitional and postmenopausal), each having 1 or 0. The variables together with the other predictor variables (age, age at menarche, parity, educational level, physical activity (hours per week of moderate and vigorous activities), dietary energy intake, dietary soy protein intake and BMI) were entered into the regression simultaneously. Predictors included were initially based on previous knowledge from literature review. A final model was achieved by manual removal of variables that did not have meaningful or significant influence on the dependent variable. All data were analyzed by using the Statistical Package for Social Sciences, version 13.0 (SPSS, Chicago, IL, USA).

Results

Characteristics of study population

The mean age of the participants (N=438) at baseline was 49.9 years (s.d. 2.7). Overall, 93% were married, 59% were housewives and 56.5% had primary level of education or below. The prevalence of smoking and drinking were relatively low, 3.9 and 3.9%, respectively.

A total of 287 women were retained up to 30-month follow-up. The reasons for lost to follow-up were mainly ‘too busy,’ ‘lost interest in the study’ or had moved and could not be contacted. The baseline characteristics of those retained and lost to follow-up were generally similar (Table 1). The percentages of overweight (BMI 23.0–26.9) or obese (BMI 27.0) were 44.3 and 19.1%, respectively, among those retained with a similar distribution among those lost to follow-up.

Table 1 Baseline characteristics of subjects retained at follow-up and of those lost to follow-up

Sixty percent and 14% of the women were pre- and perimenopausal at baseline. Sixty-nine of the 162 baseline premenopausal women had gone through menopausal transition during the 30-month follow-up. Among the 35 perimenopausal women, 33 had transitioned to postmenopausal stage by 30 months.

Baseline cross-sectional body composition

Figure 1 shows the baseline cross-sectional BMI adjusted data of LM, TFM, leg fat mass and T–LFMR by menopausal status and premenopausal age or years since menopause. The data revealed a lower LM, higher TFM and T–LFMR among transitional and postmenopausal women. The differences of the adjusted mean values between women with menopausal transition and premenopausal were −1.7, 4.8 and 5.3% for LM, TFM and T-LFMR, respectively. The respective values for postmenopausal women were −3.9, 2.6 and 8.1% (Table 2).

Figure 1
figure1

Baseline cross-sectional body composition measurements by age-menopausal status, adjusted for body mass index (kg m−2).

Table 2 Baseline cross-sectional values (mean±s.d.) of body composition measurements

Changes of body composition over follow-up

A small and statistically insignificant decrease in height over the 30-month follow-up was noted with a mean change of −0.03% for premenopausal women and −0.08% for transition and postmenopausal women; whereas an insignificant weight gain of 0.9 and 1% increase in BMI was noted in postmenopausal women only (data not shown).

Women who went through menopausal transition had a small but significant percentage loss of LM (P<0.01), whereas postmenopausal women had a 3% increase in fat mass over follow-up (P<0.05) (Table 3). Percent body fat also increased significantly over follow-up (P<0.05) in both the transitional and postmenopausal women. The most noted changes were observed in a 5 and 6% increase in TFM in transitional and postmenopausal women, respectively. Significant increases in T–LFMR over follow-up were noted in all three groups of women, but the increases were more noted in the transitional and postmenopausal women. Repeated measures analysis of variance also showed similar trends with significant time effects for % reduction of LM, % increase in TFM and T–LFMR in all menopausal groups, and increase in FM and % BF in the transitional group.

Table 3 Mean values (±s.d.) and changes of body composition measurements over follow-up period

Multivariate linear regression models (Table 4) revealed that menopausal status remained a significant predictor of follow-up percentage change of LM, BF%, TFM and T–LFMR, even adjusted for the other covariates (baseline measurement, age, educational level, age of menarche, parity, follow-up changes of physical activity, soy protein intake and dietary energy intake). Except for the model for change of LM, parity, change of physical activity, soy protein intake and dietary energy intake were removed from the final models, as they had little contribution to the dependent variables. Similar results were observed with BMI (as continuous data) included in the multivariate model (data not shown).

Table 4 Multiple regression analysis on association between menopausal status and changes of body composition (from baseline to the 30-month follow-up)

Age was negatively associated with percentage changes of TFM and T–LFMR. Age of menarche was positively associated with percentage changes of BF and TFM. Increase in physical activities and dietary soy protein intake had a positive effect on change of LM. Change of LM over follow-up was negatively associated with change of BF% and T–LFMR.

