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Journal of Clinical Endocrinology & Metabolism , doi:10.1210/jc.2007-1040
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The Journal of Clinical Endocrinology & Metabolism Vol. 92, No. 10 3809-3815
Copyright © 2007 by The Endocrine Society

Effects of Weight Control during the Menopausal Transition on Bone Mineral Density

Hyun A. Park, Jung S. Lee, Lewis H. Kuller and Jane A. Cauley

Seoul Paik Hospital (H.A.P.), College of Medicine, University of Inje, Seoul 100-032, Korea; Department of Foods and Nutrition (J.S.L.), University of Georgia, Athens, Georgia 30603; and Department of Epidemiology (L.H.K., J.A.C.), Graduate School of Public Health, University of Pittsburgh, Pittsburgh, Pennsylvania 15261

Address all correspondence to: Jane A. Cauley, Dr.P.H., University of Pittsburgh, Department of Epidemiology, 130 DeSoto Street, A524 Crabtree Hall, Pittsburgh, Pennsylvania 15261. E-mail: jcauley{at}edc.pitt.edu.


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
Background: Studies of weight loss and changes in bone mineral density (BMD) have primarily been short-term trials in obese subjects.

Objective: We examined the effects of a 5-yr intervention designed to prevent menopausal weight gain or promote modest weight loss on BMD in premenopausal women participating in the Women’s Healthy Lifestyle Project.

Design: We enrolled 373 premenopausal women (age 44–50 yr) and randomly assigned them to either lifestyle intervention (175 women, low-fat dietary modification, weight loss, and physical activity intervention) or control group (198 women). BMD and body weight were measured at baseline, annual follow-up visits (18, 30, 42, and 54 months), and two postintervention follow-ups (66 and 78 months). BMD was measured by dual x-ray absorptiometry.

Results: Over the 54 months of intervention, women in the intervention group lost 0.4 kg, whereas control women gained 2.6 kg (P = 0.011). The intervention group experienced significantly greater hip bone loss (–0.20%/yr) than the control group (–0.03%/yr). During the postintervention, differences in rates of bone loss disappeared. When considering both menopausal status and use of hormone therapy (HT), the annualized BMD changes were lower in women reporting HT use; nevertheless, among women on HT, those who lost more than 3% body weight experienced greater total hip BMD loss (–0.25%/yr) compared with those who gained weight (–0.02%/yr) (P = 0.025).

Conclusions: Women randomized to a lifestyle intervention aimed at preventing menopausal weight gain or promoting modest weight loss experienced greater rates of hip bone loss than control women.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
DURING THE MENOPAUSAL transition, women gain an average of 1 pound body weight per year (1), which may contribute to menopause-associated unfavorable changes in lipid profiles (2). Therefore, weight reduction is often encouraged in overweight perimenopausal women, and weight maintenance is recommended in normal-weight perimenopausal women (3). On the other hand, weight change is associated with changes in bone mineral density (BMD) (4, 5). Weight reduction during the menopausal transition may be particularly worrisome because of concurrent menopause-induced bone loss. It is estimated that women annually lose 1.15% of spine BMD and 0.85% of femur neck BMD in the immediate postmenopausal period tapering off to 0.20 and 0.57%, respectively, in the late postmenopausal period (6).

Most studies on the relationship between weight change and BMD change were either short-term intervention trials in obese subjects (7, 8) or longitudinal observational studies of natural weight change in older adults (9, 10, 11). Little is known about the long-term effects of weight maintenance or weight reduction on BMD in healthy premenopausal women while they undergo the menopausal transition.

