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Obstetrics & Gynecology 2000;96:13-17
© 2000 by The American College of Obstetricians and Gynecologists
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ORIGINAL RESEARCH

Effect of Non–Weight-Bearing Body Fat on Bone Mineral Density Before and After Menopause

TSUTOMU DOUCHI, MD, SHINAKO YAMAMOTO, MD, RIKI KUWAHATA, MD, TOSHIMICHI OKI, MD, HIDEKI YAMASAKI, MD and YUKIHIRO NAGATA, MD

From the Department of Obstetrics and Gynecology, Faculty of Medicine, Kagoshima University, Kagoshima, Japan.

Address reprint requests to: Tsutomu Douchi, MD Kagoshima University, Department of Obstetrics and Gynecology, Faculty of Medicine, 8-35-1 Sakuragaoka, Kagoshima, 890-8520, Japan


   Abstract
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Abstract
Materials and Methods
 Results
 Discussion
 References
 
Objective: To investigate the difference in the effect of non–weight-bearing body fat mass on bone mineral density between premenopausal and postmenopausal women.

Methods: We studied 252 regularly menstruating pre-menopausal women and 213 postmenopausal women with right side dominance. Age, years since menopause (in post-menopausal women), height, weight, and body mass index were recorded. Bone mineral density of non–weight-bearing sites (ie, arms), weight-bearing sites (ie, lumbar spine including L2–4 and legs), and body fat mass were measured by whole-body scanning with dual-energy x-ray absorptiometry. Body fat mass was also measured by dual energy x-ray absorptiometry.

Results: Body fat mass did not differ between groups. In postmenopausal women, body fat mass correlated positively with bone mineral density of the left leg (r = .41, P < .001), right leg (r = .36, P < .001), left arm (r = .31, P < .001), and lumbar spine (r = .27, P < .001). The correlation between body fat mass and bone mineral density of the left arm remained significant after adjusting for age, years since menopause, and height. In premenopausal women, body fat mass correlated positively with bone mineral density of left leg (r = .37, P < .001) and right leg (r = 0.31, P < .001), but correlated weakly with bilateral arms (r <= .19) and lumbar spine bone mineral density (r = 0.13, P < .05).

Conclusion: The effect of non–weight-bearing body fat on bone mineral density was greater in postmenopausal than premenopausal women.

Many factors affect bone mineral density, and they operate differently at various stages of life. Some factors have a strong influence on it during certain periods of life, then have reduced effects at other times. Obese women have elevated bone mineral density,1–4 which might be attributable to the weight-bearing effect and non–weight-bearing effect of body fat mass on bone mineral density. The non–weight-bearing effects of body fat mass might include increased serum estrogen levels from aromatization of androgen in the adipose tissue. However, it remains unclear whether a difference exists in the non–weight-bearing effect of body fat mass on bone mineral density between premenopausal and postmenopausal women.

Bone mineral density of the horizontal axis, such as the arms, is not influenced by the weight-bearing effect of body fat mass but is influenced by the non–weight-bearing effect. Thus, to investigate the difference in non–weight-bearing effect of body fat mass on bone mineral density between premenopausal and post-menopausal women, we measured it at various sites of the segmental regions.


   Materials and Methods
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Abstract
 Materials and Methods
Results
 Discussion
 References
 
We studied 282 premenopausal and 252 postmenopausal Japanese women with right side dominance who had requested screening for uterine cancer, ovarian tumors, or hyperlipidemia. Subjects were recruited between July 1996 and August 1999 in the Department of Obstetrics and Gynecology, Kagoshima University Hospital. We excluded 69 subjects with chronic or acute diseases (n = 20), ovarian tumors (n = 13), uterine cancer (n = 5), prescription of oral contraceptives (OCs) (n = 5), prescription of postmenopausal hormone replacement therapy (HRT) (n = 15), excessive alcohol consumption (n = 13), cigarette smoking (n = 15), and endurance physical training (n = 17) (some subjects had multiple exclusion factors). The remaining 252 pre-menopausal and 213 postmenopausal women were enrolled. No subjects had taken medications likely to affect bone mineral density. All of the premenopausal women were menstruating regularly. All of the post-menopausal women had natural menopause. Subjects were considered to have entered menopause if they had not menstruated for at least 12 months before the investigation.

Baseline characteristics including age, years since menopause (in postmenopausal women), height, weight, and body mass index (BMI) were recorded for each subject. Body mass index was calculated as weight (kg) divided by height squared (m2). Bone mineral density of the horizontal axis (ie, arms) and vertical axis (ie, lumbar spine, including L2–4 and legs) were measured by whole-body scanning with dual-energy x-ray absorptiometry (QDR 2000/W, Hologic Inc., Waltham, MA). Body fat mass was also measured by dual-energy x-ray absorptiometry. The reproducibility of body fat mass was determined in 14 women, each of whom was measured twice at 1-week intervals; the coefficient of variation in those women was less than 2.0%. All recordings were made by the same experienced examiner, who was masked to the study status.

