Elsevier

Bone

Volume 53, Issue 1, March 2013, Pages 34-41
Bone

Original Full Length Article
Associations between body composition and bone density and structure in men and women across the adult age spectrum

https://doi.org/10.1016/j.bone.2012.11.035Get rights and content

Abstract

Background/purpose

The objective of this study was to identify independent associations between body composition and bone outcomes, including cortical structure and cortical and trabecular volumetric bone mineral density (vBMD) across the adult age spectrum.

Methods

This cross-sectional study evaluated over 400 healthy adults (48% male, 44% black race), ages 21–78 years. Multivariable linear regression models evaluated associations between whole-body DXA measures of lean body mass index (LBMI) and fat mass index (FMI) and tibia peripheral quantitative CT (pQCT) measures of cortical section modulus, cortical and trabecular vBMD and muscle density (as a measure of intramuscular fat), adjusted for age, sex, and race. All associations reported below were statistically significant (p < 0.05).

Results

Older age and female sex were associated with lower LBMI and muscle strength. Black race was associated with greater LBMI but lower muscle density. Greater FMI was associated with lower muscle density. Cortical section modulus was positively associated with LBMI and muscle strength and negatively associated with FMI. Adjustment for body composition eliminated the greater section modulus observed in black participants and attenuated the lower section modulus in females. Greater LBMI was associated with lower cortical BMD and greater trabecular BMD. FMI was not associated with either BMD outcome. Greater muscle density was associated with greater trabecular and cortical BMD. Associations between body composition and bone outcomes did not vary by sex (no significant tests for interaction).

Conclusions

These data highlight age-, sex- and race-specific differences in body composition, muscle strength and muscle density, and demonstrate discrete associations with bone density and structure. These data also show that age-, sex- and race-related patterns of bone density and strength are independent of differences in body composition. Longitudinal studies are needed to examine the temporal relations between changes in bone and body composition.

Highlights

► Section modulus declines with age in women only, a finding not explained by age/sex differences in lean body mass. ► Section modulus was positively associated with lean body mass index and muscle strength and negatively associated with fat mass index. ► Adjustment for differences in body composition eliminated the greater section modulus observed in black participants. ► Greater lean body mass index was associated with lower cortical bone density and greater trabecular bone density. ► Associations between body composition and bone outcomes did not vary by sex (no significant tests for interaction).

Introduction

Body composition varies according to age, sex, and racial background, and contributes to the normal variability in bone structure and bone mineral density (BMD) among adults. Aging is associated with loss of muscle mass and quality, and age-related muscle loss is accompanied by fat gain in older adults [1]. It is well established that low body mass index (BMI) is a risk factor for osteoporosis and fracture [2]; however, studies of the independent contributions of lean mass and fat mass to bone health have yielded conflicting results. For example, an early dual energy X-ray absorptiometry (DXA) report from the Health, Aging, and Body Composition study (Health-ABC) of men and women, ages 70 to 79 years, concluded that lean mass and fat mass were both positively associated with BMD, however, the associations varied according to sex, measurement site, and the index used to adjust for bone size [3]. A subsequent Women's Health Initiative study reported that femur BMD and cross-sectional area (CSA) were greater in women with higher BMI and values scaled in proportion to lean mass but not fat or total body mass [4]. More recent studies suggested differential effects of subcutaneous versus visceral fat mass. The majority of studies employing computed tomography (CT) measures of fat distribution demonstrated that visceral adipose tissue was negatively associated with BMD and bone structure [5], [6], [7], [8].

The “functional muscle–bone unit” approach posits that bone adapts to the mechanical forces to which it is subjected in order to keep the bone strength at a constant set point [9]. A recent peripheral quantitative computed tomography (pQCT) study in men ages  65 years, enrolled in the Osteoporotic Fractures in Men Study (MrOS) demonstrated that leg power and physical activity were positively associated with bone size and estimates of bone compressive strength [10]. Muscle metabolism may also affect bone health; fatty infiltration of muscle was associated with a higher risk of fracture in Health-ABC participants, independent of BMD, muscle CSA, and muscle strength [11], [12]. These data support the concept that differences in lean mass and muscle quality between subjects of varying age, sex, race, and total fat mass play a critical role in determining epidemiologic associations between these variables and bone outcomes, including fractures.

Prior studies of the functional muscle–bone unit and the impact of adiposity on BMD and bone structure were largely limited to elderly or adolescent participants, were frequently restricted to males or females, and usually did not examine race differences. A recent study demonstrated positive associations between skeletal muscle mass and bone density and structure at multiple skeletal sites; however, the cohort was > 96% white, and the study did not include measures of adiposity [13]. To our knowledge, no prior studies examined measures of volumetric BMD, cortical structure, body composition, muscle strength, and muscle density across the age range from young adults to the elderly in a multiethnic sample.