The Women’s Healthy Lifestyle Project (WHLP) study was a 5-yr lifestyle intervention trial designed to test the hypothesis that an increase in low-density lipoprotein (LDL) cholesterol and weight gain with menopause can be prevented by lifestyle intervention focused on a low-fat diet and exercise intervention. BMD was measured at baseline, at annual follow-up visits during the trial, and at two postintervention period visits. We previously reported greater BMD loss in the intervention group at the 18-month follow-up (12). In the current analysis, we extend these findings and compared annualized rates of BMD change in the intervention and control group at the end of the intervention (54 months) and during a 2-yr observational follow-up (78 months). We also tested the hypothesis that menopausal status and hormone therapy (HT) influence the relationship between weight change and BMD change in women transitioning across menopause.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Study design

Detailed descriptions of this study have been published previously (13, 14). Figure 1Go shows the WHLP study flow. In brief, 535 premenopausal women were recruited from voter registration lists from Allegheny County, Pennsylvania. Eligibility criteria included age 44–50 yr old; premenopausal (<2 months amenorrheic in the past 6 months and not on HT); diastolic blood pressure less than 100 mm Hg, body mass index (BMI) between 20.0 and 33.9 kg/m2; fasting glucose less than 140 mg/dl; LDL cholesterol between 80 and 160 mg/dl; total cholesterol between 160 and 260 mg/dl; not on any lipid-lowering, insulin, thyroid, antihypertensive, or psychotropic medication; not having received any cancer treatment in the past 5 yr; and not having participated in a commercial weight reduction program within the past 4 months.


Figure 1
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  		FIG. 1. The WHLP flow chart.

 
Participants were randomly assigned to either the lifestyle intervention group or control group. Women assigned to the intervention group were given a 5-yr behavioral program aimed at reducing total dietary fat intake to 25% of total energy intake and saturated fat to 7% and increasing weekly physical activity to 1000–1500 kcal by increasing activities such as walking. All participants were given a modest weight loss goal according to their baseline BMI: weight loss of 2.3 kg for women with BMI of 24.44 kg/m2 or less, 4.5 kg for BMI of 24.45–26.44 kg/m2, and 6.8 kg for BMI of 26.45 kg/m2 or more. Women were asked to follow a 1300–1500 kcal meal plan for 4 wk. Subsequently, participants were encouraged to modify the meal plan to include favorite foods while continuing to maintain the study’s dietary goals. The intervention included an intensive group program during the first 6 months and follow-up group sessions by trained interventionists with expertise in nutrition and behavioral intervention. Women in the control group were given general nutritional advice and guidelines on low-fat diet. Both groups were asked to undergo clinic assessments at follow-up visits at 6, 18, 30, 42, and 54 months and two postintervention measurements at 66 and 78 months.

The primary outcomes of the trial were differences in the change of LDL cholesterol and weight between intervention and control groups at the end of the trial (54 months). BMD was a secondary outcome. The protocol was approved by the Institutional Review Board at the University of Pittsburgh.

Weight/height measurement

Weight was measured using a standardized balance beam scale, and height was measured using a stadiometer (Perspective Enterprises Inc., Kalamazoo, MI) while wearing light clothing without shoes. BMI was calculated as the weight in kilograms divided by the square of the height in meters.

Weight change was calculated by subtracting weight at the baseline examination from weight at the 78-month examination and was expressed as a percentage of the baseline value. The percentage weight change over the follow-up period was further categorized into three groups: weight loss greater than 3% (weight loss group), weight loss or gain of no more than 3% (weight stable group), and weight gain greater than 3% (weight gain group), based on the criteria suggested by Stevens et al. (15).

Assessment of menopause/hormone use status

Menstruation and hormone use were assessed at every follow-up clinic assessment using a questionnaire. Menopause was defined as the cessation of menstruation and/or use of HT for 12 months. We classified women as premenopause, postmenopause on HT, and postmenopause not on HT based on their 78-month information.

