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Depressive Symptoms and Changes in Body Weight Exert Independent and Site-Specific
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Effects on Bone in Post-Menopausal Women Exercising For One Year
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Laura A. Milliken1, Ph.D. (Corresponding Author and Reprints); Jennifer Wilhelmy2, M.S.;
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Catherine J. Martin2, M.A.; Nuris Finkenthal2, M.S.; Ellen Cussler2, M.S.; Lauve Metcalfe2,
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M.S.; Terri Antoniotti Guido2, P.T.; Scott B. Going3, Ph.D.; and Timothy G. Lohman2, Ph.D.
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Morrissey Blvd., Boston, MA 02125 Phone: 617-287-7483 Fax: 617-287-7504 Email:
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laurie.milliken@umb.edu
Department of Exercise and Health Sciences, University of Massachusetts Boston, 100
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Department of Physiology, University of Arizona, Tucson, AZ, 85721
Department of Nutritional Sciences, University of Arizona, Tucson, AZ, 85721
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Word Count: 2509 words in text; 4225 words in all sections; 3 Tables & 5 Figures
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Running Head: Depressive Symptoms, Body Weight & Bone
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1
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Abstract
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Background: Lower bone mineral density (BMD) has been documented in clinically depressed
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populations and depression is the second most common chronic medical condition in general
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medical practice. Therefore, the purpose of this study was to determine whether depressive
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symptoms, vitality, and body weight changes were related to one-year BMD changes after
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accounting for covariates.
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Methods: Healthy postmenopausal women (n = 320; 40-65 years) were recruited and 266
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women completed the study. Participants were 3-10 years postmenopausal, sedentary, and either
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taking HRT (1-3.9 years) or not taking HRT (at least 1 year). Exclusion criteria were: smoking,
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history of fractures, low BMD, body mass index >32.9 or <19.0, or bone altering medications.
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Regional BMD was measured from dual-energy x-ray absorptiometry at baseline and one year.
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Self-reported depressive symptoms and vitality were measured using standard questionnaires.
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Results: Both the vitality and depressive symptoms scores were related to BMD changes at the
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femur but not at the greater trochanter or spine. Weight change was a predictor of BMD changes
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in the trochanter and spine but not the femoral neck. Weight change and vitality / depressive
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symptoms had differential and site specific effects on BMD changes at the hip. Vitality and
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depressive symptoms related to femoral neck changes and weight change related to greater
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trochanter changes.
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Conclusions: The negative impact of depressive symptoms on BMD in this population of
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postmenopausal women was independent of body weight or other behavioral factors such as
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calcium compliance or exercise.
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2
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Introduction
The loss of bone mineral density (BMD) with aging is a result of the complex
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interactions of hormonal, environmental, nutritional and genetic factors. In recent years,
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psychological status has been identified as another factor possibly related to the loss of BMD
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(1,2). In clinically depressed populations, significantly lower BMD has been found compared to
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non-depressed controls (3-7). Lower BMD in depressed populations could be related to
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depression itself or to other behavioral disturbances that occur as a result of depression. Factors
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sometimes associated with depression such as lower levels of physical activity, changes in body
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weight, lower calcium compliance, or anti-depressant medications have been postulated as
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underlying causes of bone loss (8). It is also possible that the depressed state alters the metabolic
55
hormonal milieu resulting in bone mineral loss (9).
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The difference in BMD between depressed and non-depressed populations has been
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documented in both medicated and non-medicated individuals, in males and females, and in
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those who were clinically depressed as well as in those with undiagnosed but severe depressive
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episodes (3-7). Despite these findings, there have been no large prospective trials examining
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bone loss and depressive symptoms. Additionally, no studies have focused on depressive
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symptoms measured in an apparently healthy population nor have studies accounted for the
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potential behavioral factors (changes in body weight or low calcium compliance) that are likely
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to also contribute to bone loss. The clinical relevance is unambiguous considering that
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depression is the second most common chronic condition encountered in general medical
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practice (10). Therefore, the purpose of this study was to determine whether depressive
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symptoms, indicators of well being, and changes in body weight were significantly related to
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one-year BMD changes after accounting for behavioral factors (e.g. calcium compliance,
3
68
exercise and use of hormone replacement) and other related factors (baseline BMD, age). In
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addition, in a subset of women who were exercising, we sought to determine whether depressive
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symptoms were associated with bone changes after accounting for body weight change, exercise
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compliance and the cumulative amount of weight lifted over one year of training, as well as other
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important covariates.