Default software readings divided body measurements into areas corresponding to arms, trunk, and legs. The trunk region was delineated by an upper horizontal border below the chin, vertical borders lateral to the ribs, and a lower border formed by oblique lines through the hip joints. The leg region was defined as tissue below the oblique lines passing through the hip joints. Institutionally approved informed consent was obtained from all subjects, and this study was conducted in accordance with the Helsinki Declaration.

Intergroup comparisons were made using Student t test. All variables were distributed normally, so correlation between variables and regional bone mineral density was assessed by calculating Pearson’s correlation coefficient. On multiple regression analysis, the dependent variable was regional bone mineral density, and independent variables were body fat mass, age, years since menopause, and height. Weight, BMI, and percentage of body fat were excluded from multiple regression analysis because they are similar to body fat mass as an indicator of overall adiposity. On multiple regression analysis, the strength of correlation was shown using standardized regression coefficient, which is a variable similar to Pearson’s correlation coefficient. P < .05 was considered statistically significant.


   Results
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Abstract
 Materials and Methods
 Results
Discussion
 References
 
Table 1Go shows baseline characteristics and bone mineral density. Although regional densities were significantly lower in postmenopausal than in premenopausal women, body fat mass did not differ between groups.


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  		Table 1. Baseline Characteristics
 
Table 2Go shows the correlation coefficients of body fat mass with bone mineral density. In premenopausal women, body fat mass correlated positively with density of the left leg (r = .37, P < .001) and right leg (r = 0.31, P < .001) but correlated weakly with bilateral arms (r <= .19) and lumbar spine density (r = 0.13, P < .05). In postmenopausal women, body fat mass correlated positively with density of the left leg (r = .41, P < .001), right leg (r = .36, P < .001), left arm (r = .31, P < .001), and lumbar spine (r = .27, P < .001) but correlated weakly with the right arm density (r = .18, P < .01).


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  		Table 2. Correlation of Body Fat Mass With Bone Mineral Density
 
Table 3Go shows the relationship between body fat mass and density on multiple regression analysis. In pre-menopausal women, body fat mass was significantly correlated with leg density (P < .001) irrespective of age and height but weakly correlated with left arm density (P < .01). Body fat mass was not correlated with bone mineral density of right arm, lumbar spine, or total body. In postmenopausal women, body fat mass positively correlated with bone mineral density in all segmental regions, including weight-bearing and non–weight-bearing sites, irrespective of age, years since menopause, and height. In all segmental regions, standardized regression coefficients between body fat mass and density were greater in postmenopausal than pre-menopausal women.


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  		Table 3. Body Fat Mass Related to Bone Mineral Density After Adjustment for Age and Height by Multiple Regression Analyses
 

   Discussion
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Abstract
 Materials and Methods
 Results
 Discussion
References
 
To investigate the non–weight-bearing effect of body fat mass on bone mineral density, several studies measured density of the vertical axis including lumbar spine, femoral neck, and total body.2–6 However, density of the vertical axis is influenced by weight-bearing and non–weight-bearing effects of body fat mass. Thus, it is not always easy to differentiate non–weight-bearing from the weight-bearing effects of body fat mass on density. In the present study, we included density measurements of the arms to investigate the non–weight-bearing effects of body fat mass on bone mineral density.

In a longitudinal study, Guo et al7 found significant age-related decreases in fat-free mass and height, and increases in body fat mass, percentage of body fat, weight, and BMI. Although we also believed that body fat mass expressed as a percentage of body fat mass and BMI were significantly higher in postmenopausal women, the absolute amount of body fat and weight did not differ between premenopausal and postmenopausal women. The major reason for the discrepancies might be that our study was cross sectional. In addition, differences in body size, lifestyle, and diet between white and Asian populations might also contribute to these discrepancies. We found that body fat mass correlated better with bilateral leg density than with lumbar spine density in premenopausal and postmenopausal women. Naturally, bone mass of the lower segmental regions has more weight-bearing effects of body fat mass than the upper regions. Thus, differences in the strength of those correlations can be explained partially by the difference in weight-bearing effects of body fat mass between legs and lumbar spine.