BMD

The BMD of the lumbar spine (L1–L4), total hip (femoral neck), and whole body were measured by dual x-ray absorptiometry with the array mode (Hologic QDR 2000; Hologic Inc., Bedford, MA) at the baseline and 18-, 30-, 42-, and 54-month clinic visits and at the 66- and 78-month poststudy follow-up visits. A certified technician blinded to the treatment assignment carried out the measures. The scans were analyzed with Hologic software version 7.10 with the compare feature. The study quality control program included daily measurement of an anthropometric spine phantom and weekly measurement of a hip phantom. In addition, the BMD quality control center (University of California, San Francisco, CA) certified all technicians and reviewed a random sample of all scans and all flagged scans. The coefficients of variation for phantoms scanned were 1.5 and 1.3% for the lumbar spine and femoral neck, respectively. The change in BMD was expressed as an annualized percentage of the baseline BMD as percent change in BMD per year.

Other measurements

Dietary calcium intake from foods and supplements was assessed annually using the Block Food Frequency Questionnaire that included 14 foods accounting for more than 95% of calcium intake in the American diet (16, 17). Total calcium intake (milligrams per day) was calculated by summing dietary calcium intake and daily dosage of calcium supplements. A modified Paffenbarger questionnaire was used to estimate weekly physical activity and sport/recreational activity (18). Demographic and other health behavior (smoking and alcohol intake) information were also assessed.

Analytic sample

Because of the significant differences in BMD between Caucasians and African-American women (for all measure sites, P < 0.001) and the small number of African-American participants (43 persons, 8%), we limited our analysis to Caucasian women (n = 492). Of 252 and 240 women in the control and intervention groups, 198 (78.6%) and 175 (72.9%) completed the 78-month follow-up, respectively. No significant differences were found in baseline characteristics between women who did and did not complete the 78-month follow-up, except in the femoral neck BMD (0.816 vs. 0.777 g/cm2) and sports activity (686 vs. 456 kcal/wk), respectively.

Statistical analysis

Student’s t test and Wilcoxon rank sum test were performed to assess differences in continuous measures collected at baseline between control and intervention groups. The {chi}2 test was used for categorical variables. Differences in weight change between control and intervention groups over time were analyzed using repeated-measures ANOVA. Between-group differences at each follow-up point were assessed with the independent-sample t test. To compare differences in annualized BMD change between control and intervention at each of six measurement points, the general linear model was used. Multivariate analysis was used to assess the independent associations among weight change, menopause/hormone use status, and BMD changes over 78 months while controlling for factors associated with weight change and BMD changes in perimenopausal women including baseline age, baseline weight, baseline height, baseline regional BMDs, smoking, and sports activity change. Because there was no significant weight change by intervention group interactions for any of the regional BMDs, the data for control and intervention groups were pooled together in the multivariate analysis. We also examined the interactions between weight change and menopause/HT use in the models to test their modifying effect on BMD change. All statistical analysis was conducted using the SPSS 11.5 statistical packages, and statistical significance was set at P < 0.05. All P values were two tailed.


   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
Table 1Go presents the selected baseline characteristics of study participants. The characteristics of women in the control and intervention groups were similar. No significant differences were found in BMD between groups at baseline.


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  		TABLE 1. Baseline characteristics of 373 WHLP participants

 
Changes in body weight are displayed in Fig. 2Go. Women in the intervention group lost 3.1 kg body weight at the 18-month follow-up and on average were 3.3 kg lighter than the control group. However, the difference in weight change between the groups attenuated over time. Compared with the control group, the intervention group experienced an average of 2.8 kg (68.8 vs. 66.0 kg) lower body weight at 54 months (the end of study) and of 2.0 kg (69.6 vs. 67.6 kg) lower body weight at the 78-month postintervention period visits. Overall, women in the intervention group lost 0.4 kg, and women in the control group gained 2.6 kg during the intervention (54 months). At the end of the two poststudy visits (month 78), intervention and control women had gained 1.2 and 3.4 kg, respectively, over 78 months.


Figure 2
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  		FIG. 2. Weight change in intervention (n = 198) and control groups (n = 175).