This cross-sectional study in 500 adults, ages 21 to 78 years included DXA measures of whole body and regional lean and fat mass, tibia pQCT measures of muscle area, muscle density, trabecular and cortical volumetric BMD and cortical structure, and dynamometric measures of isometric muscle strength. The objectives were to (1) determine the effects of age, sex, and race on lean body mass, muscle strength, and muscle density; (2) determine the effects of age, sex and race on trabecular and cortical BMD, cortical section modulus (a summary measure of cortical dimensions); and (3) examine associations between body composition and bone outcomes.

Section snippets

Study setting and participants

Adults, ages 21 to 78 years, were enrolled as healthy reference participants for bone studies at the Children's Hospital of Philadelphia (CHOP) and University of Pennsylvania (UPENN) between March of 2004 and June of 2008. Participants were recruited from UPENN internal medicine clinics and the surrounding community using flyers and newspaper advertisements. Exclusion criteria included a history of chronic diseases or medications known to affect nutrition or bone health, such as a reported

Subject characteristics

The participant characteristics are summarized in Table 1 according to sex and race. Black women had significantly greater BMI and FMI, compared with all other groups. Within males and females, tibia length was significantly greater in blacks compared with non-blacks (p < 0.001), relative to height.

Muscle outcomes

Table 2 summarizes the multivariable models for DXA whole body LBMI, pQCT muscle density, and muscle strength. LBMI was lower in older participants and women, greater in blacks, and positively

Discussion

These data demonstrated distinct associations between body composition and cortical dimensions, and trabecular BMD and cortical BMD (summarized in Table 5). Greater LBMI and muscle strength were independently associated with greater section modulus, while greater FMI was associated with lower section modulus after adjustment for LBMI. Travison et al. reported a positive effect of LBMI and a negative effect of FMI on DXA-based estimates of cortical structure in the proximal femur in men [26].

Conflicts of interest

The authors have no potential conflicts of interest to disclose.

References (44)

  • T.J. Beck et al.

    Does obesity really make the femur stronger? BMD, geometry, and fracture incidence in the Women's Health Initiative-Observational Study

    J Bone Miner Res

    (Aug 2009)
  • Y. Sheu et al.

    The role of bone marrow and visceral fat on bone metabolism

    Curr Osteoporos Rep

    (2011)
  • H.S. Choi et al.

    Relationship between visceral adiposity and bone mineral density in Korean adults

    Calcif Tissue Int

    (2010)
  • M. Russell et al.

    Visceral fat is a negative predictor of bone density measures in obese adolescent girls

    J Clin Endocrinol Metab

    (2010)
  • V. Gilsanz et al.

    Reciprocal relations of subcutaneous and visceral fat to bone structure and strength

    J Clin Endocrinol Metab

    (2009)
  • J.M. Burnham et al.

    Bone density, structure, and strength in juvenile idiopathic arthritis: importance of disease severity and muscle deficits

    Arthritis Rheum

    (2008)
  • T. Lang et al.

    Computed tomographic measurements of thigh muscle cross-sectional area and attenuation coefficient predict hip fracture: the Health, Aging, and Body Composition Study

    J Bone Miner Res

    (2010)
  • A.L. Schafer et al.

    Fat infiltration of muscle, diabetes, and clinical fracture risk in older adults

    J Clin Endocrinol Metab

    (2010)
  • N.K. Lebrasseur et al.

    Skeletal muscle mass is associated with bone geometry and microstructure and serum IGFBP-2 levels in adult women and men

    J Bone Miner Res

    (2012)
  • M.B. Leonard et al.

    Effects of sex, race, and puberty on cortical bone and the functional muscle bone unit in children, adolescents, and young adults

    J Clin Endocrinol Metab

    (2010)
  • D. Liu et al.

    Tibial geometry is associated with failure load ex vivo: a MRI, pQCT and DXA study

    Osteoporos Int

    (2007)
  • J.N. Farr et al.

    Skeletal muscle fat content is inversely associated with bone strength in young girls

    J Bone Miner Res

    (2011)
  • Cited by (0)

    Funding: This work was supported by NIH grants R01DK064966 and K24DK076808, and the University of Pennsylvania Clinical Translational Research Center (UL1-RR024134). Dr. Alexander was supported by the Bertha Dagan Berman-FOCUS Medical Student Fellowship.

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