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Methods
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Three hundred and twenty postmenopausal women aged 40-65 years were recruited and
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266 women completed the one-year study. Women were 3-10 years past menopause (natural or
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surgical), participated in less than 120 minutes of exercise per week, and were willing to be
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randomized to an exercise or control group. Exclusion criteria included: smokers, those with a
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history of fractures, low BMD (Z score of –3.0 or less), body mass index (kg/m2) >32.9 or <19.0,
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or those taking any bone altering medication (except HRT). At the study’s start, subjects were
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either taking HRT (for 1-3.9 years) or not taking HRT (for at least 1 year) and were randomized
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within group to either a 1-year supervised exercise training program or the control group (Figure
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1). All subjects received 800 mg of calcium citrate daily (Citrical!, Mission Pharmacal, San
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Antonio, TX) and compliance was measured through pill counts. Exercise compliance and
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weight lifted throughout one year were monitored using workout logs. All protocols were
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approved by the University of Arizona’s Institutional Review Board and informed consent was
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obtained from each participant. The main effects of exercise with and without HRT on BMD
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have been published (11). The present study is a secondary analysis of the original database.
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Two women were excluded from analyses due to noncompliance to the study protocol and their
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sizable influence on the regression results. Both women lifted 30% more than the next highest
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lifters, one by attending 50% more sessions and the other by performing up to 75% more
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repetitions on most exercises. The final sample size was 264.
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Lumbar spine, femoral neck and greater trochanter BMDs (g/cm2) were measured in
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duplicate (within 7 days) on medium speed at baseline and at one year using a Lunar DPX-L
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(version 1.3y, Lunar Radiation Corporation, Madison, WI) dual-energy x-ray absorptiometer
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(DXA). The average of the two scans was used in all analyses. Scan analysis was performed by
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one certified technician using the extended research analysis feature. DXA calibration was
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performed daily using a calibration block supplied by the manufacturer. The coefficient of
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variation for this block was 0.6%. BMD precision, expressed as a percent of mean BMD, was
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less than 2.4% for each BMD site.
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Subjects completed several questionnaires at baseline including the Medical Outcomes
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Study 36-item Short-Form Health Survey (SF-36) (12) and the 21 item Beck Depression
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Inventory (BDI) (13). Demographic information was also collected through a questionnaire.
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Body weight (kg) was measured to the nearest 0.1 kg at baseline and at one year using a digital
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scale (SECA, Model 770, Hamburg, Germany) and height was measured to the nearest 0.1cm
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with a Schorr measuring board.
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Statistical Analysis
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Multiple regression was used to determine whether one year changes in body weight and
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baseline BDI, vitality (from SF-36), or general well-being (from SF-36) could significantly
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account for variability in one year changes in femoral neck, greater trochanter, and spine BMD.
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After adjusting for covariates (baseline BMD, baseline body weight, age, exercise group
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assignment, HRT use and calcium compliance), changes in body weight plus either BDI, vitality
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or general well-being variables were added to predict the one-year changes in regional BMD.
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For the subset of women who exercised, the impact of the cumulative amount of weight lifted
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during the one-year exercise program, exercise compliance, changes in body weight along with
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BDI or vitality were tested, adjusted for the above covariates except exercise group assignment.
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All analyses were carried out using the Statistical Package for Social Sciences (SPSS, v 11.5,
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Chicago, IL).
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Results
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Subject physical characteristics for body mass index (BMI), regional BMD and baseline
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values for vitality and depressive symptoms are given in Table 1. Bone density values for our
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sample of postmenpausal women are similar to others measured using similar technology (14-
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17). Figures 2 and 3 show frequency distributions for BDI and changes in body weight. Table 2
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shows the standardized regression coefficients for the 3 models predicting one-year changes in
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each regional BMD site with the change in body weight plus either vitality or depressive
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symptoms as predictors. Both the vitality and BDI scores were significantly related to BMD
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changes at the femur but not at the greater trochanter or spine. Vitality was a positive predictor
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of femoral BMD changes over one year (p = 0.034). BDI was a negative predictor of one-year
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BMD changes at the femoral neck (p = 0.026). General well-being (from the SF-36) was not a
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significant predictor of BMD changes. The results for depressive symptoms were substantiated
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by replacing BDI in the regression model with either the probability of depression (calculated
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using the Women’s Health Initiative’s formula) or a single question about depressive symptoms
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(“Have you felt depressed or sad much of the time in the past year?”). These alternate variables
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also significantly predicted femoral neck BMD changes (p = 0.09 and 0.01, respectively).