The strength of the correlation between body fat mass and nondominant arm density was significantly greater in postmenopausal women than premenopausal women. Bone mass in the arms does not have weight-bearing effect but is influenced by the non–weight-bearing effect of body fat mass. We are interested in determining the reasons for the stronger correlation of body fat mass with nondominant arm density in post-menopausal women. One hypothesis is that in post-menopausal women aromatization of androstenedione in the adipose tissue produces estrone (E1), which is a major source of estrogen.8 Unfortunately, we did not measure serum estrogen levels of our subjects, so we can not directly address density in combination with serum estrogen levels. However, a single measurement of serum estrogen levels does not always indicate a woman’s cumulative exposure to estrogen.9 Although obese premenopausal and postmenopausal women have high aromatized estrogen levels, ovarian rather than aromatized estrogen is more dominant in circulation during menstruation. We believe that the effect of estrogen from extraglandular aromatization on bone density is masked by the greater amount of ovarian estrogen in premenopausal women, which supports the findings of Drinkwater et al,10 who found that body composition (fat and lean mass component) had no direct influence on bone density in normal premenopausal women. In some studies, for women with prolonged amenorrhea, circulating estrogen from extra-glandular aromatization was important in preventing bone mineral loss.10–12 Warren et al11 reported that the effect of amenorrhea on bone density in ballet dancers was primarily mediated by low body weight. Drinkwater et al10 also found that obesity became more important as severity of menstrual irregularities increased. The effect of aromatized estrogen on density might be evident after profound and prolonged depletion of ovarian estrogens, as in long-term amenorrhea. Our results disagree with those of Aloia et al,13 who showed that adiposity did not affect prevention of bone loss, but they did not separate postmenopausal from premenopausal women in their analysis. The non–weight-bearing effect of body fat mass on bone density might be diminished in such a mixed group of premenopausal and postmenopausal women. Upper body fat distribution is common in postmenopausal women.14–17 Serum sex hormone-binding globulin levels are lower in women with upper body fat distribution than those with lower body fat distribution.18 There is an inverse relationship between sex hormone-binding globulin and bone mineral density in postmenopausal women19,20; therefore, sex hormone-binding globulin might contribute to stronger correlation of fat mass with density in postmenopausal women. Increased insulin resistance, which is associated with abdominal fat, also might be associated with a difference in density.21–23 Normal premenopausal women are prone to fewer changes in density in response to various risk factors for bone mineral loss than postmenopausal women. Pre-menopausal women have several factors that inhibit bone mineral loss that postmenopausal women do not have, including youth, functioning ovaries, greater daily physical activity, healthier daily diet, greater muscle strength,24,25 and higher baseline bone mineral density. Thus, slender premenopausal women might have less bone mineral loss than slender postmenopausal women.

The strength of the correlation of body fat mass with dominant arm density was uniformly weak in pre-menopausal and postmenopausal women. Humans are walking, standing, and handling beings. Daily physical activity and muscle strength are naturally greater in the dominant arm. Women are prone to fewer changes in density in the dominant arm even with older age. Those two factors are also important determinants of regional bone density.24,25 Thus, the non–weight-bearing effect of body fat mass on density might be reduced relatively in the dominant arm in premenopausal and postmenopausal women.


   Footnotes
 
PII S0029-7844(00)00814-0

Received October 20, 1999. Received in revised form January 10, 2000. Accepted January 20, 2000.


   References
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Abstract
 Materials and Methods
 Results
 Discussion
 References
 
1. Dawson-Hughes B, Shipp C, Sadowski L, Dallal G. Bone density of the radius, spine, and hip in relation to percent of ideal body weight in postmenopausal women. Calcif Tissue Int 1987;40: 310–4.[Medline]

2. Ribot C, Tremollieres F, Pouilles JM, Bonneu M, Germain F, Louvet JP. Obesity and postmenopausal bone loss: The influence of obesity on vertebral density and bone turnover in postmenopausal women. Bone 1987;8:327–31.[Medline]

3. Hassager C, Christiansen C. Influence of soft tissue body composition on bone mass and metabolism. Bone 1989;10:415–9.[Medline]

4. Shiraki M, Ito H, Fujimaki H, Higuchi T. Relation between body size and bone mineral density with special reference to sex hormonees and calcium regulating hormones in elderly females. Endocrinol Jpn 1991;38:343–9.[Medline]

5. Douchi T, Yamamoto S, Nakamura S, Oki T, Maruta K, Nagata Y. Bone mineral density in postmenopausal women with endometrial cancer. Maturitas 1999;31:165–70.[Medline]

6. Goulding A, Taylor RW. Plasma leptin values in relation to bone mass and density and to dynamic biochemical markers of bone resorption and formation in postmenopausal women. Calcif Tissue Int 1998;63:456–8.[Medline]