 
Table 2Go shows the between-group difference in the annual percent changes in five regional BMDs from baseline to the 78-month follow-up. During the intervention period (up to 54 months), the intervention group lost significantly more BMD than the control group at the total hip and femoral neck but not at the spine or whole body after controlling for age and baseline BMD. These differences were maintained over the intervention period. After additional adjustment of the interim weight change, the observed differences between the groups disappeared.


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  		TABLE 2. Baseline BMD and annualized BMD changes for intervention (n = 198) and control (n = 175) groups

 
At the 78-month follow-up, 34.8% (130 women) of the participants were still menstruating regularly. Of the 243 postmenopausal women, 65.4% were on HT.

Table 3Go shows annualized BMD changes by the weight change categories after combining control and intervention groups together. Annualized changes at total hip and femoral neck decreased significantly from the weight loss to the weight gain group for all participants and also for subgroups stratified by menopause/HT use. The annualized rate of change over the 78 months of follow-up was smallest in women who were still premenopausal at the 78-month visit. However, premenopausal women in the weight loss group lost BMD, whereas premenopausal women in the weight gain group gained BMD. The annualized rate of BMD loss was greater among the postmenopausal women not on HT compared with the postmenopausal women on HT. The average duration of HT use in these women was 2.2 ± 1.7 yr. Nevertheless, weight loss in each group was associated with greater BMD loss at the hip. Change in lumbar spine BMD was not significantly associated with weight change. Duration of HT was not related to change in BMD.


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  		TABLE 3. Annualized BMD changes (percent per year) by weight change category and 78-month menopausal status

 
In multivariate models, annual relative weight changes over the follow-up period were significantly associated with the changes in BMD at total hip and femur neck even after controlling for baseline age, baseline weight, baseline regional bone density, participating in the intervention, smoking, and sports activity change. With each percent decrease in percent weight change from baseline, annual BMD would decrease 0.034 and 0.042% at total hip and femur neck, respectively (Table 4Go). Weight change was not significantly related to changes in BMD at the spine or whole body. There was no significant interaction effect between weight change and menopause/HT use for the prediction of the changes in BMD at any region (all P values > 0.05).


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  		TABLE 4. Regression coefficients of percent weight change and menopausal hormone use status on annual regional BMD changes (percent) over 78-month period

 

   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
To our knowledge, this is the first study to examine the effect of a lifestyle intervention on BMD change across menopause. Unlike previous intervention studies focused on obese women, the average BMI in women in our study was in the normal range. Finally, most previous weight loss interventions were short-term, less than 1 yr (19, 20, 21, 22). Our intervention was over 54 months with extended follow-up postintervention for 2 yr.

The WHLP lifestyle intervention was overall successful in preventing weight gain and its associated increases in LDL cholesterol (14). At the end of the intervention (54 months), women in the intervention group gained an average of 2.8 kg less than women in the control group. However, during the intervention, women in the intervention group also experienced greater loss in BMD, especially at the total hip and femoral neck. Adjustment for weight change attenuated these differences, providing strong evidence that the differences in BMD change by intervention group were, indeed, mediated by weight change. Two years after the intervention was stopped, the weight differences between the two groups were smaller, and accordingly, differences in BMD were generally absent.

The greater loss in hip BMD among women who experienced a weight loss of 3% or more was consistent across menopausal status. The annual rate of femoral neck bone loss among postmenopausal women not on HT was 1.4% compared with 0.75% for women who gained weight. If these losses continued over 5 yr, the average loss of BMD among women who lost weight would be about 7%. This amount of bone loss is significant and has been linked to an increased risk of hip fracture (23, 24), the most devastating osteoporotic fracture. About one third of our participants were still menstruating at the final 78-month follow-up. These women were on average in their mid-50s, and it is likely that they were in the perimenopausal transition. Some studies have suggested that menopause-associated bone loss begins in the late perimenopausal period (25). Nevertheless, among menstruating women, the rate of hip bone loss was 50% slower among women who gained weight, even after adjusting for their baseline BMD and body weight. Previous studies of weight intervention in younger premenopausal women showed either a small decrease in BMD or no change (21, 26).