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After accounting for the effects of baseline bone density, baseline body weight, age,
calcium compliance, HRT use and exercise group assignment, weight change was a predictor of
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1-year BMD changes in the trochanter (p< 0.01), and spine (p < 0.10) but not the femoral neck.
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Weight change after one year and vitality or BDI had differential and site specific effects on
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bone density changes at the hip, with vitality and BDI related to femoral neck changes and
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weight change related to BMD changes in the greater trochanter. When comparing the
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standardized regression coefficients (ß), we found that the magnitude of the effect for BDI (ß = -
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0.139) exceeded the effects of exercise in HRT users and non-users (ß = 0.070 and 0.101,
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respectively). At the greater trochanter, the change in body weight (ß = 0.211) was a more
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powerful predictor of BMD change than HRT use (ß = 0.085) and exercise group assignment in
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HRT users and non-users (ß = 0.131 and 0.190, respectively). Weight increases were associated
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with a greater change in trochanter BMD while weight decreases were associated with a smaller
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change in trochanter BMD. Figures 3 and 4 illustrate the result on bone in response to arbitrarily
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selected high and low values of BDI, vitality, and body weight changes.
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In the subset of women who exercised (n = 140), the effects of vitality and BDI were
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examined after accounting for age, baseline BMD, HRT use, the change in body weight, baseline
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body weight, exercise compliance, calcium compliance and the cumulative amount of weight
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lifted over one year (Table 3). Increased vitality was associated with greater BMD changes at
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the femoral neck (p = 0.065). At all other sites, neither vitality nor BDI (or alternate depression
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indices) were related to BMD changes. Changes in body weight also were not related to BMD
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changes at any BMD site. The cumulative amount of weight lifted during the one year program
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predicted BMD changes (p < 0.01) at the greater trochanter.
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Discussion
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Factors that affect the loss of BMD in postmenopausal women are numerous and include
age, exercise, HRT use, calcium intake, the loss of body weight and psychological factors. The
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link between depression and bone loss has been documented in clinically depressed populations,
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mostly based on cross-sectional studies examining either those acutely ill with a major
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depressive episode (3,7,18) or those identified as depressed using standardized diagnostic
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checklists or interviews (3-5,19,20). In each case, lower regional BMD or elevated bone
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remodeling, a precursor to bone loss, was found in the depressed versus controls. Robbins (21)
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found a significant negative association between depression and hip BMD (measured once 2
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years after the assessment of depression) in a large (n = 1566) random sample of males and
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females aged 65 – 100 years, 16% of whom were clinically depressed. In a sample of 102
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Portuguese white women selected for elevated depression, those with osteoporosis were
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significantly more depressed (BDI = 16.6) than women without osteoporosis (BDI = 13) (22). In
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the only prospective study, Schweiger (6) found greater 2-year spine BMD loss in 18 depressed
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patients (receiving medication and outpatient treatment) compared to 21 controls. In contrast to
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most studies, Amsterdam (23) and Reginster (24) did not find a BMD depression relationship.
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However, in both studies, most (24) or all (23) of the analyses may have been limited due to low
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statistical power. Unique to our longitudinal study was an association between one-year BMD
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changes and initial levels of self-reported depressive symptoms and vitality, after accounting for
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several important covariates.
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The present results, a secondary analysis of data from a previously published clinical trial
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(11), provide evidence that this link between depressive symptoms and bone loss exists in a
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population that exhibited much lower levels of depressive symptoms than those in previous
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studies (Figure 2). For example, the mean score on the BDI was 4.5 with a range of 0-27. The
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percent of individuals who scored greater than 9 on the BDI in the present study was 12.5%
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whereas 64.7% scored >9 in the Coehlo (22) study. We found that depressive symptoms were
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significantly related to BMD changes at the femoral neck and accounted for an additional 2.2%
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of variation in that site. This is consistent with Michelson (4) and Reginster (24) who reported
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that the largest differences between the BMD of the depressed and non-depressed occurred at the
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femur. Also consistent with the present study, Robbins (21) reported that depression accounted
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for an additional 2% of the variability in the total hip BMD in a regression model accounting for
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age, race, gender, alcohol use, smoking, estrogen use and body mass index. Similar to both
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Amsterdam (23) and Reginster (24), we did not find significant effects of depressive symptoms
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on the BMD loss at the lumbar spine.