Discussion

In this study of the influence of menopausal status and transition on body composition, we observed a trend in the decrease of LM, and an increase in the %BF, TFM and T–LFMR in the cohort, but the changes were more pronounced among postmenopausal women and those undergoing menopausal transition. Menopausal status remained a significant predictor of these changes in body composition even taking into account other predictors such as age, education level, age of menarche and change in LM over follow-up.

Our findings on changes of body fat in perimenopausal women are consistent with several previous cross-sectional6, 10, 16, 19 and cohort22 studies, but not with some other studies.7, 13 Our longitudinal data revealed that after adjusting for the other predictors, age was not associated with change of LM, and was negatively associated with percentage changes of TFM and T–LFMR. Our data were consistent with some previous evidence that LM decreases6 while total and central body fatness increase with menopausal transition. A cross-sectional study which included the Chinese ethnic group also revealed a lower LM in perimenopausal and postmenopausal women.6 A recent study with annual measurements of body composition for 4 years in 156 US women aged 43 years and above22 suggested that menopause per se was associated with an increase in total body fat and visceral fat. Other longitudinal studies also showed similar results.9, 12 In contrast, Pansini et al.13 showed in a cross-sectional study that age was the main determinant of fat mass increase in the upper body (trunk and arms) in postmenopausal women. Another cross-sectional study15 in Chinese women indicated an age-related increase in abdominal fat, but this study did not consider the effect of menopausal status.

Our study used the DXA to estimate total and regional body composition. Hydrodensitometry has been considered the reference method for assessing body composition, but its administration is rather cumbersome for use in large-scale population-based studies. DXA is a relatively new technique for estimating total and regional body composition based on the differential attenuation by the body of photons at two energy levels.32, 33 It has the ability to show the regional distribution of body fat and provides good precision for body composition measurements. However, despite strong correlations found with measurements from hydrodensity, some significantly different findings have also been noted.34 The measurement results may also differ among different DXA models, modes of data collection and softwares used for data analysis.34 However, our use of the same DXA machine and method throughout this 30-month longitudinal study helped to minimize these potential sources of inaccuracies. Several investigators using this technique to assess menopause-related changes in body fat distribution6, 16, 23 also showed an independent effect of menopause on change in body fat distribution and an increase in central obesity.

Age at menarche was closely related to the hormonal milieu of the body, which in turn might influence the development of fat mass and its distribution in later years. Our data revealed that later age at menarche was independently related to an increase in body fat and trunk fat over follow-up. The finding was consistent with the results of a cross-sectional study conducted among 44 487 pre- and postmenopausal women aged 40–65 years,17 but contradictory to some other cross-sectional35, 36 and longitudinal21 studies. Therefore, the influence of age at menarche on body fat distribution at menopause still remained controversial.

Some studies17, 21 found a significant association between parity and adiposity in midlife women. Parity was weakly associated with waist-to-hip ratio in the cross-sectional study conducted by Troisi et al.17 Parity was also found to be a reproductive factor most associated with gradual changes in body fat distribution in a longitudinal study of 1462 randomly selected middle-aged women.21 However, our data did not show a significant influence of parity on menopausal changes in fat distribution.

Sex hormones have been suggested to have a central role in menopause-associated changes in body fatness and body fat distribution. Estrogen levels decline progressively with the menopausal transition, whereas the ovary continues to secrete small amounts of androgens.12 Adrenal androgens such as dehydroepiandrostenedion (DHEA) and DHEA sulfate, which can be converted to estrogens in peripheral tissues, remain as the major source of estrogen in postmenopausal women.2, 37 A number of studies suggested that menopause-induced hormonal changes may contribute to central body fat distribution. Increased free testosterone levels and lower SHBG in premenopausal and postmenopausal women were associated with both overall adiposity and upper body adiposity.28, 38, 39, 40 Some observational studies and clinical trials have reported the association of use of hormonal therapy with lower waist-to-hip ratio or central body fat distribution.5, 17, 38, 41, 42, 43, 44, 45 Changes in body fat distribution during menopausal transition could thus be related to the dynamics of estrogens, SHBG or the relative androgenicity, which are modified by the menopause transition.8, 46 The SWAN study has noted a lower estrodiol and SHBG concentration in Chinese-American women who also had comparatively lower mean BMI values.23 Regional changes in adipose tissue accumulation may also be explained by a lower lipoprotein lipase activity, lipoloytic responsiveness, and the sensitivity of femoral and abdominal adipocytes and subsequently increased abdominal fat deposits during transitional and postmenopausal stages.47, 48, 49, 50