7. Guo SS, Zeller C, Chumlea WC, Siervogel RM. Aging, body composition, and lifestyle: The Fels Longitudinal Study. Am J Clin Nutr 1999;70:405–11.[Abstract/Free Full Text]

8. Judd HL, Shamonki IM, Frumar AM, Lagasse LD. Origin of serum estradiol in postmenopausal women. Obstet Gynecol 1982;59: 680–6.[Abstract/Free Full Text]

9. Zhang Y, Kiel DP, Kreger BE, Cupples LA, Ellison RC, Dorgan JF, et al. Bone mass and the risk of breast cancer among postmenopausal women. N Engl J Med 1997;336:611–7.[Abstract/Free Full Text]

10. Drinkwater BL, Bruemner B, Chesnut CH 3d. Menstrual history as a determinant of current bone density in young athletes. JAMA 1990;263:545–8.[Abstract]

11. Warren MP, Brooks-Gunn J, Fox RP, Lancelot C, Newman D, Hamilton WG. Lack of bone accretion and amenorrhea: Evidence for a relative osteopenia in weight-bearing bones. J Clin Endocrinol Metab 1991;72:847–53.[Abstract]

12. Biller BMK, Baum HBA, Rosenthal DI, Saxe VC, Charpie PM, Klibanski A. Progressive trabecular osteopenia in women with hyperprolactinemic amenorrhea. J Clin Endocrinol Metab 1992;75: 692–7.[Abstract]

13. Aloia JF, McGowan DM, Vaswani AN, Ross P, Cohn SH. Relationship of menopause to skeletal and muscle mass. Am J Clin Nutr 1991;53:1378–83.[Abstract/Free Full Text]

14. Trémollieres FA, Pouilles JM, Ribot CA. Relative influence of age and menopause on total and regional body composition changes in postmenopausal women. Am J Obstet Gynecol 1996;175:1594–600.[Medline]

15. Ley CJ, Lees B, Stevenson JC. Sex- and menopause-associated changes in body-fat distribution. Am J Clin Nutr 1992;55:950–4.[Abstract/Free Full Text]

16. Panotopoulos G, Ruiz JC, Raison J, Guy-Grand B, Basdevant A. Menopause, fat and lean distribution in obese women. Maturitas 1996;25:11–9.[Medline]

17. Ijuin H, Douchi T, Oki T, Maruta K, Nagata Y. The contribution of menopause to changes in body-fat distribution. J Obstet Gynaecol Res 1999;25:367–72.[Medline]

18. Kirschner MA, Samojlik E, Drejka E, Szmal E, Schneider G, Ertel N. Androgen-estrogen metabolism in women with upper body versus lower body obesity. J Clin Endocrinol Metab 1990;70:473–9.[Abstract]

19. Gillberg P, Johansson AG, Ljunghall S. Decreased estradiol levels and free androgen index and elevated sex hormone-binding globulin levels in male idiopathic osteoporosis. Calcif Tissue Int 1999;64:209–13.[Medline]

20. Center JR, Nguyen TV, Sambrook PN, Eisman JA. Hormonal and biochemical parameters in the determination of osteoporosis in elderly men. J Clin Endocrinol Metab 1999;84:3626–35.[Abstract/Free Full Text]

21. Kim JG, Shin CS, Choi YM, Moon SY, Kim SY, Lee JY. The relationship among circulating insulin-like growth factor components, biochemical markers of bone turnover and bone mineral density in postmenopausal women under the age of 60. Clin Endocrinol (Oxf) 1999;51:301–7.[Medline]

22. Mora S, Pitukcheewanont P, Nelson JC, Gilsanz V. Serum levels of insulin-like growth factor I and the density, volume, and cross-sectional area of cortical bone in children. J Clin Endocrinol Metab 1999;84:2780–3.[Abstract/Free Full Text]

23. Vestergaard P, Hermann AP, Orskov H, Mosekilde L. Effect of sex hormone replacement on the insulin-like growth factor system and bone mineral: A cross-sectional and longitudinal study in 595 perimenopausal women participating in the Danish Osteoporosis Prevention Study. J Clin Endocrinol Metab 1999;84:2286–90.[Abstract/Free Full Text]

24. Douchi T, Kosha S, Kan R, Nakamura S, Oki T, Nagata Y. Predictors of bone mineral loss in patients with ovarian cancer treated with anticancer agents. Obstet Gynecol 1997;90:12–5.[Abstract]

25. Douchi T, Yamamoto S, Nakamura S, Oki T, Maruta K, Nakae M, et al. Lean mass as a significant determinant of regional and total body bone mineral density in premenopausal women. J Bone Miner Metab 1998;16:17–20.




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