HT has been shown to modify the relationship between weight change and BMD change. In the Osteoporosis Risk Factor and Prevention Study (OSTPRE) cohort, weight loss predicted bone loss at femur neck and lumbar spine only in women not on HT (4). Macdonald et al. (27) reported that the effect of weight change on BMD change at the femoral neck and lumbar spine was not significant among current HT users. Nevertheless, weaker protective effects of HT were observed in our study. Bone loss was attenuated in women on HT but remained statistically significant, suggesting that use of HT may not totally protect women from weight loss-associated bone loss.

The relationship between weight change and BMD change was significant at the total hip and femoral neck but not at the spine and whole body. Most (4, 6, 11) but not all (22, 28) observational studies have shown a significant reduction in lumbar spine BMD with weight loss. Weight intervention studies in both premenopausal women (28) (mean age 38 yr) and in older postmenopausal women (22) (mean age 63 yr) have shown that lumbar spine BMD was maintained despite weight reduction. A recent comprehensive review reported that high-intensity resistance activity resulted in increasing spine but not hip BMD (29). In our study, sports activity was a significant predictor of change in lumbar spine BMD (data not shown). Thus, it’s possible that women in the intervention group increased their sports activity, and thus, despite their weight loss, they did not experience a loss in spine BMD. The lumbar spine BMD site contains a higher percentage of trabecular bone, and menopause primarily influences loss of trabecular bone. The effect of weight loss on trabecular bone may be modest in comparison with the effects of menopause.

To mitigate weight loss-associated bone loss, increasing physical activity is often recommended. The intervention group was asked to increase their weekly physical activity to 1000–1500 kcal primarily by increasing activities such as walking. However, total physical activity was not associated with changes in BMD at any site. The total physical activity primarily reflected walking activity. Thus, it’s possible that the intensity of our physical activity intervention was not sufficient to exert an independent effect on BMD or to overcome the negative effect of weight loss. Additional intervention trials should include more intensive resistance training to test whether these intensive interventions can offset the weight loss-associated bone loss.

There are a number of strengths to our study. We tested a long-term intervention in a group of generally healthy premenopausal women on BMD changes across menopause. Our retention rate was excellent. The intervention was chosen because it could be applicable to most women. BMD was measured annually using state of the art methods. We continued follow-up 2 yr after the intervention ceased. We collected information on a number of important covariates. Nevertheless, our study has several limitations. We measured weight on an annual basis and may have missed considerable fluctuations in weight especially among the intervention group. We collected information on HT at the final follow-up visit, but duration of use was for only 2 yr. Longer duration of use of HT may indeed provide protection from weight loss-induced bone loss.

In summary, a lifestyle intervention targeted to healthy premenopausal women to prevent weight gain or produce moderate weight loss was associated with significant loss in BMD at the hip. Both weight change and menopausal transition/hormone use were strong independent predictors of hip BMD change. Use of hormones may attenuate the weight change-related bone change but did not totally protect women against bone loss. Therefore, clinicians should consider the potential loss of BMD when providing lifestyle and weight loss recommendations to midlife women.


   Footnotes
 
This work was supported by the National Institutes of Health Grant HL-45167.

Disclosure Statement: J.A.C. has received research support from Merck & Co., Eli Lilly & Co., Pfizer Pharmaceuticals, and Novartis Pharmaceuticals. She has also received consulting fees from Eli Lilly & Co. and Novartis Pharmaceuticals. She is on the speaker’s bureau for Merck & Co. All other authors have nothing to disclose.

First Published Online July 17, 2007

Abbreviations: BMD, Bone mineral density; BMI, body mass index; HT, hormone therapy; LDL, low-density lipoprotein; WHLP, Women’s Healthy Lifestyle Project.

Received May 9, 2007.

Accepted July 11, 2007.


   References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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