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Depression is often associated with behavioral factors such as low activity levels or
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changes in body weight that could influence bone independently of other depressive
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symptomatology. While these behavioral factors contribute to bone loss in individuals who are
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depressed, depressive symptoms increase the one-year loss of BMD even after accounting for the
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influence of behavioral factors such as exercise group assignment, calcium supplement
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compliance, and changes in body weight. Hence, depression may exert its negative effect on
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bone through mechanisms that are, at least in part, unrelated to behavior. In addition, the
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influence of depressive symptoms on femoral neck BMD was larger than the exercise effect
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(Figure 4). Though one-year effects are generally small, the negative impact may become
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substantial if this depression-related loss persists long-term or if it is combined with other
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negative factors affecting BMD.
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Sub-analyses performed on the women who exercised (n = 140) showed the impact of
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depressive symptoms or vitality on BMD changes after accounting for exercise compliance and
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weight lifted, rather than simply the exercise group assignment. BMD changes at the femoral
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neck were associated with self-reported vitality (p = 0.065), but not depressive symptoms (p =
9
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0.199) (Table 3). Noteworthy was the persistence of vitality as a predictor of BMD changes
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even after accounting for the effects of HRT use, exercise program compliance, calcium
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supplement compliance, and the amount of weight lifted over the one-year program. The effect
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of low vitality on changes in BMD was not a function of poor program compliance or
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performance.
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Although the present study was not designed to reduce body weight and the average body
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weight change was negligible (0.22 kg), there was a considerable range of changes in weight (-
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13.9 to +12.2 kg) (Figure 3) and these changes in weight had moderate effects on BMD changes.
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The effect of weight change was a more important factor affecting femoral neck bone changes
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than both exercise and HRT use (Figure 5). When only the exercisers were examined (Table 3),
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the amount of weight lifted was the most important factor affecting trochanter BMD changes and
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changes in body weight were not significant.
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The phenomenon of weight loss associated bone loss has been reported consistently (25-
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31). Because of this, bone density clinical trials generally attempt to minimize weight loss
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throughout the intervention. Despite any investigators best efforts, moderate weight changes
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may occur and will confound the overall results. As covariates of bone density changes are
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identified, such as depressive symptoms or weight loss, investigators should account for their
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confounding effects when interpreting the final results of long-term exercise trials. Also,
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because weight loss and depression have differential site-specific effects, it is important for
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investigators to examine the femoral neck and greater trochanter areas rather than only “total
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hip” BMD.
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In summary, the negative impact of depressive symptoms on BMD in this population of
postmenopausal women was independent of changes in body weight and varying calcium
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compliance, and was not ameliorated by assignment to a strength-training program. Further, the
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impact of depressive symptoms (at the femoral neck) and weight change (at the greater
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trochanter) was comparable to or exceeded the impact of hormone use and exercise training.
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These results suggest that the presence of depressive symptoms may be clinically relevant with
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regard to bone health. Future bone density clinical trials should control for the change in body
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weight and for depressive symptoms when assessing the osteogenic potential of any intervention.
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Acknowledgements: Supported by the National Institute for Arthritis, and Musculoskeletal and
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Skin Diseases, National Institutes of Health (AR39559) and by Mission Pharmacal (San Antonio,
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TX). Address correspondence to: Laura A. Milliken, PhD., Department of Exercise and Health
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Sciences, University of Massachusetts Boston, 100 Morrissey Blvd., Boston, MA 02125 Email:
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laurie.milliken@umb.edu
11
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15
Table 1: Subject Physical Characteristics (n = 264).
Variable
Mean
SD
Minimum
Maximum
Age (yrs)
55.6
4.8
40.2
66.3
Baseline BMI (kg/m2)
25.6
3.8
17.9
35.5
Baseline Weight (kg)
68.3
11.5
46.1
110.7
Baseline Height (cm)
163.3
6.6
144.0
185.6
1 Year Weight Change (kg)
0.22
3.1
-13.9
12.2
1-Year Calcium Compliance (%)
91.2
14.3
4
114
Baseline Vitality Score (SF-36)
68.13
17.7
5
100
Baseline BDI
4.52
4.5
0
27
Femur Neck
0.873
0.121
0.616
1.291
Trochanter
0.745
0.110
0.490
1.194
Spine (L2-4)
1.130
0.155
0.739
1.719
Femur Neck
0.0056
0.033
-0.0960
0.0940
Trochanter
0.0063
0.028
-0.1060
0.0810
Spine (L2-4)
0.0034
0.027
-0.0730
0.0890
Baseline BMD (g/cm2)
1 Year Change in BMD
(g/cm2)
16
Table 2: Standardized regression coefficients for the prediction of BMD changes over one year for covariates plus the change
in body weight and either vitality or depressive symptoms (n = 264). Adjusted R2 is for the variables indicated plus age,
baseline BMD, and baseline body weight.