Reduction in energy expenditure and resting metabolic rate with age and menopausal transition might also partly explain the decrease in LM, increase in fat mass and preferential abdominal fat accumulation.6, 22 Kanaley et al.51 reported that physical activity was a stronger predictor than age and menopausal status on the variability of abdominal fat in premenopausal women. In our study, physical activity seemed to exert a protective effect on loss of LM but was not associated with body fat distribution after adjusting for other predictors.

Among the few longitudinal studies,21, 22 Lovejoy et al.22 showed that 24-h and sleeping energy expenditure decreased significantly during the 4-year follow-up period; however, the decrease was greater among women who became postmenopausal compared with the premenopausal controls. Potential mechanisms of the effects of menopause on energy regulation include the possible effects of circulating estrogens and/or androgens on fat-free mass and changes in diet composition in relation to the onset of menopause.22

It is of interest to note that increased dietary soy protein intake had an independent protective effect on the reduction of LM over follow-up. Soy protein intake has been found to be related to a mild favorable effect on bone mass and weight reduction in postmenopausal Chinese women.52, 53 Being a high-quality protein source and containing isoflavones with estrogen-like effect, soy protein might contribute to the preserving effect of LM. More research on this area in perimenopausal women is warranted.

Multiethnic study of perimenopausal women in the United States has revealed smaller body size and lower estradiaol and SHBG levels in Chinese women compared with the Caucasian, Hispanic and African-American counterparts.24 A 6-year longitudinal study in the United States has shown a 1.6% annual increase in fat mass but little change in LM in the African-American and Caucasian cohort aged 42–52 years at baseline, but no report on the Asian-American women has yet been published. This is the first report on longitudinal changes of body composition among Asian perimenopausal women.

There are a few limitations in this study. The analysis is based on post hoc data analyses from a study originally designed to investigate bone changes and osteoporosis in perimenopausal Chinese women.26 The body composition was based on DXA measurements. Although with good precision, its measurement accuracy is still of concern. Moreover, data on the use of herbal supplements have not been collected, although we have excluded women taking medications affecting bone metabolism.

Our study also bears several strengths. First, although a number of previous studies have investigated the changes of body fat distribution in relation to menopausal transition, the age range of study subjects was relatively wide.2, 6, 9, 19, 54 Our study was confined to women aged 45–55 years, and had investigated changes among women within each of the menopausal status during the 30-month follow-up. Second, our study is among the few that have investigated the effect of menopausal transition on changes of fat distribution longitudinally. Third, we used the same DXA machine for the longitudinal body composition measurements and this would minimize the between-machine variations. Fourth, our study took into account age and other potential confounders and observed that menopause status was independently associated with the increase and redistribution of fat mass. Fifth, this study has a reasonable sample size (n=265) of a relatively homogenous group, when compared with other prospective study on this topic. We were able to capture 69% of the baseline premenopausal women undergoing transition during follow-up. Finally, all women in the study population were free from the use of exogenous hormones, so the effect of natural menopause can be more clearly observed.

Conclusion

In conclusion, our longitudinal data confirmed that menopausal transition was associated with an acceleration in the accumulation of abdominal adipose tissue. Compared with women who remained premenopausal, women undergoing menopausal transition and postmenopausal women were characterized by a significant increase in the proportion of android fat and the T–LFMR.

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Ho, S., Wu, S., Chan, S. et al. Menopausal transition and changes of body composition: a prospective study in Chinese perimenopausal women. Int J Obes 34, 1265–1274 (2010). https://doi.org/10.1038/ijo.2010.33

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Keywords

  • menopausal transition
  • body composition
  • body fat
  • trunk fat mass

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