Independent
Variables
Exercise effect (for
HRT users)
Dependent Variables (one-year changes)
Femoral Neck
Trochanter
Models
Models
0.053
0.070
0.061
0.192*
Exercise effect (for
HRT non-users)
0.105‡
0.101‡
0.078
0.129
†
0.131
Calcium Compliance
-0.014
-0.031
-0.031
0.051
HRT Use
0.171*
0.162*
0.143*
5.5
5.5
Change in body weight
0.020
0.022
Vitality
0.130
R2 (for Covariates)
Beck Depression
Inventory
0.227*
-0.031
-0.028
-0.041
†
0.104‡
0.067
0.059
0.084
0.055
0.037
0.084
0.073
0.094
0.083
0.085
0.072
0.239*
0.233*
0.256*
4.3
3.8
3.8
4.7
5.4
5.4
6.4
0.011
0.212*
0.211*
0.223*
0.112‡
0.113‡
0.110‡
-0.017
“Depressed Much of
Past Year” (n = 243)
R2 (Overall)
* p < 0.01
†
p < 0.05
‡ p < 0.10
0.190*
†
-0.139
†
0.023
0.027
-0.175*
6.5
6.7
Spine
Models
6.4
-0.071
-0.058
7.6
7.6
9.3
-0.008
5.9
6.4
6.8
17
Table 3: Standardized regression coefficients for the prediction of BMD changes over one year for exercisers including the
change in body weight and either vitality or depression (n = 140). Adjusted R2 is for the variables indicated plus age, baseline
BMD, and baseline body weight.
Independent
Variables
HRT Use
Dependent Variables (one-year changes)
Femoral Neck
Trochanter
Spine
Models
Models
Models
0.112
0.122
0.108
0.106
0.179
†
0.178
Calcium Compliance
0.191‡
0.160
0.103
0.127
0.157
0.125
Exercise Compliance
-0.144
-0.136
-0.280‡
-0.291‡
-0.012
0.010
Weight Lifted
0.041
0.051
0.444*
0.464*
0.057
0.013
1.0
1.0
8.4
8.4
4.3
4.3
Change in Body Weight
0.107
0.100
0.113
0.117
0.028
0.020
Vitality
0.162‡
R2 (for Covariates)
Beck Depression
Inventory
R2 (Overall)
* p < 0.01
†
p < 0.05
‡ p < 0.10
0.010
-0.121
3.2
1.9
-0.069
0.090
8.1
†
8.8
-0.115
3.4
4.1
18
Figure 1: Participant recruitment and randomization.
19
Figure 2: Frequency distribution for the Beck Depression Inventory (n = 264).
90
80
Number of Subjects
70
60
50
40
30
20
10
0
0-1
2-3
4-5
6-7
8-9
10-11
12-13
14-15
16-17
18-19
20-21
22-23
24-25
26-27
Ranges of Scores
20
Figure 3: Frequency distribution for the one year change in body weight (n = 264)
80
70
Number of Subjects
60
50
40
30
20
10
0
>12.1
12-10.1
10-8.1
8-6.1
6-4.1
Weight Lost (kg)
4-2.1
2-0.1
0-1.9
2-3.9
4-5.9
6-7.9
8-9.9
>10
Weight Gained (kg)
21
Figure 4: Changes in BMD for high and low depression and vitality scores and exercise group status.
0.025
Femoral Neck BMD Changes (g/cm2)
0.020
0.015
0.010
Exercise Group
0.005
Beck Depression Inventory
0.000
SF-36 Vitality
-0.005
-0.010
BDI = 25
BDI = 1
Score = 5
Score = 100
No Ex Group
Ex Group
22
Figure 5: Changes in femur and trochanter BMD for the mean and 2 SDs above and below the mean for the change in weight.
0.015
BMD Changes (g/cm2)
0.010
0.005
0.000
-0.005
-0.010
Femoral Neck
Trochanter
-0.015
Weight change = +2 SD
Weight change = -2 SD
23